A call to action: Antiracist patient engagement in adolescent and young adult oncology research and advocacy

Abstract

Amidst the concurrent global crises of coronavirus disease 2019 (COVID-19), uprisings against Anti-Black racism and police brutality, as well as anti-Asian racism and violence, the field of medicine found itself simultaneously called upon to respond as essential workers in the public health devastation of COVID-19, and as representatives of healthcare institutions wrought with the impacts of systemic racism. Clinicians, researchers, and advocates in adolescent and young adult (AYA) oncology, must come together in authentic activism to begin the work of creating structural change to advance antiracist approaches to patient engagement in AYA oncology research and advocacy. Critical review of existing practices is needed to ensure that ethical and effective research methods are employed when engaging with racial and ethnic minority AYA patients with cancer, who may be particularly vulnerable and exploited in the current context.

On the evening of Monday, 25 May 2020, amidst a surging coronavirus disease 2019 (COVID-19) pandemic, George Floyd, an unarmed 46-year-old black man, was murdered. Mr Floyd was murdered by police, while in their custody for allegedly attempting to use a counterfeit US$20 bill to purchase a pack of cigarettes. The viral video of the murder prompted mass protests and uprisings worldwide. Across every industry sector, organizations declared that Black Lives Matter in their respective missions.

These concurrent global crises exposed long-standing power structures that have benefitted white citizens, while imposing a greater burden of disease, mortality, and psychosocial harm on racial/ethnic minorities. Racial consciousness among non-black people was raised to such a compelling level that predominantly white institutions responded to the negative impacts of persistent racism and health disparities suffered by our black citizens. Following Mr Floyd's murder, heightened global interest in the problem of racism and police brutality retrospectively amplified other recent murders of unarmed African–Americans. On a Sunday afternoon, 3 months earlier (23 February 2020), Ahmaud Arbery, a 25-year-old black man, was jogging in a residential neighborhood when he was fatally gunned down by two white vigilantes who racially profiled and pursued him. In the dead of night on Friday,13 March 2020, 2 months prior to Mr Floyd's murder, Breonna Taylor, a 26-year-old black healthcare worker, was murdered in her own home during a police raid by two white plainclothed officers.

As the COVID-19 outbreak drastically altered our social world, vast misinformation fueled public fears, xenophobia, and a sharp increase in violence and racism against Asian people and their communities across the globe. According to the Center for the Study of Hate Crime and Extremism, anti-Asian hate crimes in the United States' major cities increased by 145% between 2019 and 2020, despite an overall decrease of 6% for the general population [1]. Meanwhile, the Stop AAPI (Asian American and Pacific Islander) Hate reporting center received 3,795 reports of anti-Asian incidents during the one-year period from March 19, 2020 to 28 February 2021, noting that these data represent only a fraction of the actual number of anti-Asian incidents [2]. In the early evening of Tuesday, 16 March 2021, against this backdrop of increasing anti-Asian sentiment over the preceding year, a series of related mass shootings occurred at three spas in Atlanta (GA, USA). A white gunman killed eight people, six of whom were Asian women: Soon Chung Park, Hyun Jung Grant, Sun Cha Kim, Yong Ae Yue, Delaina Ashley Yaun, Paul Andre Michels, Xiaojie Tan and Daoyou Feng. One person was left severely wounded: Elcias Hernandez-Ortiz [3].

In effect, practitioners in the field of medicine became active stakeholders in two simultaneous sociopolitical disasters, as front-line essential workers in the public health devastation of COVID-19, and as representatives of healthcare institutions wrought by the impacts of perpetuating a long history of systemic racism. To date, responses from the medical community have included calls to action for antiracist approaches that support greater accountability for racial and ethnic disparities in the provision of healthcare [4,5] and the conduct of healthcare research [6,7]. The authors advise healthcare institutions on how to dismantle and replace existing systems rooted in white supremacy, thereby moving beyond insufficient traditions of mere awareness and acknowledgement on issues of racial and ethnic inequity [4–7].

In 2020, there were an estimated 89,500 new incidences of cancer among adolescents and young adults (AYA) between ages 15–39 years in the USA, which is consistent with the overall increasing trend in cancer incidence for AYAs during the recent decade (2007–2016) [8,9]. Five-year survival rates for all cancer types among AYAs have seen gradual improvements since the 1970s [8]. When disaggregated, however, racial and ethnic minority AYAs have not seen these improvements, and actually experience lower five-year survival rates for all cancer types. This worsening trend is especially observed among non-Hispanic and black individuals, who comprise 75% of racial and ethnic minority AYAs [8,10,11].

Like the overall healthcare research sector, AYA oncology researchers have made slow progress on critical issues of health equity, including the lack of racial and ethnic diversity among principal investigators of NIH-funded studies [12–15], persistent gaps in knowledge about racial and ethnic minority AYA patients [16], and long-established racial and ethnic disparities in AYA health outcomes that have seen little or no improvement [16,17]. Even as they cope with the devastation of cancer, AYAs are still-developing patients, whose growth depends upon social interactions for firsthand experiences to meet their two primary developmental challenges: (1) learning to resolve intrapersonal conflicts between autonomy and dependence, and (2) establishing intimate interpersonal relationships [18–22]. As a consequence, AYAs may be particularly vulnerable to discrimination and exploitation by self-interested organizations. To genuinely advance antiracist AYA cancer care and research, our methods cannot continue to be rooted in racism and white supremacy. For example, BIPOC (Black, indigenous, or people of color) AYAs are commonly tokenized by predominantly white-led and white-serving organizations, who call upon individual BIPOC patients to serve as performative representatives of cancer disparities experienced by their racial group, regardless of whether that particular BIPOC AYA individual has actually experienced the disparities of interest. On research projects, racial and ethnic minority AYA patient advocates commonly find themselves utilized as token afterthoughts – asked to formally acknowledge support for research studies that they had no part in developing, and often, with implications they may not comprehend [23].

As clinicians, researchers, and advocates in AYA oncology, we come together to begin the work of creating structural change to improve patient engagement in the conduct of research in partnership with racial and ethnic minority AYA patient advocates. In a demonstration of authentic activism, we present this review and discussion of current practices in AYA oncology research and advocacy, and offer recommendations to advance an antiracist future for patient engagement. Critical review of existing research practices is needed to ensure that ethical and effective methods are employed when engaging with vulnerable racial and ethnic minority AYA patients.

Antiracism & engaging AYAs in the conduct of research

BIPOC patients in healthcare settings have experienced vast mistreatment in the name of research [24], from historical malicious disregard (e.g., the Tuskegee syphilis study [25]) to more recent exploitation and/or exclusion, such as disproportionately low COVID vaccine inoculation rates among Latino Americans despite their overrepresentation as essential workers during the pandemic [4]. To avoid these discriminatory practices and mitigate inherent power differentials within the research process, employing a conscious antiracist lens is critical for valid research focused on racial and ethnic minorities [26]. The antiracism scholar, Ibram X. Kendi, defines racism as a policy or idea that creates and perpetuates inequality between people of different races [27]. In contrast, antiracism is defined as a policy or idea that creates an equitable society for all races. Kendi poignantly asserts that, across American history, the heartbeat of racism has been denial, and the sound of that heartbeat is “I'm not a racist” [27]. He further explains that there is no such thing as a policy being not racist [27]. Policies are either antiracist: creating an equitable society; or racist: contributing to inequities [27]. Antiracism calls upon AYA oncology to depersonalize reactions to racism, acknowledge mistakes, and take corrective actions in a timely manner.

It is important to distinguish antiracism from liberal multiculturalism. Often, AYA oncology is given credit for antiracist action, when their efforts to promote cultural diversity and inclusion are, in fact, not expressions of antiracism, but rather liberal multiculturalism. Liberal multiculturalism suggests that the primary social justice issues between different cultural groups are a lack of recognition of positive contributions, misunderstandings, miscommunication, and prejudice of individuals as the root causes [26]. Refuting this oversimplification, antiracism prioritizes systemic injustice and other forms of societal oppression as the causes of inequities [27].

Given the dynamic nature of AYAs' evolving psychosocial context, inclusion of racial and ethnic minority AYAs in the conduct of research on their own terms is necessary, and must be approached with both antiracism and developmental appropriateness. Developmental psychologists acknowledge that the experience of discrimination related to being a racial or ethnic minority is an expanded adverse childhood experience (ACE), a psychological trauma associated with individual- and community-level stressors that AYAs are challenged to learn to cope with while they make passage from childhood to adulthood [28]. It follows that AYAs from racial and ethnic minority groups may be particularly susceptible to exploitation during periods of individual and societal upheaval, such as the current climate defined by COVID-19 and racial unrest [29].

PCORI framework for patient engagement

The Patient-Centered Outcomes Research Institute (PCORI) was authorized in 2010 under the Patient Protection and Affordable Care Act, and charged with generating scientific evidence to inform health decisions by engaging with patients, clinicians, payers, and other healthcare stakeholders in the research process [29]. The PCORI Framework for Patient Engagement is the gold standard for patient engagement in research, and organizes all activities in the research process into four domains (Figure 1) and six core principles (Table 1) [30]. Transparency-honesty-trust are presented together because they share common strategies and are dependent on one another. According to PCORI, patient engagement is defined as the involvement of patients and other stakeholders throughout the planning, conduct, and dissemination of the proposed projects. Employing an antiracist and developmentally-appropriate lens, the authors review current patient engagement practices in AYA oncology, and utilize the four domains of research according to PCORI as an organizing structure to discuss current strengths and unmet needs, while also offering recommendations to promote greater inclusion of racial and ethnic minority AYA patient perspectives.

Figure 1. . Four domains of research according to Patient-Centered Outcomes Research Institute.

Used with permission of the Patient-Centered Outcomes Research Institute. © 2015. Patient-Centered Outcomes Research Institute. All Rights Reserved.

Table 1. . Patient-Centered Outcomes Research Instituteengagement core principles and potential strategies.

Reciprocal Relationships • Include patient and stakeholder partners as key personnel • Collaboratively define clearly stated roles and inclusive decision making  Partnerships • Request reasonable time commitments and appreciate contributions • Demonstrate commitment to diversity and cultural humility Colearning • Ensure patients and other stakeholders understand the research process • Prioritize patient-centeredness and stakeholder education Transparency-Honesty-Trust • Implement open and honest communication that supports inclusive decision making • Employ transparent research processes by disseminating results to stakeholders

Reproduced with permission from [31].

Token versus genuine patient engagement

The current review is centered on a shared value for genuine (as opposed to token) engagement with AYA patient advocates across the research process to generate scientific evidence that responds to the highest-priority issues of relevance to AYAs following a diagnosis of cancer. Token engagement (or tokenism) in research efforts is defined as the practice of making perfunctory or symbolic efforts to include patients simply for the sake of appearance (e.g., failing to give patients any decision-making authority while touting their involvement in publications or at conferences). In contrast, genuine engagement equips patients with real power to affect outcomes [24]. Hahn and colleagues' qualitative study (n = 50) examined conversations among key stakeholders in healthcare research (patient advocates, community clinicians, and academic researchers) in response to the question, “How do we move beyond tokenism in patient engagement?” Content analysis of participants' responses produced examples of genuine and token engagement that were subsequently categorized into three domains: (1) methods/structure of engagement, (2) intent, and (3) relationship building [24]. The authors also suggest that examples within each domain of engagement can be graded along a genuine–token continuum, with relative ratings of either more genuine or more token engagement that can in turn guide researchers interested in implementing real engagement with patients and community partners. Specifically, within the patient engagement domain of relationship building, one example of more genuine engagement to build trust and rapport is the presence of mutual benefits (Table 1), whereas more token engagement occurs when the benefit is not mutual [24].

Existing strengths in AYA patient engagement

One area where AYA patient engagement has achieved notable success is in the utilization of Internet-based social support networks and social media. Patient networks are effective mechanisms for the delivery of research outcomes while also ensuring that research-related communications, such as study recruitment flyers and informed consent language, are relevant to the stakeholders most impacted [32–34]. Within oncology, AYA patients are characterized by the greatest social media savvy compared with other patient care populations, which has made social media an effective medium for raising awareness about clinical trials among these so-called “digital natives” [34,35]. What's more, the COVID-19 pandemic has ignited rapid uptake of telemedicine among AYA oncology patients and providers, pointing to great potential for ever-expanding innovation in cancer care [35], and holding much promise for optimizing patient engagement at each stage of the research process [36].

A second area of strength in AYA patient engagement is the employment of cancer patients on research teams as embodied researchers, who hold lived experiences of the phenomena of interest while they lead its empirical investigation [37–40]. In Dei and colleagues' examination of critical issues in antiracist research methodologies, the authors emphasize the importance of embodied knowledge that can only be obtained through lived experience [26]. Embodied knowledge is defined as “personal feelings, emotional and spiritual connectedness, and a deep passion and commitment to seek knowledge and use these things to transform existing conditions as a noble cause that emanates from within the self.” Patient perspective becomes an integral part at every stage of research, and can be especially valuable when patients work in research contexts investigating cancers they have had. Following the leadership of patient-turned-scientists and survivor-scientists can also inform research questions that are especially pertinent to various facets of AYA life after a cancer diagnosis and treatment [38,39]. There is increasing evidence that elevated levels of patient engagement are associated with better adherence and health outcomes, including better clinical indicators, more healthy behaviors, greater use of women's preventive screening tests, and a decrease in medical-related financial burden [41,42]. Such patient engagement can help to better examine how factors such as health disparities and cancer care delivery options affect cancer patients' survivorship and risk of recurrence [43].

Recommendations for topic selection & research prioritization

Timing of patient engagement

Patient engagement must begin with the discussion of potential research topics and extend to the highest levels of strategic planning within health systems and academic institutions (Table 2). The preponderance of current research engages patient advocates at a point where the subject matter and direction for research has already been decided [43]. This practice introduces the patient to the research process at a point where they must apply their knowledge and experience to someone else's research priorities and agenda. This conundrum likely leads to more token use of patient advocates in the validation of research topics and priorities. The most critical area for positive change to defeat this type of tokenism in research topic selection and prioritization is to have patients involved in the strategic planning of research at the highest level in health systems and academic institutions, and in doing so, inform research priorities for grant funding at the national level [24,44]. Early and foundational engagement can transform research perspectives and significantly increase patient influence and empowerment.

Table 2. . Recommendations for antiracist patient engagement in research^†.

Topic selection and research prioritization

Extend timing of patient engagement  Patient engagement must begin with the discussion of potential research topics, and extend to the highest levels of strategic planning.

Identify racial and ethnic disparities in research area of interest  In all research, it must be incumbent on researchers to first identify if there are racial/ethnic disparities that exist in the area of study.

Increase sociodemographic diversity among AYA patient advocates  Issues of recruitment and access must be examined and addressed to improve the persistent lack of sociodemographic diversity among AYA patients who serve as advisors and who provide patient-reported input.

Proposal review: design and conduct of research

Provide education and honest disclosure to AYA patient advocates  Investigators must fully educate and inform patients so they can make meaningful contributions; make honest and complete disclosure to AYAs about the costs and benefits of being a patient who engages with the oncology research process.

Prioritize responsiveness to BIPOC AYAs' developmental challenges  Racial and ethnic discrimination is an expanded ACE that researchers must consider, as it may influence what is developmentally appropriate for BIPOC AYAs.

Address between-group power dynamics  Acknowledgement and responsiveness to power differentials between and within sociodemographic groups must be incorporated to enable true partnership.

Dissemination and implementation of results

Avoid persistent tokenism of the same AYAs  AYA oncology is culpable for token use of the same patient advocates repeatedly in representation of patient perspectives in the dissemination and implementation processes.

Establish new incentives in academic research  New incentives in academia are needed to ensure that research results are disseminated to the communities who will benefit from the findings, and BIPOC-embodied researchers can be instrumental to this process.

Invest additional resources and support for hard-to-reach communities  Regardless of whether embodied researchers are employed, dissemination of study results to particularly hard-to-reach communities typically demands additional resources and support.

Evaluation

Rectify overrepresentation of sociodemographic privilege  Participation in evaluation often requires high engagement from patient advocates at a professional level that is usually not conducive to still-developing AYAs' availability and capacity.

Optimize virtual access to evaluation events  COVID-19 has demonstrated that the US healthcare system can quickly restructure itself in response to vast changes brought about by a global pandemic, which holds great promise for urgently dismantling racism, and supplanting with structures that support antiracist practices.

^†Recommendations are organized according to PCORI Framework for Patient Engagement's four domains of research.

ACE: Adverse childhood experience; AYA: Adolescent and young adult; BIPOC: Black, indigenous, or person of color.

Identification of existing racial and ethnic disparities

In all research, it is incumbent on researchers to first identify if there are racial or ethnic disparities that exist in the area of study (Table 2). These may be systemic or institutional barriers, clinical outcomes, social barriers, psychological challenges and so on, depending on what research is being undertaken. One of the very first questions in the selection of a research topic relevant to racial and ethnic minority AYA patients with cancer should be whether the research can have a positive impact on reducing health-related inequities. Research questions should be shaped by the answers to these questions from the outset [28].

Socioeconomic diversity among AYA patient advocates

Issues of recruitment and access must be examined and addressed to improve the persistent lack of socioeconomic diversity among AYA patients who serve as advisors and provide patient-reported input (Table 2). The majority of patient advocates who advise on research studies tend to be white, higher socioeconomic status, well educated, and well connected to supportive care [26]. Consequently, AYAs are commonly described as a monolithic body, despite encompassing a wide range of chronological ages, developmental stages, and life experiences. Patient advocates engaged with the research process are often a reflection of those who have participated in clinical trial studies, and data shows that the preponderance of AYA enrollees in oncology cooperative group clinical trials are male and white [45]. Per the National Cancer Institute's (NCI) SWOG (formerly the Southwest Oncology Group) Cancer Research Network's experience from 1993 to 2017, SWOG AYA patients were less female (44.7% vs 48.8%, p <0.0001), Black (10.4% vs 11.8%, p = 0.0001), and Hispanic (8.0% vs 12.4%, p < 0.0001) than AYA patients in the United States cancer population [46]. Thus, there is under-representation of BIPOC in both the available data and in the representation of advocates who participate in guiding research agendas.

Recommendations for proposal review: design & conduct of research

Education & honest disclosure to AYA patient advocates

To truly engage racial and ethnic minority AYA patients in designing and conducting research, investigators must be sure to fully educate and inform patients so they can make meaningful contributions (Table 2). Much research in both scientific and health services is clouded by the language and mystique of the specialist area [47,48]. Researchers may have had a lifetime of education and engagement in their chosen research area. To create true equality in patient engagement, these still-developing patients must come to fully understand the purpose, design, and conduct of the research [24,49]. If the investigators make independent decisions on study procedures, and subsequently convene the community advisory group to simply approve what is already decided, then genuine patient engagement has not been achieved.

Furthermore, honest and complete disclosure to AYAs about the costs and benefits of being a patient with cancer who engages with the oncology research process is necessary (Table 2). There is too much conversation about resiliency and grit and not enough about the physical and emotional costs of patient advocacy work. For racial and ethnic minority AYA patients with cancer, this cost is especially notable [50]. When engaging with racial and ethnic minority AYA patient advocates, a trauma-informed approach should be part of antiracist research methods [28].

Genuine education and disclosure to AYA patient advocates means using the preferred natural language of the patient (e.g., plain English) in dialogue and written materials [51,52], giving space and time for understanding [24], and encouraging and supporting advocacy to instill confidence to challenge, question, and debate [24]. At a structural level, researchers and their teams should be expected to demonstrate genuine patient engagement to their institutions [53], and show evidence of patient satisfaction in study design and conduct [51]. Institutions and research systems must modify their own policies and practices to enable and support researchers to deliver genuine patient engagement [53]. Genuine patient engagement should be acknowledged and valued by academia, in line with publications that are the de facto currency of academic success and productivity. The process of engagement itself–establishing genuine relations with patient advocates who share the same ultimate goal to improve real-world health challenges–is as valuable as the research outcomes [51].

Responding to BIPOC AYAs' developmental challenges

Racial and ethnic discrimination is an expanded ACE that researchers must consider, as it may influence what is developmentally appropriate for BIPOC AYAs (Table 2). BIPOC AYAs are at greater risk of experiencing trauma because of societal treatment based on their status as racial or ethnic minorities, potentially resulting in unique developmental issues [28]. Expanding the body of research that is inclusive of BIPOC AYAs, and acknowledges the distinct developmental challenges of adolescence (identity formation) and young adulthood (engagement in personal and professional relationships), is essential [26,54,55]. Current programs supporting academic, career, financial, and personal needs of AYAs ensure that good medical outcomes do not come at the cost of failure in these developmental domains. When BIPOC AYAs are represented in research, and not only singled out for isolated studies, AYA oncology will be better-equipped to generate a nuanced understanding of the impact of a cancer diagnosis across the various stages of psychosocial development (identity, independence, relationships, goal setting, and self-sufficiency) that captures sociodemographic influences for the entirety of the AYA population.

Awareness & responsiveness to between-group power dynamics

Acknowledgement and responsiveness to power differentials between and within sociodemographic groups must be incorporated to enable true partnership in research (Table 2). In the current discussion around racism and the intersectionality of multiple sociodemographic identities, we are missing much-needed dialogue about what group membership means, and the power that comes with membership or nonmembership in a certain group [28,56] What that discussion is missing is recognition of power hierarchies across groups. For example, higher socioeconomic status influences one's intersectional experience of other aspects of identity, such as race and gender [56]. Similarly, there have not been enough conversations about how these groups come together, and the power differentials that may compromise a true partnership [53,56,57].

Recommendations for dissemination & implementation of results

Persistent tokenism of the same AYAs

AYA oncology is culpable for repeated token use of the same patient advocates in representation of patient perspectives in the dissemination and implementation processes (Table 2). Consequently, oncology researchers are not connecting with hard-to-reach AYAs who may be in great need of, but remain excluded from, participation in such research activities [58]. These communities are not as hard to reach as we think. We simply need to include stakeholders with meaningful ties to racial and ethnic minority communities to lead and champion–not just participate symbolically–in dissemination and implementation [24,26]. Representation of various patient perspectives helps limit the erasure, omission, and misconstruing of diverse BIPOC experiences, moving away from a Eurocentric paradigm [16].

Tokenizing the same AYAs is akin to research bias from convenience sampling, which produces results that are not representative of the entire population of interest. In this case, the bias swings toward the dominant culture and those AYAs who are well connected to the healthcare system, receiving adequate cancer care, and have their medical and psychosocial needs met. To prevent such bias, AYA oncology researchers should adopt a community-based participatory research (CBPR) approach for building authentic relations with hard-to-reach populations, as has proven successful in public health settings [59–61]. Following long-established best practices for outreach to socially disadvantaged groups, such as planning for higher resourcing and operating costs via community partnerships, is critical to securing representation from racial and ethnic minority AYAs, who are more likely to face issues of access and barriers to care [62].

New incentives in academia & BIPOC-embodied researchers

New incentives in academia are needed to ensure that research results are disseminated to the communities that will benefit from these findings, and BIPOC-embodied researchers can be instrumental to this process (Table 2). PCORI focuses on the dissemination and implementation phase so heavily because it is evident that genuine patient engagement at this stage of research is lacking [30,63]. Academic researchers are incentivized and evaluated based on research grants and peer-reviewed publications [64]. Thinking beyond that sphere into real-world contexts can be challenging. It takes time for research to get from bench to bedside, and then to community [65], and that's if it even makes it into the community. Some social scientists in AYA oncology believe their job ends with journal publication [66].

Additionally, it is problematic that the field of oncology research only considers certain types of people–those without lived experience of the research topics–to have the capacity for scientific objectivity. BIPOC researchers and patients are commonly assumed not to be objective [67]; “It's ‘me-search,’ not research.” Critics erroneously believe that their embodiment of lived experiences is synonymous with investigator bias and at odds with rigor, as BIPOC researchers choose to focus on research topics of pertinence to their own communities. But all researchers will always have their own theories–implicit or explicit–about what they are attempting to investigate, regardless of whether they have embodied experiences similar to their study participants. BIPOC embodied researchers may be uniquely equipped to pursue inquiries on topics and in ways that might not otherwise be derived. They are necessary contributors to the scientific knowledge base, who may also have exclusive access to BIPOC stakeholders and communities that directly benefit from the results of their research [37–40].

Additional resources & support for hard-to-reach communities

Regardless of whether embodied researchers are employed, dissemination of study results to particularly hard-to-reach communities typically demands additional resources and operational support (Table 2) [26]. For example, research where the outcomes suggest that some form of information and education campaign is needed to change health behaviors must ensure that these findings are presented to the appropriate community leaders and decision makers, who can respond and support further dissemination and implementation of findings. Research should not be undertaken unless there is a clear plan for sharing the study results with the relevant communities [24,26]. Publication of findings should never be the only goal of research. Publication is only dissemination within the scientific community, especially when articles are located behind cost-prohibitive paywalls; therefore, it must be accompanied by a plan to inform change where change is needed [68].

Recommendations for evaluation

Overrepresentation of sociodemographic privilege

Participation in evaluation often requires high engagement from patient advocates at a professional level that is usually not conducive to still-developing AYAs' availability and capacity (Table 2). It must almost become the patient advocate's full-time job to stay engaged with late-breaking research [43]. This can prove a burden for the average patient [53], and may be particularly burdensome for racial and ethnic minority AYAs, who might have limited resources and face additional barriers to engagement. Given these practical hurdles, patients who are engaged in advocacy tend to be of higher socioeconomic status, often retirees, who have available time and resources to withstand the structures of reimbursement for expenses such as travel [53]. Organizational structures for inclusion of patient engagement are not friendly to patients who are not part of an overwhelmingly white, select, often socially elite, and culturally dominant group [53].

Virtual access to evaluation events

COVID-19 has demonstrated that the United States healthcare system can quickly restructure itself in response to tremendous changes brought about by a global pandemic. This holds great promise for urgently dismantling racism, and supplanting with structures that support antiracist practices, if we so choose (Table 2). For example, before COVID-19 put limits on research conferences and travel, evaluation often required in-person attendance at conferences, with potentially prohibitive travel expenses and less-than-hospitable or unclear organization of group meetings. When research conferences moved to virtual platforms, patient advocates were given opportunities to participate without incurring high costs. Due to the multiplicity of potentially confounding factors, it may be difficult to determine whether increased participation in oncology meetings among racial and ethnic minority participants has been observed during the COVID-19 pandemic, and whether this increase is associated with the greater accessibility of a digital platform. The proliferation of digital technologies spurred by COVID-19 may be positive encouragement for further examination of digital dissemination and evaluation approaches aimed at improving access to presentations of late-breaking research for at least a subset of racial and ethnic minority AYA patient advocates.

PCORI's Core Principles of Patient Engagement

Across the aforementioned four domains of research activities, transparency-honesty-trust is the most salient patient engagement principle when engaging with racial and ethnic minority AYA patients with cancer. Table 1 shows PCORI's six principles of patient engagement, with transparency-honesty-trust presented in combination as principles four through six. For racial and ethnic minorities, who have historically been marginalized, lied to, experimented on, oppressed, ignored, and traumatized by healthcare systems, this principle is especially critical [50]. Transparency-honesty-trust is the only successful route from information to implementation. Without the belief that the benefit is ultimately the patient's, there can never be buy-in, especially in a population that bears skepticism as necessary armor.

As clinicians, service providers, researchers and advocates in health settings, we bring this systemic track record to our patient encounters. Healthcare institutions must create relationships where racial and ethnic minority AYA cancer patients will not (re-)experience historical discrimination or trauma [69]. In order to do that, enacting durable structural changes that enable relationships based on a solid foundation of transparency-honesty-trust is paramount (Table 1); we must start there to get to the other principles of engagement—reciprocal relationships, partnerships, and colearning [70]. Genuine, not token, engagement begins there.

One major challenge to upholding the principle of transparency-honesty-trust is the lack of BIPOC in leadership roles within research and advocacy that have the resources, available time, and power to create meaningful change. Less than 2.4% of the National Institutes of Health (NIH) grant application reviewers are Black or African American [71], and only 1.5% of R01 grant applications received by NIH are from Black or African American investigators [72]. Hoppe and colleagues' study of NIH grant application review and award trends between 2011 and 2015, found that relative to white investigators, Black or African-American investigators tend to propose research topics with low award rates, such as research at the community and population level, as opposed to more basic science-oriented and mechanistic investigations that achieve higher award rates [71]. To reverse this trend, the funding priorities of grant makers, the majority of whom are white, should be informed by the work of Black investigators and their communities, rather than vice-versa. In order for predominantly white leadership to build systems of research to ensure transparency-honesty-trust for racial and ethnic minority patients, it must be demanded by funding criteria, rather than relying on intrinsic motivation. Additionally, genuine patient engagement may require AYA oncology leaders to accept that research structures themselves might need to change and adapt to accommodate diversity [24,26,56]. Academic and institutional policies that support structural racism must be removed and/or rewritten to fix systems that perpetuate inequities among racial and ethnic minorities. For example, the R01 Transformative Research Award is the highest research grant offered by NIH. Current criteria for membership on NIH R01 proposal review committees requires that these select reviewers must themselves be a previously-funded principal investigator of an NIH R01 award. BIPOC researchers remain sharply underrepresented among NIH-funded principal investigators [12–14]. Thus, such a policy perpetuates a long history of underinvestment in projects driven by the needs and perspectives of BIPOC researchers and their communities [13].

Furthermore, AYA oncology researchers must approach patient engagement with racial and ethnic minority AYAs with openness and adaptability to ensure that trust and engagement centers on addressing patient advocates' experiences of power differences, rather than researchers' tolerance of racial and ethnic diversity [24,26]. In this authentic process, researchers must prioritize a readiness to move out of their comfort zones and away from traditions of maladaptive strategies to truly accommodate difference [56]. In order to advance antiracist transformation, researchers and their institutions must commit to continuous personal and institutional practices of unlearning, re-evaluating, and responding to implicit biases, thereby cultivating cultural humility in an environment that facilitates growth [73].

Compensation for patient advocates should be compulsory. Financial compensation for contributions to research projects is especially necessary for BIPOC AYA patient advocates, given that participation may be particularly burdensome due to their transitional life stage, high risk of financial hardship resulting from the disruption of cancer on their work lives, and often, lack of generational wealth [74,75]. PCORI provides a model for addressing fair compensation for engaged research partners that organizes patient engagement into four levels from lowest to highest contribution of effort: inform, consult, collaborate, and stakeholder directed (Table 3) [76]. According to PCORI's framework for financial compensation, corresponding levels of compensation at each level of contribution may vary. This framework can benefit from further details on the amount and process of financial compensation. For example, naming a timeframe for compensation within which patient advocates can anticipate the balance due to them and providing a validated formula (e.g., based in comparable industry standards such as market rate for similar consultation and federal per diem rates) that researchers can use to calculate a fair and equitable amount of compensation at each level of patient engagement in a given research study.

Table 3. . Sample model addressing fair compensation for engaged research partners.

Engagement activity levels		Varying compensation levels
I. Inform	Simply informing	Communicating plans to the patient community
II. Consult	Consulting on decision	Offering opinions, advice, feedback
III. Collaborate	Deciding together, acting together	Joint decisions solicited, taking actions jointly
IV. Stakeholder directed	Encouraging independent initiatives	Leading to patient/caregiver/organization-generated research

Used with permission of the Patient-Centered Outcomes Research Institute. © 2016. Patient-Centered Outcomes Research Institute. All Rights Reserved.

Conclusion

Although structural racism and white supremacy in patient engagement may be a seemingly intractable challenge, we have begun the conversation by employing an antiracist and developmentally-appropriate lens to critique current patient engagement practices in AYA oncology research and advocacy. We utilized the PCORI framework of patient engagement as an organizing structure to present our review and recommendations, aimed at advancing greater inclusivity of racial and ethnic minority AYAs and genuine approaches to patient engagement toward this goal. The PCORI principles of patient engagement ground the discussion in shared values for bolstering transparency-honesty-trust with patients across the research process.

Future perspective

The first decade-and-a-half of AYA oncology brought greater research attention and increased empirical knowledge of the lack of improvement in survival rates and constellation of unique psychosocial challenges for patients diagnosed between ages 15–39 years. In the next phase of growth for AYA oncology, we challenge the field to pursue its research questions with structural reinforcements to prevent unnecessary harm to racial and ethnic minority patients engaged in the conduct of research. We are optimistic that the interprofessional community of AYA oncology can sustain positive progress with antiracist approaches to patient engagement by working together in authentic activism to erect durable structures that encourage, support and incentivize genuine efforts.

Future research should investigate the perspectives of racial and ethnic minority AYA patients and their responses to the recommendations proposed in our current discussion among AYA oncology professionals. Such an endeavor would produce scientific evidence on antiracist patient engagement that is validated by AYAs themselves, through meaningful collaboration between researchers and key stakeholders. Authentic activism from AYA oncology professionals and greater representation of racial and ethnic minority AYA patients in the development of patient engagement strategies are essential to effectively inform genuine antiracist and developmentally-appropriate patient engagement in AYA oncology.

Executive summary.

• Amidst concurrent global crises of COVID-19, uprisings against anti-Black racism and police brutality, as well as anti-Asian racism and violence, the field of medicine found itself simultaneously called to respond as both essential workers and representatives of healthcare institutions wrestling with systemic racism.

• COVID-19 is proof-positive that massive structural changes in healthcare are possible with sufficient impetus to adapt to a crisis.

Antiracism & engaging AYAs in the conduct of research

• Antiracist patient engagement in the conduct of adolescent and young adult (AYA) oncology research requires approaches that value both antiracism and developmental appropriateness, given Black, indigenous, and people of color (BIPOC) AYAs' dynamic psychosocial context, and their unique experience of expanded adverse childhood experiences (ACE) associated with racial and ethnic discrimination.

PCORI framework for patient engagement

• By employing an antiracist and developmentally-appropriate lens, we review current patient engagement practices in AYA oncology, and utilize the PCORI Framework for Patient Engagement as an organizing structure to discuss current strengths and unmet needs, and offer recommendations to promote greater inclusion of racial and ethnic minority AYA patient perspectives.

Token versus genuine patient engagement

• This review is centered on a shared value for genuine (as opposed to token) engagement with AYA patients across the cancer-research process, which requires shared values for both antiracism and developmental appropriateness given the dynamic nature of AYAs' evolving psychosocial context.

Recommendations for topic selection & research prioritization

• Patient engagement must begin with the discussion of potential research topics, and extend to the highest levels of strategic planning within health systems and academic institutions.

• In all research, it must be incumbent on researchers to first identify whether there are racial or ethnic disparities that exist in the area of study.

• Issues of recruitment and access must be examined and addressed to improve the persistent lack of sociodemographic diversity among AYA patients who serve as advisors, and who provide patient-reported input.

Recommendations for proposal review: Design & conduct of research

• To truly engage racial and ethnic minority AYA patients in designing and conducting research, investigators must fully educate and inform patients so they can make meaningful contributions.

• Honest and complete disclosure to AYAs about the costs and benefits of being a patient with cancer engaged with the oncology research process is necessary.

• Racial and ethnic discrimination is an expanded adverse childhood experience (ACE) that researchers must consider, as it may influence what is developmentally appropriate for BIPOC AYAs.

• Acknowledgement and responsiveness to power differentials between and within sociodemographic groups must be incorporated to enable true partnership in research.

• AYA oncology is culpable for token use of the same patient advocates repeatedly in representation of patient perspectives in the dissemination and implementation processes, which is akin to research bias from convenience sampling and produces results that are not representative of the entire population of interest.

• New incentives in academia are needed to ensure that research results are disseminated to the communities that will benefit from the findings, and BIPOC-embodied researchers can be instrumental to this process.

Recommendations for dissemination & implementation of results

• Dissemination of study results to particularly hard-to-reach communities typically demands additional resources and operational support.

Recommendations for evaluation

• Participation in evaluation often requires high engagement from patient advocates at a professional level that is usually not conducive to still-developing AYAs' availability and capacity.

PCORI's core principles of patient engagement

• Transparency-honesty-trust is the key principle for advancing genuine patient engagement over tokenism.