Annals of Surgical Oncology 10:108-112 (2003)
© 2003 Society of Surgical Oncology
Local Recurrence After Skin-Sparing Mastectomy: Tumor Biology or Surgical Conservatism?
Grant W. Carlson, MD,
Toncred M. Styblo, MD,
Robert H. Lyles, PhD,
John Bostwick, MD,
Douglas R. Murray, MD,
Charles A. Staley, MD and
William C. Wood, MD
From the Winship Cancer Institute and the Department of Biostatistics, Rollins School of Public Health, Emory University School of Medicine, Atlanta, Georgia.
Correspondence: Address correspondence and reprint requests to: Grant W. Carlson, MD, Winship Cancer Institute, 1365B Clifton Rd., Atlanta, GA 30322; Fax: 404-778-4255; E-mail: grant_carlson{at}emory.org
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ABSTRACT
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Background: Long-term follow-up of the use of skin-sparing mastectomy (SSM) in the treatment of breast cancer is presented to determine the impact of local recurrence (LR) on survival.
Methods: A total of 539 patients were treated for 565 cases of breast cancer by SSM and immediate breast reconstruction from January 1, 1989 to December 31, 1998. The American Joint Committee on Cancer pathological staging was stage 0 175 (31%), stage I 135 (23.9%), stage II 173 (30.6%), stage III 54 (9.6%), stage IV 8 (1.4%), and recurrent 20 (3.5%). The mean follow-up was 65.4 months (range, 23.7–86.3 months). Five patients were lost to follow-up.
Results: Thirty-one patients developed a LR during the follow-up including five who received adjuvant radiation. The distribution of LR stratified by cancer stage was stage 0 1, stage I 5, stage II 17, stage III 6, and recurrent 2. The overall LR was 5.5%. Twenty-four patients (77.4%) developed a systemic relapse and 7 (22.6%) patients remained free of recurrent disease at a mean follow-up of 78.1 months. The cancer stage of those remaining disease free was stage 0 1 (100%), stage I 4 (80%), and stage II 2 (11.8%).
Conclusions: LR of breast cancer after SSM is not always associated with systemic relapse.
Key Words: Breast • Cancer • Skin-sparing mastectomy • Recurrence
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INTRODUCTION
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Skin-sparing mastectomy (SSM) is increasingly used to treat patients with breast cancer. It removes the breast, nipple-areola complex, previous biopsy incisions, and skin overlying superficial tumors.1 Preservation of the inframammary fold and native skin greatly enhances the aesthetic results of immediate breast reconstruction (IBR). Early data indicate that the local recurrence (LR) rate is similar to conventional mastectomy.2,3 Long-term follow-up of the use of SSM in the treatment of breast cancer is presented to determine the impact of LR on survival.
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PATIENTS AND METHODS
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A retrospective review of 539 consecutive patients treated for 565 cases of breast cancer by SSM and immediate reconstruction from January 1, 1989 to December 31, 1998 at Emory University Hospital was performed. Individual records were analyzed for demographic, oncologic, and reconstructive data. The American Joint Committee on Cancer staging system for breast cancer was used. A SSM removed the breast, nipple-areola complex, skin overlying superficial tumors, and previous incisions. The native skin envelope and inframammary fold were preserved. During the study period, sentinel lymph mapping was only used in conjunction with axillary dissection.
Types of SSM
The type of SSM was classified by the type of incision used and the amount of skin removed (Fig. 1).2 A type I SSM was commonly used in cases of nonpalpable cancer diagnosed by needle biopsy. A lateral extension of the incision was sometimes necessary to improve exposure to the axillary tail. A type II SSM was used when a superficial tumor or previous biopsy was in proximity to the areola. Type III SSM was used when the superficial tumor or previous incision was remote from the areola. A type IV SSM was used in large, ptotic breasts when a reduction was planned on the opposite breast.
Statistical Analysis
Descriptive statistics were compiled to characterize the patient population. Nonparametric Wilcoxon rank sum tests were used to determine factors associated with the length of disease-free interval among patients who experienced LR. The primary analysis was restricted to patients who experienced LR within 36 months or who were free of LR after at least 36 months of follow-up. 
2 tests of association were applied to determine factors univariately associated with the 36-month recurrence rate. For multivariable analysis, a logistic regression model was used to assess which significant variables were independent predictors. All analyses were carried out via the SAS statistical software package (SAS Institute, Inc., Cary, NC).
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RESULTS
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The mean patient age at cancer diagnosis was 48.4 years. The AJCC pathological staging for the 565 cases of breast cancer was stage 0 175 (31%), stage I 135 (23.9%), stage II 173 (30.6%), stage III 54 (9.6%), stage IV 8 (1.4%), and recurrent 20 (3.5%) (Fig. 2). The mean follow-up was 65.4 months (median, 61.6 months). Five patients were lost to follow-up. The distribution of SSM types was type I 186 (33%), type II 292 (52%), type III 40 (7%), and type IV 47 (8%). There was no correlation between the type of SSM performed and the tumor stage by pairwise analysis.
Adjuvant Radiotherapy
Adjuvant radiotherapy was administered in 43 cases. It was administered for large tumors, those with close margins, and those with four or more lymph nodes involved with metastatic disease. The distribution of adjuvant radiation by stage was stage II 20, stage III 20, and stage IV 3. The number of metastatic lymph nodes involved was >3 in 29 cases (67.4%) receiving adjuvant radiation. Fifteen (75%) of the cases of stage II tumors who received radiation had >3 lymph nodes involved, compared with 11 cases (55%) of stage III tumors and 3 cases (100%) of stage IV tumors.
LR
Thirty-one patients developed a LR during the follow-up period. Isolated LRs were treated with surgical resection and radiotherapy if not previously administered. The distribution of LR stratified by tumor stage is depicted in Table 1. Nineteen patients (61.3%), who recurred locally, died of disease, 5 (16.1%) were alive with disease, and 7 (22.6%) had no evidence of recurrent disease at the time of last follow-up. The disease status at the time of last follow-up stratified by tumor stage is depicted in Table 2. The mean follow-up for patients with no evidence of disease after treatment of a LR was 78.1 (55.2–103.8) months. LRs occurred in five patients (11.6%) who had received radiotherapy (Table 3). All three patients with stage II disease who underwent radiation and recurred had greater than three lymph nodes involved with metastases as did one of the two patients with stage III disease.
Disease-Free Interval
The mean disease-free interval of those that recurred locally was 19.8 months (range, 2.9–61.6 months). The mean disease-free interval stratified by tumor stage is depicted in Table 4. Nonparametric tests were performed to see if any factors were associated with the length of the disease-free interval among the 31 patients with LR. A statistically significant association was detected only for grade and the administration of adjuvant radiotherapy (Table 5).
Univariate Analysis
Pairwise analysis of various factors related to LR was examined by 2 test (Table 6). Nodal stage was stratified into three groups: no nodal involvement, one to three lymph nodes involved, and greater than three lymph nodes involved. Cancer stage was stratified using stages I–III because of the low recurrence in the stage 0 group and the small sample size (n = 4 and n = 2, respectively) in the stage IV and recurrent group.
Multivariate Analysis
In the pairwise associations, all of the variables except SSM type were significant predictors of local recurrence within 36 months. Because of the extremely low recurrence rate in the stage 0 group, it was dropped from the multivariate analysis. Groups were formed in an attempt to account for all of the categories for each risk factor (Table 7). The +LNs > 3 group was compared with +LNs 
3 group, holding all other variables constant. The stage II group is compared with stage I tumors as is the combined stage III/IV group. Tumor grade and the presence of lymphovascular invasion were independent predictors of LR.
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DISCUSSION
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Histological examination of LRs after mastectomy for cancer rarely shows identifiable breast tissue. Much of the early surgical literature associated locoregional relapse with inadequate surgical technique. Recurrences were felt to result from tumor left behind at the time of surgery. Despite varying surgical approaches, the locoregional recurrence rate after total mastectomy for breast cancer has remained relatively constant over the years. It is clear that other factors are involved as the dominant predictors of LRs. The stage of the tumor at the time of excision, including size and nodal involvement predict locoregional recurrences (Table 6). More advanced stages have a more rapid local relapse as depicted in Table 4. In the present study, the mean time to the appearance of clinically overt local disease was 10.8 to 25.9 months depending on the tumor stage. The LRs developed in the skin and subcutaneous tissue and were detected on clinical examination. It could not be determined if the LRs would have been encompassed by traditional mastectomy incisions. It has been reported that disseminated disease almost invariably follows locoregional recurrence after total mastectomy. Gilliland et al. reviewed 60 patients with isolated LR of breast cancer.4 All of the patients eventually died of metastatic breast cancer. This suggested that LR is rarely an isolated event that can be ascribed to inadequate surgical excision but rather represents a component of wide spread relapse.
There have been several reports addressing LR after SSM. Slavin et al. reviewed 51 patients treated for breast cancer (ductal carcinoma-in-situ [DCIS] 26, invasive 25) by SSM and IBR.5 One LR (2%) was noted in a patient with stage I disease with a mean follow-up of 45 months. Newman et al. found LRs in 23 of 372 patients (6.2%) with T1/T2 tumors treated by SSM and immediate reconstruction.3 The median follow-up was 26 months after LR with 14 (61%) of the patients being alive without evidence of recurrence. The authors concluded that the LR rate with SSM is low and that the likelihood of survival is high.
LR of DCIS after mastectomy has been reported. The patient in this series who recurred had an intermediate grade lesion with necrosis. The mammogram at the time of SSM did not reveal diffuse microcalcifications. Rubio et al. reviewed 95 patients treated with SSM and IBR for DCIS.6 LRs were noted in three patients (3%) at a median follow-up of 3.7 years. One of the recurrences appears to be isolated, one patient had systemic disease failure, and one patient was lost to follow-up.
The above-mentioned studies all had relatively short follow-up, which prevented any definitive conclusions regarding long-term prognosis. The present study, with a median follow-up of 65.4 months, confirms that there is a subset of patients with early disease who can be salvaged with aggressive local treatment after LR. The mean follow-up of the seven patients who have remained free of distant recurrence after LR was 78.1 months. Surgical conservatism may play a role in isolated LRs in patients with early-stage disease treated by SSM.
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CONCLUSIONS
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LRs after SSM are influenced by advanced tumor stage and the absence of estrogen receptor expression. High-tumor grade and lymphovascular invasion are independent predictors of LR. LR of breast cancer after SSM is not always associated with systemic relapse. Patients with early-stage disease may be salvaged with surgical resection and radiotherapy.
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Footnotes
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A total of 539 patients were treated for 565 cases of breast cancer by skin-sparing mastectomy (SSM). Local recurrences developed in 31 cases. Seven (22.6%) patients remained free of recurrent disease at a mean follow-up of 78.1 months. Local recurrence of breast cancer after SSM is not always associated with systemic relapse.
Received for publication March 19, 2002.
Accepted for publication October 23, 2002.
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REFERENCES
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- Carlson GW. Skin sparing mastectomy: anatomic and technical considerations. Am Surg 1996; 62: 151–5.[Medline]
- Carlson GW, Bostwick J III, Styblo TM, et al. Skin-sparing mastectomy. Oncologic and reconstructive considerations. Ann Surg 1997; 225: 570–5.[CrossRef][Medline]
- Newman LA, Kuerer HM, Hunt KK, et al. Presentation, treatment, and outcome of local recurrence after skin-sparing mastectomy and immediate breast reconstruction. Ann Surg Oncol 1998; 5: 620–6.[Abstract]
- Gilliland MD, Barton RM, Copeland EM. The implications of local recurrence of breast cancer as the first site of therapeutic failure. Ann Surg 1983; 197: 284–7.[Medline]
- Slavin SA, Schnitt SJ, Duda RB, et al. Skin-sparing mastectomy and immediate reconstruction: oncologic risks and aesthetic results in patients with early-stage breast cancer. Plast Reconstr Surg 1998; 102: 49–62.[Medline]
- Rubio IT, Mirzan N, Sahin AA, et al. Role of specimen radiography in patients treated with skin-sparing mastectomy for ductal carcinoma in situ of the breast. Ann Surg Oncol 2000; 7: 544–8.[Abstract]
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ABSTRACT
INTRODUCTION
