Context Despite the importance of diversity of cancer trial participants with
regard to race, ethnicity, age, and sex, there is little recent information
about the representation of these groups in clinical trials.
Objective To characterize the representation of racial and ethnic minorities,
the elderly, and women in cancer trials sponsored by the National Cancer Institute.
Design, Setting, and Patients Cross-sectional population-based analysis of all participants in therapeutic
nonsurgical National Cancer Institute Clinical Trial Cooperative Group breast,
colorectal, lung, and prostate cancer clinical trials in 2000 through 2002.
In a separate analysis, the ethnic distribution of patients enrolled in 2000
through 2002 was compared with those enrolled in 1996 through 1998, using
logistic regression models to estimate the relative risk ratio of enrollment
for racial and ethnic minorities to that of white patients during these time
periods.
Main Outcome Measure Enrollment fraction, defined as the number of trial enrollees divided
by the estimated US cancer cases in each race and age subgroup.
Results Cancer research participation varied significantly across racial/ethnic
and age groups. Compared with a 1.8% enrollment fraction among white patients,
lower enrollment fractions were noted in Hispanic (1.3%; odds ratio [OR] vs
whites, 0.72; 95% confidence interval [CI], 0.68-0.77; P<.001) and black (1.3%; OR, 0.71; 95% CI, 0.68-0.74; P<.001) patients. There was a strong relationship between age and
enrollment fraction, with trial participants 30 to 64 years of age representing
3.0% of incident cancer patients in that age group, in comparison to 1.3%
of 65- to 74-year-old patients and 0.5% of patients 75 years of age and older.
This inverse relationship between age and trial enrollment fraction was consistent
across racial and ethnic groups. Although the total number of trial participants
increased during our study period, the representation of racial and ethnic
minorities decreased. In comparison to whites, after adjusting for age, cancer
type, and sex, patients enrolled in 2000 through 2002 were 24% less likely
to be black (adjusted relative risk ratio, 0.76; 95% CI, 0.65-0.89; P<.001). Men were more likely than women to enroll in
colorectal cancer trials (enrollment fractions: 2.1% vs 1.6%, respectively;
OR, 1.30; 95% CI, 1.24-1.35; P<.001) and lung
cancer trials (enrollment fractions: 0.9% vs 0.7%, respectively; OR, 1.23;
95% CI, 1.16-1.31; P<.001).
Conclusions Enrollment in cancer trials is low for all patient groups. Racial and
ethnic minorities, women, and the elderly were less likely to enroll in cooperative
group cancer trials than were whites, men, and younger patients, respectively.
The proportion of trial participants who are black has declined in recent
years.
Ten years have passed since Congress responded to concerns about unequal
access to clinical trials and enacted the National Institutes of Health (NIH)
Revitalization Act, which encouraged representation of women and minority
patients in NIH-sponsored research.1 Ensuring
broad access to research studies has subsequently been an important aim of
national research policy. The National Cancer Institute (NCI) has addressed
concerns about enhancing heterogeneity of trial populations through multiple
mechanisms, including the creation of Minority Community Clinical Oncology
Programs, the development of focused initiatives in partnership with the Centers
for Disease Control and Prevention and academic medical centers, and emphasis
on trials that focus specifically on the elderly.2,3 Moreover,
while the NCI budget has grown from approximately $2 billion in 1993 to approximately
$4 billion in 2002,4 and the number of trial
participants has increased, it is not clear if minorities, women, and the
elderly have shared in this growth.5
Investigations of race- and sex-based disparities in cancer trial participation
have yielded conflicting results. A study of black and Hispanic participation
between 1991 and 1994 concluded that these groups were represented in cancer
trial populations in equal proportion to the cancer disease burden in these
groups.6 This report was confirmed by a subsequent
analysis of enrollment by the Southwestern Oncology Group that compared the
proportion of blacks and Hispanics enrolled in trials for 15 cancer types
with their share of the US cancer population between 1993 and 1996.7 Notably, the authors found that representation of
minorities varied substantially with the type of cancer. Blacks with leukemia,
head and neck, or prostate cancer were more likely than white patients to
enroll, while blacks with lymphoma or ovarian cancer were less likely than
whites to enroll.7 Similarly, studies have
found equivalent representation of women and men for some non–sex-specific
conditions, and a sex disparity for others.7-10 The
study of Southwestern Oncology Group enrollment (1993-1996) noted sex disparities
in only 3 of the 11 cancer types.7 However,
it is unclear whether race and sex disparities are present in more recent
studies, or whether they persist after accounting for age.
Recommendations for enrollment of elderly patients were conspicuously
absent from the NIH Revitalization Act. Although elderly patients represent
approximately two thirds of cancer patients, they account for only 25% to
30% of clinical trial participants.7,11 Elderly
minorities, theoretically subject to the combined barriers to participation
that characterize elderly and minority communities, may have the greatest
risk of low trial participation.12-14 However,
there is a paucity of contemporary data about the enrollment of elderly minority
patients in cancer research trials.
Given the importance of broad representation in cancer trials and the
considerable emphasis that Congress has placed on achieving this goal, we
conducted 2 complementary analyses of recent enrollment in NCI-sponsored Clinical
Trial Cooperative Group therapeutic trials. First, we compared patients enrolled
in breast, colorectal, lung, or prostate trials in 2000 through 2002 with
population-based cancer incidence data. We determined whether age, sex, or
racial and ethnic disparities in participation exist, and whether the magnitude
of disparities varies according to age group and cancer type. We then assessed
temporal changes in enrollment among racial and ethnic groups, comparing patients
enrolled in 2000 through 2002 with those enrolled in 1996 through 1998.
Enrollment data for NCI-sponsored therapeutic trials for 1996 through
2002 were obtained from the NCI Clinical Data Update Service, a database that
contains patient-level information about participants in all NCI-sponsored
Clinical Trial Cooperative Group trials. Cancer incidence data (1995 through
1999) were obtained from the NCI Surveillance, Epidemiology, and End Results
(SEER) program,15 which incorporates incidence
data from 11 cancer registries across the country and is regarded as the most
authoritative representation of national cancer trends.15 We
obtained information on age exclusion criteria for the 50 largest trials from
the NCI's PDQ Database of Clinical Trials.16 Because
none of these databases included personal identifiers, this study received
a waiver of the informed consent requirement.
National and SEER county population estimates by 5-year age group, race,
ethnicity, and sex were obtained from the bridged single race estimates provided
in the US census.17,18 In the
2000 census, 2% of the US population indicated more than 1 racial category.18,19 To reconcile the census 2000 data
with other databases that only allow a single race for each individual, these
bridged estimates use a complex formula to assign races to individuals who
had indicated more than 1 race.17
Our study included participants in breast, colorectal, lung, and prostate
cancer trials, as these were the 4 most common causes of cancer-related mortality
during the study period.20 Only female participants
were included for breast cancer trials since the number of male participants
was negligible. We only included participants in cooperative group therapeutic
trials who were 30 years of age and older and had a single documented racial
or ethnic group, age, and sex. Trials of surgical interventions were excluded.
Race and Ethnicity. From 1996 through 2001, Cancer Therapy Evaluation Program (CTEP) trial
participants were assigned to 1 of 5 mutually exclusive categories: white,
black, Asian/Pacific Islander, American Indian/Alaskan Native, or Hispanic.
In 2002, CTEP required that race and ethnicity (Hispanic or non-Hispanic)
be coded as separate categories. To reconcile the 2002 race/ethnicity definitions
with the CTEP data from prior years, we defined all participants who indicated
that they were of Hispanic ethnicity as "Hispanic." Population data from the
US census were assigned to 1 of the following mutually exclusive groups: Hispanic,
white non-Hispanic, black non-Hispanic, Asian/Pacific Islander non-Hispanic,
and American Indian/Alaskan Native non-Hispanic.
Cancer Incidence. Cancer incidence rates in each 5-year age, race, and sex category were
estimated by dividing the number of cases in SEER by the corresponding population
of the SEER counties. These rates were then applied to the corresponding categories
in the US population and then summed over all categories for national estimates
of annual cancer incidence for each category of interest.7,21 Cancer
incidence was assumed to be fixed during the study period.
We defined the enrollment fraction as the number
of trial enrollees divided by the estimated US cancer cases in each subgroup.
Pearson χ2 tests of independence were performed to assess the
relationship between enrollment fractions in various racial/ethnic and age
groups in the 2000 through 2002 time period. Similar tests were conducted
after stratifying by age and cancer type, and crude odds ratios (ORs) were
estimated within each strata. We performed sex comparisons for the 2 non–sex-specific
cancers in our analysis, colorectal and lung cancer.
For the analysis of temporal changes, we compared the proportion of
trial participants represented by each racial or ethnic group in 2000 through
2002 with the proportion enrolled in 1996 through 1998. Patients enrolled
in 1999 were omitted from this analysis, as preliminary multivariate analysis
suggested that trends in representation of some racial groups began to change
during this year. We used a polytomous logistic regression model to determine
the relationship between time period and racial distribution of trial participants,
using racial group as the outcome variable and adjusting for age, cancer type,
and sex. We used this approach because the outcome consisted of multiple nominal
categories (ie, 5 racial groups), and this method allowed us to use a single
model to assess the relation between time and racial distribution. We performed
tests for interaction between cancer type and time period and patient age
group and time period. To account for the fact that participants might be
independent across trials, but not necessarily within trials, we used Huber-White
robust variance estimates to allow for clustering by trial.22 We
conducted a sensitivity analysis by repeating the regression using only the
50 largest trials, and again after excluding the 4 trials from this sample
that had age limits on eligibility. STATA 6.0 was used for all analyses.22
From 1996 through 2002, 75 215 patients were enrolled in NCI-sponsored
cooperative group nonsurgical treatment trials for breast, lung, colorectal,
or prostate cancers (Table 1).
Approximately 3.1% of trial participants were Hispanic, 85.6% were white,
9.2% were black, 1.9% were Asian/Pacific Islanders, and 0.3% were American
Indians/Alaskan Natives. Table 1 also
includes the proportion of cancer patients 30 years of age and older diagnosed
in the United States in 2000 in each racial and ethnic group, as well as the
distribution of race and ethnicity in the general population of adults. Breast
cancer patients represented 54.2% of trial participants, although they accounted
for only 27.9% of incident cancer cases. Although cancer incidence was evenly
divided among the 3 age groups (30-64, 65-74, ≥75 years), the representation
of trial participants was heavily skewed toward the youngest age group (68.0%
of trial participants were 30-64 years old).
Trial participants represented approximately 1.7% of the total number
of incident cancer cases diagnosed during the 2000 through 2002 study period
(Table 2). When all 4 cancer types
were considered in aggregate, Hispanics and blacks were underrepresented.
Compared with a 1.8% enrollment fraction among white cancer patients, only
1.3% of Hispanic patients (OR vs whites, 0.72; 95% confidence interval [CI],
0.68-0.77; P<.001) and 1.3% of black patients
(OR, 0.71; 95% CI, 0.68-0.74; P<.001) participated
in trials. The enrollment fraction of Asian/Pacific Islanders (1.7%) was not
significantly different than for whites. American Indians/Alaskan Natives
had a higher enrollment fraction than whites (2.5% vs 1.8%) that was statistically
significant (P<.001).
The enrollment fractions varied substantially with cancer type, as did
racial disparities in enrollment fractions (Table 2). While breast cancer trial participants represented 3.2%
of incident breast cancer patients, the enrollment fraction was only 1.9%
for colorectal cancer and 0.8% for patients with either lung or prostate cancer.
Black patients with breast, colorectal, or lung cancers were significantly
less likely to participate in trials than were their white counterparts (ORs:
0.74, 0.64, 0.61, respectively; P<.001 for all
ORs). In contrast, the enrollment fractions for blacks were slightly greater
than for whites in prostate cancer trials (1.0% of blacks vs 0.8% of whites;
OR, 1.18; 95% CI, 1.09-1.28; P<.001). Hispanic
patients were less likely to enroll than white patients for all 4 cancer types,
whereas Asian/Pacific Islanders were less likely to enroll than white patients
only for lung and colorectal cancer trials.
There was a strong relationship between age and enrollment fraction.
Among patients 30 to 64 years old, the enrollment fraction was 3.0%, and this
decreased to 1.3% among 65- to 74-year-old patients and 0.5% for patients
75 years of age and older (Table 3).
In each racial group, there were significantly lower enrollment fractions
for elderly patients. The OR for trial enrollment for white elderly (≥75
years) patients vs nonelderly (30-64 years) patients was 0.14 (95% CI, 0.14-0.15; P<.001). For black cancer patients 75 years of age and
older, the enrollment fraction was 0.4% compared with 1.8% for nonelderly
black cancer patients (OR, 0.24; 95% CI, 0.21-0.27; P<.001).
Similar disparities were noted in Hispanics, Asian/Pacific Islanders, and
American Indians/Alaskan Natives (Table
3).
Men had higher enrollment fractions than women for trials involving
colorectal cancer (2.1% vs 1.6%; OR, 1.30; 95% CI, 1.24-1.35; P<.001) and lung cancer (0.9% vs 0.7%; OR, 1.23; 95% CI, 1.16-1.31; P<.001 [Table 4]).
When stratified by age group, there was no disparity in enrollment rates between
young men and women (younger than 65 years). Among elderly subgroups, however,
statistically significant disparities were noted. Among colorectal cancer
patients, men 65 to 74 years of age were more likely to enroll than women
(OR, 1.18; 95% CI, 1.08-1.28; P<.001); the sex
disparity was somewhat larger in the 75 years and older age group (OR, 1.54;
95% CI, 1.35-1.76; P<.001). Similar findings were
noted in lung cancer patients. Although there was no significant sex disparity
in the youngest age group, disparities were noted in patients 65 to 74 years
of age (OR, 1.40; 95% CI, 1.26-1.56; P<.001) and
for the 75 years and older age group (OR, 1.71; 95% CI, 1.41-2.07; P<.001).
Temporal Changes in Enrollment
From 1996 through 2002, the annual number of trial participants increased
from approximately 8000 to approximately 12 000 (Table 5). During this period, the percentage of trial participants
who were racial or ethnic minorities decreased. Hispanic and black patients
represented 3.7% and 11.0% of trial participants in 1996, respectively. These
respective groups represented 3.0% and 7.9% of participants in 2002. After
adjusting for age, sex, and cancer type, participants enrolled in 2000 through
2002 were less likely to be black (in comparison to whites; adjusted relative
risk ratio, 0.76; 95% CI, 0.65-0.89; P<.001) than
those enrolled in 1996 through 1998. There was no significant change in the
representation of other racial and ethnic groups during the study period.
The results did not change when analyzing only the 50 largest trials or after
excluding the 4 trials from this group that had age exclusions. There were
no significant interactions between time period and either cancer type or
age group. When we performed 2 additional multivariate analyses, using age
(≥65 years) and sex as the outcome variables, respectively, we found that
there was no change in the representation of elderly or women between 1996-1998
and 2000-2002.
Although the trial enrollment rate increased by almost 50% during 1996
through 2002, the proportion of trial participants who were not white actually
declined during this period. These results persisted after accounting for
cancer type, age, and sex and are especially notable given the 1993 NIH Revitalization
Act and the emphasis placed on increasing minority participation in cancer
trials over the past decade. We also found that blacks and Hispanics were
significantly less likely than whites to enroll in NCI-sponsored cooperative
group trials in 2000 through 2002. In our analysis, the magnitude and direction
of racial disparities varied with cancer type. While blacks had significantly
lower enrollment fractions in breast, lung, and colorectal cancer trials when
compared with whites, the representation of blacks and whites in prostate
cancer trials was comparable. This demonstrates that equitable participation
is possible and implies that there may be lessons from the design, marketing,
and recruitment strategies used for prostate cancer trials that can help address
underrepresentation in trials of other cancer types.
Our study also demonstrates that elderly patients, both minorities and
whites, were strikingly underrepresented compared with their younger counterparts.
Although the elderly accounted for approximately one third of participants
in breast, lung, colorectal, or prostate cancer trials, they accounted for
approximately two thirds of patients for these 4 cancer types. This strikingly
low participation rate has been remarkably consistent over the past decade,
as prior work has demonstrated that elderly patients represented approximately
one third of trial participants in 1992, 1993-1996, and 1997-2000.7,11,23 In effect, there has
been little progress in the representation of elderly patients in cancer trials
over the past 10 years. Our finding that elderly minorities are particularly
underrepresented underscores the importance of identifying obstacles to trial
participation for this group.
Of note, sex disparities were a function of age. Men and women 30 to
64 years of age with colorectal or lung cancers were equally likely to participate
in trials; older men were more likely to enroll than older women. Our results,
although limited to 2 cancer types, are consistent with recent reports of
underrepresentation of women in heart failure trials and suggest that there
is an important interaction between age and sex in trial enrollment.8 Further studies are needed to better understand the
social, economic, logistical, and other factors that are responsible for the
disproportionately low enrollment of elderly women.
Past discussions and research on minority enrollment have highlighted
several barriers that are more prevalent among specific minority groups.24 Past and ongoing patterns of discrimination have
also resulted in decreased trust in the health care system in general among
minority patients.12,25,26 Minorities
are more likely to express concerns about exploitation, dishonesty regarding
risks of experimental treatment, and motivations of researchers.27-30 Other
studies have suggested that minority patients may be less likely than whites
to be offered trial participation.31 Socioeconomic
factors also present a substantial barrier, as the disproportionately low
income of many minorities may be associated with lack of access to health
care in general and subsequently to clinical trials.24 Social
and cultural factors are also important, as language and cultural differences
can hinder communication between investigators and prospective participants.26,32,33 Race-related variability
in stage of diagnosis and stringent trial exclusion criteria may also contribute
to disparities in trial eligibility and participation.11,27
Applying trial results to patients who would not have been eligible
to participate has been associated with harm.34 It
has been promulgated that "appropriate" representation of specific patient
subpopulations is necessary to further understanding of race/ethnicity–based
differences in presentation, prognosis, and response to therapy.35-40 The
most commonly used measure of "appropriateness" is proportionality—that
the distribution of trial participants across race or age groups should mirror
the distribution of cancer in the general population.6-8 This
is notably distinct from the "valid analysis" measure of inclusion that forms
the foundation of the NIH Revitalization Act, which requires inclusion of
adequate numbers of minority patients to " . . . conduct valid analyses of
the intervention effect in subgroups."1 However,
it is unlikely that trials that include participants with the same distribution
as can be found in the community will have sample sizes large enough for subgroup
analysis.41,42 Future work should
explore what degree of representation is "optimal," as inadequately powered
subgroup analyses serve little purpose beyond hypothesis generation.41 While ensuring that trial results are generalizable
to the population is imperative, it is still unclear how best to achieve this
goal. In some instances, it might be beneficial to design trials specifically
to address clinical subgroups in instances when differences in presentation,
prognosis, and response to therapy have been suggested by preliminary data.
For instance, some studies should be designed exclusively for racial groups
that face a higher incidence of specific cancer types or for elderly patients
who are more likely to have significant comorbidities that affect presentation
or response to therapy.
We focused on NCI trials because NCI is the single largest sponsor of
cancer trials and has focused on ensuring access to trials for minority and
elderly patients. The NCI group clinical trials database covers the majority
of federally funded cancer trials, but it does not include NCI-funded noncooperative
group trials, or trials funded by private industry, nonprofit foundations,
or other branches of the government. We focused our analysis on 4 cancers
not only because they were the 4 leading causes of cancer death, but also
because they include more than half of NCI group trial participants.7 However, the types of cancer and trials we analyzed
were not inclusive and thus may not be representative. It is also possible
that inaccurate recording of race and ethnicity in either SEER or CTEP data
could affect the accuracy of our results.43 Finally,
our sample size for the Hispanic, American Indian/Alaskan Native, and Asian/Pacific
Islander populations was relatively small, making our results for these groups
less robust.
Whether the rationale for including minorities, women, and the elderly
is framed in terms of equity in access to trials, generalizability of the
results, or the need for valid subgroup analyses, our findings suggest that
the emphasis placed on increasing minority and elderly trial participation
over the last decade has fallen short of the mark. Increases in NCI funding
in the late 1990s and other efforts to enhance trial participation have enhanced
the overall trial enrollment volume, but these gains disproportionately accrued
to white patients. These findings are of concern given the high profile of
minority and elderly underrepresentation and the efforts that the NCI has
made to address this problem.3,44-46 To
ascribe trial designs or inadequate efforts by the NCI as the culprits would
be an oversimplification, as the barriers likely include variations in patient
health status, disease characteristics, attitudes, beliefs, sociodemographic
factors, and access to care. Given the substantial cancer burden borne by
minorities and the elderly, it is apparent that other policies and initiatives
will be required to ensure broad access to trials and broad applicability
of their results.
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