Available online at www.sciencedirect.com

EJSO 39 (2013) 320e328 www.ejso.com

Review

Skin sparing mastectomy and immediate breast reconstruction: A review

A. Agrawal a,c,*, D.M. Sibbering b, C-A. Courtney b

aUniversity of Nottingham, Division of Breast Surgery, Royal Derby Hospital, Derby, UKbDepartment of Breast Surgery, Royal Derby Hospital, Derby, UK

cNottingham Breast Institute, Nottingham, UK

Accepted 17 December 2012

Available online 17 January 2013

Abstract

Aims: Skin Sparing Mastectomy (SSM) is widely practised now in major centres which manage large numbers of breast cancer but anxietystill exists over the safety of SSM both from oncological and aesthetic points of view. We aim to review literature to date in SSM andsummarise and discuss the current evidence.Methods: Studies were identified by an online search of the English language literature in the PubMed database till April 2012 followed byan extensive review of bibliographies from relevant articles.Results: There is abundance of evidence with regards to the safety of SSM both oncologically and aesthetically especially in immediatebreast reconstruction. The use of SSM technique broadens the repertoire of oncoplastic techniques and at the same time facilitates suchtechniques by preserving patient’s native skin and anatomical landmarks.Conclusions: SSM is a safe technique providing better cosmetic outcome without compromising oncological safety as per the current ev-idence. However, prospective data collection of its application in various newer types of reconstructions, and continuing long-term follow-up of current data series would be prudent to evaluate long-term outcomes.� 2012 Elsevier Ltd. All rights reserved.

Keywords: Mastectomy; Breast; Skin sparing; Oncoplastic; Reconstruction

Introduction

Skin Sparing Mastectomy (SSM), essentially involvesexcision of whole of the breast tissue including thenipple-areola complex (NAC) whilst sparing or preservingthe breast skin envelope. Nipple sparing mastectomy(NSM), in contrast, is SSM along with preservation of theNAC although often, rather confusingly, used interchange-ably with SSM. The term subcutaneous mastectomy (SCM)is referred to when a substantial amount of breast tissue ispreserved such as in gynaecomastia but again erroneously

* Corresponding author. Breast Surgery, Graduate Entry Medicine

(GEM) School, University of Nottingham, Royal Derby Hospital, Derby

DE22 3DT, UK. Tel.: þ44 (0) 1332 724881.

E-mail addresses: amit.agrawal@nottingham.ac.uk, docagrawal@

hotmail.com (A. Agrawal).

0748-7983/$ - see front matter � 2012 Elsevier Ltd. All rights reserved.

http://dx.doi.org/10.1016/j.ejso.2012.12.015

used interchangeably with either SSM or NSM though itshould be a redundant term not to be used in cancer surgery.

The concept of mastectomy whilst sparing the skin wasfirst described by Freeman in 1962.1 He described subcuta-neous mastectomy in benign conditions of the breastwherein excision of the NAC was not necessary. Later,early series from 1985 onwards by Toth and colleaguespopularised immediate breast reconstruction (IBR) withSSM in breast cancer.2,3 Current practice involves usingSSM in therapeutic as well as risk reducing setting suchas BRCA gene mutation positive or high risk familyhistory.

Most guidelines including the Association of Breast Sur-gery (ABS) guidelines (in the United Kingdom)4 recommendthat IBR should beoffered to every patient undergoingmastec-tomy, if deemed safe oncologically. In the context of IBR,SSM provides a better choice over simplemastectomy by pre-serving the natural native skin envelope. At the same time, it

321A. Agrawal et al. / EJSO 39 (2013) 320e328

facilitates a favourable aesthetic outcome by minimal distur-bance of breast foot-print and borders especiallywith the pres-ervation of the infra-mammary fold.5e8

Acceptance of SSM though initially hesitant (mainly dueto apprehension of increased local recurrence (LR) ratesover conventional mastectomy) has rapidly become a rou-tine practice. ABS recommends a standard of <5% LR at5 years following (any) mastectomy with a desired targetof <3% at 5 yrs. There have been recent publications ofseveral series demonstrating the oncological safety ofSSM with IBR. We, therefore, present an overview of re-cent literature in relation to SSM and IBR for breast cancerand discuss its oncological and aesthetic safety.

Indications

Generally accepted indications for mastectomy are:

-patient choice,-multi-centric disease (multiple foci in different quad-rants as opposed to multi-focal disease in a singlequadrant),-large in-situ disease or diffuse micro calcifications,-large tumour size to breast volume ratio which pre-cludes breast conservation surgery (including volumedisplacement techniques),-failed initial conservation surgery necessitatingmastectomy-recurrence of disease in a previously conserved breast-RT (radiotherapy) not possible after conservation sur-gery such as previous mantle RT for Hodgkin’s disease,in those with collagen vascular diseases and in thosewith Tp53 mutation

When IBR is desired, SSM is increasingly the preferredtype of mastectomy especially9 when there is low likeli-hood of adjuvant RT such as in in-situ disease, Grade 1 dis-ease (ElstoneEllis modification of BloomeRichardson),10

non-lympho-vascular invasive disease. However, as dis-cussed later in the “SSM and RT” section, the likelihoodof RT is deemed by many to be not an absolute contra-indication to surgery especially when purely autologous re-construction is planned.

Incisions

The incisions employed for SSM in general has beencomprehensively grouped into four types by Carlson11:

-Type I ¼ circum-areolar (in wide areola), small ellipsearound areola or circum-areolar with transverse lateralextension like tennis racquet (for small areola),-Type II ¼ bi-lobed or dumb-bell shaped incision to in-clude both the areola and the skin over the tumour(when the tumour is close to areola but separate fromNAC),

-Type III ¼ separate incisions for the areola and the skinover the tumour (when there is significant distance be-tween NAC and superficial tumour or previous incision),-Type IV ¼ wise-pattern (in Grade 3 or 4 ptotic breastsespecially combined with contra-lateral reductionmammoplasty. Increasingly, with the use of a Wise pat-tern incision, the dermis of the lower pole can be de-epithelialised and preserved for use as a hammock(also known as dermal sling) to provide more robust in-ferior pole cover and support to the implant in implantbased reconstruction or even to allow direct placementof the implant rather than a tissue expander.12,13

Apart from the types elegantly described by Carlson,other incision patterns have been utilised by other authors.Recently, Hall-Findlay vertical reduction mammaplastypattern has been reported for SSM with autologous tissueIBR (such as LD, DIEP flaps).14 Various groups have de-scribed endoscopic or video assisted SSM with either im-plant based IBR15e17 or LD flap based IBR18 using5e6 cm lower axillary incision after Sentinel lymph nodebiopsy (SNB) or level I/II dissection through the sameincision.

SSM and axillary procedure

The standard method of axillary staging is SNB eitherwith a single/dual dye (patent blue V dye and/or 99Tcmradio-isotope) technique with a separate incision unlesseasily accessible through the breast incision. If the SNBdemonstrates lymph node metastases, completion axillarynode clearance could be challenging and potentially riskyespecially if an autologous/perforator flap dependent onthe LD pedicle has been performed such as the LD/TDAPflap or TRAM based on the LD pedicle.19 Alternativemethods suggested in the SSM with IBR setting are intra-operative assessment20 of sentinel nodes or upfront SNBprior to mastectomy21 but these are not standard modesof practice at present.

SSM and reconstructive options

Individual reconstructive options in SSM are largelyguided by patient’s choice and surgeons experience as dis-cussed further.

Implant reconstruction

Two stage expander-implant based reconstructionSSM technique can be used for the placement of a sub-

muscular tissue expander followed by a second surgery forthe placement of a fixed volume silicone implant without theneed for additional flap cover. This is especially suitable forpatients who have the least predicted possibility of adjuvantRT, for example in-situ or low grade disease, though some au-thors have argued against selecting patients using this

322 A. Agrawal et al. / EJSO 39 (2013) 320e328

criterion.22 Due to possible interference with RT by the metalin the tissue expanders with integral inflation port, expanderswith remote port may be an alternative choice.

One stage implant reconstructionSSM technique could be used for IBR using total sub-

muscular permanent one stage expandable implant (Beckeradjustable silicone-saline implant).23,24 However, this maybe achievable only in relatively small breastedwomenwithoutflap cover due to the limitations of the degree of expansion ofthe skin and the pectoral muscles. One stage implant recon-struction following SSM in previously augmented patientshas been shown to be a viable optionwith placement of the im-plant in the existing submuscularesubfascial pocket and rein-forcing it with the existing capsule.25

Implant reconstruction with dermal flapSSM technique is used in large-breasted patients

wherein the redundant lower pole skin can be de-epithelialised and used as a hammock both to provide ptosis(and thus symmetry with contra-lateral side) and also assufficient cover to the expander/implant by approximatingthe upper edge of the flap with the detached lower edgeof the pectoralis major muscle.12,13,26 For example, Navaand colleagues13 used a medium size of 444.3 cc of onestage implant for large ptotic breasts with a sternal notchto nipple distance >25 cm with good results.

Acellular dermal matrix (ADM) assisted implantreconstruction

In a similar fashion to the dermal sling, a range of com-mercially available ADMs (Strattice�, Alloderm�, Life-cell; Surgimend�, Q Medical, Veritas�, Synovis;DermaMatrix�, DePuySynthes; NeoForm�, FlexHD�,Mentor; etc.) can be used not only to provide ptosis and ex-tra cover to the expander/implant but also to provide addi-tional layer to reduce implant visibility/palpability.27,28 Intheir meta-analysis of 16 eligible studies, Ho and col-leagues29 stated that compared to non-ADM reconstruc-tions, ADM reconstructions were associated with lowerrates of capsular contracture but had a higher likelihoodof seroma (pooled OR, 3.9; 95% CI, 2.4e6.2), infection(pooled OR, 2.7; 95% CI, 1.1e6.4) and reconstructive fail-ure (pooled OR, 3; 95% CI, 1.3e6.8). Role of ADM inminimising adverse cosmetic sequel following RT in SSMand IBR is discussed further in adjuvant RT section.

Autologous breast reconstruction

Latissimus dorsi flapStudies have reported SSM with IBR using the LD

flap.24,30e32 Other studies have also reported IBR withthe LD miniflap.33

Abdominal flap breast reconstructionBesides, common abdominal flaps such as the TRAM

flap,6,34e38 DIEP flap,39 other less common abdominal/non-abdominal flaps24 such as SIEA (superficial inferiorepigastric artery flap), SGAP (superior gluteal artery flap)have also been used for reconstruction following SSM.

SSM and skin flap viability

Besides the complications inherent to simple mastec-tomy such as bleeding, infection, wound healing issues;skin flap necrosis and loss is seen more commonly follow-ing SSM than following simple mastectomy. Carlson statedthe rate of native skin flap necrosis to vary between 10 and22% ranging from epidermal peeling to full thickness skinloss.11 The ‘National Mastectomy and Breast Reconstruc-tion Audit (NMBRA)’ in the UK revealed that 7.6% pa-tients were returned to theatre for local complicationwhich included wound infection, skin flap necrosis requir-ing debridement and haematoma.40

The superficial plane of dissection between the subcuta-neous fat and the breast tissue has been shown to be indis-tinct in approximately 44% of patients in microscopicexamination of 62 breast resection specimens.41 This planeof dissection is important in ensuring that the mastectomyis achieved completely without any oncological compro-mise by leaving residual breast tissue. The plane of mastec-tomy in SSM is the same as in simple mastectomy exceptthat technically it is more challenging and needs more pa-tience given the limitations of the space for surgical fingersand instruments and also the lack of panoramic view of theplanes as in simple mastectomy.

Studies have looked into the amount of possible residualbreast tissue after SSM given the inherent access limita-tions, particularly in circum-areolar incisions and the con-flicting requirements of removing all of the breast tissuefor oncological purposes vs. the possibility of compromis-ing flap viability by reducing flap thickness. Torresanet al.42 analysed the margins of 42 SSM flap for evidenceof breast tissue and/or disease. They reported presence ofresidual breast tissue in 59.5% and disease in 9.5% ofSSM, especially in skin flaps thicker than 5 mm. In anotherrecent study, residual breast tissue was seen in 6% (n ¼ 4)of 66 SSM skin excised for pathological assessment thoughthis did not translate to any recurrence at a median followup of 33.5 months.43

Surgical practice for SSM varies between the use ofscalpel, scissors, mono-polar diathermy, bi-polar diathermy,harmonic scalpel,15,16 radiofrequency coagulation44 with orwithout hydro-dissection using local anaesthetic solutionwith or without adrenaline to encourage haemostasis. Tech-nically, skin flap necrosis has been shown to be the samewith scalpel dissection when compared with diathermy ina retrospective study of 151 SSM.45 These authors foundthat increased body mass index (BMI), breast mass ofmore than 750 g and sternal notch to nipple distance of

323A. Agrawal et al. / EJSO 39 (2013) 320e328

more than 26 cm were significantly associated with flap-related complications in the absence of diabetes andsmoking.

Another study44 of the use of radiofrequency coagula-tion and conventional diathermy in 60 patients showed nosignificant difference but the skin flap complication ratewas higher in smokers and those with a ‘tennis racquet’type incision compared to circum-areolar incision. Therewas a higher incidence ( p ¼ 0.0977) of wound breakdownin the tennis racquet incision in the Davies study45 althoughthe Wise-pattern incision was significantly associated withwound dehiscence.

SSM and adjuvant radiotherapy

The need for adjuvant chest wall radiotherapy (RT) fol-lowing mastectomy is determined by the estimated risk ofloco-regional recurrence. This can be influenced by severalfactors including tumour grade, the presence of lympho-vascular invasion, the HER2 status and the presence of ax-illary lymph node metastases.

The current NICE guidelines46 recommend chest wallRT in invasive disease depending upon risk categorisation:

-Low risk i.e., lymph node negative disease ¼ no RT(unless dictated by tumour size >5 cm or other domi-nating factors)-Intermediate risk i.e., 1e3 positive lymphnodes ¼ variable practice but currently the focus ofan ongoing randomised trial wherein the mastectomypatients with 1e3 nodes, lympho-vascular disease,grade III or ER negative disease and those under 40years of age are randomised to either RT or no RT47

-High risk i.e., >4 positive nodes or tumour at any resec-tion margin ¼ RT recommended.

There has been much debate regarding the safety of RTin SSM in terms of skin flap viability, wound healing andcosmetic outcome. Generally, when there is a substantialpossibility of adjuvant RT, current options are either for de-layed BR (over IBR) or autologous BR (over implant only).However, there are increasing reports suggesting that unto-ward aesthetic outcomes could be mitigated by usage ofnewer techniques and products such as ADM.

A recent study48 compared IBR in 40 SSM vs. 60 non-SSM in patients who had stage III disease and receivedneo-adjuvant chemotherapy and adjuvant RT. The authorsshowed that the rate of complications needing surgical in-tervention were significantly higher (37.5% vs. 5%,p < 0.001) in the SSM group. However, the 2-year loco-regional control, breast cancer specific survival and overallsurvival compared favourably with the conventional mas-tectomy group. RT is not always implicated as the dominantcause of complications as 60% (9 of 15 patients) of compli-cations in SSM and 33% (1 of 3 patients) of complicationsin non-SSM reconstructions occurred prior to the

administration of RT. In contrast, a retrospective study of227 implant based reconstruction showed an increasedrate of re-operation but not in complication or capsular con-tracture rates following SSM & RT.49 15% complicationrates & 10% re-operation rates were claimed to be betterthan previously so authors continue to recommend theirpractice.

It is generally believed that the use of ADM reduces theincidence of complications in implant based reconstructionespecially post-RT. However, Chun and colleagues,50 in a ret-rospective comparison of 269 reconstructions with ADM(with either expander or implant) vs. 146 reconstructionswithout ADM, showed that seroma, serious infections andserious skin flap necrosis (full thickness skin necrosis requir-ing surgical debridement) were all significantly commoner inADM group (seroma and major infections persisting afterexclusion of autologous flap reconstructions). On multiplelogistic regression analysis, besides BMI, ADM was a signif-icant risk factor for seroma (OR ¼ 4.24, p ¼ 0.018) and in-fection (OR ¼ 5.37, p ¼ 0.006). There were no significantdifferences in age, smoking status or RT between the twogroups but BMI and the mastectomy weight were signifi-cantly higher in the ADM group. The authors concludedthat the rate of infection could be due to increased aspira-tions needed in this group due to the higher incidence of se-roma formation.

A recent paper28 also showed that the use of ADM wasassociated with 3-fold risk of post-operative complicationson univariate logistic regression analysis of 56 patients (25of the 56 patients, p ¼ 0.007). RT was also a high risk fac-tor, though not significant, for complications (odds ratio of0.45, p ¼ 0.22) over and above age 50 years, BMI >27 kg/m2, smoking, diabetes and chemotherapy. This analysisalso showed that RTwas a significant risk factor for implantloss (odds ratio of 8.09, p ¼ 0.04) whilst other factors (asabove) were non-significant.

In the context of adjuvant RT, evidence is awaited re-garding the short and long term oncological and cosmeticoutcomes following publication of START trial in 2008,51

wherein instead of the conventional dosage of 50 Gy in25 fractions over 5 weeks, 40 Gy in 15 fractions over 3weeks are administered.

SSM and locally advanced breast cancer

As SSM involves preserving the skin of the breast, anyinvolvement of the skin of the breast (such as ulceration,fungation, peau d’orange) in locally advanced breast cancer(LABC) may limit the usage of this technique but may notpreclude it altogether. Discrete areas of skin tethering donot necessarily translate to involvement of skin and arenot a contraindication to SSM (Peyser, Abel et al., 2000).

A prospective series of 25 patients with stage IIB(n ¼ 12) and stage III (n ¼ 13) disease over 1996e1998 un-derwent SSM (without prior neo-adjuvant chemotherapy)with either TRAM or LD flap reconstruction. At a median

324 A. Agrawal et al. / EJSO 39 (2013) 320e328

follow-up of 49.2 (range 33e64) months, local recurrence(LR) was identified in 1 patient (4%) and systemic recur-rence (SR) in 4 (16%).52

A retrospective Korean study53 of 87 patients who under-went SSM (without prior neo-adjuvant chemotherapy) be-tween 1996 and 2005 showed a LR rate of 4.6% (4/87) forstage IIBeIII disease and 7.7% (2/26) for T3 tumours. Stagespecific LR rates were 12.5% (1/8, stage IIB), 1.9% (1/54,stage IIIA) and 8% (2/25, stage IIIC) which were not signif-icantly different from conventional mastectomy rates of 0%(0/54), 1.7% (7/420) and 3.9% (133/336) respectively at 5years. They also demonstrated that there was no significantdifference in the disease free survival (DFS) and the overallsurvival (OS) between the two groups.

SSM after neo-adjuvant therapies in locally advancedbreast cancer

Neo-adjuvant chemotherapy

Notwithstanding the preceding section, evidence is accu-mulating regarding the use of neo-adjuvant chemotherapyin the locally advanced setting. As well as providing earlysystemic oncological control, neo-adjuvant chemotherapycan also downsize the tumour to facilitate reconstructiveoptions such as SSM.

As discussed in adjuvant RT section, Prabhu et al.48

showed that the 2-year loco-regional control, breast cancerspecific survival and overall survival were favourable in 40SSM (but not significant) patients following neo-adjuvantchemotherapy and adjuvant RT vs. 60 non-SSM patientswith stage III disease but the rate of complications (needingsurgical intervention) were significantly (37.5% vs. 5%,p < 0.001) higher in SSM group.

Similarly, in another study, short-term post-operative com-plications in 37 women (with 48 immediate reconstructions)with LABC between 2006 and 2009 were less in those withneo-adjuvant compared with those who did not have neo-adjuvant chemotherapy (15% vs. 29%, p ¼ 0.042) althoughthe rate of prosthetic loss was similar e 8% vs. 11%,p ¼ 0.566,.54

Neo-adjuvant radiotherapy

A small study55 showed significantly higher capsularcontracture rates and native skin flap compromise followingSSM (n ¼ 8) after pre-operative RT than after SSM withoutpre-operative RT (n ¼ 20). This study also found thatTRAM flap reconstruction had better results than LD flapin this setting.

Outcome studies in SSM

There is general lack of outcome studies comparingSSM with conventional mastectomy with or without IBRwith most being comparative studies between SSM and

breast conserving surgery (BCS). Although not valid com-parisons, some are briefly discussed here to highlight theoutcomes of SSM in those comparisons.

An early study by Rainsbury and colleagues33 showedthat the outcomes (complications, functional disability, cos-metic and psychological morbidity) in SSM and IBR withLD flap were less favourable compared to BCS and LDminiflap reconstruction. Adjuvant RT alone did not explainthe higher rate of complications in the SSM group as 12 of57 SSM patients had adjuvant RT compared 37 of 59 LDminiflap reconstructions. However, authors did note signif-icant association between smoking and SSM complicationsin their conclusion.

In a study of 130 patients who hadLDor prosthesis or bothduring 2001e2008, at a median FU of 36 (6e101) monthsthere was no LR but 8 SR.56 Also, there were 2 implant re-movals and 1 marginal skin ischaemia. Capsulotomy wasneeded for significant capsular contracture in 85% (23/27)of patients who had RT compared to 13% (13/100) who didnot have RT. In the same study, a postal questionnaire surveyused VAS (Visual Analogue Scale) to assess patient satisfac-tion. With a response rate of 64.6%, a median VAS score of 9(5e10) was recorded with no significant difference betweenLD flap (mean¼ 9.3, median¼ 10) and implant (mean¼ 9,median ¼ 10) reconstructions.

Another study57 which assessed QoL by using validatedbreast cancer specific questionnaires (EORTC-QLQ-B23and FACT-B) at least 12 months (mean FU of 36 months)following completion of adjuvant chemo-radiotherapy in179 SSM reported comparable QoL scores with 160 age-matched women undergoing BCS. 41% (n ¼ 102) patientshad RT with 75 returning the QoL questionnaire and therewas no difference in the QoL reported between this groupand those who did not receive RT. Modified Baker58 ClassIV capsular contracture was seen in 11% (n ¼ 28) patients(all with prosthesis) with majority without RT (64%,n ¼ 18). There was no significant difference ( p ¼ 0.561)between those with RT and those without RT. No patientwith an extended LD flap had Grade IV contracture though41% received RT (7/17).

In the UK, a prospective trial is studying the quality oflife (QoL) following autologous reconstruction (extendedLD flap) in patients with or without RT.59,60

Recurrence rates following SSM

As will be evident later in this section, there is wide varia-tion in the reported LR rates (0e24%)57 and loco-regional re-currence rates (2e20%).61 One of the early reports from anexperienced centre (MD Anderson) stated the LR rate to be7%62 at a median FU ofmore than 6 years to recently reportedLR rate of 2.9% from another experienced centre (Glasgow)after longest reported FU of median of almost 10 years.24

This improvement in the rate of LR or loco-regional recur-rence (LRR) may be a reflection of earlier diagnosis and im-provements in adjuvant therapies.

325A. Agrawal et al. / EJSO 39 (2013) 320e328

Early reports from MD Anderson reported a regional re-currence (RR) rate of 2.6% in 545 patients with SSM andIBR.34 A subset of 95 patients who had FU > 4 yearsshowed the rate to be 4.2%. 104 patients from the same co-hort who had FU > 5 years showed a LR rate of 6.7% anda SR rate of 12.5%.63 After 6 years of FU, authors62 re-ported a LR rate of 7.0% in 114 SSM patients whilst theLR rate was 7.5% in 40 non-SSM patients. These seriesof publications from the same centre aptly demonstratethe importance of long-term FU in determining the true re-currence rates after breast cancer surgery.

Reported rates of LRs in SSM are listed in Table1.3,13,24,30,61,62,64e76

Vaughan study67 showed a significant decrease in sur-vival in patients with LR (5.3%, 11 out of 210 SSM) com-pared to those without recurrences ( p < 0.006). Two of theLR in this study was initial pure DCIS. Carlson et al.77

showed a LR rate of 3.3% in 223 patients with DCIS.High tumour grade was significantly associated with recur-rence. Sheikh’s study74 associated increased LR rates withyounger age, larger tumours, multiple ipsilateral tumoursand palpable tumours with close/positive margin (<2 mm).

Nine out of 11 recurrences in the Vaughan study were inthe index quadrant.67 Interestingly, study by Sheikh et al.74

showed that upper inner quadrant tumour were significantlyless likely to have clearance margin (>2 mm). However,this did not raise the risk of LR in this quadrant but longerterm FU data is warranted.

Glasgow reported the longest FU study reported so far24

in 207 patients (invasive ¼ 153, in-situ ¼ 54) with SSM

Table 1

Literature reporting local recurrence rates following skin sparing mastectomy (c

Authors et al. SSM/vs. Mx (n); FU

(follow-up) in months (m

Newman et al., 199864 372 SSM; median FU ¼Toth et al., 19993 50 SSM; median FU ¼ 5

Medina-Franco et al., 200265 173 SSM; median FU ¼Carlson et al., 200375 539 SSM; median FU ¼

Drucker-Zertuche et al., 200766 105 SSM; mean FU ¼ 5

Vaughan et al., 200767 210,206 SSM; median F

Lanitis et al., 201030

Meta-analysis of 7

studies61,62,68e71,76

825 SSM vs. 2518 Mx; m

FU for studies ¼ 37.5e1

Kinoshita et al., 201172 73 SSM vs.129 Mx; mea

Nava et al., 201113 77 SSM; median FU ¼ 3

Sheikh et al., 201174 177 SSM vs. 249 Mx; m

Peled et al., 201273 126 SSM; median FU ¼Romics et al., 201224 207 SSM; median FU ¼

and IBR (between 1995 and 2000). The median time to re-currence was 36 (7e128) months and the breast cancer spe-cific survival was 90.8%. Most recurrences were in invasivedisease (24.8%) with 3.9% LR, 11.1% LRR and 13.7% SRwith significantly higher risk in lymph node positive dis-ease (95% CI, 0.04e0.31, p ¼ 0.009), higher stage disease( p < 0.001) and tumour grade ( p ¼ 0.031). The authorsalso reported a higher risk of recurrence (95% CI,0.02e0.23, p ¼ 0.018) in those with autologous reconstruc-tion than those with implant-based reconstructions. How-ever, this was a reflection of disease stage than the typeof mastectomy or reconstruction as higher stage diseasehad less implant-based reconstruction perhaps due to antic-ipated likelihood for adjuvant RT which is more likely tocompromise implant-based reconstruction than autologousreconstruction.

Nipple sparing mastectomy

NSM is becoming an accepted practice and replacingSSM and we discuss NSM briefly as detailed review is out-side the scope of this paper. Spear and colleagues78 re-viewed practice of NSM in their review and suggested analgorithm for selection of patients for therapeutic indicationof NSM. Essentially the indications are similar to SSM withthe obvious exception of the tumour proximity to NAC.They suggested that selection criteria for NSM (tumour<3 cm, >2 cm distance from NAC, node negative, noskin involvement and no inflammatory breast cancer), therisk of occult tumour will be between 5 and 15% reduced

hronological order of publication).

)

LR (%)

26 m 6.2%

1.5 m 0%

73 m 4.5%

61.6 m 5.5% [0.6, 3.0, 10.4, 11.1,

0% in Stage 0, I, II, III, IV

respectively]

1 m 1%

U ¼ 58.6 m 5.3% (9 of 11 in the index

quadrant)

edian

01 m

5.7% SSM (3.8e10.4)vs. 4.0% Mx (1.7e11.5)

OR ¼ 1.14

(95% CI, 0.78e1.68)[Systemic recurrence ¼8.3% SSM vs. 12.1% Mx;

OR ¼ 0.63, 95% CI, 0.43e0.92]

n FU ¼ 30 m 2.7% SSM vs. 3.9% Mx

6 m 0.5%/year

ean FU ¼ 28 m 1.1% SSM vs. 0.8% Mx

(non-significant);

[positive or close margin, 29%

SSM vs. 12% Mx; p < 0.01]

28 m 2.4%

119(14e163) m 2.9% (8.2% loco-regional,

10.6% systemic recurrence)

326 A. Agrawal et al. / EJSO 39 (2013) 320e328

further if frozen section was used. They also noted that ma-jority recurrences were in the NAC which could be easilyexcised under local anaesthesia. However, Hensen79 in re-sponse to this article explained rationale for expandingthe indications further and including tumours <4 cm andnode positive disease.

Largest series of 934 NSM from Milan80 found positiveretroareolar margin as the sole risk factor for necrosis(4.2% NAC necrosis) with literature ranging from 0 to48%.80 Age, BMI, menopausal status, smoking, tumoursize, axillary lymph node status and histopathological sta-tus were not risk factors. However, a prospective study of50 NSM from the same institute81 confirmed that total nip-ple necrosis is unusual. However, partial nipple necrosis isnot infrequent but heals with or without debridement withrisk factors being young age, smoking, thin areolar flapthickness (<5 mm) and superior circum-areolar incisionpresumably due to division of blood supply.

Conclusions

Thus, overall current literature confirms the comparablesafety of SSM and simplemastectomy as there is no increasedLR.SRappears higher thanLRbut this is dependent on tumourbiology & systemic therapy factors. Current literature alsoconfirms the cosmetic outcome and overall patient satisfactionwith SSM based breast reconstruction. However, prospectivedatabase of applications of newer SSM based reconstructivetechniques should be maintained to evaluate further long-term safety and cosmetic outcome.

Funding source

None.

Conflicts of interest

The authors declare that they have no conflict of interestin preparation of this manuscript.

References

1. Freeman BS. Subcutaneous mastectomy for benign breast lesions with

immediate or delayed prosthetic replacement. Plastic and Reconstruc-

tive Surgery and the Transplantation Bulletin 1962;30:676–82.

2. Toth BA, Lappert P. Modified skin incisions for mastectomy: the need

for plastic surgical input in preoperative planning. Plastic and Recon-

structive Surgery 1991;87(6):1048–53.

3. Toth BA, Forley BG, Calabria R. Retrospective study of the skin-

sparing mastectomy in breast reconstruction. Plastic and Reconstruc-

tive Surgery 1999;104(1):77–84.

4. ABS. Surgical guidelines for the management of breast cancer. Euro-

pean Journal of Surgical Oncology: the Journal of the European So-

ciety of Surgical Oncology and the British Association of Surgical

Oncology 2009;35(Suppl. 1):1–22.

5. Carlson GW. Skin sparing mastectomy: anatomic and technical con-

siderations. The American Surgeon 1996;62(2):151–5.

6. Rand RP, et al. Skin-sparing mastectomy with immediate tissue recon-

struction. The Western Journal of Medicine 1996;164(2):166.

7. Patani N, Mokbel K. Oncological and aesthetic considerations of skin-

sparing mastectomy. Breast Cancer Research and Treatment 2008;

111(3):391–403.

8. Slavin SA, et al. Skin-sparing mastectomy and immediate reconstruc-

tion: oncologic risks and aesthetic results in patients with early-stage

breast cancer. Plastic and Reconstructive Surgery 1998;102(1):49–62.

9. Baildam AD. Skin-sparing mastectomy. European Journal of Cancer

2011;47(Suppl. 3):S342–3.

10. Elston EW, Ellis IO. Method for grading breast cancer. Journal of

Clinical Pathology 1993;46(2):189–90.

11. Carlson GW. Technical advances in skin sparing mastectomy. Interna-

tional Journal of Surgical Oncology 2011;2011:396901.

12. Goyal A, et al. Outcome after autologous dermal sling-assisted imme-

diate breast reconstruction. British Journal of Surgery 2011;98(9):

1267–72.

13. Nava MB, et al. Skin/nipple sparing mastectomies and implant-based

breast reconstruction in patients with large and ptotic breast: oncolog-

ical and reconstructive results. Breast 2012;21(3):267–71.

14. Serra MP, Staley H. The Hall-Findlay mammaplasty pattern for skin-

sparing mastectomy. Case report. Il Giornale di chirurgia 2012;

33(1e2):14–6.15. Ito K, et al. Endoscopic-assisted skin-sparing mastectomy combined

with sentinel node biopsy. ANZ Journal of Surgery 2008;78(10):

894–8.

16. Ho WS, Ying SY, Chan AC. Endoscopic-assisted subcutaneous mas-

tectomy and axillary dissection with immediate mammary prosthesis

reconstruction for early breast cancer. Surgical Endoscopy 2002;

16(2):302–6.

17. Kitamura K, et al. Early results of an endoscope-assisted subcutaneous

mastectomy and reconstruction for breast cancer. Surgery 2002;

131(Suppl. 1):S324–9.

18. Nakajima H, et al. Video-assisted total glandectomy and immediate re-

construction for breast cancer. Biomedicine &

Pharmacotherapy ¼ Biomedecine & Pharmacotherapie 2002;

56(Suppl. 1):205s–8s.

19. Kuerer HM, Krishnamurthy S, Kronowitz SJ. Important technical con-

siderations for skin-sparing mastectomy with sentinel lymph node dis-

section. Archives of Surgery 2002;137(6):747.

20. Meretoja TJ, et al. Sentinel node biopsy with intraoperative diagnosis

in patients undergoing skin-sparing mastectomy and immediate breast

reconstruction. European Journal of Surgical Oncology: the Journal

of the European Society of Surgical Oncology and the British Associ-

ation of Surgical Oncology 2007;33(10):1146–9.

21. Schrenk P, et al. The use of sentinel node biopsy in breast cancer pa-

tients undergoing skin sparing mastectomy and immediate autologous

reconstruction. Plastic and Reconstructive Surgery 2005;116(5):1278–

86.

22. Lambert K, Mokbel K. Does post-mastectomy radiotherapy represent

a contraindication to skin-sparing mastectomy and immediate recon-

struction: an update. Surgical Oncology 2012;21(2):e67–74.

23. Toth BA, Le HN. Invited discussion: immediate breast reconstruction

with expandable permanent anatomical implants after skin-sparing

mastectomy: aesthetic and technical refinements. Annals of Plastic

Surgery 2004;52(4):365–6.

24. Romics Jr L, et al. Ten-year follow-up of skin-sparing mastectomy fol-

lowed by immediate breast reconstruction. The British Journal of Sur-

gery 2012;99(6):799–806.

25. Salgarello M, et al. Immediate breast reconstruction after skin- or

nipple-sparing mastectomy for previously augmented patients: a per-

sonal technique. Aesthetic Plastic Surgery 2012;36(2):313–22.

26. Hammond DC, et al. Use of a skin-sparing reduction pattern to create

a combination skin-muscle flap pocket in immediate breast reconstruc-

tion. Plastic and Reconstructive Surgery 2002;110(1):206–11.

27. Endress R, Choi MSS, Lee GK. Use of fetal bovine acellular dermal

xenograft with tissue expansion for staged breast reconstruction.

327A. Agrawal et al. / EJSO 39 (2013) 320e328

Annals of Plastic Surgery 2012;68(4):338–41. http://dx.doi.org/

10.1097/SAP.0b013e31823b68d0.

28. Kobraei EM, et al. Risk factors for adverse outcome following skin-

sparing mastectomy and immediate prosthetic reconstruction. Plastic

and Reconstructive Surgery 2012;129(2):234e–41e.

29. Ho G, et al. A systematic review and meta-analysis of complications

associated with acellular dermal matrix-assisted breast reconstruction.

Annals of Plastic Surgery 2012;68(4):346–56.

30. Lanitis S, et al. Comparison of skin-sparing mastectomy versus non-

skin-sparing mastectomy for breast cancer: a meta-analysis of obser-

vational studies. Annals of Surgery 2010;251(4):632–9.

31. Abdalla HM, et al. Immediate breast reconstruction with expander as-

sisted latissimus dorsi flap after skin sparing mastectomy. Journal of

the Egyptian National Cancer Institute 2006;18(2):134–40.

32. Kim J, et al. Immediate extended latissimus dorsi flap reconstruction

after skin-sparing mastectomy for breast cancer associated with paraf-

finoma: report of a case. Surgery Today 2011;41(12):1680–3.

33. Gendy RK, Able JA, Rainsbury RM. Impact of skin-sparing mastec-

tomy with immediate reconstruction and breast-sparing reconstruction

with miniflaps on the outcomes of oncoplastic breast surgery. The Brit-

ish Journal of Surgery 2003;90(4):433–9.

34. Singletary SE. Skin-sparing mastectomy with immediate breast recon-

struction: the M.D. Anderson Cancer Center experience. Annals of

Surgical Oncology 1996;3(4):411–6.

35. Hidalgo DA. Aesthetic refinement in breast reconstruction: complete

skin-sparing mastectomy with autogenous tissue transfer. Plastic and

Reconstructive Surgery 1998;102(1):63–70. [discussion 71e2].36. Hidalgo DA, et al. Immediate reconstruction after complete skin-

sparing mastectomy with autologous tissue. Journal of the American

College of Surgeons 1998;187(1):17–21.

37. Gherardini G, et al. Immediate breast reconstruction with the trans-

verse rectus abdominis musculocutaneous flap after skin-sparing mas-

tectomy. International Surgery 2001;86(4):246–51.

38. Kim HJ, et al. Nipple areola skin-sparing mastectomy with immediate

transverse rectus abdominis musculocutaneous flap reconstruction is

an oncologically safe procedure: a single center study. Annals of Sur-

gery 2010;251(3):493–8.

39. Munhoz AM, et al. Immediate skin-sparing mastectomy recon-

struction with deep inferior epigastric perforator (DIEP) flap.

Technical aspects and outcome. The Breast Journal 2007;13(5):

470–8.

40. NMBRA. National Mastectomy and Breast Reconstruction Audit. UK.

Fourth annual report, 2011 2011;. Availablefrom: http://www.ic.nhs.

uk/webfiles/Services/NCASP/audits%20and%20reports/NHS%20IC%

20MBR%202011%20Final%20Interactive%2016-03-11.pdf.

41. Beer GM, et al. Incidence of the superficial fascia and its relevance in

skin-sparing mastectomy. Cancer 2002;94(6):1619–25.

42. TorresanRZ, et al. Evaluation of residual glandular tissue after skin-sparing

mastectomies. Annals of Surgical Oncology 2005;12(12):1037–44.

43. Dreadin J, et al. Risk of residual breast tissue after skin-sparing mas-

tectomy. The Breast Journal 2012;18(3):248–52.

44. Meretoja TJ, et al. Complications of skin-sparing mastectomy fol-

lowed by immediate breast reconstruction: a prospective randomized

study comparing high-frequency radiosurgery with conventional dia-

thermy. Annals of Plastic Surgery 2008;60(1):24–8.

45. Davies K, et al. Factors affecting post-operative complications follow-

ing skin sparing mastectomy with immediate breast reconstruction.

Breast 2011;20(1):21–5.

46. NICE. CG80. Early and locally advanced breast cancer: full guideline

2009;.http://guidance.nice.org.uk/CG80/Guidance/pdf/English.

47. SUPREMOtrial. Selective use of postoperative radiotherapy aftEr

MastectOmy.http://www.supremo-trial.com/ 2012.

48. Prabhu R, et al. The impact of skin-sparing mastectomy with immedi-

ate reconstruction in patients with Stage III breast cancer treated with

neoadjuvant chemotherapy and postmastectomy radiation. Interna-

tional Journal of Radiation Oncology, Biology, Physics 2012;82(4):

e587–93.

49. Hughes K, et al. The effect of radiotherapy on implant-based breast re-

construction in the setting of skin-sparing mastectomy: clinical series

and review of complications. Anticancer Research 2012;32(2):553–7.

50. Chun YS, et al. Implant-based breast reconstruction using acellular

dermal matrix and the risk of postoperative complications. Plastic

and Reconstructive Surgery 2010;125(2):429–36.

51. Bentzen SM, et al. The UK Standardisation of Breast Radiotherapy

(START) Trial B of radiotherapy hypofractionation for treatment of

early breast cancer: a randomised trial. Lancet 2008;371(9618):

1098–107.

52. Foster RD, et al. Skin-sparing mastectomy and immediate breast recon-

struction: a prospective cohort study for the treatment of advanced stages

of breast carcinoma. Annals of Surgical Oncology 2002;9(5):462–6.

53. Lim W, et al. Oncological safety of skin sparing mastectomy followed

by immediate reconstruction for locally advanced breast cancer. Jour-

nal of Surgical Oncology 2010;102(1):39–42.

54. Donker M, et al. Surgical complications of skin sparing mastectomy

and immediate prosthetic reconstruction after neoadjuvant chemother-

apy for invasive breast cancer. European Journal of Surgical Oncol-

ogy: the Journal of the European Society of Surgical Oncology and

the British Association of Surgical Oncology 2012;38(1):25–30.

55. Chang EI, Ly DP, Wey PD. Comparison of aesthetic breast reconstruc-

tion after skin-sparing or conventional mastectomy in patients receiv-

ing preoperative radiation therapy. Annals of Plastic Surgery 2007;

59(1):78–81.

56. Reefy S, et al. Oncological outcome and patient satisfaction with skin-

sparing mastectomy and immediate breast reconstruction: a prospec-

tive observational study. BMC Cancer 2010;10:171.

57. Heneghan HM, et al. Quality of life after immediate breast reconstruc-

tion and skin-sparing mastectomy e a comparison with patients under-

going breast conserving surgery. European Journal of Surgical

Oncology: the Journal of the European Society of Surgical Oncology

and the British Association of Surgical Oncology 2011;37(11):937–43.

58. Spear SL, Baker Jr JL. Classification of capsular contracture after

prosthetic breast reconstruction. Plastic and Reconstructive Surgery

1995;96(5):1119–23. [discussion 1124].

59. QUEST A, T., http://www.controlled-trials.com/ISRCTN38846532/.

60. QUEST B, T. http://www.controlled-trials.com/ISRCTN92581226/.

61. Greenway RM, Schlossberg L, Dooley WC. Fifteen-year series of

skin-sparing mastectomy for stage 0 to 2 breast cancer. American

Journal of Surgery 2005;190(6):918–22.

62. Kroll SS, et al. Local recurrence risk after skin-sparing and conven-

tional mastectomy: a 6-year follow-up. Plastic and Reconstructive

Surgery 1999;104(2):421–5.

63. Kroll SS, et al. Risk of recurrence after treatment of early breast can-

cer with skin-sparing mastectomy. Annals of Surgical Oncology 1997;

4(3):193–7.

64. Newman LA, et al. Presentation, treatment, and outcome of local re-

currence afterskin-sparing mastectomy and immediate breast recon-

struction. Annals of Surgical Oncology 1998;5(7):620–6.

65. Medina-Franco H, et al. Factors associated with local recurrence after

skin-sparing mastectomy and immediate breast reconstruction for in-

vasive breast cancer. Annals of Surgery 2002;235(6):814–9.

66. Drucker-Zertuche M, Robles-Vidal C. A 7 year experience with imme-

diate breast reconstruction after skin sparing mastectomy for cancer.

European Journal of Surgical Oncology: the Journal of the European

Society of Surgical Oncology and the British Association of Surgical

Oncology 2007;33(2):140–6.

67. Vaughan A, et al. Scientific presentation award. Patterns of local breast

cancer recurrence after skin-sparing mastectomy and immediate breast

reconstruction. American Journal of Surgery 2007;194(4):438–43.

68. Horiguchi J, et al. A comparative study of subcutaneous mastectomy

with radical mastectomy. Anticancer Research 2001;21(4B):2963–7.

69. Gerber B, et al. The oncological safety of skin sparing mastectomy

with conservation of the nipple-areola complex and autologous recon-

struction: an extended follow-up study. Annals of Surgery 2009;

249(3):461–8.

328 A. Agrawal et al. / EJSO 39 (2013) 320e328

70. Simmons RM, et al. Local and distant recurrence rates in skin-sparing

mastectomies compared with non-skin-sparing mastectomies. Annals

of Surgical Oncology 1999;6(7):676–81.

71. Ueda S, et al. Cosmetic outcome and patient satisfaction after skin-

sparing mastectomy for breast cancer with immediate reconstruction

of the breast. Surgery 2008;143(3):414–25.

72. Kinoshita S, et al. Retrospective comparison of non-skin-sparing mas-

tectomy and skin-sparing mastectomy with immediate breast recon-

struction. International Journal of Surgical Oncology 2011;2011:

876520.

73. PeledAW, et al. Outcomes after total skin-sparingmastectomy and imme-

diate reconstruction in 657 breasts. Annals of Surgical Oncology 2012;

19(11):3402–9.

74. Sheikh F, et al. Inadequate margins of excision when undergoing mas-

tectomy for breast cancer: which patients are at risk? Annals of Surgi-

cal Oncology 2011;18(4):952–6.

75. Carlson GW, et al. The use of skin sparing mastectomy in the treat-

ment of breast cancer: the Emory experience. Surgical Oncology

2003;12(4):265–9.

76. Carlson GW, et al. Skin-sparing mastectomy. Oncologic and recon-

structive considerations. Annals of Surgery 1997;225(5):570–5. [dis-

cussion 575e8].

77. Carlson GW, et al. Local recurrence of ductal carcinoma in situ after

skin-sparing mastectomy. Journal of the American College of Sur-

geons 2007;204(5):1074–8. [discussion 1078e80].

78. Spear SL, et al. Nipple-sparing mastectomy. Plastic and Reconstruc-

tive Surgery 2009;123(6):1665–73.

79. Jensen JA. Nipple-sparing mastectomy: what is the best evidence for

safety? Plastic and Reconstructive Surgery 2012;124(6):2195–7.

80. Lohsiriwat V, et al. Do clinicopathological features of the cancer pa-

tient relate with nipple areolar complex necrosis in nipple-sparing

mastectomy? Annals of Surgical Oncology 2012; Oct 16. [Epub ahead

of print].

81. Algaithy ZK, et al. Nipple sparing mastectomy: can we predict the

factors predisposing to necrosis? European Journal of Surgical

Oncology: the Journal of the European Society of Surgical Oncol-

ogy and the British Association of Surgical Oncology 2012;38(2):

125–9.