clough k oncoplasty bjs

Original article

Oncoplastic surgery for breast cancer based on tumourlocation and a quadrant-per-quadrant atlas

K. B. Clough1, T. Ihrai1,2, S. Oden1, G. Kaufman1, E. Massey1 and C. Nos1

1The Paris Breast Centre – L’Institut du Sein, Paris, and 2Breast Cancer Unit, Centre Antoine Lacassagne, Nice, FranceCorrespondence to: Dr K. B. Clough, The Paris Breast Centre – L’Institut du Sein, 7 Avenue Bugeaud, 75116 Paris, France(e-mail: [email protected])

Background: The majority of published techniques for oncoplastic surgery rely on an inverted-Tmammoplasty, independent of tumour location. These techniques, although useful, cannot be adaptedto all situations. A quadrant-per-quadrant atlas of mammoplasty techniques for large breast cancers wasdeveloped in order to offer breast surgeons a technique dependent on tumour location, which reducesthe risk of postoperative complications and delay to adjuvant therapy.Methods: From 2005 to 2010, a series of eligible women with breast cancer were treated by quadrant-specific oncoplastic techniques. All complications and any delay to adjuvant treatment were recordedprospectively, along with local and distant cancer recurrences. Cosmetic outcome was evaluated using afive-point scale.Results: A total of 175 patients were analysed. The median tumour size, after histological examination,was 25 (range 4–90) mm. Twenty-three patients (13·1 per cent) had involved margins. Seventeen ofthese patients were treated by mastectomy and three had a re-excision. Complications occurred in 13patients (7·4 per cent), which led to a delay to adjuvant treatment in three (1·7 per cent). After a medianfollow-up of 49 (range 23–96) months, three patients had developed a local recurrence. The mean scoreafter cosmetic evaluation was 4·6 of 5.Conclusion: A quadrant-per-quadrant approach to oncoplastic techniques for breast cancer wasdeveloped that tailors the mammoplasty for each tumour location. This panel of techniques shouldbe a useful guide for breast surgeons, and extends the possibilities for breast conservation for large orpoorly limited cancers, with a low complication rate and good cosmetic results.

Paper accepted 11 June 2012Published online in Wiley Online Library (www.bjs.co.uk). DOI: 10.1002/bjs.8877

Introduction

For decades women with breast cancer were offered twosurgical options: small lesions were treated with lumpec-tomy and radiotherapy (breast-conserving therapy, BCT),and large tumours by mastectomy. Oncoplastic surgeryemerged as an additional surgical strategy 20 years ago1,2.The objective was to allow oncologically safe breast con-servation, by performing a wide excision for large or poorlylocated tumours, while limiting the risk of postoperativedeformities. Most publications suggest that there is a majorrisk of deformity after standard BCT when more than20 per cent of the breast volume is excised3. In this setting,simple reshaping methods are not appropriate and morecomplex techniques are required, hence the growing use ofoncoplastic surgery.

The plastic surgery techniques transferred to thefield of breast cancer were initially based on inverted-Tmammoplasty1,2. They were designed for central or lower-pole cancers and are not well adapted to all tumour loca-tions. However, the majority of breast surgeons performingoncoplastic surgery still use inverted-T mammoplasty tech-niques, irrespective of tumour location. A wide excision inthe inner or outer quadrants of the breast can requirecomplex reshaping. Filling of the excision cavity relies on aglandular flap and is not easily achieved with an inverted-Tmammoplasty.

A quadrant-per-quadrant atlas was designed by devel-oping different mammoplasty techniques based on a directapproach to the tumour4. The incision is integrated into aspecific mammoplasty resection pattern, which is differentfor each quadrant of the breast. This approach avoids the

2012 British Journal of Surgery Society Ltd British Journal of Surgery 2012; 99: 1389–1395Published by John Wiley & Sons Ltd

1390 K. B. Clough, T. Ihrai, S. Oden, G. Kaufman, E. Massey and C. Nos

use of long glandular flaps to fill in large excision cavities,as these flaps might induce fat and glandular necrosis andlead to complications that could delay adjuvant treatment.The strategy was applied to a consecutive series of womenwith breast cancer who required mammoplasty.

Methods

Women with breast cancer treated at the Paris Breast Cen-tre by level 2 oncoplastic surgery techniques from 2005 to

Table 1 Oncoplastic surgery levels of the breast

Oncoplasticsurgery level Description

1 Less than 20% of breast volume excisedNo skin excison requiredNo mammoplasty required

2 Anticipation of 20–50% breast volume excisionExcision of excess skin required to reshape breastBased on mammoplasty techniques

2010 were included in the study. In the present classifica-tion of oncoplastic techniques (Table 1)4, level 2 techniquesare those required when the surgeon anticipates a breastvolume resection of more than 20 per cent. The breastreshaping is then performed by a mammoplasty techniquewith skin excision and nipple–areola recentralization. Allpatients had been discussed previously by a multidisci-plinary team to define the optimal treatment. Patient selec-tion was based on preoperative clinical and radiologicalevaluation of the ratio between the planned excision volumeand the breast volume. Some patients may have had multi-ple reasons for oncoplastic surgery. Contralateral surgeryfor breast symmetry was considered at the initial assessmentand offered to patients undergoing a large-volume resec-tion that might result in a size discrepancy. Risk factorsfor complications such as fatty breasts, smoking, obesity ordiabetes were recorded prospectively for each patient.

Mammoplasty techniques

Selection of technique was based on tumour location usingthe quadrant-per-quadrant atlas (Fig. 1)4. Each location

Upper quadrant junction:inferior pedicle mammoplasty

Upper inner quadrant:round block or

batwing technique

Upper outer quadrant:lateral mammoplasty

Lower inner quadrant:V mammoplasty

Lower outer quadrant:J mammoplasty

Lower quadrant junction:superior pedicle mammoplasty

Fig. 1 Quadrant-per-quadrant atlas of oncoplastic techniques for breast cancer

2012 British Journal of Surgery Society Ltd www.bjs.co.uk British Journal of Surgery 2012; 99: 1389–1395Published by John Wiley & Sons Ltd

Oncoplastic surgery for breast cancer 1391

is served by a specific mammoplasty, rather than a ‘one-technique-fits-all’ inverted-T technique. Starting in theupper pole of the left breast and working clockwise, theindividual techniques are described, except for the mostcommonly used inverted-T mammoplasty.

Tumours of the upper pole: 11 to 1 o’clockAn inferior pedicle mammoplasty, via an inverted-Tincision5, is the most appropriate method. A round blocktechnique6 is a suitable alternative to the inferior pedicle.

Tumours of the upper outer quadrant: 1 to 3 o’clockA lateral mammoplasty technique7 is used. A large portionof the upper outer quadrant can be removed by a directapproach, excising the skin overlying the tumour, withtwo oblique incisions from the nipple–areola complex(NAC) towards the axilla, similar to a quadrantectomy.The parenchymal excision roughly follows the skinexcision, but can be extended in any direction. Breastreshaping is performed by undermining the remaininglateral and central gland from the pectoralis majormuscle, without detaching it from the skin, in order tomaintain good vascularization. Complete detachment ofthe retroareolar gland from the NAC enables mobilizationof the central gland for volume redistribution. Theglandular flaps are then sutured into the cavity. TheNAC is displaced medially in its optimal position, atthe centre of the new breast mound. A periareolarcrescent of skin is de-epithelialized to allow NACcentralization. This lateral mammoplasty results in a longradial scar over the original tumour site with a periareolarextension.

Tumours of the lower outer quadrant: 3 to 5 o’clockThe J mammoplasty, originally described by Elbaz8

for breast reduction, is suitable in this area. As forall lower-pole excisions, the NAC is carried on a de-epithelialized superior pedicle. This J mammoplasty issimilar to the lateral mammoplasty technique for upperouter quadrant cancers, but the incision starts at themediolateral edge of the de-epithelialized periareolararea, and then extends downwards to the inframammarycrease. A more medial incision follows a similar pattern,joining the first incision in the inframammary crease.The parenchymal excision follows the skin patternin the shape of a J for the right breast and areversed J for the left breast. The retroareolar glandis then detached from the NAC, and the threeglandular flaps (central, lateral and medial) can bemobilized into the excision cavity to achieve an equitableredistribution of the remaining breast volume. The NAC

is centralized into its optimal position after superomedialde-epithelialization.

Tumours of the lower pole: 5 to 7 o’clockThe inverted-T mammoplasty with a superior pedicle isthe technique of choice for tumours of the lower pole, asdescribed previously9.

Tumours of the lower inner quadrant: 7 to 9 o’clockThe inverted-T mammoplasty may also be used in thislocation. However, inverted-T techniques are better suitedto lower-pole tumours located immediately beneath theskin resection of the Wise pattern. The lower innerquadrant V mammoplasty is more suitable for breasttumours at this location. The procedure involves excisinga pyramidal section of gland, with its base located in thesubmammary fold and apex at the border of the areola. Thesection is removed, including the skin attached to the glanddown to the pectoralis fascia. The submammary fold isthen incised, from the resection site to the anterior axillaryline to allow adequate rotation of the remaining glandinto the defect. The lower pole of the breast is entirelyundermined from the pectoralis muscle and transferredmedially to fill the defect. The NAC is then recentralizedon a de-epithelialized superolateral pedicle.

Tumours of the upper inner quadrant: 9 to 11 o’clockThe batwing technique for tumours in the upper innerquadrant was first described by Anderson and colleagues10.However, this technique does not allow the excision ofmore than 20 per cent of breast volume. A round blockmammoplasty is also suitable for tumours at this location.

Outcome analysis

In all patients the cavity was clipped to enable postoperativelocalization of the original tumour bed. Histologicalspecimens were analysed with particular reference toinvolved surgical margins. All patients were followedup regularly after surgery, at 4-month intervals for5 years and then twice yearly for a further 5 years.All complications and any delay to adjuvant treatmentwere recorded prospectively, as well as local and distantcancer recurrences. The cosmetic outcome was evaluatedsystematically by the surgeon during postoperative follow-up, and photographs were reviewed by a panel of threeobservers. The cosmetic result was rated on a five-pointscale (excellent, 5; good, 4; fair, 3; poor, 2; bad, 1)11.

Statistical analysis

Continuous variables data are presented as median (range).Nominal values were compared using the χ2 test, and



Table 2 Indications for level 2 oncoplastic techniques

No. of patients (n = 175)

Tumour size 94 (53·7)Poor tumour limitation 35 (20·0)Involved margins after lumpectomy 23 (13·1)Neoadjuvant treatment 39 (22·3)Localization of tumour 43 (24·6)Breast asymmetry 9 (5·1)Multifocal cancer 27 (15·4)Skin retraction or skin invasion by cancer 34 (19·4)Other 7 (4·0)

Values in parentheses are percentages.

ordinal values with the Kruskal–Wallis test. P < 0·050was considered statistically significant. Statistical analysiswas done using Stata version 10 (StataCorp LP, CollegeStation, Texas, USA).

Results

A total of 175 patients had level 2 oncoplastic surgerybetween 2005 and 2010. Indications for use of a level 2technique are shown in Table 2. The median age of thepatients was 58 (31–80) years. The median preoperativeclinical tumour size was 25 (10–80) mm. Thirty-eightpatients had preoperative chemotherapy to downsize thetumour and allow breast conservation.

One hundred and sixteen patients had invasive ductalcarcinomas, 25 had invasive lobular carcinomas and 32 hadductal carcinoma in situ (DCIS). Tumours in the remainingtwo patients had rare histological subtypes (1 cystic adenoidcarcinoma, 1 phyllodes). The median weight of the resec-tion specimen was 125 (17–680) g. Median tumour sizeat histological examination was 25 (4–90) mm: 30 mm forDCIS, 26 mm for invasive lobular carcinoma and 21 mmfor invasive ductal carcinoma.

The margins were involved with cancer in 23 patients(13·1 per cent). The rate of involved margins was stronglyassociated with the histological subtype: nine (7·8 per cent)of 116 patients with invasive ductal carcinomas, four(16 per cent) of 25 with invasive lobular carcinomas andten (31 per cent) of 32 with DCIS had involved margins(P = 0·025). Of the 23 patients with involved margins, 17were treated by mastectomy and three required a localre-excision. After multidisciplinary discussion, the threeremaining patients were not reoperated on as they hadminor margin involvement, and favourable histopatholog-ical prognostic factors and age. All patients had postoper-ative breast irradiation. Thirty-eight patients with invasivecarcinomas received neoadjuvant or adjuvant treatment, orboth in the form of chemotherapy and/or hormone therapy.

Complications occurred in 13 patients (7·4 per cent),which led to a delay in adjuvant treatment in three(1·7 per cent). The complications were predominantlyinfections (6 patients) and fat necrosis (5). Other com-plications included haematoma and areola slough. Allcomplications were handled in the outpatient setting andno patient required reoperation.

The median follow-up was 49 (23–96) months. Threepatients (1·7 per cent) developed an ipsilateral breast recur-rence, four developed an axillary recurrence and 11 pre-sented with distant metastasis. One patient died from breastcancer.

A contralateral breast reduction was performed in 47patients (26·9 per cent) for breast symmetry, during theinitial oncoplastic surgery in 34 patients and as a sec-ondary procedure in 13. A superior pedicle mammoplastywas performed in 32 patients. A higher rate of contralat-eral surgery was observed when the oncoplastic procedurerelied on an inverted-T mammoplasty: 20 (48 per cent)of 42 versus 27 (20·3 per cent) of 133 patients for othertechniques (P < 0·001).

Fig. 2 V mammoplasty for a 40-mm carcinoma of the lower inner quadrant of the left breast



Cosmetic evaluation was available for 80 patients(45·7 per cent). The mean cosmetic score was 4·6. Thecosmetic scores were 5 (very good) and 4 (good) in 68patients (85 per cent) (Fig. 2; Figs S1 and S2, supportinginformation).

Discussion

Oncoplastic surgery offers an alternative to mastectomyfor large or poorly located tumours. Although ideallysuited for tumours located in the lower pole, inverted-T mammoplasty is not suitable for all tumour locations.Oncoplastic surgery cannot be a ‘one-technique-fits-all’solution. A quadrant-per-quadrant atlas of oncoplastictechniques depending on the tumour location was devel-oped, based on the experience of various mammoplastytechniques at the Paris Breast Centre. The excisiondefect was filled with adjacent breast tissue, allowingdirect closure of the excision cavity followed by breastreshaping.

The latissimus dorsi miniflap is an alternative volumereplacement technique12–14. However, this flap is a majorreconstructive option to be considered in the event ofcancer recurrence after BCT and radiotherapy, and thistissue should therefore be conserved whenever possible.The quadrant-per-quadrant approach is based on an enbloc resection of the tumour and overlying skin. Thisavoids extensive subcutaneous undermining and alwaysallows reshaping of the breast using the appropriatemammoplasty.

One of the major concerns about BCT is the rate ofinvolved margins (20–40 per cent), leading to re-excisionor mastectomy15. In the present series, even though themedian tumour size (25 mm) was larger than in most seriesof conservative surgery, only 13·1 per cent of patientshad involved margins. The rate of positive margins wasstrongly associated with the histological subtype. Thiscan be explained by the greater tumour size of DCIScompared with invasive carcinoma, but also by the fact thatDCIS and invasive lobular carcinomas are, respectively,non-palpable and ill defined lesions. Despite the largeresection volume, a more accurate preoperative tumoursize assessment by radiographic imaging would probablymake the resection more precise and decrease the riskof re-excision for such lesions16. When re-excision wasrequired, BCT was rarely performed, because the volumeof the remaining breast would not allow further resectionwithout major deformity.

Although median follow-up in the present seriesis limited to 49 months, the quadrant-per-quadrantoncoplastic approach appeared to be oncologically safe.

The observed local recurrence rate was 1·7 per cent. Ina previously published series of 101 patients who hadinverted-T mammoplasty for large lower-pole tumourswith a median size of 32 mm, the local recurrence ratewas 9·4 per cent at a median follow-up of 48 months9.The present series reports an extension of oncoplasticprocedures for tumours located in all quadrants of thebreast. It confirms the findings of the three main publishedseries with long-term follow-up, which all demonstratedthat oncoplastic surgery is a safe procedure for breastcancer treatment, and allows wide excision with a low rateof involved margins9,17–19.

Postoperative complications have a negative oncologicalimpact by delaying adjuvant therapy. The complicationrate in this study was low and only 1·7 per cent ofthe patients had their postoperative treatment delayed.This compares favourably with other oncoplastic seriesin which inverted-T techniques were applied to allquadrants, and complication rates ranged from 16 to24 per cent20–22. The complications observed in thesestudies could have been due to the use of inverted-Tmammoplasty for all tumours, regardless of location. Fortumours not located in the lower pole, the lumpectomydefect must be filled with a long dermoglandularflap, with a risk of glandular necrosis owing to insufficientblood supply, and delayed wound healing.

All techniques of the quadrant-per-quadrant approachgave satisfactory cosmetic results. Oncoplastic techniquesavoid breast deformities. Despite a smaller volume, theshape and the form of the breast is preserved. Most patientsdo not request, or require, further surgery for cosmesis. Todate, no cosmetic sequelae have been observed despite theuse of breast irradiation. The higher rate of contralateralsurgery for breast symmetry following the inverted-Tmammoplasty compared with other techniques was dueto the larger resection volumes. Immediate contralateralbreast reduction was proposed for patients with largeresection volumes, which explains the low rate of delayedsurgery for breast symmetry.

The present surgical approach based on tumour locationhas some limitations. The techniques used mainly involvedirect incisions. These scars are rarely conspicuous becausethey become less visible after radiotherapy; however,they are much longer than usual lumpectomy scars, andpatients should be warned of this drawback. Level 2oncoplastic surgery should be reserved for patients whocannot be treated with more limited excisions. Difficultiesin performing level 2 oncoplastic techniques constitutea limitation to the implementation of the quadrant-per-quadrant atlas. However, training in these techniques canbe acquired gradually in dedicated units.



This study has confirmed that the techniques outlinedin the quadrant-per-quadrant atlas of oncoplastic surgerytechniques for breast cancer, based on a specificmammoplasty technique for each tumour location, areassociated with a low reoperation rate and a low risk of delayto adjuvant therapy. Oncoplastic surgery techniques extendthe possibilities of breast conservation for patients withlarge or poorly limited cancers, with good cosmetic results.

Disclosure

The authors declare no conflict of interest.

References

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Supporting information

Additional supporting information may be found in the online version of this article:

Fig. S1 J mammoplasty for a carcinoma located in the lower outer quadrant (Word document)

Fig. S2 Lateral mammoplasty for a 35-mm carcinoma of the upper outer quadrant of the left breast (Worddocument)

Please note: John Wiley & Sons Ltd is not responsible for the functionality of any supporting materials suppliedby the authors. Any queries (other than missing material) should be directed to the corresponding author for thearticle.

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