An Intervention-Based Approach to Achieve Racial Equity in Gynecologic Oncology : Obstetrics & Gynecology

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Gynecology: Narrative Review

An Intervention-Based Approach to Achieve Racial Equity in Gynecologic Oncology

Gamble, Charlotte MD, MPH; Woodard, Tyler J. MD, MEd; Yakubu, Ayesha I. MD; Chapman-Davis, Eloise MD

Author Information

Division of Gynecologic Oncology, MedStar Washington Hospital Center, and Georgetown University, Washington, DC; the Division of Gynecologic Oncology, Washington University School of Medicine in St. Louis, St. Louis, Missouri; the Department of Obstetrics and Gynecology, Virginia Commonwealth University, Richmond, Virginia; and the Department of Obstetrics and Gynecology, Weill Cornell Medicine, New York, New York.

Corresponding author: Charlotte Gamble, MD, MPH, Division of Gynecologic Oncology, MedStar Washington Hospital Center, Washington, DC; [email protected].

Financial Disclosure The authors did not report any potential conflicts of interest.

Each author has confirmed compliance with the journal's requirements for authorship.

Peer reviews and author correspondence are available at https://links.lww.com/AOG/D366.

This is an open access article distributed under the terms of the Creative Commons Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC-ND), where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

Obstetrics & Gynecology 142(4):p 957-966, October 2023. | DOI: 10.1097/AOG.0000000000005348

Racial inequities within gynecologic oncology exist at every step of the cancer continuum. Although the disparities have been well described, there is a significant gap in the literature focused on eliminating inequities in gynecologic cancer outcomes. The goal of this narrative review is to highlight successful, evidence-based interventions from within and outside of gynecologic oncology that alleviate disparity, providing a call to action for further research and implementation efforts within the field. These solutions are organized in the socioecologic framework, where multiple levels of influence—societal, community, organizational, interpersonal, and individual—affect health outcomes.

Racial disparities in outcomes for people with gynecologic cancers have been well documented over the past two decades.1–6 The Black–White gap in survival for patients with cervical, ovarian, and endometrial cancers remains statistically and clinically significant and has persisted over time.7 The etiology of these disparities involves every step of the cancer continuum, from diagnosis and treatment, to survivorship and palliative care.8

Racial inequities in oncology are grounded in systemic injustices that disproportionately affect Black patients and their ability to access high-quality cancer care.9 Examples of these societal drivers include environmental injustice, segregation, differences within the insurance marketplace, and intergenerational poverty.10 Layered on these societal ills are incompletely understood aspects of tumor biology that compound and magnify the survival gap.11 Our health system is not immune to societal injustices, with an infrastructure based on multiple systems that were built for affluent patients without a defined focus to improve outcomes for vulnerable and minoritized people.12

Although these disparities have been well described, a significant opportunity remains to further both the development and adaption of interventions that reduce and eliminate inequity in clinical care and outcomes. Beyond this, continuous policy change is necessary to fund and maintain achievements in health equity (Fig. 1). The Society of Gynecologic Oncology, the American Society of Clinical Oncology, and the American Association for Cancer Research all have released calls to action for the elimination of disparities.13–15 The goal of this narrative review is to highlight interventions that can be developed or adopted within gynecologic oncology to eliminate racial inequities in gynecologic cancer outcomes.

F1
Fig. 1.:
The arc of health equity research, demonstrating the multiple phases or generations of health equity research. Adapted from Kilbourne AM, Switzer G, Hyman K, Crowley-Matoka M, Fine MJ. Advancing health disparities research within the health care system: a conceptual framework. Am J Public Health 2006;96:2113-21. doi: 10.2105/AJPH.2005.077628.

Due to the legacy of slavery and insidious anti-Black racism in the United States and in our health systems, we acknowledge that the most striking injustices in gynecologic cancer care disproportionately affect Black or African American patients.8,16 Yet the challenges and solutions discussed within this review can be extrapolated to inform, and in some cases directly address, injustices that affect other vulnerable groups: minoritized ethnic groups (Latinx community, Asian Pacific Islanders, Native peoples), immigrants, people who are justice-involved, people within the LGBTQ+ (lesbian, gay, bisexual, transgender, queer+) community, people who are disabled, people who are experiencing homelessness, and people who have low incomes or are geographically constrained. Recognizing the intersectionality of these identities is critical not only to understanding disparate outcomes but to creating solutions that center the margins.17,18 We organize evidenced-based strategies within the socioecologic framework. This framework describes the way in which multiple levels of influence—societal, community, organizational, interpersonal, and individual—all affect health outcomes.19,20 Each of these levels present opportunities for the development of targeted interventions to eliminate inequity within gynecologic oncology (Fig. 2).

F2
Fig. 2.:
The socioecologic framework that can be applied to an intervention-based approach to health equity within gynecologic oncology. Clinicians and research scientists may actively engage at any level to develop and adopt innovative solutions to eliminate inequity in gynecologic oncology. Data from McLeroy KR, Bibeau D, Steckler A, Glanz A. An ecological perspective on health promotion programs. Health Educ Q 1988;15:351−77.

POLICY

At the policy level, two examples of strategies that have the potential to reduce racial inequity in gynecologic cancer outcomes include increasing National Institutes of Health (NIH) funding dedicated to the development and equitable adoption of novel therapeutics for gynecologic cancers and eliminating insurance barriers to care.

Federal Research Funding

Ovarian, cervical, and uterine cancers remain underfunded relative to other cancer types.21 Endometrial cancer, a disease that disproportionately affects Black patients, has the second largest Black–White survival gap of all cancers (more than 20%) and is increasing in lethality. Importantly, uterine cancer remains among the lowest-funded diseases in the National Cancer Institute (NCI) budget.21,22 In January 2023, Congress passed HR 2617, an omnibus bill that increased cancer research funding and addressed Medicare cuts. This bill will effectively increase research funding for the NIH by $2.5 billion, the NCI by $408 million, and the U.S. Food and Drug Administration by $226 million.23,24 In 2023, there is specific funding through the Office of Research on Women's Heath targeted to chronic conditions understudied among women, including gynecologic malignancies as a focus topic.25

However, without funding strategies dedicated to operationalizing equity, we risk widening disparities. In fact, this very concern has been demonstrated for melanoma. National Cancer Institute funding of melanoma research increased from $97.7 million in 200726 to $126.2 million in 2014.27 This was associated with multiple phase 3 trials that led to new drug approvals and a 6% reduction in mortality between 2013 and 2017.28 Yet, White patients disproportionately received immunotherapies in their early rollout, and the Black–White 5-year survival gap subsequently widened to become the widest of all cancer types in the United States at 24%.29,30

As we look to expand access to federal funding for gynecologic cancer research, we also need to hold researchers accountable by mandating equity measures as part of funded research studies. There are several initiatives through the NIH that deliberately fund research focused on achieving equity. The Transformative Research to Address Health Disparities and Advance Health Equity initiative carries $58 million in funding from the NIH Common Fund, and, in 2021, awarded 11 innovative grants that addressed health equity.31 The recent UNITE initiative strives to end structural racism, diversify the biomedical research workforce, and center minority health research funding in a direct response to a January 2021 Executive Order from the Biden Administration to advance racial equity.32

Insurance Marketplace

Insurance barriers that contribute to health disparities within gynecologic oncology include the nonexpansion of Medicaid in nine states, unequal coverage benefits under Medicare and private insurance plans, unequal access to specialists and NCI-designated cancer centers, escalating specialty drug costs and reimbursement practices, and financial toxicity.33,34 Through the Patient Protection and Affordable Care Act, Medicaid expansion helped provide insurance coverage for more than 20 million people.35 For patients with gynecologic cancers, Medicaid expansion is associated with more timely treatment and surgery, increases in early-stage diagnosis, and improved postoperative morbidity and mortality.36,37 The states that have not expanded Medicaid include Alabama, Florida, Georgia, Kansas, Mississippi, South Carolina, Tennessee, Texas, and Wyoming.38 This leaves more than 2.1 million uninsured people in these states who are not poor enough to qualify for the state-based Medicaid program but would otherwise qualify if their state adopted the federal expansion.39 For example, in Alabama, a state that is 35% Black, to qualify for the state Medicaid program, parents must earn less than 18% of the federal poverty level ($4,145 for a family of three annually). In addition, adults without dependent children are not eligible for Medicaid.

Further harms for people with low incomes include work requirements as a condition of Medicaid eligibility. These mandates have been shown to be politically driven barriers with racist roots that may lead to worse outcomes among marginalized individuals.40 For example, working people in Arkansas lost coverage in 2018 due to failure to report their jobs: there was a 6% drop in insurance coverage for people aged 30–49 years, people were not able to report their work due to a dysfunctional online-reporting system, and, ultimately, there was no change in employment and community engagement.41 Conversely, Medicaid expansion in Montana led to a significant 6-percentage-point increase in labor force participation among nondisabled individuals with low incomes aged 18–64 years.42

COMMUNITY

At the community level, interventions that can achieve racial equity in gynecologic oncology include reciprocal collaboration between health systems and community organizations, implementing outreach clinical practices, and funding programs addressing social determinants of health.

Environmental, neighborhood, and socioeconomic factors contribute to delays in diagnosis and more advanced-stage disease that disproportionately affect minoritized patients with gynecologic cancers.43,44 Since 2012, all NCI-designated cancer centers are required to incorporate community outreach and engagement across all programming.45 Specific funding supplements exist to encourage the development of community outreach and engagement programs across cancer centers, and programs have leveraged this funding to deepen community partnerships.46

To address social determinants of health, a multisector approach is necessary.47 The most successful interventions that have closed, and in some cases eliminated, racial disparities required multi-year, multi-level efforts. For example, the Delaware Cancer Consortium, with a tremendous amount of political will, secured statewide funding to cover the following: reimbursement for colonoscopies for uninsured residents with incomes up to 250% of the federal poverty level, 2 years of cancer care for uninsured residents with incomes up to 650% of the federal poverty level, and implementation of aggressive outreach, community partnerships, marketing campaigns, and care navigation for colorectal cancer with a focus on the Black community. Within 7 years, the Black–White disparities in screening and incidence of colorectal cancer were eliminated and the disparity in mortality was significantly narrowed.48

ORGANIZATIONAL

At the organizational level, solutions to achieve equity within gynecologic oncology include implementing care-navigator programs and medical–legal partnerships, collecting data for assessing equity, leveraging clinical decision–support systems, and diversifying clinical trials. Within this level, we include care team education and accountability regarding inclusive language and consideration of an equity checklist at clinic visits.

Patient Navigation

Patient-navigation programs are designed to help patients navigate the complex health care system, overcome barriers to care, and access appropriate resources and services (Fig. 3).49 In doing so, care navigators reduce disparities in timely cancer care.50,51 Women who use navigation services have fewer missed colposcopy appointments than those who do not receive navigation services.52 They are more likely to complete Pap tests compared with those who do not receive navigation services (70% vs 11% in a New York City study and 33% vs 10% in a Missouri study).53,54 In a secondary analysis of data from the NCI Patient Navigation Research program, researchers studied the effects of care navigators on delays in care from an abnormal screening test result for breast, cervical, colorectal, or prostate cancer to diagnostic resolution and treatment. They found that the implementation of a care-navigator program eliminated disparities by housing type, employment status, and marital status.55 For patients with cervical cancer, a care-navigator program improved initiation rates of radiation therapy, use of appropriate chemotherapy, and rates of timely completion of radiation and was associated with significantly improved survival.56 Care-navigator programs can also be cost effective, saving one health system more than $19 million annually.57

F3
Fig. 3.:
Care Navigator Framework within women's health.49 Reprinted from McKenney KM, Martinez NG, Yee LM. Patient navigation across the spectrum of women's health care in the United States. Am J Obstet Gynecol 2018;218:280–6. doi: 10.1016/j.ajog.2017.08.009. Copyright 2018, with permission from Elsevier.

Medical–legal partnerships can also serve a role in patient support and addressing racial equity.58 For example, Roswell Park Cancer Institute founded a medical–legal partnership, called the Legal Services Program, under a local legal services agency.59 Initially directed toward patients at the end of life and then broadened to all patients with recurrent cancer, this program was staffed by a social worker and an attorney. Between 2004 and 2007, 194 patients were referred to the program. Most services involved custody planning, guardianships, benefits advocacy, estate planning, and advance care planning. Beyond helping to secure stable housing, insurance, and hospice services for patients, the program allowed the hospital to recoup, at no costs to patients, more than $900,000 for what would have been uncompensated care.

Organizational Quality-Improvement Data for Equity

There have been significant improvements in standardizing race and ethnicity data since the foundational Institute of Medicine report, “Race, Ethnicity and Language Data: Standardization for Health Care Quality Improvement.”60 However, granular data on social risk factors still are not standardized. Capturing financial strain, stress, depression, social ties, intimate partner violence, and current residential neighborhood poverty may help institutions identify opportunities to target interventions to achieve equity in the care-delivery system. Calls have been made to consider the routine screening of all patients for social determinants of health, leveraging the electronic medical record system to capture social needs.61 Social needs screening has been implemented successfully within gynecologic practices and demonstrates a significant opportunity for intervention.62,63 These interventions can be in the form of the Health LEADS model, in which patients are screened, referred to social resources, and followed up to ensure successful resolution of their identified need.64

Equity-Based Clinical Decision–Support Tools

Adaptation of equity-based clinical decision–support tools has the potential to eliminate disparity by standardizing practices. Integrated into electronic medical records, these systems increase adherence to guidelines for prevention and treatment of disease and offer screening for the most vulnerable patients.65–67 For example, a mandatory clinical decision–support tool eliminated racial disparities in best practice venous thromboembolism prophylaxis between Black and White patients admitted to a surgical trauma service (from 70.1% vs 56.6% to 84.5% vs 85.5%).68 The Centers for Disease Control and Prevention is developing a computer-based clinical decision–support tool for cervical cancer screening and management, with a goal of providing the latest guidelines in a useable format to clinicians.69 With the rapidly accelerating data and guidelines surrounding the adjuvant management of endometrial cancer based on molecular features, clinical decision–support tools hold significant potential for helping patients and clinicians navigate these nuanced decisions.

Racial Equity in Clinical Trial Enrollment

Black patients remain systematically understudied in clinical trials.70 In a recent study on the role of immunotherapy to treat advanced or recurrent endometrial cancer, only 3.7% (31/827) of study participants were Black. This was a global trial, and there were no study sites in Africa.71

The American Society of Clinical Oncology and the Association of Community Cancer Centers have partnered to create online resources to help clinical researchers leverage evidence-based strategies to improve equity in clinical trial design and enrollment. These can be found at asco.org/asco-accc. Site visits have been performed at institutions that applied to be part of the pilot study on self-assessment, with 63% reporting successful identification of strategies to increase diversity in clinical trial enrolment.72 Ensuring that patient voice is central to clinical trial design is a necessary step in achieving racial equity.73,74 Within gynecologic oncology, the patient-oriented trial design has yet to fully materialize.75,76

Clinician-Level Interventions

A fundamental reorientation to an understanding of systemic racism is necessary to recognize drivers of suboptimal survival for Black patients.77 Integrating equity competencies for clinicians into each patient-care encounter has been suggested as a potential opportunity for intervention.16 This includes eliminating stigmatizing language within the patient medical record that otherwise perpetuates bias and inequitable care.78,79 Intentional, unbiased language within gynecology is particularly important as we strive for reproductive justice.80 We suggest the adoption of “equity checklists” that may help to ensure that every patient encounter includes a thorough consideration of social determinants of health, minimizes clinician bias, and standardizes appropriate referrals and clinical management (Box 1). At Yale, an equity checklist was systematically incorporated into gynecologic quality and safety reviews, and investigators found nearly half of preventable adverse events could be attributed to the effects of bias, racism, and social determinants of health.81 Consideration of incorporating the Everyday Discrimination Scale—a validated survey to measure exposure to microaggressions—to the patient encounter adds yet another level of understanding from which clinicians may gain insight into the risk that racism poses to minoritized patients.82,83

Box 1.

Clinician Competencies and Equity Checklist

  1. A. Clinician competencies
    1. Am I aware of the disparities that exist in the incidence and mortality rates of this gynecologic cancer that may affect this patient?
    2. Have I taken the time to learn about the cultural, social, and economic factors that may affect the health outcomes of this patient?
    3. Am I using patient-centered language that is culturally sensitive and respectful when communicating with this patient?
    4. Have I discussed all treatment options, including clinical trials, with this patient and provided them with the necessary information to make informed decisions?
    5. Have I considered the effect of social determinants of health, such as housing, employment, and access to healthy food, on the health outcomes of this patient?
    6. Have I ensured that this patient has access to adequate health care resources, including specialist referrals, support groups, and counseling services?
    7. Have I worked with this patient to develop a treatment plan that is personalized to their needs, preferences, and values?
    8. Have I created a safe and welcoming environment that is free from discrimination, racism, and bias for this patient?
  2. B. Health Equity Checklist
    • Genetic or molecular sequencing
    • Palliative care referral
    • Social needs screening
    • Everyday Discrimination Scale
    • Legal needs screening
    • Care navigator referral
    • Eligibility for clinical trial
    • Vaginal brachytherapy plan for patients with cervical cancer
    • Documentation of reasoning for deviation from standard of care

INTERPERSONAL

At the interpersonal level, interventions with the potential to alleviate inequity within gynecologic oncology include reciprocal partnership with patient-advocacy groups and faith-based organizations to improve social support.

Although all cancer survivors face significant levels of anxiety, depression, and stress, these disproportionately affect Black women.84 The role of social support and social attachment is associated with improved health outcomes and cancer survival.85 Patient-advocacy groups can form community and encourage agency in survivorship. ECANA (the Endometrial Cancer Action Network for African Americans) provides a platform for and by Black women with endometrial cancer and is one such example of a patient-led organization.86 The multisite SISTER (Social Interventions for Support During Treatment for Endometrial Cancer and Recurrence) study, developed through patient-stakeholder assessment,87 randomizes Black endometrial cancer survivors to various forms of social support—enhanced standard of care, one-on-one peer support, and group peer support.88 Partnerships with faith-based organizations also represent opportunities to build awareness, social support, and research infrastructure.89,90 This has been successfully piloted in Project CHURCH (Creating a Higher Understanding of Cancer Research and Community Health), a partnership between MD Anderson Cancer Center and local Houston-based churches.91 Through this partnership, a large cohort study is accruing, care-navigator programs have been instituted, and research mentorship and patient engagement have all increased.

INDIVIDUAL

Finally, at the individual level, solutions that can be piloted by clinicians and academicians to address equity within gynecologic oncology include the creation and intentional dissemination of patient-education materials designed to reach the most vulnerable patients in the context of historical disenfranchisement.

For both Black and White women, delayed diagnosis in endometrial cancer involves a lack of knowledge about menopause, negative health care experiences, and inadequate physician response.92,93 Increasing awareness can be accomplished through media campaigns94 and community-education programs.95 The Society of Gynecologic Oncology and the Foundation for Women's Cancer have partnered on a social medial campaign—Move the Message—to help spread awareness of gynecologic cancers and provide patient information (https://foundationforwomenscancer.org/get-involved/move-the-message/). In a gynecologic cancer education campaign, simple education videos helped to increase the percentage of women who correctly identified that human papillomavirus (HPV) causes vaginal cancer (39–65%) and vulvar cancer (26–60%).96 More women were also able to correctly identify the recommended age groups for the HPV vaccine (15%–30%) and that the Pap test screens for cervical cancer (58–73%). The PALS (Patient Activated Learning System) platform has been leveraged to develop educational videos on HPV, Pap tests, and colposcopies.97 Development of similar content addressing gynecologic topics such as abnormal uterine bleeding, bloating, and early satiety; understanding family history; and basic management of gynecologic cancers is needed.

CONCLUSIONS

Promoting health equity in the treatment of patients with gynecologic malignancies requires a multifaceted approach that addresses every level of the socioecologic model. This requires a fundamental reorientation of disparities research priorities to move into the intervention space rather than description of disparities.98 These priorities must acknowledge the role that structural and interpersonal racism has had in defining the historical boundaries of our research infrastructure and health systems. Leaders from the American Association for Cancer Research, the American Society of Clinical Oncology, the NCI, and the American Cancer Society have created a foundational list of recommendations to achieve these research goals.99

Raising awareness to build empathy and reduce racial prejudice ideologies and stereotypes that form the basis of health and social policy is foundational to building political will in funding these longitudinal, multi-level interventions.100 By developing novel interventions and tailoring established solutions to our unique population of patients with or at risk for developing gynecologic cancers, we can eliminate disparities in gynecologic oncology care and patient outcomes. We have documented the inequity time and time again. It's time we acted.

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