Interventions to increase follow-up of abnormal cervical cancer screening results: A systematic literature review and meta-analysis.

INTRODUCTION: Ensuring timely follow-up of abnormal screening results is essential for eliminating cervical cancer. OBJECTIVE: The purpose of the study was to review single and multicomponent interventions designed to improve follow-up of women with abnormal cervical cancer screening results. We report on effectiveness across studies, and describe what aspects of these interventions might be more impactful. METHODS: Publications were searched between January 2000 and December 2022. The search included observational, quasi-experimental (pre-post studies) and randomized controlled studies describing at least one intervention to increase follow-up of women with abnormal cervical cancer screening results. Outcomes of studies included completion of any follow-up (i.e., attending a follow-up appointment), timely diagnosis (i.e., colposcopy results within 90 days of screening) and time to diagnostic resolution (i.e., days between screening and final diagnosis). We assessed risk of bias for observational and quasi-experimental studies using the Newcastle-Ottawa Scale (NOS) tool and the Cochrane collaboration tool for randomized studies. We conducted a meta-analysis using studies where data were provided to estimate a summary average effect of the interventions on follow-up of patients and to identify characteristics of studies associated with an increased effectiveness of interventions. We extracted the comparison and intervention proportions of women with follow-up before and after the intervention (control and intervention) and plotted the odds ratios (ORs) of completing follow-up along with the 95% confidence intervals (CIs) using forest plots for the interventions vs. controls when data were available. FINDINGS: From 7,457 identified studies, 28 met the inclusion criteria. Eleven (39%) of the included studies had used a randomized design. Most studies (63%) assessed completion of any follow-up visit as the primary outcome, whereas others measured time to definite diagnosis (15%) or diagnostic resolution (22%). Navigation was used as a type of intervention in 63% of the included studies. Most interventions utilized behavioral approaches to improve outcomes. The overall estimate of the OR for completion of follow-up for all interventions was 1.81 (1.36-2.42). The highest impact was for programs using more than one approach (multicomponent interventions) to improve outcomes with OR = 3.01 (2.03-4.46), compared with studies with single intervention approaches with OR = 1.56 (1.14-2.14). No statistical risks were noted from publication bias or small-study effects in the studies reviewed. CONCLUSION: Our findings revealed large heterogeneity in how follow-up of abnormal cervical cancer screening results was defined. Our results suggest that multicomponent interventions were more effective than single component interventions and should be used to improve follow-up after abnormal cervical cancer screening results. Navigation appears to be an important tool for improving follow-up. We also provide recommendations for future studies and implications for policy in terms of better defining outcomes for these interventions.

The Mulher Study: cervical cancer screening with primary HPV testing in Mozambique.

OBJECTIVE: To evaluate cervical cancer screening with primary human papillomavirus (HPV) testing in Mozambique, a country with one of the highest burdens of cervical cancer globally. METHODS: Women aged 30-49 years were prospectively enrolled and offered primary HPV testing using either self-collected or provider-collected specimens. Patients who tested positive for HPV underwent visual assessment for treatment using visual inspection with acetic acid to determine eligibility for thermal ablation. If ineligible, they were referred for excision with a loop electrosurgical excision procedure, for cold knife conization, or for cervical biopsy if malignancy was suspected. RESULTS: Between January 2020 and January 2023, 9014 patients underwent cervical cancer screening. Median age was 37 years (range 30-49) and 4122 women (45.7%) were patients living with HIV. Most (n=8792, 97.5%) chose self-collection. The HPV positivity rate was 31.1% overall and 39.5% among patients living with HIV. Of the 2805 HPV-positive patients, 2588 (92.3%) returned for all steps of their diagnostic work-up and treatment, including ablation (n=2383, 92.1%), loop electrosurgical excision procedure (n=169, 6.5%), and cold knife conization (n=5, 0.2%). Thirty-one patients (1.2%) were diagnosed with cancer and referred to gynecologic oncology. CONCLUSION: It is feasible to perform cervical cancer screening with primary HPV testing and follow-up in low-resource settings. Participants preferred self-collection, and the majority of screen-positive patients completed all steps of their diagnostic work-up and treatment. Our findings provide important information for further implementation and scale-up of cervical cancer screening and treatment services as part of the WHO global strategy for the elimination of cervical cancer.

Elimination of cervical cancer in Latin America (Project ECHO-ELA): lessons from phase one of implementation.

We describe the outcomes of The Extension for Community Healthcare Outcomes-Elimination of Cervical Cancer in The Americas (ECHO-ELA) program, which was developed as a tri-lateral cooperation between Pan American Health Organization (PAHO), the U.S. National Cancer Institute (NCI) and The University of Texas MD Anderson Cancer Center (MD Anderson). The program's purpose is to disseminate strategies for cervical cancer prevention and is structured around the three pillars of the World Health Organization's (WHO) Cervical Cancer Elimination Strategy and the associated 90-70-90 target goals. The target audience includes health authorities from Latin American and Caribbean countries, as well as PAHO's non-communicable disease Focal Points in country offices as well as clinical and public health collaborators. The virtual sessions are held in Spanish for 1.5 hours every month using the ECHO® format. From May 2020 to June 2021, 14 ECHO sessions were held with an average of 74 participants per session (range: 46 - 142). We conducted two anonymous surveys (baseline and follow up) and two focus groups. Respondents stated that the topics they learned the most about included the state of HPV vaccination in the region and strategies for implementing HPV vaccination. Identified needs included support between ECHO sessions and country-specific technical assistance. The ECHO-ELA program provides a forum for increased collaboration between countries in Latin America/Caribbean and the dissemination of best-practice strategies to reach the WHO Cervical Cancer Elimination target goals.

Se describen los resultados del programa ECHO® (Extension for Community Healthcare Outcomes) para la eliminación del cáncer cervicouterino en las Américas (ECHO-ELA), que se concibió como una cooperación trilateral entre la Organización Panamericana de la Salud (OPS), el Instituto Nacional del Cáncer de los Estados Unidos (NCI) y el centro contra el cáncer MD Anderson (MD Anderson) de la Universidad de Texas. La finalidad del programa es difundir las estrategias para la prevención del cáncer cervicouterino, y está estructurado en torno a los tres pilares de la estrategia para la eliminación del cáncer cervicouterino de la Organización Mundial de la Salud (OMS) y los objetivos 90-70-90 conexos. El público destinatario comprende autoridades de salud de países de América Latina y el Caribe, así como los puntos focales de la OPS para las enfermedades no transmisibles en las Representaciones en los países, además de colaboradores en el ámbito clínico y de la salud pública. Las sesiones virtuales se llevan a cabo en español, durante 1,5 horas cada mes, utilizando el formato ECHO®. De mayo del 2020 a junio del 2021 se celebraron 14 sesiones de ECHO, con un promedio de 74 participantes por sesión (límites: 46-142). Se realizaron dos encuestas anónimas (al inicio y de seguimiento) y dos grupos de opinión. Los encuestados declararon que los temas sobre los que más aprendieron fueron la situación de la vacunación contra el VPH en la región y las estrategias para poner en marcha la vacunación contra el VPH. Entre las necesidades mencionadas figuraban el apoyo entre las sesiones de ECHO y la asistencia técnica específica para cada país. El programa ECHO-ELA brinda un foro para una mayor colaboración entre los países de América Latina y el Caribe y para difundir las estrategias sobre las mejores prácticas, a fin de alcanzar los objetivos de la OMS de eliminación del cáncer cervicouterino.

Este trabalho descreve os resultados do programa Extension for Community Healthcare Outcomes para eliminação do câncer do colo do útero nas Américas (ECHO ELA), desenvolvido na forma de cooperação trilateral entre a Organização Pan-Americana da Saúde (OPAS), o Instituto Nacional do Câncer dos Estados Unidos (NCI) e o MD Anderson Cancer Center da Universidade do Texas (MD Anderson). O programa visa a disseminar estratégias para a prevenção do câncer do colo do útero e está estruturado em torno dos três pilares da estratégia de eliminação do câncer do colo do útero da Organização Mundial da Saúde (OMS) e das Metas 90-70-90 associadas. O público-alvo inclui autoridades sanitárias de países da América Latina e do Caribe, bem como os pontos focais de doenças não transmissíveis nas representações da OPAS nos países, além de colaboradores clínicos e de saúde pública. Todos os meses, são realizadas sessões virtuais de uma hora e meia em espanhol usando o formato ECHO®. No período de maio de 2020 a junho de 2021, foram realizadas 14 sessões do ECHO, com uma média de 74 participantes por sessão (variação: 46 a 142). Foram realizadas duas enquetes anônimas (linha de base e acompanhamento) e dois grupos focais. Os entrevistados afirmaram que os tópicos sobre os quais mais aprenderam foram a situação da vacinação contra o HPV na região e as estratégias para implementar a vacinação contra o HPV. As necessidades identificadas incluíam apoio entre as sessões do ECHO e assistência técnica específica para o país. O programa ECHO ELA oferece um fórum para aumentar a colaboração entre os países da América Latina e do Caribe e difundir melhores práticas para atingir as metas de eliminação do câncer do colo do útero da OMS.

Elimination of cervical cancer in Latin America (Project ECHO-ELA): lessons from phase one of implementation / Eliminación del cáncer cervicouterino en América Latina (Proyecto ECHO-ELA): aprendizajes de la primera fase de implementación / Eliminação do câncer do colo do útero na América Latina (Projeto ECHO-ELA): lições da primeira fase de implementação

ABSTRACT We describe the outcomes of The Extension for Community Healthcare Outcomes-Elimination of Cervical Cancer in The Americas (ECHO-ELA) program, which was developed as a tri-lateral cooperation between Pan American Health Organization (PAHO), the U.S. National Cancer Institute (NCI) and The University of Texas MD Anderson Cancer Center (MD Anderson). The program's purpose is to disseminate strategies for cervical cancer prevention and is structured around the three pillars of the World Health Organization's (WHO) Cervical Cancer Elimination Strategy and the associated 90-70-90 target goals. The target audience includes health authorities from Latin American and Caribbean countries, as well as PAHO's non-communicable disease Focal Points in country offices as well as clinical and public health collaborators. The virtual sessions are held in Spanish for 1.5 hours every month using the ECHO® format. From May 2020 to June 2021, 14 ECHO sessions were held with an average of 74 participants per session (range: 46 - 142). We conducted two anonymous surveys (baseline and follow up) and two focus groups. Respondents stated that the topics they learned the most about included the state of HPV vaccination in the region and strategies for implementing HPV vaccination. Identified needs included support between ECHO sessions and country-specific technical assistance. The ECHO-ELA program provides a forum for increased collaboration between countries in Latin America/Caribbean and the dissemination of best-practice strategies to reach the WHO Cervical Cancer Elimination target goals.

RESUMEN Se describen los resultados del programa ECHO® (Extension for Community Healthcare Outcomes) para la eliminación del cáncer cervicouterino en las Américas (ECHO-ELA), que se concibió como una cooperación trilateral entre la Organización Panamericana de la Salud (OPS), el Instituto Nacional del Cáncer de los Estados Unidos (NCI) y el centro contra el cáncer MD Anderson (MD Anderson) de la Universidad de Texas. La finalidad del programa es difundir las estrategias para la prevención del cáncer cervicouterino, y está estructurado en torno a los tres pilares de la estrategia para la eliminación del cáncer cervicouterino de la Organización Mundial de la Salud (OMS) y los objetivos 90-70-90 conexos. El público destinatario comprende autoridades de salud de países de América Latina y el Caribe, así como los puntos focales de la OPS para las enfermedades no transmisibles en las Representaciones en los países, además de colaboradores en el ámbito clínico y de la salud pública. Las sesiones virtuales se llevan a cabo en español, durante 1,5 horas cada mes, utilizando el formato ECHO®. De mayo del 2020 a junio del 2021 se celebraron 14 sesiones de ECHO, con un promedio de 74 participantes por sesión (límites: 46-142). Se realizaron dos encuestas anónimas (al inicio y de seguimiento) y dos grupos de opinión. Los encuestados declararon que los temas sobre los que más aprendieron fueron la situación de la vacunación contra el VPH en la región y las estrategias para poner en marcha la vacunación contra el VPH. Entre las necesidades mencionadas figuraban el apoyo entre las sesiones de ECHO y la asistencia técnica específica para cada país. El programa ECHO-ELA brinda un foro para una mayor colaboración entre los países de América Latina y el Caribe y para difundir las estrategias sobre las mejores prácticas, a fin de alcanzar los objetivos de la OMS de eliminación del cáncer cervicouterino.

RESUMO Este trabalho descreve os resultados do programa Extension for Community Healthcare Outcomes para eliminação do câncer do colo do útero nas Américas (ECHO ELA), desenvolvido na forma de cooperação trilateral entre a Organização Pan-Americana da Saúde (OPAS), o Instituto Nacional do Câncer dos Estados Unidos (NCI) e o MD Anderson Cancer Center da Universidade do Texas (MD Anderson). O programa visa a disseminar estratégias para a prevenção do câncer do colo do útero e está estruturado em torno dos três pilares da estratégia de eliminação do câncer do colo do útero da Organização Mundial da Saúde (OMS) e das Metas 90-70-90 associadas. O público-alvo inclui autoridades sanitárias de países da América Latina e do Caribe, bem como os pontos focais de doenças não transmissíveis nas representações da OPAS nos países, além de colaboradores clínicos e de saúde pública. Todos os meses, são realizadas sessões virtuais de uma hora e meia em espanhol usando o formato ECHO®. No período de maio de 2020 a junho de 2021, foram realizadas 14 sessões do ECHO, com uma média de 74 participantes por sessão (variação: 46 a 142). Foram realizadas duas enquetes anônimas (linha de base e acompanhamento) e dois grupos focais. Os entrevistados afirmaram que os tópicos sobre os quais mais aprenderam foram a situação da vacinação contra o HPV na região e as estratégias para implementar a vacinação contra o HPV. As necessidades identificadas incluíam apoio entre as sessões do ECHO e assistência técnica específica para o país. O programa ECHO ELA oferece um fórum para aumentar a colaboração entre os países da América Latina e do Caribe e difundir melhores práticas para atingir as metas de eliminação do câncer do colo do útero da OMS.

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

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.

Hands-On Training Courses for Cervical Cancer Screening, Diagnosis, and Treatment Procedures in Low- and Middle-Income Countries.

In 2018, there were approximately 570,000 new cases of cervical cancer worldwide. More than 85% of cases occurred in low- and middle-income countries (LMICs), primarily because of poor access to screening and a limited number of medical providers trained to diagnose and treat cervical precancerous lesions. Our objective was to provide locally arranged, hands-on training courses for medical providers in LMICs to learn to perform cervical cancer screening, diagnosis, and treatment procedures. The courses included didactic lectures and hands-on training stations using low-cost simulation models developed by bioengineers and students at Rice University in Houston, TX, United States, and the Malawi Polytechnic in Blantyre, Malawi. The hands-on training stations included visual inspection with acetic acid (VIA), colposcopy, cervical biopsy, endocervical curettage, loop electrosurgical excision procedure (LEEP), and thermal ablation. Provider pre- and postcourse confidence levels in performing the procedures were evaluated. From February 2017 to January 2020, we arranged 15 hands-on training courses in seven cities across six countries (El Salvador, Mozambique, Trinidad and Tobago, Lesotho, Malawi, and Nepal). Overall, there were 506 participants. The average number of participants per course was 38 (range 19-92). The participants included doctors, nurses, and midwives. The course duration varied from 1 to 3 days. Increased confidence in performing VIA, colposcopy and cervical biopsy, ablation, and LEEP was reported by 69%, 71%, 61%, and 76% of participants, respectively. Our findings suggest that locally arranged, hands-on cervical cancer prevention training courses in LMICs can improve provider confidence in performing cervical cancer screening, diagnosis, and treatment procedures. These courses are part of a larger strategy to build local capacity for delivering and improving cervical cancer prevention services in LMICs.

Project ECHO Cancer Initiative: a Tool to Improve Care and Increase Capacity Along the Continuum of Cancer Care.

Solving health problems requires not only the development of new medical knowledge but also its dissemination, particularly to underserved communities. The barriers to effective dissemination also contribute to the disparities in cancer care experienced most everywhere. This concern is particularly acute in low and middle-income countries which already bear a disproportionate burden of cancer, a situation that is projected to worsen. Project ECHO (Extension for Community Healthcare Outcomes) is a knowledge dissemination platform that can increase workforce capacity across many fields, including cancer care by scaling best practices. Here we describe how Project ECHO works and illustrate this with existing programs that span the cancer care continuum and the globe. The examples provided combined with the explanation of how to build effective Project ECHO communities provide an accessible guide on how this education strategy can be integrated into existing work to help respond to the challenge of cancer.

American Society of Clinical Oncology (ASCO) Cervical Cancer Prevention Program: A Hands-On Training Course in Nepal.

Cervical cancer is the leading cause of death among women in Nepal. The American Society of Clinical Oncology (ASCO) and The University of Texas MD Anderson Cancer Center collaborated with international and local experts to hold a cervical cancer prevention course in Nepal in November 2019. The course included didactic lectures and a hands-on workshop. The didactic lectures included the epidemiology of cervical cancer globally and locally, cervical cancer screening guidelines, human papillomavirus vaccination, colposcopy and visual inspection with acetic acid (VIA), cervical dysplasia, and cervical cancer treatment. The hands-on workshop consisted of four stations: (1) VIA; (2) colposcopy, cervical biopsy, and endocervical curettage; (3) thermal ablation; and (4) loop electrosurgical excision procedure (LEEP). A train-the-trainer model short course was held by the international faculty to assist six local faculty to become familiar with the instruments, procedures, and models used in the hands-on training stations. Forty-two people (84% gynecologist, 8% radiation oncologist, and 8% other) attended the course. Following the course, the international faculty visited the regional hospitals for additional educational activities. Increased knowledge in cervical cancer screening guidelines and ability in performing VIA, colposcopy and cervical biopsy, thermal ablation, and LEEP were reported by 89%, 84%, 84%, 87%, and 84% of participants, respectively, from the postcourse on-site evaluations. From the 6-month follow-up survey, all respondents reported that they had made practice changes based on what they learned in the course and had implemented or tried to implement the cervical cancer screening guidelines presented at the course. In conclusion, the course evaluations suggested an improvement in participants' ability to perform cervical cancer screening and diagnostic procedures and reported the changes in practices after training.