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Disparities and Survival Among Breast Cancer Patients
Affiliations of authors: Meyers Primary Care Institute, University of Massachusetts Medical School, Fallon Foundation, and Fallon Community Health Plan, Worcester, MA (TSF, CD, HF); Center for Health Studies, Group Health Cooperative, Seattle, WA (DSMB, GH); Center for Research and Evaluation, Kaiser Permanente Southern California, Pasadena, CA (SE, JY); Clinical Research Unit, Kaiser Permanente Colorado, Denver, CO (EJK, JE); Center for Health Services Research, Henry Ford Health System, Detroit, MI (LL, RK); Center for Health Research, Northwest/Hawaii, Kaiser Permanente Northwest, Portland, OR (DJB, MCH); Division of Research, Kaiser Permanente Northern California, Oakland, CA (LH, LL)
Correspondence to: Terry S. Field, DSc, Meyers Primary Care Institute, 630 Plantation St., Worcester, MA 01605 (e-mail: tfield{at}meyersprimary.org).
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ABSTRACT |
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Background: Although rates of survival for women with breast cancer have improved, the survival disparity between African American and white women in the United States has increased. Purpose: To determine whether this survival disparity persists in an insured population with access to medical care. Methods: In this retrospective cohort study, we extracted data from the tumor registries of six nonprofit, integrated health care delivery systems affiliated with the Cancer Research Network and assessed the survival of African American (n = 2276) and white (n = 18 879) female enrollees who were diagnosed with invasive breast cancer from January 1, 1993, through December 31, 1998. Cox proportional hazards regression was used to estimate the death rate among African American women relative to that of white women after adjustment for potential explanatory factors including stage at diagnosis, tumor characteristics, and treatment. Results: Five-year survival was lower for African American women (73.8%) than for white women (81.6%). African American women were less likely to have tumor characteristics with good prognosis. Controlling for age at diagnosis, stage, grade, tumor size, and estrogen and progesterone receptor status, the adjusted hazard rate ratio for African American women was 1.34 (95% confidence interval = 1.22 to 1.46). Similar risks were found among women ages 20–49 and 50 and older. Controlling for treatment slightly lowered the hazard rate ratio to 1.31 (95% confidence interval = 1.20 to 1.43). Conclusions: Among women with invasive breast cancer, being insured and having access to medical care does not eliminate the survival disparity for African American women.
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INTRODUCTION |
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Although rates of survival for women with breast cancer have improved during the last two decades, the survival disparity between African American and white women has increased (1–3). A number of potential explanatory factors have been investigated including the stage of disease at the time of diagnosis (4–7); access to health insurance and medical care (8,9); variability in the aggressiveness of treatment (10–15); environmental, socioeconomic, and psychosocial factors (16–19), and differences in underlying tumor biology (20–26).
Few studies have been able to assess outcomes in populations with apparent equal access to medical care. Several studies based in the U.S. Department of Defense healthcare system have found a higher risk of death for African American women with breast cancer despite being treated in an equal access system with standardized treatment approaches (27,28). A study of survival among women with breast cancer enrolled in a single managed care organization found differences between African American and white women that were mitigated by control for treatment and eliminated by controlling for indicators of socioeconomic level (29). However, this study was based in only one health care delivery site. Because clinical trials ensure equal treatment, they are another source of equal access to care. However, trials of breast cancer therapy have enrolled few African American women (30–32), and participants have been matched on specific cancer characteristics, limiting confidence that the trial outcomes are representative of the range of breast cancers found among African American women.
To contribute further to the evidence on possible associations between access to health insurance and medical care and survival disparities, we conducted a study based on data from the "virtual tumor registry" of the Cancer Research Network (CRN) (33). The CRN is a consortium of research organizations affiliated with nonprofit integrated health care delivery systems and the National Cancer Institute. The CRN has instituted a virtual tumor registry that consists of data sets located at the individual health care sites with a standard variable set and coding scheme, allowing merges of data for specific studies.
Our objectives in this study were to determine whether disparities in survival between African American and white women with breast cancer would persist in a large, insured, multiracial population without obvious barriers to access to medical care, and to identify any factors associated with racial disparities that could serve as points of possible interventions at the healthcare system level.
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METHODS |
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Setting and Population
The CRN consists of the research programs, enrollee populations, and databases of 11 integrated health care organizations that are members of the HMO Research Network. The health care delivery systems participating in the CRN are Group Health Cooperative, Harvard Pilgrim Health Care, Henry Ford Health System/Health Alliance Plan, HealthPartners Research Foundation, the Meyers Primary Care Institute of the Fallon Healthcare System/University of Massachusetts, and Kaiser Permanente in six regions: Colorado, Georgia, Hawaii, Northwest (Oregon and Washington), Northern California, and Southern California. The 11 health plans have nearly 10 million enrollees. The CRN conducts collaborative research on variations in cancer prevention and treatment policies and practices.
The six CRN sites participating in this study are predominantly staff-model managed care organizations with tumor registries that capture cancer diagnoses for their full population of enrollees (Henry Ford Health System in Detroit, MI; Group Health Cooperative in Seattle, WA; and Kaiser Permanente in four regions: Colorado, Northwest [Oregon and Washington], Northern California and Southern California). Collectively, these six sites provided care to over 7 million enrollees in 1998. Study subjects were health plan members who were diagnosed with incident invasive breast cancer between January 1, 1993, and December 31, 1998, while they were enrolled in one of these managed care organizations. The study was limited to female subjects who were age 20 years or older at the time of the breast cancer diagnosis.
The protocol for this study was reviewed and approved by the institutional review boards of all participating institutions.
Definitions
The tumor registries at these sites contain data elements consistent with the Surveillance, Epidemiology, and End Results (SEER) program's registries. We limited our study to invasive cancers, defined using the behavior and SEER summary stage variables. Cancer type was established by combining the registries' primary site and morphology variables. These variables were coded using International Classification of Diseases for Oncology, 3rd edition (ICD-03). Cancers that did not constitute solid tumors were identified and excluded based on morphology codes; breast cancer was identified from the remaining diagnoses based on site codes. We used morphology codes to categorize breast cancer into comedo, ductal, ductal/lobular, inflammatory, lobular, medullary, mucinous, Paget's, papillary, phyllodes, tubular, or other histology. The tumor registries coded tumor grade as well differentiated, moderately differentiated, poorly differentiated, not differentiated, or unknown. Registries at five sites also coded the stage of cancer at diagnosis using the American Joint Committee on Cancer (AJCC), 5th edition staging scheme, which we categorized as stages I, IIA, IIB, III, IV, and unknown/unstaged. Tumor size was available for most women and was categorized as less than 2.0 cm, 2.0 to less than 5.0 cm, 5.0 cm or larger, diffuse/other, or unknown. The sites' tumor registries had information on the estrogen receptor test results for a portion of their breast cancer patients, categorized as positive, negative, test not done, or unknown. We categorized women with missing receptor status as having unknown receptor status. Results of progesterone receptor tests were less commonly available. All site registries included data on the receipt of surgery, radiation therapy, chemotherapy, and hormone therapy during the initial treatment phase.
We linked all enrollees identified in the cancer registry data to enrollment files to extract a complete enrollment history. At the time of the data extraction, all cancer registry and enrollment data at each site were current as of December 31, 2003. Follow-up began on the diagnosis date and ended on the earliest among the dates of death, disenrollment, or December 31, 2003. We calculated the length of enrollment in the health plan before the date of the breast cancer diagnosis and categorized it as less than 30 days, 30 to less than 180 days, 180 days to less than 1 year, 1 year to less than 4 years, 4 years to less than 10 years, or 10 years or longer.
Demographic characteristics were drawn from the tumor registry data. Only non-Hispanic white and African American women were eligible for the study. To exclude Hispanic women, the race and ethnicity variables were combined and women were identified as Hispanic according to the Hispanic variable, including those with a Spanish surname (34). Age at the time of diagnosis was directly extracted from the registry data.
Endpoints
We evaluated three end points: death from any cause (n = 4942), death from breast cancer (n = 1491), and death from any cancer (n = 1777). Follow-up for all-cause mortality in this population is very thorough because it is directly associated with continued enrollment in the health plan. However, cause of death data in the tumor registries are not as consistently collected and were missing or inconclusive for 50% of the deaths. Cause of death was coded in several ways (ICD-9CM, ICD-10CM, and ICDO); therefore, codes were manually searched to identify deaths from cancer. Women who disenrolled from their health plan during the follow-up period for reasons other than death were censored at the time of disenrollment (n = 3843, 18% of the cohort).
Statistical Analyses
We began analyses by determining the distribution of age, the tumor characteristics, and the previous enrollment history for African American and white women and calculating 5-year survival according to race. We conducted subanalyses for AJCC stage from the sites with available data.
We divided the cohort by age at diagnosis into those ages 20–49 years and those aged 50 years or older to assess the possibility of age-specific racial disparities in survival. Age 50 was chosen as the split point as a proxy for menopausal status (7,35,36). We calculated the frequency distributions for tumor characteristics for African American and white women in each age group.
We fit Cox proportional hazards regression models in the entire cohort and separately in the two age groups to determine the extent to which stage at diagnosis and tumor characteristics explained any disparities in survival. The proportional hazards assumption for race in the Cox regression models was visually evaluated by review of the Schoenfeld residuals (37) and graphical assessment of the Cox proportional hazards functions (38). The assumption was not met during the initial 84 days after diagnosis, but from that point in time the hazards remained proportional. We fit all Cox models beginning at day 85 after diagnosis and described outcomes during the initial 84 days separately. We tested interaction terms between each group of tumor characteristic variables and race and between CRN site, year of diagnosis, and the treatment variables and race, and we found none to be significant.
We investigated the possibility that treatment explained any differences in survival through several approaches. We constructed Cox regression models that added control for variables indicating receipt of each of the four major types of therapy in the entire cohort and the two age groups and ran a Cox regression model in the subgroup of women age 50 years and older who were diagnosed at local stage with small tumors and who received surgery, radiation therapy, and either chemotherapy or hormone therapy.
We also assessed the frequency distribution of tumor characteristics by race for women diagnosed at local stage and ran Cox regression models predicting mortality within each age group.
All analyses were conducted using SAS version 9.1.
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RESULTS |
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Characteristics of the Study Population
From 1993 through 1998, 2276 African American women and 18 879 white women were diagnosed with invasive breast cancer at the six CRN sites. Unadjusted 5-year survival was lower for African American women (73.8%) than for white women (81.6%) (Table 1). During the 5 years following the breast cancer diagnosis, 13% of African American women and 12% of white women disenrolled from their health plan for reasons other than death. Fewer African American women had tumor characteristics associated with good prognosis: They had lower rates of being diagnosed at local stage or in AJCC stages I and IIA, having well-differentiated tumors, positive estrogen receptor status, and small tumor size. Information on progesterone receptor status was unavailable for the majority of women. Length of enrollment prior to diagnosis was very similar for the two groups.
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Age is closely associated with breast cancer survival; most studies have found that younger, premenopausal women with breast cancer are more likely to have tumor characteristics with adverse prognoses (39–43). African American women are generally diagnosed with breast cancer at a younger age than white women (21,44,45). Among the African American women in our cohort, 35.1% were diagnosed while younger than 50 year of age, compared to 20.9% of white women (Table 1). Five-year survival was lower for African American women than for white women in both age groups. Among African American and white women, younger women had less favorable tumor characteristics than older women. African American women had less favorable tumor characteristics than white women regardless of age. The distributions of stage at diagnosis, tumor grade, and estrogen receptor status for older African American women were similar to that of younger white women.
During the first 84 days following diagnosis the hazard curves for death for African American and white women were entwined and crossed, and this time period was excluded from the multivariate analyses. During that period, 1.0% of the African American women (N = 22) and 0.8% of white women (N = 157) died, and 20 African American women and 103 white women disenrolled from their health plans.
Multivariable Analyses of Survival
Within the remaining cohort of 2234 African American and 18 619 white women, we conducted Cox regression models for the complete cohort and separately by age group (Table 2). African American women had increased risks of death compared to white women regardless of age. Inclusion of potential confounding variables related to tumor characteristics lowered the hazard rate ratio for African American women under age 50 years but had only a small effect among those age 50 years and older. We conducted analyses in the subset of women enrolled in the five sites whose tumor registries included AJCC stage, replacing SEER summary stage variables with AJCC stage. Inclusion of AJCC stage lowered the additional risk of death associated with being African American in the older age group: for the entire cohort the hazard rate ratio was 1.24 (95% confidence interval [CI] = 1.12 to 1.39), for women under age 50 years the hazard rate ratio was 1.37 (95% CI = 1.10 to 1.71), and for those age 50 years and older the hazard rate ratio was 1.20 (95% CI = 1.05 to 1.36). Despite the unfavorable tumor characteristics of African American women, controlling for these characteristics did not fully explain their higher risk of death.
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Previous studies have documented that cancer-related deaths are often misclassified (46–48). Therefore, our primary analyses focused on death from any cause. However, to assess the possibility that our results were caused by increased death rates from non–breast cancer conditions among African American women, we conducted Cox regression models controlling for tumor characteristics with death from breast cancer as the outcome and with death from any cancer as the outcome. The adjusted risk of death from breast cancer for African American women was 1.48 (95% CI = 1.26 to 1.73); the adjusted risk of death caused by any cancer for African American women was 1.49 (95% CI = 1.28 to 1.74).
We used a variety of approaches to assess the possibility that differences in treatment might explain any racial disparities in survival. Investigators have suggested that assessing survival by stage at diagnosis provides a way for testing whether aggressiveness of treatment is a partial explanation for survival disparities (49); for women diagnosed at local stage, there are available treatments with high success rates so that inadequate treatment would be associated with large differences in outcome; for women diagnosed at distant stage treatment is not highly successful so survival disparities would be smaller. To assess this possibility, we conducted Cox regression models predicting mortality separately by stage at diagnosis as well as in subgroups of women with positive tumor characteristics, including estrogen receptor–positive status and those with well-differentiated tumors. Among women diagnosed at local stage the hazard rate ratio for African American women was 1.42 (95% CI = 1.23 to 1.64), at regional stage 1.22 (95% CI = 1.07 to 1.39), and at distant stage 1.41 (95% CI = 1.09 to 1.84). Among women with estrogen receptor–positive tumors, the hazard rate ratio for African American women was 1.30 (95% CI = 1.12 to 1.49). Among women with well-differentiated tumors the survival disparity was eliminated—the hazard rate ratio for African American women was 1.04 (95% CI = 0.73 to 1.49), but this group only included 237 African American women, and the confidence interval was wide.
Although the treatment data available from the tumor registries were of limited specificity, we were able to identify whether any type of surgery, radiation therapy, chemotherapy, or hormone therapy was provided to these women (Table 3). African American women in both age groups diagnosed at local or regional stage were significantly less likely than white women (P<.0001) to receive surgery, radiation therapy, and hormone therapy. Inclusion of treatment variables in the Cox regression models lowered the hazard rate ratios: Among the full cohort, the adjusted risk of dying for African American women was 1.31 (95% CI = 1.20 to 1.43); among women under age 50 years, the risk was 1.33 (95% CI = 1.12 to 1.58), and among women age 50 years and older, the risk was 1.28 (95% CI = 1.16 to 1.43).
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To determine whether African American and white women with similar tumor characteristics who received similar treatment had parallel outcomes, we assessed survival in the subgroup of women who were age 50 years and older, diagnosed at local stage, with tumors smaller than 2.0 cm, who received surgery, radiation therapy, and either chemotherapy or hormone therapy. Within this group the hazard rate ratio associated with being African American was 1.35 (95% CI = 0.81 to 2.22). This was a much smaller group that included only 136 African American women, and the confidence interval was wide.
Characteristics of Women Diagnosed at Local Stage
Prior studies have found that African American women are diagnosed with breast cancer at later stages than white women. To assess the extent to which aggressive efforts to shift the time of diagnosis to a point when the cancers of African American women were localized would lessen any survival disparities, we examined tumor characteristics of women diagnosed at local stage (Table 4). Even with cancers diagnosed at local stage, African American women were significantly more likely to have tumor characteristics with poor prognosis than white women in each age group (P<.0001). In parallel with our findings across all stages, older African American women with breast cancer diagnosed at local stage had tumor characteristics similar to those of younger white women.
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DISCUSSION |
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TopNotesAbstractIntroductionMETHODSRESULTSDISCUSSIONReferences |
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African American women with invasive breast cancer in this study had worse survival than white women, despite having health insurance and apparent equal access to medical care. This was true for women younger and older than age 50 years, diagnosed at local, regional, or distant stage. African American women were less likely to have tumor characteristics with good prognosis; however, controlling for these characteristics did not eliminate the survival disparity. The only subgroup in which African American women did not have a survival disadvantage was women with well-differentiated tumors. This group included very few African American women, and the hazard rate ratio had a wide confidence interval. Several additional prognostic tumor characteristics have recently been found to differ in frequency among racial groups including high nuclear grade, necrosis, and alterations in p53 and c-me (26). These factors were not captured in the tumor registries, and the extent to which they may explain survival disparities is not yet fully understood. The possibility that differences in tumor characteristics explain survival differences is still an open question.
Differences in overall health status and rates of comorbid conditions might explain the differences found in all-cause mortality. However, analyses that focused specifically on mortality from breast or other cancers found even larger hazard ratios for African American women.
We used several approaches to assess the extent to which differences in treatment aggressiveness accounted for the racial survival disparity. Although the rates of provision of the major treatment modalities did differ by race, control for receipt of these treatments did not eliminate the disparity. African American women remained at higher risk of death even in the subgroup of women diagnosed at local stage with small tumors who received surgery, radiation, and either chemotherapy or hormone therapy. This does not eliminate the possibility that treatment differences are an explanation. The treatment data available in the tumor registries were limited and did not include information on aspects of quality, delays in the timing of care, or whether treatment regimens were actually completed, or details on the specific types of surgery, radiation, or chemotherapy agents. Racial differences in these aspects of treatment may exist despite insured status and may result from either patient or health care system issues or from differences in tumor biology.
All of the women in this study had health insurance and were enrolled in managed care plans. Approximately 75% of the women in both racial groups had been enrolled in the same plan for more than 4 years, and similar percentages of both groups of women remained enrolled after the breast cancer diagnosis. This implies similar access to care. However, a number of additional factors may affect access. Each organization has a variety of plan alternatives with varying copays and other financial hurdles that could affect access for enrollees with limited incomes. Medical offices and facilities providing cancer-specific treatments may not be located near the areas where African American enrollees reside; problems with travel have been found to affect receipt of some breast cancer treatments (50,51). The not-for-profit managed care plans involved in this study serve predominantly working and middle-class populations. This indicates that their African American and white enrollees are not likely to be either impoverished or wealthy. However, there may be substantial differences in the level of financial resources between the two groups. The out-of-pocket expenses involved in cancer care (52–54), and the frequent need for time taken from work for both the patients and their care givers (55), could also affect the timing and thoroughness of the women's participation in treatment regimens. A previous study set in one managed care plan found that control for median household income based on census data eliminated an apparent survival disparity between African American and white women (29). These data were not available for the cohort examined in this study. The ways in which financial resources affect access to care and treatment in an insured population are not well understood and require additional research.
Health insurance and financial resources are not the only factors that may affect access to care. Attempts to understand health disparities among racial and ethnic groups have also highlighted the role of patient–physician communication during medical visits. Several studies have found that the communication patterns of physicians differ between white and African American patients (56) and that African American patients are more likely to perceive racism, report mistrust of the medical care system, and be less satisfied with their care (57). In focus groups with cardiac patients, investigators found that African American patients wanted to build a trusting relationship with physicians before agreeing to invasive procedures and complained that this trust was lacking (58). Research is needed on communication between physicians and African American cancer patients and its effect on treatment and outcomes.
This study was based in six large, integrated health care delivery systems. One of its intentions was to identify potential interventions for reducing any racial disparities detected. No clear directions emerged. There is a possibility that increasing mammography screening among African American women would shift more diagnoses to earlier stages. In parallel with white women, survival rates among African American women were directly associated with stage at diagnosis (e.g., 87.8% of those diagnosed in AJCC stage I survived for at least 5 years, compared to 83.6% diagnosed in stage IIA, 71.8% in stage IIB, 48.5% in stage III, and 9.4% in stage IV). However, survival disparities in comparison to white women persisted. A recent cost/benefit analysis of interventions for African American women with breast cancer concluded that improvements in treatment are a more cost-effective approach than increased screening (59). More information is required about the details of treatment provided to African American women and race-specific rates of mammographic screening in these managed care plans before a similar analysis can be conducted for this setting of care.
Having health insurance and apparently equal access to medical care did not eliminate disparities in breast cancer survival for this group of African American women. This may have resulted from differences in treatment, more aggressive pathology, less effective follow-up, or the interaction between African American women and the health care system. If we are to reduce the health disparities for African American cancer patients in the U.S. health care system, we must focus more research on all aspects of access to medical care with attention to the details of how socioeconomic factors and patients' interactions with the health care system affect their care.
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NOTES |
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This study was carried out under the auspices of the Cancer Research Network, supported by a grant from the National Cancer Institute, CA79689. Dr. Buist's time was supported by CRTG-02–024–01-CCE, a grant from the American Cancer Society.
The overall goal of the CRN is to increase the effectiveness of preventive, curative and supportive interventions that span the natural history of major cancers among diverse populations and health systems, through a program of collaborative research. This overarching aim of the CRN, coupled with the expertise of the investigative team, and geographically-dispersed population base, fosters efficient and effective research on variations in cancer prevention and treatment policies and practices.
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