Cancer‐Specific health equity metrics in the United States of America: A scoping review

Abstract Health disparities in cancer care persist, and in some cases are growing, despite decades of research aimed at achieving equal outcomes for all Americans. There is growing consensus that reducing disparities will require a shift from aiming to provide care that is equal, to aiming to provide care that is equitable. The current landscape of metrics and interventions that move beyond equality (i.e., care provided equally to all patients) and towards equity (i.e., care provided variably and justly such that patients achieve equal outcomes) have not been characterized. Thus, the aim of this scoping literature review was to identify cancer‐specific health equity metrics and interventions, and to explore current gaps in the field. Following PRISMA guidelines, PubMed, CINAHL, PsycInfo, and Scopus were searched for studies published in English between 2012 and 2022 that implemented a metric to identify or an intervention to address cancer care inequities in the United States. The search returned 36,724 unique articles, of which 40 articles (1%) included an intervention to advance health equity. Metrics included timeliness of screening and treatment, receipt of goal‐concordant care, and survival. The vast majority of articles were cross‐sectional or cohort studies that described health disparities using one or more outcome metrics. Gaps identified included research on receipt of guideline‐concordant care, interventions addressing multiple levels of structural and social determinants of health, inclusion of children and families, and patient‐reported outcomes or other sources of data that could help inform interventions to advance equity.

screening, incidence, treatment, and outcomes for a range of communities and cancer types. Health disparity is defined as a preventable difference in the burden of disease, outcomes of treatment, and opportunity to achieve optimal health that socially disadvantaged populations experience compared to the population as a whole. 1 Health disparities are driven by social disadvantage or social inequity, which is "the unfavorable social, economic, or political conditions that some groups of people systematically experience based on their relative position in social hierarchies". 2 The broad constellation of social, economic, political, and environmental factors that influence an individual's health are referred to as social determinants of health, and these directly affect health equity, or the "attainment of the highest level of health for all people". 1 There is growing consensus that reducing disparities will require a shift from aiming to provide care that is equal (i.e., care provided equally to all patients), to aiming to provide care that is equitable (i.e., care provided variably and justly such that patients achieve equal outcomes). However, the current landscape of metrics and interventions that move beyond equality and towards equity have not been characterized systematically.
At a time when treatment options and survivorship rates continue to improve for most major types of cancer, vast inequities in cancer incidence and receipt of guideline-concordant treatment persist for racial and ethnic minority groups. 3 Additionally, evidence shows that children, adolescents and young adults, the uninsured, immigrants, refugees, asylum seekers, individuals with disabilities, sexual and gender minorities, and people residing in low-access areas continue to face hurdles in cancer screening and treatment. [4][5][6] Fundamentally, disparities in cancer control, treatment, and outcomes are rooted in the unequal distribution of health determinants, that is, social-structural factors that include institutional and living environments and include health literacy, financial status, and perception of cancer/cancer prevention. 7,8 Efforts to conceptualize the factors affecting cancer outcomes and equity in cancer care led to the development of the National Cancer Institute's research agenda that emphasized multilevel interventions for addressing the individual patient and at least two levels of contextual influence. 9 Moreover, as part of the American Cancer Society's Cancer Control Blueprint series, Alcaraz et al. 7 highlighted the identification of (1) cancer disparities, (2) populations with whom targeted interventions should be co-developed, implemented and evaluated, and (3) metrics for evaluating cancer-related health equity interventions as critical steps needed to advance the field.
A brief timeline summarizing national efforts towards cancer-related health equity is provided as Data S1. In response to these initiatives, some successful interventions for improving health equity have emerged. [10][11][12] However, the current state of such interventions has not been characterized systematically, and validated metrics for assessing the influence of cancer-related health equity interventions remain elusive. Therefore, the purpose of this scoping review was to identify cancer-specific health equity interventions and metrics that have been deployed in practice, to examine how these indicators have been implemented and evaluated across the cancer care continuum, and to identify current research gaps in the field.

| METHODS
We followed the preferred reporting items for systematic reviews and meta-analyses (PRISMA) statement 13 extension for scoping reviews. 14 The literature search was conducted from January 4, 2022, to May 17, 2022, with consultation from a professional librarian. The time frame of the literature search was prompted by the authors' review of widening disparities in cancer care caused by the COVID-19 pandemic and compilation of research priorities. 15 Publications from peer-reviewed journals were searched using the databases Pubmed/Medline, PsychInfo, CINAHL, and Scopus using the following Boolean/phrase or string: ("Neoplasms/diagnostic imaging" [Mesh] OR "Neoplasms/economics" [Mesh] OR "Neoplasms/education" [Mesh] OR "Neoplasms/epidemiology" [Mesh] OR "Neoplasms/ genetics" [Mesh] OR "Neoplasms/pathology" [Mesh] OR "Neoplasms/prevention and control" [Mesh] OR "Neoplasms/psychology" [Mesh]) AND health disparities OR health equity or (oncology OR cancer AND interventions AND health equity) without filters published between 2012 to 2022.
Articles were eligible for inclusion if they were (1) fulltext, (2) English language, (3) prospective or retrospective research studies of any design, (4) implemented and/or evaluated one or more interventions designed to address inequities in cancer care using a specific metric, (5) conducted in the United States, and (6) published between 2012 and 2022. Exclusion criteria were as follows: (1) case studies, review articles, and studies focused only on identifying an inequity or disparity in cancer care. While educational programs to either increase knowledge, beliefs, and attitudes about cancer screening 16,17 or increase participation in clinical research trials 18 have been well-studied, we were specifically interested in methods or interventions that measured an impact on one or more cancer-related health equity metrics.
Two authors independently screened each abstract, and discrepancies were resolved by a third author. Articles that met criteria for inclusion following full-text review were abstracted to describe the study purpose and design, population, metric(s) and main findings.

| RESULTS
A total of 14,078 publications underwent full-text review, after removal of duplicates and retrieval of articles ( Figure 1). Of these, a majority were removed because studies focused on identifying a health disparity in the study population but did not include an intervention for addressing cancer-related health equity or a method for addressing cancer-related health equity. In total, 40 articles were included after full-text review (Table 1).
Of these 40 articles, the majority addressed cancer screening, with most (n = 13) focusing on reducing inequities in colorectal cancer (CRC) screening. One article addressed lung cancer screening, 19 four articles addressed breast cancer screening with mammography [20][21][22] or sameday biopsy. 23 Seven articles addressed cervical cancer screening [24][25][26][27][28][29] or follow-up colposcopy. 30 Eight articles described interventions focused on improving cancer-related health equity. Several studies (n = 6) included a metric pertaining to receipt of standard care [31][32][33][34] or survival duration/mortality. 33,35 One study evaluated the rate of clinical trial enrollment 36 while another evaluated shared decision-making, decision regret, and quality of life. 37 Two articles included cancer survivors or family caregivers, using interventions focused on improving physical activity for cancer-related symptoms and quality of life 38 or telehealth support for family members in palliative care to reduce caregiver distress and increase quality of life. 39 Other studies (n = 4) investigated methods for addressing cancer-related health equity through expansion of Medicare eligibility, 40,41 implementation of current screening guidelines or the implementation of recommendations from the U.S. Preventative Services Task Force for lung cancer screening. 42 One article studied the impact of cancer diagnosis and treatment on employment income loss and health insurance. 43

| Strategiesforimprovingequityin cancerscreening
Across the studies we reviewed, efforts to improve equity of screening rates in different populations with cancer F I G U R E 1 Preferred reporting items for systematic reviews and meta-analyses flow diagram of review screening process. There was no significant increase in CRC screening overall but the mail and monetary and mail and lottery interventions increased FIT completion (7.7%, 7.1%) compared to mail only group. These interventions increased FIT completion more among patients with Medicaid insurance

Author,year Purpose Design/Sample
Hendren et al. 46 Assess a multimodal intervention (letters, automated phone calls, prompts, and mailed fecal immunochemical testing (FIT) kit) on cancer screening among patients in a safety-net primary care practice 366 average-risk patients over-due for mammography or colorectal cancer screening randomly assigned to intervention (n = 185) or usual care (n = 181) Screening interventions for cancer-related health equity Hirko et al. 47 To determine the effect of a mailed motivational messaging screening reminder letter with option to call and request a free at-home fecal immunochemical screening test (intervention) or standard letter reminding screening due (control) 7812 adults age 50-75 years old due for colorectal cancer screening in a rural health system randomly assigned to the intervention (n = 3906) or control (n = 3906) group Horne et al. 52 Investigate the effect of patient navigation on increasing colorectal cancer screening among older African Americans 1220 adults were randomized to the control group receiving printed education materials or intervention that received a patient navigator plus printed materials Huf et al. 49 Compare the effectiveness of a single text message outreach to serial text messaging and mailed fecal home test kits on colorectal cancer screening rates.  25 Evaluate the effectiveness of a multifaceted and culturally appropriate intervention in increasing Pap testing rates in Vietnamese American women 30 Vietnamese community organizations were randomized to either intervention or control condition; 1416 participants were followed. Intervention consisted of group-based education by community health educators, multimedia educational materials in Vietnamese and reminders Miller et al. 26 Explore the impact of a tailored telephone counseling intervention on increasing follow-up adherence after an abnormal Pap smear result among low-income, minority women 211 women were randomly assigned to receive (1) telephone counseling tailored to the barriers elicitied,  22 Develop and evaluate a mammography intervention that provides hope about cancer prevention and treatment.
25 participants were randomized to the intervention (n = 13) or control group (n = 12) Studts et al. 30 Test the effectiveness of a faith-placed lay health advisor intervention to increase cervical cancer screening among middle-aged and older women with low screening rates 345 women randomized to treatment (n = 176) or wait-list control group (n = 169). Intervention provided lay health advisor home visits and newsletters addressing barriers to screening Thompson et al. 29 Investigate two approaches to increase cervical cancer screening among Latinas enrolled in a federally qualified health center 443 Latinas were randomized to (1)  Consistent with these prior studies, results from the current review suggest that telephone outreach providing support and education can improve CRC screening return among women in Medicaid-managed care organizations. 44 Arnold et al. 45 found that follow-up phone calls (either automated or personal) following mail return of fecal immunochemistry test (FIT) kits were associated with improved screening returns among rural residents. Use of mailings and automated phone calls was also associated with increased CRC screening rates for participants in a safety-net primary care practice, 46 as well as rural residents. 47 Goldman et al. 48 also found that use of text messages and automated phone calls, combined with a personal call from a patient navigator for those overdue for cancer screening at 3-months, increased FIT return rates compared to usual care. Use of serial text messages versus a single text message was 17.3% more effective for improving FIT return rates among a largely Black/African American sample. 49 Other strategies for increasing equity in cancer screening included culturally sensitive educational materials paired with a lay navigator or community educator. Bastani et al. 50 tested whether pairing telephone counseling with ethnically targeted print materials tailored to individual's unique risk factors could improve CRC screening rates among those unscreened at 6 months. Results found that the pairing intervention was effective for improving CRC rates in Asian, Latinx, and White, but not Black/African American participants. Similarly, Cole et al. 51 tested whether adding telephone-based patient navigation to motivational interviewing improved CRC screening among older Black men, 51 finding both navigation alone and adding navigation to motivational interviewing was superior to motivational interviewing alone. Other studies demonstrated that the use of patient navigation was also more effective than printed materials for improving CRC screening among older Black men. 52 Use of lay health educators was also effective in improving CRC screening rates among Filipino Americans, 53 and both professional and community-based peer navigators were effective at improving CRC screening among Black/ African Americans. 54 While efforts to promote CRC screening using community-based interventions were associated with improvements in outcomes, the degree to which communitybased interventions improved equity for different racial and ethnic groups were mixed. Brown et al. 55 evaluated the impact of a citywide public health campaign for promoting screening colonoscopy and found that while overall incidence and mortality related to colorectal cancer declined, Black residents continued to have higher incidence and mortality rates. Conversely, a communitybased cancer screening program delivered through local libraries was associated with higher CRC screening, especially among respondents born outside the United States and those who were least engaged in care. 28 Other information or incentive-based strategies have been tested with limited efficacy. 56,57 Ten articles highlighted the importance of individualized, culturally appropriate outreach strategies and/ or involving social support resources (interpersonal or network) for improving cancer screening rates among minority populations. Cervical cancer screening rates improved with a lay health worker-delivered intervention called AMIGAS among women of Mexican origin 24 and a multifaceted and culturally appropriate group-based intervention among Vietnamese American women. 25 Other culturally sensitive interventions that provided more social interaction with participants were also effective in improving screening rates. 27,29,30 While mailings and automated phone calls appeared to be effective in improving overall breast cancer screening rates, 46 use of individualized risk assessment was effective in improving mammography rates among racial and ethnic minority groups at higher risk for breast cancer. 21 However, breast cancer screening rates were more likely to improve when a support person was identified among Native American women 22 or when engaging Latinas personal and social breast cancer screening network compared to only addressing personal risk factors. 20 Conversely, tailored telephone counseling had a significant effect on adherence to follow-up recommendations after an abnormal Pap test compared to mailed home materials or standard care among low-income women. 26

| Treatmentinterventionstoimprove cancer-relatedhealthequity
While efforts to increase equity in cancer screening between groups facing disparities were a major focus among articles we reviewed, fewer articles focused on interventions aimed at improving equity in treatment, with several notable exceptions. Cykett et al. 31 used a pragmatic design to evaluate the impact of providing clinicians real-time warnings about missed appointments and procedures using the electronic health record (EHR), race-specific feedback on completion rates, and follow-up/intervention by a nurse navigator. Results found that the intervention was associated with reduction in disparities in receipt for curative treatment among Black/African American patients.
Similarly, a lay navigation program at a public safetynet hospital for women with cervical cancer was associated with an almost 20% increase in receipt of curative treatment with chemoradiotherapy among participants. 32 However, results were not universal; evaluation of a multidisciplinary breast program on timeliness of care from diagnosis to treatment found the program was not impactful in improving delivery of screening, work-up, and treatment for women due to inadequate infrastructure and support. 34 Nattinger et al. 35 examined the effect of ending a policy that precluded payment for breast cancer surgery among Medicaid beneficiaries in New York. Results found evidence of improved 3-year survival and a 53% reduction in socioeconomic disparity during implementation of the policy. In addition, use of a cancer care equity program designed to mitigate the financial burdens associated with transportation and lodging for participants in clinical trials led to a significant increase in clinical trial enrollment, including among females and individuals who were younger, living further away, living with metastatic disease, and with lower incomes. 36 In 2021, Swayze et al. 21 evaluated the impact of establishing a local gynecologic oncology office on access to care, guideline-concordant care, and median survival among women with cervical cancer. Results showed that women receiving care locally were more likely to undergo guideline-concordant care, with an increase in median survival from 30.8 to 52.5 months. Likewise, Durand et al. 37 compared different decision support tools for patients with breast cancer, finding that a picture option grid led to higher knowledge, improved decision process, lower decision regret and more shared decision-making compared to usual care, especially among women with lower socioeconomic status and health literacy scores. However, the interventions did not affect concordance of care, treatment choice, or levels of patient-reported anxiety.

| Interventionsaddressingequityin cancersurvivorsandcaregivers
Only two of the 40 studies reviewed described interventions designed to improve equity in outcomes for cancer survivors or family caregivers. Hirko et al. 38 evaluated the impact of a clinic-based physical activity program for rural-residing cancer survivors. While only 0.59% of the eligible cancer survivors participated, the intervention was associated with improvements in fatigue, constipation, pain, and sleep quality post-intervention. Similarly, Dionne-Odom et al. 39 assessed the effectiveness of a lay navigator-led early palliative care telehealth intervention for Black/African American and/or rural-dwelling family caregivers of individuals with advanced cancer. The intervention was found to be feasible, acceptable, and was associated with statistically significant reductions in distress and higher quality of life scores compared to the control group.

| Methodstoevaluatecancer-related healthequity
Of the five studies employing methods for evaluating health equity, four examined the effect of policy level changes, including adoption of cancer screening recommendations from the U.S. Preventative Task Force (USPTF) and Medicaid expansion. Chapman et al. 58 studied a 1980 U.S. birth cohort of Black and White women, comparing tradeoffs of breast cancer screening strategies between groups. Results found that initiating biennial screening in Black women at age 40 could reduce disparities in breast cancer mortality with benefit-harm ratios similar to White women ages 50 to 74 years old who are screened biennially. Likewise, Ritzwoller et al. 42 examined the impact of the 2021 USPTF expansion of lung cancer screening eligibility, finding that the expansion led to a 53.7% increase in lung cancer screening eligibility across five community-based healthcare systems. Of note, under the expanded eligibility criteria, a larger proportion of women and more racial and ethnic minority groups were eligible for lung cancer screening, underscoring the potential impact of policy-level changes in efforts to reduce disparities in cancer-related outcomes.
Similarly, when Li, Najarian & Halpern 40 examined whether Medicaid expansion influenced endocrine therapy prescriptions used to treat breast cancer in racially more diverse and less diverse states, they found that Medicaid expansion increased the number of endocrine therapy prescriptions filled, particularly in racially more diverse expansion states. Another study found that Medicaid expansion was associated with decreased uninsurance, increased early-stage diagnosis of genitourinary cancers, and increased active surveillance for low-risk prostate cancers, especially among low-income populations. Biddell et al. 43 examined the impact of cancer diagnosis and treatment on employment income and health insurance in a national sample of adults. They found that Non-Hispanic Black and Latinx patients had a 10.2% and 12.4% higher probability of substantial income loss, and a 9.3% and 10.0% higher probability of changes in health insurance compared to Non-Hispanic White patients.

| DISCUSSION
The purpose of this scoping review was to identify cancerspecific health equity interventions and metrics that have been deployed in practice, to examine how these indicators have been implemented and evaluated across the cancer care continuum, and to identify current research gaps in the field. Results of the review led to several key findings and identified gaps in the field, which are discussed below.
First, the studies included in the review demonstrate that a major focus for the field related to equity has been cancer screening. Results suggest that use of strategies designed to improve outreach and follow-up can positively improve cancer screening rates (especially, CRC screening rates), and-critically-that these approaches may be effective for improving screening rates in populations disproportionately impacted by cancer such as Black/ African Americans and rural Americans. 26,45,46,[48][49][50] With advances in technology and home-based screening methods, it is incumbent for healthcare systems and insurers to facilitate more accessible options for cancer screening, especially for individuals with known risk factors and hourly workers who are greatly impacted by taking time off work for screening appointments.
Second, the review findings underscore the importance of using community engagement to build support for cancer screening in communities facing systematic inequalities. 20,28,[51][52][53][54][55] Overall, outreach by professional healthcare providers and lay educators alike appears to improve screening rates, including minority groups. 25,29,30 In addition, results suggest that strategies designed to increase access to cancer screening can reduce disparities in guidelineconcordant screening. 19,23 However, additional evidence is needed to clarify which strategies are likely to be most effective for building engagement in different communities.
Third, and closely related, access to patient navigation during screening and treatment can positively impact cancer-related health equity. 31,32 Use of technology to identify patients who may benefit from navigation 31 as well as policies to reduce financial burden associated with cancer treatment may positively influence timeliness in receiving treatment and reduce disparities in mortality. 35 Of note, Patel and colleagues [59][60][61] have an ongoing study that tests an intervention designed to improve advance care planning and symptom management among low-income and minority hourly-wage workers with cancer by providing a lay health worker to all patients newly diagnosed with cancer. The intervention aims to educate and activate patients to engage in advance care planning and symptom management with their oncology providers and will assess quality of life, patient activation and satisfaction with decision-making, symptom burden and total healthcare use and costs.
Findings from the scoping review also suggest that strategies designed to increase access to cancer specialists and resources needed to participate in cancer clinical trials (including travel and lodging) can help reduce disparities in receipt of guideline-concordant care and clinical trial participation. In addition, the results support the effectiveness of health services designed for cancer survivors and family caregivers on reducing disparities in cancerrelated symptoms and caregiver distress. 38,39 A notable finding was the importance of evaluating the impact of policy changes on both cancer outcomes and equity. Several studies found that policy changes were associated with reductions in disparities. 40,41,58 Ritzwoller et al. 42 evaluation of the USPTF expansion for lung cancer screening eligibility provides actionable steps to inform the community so that newly eligible patients are aware and can access screening. The financial impact of cancer diagnosis and treatment creates a widening disparity that requires a multifaceted approach. 43 Mohan and Chattopadhyay 11 conducted a systematic review of economic evaluations of interventions leveraging social determinants of health, such as patient navigators, transportation assistance, and hometesting, to improve screening for breast, cervical and colorectal cancer. Improved cancer screening for underserved communities was cost effective with a median intervention cost of $123.87, a median incremental cost per additional person screened of $250.37, and a median incremental cost per quality-adjusted life-year (QALY) of $3120.00.
Finally, results from this scoping review highlight the lack of clarity about how best to measure equity (or a lack thereof) in the various dimensions of the cancer continuum. While it is clear that equity has been a consistent focus for the field for decades, studies evaluating interventions specifically designed to address equity, or to evaluate the degree to which certain outcomes can serve as reliable "equity metrics" in the cancer space are lacking. The lack of generalizable equity metrics in the oncology space underscores both the contextual and often layered nature of barriers that can prevent individuals from getting equitable access to prevention, screening, diagnosis, treatment, and survivorship care for cancer. Adding to this challenge, it could be argued that, in certain populations, metrics such as knowledge of CRC and intent to screen could be considered equity metrics, although the degree to which these endpoints directly measure equity, or merely act as mirrors reflecting deeper issues of equity, remains to be determined.

| Gapsincancer-relatedhealth equityresearch
While this scoping review identified studies across the cancer care continuum, approximately 20% of the studies only incorporated one level of intervention for addressing health disparities, such as outreach and follow-up calls. Addressing other social determinants of health and structural barriers, including cancer services in local communities, receipt of guideline-concordant care, reduced or free screening and treatment, and living wages or timeoff to undergo screening and treatment are critical areas that have yet to be studied. Evidence to inform the most effective strategies for building engagement in different communities and in using patient-reported outcomes or other sources of data advance equity are also needed. In addition, all of the identified studies were conducted in adult populations, lacking participants who were children or families with children. It has been estimated that scaleup of interventions for improving access to healthcare services and childhood cancer treatment could not only avert childhood deaths from cancer but would produce a net global lifetime productivity gain. 62 Studies to address the structural barriers of underserved populations, childhood cancer disparities and the impact on the family unit are especially needed to advance equity across the cancer care continuum.

| Limitations
The scoping review was focused on cancer-specific health equity metrics in the United States of America, and results of the review should only be generalized in this context. As a scoping review, the approach to the literature search was systematic but not exhaustive, and other interventional cancer studies may not have been included. Bias may have influenced the interpretation of findings and identification of cancer-related health equity metrics that have been previously studied and or tested due to the search strategy, only including research studies published in the English language, conducted in the United States of America, and within the specific time frame. While the scoping review only provides a snap shot of important work in the field of cancer-related health equity metrics, the intention was to highlight crucial gaps and strategies to advance future research in the United States of America.

| Conclusion
This scoping review identified interventions that were effective in reducing cancer-related disparities and health equity metrics that may be useful for future studies to incorporate. Interventions that were found to be effective in reducing disparities included patient reminders, access to patient navigators and local services, culturally sensitive outreach and support resources (i.e., social support, transportation), and policies to expand covered services for cancer screening and treatment. Evidence to inform the most effective strategies for building community engagement in cancer screening as well as the use of patientreported outcomes and other sources of date to evaluate cancer-related outcomes is needed. Cancer-related health equity metrics used to evaluate whether the interventions were associated with more equitable outcomes included traditional measures (i.e., rate of screening or morbidity and mortality) as well as more nuanced metrics such as the rate of early-stage versus late-stage diagnosis, receipt of guideline-and goal-concordant care, and financial burden of cancer screening and treatment. A majority of the research studies included in the scoping review were focused on cancer screening, suggesting that more interventional research is needed to advance equity in treatment and survivorship outcomes, especially among underserved populations. Finally, interventions developed to address the social and structural barriers of low-resourced communities, caregivers, and children or families with children are crucial for advancing health equity across the cancer care continuum.

FUNDINGINFORMATION
No funding was received for this work. This research was supported (in whole or in part) by HCA Healthcare and/ or an HCA Healthcare affiliated entity. The views expressed in this publication represent those of the authors and do not necessarily represent the official views of HCA Healthcare or any of its affiliated entities.

CONFLICTOFINTERESTSTATEMENT
The authors declare no conflicts of interest.

DATAAVAILABILITYSTATEMENT
Data compiled for the literature review are available upon request.