Nipple-sparing mastectomy: Where are we now?

Surgical Oncology (2008) 17, 261e266

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REVIEW

Nipple-sparing mastectomy: Where are we now? Alice P. Chung*, Virgilio Sacchini Breast Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY 10065, USA Accepted 7 March 2008

KEYWORDS Nipple-sparing mastectomy; Risk reduction; Nippleeareolar complex preservation

Abstract Surgical treatment of breast cancer has evolved from radical mastectomy with routine removal of the nippleeareolar complex (NAC) to breast conservative therapy with preservation of the breast and NAC. When breast conservation is not appropriate or the patient desires mastectomy for risk reduction, conventional therapy still consists of mastectomy with removal of the NAC, followed by reconstruction. Rising interest in improved cosmesis has led to the introduction of the skin-sparing and nipple-sparing mastectomy (NSM) as potential alternatives to mastectomy. There has been much controversy regarding the oncologic safety of these procedures, and the NSM has also introduced a set of complications, such as nipple and areolar necrosis, that are not a concern with total mastectomy. From our review of the literature, we feel that NSM may be a viable option in the appropriate setting, and that its risks and complications are acceptable when compared to the traditional surgical treatment of breast cancer. ª 2008 Elsevier Ltd. All rights reserved.

Contents Historical background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Oncologic safety . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Technique and complications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conflict of interest statement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

262 262 263 265 265 265

Abbreviations: NAC, nippleeareolar complex; NSM, nipple-sparing mastectomy; BCT, breast-conservation therapy; DCIS, ductal carcinoma in situ. * Corresponding author. Tel.: þ1 212 639 7608; fax: þ1 212 717 3214. E-mail address: [email protected] (A.P. Chung). 0960-7404/$ - see front matter ª 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.suronc.2008.03.004

262

Historical background The technique of subcutaneous mastectomy followed by reconstruction was first reported in 1962 by Freeman [1]. Indications for this procedure included severe cystic disease, unremitting mastodynia, chronic mastitis, parenchymal scarring from infection, trauma, or multiple biopsies, fibrous disease of the breast, positive family history of breast cancer, and proven malignancy of the breast. The technique involves division of Cooper’s ligaments while leaving ‘‘a minute amount of breast parenchyma attached to the dermis.’’ As this procedure became more widespread, the question of whether or not a thoroughly performed subcutaneous mastectomy was an effective means of providing prophylaxis in women at high risk for breast cancer arose. Pennisi and Capozzi [2] reported a 10-year follow-up of 1500 patients who underwent subcutaneous mastectomy for proliferative fibrocystic disease, macrocystic disease, or other high-risk factors. They found that only 0.4% of patients developed breast cancer after subcutaneous mastectomy. A more recent study by Hartmann et al. [3] looked at 693 women with a family history of breast cancer who had bilateral prophylactic mastectomy with a median follow-up of 14 years. Ninety percent of the procedures performed were subcutaneous mastectomies, and this was associated with a reduction in the incidence of breast cancer of at least 90%. Others [4,5] demonstrated that patients undergoing breast reduction surgery had a 28e39% decreased risk of breast cancer. Brinton et al. [6] substantiated these findings and also found that breast cancer risk in these patients was reduced in proportion to the amount of tissue removed. From this work it is evident that the greatest risk reduction is achieved by removal of as much breast tissue as possible. With increasing awareness of breast cancer risk, as well as the discovery of the BRCA mutation, there has been a rising interest in risk-reducing mastectomy as an acceptable alternative to breast cancer screening in high-risk patients. Although total mastectomy yields the greatest risk reduction, it can be disfiguring, especially in the absence of breast reconstruction. The skin-sparing mastectomy was introduced by Toth and Lappert in 1991 [7] as a variation to the mastectomy optimized for reconstruction. With this technique, the majority of the patient’s natural breast skin envelope is left in situ for reconstruction, allowing preservation of the inframammary fold and breast contour, and reducing the need for contralateral breast adjustment to achieve symmetry. The oncologic safety of this procedure has been questioned, and multiple studies have demonstrated the recurrence rate of skin-sparing mastectomy to be equivalent to modified radical mastectomy [8e13] (Table 1). Although the NAC is removed with this technique, nipple reconstruction can be performed with a skin graft and tattoo. However, multiple surgical procedures are frequently required to achieve an acceptable cosmetic outcome. Jabor and colleagues [14] reported a high level of dissatisfaction with nippleeareolar reconstructions, with only 16% of patients stating they had no desire to change their reconstruction. The remaining patients reported dissatisfaction, in decreasing order, with the nipple projection, color match, shape, size, texture, and position

A.P. Chung, V. Sacchini Table 1

Recurrence rate of skin-sparing mastectomy

Study

No. of SSM

Local recurrence (%)

Follow-up (month)

Newman et al. [8] Simmons et al. [9] Kroll et al. [10] Medina-Franco et al. [11] Spiegel and Butler [12] Carlson et al. [13]

372 77 114 176 177 565

6.2 3.9 7.0 4.5 5.6 5.5

26 60 72 73 118 65

SSM, skin-sparing mastectomy.

of their reconstructed NAC. NSM eliminates these factors as a source for discontent. The desire for continued improvements in cosmesis has largely been patient-driven, and these results have led to the investigation of the feasibility of NSM.

Oncologic safety Routine removal of the nipple in mastectomies has been performed based on the presumed risk of occult nipple involvement. Studies have shown that nipple involvement varies from 0 to 58% depending on the size of the primary breast tumor, location, multicentricity, lymph node positivity, and presence of an extensive intraductal component [15e23] (Table 2). Simmons et al. [22] found that occult nipple involvement occurred in 10.7% of mastectomy specimens. This number fell to 6.7% after excluding tumors that were centrally located, greater than 2 cm, and had two or more positive nodes. When the nipple and areola were analyzed separately, only 0.9% of patients had involvement of the areola. Vlajcic and colleagues [24] identified prognostic factors predictive of NAC involvement. According to their analysis, the NAC could be safely preserved with tumor size <2.5 cm and tumor-to-nipple distance >4 cm. A number of retrospective studies have examined the oncologic safety of the NSM using similar patient selection criteria [25e29] (Table 3). Gerber et al. [25] compared results of 112 patients with tumors more than 2 cm from the nipple who underwent NSM with 134 patients with similar stage who had modified radical mastectomy. In the

Table 2 2005

Nipple involvement variation by study, 1976e

Study

Year

No. of specimens

Nipple involvement (%)

Smith et al. [15] Parry et al. [16] Lagios et al. [17] Wertheim and Ozzello [18] Luttges et al. [19] Santini et al. [20] Laronga et al. [21] Simmons et al. [22] Sikand et al. [23]

1976 1977 1979 1980

541 200 149 1000

12.2 8 30 23

1987 1989 1999 2002 2005

166 1291 286 217 220

38 12 5.6 6.7 7

Nipple-sparing mastectomy

263

Table 3 Oncologic safety of nipple-sparing mastectomy in studies with similar patient selection criteria Study

No. of cases

Local Follow-up recurrence (%) (month)

Gerber et al. [25] Caruso et al. [26] Sacchini et al. [27] Petit et al. [28] Benediktsson and Perbeck [29] Benediktsson and Perbeck [29]

112 50 123 106 (IORT) 47 (RT)

5.4 12 2 1 8.5

169 (no RT) 28.4

52 66 24.6 13 156 156

IORT, intraoperative radiation therapy; RT, radiation therapy.

modified radical mastectomy group, 8.2% of patients recurred after a median follow-up of 59 months. The NSM group had a recurrence rate of 5.4%, with only one recurrence appearing in the nipple. This was treated with wide excision, and the patient was reported to be free of disease after 52 months. Caruso et al. [26] considered NSM in patients with early stage tumors that were peripherally located and added reconstructive criteria for patient selection. These criteria included small- to moderate-sized breasts with moderate to minimal ptosis and juvenile or healthy appearing skin. Their study included 50 patients with a 12% overall recurrence rate at mean follow-up of 66 months. One patient recurred locally in the nipple and was successfully treated with NAC excision. Sacchini and colleagues [27] evaluated 123 patients who had NSM with reconstruction for either prophylaxis, treatment of breast cancer, or both at four large centers. Their inclusion criteria included patients with tumors >1 cm from the areola and ptosis less than grade 4. Only two patients treated for cancer were found to have a recurrence, and one patient died from distant metastases 50 months after NSM. Breast cancer developed in two patients who had NSM for prophylaxis, one in the upper outer quadrant of the breast and one in the axillary tail. No patients had a recurrence or cancer development in the NAC. Expanding the selection criteria for NSM has been suggested by some authors who have performed NSM followed by intraoperative radiation therapy and immediate reconstruction. Petit et al. [28] investigated this technique in 102 patients with large, multicentric tumors clinically distant from the NAC. After an average followup of 13 months, only one local recurrence was reported under the clavicle, far from the NAC. Early radiodystrophy (depigmentation) was reported in 7.5%, 10.4% of patients developed sloughing of the superficial areolar skin, and 4.7% had complete necrosis of the nipple. Benediktsson and Perbeck [29] conducted the only prospective trial on NSM with a primary endpoint of survival. They examined 216 patients with NSM for the treatment of unilateral breast cancer with a median follow-up of 13 years. Their patient population included patients with T1eT3 tumors, multicentricity (73%), and axillary lymph node involvement (40.3%). Forty-seven received adjuvant radiotherapy; 53 had chemotherapy; 122 were placed on hormonal therapy. The frequency of localeregional

recurrence was 8.5% among patients who received radiation therapy, and 28.4% among non-irradiated patients. The disease-free survival of 51.3% and overall survival of 76.4% were comparable to that of conventional mastectomy performed in other trials. In their study, radiotherapy effectively lowered the frequency of local recurrence. Based on these studies, NSM appears to be oncologically safe for appropriately selected patients. However, additional longterm follow-up is needed, and these patients should be followed with special surveillance following NSM.

Technique and complications The NSM leaves the dermis and epidermis of the nipple but removes the major ducts from within its lumen. Dissection of the ducts should be performed with scissors rather than with electrocautery to avoid thermal damage to the NAC. Nipple eversion may facilitate dissection and removal of the tissue core within the nipple. These ducts should be sent to pathology as a separate specimen, and the nipple must be removed if any carcinoma is identified. Traction of the mastectomy flaps should be avoided to prevent damage to small capillaries, which can lead to necrosis of the skin flap, nipple, or areola. Immediate reconstruction can be performed with placement of a tissue expander or implant, or creation of a TRAM or latissimus dorsi flap. There are four different types of skin incisions for NSM [27] (Fig. 1aed). The periareolar incision with lateral extension can be performed inferior or superior to the NAC. This allows excellent exposure for dissection of the retroareolar ducts and lateral breast tissue. The lateral extension can extend up to 7 cm, facilitating dissection of the lateral margin of the pectoral muscle for implant placement. This incision, however, may compromise blood supply at the periphery of the flap and areola, and can cause ischemia of the inferior half of the areola. The transareolar incision with perinipple and lateralemedial extension may reduce the risk of ischemia of the lower portion of the areola, but one must take caution to avoid dividing the perinipple artery arising from the breast parenchyma. A disadvantage of this incision is the potential for perinipple scarring, leading to downward nipple projection. The transareolar and transnipple incision with medial and lateral extension involves bivalving the nipple. This incision does not compromise the vascularity of the nipple or areola and provides the best exposure to the retroareolar ducts. The last type of incision is the mammary crease incision that can be performed inferiorly or laterally [30]. With this incision, the scar is the least evident, and the vascularization of the skin flap is preserved by the superior and medial vessels. However, access to the breast parenchyma in the parasternal and subclavicular regions is limited, and adequate removal of tissue in these regions may be compromised. This problem can be improved with the aid of the fiberoptic-lighted retractor. Palmieri et al. [31] proposed a two-stage technique of delayed nipple-sparing modified subcutaneous mastectomy in an effort to address complete removal of all mammary tissue, including the main lactiferous ducts, while retaining the integrity of the NAC. The first step involves NAC ‘‘autonomization’’ by using a periareolar incision under

264

A.P. Chung, V. Sacchini

Figure 1 (a) Periareolar incision with lateral extension; (b) transareolar incision with perinipple and lateralemedial extension; (c) transareolar and transnipple incisions with medial and lateral extensions; and (d) mammary crease incision.

local tumescent anesthesia and electrified laparoscopic scissors to detach the galactophore stalk from the nipple while coagulating the deep vascular plexus. The NSM with implant placement is then performed as the second step under general anesthesia 3 weeks later. They observed one case of NAC necrosis that occurred during the NAC autonomization. In this case, the NSM was delayed for 6 weeks to allow dermal revascularization, and the final outcome was satisfactory. While the rationale for this technique is logical, the addition of a separate surgical procedure adds to the complexity of the NSM and may introduce possibilities for additional complications. One of the most concerning complications of NSM is nipple or areolar necrosis, which can lead to implant loss. Viability of the NAC relies on preservation of the blood supply to the nipple, ducts, and the surrounding skin. Rusby and colleagues [32] conducted a study of nipple microvessels and their position relative to lactiferous ducts in 48 mastectomy specimens. They found the mean nipple diameter to measure 11.1 mm and the mean duct bundle to be 5.2 mm. The peripheral 2 mm of a non-irradiated nipple was found to contain 50% of the blood vessels in cross-section, whereas 66% of the blood vessels were identified in 3 mm of the periphery. According to their study, leaving a peripheral rim of 2 mm of nipple skin and subcutaneous tissue resulted in complete excision of the duct bundle in 96% of cases, while a peripheral rim of 3 mm would lead to complete excision in 87%.

The rate of nipple necrosis varies from 2 to 20% [26e 28,33e36] (Table 4), with higher rates reported in studies involving radiation therapy. Nipple necrosis can be a severe complication leading to exposure and eventual loss of the implant. Caruso et al. [26] described three cases of implant loss secondary to nipple necrosis. However, nipple necrosis can be partial and does not always result in complete necrosis and skin loss. Crowe et al. [33] described superficial tissue loss of the NAC as a common finding in their cohort during the first 7e21 postoperative days, but this resolved over time, and these patients eventually healed with good cosmesis. They ultimately reported only three (6%) cases of partial

Table 4 therapy

Nipple necrosis in studies involving radiation

Study

No. of cases

Partial Total necrosis (%) necrosis (%)

Crowe et al. [33] Caruso et al. [26] Sacchini et al. [27] Psaila et al. [34] Komorowski et al. [35] Petit et al. [28] Bistoni et al. [36]

48 50 192 139 38 300 (IORT) 10 (RT)

6.3 2 6.8 1 5.7 9.7 20

0 0 4.5 1 7.9 3.3 0

IORT, intraoperative radiation therapy; RT, radiation therapy.

Nipple-sparing mastectomy necrosis with no cases of skin or implant loss. In Gerber’s study [25], 9.8% of patients had partial nipple necrosis with no cases of complete necrosis. Sacchini et al. [27] reported a nipple necrosis rate of 11%, but 59% of these cases involved less than one-third of the nipple. As a result, 90% spontaneously settled, 10% required removal of the nipple, and only 2% resulted in implant exposure with subsequent loss of the implant. While preserving the blood supply to the NAC is the key factor to preventing necrosis, Komorowski et al. [35] found that younger age was associated with higher NAC viability, and they concluded that NSM was a safer procedure for women less than 45 years of age.

Conclusions While mastectomy with or without immediate reconstruction has been established as the standard treatment for risk reduction with acceptable rates of local recurrence, NSM has evolved as an alternative technique to improve the overall quality of life for women. There is no question that risk-reducing mastectomy provides the lowest rate of local recurrence. However, a surprisingly high number of patients are dissatisfied with the nipple reconstruction performed with conventional mastectomy. NSM provides a natural appearing nipple with a better cosmetic outcome and enables the patient to have a truer sensation of having her own breast. In addition, the procedure spares the patient from multiple operations that are required with nipple reconstruction, decreasing the anxiety and costs associated with nipple reconstruction. With the current outcomes reported for NSM, it should not only be considered for risk reduction, but should not be excluded as a treatment option for patients with breast cancer. The advent of breast-conservation therapy (BCT) altered the concept of breast cancer surgery, enabling women with breast cancer to preserve their body image. It has since replaced mastectomy as the most common standard treatment for breast cancer. However, it still carries a risk of local recurrence, ranging from 8.8 to 20% with long-term follow-up. Local recurrence can be psychologically devastating for patients [37]. Systemic therapy and additional surgery are required for invasive local relapses [38], adding to the emotional stress and leading to additional health expenses. Furthermore, breast reconstruction, when performed for recurrence, can be much more difficult in the face of irradiated tissue, and the chance of a successful cosmetic result is significantly decreased [39]. There is also recent evidence that local relapses may influence survival [40], and that perhaps the recurrences associated with BCT should not be accepted. NSM may result in a lower recurrence rate than BCT. For women who wish to preserve as much of their own breast as possible, NSM may be considered as an alternative surgical option to BCT for the treatment of small peripheral tumors or ductal carcinoma in situ (DCIS). NSM provides a better cosmetic outcome than mastectomy, and the recurrence rates reported thus far appear to be better than that of BCT. In conclusion, NSM appears to be oncologically safe in patients choosing mastectomy for risk reduction and for those with small peripheral tumors or DCIS. Additional studies with longer follow-up should be done to corroborate

265 the available evidence on the local recurrence rate for this procedure. Currently, NSM should be performed under protocol or with special surveillance, and explicit consent should be obtained from patients. It should still be presented to patients as an investigational modality in those who meet certain selection criteria and not as a replacement for the standard total mastectomy.

Conflict of interest statement All authors hereby disclose any financial and personal relationships with other people or organizations that could inappropriately influence (bias) this publication. This excludes employment, consultancies, stock ownership, honoraria, paid expert testimony, patent applications/registrations, and grants or other funding.

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