September 15, 2007, Volume 120, Issue 4 , pp.823-1094

BREAST ORIGINAL ARTICLES 823 Measuring Quality of Life in Cosmetic and Reconstructive Breast Surgery: A Systematic Review of Patient-Reported Outcomes Instruments. Andrea L. Pusic, M.D., M.H.S.; Constance M. Chen, M.D., M.P.H.; Stefan Cano, Ph.D.; Anne Klassen, Ph.D.; Colleen McCarthy, M.D.; E Dale Collins, M.D.; Peter G. Cordeiro, M.D. BREAST ORIGINAL ARTICLES: Discussion 838 Discussion. Martin Jeffery Moskovitz, M.D. BREAST ORIGINAL ARTICLES 840 Intraoperative Sensorcaine Significantly Improves Postoperative Pain Management in Outpatient Reduction Mammaplasty. Alfred T. Culliford IV, M.D.; Jason A. Spector, M.D.; Roberto L. Flores, M.D.; Otway Louie, M.D.; Mihye Choi, M.D.; Nolan S. Karp, M.D. 845 Reduction Mammaplasty: A Significant Improvement at Any Size. Jason A. Spector, M.D.; Nolan S. Karp, M.D. BREAST IDEAS AND INNOVATIONS 851 Pedicle Preservation Technique for Arterial and Venous Turbocharging of Free DIEP and Muscle-Sparing TRAM Flaps. Charles Y. Tseng, M.D.; Patrick O. Lang, B.A.; Nicole A. Cipriani, M.S.; David H. Song, M.D. EXPERIMENTAL ORIGINAL ARTICLES 855 Intrinsic Axial Vascularization of an Osteoconductive Bone Matrix by Means of an Arteriovenous Vascular Bundle. Elias Polykandriotis, M.D.; Andreas Arkudas, M.D.; Justus P. Beier, M.D.; Andreas Hess, Ph.D.; Peter Greil, Ph.D.; Thomas Papadopoulos, M.D.; Jurgen Kopp, M.D.; Alexander D. Bach, M.D.; Raymund E. Horch, M.D.; Ulrich Kneser, M.D. 869 A Novel In Vivo Model of Human Hemangioma: Xenograft of Human Hemangioma Tissue on Nude Mice. Yunman Tang, Ph.D., M.D.; Wenying Liu, Ph.D., M.D.; Song Yu, Ph.D., M.D.; Yong Wang, M.D.; Qiang Peng, M.D.; Zhongxun Xiong, M.D.; Yonggang Wang, M.D.; Ting Wei, M.D. 879 The Effect of Topical Mitomycin C on Full-Thickness Burns. Heath Tennyson, M.D.; Eric R. Helling, M.D.; Joseph Wiseman, M.D.; Edward Dick, D.V.M.; Robert C. Lyons, M.D.

RECONSTRUCTIVE HEAD AND NECK: ORIGINAL ARTICLES 887 Defects of the Nose, Lip, and Cheek: Rebuilding the Composite Defect. Frederick J. Menick, M.D. 899 Aesthetic Management of the Ear as a Donor Site. Davinder J. Singh, M.D.; Scott P. Bartlett, M.D. RECONSTRUCTIVE HEAD AND NECK: ORIGINAL ARTICLES: Discussion 909 Discussion. Charles H. Thorne, M.D. RECONSTRUCTIVE HEAD AND NECK: ORIGINAL ARTICLES 910 Incomplete Excision of Squamous Cell Carcinoma of the Skin: A Prospective Observational Study. Pee-Yau Tan, M.B.B.S.; Edmund Ek, M.B.B.S.; Shirley Su, M.B.B.S.; Francesco Giorlando, M.B.B.S.; Tam Dieu, F.R.A.C.S. 917 Botulinum Toxin in Facial Palsy: An Effective Treatment for Contralateral Hyperkinesis. Maurício de Maio, M.D.; Ricardo Ferreira Bento, M.D., Ph.D. RECONSTRUCTIVE HEAD AND NECK: ORIGINAL ARTICLES: Discussion 928 Discussion. Jean Carruthers, M.D. RECONSTRUCTIVE TRUNK: ORIGINAL ARTICLES 929 Sternotomy Wounds: Rectus Flap versus Modified Pectoral Reconstruction. Steven P. Davison, M.D., D.D.S.; Mark W. Clemens, M.D.; Deana Armstrong, M.D.; Ernest D. Newton, M.D.; William Swartz, M.D. 935 Progressive Tension Sutures in the Prevention of Postabdominoplasty Seroma: A Prospective, Randomized, Double-Blind Clinical Trial. Patricio Andrades, M.D.; Arturo Prado, M.D.; Stefan Danilla, M.D.; Claudio Guerra, M.D.; Susana Benitez, M.D.; Sergio Sepulveda, M.D.; Carlos Sciarraffia, M.D.; Vicente De Carolis, M.D. RECONSTRUCTIVE TRUNK: ORIGINAL ARTICLES: Discussion 947 Discussion. Harlan Pollock, M.D.; Todd Alan Pollock, M.D. 949 Discussion. Sumeet S. Teotia, M.D. RECONSTRUCTIVE LOWER EXTREMITY: ORIGINAL ARTICLES 952 Free Tissue Transfer to the Lower Extremity Distal to the Zone of Injury: Indications and Outcomes over a 25-Year Experience. Jason A. Spector, M.D.; Steven Levine, M.D.; Jamie P. Levine, M.D.

960 Functional Reconstruction of the Extensor Mechanism following Massive Tumor Resections from the Anterior Compartment of the Thigh. Tamir Pritsch, M.D.; Martin M. Malawer, M.D.; Chia-Chun Wu, M.D.; Malcolm H. Squires, M.S.; Jacob Bickels, M.D. HAND/PERIPHERAL NERVE ORIGINAL ARTICLES 971 Free Vascularized Tissue Transfer to Preserve Upper Extremity Amputation Levels. Alessio Baccarani, M.D.; Keith E. Follmar, M.D.; Giorgio De Santis, M.D.; Roberto Adani, M.D.; Massimo Pinelli, M.D.; Marco Innocenti, M.D.; Steffen Baumeister, M.D.; Henning von Gregory, M.D.; Günter Germann, M.D., Ph.D.; Detlev Erdmann, M.D., Ph.D., M.H.S.; L Scott Levin, M.D. 982 Changes in the Lymph Structure of the Upper Limb after Axillary Dissection: Radiographic and Anatomical Study in a Human Cadaver. Hiroo Suami, M.D., Ph.D.; Wei-Ren Pan, M.D.; G Ian Taylor, M.D. PEDIATRIC/CRANIOFACIAL ORIGINAL ARTICLES 993 True Lambdoid Craniosynostosis: Long-Term Results of Surgical and Conservative Therapy. James M. Smartt Jr, M.D.; Russell R. Reid, M.D., Ph.D.; Davinder J. Singh, M.D.; Scott P. Bartlett, M.D. 1004 The Incidence of Late Cephalohematoma following Craniofacial Surgery. Shadi Ghali, M.R.C.S.; Kevin R. Knox, M.D.; Sean Boutros, M.D.; Charles H. Thorne, M.D.; Joseph G. McCarthy, M.D. 1009 Reduction of Morbidity of the Frontofacial Monobloc Advancement in Children by the Use of Internal Distraction. Eric Arnaud, M.D.; Daniel Marchac, M.D.; Dominique Renier, M.D. 1027 Treatment Outcomes of Orthodontic Treatment, Corticotomy-Assisted Orthodontic Treatment, and Anterior Segmental Osteotomy for Bimaxillary Dentoalveolar Protrusion. Jin-Kyung Lee, D.D.S., M.S.D.; Kyu-Rim Chung, D.D.S., M.S.D., Ph.D.; Seung-Hak Baek, D.D.S., M.S.D., Ph.D. COSMETIC ORIGINAL ARTICLES 1037 Transblepharoplasty Ptosis Repair: Three-Step Technique. Clinton D. McCord, M.D.; Hisham Seify, M.D.; Mark A. Codner, M.D. Supplemental Digital Content is available in the text. 1045 Experience with Fibrin Glue in Rhytidectomy. Frank M. Kamer, M.D.; Davis B. Nguyen, M.D. COSMETIC ORIGINAL ARTICLES: Discussion 1052 Discussion. Charles H. Thorne, M.D.

COSMETIC ORIGINAL ARTICLES 1053 Chin Surgery VI: Treatment of an Unusual Deformity, the Tethered Microgenic Chin. Jason A. Spector, M.D.; Stephen M. Warren, M.D.; Barry M. Zide, M.D., D.M.D. 1060 Versatility of the Superomedial Pedicle in Managing the Massive Weight Loss Breast: The Rotation-Advancement Technique. Albert Losken, M.D.; Daniel J. Holtz, M.D. CME 57e Lip Reconstruction. Bardia A. Anvar, M.D.; Brandon C. D. Evans; Gregory R. D. Evans, M.D. SAFETY & EFFICACY REPORT 1071 Mexoryl: A Review of an Ultraviolet A Filter. Gehaan D'Souza, B.S.; Gregory R. D. Evans, M.D.; Plastic Surgery Educational Foundation Technology Assessment Committee EDITORIAL 1077 Changing Role of the Library in Plastic Surgery Education Today. Rod J. Rohrich, M.D.; Ron Hoxworth, M.D.; Daniel Sullivan, M.Div. 1079 What Is Plastic Surgery and Who Decides? Thomas R. Stevenson, M.D. REVIEW 1081 "Spitz's Nevus": Reassessment Critical, Revision Radical. Steven D. Macht, M.D. LETTERS 1083 The Sitting, Oblique, and Supine Marking Technique for Reduction Mammaplasty and Mastopexy. Tilman Stasch, M.R.C.S.(Ed.); Feliciano Ciccarelli, M.D. 1083 The Sitting, Oblique, and Supine Marking Technique for Reduction Mammaplasty and Mastopexy: Reply. Fahmy S. Fahmy, F.R.C.S.I.(Plast.) 1083 Simultaneous Endoscope-Assisted Contralateral Breast Augmentation with Implants in Patients Undergoing Postmastectomy Breast Reconstruction with Abdominal Flaps. Sara Di Lorenzo, M.D.; Adriana Cordova, Assoc. Prof. 1084 Simultaneous Endoscope-Assisted Contralateral Breast Augmentation with Implants in Patients Undergoing Postmastectomy Breast Reconstruction with Abdominal Flaps: Reply. Betul Gozel Ulusal, M.D.; Ming-Huei Cheng, M.D., M.H.A. 1085 A Case for Sending Mastectomy Scars for Routine Histopathology. Manish Sinha, M.R.C.S.Ed., Sp.R.; Saurabh Gupta, M.R.C.S., S.H.O.; Fiona J. Hogg, F.R.C.S.(Plast.)

VIEWPOINTS 1087 Durability of Nasal Reconstruction in an Adolescent with Relapsing Polychondritis Treated with Infliximab. David Bell, M.D., D.D.S.; Dowain Wright, M.D., Ph.D.; Peter D. Witt, M.D. 1088 Lateral Septal Preservation: A Technique to Improve Projection in Inferior Pedicle Reduction Mammaplasty by Preventing Lateral Displacement of the Pedicle. Adil Ceydeli, M.D., M.S.; John Louis, M.D.; Jack Yu, M.D., D.D.S., M.S.; Edmond Ritter, M.D. 1089 A Baby with Osteomyelitis after a Grade II Burn. Shinichi Asamura, M.D.; Kenji Fukunishi, M.D.; Kazuhide Matunaga, D.D.S.; Takahiro Hashimoto, M.D.; Noritaka Isogai, M.D. 1090 Reconstruction of an Achilles Tendon Defect with Vascularized Abdominal Wall Fascia. Daniel F. Haynes, M.D. 1092 Use of the Vacuum-Assisted Closure System in the Treatment of Enterocutaneous Fistulas: A Follow-Up. Detlev Erdmann, M.D., Ph.D.; Michael S. Wong, M.D.; Salvatore C. Lettieri, M.D.; L Scott Levin, M.D.; Laura A. Gunn, M.D. 1092 Comparing the Ultrasonically Activated Scalpel (Harmonic) with High- Frequency Electrocautery for Postoperative Serous Drainage in Massive Weight Loss Surgery. Alexander Stoff, M.D.; Matthias A. Reichenberger, M.D.; Dirk F. Richter, M.D. OBITUARY 1094 Dr. Ulrich T. Hinderer Meise, 1924 to 2007. Miguel Chamosa, M.D.; Ezequiel Rodriguez, M.D. ANNOUNCEMENTS 65e ASPS/PSEF SPONSORED SYMPOSIA AND WORKSHOPS. 66e INTERNATIONAL MEETINGS AND SYMPOSIA.

BREAST

Measuring Quality of Life in Cosmetic and Reconstructive Breast Surgery: A Systematic Review of Patient-Reported Outcomes Instruments

Andrea L. Pusic, M.D., M.H.S. Background: Patient-reported outcomes in cosmetic and reconstructive breast Constance M. Chen, M.D., surgery are increasingly important for clinical research endeavors. Traditional M.P.H. surgical outcomes, centered on morbidity and mortality, remain important but Stefan Cano, Ph.D. are no longer sufficient on their own. Quality of life has become a crucial Anne Klassen, Ph.D. research topic augmenting traditional concerns focused on complications and Colleen McCarthy, M.D. survival. Given this, reliable and valid patient questionnaires are essential for E. Dale Collins, M.D. aesthetic and reconstructive breast surgeons. Peter G. Cordeiro, M.D. Methods: The authors performed a systematic literature review to identify pa- New York, N.Y.; London, tient-reported outcome measures developed and validated for use in cosmetic United Kingdom; Vancouver, and reconstructive breast surgery patients. Qualifying instruments were assessed British Columbia, Canada; and for adherence to international guidelines for health outcomes instrument de- Lebanon, N.H. velopment and validation. Results: The authors identified 227 health outcomes questionnaires used in breast surgery studies. After 135 generic instruments, 65 ad hoc instruments, seven oncologic instruments, 11 education questionnaires, and two non–En- glish-language questionnaires were excluded, seven measures remained. De- tailed analysis revealed that six of the seven measures had undergone limited development and validation. Only one measure, the Breast-Related Symptoms Questionnaire, demonstrated adequate development and validation in its target population. It had, nevertheless, significant content limitations. Conclusions: Valid, reliable, and responsive instruments to measure patient- reported outcomes in cosmetic and reconstructive breast surgery are lacking. To demonstrate the benefits of aesthetic and reconstructive breast surgery, future research to rigorously develop and validate new cosmetic and reconstructive breast surgery-specific instruments is needed. (Plast. Reconstr. Surg. 120: 823, 2007.)

osmetic and reconstructive breast surgeons important, they are no longer sufficient on their strive to satisfy their patients with respect own. Comprehensive measurement of surgical to aesthetic results, body image, and qual- outcomes requires the combination of both ob- C 1 ity of life. Clinical outcomes research in cosmetic jective and subjective measures. and reconstructive breast surgery reflects this To appropriately measure the effect of surgi- effort and is increasingly focused on evaluating cally relevant outcomes, well-developed and val- patient satisfaction and quality of life. Although idated patient questionnaires are needed. Pa- traditional surgical outcomes, such as postoper- tient questionnaires that are not formally ative complications and mortality rates, remain developed or tested (ad hoc questionnaires) may pose reasonable questions, but unless they are From the Memorial Sloan-Kettering Cancer Center, Univer- psychometrically tested, we cannot be confident sity College London, University of British Columbia, and about their reliability (i.e., ability to produce con- Dartmouth-Hitchcock Medical Center. sistent and reproducible scores) or validity (i.e., Received for publication February 17, 2006; accepted May ability to measure what is intended to be mea- 12, 2006. sured). Using an ad hoc questionnaire may be Copyright ©2007 by the American Society of Plastic Surgeons likened to using a surgeon’s hand span to mea- DOI: 10.1097/01.prs.0000278162.82906.81 sure the width of a breast because a tape mea-

www.PRSJournal.com 823 Plastic and Reconstructive Surgery • September 15, 2007 sure is not available. In the twelfth century, un- Table 1. Comparison of Types of Questionnaires for der the reign of Henry I, the unpredictability of Use in Breast Surgery Studies by Their Psychometric using the wildly variable human foot as a mea- Properties suring stick led to the invention of the standard- Psychometric Properties ized 12-inch ruler.2 The science of outcomes studies demands no less. Type of In the absence of validated instruments spe- Questionnaire* Reliability Validity Responsiveness cific to cosmetic or reconstructive breast sur- Ad hoc ? ? ? Generic ϩϩϩ ϩϩ ϩ gery, many studies use generic instruments. A Surgery specific ϩϩϩ ϩϩϩ ϩϩϩ generic instrument is a broad-based question- *An ad hoc instrument is a questionnaire that has not been formally naire, such as the Short Form-36, that mea- developed or tested. While such instruments may pose reasonable sures health-related quality of life in diverse questions, they may not be reliable (i.e., produce consistent and reproducible scores) or valid (i.e., measure what is intended to be patient populations. While such instruments measured). A generic instrument is a broad-based questionnaire, may be reliable, they may not be sensitive such as the Short Form-36, that measures health-related quality of life enough to measure changes as a result of sur- in diverse patient populations. While such instruments may be reli- able, they may not be sensitive or responsive enough to measure gical intervention or to capture all aspects of changes as a result of surgical intervention or to capture all aspects outcome specific to breast surgery.3 The ap- of outcome specific to breast surgery. propriateness of an instrument designed to measure change over time is determined not only by its reliability and validity but also by its that have undergone formal development and responsiveness (i.e., sensitivity to change). To validation. The secondary objective was to sys- evaluate the efficacy of an intervention such as tematically evaluate these breast surgery– cosmetic or reconstructive breast surgery, the specific measures to determine the extent to instrument must be calibrated to detect a dif- which they meet internationally established ference after the action. Responsiveness of criteria based on guidelines set by the Scien- health status measures has thus been denoted tific Advisory Committee of the Medical Out- comes Trust for health-related outcome as one of the Holy Trinity of necessary psycho- 5 metric properties of health status instruments: measures. This appraisal will identify the best reliability, validity, and responsiveness.4 instruments currently available. It will also An operative procedure that preserves or im- guide efforts to develop new breast surgery– proves breast appearance produces changes that specific instruments that can be used in future can affect multiple spheres of function, or “do- studies. mains,” that are related to quality of life—not just body image but also physical, psychological, METHODS and sexual functioning. Instruments that are This study was reviewed and approved by the limited to just one domain, such as aesthetic institutional review boards of Memorial Sloan- appearance, may not capture the entirety of the Kettering Cancer Center, in New York City, and changes that occur after breast surgery. For ex- the University of British Columbia, in Vancou- ample, an instrument designed to detect a dif- ver, Canada. ference in aesthetic outcome will not be able to The topic “quality of life following cosmetic or measure change in a patient’s sense of sexual reconstructive breast surgery” was explored to de- desirability or femininity. To correctly identify termine significant issues (conceptual mapping). and measure these various dimensions, it is nec- From this, a search strategy was devised using the essary to develop a surgery-specific instrument following key terms: mammaplasty, surgery, plas- that considers multiple domains. tic, breast, cosmetic techniques, breast reconstruc- The use of reliable, valid, and responsive tion, breast surgery, aesthetic surgery, question- patient questionnaires is essential to provide naires, quality of life, and patient satisfaction. information about the impact and effective- Using the above-identified key terms, an elec- ness of breast surgery (Table 1). Ad hoc out- tronic bibliographic search was conducted to find come tools may be inadequate as they lack relevant instruments from 1966 to the present. proven reliability and validity. Generic mea- Comprehensive searches were performed in the sures may be insufficient because they may not following databases: MEDLINE, PreMEDLINE, be responsive to surgical change. Thus, the Ebase (Excerpta Medica), CINAHL (nursing da- primary objective of this study was to identify tabase), HAPI (Health and Psychosocial Instru- existing breast surgery–specific instruments ments), Science Citation Index/Social Sciences

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Citation Index, Ovid Evidence Based Medicine pletes the instrument development. In stage III, databases, and PsychINFO (psychological ab- psychometric evaluation or validation of the mea- stracts). Limits were placed on each search to ex- sure is performed; the instrument, in its final clude non-English citations and studies on child form, is administered to large populations of pa- subjects. All instruments included in the review tients to determine questionnaire acceptability, were identified as patient-reported outcome ques- internal consistency reliability, item total correla- tionnaires measuring quality of life and/or satis- tions, test-retest reliability, validity within scale, faction after cosmetic or reconstructive breast validity in comparison with other measures, and surgery that had undergone development and val- responsiveness.6 Using these guidelines, we re- idation in a cosmetic or reconstructive breast sur- viewed the development and validation criteria gery population. used to create each questionnaire. We also sum- To find relevant articles not detected in the marized the content domains covered by each electronic bibliographic search, a follow-up review questionnaire. of references was performed. After examining ti- tles and abstracts, we examined reference lists, RESULTS tables, and texts in the pertinent articles to find all Our systematic review of the English-lan- patient-reported outcome questionnaires evaluat- guage literature revealed a limited number of ing satisfaction and/or quality of life after cos- patient-reported outcome questionnaires that metic and reconstructive breast surgery. All in- had been formally developed and validated in a struments cited in the articles were assessed for cosmetic or reconstructive breast surgery pop- evidence regarding their development and vali- ulation. Intellectual mapping and serial elec- dation criteria. Instruments without evidence of tronic bibliographic searches identified 160 ar- any development or validation process (i.e., ad ticles. After we followed up on references, 64 hoc instruments) were excluded. If an article additional articles were noted. From these contained no information regarding instrument sources, 219 instruments were identified. A development or validation, the corresponding manual search of archival documents in the author was contacted and queried. For question- American Society of Plastic Surgery library re- naires not cited in the academic literature, archi- vealed four more instruments, for a total of 227 val documents were sought. instruments. Inclusion/exclusion criteria were Questionnaires were appraised for adher- applied, and 220 measures were eliminated (Fig. ence to international guidelines for the devel- 1). Eliminated measures included two non–En- opment and validation of health outcomes mea- 7–9 6 glish-language questionnaires, seven oncologic sures. Cano et al. have described a rigorous, breast cancer questionnaires,10–27 11 breast educa- three-stage system for health outcomes instru- tion and knowledge questionnaires,28–34 65 ad hoc ment development based on guidelines set by instruments that had not undergone develop- the Scientific Advisory Committee of the Med- 11,32,35–97 5,6 ment and/or validation, and 135 generic ical Outcomes Trust. This approach includes instruments.7,8,10–12,15,16,19,21,23,24,27,32,35,36,44,91,94,95,98–228 step-by-step procedures for item generation, Thus, we identified a total of seven patient-reported item reduction, and psychometric evaluation. instruments measuring satisfaction and/or breast- Stage I defines the conceptual model to be mea- related quality of life that had undergone develop- sured and generates a pool of items to ensure all ment and validation in a cosmetic or reconstructive important areas are considered for inclusion in breast surgery population (Fig. 1). These instru- the final scale. Preliminary versions of the instru- ments were subdivided into the following categories: ment are then developed from three sources: re- breast augmentation (n ϭ 4), breast reduction (n ϭ view of the literature, qualitative interviews with 1), and breast reconstruction (n ϭ 2) (Table 2). patients, and expert opinion. The item pool is Assessment of their development and validation is then pretested or piloted on a small sample of summarized in Table 3. An evaluation of their do- patients to clarify ambiguities in the wording of main categories is presented in Table 4. items, confirm appropriateness, and determine acceptability and completion time. In stage II, field-testing is performed on a larger sample of Breast Augmentation patients. Questions are eliminated according to Four instruments were developed specifi- item redundancy, endorsement frequencies, cally for breast augmentation patients by breast missing data, factor analysis, and tests of scaling implant manufacturers. Dow Corning devel- assumptions. This “item reduction” process com- oped a questionnaire that rates patient satisfac-

825 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 1. Flow diagram of search strategy.

tion, psychosocial outcomes, concerns, and ben- pha for these scales ranged from 0.83 to 0.92, efits-to-risks appraisals in women who had indicating internal consistency reliability. received bilateral breast augmentation with Dow The McGhan Medical Corporation developed Corning silicone implants.229 Derived from fo- an instrument for their Saline-Filled Mammary cus group research and previous literature, the Implant Augmentation Clinical Study that in- Dow Corning questionnaire identifies factor cludes sections measuring quality of life and “ac- scales to measure body image, self-image, and tivities and lifestyles.” The questionnaire was de- sexual/social improvements; a Cronbach’s al- veloped from previously validated measures and

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Table 2. Cosmetic and Reconstructive Breast Surgery-Specific Instruments Instruments Studies Describing Instrument Studies Using Instrument Breast augmentation Dow Corning Cash et al., 2002229 Cash et al., 2002229 McGhan McGhan, 199510 McGhan, 1995231 Breast Implant Replacement Study (BIRS) LipoMatrix, Inc. (unpublished) LipoMatrix, Inc. (unpublished) Breast Evaluation Questionnaire (BEQ) Anderson et al., 200514 Breast reduction Breast-Related Symptoms Questionnaire (BRSQ) Thoma et al., 200511 Kerrigan et al., 2001100 Kerrigan et al., 2001100 Kerrigan et al., 2002232 Kerrigan et al., 2002232 Collins et al., 2002232 Breast reconstruction Michigan Breast Reconstruction Outcomes Alderman et al., 2000149 Study—Satisfaction questionnaire (MBROS-S) Alderman et al., 200017 Krueger et al., 200118 Michigan Breast Reconstruction Outcomes Study—Body Image questionnaire (MBROS-BI) Wilkins et al., 200010 Wilkins et al., 200010

Table 3. Patient-Reported Breast Surgery Outcome Instruments: Development and Validation Criteria Breast Surgery–Specific Questionnaires

Augmentation Reduction Reconstruction

Method/Evaluation Dow Corning McGhan BIRS BEQ BRSQ MBROS-S MBROS-BI Item generation Patient interviews ●● Literature ●●●●●●● Expert opinion ●●●●●●● Develop conceptual model ●● ●●● Item reduction Expert opinion ●● ● ● ● Item redundancy ● Endorsement frequencies ● Missing data ● Factor analysis ●●●●● Tests of scaling assumptions ● Psychometric analyses Acceptability ●● ● ● ● Internal consistency reliability ●●●● Item total correlations ●● Interrater reliability ●● Test-retest reliability ●● Validity within scale ● Validity comparison with other measures ●● Validity hypothesis testing ● Responsiveness ● BIRS, Breast Implant Replacement Study; BEQ, Breast Evaluation Questionnaire; BRSQ, Breast-Related Symptoms Questionnaire; MBROS-S, Michigan Breast Reconstruction Outcomes Study–Satisfaction; MBROS-BI, Michigan Breast Reconstruction Outcomes Study–Body Image. has a clearly stated conceptual model.230 No fur- breast augmentation patients.230 There was no evi- ther data are available on the psychometric prop- dence of formal conceptual mapping or consider- erties of the instrument. ation of multiple domains. In addition, patient in- LipoMatrix, Inc., also developed a question- terviews were not part of the development process. naire for their Breast Implant Replacement Study Validated by academic researchers on 1244 women to evaluate the use of Trilucent breast implants. seeking augmentation mammaplasty, factor analysis Questions were taken from previously validated was performed. Discriminant validity was demon- measures. No further data are available on the strated against the Tennessee Self-Concept Scale psychometric properties of the instrument. and the Multidimensional Body Self-Relations Ques- Finally, Mentor developed the Breast Evalua- tionnaire. Psychometric tests showed evidence of ad- tion Questionnaire, which was designed to assess equate internal consistency and test-retest reliability patient satisfaction with aesthetic outcomes among (Cronbach’s alpha Ͼ0.70).

827 Plastic and Reconstructive Surgery • September 15, 2007

Table 4. Patient-Reported Breast Surgery Outcomes Instruments: Domain Analysis Breast Surgery–Specific Questionnaires

Augmentation Reduction Reconstruction

Method/Evaluation Dow Corning McGhan BIRS BEQ BRSQ MBROS-S MBROS-BI Health-related quality of life Social support from family and friends ●● ● Concerns about treatment ●●● Concerns about general health ●● Concerns about cancer recurrence ●● Satisfaction with treatment ●●● ● Difficulty finding clothes that fit ●●● Satisfaction with quality of life ● Inconvenience of medical visits/hospital Concerns about postoperative complications ●●● Career issues ● Body image Concerns about scarring ●● Breast size/shape/firmness ●●●●●● Appearance in clothes ●●●● Appearance in bathing suit ●● ● Appearance naked ●●●● Self-consciousness around others ●●●● Physical attractiveness ●●● ● Satisfaction with body ●●● ● Ability to look at self ● Prosthesis issues Hair loss/thinning Weight changes ● Psychological functioning Self-confidence and self-esteem ●● ● Personal relationships ●● Ability to enjoy life ●● Negative feelings about self ●● Negative feelings about others ● Avoidance of uncomfortable situations ● Feelings of femininity ●● Satisfaction with employment Coping skills ●● Feelings of distress and worry ●● Physical functioning Limitations of physical activity ●● ● Ability to work ● Ability to go out or travel ● Pain issues ●●● ● Feeling ill or unwell ●● Breast-related skin problems ● Swelling ● Sensory changes ●●● ● Decreased energy ● Insomnia ● Memory/concentration issues ● Chemotherapy side effects Sexual functioning Changes in sexual activity ●● Self-consciousness during sexual activity ●● ● Feeling desirable/sexually active ●●● Satisfaction with sex life ●●● Interested in sex Importance of breasts for sexuality ●●● Vaginal dryness/painful intercourse BIRS, Breast Implant Replacement Study; BEQ, Breast Evaluation Questionnaire; BRSQ, Breast-Related Symptoms Questionnaire; MBROS-S, Michigan Breast Reconstruction Outcomes Study–Satisfaction; MBROS-BI, Michigan Breast Reconstruction Outcomes Study–Body Image.

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Breast Reduction naires. Only seven instruments, however, had The Breast-Related Symptoms Questionnaire undergone any degree of development and val- is the only instrument that was uniquely designed idation. Upon more rigorous examination, six to evaluate breast reduction outcomes.231 It mea- of the seven instruments identified for use in sures breast symptoms only and does not assess cosmetic or reconstructive breast surgery pa- other aspects of quality of life after breast surgery tients were not appropriately developed or val- (e.g., psychosocial or sexual functioning). A 13- idated according to the criteria of the Medical item scale developed by an expert panel and pa- Outcomes Trust and cannot be recommended tient focus groups, the questionnaire contains without reservations. All four of the breast aug- questions about breast-related symptoms and co- mentation surgery instruments were developed morbidities, producing two scores. The first, the by private industry, with limited information breast symptom summary score, is obtained by published about their development and valida- calculating the mean of all 13 items. The second, tion processes. With regard to reconstructive a physical symptom count, is computed from seven breast surgery, the two Michigan Breast Recon- items of the 13-item scale. Specifically designed for struction Outcomes Study questionnaires use in a breast reduction study entitled Breast showed evidence of validation, but the instru- Reduction: Assessment of Value and Outcomes, ments were not developed according to ac- the Breast-Related Symptoms Questionnaire was cepted standards. Both questionnaires lacked one of five measures included in the survey. Factor patient input and formal item reduction.100 Only analysis and test-retest reliability were evaluated as the Breast-Related Symptoms Questionnaire, part of a pilot study. The questionnaire recently which is specific to breast reduction surgery, underwent further validation, and data analysis showed evidence of adequate development and that confirmed its face and predictive validity.145 validation. Nevertheless, it had significant con- tent limitations. It measured breast reduction symptoms but failed to address other domains, Breast Reconstruction such as aesthetics and body image. Two measures were identified that assess qual- Patient interviews are a particularly important ity of life after breast reconstruction surgery. component of instrument development. Irrespec- These measures originated from the Michigan tive of this, most of the questionnaires reviewed in Breast Reconstruction Outcomes Study. The this article were developed largely without patient study’s Satisfaction questionnaire was generated input. The Breast-Related Symptoms Question- by an expert panel and is composed of seven items. naire was the only cosmetic and reconstructive Formal item reduction was not performed, but breast surgery–specific instrument that reported factor analysis was used to group the seven items any patient involvement at all. In-depth qualitative into two scales measuring general satisfaction (five 100 interviews are critical to item generation, as they items) and aesthetic satisfaction (two items). produce questions that are relevant and important The study’s Body Image questionnaire is a condi- to patients. Expert opinion and literature review tion-specific, nine-item, single-construct scale de- alone cannot be expected to uncover all issues that signed to evaluate patient perceptions of physical 232 patients consider significant. Without adequate appearance after breast reconstruction. These patient input, those questions that matter most to questions were similarly developed by an expert patients may remain unasked. panel and were validated in the course of the It is also important that outcome measures be Michigan study. For this second questionnaire, developed and validated for a specific target pop- Cronbach’s alpha was found to be 0.89, indicating ulation. Often used to supplement ad hoc instru- good internal consistency for the single construct ments, many generic instruments identified in this of body image. review were designed to measure quality of life, body image, physical functioning, psychological DISCUSSION functioning, or sexual functioning in the general The common denominator of the instru- population. Not developed specifically among cos- ments in this review is that they address some metic or reconstructive breast surgery patients, aspect of the patient’s subjective experiences however, these generic instruments cannot be ex- with cosmetic or reconstructive breast surgery pected to possess adequate responsiveness for such and underwent a formal development and val- patients. For example, the Multidimensional Body idation process. An extensive systematic litera- Self-Relations Questionnaire is a body image instru- ture review revealed many ad hoc question- ment developed for a nonsurgical population that

829 Plastic and Reconstructive Surgery • September 15, 2007 has been used in a number of plastic surgery breast surgery studies, few have undergone any studies.32,98,100–102,115,145,168,169,178,180,181,183,184,190 With formal development or validation. With the ex- subscales focused on areas such as fat anxiety, ception of the Breast-Related Symptoms Question- dieting, and eating restraint, its questions fail to naire, the instruments examined in this review did address the body image concerns of cosmetic and not show evidence of adequate development and reconstructive breast surgery patients, such as scar- validation as described by the Medical Outcomes ring and breast size. Trust. Without proper measurement tools, study In general, condition- or surgery-specific results are considerably less meaningful. That is, if measures allow greater responsiveness to inter- a study produces results based on an instrument vention-related change when compared with ge- that cannot be shown to measure what it is in- neric measures.233 The Short Form-36, for ex- tended to measure in a consistent and reproduc- ample, was the most widely used instrument in ible fashion, then the conclusions drawn cannot cosmetic and reconstructive breast surgery stud- claim to be reliable or valid. ies. In a recent study prospectively evaluating Patient-reported outcome questionnaires the sensitivity of the Short Form among surgical should ideally undergo full development and patients, however, the author concluded that validation as outlined by the Scientific Advisory while the form can measure changes in health Committee of the Medical Outcomes Trust. Im- status as caused by disease, it was too insensitive portantly, patient interviews should be an inte- to measure the effects of surgery on improvement gral part of the item generation process. Appro- in health status.232 Another study among breast priate instruments should be specific to reduction patients found that while the Short outcomes following cosmetic and reconstructive Form-36 had a high responsiveness in the phys- breast surgery, as generic measures are unlikely ical summary score, its responsiveness in the to address surgery-specific outcomes and may mental summary score was much lower.101 Since have inadequate responsiveness to detect sur- properly developed disease-specific instru- gery-related changes over time. To take this a ments, by definition, focus on the ailment under step further, a useful instrument should be not study, they are custom-designed to measure the only breast surgery–specific but should focus on most relevant domains. Not surprisingly, the specific types of breast surgery, whether it be more closely calibrated the instrument, the breast augmentation, breast reduction, or breast more sensitive it will be to the condition in ques- reconstruction. It is important to adopt the op- tion. For example, the same breast reduction timal approach for measuring patient satisfac- study that discerned a difference in responsive- tion and quality of life in cosmetic and recon- ness between the physical and mental summary structive breast surgery patients so that new scores of the Short Form-36 found that the studies will have a meaningful basis from which Breast-Related Symptoms Questionnaire, which to compare surgical results. To adequately dem- was specifically designed to evaluate breast re- onstrate the benefits of cosmetic and recon- duction patients, was 2.5 times more responsive structive breast surgery, future research to rig- than the Michigan Breast Reconstruction Out- orously develop and validate new instruments is comes Study and physical summary score of the thus needed. Short Form-36 in sensing changes brought about by reduction mammaplasty in patients with breast Andrea Pusic, M.D., M.H.S. 101 Memorial Sloan-Kettering Cancer Center hypertrophy. Generic instruments may play a 1275 York Avenue complementary role in patient-reported out- New York, N.Y. 10021 comes studies, but they are not sensitive enough to [email protected] detect the full range of changes that occur after cosmetic and reconstructive breast surgery. DISCLOSURE CONCLUSIONS None of the authors has a financial interest in any Patient-reported instruments designed to of the products, devices, or drugs mentioned in this measure satisfaction and quality of life after cos- article. metic and reconstructive breast surgery ask pa- tients to report views, feelings, and experiences REFERENCES that are unavoidably personal phenomena. While 1. Cano, S. J., Browne, J. P., and Lamping, D. L. Patient-based many patient-reported outcome questionnaires measures of outcome in plastic surgery: Current approaches have been used in cosmetic and reconstructive and future directions. Br. J. Plast. Surg. 57: 1, 2004.

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77. Moskovitz, M. J., Muskin, E., and Baxt, S. A. Outcome study Cancer Co-operative Group (BCCG). Eur. J. Cancer 34: 307, in liposuction breast reduction. Plast. Reconstr. Surg. 114: 55, 1998. 2004. 96. Gui, G. P., Kadayaprath, G., Tan, S. M., et al. Evaluation of 78. Netscher, D. T., Sharma, S., Thornby, J., et al. Aesthetic outcome after immediate breast reconstruction: Prospec- outcome of breast implant removal in 85 consecutive pa- tive comparison of four methods. Plast. Reconstr. Surg. 115: tients. Plast. Reconstr. Surg. 100: 206, 1997. 1916, 2005. 79. Ohlsen, L., Ponten, B., and Hambert, G. Augmentation 97. Spector, J. A., Kleinerman, R., Culliford, A. T., and Karp, mammaplasty: A surgical and psychiatric evaluation of the N. S. The vertical reduction mammaplasty: A prospective results. Ann. Plast. Surg. 2: 42, 1979. analysis of patient outcomes. Plast. Reconstr. Surg. 117: 374, 80. Park, A. J., Chetty, U., and Watson, A. C. 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152. Chung, K. C., Hamill, J. B., Kim, H. M., Walters, M. R., and 170. Cash, T. F. The situational inventory of body-image dys- Wilkins, E. G. Predictors of patient satisfaction in an out- phoria: Psychometric evidence and development of a short patient plastic surgery clinic. Ann. Plast. Surg. 42: 56, 1999. form. Int. J. Eat. Disord. 32: 362, 2002. 153. Hermans, B. J., Boeckx, W. D., De Lorenzi F., and van der 171. Cash, T. F., Melnyk, S. E., and Hrabosky, J. I. The assessment Hulst, R. R. Quality of life after breast reduction. Ann. Plast. of body image investment: An extensive revision of the Surg. 55: 227, 2005. appearance schemas inventory. Int. J. Eat. Disord. 35: 305, 154. Elder, E. E., Brandberg, Y., Bjorklund, T., et al. Quality of 2004. life and patient satisfaction in breast cancer patients after 172. Cash, T. F., Santos, M. T., and Williams, E. F. 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227. Hermans, B. J., Boeckx, W. D., De Lorenzi, F., and van der Study Protocol (Unpublished archival document). Arling- Hulst, R. R. Quality of life after breast reduction. Ann. Plast. ton Heights, Ill.: ASPS Archives, 1995. Surg. 55: 227, 2005. 231. Anderson, R. C., Cunningham, B., Tafesse, E., and 228. Elder, E. E., Brandberg, Y., Bjorklund, T., et al. Quality of Lenderking, W. R. Validation of the Breast Evaluation life and patient satisfaction in breast cancer patients after Questionnaire for use with breast surgery patients. Plast. immediate breast reconstruction: A prospective study. The Reconstr. Surg. 118: 597, 2006. Breast 14: 201, 2005. 232. Kerrigan, C. L., Collins, E. D., Kim, H. M., et al. Reduction 229. Cash, T. F., Duel, L. A., and Perkins, L. L. Women’s psy- mammaplasty: Defining medical necessity. Med. Decis. Mak- chosocial outcomes of breast augmentation with silicone ing 22: 208, 2002. gel-filled implants: A 2-year prospective study. Plast. Reconstr. 233. Alderman, A. K., Wilkins, E. G., Lowery, J. C., Kim, M., Surg. 109: 2112, 2002. and Davis, J. A. Determinants of patient satisfaction in 230. McGhan Medical Corporation. McGhan Medical Corpora- postmastectomy breast reconstruction. Plast. Reconstr. tion Saline-Filled Mammary Implant Augmentation Clinical Surg. 106: 769, 2000.

Instructions for Authors: Update Registering Clinical Trials Beginning in July of 2007, PRS will require all articles reporting results of clinical trials to be registered in a public trials registry that is in conformity with the International Committee of Medical Journal Editors (ICMJE). All clinical trials, regardless of when they were completed, and secondary analyses of original clinical trials must be registered before submission of a manuscript based on the trial. Phase I trials designed to study pharmacokinetics or major toxicity are exempt. Manuscripts reporting on clinical trials (as defined above) should indicate that the trial is registered and include the registry information on a separate page, immediately following the authors’ financial disclosure information. Required registry information includes trial registry name, registration identification number, and the URL for the registry. Trials should be registered in one of the following trial registries: ● http://www.clinicaltrials.gov/ (Clinical Trials) ● http://actr.org.au (Australian Clinical Trials Registry) ● http://isrctn.org (ISRCTN Register) ● http://www.trialregister.nl/trialreg/index.asp (Netherlands Trial Register) ● http://www.umin.ac.jp/ctr (UMIN Clinical Trials Registry) More information on registering clinical trials can be found in the following article: Rohrich, R. J., and Longaker, M. T. Registering clinical trials in Plastic and Reconstructive Surgery. Plast. Reconstr. Surg. 119: 1097, 2007.

837 DISCUSSION

Measuring Quality of Life in Cosmetic and Reconstructive Breast Surgery: A Systematic Review of Patient-Reported Outcomes Instruments Martin Jeffery Moskovitz, M.D. Paramus, N.J.

r. Pusic and co-authors present a startling ity and strives to maintain scientific objectivity Dinvestigation on the use of patient-based using absolute units and reporting results that outcome studies in plastic surgery of the can be verified and duplicated, outcome studies breast. It is startling because it encompasses 40 must look beyond those parameters. Patient satis- years of plastic surgery literature, examines faction, quality of life, and similar measurements 223 separate outcomes questionnaires, and are now acknowledged to be as important as the finds that in that time only one instrument was measured quantity of life in terms of days or developed, tested, and validated according to years. In plastic surgery, these factors are even sound investigative principles. Looking at it more important and widespread, since so much another way, more than 99.5 percent of the of our specialty deals with restoring form and plastic surgery literature on patient-reported improving aesthetics, neither of which can be breast surgery could be faulty. Of course, it is measured objectively. not reasonable to think that nearly the entirety The need for subjective testing in plastic of breast-related outcome studies is incorrect, surgery is clear. This article documents 223 but it is important to understand what is wrong attempts at subjective assessment in breast sur- with the current system and what can be done gery alone. The problem, however, is that re- to fix it. searchers often assume that subjective re- “Outcome studies aim to gain a more thor- search needs no specific validation. I am guilty ough understanding of how often a treatment of this same error. In a recent outcome study works and what about it works for whom.”1 on breast surgery,2 I formulated my own ad This definition serves as a reasonable starting hoc questionnaire and tabulated its results. I point to examine just what an outcome study believe that the results were valid and the find- is, why it is important, and how we should go ings important, but I cannot defend my study’s about understanding and performing such potential lack of reliability, validity, and re- studies in the future. sponsiveness, which was so well elucidated in Outcome studies look at the end result of this article. In a subsequent research study,3 I treatment, not at the molecular or organ- saw the possible shortcomings of an ad hoc system aspects of the intervention. Traditional questionnaire and I chose to use several of the medical tests, measured in such familiar units generic instruments mentioned in this article as grams per liter or mean survival time, are (the Short Form-36 and the Multidimensional applied easily in standard medical research Body Self-Relations Questionnaire) as well as but cannot be applied as simply to outcome the Breast-Related Symptoms Questionnaire studies. Outcome studies need to be teased developed by Collins et al.4 I found, however, apart to look at the reasons behind a treat- that the difficulties in using generic instru- ment’s success and failure. Investigators look ments in plastic surgery are readily apparent as beyond the effects on a cell or organ to accu- studies proceed. Patients do not understand rately designate a successful outcome. Broader the broad questions in regard to their specific viewpoints are used to establish the definitions operation, and their particular state of health of success and failure, and these broader view- on a given day can easily undo all the improve- points introduce the concept of subjectivity ments brought by an operation well done and into medical research. While traditional med- an overall excellent outcome. This is why the ical investigation shuns any aspect of subjectiv- particular type of outcome study addressed by Pusic et al., the patient-reported outcome, is so Received for publication May 31, 2006. important in plastic surgery and all the more Copyright ©2007 by the American Society of Plastic Surgeons reason why such instruments need to function DOI: 10.1097/01.prs.0000277650.03970.fd properly.

838 www.PRSJournal.com Volume 120, Number 4 • Discussion

A plastic surgery adage states, “function over availability of such instruments would tremen- form and form over scar,” meaning that as we dously aid plastic surgeons and their patients. give a patient an improvement in function, he or Martin Jeffery Moskovitz, M.D. she will tolerate a variation from the norm in Image Plastic Surgery form, and as we give an improvement in overall 104 Route 17 N, Suite 105 form, a patient will tolerate the obligatory scar. I Paramus, N.J. believe this maxim is generally true, and it con- [email protected] tains all the subjectivity of plastic surgery rolled into a simple phrase. We are constantly striving DISCLOSURE to improve our patients’ condition, but there is The author of this discussion has no financial in- always a trade-off involved. The final outcome of terest in any of the products, devices, or drugs mentioned many operations can never be objectively mea- in this article. sured and will rely on subjective, patient- REFERENCES reported outcome instruments to help us under- 1. Owen, P. L. Measuring Treatment Progress. Deerfield Beach, Fla.: stand our successes and failures. It is imperative, Health Communications, Inc., 2003. therefore, that we have at our disposal a set of 2. Moskovitz, M. J., Muskin, E., Baxt, S. A., et al. Outcome study reliable, validated, and responsive measuring in- in liposuction breast reduction. Plast. Reconstr. Surg. 114: 55, struments. The use of these instruments is no 2004. less important than the use of standardized rul- 3. Moskovitz, M. J., Baxt, S. A., Jain, A., and Hausman, R. E. ers in our markings or scales in our operating Liposuction breast reduction: A prospective trial in African- American women. Plast. Reconstr. Surg. 119: 718, 2007. rooms. I agree with the authors that the devel- 4. Collins, E. D., Kerrigan, C. L., Kim, M., et al. The effectiveness opment of such instruments is sorely needed, of surgical and nonsurgical interventions in relieving the symp- and I believe the widespread introduction and toms of macromastia. Plast. Reconstr. Surg. 109: 1556, 2002.

Future Meetings of the American Society of Plastic Surgeons The following are the planned sites and dates for future annual meetings of the American Society of Plastic Surgeons: 2007 Baltimore, Md. October 26 to 31 2008 Chicago, Ill. October 31 to November 4 2009 Seattle, Wash. October 23 to 28 2010 Toronto, Canada October 1 to 6 2011 Denver, Colo. September 23 to 28 2012 Washington, D.C. November 1 to 7

839 BREAST

Intraoperative Sensorcaine Significantly Improves Postoperative Pain Management in Outpatient Reduction Mammaplasty

Alfred T. Culliford, IV, M.D. Background: Breast reduction is one of the most frequently performed plastic Jason A. Spector, M.D. surgical procedures in the United States; more than 160,500 patients underwent Roberto L. Flores, M.D. the procedure in 2005. Many outpatient reduction mammaplasty patients report Otway Louie, M.D. the greatest postoperative discomfort in the first 48 hours. The authors’ inves- Mihye Choi, M.D. tigated the effect of intraoperative topical application of the long-acting local Nolan S. Karp, M.D. anesthetic agent bupivacaine (Sensorcaine or Marcaine) on postoperative pain, New York, N.Y. time to postanesthesia care unit discharge, and postoperative use of narcotic medication. Methods: In a prospective, randomized, single-blind trial, intraoperative use of Sensorcaine versus placebo (normal saline) was compared. Postoperative pain was quantified using the visual analogue scale, and time to discharge from the postanesthesia care unit was recorded. Patients documented their outpatient pain medication usage. Results: Of the 37 patients enrolled in the study, 20 were treated with intra- operative topical Sensorcaine and 17 received placebo. Patients treated with Sensorcaine were discharged home significantly faster (2.9 hours versus 3.8 hours, p ϭ 0.002). The control arm consistently had higher pain scores in the postanesthesia care unit (although not statistically significant) than the Sens- orcaine group using the visual analogue scale system. Furthermore, patients receiving Sensorcaine required significantly less narcotic medication while re- covering at home (mean, 3.5 tablets of Vicodin) than the control group (mean, 6.4 tablets; p ϭ 0.001).There were no complications resulting from Sensorcaine usage. Conclusions: This prospective, randomized, single-blind study demonstrates that a single dose of intraoperative Sensorcaine provides a safe, inexpensive, and efficacious way to significantly shorten the length of postanesthesia care unit stay and significantly decrease postoperative opioid analgesic use in patients un- dergoing ambulatory reduction mammaplasty. (Plast. Reconstr. Surg. 120: 840, 2007.)

reast reduction is one of the most fre- other surgical procedures, there has been a par- quently performed plastic surgical proce- adigm shift toward outpatient surgery. At dures in the United States, with 160,531 present, many of the patients who undergo out- B 1 women undergoing the procedure in 2005. The patient reduction mammaplasty report that the medial pedicle breast reduction has been per- greatest period of postoperative discomfort is formed more frequently in recent years. As with the first 48 hours. The goal of our study is to provide a safe, inexpensive method (Ͻ$10 per From the Division of Plastic, Reconstructive, and Hand patient) to patients that has the potential to Surgery, Staten Island University Hospital; Division of Plas- tic Surgery, Weill Cornell College of Medicine; and Institute decrease the amount of narcotic used during the of Reconstructive Plastic Surgery, New York University postoperative period and to allow patients to be School of Medicine. discharged from the recovery room to home Received for publication April 4, 2006; accepted June 21, faster. Anticipated benefits include minimizing 2006. the well-known side effects of opioid usage (e.g., Copyright ©2007 by the American Society of Plastic Surgeons nausea, constipation, confusion) through lower- DOI: 10.1097/01.prs.0000277647.42662.29 ing the postoperative requirements. Furthermore,

840 www.PRSJournal.com Volume 120, Number 4 • Intraoperative Sensorcaine discharge from the hospital earlier has the poten- staff and patients were not aware of which arm the tial to provide the patient with significant cost sav- patient was randomized to. After 10 minutes, and ings. before placement of final postoperative dressing, the indwelling fluid was removed by suction. PATIENTS AND METHODS Patient postoperative pain in the postanesthe- All patients undergoing vertical reduction sia care unit was quantified by the recovery room mammaplasty were eligible for this study.2 Ap- nursing staff on arrival and then on an hourly basis proval was obtained for the study from the Office until discharge using the visual analogue scale.9–13 of Institutional Board of Research Associates at the Total time spent in the recovery room was re- New York University School of Medicine. After an corded. Patients were discharged directly to home informed discussion of the risks, benefits, alter- from the recovery room. In addition, anesthesia natives, and options, participating patients were records for all patients were collected. At home, randomized to either placebo (10 cc of 0.9% ster- patients recorded (on a standard data sheet) when ile normal saline applied to each breast) or Sen- and how much pain medication was consumed. All sorcaine (AstraZeneca LP, Wilmington, Del.) (10 cc patients in this study were prescribed Vicodin of 0.25% applied to each breast). The study was (acetaminophen and hydrocodone; Abbott Lab- single-blind because the surgeons knew whether oratories, Abbott Park, Ill.), one to two tablets they were delivering Sensorcaine or saline pla- every 8 hours as needed. Data sheets were col- cebo. The randomization data and patient iden- lected on the patient’s first postoperative visit (typ- tifiers were kept in a separate, password-protected ically, postoperative day 3), at which point both database that was maintained exclusively by the drains were removed. office manager of the senior surgeon. All patient Once all the data were compiled in spread- information was anonymous. There were no other sheet format, statistical analysis was performed us- concurrent surgical procedures performed in these ing a t test. A value of p Ͻ 0.05 was considered patients. There was no compensation or other con- significant. Complete data were available on all siderations provided to patients in this study. patients. Sensorcaine is a safe drug, provided that one does not exceed the recommended dose. With RESULTS 0.25% Sensorcaine (used in this study), compli- There were 40 patients enrolled in this study, cations are exceedingly rare if the total dose is less 20 patients in each group. After randomization, than 175 mg when given subcutaneously. The tox- three patients (from the control group) were ex- icity of Sensorcaine is similar to that of other cluded from analysis (one patient eventually de- amide local anesthetics. These are related to in- sired abdominal liposuction after she was sched- creased plasma levels, which may be attributable to uled for breast reduction only, one patient spent overdosage, unintentional intravascular injection, a single night in the hospital for excessive nausea or slower metabolic degradation. The principal ad- related to anesthesia, and one patient did not verse effects affect the central nervous and the car- reveal that she was taking significant amounts of diovascular systems. Restlessness, anxiety, dizziness, analgesics for back pain and several psychotropic tinnitus, blurred vision, or tremors may occur, rarely medications). proceeding to convulsion. With inadvertent intra- There was no significant difference in patient vascular injection leading to an abrupt increase in age or weight of surgical specimens (Table 1). Pa- plasma levels, myocardial depression, arrhythmias, tients who received Sensorcaine intraoperatively or heart block may occur. Again, these complica- were discharged to home nearly 1 hour earlier than tions are all extraordinarily rare when the recom- those in the control group (mean, 2.9 hours versus mended dose is given appropriately.3–7 3.8 hours; p ϭ 0.003). Table 2 summarizes patient Vertical breast reduction was performed by one of the two senior surgeons (M.C. and N.S.K.) with the assistance of a plastic surgery resident.1,8 Table 1. Patient Demographics* One 10-mm Jackson-Pratt drain was routinely used Control Sensorcaine p (20 ؍ n) (17 ؍ in each side of the bilateral reduction mamma- (n plasty. Immediately before the final subcuticular Age, years 32.2 32.9 0.803 running closure, 10 cc of either placebo or Sen- Specimen weight, g Right 439.4 382.7 0.273 sorcaine was instilled into the Jackson-Pratt drain Left 431.3 392.9 0.477 and allowed to dwell within the surgical wound by *All data are reported as mean values. There were no significant clamping the drain for 10 minutes. Recovery room differences in patient age or specimen weight.

841 Plastic and Reconstructive Surgery • September 15, 2007

Table 2. Postoperative Patient Data* Control Sensorcaine Statistical p Significance (20 ؍ n) (17 ؍ n) Time in PACU, hours 3.8 2.9 0.003 Yes Pain scale, VAS Arrival in PACU 2.4 2.1 0.76 No 1 hr in PACU 3.2 2.9 0.73 No 2 hr in PACU 3.2 2.9 0.59 No 3 hr in PACU 2.9 2.4 0.45 No 4 hr in PACU 2.0 1.3 0.56 No PACU, postanesthesia care unit; VAS, visual analogue scale. *All data are reported as mean values. data obtained from the recovery room. Using the group (p ϭ 0.001). No patients in either group visual analogue scale to assess the level of pain required opioid analgesics after the third postop- experienced postoperatively, a trend was seen be- erative day. There were no treatment-related com- tween the two groups of a consistently lower pain plications and no adverse effects associated with score in the Sensorcaine group. Although this dif- Sensorcaine usage. ference was not statistically significant (largely re- lated to the number of patients), it does demon- DISCUSSION strate a trend (Fig. 1). Local anesthetic agents to ameliorate postop- Postoperatively (Table 3), patients in the Sen- erative pain and discomfort are commonly used in sorcaine group required significantly less oral opi- plastic surgery.14–17 There is increasing evidence oid analgesics while recovering at home (an aver- in various fields of surgery that the practice of age of 3.5 Vicodin tablets for Sensorcaine-treated “preemptive” anesthesia decreases postoperative patients versus 6.2 Vicodin tablets for the placebo pain.9–13 Previous reports have demonstrated that

Fig. 1. Postoperative patient data. Pain core measured using the visual analogue scale system. No pain is recorded as 0 and maximal pain is 10 on the y axis. Pain level on arrival in the postanesthesia care unit is represented as hour 0 on the x axis.

Table 3. Outpatient Data Control Sensorcaine Statistical p Significance (20 ؍ n) (17 ؍ n) Pain medication used POD 1 3.5 2.15 0.002 Yes POD 2 1.9 1.1 0.02 Yes POD 3 0.9 0.45 0.05 Yes POD 1–3 6.4 3.5 0.001 Yes POD, postoperative day. *All data are reported as mean values (all pain medication was regular strength Vicodin, in tablets).

842 Volume 120, Number 4 • Intraoperative Sensorcaine infiltration of the breast parenchyma with a solu- Sensorcaine group) when the pain scores were tion containing local anesthetics and epinephrine assessed in the postanesthesia care unit. We feel before performing reduction mammaplasty was this may exist for two reasons. First, a relatively safe and effective for reducing blood loss and post- small sample size may not show a statistical differ- operative patient discomfort.5,6,18–20 Despite this ence that a larger one would. Second, visual an- practice, patients may still have significant postop- alogue scale scores are obtained on patients while erative pain. In addition, infiltration of the breast in the postanesthesia care unit, and those patients tissue with long-acting and potentially cardiotoxic who are able to be discharged from the postan- agents such as Sensorcaine can be risky. To avoid the esthesia care unit earlier, it is assumed, should potential complications associated with infiltration have a lower pain score than those remaining be- of the breast parenchyma, Holmgren and Tarpila hind. The patients who may add to the signifi- studied topical application of Sensorcaine into the cance in this particular analysis are selecting them- surgical cavity.3 Although they demonstrated a sta- selves out, by definition, by their being discharged tistically significant reduction in postoperative from the postanesthesia care unit. Normality of pain and morphine use, their patients remained the data were assumed during our analysis. hospitalized overnight while receiving intermit- tent (every 5 hours) instillation of the local anes- CONCLUSIONS thetic into the wound or surgical cavity. Because The results of this study show that a single reduction mammaplasty is now routinely per- intraoperative infusion of Sensorcaine is a safe and formed as an ambulatory procedure in the United effective method for decreasing postoperative States, this would not be a practical approach. Other pain medication requirements by nearly one-half. authors have successfully used specialized infusion Patients were able to be discharged to home from pumps to deliver the local anesthetic after discharge the recovery room faster when Sensorcaine was from the hospital.4 However, this treatment modality administered in the operating room. There was a has the obvious disadvantage of increased cost asso- minimal increase in cost (approximately $10). As ciated with the equipment used. the Sensorcaine or placebo was injected into drains We sought to develop a preemptive anesthesia that are part of our normal postoperative routine, protocol for our reduction mammaplasty patients there was no additional surgical equipment neces- that was simple, cheap, and effective. Our intra- sary. We now use this protocol routinely in all pa- operative delivery of Sensorcaine to the surgical tients undergoing breast reduction. wound bed meets these three criteria. This study clearly demonstrates a significant benefit to pa- Nolan S. Karp, M.D. 305 East 47th Street, Suite 1A tients who received intraoperative Sensorcaine. New York, N.Y. 10017 These patients required only half the amount of [email protected] opioid oral analgesics once discharged from the hospital compared with the patients in the pla- DISCLOSURE cebo group. There are no financial disclosures for any of the Furthermore, these patients left the hospital contributing authors. approximately 1 hour earlier than the control arm. At our institution, patient savings from this REFERENCES earlier discharge can be substantial. Patients are 1. American Society for Aesthetic Plastic Surgery website. Avail- charged a flat fee of $2300 for operating room fees able at: http://www.surgery.org/download/2005stats.pdf. Accessed March 30, 2006. and the first 2 hours in the recovery room. For 2. Spector, J. A., Kleinerman, R., Culliford, A. T., and Karp, N. each additional hour exceeding 2 hours in the re- D. The vertical reduction mammaplasty: A prospective anal- covery room, patients are charged $500 per hour. ysis of patient outcomes. Plast. Reconstr. Surg. 117: 374, 2006. Consequently, patients who received Sensorcaine 3. Holmgren, R. T., and Tarpila, E. Intermittent injection of saved an average of $500 (the Sensorcaine used bupivacaine into the margin or the cavity after reduction mammaplasty. Scand. J. Plast. Reconstr. Surg. Hand Surg. 39: cost approximately $10 per dose). Given the cost 218, 2005. of the single dose of the Sensorcaine, it seems 4. Lu, L., and Fine, N. A. The efficacy of continuous local logical to use this on a regular basis. anesthetic infiltration in breast surgery: Reduction mamma- Although there are statistical differences be- plasty and reconstruction. Plast. Reconstr. Surg. 115: 1927, tween the two groups in time spent in the post- 2005. 5. Metaxotos, N. G. Asplund, O., and Hayes, M. The efficacy of anesthesia care unit and total outpatient pain bupivacaine with adrenaline in reducing pain and bleeding medication consumption, there was no significant associated with breast reduction: A prospective trial. Br. J. difference (just a trend for lower scores in the Plast. Surg. 52: 290, 1999.

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6. Mottura, A. A. Local anesthesia in reduction mastoplasty for 14. Holmgren, R., and Tarpila, E. Intermittent injection of bu- out-patient surgery. Aesthetic Plast. Surg. 16: 309, 1992. pivacaine into the margin or the cavity after reduction mam- 7. AstraZeneca. Sensorcaine package insert. Wilmington, Del.: maplasty. Scand. J. Plast. Reconstr. Surg. Hand Surg. 39: 218, AstraZeneca LP. 2005. 8. Karp, N. S. Medial pedicle/vertical breast reduction made 15. Rosenblatt, W. A splash twist to a painless breast augmenta- easy: The importance of complete inferior glandular resec- tion. Plast. Reconstr. Surg. 112: 715, 2003. tion. Ann. Plast. Surg. 52: 458, 2004. 16. Tebbets, J. Achieving a predictable 24 hour return to normal 9. Dahl, J. B., and Kehlet, H. The value of pre-emptive analgesia activities after breast augmentation: Part I. Refining practices in the treatment of postoperative pain. Br. J. Anaesth. 70: 434, by using motion and time study principles. Plast. Reconstr. 1993. Surg. 109: 273, 2002. 10. Bunemann, L., Thorshauge, H., Herlevsen, P., Iversen, A. D., 17. Weiss, A. A tumescent twist to breast augmentation. Plast. and Nielsen, F. B. Analgesia for outpatient surgery: Placebo Reconstr. Surg. 110: 1810, 2002. versus naproxen sodium (a non-steroidal anti-inflammatory 18. Rosaeg, O. P., Bell, M., Cicutti, N. J., Dennehy, K. C., Lui, drug) given before or after surgery. Eur. J. Anaesthesiol. 11: 461, 1994. A. C., and Krepski, B. Pre-incision infiltration with lidocaine 11. Gottschalk, A., Wu, C. L., Ochroch, E. A., et al. Current reduces pain and opioid consumption after reduction mam- treatment options for acute pain. Expert Opin. Pharmacother. maplasty. Reg. Anesth. Pain Med. 23: 575, 1998. 3: 1599, 2002. 19. Fayman, M., Beeton, A., Potgieter, E., and Becker, P. J. Com- 12. Priya, V., Divatia, J. V., Sareen, R., and Upadhye, S. Efficacy parative analysis of bupivacaine and ropivacaine for infiltra- of intravenous ketoprofen for pre-emptive analgesia. J. Post- tion analgesia for bilateral breast surgery. Aesthetic Plast. Surg. grad. Med. 48: 109, 2002. 27: 100, 2003. 13. Xie, W., Strong, J. A., Meij, J. T., Zhang, J. M., and Yu, L. 20. Di Marco, P., Grippaudo, F. R., Della Rocca, G., and De Vita, Neuropathic pain: Early spontaneous afferent activity is the R. Role of pre-emptive analgesia in reduction mammaplasty. trigger. Pain 116: 243, 2005. Scand. J. Plast. Reconstr. Surg. Hand Surg. 35: 297, 2001.

Instructions for Authors: Update Ethical Approval of Studies/Informed Consent Authors of manuscripts that describe experimental studies on either humans or animals must supply to the Editor a statement that the study was approved by an institutional review committee or ethics committee and that all human subjects gave informed consent. Such approval should be described in the Methods section of the manuscript. For studies conducted with human subjects, the method by which informed consent was obtained from the participants (i.e., verbal or written) also needs to be stated in the Methods section. In those situations where a formal institutional review board process is not available, the authors must indicate that the principles outlined in the Declaration of Helsinki have been followed. More information regarding the Declaration of Helsinki can be found at http://www.wma.net/e/policy/b3.htm.

844 BREAST

Reduction Mammaplasty: A Significant Improvement at Any Size

Jason A. Spector, M.D. Background: Reduction mammaplasty has been shown to be efficacious in Nolan S. Karp, M.D. reducing the burden of symptoms and improving the quality of life for patients New York, N.Y. with macromastia. However, most insurance carriers will not reimburse for mammaplasties involving less than 1000 g of total tissue resected. To refute this arbitrary policy, the authors set out to examine the effect of reduction mam- maplasty in which less than 1000 g of breast tissue was resected on patients’ macromastia-related symptoms and macromastia-related quality-of-life factors. Methods: All patients were given a custom-designed questionnaire designed to evaluate macromastia-related symptoms and other macromastia-related quality- of-life issues. Patients were then provided the same questionnaire at their final postoperative visit between 3 and 12 months after surgery. Results: A total of 59 patients underwent reduction mammaplasty of less than 1000 g. Reduction mammaplasty less than 1000 g resulted in significant de- creases in all macromastia-related symptoms analyzed, including upper back pain, lower back pain, neck pain, arm pain, shoulder pain, hand pain, breast pain, headaches, rashes, and/or itching and painful bra strap grooving (all p Ͻ 0.00002). Furthermore, reduction mammaplasty resulted in significant improve- ment in all quality-of-life factors analyzed, including difficulty buying clothes and bras, difficulty participating in sports, and difficulty running (all p Ͻ 0.00001). Conclusions: Reduction mammaplasty totaling less than 1000 g offers substan- tial relief of macromastia-associated symptoms and results in significant im- provement in patients’ quality of life. This prospective study conclusively dem- onstrates that reduction mammaplasty totaling less than 1000 g should be a fully reimbursable procedure. (Plast. Reconstr. Surg. 120: 845, 2007.)

eduction mammaplasty has been shown to Despite the observation that even “small” re- be efficacious in reducing the burden of ductions confer significant improvement for pa- Rsymptoms and improving the quality of life tients, most insurance carriers will not cover the for patients with macromastia. Several (mostly procedure unless more than 500 g of tissue per retrospective) studies have clearly demonstrated breast is resected.37–39 However, this is a com- that reduction mammaplasty ameliorates macro- pletely arbitrary number, and it is clear to most mastia-associated symptoms such as neck pain, plastic surgeons that the term macromastia may back pain, and painful bra grooving while im- be applied to many women with moderate breast proving quality of life by allowing patients to hypertrophy who may require less than 1000 g of more easily purchase clothing and participate in total resection to improve their breast-related sporting activities.1–36 symptoms. Most studies demonstrating the benefits of re- From the Division of Plastic Surgery, Weill Cornell College of duction mammaplasty have examined heteroge- Medicine, Cornell University, New York Presbyterian Hos- neous cohorts of patients, few of whom had less pital, and the Institute of Reconstructive Plastic Surgery, than 500 g resected per breast. To rectify this de Division of Plastic Surgery, New York University School of facto discriminatory practice against those Medicine. women with symptomatic breast hypertrophy Received for publication April 6, 2006; accepted May 29, 2006. that is not large enough (on a purely weight Presented at the Northeastern Society of Plastic and Recon- basis) to meet the requirements of most third- structive Surgery meeting, in Boston, Massachusetts, No- party payers, we set out to answer the following vember 30, 2006. question—Do “small” breast reductions Copyright ©2007 by the American Society of Plastic Surgeons (Ͻ1000 g total) significantly improve patient macromastia-related symptoms and other asso- DOI: 10.1097/01.prs.0000277660.49802.76 ciated quality-of-life factors?

www.PRSJournal.com 845 Plastic and Reconstructive Surgery • September 15, 2007

PATIENTS AND METHODS and postoperative data, and a chi-square test was Beginning in July of 2002, all patients under- used to compare complication rates. going breast reduction surgery by the senior author (N.S.K.) were given a custom-designed RESULTS questionnaire designed to evaluate the macromas- At the time of the submission of this article, a tia-related symptoms and other macromastia-re- total of 171 patients had completed their postop- lated quality-of-life issues. This questionnaire, erative questionnaires. Twenty patients did not which was given to patients at the time of their complete their questionnaires and were excluded initial consultation, was designed in large part on from analysis. Fifty-nine patients had reductions the basis of the previously validated surveys used by totaling less than 1000 g. Fifty-five procedures (93 Schnur et al.3 and Collins et al.14 Responses were percent) were vertical reduction mammaplasties, given on a scale from 1 (none/never) to 5 (al- and four (7 percent) were Wise-pattern inferior ways). Patients were then provided the same ques- pedicle procedures. The overall average weight of tionnaire at their final postoperative visit, usually reduction per breast was 415 g (range, 155 to 570 g). between 3 months and 1 year after surgery.18 For Of the 59 patients, 17 had reductions totaling less patients who failed to return for a final postoper- than 750 g (15 vertical reduction mammaplasties ative visit, a questionnaire was sent by mail. The and two Wise-pattern inferior pedicle procedures), senior author performed all operations. The 42 had reductions between 750 and 1000 g (40 ver- method of breast reduction chosen depended on tical reduction mammaplasties and two Wise-pattern several variables such as estimated weight of re- inferior pedicle procedures). In the less-than-750-g duction, projected nipple movement, and pa- reduction group, the average weight of reduction tient/surgeon choice. Although there were no ab- was 626 g, with an average decrease of 1.7 cup sizes. solute parameters, in general, vertical reduction In the 750- to 1000-g reduction group, the average mammaplasty was usually chosen if there was suf- weight of reduction was 916 g, with an average de- ficient skin elasticity and the reduction was esti- crease of 2.1 cup sizes. Other pertinent patient vital mated to be less than 1000 g (per breast) or if the statistics are listed in Table 1. nipple movement was estimated to be less than 12 There were no major complications (defined cm. For the remainder of the reductions, a Wise- as readmission to the hospital for infection, reop- pattern with the nipple-areola complex based on eration for bleeding or nipple loss, or an operative an inferior pedicle was performed. All patients evacuation of a hematoma). In the less-than-750-g over the age of 40 years were required to have group, there were four minor complications (one negative mammography within 1 year before sur- superficial infection and three seromas requiring gery. aspiration) and in the 750- to 1000-g group, there The Wise pattern reduction mammaplasties were 12 minor complications (four superficial in- were performed in the standard fashion.40 The fections and eight seromas requiring aspiration). method of vertical reduction mammaplasty is based Minor office revisions, defined as scar revision or in part on the technique described by Hall-Findlay,41 excision, were performed in three patients in the with some modifications as previously described by less-than-750-g group and in none of the 750- to the senior author.18,42 A Wilcoxon matched-pairs 1000-g group. All revisions were performed under signed rank test was used to compare preoperative local anesthesia. There was no significant differ-

Table 1. Patient Variables Stratified by Total Breast Tissue Resected Reduction Mammaplasty

Patient Variables <750 g (%) 750–1000 g (%) p No. of patients 17 (29) 42 (71) N/A Age, years 36.9 36.1 NS Body mass index 24.0 Ϯ 2.8 25.5 Ϯ 2.8 NS Average follow-up, days postoperatively 159 156 NS Average total weight of resection, g 626 Ϯ 112 916 Ϯ 67 N/A Previous physical therapy 9 (56) 14 (33) N/A Previous chiropractic therapy 10 (63) 16 (38) N/A Previous back radiographs 9 (56) 12 (29) N/A Previous back surgery 0 1 (2) N/A Previous neck surgery 0 0 N/A N/A, statistical comparison not applicable; NS, not statistically significant by t test.

846 Volume 120, Number 4 • Reduction Mammaplasty

Table 2. Complications Stratified by Total Breast cluding upper back pain (3.9 preoperatively ver- Tissue Resected sus 1.5 postoperatively; p Ͻ 0.00003), lower back Complications <750 g 750–1000 g pain (3.8 preoperatively versus 1.3 postopera- Ͻ Seroma requiring aspiration 3 8 tively; p 0.00003), neck pain (3.4 preopera- Superficial infection 1 4 tively versus 1.5 postoperatively; p Ͻ 0.00024), Wound breakdown 0 0 arm pain (1.9 preoperatively versus 1.1 postop- Hematoma evacuation in eratively; p Ͻ 0.0039), shoulder pain (3.5 pre- operating room 0 0 Ͻ Scar revision (other than operatively versus 1.4 postoperatively; p dog-ear) 1 0 0.00003), breast pain (2.2 preoperatively versus Dog-ear revision 2 0 1.5 postoperatively; p Ͻ 0.01), headaches (2.9 Total no. of patients with Ͻ complications* 7† 9† preoperatively versus 1.4 postoperatively; p *Three patients in the 750 to 1000-g total tissue resected group had 0.0046), rashes and/or itching (2.9 preopera- two complications each. tively versus 1.1 postoperatively; p Ͻ 0.002), and †Chi-square ϭ 2.39 with 1 degree of freedom; difference not signif- painful bra strap grooving (3.7 preoperatively ϭ icant (significance set at p 0.05). versus 1.1 postoperatively; p Ͻ 0.00006). The improvement in hand pain (1.5 preoperatively ence in the rate of complications between the two versus 1.2 postoperatively) did not reach statis- Ͻ groups (Table 2). tical significance (p 0.10) (Table 3). Quality-of-Life Factors Reduction Mammaplasty: Less than 750 g Total The effect of reduction mammaplasty (Ͻ750 g Weight Resected of total breast tissue resected) on several quality-of- Macromastia-Associated Symptoms life factors was assessed. Reduction mammaplasty The effect of reduction mammaplasty on sev- resulted in significant improvement in all quality-of- eral macromastia-related symptoms was assessed life factors analyzed, including difficulty buying in patients who had less than 750 g of total breast clothes and bras (4.6 preoperatively versus 1.4 post- tissue resected. Reduction mammaplasty re- operatively; p Ͻ 0.00003) difficulty participating in sulted in significant decreases in all but one of sports (4.1 preoperatively versus 1.2 postoperatively; the macromastia-related symptoms analyzed in- p Ͻ 0.00002), and difficulty running (4.4 preoper-

Table 3. Macromastia-Associated Symptoms Stratified by Total Breast Tissue Resected Reduction Mammaplasty <750 g Reduction Mammaplasty 750–1000 g Macromastia-Associated Symptoms Preoperatively Postoperatively p Preoperatively Postoperatively p Upper back pain 3.9 Ϯ 1.2 1.5 Ϯ 0.7 Ͻ0.00003* 3.7 Ϯ 1.3 1.5 Ϯ 0.8 Ͻ0.00001* Lower back pain 3.8 Ϯ 1.2 1.3 Ϯ 0.6 Ͻ0.00003* 3.5 Ϯ 1.2 1.4 Ϯ 0.7 Ͻ0.00001* Neck pain 3.4 Ϯ 1.6 1.5 Ϯ 0.5 Ͻ0.00024* 3.7 Ϯ 1.3 1.4 Ϯ 0.8 Ͻ0.00001* Arm pain 1.9 Ϯ 1.6 1.1 Ϯ 0.3 Ͻ0.0039* 2.5 Ϯ 1.4 1.1 Ϯ 0.3 Ͻ0.00001* Shoulder pain 3.5 Ϯ 1.4 1.4 Ϯ 0.5 Ͻ0.00003* 3.6 Ϯ 1.2 1.3 Ϯ 0.7 Ͻ0.00001* Hand pain 1.5 Ϯ 1.1 1.2 Ϯ 0.5 NS 2.1 Ϯ 1.3 1.2 Ϯ 0.6 Ͻ0.00002* Breast pain 2.2 Ϯ 1.3 1.5 Ϯ 0.6 Ͻ0.01* 3.1 Ϯ 1.2 1.6 Ϯ 0.7 Ͻ0.00001* Headaches 2.9 Ϯ 1.5 1.4 Ϯ 1.0 Ͻ0.0046* 2.8 Ϯ 1.3 1.4 Ϯ 0.8 Ͻ0.00001* Rashes and/or itching 2.9 Ϯ 1.8 1.1 Ϯ 0.3 Ͻ0.002* 3.1 Ϯ 1.3 1.2 Ϯ 0.5 Ͻ0.00001* Painful bra strap grooving 3.7 Ϯ 1.6 1.1 Ϯ 0.2 Ͻ0.00006* 4.2 Ϯ 1.0 1.2 Ϯ 0.7 Ͻ0.00001* NS, not significant. *Statistically significant by Wilcoxon matched-pairs signed-rank test.

Table 4. Macromastia-Related Quality-of-Life Factors Stratified by Total Breast Tissue Resected Reduction Mammaplasty <750 g Reduction Mammaplasty 750–1000 g

Quality-of-Life Factors Preoperatively Postoperatively p Preoperatively Postoperatively p Difficulty buying clothes and bras 4.6 Ϯ 1.2 1.4 Ϯ 0.5 Ͻ0.00003* 4.4 Ϯ 0.9 1.3 Ϯ 0.8 Ͻ0.00001* Difficulty participating in sports 4.1 Ϯ 1.3 1.2 Ϯ 0.4 Ͻ0.00002* 4.3 Ϯ 1.0 1.4 Ϯ 1.0 Ͻ0.00001* Difficulty running 4.4 Ϯ 1.3 1.1 Ϯ 0.3 Ͻ0.00003* 4.4 Ϯ 1.0 1.4 Ϯ 0.9 Ͻ0.00001* *Statistically significant by Wilcoxon matched-pairs signed rank test.

847 Plastic and Reconstructive Surgery • September 15, 2007 atively versus 1.1 postoperatively; p Ͻ 0.00001) (Ta- third-party payers will usually refuse reimbursement ble 4). for breast reductions totaling less than 1000 g (500 g per breast). Arbitrary limits do not take into con- Reduction Mammaplasty: 750 to 1000 g Total sideration the patient’s height or weight. Obviously, Weight Resected the impact of DD breasts on a small woman near ideal body weight are very different from the same Macromastia-Associated Symptoms size breasts on an overweight woman several inches The effect of reduction mammaplasty on sev- taller. How this 500-g floor was determined by the eral macromastia-related symptoms was assessed insurance carriers has always been mysterious, but in patients who had 750 to 1000 g of total breast on examining all available studies regarding reduc- tissue resected. Reduction mammaplasty resulted tion mammaplasty, there is a paucity of outcomes in significant decreases in all macromastia-related data regarding “smaller” breast reductions, or those symptoms analyzed, including upper back pain less than 500 g per breast. Most studies are retro- (3.7 preoperatively versus 1.5 postoperatively), spective, and few if any include subjects whose re- lower back pain (3.5 preoperatively versus 1.4 post- ductions totaled less than 1000 g. operatively), neck pain (3.7 preoperatively versus Compelled by anecdotal experience and the 1.4 postoperatively), arm pain (2.5 preoperatively desire to have data with which insurance compa- versus 1.1 postoperatively), shoulder pain (3.6 pre- nies could be rebutted, we endeavored to more operatively versus 1.3 postoperatively), breast pain rigorously examine the question of whether or not (3.1 preoperatively versus 1.6 postoperatively), head- “small” breast reductions conferred significant im- aches (2.8 preoperatively versus 1.4 postoperatively), provement. Our prospectively collected data con- rashes and/or itching (3.1 preoperatively versus 1.2 clusively demonstrate that reduction mamma- postoperatively), and painful bra strap grooving (4.2 Ͻ plasty less than 1000 g total provide significant preoperatively versus 1.2 postoperatively) (all p relief from all macromastia-related symptoms ex- 0.00001). The effect of reduction mammaplasty on amined (e.g., neck, back, arm pain) and all mac- hand pain was also significant (2.1 preoperatively Ͻ romastia-related quality-of-life factors examined versus 1.2 postoperatively; p 0.00002) (Table 3). (e.g., difficulty playing sports, buying clothes). Quality-of-Life Factors This significant improvement in all factors exam- The effect of reduction mammaplasty (750 ined was seen even in the cohort of patients whose to 1000 g total breast tissue resected) on several reductions totaled less than 750 g (with the ex- quality-of-life factors was assessed. Reduction ception of hand pain). mammaplasty resulted in significant improve- The patient population in this study was younger ment in all quality-of-life factors analyzed, in- (mean age, 36 years) and thinner (mean body mass cluding difficulty buying clothes and bras (4.4 index, 25) compared with other reduction mamma- preoperatively versus 1.3 postoperatively), diffi- plasty outcomes studies. This younger, thinner, and culty participating in sports (4.3 preoperatively presumably more active group of patients may be versus 1.4 postoperatively), and difficulty run- more sensitive to the burdens associated with even ning (4.4 preoperatively versus 1.4 postopera- slightly larger breasts. This is an idea that deserves Ͻ tively) (all p 0.00001) (Table 4). more scrutiny. Our complication rate was less fre- quent than the published parameters. This likely DISCUSSION reflects the smaller nature of the breast reduction Perhaps no other plastic surgical procedure and the younger average age and smaller average has been studied as rigorously as reduction body mass index of our cohort. mammaplasty regarding patient outcomes. The overwhelming majority (93 percent) of More than 30 studies have demonstrated that reduction mammaplasties in this study were per- breast reduction results in significant improve- formed according to our “vertical” reduction ment in a myriad of patient macromastia-related technique (a modification of Hall-Findlay’s tech- symptoms and other macromastia-related quality- nique).41–43 This reflects our preference to use this of-life factors.1–36 These findings have been con- technique when performing reductions totaling sistent regardless of the type of surgical approach less than 1000 g in mildly to moderately ptotic (Wise pattern or “short scar”) or pedicle used to breasts. However, as we have recently demon- transpose the nipple-areola complex. strated, there is no reason to suppose that had a Armed with these compelling data, plastic sur- Wise-pattern been used more frequently in this geons have been able to induce insurance compa- group of patients, the improvement in symptoms nies to cover many of these procedures. However, would have differed.18

848 Volume 120, Number 4 • Reduction Mammaplasty

Because this study examines only patients who 2. Mandrekas, A. D., Zambacos, G. J., Anastasopoulos, A., et al. have had breast reduction, does this inherently Reduction mammaplasty with the inferior pedicle technique: Early and late complications in 371 patients. Br. J. Plast. Surg. cause a reporting bias? That is, are we only seeing 49: 442, 1996. the subset of patients who are most symptomatic 3. Schnur, P. L., Schnur, D. P., Petty, P. M., et al. Reduction or most sensitive to mild to moderate breast hy- mammaplasty: An outcome study. Plast. Reconstr. Surg. 100: pertrophy? The answer is likely yes, but that does 875, 1997. not detract from the justifiability and necessity of 4. Shakespeare, V., and Cole, R. P. Measuring patient-based outcomes in a plastic surgery service: Breast reduction sur- these procedures. As discussed by Kerrigan et al., gical patients. Br. J. Plast. Surg. 50: 242, 1997. there are several other disease states where dis- 5. Godwin, Y., Wood, S. H., and O’Neill, T. J. A comparison of crepancies exist between the severity of physical the patient and surgeon opinion on the long-term aesthetic finding and the magnitude of symptoms.44,45 outcome of reduction mammaplasty. Br. J. Plast. Surg. 51: 444, Within our cohort of patients, more than one- 1998. 6. Faria, F. S., Guthrie, E., Bradbury, E., et al. Psychosocial third of patients had radiographs, chiropractic in- outcome and patient satisfaction following breast reduction tervention, or physical therapy for symptoms re- surgery. Br. J. Plast. Surg. 52: 448, 1999. lated to their breasts. This is particularly striking 7. Hidalgo, D. A. Improving safety and aesthetic results in in- given the fact that none of these women had larger verted T scar breast reduction. Plast. Reconstr. Surg. 103: 874, than DD cup size breasts and all had resolution of 1999. 8. Lejour, M. Vertical mammaplasty: Early complications after their symptoms with reductions totaling less than 250 personal consecutive cases. Plast. Reconstr. Surg. 104: 764, 1000 g. We are encouraging or justifying reduc- 1999. tion mammaplasty not for all women with mild to 9. Temple, C. L., and Hurst, L. N. Reduction mammaplasty moderate breast hypertrophy but specifically for improves breast sensibility. Plast. Reconstr. Surg. 104: 72, 1999. the subgroup of women within that is most sen- 10. Behmand, R. A., Tang, D. H., and Smith, D. J., Jr. Outcomes in breast reduction surgery. Ann. Plast. Surg. 45: 575, 2000. sitive to and thus experiences the most severe 11. Ramon, Y., Sharony, Z., Moscona, R. A., et al. Evaluation and symptoms. Presumably, this is the self-selecting comparison of aesthetic results and patient satisfaction with group of women with mild to moderate breast bilateral breast reduction using the inferior pedicle and hypertrophy who are presenting to the plastic sur- McKissock’s vertical bipedicle dermal flap techniques. Plast. geon’s office for reduction mammaplasty less to- Reconstr. Surg. 106: 289, 2000. 12. Chadbourne, E. B., Zhang, S., Gordon, M. J., et al. Clinical taling than 1000 g. outcomes in reduction mammaplasty: A systematic review and meta-analysis of published studies. Mayo Clin. Proc. 76: 503, 2001. CONCLUSIONS 13. Jones, S. A., and Bain, J. R. Review of data describing out- The data from this prospective, longitudinal comes that are used to assess changes in quality of life after study corroborate the widely held impression of reduction mammaplasty. Plast. Reconstr. Surg. 108: 62, 2001. many plastic surgeons that macromastia is not a 14. Collins, E. D., Kerrigan, C. L., Kim, M., et al. The effectiveness of surgical and nonsurgical interventions in relieving the term that can be defined by a number but rather symptoms of macromastia. Plast. Reconstr. Surg. 109: 1556, needs to be considered within the context of the 2002. individual patient. It is now clear that significant 15. Cruz-Korchin, N., and Korchin, L. Vertical versus Wise pat- symptomatic improvement occurs when less than tern breast reduction: Patient satisfaction, revision rates, and 1000 g (or even 750 g) of breast tissue is resected. complications. Plast. Reconstr. Surg. 112: 1573, 2003. 16. Harbo, S. O., Jorum, E., and Roald, H. E. Reduction mam- Insurance carriers take note: small breast reductions maplasty: A prospective study of symptom relief and alter- are not just mastopexies by another name but are ations of skin sensibility. Plast. Reconstr. Surg. 111: 103, 2003. themselves effective curative procedures for the bur- 17. Blomqvist, L., and Brandberg, Y. Three-year follow-up on densome condition of breast hypertrophy. clinical symptoms and health-related quality of life after re- duction mammaplasty. Plast. Reconstr. Surg. 114: 49, 2004. Nolan S. Karp, M.D. 18. Spector, J. A., Kleinerman, R., Culliford, A. T., and Karp, 305 East 47th Street, Suite 1A N. S. The vertical reduction mammaplasty: A prospective New York, N.Y. 10017 analysis of patient outcomes. Plast. Reconstr. Surg. 117: 374, [email protected] 2006. 19. Hermans, B. J., Boeckx, W. D., De Lorenzi, F., et al. Quality of life after breast reduction. Ann. Plast. Surg. 55: 227, 2005. DISCLOSURE 20. Freire, M., Neto, M. S., Garcia, E. B., et al. Quality of life after Neither of the authors of this article has any finan- reduction mammaplasty. Scand. J. Plast. Reconstr. Surg. Hand Surg. 38: 335, 2004. cial interests to disclose. 21. Sood, R., Mount, D. L., Coleman, J. J., III, et al. Effects of reduction mammaplasty on pulmonary function and symp- REFERENCES toms of macromastia. Plast. Reconstr. Surg. 111: 688, 2003. 1. Lassus, C. A 30-year experience with vertical mammaplasty. 22. Chao, J. D., Memmel, H. C., Redding, J. F., et al. Reduction Plast. Reconstr. Surg. 97: 373, 1996. mammaplasty is a functional operation, improving quality of

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life in symptomatic women: A prospective, single-center 34. Gonzalez, F., Walton, R. L., Shafer, B., et al. Reduction mam- breast reduction outcome study. Plast. Reconstr. Surg. 110: maplasty improves symptoms of macromastia. Plast. Reconstr. 1644, 2002. Surg. 91: 1270, 1993. 23. Chalekson, C. P., Neumeister, M. W., Zook, E. G., et al. 35. Hughes, L. A., and Mahoney, J. L. Patient satisfaction with Outcome analysis of reduction mammaplasty using the mod- reduction mammaplasty: An early survey. Aesthetic Plast. Surg. ified Robertson technique. Plast. Reconstr. Surg. 110: 71, 2002. 17: 345, 1993. 24. Tykka, E., Asko-Seljavaara, S., and Hietanen, H. Patients’ satis- 36. Brown, D. M., and Young, V. L. Reduction mammaplasty for faction with breast reconstruction and reduction mammaplasty. macromastia. Aesthetic Plast. Surg. 17: 211, 1993. Scand. J. Plast. Reconstr. Surg. Hand Surg. 35: 399, 2001. 37. Sommer, N. Z., Zook, E. G., and Verhulst, S. J. The prediction 25. Blomqvist, L., Eriksson, A., and Brandberg, Y. Reduction of breast reduction weight. Plast. Reconstr. Surg. 109: 506, mammaplasty provides long-term improvement in health 2002. status and quality of life. Plast. Reconstr. Surg. 106: 991, 2000. 38. Becker, H. Breast reduction insurance denials. Plast. Reconstr. 26. Mizgala, C. L., and MacKenzie, K. M. Breast reduction out- come study. Ann. Plast. Surg. 44: 125, 2000. Surg. 114: 1687, 2004. 27. Shakespeare, V., and Postle, K. A qualitative study of patients’ 39. Wagner, D. S., and Alfonso, D. R. The influence of obesity views on the effects of breast-reduction surgery: A 2-year and volume of resection on success in reduction mamma- follow-up survey. Br. J. Plast. Surg. 52: 198, 1999. plasty: An outcomes study. Plast. Reconstr. Surg. 115: 1034, 28. Glatt, B. S., Sarwer, D. B., O’Hara, D. E., et al. A retrospective 2005. study of changes in physical symptoms and body image after 40. Bostwick, J., III. Reduction mammaplasty. In J. Bostwick, III reduction mammaplasty. Plast. Reconstr. Surg. 103: 76, 1999. (Ed.), Plastic and Reconstructive Breast Surgery. St. Louis, Mo.: 29. Atterhem, H., Holmner, S., and Janson, P. E. Reduction Quality Medical, 2000. P. 371. mammaplasty: Symptoms, complications, and late results. A 41. Hall-Findlay, E. J. A simplified vertical reduction mamma- retrospective study on 242 patients. Scand. J. Plast. Reconstr. plasty: Shortening the learning curve. Plast. Reconstr. Surg. Surg. Hand Surg. 32: 281, 1998. 104: 748, 1999. 30. Bruhlmann, Y., and Tschopp, H. Breast reduction improves 42. Karp, N. S. Medial pedicle/vertical breast reduction made symptoms of macromastia and has a long-lasting effect. Ann. easy: The importance of complete inferior glandular resec- Plast. Surg. 41: 240, 1998. tion. Ann. Plast. Surg. 52: 458, 2004. 31. Raispis, T., Zehring, R. D., and Downey, D. L. Long-term functional results after reduction mammaplasty. Ann. Plast. 43. Hall-Findlay, E. J. Pedicles in vertical breast reduction and Surg. 34: 113, 1995. mastopexy. Clin. Plast. Surg. 29: 379, 2002. 32. McMahan, J. D., Wolfe, J. A., Cromer, B. A., et al. Lasting 44. Kerrigan, C. L., Collins, E. D., Kneeland, T. S., et al. Mea- success in teenage reduction mammaplasty. Ann. Plast. Surg. suring health state preferences in women with breast hyper- 35: 227, 1995. trophy. Plast. Reconstr. Surg. 106: 280, 2000. 33. Dabbah, A., Lehman, J. A., Jr., Parker, M. G., et al. Re- 45. Kerrigan, C. L., Collins, E. D., Kim, H. M., et al. Reduction duction mammaplasty: An outcome analysis. Ann. Plast. mammaplasty: Defining medical necessity. Med. Decis. Making Surg. 35: 337, 1995. 22: 208, 2002.

Membership in the American Society of Plastic Surgeons For information regarding membership in the American Society of Plastic Surgeons, contact: American Society of Plastic Surgeons 444 E. Algonquin Road Arlington Heights, Ill. 60005 Tel: 847-228-9900 Fax: 847-228-9131

850 IDEAS AND INNOVATIONS

Pedicle Preservation Technique for Arterial and Venous Turbocharging of Free DIEP and Muscle-Sparing TRAM Flaps

Charles Y. Tseng, M.D. Patrick O. Lang, B.A. Nicole A. Cipriani, M.S. David H. Song, M.D. Chicago, Ill.

utologous tissue transfer is a reliable deep inferior epigastric artery and vein. The pedi- method for breast reconstruction and is cle preservation technique described in this article Aconsidered by many to be the optimal is easily incorporated into standard methods of technique for postmastectomy breast reconstruc- flap dissection and provides a “lifeboat” for these tion.1 The move from free transverse rectus ab- delicate flaps that is readily used when the need for dominis musculocutaneous (TRAM) flaps to improved arterial perfusion and venous drainage is muscle-sparing and perforator free flaps is a sig- suspected or becomes apparent. nificant advance associated with decreases in postoperative pain and donor-site morbidity.2 In PATIENTS AND METHODS patients whose flaps demonstrate intraoperative Before making incisions, patients are evalu- arterial insufficiency or venous congestion, mi- ated using Doppler ultrasound to identify and crovascular augmentation using “turbocharging” mark the location of perforators of the deep in- or “supercharging” techniques has been ferior epigastric artery. The expected location of described.3–9 In the automotive world, turbo- the superficial inferior epigastric system is also charging is the use of the engine’s own exhaust marked on the abdomen. Incisions are made with for additional power. Similarly, surgical turbo- care to preserve the superficial inferior epigastric charging describes vascular augmentation using artery and vein. If the superficial inferior epigas- a vascular source present within the flap territory tric pedicle is present, pulsatile, and of sufficient either directly or by means of an interposed vein caliber, we dissect it to its origin from the femoral graft. Surgical supercharging describes vascular vessels for superficial inferior epigastric artery free augmentation using distant, unrelated source flap reconstruction. If the superficial inferior epi- vessels.10,11 Current microvascular turbocharging gastric pedicle is pulseless or small, we dissect the and supercharging techniques require harvest of superficial inferior epigastric pedicle to the point a vein graft conduit or dissection of a secondary where it crosses the inguinal ligament for a length donor vessel site, and options for intraoperative of approximately 3 to 5 cm. We then proceed with free flap salvage that stay true to the goals of DIEP flap dissection and base it on either the limiting donor- and recipient-site morbidity are medial or lateral row perforators. Furthermore, limited. when the deep inferior epigastric pedicle runs We present a novel technique and case series extramuscularly along the posterior aspect of the of arterial, venous, and arterial/venous turbo- rectus abdominis muscle, we routinely save— charging of deep inferior epigastric perforator rather than ligate—the non–perforator commit- (DIEP) and muscle-sparing TRAM flaps using ted branch (Fig. 1); preservation of this branch the non–perforator committed branch of the creates a long (5 to 8 cm) in situ arterial and venous conduit and adds little additional time to From the Section of Plastic and Reconstructive Surgery, Uni- the reconstructive procedure. We then harvest the versity of Chicago Hospitals, and the University of Chicago, flap, anastomose the artery and vein to the inter- Pritzker School of Medicine. nal mammary vessels, and inset. Received for publication June 20, 2006; accepted October 24, In situations when the flap appears suspicious 2006. for arterial insufficiency or venous congestion, the Copyright ©2007 by the American Society of Plastic Surgeons lifeboat is used to salvage the flap by constructing DOI: 10.1097/01.prs.0000277663.50061.83 arterial and/or venous turbocharging circuits to

www.PRSJournal.com 851 Plastic and Reconstructive Surgery • September 15, 2007 augment blood flow. Since developing the pedicle CASE REPORTS preservation technique, we have had the occasion Cases 1 and 2 to use it in three cases. These cases (two illustrated In case 1, arterial turbocharging was performed (Fig. 2, and one described for brevity) demonstrate the above). In case 2, venous turbocharging was performed (Fig. 2, versatility of the technique. center). Case 3 In case 3, arterial and venous turbocharging was performed (Fig. 2, below). A 59-year-old woman with a history of left breast cancer underwent mastectomy, followed by adjuvant chemo- therapy and radiation therapy. She presented for delayed left breast reconstruction. The flap was elevated using standard techniques beginning laterally to expose the superficial epigastric vessels. The super- ficial inferior epigastric artery was pulseless, and examination of the ipsilateral medial and lateral deep inferior epigastric artery perforators revealed them to be small. Therefore, we opted for muscle-sparing TRAM flap reconstruction. The me- dial row perforators and a small sliver of surrounding muscle were dissected free from the body of the rectus. The lateral (non–perforator committed) branch of the deep inferior epi- gastric pedicle was dissected and saved (Fig. 3). The deep in- ferior epigastric pedicle was transected and the flap transferred to the chest wall where an end-to-end anastomosis to the ipsi- lateral internal mammary vessels was completed. As we inset the flap, zone 3 appeared compromised. The arterial anastomosis was patent, but no arterial flow in zone 3 could be detected by Doppler ultrasound. Therefore, we con- structed an arterial turbocharge circuit from the lateral (non– perforator committed) branch of the deep inferior epigastric artery to the superficial inferior epigastric artery to augment arterial perfusion to the flap. Thereafter, the distal segment exhibited good coloration and capillary refill. Repeated Dopp- ler ultrasound demonstrated pulsatile arterial flow. However, after allowing the flap to perfuse for 20 minutes, we noticed that the superficial inferior epigastric vein appeared engorged. To avoid the possibility of venous congestion and flap loss, we performed venous turbocharging of the flap by anastomosing the superficial inferior epigastric vein to the lateral (non–per- forator committed) branch of the deep inferior epigastric vein (Figs. 2, below, and 4). There were no other complications, and the patient was discharged a few days later. Follow-up revealed no partial flap loss or late fat necrosis.

DISCUSSION Free flap breast reconstruction offers unpar- alleled flexibility and superior outcomes. Both muscle-sparing TRAM and DIEP flaps are proven to be reliable techniques for autologous breast reconstruction and have become the workhorse for most microsurgical breast surgeons. Free mus- cle-sparing TRAM and DIEP flaps are associated with less postoperative pain, reduced donor-site morbidity, and improved abdominal wall integrity. Compared with pedicled and free TRAM flaps, the Fig. 1. Schematic illustration of the technique. (Above) Deep in- often delicate muscle-sparing and perforator free ferior epigastric pedicle with medial and lateral row perforators flaps are at increased risk for arterial insufficiency insitu.(Center)StandardDIEPflapbasedonasinglerowofmedial and/or venous congestion, with consequent par- perforators. (Below) Preservation of the lateral (non–perforator tial flap loss or fat necrosis. Not uncommonly, an committed) branch of the pedicle. If the flap is based on the lat- intraoperative flap event after committing to the eral perforators, the medial branch of the pedicle is preserved. DIEP or muscle-sparing TRAM flap is seen.

852 Volume 120, Number 4 • Pedicle Preservation

The pedicle preservation technique that we de- scribe creates an intraoperative lifeboat consisting of a long, native, in situ arterial and venous conduit. When confronted with intraoperative evidence or suspicion of arterial insufficiency or, more com-

Fig. 3. Preservation of the non–perforator committed deep in- ferior epigastric branch and superficial inferior epigastric pedicle in a muscle-sparing TRAM flap. The deep inferior epigastric pedi- cle is indicated by the black arrow. The medial (perforator com- mitted) branch of the deep inferior epigastric pedicle is indicated by the black arrowhead. The lateral (non–perforator committed) branch of the deep inferior epigastric pedicle is indicated by the white arrowhead. The superficial inferior epigastric artery and vein are indicated by the white arrow.

monly, venous congestion, this lifeboat can be used to salvage these afflicted flaps through the creation of arterial and/or venous turbocharge circuits.

Fig. 4. Deep inferior epigastric artery/vein–to–superficial infe- riorepigastricartery/veinarterialandvenousturbocharging.The Fig. 2. Schematic illustration of arterial and/or venous turbo- deep inferior epigastric pedicle is indicated by the black arrow. charging in three cases. (Above) Deep inferior epigastric artery The lateral (non–perforator committed) branch of the deep infe- (DIEA)–to–contralateral DIEA perforator arterial turbocharging. rior epigastric artery and vein anastomosed to the superficial in- (Center) Deep inferior epigastric vein (DIEV)–to–superficial infe- ferior epigastric artery and vein is indicated by the white arrow- rior epigastric venous (SIEV) turbocharging. (Below) Deep inferior head. The medial (perforator committed) branch of the deep epigastric artery/vein (DIEA/V)–to–superficial inferior epigastric inferior epigastric artery and vein to the flap is indicated by the artery/vein (SIEA/V) arterial and venous turbocharging. black arrowhead.

853 Plastic and Reconstructive Surgery • September 15, 2007

Preserving the non–perforator committed 2. Schusterman, M. A. The free TRAM flap. Clin. Plast. Surg. 25: branch of the deep inferior epigastric pedicle 191, 1998. when possible adds little additional operative 3. Harashina, T., Sone, K., Inoue, T., et al. Augmentation of circulation of pedicled transverse rectus abdominis muscu- time, obviates procurement of an interposition locutaneous flaps by microvascular surgery. Br. J. Plast. Surg. vein graft, precludes dissection of a secondary 40: 367, 1987. donor artery or vein, uses vessels that are good 4. Semple, J. Retrograde microvascular augmentation (turbo- size matches, stays true to the goal of minimizing charging) of a single-pedicle TRAM flap through a deep donor-site morbidity, and expands the number inferior epigastric arterial and venous loop. Plast. Reconstr. of microsurgical techniques with which the sur- Surg. 93: 109, 1994. 5. Wechselberger, G., Shoeller, T., Bauer, T., et al. Venous geon can effectively address these intraoperative superdrainage in deep inferior epigastric perforator flap problems. breast reconstruction. Plast. Reconstr. Surg. 108: 162, 2001. 6. Barnett, G., Carlisle, I., and Gianoutsos, M. The cephalic David H. Song, M.D. vein: An aid in free TRAM flap breast reconstruction. Plast. Section of Plastic and Reconstructive Surgery Reconstr. Surg. 97: 71, 1996. University of Chicago Hospitals 7. Yanaga, H., Tai, Y., Kiyokawa, K., et al. An ipsilateral superd- 5841 South Maryland Avenue, MC 6035 rainaged transverse rectus abdominis myocutaneous flap for Chicago, Ill. 60637 breast reconstruction. Plast. Reconstr. Surg. 103: 465, 1999. [email protected] 8. Blondeel, P. N., Arnstein, M., Verstraete, K., et al. Venous DISCLOSURE congestion and blood flow in free transverse rectus abdomi- None of the authors has a financial interest in any nis myocutaneous and deep inferior epigastric perforator flaps. Plast. Reconstr. Surg. 106: 1295, 2004. of the products, devices, or drugs mentioned in this 9. Niranjan, N. S., Khandwala, A. R., and MacKenzie, D. M. article. Venous augmentation of the free TRAM flap. Br. J. Plast. Surg. 54: 335, 2001. REFERENCES 10. Civelek, B., Kargi, E., Akoz, T., et al. Turbocharge or super- 1. Kroll, S. S., and Baldwin, B. A comparison of outcomes using charge? Plast. Reconstr. Surg. 104: 1303, 1998. three different methods of breast reconstruction. Plast. Re- 11. Hallock, G. Simplified nomenclature for compound flaps. constr. Surg. 90: 455, 1992. Plast. Reconstr. Surg. 105: 1465, 2000.

Contacting the Editorial Office To reach the Editorial Office, please use the following contact information: Plastic and Reconstructive Surgery Rod J. Rohrich, M.D., Editor-in-Chief St. Paul’s Hospital 5909 Harry Hines Boulevard Room HD01.544 Dallas, Texas 75235-8820 Tel: 214-645-7790 Fax: 214-645-7791 E-mail: [email protected]

854 EXPERIMENTAL

Intrinsic Axial Vascularization of an Osteoconductive Bone Matrix by Means of an Arteriovenous Vascular Bundle

Elias Polykandriotis, M.D. Background: The purpose of this study was to generate an autonomously vas- Andreas Arkudas, M.D. cularized hard-tissue construct suitable for microsurgical transfer. The effector Justus P. Beier, M.D. of vascularization was an arteriovenous bundle inserted into a specially designed Andreas Hess, Ph.D. channel in the matrix. The authors also evaluated corrosion cast and intravital Peter Greil, Ph.D. magnetic resonance angiography as methods for monitoring and quantifying Thomas Papadopoulos, M.D. the angiogenic response. Jurgen Kopp, M.D. Methods: Thirty inbred male Lewis rats were divided into two groups. In both Alexander D. Bach, M.D. groups (n ϭ 15), a disk of processed bovine cancellous bone matrix was placed Raymund E. Horch, M.D. into an isolation chamber. In group A, a ligated arteriovenous bundle was Ulrich Kneser, M.D. inserted into the biogenic matrix as a vascular carrier. In group B, there was no Erlangen, Germany vascular carrier. At 2, 4, and 8 weeks after implantation, four constructs per group were evaluated by means of histology and histomorphometry and one by scanning electron microscopy of vascular corrosion casts. Micro–magnetic res- onance angiography was used for intravital evaluation of the vascularized ma- trices. Results: Vascular density was higher in group A. The capillary network in group A displayed a higher degree of maturation, with organization into vessels of different orders. Both the sprouting and intussusceptive modes of angiogenesis could be documented. Micro–magnetic resonance angiography showed a pa- tency rate of approximately 75 percent in the bundle. Conclusions: The authors zeroed in on the issue of vascularization. The results might provide a basis for further investigations on induction of bone formation in axially prevascularized matrices. Axially vascularized bone substitutes might solve issues of availability in mass and form and provide perfusion autonomy in sites of impaired circulation. (Plast. Reconstr. Surg. 120: 855, 2007.)

uring the past decade, there has been results and gave some further insight into the extensive research on biomaterials and interaction of biomaterials with a complex bio- Dtheir biomimetic properties.1 After in logical system such as an entire organism. Mean- vitro evaluation, constructs derived from these while, vascularity and cellularity are considered matrices were introduced into animals for in vivo core processes toward biointegration and spe- evaluation. Subcutaneous,2 intraabdominal,3,4 cific function. Tissue engineering research is ori- and intramuscular5 implantation of different ented toward strategies potentiating differentia- types of cell-seeded constructs provided valuable tion and enhancing angiogenesis. Vascularity has special significance for applica- From the Departments of Plastic and Hand Surgery, Surgical tions in the field of reconstructive surgery. Free Pathology, and Pharmacology and Toxicology, University of vascularized tissue transfer into compound de- Erlangen Medical Center, and Institute of Materials Science, fects is a common scenario after traumas with Glass, and Ceramics, University of Erlangen. 6 Received for publication December 2, 2005; accepted April segmental tissue loss and osteitis and after ex- 17, 2006. tensive tumor resection and subsequent Presented in part at the Second International Conference on radionecrosis.7 In these cases, good intrinsic Tissue Engineering, in Crete, Greece, May 22 through 27, blood perfusion of the tissue transplant is man- 2005. datory; even more so when bone replacement is Copyright ©2007 by the American Society of Plastic Surgeons required in the setting of segmental osseous de- DOI: 10.1097/01.prs.0000277664.89467.14 fects with concomitant soft-tissue damage. With

www.PRSJournal.com 855 Plastic and Reconstructive Surgery • September 15, 2007 the use of free vascularized compound flaps, vascularized bone substitutes. Transformation of several grave conditions are now amenable to a these prevascularized solid matrices into bioarti- surgical therapy that is likely to not only save the ficial bone tissue either by use of osteoinductive extremity but also preserve functionality.8,9 proteins or by injection of osteogenic cells will The actual effectors of repair and remodelling be the subject of subsequent studies. of bone are the cellular components (i.e., the osteoblasts and the osteoclasts). Thus, for a bio- MATERIALS AND METHODS material to become bioartificial bone, the leap is Experimental Design and Groups the transition to cellularity. Cellularity can be Animals with a processed bovine cancellous achieved by cell loading of these constructs be- bone matrix containing an arteriovenous bundle fore implantation, as with three-dimensional cul- 10 were incorporated into group A, whereas group B ture systems or, alternatively, it can be induced was composed of animals with a construct void of after implantation with the use of osteoinductive 11,12 vascular carrier. Each group contained 15 animals. factors. In both strategies, adequate vascular- The explantation intervals were 2, 4, and 8 weeks ization of the construct is imperative; no given after the initial operation for both groups. De- cell can ever survive if it is situated farther than ␮ 13–16 tailed analysis of the different subgroups is pro- 200 m from a blood vessel. Established re- vided in Table 1. constructive surgical concepts for free flap fabrication17 can be used for prevascularization Animals and neovascularization of tissue blocks either before cell seeding or concomitant with implan- A total of 30 inbred male Lewis rats weighing tation. approximately 250 g each were used in this study In the present study, we attempted to generate (Charles River, Sulzfeld, Germany). The experi- a vascularized construct suitable for microsurgi- mental protocol was approved by the interinstitu- cal transfer based on the principle of an arterio- tional academic committee for animal studies and venous bundle as the vascular carrier within a the local authorities. The animals were fed stan- solid porous matrix. The arteriovenous bundle dard rat chow and tap water ad libitum. They were has been described before as an effective means kept on a 12-hour light/dark cycle. of intrinsic vascularization.18,19 Special attention was paid to the morphology of the neovascular Tissue Isolation Chamber network and the kinetics of angiogenesis. An A cylindrical Teflon chamber was con- innovative matrix design was used, optimized to structed by the Institute of Materials Research, accommodate the vascular bundle in a specially Division of Glass and Ceramics, University of designed channel. In the same study, we per- Erlangen. The chamber was composed of a basal formed corrosion cast and intravital nuclear plate (diameter, 15 mm) under a cylindrical magnetic resonance angiography as methods for shell (height, 6 mm; diameter, 12 mm) and an monitoring and quantifying the angiogenic re- upper cup (height, 2 mm; diameter, 14 mm). sponse. This is the first step toward creation of The basal plate had two peripheral perforations

Table 1. Groups and Study Design* Histology Corrosion Cast MRI Weeks after Implantation (no. of constructs) (no. of constructs) (intravital) Group A (AV bundle) 2 4 (1) 1 0 4 4 (2) 1 0 8 4 (1) 1 4† (1) Group B (control, no vascular carrier) 2410 4410 8414† MRI, magnetic resonance imaging; AV, arteriovenous. *Thirty animals were divided into two groups (n ϭ 15). In group A, an arteriovenous bundle was used as the vascular carrier inside the matrix. In group B, the matrix was devoid of vascular carrier. For both groups, explantation intervals were 2, 4, and 8 weeks after the initial operation. Four animals per group and explantation interval were evaluated by histology and histomorphometry. Corrosion cast was performed on six and micro–magnetic resonance imaging on eight constructs of the different subgroups. †Animals survived and were incorporated into the corresponding histologic evaluation subgroup (in parentheses) constructs displaying partial thrombosis.

856 Volume 120, Number 4 • Vascularization of Bone Matrix

Fig.1. (Left)Theisolationchamberwithadiameterof15mmandaheightof8mm.Thebasalplate(B)hadtwoperipheral perforations(P)forstabilizationonthefasciaofthemedialmusculatureofthethigh.Afterclosureofthelid(L)onthetop, the only communication to the surrounding tissues is a proximal aperture for entrance of the arteriovenous bundle. (Right)Schematicrepresentationoftheconstructandthelevelsofevaluation.Histologicspecimenswereobtainedfrom three planes: proximally (1) adjacent to the entrance of the bundle (A, V) into the matrix (M), centrally (2), and distally (3). Planes 1 and 3 were 2.5 mm proximal and distal to the central plane (2). Every section was subdivided into nine areas: two digital photographs were obtained from each of these areas and the number of black-stained capillary lumina was documented. The vessels entered the matrix into a specially drilled central canal (C). for stabilization on the fascia of the medial mus- cular bundle was inserted into the xenogenic bone culature of the thigh (Fig. 1, left). matrix. The vessel-bone complex was placed in the isolation chamber. Processed Bovine Cancellous Bone Construct In group B (control group), a chamber contain- ing the matrix was inserted subcutaneously into the The matrix was composed of processed bo- medial thighs of the rats without any vascular axis vine cancellous bone (Tutogen Medical AG, inside. All animals received 0.2 ml benzylpenicillin- Neunkirchen, Germany). The pore size of the ma- benzathine (Tardomycel; Bayer, Leverkusen, Ger- trix was 400 to 1000 ␮m, with a porosity of 65 to many), buprenorphine (0.3 mg/kg rat weight) 80 percent rendered acellular and nonantigenic (Temgesic; Essex Chemie AG, Luzern, Switzerland), by a standardized procedure. Canals for future and heparin (80 IU/kg) (Liquemin; Ratiopharm, injection of gel-immobilized osteoblasts were in- Ulm, Germany) postoperatively. cluded in the matrix design. The matrix was a disk 9 mm in diameter with a channel along its long Explantation axis. The channel was elliptical on cross-section All explantations were performed under gen- (2 ϫ 3 mm), allowing for optimal accommodation eral anesthesia with intraperitoneal injection of of the arteriovenous bundle (Fig. 1, right). xylazine (Rompun, 24 mg/kg; Bayer, Leverkusen, Germany) and ketamine (Ketavet, 80 mg/kg; Surgical Procedures Parke Davis, Morris Plains, N.J.; dosage, 0.1 ml/ All implantation procedures took place under 100 g). Before explantation, the aorta and inferior general anesthesia with isoflurane (Baxter, vena cava were exposed through a median incision Unterschlei␤heim, Germany). In group A (arte- from the xiphoid process to the pubic symphysis. riovenous bundle), the right femoral vessels and The aorta was then cannulated through a 24- nerve were exposed by means of a longitudinal gauge catheter and the inferior vena cava was sev- incision from the inguinal ligament to the knee. ered. Then, the lower extremities were perfused The sheath of the neurovascular bundle was with the India ink or the methylmethacrylate mix- opened over the nerve, and the artery and vein ture. were dissected from the femoral nerve but were left connected to each other by connective tissue. India Ink Injection They were then ligated at their bifurcation at the This method was a modification of that used by popliteal level and transected. After that, the vas- Brey et al.20 After catheterization of the distal de-

857 Plastic and Reconstructive Surgery • September 15, 2007 scending aorta, the rats were perfused with ap- aging investigation, the animals were anaesthe- proximately 200 ml of heparinized Ringer’s solu- tized using isoflurane. The measuring period was tion (100 IU/ml, 37°C) until the returning fluid approximately 90 minutes. The animals recovered from the severed inferior vena cava was clear. The quickly and were later killed for histologic exam- caudal vascular system was perfused with 20 ml of ination. a 5% gelatine solution (Gelatine-Gold, 180 bloom; Carl Roth GmbH, Karsruhe, Germany), 4% Man- Corrosion Cast Technique nitol (D-Mannit; Neolab, Heidelberg, Germany), After cannulation of the aorta, the vascular and 50% v/v India ink in 37°C. The rat was placed system of the rat was rinsed with approximately 200 in –20°C for approximately 30 minutes and the ml of heparinized Ringer’s solution (100 IU/ml) un- bone constructs were fixed in a 3.5% formalin der hydrostatic pressure between 80 and 100 solution. mmHg until fluid escaping from the severed in- ferior vena cava was clear. The system was then Histology rinsed with 10 ml of half-strength Karnovsky so- After fixation in 3.5% formalin for 24 hours, lution (0.25% glutaraldehyde, 0.25% paraformal- the constructs were rinsed in water and left for dehyde, and 0.1 M Na-cacodylate buffer adjusted decalcification in ethylenediaminetetraacetic acid to a pH of 7.2). The caudal vascular system was for approximately 10 to 14 days. After that, the perfused with 20 ml of a methylmethacrylate resin specimens were dehydrated in graded ethanols in a mixture of 4:1 prepolymerized oligomer to and sectioned in three equal planes perpendicular methylmethacrylate monomer (Sigma Aldrich to the vascular carrier. Finally, the four segments Chemie GmbH, Munich, Germany) and benzoyl were embedded in paraffin and thin sections were oxide as a catalyst (Mercox; Ladd Research Indus- sampled: proximal pole, middle of the construct, tries, Burlington, Vt.) using a method described by and distal pole. Specimen thickness was set to 5 Lametschwandtner et al.21 ␮m, and hematoxylin and eosin stains were per- The rat was left for at least 6 hours in a warm formed using a fully automated process (Jung water bath (50°C). During this step, called “tem- Auto Stainer XL; Leica Microsystems, Nussloch, pering,” the resin was allowed to polymerize fully Germany). into the polymethylmethacrylate vascular replica. The construct was then left for 12 hours in 7.5% Magnetic Resonance Angiography sodium hydroxide at 60°C. The cycle was repeated three times. Decalcification was achieved by leav- The equipment used was a 4.7-T Bruker Bio- ing the processed bovine cancellous bone matrix Spec scanner (Bruker BioSpin, Rheinstetten, Ger- in 2.5% hydrochloric acid solution at room tem- many) with a scanner bore of 40 cm. Homogenous perature for 12 hours. For removal of the calcium excitation was facilitated by a whole-body birdcage rests, the vascular cast was placed into a 5% formic resonator. For maximal signal-to-noise ratio, a acid solution for 15 minutes. Final drying was per- 3-cm surface coil located directly above the vas- formed by lyophilization. The vascular replicas cularized matrix was used as the receiver coil. An- were investigated under scanning electron micros- giographic data sets were acquired using a non- copy and were then denuded under a dissection triggered three-dimensional inflow technique microscope for exposure of the central vascular (flow-compensated gradient echo sequence; ex- axis and the luminal sprouts. cited slab dimensions were 25.6 ϫ 25.6 ϫ 25.6 mm, measured matrix dimensions were 256 ϫ 256 ϫ 64 mm, TR ϭ 40 msec, TE ϭ 4.9 msec, four averages, Morphometric Analysis with a flip angle of 40 degrees). The MRIan soft- Cross-sections were taken from the proximal, ware (www.biocom-online.de) was used for evalu- middle, and distal segments of the processed bo- ation of volume data sets and AMIRA software vine cancellous bone construct (Fig. 1, right). The (www.mc.com/tgs) was used for visualization. In proximal and distal planes were chosen symmet- data sets acquired by the magnetic resonance in- rically at 2.5 mm from the central plane, which in flow technique, blood flow from vessels and per- turn had to be perpendicular to the vascular axis fused regions in general correspond to high signal itself and represented the point of maximal cross- intensities (bright voxels). These high-intensity re- section of the matrix (Fig. 1, right). All cross-sec- gions can be visualized three dimensionally using tions were divided into nine equal sectors. Two so-called maximum intensity projections and iso- randomly selected images of each sector were ac- surface renderings. For magnetic resonance im- quired with a Leica microscope and digital camera

858 Volume 120, Number 4 • Vascularization of Bone Matrix under 200ϫ magnification. The images were eval- 2-week groups, none of the constructs showed uated by two independent and blinded observers. black staining (vascularization) at the distal pole. The number of vascular lumina per field was doc- However, there was some dark staining at the prox- umented, and mean values were calculated for any imal pole of three of four constructs from group single construct. A (AV bundle group). That was not the case in group B (control group). Statistical Analysis In the 4-week groups, there was increased The normal distribution of the counted num- staining of the matrices. Two constructs from ber of vascular lumina per field was assessed with group A showed dark coloration even at the distal the method of Kolmogorov-Smirnov with Lillief- pole. In the other two, there was dark coloration ors correction. The experimental design could be in the proximal segment but not farther from the defined as a two-way factorial design (treatment by middle of the construct. In group B (control), time period) with three levels of nested observa- there was dark pigmentation at the proximal pole tions. A three-way analysis of variance was per- in two of the disks, whereas the other two showed formed with treatment, time periods, and planes no staining at all. as factors and the computation of interaction In the 8-week groups, there were similar re- terms. Values are given as mean Ϯ SD. The sig- sults. In group A, three of the four constructs nificance level was set at ␣ ϭ 0.05. showed dark coloration throughout the entire construct (Fig. 2, left). In the fourth construct, the RESULTS black dye was visible near the proximal aperture and in the central segments. In group B, there was Experimental Animals moderate staining at the proximal pole of all four All animals survived throughout the entire constructs (Fig. 2, right). length of the experiment and tolerated anesthetic In all constructs of group A (arteriovenous procedures well; there were no major postopera- bundle), the vessels emerged from the depth of tive complications such as hematomas, wound de- the matrix. In the control groups, there was a hiscence, or infection. Perfusion of the extremi- continuity of black vessels from the opening of the ties was undisturbed at any time. chamber toward the distal portions. Macroscopic Observations Histologic Analysis After India ink perfusion, at the time of ex- The matrix stained intensely for eosin because plantation, the constructs were investigated for of the remaining extracellular matrix of the pro- evidence of successful vascularization. In the cessed bovine cancellous bone matrix, with

Fig.2. (Left)GroupA(arteriovenousbundle).Neocapillariesemergefromthecoreoftheconstruct,wherethevascularaxislies (intrinsic vascularization). The matrix is arborized uniformly with a dense neovascular network. C, isolation chamber; M, matrix; B, arteriovenous pedicle entering the matrix proximally. (Right) Group B (control). Angiogenesis propagated slowly from the proximal aperture of the isolation chamber toward the far distal end of the matrix. The matrix was only partially filled at its proximal portion with neocapillaries originating from the aperture of the isolation chamber, “from outside” (extrinsic vascu- larization).

859 Plastic and Reconstructive Surgery • September 15, 2007

Fig.3. Tissueformationintheporousmatrix(histologichematoxylinandeosinstainingandIndiainkinjection;below,right,proximal plane; other pictures, distal plane. (Above, left) Group A (arteriovenous bundle) at 2 weeks. Neovascular outgrowth from the patent arteriovenous axis is already evident at the central portions of the matrix. The vessels emerge “from within” (intrinsic vascularization). Pores at the periphery do not contain any fibrovascular tissue at this time (12.5ϫ magnification). (Above, right) Group B at 2 weeks. Virtuallynoformationofvascularizedtissueisevidentinmatricesfromthecontrolgroup(groupB)atthistime(12.5ϫmagnification). (Center and below, left) Group A at 8 weeks. Almost the entire matrix is occupied with vascularized tissue emerging from the cen- ter toward the periphery. Morphologically, there is formation of loose fibrovascular tissue around numerous capillaries of variable caliber. Variability in luminal diameter implicates high level of maturity of the neovascular network (center, left 12.5ϫ magnification; below, left 100ϫ magnification). (Center and below, right) Group B at 8 weeks. In contrast, in group B (control), tissue generation propagated slowly and failed to occupy the entire matrix. The newly formed tissue at the proximal parts of the matrix (below, right) occurred in parts with an inflammatory character and with granulocyte infiltration (center, right, 12.5ϫ magnification; below, right, 100ϫ magnification).

860 Volume 120, Number 4 • Vascularization of Bone Matrix

Fig.4. MorphologyofthevascularaxisingroupAat8weeks(histologichematoxylinandeosinstainingandIndiainkinjection, distal plane). (Left) Even a partially thrombosed vascular pedicle with an occluded artery induces significant tissue within the porous matrix (A, distally thrombosed femoral artery; V, patent femoral vein; C, capillaries at the distal portion of the implant; 12.5ϫmagnification).(Right)Intimalhyperplasiaarterycausedbyhighpulsatilepressureonthearterialsideafterdistalligation (A, artery; V, vein; 40ϫ magnification). minute empty round spaces representing the sites inflammatory reaction (Fig. 3, below, right). There of the osteocytes before processing. Within the was no sign of osteogenesis under vascularized or pores of the matrix, there was newly formed vas- nonvascularized conditions. cularized tissue with fibrocytes, loose connective tissue, and vessels that stained black because of the Morphometry India ink gel (Fig. 3). In the 2-week groups, there were marked dif- In group A, the vascular axis was filled with ferences in terms of vascular density and area cov- either India ink or erythrocytes, depending on the ered with highly vascularized loose connective tis- patency or thrombosis of the vessels. Partial distal sue. Group A (bundle) displayed a higher capacity thrombosis of the pedicle could be observed in for angiogenesis, with 0.87 Ϯ 1.02 vessels per field four of 12 constructs from group A but only at the of view, as opposed to 0 Ϯ 0 in the control group outmost distal planes. A vivid angiogenic response (group B). was evident up to the level where both or one of Similar results could be obtained in the 4-week the vessels (usually the vein) remained patent subgroups, with 7.38 Ϯ 9.61 (group A) versus (Fig. 4, left). In the 8-week group, we could observe 3.38 Ϯ 6.77 (group B), and in the 8-week sub- a marked intimal hypertrophy of the arterial wall. groups, with 9.84 Ϯ 10.88 (group A) and 2.55 Ϯ Vascular alterations of the vein were not as prom- 3.20 (group B). The results are displayed graph- inent (Fig. 4, right). In the constructs with partial ically in Figure 5. thrombosis, there were some morphologic Overall, in group A (arteriovenous bundle), changes of the angiogenic response distal to the there was a steady increase in vascular growth over level of partial occlusion with inflammatory com- the different time subgroups from weeks 2 to 8. ponents present. The fibrovascular growth at Such was not the case in group B (control). These patent segments was characterized by loose con- results could be confirmed by a three-factor anal- nective tissue of low cellularity and high capillary ysis of variance, where group (F ϭ 6.0, p ϭ 0.017) density (Fig. 3, below, left). and time (F ϭ 4.8, p ϭ 0.012) were identified as In group B, there was a limited angiogenic significant factors. response. In the 4 and 8 week subgroups, there was tissue generation only at the very proximal parts of the construct near the orifice of the isolation Corrosion Casts chamber. The tissue elements here were a mixture In group A, under 50ϫ to 100ϫ magnification, of polymorphonuclear infiltration with vascular there was a considerable increase in volume of elements and a fibrotic reaction resembling an arborization over time. The neovascular network

861 Plastic and Reconstructive Surgery • September 15, 2007

applied for maturation and remodeling. Under 500ϫ to 1000ϫ magnification, there were marked ultrastructural differences between the arterial and venous sides of the neovascular network. The arteries and arterioles displayed spindle-like im- pressions arranged parallel to the long axis of the vessels, implying elongated endothelial cells (Fig. 6, below, right). On the contrary, on the venous parts of the circulation, the impressions of the nuclei of the endothelial cells were randomly ar- ranged and acquired a rather circular shape. Plas- tic strips depicting plastified pericytes and circular impressions implicating the presence of flow-reg- ulating structures were further indications of a Fig. 5. Quantification of vascularization. In group A (arterio- highly evolved vascular network. Again, the vas- venous bundle), there was a significant and steady increase in cular replicas in group B did not display any axial vascular growth over time. This was not the case in group B. Each differentiation. bar represents 216 nested measurements in three standardized ϭ Ϯ planes of four constructs (n 4). Values are given as mean SD. Magnetic Resonance Angiography Micro–magnetic resonance imaging was used concentrated along the patent arteriovenous bun- to identify patent arteriovenous bundles before dle (Fig. 6, above, left). Patency could be assessed explantation and to perform flow measurements. by microdissection of the vascular replica to ex- From four constructs measured in group A (arte- pose the central arteriovenous axis. All three spec- riovenous bundle), three were identified as imens were patent. patent. This finding could be confirmed on ex- In the control group, there was merely a vas- plantation and histologic examination. The arterio- cular ingrowth from the orifice of the chamber. venous bundle could be readily visualized in the rest The capillaries originated from vessels outside the of the constructs. However, neocapillary growth in chamber, such as the subdermal plexus of the the matrix could not be demonstrated because of thigh or alternatively the inguinal fat pad perfused limitations in resolution. The patent arteriovenous by the pelvic artery. The pattern was multidirec- bundle could be monitored throughout the ex- tional, without an axial component (Fig. 6, above, periment. In the control animals, no vessels or right). capillaries could be detected in any of the four Under 250ϫ to 500ϫ magnification, multiple constructs investigated. Vessels in the subdermal hot spots of ongoing angiogenesis could be iden- plexus, right beneath the surface coil, and other tified, as displayed by numerous neocapillary major vessels, such as the pelvic artery, were sprouts (Fig. 6, center, left). Alternatively, non- readily displayed (Fig. 7, below). sprouting angiogenesis in the form of “dichoto- mization” or “interstitial bridging” could be seen, DISCUSSION representing the intussusceptive form of angio- Studies on vascularization of bioartificial bone genesis (Fig. 6, center, right). were conducted as early as the advent of bone After 8 weeks, the neovascular network showed tissue engineering itself.22 Because angiogenesis a high degree of remodeling, with a hierarchical meets inflammation on the preinflammatory organization of vessels into different orders. The stage,23,24 in vivo studies on reaction of adjacent density of capillaries did not increase, but the pres- tissues inevitably involved the evaluation of the ence of closed arches indicated formation of a angiogenic response as well.25 Soon it became ev- capillary loop. After preparation, the arterio- ident that vascularization potentiated osseointe- venous bundle displayed minute fistulas between gration, osteoconduction, and osteoinduction of artery and vein. The presence of these microfis- bioartificial bone substitutes.26 tulas coincided with the patency of the bundle Several in vitro strategies showed promising (Fig. 6, below, left). results. Mooney and Mikos27 used co-cultures of In group B, the angiogenic phenomena osteogenic and endothelial progenitor cells to (sprouts and interstitial bridging) could also be populate three-dimensional matrices and pro- identified but to a far lesser extent. The same duce capillaries in vitro. In this case, preexisting

862 Volume 120, Number 4 • Vascularization of Bone Matrix

Fig. 6. Micromorphology of vascular replicas at 8 weeks (scanning electron microscopy). (Above, left) Group A (arteriovenous bundle). Axial pattern of vascularization with arborization around the arteriovenous bundle (ar- rows). (Above, right) Group B (control). Random pattern of neovascularization from the orifice of the isolation chamber. (Center and below) Group A (arteriovenous bundle). (Center, left) Sprouting angiogenesis. Numerous neocapillary sprouts (arrows) in a “hot spot,” an area of high angiogenic activity. (Center, right) Intussusceptive angiogenesis. Generation of new capillaries through dichotomesis of existing vessels (arrows). (Below, left) Mi- crofistulas between the femoral artery and vein ensure initial patency of the arteriovenous bundle (arrows). (Below,right)Theendothelialcellsonarteriesdisplayadistinctorientationparalleltobloodflowasdemonstrated by spindle-like impressions of their nuclei in the corrosion cast.

863 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 7. Intravital magnetic resonance imaging. (Above) Group A (arteriovenous bundle) at 8 weeks. (Above, left) The vascular bundle (asterisk) could be demonstrated by using the inflow technique. Bright voxels were visualized by means of isosurface rendering for three-dimensional reconstruction of the bundle in the matrix. (Above, right) Perfusion originating from the vascular axis (asterisk). Arrows indicate the subdermal plexus directly under the surface coil. (Below) Group B (control) at 8 weeks. The supplementary surface coil poten- tiated vivid visualization of the subdermal vascular plexus and the muscular plexus of the adductors of the medial thigh of the rat. In contrast, the matrix appears devoid of perfusion. capillaries enhanced the angiogenic front after in pand its vascular network into the construct in vivo implantation. The interactions between en- time for an adequate amount of cells to survive dothelial cells and osteoblasts in vitro were as- and ensure physiologic function of the engi- sessed in previous works of the authors on the neered tissue block. These concepts showed co-culture spheroid model.28 In other studies, ma- promising results, especially when adequate local trices loaded with inducers of neovascularization conditions with rich perfusion were present and such as vascular endothelial growth factor and the volume-to-surface ratio of the constructs was basic fibroblast growth factor were evaluated,29,30 kept low (i.e., small constructs in healthy recipi- and there were even some scarce attempts with ents). This mode of angiogenesis from the outside cells transfected with angiogenic factors.31,32 was termed extrinsic vascularization.33 This term All of these approaches were based on the stood in opposition to the intrinsic mode of an- assumption that the surrounding tissue will ex- giogenesis preserved for vascularization from

864 Volume 120, Number 4 • Vascularization of Bone Matrix within the tissue substitute by inserting a func- distant site as a compound prefabricated flap. This tioning vessel in its core. modality of flap prefabrication has been already This latter mode of vascularization has been used in the clinical setting.39,40 The flap can be applied in a plethora of different experimental rotated into an adjacent site as a pedicled tissue settings with different types of vascular carrier. A block or it can be transplanted into a distant area popular configuration is that of an arteriovenous by standard microsurgical techniques as a free loop with or without interposition of a venous flap. Second, the construct can be fully suspended autograft. Since its introduction in 1979,34 it has on the vascular pedicle during manipulations such been used widely in rats18,35 for generation of new as secondary cell loading without interrupting per- fibrovascular tissue. Although it offers excellent fusion from the core. angiogenic characteristics, its applicability is lim- The production of fibrovascular tissue dem- ited by the elaborate microsurgical skills required onstrated in the histologic specimens, the increase for the construction of the arteriovenous shunt. In in the number of capillaries shown through his- other investigations, a vascular pedicle in a flow- tomorphometry, and the increased arborization through pattern was placed within a bone graft displayed by the microvascular replicas confirmed and successfully generated ectopic vascularized that a vascular carrier inserted into the solid ma- 36 bone. Bone morphogenetic proteins were also trix can provide for enhanced neovascularization, 37 used to bring about ossification of a periosteal even in the case of partial thrombosis at the very island flap. The model was tested successfully on 38 distal segments of the pedicle. Obviously, the main rats with segmental bone defects. However, the mechanism for distal thrombosis was a vascular use of bone morphogenetic proteins harbored the overload being presented to the distal circuit be- problem of uncontrolled heterotopic ossification. cause of the distal ligation and the transfer into a In an attempt to develop a new strategy in- solid matrix. The flow in the distal vessels did not cluding intrinsic vascularization of a matrix and exceed the “critical thrombotic threshold level,” 41 subsequent seeding with bone-specific cells, we so that stagnating blood elements organized into investigated the distally ligated vascular pedicle as a longitudinal thrombus. In previous studies with a means of prevascularization of a solid porous nonsolid matrices, the bundle had also performed construct. Processed bovine cancellous bone was well in terms of vascular patency.18 Proximally, the chosen as the material because it is already ap- presence of microfustulas between the arterial proved for clinical use and displays suitable me- chanical properties for osteosynthetic fixation in and the venous limb obviously allowed for a min- osseous lesions. In previous studies conducted by imal initial flow and gave rise to an arteriovenous the authors, processed bovine cancellous bone circuit through the process of arteriogenesis. Par- was evaluated in vitro by means of three-dimen- tial distal thrombosis of the pedicle was a phe- sional culture and was found to provide a suitable nomenon identified histologically and macro- biomaterial for adhesion and differentiation of scopically after India ink injection and did not primary osteoblasts.10 Furthermore, when im- influence the axial character of the vascularization planted into calvarial defects it exhibited good or the presence of new capillaries. That means biointegration, highly osteoconductive proper- there was still a patent artery and vein exiting the ties, and enhanced bone healing. The matrix itself isolation chamber and there were India ink–filled displayed no osteoinductive or osteogenic poten- capillaries around the thrombosed segment evi- tial whatsoever, neither after orthotopic implan- dently bypassing it. In the distant segments, the tation in the former studies nor after insertion of neovascularization proceeded along the disinte- the arteriovenous bundle during the present in- grating thrombosed vessels. There could be two vestigation. This fact was favorable insofar as it different factors leading to this phenomenon. qualified the matrix for later studies on the effi- First, the inflammation around the thrombosed cacy of cell loading as a bone-forming strategy. vessels brought about an angiogenic response, be- This study confirmed the assertion that a vas- cause production of vascular endothelial growth cular carrier inserted into the solid matrix can factor is highly enhanced at the preinflammatory induce enhanced neovascularization. Further- level and platelets are a major source of the more, the hereby generated vascular tree has an factor.24 Second, apoptotic and dying cells have axial pattern and depends exclusively on the fem- been found to excrete basic fibroblast growth fac- oral vascular pedicle for perfusion. This offers a tor in high amounts, providing for an additional double advantage. First, insertion of a vascular angiogenic effect around a thrombus. These pro- carrier into a matrix renders it transferable to a cesses are similar to those of recanalization and

865 Plastic and Reconstructive Surgery • September 15, 2007 arteriogenesis after thrombus formation else- plete vascularization. In rats, ligation of the fem- where in the body.42 oral vessels does not compromise perfusion of the Scanning electron microscopy of corrosion extremity. Furthermore, distal ligation of the fem- casts is a powerful method for displaying the three- oral vessels in rats does not lead to complete dimensional characteristics of a microvascular net- thrombosis of the arteriovenous bundle, even if work. Both direct luminal sprouting and new cap- the vascular axis is inserted into a solid matrix. illary formation from the perivascular connective Thus, in the rat, this model has the advantages of tissue gave rise to a dense vascular network. By being relatively simple and yet clinically relevant. assessing the orientation of the impressions of the In large animals and humans, the choice of the nuclei of the endothelial cells on the methyl- vascular axis will be different and the issue of methacrylate cast, we could draw conclusions re- thrombosis can be overcome by a distal arterio- garding the flow characteristics in the individual venous fistula construction, a standard procedure vessels. In arteries, these impressions had the ap- in vascular surgery.41 Along with matrix modula- pearance of parallel spindles and the vascular wall tion, cell transplantation into prevascularized ma- was smooth and round. In contrast, the endothe- trices might develop into a major trend in the lial cells at the venous part of the circulation are years to come. In the future, bioartificial axially randomly arranged; the venous wall displays cir- vascularized bone tissue may be generated for clin- cular wrinkles. Variability in vascular caliber im- ical application in reconstructive surgery. Induc- plies a vascular network in the late remodeling tion of bone formation in prevascularized solid phase, where regression and persistence of capil- laries along with loop formation give rise to the matrices by means of injection of osteoblasts is typical hierarchy from artery to arteriole, precap- therefore the subject of ongoing research in our illary arteriole, capillary, postcapillary venule, and laboratory. Osteogenic bioartificial bone substi- venule draining into a vein. Connections between tutes harbor great potential for treatment of os- the two vessels in the arteriovenous bundle ensure seous defects because they will offer unlimited patency until a more extensive capillary intercon- availability, diminish donor-site morbidity, and nection is established. come in any needed form and size according to Magnetic resonance angiography is a nonin- the defect. First steps in this direction have been vasive method for assessing perfusion, and recent reported: vascularization of bioartificial bone sub- advances have increased its applicability in exper- stitutes by means of muscular flap prefabrication iments on angiogenesis with small animals. It of- is a clinical reality.5 Axial vascularization, as inves- fers two significant advantages. First, it potentiates tigated in the present study, might be a missing repeated serial measurements on the same animal link toward application of bone engineering con- in different time periods. Second, it represents a structs in vivo by rendering them able to resist means of monitoring that can be used in the clin- infections and promote bone healing in sites of ical setting after the biotechnology under investi- suboptimal soft-tissue conditions, with minimal gation is integrated into clinical routine. In the fu- donor-site morbidity. ture, magnetic resonance imaging will be able not only to display favorable perfusion characteristics Raymund E. Horch, M.D. Department of Plastic and Hand Surgery within a tissue-engineered construct but also to mon- University of Erlangen Medical Center 43 itor cell viability after cell transplantations. There- Krankenhausstrasse 12 fore, we attempted to relate this method to cor- 91054 Erlangen, Germany rosion casting and histomorphometry by India [email protected] ink, which are widely used techniques for assess- ment of vascular growth kinetics. ACKNOWLEDGMENTS This study was supported by research grants from the CONCLUSIONS University of Erlangen (ELAN Program and the IZKF) This study dealt with the vascular bundle as a and from Tutogen Medical, Inc. The authors thank Peter pattern of intrinsic vascularization of a solid ma- Reinhardt for support for the construction of the isolation trix. This vascular pattern offers an experimental chambers and A. Lametschwandtner for instruction in setting with great flexibility, because it does not the corrosion cast technique. They also thank T. Fey and require elaborate microsurgical techniques for E. Springer for the investigations using the scanning initial insertion into the construct. However, mi- electron microscope and Dr. U. Reulbach for support with crosurgical transfer remains an option after com- statistical analysis.

866 Volume 120, Number 4 • Vascularization of Bone Matrix

DISCLOSURE 19. Cronin, K. J., Messina, A., Knight, K. R., et al. New murine None of the authors has a financial interest in any model of spontaneous autologous tissue engineering, com- bining an arteriovenous pedicle with matrix materials. Plast. of the products, devices, or drugs mentioned in this Reconstr. Surg. 113: 260, 2004. article. 20. Brey, E. M., King, T. W., Johnston, C., et al. A technique for quantitative three-dimensional analysis of microvascular REFERENCES structure. Microvasc. Res. 63: 279, 2002. 1. Salgado, A. J., Coutinho, O. P., and Reis, R. L. Bone tissue 21. Lametschwandtner, A., Lametschwandtner, U., and Weiger, engineering: State of the art and future trends. Macromol. T. Scanning electron microscopy of vascular corrosion casts: Biosci. 4: 743, 2004. Technique and applications. Updated review. Scanning Mi- 2. Kneser, U., Voogd, A., Ohnolz, J., et al. Fibrin gel-immobi- crosc. 4: 889, 1990. lized primary osteoblasts in calcium phosphate bone cement: 22. Vacanti, C. A., Kim, W., Upton, J., et al. Tissue-engineered In vivo evaluation with regard to application as injectable growth of bone and cartilage. Transplant. Proc. 25: 1019, 1993. biological bone substitute. Cells Tissues Organs 179: 158, 2005. 23. Ito, A., Hirota, S., Mizuno, H., et al. Expression of vascular 3. Kneser, U., Kaufmann, P. M., Fiegel, H. C., et al. Long-term permeability factor (VPF/VEGF) messenger RNA by plasma differentiated function of heterotopically transplanted hepa- cells: Possible involvement in the development of edema in tocytes on three-dimensional polymer matrices. J. Biomed. chronic inflammation. Pathol. Int. 45: 715, 1995. Mater. Res. 47: 494, 1999. 24. Dvorak, H. F., Detmar, M., Claffey, K. P., et al. Vascular 4. Peter, S. J., Miller, M. J., Yasko, A. W., et al. Polymer concepts permeability factor/vascular endothelial growth factor: An in tissue engineering. J. Biomed. Mater. Res. 43: 422, 1998. important mediator of angiogenesis in malignancy and in- 5. Warnke, P. H., Springer, I. N., Wiltfang, J., et al. Growth and flammation. Int. Arch. Allergy Immunol. 107: 233, 1995. transplantation of a custom vascularised bone graft in a man. 25. Kirkpatrick, C. J., Krump-Konvalinkova, V., Unger, R. E., et Lancet 364: 766, 2004. al. Tissue response and biomaterial integration: The efficacy 6. Yazar, S., Lin, C., and Wei, F. One-stage reconstruction of of in vitro methods. Biomol. Eng. 19: 211, 2002. composite bone and soft-tissue defects in traumatic lower 26. Vacanti, J. P., Langer, R., Upton, J., et al. Transplantation of extremities. Plast. Reconstr. Surg. 114: 1457, 2004. cells in matrices for tissue regeneration. Adv. Drug Deliv. Rev. 7. Rand, R., Maser, B., Dry, G., et al. Reconstruction of irradi- 33: 165, 1998. ated postpneumonectomy empyema cavity with chain-link 27. Mooney, D. J., and Mikos, A. G. Growing new organs. Sci. Am. coupled microsurgical omental and TRAM flaps. Plast. Re- 280: 60, 1999. constr. Surg. 105: 183, 2000. 28. Wenger, A., Stahl, A., Weber, H., et al. Modulation of in vitro 8. Langstein, H. N., and Robb, G. L. Reconstructive approaches angiogenesis in a three dimensional spheroidal coculture in soft tissue sarcoma. Semin. Surg. Oncol. 17: 52, 1999. model for bone tissue engineering. Tissue Eng. 10: 1536, 9. Lipa, J. E., Novak, C. B., and Binhammer, P. A. Patient- 2004. reported donor-site morbidity following anterolateral thigh 29. Murphy, W. L., Peters, M. C., Kohn, D. H., et al. Sustained free flaps. J. Reconstr. Microsurg. 21: 365, 2005. release of vascular endothelial growth factor from mineral- 10. Stangenberg, L., Schaefer, D. J., Buettner, O., et al. Differ- ized poly(lactide-co-glycolide) scaffolds for tissue engineer- entiation of osteoblasts in three dimensional culture in pro- ing. Biomaterials 21: 2521, 2000. cessed cancellous bone matrix: Quantitative analysis of gene 30. Perets, A., Baruch, Y., Weisbuch, F., et al. Enhancing the vas- expression based on real-time reverse transcription-polymer- cularization of three-dimensional porous alginate scaffolds by ase chain reaction. Tissue Eng. 11: 855, 2005. incorporating controlled release basic fibroblast growth factor 11. Reddi, A. Morphogenesis and tissue engineering of bone and microspheres. J. Biomed. Mater. Res. A 65: 489, 2003. cartilage: Inductive signals, stem cells, and biomimetic bio- 31. Totsugawa, T., Kobayashi, N., Okitsu, T., et al. Lentiviral materials. Tissue Eng. 6: 351, 2000. transfer of the LacZ gene into human endothelial cells and 12. Schmoekel, H., Weber, F., Schense, J., et al. Bone repair with human bone marrow mesenchymal stem cells. Cell Trans- a form of BMP-2 engineered for incorporation into fibrin cell plant. 11: 481, 2002. ingrowth matrices. Biotechnol. Bioeng. 89: 253, 2005. 32. Mayer, H., Bertram, H., Lindenmaier, W., et al. Vascular 13. Horch, R. E., Bannasch, H., and Stark, G. B. Transplantation endothelial growth factor (VEGF-A) expression in human of cultured autologous keratinocytes in fibrin sealant bioma- mesenchymal stem cells: Autocrine and paracrine role on trix to resurface chronic wounds. Transplant. Proc. 33: 642, osteoblastic and endothelial differentiation. J. Cell. Biochem. 2001. 95: 827, 2005. 14. Goldstein, A. S., Juarez, T. M., Helmke, C. D., et al. Effect of 33. Cassell, O. C., Hofer, S. O., Morrison, W. A., et al. Vascu- convection on osteoblastic cell growth and function in bio- larisation of tissue-engineered grafts: The regulation of an- degradable polymer foam scaffolds. Biomaterials 22: 1279, giogenesis in reconstructive surgery and in disease states. Br. 2001. J. Plast. Surg. 55: 603, 2002. 15. Greene, H. S. N. Heterologous transplantation of mamma- 34. Erol, O. O., and Spira, M. New capillary bed formation with lian tumors. Exp. Med. 73: 461, 1961. a surgically constructed arteriovenous fistula. Surg. Forum 30: 16. Folkman, J., and Hochberg, M. Self-regulation of growth in 530, 1979. three dimensions. J. Exp. Med. 138: 745, 1973. 35. Kneser, U., Polykandriotis, E., Ohnolz, J., et al. Engineering 17. Khouri, R., Upton, J., and Shaw, W. Prefabrication of com- of vascularized transplantable bone tissues: Induction of ax- posite free flaps through staged microvascular transfer: An ial vascularization in an osteconductive matrix using an ar- experimental and clinical study. Plast. Reconstr. Surg. 87: 108, teriovenous loop. Tissue Eng. 12: 1721, 2006. 1991. 36. Lee, J. H., Cornelius, C. P., and Schwenzer, N. Neo-osseous 18. Tanaka, Y., Sung, K. C., Tsutsumi, A., et al. Tissue engineering flaps using demineralized allogeneic bone in a rat model. skin flaps: Which vascular carrier, arteriovenous shunt loop or Ann. Plast. Surg. 44: 195, 2000. arteriovenous bundle, has more potential for angiogenesis and 37. 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a matrix and rh-BMP-2 (bone morphogenetic protein) in the 41. Dardik, H. The use of an adjunctive arteriovenous fistula in rat model. Mund Kiefer Gesichtschir. 4 (Suppl. 2): S454, 2000. distal extremity bypass grafts with outflow obstruction. In R. 38. Vogelin, E., Jones, N. F., Huang, J. I., et al. Healing of a Kempczinski (Ed.), The Ischemic Leg. Chicago: Year Book critical-sized defect in the rat femur with use of a vascularized Medical, 1985. P. 463. periosteal flap, a biodegradable matrix, and bone morpho- 42. Collinson, D. J., and Donnelly, R. Therapeutic angiogenesis genetic protein. J. Bone Joint Surg. (Am.) 87: 1323, 2005. in peripheral arterial disease: Can biotechnology produce an 39. Pribaz, J. J., Maitz, P. K., and Fine, N. A. Flap prefabrication effective collateral circulation? Eur. J. Vasc. Endovasc. Surg. 28: using the Љvascular craneЉ principle: An experimental study 9, 2004. and clinical application. Br. J. Plast. Surg. 47: 250, 1994. 43. Stabler, C. L., Long, R. C., Sambanis, A., et al. Noninvasive 40. Tark, K. C., Khouri, R. K., Shin, K. S., et al. The fasciovascular measurement of viable cell number in tissue-engineered con- pedicle for revascularization of other tissues. Ann. Plast. Surg. structs in vitro, using 1H nuclear magnetic resonance spec- 26: 149, 1991. troscopy. Tissue Eng. 11: 404, 2005.

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868 EXPERIMENTAL

A Novel In Vivo Model of Human Hemangioma: Xenograft of Human Hemangioma Tissue on Nude Mice

Yunman Tang, Ph.D., M.D. Background: Experimental models of human infantile hemangiomas are Wenying Liu, Ph.D., M.D. needed, although none of the current ones is ideal in representing the natural Song Yu, Ph.D., M.D. development of hemangioma. In this article, the authors present a nude mice Yong Wang, M.D. model of human hemangioma with serial morphologic findings on grafts. Qiang Peng, M.D. Methods: A specimen of rapidly growing hemangioma tissue was obtained Zhongxun Xiong, M.D. surgically from a 2-month-old boy and was cut into 96 pieces, which were Yonggang Wang, M.D. implanted subcutaneously into nude mice, six pieces each. During the 6-month Ting Wei, M.D. experimental period, gross view, hematoxylin and eosin staining, double im- Chengdu, People’s Republic of China munofluorescent labeling with mouse antihuman CD31 and fluorescein iso- thiocyanate–labeled rat antimouse CD34, and transmission electron micro- scopic observation were performed. Results: Eighty-one of the 96 grafts (84.4 percent) survived and grew during the second month to 3 to 4 months after transplantation, followed by gradual involu- tion. Histologic examination showed cellular edema, degeneration, and necrosis in the early stage. From approximately 30 days, cellular density increased and karyo- kinesis was identified at 45 days. At 2 months, the grafts were composed mainly of hemangioma tissue and signs of involution appeared. Thereafter, signs of involu- tion turned significant and the grafts were replaced with fibrofatty tissue. It was confirmed through double immunofluorescent labeling that the chief cellular components were endothelial cells of human origin. Findings on ultrastructural investigation were concordant with those on light microscopic observation. Conclusions: With human hemangioma tissue implanted into nude mice, an an- imal model was established successfully. The development of grafts after ischemia resembled the natural course of human infantile hemangioma. (Plast. Reconstr. Surg. 120: 869, 2007.)

nfantile hemangioma (usually abbreviated as human hemangioma is limited by intrinsic de- hemangioma), the most common tumor of fects (i.e., the models are not neoplasms at all, or Iinfancy, is a benign vascular neoplasm result- are not benign in nature, or are not in vivo). In ing from abnormal proliferation of endothelial this article, we provide a novel animal model of cells and angiogenesis. With high prevalence human infantile hemangioma by xenografting and embarrassed status in clinical treatment, the human hemangioma tissue onto immunodefi- original defect or detailed underlying pathogen- cient nude mice. As shown in serial morphologic esis is far from elucidated. In the attempt to investigations, most of the grafts were engrafted achieve a greater understanding of its behavior and revealed rapid growth after the ischemic stage, and the therapeutic effects of certain drugs, var- followed by gradual regression and replacement ious models of hemangioma have been with fibrofatty tissue. The development of the established.1–19 However, the value of these mod- xenografts after surviving ischemia resembled the els in representing the natural development of natural course of human infantile hemangioma.

From the Department of Pediatric Surgery, West China Hos- PATIENTS AND METHODS pital of Sichuan University. Tumor Procurement, Xenografting, Received for publication December 27, 2005; accepted April and Harvesting 2, 2006. The primary tumor was obtained surgically Copyright ©2007 by the American Society of Plastic Surgeons from a 2-month-old boy who was referred to our DOI: 10.1097/01.prs.0000277661.49581.c9 department for a rapidly growing mass in the

www.PRSJournal.com 869 Plastic and Reconstructive Surgery • September 15, 2007 waist. Informed consent was obtained from the osmium tetroxide. Dehydration was performed in parents for experimental investigations. The cu- a series of graded ethanols and finally in pro- taneous portion and obvious fibrofatty tissue were pylene oxide. The sections were embedded and removed from the specimen, and the remainder then stained with uranyl acetate and lead citrate. of the subcutaneous tumor was cut into small Photographs were taken using a transmission pieces of approximately 5 ϫ 4 ϫ 3 mm. Under electron microscope (H-600IV; Hitachi, Tokyo, anesthesia with intraperitoneal injection of 2.5% Japan). pentobarbital (45 mg/kg), 16 nude mice were implanted with the tumor pieces subcutaneously, RESULTS six pieces each. At 2, 3, 5, 7, 15, 30, and 45 days, Tumor-Loading Nude Mice and then once per month until the end of the experiment at 6 months, the grafts were harvested Before being killed, all of the nude mice were under anesthesia, three grafts each time. alive, except for one, which seemed to be dying, with a decrease of body weight and activity and Gross View and Measurement wrinkling of the skin at 5 months. At 1, 2, 3, 5, and 7 days after grafting, and then two times per week until the end of the third Gross View month, and then once per week until the end of Within 15 to 30 days after transplantation, 13 the sixth month, the grafts were observed with the grafts were found to be decreasing in size pro- naked eye and palpated for texture. The maximal gressively and had disappeared by month 2. Most length (a) of grafts and the perpendicular length of the remaining grafts survived and were altered (b) were measured four times per month with a in size, as shown in Figure 1. The size of the grafts sliding caliper. The volume (V) of grafts was esti- increased slightly during the first 2 weeks and then mated as V ϭ ␲/6 ϫ a ϫ b2.20 shrank a little over the next 2 weeks. During the second month, the grafts grew rapidly and Hematoxylin and Eosin Staining achieved their maximum size at 2 months, then slowly involuted, and at the end of experiment (6 The specimens were formalin-fixed and par- months), their size seemed stable at a level of affin-embedded. Four-micrometer sections were approximately one-third to one-half their primary deparaffinized and stained with hematoxylin and volume. eosin. Before transplantation, the hemangioma pieces were light red or white and were translu- Double Immunofluorescent Labeling cent. When transplanted into the host, the grafts The sections were deparaffinized, hydrated, and were pink and soft as observed from outside of the treated with peroxide solution for 15 minutes, fol- skin (Fig. 2, above, left). At 2 days, 21 of the 96 grafts lowed by a high-pressure retrieval protocol. After turned blue (one of them was harvested at 3 days) incubation in serum-blocking solution for 20 min- and then hardened at 5 days. From day 15 on, 18 utes, the slides were incubated with mouse antihu- of them gradually turned lighter in color and man CD31 monoclonal antibody (dilution, 1:100; softer in texture, and the other two were still hard Zhongshan, Beijing, China) overnight. The slides and the color turned lighter and they disappeared were then incubated for 1 hour with tetramethyl by the end of month 2. Most of the grafts (75 of rhodamine isothiocyanate–labeled goat anti- 96) remained pink and soft during the early stage, mouse immunoglobulin antibody (dilution, and 11 of them turned pale and vanished within 1:500; Molecular Probes, Eugene, Ore.) and flu- 2 months. The rest of these 75 grafts, except those orescein isothiocyanate–labeled rat antimouse harvested earlier, turned red during the second CD34 monoclonal antibody (dilution, 1:500; month (Fig. 2, above, right) and then gradually Santa Cruz Biotechnology, Santa Cruz, Calif.). Im- turned purple, and they remained soft. Such red ages were captured using a multiphoton confocal or purple grafts appeared fresh red when viewed microscope (Bio-Rad MRC-1042MP; BioRad, directly during harvesting. During the last 3 Hemel Hempstead, United Kingdom). months, the color of the grafts turned lighter again and eventually turned light yellow or pale Transmission Electron Microscopy (Fig. 2, below, right). Specimens for electron microscopic examina- During the entire experimental period, the tion were fixed with 3% glutaraldehyde and 0.2 M grafts were easy to recognize, and at harvesting, phosphate buffer, rinsed, and postfixed in 1% they were found wrapped with capsule and were

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Fig. 1. Development of graft size (mean Ϯ SE) and alteration of sample size with time.

Fig. 2. Gross views of grafts. (Above, left) Pieces of human hemangioma tissue grafted into nude mice on the subcutaneous layer. (Above, right) At 45 days. (Below, left) At 3 months, the graft was fresh red in color. (Below, right) At 6 months, the grafts shrank in size and appeared like fibrofatty tissue.

871 Plastic and Reconstructive Surgery • September 15, 2007 distinctive from the host tissue (Fig. 2, below, left). fibrous and/or fatty tissue (Fig. 3, below, right). In Fibrous capsule with a network of fine blood ves- addition, two grafts that decreased in size in the sels was first seen in grafts harvested at 3 days. early stage and were harvested at 7 and 15 days, Apparent blood vessels surrounding the grafts respectively, were proved to be necrotic tissue. could be recognized from outside the skin from the second week on. Double Immunofluorescent Labeling of Endothelial Cells Hematoxylin and Eosin Staining In the primary tumor, most of the cellular components were endothelial cells of human or- Under light microscopy, the primary tumor igin and stained red. The endothelial cells assem- was typical infantile hemangioma in the prolifer- bled in nests, and the capillary lumens were small ative phase. The parenchymal cells of the tumor and irregular (Fig. 4, above, left). assembled in nests or lobules, and there were mul- At 2 days, the structure of the grafts was tiple irregular capillaries within the nests or lob- similar to that of the primary tumor. At 3 days, ules (Fig. 3, above, left). few capillaries of mouse origin were found in the At 2 days after transplantation, the architec- margin zone and the human endothelial cells ture of hemangioma tissue was maintained, and were decreased in number (Fig. 4, above, center). cellular edema was evident. At 3 days, fibrous cap- At 5 days, some of the vessels were dilatated and sule was found surrounding the grafts, and sub- lined with flat human endothelial cells. At 7 to capsular hemorrhage was identified in a graft that 15 days, the number of human endothelial cells turned blue at 2 days. Tissue in the peripheral decreased further and they accumulated in lob- zone maintained features of hemangioma, and in ules (Fig. 4, above, right). At 30 days, the number the central zone, cellular density was low and the of human endothelial cells was still small, cells predominantly abutted the enlarged vessels. whereas in some lobules, the cellular density The interstitial substance was loose. At 5 days, the increased, and at 45 days, the cellular density of hemangioma tissue was distributed in lobules sep- human endothelial cells became the highest and arated by broad bands of hyaline degeneration. was even higher than that of the primary tumor Within the lobules, cells crowded together and (Fig. 4, below, left). In slides of grafts harvested at most of the capillary lumens were dilatated and 2 months, human endothelial cells were distrib- engorged with blood cells. Hyaline degeneration uted throughout the fields, whereas some blood was evident in the center of some lobules. At 15 vessels were dilatated and the cellular density days, coagulation necrosis was dramatic in the cen- was decreased. The vessels enlarged further and tral area and karyopyknosis, karyolysis, and cellu- the microscopic appearance of grafts became lar necrosis were common (Fig. 3, above, right). At sponge-like at 3 months (Fig. 4, below, center), 30 days, the hemangioma lobules grew in area and which was consistent with the appearance re- number. The intralobular cellular density in- vealed on hematoxylin and eosin staining. In creased and the capillary lumens were small. The later harvests, human endothelial cells de- areas of hemangioma further expanded and creased in number dramatically, and several re- karyogenesis was frequent in grafts harvested at 45 sidual blood vessels lined with flat human en- days (Fig. 3, center, left). At 2 months, hemangioma dothelial cells were recognizable (Fig. 4, below, tissue occupied almost the entire grafts, whereas right). the cellular density decreased and some capillaries were dilatated (Fig. 3, center, right). At 3 months, the grafts were sponge-like under light micros- Transmission Electron Microscopy copy. There were multiple dramatically dilatated Under transmission electron microscopy, en- blood vessel lakes and, within the trabecula, were dothelial cells with tiny lumens were the chief crowded cells and small-caliber capillaries (Fig. 3, components of the primary tumor. The endothe- below, left). In specimens harvested later, fibrous lial cells were plump and crowed together with tissue and fat tissue emerged and gradually sepa- intercellular tight junction. The nuclei were large, rated the hemangioma tissue into lobules again. with serrated karyolemma. Plasmalemmal vesicles Within the hemangioma lobules, signs of degen- were predominant and Weibel-Palade’s bodies eration were predominant, and residual capillar- were scarce. Microfilaments were found adjacent ies with dilatated lumens were scattered in the to the cellular membrane of the luminal side and fibrofatty area. In many grafts harvested at 4 to 6 multiple finger-like processes were present on the months, the fields were completely occupied by luminal membrane. The capillary lumens were

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Fig. 3. Light microscopic view of grafts (hematoxylin and eosin staining). (Above, left) The primary human hemangioma tissue. (Above,right)At15days,coagulationnecrosiscanbeobservedinthecentralarea.(Center,left)At45days,cellulardensityoftumoral endothelial cells was high, with evident karyogenesis (K). (Center, right) At 2 months, the microscopic appearance of the graft was typical hemangioma with some of the microvessels dilatated. (Below, left) At 3 months, the graft was sponge-like under light microscopy, with greatly distended blood vessels. (Below, right) At 6 months, signs of involution were evident, with a decrease of cellular density, deposition of fibrous tissue, and remaining dilatated microvessels (bar ϭ 100 ␮m). walled with few or single endothelial cell(s) and lum, and a decrease of mitochondrial crests in were oppressed by the plump cells into shallow number. At 5 days, the number of endothelial and irregular clefts (Fig. 5, above, left). cells was decreased. Perfect, round capillaries At 2 days, the architecture of grafts was sim- were found within the cytoplasm of some endo- ilar to that of the primary tumor, but there were thelial cells; therefore, the cells appeared ring- signs of cellular edema, such as dilatation of like (Fig. 5, above, right). Cellular necrosis and mitochondrion and endocytoplasmic reticu- interstitial collagen deposition were obvious. At

873 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 4. Double immunofluorescent labeling. Endothelial cells of human origin were stained red and those of mouse origin were stained green; red blood cells were double stained yellow. (Above, left) Primary human hemangioma tissue with nested en- dothelial cells of human origin. (Above, center) At 3 days, human endothelial cells decreased in density with a capillary of mouse origin located in the periphery. (Above, right) At 15 days, human endothelial cells survived in small numbers. (Below, left)At45 days, the density of human endothelial cells was high. (Below, center) At 3 months, the graft was sponge-like, with distended blood vessels and accumulation of tumoral endothelial cells within the trabeculas. (Below, right) At 6 months, remnant human endothelial cells (bar ϭ 10 ␮m).

15 days, endothelial cells were scattered with uniform karyoplasm to near normal flat cell lining background necrosis tissue, collagen, and inter- the lumen of dilatated blood vessels. At 3 months, stitial cells such as fibroblasts. The endothelial the cellular density of endothelial cells decreased cells were morphologically similar to those har- and there were greatly enlarged vessels lined with vested at 5 days and the organelles were near flat endothelial cells, and other endothelial cells normal. At 30 days, endothelial cells were as- were plump and crowded tightly in groups within sembled in small groups and the groups were the trabecula. At 4 months, the number of endo- surrounded by collagen bundles. Some of the thelial cells decreased further and the cells were endotheliocyte nuclei were large and the elec- scattered. Within some blood vessels, endovascu- tron density of karyoplasm was low. At 45 days, lar thrombopoiesis and organization were ob- the number of endothelial cells increased and served and the cellular membrane of the lining the cells were crowded tightly. Most of the nuclei endothelial cells was broken. Signs of cell death were large and the karyoplasm was uniform and were revealed, such as chromatin margination, light (Fig. 5, below, left). There were still large areas of interstitial tissue with prominent colla- karyorrhexis, cytoplasm pyknosis, and secondary gen deposition. At 2 months, interstitial compo- lysosome formation within the cytoplasm (Fig. 5, nents diminished and the population of endothe- below, right). Deposition of collagen and accumu- lial cells was high. The morphology of endothelial lation of fibroblasts were evident. At 6 months, cells varied from plump cell with large nucleus and endothelial cells were scarce and most of them

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Fig. 5. Transmission electron microscopy. (Above, left) Endothelial cell of primary human hemangioma with irregular and narrow intracellular capillary lumen. (Above, right) At 5 days, a ring-like endothelial cell was shown at the left lower corner. (Below, left) At 45 days, two endothelial cells were observed surrounding the irregular capillary lumen, within which a red blood cell was recognizable. (Below, right) At 4 months, signs of degeneration including collagen deposition, chromatin margination, and secondary lysosome formation were shown (bar ϭ 10 ␮m). were flat. Collagen fibers, fibroblasts, and adipo- ities (i.e., glucocorticoids, interferon, and surgery) is cytes were the chief components of the grafts. ideal, partly because the pathogenesis of hemangi- oma and the mechanism of its proliferation and triggering of apoptosis is far from clear. One of the DISCUSSION chief obstacles to exploring the pathogenesis is the Hemangioma is a benign vascular tumor arising scarcity of proper models for further research. For from proliferation of endothelial cells. It affects ap- many years, specialists have been attempting to es- proximately 10 percent of children, making it the tablish their own models of human “hemangiomas.” most common tumor of infancy. It generally appears Ritter reported in 1966 that cockscomb was used in within the first weeks postpartum, proliferates rap- 1 idly during the first year of life, and then spontane- research of “hemangioma” therapy with laser. As ously involutes over a period of several years. For hemangioma is a real tumor rather than a vascular most children with hemangioma, the lesions are malformation, this model was limited to investiga- small and pose no threat or complication, but some tions on the therapeutic effect of laser on certain 1,3 hemangiomas grow dramatically and destroy tissue, vascular malformations. Sato et al. reported that impair function, or even threaten life. Another prob- vascular tumors were induced with a 100 percent lem is whether it is necessary to interfere with and, success rate in BALB/c mice with subcutaneous in- if so, when, especially when the lesions are located jection of 1,2-dymethylhydrazine, and the tumors on the face, finger, breast, anus, and so forth. Un- resembled human kaposiform angiosarcoma in fortunately, none of the current therapeutic modal- morphology.4 On the basis of a hypothesis about

875 Plastic and Reconstructive Surgery • September 15, 2007 virus in the pathogeny of vascular tumors, polyoma- grew in number and formed neovessels. The cel- virus by itself and its active gene constituent PymT lular density and the proliferative activity of the (polyomavirus middle T antigen) were administered endothelial cells reached the peak level at 45 days. to animals and induced multifocal endothelial The proliferating endothelial cells were plump tumors.6–9 However, the tumors were malignant and and juvenile in ultrastructure and crowded to- invasive and the animals soon died of massive bleed- gether in clusters, and karyogenesis was frequent. ing and anemia. When cardiovascular researchers Capillary lumens were small and irregular. Such complained about the deleterious effect of angioma histologic findings were similar to those in human formation in vascular endothelial growth factor gene hemangioma in the proliferative phase. At ap- therapy of myocardial infarction,14 others were in- proximately 2 months, the number of endothelial spired and applied this technique to the establish- cells of human origin was the largest, the prolif- ment of an animal model of vascular tumors.15 Be- erative activity was decreased, and signs of invo- nign vascular tumors were induced, and these lution such as dilatation of vascular lumina and thrived in the animals. A more appropriate model is flattening of endothelial cells emerged. Dilatation in vitro culture of human hemangioma tissue or of blood vessels gradually turned prominent so endothelial cells, which reflects more genuine prop- that, at 3 to 4 months, the grafts were sponge-like erties of hemangioma.16–19 When human hemangi- under microscopy (i.e., with multiple dramatically oma tissue was cultured in vitro, formation of mi- dilatated blood vessels, endothelial cells accumu- crovessels was recognized, and varied behavior was lated in the trabecula, and multiple capillaries of identified when specimens from hemangiomas of diverse sizes). After that, fibrous tissue gradually varied phases were involved. This model provides a turned prominent and fat tissue emerged, and platform for investigations of the biological behavior human endothelial cells accumulated in islands of endothelial cells in hemangioma tissue and is again, with signs of degeneration. At 5 to 6 widely applied in research of in vitro biological prop- months, some of the grafts vanished completely erties and in investigations of therapeutic effects of and some were replaced with fibrofatty tissue, and certain pharmaceutical materials. several dilatated microvessels lined with human Being immunodeficient, athymic nude mice endothelial cells were scattered within the fibro- have the ability to tolerate xenografted living tis- fatty background. sues and are widely applied in medical investiga- Hemangioma is characterized by rapid growth tions, especially in establishment of animal models in the early stage followed by slow and spontane- for human diseases such as malignancies. Mean- ous involution. In the involuted phase, some of the while, some authors have reported that xe- hemangiomas vanish and normal tissue is re- nografted normal human tissue or tissue from stored, and the rest may regress with telangiecta- patients with benign diseases survived in the bod- sia, laxity, hypoelastic patches, scarring, or a fi- ies of nude mice.21–25 brofatty residuum. Serial morphologic With such a background, it is rational to suppose investigations indicate that this model resembles that human hemangioma tissue is likely to survive the natural development of human infantile hem- and retain its principal morphologic and biological angioma. properties when implanted into nude mice. In our Three days after grafting, fine blood vessels pilot investigation on the establishment of a nude were found in the capsules of grafts, which is a mouse model for human hemangioma,26 it was consistent finding in investigation of revascular- shown that the human hemangioma tissue sur- ization of xenografted human normal tissue on vived and retained its principal tumoral features. nude mice.27 Interestingly, more than one-fifth of Thereafter, modifications were attempted and a the grafts turned blue or purple as early as 2 days stable protocol was achieved in an estrogen-free after grafting, and histologic examination proved fashion, and serial morphologic details were ob- it to be subcapsular hemorrhage or hematoma, tained, as presented here. When human infantile suggesting that the grafts obtained their blood hemangioma tissue was grafted onto nude mice, supply earlier. After being resected from the hu- most of the grafts became engrafted and a few man body, the hemangioma tissue was nearly regressed in the early stage. In the early stage blood-free and appeared light red or pale. The (approximately 2 to 4 weeks after grafting), ne- only means of blood supply in such hemorrhage crosis, fibrosis, and a decrease of endothelial cells is from the host. One of the possible explanations were evident, as a result of ischemia. After that, the is that there were numerous vessels within the residual endothelial cells, distributed mainly in hemangioma tissue and they were open after be- the periphery and areas adjacent to blood vessels, ing cut into small pieces, with early connection of

876 Volume 120, Number 4 • Model of Human Hemangioma blood vessels with those of the host, the mouse hemangioma. After an ischemic stage, which blood entered the grafts and flowed out through lasted for approximately 3 to 4 weeks, a prolifer- other openings. ating phase was observed, the duration of which When xenografted onto nude mice, both ma- was less than 1 month, followed by an involuting lignant and benign human tissues obtain their blood phase for 3 to 4 months or more. Regarding the supplies mainly by recruitment of host endothelial natural course of human infantile hemangioma, cells and subsequent neovascularization.27,28 In con- the tumor usually emerges within the first few trast, others have reported long-term survival of hu- weeks of life, grows rapidly during the following 6 man endothelial cells in the bodies of nude mice to 8 months, and then subsides gradually in the when human dermal endothelial cells were ex- subsequent 5 to 7 years or more. The possible panded in vitro before transplantation, suggesting influential factors of such a difference in time that when there is a sufficient number of donor course between xenografts and native human endothelial cells, these cells may function and de- hemangiomas include the following: (1) the orig- liver blood within the graft.29 As shown by double inal hemangioma tissue was not in its earliest stage immunofluorescent labeling, most of the endothe- of growth (thus, in the model, the grafts might lial cells were of human origin. Mouse endothelial have an altered starting point of development); cells appeared early, but they were located mainly in (2) during the ischemic stage, necrosis and apo- the periphery of the grafts in small numbers. This ptosis of tumorous endothelial cells might inter- phenomenon indicates that the blood supply system fere with the subsequent development of the in the grafts depended on neovascularization from grafts, or ischemia might disturb the balance be- human endothelial cells in hemangioma tissue. tween proliferative and apoptotic activity in the More importantly, if it is true, the xenografted hem- hemangioma tissue; (3) the circulatory factors or angioma tissue may retain a certain degree of inde- other cells from the host might influence the de- pendence from the host and may not be replaced by velopment of the grafts, although the blood supply host cells for a relatively long period. This might be of the grafts seemed to depend mainly on neo- of essential importance for further investigations vascularization from human endothelial cells; and with this model. (4) a difference in the life cycles of nude mice and As evidenced by histologic and ultrastructural humans might have some influence on the devel- examinations, the human endothelial cells in opment of xenografted human endothelial cells. grafts showed a high level of proliferation after In contrast, the diminished time course may be a surviving ischemia, and this level was even higher great convenience for experimental research. than that of the original tumor. The underlying mechanism was not elucidated in the current study, but it might be explained by a well-known CONCLUSIONS theory that ischemia is a strong stimulator of an- A novel model of human hemangioma was es- giogenesis and that, during ischemia, the level of tablished, and the results of morphologic investiga- several mitotic factors of endothelial cells, such as tions indicated that this model could imitate the vascular endothelial growth factor, are elevated. natural course of human hemangioma, although Another unique phenomenon was observed on the details of its morphologic and biological prop- transmission electron microscopy, the fact that dur- erties need to be elucidated further. On the basis of ing the early stage of engraftment, especially at 5 to this model, discovery of the underlying pathogene- 15 days, many of the endothelial cells were ring-like sis, triggers of involution, and therapeutic effects of (i.e., there was vacuolation within the cytoplasm of certain drugs for human hemangioma might be endothelial cells where the lumen was perfectly closer being realized. These are what we will attempt round and blood cells were found within some of the to find in our future explorations. vacuoles). Generally, angiogenesis activity is up-reg- Wenying Liu, Ph.D., M.D. ulated in ischemia, and vasodilative factors are acti- Department of Pediatric Surgery vated; such active intracellular neovascularization West China Hospital of Sichuan University with prominent dilative tension may be a response to Chengdu 610041, P. R. China ischemic stimulation or an attempt to obtain a [email protected] greater blood supply. Within a 6-month experimental period, a ACKNOWLEDGMENT near-integrated fluctuation of development was The present study was supported by a grant from the observed on the grafts, which was observed to re- Ph.D. Programs Foundation of the Ministry of Educa- semble the natural course of human infantile tion of China (no. 20020610068).

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DISCLOSURE 14. Lee, R. J., Springer, M. L., Blanco-Bose, W. E., et al. VEGF The authors have no conflicts of interest to disclose. gene delivery to myocardium: Deleterious effects of unreg- ulated expression. Circulation 102: 898, 2000. 15. Kitajima, S., Liu, E., Morimoto, M., et al. Transgenic rabbits with increased VEGF expression develop hemangiomas in REFERENCES the liver: A new model for Kasabach-Merritt syndrome. Lab. 1. Ritter, E. J. The chicken comb and wattle as an experimental Invest. 85: 1517, 2005. model for the therapy of hemangiomas: Preliminary laser 16. Yu, Y., Varugheses, J., Brown, L. F., et al. Increased tie2 studies. Life Sci. 5: 1903, 1966. expression, enhanced response to angiopoietin-1, and dys- 2. Soldatskii, I.u.L., Shekhter, A. B., Ponkratenko, A. D., et al. regulated angiopoietin-2 expression in hemangioma-derived Effect of cryotherapy and laser destruction on experimental endothelial cells. Am. J. Pathol. 159: 2271, 2001. model of human vascular tumor. 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Cancer Res. 46: 362, 1986. Chin. J. Pediatr. Surg. 21: 115, 2000. 5. Soffer, D., Resnick-Roguel, N., Eldor, A., et al. Multifocal 21. Valerio, M. G., Fineman, E. L., Bowman, R. L., et al. Long- vascular tumors in fowl induced by a newly isolated retrovi- term survival of normal adult human tissues as xenografts in rus. Cancer Res. 50: 4787, 1990. congenitally athymic nude mice. J. Natl. Cancer Inst. 66: 849, 6. Liekens, S., Andrei, G., Vandeputte, M., et al. Potent inhi- 1981. bition of hemangioma formation in rats by the acyclic nu- 22. Jungheim, K., Schumm-Draeger, P. M., and Usadel, K. H. cleoside phosphonate analogue cidofovir. Cancer Res. 58: Graves’ disease: Xenotransplantation model (athymic nude 2562, 1998. mice). J. Mol. Med. 77: 185, 1999. 7. Bautch, V. L., Toda, S., Hassell, J. A., et al. Endothelial cell 23. Pouliot, R., Larouche, D., Auger, F. A., et al. Reconstructed tumors develop in transgenic mice carrying polyoma virus human skin produced in vitro and grafted on athymic mice. middle T oncogene. Cell 51: 529, 1987. Transplantation 73: 1751, 2002. 8. Taraboletti, G., Belotti, D., Dejana, E., et al. Endothelial cell 24. Honaramoz, A., Synedaker, A., Boiani, M., et al. Sperm from migration and invasiveness are induced by a soluble factor neonatal mammalian testes grafted in mice. Nature 418: 778, produced by murine endothelioma cells transformed by 2002. polyoma virus middle T oncogene. Cancer Res. 53: 3812, 1993. 25. Guerret, S., Govignon, E., Hartmann, D. J., et al. Long-term 9. Kiefer, F., Anhauser, I., Soriano, P., et al. Endothelial cell remodeling of a bilayered living human skin equivalent transformation by polyomavirus middle T antigen in mice (Apligraf) grafted onto nude mice: Immuno-localization of lacking Src-related kinases. Curr. Biol. 4: 100, 1994. human cells and characterization of extracellular matrix. 10. Dubois-Stringfellow, N., Kolpack-Martindale, L., Bautch, Wound Repair Regen. 11: 35, 2003. V. L., et al. Mice with hemangiomas induces by transgenic 26. Peng, Q., Liu, W., Tang, Y., et al. The establishment of the endothelial cells: A model for the Kasabach-Merritt syn- hemangioma model in nude mouse. J. Pediatr. Surg. 40: 1167, drome. Am. J. Pathol. 144: 796, 1994. 2005. 11. Dubois-Stringfellow, N., Jonczyk, A., and Bautch, V. L. Per- 27. Duprez, K., Bour, C., Merle, M., et al. Human nerve xe- turbations in the fibrinolytic pathway abolish cyst formation nografting in nude mouse: Experimental study of graft re- but not capillary-like organization of cultured murine en- vascularization. Microsurgery 12: 1, 1991. dothelial cells. Blood 83: 3206, 1994. 28. Gray, D. R., Huss, W. T., Yau, J. M., et al. Short-term prostate 12. Liekens, S., Verbeken, E., Vandeputte, M., et al. A novel primary xenografts: An in vivo model of human prostate animal model for hemangiomas: Inhibition of hemangioma cancer vasculature and angiogenesis. Cancer Res. 64: 1712, development by the angiogenesis inhibitor TNP-470. Cancer 2004. Res. 59: 2376, 1999. 29. Supp, D. M., Wilson-Landy, K., and Boyce, S. T. Human 13. Primo, L., Roca, C., Ferrandi, C., et al. Human endothelial dermal microvascular endothelial cells from vascular analogs cells expressing polyoma middle T induce tumors. Oncogene in cultured skin substitutes after grafting to athymic mice. 19: 3632, 2000. F.A.S.E.B. J. 16: 797, 2002.

878 EXPERIMENTAL

The Effect of Topical Mitomycin C on Full-Thickness Burns

Heath Tennyson, M.D. Background: Burns result in substantial morbidity because of fibroblast prolif- Eric R. Helling, M.D. eration and contracture. Mitomycin C is a chemotherapeutic agent known to Joseph Wiseman, M.D. suppress fibroblast proliferation. It is used in ophthalmologic disorders and Edward Dick, D.V.M. reduces scarring in upper aerodigestive surgery. No study of the effect of Robert C. Lyons, M.D. mitomycin C on cutaneous burns has been performed. This study examined San Antonio, Texas; and Landstuhl, burn healing in the presence of topical mitomycin C by evaluation of wound Germany appearance, contraction, and histology in a pig model. Methods: Standardized full-thickness burns were produced on the flanks of three pigs. One animal received no further therapy and was an external control. Two animals underwent placement of topical mitomycin C, 0.4 mg/ml, on selected burn sites for 5 minutes. This was repeated 2 and 4 weeks after injury. Evaluation was performed at 2 and 6 months using a clinical assessment scale and a visual analogue scale. Scar length and histologic analysis were also evaluated. Results: Clinical assessment scale and visual analogue scale scores showed im- proved appearance in the untreated external control wounds versus the untreated internal control and treated wounds (p Ͻ 0.001). Wound contraction was not significantly different between groups. Histologic characteristics between groups were similar except for epidermal hyperplasia, which was decreased in the untreated external control (p Ͻ 0.05) at 2 months after treatment. Conclusions: Topical mitomycin C treatment of full-thickness burn wounds at 0.4 mg/cc for three courses does not improve, and may worsen, clinical appearance and scarring during early healing. There is no difference in histology during the long- term healing process. Scar contraction was unchanged. (Plast. Reconstr. Surg. 120: 879, 2007.)

urns can result in disfiguring scarring, burn creased production of collagen that results in this contractures, and loss of skin pliability, loss of pliability and scar formation. During acute Bwhich can result in significant functional dis- burn healing, it would be advantageous to suppress abilities. Fibroblasts are responsible for the in- fibroblast proliferation while epithelial growth oc- curs to improve pliability and appearance of the From the Otolaryngology Service, Brooke Army Medical Cen- wound and to reduce scar contraction. ter, Fort Sam Houston; Plastic Surgery Service, University of Mitomycin C was originally isolated as an an- Texas Health Sciences Center; Otolaryngology Service, Land- tibiotic from Streptomyces caespitosus in 19581 and stuhl Regional Medical Center; Veterinary Service, U.S. Army Institute of Surgical Research, Fort Sam Houston; and was used as a chemotherapeutic agent. Mitomy- Plastic Surgery Service, Audie L. Murphy Veterans Affairs cin C acts as a DNA alkylating agent, inhibiting Medical Center. DNA synthesis and cross-linking DNA. Its action Received for publication November 28, 2005; accepted April is most prominent during the late G1 and early S 5, 2006. phases of the cell cycle.2 In the early 1990s, it was All research was performed at the U.S. Army Institute for recognized as a fibroblast antiproliferation agent Surgical Research (Burn Unit), Fort Sam Houston, San and shown to cause growth arrest in fibroblasts Antonio, Texas. This study does not necessarily represent the 3,4 views of the U.S. Army or the U.S. government. for up to 36 days after a single treatment. A Presented in part by Heath Tennyson at the 109th Annual dose-dependent duration of suppression has also Meeting of the American Academy of Otolaryngology–Head been shown to occur.5 It ultimately found use in and Neck Surgery, in Los Angeles, California, on September the treatment of pterygium and glaucoma and 27, 2005. was adapted to nasal, oropharyngeal, and laryn- Copyright ©2007 by the American Society of Plastic Surgeons geal surgery in 1997 for prevention of scar con- DOI: 10.1097/01.prs.0000277666.07097.55 tracture after surgery.

www.PRSJournal.com 879 Plastic and Reconstructive Surgery • September 15, 2007

Clinical studies to date have focused primarily on eye or mucosal and aerodigestive wound heal- ing. There is a paucity of studies regarding mit- omycin C and dermal healing. No controlled studies have examined the use of mitomycin C on surface wounds or burns. In this study, the authors evaluate the effects of three serial treatments of topical mitomycin C ap- plication over a full-thickness burn in a pig model. Histologic changes, clinical scar attributes, and measured scar contracture were evaluated to deter- mine whether there was a difference in outcome.

MATERIALS AND METHODS Fig. 1. Each animal received a total of 30 full-thickness burn After authorization from our institutional an- wounds (15 burns per flank). imal use committee, three 20- to 30-kg domestic Yorkshire crossbred female swine were used in this study. All animals were observed for 1 week to ex- control burn wounds underwent application of clude the possibility of preexisting disease. Complete topical mitomycin C (0.4 mg/ml) on the mitomy- blood count and blood chemistries were collected cin C–treated wounds using soaked 7.5 ϫ 2.5-cm from each animal for a baseline before burn wound cotton pledgets for 5 minutes (Fig. 1). They re- injury and mitomycin C application. Two of the pigs ceived no treatment on the internal control burn were designated to represent the treated and inter- wounds. nal control groups and the third animal represented After treatment, the pledgets were removed an untreated external control group. and the animal was awakened, extubated, and caged. The remaining burn wound sites remained Burn Injury untreated and served as internal controls. One All animals underwent general anesthesia and animal served as the external control and did not endotracheal intubation. The pigs were shaved receive any topical mitomycin C therapy after over the back and bilateral flanks. All animals were burn injury. Five days later, five of the wounds in surgically prepared with a chlorhexidine scrub the external control group pig underwent a 7-mm and rinsed with sterile saline. punch biopsy to verify burn wound depth. Each animal flank was marked into 15 differ- Two weeks after full-thickness burn injury, any ent 7.5 ϫ 2.5-cm areas with the use of a mapping remaining unseparated eschar was gently re- template so that burn locations were similar in all moved from the burn wounds under general an- animals. Using a 7.5 ϫ 2.5-cm, 166-g brass bar esthesia. A second treatment of mitomycin C to heated in a water bath to 100ºC after a burn pro- previously treated mitomycin C wounds was per- tocol developed by Singer et al.,6 full-thickness formed as described above. Serum chemistries burns were created by a 30-second application of and complete blood counts were taken from each the brass bar under its own weight at the skin sites animal during each mitomycin C treatment and at designated by our template. The brass bar was each wound evaluation time point to determine wiped dry before each application. Three identical possible toxic side effects of mitomycin C, such as brass bars were used on a rotating basis during thrombocytopenia, leukocytopenia, and renal dys- burn injury to ensure consistent temperatures dur- function. Two weeks after the second treatment, the ing serial application. Each animal received a total of final application of mitomycin C was performed on 30 full-thickness burn wounds (15 burns per flank). the previously mitomycin C–treated wounds. Immediately after burn injury, each wound underwent pinpoint tattooing on each side of Wound Assessment each wound in the plane of its longest axis using At 2 months after burn injury, all wounds were a template to ensure consistent length. These two examined under general anesthesia for wound tattoo points were used to assess wound contrac- appearance (Fig. 2). The examiner was blinded to tion at baseline, at 2 months, and at 6 months. In treated, internal control, and external control addition, after burn wound injury, the two animals groups and simply assessed each individual containing the mitomycin C–treated and internal wound. The measurement used was a visual ana-

880 Volume 120, Number 4 • Mitomycin C and Full-Thickness Burns

Table 2. Histologic Assessment Scale* Score Hyperkeratosis Absent 1 Present 0 Epidermal hyperplasia Absent 1 Present 0 Hair follicles Absent 1 Present 0 Apocrine glands Present 1 Absent 0 Smooth muscle Present 1 Absent 0 Collagen orientation Fig. 2. All wounds were examined under general anesthesia for Normal 3 wound appearance. Abnormal collagen in the papillary dermis 2 Abnormal collagen in the upper reticular dermis only 1 Table 1. Visual Analogue Scale and Clinical Abnormal collagen in the upper and lower Assessment Scale half of the reticular dermis 0 Fibroplasia (increased no. of fibrocytes) Visual Analogue Scale (length, 10 cm metered in 1-mm Absent 1 increments) Present 0 Excellent 0------10 Poor Vascular Absent 1 Clinical Assessment Scale Present 0 A Color (compared to surrounding Score *Best total score is the sum of individual scores (0–10), where the best skin) possible outcome is 10 and the worst outcome is 0. Perfect 1 Slight mismatch 2 Obvious mismatch 3 formalin for examination by a veterinary pathol- Gross mismatch 4 ogist in a blinded fashion with regard to the group. B Matte 1 8 Shiny 2 A histologic scale adapted from Singer et al. was C Contour used (Table 2). The process was repeated at 6 Flush with surrounding skin 1 Slightly proud/indented 2 months and the study was terminated. Hypertrophic 3 D Distortion Wound Contracture None 1 Mild 2 After burn injury and subsequent tattooing, Moderate 3 each wound was measured with a caliper from Severe 4 E Texture tattoo point to tattoo point and measurements Normal 1 were recorded to within 0.01 millimeter. This ini- Just palpable 2 tial measurement served as a baseline. Additional Firm 3 Hard 4 measurements were performed in the same man- Total score ______ner at 2 and 6 months after burn injury. Wound VAS score ______contraction was assessed using the following VAS, visual analogue scale. equation: [(Baseline wound length Ϫ Postinjury wound length)/(Baseline wound length)] ϫ 100 percent. Wound contraction at 2 months and 6 logue scale and a clinical assessment scale adapted months was expressed as a percentage of baseline from Beausang et al.7 (Table 1). Next, 10 of 30 wound length. treated wounds and 10 of 30 internal control un- treated wounds from pigs 1 and 2 and 10 of 30 Statistical Analysis wounds from pig 3 (external control untreated) Clinical assessment scale, visual analogue underwent 7-mm punch biopsy in the center of scale, and wound contraction results were ana- each wound. Biopsy specimens were not obtained lyzed using a two-factor analysis of variance and from the remaining wounds until future time Student-Newman-Keuls tests. Statistical signifi- points. Punch biopsy specimens were placed in cance was determined as a value of p Ͻ 0.05. Cor-

881 Plastic and Reconstructive Surgery • September 15, 2007 relation between the visual analogue scales and clinical assessment scales was performed using the Spearman rank correlation test. Histologic results were analyzed using the Spearman rank correlation, Kruskal-Wallis analy- sis of variance, and Mann-Whitney rank sum test. We used a parametric analysis of variance for tests on visual analogue scale, clinical assessment scale, and wound contraction because we had no two-factor nonparametric analysis of variance. We confirmed the results with a Kruskal-Wallis (one-way) analysis of variance and Mann-Whitney rank sum tests.

RESULTS Visual Analogue Scale External control wounds had a better appear- ance at both time points when compared with the internal control and treated groups (p Ͻ 0.05, Student-Newman-Keuls test). The average visual analogue scale score at 2 and 6 months for the Fig.3. Boxplotofscarring[visualanaloguescale(VAS)]bygroup internal control was 3.9 and 2.1; mitomycin and time. In the box plots, the median is the dark line within the C–treated, 3.8 and 2.5; and external control, 0.7 box. The box is defined by the 25th and 75th percentiles; thus, 50 and 1.0, respectively. There was no apparent dif- percent of the cases have values within the box. The error flags ference between the appearance of the mitomy- represent the largest and smallest observed values that are not cin C–treated and internal control groups at any outliers (n ϭ 30 treatment sites for each group). VAS2, visual an- time point. The appearance of the mitomycin alogue scale results at 2 months after burn injury; VAS6, visual C–treated and internal control scars varied analogue scale results at 6 months after burn injury. more than the internal control. The distribution is plotted in Figure 3. Histologic Assessment Scale There were no significant differences between Clinical Assessment Scale treatment groups for hyperkeratosis, presence of The external control group was significantly hair follicles, smooth muscle, collagen orienta- Ͻ (p 0.001, Student-Newman-Keuls test) different tion, fibroplasia, or vascular proliferation at any (improved appearance) from the internal control time point. The only significant difference oc- and the mitomycin C–treated groups with respect curred with decreased epidermal hyperplasia in to color, contour, surface, distortion, texture, and the external control group (p Ͻ 0.001, Kruskal- total clinical assessment scale score. The average Wallis analysis of variance); however, by 6 months clinical assessment scale scores at 2 and 6 months there was no difference in epidermal hyperplasia were 10.6 and 9.6 for the internal control, 11.2 and between any of the groups (Fig. 5). 10.1 for the treated, and 6.3 and 7.8 for the ex- ternal control groups, respectively. The internal control group was not significantly different Correlation of Visual Analogue Scale and from the treated group (p Ͻ 0.05, Student-New- Clinical Assessment Scale Scores with the man-Keuls test) for any of the clinical assess- Histologic Scale ment score subclassifications or the total clinical The clinical assessment scale and visual ana- assessment scale score. The appearance of mito- logue scale scores showed good correlation ac- mycin C–treated and internal control scars varied cording to the Spearman rank correlation test (at more than external control scars. In addition, ap- 2 months, r ϭ 0.922, r 2 ϭ 0.850, p Ͻ 0.001, n ϭ 90; pearance was initially worse for internal control at 6 months, r ϭ 0.844, r 2 ϭ 0.712, p Ͻ 0.001, n ϭ and mitomycin C–treated scars at 2 months but 90). Clinical assessment scale and visual analogue improved by 6 months, whereas scars for the ex- scale scores were poorly correlated with the his- ternal control continued to worsen with time (Fig. tologic assessment scale when the Spearman rank 4). Ultimately, all groups approached similar correlation test was used. The best correlation scores at 6 months. was between visual analogue scale scores at 6

882 Volume 120, Number 4 • Mitomycin C and Full-Thickness Burns

DISCUSSION This is the first controlled study of the appli- cation of mitomycin C in burns. Our initial hy- pothesis was that mitomycin C may improve wound healing, appearance, and scarring because of suppressed fibroblast proliferation. This was based on existing literature in which topical mit- omycin C therapy has been shown to be effective in decreasing scarring in the aerodigestive tract. In addition, its efficacy in the aerodigestive tract also seems to be long-lasting.9,10 The fact that our external control appeared better than the internal control and treated wounds based on our clinical assessment scale and visual assessment scale scores was surprising. In addition, it was clinically evident to nonblinded observers that one group was clearly healing bet- ter, so this was not a subtle finding. Only a few studies have evaluated mitomycin C for use on Fig. 4. Box plot of appearance [clinical assessment scale (CAS) keratinizing epithelial wounds. Ribeiro et al.11 score] by group and time. In the box plots, the median is the dark studied topically mitomycin C–treated rat model line within the box. The box is defined by the 25th and 75th per- surgical wounds in an internally controlled pro- centiles; thus, 50 percent of the cases have values within the box. spective study. These wounds were small exci- The error flags represent the largest and smallest observed val- sional defects. This group used a histologic scale ues that are not outliers (n ϭ 30 treatment sites for each group). and clinical assessment to evaluate the wounds CAS2, clinical assessment scale score results at 2 months after until 12 weeks after treatment. The mitomycin burn injury; CAS6, clinical assessment scale score results at 6 C–treated wounds revealed clinically reduced months after burn injury. wound healing compared with controls, including delayed eschar healing. There were no differences clinically between the two groups by 4 weeks, how- months and the clinical assessment score for ever. Likewise, mitomycin C–treated wounds collagen loss at 2 months (r ϭ –0.609, r 2 ϭ 0.371, showed significantly decreased fibrosis compared p Ͻ 0.001, n ϭ 29). with controls. Twelve weeks after treatment, there was no difference clinically or histologically. Wound Contraction The choice of mitomycin C dosing was based There was a statistically significant difference on review of the literature. Topical mitomycin C of increasing wound contraction over time within dosing varies widely, ranging from concentrations groups (p Ͻ 0.001, two-factor analysis of variance). of 0.001 mg/ml (which has minimal antiprolifera- Wound length at 2 months was similar to initial tive effects) to 1.0 mg/ml.5,13 Higher doses of mi- length, with minimal variance in all groups. At 6 tomycin C tend to be cytocidal to fibroblasts and months, wound contraction was evident, with the lower doses tend to exhibit an antiproliferative external control length contracting an average of effect. Topical mitomycin C application usually 22.5 percent; the internal control, 36.1 percent; involves 3 to 5 minutes of drug exposure of the and treated, 36.5 percent. However, when ana- wound surface using cotton pledgets. Several stud- lyzed, there was no statistical difference in wound ies indicate that fibroblasts eventually recover Ͼ contraction between treatment groups (p 0.05, from the antiproliferative effects of mitomycin C two-factor analysis of variance). The distribution is with an increase in numbers in cell cultured fi- plotted in Figure 6. broblasts harvested from tissue treated with mit- omycin C in vivo.12 Simman et al.5 have shown that Serum Basic Metabolic Panel and Complete fibroblast growth begins to recover 2 to 3 weeks Blood Count Results after mitomycin C therapy, but others have shown There was no evidence of cytopenia or renal that the effects of topical mitomycin C may last as dysfunction based on serial complete blood count long as 48 days.12 We felt that dosing 0.4 mg/ml or serum blood chemistries during the study. topically for 5 minutes was a common treatment

883 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 5. Distribution of epidermal hyperplasia by treatment and time. Epidermal hyperplasia in the external control group at 2 months (Ext 2) was significantly different from that for all other treatments and times. There were no other significant differences. Ext 2 and Ext 6 represent epidermal hyperplasia results for the external control group at 2 and 6 months after burn injury, respectively. Likewise, Int 2 and Int 6 and Treat 2 and Treat 6 represent results for internal control and mitomycin C–treated results at 2 and 6 months, respectively. regimen in the literature, which would likely have difference in any histologic parameters between a clinical response without being excessively cyto- or within the wound groups. cidal. The results of the internal control and the The results of the histologic assessment scale treated groups were not significantly different did not correlate well with the clinical assessment throughout the study regarding any evaluation scale and visual analogue scale scores. Beausang et parameters. Possible explanations include diffu- al. showed good correlation between their clinical sion of mitomycin C from nearby treated wounds assessment scale/visual analogue scale (used in into internal control wounds. Alternatively, sys- this study) and a histologic assessment scale based temic absorption may have played a role in deliv- on arrangement of collagen fiber orientation, col- ering unintended mitomycin C to internal control lagen fiber density, collagen fiber maturity, and wounds. If future studies are performed, it may be appearance of epidermal rete ridges when evalu- worthwhile to assess systemic absorption and local ating in situ scars before scar revision in humans. tissue mitomycin C concentrations. We used a histologic scale that evaluated the pres- One limitation of our study was the lack of ence or absence of several epidermal and dermal burn depth verification for each wound. Pig skin attributes and was straightforward for a pathol- (similar to human skin) is not uniform in thick- ogist to evaluate.8 Perhaps a histologic scoring ness and varies with location. Initially, we ran- system looking mainly at collagen fiber charac- domly chose five wounds from the external con- teristics (versus broader dermal/epidermal char- trol animal and performed 7-mm punch biopsies acteristics) would reveal more significant differ- 5 days after full-thickness burn injury in each ences. wound. These biopsies revealed that these Sewall et al.14 showed decreased wound con- wounds were full-thickness burn injuries to the traction in a controlled trial involving full-thick- level of the subcutaneous fat. An argument for ness wide excisional skin wounds that underwent the validity of our study concerning uniform topical mitomycin C therapy. Some wounds un- burn depth was no significant difference in any derwent two serial doses of topical mitomycin C parameters of our histologic scale, with the ex- and some wounds were treated with different ception of epidermal hyperplasia. Epidermal hy- doses of mitomycin C. They showed nine times less perplasia was decreased in the external control wound contraction at day 29 after full-thickness group at 2 months. At 6 months, there was no skin excision in the mitomycin C–treated wounds

884 Volume 120, Number 4 • Mitomycin C and Full-Thickness Burns

the study may also have introduced wound con- tracture measurement errors into our study. We chose young pigs because of the ease in managing smaller animals. Logistically, it is very difficult to manage large, adult pigs in these studies because of their weight and special housing requirements. Ideally, wound contracture would be best exam- ined using a nongrowing adult animal model in identical nondynamic skin regions. Despite promising literature for aerodigestive scarring, it appears that the dosing regimen for full- thickness burns in our study did not result in im- proved (and may have slightly worsened) healing. It is unclear what differences exist between the aero- digestive tract and cutaneous epithelium that result in this difference. Our dosing regimen was drawn from existing noncutaneous treatment regimens; however, it may not have been optimal for our ap- plication. There is no doubt that the dosing did cause a change in wound healing. Perhaps more Fig. 6. Box plot of length by group and time. In the box plots, the frequent dosing at lower concentrations would be medianisthedarklinewithinthebox.Theboxisdefinedbythe25th optimal for cutaneous wounds. In this pilot study, we and 75th percentiles; thus, 50 percent of the cases have values essentially took an “educated guess” at what an ap- within the box (n ϭ 30 in each group). The error flags represent the propriate dosing regimen might be. Multiple dosing largest and smallest observed values that are not outliers. LENPCT2 regimens controlled within a larger study may help and LENPCT6 represent the percentage of wound contracture for establish dose-response curves. group at 2 and 6 months after burn injury, respectively. The ultimate treatment for burn patients would be some type of therapy that would allow (or promote) regeneration of epithelial cells while compared with the control. In their study, there was retaining elasticity and suppressing scarring. De- no difference in the different dosing regimens.14 spite a clinically negative result in this initial pilot Unfortunately, their last wound contraction mea- study, we feel that the theory of control or sup- surement was at day 29, and long-term data were pression of fibroblast proliferation during burn not available. In our study, there was no significant healing could have a profound clinical outcome. difference in wound contraction between any Perhaps future mitomycin C studies should focus groups. Contraction was determined as a percent- on identifying why there are different responses in age of wound length at 2 months or 6 months keratinizing and nonkeratinizing epithelium and compared with wound length immediately after how this can be applied to treatment of cutaneous full-thickness burn injury. The confounding vari- injury. Other investigative areas may include mi- ables in measuring full-thickness burn wound con- tomycin C and cultured epithelium and localized tracture in our study included positioning of the burn contracture and partial-thickness wounds. animal during measurement. Flexion or exten- sion of the legs, neck, or spine can change wound CONCLUSIONS length in the porcine model. At each time point, This is the first prospective, controlled study to the pig position was kept as constant as possible. evaluate the clinical, histologic appearance and Position of the burn, flank versus back versus an- wound contraction in a full-thickness burn with terior versus posterior, may have contributed to topical mitomycin C. Treating full-thickness burn any error generated here. wounds with topical mitomycin C at 0.4 mg/cc for As previously stated, thickness variance ac- 5 minutes in three serial treatments does not result cording to body position could also introduce dif- in improved clinical or histologic appearance (and ferences in burn depth. The pigs involved in this may actually worsen appearance slightly). It does study were also young, growing pigs. Each animal not significantly reduce long-term wound contrac- grew at approximately the same rate based on ture in full-thickness burn wounds. There was no weight over the course of the study. Animal growth evidence of any thrombocytopenia, leukocytope- or differences in growth between animals during nia, or renal dysfunction on the basis of pretreat-

885 Plastic and Reconstructive Surgery • September 15, 2007 ment and serial posttreatment laboratory exami- 5. Simman, R., Alani, H., and Williams, F. Effect of mitomycin nations after topical mitomycin C therapy. C on keloid fibroblasts: An in vitro study. Ann. Plast. Surg. 50: 71, 2003. LTC Eric R. Helling, M.D. 6. Singer, A., Berruti, L., Thode, H., and McClain, S. Standard- Plastic Surgery Service ized burn model using a multiparametric histologic analysis Tripler Army Medical Center of burn depth. Acad. Emerg. Med. 7: 1, 2000. 1 Jarrett White Road 7. Beausang, E., Floyd, H., Dunn, K., Orton, C., and Ferguson, Honolulu, Hawaii 96859-5000 M. A new quantitative scale for clinical scar assessment. Plast. [email protected] Reconstr. Surg. 102: 1954, 1998. 8. Singer, A. J., Thode, H., and McClain, S. Development of a ACKNOWLEDGMENTS histologic scale to quantify cutaneous scars after burns. Acad. All funding was obtained through the U.S. Army Emerg. Med. 7: 1083, 2000. (Brooke Army Medical Center, Fort Sam Houston, San 9. Cable, B., Pazos, G., Brietzke, S., and Mair, E. Topical mit- Antonio, Texas). omycin therapy in the pediatric airway: State of the art. Otolaryngol. Head Neck Surg. 13: 53, 2002. DISCLOSURES 10. Rahbar, R., Jones, D., Nuss, R., et al. The role of mitomycin in the prevention and treatment of scar formation in the No author has any financial interest with any aspect pediatric aerodigestive tract: Friend or foe? Arch. Otolaryngol. of this study and no author received any compensation Head Neck Surg. 128: 401, 2002. for performing this study. 11. Ribeiro, Fde. A., Guaraldo, L., Borges, J., Zacchi, F., and Eckley, C. Clinical and histological healing of surgical REFERENCES wounds treated with mitomycin C. Laryngoscope 114: 148, 1. Hata, T., Sano, Y., and Sugawara, R. A new antibiotic from 2004. Streptomyces. Int. J. Antibiot. 9: 141, 1956. 12. Occleston, N., Daniels, J., Tarnuzzer, R., et al. Single expo- 2. Manufacturer package insert: Mitomycin-C. A.G. Scientific sures to antiproliferatives: Long term effects on ocular fi- Inc., 6450 Lusk Blvd., Suite E102, San Diego, Calif. 92121. broblast wound healing behavior. Invest. Ophthalmol. Vis. Sci. 3. Khaw, P., Doyle, J., Sherwood, M., Grierson, I., Schultz, G., 38: 1998, 1997. and McGorray, S. Prolonged localized tissue effects from 5 13. Ingrams, D., Volk, M., Biesman, B., Brian, S., Pankratov, M., minute exposures to fluorouracil and mitomycin C. Arch. and Shapshay, S. Sinus surgery: Does mitomycin C reduce Ophthalmol. 111: 263, 1993. stenosis? Laryngoscope 108: 883, 1998. 4. Daniels, J., Occleston, N., Crowston, J., and Khaw, P. Effect 14. Sewall, G., Robertson, K., Connor, N., Heisey, D., and Hartig, of antimetabolite induced cellular growth arrest on fibro- G. Effects of topical mitomycin on skin wound contraction. blast-fibroblast interactions. Exp. Eye Res. 69: 117, 1999. Arch. Facial Plast. Surg. 5: 59, 2003.

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886 RECONSTRUCTIVE

Defects of the Nose, Lip, and Cheek: Rebuilding the Composite Defect

Frederick J. Menick, M.D. Background: The face can be divided into regions (units) with characteristic Tucson, Ariz. skin quality, border outline, and three-dimensional contour. A defect may lie entirely within a single major unit or encompass several adjacent units, creating unique problems for repair. Composite defects overlap two or more facial units. Nasal defects often extend into the adjacent lip and cheek. The simplest solution may appear to be to simply “fill the hole”—just replace the missing bulk. Poor contour, incorrect dimension, malposition, asymmetry, poor blending into ad- jacent normal tissues, and a patch-like repair often follow. Methods: The following principles of regional unit repair were applied to guide these complex reconstructions: (1) reconstruct units, not defects; (2) alter the wound in site, size, shape, and depth; (3) consider using separate grafts and flaps for each unit and subunit, if appropriate; (4) use “like” tissue for “like” tissue; (5) restore a stable platform; (6) build in stages; (7) use distant tissue for “invisible” needs and local skin for resurfacing; and (8) disregard old scars. Results: Clinical cases of increasing composite complexity were repaired with local, regional, and distant tissues. Excellent aesthetics and function were ob- tained. Conclusions: Careful visual analysis of the normal face and the defect can direct the choice, timing, and technique of facial repair. Regional unit principles provide a coordinated approach to the vision, planning, and fabrication of these difficult wounds. The entire repair should be intellectually planned, designed step by step, and laid out in a series of coordinated steps, with general principles applied to successfully repair composite defects of the nose, lip, and cheek. (Plast. Reconstr. Surg. 120: 887, 2007.)

isually, the face is seen as a confluent, In contrast, the central units of the nose, lips, unified gestalt of flowing expansive spaces and eyelids are highly three-dimensional and Vand complexly contoured features. Aes- with a fixed border outline. They demand our thetically and anatomically, it can be divided into primary gaze. Because the entire area of these interrelated regions, each with its own unique central units is seen in most views, its contralat- character—individual geographic areas defined eral comparison with the opposite normal side by expected facial skin color, surface character (e.g., ala with ala) demands symmetry in posi- (smooth, pitted), skin thickness, hair quality tion, outline, and shape. The restoration of ap- (fine, matte, beard, scalp), mobility, subcutane- pearance after reconstruction requires the resto- ous fat distribution, muscle expression, and ration of the “normal”—the facial units.1,2 three-dimensional shape. Surgeons describe The cheek is broad, flat, and expansive, join- these topographic areas as facial units. Each unit ing the nose in a gentle advancing slope into the and subunit are visually defined by their charac- nasal sidewall while abutting the lip at the well- teristic skin quality, border outline, and three- defined change in contour defined by the naso- dimensional contour. The peripheral units are labial fold. Note that the ala sits medial to the the forehead, cheek, and chin. They are flat, nasolabial fold where it rises from the lip (not expansive areas with a variable outline and (like the cheek). A hairless triangle of lip lies between a picture frame) are of secondary visual interest. the alar base and the nasolabial fold. The naso- labial fold extends upward lateral to the normal Received for publication November 11, 2005; accepted April alar crease. 20, 2006. The gently contoured soft-tissue landmarks of Copyright ©2007 by the American Society of Plastic Surgeons the lip are marked by the philtrum columns, the DOI: 10.1097/01.prs.0000277662.51022.1d cupid’s bows, and the symmetrical vermilion.

www.PRSJournal.com 887 Plastic and Reconstructive Surgery • September 15, 2007

The skin, subcutaneous fat, and muscle of the lip more than 50 percent of a convex nasal subunit are supported by the underlying maxilla. The lip and a transposition flap is planned to resurface unit projects slightly forward of the facial mass. the nose, it is useful to discard adjacent normal The superior border of the lip abuts the alar tissue within the subunit and resurface the entire base and nostril sill. subunit, rather than only patching the defect. As The nose projects from the central facial plat- originally described, the reconstructive implica- form of the lip and cheek. Its delicate and com- tions of units and subunits did not distinguish plex three-dimensional contours define the na- clearly between peripheral and central units or sal subunits and establish the requirement for among convex, flat, or concave subunits. Over precise symmetry and spatial relationships to the time, it has become evident that the subunit contralateral nasal subunits and to all adjacent principle should be applied to central convex facial features, defining the length, width, and subunits (seen in primary gaze and requiring position of the nose. contralateral symmetry between the normal and When tissues are missing because of cancer reconstructed side) when using skin flaps. Flaps ablation, trauma, or congenital deficiency, a pincushion; grafts do not. Trapdoor contraction wound may lie entirely within a single major occurs in the recipient bed under flaps (but not unit. Frequently, however, a defect encom- grafts). When an entire convex subunit is resur- passes several adjacent units, creating unique faced, the pincushion effect created by wound problems for repair. Composite defects are maturation in the recipient site and around its those that overlap two or more facial units. 360-degree peripheral scar causes the flap to Often a nasal defect extends into the adjacent bulge, effectively augmenting the effect of carti- lip and cheek, presenting as a large, three- lage support grafts in recreating a convex exter- dimensional loss that encompasses several nal unit shape. This avoids the patch-like trap- units. Remember that aesthetic and anatomi- door effect that may occur when a small flap is cal tissue deficiencies and, thus, the require- placed within part of the round tip or alar sub- ments for repair of each facial area vary in units. Flaps should often be designed to replace cover, lining, support, and soft- and hard- topographic units, not defects. This applies, pri- tissue deficiency and in quality, outline, and marily, to convex central units being repaired contour. with a transposition flap—not to the dorsum or The simplest solution may appear to be to sidewall. simply “fill the hole”—just replace the missing Third, the obvious temptation when repairing bulk. Although a healed wound is a worthy ob- a composite defect is to fill the single defect with jective, the most important function of the face a single flap (often during a single operation). is to appear normal. Therefore, success is deter- Unfortunately, it is difficult to reproduce the mined by aesthetics, not simple wound closure. delicate three-dimensional character of multiple Several traps await the unsuspecting surgeon units with a single flap. Revisional procedures when repairing a composite wound. undertaken to divide a single flap into a cheek, First, the defect may not reflect the actual lip, and nose usually fail. Frequently, the single tissue loss. Wounds are enlarged by edema, local flap appears as a bulging, oversized, stuffed anesthesia, gravity, or tension or diminished by patch. Geometrically, however, the shortest dis- scar contraction or previous attempts at recon- tance between two points is a straight line. In struction. If a flap or graft that is too small is fact, a single large flap may represent a tissue positioned within the defect, it displaces adja- shortage, rather than excess, which prevents the cent landmarks inward. If too large a flap is used, surface skin from following the required com- it pushes the adjacent tissues outward, displacing plex three-dimensional shapes of the nose, lip, normal facial landmarks and creating perma- and cheek. Scar contraction also draws a single nent asymmetry and malposition. Thus, missing flap into a dome-like mass, outlined by patch-like tissue must be replaced in exact volume, depth, peripheral scars. Use of separate flaps (or grafts) and outline. The solution is to design flaps from for each facial unit should be considered when precise templates based on the contralateral nor- repairing composite defects. mal or ideal, not the defect. Fourth, although contour is the primary deter- Second, it is helpful to alter a wound in site, minant of normal, each unit is distinguished by size, shape, and depth when reconstructing its unique, geographic areas of skin color, tex- units. The “subunit principle” is often applied in ture, hair quality, and thickness. Donor materials nasal reconstruction.2 If a defect encompasses should be chosen that most exactly replace each

888 Volume 120, Number 4 • Nose, Lip, and Cheek Defects unit. “Like” tissue (nearly identical to what is tion. Poor results lead to patient dissatisfac- missing) is best replaced with “like” tissue— tion, not the number of stages or the cheek for cheek, lip for lip, and forehead or complexity of individual procedures. Time to nasolabial tissue for nose.3,4 Such an approach observe and plan is vitally important. Define a reestablishes the unique surface characteristics goal, adopt a plan, and proceed in stages with of each unit by using ideal materials for cover, the ideal in mind. lining, and support. Simultaneously, the donor Eighth, late attempts to subdivide and shape burden is shared, often limiting later donor a single, large, haphazard repair into individ- deformity.5 ual units require overcoming the patient’s and Fifth, the difficulty in facial reconstruction de- the surgeon’s fear of “scars.” Traditionally, to rives from the unique character of the face. By “debulk” a flap, its edges are elevated in stages necessity, distant free flaps have become a first through peripheral border incisions. However, choice for large, complicated wounds. Unfortu- the exposure is poor; the “debulking” is vaguely nately, distant tissue does not match facial skin planned and crudely performed during multiple in color, texture, or thickness; nor does it have a stages over months. In fact, old scars should be facial shape. Distant skin always appears as a disregarded. Using accurate templates based on mismatched patch within residual normal facial the contralateral normal or ideal, the expected skin. Thus, initially, free flaps should be supplied three-dimensional concavity of the alar crease or to a complex facial defect to provide bulk, pro- nasolabial fold is marked with ink and incised. tect vital structures, revascularize local tissue, Under direct view, the underlying soft tissue is and reestablish a facial platform. At a later stage, delicately sculpted in three dimensions. The local tissues are used for aesthetic cover. Distant overlying skin is reapproximated to the newly tissue provides for the “invisible” requirements contoured subcutaneous shaped framework with (lining and support) but is not used to replace quilting sutures and the wound closed. Although surface skin.6,7 Only local grafts and flaps a new “scar” is present, it lies “hidden” in the “match” residual facial skin. Only local facial skin expected unit border outline. The old periph- should be used to resurface the face. eral flap scar “disappears” because the visual Sixth, the nose sits on a platform of lip and shape of the unit is correct. cheek at a precise location and angle. Dis- Ninth, cover and lining replacements must placement of a successful nasal repair, even be thin and conforming so they do not bulge when malpositioned by only a few millimeters, inward, obstructing the nasal airway, or out- can create significant distortion. It must be ward, distorting the external shape. However, remembered that soft tissues frequently shift the primary determinant of facial shape is its because of the early effects of resolving local three-dimensional middle architectural layer. anesthesia and edema, and the late effects of Cartilage and bone grafts should be positioned gravity, tension, and scar contraction. If the during nasal repair before wound maturation underlying lip-cheek platform is unstable, it to support, shape, and brace cover and lining may shift and drag a reconstructed ala inferi- against scar contraction. They can be placed orly and laterally over time. The larger and primarily at the time of flap transfer or in a deeper the defect, the greater the risk. Thus, delayed primary fashion at an intermediate in deep, larger defects, the lip and cheek operation before forehead flap division.8 If should be repaired initially. Then, the nose is placed secondarily, months later, the late fixed rebuilt at a later stage when the underlying fibrosis of unsupported soft tissue prevents re- platform is stable. modeling of the covering flaps during late Seventh, surgeons frequently fail to appreci- revisions. Detailed three-dimensional sculp- ate the many advantages of surgical staging. ture of subcutaneous fat, frontalis muscles, Time permits a repair to “mature”—ensuring and scar during the intermediate operation of a stable platform, verifying vascular viability, a three-stage forehead flap nasal repair or and permitting the use of excess material for when recreating the subtle contours of the alar hinge-over flaps or other secondary applica- crease and nasolabial fold during later revi- tions such as delay or prefabrication, and in- sions (disregarding old scars) is very helpful. termediate soft-tissue sculpturing. “Difficult” Remember that surface contour reflects the facial repairs require a clear visualization of underlying shape of the soft- and hard-tissue the desired end result and a carefully formu- architecture and must be reestablished in lated plan before the initial surgical interven- three dimensions. Use primary and delayed

889 Plastic and Reconstructive Surgery • September 15, 2007 primary support and detailed soft-tissue sculp- remaining normal tissue within the left alar sub- ture to recreate facial three-dimensional con- unit. An exact pattern of the right contralateral tour. alar subunit was outlined just above the left na- solabial crease. Because the residual cheek de- PATIENT STUDY 1: SUPERFICIAL fect included the cutaneous portion of the na- COMPOSITE DEFECT OF THE ALA, LIP, solabial flap, the nasolabial flap was designed AND UPPER LIP with a subcutaneous pedicle, perfused by axial The defect after excision of a recurrent basal perforators from the facial and inferior orbital cell carcinoma of the left alar base extended into arteries. A conchal cartilage graft was fixed to the adjacent subcutaneous tissues of the ala, the residual lining with fine polypropylene su- cheek, and upper lip (Fig. 1, above, left). Each tures. It acted as an internal scaffold, maintain- individual unit was reconstructed separately. ing rim support and alar contour. The flap was The regional units of the nose and lip were thinned distally to 3 mm of subcutaneous fat and outlined with methylene blue. The left nasola- transferred to resurface the entire alar subunit bial fold was incised and the residual lip skin was (Fig. 1, below, left). Three weeks later, after di- rotated medially and superiorly, resurfacing the vision of the pedicle, the residual cheek defect upper lip and alar base (Fig. 1, right). The defect was closed by cheek advancement and the alar of the left ala was enlarged by excision of the base inset completed. Months later, most of the

Fig.1. (Above,left)Superficialdefectoftheleftala,lip,andcheek.(Right)Incisingalongthenasolabialfold, the lip component is repaired by rotation advancement of the residual lip. (Below, left) After subunit excision of residual normal skin within the left ala, the lining is supported and shaped with a conchal primary cartilage graft. Based on the right contralateral normal ala, an exact template is used to design a nasolabial flap supplied by subcutaneous perforators. A nasolabial flap is transposed to resurface the left ala subunit. (Reproduced with permission from Menick, F., and Burget, G. Nasal reconstruction: Creating a visual illusion. Adv. Plast. Reconstr. Surg. 6: 193, 1990.)

890 Volume 120, Number 4 • Nose, Lip, and Cheek Defects

and the soft-tissue defect is “filled” with local fat. Adjacent nasolabial skin can be transposed as an extension of a superiorly based cheek flap or as a nasolabial flap based on the subcutaneous perfo- rators from the facial and angular arteries. Sub- cutaneous fat under the residual cheek, lateral to the defect, is hinged-over, like the page of a book, to provide missing bulk. At the first stage, the regional units of the nose were outlined, as were the lip and nasolabial fold landmarks. The nasolabial fold was incised and the cheek elevated with 3 to 4 mm of subcutaneous fat. The underlying fatty soft tissue, based medi- ally, was incised as a turnover flap3 and hinged- over to fill the soft-tissue defect anterior to the maxilla (Fig. 3, above, right). The cheek skin was then rotated superiorly and medially using a back- cut at or above the commissure to resurface the cheek defect. The upper lip defect was resurfaced as a small extension of the cheek flap (Fig. 3, below, right). The lip-cheek platform was restored. Note that the left nasolabial fold was obliterated by the Fig. 2. Postoperative result without revision. The individual displacement of cheek skin within the lateral lip units of the ala, lip, and cheek are restored with scars hidden in unit. The nose was not reconstructed at this initial the joints between units. (Reproduced with permission from operation. Menick, F., and Burget, G. Nasal reconstruction: Creating a visual One month to 6 weeks later, the platform was illusion. Adv. Plast. Reconstr. Surg. 6: 193, 1990.) stable. The nose was repaired. Exact templates were made of the contralateral normal upper lip residual scars are hidden in the normal contour and ala. The upper lip template was used to mark lines of the face. The three-dimensional char- the ideal width and position of the new alar base, acter of the alar base is restored (Fig. 2). sill, and nasolabial fold. Using the contralateral alar subunit template as a guide, the outline of the ideal left ala was marked, and residual normal skin PATIENT STUDY 2: DEEP COMPOSITE was excised. Skin from the residual ala was hinged- DEFECT OF NOSE, LIP, AND CHEEK over for lining. A primary cartilage graft, based on A more significant defect of a left ala, cheek, the contralateral normal ala, was designed to sup- and upper lip is present after Mohs’ excision of a port and shape the reconstructed left ala. The twice recurrent basal cell skin cancer previously same pattern was used to design a two-stage fore- treated by excision and later by radiation therapy. head flap that was transferred to resurface the A modest amount of the superior orbicularis mus- entire alar subunit (Fig. 4). The forehead flap cular sphincter has been excised. A repair is pedicle was divided 3 weeks later. Four months planned to replace missing tissues with like tissues, later, slight fullness at the junction of the left restoring each individual unit to its exact outline, dome and ala was sculpted by reopening the an- size, and three-dimensional contour (Fig. 3, left). terior aspect of the alar unit incision. The ideal left When a full-thickness defect of the entire nasolabial fold, based on a pattern of the con- height of the upper lip is present, a cross-lip Abbe´ tralateral normal ala, was marked and directly in- flap that transfers skin, orbicularis muscle, vermil- cised to allow subcutaneous sculpturing to restore ion, and mucosa is the first choice.9 However, if the expected flat upper lip surface and the full the upper lip loss is incomplete and the muscle nasolabial fold. The aesthetic contours of the lip, sphincter in the inferior one-half of the lip is in- cheek, and nose join are satisfactory after repair. tact, a cheek skin flap and fat flap transposition The distracting scar of the cheek flap extension can be used to fill the soft-tissue void in the su- used to resurface the superior aspect of the upper perior lip anterior to the maxilla. Such a flap is lip has “disappeared” because the nasolabial static and provides no muscular function. The crease, created by direct incision, has reestab- missing external skin is replaced with cheek skin lished the expected facial contour (Figs. 5 and 6).

891 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 3. (Left) Defect of the left ala, lip, and cheek extending into the deep premaxillary soft tissues. (Above, right) At the first stage, a medially based fat flap is hinged-over to fill in missing soft-tissue bulk over the piriform aperture. (Below, right) The cheek is repaired with a cheek rotation advancement flap designed with a nonsubunit extension to resurface the lip.

PATIENT STUDY 3: FULL-THICKNESS around the oral commissure and into the mental LOSS OF THE LEFT ALA, COLUMELLA, crease. Thus, the nasolabial and submental folds AND NASAL SILL, ONE-HALF OF THE were marked and incised. An inferior laterally UPPER LIP, AND MEDIAL CHEEK based cheek flap was rotated to resurface the A massive recurrent basal cell carcinoma, orig- cheek defect. This restored the missing cheek skin inating in the right alar base and upper lip, re- and positioned the scar within the nasolabial fold quired full-thickness excision of the right cheek, and submental crease. The residual dog-ear at the two-thirds of the upper lip, the entire columella, upper end of the rotation would be revised at a and the right ala and nasal sill (Fig. 7, left). Cover, later stage. The lining defect was closed primarily. lining, and support for the nose, lip, and cheek The lip itself can be divided into topographic were missing. The aesthetic reconstruction of an upper lip full-thickness defect requires replacement subunits: a lateral subunit bordered by the phil- of all missing components (cover, lining, and mus- trum column, nostril sill, alar base, and the naso- cular support) with tissue that functions as a lip and labial crease, and a medial topographic subunit cosmetically reestablishes a normal appearance. that is one-half of the philtrum. In this case, Only the lower lip has the surface appearance, form, slightly more than half the upper lip and the alar and muscular function required for a major full- base and columella were missing. A subunit cross- thickness loss of the upper lip. Such a complex de- lip Abbe´ flap9 was designed in the midline of the fect of the nose, lip, and cheek must be recon- lower lip. A precise pattern of the missing hemilip structed in stages with ideal materials. topographic subunit was designed using the left The nasolabial fold normally extends inferi- hemilip as a model. An extension to the Abbe´ flap orly, lateral to the alar groove, and passes laterally was included to replace the missing nostril floor,

892 Volume 120, Number 4 • Nose, Lip, and Cheek Defects

Fig.4. Later,astableplatform,asubunitexcisionofresidualnor- Fig. 6. Another postoperative view of the three-dimensional mal skin and scar within the left ala subunit, is performed. A pri- restoration of defect. mary ear cartilage support batten graft is positioned. A left para- median forehead flap resurfaces the left alar unit.

a second stage, the lip pedicle was divided. The dog-ear at the right infraorbital margin was ex- cised. Unlike the traditional cross-lip Abbe´ flap, which is positioned to straddle the defect and to replace only one-half of the defect to limit lower lip deformity, this subunit flap is designed as an exact pattern of the missing tissue and in the mid- line of the lower lip, regardless of the site or size of the defect. On donor closure of the lower lip, symmetry of the lower lip and its commissures are maintained. Because the ala sits on a platform of the lip and cheek at a precise facial location and angle, no attempt was made to reconstruct the right ala at this time. Once the platform was stable, at a second stage 2 months later, the right ala was reconstructed as an exact subunit with a prefab- ricated right paramedian forehead flap designed from a template of the contralateral normal ala. Eight months after the initial reconstruction, like tissue (nose, cheek, and lip) was replaced in kind. Border scars were positioned aesthetically Fig. 5. Postoperative result with three-dimensional restoration and the orbicularis sphincter was reconstituted of the defect. with an intact and symmetrical commissure and upper lip and lower lip symmetry. Spontaneous reinnervation of both sensory and motor function alar base, and columella. This full-thickness lower occurred within 1 year. The left nasolabial crease lip flap was incised and rotated 180 degrees on a had been previously distorted by past excisions. 1-cm-wide pedicle based on the posterior vermil- The right upper lip was reconstructed to match it ion and mucosa (Fig. 7, right). Two weeks later, at (Fig. 8).

893 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 7. (Left) Defect after excision of the upper lip, columella, nasal sill, right ala, and medial cheek. (Right) At the first stage, the cheek is repaired with a laterally based cheek rotation advancement flap that follows the nasolabial fold into the submental crease. Basedonapatternoftheleftcontralateralnormalresiduallip,asubunitcross-lipAbbe´ flap is designed and positioned in the middle of the lower lip. The lip flap includes additional tissue to replace the nasal sill and columella. At a second stage, based on a pattern of the contralateral left normal ala, a subunit reconstruction of the missing right ala is accom- plishedwitharightparamedianprefabricatedforeheadflapforcover,lining,andsupport. (Reproduced with permission from Menick, F., and Burget, G. Nasal reconstruction: Cre- ating a visual illusion. Adv. Plast. Reconstr. Surg. 6: 193, 1990.)

Fig. 8. Postoperative results after pedicle division. (Reproduced with permission from Menick, F., and Burget, G. Nasal reconstruction: Creating a visual illusion. Adv. Plast. Reconstr. Surg. 6: 193, 1990.)

894 Volume 120, Number 4 • Nose, Lip, and Cheek Defects

Fig. 9. Massive defect after squamous carcinoma of the septum and failed irradiation rhinec- tomy, medial maxillectomy, and total excision of the upper lip with an inadequate repair with fan flaps. (Reproduced with permission from Menick, F. Facial reconstruction with local and distant tissue:Theinterfaceofaestheticandreconstructivesurgery.Plast.Reconstr.Surg.102:1424,1998.)

Fig. 10. (Left) At a first stage, the fan flaps are divided, a split rib graft is fixed to the maxillary tuberosities, and the oronasal defect is separated with a wraparound latissimus dorsi free flap and skin graft. (Center) At a second stage, excess skin and subcutaneous tissue of the latissimus free flap are excised. The lip unit is resurfaced with a right superficial temporal artery island hair-bearing scalp flap. Both cheeks are advanced to resurface the medial cheek defects. The major components of the lip and cheek units have been restored. (Right) During a third stage, nasal lining was supplied with a free radial forearm flap for lining that was covered externally with a split-thickness skin graft for temporary cover. Because scalp hair grew within the hairless triangles of the upper lip, both cheek flaps were further advanced to resurface the hairless triangles of the lip while maintaining hair-bearing scalp to create a mustache. Later, at a fourth stage, the split-thickness skin graft is discarded. A rib bone–cartilage dorsal cantilever graft and a columellar strut are positioned. (Reproduced with permission from Menick, F. Facial reconstruction with local and distant tissue: The interface of aesthetic and reconstructive surgery. Plast. Reconstr. Surg. 102: 1424, 1998.)

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Fig. 11. (Above, left) Nasal cover is supplied with a paramedian forehead flap. (Above, right)Atafifthstage,duringtheintermediateoperationofathree-stageforeheadflap, the forehead skin is elevated with a few millimeters of subcutaneous fat. Underlying excess soft tissues are sculpted by excision. Delayed primary support grafts for the ala, sidewall, and tip are placed over thin lining. The forehead flap is returned to the re- cipient site. (Below) At a sixth stage, the forehead flap pedicle is divided. Disregarding all scars, direct incisions are made in the ideal nasolabial folds. The soft tissues are sculptedtorestoretheflatsurfaceoftheupperlipandtherounder,fullersurfaceofthe medial cheeks, defined by the nasolabial crease. (Reproduced with permission from Menick, F. Facial reconstruction with local and distant tissue: The interface of aesthetic and reconstructive surgery. Plast. Reconstr. Surg. 102: 1424, 1998.)

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PATIENT STUDY 4: MASSIVE CENTRAL tissue was sculpted by excision of excess latissimus FACIAL LOSS skin and subcutaneous tissue to improve the con- A 69-year-old man presented years after radical tour of the cheek and upper lip. Bilateral cheek nasectomy, bilateral partial maxillectomy, and to- flaps were rotated and advanced to resurface the tal upper lip resection for a multiply recurrent medial cheeks. A scalp flap based on the right squamous cell carcinoma of the septum unrespon- superficial temporal vessels was passed under the sive to previous radiation therapy, chemotherapy, right cheek flap to resurface the upper lip with and surgery. Bilateral fan flaps had been moved to hair-bearing scalp, allowing the later growth of a recreate a soft-tissue upper lip partition. His palate mustache (Fig. 10, center). At a third stage, a free remained unrepaired. His visible deformity, un- radial forearm flap, anastomosed to the right fa- intelligible speech, requirement for tube feeding, cial vessels, was positioned skin inward to provide and constant drooling motivated repair (Fig. 9). nasal lining. Its external raw surface was tempo- Staged reconstruction using local and distant tis- rarily skin grafted. Hair-bearing scalp skin, which sue was planned.4 had been moved, within the normally “hairless” At the first stage, the upper lip fan flaps were triangle of the superior lip medial to the nasolabial split. A rib graft was positioned “in the breeze” fold was excised, allowing the right and left cheek from one maxillary tuberosity to the other to pro- flaps to be further advanced to the expected junc- vide central facial support and projection. This tion of the hairless upper lip and mustache. Sub- bony scaffold was covered with free latissimus sequently, the skin graft was excised, the free flap dorsi myocutaneous flap anastomosed to the left thinned for nasal lining, and an osteocartilaginous facial vessels. The nasal “palate” surface was cov- dorsal rib graft and columellar strut positioned to ered with back skin and the “oral” surface with a restore a central nasal support. This was covered split-thickness skin graft. This separated the oral with a left paramedian forehead flap (Fig. 10, right, and nasal cavities and established a central mid- and Fig. 11, above, left). At a later date, the fore- facial platform (Fig. 10, left). At a second stage, soft head flap was elevated, soft tissue sculpted in an

Fig. 12. Postoperative result after free flap reconstruction of the face to supply a maxillary platform, oronasal separation, and nasal lining. Local facial tissues were used to resurface the nose, lip, and cheek. (Reproduced with permission from Menick, F. Facial reconstruction with local and distant tissue: The interface of aesthetic and reconstructive surgery. Plast. Reconstr. Surg. 102: 1424, 1998.)

897 Plastic and Reconstructive Surgery • September 15, 2007 intermediate operation,8 and further rib and con- 5. Avoid the use of “one hole” and “one flap” chal ear positioned to support the alae, sidewalls, when reconstructing composite defects that and tip (Fig. 11, above, right). Subsequently, the encompass multiple facial units. forehead flap was divided. The ideal nasolabial 6. Use like tissues for like. Use local tissue for fold was marked. Nasolabial creases were recon- facial resurfacing and distant tissue for invis- structed by incising each cheek flap at the site of ible needs. the ideal nasolabial fold and sculpting the subcu- 7. Use primary and delayed primary cartilage taneous tissues to recreate the contour of the ex- and bone grafts to create a hard-tissue archi- pected hairless flat triangle of the upper lip and its tecture, and use detailed subcutaneous border with the ideal full nasolabial fold (Fig. 11, sculpture to shape soft tissues into a middle below). supportive architecture during the interme- Postoperatively, the patient can speak clearly, diate operations of a three-stage forehead maintain oral input, and no longer drools. The flap and during revisions. oral and nasal cavities are separated, facial pro- 8. Build in units. jection is restored, and the expected contours and 9. Use surgical staging to advantage. skin quality of a normal face are reestablished. He Frederick J. Menick, M.D. remains well 9 years after reconstruction (Fig. 12). 1102 North El Dorado Place Tucson, Ariz. 85715 [email protected] DISCUSSION DISCLOSURE The first prerequisite for facial reconstruction The author has no financial interest in any of the is clear visualization of the goal and a commitment products, devices, or drugs mentioned in this article. to achieve it. The entire repair should be intel- lectually planned, designed step by step, and laid REFERENCES out in a series of coordinated steps. General 1. Menick, F. Artistry in aesthetic surgery: Aesthetic perception 1–4,6 and the subunit principle in facial aesthetic surgery. Clin. Plast. principles should be applied to successfully Surg. 14: 726, 1987. repair composite defects of the nose, lip, and 2. Burget, G., and Menick, F. The subunit principle in nasal cheek. reconstruction. Plast. Reconstr. Surg. 76: 236, 1985. 3. Gillies, H., and Millard, D. R. The Principles and Art of Plastic 1. The alar base subunit must be precisely po- Surgery. Boston: Little, Brown, 1957. sitioned on a stable, newly reconstructed 4. Millard, D. R. Principlization of Plastic Surgery. Boston: Little, Brown, 1986. platform. 5. Menick, F. Facial reconstruction in regional units. Perspect. 2. Exact patterns based on the contralateral Plast. Surg. 8: 104, 1994. norm allow the correct positioning of land- 6. Menick, F. Facial reconstruction with local and distant tissue: marks and incisions and the exact replace- The interface of aesthetic and reconstructive surgery. Plast. Reconstr. Surg. 102: 1424, 1998. ment of missing tissues. 7. Burget, G. C. Optimal use of microvascular free flaps, cartilage 3. Preexisting scars can often be ignored. Con- grafts and a paramedian forehead flap for the aesthetic re- tour is the primary determinate of what is construction of the nose and adjacent facial units. Plast. Re- normal, and direct incisions (disregarding constr. Surg. (in press). old scars) often allow more precise subcuta- 8. Burget, G., and Menick, F. Aesthetic restoration of one-half of the upper lip. Plast. Reconstr. Surg. 76: 239, 1985. neous sculpture. 9. Menick, F. A ten-year experience in nasal reconstruction 4. Alter the wound in site, size, shape, and depth with the three-stage forehead flap. Plast. Reconstr. Surg. 109: as necessary to recreate the expected units. 1839, 2002.

898 RECONSTRUCTIVE

Aesthetic Management of the Ear as a Donor Site

Davinder J. Singh, M.D. Background: The ear is a frequently used donor site for facial reconstruction. Scott P. Bartlett, M.D. It serves as an ideal source for skin, cartilage, and composite grafts because of Philadelphia, Pa. its color and texture match. However, because of the prominent location of the ears, the prevention of donor-site problems such as scarring and resultant asymmetries is equally important in creating an overall aesthetic facial recon- struction. The purpose of this review was to describe surgical techniques of minimizing ear donor-site morbidity as a consequence of harvesting of com- posite chondrocutaneous grafts. Methods: A retrospective analysis was performed of all patients who underwent nasal reconstruction performed by the senior surgeon (D.J.S.) between 1987 and 2003, to identify those patients in whom a composite chondrocutaneous au- ricular graft was used. Photographs, surgical technique, and aesthetic outcomes were reviewed for those patients identified as having donor auricular composite grafts. Results: Three hundred fifty-seven nasal reconstructions were performed. Of the 357 reconstructions, 67 involved harvest of preauricular or postauricular full-thickness skin graft, and 79 involved use of auricular cartilage. Sixteen of the 79 involved harvesting of auricular composite grafts. For these 16 patients, defect size, donor site, and closure of donor site are described and indications for certain techniques are delineated. Conclusions: The harvest of composite grafts is challenging in technical design and in closure of the defect. In this patient series, the donor defects were closed primarily in one of six ways, depending on the size of the cartilage and skin graft required. These techniques allowed adequate harvest of donor tissue while preserving the aesthetics of the ear. (Plast. Reconstr. Surg. 120: 899, 2007.)

uch has been written about the tech- or postauricularly.20 Although the donor defects niques of facial and particularly nasal from harvesting auricular skin grafts and carti- Mreconstruction using tissues from the lage grafts may be closed without much diffi- ear.1–19 The ear is an ideal donor site in that it culty, the harvest of composite grafts poses more frequently provides sufficient tissue for aesthetic of a challenge in preserving aesthetics and func- and functional reconstruction. It serves as a tion of the ear.21–23 source of skin, cartilage, and composite grafts. Donor-site problems specific to the ear are Skin grafts may be harvested from the preauric- asymmetries in size, shape, position, and volume, ular area, taking advantage of skin laxity and and scarring leading to contractures, banding, contour in placing scars discretely. Postauricular webbing, and distortion. The scars may be wid- skin grafts are also easily accessed. Cartilage ened, hypertrophic, or hypopigmented/hyper- pigmented. The purpose of this review is to de- grafts are most frequently harvested from the scribe techniques whereby the aesthetics and conchal bowl, and may be taken preauricularly function of the ear are preserved in its use as a From the Division of Plastic Surgery, University of Pennsyl- donor site. These techniques prevent the need vania, Hospital of the University of Pennsylvania. for helical rotation/advancement flaps and skin 22–24 Received for publication November 27, 2005; accepted April grafts by allowing primary closure of the do- 14, 2006. nor defect with an aesthetic result. Presented at the Aesthetic Facial Reconstruction in Adults and Children Symposium, in San Diego, California, Feb- PATIENTS AND METHODS ruary of 2004. A retrospective analysis of all patients who un- Copyright ©2007 by the American Society of Plastic Surgeons derwent nasal reconstruction by the senior sur- DOI: 10.1097/01.prs.0000277659.88395.a5 geon between 1987 and 2003 was performed to

www.PRSJournal.com 899 Plastic and Reconstructive Surgery • September 15, 2007 identify those patients in whom a composite chon- hairline, and the defect is closed primarily as drocutaneous auricular graft was used. The fol- shown in Figure 1. lowing data were obtained: age, size of defect, type of reconstruction, donor site, size of donor tissue, Technique 2 management of donor site, complications with re- Occasionally, a wider cartilaginous base of 1 to construction and/or donor site, and aesthetic out- 1.5 cm is needed for larger defects of the alar rim come of the donor site. Photographs and surgical as shown in Figure 2, above. The auricular defect technique were reviewed for those patients iden- resulting from this size harvest requires running tified as having donor auricular composite grafts. the dog-ear anteriorly into the hairline and pos- teriorly into the triangular fossa. In running the RESULTS dog-ear posteriorly, a full-thickness wedge of car- tilage from the triangular fossa must be excised to Of the 357 nasal reconstructions, 67 involved prevent buckling of the fossa (Fig. 2, below). harvest of preauricular or postauricular full-thick- ness skin graft, and 79 involved use of auricular Technique 3 cartilage. Sixteen of the 79 involved harvesting of auricular composite grafts. Fourteen of the 16 If the vertical dimension (height) of the nasal grafts were used in nasal reconstruction after defect is short (Fig. 3, above, left), the composite Mohs’ procedures and the remaining two for de- graft is harvested from the anterior aspect of the layed nasal reconstruction after dog bite injury. helical root (Fig. 3, above, right and below, left) and The average age for these patients was 60 years the dog-ear must be run superiorly and inferiorly (range, 12 to 81 years). The average size of the (Fig. 3, below, right). This provides adequate tissue composite graft harvested was 1.44 ϫ 1.12 cm for the nasal reconstruction and an aesthetic clo- (range, 1 ϫ 1cmto2ϫ 3 cm). The base of the sure without disturbing the size of the ear (Fig. 4). helix was the most commonly used area for com- posite graft harvest. It was repaired aesthetically by Technique 4 using the following techniques. When composite grafts 1 to 1.2 cm wide are needed from the base of the helix, the defect may be closed primarily by advancing the helical rim Technique 1 forward. However, depending on the anatomy, If the auricular tissue needed is less than 1 cm, this may lead to overprojection of the ear, as seen the composite graft is harvested from the root of in the patient shown in Figure 5. This overprojec- the helix. The dog-ear is run anteriorly toward the tion should to be addressed at the time of the

Fig. 1. Harvest of a small composite graft (Ͻ1 cm) with primary closure by running the dog- ear anteriorly into the hairline. This closure preserves contour of the ear.

900 Volume 120, Number 4 • Ear as a Donor Site

Fig. 2. (Above) A wider defect of the alar rim requires a larger composite graft from the helical base, as seen by the markings on the ear.(Below)Closureofthedefectisaccomplishedbyrunningthedog-earanteriorlyintothehairlineandposteriorlyintothetriangular fossa. A full-thickness wedge of cartilage must be removed from the triangular fossa to prevent buckling of the ear. harvest with a postauricular incision and a scapho- patient, it can be taken either preauricularly or mastoid suture to match the prominence with the postauricularly, as demonstrated by the line draw- contralateral ear. ings. Figure 8 shows the skin (solid lines) and cartilaginous (dotted lines) incisions that could be Technique 5 made for harvesting of an extended skin graft with For tissue requirements greater than 1.5 cm in the composite graft. The extended full-thickness width, as seen in the patient shown in Figure 6, skin graft was taken posterior (dotted white line), above, the donor graft can be obtained from the which also provided access for the scaphomastoid base of the helix. However, closure of the defect suture. The solid blue line marks the skin excision is more intricate. A simple helical advancement anteriorly and the dotted red lines indicate the would result in significant distortion and over- cartilaginous incision (Fig. 9). Placement of the projection. To prevent this, a V-shaped wedge of skin is harvested, but a “half-star” pattern of car- graft on the nasal defect demonstrates the amount tilage at the apex of the V is taken (Fig. 6, below). of ideal auricular tissue available for facial recon- In addition, a postauricular incision with a scapho- struction (Fig. 10). mastoid suture is needed. This prevents cupping Table 1 lists the graft sizes required to recon- of the ear with closure (Fig. 7). struct the nasal defect, auricular sites of graft har- vest, and auricular donor defect closure tech- Technique 6 niques referenced to the descriptions above. When an extended skin graft component is One patient required a revision of the ear after needed with the composite graft, as seen in this primary closure. The revision involved a postau-

901 Plastic and Reconstructive Surgery • September 15, 2007

Fig.3. Thenasaldefectiswidebutshortinitsverticaldimension.Thisallowsharvestfromtheanteroinferiorhelicalrim.Primary closure is achieved by running the dog-ear superiorly and inferiorly. ricular incision with placement of chondromas- at the expense of the auricular aesthetics. The goal toid sutures to set back the ear after helical rim of this article is to present more simplified tech- advancement was performed as the primary clo- niques of aesthetic primary closure of auricular de- sure. The aesthetic outcome of the auricular do- fects when harvesting tissue for use at other sites. nor sites was viewed as excellent by the patients The auricle and its surrounding skin are most and the senior surgeon. frequently used for harvest of full-thickness skin grafts and conchal cartilage, and the closure of these DISCUSSION donor defects is rarely difficult and infrequently Numerous authors have demonstrated the util- leaves residual deformity. In contrast, the harvest of ity of auricular tissue in nasal reconstruction,1–19 but composite grafts is much more challenging in tech- little has been written on the management of the ear nical design and in closure of the defect. as a donor site. Many of the techniques used in Composite grafts can be harvested from virtu- closure of the donor defect come from the repair of ally any location on the ear, and some of the donor primary auricular defects secondary to trauma or defects can be closed primarily, whereas others cancer resection.24–26 Various methods of repairing require more extensive technique to prevent au- the ear have been described; however, many use ricular distortion. The lobule is a good source of complex advancement or rotational flaps and/or tissue match for columellar defects, and the ma- full-thickness skin grafts.22,27 When the only defect is jority of the lobe defects can be closed primarily the auricular wound, the focus is on its repair. When without distortion, as seen in Figure 11. using auricular tissue to reconstruct a nasal or facial The conchal cartilage is also a frequent site for defect, the focus is on the repair of this defect, often composite grafts. If a small amount of skin is

902 Volume 120, Number 4 • Ear as a Donor Site

Fig. 4. Photographs demonstrate inset of graft and aesthetic outcomes of nasal reconstruction and the auricular donor site in comparison with the contralateral ear.

Fig. 5. With harvest of a small (1 to 1.2 cm) composite graft, closure can be achieved by helical rim advancement. However, over- projection of the ear may result, as seen in this series of photographs.

903 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 6. (Above) This nasal defect requires a larger composite graft with a width of 1.8 cm. The harvest site on the auricle is demonstrated by the purple lines.(Below) Closure for this size auricular defect involves a V-shaped wedge of skin and ahalf-starpatternofcartilageexcisionattheapexoftheV.Thesolidlinesindicateskinincisionandthedottedstarpattern demonstrates cartilaginous incisions. If the cartilage is not excised in this manner, cupping of the ear will occur with closure. In addition, a postauricular incision with a scaphomastoid suture is performed. needed, it can be harvested anteriorly and the of the helix. The donor defects in this series of defect closed primarily. If a large amount of skin patients were closed primarily by one of six tech- is needed, skin grafting of this area may be nec- niques based on the size of the cartilage and skin essary. graft required and the anatomy of the ear. The Helical rim composite grafts may provide the goal was to provide symmetry with the contralat- best contour match for the defect. The helical eral ear and to preserve the normal contour of the rim can generally be closed primarily. Primary external ear. closure may cause distortion and notching of Previous authors have described alternative the rim, as shown in Figure 12. Incorporation of methods of closing similarly sized auricular de- one or more Z-plasties during closure may there- fects. Comparison with their methods is made with fore be advisable. the techniques described in this article. In this series of patients, chondrocutaneous Technique 1 involves closure for auricular de- grafts were taken more commonly from the base fects in which less than 1 cm width of graft is

904 Volume 120, Number 4 • Ear as a Donor Site

Fig. 7. The ear shape and projection of the ear are maintained after closure.

Fig. 8. Occasionally, an extended skin graft is needed in addition to the composite graft for reconstruction of nasal defects. The solid lines indicate skin incisions and the dotted line indi- cates a cartilaginous incision. (Right) The solid lines represent the harvest of a postauricular full-thickness skin graft.

harvested. The graft is harvested from the helical Technique 2 is used for defects with cartilag- base, and the dog-ear is excised anteriorly, allow- inous requirements of 1 to 1.5 cm. The resultant ing primary closure of the donor defect. Burget helical defect requires running the dog-ear ante- and Menick have described two other methods of riorly into the preauricular skin and posteriorly closure, one in which the preauricular skin is un- into the triangular fossa. A full-thickness wedge of dermined and advanced superiorly. The second cartilage must also be removed for closure without method involves a tubed flap with a conchal car- buckling of the fossa. tilage graft insertion for reconstruction of the har- Technique 3 is used when the vertical dimen- vested helix.28 Although Burget and Menick’s sion of the composite graft needed is short. The techniques are effective in achieving an aesthetic graft can be harvested from the most anterior, closure, they entail further incisions and a more inferior component of the helical rim, and the complex closure. Furthermore, long-term results defect closed by running the dog-ear superiorly by these methods have not been published. and inferiorly.

905 Plastic and Reconstructive Surgery • September 15, 2007

Table 1. Graft Sizes Required to Reconstruct Nasal Defects, Auricular Sites of Graft Harvest, and Auricular Donor Defect Closure Techniques Technique Patient Graft Size (cm) Harvest Location Type 1 1.2 ϫ 1.0 Base of helix 4 2 2.2 ϫ 1.1 Superior helix 5 3 1.7 ϫ 1.5 Base of helix 5 4 1.4 ϫ 1.1 Base of helix 2 5 2.0 ϫ 1.5 Base of helix 5 6 1.8 ϫ 0.8 Base of helix 3 7 1.6 ϫ 1.2 Base of helix 5 8 1.0 ϫ 1.0 Base of helix 1 9 2.0 ϫ 1.5 Base of helix 5 10 1.2 ϫ 1.0 Base of helix 4 11 0.8 ϫ 1.3 Base of helix 1 12 1.5 ϫ 1.2 Base of helix 2 13 1.5 ϫ 1.0 Base of helix 5 14 3.0 ϫ 1.3 Base of helix 3 15 1.5 ϫ 1.0 ϫ 3.0 Base of helix with 6 skin graft extension 16 1.8 ϫ 1.2 Superior helix 5

Fig. 9. The solid blue line marks the skin excision anteriorly and the dotted red lines indicate the cartilaginous incisions. This pat- tern of harvest allows for closure without cupping and buckling dressed with a scaphomastoid suture, by means of of the ear. a postauricular incision, at the time of primary repair. Technique 5 is used to close defects from har- Technique 4 is used to close defects resulting vest of composite grafts with a width greater than from harvest of composite grafts 1 to 1.2 cm in 1.5 cm. Simple advancement of the helical rim for width from the base of the helix. Occasionally, the closure would result in significant distortion and defect may be closed primarily by advancing the overprojection. To prevent this, a V excision of helical rim forward. However, this may result in composite graft is harvested and the donor defect overprojection of the auricle. It should be ad- is converted into a half-star pattern at the apex of

Fig. 10. These photographs show the amount of auricular tissue available for nasal reconstruc- tion and the inset of the composite graft and full-thickness skin graft.

906 Volume 120, Number 4 • Ear as a Donor Site

Fig.11. Thelobuleisagoodsourceoftissuematchforcolumellardefects,andthemajorityofthedonorsitescanbeclosedprimarily, as seen here, without distortion of overall shape.

Fig. 12. Composite grafts may be harvested from the lateral helical rim and closed primarily. However, primary closure of the helical rim in this area may result in distortion and notching, as seen in this patient. the V to allow closure without creating cupping of half-star pattern and scaphomastoid suturing. For the upper third of the auricle. In addition, a the larger composite donor sites, the question scaphomastoid suture is placed to match projec- arises as to whether to consider an Antia-Buch type tion with the other ear. Tanzer described a similar closure.29 Although this is an elegant method of technique for repair of the helical rim for con- reconstruction of helical rim defects, it may be genital deformities.24 complex and time consuming and has not been Technique 6 is applicable for larger soft-tissue necessary in any of our cases to date. needs that encompass a composite graft and a Depending on the size of composite graft re- full-thickness skin graft. This may be harvested in quired, closure of the defect on the basis of these continuity either preauricularly or postauricularly techniques results in an overall smaller ear but and closed by converting the auricular defect to a preserves the contour and projection of the ear.

907 Plastic and Reconstructive Surgery • September 15, 2007

Most patients in this age group accept a smaller ear 9. Avelar, J. M., Psillakis, J. M., and Viterbo, F. Use of large in exchange for an aesthetic nasal reconstruction composite grafts in the reconstruction of deformities of the nose and ear. Br. J. Plast. Surg. 37: 55, 1984. with a good color and texture match and fewer 10. Clarimont, A. A., and Conley, J. J. The uses and limitations stages of reconstruction. of auricular composite grafts. J. Otolaryngol. 7: 249, 1978. 11. Symonds, F. C., and Crikelair, G. F. Auricular composite grafts in nasal reconstruction: A report of 36 cases. Plast. CONCLUSIONS Reconstr. Surg. 37: 433, 1966. Various techniques can be used to close the 12. Argamaso, R. V. An ideal donor site for the auricular com- auricular donor site while obtaining an aesthetic posite graft. Br. J. Plast. Surg. 28: 219, 1975. match of contour and projection with the con- 13. Friedman, H. I., Stonerock, C., and Brill, A. Composite ear- lobe grafts to reconstruct the lateral nasal ala and sill. Ann. tralateral ear. The ear is an ideal donor site for Plast. Surg. 50: 275, 2003. facial reconstruction and should also be repaired 14. Gubisch, W., and Ludwig, C. Composite grafts in secondary aesthetically to minimize scarring and asymme- rhinoplasties. Am. J. Cosmet. Surg. 6: 91, 1989. tries. 15. Vasconez, L. O., Gamboa-Bobadilla, M., and Core, G. B. Treatment of paralytic ectropion with composite chondro- Scott P. Bartlett, M.D. cutaneous graft. Ann. Plast. Surg. 33: 557, 1994. Division of Plastic Surgery 16. Field, L. M. Nasal alar rim reconstruction utilizing the crus University of Pennsylvania of the helix, with several alternatives for donor site closure. 3400 Spruce Street J. Dermatol. Surg. Oncol. 12: 253, 1986. 10 Penn Tower 17. Bennett, J. E. Reconstruction of lateral nasal defects. Clin. Philadelphia, Pa. 19104 Plast. Surg. 8: 587, 1981. [email protected] 18. Orticochea, M. A new method for total reconstruction of the nose: The ears as donor areas. Clin. Plast. Surg. 8: 481, 1981. 19. Stucker, F. J., Jr., and Shaw, G. Y. The perichondrial cuta- DISCLOSURE neous graft: A 12-year clinical experience. Arch. Otolaryngol. Neither of the authors has a financial interest in any Head Neck Surg. 118: 287, 1992. of the products, devices, or drugs mentioned in this 20. Guyuron, B. Simplified harvesting of the ear cartilage graft. Aesthetic Plast. Surg. 10: 37, 1986. article. 21. Khosh, M. M., Horn, C. E., and Honrado, C. P. Closure of conchal cartilage harvest sites via absorbable quilting suture. REFERENCES Arch. Facial Plast. Surg. 6: 202, 2004. 1. Hirohi, T., and Yoshimura, K. Surgical correction of re- 22. Strucker, F. J., and Sanders, K. W. A method to repair au- tracted nostril rim with auricular composite grafts and an- ricular defects after perichondrial cutaneous grafting. La- choring suspension. Aesthetic Plast. Surg. 27: 418, 2003. ryngoscope 112: 1384, 2002. 2. Constantian, M. B. Indications and use of composite grafts in 23. Sawada, Y., Nakajima, T., and Yoshimura, Y. Auricular com- 100 consecutive secondary and tertiary rhinoplasty patients: posite graft from the scapha and its repair using a retroau- Introduction of the axial orientation. Plast. Reconstr. Surg. ricular subcutaneous pedicle flap. Aesthetic Plast. Surg. 11: 53, 110:1116, 2002. 1987. 3. Ozek, C., Gundogan, H., Bilkay, U., Alper, M., and Cagdas, 24. Tanzer, R. C. Congenital deformities of the auricle. In J. M. A. Nasal columella reconstruction with a composite free flap Converse (Ed.), Reconstructive Plastic Surgery, Vol. 3. Philadel- from the root of auricular helix. Microsurgery 22: 53, 2002. phia: Saunders, 1977. Pp. 1671–1719. 4. Raghavan, U., and Jones, N. S. Use of the auricular composite 25. Kontis, T. C., and Papel, I. D. Reconstruction of congenital graft in nasal reconstruction. J. Laryngol. Otol. 115: 885, 2001. and acquired auricular scaphal deficiencies. Arch. Facial Plast. 5. Karen, M., Chang, E., and Keen, M. S. Auricular composite Surg. 5: 263, 2003. grafting to repair nasal vestibular stenosis. Otolaryngol. Head 26. Elsahy, N. I. Reconstruction of the ear after skin and peri- Neck Surg. 122: 529, 2000. chondrium loss. Clin. Plast. Surg. 29: 187, 2002. 6. Hatoko, M., Tanaka, A., Kuwahara, M., Niitsuma, K., and 27. Schroeder, W. A., Jr. Closure of conchal defects: The hinged Ioka, H. Auricular composite graft for skin defect of the retroconchal island flap with overlying cutaneous transpo- philtrum dimple. J. Craniofac. Surg. 14: 228, 2003. sition flap. Dermatol. Surg. 21: 560, 1995. 7. Giberson, W. G., and Freeman, J. L. Use of free auricular 28. Burget, G. C., and Menick, F. J. Unilateral full-thickness nasal composite graft in nasal alar/vestibular reconstruction. defects. In Aesthetic Reconstruction of the Nose. St. Louis, Mo.: J. Otolaryngol. 21: 153, 1992. Mosby, 1994. Pp. 205–267. 8. Mayes, M. D., and Yessenow, R. S. The use of composite 29. Antia, N. H., and Buch, V. I. Chondrocutaneous advance- auricular grafts in nasal reconstruction. J. Dermatol. Surg. ment flap for marginal defect of the ear. Plast. Reconstr. Surg. Oncol. 14: 994, 1988. 39: 472, 1967.

908 DISCUSSION

Aesthetic Management of the Ear as a Donor Site

Charles H. Thorne, M.D. New York, N.Y.

he authors present an algorithm for the clo- the authors are referring to that portion of the Tsure of auricular defects resulting from har- anterior helical rim, near the ear/cheek junc- vest of chondrocutaneous composite grafts for tion, where the crus of the helix has emerged nasal reconstruction. The data are derived from from the concha to become actual helical rim. a series of 357 nasal reconstruction cases per- This is well shown in the authors’ Figure 2, below, formed over a 16-year period by a talented and left. Based on the experience described by Baker, experienced surgeon. If the frequency of com- I suggest that the donor site for these grafts posite grafts in this series is dissected further, the could have been shifted slightly downward, so 16 cases of composite grafts account for approx- that the grafts were harvested from the crus of imately 4.5 percent of the total number or one the helix, within the concha. The cutaneous por- case per year in the experience of a surgeon who tion would be oriented as a transverse triangle, performs approximately one nasal reconstruc- similar to what the authors show in Figure 2, tion every 2 weeks. below, left, but slightly lower on the cheek. The Composite grafts from the ear to the nose, result of this small shift in the donor site is that therefore, are not common in the spectrum of the defect resulting from harvest of the crus of techniques available for nasal reconstruction. the helix is within the concha, not the helical They are only appropriate for defects involving rim, and can be closed primarily without any the alar rim with minimal lining deficits. The deformity to the helical contour. The cutaneous cutaneous coverage requirements of these de- defect is closed by advancing the cheek, using a fects are such that they are “graftable,” rather face lift–type incision, with the resulting trans- than requiring flap coverage. verse scar well hidden below the sideburn. Al- The largest series of composite grafts to the though it is an apparently small alteration in nose has been presented by Baker.1 The key technique, the permutation described above can surgical teaching point is to keep the truly com- make closure significantly easier and less con- posite portion small. The overall graft can be spicuous. quite large but consists mostly of full-thickness Charles H. Thorne, M.D. skin graft. The composite portion, however, is New York University School of Medicine small, so that no portion of the composite graft 812 Park Avenue is more than 5 mm (approximately) from vascu- New York, N.Y. 10021-2759 larized tissue. [email protected] I would quibble with only one aspect of the article, and that is the location chosen for most DISCLOSURE of the grafts. The authors state that most grafts The author has no financial interest in any of the were taken from the base of the helix. By “base,” products, devices, or drugs mentioned in this article. REFERENCE Received for publication May 14, 2006. Copyright ©2007 by the American Society of Plastic Surgeons 1. Baker, D. C. Composite grafts to the nose. Presented at the American Association of Plastic Surgeons meeting, Laguna DOI: 10.1097/01.prs.0000256482.91217.1c Niguel, Calif., May 2000.

www.PRSJournal.com 909 RECONSTRUCTIVE

Incomplete Excision of Squamous Cell Carcinoma of the Skin: A Prospective Observational Study

Pee-Yau Tan, M.B.B.S. Background: Squamous cell carcinoma is the second most common cancer of Edmund Ek, M.B.B.S. the skin. It behaves differently from basal cell carcinoma. Few large-scale studies Shirley Su, M.B.B.S. have identified risk factors for incomplete excision of cutaneous squamous cell Francesco Giorlando, M.B.B.S. carcinoma. The authors report the largest prospective study to identify the risk Tam Dieu, F.R.A.C.S. factors for incomplete excision of these lesions. Adelaide and Victoria, Australia Methods: A total of 517 histopathologically confirmed squamous cell carcino- mas were excised from January of 2001 to December of 2002 at the Peter MacCallum Cancer Institute. Of these, 480 primary excisions were analyzed. Data pertaining to patient age, sex, lesion size, margin of excision, recurrence, previous excision, site, anesthetic choice, and repair method were collected prospectively. Results: The overall incomplete excision rate was 6.3 percent. Lesions on the ear (p Ͻ 0.003), re-excisions (p Ͻ 0.001), and invasive lesions (p Ͻ 0.001) were associated with the highest incomplete resection rates. Age (p ϭ 0.61), sex (p ϭ 0.075), tumor size (p ϭ 0.521), surgeon’s experience (p ϭ 0.092), and recurrent lesions (p ϭ 0.408) were not statistically significant risk factors. Conclusions: Statistically significant risk factors were ear lesions, invasive le- sions, and previously incompletely excised lesions referred for re-excision. The authors recommend more care with tumor markings, taking margins of at least 5 mm, using deeper margins, and referring patients to more experienced centers. (Plast. Reconstr. Surg. 120: 910, 2007.)

kin cancer is common, with basal cell car- The goal of surgical treatment is to achieve cinoma the most common type, accounting curative en bloc resection, rather than piece- Sfor approximately 75 to 80 percent of all meal resection,8 while minimizing cosmetic dis- skin malignancies. Squamous cell carcinoma is tortion. For basal cell carcinoma, the likelihood the second most common type, accounting for of recurrence is well demonstrated to be directly 15 to 39 percent.1–3 Unlike basal cell carcinoma, related to the adequacy of excision.8 The same squamous cell carcinoma has the potential to evidence for squamous cell carcinoma is lacking. metastasize. Occasionally, local adjuvant radio- Nevertheless, given its potential for metastasis, therapy is indicated for a high-grade, locally ad- with reported rates of 5 to 47 percent, early, 4 vanced lesion with a high risk of metastasis ; complete excision is desirable, though this is not nevertheless, surgical excision remains the treat- always possible.1,3,5–8,10,11 The dilemma of radical ment of choice. Recommended excision mar- surgical margins versus conservative narrow mar- gins vary, according to patient and tumor fac- 4–7 gins, and hence the risk of incomplete resection, tors, from 2 mm to 3 cm. has led to various guidelines and techniques for avoiding incomplete excision of skin lesions.4–7 From the Flinders Medical Center; St. Vincent’s Hospital; Southern Health Care Network; Peter MacCallum Cancer Recently, the incomplete excision rates for non- Institute; and Department of Plastic and Reconstructive melanoma skin cancers have been reported to Surgery, Southern Health Care Network. range from 5.8 percent12 to 15.9 percent5; some Received for publication September 24, 2005; accepted April studies make no distinction between squamous 20, 2006. and basal cell carcinoma,1 and in those that fo- Copyright ©2007 by the American Society of Plastic Surgeons cused on squamous cell carcinoma, the numbers DOI: 10.1097/01.prs.0000277655.89728.9f were too small to be significant.5,12 Given that these

910 www.PRSJournal.com Volume 120, Number 4 • Squamous Cell Carcinoma two types of lesions behave differently, we believe RESULTS that squamous cell carcinoma should be analyzed Of a total of 2582 lesions excised, 517 (20 separately, particularly with regard to the risk fac- percent) were squamous cell carcinomas. Of tors associated with incomplete excision. these, 480 (92.8 percent) were primary excisions, 27 (5.2 percent) were excisions of recurrent le- sions, and 10 (1.9 percent) were re-excisions of PATIENTS AND METHODS previously incompletely excised lesions (Table 1). From January of 2001 to December of 2002, The incomplete excision rate was 6.3 percent 2582 skin tumors were excised from 1223 patients (30 of 480) for primary excision, 11.1 percent at the Peter MacCallum Cancer Institute. Data (three of 27) for recurrent lesion excision, and 60 were collected prospectively and entered into a percent (six of 10) for re-excision of previously standardized form. All patients referred to the incompletely excised lesions. Unless otherwise institute with skin lesions for which malignancy specified, data in this study are based on primary could not be clinically excluded were recruited. excisions. Patients with punch, shave, or incisional biopsies and palliative excisions were excluded. Cases with Age incomplete or incorrectly entered proformas were The mean age of the 477 patients who under- excluded (79 patients with 96 lesions), including went primary excision was 75.8 years (Fig. 1). The 56 lesions for which the pathology report was median age was 77, and the range was 38 to 96 equivocal (i.e., there was uncertainty as to the true years (Table 2). The mean ages of patients with nature of the lesion). The raters were three con- incompletely and completely excised lesions were sultants, a plastic surgery trainee (usually first year, 74.8 and 75.7 years, respectively. This slight dif- on a 6-month rotation), and an experienced clin- ference was not statistically significant on Stu- ical assistant. dent’s unpaired t test (p ϭ 0.61). When analyzed All pathology specimens were examined and with a cut-off age of 75 years, 9 percent incomplete reported on by the Department of Pathology at the excision was seen with the younger cohort com- same center. The excised specimens were initially pared with 6.3 percent, although this difference immersed in silver nitrate before 2- to 3-mm-thick was not statistically significant. serial transverse sections were made. The number of sections cut was at the discretion of the pathol- ogist. An incomplete margin was defined by the Sex pathologist as the presence of tumor at the sur- In our series, 76.7 percent of lesions (368 of gical margin. 480) were removed from men and 23.3 percent The data collected included patient age and (112 of 480) were from women, for a ratio of 3.3:1. sex, tumor site and size, preoperative clinical di- The incidence of incomplete excision was 7.3 per- agnosis, type of anesthesia, pathology results, and cent (27 of 368) for men and 2.7 percent (three the presence or absence of invasion or tumor at of 112) for women. The difference was not statis- ϭ the surgical margin. The macroscopic surgical tically significant (p 0.075). margin, method of reconstruction, and experi- For women, 42.9 percent of lesions (48 of 112) ence of the surgeon were also collected. were on the head and 47.3 percent (53 of 112) All data were collated and entered into the were on the limbs. For men, 65.8 percent (242 of Filemaker Pro program and analyzed using the 368) were located on the head and 20.7 percent SPSS version 11 software package. Unless other- (76 of 368) were on the limbs (Table 3). wise stated, information analyzed and presented pertains to primary excision for squamous cell Anatomical Site carcinoma (n ϭ 480). Numbers in the “re-exci- Sixty percent of squamous cell carcinomas sion” and “recurrence” groups were too small for (290 of 480) occurred on the head, 26.8 percent the characteristics to be analyzed with meaning. (129 of 480) were on the limbs, 6.7 percent (32 of Chi-square analysis was used to determine statis- 480) were on the neck, and 6 percent (29 of 480) tical significance. Where the expected value of were on the trunk. The rates of incomplete exci- one or more cells was less than 5, Fisher’s exact test sion varied according to anatomical site, as fol- was used instead. Results were considered to be lows: head, 7.6 percent (22 of 290) (p ϭ 0.135); statistically significant for p values less than 0.05. trunk, 6.9 percent (two of 29) (p ϭ 0.701, Fisher’s The 95 percent confidence interval and odds ratio exact test); neck, 6.3 percent (two of 32) (p ϭ 1, were obtained for significant risk factors. Fisher’s exact test); and limbs, 3.1 percent (four of

911 Plastic and Reconstructive Surgery • September 15, 2007

Table 1. Risk Factors Investigated for Incomplete Excision of Squamous Cell Carcinoma* Risk Factor/Variable Incomplete Resection Versus Others p Odds Ratio Nature Primary 6.3% (30/480) 24.3% (9/37) Ͻ0.001† 2.088–11.135 Recurrence* 11.1% (3/27) 7.3% (36/490) 0.447† Re-excision* 60% (6/10) 6.5% (33/507) Ͻ0.001† 5.79–80.13 Age Ͻ75 years old 9.0% (21/233) 6.3% (18/284) 0.252‡ Male sex 7.3% (27/368) 2.7% (3/112) 0.075‡ Anatomical site Head 7.6% (22/290) 4.2% (8/190) 0.135‡ Limb 3.1% (4/129) 7.4% (26/351) 0.084‡ Neck 6.3% (2/32) 6.3% (28/448) 1† Trunk 6.9% (2/29) 6.2% (28/451) 0.701† Site on head Ear 20.5% (9/44) 4.8% (21/436) 0.001† 2.16–11.93 Forehead 4.8% (3/63) 6.5% (27/417) 0.785† Cheek 5.2% (3/58) 6.4% (27/422) 1† Nose 13.0% (3/23) 5.9% (27/457) 0.167† Tumor size Ͻ10 mm 5.6% (14/251) 7.0% (16/229) 0.524‡ Ͻ20 mm 7.1% (14/196) 5.6% (16/284) 0.502‡ Ͼ20 mm 6.1% (2/33) 5.9% (28/477) 1† Excision margin Ͻ5 mm 6.4% (30/469) 0% (0/11) 1† Consultant surgeon 8.5% (4/47) 6.0% (26/433) 0.521† Anesthesia Local (Ϯsedation) 5.9% (27/455) 12.0% (3/25) 0.2† Regional 0% (0/9) 6.4% (30/471) 1† General 18.8% (3/16) 5.8% (27/464) 0.071† Invasive SCC 40.0% (2/5) 5.9% (28/475) 0.034† 1.7 to 66.3 Repair Direct 5.6% (23/409) 9.9% (7/71) 0.184† Flap 8.8% (3/34) 6.1% (27/446) 0.461† Graft 10.8% (4/37) 5.9% (26/443) 0.275† SCC, squamous cell carcinoma. *All variables except those marked with an asterisk were based on the analysis of 480 cases of primary excision. †Fisher’s exact test. ‡Chi-square test.

Fig. 1. Primary squamous cell carcinoma lesions, age versus incidence. Note the mode at 79 years.

912 Volume 120, Number 4 • Squamous Cell Carcinoma

Table 2. Descriptive Statistics: Age, Unpaired t Test in all three cases. This was not statistically signif- .(icant (p ϭ 1, Fisher’s exact test (0.61 ؍ p) Age Incomplete Complete Total Surgeon’s Experience Median, years 74 77 77 Mean, years 74.8 75.7 75.71 The registrar and clinical assistant performed Minimum and maximum, 90 percent of the operations (433 of 480), and years 54, 88 38, 96 SD, years 8.4 9.4 consultants performed 9.8 percent (47 of 480). Total 28 448 477 Their incomplete excision rates were 6 percent (26 of 433) and 8.5 percent (four of 47), respec- tively. The difference was not statistically signifi- cant (p ϭ 0.521). Table 3. Site of Lesion versus Patient Sex (p < 0.0005) Female Male Total Type of Anesthetic (n) (n) (n) Most squamous cell carcinomas (94.8 percent, Head 48 242 290 or 455 of 480) were excised with the patient under Limbs 53 76 129 Neck 6 26 32 local anesthetic with or without sedation. This Trunk 5 24 29 group had an incomplete excision rate of 5.9 per- Total 112 368 480 cent (27 of 455). General anesthesia was used in 3.3 percent (16 of 480) and had an incomplete excision rate of 18 percent (three of 16). Regional 129) (p ϭ 0.084). This difference was not statisti- anesthesia was associated with no incomplete ex- cally significant. cisions. The difference was not statistically signif- Of the lesions excised from the head, the rate icant. of incomplete excision was highest for the ear, at 20.5 percent (nine of 44 lesions) (p ϭ 0.001, Invasive Character Fisher’s exact test; 95% CI for odds ratio, 2.16 to Four squamous cell carcinomas had nerve in- 11.93). Of these nine excisions, four were incom- vasion and one involved the deep fascia. All five plete at the deep margins and five were incom- were on the head, specifically, the ear, nose, scalp, plete at the lateral margins. Rates for other sites preauricular region, and temple. Of these five in- were as follows: forehead, 4.8 percent (three of vasive lesions, two were incompletely excised. This 63); cheek, 5.2 percent (three of 58); lips, 7 per- was statistically significant (p ϭ 0.034, Fisher’s ex- cent (one of 14); nose, 13 percent (three of 23); act). The 95 percent confidence interval for odds postauricular region, 100 percent (one of one); ratio was 1.7 to 66.3. There was no vascular inva- scalp, 2.5 percent (one of 40); and temple, 3.8 sion in our series. percent (one of 26). These rates were not statis- tically significant. The inner canthus (n ϭ 3), Method of Repair outer canthus (n ϭ 4), and preauricular region The rate of incomplete excision was 5.6 per- (n ϭ 7) had no incomplete excisions. cent (23 of 409) for direct closure, 8.8 percent (three of 34) for flap repair, and 10.9 percent (four of 37) for graft repair. The difference was Lesion Size not statistically significant. The incomplete excision rates for squamous cell carcinomas of less than 10 mm, less than 20 Margin of Incomplete Excision mm, and greater than 20 mm in diameter were 5.6 The lateral margins were involved in incom- percent (14 of 251), 7.1 percent (14 of 196), and plete excision in 62 percent (18 of 29), compared 6.1 percent (two of 33), respectively; these rates with the deep margin in 34 percent (10 of 29). were not statistically significant. Both margins were involved in 3.4 percent (one of 29). The margin was not specified in one case. Margin of Excision Surgical margins of 2 to 5 mm had an incom- Recurrent Lesions plete excision rate of 6.4 percent (30 of 469). Of the total 517 squamous cell carcinoma, 5.2 There were no incomplete excisions in the eight percent (n ϭ 27) were recurrent lesions. Distri- cases with margins of 5 to 10 mm. Margins of more bution of recurrent lesions was comparable to that than 10 mm resulted in no incomplete excisions of primary excision (Table 4). Most (74.1 percent,

913 Plastic and Reconstructive Surgery • September 15, 2007 percent of all incompletely excised squamous 62 (0.39؍Table 4. Site of Lesion versus Primary Excision (p 1 Site Recurrence Primary Total cell carcinomas, consistent with other reports. For re-excisions (i.e., lesions referred for wider Head 20 290 310 Limbs 6 129 135 excision margins), the incomplete rate was sur- Neck 1 32 33 prisingly not higher. There are no other published Trunk — 29 29 data specifically on re-excisions for comparison. It Total 27 480 507 was observed that with lesions incompletely ex- cised a second time, most of these lesions (five of six) were in the head and all had incompletely or 20 of 27) were from the head, 22.2 percent (six excised deep margins, and most (four of six) also of 27) were from the limbs, and 3.7 percent (one had the lateral margin involved. This finding un- of 27) were from the neck. Of those that recurred derscores the aggressiveness and difficulty in treat- in the head, 30 percent (six of 20) were on the ear. ing these incompletely excised squamous cell car- Overall, the incomplete excision rate in the re- cinomas. Great care and experience are needed to current lesion group was 11.1 percent (three of ensure complete excision of these lesions on the 27) (Table 1). These incompletely excised lesions second attempt. were located on the limb, ear, and forehead. The Although age is related to the prevalence of lesion on the forehead was also an invasive lesion. squamous cell carcinoma,4,12 it does not confer a risk of incomplete excision. The mean age of our Re-Excision patients with incomplete resection (74.8 years) was very similar to that of patients with complete A total of 1.9 percent of lesions (10 of 517) resection (75.7 years), contrary to Reid’s12 obser- were referred for re-excision due to previously vations. incompletely excised squamous cell carcinoma. There was a 3:1 male preponderance for cu- Of these 10 lesions, six were again incompletely taneous squamous cell carcinoma. Ang et al.5 excised. All except one were from the head; of stated that being male was associated with a higher these, three were on the cheek and two were on risk of having an incomplete excision. Our data the nose. The only invasive lesion in this group was confirmed this (7.3 percent versus 2.8 percent), located on the cheek and was incompletely ex- although this difference was not statistically sig- cised. In all of these incompletely excised lesions, nificant. It is interesting to note that the distribu- the deep margins were involved; the lateral mar- tion of squamous cell carcinoma has a gender gin was also involved in four of these lesions. disparity. In females, more than half of squamous cell carcinomas were excised from the limbs, DISCUSSION whereas in males, most occurred in the head. This The incidence of squamous cell carcinoma difference was statistically significant (Table 3, p Ͻ increases with age and appears to be related to 0.005) and may be related to the clothing habits cumulative sun exposure.4 For a primary excision, of the sexes. Further larger scale observational the incomplete excision rate ranges from 5.8 per- studies are required to determine whether sex is cent to 15.9 percent.1,3,5–8,10,11 The subsequent like- indeed a risk factor. lihood of recurrence within 5 years ranges from In our series, the head had the highest incom- 5.7 percent to 8.1 percent.2,9 plete excision rate compared with the rest of the At the Peter MacCallum Cancer Institute, sur- body. It was also the site of highest recurrence gical excision is the first-line treatment for resect- after a previous excision. This concurs with the able cutaneous squamous cell carcinoma. Our in- findings of Reid12 but differs from the Singapore complete excision rate, 6.1 percent, compares experience.5 Again, even within the re-excision favorably with that of other series (10.9 percent to group, most (five of six) of the incomplete exci- 15.9 percent).5,9,11 sions occurred on the head. The ear was the third The incomplete excision rate was 6.3 per- most common site of squamous cell carcinoma cent (30 of 480) for primary excisions, 11.1 per- occurrence, and these lesions had the highest rate cent (three of 27) for recurrent lesions, and 60 of incomplete excision (20.5 percent; 95% CI of percent (six of 10) for re-excision of previously odds ratio, 2.16 to 11.93). This was statistically incompletely excised lesions. The differences significant (p Ͻ 0.001, Fisher’s exact) and not were statistically significant for primary excision surprising, given the well-known predilection for and re-excisions (p Ͻ 0.001). As expected, the skin cancers to extend deeply, presumably along lateral margin was most commonly involved, in the embryonic fusion places. The incompleteness

914 Volume 120, Number 4 • Squamous Cell Carcinoma occurs equally at the deep or lateral margins. All sus registrars. We observed that lesions excised by of the ear lesions (n ϭ 44) were excised with 2- to a consultant surgeon had a higher incomplete 5-mm margins. A similar experience was reported excision rate compared with those excised by reg- by Talbot and Hitchcock.1 For the ear, we again istrars (8.5 percent versus 6 percent, respectively) emphasize the need for great care, experience, (p ϭ 0.521, Fisher’s exact). This same observation and consideration of larger excision margins up to was made by Talbot and Hitchcock1 in their study 5 mm where feasible. The nose also had a high comparing the rates of incomplete excision of incomplete excision rate (13 percent), but this was mixed lesions from general practitioners, sur- not statistically significant. geons, and registrars. They suggested that consul- Due to the higher risk of incomplete excision tant surgeons tended to operate on larger lesions in the ear, we strongly recommend orientating the and in more difficult sites compared with general excised specimens, in anticipation of a subsequent practitioners. Again, in a study of a large series of wider excision. We believe a wide margin of at least basal cell carcinomas, Dieu and Macleod,3 ob- 5 mm where feasible, together with careful inspec- served that registrars obtained a lower incomplete tion under good lighting and magnification, is excision rate and opined that selection bias could advisable. be a factor. Our study concurs with these conclu- Tumor size was not associated with a higher sions. incomplete excision rate, contrary to Ang et al.’s The use of local anesthesia is associated with a conclusion.5 In our series, midsize lesions (be- lower incomplete excision rate compared with tween 10 and 20 mm) had a slightly higher risk of general anesthesia (5.9 percent versus 18.8 per- being incompletely excised, although this was not cent). This was not statistically significant. Gener- statistically significant. ally, local anesthesia is preferred for patient fac- There are various guidelines on surgical mar- tors and if tumors are small and simple. However, gins for squamous cell carcinoma. Brodland and we noted earlier that tumor size was not a factor Zitelli6 recommended a 6-mm surgical margin for in incomplete excision. General anesthesia is usu- lesions larger than 20 mm, histological grades 2 ally required if the tumors are considered difficult. through 4, lesions that are located on the scalp, Tumor invasiveness was strongly associated ears, eyelid, nose, or lips, and invasion to the level with incomplete excision of the primary squamous of subcutaneous tissue. Otherwise, they recommend cell carcinoma (p Ͻ 0.001). This was not surpris- a 4-mm margin. Their recommendations are based ing, but unfortunately, invasiveness is a postop- on a study of 141 cases of squamous cell carcinoma erative finding. Further studies correlating clin- excised by Mohs micrographic surgery, to achieve a ical appearance and squamous cell carcinoma 95 percent clearance rate. Similarly, the National behavior may elucidate the importance of this Comprehensive Cancer Network of America’s observation. guideline recommendations for 2000, based on risk Most of the lesions in our series were closed stratification according to location of the lesion, rec- directly. Although there was a lower rate of in- ommended surgical margins starting from 6 mm.7 complete excision for wounds closed directly (5.6 We do no believe such radical margins for all squa- percent) compared with those requiring a flap mous cell carcinoma are warranted. More recently, (8.8 percent) or graft (10.8 percent), this was not Thomas et al.,8 in a prospective study of Mohs mi- statistically significant. crographic surgery, recommended a 4-mm margin Despite histologically cleared margins, occult for nonmelanotic skin cancers up to 20 mm wide residual tumor cells may exist and result in a re- and a 3-mm margin if the tumor’s border was dis- current growth.6,8 In our series, 7.2 percent of tinct, to achieve 97 percent clearance. We agree with cases were recurrent lesions. In a meta-analysis, these recommendations. Alam and Ratner2 reported that squamous cell In our series, we observed that the lesions carcinoma recurrence and metastasis were more treated with wider excision margins, of 5 mm or likely at certain sites, such as the scalp, forehead, more, resulted in no incomplete excisions. These and nose. Rowe et al.9 further stated that squa- results, however, were not statistically significant mous cell carcinoma tends to recur with original because of the small number of patients in this tumor sizes greater than 2 cm, tumor depth of 4 group (p ϭ 1, Fisher’s exact). Furthermore, cau- mm or greater, Clark levels of 4 and 5, poor his- tious interpretation is required because of poten- tological differentiation, sites such as the ear or tial selection bias. lip, perineural involvement, non–sun-exposed Caution is to be exercised in interpreting rates skin, and immunosuppressed patients. In their of incomplete excision by consultant surgeons ver- review article, Rowe et al.9 quoted a postsurgical

915 Plastic and Reconstructive Surgery • September 15, 2007 recurrence rate of 15.7 percent for squamous cell DISCLOSURE lesions larger than 2 cm and 5.8 percent for None of the authors has any financial interest or smaller lesions, for an overall 5-year recurrence commercial associations that might create a conflict of rate of around 8 percent.2,9 In our series, most interest with information presented in this article. recurrent lesions (74.1 percent) were on the head, and the highest proportion were from the ear. Overall, our series showed that recurrent lesions REFERENCES were more likely to be incompletely excised (11 1. Talbot, S., and Hitchcock, B. Incomplete primary excision of percent) than primary excisions, although this was cutaneous basal and squamous cell carcinomas in the Bay of not statistically significant. We do not have infor- Plenty. N. Z. Med. J. 117: 1192, 2004. 2. Alam, M., and Ratner, D. Cutaneous squamous cell carci- mation on the original lesion. noma. N. Engl. J. Med. 344: 975, 2001. 3. Dieu, T., and Macleod, A. M. Incomplete excision of basal CONCLUSIONS cell carcinomas: A retrospective audit. Aust. N. Z. J. Surg. 72: Our large, prospective, observational study had 219, 2002. an incomplete excision rate of 6.3 percent, which 4. Pohl, M. J. Skin cancer. In J. Toouli (Ed.), Integrated Basic compares favorably with published data. Statistically Surgical Sciences. London: Arnold, 2000. Chap. 21.3, pp. 401– 409. significant risk factors were ear lesions, invasive le- 5. Ang, P., Tan, A. W., and Goh, C. L. Comparison of completely sions, and lesions for wider re-excision. For these versus incompletely excised cutaneous SCC. Ann. Acad. Med. high-risk squamous cell carcinomas, we recommend Singapore 33: 68, 2004. careful inspection of the tumor margin with good 6. Brodland, D. G., and Zitelli, J. A. Surgical margins for exci- lighting and magnification, a wider margin (5 mm), sion of primary cutaneous SCC. J. Am. Acad. Dermatol. 27: 241, 1992. and a deeper plane. Referral to more experienced 7. Miller, S. J. The National Comprehensive Cancer Network surgeons should be considered. Factors that may be (NCCN) guidelines of care for nonmelanoma skin cancer. important but did not reach statistical significance Dermatol. Surg. 26: 289, 2000. included male sex, use of general anesthesia, and 8. Thomas, D. J., King, A. R., and Peat, B. G. Excision margins margin of excision. Factors that may be confounding for nonmelanotic skin cancer. Plast. Reconstr. Surg. 112: 57, 2003. included age, size of lesions, method of repair, and 9. Rowe, D. E., Carroll, R. J., and Day, C. L. Prognostic factors experience of the surgeon. for local recurrence, metastasis, and survival rates in squa- mous cell carcinoma of the skin, ear and lip. J. Am. Acad. Pee-Yau Tan, M.B.B.S. Dermatol. 26: 976, 1992. Department of Surgery 10. Stal, S., and Spira, M. Basal and squamous cell carcinoma of Monash Medical Center the skin. In Grabb and Smith’s Plastic Surgery. 5th Ed. Phila- 17 Simpson Drive delphia: Lippincott-Raven, 1997. Pp. 107–120. Mt. Waverly, Victoria 3149, Australia 11. Hallock, G. G., and Lutz, D. A. A prospective study of the [email protected] accuracy of the surgeon’s diagnosis and significance of pos- ACKNOWLEDGMENTS itive margins in non-melanoma skin cancers. Plast. Reconstr. Surg. 107: 942, 2001. The authors are grateful to the plastic surgery consult- 12. Reid, B. Reducing the incomplete excision of non melano- ants Allan Macleod, Darrell Nam, and William Gilbert for cytic skin cancers in Australian general practice. Aust. Fam. their involvement in the data collection process. Physician 29: 278, 2000.

916 RECONSTRUCTIVE

Botulinum Toxin in Facial Palsy: An Effective Treatment for Contralateral Hyperkinesis

Maurı´cio de Maio, M.D. Background: The treatment of facial paralysis aims to recover symmetry in both Ricardo Ferreira Bento, static and dynamic states, which are seriously affected by the progressive con- M.D., Ph.D. tralateral hyperkinesis. Botulinum toxin may be used to reduce facial asymmetry Sa˜o Paulo, Brazil in patients suffering from facial paralysis. Methods: Eighteen patients (12 female and six male patients) with facial palsy and contralateral hyperkinesis were injected with 112.5 units (0.9 ml) of Dysport (botulinum toxin type A) distributed evenly in the muscles of the perioral area. The patients were examined at 14, 28, 42, 56, 90, 150, and 180 days after the injection. Patients evaluated the degree of improvement at each time point. In addition, three evaluators made static (relaxed state) and dynamic (maximum contraction while smiling) assessments using a series of measurements obtained with a digital caliper, and the mean was used as the reference value. Results: The quantitative analysis demonstrated a significant reduction in hy- perkinesis that lasted approximately 180 days. There was a significant or mod- erate improvement in most of the cases. All of the patients were very satisfied with the treatment. Adverse events were short-lived (mainly during the first 15 days) and related to difficulty in drinking without liquid loss (nine of 18) and difficulty in chewing without food loss (three of 18). Conclusion: Injection of botulinum toxin was effective in reducing muscular hyperkinesis in the hemiface opposite that affected by facial paralysis, with mild and short-term side effects. (Plast. Reconstr. Surg. 120: 917, 2007.)

he facial nerve (cranial nerve pair VII) is has not been well defined.3 Patients with facial responsible for stimulating the muscles that paralysis often experience speech impairment Tmimic, creating a balance between the syn- and swallowing or chewing difficulties, and al- ergistic and antagonistic forces that act on the tered facial aesthetics that can affect, in a strik- facial structures. It is also responsible for the ing manner, their ability to express emotion, muscular tonus when a person is in a relaxed such as pleasure.4 Because the ability to generate state and for the voluntary and involuntary con- a smile is key to an individual’s ability to express traction of the muscles on each side of the face.1 acceptance, embarrassment, happiness, delight, The facial nerve innervates the muscles in the and agreement, the facial paralysis patient’s dif- frontal and orbital regions of the face and the ficulty in doing so can negatively affect self- upper and lower lips; these muscles are respon- image5 and compromise their emotional state.6 sible for facial movements and, as a result, for Patients with facial paralysis exhibit common representing human emotions.2 Damage to the characteristics. By comparison with the unaf- facial nerve, which can result from cerebral vas- fected side of the face, the side affected by the cular dysfunctions, iatrogenic or noniatrogenic paralysis has fewer wrinkles (because of a lack of damage caused during operations, or damage muscular traction on the dermis), a less evident resulting from trauma, can cause facial paralysis. nasolabial fold, and a drooping of the corner of Idiopathic or paralysis of unknown origin is the the mouth and the brow. The nonaffected side most frequent type of facial paralysis; its cause of the face responds to the facial paralysis with a hyperkinetic reaction of the muscle tissues attrib- From the Department of Otolaryngology, Faculty of Medicine, utable to the lack of tonus on the paralyzed side. University of Sa˜o Paulo. This imbalance of vectoral forces creates facial Received for publication November 22, 2005; accepted deviations that are observed when the patient is March 17, 2006. at rest or is attempting to smile (Fig. 1). Copyright ©2007 by the American Society of Plastic Surgeons The muscles on the paralyzed side of the face DOI: 10.1097/01.prs.0000244311.72941.9a do not move. As a result, there is an imbalance

www.PRSJournal.com 917 Plastic and Reconstructive Surgery • September 15, 2007

techniques for suspending or resecting skin, such as rhytidectomy, blepharoplasty, and cor- rection of lagophthalmos, can further improve the aesthetic results.17–20 Botulinum toxin blocks the release of neuro- transmitters that innervate muscles and cause them to contract.21 When injected into facial mus- cles, botulinum toxin has been found to reduce the facial asymmetry encountered in patients suf- fering from facial paralysis22 and has being used to treat synkinesis,23–25 hyperlacrimation,26,27 hyperkinesis,28 and frontal and marginal mandib- ular impairment after rhytidectomies.29,30 The re- sults of the treatment for synkinesis and hyperlac- rimation in facial paralysis patients have been so significant that botulinum toxin is considered by some to be the best treatment with which to coun- teract the motor and autonomic effects caused by 26,27 Fig. 1. A 50-year-old man with facial paralysis and facial asym- aberrant neural regeneration. metryasaresultofabraintumorin1991.Therightsideofhisface Botulinum toxin type A has been developed 31 demonstrates hyperkinesias. The left side is paralyzed, and the for cosmetic and therapeutic use in the face. right side exhibits overcontraction during smiling. The nonpara- The objective of this study was to evaluate the lyzed side presents the distortion in both static and dynamic role of botulinum toxin type A in the treatment states, and it was this overcontraction that was treated. of facial muscular hyperkinesis on the side op- posite that affected by facial paralysis to restore facial symmetry. between the sides of the face. The muscles on PATIENTS AND METHODS the nonparalyzed side of the face, having no This study was approved by the Ethics Com- muscular opponent, overcontract. The nonpara- mittee of the Clinics Hospital of the Medical lyzed side of the face presents deviations in the School of the University of Sao˜ Paulo on Septem- labial, nasal, and orbital regions, even when the ber 10, 2003 (no. 690/03). Eighteen patients (12 muscles are in a relaxed state. In these cases, female patients and six male patients), with a facial rotation occurs toward the side of the face mean age of 40.3 years (range, 17 to 70 years), who that has not been affected, making the nonpara- had been suffering from facial paralysis on one lyzed side of the face shorter. side of the face for a period for more than 1 year Treatment of facial paralysis seeks to reestab- were included in the study. The cause included lish the symmetry of the mouth in the person’s four cases of unknown origin, eight cases of tumor smile and to obtain the contraction of the oral ablation, one case with a congenital origin, and and palpebral sphincters, which are the most five caused by traumas (one physical fight, two important elements in the facial aesthetics that gunshot wounds, one car accident, and one fall are lost. In the acute phase, idiopathic palsy may from a height). None of the patients received con- be treated with the steroid dexamethasone as a current treatment on the opposite side of the par- conservative treatment for facial paralysis, al- alyzed face. Patients were specifically told to avoid though it may promote no significant differ- the use of aspirin or anticoagulant drugs before ences in recuperation time.7 Current techniques treatment. for treating facial paralysis include nerve grafts, The patients were injected with botulinum muscle transfers, myofunctional approaches, toxin type A (Dysport, Speywood Biopharm Ltd. and microsurgical patches, which unfortunately for Beaufour-Ipsen International, Paris, France). are not able to grant the patient facial Dysport is made up of lyophilized powder and balance.8–14 The best results are obtained contains 500 (nominal) units of botulinum toxin through a variety of techniques, including reduc- type A. The drug was reconstituted in 4 ml of 0.9% ing the hyperactivity (hyperkinesis) of the non- sodium chloride solution to yield a concentration affected side through selective myotomy, myec- of 12.5 units of Dysport for each 0.1 ml of resus- tomy, or neurectomy.15,16 The addition of pended solution. The dose of Dysport was deter-

918 Volume 120, Number 4 • Botulinum for Facial Hyperkinesis mined from a pilot study. The drug was adminis- tered by means of intramuscular injection with a 30½-gauge insulin needle inserted at a 45-degree angle from the skin’s surface. No topical anesthe- sia was necessary, although in more sensitive pa- tients, EMLA Cream (AstraZeneca, London, En- gland) may be applied. A total of 112.5 units (0.9 ml) was injected into each patient’s facial muscles on the nonaffected side of the face as follows: 12.5 units (0.1 ml) into the zygomatic major and 6.25 units (0.05 ml) into the zygomatic minor muscles at their points of origin; 6.25 units (0.05 ml) into the levator labii superioris alaeque nasi muscle at the level of the nasal arch; 6.25 units (0.05 ml) into the levator labii superioris muscle at the orbital mar- gin; 12.5 units (0.1 ml) into the modiolus area 0.5 cm from the corner of the mouth; 25 units (0.2 ml) into the risorius muscle 2 cm from the corner of the mouth; 25 units (0.2 ml) into the depressor anguli oris muscle 5 cm from the corner of the mouth; and 18.75 units (0.15 ml) into the depres- sor labii inferioris 1 cm from the mucic-cutaneous Fig. 2. Locations for facial injections of Dysport: 1, zygomatic transition. Facial anatomical landmarks and in- major; 2, zygomatic minor; 3, levator labii superioris; 4, levator structing the patients to contract and relax the labii superioris alaeque nasi; 5, risorius; 6, modiolus area; 7, de- facial muscles was sufficient to ensure the location pressor anguli oris; and 8, depressor labii inferioris. of the muscles so that injections could be given at the exact location. All patients were treated with the same dose in the same areas (fixed dose and uals vary in both side-to-side facial symmetry and locations). Figure 2 shows the locations of the in their ability to execute different facial ex- injections. Patients were told to avoid massaging pressions. Facial expressions are a function of the injection sites after treatment. the relationship between muscle electrical ac- Patients were evaluated 14, 28, 42, 56, 90, 150, tivity and skin motion.32 Linear measurement is and 180 days after the Dysport injection. Patients a technique that involves measuring facial dis- were informed that, regardless of the date of their tances from reference landmarks.33,34 This sys- previous visit, they should contact the investigator tem is used to quantify facial motion and has to schedule an appointment to confirm that been developed to remove the human factor of muscle contraction was completely regained. Pa- judgment. Distance changes observed on the tients were photographed at each visit using a surface of the face reflect the force generated by digital camera in the relaxed condition and in the facial muscles.33 Quantitative measurements maximum muscular contraction (dynamic state) were taken by three evaluators with a digital while smiling. caliper [Mitutoyo, model MIP/E, code no. 500- The patients were clinically assessed before 143B (Mitutoyo, Tokyo, Japan); resolution, 0.01 treatment for the cause of the facial paralysis: mm/nominal capacity; 150 mm/precision; er- health problems, such as neurologic disorders and ror margin, Ϯ00.02 mm; repetitivity, 0.01 mm] acute myasthenia; previous operations; and treat- at three axes, X, Y, and Z, and the mean was used ments received on the hemiface suffering from as the reference value. For the X axis, measure- facial paralysis and on the opposite, nonaffected ment X1 corresponds to the distance between side. At each visit following treatment, the patients the endocanthion (inner corner of the ocular were objectively (quantitative) and subjectively rim) to the cheilion (corner of the mouth) when (qualitative) evaluated to determine the effect and the patient’s face is relaxed, and measurement tolerability of the treatment. X2 corresponds to the same distance when the The objective evaluation entailed static (re- patient is smiling (maximum contraction). For laxed) and dynamic (maximum muscle contrac- the Y axis, measurement Y1 corresponds to the tion during smile) evaluations on the hemiface distance between the exocanthion (outer cor- opposite the side with facial paralysis. Individ- ner of the ocular rim) and the cheilion when the

919 Plastic and Reconstructive Surgery • September 15, 2007 patient’s face is relaxed, and measurement Y2 RESULTS corresponds to the same distance when the pa- The X axis measured the distance between the tient is smiling (maximum contraction). For the cheilion and the endocanthion in static and dy- X axis, measurement Z1 corresponds to the dis- namic states. Measurements were obtained for tance between the tragion (region of the tragus) static and dynamic states for patients from day 0 to the cheilion when the patient’s face is relaxed until day 180. For both states, the greatest mea- and measurement Z2 corresponds to the same surement (indicative of greatest correction of hy- distance when the patient is smiling (maximum perkinesis) was observed at day 28. Before injec- contraction). The measurements are shown in tion, the mean difference between the static and Figure 3 (static and dynamic states). The differ- Ϯ ence between each static and dynamic measure- dynamic measures for the X axis was 4.5 1.86 ment (change in millimeters) was analyzed mm. This difference continued to decrease until 35,36 day 28 (2.35 Ϯ 1.45 mm) (Fig. 4). The period of through a curve. Objective analyses were un- Ͻ dertaken by three observers, and the mean was action was statistically significant (p 0.00001, used as the reference value. The axes were mea- analysis of variance). Multiple comparisons re- sured at the same points according to the an- vealed statistically significant differences between ϭ thropometry of the face: en–ch, ex–ch, and tr– ch, the measurement on day 0 and days 14 (p both in static and dynamic positions.37 The mea- 0.00023), 28 (p ϭ 0.00014), 42 (p ϭ 0.00044), 56 surement landmarks did not change during the (p ϭ 0.00044), 90 (p ϭ 0.00037), and 150 (p ϭ evaluations. 0.0037). Subjective evaluations were made by the pa- The Y axis measured the distance between the tients at all visits. The degree of improvement in cheilion and the exocanthion in static and dy- appearance was analyzed using the following namic states. Measurements were obtained for scale: worsening (Ϫ1), lack of improvement (0), static and dynamic states for patients from day 0 slight improvement (1), moderate improve- until day 180. For both states, the greatest mea- ment (2), or significant improvement (3). The surement (indicative of correction of hyperkine- patient’s satisfaction with the treatment results sis) was observed at day 42. Before injection, the was also undertaken through the following mean difference between the static and dynamic scale: dissatisfied (0), satisfied (1), or very sat- measures for the Y axis was 8.07 Ϯ 3.23 mm. This isfied (2). The statistical testing adopted was difference continued to decrease until day 42 that of the Hartley test to check the homoge- (3.81 Ϯ 2.35 mm) (Fig. 5). The period of action neity of the variances and, subsequently, to an- was statistically significant (p Ͻ 0.00001, analysis of alyze the variance of measurements repeated in variance). Multiple comparisons revealed statisti- one factor (analysis of variance) and the New- cally significant differences between the measure- man-Keuls test for multiple comparisons. Ad- ϭ ϭ verse events were ascertained at all study visits. ment on day 0 and days 14 (p 0.00012), 28 (p

Fig.3. LocationsoffociX1,Y1,andZ1(left,static)andX2,Y2,andZ2(right,dynamic)ona60-year-oldwomanwithfacialparalysis as a result of a meningioma. The left side of her face demonstrates hyperkinesia.

920 Volume 120, Number 4 • Botulinum for Facial Hyperkinesis

Fig.4. MeandifferenceinmeasurementoftheXaxisinpatientsbetweenstaticanddynamicstates; the shortest distance between both measures was observed on day 28.

Fig.5. MeandifferenceinmeasurementoftheYaxisinpatientsbetweenstaticanddynamicstates; the shortest distance between both measures was observed on day 42.

0.00012), 42 (p ϭ 0.00012), 56 (p ϭ 0.00014), 90 significant differences between the measurement (p ϭ 0.00011), and 150 (p ϭ 0.00039). on day 0 and days 14 (p ϭ 0.00014), 28 (p ϭ The Z axis measured the distance between the 0.00012), 42 (p ϭ 0.00012), 56 (p ϭ 0.00012), 90 cheilion and the tragion in static and dynamic (p ϭ 0.00011), 150 (p ϭ 0.00012), and 180 (p ϭ states. Measurements were obtained for static and 0.0014). dynamic states for patients from day 0 until day To evaluate the loss of Dysport action over 180. For both states, the greatest measurement time, the proportion of differences between the (indicative of correction of hyperkinesis) was ob- static and dynamic measures was calculated for served at day 42. Before injection, the mean dif- each visit and compared with the value measured ference between the static and dynamic measures before injection. For the X axis, the best result was for the Z axis was 12.88 Ϯ 4.40 mm. This differ- observed on day 28 (mean difference between the ence continued to decrease until day 42 (5.49 Ϯ static and dynamic measures versus the static and 2.44 mm) (Fig. 6). The period of action was sta- dynamic measures on day 0, 46.86 Ϯ 34.25). By tistically significant (p Ͻ 0.00001, analysis of vari- comparison to the result on day 28, the percentage ance). Multiple comparisons revealed statistically loss of action was 26.6 percent on day 42, 26 per-

921 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 6. Mean difference in measurement of the Z axis in patients during static and dynamic states; the shortest distance between both measures was observed on day 42.

Fig. 7. Differences between static and dynamic measures for the X axis at each visit compared with day 0.

cent on day 56, 26.2 percent on day 90, 38.9 per- action was 4.9 percent on day 56, 23.2 percent on cent on day 150, and 94.7 percent on day 180 (Fig. day 90, 45 percent on day 150, and 69.7 percent 7). For the Y axis, the best result was observed on on day 180 (Fig. 9). day 14 (mean difference between the static and Results for two patients are provided in Figures dynamic measures versus the static and dynamic 10 and 11. The photographs reveal visual improve- measures on day 0, 52.87 Ϯ 20.09). By comparison ment in terms of facial symmetry in both static and with the result on day 14, the percentage loss of dynamic states. Before injection, there is a devia- action was 3.4 percent on day 28, 5.7 percent on tion of both the nose and the lips and the teeth are day 42, 19.9 percent on day 56, 19.1 percent on day evident. After injection, the patients demonstrate 90, 55.8 percent on day 150, and 84 percent on day facial balance in both the nose and lips and the 180 (Fig. 8). For the Z axis, the best result was teeth are not unnaturally exposed. obtained on day 42 (mean difference between the In terms of patient satisfaction, 17 of 18 pa- static and dynamic measures versus the static and tients (94 percent) reported that they were sat- dynamic measures on day 0, 55.10 Ϯ 19.79). By isfied or very satisfied with their results on day comparison with the result on day 42, the loss of 14. All patients reported that they were satisfied

922 Volume 120, Number 4 • Botulinum for Facial Hyperkinesis

Fig. 8. Differences between static and dynamic measures for the Y axis at each visit compared with day 0.

Fig. 9. Differences between static and dynamic measures for the Z axis at each visit compared with day 0. or very satisfied with their results on days 28, 42, Every effort was made to identify potential ad- 56, 90, and 150. This decreased to 94 percent verse events, irrespective of whether such events (17 of 18) on day 150 and to 78 percent (14 of were deemed to be related to treatment. Compli- 18) on day 180. The improvement in appear- cations were initially observed at day 7 when re- ance noted by each patient increased gradually. laxation of the muscles was first observed. By day On day 14, 13 of 18 (72 percent) reported a 14, almost 100 percent of the muscle relaxation moderate or significant improvement. Patient was obtained and a dramatic change in muscular improvement was graded as moderate or signif- coordination occurred. Sixteen of 18 patients (89 icant by all patients (18 of 18) on days 28, 42, 56, percent) experienced at least one adverse event at and 90. On day 150, 13 of 18 patients (72 per- the treated area, which was considered by all of the cent) reported a moderate or significant im- patients to be mild and directly related to the provement. On day 180, 10 of 18 patients (56 abrupt blocking of the perioral muscles. Mild dif- percent) reported a moderate or significant im- ficulty in drinking without liquid loss (no oral provement. There was a statistically significant incontinence for liquids) was reported by nine of improvement between day 14 and day 90 (p Ͻ 18 patients (50 percent); mild difficulty in chew- 0.0005, Friedman test). ing without food loss (no oral incontinence for

923 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 10. Before injection, a 29-year-old woman with paralysis of unknown origin demonstrates deviation of the nose and lips and visible teeth (left). The right side of her face demonstrates hyperkinesia. Four months after injection, the patient demon- strates facial balance and normal presentation of teeth (right).

Fig. 11. Before injection, a 32-year-old woman with facial paralysis as a result of a brain tumor demonstrates an overcontrac- tion of the lateral and upper levators of the mouth (left). The right side of her face demonstrates hyperkinesia. One month after injection, the patient demonstrates a balanced smile (right). solids) was reported by three of 18 patients (17 relaxed and dynamic states. Current treatments percent); difficulties in speaking or swallowing was are unpredictable in terms of providing aesthetic reported by six of 18 patients (33 percent); and and functional improvement to facial paralysis difficulties while trying to kiss or pucker lips was patients.8,11,32,38–40 Facial symmetry is often en- reported by three of 18 patients (17 percent). hanced in the static state, but the dynamics are still These conditions ultimately resolved. On day 90, imbalanced because of the absence of movement one patient still complained of difficulty in drink- on the paralyzed hemiface and the hyperkinesis ing, one complained of difficulty speaking quickly, on the opposite side.41 In addition, treatment of and one complained of pain while talking. Four contralateral hyperkinesis by neurectomies, my- patients were found to have deviation of the ectomies, or myotomies may produce complica- mouth to the hyperkinetic side beginning at day tions such as paresthesia, hyperesthesia, partial 150, which is indicative of the beginning of the loss paresis, asymmetry, and incomplete corrections of the effect. and recurrence, without achieving appropriate fa- cial balance.15,16,42–44 DISCUSSION Botulinum toxin prevents muscle contraction. The process of rehabilitation in facial paral- The injection of botulinum toxin in the facial ysis aims at recovering facial symmetry in both muscles for the treatment of facial paralysis pa-

924 Volume 120, Number 4 • Botulinum for Facial Hyperkinesis tients has been described in the medical literature patients reported difficulties in speaking or swal- and has been found to be very successful in the lowing. The mechanism of difficulties in swallow- temporary relief of their symptoms.22,41 In this in- ing was not investigated in this study, but it is likely vestigation, 18 patients were injected with a total to be because one side of the face is paralyzed and of 0.9 ml (112.5 units) of Dysport botulinum the muscles on the other side of the face com- type A into the muscles that control the nasal pensate for swallowing and chewing. For example, arch, the upper and lower lips, and the corners it is not uncommon for some mimetic muscles to of the mouth. Exact muscular blocking was ob- be adjunctive to function, such as the orbicularis tained because of the low diffusion rate of bot- oris, orbicularis oculi, and platysma muscles. Fa- ulinum toxin type A.45 These are the muscles cial palsy presents a complete rearrangement of responsible for generating a smile and register- muscular behavior for the face, and as a result, ing emotion on the face. The objective of the nerve blocking with Dysport may alter previous injection was to create balance with the para- adaptations for drinking, eating, speaking, and so lyzed side of the face by weakening, in a uniform forth. For most patients, the alterations were matter, the forces that act on the region of the found to be much improved at later visits, dem- oral sphincter. All of the patients in this study onstrating that the patients were able to adapt to showed a significant reduction in muscular ac- the abrupt change in the muscles that control tivity as evidenced by increased measurements facial expression. One patient complained of pain of the X, Y, and Z axes in static and dynamic while talking. This pain is likely to be a result of the states at most time periods. The onset of im- patient using the muscles on just one side of the provement was observed on day 7. Optimal im- face to compensate for an activity (talking) that provement (defined as the time of maximum normally requires action by muscles on both sides contraction of muscles) was observed on day 28 of the face. It is likely that the persistence and (X axis), day 42 (Y axis), and day 42 (Z axis). intensity of the adverse events were related to the The delay in improvement is likely to be a func- dose injected and the gravity of the facial palsy and tion of the type and size of the muscles and the contralateral hyperkinesias. It may be possible the degree of hyperkinesia. Differences among to reduce the prevalence of adverse events if the the axes are likely to represent differences in the treatment is undertaken in two steps. It is also degree of contraction and muscle size. In addi- important for patients to have muscular training tion, the Y and Z axes are longer than the X axis. before and after the procedure so that they can Furthermore, a great majority of patients re- better adapt to the change in movement. ported moderate or significant improvements in The dosage of botulinum toxin examined in appearance on all study days (72 percent on day this study (a total of 112.5 units) may have been 14; 100 percent on days 28, 42, 56, 90; 72 percent too small for some patients to totally control their on day 150; and 56 percent on day 180). This hyperkinesis or even too strong such that it caused observation is consistent with a study by May et adverse events. In clinical practice, it may be pru- al.44 that found that 100 percent of patients with dent to begin with small doses and, if necessary, Bell’s palsy were successfully treated with botu- complement them after 15 days to minimize the linum toxin compared with 92 percent of pa- incidence of complications. tients treated surgically. The vast majority of Administration of botulinum toxin is a proce- patients in our study were very satisfied with the dure that can be conducted in the physician’s treatment at all time periods. office without the need for local anesthesia. This Adverse events are rare with facial injections of study demonstrates that facial injection of botuli- botulinum toxin46 and are generally linked to high num toxin improves the facial aesthetics of facial doses.47 In this study, there were no early compli- paralysis patients with few and limited adverse cations such as hematomas, infections, or allergies events. This treatment may be an indispensable to the botulinum toxin, nor did irreversible com- resource as a nonsurgical treatment, as a thera- plications occur. Fifty percent of the patients com- peutic test, or as a complementary measure in plained of mild difficulty in drinking without liq- postsurgical treatments, after patients have under- uid loss or chewing without food loss and gone neurectomies or myectomies. Botulinum difficulties in speaking and smiling at the day-14 toxin should be considered a treatment for tem- visit (14 days after the injection). Around this porary or permanent asymmetries in patients who time, patients had to learn to coordinate the suffer from facial palsy,48 particularly in children muscles, and the rate of adverse events decreased and adolescents where the effects of facial palsy dramatically thereafter. Thirty-three percent of during musculoskeletal development are well

925 Plastic and Reconstructive Surgery • September 15, 2007 known, as are the distortions that result from this 12. Kermer, C., Millesi, W., Paternostro, T., et al. Muscle-nerve- condition. Clear documentation and adult con- muscle neurotization of the orbicularis oris muscle. J. Crani- omaxillofac. Surg. 29: 302, 2001. sent are critical when this treatment is used in 13. Labbe, D. Lengthening temporalis myoplasty. Rev. Stomatol. children. Chir. Maxillofac. 103: 79, 2002. 14. Bernardes, D. F. F., Gomez, M. V. S., Pirana, S., and Bento, R. F. Functional profile in patients with facial paralysis CONCLUSIONS treated in a myofunctional approach. Pro Fono 16: 151, 2004. 15. Muhlbauer, W., Fairley, J., and van Winderger, J. Mimetic A significant reduction in muscular hyperki- modulation for problem creases of the face. Aesthetic Plast. nesis was obtained with botulinum toxin (Dys- Surg. 19: 183, 1995. port). Overall aesthetic appearance was improved, 16. Dobie, R. A., and Fisch, U. Primary and revision surgery especially on dynamic analyses. Most of the pa- (selective neurectomy) for facial hyperkinesia. Arch. Otorhi- tients had an excellent improvement and were nolaryngol. Head Neck Surg. 112: 154, 1986. 17. Moser, G., and Oberascher, G. Reanimation of the paralyzed very satisfied with the treatment. Adverse events face with new gold weight implants and Goretex soft-tissue improved progressively as patients adapted to patches. Eur. Arch. Otorhinolaryngol. 1: S76, 1997. their new ability to express emotion. 18. Adant, J. P. Endoscopically assisted suspension in facial palsy. Plast. Reconstr. Surg. 102: 178, 1998. Mauricio de Maio, M.D. 19. Wong, G. B., Stokes, R. B., Stevenson, T. R., et al. Endoscop- Av. Ibirapuera, 2907 - cj. 1202 ically assisted facial suspension for the treatment of facial Moema, Sa˜o Paulo 04029-200, Brazil palsy. Plast. Reconstr. Surg. 103: 970, 1999. [email protected] 20. Shumrick, K. A., and Pensak, M. L. Early perioperative use of polytef suspension for the management of facial paralysis after extirpative skull base surgery. Arch. Facial Plast. Surg. 2: DISCLOSURES 243, 2000. Neither of the authors has any commercial associa- 21. Sulica, L. Botulinum toxin: Basic science and clinical uses in otolaryngology. Laryngoscope 111: 218, 2001. tions, including consultancies, stock ownership or other 22. Neuenschwander, M. C., Pribitkin, E. A., and Sataloff, R. T. equity interests, or patent licensing arrangements, or Botulinum toxin in otolaryngology: A review of its actions received payments for conducting or publicizing the study and opportunity for use. Ear Nose Throat J. 79: 788, 2000. described in this article. 23. Badarny, S., Giladi, N., and Honigman, S. Botulinum toxin injection effective for post-peripheral facial nerve palsy syn- kinesis. Harefuah 135: 106, 1998. REFERENCES 24. Sadiq, S. A., and Downes, R. N. A clinical algorithm for the 1. Aviv, J. E., and Urken, M. L. 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Indication, technique and results treatment of crocodile tears by injection of botulinum toxin of facial nerve reconstruction. Acta Neurochir. 130: 125, 1994. into the lacrimal gland: A case report. Ophthalmology 106: 5. Boerner, M., and Seiff, S. Etiology and management of facial 2322, 1999. palsy. Curr. Opin. Ophthalmol. 5: 61, 1994. 28. Dressler, D., and Schonle, P. W. Hyperkinesias after hypo- 6. Dawidjan, B. Idiopathic facial paralysis: A review and case glossofacial nerve anastomosis: Treatment with botulinum study. J. Dent. Hyg. 75: 316, 2001. toxin. Eur. Neurol. 31: 44, 1991. 7. Bento, R. F., Bogar, P., and Lorenzi, M. C. Treatment com- 29. Clark, R. P., and Berris, C. E. Botulinum toxin: A treatment parison between dexamethasone and placebo for idiopathic for facial asymmetry caused by facial nerve paralysis. Plast. palsy. Eur. Arch. Otolaryngol. Dec.: S535, 1994. Reconstr. Surg. 84: 353, 1989. 8. Fine, N. A., Pribaz, J. J., and Orgill, D. P. Use of the innervated 30. Tulley, P., Webb, A., Chana, J. S., et al. Paralysis of the platysma flap in facial reanimation. Ann. Plast. Surg. 34: 326, marginal mandibular branch of the facial nerve: Treatment 1995. options. Br. J. Plast. Surg. 53: 378, 2000. 9. Guereissi, J. O. Selective myectomy for postparetic facial 31. Carruthers, A., and Carruthers, J. Botulinum toxin type A: synkinesis. Plast. Reconstr. Surg. 87: 459, 1991. History and current cosmetic use in the upper face. Semin. 10. Ueda, K., Hari, K., Asato, H., et al. Evaluation of muscle graft Cutan. Med. Surg. 20: 71, 2001. using facial nerve on the affected side as a motor source in 32. Kukwa, A., Marchel, A., Pietniczka, M., et al. Reanimation of the treatment of facial paralysis. Scand. J. Plast. Reconstr. Surg. the face after facial nerve palsy resulting from resection of a Hand Surg. 33: 47, 1999. cerebellopontine angle tumor. Br. J. Neurosurg. 8: 327, 1994. 11. Terzis, J. K., and Kalantarian, B. Microsurgical strategies in 33. Burres, S. A. Facial biomechanics: The standards of normal. 74 patients for restoration of dynamic depressor muscle Laryngoscope 95: 708, 1985. mechanism: A neglected target in facial reanimation. Plast. 34. Burres, S., and Fisch, U. The comparison of facial grading Reconstr. Surg. 105: 1917, 2000. systems. Arch. Otolaryngol. Head Neck Surg. 112: 755, 1986.

926 Volume 120, Number 4 • Botulinum for Facial Hyperkinesis

35. Burres, S. A. Objective grading of facial paralysis. Ann. Otol. 43. Harii, K., Asato, H., Yoshimura, K., et al. One-stage transfer Rhinol. Laryngol. 95: 238, 1986. of the latissimus dorsi muscle for reanimation of a paralyzed 36. Burres, S. A. The qualification of synkinesis and facial pa- face: A new alternative. Plast. Reconstr. Surg. 102: 941, 1998. ralysis. Eur. Arch. Otolaryngol. Dec.: S177, 1994. 44. May, M., Croxson, G. R., and Klein, S. R. Bell’s palsy: Man- 37. Farkas, L. G. Anthropometry of the Head and Face, 2nd Ed. New agement of sequelae using EMG rehabilitation, botulinum York: Raven Press, 1997. Pp. 545–557. toxin, and surgery. Am. J. Otol. 10: 220, 1989. 38. Kumar, P. A. Cross-face reanimation of the paralysed face 45. Dodd, S. L., Rowell, B. A., Vrabas, I. S., et al. A comparison with a single stage microneurovascular gracilis transfer with- of the spread of three formulations of botulinum neurotoxin out nerve graft: A preliminary report. Br. J. Plast. Surg. 48: 83, A as determined by effects on muscle function. Eur. J. Neurol. 1995. 5: 181, 1998. 39. Kozak, J., Voska, P., and Tichy, M. Contemporary state of 46. Laskawi, R. Combination of hypoglossal-facial nerve anasto- surgical treatment of facial nerve paresis: Preliminary expe- mosis and botulinum toxin injections to optimize mimic rience with new procedures. Acta Chir. Plast. 39: 125, 1997. rehabilitation after removal of acoustic neurinomas. Plast. 40. Bikhazi, N. B., and Maas, C. S. Refinement in the rehabili- tation of the paralyzed face using botulinum toxin. Otolar- Reconstr. Surg. 99: 1006, 1997. yngol. Head Neck Surg. 117: 303, 1997. 47. Armstrong, M. W., Mountain, R. E., and Murray, J. A. Treat- 41. Faria, J. C. M. A Critical Study of the Treatment of Facial Palsy ment of facial synkinesis and facial asymmetry with botuli- through a Gracilis Transfer (doctoral thesis). Sao Paulo: Med- num toxin type A following facial nerve palsy. Clin. Otolar- ical College, University of the State of Sao Paolo, 2002. yngol. 21: 15, 1996. 42. Arden, R. L., and Sunhat, P. K. Vertical suture placation of 48. Ueda, K., Hari, K., Asato, H., et al. Neurovascular free muscle the orbicularis oris muscle: A simple procedure for the cor- transfer combined with cross-face nerve grafting for the treat- rection of unilateral marginal mandibular nerve paralysis. ment of facial paralysis in children. Plast. Reconstr. Surg. 101: Facial Plast. Surg. 14: 173, 1998. 1765, 1998.

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927 RECONSTRUCTIVE

Sternotomy Wounds: Rectus Flap versus Modified Pectoral Reconstruction

Steven P. Davison, M.D., Background: Infected sternotomy wounds occur in 0.5 to 8.4 percent of open D.D.S. heart operations. They are complex problems, with a mortality rate of 8.1 to 14.8 Mark W. Clemens, M.D. percent despite flap closure. For closure, the pectoralis major flap has had Deana Armstrong, M.D. considerable success. However, in providing coverage to the lower third of the Ernest D. Newton, M.D. sternum, it may be deficient. Modifications to improve closure have included a William Swartz, M.D. rectus flap or an anterior rectus fascia extension to the pectoralis flap. Pittsburgh, Pa.; and Washington, Methods: This retrospective study of 130 consecutive sternotomy wounds com- D.C. pares 41 bilateral pectoralis major muscle flaps with a modified anterior rectus fascia extension against 56 rectus abdominis muscle flaps alone in addressing the lower third of the sternum following dehiscence. Results: Pectoralis flaps with rectus fascia extension and rectus flaps have similar success, postoperative course, and morbidity and mortality rates. The pectoralis flaps with rectus fascia extensions prevented superior dehiscence, but this mod- ification does not eliminate dehiscence of the distal third of the sternum. Conclusions: The rectus muscle alone proved superior in coverage to the in- ferior sternum. Sternal wounds should be covered preferentially by a pectoralis flap to cover a superior infection and by a rectus flap if the dehiscence is localized to the distal third. (Plast. Reconstr. Surg. 120: 929, 2007.)

edian sternotomy is one of the most search for the most effective method of treat- common operations performed today. It ment. Mis the preferred approach to the ante- The treatment options in the past ranged rior mediastinum and for surgical treatment of from leaving the wound open to heal by second- coronary artery disease. The sternum becomes ary intention to debridement and rewiring cou- infected postoperatively in 0.5 to 8.4 percent1–19 pled with antibiotic irrigation therapy.18,24,25 In of open heart operations, leading to the possible the past quarter century, well-vascularized flaps sequelae of osteomyelitis, dehiscence, and have been shown to provide stable coverage to death. Sternotomy wounds are complex prob- the sternotomy wound after radical debride- lems because of their proximity to the heart, ment. In 1976, Lee et al. initiated the idea of an lungs, and abdominal cavity and the lack of cov- omental flap for closure of this deficit.26 In 1980, erage to these vital organs following debride- Jurkiewicz et al. reported the use of pectoral ment. They have mortality rates of 8.1 to 14.8 muscle flaps.4 These treatment strategies have in- 1–3,6,10,14,17,18,20 percent. Hospital stays are pro- creased long-term success from 50 percent4,12,26 to longed by a mean of 30 days, but can take 5.5 1,2,5,17,27,28 1,17,18,21 now 90 to 99 percent. The average length months, with up to four reoperations. The of hospital stay has dropped from 84 days to under cost of an infected sternotomy doubles to qua- 2,4–6,9,17,29 1,22,23 13 days. Although the sternum is normally druples hospital expenses. The significant lacking muscular coverage, in treating an infected morbidity and mortality associated with sternot- sternum, the use of muscle flaps has substantially omy infections has spurred a longstanding reduced both hospital stay and mortality from this From West Penn Hospital, Shadyside Hospital, and the difficult problem. In addition, the muscle provides Division of Plastic and Reconstructive Surgery, Georgetown structural protection to the vital structures beneath University Medical Center. following massive sternal debridement. Received for publication January 3, 2006; accepted February Pectoralis major and rectus abdominis have 17, 2006. become first-line flaps,30 with the pectoral fa- Copyright ©2007 by the American Society of Plastic Surgeons vored between the two.3,9 The omentum is gen- DOI: 10.1097/01.prs.0000253443.09780.0f erally thought of as a second-line treatment

www.PRSJournal.com 929 Plastic and Reconstructive Surgery • September 15, 2007 choice.30 A major limitation of the pectoralis was closed, and a two-layer closure of the abdom- major flap has been coverage of the inferior inal area was completed. third of the sternotomy wound.7,8,14,31–35 It is the The pectoralis major flap, modified with an- most common site for dehiscence after flap terior rectus fascia, was harvested through the repair.2,14,26,30,31,34–36 midline sternotomy incision extended 5 cm infe- In this study, the authors evaluated two differ- riorly. A plane was developed between the pecto- ent flap options that address the inferior third of ralis and the subcutaneous tissue bilaterally to the the sternotomy wound. The two senior authors mid nipple line. Both pectoralis muscles were (S.P.D. and M.W.C.) have independently used sharply elevated from their costal and sternal in- either a rectus abdominis flap alone or a modi- sertions, continuing the dissection in a subpec- fied pectoralis major flap with anterior rectus toral plane to allow bilateral advancement to the sheath extension for coverage of dehisced ster- midline without tension. The humeral attach- notomy wounds. The purpose of this article is to ments of the pectoralis muscles were left intact compare these two treatment protocols in terms and the thoracoacromial arteries were carefully of efficacy and complications focusing on the preserved. The internal mammary artery perfora- lower third of the sternum. tors were clipped or coagulated. The insertion of the pectoralis muscles was released with preserva- tion of the long thoracic artery to aid in a tension- PATIENTS AND METHODS free closure. In the inferomedial portion, the pec- This is a retrospective review of two series of toral muscle was elevated in continuity with the consecutive patients treated for infected sternot- anterior rectus fascia, leaving the rectus muscle omy wounds. Each series used a different tech- undisturbed. The rectus fascia was lifted up with nique on a similar demographic patient popula- the pectoralis fascia. At least 5 cm of the anterior tion (age range, 52 to 86 years; mean, 67.5 years) rectus fascia to the first imbrication was harvested. at adjacent medical facilities. Both hospitals serve Inferiorly, the anterior rectus fascia is separated equal income populations. from the rectus (Fig. 1). The pectoralis muscles Hospital records were reviewed for patients were imbricated medially. A two-layer closure of treated for sternal dehiscence/infection from Jan- the subcutaneous tissue and skin complete the uary of 1985 to December of 1998. Chart review procedure. Both reconstruction techniques were evaluated flap technique, postoperative success, used after aggressive staged debridement. Only recovery time, reoperation rate, morbidity, and very mild infections limited to superficial dermis mortality. A postdischarge written survey com- and subcutaneous soft tissue were debrided and pleted follow-up results. Follow-up was limited to closed in one stage. Drains were used and intra- 2 to 4 years (average, 2.8 years). Results were an- venous antibiotics were given for 3 to 6 weeks after alyzed using the Fisher’s exact test. surgery. The rectus flap closure was based on the su- perior epigastric pedicle. The sternotomy incision RESULTS was continued inferiorly 3 cm lateral to the um- A total of 130 patients with sternotomy wounds bilicus directly over the rectus. During rectus har- were treated, 107 with muscle flaps, 12 with omen- vest, a skin bridge was preserved if possible; how- tal flaps, and 11 with local wound management ever, this was dependent on where the sternotomy only. Average time to presentation was 7 to 10 days, incision ended. The anterior rectus sheath was with drainage (22 patients), dehiscence (15 pa- opened and elevated from the underlying muscle. tients), cellulitis (12 patients), and click (seven The rectus insertion to the pubis was sectioned at patients) the predominant symptoms. The most the ligament. The inferior epigastric artery was common organisms present in the 92 patients with identified and clipped. Note that none of the rec- positive cultures was Staphylococcus aureus in 55 tus flaps were delayed or required supercharging; patients (60 percent), mixed infection with S. au- however, the authors advocate harvesting the deep reus in 10 patients (11 percent), group D Entero- inferior epigastric artery as an intraoperative “life- coccus in 11 patients (12 percent), and Serratia boat” should the adequacy of rectus perfusion be marcescens in 10 patients (11 percent). in question. The lateral intercostal perforators Modified pectoralis reconstruction was used in were coagulated with bipolar electrocautery and 41 patients and rectus reconstruction was used in the rectus was raised. The superior epigastric and 56 patients (Table 1). Success was defined as a as many of the superior anterior intercostal per- healed wound and a discharged patient at 30 days forator arteries were preserved. The rectus sheath postoperatively. This was attained in 85 percent

930 Volume 120, Number 4 • Sternotomy Wounds

Fig. 1. In the modified pectoralis flap, the superior anterior rectus sheath is separated from the inferior portion of the sheath. The superior anterior rectus sheath is then left in continuity with the pectoralis muscle and fascia, giving continuous coverage to the lower third of the sternum.

Table 1. Morbidity and Mortality of 41 Modified Without isolating the sites of dehiscence, there Pectoral Flaps versus 56 Rectus Abdominis Flaps were no significant differences in success, mor- Ͼ Pectoral/Rectus Rectus bidity, or mortality between groups (p 0.05). Fascia Extension Abdominis Morbidity/Mortality (%) (%) DISCUSSION Superior dehiscence 0 (0) 8 (14.2) Inferior dehiscence 6 (14.6) 0 (0) The advantage in wound closure and the de- Hematoma/seroma 6 (14.6) 2 (3.6) crease in mortality associated with vascularized Harvest complication 0 (0) 9 (16) flap closure in sternal wound infection is well doc- Hernia 0 (0) 1 (1.8) 2–9,14,18,26,30,34 Deep venous thrombosis 1 (2.4) 0 (0) umented by large studies. The number Death (unrelated to of flap options discussed—pectoralis turnover or reconstructive surgery) 2 (4.9) 4 (7.1) pedicle,2–4,5,9,14,18,31,32,36,37 latissimus dorsi,2,5,9,31 rec- tus abdominis,2,5,7–9,37–39 or omental9,14,26,30—sug- gests that the ideal flap does not exist. A combi- for the modified pectoralis patients and 86 per- nation of flaps is sometimes required, particularly cent in the rectus population. The average time to deal with difficult areas such as the inferior for recovery was 14.4 and 15 days, respectively. third of the sternum. In this study, the authors Modified pectoralis reconstruction had 34 evaluated a modification of the pectoralis major percent morbidity, with inferior wound dehis- flap compared with the rectus abdominis flap to cence in six patients, hematoma/seroma in seven treat acute infections of the sternum, particularly patients, and deep venous thrombosis in one pa- the inferior third of the sternotomy. tient. Thirty-day mortality was two of 41. The clinical course of these patients is typical Rectus reconstruction had 34 percent morbid- of sternotomy infection and dehiscence, with a ity, with flap tip necrosis and superior dehiscence presentation delayed 10 days postoperatively.1,6,17,29 in eight patients, abdominal skin breakdown in The typical patient population presents with S. nine patients, seroma/hematoma in two patients, aureus,1,3,5–7,11,18,34 and this was reiterated in our study and hernia in one patient. Mortality was four of 56. as the most common organism (60 percent). S. marc- The rectus group showed a statistically signif- escens involved 11 percent of cases in our study, pos- icant improvement in preventing dehiscence of sibly reflecting a trend in hospital colonization. the inferior third (p ϭ 0.0045), and the pectoral The considerable success of the pectoralis ma- series displayed a statistically significant advantage jor flap has been extensively discussed.40 It is based in preventing superior dehiscence (p ϭ 0.0192). on the thoracoacromial artery, unaffected by the

931 Plastic and Reconstructive Surgery • September 15, 2007 harvesting of the internal mammary arteries for coronary graft. It is presently the favored muscle flap for covering infected sternotomy wounds.3,9 A major limitation of the pectoralis major flap has been coverage of the inferior third of the sternot- omy wound. Studies have shown that the lower portion of wounds, near the xiphisternum, is the most common site of dehiscence after flap repair.2,14,26,31,32,34–36 The pectoral and latissimus flaps alone are unsuccessful in this area. The rectus abdominis flap has been advocated as an alternative to the pectoralis major flap. It is pedicled on the superior epigastric artery; how- ever, it can survive in the absence of the internal 5,8,21,35 mammary artery. Coverage using the rectus Fig. 2. Wound dehiscence at the inferior third of the sternal re- abdominis is advocated based on its ease of dis- construction in a patient with modified pectoralis major flap section and its wide arc of rotation. It can easily reconstruction. cover the lower third of the sternum but can also reach as high as the sternal notch.7 One presumed morbidity associated with this technique is her- nia formation or protrusion of the peritoneum through the abdominal wall, described to occur in as much as 50 percent in some studies9 but only found in 2 percent of our rectus flap patients. By leaving the rectus fascia in place with a two-layer closure, we significantly diminished this compli- cation. Both of these flaps have similar success rates for sternal wound closure at 30 days of 85 and 86 percent, with average recovery being 15 days, which is an improvement from results reported with other methods. Although the rectus group had a mortality rate double that of the pectoral group, the deaths in this series were all related to Fig. 3. The upper chest at the level of the inframammary fold is the patients’ cardiac or cardiopulmonary status, shown. Note the superior dehiscence of the rectus flap seen not the procedure or surgical complications. This through the distal sternal incision. confirms and emphasizes the underlying risk fac- tors these patients have and the serious nature of a sternal infection.41 The most significant finding was the differ- the lower third of the sternum. Salvage of either ence in flap morbidities. The pectoralis-rectus fas- defect in six patients of each group was performed cial flap broke down at the inferior third (Fig. 2) using the alternative flap. in six of 41 patients. This was the area the rectus The predominant complication in the pecto- fascia modification was designed to protect. This ralis major flaps was hematoma and seroma for- area of the combination musculofascial flap con- mation, whereas in the rectus abdominis flap the tains only fascia and is by principle the weakest problem in nine of 56 patients was abdominal area of the closure. The wound dehiscence in the wound breakdown (Fig. 4). Here, the skin and fat rectus flaps was at the distal tip of the rectus, of the abdomen became necrotic because of the leading to a superior wound defect (Fig. 3). In the disruption and transposition of the major blood area of the lower third of the sternum, the mus- supply to this area. These patients were frequently cular flap of the rectus was significantly superior to obese, an independent risk factor for sternal the fascial coverage of the pectoral group, 0 per- wound dehiscence.10,17,32 Harvesting the rectus cent and 15 percent dehiscence, respectively. This muscle eliminates the zone 1 blood supply to the illustrates that the rectus flap is superior in oblit- abdominal skin, perpetuating fat necrosis, and re- erating the dead space and promoting healing in sults in considerable donor-site morbidity. To pre-

932 Volume 120, Number 4 • Sternotomy Wounds

used had the right ventricle stuck to the underside of the right sternum at the time of debridement. Risk of rupture of the right ventricle at this time is substantial if the potential for this is not appre- ciated. The dissection of the sternum off the peri- cardium must be very carefully completed, espe- cially when the planes are disturbed by infection.

CONCLUSIONS A high rate of success (85 and 86 percent) was found in this study for closure of infected sternot- omy wounds either with pectoralis major modified with rectus fascia extension or with a rectus ab- dominis flap. The complications of the pectoralis Fig. 4. The superior abdominal wall of a morbidly obese patient flap are located in the lower sternal area, with is shown. Note fat necrosis along incision emphasizing compro- wound dehiscence and hematoma/seroma the mised zone 1 vascular supply following rectus reconstruction. most common complications. The major compli- cations for the rectus abdominis flap group were donor-site necrosis, and if dehiscence did occur, it vent this complication, endoscopic harvest of the was located in the superior tip. The rectus abdo- rectus42,43 may be used to preserve collateral supply minis flap is superior in addressing the lower third and improve recovery time. Several studies have and should be used over the pectoral, with or shown that the use of vacuum-assisted closure without the anterior rectus fascia extension, if the devices23,44,45 as a bridge to flap closure of sternal infection is concentrated in this inferior region. wounds improves recovery time and success. An- other recent study demonstrated the advantages Mark Clemens, M.D. Division of Plastic and Reconstructive Surgery of transverse plate fixation for stabilization of the Georgetown University Medical Center sternal skeletal structure leading to earlier extu- 3800 Reservoir Road, NW bation, low incidences of recurrence, and more Washington, D.C. 20007 reliable healing.45,46 Further studies are warranted [email protected] to evaluate the efficacy of combining these tech- niques. ACKNOWLEDGMENT Patients now receiving coronary artery bypass The authors acknowledge Michael Javernick for as- grafting through a median sternotomy have com- sistance with the modified pectoral illustration. plications preventing percutaneous transluminal coronary angioplasty. Although the rates of sternal DISCLOSURE infection are currently 0.5 to 8.4 percent, this rate None of the authors has a financial interest in any is likely to climb because of this sicker patient of the products, devices, or drugs mentioned in this population. article. Of note is a recent article that stated that the omental flap is superior to the pectoral flap in REFERENCES preventing sepsis-related morbidity in a 33-patient 1. Smith, J. M., Glasser, R. S., Osborne, B., et al. Sternal wound 14 complications after open heart surgery: Results from 3524 con- study. The disadvantage of this procedure is that secutive operative procedures. Contemp. Surg. 43: 197, 1993. it requires a laparotomy that could spread infec- 2. Jones, G., Jurkiewicz, M. J., Bostwick, J., et al. Management tion from the thoracic cavity to the abdomen, or of the infected median sternotomy wound with muscle flaps: possibly vice versa. This approach also leads to The Emory 20 year experience. Ann. Surg. 225: 766, 1997. greater hernia formation. Because of these two 3. Pairolero, P. C., Arnold, P. G., and Harris, J. B. Long-term results of pectoralis major muscle transposition for infected possibilities, it is reserved for secondary closure sternotomy wounds. Ann. Surg. 213: 583, 1991. after pectoral or rectus flaps have failed. 4. Jurkiewicz, M. J., Bostwick, J., Hester, T. R., Bishop, J. B., and Craver, J. Infected median sternotomy wound: Successful treatment by muscle flaps. Ann. Surg. 191: 738, 1979. Operative Warning 5. Nahai, F., Rand, R., Hester, R., et al. Primary treatment of infected sternotomy wound with muscle flaps: A review of 211 A point deserving particular attention that was consecutive cases. Plast. Reconstr. Surg. 84: 434, 1989. found by reviews of operative notes was that seven 6. Martin, R. D. The management of infected sternotomy of 56 patients in whom a rectus abdominis was wounds. Ann. Plast. Surg. 22: 243, 1989.

933 Plastic and Reconstructive Surgery • September 15, 2007

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Bipedicle muscle flaps in fection after cardiac surgery. Ann. Thorac. Surg. 38: 415, 1984. sternal wound repair. Plast. Reconstr. Surg. 101: 356, 1998. 13. Breyer, R. H., Mills, S. A., Hudspeth, A. S., et al. A prospective 33. Nahai, F., Morales, L., Bone, D. K., and Bostwick, J. Pectoralis study of sternal wound complications. Ann. Thorac. Surg. 37: major muscle turnover flaps for closure of the infected ster- 412, 1984. notomy wound with preservation of form and function. Plast. 14. Lopez-Monjardin, H., De-la-Pena-Salcedo, A., Mendoza- Reconstr. Surg. 70: 471, 1982. Munoz, M., Lopez-Yanez-de-la-Pena, A., Palacio-Lopea, E., 34. Pairolero, P. C., and Arnold, P. G. Management of recalci- and Lopez-Garcia, A. Omentum flap versus pectoralis major trant median sternotomy wounds. J. Thorac. Cardiovasc. Surg. flap in the treatment of mediastinitis. Plast. Reconstr. Surg. 90: 523, 1985. 101: 1481, 1998. 35. Netscher, D. T., Eladoumikdachi, F., and Goodman, C. M. Rectus abdominis muscle flaps used successfully for median 15. Robicsek, K. F. Postoperative sterno-mediastinitis. Am. Surg. sternotomy wounds after ipsilateral internal mammary artery 66: 184, 2000. ligation. Ann. Plast. Surg. 47: 223, 2001. 16. Fairchild, P. G., and Gantz, N. M. Mediastinal and sternal 36. Mathes, S. J. The principles of muscle and musculocutaneous infections. Card. Surg. State Art Rev. 2: 407, 1988. flaps. In J. G. McCarthy (Ed.), Plastic Surgery, Vol. 1. Phila- 17. Yuen, J. C., Zhou, A. T., Serafin, D., and Georgiade, G. S. delphia: Saunders, 1990. Long-term sequelae following median sternotomy wound in- 37. Russell, R. C., Feller, A. M., Elliott, L. F., et al. The extended fection and flap reconstruction. Ann. Plast. Surg. 35: 585, 1995. pectoralis major myocutaneous flap: Uses and indications. 18. Scullly, H. E., Leclerc, Y., Martin, R. D., et al. Comparison Plast. Reconstr. Surg. 88: 814, 1991. between antibiotic irrigation and mobilization of pectoral 38. Solomon, M. P., and Granick, M. S. New reconstruction method muscle flaps in treatment of deep sternal infections. J. Thorac. for sternotomy wounds. Perspect. Plast. Surg. 8: 61, 1994. Cardiovasc. Surg. 90: 523, 1985. 39. Clarkson, J. H., Probst, F., Niranjan, N. S., et al. Our expe- 19. Grossi, E. A., Culliford, A. T., Krieger, K. H., et al. A survey rience using the vertical rectus abdominis muscle flap for of 77 major infectious complications of median sternotomy: reconstruction in 12 patients with dehiscence of a median A review of 7,949 consecutive operative procedures. Ann. sternotomy wound and mediastinitis. Scand. J. Plast. Reconstr. Thorac. Surg. 40: 214, 1985. Surg. Hand Surg. 37: 266, 2003. 20. Weinstein, R. A., Jones, E. L., Schwarzmann, A. W. Sternal 40. AschermanJ., PatelS., Malhotra, S., and Smith, C. Manage- osteomyelitis and mediastinitis after open heart operation: ment of sternal wounds with bilateral pectoralis major myo- Pathogenesis and prevention. Ann. Thorac. Surg. 21: 442, cutaneous advancement flaps in 114 consecutively treated 1976. patients: Refinements in technique and outcomes analysis. 21. Arnold, P. G., and Pairolero, P. C. Chest-wall reconstruction: Plast. Reconstr. Surg. 114: 676, 2004. An account of 500 consecutive patients. Plast. Reconstr. Surg. 41. Ahumada, L. A., de la Torre, J. I., RayP. D., et al. Comorbidity 98: 804, 1996. trends in patients requiring sternectomy and reconstruction. 22. Loop, F. D., Lytre, B. W., Cosgrove, D. M., et al. Sternal Ann. Plast. Surg. 54: 264, 2005. wound complications after isolated coronary artery bypass 42. Dabb, R., Wrye, S., and Hall, W. Endoscopic harvest of the grafting: Early and late morbidity, mortality, and cost of care. rectus abdominis muscle. Ann. Plast. Surg. 44: 491, 2000. Ann. Thorac. Surg. 49: 179, 1990. 43. Sawaizumi, M., Onishi, K., and Maruyama, Y. Endoscopic-as- 23. Hersh, R. E., Jack, J. M., Dahman, M. I., Morgan, R. F., and sisted rectus abdominis muscle flap harvest for chest wall re- Drake, D. B. The vacuum-assisted closure device as a bridge construction: Early experience. Ann. Plast. Surg. 37: 317, 1996. to sternal closure. Ann. Plast. Surg. 46: 250, 2001. 44. Song, D. H., Wu, L. C., Lohman, R. F., Gottlieb, L. J., and 24. Shumacker, H. B., and Mandelbaum, I. Continuous antibi- Franczyk, M. Vacuum assisted closure for the treatment of otic irrigation in the treatment of infection. Arch. Surg 86: sternal wounds: The bridge between debridement and de- 384, 1963. finitive closure. Plast. Reconstr. Surg. 111: 92, 2003. 25. Bryant, L. R., Spencer, F. C., and Trinkle, J. K. Treatment of 45. Agarwal, J. P., Ogilvie, M., Wu, L. C., et al. Vacuum-assisted median sternotomy infection by mediastinal irrigation with closure for sternal wounds: A first-line therapeutic manage- an antibiotic solution. Ann. Surg. 169: 914, 1969. ment approach. Plast. Reconstr. Surg. 116: 1035, 2005. 26. Lee, A. B., Schimert, G., Shaktin, S., and Seigel, J. H. Total 46. Cicilioni, O. J., Stieg, F. H., and Papanicolaou, G. Sternal excision of the sternum and thoracic pedicle transposition of wound reconstruction with transverse plate fixation. Plast. the greater omentum: Useful stratagems in managing severe Reconstr. Surg. 115: 1297, 2005.

934 RECONSTRUCTIVE

Progressive Tension Sutures in the Prevention of Postabdominoplasty Seroma: A Prospective, Randomized, Double-Blind Clinical Trial

Patricio Andrades, M.D. Background: The purpose of this study was to evaluate the seroma reduction Arturo Prado, M.D. capabilities of progressive tension sutures and compare them with the conven- Stefan Danilla, M.D. tional use of drains. Claudio Guerra, M.D. Methods: Sixty female patients were randomized into four groups: group 1 (con- Susana Benitez, M.D. trol, no drains, and no progressive tension sutures), group 2 (progressive tension Sergio Sepulveda, M.D. sutures alone), group 3 (drains alone), and group 4 (progressive tension sutures Carlos Sciarraffia, M.D. and drains). All patients underwent a classic abdominoplasty and drains were left Vicente De Carolis, M.D. for 7 days in the corresponding groups. Clinical and ultrasound assessments were Santiago, Chile performed 2 weeks after the operation by blinded evaluators. Punctures, volumes, nonseroma complications, and aesthetic outcome were also measured. Results: Surgical time was 50 minutes longer in groups 2 and 4. Drain outputs were higher in group 3 than in group 4. The clinical and ultrasound seroma frequency was 35 percent and 90 percent respectively, without significant differences among the groups. The control group was interrupted at 10 patients because of consid- erably larger seromas and an increased amount of punctures needed for treatment. No differences were found in the other groups. There were no differences with respect to complication rates and aesthetic outcome after follow-up. Conclusions: Progressive tension sutures increase surgical time, reduce drain out- puts, and have the same clinical and ultrasound seroma frequency as the use of drains alone. The combination of both methods simultaneously does not add any advantages. However, complications and interventions increase if at least one of them is not used. The mechanism of action of progressive tension sutures could be the compartmentalization of the fluid collection under the flap facilitating absorption. (Plast. Reconstr. Surg. 120: 935, 2007.)

bdominoplasty is a surgical procedure de- surgical technique, and combination with lipo- signed to correct anterior abdominal wall suction or other procedures.16 Adeformity by acting on its three main ele- One of the most frequent postabdominoplasty ments: skin, fat, and the musculoaponeurotic complications is seroma formation. This is con- layer.1 Despite being considered a safe proce- sidered an early, local, and relatively minor com- dure, abdominoplasty (like other operations) is plication. The incidence of seroma after abdomi- not free of complications. The reported overall noplasty varies enormously as reported in the complication rate ranges from 4 to 80 literature,2–15 with an accepted standard of 10 percent,2–15 depending on multiple factors. percent.17 Its cause has been described implicat- Among the most important factors are patient ing many probable mechanisms, such as vascular body mass index, extension of flap undermining, and lymphatic channel disruption, dead space formation, and the presence of shearing forces From the Plastic Surgery Division, Department of Surgery, between the flap and fascia with release of in- Jose Joaquin Aguirre Clinical Hospital, University of Chile 18 School of Medicine. flammatory mediators. Seroma formation is Received for publication December 12, 2005; accepted March usually a self-limited phenomenon that can oc- 21, 2006. casionally cause significant problems. The exis- Presented at the Chilean Society of Plastic Surgery meeting, tence of a liquid collection between the abdom- in Santiago, Chile, August 25, 2005. inal wall and flap increases pressure that, Copyright ©2007 by the American Society of Plastic Surgeons transmitted to the flap, can cause wound dehis- DOI: 10.1097/01.prs.0000253445.76991.de cence and flap necrosis. It can also be contami-

www.PRSJournal.com 935 Plastic and Reconstructive Surgery • September 15, 2007 nated and predispose to infection. Rare second- sion sutures and compare them with the absence ary effects such as chronic liquid accumulation of preventive measures and the use of drains. Four with pseudocyst formation19,20 and systemic in- study groups were planned: group 1 (control, no flammatory response syndrome21 have also been drains and no progressive tension sutures), group reported. Although benign in nature, seromas 2 (progressive tension sutures alone), group 3 always cause discomfort and anxiety in the pa- (drains alone), and group 4 (progressive tension tient, generating frequent office visits, proce- sutures and drains). The allocation for treatment dures for treatment, and increased costs. was performed by computer-generated random Prevention, defined as any possible measure numbers. that avoids or reduces the chances of seroma formation, seems to be the best treatment. An Patients and Settings effective seroma prevention method should be Nonoverweight female patients with an ante- able to seal lymphatic and vascular tissue chan- rior abdominal wall deformity type IV as described nels, obliterating dead space, providing strength by Matarasso,41,42 without comorbidity, were in- to the overlying skin flap, decreasing shearing cluded in the study. All patients underwent sur- forces, and promoting wound healing with an gery at the University of Chile Clinical Hospital 18 uneventful recovery. Multiple preventive mea- between January of 2003 and January of 2005. sures have been proposed, such as avoidance of electrocautery,22,23 long-term distant exit Surgical Technique drains,24 pressure dressings,25 sclerotherapy,26,27 endoscopic techniques,28–30 fibrin glue,31–34 and Preoperative markings were performed in the 35–39 standing position (Fig. 1). All patients underwent internal fixation techniques. None of them 2 has proved to be completely effective and free of a classic abdominoplasty procedure under gen- complications; therefore, seromas still arise. eral anesthesia and a one-dose preoperative anti- Internal fixation techniques consist of placing biotic prophylaxis. Flap elevation was performed sutures at periodic intervals between the flap and with electrocautery, and midline fascia plication the fascia. Mladick was the first author to briefly was performed in one layer with a running non- refer to them in the literature.35,36 Baroudi and absorbable suture. The allocation group was com- Ferreira37 described them more extensively as municated to the surgeon just before starting clo- “quilting sutures” in combination with suction sure. If progressive tension sutures were used, 30 drains to reduce dead space and shearing forces. to 40 separate fixation and advancement sutures Pollock and Pollock38 renamed this technique were placed between the flap and the fascia using an absorbable material as described by Pollock “progressive tension sutures” because it also al- 38 lows tension-free advancement of the abdominal and Pollock (Fig. 1). If drains were used, two flap in a proximal to distal direction. They used closed suction drains were placed with exit at the this method without drains and in various ab- pubis 3 cm below the incision. A 150-cc flank li- dominal wall procedures with adequate results in posuction with a previous 80-cc infiltration was a retrospective study.39 The only prospective, carried out to improve contouring results in all randomized trial reported considering this type patients. No liposuction of the dorsum or any of sutures is a study by McCarthy et al., where the additional surgical procedures were performed. reduction of seroma in transverse rectus abdo- All patients were discharged from the hospital 24 minis musculocutaneous flap reconstruction was hours after surgery. Elastic garments were indi- assessed after using progressive tension sutures.40 cated at the moment of discharge for at least 3 to However, no evidence supports its use in aes- 4 weeks. Other indications included nonbed rest, thetic abdominoplasty. The purpose of this study light meals, and progressive resumption of normal was to adequately assess the role of progressive activities. If drains were used, they were left in place tension sutures in reducing postabdominoplasty and the patient was trained in daily home measure- seroma. ments until the next office control (Fig. 2).

PATIENTS AND METHODS Outcomes and Follow-Up Operative time was measured from the mo- Design ment of the first incision until wound closure was A prospective, randomized, double-blind, con- finished. Patients were controlled on a weekly ba- trolled factorial study was designed to evaluate the sis. Drains were removed and daily debits were seroma-reducing capabilities of progressive ten- recorded for groups 3 and 4 and at the first control

936 Volume 120, Number 4 • Postabdominoplasty Seroma

Fig. 1. (Above, left) Preoperative markings: a 10-cm transverse line is highlighted at the pubis level and another at the umbilical level;themidpointbetweenbothisdetermined,whereanothertransverselineismarkedjoiningtheanteriorsuperioriliaccrest; the points are connected and a transverse infraumbilical lozenge is obtained. (Above and below, right) Thirty to 40 separate nonabsorbablefixationandadvancementsuturesareplacedbetweentheflapandthefasciaaftermidlineplication.(Below,left) Sonogram obtained at postoperative day 10 showing liquid accumulation under the flap and a progressive tension suture compartmentalizing effect (arrow).

(postoperative day 7). An ultrasound examination initiated by puncture with a 21-gauge needle and of the anterior abdominal wall was programmed the aspirated volume and quality was also assessed. between the postoperative days 10 and 12. On the The patient was controlled in 1 week, punctures second control (postoperative day 14), assessment were repeated weekly until no liquid was aspirated, of seroma formation was performed by clinical and a second ultrasound examination was pro- and ultrasound examination. Clinical evaluation grammed when the patient had a third positive consisted of the appraisal of seroma symptoms puncture. The patient, radiologist, and surgeon (bulginess, distention, liquid accumulation sensa- who performed office controls were unaware of tion) and signs (palpation and percussion of the the group allocation but were obviously aware of wave sign). Ultrasound was performed by a radi- the presence of drains. ologist to measure volume, number of compart- Follow-up included all patients for 6 months. ments, and localization of any liquid accumulation All nonseroma complications were also recorded encountered (Fig. 1). If clinical and ultrasound prospectively. Six months after surgery, aesthetic evaluation were negative for seroma, the patient evaluation was performed by each of the patients was seen again in 2 weeks. If clinical and/or ul- and by three masked plastic surgeons. Patients trasound evaluation were positive for seroma, the applied a subjective scale ranging from 1 to 10 volume, compartments, and localization of the (1 ϭ poor, 10 ϭ the best) on themselves and the liquid were recorded. In these cases, treatment was three masked plastic surgeons applied an objec-

937 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 2. Follow-up decision algorithm (see text for detailed explanation). tive grading system for the evaluation of cosmetic series, and receiver operating characteristic curve surgical results as described by Strasser.43,44 This analysis and logistic regression were used for di- scale considers five items: malposition, distortion, agnostic tests. asymmetry, contour deformity, and scar aspect. Each item is graded as excellent (0), good (1), mediocre (5), or poor (15) for a total that may Ethical Considerations range from 0 to 75. This final score is considered This study was approved by the Department of excellent if it is equal to 0, good between 1 and 4, Surgery Ethical Committee of the University of mediocre between 5 and 14, and poor for more Chile Clinical Hospital. All patients accepted to than 15. enroll in this study signed informed consents. An internal analysis was programmed after complet- ing 10 patients for each group to evaluate early Statistical Analysis differences and ethical problems. A sample size of 60 patients was estimated by means of nQuery 4.0 software (Statistical Solu- tions, Saugus, Mass.). Assuming that the common RESULTS SD is 45.000, for a sample size in each of the four The four groups were comparable with respect groups of 15, a one-way analysis of variance will to sex, age, body mass index, comorbidity, and have a 90 percent power to detect a 0.050 level smoking habits, proving the concealment of ran- mean difference at the characterized variance of domization (Table 1). The adjustment for multi- a mean of 550.000, Normally distributed contin- ple comparisons shows that operative time was uous variables are described as mean and SD; non- longer in groups 2 and 4, where progressive ten- parametric continuous and ordinal variables are sion sutures were used, by an average of 50 min- described as median, interquartile range, and utes (4.2 Ϯ 0.1 minutes versus 3.3 Ϯ 0.2 minutes; range. Nominal categorical variables are de- p Ͻ 0.001). Excluding the groups where no drains scribed as percentages. For statistical significance, were used, there were significantly lower drain an alpha error of less than or equal to 0.05 was debits in group 4 (with progressive tension su- considered. All confidence intervals are described tures) compared with group 3 (without progres- at 95 percent. The Fisher’s exact test was used for sive tension sutures) during the first postoperative categorical variables. For simple comparisons of week (coefficient, Ϫ38.1; p Ͻ 0.0001; 95 percent continuous variables, the t test or the Wilcoxon confidence interval, Ϫ52.3 to Ϫ23.8) (Fig. 3). Se- test was used, and for multiple comparisons, anal- roma was detected clinically in 35 percent of the ysis of variance or the Kruskal-Wallis test was used, patients and by ultrasound in 90 percent, without depending on the distribution of the results. Gen- statistical differences between the groups (Table eral estimated equations were used for temporal 2). Ultrasound seroma volume was higher in the

938 Volume 120, Number 4 • Postabdominoplasty Seroma

Table 1. General Results Group 4, Group 1, Group 2, Group 3, PTS and Drain Total p (55 ؍ n) (15 ؍ n) (15 ؍ Drain (n (15 ؍ PTS (n (10 ؍ Control (n Female, % 100 100 100 100 100 NS Age, years 40.7 Ϯ 5.8 38.5 Ϯ 4.6 40.1 Ϯ 9.5 39.7 Ϯ 6.1 39.8 Ϯ 6.5 NS BMI 26.7 Ϯ 2.5 27.0 Ϯ 2.1 25.3 Ϯ 3.5 26.4 Ϯ 2.5 26.4 Ϯ 2.7 NS Other disease, % 0 0 0 0 0 NS Smoking, % 20.0 26.7 26.7 33.3 26.7 NS Surgical time, hours 3.3 Ϯ 0.3 4.2 Ϯ 0.4* 3.2 Ϯ 0.6 4.1 Ϯ 0.5* 3.7 Ϯ 0.5 Ͻ0.001 PTS, progressive tension sutures; BMI, body mass index; NS, not significant. *Significantly higher than control and drainage groups, but without differences among them.

Fig. 3. Graphic showing drain output during the first 7 postoperative days in the groups where drains were used (groups 3 and 4). Drain outputs (D) were signifi- cantly lower in group 4, where progressive tension sutures (PTS) were used.

Table 2. Clinical and Ultrasound Evaluation Outcomes Group 4, Group 1, Group 2, Group 3, PTS and Drain Total p (55 ؍ n) (15 ؍ n) (15 ؍ Drain (n (15 ؍ PTS (n (10 ؍ Control (n Clinical seroma, % 50 33 33 27 35 NS US seroma, % 100 87 87 93 90 NS US seroma volume, m) 155* 64 45 55 80 Ͻ0.001 Range 90–220 0–90 0–200 0–110 0–220 IQR 130–200 36–79 10–80 40–70 55–165 No. of compartments on US 1 3† 1 3† 2 0.001 Range 1–2 0–4 0–3 0–5 0–5 IQR 1–1 2–3 1–1 2–4 1–4 Second US evaluation Ͻ0.001 No. 10* 4 3 3 20 Percent 100 26.6 20 20 36.4 Volume on second US 109* Laminar Laminar Laminar — Ͻ0.001 No. of compartments on second US 1 1 1 2 — NS PTS, progressive tension sutures; US, ultrasound; IQR, interquartile range; NS, not significant. *Statistical differences for group 1 only, with no differences for the other studied groups. †Significantly higher than control and drainage groups, but without differences among them.

939 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 4. Box plot graph of postabdominoplasty serum collection under the flap measured with ultrasound shown by group distribution. PTS, progressive tension sutures; D, drains. control group than in the other groups, where the the other groups (p Ͻ 0.001) (Table 3). There average volume was less than 65 ml (Fig. 4). were no puncture differences among groups 2, Groups with progressive tension sutures (groups 2 3, and 4. None of the patients in these groups and 4) had a higher number of liquid compart- needed more than four punctures for seroma ments found by ultrasound examination (p Ͻ treatment. When a fourth puncture was needed, 0.001). Adding potential confounders to the they were all negative for liquid aspiration. For model (e.g., age, body mass index, complications, all these reasons, the control branch was stopped tobacco use) did not change the results. after the intermediate evaluation, and only 10 pa- All patients in group 1 needed a second ul- tients were completed. trasound evaluation after 3 weeks, and higher vol- Nonseroma complications are listed in Table 4. umes were still found (p Ͻ 0.001). Group 1 also No patient was lost to follow-up and no major com- needed more punctures for drainage, had a plications were observed. The general complication higher number of positive punctures, and had rate was 34.5 percent, with no differences between larger amounts of fluid drained by puncture than the four studied groups, although a tendency for a

Table 3. Results of Seroma Punctures Group 4, Group 1, Group 2, Group 3, PTS and Drain Total p (55 ؍ n) (15 ؍ n) (15 ؍ Drain (n (15 ؍ PTS (n (10 ؍ Control (n Punctures needed until negative 9* 1 2 1 2 Ͻ0.001 Range 7–13 0–4 0–4 0–4 0–13 IQR 8–10 0–4 1–3 0–2 1–4 Positive puncture (%) First puncture 100 54 62 50 — NS Second puncture 90* 31 23 21 — Ͻ0.05 Third puncture 90* 31 23 7 — Ͻ0.05 Fourth puncture 90* 0 0 0 — Ͻ0.05 Puncture volume (ml) First puncture 170* 50 35 30 — Ͻ0.05 Second puncture 150* 30 10 10 — Ͻ0.05 Third puncture 140* 20 30 5 — Ͻ0.05 Fourth puncture 100* 0 0 0 — Ͻ0.05 PTS, progressive tension sutures; IQR, interquartile range; NS, not significant. *Statistical differences only for group 1. There were no differences between the other groups.

940 Volume 120, Number 4 • Postabdominoplasty Seroma

Table 4. Nonseroma Complications Group 4, Group 1, Group 2, Group 3, PTS and Drain Total p (55 ؍ n) (15 ؍ n) (15 ؍ Drain (n (15 ؍ PTS (n (10 ؍ Control (n Hemorrhage 0 0 0 0 0 NS Infection* 1 1 1 2 5 (9.1%) NS Dehiscence 1 1 2 0 4 (7.3%) NS Umbilical† 2 1 2 2 7 (12.7%) NS Flap necrosis 0 0 0 0 0 NS DVT/PE 0 0 0 0 0 NS Scarring 1 0 0 0 1 (1.8%) NS Asymmetry‡ 0 0 1 1 2 (3.6%) NS Overall complication rate 5 (50%) 3 (20%) 6 (40%) 5 (33%) 19 (34.5%) NS PTS, progressive tension sutures; NS, not significant; DVT, deep venous thrombosis; PE, pulmonary embolism. *No deep or necrotizing infections, only superficial. †Infection, dehiscence, and necrosis. ‡Dog-ears or bulging flaps.

Table 5. Aesthetic Evaluation Group 4, Group 1, Group 2, Group 3, PTS and Drain Total p (55 ؍ n) (15 ؍ n) (15 ؍ Drain (n (15 ؍ PTS (n (10 ؍ Control (n Subjective evaluation* 8 8 9 9 9 NS Range 3–9 6–10 4–10 3–10 7–9 IQR 7–9 7–9 8–9 7–9 3–10 Strasser Scale* 6.5 5 4 3 4 Range 2–19 1–10 0–14 1–18 0–19 IQR 4–10 3–5 2–7 2–7 3–7 NS PTS, progressive tension sutures; IQR, interquartile range; NS, not significant. *See text for detailed information. higher complication rate could be seen for group 1. 1.64; p ϭ 0.0064) and that age and smoking were Subjective and objective aesthetic evaluation at not. Body mass index was also a significant prog- 6-month follow-up showed no dissimilarity between nostic factor for objective (Spearman’s ␳, the groups (Table 5). Illustrative cases of patients Ϫ3580; p ϭ 0.0073) and subjective (Spearman’s with and without progressive tension sutures can be ␳, –0.4147; p ϭ 0.0016) aesthetic outcome. This seen in Figures 5 and 6, respectively. was not affected by other variables such as age, Positive clinical evaluation for seroma de- tobacco use, or treatment allocation. termined higher volumes of liquid under the flap, with a significant statistical difference when DISCUSSION compared with negative clinical evaluation (106 The overall complication and seroma rates af- ml versus 47 ml) (p ϭ 0.0038) (Fig. 7). Positive ter abdominoplasty have large variations reported clinical evaluation also established an increased in literature, with an incidence of postabdomino- number of punctures needed for treatment plasty seroma ranging between 1 and 57 percent (four versus two) (p Ͻ 0.05) and higher overall (Table 6). This great inconsistency could be ex- complication probability (0.43 versus 0.28) (p Ͻ plained by the fact that most of these studies are 0.05). Ultrasound volume had a direct relation- retrospective and therefore include different pop- ship with complication probability, and a cut-point ulations with different techniques, clinical assess- of 80 ml was recognized as the volume that more ment alone, and no clear definition of seroma. accurately predicts postoperative problems (odds The clinical seroma frequency found in this study, ratio, 6; 95 percent confidence interval, 1.77 to although somewhat high as compared with values 20.30; p ϭ 0.004) (Fig. 8). Clinical evaluation had reported in the literature, may be explained by a a 65 percent sensitivity and a 78 percent specificity selection bias. Because the masked clinical evalu- to detect more than 80 ml of liquid accumulation. ators were supposed to examine the abdomen in Multivariate analysis showed that body mass index search of liquid, they were prone to find seroma was a predictive factor for complications (odds rather than not. This bias, however, does not ex- ratio, 1.32; 95 percent confidence interval, 1.07 to plain the surprising ultrasound seroma frequency

941 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 5. Preoperative and 6-month follow-up photographs of a 45-year-old patient from group 3 (with drains alone).

Fig. 6. Preoperative and 6-month follow-up photographs of a 42-year-old patient from group 2 (with progressive tension sutures alone).

942 Volume 120, Number 4 • Postabdominoplasty Seroma

Fig. 7. Box plot graph showing increased ultrasound volume when there was a positive clinical evaluation for seroma.

Fig.8. Graphshowingthedirectrelationshipbetweenultrasoundvolumeandthe probability of having a complication. A volume of 80 ml was recognized as the amount of liquid that more accurately predicts postoperative problems.

of 90 percent that was detected. Ultrasound of the consideration, an inevitable question arises: When abdominal wall following abdominoplasty has al- does a fluid collection become a dangerous threat ready been proved to be useful method that pro- for postoperative recovery? vides a noninvasive, accurate, and low-cost diag- A problematic fluid collection could be de- nosis of fluid collections in the abdominal fined as any liquid gathering under the flap that wall.45–47 In this study, if ultrasound examination determines elevated numbers of interventions and could have been performed daily and by different complications. From the data obtained in this radiologists, almost all of the patients would have work, over 80 ml could be considered the volume been diagnosed as having a variable amount of of a problematic collection. Clinical evaluation liquid under the flap.17 It seems that seroma is not had an adequate accuracy to detect problematic a complication but a normal part of postabdomi- liquid accumulation under the flap and was asso- noplasty evolution. Taking these elements into ciated with increased punctures and higher com-

943 Plastic and Reconstructive Surgery • September 15, 2007

Table 6. Overall Complication and Seroma Rates after Abdominoplasty in the Literature Year of Sample Overall Seroma Authors Publication Size Complication Rate (%) Incidence (%) Pitanguy2 1975 539 14* 6 Grazer and Goldwyn3 1977 10.490 15* 4* Avelar4 1983 130 22* 10 Hester et al.5 1989 563 19* 2.5 Teimourian and Rodgers6 1989 26.562 4* 1.2* Dillerud7 1990 487 9* 1 Floros and Davis8 1991 133 15–68* 24* Matarasso9 1995 150 30* 10 Vastine et al.10 1999 90 30–80* 12–20* Chaouat et al.11 2000 258 22 11 Van Uchelen et al.12 2001 86 14 6–57* Hensel et al.13 2001 199 32 28 Kryger et al.14 2004 153 11 7 Stevens et al.15 2005 406 15 7 *Values approximately deducted from the data in the study. plication rates. Then, clinical evaluation becomes mastectomy,51 to the latissimus dorsi donor site,52 the main tool to determine when a collection and in abdominoplasty.53 However, they are expen- turns into an awkward setback. For example, if sive, cumbersome to apply, and have a risk of infec- clinical assessment does not detect any fluid, the tious disease transmission. Therefore, further stud- chances of having postoperative problems are low, ies are required for safety evaluation. Finally, but it does not mean that there is no fluid under internal fixation techniques, such as quilting or pro- the flap. On the contrary, if the presence of liquid gressive tension sutures, have appeared as new meth- is suspected clinically, there are more chances for ods of diminishing complications in abdominoplasty interventions and complications. Although se- by reducing dead space and tension on the flap. roma treatment was not within the scope of this Nevertheless, they are not easy to place, dimpling of study, a closer assessment of these patients is rec- the flap may appear, and surgical time may be ommended. Seroma formation is a process regu- extended. lated by the balance of secretion and reabsorption In our study, progressive tension sutures sig- of fluid.48 In patients where this balance breaks, nificantly lengthened operative time by an av- such as in the presence of large-volume quantities erage of 50 minutes. As McCarthy et al. found in or volumes that do not decrease after follow-up, their study with progressive tension sutures in multiple liquid aspirations may be needed at fre- transverse rectus abdominis musculocutaneous quent intervals. flap reconstruction, we found that these sutures Prevention seems to be the best treatment for decrease daily drain output; however, they do seroma formation. Preventive measures may be not decrease clinical and ultrasound seroma for- classified into five groups: general, drainage, ex- mation, seroma volume, and the need for punc- ternal compression, tissue adhesives, and internal ture when compared with groups including fixation techniques. General measures include ad- drains or both drains and progressive tension equate patient selection (body mass index Ͻ30, sutures simultaneously. In addition, progressive with controlled or no comorbidity), avoidance of tension sutures do not decrease the complica- electrocautery, limited undermining, restricted tion rate or improve aesthetic outcome. Our extension of liposuction, and leaving a thin layer of hypothesis is that progressive tension sutures fat tissue over the fascia to promote absorption.49,50 redistribute liquid by dividing the fluid under Drainage is one of the most accepted and universal the flap into compartments, transforming an methods of prevention, but drains are also a source eventual lagoon of liquid into a series of small of retrograde bacterial migration, local inflamma- pockets of fluid. This could be an explanation as tion, and patient discomfort. External compression to why ultrasound detected higher number of techniques, including compression dressings, gar- compartments in the groups with progressive ments, and casts, must be used for a long period and tension sutures. This compartmentalization pro- are uncomfortable for the patient. Tissue adhesives, cess also determines that some pockets will such as commercial or autologous fibrin sealants, never contact the drain placement site, thus ex- have a variable success in the reducing seroma rate plaining the lower drain output. The same in- in vitro.18 In vivo, they have been applied after cidence of seroma with the use of progressive

944 Volume 120, Number 4 • Postabdominoplasty Seroma tension sutures or drains alone could also fall 7. Dillerud, E. Abdominoplasty combined with suction lipec- under the same theory, because small pockets of tomy: A study of complications, revisions and risk factors in 487 cases. Ann. Plast. Surg. 25: 333, 1990. liquid are more easily absorbed than larger la- 8. Floros, C., and Davis, P. K. Complications and long-term goons. Unfortunately, for the same reasons, it results following abdominoplasty: A retrospective study. Br. seems that both techniques are not synergistic, J. Plast. Surg. 44: 190, 1991. and therefore the association of progressive ten- 9. Matarasso, A. Liposuction as an adjunct to a full abdomino- sion sutures with drains does not reduce seroma plasty. Plast. Reconstr. Surg. 95:829, 1995. 10. Vastine, V. L., Morgan, R. F., Williams, G. S., et al. Wound development or improve results. complications of abdominoplasty in obese patients. Ann. Plast. Surg. 42: 34, 1999. CONCLUSIONS 11. Chaouat, M., Levan, P., Lalanne, B., et al. Abdominal der- Seroma preventive measures must always be molipectomies: Early postoperative complications and long- used to lower the incidence of fluid collections term unfavorable results. Plast. Reconstr. Surg. 106: 1614, 2000. after abdominoplasty. If such measures are not 12. Van Uchelen, J. H., Werker, P. M., and Kon, M. Complica- implemented, large amounts of seroma fluid will tions of abdominoplasty in 86 patients. Plast. Reconstr. Surg. accumulate, generating more interventions, com- 107: 1869, 2001. plications, and disastrous results. Drains, progres- 13. Hensel, J. M., Lehman, J. A., Tantri, P., et al. An outcomes sive tension sutures, or both have the same clinical analysis and satisfaction survey of 199 consecutive abdomi- noplasties. Ann. Plast. Surg. 46: 357, 2001. and seroma incidence, overall complication rate, 14. Kryger, S. B., Fine, N. A., and Mustoe, T. A. The outcome of and aesthetic outcome. The decision of what to abdominoplasty performed under conscious sedation: Six- use must be based on patient and surgeon pref- year experience in 153 consecutive cases. Plast. Reconstr. Surg. erences together with an analysis of the advantages 113: 1807, 2004. and disadvantages of each method for each par- 15. Stevens, W. G., Cohen, R., Vath, S., et al. Does lipoplasty really add morbidity to abdominoplasty? Revisiting the controversy ticular case. For the time being, we will continue with a series of 406 cases. Aesthetic Surg. J. 25: 353, 2005. our search for a better method of postabdomino- 16. Matarasso, A. Abdominal dermolipectomies: Early postop- plasty seroma prevention. erative complications and long-term unfavorable results (Dis- cussion). Plast. Reconstr. Surg. 106: 1619, 2000. Patricio Andrades, M.D. 17. Zimman, O. A., Butto, C. D., and Ahualli, P. E. Frequency of University of Chile seroma in abdominal lipectomies. Plast. Reconstr. Surg. 108: Del Mirador 2255 depto. 1001 1449, 2001. Las Condes, Santiago, Chile 18. Kulber, D. A., Bacilious, N., Peters, E. D., et al. Use of fibrin [email protected] sealant in the prevention of seromas. Plast. Reconstr. Surg. 99: 842, 1997. ACKNOWLEDGMENTS 19. Zecha, P. J., and Missotten, F. E. Pseudocyst formation after This study was supported by the University of Chile abdominoplasty: Extravasations of Morel-Lavalle´e.Br. J. Plast. Surg. 52: 500, 1999. Clinical Hospital. 20. Keramidas, E. G., Rodopoulou, S., and Khan, U. Pseudo-cyst formation after abdominoplasty combined with liposuction: DISCLOSURE A case report and review of the literature. Eur. J. Plast. Surg. None of the authors has a financial interest or com- 28: 400, 2005. mercial association that poses or creates a conflict of 21. Kargi, E., Akduman, D., Dokuzoguz, B., et al. Late compli- cation of abdominoplasty in an obese patient: Systemic in- interest in this study. flammatory response syndrome and seroma. Plast. Reconstr. Surg. 111: 1568, 2003. REFERENCES 22. Porter, K., O’Connor, S., and Lopez, M. Electrocautery as a 1. Prado, A., Andrades, P., and Benitez, S. Abdominoplasty: The factor in seroma formation following mastectomy. Am. use of polypropylene mesh to correct the myoaponeurotic- J. Surg. 176: 8, 1998. layer deformity. Aesthetic Plast. Surg. 28: 144, 2004. 23. Kuzon, W., Crawford, R., Binhammer, P., et al. Effect of 2. Pitanguy, I. Abdominal lipectomy. Clin. Plast. Surg. 2: 401, electrosurgical technique on wound healing and early com- 1975. plication rate following abdominal dermolipectomy. Ann. 3. Grazer, F. M., and Goldwyn, R. M. Abdominoplasty assessed Plast. Surg. 37: 245, 1996. by survey, with emphasis on complications. Plast. Reconstr. 24. Zide, B. To reduce your seroma rate. Plast. Reconstr. Surg. 103: Surg. 59: 513, 1977. 1098, 1999. 4. Avelar, J. M. Abdominoplasty: Technical refinement and 25. Pitanguy, I. Evaluation of body contouring surgery today: A analysis of 130 cases in 8 years follow-up. Aesthetic Plast. Surg. 30-year perspective. Plast. Reconstr. Surg. 105: 1499, 2000. 7: 205, 1983. 26. Nichter, L. S., Morgan, R. F., Dufresne, C. R., et al. Rapid 5. Hester, T. R., Baird, W., Bostwick, J., et al. Abdominoplasty management of persistent seromas by sclerotherapy. Ann. combined with other major surgical procedures: Safe or Plast. Surg. 11: 233, 1983. sorry? Plast. Reconstr. Surg. 83: 997, 1989. 27. Laverson, S. Polidocanol for refractory seroma. Plast. Recon- 6. Teimourian, B., and Rodgers, W. B. A national survey of str. Surg. 104: 1212, 1999. complications associated with suction lipectomy: A compar- 28. Aly, A., Avila, E., and Cram, A. Endoscopic plastic surgery. ative study. Plast. Reconstr. Surg. 84: 628, 1989. Surg. Clin. North Am. 80: 1373, 2000.

945 Plastic and Reconstructive Surgery • September 15, 2007

29. Zukowski, M. L., Ash, K., Spencer, D., Malanoski, M., and 42. Matarasso, A. Abdominolipoplasty: A system of classification Moore, G. Endoscopic intracorporal abdominoplasty: A re- and treatment for combined abdominoplasty and suction- view of 85 cases. Plast. Reconstr. Surg. 102: 516, 1998. assisted lipectomy. Aesthetic Plast. Surg. 15: 111, 1991. 30. Ferraro, F. J., Zavitsanos, G. P., Van BuskirkE. R., et al. Im- 43. Strasser, E. J. An objective grading system for the evaluation of proving the efficiency, ease, and efficacy of endoscopic ab- cosmetic surgical results. Plast. Reconstr. Surg. 104: 2282, 1999. dominoplasty. Plast. Reconstr. Surg. 99: 895, 1997. 44. Strasser, E. J. Application of an objective grading system for 31. Saltz, R., Sierra, D., Feldman, D., et al. Experimental and clinical evaluation of cosmetic surgical results. Plast. Reconstr. Surg. applications of fibrin glue. Plast. Reconstr. Surg. 88: 1005, 1991. 109: 1733, 2002. 32. Anton, S. H., Milimir, N. M., and Hans, A. Fibrin glue to prevent 45. Stocchero, I. N. Ultrasound and seromas (Letter). Plast. Re- seroma formation. Plast. Reconstr. Surg. 101: 1744, 1998. constr. Surg. 91: 198, 1993. 33. Johnson, L., Cusick, T. E., Helmer, S., et al. Influence of 46. Mohammad, J. A., Warnke, P. H., and Stavraky, W. Ultra- fibrin glue on seroma formation after breast surgery. sound in the diagnosis and management of fluid collection Am. J. Surg. 189: 319, 2005. complications following abdominoplasty. Ann. Plast. Surg. 41: 34. Weinrach, J. C., Cronin, E. D., Smith, B. K., et al. Preventing 498, 1998. seroma in the latissimus dorsi flap donor site with fibrin 47. Stochero, I. N. Ultrasound in the diagnosis and management sealant. Ann. Plast. Surg. 53: 12, 2004. of fluid collection complications following abdominoplasty. 35. Mladick, R. Progressive tension sutures to reduce complica- Ann. Plast. Surg. 52: 331, 2004. tions in abdominoplasty. Plast. Reconstr. Surg. 107: 619, 2001. 48. Hafezi, F., and Nouhi, A. H. Abdominoplasty and seroma. 36. Georgiade, G. S., Georgiade, N. G., Riefkohl, R., and Barwick, W. Textbook of Plastic, Maxillofacial, and Reconstructive Surgery, Ann. Plast. Surg. 48: 109, 2002. 2nd Ed. Baltimore: Williams & Wilkins, 1992. 49. Teimourian, B. Management of seroma in abdominoplasty. 37. Baroudi, R., and Ferreira, A. Seroma: How to avoid it and Aesthetic Surg. J. 25: 510, 2005. how to treat it. Aesthetic Surg. J. 18: 439, 1998. 50. Baxter, R. A. Controlled results in abdominoplasty. Aesthetic 38. Pollock, H., and Pollock, T. Progressive tension sutures: A Plast. Surg. 25: 357, 2001. technique to reduce local complications in abdominoplasty. 51. Johnson, L., Cusick, T. E., Helmer, S., et al. Influence of Plast. Reconstr. Surg. 105: 2583, 2000. fibrin glue on seroma formation after breast surgery. 39. Pollock, H., and Pollock, T. Progressive tension sutures in Am. J. Surg. 189: 319, 2005. abdominoplasty. Clin. Plast. Surg. 31: 583. 2004. 52. Weinrach, J. C., Cronin, E. D., Smith, B. K., et al. Preventing 40. McCarthy, C., Lennox, P., Germann, E., et al. Use of ab- seroma in the latissimus dorsi flap donor site with fibrin dominal quilting sutures for seroma prevention in TRAM sealant. Ann. Plast. Surg. 53: 12, 2004. flap reconstruction: A prospective, controlled trial. Ann. 53. Cruz-Korchin, N., and Korchin, L. The use of fibrin sealant Plast. Surg. 54: 361, 2005. (Tisseel) in abdominoplasty. Plast. Reconstr. Surg. 116 41. Matarasso, A. Abdominoplasty. Clin. Plast. Surg. 16: 289, 1989. (Suppl.): 23, 2005.

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946 DISCUSSION

Progressive Tension Sutures in the Prevention of Postabdominoplasty Seroma: A Prospective, Randomized, Double-Blind Clinical Trial

Harlan Pollock, M.D. Todd Alan Pollock, M.D. Dallas, Texas

he authors are to be commended for the Scarpa’s fascia was not included. This weaker, Tthoroughness of their experimental model, less secure fixation might result in an avulsion data presented, and extensive review of the liter- or partial disruption of flap adherence that ature and list of references. However, in our allows enough movement to promote seroma extensive experience without a single clinically formation. significant seroma, it is difficult for us to under- Of course, another reason for the different stand the reason for the high incidence (35 per- rates of seroma formation observed in our ex- cent) of seromas in the group of patients who perience compared with that found in the have had fixation sutures used. The experimen- study could be our failure to detect small fluid tal design seemed appropriate and generally ob- collections. Because this study was designed to jective. identify all fluid collections both clinically and Yet, in our published series of 65 patients and with ultrasound, there may have been a ten- our subsequent experience with nearly 500 ab- dency to overdiagnose the presence of sero- dominoplasty patients who had progressive ten- mas. The real question is, When is a seroma sion sutures used with no use of suction drains clinically significant? Although in our experi- and early ambulation in an upright posture, we ence, we have neither clinically diagnosed nor observed no clinically significant seromas.1 Al- treated any seromas, it is possible that we may though this was a retrospective study, the com- have failed to diagnose small fluid collections. plete absence of this complication in sequential However, none of our patients developed any patients is a significant finding. Similar results aesthetic or functional sequelae that could be have been reported by others using fixation related to an undiagnosed seroma. Perhaps sutures.2–5 In attempting to reconcile the results the progressive tension sutures give an ade- of this study in light of our clinical experience, quate fixed surface area to allow healing of the we believe that the marked disparity in outcomes opposed surfaces and limit accumulation to an is likely related to differences in surgical tech- amount manageable for easy reabsorption. niques. Finally, it is our experience that the number It is our opinion that the mechanism for se- of sutures is not the significant factor in the roma formation is the shearing force between success of the progressive tension sutures. Al- the mobile skin/fat flap and the abdominal wall though the authors describe using 30 to 40 preventing healing.6 The secure fixation pro- sutures, we routinely use approximately 15 to vided by progressive tension sutures affixing the 20 sutures to accomplish a secure fixation. superficial fascia to the deep fascia under ten- Despite the inability for progressive tension sion in an advanced position prevents any move- sutures to eliminate seroma formation in the ment. If the fixation sutures in this study were abdominoplasty series reported, we remain placed under minimal or no tension, there is the highly enthusiastic about this technique. Even potential for shifting of the tissues and disrup- though the authors have shown only an equal tion of healing. rate of seroma formation with the use of drains Another possible technical variation could or progressive tension sutures, the elimination occur if the sutures were placed superficially of the need for postoperative drains, often for on the deep surface of the skin/fat flap and if extensive periods of time, is of benefit to the patient. Although we cannot definitively ex- Received for publication May 3, 2006. plain the reasons for the different experiences Copyright ©2007 by the American Society of Plastic Surgeons with this technique, we must extol the authors’ DOI: 10.1097/01.prs.0000253546.05360.c1 well-designed experiment. We will continue to

www.PRSJournal.com 947 Plastic and Reconstructive Surgery • September 15, 2007 investigate what difference might account for REFERENCES our disparate experiences in the use of pro- 1. Pollock, H., and Pollock, T. Progressive tension sutures: A gressive tension sutures, which in our experi- technique to reduce local complications in abdominoplasty. ence is a simple addition to abdominoplasty Plast. Reconstr. Surg. 105: 2583, 2000. 2. Baxter, R. Controlled results with abdominoplasty. Aesthetic that significantly reduces complications. Plast. Surg. 25: 357, 2001. 3. Said, T. A. The use of progressive tension sutures for few Harlan Pollock, M.D. complications and speed recovery. Kasr El Aini J. Surg. 6: 2, 8305 Walnut Hill Lane, Suite 210 2005. Dallas, Texas 75231 4. Rios, J. L., Pollock, T., and Adams, W. P. Progressive tension [email protected] sutures to prevent seroma formation after latissimus dorsi harvest. Plast. Reconstr. Surg. 112: 1779, 2003. 5. Mladick, R. Progress tension sutures to reduce complications DISCLOSURE in abdominoplasty. Plast. Reonstr. Surg. 107: 619, 2001. The authors have no financial interest in any of the 6. Pollock, H., and Pollock, T. Progressive tension sutures in products, devices, or drugs mentioned in this article. abdominoplasty. Clin. Plast. Surg. 31: 583, 2004.

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948 DISCUSSION

Progressive Tension Sutures in the Prevention of Postabdominoplasty Seroma: A Prospective, Randomized, Double-Blind Clinical Trial Sumeet S. Teotia, M.D. Dallas, Texas

bdominoplasty is a versatile, increasingly (n ϭ 15). According to their protocol, all drains Apopular, and widely performed procedure were removed on postoperative day 7 and a clinical that successfully treats anterior truncal aesthetic examination was performed. Patients were exam- deformities. In addition to the rare and dreaded ined again at approximately postoperative day 14 complication such as a pulmonary embolism or and a “blinded” clinical and ultrasound assessment complete wound dehiscence, another complica- of seroma was performed. Patients with detectable tion exists that instills a similar dread for both seroma were drained percutaneously and returned the plastic surgeon and the patient: a persistent weekly with a repeated ultrasound until seroma seroma. It is dreadful because when a seroma resolved. Seroma resolved in all but the control from abdominoplasty develops, the surgeon in- group after three aspirations. Excluding the con- vites the nuisance of multiple clinic visits for trol group, the overall clinically detectable seroma painful fluid aspirations, variable patient re- rate was 31 percent and the ultrasound detectable sponses, and the possibility of an operation rate was 89 percent. Individually, the group with should a persistent seroma cavity develop. At this progressive tension sutures only and drain only time, I know that both my patient and I are had a seroma rate of 33 percent, and the group quietly praying for perhaps two different rea- with progressive tension sutures and drains had a sons: the patient hopes not to come back again rate of 27 percent. The overall complication rate of to the clinic for fluid aspirations, and I hope no the entire study group was 34.5 percent, with in- formation of an oozing, recalcitrant, epithelial fection, dehiscence, and abnormal umbilical heal- cavity takes place. My algorithm for the treat- ing being most common. Average patient fol- ment of seroma is generally as follows: (1) repet- low-up was 6 months, with satisfactory aesthetic itive aspirations closely spaced apart to prevent outcome based on an assigned scale. No evidence further accumulation of seroma, (2) injection of of benefit by adding progressive tension sutures to antibiotic (such as tetracycline or neomycin) ei- drains was obtained. The authors concluded that ther directly or through a replaced seroma cath- placing progressive tension sutures is time consum- eter, (3) placement of a larger drain with or ing and has a similar rate of seroma formation as without additional antibiotic, and (4) surgical using drains only. decortication with drains and quilting sutures. Given this, I was surprised by the results of the Restriction of activity or wearing compression study. The study added to the confusion of avail- garment seems homeopathic at this moment. able data that exist regarding progressive tension Thus, it was with anticipation that I read the sutures in abdominoplasty.1–3 The utility of pro- article by Andrades et al. The authors present a gressive tension sutures is based on the theory prospective, randomized, double-blind study to that eliminating dead space reduces fluid collec- evaluate the success of progressive tension sutures tion in a wound that is prone to seroma. Cre- in preventing postabdominoplasty seroma. This is ation of dead space anywhere in the body invites the only such randomized study addressing the accumulation of serum by lymphatic disruption; role of progressive tension sutures in evaluating thus, elimination of that dead space would the- seroma from abdominoplasty. Patients were ran- oretically decrease and eventually eliminate a domized into four groups: control (with no drains serous cavity. Unlike quilting sutures, which sim- or progressive tension sutures, n ϭ 10), progressive ply appose layers of tissue that close dead space, tension sutures only (n ϭ 15), drains only (n ϭ progressive tension sutures have the additional 15), and progressive tension sutures with drains benefit of laminar tissue advancement with ten- sion distributed over a broad surface. Received for publication June 12, 2006. The primary weakness of the study is its lack of Copyright ©2007 by the American Society of Plastic Surgeons power. Prospective, randomized, blinded studies DOI: 10.1097/01.prs.0000253558.03099.bf can convey a powerful message, and there is a lack

www.PRSJournal.com 949 Plastic and Reconstructive Surgery • September 15, 2007 of such designed studies in aesthetic surgery. The tent high volume implies that the drains should authors’ attempt is noteworthy and I praise their continue. Any earlier removal of drains is an invi- effort to undertake such a trial. However, many tation for a seroma. All patients in this study had factors must be accounted for when initiating a drains removed on postoperative day 7. From the randomized trial: no selection bias, a high enough data, the volume of total daily average output from power to detect a meaningful difference, a well- drains before removal was unclear. I understand designed protocol that guides the study to prove or that a standard day on which to remove the drains disprove a proposed null hypothesis, appropriate provided “equal” comparison among all four patient selection, and adherence to some normally groups; however, this may have offset the benefit of accepted clinical management. Unfortunately, this using both progressive tension sutures and drains. study may have come short in all of the above I believe that the study could have benefited from criteria. leaving the drains in until the outputs were insig- The authors divided the groups equally and had nificant enough to warrant removal. It is interest- well-matched patients with regard to age, body ing to note that when comparing ultrasound versus mass index, and history of smoking. Alarmingly, a clinical evaluation of seroma, data were recon- little over 25 percent of the patients were smokers, structed to show a “minimum” volume of 80 ml and it was unclear whether patients had stopped that could be clinically problematic. Again, this is a smoking before surgery. In the group with both “statistically” generated number and should fit the progressive tension sutures and drains, one-third patient accordingly: a patient with a low body mass of patients were smokers. The overall complication index may have a low number compared with rate for the entire study was 34.5 percent, and I those with a high body mass index. I agree that admire the authors’ honesty in their self-criticism drains can cause local irritation and add to patient and reporting of their results. If truly self-critical, discomfort, but I disagree with the authors’ state- we will all find that, much short of perfection, our ment that drains are a source of bacterial migra- true complication rate is probably higher than we tion. It is a surgical myth that drains cause retro- think. Most likely, smoking contributed to the grade bacterial infection. higher rate of overall complications. The authors conclude that progressive tension In general, smokers carry higher morbidity, and sutures are time consuming, are not easy to place, the occurrence of seroma is not an exception to and cause flap dimpling. In this article, technique the rule. Could the beneficial advantages of pro- makes a difference. I believe that using adjunctive gressive tension sutures be offset by including a measures in surgery should not be time consum- group of high-risk patients? The question cannot ing. Other limited locations for placing progressive be answered without another adequately designed tension sutures have been described.4 One can use study comparing normal versus high-risk patients. a technique of placing either interrupted or run- One can argue that perhaps progressive tension ning 2-0/3-0 Vicryl (Ethicon, Inc., Somerville, N.J.) sutures would be ideal for high-risk patients, such above and below the umbilicus in the midline only. as smokers and those with a high body mass index. The suture approximates Scarpa’s fascia to the cen- However, determining the role of progressive ten- trally plicated rectus fascia with advancement. Umbi- sion sutures in high-risk patients was not the intent licus insetting is easier and tension is distributed cen- of this study. In this particular study, even if com- trally. Alternate lateral running or interrupted parisons with nonsmokers were made, the groups sutures may also be placed. The placement of pro- would be too small to derive any meaningful con- gressive tension sutures does not add significantly to clusion. Multivariate analysis in a small cohort of the length of surgery, and dimpling is not a problem. patients can yield dangerous conclusions. Includ- Finally, I believe that there is a positive benefit to ing smokers in this study with other confounding using progressive tension sutures in abdomino- variables was a significant shortcoming. plasty. Progressive tension sutures are adjunctive The most consistent and standard method of measures and should not be abandoned entirely, preventing seroma is passive drainage through sub- but their exact role is yet to be determined. Placing cutaneously tunneled drains. The most common drains should still be the standard of care and indication for removing drains is consecutively de- safety in abdominoplasty. If progressive tension su- creasing output. Many surgeons use a random cut- tures are placed, they should accompany drains off of 20 to 30 ml/day per drain before removal of and be efficient. Progressive tension sutures have drains. We trust and rely on our patients to keep a been shown to decrease drain output, shorten the detailed account of drainage, and for the most duration of drain placement, and decrease the part, we can decipher their data sheets. A persis- overall complication rate.

950 Volume 120, Number 4 • Discussion

Wearing belts and suspenders may not be fash- DISCLOSURE ionable, and wearing one or the other may alone The author has no financial interest in any of the be sufficient; however, occasionally it is prudent to products, devices, or drugs mentioned in this article. use them both. I believe that drains (“belts”) and progressive tension sutures (“suspenders”) to- REFERENCES gether have benefits, and until one can show in a 1. Mladick, R. Progressive tension sutures to reduce compli- large, well-designed, randomized, prospective cations in abdominoplasty. Plast. Reconstr. Surg. 107: 619, study that they are unhelpful, I prefer to “wear” 2001. both of them. 2. Baroudi, R., and Ferreira, A. Seroma: How to avoid it and how to treat it. Aesthetic Surg. J. 18: 439, 1998. Sumeet S. Teotia, M.D. 3. Pollock, H., and Pollock, T. Progressive tension sutures: A Department of Plastic Surgery technique to reduce local complications in abdominoplasty. University of Texas at Southwestern Medical Center Plast. Reconstr. Surg. 105: 2583, 2000. 5323 Harry Hines Boulevard 4. Khan, S., Teotia, S. S., Mullis, W. F., et al. Do progressive Dallas, Texas 75390 tension sutures really decrease complications in abdomino- [email protected] plasty? Ann. Plast. Surg. 56: 14, 2006.

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951 RECONSTRUCTIVE

Free Tissue Transfer to the Lower Extremity Distal to the Zone of Injury: Indications and Outcomes over a 25-Year Experience

Jason A. Spector, M.D. Background: Microvascular free flap anastomoses performed for lower extrem- Steven Levine, M.D. ity reconstruction are traditionally proximal to the zone of injury. The authors Jamie P. Levine, M.D. assessed the feasibility and outcomes of microvascular free flaps with anasto- New York, N.Y. moses performed distal to the zone of injury. Methods: The authors retrospectively reviewed all microvascular free flaps per- formed at their institution over the past 10 years for lower extremity recon- struction and compared this group with their previously published experience (January of 1979 through August of 1995). Between September of 1995 and May of 2005, 119 flap procedures were performed for lower extremity reconstruction. Twenty-eight flaps (24 percent) were anastomosed distal to the zone of injury and 87 (76 percent) were anastomosed proximally. There were insufficient data on the location of the anastomosis for four free flaps (all successful). Results: Twenty-seven of 28 distal microvascular free flaps were successful (96 percent); two (7 percent) required emergent postoperative reexploration of the anastomosis. Of the 87 proximal flaps, 79 (91 percent) were successful and eight (9 percent) failed. There was no statistically significant difference in the success rate of microvascular free flaps between the proximal and distal anastomosis groups (p ϭ 0.30, Fisher’s exact test). Combined with the data from the authors’ previous series (January of 1979 to August of 1995), there were 63 free flaps with anastomosis performed distal to the zone of injury; 61 (97 percent) were successful. Conclusion: The authors’ extensive 25-year experience with lower extremity re- construction demonstrates that in appropriately selected patients, free tissue trans- fer to recipient vessels distal to the zone of injury is reliable and in certain cases preferable. (Plast. Reconstr. Surg. 120: 952, 2007.)

econstruction of lower extremity defects macroscopically evident, and failure to recog- resulting from trauma, ablative surgery, or nize the true extent of this zone is cited as a recalcitrant infection often requires trans- leading cause of microsurgical anastomotic R 1,2 fer of healthy tissue from distant sites. Unlike the failure. trunk or head and neck regions, an entire cir- As a result, when performing microvascular cumferential segment of the lower extremity is tissue transfer, the surgeon may look outside of often damaged. Many lower extremity wounds the zone of injury either distally or proximally to resulting from trauma are high-energy injuries perform an anastomosis. Logically, it would fol- with a substantial “zone of injury.”1,2 This throm- low that the surgeon would prefer to perform a bogenic zone is known to extend beyond what is microvascular anastomosis proximal to the zone of injury because this would prevent the theoret- From the Division of Plastic Surgery, Weill Cornell Medical ical risks associated with blood flow traversing College, and Institute of Reconstructive Plastic Surgery, Di- the damaged tissue.3 Despite the inherent logic vision of Plastic Surgery, New York University School of of this approach, a proximal anastomosis is not Medicine. always practical or even feasible. Received for publication January 26, 2006; accepted June 9, 2006. Previous reports in the literature, including Presented at the 23rd Annual Meeting of the Northeastern one from our institution, have demonstrated Society of Plastic and Reconstructive Surgeons, in Boston, successful outcomes in microvascular free tissue Massachusetts, November 30, 2006. transfer to the lower extremity using recipient Copyright ©2007 by the American Society of Plastic Surgeons vessels distal to the zone of injury in appropri- 4–6 DOI: 10.1097/01.prs.0000255175.92201.c7 ately selected patients. In the 10 years since

952 www.PRSJournal.com Volume 120, Number 4 • Lower Extremity Free Tissue Transfer our last publication, we have performed free Analysis of patient outcomes was performed with tissue transfer for lower extremity reconstruction Fisher’s exact test. in 119 additional patients. The primary purpose of this study is to examine the feasibility and RESULTS reliability of using recipient vessels distal to the Of the 119 microvascular free flaps performed zone of injury when performing microvascular between September of 1995 and May of 2005 for free tissue transfer to the lower extremity. Sec- lower extremity reconstruction, 28 (24 percent) ondarily, we also analyze general trends in our were performed on 26 patients using recipient institution’s approach to lower extremity recon- vessels distal to the zone of injury. Two patients struction, with particular emphasis on a signifi- received two consecutive successful distally anas- cant change in the number of free flaps per- tomosed microvascular free flaps. In one case, a formed per annum. rectus muscle flap was performed for soft-tissue coverage followed by a fibula microvascular free flap 1 year later to address tibial nonunion. In the PATIENTS AND METHODS other case, a rectus muscle flap was performed The records of all patients who underwent acutely (1 day after injury). Although this micro- lower extremity reconstruction with microvascular vascular free flap was completely viable, further free flaps from September of 1995 through May of necrosis of the adjacent tissue necessitated a sec- 2005 at New York University Medical Center ond distally anastomosed microvascular free flap (Tisch Hospital, Bellevue Hospital, and the Man- (latissimus) 5 weeks later that was also successful. hattan Veterans Affairs Hospital) were reviewed There were 21 men and five women, ranging in retrospectively in accordance with New York Uni- age from 18 to 79 years (median, 31 years). The versity Institutional Review Board procedures. time interval between injury and repair ranged Age, type of injury, type of free flap, time between from 0 days to 20 years (median, 43 days). Indi- injury and reconstruction, recipient vessels, whether cations for microvascular free flap reconstruction the recipient vessels were proximal or distal to the were severe soft-tissue defects (21 cases), chronic zone of injury, postoperative outcome, and compli- osteomyelitis (six cases), and an osteomyelitis with cations were recorded. A viable flap at the time of nonunion (one case). discharge was considered a successful outcome. A Of the 28 distally based microvascular free failure was defined as a nonviable microvascular free flaps, 11 were acute (Ͻ21 days), four were sub- flap that required a subsequent free flap or flaps for acute (22 to 60 days), and 13 were chronic (Ͼ60 limb salvage. In addition to comparing outcomes days). The microvascular free flap donor sites in- (proximal versus distal) over the past 10 years, this cluded rectus abdominis (n ϭ 16), latissimus dorsi group of patients was compared with the (previously (n ϭ 7), parascapular (n ϭ 1), tensor fasciae latae reported) cohort of patients who had undergone flap (n ϭ 1), and fibula (n ϭ 3). The recipient lower extremity reconstruction with microvascular arteries used for anastomoses distal to the zone of free flaps at our institution between 1979 and August injury were the posterior tibial (n ϭ 20), anterior of 1995.4 tibial (n ϭ 5), circumflex femoris (n ϭ 1), dorsalis Wounds were classified as acute (up to 21 days), pedis (n ϭ 1), and popliteal (n ϭ 1). The one subacute (21 to 60 days), and chronic (longer than failure in this group was a tensor fasciae latae 60 days), based on the length of time between injury performed 43 days after injury. and microvascular free flap coverage.4 Patients un- The single anastomosis using the popliteal artery derwent preoperative angiography of the affected required a saphenous vein graft. The venous anas- limb only if clear pulses were not discernable (Fig. tomoses in 27 flaps were end to end to the venae 1). In addition, in patients whose injury clearly in- comitantes, whereas a single flap was anastomosed volved destruction of the compartment housing, a end to side to the femoral vein. Twenty-three were corresponding vascular structure (e.g., anterior to a single vein and five were performed to two veins. compartment/anterior tibial vascular bundle), and Eighteen arterial anastomoses were made end to in whom distal pulses remained discernible, angiog- side, eight were made end to end, and in two cases raphy was used specifically to rule out retrograde the type of anastomosis was unknown. These data pulsatile flow. Over the past few years, conventional are summarized in Table 1. angiography has been replaced by magnetic reso- Twenty-seven (96 percent) of the microvascu- nance angiography except when specifically contra- lar free flaps performed distal to the zone of injury indicated. Any clinical suspicion of questionable ve- were successful and one (4 percent) failed. Emer- nous damage mandated a duplex examination. gent reoperation to evaluate anastomotic patency

953 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 1. Evaluation of lower extremity defects. was necessary for salvage in two (7 percent) free anastomotic revision or hematoma evacuation (p ϭ flaps. In both cases, the pedicle was revised at the 0.24, Fisher’s exact test) (Table 2). There were original (distal) location. In one of those cases, insufficient data on the location of the anastomo- venous thrombectomy resulted in flap salvage. In sis for four (3 percent) free flaps (all successful) the other case (arterial thrombosis), flow could performed during this interval. not be successfully reestablished. Eighty-seven When combining the data obtained from Sep- flaps (76 percent) were performed on 78 patients tember of 1995 through June of 2005 with that of with microvascular anastomoses proximal to the our previous series (January of 1979 through Au- zone of injury. Seventy-nine (91 percent) were gust of 1995), of a total of 570 microvascular free successful and eight (9 percent) failed. Thirteen flaps (for 566 of these, we had anastomotic data), (15 percent) free flaps performed proximal to the 63 (11 percent) were performed using recipient zone of injury required emergent reexploration vessels distal to the zone of injury. The overall for salvage (anastomotic revision or hematoma success rate for these distal microvascular free evacuation). Comparing data with the group that flaps was 97 percent (61 of 63 successful). Seven had anastomoses distal to the zone of injury, distal free flaps required emergent reexploration there was no statistically significant difference in the for anastomotic revision or hematoma evacuation. success rate of free tissue transfer between the prox- Of the 566 total lower extremity microvascular imal and distal anastomosis groups (p ϭ 0.30, Fish- free flaps, 503 (89 percent) were performed using er’s exact test) or postoperative reexploration for recipient vessels proximal to the zone of injury. Of

954 oue10 ubr4 Number 120, Volume

Table 1. Patient Summary: Microvascular Free Flaps with Recipient Vessels Distal to the Zone of Injury Interval from Injury to Recipient Vein Age Repair Recipient (No. of Patient (yr) Gender (days) Type of Injury Artery Anastomoses) Anastomosis Flap Complications Outcome 1 29 M 304 L tib osteo PT VC (1) ES Rectus Success 228MϾ91 L tib/fib fx PT VC (1) ES Rectus Success 3 30 M 61 R tib/fib fx PT VC (1) ES Rectus Success 448MϾ91 L tibia osteo PT VC (1) Unknown Rectus Partial inset Success

breakdown • Ͼ

562M 91 R tib/fib fx DP VC (1) ES Rectus Success Transfer Tissue Free Extremity Lower 6 32 F 5 R tib/fib fx PT VC (1) EE Rectus Success 7 21 M 7 L tib/fib fx AT VC (1) EE Rectus Success 22 M 365 L tib/fib fx PT VC (1) ES Fibula Success osteo/nonunion 879FϾ91 R thigh osteo Circumflex VC (1) Unknown LD Success femoris 9 18 M 30 L tib/fib fx PT VC (2) ES LD Success 10 62 M 42 L tib/fib fx PT VC (1) ES Rectus Success 11 57 M 2555 R tib osteo PT VC (1) EE Rectus Success 12 40 F 7300 R knee tumor PT VC (1) ES LD Success 13 49 M 0 L tib/fib fx PT VC (2) EE LD Success 14 21 M 0 R knee tumor AT VC (1) EE LD Success 15 57 M 12 L tib/fib fx PT VC (1) EE Rectus Success 16 45 M 1 L femur tumor Pop/(via Femoral ES LD Success SVG) 17 73 F 43 L degloving injury PT VC ES Tensor fasciae Reexploration for Failure latae arterial thrombosis (kinked pedicle) 18 27 M 69 R tib/fib fx PT VC ES Rectus Reexploration for Success foreign body in donor site 29 27 M 1 L tib/fib fx PT VC (2) ES Parascapular Reexploration for Success venous thrombosis 20 27 M 0 R tib/fib fx PT VC (2) ES Rectus Success 21 19 M 87 L tib/fib fx with AT VC ES Rectus Success osteo (endoscopic) 22 20 M 1 R tib/fib fx PT VC ES Rectus Success 20 M 34 R tib/fib fx AT VC EE LD Success 23 31 M 26 R tib/fib fx PT VC (2) ES Rectus Success 24 25 M 178 R tib/fib fx with PT VC ES Rectus Success osteo 25 47 M 1 L tib/fib fx PT VC ES Fibula Success 26 51 F 87 R tib/fx fx AT VC EE Fibula Success AT, anterior tibial artery; PT, posterior tibial artery; Pop, popliteal artery; VC, venae comitantes; SVG, saphenous vein graft; EE, end to end; ES, end to side; LD, latissimus dorsi; L, left; R, 955 right; tib, tibia; fib, fibula; fx, fracture; osteo, osteomyelitis. Plastic and Reconstructive Surgery • September 15, 2007

Table 2. Lower Extremity Free Flaps (September of 1995 through May of 2005)* Distal (%) Proximal (%) p Total Patients 28 87 — 115 Success 27 (96) 79 (91) 0.30 106 Failure 1 (4) 8 (9) — 9 Emergent postoperative intervention for reexploration of anastomosis or hematoma evacuation 2 (7) 13 (15) 0.24 15 (13) Nonemergent postoperative intervention other than anastomosis exploration or hematoma evacuation (i.e., split-thickness skin graft) 2 (7) 8 (9) 0.54 10 (9) *Does not include four flaps for which the location of the anastomosis was not known.

Table 3. New York University Medical Center Lower Extremity Free Tissue Transfer with Anastomosis Distal to the Zone of Injury: Current versus Previous Experience Previous Experience: Present Experience: September January of 1979–August of of 1995–May of 2005 (%) 1995 (%) Distally anastomosed MVFF 28/115 (24) 35/451 (8) Type of flap Rectus 16 (57) 8 (23) Latissimus dorsi 7 (25) 12 (34) Parascapular 1 (ϳ3.5) 8 (23) TFL 1 (ϳ3.5) 1 (1.5) Fibula 3 (11) Gracilis 3 (9) Serratus 2 (6) Temporalis 1 (1.5) Recipient artery Posterior tibial 20 (71) 22 (63) Anterior tibial 5 (18) 8 (23) Circumflex femoris 1 (3.67) Dorsalis pedis 1 (3.67) 4 (11) Popliteal 1 (3.67)* 1 (3) Recipient vein Venae comitantes 27 (96) 28 (80) Femoral 1 (4) Superficial vein 7 (20) Success rate 27 (96) 33 (94) Emergent reexploration for revision of anastomosis or hematoma evacuation 2 (7) 5 (15) MVFF, microvascular free flaps; TFL, tensor fasciae latae. *Popliteal by means of saphenous vein graft. these 503 microvascular free flaps, 470 (93 per- extremity defects requiring free tissue transfer are cent) were successful and 36 failed (7 percent). often traumatic in origin.17 These high-energy in- Data were unavailable for four (Ͻ1 percent) mi- juries result in tissue damage greater than that crovascular free flaps performed during this time which is macroscopically or even microscopically period (Table 3). apparent. Within this zone of injury, which may extend several centimeters beyond the apparent DISCUSSION wound, susceptible tissue such as vascular endo- Microvascular free tissue transfer to the lower thelium may be irreversibly damaged. In addition, extremity historically has had the highest failure perivascular injury might alter both arterial and rate of any body region, with flap loss rates ranging venous flow dynamics and further increase the from 4 to 20 percent,7–11 compared with 3 to 5 chance of thrombosis.18 Early experience in percent for head and neck.12,13 However, many the microsurgical reconstruction of traumatized groups with significant experience have reported lower limbs demonstrated that intimal damage success rates of greater than 90 percent.10,11,14–16 within the zone of injury increased the likelihood Although multifactorial, one of the principal rea- of thrombosis and subsequent flap failure.2,5,18–22 sons for this inferior outcome is the fact that lower Lower extremity defects created during tumor ex-

956 Volume 120, Number 4 • Lower Extremity Free Tissue Transfer tirpation may also result in a wide though more distal) to the lower extremity whether the anas- controlled zone of injury. tomosis was performed proximal or distal to the To avoid traumatized endothelium when per- zone of injury. forming lower extremity free tissue transfer, the The posterior tibial artery (69 percent) and its reconstructive surgeon may look for recipient ves- associated venae comitantes (97 percent) were the sels either proximal or distal to the zone of injury. recipient vessels most frequently chosen when per- Because of the intercalary nature of these defects, forming distal anastomoses because of their easy a recipient site distal to the zone of injury may have access. Whereas in the first 16 years of our expe- potential problems associated with blood flow tra- rience with lower extremity reconstruction distal versing the injured tissue. Furthermore, vessels to the zone of injury superficial veins were chosen distal to the zone of injury may simply be of smaller as recipient vessels in 20 percent of the cases, in caliber than those located proximal to the zone of the past 10 years, the adjacent venae comitantes injury. were used in all but one flap. This likely reflects the Proximal vessels, however, are located deep realization that, although the comitantes may be within the muscle and require more extensive dis- smaller than their superficial venous counterparts, section and often muscle division to expose the they are reliable and, because of their immediate recipient vessel for the microanastomosis. In ad- proximity to the recipient artery, they are techni- dition, the flap pedicle may need to cross the knee cally easier to use. joint, thereby making it vulnerable to kinking with Another interesting finding in these data are patient leg movement in the postoperative period. the significantly decreased number of lower ex- Furthermore, one or more vein grafts and/or a tremity free tissue transfers over the past 10 years tunneled pedicle might be required with proximal (1995 to 2005) compared with the 16 years prior anastomoses, each of which may predispose the (1979 to 1995). In the more recent period, an flap to thrombosis. In contrast, distal vessels (pos- average of 12 microvascular free flaps per annum terior tibial and dorsalis pedis) are more superfi- were performed for lower extremity reconstruc- cial. Their location makes the anastomosis tech- tion, in contrast to 28 per year during the initial nically easier, requires a shorter pedicle, and may 16 years. Several factors are likely responsible for obviate the possibility of tunneling the pedicle or this difference, such as decreased need for recon- interposition grafts. There is no need to divide struction (possibly attributable to increased motor muscles or to cross the knee joint (Table 4). vehicle safety), alterations in reimbursement, and In the current series, representative of our past changes in personnel. In addition, the discovery of 10 years of experience with lower extremity re- “new” local flaps such as the neurocutaneous re- construction with 119 microvascular free flaps (in verse sural artery flap, and further refinements in 115 of which the location of the anastomosis was the use of local tissues have provided many al- known), 24 percent of lower extremity free tissue ternatives to free tissue transfer.23–25 Skin and transfers were anastomosed to recipient vessels fascial substitutes such as AlloDerm (LifeCell distal to the wound. In the previous 16 years, only Corp., Branchburg, N.J.) and Integra (Integra 8 percent of free tissue transfers were performed Lifesciences Corp., Plainsboro, N.J.) may also al- accordingly. However, when looking at the overall low coverage of wounds previously destined for 25-year experience, there was no statistically sig- microvascular free flaps.26,27 nificant difference in the success of free tissue Perhaps the most significant contributory fac- transfer (93 percent proximal versus 97 percent tor to the decrease in frequency of microvascular free flap lower extremity reconstruction was the implementation of the vacuum-assisted closure Table 4. Lower Extremity Distal Anastomosis device as a first-line treatment, beginning in the Advantages latter half of the 1990s.28–31 This device, combined Distal vessels more superficial with a greater coordination of care between the Technically easier anastomosis Shorter pedicle orthopedic and plastic surgery services, has con- No tunneled pedicle or vein graft tributed significantly to the drastic decrease in the No need to cross knee joint number of lower extremities requiring free tissue No need to divide muscles 32 Disadvantages transfer. Arterial supply and venous drainage of the flap passes Our algorithm for selecting candidates for dis- through the zone of injury with potentially tal anastomosis is outlined in Figure 1. Evaluation unrecognized endothelial and perivascular injury Potentially smaller caliber vessels of lower extremity arterial integrity begins with physical examination. Use of distal recipient ves-

957 Plastic and Reconstructive Surgery • September 15, 2007 sels is clearly contraindicated only if there is clear transfer to recipient vessels distal to the zone of evidence (on physical examination) of injury to injury is reliable and in certain situations even the vessels within or distal to the zone of injury. If preferable. palpable pulses are present and there is no clear Jamie P. Levine, M.D. evidence of vessel injury or associated compart- New York University School of Medicine ment destruction, angiography is usually not 530 1st Avenue indicated.33–35 Because of the negligible morbidity New York, N.Y. 10016 associated with magnetic resonance angiography, this test is used when there is any uncertainty DISCLOSURE regarding vascular status of the lower extremity The authors have no financial interests to disclose. (e.g., a question of retrograde pulses). If the pa- tient is not able to undergo magnetic resonance REFERENCES scanning, a traditional angiogram is obtained as 1. Hammert, W. C., Minarchek, J., and Trzeciak, M. A. Free-flap indicated. Evaluation of venous outflow also de- reconstruction of traumatic lower extremity wounds. pends primarily on physical examination for signs Am. J. Orthop. 29: 22, 2000. of obstruction. A venous duplex examination is 2. Acland, R. D. Refinements in lower extremity free flap sur- indicated only if there is evidence of venous in- gery. Clin. Plast. Surg. 17: 733, 1990. 3. Hallock, G. G. Liability of recipient vessels distal to the zone sufficiency. It is critical to evaluate the patency of of injury when used for extremity free flaps. J. Reconstr. Mi- the recipient vein(s) intraoperatively by injecting crosurg. 12: 89, 1996. heparinized saline after division and noting an 4. Kolker, A. R., Kasabian, A. K., Karp, N. S., et al. Fate of free unresisted flush. If resistance is encountered, flap microanastomosis distal to the zone of injury in lower another recipient vein should be chosen. A two- extremity trauma. Plast. Reconstr. Surg. 99: 1068, 1997. 5. Stompro, B. E., and Stevenson, T. R. Reconstruction of the team approach is recommended so that recipi- traumatized leg: Use of distally based free flaps. Plast. Recon- ent vessels may be fully evaluated for their suit- str. Surg. 93: 1021, 1994. ability for anastomosis before the completion of 6. Mathes, S. Reconstruction of the traumatized leg: Use of the flap elevation. If there is significant doubt about distally-based free flaps (Discussion). Plast. Reconstr. Surg. 93: the availability of either proximal or distal re- 1026, 1994. 7. Tsai, T. M., Bennett, D. L., Pederson, W. C., et al. Compli- cipient vessels, suitable recipient vessels should cations and vascular salvage of free-tissue transfers to the be explored and ensured before initiating flap extremities. Plast. Reconstr. Surg. 82: 1022, 1988. elevation. 8. Bowen, V., and Manktelow, R. T. Complications and unsat- It should be noted that because of the ret- isfactory results in the microsurgical reconstruction of lower rospective nature of this study, in most cases the extremities. Microsurgery 14: 196, 1993. 9. Muramatsu, K., Shigetomi, M., Ihara, K., et al. Vascular com- exact reasons why vessels proximal or distal to plication in free tissue transfer to the leg. Microsurgery 21: 362, the defect were chosen could only be inferred 2001. from the data. Ultimately, the choice of whether 10. Khouri, R. K., and Shaw, W. W. Reconstruction of the lower to use recipient vessels distal to the zone of extremity with microvascular free flaps: A 10-year experience injury depends on objective variables (e.g., lo- with 304 consecutive cases. J. Trauma 29: 1086, 1989. 11. Melissinos, E. G., and Parks, D. H. Post-trauma reconstruc- cation of defect, availability and patency of ves- tion with free tissue transfer: Analysis of 442 consecutive sels, size) and subjective parameters (e.g., sur- cases. J. Trauma 29: 1095, 1989. geon preference, clinical judgment) Finally, 12. Rosenthal, E., Carroll, W., Dobbs, M., et al. Simplifying head when attempting salvage of a single-vessel leg, and neck microvascular reconstruction. Head Neck 26: 930, both the surgeon and the patient must be pre- 2004. 13. Esclamado, R. M., and Carroll, W. R. The pathogenesis of pared for the possibility that anastomotic throm- vascular thrombosis and its impact in microvascular surgery. bosis may cause distal occlusion with resultant Head Neck 21: 355, 1999. limb loss. 14. Buncke, H. J. D. F. (Ed.). Symposium on Clinical Frontiers in Reconstructive Microsurgery. St. Louis: Mosby, 1984. SUMMARY 15. May, J. W., Jr., Gallico, G. G., III, and Lukash, F. N. Micro- vascular transfer of free tissue for closure of bone wounds of The choice of a distal recipient vessel must be the distal lower extremity. N. Engl. J. Med. 306: 253, 1982. judicious. It is predicated on the primary criterion 16. Godina, M. Early microsurgical reconstruction of complex of uninterrupted arterial and venous flow through trauma of the extremities. Plast. Reconstr. Surg. 78: 285, 1986. the zone of injury. If vascular flow is altered or 17. Gorman, P. W., Barnes, C. L., Fischer, T. J., et al. Soft-tissue interrupted, a proximal anastomosis is required. reconstruction in severe lower extremity trauma: A review. Clin. Orthop. Relat. Res. 243: 57, 1989. However, our extensive 25-year experience with 18. Grotting, J. C. Prevention of complications and correction of lower extremity reconstruction demonstrates that postoperative problems in microsurgery of the lower extrem- in appropriately selected patients, free tissue ity. Clin. Plast. Surg. 18: 485, 1991.

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19. Chen, H. C., Chuang, C. C., Chen, S., et al. Selection of 28. Antony, S., and Terrazas, S. A retrospective study: Clinical recipient vessels for free flaps to the distal leg and foot experience using vacuum-assisted closure in the treatment of following trauma. Microsurgery 15: 358, 1994. wounds. J. Natl. Med. Assoc. 96: 1073, 2004. 20. Serafin, D., Sabatier, R. E., Morris, R. L., et al. Reconstruction 29. Parrett, B. M., Matros, E., Pribaz, J. J., et al. Lower extremity of the lower extremity with vascularized composite tissue: trauma: Trends in the management of soft-tissue reconstruc- Improved tissue survival and specific indications. Plast. Re- tion of open tibia-fibula fractures. Plast. Reconstr. Surg. 117: constr. Surg. 66: 230, 1980. 1315, 2006. 21. Khouri, R. K. Avoiding free flap failure. Clin. Plast. Surg. 19: 30. Attinger, C., and Cooper, P. Soft tissue reconstruction for 773, 1992. calcaneal fractures or osteomyelitis. Orthop. Clin. North Am. 22. Lidman, D., and Daniel, R. K. Evaluation of clinical micro- 32: 135, 2001. vascular anastomoses: Reasons for failure. Ann. Plast. Surg. 6: 31. Herscovici, D., Jr., Sanders, R. W., Scaduto, J. M., et al. Vac- 215, 1981. uum-assisted wound closure (VAC therapy) for the manage- 23. Hallock, G. G. Complications of 100 consecutive local fas- ment of patients with high-energy soft tissue injuries. J. Or- ciocutaneous flaps. Plast. Reconstr. Surg. 88: 264, 1991. thop. Trauma 17: 683, 2003. 24. Masquelet, A. C., Romana, M. C., and Wolf, G. Skin island 32. Bihariesingh, V. J., Stolarczyk, E. M., Karim, R. B., et al. Plastic flaps supplied by the vascular axis of the sensitive superficial solutions for orthopaedic problems. Arch. Orthop. Trauma nerves: Anatomic study and clinical experience in the leg. Surg. 124: 73, 2004. Plast. Reconstr. Surg. 89: 1115, 1992. 33. Dublin, B. A., Karp, N. S., Kasabian, A. K., et al. Selective use 25. Price, M. F., Capizzi, P. J., Watterson, P. A., et al. Reverse sural of preoperative lower extremity arteriography in free flap artery flap: Caveats for success. Ann. Plast. Surg. 48: 496, 2002. reconstruction. Ann. Plast. Surg. 38: 404, 1997. 26. Violas, P., Abid, A., Darodes, P., et al. Integra artificial skin 34. Lutz, B. S., Ng, S. H., Cabailo, R., et al. Value of routine in the management of severe tissue defects, including bone angiography before traumatic lower-limb reconstruction exposure, in injured children. J. Pediatr. Orthop. B 14: 381, with microvascular free tissue transplantation. J. Trauma 44: 2005. 682, 1998. 27. Abai, B., Thayer, D., and Glat, P. M. The use of a dermal 35. Lutz, B. S., Wei, F. C., Machens, H. G., et al. Indications and regeneration template (Integra) for acute resurfacing and limitations of angiography before free-flap transplantation to reconstruction of defects created by excision of giant hairy the distal lower leg after trauma: Prospective study in 36 nevi. Plast. Reconstr. Surg. 114: 162, 2004. patients. J. Reconstr. Microsurg. 16: 187, 2000.

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959 RECONSTRUCTIVE

Functional Reconstruction of the Extensor Mechanism following Massive Tumor Resections from the Anterior Compartment of the Thigh

Tamir Pritsch, M.D. Background: The authors describe the surgical technique and functional re- Martin M. Malawer, M.D. sults of extensor mechanism reconstruction after major resections of soft-tissue Chia-Chun Wu, M.D. tumors from the anterior compartment of the thigh. Malcolm H. Squires, M.S. Methods: Between 1983 and 2003, 78 patients with soft-tissue sarcomas of the Jacob Bickels, M.D. anterior compartment of the thigh were operated on at the authors’ institution. Washington, D.C. Sixteen patients with extensive resections of the quadriceps muscle and one patient with a complete resection of the femoral nerve underwent functional extensor mechanism reconstruction. Depending on the type of resection, one or more of the following muscles were used for reconstruction: the sartorius, biceps femoris, semitendinosus muscles. After two patients with a follow-up of less than 12 months were excluded, 15 patients were evaluated. The authors performed a retrospective analysis of these patients’ medical records, with an emphasis on functional outcome. Results: According to the Musculoskeletal Tumor Society score, functional results were estimated to be good to excellent in 13 patients and fair in two. Most patients had a satisfactory active range of motion, and muscle strength and functional results correlated with the extent of resection. Conclusion: The authors recommend functional muscle transfer reconstruction after extensive resection of the quadriceps muscle or resection of the femoral nerve with one or more of the following muscles: the sartorius, the biceps femoris, and the semitendinosus muscles. (Plast. Reconstr. Surg. 120: 960, 2007.)

he anterior compartment of the thigh is found a direct correlation between the extent of the most common location for soft-tissue resection and the isometric strength of the mus- Tsarcomas.1 Resection of tumors in this loca- cle. Capanna et al.3 reported the effect of quad- tion may necessitate en bloc removal of a con- riceps resection on functional outcomes in pa- siderable portion of the quadriceps muscle. tients who underwent distal femoral resection Such a resection may result in a significant de- and prosthetic reconstruction. They likewise crease in muscle strength and may lead to poor concluded that the degree of resection had an functional outcome. In this study, we evaluated important influence on functional results. the outcomes of 15 patients who underwent ma- If a significant amount of quadriceps muscle is jor resections of soft-tissue tumors from the an- resected or if the femoral nerve must be killed, terior compartment of the thigh and functional we routinely reconstruct the extensor mecha- reconstruction of the extensor mechanism. nism to restore strength and to balance patellar Markhede and Stener2 examined the func- tracking. The long head of the biceps femoris tional results after quadriceps resection and muscle is used for reconstruction of the lateral From the Department of Orthopaedic Oncology, Washington aspect of the quadriceps muscle, and the sarto- Cancer Institute, Washington Hospital Center. rius muscle, the semitendinosus muscle, or both Received for publication February 21, 2006; accepted June are used for reconstruction of the medial aspect 9, 2006. of the quadriceps muscle. Copyright ©2007 by the American Society of Plastic Surgeons A search of the English literature failed to DOI: 10.1097/01.prs.0000256477.01388.de uncover any reports on similar muscle transfer

960 www.PRSJournal.com Volume 120, Number 4 • Extensor Mechanism Reconstruction techniques for the reconstruction of the exten- the introduction of magnetic resonance imaging). sor mechanism following soft-tissue tumor resec- Eight patients were treated with induction che- tions and identified only a few reports on latissi- motherapy, nine patients were treated with che- mus dorsi functional transplantation. The motherapy after surgery, and 13 patients under- purpose of this study was to describe the surgical went postoperative radiation therapy. techniques, provide a systematic treatment ap- Fourteen of the 15 resections included a large proach, and report the functional results of mus- amount of the quadriceps muscle. The single ex- cle-transfer reconstruction of the extensor mech- ception was a patient whose femoral nerve was anism after resection of soft-tissue tumors from excised because of malignant peripheral nerve the anterior compartment of the thigh. sheath tumor and who as a result had total paral- ysis of the quadriceps muscle. The median re- PATIENTS AND METHODS sected specimen size was 828 cm3 (range, 480 to Between 1983 and 2003, 78 resections of soft- 4930 cm3). tissue tumors from the anterior compartment of We categorized the types of resections accord- the thigh were performed by the senior author ing to anatomical considerations (Fig. 1). The re- (M.M.M.). From these, we identified 17 patients sections of five patients involved mainly the vastus (22 percent) who underwent extensive soft-tissue lateralis (type A), the resections of six patients resection and muscle transfer reconstruction of involved mainly the vastus medialis (type B), and the extensor mechanism. Two patients with a fol- the resections of two patients involved the rectus low-up of less than 1 year because of early death as femoris and vastus intermedius (type C). One pa- a result of metastatic disease were excluded from tient underwent a subtotal resection of the quad- the study. The remaining 15 patients included 12 riceps muscle (type D). The vastus intermedius male patients and three female patients who was often involved in type A and type B resections. ranged in age from 14 to 70 years (median, 45 Patients who underwent isolated resections of the years). Indications for surgery included high- rectus femoris were usually treated with tenodesis grade soft-tissue sarcomas of the anterior com- of the vastus medialis to the vastus lateralis and partment of the thigh (n ϭ 12), recurrent low- were not included in this study. grade soft-tissue sarcomas of the anterior All patients who had type A resections under- compartment of the thigh (n ϭ 1), and recurrent went reconstruction with the long head of the aggressive fibromatosis of the anterior compart- biceps femoris (Figs. 2 and 3), and all patients who ment of the thigh (n ϭ 2) (Table 1). Patients who had type B or type C resections underwent recon- underwent nonextensive resections, for whom struction with the sartorius muscle (Figs. 4 and 5). muscle transfer was performed mainly to cover The patient with the type D resection underwent bone, joint, or vasculature, were not included in reconstruction with the long head of the biceps fem- this study. oris muscle, the sartorius muscle, and the semiten- Staging studies were performed before surgery dinosus muscle (Fig. 6). The patient whose femoral for all patients. Imaging studies included plain nerve was resected underwent reconstruction of the radiography, computed tomography, and mag- extensor mechanism with both the long head of the netic resonance imaging of the thigh (except for biceps femoris and the semitendinosus muscles; we the first few cases, which were performed before did not transfer the sartorius muscle in that patient because it is innervated by the femoral nerve and thus was paralyzed as well. Table 1. Histopathologic Diagnoses of the 15 Patients Treated with Soft-Tissue Tumor Resection from the Anterior Compartment of the Thigh and Surgical Technique Extensor Mechanism Reconstruction Unique Anatomical Considerations Tumor Type No. of Patients The criterion for the success of a muscle-flap Malignant soft-tissue tumors transfer is maintenance of a pattern of circulation Malignant fibrohistiocytoma 4 that is consistent in location and resistant to the High-grade liposarcoma 3 Recurrent low-grade liposarcoma 1 effect of radiation therapy and superficial trauma. Leiomyosarcoma 3 The surgical manipulation of the muscle flap must MPNST 2 not interrupt its circulation; therefore, a precise Benign aggressive soft- tissue tumors Recurrent aggressive fibromatosis 2 knowledge of the location and pattern of the vas- Total 15 cular pedicle(s) is required. Mathes and Nahai4 MPNST, malignant peripheral nerve sheath tumor. described five patterns of muscle vascular anat-

961 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 1. A schematic representation of the quadriceps resection types: A, resection of the vastus lateralis; B, resection of the vastus medialis; C, resection of the rectus femoris and vastus intermedius; D, Subtotal resection of the quadriceps muscle. Type A and type B resections often include the vastus intermedius as well. omy. The sartorius muscle is supplied by the su- Sartorius Transfer perficial femoral artery and has a segmental vas- After completion of the resection, the sarto- cular pattern (type IV). Each pedicle provides rius muscle is released, but not transected, from its circulation to a portion of the muscle, and division distal insertion on the medial aspect of the prox- of more than three pedicles during the elevation imal tibia (Figs. 4 and 5). The aim is to transfer the of the flap may result in distal muscle necrosis. The muscle anteriorly to the midline to achieve a strait hamstring muscles are supplied by branches of the line of pull between its origin on the anterior profunda femoris artery and have proximal dom- superior iliac spine and the patella. After ligating inant vascular pedicles and distal minor pedicles only two to three distal vascular branches, the (type II vascular pattern). Complete elevation of sartorius can easily be transferred toward the mid- the muscles is possible when the dominant prox- line and sutured to the patellar tendon, the pa- imal vascular pedicles are preserved.4 tella, and the remains of the quadriceps tendon. Hamstring Transfer Because the sartorius muscle has a type IV vascular After completion of the resection, the long pattern, care should be taken not to ligate more head of the biceps laterally or the semitendinosus than three vascular branches to prevent distal flap medially is transected from its insertion on the necrosis.4 head of the fibula or proximal tibia, respectively Postoperatively, all patients are initially treated (Figs. 2 and 3). This transection should be as far with a knee extension brace. Three to 4 weeks after distal as possible to retain a tendinous portion of surgery, an intensive physical therapy program for the muscle. The muscles are transferred anteriorly muscle strengthening and knee range of motion to the midline so that they will have an almost begins. Weaning off the brace proceeds gradually, in direct line of pull. Only a few deep perforating accordance with the patient’s functional improve- branches need to be ligated during this proce- ment. dure. Because of the type II vascular pattern of the All patients were followed for a minimum of 18 hamstring muscles, ligation of distal branches months after surgery (range, 1.5 to 15 years; me- does not jeopardize their vitality.4 Then, using dian, 6.5 years). The retrospective analysis of the heavy, nonabsorbable sutures, the muscles are patient’s medical records included functional out- transplanted onto the patella and the remains of come, knee stability and range of motion, exten- the quadriceps tendon and rectus femoris. sor mechanism strength evaluation, complication

962 Volume 120, Number 4 • Extensor Mechanism Reconstruction

Fig. 2. Type A resection (vastus lateralis and vastus intermedius) and reconstruction with biceps femoris transfer. (Above, left) Pre- operative view of a patient with a large malignant soft-tissue sarcoma in the lateral aspect of the anterior compartment of the thigh. (Above, right) Resection includes the vastus lateralis and part of the vastus intermedius and rectus femoris. (Below, left) After com- pletion of the resection, the lateral aspect of the femur is exposed. (Below, right) The long head of the biceps femoris is transferred anteriorly and sutured to the patella and the remains of the quadriceps tendon and rectus femoris (RF).

Fig.3. SchematicdepictionsofmuscletransferfortypeAresection(vastuslateralis with or without vastus intermedius). The long head of the biceps femoris is trans- ferred anteriorly and sutured to the patella, the quadriceps tendon, and the rectus femoris muscle.

963 Plastic and Reconstructive Surgery • September 15, 2007

who underwent radical resection and muscle transfer reconstruction of the extensor mecha- nism between 1983 and 2003.

Strength and Range of Motion At their most recent follow-up, four patients (26.7 percent) achieved normal active range of motion. Fourteen patients (93.3 percent) had full passive knee extension, and one had a flexion contracture of 10 degrees. Four patients (26.7 per- cent) achieved normal active knee flexion, 10 pa- tients (66.7 percent) had mild to moderate im- pairment in knee flexion (range, 90 to 120 degrees), and one patient had 70 degrees of active and passive knee flexion. Five patients (33.3 per- cent) sustained extension lag of 10 to 30 degrees (Table 3). The strength of the extensor mecha- nism was estimated to be 3/5 in three patients (20 percent), 4/5 in four patients (26.7 percent), and 5/5 in eight patients (53.3 percent). The extent of resection had a clear impact on the strength of the extensor mechanism. Patients who underwent resections of less than 850 cm3 had Fig. 4. Schematic depiction of muscle transfer for type B resec- a significantly stronger extensor mechanism than tion (vastus medialis with or without vastus intermedius). The patients whose resection sizes were larger than 850 sartorius muscle is transferred anteriorly but not detached from cm3 (p ϭ 0.024). Of the seven patients who un- its distal insertion, and sutured to the patellar tendon, patella, derwent resections measuring less than 850 cm3, quadriceps tendon, and rectus femoris muscle. six had normal strength; the remaining patient had mild weakness of the extensor mechanism. Two of the three patients with 3/5 muscle strength rate, and the incidence of local recurrence and had resections of more than 1200 cm3, and the distant metastasis. Table 2 details the grading sys- third patient had complete resection of the fem- tem according to which muscle strength assess- oral nerve and total paralysis of the quadriceps 5 ments were made. Functional outcomes were as- muscle. Knee stability was intact in all patients, and sessed according to the Musculoskeletal Tumor none had complaints consistent with patellofemo- 6 Society system. This system assigns numerical val- ral instability. ues for each of six categories: pain, function, emo- tional acceptance, support, gait, and walking abil- ity. Outcomes were categorized according to the Functional Results following accepted index: excellent, greater than According to the Musculoskeletal Tumor So- 90 percent; good, 80 to 89 percent; fair, 60 to 79 ciety score, functional results were estimated to be percent; and poor, less than 59 percent. Results good to excellent in 13 patients (86.7 percent) presented here are based on each patient’s most and fair in two patients (Table 3). There was a recent follow-up. marginally significant correlation between resec- The correlations between the size of resection tion sizes of less than 850 cm3 and better func- and extensor mechanism strength and between tional results (p ϭ 0.083). Both patients whose the size of resection and functional results were functional results were fair had resections of more tested using the Spearman rank correlation sta- than 1200 cm3. One patient underwent a com- tistical test. A value of p Ͻ 0.05 was considered bined reconstruction with the long head of the significant. biceps femoris muscle, the sartorius muscle, and the semitendinosus muscle after type D resection; the other was a 70-year-old patient who underwent RESULTS type A resection and reconstruction with the long We evaluated 15 patients with soft-tissue tu- head of the biceps femoris because of malignant mors of the anterior compartment of the thigh fibrous histiocytoma.

964 Volume 120, Number 4 • Extensor Mechanism Reconstruction

Fig. 5. Schematic depictions of muscle transfer for type C resection (rectus femoris andvastusintermedius).Thesartoriusmuscleismobilizedanteriorlyandsuturedto the patella and the remains of the quadriceps tendon.

Fig. 6. Schematic depictions of muscle transfer for type D resection (subtotal resection). Thebicepsfemorislaterallyandthesartoriusandsemitendinosusmediallyaretransferred anteriorly, tenodesed to each other, and sutured to the patella.

965 Plastic and Reconstructive Surgery • September 15, 2007

Table 2. Grading System for Quadriceps Muscle cles have been used to substitute for the paralyzed Strength* quadriceps. Goldthwait7 was the first to report on Grade Value Movement a sartorius transfer, and Fritz Lange used a biceps 8 5 Normal Able to extend knee against gravity femoris transfer in 1900. Other authors, mostly with maximal resistance during the first half of the twentieth century, re- 4 Good Able to extend knee against gravity ported their experience in various muscle-transfer with some (moderate) resistance techniques for quadriceps paralysis.8–11 In 1996, 3 Fair Able to extend knee against gravity 12 2 Poor Able to extend knee when gravity Hossein et al. reported on 15 polio patients with eliminated quadriceps paralysis who underwent extensor 1 Trace Evidence of slight contractility but mechanism reconstruction with biceps femoris no joint motion 0 Zero No contraction palpated muscle transfers. Eighty-six percent of these pa- Data derived from Sepega, A. A. Muscle performance evaluation in tients had good to excellent results, and the mean orthopedic practice. J. Bone Joint Surg. (Am.) 1562: 72, 1990. extension lag was 30 degrees. The purpose of this study was to describe the surgical techniques, provide a systematic treat- Tumor Status and Postoperative Complications ment approach, and evaluate the clinical out- One patient who had been treated with radi- comes of patients who underwent muscle transfer ation therapy before surgery developed wound reconstructions of the extensor mechanism after dehiscence. It was treated successfully with local resections of soft-tissue tumors from the anterior debridement and primary closure. One patient compartment of the thigh. Our inclusion criterion had regional recurrence in the groin that neces- was a need for functional reconstruction because sitated further resection, and four patients with of severe compromise of the quadriceps muscle. high-grade soft-tissue sarcomas developed distant We excluded all patients in whom muscle flaps metastasis. were used mostly for bone and neurovascular cov- erage. DISCUSSION The functional outcomes presented here in- The anterior compartment of the thigh is the dicate that sartorius, semitendinosus, and biceps most common compartment for soft-tissue sarco- femoris muscle transfers are successful techniques mas; however, in our series, only 22 percent of for reconstruction of the extensor mechanism in these cases underwent massive resections that ne- patients with extensive compromise of the quad- cessitated functional reconstruction of the exten- riceps muscle. Thirteen patients (86.7 percent) in sor mechanism. our series had good to excellent functional results; Our reconstruction techniques were based on the other two had fair results. Range of motion was methods for quadriceps reconstruction that had generally satisfactory, and muscle strength was in- been originally designed for the treatment of po- tact in 53.3 percent of patients and mildly dimin- lio patients with quadriceps paralysis. Various mus- ished in 26.7 percent of patients. Only three pa-

Table 3. Clinical Data of the Type and Size of Resection, and Functional Results of 15 Patients Who Underwent Muscle Transfer Reconstruction of the Extensor Mechanism Age Resection Resection Extensor Lag Active Flexion MSTS Functional Patient (yr) Type Size (cm3) (degrees) (degrees) Strength Score 1 67 C 480 0 135 5 Excellent 2 57 C 560 0 120 5 Excellent 3 45 B 648 0 100 5 Excellent 4 40 B 720 20 135 4 Good 5 55 B 768 0 130 5 Excellent 6 36 A 810 0 110 5 Excellent 7 14 B 828 0 130 5 Excellent 8 27 A 872 0 100 4 Excellent 9 54 A 1220 30 90 3 Fair 10 45 B 1430 10 70 4 Good 11 70 D 1912 20 90 3 Fair 12 54 B 2200 0 120 5 Excellent 13 60 A 3600 0 130 5 Excellent 14 41 A 4930 0 115 4 Good 15 38 FN N/A 25 90 3 Good MSTS, Musculoskeletal Tumor Society; FN, femoral nerve; N/A, not applicable.

966 Volume 120, Number 4 • Extensor Mechanism Reconstruction tients (20 percent) had 3/5 muscle strength of the None of the patients who underwent extensor extensor mechanism. mechanism reconstruction with the hamstring The extent of resection significantly corre- muscles demonstrated functional impairment in lated with muscle strength and correlated with knee flexion. Markhede and Stener2 studied the marginal significance with functional results. Most functional implications of hamstring muscle re- patients with extensor mechanism weakness un- section and concluded that despite a loss of 24 and derwent resections of more than 850 cm3, and 28 percent of isometric knee flexion strength both patients with fair results had resections of when the semitendinosus or the biceps femoris more than 1200 cm3. muscles were resected, respectively, resection of As a control group, we relied on data from the one of the hamstring muscles did not cause any English literature regarding the functional results functional impairment; only the complete resec- after quadriceps resection. Markhede and Stener2 tion of all three hamstring muscles moderately examined the postoperative function in 17 pa- impaired knee flexion. Because the hamstring tients who underwent quadriceps muscle resec- transfer techniques described in this study in- tions. They found that the isometric strength of volved only the long head of the biceps femoris the muscle decreased by 22, 33, 55, and 76 percent muscle with or without the semitendinosus mus- when one, two, three, or more components of the cle, and because the majority of the knee flexors quadriceps muscle were resected, respectively. Ca- (i.e., the semimembranosus, the short head of the panna et al.3 reported on the functional effect of biceps femoris, and the gastrocnemius muscles) quadriceps resection combined with distal femo- were not involved in any of the reconstructive ral resection and prosthetic reconstruction in pa- procedures, the absence of negative functional tients with malignant bone tumors. They con- implications on knee flexion is not surprising. cluded that the degree of quadriceps resection has Another reported reconstruction method for a strong impact on functional outcome. In their large defects of the quadriceps muscle is func- series, eight patients had sartorius or biceps fem- tional reconstruction with latissimus dorsi trans- oris muscle-transfer reconstructions; three recon- plantation. Ihara et al.15 reported on 23 patients structions where performed for extensive resec- who underwent free reinnervated functional mus- tions of the quadriceps and five were performed cle transplantations following upper and lower for nonextensive resections or total resections of extremity sarcoma resections; latissimus dorsi the quadriceps muscle. These authors did not de- functional transplantations were used for the re- scribe their techniques, nor did they provide in- construction of eight large defects of quadriceps formation on the range of motion of the knees or muscles. Although a detailed description of the the strength of the extensor mechanisms follow- results of those eight patients is lacking, the overall ing surgery; nonetheless, they concluded that only reported functional outcomes were satisfactory, patients with extensive quadriceps resections ben- and all but one patient, whose quadriceps was efited from the reconstructive procedures. completely excised, demonstrated knee extension Malawer13 performed a gait electromyographic strength greater than 2/5. Two other case reports analysis on a patient who underwent distal femoral on reconstruction of the extensor mechanism us- resection, endoprosthetic replacement, and ex- ing latissimus dorsi functional transplantation also tensor mechanism reconstruction with the sarto- reported good functional results.16,17 rius and biceps femoris muscles. It revealed that 6 Because of the paucity of reported data and months after the operation, both muscles were the lack of comparative studies, it is difficult to recruiting in phase with the rectus femoris of the adequately compare the functional results of la- same limb. tissimus dorsi transplantation to the results of the The biceps femoris and semitendinosus make reconstruction techniques presented here; how- good muscle transfers because of their proximal ever, there are several advantages to muscle trans- blood supply (type IV vascular pattern), which en- fers over muscle functional transplantation: an ables one to ligate distal branches and to shift the available specialized microneurovascular team is muscles anteriorly without the risk of flap necrosis.3 not necessary, the operative time is significantly The sartorius muscle is very useful for reconstructing shorter, there is no donor-site morbidity, and re- the extensor mechanism because it is innervated, as covery time is shorter because the innervation of is the quadriceps muscle, by the femoral nerve, and the transferred muscles is not compromised and will thus easily adapt to its new function and work in soft-tissue healing is the only limiting factor for phase with the remaining quadriceps.14 their activation as knee extensors.

967 Plastic and Reconstructive Surgery • September 15, 2007

Ihara et al.15 reported a mean operative time surgeon, who usually faces the challenge of re- of 7.6 hours for tumor resection and free muscle constructing the large defects. In addition, high- flap functional reconstruction and a constant op- energy trauma to the thigh, aggressive debride- erative time of 4 hours for harvesting the flap, ment of the quadriceps muscle because of placing it in a new position, and performing the fulminant infection, and other nononcologic sce- microsurgical repair. In addition, the average time narios can severely compromise the extensor for the appearance of motor unit potentials in mechanism. Applying the reconstructive proce- their series was 6 months, and visible contractions dures presented in this article may improve the of muscles usually appeared 1 to 2 months after end functional outcomes in such cases as well. reinnervation. Tamir Pritsch, M.D. Nevertheless, considering its good reported Orthopedic Oncology, C2173 functional results, we believe latissimus dorsi Washington Cancer Institute transplantation should be used whenever the mus- 110 Irving Street, NW cle transfers presented in this study cannot be Washington, D.C. 20010 performed. In addition, combining the two re- [email protected] constructive techniques might yield better func- tional results in patients whose quadriceps mus- ACKNOWLEDGMENT cles were completely resected. Funding was provided exclusively by the Department of Orthopaedic Oncology of the Washington Cancer In- CONCLUSIONS stitute, Washington, D.C. On the basis of the results reported here, we suggest muscle transfers as the reconstructive pro- DISCLOSURES cedures of choice after extensive resection of the None of the authors has any financial arrangements or quadriceps muscle or resection of the femoral potential conflicts of interest to disclose. This study was not nerve. For resections of the lateral aspect of the sponsored by any external entities or commercial interests. quadriceps muscle (type A), reconstruction with the long head of the biceps femoris muscle is most REFERENCES appropriate. For resections of the medial aspect of 1. Enneking, W. F., Spanier, S. S., and Malawer, M. M. The effect the quadriceps muscle and for resections of the of the anatomic setting on the results of surgical procedures for middle portion (type B and type C, respectively), soft parts sarcoma of the thigh. Cancer 47: 1005, 1981. reconstruction with the sartorius muscle is recom- 2. Markhede, G., and Stener, B. Function after removal of var- mended. For subtotal resections of the quadriceps ious hip and thigh muscles for extirpation of tumors. Acta Orthop. Scand. 52: 373, 1981. (type D), reconstruction with the sartorius, the 3. Capanna, R., Ruggieri, P., Biagino, R., et al. The effect of semitendinosus, and the long head of the biceps quadriceps excision on functional results after distal femoral femoris is recommended. When the femoral nerve resection and prosthetic replacement of bone tumors. Clin. is excised, reconstruction should include the long Orthop. Relat. Res. 267: 186, 1991. head of the biceps femoris for the lateral aspect 4. Mathes, S. J., and Nahai, F. Vascular anatomy of muscle: Classification and application. In S. J. Mathes and F. Nahai and the semitendinosus muscle for the medial (Eds.), Clinical Applications for Muscle and Musculocutaneous aspect. The sartorius muscle is not used because it Flaps, 1st Ed. St. Louis, Mo.: Mosby, 1982. P. 16. is innervated by the femoral nerve and will also be 5. Sepega, A. A. Muscle performance evaluation in orthopedic paralyzed in these patients. We believe that latis- practice. J. Bone Joint Surg. (Am.) 1562: 72, 1990. simus dorsi functional transplantation should be 6. Enneking, W. F., Dunham, W., Gebhardt, M. C., et al. A system for the functional evaluation of reconstructive pro- used when the muscle transfers described in this cedures after surgical treatment of tumors of the musculo- study cannot be performed, and possibly in con- skeletal system. Clin. Orthop. Relat. Res. 286: 241, 1993. junction with the hamstring and sartorius trans- 7. Goldthwait, J. E. The direct transplantation of muscles in the fers for functional reconstruction of the extensor treatment of paralytic deformities. Trans. Am. Orthop. Assoc. mechanism following complete resection of the 10: 246, 1897. 8. Broderick, T. F., Reidy, J. A., and Barr, J. S. Tendon trans- quadriceps muscle. plantation in the lower extremity: A review of end results in Finally, we believe that this study is of interest poliomyelitis II. J. Bone Joint Surg. (Am.) 34: 909, 1952. not only to orthopedic oncologists but to plastic 9. Kuhlmann, R. F., and Bell, J. F. A clinical evaluation of surgeons as well. Soft-tissue sarcomas are rare dis- tendon transplantation for poliomyelitis affecting the lower eases, usually treated in tertiary referral centers extremities. J. Bone Joint Surg. (Am.) 34: 915, 1952. 10. Mayer, L. Tendon transplantation on the lower extremity. and multimodality surgical treatment is often re- Inst. Course Lect. 6: 189, 1949. quired, including an orthopedic oncologist, a gen- 11. Ober, F. R. Tendon transplantation in the lower extremity. eral surgeon, a vascular surgeon, and a plastic N. Engl. J. Med. 209: 52, 1933.

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12. Hossein, S. G., Mahzad, J., and Bahram, Z. Hamstring tendon 15. Ihara, K., Shigetomi, M., Kawai, S., Doi, K., and Yamamoto, transfer for quadriceps femoris paralysis. J. Pediatr. Orthop. 16: M. Functioning muscle transplantation after wide excision of 765, 1996. sarcomas in the extremity. Clin. Orthop. Relat. Res. 358: 140, 13. Malawer, M. M. Distal femoral osteogenic sarcoma: Principles 1999. of soft-tissue resection and reconstruction in conjunction with 16. Hallock, G. G. Restoration of quadriceps femoris function prosthetic replacement (adjuvant surgical procedures). In J. with a dynamic microsurgical free latissimus dorsi transfer. Lane (Ed.), Design and Application of Tumor Prostheses for Bone and Ann. Plast. Surg. 52: 89, 2004. Joint Reconstruction. New York: Thieme-Stratton, 1983. P. 297. 17. Willcox, T. M., Smith, A. A., Beauchamp, C., and Meland, 14. Malawer, M. M., and Kellar-Graney, K. Soft-tissue reconstruc- N. B. Functional free latissimus dorsi muscle flap to the tion after limb-sparing surgery for tumors of the upper and proximal lower extremity. Clin. Orthop. Relat. Res. 410: lower extremities. Oper. Tech. Orthop. 14: 276, 2005. 285, 2003.

Online CME Collections This partial list of titles in the developing archive of CME article collections is available online at www. PRSJournal.com. These articles are suitable to use as study guides for board certification and/or recertification, to help readers refamiliarize themselves on a particular topic, or to serve as useful reference articles. Articles less than 3 years old can be taken for CME credit. Reconstructive Lower Extremity Lower Extremity Microsurgical Reconstruction—Lior Heller and L. Scott Levin Pharmacologic Optimization of Microsurgery in the New Millennium—Matthew H. Conrad and William P. Adams, Jr. Direct and Indirect Perforator Flaps: The History and the Controversy—Geoffrey G. Hallock The “Gent” Consensus on Perforator Flap Terminology: Preliminary Definitions—Phillip N. Blondeel et al. Further Clarification of the Nomenclature for Compound Flaps—Geoffrey G. Hallock

969 HAND/PERIPHERAL NERVE

Free Vascularized Tissue Transfer to Preserve Upper Extremity Amputation Levels

Alessio Baccarani, M.D. Background: Free vascularized tissue transfer to preserve upper extremity am- Keith E. Follmar, M.D. putation level is an uncommon procedure. The authors investigate the role of Giorgio De Santis, M.D. free tissue transfer in preserving both morphology and function of the ampu- Roberto Adani, M.D. tated upper extremity, with the goal of facilitating prosthetic rehabilitation. Massimo Pinelli, M.D. Methods: Thirteen patients who underwent microsurgical free tissue transfer to Marco Innocenti, M.D. preserve upper extremity amputation level were reviewed retrospectively. These Steffen Baumeister, M.D. cases were selected from four centers: Duke University Medical Center Henning von Gregory, M.D. (Durham, N.C.) University Hospital of Modena (Modena, Italy), Careggi Uni- Gu¨nter Germann, M.D., Ph.D. versity Hospital (Florence, Italy), and the University of Heidelberg (Heidelberg, Detlev Erdmann, M.D., Ph.D., Germany). Parameters that were evaluated included age, sex, cause of the defect, M.H.S. reconstructive procedure, structures to be salvaged, and functional outcome, L. Scott Levin, M.D. among others. Durham, N.C.; Modena and Florence, Results: The cause of amputation was trauma in 92 percent of patients. Mean Italy; and Heidelberg, Germany age was 32 years. In 31 percent of the cases, an emergency free fillet flap was used, and in the remaining 69 percent, a traditional free flap was performed. Struc- tures/function to be preserved included pinch function to the hand, function of the elbow and shoulder joints, and skeletal length greater than 7 cm. Com- plications occurred in 38 percent of the cases, but the final goal of the procedure was achieved in all cases. A treatment algorithm for the management of the amputated upper extremity is presented. Conclusion: Use of free vascularized tissue transfer for preservation of upper extremity amputation level in well-selected cases facilitates prosthetic rehabilitation and improves residual limb function. (Plast. Reconstr. Surg. 120: 971, 2007.)

pper extremity defects resulting from process can be challenging in these patients, trauma and oncologic resections often re- especially in acute trauma situations. Decisions Uquire sophisticated reconstructive strate- related to hemodynamic stability, indication for gies. Total limb salvage is always the primary goal surgery, timing of surgery, and the operative to be pursued. In those circumstances in which plan must be made. If a traditional free flap is amputation is unavoidable, every effort should chosen to preserve part of the injured extremity, be made to provide the patient with the most donor-site morbidity must be carefully weighed functional residual limb, given the patient’s pre- against the benefit the patient is to derive from reconstruction status. This usually means preser- preserving the amputation level. vation of skeletal length and, when possible, sal- The “spare part” concept has become well- vage of a critical joint. The decision-making accepted for both the emergency and the elec- tive surgical treatment of oncologic resections1 From the Division of Plastic, Reconstructive, Maxillofacial, and of massive traumatic injuries to the limbs.2–7 and Oral Surgery, Duke University Medical Center; Division The rotation-transposition and the less frequent of Plastic and Reconstructive Surgery, University of Modena microsurgical transfer of tissue from a nonre- and Reggio Emilia; Division of Reconstructive Microsurgery, Careggi University Hospital; and Department of Plastic, plantable amputated segment to cover an in- Reconstructive, and Hand Surgery, BG Trauma Center jured extremity (fillet flap) represent well- Ludwigshafen, University of Heidelberg. established technical resources.8 Received for publication April 25, 2006; accepted July 7, Those so-called salvage replantations have 2006. been frequently reported in the lower extremity Copyright ©2007 by the American Society of Plastic Surgeons for knee preservation9,10 but less frequently for DOI: 10.1097/01.prs.0000256479.54755.f6 the upper extremity.11 The obvious benefit in

www.PRSJournal.com 971 Plastic and Reconstructive Surgery • September 15, 2007 the use of spare parts is the avoidance of any retrospectively the role of free tissue transfers in additional donor-site morbidity.12,13 Transferring preserving both morphology and function of tissue from a nonreplantable limb is, however, amputated upper extremities and to describe a not always possible. If the limb is so severely treatment algorithm based on the results of our injured as to be rendered “nonreplantable,” it is multicenter study. frequently also too severely injured to serve as a source of spare parts of sufficient size. Further- PATIENTS AND METHODS more, the amputation specimen may have been In 13 cases, free vascularized tissue was trans- ischemic for a prolonged period of time before ferred to an upper extremity amputation site to pre- revascularization is logistically possible. serve amputation level. These cases came from four Alternatively, traditional (nonfillet) free com- centers: Duke University Medical Center (Durham, posite tissue transfers to upper extremity ampu- N.C.), Modena University Hospital (Modena, Italy), tation sites can be performed. Perhaps because Carreggi Hospital (Florence, Italy), and the Univer- of the donor-site morbidity, this is a less common sity of Heidelberg (Heidelberg, Germany). procedure, and its true indications are somewhat Patient data were collected retrospectively by controversial.14 In fact, no sizable series report- means of a chart review. Parameters recorded in- ing the use of microsurgical free flaps to pre- cluded age, gender, occupation, cause of defect, serve upper extremity amputation levels has prereconstruction diagnosis, amputation site with- been reported in the literature, to our knowl- out free flap, reconstructive procedure (type of edge. The goal of this study was to investigate free tissue transfer), structures to be salvaged,

Table 1. Patients’ Preoperative Characteristics Age Patient City (yr) Sex Occupation Cause Diagnosis/Defect 1 Durham, N.C. 21 Female NA Trauma (MVC, ejected) RUE above-elbow traumatic amputation (complete), humerus intact 2 Durham, N.C. 48 Male Laborer Trauma (RUE trapped Right proximal forearm in shredder machine) amputation 3 Durham, N.C. 33 Male Golf instructor Traumatic/occupational Right midforearm (drilling post holes) amputation (10 cm of exposed radius and ulna) 4 Durham, N.C. 44 Male NA Trauma/occupational Right forearm avulsion injury 5 Florence, 67 Female NA Soft-tissue sarcoma, RUE below-shoulder Italy right elbow amputation 6 Florence, 28 Male NA Trauma (crush) Avulsion amputation of the Italy middle right forearm with more proximal soft- tissue involvement 7 Modena, Italy 21 Male Desk job Trauma (MVC) RUE exposed amputation (proximal humerus) 8 Modena, Italy 30 Male Laborer Trauma (bomb blast) Right midforearm amputation (7 cm of exposed radius and ulna) 9 Modena, Italy 35 Female Teacher Trauma (MVC) RUE exposed amputation (mid humerus) 10 Modena, Italy 32 Male Desk job Trauma (thermal and Right hand, necrosis of compression injury) digits II–V (exposed F1) 11 Heidelberg, 19 Male Heavy laborer Trauma (friction burn Right hand, necrosis of Germany in an industrial digits II–V (exposed MCP machine) joints) 12 Heidelberg, 21 Male Factory worker Trauma (thermal and Right hand and forearm Germany compression injury) necrosis 13 Heidelberg, 14 Female Trauma (high-voltage LUE below-shoulder Germany burn, 43% TBSA), s/p amputation proximal arm amputation MVC, motor vehicle collision; RUE, right upper extremity; MCP, metacarpophalangeal; TSBA, total body surface area; s/p ϭ status post; LUE, left upper extremity; NA, not available.

972 Volume 120, Number 4 • Free Vascularized Tissue Transfer postoperative complications, length of hospital University Hospital (n ϭ 4), Carreggi Hospital stay, functional outcome (including prosthetic re- (n ϭ 2), and the University of Heidelberg (n ϭ 3). habilitation), and length of follow-up. In each Age ranged from 14 to 67 years (mean, 32 years). case, the operating surgeon was consulted to eval- Nine patients were male and four were female. All uate all aspects of long-term outcome, including patients’ preoperative characteristics are summa- wound healing, preservation of length, and func- rized in Table 1. tional status. Preoperative data, operative data, The cause of the defect was mechanical and outcomes were summarized in tabular format. trauma in eight patients (61.5 percent), burn or Because of the small number of patents, no sta- electrical injury in four patients (31 percent), tistical analysis was performed. and oncologic resection in one patient (8 per- cent). In two cases, the defect was to the hand, RESULTS and in the other 11 cases the upper extremity Patients from all four centers were included: was injured more proximally (shoulder/arm, Duke University Medical Center (n ϭ 4), Modena five cases; elbow/forearm, six cases).

Table 2. Amputation Level without Free Flap, Procedures, and Indications Amputation Site without Structures to Be Salvaged Patient Free Flap Procedure (Indication) 1 Mid transhumeral Right forearm myocutaneous fillet flap Salvage of distal 50% of humerus (brachial artery to axillary artery, brachial and cephalic veins) 2 Elbow disarticulation Right forearm fillet flap (radial and Salvage of proximal third of forearm ulnar arteries to brachial artery, veins not specified) 3 Distal transhumeral Right hand/forearm fillet flap Salvage of the elbow joint plus 10 cm (brachial artery to axillary artery, of forearm brachial and cephalic veins) 4 Distal transhumeral Anterolateral thigh flap to right Salvage of the elbow joint forearm (perforating artery to brachial artery, brachial vein) 5 Forequarter/shoulder Right forearm myocutaneous fillet flap Large skin defect that needed a free disarticulation to cover the exposed shoulder joint flap, reduced the morbidity of the (radial and ulnar artery to axillary reconstructive procedure artery) 6 Distal transhumeral/elbow Coverage of the forearm bone stumps Salvage of the elbow joint disarticulation with a free latissimus dorsi 7 Shoulder disarticulation Free latissimus dorsi (contralateral) Salvage of proximal third of humerus; to avoid shortening of the stump with subsequent impossibility for the prosthesis to grip 8 Distal transhumeral Free latissimus dorsi Salvage of the elbow joint plus 7 cm of forearm 9 Shoulder disarticulation Free latissimus dorsi (contralateral) Salvage of proximal 50% of humerus; to avoid shortening of the stump with subsequent impossibility for the prosthesis to grip 10 MCP joints Free lateral arm flap to cover the four Salvage of MCP joints and F1 of the joints; secondary expansion of the four digits flap with tubular expander after 1 mo, followed by separation of the flap into four parts 11 Metacarpal heads Free parascapular (failed), free Salvage of MCP joints latissimus dorsi (failed) 12 Proximal-mid transradial Free latissimus dorsi Salvage of middle-distal third of forearm 13 Proximal transhumeral Free fibula to proximal amputation Arm elongation stump of humerus, pedicled latissimus dorsi to provide soft-tissue coverage MCP, metacarpophalangeal.

973 Plastic and Reconstructive Surgery • September 15, 2007

Table 3. Complications and Functional Outcome Hospital Functional Outcome, Stay Including Prosthetic Patient Postoperative Complications (days) Rehabilitation Follow-Up Comments 1 None 12 Good; Utah arm 1 yr 2 Partial necrosis of fillet flap 18 Good; body-powered 1yr requiring I&D below-elbow prosthesis 3 None 25 Excellent; body-powered 1yr below-elbow prosthesis 4 Reanastomosis of vein on 39 Stump preserved; no 4mo POD 1, flap failure, prosthesis pedicled thoracoabdominal flap 5 None 15 No prosthesis Died 2 yr postoperatively secondary to lung metastasis 6 None 18 No prosthesis 12 yr 7 None 10 Satisfactory; body- 3 yr Ipsilateral latissimus powered above-elbow dorsi not available prosthesis 8 None 13 Good; mechanical 11 yr below-elbow prosthesis 9 Venous congestion 12 Good; mechanical 12 yr Ipsilateral latissimus (conservative treatment) above-elbow prosthesis dorsi not available 10 None 7 Excellent; preserved 5yr hand grip 11 Flap failure, covered with 48 Wears cosmetic 2yr pedicled groin flap prothesis but used hand only as adjunct; is changing job 12 None 25 Change of job; 1yr adjunctive hand, myoelectrical prothesis 13 POD 4 fibular dislocation, 20 Satisfactory; cosmetic 6yr reosteosynthesis with prosthesis external fixator, 5 mo postoperative sequestrectomy, delayed union I&D, irrigation and debridement; POD, postoperative day.

In four cases (31 percent), a free fillet flap was In both hand cases, the goal was to preserve used to preserve the stump. In the other nine the metacarpophalangeal joints and some length cases, a traditional free flap was harvested (five in the proximal phalanxes to maintain a functional latissimus dorsi, one lateral arm, one anterolateral pinch. In five cases (38 percent), the microsurgical thigh, one parascapular, and one free fibula). procedure was carried out to preserve the elbow

Fig. 1. Amputated limb of patient 2.

974 Volume 120, Number 4 • Free Vascularized Tissue Transfer joint; in one case (8 percent), the procedure aimed fibular flap was complicated by delayed union. to preserve additional length in the distal forearm; In addition, one patient died after 2 years be- in one case, the goal was to preserve the shoulder cause of advanced metastatic disease. Hospital joint (8 percent); and in four cases (31 percent), stays ranged from 7 to 48 days (mean, 20 days), the procedure was carried out to maintain skeletal and the postoperative follow-up ranged from 6 length in the proximal upper arm. Table 2 sum- months to 12 years (mean, 4.3 years). Table 3 marizes for each patient where the amputation summarizes complications, length of hospital would have been without the reconstructive pro- stay, and outcome. Three cases from three dif- cedure, the microsurgical procedure that was per- ferent centers are described below that deal with formed, and the relative indication (i.e., the struc- preservation of amputated stumps to the fore- tures to be salvaged). arm, to the hand, and to the arm, respectively. Five patients (38 percent) had postoperative complications. Three free flaps were lost, two of CASE REPORTS which were on the same patient: one flap had Patient 2 partial necrosis, one had vascular impairment A 48-year-old right-handed man presented with a right upper but was conservatively salvaged, and the free extremity complete crushing-avulsion amputation to the prox-

Fig. 2. A free fasciocutaneous fillet flap based on both radial and ulnar arteries was harvested from the amputated forearm and transferred to the residual stump in patient 2 (left, free fillet flap; right, flap inset into recipient site).

Fig. 3. Patient 2. Outcome with prosthesis.

975 Plastic and Reconstructive Surgery • September 15, 2007 imal third of the forearm, with a significant radial and ulnar on both radial and ulnar arteries was promptly harvested bony defect and extensive soft-tissue degloving to the proximal from the amputated forearm (Fig. 2, left) and transferred to stump. The forearm was not reimplantable (Fig. 1). On the the residual stump, preserving the elbow joint and 7 cm of patient’s presentation, a free fasciocutaneous fillet flap based skeletal length below the elbow (Fig. 2, right). The median

Fig.4. Patient10,whopresentedwithnecrosisofdigitsIIthroughV,underwentdebridementandcoverageofthebony stumps with a free lateral arm flap. The flap was then expanded and the digits were separated as shown. (Above, left) Placement of a tubular expander under lateral arm flap. (Above, right) Expansion of tubular expanders; (center) surgical separation of the digits, in two stages; (below) outcome.

976 Volume 120, Number 4 • Free Vascularized Tissue Transfer nerve from the flap was coapted to the proximal stump to fibula flap covered by a pedicled ipsilateral latissimus dorsi. restore sensation. Both the flaps were successful, but the fibula was dislocated on Postoperatively, the flap had partial necrosis, which was de- postoperative day 4, and stabilization was thus achieved with an brided and subsequently skin grafted. The flexion-extension of the external fixator (Fig. 5). The overall follow-up was character- elbow was maintained, and the patient was able to fit a below-elbow ized by delayed union and infection treated with additional mechanical prosthesis that restored a pinch function (Fig. 3). sequestrectomy and bone grafts. The patient was able to wear Good functional results were achieved at 1-year follow-up. a cosmetic prosthesis, and 70 degrees of abduction and 70 degrees of extension were preserved (Figs. 6 and 7). Patient 10 A 32-year-old right-handed man presented with a combined compression/thermal injury to the right hand. Digits II DISCUSSION through V were necrotized and unsalvageable distal to the Based on the analysis of this series and on the proximal interphalangeal joint. After soft-tissue debridement, microsurgical experience the authors have de- the first phalanx remained exposed in all digits. A free lateral arm flap was harvested and transplanted to the hand to cover veloped over the years in dealing with complex 15–18 all four bony stumps. The superficial radial artery was attached limb reconstructions, the authors propose a to the superficial palmar arch, on the ulnar side. The venous treatment algorithm for management of the am- anastomosis was carried out using a superficial dorsal vein. The putated upper extremity (Fig. 8). This algorithm flap healed uneventfully. allows the treating physician to take into ac- A tubular 2 ϫ 4.5-cm skin expander was then inserted under the flap and expanded (Fig. 4, above). Two additional surgical steps count the functional benefit that the patient allowed for separation of all the proximal phalanxes, providing would derive from preserving the amputation adequate soft-tissue coverage of the bony stumps circumferentially level, and compare that outcome with the pro- (Fig. 4, center). Long-term follow-up demonstrated a satisfactory result in providing pinch function (Fig. 4, below). Patient 13 A 14-year-old girl presented with a short-stump below-shoul- der amputation following a 43 percent total body surface area high-voltage burn. The short stump was lengthened with a free

Fig. 5. A short amputation stump was lengthened with a free fibula flap covered by a pedicled ipsilateral latissimus dorsi in patient13.Anexternalfixatorwasusedtostabilizethedislocated fibula. Reprinted with permission of Springer Science and Busi- Fig. 6. Patient 13. Functional results. Reprinted with permission ness Media. © Der Chirurg. Baumeister, S., Germann, G., Geissler, of Springer Science and Business Media. © Der Chirurg. Baumeis- G.,Dragu,A.,andSauerbier,M.Reconstructionofburnedextrem- ter, S., Germann, G., Geissler, G., Dragu, A., and Sauerbier, M. Re- ities by free flap transplantation (in German). Chirurg 75: 568, construction of burned extremities by free flap transplantation 2004. (in German). Chirurg 75: 568, 2004.

977 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 7. Patient 13. Outcome with prosthesis. Reprinted with permission of Springer Science and Business Media. © Der Chirurg. Baumeister, S., Ger- mann, G., Geissler, G., Dragu, A., and Sauerbier, M. Reconstruction of burned extremities by free flap transplantation (in German). Chirurg 75: 568, 2004.

spective of a prosthetic rehabilitation. The rel- Kuntscher et al.8 in 2001 proposed a classifi- ative indications for providing soft-tissue cover- cation system of fillet flaps based on a series of 104 age to the amputation stump by free tissue cases, which we consider to be of great relevance transfer are outlined in Table 4. though tangential to the purpose of the present Since its introduction in 1973,19 microsurgi- study. In our treatment algorithm, fillet flaps rep- cal free tissue transfer has been a valuable op- resent the first reconstructive choice to preserve tion in the surgical management of traumati- length of a critical joint or an amputated stump. cally injured upper limbs. However, free tissue Despite the fact that ischemia time is a much less transfer to an upper extremity amputation important aspect in free fillet fasciocutaneous stump is an uncommon procedure. The absence flaps than it is in major replantation surgery (as of larger series in the literature on this topic and the flap contains no muscle),11,13,14 in only 30 per- the fact that only 13 cases were collected from cent of the presently reported cases was the fillet our four microsurgery trauma centers in a 12- flap available for microsurgical transfer. In the year retrospective review suggests that this need remaining 70 percent, a traditional free tissue is rare. transfer was performed. In 1986, Russel and colleagues described mi- Although major advancements have been crovascular surgery in an emergency setting using made in the field of upper limb functional pros- undamaged spare parts for reconstruction of a thetics, the gap between what the amputee desires below-knee amputation.20 Several authors subse- and the replacement received remains more evi- quently reported elective microvascular free tissue dent than with prosthetic devices in other parts of transfer to amputation sites of the lower extremity the body. This discrepancy increases with higher using free flaps that were based predominantly on levels of amputation.27–30 Specifically, when an am- the subscapular vascular system.21,22 putation is required at the shoulder or forequarter Shenaq et al.23 reported three cases of second- level, prosthetic function is very difficult to re- ary reconstruction of upper extremity amputation store. This is attributable to a combination of the sites with microvascular free tissue transfer in weight of the prosthetic components and the in- 1987, and the concept of immediate spare part use creased energy expenditure necessary to operate for preservation of length of the upper extremity the prosthesis. For this reason, most individuals after amputation was emphasized by Weimberg et with this level of amputation choose a cosmetic al. in 1997.24 Before this, Hammond described prosthesis that serves only to improve body image three cases in which free fillet flaps were used for and the fit of clothing. reconstruction of the upper extremity.25 Other Above-elbow or below-elbow amputees may be case reports and very small series (two or three fitted with either body-powered or myoelectric patients) were reported in the literature over the prostheses that provide satisfactory functional subsequent years.11,26 results.31 With the myoelectric device, a below-

978 Volume 120, Number 4 • Free Vascularized Tissue Transfer

Fig. 8. Treatment algorithm for management of the amputated upper extremity. Therapeutic actions are in bold; questions that determine the path along the decision tree are in plain text. elbow amputee can initiate palmar tip grasp or nation function to the forearm. We do not con- other types of grip by contracting residual forearm sider this to be a major indication to perform a flexors and can release by contracting residual free tissue transfer to the amputated site. extensors. The complication rate in the presented se- The advantage of preserving the wrist joint is ries was found to be fairly high. However, in all attributable to the preservation of the pronosupi- cases but two, the free tissue transfer survived,

979 Plastic and Reconstructive Surgery • September 15, 2007

Table 4. Indications for Free Tissue Transfer to REFERENCES Provide Soft-Tissue Coverage of Amputation Stump 1. Cordeiro, P. G., Cohen, S., Burt, M., and Brennan, M. F. The Major indications total volar forearm musculocutaneous free flap for recon- Shoulder joint preservation (forequarter amputation or struction of extended forequarter amputations. Ann. Plast. shoulder disarticulation is converted to a transhumeral Surg. 40: 388, 1998. amputation) 2. Tran, N. V., Evans, G. R. D., Kroll, S. S., et al. Free fillet Elbow joint preservation (transhumeral amputation or extremity flap: Indications and options for reconstruction. elbow disarticulation is converted to a transradial Plast. Reconstr. Surg. 105: 99, 2000. amputation) 3. Foster, R. J., Barry, R. J., Holloway, A., and Burney, D. W., III. Preservation of pinch function to the hand (wrist A 50-cm fillet flap for preservation of maximal lower extrem- disarticulation or transcarpal amputation is converted ity residual limb length. Clin. Orthop. 178: 216, 1983. to a phalanx amputation) 4. Frieden, R. A. Amputation after tibial fracture: Preservation Skeletal preservation Ͼ7 cm below shoulder/below of length by use of a neurovascular island (fillet) flap of the elbow (significantly improves prosthetic fit and foot. J. Bone Joint Surg. (Am.) 71: 1109, 1989. functional performance) 5. Gainor, B. J. Osteocutaneous digital fillet flap: A technical Minor indications modification. J. Hand Surg. (Br.) 10: 79, 1985. Wrist joint preservation (transradial amputation or wrist 6. Hallock, G. G. Isle of palm and sole fillet flaps. Ann. Plast. disarticulation is converted to a transcarpal Surg. 26: 514, 1991. amputation, and prosupination is maintained) 7. Katsaros, J., and Proudman, T. W. The very long posterior Skeletal preservation between 5 and 7 cm below tibial artery island flap. Br. J. Plast. Surg. 44: 599, 1991. shoulder/below elbow (5 cm is the minimal length 8. Kuntscher, M. V., Erdmann, D., Homann, H. H., Steinau, required for a prosthesis to fit) H. U., Levin, S. L., and Germann, G. The concept of fillet flaps: Classification, indications, and analysis of their clinical value. Plast. Reconstr. Surg. 15: 885, 2001. 9. Sanders, W. E. Amputation after tibial fracture: Preservation and in all cases the amputation level was eventually of length by use of a neurovascular island (fillet) flap of the preserved. foot. J. Bone Joint Surg. (Am.) 71: 435, 1989. 32 10. Steinau, H. U., Germann, G., Buttemeyer, R., Hussmann, J., Finally, as other authors have stated previously, and Hebebrand, D. Reconstructive surgery of knee para- we consider nerve repair to be a straightforward articular amputation stumps. Unfallchirurgie 19: 272, 1993. maneuver that takes minutes and adds the potential 11. Cavadas, P. C. The free forearm fillet flap in traumatic arm benefits of a better fit of the prosthesis and a reduced amputation. Plast. Reconstr. Surg. 98: 1119, 1996. likelihood of pressure ulcers. It should therefore be 12. Chiang, Y. C., Wei, F. C., Wang, J. W., and Chen, W. S. Reconstruction of below-knee stump using the salvaged foot performed when possible. fillet flap. Plast. Reconstr. Surg. 96: 731, 1995. 13. Cavadas, P. C., and Raimondi, P. Free-fillet flap of the hand for elbow preservation in non replantable forearm amputa- CONCLUSIONS tion. J. Reconstr. Microsurg. 20: 363, 2004. Upper extremity amputations are not as 14. Erdmann, D., Sudin, B. M., Yasui, K., Wong, M. S., and Levin, L. S. Microsurgical free flap transfer to amputation sites: common as lower extremity amputations; how- Indications and results. Ann. Plast. Surg. 48: 167, 2002. ever, they present unique challenges to the sur- 15. Levin, L. S., Goldner, R. D., Urbaniak, J. R., Nunley, J. A., and geon, prosthetist, and amputee. Appropriate Hardaker, W. T. Management of severe musculoskeletal in- surgical management of the residual limb rep- juries of the upper extremity. J. Orthop. Trauma 4: 432, 1990. resents the key factor in providing the patient 16. Levin, L. S., Erdmann, D., and Germann, G. The use of fillet flaps in upper extremity reconstruction. J. Am. Soc. Surg. with the most functional outcome possible. Mi- Hand 2: 39, 2002. crosurgical free tissue transfer to preserve am- 17. Levin, L. S., and Erdmann, D. Primary and secondary mi- putation level is a valid option in well-selected crovascular reconstruction of the upper extremity. Hand cases. Clin. 17: 447, 2001. 18. Levin, L. S. Orthoplastic reconstruction of the arms and legs. Detlev Erdmann, M.D., Ph.D. In M. Siemionow (Ed.), Tissue Surgery. New York: Springer, Division of Plastic, Reconstructive, Maxillofacial, and 2006. Oral Surgery 19. Daniel, R. K., and Taylor, G. I. Distant transfer of an island Duke University Medical Center, Box 3181 flap by microvascular anastomoses: A clinical technique. Durham, N.C. 27710 Plast. Reconstr. Surg. 52: 111, 1973. [email protected] 20. Russel, R. C., Vitale, V., and Zook, E. C. Extremity recon- struction using the “fillet of sole flap.” Ann. Plast. Surg. 17: 65, 1986. DISCLOSURES 21. Frykman, G. C., and Jobe, C. M. Amputation salvage with No specific devices, drugs, or other commercial prod- microvascular free flap from the amputated extremity. J. Trauma 27: 326, 1987. ucts are mentioned in this article, and none of the au- 22. Germann, G., Bickert, B., Steinau, H. U., et al. Versatility and thors has any relevant financial ties or conflicts of interest reliability of combined flaps of the subscapular system. Plast. related to this article. Reconstr. Surg. 103: 1386, 1999.

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23. Shenaq, S. M., Krouskop, T., and Stal, S. Salvage of amputation 28. Weir, R. F. Tunnel cineplasty as a control input for externally- stumps by secondary reconstruction utilizing microsurgical powered prosthetic components. Med. Orthop. Tech. 121: 9, free-tissue transfer. Plast. Reconstr. Surg. 79: 861, 1987. 2001. 24. Weimberg, M. J., Al-Qattan, M. M., and Mahoney, J. “Spare 29. Spires, M. C., and Miner, L. Upper extremity amputation and part” forearm free flaps harvested from the amputated limb prosthetic rehabilitation. In M. Grabois (Ed.), Physical Med- for coverage of amputation stumps. J. Hand Surg. (Br.) 22: icine and Rehabilitation: The Complete Approach. Malden, Mass.: 615, 1997. Blackwell Science, 2000. Pp. 549–582. 25. Hammond, D. C., Matloub, H. S., Kadz, B. B., Yousif, N. J., 30. Glennon, T. P., and Smith, B. S. Amputations. In S. J. Gar- Sanger, J. R., and Larson, D. L. The free-fillet flap for re- rison (Ed.), Handbook of Physical Medicine and Rehabilitation construction of the upper extremity. Plast. Reconstr. Surg. 94: Basics. Philadelphia: Lippincott, 1995. Pp. 34–60. 507, 1994. 31. Leonard, J. A., and Meier, R. H. Upper and lower extremity 26. Richards, A., Klaasen, M., and Parkhouse, N. The free-fillet prosthetics. In J. A. De Lisa (Ed.), Rehabilitation Medicine: flap for reconstruction of the upper extremity. Plast. Reconstr. Principles and Practice. Philadelphia: Lippincott-Raven, 1998. Surg. 96: 488, 1995. Pp. 669–696. 27. Baumgartner, R. Upper extremity amputation and prosthet- 32. Cavadas, P. C. The free forearm fillet flap in traumatic arm ics. Med. Orthop. Tech. 1: 5, 1992. amputation. Plast. Reconstr. Surg. 98: 1119, 1996.

Online CME Collections This partial list of titles in the developing archive of CME article collections is available online at www. PRSJournal.com. These articles are suitable to use as study guides for board certification and/or recertification, to help readers refamiliarize themselves on a particular topic, or to serve as useful reference articles. Articles less than 3 years old can be taken for CME credit. Hand/Peripheral Nerve Effective Surgical Treatment of Cubital Tunnel Syndrome Based on Provocative Clinical Testing without Electrodiagnostics—Daniel P. Greenwald et al. The Neuromuscular Compartments of the Flexor Carpi Ulnaris—Aymeric Y. T. Lim et al. Restoration of Elbow Flexion after Brachial Plexus Injury: The Role of Nerve and Muscle Transfers—Karol A. Gutowski and Harry H. Orenstein Extensor Tendon: Anatomy, Injury, and Reconstruction—W. Bradford Rockwell et al. Upper Extremity Microsurgery—William C. Pederson Secondary Carpal Tunnel Surgery—Thomas H. H. Tung and Susan E. Mackinnon Current Approach to Radial Nerve Paralysis—James B. Lowe, III et al. Alternatives to Thumb Replantation—Christoph Heitmann and L. Scott Levin Management of Secondary Cubital Tunnel Syndrome—James B. Lowe, III, and Susan E. Mackinnon Mycobacterium marinum Infections of the Upper Extremity—Christopher L. Hess et al. Posttraumatic Thumb Reconstruction—Arshad R. Muzaffar et al. Thumb Trapeziometacarpal Arthritis: Treatment with Ligament Reconstruction Tendon Interposition Arthroplasty—Ashkan Ghavami and Scott N. Oishi

981 HAND/PERIPHERAL NERVE

Changes in the Lymph Structure of the Upper Limb after Axillary Dissection: Radiographic and Anatomical Study in a Human Cadaver

Hiroo Suami, M.D., Ph.D. Background: There have been very few anatomical reports on the changing Wei-Ren Pan, M.D. lymph structure of the upper limb after axillary dissection despite its clinical G. Ian Taylor, M.D. significance for predicting skin cancer recurrence in the limb and secondary Melbourne, Victoria, Australia lymphedema. The authors used both upper limbs harvested from a fresh human cadaver that had undergone unilateral right radical mastectomy and radical axillary dissection for breast cancer. Methods: Hydrogen peroxide was used to identify and inflate the lymphatic vessels. Individual channels were injected with a radiopaque lead oxide mixture and recorded on x-ray film. Results: Results from the normal left upper limb were similar to results from the authors’ previous studies. However, the right limb from the mastectomy side showed remarkable differences and revealed that the lymph node clearance in the axilla had been incomplete on that side. The major difference was the almost complete absence of the superficial lymphatic network in the right arm, prox- imal to the elbow, because of fibrosis and blockage of the lymphatic channels. A circuitous pathway was identified that bypassed the blocked lymphatics in the arm to reach the deep system. This was facilitated often by backflow through precollectors and avalvular lymph capillaries in the dermis of the forearm, to reach eventually the few remaining lymph nodes in the axilla. Conclusions: Previously undetected lymph channels connecting the superficial and the deep lymphatic system had opened up because of the blockage of superficial lymphatic vessels caused by axillary dissection. It is presumed that these channels prevented lymphedema in this case. (Plast. Reconstr. Surg. 120: 982, 2007.)

ince Halsted1 reported chronic edema of it is difficult to predict before surgery which the upper limb after mastectomy for breast patients will be afflicted. Lymphangiographic Scancer, lymphedema has become a well- studies2–15 of patients after axillary dissection de- known postoperative side effect. The treatment scribe changes in lymphatic pathways of the up- for acquired lymphedema of the upper limb per limb. However, lymphangiography requires after axillary dissection is a challenging problem the patient to remain in the same position for for plastic surgeons. The cause of lymphedema is lengthy periods during the examination of just not fully understood and therefore at this time one vessel. It also uses an oil contrast medium, there is still no recognized cure. Although it is which can cause blockages and inflammation of agreed that secondary lymphedema is caused by the lymph channels, and the symptoms may be- 16 the inability of the lymphatic network to cope come worse. with the drainage of extracellular tissue fluid Lymphoscintigraphy is now used more com- following ablation of the regional lymph nodes, monly for examination of the lymphatic system than lymphangiography. Lymphoscintigraphy is From the Jack Brockhoff Reconstructive Plastic Surgery Re- useful for quantitative diagnosis of lymphedema search Unit, Royal Melbourne Hospital, Department of Anat- by checking the clearance time of injected radio- omy and Cell Biology, University of Melbourne. active substances.17 However, it is not suitable for Received for publication May 17, 2006; accepted August 10, accurately mapping the exact course of every 2006. lymph vessel. Early anatomical studies were un- Copyright ©2007 by the American Society of Plastic Surgeons dertaken using dye or mercury, and the results DOI: 10.1097/01.prs.0000277995.25009.3e were usually only drawings.18–20 Gerota’s method

982 www.PRSJournal.com Volume 120, Number 4 • Lymph Structure of the Upper Limb in 189621 using blue oil painting color is still a tected. The study commenced at the fingertips. A common method of finding lymphatic vessels. mixture of blue drawing ink and hydrogen per- However, it is not suitable for identifying and oxide was injected into the dermis of the fingertips mapping the course of the collecting vessels. (Fig. 1). The epidermis and superficial part of the There have been very few anatomical reports dermis were carefully removed. Precollectors sit- on the changing lymph structure of the upper uated in the dermal layer and lymph collecting limb after axillary dissection. There have been vessels situated in the subcutaneous tissue were no reports comparing both upper limbs of a identified using blue ink and the oxygen bubbles cadaver after unilateral mastectomy. Our new absorbed into the lymph channels from the hy- radiographic cadaver injection technique for in- drogen peroxide. We used special finely stretched vestigating the lymphatic system22–24 has been glass needles for cannulating the lymphatic vessels applied to this study to examine the changes in smaller than 0.3 mm and 30-gauge needles for the the lymph structure after axillary dissection in larger vessels.23 one limb and to compare these results with those The injection mixture consisted of 3 g of or- obtained from the opposite, normal limb (Figs. 1 ange lead oxide, 0.5 g of powdered milk, and 20 through 8). ml of hot water (40°C). The lead oxide and milk powder were ground well using an agate mortar MATERIALS AND METHODS and pestle before adding hot water. A microma- The cadaver was an 81-year-old woman who nipulator was used for the cannulation. The in- had undergone a total right mastectomy with ax- jection was begun gently by hand with a 1-ml illary node clearance 11 years previously. All nodes syringe commencing in the index fingertip. Re- were clear of cancerous cells. She did not receive sistance in the syringe or leakage from the vessel radiation treatment and she did not have any signs at the injection point indicated the end of the of lymphedema or cancer recurrence after the injection. At this point, an unusual phenomenon operation. Her death was caused by chronic heart occurred that is explained later. A blush of orange failure. We used both upper limbs, including the lead oxide was seen in the skin on the front of the armpits, as forequarter specimens. forearm during injection into the finger (Fig. 6). The lymph investigation was commenced in The procedure was repeated for all the lymphatic the abnormal right upper limb, and the normal vessels as they were identified in the hand and left limb was preserved in a deep freezer. Applying traced proximally up the forearm and arm. It is to our method,22–24 all of the lymph collecting vessels be noted that the injectant sometimes stopped at (approximately 0.3 mm in diameter) were de- an interval lymph node. When this occurred, hy- drogen peroxide was injected directly into the lymph node so that the efferent lymph vessel could be identified and the injection continued. Injections were repeated until the injectant reached the subclavian vein. Subsequently, ra- diolucent venous injections using a mixture of blue color ink and gelatin were performed to compare the course of the veins with those of the lymphatic vessels. The limb was radiographed and then an axial lateral incision line parallel with and close to the cephalic vein that avoided cutting the lymph ves- sels was made and the bones were removed. The specimen, including skin, deep fascia, and mus- cles, was spread on a board and radiographed (65 kV; 0.03 S; distance, 150 cm) (Figs. 2 and 3). A Fig. 1. Precollectors in the dermis (PC) and lymph collecting ves- meticulous dissection was undertaken to obtain an sels (LC) in the subcutaneous tissue of the fingertip were identi- accurate three-dimensional structure of the lym- fied using a mixture of blue ink and hydrogen peroxide. The phatics and their relationship to the veins and the lymph collecting vessels were injected with a radiopaque lead deep fascia. This involved a tedious, painstaking oxide mixture (orange). The arrow points to a valve that normally removal of epidermis, dermis, and fat globules prevents backflow from the lymph collecting vessels. from around and between the precollecting and

983 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 2. Radiographs of the skin and soft tissues of the normal left upper limb (right) and abnormal right upper limb (left), including the deep fascia and mus- cles,forcomparison.Theintegumenthasbeensplitalongthelateralborderofthe limb and unwrapped. Note that the number of lymph vessels was less in the abnormal right arm, especially above the elbow, and that there are still some lymph nodes in the axilla on this side following clearance (arrows). collecting lymph channels. This method was re- vessels reached the web space, they changed their peated on the left arm (Fig. 4). course toward the dorsal side of the hand. There- The radiographic images were scanned, the after, they repeatedly converged and diverged to lymphatic vessels traced, and the channels color interconnect, gradually changing their course to- coded in relation to the deep fascia (Fig. 3). Fi- ward the medial side of the upper arm above the nally, the lymphatic channels from the normal left level of the elbow joint. The diameter of the vessels upper limb were traced retrogradely from each remained uniform. We found the superficial lym- regional lymph node and color coded to deter- phatic system to consist of a wavy network that mine their territories (Fig. 5). Each upper limb often paralleled the cephalic and basilic veins, and required 5 weeks for injections and dissections to the most superficial lymph vessels flowed into the be completed. regional lymph nodes in the armpit (Figs. 2 and 3, right). However, the lymph vessels that arose from RESULTS the middle and ring fingers in the third web space coursed beside the cephalic vein on the lateral side Normal Left Upper Limb of the forearm and arm. They did not head toward The lymphatics of the digits were found to the medial side of the arm, as seen in previous begin as a horizontal network of precollectors in studies,24 but converged below the elbow to pass as the dermis and subdermal region. Valves were a single vessel through three interval lymph nodes found at the junction between precollectors and in the proximal arm (Figs. 3, right and 5). This the lymph collecting vessels that prevented back- vessel then bypassed the axillary lymph nodes and flow (Fig. 1). One to three lymph collecting vessels went straight to the subclavian vein. were found running beside the neurovascular No connections were found between the su- bundle on each side of the finger.23,24 Once the perficial and deep lymphatics in the hand and

984 Volume 120, Number 4 • Lymph Structure of the Upper Limb forearm when the former vessels were injected. The significant difference between the super- The connections between the superficial and the ficial and deep lymph vessels was that the former deep lymphatic system were found only above the vessels went straight to the regional lymph nodes elbow along the basilic vein. Lymph vessels that in the axilla, whereas the latter first passed through arose from the remaining sides of the middle, ring, several interval lymph nodes before reaching the and little fingers ran posteriorly along the side of the armpit. Thereafter, lymph vessels passed through forearm. When they passed above the elbow joint, several lymph nodes before merging into one vessel they took a short turn toward the basilic vein and to reach the subclavian vein (Fig. 5). pierced the deep fascia to form a single channel. This deep lymph vessel followed the basilic vein beneath the deep fascia. It passed through two Abnormal Right Upper Limb interval lymph nodes before reaching the regional Initially, the pattern of the lymph collecting lymph nodes in the axilla. vessels in the distal third of the finger was similar We found a second deep lymph vessel running to the pattern in the left hand. Thereafter, their under the deep fascia in the forearm. The vessel pathways were interrupted and diverted at fre- was found near the wrist joint, but its origin was quent intervals because of segments of blocked unknown. It coursed beside the radial artery and lymph channels, subsequently found to be caused passed through several interval lymph nodes be- by fibrosis, narrowing, and blockage of these chan- fore reaching a lymph node in the axilla (Fig. 3). nels (Figs. 2 through 4, 6, and 7). In this specimen, we could not find lymph vessels In the index and middle fingers, because of around the ulnar artery. obstruction, the lymph collecting vessels that ran

Fig. 3. Tracing of lymphatics of the abnormal right limb (left) and the normal left limb (right) with regardtothedepthofeachvessel.Theleadoxidebackflowfromthecollectinglymphaticchannels to the precollectors (orange) can only be seen in the abnormal right upper limb. Note in the abnormal limb that the lymphatic flow has been diverted into the deep system above the elbow, that interval nodes are prominent in this region, and that some nodes still exist in the axilla.

985 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 4. Comparison of the dorsal side of both hands after the lead oxide injection. The left hand (right) revealed a normal appearance of lymph vessels (orange). On the right hand (left), however, not many lymph vessels could be found. Note the unusual vessel (arrows) travers- ing the hand.

along their contiguous sides did not drain through the second web space to the dorsum of the hand. Instead, their pathways were diverted across the back of each finger to their opposite sides by backflow through precollectors in the dermis (Figs. 2 and 3, left). From the ulnar side of the index finger, the lymphatic pathway was again diverted through a channel that passed through the second web space to emerge in the palm and course with the palmar metacarpal artery. When the vessel reached the thenar em- inence, it was again diverted by reverse flow through a network of precollectors in the dermis and subdermis before reaching collecting ves- sels at the wrist. On the dorsum of the hand, few vessels could be found, unlike the left limb. However, a peculiar vessel was seen to connect the lymph vessels trans- versely (Fig. 4, left). An orange stain in the skin in the forearm region, noted previously (see above), was found to be caused by lead oxide backflow into precollectors in the dermis. The radiograph showed clearly the precollector network that con- nected adjacent lymph collecting vessels (Fig. 6). Fig. 5. Tracing of lymphatics distally from each regional lymph On the dorsal side of the forearm, a connec- node, color coded to define their territories in the normal left tion between the superficial and the deep lym- upper limb (compare with Fig. 3, right). The color chart shows the phatics was observed. At first, the vessel ran axially hierarchy of lymph vessels draining the third web space. Note but changed its path and coursed deep. It pene- that the orange vessel bypasses the axillary lymph nodes and trated the deep fascia and ran along the posterior that one sentry node (gray) drains the largest area. interosseous artery and then reached a small in-

986 Volume 120, Number 4 • Lymph Structure of the Upper Limb

Fig. 7. The results of histologic studies for comparing normal lymph vessels harvested from the normal left arm (above) and atrophic lymph vessels harvested from the abnormal right arm (below). The image below shows that the vessel wall is much thicker than that in the image above.

showed the differences between a normal vessel from the left arm and a vessel harvested from the right arm. The vessels from the mastectomy side were encased with a thick fibrous layer (Fig. 7). This observation suggested a chronic inflamma- tory reaction around the vessel. Deep lymphatic vessels were found beside the radial and ulnar arteries at the wrist. The vessel Fig. 6. (Above) An orange stain caused by lead oxide backflow that ran along the ulnar artery coursed superfi- intothedermiswasobservedintherightforearmregion.(Center) cially and became a superficial lymph vessel. The Higher magnification shows precollectors filled with lead oxide course of the deep vessel beside the radial artery inthedermis.(Below)Aradiographofthesameareashowingthat was similar to the lymphatic pathway demon- the precollectors (PC) connected lymph collecting vessels (LC). strated in the left arm. Above the elbow joint, the vessel ran beneath the deep fascia with the basilic vein and passed through several interval lymph terval lymph node near the humeroulnar joint nodes before it reached the axilla (Figs. 2, left and (Figs. 2, left and 3, left). 3, left). Clearly, the interval lymph nodes in the In the upper arm, superficial lymph vessels right arm from the mastectomy side were far larger could not be found. Histologic examination than those from the normal left arm (Fig. 8).

987 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 9. The lymphatic territories of each sentinel lymph node in the normal left limb, colored to match Figure 5. One lymph node (gray)almostcoverstheentireanteriorregion.However,thepos- terior side is divided into several lymph territories.

Fig.8. Imagesdepictingtheepitrochlearlymphnodesintheleft The color-coded tracing of the lymphatic ves- arm (above) and in the right arm (below). It is clear that the lymph sels of the arm is summarized in Figures 5 and 9. nodes from the abnormal right arm (below) are much larger. The All the lymph vessels that ran along the anterior arrow indicates the direction of lymphatic flow. surface of the limb passed into one main (sentry) lymph node (gray). However, lymph vessels that ran along the posterior surface revealed more va- Histologic examination revealed no evidence of riety. Some lymph vessels that ran in the midpos- cancerous cell metastasis to account for the large terior surface drained into a small regional lymph size of the interval nodes in the right arm. node in the axilla, and lymph vessels that ran beside the cephalic vein bypassed the regional DISCUSSION lymph nodes in the axilla. Although one case study is presented, we were able to compare the lymphatic pathway in the limb Lymphatics in the Abnormal Right Arm on the side of the axillary clearance, which did not Several types of unusual lymph pathways develop lymphedema, with the opposite, normal that we had never seen before were identified extremity. This study has revealed much informa- in this study. We have summarized our findings tion that may lead to a better understanding of the as schematic diagrams in Figures 10 and 11. pathogenesis of lymphedema and the spread of These show the sites where these lymphatic secondary cancer deposits. pathway changes were observed. Type A represents backflow to precollectors Lymphatics in the Normal Left Arm and the avalvular lymphatic capillaries in the der- We have investigated 23 upper limb lymphatic mis. It is caused by incompetent valves situated studies and published the results from 14 of these between precollectors and lymph collecting ves- studies.24 The results of this left arm from the sels similar to that seen in the pathogenesis of normal side showed no significant differences varicose veins in the skin. There have been many from our previous results. reports describing this observation under some

988 Volume 120, Number 4 • Lymph Structure of the Upper Limb

Fig. 10. Schematic diagrams showing lymphatic pathway changes after a blockage of the lymph collecting vessel. Type A, backflow to precollectors in the dermis; Type B, connection between the superficial lymph collecting vessel; Type C, connection between the superficial and deep lymph collecting vessel; Type D, becoming atrophic; Type E, formation of lymphovenous shunt.

pathologic conditions.2,7–12,25 In particular, it is ap- the lower limb. Malek et al.26 observed these com- parent in studies of lymphedematous limbs. This munications using lymphangiography in the lower seems also to be relevant to in-transit recurrence leg of a patient with lymphedema. of skin malignancies, which often deposit in the Type D illustrates what happens when lymph dermis. vessels become atrophic and disappear in the Types B and C describe the opening of a chan- proximal upper arm. It is these atrophic vessels nel between lymph collecting vessels. Type B is a that we used for histologic examination (Fig. 7). connection between the superficial vessels and The histologic results show chronic inflamma- type C is a connection between the superficial and tion around lymph vessels, and this is consid- deep vessel. Crockett25 reported a collateral route ered to be one of the reasons for lymph vessel of drainage from an obstructed superficial trunk blockage. The literature reports3,5,7 absence or into an unobstructed deep system using ampu- obstruction of distinct lymphatic channels at tated limbs in the case of a Marjolin carcinoma of different levels after axillary dissection. Espe-

989 Plastic and Reconstructive Surgery • September 15, 2007

terval lymph node swelling: (1) inflammatory re- action to the superficial lymph vessels, which were blocked by the axillary dissection; and (2) work hypertrophy in compensation for ablated lymph nodes in the axillary region. That the right arm was not lymphedematous appears to be attributable to (1) patency of the deep lymphatic system together with some resid- ual axillary lymph nodes that had not been re- moved at the original gland dissection; (2) un- usual communication between the superficial and deep lymphatic system; and (3) cross-connections between superficial collecting lymph channels fa- cilitated by reverse flow through precollectors, whose valves have become incompetent, and lym- phatic capillaries in the dermis, which have no valves.28 Goffrini et al.,4 using lymphangiography, studied the cases of 63 radical mastectomy patients that lacked swelling of the arm. They demon- strated the regeneration of an axillary lymphatic network anastomosing the severed arm lymph channels as a fourth pathway. We described also an intact deep lymphatic pathway from the up- per limb to the subclavian vein in the abnormal Fig. 11. Radiograph showing the sites in the abnormal right arm. However, our results do not confirm that arm where types A, B, C, and D were observed as illustrated in the pathway regenerated but rather that it was Figure 10. preserved. In recent years, the sentinel lymph node bi- opsy technique offers less morbidity to breast can- cially in the case of a patient suffering from cer and melanoma patients. However, we have lymphedema, very few lymph vessels were found little knowledge of lymphatic structure changes at the wrist. Altorfer et al. reported in their after surgical treatment. We need more studies to experimental study of dogs that the vessel walls confirm our findings of lymph network changes in of precollectors and lymph collecting vessels the postoperative cadaver following axillary dis- were thickened and sclerosed.27 section and especially to obtain further compar- Type E describes the formation of a lym- ative studies of the upper limb with and without phovenous shunt in the peripheral region. In our lymphedema. study, this type of communication was not found. However, Aboul-Enein et al. proved the CONCLUSIONS existence of a lymphovenous shunt in a case of We had a rare opportunity to investigate the a nonedematous postmastectomy arm.15 They lymphatic system of both upper limbs harvested used lymphangiography. Several articles suggest from a cadaver after unilateral mastectomy and the possibility that lymphovenous shunts form axillary gland clearance. In the normal left arm, in some pathologic conditions, such as postop- there was no communication seen between the eratively, in congenital lymphedema, and in superficial and deep lymphatics except in the ep- cancer.6,13 itrochlear region. However, the lymphatic path- There have been no reports about the differ- ways of the right arm on the mastectomy side ences in the size of interval lymph nodes. Lymph- showed significant differences: obliteration of su- adenopathy is caused mostly by cancer metastasis perficial lymph vessels, dermal backflow, unusual or immunologic reaction against inflammation. In communication between the superficial and deep this case, the patient had been free from cancer lymphatics, and interval lymph node enlarge- for 11 years; therefore, breast cancer metastasis to ment. These changes seem to facilitate lymph the lymph nodes is unlikely. Histologic examina- drainage after sporadic blockage of the lymph tion also showed no sign of cancerous cells in tract, especially proximal in the limb. We hope this those nodes. We propose two reasons for the in- study provides further information about the

990 Volume 120, Number 4 • Lymph Structure of the Upper Limb cause of lymphedema and recurrence of malig- 9. Feldman, M. G., Kohan, P., Edelman, S., and Jacobson, J. H. nant skin tumors after primary surgery. Lymphangiographic studies in obstructive lymphedema of the upper extremity. Surgery 59: 935, 1966. Hiroo Suami, M.D., Ph.D. 10. Hughes, J. H., and Patel, A. R. Swelling of the arm following The Jack Brockhoff Reconstructive Plastic Surgery radical mastectomy. Br. J. Surg. 53: 4, 1966. Research Unit, E533 11. Thompson, N. The surgical treatment of chronic lymphoe- Medical Building dema of the extremities. Surg. Clin. North Am. 47: 445, 1967. Department of Anatomy and Cell Biology 12. Thompson, N. The surgical treatment of advanced post mas- University of Melbourne tectomy lymphoedema of the upper limb. Scand. J. Plast. Grattan Street Reconstr. Surg. 3: 54, 1969. Parkville 3050, Victoria, Australia 13. Edwards, J. M., and Kinmonth, J. B. Lymphovenous shunts in [email protected] man. B.M.J. 4: 579, 1969. 14. O’Brien, B. M., Sykes, P. J., Trelfall, G. N., and Browning, F. S. C. Microlymphaticovenous anastomoses for obstructive ACKNOWLEDGMENTS lymphoedema. Plast. Reconstr. Surg. 60: 197, 1977. The authors are indebted to the Jack Brockhoff Foun- 15. Aboul-Enein, A., Eshmawy, I., Arafa, S., and Abboud, A. The role of lymphovenous communication in the development of dation, the Colonial Foundation, and the National post mastectomy lymphedema. Surgery 95: 562, 1984. Health and Medical Research Council for funding this 16. Casley-Smith, J. R., Foldi, M., Ryan, T. J., et al. Lymphoe- research, and the Royal Melbourne Hospital and the dema: Summary of the 10th International Congress of Lym- Department of Anatomy and Cell Biology at the Univer- phology. Working group discussions and recommendations. sity of Melbourne for their continuous support. The au- Lymphology 18: 175, 1985. 17. Weissleder, H., and Weissleder, R. Lymphedema: Evaluation thors thank Prue Dodwell for her administrative coordi- of qualitative and quantitative lymphoscintigraphy in 238 nation of this project. patients. Radiology 167: 729, 1988. 18. Cruikshank, W. C. The Anatomy of Absorbing Vessels of the Hu- man Body. London: G. Nicol, 1786. DISCLOSURE 19. Mascagni, P. Vasorumlymphaticorum Corporis Humani Historia et None of the authors has a financial interest in any Ischonographia. Sienna: Pazzini Carli, 1787. of the products, devices, or drugs mentioned in this 20. Sappey, P. C. Anatomie, Physiologie, Pathologie des vaisseaux lymphatiques. Paris: Adrien Delahaye, 1874. article. 21. Gerota, D. Zur Technik der Lymphogeffassinjection: Eine neue Injectionsmasse fur Lymphgefasse. Polychrom Injec- REFERENCES tion. Anat. Anzeiger 12: 216, 1896. 1. Halsted, W. S. The swelling of the arm after operations for 22. Suami, H., Taylor, G. I., and Wei-Ren, P. A new radiographic cancer of the breast: Elephantiasis chirurgica. Its cause and cadaver injection technique for investigating the lymphatic prevention. Bull. Johns Hopkins Hosp. 32: 309, 1921. system. Plast. Reconstr. Surg. 115: 2007, 2005. 2. Wallace, S., Jackson, L., Schaffer, B., et al. Lymphangiograms: 23. Suami, H., Taylor, G. I., O’Neill, J. K., and Wei-Ren, P. Re- Their diagnostic and therapeutic potential. Radiology 76: 179, finements of the radiographic cadaver injection technique 1961. for investigating minute lymphatic vessels. Plast. Reconstr. 3. Bower, R., Danese, C., Debbas, J., and Howard, J. M. Ad- Surg. 120: 61, 2007. vances in diagnosis of diseases of the lymphatics. J.A.M.A. 24. Suami, H., Taylor, G. I., and Pan, W. R. The lymphatic ter- 181: 687, 1962. ritories of the upper limb: Anatomical study and clinical 4. Goffrini, P., Bobbio, P., Peracchia, G., and Pellegrino, F. implications. Plast. Reconstr. Surg. 119: 1813, 2007. Modalita di ripristino della circolazione limfactica dell’arto 25. Crockett, D. J. Lymphatic anatomy and lymphoedema. Br. J. superiore e dell’ascella dopo l’intervento di madtectomia Plast. Surg. 18: 12, 1965. redicale. Ateneo Parmense 33: 60, 1962. 26. Malek, P., Belan, A., and Kocandrle, V. L. The superficial and 5. Smith, C. A. Studies on lymphedema of the extremities. Ann. deep lymphatic system of the lower extremities and their Surg. 156: 1010, 1962. mutual relationship under physiological and pathological 6. Wallace, S., Jackson, L., Dodd, G. D., and Greening, R. R. conditions. J. Cardiovasc. Surg. 5: 686, 1964. Lymphatic dynamics in certain abnormal states. A. J. R. Am. J. 27. Altorfer, J., Hedinger, C., and Clodius, L. Light and electron Roentgenol. 91: 1187, 1964. microscopic investigation of extremities of dogs with exper- 7. Danese, C., and Howard, J. M. Post mastectomy lymphedema. imental chronic lymphostasis. Folia Angiol. 25: 141, 1977. Surg. Gynecol. Obstet. 120: 797, 1965. 28. Leak, L. V. Lymphatic vessels. In J. V. Johannessen (Ed.), 8. El-Kharadly, M. E. A., and Enein, A. A. Post-mastectomy Cardiovascular System, Lymphoreticular and Hematopoietic System. swelling of the arm. Br. J. Cancer 19: 30, 1965. New York: McGraw-Hill, 1980. Pp. 159–183.

991 PEDIATRIC/CRANIOFACIAL

True Lambdoid Craniosynostosis: Long-Term Results of Surgical and Conservative Therapy

James M. Smartt, Jr., M.D. Background: True lambdoid synostosis is a rare malformation. Few clinical Russell R. Reid, M.D., Ph.D. reports have examined the efficacy of conservative or surgical management in Davinder J. Singh, M.D. the care of these patients. Scott P. Bartlett, M.D. Methods: All patients with a diagnosis of true lambdoid synostosis treated by Philadelphia, Pa. the senior author (S.P.B.) at The Children’s Hospital of Philadelphia be- tween 1990 and 2005 were included in the study. Both qualitative and quantitative assessments of craniofacial growth were performed following either conservative or surgical management. Qualitative assessments were made based on preoperative and postoperative photographs, computed tomographic scans, and a review of patient charts. A quantitative assessment of ear position was performed using craniometric analysis and the appro- priate statistical tests. Results: The study included nine patients—six who underwent surgical in- tervention and three who did not undergo transcranial surgery to date. The authors’ analysis of patient data revealed a predictable craniofacial dysmor- phism manifest as occipital flattening, an ipsilateral occipitomastoid bulge, and a pronounced hemifacial deficiency. Generally, these malformations improved following operative management. A quantitative analysis of pre- operative and postoperative ear position displayed no statistically significant vertical or anteroposterior displacement. In one untreated patient, true lambdoid synostosis resulted in persistent severe asymmetry of the cranial vault and facial skeleton. Conclusions: True lambdoid synostosis, if left untreated, results in pronounced craniofacial asymmetry. Although a diversity of clinical presentations exists, diag- nostic features include occipital flattening, an ipsilateral occipitomastoid bulge, and a contralateral hemifacial deficiency. Posterior vault switch cranioplasty is an ef- fective treatment for true lambdoid synostosis when performed in the first year of life. (Plast. Reconstr. Surg. 120: 993, 2007.)

rue lambdoid craniosynostosis is a rare mal- cles have discussed the surgical management of formation. Accounting for 1 to 4 percent of patients with lambdoid synostosis.6–14 However, Tall cases of craniosynostosis, true lambdoid the majority of these reports have included sub- synostosis occurs once in every 40,000 sets of patients who likely do not fit the strict births.1–3 Although the recent literature compar- diagnostic criteria for true lambdoid synostosis. ing the diagnostic evaluation of patients with Furthermore, although some articles do discuss true lambdoid synostosis and deformational pla- the results of surgical therapy in patients with 1–3 giocephaly exists,2–5 only a small number of arti- true lambdoid synostosis, none offers long- term follow-up documenting the results of con- From the Division of Plastic Surgery, The Children’s Hospital servative or surgical management. The aim of of Philadelphia, and the Department of Surgery, University this study was to examine the clinical presenta- of Pennsylvania Medical Center. tion and long-term outcomes of patients with Received for publication January 9, 2006; accepted May 14, true lambdoid synostosis treated both surgically 2006. and conservatively at a large craniofacial center. Presented at the 11th Biennial Meeting of the International Society of Craniofacial Surgery, in Queensland, Australia, PATIENTS AND METHODS September 11 through 14, 2005. Inclusion and Exclusion Criteria Copyright ©2007 by the American Society of Plastic Surgeons A retrospective chart review of patients treated DOI: 10.1097/01.prs.0000278043.28952.e8 over the past 15 years at the Craniofacial Center of

www.PRSJournal.com 993 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 1. Characteristics of all patients at our institution with a diagnosis of lambdoid synos- tosis.Ofthefinalninepatientsincludedinthestudy,onesufferedfromanassociatedanomaly (cleft lip–cleft palate).

The Children’s Hospital of Philadelphia (1990 and rotated 90 to 180 degrees until the best fit is through 2005) was conducted. Any patient with achieved. These flaps are positioned and fixed computed tomography–diagnosed true lambdoid anteriorly, with any resulting gaps in the ipsilateral synostosis initially evaluated by the senior author posterior vault reduced through advancement of (S.P.B.) was included in the study. Exclusion criteria an occipital bar harvested from the inferior mar- included the involvement of multiple sutures, inad- gin of the dissection. Any further gaps in the af- equate patient data, and patients no longer actively fected side of the posterior vault are filled using followed by the craniofacial center (Fig. 1). cranial bone grafts drawn from the anterior mar- gin of the contralateral bone flap. In the majority Surgical Technique of cases, rigid fixation of the bony skeleton was All patients who received surgical treatment in provided through the application of resorbable the study underwent the same operative proce- plating systems and supplemented with traditional dure. Operative management included a switch 26-gauge stainless steel wires. cranioplasty with occipital bar advancement (Fig. In the two cases presenting to our clinic be- 2). In this procedure, the posterior cranial vault is yond the second year of life, one was managed by bisected and two bone flaps raised. On the af- extracranial contouring with bone grafts and bone fected side, the basicranium is osteotomized, re- ceramics (as the parents wished to avoid any trans- leased, and positioned posteriorly to provide sym- cranial procedure), whereas the other patient, metry with the unaffected side. The bone flaps are now 3 years old, will undergo formal switch cra- then transposed to the opposite side (“switched”) nioplasty as described above. A third patient yet to

994 Volume 120, Number 4 • True Lambdoid Craniosynostosis

Fig.2. Operativetechnique.Intraoperativephotographsoftechniqueusedinthecorrectionoftruelamb- doid synostosis. The surgical technique involves the repositioning and advancement of an occipital bar with occipitoparietal reshaping using a switch cranioplasty technique. be treated is 8 months old at the time of this tance (external auditory meatus to nasofrontal hori- report, and will undergo switch cranioplasty in the zontal)normal, where nasofrontal horizontal is the line near future. extrapolated from the nasofrontal suture to the oc- ciput. To rule out the possibility that the differ- Qualitative Assessment of Craniofacial Growth ences between affected and normal sides did not merely represent a standard variation in the pop- Patient charts, photographs, and radiographic ulation, the above indices were also calculated materials were screened in detail for the following: from three-dimensional computed tomographic (1) age at initial evaluation; (2) age at initial sur- images obtained from a control group of sex- gery; (3) preoperative and postoperative features matched trauma patients from the radiographic of lambdoid synostosis (occipital flattening, ipsi- database at The Children’s Hospital of Philadel- lateral occipitomastoid prominence, compensa- phia (n ϭ 10). Pediatric trauma patients who ex- tory craniofacial morphology, ipsilateral ear dis- perienced fractures of the cranial vault, anterior placement); (4) associated craniosynostoses and cranial base/frontal sinus, nasoorbital ethmoid re- diagnoses; (4) surgical technique and complica- gion, or orbital roof, thereby affecting the normal tions; and (5) secondary procedures. Outcome position of the external auditory meatus or naso- parameters assessed included cranial vault shape, frontal suture, were excluded. Results are ex- frontofacial symmetry, occipitomastoid contour, pressed as mean Ϯ SEM. Differences between and ear position. craniometric indices of patient and control pa- tients were analyzed statistically by the paired t test Quantitative Assessment of Ear Asymmetry (Microsoft Excel; Microsoft Corp., Redmond, To quantify the preoperative and postoperative Wash.). In all analyses, values of p Ͻ 0.05 represent position of the ear, craniometric analysis was per- statistical significance. formed on three-dimensional surface reformatted digital images, comparing the relative position of the RESULTS external auditory meatus between affected and nor- mal sides of each patient. Two indices were mea- Patient Characteristics sured to determine the relative discrepancy between Of all patients treated for craniosynostosis at the affected and normal sides in both the antero- our institution, 17 were initially identified with a posterior (horizontal) and craniocaudad (vertical) diagnosis of true lambdoid craniosynostosis. Eight planes: (1) distance (external auditory meatus to of these patients were excluded from the study nasofrontal suture)affected/(external auditory meatus because of multiple suture involvement, inade- to nasofrontal suture)normal, (2) distance (external quate data, or a lack of follow-up. Nine patients auditory meatus to nasofrontal horizontal)affected/dis- were included in the study (Fig. 1). Two of these

995 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 3. Preoperative and postoperative calvarial shape in six patients as de- picted in axial views of three-dimensional computed tomographic scans. The y axis indicates time in years. (Above) Preoperative head shapes. The side of the affected suture is indicated using a star adjacent to the photograph. Note the frequency of contralateral forehead retrusion in this series. (Second row, third row, and below) Calvarial shape at 3, 7, and more than 10 years postoperatively. Note the resolution of both posterior and anterior plagiocephaly following sur- gical intervention. patients presented later in life after having re- (Figs. 3 and 4). In six of nine cases, contralateral ceived neither surgical therapy nor treatment with frontal retrusion was seen on the vertex view of a cranial remodeling helmet. A third is scheduled their digital photographs and three-dimensional for operative treatment in the near future. The computed tomographic scans. In the remaining remaining six patients underwent surgical man- three cases, the frontal asymmetry was negligible agement of their deformity. Among the six pa- (Fig. 3). Moreover, a consistent frontofacial asym- tients receiving operative management transcra- metry, with hemifacial deficiency contralateral to nially, the average age of initial evaluation was 5.2 the affected lambdoid suture, was found in all months (range, 2 to 14 months) and the average patients (Fig. 5). These features of craniofacial age of initial surgery was 8.3 months (range, 5 to dysmorphism were most visible in those patients 16 months). In all cases of operative management, who underwent no surgical intervention (Figs. 6 computed tomographic findings of true lambdoid and 7). synostosis were confirmed intraoperatively. The average length of follow-up was 7 years (range, 3 to 12 years). There was one patient with an asso- Quantitative Assessment of External Auditory ciated anomaly in our series (unilateral cleft lip– Meatus Position cleft palate). In this series, there were no deaths, major or minor complications (including reop- Craniometric analysis revealed no statistically eration), or perturbations in cognitive develop- significant differences between preoperative, post- ment grossly appreciated. Average length of hos- operative, and control (trauma) subjects in both Ϯ Ϯ Ϯ pital stay after surgery was 4.0 days. horizontal (1.03 0.06, 0.97 0.06, and 0.98 0.04, respectively; p Ͼ 0.10), and vertical (1.2 Ϯ 0.25 versus 0.98 Ϯ 0.1 versus 0.95 Ϯ 0.07; preop- Qualitative Assessment of Preoperative erative versus postoperative versus control group, Craniofacial Dysmorphism p ϭ 0.06 preoperative versus control; p ϭ 0.09 All patients demonstrated ipsilateral occipital preoperative versus postoperative) dimensions flattening and an ipsilateral occipitomastoid bulge (Fig. 8).

996 Volume 120, Number 4 • True Lambdoid Craniosynostosis

Fig. 4. Preoperative and postoperative calvarial shape in six patients as de- picted in posterior views of three-dimensional computed tomographic scans. The side of the affected suture is indicated using a star adjacent to the photo- graph.Theyaxisindicatestimeinyears.(Above)Preoperativeheadshapes.Note the ipsilateral mastoid prominence exhibited by all patients. (Second row, third row, and below) Follow-up computed tomographic scans at 3, 7, and more than 10 years postoperatively. Note the improvement of mastoid asymmetry in most patients following surgical intervention.

Postoperative Assessment of Craniofacial the malformation has precluded most practitio- Dysmorphism ners from documenting the efficacy of any surgical In patients who were managed surgically, intervention. Excluding earlier articles in which craniofacial dysmorphism improved steadily over diagnostic criteria likely included a majority of time. Specifically, posterior vault switch cranio- patients with deformational plagiocephaly,6,8–16 in plasty led to normalization of the cranial vault this article we describe the largest series to date shape in the majority of patients examined documenting the surgical management of pa- (Figs. 3 and 4). Similarly, reduction of the oc- tients with true lambdoid synostosis. Furthermore, cipitomastoid prominence characteristic of this this series is the only one to provide an analysis of disease also occurred, although complete nor- long-term results following surgical intervention. malization of this region was not seen. Despite Much of the recent literature regarding lamb- surgical intervention, the contralateral hemifa- doid synostosis focuses on the diagnostic differ- cial deficiency characteristic of these patients ences between the true malformation and abnor- often persisted. mal head shapes created through deformational forces. To this end, some authors believe that pre- dictable differences exist between both categories DISCUSSION of patients, whereas others find diagnosis based on True lambdoid synostosis is a rare malforma- certain morphologic characteristics less reliable. tion for which an optimal form of management Huang et al., reporting on a series of patients with remains elusive. Although the recent literature posterior plagiocephaly, believe that the clinical has provided many articles that discuss the diag- presentation of the two groups is “distinctively nostic differences between deformational plagio- different.”2,5 Although both groups of patients cephaly and true lambdoid synostosis, a corre- present with ipsilateral occipital flattening and spondingly small number of articles have provided contralateral posterior bossing, these authors con- meaningful outcomes following surgical interven- tend that patients with true lambdoid synostosis tion. Ultimately, it is likely that the rare nature of manifest superior and lateral parietal bossing,

997 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 5. Contralateral hemifacial deficiency persists despite surgical correction. Preoperative and postop- erative photographs of three patients. (Above, left) Patient with right lambdoid synostosis at 2 months of age. Note the contralateral supraorbital, maxillary, and mandibular asymmetry. (Above, right) Postopera- tive view. (Center, left) Preoperative photograph of a patient with right lambdoid synostosis at 14 months of age. (Center, right) Note the residual left hemifacial deficiency. (Below, left) Preoperative view of a patient with right lambdoid synostosis at 4 months of age. (Below, right) Postoperative view at 12 years’ follow-up. Again, note the residual left hemifacial deficiency.

998 Volume 120, Number 4 • True Lambdoid Craniosynostosis

Fig. 6. Results following conservative management of true lambdoid synostosis. Photographs and three-dimensional computed tomographic scans of a patient with untreated left lambdoid synos- tosisthatpresentedattheageof14years.Notetheuncorrectedsequelaeofthemalformation,including ipsilateral occipital flattening, ipsilateral mastoid prominence, and hemifacial deficiency. contralateral frontal bossing, an ipsilateral occip- on the morphology of two patients with true lamb- itomastoid bulge, and a posteriorly and inferiorly doid synostosis, David and Menard1,17 argued that displaced ear. The consistent nature of these find- patients with true lambdoid synostosis were more ings in their patient population led the authors to likely to suffer from an anteriorly rather than pos- advocate the term “trapezoid shaped head” as a teriorly displaced ear. Mulliken et al.,3 reviewing descriptor of these rare patients. David and the available computed tomographic scans of Menard,1,17 and subsequently Mulliken et al.,3 seven infants with true lambdoid synostosis, ar- were the first authors to question the reliability of gued that patients with lambdoid synostosis were certain morphologic characteristics in the differ- no more likely to suffer forehead asymmetry than ential diagnosis of the two disease processes. Based patients with deformational plagiocephaly. Fur-

999 Plastic and Reconstructive Surgery • September 15, 2007

Fig.7. Resultsfollowingconservativemanagementoftruelambdoidsynostosis.Three-dimensionalcom- puted tomographic scans of a patient with untreated left lambdoid synostosis that presented at the age of 3 years. Note the uncorrected sequelae of the malformation, including ipsilateral occipital flattening, ipsilateral mastoid prominence, and hemifacial deficiency. thermore, the ear position that was of particular of the forehead described by Huang et al. and diagnostic significance for Huang et al. was found David and Menard1,2,5,17 is an inconsistent feature to be posteriorly displaced in a minority of cases of the malformation. In our series, six patients and symmetric in nearly half.2 displayed contralateral frontal retrusion, whereas The results of our study suggest that patients in the remaining three patients, the anterior cra- with true lambdoid synostosis exhibit a character- nial vault was perceived as nearly symmetrical. In istic and reproducible craniofacial dysmorphism. this respect, our findings are similar to those of Nonetheless, the characteristics of our patients are Mulliken et al.,3 who believe that changes in the not entirely consistent with descriptions provided anterior cranial vault are less predictable. Further- by other authors. The patients in this series ex- more, the anteroposterior and vertical position of hibited the deformities of the posterior skull dis- the external auditory meatus was variable, a dis- played by all patients with true lambdoid synosto- tribution confirmed by the lack of statistically sig- sis, characteristics that have been agreed on by all nificant data produced by our craniometric anal- authors addressing the pure malformation.1–3,17 ysis. Given the larger series of patients examined Based on a careful and meticulous review of pa- in the current analysis and the variability of the tient data in our series, the contralateral bossing findings in the anterior cranial vault and external

1000 Volume 120, Number 4 • True Lambdoid Craniosynostosis

Fig.8. Assessmentofearposition.(Above)Verticalearpositionwasevaluatedusingcraniometricanalysis.Thehorizontaldashedline wasdrawnfromthenasofrontalsuturetotheocciput.Fromthere,aperpendicularline(star)isdrawntotheexternalauditorymeatus. (Below) Horizontal ear position as determined by craniometric analysis. A line is drawn from the nasofrontal suture to the external auditory meatus as depicted in the figure. Bars represent means of the preoperative, postoperative, and trauma control groups. Error bars represent the SEM. auditory meatus, we are inclined to deemphasize external auditory meatus alone. Furthermore, our the diagnostic significance ascribed to these two results further call into question the ability of prac- characteristics. titioners to differentiate between true lambdoid syn- Using the presentation of our untreated adoles- ostosis and deformational plagiocephaly based on cent as a touchstone, we believe that true lambdoid morphologic characteristics alone. synostosis results in a pronounced craniofacial dys- The literature addressing the surgical man- morphism, the most consistent preoperative find- agement of patients with posterior plagiocephaly ings of which are as follows: (1) occipital flattening is difficult to navigate because of the diagnostic on the affected side, (2) an ipsilateral mastoid prom- uncertainty that dominated the field during the inence, and (3) a pronounced hemifacial deficiency 1980s and 1990s. In this respect, the literature can that manifests as hypoplasia of bone and soft tissues be divided into two categories: those studies with of the contralateral facial structures. In this respect, outcomes that likely include a significant number it is important to recognize that patients with true of patients with deformational plagiocephaly and lambdoid synostosis suffer a craniofacial dysmor- those for which the inclusion criterion was strictly phism that is not confined to the calvarial vault and limited to patients with true lambdoid synostosis

1001 Plastic and Reconstructive Surgery • September 15, 2007 diagnosed by computed tomography. The first mastoid prominence characteristic of the malfor- group of articles provides descriptions of the sur- mation. Although these results are encouraging, gical management of a strikingly large number of certain features of the malformation persist fol- patients (range, 21 to 74 total patients).6–8,13–16,18,19 lowing surgery, especially the contralateral facial Examples of relative significance include the con- deficiency, which demonstrated only partial reso- tribution of Pople et al.,19 whose patient sample lution in this series of patients. included nine infants with true lambdoid synos- tosis confirmed by pathologic tissue diagnosis. The authors advocate the use of a lambdoid strip CONCLUSIONS craniectomy with barrel staving of the surround- True lambdoid craniosynostosis is a rare dis- ing bone flaps for correction of the deformity. ease best addressed with early surgical interven- Although the authors’ experience with this man- tion. Although the patients in our series demon- agement technique was positive as judged by the strate deformities of the posterior vault consistent subjective assessment of parents and practitioner, with other reports, our analysis emphasizes the the mean follow-up time was only 6 months.19 The following preoperative characteristics: a hemifa- remainder of reports deploy diagnostic criteria for cial deficiency contralateral to the fused suture, lambdoid synostosis that is either no longer ac- and an equivocal ipsilateral ear position on a skel- cepted (increasing severity of the deformity with etal level. Switch cranioplasty leads to long-term time or perisutural sclerosis seen on plain radio- normalization of cranial vault shape, correction of graphs) or somewhat vague.6–8,13,14,16,18 Whatever occipitomastoid contour, and partial resolution of the shortcomings of these reports, it is noteworthy frontofacial asymmetry. that the majority conclude that surgical interven- Scott P. Bartlett, M.D. tion was efficacious in restoring craniofacial sym- Department of Surgery metry in the vast majority of patients, despite the University of Pennsylvania diversity of techniques used in surgical manage- 10 Penn Tower ment. Philadelphia, Pa. 19104 Considering the reports that specifically discuss [email protected] patients with true lambdoid synostosis, there remain few data on which to evaluate the efficacy of surgical DISCLOSURES intervention. Huang et al.,2 in reviewing the expe- None of the authors involved in the production of rience of two institutions, note only that four patients this article has any commercial associations that might received surgical management of their deformities pose or create a conflict of interest with information but offer no statements regarding results. The article presented herein. Such associations include consultan- by Mulliken et al.3 documents the surgical manage- cies, stock ownership, or other equity interests; patent ment of 12 infants presenting with posterior plagio- licensing arrangements; and payments for conducting or cephaly. Although seven of these patients had com- publicizing a study described in the article. No intra- puted tomography–documented true lambdoid mural or extramural funding supported any aspect of synostosis, the authors offer no assessment of their this work. surgical results. Finally, David and Menard1 docu- ment the surgical management of two patients un- dergoing surgery for true lambdoid synostosis. REFERENCES These two patients were managed using either 1. David, D. J., and Menard, R. M. Occipital plagiocephaly. Br. J. Plast. Surg. 53: 367, 2000. fronto-orbital advancement or occipital craniec- 2. Huang, M. H., Gruss, J. S., Clarren, S. K., et al. The differ- tomy. In reviewing the outcomes, the authors state ential diagnosis of posterior plagiocephaly: True lambdoid only that these patients were “judged by their parents synostosis versus positional molding. Plast. Reconstr. Surg. 98: to be without notable improvement.” 765, 1996. The current series offers the most significant 3. Mulliken, J. B., Vander Woude, D. L., Hansen, M., LaBrie, R. A., and Scott, R. M. Analysis of posterior plagiocephaly: evaluation of surgical efficacy in the literature to Deformational versus synostotic. Plast. Reconstr. Surg. 103: date. In this article, we document long-term fol- 371, 1999. low-up of patients with isolated true lambdoid syn- 4. Ehret, F. W., Whelan, M. F., Ellenbogen, R. G., Cunningham, ostosis treated with an occipital switch cranioplasty M. L., and Gruss, J. S. Differential diagnosis of the trapezoid- technique performed during the first year of life. shaped head. Cleft Palate Craniofac. J. 41: 13, 2004. 5. Huang, M. H., Mouradian, W. E., Cohen, S. R., and Gruss, J. In the majority of cases, this surgical intervention S. The differential diagnosis of abnormal head shapes: Sep- resulted in a significant improvement in the pa- arating craniosynostosis from positional deformities and nor- tient’s occipital flattening and resolution of the mal variants. Cleft Palate Craniofac. J. 35: 204, 1998.

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6. Thaller, S. R., Hoyt, J., and Boggan, J. Surgical correction of 13. Goodrich, J. T., and Argamaso, R. Lambdoid stenosis (pos- unilateral lambdoid synostosis: Occipital rotation flap. terior plagiocephaly) and craniofacial asymmetry: Long- J. Craniofac. Surg 3: 12, 1992. term outcomes. Childs Nerv. Syst. 12: 720, 1996. 7. Zoller, J. E. Standardized occipital advancement: A new 14. Muakkassa, K. F., Hoffman, H. J., Hinton, D. R., Hendrick, method for therapy of lambda suture synostosis (in German). E. B., Humphreys, R. P., and Ash, J. Lambdoid synostosis: Mund Kiefer Gesichtschir. 1 (Suppl.): S75, 1998. Part 2. Review of cases managed at The Hospital for Sick 8. Zoller, J. E., Mischkowski, R. A., and Speder, B. Preliminary Children, 1972–1982. J. Neurosurg. 61: 340, 1984. results of standardized occipital advancement in the treat- 15. Carson, B. S., James, C. S., VanderKolk, C. A., and Guarnieri, ment of lambdoid synostosis. J. Craniomaxillofac. Surg. 30: 343, M. Lambdoid synostosis and occipital plagiocephaly: Clinical 2002. decision rules for surgical intervention. Neurosurg. Focus 2: e5, 9. Persing, J. A., Delashaw, J. B., Jane, J. A., and Edgerton, M. 1997. T. Lambdoid synostosis: Surgical considerations. Plast. Re- 16. Sgouros, S., Goldin, J. H., Hockley, A. D., and Wake, M. J. constr. Surg. 81: 852, 1988. Posterior skull surgery in craniosynostosis. Childs Nerv. Syst. 10. McComb, J. G. Treatment of functional lambdoid synostosis. 12: 727, 1996. Neurosurg. Clin. North Am. 2: 665, 1991. 17. Menard, R. M., and David, D. J. Unilateral lambdoid synostosis: 11. Jimenez, D. F., Barone, C. M., Argamaso, R. V., Goodrich, J. Morphological characteristics. J. Craniofac. Surg. 9: 240, 1998. T., and Shprintzen, R. J. Asterion region synostosis. Cleft 18. Dias, M. S., and Klein, D. M. Occipital plagiocephaly: De- Palate Craniofac. J. 31: 136, 1994. formation or lambdoid synostosis? II. A unifying theory re- 12. Jimenez, D. F., and Barone, C. M. The Sunrise Technique: garding pathogenesis. Pediatr. Neurosurg. 24: 69, 1996. The correction of occipital plagiocephaly using bandeau 19. Pople, I. K., Sanford, R. A., and Muhlbauer, M. S. Clinical occipital plate and radial osteotomies. Pediatr. Neurosurg. 22: presentation and management of 100 infants with occipital 162, 1995. plagiocephaly. Pediatr. Neurosurg. 25: 1, 1996.

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1003 PEDIATRIC/CRANIOFACIAL

The Incidence of Late Cephalohematoma following Craniofacial Surgery

Shadi Ghali, M.R.C.S. Background: Cranial vault remodeling procedures are carried out for both Kevin R. Knox, M.D. syndromic and nonsyndromic craniosynostosis as well as to correct some ac- Sean Boutros, M.D. quired deformities of the cranial vault. These procedures improve not only Charles H. Thorne, M.D. cosmesis but also neurological symptoms. The purpose of this study was to Joseph G. McCarthy, M.D. determine the incidence of “late” cephalohematoma, an underreported com- New York, N.Y., and Houston, Texas plication following these complex procedures. Methods: A total of 113 patients underwent 127 cranial vault remodeling pro- cedures using autogenous bone over a 6-year period. All patients who developed a late cephalohematoma 75 days or more after surgery were recorded. The time, size, and location of the cephalohematoma, the treatment performed, and the length of follow-up were also recorded. Ages at initial operation and postop- erative follow-up were compared between patient groups for statistical differ- ences. Results: Of the 113 patients, 17 developed 18 late cephalohematoms. The incidence for this complication was 15 percent. The median age at operation for all patients was 10 months, and most late cephalohematomas occurred 208 days later (range, 77 to 1416 days), at 12 to 24 months of age. Fronto-orbital advancement was the most commonly performed procedure, and 83.3 percent of late cephalohematomas occurred in the frontal region. No cephalohemato- mas became infected or required any operative intervention, but they were aspirated. Conclusions: Surgeons should inform prospective parents of patients under- going cranial vault remodeling procedures of this potential complication. This will improve parental awareness and possible avoidance strategies in future patients. Further evaluation and follow-up are required to determine the min- imum length of postoperative time after which late cephalohematomas do not occur. (Plast. Reconstr. Surg. 120: 1004, 2007.)

ranial vault remodeling is performed for a hematoma, otherwise known as a cephalohema- variety of clinical conditions. Most com- toma, following light trauma. Cephalohema- Cmonly, it is performed for the correction of toma can occur early in the postoperative course congenital malformations resulting from cranio- but may also occur several months to several synostosis, but it is also occasionally required for years after the original operation. Late cephalo- correction of acquired cranial deformities fol- hematoma is generally ignored and not given lowing traumatic injury or neurosurgical significant attention in preoperative discussions procedures.1–4 or consultations. The purpose of this study was After cranial vault remodeling procedures, pa- to review cranial vault remodeling procedures to tients occasionally present with a subperiosteal determine the incidence and treatment of cephalohematomas over a 6-year period from From the Institute of Reconstructive Plastic Surgery, New September of 1998 to June of 2004 following York University Medical Center; Houston Plastic and cranial vault remodeling procedures. Craniofacial Surgery; and Hermann Hospital and Her- mann Children’s Hospital. Received for publication January 12, 2006; accepted April PATIENTS AND METHODS 5, 2006. This retrospective chart review was approved The first two authors contributed equally to this article. by the New York University Institutional Review Copyright ©2007 by the American Society of Plastic Surgeons Board. All patients undergoing cranial vault re- DOI: 10.1097/01.prs.0000277997.56941.e5 modeling procedures by the two senior authors

1004 www.PRSJournal.com Volume 120, Number 4 • Incidence of Late Cephalohematoma

Table 1. Case Summary Data Late No Late Cephalohematoma Cephalohematoma Total (%)* p Boys 7 48 55 (49) Girls 10 48 58 (51) Age at first operation, months 0.74 Median 10 10 Range 3–192 2.5–216 Postoperative time to develop a late cephalohematoma, days Median 208 — Range 77–1416 — Age at late cephalohematoma, months Median 16.7 — Range 7.7–218.3 — Follow-up, days 0.36 Median 384 492 Range 90–2161 89–2244 *Total no. of patients, n ϭ 113.

(J.G.M. and C.H.T.) over a 6-year period between for inclusion in the study. The series included 55 September of 1998 and June of 2004 at New York boys and 58 girls, with a median age of 10 months University Medical Center were included in the (range, 2.5 to 216 months). Seventeen patients study. Patients who were treated with alloplastic (seven boys and 10 girls) developed 18 late cepha- material such as methylmethacrylate or synthetic lohematomas from a total of 113 patients (15.0 materials for repair of calvarial defects were ex- percent) and 127 procedures (Tables 1 and 2). cluded from the study, as these materials present The median age at operation of patients de- confounding variables for subperiosteal healing. veloping a late cephalohematoma was 10 months All charts were reviewed individually and all (range, 3 to 192 months). This was not signifi- patients who developed cephalohematomas were cantly different from the median age of patients at isolated. To exclude “early” operative cephalohe- operation who did not progress to the develop- matomas or fluid collections, all hematomas oc- ment of a late cephalohematoma, which was also curring within the first 75 postoperative days were 10 months (range, 2.5 to 216 months) (p ϭ 0.74) excluded. “Late” cephalohematomas were there- (Table 1). fore defined as cephalohematomas developing The median postoperative time to the devel- more than 75 days after a cranial vault surgical opment of a late cephalohematoma was 208 days intervention. (range, 77 to 1416 days) and the median age at the For patients who met the criteria for late time of this occurrence was 16.7 months (range, cephalohematoma, the median time to the devel- 7.7 to 218.3 months) (Table 1). There was no opment of a cephalohematoma, the age at devel- significant difference between the median fol- opment of a late cephalohematoma, the size and low-up period for patients who developed a late location of the cephalohematoma, the treatment cephalohematoma, 384 days (range, 90 to 2161 performed, and the median follow-up period were days), compared with those patients who did not recorded. Normally, patients are followed up at 1 develop a late cephalohematoma, 492 days (range, week, 3 weeks, 6 weeks, 3 months, 6 months, and 89 to 2244 days) (p ϭ 0.36) (Table 1). 1 year after discharge from the hospital. Measures such as median age at operation and Table 2. Procedural Frequency median follow-up period were compared for sta- No. of Late No Late tistical significance between the groups using a Procedures Cephalohematoma Cephalohematoma Mann–Whitney rank sum analysis, and a value of Ͻ 1 16* 95 p 0.05 was considered statistically significant. 21†4 Unless otherwise stated, all outcomes are ex- 301 pressed as median times. 401 Total 17 110 *In one patient, a second cephalohematoma developed 1416 days RESULTS after the initial procedure and 1250 days after the initial late cepha- lohematoma. From September of 1998 to June of 2004, 113 †One cephalohematoma occurred 191 days after the second proce- patients underwent 127 procedures and qualified dure.

1005 Plastic and Reconstructive Surgery • September 15, 2007

Table 3. Segregation by Age of Patients at the Initial cephalohematomas became infected or required Operation any further operative intervention. No Late Cephalohematoma Cephalohematoma DISCUSSION Age (%) (%) p Fronto-orbital advancement and cranial vault Յ12 months 74 (67.3) 13 (76.5) 0.82 remodeling procedures are carried out on a range 12–24 months 14 (12.7) 2 (11.7) 0.75 Ͼ of syndromic and nonsyndromic craniofacial 24 months 22 (20) 2 (11.7) 0.35 5–9 Total 110 17 deformities. Early surgery in craniosynostosis improves prognosis, allowing functional brain de- compression and resolution of the morphologic Table 4. Segregation by Age at Occurrence of a Late problem.10–14 Cephalohematoma Boutros et al.15 investigated healing at the peri- Age No. osteum/bone interface after raising and reattach- Յ12 months 2 ing a pedicled scalp flap in a guinea pig model. 12–24 months 10 After a 90-day period, the strength of adherence, Ͼ24 months 6 measured biomechanically, of the periosteum to Total 18 the underlying cranium plateaued at 80 percent compared with the control group. This is in keep- ing with experimental wound healing in skin in Seventeen of the 18 hematomas (94.4 per- which the tensile strength of a wound levels off at cent) occurred in 16 patients undergoing only one approximately 80 percent of the original un- procedure, with one patient developing a second wounded skin.16,17 This study, however, examined cephalohematoma 1250 days after the initial the healing at the periosteum/bone interface and cephalohematoma. Also, one patient developed a therefore the strength of adherence between a hematoma 191 days after a second cranial vault vascularized periosteal flap and vascularized bone remodeling procedure (Table 2). There was no in a mature animal. Subperiosteal brow-lift pro- significant difference in the age of patients at ini- cedures represent the clinical equivalent of vas- tial operation (Table 3) and the majority of late cularized periosteum and vascularized bone heal- cephalohematomas occurred between the ages of ing. A high incidence of late cephalohematoma 12 and 24 months (Table 4). has not been observed or reported in patients Procedures performed included cranial vault undergoing these procedures. remodeling for sagittal suture synostosis [25 (19.7 During fronto-orbital advancement and cra- percent)], fronto-orbital advancement [86 (67.7 nial vault remodeling procedures, portions of the percent)], and other cranioplasties including rib cranial vault are removed, reshaped, and replaced graft [16 (12.6 percent)]. No significant differ- as devascularized bone grafts.18–20 In situ, the cal- ences were found in occurrence with regard to the varia receives its blood supply from extracranial type of procedure performed. sources by means of the periosteum and intracra- In this series, all cephalohematomas were the nial sources through the dura mater.11,21 There- result of light trauma, such as a fall from a bed or fore, once harvested and removed from its blood a low-impact bump into a wall. Cephalohema- supply, free bone grafts are completely reliant on tomas averaged 15 cc in size and occurred most the recipient soft tissues/remaining periosteum frequently in the frontal region [15 of 18 (83.3 and dura for their revascularization and nutrition. percent)]. Treatment of cephalohematomas Adequate blood supply is also critical for wound larger than 10 cc was by aspiration. Patients were healing.22,23 The dependence of wound healing on given topical EMLA Cream (AstraZeneca, Lon- an adequate blood supply is all too evident both don, England) and aspirated with a 16-gauge nee- experimentally and clinically in diabetic and vas- dle or a 16-gauge Angiocath (Becton Dickinson culopathic patients with chronic wounds.24–26 Infusion Therapy Systems, Inc., Sandy, Utah) in We hypothesized therefore that because these the most dependent portion of the cephalohema- free bone grafts have to engraft and therefore toma. Povidone-iodine ointment preparation of establish an adequate blood supply from recipient the area was also carried out before aspiration in tissue beds, this may result in a limited healing the clinic setting. A maximum of three aspirations capability,27,28 ultimately leading to decreased were performed, one per week, over a 3-week pe- overall strength of adherence at the soft-tissue/ riod until there was no evidence of residual he- bone interface of a healed segment of calvaria matomas, or the size estimate was less than 5 cc. No following a cranioplasty procedure such as cranial

1006 Volume 120, Number 4 • Incidence of Late Cephalohematoma vault remodeling. This lack of full strength at the in this review covers a 6-year period and the me- soft-tissue/bone interface would leave the recon- dian time to development of a late cephalohema- structed cranium at an increased risk of cephalo- toma was 208 days (range, 77 to 1416 days), the hematoma following light trauma. incidence of late cephalohematomas will almost Furthermore, the two senior authors have ob- certainly be an underestimate of the final value. served in secondary cranioplasty procedures and All treatments in this series were carried out in in procedures in syndromic patients requiring ac- the clinic setting. Serial aspirations using EMLA cess through a coronal exposure that reelevation Cream applied topically29,30 45 minutes before as- of the scalp in the subperiosteal plane is very dif- piration, and a 16-gauge needle or a 16-gauge ferent from that in the original exposure. It is in Angiocath, was the technique used. No patient fact rare not to encounter a very loose attachment required more than three serial aspirations. There of the periosteum to the underlying bone. were no long-term sequelae from the cephalohe- This theoretical susceptibility to develop a matomas and no secondary infections requiring loose adherence at the soft-tissue/bone interface formal debridement or drainage under general resulting in cephalohematoma, in combination anesthesia. with our clinical observations, prompted this To our knowledge, this is the only series that study, the aim of which was to determine the in- has specifically focused on the incidence of late cidence of late cephalohematoma following cra- cephalohematoma following cranial vault remod- nial vault remodeling procedures. Early cases of eling procedures. We believe that the incidence of postoperative cephalohematoma were excluded this complication is related more to the healing from the analysis to minimize the influence of the process at the soft-tissue/bone interface with avas- procedure itself on the development of a cepha- cular bone than to the initial cranial vault remod- lohematoma. Although this cannot be excluded eling procedure per se. altogether, 75 days was chosen as the cutoff, mir- Because late cephalohematomas occurred in roring the plateau in the rate of wound healing over 15 percent of patients undergoing cranial observed by other investigators.15–17 vault remodeling in this series, it is important to We found that the development of a late inform the parents of patients undergoing cranial cephalohematoma was not a rare occurrence fol- vault remodeling about the likelihood of this com- lowing fronto-orbital advancement and cranial plication late in the patient’s postoperative course. vault remodeling procedures but indeed occurred This will improve parental awareness and possible in nearly one in six patients (15.0 percent), and avoidance of this complication in these patients. was invariably the result of light head trauma. This Finally, serial aspiration was an effective treatment complication occurred in the frontal region 83.3 modality, and no long-term morbidity was seen. percent of the time, reflecting not only the site of Further evaluation and follow-up are required to operation but also the region most prone to injury determine the minimum length of postoperative in the mobile child. time—currently 1416 days—after which late Our usual level of dissection in the frontal cephalohematomas do not occur in this and fu- region is in the subgaleal plane to the midfore- ture series. head and the subperiosteal plane thereafter over Sean Boutros, M.D. the supraorbital ridge and brow and the lateral Houston Plastic and Craniofacial Surgery orbital rim. Periosteum over osteotomized bone 6410 Fannin, Suite 732 rarely remains intact following these procedures, Houston, Texas 77030 which may explain this high incidence of late [email protected] cephalohematoma. There were no significant differences between patients in terms of age at first operation, but most DISCLOSURE of those patients who went on to develop a late None of the authors has a financial interest in any cephalohematoma were operated on before 12 of the products, devices, or drugs mentioned in this months of age (Table 3). Most late cephalohema- article. tomas occurred between 12 and 24 months (Table 4). This may reflect the median time to develop a REFERENCES cephalohematoma (208 days) after the first oper- 1. Dujovny, M., Aviles, A., Agner, C., Fernandez, P., and Char- bel, F. T. Cranioplasty: Cosmetic or therapeutic? Surg. Neurol. ation, or may reflect an increased frequency of 47: 238, 1997. falls in the 12- to 24-month age group as these 2. Segal, D. H., Oppenheim, J. S., and Murovic, J. A. Neuro- patients learn to walk. As the maximum follow-up logical recovery after cranioplasty. Neurosurgery 34: 729, 1994.

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3. Stula, D., and Muller, H. R. Cranioplasty after extensive 17. Robinson, J. B., and Friedman, R. M. Wound healing and decompressive craniotomy with displacement of the cerebral closure. Select. Read. Plast. Surg. 8: 18,1996. hemisphere: CA analysis (in German; author’s translation). 18. Marchac, D., Cochignon, J., Clay, C., and Rey, A. Repair of Neurochirurgia (Stuttg.) 23: 41, 1980. the orbit roof by duplication of the frontal bone flap (in 4. Stula, D. The problem of the “sinking skin-flap syndrome” in French). Nouv. Presse Med. 2: 2413, 1973. cranioplasty. J. Maxillofac. Surg. 10: 142, 1982. 19. Psillakis, J. M., Nocchi, V. L., and Zanini, S. A. Repair of large 5. Marchac, D., and Renier, D. Cranio-facial surgery for cranio- defect of frontal bone with free graft of outer table of parietal synostosis. Scand. J. Plast. Reconstr. Surg. 15: 235, 1981. bones. Plast. Reconstr. Surg. 64: 827, 1979. 6. McCarthy, J. G. New concepts in the surgical treatment of the 20. McCarthy, J. G., and Zide, B. M. The spectrum of calvarial craniofacial synostosis syndromes in the infant. Clin. Plast. bone grafting: Introduction of the vascularized calvarial Surg. 6: 201, 1979. bone flap. Plast. Reconstr. Surg. 74: 10, 1984. 7. Marchac, D., Renier, D., and Broumand, S. Timing of treat- 21. Cutting, C. B., McCarthy, J. G., and Berenstein, A. Blood ment for craniosynostosis and facio-craniosynostosis: A 20- supply of the upper craniofacial skeleton: The search for year experience. Br. J. Plast. Surg. 47: 211, 1994. composite calvarial bone flaps. Plast. Reconstr. Surg. 74: 603, 8. McCarthy, J. G., Glasberg, S. B., Cutting, C. B., et al. Twenty- 1984. year experience with early surgery for craniosynostosis: I. 22. Clark, R. A. F. The Molecular and Cellular Biology of Wound Isolated craniofacial synostosis—Results and unsolved prob- Repair, 2nd Ed. New York: Plenum Press, 1996. 23. Singer, A. J., and Clark, R. A. Cutaneous wound healing. lems. Plast. Reconstr. Surg. 96: 272, 1995. N. Engl. J. Med. 341: 738, 1999. 9. McCarthy, J. G., Glasberg, S. B., Cutting, C. B., et al. Twenty- 24. Fahey, T. J., III, Sadaty, A., Jones, W. G., Barber, A., Smoller, year experience with early surgery for craniosynostosis: II. B., and Shires, G. T. Diabetes impairs the late inflammatory The craniofacial synostosis syndromes and pansynostosis— response to wound healing. J. Surg. Res. 50: 308, 1991. Results and unsolved problems. Plast. Reconstr. Surg. 96: 284, 25. Tepper, O. M., Galiano, R. D., Capla, J. M., et al. Human 1995. endothelial progenitor cells from type II diabetics exhibit 10. Abe, H., Ikota, T., Akino, M., Kitami, K., and Tsuru, M. impaired proliferation, adhesion, and incorporation into Functional prognosis of surgical treatment of craniosynos- vascular structures. Circulation 106: 2781, 2002. tosis. Childs Nerv. Syst. 1: 53, 1985. 26. Kerstein, M. D. The non-healing leg ulcer: Peripheral vas- 11. McCarthy, J. G., May, J. W., and Littler, J. W. Plastic Surgery, cular disease, chronic venous insufficiency, and ischemic 1st Ed., Vol. 2. Philadelphia: Saunders, 1990. vasculitis. Ostomy Wound Manage. 42 (10A Suppl.): 19S, 1996. 12. Bottero, L., Lajeunie, E., Arnaud, E., Marchac, D., and Re- 27. Losken, H. W., Pollack, I. F., and Singhal, V. K. Vascularized nier, D. Functional outcome after surgery for trigonoceph- fronto-orbital advancement. J. Craniofac. Surg. 7: 107, 1996. aly. Plast. Reconstr. Surg. 102: 952, 1998. 28. Stevenson, S. Enhancement of fracture healing with autog- 13. Marentette, L. J., and Kim, J. Y. Correction of nonsyndromal enous and allogeneic bone grafts. Clin. Orthop. Relat. Res. 355 craniosynostosis. Facial Plast. Surg. Clin. North Am. 9: 93, 2001. (Suppl.): S239, 1998. 14. Flores-Sarnat, L. New insights into craniosynostosis. Semin. 29. Kleiber, C., Sorenson, M., Whiteside, K., Gronstal, B. A., and Pediatr. Neurol. 9: 274, 2002. Tannous, R. Topical anesthetics for intravenous insertion in 15. Boutros, S., Bernard, R. W., Galiano, R. D., Addona, T., children: A randomized equivalency study. Pediatrics 110. Stokes, B., and McCarthy, J. G. The temporal sequence of 758, 2002. periosteal attachment after elevation. Plast. Reconstr. Surg. 30. Eichenfield, L. F., Funk, A., Fallon-Friedlander, S., and Cun- 111: 1942, 2003. ningham, B. B. A clinical study to evaluate the efficacy of 16. Geever, E. F., Stein, J. M., and Levenson, S. M. Variations in ELA-Max (4% liposomal lidocaine) as compared with eutec- breaking strength in healing wounds of young guinea pigs. tic mixture of local anesthetics cream for pain reduction of J. Trauma 5: 624, 1965. venipuncture in children. Pediatrics 109: 1093, 2002.

1008 PEDIATRIC/CRANIOFACIAL

Reduction of Morbidity of the Frontofacial Monobloc Advancement in Children by the Use of Internal Distraction

Eric Arnaud, M.D. Background: Surgical treatment of faciocraniosynostosis is a complex problem Daniel Marchac, M.D. that includes both function and aesthetics. Treatment goals are to prevent Dominique Renier, M.D. further neurologic disorders and to correct the morphologic impairment. Paris, France Methods: Thirty-six patients with faciocraniosynostosis (mean age, 5.2 years) were evaluated prospectively after frontofacial monobloc advancement and quadruple internal distraction. Four distractors were used in combination with a frontofacial monobloc advancement osteotomy. Complications and advance- ment were evaluated clinically and radiographically. Respiratory status was eval- uated by polysomnography. Relapse was evaluated by comparing results at the time of distractor removal to 6-month values. The mean follow-up was 30 months. Results: Distraction was completed in 35 patients. Twenty-eight patients (80 percent) completed their distraction uneventfully in the initial period. In seven patients, a problem related to the distraction devices required revision surgery, and subsequently six of them completed the distraction. One patient died the day after surgery from acute brain tonsillar herniation before distraction was begun. The exorbitism was corrected clinically in all patients in whom distrac- tion was completed (n ϭ 34). A class I occlusal relationship was obtained in 28 of 35 patients (80 percent). When respiratory impairment was present, it was corrected in all but two cases (14 of 16). A septic frontal osteonecrosis occurred in one patient 2 months after distraction was completed (frontal bone loss in one of 35 patients). Reossification at time of distractor removal was limited. Relapse has been observed predominantly at the occlusal level (six of 35) and more frequently in Pfeiffer syndrome. Conclusions: Internal distraction allows for early correction of respiratory im- pairment and exorbitism of faciocraniosynostosis, and limits the major risks of frontofacial monobloc advancement. Previous operations performed before the frontofacial monobloc advancement increased its morbidity. (Plast. Reconstr. Surg. 120: 1009, 2007.)

urgical treatment of faciocraniosynostosis is skull volume. The simultaneous correction of a complex problem that includes both frontofacial retrusion prevents both corneal ex- Sfunction and aesthetics. Treatment goals posure resulting from exorbitism, chronic hy- are to prevent further neurologic disorders and poxemia caused by impaired upper airways, and to correct the morphologic impairment. The a distorted morphologic appearance. Frontofa- risk of mental retardation (and/or blindness) by cial monobloc advancement can simultaneously an increase of intracranial pressure should be correct frontal and facial retrusion by allowing treated preemptively with early augmentation of enlargement of both orbits and airways.1,2 How- ever, as a result of the necessary osteotomy of the From the Unite´ de Chirurgie Craˆnio-Faciale, Hoˆpital Necker floor of the anterior skull base, the frontofacial Enfants Malades. monobloc advancement produces two poten- Received for publication November 11, 2005; accepted April tially detrimental consequences: the creation of 20, 2006. a retrofrontal dead space and the communica- Copyright ©2007 by the American Society of Plastic Surgeons tion between the anterior base of the skull and DOI: 10.1097/01.prs.0000278068.99643.8e the nasal cavity. As a consequence, infections can

www.PRSJournal.com 1009 Plastic and Reconstructive Surgery • September 15, 2007 occur, leading to reoperation and eventually life- ment and distraction with promising results,23–27 threatening complications (e.g., meningitis, ne- with either internal or external distraction devices. crosis of the frontal bone).3–6 Twenty years ago, Nevertheless, some craniofacial surgeons world- in our center, the rate of frontal infections had wide still remain hostile to this procedure because been evaluated to be close to 30 percent, and of the fear of the risks. We present our experience there was an unacceptable mortality rate of 15 with the first 36 frontofacial monobloc advance- percent (unpublished data). Therefore, this pro- ments performed with a double pair of internal cedure has been limited historically in its use in distraction devices in infants and children with our center, but also by most international teams, faciocraniosynostosis25,28–30 treated surgically in our who experienced similar complication rates. unit between September of 2000 and November of Nevertheless, some outstanding surgeons re- 2004. ported lower rates of complications for frontofa- cial monobloc advancement without distraction, PATIENTS AND METHODS but pointed out the detrimental effect of combi- Thirty-six patients underwent a frontofacial nation with a ventricular shunt.6 Nevertheless, monobloc advancement procedure in the cranio- we consider a worthwhile surgical treatment one facial unit of Necker Enfants Malades Hospital in that can be carried out by an average craniofacial Paris between September of 2000 and October of surgeon with safe and reliable results: frontofa- 2004 and were studied prospectively. The mean cial monobloc advancement without distraction age at surgery was 5.2 years, ranging from 7 did not comply with these requirements. Several months to 13 years. All patients presented with ancillary procedures such as filling of the ante- faciocraniosynostosis. There were 19 cases of rior cerebral fossa by a flap or the lamellar split Crouzon syndrome, eight cases of Pfeiffer syn- osteotomy have been proposed, adding to the drome, eight cases of Apert syndrome, and one complexity of the procedure.7–10 Nevertheless, case of Shprintzen-Goldberg syndrome. Three of frontofacial monobloc advancement remains a the patients with Pfeiffer syndrome were suffering powerful surgical technique with the potential of with recurrent proptosis and chronic conjunctivi- providing complete correction of faciocraniosyn- tis, threatening their vision. All patients presented ostosis. The principal indications for frontofacial with a maxillary retrusion causing a class III oc- monobloc advancement were usually restricted clusal relationship, with 16 of them suffering from to vision-threatening exorbitism or severe an airway impairment leading to night hypoxemia breathing impairments in infants in whom the (diagnosed by polysomnography with an oxygen benefits outweigh the risks.5,11,12 level less than 95 percent). Six of the affected The routine treatment of faciocraniosynosto- patients required a permanent tracheostomy (six sis can be managed by a two-stage strategy that of 16) for an impaired airway. Nocturnal snoring diminishes the risks. We have traditionally was a common feature encountered in almost all treated craniosynostosis by a frontoorbital ad- patients and was not considered a major impair- vancement before 1 year of age.13–15 Treatment ment if the polysomnogram was normal. of the facial retrusion has usually been delayed: All 36 patients (group A) underwent fronto- the facial advancement (Le Fort III type) is per- facial monobloc advancement with distraction. formed at 5 to 6 years of age or even later, unless Among these patients, 25 children (subgroup A1) a severe breathing impairment requires an ear- underwent frontofacial monobloc advancement lier surgical correction. A secondary maxillary as the first procedure in the anterior region with- advancement (Le Fort I) might be necessary out having undergone any previous surgery such after 14 years of age to correct the maxillary as fronto-orbital advancement or Le Fort III ad- hypoplasia caused by its congenital lack of vancement. Procedures such as cerebral ventricu- growth, to obtain a class I occlusion. lostomy, shunting, posterior expansion, and lateral With the successful use of distraction techniques skull vault decompression were not considered to be in the hypoplastic mandible of hemifacial primary procedures because they were not affecting microsomia,16,17 distraction has gained general ac- the anterior anatomical region. In this subgroup, A1, ceptance as a surgical tool in craniofacial surgery. four patients were treated for active hydrocephalus, In other congenital disorders that required bony leading to a shunt in two patients and a ventricul- lengthening to improve the stigmatic features, dis- ocisternostomy in two other patients. Eleven chil- traction has also been applied with great dren (subgroup A2) had previously undergone a success.18–22 Preliminary reports have described the fronto-orbital advancement, a Le Fort III advance- combination of frontofacial monobloc advance- ment, or both, with an insufficient result necessitat-

1010 Volume 120, Number 4 • Frontofacial Monobloc Advancement ing reoperation. Among the secondary cases was crews, 2 mm in diameter and 5 mm in length (Fig. found a high proportion of cases of Pfeiffer syn- 2). In four patients, rigid fixation was performed drome (five of 11), one of whom was underweight, by miniplates, either metallic or resorbable, to which could have been linked to severe chronic hy- reinforce the fragile frontozygomatic junction. In poxemia. In this subgroup, A2, one patient only had five patients, a transfacial pin (Kirschner wire, 2.5 been shunted previously. mm) was used to stabilize the zygomas in a hori- A total of 36 patients are presented in this zontal plane, avoiding malar dysjunction and to study: subgroup A1 (n ϭ 25), primarily treated by reinforce the distraction system. The communi- frontofacial monobloc advancement with distrac- cation between the base of the skull and the nasal tion; and subgroup A2 (n ϭ 11), secondarily cavity was obturated with a patch of periosteum treated by frontofacial monobloc advancement. and fibrin glue,33 or with a pericranial pedicled The mean follow-up after surgery was 2.5 years, flap. The average duration of the surgical proce- ranging from 1 to 5 years. dure was approximately 210 minutes (range, 140 to 275 minutes). Surgical Technique and Distractors Frontofacial monobloc with complete osteot- omy was performed.2 The forehead bony flap was Distraction Protocol and Consolidation Phase elevated (35 of 36) in all cases, except in one patient After a mean latency period of 5 days, the in whom a “true monobloc” was performed.31 This distraction protocol was standardized as one ad- true monobloc was our first case (September of vancement of 1 mm per day for each of the four 2000). Because of its inherent additive complexity, distractors, unless a cerebrospinal fluid leak oc- and high potential perioperative morbidity, we curred. A genuine leak occurred in five patients. have abandoned its use, as will be discussed later. These presented the day after the procedure, and In all other patients, elevation of the forehead distraction was delayed until the leakage had sub- allowed easy access to the anterior skull base, lat- sided. In these cases, the start of distraction was eral trimming of the inferior edge, and fixation by delayed to between 9 and 15 days after frontofacial metallic wires to allow posterior rotation of the monobloc advancement. forehead.32 Pterygomaxillary bilateral dysjunction Thirty minutes before distraction, patients and mobilization of the face with Rowe forceps were given an oral analgesic. In the youngest pa- were performed in a standardized fashion (Fig. 1). tients, a 3-minute inhalation of nitrous oxide was Two pairs of internal distraction devices (cra- given in addition immediately before activation of nial and temporomalar, Martin-Medizin) were im- the distractors. With the cranial distractor range planted in each patient. Fixation of each distractor being 0.3 mm, the advancement was 0.9 mm was carried out with four Champy metallic minis- (three turns) per day. With the range of the tem- poral distractor being 0.5 mm, the advancement was 1 mm (two turns) per day. Both frontal dis- tractors were advanced to their maximum range (20 mm). Advancement of the temporal distrac- tion devices was stopped when an occlusal over- correction or a class I occlusion was obtained, which took up to 35 days. At the end of the dis- traction period, the flexible activation rods of the devices were cut or left intact, depending on the tolerance of the devices. A minor inflammatory reaction around the pins was commonly observed in most patients. The consolidation phase was modified during the study. In the first six patients, the devices were left in place for less than 5 months (3 to 4 months). Subsequently, the devices were left in place at least 6 months, because an immediate relapse was ob- served in a few patients after removal of the de- vices. A consolidation period of 6 months was Fig. 1. Design of osteotomy with distractors. (A) Frontal distrac- thought to reduce the risk of immediate relapse. tors and (B) temporal distractors. The removal of the devices required a coronal

1011 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 2. (Left) Operative view and (right) postoperative lateral radiograph showing parallel distractors in place. approach in most cases, but in a few instances, surgery and patients undergoing secondary sur- temporal incisions were sufficient. gery.

Evaluations Evaluation of Improvement With the study being prospective, some sub- The achievement of correction was evaluated groups were defined according to the duration of clinically by the degree of exorbitism and by the follow-up. The assessment of complications re- occlusal relationship. The respiratory status if pre- lated to the procedure, the degree of the achieved viously impaired was also evaluated by polysom- advancement, and the importance of relapse were nography. With the improvement being obtained evaluated for each subgroup. progressively during the distraction phase, but with significant initial swelling, the evaluations Complications were carried out later, at two principal dates, as Complications after frontofacial monobloc ad- detailed on the evaluation chronologic protocol: vancement were defined as follows: Early evaluation: This evaluation corresponded to Immediate complications: Before distraction was ini- the result at the time of removal of the distrac- tiated (group A, n ϭ 36, corresponding to the tors. Twenty-four of 35 had undergone primary latency period). surgery (subgroup E1) and 11 had undergone Distraction complications: During the distraction secondary surgery (subgroup E2). A radio- phase (group D, n ϭ 35). graphic assessment of reossification was also Postdistraction complications: After distraction was carried out at that time. completed, until the removal of distractors Late evaluation: Six months after the distractors (group pD, n ϭ 35, corresponding to the con- were removed, the same clinical and radio- solidation phase). graphic assessments were carried out. Three Late complications: During the 6 months after re- patients were completely lost to follow-up. Thirty- moval of distractors. Three patients were lost to two were available for respiratory assessment. follow-up, which explains why this group is ϭ smaller (n 32). This period started at the Evaluation of Relapse time of distractor removal with the early evalu- We defined relapse as the loss of advancement ation and ended 6 months later, when the late occurring within the first 6 months of the removal evaluation was carried out. of the distractors. The assessment of relapse was Comparisons were made in each group be- determined by comparing clinically the early and tween subgroups of patients undergoing primary late evaluations (both early and late evaluations

1012 Volume 120, Number 4 • Frontofacial Monobloc Advancement were obtained in 32 patients). In this subgroup of the leakage did not subside spontaneously after 72 patients, a comparison of relapse was carried out hours after surgery (two of five patients with ce- between the subgroup of patients in whom the rebrospinal fluid leaks). Of these five patients, two distractors had been left in place for less than 5 were primary cases (two of 24 primary) and three months (n ϭ 4) and those in whom the distrac- were secondary cases (three of 11 patients). This tors were left in place for more than 6 months difference of occurrence of cerebrospinal fluid (n ϭ 28). Ossification of the coronal gap and leak between primary and secondary patients was zygomatic gap created by distraction was also obviously not significant. Mucous secretions orig- analyzed with three-dimensional computed to- inating from the mucosal cuts were present in mographic scans at the time of distractor re- almost all patients but should not be misdiagnosed moval and 6 months later. as cerebrospinal fluid leaks, because they had usu- ally resolved within 3 days of surgery. RESULTS Distraction Complications In all children in whom distraction was per- Of the 35 patients who underwent the distrac- formed, frontofacial monobloc advancement led tion protocol, three experienced problems with to improvements of the preexisting condition at the devices requiring immediate reoperation. The the orbital and/or at the occlusal level, even if a problems during the active phase of distraction complication occurred. If a reoperation was nec- were related mainly to mechanical deficiencies of essary, or if distraction had to be interrupted be- the devices, as shown in Table 1. These problems cause of a complication, some improvement was occurred during the first half of the study (devel- still obtained. opmental phase) and did not occur later. A device rod break occurred in two primary patients (two Evaluation of Complications of 140 devices), and one fixation failure occurred Immediate Complications in one secondary patient. They required immedi- One patient died 10 hours after uneventful ate reoperation to replace the device or its fixa- operation as a result of an acute tonsillar hernia- tion. The distraction could then be continued un- tion associated with major brain edema. This was til completion. most likely attributable to a preexisting Chiari mal- An infection of one device occurred in one formation combined with an intracerebral hema- primary patient during the active phase of distrac- toma caused by a vascular drainage abnormality. tion and required removal of the device and aban- This sole major immediate complication occurred donment of distraction. Only partial improvement in the first hours of the intensive care unit stay in was obtained in this patient, with a better improve- a 4.5-year-old patient who had suffered from ment at the orbital level than at the maxillary level. chronic raised intracranial pressure despite a pre- During the active phase of distraction, all early vious attempt at skull vault decompression by an- complications occurred evenly in both primary other team 2 years previously. This major dramatic and secondary cases (Table 1), mainly in the first complication [one of 36 (3 percent)] was not di- half of our operative experience. It led to a sig- rectly linked to the distraction process. nificant rate of reoperation during the distraction The subsequent group of 35 patients (group phase of 20 percent. Only in the case of device D) was analyzed prospectively. In five of 35 pa- infection was distraction abandoned [one of 35 (3 tients, a genuine cerebrospinal fluid leak occurred percent)]. immediately after surgery (14 percent). Lumbar Uneven distraction occurred in three patients drainage was not always used but was indicated if (two primary cases and one secondary case), re-

Table 1. Complications No. Device Failure Device Infection Until 2003 After 2003 Device complications during distraction phase Primary 24 2 1 2 1 Secondary 11 1 0 1 0 Uneven Frontal Frontal Delayed Late No. Distraction Osteitis Necrosis Leakage Infection Total p Complications according to pathology Pfeiffer 8 2 0 1 1 1 5 0.05 Others 27 1 1 0 0 1 3

1013 Plastic and Reconstructive Surgery • September 15, 2007 quiring a second operation to correct the axis of One patient with Pfeiffer syndrome was diag- the face by using a transfacial pin. The occurrence nosed with a recurrent cerebrospinal fluid leak of uneven distraction that required a second op- after an initial cerebrospinal fluid leak had re- eration seemed to be age-related, because this oc- solved spontaneously. In this patient, an eth- curred among the youngest patients, those moidal pseudomeningocele was suspected, and a younger than 18 months. Conversely, none of the permanent lumboperitoneal shunt solved the older patients presented with this problem. The problem (this corresponded to the third lumbar difference between the age groups was significant drainage in the series). Ͻ (p 0.02). Outcome of Infections Related to Previous Therefore, distraction was completed unevent- Surgical Treatment fully in 28 of 35 patients (80 percent). In six of The major infection that led to loss of the seven patients, distraction could be completed af- frontal bone occurred in a secondary case. How- ter revision surgery was performed secondarily. ever, because of the size of the samples, the dif- Therefore, the total number that completed that ference was not significant. protocol was 34 of 35 patients (97 percent). Analysis of Major Complications Related to Postdistraction Complications Previous Surgical Treatment The most common complications during the All major complications requiring a corrective retention phase were infections. Abscesses of the procedure (frontal bone loss, pseudoencephalo- forehead region occurred in two patients requir- cele, and delayed permeability of the anterior ce- ing drainage. One patient, who had undergone rebral fossa) occurred in patients in whom the multiple operations in the past (frontoorbital ad- frontofacial monobloc advancement was not the vancement, Le Fort III), presented with osteone- primary procedure, except in one case of partial crosis of the entire frontal bone that necessitated resorption of the forehead in a primary patient. its removal 2 months after an uneventful distrac- This difference was significant (p ϭ 0.05). tion had been completed. In one other patient, an Analysis of Complications Related to the infection of the cranial distractor necessitated its Underlying Abnormality removal. This preceded an abscess and a partial By compiling all complications (except device osteitis of the frontal bone. In this latter case, the failures) and dividing groups according to the sequelae of the infection were less severe, leading underlying abnormality, it appeared that most only to a partial resorption of the forehead. The (uneven distraction, osteitis, forehead necrosis, infection rate during the consolidation phase was late infection, and delayed cerebrospinal fluid 6 percent, and the rate of forehead loss was 3 leak) occurred in cases of Pfeiffer syndrome (five percent (one secondary case). of eight) compared with the other faciocraniosyn- A minor inflammatory reaction limited to the ostosis patients (three of 27). This difference was orbital region occurred in six patients during the statistically significant (Table 1) (p ϭ 0.05). retention phase that was successfully managed with antibiotics alone. A painless limitation of buc- cal opening was found (very commonly) in half of Assessment of Distraction Results at the End of the patients, which was treated conservatively by the Consolidation Period daily physiotherapy. In two patients, the period The degree of advancement obtained by the required after completion of distraction to recover procedure was evaluated at the time of device a normal incisor distance was 8 months. removal (early evaluation). This early evaluation Late Complications was based on the clinical correction of exorbitism, A late subcutaneous infection in the frontal respiratory impairment, and occlusal status. All 35 region occurred 1 month after retrieval of the patients were also evaluated radiographically. distraction devices. This patient, who had un- Early Evaluation: At the Time of Distractor dergone multiple previous operations with Removal Pfeiffer syndrome (one monobloc, one fron- In patients who completed the distraction pro- toorbital advancement, one Le Fort III, and one cess to the maximum range of 20 mm, a complete cranioplasty), developed an abscess a few days correction of exorbitism was achieved (Figs. 3 and after he blew his nose forcefully. During the 4, above and center). In the remaining patients who operation, it seemed that nonvascularized bone had sustained an infectious complication leading from the previous cranioplasty (autogenous to an interruption of the process, an improvement split ribs) was the nidus of infection. at the orbital level was nevertheless achieved.

1014 Volume 120, Number 4 • Frontofacial Monobloc Advancement

Fig. 3. Early result in a true monobloc in a 7-month-old Pfeiffer syndrome patient. (Above) Before distrac- tion. (Below) Four months after distraction.

Respiratory improvement was obtained in all stage in the coronal gap, and never present at the patients but two (14 of 16). As a result of this, four zygomatic level (Fig. 4, center and below). of six patients with a tracheostomy were decan- nulated (some of them being decannulated after Assessment of Relapse and Reossification removal of distractors, to make the second anes- A late evaluation was carried out 6 months thesiology management simpler). The respiratory after early evaluation, using the same criteria. To status of the remaining 11 patients improved by assess the stability of the achieved advancement, enlargement of the airways. As a consequence, the results of the early and late evaluations were sleep apnea improved (Table 2). compared with each other. This double evaluation Twenty-eight patients (80 percent) achieved a was obtained in only 32 patients, because three class I occlusal relationship at the time of removal patients were lost to follow-up as a result of geo- of the distractor devices. In seven patients, the graphic remoteness (such as the Pacific Islands, maxillary advancement was incomplete: three pa- with limited possibilities of communication), in- tients achieved only a dental alignment, and in the cluding the youngest patient in the series (Figs. 3 four remaining patients a class III malocclusion and 4), who was from South America. Among the was retained. subgroup of 32 revised patients, 21 had no surgical On three-dimensional reconstruction, in all intervention before the frontofacial monobloc ad- patients, the reossification was very limited at this vancement, whereas 11 patients had undergone

1015 Plastic and Reconstructive Surgery • September 15, 2007

previous surgery to the anterior skull vault. Among those 32 patients available for double evaluation, four patients kept the distractors in place less than 5 months. In the remaining 28 patients, the con- solidation phase lasted at least 6 months. The re- sults of the comparison were as follows: 1. The correction of exorbitism was evaluated clinically and considered stable in all pa- tients except in a Pfeiffer syndrome patient who had been operated on previously in whom the consolidation period was only 3 months (Figs. 5 through 7). 2. The respiratory status was stable between early and late evaluation in all patients (Ta- ble 2), except for the same Pfeiffer syn- drome patient (patient 2 in the series) who sustained a relapse at all levels of the face back to the original relationship, requiring eventually a tracheostomy (Fig. 8). 3. In all controlled patients, there was a lack of complete ossification in the coronal osteot- omy gap between the distracted frontal seg- ments on three-dimensional computed to- mographic scan reconstruction at 6-month follow-up (Figs. 9 through 13). Some mar- ginal reossification occurred between the bony edges, but the bony link was limited to the tongue and groove of the upper osteot- omy. Even in the 7-month-old Pfeiffer syn- drome patient who had a true monobloc osteotomy, there was no ossification in the coronal gap at the time of removal of dis- tractors (Fig. 4, below). There was also a poor reossification in the zygomatic osteotomy (Fig. 12, right). 4. The correction of occlusion deteriorated in six patients, with an evolution from class I to an end-to-end (class III) relationship. Exact measurements of the relapse were not avail- able because of the difficulty of clinical as- sessments at young ages. The end-to-end re- lationship was considered as a recurrent class III (Figs. 14 and 15).

DISCUSSION The principle of the simultaneous correction of the frontal and facial retrusion as a single-stage procedure is certainly satisfying, but the high mor- Fig. 4. Computed tomographic scans of the patient shown in Fig- bidity of the classic frontofacial advancement pro- ure3.(Above)Beforedistraction(lateralview).(Center)Threemonths cedure (without distraction) outweighs the after distraction. Observe the lack of bony reossification at the time benefits.3–6 As a consequence, most teams have of distractor removal. (Below) Six months after distraction (i.e., 3 restricted or even abandoned its use.15,34 Some months after removal of distractors). Observe the limited reossifica- authors have pointed out the detrimental role of tion despite true monobloc design in a young patient. previous shunting6 and the low risks of the classic

1016 Volume 120, Number 4 • Frontofacial Monobloc Advancement

Table 2. Evaluation of Respiratory Status after Frontofacial Monobloc Advancement Patient Condition I/II Resp-Pre Resp-EE Resp-LE 1 P I 80 N Lost 2P IIϽ80 N Tracheostomy 3 C I Snore N N 4 C I Snore N N 5 C I 90 N Lost 6 C I Snore N N 7 P II 82 N Snore 8 A I Snore N N 9CINNN 10 A I Snore N N 11 A I Tracheostomy N N 12 C II Ͻ80 N N 13 C I Snore N N 14 C I Ͻ80 N N 15CINNN 16CIINNN 17 P II 85 N N 18CINNN 19 C I 90 N N 20 C II Tracheostomy Tracheostomy Tracheostomy 21 A I Snore N Snore 22 P II Tracheostomy N N 23 A I Snore N N 24 P I Tracheostomy Tracheostomy Lost 25 C II Snore N N 26AINNN 27 C I Snore N N 28 C I Snore N N 29 C I Ͻ85 N N 30 Other II N N N 31 P II 90 N N 32 C I Snore N N 33 C I Tracheostomy N ϩ TN 34 C I Tracheostomy N ϩ TN 35 C II Snore N N Resp-Pre, respiratory status before snore; Resp-EE, respiratory status at the time of removal of distractors; Resp-LE, respiratory status 6 months after removal of distractors; P, Pfeiffer syndrome; C, Crouzon syndrome; A, Apert syndrome; I, primary status; II, secondary status; N, normal; N ϩ T, tracheostomy to be removed soon because of normal results (results are indicated in percentage of oxygen night measurements). procedures, but our experience was quite oppo- obtained in all patients in whom distraction had site: in our center (like in some others), the classic been initiated. The advancement of 20 mm approach of frontofacial monobloc advancement achieved by our cranial distractor was usually suf- had led to an unacceptable 30 percent rate of ficient and corresponded to the fronto-orbital ad- complications. Since 2000, the morbidity in our vancement of the classic procedure performed by study, although still significant, has decreased dra- our team. The temporozygomatic distractor has matically. Moreover, in our series, none of the fewer limitations, as it can distract up to 30 mm in previously shunted patients experienced compli- our pediatric model and 40 mm in the adult ver- cations with the combination of frontofacial sion. There is little doubt that the gradual ad- monobloc advancement and distraction. The ap- vancement obtained by distraction limits the ret- plication of distraction techniques in the field of rofrontal dead space,35 allows progressive anterior craniofacial surgery broadened the spectrum of expansion of the brain to occur, and therefore surgical modalities, especially by decreasing sur- reduces complications. One of our main indica- gical morbidity and increasing efficacy. Our ex- tions for early frontofacial monobloc advance- perience with monobloc distraction certainly con- ment with distraction is correction of upper airway firms this observation. The morbidity associated respiratory problems linked to faciocraniosynos- with frontofacial monobloc advancement with dis- tosis. Significant obstructive airway problems were traction could not be completely eliminated but encountered in half of our patients. It is our feel- occurred less often than in the classic frontofacial ing that, in the past, these respiratory problems monobloc advancement without distraction. might have been underestimated, because the Dealing with the correction of exorbitism and polysomnographic studies were not part of our maxillary retrusion, a significant improvement was routine preoperative evaluation. Subsequently, we

1017 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 5. A 1.2-year-old Pfeiffer syndrome patient treated secondarily with 4 months’ consolidation. (Above) Before distraction. (Below) After distraction. have found that almost 40 percent of our patients hypothesized that the acute increase in intracra- present with respiratory impairment.36 The fronto- nial pressure was triggered by a minor intracere- facial monobloc advancement with distraction bral hematoma in a patient with a preexisting presents a solution for these young patients with venous drainage malformation. Subsequently, we chronic hypoxemia in whom fronto-orbital ad- have included in our protocol the surgical release vancement is indicated early in life.37 of the foramen magnum whenever any doubt of The complications that occurred could be di- tonsillar herniation was present before any treat- vided in several categories according to the phase ment. Intraoperatively, we also perform an imme- of the treatment protocol. Some of these resolved diate 5-mm advancement of the forehead to limit with experience. Among the immediate compli- the risk of postoperative intracranial hyperten- cations, the death that occurred in the first 10 sion. This immediate advancement might contrib- hours after an uneventful procedure is extremely ute to the reduction of osteogenesis in the dis- regrettable. The exact cause of death remains un- traction sites, in comparison with other authors,31 clear in this patient who had suffered chronic but we consider the immediate skull pressure re- intracranial hypertension. Acute intracranial hy- lease as a vital priority, even if it partially compro- pertension occurred while the patient was still in- mises some bony reossification, which can be com- tubated in the intensive care unit. It has been pensated for by a longer consolidation period.

1018 Volume 120, Number 4 • Frontofacial Monobloc Advancement

Fig.6. (Left)RadiographofthepatientshowninFigure5,takenattheendofdistraction.(Right)Computed tomographic scan taken at the end of distraction.

where cerebrospinal fluid leakage persisted, a transient external lumbar drain was placed as a safety precaution, and the beginning of distrac- tion was delayed. Despite a delay of up to 15 days, distraction could still be performed. During the active phase of distraction, the complications were linked mainly to the devices, especially in the early stages of our study. However, recent progress in the development of the distrac- tion devices has helped to minimize these prob- lems. Rigid fixation of the distractors should be performed preferably with metallic screws with this generation of devices. However, resorbable screws have been used successfully in the temporal region for our temporozygomatic distractor in Le Fort III osteotomies since 1999.22 Using our cra- nial distraction devices with autoretentive hooks, Fig. 7. Lateral view of the patient shown in Figures 5 and 6, 1 less forces are required and a partially resorbable year after removal of distractors. Observe the relapse of facial fixation system should be available in the near retrusion. future. To limit infection during the distraction phase, particular attention should be paid to local wound care, especially to the activation rods of the devices, because progression of an infection can Cerebrospinal fluid leakage was observed less be detrimental. Frontofacial monobloc advance- commonly in the patients who had not previously ment results in an unavoidable bacteriologic con- undergone surgery of the anterior craniofacial tamination of temporarily placed implants until skeleton, although the difference was not statisti- their removal. This is particularly critical in pa- cally significant. Obliteration of the anterior ce- tients who have undergone prior surgery, who may rebral fossa/nasal cavity junction with bilateral harbor fragments of poorly vascularized bone pedicled periosteal flaps might be beneficial to grafts. Minor inflammatory reactions at the pin prevent infection and leakage. Cerebrospinal sites were common. Bacteriologic cultures from fluid leakage is not regarded by our neurosurgical pin sites were regularly performed on a systematic colleagues as a major problem, and the minor basis even without signs of infection, but antibiotic leaks ceased spontaneously within 72 hours with- treatment was only indicated if an extensive in- out requiring any treatment. In the few cases flammatory reaction occurred. There was discus-

1019 Plastic and Reconstructive Surgery • September 15, 2007

Fig.8. (Above)PolysomnogramofthepatientshowninFigures5through7,show- ing normalized night oxygen level at the end of the consolidation phase. Observe the stable baseline between 95 and 100 percent of oxygen. (Below) Polysomno- gram demonstrating abnormal night oxygen level 1 year after removal of distrac- tors. Observe the drops in oxygen level as low as 75 percent.

sion about preventive prolonged antibiotic ther- During the retention phase, we faced a severe apy, but it was not integrated into our routine infectious complication resulting in the complete protocol. frontal bone loss in one patient who had under- In the few patients in whom the distraction gone multiple previous operations. In another pa- had to be interrupted before completion, the sur- tient, a partial resorption attributable to osteitis gical result was better at the orbital than at the also necessitated a secondary procedure to re- maxillary level. Advancement at the maxillary level move infected bone fragments. In both cases, a is often more difficult to obtain. Correction of the significant improvement was nevertheless ob- maxillary retrusion was also less satisfactory in tained at the maxillary and orbital levels. Reduc- the secondary operation, probably as a result of ing the rate of distraction from 1 mm per day to the restrictive forces of the soft-tissue envelope 0.5 mm per day would probably minimize the risks caused by scarring. In selected cases of secondarily but would increase the time of distraction. The treated patients, a transfacial pin was used con- obturation of the communication between the na- comitantly to stabilize the midface in the horizon- sal cavity and the cerebral anterior fossa would tal plane. Despite a complete pterygomaxillary dis- certainly minimize the infection risk. We advocate junction, the mobilization of the skeleton could be the use of a pericranial pedicled flap or a galeal incomplete in patients younger than 18 months. flap as part of a routine procedure, which can be In these cases, a transfacial pin might be indicated easily performed by elevation of the frontal bony routinely to allow a more efficient advancement flap. The true monobloc osteotomy could theo- and to avoid collapse of the facial skeleton, which retically limit the infection risk, because the fore- would result in uneven distraction. However, this head remains vascularized31 but does not allow was not necessary in all patients younger than 18 sufficient space for the suture of the flaps in the months. Distraction could easily be performed in retrofrontal area. This vascularization no longer patients as young as only 7 months, provided ad- exists in secondarily treated patients in whom an juvant rigid fixation (preferably resorbable) was osteotomy at the level of the supraorbital bar had performed at the frontozygomatic junction to re- already been performed and which represented a inforce the less solid skeleton.38 high-infection-risk group. It is in these secondarily

1020 Volume 120, Number 4 • Frontofacial Monobloc Advancement

Fig. 10. View of the patient shown in Figure 9, 3 years after re- moval of distractors.

treated patients in whom the brain was less likely to reexpand that the true monobloc is no longer possible because of the previous osteotomy line, which is usually poorly reossified. In addition, the true monobloc does not allow reshaping of the forehead, which is often necessary, especially in prominent forms of brachycephaly, as in syn- dromic patients. By detaching the forehead com- pletely, a tiny bilateral triangular resection of both lateral parts of the inferior edge of the forehead flap can be performed. Inferior fixation of the forehead to the supraorbital bar with metallic wires only and posterior trimming limited the ret- rofrontal dead space32 and allowed the forehead to self-correct. Depending on the clinical situation, one has to discuss the use of internal versus external distractors to provide the best distraction for patients. The external device has the advantage of a greater versatility of vectors during the dis- traction phase, and the simplicity of removal. It has gained wide acceptance, and promotors of external distractors have reported quite satis- factory results with the use of the rigid external distraction system.37–40 In our unit, internal de- vices have been used since the very beginning because they were more applicable in our Fig. 9. Stable result in a 3-year-old Pfeiffer patient with an youngest patients, those younger than 1 year. 8-month consolidation phase and a 3-year follow-up. (Above) Be- There is little doubt that at this young age, an fore distraction. (Center) After distraction. (Below) Six months af- external device, even reduced in size, is inade- ter removal of distractors. quate. An additional advantage is that the con-

1021 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 11. (Left) Before distraction. (Right) After distraction.

Fig. 12. (Left) Six months after removal of distractors. (Right) Three years after removal of distractors. solidation phase can be extended as needed. after a frontofacial monobloc advancement, Immediate relapse after removal of the distrac- which made us consider increasing the reten- tion devices occurred in a secondarily treated tion phase up to at least 6 months. Such a long patient with Pfeiffer syndrome who underwent consolidation phase makes the use of external a complete anterior cranial vault reconstruction distraction device less practical, although the of the supraorbital bar at the same time as the achievement of correction is in theory equiva- monobloc. Exophthalmus recurred, and respi- lent between internal and external devices. Nev- ratory impairment was confirmed by polysom- ertheless, Fearon has recently confirmed that, nography. The relapse may have been related to for Le Fort III advancement, a short consolida- a too-short consolidation phase of 4 months, tion phase of 4 weeks was sufficient to ensure which did not allow reossification in the cranial stability using a rigid external distraction vault to occur. The coronal gap created by dis- device.41 To the best of our knowledge, no study traction is a critical zone for achieving stability has yet been published to compare internal ver-

1022 Volume 120, Number 4 • Frontofacial Monobloc Advancement

Fig. 13. Lateral computed tomographic scans after distraction (left) and 6 months after distractor removal (i.e., 14 months after distraction has been completed; right). Observe the partial coronal reossification.

Fig. 14. (Left) Preoperative occlusion with upper retrusion of 15 mm. (Above, right) Occlusion at the end of distraction (class I relationship). (Below, right) Occlusion 3 years after removal of distractors. Relapse has occurred.

1023 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 15. (Left) Preoperative lateral radiographic view. (Center) Postdistraction lateral view. (Below) End-to-end class III relationship 3 years later.

sus external devices in frontofacial monobloc more prone to maxillary relapse. The monobloc advancement or Le Fort III advancement. The can neither solve these problems nor correct a use of a double pair of distractors in our patients diminished vertical height of the midface. Ad- allowed simultaneous advancement at two dif- ditional surgery will be necessary in these chil- ferent levels of the face: the orbital and maxil- dren, because normal growth does not occur in lary levels. The two different vectors compen- faciocraniosynostosis, and a genetically pro- sated for the lower versatility in comparison with grammed deterioration of the results will be the external devices. unavoidable until adulthood. Moreover, some The data from this study showed that an of the faciocraniosynostosis patients present early frontofacial monobloc advancement using with smaller than normal mandibles. internal distraction devices is a feasible solution for children who present with respiratory prob- CONCLUSIONS lems. Although a second operation for removal Larger series and additional long-term results of internal devices represents a drawback com- will confirm whether these results using frontofa- pared with the external devices, the overall ben- cial monobloc advancement with distraction can efits outweigh the disadvantages. We believe be improved by modifying the devices. In sum- that, in the near future, the second step may no mary, the early frontofacial monobloc advance- longer be necessary because partially resorbable ment represents a valid surgical technique and a devices will provide enough strength during the powerful tool with which to improve respiratory active phase of distraction. In the neonatal pe- impairment and exorbitism related to faciocra- riod, the use of springs may present an additive niosynostosis. The overall complication rate is sig- surgical option in early frontofacial monobloc nificantly less than with a standard monobloc pro- advancement.42 Relapse occurred mainly at the cedure without distraction, especially in patients maxillary level. Patients presenting with a pre- treated for the first time and with a long consol- operative open bite, especially with a severely idation period. Patients with Pfeiffer syndrome or retruded and posteriorly rotated maxilla, were those who have undergone multiple previous op-

1024 Volume 120, Number 4 • Frontofacial Monobloc Advancement erations should be managed more cautiously be- 12. Tessier, P. The monobloc frontofacial advancement: Do the cause of the higher risk of complications but cer- pluses outweigh the minuses? (Discussion). Plast. Reconstr. Surg. 91: 988, 1993. tainly should not be excluded from frontofacial 13. Marchac, D., and Renier, D. (Eds.). Craniofacial Surgery for monobloc advancement with distraction. Craniosynostosis. Boston: Little, Brown, 1982. 14. Persing, J. A., Jane, J. A., and Edgerton, M. T. Surgical treat- Eric Arnaud, M.D. ment of craniosynostosis. In J. A. Persing, M. T. Edgerton, Unite´ de Chirurgie Craˆnio-Faciale and J. A. Jane (Eds.), Scientific Foundations and Surgical Treat- Hoˆpital Necker ment of Craniosynostosis. Baltimore: Williams & Wilkins, 1989. 130 rue de la Pompe Pp. 117–238. Paris 75116, France 15. Marchac, D., and Arnaud, E. Midface surgery from Tessier to [email protected] distraction. Childs Nerv. Syst. 15: 681, 1999. 16. McCarthy, J. G., Schreiber, J., Karp, N., Thorne, C. H., and Grayson, B. H. Lengthening of the human mandible by ACKNOWLEDGMENTS gradual distraction. Plast. Reconstr. Surg. 89: 1, 1992. Dr. M. P. Morisseau-Durand, Dr. E. Mireau, and 17. Molina, F., and Ortiz-Monasterio, F. Mandibular elongation Dr.P.Gue´rin (Paris) are thanked for their help in and remodeling by distraction: A farewell to major osteoto- mies. Plast. Reconstr. Surg. 96: 825, 1995. providing polysomnographic studies. Dr. Bianca Knoll 18. Marchac, D., and Arnaud, E. La distraction du maxillaire (United States), Dr. Greg O’Toole (United Kingdom), supe´rieur. Ann. Chir. Plast. Esthet. 42: 557, 1997. and Dr. Hop Le (United States), fellows in the unit, are 19. Diner, P. A., Kollar, E. A., Martinez, H., and Vazquez, M. P. thanked for their help in preparing the article. Submerged intraoral device for mandibular lengthening. J. Craniomaxillofac. Surg. 25: 116, 1997. 20. Chin, M., and Toth, B. A. Le Fort III advancement with DISCLOSURE gradual distraction using internal devices. Plast. Reconstr. Surg. 100: 819, 1997. None of the authors has a financial interest in the 21. Polley, J. W., and Figueroa, A. A. The management of cleft distractors produced by Martin-Medizin (Tuttlingen, maxillary hypoplasia with the RED device. Proceedings of the 1st Germany). International Congress on Cranial and Facial Bone Distraction Processes, Paris, France, June 19–21, 1997. Pp. 255–260. 22. Arnaud, E., Marchac, D., and Renier, D. Complications of REFERENCES midface distraction in children and modification by internal 1. Tessier, P. The definitive plastic surgical treatment of the device with transfacial pin. Proceedings of the 2nd International severe facial deformities of craniofacial dysostosis: Crouzon’s Congress on Cranial and Facial Bone Distraction Processes, Paris, and Apert’s diseases. Plast. Reconstr. Surg. 48: 419, 1971. France, June 17–19, 1999. Pp. 211–215. 2. Ortiz-Monasterio, F., Fuente del Campo, A., and Carillo, A. 23. Polley, J. W., Figueroa, A. A., Charbel, F. T., Berkowitz, R., Advancement of the orbits and the midface in one piece, Reisberg, D., and Cohen, M. Monobloc craniomaxillofacial combined with frontal repositioning for the correction of distraction in a newborn with severe craniofacial synostosis: Crouzon’s deformities. Plast. Reconstr. Surg. 61: 507, 1978. A preliminary report. J. Craniofac. Surg. 6: 421, 1995. 3. Whitaker, L. A., Munro, I., Salyer, K. E., Jackson, I. T., Ortiz- 24. Cohen, S. R., Boydston, W., Burstein, F. D., and Hudgins, R. Monasterio, F., and Marchac, D. Combined report of prob- Monobloc distraction osteogenesis during infancy: Report of lems and complications in 793 craniofacial operations. Plast. a case and presentation of a new device. Plast. Reconstr. Surg. Reconstr. Surg. 64: 198, 1979. 101: 1919, 1998. 4. David, D. J., and Cooter, R. D. Craniofacial infection in 10 years 25. Arnaud, E., Marchac, D., and Renier, D. Avancement fronto- of transcranial surgery. Plast. Reconstr. Surg. 80: 213, 1987. facial pre´coce avec distraction pour faciocranioste´nose chez 5. Fearon, J. A., and Whitaker, L. A. Complications with facial l’enfant. Ann. Chir. Plast. 46: 268, 2001. advancement: A comparison between the Le Fort III and 26. Nadal, E., Dogliotti, P., Rodriguez, J. C., and Zuccaro, G. monobloc advancement. Plast. Reconstr. Surg. 91: 990, 1993. Craniofacial distraction osteogenesis en bloc. J. Craniofac. 6. Kawamoto, H. Complications of the monobloc frontofacial Surg. 11: 246, 2000. advancement. In Proceedings of the 67th Congress of the American 27. Raposo de Amaral, C. M., Buzzo, C. L., Rinco, T., Bueno, M. Plastic Surgery Society, May 3, 1988. A. C., Turchiari, L. A. B., and Raposo de Amaral, C. E. Long 7. Anderl, H., Muhlbauer, W., Twerdy, L., and Marchac, D. term follow-up: Report of 17 cases of craniosynostosis. In K. Frontofacial advancement with bony separation in craniofa- Salyer (Ed.), Proceedings of the 10th International Society for cial dysostosis. Plast. Reconstr. Surg. 71: 303, 1983. Craniofacial Surgery, Monterrey, California, 2003. Bologna: 8. Jackson, I. T., Adham, M. N., and Marsh, W. R. Use of the Medimond, 2004. Pp. 81–84. galeal frontalis myofascial flap in craniofacial surgery. Plast. 28. Arnaud, E., Marchac, D., and Renier, D. Quadruple internal Reconstr. Surg. 77: 905, 1986. distraction with early frontal-facial advancement for facio- 9. Fisher, J., and Jackson, I. T. Microvascular surgery as an craniodysostosis (in French). Rev. Stomatol. Chir. Maxillofac. adjunct to craniomaxillofacial reconstruction. Br. J. Plast. 105: 13, 2004. Surg. 42: 146, 1989. 29. Arnaud, E., Marchac, D., and Renier, D. Evaluation of qua- 10. Salyer, K. E., Hall, C. D., and Joganic, E. F. Lamellar split druple internal distraction with monobloc advancement in osteotomy: A new craniofacial technique. Plast. Reconstr. Surg. infants. In E. Arnaud and P. A. Diner (Eds.), Proceedings of the 86: 845, 1990. 4th International Congress on Cranial and Facial Bone Distraction 11. Wolfe, S. A., Morrison, G., Page, L. K., and Berkowitz, S. The Processes, Paris, France, July 3–6, 2003. Pp. 455–460. monobloc frontofacial advancement: Do the pluses outweigh 30. Arnaud, E., Marchac, D., and Renier, D. Quadruple internal the minuses? Plast. Reconstr. Surg. 91: 977, 1993. distraction with monobloc advancement: Experience with 20

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cases. In K. Salyer (Ed.), Proceedings of the 10th International ternational Congress on Cranial and Facial Bone Distraction Society for Craniofacial Surgery. Monterey, California, 2003. Processes, Paris, France, June 14–16, 2001. Pp. 489–493. Bologna: Medimond, 2004. Pp. 77–79. 37. Polley, J. W. Monobloc distraction osteogenesis in pediatric 31. Molina, F. From midface distraction to the “true mono- patients with severe syndromal craniosynostosis (Discus- block”. Clin. Plast. Surg. 31: 463, 2004. sion). J. Craniofac. Surg. 15: 1001, 2004. 32. Denny, A. D., Kalantarian, B., and Hanson, P. R. Rotation 38. Shin, J. H., Duncan, C. C., and Persing, J. Monobloc distrac- advancement of the midface by distraction osteogenesis. tion: Technical modification and considerations. J. Craniofac. Plast. Reconstr. Surg. 111: 1789, 2003. Surg. 14: 763, 2003. 33. Saltz, R., Sierra, D., Feldmann, D., Saltz, M. B., Dimick, A., 39. Nishimoto, S., Oyama, T., Shimizu, F., et al. Fronto-facial monobloc advancement with rigid external distraction and Vasconez, L. Experimental and clinical applications of (RED-II) system. J. Craniofac. Surg. 15: 54, 2004. fibrin glue. Plast. Reconstr. Surg. 88: 1005, 1991. 40. Meling, T. R., Due-Tonnessen, B. J., Hogevold, H. E., Skjel- 34. Whitaker, L. A., Broennle, A. M., Kerr, L. P., and Herlich, A. bred, P., and Arctander, K. Monobloc distraction osteogen- Improvements in craniofacial reconstruction: Methods evolved esis in pediatric patients with severe syndromal craniosynos- in 235 consecutive patients. Plast. Reconstr. Surg. 65: 561, 1980. tosis. J. Craniofac. Surg. 15: 990, 2004. 35. Posnick, J., Al-Qattan, M., and Armstrong, D. Monobloc and 41. Fearon, J. Halo distraction of the Le Fort III in syndromic facial bipartition for reconstruction of craniofacial malfor- craniosynostosis: A long term assessment. Plast. Reconstr. Surg. mations: A study of extradural dead space and morbidity. 115: 1524, 2005. Plast. Reconstr. Surg. 97: 1118, 1996. 42. Gewalli, F., da Silva Guimaraes-Ferreira, J. P., Maltese, G., 36. Mireau, E., Arnaud, E., Lajeunie, E., Marchac, D., and Re- Ortengren, U., and Lauritzen, C. Expander elements in nier, D. Improvement of upper airway obstruction in Crou- craniofacial surgery: An experimental study in rabbits. Scand. zon syndrome by facial distraction. Proceedings of the 3rd In- J. Plast. Reconstr. Surg. Hand Surg. 35: 149, 2001.

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1026 PEDIATRIC/CRANIOFACIAL

Treatment Outcomes of Orthodontic Treatment, Corticotomy-Assisted Orthodontic Treatment, and Anterior Segmental Osteotomy for Bimaxillary Dentoalveolar Protrusion

Jin-Kyung Lee, D.D.S., M.S.D. Background: The purpose of this study was to compare treatment outcomes of Kyu-Rim Chung, D.D.S., orthodontic treatment, anterior segmental osteotomy, and corticotomy-assisted M.S.D., Ph.D. orthodontic treatment for resolution of bimaxillary dentoalveolar protrusion. Seung-Hak Baek, D.D.S., Methods: The samples consisted of 65 Korean adult female patients with bi- M.S.D., Ph.D. maxillary dentoalveolar protrusion who had achieved a good treatment result Seoul, South Korea and were divided into group 1 (orthodontic treatment), group 2 (corticotomy- assisted orthodontic treatment with skeletal anchorage in the maxilla and an- terior segmental osteotomy in the mandible), or group 3 (anterior segmental osteotomy in the maxilla and mandible). The hard- and soft-tissue variables were measured from lateral cephalographic tracings at pretreatment and posttreat- ment stages. Statistic analyses were performed to compare differences in pre- treatment and change from pretreatment to posttreatment. Results: Group 3 showed the largest amount of basal bone retraction and the least amount of upper incisor inclination change and upper alveolar bone bending among the three groups. The amounts of change in the upper lip projection and angulation were greater in group 2 than in group 1. Group 3 showed a decrease of the upper incisal exposure, whereas group 1 showed an increase. Upper central incisor to Frankfurt horizontal plane, upper and lower alveolar ridge angle, Pog-N perpendicular, and anteroposterior dis- crepancy indicator were selected as significant variables for discriminating the three groups. Conclusions: The results of this study show that orthodontic treatment or corti- cotomy-assisted orthodontic treatment is indicated for those with severe incisor proclination with normal basal bone position, although corticotomy-assisted orth- odontic treatment can be advantageous for adult patients concerned with treatment duration. Anterior segmental osteotomy is recommended for bimaxillary dentoal- veolar protrusion patients with a gummy smile, basal bone prognathism, relatively normal incisor inclination, and relatively underdeveloped chin position. (Plast. Reconstr. Surg. 120: 1027, 2007.)

ttractive faces may range from slightly flat ment for correction of deformation.1 Bimaxillary (Apollonian) to mildly bimaxillary protru- protrusion is common in African American and Asive, but marked deviations in either direc- Asian populations.2,3 tion warrant orthodontic and/or surgical treat- There are two traditional methods to achieve these goals and to treat bimaxillary protrusion. From the Department of Orthodontics, School of Dentistry, The first is orthodontic treatment and the sec- Seoul National University Dental Hospital; private clinic; ond is anterior segmental osteotomy. and Department of Orthodontics, Institute of Dental Re- search, School of Dentistry, Seoul National University. Orthodontic treatment is the most common Received for publication January 11, 2006; accepted August way of treating bimaxillary protrusion. Recent 11, 2006. advances in orthodontic techniques, such as Copyright ©2007 by the American Society of Plastic Surgeons the orthodontic miniscrew, allow maximum an- DOI: 10.1097/01.prs.0000277999.01337.8b chorage and further simplify the procedure.4 How-

www.PRSJournal.com 1027 Plastic and Reconstructive Surgery • September 15, 2007 ever, structural changes such as a decrease in the PATIENTS AND METHODS cancellous bone volume and blood supply in The samples consisted of 65 Korean adult fe- adults can reduce the rate of tooth movement. male patients with bimaxillary protrusion who had To overcome the limitations of orthodontic received orthodontic treatment or anterior segmen- treatment, anterior segmental osteotomy is tal osteotomy at the Department of Orthodontics, sometimes recommended. Anterior segmental Seoul National University Dental Hospital, and cor- osteotomy can markedly reduce the treatment ticotomy-assisted orthodontic treatment at a local period over conventional orthodontic treat- orthodontic clinic (Seoul, Korea). These three treat- ment and achieve immediate improvement of ment methods were assigned randomly by the cli- the facial profile. This is one of the most at- nician’s decision regarding the same chief com- tractive advantages of anterior segmental os- plaint. Only women were selected, to exclude sexual teotomy for adult patients.5 Despite the appar- bias in the results. The sampling criteria for bimax- ent clinical success of anterior segmental illary protrusion were as follows: (1) Angle class I osteotomy, postoperative complications are as molar relationship, (2) no severe vertical discrep- Ͻ Ͻ follows: ischemic necrosis of the anterior seg- ancy (55.0 degrees overbite depth indicator ment, wound dehiscence at the osteotomy site, 85.0 degrees), (3) no severe anteroposterior skel- etal discrepancy (75.0 degrees Ͻ anteroposte- and devitalization of the teeth adjacent to the Ͻ osteotomy site.6 rior discrepancy indicator 97.0 degrees), (4) The most recent treatment method for bimax- crowding less than 3 mm, (5) Rickett’s aesthetic illary protrusion is corticotomy-assisted orth- line to lower lip distance greater than 2 mm, (6) odontic treatment with skeletal anchorage, interincisal angle less than 125 degrees, (7) chin point deviation less than 3 mm, and (8) no which was introduced as a compromise be- symptoms of temporomandibular joint disor- tween anterior segmental osteotomy and orth- der. The samples achieved a good treatment odontic treatment.7 It is more conservative to result, such as a pleasing soft-tissue profile and reduce the ischemic complications by cutting an Angle class I canine and molar relationship. only the cortical bone. Corticotomy allows for The samples were divided into three groups bending of the anterior bony segment by elim- according to treatment method (Table 1). Group inating the cortical bone when retraction force 1 samples (n ϭ 29) were treated with conventional is applied. orthodontic treatment and maximum anchorage Although there have been several studies on the using transpalatal arch and/or headgear. Group 2 treatment consequences of orthodontic treatment samples (n ϭ 20) were treated with corticotomy- and anterior segmental osteotomy on the correc- assisted orthodontic treatment and skeletal an- tion of bimaxillary protrusion,3,5,6,8 it is necessary to chorage (C-implant, Martin Co., Germany) in the investigate the treatment outcomes of corticotomy- maxilla, and with anterior segmental osteotomy in assisted orthodontic treatment on bimaxillary pro- the mandible. The reason why anterior segmental trusion. Therefore, the purpose of this study was to osteotomy was performed in the mandible is that compare the treatment outcomes of all three anterior segmental osteotomy in the mandible has methods on bimaxillary protrusion, which could a genioplasty effect that gives the best aesthetic provide a guideline for establishing the differential result. Group 3 samples (n ϭ 16) were treated with diagnosis and treatment plan for patients with bi- anterior segmental osteotomy in the maxilla and maxillary protrusion. mandible. We selected patients who were treated

Table 1. Sample Characteristics (16 ؍ Group 3 (n (20 ؍ Group 2 (n (29 ؍ Group 1 (n Multiple Mean SD Mean SD Mean SD Significance Comparison Age 25yr0mo 7yr1mo 28yr2mo 6yr9mo 25yr0mo 3yr5mo NS NS Treatment period, months 27 7 19 6 14 4 0.000 (1, 2)*, (1, 3)† Group 1, conventional orthodontic treatment; group 2, corticotomy-assisted orthodontic treatment in the maxilla and anterior segmental osteotomy in the mandible; group 3, anterior segmental osteotomy in the maxilla and mandible; NS, not significant. The differences in age and treatment period among groups were tested by one-way analysis of variance and verified with the Scheffe´ multiple comparison test: *p Ͻ 0.01; †p Ͻ 0.001.

1028 Volume 120, Number 4 • Bimaxillary Dentoalveolar Protrusion

Fig. 1. (Left) Hard-tissue landmarks: 1,S;2,N;3, Or; 4, Po; 5, Ar; 6, ANS; 7, PNS; 8,A;9, Sd; 10, U1E; 11, U1A; 12, L1E; 13, L1A; 14, Id; 15,B;16, Pog; 17, Gn; 18, Me; 19, Go. (Right) Soft-tissue landmarks: 20,N=; 21, Pn; 22, Cm; 23, Sn; 24,A= (Ss); 25, Ls; 26, UL; 27, Stms; 28, Stmi; 29, LL; 30, Li; 31,B= (Si); 32,Pm=; 33, Pog=. with the Wunderer method for the retraction of nification between Seoul National University Den- the anterior maxillary segment, which allows for tal Hospital and a local clinic was accounted for by precise adjustment of the segment.5 All patients factoring in the magnification ratio. Measure- were treated with a 0.022-inch slot preadjusted ments of angulation and distance were calculated edgewise appliance (MBT or Clarity; 3M Unitek to the nearest 0.01 degree and 0.01 mm. Dental Products, Monrovia, Calif.). Nineteen skeletal and 14 soft-tissue landmarks Lateral cephalometric radiographs were taken are defined in Figure 1. Six angular and two linear in centric occlusion in the natural head position.9 variables were selected for skeletal measurements Pretreatment and posttreatment lateral cephalo- (Fig. 2), six angular and two linear variables for grams were traced and digitized by one operator. dental measurements (Fig. 3), and three angular A measurement program was set up on the V-Ceph and nine linear variables for soft-tissue measure- (Cybermed, Seoul, Korea). The difference in mag- ments (Figs. 4 and 5).

Fig.2. Skeletalmeasurements.(Left)1,SNA(degrees);2,AtoN-perpendicular(mm).(Center)3,SNB(degrees);4,Pog-Nperpendicular (mm); 5, SN-GoMe (degrees). (Right) 6, ANB (degrees); 7, ODI (degrees); 8, APDI (degrees). HP, horizontal plane (7 degrees’ angulation from the SN plane); APDI, anteroposterior discrepancy indicator, sum of palatal plane angle (␣), Downs’ facial plane angle (␥), and AB to facial plane angle (␦); ODI, overbite depth indicator, sum of palatal plane angle (␣) and AB–mandibular plane angle (␤).

1029 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 3. Dental measurements. (Left) 1, U1-FH (degrees); 2, IMPA (degrees); 3, IIA (degrees). (Center) 4, Upper alveolar ridge angle- (degrees); 5, lower alveolar ridge angle (degrees); 6, U1 to alveolar ridge (AR) (degrees). (Right) 7, Overjet (mm); 8, overbite (mm); U1, upper central incisor; FH, Frankfurt horizontal plane; U1 to FH, angle between (UIE-UIA) and (Po-Or); IMPA, lower central incisor (LIA-LIE)–mandibularplane(Go-Me);IIA,interincisalangle;L1,lowercentralincisor;upperalveolarridgeangle(UALRA),anglebetween palatalplaneandupperalveolarridgeline(linebetweensupradentaleandApoint);palatalplane,planebetweenANSandPNS;lower alveolar ridge angle (LALRA), angle between mandibular plane and lower alveolar ridge line (line between infradentale and B point); mandibular plane, plane between Go and Me; U1 to AR, ␣(U1 to FH)-␤ (alveolar ridge line to FH); Overjet, distance between U1E and L1E; Overbite, sum of distance between U1E and occlusal plane and between L1E and occlusal plane.

One-way analysis of variance was performed and 3 were too small to perform multivariate to compare the differences among the three normality, the step-wise discriminant function groups at the pretreatment stage and change analysis was performed to determine decisive from pretreatment to posttreatment. The results differential diagnostic predictors at the pre- were verified with the Scheffe´ multiple compar- treatment stage. ison test. Although the sample sizes of groups 2 RESULTS Sample Characteristics Although mean ages at pretreatment of the three groups were not significantly different, the mean treatment period of group 1 was signifi- cantly longer than that of group 2 (p Ͻ 0.01) and group 3 (p Ͻ 0.001).

Comparison of Differences in the Skeletal and Dental Variables among the Three Groups at the Pretreatment Stage Group 1 showed more anteriorly positioned maxilla (SNA, p Ͻ 0.01) and mandible (SNB, p Ͻ 0.01; Pog to N-perpendicular, p Ͻ 0.05) than group 2 (Table 2 and Fig. 6). Although groups 2 and 3 had a steeper mandibular plane (Sn-GoMe, group 1 ver- sus group 2, p Ͻ 0.001; group 1 versus group 3, p Ͻ 0.05) than group 1, ANB, overbite depth indicator,10 Fig. 4. Soft-tissue angular variables. 1, NLA (degrees); 2, upper and anteroposterior discrepancy indicator11 showed NLA(degrees);3,lowerNLA(degrees);NLA,nasolabialangle(Cm- no significant differences among the three groups, Sn-UL); THL, true horizontal plane (plane parallel to FH); upper which means that there were no significant differ- NLA, angle between Cm-Sn and THL; lower NLA, angle between ences in the anteroposterior and vertical relation- THL and Sn-UL. ships between the maxilla and mandible.

1030 Volume 120, Number 4 • Bimaxillary Dentoalveolar Protrusion

Fig. 5. Soft-tissue linear variables. (Left) 1, interlabial gap (mm); 2, U1 exposure (mm). (Center) 3, EL-UL (mm); 4, EL-LL (mm). (Right) 5, TVL(N=)-A= (mm); 6, TVL(N=)-UL (mm); 7, TVL(N=)-LL (mm); 8, TVL(N=)-B= (mm); 9, TVL(N=)-Pog= (mm). Interlabial gap, vertical distance between Stms and Stmi; U1 exposure, vertical distance between Stms and IS; EL, Ricketts’ aesthetic line (line connecting Pn and Pog=); UL, upper lip; LL, lower lip; Pog=, soft-tissue Pog; TVL(N=), a constructed line perpendicular to the true horizontal plane through soft-tissue nasion; A=, soft-tissue A; B= (Si), soft-tissue B.

The maxillary incisors were significantly more Comparison of Differences in the Soft-Tissue proclined in group 1 than in group 2 (U1 to FH, Variables among the Three Groups at the p Ͻ 0.05) and group 3 (U1 to FH, p Ͻ 0.001). There Pretreatment Stage were no significant differences in overbite or overjet There were no differences in nasolabial angle, among the groups. The alveolar bone for the upper upper nasolabial angle, lower nasolabial angle, and lower anterior teeth (upper alveolar ridge angle; and the projection of the upper lip (TVL-ULP, lower alveolar ridge angle) were more proclined in E-UL) among the three groups (Table 3 and Fig. group 2 than in group 1 (p Ͻ 0.05). 7). Also, there were no significant differences in

Table 2. Comparison of Skeletal and Dental Variables at the Pretreatment Stage among the Three Groups Group 1 Group 2 Group 3 Multiple Variables Mean SD Mean SD Mean SD Significance Comparison SNA, degrees 82.75 2.90 79.90 3.14 81.81 3.30 0.009 (1,2)† A to N-perp, mm 1.29 3.48 –1.23 3.56 –0.57 3.94 0.048 SNB, degrees 80.22 3.17 76.79 2.83 78.06 3.84 0.002 (1,2)† Pog to N-perp, mm –3.55 7.45 –8.96 5.59 –9.98 8.80 0.008 (1,2)*(1,3)* ANB, degrees 2.53 2.20 3.15 2.51 3.75 1.59 0.197 ODI, degrees 70.46 7.05 69.47 7.21 72.69 6.55 0.382 APDI, degrees 85.33 4.53 82.28 4.32 83.68 4.24 0.063 SN-GoMe, degrees 33.42 3.75 38.86 4.92 37.77 4.83 0.000 (1,2)‡(1,3)* U1 to FH, degrees 125.05 5.48 120.38 5.73 116.24 5.31 0.000 (1,2)*(1,3)‡ IIA, degrees 107.90 5.71 110.33 5.53 113.11 6.89 0.023 (1,3)* IMPA, degrees 101.98 5.76 99.35 6.58 100.51 4.32 0.287 Overbite, mm 0.78 1.42 0.99 1.60 1.25 1.53 0.606 Overjet, mm 4.37 1.43 4.70 1.80 3.83 0.97 0.221 UALRA, degrees 114.97 5.93 119.14 4.68 114.91 4.57 0.016 (1,2)* U1 to AR, degrees 10.51 5.04 2.08 5.69 4.59 5.94 0.000 (1,2)‡(1,3)† LALRA, degrees 99.65 6.37 94.10 5.41 98.02 6.73 0.011 (1,2)* Group 1, orthodontic treatment; group 2, corticotomy-assisted orthodontic treatment in the maxilla and anterior segmental osteotomy in the mandible; group 3, anterior segmental osteotomy in the maxilla and mandible; A to N-perp, A to N-perpendicular; Pog to N-perp, Pog to N-perpendicular; U1, upper central incisor; IIA, interincisal angle; UALRA, upper alveolar ridge angle; U1 to AR, U1 to upper alveolar ridge angle; LALRA, lower alveolar ridge angle. The differences in skeletal and dental variables among the groups were tested by one-way analysis of variance and verified with the Scheffe´ multiple comparison test: *p Ͻ 0.05; †p Ͻ 0.01; ‡p Ͻ 0.001.

1031 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 6. Comparison of profilogram between pretreatment and posttreatment. (Left) Example of group 1 (orthodontic treatment). (Center) Example of group 2 (corticotomy assisted with skeletal anchorage in the maxilla and anterior segmental osteotomy in the mandible). (Right) Example of group 3 (anterior segmental osteotomy in the maxilla and mandible).

Table 3. Comparison of Soft-Tissue Variables at the Pretreatment Stage among the Three Groups Group 1 Group 2 Group 3 Multiple Variables Mean SD Mean SD Mean SD Significance Comparison NLA, degrees 91.94 18.28 86.81 12.51 93.58 11.40 0.359 Upper NLA, degrees 22.65 10.88 21.41 7.04 23.32 9.86 0.828 Lower NLA, degrees 69.28 10.32 65.41 9.18 70.26 6.60 0.226 EL-ULP, mm 1.77 2.20 2.79 2.09 2.37 2.16 0.262 EL-LLP, mm 4.55 1.87 5.20 2.60 5.61 2.88 0.333 ILGAP, mm 0.79 1.33 1.64 2.05 2.32 2.00 0.021 (1,3)* U1EXP, mm 2.37 1.61 2.88 2.19 3.32 1.55 0.227 TVL(N=)-A=, mm 8.19 3.29 6.34 3.29 6.25 3.12 0.074 TVL(N=)-ULP, mm 15.29 4.28 13.29 4.38 13.02 3.66 0.133 TVL(N=)-LLP, mm 13.72 5.61 10.62 5.02 10.42 4.41 0.054 TVL(N=)-B=, mm 4.60 6.32 0.27 5.63 –0.16 5.01 0.011 (1,3)* TVL(N=)-Pog=, mm 3.10 8.15 –2.85 6.30 –2.84 7.02 0.008 (1,2)*(1,3)* Group 1, orthodontic treatment; group 2, corticotomy-assisted orthodontic treatment in the maxilla and anterior segmental osteotomy in the mandible; group 3, anterior segmental osteotomy in the maxilla and mandible; EL, Ricketts’ aesthetic line; A-A=, soft-tissue thickness on A point; U1EXP, upper incisor exposure; TVL(N=), a constructed line perpendicular to the true horizontal plane through soft-tissue nasion. The differences in soft-tissue variables among the groups were tested by one-way analysis of variance and verified with the Scheffe´ multiple comparison test: *p Ͻ 0.05; †p Ͻ 0.01; ‡p Ͻ 0.001.

Fig. 7. Comparison of facial profile between pretreatment and posttreatment. (Left) Example of group 1 (orthodontic treatment). (Center) Example of group 2 (corticotomy assisted with skeletal anchorage in the maxilla and anterior segmental osteotomy in the mandible). (Right) Example of group 3 (anterior segmental osteotomy in the maxilla and mandible).

1032 Volume 120, Number 4 • Bimaxillary Dentoalveolar Protrusion

Table 4. Comparison of the Amount of Change in Skeletal and Dental Variables among the Three Groups Group 1 Group 2 Group 3 Multiple Variables Mean SD Mean SD Mean SD Significance Comparison ⌬SNA, degrees 0.56 1.84 –0.33 2.06 –3.96 2.78 0.000‡ (1,3)‡(2,3)‡ ⌬A to N-perp, mm 0.77 2.04 –0.36 2.17 –4.32 3.17 0.000‡ (1,3)‡(2,3)‡ ⌬SNB, degrees –0.57 1.64 –2.14 1.29 –2.64 1.72 0.000‡ (1,2)†(1,3)‡ ⌬Pog to N-perp, mm –0.30 2.95 –0.82 2.46 0.37 4.43 0.550 ⌬ANB, degrees 1.13 1.20 1.78 1.74 –1.34 1.63 0.000‡ (1,3)‡(2,3)‡ ⌬ODI, degrees 1.59 2.05 3.74 2.46 –0.91 3.82 0.000‡ (1,2)*(1,3)*(2,3)‡ ⌬APDI, degrees –2.01 2.34 –4.60 2.86 –1.75 2.78 0.001† (1,2)†(2,3)† ⌬SN-GoMe, degrees 0.64 1.60 0.43 0.96 0.38 1.34 0.786 ⌬U1 to FH, degrees –18.84 5.60 –19.43 5.10 –8.65 5.51 0.000‡ (1,3)‡(2,3)‡ ⌬IIA, degrees 31.74 9.37 25.62 7.56 14.93 7.53 0.000‡ (1,3)‡(2,3)† ⌬IMPA, degrees –13.42 5.70 –6.57 5.29 –6.54 4.98 0.000‡ (1,2)‡(1,3)‡ ⌬Overbite, mm 1.51 1.45 1.03 2.04 0.29 1.91 0.092 ⌬Overjet, mm –0.51 1.61 –1.17 2.14 –0.18 1.37 0.215 ⌬UALRA, degrees –12.34 4.68 –15.71 5.31 –5.17 5.01 0.000‡ (1,3)‡(2,3)‡ ⌬U1 to AR, degrees –6.45 5.70 –3.96 5.65 –4.68 5.68 0.293 ⌬LALRA, degrees –14.17 6.53 –5.17 6.24 –4.96 7.92 0.000‡ (1,2)‡(1,3)‡ Group 1, orthodontic treatment; group 2, corticotomy-assisted orthodontic treatment in the maxilla and anterior segmental osteotomy in the mandible; group 3, anterior segmental osteotomy in the maxilla and mandible; APDI, anteroposterior discrepancy indicator; ⌬, amount of change between pretreatment and posttreatment; A to N-perp, A to N-perpendicular; Pog to N-perp, Pog to N-perpendicular; U1, upper central incisor; IIA, interincisal angle; UALRA, upper alveolar ridge angle; U1 to AR, U1 to upper alveolar ridge angle; LALRA, lower alveolar ridge angle. The amount of change in skeletal and dental variables among the groups was tested by one-way analysis of variance and verified with the Scheffe´ multiple comparison test: *p Ͻ 0.05; †p Ͻ 0.01; ‡p Ͻ 0.001.

Table 5. Comparison of the Amount of Change in Soft-Tissue Variables among the Three Groups Group 1 Group 2 Group 3 Multiple Variables Mean SD Mean SD Mean SD Significance Comparison NLA, degrees 6.88 16.28 17.59 8.61 11.10 12.07 0.027* (1,2)* Upper NLA, degrees –0.22 10.54 2.66 8.10 1.47 7.81 0.555 Lowe NLA, degrees 7.11 9.45 14.93 4.74 9.64 8.30 0.005† (1,2)† EL-ULP, mm –2.17 1.56 –3.53 1.52 –3.87 1.14 0.000‡ (1,2)†(1,3)† EL-LLP, mm –3.67 1.70 –5.36 1.83 –5.94 2.31 0.000‡ (1,2)*(1,3)‡ ILGAP, mm –0.11 1.50 –1.20 2.11 0.41 4.23 0.162 U1EXP, mm 0.58 1.32 0.16 1.33 –0.67 1.41 0.016* (1,3)* TVL(N=)-A=, mm –0.74 1.62 –0.73 2.06 –1.18 2.36 0.729 TVL(N=)-ULP, mm –2.54 2.36 –4.30 1.97 –3.43 2.43 0.033* (1,2)* TVL(N=)-LLP, mm –4.12 2.70 –5.96 2.21 –5.30 2.89 0.051 TVL(N=)-B=, mm –2.65 2.76 –3.84 4.13 –2.53 2.81 0.372 TVL(N=)-Pog=, mm –0.84 3.32 –0.74 4.02 1.15 2.87 0.156 Group 1, orthodontic treatment; group 2, corticotomy-assisted orthodontic treatment in the maxilla and anterior segmental osteotomy in the mandible; group 3, anterior segmental osteotomy in the maxilla and mandible; ⌬, amount of change between pretreatment and posttreatment; NLA, nasolabial angle; MLA, metolabial angle; EL, Ricketts’ aesthetic line; UL, upper lip; LL, lower lip; ILGAP, interlabial gap; U1EXP, upper incisor exposure; TVL(N=), a constructed line perpendicular to the true horizontal plane through soft-tissue nasion. The amount of change in soft-tissue variables among groups was tested by one-way analysis of variance and verified with the Scheffe´ multiple comparison test: *p Ͻ 0.05; †p Ͻ 0.01; ‡p Ͻ 0.001. the upper incisor exposure (U1 exp) among the can reposition the A point more posteriorly than three groups. orthodontic treatment and corticotomy-assisted orthodontic treatment, there was a greater de- Comparison of the Amount of Change in the crease in SNA and ANB in group 3 than in groups Skeletal and Dental Variables 1(p Ͻ 0.001) and 2 (p Ͻ 0.001). Posterior movement of the maxilla (change An increase in overbite depth indicator in SNA and change in A to N-perpendicular) in means a bite deepening tendency in group 1 and group 3 and of the mandible (change in SNB) in group 2. Group 3 showed a decrease in overbite group 2 and group 3 were significantly greater depth indicator. These findings showed that the than in groups 1 (p Ͻ 0.001) and 2 (p Ͻ 0.001), vertical control of the anterior bony segment and in group 1 (p Ͻ 0.001), respectively (Table 4 was possible with anterior segmental osteotomy and Fig. 6). Because anterior segmental osteotomy in group 3.

1033 Plastic and Reconstructive Surgery • September 15, 2007

Table 6. Stepwise Discriminant Analysis creased more significantly than in group 1 Ͻ Nonstandardized Canonical (change in lower nasolabial angle, p 0.01). Discriminant Function These findings mean that group 1 has the least Coefficients amount of change in upper lip projection and Predictable angulation. In change of the upper incisor expo- Variable Function 1 Function 2 sure, there was an opposite change in group 1 and Pog-N per, mm 0.088 0.043 in group 3 (p Ͻ 0.05). APDI, degrees 0.097 0.144 U1-FH, degrees 0.154 –0.187 UALRA, degrees –0.260 –0.038 LALRA, degrees 0.105 0.071 Stepwise Discriminant Analysis Constant –6.433 8.418 Through the entry statistics for stepwise selec- Functions at tion, five variables were selected (Tables 6 and 7). Group Centroids Unstandardized discriminant function coeffi- Function 1 Function 2 cients of the selected variables, along with a cal- Group 1 1.524 –0.141 culated constant (Table 6), led to the following Group 2 –1.638 –0.496 equations that calculate individual scores for as- Group 3 –0.715 0.876 sessing a patient with bimaxillary protrusion to APDI, anteroposterior discrepancy indicator; Pog-N per, Pog to N one of the three treatment groups. perpendicular; U1, upper central incisor; UALRA, upper alveolar ridge angle; LALRA, lower alveolar ridge angle; group 1, orthodontic The centroids of each group in function 1 and treatment; group 2, corticotomy-assisted orthodontic treatment in function 2 are shown in Table 6. For example, if the maxilla and anterior segmental osteotomy in the mandible; the value of function 1 is above 1.524, it can be group 3, anterior segmental osteotomy in the maxilla and mandible. Function 1 ϭ 0.088 ϫ Pog to N perpendicular (mm) ϩ 0.097 ϫ APDI considered as a candidate for orthodontic treat- (degrees) ϩ 0.154 ϫ U1 to FH (degrees) – 0.260 ϫ UALRA (degrees) ϩ ment (group 1). If the value is below –1.638, it can 0.105 ϫ LALRA (degrees) – 6.433. be treated with corticotomy-assisted orthodontic Function 2 ϭ 0.043 ϫ Pog to N perpendicular (mm) ϩ 0.144 ϫ APDI (degrees) – 0.187 ϫ U1 to FH (degrees) – 0.038 ϫ UALRA (degrees) ϩ treatment in the maxilla and anterior segmental 0.071 ϫ LALRA (degrees) ϩ 8.418. osteotomy in the mandible (group 2). If it is ap- proximately –0.715, it can be assigned to anterior segmental osteotomy (group 3). If the value of The changes of the upper incisor proclination function 1 is not matched to any centroids values, (change in U1 to FH) in group 3 were significantly Ͻ Ͻ function 2 can be used to determine the values. smaller than in groups 1 (p 0.001) and 2 (p The percentage of correctly classified cases 0.001). Interestingly, the changes in overbite and was 81.5 percent (Table 7). Three patients in overjet were not significantly different among the group 1, six in group 2, and four in group 3 were three groups. Bending of the upper alveolar ridge misclassified. in group 3 was less than in groups 1 (p Ͻ 0.001) and2(p Ͻ 0.001). DISCUSSION Because orthodontic tooth movement is the Comparison of the Amount of Change in the result of bone remodeling secondary to mechan- Soft-Tissue Variables ical force and teeth usually move at the rate of The upper lip projection in groups 2 and 3 approximately 1 mm per month, closure of the (change in E-UL, group 1 versus group 2, p Ͻ 0.01, first premolar extraction space can take more than group 1 versus group 3, p Ͻ 0.01; change in TVL- 8 months.12 In this study, a longer treatment pe- ULP, group 1 versus group 2, p Ͻ 0.05) decreased riod in the orthodontic treatment group than in significantly more than in group 1 (Table 5 and the corticotomy-assisted orthodontic treatment Fig. 7). The upper lip angulation in group 2 in- (p Ͻ 0.01) and anterior segmental osteotomy

Table 7. Classification Results* Predicted Group Membership (%) Actual No. of Group Cases Group 1 Group 2 Group 3 Total Group 1 29 26 (89.7) 0 (0) 3 (10.3) 29 (100.0) Group 2 20 1 (5.0) 14 (70.0) 5 (25.0) 20 (100.0) Group 3 16 1 (6.3) 2 (12.5) 13 (81.3) 16 (100.0) Group 1, orthodontic treatment; group 2, corticotomy-assisted orthodontic treatment; group 3, anterior segmental osteotomy. *Proportion of original cases correctly classified: 81.5 percent.

1034 Volume 120, Number 4 • Bimaxillary Dentoalveolar Protrusion groups (p Ͻ 0.001) (Table 1) suggests that corti- creased significantly in orthodontic treatment but cotomy-assisted orthodontic treatment and ante- decreased in anterior segmental osteotomy (Table rior segmental osteotomy can be the preferred 5 and Fig. 6). In corticotomy-assisted orthodontic methods in adult bimaxillary protrusion patients treatment, an increase of upper incisor exposure because of shorter treatment periods. was observed, although it was not statistically sig- Before treatment, there were no significant nificant (Table 5 and Fig. 6). In patients with differences in the anteroposterior and vertical re- bimaxillary protrusion and a gummy smile, ante- lationships between the maxilla and mandible rior segmental osteotomy can control the vertical (Table 2) or in the projection and angulation of repositioning of the anterior segment and im- the upper lip among the three groups (Table 3). prove the gummy smile. However, bony chin position in the orthodontic In the present study, nasolabial angle and treatment group was more anteriorly placed than lower nasolabial angle increased in all groups (Ta- in the corticotomy-assisted orthodontic treatment ble 5); however, the amount of increase was great- or anterior segmental osteotomy groups (Table est in group 2, followed by group 3 and group 1 2). The effect of lip retraction is relatively not well (Table 5 and Fig. 7). In contrast, change in the expressed in the patients with underdeveloped chins; therefore, anterior segmental osteotomy or upper nasolabial angle was not significantly dif- corticotomy-assisted orthodontic treatment can ferent among the three groups (Table 5). There- be considered to maximize the soft-tissue change fore, an increase in nasolabial angle after treat- rather than orthodontic treatment. When consid- ment is related more to the retraction of the upper ering that proclination of the upper incisor and lip than to the change in the nose regardless of the alveolar ridge angle showed a significant differ- type of treatment used. ence among the three groups (Table 2), the upper For retraction of the upper lip, corticotomy- incisor and alveolar bone variables and bony chin assisted orthodontic treatment was more efficient position had greater influence on selecting treat- than orthodontic treatment (Table 5 and Fig. 7). ment option for these bimaxillary protrusion pa- The controlled tipping of the upper incisors and tients. lingual bending of the alveolar bone in the cor- Although the movement patterns of the upper ticotomy-assisted orthodontic treatment group incisors in groups 1 and 2 were almost “controlled made the upper lip move more posteriorly than in tipping,” the upper incisor was retracted with the orthodontic treatment group. This suggests bodily movement in group 3 (Table 4 and Fig. 6). that corticotomy-assisted orthodontic treatment If the upper incisors have a normal inclination, with skeletal anchorage can be advantageous for orthodontic treatment or corticotomy-assisted achieving the maximum retraction of the upper orthodontic treatment can bring out severe lin- incisors in patients with severe proclination of the gual tipping of these teeth. upper incisors and the alveolar bone. Change of the upper and lower alveolar To determine the best skeletal and dental vari- ridge angle means bending of the alveolar bone ables that could aid in the differential diagnosis of by orthodontic treatment and corticotomy- patients with bimaxillary protrusion among orth- assisted orthodontic treatment and reposition- odontic treatment, corticotomy-assisted orthodon- ing of the anterior bony segment by anterior tic treatment, and anterior segmental osteotomy, segmental osteotomy. In this study, the amount discriminant analysis with stepwise inclusion of of alveolar bone bending by orthodontic treat- variables was applied. The purpose of the stepwise ment or corticotomy-assisted orthodontic treat- ment was significantly greater than reposition- selection was to locate a more parsimonious subset ing of the anterior bony segment by anterior of variables that could discriminate nearly as well segmental osteotomy (Table 4 and Fig. 6). These as, if not better than, the full set. Percentages of findings suggest that orthodontic treatment and the correct prediction of candidates was 89.7 per- corticotomy-assisted orthodontic treatment cent for orthodontic treatment (group 1), 81.3 bend the alveolar bone lingually and anterior percent for anterior segmental osteotomy (group segmental osteotomy repositions the anterior 3), and 70.0 percent for corticotomy-assisted orth- bony segment with bodily movement. odontic treatment (group 2) (Table 7). These per- Upper incisor exposure should be considered centages indicate that the discriminant function when choosing a treatment option for patients 1 will be clinically useful in deciding which of with bimaxillary protrusion who have a vertical the three methods treats patients with bimaxil- excess of the maxilla. Upper incisor exposure in- lary protrusion.

1035 Plastic and Reconstructive Surgery • September 15, 2007

CONCLUSIONS create a conflict of interest with information presented in Clinicians must attempt to obtain the best fa- this article. cial aesthetics without compromising dental aes- thetics, stability, and function. If the patient has a REFERENCES class I skeletal pattern and proclined upper and 1. Wolfe, S. A., Hu, L., and Berkowitz, S. In search of the harmonious face: , with an examination of lower incisors, orthodontic treatment can pro- the indications for retrograde maxillary displacement. Plast. duce a good result. In patients with relatively nor- Reconstr. Surg. 99: 1261, 1997. mal upper incisor inclination, a class I skeletal 2. Farrow, A. L., Zarrinnia, K., and Azizi, K. Bimaxillary pro- pattern, relatively poor chin development, and a trusion in black Americans: An esthetic evaluation and the gummy smile, anterior segmental osteotomy can treatment considerations. Am. J. Orthod. Dentofacial Orthop. 104: 240, 1993. be a better option for reducing the lip protrusion 3. Keating, P. J. The treatment of bimaxillary protrusion: A without unwanted change of the upper incisor cephalometric consideration of changes in the inter-incisal inclination. In patients with severe proclination of angle and soft tissue profile. Br. J. Orthod. 13: 209, 1986. the upper incisors and the alveolar bone, corti- 4. Bae, S. M., Park, H. S., Kyung, H. M., Kwon, O. W., and Sung, cotomy-assisted orthodontic treatment can be ad- J. H. Clinical application of micro-implant anchorage. J. Clin. Orthod. 36: 298, 2002. vantageous for achieving the maximum retraction 5. Kim, J. R., Son, W. S., and Lee, S. G. A retrospective analysis in a shorter treatment period than orthodontic of 20 surgically corrected bimaxillary protrusion patients. Int. treatment. The skeletal, dental, and soft-tissue J. Adult Orthodon. Orthognath. Surg. 17: 23, 2002. variables and discriminant functions in this 6. Scheideman, G. B., Kawamura, H., Finn, R. A., and Bell, W. H. study could contribute to the differential diag- Wound healing after anterior and posterior subapical osteot- omy. J. Oral Maxillofac. Surg. 43: 408, 1985. nosis and treatment planning for bimaxillary 7. Chung, K. R., Oh, M. Y., and Ko, S. J. Corticotomy-assisted protrusion between orthodontic treatment, cor- orthodontics. J. Clin. Orthod. 35: 331, 2001. ticotomy-assisted orthodontic treatment, and 8. Baek, S. H., and Kim, B. H. Determinants of successful treat- anterior segmental osteotomy methods. ment of bimaxillary protrusion: Orthodontic treatment ver- sus anterior segmental osteotomy. J. Craniofac. Surg. 16: 234, Seung-Hak Baek, D.D.S., M.S.D., Ph.D. 2005. Department of Orthodontics 9. Lundstrom, F., and Lundstrom, A. Natural head position as School of Dentistry a basis for cephalometric analysis. Am. J. Orthod. Dentofacial Seoul National University Orthop. 101: 244, 1992. Yeonkun-dong #28 10. Kim, Y. H. Overbite depth indicator with particular reference Jongro-ku, Seoul 110-768, South Korea to anterior open-bite. Am. J. Orthod. 65: 586, 1974. [email protected] 11. Kim, Y. H., and Vietas, J. J. Anteroposterior dysplasia indi- cator: An adjunct to cephalometric differential diagnosis. DISCLOSURES Am. J. Orthod. 73: 619, 1978. 12. Bilodeau, J. E. Nonsurgical treatment with rapid mandibular There was no financial support, benefit, or interest canine retraction via periodontal ligament distraction in an for any of the authors, and there were no commercial adult with a class III malocclusion. Am. J. Orthod. Dentofacial associations or financial disclosures that might pose or Orthop. 128: 388, 2005.

1036 COSMETIC

Transblepharoplasty Ptosis Repair: Three-Step Technique

Clinton D. McCord, M.D. Background: The ability to predict postoperative lid levels in ptosis surgery has Hisham Seify, M.D. been refined over the years, but there is no completely predictable formula with Mark A. Codner, M.D. which to predict the final tension in the upper lid that determines the final Atlanta, Ga.; and Newport, Calif. upper lid level. A significant percentage of patients continue to require post- operative surgical revision. The authors studied the effectiveness of a technique for the quantitation of aponeurotic repair that is not a measured resection procedure, does not require voluntary patient cooperation, and can be per- formed under general anesthesia. Methods: The surgical technique involves reapproximation of specific anatom- ical landmarks, adjustment of upper lid level by eyelid gapping, and adjustment of upper lid tension with a spring-back test. Consecutive patient charts were reviewed retrospectively for age, sex, clinical examination, levator function, and outcomes, including revision rate and patient satisfaction. A total of 144 pro- cedures were performed for 80 patients (64 bilateral and 16 unilateral). The series was reported for a 3-year period (2002 through 2005). The mean age was 62 years (range, 40 to 85 years). The average follow-up was 18 months. All patients had acquired adult ptosis with levator dehiscence and good levator function. Results: The criterion for surgical revision was a greater than 1-mm asymmetry between the eyelids or patient dissatisfaction. Twelve patients (15 percent) were considered to be slightly asymmetric postoperatively, but only two (2.5 percent) exceeded the criterion and required surgical revision in the early postoperative period (Ͻ1 year). Conclusion: Tarso levator surgery can be performed under general anesthesia using a three-step technique to correct ptosis with a superior predictability. (Plast. Reconstr. Surg. 120: 1037, 2007.)

ormal upper eye lid position may vary but, history or characteristic lagophthalmos on down- in general, the upper lid levels have a gaze. Acquired ptosis is a group of disorders of Nsymmetrical position and show a symmet- mixed physiologic and anatomical elements, but rical amount of visible iris (“color”) above the most of the patients presenting to the surgeon pupil. Cases of congenital ptosis should be ex- are of the involutional type with deficiency in the cluded as candidates for this procedure because aponeurosis of the levator. The ptotic lid in this their response to surgery is different. The levator group of patients results from thinning and muscle in these patients is stiff and does not stretching in the aponeurosis and downward respond well to aponeurotic surgery. Ptosis pre- shift of the tarsal plate. Patients in this group can senting in advancing age could still be of the have significant ptosis, with good to congenital variety and should be recognized by a

From Paces Plastic Surgery and University of California at Irvine. Supplemental digital content is available for Received for publication November 28, 2005; accepted April this article. A direct URL citation appears in 5, 2006. the printed text; simply type the URL address Winner of the Sherrell J. Aston Award for best presentation into any web browser to access this content. at the 2006 meeting of the American Society for Aesthetic Clickable links to the material are provided in Plastic Surgery. the HTML text of this article on the Journal’s Copyright ©2007 by the American Society of Plastic Surgeons Web site (www.PRSJournal.com). DOI: 10.1097/01.prs.0000278000.36558.98

www.PRSJournal.com 1037 Plastic and Reconstructive Surgery • September 15, 2007

Table 1. Causes of Pseudoptosis duced, used for a number of years, and presently ● Contralateral lid retraction (thyroid disease or other) is the most popular technique. During surgery, the ● Enophthalmos (or contralateral exophthalmos) patient will be asked to voluntarily open his or her ● Upper lid pressure (dermatochalasis, brow ptosis, eyelids and the surgeon will adjust the sutures tumor) until the eyelids reach the desired level.6,7 This ● Spasm or guarding (essential blepharospasm, hemifacial spasm) technique requires minimal local anesthesia, min- ● Misdirected regeneration facial nerve imal sedation, absence of any akinesia of the le- vator from the local anesthetic, and absence of any epinephrine effect on the Mu¨ller’s muscle, which excellent levator function. On examination of can alter the upper lid position and confuse the the upper lid, thinning of the tissues above the adjustment.8 In most cases, the patient is asked to tarsal plate and a high lid crease can be charac- sit up on the operative table so that their lid po- teristic but may be masked by dermatochalasis sition can be evaluated. Even with this fairly te- and herniated fat. The differential diagnosis of dious technique of quantitation, there is an ap- ptosis and pseudoptosis should always be consid- proximately 10 percent revision rate in these ered in cases of acquired ptosis (Table 1). Addi- patients.9,10 tional tests may be needed to rule out a neuro- The aesthetic surgeon faces a problem when myopathic condition. combining ptosis repair with other aesthetic pro- Diagnosis must be made of asymmetric upper cedures that require a general anesthetic. One lid ptosis, not to be confused with true unilateral must first perform the ptosis procedure with local ptosis. If ptosis correction is performed in the anesthesia and sedation, and then have a general most ptotic eyelid in asymmetric cases without anesthetic induction, necessitating re-preparing correcting the contralateral milder ptosis, the the patient so that the other procedures can be uncorrected side will worsen postoperatively. performed. These cases should be treated as bilateral cases. The authors have developed and are using a In the present series, ocular examination had technique for quantitating adult aponeurotic de- been performed in all patients, including mea- hiscence under general anesthesia without patient surement of presurgical visual acuity, pupillary cooperation that not only allows a single general examination, motility examination, evaluation of anesthetic but also has a much higher predictabil- Bell’s phenomenon, and examination to note ity than voluntary cooperation. The surgical tech- any preexisting keratopathy. Eyelid measure- nique includes three essential steps performed ments included levator muscle function and the under general anesthesia using one central lifting distance from the light reflex on the patient’s suture. First, two specific anatomical landmarks cornea to the central upper eyelid margin in are approximated with a single suture (the supe- primary gaze position. Compensatory brow arch- rior tarsal plate in line with the pupil, 3 mm inside ing was noted and taken into account. All pa- the upper edge and the musculoaponeurotic junc- tients had good to excellent levator function tion in the levator muscle). Second, the suture is (Ն12 mm). Patient charts were reviewed retro- tightened until the gapping between the upper spectively identifying age, sex, clinical examina- and lower lids is symmetrical between the two eyes. tion, preoperative levator function, and out- Third, the suture tension is further adjusted, if comes including revision rate and patient necessary, until the spring-back between the up- satisfaction. Photographs were available in all per and lower lids is symmetrical between the two patients for evaluation. eyes. Adjustment and suture tension and position- ing may be necessary to achieve this symmetry. In EXISTING TECHNIQUES FOR PTOSIS unilateral cases, only the first step is necessary. SURGERY (See Video, Supplementary Digital Content 1, In the past, it has been the practice to quan- which demonstrates transblepharoplasty acquired titate ptosis surgery by measuring the amount of ptosis aponeurotic repair using the three-step tissue removed from the eyelid with the hope of technique, http://links.lww.com/A31.) predicting the final lid level (“cookie-cutter” tech- nique). This technique was performed with rea- sonable results.1–5 After this, to further increase MATERIALS AND METHODS the predictability of the postoperative lid level, a A lid crease incision is made at the desired technique using voluntary cooperation by the pa- level, usually at the upper border of the tarsal plate tient while awake using local anesthesia was intro- (approximately 9 to 10 mm above the lash line).

1038 Volume 120, Number 4 • Transblepharoplasty Ptosis Repair

Fig. 1. (Left) The upper lid following an open sky blepharoplasty after excision of skin orbicularis and under- lying septum. (Right) The normal levator anatomy: muscular portion of the levator muscle, the levator apo- neurosis, and the musculoaponeurotic junction as seen through the blepharoplasty incision.

A preceding upper lid blepharoplasty may be per- edge of the tarsal plate (Fig. 2). It is not necessary formed with removal of appropriate skin and mus- to disturb the Mu¨ller’s muscle or the superior cle and preaponeurotic fat above the crease incision. vascular arcade, thus reducing the amount of The “open sky” technique of upper blepharoplasty bleeding during the procedure (Fig. 3). After the with excision of a block of skin and corresponding aponeurosis has been dissected free from the Mu¨l- underlying orbicularis and septum gives the clear- ler’s muscle, a 6-0 double-armed suture, with small est exposure of the levator muscle and its apo- neurosis.

Anatomy Identification The aponeurosis is white but may vary in ap- pearance. In some cases, the aponeurosis may be relatively intact; however, usually, it is rarefied and stretched with Mu¨ller’s muscle and the superior vascular arcade visible through the tissue at the superior edge of the tarsus. The muscular portion of the levator is exposed by retraction of the preaponeurotic fat. Pinkish to brownish striations of the muscle can be easily seen inserting on the aponeurosis, which forms the important landmark of the musculoaponeurotic junction (Fig. 1). On occasion, in some older patients there may be some fatty degeneration in the levator muscle, which por- tends further weakening of the muscle with age.

First Step: Anatomical Landmark Reapproximation The aponeurosis is marked at the superior Fig.2. Drawingdepictingtheincisionofthelevatoraponeurosis tarsal border and incised just inside the superior just inside the superior edge of the tarsal plate.

1039 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 3. Frontal and sagittal views of the upper lid showing dissection of the levator aponeurosis away from the tarsal plate and underlying the Mu¨ller’s muscle. cutting needles, is introduced half-thickness near should be placed in the exact vertical line with the (within 2 to 3 mm) the upper edge of the tarsal pupil (Fig. 4). This aspect is important when deal- plate. This suture is the central lifting suture and ing with involutional patients who have a lateral displacement of the tarsal plate.11,12 A double- armed suture is used, which is then passed be- neath the levator aponeurosis. Then, the needles are brought up through the levator at the junction of the white aponeurosis and the levator muscle— the musculoaponeurotic junction (Fig. 5). The central double-armed suture is the lifting suture, the “motor” for lifting the lid. Additional sutures are rarely used but may be used for contouring if needed. Additional nasal sutures are never used and temporal sutures are used rarely. In bilateral cases, after anatomical markers are used for surgery, further steps of adjustment are needed to ensure symmetry of the correction. Pre- operatively, it is important to determine whether ptosis is bilateral because bilateral but asymmetric ptosis commonly exists. Patients with lesser amounts of contralateral ptosis are considered as having bilateral ptosis and treated as such. Regardless of the symmetry or asymmetry of the ptosis, the use of anatomical markers is the same.

Fig. 4. Diagrammatic view of the upper lid showing placement Second Step: Intraoperative Eyelid Gapping of the central lifting suture just inside the superior edge of the The suture attaching the tarsus to the levator tarsalplateinlinewiththepupil.Inmostcases,thetarsalplatehas is tightened until the gapping or separation of the shifted laterally so that the apex of the tarsal plate is lateral to upper and lower eyelids is symmetrical between suture placement. both eyes. A caliper is usually used for precise

1040 Volume 120, Number 4 • Transblepharoplasty Ptosis Repair

Fig.5. Frontalandsagittalviewsoftheupperlidshowingthedouble-armedsutureplacedthrough the musculoaponeurotic junction after its placement in the tarsal plate. measurement of the separation (Fig. 6). The ab- Third Step: Adjustment of the Eyelid solute amount of gapping is not critical and may Spring-Back vary from patient to patient, but the amount of Even though intraoperative gapping may be gapping must be symmetrical. symmetrical from side to side, there may be differ- ences in suture tension of the upper lids that may cause unequal position of the upper lids postoper- atively. This problem is compensated for by adjust- ing suture tension in the lids until the spring-back test is equal in both upper lids. With this step, the upper lid is pulled down by the lashes to the edge of the lower lid and then released. This step is per- formed after adjustment of the equalization of gap- ping of the eyelids has been performed. The velocity of the upward lid movement of opening is observed and tension in the sutures must be equalized, or the suture modified, until the velocity of spring-back is symmetrical in both upper lids. After the final steps of equalization, the skin incision in the upper lid can be closed in the usual manner. Occasionally, skin closure sutures are used to attach the skin muscle edges of the levator if a more accentuated crease is desired. It should be Fig. 6. After the suture is tightened, approximating the tarsal mentioned that bilateral asymmetric upper lid ptosis plate to the musculoaponeurotic junction, measurement of the should also be treated in the matter described above gappingbetweentheupperandlowereyelidisnoted.Inbilateral with symmetrical landmark approximation, upper cases of ptosis repair, the gapping should be equal. After a gap- lid gapping, and upper lid spring-back. ping, measurement of the symmetry of spring-back is performed In truly unilateral cases, repair by anatomical in the bilateral cases to ensure symmetrical tension. markers alone (tarsal plate to musculoaponeuro-

1041 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 7. Views of a patient before and after ptosis repair, with overcorrection and massage exercise. tic junction) is the only step used for quantitation mean age was 62 years (range, 40 to 85 years). The of repair. In some patients with unilateral ptosis, average follow-up was 18 months. The criterion for this may produce a mild overcorrection. This po- desired result was no asymmetry greater than 1 sition is the most desirable position other than mm or patient satisfaction. perfect position, because postoperative downward A total of 12 patients (15 percent) were con- traction massage will easily overcome a mild over- sidered slightly asymmetric postoperatively. Eight correction. Postoperatively, if the eyelid is slightly patients presented with overcorrection and be- overcorrected, stretching the overcorrected up- came symmetric with traction massage. Four pa- per lid downward, with or without local anesthesia, tients presented with undercorrection. Two pa- in the early postoperative period will correct these tients (2.5 percent) required surgical revision for mild overcorrections (Figs. 7 and 8). undercorrection in the early postoperative period (Ͻ1 year). Four patients presented with recurrent RESULTS ptosis and asymmetry after 1 year (presumed in A total of 144 procedures were performed on disease progression); two of them required revi- 80 patients (64 bilateral and 16 unilateral). The sion surgery. Figures 9 and 10 show representative patients in whom the surgical technique for ptosis repair was used.

DISCUSSION Voluntary cooperation of the patient in the operating room (the most popular and precise ptosis procedure to date) can be a tedious affair. Variations in sedation may affect patient cooper- ation, local anesthesia may affect levator function, and epinephrine can cause contraction of the Mu¨ller’s muscle, obscuring the true resting lid level. If the patient requires a general anesthetic because more extensive surgery is also to be per- formed, the use of voluntary cooperation is not available without two types of anesthesia. The revision rate in patients when voluntary cooperation is used for ptosis correction has been Fig. 8. A patient performs massage exercise. reported to range from 9 to 12 percent.9,10 Various

1042 Volume 120, Number 4 • Transblepharoplasty Ptosis Repair

Fig. 9. Under general anesthesia, this patient underwent ptosis repair combined with an endoscope-assisted eyebrow forehead lift, lower lid, midface lift, and upper blepharoplasty. No postoperative adjustments were needed.

Fig.10. Undergeneralanesthesia,thispatientunderwentptosisrepaircombinedwithlower and upper lid blepharoplasty. endpoints are cited as the criteria for satisfactory in this series were performed under general an- results. In this study, we retrospectively reviewed esthesia. It is possible to use the three-step tech- 80 patients who required aponeurotic repair. Most nique under local anesthesia with only anatomical cases were combined with an aesthetic operation; reapproximation, gapping, and spring-back eval- some were operated on for ptosis alone. All cases uation and avoid the step of voluntary coopera-

1043 Plastic and Reconstructive Surgery • September 15, 2007 tion. The technique of repair of the aponeurotic Hisham Seify, M.D. defect was accomplished with a central lifting su- Clinton D. McCord, M.D. 12 3200 Downwood Circle, Suite 640 ture that has been used by the authors for years. Atlanta, Ga. 30327 More recently reported, the single suture can be [email protected] placed through a small central incision and be effective.13 It is to be noted that, in our series, 12 patients DISCLOSURE (15 percent) were felt postoperatively to have mild None of the authors has any financial interests re- asymmetry; only two patients required postoper- lated to this article. ative revision surgery. Postoperatively, patients with mild overcorrection were instructed to per- REFERENCES form lid massage (stretching). Four patients had 1. Beard, C. The surgical treatment of blepharoptosis: A quan- initial excellent results but presented after 2 years titative approach. Trans. Am. Ophthalmol. Soc. 64: 401, 1966. with some upper eyelid asymmetry because of re- 2. Berke, R. N. Results of resection of the levator muscle currence of ptosis in one eye; two of these patients through a skin excision and congenital ptosis. Arch. Ophthal- mol. 61: 177, 1959. required revision. To assess the outcome of the 3. Fasanella, R. M., and Servat, J. Levator resection for minimal surgical technique, patients developing ptosis af- ptosis: Another simplified operation. Arch. Ophthalmol. 65: ter 1 year were considered not in the revision rate 493, 1961. but rather as progression of the disease process. 4. Putterman, A. M., and Urist, M. J. Muller’s muscle-conjunc- The ease with which aponeurotic repair using tival resection. Arch. Ophthalmol. 93: 619, 1975. 5. McCord, C. D., Jr. An external minimal ptosis procedure: the three-step approach can be performed, usually External tarsoaponeurectomy. Trans. Am. Acad. Ophthalmol. under general anesthesia in our hands, surpasses Otolaryngol. 79: 683, 1975. that of the method of voluntary cooperation un- 6. Anderson, R. L., and Dixon, R. S. Aponeurotic ptosis surgery. der local anesthesia. The 2.5 percent revision rate Surg. Arch. Ophthalmol. 97: 1123, 1971. in our patients also surpasses the predictability of 7. Linberg, J. V., Vazquez, R. J., and Chao, G. M. Aponeurotic ptosis repair under local anesthesia prediction of results the voluntary cooperation method. The described from operative lid height. Ophthalmology 95: 1046, 1988. technique may have a bias toward slight overcor- 8. Bartley, G. B., Lowery, J. C., and Hodge, D. O. Results of rection, particularly in unilateral cases. Because levator advancement blepharoptosis repair using a standard mild overcorrections, or even severe overcorrec- protocol: Effect of epinephrine induced eyelid position tions with use of supraorbital anesthesia, can be change. Trans. Am. Ophthalmol. Soc. 94: 165, 1966. 9. Shore, J. W., Bergin, D. J., and Garrett, S. N. Results of stretched downward easily within the first week, blepharoptosis surgery with early postoperative adjustment. overcorrection is preferable to undercorrection, Ophthalmology 97: 1502, 1990. which requires cutting surgical revision. 10. McCulley, T. J., Kersten, R. C., Kulwin, T. R., and Feuer, W. J. Outcome and influencing factors of the external levator CONCLUSIONS palpebrae superioris aponeurosis advancement for blepha- roptosis. Ophthal. Plast. Reconstr. Surg. 19: 388, 2003. Tarso levator surgery can be performed under 11. McCord, C. D., and Tanenbaum, M. (Eds.). Levator surgery. general anesthesia using a three-step technique to In Oculoplastic Surgery, 2nd Ed. New York: Raven, 1987. Pp. correct ptosis with a superior predictability. It is 346–347. felt that this technique offers a simplified ap- 12. McCord, C. D. Levator surgery. In Eyelid Surgery: Principles and proach to aponeurotic repair that is more pre- Techniques. New York: Lippincott-Raven, 1995. Pp. 114–117. 13. Frueh, B. R., Musch, D. C., and McDonald, H. M. B. Efficacy dictable and also allows the repair to be combined and efficiency of a small incision, minimal dissection pro- with aesthetic cases that require a general anes- cedure versus a traditional approach for correcting aponeu- thetic. rotic ptosis. Ophthalmology 111: 2158, 2004.

1044 COSMETIC

Experience with Fibrin Glue in Rhytidectomy

Frank M. Kamer, M.D. Background: The authors conducted a large, prospective, controlled trial of Davis B. Nguyen, M.D. fibrin glue in rhytidectomy using a wide set of variables. Beverly Hills and Los Angeles, Calif. Methods: Two hundred consecutive patients undergoing elective rhytidec- tomy were studied. One hundred patients received fibrin glue over a 1-year period and were followed prospectively. Another 100 patients from the previous year who had not received fibrin glue had their charts reviewed retrospectively. All patients underwent bilateral face lifts using the deep plane technique. Results: The following data were observed for the glue versus nonglue patients: expanding hematoma rate, 1 percent versus 3 percent (p Ͼ 0.05); seroma rate, 1 percent versus 7 percent (p Ͼ 0.05); and prolonged indura- tion, edema, and ecchymosis, 0 percent versus 22 percent (p Ͻ 0.05). The pain score for glue versus nonglue patients was 100 percent minimal versus 95 percent minimal and 5 percent moderate (p Ͼ 0.05). The average score for patient satisfaction (scale, 1 to 10, with 10 being best) for glue versus nonglue patients was 9.5 versus 9.0 (p Ͼ 0.05). Conclusions: The use of fibrin glue was associated with some benefits for rhytidectomy. Fibrin glue eliminated the use of drains. The difference in expanding hematoma was clinically, but not statistically, significant. The seroma rate was decreased and neared statistical significance. There was an impressive immediate decrease in postoperative swelling. The fibrin glue was most advantageous in eliminating prolonged induration, edema, and ec- chymosis. There were no statistical differences between groups for patient satisfaction or pain. The use of fibrin glue has been shown to reduce some of the morbidity and severe complications of face lifting. (Plast. Reconstr. Surg. 120: 1045, 2007.)

ibrin tissue adhesive was used for topical Fibrin sealant has been studied previously for hemostasis during World War I.1 Its use was its use in rhytidectomy. Benefits have included revived in 1972 for sutureless microanasto- decreased drainage, swelling, ecchymosis, and F 2 moses of nerve grafts. Since then, there have hematoma rates. Previous reports have been lim- been applications in many areas of surgery, in- ited by the small number of patients, the small cluding heart surgery,3 thoracic surgery,4 number of variables studied, or the lack of pro- otolaryngology,5–7 abdominal surgery,8 maxillo- spective data. The aim of this study was to con- facial surgery,9 and trauma surgery. Despite mar- duct a large, prospective, controlled trial of fi- keting since the 1980s, fibrin sealant has been brin glue in rhytidectomy for a wide set of used more widely in Europe than in the United variables including hematoma rate; seroma rate; States. Although being described extensively,10–16 levels of ecchymosis, edema, and induration; the use of fibrin glue in aesthetic surgery has pain scores; and overall patient satisfaction. been limited. PATIENTS AND METHODS From The Lasky Clinic; Department of Surgery, Division The setting was the Lasky Clinic, an accredited of Facial Plastic and Reconstructive Surgery, University of Southern California School of Medicine; and Depart- outpatient surgical center in Beverly Hills, Cali- ment of Head and Neck Surgery, Division of Facial Plastic fornia. The study was a prospective, controlled and Reconstructive Surgery, University of California, Los trial. Two hundred patients undergoing elective Angeles School of Medicine. rhytidectomy in consecutive fashion were studied. Received for publication December 2, 2005; accepted April 2, One hundred of these patients received fibrin 2006. glue over a 1-year period from August of 2004 to Copyright ©2007 by the American Society of Plastic Surgeons September of 2005 and were followed prospec- DOI: 10.1097/01.prs.0000278092.28351.c9 tively. Another 100 patients from the previous year

www.PRSJournal.com 1045 Plastic and Reconstructive Surgery • September 15, 2007

(August of 2003 to August of 2004) who had not received fibrin glue had their charts reviewed ret- rospectively and/or were interviewed by means of telephone. All patients underwent bilateral face lifts using the deep plane technique, as previously described by the senior surgeon (F.M.K.),17 which also involves skin undermining and large skin flaps at multiple levels, including the preauricular region, postauricular region, and the neck. All procedures were performed by the same surgeon (F.M.K.). The only change made in performing the operation re- lates directly to the use of the fibrin glue. The following technique was used for patients receiving the fibrin glue. The fibrin sealant is re- constituted with a mixture made from fibrinogen, Fig. 2. The surgeon must ensure that the flaps are held firmly for factor XIII, aprotinin, calcium chloride, and 3 minutes after application of the fibrin glue. thrombin. The thrombin is diluted to a concen- tration of 5 IU/ml. Using a nitrogen tank, an even application of the fibrin sealant is ensured for a small volume (1 ml) on each side (Fig. 1). In addition to the fibrin glue being applied to the tem- poral and cheek regions (as with previous studies), the sealant is also applied under the large skin flaps in the postauricular region and neck. A total of 3 minutes is allotted for holding the skin flaps down once the glue is sprayed (Fig. 2). Thereafter, the skin is excised and sutured in sequential fashion. No drains are used (Fig. 3). To apply moderate com- pression and wound coverage, a light protective dressing is frequently applied for a day or two before having the patients wash their hair and face. Com- parisons were made with regard to hematoma rate, seroma rate, levels of induration/edema/ecchymo- Fig. 3. The skin flaps are sequentially excised and sutured fol- sis, pain levels, and patient satisfaction. Proportions lowing application of the fibrin glue. were compared using Fisher’s exact test. Means were compared using two-sample t tests. RESULTS Two hundred patients were studied. The 100 fibrin glue patients consisted of six men and 94 women. Their age range was 45 to 81 years (mean, 58 years). The 100 non–fibrin glue patients con- sisted of four men and 96 women. Their age range was 45 to 78 years (mean, 59 years). A drain was placed in the first patient in which fibrin glue was applied. Thereafter, no drains were used in the fibrin glue group. All non–fibrin glue patients had drains placed. The patients were evaluated post- operatively at 24 hours, 48 hours, 1 week, 1 month, and 3 months. The following data were observed for fibrin glue patients versus non–fibrin glue pa- tients: expanding hematoma rate, 1 percent versus 3 percent (p Ͼ 0.05); localized hematoma rate, 2 Fig. 1. The mixture is evenly sprayed using a nitrogen gas tank percent versus 3 percent (p Ͼ 0.05); seroma rate, source. 1 percent versus 7 percent (p Ͼ 0.05); and pro-

1046 Volume 120, Number 4 • Fibrin Glue in Rhytidectomy

Table 1. Results therefore presenting more realistic data, espe- Fibrin Glue Non–Fibrin cially because such patients have been observed to ,have a higher risk of hematoma. In this 1994 study (100 ؍ Glue (n (100 ؍ n) Expanding hematoma* 1% 3% Marchac purported the use of fibrin glue as ben- Localized hematoma* 2% 3% eficial toward reducing hematomas, lowering the Seroma* 1% 7% incidence of edema and ecchymosis, and elimi- Prolonged induration, edema, and nating drains and postoperative dressings. It is ecchymosis† 0% 22% surprising that the most recent article by Marchac Pain* 100% minimal 95% minimal and Greensmith21 contradicts their initial find- 5% moderate ings. Although it was a prospective study, there Satisfaction score (1–10)* 9.5 9.0 were only 30 patients studied. It was unclear why *p Ͼ 0.05. Marchac would change his thinking after 17 years †p Ͻ 0.001. of usage based on such a small study. He stated that cost was an issue. He used 5 ml of the product, whereas we have found a total of 2 ml to be more longed induration, edema, and ecchymosis, 0 per- cost effective and sufficient. Overall, the study by Ͻ cent versus 22 percent (p 0.001) (Table 1). The Marchac and Greensmith was unclear because, in score for pain for fibrin glue patients versus non– the end, they still advocated the use of the fibrin fibrin glue patients was 100 percent minimal ver- glue for high-risk patients such as agitated pa- sus 95 percent minimal and 5 percent moderate Ͼ tients, hypertensive patients, and male patients. (p 0.05). The average score for patient satisfac- This study has shown that drains are no longer tion (scale ranging from 1 to 10, with 10 being needed. A drain was used in our first fibrin glue best) for fibrin glue patients versus non–fibrin Ͼ patient for a sense of security. However, no drains glue patients was 9.5 versus 9.0 (p 0.05). were used thereafter. The senior surgeon also did not use drains in a 1984 retrospective study of 512 DISCUSSION non–deep plane rhytidectomies.22 The presence Fibrin sealant has been used successfully in of a drain stimulates fluid accumulation and re- many fields of surgery. It has been approved by the moves unwanted excess exudates and blood. In U.S. Food and Drug Administration for colostomy addition, their presence and negative pressure can closure, cardiopulmonary bypass, and splenic sur- disrupt the action of the fibrin glue. Fibrin glue gery. Its use in aesthetic surgery, especially rhyti- may reduce the incidence of expanding hema- dectomy, has been less widespread. The use of toma. Although not statistically significant, the fibrin glue has been associated with some benefits expanding hematoma rate (those requiring evac- for rhytidectomy.18 Several studies have used fibrin uation within the first 24 hours) showed a differ- glue for hemostasis. Bruck4 and Oliver et al.19 ence: 1 percent for fibrin glue patients versus 3 found decreased suction drainage and decreased percent for non–fibrin glue patients. It should be swelling, yet their studies were small. Our study noted that the one fibrin glue patient who did included a large number of patients: 200. Another experience an expanding hematoma was a man. strength of our study was the prospective nature in The localized hematoma rate (hematoma requir- which 100 patients received fibrin glue and were ing office aspiration after the first 24 hours) was followed closely. These patients were controlled by similar: 2 percent for fibrin glue patients versus 3 comparing them with 100 non–fibrin glue pa- percent for non–fibrin glue patients. Both of the tients. Our study also differed from other studies fibrin glue patients experiencing a localized he- in the more comprehensive application of the matoma had a history of hypertension, and one of product. For instance, Bruck only sprayed the fi- those two was a man with a postoperative blood brin glue in the cheek region. We used the glue in pressure of 190/110 mmHg. The other was a multiple areas, including the cheek, postauricular, woman who had a blood pressure of 170/100 and neck regions. The study by Marchac and mmHg postoperatively and may have been nutri- Sandor20 was a large study similar to ours. How- tionally depleted as suggested by hyponatremia in ever, several differences should be noted. Their her blood work. The difference in seroma rate (1 study appeared to be entirely retrospective. Mar- percent for fibrin glue patients versus 7 percent chac’s study also had several exclusion criteria, for non–fibrin glue patients) neared statistical sig- such as male sex, smokers, history of hypertension, nificance (p ϭ 0.06) and was definitely clinically and revision cases. Our study incorporated all pa- significant. This is in contrast to Matarasso and tients and had no such exclusion parameters, Rizk, who found that despite the fibrin glue, “small

1047 Plastic and Reconstructive Surgery • September 15, 2007 fluid collection(s) required needle aspiration in levels, which showed no significant difference be- the office.”23 Nonetheless, they found the fibrin tween both groups. The decreased seroma rate glue to be very useful in short flap rhytidectomies and the decreased level of induration, ecchymosis, as well.24 The most remarkable observation was the and edema may point to the fibrin glue’s benefits difference between both groups for prolonged of closing dead space and stimulating the clotting induration, ecchymosis, and edema beyond 2 factors of the coagulation cascade. We have noted weeks (0 percent versus 22 percent, p Ͻ 0.05). This an impressive immediate decrease in postopera- was manifested by the complete elimination of the tive swelling. This may be attributable to the sup- need for postoperative treatments for residual pression of the normal exudative phase of wound lumps and bumps. Another point is that of the 100 healing by the artificial seal (Fig. 5). We have also patients in whom the fibrin glue was used, five hypothesized that other factors, such as wound- were men, and the expanding hematoma oc- healing factors, may also be stimulated. On a sub- curred in one of those five patients. Men are jective level, all patients receiving fibrin glue, even known to be at a higher risk for expanding he- a few hours postoperatively, generally appeared matoma. One might speculate that this complica- more comfortable, happier, and less downtrod- tion could have been higher in the men had the den. The fibrin glue appears to augment healing, fibrin glue not been used (Fig. 4). Other objective as the patients’ appearance at 1 week is often data measured were patient satisfaction and pain comparable to that of non–fibrin glue patients at

Fig. 4. A male patient benefiting from the fibrin glue for rhytidectomy. (Above, left) Preoperative view. (Above, right) One day postoperatively. (Below, left) One week postoperatively. (Below, right) One month postoperatively.

1048 Volume 120, Number 4 • Fibrin Glue in Rhytidectomy

Fig. 5. A fibrin glue patient (left) preoperatively and (right) 2 days postoperatively shows minimal edema and ecchymosis.

3 weeks (Figs. 6 through 8). A more objective study side. The time of holding the skin flaps down evaluating this, such as quantifying growth factors in should be 3 minutes, and the technique of hold- serum, may be considered in the future. Confirma- ing the flaps should be precise. Anecdotally, we tory feedback has also come from revision rhytidec- have heard of surgeons not experiencing good tomy patients who express that their postoperative results with the fibrin glue. This may be because course using fibrin glue was much smoother and of inappropriate dilution, too little or too much more comfortable than their previous experience fibrin glue, and improper technique. We believe without the fibrin glue. that we have addressed these points with metic- Important points should be made regarding ulous detail, and we have not experienced any the correct application of the fibrin glue. The complications with the fibrin glue. operating surgeon must adhere strictly to the It is noteworthy to mention the potential con- mixing and application suggestions offered by cern about virus and prion transmission because the manufacturer (Baxter, Deerfield, Ill.). The human blood is used to prepare the fibrin glue. thrombin should be diluted from 500 IU/ml to However, the human fibrinogen is heat-treated to 5 IU/ml. The amount of glue should be 1 ml per 60ºC, which is known to inactivate the human

Fig.6. Afibringluepatient(left)preoperativelyand(right)1weekpostoperativelyshowsminimaledemaand ecchymosis.

1049 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 7. A fibrin glue patient (left) preoperatively and (right) with minimal edema and ecchymosis at 1-week follow-up.

Fig. 8. A fibrin glue patient (left) preoperatively, (center) 1 week postoperatively, and (right) 2 weeks postoperatively demonstrating a smooth course, with minimal edema and ecchymosis.

T-lymphotropic type III virus.13 The repeated ever, there has been no evidence of prion infec- screening of blood donors and the finished prod- tion or hypersensitivity by means of blood transfer. uct for antiviral antibodies is an additional safety Nonetheless, precautions are undertaken, as the measure.18 A recent study into the risk of trans- bovine donor specimen is certified, and the apro- mission of infective viruses such as hepatitis B and tinin is of non–central nervous system origin. An- C, human immunodeficiency virus, and human other preventive measure against potential prion T-lymphotropic virus, found no cases in over infection is that certain human donors are ex- 20,000 blood transfusions.25 The only case re- cluded such as Creutzfeldt-Jakob disease patients ported of viral transmission was parvovirus B19. and all neurosurgical patients. Donor blood is now screened for this. Aprotinin is Limitations of the product should be ad- the fibrinolysis inhibitor isolated from a bovine dressed. The cost of the product is a consideration source, which may be a cause for concern. How- (typically $250 per 3 cc). Additional operating

1050 Volume 120, Number 4 • Fibrin Glue in Rhytidectomy room time is another factor. The surgeon takes 6. Staindl, O. Die Gewebeklebung mit hochkonzentriertem, time to apply the product and to apply pressure humanen Fibrinogen am Beispiel der freien, autologen afterward. This may also break the flow of the Hauttransplantation. Arch. Otorhinolaryngol. 217: 219, 1977. 7. Staindl, O. The healing of wounds and scar-formation under operation. The product also should not be per- the influence of a tissue adhesion system with fibrinogen, ceived as a definitive protectant against hema- thrombin, and coagulation factor XIII. Arch. Otolaryngol. 222: toma. It should not supplant adequate hemostasis. 241: 1979. 8. Marczell, A., Efferdinger, F., Spoula, H., and Stierer, M. CONCLUSIONS Anwendungsbereiche des Fibrinklebers in der Abdominal- The use of fibrin glue was associated with some chirurgie. Acta Chir. Aust. 11: 137, 1979. benefits for rhytidectomy. Fibrin glue eliminated 9. Matras, H., Braun, F., Lassmann, H., Ammerer, H. P., and Mamoli, B. Plasma clot welding of nerves. J. Maxillofac. Surg. the use of drains. The difference in expanding 4: 236, 1973. hematoma was not statistically significant but was 10. Bruck, H. G. Fibrin tissue adhesion and its use in rhytidec- clinically significant. The seroma rate was de- tomy: A pilot study. Aesthetic Plast. Surg. 6: 197, 1982. creased and neared statistical significance. The 11. Holle, J., Freilinger, G., and Mandl, H. The use of a fibrin fibrin glue was most advantageous in eliminating adhesive system in plastic surgery. In J. F. Ely (Ed.), Trans- prolonged induration, edema, and ecchymosis. actions of the Seventh International Congress of Plastic and Recon- structive Surgery. Rio de Janeiro: Sociedade Brasileira de The fibrin glue appears to promote wound heal- Cirurgia Plastica, 1979. ing, suggested by a subjectively smoother postop- 12. Mandel, M. A. Closure of blepharoplasty incisions with au- erative course. The wound-healing growth factors tologous fibrin glue. Arch. Ophthalmol. 108: 842, 1990. could be quantified in a future study. The senior 13. Marchac, D., Pugash, E., and Gault, D. The use of sprayed author believes that the use of fibrin glue in face fibrin glue for face lifts. Eur. J. Plast. Surg. 10: 139, 1987. lifting has overwhelmingly been shown to reduce 14. Rheims, D., Meyer, R., and Daverio, P. J. Application de la some of the morbidity and severe complications of colle fibrine en chirurgie plastique, reconstructive et esthe- tique cervicofaciale. Ann. Chir. Plast. Esthet. 31: 384, 1986. this frequently performed operation. This study 15. Toledo, L. S. Blepharoplasty with fibrin seal. In H. B. Williams has clearly shown that in one surgeon’s long-ex- (Ed.), Transactions of the VIIIth International Congress of Plastic and perienced hands, with one patient population and Reconstructive Surgery. Montreal: McGill University, 1983. with one surgical and gluing technique, the use of 16. Germani, G., Passarino, M., Datta, G., D’Agostino, G., Grach- fibrin glue is an effective and useful adjunct to ero, E., and Casale, A. Utilizzazione della colla di fibrina in face-lifting surgery. chirurgia plastica. Riv. Ital. Chir. Plast. 14: 443, 1982. 17. Kamer, F., and Frankel, A. SMAS rhytidectomy vs. deep plane Davis B. Nguyen, M.D. rhytidectomy: An objective comparison. Plast. Reconstr. Surg. The Lasky Clinic 102: 3, 1998. 201 South Lasky Drive 18. Fezza, J. P., Cartwright, M., Mack, W., and Flaharty, P. The Beverly Hills, Calif. 90212 use of aerosolized fibrin glue in face-lift surgery. Plast. Re- [email protected] constr. Surg. 110: 658, 2002. 19. Oliver, D. W., Hamilton, S. A., Figle, A. A., Wood, S. H., and DISCLOSURE Lamberty, B. G. A prospective, randomized, double-blind Neither of the authors has a financial interest in any trial of the use of fibrin sealant for face lifts. Plast. Reconstr. of the products, devices, or drugs mentioned in this article. Surg. 108: 7, 2001. 20. Marchac, D., and Sandor, G. Face lifts and sprayed fibrin REFERENCES glue: An outcome analysis of 200 patients. Br. J. Plast. Surg. 47: 306, 1994. 1. Flemming, I. Fibrin glue in face lifts. Facial Plast. Surg. 8: 1, 21. Marchac, D., and Greensmith, A. L. Early postoperative ef- 1992. ficacy of fibrin glue in face lifts: A prospective randomized 2. Matras, H., Dinges, H. P., Lassmann, H., and Mamoli, B. Zur trial. Plast. Reconstr. Surg. 115: 3, 2005. nahtlosen interfaszikularen Nerventransplantation im Tier- 22. Kamer, F., Churukian, M., and Damiani, J. 512 rhytidecto- experiment. Wien Med. Wochenschr. 122: 517, 1972. 3. Spangler, H. P., Braun, F., Holle, J., Moritz, E., and Wolner, mies: A retrospective study. Arch. Otolaryngol. 110: 368, 1984. E. Die locale Anwendung von Fibrinogen und Kollagen zur 23. Matarasso, A., and Rizk, S. Use of fibrin sealant in short scar face Blutstillung in der Herzchirurgie. Wien Med. Wochenschr. 126: lift. In R. Saltz and D. Toriumi (Eds.), Tissue Glues in Cosmetic 86: 1976. Surgery. St. Louis: Quality Medical, 2004. Pp. 133–147. 4. Scheele, J., Muhe, E., and Wopfner, F. Fibrinklebung-eine 24. Matarasso, A., Rizk, S., and Markowitz, J. Short scar facelift neue Behandlungsmethode beim persistierenden und rez- with use of fibrin sealant. Dermatol. Clin. 23: 495, 2005. idivierenden Spontapneumothorax. Chirurg 49: 236: 1978. 25. Regan, F., Hewitt, P., Barbara, J. A., and Contreras, M. 5. Gastpar, H., Kastenbauer, E. R., and Behbehani, A. A. Erfahr- Prospective investigation of transfusion transmitted infec- ungen mit einem humanen Fibrinkleber bei operativen Ein- tion in recipients of over 20 000 units of blood. B.M.J. 320: griffen im Kopf-hals-bereich. Laryngol. Rhinol. 58: 389, 1979. 403, 2000.

1051 DISCUSSION Experience with Fibrin Glue in Rhytidectomy Charles H. Thorne, M.D. New York, N.Y.

he authors present a series of 200 face-lift pro- The same applies to the 22 percent incidence of Tcedures by a single surgeon in an effort to eval- prolonged induration, edema, and ecchymosis in the uate the extent to which fibrin glue reduces face-lift non–fibrin glue group. I am familiar, and I suspect all morbidity. Half of the patients received fibrin glue surgeons are familiar, with prolonged induration in the without drains and were evaluated prospectively. neck in patients who have undergone open neck pro- The remaining half received no fibrin glue, had cedures with unevacuated or incompletely evacuated drains, and were evaluated retrospectively. hematomas. It is hard to imagine a 22 percent inci- Despite the subjective sense of the senior author, dence of prolonged induration, however. The swelling an experienced face-lift surgeon, that glue reduces that normally occurs after face lifting and exists in the the morbidity of the procedure, there was no statis- 3-week to 3-month postoperative period is generally tical difference between the fibrin glue and non– one that obscures wrinkles and that the patients find fibrin glue groups in terms of expanding hematoma, desirable, not one of firm induration for which the localized hematoma, or seroma. In addition, there surgeon is seeking a cure. was no statistical difference in pain or patient satis- The illustrations are not especially helpful, faction. There was, however, a statistically significant showing excellent postoperative results but with- reduction in prolonged induration, edema, and ec- out comparison with any non–fibrin glue patients. chymosis from 22 percent in the non–fibrin glue The amount of discoloration and swelling exhib- group to 0 percent in the fibrin glue group. ited by these patients is approximately what I The study provides more data than previous would expect in my best cases (not my average publications regarding the efficacy of fibrin glue cases) without the use of fibrin glue. in face lifting but has several weaknesses that make In summary, the authors are to be commended it difficult to draw the definitive conclusions cited for compiling such a large series. It is precisely this by the authors. First, the study design was not type of busy, single-surgeon study that is required to blind. The surgeons knew which patients received answer clinical questions of this type. We thank them fibrin glue and could have, whether consciously or for submitting these data to our Journal. The data are not, paid more attention to hemostasis in these insufficient, however, to support the conclusion that patients than in the non–fibrin glue patients. glue has been “overwhelmingly shown to reduce The two groups were similar in terms of age and some of the morbidity and severe complications of sex distribution, but what about blood pressure? Be- face lifting.” In addition, the conclusion that fibrin cause postoperative blood pressure control is now glue “appears to promote wound healing” is not considered the single most important factor in re- warranted from the data presented. ducing hematoma rate, it would be important to The ultimate answer regarding the efficacy of know how the two groups compared in this regard. fibrin glue after face lifting, if we ever get one, will Other comparative data would be helpful. For require a prospective, blinded study, where nei- example, what percentage of non–fibrin glue versus ther the surgeon nor the patient is aware of fibrin glue patients underwent an open procedure whether the material used is glue or placebo. In on the neck? Most surgeons feel that such patients the meantime, the reader is left to envy the au- have a higher incidence of hematoma than those thor’s good surgical results and to decide whether with lateral access only, and a difference in the two this study is compelling enough to abandon drains groups could influence the result. and buy glue. Although the study suggests a ben- The non–fibrin glue group had a 7 percent in- efit, my gut tells me to stick with drains. cidence of “seroma.” I am familiar with numerous types and extents of hematoma after face lift but do DISCLOSURE not think I have encountered a seroma of the type The author has no financial interests in any of the one associates with abdominoplasty. I am not as sur- drugs, devices, or products described in the discussion or prised by the low rate of seroma with fibrin glue as in the discussed article. I am with the high rate without fibrin glue. Charles H. Thorne, M.D. Received for publication April 8, 2006. New York University School of Medicine 812 Park Avenue Copyright ©2007 by the American Society of Plastic Surgeons New York, N.Y. 10021 DOI: 10.1097/01.prs.0000278002.74585.8d [email protected]

1052 www.PRSJournal.com COSMETIC

Chin Surgery VI: Treatment of an Unusual Deformity, the Tethered Microgenic Chin

Jason A. Spector, M.D. Background: Although the condition is rare, some children are born with Stephen M. Warren, M.D. cervical clefts or masses that require repair during infancy. The scarring in the Barry M. Zide, M.D., submental region can tether the developing mandible at the menton, producing D.M.D. a developmental microgenia or “tethered chin.” New York, N.Y. Methods: A retrospective review of the senior author’s (B.M.Z.) patient records was performed; three cases of tethered chin were identified. In each case, a staged surgical approach was used. Results: In two cases, previous unsuccessful surgery complicated the initial presentation. In all cases, the underlying soft-tissue anomalies were addressed and the microgenia was corrected. Satisfactory aesthetic and functional results were obtained. Conclusions: The tethered chin represents a rare entity. Correction of the tethered chin requires a comprehensive understanding of the underlying ab- normality and an appreciation of the multiple factors that contribute to chin function and aesthetics. (Plast. Reconstr. Surg. 120: 1053, 2007.)

lastic surgeons are often consulted for treat- also because there are associated soft-tissue defi- ment of microgenia. Small chins may be de- ciencies that need to be addressed. Further- ficient sagittally, vertically, or occasionally more, many of these patients have a history of P 1,2 some combination of the two. Although pa- previous chin and neck surgery. tients commonly present with an isolated com- In this article, we report on three cases of teth- plaint of having a small chin, microgenia may ered chins. Reflecting the heterogeneous presen- also occur with or secondary to certain craniofa- tation of this entity, each case is approached in a cial abnormalities.3 When the deficiency is mild, unique fashion depending on the degree of bony an appropriately placed alloplastic implant or and soft-tissue deficiency and history of previous advancement genioplasty may provide a pleasing surgery. We demonstrate that with careful consid- aesthetic result.1,4,5 More severe and unusual de- eration of these factors, the tethered and micro- ficiencies may require combinations of treat- genic chin can be corrected with gratifying results. ments to achieve an appropriate result.6 Rarely, microgenia results from a deficiency of PATIENTS AND METHODS growth caused by extrinsic factors that prevent A retrospective review of the senior author’s normal anterior movement of the chin. Com- (B.M.Z.) patient records over the past 5 years was monly, these chins are tethered secondary to performed. Three cases of tethered chin were iden- scarring from a full-thickness burn.7–10 Alterna- tified. Evaluation of chin aesthetics and projec- tively, the restrictive force may be secondary to a tion was made according to the senior author’s central fibrous band that is either congenital in previously published algorithm (Chin Surgery I: nature or that forms subsequent to surgery per- QUAC analysis).4 In general, chin projection was formed in the midline of the neck in infancy.11–13 determined by the position of a vertical line dropped These cases can be extremely challenging not from the labial surface of the lower incisors. In each only because the microgenia is often severe but case, a staged surgical approach was used to correct the tethering and associated microgenic chin defor- From the Weill Cornell Medical College and the Institute of mity. Patients were followed for a minimum of 6 Reconstructive Plastic Surgery, New York University School months after their last surgical procedure. of Medicine. Received for publication February 16, 2006; accepted May CASE REPORTS 3, 2006. Case 1 Copyright ©2007 by the American Society of Plastic Surgeons A 15-year-old girl was born with a midline cervical cleft and DOI: 10.1097/01.prs.0000278003.44931.34 underwent a soft-tissue neck Z-plasty in infancy. At age 9, the

www.PRSJournal.com 1053 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 3. Lateral cephalogram of the patient in case 1 taken after the initial corrective surgery. After performing a jumping genio- plasty, the mobilized segment was fixated to the proximal man- dible with screws.

some of the lower mentalis. The patient stated that she had to make a conscious effort to close her lips. Radiographs showed bony erosion below the incisor roots with an osteophytic muscle pull bone spur at the inferior symphysis (Fig. 1). She had already had orthodontic treatment and her occlusion was stable and acceptable. On physical examination, there was a marked chin deficiency with midline cervical scarring that pulled on the central lower chin on neck elevation. The two implants were easily palpated and mobile (Fig. 2). Fig. 1. Case 1. (Above) An osteophytic bone spur at the inferior Operative Approach symphysis (arrow) is evident on the lateral cephalogram. (Below) In stage 1, both previously placed implants were removed Bone erosion (secondary to previous alloplastic implant place- and an advancement jumping genioplasty was performed. The ment) is clearly seen below the incisor roots (arrows). posterior aspect of the distal segment was fixated to the anterior portion of the proximal mandible with screws (Fig. 3). In stage 2 (1 year after stage 1), the soft tissue of the neck patient’s severe micrognathia was treated with a silicone chin was released, Z-plasties were performed, and a high-density implant. A second silicone implant was placed on top of the first porous polyethylene implant (implant height reduced) was at age 12. In the years since her implants were placed, bone screwed onto the advanced pogonion to provide an additional erosion occurred and the top implant slid cephalad, detaching 6 mm of projection (Fig. 4).

Fig. 2. Case 1. Preoperative anteroposterior and lateral views (with implants in place). Marked chin deficiency is evident (even with two stacked alloplastic implants), as is significant midline scarring.

1054 Volume 120, Number 4 • Tethered Microgenic Chin

high-density porous polyethylene implant (from which the top half was removed so that projection would be maximal at the pogonion) was secured in place with four screws (Fig. 7). Case 3 A 17-year-old boy underwent excision of a thyroglossal duct cyst in infancy with subsequent Z-plasty of the neck. He presented with neck tightness on head elevation. There was no history of prior jaw surgery, but he had undergone orthodontia with bicuspid extrac- tion in all quadrants. The patient had a very tight neck with a prominent central band extending from the mid chin to the thyroid cartilage (Fig. 8). A lateral cephalogram demonstrated a deficient chin with an osteophyte present at the inferior symphysis, suggestive of tight muscle attachments (Fig. 9). Operative Approach In stage 1, a transverse neck incision closed vertically with Z-plasty and muscle detachment from the lower symphysis was performed. A Z-plasty was performed on the platysma. In stage 2 (8 months after stage 1), a jumping advancement genioplasty was performed with the back edge of the distal segment stabi- lized against the proximal segment with four screws (Fig. 10). After surgery, kenalog was injected into the scar.

DISCUSSION Microgenia is a common anomaly that often presents as an isolated condition. Occasionally, lack of chin projection results from tethering of the chin to a midline cervical band that occurs secondary to an injury (i.e., burn contracture)7–10 Fig. 4. Case 1. Final postoperative anteroposterior and lateral or surgery of the same area during infancy (e.g., views. Both chin projection and neck contour have improved. for midline thyroglossal duct or cervical cleft).11–13 The resultant midline scar may serve as a tether, preventing normal anterior growth of the chin. It Case 2 is also possible that some of the growth distur- A 27-year-old man was born with a cervical cleft. The patient bance is related to the original midline abnormal- underwent a corrective procedure as an infant and subse- ity. The cases presented in this article represent quently had chin advancement surgery that he said caused his lower teeth to show. He sought further corrective surgery but the heterogeneous presentation of the tethered was advised by multiple surgeons that he was “finished” and chin. This is a rare entity; these three cases were should have no further surgery. He was taking antidepressant collected over 5 years by the senior author, whose medication and in therapy. On physical examination, there was practice sees a fairly large volume of chin-related deficient chin projection with (surgical) tethering scars present problems. The microgenia ranges from moderate on the neck. The gingiva of the lower incisors was visible at rest. The sulcus was low and scarred and there was only fair function to severe; in one case, the chin was “virgin,” of the mentalis muscle (Fig. 5, above). The lateral cephalogram whereas in the two other cases there had been showed the advanced segment with excess menton below the failed corrective attempts and other iatrogenic level of the advanced segment (Fig. 5, below). problems. In each case, a staged surgical approach Operative Approach was used to correct the tethering and associated In stage 1, the mentalis was resuspended (using Mitek an- microgenic chin deformity to prevent devascular- chors placed high on the alveolus between the central incisors ization of the advanced segment that might occur and between the central and right lateral incisors) with con- with concomitant significant soft-tissue mobiliza- comitant subperiosteal release of the soft tissue from first bi- tion and osteotomy. cuspid on the right to the first bicuspid on the left along with 4 cm of skin undermining over the platysma. A V-Y advance- In the first case presented, initial surgical plan- ment was performed in the neck to further release the soft ning was doomed to failure based on external tissue. Chin support was used postoperatively during the day for forces acting on the implants. The implants them- 1 week and at night for 1 month (Fig. 6). selves, placed in an unorthodox stacked fashion, In stage 2 (6 months after stage 1), submental exposure was resulted in further erosion of the underlying used for neck scar Z-plasties and release of the submuscular scar tissue. By means of a submental approach, excess bone below bone. Disruption of the mentalis muscle attach- the lowest level of the previously advanced segment was burred ments worsened the patient’s appearance and down to provide normal chin height and pogonion position. A threatened oral competence. The scarred soft tis-

1055 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 5. Case 2. Preoperative views. (Above, left) There is excessive lower incisor show as a result of previous operations. (Above, right) Scars are present on the neck from previous operations. (Below) The lateral cephalogram demonstrates the previously advanced segment with excess menton below the level of the advanced segment. Although pogonial projection is good, it is located too high on the chin.

Fig. 6. Case 2. Postoperative appearance of the patient after the first stage. Note the improved position of the lower lip at rest. The chin projection is adequate. The soft-tissue tether, however, will require further revision in a second stage.

1056 Volume 120, Number 4 • Tethered Microgenic Chin

Fig. 7. Case 2. Final postoperative appearance. Note the improved cervicomental angle. sue of the neck that was presumably the primary improved projection, and the mentalis muscle was cause of the tethering was not addressed. reattached at an anatomically appropriate posi- The corrective surgical plan, carried out in two tion to improve its function. In the second stage, steps, was performed to provide a foundation for the soft-tissue tether was released. To provide ad-

Fig. 8. Case 3. Preoperative views show the significant midline tethering cord that nearly obliterates the cervicomental angle and restricts neck extension (above). There is poor chin projection (below).

1057 Plastic and Reconstructive Surgery • September 15, 2007

alloplastic implant. The removal of the significant subpogonial bone reduced chin height appropri- ately and allowed for tension-free cover of the allo- plastic implant without negatively affecting the lip. This case demonstrates several of the tech- niques outlined in our previous “chin” articles: the advantages conferred by the extraoral approach to the chin,14,15 the importance of the integrity of the mentalis muscle,16 the need to custom contour implants before placement,17and the soft-tissue adjustments essential to optimizing chin and neck contour.15 The final patient presented was the only one not to have undergone a previous attempt to correct the Fig. 9. Lateral cephalogram demonstrating deficient chin pro- tethering. As a result, correction was more straight- jection with an inferior symphyseal osteophyte secondary to the forward; in the first stage the soft-tissue tether was tethering cord (arrow). treated, and in the second stage, the deficient pro- jection was improved with an advancement jumping genioplasty (the order of which problem was ad- ditional and stable projection, a high-density po- dressed first was inconsequential). rous polyethylene implant (height reduced) was placed and fixated with screws, giving the patient a satisfactory result (Fig. 4). In this case, an allo- CONCLUSIONS plastic implant was selected to obviate the need to Three dissimilar cases of tethered chin are saw through previously placed screws (which presented with three varying methods of correc- would be mandatory if an osseous genioplasty tion based on history and abnormality. In all cases, were performed). both the soft-tissue tether and the deficient pro- In the second case, the initial aim was to cor- jection were addressed successfully. rect the deformity created by previous operations. Barry M. Zide, D.M.D., M.D. In the first stage, by means of an intraoral route Division of Plastic Surgery with extensive undermining, the mentalis muscle 420 East 55th Street, Suite 1D was resuspended to its anatomically appropriate New York, N.Y. 10022 position just below the dental cervices. In the sec- [email protected] ond stage, release of the tethering submental soft tissue was performed while projection was aug- DISCLOSURE mented by precise placement of a reduced height The authors have no financial interests to disclose.

Fig. 10. Case 3. Postoperative views show the increased chin projection and the improvement in the cer- vicomental angle. The slightly hypertrophic scar is currently being treated with steroid injections.

1058 Volume 120, Number 4 • Tethered Microgenic Chin

REFERENCES 9. Nahlieli, O., Kelly, J. P., Baruchin, A. M., et al. Oro-maxil- lofacial skeletal deformities resulting from burn scar con- 1. McCarthy, J. G., Ruff, G. L., and Zide, B. M. A surgical system tractures of the face and neck. Burns 21: 65, 1995. for the correction of bony chin deformity. Clin. Plast. Surg. 10. Chen, T. M., Wang, H. J., and Chou, T. D. Correction of 18: 139, 1991. retrusive chin in the reconstruction of face and neck burns 2. McCarthy, J. G. Microgenia: A logical surgical approach. Clin. using sliding genioplasty. Burns 31: 918, 2005. Plast. Surg. 8: 269, 1981. 11. Wood, G. A., and Deister, E. Anterior midline neck webbing 3. McCarthy, J. G., Grayson, B. H., Colen, S. R., Coccaro, P. with microgenia and symphyseal exostosis. Oral Surg. Oral J., and Wood-Smith, D. Surgery of the jaws. In J. G. Mc- Med. Oral Pathol. 56: 128, 1983. Carthy (Ed.), Plastic Surgery. Philadelphia: Saunders, 1990. 12. Mlynarek, A., Hagr, A., Tewfik, T. L., et al. Congenital mid- P. 1188. line cervical cleft: Case report and review of literature. Int. 4. Zide, B. M., Pfeifer, T. M., and Longaker, M. T. Chin surgery: J. Pediatr. Otorhinolaryngol. 67: 1243, 2003. I. Augmentation—The allures and the alerts. Plast. Reconstr. 13. Daw, J. L., Jr., and Patel, P. K. Double-opposing Z-plasty for Surg. 104: 1843, 1999. correction of midline cervical web. J. Craniofac. Surg. 14: 774, 5. Guyuron, B., and Raszewski, R. L. A critical comparison of 2003. osteoplastic and alloplastic augmentation genioplasty. Aes- 14. Zide, B. M., and Longaker, M. T. Chin surgery: II. Submental thetic Plast. Surg. 14: 199, 1990. ostectomy and soft-tissue excision. Plast. Reconstr. Surg. 104: 6. Sclaroff, A., and Williams, C. Augmentation genioplasty: 1854, 1999. When bone is not enough. Am. J. Otolaryngol. 13: 105, 1992. 15. Spector, J. A., Warren, S. M., and Zide, B. M. Chin IV: Treat- 7. Masson, C. L., and Janvier, H. Dento-maxillo-facial deformi- ment of the large chin: Analytic insights for improving out- ties following cicatricial retractions of the neck, sequelae of comes. Plast. Reconstr. Surg. 120: 530, 2007. burns in childhood. Ann. Chir. Plast. 17: 254, 1972. 16. Zide, B. M. The mentalis muscle: An essential component of 8. Katsaros, J., David, D. J., Griffin, P. A., et al. Facial dysmor- chin and lower lip position. Plast. Reconstr. Surg. 105: 1213, 2000. phology in the neglected paediatric head and neck burn. 17. Zide, B. M., and Boutros, S. Chin surgery III: Revelations. Br. J. Plast. Surg. 43: 232, 1990. Plast. Reconstr. Surg. 111: 1542, 2003.

PRS Mission Statement The goal of Plastic and Reconstructive Surgery௡ is to inform readers about significant developments in all areas related to reconstructive and cosmetic surgery. Significant papers on any aspect of plastic surgery—original clinical or laboratory research, operative procedures, comprehensive reviews, cosmetic surgery—as well as selected ideas and innovations, letters, case reports, and announcements of educational courses, meetings, and symposia are invited for publication.

1059 COSMETIC

Versatility of the Superomedial Pedicle in Managing the Massive Weight Loss Breast: The Rotation-Advancement Technique

Albert Losken, M.D. Background: Management of the breast following massive weight loss is chal- Daniel J. Holtz, M.D. lenging. Specific issues include an unstable envelope (skin laxity) and an un- Atlanta, Ga. stable mound (decent and volume loss). The evolution of a technique is pre- sented. Methods: A retrospective review of all massive weight loss patients who under- went superomedial pedicle mastopexy techniques was performed. The current procedure involves incorporating the lower pole of the breast and rotating it superiorly. The lateral breast flap is then advanced medially and plicated. This essentially (1) autoaugments the upper pole, (2) narrows the wide breast, (3) provides an internal sling, and (4) redefines and secures the inframammary fold. Results: Thirty-five patients were included in the series. The average body mass index was 26.5, and the average weight loss was 121 pounds. Six patients (17 percent) had mastopexy augmentation. Wise pattern skin takeout was per- formed in 89 percent of patients. The revision rate for the series was 11 percent. The average follow-up was 1.7 years. Conclusions: The superomedial pedicle is a versatile, well-vascularized pedicle that allows for glandular plication of the lower pole and autoaugmentation of the upper pole once rotated. Parenchymal shaping through plication and sus- pension of the breast mound should improve breast shape over time, theoret- ically reducing the incidence of recurrent ptosis as breast shape relies less on the often inelastic skin envelope. It applies a familiar and reliable technique, with certain modifications, to improve results and maintain shape in the long, deflated, massive weight loss breast. (Plast. Reconstr. Surg. 120: 1060, 2007.)

ariatric surgery continues to offer the great- nancy, and gravity, those following massive weight est degree of sustained weight loss to the loss pose additional challenges. Numerous physio- Bmorbidly obese patient.1 As plastic surgeons logic and anatomical factors exist, and the tradi- embrace the growing need for body contouring tional mastopexy reduction techniques are often procedures, we are beginning to recognize the insufficient. To best manage these patients, it is complexity of the contour deformities following crucial that one examines and understands the 2,3 massive amounts of weight loss. Although the deformity to best achieve the goals. The two main breast represents only one aspect of the massive issues following massive weight loss are that the weight loss patient, the deformity is often complex, breast has an unstable envelope, with significant skin blending into the upper abdomen, lateral chest, laxity, and an unstable mound, with loss of volume and arm. The long, deflated, ptotic breast follow- and form. The breast is often very ptotic, laterally ing massive weight loss is still poorly understood, displaced, with a flat upper pole. The chest can be and although we are familiar with intricacies re- wide, with ill-defined landmarks and a loose infra- lated to breast ptosis as the result of age, preg- mammary fold. The patient’s body habitus is also a From the Division of Plastic and Reconstructive Surgery, contributing factor. These are some of the reasons Emory University School of Medicine. why management of the breast following massive Received for publication February 4, 2006; accepted August weight loss is challenging and often requires addi- 1, 2006. tional steps to maintain shape and size expecta- Copyright ©2007 by the American Society of Plastic Surgeons tions and to minimize recurrence of the deformity. DOI: 10.1097/01.prs.0000278004.24650.e6 The purpose of this report is to discuss our tech-

1060 www.PRSJournal.com Volume 120, Number 4 • Massive Weight Loss Breast nique using a familiar procedure with certain mod- extension into the lower end of the new areolar ifications that seem to be beneficial in addressing opening, depending on the length of the pedicle some of the above-mentioned issues in the long or and the amount of rotation necessary. Conservative deflated massive weight loss breast. vertical medial and lateral pillar markings are then drawn in the usual fashion based on the breast me- PATIENTS AND METHODS ridian, stopping 2 to 3 cm above the inframammary All patients at Emory University Hospitals fold. The superomedial pedicle is then incorporated from July of 2003 to January of 2006 with a history as an extension into this V-shaped pattern. of massive weight loss who underwent superome- Operative Technique dial pedicle reduction or mastopexy by a single The extended superomedial pedicle is deepi- surgeon (A.L.) were included in this series. Patient thelialized and the dermoglandular pedicle is demographics included age, body mass index at then incised vertically down toward the chest wall, the time of body contouring, weight loss, risk fac- with no undermining (Fig. 1). Elevation of the tors, nipple to notch measurements, and degree of pedicle off the chest wall is required inferiorly for ptosis. The operative data points included skin rotation into the upper pole; however, central at- takeout pattern (Wise versus vertical), weight of tachments are left intact to maximize pedicle vi- tissue resected, and use of an implant. The out- ability. This allows for safe pedicle back-cut for come data points collected were complications nipple inset when necessary. Once the dermoglan- and the need for revisional surgery. Patients in dular pedicle has been created, the excess skin whom the procedure had been performed more and parenchyma is resected, depending on the than 6 months previously were asked to informally size and shape desired. The breast parenchyma is evaluate their aesthetic result (5 ϭ excellent, 4 ϭ transected from the lateral aspect of the pedicle good, 3 ϭ fair, 2 ϭ mediocre, and 1 ϭ poor) based superiorly to create a pocket for the autoaugmen- on a series of parameters including volume, sym- tation. The pedicle is then rotated superiorly and metry, shape of the breast mound, and symmetry suspended as needed to fill the upper pole (Fig. of the nipple-areola complex. 2). Parenchymal plication is then performed by The technique evolved over the series, and bringing the medial and lateral pillar together certain modifications were applied as the com- with 2-0 polydioxanone suture to reshape and nar- plexity of the deformities became more apparent. row the lower pole of the breast. This can also The current technique involves glandular reshap- redefine and tighten the inframammary fold at a ing and autoaugmentation in a rotation-advance- higher elevation if necessary. Lateral parenchymal ment pattern, described below. plication is performed in a horizontal orientation as needed. Once the breast mound has been shaped, the skin envelope is redraped and any Technique excess skin removed (Fig. 3). Lateral breast skin is Marking advanced medially to redefine the lateral breast The patient is marked preoperatively in the and eliminate the lateral breast roll. standing position. The midaxial line of the breast When implant augmentation is performed at and the existing inframammary fold is marked. the time of mastopexy, the subglandular pocket is The proposed nipple location is determined just created by undermining the superomedial pedi- above the inframammary fold. This typically re- cle. The width of the extended superomedial pedi- sults in a suprasternal notch to nipple distance of cle drawn preoperatively is more conservative to 20 to 23 cm, depending on the height of the minimize the risk of overresection of lower pole patient, level of the inframammary fold, and de- skin. Adjustments in breast mound are performed sired size after the mastopexy (depending on im- before final skin takeout. plant use and autoaugmentation). The inframam- mary fold is often loose and subsequently lower RESULTS than desired, which needs to be taken into con- sideration when determining nipple height. A Demographics mosque-shaped areolar pattern is then drawn, as Thirty-five women (70 breasts) underwent described previously,4,5 with a diameter of approx- mastopexy using the superomedial pedicle and imately 5 cm and a length of the periareolar scar were included in the series. The average weight of less than 16 cm. Markings are then completed loss was 121 pounds (range, 90 to 200 pounds), in the standard Wise and vertical fashion (Fig. 1). which had been stable for at least 6 months. The The superomedial pedicle is then drawn with an average age was 48 years (range, 25 to 70 years),

1061 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 1. The superomedial pedicle is deepithelialized and dissected down to the inframammary fold and chest wall. Wise pattern markings have been used to excise excess skin laterally. Note the lower pole parenchymal defect once the pedicle has been rotated superiorly. with all but three patients having undergone gas- takeout (31 of 35); the remaining 11 percent had tric bypass surgery. Their average body mass index vertical skin takeout. No drains were used post- at time of body contouring was 26.5 (range, 23 to operatively, and no blood transfusion was neces- 39), with additional risk factors being hyperten- sary. When performed without any other body sion (n ϭ 10), diabetes (n ϭ 6), smoking (n ϭ 2), contouring procedures, patients were discharged and history of deep venous thrombosis (n ϭ 1). on the day of surgery. The majority of patients had second- or third- degree ptosis, with an average nipple to notch distance of 31 cm (range, 24 to 40 cm). Outcome The average follow-up was 1.7 years (range, 5 to Procedure 32 months). Breast complications included minor The majority of patients [28 of 35 (80 percent)] wound dehiscence with delayed healing (n ϭ 3), had simultaneous body contouring procedures at hypertrophic scarring (n ϭ 1), wound infection the time of mastopexy-abdominoplasty (n ϭ 22), (n ϭ 1), and capsular contracture (n ϭ 1). There brachioplasty (n ϭ 7), inner thigh lift (n ϭ 3), or were no patients with significant fat necrosis or loss facial rejuvenation (n ϭ 1). Implant augmentation of nipple viability. Patient satisfaction was deter- mastopexy was used in six patients (17 percent), mined using a series of parameters on the 20 most with the average volume being 260 cc (range, 200 recent patients for whom at least 6 months had to 350 cc) per side. All implants were placed in the elapsed after the procedure. This revealed an ac- subglandular location. The average amount of vol- ceptable result (fair ϭ 3 to excellent ϭ 5) 90 percent ume resected was 41 g (range, 0 to 367 g). Eighty- of the time, with the average being 4.1 (range, 2 to nine percent of patients had a Wise pattern skin 5). Two patients rated their result as mediocre.

1062 Volume 120, Number 4 • Massive Weight Loss Breast

Fig. 2. The extended superomedial pedicle has been rotated su- periorlyandsuspendedforautoaugmentation.Thelateralbreast is advanced medially to allow for parenchymal plication and clo- sure of the vertical pillars.

Reoperation Rate The revision rate in the series was 11 percent (four of 35). Two patients required surgical revi- sion for recurrent ptosis within the first 9 months after the procedure. This was accomplished easily by glandular plication, nipple elevation, and skin envelope tightening. Both of these had implants Fig. 3. A 25-year-old woman after a 150-pound weight loss. She placed at the time of the initial mastopexy proce- underwent superomedial pedicle Wise pattern mastopexy with dure and were early in the series where limited autoaugmentation and parenchymal plication. Note intraoper- parenchymal plication had been performed. The ativerotation-advancementandglandularshaping,withevident other two patients required scar revision for hy- upper pole fullness Skin is redraped over the shaped breast pertrophic scarring, nipple shape, and some de- mound. gree of breast asymmetry.

dial pedicle reduction or mastopexy, making the DISCUSSION learning curve minimal. The procedure takes ap- Breast and body contouring following massive proximately 1.5 to 2 hours, depending on the size weight loss is on the rise.3 As we evolve in our of the breast and the extent of the deformity. With management of massive weight loss patients, tech- the growing demand for massive weight loss body niques with which to best manage these patients contouring, new techniques based on old princi- with complex deformities evolve and vary. The ples will undoubtedly become more popular as we superomedial technique has been used in this se- continue to search for better ways to manage this ries that evolved into a rotation-advancement ap- relatively new and growing area in our specialty. proach to reshape the ptotic deflated breast fol- The goals of both reconstructive and aesthetic lowing massive weight loss. This technique was breast surgery are to meet size and shape expec- inspired by necessity and applied to the massive tations, preserve function, achieve symmetry, and weight loss patient based on many of the basic minimize scars. In massive weight loss patients, the concepts and principles as discussed by Lejour and delineation between reconstructive and aesthetic Hall-Findlay.4–6 The preoperative markings and surgery becomes less well defined, and the pa- technique are similar to those for the superome- tients not only seek alleviation of skin symptoms,

1063 Plastic and Reconstructive Surgery • September 15, 2007 but are also interested in more definition to the will theoretically maintain breast shape with up- breast and alleviation of significant ptosis and vol- per pole fullness and minimize recurrence of ume loss with the associated physical and emo- ptosis. The importance of this is especially mag- tional ramifications. This is often a challenging nified in the massive weight loss patient where endeavor, and it becomes crucial that the patient any reliance on the inelastic skin envelope for and surgeon have realistic expectations regarding breast reshaping will invariably contribute to results and potential outcome, especially regard- recurrence of breast ptosis. The skin envelope is ing the potential for recurrent ptosis. very relaxed, with the skin being thin and atro- The types of breast deformities seen following phic. These principles are not new, as Lejour massive weight loss are relatively new, and to best recognized the importance of such glandular manage these patients and assess outcomes, it is suturing.4 Another benefit to this type of glan- important that we understand the defect. Classi- dular plication and parenchymal advancement fication systems exist for breast ptosis; however, is that is helps to narrow the base of an otherwise these are based mainly on nipple position. The wide breast deformity, and redefines a blunted degree of ptosis following massive weight loss has or occasionally lower inframammary fold, and both a glandular component and a true ptosis helps reposition the laterally displaced breast component, stressing the importance of evaluat- mound on the chest wall. Although this tech- ing not only the nipple position but the gland and nique is applicable through the vertical pattern skin envelope as well.7,8 The Pittsburgh Rating in patients with lesser deformities and relatively Scale has recently been developed to measure con- good skin quality, the majority will require a tour deformities following weight loss, with po- Wise pattern skin takeout to address the lateral tential applications in preoperative planning and chest wall deformity and axillary skin rolls evaluating results.9 However, assessing the breast (Fig. 5). deformities and evaluating long-term results re- The issue regarding simultaneous mas- mains a challenge and will always have a certain topexy augmentation has yet to be answered in degree of subjectivity. The maintenance of shape the massive weight loss breast. Although the saf- over time might best be demonstrated by longi- est approach might be a staged mastopexy, glan- tudinal evaluation of results through a combina- dular reshaping followed by implant augmenta- tion of three-dimensional images of the breast10,11 tion if necessary, this is not always desired or and comprehensive yet easy-to-use rating scales. financially feasible for the patient. In patients The superomedial technique has worked for with significant deformities (in terms of breast us and has proven to be a reliable and versatile ptosis and volume loss) who desire additional technique, with the benefits for various aspects implant augmentation, it might be safer to stage of the massive weight loss breast deformity being implant placement until a later procedure. This numerous. The dermoglandular pedicle is often will minimize the incidence of recurrent ptosis short and well vascularized. Nipple viability has or concerns about nipple viability and allow mi- not been an issue, and the superomedial orien- nor adjustments at the second procedure to im- tation allows for safe placement of a subglan- prove shape, symmetry, and final outcome. How- dular or submuscular implant through the tra- ever, when an implant is placed at the time of ditional approach without jeopardizing the mastopexy, it is important to finalize mound blood supply (Fig. 4). The subglandular implant adjustments through glandular shaping and im- location is preferred, as it improves projection plant augmentation before skin takeout and and provides a more natural appearance. When tightening of the skin envelope. The vertical implants are placed in the subglandular loca- pillars in this technique help support the im- tion, this does require undermining the supero- plant, and smaller implants are preferable, as medial pedicle off the chest wall. The ability to the heavier implants might contribute to the risk use the vascularized extension of the superome- of scar widening and recurrent ptosis. The ex- dial pedicle to autoaugment the upper pole pro- tended portion of the pedicle is kept narrow to vides fullness to an area that is often devoid of allow for safe closure, which is reasonable be- volume and otherwise difficult to fill without cause the upper pole fullness relies less on the implants. The rotation of this extended supero- autoaugmentation when an implant is used. A medial pedicle provides a parenchymal defect in certain degree of recurrent ptosis in the massive the inferior pole that is then amenable to pa- weight loss patient is expected; however, this is renchymal plication and lateral breast advance- often magnified when implants are used, lead- ment. This creates an internal support sling that ing to the higher revision rate in that category

1064 Volume 120, Number 4 • Massive Weight Loss Breast

Fig.4. Preoperativeimagesofa36-year-oldwomanaftera185-poundweightloss.(Left)Shehaswide,atrophicbreasts,withinelastic skin, major ptosis, and asymmetry. (Right) Images obtained 18 months after superomedial mastopexy, parenchymal plication, and a300-ccsubglandularimplantaugmentation.Shapeandsizehavebeenpreservedwithtimeandthebreasthasbeennarrowed,with improved definition. in our series. The combined approach is now described a technique using a lower thoracic used with caution in the massive weight loss parenchyma flap tunneled underneath the patient, and it is crucial that the patient under- prepectoral fascia providing a fascial suspension stands the potential risks preoperatively. component to their mastopexy.12 Other tech- Attempts are continually being made to im- niques have been described to maintain shape prove long-term shape following mastopexy and following mastopexy using different suspension reduction mammaplasties. Ritz et al. recently type sutures, parenchymal flaps, and muscle

1065 Plastic and Reconstructive Surgery • September 15, 2007

Fig. 5. Preoperative images (left) of a 51-year-old woman after a 90-pound weight loss. She has long, deflated breasts with stretch marks and thin, inelastic skin. (Right) Seven-month postoperative views after bilateral mastopexy using the Wise pattern rotation- advancement technique. slings.13–17 Although these concepts are not tive attempts to minimize ptosis, we realize that in unique to the massive weight loss patient, their this patient population, a certain degree of recur- importance is magnified, given the underlying rent ptosis is almost inevitable. Although ptosis anatomy and physiology. was evident in some patients postoperatively, most In this series, our technique evolved into more were still satisfied with their aesthetic result and aggressive glandular plication and autoaugmen- report significant improvement. The goal is to tation. Complication rates, revision rate, and pa- minimize recurrent ptosis to the point where both tient satisfaction were used as measures of success patient and surgeon satisfaction is sufficient to following superomedial pedicle mastopexy for the eliminate the need for revisional surgery; however, massive weight loss patient. We recognize that we realize that some changes over time are not other factors are important when it comes to eval- uncommon (Figs. 6 and 7). uating outcomes, including objective and subjec- Over the next few years, there will undoubt- tive breast measurements, and these will be ad- edly be numerous techniques in the literature de- dressed in future studies as our experience scribing ingenious ways to reshape the massive broadens with longer follow-up. One of the main weight loss breast, using some degree of glandular goals with this approach is to minimize breast pto- shaping, parenchymal suspension, and autoaug- sis and maintain shape over time. Although our mentation. This series merely represents another series is small and with intermediate follow-up, we alternative technique that we feel is reliable and have noticed that the need for revisional surgery reproducible and that works for us in the majority secondary to recurrent ptosis has been reduced of cases. It addresses and corrects many of the through careful attention to shaping of the breast intrinsic problems inherent to patients following mound with parenchymal plication, glandular sus- massive weight loss, in an attempt to provide lasting pension, and autoaugmentation. Despite proac- shape and improve patient satisfaction. Longer fol-

1066 Volume 120, Number 4 • Massive Weight Loss Breast

Fig. 6. Longitudinal evaluation of results. (Above) Preoperative images of a 39-year-old woman after a 148-pound weight loss. (Below) Postoperative views 4 weeks after superomedial pedicle Wise pattern mastopexy with autoaugmentation and parenchymal placation.

Fig.7. Longitudinalevaluationofresultsat1yearpostoperatively,withsomevolumelossbutmaintenanceofshapeandnipple position over time. low-up in a larger series will be helpful. We do rec- ment is similarly involved. As the incidence of bari- ognize that it is not without limitations and will not atric surgery continues, the number of women seek- necessarily be the technique of choice for all breasts. ing aesthetic and reconstructive breast surgery and These deformities are complex and their manage- body contouring will continue to rise.

1067 Plastic and Reconstructive Surgery • September 15, 2007

CONCLUSIONS 4. Lejour, M. Vertical mammaplasty and liposuction of the breast. Plast. Reconstr. Surg. 94: 100, 1994. The rotation-advancement technique using 5. Hall-Findlay, E. J. A simplified vertical reduction mamma- the superomedial technique with certain modifi- plasty: Shortening the learning curve. Plast. Reconstr. Surg. cations is safe, reliable, and reproducible. It is 104: 748, 1999. relatively easy to apply to most patients with breast 6. Lassus, C. A 30-year experience with the vertical mamma- ptosis and the majority of massive weight loss plasty. Plast. Reconstr. Surg. 97: 373, 1996. 7. Brink, R. Management of true ptosis of the breast. Plast. breast deformities. Ways to minimize the inci- Reconstr. Surg. 91: 657, 1993. dence of recurrent ptosis in massive weight loss 8. Regnault, P. Breast ptosis: Definition and treatment. Clin. patients include glandular shaping though plica- Plast. Surg. 3: 193, 1976. tion and suspension techniques, autoaugmenta- 9. Song, A. Y., Jean, R. D., Hurwitz, D. J., Fernstrom, M. H., tion, and staging implant augmentation. The goal Scott, J. A., and Rubin, P. J. A classification of contour de- formities after bariatric weight loss: The Pittsburgh Rating is to maintain shape and symmetry over time and Scale. Plast. Reconstr. Surg. 116: 1535, 2005. to minimize the need for revisional surgery. 10. Galdino, G. M., Nahabedian, M., Chiaramonte, M., Geng, J. Z., Klatsky, S., and Manson, P. Clinical applications of Albert Losken, M.D. three-dimensional photography in breast surgery. Plast. Re- Division of Plastic Surgery constr. Surg. 110: 58, 2000. Emory University School of Medicine 11. Losken, A., Seify, H., Denson, D. D., Paredes, A. A., and 550 Peachtree Street, Suite 84300 Carlson, G. W. Validating three-dimensional imaging of the Atlanta, Ga. 30308 breast. Ann. Plast. Surg. 54: 471, 2005. [email protected] 12. Ritz, M., Silfen, R., and Southwick, G. Fascial suspension mastopexy. Plast. Reconstr. Surg. 117: 86, 2006. 13. Ribeiro, L. A new technique for reduction mammaplasty. DISCLOSURE Plast. Reconstr. Surg. 55: 330, 1975. Neither of the authors has a financial interest in any 14. Graf, R., and Biggs, T. M. In search of better shape in mas- of the products, devices, or drugs mentioned in this article. topexy and reduction mammaplasty. Plast. Reconstr. Surg. 110: 309, 2002. 15. Caldeira, A. M., and Lucas, A. Pectoralis major muscle flap: REFERENCES A new support approach to mammaplasty, personal tech- 1. Livingston, E. H. Obesity and its surgical management. nique. Aesthetic Plast. Surg. 24: 58, 2000. Am. J. Surg. 184: 1, 2002. 16. Lockwood, T. Reduction mammaplasty and mastopexy with 2. O’Connell, J. B. Bariplastic surgery. Plast. Reconstr. Surg. 113: superficial fascial support system suspension. Plast. Reconstr. 1530, 2004. Surg. 103: 1411, 1999. 3. Gastric bypass surgery popularity leads to jump in plastic 17. Eaves, F. F. Mastopexy after massive weight loss. Presented at surgery procedures. Press Release: American Society of Plastic the 21st Annual Breast Surgery Symposium, Atlanta, Ga., Surgeons, March 10, 2003. January 20–23, 2005.

1068 CME

Lip Reconstruction

Bardia A. Anvar, M.D. Learning Objectives: After studying this article, the participant should be able Brandon C. D. Evans to: 1. Understand perioral anatomy and function. 2. Analyze lip defects. 3. Gregory R. D. Evans, M.D. Understand the paradigm behind lip reconstruction. 4. Become familiar with Orange, Calif. the wide variety of techniques available for reconstruction and their appropriate application. Summary: Lip reconstruction remains challenging. Accurate analysis of the defect and a thorough understanding of the anatomy and options for re- construction will maintain the functional and aesthetic quality of this sen- sitive area. (Plast. Reconstr. Surg. 120: 57e, 2007.)

erioral defects may result from trauma, ma- labial melanotic macules, and infectious pro- lignancy, and congenital defects. These de- cesses such as noma.1 The nature of the disease Pfects may cause loss of function, as the becomes important when deciding appropriate upper and lower lips are essential in the protec- margins of resection and resultant defect size. tion and maintenance of oral competence. The lips not only allow for function in feeding and hygiene but are important for the maintenance ANATOMY of the social smile. Management of lip defects A thorough understanding of anatomy is nec- remains a significant reconstructive challenge essary to allow correction to its normal form. The requiring extensive preoperative planning for musculature defines the function of the lip, and the restoration of function and cosmesis. For the incomplete approximation may lead to dimpling more simple oral defects, local tissue advance- and scarring. The upper and lower lips are formed ment and flaps are best; however, more ad- by a three-layer structure of skin, muscle, and mu- vanced defects may require free tissue transfer. cosa. The outer border is formed by the vermilion, Initial management requires identification of which has a modified mucosa and does not con- the extent of injury before the application of tain glandular tissue. The vermilion is the muco- such closure techniques. cutaneous junction between the inner mucosa Cancer resection causes the majority of lip and outer skin. Its repair is critical, as minute defects; however, trauma and burns are also con- defects are easily noticeable.2 The vermilion is re- tributors. Squamous cell carcinoma is the most ferred to as the red lip because of its thin epithelial common malignancy affecting the lip, unlike the architecture and underlying blood vessels.3 The rest of the face, where basal cell cancer is pre- outer anatomy of the lip consists of Cupid’s bow, dominant. Smoking and sun exposure are the a philtrum, a central tubercle, and a fullness in the two greatest environmental factors contributing lower lip. The underlying musculature is defined to lip cancer. Thus, because the lower lip re- by the orbicularis oris plus more than a dozen ceives more ultraviolet exposure than the upper paired muscles whose actions are elevation, de- lip it, is the site of more than 90 percent of cancers. Less common malignancies involving pression, and function for sphincteric movement. the lip are microcystic adnexal carcinoma and Many of these perioral muscles originate or insert Merkel cell carcinoma, whereas other disease at the modiolus, a fibrous structure that attaches processes that affect the lip are granulomatous to the deep layers of skin at the level of the com- cheilitis, vascular lesions (hemangiomas), nevi, missures. The deep fibers of the orbicularis are oriented horizontally, and defects in the lip may From the Aesthetic and Plastic Surgery Institute, University appear exaggerated because the resting tone of of California, Irvine. the orbicularis pulls wound edges apart. The de- Received for publication January 25, 2006; accepted April pressor muscles of the lips are the anguli oris, the 14, 2006. labii inferioris, and the platysma. The levator labii Copyright ©2007 by the American Society of Plastic Surgeons superioris, zygomaticus, risorius, and mentalis DOI: 10.1097/01.prs.0000278056.41753.ce muscles elevate the lip. Together these muscles

www.PRSJournal.com 57e Plastic and Reconstructive Surgery • September 15, 2007 provide the competency of a circular complex, which provides form and function.1 The lips contain a number of nerves for both motor and sensory function, whose preservation and reconstruction are necessary. The sensory supply to the upper lip is from the infraorbital branch of the trigeminal nerve, whereas the men- tal branch of the trigeminal nerve supplies sensory innervation to the lower lip. The buccal and man- dibular branches of the facial nerve supply motor innervation to the musculature of the lips. With the exception of the marginal mandibular nerve, which courses superficially to innervate the men- talis muscle, these nerves enter deep to muscle. Cognizance of these nerves is important to con- struct innervated myocutaneous flaps. A critical element to the advancement of local flaps in lip repair is adequate vascularization. Blood supply is through the facial artery, which branches to form the superior and inferior labial arteries. These labial arteries course superficial to the orbicularis oris muscle and deep to the mu- cosal surface of the lip. Venous drainage is usually concomitant with arterial flow; however, the up- per lip may drain by means of the ophthalmic vein, a route for intracranial infection.

LIP RECONSTRUCTION TECHNIQUES General Considerations To maintain the natural aesthetic appearance of the lip, consideration must be given to topo- graphic boundaries and aesthetic subunits. The aesthetic subunit boundaries—the melolabial fold, mental crease, and philtral ridges—must be preserved and used to help camouflage scars. Therefore, these units must be marked before injecting local anesthesia. When a substantial por- tion of these aesthetic subunits is compromised, replacement of the entire subunit may be a better alternative. Vertical scars are favorable because of the radial direction of the lines of tension and be- cause they prevent downward scarring of the lip.1

Primary Repair Fig. 1. Resection and primary closure in a 64-year-old patient Small full-thickness defects, between a quarter with basal/squamous cell carcinoma to the lower lip. and a third of the lip, may be closed primarily. These defects are usually 2 cm or smaller (Fig. 1). Local tissue should be used whenever possible to symmetry in primary closure. Excision of tissue is provide minimal donor-site morbidity and the best usually in the shape of a V; however, a pentagonal overall color and texture match.2 Vermilion and or W technique for resection can be performed.5 skin must be excised to allow tension-free closure.4 Vermilion-only defects can be corrected with The junction between the vermilion and sur- advancement of the labial mucosa, which is rounding skin is outlined by a linear prominence, then redraped over the underlying orbicularis the white roll. The excision of the white lip allows musculature.2 In this type of repair, the dissection

58e Volume 120, Number 4 • Lip Reconstruction plane is between the muscle and the mucosa. In- ment rotation flaps such as the Karapandzic traoral releasing incisions or a V-Y advancement of and/or Gillies. Each flap has its advantages, de- the mucosa may be used to relieve tension on the pending on the site of the defect. Mucosal and closure. Yano et al. describe the correction of shal- tongue flaps are also well described. low defects of the lower lip with a V-Y advancement The Abbe´ Flap flap followed by a tongue flap to replace the mu- The Abbe´ flap, first described by Sabatani and cosal surface and vermilion.6 This flap is designed then further by Abbe´, is designed to primarily in the form of a triangle with an inferior apex, correct midline defects of the upper lip.3 This flap situated at the edge of the mandible. A 1- or 2-cm is described as a rotational or lip-switch flap whose lateral subcutaneous dissection is described to al- primary blood supply is from the coronal branch low for adequate upward advancement. The flap of the labial artery. There is no large venous struc- is advanced as a musculocutaneous flap, thus al- ture associated with the flap; therefore, venous lowing preservation of the oral sphincter. A two- return must be guaranteed with adequate recruit- layer closure of skin and subcutaneous tissue is ment of adjacent tissue. The flap is designed to be performed joining the flap to the vermilion. Po- the same height as the defect and approximately tential complications of labial-buccal advance- one-half the width. The flap is created through a ment include thinning of the lip as a result of scar full-thickness incision, with preservation of the la- contracture, excessive lip fullness from overad- bial artery. The flap is rotated 180 degrees into the vancement of the flap, and color mismatch. Boc- defect, with careful maintenance of blood supply chi et al. report their experience with 16 patients from the pedicle. A multilayer closure is per- with double V-Y advancement flaps, and in no formed, with attention to the muscular layer and instance was there vascular compromise or other creation of the vermilion border. As a result of the complications such as microstomia, retracted closed oral aperture, the patient is placed on a soft scars, or hypomobility.8 or liquid diet for the period of vascular ingrowth. This cross-lip flap is then divided 2 to 3 weeks later Local Flap Techniques and inset, when surrounding vascular inflow is Defects that are between one-third and two- established (Fig. 2). thirds the total lip length represent the most com- Estlander Flap plex decision-making challenge. Two major tech- Similar to the Abbe´ flap, the Estlander flap is niques are available to reconstruct these defects: a cross-lip flap, which has its point of rotation at (1) transoral cross-lip flaps such as the Abbe´ the commissure. In contrast to the Abbe´ flap, the and/or Estlander; and (2) circumoral advance- Estlander is designed for a one-stage reconstruc-

Fig. 2. Preoperative and postoperative views of a 65-year-old man with resection of a squa- mous cell carcinoma to the upper lip. The defect was reconstructed with an Abbe´ flap.

59e Plastic and Reconstructive Surgery • September 15, 2007

Fig. 4. Diagram of the Karapandzic technique. Fig. 3. The Estlander flap was used for left commissure recon- struction, and the right Karapandzic was used to reconstruct the therefore there is less microstomia. Because the lower lip. orbicularis is not fully dissected and advanced, but rather is pulled with the pedicle, full function and sensation may not return. Oral incompetence may tion. Similar in design to the Abbe´ flap, it is equiv- also result. Modifications of this technique in- alent in height to the defect and half the width. It clude the use of a Z-plasty to allow better turning is usually designed as a triangle at the commissure. of the pedicle around the commissure. This results in a proportionate size reduction in Karapandzic Technique both lips. The flap can be designed to lie within The Karapandzic technique is a one-stage re- the melolabial crease, to reduce the size of the construction designed for central lower lip defects donor site; however, revision of the commissure (Fig. 4). The method is an advancement-rotation may be necessary.7 Meticulous suturing of the mus- flap that maintains both lip mobility and sensa- cles to reconstitute the orbicularis ring and accu- tion, reuniting the lower lip by means of radially rate approximation of the vermilion-cutaneous oriented incisions across the outer perioral area. border are essential for obtaining excellent re- Partial-thickness incisions are made that preserve sults. Both the Estlander and Abbe´ flaps are de- the neurovascular bundle. Muscle fibers are mo- nervated. Return of sensory function is usually in bilized by blunt dissection, and neurovascular the following order: pain, touch, and tempera- structures are identified and preserved. Critical to ture. Hypersensitivity of the flap may also occur the success of the procedure is the planning of the but usually resolves after the first year (Fig. 3). incisions. Some surgeons recommend placing in- Gillies Fan Flap cisions starting at the nasolabial folds,9 but it is also The Gillies fan flap is a modification of the acceptable to create semicircular incisions from cross-lip technique that advances the remaining the defect. The mucosa is cut only if needed to lip segment with a portion of the opposing ipsi- correct intraoral defects. The width of the lip seg- lateral lip. In lower lip defects, a fan-shaped flap ments to be transferred is equal to the vertical is created through a full-thickness incision from height of the lip defect. It is important to maintain the inferior aspect of the defect, which extends a consistent flap thickness. A side effect to the laterally around the commissure and superiorly repair is of course the reduction in the size of the into the melolabial fold.1 The secondary incision oral aperture. The final result; however, is an in- is taken toward the superior vermilion, without tact oral opening with good function, sensation, compromise to the superior labial artery. On com- and mobility (Fig. 3). pletion of these incisions, the flap is then rotated Nasolabial Flap and advanced into the defect. The advantage to Based on perforating branches of the terminal this technique is that it uses greater tissue, and angular artery, the nasolabial flap provides smaller

60e Volume 120, Number 4 • Lip Reconstruction tissue volume replacement. Its use is primarily bulk of the tongue also recreates the natural pout for partial defects of the lateral upper or lower of the lower lip.10 lip. The secondary defect is closed with adjacent cheek tissue. These flaps are designed on a qua- Total Lip Reconstruction si-axial blood supply and may need to be sup- Patients with total lip defects present great plied by the facial artery if the size is appropri- reconstructive challenges, often healing to signif- ate. When performing this operation, the flap is icant dysfunction and disability. Large defects usu- elevated in a plane above the orbicularis muscle ally involve the lower lip, given its greater prepon- and is inset into the defect. Design of this flap derance of carcinoma. If three-fourths of the adjacent to the defect will facilitate a better out- remaining lip is intact, the possibility of repairing come. However, pin cushioning and oblitera- with residual lip tissue may apply. When en- tion of the nasolabial crease are noticeable 3,5 countering these cases, one may use local flap disadvantages. reconstruction by means of the Bernard–von Tongue Flap Burrow–Webster technique. However, if there is In contrast, although no longer frequently a lack of residual lip tissue, one must use more used, a tongue flap may reconstruct significant complex techniques such as microvascular free tissue loss. The ventral surface of the tongue is tissue transfer. preferable for use because it matches the vermil- The Bernard–von Burrow–Webster ion more closely in color and texture than the Technique dorsum. An appropriate amount of tongue equal The Bernard technique uses cheek tissue to to the size of the defect is taken, which is then replace defects. In this procedure one must excise approximated to the anterior lip defect. The flap the Burrow’s triangle at the superior and inferior is unrolled and then sutured. The flap is main- margins of the flap to facilitate advancement (Fig. tained for a period of 14 days, after which time it 5, left). A horizontal full-thickness or partial-thick- is divided and inset. The residual tongue defect is ness incision is usually extended laterally from the then sutured closed. During the 14-day period, the commissure. A triangular standing cutaneous de- patient must take care not to bite through the pedi- formity is then created; this allows adequate mo- cle. This can be ensured by cementing the molars bility of the lower lateral lip elements without apart.1 The patient may regain functional use of cheek distortion. The inferior segment of the flap the tongue if an aggressive rehabilitation program is advanced medially for reconstruction. The miss- is undertaken. The disadvantages of a tongue flap ing vermilion may be created with either a buccal are as follows: (1) multistage procedures are re- mucosal flap or a tongue flap. When performed quired and (2) the tissue replacement does not bilaterally, a total defect may be reconstructed. In parallel the mucosa exactly. Nevertheless, tongue this technique, upper lip reconstruction is accom- flaps have favorable results because of their ex- plished by means of four triangles of cheek skin, cellent blood supply, mobility, and proximity. The and lower lip reconstruction with the excision of

Fig. 5. The modified Bernard–von Burrow–Webster technique.

61e Plastic and Reconstructive Surgery • September 15, 2007 three triangles. Although originally designed as a tion of the recipient vessels will determine ade- full-thickness reconstruction, cutaneous excision quate flap viability. An accurate template must be only may be performed. This is an excellent flap made under physiologic tension because after re- with limited remaining lip because it does not section the cut ends of the cheek and lip retract. depend on residual lip tissue for reconstruction. Some authors recommend Esmarch bandages as This technique is not limited to correction of large template material.4 The skin paddle of the flap is defects, and excellent results may be obtained in fashioned according to the size of the defect and defects that are one-third to two-thirds of total lip. oral mucosa plus external face. In consideration to Because this is an adynamic reconstruction, pa- suspension of the flap, the palmaris longus may be tients will have postoperative drooling (Fig. 5, cen- used. The tendon is anchored to the modiolus, the ter and right). orbicularis, or both. It is imperative to adjust the Combined Flaps tension of the tendon to allow appropriate oral A multistage repair with a combination of flaps competence. The palmaris tendon may also be to repair the lower lip may also be used. Initial fashioned to the nasolabial area or the malar peri- reconstruction with extended Karapandzic flaps osteum. Attaching the tendon to muscle allows a allows for restoration of the sphincter. Although more dynamic functioning lip. In total or near the appearance will be compromised, function total full-thickness defects of the lip, this flap is an will be maintained even if the flaps are extended excellent option. In a recent clinical series, 12 from the nasal alae. Further modifications with patients underwent this type of reconstruction, cross-lip flaps to restore symmetry and balance with 100 percent flap survival.13 All patients had between the upper and lower lips may then follow. excellent static suspension; however, one patient By using two Abbe´ flaps, one may create greater did not have oral competence during speaking fullness in the upper lip. This type of technique and eating. Potential complications of total lip was successful in patients with large arteriovenous reconstruction include hypertrophic scarring, dis- malformations extending from the lower lip to the figurement, loss of sensation, potential microsto- chin that required resection.11 A modification of mia, loss of oral competence, and loss of the nat- these techniques with bilobed and Karapandzic ural gingivobuccal sulcus, making denture use flaps has been described to correct defects greater difficult.3,14 This flap may also be combined with than 80 percent of the lower lip8 (Fig. 3). temporalis muscle for reconstruction of defects of Once again, one can use aesthetic boundaries the lower lip, which include the oral commissure15 such as the philtral columns and the peaks of the (Fig. 6). Cupid’s bow to camouflage scars and enhance Alternative Free Flaps overall appearance. Subsequently, oral commis- Other microvascular approaches include the suroplasty may be performed to increase the oral gracilis free flap. Total lower lip reconstruction aperture. One method of commissuroplasty is to can be performed with such a technique as de- resect a triangle of skin with its apex located at the scribed by Lengele et al.16 The gracilis muscle may site of the new commissure. The remaining supe- be prefabricated by performing vascular augmen- rior and inferior lip elements are then reapproxi- tation. A long strip of fascia lata may be used as a mated. Alternatively, the existing commissure may supportive tendon. A neomucosal lining may also be split into two flaps containing both vermilion be obtained by placing silicone along the previ- 7 and muscle. However, this method creates a thin- ously exposed deep part of the gracilis. A second- ner lip at the edges. Thus, by using a number of stage operation is then performed where the me- techniques in series, even large defects may be dial circumflex vessels are anastomosed to the closed with remaining lip tissue, and commissuro- facial vessels and the nerve to the gracilis is at- plasty is a useful tool for increasing the size of the tached to the marginal facial branch. The tendon final oral aperture. is attached to the zygomaticus muscle.17 Radial Artery Forearm Flap Upper lip defects, although rare, may be re- Finally, with no remaining lip, microvascular constructed with a temporal scalp free flap. This reconstruction may be necessary. The most com- gives both an outer hair-bearing area and an inner monly used free flap is the radial forearm, which mucosal area.18 is usually transferred along with the palmaris lon- gus tendon for lip support.12 This flap can be transferred as a sensate flap by a neurorrhaphy of Postoperative Care and Complications the lateral antebrachial cutaneous nerve to the A number of factors come into consideration mental or inferior alveolar nerve. Initial evalua- in lip repair. Oral function, competence, and form

62e Volume 120, Number 4 • Lip Reconstruction

The complications of lip repair relate mostly to aesthetics and functional loss. Microstomia re- sults from inadequate tissue recruitment and makes it hard for patients to eat, wear dentures, and have a normal appearance. Once again, com- missuroplasty can be performed to correct prob- lems such as microstomia or rounding of the com- missure. Indeed, techniques that circularize the exist- ing sphincter, such as Karapandzic flaps, produce the most function. Radial forearm free flaps, in contrast, do not appear to move substantially and only serve as a platform against which the upper lip can close.4 Additional potential complications of total lip reconstruction include loss of the nat- ural gingivobuccal sulcus. One may avoid these potential pitfalls by careful preoperative planning and meticulous surgical technique.

CONCLUSIONS Lip reconstruction is challenging. With appro- priate techniques and the use of surrounding tis- sues, restoration of appropriate form and function can be achieved. Gregory R. D. Evans, M.D. Aesthetic and Plastic Surgery Institute University of California, Irvine 200 South Manchester, Suite 650 Orange, Calif. 92782 Fig. 6. An example of elevation of a radial forearm flap used for [email protected] reconstruction. DISCLOSURE are primary; however, innervation, sensation, and None of the authors has a financial interest in any of final cosmesis complete the end result. When per- the products, devices, or drugs mentioned in this article. forming minor repair, tissue alignment is critical. REFERENCES With larger defects, the choice of repair becomes 1. McCarn, K. E., and Park, S. S. Lip reconstruction. Facial Plast. more imperative. With cross-lip flaps, careful at- Surg. Clin. North Am. 13: 301, 2005. tention is reserved for arterial supply and flap 2. Coppit, G. L., Lin, D. T., and Burkey, B. B. Current concepts viability. Free flaps allow a one-stage correction for in lip reconstruction. Curr. Opin. Otolaryngol. Head Neck Surg. large defects; however, morbidity is a consider- 12: 281, 2004. ation in these cases. Other strategies such as re- 3. Krunic, A. L., Weitzul, S., and Taylor, R. S. Advanced recon- structive techniques for the lip and perioral area. Dermatol. construction with tongue flaps are less favorable Clin. 23: 43, 2005. but are options. In instances where there is a lack 4. Langstein, H. N., and Robb, G. L. Lip and perioral recon- of adequate mucosa, one may use mucosal mesh- struction. Clin. Plast. Surg. 32: 431, 2005. ing techniques similar to that performed on skin 5. Dupin, C., Metzinger, S., and Rizzuto, R. Lip reconstruction grafts.19 after ablation for skin malignancies. Clin. Plast. Surg. 31: 69, 2004. After surgery, it is important to monitor func- 6. Yano, K., Hosokawa, K., and Kubo, T. Combined tongue flap tion, mobility, and cosmesis. Results may be doc- and V-Y advancement flap for lower lip defects. Br. J. Plast. umented by photographs of a patient with an open Surg. 58: 258, 2005. and closed mouth, at rest, and in function. Some 7. Kroll, S. (Ed.). Lip reconstruction. In Reconstructive Plastic authors further advocate the use of dynamic im- Surgery for Cancer. St. Louis, Mo.: Mosby Year Book, 1996. Pp. 201–209. aging to monitor the functional outcome of the 8. Bocchi, A., Baccarani, A., Bianco, G., Castagnetti, F., and repair. Follow-up surgery is often necessary, and Papadia, F. Double V-Y advancement flap in the management speech must also be monitored. of lower lip reconstruction. Ann. Plast. Surg. 51: 205, 2003.

63e Plastic and Reconstructive Surgery • September 15, 2007

9. Ong, W. C., Lim, J., and Lim, T. C. A modification of the 15. Jeng, S. F., Kuo, Y. R., Wei, F. C., Su, C. Y., and Chien, C. Y. bilobed and Karapandzic flap used for reconstruction of the Reconstruction of concomitant lip and cheek through-and- lower lip. Plast. Reconstr. Surg. 115: 2154, 2005. through defects with combined free flap and an advance- 10. Hitoshi, O., Koichi, M., Yoshiyuki, T., Hiroto, I., Hideaki, S., and ment flap from the remaining lip. Plast. Reconstr. Surg. 113: Mikio, K. A case of lower lip defect reconstructed with buccal 491, 2004. mucosa and a tongue flap. J. Craniofac. Surg. 15: 614, 2004. 16. Lengele, B. G., Testelin, S., Bayet, B., and Devauchelle, B. 11. Kiyokawa, K., Takagi, M., Fukushima, J., Kizuka, Y., Inoue, Y., Total lower lip functional reconstruction with a prefabri- and Tai, Y. Surgical treatment following huge arteriovenous cated gracilis muscle free flap. Int. J. Oral Maxillofac. Surg. 33: malformation extending from the lower lip to the chin: 396, 2004. Combination of embolization, total resection, and a double 17. Jeng, S. F., Kuo, Y. R., Wei, F. C., Su, C. Y., and Chien, C. cross lip flap. J. Craniofac. Surg. 16: 443, 2005. Y. Reconstruction of extensive composite mandibular de- 12. Sadove, R. C., Luce, E. A., and McGrath, P. C. Reconstruction fects with large lip involvement by using double free flaps of the lower lip and chin with the composite radial forearm- and fascia lata grafts for oral sphincters. Plast. Reconstr. palmaris longus free flap. Plast. Reconstr. Surg. 88: 209, 1991. 13. Jeng, S. F., Kuo, Y. R., Wei, F. C., Su, C. Y., and Chien, C. Y. Surg. 115: 1830, 2005. Total lower lip reconstruction with a composite radial fore- 18. Chang, K. P., Lai, C. S., Tsai, C. C., Lin, T. M., and Lin, S. D. arm-palmaris longus tendon flap: A clinical series. Plast. Re- Total upper lip reconstruction with a free temporal scalp constr. Surg. 113: 19, 2004. flap: Long-term follow-up. Head Neck 25: 602, 2003. 14. Eguchi, T., Nakatsuka, T., Mori, Y., and Takato, T. Total re- 19. Ay, A., Aytekin, A., and Aytekin, O. Mucosal meshing tech- construction of the upper lip after resection of a malignant nique in lip reconstruction with unilateral gate flap. Plast. melanoma. Scand. J. Plast. Reconstr. Surg. Hand Surg. 39: 45, 2005. Reconstr. Surg. 114: 147, 2004.

64e SAFETY & EFFICACY REPORT

Mexoryl: A Review of an Ultraviolet A Filter

Gehaan D’Souza, B.S. Summary: It is widely known that ultraviolet light causes skin damage and Gregory R. D. Evans, M.D. melanoma. Different wavelengths of ultraviolet light penetrate the skin at dif- Plastic Surgery Educational ferent depths, causing varying levels of damage. Higher wavelengths tend to Foundation Technology penetrate deeper and, consequently, are thought to induce a myriad of skin Assessment Committee conditions, thereby playing a significant role in the photoaging process. Sun- Orange, Calif. screens containing the ultraviolet A blocker Mexoryl are important in impeding ultraviolet A light, potentially reducing many of the characteristics of skin aging and preventing biochemical changes that can lead to nonmelanoma carcinoma. Until now, sunscreen products sold in the United States focused on blocking ultraviolet B light. Those that did provide ultraviolet A filtering contained physical blocks (zinc oxide or titanium dioxide) or the chemical block Parsol 1789 (avobenzone). These broad-spectrum sunscreens have limitations, such as degradation under ultraviolet exposure, that resulted in decreased effectiveness. Mexoryl, a novel ultraviolet A filter, provides efficient ultraviolet A coverage, better photostability, and enhanced water resistance. Sunscreens containing Mexoryl are widely used in Europe and Canada. It was not until July 24, 2006, that the U.S. Food and Drug Association approved the compound. (Plast. Reconstr. Surg. 120: 1071, 2007.)

ncreased exposure to ultraviolet radiation has dients that both block and absorb ultraviolet been correlated with an increase in skin can- light. Icer cases over the past two decades.1–4 The One might apply sunscreen both to protect incidence of all skin cancers has been rising 4 to against varying degrees of skin cancer and to 5 percent each year, with more than 1.3 million protect against photoaging. Most people, how- new cases diagnosed annually. With a growth ever, do not realize that their sunscreen might rate faster than any other cancer, the incidence not be blocking all types of ultraviolet light effi- of melanoma has nearly tripled in the last four ciently. Ultraviolet light is a form of radiation decades. It is estimated that more than 1 million that is not visible to the human eye. Ultraviolet cases of nonmelanoma skin cancer were diag- wavelengths are subdivided into three catego- nosed in the United States in 2006 alone.5 ries: ultraviolet A light (320 to 400 nm), ultravi- To protect themselves from ultraviolet light, olet B light (280 to 320 nm), and ultraviolet C individuals avoid excessive sun exposure, wear light (Ͻ280 nm). The deeper-penetrating ultra- protective clothing, and use a variety of environ- violet A component of the solar spectrum pre- mental precautions, such as diffusion shields or sents a higher degree of risk of photoaging. The blocking films.4 They also apply sunscreen when ultraviolet B component presents the increased sun exposure is anticipated. degree of risk of developing a cutaneous It is important to note that the method of neoplasm.2 action between these ultraviolet-ameliorating de- In studies using solar-simulated radiation,6 vices differs. Ultraviolet rays can be both re- sunscreens containing both ultraviolet B and A flected and absorbed by a surface. A diffusion filters provided better protection than sun- shield, blocking film, or simple small-brimmed screens that contained only ultraviolet B filters. hat physically blocks ultraviolet radiation.2 On Protection increases proportionally with the the other hand, most sunscreens contain ingre- presence of ultraviolet A filters and the sun- screen’s ability to absorb ultraviolet A light. From the Aesthetic and Plastic Surgery Institute, The Uni- Sunscreens have different formulations versity of California, Irvine. around the world. Sun protection agents should Received for publication March 12, 2007; accepted May 11, be cosmetically pleasant, nontoxic, equally effec- 2007. tive against ultraviolet A and B, photostable, and Copyright ©2007 by the American Society of Plastic Surgeons water resistant, as well as have a high sun protec- DOI: 10.1097/01.prs.0000280561.02915.3a tion factor. These products normally contain

www.PRSJournal.com 1071 Plastic and Reconstructive Surgery • September 15, 2007 physical blockers, such as zinc oxide or titanium rays and, therefore, at protecting the skin from dioxide. The ultraviolet A chemical blocking sunburn. For example, if you normally begin to agent Parsol 1789 (avobenzone) is also available.2 tan or burn after 20 minutes in the sun, an SPF Each sunscreen ingredient has advantages and of 15 will extend your ultraviolet B protection 15 limitations. Titanium dioxide offers excellent ul- times longer, or to 300 minutes. Theoretically, if traviolet A-II protection but decreased ultravio- applied properly, SPF 30 protects the skin twice let A-I filtering.2 In addition, Parsol 1789 and as long as SPF 15; however, it is important to zinc oxide provide adequate ultraviolet A-I pro- note that the amount of protection provided by tection but lack ultraviolet A-II blocking action. the SPF is actually determined by the percentage Parsol 1789 also tends to lose effectiveness after of harmful rays it is able to filter. SPF 15 is able 1 hour under the sun.7 The opacity of titanium to filter 93 percent of ultraviolet B rays, whereas dioxide and zinc oxide tends to yield a less than SPF 30 can filter up to 97 percent of ultraviolet B satisfying cosmetic result when these products rays.9,10 2 are spread on the skin. Specific commercial While there are multiple methods to measure sunscreens with each ingredient are listed in ultraviolet A protection, in 2001, the American Table 1. Academy of Dermatology, at the consensus con- Before U.S. Food and Drug Association ap- ference on ultraviolet A protection, recom- proval of the sunscreen/moisturizer La Roche- mended the use of the Protection Factor Ultra- Posay Anthelios, with ultraviolet A filter Mexoryl, violet A, or PFA, grading system. This system most sunscreens sold in the United States fo- measures the ultraviolet A protection level by the cused on blocking ultraviolet B rays; as a result, persistent pigment darkening method. This they are largely deficient in blocking ultraviolet grading system is analogous to the SPF grading A light. European and Canadian sunscreens system in that it is a guide demonstrating the have contained the ultraviolet A blocker Mexoryl ability of a sunscreen to protect against a certain for the last two decades. wavelength of ultraviolet radiation. Since PFA is Studies from Lavker et al.8 note that many a similar ratio correlating to the SPF scale, ex- sunscreens advertise a high sun protection fac- tended protection follows the same pattern.11 tor, or SPF. The SPF grading system is based on For example, if you normally begin to tan or ultraviolet B effects, most notably the prevention burn after 20 minutes in the sun, a PFA of 15 will of erythema, and only minimally on ultraviolet A effects. The SPF is a ratio that indicates how extend your ultraviolet A protection 15 times effective a sunscreen is at blocking ultraviolet B longer, or to 300 minutes. The American Academy of Dermatology and the Skin Cancer Foundation recommend using a sunscreen with an SPF of 15 for basic protection Table 1. Summary of Commercial Sunscreens by year round.12 SPF 15 blocks 93 percent of dam- Ingredient* aging ultraviolet rays.9 The American Academy Parsol 1789 Titanium of Dermatology insists on an even proportional- (avobenzone) (broad- Dioxide/Zinc ity of ultraviolet A to ultraviolet B protection, spectrum sunscreens) Oxide Mexoryl that is, a 1:1 SPF/PFA ratio: an increase in the Solbar AVO (SPF 32) Dura Screen La Roche- SPF (ultraviolet B protection) of a sunscreen (SPF 30) Posay must be accompanied by a proportional increase Anthelios 9 Cream in the PFA (ultraviolet A protection). With Coppertone Shade Estee Lauder Ombrelle these guidelines, La Roche-Posay currently rec- Spray/Sunblock Sunblock Sunscreen ommends a balanced protection of SPF 15 and (SPF 30/45) (SPF 30) Lotion/Spray PFA 15, advertising 15 times the protection of 12 Cetaphil Daily Facial Neutrogena Skin one’s unprotected skin. Moisturizer Sunblock The effectiveness of a sunscreen is ideal when (SPF 15) (SPF 30) 2 mg/cm2 or more is used.9 Sunscreen should be Presun Ultra Lotion/ Presun Sensitive Gel (SPF 30) Block (SPF 30) applied after strong activity that may wash off SPF, sun protection factor. sunscreen (e.g., towel drying, rubbing, sweating, *From Ting, W. W., Vest, C. D., and Sontheimer, R. Practical and and exposure to water). Other simple measures experimental consideration of sun protection in dermatology. Int. J. to protect oneself from ultraviolet light include Dermatol. 42: 505, 2003; and Ombrelle Canada. Products. Available at www.ombrelle.com/en/index.html. 2006. Accessed December 19, limiting sun exposure between 10 a.m. to 4 p.m., 2006. avoiding ultraviolet reflection surfaces (water,

1072 Volume 120, Number 4 • Mexoryl snow, and sand), checking daily ultraviolet indi- cyte layer. Mexoryl decreases instability in the me- ces, and eliminating photosensitizing drugs.2 lanocyte layer by lessening the formation of radical oxidative species when compared with a ULTRAVIOLET A DAMAGES LEADING sunscreen lacking this ultraviolet A filter.14 TO PHOTOAGING/MEXORYL (ULTRAVIOLET A FILTER) ULTRAVIOLET A DAMAGES AT THE PROTECTION TUMOR/IMMUNE LEVEL Studies have demonstrated that exposure to Mexoryl may provide greater protection against ultraviolet A irradiation can generate connective the upregulation and mutation of tumor suppres- tissue damage, such as elastosis.13 This inability of sor gene p53 than ultraviolet B filters alone. Mu- the skin to recover after deformation is the pri- tations in p53 are the most common gene muta- mary histological feature of photoaged skin.13 tions found in human cancers, particularly These changes manifest in the wrinkling, sagging, squamous cell carcinoma.14 Ultraviolet A filters increasing patchy appearance, wilting, and in- further serve to decrease the incidence of carci- creasing dryness and roughness of skin.14 nomas of the skin to a greater degree than a sun- Seite et al.1 demonstrated that this aging of the screen with only ultraviolet B blockers. skin, caused by ultraviolet A light, might be due to Mexoryl was found to decrease the ultraviolet A increased lysozyme and alpha-1 antitrypsin on impairment of the immune system. The process is elastin fibers, increased stratum corneum thick- thought to involve Langerhans cells, the epidermal ening, and enhanced epidermal ferritin expres- dendritic cells involved in antigen presentation.17 sion. Large glycoproteins, such as tenascin, are Mexoryl works by lessening the inhibition of con- unregulated in the resulting epidermal hyperpro- tact hypersensitivity response to chemical aller- liferation due to ultraviolet A irradiation, leading gens and delayed-type hypersensitivity response to to wrinkles and loss of elasticity in skin. recall antigens.14 Ultraviolet radiation-mediated Seite et al.1 have also shown that ultraviolet A immunosuppression is thought to be one of the photoprotection reduces the alterations that lead most important factors in the development of skin to photoaging. However, the molecular level at cancers such as melanoma.18 which Mexoryl is supposed to work has not been investigated. MEXORYL SX/MEXORYL XL Mexoryl comes in two formulations: SX (with ULTRAVIOLET A DAMAGES AT THE terephthalylidene dicamphor sulfonic acid; Chimex KERATINOCYTE/MELANOCYTE LEVEL SA, Le Thilay, France) and XL (with drometrizole Bernerd et al.15 conducted experiments with trisiloxane). Each one is able to reduce the effect two sunscreen products containing either an ul- of ultraviolet A light, thus protecting the skin from traviolet A filter (Mexoryl) or an ultraviolet B filter undesirable pigmentation. Mexoryl SX and XL (2-ethylhexyl-p-methoxycinnamate). They used have been shown to work synergistically to obtain an in vitro reconstructed human skin model. Since a higher level of pigmentation protection. The the different skin layers are formed in this three- reasoning behind this is that they correspond in dimensional system, the different sunscreen prod- formulation. Whereas Mexoryl SX (with tereph- ucts can be applied to the skin to mimic a more thalylidene dicamphor sulfonic acid) is hydro- realistic situation. The investigators demonstrated philic, Mexoryl XL (with drometrizole trisiloxane) that epidermal keratinocytes were preferentially is lipophilic. Furthermore, there are slight differ- targeted by ultraviolet B light, whereas ultraviolet ences in maximum absorption. Mexoryl SX is an A light induced major alterations in the dermal ultraviolet A filter with maximum absorption at compartment. Ultraviolet B light mainly induces 345 nm, whereas Mexoryl XL has two peaks, one pyrimidine dimers and pyrimidine-pyrimidone at 303 nm and the other at 345 nm.19 photo products, in contrast to ultraviolet A light, which mostly causes strand breaks and oxidative COMMERCIAL PRODUCTS damage through endogenous photosensitization.16 CONTAINING MEXORYL Mexoryl was shown to protect genomic DNA dam- Mexoryl sunscreens have been patented by the age in the keratinocyte layer and, by an unknown L’Oreal parent company. Since the early 1990s, mechanism, to decrease breaks in the DNA back- they have been sold under the La Roche-Posay bone in this layer.14 brand Anthelios and under the L’Oreal brand Ultraviolet A radiation triggers the develop- Ombrelle in Europe and Canada.12 Since U.S. ment of radical oxidative species in the melano- Food and Drug Administration approval in 2006,

1073 Plastic and Reconstructive Surgery • September 15, 2007

Mexoryl is available in the United States as An- Table 3. The L’Oreal Ombrelle Line (SPF/PFA ratio 1:1)* thelios. Regular 12 According to La Roche-Posay advertisements, Protection Kids Protection Sport Protection Anthelios SX provides balanced ultraviolet A and Lotion –- –- B protection with a 1:1 ratio of SPF/PFA protec- SPF/PFA 15 tion, which is in accordance with American Acad- Lotion Lotion SPF/PFA 30 Lotion SPF/PFA 30 emy of Dermatology guidelines.9 Anthelios SX is SPF/PFA 30 Lotion Lotion SPF/PFA 30 –- also advertised as a light, nongreasy, fragrance- SPF/PFA 30 (sensitive skin) free product. It is allergy tested, PABA-free, and extreme suitable for sensitive skin and offers 24-hour Lotion Lotion SPF/PFA 45 Lotion SPF/PFA 45 hydration.3 According to La Roche-Posay (Gail Be- SPF/PFA 45 Spray SPF/PFA –- Spray SPF/PFA 15 lott, written communication, January of 2007), An- 15/30 thelios SX was formulated as a daily moisturizer Cream –- –- with sunscreen. It is not water resistant and is SPF/PFA 60 therefore not intended for use while swimming. Lip balm –- –- SPF/PFA 30 The La Roche-Posay model works in associa- Fragrance-/ Greater water Sweatproof, tion with a patented photostabilization system. colorant-free resistance, high waterproof, The system indicates that the sunscreen’s protec- safety tolerance, nonslippery, will tion system includes active ingredients that do not fragrance- and not run into eyes lose effectiveness under sunlight. Problems with colorant-free SPF, sun protection factor; PFA, protection factor ultraviolet A. previous ultraviolet A blockers (such as Parsol *From Ombrelle Canada. Products. Available at www.ombrelle.com/ 2 1789 alone) included decreased photostability. en/index.html. 2006. Accessed December 19, 2006. The La Roche-Posay system contains the ultravi- olet A/B filter Parsol 1789 (avobenzone) and the ultraviolet B filter octocrylene, which stabilizes L’Oreal’s Ombrelle brand was launched in Parsol 1789.3 Mexoryl SX is photostable on its own. 1990. Containing Mexoryl, it is sold worldwide but La Roche-Posay’s patented photostable associa- has not been approved by the Food and Drug tion of avobenzone, octocrylene, and Mexoryl pro- Administration for sale in the United States (Gail vides complete broad-spectrum ultraviolet protec- Belott, written communication, January of 2007). tion with the highest level of protection across the These Ombrelle sunscreens contain the same for- ultraviolet A spectrum.20 According to La Roche- mulations as the Anthelios line but are categorized Posay (Gail Belott, written communication, Janu- as regular protection, kids protection, and sport 21 ary of 2007), products that are formulated to ab- protection (Table 3). This line also advertises a sorb in the ultraviolet A region typically would not 1:1 SPF/PFA ratio. interfere with products formulated to absorb in The Ombrelle regular protection formula the ultraviolet B region. Furthermore, the addi- comes in a lotion, spray, cream, and a lip balm, is tional products in Mexoryl, such as the moistur- fragrance- and colorant-free, and will maintain izers, do not interact with the ultraviolet filters. effectiveness under normal sun exposure. The La Roche-Posay sells Mexoryl-containing sun- kids protection formula is advertised as having screens in creams, sprays, and lip balms in varying greater water resistance. The sport line advertises SPF levels (30, 45, and 60) worldwide, with a cor- a sweatproof, waterproof, and nonslippery protec- relating PFA level for a 1:1 ratio (Table 2).12 The tion that is specially formulated not to run into the Anthelios line sold in the United States is only eyes. It is important to note that although it is approved for SPF 15/PFA 15 (Gail Belott, written advertised as “waterproof,” sunscreen should be communication, January of 2007). applied after any strong activity that may wash off sunscreen (e.g., towel drying, rubbing, sweating, and exposure to water).2 Table 2. The La Roche-Posay Anthelios Line (SPF/PFA ratio 1:1)* FUTURE DIRECTIONS The above findings delve into the details of the Cream Lotion Spray Lip Balm ultraviolet A blocker Mexoryl, but more work must Cre`me Lait (milk) Spray Lip Cre`me be done on the long-term safety and adverse af- SPF 60 SPF/PFA 45 SPF/PFA 30 SPF/PFA 50 fects of this sunscreen product. Work revolving SPF, sun protection factor; PFA, protection factor ultraviolet A. *From La Roche-Posay. Anthelios SX. Available at www. anthelios.com/ around possible inflammatory processes, carcino- anthelios-medical_prof.html. 2006. Accessed December 19, 2006. genic properties, and adverse skin changes di-

1074 Volume 120, Number 4 • Mexoryl rectly resulting from Mexoryl exposure must be 2. Ting, W. W., Vest, C. D., and Sontheimer, R. Practical and resolved. This may be possible with the new in vitro experimental consideration of sun protection in dermatol- ogy. Int. J. Dermatol. 42: 505, 2003. reconstructed human skin model propounded by 3. La Roche-Posay. About Anthelios SX. Available at www. 15 Bernerd et al. anthelios.com/product.html. 2006. Accessed December 19, Although the PFA scale is used to measure 2006. ultraviolet A protection, use of this particular scale 4. Meyer, N., Pruvost-Balland, C., Bourdon-Lanoy, E., Maubec, is widely debated. Strong research revolving around E., and Avri, M. F. Awareness, knowledge and attitudes to- wards sun protection among skin cancer-treated patients in this grading system is important to reach a consensus France. J. Eur. Acad. Dermatol. Venereol. 21: 520, 2007. for both research and commercial use. 5. Skin Cancer Resource Center. Medscape Today from WebMD. May 8–9, 2007. Available at www.medscape.com/ resource/skincancer. Accessed May 9, 2007. CONCLUSIONS 6. Fourtanier, A., Gueniche, A., Compan, D., Walker, S. L., and The novel ultraviolet A blocker Mexoryl has Young, A. R. Improved protection against solar-simulated been shown to play an integral role in blocking radiation-induced immunosuppression by a sunscreen with ultraviolet light. Ultraviolet A light has been found enhanced ultraviolet A protection. J. Invest. Dermatol. 114: 620, 2000. to cause varying degrees of skin damage, from non- 7. Bouillon, C. Recent advances in sun protection. J. Dermatol. melanoma skin carcinoma to elastosis, a prominent Sci. 23 (Suppl. 1): S57, 2000. histological feature of photoaged skin.13 Mexoryl 8. Lavker, R. M., Gerberick, G. F., Veres, D., Irwin, C. J., and has been found to diminish DNA damage, de- Kaidbey, K. H. Cumulative effects from repeated exposures crease instability in the melanocyte layer by lessen- to suberythemal doses of UVB and UVA in human skin. J. Am. Acad. Dermatol. 32: 53, 1995. ing the formation of radical oxidative species, de- 9. American Academy of Dermatology. Sunscreen 101. Available crease mutation of the tumor suppressor gene at www.aad.org/public/News/NewsReleases/PressϩReleaseϩ p53, and lessen impairment of the immune system, Archives/SkinϩCancerϩandϩSunϩSafety/Sunscreen101.html. all of which are caused by ultraviolet A light.14 The 2003. Accessed December 19, 2006. ultraviolet A filter provides efficient ultraviolet A 10. American Academy of Dermatology. Facts about sun- screens. Available at www.aad.org/public/News/DermInfo/ coverage, better photostability, and enhanced wa- DInfoSunscreenFAQ.html. 2006. Accessed January 22, 2007. 3 ter resistance compared with previous filters. 11. La Roche-Posay. Anthelios SX UVA protection measurement Because of its ability to block harmful ultravi- studies. Available at www.anthelios.com/pdf/UVA_RAYS_ olet A rays, Mexoryl will likely have beneficial ap- PROTECTION_MEASUREMENT.pdf. 2006. Accessed De- plications in the science of skin care. The reduc- cember 19, 2006. 12. La Roche-Posay. Anthelios SX. Available at www.anthelios. tion in carcinoma, immune impairment, and com/anthelios-medical_prof.html. 2006. Accessed December photoaging could prove crucial to the field of 19, 2006. plastic surgery. Consumers in Europe and Canada 13. Venna, S. S., and Gilchrest, B. A. Skin aging and photoaging. have been able to purchase products containing Skin Aging 12: 56, 2004. Mexoryl since the early 1990s, but only recently 14. Fourtanier, A., Bernerd, F., Bouillon, C., Marrot, L., Moyal, D., and Seite, S. Protection of skin biological targets by dif- have consumers in the United States been able to ferent types of sunscreens. Photodermatol. Photoimmunol. Pho- do so. With the Food and Drug Administration’s tomed. 22: 22, 2006. approval in 2006, Mexoryl has become widely 15. Bernerd, F., Vioux, C., and Asselineau, D. Evaluation of the available and will serve as a beneficial skin care protective effect of sunscreens on in vitro reconstructed hu- option for our patients. man skin exposed to UVB or UVA irradiation. Photochem. Photobiol. 71: 314, 2000. Gregory R. D. Evans, M.D. 16. Fourtanier, A., Labat-Robert, J., Kern, P., Berrebi, C., Gracia, Aesthetic and Plastic Surgery Institute A. M., and Boyer, B. In vivo evaluation of photoprotection 200 S. Manchester Avenue, Suite 650 against chronic ultraviolet-A irradiation by a new sunscreen Orange, Calif. 92868 Mexoryl SX. Photochem. Photobiol. 55: 549, 1992. [email protected] 17. Seite, S., Zucchi, H., Moyal, D., et al. Alterations in human epidermal Langerhans cells by ultraviolet radiation: Quan- titative and morphological study. Br. J. Dermatol. 148: 291, DISCLOSURE 2003. Neither of the authors receives any type of royalties 18. Kripke, M. L. Ultraviolet radiation and immunology: Some- nor is a paid consultant of La Roche-Posay or its parent thing new under the sun. Presidential address. Cancer Res. 54: 6102, 1994. company L’Oreal. 19. Moyal, D. Prevention of ultraviolet-induced skin pigmenta- tion. Photodermatol. Photoimmunol. Photomed. 20: 243, 2004. REFERENCES 20. La Roche-Posay. Mexoryl SX. Available at www.anthelios. 1. Seite, S., Moyal, D., Richard, S., et al. Mexoryl SX: A broad com/anthelios-aboutmexoryl.html. 2006. Accessed Decem- absorption UVA filter protects human skin from the effects ber 19, 2006. of repeated suberythemal doses of UVA. J. Photochem. Photo- 21. Ombrelle Canada. Products. Available at www.ombrelle. biol. B. 44: 69, 1998. com/en/index.html. 2006. Accessed December 19, 2006.

1075 EDITORIAL

Changing Role of the Library in Plastic Surgery Education Today

Rod J. Rohrich, M.D. Ron Hoxworth, M.D. Daniel Sullivan, M.Div. Dallas, Texas

My lifelong love affair with books and reading con- While this new system is at times cold and tinues unaffected by automation, computers, and all mechanistic, in some ways it represents a distinct other forms of the twentieth-century gadgetry. advantage in the acquisition and distribution of —From Books in My Life, Robert Downs (1903–) knowledge. Information is shared with a countless What is the role of the library in modern-day number of resources and references that are up- society and academia? Has the advent of the In- dated on a day-to-day basis from around the globe. ternet rendered the library obsolete? A recent visit Knowledge no longer filters down slowly from a to the local campus library, a visit by the senior limited number of sources, nor is it limited to the author to a public library with his children, and resources of the local library. Rather, it is imme- discussions with both residents and students pre- diately available from a variety of search engines cipitated this question. Public libraries are becom- and Web sites. This accessibility provides a distinct ing repositories for the homeless in large cities, advantage for students and residents, as informa- which is problematic. Historically, the library rep- tion is often a keystroke away. The relevant texts resented the center of academic pursuits. Hours and articles can be accessed from anywhere, were spent searching through the stacks, working thereby obviating a visit to the library for routine on term papers, doing research, and even finding issues or questions. This instant access now seems a book to read for fun. The library was the place to permeate all levels of our society. As physicians, we see this in the form of patients who arrive in our to learn, think, relax, and even socialize. It also offices armed with a plethora of information and afforded the opportunity to work without the a corresponding number of questions. This often threat of distraction or interruption while enjoy- represents a double-edged sword, as patients need ing peace and solitude. One may recall applying to be apprised of which information is relevant for a library card as a youngster and relying on the and accurate. librarian for lenience when returning a book late. In some instances, the volume of information This same librarian, it seemed, had an endless (or misinformation) available and the immediate- knowledge of reference texts, authors, and journal ness of access may prove confounding, but this titles. Dewey decimal system aside, the librarian same information and real-time interaction have was truly an endless resource who garnered much fueled much-needed research and intellectual cu- attention and respect. riosity within society. This is especially true for the Now, it seems that times have changed. User fields of science and medicine. Much of our daily access codes and online resources have replaced routine revolves around the sharing of informa- library cards. On a recent visit to the library, the tion with colleagues, coworkers, and patients via senior author was surprised to find that the “at- the Web. Questions can often be resolved with a tendant” behind the counter could do little more quick Web search rather than countless hours than give directions to an information specialist spent in the library in the hope that the relevant via telephone, who subsequently gave directions to information in the form of texts, journals, and so an online access catalog; one needed to obtain a on will be available. user number for such online access. Initially, this Libraries, in parallel with society in general proved a frustrating endeavor, but things did work and learning in particular, are undergoing a dig- out. It seems the world-wise librarian had been ital transformation. One effect of this transforma- replaced by the World Wide Web. tion is the diminishing physicality involved with learning. Books, journals, and videos more and Copyright ©2007 by the American Society of Plastic Surgeons more often are becoming downloadable files DOI: 10.1097/01.prs.0000244310.36191.80 rather than physical objects. This transformation

www.PRSJournal.com 1077 Plastic and Reconstructive Surgery • September 15, 2007 is most dramatically seen with videos, and is being Interestingly, while a number of individuals seen with journals and books. Fifteen years ago, mentioned that they saved time by not going to the video stores rented VHS tapes. They were physi- library as often, they still felt that the library was cally large, slow objects and degraded in quality the most productive atmosphere, and they used it with use. Six years ago, video stores committed to when preparing for examinations, meeting and the DVD format. DVDs, still physical objects, are collaborating with colleagues, or writing and re- much smaller, are fast, and do not degrade with viewing manuscripts. The privacy and solitude af- use—they have product longevity. Today, we’re forded by the library make concentrating on the seeing the shift to digital downloads. These down- work at hand easier and provide an escape from loads are nonphysical, they consume no physical outside distractions. Simply stated, most individ- space, are fast, and have a theoretically infinite uals still feel that they accomplish the most work longevity. Is there something important in the when they are at the library. For those of us who simple physicality of books and journals? Is the are concerned that the library has become out- process of learning somehow fundamentally dif- dated, this finding is reassuring. Some individuals ferent when the use of physical objects, such as also indicated a desire to peruse the actual texts texts, is minimized? If learning involves not only rather than the online PDF files, especially for the a transfer of information but also a relationship classic journals and texts. It is hard to dispute that with the objects of learning, how will the digital there is a certain nostalgia associated with reading revolution—and the changing role of the li- the actual manuscripts; such a connection is lost brary—change the nature of the learner-subject on the computer screen. But is this being lost by relationship? our children and the next generation of plastic A recent informal poll of students, residents, surgeons? We truly hope not! The senior author and faculty in the Department of Plastic Surgery at recalls some of the most memorable times in col- University of Texas Southwestern Medical Center lege and medical school (of course, he barely had revealed that most did a majority of their routine a place to live that was inhabitable at either), but work via Web-based computer access at work or at the library was a meeting place, a learning place, home, rather than at the library. It is the conve- a place of solitude that created a sense of accom- nience of access that seems to be responsible for plishment after a long night of study in prepara- this phenomenon, especially during those late tion for the next examination. nights when duty calls but the library is closed. It is often said that change is a good thing. When asked how often they visit the library, stu- Change can represent a necessary growth and evo- dents and residents reported an average of less lution, which is especially true in medicine. A sim- than once a week; for faculty, it was even less. Most ilar analogy can be applied to the role the library answered that it is faster and easier to use the has developed in recent years. It is still the place computer for routine tasks. Further, many implied we can rely on to learn, think, relax, and socialize, that they accomplished more and saved time with- but it is no longer the only source we have for out having to go to the library “for everything.” sharing information. And that, as the saying goes, This is not to say that the library has become is probably a good thing. obsolete. Instead, the role of the library has changed and is evolving along with how we obtain A library represents the DNA of a culture. and share information. The presence of computer —Jose G. Martı´n-Rodrı´guez, M.D. workstations with countless online resources ex- emplifies this trend. In addition, not all journals Rod J. Rohrich, M.D. have extensive online access (as Plastic and Recon- Editor-in-Chief St. Paul’s Hospital structive Surgery does), especially publications that 5909 Harry Hines Boulevard, HD01.544 are more than 10 years old. In this case, a visit to Dallas, Texas 75235-8820 the library is necessary. [email protected]

1078 EDITORIAL

What Is Plastic Surgery and Who Decides?

Thomas R. Stevenson, M.D. Sacramento, Calif.

e are finishing a face lift consultation tice requires expertise, involves few emergency and my nurse puts away our mirror. calls, and pays the bills. But who among us en- WAmy, rearranging her hair, asks a famil- tered residency simply hoping to be a successful iar question, “Why do they call it plastic surgery?” cosmetic surgeon? Unfortunately, if whittled I fumble through an explanation of Carl von down to a financially viable “chip,” plastic sur- Graefe’s use of “plastic,” meaning “to mold,” and gery would be one knife stroke away from disap- add something about having “nothing to do with pearing. No, third-party payers and financial a class of chemical compounds, but is a disci- considerations should not circumscribe our spe- pline that includes reconstructive and aesthetic cialty. surgery.” Amy’s eyes glaze over. Obviously con- Plastic surgery’s accrediting and credentialing fused but satisfied there is an answer, she walks organizations are the Plastic Surgery Residency into my manager’s office for a price quote. I am Review Committee and the American Board of left with her question and my own interpretation Plastic Surgery. Each group has a slightly differ- of it. Amy really wants to know, “What is plastic ent view of what constitutes our specialty. The surgery?” The answer depends on whom you ask. Plastic Surgery Residency Review Committee Quiz a U.S. citizen about our specialty and precisely delineates the variety and number of chances are you’ll receive a response referencing procedures each plastic surgery resident must movie stars and breast augmentation. A crude perform in order for his or her program to stay colloquial noun often will substitute for “breast.” accredited. Provide inadequate case volume and You might get a script outline from last week’s a training program risks loss of accreditation. plastic surgery reality television show. Press a Through written and oral examination pro- little further and you may hear a reference to cesses, American Board of Plastic Surgery certi- nose jobs and face lifts—occasionally cleft lip fication is granted only to those candidates who repairs or breast reconstructions. If you mention are familiar with a broad range of problems pressure sore closure or limb salvage, digital re- faced by plastic surgeons. The Residency Review plantation, or hand surgery, the reply might be, Committee and American Board of Plastic Sur- “That’s plastic surgery?” Such is our specialty’s gery determine what information a plastic sur- public perception. gery residency must impart and what a graduat- Insurers have a clearer idea of surgery’s scope ing resident must know to be board certified. but limited concerns regarding plastic surgery’s These two organizations declare what a plastic future. Give them an ICD-9 and CPT code, and surgeon starts out being, not what that surgeon they will tell you if it is covered and what they will will be doing in a mature practice. pay. Reimbursement is based on a negotiated Plastic surgeons are encouraged by the board fee-for-service scale. A plastic surgeon in private to maintain certification. Board certification is practice can decide if payment is sufficient, ac- time-limited. If a plastic surgeon wishes to main- cepting only those insurance plans that pay tain certification, that surgeon must regularly enough and rejecting others. Plastic surgeons in assess his or her patient management abilities, large multispecialty groups or academic practice identify deficiencies, and objectively demon- may not be allowed to turn down patients whose strate an effort to improve. However, this Main- plans reimburse poorly. Thus, most private prac- tenance of Certification process will not force a titioners are pushed toward performing lucrative plastic surgeon to master the same breadth of cosmetic procedures while other plastic sur- skills that surgeon possessed when he or she was geons are threatened with insolvency. Most of us initially certified. Plastic surgery’s scope cannot do some cosmetic surgery. That part of our prac- be defined by accrediting or certifying bodies. Plastic surgery training programs develop cur- Received for publication January 17, 2007. ricula based on comprehensive didactic and clin- Copyright ©2007 by the American Society of Plastic Surgeons ical outlines. Program directors are required to DOI: 10.1097/01.prs.0000278006.98901.63 educate residents across a wide spectrum. Still,

www.PRSJournal.com 1079 Plastic and Reconstructive Surgery • September 15, 2007 no two programs are identical. Some programs reconstruct burn victims, repair mangled hands, are strong in microsurgery, others in aesthetic and care for patients overseas. procedures. Newly graduated residents are as As applicants to plastic surgery programs, we different as snowflakes. Those differences grow were picked because we were capable and prom- over years of practice. Principles of problem ising in our program directors’ eyes. We were analysis and treatment planning, developed as a young surgeons who looked at things differently. resident, should be retained and used to refine Each of us vowed to be an innovator. We wanted patient care techniques. However, specific pro- to figure out a new and better way of doing cedures taught to a resident are supplanted by something. the discovery of superior ones or are shown to be Preserving that ideal and providing the ineffective, even dangerous. Who among us is chance for enthusiastic, creative young surgeons still injecting liquid silicone? When a resident to flourish is plastic surgery’s essence. Each of us finishes training, his or her perspective inter- retains a portion of that spirit. Private practitio- prets plastic surgery as that body of knowledge ners, academicians, and researchers in plastic personally amassed to date—but there will be so surgery must continue their commitment to va- much more. riety and innovation. We must encourage the Plastic surgery is defined by public opinion, American Board of Plastic Surgery and Plastic reimbursement agencies, accreditation and cer- Surgery Residency Review Committee to main- tification bodies, training program curricula, tain breadth in plastic surgery training. Our and practice patterns. Is that the entire answer? membership organizations must be stimulated to Back to Amy’s question, “What is plastic sur- provide varied educational offerings. We are ob- gery?” She may never know, but we should. I be- ligated to ensure that those opportunities we lieve plastic surgery is what plastic surgeons do.Itis enjoyed persist and are passed on to the next what we do collectively, and what this aggregate generation of plastic surgeons. body does is what each of us individually entered Thomas R. Stevenson, M.D. plastic surgery to do. Yes, it is constrained by fi- Division of Plastic Surgery nances, limited by local availability of cases, and University of California, Davis confined to its practitioners’ skills and training. Second Floor, Room 2125 Our scope may be narrowed by competing special- 2221 Stockton Boulevard ties, and certainly our practice will change. Still, we Sacramento, Calif. 95817 as a group fix clefts, treat pressure sore patients, [email protected]

American Society of Plastic Surgeons Mission Statement The mission of the American Society of Plastic Surgeons௡ is to support its members in their efforts to provide the highest quality patient care and maintain professional and ethical standards through education, research, and advocacy of socioeconomic and other professional activities.

1080 REVIEW

s a service to our readers, Plastic and Recon- the present. This monograph seems more like an Astructive Surgery® reviews books, DVDs, prac- atlas, but interestingly, it is readable from begin- tice management software, and electronic media ning to end, assuming one has a burning interest items of educational interest to reconstructive in this topic. I believe this book is targeted more and aesthetic surgeons. All items are copyrighted toward dermatologists, pathologists, and dermato- and available commercially. The Journal actively pathologists, but any discipline with an interest in solicits information in digital format (e.g., CD- the topic, even surgery, will find it worthy. ROM and Internet offerings) for review. Ackerman starts with the premise that any Reviewers are selected on the basis of relevant atypically pigmented cell found in a lymph interest. Reviews are solely the opinion of the node is defined as cancer and therefore would reviewer; they are usually published as submit- be a melanoma rather than a Spitz nevus or ted, with only copy editing. Plastic and Reconstruc- one of its many variants. He methodically ap- tive Surgery® does not endorse or recommend plies this theory to the many publications on any review so published. Send books, DVDs, and the topic, expanding it to studies on Reed’s any other material for consideration to: Jack A. spindle cell tumor, Clark’s nevus, metastasiz- Friedland, M.D., Review Editor, Plastic and Recon- ing Spitz nevus, “borderline lesions,” the “min- structive Surgery, UT Southwestern Medical Cen- imal deviation lesion,” and so on. He attempts ter, 5323 Harry Hines Boulevard, HD1.544, Dal- to clarify what is known and not known, ac- las, Texas 75390-8820. cepted and unaccepted, consistent and incon- Jack A. Friedland, M.D. sistent. For the most part, he does a magnifi- Review Editor cent job of identifying the problems that have placed us where we are today. He quotes “Spitz’s Nevus”: Reassessment Critical, nearly all of the principal authors on this topic Revision Radical to illustrate how confusing it is. I believe he has always thought this entity to be benign By A. Bernard Ackerman, M.D., with Diana Elish, M.D., (but too often misdiagnosed) and that it and Samar Shami, M.D. Pp. 360. Ardor Scribendi, Ltd., needed to be more clearly defined. In one New York, N.Y., 2007. Price: $150. section of frequently asked questions, he asks s it benign, malignant, or and answers one very cogent question: “Is Iindeterminate? This is there a histopathologist who, over the years the question asked of the of practice, has not erred in the diagnosis of pathologist with every spec- Spitz nevus and melanoma?” His answer imen submitted! is no. The Spitz nevus is an in- Throughout the initial portion of the book, teresting and confusing le- Dr. Ackerman attempts to analyze, surmise, sion, first described by pa- and even second guess each author’s motiva- thologist Sophia Spitz in tion for some of his or her statements. I found 1948. Her description was of this particularly interesting. Why did Dr. Allen, an atypically pigmented, who was a very well-known pathologist at that spindle cell skin lesion that time and Dr. Spitz’s husband, publish an arti- occurred most often in chil- cle a few years later without his wife’s input? dren. She described this entity as a benign process, Similarly, Ackerman wonders why Allen was despite one fatal case in her series of 13. This not coauthor of her landmark 1948 paper. Was lesion can be very difficult to distinguish micro- it that he disagreed with her, or just wanted scopically from melanoma. It has caused many her to have all the credit? Some of this and problems for pathologists, surgeons, dermatolo- other detective work adds favorably to the gists, and patients. All too often, it is the source of readability and ambiance of the book. litigation. “The Atlas” section of the book has many well- A. Bernard Ackerman, one of the leaders in the illustrated lesions with histopathological descrip- field of dermatopathology, attempts to cover this tions that are meticulously presented in the entity from before its inception in 1948 (1910) to usual “Ackermanian” detail; first Spitz nevi, then Reed’s nevus (a term not commonly used in reports I have seen), and then “those not readily Copyright ©2007 by the American Society of Plastic Surgeons classifiable” are presented, along with a section DOI: 10.1097/01.prs.0000280562.80044.b0 of frequently asked questions. All of this is fol-

www.PRSJournal.com 1081 Plastic and Reconstructive Surgery • September 15, 2007 lowed by “The Quiz.” This part is for the hard- fused. It did make it clearer as to why there core pathologists. The appendix even has the seems to be so little consensus. I would have original 1948 paper (reproduced as well as can loved to have read this material as a debate or be expected). “peer-reviewed” publication with opposing com- I expected to finish reading this monograph ments. Textbooks, unfortunately, are not usually with a clearer understanding of Spitz’s nevus. created this way. Unfortunately, it left me only slightly less con- Steven D. Macht, M.D.

Online CME Collections Plastic and Reconstructive Surgery is pleased to offer you Online CME Collections. Each collection represents a number of CME articles published in the Journal. These articles are suitable for use as study guides for board certification and/or re-certification, to help readers re-familiarize themselves on a particular topic, or to serve as useful reference articles. Articles less than 3 years old can be taken for CME credit. Articles are grouped in the following compilations: • According to year of publication (14 articles/collection) – 7 complete collections, 1999 to 2005 – 1 collection in process, 2006 • By topic (articles through October of 2006) – Breast (9 articles) – Cosmetic (17 articles) – Hand/Peripheral Nerve (13 articles) – Pediatric/Craniofacial (26 articles) – Reconstructive–Head and Neck (20 articles) – Reconstructive–Trunk (15 articles) – Reconstructive–Lower Extremity (5 articles) Article Format The CME articles reflect the evolution of online presentation: CME articles from 1999 are viewable in HTML format only. All CME articles from 2000 onward are in PDF format. All articles can be printed out if desired. Tests All CME articles from 1999 to 2003 have the tests included at the end of the article. These CMEs cannot be taken for credit. Answer keys are not available, but answers to every question can be found within the article. All CME articles less than 3 years old (beginning with the January 2004 CME article) are still “active”; their tests can be taken for CME credit. Tests for these CME articles can be found on the Journal Web site, under the “Online CME Articles/Tests” link. If you have not yet taken these CME tests, we encourage you to do so.

1082 LETTERS

GUIDELINES itself, the size of the other breast onto which it slides, the Letters to the Editor, discussing bed, and the angle at which the patient and her arms are material recently published in positioned. By not allowing the breast to fall medially the Journal, are welcome. They without obstruction, the subsequent change in geometry will have the best chance of ac- makes accurate marking with a straight line difficult, es- ceptance if they are received pecially in patients with very large breasts. within 8 weeks of an article’s pub- lication. Letters to the Editor We are keen to hear the authors’ experience regard- may be published with a re- ing this issue and what they believe to be the ideal sponse from the authors of the article being discussed. position for the patient to adopt. Again, we thank them Discussions beyond the initial letter and response will not for their succinct and easily adoptable description of be published. Letters submitted pertaining to published the sitting, oblique, and supine technique. Discussions of articles will not be printed. Letters to the DOI: 10.1097/01.prs.0000278197.76886.40 Editor are not usually peer reviewed, but the Journal may Tilman Stasch, M.R.C.S.(Ed.) invite replies from the authors of the original publication. All Letters are published at the discretion of the Editor. Feliciano Ciccarelli, M.D. Authors will be listed in the order in which they appear in Department of Plastic Surgery the submission. Letters should be submitted electronically Norfolk and Norwich University Hospital via PRS’ enkwell, at www.editorialmanager.com/prs/. Norwich, United Kingdom We reserve the right to edit Letters to meet requirements of space and format. Any financial interests relevant to the Correspondence to Dr. Stasch content of the correspondence must be disclosed. Submis- Department of Plastic Surgery sion of a Letter constitutes permission for the American Norfolk and Norwich University Hospital Society of Plastic Surgeons and its licensees and asignees to Colney Lane publish it in the Journal and in any other form or medium. Norwich NR4 7UY, United Kingdom The views, opinions, and conclusions expressed in the [email protected] Letters to the Editor represent the personal opinions of the individual writers and not those of the publisher, the Edi- REFERENCE torial Board, or the sponsors of the Journal. Any stated views, 1. Fahmy, F., and Hemington-Gorse, S. J. The sitting, oblique, opinions, and conclusions do not reflect the policy of any of and supine marking technique for reduction mammaplasty the sponsoring organizations or of the institutions with which and mastopexy. Plast. Reconstr. Surg. 117: 2145, 2006. the writer is affiliated, and the publisher, the Editorial Board, and the sponsoring organizations assume no responsibility Reply for the content of such correspondence. Sir: The marking of the lateral limb of the vertical markings The Sitting, Oblique, and Supine Marking in the sitting, oblique, and supine technique is done with Technique for Reduction Mammaplasty and the patient lying in the oblique position on a leveled, flat Mastopexy bed, with no pillows. The exact angle by which the patient Sir: adopts the oblique position and the position of the ipsi- e read with great interest the June 2006 article on the lateral arm are rather irrelevant, as long as the same Wsitting, oblique, and supine technique for breast re- position is maintained when the contralateral side is duction marking.1 We commend the authors for producing marked. This is to ensure postoperative symmetry. I have a straightforward, standardized technique that can be not found the size or fullness of the breast on which the adopted by experienced surgeons and trainees alike. upper breast slides to influence my approach or interfere Many surgeons have developed their own marking with the marking of a straight line. techniques over the years, often based on various DOI: 10.1097/01.prs.0000278198.32777.1d known methods. These techniques provide a great Fahmy S. Fahmy, F.R.C.S.I.(Plast.) learning experience for us as trainees, but they also Department of Plastic Surgery pose the question of uniformity. We were delighted to Countess of Chester Hospital read this article by Fahmy and Hemington-Gorse; it Liverpool Road provides a good foundation to this important step in Chester CH2 1UL, United Kingdom preoperative assessment, by offering the natural fall of [email protected] the breast as a position for marking. We have attempted to use their technique but have found that various factors influence the natural fall of the Simultaneous Endoscope-Assisted Contralateral breast when marking the lateral limb of the vertical mark- Breast Augmentation with Implants in Patients ings with the patient in the oblique position. With the Undergoing Postmastectomy Breast patient lying on her side, the upper breast adopts a medial Reconstruction with Abdominal Flaps position, and this is influenced by the fullness of the breast Sir: e read the article entitled “Simultaneous Endo- Copyright ©2007 by the American Society of Plastic Surgeons Wscope-Assisted Contralateral Breast Augmenta- DOI: 10.1097/01.prs.0000278201.07892.73 tion with Implants in Patients Undergoing Postmastec-

www.PRSJournal.com 1083 Plastic and Reconstructive Surgery • September 15, 2007 tomy Breast Reconstruction with Abdominal Flaps,” by the surgeon should choose to operate on the Betul Gozel Ulusal, Ming-Huei Cheng, and Fu Chan remaining breast using a more coherent ap- Wei (Plast. Reconstr. Surg. 118: 1293, 2006), with great proach: autologous augmentation when he or interest. We congratulate the authors on their results she performs an autologous reconstruction (i.e., and on their success rate with the cases published. bilateral transverse gracilis flaps, as described by We would like to share our opinions about some Schoeller and Wechselberger1) or breast aug- aspects of their study. mentation with implants if he or she performs a breast reconstruction using an implant. 1. We believe that the symmetrization procedure on We thank the authors for their experience and thank the opposite unaffected breast, with random bi- the editor for the opportunity to discuss this interesting opsies, is not a way to detect new carcinoma. The subject.1,3 possibility of taking a random biopsy of the con- DOI: 10.1097/01.prs.0000278199.05232.3d tralateral breast before implant placement is not safe and does not allow the surgeon to exclude a Sara Di Lorenzo, M.D. new carcinoma. Reducing the surgical manipula- Adriana Cordova, Assoc. Prof. tion of the unaffected breast is preferred when- Departments of Surgery and Oncology ever possible. Section of Plastic and Reconstructive Surgery 2. We disagree with the use of implants to create University of Studies of Palermo symmetry with the contralateral breast when the Palermo, Italy breast reconstruction is performed with autolo- Correspondence to Dr. Di Lorenzo gous tissue. If the surgeon wants to use autolo- Dipartimento di Discipline Chirurgiche ed Oncologiche gous tissue for the breast reconstruction, he or Sezione di Chirurgia Plastica e Ricostruttiva she should use the autologous technique to Universita` degli Studi di Palermo achieve symmetry with the other breast. If the Via del Vespro 123 patient wants (or needs) an augmentation of the 90127 Palermo, Italy contralateral breast with an implant, we believe [email protected] [email protected] the surgeon should use an implant for the recon- struction as well. The deep inferior epigastric REFERENCES perforator flap breast and the breast with the 1. Schoeller, T., and Wechselberger, G. Breast reconstruction by implant may be symmetrical for shape and vol- the free transverse gracilis (TUG) flap. Br. J. Plast. Surg. 57: 5, ume but not for content, and will therefore have 2004. different evolutions. The autologous reconstruc- 2. Tachi, M., and Yamada, A. Choice of flaps for breast recon- struction. Int. J. Clin. Oncol. 10: 289, 2005. tion is more permanent and the appearance of- 3. Losken, A., Carlson, G. W., Bostwick, J., III, Jones, G. E., ten improves with time, with the softening and Culbertson, J. H., and Schoemann, M. Trends in unilateral ptosing of the aging breast; implant breast recon- breast reconstruction and management of the contralateral struction results in a breast that is firmer and less breast: The Emory experience. Plast. Reconstr. Surg. 110: 89, mobile than the breast reconstructed with autol- 2002. ogous tissue. This condition and this difference will always remain the same. For the same reason, the results of correction of congenital breast asymmetry with implants are often poor and un- Reply stable. The follow-up of the cases presented is too 1,2 Sir: short. We thank Drs. Di Lorenzo and Cordova for their 3. Autologous tissue reconstruction with deep infe- interest in our article.1 We will try to explain our opin- rior epigastric perforator flaps reduces the need ions on each item. for symmetry procedures on the unaffected breast. The opposite breast is essentially the key 1. To the best of our knowledge, there are no scien- to planning unilateral breast reconstruction. Our tific data showing the detriment of biopsies or sur- opinion is that the surgeon should adjust the flap gical manipulation of the contralateral breast. Con- volume to that of the remaining breast---not the versely, since a woman with cancer in one breast other way around---using a small abdominal flap has a 3- to 4-fold increased risk of developing a new or a gracilis muscle flap, if the patient has a small cancer in the other breast, a perioperative biopsy of contralateral breast. Recreating a natural- the other breast has been advocated to detect an appearing breast mound and achieving symmetry occult tumor earlier. Anastasiadis et al.2 performed with the opposite side, without a symmetry pro- blind biopsies on the upper outer quadrant of the cedure on the opposite breast, is the first advan- opposite breast in 195 patients and found malig- tage of autologous reconstruction. nancy in 12 of them (6.2 percent). We agree that 4. Sometimes, however, the size or shape of the the balancing procedure with random biopsies on remaining breast cannot be duplicated exactly the opposite breast is not a way to exclude a sec- and symmetry is difficult to achieve. In that case, ondary breast cancer.

1084 Volume 120, Number 4 • Letters

2. The superiority of using autologous tissues over A Case for Sending Mastectomy Scars for breast implants is well established. However, the Routine Histopathology use of autologous tissue is associated with in- Sir: creased operative time, increased cost, and addi- e read with interest the article by Woerderman et tional donor-site morbidity. Therefore, we prefer Wal.1 in which they conclude that routine histo- to use it for “reconstruction” and not for purely logic analysis of mastectomy scars did not benefit their “aesthetic” (symmetrization) purposes. We do patients. Recently, similar articles have been published not agree with the necessity of using the same in plastic surgery journals and presented at scientific type of tissue for reconstruction and augmenta- meetings2–5 in which this routine practice has been tion, as Di Lorenzo and Cordova advocate. If the questioned more or less on the grounds of the costs contralateral breast augmentation is performed involved. At least one unit in the United Kingdom has using autologous tissue, the disadvantages in- abandoned its routine practice of analyzing mastec- clude an additional scar located at the inframam- tomy scars after an audit of 19 scars.3 We recently op- mary fold, additional operative time for flap dis- erated on a patient and routine histologic analysis of section and anastomoses (usually 4 to 6 hours), the scar showed recurrent cancer. We would like to the risk of re-exploration, and flap failure (2 share our experience with and thoughts on this issue. percent). Most importantly, in our series, the We performed a delayed total autologous left breast residual deep inferior epigastric perforator flap reconstruction on a 58-year-old woman using an ex- volume of 81 ml (mean volume of total deep tended latissimus dorsi flap. Fifteen years earlier, she inferior epigastric perforator flap, 608 ml; used had undergone wide local excision, axillary clearance, flap volume, 527 ml) seemed inadequate for aug- and radiotherapy for breast cancer. Three years later menting a contralateral breast mound (mean im- she was found to have a recurrence in the scar and plant volume of 189 ml was required). At a mean underwent mastectomy and chemotherapy. At the time follow-up period of 29.2 months, the shape and of reconstruction, she had a horizontal mastectomy size match were good and overall patient satisfac- scar (Fig. 1) with slight radiotherapy damage to the tion was high. skin. There was no palpable abnormality in the scar, 3. The opposite breast is one of the keys to planning chest wall, or axilla. During the procedure, she was breast reconstruction. If the size and shape of the found to have what appeared to be dense scar tissue in contralateral breast are aesthetically unpleasant, the medial part of the mastectomy scar and under the recreation of it may be desirable. In our study, all superior skin flap. The scar and additional specimens the contralateral breast augmentation proce- from under the flap were sent for routine histologic dures were requested by the patients, not sug- analysis and were reported to contain a focus of well- gested by the surgeons. Then, as reconstructive differentiated adenocarcinoma (Fig. 2). and aesthetic surgeons, we were able to discuss The patient was reassessed by the breast multidisci- with the patient that, of course, an intervention plinary team. A staging computed tomography scan to the contralateral breast could be an option to showed no evidence of any disease in the chest or obtain the best result. abdomen; a baseline magnetic resonance imaging scan 4. Please refer to answer 2. was obtained for monitoring purposes. It was thought DOI: 10.1097/01.prs.0000278227.64647.77 that tamoxifen may have been keeping her in clinical remission despite the asymptomatic relapse, and the Betul Gozel Ulusal, M.D. patient was advised to continue taking tamoxifen. It was Ming-Huei Cheng, M.D., M.H.A. Chang Gung Memorial Hospital Taipei, Taiwan Correspondence to Dr. Ulusal 9002, 2 Sok. No. 30 Oyku Apt. Dai. 5 Yesilyurt, Izmir 35370, Turkey [email protected]

REFERENCES 1. Ulusal, G. G., Cheng, M.-H., and Wei, F. C. Simultaneous endoscope-assisted contralateral breast augmentation with implants in patients undergoing postmastectomy breast re- construction with abdominal flaps. Plast. Reconstr. Surg. 118: 1293, 2006. 2. Anastasiadis, P. G., Liberis, V. A., Koutlaki, N. G., Skaphida, P. G., Avgidou, K. E., and Galazios, G. C. Incidence and de- tection of contralateral breast cancer. Breast J. 6: 178, 2000. Fig. 1. Preoperative view of the patient.

1085 Plastic and Reconstructive Surgery • September 15, 2007

ysis and that patients should be offered further treat- ment as appropriate. We do not support discontinuing this practice merely to cut costs. DOI: 10.1097/01.prs.0000278201.07892.73 Manish Sinha, M.R.C.S.Ed., Sp.R. Saurabh Gupta, M.R.C.S., S.H.O. Fiona J. Hogg, F.R.C.S.(Plast.) Institute Canniesburn Plastic Surgery Unit Glasgow Royal Infirmary Glasgow, United Kingdom Correspondence to Dr. Sinha Canniesburn Plastic Surgery Unit Glasgow Royal Infirmary 84 Castle Street Glasgow G4 0SF, United Kingdom Fig. 2. Low-power view of the mastectomy scar showing a focus [email protected] of well-differentiated adenocarcinoma (hematoxylin and eosin stain). REFERENCES 1. Woerdeman, L. A., Kortmann, J. B., and Hage, J. J. Routine histologic examination of 728 mastectomy scars: Did it benefit agreed that aromatase inhibitors would be reserved for our patients? Plast. Reconstr. Surg. 118: 1288, 2006. either a planned switch or to treat progressive disease. 2. Alam, M., Kiely, C., Shah, S. H., Lawlor, C., and O’Donnell, M. Further surgery was not advocated. She remains under Mastectomy scar histopathology of limited clinical value. Ann. regular review by the multidisciplinary team. Plast. Surg. 57: 374, 2006. In their article, the authors themselves recognize 3. Mathen, V., Khan, S., O’Brien, M., Jones, L., Harries, S., and Clarke, D. Routine histological examination of the mastec- that early detection of local recurrence is very impor- tomy scar at the time of breast reconstruction. J. Plast. Reconstr. tant, and undoubtedly such detection in mastectomy Aesthetic Surg. 59: 1248, 2006. scars could potentially benefit the patient with an early 4. Soldin, M. G., Grob, M., Dawson, A., and Cooper, M. A. Rou- 6 intervention, as reported by Zambacos et al. They re- tine histological examination of the mastectomy scar at the ported a similar case in which the patient was inciden- time of breast reconstruction: Important oncological surveil- tally found to have a recurrence based on routine his- lance? Br. J. Plast. Surg. 57: 143, 2004. tologic analysis of the scar. Their patient received 5. Alam, M., Shah, S. H. A., and O’Donnell, M. Mastectomy scar further adjuvant chemotherapy. Very few such cases are histopathology of limited clinical value. Presented at the win- known,2,6–8 but it is likely that many more have simply ter meeting of the British Association of Plastic, Reconstruc- gone unreported. tive, and Aesthetic Plastic Surgery, London, Dec. 6-8, 2006 Although it is impossible to say whether or not in the (abstract, p. 113). long run such patients would benefit from early detec- 6. Zambacos, G. J., Wilson, P. A., Miminas, D., and Morris, R. J. tion of asymptomatic recurrence, the potential for ben- Routine histological examination of the mastectomy scar at the time of breast reconstruction. Br. J. Plast. Surg. 58: 122, efit does exist. It is equally unclear whether any systemic 2005. therapy for locoregional recurrence could increase the 7. Granick, M. S., Bragdon, R. W., and Hanna, D. C. Recurrent overall survival rate. Although we agree with the au- breast carcinoma at the time of breast reconstruction. Ann. thors that the pick-up rate of recurrence is extremely Plast. Surg. 18: 69, 1987. low, unless it is proven beyond a doubt that such find- 8. Montandon, D. Incidental discovery of recurrent breast car- ings offer no benefit to the patient, we believe that the cinoma in patients seeking breast reconstruction. Br. J. Plast. scars should be routinely subjected to histological anal- Surg. 32: 318, 1979.

1086 VIEWPOINTS

GUIDELINES At the time of the operation, the patient had been in Viewpoints, pertaining to is- full clinical remission for 6 months, but she was still sues of general interest, are wel- receiving treatment with infliximab (7 mg/kg every 5 come, even if they are not related weeks) and methotrexate (27.5 mg per week). She has to items previously published. had one episode of disease flare with nasal chondritis, Viewpoints may present unique but the graft reconstruction has remained intact (Fig. techniques, brief technology up- dates, technical notes, and so on. 1). Viewpoints will be published on Relapsing polychondritis is a rare systemic inflam- a space-available basis because they are typically less time- matory disease that results in degenerative changes to sensitive than Letters and other types of articles. Please cartilage. Clinical features vary widely. McAdam et al.1 note the following criteria: provided a useful lexicon of clinical criteria to establish • Text—maximum of 500 words (not including the diagnosis (Table 1). references) This report is unusual for many reasons. First, most • References—maximum of five cases of relapsing polychondritis occur between ages 40 • Authors—no more than five • and 60. Reports of relapsing polychondritis in the pe- Figures/Tables—no more than two figures and/or one diatric population are uncommon, with about 30 cases table 2 Authors will be listed in the order in which they appear reported in the extant medical literature. Thus, it is in the submission. Viewpoints should be submitted elec- not surprising that there are only a handful of reported tronically via PRS’ enkwell, at www.editorialmanager.com/ prs/. We strongly encourage authors to submit figures in color. We reserve the right to edit Viewpoints to meet re- quirements of space and format. Any financial interests relevant to the content must be disclosed. Submission of a Viewpoint constitutes permission for the American So- ciety of Plastic Surgeons and its licensees and assignees to publish it in the Journal and in any other form or medium. The views, opinions, and conclusions expressed in the Viewpoints represent the personal opinions of the indi- vidual writers and not those of the publisher, the Editorial Board, or the sponsors of the Journal. Any stated views, opinions, and conclusions do not reflect the policy of any of the sponsoring organizations or of the institutions with which the writer is affiliated, and the publisher, the Edi- torial Board, and the sponsoring organizations assume no responsibility for the content of such correspondence.

Durability of Nasal Reconstruction in an Adolescent with Relapsing Polychondritis Treated with Infliximab Sir: e report a rare case of saddle nose deformity Wsecondary to relapsing polychondritis in an ad- olescent girl. She underwent nasal reconstruction with a costochondral graft. Stability of the autologous graft was observed more than 1 year postoperatively, despite one episode of disease exacerbation. A 14-year-old girl with relapsing polychondritis had been treated by the rheumatology service with chemo- therapeutic agents (prednisone, methotrexate, naproxen, and infliximab) for 22 months. Multiple flares of nasal chondritis for 18 months before diag- nosis had resulted in a saddle nose deformity. Severe auricular chondritis followed ear piercing. The pa- tient’s disease was recalcitrant to treatment until the Fig. 1. (Above) Preoperative view. The nasal dorsum is concave, introduction of infliximab, which induced remission. and there is an apparent cephalic rotation of the nasal tip. The concavity is present in the osseous and cartilaginous dorsum. Copyright ©2007 by the American Society of Plastic Surgeons (Below)Postoperativeview.Resultsat1yearindicatedurabilityof DOI: 10.1097/01.prs.0000278224.14221.c9 the graft despite two episodes of clinical disease progression.

www.PRSJournal.com 1087 Plastic and Reconstructive Surgery • September 15, 2007

Table 1. Clinical Criteria for Relapsing Peter D. Witt, M.D. Polychondritis* Pediatric Plastic Surgery ● Children’s Hospital Central California Bilateral auricular chondritis† Madera, Calif. ● Nonerosive seronegative inflammatory polyarthritis ● Nasal chondritis with saddle nose deformity Correspondence to Dr. Witt ● Ocular inflammation, including conjunctivitis, scleritis- 9300 Valley Children’s Place episcleritis, and iritis ● Madera, Calif. 93638-8762 Respiratory tract chondritis [email protected] ● Audiovestibular damage (vertigo and sensorineural hearing loss) REFERENCES *From McAdam, L. P., O’Hanlan, M. A., Bluestone, R., et al. Re- lapsing polychondritis: Prospective study of 23 patients and a review 1. McAdam, L. P., O’Hanlan, M. A., Bluestone, R., et al. Relaps- of the literature. Medicine (Baltimore) 55: 193, 1976. ing polychondritis: Prospective study of 23 patients and a †Recurrent chondritis of both ears is virtually pathognomonic. review of the literature. Medicine (Baltimore) 55: 193, 1976. 2. Zeuner, M., Straub, R. H., Rauh, G., Albert, E. D., Scholmer- ich, J., and Lang, B. Relapsing polychondritis: Clinical and immunogenetic analysis of 62 patients. J. Rheumatol. 24: 96, cases of saddle nose deformity in children secondary to 1997. relapsing polychondritis, and in none of those cases was 3. Herman, J. H. Clinical manifestations of relapsing polychon- reconstruction attempted. Second, the literature on dritis. Available at http://www.uptodate.com. current surgical therapy for relapsing polychondritis 4. Jones, F. R. Relapsing polychondritis: Case report. Plast. Re- offers little encouragement for surgeons to intervene constr. Surg. 51: 331, 1973. with nasal reconstruction. It is possible that nasal re- construction in this small population has been avoided because of concern about the periodic flares of inflam- Lateral Septal Preservation: A Technique to mation that might threaten the reconstruction by spe- Improve Projection in Inferior Pedicle cific disease targeting of the graft. The vulnerability of Reduction Mammaplasty by Preventing Lateral cartilage grafts to disease progression, as well as the Displacement of the Pedicle clinical resilience of grafts used for reconstruction, has Sir: not been addressed. he modified Wise pattern with inferior pedicle is What is known about nasal involvement in relapsing the most commonly utilized breast reduction tech- polychondritis? It seems to occur approximately 27 per- T nique in the United States.1 Despite the safety, simplic- cent of the time during the onset of disease and ap- ity, and predictability of the inferior pedicle technique, proximately 60 percent of the time at some point dur- it has a few drawbacks, including long incision lines and ing the course of the disease.3 The actual extent of nasal a lack of parenchymal support, which may result in involvement can vary widely, ranging from mere con- lateral displacement of the pedicle and bottoming-out gestion and rhinorrhea to epistaxis to frank destruction of the breast.1,2 of the nasal cartilage, resulting in the classic saddle nose We present a simple maneuver to increase paren- deformity.4 chymal support. Our technique prevents lateral dis- Past approaches have not modified the disease’s nat- placement of the inferior pedicle, improves projection, ural history consistently. However, with the introduc- and reduces the amount of skin tension needed to tion of the biologic anti–tumor necrosis and alpha produce a conical breast. agents, disease remission can be achieved with de- Preoperative skin markings are made for a modified creased morbidity. Wise pattern with inferior pedicle. The pedicle is de- It seems logical that reconstruction be limited to epithelialized. We prefer the “peeling orange” de-epi- selected patients whose disease is in remission, whose thelialization technique to shorten the operative time.3 systemic immunosuppression is minimal, and whose Skin incisions are then made, and a superior skin/fat psychosocial stigmatization is problematic. This report flap is raised by working from medial to lateral, ex- simply highlights the fact that adolescents affected by tending up to the clavicle. The pectoralis muscle is relapsing polychondritis may benefit from reconstruc- identified during elevation of the superior skin/fat tive surgery (correction of saddle nose deformity) using flap, and caution is taken not to pass the lateral border autogenous cartilage, and that the cannibalistic effects of the muscle, since this will be the medial aspect of the of relapsing polychondritis do not necessarily affect the retained septum. Once the lateral border of the pec- cartilage used for that reconstruction when the patient toralis muscle is reached, the undermining is stopped, is maintained on treatment with inflixinab and meth- leaving a septum, consisting of fat and fibrous tissue, otrexate. attached from skin to pectoralis fascia. The medially DOI: 10.1097/01.prs.0000278184.60488.8e undermined breast/fat tissue is resected in an en bloc David Bell, M.D., D.D.S. fashion, and raising of the superior skin flap is restarted Pediatric Plastic Surgery laterally, leaving a 1-cm-wide septum along the lateral Dowain Wright, M.D., Ph.D. border of the pectoralis muscle. The second portion of Pediatric Rheumatology the resection is then performed lateral to the septum.

1088 Volume 120, Number 4 • Viewpoints

After completion of the resection, the inferior pedicle REFERENCES is tucked into the superomedial pocket that has been 1. Rohrich, R. J., Gosman, A. A., Brown, S. A., et al. Current created. The septum along the lateral pectoral border preferences for breast reduction techniques: A survey of creates the lateral wall of the pocket when the skin flap board-certified plastic surgeons 2002. Plast. Reconstr. Surg. 114: is redraped over the inferior pedicle, defines the lateral 1724, 2004. curve of the final breast shape, and serves as an internal 2. Hawtof, D. B., Levine, M., Kapetansky, D. I., et al. Complica- brassiere (Fig. 1). tions of reduction mammaplasty: Comparison of nipple-are- The lack of parenchymal support, which may result olar graft and pedicle. Ann. Plast. Surg. 23: 3, 1989. in lateral displacement and/or bottoming-out of the 3. Ceydeli, A., and Hunter, J. G. Peeling orange: Rapid deepi- thelialization in reduction mammaplasty. Aesthetic Surg. J. 24: breast, is one of the main drawbacks of the inferior 580, 2004. pedicle reduction mammaplasty technique. To obtain a conical breast, the skin envelope is used as an external brassiere. The wider the angle between the two vertical A Baby with Osteomyelitis after a Grade II incisions, the more conical the breast. However, as the angle increases, the tension on the skin closure in- Burn creases, which predisposes the patient to unfavorable Sir: scars. Our simple maneuver minimizes the lateral dis- e describe the case of a baby with osteomyelitis at placement of the pedicle and reduces the need to use Wthe site of a grade II burn. Case reports of burn- skin envelope resection to produce a conical breast. related osteomyelitis have previously been published, In summary, lateral septal preservation in inferior but no pediatric study has reported infantile osteomy- pedicle reduction mammaplasty is simple and has a elitis following grade II burns. short learning curve. The technique is reproducible, The patient was an 11-month-old boy. He was burned with no apparent complications, and creates an aes- on the face, right anterior thoracic region, and right thetically pleasing breast shape. It requires, however, a brachium by boiled water in a pot. A grade IIs/IId burn more intricate dissection of the superior skin flap. wound was noted, and the burned area was 16 percent. DOI: 10.1097/01.prs.0000278185.71693.18 Conservative therapy was started in our emergency cen- Adil Ceydeli, M.D., M.S. ter. Fever (38.5°C or higher) occurred 5 days after injury. Culture of the wound site revealed methicillin- John Louis, M.D. resistant Staphylococcus aureus, so 120 mg/day of cef- Jack Yu, M.D., D.D.S., M.S. capene pivoxil hydrochloride was administered orally. Epithelization was favorable, despite the patient having Edmond Ritter, M.D. a slight fever (37°C), and the burn wound improved Division of Plastic and Reconstructive Surgery Medical College of Georgia slightly. The infant was referred to the plastic surgery Augusta, Ga. department 12 days after injury (Fig. 1). Fever (38.5°C Correspondence to Dr. Ceydeli Division of Plastic and Reconstructive Surgery Medical College of Georgia 1467 Harper Street, HB-5040 Augusta, Ga. 30912 [email protected]

Fig. 1. The lateral septum and superomedial pocket are shown Fig. 1. Epithelization was favorable, despite a slight fever 12 for the left breast. days after injury.

1089 Plastic and Reconstructive Surgery • September 15, 2007 or higher) persisted, and blood culture 17 days after immobility of the affected limb led to an early diagno- injury revealed methicillin-resistant S. aureus. Vanco- sis. Incision/drainage and continuous drainage mycin hydrochloride (100 mg per day) was adminis- achieved good results. However, osteomyelitis may re- tered intravenously, and pyretolysis was achieved. Ep- sult in deformity through a growth disorder of the ithelization of the burn wound was observed 27 days affected limb and differences in upper limb length. In after injury, with the disappearance of methicillin-re- the future, bone growth and the grade of deformity sistant S. aureus in the wound site. However, 30 days should be carefully evaluated. after injury, the infant was distressed and did not move In a baby, mild trauma may cause serious disorders his right upper limb. Radiographs showed a circum- due to reduced immune capacity. The present case ferential periosteal reaction involving the humeral di- suggests the risk of osteomyelitis related to grade II aphysis and metaphysis and a translucent area in the burns. Close follow-up is needed, considering the onset proximal/distal humeral metaphysic (Fig. 2). Bone of osteomyelitis after epithelization. scintigraphy revealed accumulation at the same site, DOI: 10.1097/01.prs.0000278225.45314.4f suggesting osteomyelitis. Surgery was considered nec- Shinichi Asamura, M.D. essary 34 days after injury, and incision/drainage and Kenji Fukunishi, M.D. continuous drainage were performed. The infant was discharged 54 days after injury; he was negative for Kazuhide Matunaga, D.D.S. C-reactive protein, and fever was not noted. There were Takahiro Hashimoto, M.D. no abnormal findings in the right upper limb. The sequelae of burns involving the bones and joints Noritaka Isogai, M.D. include osteomyelitis, pyogenic arthritis, and ectopic Department of Plastic and Reconstructive Surgery ossification.1–3 In a recent clinical and radiographic Kinki University School of Medicine Osaka, Japan study, Pandit et al.4 found a 2.5 percent incidence of osteomyelitis in a series of 80 burned patients. In ad- Correspondence to Dr. Asamura dition, osteomyelitis accompanies deep burns; our case Department of Plastic and Reconstructive Surgery of a patient with osteomyelitis following a grade II burn Kinki University School of Medicine is very rare case. 377-2 Ohno-higashi Osteomyelitis is classified into two types based on Osaka-sayama, Osaka 5898511, Japan [email protected] anatomical features and the patient’s condition, ac- [email protected] cording to Cienery’s classification system. In our pa- tient, we speculated that methicillin-resistant S. aureus- REFERENCES emia was involved in the pathogenesis of osteomyelitis. 1. Alfie, M., Benmeir, P., and Caspi, R. Costal osteomyelitis due However, atopic dermatitis was observed concurrently, to an electrical burn. Burns 21: 147, 1995. and topical infection cannot be ruled out; the route of 2. Mullins, R. F., Still, J. M., Savage, J. B., et al. Osteomyelitis of 5 infection remains to be clarified. the spine in a burn patient due to Candida albicans. Burns 19: In this study, the 11-month-old infant could not com- 174, 1993. plain about his symptoms, but his discomfort and the 3. Evans, E. B. Musculoskeletal changes secondary to thermal burns. In D. N. Herdon (Ed.), Total Burn Care, 1st Ed. London: Saunders, 1996. 4. Pandit, S. K., Malla, C. N., Zarger, H. U., et al. A study of bone and joint changes secondary to burns. Burns 9: 227, 1993. 5. Mader, J. T., and Mandell, G. L. Osteomyelitis. In G. L. Man- dell, J. E. Bennett, and R. Dolin (Eds.), Principles and Practice of Infectious Diseases, 5th Ed., Vol. 1. Philadelphia: Churchill- Livingstone, 2000. Pp. 1182-1196.

Reconstruction of an Achilles Tendon Defect with Vascularized Abdominal Wall Fascia Sir: egmental loss of the Achilles tendon presents a Sreconstructive challenge, especially when it is com- bined with defects in soft-tissue coverage. Several free tissue options have been reported, including conven- tional tendon reconstruction combined with an over- lying muscle or skin flap to provide soft-tissue coverage1 and composite reconstruction with the latissimus,2 ten- Fig. 2. Radiograph shows a periosteal reaction involving the hu- sor fasciae latae,3 gluteus,4 or lateral arm flaps.5 meral diaphysis and metaphysis and a translucent area in the This communication reports a composite recon- proximal/distal humeral metaphysic. struction technique for single-stage Achilles tendon re-

1090 Volume 120, Number 4 • Viewpoints pair. A rectus muscle free flap is used for soft-tissue fill and bone coverage, and its overlying vascularized ab- dominal wall fascia is used to restore tendon continuity. A 57-year-old woman presented to her orthopedic surgeon with a painful calcaneal bone spur. The bone spur was removed surgically and the Achilles tendon was reattached. A wound infection developed beneath the cast, resulting in an 8-cm segmental tendon loss (Fig. 1). The wound was debrided, and a rectus muscle flap with attached vascularized fascia was developed, taking the fascia 4 cm wide by 8 cm long. The flap was transferred with the muscle belly deep, to cover the exposed bone and fill the dead space. The fascia was secured to the proximal and distal tendon remnants with 2-0 Prolene. A segmental occlusion of the poste- rior tibial artery recipient vessel was replaced with a reversed graft of posterior tibial vena comitans. The implantable Doppler probe was used for postoperative Fig. 2. Postoperative view 4 years after tendon repair with vas- flap monitoring. A split-thickness skin graft was applied cularized abdominal wall fascia. to the outer surface of the vascularized fascia. No vascular problems were encountered with the flap. A portion of the skin graft did not survive and required regrafting. The patient used a protective struction. Flap dissection is straightforward, requiring splint for approximately 6 weeks and was transitioned no position changes on the operating room table, and to full weightbearing at 10 weeks. She was able to walk the flap vessels are large enough to be attached under without a cane approximately 5 months postopera- loupe magnification. In the future, I would use an tively. unmeshed skin graft to enhance the cosmetic result. At 4-year follow-up, the tendon repair has proved to The advantages of this technique include single-stage be durable and functional. The patient is able to climb reconstruction, acceptable donor-site morbidity, and stairs without difficulty and can support her body sustained tendon strength. weight with the repaired tendon (Fig. 2). She can dor- DOI: 10.1097/01.prs.0000278222.30739.1b siflex the affected right ankle 15 degrees (versus 10 Daniel F. Haynes, M.D. degrees on the left side) and plantarflex 30 degrees Department of Surgery (versus 35 degrees on the left side). The skin graft Division of Plastic Surgery utilized over the fascia has provided stable coverage and East Tennessee State University a cosmetically acceptable ankle contour. Box 70575 Johnson City, Tenn. 37604 In this case, the rectus fascia proved to be a durable [email protected] substitute for the Achilles tendon. It avoids the bulk associated with the lateral arm flap and gluteal flaps and shortens healing time compared with staged recon- DISCLOSURES This communication references the Cook implantable Doppler probe, as well as Prolene suture and mesh. The author has no financial interest in Cook Vascular. He owns shares of common stock in Johnson & Johnson, which produces the Ethicon line of sutures and mesh, including Prolene.

REFERENCES 1. Ronel, D. N., Newman, M. I., Gayle, L. B., and Hoffman, L. A. Recent advances in the reconstruction of complex Achilles tendon defects. Microsurgery 24: 18, 2004. 2. Lee, H. B., Lew, D. H., Oh, S. H., et al. Simultaneous recon- struction of the Achilles tendon and soft-tissue defect using only a latissimus dorsi muscle free flap. Plast. Reconstr. Surg. 104: 111, 1999. 3. Haddad, J. L., Chavez-Abraham, V., Carrera, J., et al. Micro- surgical reconstruction of the Achilles tendon with a fascia lata flap. J. Reconstr. Microsurg. 13: 309, 1997. Fig. 1. Preoperative view of the right ankle shows repair dehis- 4. Papp, C., Todoroff, B. P., Windhofer, C., and Gruber, S. cence and tendon necrosis. Partial and complete reconstruction of Achilles tendon de-

1091 Plastic and Reconstructive Surgery • September 15, 2007

fects with the fasciocutaneous infragluteal free flap. Plast. REFERENCES Reconstr. Surg. 112: 777, 2003. 1. Berry, S. M., and Fischer, J. E. Biliary and gastrointestinal 5. Berthe, J. V., Toussaint, D., and Coessens, B. C. One-stage fistulas. In S. I. Schwartz, H. Ellis, and W. C. Husser (Eds.), reconstruction of an infected skin and Achilles tendon defect Maingot’s Abdominal Operations, 10th Ed. Stamford, Conn.: with a composite distally planned lateral arm flap. Plast. Re- Appleton and Lange, 1997. Pp. 581-625. constr. Surg. 102: 1618, 1998. 2. Erdmann, D., Drye, C., Heller, L., et al. Abdominal wall defect and enterocutaneous fistula treatment using the vac- uum-assisted closure system. Plast. Reconstr. Surg. 108: 2066, 2001. Use of the Vacuum-Assisted Closure System in the Treatment of Enterocutaneous Fistulas: A Follow-Up Sir: Comparing the Ultrasonically Activated Scalpel he term fistula defines an abnormal communica- (Harmonic) with High-Frequency Electrocautery Ttion between two epithelialized surfaces. Intestinal for Postoperative Serous Drainage in Massive fistulas that communicate with the skin are enterocu- Weight Loss Surgery taneous fistulas.1 Enterocutaneous fistulas remain a challenging clinical problem associated with compli- Sir: cated postoperative courses and long-term disability, ltrasonic dissection using the Harmonic scalpel particularly in patients with solid or visceral malignan- Uhas recently emerged as a safe and reliable alter- cies, gastrointestinal conditions, or a history of multiple native to high-frequency electrocautery. The Harmonic abdominal operations. ultracision scalpel and scissor has been used success- A previous publication from our institution in 2001 fully by surgeons in laparoscopic and open surgical procedures, including cholecystectomy and breast can- introduced the vacuum-assisted closure system for 1–4 treating enterocutaneous fistulas as a nonstandard cer dissections. The aim of this prospective, single- use.2 Since this report, we have applied the system in a blinded, two-arm study was to investigate the clinical series of 15 patients with enterocutaneous fistulas by merits of the ultrasonic scalpel (Harmonic) versus clinical examination and/or radiographic confirma- high-frequency electrocautery in body lift operations tion. All cases resulted from either postoperative ero- with regard to postoperative serous drainage time and sion of exposed bowel, bowel erosion through the sub- volume. cutaneous tissue, or anastomotic leak. Lower body lift procedures without simultaneous The enterocutaneous fistulas closed if no mucosa tightening of the medial aspect of the thigh were car- was visible in the wound (n ϭ 11); no closure occurred ried out in 20 patients with two treatment arms. Tissue if mucosa was apparent (n ϭ 4). The fistula output did dissection and resection were performed using the ul- not seem to affect closure rates, and among the fistulas trasonic scalpel (Harmonic) on one side (treatment arm 1, n ϭ 20) and electrocautery on the other (treat- that closed, the mean time to closure was 13 days. ϭ Indicators for successful conservative management of ment arm 2, n 20). All operations were performed by enterocutaneous fistulas using the vacuum-assisted clo- the senior author (D.F.R.). Drainage days (i.e., number sure system seem to be large bowel fistulas and no of days until drain removal) and total drainage (i.e., visible mucosa in the wound. postoperative wound secretion via the individual DOI: 10.1097/01.prs.0000278223.62852.ce drains) were assessed as primary endpoints. In addi- tion, operative time (from first skin incision until last Detlev Erdmann, M.D., Ph.D. skin suture), postoperative complications, and the dif- Michael S. Wong, M.D. ference in preoperative and postoperative thigh cir- cumference were recorded; the pain score (per day) Salvatore C. Lettieri, M.D. was measured using a 10-point visual analog scale, with L. Scott Levin, M.D. 0 ϭ no pain and 10 ϭ the worst imaginable pain (sec- Laura A. Gunn, M.D. ondary endpoints). Student t tests for independent Division of Plastic, Reconstructive, Maxillofacial, and Oral samples were used for inferential statistical analysis. Surgery Total serous drainage volume was significantly lower Department of Surgery in the Harmonic scalpel group (891.67 Ϯ 392.09 ml) Duke University Medical Center compared with the electrocautery group (1414.38 Ϯ Durham, N.C. 656.90 ml) (p ϭ 0.007). Similarly, the number of drain- Correspondence to Dr. Erdmann age days was significantly lower in the Harmonic scalpel group (5.35 Ϯ 1.14 days, compared with 7.04 Ϯ 1.92 Division of Plastic, Reconstructive, Maxillofacial, and Oral ϭ Surgery days for electrocautery; p 0.002). Patients in the Duke University Medical Center Harmonic scalpel group reported lower pain intensity P.O. Box 3181 scores (mean score Ϯ SD for postoperative days 1 Durham, N.C. 27710 through 15, 1.84 Ϯ 0.58, compared with 2.44 Ϯ 0.71 for [email protected] electrocautery; p ϭ 0.011).

1092 Volume 120, Number 4 • Viewpoints

The incidence of complication was assessed for each Correspondence to Dr. Stoff side of the body. On the electrocautery side, seroma Department of Plastic and Reconstructive Surgery formation was observed in five patients (25 percent) Dreifaltigkeits Hospital and treated by aspiration [Harmonic side, two patients Bonner Strasse 84 (10 percent)]. Two of these five patients presented with 50389 Wesseling [email protected] bilateral seroma formation in the area of the lateral thigh, and the other three patients showed a unilateral Presented at the 37th Annual Meeting of the Ger- mass formation that required treatment by aspiration. man Society of Plastic Surgeons, in Aachen, Germany, No patient had postoperative bleeding, but one patient September 29 through October 2, 2006. (5 percent) required a postoperative blood transfusion due to extensive intraoperative blood loss that included DISCLOSURES both the electrocautery and Harmonic sides. Three Drs. Reichenberger and Stoff have no financial in- patients (15 percent) had delayed wound healing due to local wound infections that involved both sides. No terest in any of the products, devices, or drugs mentioned wound necrosis requiring treatment was assessed in this in this article. Dr. Richter has a consulting agreement study. with Ethicon. The Harmonic scalpel allows for safe and efficient tissue dissection in massive weight loss procedures. In REFERENCES addition, the results show that use of the Harmonic 1. Deo, S. V., Shukla, N. K., Asthana, S., Niranjan, B., and Srini- scalpel in tissue dissection significantly reduces the vas, G. A comparative study of modified radical mastectomy postoperative serous drainage time and volume as well using harmonic scalpel and electrocautery.. Singapore Med. J. as postoperative pain in comparison with electrocau- 43: 226, 2002. tery, with increased patient comfort postoperatively. 2. Deo, S. V., and Shukla, N. K. Modified radical mastectomy DOI: 10.1097/01.prs.0000278224.14221.c9 using harmonic scalpel. J. Surg. Oncol. 74: 204, 2000. Alexander Stoff, M.D. 3. Deo, S., Hazarika, S., Shukla, N. K., Kar, M., and Samaiya, A. A prospective randomized trial comparing harmonic scalpel Matthias A. Reichenberger, M.D. versus electrocautery for pectoralis major myocutaneous flap Dirk F. Richter, M.D. dissection. Plast. Reconstr. Surg. 115: 1006, 2005. Department of Plastic and Reconstructive Surgery 4. Amaral, J. F. Laparoscopic cholecystectomy in 200 consecutive Dreifaltigkeits Hospital patients using an ultrasonically activated scalpel. Surg. Lapa- Wesseling, Germany rosc. Endosc. 5: 255, 1995.

Plastic Surgery Educational Foundation Mission Statement The mission of the Plastic Surgery Educational Foundation® is to develop and support the domestic and international education, research, and public service activities of plastic surgeons.

1093 OBITUARY

Dr. Ulrich T. Hinderer Meise, 1924 to 2007 Miguel Chamosa, M.D. Ezequiel Rodriguez, M.D. Madrid, Spain

r. Hinderer passed away on January 1, 2007, at Dhis home in Madrid. He was 82 years old. Born in Madrid of German parents in the renowned district of Chamberı´, he always lived his life to the fullest in both the German and Spanish cultures. The outbreak of World War II found him in boarding school in Germany, and in 1941, he joined the armed forces at the tender age of 17, fighting on the front line for 3 years. Among other battles, he fought in Stalingrad and, later, as an officer, in the famous battle of the Ardennes, suf- fering severe injuries. Awarded the Iron Cross in 1945, he returned to Madrid more mature than his years, due to the harsh experiences he had en- dured during the war. He used to say, “What doesn’t destroy you makes you stronger.” Dr. Hinderer studied at the Faculty of Medi- cine at the Complutense University of Madrid, obtaining his degree in 1950. He continued his training in plastic surgery there and at the Uni- Dr. Ulrich T. Hinderer Meise, 1924 to 2007. versity of Dusseldorf. As a result of his uncountable professional successes, Dr. Hinderer was everything in plastic surgery, including professor of plastic surgery at Ulrich was a great lecturer and published hun- the Complutense University, chief editor of Span- dreds of articles in which he described original ish Plastic Surgery (now known as Ibero-Latinameri- surgical techniques in plastic surgery (articles on can Plastic Surgery), and founder and editor of the congenital anomalies, otoplasty, hypospadias, and journal Aesthetic Plastic Surgery. His contribution so on) and aesthetic surgery (such as lifting, mam- and experience helped develop these journals maplasty, and blepharoplasty). A tireless doctor, into the well-known publications they are today. plastic surgeon, founder of many scientific soci- Undeniably, his major roles were as eighth general eties worldwide, and editor of national and inter- secretary of the International Confederation of national journals, his legacy is as valuable as it is Plastic Reconstructive and Aesthetic Surgery and unforgettable. We will remember him as a great as president of the International Plastic, Recon- human being and an excellent professional; he structive, and Aesthetic Surgery Foundation. leaves us an entire life dedicated to medicine, Dr. Hinderer was honest, hard working, and showing true vocation until the last days of his life. disciplined. Blair Rogers called him the “indefat- Right now, he is probably discussing new sur- igable Hinderer,” and Tom Biggs used to say to his gical techniques with other great contributors, residents, “If you think you have found a new sur- such as Tagliacozzi, Langenbeck, Dieffenbach, gical technique, revise your bibliography, because Sanvenero-Roselli, Gonza´lez Ulloa, Salvador Cas- either it is of no importance or you will probably find tan˜ares, and others, and he is almost certainly that Hinderer has already published it!” trying to create a Society of Plastic and Aesthetic Surgery in heaven! From private practice. Rest in peace, “Uncle Uli.” Received for publication February 3, 2007; accepted February 15, 2007. Miguel Chamosa, M.D. Copyright ©2007 by the American Society of Plastic Surgeons Paseo de la Castellana 113 28046 Madrid, Spain DOI: 10.1097/01.prs.0000278183.10332.30 [email protected]

1094 www.PRSJournal.com ANNOUNCEMENTS

nnouncements of meetings and symposia Unless otherwise noted, information on the fol- should be sent to the Editor at least 9 lowing can be obtained by calling the ASPS/PSEF Amonths before they are to take place. Member Services Center toll free at 1-800-766-4955 or 847-228-9900, ext. 471 (outside the United States). Meetings listed with an “image number” (in parentheses) allow members to access ASPS/PSEF sponsored or endorsed meeting brochures and registration forms by fax 24 hours a day. To obtain a copy of a meeting brochure/registration form by fax, simply call the toll-free Faxback number, 1-800- 333-8835. Enter your fax number, followed by the number listed in the meeting information printed in this calendar. Meeting information is subject to change. PLASTIC SURGERY 2007 Please refer to the current calendar of plastic sur- The Plastic Surgery 2007 Annual Meeting will gery meetings at www.plasticsurgery.org (Upcoming be held October 26 through 31, 2007, in Balti- Events) for the most up-to-date listings. more, Md. Notable features include exclusive ma- terial not available at other national meetings and, ASPS PLASTIC SURGERY CODING WORKSHOPS new to our program, Botox and migraines, reju- The schedule for the Plastic Surgery Coding venation of the orbit, treating nonmicrotia ear Workshops for plastic surgeons and office staff for deformities, genioplasty, the semi-bionic man, 2007 is as follows: identifying psychiatric disorders, and more. New courses will discuss how to make a living from November 30 and December 1, 2007 reconstructive surgery, utilizing patient consult- The Palmer House ants for financial efficiency and time manage- Chicago, Ill. ment, and nontraditional avenues for increased revenue. The latest research findings will be pre- NORTHEASTERN SOCIETY OF PLASTIC sented on mesh in abdominal wall reconstruction, SURGEONS ANNUAL MEETING injectable fat, and genital rejuvenation. For the The Annual Meeting of the Northeastern So- CME main program, 23 credits are available. Op- ciety of Plastic Surgeons will be held October 3 tional courses offer a total of 26 credits, with the through 7, 2007, in Bermuda. For more informa- maximum based on concurrent courses (total tion, contact the Northeastern Society of Plastic Sur- maximum available, 49 credits). Advance registra- geons, tel.: 1-603-643-2325. This meeting is spon- tion ends on September 21 by mail or fax and sored by the NESPS and the ASPS/PSEF. October 8 online. For the most current meeting information, visit www.plasticsurgery.org (Upcoming COMPLICATIONS OF CRANIOMAXILLOFACIAL Events); tel.: 1-800-766-4955/1-847-228-9900, ext. SURGERY AND FACIAL AESTHETIC SURGERY 471; e-mail: [email protected]. SYMPOSIUM The Complications of Craniomaxillofacial Surgery and Facial Aesthetic Surgery Symposium will be held October 26, 2007, in Baltimore, Md. The Plastic Surgery 2007 Annual Meeting kicks off with this comprehensive symposium featuring lec- tures on difficult complications and problems in craniomaxillofacial and aesthetic facial surgery. Emphasis will be on how to treat problems as they occur and how to avoid them initially. Each ASPS/PSEF SPONSORED SYMPOSIA speaker will present his/her most difficult “prob- AND WORKSHOPS lem” cases. This conference is not intended to The following meetings are either sponsored show how well a treatment went, but to discuss or co-sponsored by the American Society of Plastic problem cases. There are 8.5 category 1 CME cred- Surgeons and/or the Plastic Surgery Educational its, with one CME credit identified for patient Foundation and are current as of this printing. safety. The course is chaired by Kevin Kelly, M.D.,

www.PRSJournal.com 65e Plastic and Reconstructive Surgery • September 15, 2007

D.D.S., and Paul Manson, M.D., and commercial through 29, 2007, in Seattle, Wash. For more in- support is provided by KLS Martin and Merck. For formation, contact the ASSH, 1-847-384-8300. This more information, contact the ASPS/PSEF, tel.: course is sponsored by the ASSH. 1-800-766-4955. This course is sponsored by the ASPS/PSEF and the ASMS. VIth INTERNATIONAL COURSE: ADVANCES IN PLASTIC SURGERY ADMINISTRATIVE PLASTIC AND AESTHETIC SURGERY ASSOCIATION ANNUAL MEETING The VIth International Course: Advances in The Plastic Surgery Administrative Association Plastic and Aesthetic Surgery will be held October Annual Meeting will be held October 26 through 17 through 20, 2007, in Barcelona, Spain. The 29, 2007, in Baltimore, Md. For more information, course chairmen are Javier de Benito, M.D., and contact the PSAA, tel.: 1-800-373-0302. Thomas M. Biggs, M.D. The course coordinator is SURGICAL AND NONSURGICAL FACIAL Juan Aguiar, M.D. For more information, contact REJUVENATION SYMPOSIUM Miriam Cabrera, tel.: 34-933-635-760; fax: 34-934- The Surgical and Nonsurgical Facial Rejuve- 101-905; e-mail: [email protected]; Web nation Symposium will be held October 27, 2007, site: www.institutodebenito.com. in Baltimore, Md. This 1-day symposium will cover traditional and new procedures, with a special pre- sentation on the history of facial rejuvenation to AESTHETIC SURGERY OF THE AGING FACE complement the individual and panel presenta- The Aesthetic Surgery of the Aging Face tions. Attendees will learn about brow lifts and course will be held November 14 through 17, periorbital rejuvenation, clinical decision making 2007, at the Waldorf Astoria Hotel, in New York, specific to facial rejuvenation, neck contouring, N.Y. This course will cover all aspects of facial nonsurgical cosmetic treatments, and patient rejuvenation. The first day will be limited to fillers, safety issues. There are 6.5 category 1 CME credits injectables, and lasers. A full day of televised sur- available, with one credit identified for patient gery will be presented. The meeting will be safety. This meeting will be chaired by Alan Gold, chaired by Sherrell J. Aston, M.D., and co-chaired M.D., and Renato Saltz, M.D. For more informa- by Thomas D. Rees, M.D. This course offers CME tion, contact the ASPS, tel.: 1-800-766-4955. This category 1 accreditation. For more information, symposium is sponsored by the ASPS/PSEF and contact Francine Leinhardt, Course Coordinator, De- the ASAPS/ASERF. partment of Plastic Surgery, Manhattan Eye, Ear, and AMERICAN SOCIETY FOR PLASTIC SURGICAL Throat Hospital, 210 East 64th Street, New York, N.Y. NURSES ANNUAL MEETING 10021; tel.: (212) 702-7728; fax: (212) 832-9126; The American Society of Plastic Surgical e-mail: [email protected]. Nurses Annual Meeting will be held October 27 through 30, 2007, in Baltimore, Md. For more 4th BARCELONA MEETING ON PERFORATOR information, contact the ASPSN, tel.: 1-800-272- FLAPS: UPDATING AND NEW HORIZONS 0136. This course is sponsored by the ASPSN. The 4th Barcelona Meeting on Perforator ASSOCIATION OF PLASTIC SURGERY ASSISTANTS Flaps: Updating and New Horizons will be held ANNUAL MEETING November 29 through 30, 2007, in Barcelona, The Association of Plastic Surgery Assistants Spain. Organized by the Department of Plastic Annual Meeting will be held October 27 through Surgery, Hospital de la Santa Creu i Sant Pau, this 31, 2007, in Baltimore, Md. For more information, year’s program will include lymph vessel surgery, contact the APSA, tel.: 1-800-753-7244. This course new local perforator flaps, perforator flaps in aes- is sponsored by the APSA. thetic surgery (breast augmentation), refinements in breast reconstruction (how to improve final INTERNATIONAL MEETINGS results), and the latest advances in perforator map- AND SYMPOSIA ping (new imaging techniques). The meeting will include live surgery, video surgery, and round- AMERICAN SOCIETY FOR SURGERY OF THE table discussions conducted by an international HAND ANNUAL MEETING faculty. For more information, contact Joana The American Society for Surgery of the Hand Dalmau, tel.: (0034) 93 433 50 12; e-mail: joana. Annual Meeting will be held September 27 [email protected]; Web site: www.fdrobert.org.

66e Volume 120, Number 4 • Announcements

INTERNATIONAL SYMPOSIUM ON PLASTIC participants will have an opportunity to benefit from SURGERY the wisdom of their teachers. For more information, The International Symposium on Plastic Surgery contact Paolo G. Morselli, M.D., Plastic Surgery Unit, S. will be held June 25 through 28, 2008, in Bologna, Orsola-Malpighi Hospital, School of Plastic Surgry, Uni- Italy. This 20-year reunion of the 1988 symposium versity of Bologna, Via Massarenti, 9, Bologna 40138, will offer “veteran” participants the opportunity to Italy; fax: 0039 051 6363641; e-mail: paolo@ reflect on how their practice has changed, and new morselli.info.

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