The Evolution of Nipple-Sparing Mastectomy (NSM)




© Springer International Publishing Switzerland 2017
Jay K. Harness and Shawna C. Willey (eds.)Operative Approaches to Nipple-Sparing Mastectomy10.1007/978-3-319-43259-5_1


1. The Evolution of Nipple-Sparing Mastectomy (NSM)



Jay K. Harness1, 2  


(1)
Center For Cancer Prevention and Treatment, St. Joseph Hospital, Orange, CA, USA

(2)
Department of Surgery, University of California Irvine Medical Center, Orange, CA, USA

 



 

Jay K. HarnessClinical Professor of Surgery



Keywords
Nipple-sparing mastectomy (NSM)Nipple–areolar complex (NAC)Breast cancerBreast reconstructionSubcutaneous mastectomy (SCM)Skin-sparing mastectomy (SSM)Modified radical mastectomy (MRM)


The evolution of the management of all aspects of breast cancer is breathtaking. We have evolved from more radical treatments to less extensive and personalized treatments with vastly improved outcomes.

The surgical management of breast cancer has also evolved dramatically over the decades from the disfiguring Halsted radical mastectomy to breast conservation, and now nipple-sparing mastectomy (NSM).

The nipple–areolar complex (NAC) defines the breast, and it makes a breast a breast. Historically, the standard of care was to discard the NAC because of possible involvement with cancer, a site for possible recurrent cancer, and the fear that we could not keep the NAC alive because of thinly created mastectomy skin flaps. The psychological benefits of restructuring or preserving the NAC have been clearly demonstrated [1, 2].


The Psychological Benefits of Preserving the Nipple


The emotional benefits of breast reconstruction include: (1) Reduction of a patient’s preoccupation with her breast cancer, (2) Facilitation of wardrobe flexibility restricted by wearing an external prosthesis, (3) Elevation of mood and less anxiety, (4) Enhancement of body image, and (5) Improvement of sexual responsiveness. Including the nipple (reconstructed or natural) as part of breast reconstruction gives a patient a sense of completeness, not present with breast contour reconstruction alone [3]. The sense of completeness allows a patient to experience herself as “like herself,” meaning close to her preoperative state [1].

Didier and colleagues showed in their study of NSM patients a very high level of satisfaction for having preserved their nipples, and less feelings of being mutilated by their mastectomies. They also found that NSM had impacted positively on patient satisfaction with cosmetic results, with femininity and body image, especially related to nakedness [2].


Historical Background


The concept that preserving the NAC is less mutilating than a total mastectomy can be documented to as early as 1882 [4]. However, the modern era of NSM really began with the report by Bromley S. Freeman, MD in 1962 [5]. The nipple-sparing mastectomies performed by Dr. Freeman at the Mayo Clinic preserved the glandular tissue beneath the NAC in order to protect the blood supply to the NAC. The term, “subcutaneous mastectomy” (SCM) is what his NSM was called, and continues to be known as today. The procedure was not for women with cancer, but those with painful and extensive fibrocystic changes of the breast. A 10-year follow-up of 1500 Mayo Clinic SCM patients for benign disease found a subsequent 0.4 % incidence of breast cancer [6]. This demonstrated the preventive or prophylactic effect of a near-total mastectomy on the development of expected subsequent breast cancers.

The initial report of the use of SCM for breast cancer treatment was in 1984 in the British Journal of Surgery by Hinton et al. [7]. Hinton reported on 98 patients undergoing SCM, with two patients having bilateral mastectomies, making a total of 100 SCMs. The series began in 1974. He compared the SCM group with a parallel group of women undergoing simple mastectomies. The majority of patients in both groups had early-stage (I, II) breast cancer. There was no statistical difference between the SCM and simple mastectomy groups when comparing local recurrence (LR), disease-free survival (DFS), and overall survival (OS) [7]. The surgery community pushed back hard against Hinton’s concept, despite the fact that he reported that the SCM group achieved local recurrence and early survival rates equivalent to those for modified radical mastectomy [7].

Another British report was published 6 years later in 1990 by C.C.R. Bishop and colleagues [8]. Their procedure was unique. They performed total mastectomies , including axillary clearances, with preservation of the nipple, together with the skin of one-half of the breast. The other half of the breast and the mastectomy site was then reconstructed with the latissimus dorsi flap and a silicone implant. From 1982 to 1988, a total of 87 women underwent total mastectomy and immediate reconstruction with their unique approach. In Group I, 63 women had their procedures for tumor recurrence after prior partial mastectomy and radiation therapy. There were no recurrences in the preserved nipples at a mean follow-up of 3.9 years. In Group II, 24 women had their procedures as primary treatment of their early-stage breast cancers with three nipple recurrences (12 %) at a mean follow-up of 3.8 years [8].


Cautious Beginnings


Despite the pushback against Hinton’s concept of SCM for breast cancer treatment, institutions in Japan, the United States, Germany, and Croatia began performing NSMs for both prevention and treatment from 1985 to 1998 [916].

The most pivotal early publication on the results of NSM was in 2003 by Gerber and colleagues from Rostock, Germany [12]. They reported on 61 patients who underwent skin-sparing mastectomy (SSM) with NAC conservation, 51 patients who had SSM without NAC conservation, and 134 patients who had a standard modified radical mastectomy (MRM) . The SSM patients, with or without NAC conservation, were younger, averaging around 49 years of age. With a mean follow-up of 59 months, only one patient had a recurrence in the preserved NAC. The minimum distance from tumor to NAC was 2 cm in those who underwent SSM with NAC conservation [12].

In 2009, Gerber then reported on the same group of patients, now with a mean follow-up of 101 months [13]. There was no difference in local regional recurrence rates or deaths in all three groups. There were no additional recurrences in the NAC-preserved SSM group, other than the one case originally reported in 2003. Their conclusion was that preservation of the NAC was oncologically safe [13].

The first American group to publish on NSM for cancer was Dr. Joseph P. Crowe and colleagues from the Cleveland Clinic [17]. Their 2004 publication reported on 54 NSMs attempted among 44 patients. Six NAC core specimens found neoplastic involvement on frozen section analysis, resulting in conversion to total mastectomies. Forty-five of the 48 completed NSMs maintained postoperative viability of the NAC; three NACs had partial necrosis. This small series covered the time period from September 2001 to June 2003 [17].

A follow-up paper from Crowe and colleagues reported on their experience with 110 consecutive patients undergoing 149 NSMs from 2001 to 2007 [18]. There were no NAC recurrences in their series. They primarily utilized lateral incisions for the performance of their NSMs. The incidents of NAC neoplastic involvement at the time of mastectomy remained at 11 % in the larger series, which was the same as their initial report in 2004 [17, 18]. Sixty-four of the 154 NSMs were for prevention, and 85 were for breast cancer treatment. Exclusion criteria for performing NSMs included patients whose tumors were larger than 3.5 cm, centrally located tumors, lymph node involvement, inflammatory breast cancer, clinical involvement of the NAC, and patients who underwent neoadjuvant chemotherapy [18].


Areolar Preservation


Contributing to the interest in NSM was a series of papers by Dr. Rachel M. Simmons and coworkers on areolar-sparing mastectomy, published between 2002 and 2004 [1921]. Their initial report in 2002 was a retrospective analysis of 217 mastectomy patients conducted to determine the frequency of malignant nipple or areolar involvement with tumor. They also analyzed the association between nipple and/or areolar involvement and prognostic factors, including tumor size, pathologic stage, nuclear-grade, axillary nodal status, and tumor location. The overall frequency of malignant nipple involvement was 10.6 %. In a subgroup of patients with tumors less than 2 cm, peripheral tumors, and two positive nodes or less, the incidence of nipple involvement was 6.7 % [19]. When the nipple and areola involvement were analyzed separately, only 2 of 217 patients (0.9 %) had involvement of the areola. All patients with areolar involvement had Stage III breast cancers that were centrally located. They concluded that the preservation of the areola with skin-sparing mastectomy, in selected patients, warranted further study.

In 2003, Simmons and her coworkers reported on a small series of 12 patients who underwent 17 areola-sparing mastectomies (ASM) [20]. The study period was only 20 months. Ten mastectomies were for prophylaxis, four for ductal carcinoma in-situ (DCIS) , and three were for peripheral infiltrating carcinomas, less than 2 cm in size. In 2004, they reported on the 2-year follow-up. They had no recurrences, one postoperative infection, and excellent cosmetic results. They concluded that ASM would be offered to selected patients, including those desiring surgical breast cancer prophylaxis , as well as those with DCIS or small peripheral infiltrating ductal carcinomas [21].


Increasing Interest in Nipple-Sparing Mastectomy


Starting in the late 1990s, multiple academic institutions in the United States, Italy, and other locations around the world began to seriously consider NSM as an alternative to SSM. From 2000 to 2010, multiple reports from these academic institutions began to appear in the surgical literature, summarizing their individual institutional experiences [1013, 17, 18, 2234]. There were multiple issues that these reports analyzed. In general, the issues focused on patient selection, operative techniques, complications, oncologic safety, and cosmetic outcomes. Most of the institutional series were small, with short-term follow-ups averaging around a mean of 20 months.

In these initial series, much of the patient selection focused on patients wanting prophylactic mastectomies for risk-reduction. Several series were predominantly preventative mastectomies as a safe way to venture into the arena of NSM.

With breast cancer patients, various safe criteria were created for patient selection . Clearly, no patients would be eligible for NSM with clinical involvement of the NAC or bloody nipple discharge. Past literature analyzing NAC involvement with cancer in mastectomy specimens found the incidence of nipple–areolar involvement ranging from 5.9 to 50 % [10, 29]. Factors that have been associated with occult nipple involvement have been tumor size, subareolar location, tumor-to-nipple distance, positive axillary nodal status, multicentric tumors, and angiolymphatic invasion [29]. As a result, most institutions chose conservative inclusion criteria for selecting patients for NSM.

A good example of this approach is the initial criteria used by Dr. Scott Spear and colleagues. Tumor size less than 3 cm, tumor location greater than 2 cm from the NAC, clinically negative axillary nodes, no skin involvement, no inflammatory cancer, or Paget’s disease were key components of their selection criteria. In addition, preoperative MRI to exclude nipple involvement and possible preoperative ultrasound-guided core biopsy of the nipple base could also be used to rule out occult involvement of the nipple. With their initial criteria, they also excluded excessively large and ptotic breasts [11].

In these early institutional reports, various types of mastectomy incisions for NSM emerged. Incision designs included: radial (lateral or 6 o’clock axis), inframammary, circumareolar, NAC-crossing, lateral/inferolateral, mastopexy-type incision, and omega/areolar incisions [11, 22, 25].

The major complication that concerned everyone was partial or full loss of the NAC. What also emerged from the early literature was that there was a “learning curve” needed for incision selection and the tedious performance of NSM. As experience grew, complication rates fell [25]. The early literature also suggested that lateral (3 and 9 o’clock), vertical (6 o’clock), and inframammary incisions had lower ischemic complications with the NAC ranging from 0 to 5 % [11, 22, 25].

The oncologic safety of preserving the NAC in cancer patients is difficult to evaluate in the early institutional series because of the short mean follow-up times. Most series reported no NAC recurrences, and low regional recurrence rates were comparable to SSM, with reconstruction [11, 25, 30]. Three series with long-term follow-up of over 5 years have reported NAC recurrence rates of 3.7 %, 1.2 % and 0 %, respectively [9, 14, 15]. If the results of all series on NSM are combined, the NAC recurrence rate averages around 0.6 %.

Why would NAC recurrences rates be so low? One important reason could be the fact that terminal ductal lobular units (TDLUs) are demonstrated in only 25 % of nipples. More importantly, the TDLUs are always found at the base of the nipple, not within the nipple proper [22]. As a result, it is likely not important to core out the nipple as part of the NSM operative technique.

Cosmetic outcomes reported by these early institutional reports found that the majority of patients had excellent to good outcomes at least 70 % of the time [12, 13, 22, 25, 28, 29].


European Institute of Oncology of Milan (EIO)



Nipple-Sparing Mastectomy Series


The largest series of NSMs in the literature comes from the EIO in Milan, Italy [2628, 30]. Their experience requires special mention. In their past description of the technique used for the performance of an NSM, they leave a thin layer of breast tissue beneath the NAC. In other words, their technique is really a SCM. To compensate for leaving breast tissue behind the NAC, they have utilized intraoperative radiation therapy to sterilize the residual breast tissue [28]. At the time of the so-called nipple-sparing mastectomy, they are delivering 16 Gy of radiation therapy directly to the NAC. It is now informally understood that they have recently abandoned this approach, and now no longer leave breast tissue on the underside of the areola, or perform intraoperative radiation therapy .

In 2012, Dr. Petit and his colleagues from the EIO, reported on a unique form of NAC recurrence in 861 patients who had undergone their NSMs. There were seven cases (0.8 %) of Paget’s disease diagnosed with an average latency patency period from NSM to recurrence of 32 months (range, 12–49) [35]. My group has also reported an identical case of Paget’s recurrence in the areola 34 months after an areolar-sparing mastectomy [36].

The etiology of Paget’s local recurrence in the NAC is unclear. The Milan Group believes that extensive DCIS, negative hormone receptors, over-expression of HER2/neu, and high pathological grade tend to be associated with more Paget’s disease local recurrence [35]. Subsequent local resection of the NACs was curative for the seven cases from Milan, and the one case from my institution.


Increasing Mastectomy Rates


Reviewing the evolution of NSM would be incomplete without also reviewing a parallel phenomenon taking place over the same time period. Women with early stage breast cancer were increasingly choosing mastectomy as their primary surgical treatment, as well as also choosing contralateral prophylactic mastectomy (CPM) , in addition to their therapeutic mastectomy [3742].

Recent published reviews of both the Surveillance Epidemiology and End Results (SEER) database and the American College of Surgeons National Cancer Database (NCD) confirm these trends [37, 39, 40, 43]. The trend has also been confirmed by a review of the New York State Cancer Registry from 1995 to 2005 [38].

For both DCIS and invasive cancers, patients are increasingly considering mastectomy, despite the fact that they are excellent candidates for breast-conserving surgery (BCS) . What are the factors driving this phenomena?

One factor is worry about in-breast recurrence after BCS. For both DCIS and invasive cancers in gene-negative patients, the local in-breast recurrence rates are estimated to be 0.8–1.2 % per year [41, 43]. Women often feel that a “bigger operation” (mastectomy) may offer a better chance for survival, despite the fact that years of clinical trial results refute that belief.

In the reports analyzing the increasing mastectomy trends, other factors are discussed that appear to contribute to the decision for mastectomy over BCS. These include: utilization of preoperative breast MRI; white race; higher household income and education levels; younger age; greater peace of mind; avoidance of radiation therapy; and fear [41, 43]. A physician recommendation for BCS or mastectomy in early stage breast cancer also plays a role. In the latest report on mastectomy trends by Kummerow and colleagues, more than 80 % of women reported that their physicians made a specific recommendation for either BCS or mastectomy. Less than 50 % of women reported being asked by their physicians whether they preferred BCS or mastectomy [43].

Kummerow also noted that the observed increase in overall mastectomy rates from 1998 to 2011 was largely attributed to a rise in bilateral mastectomy for unilateral early stage disease from 5.4 % of mastectomies in 1998 to 29.7 % in 2011 [43]. There was also a concurrent increase in reconstruction procedures from 36.9 to 57.2 % during the same time period [43].

Kummerow’s observations are a good lead-in to a discussion about increased use of contralateral prophylactic mastectomy (CPM) . Tuttle and coworkers report in 2007 brought to light what most breast surgeons were already observing; namely, a marked increase in the performance of CPMs. The CPM rate was 3.3 % for all surgically treated patients, and 7.7 % for patients undergoing initial primary mastectomy [37]. The overall CPM rates significantly increased from 1.8 % in 1998 to 4.5 % in 2003. The CPM rate for patients undergoing mastectomy increased from 4.2 % in 1998 to 11.0 % in 2003 [37]. The use of CPM in the United States more than doubled with the 6-year period of their study.

What factors are driving the increasing rate of CPM? One factor is the fear of a subsequent contralateral breast cancer . The annual incidence of subsequent contralateral invasive breast cancer has been stable for many years, estimated to be approximately 0.5–0.75 % per year [37]. For women with a diagnosis of DCIS, the estimated risk of developing either a contralateral invasive cancer or recurrent DCIS is approximately 0.6 % per year [39].

If a patient needs or chooses a unilateral mastectomy as her primary surgical treatment, a CPM may be chosen for better cosmetic symmetry and reduction of fear of subsequent contralateral cancer [40]. A family history, gene status, surveillance of the breast, anxiety, and the use of preoperative MRI are commonly cited reasons why patients are increasingly choosing CPM [3740, 42]. In addition, rates of bilateral mastectomy are higher in hospitals where immediate breast reconstruction are available, indicating a possible strong influence on women choosing bilateral mastectomy [44]. Improved reconstruction techniques, including NSM, are also likely drivers of women choosing primary and contralateral prophylactic mastectomies [3744]. As with unilateral mastectomy , patients electing CPM are better educated, white, younger, and more affluent [3740].

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Oct 14, 2017 | Posted by in Aesthetic plastic surgery | Comments Off on The Evolution of Nipple-Sparing Mastectomy (NSM)

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