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© 2002 American Society for Clinical Oncology How Sociodemographics, Presence of Oncology Specialists, and Hospital Cancer Programs Affect Accrual to Cancer Treatment TrialsByFrom the Walter Reed Army Institute of Research, Rockville, and National Cancer Institute, Bethesda, MD. Address reprint requests to Edward L. Trimble, MD, National Cancer Institute, 6130 Executive Blvd, Suite 7025, MSC 7436, Bethesda, MD 20982-7436; email: tt6m{at}nih.gov
PURPOSE: We chose to examine the impact of socioeconomic factors on accrual to National Cancer Institute (NCI)–sponsored cancer treatment trials. PATIENTS AND METHODS: We estimated the geographic and demographic cancer burden in the United States and then identified 24,332 patients accrued to NCI-sponsored cancer treatment trials during a 12-month period. Next, we examined accrual by age, sex, geographic residence, health insurance status, health maintenance organization market penetration, several proxy measures of socioeconomic status, the availability of an oncologist, and the presence of a hospital with an approved multidisciplinary cancer program. RESULTS: Pediatric patients were accrued to clinical trials at high levels, whereas after adolescence, only a small percentage of cancer patients were enrolled onto clinical trials. There were few differences by sex. Black males as well as Asian-American and Hispanic adults were accrued to clinical trials at lower rates than white cancer patients of the same age. Overall, the highest observed accrual was in suburban counties. Compared with the United States population, patients enrolled onto clinical trials were significantly less likely to be uninsured and more like to have Medicare health insurance. Geographic areas with higher socioeconomic levels had higher levels of clinical trial accruals. The number of oncologists and the presence of approved cancer programs both were significantly associated with increased accrual to clinical trials. CONCLUSION: We must work to increase the number of adults who enroll onto trials, especially among the elderly. Ongoing partnership with professional societies may be an effective approach to strengthen accrual to clinical trials.
MANY CONSIDER THE cancer care provided in National Cancer Institute (NCI)–sponsored clinical trials to represent the state of the art. The NCI sponsors multicenter, prospective clinical trials to evaluate treatment for cancer patients primarily through its system of Clinical Trials Cooperative Groups (CTCGs). These nine CTCGs conduct phase I, II, and III clinical trials. Results of these trials are commonly used to guide therapy for cancer patients in the United States and elsewhere. The NCI has previously reviewed data on accruals from all cooperative groups to determine whether the patients enrolled onto these clinical trials were representative of cancer patients in the United States. The purpose of these analyses has been to ensure that the trials sponsored by the NCI would generate information to help guide therapy for the broad range of cancer patients in the United States, as well as to document compliance with Federal law and National Institutes of Health (NIH) guidelines. In this study, we examined the impact of patient age, sex, race/ethnicity, state and region of residence, and various proxies of socioeconomic status (SES) on accrual to trials conducted by the NCI’s CTCGs during a 12-month period. In addition, we explored the possibility of a correlation between clinical trial accrual and the number of oncology specialists, the presence of hospital-based multidisciplinary cancer programs, and the unemployment rate in the state of residence.
Our goal was to assess how representative cancer patients accrued to NCI-sponsored treatment trials are of new cancer patients in the entire United States for a range of socioeconomic, demographic, and geographic variables. There is no national cancer reporting system yet in place, so we estimated the geographic and demographic United States cancer burden using Census data and NCI Surveillance, Epidemiology, and End Results (SEER) incidence data. Census Bureau data (http://www.census.gov) includes detailed information on sex, age, race/ethnicity, and health insurance for populations in the United States at the county and state levels. We used United States Census Regions and Divisions for broad geographic analysis. The NCI’s SEER data, based on approximately a 14% sample of incident cancer cases in the United States, provides information on cancer incidence in the United States by age range, sex, and race/ethnicity. We combined census and cancer incidence data to develop a portrait of the geographic and demographic patterns of cancer in the United States. The number of new cancer cases in the United States, using census population estimates at the county level for sex- and race-specific populations, was calculated with estimates of cancer incidence rates from SEER data for these specific sex, age, and racial groupings by county and state. We then assumed that any of these patients with newly diagnosed cancers should have equal probability of access to treatment in an NCI-sponsored cancer treatment clinical trial, based on the actual numbers of patients accrued to such trials nationwide. For each geographic level, we were able to calculate the expected number of cancer patients accrued to clinical trials. Analyses are based on a comparison of the observed number of cancer patients enrolled onto clinical trials to the expected number of cancer patients accrued to clinical trials at each geographic level. We examined accrual by age, sex, geographic location, health insurance status, including state market penetration by health maintenance organizations (HMOs), several proxy markers of SES, including state unemployment rate, average county income level, and county educational level, availability of an oncologist who was a member of the American Society of Clinical Oncology (ASCO), and the availability of a hospital with a cancer program approved by the American College of Surgeons (ACOS) Commission on Cancer (CoC). Data on county income, education level, poverty, and unemployment were obtained from the United States Census (http://www.census.gov). The effect of the urban/rural character of a county and the proximity to a metropolitan statistical area was assessed using Bureau of the Census Beale Coding. Unemployment rates by state were obtained from the United States Bureau of Labor Statistics Web site (http://www.bls.gov). ASCO is a professional society whose members include physicians and other professionals who care for cancer patients. Their membership includes medical, pediatric, radiation, gynecologic, and surgical oncologists. ASCO members were identified via the ASCO Web site (http://www.asco.org). The ACOS CoC grants approvals to hospitals for their cancer programs.1 Approval is based on the presence of a full range of services for cancer patients available at each hospital and by referral, a cancer registry, a program of educational cancer conferences, and a multidisciplinary cancer committee. The CoC also encourages the formation of multidisciplinary tumor boards, which make recommendations for the management of patients’ newly diagnosed cancer. In 1999, the CoC added that each hospital must accrue at least two patients to CTCG studies. ACOS CoC hospitals with ACOS CoC–approved cancer programs were identified via the ACOS Web site (http://www.facs.org). Data on the penetration of HMOs by state was obtained at the Web site of Managed Care On-Line (http://www.mcareol.com/). Through the Cancer Therapy Evaluation Program (CTEP), the NCI provides financial support for CTCGs to conduct research on new and better methods of cancer treatment. As part of its oversight responsibility, CTEP receives quarterly electronic reports from the cooperative groups on patient accrual into treatment trials. We used data from 1 year of accrual (April 1998 to April 1999), a total of 24,332 patients. For each patient, the data consisted of ZIP code of residence, birth date, sex, race/ethnicity, and method of payment. When possible, we used ZIP codes to assign individuals to counties and states. Our analysis did not include data on accrual to NCI-supported clinical trials, conducted under investigator-initiated mechanisms, such as P01 and R01 grants, for whom geographic and demographic data were not available. In addition, geographic and demographic data on accrual to trials conducted at NCI-designated Clinical and Comprehensive Cancer Centers were not available, nor were data on accrual to trials sponsored by pharmaceutical companies outside the CTCGs. Race and ethnicity were coded in accordance with NIH guidelines: American Indian/Alaska Native/Native Hawaiian, Asian and Pacific Islander, black/African-American, Hispanic/Latino, White, other, and unknown. Method of payment was coded as follows: private insurance, Medicare, Medicare and private insurance, Medicaid, Medicaid and Medicare, military and veterans’ insurance, self-pay (no insurance), no means of payment (no insurance), and other/unknown. Two software programs were used for geographic mapping of relevant data: Microsoft MapPoint (version 1.0; Microsoft, Redmond, WA) and ESRI’s ArcView (version 2.3; ESRI, Redlands, CA).
Age The age distribution of patients accrued to NCI-sponsored clinical treatment trials is shown in Table 1. When the number of patients who entered clinical trials is compared with the estimated number of patients with cancer in each decade of age, the pediatric accrual to clinical trials clearly dwarfs that of adult patients (Fig 1). More than half of children aged 5 to 9 years are accrued to NCI-sponsored clinical trials compared with less than 1% of adults aged 75 to 79 years of age. The highest percentage of adult patients is accrued to clinical trials between age 40 and 55 years.
Sex A slight majority (56%) of patients enrolled onto NCI-sponsored clinical treatment trials are female. On the basis of SEER cancer age- and sex-specific data, approximately 47% of patients with newly diagnosed cancer are female, whereas 53% are male. Figure 1 demonstrates the distribution of female-to-male accrual to clinical trials compared with the estimated number of cancer patients by decade of age. There were no significant differences by sex in accrual to clinical trials, although more women than men were accrued to clinical trials from age 30 years onward. Table 2 demonstrates observed accrual by sex among patients with common non–gender-specific cancers, contrasted with the estimated cancer incidence by sex during this same period.2 During the period of observation, 119 trials were open to women with sex-specific cancers and 27 trials were open to men with sex-specific cancers.
Race/Ethnicity Accrual by decade of age and sex for white, black, Hispanic, and Asian Americans is shown in Figs 2 and 3. The percentage of white patients enrolled onto clinical trials parallels that of the overall population. Different patterns are seen for black, Asian-American, and Hispanic cancer patients. Black children and young adults have accrual to clinical trials comparable to their white peers, as do black women. The percentage of black men who have cancer and are from age 30 to 59 years and accrued to clinical trials is markedly lower than the percentage of white men with cancer in this age group. Asian-American and Hispanic children and young adults have accrual to clinical trials comparable to their white peers. Thereafter, from age 30 until age 80 years, the percentage of Asian-Americans and Hispanics, both men and women, accrued to clinical trials is less than that of white men and women. The absolute numbers of black, Asian-American, Hispanic, and white individuals with cancer accrued to clinical trials are shown in Table 3.
Insurance Status Insurance status for the United States population and for patients accrued to NCI-sponsored clinical treatment trials overall is shown in Table 4. Compared with the United States population, patients who are enrolled onto clinical trials are significantly less likely to be uninsured and more likely to have Medicare. We observed no difference between the percentage of individuals who have private insurance and are enrolled onto clinical trials and the percentage of individuals who have private insurance in the general population. We did observe a trend toward lower accrual in states with the highest HMO market penetration (P = .076). In the quartile of states with the highest HMO market penetration (average 41%), the median observed/expected accrual was 0.9, compared with 1.1 in the lower three quartiles of states (data not shown).
Place of Residence A patient’s place of residence, as determined by ZIP code, has a statistically significant effect on accrual to NCI-sponsored clinical trials. Certain states and regional areas of the United States have significantly lower or higher accrual to clinical trials than the nationwide accrual figures (Fig 4). Delaware, Iowa, Minnesota, New Hampshire, and North Dakota had the highest rates of accrual per number of incident cancer cases, whereas Alabama, Arkansas, Florida, Georgia, Kentucky, and West Virginia had the lowest rates of accrual per number of incident cancer cases. Overall, however, the highest observed accrual to clinical trials was in suburban areas (Tables 5 to 7). These analyses were adjusted for population density as well as age, sex, and race/ethnicity cancer incidence patterns.
Income SES also seemed to influence participation in cancer clinical trials. As described above, we used several proxies for SES, including mean county income level, mean county poverty level, mean county education level, and mean state unemployment rate. With all measures, areas with higher socioeconomic levels had significantly higher levels of clinical trials accrual (Tables 5 to 7). Urban areas with high county incomes had the highest rates of observed accruals to clinical trials (data not shown).
Presence of Oncology Specialists
Presence of Hospitals With ACOS-Approved Cancer Programs
Multivariate Analysis
In 2000, it was estimated that 1.2 million cases of cancer would be diagnosed and 552,200 patients would die from cancer. For these patients and their physicians, decisions on therapy are based in large part on what we know about treatment outcomes for patients with similar types and stages of cancer. The most accurate data are derived from the experience of a large group of patients treated in a standard manner, such as those enrolled onto clinical trials. A critical issue, however, is whether the patients enrolled onto clinical trials are representative of the general cancer population. Will treatment identified as effective in a clinical trial be effective when used outside a clinical trial? Are the patients enrolled onto clinical trials different from those who are not enrolled onto clinical trials? We need to answer these questions to study related concerns, including the following: What factors influence accrual to clinical trials? How can we recruit more diverse patients to clinical trials? Our study is limited to 12 months’ accrual and data for approximately 24,000 patients. In addition, we did not have access to data on patients accrued to studies not conducted through the CTCGs, such as those at NCI-designed cancer centers or those run by the pharmaceutical industry. Our conclusions, therefore, should not be extended to the general population of cancer patients enrolled onto all clinical trials. The strong accrual of children to NCI-sponsored cooperative group trials has previously been noted. More than half of children aged 0 to 10 years are accrued to clinical trials. The centralized nature of cancer care for children, in which most children with cancer are treated at pediatric hospitals with expertise in cancer management, seems to facilitate accrual to clinical trials. The proportion of children accrued varies by diagnosis and whether a national trial is available.3 The commitment of the pediatric oncology community to clinical trials should also be underscored. The marked improvement in survival for children with cancer is due in large part to the timely completion of clinical trials, as well as to the widespread adoption of recommendations for treatment derived from these trials. In general, there does not seem to be major racial/ethnic variation in outcome among children with cancer. Among the minority groups studied, blacks, Asian-Americans, and Hispanics, children ages 0 to 10 years are accrued at rates comparable to white children. Previous studies have shown that accrual of adolescent cancer patients into clinical trials was lower than that for children.3 Our study shows the same. To some extent, the lower accrual rate represents the occurrences in adolescents of tumor types for which survival is excellent and for which clinical trials are not available (eg, thyroid cancer, low-stage melanoma). Even for tumor types for which clinical trials are available, such as acute myelogenous leukemia and acute lymphoblastic leukemia, accrual rates for adolescents are lower than those for younger children. The Children’s Oncology Group and the NCI have begun a program to encourage the recruitment of adolescents and young adults with cancer into clinical trials. For adult cancer patients, those older than age 19 years, the CTCGs accrue only 2.5% of cancer patients. The contrast with children and adolescents is striking. Among adults, those 80 years of age or older are least likely to be enrolled, followed by those aged 30 to 39 years. These data are consistent with two previous studies that examined accrual of older patients to CTCG studies.4,5 A variety of factors have been proposed as potential explanations for the lower trial accrual associated with advancing age. These include patient and physician expectation, lack of social support, comorbidity, and unwillingness to pay for clinical trials by third-party payers. Until recently, the Centers for Medicare and Medicaid Services, which provides Medicare insurance to most older patients in the United States, considered phase I, II, and III clinical trials to be "experimental" and not eligible for coverage. In June 2000, President Clinton issued an executive order mandating that the Centers for Medicare and Medicaid Services pay for patient care costs associated with NIH-sponsored clinical trials. As of September 17, 2000, the categories of trial discussed in this article are now eligible for coverage. Doubling the number of adult patients enrolled onto cancer treatment trials, from 2.5% to 5%, would permit more rapid completion of ongoing trials and future trials. The NCI and the National Institute on Aging (NIA) have supported research in the CTCGs to identify appropriate treatment for older patients. Three trials whose eligibility is restricted to patients older than 60 years are currently open. The NIA has also funded the CTCGs to study barriers to clinical trials among patients with breast cancer and ovarian cancer.6,7 The NIA and NCI have jointly issued a Program Announcement (98-069) soliciting research proposals into the treatment of cancer among older patients. No research proposals have yet been funded under this program announcement. There are no marked differences between the accrual of men and women to clinical trials for those between ages 0 and 39 years and those 70 years or older. Between the ages of 40 and 69 years, women are accrued at higher rates than men. This discrepancy may reflect the greater burden of breast and gynecologic cancers on women during these years, as well as the ongoing commitment of the cooperative groups to study cancers that occur in women. Six of the nine cooperative groups conduct breast cancer studies, for example, and three groups conduct studies among women with gynecologic cancer. Among the common cancers that are not sex-specific, fewer women were accrued than men. In accordance with NIH guidelines regarding accrual of women to clinical trials, cited below, we will continue to monitor these accrual rates closely to determine whether efforts to recruit women with these particular cancers should be strengthened. The NIH Revitalization Act of 1993 (Public Law 103-43) mandated that NIH ensure that women and minorities and their subpopulations be included in all human subject research, that women and minorities and their subpopulations be included in phase III clinical trials in numbers adequate to allow for valid analyses of differences in intervention effect, and that NIH initiate programs and support for outreach efforts to recruit and retain women and minorities and their subpopulations as volunteers in clinical studies. The NIH subsequently developed guidelines for the inclusion of women and minorities in clinical research, published in the Federal Register in March 1994. The Institute of Medicine has recently issued a report, The Unequal Burden of Cancer: An Assessment of NIH Research and Programs for Ethnic Minorities and the Medically Underserved.8 Among the recommendations made by the Institute of Medicine’s Committee on Cancer Research Among Minorities and the Medically Underserved were that the NCI work with other institutions to overcome barriers to clinical trials accrual among ethnic minority and medically underserved patients, as well as report on their accrual and retention in clinical trials. They also recommended that accrual among rural residents, individuals without insurance, and individuals of low SES or level of literacy be reported. In 1998 and 1999, the NCI sponsored workshops on the participation of minorities and women in clinical cancer research. Proceedings of these workshops, which included both cancer treatment and cancer prevention trials, have been published.9 Studies suggest that there is limited genetic variability between racial and ethnic groups.10,11 If so, then the race/ethnicity per se of a cancer patient may not influence response to treatment and outcome. More likely, cultural milieu and SES will affect a cancer patient’s willingness to participate in cancer prevention activities, cancer screening programs, and regular medical care and clinical trials and adhere to recommended cancer treatment. Race and ethnicity, however, may function as a proxy for cultural and socioeconomic factors, which in turn may influence a patient’s perspective on clinical trials. In addition, a person’s SES may well affect the presence of comorbidities.12-14 Nonetheless, in certain cancer sites, it seems that race/ethnicity may function as a proxy for biologic differences in cancers. The breast cancers that occur among black women under age 40 years, for example, seem to be more aggressive than those that occur among their aged-matched white peers.15,16 Both the age distribution of prostate cancer and prostate-specific antigen expression that occur in black men are different from those in white men.17-19 Compared with children with cancer, all racial and ethnic groups with cancer are underrepresented in clinical trials. Only 2.5% of adult cancer patients are enrolled onto treatment trials, contrasted with 50% of children with cancer. Up to age 29 years, the rates of accrual to clinical trials for black, Asian-American, Hispanic, and white individuals are comparable. Between ages 30 and 79 years, however, accrual rates for black men as well as Asian-American and Hispanic men and women are slightly lower that those of white, age-matched peers. The data on the younger age groups suggest that there may well be among minority adult populations barriers to cooperative group trials that are not present among children. Improved access to medical care and a reduction in socioeconomic disparities are needed to strengthen accrual to clinical trials. In addition, more efforts to elucidate the molecular genetics of cancer will permit us to delineate the relative contributions of SES, race/ethnicity, and cancer biology to cancer outcome. Altogether, this combination of knowledge and improved access to care may also permit the development of more effective therapy. Regional variation in cancer treatment has previously been reported. We now report marked regional and state variation in accrual of patients to clinical trials. We need to ascertain why these differences exist. Do they reflect state and local efforts to improve access to cancer specialists and treatment? Does physician commitment to clinical trials vary geographically? What is the interaction between the different NCI-sponsored mechanisms for clinical trials support and observed accrual? The NCI’s Community Clinical Oncology Program, for example, sponsors multiple sites in the West North Central Region, where trial accrual is highest in the nation. The NCI is currently evaluating a number of approaches to enhance accrual to clinical trials.20 The pattern of accruals also points out areas where promotion of clinical trials might be effective. The NCI does not pay for the routine patient care costs associated with NCI-sponsored cancer clinical trials. These costs have been paid by third-party payers or the patients themselves or absorbed by the treating physicians and institutions. The NCI has worked closely with private third-party payers to gain their support for clinical cancer trials coverage. The NCI has signed clinical trials agreements with both the Department of Defense (DOD) and the Department of Veterans Affairs so that men and women who are eligible for care through these two systems can have access to NCI-sponsored clinical trials. The DOD is currently making coverage of phase II and III treatment trials, as well as prevention and early detection trials, a permanent benefit. In addition, the DOD is beginning a demonstration project for phase I trials. The recent Presidential directive will permit the Centers for Medicare and Medicaid Services to pay for patient care costs of Medicare patients who are enrolled onto clinical cancer trials. We did observe a trend suggesting a detrimental effect on clinical trial accrual associated with increasing HMO market penetration. Ongoing dialogue among the NCI, HMO leadership, and cancer advocacy groups will be needed to ensure that patients who are covered by HMOs have access to NCI-sponsored clinical trials. A recent estimate suggests that 44 million Americans lack health insurance.21 Uninsured patients are more likely to present with advanced cancer and to have delays getting access to cancer specialists. Uninsured patients are also more likely to be of lower SES and less likely to have effective social support.22,23 In our data, patients accrued to clinical trials were significantly less likely to be uninsured compared with the general population. Patients accrued to clinical trials were also more likely to have Medicare than the general population. SES has been noted to affect cancer stage at diagnosis as well as cancer outcome.23-25 Lower SES levels are associated with more advanced stage at diagnosis and cancer outcome. Proxy measures for SES include family income, education level, and location of residence. NCI currently requires that the cooperative groups collect ZIP code of residence for cancer patients accrued to clinical trials. In our study, the mean income of the county of residence was strongly associated with the level of clinical trials accrual. Cancer patients who lived in counties with a higher mean income level were more likely to be accrued into clinical trials than cancer patients who lived in counties with lower income levels. Other proxy measures of SES, namely, percentage of the population in poverty, unemployment rates, and education level of the population, had the same correlation with clinical trials accrual. Accrual to recent large breast and prostate prevention trials has also been characterized by a large proportion of patients with higher education levels than the national average.26,27 Recruitment to prevention trials, however, may be more difficult than recruitment to treatment trials. Patients who have received a diagnosis of cancer and know that they need treatment may be more amenable to the possibility of a treatment trial than would an asymptomatic patient who is at risk for cancer and is offered a prevention trial. Additional efforts will be necessary to increase the proportion of cancer patients of low SES to clinical trials.28 These efforts may require additional time and expenditures for trial promotion, recruitment, and retention among traditionally underserved populations. Recent work in the NCI-sponsored ASCUS-LSIL Triage Study, for women with abnormal Pap smears, has demonstrated that such targeted efforts can be successful in recruiting and retaining in clinical trials individuals of low SES.29 The ASCO represents physicians and other professionals who care for cancer patients. Their stated goals include "advocating public policy . . . that support increased clinical cancer research" and "advancing the training of physicians . . . in clinical cancer research." A recent survey of 5,900 cancer patients found that patients were more likely to participate in a clinical trial when their doctor helped them find an appropriate trial, educated them about the pros and cons of clinical trials participation, and encouraged them to consider a clinical trial.30 As part of the same effort, 225 oncologists were surveyed. These oncologists reported that the additional paperwork associated with clinical trials was an obstacle to their participation in clinical trials. Our study found that the number of ASCO physicians per 1,000 cancer patients was positively associated with the number of patients accrued to clinical trials, underscoring the importance of NCI partnership with ASCO and other professional societies to enhance clinical trials accrual. Recent NCI efforts to overcome barriers to clinical trials accrual, including paperwork, may be found on the NCI Web site (http://cancertrials.nci.nih.gov/system/index.html). The ACOS CoC mandates that hospital cancer programs have a full range of services for cancer patients available at each hospital and by referral, a cancer registry, a program of educational cancer conferences, and a multidisciplinary cancer committee. The CoC also encourages the formation of multidisciplinary tumor boards, which make recommendations for the treatment of patients with newly diagnosed cancer. In 1999, the CoC added that each hospital must accrue at least two patients to cooperative group studies. In our analysis, the presence of a CoC-approved tumor program was even more important than the number of ASCO physicians in strengthening clinical trials accrual. This may reflect the benefit of a multidisciplinary forum committed to evidence-based medicine, as well as an institutional commitment to clinical cancer research. In conclusion, our "snapshot" of accrual to NCI-sponsored CTCG treatment studies served to focus attention on several issues. To enhance clinical trials accrual, we must work to increase the number of adults who are enrolled onto trials, particularly among the elderly. Continued efforts to recruit black, Asian-American, and Hispanic adults are also needed. Social marketing, based on consumer demographics, which has been used in prevention and screening efforts, may also be helpful in promoting accrual and retention of cancer patients in clinical trials. A more accurate proxy measure of SES would improve future analyses. Certain states seem to be excellent targets for promotion of accrual to clinical trials. Ongoing partnership with professional societies and the ACOS CoC also may be an effective approach to strengthen accrual to clinical trials. Finally, we must continue to encourage third-party payers to support the participation of cancer patients in clinical trials.
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Landis SH, Murray T, Bolden S, et al: Cancer statistics, 1999. CA Cancer J Clin 49: 8-31, 1999 3. Bleyer WA, Tejeda H, Murphy SB, et al: National cancer clinical trials: Children have equal access; adolescents do not. J Adolesc Health 21: 366-373, 1997[CrossRef][Medline]
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Hutchins LF, Unger JM, Crowley JJ, et al: Underrepresentation of patients 65 years of age or older in cancer-treatment trials. N Engl J Med 341: 2061-2067, 1999 5. Trimble EL, Carter CL, Cain D, et al: Representation of older patients in cancer treatment trials. Cancer 74: 2208-2214, 1994 (suppl)[CrossRef][Medline] 6. Moore DH, Brunetto V: The impact of age upon protocol versus alternative treatment of women with ovarian cancer. Gynecol Oncol 68: 118, 1998 (abstr 190) 7. Kemeny M, Muss HB, Kornblith AB, et al: Barriers to participation of older women with breast cancer in clinical trials. Proc Am Soc Clin Oncol 19: 602a, 2000 (abstr 2371) 8. Haynes MA, Smedley BD: Institute of Medicine (US) Committee on Cancer Research Among Minorities and the Medically Underserved. Washington, DC, National Academy Press, 1999 9. Underwood SM, Alexander GA: Participation of minorities and women in clinical cancer research. Ann Epidemiol 10: S1-S2, 2000[CrossRef] 10. Mountain JL, Cavalli-Sforza LL: Multilocus genotypes, a tree of individuals, and human evolutionary history. Am J Hum Genet 61: 705-718, 1997[Medline]
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Goodman AH: Why genes don’t count (for racial differences in health). Am J Public Health 90: 1699-1702, 2000
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Brawley OW, Freeman HP: Race and outcomes: Is this the end of the beginning for minority health research? J Natl Cancer Inst 91: 1908-1909, 1999 13. Freeman HP: The meaning of race in science: Considerations for cancer research—Concerns of special populations in the National Cancer Program. Cancer 82: 219-225, 1998[CrossRef][Medline]
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Smith GD: Learning to live with complexity: Ethnicity, socioeconomic position, and health in Britain and the United States. Am J Public Health 90: 1694-1698, 2000 15. Franzini L, Williams AF, Franklin J, et al: Effects of race and socio-economic status on survival of 1,332 black, Hispanic, and white women with breast cancer. Ann Surg Oncol 4: 111-118, 1997[CrossRef][Medline] 16. Lyman GH, Kuderer NM, Lyman SL, et al: Importance of race upon breast cancer survival. Ann Surg Oncol 4: 80-87, 1997[CrossRef][Medline] 17. Fowler JE Jr, Bigler SA: A prospective study of the serum prostate specific antigen concentrations and Gleason histologic scores of black and white men with prostate carcinoma. Cancer 86: 836-841, 1999[CrossRef][Medline]
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Robbin AS, Whittemore AS, Thom DH: Differences in socioeconomic status and survival among white and black men with prostate cancer. Am J Epidemiol 151: 409-416, 2000 19. Farkas A, Marcella S, Rhoads CG: Ethnic and racial differences in prostate cancer incidence and mortality. Ethn Dis 10: 69-75, 2000[Medline] 20. National Cancer Institute: Cancer Clinical Trials: A New National System. Bethesda, MD, National Cancer Institute. Available at http://www.cancer.gov/common/popups/popNationalSystem.htm
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Adler NE, Boyce WT, Chesney MA, et al: Socioeconomic inequalities in health: No easy solution. JAMA 269: 3140-3145, 1993 23. Auvinen A, Karjalainen S: Possible explanations for social class differences in cancer patient survival, in Kogevinas M, Pearce N, Susser M, et al (eds): Society Inequalities and Cancer. Lyon, France, International Agency for Research on Cancer, 1997, pp 377-397 (IARC Scientific Publications No 138) 24. Kogevinas M, Porta M: Socioeconomic differences in cancer survival: A review of the evidence, in Kogevinas M, Pearce N, Susser M, et al (eds): Society Inequalities and Cancer. Lyon, France International Agency for Research on Cancer, 1997, pp 177-206 (IARC Scientific Publications No 138)
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Boyd C, Zhang-Salomons JY, Groome PA, et al: Associations between community income and cancer survival in Ontario, Canada, and the United States. J Clin Oncol 17: 2244-2255, 1999
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Fisher B, Costantino JP, Wickerham DL, et al: Tamoxifen for prevention of breast cancer: Report of the National Surgical Adjuvant Breast and Bowel Project P-1 Study. J Natl Cancer Inst 90: 1371-1388, 1998 27. Brawley OW, Parnes H: Prostate cancer treatment trials in the United States of America. Eur J Cancer 36: 1312-1315, 2000 28. McCabe MS, Varricchio CG, Padberg RM: Efforts to recruit the economically disadvantaged to national clinical trials. Semin Oncol Nurs 10: 123-129, 1994[CrossRef][Medline] 29. Schiffman M, Adrianza ME: ASCUS-LSIL Triage Study: Design, methods, and characteristics of trial participants. Acta Cytol 44:726-742, 200 30. Comis RL, Aldige CR, Stovall EL, et al: A quantitative survey of public attitudes towards cancer clinical trials. Proc Am Soc Clin Oncol 19: 451a, 2000 (abstr 1769) Submitted January 12, 2001; accepted January 28, 2002.
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Copyright © 2002 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
