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Journal of Clinical Oncology, Vol 25, No 9 (March 20), 2007: pp. 1089-1098 © 2007 American Society of Clinical Oncology. DOI: 10.1200/JCO.2006.09.1710 Racial Disparities in Treatment and Survival of Male Breast Cancer
From the Department of Medicine and the Herbert Irving Comprehensive Cancer Center, College of Physicians and Surgeons; and the Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, NY Address reprint requests to Dawn L. Hershman, MD, MS, Columbia University, 161 Fort Washington Ave, 10-1068, New York, NY 10032; e-mail: dlh23{at}columbia.edu
Purpose: Black women with breast cancer have poorer survival than do white women, but little is known about racial disparities in male breast cancer. We analyzed race and other predictors of treatment and survival among men with stage I-III breast cancer. Patients and Methods: We used the Surveillance, Epidemiology, and End Results (SEER) Medicare database to identify men 65 years of age or older diagnosed with stage I-III breast cancer from 1991 to 2002. Multivariate regression was used to compare those treated with those not treated with either chemotherapy or radiation therapy, adjusting for known clinical and demographic factors. Cox proportional hazards regression models were used to analyze survival. Results: Of 510 male breast cancer cases (456 white, 34 black), 94% underwent mastectomy, 28% received adjuvant chemotherapy, and 29% received radiation therapy. Among those with known hormone receptors, 95% had hormone-sensitive tumors. In a multivariate analysis, chemotherapy was associated with younger age, advanced stage, and hormone receptor–negative tumors. Radiation therapy was associated with younger age and advanced stage. Black men were approximately 50% less likely to undergo consultation with an oncologist and subsequently receive chemotherapy; however, the results did not reach statistical significance. The breast cancer–specific mortality hazard ratio was more than tripled for black versus white men (hazard ratio = 3.29; 95% CI, 1.10 to 9.86). Conclusion: After adjustment for known clinical, demographic, and treatment factors, there was an association of black race with increased male breast cancer–specific mortality. Although male breast cancer is rare, the reasons for these disparities need to be better understood.
Male breast cancer (MBC) is a rare disease; it accounts for less than 1% of all breast cancers and less than 1% of malignancies in men,1 but its incidence has been increasing.2,3 In 2006, an estimated 1,700 new cases of MBC will be diagnosed, and approximately 400 men will die as a result of this disease.4 The male-to-female breast cancer incidence ratio is higher among black patients than among white patients,5 and black men have higher age-adjusted incidence rates (1.65/100,000) than do white men (1.31/100,000).6 Black women also have higher breast cancer incidence rates than do white women before age 45 years, but lower rates at older ages. At all ages, black women with breast cancer have higher mortality rates. Some of the disparity in survival is attributable to differences in stage distribution at diagnosis, but it is present even within stage.7,8 Black women's breast cancers are also more likely than white women's to have unfavorable biologic parameters, such as negative estrogen-receptor status, high nuclear grade, and high S-phase fraction.8,9 However, studies indicate that significant differences in survival remain even after controlling for stage and biologic factors.10,11 Small studies of racial disparities in MBC have been similar to those in female breast cancer.12 Optimal management of breast cancer in men has been difficult to determine because the rarity of this disease makes randomized trials impractical. Retrospective analyses of small series of patients with node-positive MBC treated with adjuvant chemotherapy have reported 5-year survival rates of 80% to 85%, substantially better than those of historical controls.13-17 Similarly, several studies suggest that radiation therapy reduces the risk of local recurrence, but does not affect overall survival.15,18 Without established criteria for adjuvant treatment, men with breast carcinoma may be more likely to receive suboptimal treatment.19 To our knowledge, this article is the first to investigate factors, including race, that may predict the use of adjuvant chemotherapy and radiation therapy and the outcomes of such treatment among elderly men diagnosed with early-stage breast cancer.
Data Source The Surveillance, Epidemiology, and End Results (SEER) cancer registry provides information on tumor site, histology, stage, and individual demographic information, as well as primary surgical and radiation treatment and survival outcomes, for cancers occurring in approximately 14% of the US population. In 2000, the number of sites was increased to represent 24% of the US population. The Medicare claims files contain diagnostic and treatment data for patients on Medicare.20 We used the linked SEER-Medicare database for our analyses.
Sample Selection Medicare claims data were used to determine initial consultation with either a medical oncologist or radiation oncologist. Using the Health Care Financing Administration's (HCFA's) national Common Procedure Coding System (HCPCS), we identified patients who had received a specified chemotherapeutic drug within 120 days after their cancer diagnosis according to the information collected in their physician claims files, hospital outpatient claims files, or Medicare provider review files. First, we searched for cyclophosphamide (J9070, J9080, J9090-97), methotrexate (J8610, J9250, J9260), fluorouracil (J9190), doxorubicin (J9000, J9001), and paclitaxel (J9265). Then, we searched by level II HCPCS codes (J9XXX, 964XX, 965XX, Q0083-85); International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM) diagnostic codes (V581, V662, E9331, E9307); and procedure codes (9925) from physician claims files or outpatient or admission hospital claims for evidence of chemotherapy delivery. Among patients who did not have specific J9XXX chemotherapy HCPCS codes, these codes were used to capture any evidence that an unspecified chemotherapeutic drug was given during the 120 days after diagnosis. Radiation therapy was defined by claims data within 12 months of diagnosis to avoid including patients who received palliative treatments for metastatic disease.
Sociodemographic and Clinical Variables We generated an aggregate socioeconomic status (SES) score from a hierarchy of income data from the 2000 census from a method adapted from Kreiger at al.24 Patients were ranked on a 1 to 5 scale, with 1 as the lowest value, based on a formula incorporating census tract median income, ZIP code median income, census per-capita income, and ZIP code per-capita income; patients for whom all of these values were missing were assigned to the lowest SES category. To assess the prevalence of comorbid disease in our cohort, we used the Klabunde adaptation of the Charlson comorbidity index.25 All relevant ICD-9 diagnosis codes, ICD-9 procedure codes, and HCPCS procedure codes within hospital claim files and physician claim files were searched to identify individuals with a history of these selected comorbidities from 365 days before to 120 days after diagnosis of cancer. Each category was weighted based on the Charlson index.
Outcome Assessment
Statistical Analysis
Baseline Descriptive Statistics We identified 510 men, ages 65 years or older, with stage I-III breast cancer diagnosed between 1991 and 2002 (Table 1). The median follow-up was 58.5 months, and 242 men died during the follow-up period, including 215 deaths (47%) among white patients and 18 deaths among black patients (53%). There were 39 breast cancer–specific deaths among white patients (12.7%) and eight (30.8%) among black patients. The oldest patient at diagnosis was 103 years, and the median age was 76 years. Most of the patients in the sample were non-Hispanic white (89.4%), and most resided in central and fringe counties of metropolitan areas with populations greater than 250,000 (92.9%). The stage distribution of breast cancer was 36.9% stage I, 38.4% stage IIa, 14.3% stage IIb, and 10.4% stage III. The distribution by HR status was 4% negative, 71% positive, and 25% unknown.
The overwhelming majority of patients (94%) underwent mastectomy; only 30 (6%) had a lumpectomy. Approximately 28% received adjuvant chemotherapy, and 29% received radiation therapy. Of those who received chemotherapy, 63.2% received cyclophosphamide, 30.4% doxorubicin, and 21.4% a taxane. Black men were more likely to have advanced-stage disease (P = .04) and larger tumor sizes (P = .01) compared with white men. A higher proportion of black compared with white men had positive lymph nodes (45% v 34%), poorly differentiated tumors (44% v 32%), and a comorbidity score more than 0 (53% v 38%), but those differences were not statistically significant (Table 1).
Predictors of Adjuvant Treatment
Both consultation with a radiation oncologist and receipt of radiation therapy were associated with stage at diagnosis, lymph node status, and tumor grade. Being diagnosed at a teaching hospital was associated with seeing a radiation oncologist but not with receiving radiation therapy (Table 4). Patients diagnosed in the late 1990s were more likely to see a radiation oncologist and to receive radiation therapy than were those diagnosed earlier. In a multivariate logistic regression model, younger patients, those with more advanced stage, and those diagnosed more recently were more likely to receive radiation (Table 3).
Patients did not differ by race in likelihood of referral or receipt of chemotherapy or radiation therapy (Tables 2 and 4). After adjustment for known clinical and demographic factors, we found that black men were approximately 48% less likely to be referred to a medical oncologist and 56% less likely to receive chemotherapy, but these differences were not statistically significant (Table 3).
Mortality and Survival
We found that, among elderly male Medicare recipients with stage I-III breast cancer, younger age, advanced stage, and HR-negative status appropriately influenced decisions regarding chemotherapy and radiation therapy use. After controlling for clinical and demographic characteristics, patients who received adjuvant chemotherapy or radiation therapy did not have better overall or breast cancer–specific survival than patients who did not receive these therapies. However, of the 510 patients in the sample, only 145 received chemotherapy and 150 radiation. Nearly 80% of those patients had stage II or III disease, and, therefore, a worse prognosis. Therefore, because these patients who received treatment also had worse disease, our ability to detect small treatment effects may have been obscured. Similar to racial disparities in female breast cancer, black men also had higher BCM compared with white men. The medical literature regarding breast cancer in men consists mainly of small, single-institution, retrospective series. Because male breast cancer is rare, treatment strategies are not based on randomized clinical trials, but on extrapolation from trials with female subjects. However, men with breast cancer are older, are more likely to have HR-positive tumors, and present with more advanced stage than women do with breast cancer.1 Clinical outcomes are comparable between men and women with breast cancer when matched for age and stage.18,27 However, men have lower overall survival rates compared with women, likely due to later stage at presentation, more advanced age, and high rates of death from comorbid illnesses.28 A French study found that 40% of male breast cancer patients died as a result of intercurrent illness.18 Among female patients in the SEER-Medicare database, only approximately 10% to 15% receive adjuvant chemotherapy for breast cancer,29,30 and only 11% receive postmastectomy radiation.31 In our sample of MBC patients, of whom 71% had hormone-sensitive tumors, nearly 30% received at least one of those treatments, perhaps because of their later stage of presentation, or other unmeasured factors. Treatment has been found to improve the survival of elderly women only if they are HR negative and lymph node positive.30,32 However, one of the limitations of our study is that, among 34 black men included in this sample, only eight men received adjuvant chemotherapy, and there were eight breast cancer–specific deaths. Our small sample size may have limited our ability to observe a survival benefit in a comparable subset of men. In our sample, black men were about half as likely to consult with a medical oncologist and receive adjuvant chemotherapy as were white men. These results may have not reached statistical significance because our sample included only 34 black men. Black men had a greater than three-fold increased risk of dying as a result of their breast cancer compared with white men. Similar findings have been observed in women with breast cancer.33 In another population-based study of male breast cancer patients, 5-year survival rates were 66% for white men and 57% for black men.12 Racial disparities in breast cancer outcomes between black and white women have been attributed to advanced stage at diagnosis, negative HR status, higher tumor grade, reduced access to health care, and other socioeconomic factors.34-36 Similar factors may contribute to the poor outcomes we observed among black men with breast cancer. Some of the effects of race on survival may result from suboptimal treatment. Studies by our group and others have suggested that black women are less likely to receive optimal systemic adjuvant breast cancer therapy than are white women.37-39 The disparity in outcomes became more pronounced in the late 1980s, corresponding to the increased use of mammographic screening and the introduction of adjuvant therapy for this disease.40 Only 50% of black women who may be eligible for adjuvant chemotherapy are estimated to be receiving it.7 Treatment delays also appear to contribute to worse outcomes among black women.41,42 We were among the first to report that undertreatment contributed to the association of race with survival in women with breast cancer.43 Studies in other malignancies have found differences by race in subspecialty referrals,44-46 access to lung cancer surgery,47 prostate cancer surgery,48,49 treatment for colorectal cancer,50-52 and use of chemotherapy for metastatic lung cancer.53 Determinants of suboptimal cancer treatment may include inadequate physician-patient communication, treatment-related toxicity, racial differences in drug metabolism, social support networks, comorbidities, and other factors. One limitation of our study is that it included only patients 65 years of age or older. However, in the United States, male breast cancer is predominantly a disease of elderly men. The median age at diagnosis in men is 68 years, compared with 63 years in women.54 Older patients are less likely to receive the standard treatment for cancer.55 Data about the effects of adjuvant chemotherapy for breast cancer among women older than 70 years are sparse because only small numbers of women over age 70 have been included in controlled trials.56 Population-based studies have shown a benefit of adjuvant chemotherapy in elderly women with HR-negative tumors.30 Studies by our group have shown that advanced age is inversely associated with referral to radiation oncologists and medical oncologists, receipt of radiation and chemotherapy once referred, and delay in initiating radiation and chemotherapy.33,57 Because Medicare does not bill for oral therapies, we were unable to investigate the use of adjuvant hormonal therapy. Carcinomas of the male breast are more likely to be HR sensitive than are female breast cancers. In a large population-based cohort, more than 90% of breast cancers in men were estrogen-receptor positive and 81% were progesterone-receptor positive, compared with 76% and 67%, respectively, in women.2 The decrease in case fatality rate from breast cancer in most developed countries is due, at least in part, to the use of adjuvant hormonal therapy. The Early Breast Cancer Trialists’ Collaborative Group overview of randomized trials of adjuvant tamoxifen showed that during approximately 15 years of follow-up, 5 years of tamoxifen reduced the annual breast cancer death rate by 31%.58 Given the high prevalence of HR positivity in male breast cancers, these patients may derive more benefit from adjuvant hormonal therapy than from chemotherapy. Several population-based studies of elderly women with breast cancer indicate that 85% of those with hormone-sensitive tumors initiate hormonal therapy.59 In our sample, 72% of white men but only 56% of black men had hormone-sensitive tumors, and 24% of white men but 38% of black men had unknown hormone status. Given their adverse staging and hormone status, black men should have been more likely than white men to receive chemotherapy. Undertreatment may, therefore, account for the racial disparity in breast cancer–specific survival among men. The decision about whether to pursue adjuvant cancer treatments involves judgment on the part of the physician, patient preferences, cultural beliefs, and the overall functional status of the patient. A major limitation of our study is the absence of data on performance status or functional impairment. Performance status has been linked to cancer survival,60,61 and is also likely to be associated with the decision to treat with adjuvant chemotherapy and radiation therapy. In this population-based data set, only a small fraction of elderly men with early-stage breast cancer were treated with adjuvant chemotherapy or radiation therapy. Similar to observations in black women, after controlling for both clinical, treatment, and demographic factors, black men were more likely to die from their breast cancer compared with white men. This study supports more investigation into clinical and biologic factors that contribute to the racial disparities in male breast cancer through other similar population-based registries, cooperative groups, and HMO networks.
The authors indicated no potential conflicts of interest.
Conception and design: Katherine D. Crew, Alfred I. Neugut, George Raptis, Dawn L. Hershman Financial support: Alfred I. Neugut, Dawn L. Hershman Collection and assembly of data: Katherine D. Crew, Xiaoyan Wang, Dawn L. Hershman Data analysis and interpretation: Katherine D. Crew, Alfred I. Neugut, Xiaoyan Wang, Judith S. Jacobson, Victor R. Grann, Dawn L. Hershman Manuscript writing: Katherine D. Crew, Alfred I. Neugut, Judith S. Jacobson, Victor R. Grann, Dawn L. Hershman Final approval of manuscript: Katherine D. Crew, Alfred I. Neugut, Xiaoyan Wang, Judith S. Jacobson, Victor R. Grann, George Raptis, Dawn L. Hershman
This study used the linked Surveillance, Epidemiology, and End Results (SEER) -Medicare database. The interpretation and reporting of these data are the sole responsibility of the authors. The authors acknowledge the efforts of the Applied Research Branch, Division of Cancer Prevention and Population Science, NCI; the Office of Information Services, and the Office of Strategic Planning, Health Care Financing Administration; Information Management Services (IMS) Inc; and the SEER Program tumor registries in the creation of the SEER-Medicare database.
Supported by a National Cancer Institute (NCI) -funded postdoctoral fellowship (T32-CA09529) to K.D.C., a K05 Award (CA89155) and an American Cancer Society grant (RSGT-01-02404-CPHPS) to A.I.N., an American Cancer Society Award (CRTG-98-260-01) to V.R.G., and an K07 Award from the NCI (CA95597) to D.L.H. Authors’ disclosures of potential conflicts of interest and author contributions are found at the end of this article.
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Cancer 94:1961-1967, 2002[CrossRef][Medline] Submitted September 13, 2006; accepted December 18, 2006.
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Copyright © 2007 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
= 0.94) and 94% agreement on whites (
2 tests. Multivariate logistic regression models were created using consultation and receipt of chemotherapy and radiation therapy as the dependent variables, and demographic and clinical characteristics as independent variables. We developed Cox proportional hazards regression models with all-cause and breast cancer–specific mortality (BCM) as the dependent variables. The Kaplan-Meier analysis was used to plot survival curves for elderly black and white men with early-stage breast cancer. 
