Original article

Oncoplastic surgery for breast cancer based on tumour location and a quadrant-per-quadrant atlas
K. B. Clough1 , T. Ihrai1,2 , S. Oden1 , G. Kaufman1 , E. Massey1 and C. Nos1
1 The Paris Breast Centre LInstitut du Sein, Paris, and 2 Breast Cancer Unit, Centre Antoine Lacassagne, Nice, France Correspondence to: Dr K. B. Clough, The Paris Breast Centre LInstitut du Sein, 7 Avenue Bugeaud, 75116 Paris, France (e-mail: krishna.clough@orange.fr)

Background: The majority of published techniques for oncoplastic surgery rely on an inverted-T

mammoplasty, independent of tumour location. These techniques, although useful, cannot be adapted to all situations. A quadrant-per-quadrant atlas of mammoplasty techniques for large breast cancers was developed in order to offer breast surgeons a technique dependent on tumour location, which reduces the 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 quadrantspecic oncoplastic techniques. All complications and any delay to adjuvant treatment were recorded prospectively, along with local and distant cancer recurrences. Cosmetic outcome was evaluated using a ve-point scale. Results: A total of 175 patients were analysed. The median tumour size, after histological examination, was 25 (range 490) mm. Twenty-three patients (131 per cent) had involved margins. Seventeen of these patients were treated by mastectomy and three had a re-excision. Complications occurred in 13 patients (74 per cent), which led to a delay to adjuvant treatment in three (17 per cent). After a median follow-up of 49 (range 2396) months, three patients had developed a local recurrence. The mean score after cosmetic evaluation was 46 of 5. Conclusion: A quadrant-per-quadrant approach to oncoplastic techniques for breast cancer was developed that tailors the mammoplasty for each tumour location. This panel of techniques should be a useful guide for breast surgeons, and extends the possibilities for breast conservation for large or poorly limited cancers, with a low complication rate and good cosmetic results.
Paper accepted 11 June 2012 Published online in Wiley Online Library (www.bjs.co.uk). DOI: 10.1002/bjs.8877

Introduction

For decades women with breast cancer were offered two surgical options: small lesions were treated with lumpectomy and radiotherapy (breast-conserving therapy, BCT), and large tumours by mastectomy. Oncoplastic surgery emerged as an additional surgical strategy 20 years ago1,2 . The objective was to allow oncologically safe breast conservation, by performing a wide excision for large or poorly located tumours, while limiting the risk of postoperative deformities. Most publications suggest that there is a major risk of deformity after standard BCT when more than 20 per cent of the breast volume is excised3 . In this setting, simple reshaping methods are not appropriate and more complex techniques are required, hence the growing use of oncoplastic surgery.
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The plastic surgery techniques transferred to the eld of breast cancer were initially based on inverted-T mammoplasty1,2 . They were designed for central or lowerpole cancers and are not well adapted to all tumour locations. However, the majority of breast surgeons performing oncoplastic surgery still use inverted-T mammoplasty techniques, irrespective of tumour location. A wide excision in the inner or outer quadrants of the breast can require complex reshaping. Filling of the excision cavity relies on a glandular ap and is not easily achieved with an inverted-T mammoplasty. A quadrant-per-quadrant atlas was designed by developing different mammoplasty techniques based on a direct approach to the tumour4 . The incision is integrated into a specic mammoplasty resection pattern, which is different for each quadrant of the breast. This approach avoids the
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K. B. Clough, T. Ihrai, S. Oden, G. Kaufman, E. Massey and C. Nos

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

Methods

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

Table 1

Oncoplastic surgery levels of the breast

Oncoplastic surgery level 1

Description Less than 20% of breast volume excised No skin excison required No mammoplasty required Anticipation of 2050% breast volume excision Excision of excess skin required to reshape breast Based on mammoplasty techniques

2010 were included in the study. In the present classication of oncoplastic techniques (Table 1)4 , level 2 techniques are those required when the surgeon anticipates a breast volume resection of more than 20 per cent. The breast reshaping is then performed by a mammoplasty technique with skin excision and nippleareola recentralization. All patients had been discussed previously by a multidisciplinary team to dene the optimal treatment. Patient selection was based on preoperative clinical and radiological evaluation of the ratio between the planned excision volume and the breast volume. Some patients may have had multiple reasons for oncoplastic surgery. Contralateral surgery for breast symmetry was considered at the initial assessment and offered to patients undergoing a large-volume resection that might result in a size discrepancy. Risk factors for complications such as fatty breasts, smoking, obesity or diabetes were recorded prospectively for each patient.

Mammoplasty techniques
Selection of technique was based on tumour location using the 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

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is served by a specic mammoplasty, rather than a onetechnique-ts-all inverted-T technique. Starting in the upper pole of the left breast and working clockwise, the individual techniques are described, except for the most commonly used inverted-T mammoplasty.

is centralized into its optimal position after superomedial de-epithelialization.

Tumours of the upper pole: 11 to 1 oclock An inferior pedicle mammoplasty, via an inverted-T incision5 , is the most appropriate method. A round block technique6 is a suitable alternative to the inferior pedicle. Tumours of the upper outer quadrant: 1 to 3 oclock A lateral mammoplasty technique7 is used. A large portion of the upper outer quadrant can be removed by a direct approach, excising the skin overlying the tumour, with two oblique incisions from the nippleareola complex (NAC) towards the axilla, similar to a quadrantectomy. The parenchymal excision roughly follows the skin excision, but can be extended in any direction. Breast reshaping is performed by undermining the remaining lateral and central gland from the pectoralis major muscle, without detaching it from the skin, in order to maintain good vascularization. Complete detachment of the retroareolar gland from the NAC enables mobilization of the central gland for volume redistribution. The glandular aps are then sutured into the cavity. The NAC is displaced medially in its optimal position, at the centre of the new breast mound. A periareolar crescent of skin is de-epithelialized to allow NAC centralization. This lateral mammoplasty results in a long radial scar over the original tumour site with a periareolar extension. Tumours of the lower outer quadrant: 3 to 5 oclock The J mammoplasty, originally described by Elbaz8 for breast reduction, is suitable in this area. As for all lower-pole excisions, the NAC is carried on a deepithelialized superior pedicle. This J mammoplasty is similar to the lateral mammoplasty technique for upper outer quadrant cancers, but the incision starts at the mediolateral edge of the de-epithelialized periareolar area, and then extends downwards to the inframammary crease. A more medial incision follows a similar pattern, joining the rst incision in the inframammary crease. The parenchymal excision follows the skin pattern in the shape of a J for the right breast and a reversed J for the left breast. The retroareolar gland is then detached from the NAC, and the three glandular aps (central, lateral and medial) can be mobilized into the excision cavity to achieve an equitable redistribution of the remaining breast volume. The NAC
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Tumours of the lower pole: 5 to 7 oclock The inverted-T mammoplasty with a superior pedicle is the technique of choice for tumours of the lower pole, as described previously9 . Tumours of the lower inner quadrant: 7 to 9 oclock The inverted-T mammoplasty may also be used in this location. However, inverted-T techniques are better suited to lower-pole tumours located immediately beneath the skin resection of the Wise pattern. The lower inner quadrant V mammoplasty is more suitable for breast tumours at this location. The procedure involves excising a pyramidal section of gland, with its base located in the submammary fold and apex at the border of the areola. The section is removed, including the skin attached to the gland down to the pectoralis fascia. The submammary fold is then incised, from the resection site to the anterior axillary line to allow adequate rotation of the remaining gland into the defect. The lower pole of the breast is entirely undermined from the pectoralis muscle and transferred medially to ll the defect. The NAC is then recentralized on a de-epithelialized superolateral pedicle. Tumours of the upper inner quadrant: 9 to 11 oclock The batwing technique for tumours in the upper inner quadrant was rst described by Anderson and colleagues10 . However, this technique does not allow the excision of more than 20 per cent of breast volume. A round block mammoplasty is also suitable for tumours at this location. Outcome analysis
In all patients the cavity was clipped to enable postoperative localization of the original tumour bed. Histological specimens were analysed with particular reference to involved surgical margins. All patients were followed up regularly after surgery, at 4-month intervals for 5 years and then twice yearly for a further 5 years. All complications and any delay to adjuvant treatment were recorded prospectively, as well as local and distant cancer recurrences. The cosmetic outcome was evaluated systematically by the surgeon during postoperative followup, and photographs were reviewed by a panel of three observers. The cosmetic result was rated on a ve-point scale (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 2 test, and
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K. B. Clough, T. Ihrai, S. Oden, G. Kaufman, E. Massey and C. Nos

Table 2

Indications for level 2 oncoplastic techniques

No. of patients (n = 175)

Tumour size Poor tumour limitation Involved margins after lumpectomy Neoadjuvant treatment Localization of tumour Breast asymmetry Multifocal cancer Skin retraction or skin invasion by cancer Other

94 (537) 35 (200) 23 (131) 39 (223) 43 (246) 9 (51) 27 (154) 34 (194) 7 (40)

Values in parentheses are percentages.

ordinal values with the KruskalWallis test. P < 0050 was considered statistically signicant. Statistical analysis was done using Stata version 10 (StataCorp LP, College Station, Texas, USA).
Results

A total of 175 patients had level 2 oncoplastic surgery between 2005 and 2010. Indications for use of a level 2 technique are shown in Table 2. The median age of the patients was 58 (3180) years. The median preoperative clinical tumour size was 25 (1080) mm. Thirty-eight patients had preoperative chemotherapy to downsize the tumour and allow breast conservation. One hundred and sixteen patients had invasive ductal carcinomas, 25 had invasive lobular carcinomas and 32 had ductal carcinoma in situ (DCIS). Tumours in the remaining two patients had rare histological subtypes (1 cystic adenoid carcinoma, 1 phyllodes). The median weight of the resection specimen was 125 (17680) g. Median tumour size at histological examination was 25 (490) mm: 30 mm for DCIS, 26 mm for invasive lobular carcinoma and 21 mm for invasive ductal carcinoma.

The margins were involved with cancer in 23 patients (131 per cent). The rate of involved margins was strongly associated with the histological subtype: nine (78 per cent) of 116 patients with invasive ductal carcinomas, four (16 per cent) of 25 with invasive lobular carcinomas and ten (31 per cent) of 32 with DCIS had involved margins (P = 0025). Of the 23 patients with involved margins, 17 were treated by mastectomy and three required a local re-excision. After multidisciplinary discussion, the three remaining patients were not reoperated on as they had minor margin involvement, and favourable histopathological prognostic factors and age. All patients had postoperative breast irradiation. Thirty-eight patients with invasive carcinomas received neoadjuvant or adjuvant treatment, or both in the form of chemotherapy and/or hormone therapy. Complications occurred in 13 patients (74 per cent), which led to a delay in adjuvant treatment in three (17 per cent). The complications were predominantly infections (6 patients) and fat necrosis (5). Other complications included haematoma and areola slough. All complications were handled in the outpatient setting and no patient required reoperation. The median follow-up was 49 (2396) months. Three patients (17 per cent) developed an ipsilateral breast recurrence, four developed an axillary recurrence and 11 presented with distant metastasis. One patient died from breast cancer. A contralateral breast reduction was performed in 47 patients (269 per cent) for breast symmetry, during the initial oncoplastic surgery in 34 patients and as a secondary procedure in 13. A superior pedicle mammoplasty was performed in 32 patients. A higher rate of contralateral surgery was observed when the oncoplastic procedure relied on an inverted-T mammoplasty: 20 (48 per cent) of 42 versus 27 (203 per cent) of 133 patients for other techniques (P < 0001).

Fig. 2

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

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Cosmetic evaluation was available for 80 patients (457 per cent). The mean cosmetic score was 46. The cosmetic scores were 5 (very good) and 4 (good) in 68 patients (85 per cent) (Fig. 2; Figs S1 and S2, supporting information).
Discussion

Oncoplastic surgery offers an alternative to mastectomy for large or poorly located tumours. Although ideally suited for tumours located in the lower pole, invertedT mammoplasty is not suitable for all tumour locations. Oncoplastic surgery cannot be a one-technique-ts-all solution. A quadrant-per-quadrant atlas of oncoplastic techniques depending on the tumour location was developed, based on the experience of various mammoplasty techniques at the Paris Breast Centre. The excision defect was lled with adjacent breast tissue, allowing direct closure of the excision cavity followed by breast reshaping. The latissimus dorsi miniap is an alternative volume replacement technique12 14 . However, this ap is a major reconstructive option to be considered in the event of cancer recurrence after BCT and radiotherapy, and this tissue should therefore be conserved whenever possible. The quadrant-per-quadrant approach is based on an en bloc resection of the tumour and overlying skin. This avoids extensive subcutaneous undermining and always allows reshaping of the breast using the appropriate mammoplasty. One of the major concerns about BCT is the rate of involved margins (2040 per cent), leading to re-excision or mastectomy15 . In the present series, even though the median tumour size (25 mm) was larger than in most series of conservative surgery, only 131 per cent of patients had involved margins. The rate of positive margins was strongly associated with the histological subtype. This can be explained by the greater tumour size of DCIS compared with invasive carcinoma, but also by the fact that DCIS and invasive lobular carcinomas are, respectively, non-palpable and ill dened lesions. Despite the large resection volume, a more accurate preoperative tumour size assessment by radiographic imaging would probably make the resection more precise and decrease the risk of re-excision for such lesions16 . When re-excision was required, BCT was rarely performed, because the volume of the remaining breast would not allow further resection without major deformity. Although median follow-up in the present series is limited to 49 months, the quadrant-per-quadrant oncoplastic approach appeared to be oncologically safe.
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The observed local recurrence rate was 17 per cent. In a previously published series of 101 patients who had inverted-T mammoplasty for large lower-pole tumours with a median size of 32 mm, the local recurrence rate was 94 per cent at a median follow-up of 48 months9 . The present series reports an extension of oncoplastic procedures for tumours located in all quadrants of the breast. It conrms the ndings of the three main published series with long-term follow-up, which all demonstrated that oncoplastic surgery is a safe procedure for breast cancer treatment, and allows wide excision with a low rate of involved margins9,17 19 . Postoperative complications have a negative oncological impact by delaying adjuvant therapy. The complication rate in this study was low and only 17 per cent of the patients had their postoperative treatment delayed. This compares favourably with other oncoplastic series in which inverted-T techniques were applied to all quadrants, and complication rates ranged from 16 to 24 per cent20 22 . The complications observed in these studies could have been due to the use of inverted-T mammoplasty for all tumours, regardless of location. For tumours not located in the lower pole, the lumpectomy defect must be lled with a long dermoglandular ap, with a risk of glandular necrosis owing to insufcient blood supply, and delayed wound healing. All techniques of the quadrant-per-quadrant approach gave satisfactory cosmetic results. Oncoplastic techniques avoid breast deformities. Despite a smaller volume, the shape and the form of the breast is preserved. Most patients do not request, or require, further surgery for cosmesis. To date, no cosmetic sequelae have been observed despite the use of breast irradiation. The higher rate of contralateral surgery for breast symmetry following the inverted-T mammoplasty compared with other techniques was due to the larger resection volumes. Immediate contralateral breast reduction was proposed for patients with large resection volumes, which explains the low rate of delayed surgery for breast symmetry. The present surgical approach based on tumour location has some limitations. The techniques used mainly involve direct incisions. These scars are rarely conspicuous because they become less visible after radiotherapy; however, they are much longer than usual lumpectomy scars, and patients should be warned of this drawback. Level 2 oncoplastic surgery should be reserved for patients who cannot be treated with more limited excisions. Difculties in performing level 2 oncoplastic techniques constitute a limitation to the implementation of the quadrant-perquadrant atlas. However, training in these techniques can be acquired gradually in dedicated units.
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K. B. Clough, T. Ihrai, S. Oden, G. Kaufman, E. Massey and C. Nos

This study has conrmed that the techniques outlined in the quadrant-per-quadrant atlas of oncoplastic surgery techniques for breast cancer, based on a specic mammoplasty technique for each tumour location, are associated with a low reoperation rate and a low risk of delay to adjuvant therapy. Oncoplastic surgery techniques extend the possibilities of breast conservation for patients with large or poorly limited cancers, with good cosmetic results.
Disclosure

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The authors declare no conict 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 (Word document) Please note: John Wiley & Sons Ltd is not responsible for the functionality of any supporting materials supplied by the authors. Any queries (other than missing material) should be directed to the corresponding author for the article.

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