Annals of Surgical Oncology 10:628-634 (2003)
© 2003 Society of Surgical Oncology
Chest Wall Recurrence After Mastectomy Does Not Always Portend a Dismal Outcome
Anees Chagpar, MD, MSc,
Funda Meric-Bernstam, MD,
Kelly K. Hunt, MD,
Merrick I. Ross, MD,
Massimo Cristofanilli, MD,
S. Eva Singletary, MD,
Thomas A. Buchholz, MD,
Frederick C. Ames, MD,
Sylvie Marcy, BSN,
Gildy V. Babiera, MD,
Barry W. Feig, MD,
Gabriel N. Hortobagyi, MD and
Henry M. Kuerer, MD, PhD
From the Departments of Surgical Oncology (AC, FM-B, KKH, MIR, SES, FCA, SM, GVB, BWF, HMK), Medical Oncology (MC, GNH), and Radiation Oncology (TAB), The University of Texas M. D. Anderson Cancer Center, Houston, Texas.
Correspondence: Address correspondence and reprint requests to: H. M. Kuerer, MD, PhD, Department of Surgical Oncology, Box 444, The University of Texas M. D. Anderson Cancer Center, 1515 Holcombe Blvd., Houston, TX 77030; Fax: 713-792-4689; E-mail: hkuerer{at}mdanderson.org
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ABSTRACT
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Background: Chest wall recurrence (CWR) after mastectomy often forecasts a grim prognosis. Predictors of outcome after CWR, however, are not clear.
Methods: From 1988 to 1998, 130 patients with isolated CWRs were seen at our center. Clinicopathologic factors were studied by univariate and multivariate analyses for distant metastasis–free survival after CWR. The median post-CWR follow-up was 37 months.
Results: Initial nodal status was the strongest predictor of outcome by univariate analysis. Other significant factors included initial T4 disease, primary lymphovascular invasion, treatment of the primary tumor with neoadjuvant therapy or radiation, time to CWR >24 months, and treatment for CWR (surgery, radiation, or multimodality therapy). Multivariate analysis also found initial nodal status to have the greatest effect; time to CWR and use of radiation for CWR were also independent predictors. Three groups of patients were identified. Low risk was defined by initial node-negative disease, time to CWR >24 months, and radiation for CWR; intermediate risk had one or two favorable features; and high risk had none. The median distant metastasis–free survival after CWR was significantly different among these groups (P < .0001).
Conclusions: Patients with CWR are a heterogeneous population. Patients with initial node-negative disease who develop CWR after 24 months have an optimistic prognosis, especially if they are treated with radiation.
Key Words: Breast cancer • Chest wall recurrence • Prognosis • Mastectomy
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INTRODUCTION
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Chest wall recurrence (CWR) after mastectomy occurs in 5% to 40% of breast cancer patients1–10 and is generally believed to forecast a grim outcome. These recurrences are often followed by distant metastasis9–14 and death.11 As a result, some authors have advocated a palliative approach to the management of patients with CWR after mastectomy.11,15 Others, however, suspect that a subgroup of these patients exists for whom prognosis is not so guarded and for whom aggressive therapy is therefore warranted.16–28
A number of studies have illustrated that survival after CWR is influenced by a multitude of factors.16–30 Although it is widely accepted that the length of the disease-free interval between mastectomy and CWR is a key prognostic variable,16–19,21–23,25–28,30 controversy exists regarding the importance of other factors in determining prognosis. Several studies have indicated that features intrinsic to the type of CWR may affect survival after CWR,16,17,19,22,23,28,29 but the effect of the initial primary tumor features on survival after CWR remains unknown.18,19,28–30 Few multivariate analyses have been published relating to factors that affect outcome after postmastectomy CWR.16–20 As a result, the optimal management of patients with CWR continues to be a topic of debate.
We therefore sought to determine the effect of a number of clinicopathologic variables, including primary tumor features, on overall survival and distant metastasis–free survival (DMFS) in patients with CWR after mastectomy. We also investigated the effects of various treatment modalities on overall survival and DMFS in such patients.
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METHODS
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Between 1988 and 1998, 155 patients who had previously undergone mastectomy for breast cancer presented at our institution with CWR. CWR was defined as a pathologically confirmed recurrence of breast cancer that occurred in the skin, subcutaneous tissue, or muscle of the chest wall with or without accompanying nodal metastases. Of the 155 patients with CWR, 25 had synchronous distant metastases. These patients were excluded from our analysis. The charts of the remaining 130 patients with CWR with or without associated nodal disease were reviewed. This study was approved by The University of Texas M. D. Anderson Cancer Center Institutional Review Board.
The following factors were recorded: primary tumor features (including tumor size, nodal status, tumor grade, margin status, presence of lymphovascular invasion, estrogen- and progesterone-receptor status, and clinical features suggestive of inflammatory carcinoma); modalities used to treat the primary tumor (neoadjuvant therapy; adjuvant systemic therapy, including hormonal therapy and chemotherapy; and adjuvant radiotherapy); time from initial diagnosis of breast cancer to CWR; features of the CWR (including size, erythema, ulceration, number of nodules, and presence of accompanying nodal metastasis); and modalities used to treat the CWR (surgery, systemic therapy, and radiotherapy). Outcome measures were additional CWR, development of distant metastasis, and death.
Factors potentially predicting additional CWR and the development of distant metastatic disease after CWR were assessed by using likelihood ratio tests for discrete variables and Mann-Whitney U-tests for continuous variables. Survival analyses were performed for overall and DMFS after CWR. Univariate survival analyses were performed with the Kaplan-Meier method, and multivariate survival analyses were performed with Cox regression. Distinct groups of patients were identified on the basis of factors shown to be significant predictors of DMFS on multivariate analysis. All statistical analyses were performed with SPSS version 10.1 (SPSS Inc., Chicago, IL).
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RESULTS
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Patient Demographics
The median age at initial diagnosis of breast cancer was 49 ± 12 years (range, 25–80 years); 68 patients (52.3%) were 50 years of age or younger. Ninety-eight patients (75.4%) were white, 17 (13.1%) were Hispanic, 11 (8.5%) were black, and the remaining 4 (3.0%) were of unspecified ethnicity.
Primary Tumor Characteristics and Treatment
Primary tumor characteristics for the entire cohort are listed in Table 1. The median primary tumor size was 2.80 cm, with an SD of 1.97 cm.
Thirty-one patients (23.8%) were treated with neoadjuvant systemic therapy. Twenty-five patients (19.2%) underwent breast reconstruction after mastectomy. Eighty-five patients (65.4%) were treated with adjuvant systemic therapy (chemotherapy, hormonal therapy, or both). Twenty-eight patients (21.5%) received postmastectomy radiotherapy.
CWR Characteristics and Treatment
The median time from initial diagnosis of breast cancer to CWR was 25.5 months (range, .4–340 months); 58 patients (45.4%) presented within 24 months of diagnosis of their primary tumor. The median age at diagnosis of CWR was 52.4 years, with an SD of 11.9 years. The median size for CWR was 1.8 cm, with an SD of 2.6 cm. Seventy-eight patients (60%) had uninodular recurrences, and 25 (19.2%) had multinodular recurrences; in the remaining 27 patients (20.8%), the number of nodules was not specified. In most cases, the CWR was not ulcerated (122 patients; 93.8%) and was not erythematous (111 patients; 85.4%). In only six cases (4.6%) was the CWR associated with concomitant nodal metastasis.
Four patients (3.1%) refused any treatment of their CWR. The remaining 126 patients were treated with surgery, radiotherapy, systemic therapy, or a combination of these modalities (Table 2).
Follow-Up
The median follow-up time after the initial diagnosis of breast cancer was 68.5 months (range, 10.4–368.4 months), and the median follow-up time after diagnosis of CWR was 37.4 months (range, 2.9–166.8 months). The median follow-up time for surviving patients was 93.3 months (range, 27.6–368.4 months) after diagnosis of the primary tumor and 43.3 months (range, 5.4–166.8 months) after diagnosis of the CWR. At the time of their last follow-up, 41 patients (31.5%) were alive with no evidence of disease, 25 (19.2%) were alive with disease, and 64 (49.2%) had died of disease.
Additional CWRs
Twenty-nine patients (22.3%) had an additional CWR. The median interval between diagnosis of the first and second CWRs was 16.6 months (range, 5.1–84.27 months). Univariate analyses of primary tumor characteristics, primary tumor treatment factors, time to CWR, characteristics of CWR, and treatment of CWR did not demonstrate any factors significantly predictive of an additional CWR.
Distant Metastases
Of the 130 patients in our series, 67 (51.5%) never developed distant metastatic disease. Among the 63 (48.5%) who did manifest metastatic disease, the distribution of distant sites of disease was as follows: bone, n = 23 (17.7%); supraclavicular nodes, n = 12 (9.2%); lung, n = 10 (7.7%); liver, n = 8 (6.2%); brain, n = 6 (4.6%); and other sites, n = 4 (3.1%). The median time from initial diagnosis of breast cancer to distant metastasis was 44.2 months (range, 10.3–315.5 months), and the median time from the CWR to distant metastasis was 17.2 months (range, 0–119.2 months). Univariate analyses revealed that positive nodal status was the only factor predictive of distant metastasis after CWR (P = .027).
Overall Survival
The actuarial 5- and 10-year overall survival rates (±SD) after CWR for the entire cohort were 47.8% ± 5.2% and 29.3% ± 6.7%, respectively; the median overall survival after CWR was 59 ± 12 months. Univariate analyses of a number of factors were performed by using the method of Kaplan and Meier for overall survival after CWR. Results for primary tumor characteristics and treatment of the primary tumor are listed in Table 3. Results for CWR characteristics and treatment of the CWR are listed in Table 4. A Cox multiple regression analysis was performed with the variables identified as significant on univariate analysis. The factors that emerged as significant predictors of worse overall survival were positive initial nodal status (odds ratio [OR], 4.61; 95% confidence interval [CI], 1.93–11.01; P = .001), lack of radiotherapy for treatment of CWR (OR, 3.69; 95% CI, 1.48–9.22; P = .005), time to CWR of 
24 months (OR, 2.50; 95% CI, 1.04–6.02; P = .041), and use of adjuvant systemic therapy for treatment of the primary tumor (OR, 2.27; 95% CI, 1.01–5.12; P = .047).
Distant Metastasis–Free Survival
The 5- and 10-year actuarial DMFS rates after CWR for the entire cohort were 41.4% ± 5.4% and 28.1% ± 6.9%, respectively; the median DMFS (±SD) was 40 ± 8 months. Univariate Kaplan-Meier analyses for a variety of factors were performed for DMFS after CWR. Results for primary tumor characteristics are listed in Table 5, and results for CWR characteristics and treatment are listed in Table 6. By using the factors identified as significant on univariate analysis, a Cox multivariate analysis was performed. The only factors that remained statistically significant predictors of poor DMFS were positive initial nodal status (OR, 3.13; 95% CI, 1.57–6.27; P = .001), lack of radiotherapy for treatment of the CWR (OR, 2.72; 95% CI, 1.36–5.43; P = .005), and time to CWR of 24 months (OR, 2.43; 95% CI, 1.29–4.58; P = .006).
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TABLE 5. Distant metastasis–free survival after chest wall recurrence according to primary tumor characteristics and treatment
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TABLE 6. Distant metastasis–free survival after chest wall recurrence (CWR) according to CWR characteristics and treatment
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Stratification of Patients by Prognosis
By using the three features that were found on multivariate analysis to be significant predictors of both overall survival and DMFS after CWR, three patient groups were identified: (1) a low-risk group (n = 19), defined as having all three favorable features (node negative, CWR >24 months after diagnosis of the primary tumor, and receipt of radiotherapy for CWR); (2) an intermediate-risk group (n = 89), with one or two of these features; and (3) a high-risk group (n = 22), with none of these favorable features. Kaplan-Meier analyses for overall survival and DMFS were then performed, stratifying for these risk groups. The median overall survival times after CWR for the low-, intermediate-, and high-risk groups were 141 ± 13 months, 54 ± 13 months, and 16 ± 2 months, respectively (P < .001). The corresponding 5-year actuarial overall survival rates were 86.1% ± 9.4%, 47.5% ± 6.2%, and 0%, respectively, and the 10-year actuarial overall survival rates were 75.4% ± 13.0%, 25.1% ± 7.8%, and 0%, respectively (P < .001). Similarly, the median DMFS times were 132 ± 14 months for the low-risk group, 39 ± 10 months for the intermediate-risk group, and 11 ± 3 months for the high-risk group (P < .001). The corresponding 5-year actuarial DMFS rates were 79.5% ± 11.3%, 40.6% ± 6.4%, and 0%, respectively, and the 10-year actuarial DMFS rates were 79.5% ± 11.3%, 23.4% ± 7.9%, and 0%, respectively (P < .001). The survival curves for overall survival and DMFS are shown in Figs. 1 and 2
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FIG. 1. Overall survival after chest wall recurrence (CWR) for low-, intermediate-, and high-risk groups.
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FIG. 2. Distant metastasis–free survival after chest wall recurrence (CWR) for low-, intermediate-, and high-risk groups.
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DISCUSSION
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CWR after mastectomy poses a challenge for the clinician. Although patients with CWR after mastectomy are often believed to have a bleak prognosis, these patients are a heterogeneous population. We, along with other investigators, have previously demonstrated that long-term survival after CWR is possible in some patients. However, a distinct population of patients with an optimistic prognosis had not until now been clearly defined. In the study reported here, we demonstrated that initially node-negative patients who developed a CWR >24 months after diagnosis of their primary tumor had a relatively favorable prognosis, especially if they were treated with radiotherapy, compared with patients with CWR without these features.
Although a number of factors, including primary tumor size, nodal status, positive margins, tumor grade, and lymphovascular invasion, have been reported to predispose to the development of CWR after mastectomy,31 controversy still exists regarding the effect of these features on prognosis after CWR. We found that positive initial nodal status was the only significant factor predisposing to the development of distant metastatic disease after CWR, and we found that this factor was of paramount importance in determining survival. This finding has been debated in the literature: some have concluded that initial nodal status plays a role in post-CWR prognosis,16,17,20–24,26,27 and others have found the opposite.18,19,25,28,30
Our finding that time to CWR was an important factor in determining post-CWR survival is in agreement with most previously published studies.16–19,21–23,25–28,30 Whether the effect of time to CWR is a direct result of the initial tumor biology or residual disease remains an issue of contention. Some authors have reported that characteristics of the CWR itself (such as the number of nodules, size of CWR, and location of CWR) may be important in determining survival after CWR,16,17,19,22,23,28,29 whereas others have not found this to be the case.18,20,21,24–27 In this study, we found that none of the factors intrinsic to the CWR itself were statistically significant predictors of overall survival or DMFS in multivariate analysis. Indeed, the lack of multivariate analyses with large numbers of patients has clouded the issue of which prognostic variables are truly significant in determining survival after CWR. Most studies used only univariate methods of statistical analysis,21–30 and all of the prior multivariate analyses included patients with isolated nodal recurrences as part of their study population.16–20
In addition to initial nodal status and time to CWR, we found that the development of CWR after treatment of the primary tumor with adjuvant systemic therapy forecasted a worse outcome in terms of overall survival after CWR. This is in keeping with the findings of Mora et al.18 It is important to recognize that our study, like that of Mora et al., was retrospective and could not control for the choice of therapy. Therefore, it is quite possible that patients who were believed to have a worse prognosis were more likely to receive adjuvant systemic therapy. This factor, however, did not maintain its significance in the analysis of DMFS. One possible explanation is not that CWRs that occur after systemic therapy necessarily cause a more rapid appearance of distant metastases, but rather that metastases, when they appear, are more likely to be resistant to therapy and, therefore, result in shorter postmetastasis survival. This is an interesting finding and one that deserves further study.
We also found that radiotherapy was of paramount importance in the treatment of patients with CWR and was associated with significantly prolonged survival. Appropriate treatment of CWR has been a topic of debate in the literature, and, again, few large studies have examined the effect of each treatment modality on survival. Our important finding regarding radiotherapy should prompt clinicians to consider using this modality when possible in the setting of postmastectomy CWR. At the M. D. Anderson Cancer Center, it is currently our standard practice to treat all patients with CWR with radiotherapy unless there is an obvious contraindication.
Some data in the literature suggest that treating patients with postmastectomy CWR with both systemic therapy and irradiation may be of benefit.32,33 Our retrospective study was not designed specifically to study this issue and, in fact, could not have shown a significant survival difference based on systemic therapy because most of the patients in the series were treated with some form of systemic therapy, reflecting the contemporary philosophy of the liberal use of this modality.
Further studies are warranted to analyze the effect of clinicopathologic variables in the setting of isolated CWR after mastectomy and the role of various modalities in the optimal treatment of patients with CWR. This study, however, should serve to aid clinicians in identifying a subset of patients for whom long-term survival after CWR is possible and in whom aggressive management, including radiotherapy, is warranted. In addition, this model of identifying patients with different outcomes after CWR may also be useful in stratifying patients in clinical trials designed to test or compare therapies for CWR.
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FOOTNOTES
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Predictors of outcome after chest wall recurrence (CWR) after mastectomy are not well elucidated in the literature. We demonstrated the effect of primary tumor features on survival after CWR and defined groups of patients with significantly different outcomes.
Received for publication January 2, 2003.
Accepted for publication March 4, 2003.
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ABSTRACT
INTRODUCTION
