Introduction
Historically, breast cancer was managed by radical mastectomy. Since then, the pendulum has turned such that the majority of breast cancer is safely managed with breast conserving therapy. However, some women still require or prefer mastectomy and a number of advances in surgical technique including both oncologic resection and reconstruction have allowed for improved esthetic outcome.
Skin-sparing mastectomy (SSM), nipple-sparing mastectomy (NSM), and areola-sparing mastectomy (ASM) have all been described in recent literature and have been tested for oncologic safety and patient satisfaction with esthetic outcome. These techniques all provide improved cosmesis, especially when coupled with immediate breast reconstruction (IBR).
The following is a brief description and literature review of SSM, NSM, and ASM for the management of breast carcinoma.
Skin-sparing mastectomy
Surgical technique and considerations
SSM includes removal of all breast parenchyma, any existing biopsy scar, and complete resection of the nipple/areolar complex (NAC). The surgical oncologist and reconstructive surgeon work together to select the most desirable incision – three of the most common being periareolar, modified elliptical, and mastopexy/reduction mastoplasty [Reference Simmons1]. Modifications such as axillary incisions or medial–lateral extensions can be added to increase exposure to axillary contents, prior biopsy scars, and tumor areas [Reference Simmons, Fish and Gayle2]. Sentinel node biopsy and/or axillary dissection can also be performed when indicated for invasive disease.
Options for breast reconstruction for SSM include tissue expander/implant, transverse rectus abdominis myocutaneous flap (TRAM), deep inferior epigastric perforator (DIEP) flap, latissimus dorsi flap, or gluteal flap [Reference Simmons1]. Selection depends on individual patient characteristics. Complications of SSM with IBR include flap necrosis, native skin necrosis, hematoma, and implant failure [Reference Simmons1]. The incidence of flap and skin necrosis varies between 0% and 12% across studies [Reference Omranipour, Bobin and Esouyeh4–Reference Carlson, Bostwick and Styblo7]; however, overall complication rates were not found to be significantly different compared to non-SSM (NSSM). One report by Carlson and colleagues showed that native skin flap epidermolysis occurred in 10.7% of patients with SSM and in 11.2% of those with NSSM (P = non-significant) [Reference Carlson, Bostwick and Styblo7].
Oncologic safety
A number of both retrospective and prospective studies over the past decade have verified the oncologic safety of SSM in select patients. Our group retrospectively investigated local recurrence (LR) and distant recurrence (DR) in patients receiving SSM (n = 77) and NSSM (n = 154) [Reference Simmons, Fish and Gayle2]. After a mean follow-up of 15.6 months, both LR and DR rates were not significantly different between the two groups, along with 5-year actuarial disease-free survival for LR and DR. Likewise, the 5-year overall survivals between SSM and NSSM groups were similar at 7.8% and 6.5%, respectively. A similar retrospective study by Rivadeneira and colleagues with a different group and having a mean follow-up time of 38.4 months reported similar findings [Reference Rivadeneira, Simmons and Fish8].
Outcomes data of several recent studies of SSM are listed in Table 1. LR varied between 0% and 5.6%, while DR varied between 2.1% and 16% [Reference Simmons, Fish and Gayle2,Reference Omranipour, Bobin and Esouyeh4–Reference Foster, Esserman and Anthony6,Reference Carlson, Styblo and Lyles9,Reference Spiegel and Butler10]. An important consideration in the variability demonstrated in recurrence rates, particularly DR, is the differences in the distribution of disease stage. Foster et al. investigated outcomes in both early- and late-stage disease. They found DR as high as 16%; however, all these occurred in patients with stage IIIA disease or higher [Reference Carlson, Bostwick and Styblo7]. In all but one of the studies listed, there were no recurrences in patients with stage 0 or stage I disease, and in the remaining study, only six out of 539 patients (5.5%) with early disease had LR [Reference Carlson, Styblo and Lyles9]. Similarly, Downes et al. investigated the utility of SSM with IBR in 38 patients with high-risk breast cancer (disease stage IIA or greater; mean follow-up: 52.9 months). LR was seen in 2.6%, while DR was seen in 26.3% [Reference Downes, Glatt and Kanchwala11].
Table 1 Literature review of oncologic outcomes of skin-sparing mastectomy with immediate breast reconstruction.
F/U: follow-up; LR: local recurrence; DR: distant recurrence; DCIS: ductal carcinoma in situ; NR: not recorded.
In addition to disease stage, other tumor factors related to disease recurrence after SSM include poor tumor differentiation, lymphovascular invasion, tumor size greater than 2 cm, and node-positive disease [Reference Simmons, Fish and Gayle2,Reference Carlson, Styblo and Lyles9,Reference Spiegel and Butler10]. These data indicate that careful patient selection is necessary to minimize cancer recurrence in patients receiving SSM.
Nipple-sparing mastectomy
Surgical technique and considerations
Similar to SSM, NSM involves removal of all breast parenchyma and previous scars; however, the skin envelope, including the dermis and epidermis of the nipple and areola, is left intact. Importantly, the nipple core should be sent for frozen section and any evidence of NAC involvement precludes the procedure, as removal of the nipple remnant is necessary. Similarly, the final pathology positive for NAC involvement necessitates further management either with repeat surgery and NAC removal or with other therapy, such as radiation. Sentinel node biopsy and axillary dissections can be performed as indicated.
Careful planning of the incision is critical, as consideration must be given not only to prior biopsy scars, tumor location, and reconstructions but also to NAC vascularization. Sacchini described four different skin incisions for NSM, including an inferior or superior periareolar incision with lateral extension, which offers good surgical exposure but may compromise blood supply to the flap periphery and areola; transareolar with perinipple and lateral–medial extension, with the possible sequelae of perinipple artery division or scarring; transareolar and transnipple with extensions; or a mammary crease incision inferiorly or laterally, which may offer the best preservation of flap vascularity [Reference Sacchini, Pinotti and Barros13]. Radial transareolar incisions have been associated with reduced NAC loss and improved surgical outcomes [Reference Wijayanayagam, Kumar and Roster14,Reference Stolier, Sulllivan and Dellacroce15].
The most important technical concern is the preservation of adequate vascularization to the NAC to prevent necrosis. The vascular anatomy of the NAC shows significant variation in sources and patterns of blood supply between individuals. The internal and lateral thoracic, internal mammary, and intercostal arteries have been shown to contribute in varying and overlapping amounts to NAC vascularization. Both radial and loop anastomotic vascular patterns have been described, and these patterns have important surgical implications in the maintenance of sufficient NAC blood supply. One study reported NAC necrosis as high as 11%, almost half of which was in the setting of TRAM reconstruction. As in SSM, other possible complications include flap or skin necrosis, wound infection, and implant loss [Reference Sacchini, Pinotti and Barros13].
Considerations for the type of reconstruction slightly differ for NSM than for SSM. Importantly, tension on the skin via subcutaneous implants may impact blood supply to the skin and NAC. Tissue expanders and muscle flaps such as latissumus dorsi, TRAM, and DIEP have been utilized, although there appears to be lower complication rates with initial tissue expander use [Reference Sacchini, Pinotti and Barros13,Reference Wijayanayagam, Kumar and Roster14]. Sacchini et al. [Reference Sacchini, Pinotti and Barros13] investigated 192 NSMs in 123 patients receiving either subpectoral or subcutaneous implants, tissue expanders, or TRAM reconstructions. Complications included flap necrosis, nipple/areola necrosis, or implant loss when applicable. Complications occurred in 22% of those receiving subpectoral or subcutaneous reconstruction, in 13% of those receiving tissue expanders, and in 32% of TRAM reconstructions.
Oncologic safety
Although offering improved cosmesis, the oncologic consequence of NSM must be thoroughly considered, as any occult cancer or remaining breast tissue poses a significant risk to the patient. Reported rates of malignancy involvement within the nipple range from 0% to 58%, depending on the size of the primary breast tumor, location, multicentricity, and lymph node positivity [Reference Sacchini, Pinotti and Barros13,Reference Laronga, Kemp and Johnston16–Reference Verma, Kumar and Joshi20]. Our group retrospectively investigated 217 mastectomy specimens for malignant involvement of the nipple, areola, or both. We found 10.6% of specimens had nipple involvement. However, when a subgroup of patients with tumors <2 cm, peripheral tumors, and two or fewer positives nodes was analyzed, the rate dropped to 6.7% [Reference Simmons, Brennan and Christos17]. In another study, factors found to be associated with NAC preservation were tumor nipple distance >4 cm and absence of lymphovascular invasion [Reference Vlajcic, Rado and Standec21].
Table 2 summarizes cancer outcomes in recent studies of NSM with IBR. LR ranged from 2% to 24%, while DR ranged from 1.4% to 20%. Overall patient survival ranged from 76.4% to 100% [Reference Sacchini, Pinotti and Barros13,Reference Caruso, Ferrara and Castiglione22–Reference Petit, Veronesi and Orecchia24]. Benediktsson and Perbeck [Reference Benediktsson and Perbeck23] reported much higher LR and DR rates, and the lower overall survival compared to other studies was due to subcutaneous mastectomy being used, which the authors attributed to comparatively reduced rates of adjuvant radiation use. Importantly, in all the studies listed, patients with small tumor size, early-stage disease, and peripherally located tumors were preferentially selected, indicating that NSM may be more beneficial in this select subgroup of patients; however, a risk of recurrence is not negligible and patients must be counseled and followed appropriately.
Table 2 Literature review of oncologic outcomes of nipple-sparing mastectomy with immediate breast reconstruction for breast cancer.
F/U: follow-up; LR: local recurrence, DR: distant recurrence, OS: overall survival, NAC: nipple–areolar complex, UOQ: upper outer quadrant; IORT: intraoperative radiation therapy.
Areola-sparing mastectomy
Surgical technique and considerations
The ASM technique includes resection of the nipple, any existing biopsy scar, and removal of all breast parenchyma; however, the areola is preserved. A minimal amount of skin is removed, similar to SSM, which provides a natural envelope of skin for superior reconstruction. Incisions may be completely intra-areolar (either S-shaped or linear), linear intra-areolar with extra-areolar extension, inverted-T infra-mammary crease, or infra-mammary crease and perinipple, with or without additional axillary incision. The undersurface of the areolar flap can be touch-prepped for cytological evaluation at the discretion of the surgical oncologist if there is concern regarding margins in this area. Complications and reconstruction options are similar to those for SSM.
Oncologic safety
Sparing the areola improved reconstruction with either prosthetic implants or flaps. This patient satisfaction is justified, however, only if oncologic safety is not compromised. While numerous studies have investigated the malignant involvement of the NAC in breast cancer, the anatomic differences between the nipple and areola, however, necessitate separate investigation of possible malignant involvement [Reference Giacometti and Montagna25,Reference Schnitt, Goldwyn and Slavin26]. In our pathologic study of 217 mastectomy specimens, we found malignant areola involvement to be less than 1% for patients with small, infiltrating carcinoma and no areola involvement in DCIS [Reference Simmons, Brennan and Christos17]. With these data, we retrospectively analyzed 17 ASMs in 12 patients with IBR. Mean patient follow-up was 7 months (range 2–17 months). Ten ASMs were performed for breast cancer prophylaxis, four for DCIS, and three for infiltrating ductal carcinoma. Thirteen were done with tissue expanders and the remaining with TRAM flaps. There was one post-operative complication (local wound infection) and no instance of LR or DR [Reference Simmons, Hollenbeck and Latrenta27].
Our data indicate that ASM may be a safe option for selected patients; however, prospective trials that are currently ongoing will provide valuable additional information on the safety and efficacy of this technique.
Conclusion
With meticulous patient selection and well-planned surgical technique, conservation of the skin, areola, and possibly the nipple can provide satisfactory oncologic and esthetic outcomes with minimal complications and improved patient satisfaction.
