Affiliations of authors: R. M. Hoffman, Medicine Service, Department of Veterans Affairs Medical Center, Albuquerque, NM, and New Mexico Tumor Registry, University of New Mexico Health Sciences Center, Albuquerque; W. C. Hunt, New Mexico Tumor Registry, University of New Mexico Health Sciences Center; F. D. Gilliland, A. S. Hamilton, Department of Preventive Medicine, University of Southern California, Los Angeles; J. W. Eley, Georgia Center for Cancer Statistics, Rollins School of Public Health, Emory University, Atlanta, GA; L. C. Harlan, A. L. Potosky, Division of Cancer Control and Prevention, National Cancer Institute, Bethesda, MD; R. A. Stephenson, Utah Cancer Registry and Division of Urology, University of Utah School of Medicine, Salt Lake City; J. L. Stanford, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA, and Department of Epidemiology, University of Washington; P. C. Albertson, Division of Urology, University of Connecticut Health Sciences Center, Farmington.
Correspondence to: Richard M. Hoffman, M.D., M.P.H., General Internal Medicine 111GIM, Department of Veterans Affairs Medical Center, 1501 San Pedro Dr., S.E., Albuquerque, NM 87108 (e-mail: rhoffman{at}unm.edu).
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ABSTRACT |
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INTRODUCTION |
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A number of explanations have been proposed to account for the disparity in the stage at diagnosis. For example, demographic characteristics, socioeconomic status, and comorbidity may limit cancer screening in the African-American population and contribute to a delayed diagnosis. Another explanation is that racial differences in tumor biology, possibly attributable to differences in dietary, hormonal, or molecular factors, may lead to more aggressive tumors (4,5). However, attempting to explain the disparity in the stage at diagnosis between African-Americans and other ethnic groups has been difficult because, to our knowledge, no previous studies have assembled large cohorts and collected comprehensive individual-level data.
The Prostate Cancer Outcomes Study (PCOS) was initiated in 1994 to collect individual-level data from a population-based cohort of men with newly diagnosed prostate cancer to assess the effects of cancer treatments, including radical prostatectomy and radiation therapy, on health-related quality-of-life outcomes. The objective of the current analysis was to use these data to determine the association, if any, between race/ethnicity and prostate cancer clinical stage after adjusting for demographic, socioeconomic, clinical, and pathologic factors.
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SUBJECTS AND METHODS |
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The PCOS is based on an existing tumor registry system, the National Cancer Institute's Surveillance, Epidemiology, and End Results (SEER)1 Program, which provides information on cancer incidence and survival for the United States. Details of the PCOS have been published elsewhere (6). Briefly, the PCOS used a rapid case ascertainment system to identify men diagnosed with microscopically confirmed invasive carcinoma of the prostate between October 1, 1994, and October 31, 1995, in six SEER tumor registries. Patients were diagnosed in the states of Connecticut, Utah, and New Mexico and in the metropolitan areas of Atlanta, GA, Los Angeles County, CA, and King County, WA (which includes Seattle). All men up to age 90 years at the time of diagnosis were eligible, except in King County, where men less than age 60 years were not included in the study because they were eligible for another ongoing study. The study was approved by the institutional review board of each participating institution.
Eligible patients were sampled within strata of age, race/ethnicity, and tumor registry to ensure adequate demographic representation. Patients from ethnicities other than non-Hispanic white, African-American, or Hispanicthat is, usually either Asian or Native Americanwere excluded because the numbers in these groups were small and identifying race/ethnicity at the time of sampling was difficult.
The PCOS randomly sampled a total of 5672 subjects from the 11 137 eligible prostate cancer cases. This sample size was selected to provide sufficient power to detect differences in quality-of-life outcomes between the radical prostatectomy and radiation therapy groups and to ensure sufficient numbers of racial/ethnic minorities for assessing outcomes in different population subgroups. Among the sampled patients in the PCOS, 3173 (55.9%) men completed a health-related quality-of-life survey questionnaire 6 months after initial diagnosis. We used data collected from these responders to evaluate the association between race/ethnicity and cancer stage at diagnosis. Responders were similar to the nonresponders with respect to age, previous prostate-specific antigen (PSA) testing, and proportion of advanced cancers. Nonresponders were more often nonwhite and without private health insurance (6).
Data Collection
Investigators contacted patients by mail and/or telephone and requested them to sign a release form allowing review of all medical records from any physicians and facilities providing care for prostate cancer. With the use of a standard protocol, trained abstractors reviewed medical records from hospitals, freestanding radiologic or surgical centers, clinics, and private physician offices. Abstractors collected information on demographic factors, diagnostic procedures, PSA levels, clinical staging procedures and results, biopsy results, tumor characteristics, and treatment details. A random sample of 5% of records was reabstracted to assess and correct systematic coding errors.
Additional data were collected from the self-administered health-related quality-of-life questionnaire survey that included questions about general and disease-specific measures of health-related quality of life, prediagnostic symptoms, and specific treatments received for prostate cancer. Demographic and socioeconomic questions were used to determine race/ethnicity, employment status, educational level, household income, insurance status, and marital status. A question assessing comorbidity asked about 12 medical conditions that are likely to affect prostate cancer treatment decisions and long-term quality of life. If the patient reported being told by a doctor that he had a stroke, inflammatory bowel disease, liver disease, or ulcers, he received 1 point on his comorbidity score for each condition. If the patient responded that any of eight conditionsarthritis, diabetes, depression, hypertension, chest pain, heart attack, heart failure, or chronic lung diseaselimited his activity or required prescription medications, he received 1 additional point. In the analyses, comorbidity scores were divided into the categories of 0, 1, 2, and greater than or equal to 3 points. Patients were also asked to recall baseline urinary function, including the presence of obstructive and irritative urinary symptoms.
Clinical cancer stage determinations were based on an algorithm that used clinical information, diagnostic tests, and biopsy results abstracted from medical records. The algorithm was necessary because the community-based medical records were not detailed enough to classify cases with TNM (tumornodemetastasis) staging (7). The algorithm defined T1 tumors as confined to the prostate with a normal digitalrectal examination and no positive scans (magnetic resonance imaging, computed tomography, and bone scan) or evidence of metastases. T2 tumors were defined as confined to the prostate, with abnormal or suspicious digitalrectal examinations, but no positive scans or evidence of metastases. T3 tumors were defined as extending beyond the prostate but with no positive scans or evidence of metastases. T4 tumors were defined as those with at least one positive scan, distant metastases, or positive lymph nodes.
Statistical Analysis
All regression models were performed with the Survey Data Analysis statistical package (8). The HorvitzThompson weight, which is the inverse of the sampling proportion for each sampling stratum (defined by age, race/ethnicity, and study area), was used to obtain unbiased estimates of the regression parameters for all eligible prostate cancer patients in the PCOS areas. All estimates presented in this report are weighted to this population. The sampling and weighting strategies are described in more detail elsewhere (6). All P values were two-sided.
Contingency tables and logistic regression models were used to analyze the association of race/ethnicity with clinically advanced-stage cancer (i.e., stage T4). The dependent variable for all logistic regression analyses was clinically advanced-stage tumor (stage T4). Independent variables included, in addition to race/ethnicity, demographic factors (age at diagnosis, geographic region, and marital status), socioeconomic factors (educational level, household income, insurance status, and employment status), clinical factors (previous PSA testing, urinary symptoms, and medical comorbidity), and histologic grade (Gleason score). Gleason scores were used as a marker for tumor aggressiveness because they can be used to predict mortality and tumor progression independently of tumor stage (9,10). Although data were collected on PSA testing, PSA levels were not included in the model predicting advanced-stage cancer because elevated levels are often the consequences of large tumor volume and advanced stage (11,12). We also examined interactions between race/ethnicity and other independent variables in the regression model.
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RESULTS |
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We next assessed the interactions between ethnicity and all of the variables by regression analyses. Table 2 shows the univariate and multivariate (adjusted simultaneously for all study variables) odds ratios (ORs) for associations between demographic and socioeconomic factors, clinical factors, and grade with clinically advanced-stage cancer. The highest OR in the multivariate analysis (OR = 10.3; 95% confidence interval [CI] = 4.92 to 21.6) was for Gleason scores of 8 to 10 compared with Gleason scores of 2 to 4 (Table 2
). Insurance status, employment status, previous PSA testing, and urinary frequency symptoms were also statistically significant variables (Table 2
). There were no statistically significant interactions between these variables and race/ethnicity.
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DISCUSSION |
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Our findings are consistent with previous reports (3,1323) showing that African-Americans have a twofold increased risk of presenting with advanced-stage prostate cancer compared with non-Hispanic whites. We found a similar risk increase, although the proportion of advanced disease in African-Americans in our study was just 12% compared with previously reported frequencies of 20%35% (3,1727). However, the disparity in the frequency may be a reflection that these other studies collected data only through the early 1990s, and the incidence of distant disease has sharply declined during the past decade (3,24).
Racial and ethnic disparity in the stage at diagnosis is clinically important because stage strongly predicts survival. Indeed, adjusting for other causes of death, the 5-year relative survival for men with advanced-stage prostate cancer is only 34% compared with nearly 99% for men diagnosed with either localized or regional-stage disease (3). The prostate cancer mortality rate is substantially higher for African-Americans than for non-Hispanic whites (3,24,25), but the racial difference generally disappears after adjusting for stage (1517,26,27). Although some SEER reports have shown poorer survival for African-Americans across all stages of disease (3,24), data in those reports were not adjusted for socioeconomic or demographic factors. In addition, the SEER categories of localized, regional, and distant are less precise than other currently used staging systems (28).
Socioeconomic factors have been hypothesized to explain the racial and ethnic differences in the stage of prostate cancer at diagnosis because limited education, low income, and lack of insurance are barriers to receiving health care (2931). African-Americans, who are disproportionately represented in the lower socioeconomic levels, are believed to have less access to health care and preventive services than non-Hispanic whites, which delays diagnosis and leads to presenting with clinically advanced disease (32). Our study, which used a large population-based cohort and collected individual-level data, found that insurance status and employment status were associated with the risk for presenting with advanced disease. However, our observations are consistent with those of other investigators because we found that socioeconomic factors alone cannot adequately explain the higher percentage of advanced disease in African-Americans (18,19,23,25,32). Several studies (16,17,33) in Veterans Affairs (VA) hospitals, where access to health care was presumed equal for all eligible veterans, consistently found considerably higher proportions of advanced cancer in African-Americans. Tumor registry data from Washington, DC, and Connecticut also demonstrated appreciably higher rates of advanced disease in African-Americans that persisted after adjustment for socioeconomic status by use of census tract data (19,21). However, the assumption that VA eligibility creates equal access to health care is debatable; moreover, census tract data provide only an estimate of socioeconomic factors related to health-care usage. Optenberg et al. (15) provided stronger evidence discounting the effect of socioeconomic factors by retrospectively studying a U. S. Department of Defense cohort that had equal access to free medical care. Although screening was systematically offered to this population, African-Americans were still more than twice as likely as whites to present with advanced disease.
The consistent failure to adequately explain differences in stage by looking at household income, employment status, educational level, and insurance status suggests that this widely used constellation of socioeconomic factors may not sufficiently represent access to and use of health care. We did not ask subjects about several additional factors, such as whether they had a source for regular health care and routinely received preventive services, nor did we obtain data on access factors, such as literacy (34) or transportation. In addition, we did not survey subjects about their knowledge, attitudes, and beliefs about cancer, factors that have been identified previously as important determinants of seeking health care. Powell et al. (35) proposed that negative attitudes and behaviors toward the health-care system also present important barriers to obtaining health care for African-Americans. African-Americans, particularly in lower socioeconomic groups, are often poorly informed about prostate cancer (36,37) and are less willing than non-Hispanic whites to participate in screening programs (38).
Another explanation for the lack of association between cancer stage and conventional socioeconomic factors is that biologic factors, such as tumor aggressiveness, may better explain the advanced stage of prostate cancer at presentation in African-Americans. When we adjusted for either clinical factors (comorbidity, urinary symptoms, and PSA testing) or tumor aggressiveness (Gleason score), we observed comparable confounding effects on the association between race/ethnicity and presenting with advanced-stage disease. However, 33% of all prostate cancers and 66% of advanced-stage cancers were associated with Gleason scores from 7 to 10. None of the other adverse clinical factors (high comorbidity scores, frequent urinary symptoms, or lack of PSA testing) were as prevalent as high Gleason scores, and they accounted for a much smaller proportion of advanced-stage disease. African-Americans appeared to have more aggressive cancers because they had the highest overall proportion of poorly differentiated cancers (16.8%) and were more likely than non-Hispanic whites to have poorly differentiated cancers within all clinical stages except T2. Our findings agree with those of other investigators, who have also reported African-Americans having an increased stage-adjusted burden of high histologic-grade cancer (21,3941). Nonetheless, separating the variables into socioeconomic and tumor aggressiveness factors may not be a helpful distinction, because studies have suggested that African-Americans' increased risk for aggressive cancer may be related to the influence of socioeconomic factors, such as diet or lifestyle on androgen status or genetic susceptibility (4245).
A potential limitation to our study was selection bias: 44.1% of the eligible subjects were excluded because they did not complete a 6-month questionnaire and/or they did not have their medical records abstracted. Excluded patients were different from responders in race/ethnicity and insurance status. However, when we analyzed the collected data by use of survey nonresponse weights, which are equal to the inverse of the response level within each sampling stratum, the estimates for the regression coefficients were not substantially changed. Furthermore, there were no substantial differences between responders and nonresponders in age distribution, previous PSA testing, or Gleason score. Because these factors were the most important potential confounders in our study cohort, the relative similarity between responders and nonresponders suggested that important selection bias was unlikely.
Because there are no primary prevention strategies for prostate cancer, reducing the racial disparity in stage and survival may require offering African-Americans earlier and more aggressive screening. The rationale for this approach comes from recent data showing declining incidence rates of advanced-stage prostate cancer and an increasing proportion of clinically localized cancers in men overall (3), findings that may be partly attributable to the advent of PSA testing (2). The American Urological Association (46) and the American Cancer Society (47) identify African-Americans as a high-risk group and recommend annual screening with digitalrectal examination and PSA beginning at age 40 years, a decade earlier than recommended for men of average risk. However, currently there are no data from randomized controlled trials showing that screening decreases the proportion of advanced-stage disease or reduces mortality. Although results from ongoing screening studies (48,49) should eventually provide guidance for PSA testing, these studies are several years from completion.
Ultimately, any efforts to reduce prostate cancer mortality in African-Americans will have to address the factors accounting for the racial disparity in clinical stage at diagnosis. Our results suggest that conventional socioeconomic factors, clinical factors, or tumor grade do not fully explain this disparity. Therefore, further research needs to be directed at the identification of biologic markers and genetic susceptibility factors, as well as additional socioeconomic factors, including use of health-care systems, distance from health care, diet, literacy, and health beliefs.
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NOTES |
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Supported by Public Health Service contracts N01PC67007, N01CN67009, N01PC67010, N01PC67006, N01PC67005, and N01PC67000 from the National Cancer Institute, National Institutes of Health, Department of Health and Human Services, and by the Department of Veterans Affairs Medical Center, Albuquerque, NM.
Presented in part at the 22nd Annual Meeting of the Society of General Internal Medicine, San Francisco, CA, May 1, 1999.
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Manuscript received March 22, 2000; revised December 6, 2000; accepted December 18, 2000.
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