Winning hearts & minds: prostate cancer outreach and clinical trial enrollment in minority men

Introduction

Federal mandates exist to ensure the inclusion of women and minorities in federally funded research. Perhaps just as important, NIH funding can be restricted if a study does not have a plan to enroll sufficient numbers of women and minorities, when appropriate. Despite this, Black, Indigenous, and People of Color (BIPOC) continue to participate less frequently than White people in a variety of research settings (1-3). Limited enrollment of these groups in clinical trials limits generalizability of results and may even lead to ineffective or harmful treatment in minority groups. Although there exist numerous factors contributing to lower levels of participation in BIPOC, such as sociocultural factors, limited access to healthcare services, and lower levels of health literacy, the mistrust of academic and research institutions is the most significant reported barrier (4-7). Historical maltreatment of BIPOC communities stemming from institutional and historical racism has contributed, at least in part, to a pervasive culture of mistrust in scientific and healthcare institutions (8).

Historical context

The Tuskegee syphilis study is a historical example widely recognized as a source of mistrust in scientific institutions. This study was an observational study of 400 sharecroppers with untreated syphilis conducted to document the natural course of the disease in Black patients. Participants were not informed that they had syphilis, were not given treatment, and were not given counseling to avoid spread of the communicable disease. The study lasted from 1932 to 1972 and was conducted by the United States (U.S.) Public Health Service (9). Both the extent and duration of the mistreatment and deception of those enrolled is unparalleled in modern medical history, and resulted in nationalized changes to the review and approval process of human subjects’ research (10).

Despite these advances, more recent studies have taken place which have further sewed mistrust in the Black community. In the 1990s, the Department of Energy sponsored studies to determine the human body’s resistance to radiation. In one study, patients with late-stage cancer were exposed to high doses of full-body radiation. The patients were informed that this was a final effort to stop continued metastatic spread of their cancer. Further, no informed consents of the research participants were obtained in this study (11).

These notable examples, amongst others, have directly contributed to significant mistrust by the Black community in scientific institutions, which continues to hinder enrollment into contemporary research studies.

Mistrust of research and academic institutions by Black communities is further complicated by other co-related societal issues. Within healthcare, patients may report feelings of neglect and commonly cite a lack of knowledge regarding etiology and pathology unique to their ethnicity (12). Direct or indirect experiences of disregard for cultural norms among health care workers may lead to overall mistrust of the healthcare system. Other concerns voiced within Black communities include the perception of lack of choice over treatment in clinical trials, a lack of social support (as family or community members may mistrust institutions), and a paucity of understanding of the research process (13-15).

Similar to the Black community, American Indians have also faced historical challenges regarding research, which was often conducted by outsiders who were culturally unaware of the groups that they worked with. This issue is compounded by conflict, forced migration, and genocide that Indian American tribes faced over the past several centuries. As a result, research was often exploitative and perceived by those enrolled in the studies as ignorant of the beliefs or wishes of American Indians (16). For example, research on syphilis in the 1980s within one tribe resulted in ostracization of both adults and children as scientific articles failed to mask the community members’ identities sufficiently (17). Similarly, researchers have disregarded privacy requests by the Navajo Nation to not list sites associated with the hantavirus pulmonary syndrome (18). Numerous other examples exist, further contributing to mistrust and lack of inclination to enroll in clinical trials. Further compounding this issue, many American Indians sense that researchers treat their ethnicity as a monolith, where many cultural and genetic differences exist between geographically disparate tribes. Many non-Indian researchers and investigators tend to lump together vastly different groups under the umbrella term Indian (16). This ignores the large impact that culture, religion, language, geography, genetics and genomics may impart on a group’s view and understanding of clinical research.

In addition to Black and Indian Americans, other groups also are significantly under-enrolled in clinical trials. This is especially true for Latinos, who are the largest minority group in the U.S., currently representing approximately 15% of the population. Despite their large population, they comprise only 2–3% of enrollees in oncologic clinical trials (2,19). Compared to their Black counterparts, Latinos shared similar concerns of mistrust, such as fear of experimentation. However, they overall have fewer concerns regarding racism in healthcare. Instead, mistrust focuses on fear of deportation (for those that are undocumented) if they participate in research, lack of accessible information, and language barriers (20). However, it is important to note that research on barriers to access and inclusion of Latinos within clinical studies is limited due to many studies including Latinos within other groups (mixed ethnicity, other ethnicity) or being focused primarily on Mexican-Americans.

Any population, racial or otherwise, is capable of internalizing stereotypes. Minority populations are also capable of internalizing racial stereotypes about their own abilities, which can negatively impact health practices, outcomes, and even participation in clinical research. This phenomenon is partially related to adverse effects on the patient-physician relationship, resulting in communication delays with the patient, discounting of information from the physician, and/or lower levels of adherence (21,22). These same stereotypes can also shape how healthcare or scientific organizations interact with members of minority communities. For example, in the case of Black women, a variety of societal stereotypes (strong mother, welfare mother, etc.) can influence treatment and enrollment opportunities (23,24). Strong patient-physician relationships are vital for participation in research, regardless of race/ethnicity, and thus internalized racism on the part of both patient and physician may result in additional barriers to enrollment (19,25).

Current rates of clinical trial enrollment in minority and underserved communities

Studies that lack large segments of the general population are not generalizable, by nature. Without inclusivity, the healthcare system cannot hope to deliver on targeted therapies, especially for diseases that are prevalent among many sub-populations. Given that research has historically been conducted by White researchers on White research participants, the “gold standards” for research processes have been transferred to minority groups with incorrect assumptions of efficacy (8). Furthermore, medicine is moving towards individualizing treatment approaches. There is a growing field of pharmacogenomics that studies how genetic factors contribute to drug effectiveness and toxicity, which is influenced by racial and ethnic diversity (2). This issue of lack of diversity within clinical studies was first raised in the early 1990s, and the National Institutes of Health (NIH) enacted the Revitalization Act in 1993, which encouraged the inclusion of women and ethnic minority groups in NIH-sponsored research (26). Since then, the evaluation of appropriate representation for women and minorities is part of the NIH peer-review process for research studies, where applicable (2).

Discouragingly, in the three decades since the Revitalization Act, the proportion of minorities participating in cancer clinical trials to the population of minorities in the U.S. remains persistently low (26). Additionally, minorities are paradoxically under-represented in cancer clinical trials while being disproportionately burdened by cancer (26). When focusing on the first decade after the Revitalization Act, there were over 75,000 participants in National Cancer Institute (NCI) sponsored trials for breast, lung, colorectal, and prostate cancer (2). Of those participants, only 14.4% comprised all minorities combined (although evenly distributed between men and women) (2). When divided by subgroup, 9.2% were Black, 3.1% were Hispanic, 1.9% were Asian Pacific Islander, and 0.3% were American Indian (2). Additionally, the percentages of minority participants decreased from 1996 to 2002 while the yearly number of participants increased (2). When examining NCI-sponsored or co-sponsored clinical trials from 1993 to 2013, less than 2% of trials primarily or specifically focused on racial or ethnic minorities (26). In the 30 years since being enacted, it is difficult to give a passing grade to the Revitalization Act.

The incidence and mortality rates of prostate cancer, in particular, vary among different racial groups (27,28). When compared to White men, Black men have 60% higher incidence of prostate cancer, are more likely to be diagnosed at a younger age, have more aggressive cancer at diagnosis, are more likely to be undertreated for high-risk disease, and have more than twice the prostate cancer-specific mortality rates (27). Hispanic men are also more likely to be diagnosed with advanced stage prostate cancer and to have higher tumor grades compared to non-Hispanic White men (27). In addition, Native American men have higher mortality rates due to prostate cancer compared to White men (28). Filipinos, South Asians, and Pacific Islanders in the U.S. are all more likely to present with advanced prostate cancer compared to White men (27).

Even though there is an underrepresentation of minorities in prostate cancer trials, there are some improvements in representation given the now widely acknowledged racial disparities in prostate cancer incidence and mortality. When compared to phase II and III clinical trials for kidney and bladder/urothelial cancers in 2000–2017, all three types of cancer trials had poor minority representation, but prostate cancer trials had the highest among them (29). Similarly, while there is underrepresentation of minorities in prostate cancer trials globally, the U.S. has the highest representation of minorities when compared to Canada, Australia, and Europe (28). Within NCI-sponsored studies from 1996 to 2002, only in prostate cancer was the enrollment fraction slightly greater in Black men than White men (2). When looking at phase III prostate cancer trials from 2003 to 2014, enrollment of Black/African American men increased over time (27). Despite this progress in clinical trial inclusiveness, there is consistently an underrepresentation of Hispanic men in all phases of prostate cancer trials (2,27,29). It is also worth noting that although Asian and Native American men were underrepresented in relation to the populations in the U.S., their representation in relation to the incidences of prostate cancer were equivocal (2,27,29).

Recent studies have attempted to address the lack of diversity in prior research on prostate cancer biomarkers. The four-kallikrein (4K) panel (available commercially from Opko as the 4K score) has been demonstrated to improve detection of aggressive prostate cancer on biopsy as compared to prostate-specific antigen (PSA), alone (30). However, in a large meta-analysis of studies on the 4K panel, totaling 11,314 subjects, only 3.5% were of African descent. Furthermore, there were limited individuals from other non-White or non-Black groups (31). Lack of diversity and insufficient data, therefore, limits the generalizability of the 4K panel to non-White individuals. However, a nested case-control study on use of the 4K panel including men from Black, Latino, Japanese, Native Hawaiian, and White ancestry in the Multiethnic Cohort (MEC) was conducted. The study suggested that the 4K panel was superior to PSA in discriminating the risk of aggressive prostate cancer on biopsy across multiethnic populations. Interestingly, even though the 4K score was originally studied on primarily White subjects, it had better discriminative ability in Latino, Native Hawaiian, and Japanese men (32). Studies such as this highlight the need for inclusion of a broad diversity of individuals in biomarker validation trials.

To ameliorate the racial disparities in clinical trial participation, it is necessary to improve our understanding of the factors contributing to underrepresentation. The scientific community must acknowledge that fear and/or mistrust of the medical and scientific communities is a barrier to minority participation in clinical studies (8,33). Additionally, the reasoning for mistrust may be different for each community (8). For example, the mistrust for Black Americans may stem from the history of racism and cite specific studies, such as Tuskegee, while the mistrust for Native Hawaiians may stem from the historical experiences of colonialism (8).

Interestingly, accounting for the common barrier of fear and/or mistrust, there have been studies suggesting an insignificant difference in the willingness to participate in clinical trials among different races (8).

Regarding prostate cancer, specifically, surveys reveal a willingness among White, Latino, African American, and Asian American men to participate (34). Given these results, there are perhaps other factors contributing to the racial disparity of clinical trial participation. Other common barriers of participation in clinical trials include study feasibility, lack of awareness of and information about clinical trials, and lack of social or community support (8,33). Similar to mistrust, these other barriers to participation may vary among different racial groups. For example, in one study, lack of social support, specifically family support, was a significant barrier for Asian Americans (8). These are broad characteristics of barriers to participation for minorities, and understanding the nuances of these barriers may help improve minority recruitment in clinical trials.

Given the known racial disparities in cancers, the large Prostate, Lung, Colorectal, and Ovarian multicenter randomized trial was conducted to evaluate the effectiveness of organized vs. opportunistic prostate cancer screening, and post-hoc analyses were conducted to evaluate the recruitment and screening effectiveness of Black and Hispanic individuals in this trial (35). Despite the emphasis on, and increased efforts to recruit ethnic minorities for this trial, the minority enrollment levels were comparable to other cancer screening or prevention trials with continued underrepresentation of Black and Hispanic individuals (35). In this study, the researchers made a concerted effort to address cultural and linguistic factors as well as financial factors but did not change recruitment of minority individuals (35).

In the Prostate Cancer Prevention Trial, which investigated the effectiveness of finasteride in preventing prostate cancer in at-risk men, researchers encountered difficulties recruiting African American and Hispanic participants. Their recruitment focused specifically on community education and disseminating information about the study to disparate racial and ethnic groups. Despite these efforts, there was no increase in enrollment or randomization of minorities into the study (36).

Similarly, studies have been conducted to assist in the decision-making process for prostate cancer treatment. Historically, decision support interventions were primarily used for White men and were associated with improved knowledge about prostate cancer, decreased decision conflict, and increased patient involvement in decision making (37). With the understanding that Black and other minority men have not been targeted for such decision aids, a randomized control trial was conducted where Black and other minority men were the focus of tailored telephone education for prostate cancer testing (37). The results were promising, as the intervention group demonstrated greater knowledge, lower decision conflict, and a higher likelihood of discussing prostate cancer testing than the control group after intervention (37). In a multicenter randomized control trial, treatment decision aids were used to educate men with localized prostate cancer (38). There was a focus on oversampling minority men with a primary outcome of prostate cancer knowledge (38). While the study showed no improvement in knowledge with decision aids, the study helps advance the understanding of what may better assist minorities in prostate cancer decision making while endeavoring to bridge the racial disparities in prostate cancer (38). Despite the disparate rates of adverse prostate cancer metrics in Black men, clinical trials on prostate cancer have predominately enrolled White men. Racial disparities continue to persist in clinical trials, which limits their generalizability. As a result, clinicians may continue to rely on incomplete or inadequate guidelines for minority patients.

Efforts are continuously endeavoring to increase minority recruitment in the research community. To date, however, there are still a paucity of trials designed specifically to stratify results based on race, or conducting trials specifically focusing on the intersectionality of race. Until there is an improved understanding of the barriers to recruitment of minorities in clinical trials, and concerted efforts to address these hurdles, there will likely continue to be racial disparities in clinical trials.

Future directions

Academic and healthcare institutions cannot sit idly by, hoping for change to occur. Rather, they must pursue it. Further, there are few nations as well poised to progress medical literature in this domain, given the population diversity, research infrastructure, and resources of the U.S. Despite past exploitation, work is being done to regain the trust of underserved and vulnerable communities to ensure equal access to clinical trials and narrow disparate accrual rates.

As previously discussed, various minority communities have different views on research and are historically skeptical of participation. The Black community remains influenced by the previous harms of the Tuskegee study (39,40) but there are other reasons for research participation apprehension, such as questions regarding research integrity (5,10,39,41-44), perceived racism by researchers (45), and overall lack of trust in the healthcare system (43). Conversely and unexpectedly, Asians cite family involvement in decision-making as a barrier to participation in clinical trials, as the informed consent and decision-making process typically only focuses on the individual subject and does not make a concerted effort to involve the family (46). As a barrier to participation in clinical trials, Pacific Islanders have reported concerns about overgeneralization of their community (47).

To facilitate equal access and ensure the appropriate participation of minorities in genitourinary clinical trials, various interventions have been employed, depending on the community. For example, in the Black community, successes have been achieved with additional safety assurances or compensation (41,44,48,49), interacting with research team members from the Black community (41,43), and observing the accrual of diverse communities into the trial alongside them (39). Additional safety assurances including the use of a digital video disk (DVD) explaining research protections and the informed consent process to Black patients increased their willingness to participate in a hypothetical clinical trial from 27% to 43% (49). In addition to using the aforementioned techniques, it has been reported that physically locating clinical research offices within underserved Washington, DC communities yielded a 62% increase in minority enrollment in nontherapeutic cancer clinical trials over 3 years (50). In Asian American families, consenting and recruiting patients as a family unit to participate in clinical trials has yielded improved participation (51-53). Amongst Pacific Islanders, community input on how findings are used and reported as well as updating the families of participants of trial progress has facilitated participation in clinical trials (47). Despite the promise of various interventions from compensation to increased dialogue prior to enrollment, the greatest barrier to enrollment remains eligibility as described in a multi-institutional randomized clinical trial in men with prostate cancer who had the potential to become eligible for therapeutic prostate cancer clinical trials (54).

Beyond minority communities, work has been done to provide additional protection to historically exploited populations, such as prisoners. The Department of Health and Human Services releases regulations and guidelines on additional research protections for research involving prisoners. States and institutions also typically require more extensive approval processes to conduct research on prisoners.

Our review is not without limitations. One limitation is the relatively lower number of studies on Latino, Asian, and Native American men. Additionally, increasing participation of specific racial subgroups is not well described within the literature. Despite these limitations, our review presents a wide range of both primary and secondary sources. Further, the most well-developed literature on recruitment of minority men for clinical trials available for inclusion is on Black men, the most disproportionately affected by prostate cancer, the subject of this review.

Conclusions

Finally, although the literature on increasing participation in clinical trials by the Black population is maturing, there is a need for further work on increasing trial participation amongst Latinos, Asians, and Pacific Islanders. Further, there is a need for research into subgroups within and across all racial groups as race remains a very broad categorization of many diverse individuals.

Acknowledgments

Funding: None.

Footnote

Peer Review File: Available at https://tcr.amegroups.com/article/view/10.21037/tcr-24-868/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tcr.amegroups.com/article/view/10.21037/tcr-24-868/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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