Building Capacity for Cervical Cancer Prevention in U.S.-Affiliated Pacific Islands: The Pacific Against Cervical Cancer Project

Abstract

The U.S.-affiliated Pacific Islands (USAPI) have higher cervical cancer incidence and mortality rates and lower screening coverage compared with the United States. This is likely because of economic, geographical, health care delivery, and cultural barriers for women living in these resource‐constrained, isolated regions. The most recent U.S. and World Health Organization cervical cancer screening guidelines recommended primary human papillomavirus (HPV) testing as one screening option or the preferred screening modality. Primary HPV screening-based strategies offer several advantages over current screening methods in the USAPI. However, adoption of this newer screening modality has been slow in the United States and not yet incorporated into USAPI screening programs. The U.S. Centers for Disease Control and Prevention and partners initiated the Pacific Against Cervical Cancer (PACe) project in 2019 to evaluate the feasibility, acceptability, and cost‐effectiveness of primary HPV testing-based strategies in Guam and in Yap, Federated States of Micronesia. This report provides an overview of the PACe project and outlines the approaches we took in implementing primary HPV testing as a new cervical cancer screening strategy (including the option of self-sampling in Yap), encompassing four core components: (1) community engagement and education, (2) medical and laboratory capacity building, (3) health information and system improvement, and (4) modeling and cost-effectiveness analysis. The PACe project provides examples of systematic implementation and resource appropriate technologies to the USAPI, with broader implications for never screened and under-screened populations in the United States and Pacific as they face similar barriers to accessing cervical cancer screening services.

Introduction

Cervical cancer burden and disparities in the U.S.-affiliated Pacific Islands

The U.S.-affiliated Pacific Islands (USAPI) comprise six jurisdictions, including three U.S. flag territories (American Samoa, Guam, and the Commonwealth of the Northern Mariana Islands) and three freely associated states (Republic of the Marshall Islands, Republic of Palau, and the Federated States of Micronesia, FSM, composed of four states: Yap, Pohnpei, Kosrae, and Chuuk). The USAPI encompass an extensive geographic area with diverse cultures, languages, and socioeconomic and political contexts.

Cervical cancer was the third leading cause of new cancer cases among females in the USAPI during 2007–2020.¹ The cervical cancer age-standardized incidence rate was 16.7 per 100,000 women in the USAPI compared with 7.8 per 100,000 in the United States during 2007–2020.¹ A higher proportion of cervical cancer cases in the USAPI were diagnosed at a later stage where prognosis is poor. In FSM, over 70% of cervical cancers were diagnosed at a late stage compared with 15% in the United States, and only 46% of these women were alive within 5 years of the diagnosis compared with 67% in the United States.^1,2

Cervical cancer is preventable through human papillomavirus (HPV) vaccination, cervical cancer screening, and appropriate follow-up after abnormal screening results. However, screening uptake in the USAPI is low. The estimated proportion of women aged 21–65 years who were not up to date with cervical cancer screening ranged from 29% to 71% among USAPI,³ compared with 15% in the United States.⁴

The lower cervical cancer screening coverage in the USAPI is likely associated with various economic, geographic, and cultural barriers.^5,6 Health care barriers include a shortage of trained medical and public health workforce personnel, limited laboratory infrastructure, a lack of medical equipment and supplies, and ineffectual health information systems. Many women in the USAPI live in geographically isolated atolls and islands, rendering access to timely screening and follow-up services a major challenge. The awareness and acceptance of emerging cervical cancer screening methods and technologies among health care providers are low.⁷ Stigma associated with HPV being a sexually transmitted infection and fear of pelvic examination are common (personal communication with local partners).

Current U.S. and World Health Organization cervical cancer screening recommendations

The USAPI have been using various cervical cancer screening methods including cytology, cotesting (cytology in conjunction with HPV testing), and visual inspection with acetic acid (VIA). Cervical cancer screening guidelines and technology have evolved rapidly in the past decade, transitioning to HPV testing as a stand-alone screening modality (primary HPV testing). In 2018, the U.S. Preventive Services Task Force (USPSTF) recommended the use of primary HPV testing as one of the three cervical cancer screening strategies for women aged 30–65 years.⁸ The 2020 American Cancer Society guideline recommended primary HPV testing as the preferred screening method,⁹ and the American College of Obstetricians and Gynecologists endorsed primary HPV testing in 2021.¹⁰ The World Health Organization (WHO) launched the global strategy toward eliminating cervical cancer as a public health problem in 2021 and updated screening and treatment guidelines recommending HPV testing as the primary screening test.¹¹

The WHO’s Cervical Cancer Elimination global strategy includes three targets by 2030: 90% HPV vaccination coverage of eligible girls, 70% screening coverage with a high-performance test, and 90% of women with a positive screening test or a cervical lesion managed appropriately.¹² In addition, the WHO guidelines suggest that HPV testing samples can be either taken by a health care provider or self-collected by women. Self-sampling for HPV testing has been shown to be feasible, acceptable, and cost-effective in reaching never screened and under-screened populations in both low- and high-resource settings,^13–18 and it is now universally available in certain high-income countries (e.g., Australia). On May 15, 2024, the U.S. Food and Drug Administration (FDA) approved the use of self-collected vaginal specimens for HPV testing in health care settings.⁴⁰

Pacific Against Cervical Cancer Project

In 2019, the U.S. Centers for Disease Control and Prevention (CDC) and partners initiated the Pacific Against Cervical Cancer (PACe) project to establish a sustainable infrastructure to promote cervical cancer screening and management in the USAPI. Primary HPV screening had not been routinely used in the USAPI before the PACe project. In conjunction with the local departments of Health and local health system partners, the PACe project aims to improve evidence-based cervical cancer screening programs using current screening and management guidelines and to evaluate the feasibility, acceptability, and cost‐effectiveness of primary HPV screening-based strategies. In this report, we provide an overview of the PACe project conceptual model and its multifaceted strategies. Activities described here are expected to be completed by December 2024.

The PACe project identified two pilot sites, Guam and Yap, FSM. Guam is a U.S. territory and follows U.S. clinical guidelines, FDA regulatory requirements regarding medical device utilization and laboratory testing, and the reimbursement policies from the Centers for Medicare and Medicaid Services for those covered by U.S. public insurance or programs. Guam has a complex health network system with many stakeholders in cervical cancer screening, including public, private, and nonprofit organizations. As a freely associated sovereign nation, FSM can choose any of the existing cervical cancer screening and management strategies—including those from the WHO guidelines, which are appropriate and sustainable for low-resource settings. Yap has a centralized health system, and the Yap State Department of Health Services manages public health programs and the community health centers. The CDC-funded National Breast and Cervical Cancer Early Detection Program provides access to USPSTF-recommended breast and cervical cancer screening and diagnostic services among eligible low-income and uninsured residents in all USAPI jurisdictions, except for the FSM that does not currently participate in this program.

The PACe project is a multiyear effort through partnerships between the CDC Division of Cancer Prevention and Control, Pacific Island Health Officers’ Association, subject matter experts, and local partners in Yap and Guam. Each jurisdiction established Community Advisory Boards (CABs) consisting of local stakeholders who regularly meet with the project team. The team members have also conducted several site visits to Guam and Yap to build partnerships, conduct readiness assessments, and provide technical support and capacity building.

Overall Approach

The PACe project has four key interconnected components: (1) community engagement and education, (2) medical and laboratory capacity building, (3) health information and system improvement, and (4) modeling and cost-effectiveness analysis. The PACe team recognized the importance of building capacity in each component to facilitate the implementation of primary HPV testing-based screening and management strategies. We convened a multidisciplinary group of experts in areas including behavioral science, medical and laboratory protocols, and modeling and cost-effectiveness analysis. These experts also have experience in improving cervical cancer prevention and control programs in low-resource settings.

To facilitate project planning, communication, and evaluation, a logic model was developed (Fig. 1) and tailored for each jurisdiction. This model links PACe program inputs and activities to program outcomes and ultimately to the desired outcomes and goals. Inputs include resources that support the program; outputs include activities in four core components as well as the project’s expected impact. The following sections describe approaches of each of the four core components and how the approaches were adapted because of the unique challenges in each jurisdiction.

FIG. 1.

PACe project logic model. CDC, Centers for Disease Control and Prevention; DOI, Department of the Interior; HPV, human papillomavirus; PACe, Pacific Against Cervical Cancer.

1. Community Engagement and Education

Full engagement was critical to assure both a participatory decision-making process and sustainability. Thus, the first step was to establish CABs in both jurisdictions with broad representation from the health care system (including health care providers, administrators, and support staff), advocates, and representatives from the targeted communities. The structure and functioning of each CAB differ slightly in each jurisdiction. In Yap, the health care system and co-implementers of the identified strategies are well represented on the CAB with lower representation of advocates. In Guam, there is greater representation of nonprofit organizations (e.g., American Cancer Society), the research/academic sector (University of Guam), and various sub-populations, in addition to the health department. In both jurisdictions, the CABs are actively involved in all decisions on program implementation and evaluation.

In Yap, investigators conducted focus groups with women in different communities and engaged different stakeholders in informal conversations about barriers, facilitators, and solutions to promote cervical cancer screening using primary HPV testing and the option of self-sampling. The PEN-3 and Health Belief Model guided these assessments.^19–23 Owing to the COVID-19 pandemic, implementing extensive formative assessments in Guam was not possible. Thus, most of the formative work was done through informal conversations with CAB members, women’s groups, and other nonprofit organizations. The obtained information was discussed with the CABs, and all involved participants jointly drafted intervention objectives and strategies based on the findings and theoretical constructs (Supplementary Appendix Table SA1).

The formative assessments and discussions with CAB members informed the development of the educational materials, assuring that they are culturally relevant to the different jurisdictions and translated to different languages. In addition to the targeted messages that were grounded in the PEN-3 and Health Belief Model, investigators worked with a professional designer to create images that resonated with the diverse target audiences.

Capacity building of community health workers and volunteers

Health care systems in both jurisdictions have existing community health workers (CHWs) who are trained to disseminate information and health education and serve as a link between the community and the health care system. In Yap, there are also health assistants in the outer islands who can provide basic health services. In Guam, health advocates, representing different communities, were willing to be involved. However, the CHWs, health assistants, and volunteers had not received training on promoting behavior change and tailoring their strategies to motivate women to get screened. Thus, investigators made minor adaptations to an existing evidence-based CHW capacity-building program that has been successfully implemented in a variety of low-resource settings in the context of cancer prevention and control.^{13,15,24–26}

Capacity building focused on acquiring knowledge and skills according to the 12 principles of adult learning proposed by Vella,²⁷ which involves different learning strategies and an emphasis on practicing learned skills. Approximately 80% of the training focused on behavioral and community engagement strategies to promote behavior change.²⁸ In Guam, CHWs and volunteers trained together for the first 16 hours and then divided into groups to focus on the relevant skills for their roles. For instance, volunteers have a primary role of community mobilization and engagement, and CHWs have the additional role of navigating women through screening and follow-up. With support from Guam’s public health system, investigators were able to leverage their infrastructure by training CHWs who work in non-cancer-related health promotion efforts (e.g., diabetes education, COVID-19 vaccination). These CHWs were able to integrate cervical cancer prevention and control education and screening referrals in their efforts.

The approach to capacity building in Yap was slightly different as the CAB emphasized the train-the-trainer approach, whereby health care professionals were trained to continue training CHWs and health assistants. The capacity building for these trainers had three components: (1) mastering principles of adult education, basic learning, new competency development, supervisory skills, and so on; (2) modeling, whereby trainers first observed investigators training the CHWs; and (3) implementation, whereby trainers implemented the training of CHWs with immediate feedback from investigators.

2. Medical and Laboratory Capacity Building

The current medical and laboratory capacity in Yap and Guam would make it challenging to reach the WHO cervical cancer elimination targets by 2030. The PACe project presented an opportunity to build infrastructure and capacity for primary HPV testing-based screening and management strategies, which have the potential to improve screening coverage and follow-up. The PACe team also applied and received additional funding from the Department of the Interior for supporting direct clinical encounters, HPV lab testing, and obtaining lab equipment and supplies.

Yap: Rapid introduction of HPV testing and thermal ablation

In 2009, Yap adopted a screen-and-treat approach using VIA and cryotherapy for women aged 30–50 years. The FSM Comprehensive Cancer Control plan previously aimed for 28% cervical cancer screening coverage using VIA/Pap.²⁹ In response to the global elimination efforts, Yap prioritized HPV testing for 70% of eligible women, which will result in screening at least 1,680 women by 2030. With support from the PACe project, Yap adopted the WHO’s 2021 screening recommendations, incorporating self- and provider-sample collection for HPV testing and using a screen, triage, and treat algorithm on the main island (Fig. 2) and a screen and treat algorithm in neighboring islands (Fig. 3).

FIG. 2.

Screen, triage, and treat algorithm for the main island, Yap. Ablation, thermal ablation; AIS, adenocarcinoma in situ; CIN, cervical intraepithelial neoplasia; colp+/−biopsy, colposcopy with or without biopsy; FU, follow-up; HPV, human papillomavirus; hrHPV, high-risk HPV; LLETZ/LEEP, large loop excision of the transformation zone/loop electrosurgical excision procedure; VAT, visual assessment for treatment; VIA, visual inspection with acetic acid.

FIG. 3.

Screen and treat algorithm for neighboring islands, Yap. Ablation, thermal ablation; FU, follow-up; HPV, human papillomavirus; hrHPV, high-risk HPV; VAT, visual assessment for treatment (eligibility); VIA, visual inspection with acetic acid.

PACe aims to (1) implement primary HPV testing, self-sampling for HPV testing, and thermal ablation; (2) expand infrastructure; and (3) build health care provider capacity. Screening services include five Wa’ab community health centers and 17 dispensaries, adding HPV testing in existing and recently acquired GeneXpert systems (Cepheid, Sunnyvale, CA, USA). The project established a supply channel for HPV testing supplies and materials, conducted virtual training with technical support, and supplied thermal ablation devices.

Primary HPV testing implementation started with shipping samples to a commercial laboratory in Hawaii, later transitioning to on-island, point-of-care assay of both self- and provider-collected samples. PACe linked Yap with Cepheid, the GeneXpert system and HPV assay manufacturer, to organize virtual refresher trainings for master trainers, remote demonstrations of HPV assay validation, and technical assistance in setting up the GeneXpert assay platform. Results are uploaded to the canSCREEN app, a cloud-based health registry. Master trainers then mentor and oversee technicians at each of the five community health centers.

Capacity building for health care providers was deployed in three stages: orientation for stakeholders, competency-based training for clinicians, and mentorship during clinical practice. The PACe project facilitated virtual and in-person technical update on the global elimination strategy, cervical cancer screening and management guidelines, PACe project goals and strategies, and extensive clinical skills training on screening and treatment.

Linking service delivery with point-of-care laboratory services involves compiling a population-based screening list, prioritizing unscreened or under-screened women, and bringing HPV testing to places where women live and gather. On the main island, the approach includes integrating primary HPV testing into routine community health center activities, scheduled community health outreach events, and house-to-house visits. An itinerant team of clinicians from the main island will conduct screening at neighboring islands dispensaries, take back and process the samples at the main island, and relay results to relevant dispensary personnel who will communicate with their patients. The designated community health centers on the main island will invite women with positive screening results for a follow-up visit for assessment and treatment.

Guam: Preparing for primary HPV testing

Approximately 71% of women aged 21–65 years in Guam have had a Pap test in the past 3 years, with lower coverage among under-resourced communities.⁴ Guam’s providers use cytology alone or co-testing for cervical cancer screening. All cervical screening specimens are shipped to Hawaii for HPV and cytology testing through a single commercial laboratory service provider. Women who test positive face delays receiving diagnostic tests and treatment because of a limited pool of trained clinical providers for colposcopy and loop electrosurgical excision procedure. The goal of the medical and laboratory component of the PACe project in Guam is to expand screening options and enhance timely diagnosis and management of precancer and cancer following the U.S. screening and management guidelines.^8,30,31

We proposed two strategies to accomplish this goal. The first is through expanding infrastructure for primary HPV screening services. In 2022, the PACe team members conducted a readiness assessment for five Guam facilities through on-site visits and in-depth interviews with a survey filled out by each facility. We developed a score card (Supplementary Appendix Table SA2) adapted for local context from the Improving Data for Decision Making in Global Cervical Cancer Program toolkit³² to identify ways to strengthen key infrastructure, human resources, health information, and community outreach of each facility’s cervical cancer program. Two priorities emerged: using primary HPV testing and expanding access to timely colposcopy. The PACe project worked with the laboratory service provider to develop the laboratory workflow and the documentation—including the medical coding, laboratory procedure, and billing for primary HPV testing with reflex cytology. Insurance coverage concerns are being addressed through communication with public and private health insurance providers. Other efforts include obtaining new state-of-art colposcope equipment, basic clinical instruments, and consumable supplies. The second strategy is screening and management capacity building for health care providers. This strategy involves training providers through refresher courses and technology updates, including a hands-on colposcopy clinical skills training.

The PACe project in Yap and Guam aims to expedite progress toward cervical cancer elimination by adhering to primary HPV testing recommendations from WHO and USPSTF. Yap emphasizes population-based screening, treatment-inclusive capacity building, linking service delivery with point-of-care laboratory services, and an automated registry via the canSCREEN digital health platform. Guam concentrates on expanding screening options and ensuring timely diagnosis and management of precancer and cancer.

3. Health Information System Improvement

A key challenge in monitoring and improving cervical cancer incidence in the USAPI has been the lack of reliable data to inform planning and prioritizing cervical cancer screening efforts. In some islands, cervical cancer screening data are stored in Excel spreadsheets and mainly used to generate reports to funding sources, not to guide and improve screening efforts. Limited screening data in the USAPI have been collected through self-reporting in surveys,⁴ but this information is insufficient to inform screening outreach and follow-up.

The PACe project is working to improve information health systems and generating data to improve cervical cancer screening efforts by working with: (1) stakeholders in Guam and Yap as they develop and tailor their screening and treatment indicators to monitor and improve screening efforts and (2) stakeholders in Yap to implement a cloud-based cancer screening and follow-up management registry, canSCREEN.

The PACe team has worked collaboratively with stakeholders to develop indicators for the various stages of the cervical cancer screening process. Each quarter, the team records indicators to track outreach activities and capacity building of the medical workforce and lab infrastructure at each site. In addition to these programmatic data, the indicators track medical services—including screening and treatment services. The indicators agreed on by stakeholders encompassed existing measures, as well as additional ones that they believed are useful for their cervical cancer programs.

The PACe project partnered with the Australian Center for the Prevention of Cervical Cancer (ACPCC) that develops and manages canSCREEN to implement a cervical cancer screening and management registry in Yap. The canSCREEN platform is a cloud-based registry system specifically designed for population-based cancer screening programs. This registry is a fully integrated system that allows public health professionals, lab technicians, and clinicians to enter and view cancer screening data and results on one platform.³³ The PACe project and ACPCC have worked with stakeholders in Yap to tailor the registry to their program’s needs and provide needed training and technical support.

4. Modeling and Cost-effectiveness Analysis

The fourth component of the project is an evaluation to assess the effectiveness and cost-effectiveness of various cervical cancer screening strategies in the context of PACe sites. We considered (1) the combined impact of HPV vaccination, screening, and treatment of precancer and cancer to identify the optimal cervical cancer screening strategies for Guam and Yap; (2) the potential interplay between cervical screening and precancer treatment; and (3) the long-term impact of scaled-up HPV vaccination and/or invasive cervical cancer treatment access. We used the Policy1-Cervix platform, a microsimulation model, to evaluate the effectiveness and cost-effectiveness of screening by incorporating type-specific HPV infection and natural history, HPV vaccination, and cervical cancer screening and treatment data. The platform has been used for evaluations across a range of different settings, including (1) informing the targets for WHO’s strategy to eliminate cervical cancer launched in 2020, (2) informing development of 2021 WHO cervical screening guidelines for the general population of women and for women living with HIV, and (3) modeling the impacts of primary HPV testing across a range of settings, including in the Indo-Pacific region.^17,34–37

For each project site, we reviewed scientific literature, examined official reports, and consulted federal and local partners to collect data and information to input into the models, including HPV prevalence, cervical cancer burden, current screening practices, HPV vaccination coverage, and costs of cervical cancer prevention and control activities. We used this information to calibrate the Policy1-Cervix platform separately for Guam and Yap. Once a calibrated model was available for each setting, we used it to evaluate the benefits, harms, resource utilization, budget impact, and cost-effectiveness of various potential cervical cancer screening strategies. The results helped identify the optimal screening approach for each jurisdiction.

For Guam, we considered clinician-collected 5-year primary HPV screening with partial genotyping and triaging with HPV16/18, for women aged 30–65 years following the U.S. screening⁸ and management³⁰ guidelines. Two scenarios were considered to identify the optimal screening approach. First, we assumed that primary HPV screening strategies would achieve the same coverage as current practice (cytology alone or co-testing screening strategies), with the HPV vaccination coverage and precancer and cancer treatment utilization maintain the status quo. Second, we considered a scenario in which the primary HPV-based screening strategies achieve the WHO targets for cervical cancer elimination through, for example, expansion of access to screening via self-sampling for HPV testing.¹²

For Yap, we assessed the WHO-recommended screening strategies: HPV screen, triage, and treat and HPV screen and treat. For each strategy, we considered two scenarios: (1) HPV-based screening achieves 70% coverage with HPV vaccination and cervical cancer screening and treatment at the status quo; (2) HPV-based screening achieves the 70% coverage together with increased HPV vaccination and precancer and cancer treatment according to the WHO targets. In exploratory analysis, we also considered the added impact of point-of-care HPV testing on minimizing loss to follow up in HPV-positive women.

Gathering burden of disease epidemiology, cancer screening, and cost data for the USAPI is challenging because such data are scarce. Only two studies reported on HPV prevalence for American Samoa and Yap.^38,39 Cancer registry systems have been established in Guam and FSM since 2007.¹ However, at present, these cancer registries have limitations in the current vital registration system. Nevertheless, these primary data are relevant given that the alternative is estimated data by the International Agency for Research on Cancer, which, for USAPI, are generated by extrapolating incidence and mortality data from neighboring regions. The cervical cancer mortality data recorded by the cancer registries in the USAPI are likely underestimated or inaccurate, because of concerns about cause of death verification.

To overcome such challenges, we used multiple sources of data, considered plausible ranges, and ensured that decisions about input data were informed by in-depth discussions with local medical experts. For example, we held extensive discussions regarding the costs associated with screening, triaging, and follow-up for precancer and cancer treatment and discussions with federal and local immunization service officials regarding HPV vaccination coverage. The HPV vaccine was introduced to the USAPI during 2007–2010 and is part of the routine vaccination schedule.

Conclusion

This report presents an overview of the PACe project to enhance cervical cancer screening and follow-up capacity in Guam and Yap. The strategies outlined were developed and tailored to each respective jurisdiction through participatory engagement with multi-sectors of the local communities. A distinctive strength of the PACe project is its comprehensive approach, focusing on building capacity across multidisciplinary areas to ensure that prevention, screening, diagnostic, treatment, data, and community engagement strategies are coordinated and linked. This approach also includes modeling and cost-effectiveness analyses, which inform strategies that could enable cervical cancer programs to achieve their goals and be sustained in their respective environments.

Given the slow uptake of primary HPV screening and newly approved self-sampling for HPV testing in the United States, the insights gained from the PACe project hold significance not only for other USAPI but also for U.S. women who remain unscreened or under-screened. These women often encounter similar barriers to accessing cervical cancer screening and follow-up services. The PACe project, therefore, may serve as a valuable source of knowledge and experience, with broader implications for improving women’s health outcomes.

Authors’ Contributions

Conceptualization: J.Q., I.S., E.L., V.S., D.T.N.N., M.S., N.P.; Methodology: All authors; Writing—original draft: J.Q., I.S., E.L., V.S., D.T.N.N., K.S.; Writing—review & editing: All authors; Visualization: J.Q., E.L., I.S; Funding acquisition: M.S., J.Q., V.S.

Disclaimer

The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.

Author Disclosure Statement

No competing financial interests exist.

Funding Information

The work presented in the article was supported in part by a cooperative agreement from the CDC under the following prime award number: CDC 6 NU58DP007132. Other support came from NCI U54 CA143727 (University of Guam/Cancer Research Center of Hawai‘i Partnership) and CDC 1 U58 DP007132 (Pacific Regional Central Cancer Registry).