Volume replacement and displacement techniques in oncoplastic surgery.

Introduction

Breast-conserving surgery (BCS) is now an established surgical modality and is the preferred standard of care for management of women with early-stage breast cancer. Longer-term follow-up data from several prospective randomised controlled trials and limited meta-analysis have demonstrated equivalent survival for BCS compared with radical mastectomy [1,2]. Introduction of conservative forms of breast surgery has coincided with instigation of widespread mammographic screening over the past 25 years. With a smaller average tumour size at presentation, the majority of patients are eligible for BCS though rates of mastectomy are variable at both institutional and geographical levels. Within the UK, rates of BCS vary from 5-70% with an average of 58% [3]. These variations in patterns of surgical management are likely to reflect differences in philosophy and training among surgeons together with an element of fear and concern about recurrence. Selection of patients for BCS is of crucial importance with an inverse relationship between the oncological demands for surgical radicality on the one hand and cosmesis on the other. There is a balance between the risk of local recurrence and cosmetic results and the newer techniques of oncoplastic surgery are advancing the limits of surgical resection. These present exciting prospects for preserving a cosmetically acceptable breast while satisfying oncological mandates.

Selection of patients for oncoplastic surgery

Most patients deemed eligible for BCS will have a favourable tumour to breast size ratio and be suitable for conventional forms of wide local excision in which the tumour is excised with an approximately 2-cm margin of surrounding breast tissue without any formal breast re-modelling. Though a re-excision may be required in up to one-quarter of cases to achieve microscopically clear radial resection margins (at least 2-3 mm), an optimal cosmetic outcome should be attainable in the longer term after radiotherapy to the breast in most cases. Conversely, mastectomy is clearly indicated in some patients on the basis of tumour size and/or location, multifocality or patient choice.

Between these two extremes is a 'grey area' in which the limits of BCS are being approached and the patient may be better served with a skin-sparing mastectomy and immediate breast reconstruction at the outset [4]. For these patients, there is a risk that the tumour cannot be adequately excised without cosmetic detriment. It becomes progressively more difficult to achieve a good cosmetic outcome as the proportion of breast tissue removed increases. Studies have shown that cosmetic results relate to both breast size and weight of the resected specimen. Though the absolute volume of tissue excised is dependent on the surgeon, a greater percentage excision is associated with larger tumours. When more than 10-20% of breast tissue is removed, there is a risk of an unsatisfactory cosmetic result. Relatively modest losses of 5-10% of breast volume from tumours in the medial and inferior quadrants can adversely affect cosmesis [5]. Cochrane and colleagues have validated a method for estimating the percentage of breast volume excised (EPBVE) from mammographic measurements together with the weight of the resected specimen (specific gravity of breast tissue approximately 1.00). The EPBVE was found to be a key determinant of cosmetic outcome and patient satisfaction following BCS [5]. Psychological adjustment following BCS correlates with cosmesis and results of BCS have hitherto failed to meet patient expectations in up to 30% of cases [6,7]. Oncoplastic techniques provide the opportunity for enhancing quality of life by improving cosmetic outcome and psychological well-being.

Oncoplastic procedures often permit wide resection of tissue which increases the chance of tumour-free margins. Furthermore, positive margins under these circumstances usually reflect extensive disease for which mastectomy (rather than re-excision) is indicated. It has been suggested that the chance of local relapse could be reduced by more aggressive approaches to BCS [8,9] but there are currently no data on longer-term follow-up of these oncoplastic procedures. Moreover, there is no information from clinical trials on the safety of BCS for invasive tumours in excess of 4 cm [10]. Though margin status and the presence or absence of an extensive in situ component are the principle determinants of local recurrence, consistent associations have been found for tumours >2 cm [11]. For node-positive patients, tumour size exceeding 5 cm was the only risk factor for local recurrence on multivariate analysis [12]. Therefore, it is likely that the risk of relapse would remain high for larger tumours despite adequate surgical clearance. Nonetheless, it may be possible to excise large areas of non-high-grade ductal carcinoma in situ (DCIS; >4 cm) with clear margins and partially reconstruct the breast with autologous tissue replacement. Age less than 35 years and family history of breast cancer are additional factors that must be considered when selecting patients for either oncoplastic surgery with a high EPBVE or skin-sparing mastectomy with whole-breast reconstruction (higher risk of local recurrence or de novo cancer risk). Though it may not be feasible in routine clinical practice to formally estimate the EPBVE from radiological measurements of tumour and breast size, magnetic resonance imaging assessment of all patients is advisable. This can confirm unifocality or exclude multifocal disease involving different quadrants. Where imaging is equivocal and tumour parameters are borderline for BCS, it may be preferable to undertake a two-stage procedure; initial 'wide' local excision of tumour permits full histopathological evaluation with assessment of margins. A definitive oncoplastic procedure can subsequently be carried out either 2-3 weeks later or following radiotherapy to the breast. A one-stage procedure is optimal and avoids any technical difficulties relating to the sequelae of previous surgery and radiotherapy (scarring, fibrosis). There are less likely to be problems with skin viability when completion mastectomy is undertaken after simple excision of tumour compared with a more complex oncoplastic procedure with parenchymal undermining and transposition.

There is a higher chance of wound infection and fat necrosis in patients who smoke, are obese (body mass index >30), have large breasts or are diabetic, and these potential complications and their effect on further oncological treatment should be fully discussed with the patient.

Techniques of oncoplastic surgery

Oncoplastic surgery in the context of partial breast reconstruction encompasses both volume replacement and volume displacement techniques. The former import additional tissue in the form of a flap and attempt to compensate for loss of volume from surgical ablation. By contrast, the latter rearrange the remaining breast tissue using methods of glandular advancement which serve to re-distribute the parenchyma and minimise the impact of wide local excision. In effect, the volume loss is absorbed over a wider area with concomitant re-shaping of the breast. Volume displacement surgery is less extensive than for autologous tissue transfer and there is no donor site morbidity. However, the reconstructed breast is of smaller overall volume and a symmetrisation procedure on the contralateral side is often required. This applies particularly to therapeutic mammoplasty where tumour excision is incorporated into a standard or modified reductional procedure.

Volume displacement represents the simplest option for partial breast reconstruction and is usually preferred over techniques for volume replacement which involve more extensive surgery with harvesting of a myocutaneous or subcutaneous flap. These flaps cannot subsequently be used for whole-breast reconstruction should the patient develop local recurrence and require mastectomy. Volume displacement techniques are only possible in patients with medium to large breasts, whereas replacement techniques are suited to small breasted women. The choice of method is determined by both the breast volume and the size of the surgical cavity for infill.

Volume replacement techniques

The majority of these techniques use the latissimus dorsi muscle which can be harvested as either a myocutaneous [13,14] or myosubcutaneous flap [15,16] (Table 1). The former incorporates an island of overlying skin which can be used to replace any excised breast cutis. Usually BCS does not involve resection of skin except for quadrantectomy and a latissimus dorsi flap is ideally suited to reconstruction following quadrantic resection of a tumour in the upper outer quadrant in which the parenchyma together with a narrow radial ellipse of skin has been removed. Noguchi and colleagues first described this method of partial breast reconstruction in 1990 in a series of Japanese women undergoing quadrantectomy for breast cancer [13]. Most of these cases involved a latissimus dorsi musculosubcutaneous flap which was partially mobilised through the quadrantectomy incision. The method for transposing the flap onto the anterior chest wall was adapted for medial and central defects by tunnelling the flap deep to the pectoralis muscle and delivering this at the base of the surgical cavity. The benefit of partial breast reconstruction with volume replacement in terms of both cosmesis and patient satisfaction was most evident for patients with small breasts. Three-quarters of these women were judged to have excellent cosmetic results on combined subjective and objective assessment compared to none of those with large breasts who underwent a similar method of volume replacement.

Rainsbury's group described a modified version of the latissimus dorsi (LD) musculosubcutaneous flap which is popularly known as the 'LD mini-flap' [15,16]. The LD muscle was harvested with a laterally placed lazy-S incision through which resection of breast and axillary tissue was simultaneously performed. No skin overlying the LD muscle was removed, though subcutaneous fat could be employed to enhance tissue bulk if necessary. The technique is best suited to tumours in the superior and central (2 cm deep to nipple) aspects of the breast (Figure 1a and b). Tumour bed biopsies with frozen section can reduce the chance of positive margins and permit immediate mastectomy if a second set of biopsies after routine cavity re-excision are also positive [16].

Dixon and colleagues incorporated the LD mini-flap into a two-stage procedure with a 'delayed-immediate' axillary dissection and partial breast reconstruction 5-10 days after initial tumour excision. Where re-excision was indicated, this was performed at the same time and the flap harvested through an extended axillary incision [17].

The volume of tissue within a typical latissimus dorsi musculosubcutaneous flap is usually sufficient for partial breast reconstruction, but adequate mobilisation is required to ensure there is an optimal length of muscle. It is generally difficult to use an LD flap for volume replacement within the inferior quadrants of the breast. There is no evidence for any significant atrophy with time and these radiolucent flaps do not interfere with follow-up imaging of the ipsilateral breast. Variants of this basic flap have been reported which aim to reduce muscle disruption and hence donor site morbidity [18]:

* thoraco-dorsal artery perforator (TDAP) flap--this pedicled flap harvests only the skin or subcutaneous fat overlying the LD muscle;

* intercostals artery perforator (ICAP) flap--the skin or fat overlying the lateral chest wall can alternatively be supported by the intercostals artery perforator vessels;

* muscle-sparing latissimus dorsi flap--this is mainly composed of subcutaneous adipose tissue.

[FIGURE 1 OMITTED]

Volume displacement techniques

Several options are available for volume displacement which constitutes a spectrum of techniques of varying complexity (Table 2) [19-23]. The common aim of volume displacement is to utilise the remaining breast tissue to fill the defect resulting from extirpation of the tumour. As previously discussed, resections which lead to loss of >10-20% of breast volume are likely to incur significant cosmetic detriment and to demand some form of 'infill' to create an acceptable cosmetic outcome in the longer term. Displacement techniques re-shape the breast through advancement, rotation or transposition of existing parenchyma and skin with a resultant decrease in overall breast volume.

Simple breast tissue mobilisation

The cosmetic outcome after removal of a relatively small volume of tissue can be enhanced by simple mobilisation of breast tissue adjacent to the surgical cavity. The extent of this mobilisation depends on the size of the defect and may involve undermining the whole breast plate (Figure 2). Extensive mobilisation of breast tissue can sometimes threaten the blood supply to both glandular tissue and skin. This can lead to post-operative necrosis and secondary sepsis or can compromise flap viability in the event of future mastectomy.

Local tissue flaps

Larger defects such as those resulting from quadrantectomy cannot be adequately filled by simple mobilisation and require creation of a formal flap of local breast tissue. Grisotti described an advancement rotation flap for filling a central defect after removal of the nipple-areola complex [24,25]. This is a dermatoglandula flap based on an inferior pedicle (Figure 3) and has a skin paddle which replaces the nipple-areola complex and can be used to fashion a new areola immediately. The tumour is excised together with the nipple-areola complex as a column of tissue from the subcutaneous layer to the pectoral fascia. A skin island is mobilised which will form the new nipple-areola complex and viability of the skin is maintained by creation of a dermatoglandular bridge based inferiorly and corresponding in width to the diameter of the skin disc. The neo-areola is formed by the skin island and the breast parenchyma fills the defect (nipple reconstruction is done as a delayed procedure). An interesting approach for parenchymal redistribution following removal of peri-areolar tumours which are not located in the retro-areolar region is the round block technique [26] (Figure 4). This involves mobilisation of the nipple-areola complex with formation of a zone of de-epithelialisation or 'corona' around the nipple-areola complex. Dissection is continued into the relevant quadrant with wide excision of the tumour. Glandular tissue around the defect is undermined to allow closure of the defect. The skin edges are sutured to the areola and the de-epithelialised zone is buried. This is a good example of how volume displacement techniques can 'absorb' the local defect over a wider area of breast substance [4].

[FIGURE 2 OMITTED]

[FIGURE 3 OMITTED]

Breast reduction techniques and therapeutic mammoplasty

Over the past decade, several reports have emerged describing integration of local tumour excision with a classical reduction mammoplasty procedure. Most of these cases involve patients with relatively large breasts and/or who desire smaller breasts and have a tumour located in the zone of resection for a conventional Wise pattern reduction mammoplasty [27-29]. This includes inferior pole tumours from the 3 to 9 o'clock positions together with tumours immediately above the nipple-areola complex in medium to large breasts. With appropriate patient selection, this epitome of oncoplastic surgery can permit wide tumour excision and yield excellent cosmetic results with maintenance of skin and nipple sensation. However, there are few rigorous studies evaluating either oncological or cosmetic outcomes. Clough and colleagues [30] reported the results of a series of 101 patients who underwent tumour excision as part of a reduction mammoplasty procedure. In more than three-quarters of patients, a superior pedicle technique was used and a contralateral matching procedure was required. Mean tumour size was more than 3 cm and there were positive margins in 11 cases which were managed with either mastectomy or a radiation boost to the tumour bed (no patients underwent re-excision to obtain clear margins). The actuarial 5-year local recurrence rate was 9.4%, and over 80% of patients had a 'fair to excellent' result at 5 years [30]. Similarly, favourable results have been reported by other surgeons, albeit with smaller numbers of patients [31,32]. Reduction mammoplasty can also be used for removal of small inferior quadrant tumours when a patient has large breasts but requests a smaller breast size (Figure 5a-c).

[FIGURE 4 OMITTED]

Against this background, the Nottingham group have recently championed the concept of 'therapeutic mammoplasty' (TM) in which a combination of reduction mammoplasty and radiotherapy is used to treat breast cancers deemed appropriate for BCS [33,34]. TM aims to improve cosmetic outcome when tumour size or location would otherwise lead to suboptimal cosmesis following conventional BCS. Though TM may permit BCS in some circumstances when mastectomy would otherwise have been indicated, it does not relax the strict oncological selection process for BCS. When the estimated risk for ipsilateral breast tumour recurrence is high, despite clear surgical margins and a good cosmetic result, mastectomy with immediate breast reconstruction should be offered. However, better cosmetic outcomes have been reported by patients undergoing partial breast reconstruction following BCS compared with mastectomy and whole-breast reconstruction [17].

[FIGURE 5 OMITTED]

TM techniques are being developed to encompass treatment of tumours which lie outside the excision site of a conventional reduction mammoplasty [33,34] (Figure 6a and b). As the local defect lies within the zone of the conserved tissue, modifications of the mammoplasty technique have evolved to fill the defect by either extension of the usual pedicle or creation of a secondary pedicle. Planning of skin incisions and appropriate orientation of the nipple-areola complex pedicle is essential for these mammoplasty techniques which demand understanding and experience of plastic surgery principles. Tumours that lie in zones inferior to the mammoplasty pillars can be excised with a classical Wise pattern reduction procedure. Those in the central and central/inferior zones are amenable to either a Wise pattern or a vertical type mammoplasty [35].

In a review of 50 consecutive cases of TM, McCulley and Macmillan reported cosmetic results to be good/excellent in 63% of cases, satisfactory in 33% and poor in 4% [36]. Tumour excision was incomplete in four cases of DCIS but all invasive carcinomas were adequately excised. In particular, no patients required re-excision and the four patients with DCIS had completion mastectomy. There were no deaths or recurrences recorded among this group of 50 TM patients at a mean follow-up of 13 months. Furthermore, no patients endured any delays in commencement of adjuvant therapy as a consequence of surgical complications [36] (Table 3).

[FIGURE 6 OMITTED]

It should be noted that a contralateral reduction is always required for TM and whenever there is uncertainty about completeness of tumour excision it is preferable to carry out a staged procedure with initial tumour excision and histopathological evaluation. A subsequent TM (and contralateral surgery) or mastectomy and whole-breast reconstruction can be undertaken. Patients will receive irradiation of the ipsilateral breast but not the contralateral side. This can potentially lead to some loss of symmetry.

The batwing and hemibatwing mammoplasty [37] (Figure 7) and crescentic excisions (Figure 8) are employed for tumours in the upper quadrants of the breast between 10 and 2 o'clock that lie relatively close to the nipple-areola complex and usually lie below the bra line. The degree of breast mobilisation and reduction is less than for a conventional Wise pattern mammoplasty, but tumours can be excised with an adequate margin and good cosmetic results. By contrast, tumours lying above the bra line are not suitable for formal mammoplasty procedures and should be managed with local tissue mobilisation and simple skin closure.

[FIGURE 7 OMITTED]

[FIGURE 8 OMITTED]

Informed consent

Both volume displacement and replacement techniques represent more complex and challenging surgery than standard wide local excision where a variable amount of breast tissue is removed, but no formal attempt is made to reconstruct the breast. Patients must be aware of the pattern of scarring which may be more extensive than anticipated for a reductional procedure. Moreover, patients must be informed of any need for surgery to the contralateral breast to achieve symmetrisation and the possibility of completion mastectomy in the event of incomplete tumour excision. The latter may be particularly traumatic after bilateral oncoplastic surgery and the patient will be faced with the prospect of whole-breast reconstruction. A woman may chose to have a normal-sized breast with a localised defect rather than a nicely shaped, but smaller breast with concomitant scarring and a contralateral breast reduction. Conversely, she may opt for a mastectomy with immediate breast reconstruction rather than an attempt at breast conservation with oncoplastic techniques in order to minimise any chances of recurrence or to avoid radiotherapy. Patients should be warned of possible delays to adjuvant treatment in the event of any complications and be made aware of fat necrosis which can give rise to a worrisome lump in the breast. Where volume replacement techniques are employed, significant donor site morbidity can occur with seroma formation and even wound dehiscence.

Conclusions

The development of oncoplastic surgery and partial breast reconstruction is a natural evolution in the application of BCS to management of breast cancer. Nonetheless, these techniques remain contentious and careful selection of patients is crucial. Partial breast reconstruction should not be attempted in patients who are not amenable to BCS from an oncological perspective and for whom mastectomy is warranted. Oncoplastic intervention can facilitate wide surgical clearance of a tumour and genuinely improve a patient's cosmetic outcome where larger resections are required. The techniques should be integrated with ablative breast surgery to avoid emergence of significant breast mutilation. However, they can be employed to correct deformities resulting from previous BCS combined with radiotherapy.

Alternatively, partial breast reconstruction can be done as a planned delayed procedure (before or after radiotherapy). Cross-speciality training opportunities are fostering increasing numbers of oncoplastic breast surgeons [38]; those surgeons without oncoplastic competencies should work cooperatively with plastic surgeons to provide a comprehensive service. Notwithstanding surgical expertise, these techniques are relevant to a limited proportion of patients and should only be offered in units managing large numbers of breast cancer patients [17].

The indications for formal volume replacement and displacement surgery in the context of BCS need clarification. Ongoing audit and evaluation will in time provide information on cosmetic results together with psychological and oncological outcomes which will guide patient selection and management.

References

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John R Benson and M Shamim Absar

Addenbrooke's Hospital, Cambridge, UK

Correspondence to: John R Benson, Cambridge Breast Unit, Addenbrooke's Hospital, Hills Road, Cambridge CB2 0QQ (email: [e-mail])

Table 1: Volume replacement techniques.

Procedure           Size of tumour    Site of tumour    Utility

Latissimus dorsi    Any conservable   Any, preferably   Good
myocutaneous flap   size              upper or lower
                                      outer quadrants

Latissimus dorsi    Any conservable   Any, preferably   Good
myosubcutaneous     size              upper or lower
miniflap                              outer quadrants

Lateral adipose     Any conservable   Lateral aspect,   Not clear
tissue flap         size              6-12 o'clock

Table 2: Volume displacement techniques.

Procedure               Size of     Site of        Opposite breast
                        tumour      tumour

Simple breast tissue    Small       Any            None
mobilisation

Extensive breast        Medium      Any            Minor adjustments/
mobilisation with                                  mastopexy
creation of new
breast mound

Round block (Benelli)   Small to    Peri-areolar   Minor nipple
                        medium                     position
                                                   adjustment

Reduction techniques

Batwing incision        Medium to   10 to 2        Minor adjustment/
                        large       o'clock        mastopexy

Hemi batwing            Medium to   10 to 2        Minor adjustment/
                        large       o'clock        mastopexy

Crescent incision       Medium to   4 to 8         Minor adjustment/
                        large       o'clock        mastopexy

Wise pattern            Medium to   3 to 9         Symmetrisation
reduction               large       o'clock        required

Central excision        Medium to   Central        Symmetrisation
reduction with          large       tumour         required
advancement of skin
glandular island on
inferior pedicle

Table 3: Common complications of therapeutic
mammoplasty.

Complication            Incidence (%)

Fat necrosis                  8
Infection                     6
Delayed wound healing         2