Principles to operationalize equity in cancer research and health outcomes: lessons learned from the cancer prevention and control research network

Reflecting their commitment to advancing health equity, the Cancer Prevention and Control Research Network (CPCRN) established a Health Equity Workgroup to identify and distill guiding principles rooted in health equity, community-engaged participatory research (CBPR), social determinants of health, and racial equity frameworks to guide its collective work. The Health Equity Workgroup utilized a multi-phase, participatory consensus-building approach to: (1) identify recurrent themes in health and racial equity frameworks; (2) capture perspectives on and experiences with health equity research among CPCRN members through an online survey; (3) engage in activities to discuss and refine the guiding principles; and (4) collect case examples of operationalizing equity principles in cancer research. Representatives from all CPCRN centers endorsed nine core principles to guide the Network’s strategic plan: (1) Engage in power-sharing and capacity building with partners; (2) Address community priorities through community engagement and co-creation of research; (3) Explore and address the systems and structural root causes of cancer disparities; (4) Build a system of accountability between research and community partners; (5) Establish transparent relationships with community partners; (6) Prioritize the sustainability of research benefits for community partners; (7) Center racial equity in cancer prevention and control research; (8) Engage in equitable data collection, analysis, interpretation, and dissemination practices; and (9) Integrate knowledge translation, implementation, and dissemination into research plans. Dissemination products, such as toolkits and technical assistance workshops, reflecting these principles will foster knowledge transfer to intentionally integrate health and racial equity principles in cancer prevention and control research.


Introduction
The year 2020 marked a social, political, and public health reckoning as communities across the United States (US) bore witness to the impact of the COVID-19 pandemic and the disproportionate burden and severity of outcomes among communities already experiencing health and economic disparities. The intersection of the COVID-19 pandemic with the Black Lives Matter Movement also motivated deep personal self-reflection and raised critical public consciousness of the need to address and reduce systemic racism. From social justice and population health perspectives, increasing awareness of, and taking action against systemic racism must occur across all spheres and disciplines of public health and health research. Achieving the vision of population health equity requires a more integrated approach than has previously been attempted in the US-one that leverages authentic community engagement and meaningful partnerships, accounts for the roles of social determinants of health (SDH), and demonstrates a deep commitment to tackling systemic racism at multiple levels of influence within the healthcare system and broader socio-political environment. In this paper, we describe a set of principles that can help achieve these objectives, derived both from the existing literature and from our experience in cancer prevention and control.
Cancer remains a significant public health problem, with 1.8 million Americans diagnosed in 2021 and more than 600,000 expected to die from cancer in 2022 [1,2]. Cancer outcome disparities in the US are expected to widen among racial and ethnic minoritized and medically underserved groups by 2030 [3,4]. These disparities persist despite evidence-based guidelines for cancer prevention, screening, and treatment that, when implemented equitably, would otherwise be expected to dramatically reduce group differences in outcomes. In response to this persistent problem, the Centers for Disease Control and Prevention (CDC) and the National Cancer Institute (NCI) established, in 2002, the Cancer Prevention and Control Research Network (CPCRN). The CPCRN is a network of academic, clinical, and community partners whose goals are to: accelerate the uptake of evidence-based strategies in cancer prevention and control in communities; increase implementation and reach in medically underserved populations to reduce disparities; investigate determinants of implementation and programmatic success; and develop the workforce in cancer prevention and control research [5,6].
The CPCRN convenes a wide array of perspectives and expertise for the common goal of reducing cancer burden [6]. The CPCRN is a 'thematic research network' of the CDC's Prevention Research Centers (PRCs) which are funded to "conduct community-based applied public health research to address chronic diseases and other leading causes of death and disability in the United States" [7]. Building on the strong community partnerships of PRCs, the CPCRN prioritizes community-engaged cancer research to increase the local relevance of the research and facilitate adoption of evidence-based interventions (EBIs). The CPCRN collaborates with local, state, and national partners representing multiple sectors, including community-based organizations, federally qualified health centers, and state and national cancer control coalitions. The CPCRN's structure fosters cross-center collaboration through multicenter workgroups to advance knowledge around a common theme (e.g., Rural Cancer, Survivorship, Implementation Science) with the goal of supporting the implementation of EBIs. Examples of the wide-ranging issues addressed by CPCRN initiatives were documented by White and colleagues [5] and demonstrate this network's ability to tackle the complex multilevel etiologies of cancer health disparities.
In many ways, these past several years concretized the historic inequities in SDH. The COVID-19 pandemic highlighted that racial and ethnic minoritized and medically underserved populations experience a disproportionate burden of morbidity and mortality due to unequal access to and distribution of social resources [8][9][10][11]. Simultaneously, the brutal murders of George Floyd, Ahmaud Arbery, Breonna Taylor, and other black men and women in the spring and summer of 2020 resulted in protests across the US, raising public consciousness of systemic racism as a fundamental contributor to poor health outcomes in racially minoritized populations [12,13].
Decades of research have documented how systemic racism is reflected in highly segregated and densely populated neighborhoods whose residents experience substantial levels of poverty and near-poverty [14][15][16][17]. These same neighborhoods are often federally designated as medically underserved areas with shortages of culturally and languageappropriate healthcare providers, as well as lack of access to high quality cancer care compared to more resourced areas. When care is sought, patients sometimes endure long waiting periods for appointments, test results, and unnecessary and expensive testing and care. Furthermore, disparities in health insurance coverage serve as additional barriers to equitable care [18]. A problematic history of racism, poor quality of care, and discrimination in the healthcare system have contributed to normative beliefs and practices that deter care seeking. Feelings of mistrust, disrespect, and loss of control are reinforced by community members' negative experiences and persistent poor health outcomes. Racial and ethnic minoritized groups often report lower quality of care, lack of respect, less communication rapport, lower trust, and higher perceived discrimination with their providers than non-Hispanic whites. According to the 2020 National Cancer Opinion (NCO) Survey, racial and ethnic minoritized groups, including Black (76%), Hispanic (70%), and Asian Americans (66%), are more likely to believe that racism can impact the healthcare a person receives compared to non-Hispanic whites (53%) [19]. In the Study of Women's Health Across the Nation (SWAN), Black participants were more likely to report racism as a barrier to breast and cervical cancer screening and unequal access to healthcare (71 vs 47%) compared to non-Hispanic whites [20]. Immigrant status adds an additional barrier to breast, cervical, and colorectal cancer screening for Latinx, Asian/Asian American and other minoritized populations [21,22]. Financial stress, language barriers, low health literacy, lack of transportation and childcare, and stigma may also limit individuals' ability to adhere to recommended screening and treatment guidelines [23][24][25][26]. Another prominent study demonstrated that even after controlling for socioeconomic status, African American men and women, Asian/Pacific Islander men, and Alaska Native/American Indian men and women still have among the highest rates of cancer mortality [27] compared to their non-Hispanic white counterparts. Persistent inequities in SDH contribute to significant disparities in cancer incidence and mortality between Asian/Pacific Islander and Alaska Native/American Indian populations and other minoritized groups [28,29]. These inequities span multiple generations and originate from longstanding discriminatory and racist policies and practices, including displacement from homelands and forced acculturation [30].
By mid-summer 2020, the growing momentum to name racism as a root cause of inequities culminated in the CDC declaring racism a serious threat to the public's health [31]. The National Institutes of Health and National Cancer Institute then issued Requests for Information (RFI) for recommendations to strengthen racial equity, diversity, and inclusion in the biomedical workforce and advance health equity research [32,33]. Taken together, these initiatives signaled to researchers and research institutions the urgency of translating this equity paradigm into their work in an authentic way. In parallel, the events of the last several years inspired reflective conversations about health equity, systemic racism, and SDH within CPCRN. As a result, we conducted a horizon scan within and across collaborating centers to understand how these concepts were being integrated and operationalized across the network. Then we conducted an environmental scan of the current and extensive literature on equity-related frameworks to identify and distill guiding principles common to CPCRN members to synergize and coordinate efforts around health equity research more meaningfully. The search parameters of the environmental scan spanned a review of literature on CBPR, community engagement, participatory, health equity, racial equity, and racial justice frameworks. In a unified commitment to centering equity in our cancer prevention and control research, the CPCRN established the Health Equity Workgroup in 2020. This group comprised representatives from all eight CPCRN Collaborating Centers, the Coordinating Center, funders, and affiliates (formally defined as faculty members, researchers, or community partners who participate in CPCRN activities, but are not funded as a network center), and was charged with developing actionable guiding principles to work towards health and racial equity in cancer prevention and control research.
Although multiple health and racial equity frameworks exist in the literature, there is less guidance on how to operationalize these frameworks in practice, particularly for implementation science and cancer prevention and control, as they focus on equity-oriented research [34,35]. This paper describes the participatory and consensus-building approach adopted by the Health Equity Workgroup to: (1) curate health and racial equity frameworks, principles, and operational definitions, (2) vet and finalize these principles with academic and community partners at our annual meetings and via survey/qualitative data collection, and (3) highlight case examples among CPCRN members to illustrate the application of these principles in community and clinical practice.

Developing guiding principles rooted in equity
The development of principles reflecting SDH, health and racial equity, and participatory approaches included a highlevel environmental scan of the academic and gray literature, a cross-center survey of CPCRN members, guided discussions in CPCRN Steering and Workgroup meetings, and consensus-building activities at two Annual CPCRN Meetings. This process was iterative and participatory, with built in feedback loops to ensure the rich expertise, perspectives, and experiences of the CPCRN centers were reflected in the equity principles and their operational definitions.
Initial discussions within the Health Equity Workgroup revolved around frameworks currently used by CPCRN centers to ground their cancer prevention and control research in equity. The most commonly cited frameworks included community-based participatory research (CBPR) [36], SDH [37], and the Minority Health and Health Disparities Research Framework [38] from the National Institute on Minority Health and Health Disparities. Further, CPCRN members noted the need to integrate implementation science frameworks-a core strength of the Network and a reflection of its long history of advancing implementation science in cancer prevention and control. Aligned with the recent calls in implementation science for an explicit focus on health equity, anti-racism, and structural racism, the Health Equity Workgroup sought to further clarify the racial equity paradigm through the additional review of the academic and gray literature [39][40][41]. The R4P framework [42], the Government Alliance on Race and Equity (GARE) [43], and Greenlining Institute [44] were flagged as important resources to center racial equity across the principles. Members of the Health Equity Workgroup reviewed the aforementioned frameworks and reports and conducted a high-level narrative synthesis to inform the first draft of nine principles common among the Network. These principles were presented to the Health Equity Workgroup and CPCRN Steering Committee to solicit preliminary feedback and guide next steps, with a goal of obtaining network-wide commitment to intentionally integrate these equity principles across CPCRN members and within workgroups.
Next, the Health Equity Workgroup disseminated an online survey to current and former members of the CPCRN, federal agency partners, and affiliate members, to assess 1 3 whether they currently apply the principle in their center's work (i.e., "Is this principle applied to your Center's work?") and to rate the relevance of each principle for a framework common across the CPCRN (i.e., "Please also rate each principle based on what you perceive as its relevance to an integrated equity framework for the CPCRN" (1 indicating lowest relevance and 5 indicating highest relevance). Respondents were also asked to share case examples from their respective centers, suggest evaluation metrics, propose alternative principles informed by their work or existing frameworks, and provide general feedback. Ratings were analyzed and open-ended responses informed operational definitions of the equity principles. The Health Equity Workgroup presented survey results, the revised set of principles, and their definitions at the CPCRN Annual Meeting in 2021 and engaged in consensus building with attendees to refine and approve each guiding principle. Overall, the 28 survey respondents and 79 Annual Meeting participants endorsed nine health and racial equity principles with minor suggestions for modifications. After the meeting, the recommended changes were incorporated into a revised set of principles.

Refining the principles through consensus building
We calculated the average relevance for each principle (score range = 1 [low relevance]-5 [high relevance]) as well as their average application in CPCRN centers. All but one principle ("Practice and Policy Translation" (P9)) were rated 4.11 or above ( Fig. 1), reflecting overall high perceived relevance to the CPCRN.
In terms of how each principle was applied in work, at least 60% of respondents felt that the principles were applied in their center's work (Fig. 2); for some, like power-sharing and capacity building (P1) and community engagement (P2), 100% of respondents stated that these are applied to their work. For others, such as "Competency in and Commitment to Racial Equity" (P7) and "Practice and Policy Translation" (P9), application was lower at 61 and 65%, respectively.
The responses to the open-ended questions provided context for these lower ratings: a few respondents stressed that a racial equity principle was indeed essential, but not yet operationalized in a systematic way within their centers. Furthermore, a few respondents stated that the "Practice and Policy Translation" label was vague and did not stress implementation explicitly. As a result of this feedback, we reconceptualized this principle as "Knowledge Translation, Implementation, and Dissemination" to reflect the growing interest in and commitment to equitable dissemination and implementation, as per the CPCRN strategic plan [45].
Through this process, nine guiding principles were approved, which are anchored in the overarching themes of Health Equity, Racial Equity, and Social Determinants of Health: (1) Engage in power-sharing and capacity building with partners; (2) Address community priorities through community engagement and co-creation of research; (3) Explore and address the systems and structural root causes of cancer disparities; (4) Build a system of accountability between research and community partners; (5) Establish transparent relationships with community partners; (6) Prioritize the sustainability of research benefits for community partners; (7) Center racial equity in cancer prevention and control research; (8) Engage in equitable data collection, analysis, interpretation, and dissemination practices; and (9)  Integrate knowledge translation, implementation, and dissemination into research plans (Fig. 3).

Applying the health and racial equity principles
In addition to specifying the principles, we also focused on their application in cancer prevention and control research to ensure they are both feasible and meaningful.  (2) patient navigation to follow-up colonoscopy. The study is designed as a type 2 hybrid effectiveness-implementation trial that will assess effectiveness at increasing CRC screening and follow-up rates while also assessing implementation outcomes. Partner CHCs are located in rural counties in western and eastern North Carolina. NYC CONNECT is guided by a community-academic-clinical partnership and aims to improve breast, cervical, and colorectal cancer screening in historically underserved immigrant and minoritized communities in four neighborhoods in New York City. The program uses a trauma-informed approach and leverages community health workers who are embedded in community and clinical settings to deliver, culturally and linguistically tailored cancer education, screening for SDH, and navigation to cancer screening services and social resources (e.g., health insurance, food assistance). In addition, NYC CONNECT works with community partners to explore systemic racism in priority neighborhoods and co-develop and implement locally relevant SDH and racial equity strategies; the goal is to examine whether interventions to account for SDH and reduce the experience of systemic racism may improve cancer screening, wellbeing, and other neighborhood-level social indicators. These three case examples serve to illustrate how the principles were operationalized in existing cancer prevention and control programs serving different populations in various settings.
We provide examples of how these guiding principles were applied in CPCRN research with diverse populations in diverse contexts [53,54]. Operationalizing equity principles through a participatory process in a collaborative network of academic and community partners is an essential step towards achieving population health and reducing cancer disparities. This process paves the path forward and guides the development of evaluation approaches to ensure accountability, quality, and meaningful gains in our collective efforts as a network to achieve cancer equity. Below, we detail next steps and examples of how the equity principles are being integrated into the work of CPCRN centers and workgroups. First, by acknowledging and measuring inequities and structural racism as fundamental causes of cancer disparities, our work must be followed with deliberate and proactive actions. A detailed description of a toolkit outlining steps towards health and racial equity in cancer prevention and control research can be found in Adsul et al. in this supplement [55]. Briefly, the toolkit includes: (1) ways to operationalize each principle; (2) actions taken within the Network to apply the principles; (3) reflection questions to guide future research; and (4) resources and methods for assessment. Aiming to operationalize and illustrate these themes further, the Health Equity Workgroup is currently conducting in-depth interviews with CPCRN centers and their community partners to assemble a comprehensive repository of how all centers are utilizing equity-advancing strategies that could be tailored and implemented across other practice and community settings and population groups.
Second, the CPCRN equity principles will formalize the integration of health equity into the mission and projects of the CPCRN. This commitment to equity is aligned with the priority of the CDC and NCI-CPCRN's current and previous funding agencies-to address SDH related to cancer disparities. Drawing from the equity principles, the • Disseminate all findings to a broad and diverse audience including policymakers, providers, academics, community partners, and community members CPCRN proposes several recommendations to diversify the cancer research workforce and improve health equity: (1) increase the diversity of the NIH and biomedical workforce (e.g., Principle 7); (2) involve representatives from minoritized communities on the decision making and scientific review committees (e.g., Principles 1, 2); (3) direct priority funding towards studies that consider the impact of more than one social/structural determinant on health outcomes (e.g., Principle 3); and (4) support long-term community-academic-clinical partnerships for meaningful and impactful health equity research (e.g., Principle 2, 6). In addition, the equity principles are also informing the development of study protocols that prioritize health equity. For example, the Cancer Survivorship Workgroup engaged in a collective reflective process to ensure their planned study on the experiences of racism and patients' engagement with survivorship care is built around the equity principles from the outset [56]. Third, heeding the warnings against "health equity tourism" [57,58], we envision the equity principles as foundational for developing metrics and evaluation tools for the CPCRN to ensure quality research and accountability to our stated commitment to equity. Importantly, members of the CPCRN centers reported that articulating their engagement with each equity principle allowed them to self-reflect, assess their performance, and identify opportunities to further advance equity in their own work. Recognizing that measurement is integral to accountability, the Health Equity Workgroup is developing and validating measures and tools that explicitly assess and evaluate research efforts across CPCRN centers.