Increasing Racial Diversity in Cancer Research and Cancer Care Donita C

Published OnlineFirst August 18, 2020; DOI: 10.1158/2159-8290.CD-20-1193

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sCienCe in soCieTy The Race toward Equity: Increasing Racial Diversity in Cancer Research and Cancer Care Donita C. Brady 1 ,2 and Ashani T. Weeraratna 3 ,4 summary: Cancer research and cancer care require deliberate attention to racial diversity. Here we comment on the ongoing issues of diversity and racism in cancer research.

inTroduCTion Transformative, intentional initiatives at our institutions and funding agencies aimed at the retention and recruitment The horrifi c murders of George Floyd, Breonna Taylor, of Black trainees and professors within the cancer research and countless others have had a profound effect on the col- enterprise are therefore critical to creating preeminent aca- lective conscience of our society, prompting us to reexamine demic research environments (1 ). Furthermore, many cancers our own bias and survey for race-based discrimination to such as breast, lung, and prostate cancers disproportionately begin to acknowledge and combat the existing racism within affect people of color, and those health disparities need to our own ivory towers. This introspection has opened the be addressed. To do this, community outreach is critical to eyes of many to the overt and implicit biases Black scien- increase screening and encourage participation in clinical tists face. Essential discussions stemming from this new trials and laboratory-based studies. However, that cannot be awakening have been uncomfortable and eye-opening, and done without building trust between underrepresented com- have resulted in many important conversations on social munities and the medical institutions that have historically media and in person on our campuses. Although people betrayed them. Here, we attempt to succinctly identify these of color face similar micro- and macroaggressions, most challenges for cancer research and care, consider solutions have not been harassed as they came to and from campus to begin effecting actual change in academia, and provide like our Black colleagues, especially many of the men, or antiracism resources. Cancer research and cancer care require feared navigating their own neighborhoods or sleeping in deliberate attention to racial diversity. their own homes. Respected leaders in our cancer research fi eld such as Robert Winn, Cancer Center Director at Vir- ginia Commonwealth University, or Otis Brawley, former Challenges, proBlems, and issues Chief Medical and Scientifi c Offi cer and Executive Vice WiThin The BlaCk CanCer researCh President for the American Cancer Society and currently a Bloomberg Distinguished Professor and Associate Direc- CommuniTy tor for Community Outreach at the Johns Hopkins Kim- The fi rst and overriding problem, not just in cancer research mel Comprehensive Cancer Center, have recently described but in all biomedical research, is the vast underrepresentation being held at gunpoint while walking to their cars, or in of minorities. The NIH defi nes underrepresented minorities front of their own homes (https://cancerletter.com/articles/ (URM) very specifi cally as “US citizens or lawful permanent 20200605_1/). This ever-present reality permeates the minds residents who are African American/Black, Hispanic/Latinx, and informs the actions of our Black colleagues, and, as a American Indian, and Alaskan Native.” Although many insti- result, sets them on a different footing from the start no tutions have focused on increasing the input into the pipe- matter their socioeconomic status or level of education. line, beginning with efforts as early as middle school, the real problem comes at that transition from training to career. Gibbs and colleagues (2, 3) have shown that the number of URM receiving PhDs between 1980 and 2013 increased 1 Department of Cancer Biology, Perelman School of Medicine, University by a factor of 9.3, as compared with a 2.6-factor increase in of Pennsylvania, Philadelphia, Pennsylvania. 2 Abramson Family Cancer Research Institute, Perelman School of Medicine, University of Penn- non-URM groups. Despite this, there was no similar increase sylvania, Philadelphia, Pennsylvania. 3Department of Biochemistry and in the number of URM faculty recruited into assistant pro- Molecular Biology, The Johns Hopkins Bloomberg School of Public Health, fessor positions, whereas non-URM scientists transitioned 4 Baltimore, Maryland. The Johns Hopkins Kimmel Cancer Center, Balti- into faculty positions at rates refl ective of their entry into more, Maryland. academia. Using a model that took all of these factors into Corresponding Authors: Ashani T. Weeraratna, Johns Hopkins Bloomberg account, the authors came to the depressing conclusion that School of Public Health, 615 N. Wolfe Street, Baltimore, MD 21205. Phone: 410-955-3655; E-mail: [email protected] ; and Donita C. Brady, Perel- with no intervention, and even in the face of exponential man School of Medicine, University of Pennsylvania, 612 BRBII/III, Phila- growth in the URM student population, faculty diversity delphia, PA 19106. E-mail: [email protected] would remain static well into the next 50 years. These models Cancer Discov 2020;10:1451–4 highlight the problem with focusing large amounts of effort doi: 10.1158/2159-8290.CD-20-1193 on increasing the pipeline without similar efforts to increase ©2020 American Association for Cancer Research. retention. Diversity, equity, and inclusion (DEI) efforts have

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Table 1. Antiracism resources

Resource Links Websites consolidating incredible resources organized https://www.projecthome.org/anti-racism-resources by subject, from self-care, to discussing racism with https://diversity.unc.edu/yourvoicematters/anti-racism-resources/ children, to active antiracism guides https://www.forbes.com/sites/juliawuench/2020/06/02/fi rst-listen-then- learn-anti-racism-resources-for-white-people/ https://drive.google.com/fi le/d/1AoFbaCEfP5qgBMjKnpsnzx5idYPdbq6x/view Antiracist movies and TV shows https://www.glamour.com/story/anti-racist-movies-tv-shows-streaming https://www.harpersbazaar.com/culture/fi lm-tv/g32961462/black-history- movies-anti-racism/ https://time.com/5847912/movies-to-watch-about-racism-protests/ Podcasts https://www.wbur.org/artery/2020/06/05/podcasts-to-listen-to-about-race- america https://www.glamour.com/story/anti-racist-podcasts-and-talks https://bellocollective.com/16-podcasts-that-confront-racism-in-america- f8f69baf529d long been focused on students, and not only are URM “Target of Opportunity” programs should be made avail- faculty not included as targets of these efforts, they are asked able. Faculty searches should include a committee member to lead them, resulting in an increased workload that often dedicated to increasing URM applications through outreach goes uncompensated. Finally, URM faculty are also sub- and solicitation. Universities should keep on hand a list of jected to a lot of bias, both conscious and unconscious. As their talented minority alumni, tracking them through their with all academics who are URM, be they Black, Indigenous, graduate training and helping to promote them as faculty or immigrant, there are multiple micro- and macroaggres- candidates. All of these are easy initiatives that can help to sions that plague us. For an eye-opening list of these, search increase URM faculty hires. From there, efforts to increase under the hashtag #BlackInTheIvory or explore the Twitter the retention of these candidates need to be made. Above all account of the same name. This “death by a thousand cuts” these is the training of non-URM faculty in what implicit or is a recipe for ensuring an absence of URM populations in unconscious bias is and how to recognize and mitigate it in academia. dealings with fellow faculty and with trainees. As with everything, however, it is critical to note that although training What Can Be Done to Increase Diversity and discussion work, the effects are not self-sustaining, and in Academia? institutions will need to commit to gauging the effectiveness First and foremost, it is critical to maintain investment of the implicit bias training with clear metrics, continued into the pipeline. Bringing URM students into the pipeline implicit bias training as the research evolves, and systems for early and fi nding ways to effectively retain them through accountability, among other initiatives. Diversity initiatives their medical or scientifi c training is critical to creating should be rewarded rather than viewed as distractions, and and increasing the pool of candidates from which to draw leadership in cancer centers can do this by including DEI at later stages. Beyond the increases in the pipeline, more efforts as “credits” toward promotion and remunerating effective partnerships between minority-serving institutions them where appropriate. Requiring statements of commit- and cancer centers could provide increased opportunities for ment to these activities at different stages of promotion recruitment and knowledge exchange. Programs should be is also one way to increase the incentive to partake in DEI established for our URM students that address transition- efforts. The goal is to include non-URM faculty in these ing to graduate school (in the form of “boot camps” prior initiatives as well, and to provide them with resources on to their matriculation), provide check-ins throughout their combating racism and on impactful responses to criticisms training with dedicated, effective mentoring circles that go of antiracism programs (e.g., those listed in Table 1 ). Further beyond professional development, and create safe spaces resources, supporting data, and actions are also beautifully within our communities, such as an “Offi ce of Diverse outlined in a 2015 article by Whittaker and colleagues (4 ) Research Training.” For the promising URM postdocs at that we strongly recommend reading. our institutions who aspire to faculty track, “Pathway to In addition to institutions and cancer centers taking a Professorship” programs that include tailored mentoring, stand, funding agencies can do the same. Although organiza- lab incubator space, and fi nancial support should be devel- tions such as the American Association for Cancer Research oped. Akin to the successful NIH Stadtman Tenure-Track (AACR), the American Society of Clinical Oncology (ASCO), Investigators, institutions and cancer centers should initiate and the American Cancer Society fund travel fellowships and recruitment symposia that provide an opportunity for can- trainee grants for URM scholars, we need to increase funding cer research–focused URM postdocs to be exposed to them. avenues for cancer research for URM as well. For example, Targeted funds for the recruitment of URM faculty such as fi ve years ago The V Foundation established the Stuart Scott

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Memorial Cancer Research Fund to provide financial sup- figures-for-african-americans.html). Community outreach port for cancer research conducted by URM faculty as well as efforts to increase screening in URM populations face the research that is dedicated to the aggressiveness, therapeutic challenge of mistrust. In addition to this mistrust, the lack responsiveness, and ultimate outcomes for Black and other of education and resources in underserved communities minority population patients with cancer. In 2011, a seminal also leads to reduced screening and to long waits before study by Ginther and colleagues indicated that URM scien- finally seeing a physician. It is also no secret that the com- tists receive grant funding at lower rates than their non-URM plaints of URM patients, specifically Black women, often fall peers (5). To address this, the NIH instituted a Scientific on unsympathetic ears (https://www.oprahmag.com/life/ Workforce Diversity Taskforce in 2014 (https://diversity.nih. health/a23100351/racial-bias-in-healthcare-black-women/). gov/building-evidence/racial-disparities-nih-funding). Amaz- Even palliative care for oncology patients is inequitable: ingly, in that short time the gap in grant funding, especially at fewer URM patients are referred to palliative care, and those the R01 equivalent level, decreased significantly, although not who are have inferior experiences (9). All these issues can be totally, and represented an 117% increase in awards granted further compounded by the chronic stress URM popula- to Black scientists. Intentional diversity programs such as tions experience due to less favorable socioeconomic status Build and the National Research Mentoring Network that and simply trying to survive in a culture that does not equipped trainees with grant-writing tools, paired them with favor them. Furthermore, many of our cancer centers find mentors with similar life experiences and academic interests, themselves at the heart of predominantly minority cities; and taught students about implicit biases they may face, thus, it is imperative to be creative about investing in those have significantly contributed to this success. Other such communities. programs, including the Research Training Opportunities for Outstanding Leaders (ReTOOL) program, have shown simi- What Can Be Done to Increase Equity in Clinical lar success. This program was designed to increase the capac- Cancer Care and Research? ity for scientific research in underserved areas and to increase First and foremost, we need to increase the number of URM representation in biomedical research. Between 2012 URM physicians in the cancer field. Of all medical disciplines, and 2019, 40 URM scientists were identified and followed, hematology and oncology are well behind other fields in and ReTOOL drove both the initial interest and ultimate their makeup of URM doctors. When compared to the US retention of these URMs in science (6). With these types of population, where 13% of the population is Black and 18% initiatives showing success and setting the stage, cancer cent- is Latinx, the numbers are dire: 2.3% of oncologists are Black ers nationwide have strong examples to follow. Indeed, many and 5.8% are Latinx. The numbers for Indigenous people are are rising to the challenge. even smaller. This stems from a pipeline issue, as only 11% of medical students are URM. What makes this issue even more urgent is that URM students are willing to work in under- Cancer in The Black Community: served communities and are arguably better equipped to do Addressing Healthcare Disparities so. Organizations such as the AACR and ASCO are taking important steps to increase diversity in their own leadership in Cancer Research and membership to provide crucial representation. These From the Tuskegee experiments to the exploitation of initiatives include the expansion of mentoring opportunities Henrietta Lacks, beautifully documented in the book Medi- for URM oncologists, the assessment of policies that could cal Apartheid by Harriet Washington (7), the participation of increase the diversity pipeline, and building upon ongoing Black people in clinical trials has a checkered history right- diversity initiatives, such as awards for medical students. fully rooted in fear and mistrust. As a result, less than 4% of In an effort initiated in 2011, the NCI created a program patients enrolled in clinical trials are Black and less than 4% through their Community Networks Program Centers that are Latinx, and less than 10% of biobanked samples in cancer provided community-based training to prepare students and clinical trials come from URM patients (8). The numbers early-stage investigators and physicians for careers in oncol- for American Indians are so low that they are hard to even ogy. Specifically, participants in the program were trained factor into these statistics. In the words of The Cancer Atlas in disparities research and strategies for reduction of cancer (https://canceratlas.cancer.org/the-burden/indigenous-pop health disparities. This remains a critical point for all physi- ulations), “Data related to cancer in these populations tend cians—once in training, oncologists need to undergo bias to be absent or of poor quality making many Indigenous training so that they can create a productive environment for peoples statistically invisible, with the majority of data that URM students and doctors. An important part of this train- exist coming from a few high-income countries.” This is a ing also needs to extend to the patients and focus on how to huge issue, affecting everything from understanding and treat patients with respect and a lack of racial bias, however appreciating the impact of environmental and comorbidity implicit it may be. biases on cancer progression to appreciating the impact of Next, we need to improve the representation of URM data input from racially biased studies into newer technolo- patients in clinical trials. The Cancer Disparities Research gies such as artificial intelligence. The import of this issue Network, for example, undertook an evaluation of biobanks is compounded by the fact that some cancers such as breast among ten representative facilities. They found that only 10% and prostate cancers disproportionately affect URM popula- of samples came from non-White patients, and only a handful tions, in whom the disease is far more aggressive (https:// of centers targeted URM populations, citing a lack of funding www.cancer.org/research/cancer-facts-statistics/cancer-facts- and other resources with which to pursue these initiatives.

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Increasing funding so that different centers can participate in Disclosure of Potential Conflicts of Interest these initiatives will be an important step. However, perhaps D.C. Brady reports funding from Merlon, Inc. (co-owner) outside the most important step for improving cancer care for URM the submitted work. A.T. Weeraratna is on the scientific advisory board patients is rebuilding trust with the hospitals. Some centers are of Healthe Lighting Sciences and has received grants from Melanoma taking innovative approaches to this, pairing with the NAACP, Research Foundation (scientific advisory board) outside the submitted for example, to learn how to better reach out to underserved work. No other potential conflicts of interest were disclosed. communities. Some have instituted community outreach programs as critical steps toward tenure and promotion to better Published first August 18, 2020. engage their physicians and overcome historically adverse rela- tionships. Strategic partnerships with key community leaders are also an important avenue for increasing screening in URM References patients and their participation in clinical trials. 1. AlShebli BK, Rahwan T, Woon WL. The preeminence of ethnic diversity in scientific collaboration. Nat Commun 2018;9:5163. 2. Gibbs KD, Basson J, Xierali IM, Broniatowski DA. Decoupling of the Conclusion minority PhD talent pool and assistant professor hiring in medical Let us end with this call to action. It is no longer enough school basic science departments in the US. Elife 2016;5:e21393. not to be racist—it is time to all come to the table and be 3. Gibbs KD Jr, McGready J, Bennett JC, Griffin K. Biomedical science Ph.D. career interest patterns by race/ethnicity and gender. PLoS One actively antiracist. What does that mean? It means not being 2014;9:e114736. a silent ally, and it means standing up for someone who 4. Whittaker JA, Montgomery BL, Martinez Acosta VG. Retention of is being treated badly. It means being a “disruptor,” in the underrepresented minority faculty: strategic initiatives for institu- words of Dr. Russell J. Ledet, or making “good trouble,” in tional value proposition based on perspectives from a range of aca- the words of the deeply mourned, recently departed Rep. John demic institutions. J Undergrad Neurosci Educ 2015;13:A136–45. Lewis. It means going out of your way to invite, amplify, cele- 5. Ginther DK, Schaffer WT, Schnell J, Masimore B, Liu F, Haak LL, et al. Race, ethnicity, and NIH research awards, Science 2011;333:1015–9. brate, and support your URM colleagues. It means approach- 6. Odedina FT, Behar-Horenstein LS, Fathi P, Kaninjing E, Nguyen J, ing your URM patients with respect and really listening to Askins N, et al. Improving representation of underrepresented minority their complaints. As a community, we need to increase URM (URM) students in oncology biomedical research workforce: outcome representation at all levels of faculty and leadership. We need evaluation from the ReTOOL Program. J Cancer Educ 2020;577–83. to appreciate and embrace the diversity that can bring impor- 7. Washington H. Medical apartheid. New York, NY: Doubleday; 2007. tant insights into everything from basic cancer research to the 8. Simon MA, de la Riva EE, Bergan R, Norbeck C, McKoy JM, Kulesza clinical practice of oncology. We provide a list of antiracism P, et al. Improving diversity in cancer research trials: the story of the Cancer Disparities Research Network. J Cancer Educ 2014;29:366–74. resources in Table 1, and we look forward to working with 9. Busolo D, Woodgate R. Palliative care experiences of adult cancer our colleagues to foster a more inclusive environment for our patients from ethnocultural groups: a qualitative systematic review students, our faculty, and our patients. protocol. JBI Database System Rev Implement Rep 2015;13:99–111.

1454 | CANCER DISCOVERY October 2020 AACRJournals.org

The Race toward Equity: Increasing Racial Diversity in Cancer Research and Cancer Care

Donita C. Brady and Ashani T. Weeraratna

Cancer Discov 2020;10:1451-1454. Published OnlineFirst August 18, 2020.

Updated version Access the most recent version of this article at: doi:10.1158/2159-8290.CD-20-1193

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