Plastic & Reconstructive Surgery:
Breast: Original Articles
Breast Reconstruction following Nipple-Sparing Mastectomy: Predictors of Complications, Reconstruction Outcomes, and 5-Year Trends
Colwell, Amy S. M.D.; Tessler, Oren M.D.; Lin, Alex M. B.S.; Liao, Eric M.D.; Winograd, Jonathan M.D.; Cetrulo, Curtis L. M.D.; Tang, Rong M.D.; Smith, Barbara L. M.D.; Austen, William G. Jr. M.D.
From the Division of Plastic Surgery, Massachusetts General Hospital, Harvard Medical School.
Received for publication June 14, 2013; accepted September 10, 2013.
Presented at the 82nd Annual Meeting of the American Society of Plastic Surgeons, in San Diego, California, October 11 through 15, 2013; the 58th Annual Meeting of the Plastic Surgery Research Council, in Santa Monica, California, May 2 through 4, 2013; and poster presentation at the 92nd Annual Meeting of the American Association of Plastic Surgeons, in New Orleans, Louisiana, April 20 through 23, 2013.
Disclosures: Amy Colwell, M.D., is a consultant for LifeCell Corp. and Allergan, Inc. She is a site investigator for the AirXpander clinical trial. There are no other disclosures.
Amy S. Colwell, M.D., Harvard Medical School, Division of Plastic Surgery, Massachusetts General Hospital, Boston, Mass. 02111, firstname.lastname@example.org
Background: Nipple-sparing mastectomy is increasingly used for treatment and prevention of breast cancer. Few data exist on risk factors for complications and reconstruction outcomes.
Methods: A single-institution retrospective review was performed between 2007 and 2012.
Results: Two hundred eighty-five patients underwent 500 nipple-sparing mastectomy procedures for breast cancer (46 percent) or risk reduction (54 percent). The average body mass index was 24, and 6 percent were smokers. The mean follow-up was 2.17 years. Immediate breast reconstruction (reconstruction rate, 98.8 percent) was performed with direct-to-implant (59 percent), tissue expander/implant (38 percent), or autologous (2 percent) reconstruction. Acellular dermal matrix was used in 71 percent and mesh was used in 11 percent. Seventy-seven reconstructions had radiotherapy. Complications included infection (3.3 percent), skin necrosis (5.2 percent), nipple necrosis (4.4 percent), seroma (1.7 percent), hematoma (1.7 percent), and implant loss (1.9 percent). Positive predictors for total complications included smoking (OR, 3.3; 95 percent CI, 1.289 to 8.486) and periareolar incisions (OR, 3.63; 95 percent CI, 1.850 to 7.107). Increasing body mass index predicted skin necrosis (OR, 1.154; 95 percent CI, 1.036 to 1.286) and preoperative irradiation predicted nipple necrosis (OR, 4.86; 95 percent CI, 1.0197 to 23.169). An inframammary fold incision decreased complications (OR, 0.018; 95 percent CI, 0.0026 to 0.12089). Five-year trends showed increasing numbers of nipple-sparing mastectomy with immediate reconstruction and more single-stage versus two-stage reconstructions (p < 0.05).
Conclusions: Nipple-sparing mastectomy reconstructions have a low number of complications. Smoking, body mass index, preoperative irradiation, and incision type were predictors of complications.
CLINICAL QUESTION/LEVEL OF EVIDENCE: Risk, III.
The combination of nipple-sparing mastectomy and immediate breast reconstruction has been gaining traction as a preferred surgical option for therapeutic and prophylactic mastectomy.1–8 Factors influencing this preference include increased early-stage treatment, prophylactic mastectomies,9 and improved aesthetic outcomes.10 Furthermore, current techniques for nipple-sparing mastectomy remove the glandular tissue from the nipple, thus differentiating them from subcutaneous mastectomies of the past, which left a significant amount of breast tissue within and under the nipple.
Nipple-sparing mastectomy has shown comparable oncologic risk when compared with traditional mastectomy, with a majority of studies reporting a low local recurrence rate of 3 percent or less.1,2,4,5,11–22 Furthermore, nipple-sparing mastectomy has proven safe in prophylactic mastectomy.2,11,14,23 These results have been maintained in long-term outcome studies,24 where nipple-sparing mastectomy shows oncologic outcomes similar to more traditional skin-sparing mastectomies.11,14,24
Currently, there are few data in the literature on reconstructive outcomes following nipple-sparing mastectomy. In this article, we review patient and technical variables to determine risk factors for complications in nipple-sparing mastectomy and to determine whether these risk factors influence reconstructive type. Five-year trends are reviewed.
PATIENTS AND METHODS
A retrospective, institutional review board–approved, chart review was performed on 500 consecutive nipple-sparing mastectomy and immediate breast reconstructions performed from June of 2007 until June of 2012. Indications for nipple-sparing mastectomy included no gross clinical, radiographic, or pathologic involvement of the nipple-areola complex. Tumor size, cancer stage, and a specific distance in centimeters from the nipple-areola complex were not considered absolute contraindications. The tissue from under the nipple was removed and sent as a separate section. A positive nipple margin was treated with nipple removal. Nipple-sparing mastectomy was performed to remove the breast tissue through five different access incisions: inferolateral inframammary fold, horizontal radial, inferior radial, periareolar (any incision involving a full-thickness incision along a portion of the areola), and through an extension of a preexisting scar.25 Patients choosing a prosthetic-based reconstruction were offered an attempt at single-stage reconstruction if their size goals were similar to their preoperative breast size. If a patient wanted a significantly larger size, a two-stage reconstruction was advised. Final determination for implant versus staged expander reconstruction was made intraoperatively after mastectomy with observation of the health of the skin flap and achievement of acceptable symmetry for bilateral cases. The health of the skin was based on observation of skin color, capillary refill, flap thickness, color change with inflation of a saline sizer to the appropriate volume, and experience of the breast surgeon.
Outcome measures examined included complications and the type of implant reconstruction (single-stage/direct-to-implant or two-stage). Complications were defined as infection requiring intravenous antibiotics, mastectomy skin flap necrosis and nipple-areola complex necrosis requiring surgical intervention, seroma, hematoma, and implant/expander loss. Predictive variables included year of study, mastectomy access incision, patient age, body mass index, initial implant volume, smoking status, preoperative and postoperative radiotherapy, previous breast cancer, and preexisting breast scar(s).
Fifty-seven women who attended a seminar on breast reconstruction at the Forces in Hereditary Breast Cancer Conference and who had breast cancer or a strong predisposition toward development of breast cancer were educated on breast reconstruction choices, nipple-sparing mastectomy, and incisions used for nipple-sparing mastectomy. A diagram was used to describe the various incisions for nipple-sparing mastectomy to avoid bias from actual patient photographs where the reconstruction itself may influence preference for incision type. They were then asked to complete a survey with the following questions:
1. The following statement best describes me: a) Breast cancer survivor, b) New diagnosis of breast cancer, c) Strong family history of breast cancer or breast cancer gene (BRCA) positive, d) Other.
2. If I have a mastectomy or had a mastectomy, reconstruction of the breast is/was:
Not important 0 1 2 3 4 5 Extremely important.
1. The mastectomy incision I prefer for a nipple-sparing mastectomy is:
____Under the nipple “periareolar”
____Under the breast “inframammary fold”
Data were analyzed using Stata version 11.2 (StataCorp, College Station, Texas). We chose alpha = 0.05 as our level of significance throughout. One-way analysis of variance was used to look for significant correlations between continuous and categorical variables (e.g., incision type, study year, complications). All positive analysis of variance findings were then investigated further with two-sample t test using the Bonferroni correction to maintain our alpha at 0.05. Chi-square analysis or Fisher’s exact test was performed to check for correlations between categorical predictors and outcomes. Univariate analysis was then performed to obtain odds ratios and 95 percent confidence intervals for positive correlations. After discovery of significant relationships between risk factors and outcomes, multivariate regression modeling was analyzed to control for possible confounders and to examine interrelations between variables found to have an impact from initial statistical testing. Values of p = 0.1 to p = 0.05 are described as a trend approaching statistical significance.
The series consisted of 285 patients, with a mean age of 45.7 years (range, 25 to 78 years) and a mean body mass index of 23.7 (range, 16.9 to 37.8) (Table 1). The mean follow-up was 2.17 years. Of patients undergoing nipple-sparing mastectomy, 98.8 percent underwent immediate reconstruction and served as the source population. Of the 500 planned nipple-sparing mastectomy and immediate reconstructions, 18 mastectomies (3.6 percent) were converted to skin-sparing mastectomies with removal of the nipple-areola complex because of positive pathologic margins either at the time of the original mastectomy (positive intraoperative margins) or if the final pathologic margins were positive. These 18 reconstructions were excluded from the analysis, and the remaining 482 reconstructions (267 patients) served as the source population for comparative outcomes. Two hundred twenty-two mastectomies (46.1 percent) were therapeutic and 260 (53.9 percent) were prophylactic. Four hundred seventeen mastectomies (86.5 percent) were bilateral and 65 (13.5 percent) were unilateral. Six percent of patients were smokers at the time of the reconstruction consultation, and 16 percent of patients received radiotherapy (8.7 percent received preoperative and 7.3 percent received postoperative radiotherapy). Sentinel lymph node dissection was performed in 350 reconstructions and 39 had axillary lymph node dissections. Reconstructions were performed with inferolateral inframammary fold [n = 246 (51 percent)], periareolar [n = 114 (23.6 percent)], extension of existing breast scar [n = 52 (10.7 percent)], horizontal radial [n = 49 (10.2 percent)], and inferior radial [n = 21 (4.4 percent)] incisions (Fig. 1). An acellular dermal matrix sling was used in 340 reconstructions (70.5 percent), 88 (18.3 percent) had partial or total muscle coverage without a sling, and 54 (11.2 percent) had Vicryl (Ethicon, Inc., Somerville, N.J.) mesh.
The total complication rate was 12.4 percent, with a mean follow-up of 2.17 years (range, 0.90 to 5.92 years) (Table 2). Complications included mastectomy skin flap necrosis (5.2 percent), nipple-areola complex necrosis (4.4 percent), infection (3.3 percent), seroma (1.7 percent), hematoma (1.7 percent), and implant loss (1.9 percent). In addition to the nipples removed for ischemia/necrosis, six were later removed for symmetry. Of the complications, 12 required a return to the operating room or readmission within 30 days.
Of the 482 reconstructions, 471 were implant-based and 11 were autologous. Two hundred eighty-six reconstructions were performed in a single stage and 185 were performed using tissue expander-implant two-stage reconstruction (Table 3 and Fig. 2).
In comparing patients who had one or more complications (n = 60) to those who did not have complications (n = 422), a periareolar incision was associated with the highest rate of total complications, whereas the inferolateral inframammary fold incision had the lowest rate of total complications (Fig. 3). Univariate logistic regression and chi-square tests identified risk factors for one or more complications (Table 4). After multivariate regression, increasing body mass index, smoking, preoperative irradiation, and a periareolar incision were significant predictors of one or more complications (Table 5). Conversely, an inframammary fold incision was a negative risk factor for complications.
In comparing single-stage to two-stage reconstruction, there were no differences in individual or total complications between the two groups (Table 6). There were more inframammary fold incisions used in the single-stage group, whereas there were more horizontal radial and inferior radial incisions in the two-stage reconstructions. Significantly more smokers had two-stage reconstruction and significantly more patients with preoperative radiotherapy had single-stage reconstruction (p < 0.005 for each).
The volume of cases for nipple-sparing mastectomy with immediate reconstruction and the percentage of direct-to-implant reconstructions increased significantly over 5 years (p < 0.05 for both). There was a trend approaching significance for the decrease of mastectomy skin flap necrosis in year 5 (Fig. 4 and Table 7). Mastectomy access incision proportions differed significantly, with a higher percentage of inframammary fold and corresponding lower percentage of periareolar-based incisions in the final year of the study (p < 0.001) (Fig. 5). The mean body mass index and mean implant volume were significantly higher in year 5 (p < 0.05 for each).
In our patient survey, 74 percent ranked breast reconstruction as extremely important (5 on a five-point scale). When asked their preference regarding incisions, 75 percent listed the inferolateral inframammary fold incision as the preferred approach.
Our retrospective review shows that patients who chose nipple-sparing mastectomy have a high rate of immediate reconstruction (98.8 percent) at the time of mastectomy. Of 500 consecutive patients undergoing nipple-sparing mastectomy and immediate reconstruction, there was a high nipple retention rate after excluding patients who underwent removal for positive margins (96 percent retention rate) and also excluding patients with nipple removal for necrosis or symmetry, for an overall nipple retention rate of 91 percent.
Early outcomes with nipple-sparing mastectomy demonstrated high rates of ischemic complications to the nipple-areola complex and mastectomy skin flaps, which led to concerns regarding implant loss and reconstructive failure with these procedures.2,15,26,27 In our series, nipple-sparing mastectomy and immediate reconstruction showed a low overall complication rate (12.4 percent). Our ischemic complications of the nipple-areola complex compare favorably to the published literature (4.4 percent versus 0.2 to 20 percent),2,11,14–18,23,24,26,28 and our explantation rate was low at 1.9 percent.
Many mastectomy access incisions have been described for nipple-sparing mastectomy, and some are linked to early reconstructive complications.2,7,29 We found that a full-thickness incision around the areola was a risk factor for nipple-areola complex necrosis, mastectomy skin flap necrosis, and total complications, which is consistent with studies that have shown risk reduction in complications with avoidance of extensive incisions around the areola.13,17,26,30 The inferolateral inframammary fold incision, as we previously described, provides ease of access for mastectomy and an aesthetically pleasing scar.25 The incision is made from the 6-o’clock position to the 9-o’clock or 3-o’clock position and thus increases in size as the breast size increases. The average length of our incisions was approximately 14 cm. In this article, it was associated with a decreased risk of total and ischemic complications.
Several factors have consistently been shown to increase early prosthetic-based breast reconstruction complications, including radiotherapy,9,31–40 body mass index, 31–34,41–45 smoking,31–34,42–45 patient age,31,42–44 and implant volume.45 In our study, body mass index, smoking, and preoperative radiotherapy were all independent risk factors for one or more complications.
The choice of single-stage or two-stage reconstruction is clearly multifactorial and dependent on patient size goals, breast anatomy, and the quality of the mastectomy skin flaps. Nipple-sparing mastectomy increases the number of patients who are potential candidates for direct-to-implant reconstruction by preserving more overall skin and surface area to place an implant, and by helping to avoid some of the flattening associated with closure of skin-sparing incisions. In addition, we found that smoking and an inferior radial incision were more common in two-stage reconstruction, likely related to the perfusion of the skin flaps and the skin tension from a vertical scar. Although the lateral radial incision was associated with more two-stage reconstructions, the most likely explanation for this finding is that we prefer to use this incision for patients who are at higher risk for nipple or skin flap ischemia to maximize the blood flow to the nipple. There were more single-stage reconstructions in patients with preoperative irradiation, which may come as a surprise to many surgeons. If possible, we prefer to perform a conservative single-stage reconstruction in these patients. Although two-stage reconstruction can be successfully performed in these patients, there is a higher rate of immediate complications in our experience secondary to skin shrinkage around the tissue expander followed by expansion and a second operation. There was no overall difference in complication rates between single-stage and two-stage reconstruction, similar to our previous comparative article.9
Our 5-year trends reflect the data presented. A team approach with breast surgical oncology and plastic surgery has led to advancements in the development of successful surgical strategies and techniques. Our breast surgeons avoid vigorous retraction and retractors with sharp teeth. Their plane of dissection is between the anatomical separation of the subcutaneous fat and the breast tissue. We are performing an increasing number of nipple-sparing mastectomy procedures as more breast oncology surgeons become comfortable with the procedure and with expansion of our indications for nipple-sparing surgery. Our data from 2007 to 2011 showed no local recurrences in our prophylactic mastectomy patients and a rate of 2.6 percent in our breast cancer patients, with no patient having involvement of the nipple.46 Our preferred incision has become the inferolateral inframammary fold incision based on the complication profile and patient preference, which was observed in our survey results but is also expressed daily in our consultations. Our number of direct-to-implant reconstructions went up in year 2 of the study but then decreased as more breast and plastic surgeons gained experience with the technique. In year 5, with experience, single-stage reconstruction is now performed in 68 percent of nipple-sparing mastectomies.
This retrospective review demonstrates that nipple-sparing mastectomy and immediate reconstruction has a high rate of success and a low rate of complications. In our experience, the inferolateral inframammary fold incision has resulted in superior reconstructive outcomes, is preferable to patients, and can reduce the need for additional procedures by allowing for a greater proportion of direct-to-implant reconstructions. Periareolar incisions increase the odds of ischemia-related complications and should be avoided in inexperienced hands. Other risk factors important to assess in deciding operative strategy include patient body mass index, smoking status, desired implant volume, and preoperative radiotherapy.
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