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Journal of Clinical Oncology, Vol 24, No 9 (March 20), 2006: pp. 1342-1349 © 2006 American Society of Clinical Oncology. DOI: 10.1200/JCO.2005.03.3472 Meta-Analysis of Survival in African American and White American Patients With Breast Cancer: Ethnicity Compared With Socioeconomic Status
From the University of Michigan, Ann Arbor; Karmanos Cancer Institute, Detroit, MI; Uniformed Services University, Bethesda, MD; Cleveland Clinic Foundation, Cleveland, OH; Brigham and Women's Hospital, Boston, MA Address reprint requests to Lisa A. Newman, MD, MPH, University of Michigan, 1500 E Medical Center Dr, Ann Arbor, MI 48109; e-mail: lanewman{at}umich.edu
PURPOSE: The extent to which socioeconomic disadvantages and inadequate health care access account for the disproportionately elevated mortality hazard observed in African American compared with white American patients with breast cancer is poorly defined. METHODS: We identified 20 studies reported between January 1980 and June 2005 that provided survival analyses in patients with breast cancer after adjusting for ethnicity and some measurement of socioeconomic status. These studies also adjusted for age and stage of disease at time of diagnosis. RESULTS: The pooled outcome data yielded estimates for the mortality hazard in 14,013 African American and 76,111 white American patients with breast cancer. Studies varied in their methods for assigning socioeconomic status, with most relying on area-wide measures such as census tract and census block data. The combined analysis (adjusted for age, stage, and socioeconomic status) revealed that African American ethnicity was associated with a statistically significant excess mortality risk in overall survival (mortality hazard, 1.27; 95% CI, 1.18 to 1.38) and in breast cancer-specific survival (mortality hazard, 1.19; 95% CI, 1.10 to 1.29). CONCLUSION: Our pooled analysis demonstrated that African American ethnicity is a significant and independent predictor of poor outcome from breast cancer, even after accounting for socioeconomic status by conventional measures. These findings support the need for further investigation of the biologic, genetic, and sociocultural factors that may influence survival in African American patients with breast cancer.
The disproportionately high breast cancer mortality in African American women, coupled with a paradoxically lower breast cancer incidence rate when compared with white American women is receiving increased attention in the medical literature. Recent studies have attempted to disentangle the coexisting influences of primary tumor biology from the socioeconomic, cultural, and behavioral factors that affect outcome. The African American community is characterized by multiple socioeconomic disadvantages1 that impact cancer control. These disadvantages create barriers to breast cancer screening as well as treatment, and are widely assumed to explain a substantial proportion of the mortality disparities.2-5 Several patterns related to breast cancer in African American women are not readily explained by socioeconomic factors. African American women are more likely to be diagnosed with early-onset disease; population-based data from the Surveillance, Epidemiology and End Results (SEER) Program confirm poorly understood differences in breast cancer age-incidence curves. For women living in the United States (ie, American women) younger than 45 years, breast cancer incidence is higher among African Americans compared with white Americans. A cross over in incidence occurs during the fifth decade of life, resulting in the overall decreased lifetime risk.6 Most of the lower lifetime risk is a consequence of diminished incidence rates for estrogen receptor-positive breast cancer.7 African American women have a higher risk of being diagnosed with hormone receptor-negative, aneuploid, and node-positive cancer.7-15 Uncertainty persists regarding the possible existence of hereditary and/or environmental factors that might predispose African American women to these biologically more aggressive phenotypes. Single-institution studies of breast cancer survival generally have limited statistical power in addressing socioeconomic status versus ethnicity as prognostic factors because of the small sample sizes of affluent minority-ethnicity patients with breast cancer that are entered into final multivariate survival analyses. In contrast, population-based registries and multicenter cohorts rarely maintain detailed socioeconomic status information. Research synthesis (meta-analysis) is a statistical tool that can potentially compensate for these inadequacies by pooling the results of appropriately-designed studies, yielding a more robust evaluation.16,17 Meta-analysis is therefore a valid approach for assessing whether African American ethnic background is an independent predictor of adverse outcome. A pooled analysis of studies published between 1980 and 200118 revealed a 22% excess risk of death (all-cause) for African American patients with breast cancer after accounting for socioeconomic background. Many recent studies have investigated the effect of ethnicity on breast cancer survival. We updated the meta-analysis to test the stability of our prior results.
We performed a National Library of Medicine MEDLINE literature search to identify articles published from January 1980 to June 2005 that analyzed breast cancer survival in African American and white American patients with breast cancer. The following terms were entered: "breast cancer" and "African American"; "breast cancer" and "race"; "breast cancer" and "ethnicity"; "breast cancer" and "black." This search was augmented by a review of manuscript references and abstracts from conference proceedings. Appropriate studies for inclusion in the meta-analysis utilized a Cox proportional hazards regression model19 for calculation of survival after adjusting for some measure of socioeconomic status. Studies based on outcomes of patients treated in an "equal-access" system (defined as a health care system in which treated patients share the same payor system; eg, military or health maintenance organization-managed-care systems) were also included, and results from these systems were analyzed separately as well. All studies adjusted for stage and age at diagnosis. Several maneuvers were used to avoid overlapping patient populations for the studies included in the pooled analysis. Geographic locations, sites of treatment, and time frame for breast cancer diagnosis were all recorded. Studies were excluded when these features suggested population overlap with other reports,14,20 in which case the study with longer follow-up or a larger data set was utilized.21,22 Data from the Department of Defense tumor registry were reported in two studies.23,24 Survival results from nonoverlapping years of patient diagnosis were entered into the analysis, with confirmation of the patient population size by the investigator of the more recent study (I. Jatoi, personal communication, September 7, 2004). All included studies analyzed ethnic background based on patients' self-reported information, as abstracted from tumor registry or medical record data. Throughout this article, the term "ethnicity" is used as opposed to "race." This term was selected because of its connotations regarding shared sociocultural features, in addition to ancestral nationality. Two studies conducted separate survival analyses with age stratification. Simon and Severson22 evaluated outcome separately for patients younger than 50 years versus those 50 years and older; Albain et al25 presented outcome stratified by menopausal status. The age-stratified subsets from these studies were entered separately in the meta-analysis.
A total of 20 studies were appropriate for the meta-analysis, and the summary statistic was reported as the mortality hazard (relative risk of death) for African American compared with white American patients with breast cancer. The random-effects model of DerSimonian and Laird26 was applied to calculate the pooled estimate, as heterogeneity between studies was expected, a priori. To test this assumption explicitly, a Cochran
Table 1 summarizes the 20 included studies,2,21-25,28-41 representing a total of 14,013 African American and 76,111 white American women diagnosed with breast cancer from 1961 to 2003. Geographically diverse communities throughout the United States were represented, and most were analyzed in retrospective reviews. A single case-case comparative study was included—the National Cancer Institute's Black White Breast Cancer Survival Study.33 Phase III clinical trials data were reported by Albain et al25; this was the only study included in the analysis that has not yet been published in manuscript form. Selected studies used either the American Joint Commission on Cancer Staging TNM system or the Local-Regional-Distant categories to adjust for extent of disease at presentation. Studies varied in method of age classification as a continuous or a categorical variable, as detailed in Table 1.
As Table 1 presents, most studies relied on area-wide measures for assignment of socioeconomic status, based on average income and educational profile for the census block or tract associated with the patient's address and/or zip code. Four studies23,24,35,36 accounted for socioeconomic status by reporting on breast cancer survival among patients treated in equal-access health care systems. One study33 assigned socioeconomic status according to self-reported data from individual patients; two other studies2,21 relied on hospital records with regard to income and source of pay for treatment. Regardless of method for assigning socioeconomic status, studies comparing resources for the African American and white American patients reported significant disparities,2,21,22,28,30,31,33,34,36,38,41 with an excess of poverty-related features among the African American patients. All studies provided a Cox proportional hazards survival analysis that adjusted for age and stage of disease at diagnosis. In addition, some adjusted for selected primary tumor features (such as hormone receptor status and/or grade)2,22-25,28-30,32-34; comorbidity2,33,35,38; and sociodemographic features such as marital status.22,23,36,39,40 One study29 also accounted for nutritional status, and 11 studies2,21-25,32-34,38,40 considered treatment issues.
Despite methodologic heterogeneity, all studies revealed survival disadvantages for African American patients in crude univariate analyses. Adjusting for socioeconomic status resulted in a loss of strength for the association between outcome and ethnic background within individual studies; in several, the correlation was no longer statistically significant.2,21,28-31,33-37,40 The pooled estimate for the hazard of mortality (all-cause) after adjustment for socioeconomic status was 1.28 (95% CI, 1.18 to 1.38), with African American ethnicity re-emerging as an independent predictor of worse overall survival (Fig 1). Results were similar for the combined analysis of the eight studies reporting breast cancer-specific mortality (Fig 2), revealing that African American patients had a 19% greater risk of death (hazard ratio, 1.19; 95% CI, 1.09 to 1.30). Tests for homogeneity of the hazard ratios across studies for both all-cause mortality (Q11 = 56.6; P
Subset meta-analyses based on type of socioeconomic status assessment are presented in Table 2. Exclusion of the one study32 that used marital status alone as a surrogate for socioeconomic status revealed an even greater survival disadvantage for African American patients with breast cancer (hazard ratio, 1.29; 95% CI, 1.19 to 1.40). Subset meta-analyses of the equal-access systems and the non-equal-access systems consistently revealed that African American ethnicity was significantly and independently associated with worse survival.
Nearly 5 years ago, we conducted a meta-analysis18 of studies that reported survival in African American and white American patients with breast cancer. This initial pooled analysis of 14 studies, involving more than 50,000 patients with breast cancer (10,000 of whom were African American) revealed a statistically significant 22% excess in mortality for the African American patients (hazard ratio, 1.22; 95% CI, 1.13 to 1.30). As shown in Figure 3, literature reviews through MEDLINE using a variety of search terms demonstrate a rapid expansion in the volume of studies addressing ethnicity and breast cancer outcome. The number of titles retrieved through a search of the years 1990 to 1994 was notably higher compared with the yield for the entire preceding decade (1980 to 1989); for every subsequent 5 years, the number of titles retrieved nearly doubled. This rapid escalation in available data motivated us to update the meta-analysis.
Six studies2,24,25,39-41 were added to the original series of 14, corresponding to a supplemental 37,062 patients with breast cancer whose outcomes contributed to the summary statistics. This follow-up meta-analysis also includes data derived from prospective, randomized clinical trials. Our earlier finding that self-reported African American ethnic background is an independent adverse prognostic feature was unchanged in the updated patient population, with an updated mortality hazard of 1.27. These results can be compared with the age-standardized death rates (unadjusted for socioeconomic factors and other confounders) reported by the SEER Program for African American as compared with white American patients with breast cancer of 35.9/100,000 and 27.2/100,000, respectively (ratio, 1.32).1 Stability of the meta-analysis results strengthens the need for advances in two research areas: (1) methods to measure effects of sociobehavioral issues and poverty on breast cancer risk, and (2) exploration of associations between African American ethnicity and variation in primary breast tumor biology. Current insights regarding these areas are inadequate. Furthermore, while our meta-analysis includes data on patients diagnosed throughout four decades, we cannot assess temporal trends related to improved breast cancer treatments. Socioeconomic status is commonly measured as a function of income; however, other factors contribute to this complex descriptor, such as environmental, dietary, cultural, behavioral, education, and access/treatment issues. These elements exert confounding effects on the cancer burden of different ethnic groups. The strategy of classifying an individual's or a community's socioeconomic status on the basis of income alone is therefore potentially misleading in the study of cancer control. Developing a successful strategy for eliminating cancer outcome disparities requires careful scrutiny of all socioeconomic status components for different population subsets.4,18,42-45 Area-wide measures of socioeconomic status (eg, census block and census tract information) may be less reliable for studies of minority-ethnicity families. These measures involve estimates of the socioeconomic status of residential areas, composed of several hundred households, based on average income and educational history. These average socioeconomic estimates are then assigned to all individuals residing in one of these geographic areas by matching address zip codes with the corresponding census block or census tract. Since several neighborhoods will be grouped together within these census regions, socioeconomic heterogeneity within small communities can be underestimated. Clusters of affluent African American families choosing to reside in predominately African American neighborhoods will be assigned the socioeconomic status of the larger area. The larger area frequently has a relatively low average income-education level, reflecting the prevalence of socioeconomic disadvantages of the general African American community. While some studies have validated these area-wide measures in capturing socioeconomic heterogeneity,46 others28 have suggested that the accuracy of estimates for individual households is inversely related to the size of the census area being averaged. Alternative measures of socioeconomic status have been proposed and require further study as we analyze ethnicity-related cancer disparities. Some candidate models are based on assessment of income inequality; social network; and social deprivation.47-50 Yabroff et al51 reported on the utility of a National Health Interview Survey-based method of measuring community socioeconomic status. Most studies of ethnicity and cancer outcome rely on patient self-identification of background. This self-reporting is artificial to some extent, because four centuries of intermarriage between the Europeans, Africans, Scandinavians, and Asians who populate the United States' "melting pot" have resulted in substantial genetic admixture for most contemporary Americans. The Human Genome Project52,53 has ushered in a new era of research that may account for ancestry by gene sequencing, and several investigators have embarked on research of genetic admixture and risk of disease.54-57 These studies have demonstrated the superiority of ancestry-informative genetic markers over skin pigmentation58,59 in the assessment of ethnic heritage. The term "ethnicity" is itself imprecise in definition; we chose to use the term ethnicity instead of "race" because the former connotes some cultural commonality in addition to shared ancestry. The extent to which the African American community should be characterized as diverse versus socioculturally homogeneous can be debated. Regardless, as this meta-analysis demonstrates, self-reported African American ethnic background is consistently shown to be associated with worse breast cancer survival. Recently, Tammemagi et al have shown that comorbidities account for a significant proportion of the mortality risk seen in African American patients with breast cancer.60 Four studies from this meta-analysis adjusted for comorbidity.2,33,35,38 Interestingly, the Tammemagi et al study also demonstrated statistically significant survival disadvantages for African American patients with breast cancer as reflected by all-cause (1.34; 95% CI, 1.11 to 1.62), breast cancer-specific (1.47; 95% CI, 1.08 to 2.00), or competing-causes-specific (1.27; 95% CI, 1.00 to 1.63) hazard ratios. It remains valid to question whether African American ethnicity as an adverse breast cancer prognostic feature is a surrogate marker for socioeconomic disadvantage and inadequate health care. Poverty rates and likelihood of being uninsured are two- to three-times higher among African Americans compared with white Americans, causing delayed diagnostic procedures and treatment. Provider-level inequalities in delivery of care have also been documented.61,62 All of these issues ultimately result in advanced-cancer stage distributions and higher mortality rates.1,63 Some investigators have in fact documented comparable responses to therapy in African American and white American patients with breast cancer after controlling for disease stage. For example McCaskill-Stevens et al found similar effectiveness and adverse effect profiles for tamoxifen64; Dignam et al found similar outcomes in an overview of National Surgical Adjuvant Breast Project clinical trials65; and Roach et al reported similar outcomes in patients treated on Cancer and Leukemia Group B protocols.66 Speculation persists regarding ethnicity-related variation in primary tumor biology as an explanation for outcome disparities. Subset analysis from phase III clinical trials of breast cancer should eliminate many confounding effects because random assignment and protocol design should standardize treatment, independent of ethnic background. Unger et al67 presented provocative results from a pooled analysis of clinical trials conducted by the Southwest Oncology Group, and found that survival disparities for African Americans as well as other minority-ethnicity patient populations were eradicated in the context of protocol-standardized management for the majority of malignancies. Interestingly however, persistent survival disadvantages were seen for African American participants in clinical trials for hormonally driven cancers such as breast, prostate, and ovarian. These results suggest that African American ethnicity may be associated with genetic or metabolic characteristics that influence breast cancer outcome. Albain et al25 explored this further in a pooled analysis of Southwest Oncology Group adjuvant therapy protocols for breast cancer. They found statistically significant differences in outcome for both pre- and postmenopausal African American participants, despite the expectation that the clinical trial mechanism would control for stage of disease, work-up, and delivery of care. The investigators nonetheless included adjustments for socioeconomic status based on census tract estimates for participants, with no substantive changes in their results. These results are included in the present meta-analysis. Data from the Women's Health Initiative (WHI)13 provided additional clinical trial-based evidence of a survival disadvantage for African American patients with breast cancer. The WHI was designed to analyze the effect of postmenopausal hormone replacement therapy versus placebo on breast cancer incidence and cardiovascular disease. With a median follow-up exceeding 6 years, WHI investigators reported risk factors associated with breast cancer incidence and mortality after stratifying by patient ethnicity. Established risk factors were found to explain differences in breast cancer burden between white Americans and all other ethnic groups, except for African Americans. For African American participants, there remained a significant increase in incidence of estrogen receptor-negative cancer, and an excess breast cancer mortality risk. The concept that disparities in breast and prostate cancer may have a unique etiology with regard to African Americans is particularly intriguing. There are several parallels observed for the effect of these two hormonally driven malignancies on African American women and men, respectively, such as younger age distribution, more advanced-stage distribution at time of diagnosis, and increased prevalence of adverse primary tumor prognostic features. The possibility of hereditary predisposition for aggressive disease related to African ancestry is currently being investigated.68-72 Hershman et al73 reported on the increased prevalence of neutropenia among African Americans and the effect of this feature on adjuvant therapy for cancer patients. Baseline WBC counts are known to be relatively lower for African Americans compared with white Americans, and this neutropenia can increase the risk for requiring chemotherapy dose reductions and/or treatment delays. Hershman et al found that this issue did correlate with decreased chemotherapy dose intensity for African American patients with breast cancer treated at Columbia Presbyterian Medical Center.73 The suspected association between vitamin D levels and breast cancer risk also warrants further study,74-76 as vitamin D levels seem to vary between African Americans and white Americans.77 This meta-analysis of socioeconomic status-adjusted breast cancer survival demonstrates that self-reported African American ethnicity is an independent predictor for worse outcome. While attempts to correct socioeconomic disparities between African Americans and white Americans must be prioritized on the public health care agenda, our study confirms the importance of research regarding primary variation in breast tumor biology and studies of cancer-related factors associated with the environment of poverty.
The authors indicated no potential conflicts of interest.
Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.
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ABSTRACT
INTRODUCTION
2 test statistic (Q statistic) was also calculated and reported.
.0001) and breast cancer-specific mortality (Q8 = 11.174; P 
