Simultaneous Intraoperative Mohs Clearance and Reconstruction for Advanced Cutaneous Malignancies

ORIGINAL ARTICLE Simultaneous Intraoperative Mohs Clearance and Reconstruction for Advanced Cutaneous Malignancies

Rahul Seth, MD; Peter C. Revenaugh, MD; Allison T. Vidimos, MD; Joseph Scharpf, MD; Ally-Khan Somani, MD; Michael A. Fritz, MD

Background: Improved control of cutaneous malig- Results: Twenty-six patients underwent large cutane- nancies using Mohs micrographic pathologic clearance ous tumor resection using intraoperative Mohs micro- has been well established. However, surgical margin con- graphic surgery. Most lesions were basal (48%) or squa- trol of advanced and complex cutaneous tumors of the mous (34%) cell carcinoma. A mean (SD) of 2.1 (0.98) head and neck is commonly performed by far less reli- resection layers were required before negative margins able frozen section margin analysis. were achieved.

Objective: To describe a routine and ideal collaboration between dermatologic surgery and facial plastic surgery/ Conclusions: We demonstrate the intraoperative tech- head and neck surgery in which the Mohs micrographic nique and utility of Mohs micrographic analysis via an method is used intraoperatively to achieve marginal clear- efficient collaborative effort. Well established for accu- ance during resection and reconstruction. racy greater than intraoperative frozen section margin analysis, intraoperative Mohs micrographic surgery pro- Methods: A single-institution retrospective analysis was vides an optimal method of intraoperative margin as- performed of patients who underwent intraoperative Mohs sessment of cutaneous malignancies. micrographic surgery. Intraoperative margins (peripheral and deep) of tissue specimens were analyzed by the Mohs surgeon. Arch Facial Plast Surg. 2011;13(6):404-410

KIN CANCER IS THE MOST COM- the operating suite using general anesthe- mon malignancy in the sia along with extensive reconstructive United States. Most of these measures. In these cases, conventional ex- are nonmelanoma skin can- cision is typically performed using gross cer, with basal cell carci- margin assessment and intraoperative fro- noma (BCC) accounting for 75% and squa- zen section analysis.5,6 In these situa- S 1 mous cell carcinoma composing 20%. tions, MMS is not commonly used de- After appropriate diagnosis, treatment of spite established increased accuracy in these lesions is typically performed by sur- margin assessment and superior tumor gical excision. Mohs micrographic sur- control.3,4,7 Given the limitations of con- gery (MMS) and conventional excision ventional margin clearance, definitive re- with margin assessment by postoperative construction of defects is often withheld permanent or intraoperative frozen sec- to observe for recurrence, resulting in ad- tion histopathologic analysis are the most ditional patient morbidity and psychoso- commonly performed excision tech- cial detriment. niques.2 Mohs micrographic surgery has Compared with permanent pathologic demonstrated advantages over other meth- analysis, frozen section analysis of the same ods of resection by providing improved tissue sample has an accuracy of 72% for margin control. Typically, MMS is used in assessing BCC.7 Accuracy is further lim- the outpatient setting for small- and me- ited by surgeon and pathologist selection Author Affiliations: Head and dium-sized tumors of the head and neck error if a complete circumferential resec- Neck Institute (Drs Seth, (Ͻ5 cm).3,4 tion margin cannot be assessed. An esti- Revenaugh, Scharpf, and Fritz) Ͼ and Dermatologic Institute Large or so-called giant tumors ( 5 mated less than 1% of the specimen’s (Drs Vidimos and Somani), cm), aggressive pathologic features, and sections are typically assessed by a patholo- Cleveland Clinic, Cleveland, involvement of multiple aesthetic units or gist.3,4 The MMS technique, in contrast, al- Ohio. critical structures may warrant excision in lows for assessment of 100% of the ex-

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©2011 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/29/2021 A Surgical excision with Only selected en face frozen frozen sections sections of peripheral and deep margin examined (sampling error leads to missed tumor) Permanent sections

True Negative A B False Negative C True Positive D False Negative E True Positive

<2% of specimen examined in standard vertical sections

Identified tumor tracked and removed using IMMS until all margins clear

Mohs micrographic sections

100% of peripheral and deep B margin examined and mapped Surgical excision with using frozen horizontal sections Mohs sections

Figure 1. The Mohs technique compared with frozen section method. A, Margin assessment by permanent and frozen section analysis assesses a small fraction of the tumor margins, leading to significant sampling error, resulting in potentially incomplete tumor resection and a lack of confidence when assessed margins are deemed to be negative. B, Frozen Mohs section analysis can assess the entire peripheral and deep surgical margin, leading to greater certainty of complete tumor resection. IMMS indicates intraoperative Mohs micrographic surgery.

cised tumor margin. Thus, MMS leads to more complete vant therapies, recurrence, survival, and follow-up data were tumor clearance and improved cure rates. Established collected and assessed. Continuous variables are presented as 5-year cure rates are shown to be up to 98.9% for primary mean (SD). and recurrent BCC and squamous cell carcinoma.8-11 As a result, MMS has been established as the crite- OPERATIVE PROCEDURE rion standard for excision of higher-risk cutaneous ma- AND TISSUE ANALYSIS lignancies.12-14 These malignancies include tumors that are recurrent, are located in areas typically at high risk General anesthesia was used in all cases, and initial tumor re- for recurrence (midface, ears, lips, and embryonic fu- section margins were jointly planned by the surgical teams. Un- sion planes), are larger than 2 cm, have ill-defined bound- like the traditional MMS technique, resection was performed aries, or have aggressive pathologic findings.2 with the intent of aggressive peripheral and deep margin clear- To achieve margin clearance greater than that pro- ance (ie, “wide-margin Mohs” that is not tissue sparing). This vided by conventional resection techniques in the man- method ideally provides margin clearance in the first 1 or 2 resection layers. Tumor mapping was performed by the Mohs mi- agement of large, complex cutaneous malignancies, we crographic surgeon, while the ablative surgeon performed the used a novel collaborative approach of intraoperative MMS initial resection. Once complete, the specimen was taken to the (IMMS) involving multiple subspecialties at Cleveland Mohs histology laboratory, where complete margin analysis was Clinic, Cleveland, Ohio (Figure 1). This method al- performed using the MMS technique by a dedicated Mohs team lows for optimal oncologic resection and immediate consisting of several technicians and Mohs surgeons. Because aesthetic and functional reconstruction of complex the Cleveland Clinic Mohs team has made resource and time defects. accommodations to enable rapid readings, large specimen reads were performed within 1 to 3 hours. Margins of particular con- cern were identified and read as a high priority to expedite fi- METHODS nal clearance. Tissues that were assessed by the Mohs technique included skin and deep tissues, muscle, fat, mucosa, A retrospective analysis was performed of patients between Sep- cartilage, and periosteum. Major nerve margins (eg, facial nerve) tember 1, 2007, and June 1, 2010, who underwent resection were assessed using frozen section by the surgical pathologist. of cutaneous head and neck malignancy using IMMS by the col- During margin analysis, additional required extirpative proce- laborative effort of Mohs dermatologic, head and neck, and fa- dures, such as maxillectomy, neck dissection, and parotidec- cial plastic surgeons. The Cleveland Clinic institutional re- tomy, were performed by the head and neck surgeon. Recon- view board approved this study. Demographic details, tumor structive efforts, including the raising of local, regional, or free abnormalities and characteristics, surgical procedures, adju- tissue flaps and acquisition of cartilage or bone grafts, were also

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D E F

Figure 2. Case 1. Wide resection margins are demarcated by the ablative surgeons (A), with intraoperative tumor mapping performed by the Mohs surgeon (B). C, Subtotal rhinectomy, left medial maxillectomy, and left infraorbital nerve excision were performed. D, The harvested anterolateral thigh fascia was used to re-create the nasal lining, and the fat component was used to reconstitute the cheek contour. E, Cervicofacial, paramedian, and nasolabial flaps were used to provide defect skin coverage. F, The patient is without recurrence 2 years after surgery and maintains an optimized cosmetic and functional reconstruction. Adapted from Dermatol Clin. 2011;29(2):319-324.

commenced during this period if they were not dependent on Case 2 the final margins. Specific areas of positive margins were marked on the mi- A 53-year-old woman presented with a large recurrent BCC in- crographic map, and the Mohs surgeon returned to the oper- volving the right side of the midface, nasal sidewall, and mu- ating suite to discuss directly these areas needing further re- cosal surface of the lateral nasal wall (Figure 3). Intraopera- section. Additional serial resection layers with immediate Mohs tive MMS was performed requiring a subtotal rhinectomy, medial interpretation were performed in a similar manner until nega- maxillectomy, and infraorbital nerve resection for perineural tive margins were achieved. Same-setting complete reconstruc- invasion. Four layers were required to clear the tumor from soft tion was performed immediately after verifying tumor clear- tissues. During margin assessment, a cervicofacial flap was el- ance. The following 3 cases illustrate the method of IMMS. evated, cartilage grafts were harvested, and eyelid reconstruction was performed. After negative margins were obtained from REPORT OF CASES all the resection surfaces, paramedian forehead and septal flaps were used to reconstruct the nose. Case 1

A 59-year-old woman presented with a multiply recurrent BCC Case 3 that initially involved the left nasofacial sulcus. The patient was previously treated and had recurrence after multiple excisions A 71-year-old woman presented with a large neglected BCC in- and radiotherapy. The extensive recurrence involved the left volving the right hemiface (Figure 4). She required an exten- nasofacial sulcus, nasal ala, dorsum, cheek, and lateral nasal sive soft-tissue resection, orbital exenteration, subtotal rhinec- wall mucosal surface (Figure 2). She underwent IMMS ne- tomy, and partial maxillectomy. The tumor was cleared in 2 cessitating a subtotal rhinectomy, left medial maxillectomy, and layers using IMMS. Although grossly appearing clear of tu- left infraorbital nerve excision. One layer was required to ob- mor, the first layer was approximately 75% positive, and a fur- tain negative margins. During margin assessment, a free an- ther 1-cm circumferential excision was required to obtain clear terolateral thigh fat/facial flap was harvested, and a cervicofa- margins on all edges. Reconstruction was initiated during mar- cial flap was elevated. Once margins were confirmed, gin assessment and included a free latissimus dorsi flap with reconstruction was performed. split-thickness skin graft and cervicofacial advancement flap.

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C D E

Figure 3. Case 2. A and B, A wide resection was performed to resect a multiply recurrent basal cell carcinoma lesion, with 4 Mohs layers required to clear the tumor. Subtotal rhinectomy, medial maxillectomy, and infraorbital nerve resection were performed. C, Cervicofacial and paramedian flaps were performed. D, Postoperative radiotherapy was performed, and a considerable right cheek contour defect was apparent. E, In a delayed manner, a buried adipofascial anterolateral thigh flap was inset to re-create facial contour and symmetry. The patient is disease free 2 years postoperatively. Adapted from Dermatol Clin. 2011;29(2):319-324.

RESULTS In 3 cases (12%), the deep layer of the resection was bone, allowing IMMS assessment of only the peripheral margins. These cases required analysis of bony deep mar- Intraoperative MMS was used in 26 patients during the gins by the surgical pathologist. study (Table 1). The mean (SD) patient age was 68.7 Immediate reconstruction was performed on all de- (12.2) years. Lesions were most commonly BCC (48%) fects, with 8 of 29 lesions (28%) undergoing free flap re- or squamous cell carcinoma (34%). Intraoperative MMS construction. Three patients (12%) required postopera- was used for similar pathologic conditions for which MMS tive radiation therapy. Indications for radiation therapy would be indicated. One patient had Gorlin basal cell ne- in these patients were recurrence, regional nodal metas- vus syndrome, and 4 (15%) had a history of solid organ tasis, and extensive infraorbital nerve involvement. Mean transplantation. Four patients (15%) had undergone pre- follow-up was 17.1 months (range, 2.8-40.9 months). vious radiotherapy. The mean resection area of tumors Twenty-one patients (81%) remain alive, and 4 (15%) was large at 60.9 cm2. Most malignancies were recur- have experienced recurrence. Of the 5 patient deaths, 3 rent (73%), and many displayed perineural invasion were of unrelated causes and due to other medical co- (38%). The nose and central face was the most fre- morbidities and 2 were due to recurrent disease. Two re- quently involved anatomical area (41%), followed by the currences occurred at the orbital apex and cavernous si- parotid and temple (28%). nus, 1 at the resection margin, and 1 patient developed Owing to aggressive initial resection, the mean (SD) nodal metastasis. number of layers required to achieve negative margins was 2.1 (0.98) (Table 2). Tumor clearance was achieved in the first resected layer in 7 cases. A maximum of 5 lay- COMMENT ers was required in 5 cases. The mean time required for Mohs micrographic margin assessment was 93.9 min- Mohs micrographic surgery is a well-established and pre- utes (range, 25-190 minutes) for the first layer, 54.5 min- ferred technique for excising cutaneous lesions, particu- utes (range, 25-130 minutes) for the second layer, and larly BCC and squamous cell carcinoma, and is associ- 41.1 minutes (range, 25-59 minutes) for the third layer. ated with high cure rates.11 Recent literature has shown If a fourth or fifth layer was needed, these required a mean the absolute accuracy of frozen section analysis in recur- of 29.7 and 38.5 minutes, respectively. rent or facial cutaneous BCC to be as low as 72%.7 This

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D E F

Figure 4. Case 3. A and B, A large neglected basal cell carcinoma involving the right upper hemiface. C, The patient required an extensive soft-tissue resection, orbital exenteration, subtotal rhinectomy, and partial maxillectomy. D-F, Reconstruction was performed after intraoperative Mohs micrographic surgery revealed full soft-tissue tumor clearance. A free latissimus myogenous flap with a split-thickness skin graft and a cervicofacial advancement flap were used. Adapted from Dermatol Clin. 2011;29(2):319-324.

difference highlights the important role that MMS may nancies. Despite the established advantages of Mohs clear- play in the operating room. Typically, MMS is per- ance, the potential for prolonged operative time due to formed on small- and medium-sized tumors in the out- large specimen reads19 and the requirement for addi- patient setting under local anesthetic. The Mohs micro- tional personnel and resource coordination have likely graphic surgeon serially removes and assesses margin hindered the development and acceptance of IMMS. We layers until a completely negative margin is reached. Be- demonstrate that these limitations can be overcome with cause the entire peripheral and deep margin is histo- an organized and routine collaborative approach to IMMS. pathologically assessed, the potential for complete tu- With dedicated efforts and resources, the Mohs mi- mor removal is higher than with traditional excision crographic surgeon can quickly read margins and direct methods, where only a small fraction of the margin may further margin resection as needed to optimize com- be examined.7-9 Transferring MMS to the operating suite plete resection. In this study, the mean read times for the for resection of large cutaneous tumors provides for more first and second resection layers were 93.9 and 54.5 min- reliable margin clearance and, thus, may improve onco- utes, respectively. During this time, the facial plastic/ logic outcomes. In addition, increased confidence in mar- head and neck surgeon can perform additional required gin control allows for simultaneous reconstruction with- extirpation, such as neck dissection, parotidectomy, and out the need for long-term defect monitoring for local maxillectomy, or initiate reconstructive efforts. recurrence. In the authors’ experience, there are minimal or no The use of IMMS for large head and neck cutaneous intraoperative delays or case time prolongation due to neoplasms using general anesthesia was first described pending Mohs histopathologic assessment. This is mainly by Levine et al15 at Cleveland Clinic in 1979. Soon there- due to 2 factors. First, appropriate advanced tumors are after in the 1980s, Baker et al16,17 similarly reported a small selected for this method. These tumors are not ame- case series using this advantageous combined-modality nable to resection under local anesthetic, and they often approach. These initial studies demonstrated the utility require complex reconstruction or ancillary extirpative of IMMS. A recent publication by Ducic et al18 demon- procedures, which are performed during ongoing mar- strates use of a “ring of Mohs” to assess the circumfer- gin interpretation. Second, a dedicated and highly effi- ential (but not deep) tissues by MMS. cient Mohs dermatologic team is used. Typically, 2 tech- To our knowledge, no studies have demonstrated regu- nical teams are reserved to allow for rapid tissue processing lar use of this technique for advanced cutaneous malig- and assessment.

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All Patients Variable Value Characteristic (N=26) Resection details Demographics Lesions, total No. 29 Age, mean (SD), y 68.7 (12.2) Layers to clear disease, mean (SD), No. 2.1 (0.98) Male sex, No. (%) 14 (54) Mohs micrographic assessment time, White race, No. (%) 25 (96) mean (SD) [range], min Pathologic condition, No. (%) All Lesions (n=29) Time to clear first layer 93.9 (47.4) [25-190] Basal cell carcinoma 14 (48) Time to clear second layer 54.5 (29.4) [25-130] Squamous cell carcinoma 10 (34) Time to clear third layer 41.1 (11.5) [25-59] Trichoblastic carcinoma 1 (3) Additional therapies performed, No. (%) Dermatofibrosarcoma 1 (3) Reconstruction performed 26 (100) Tumor characteristics Free flap reconstruction 8 (28) Area of resection per lesion, mean, cm2 60.9 Postoperative radiation therapy 3 (12) Perineural invasion, No. (%) 12 (41) Follow-up Presented with recurrent lesion, No. (%) 19 (66) Follow-up, mean (SD), mo 17.1 (10.1) Syndrome predisposing to cutaneous 1 (3) Alive, No. (%) 21 (81) malignancy, No. (%) Recurrence, No. (%) 4 (15) Transplant history, No. (%) 4 (14) Died of disease, No. (%) 2 (8) Indications for intraoperative Mohs, No. (%) Large/extensive lesion 26 (100) Recurrent lesion 19 (73) Nerve involvement 10 (38) Anatomical involvement, No. (%) tive margins (reversed from frozen section assessment) Nasal/central face 12 (41) or “close” margins on final pathologic analysis. Using Temple/parotid 8 (28) IMMS, improved effectiveness of and confidence in mar- Auricular/mastoid 3 (10) gin clearance has led to less frequent requirements for Scalp 3 (10) adjunctive radiation therapy. Forehead 1 (3) A limitation of this study is its short follow-up. How- Cheek 1 (3) ever, preliminary findings are promising that this technique is beneficial. This method is feasible, may improve patient care and outcomes, and is easily adoptable into prac- In this series, cutaneous malignancies that were treated tice by collaborative efforts at most institutions. using IMMS were large (mean, 60.9 cm2) and most of- In conclusion, in the management of cutaneous ma- ten involved the central face/nose (41%) and temple/ lignancies, Mohs margin assessment has clearly estab- parotid (28%). These lesions were also often recurrent lished advantages over traditional frozen or permanent sec- (73%) and involved nerve (38%). Reconstructive efforts tion pathologic reads. We described a routine collaborative were undertaken in 100% of patients in the same setting approach that allows for the use of this technique for tu- as resection, with 28% of patients undergoing free tis- mor clearance of advanced malignancies that necessitate sue transfer. resection under general anesthesia. This method may pro- In many intraoperative instances, Mohs micro- vide improved tumor control and optimal coordination of graphic evaluation revealed positive margins in areas that cancer extirpation and reconstruction. were not clinically suspected to have residual disease. If frozen section assessment had been used instead of IMMS, Accepted for Publication: April 29, 2011. these areas may not have been sampled or adequately as- Correspondence: Michael A. Fritz, MD, Head and Neck sessed by either the surgeon or the pathologist, creating Institute, Department of Otolaryngology–Head and Neck a false-negative sampling error. Surgery, Cleveland Clinic, 9500 Euclid Ave, Desk A71, Because follow-up in this study was relatively short, Cleveland, OH 44195 ([email protected]). only limited conclusions can be made regarding recur- Author Contributions: Study concept and design: Seth, rence and survival. However, the Mohs micrographic tech- Vidimos, Scharpf, and Fritz. Acquisition of data: Seth, nique is the best possible method of nonmelanoma skin Revenaugh, Vidimos, and Fritz. Analysis and interpreta- cancer tumor clearance, and a complete resection may tion of data: Seth, Revenaugh, Vidimos, Scharpf, Somani, decrease the high recurrence rates inherent to large non- and Fritz. Drafting of the manuscript: Seth and Fritz. Criti- melanoma skin cancer.2,8 Of the 4 recurrences in this se- cal revision of the manuscript for important intellectual ries, only 1 occurred locally at the resection margins; the content: Seth, Revenaugh, Vidimos, Scharpf, Somani, and remaining occurred regionally in the neck or at the or- Fritz. Statistical analysis: Seth and Vidimos. Administra- bital apex and cavernous sinus, presumably via perineu- tive, technical, and material support: Seth, Revenaugh, ral tracking. Vidimos, Scharpf, Somani, and Fritz. Study supervision: Postoperative radiation therapy was used in only 3 pa- Vidimos, Scharpf, and Fritz. tients (12%), which is considerably low given the ex- Financial Disclosure: None reported. tent of these large, aggressive lesions. In our experience, Previous Presentation: This study was presented at the before initiating IMMS, many indications for postopera- International Symposium on Facial Plastic Surgery; April tive irradiation in this patient population were for posi- 28, 2010; Hollywood, Florida.

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