Advancing the Science of Implementation for Resource-Limited Settings through Bidirectional Learning Around Cervical Cancer Screening

Abstract

In 2020, the highest rates of cervical cancer incidence and mortality were reported in Asian and African regions of the world. Across the globe, growing evidence confirms cancer disparities among racial and ethnic minorities, low socioeconomic status groups, sexual and gender minorities, uninsured individuals, and rural residents. Recognition of these stark disparities has led to increased global efforts for improving screening rates overall and, in medically underserved populations, highlighting the urgent need for research to inform the successful implementation of cervical cancer screening. Implementation science, defined as the study of methods to promote the integration of research evidence into health care practice, is well-suited to address this challenge. With a multilevel, implementation focus, we present key research directions that can help address cancer disparities in resource-limited settings. First, we describe several global feasibility studies that acknowledge the effectiveness of self-sampling as a strategy to improve screening coverage. Second, we highlight Project ECHO as a strategy to improve providers’ knowledge through an extended virtual learning community, thereby building capacity for health care settings to deliver screening. Third, we consider community health workers, who are a cornerstone of implementing public health interventions in global communities. Finally, we see tremendous learning opportunities that use contextually relevant strategies to advance the science of community engagement and adaptations that could further enhance the uptake of screening in resource-limited settings. These opportunities provide future directions for bidirectional exchange of knowledge between local and global resource-limited settings to advance implementation science and address disparities.

Introduction

The Asian and African regions of the world continue to report the highest cervical cancer incidence and mortality.1 The global recognition of these disparities and the growing evidence base around cervical cancer prevention has contributed to the World Health Organization’s (WHO) agenda for elimination of cervical cancer as a public health problem.2 This initiative, while important in promoting the adoption of evidence-based interventions (ie, vaccination, screening, and treatment), further highlights the urgent need for research to inform the successful implementation of cervical cancer screening. In a recent commentary, a WHO working group suggested the importance of implementation research with a specific focus on broadening stakeholder engagement, focusing on equity in reach and navigation throughout the continuum of care, and improving the readiness of health systems to increase adoption, implementation, scale-up, and sustainability of cervical cancer screening programs.3 In parallel to these foci, we highlight key research advances within the field of rural and resource-limited settings that could contribute toward enhancing the science of implementation around global cervical cancer screening efforts.

Throughout the world, cervical cancer continues to disproportionately affect individuals from racial and ethnic minorities, low socioeconomic status groups, rural residents, and those who lack access to screening, medical and oncology service.4,5 Biomedical research has resulted in a robust evidence base for the WHO-recommended interventions for cervical cancer. However, there continues to be a persistent underinvestment in cancer prevention and a failure to ensure that all population subgroups benefit from access to care, including diagnostics and treatment. Implementing cancer screening programs for populations requires the consideration of a series of steps beyond initial testing. Some of these steps may include screening and treatment approaches, further testing for diagnosis confirmation, and ensuring timely and adequate treatment for the screen-positives and re-testing for screen-negatives, as outlined in the WHO recommendations. Social, behavioral and health services research provides evidence that cancer screening efforts, including implementation and uptake, are affected by individual- and system-level contextual factors, such as economic status, place of residence, as well as health care facility resources and personnel. Implementation research, defined as the study of methods to promote the integration of research evidence into health care policy and practice, is well-suited to address this challenge.6

As a field of scientific study, implementation research is focused on: understanding the multilevel health care context; identifying strategies to help adopt, implement, and sustain interventions in health care; consider implementation outcomes (ie, acceptability, appropriateness, and feasibility, among others); along with effectiveness outcomes. Applied to cancer screening, an implementation research agenda can help ensure considerations across the cancer continuum (ie, screening, diagnostics, and treatment), target multiple ecological levels to promote implementation effectiveness of cancer screening programs, and make certain that key social and behavioral attributes of marginalized populations are incorporated into programming. As shown in Figure 1, we highlight key research directions, supported by evidence from resource-limited settings within a rural context for promoting the WHO cervical cancer elimination agenda, thereby urging bidirectional learning on promising implementation strategies from the global north and the global south.

Figure 1. Key research directions for advancing global implementation science around cervical cancer screening.

Improving Reach and Reducing Structural Barriers using Self-collected Samples for Screening

We acknowledge global feasibility studies that have created a substantial evidence base of effectiveness around using self-collected samples for cervical cancer screening. In resource-limited settings, self-sampling was perceived to be easy, painless, less embarrassing, and in some cases preferred over provider-sampling.7 Feasibility studies conducted in rural India for cervical cancer screening using home-based HPV self-sampling showed high screening compliance with reduced operational problems.8 In much of sub-Saharan Africa, screening uptake of Pap smear and visual inspection has remained low despite high willingness of women to screen, demonstrating the importance of addressing environmental constraints. HPV DNA-based testing, which offers the options for self-sampling, can shift screening from clinical to community settings thereby addressing environmental barriers to screening.9

This growing evidence for self-sampling from low- and middle-income countries (LMICs) is substantial and an important contribution toward elimination efforts across the globe, especially in the post-pandemic world.10 The recently launched “Last Mile” initiative, which is a public-private partnership, aims to validate self-sampling as a comparable, non-inferior alternative to provider-collected samples and seeks to receive regulatory approvals in the United States.11 Despite the growing interest and evidence surrounding self-sampling as a strategy to increase screening uptake,12 its implementation in resource-limited settings has been sub-optimal. With increasing evidence pointing toward the cost-effectiveness of this strategy when considering population impact,13 implementation studies, which evaluate ways in which delivery of such a strategy could be incorporated into routine services for resource-limited primary health care settings, are scarce. There is an immediate need to invest in research that is aimed at understanding how self-collected samples can be incorporated into routine clinical workflows in resource-limited health care settings, thereby reducing the burden for primary health care services and the patient.

As our global society emerges from the COVID-19 pandemic, approaches that reduce clinic visits, allow for screening outside the clinical environment, and utilize fewer clinical resources will be needed and have since gained broader acceptance.14 Self-sampling approaches can also be critical tools that improve uptake among individuals from medically underserved communities. Investing in implementation research for resource-limited settings, which serve low socioeconomic and racial/ethnic minority populations, can further contribute toward a health equity-oriented research agenda globally.15

Building Workforce Capacity using Project ECHO^® (Extension for Community Healthcare Outcomes) as a Strategy to Reach and Train Providers

Building workforce capacity to deliver cervical cancer screening services remains a challenge globally,16-18 where only a limited number of physicians and nurses are appropriately trained to provide primary health care in rural and other medically underserved areas. Limited access to academic public health and medicine further reduces the ability of this workforce to develop or improve the competencies needed to deliver cancer prevention services in an effective and efficient manner. Here, we describe one program working to address these issues.

Project ECHO is a digital mentoring platform designed to increase capacity and improve providers’ knowledge.16 Proven effective in India, Project ECHO makes knowledge accessible for health care stakeholders.19 In response to the COVID-19 pandemic, such digital platforms to connect, coordinate, and overcome barriers to care have become essential. The ECHO model has been especially important in cancer control initiatives by bringing together experts and practitioners to promote implementation capacity.20 In India, the National Institute of Cancer Prevention supports a program that aims to reach and train gynecologists, primary care physicians, nurses, and community health workers to support the implementation of a national, population-based cancer screening program. Their goals are to increase clinical capacity in low-resource settings by empowering health care providers in medically underserved areas to screen and treat patients in their own communities, thereby reducing referrals. Studies from India have shown that Project ECHO is an effective tool to develop skills, confidence, and knowledge and contribute to building capacity for health care settings to deliver screening to address global disparities in health care access.19

The global reach of this strategy exemplifies the bidirectional learning needed for advancing global implementation science. Focused on cervical cancer screening, Project ECHO has been used to connect providers in medically underserved areas of Texas, including the Texas-Mexico border, with specialists at academic health centers such as MD Anderson to discuss follow-up of cases for patients who have abnormal cervical cancer screening tests.21,22 Additional programs based on this model have been developed and implemented in Africa including a program in Cameroon, Mozambique and Nepal. The potential for Project ECHO to truly contribute to implementation of cancer screening services in health care settings, however, remains under-explored.23 There is an immediate need to evaluate existing ECHO programs and examine how and when the ECHO programs contribute to supporting care delivery and what impact the program has on population outcomes. Combined with recent advances in health care apps24 and virtual visits,25 additional telehealth opportunities could also contribute toward building capacity by task-shifting to health workers who assist or conduct screening interventions in rural settings.

Community Health Workers: Helping Patients Navigate Health Care Systems to Access Cervical Cancer Screening

Community health workers (CHWs) are an important cornerstone for implementing public health interventions in global communities.26,27 To implement cervical screening efforts, CHWs serve in many roles, including: educating the community members about cancer prevention and navigating patients through the screening process from their homes or other community spaces to the health care system.28 In public health systems across the globe, CHWs form an important interface between the community and the health care system. In many cases, CHWs live in the community they serve and, therefore, they are familiar with the social and cultural practices of members in the community. Often, they are the first to be sought out for any health-related concerns among the medically underserved populations. In Africa, CHWs have been key to delivering maternal and child health, TB, HIV/AIDS, and malaria services, to name a few.29 Considering the fact that population-based cancer screening is primarily targeting asymptomatic individuals, the CHW’s ability to engage with the community can be leveraged for increased community awareness, screening coverage, and ultimately improved navigation across the continuum.27 In fact, there is growing evidence from African30,31 and Asian countries32 on the success of task-shifting from physicians to CHWs as a potentially effective and affordable strategy for improving access to health care.33

An important gap or challenge to the implementation of cervical cancer screening with self-sampling is the follow-up of women to share results and refer for further diagnostic testing, if needed.7 This demonstrated loss-to-follow-up has at times been cited as an argument against HPV testing and in favor of “screen-and-treat” approaches with other screening methods. CHWs can be an important player in the notification and tracking of women post-screening to ensure linkage to follow-up testing and services. A systematic review of the CHW’s role in cervical cancer screening in LMICs found that CHWs have been underutilized for follow-up, while they are most commonly involved in community education and awareness raising efforts.28 Another strategy has been to use Project ECHO in combination with patient navigators to provide community outreach and education, as well as to provide navigation services for women in need of screening and follow-up in clinical settings. This comprehensive or multi-level intervention was effective in increasing cervical cancer screening, diagnosis, and treatment for women in clinics near the Texas-Mexico Border.22

Contributions to and from the Science of Engagement and Health Equity

Finally, and most importantly, we see tremendous bidirectional learning opportunities for the science of community and partnership engagement that is rooted within the Global North and primarily emerges from an understanding of the implementation of interventions, often in well-resourced settings. We believe that developing such a scientific base equivalently across the globe could inform an in-depth understanding of disparities in screening uptake and begin to move toward an equity-orientation (ie, addressing the disparities for improving screening uptake). This will require being knowledgeable of Community-Based Participatory Research (CBPR) approaches, which aim to: recognize the community; build on the assets within the community; facilitate a collaborative and equitable partnership in all phases of research; foster co-learning and capacity building; achieve a balance between knowledge generation and intervention for the mutual benefit of partners; focus on the local relevance of public health problems; engage in an iterative process; disseminate results; address issues of social determinants of health; and commit to a long-term process toward sustainability.34

Using a CBPR approach can be beneficial for both the communities served in resource-limited settings and the providers involved in the implementation. To achieve effective and efficient implementation, both deliverers and recipients of the intervention have to perceive interventions and strategies used to implement these interventions, as acceptable, appropriate, and feasible.6 Engaging with the recipients and deliverers also provides the opportunity to examine intervention and implementation strategies (ie, methods or techniques used to implement interventions, such as those mentioned in this article) to describe the core components that lead to implementation outcomes and therefore population health outcomes.6 We note here that the specific strategies shared in this article are not stand-alone strategies or isolated from each other; instead, we believe that they must be used synergistically and in combination, keeping the implementation context at the forefront.

Conclusion

The path to achieving population-level benefit from existing evidence-based interventions, such as cervical cancer screening, is clear only if we are to see it through an implementation research perspective, and address complexities associated with screening in resource-limited settings across the globe. To achieve these goals, we will need to accelerate the bidirectional exchange of information, innovations, and lessons learned as we gain a deeper understanding of context surrounding resource-limited settings, begin to examine the implementation of screening as a process that includes not just the screening test but also ensures follow-up, and the sustainability of implementation efforts. We hope that the growing emphasis on studying the implementation of evidence-based interventions will inform next steps for cancer prevention and care as we continue to emerge from the global COVID-19 pandemic.