Chest wall perforator flaps in partial breast reconstruction after breast conservation : an additional oncoplastic surgical option

Sanjit Kumar Agrawal1, Sudip Ratna Shakya1, Shashank Nigam1, Abhishek Sharma1, Soumitra S Datta2,3 and Rosina Ahmed1

1Department of Breast Oncosurgery, Tata Medical Center, Kolkata 700156, India 2Department of Palliative Care and Psycho-Oncology, Tata Medical Center, Kolkata 700156, India 3MRC Clinical Trials Unit, Institute of Clinical Trials & Methodology, University College London, WC1V 6LJ, United Kingdom

Abstract

Partial breast reconstruction using chest wall perforator flaps (CWPF) is a recent option used by breast surgeons, mainly for lateral quadrant defects with a relatively large volume of excision. We report a single-centre experience of CWPF with surgery details, compli- cations, re-excision, aesthetic and oncological outcomes. This was a prospective observational cohort study of patients who had undergone breast conservation surgery (BCS) plus CWPF reconstruction. All variables were recorded pro- spectively in the institutional database. A survey was done to analyse patient satisfaction

at about 6 months after completion of radiotherapy. Clinical Study Forty patients had CWPF based reconstruction in 3 years. 57.5 % of patients had lateral intercostal artery perforator (LICAP) flap, 5% had lateral thoracic artery perforator (LTAP) flap, 27.5% had combined LICAP plus LTAP and 10% patients had anterior intercostal artery perforator (AICAP) flap. Tumour excision cavity defect was of the lateral quadrant in 82.5%, central quadrant in 10% and medial quadrant in 7.5% of patients. The margin was positive for five patients, out of which four required cavity shave and one had a mastec- tomy. One patient had complete flap loss, and two patients developed surgical site infec- tion. 96% of patients were satisfied with the scar, and 88% were happy with the treated breast in comparison to the opposite breast. 92% were comfortable going out in public Correspondence to: Sanjit Kumar Agrawal and felt that in retrospect their decision not to have a mastectomy was correct. With a Email: [email protected] median follow up of 18 (10, 22) months, one patient died, and four had recurrences. ecancer 2020, 14:1073 CWPF may be used for partial breast reconstruction in the small non-ptotic breast with https://doi.org/10.3332/ecancer.2020.1073 excellent outcome and high patient satisfaction scores. Published: 16/07/2020 Received: 05/04/2020 Keywords: breast , oncoplastic breast surgery, chest wall perforator flap Publication costs for this article were supported by ecancer (UK Charity number 1176307). Copyright: © the authors; licensee ecancermedicalscience. This is an Open Access Background article distributed under the terms of the Creative Commons Attribution License (http:// creativecommons.org/licenses/by/3.0), which Breast conservation surgery (BCS) with whole-breast irradiation is well established in the permits unrestricted use, distribution, and management of early breast cancer. It is equivalent to mastectomy in terms of survival reproduction in any medium, provided the original and local control, with the added advantage of achieving an excellent cosmetic outcome, work is properly cited.

ecancer 2020, 14:1073; www.ecancer.org; DOI: https://doi.org/10.3332/ecancer.2020.1073 1 complications, cosmesis andpatient satisfaction. this study, we share our experience the useofwith CWPF breast reconstruction following BCS, with regards to details of surgical procedure, moderate-sized breasts largewith defects. The outcomeof CWPF-based breast reconstruction inthe Asian woman ismostly unknown. In BCS CWPFwith reconstruction was started at Tata Medical Center in2017andisincreasingly beingoffered to patients small-to-with cosmetic outcomes andbetter patient satisfaction authors have reported thatbenefits, besidesfunctional CWPFs have theaddedadvantage of minimaldonor site morbidity excellentwith scar that itcreates,mostly but thisscar gets hiddeninthebra line.However, patient satisfaction thescarwith needsto beassessed.Recently, for mastectomy orharvestflap LD inaselected groupof patients who wish to undergo BCS.CWPF isoften criticisedfor thelongchest wall excellentopportunity forbreast partial reconstruction in women small-to-moderate-sizewith non-ptotic breast andmay prevent theneed thoracicartery perforator (LTAP)as anadditionaloption flap for thereconstruction of partialbreast defects [8]. These techniques offer an tor (ICAP)flaps. They showed thesafety andfeasibility of CWPF inbreast reconstruction. In 2014,McCulley et al[8]introduced thelateral In 2005,Hamdi et al[6,7]reported theuseof CWPF intheform of thoracodorsal artery perforator (TDAP) andintercostal artery perfora- this particular scenario (small to medium-sized breasts, with thelarge tumours). tional impairment of theshoulder [5].Chest wall perforator(CWPF)-based flap reconstruction hasrecently emerged asa valuable option in (LD) myocutaneous/mini LDflaps were usedto cover large defects insmall breasts thedisadvantagewith of donor site morbidity andfunc surgeons) that choosesthereconstructionoptions basedontheexperience, tumour to breast size ratio etc. For many years, Latissimus Dorsi consensus on techniquewhich OBS shouldbeusedfor any given situation, anditisusually thetumour board (includingbreast andplastic Incases, someforms such of oncoplastic volume replacement techniques are required to achieve breast symmetry. At present, there isno For patients small towith moderate-sized breasts andlarge tumours, theremoval of themassalonemay leave anunacceptably large defect. oncological safety [4]. surgicalmethods has increaseddecade last inthe ratesBCS the globally andenabledimproved cosmetic outcomes compromisingwithout and many new surgical techniques have emerged and evolved to facilitate partialbreast reconstruction. The development of oncoplastic high patientsatisfaction and improved quality of lifeage inallthe groups [1–3].Oncoplastic breast surgery (OBS) addsto cosmetic outcomes, ecancer 2020, 14:1073; www.ecancer.org; DOI:https://doi.org/10.3332/ecancer.2020.1073 therapy, usinga4-point Likert’s scale. The survey was administered either telephonically or duringaroutine follow-up visit. Patient permis- An acquired-informal questionnaire was developed andusedto assesspatient satisfaction at least6months after completion the of radio- as per institutionalMDT decisions. surgical histopathology specimen reporthad asubsequent cavity excision to ensure clear margins. All patients received adjuvant treatment considered asanegative margin for invasive cancerfor and2mm pure carcinoma ductal insitu(DCIS). All patients with positive margins on of flap vascularisation was confirmed with an infrared enabled ICG probe. Following protocols,institutional no ink on the tumour margin was an episodeof completeloss, flap we have started theuseof intra-operative flapmonitoring usingindocyanine green (ICG) dye. The adequacy patency andposition. The flap was rotated ontheperforators to fillthebreast defect, makingsure not to or twist kinktheperforators. After lateralthe todirection, medial and perforators were identifiedand preserved. Intraoperative Doppler USG was usedto confirm perforator In themajority of cases, local excisionwide was alsodonethroughincision. theplannedflap After wide localexcision, theflap was raised in on thetumour sizeestimated andthe locationof defect. the The axillary staging was doneusingthesameincisionplannedfor raising theflap. wall perforators were markeda handheldDopplerskin using onthe ultrasound probe. Flaps were marked to includetheperforators, based the surgery inthestandingposition. The breast bandsize size andcup were measured preoperatively andrecorded inthedatabase. Chest For allpatients,tumour excisionand CWPF reconstruction were doneatthe sametimeasasingleprocedure. All patients were marked before prospectively maintained REDCapdatabase. characteristics, surgical details, adjuvant treatment and follow-up were retrieved from managementthe hospital institutional system, and a Medical Center, Kolkata, India werein thisstudy included (ethicscommittee waiver No: EC/WV/TMC/014/19). Data onclinicopathological All women underwentwho breastand partial BCS reconstruction with CWPF for breast cancer from January 2017to November 2019at Tata Methods [6–8]. 2 -

Clinical Study ecancer 2020, 14:1073; www.ecancer.org; DOI:https://doi.org/10.3332/ecancer.2020.1073 (Figure 1—superolateral quadrant tumour excision with LICAP flap). our seriestoo, theLICAP flap wasfrequently, usedmost in23patients, allof whom hadtumours located inthelateral quadrant of thebreast 3.5 cmmedialto theanterior border ofmuscle theLD ing from theintercostal segment of theintercostal vessels, arewhich commonly found inthe5thto 7thintercostal spaces between 2.5and Hamdi upper inner quadrant. CWPFs could beusedfor tumours located inany quadrant of thebreast althoughthey were mostfrequently usedlaterally, andrarely inthe in theliterature, including TDAP, LTAP, LICAP and AICAP [6–9]. Apart from TDAP, allof theseflaps were usedinour series. We found that goodwith patient-reported aestheticoutcomes morbidity. andminimal Various CWPFs usedinpartialbreast reconstruction are reported This study showed thatCWPFs offer anexcellentoption for breast partial reconstruction in women with smallandmedium-sized breasts, Discussion and medianBMI was 25.46kg/m patientshad upfront surgery patients and8(20%) had surgery postneoadjuvant chemotherapy. The medianage was 44 years (IQR39,48), Between January 2017andNovember 2019,40patients underwent CWPF for partialbreast reconstruction. Out of the40cases,32(80%) Results percentage) was usedfor thedata analysis usingSPSS23. sion was obtained for anonymised useof photographs asper protocols. institutional Summary statistics (median, interquartile range and places andfelt that inretrospect their decisionnot to have amastectomy was correct (Table 2). the scar,with and88% were happy the treatedwith breast incomparison to theopposite breast. 92% were comfortable going inpublic out Of 35patients who were at least6months post-radiotherapy, 25(71%)responded to thefollow-upsurvey questionnaire. 96% were satisfied a patient who diedof sepsisfollowing her sixthcycle of chemotherapy. There were nolocalrecurrences. one hadanaxillary recurrence (post-sentinelnode biopsy) lymph andone was to lost follow up. There was only onemortality intheseries, Thirty eight patients are under regular follow up. At amedianfollowof up 18months, four patients haddeveloped distant metastatic , shave andoneunderwentcompletion mastectomy of because extensive DCISandpatient choice. Seroma was not reported inany patient. surgical site infections (SSI) which were managed conservatively. Five (12.8%)patients hadpositive margins, of out which four required cavity One patient had totalloss, flap which was managed by debridement, andthedefect was covered flap. aminiLD with Two patients developed histopathological characters are summarisedin with nipple-areola excision, which was reconstructed by using LICAP in two patients and LICAP plus LTAP in onepatient. Surgical details and structed by LICAP/LTAPor flap combinationof two,quadrant andmedial defects (4/40)by AICAP flap. Three patients hadalateral tumour (10%) and2(5%)patients, respectively. 11(27.5%)patients hadcombined LTAP andLICAP. Lateral quadrant defects (33/40) were recon - Lateral intercostal artery perforatoranterior (LICAP), intercostal artery perforator (AICAP)andLTAP flap were performed in23(57.5%),4 Median breast bandsize was 34(IQR32,36),andthemajority of patients hadbreasts of (30%)or B size. C(52.5%)cup 16,25). All patients were discharged 24 hourswithin following thesurgical procedure. The medianfollow-up was 18(IQR10,22) months. [7, 9]reportedfirst the use of LICAP and AICAPin partialbreast flaps reconstruction. The LICAPis basedonperforators flap originat - 2 (IQR 22.97, 27.70). (IQR The median waiting timefrom diagnosisto surgery for upfront cases was 18days (IQR Table 1. [10]. The LICAP for flapismostsuitable defects inthelateral quadrant of thebreast. In 3

Clinical Study ecancer 2020, 14:1073; www.ecancer.org; DOI:https://doi.org/10.3332/ecancer.2020.1073 Table 1.Surgical andhistopathological details. Triple-negative HER 2enriched Luminal B Luminal A Tumour subtype III II I TNM stage Nx N3 N2 N1 N0 N stage T3 T2 T1 T stage 3 2 1 Tumour Grade Infiltrating mucinouscarcinoma Infiltrating ductalcarcinoma Type of carcinoma Operation time(min) Specimen(grams)weight Fully de-epithelialised Including skin Flap positioning Width (cm) Length (cm) Flap dimension Width (cm) Length (cm) Pathological tumour size Central Inferomedial Inferolateral Superomedial Superolateral Tumour location None Axillary lymphnodedissection(ALND) Sentinel lymphnodedissection(SLND) Axillary surgery N (%)/Median (IQR) 14.0 (12.0-15.0) 180 (144,190) 120 (109,157) 1.8 (1.5,2.0) 2.6 (2.0,3.0) 8.0 (7.0-9.0) 29 (72.5%) 25 (62.5%) 17 (42.5%) 13 (32.5%) 25 (62.5%) 13 (32.5%) 37 (92.5%) 21 (52.5%) 19 (47.5%) 29 (72.5%) 9 (22.5%) 7 (17.5%) 10 (25%) 24 (60%) 20 (50%) 14 (35%) 3 (7.5%) 1 (2.5%) 1 (2.5%) 3 (7.5%) 3 (7.5%) 3 (7.5%) 3 (7.5%) 1 (2.5%) 6 (15%) 8 (20%) 8 (20%) 4 (10%) 2 (5%) 2 (5%) 4

Clinical Study ecancer 2020, 14:1073; www.ecancer.org; DOI:https://doi.org/10.3332/ecancer.2020.1073 lateral perforators; E,F. Post operative pictures Figure 1. A.B. Preoperative markingandlocalization of perforators for LICAP;C,D. Thetumour was excised andtheflap was completely isolated onone Table 2.Patient satisfaction assessment. opted for amastectomy? Do you feel, inretrospect, that you shouldhave How comfortable are you going outinpublic? parison to theopposite breast? How happy are you with your treated breast incom- How satisfied are you with your scar? Highly unsatisfied 0 (0%) 0 (0%) 0 (0%) 0 (0%) Unsatisfied 3(12%) 2 (8%) 2 (8%) 1 (4%) 12 (48%) 15 (60%) Satisfied 9 (39%) 2 (8%) Highly satisfied 19 (84%) 11 (44%) 13 (52%) 9 (36%) 5

Clinical Study almost half thepatients was DCIS, with theremainder having invasive cancer. following thechanges intheSSO/ASTRO guidelines.In thisstudy, theauthors found that thediseasepresent at themargin of excision in positive margins, four were involved byand oneby DCIS theinvasive tumour. Rosenberger et al[15]recently reported their early experience dardise anegative margin afteras having BCS ‘noinkon tumour’ inpatients with invasive cancer [11].In our series,of thefive cases with We followSociety the of Surgical Oncology (SSO) and AmericanSociety for Radiation Oncology (ASTRO) consensus guidelines, which stan - to other studies, which have reported positive margins of inabout10% cases(Table 3). cosmeticoutcome andmay compromisepatient satisfaction.In our series,themargin was positive infive (12.5%)patients. This iscomparable One of the significant challenges in the useof CWPF is reoperation for positive margins. Reoperation may have an adverse effect on the to margin positivity or flaploss. intactthe with thoracodorsal givesit pedicle, surgeons anadditionaloption oftoflap cover LD thedefects insituations of reoperation due patients (Figure—Retroareolar 3 massexcision combinedwith LTAP plusLICAP flap). As theseperforators are basedontheintercostal vessels to the skinpaddle.In our series,LTAP flap was usedsolely for 2(5%),andacombination of LTAP with LICAP flap was usedin11 (27.5%) pared toLICAP the flap. The LTAPeitherbe used can flap aloneasthemainpedicle,or incombination with theLICAP, augmenting perfusion suitable for defects in the lateralof aspect the breast, and it canbe partly or wholly mobilised to allow greater reach and transposition com- thoracic vessels. LTAP perforators are found inthe3rd and 4thintercostal spaces within 2 cm of thelateral breast crease. The LTAP flapis The LTAP flap for partial breast reconstruction was first described McCulley fill defects intheinferomedial quadrant (Figure 2 —Inferomedial quadrant tumour excision with AICAP flap). lateral1–3 cm tosternal the border [9]. Theforis suitable flap defects inthemedialaspectof thebreast. In our series,it was mainly usedto The AICAP flapis based on perforators originating from themuscular or rectal segment of theintercostal vessels, which are located within anterior intercostal perforators; E.Immediate Post operative picture; F. On follow up. Figure 2. A,B. Preoperative markingandlocalization of perforators for AICAP;C,D. Thetumour was excised andtheflap was completely isolated on ecancer 2020, 14:1073; www.ecancer.org; DOI:https://doi.org/10.3332/ecancer.2020.1073 [8] and is based on single or perforatorsmultiple of the lateral 6

Clinical Study ecancer 2020, 14:1073; www.ecancer.org; DOI:https://doi.org/10.3332/ecancer.2020.1073 fluorescent dye). The additionalcost of ICG useinour set up was 20 USD only per patient, which was <1%of total surgery expense. techniquein cases perforatorssmall with to evaluate the vascularity ofintraoperatively flap (Figure 3—Flap vascularity assessment using 19]. After oneof our patientsnecrosis,had flap we started toperfusion routinely, assessflap usingICG. We especially found itauseful shown that intraoperativeofmapping perfusion flaps with ICG can predict and prevent complications in breast reconstructive surgery fluorescent angiography is a useful techniquefor theassessment of bloodflow inskinflaps[17].Several andtissueperfusion studieshave Flap related complications may have anadverse effecton cosmetic outcomes andare reportedto inup 5%–10%of cases.ICG dye-based generally not well accepted by patients.In our series,allpatients were offered excision andCWPF reconstruction asasingle-stage procedure. margins. However, intheresource-constrained country, patients are often reluctant to have , multiple andtwo-stage procedures are an axillary procedure as indicated, followed by reconstructive surgery within 2–3 weeks once final histopathology has confirmed negative thattwo-stage the method hadexcellentoutcomes high patientwith satisfaction. The two-stage process involves initiallumpectomy with Another way to avoid the consequences of positive margins is to perform the procedure as a 2-stage approach. Roy although itisavailable for useif required. In thisseries,thefrozen section was not requested for any of thepatients. a previously negative margin reportedfrozen onthe In section. our thefrozen institution, sectionisnot usedroutinely for margin assessment had frozen section to confirm excision margins, but final histopathology reports showed positive margins in 5.5% of these patients inspite of margins reported onthefinalhistopathological report.In astudy by Munhoz etal is time-consumingsection and doesnot guarantee complete excision of thetumour, andthere isalways thepossibility of having positive Intraoperative assessment of the surgical margin status usingfrozen sectionis an option which is used in some centres. However, the frozen isolated ontheperforators; D:Immediate postoppictures; E,F. On follow up.Patient was not ready for contralateral symmetrisarion. Figure 3. A. Preoperative markingandlocalization of perfortors for combined LTAP plusICAP; B. Defect after tumour excision; C. Theflap was completely [16], 218patients underwent BCS reconstructionwith and et al [13] recently showed [18, 7

Clinical Study ecancer 2020, 14:1073; www.ecancer.org; DOI:https://doi.org/10.3332/ecancer.2020.1073 for secondary correctionsis negligible. As aresult,cosmeticno additional procedure hasbeendoneinour cohort. Another limitation was setup, where thepatientsand their immediate family members thetreatment support costs mostly fromof out pocketexpenses, thedemand from additionalprocedures like deformity correction, andcontralaterallipomodelling symmetrisation. However, inour resource-constrained potentially explored in a future series to reduce the reoperation rate. Those patients minorwith contour deformities could have benefitted like body image scaleor Breast Q[20,21].In thepresent study, thefrozen section was not usedto assessthemargin status. This could be This study has some potential limitations. Patient satisfaction was assessed Likert’swith scale and needed a more robust validated method satisfaction amongpatients (90%),andour study alsohadsimilar findings. which describethe use of CWPF, in efited from theuseof CWPF, goodwith oncological outcomes andreasonable patient satisfaction. We have studiespublished, summarised reported inasimilar study doneinKorean women [12].Most of thepatients inour serieshadsmallto medium-sized breasts, andthey ben - In thepatientsatisfaction survey, which was conducted 6months after thecompletion of radiotherapy, our results were similar to those Figure 4.Indocyanine green (ICG) immunofluorescence intraoperative screen of an AICAP flap. Theflapis seen well-perfused. NR, Not Reported; MS,Muscle Sparing. Table 3.Publishedoutcome data of CWPF inpartialbreast reconstruction. Hamdi et al [6] Hamdi et al [9] Munhoz et al[14] McCulley et al[8] Roy PK JB Kim Present cohort et al[12] [13] Belgium 2004, Belgium 2006, Brazil 2011, UK 2015, UK 2016, Korea 2017, India 2019, Year, location Table 3. All of these studieshave shown acceptable surgical complication rates (around 10%) and high 31 16 13 75 40 33 40 n • • • • • • • • • • • • • • CWPF used MS LD LICAP TDAP LICAP LICAP LICAP LTAP LICAP LTAP LICAP TDAP LTAP LICAP AICAP NR NR 0 0 4 (10%) 3 (9.1%) 5 (12.5%) Margin positivity • • • • • • • • • • • • • • • Complications Partial necrosis (9.6%) Wound dehiscence: (6.4%) Seroma (12.9%) (12.5%) Wound dehiscence Fat necrosis 1(7.6%) (15.3%) Wound dehiscence Fat necrosis 2 Superficial necrosis 1 Fat necrosis 2 Superficial necrosis 1 Fat necrosis 4 Linear necrosis 8 Wound disruption 4 SSI 2(5%) Total flaploss1(2.5%) NR NR Satisfied (90%) NR (82%) Excellent/good Excellent/good (84.8%) Excellent/good (95%) Satisfaction 8

Clinical Study ecancer 2020, 14:1073; www.ecancer.org; DOI:https://doi.org/10.3332/ecancer.2020.1073 There was nofundingreceived for thisstudy. Funding disclosure The authors declare noconflicts of interest. Declaration of conflicts of interest Kumar Agrawal, Sudip Ratna Shakya), Writing—Review andediting( All authors), Final approval of manuscript (All authors). (SudipRatna Shakya, Shashank Nigam), Data Analysis (Sanjit Kumar Agrawal, SudipRatna Shakya), Writing—Original Draft Preparation (Sanjit Conceptualisation (Sanjit Kumar Agrawal), Methodology (Sanjit Kumar Agrawal, Soumitra Shankar Datta, Rosina Ahmed), Data Collection Authors’ contributions Abbreviations system. firmationof the vascularity of theraisedis helpful flap if technology the isavailable, usingintraoperative Doppler andinfrared fluorescence and goodselection preoperativeand designof planning are flaps neededto achieve agood outcome. Careful dissectionofand con theflap - has shownthat techniquemaythis for beused tumours located inlateral, central andinferomedial quadrants of thebreast. Proper patient CWPF procedures show good outcomesbreast inpartial reconstruction interms of oncological safety andpatient satisfaction. Our study Conclusion survival outcome of theCWPF-based reconstruction. sizethe smallsample andshortfollow-upduration of 18months. Long-term results from large seriesare neededto assessthecosmetic and • • • • • • • • • • • • • • • • TDAP: SSI: SSO: OBS: NR: MS: LD: LTAP: LICAP: ICAP: ICG: indocyanine green DCIS: CWPF: chest wall perforator flap BCS: AICAP: ASTRO: American Society for Radiation Oncology musclesparing latissimus dorsi surgical site infections not reported Society of Surgical Oncology breast conservation surgery oncoplastic breast surgery ductalcarcinoma insitu lateral thoracic artery perforator intercostal artery perforator thoracodorsal artery perforator lateral intercostal artery perforator anterior intercostal artery perforator 9

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Clinical Study