The recovery strategies to support cervical cancer elimination in lower-and middle-income countries (LMICs) following COVID-19 disruptions

Abstract

The COVID-19 pandemic has exacerbated the existing challenges to achieving the WHO target of eliminating cervical cancer as a public health problem by working towards the target of fewer than four cases per 100 000 women. We reviewed the literature to identify potential recovery strategies to support cervical cancer prevention programs in lower-and middle-income countries (LMICs) following COVID-19 disruptions and the extent to which strategies have been implemented. Utilising the WHO health systems framework, we mapped these recovery strategies against the six building blocks to examine their reach across the health system. Most recovery strategies were focused on service delivery, while leadership and governance played a pivotal role in the continuity of cervical cancer prevention programs during the pandemic. Leadership and governance were the drivers for outcomes in the building blocks of health information systems, financing and critical support in operationalising service delivery strategies. In the aftermath of the COVID-19 pandemic with strained health resources and economies, stakeholders would significantly influence the coverage and sustainability of cervical cancer prevention programs. The support from multisectoral stakeholders would accelerate the recovery of cervical cancer prevention programs. To achieve the WHO target by 2030, we call for future studies to understand the barriers and facilitators from the perspectives of stakeholders in order to support the decision-making processes and information required to implement recovery strategies in LMICs.

1. Introduction

Cervical cancer is the fourth most common cancer in women globally with 604 000 new cases and 342 000 deaths recorded in 2020 with the majority of patients (88%) and deaths (91%) occurring in LMICs. (Sung et al., 2021) The disproportionately high incidence and mortality rates in LMICs are attributed to the longstanding challenges of implementing and sustaining prevention programs such as cervical cancer screening and human papillomavirus (HPV) vaccination (Vale et al., 2021, de Sanjose and Holme, 2019). Therefore, cervical cancer is often not identified until it has been well advanced. Moreover, access to effective treatments such as surgery, radiotherapy and chemotherapy is often limited or non-existent. (Vale et al., 2021) The high burden is further exacerbated by the high prevalence of HIV co-infection in some LMICs, which can directly impact the immune control of HPV-positive women. (Liu et al., 2018) The burden of cervical cancer mortality is expected to rise dramatically, and WHO predicts a 27% rise in mortality in LMICs compared to just a 1% increase in HICs by 2030. (Bruni et al., 2022, Krivacsy et al., 2019).

Cervical cancer can be effectively prevented with prophylactic vaccines and new cervical screening technologies based on the detection of HPV that are more easily scaled up than cytology-based programs. In 2018, WHO called for action globally to eliminate cervical cancer as a public health problem by working towards the target of fewer than four cases per 100 000 women and implementing three strategic pillars by 2030, i.e. 90% of girls vaccinated by the age of 15 years, 70% of women screened with high precision tests at least twice in their lifetime, and 90% of women with preneoplastic lesions or cancer be treated. (Cervical cancer elimination initiative. Global Strategy to Accelerate the Elimination of Cervical Cancer as a Public Health Problem. World Health Organization: Geneva;, 2020) As of 2022, the global HPV vaccination program coverage for the first dose dropped from 20% in 2019 to 15%. (World Health Organization. Progress and Challenges with Achieving Universal Immunization Coverage., 2022) Less than 30% of LMICs had introduced an HPV vaccine into their national immunisation schedules to achieve the ambitious target from WHO. (Dorji et al., 2021) Among the LMICs with initial high vaccine uptake, many have struggled to maintain high uptake due to funding constraints and the lack of standard monitoring frameworks to evaluate the impact and drive ongoing investment in depended of the COVID-19 pandemic. (Gavi. Gavi Annual Progress Report, 2020) The current HPV vaccine coverage among girls across Gavi, the vaccine alliance, eligible countries now stands at 8%, compared to 13% globally. For screening, it was estimated that 67% of women aged 20–70 years globally and 90% of women in LMICs had never been screened for cervical cancer. (Bruni et al., 2022).

The COVID-19 pandemic has exacerbated these existing challenges to reach the elimination targets as countries diverted medical resources, professionals and equipment to manage the pandemic since Mar 2020. School closures across the world disrupted the delivery of HPV vaccines and slowed down widespread rollout in many countries, particularly in LMICs. (Toh et al., 2021) The average HPV coverage dropped 25% across six countries that have introduced vaccines with Gavi support¹⁰, and global HPV coverage decreased for the first time in 2020. (World Health Organization. Progress and Challenges with Achieving Universal Immunization Coverage., 2022) For screening tests, there was an estimated decrease of 52% globally during the pandemic. (Teglia et al., 2022, Lucas et al., 2023) In addition, the public was restrained from visiting health care facilities due to lockdowns. These three strategic pillars of cervical cancer elimination have been extensively disrupted globally; the cancer screening rate declined, vaccination programs paused, and treatments were delayed. There is a need to coordinate recovery efforts to ensure the continuity of cervical cancer prevention programs in LMICs following the COVID-19 disruptions and to build resilience into future elimination plans.

WHO has a framework to evaluate health systems and their capability as a whole to achieve equitable and sustainable health outcomes. (World Health Organization. Everybody’s Business – Strengthening Health Systems to Improve Health Outcomes : WHO’s Framework for Action. World Health Organization;, 2007) The framework consists of six core building blocks which are essential to supporting and strengthening a health system: (1) service delivery, (2) health workforce, (3) health information systems, (4) access to medicines and technologies, (5) financing, and (6) leadership and governance. Definitions of each of the components are summarised in Table 1.

Table 1.

Definitions of health system building block Adapted from “Everybody’s business -- strengthening health systems to improve health outcomes: WHO's framework for action.” (World Health Organization. Everybody’s Business – Strengthening Health Systems to Improve Health Outcomes : WHO’s Framework for Action. World Health Organization;, 2007).

System Building Blocks
Service delivery	The service delivery building block was concerned with how inputs and services were organised and managed to ensure access, quality, safety and continuity of care.
Health workforce	Health workers were all people engaged in actions whose primary intent was to protect and improve health.
Medical products, vaccines and technologies	A well-functioning health system ensured equitable access to essential medical products, vaccines and technologies of assured quality, safety, efficacy and cost-effectiveness, and their scientifically sound and cost-effective use.
Financing	A good health financing system raised adequate funds for health, ensuring people could use needed services and are protected from financial catastrophe or impoverishment associated with having to pay for them.
Information	A well-functioning health information system ensured the production, analysis, dissemination and use of reliable and timely health information by decision-makers at different health system levels, both on a regular basis and in emergencies.
Leadership and governance	The leadership and governance of health systems was about the role of the government in health and its relation to other stakeholders whose activities impact health. This involved overseeing and guiding the whole health system. It required political will and championship to reconcile competing demands for limited resources.

In this study, we reviewed the literature to identify potential recovery strategies to support cervical cancer prevention programs in LMICs following COVID-19 disruptions and the extent to which strategies have been implemented. Utilising the WHO health systems framework, we mapped these recovery strategies against the six building blocks to examine their reach across the health system and identify gaps that may impact successful scale-up and sustainability of the elimination agenda. The study methods and search strategy are described in the appendix and have been published on Prospero (CRD42022325226).

2. Strategies to recover cervical cancer prevention programs

We identified 18 potential recovery strategies for LMICs, described in 20 publications (See Fig. 1): 7 focused on service delivery; 4 access to medicines and technologies; 3 health information systems; 3 financing; and 2 on health workforce. In total, 6 of the 18 strategies had been implemented in at least one of in 10 countries, including Bangladesh, Bhutan, Cameroon, Honduras, India, Iran, Mozambique, Sri Lanka, Rwanda, and Zambia. Each is discussed in more detail below and summarised in Table 2.

Fig. 1.

PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analyses) flow diagram of information through the various phases of the systematic review.

Table 2.

Strategies to recover cervical cancer prevention programs.

System Building Blocks	Recovery strategies
Service delivery	1. Improving accessibility to prevention programs (Toh et al., 2021, Gupta et al., 2021, Nakaganda et al., 2021, Villain et al., 2021, Chaila et al., 2021, Sormani et al., 2021, Murewanhema, 2021, Vázquez Rosas et al., 2021, Basu et al., 2021, Lozar et al., 2021, Yadav et al., 2021) ○ Community outreach programs in rural areas, schools and areas with overdue women ○ Mobile clinics, door-to-door or venues near women ○ Reimbursement for travelling costs, or free transport ○ Telemedicine for consultations, clinical decision making and clinical trials
	2. Increasing compliance to treatment among women already diagnosed with pre-invasive cervical lesions (Basu et al., 2021, Budukh et al., 2021, Chargari et al., 2022, Gupta et al., 2021, Lozar et al., 2021, Villain et al., 2021, Woo et al., 2021) ○ Mobile technology (DHIS2), call centres, community health workers for follow-up ○ Improved referral pathway ○ Minimise repeat visits with screen-and-treat and rapid test result
	3. Implementing infection prevention measures (Ajenifuja et al., 2020, Basu et al., 2021, Chaila et al., 2021, Murewanhema, 2021, Sormani et al., 2021, Vázquez Rosas et al., 2021, Villain et al., 2021) ○ Infection prevention and hygiene measures ○ Social distancing to reduce overcrowding such as staggered appointments ○ Constant supply of personal protective equipment for staff ○ Keeping the clinics open
	4. Increasing community awareness(Basu et al., 2021, Budukh et al., 2021, Murewanhema, 2021, Toh et al., 2021) ○ Outreach programs through NGOs, faith-based organisations, ○ Online social media, and conventional media ○ Reduce hesitancy/fear with helplines, websites, social acceptance ○ Improve health literacy
	5. Reorganising how the cervical cancer screening services were delivered during the pandemic (Basu et al., 2021, Budukh et al., 2021, Gupta et al., 2021, Lozar et al., 2021, Villain et al., 2021) ○ Decentralisation of cervical screening and treatment services ○ Prepare contingency plan for future disruption ○ Integrate cervical screening and vaccination programs with other programs such as Anti-retroviral therapy clinics and COVID19 vaccination programs
	6. Catching up on the backlog (Ajenifuja et al., 2020, Basu et al., 2021, Gupta et al., 2021) ○ High throughput cervical screening tools like HPV self-sampling kits ○ Prioritise services for women at highest risk ○ Prioritise treatment for early-stage patients
	7.Streamlining guidelines and protocols for cervical cancer prevention in particular for special groups of women (Vorsters et al., 2022)
Health workforce	8. Provide training (Sormani et al., 2021, Vázquez Rosas et al., 2021, Budukh et al., 2021, Chargari et al., 2022, Lozar et al., 2021, Salcedo et al., 2021, Salcedo et al., 2020) ○ Mentorship in the documentation and technical support ○ Blended learning ○ Support in clinical decision-making via digital exchanging and learning platforms ○ Promote the exchange of learning among government, academic, and healthcare institutions
	9. Sufficient workforce (Chaila et al., 2021, Murewanhema, 2021) ○ Ensure adequate staffing by refreshing and retaining the healthcare provider
Medical products, vaccines and technologies	10.Implement HPV self-sampling test (Sormani et al., 2021, Budukh et al., 2021, Vorsters et al., 2022, Lozar et al., 2021, Woo et al., 2021, Gangopadhyay, 2022)
	11.Single-dose vaccination regimen (Toh et al., 2021, Vorsters et al., 2022)
	12. Maintaining the supplies of vaccines (Toh et al., 2021, Vorsters et al., 2022) ○ Strengthening partnerships with the local authority and minitry ○ Improve logistics and emergency stock
	13. Focus research on (Chargari et al., 2022, Vázquez Rosas et al., 2021) ○ Products applicable and accessible to field conditions of LMICs ○ Radiographic testing techniques, surgical treatments ○ AI imaging and triage markers for self-sampling kit
Financing	14.Ensure equitable access to vaccines, screening kits and cancer treatments in LIMCs (Vázquez Rosas et al., 2021, Vorsters et al., 2022, Chargari et al., 2022)
	15.Ensure financial sustainability of vaccination and cervical screening programs (Toh et al., 2021, Vorsters et al., 2022)
	16.Develop databases to understand the cost of cervical cancer for efficient use of resources (Vázquez Rosas et al., 2021)
Information	17.Implement population-based cancer registries (Vázquez Rosas et al., 2021, Budukh et al., 2021, Nakaganda et al., 2021, Basu et al., 2021)
	18. Increase compliance to standards with monitoring and evaluation frameworks (Chargari et al., 2022, Murewanhema, 2021) ○ Quality indicators ○ Accreditation process

3. Ensuring continuity of service delivery during the pandemic

Recommended recovery strategies for service delivery included (1) implementing infection prevention measures (Villain et al., 2021, Chaila et al., 2021, Sormani et al., 2021, Murewanhema, 2021, Vázquez Rosas et al., 2021, Basu et al., 2021, Ajenifuja et al., 2020), (2) catching up on the backlog (Basu et al., 2021, Ajenifuja et al., 2020, Gupta et al., 2021), (3) increasing community awareness (Toh et al., 2021, Murewanhema, 2021, Basu et al., 2021, Budukh et al., 2021), (4) streamlining guidelines and protocols for cervical cancer prevention in particular for special groups of women (Vorsters et al., 2022), (5) reorganising how the cervical cancer screening services were delivered during the pandemic (Villain et al., 2021, Basu et al., 2021, Vorsters et al., 2022, Nakaganda et al., 2021, Chargari et al., 2022), (6) improving accessibility (Toh et al., 2021, Gupta et al., 2021, Nakaganda et al., 2021, Villain et al., 2021, Chaila et al., 2021, Sormani et al., 2021, Murewanhema, 2021, Vázquez Rosas et al., 2021, Basu et al., 2021, Lozar et al., 2021, Yadav et al., 2021) and, (7) increasing compliance to treatment among women already diagnosed with pre-invasive cervical lesions (Basu et al., 2021, Budukh et al., 2021, Chargari et al., 2022, Gupta et al., 2021, Lozar et al., 2021, Villain et al., 2021, Woo et al., 2021).

3.1. Bringing women back to their screening and follow-up care

During the pandemic, women feared contracting COVID-19 and did not attend cervical screening and delayed treatment. Publications recommended reducing the spread of COVID-19 in health care facilities through infection prevention measures and educating communities on infection prevention measures to alleviate concerns when returning for cervical screening and follow-up services (Villain et al., 2021, Chaila et al., 2021, Sormani et al., 2021, Murewanhema, 2021, Vázquez Rosas et al., 2021, Basu et al., 2021, Ajenifuja et al., 2020). To catch up on the backlog following the lockdowns, publications recommended high throughput cervical screening tools, such as HPV tests, prioritising treatment for early-stage patients and screening women at the highest risk (Basu et al., 2021, Ajenifuja et al., 2020, Gupta et al., 2021). To get women to return for their screening and follow-up care, the recommended strategies included raising awareness of cervical cancer and improving public health literacy on the potential consequences of delaying (Toh et al., 2021, Murewanhema, 2021, Basu et al., 2021, Budukh et al., 2021). Such health promotion campaigns could be facilitated through outreach programs by faith-based organisations or non-governmental organisations. Information could be shared via social and conventional social media to reduce public hesitancy and fear. Helplines and websites could help to improve social acceptance and health literacy of cervical cancer vaccination and screening programs.

3.2. Stakeholders to instil resilience in prevention services

At the broader level, leadership and governance could play a role in the continuity of cervical cancer prevention services during and following the pandemic by introducing contingency plans for possible disruptions such as lockdowns. As the pandemic heightened, stakeholders could plan how the screening and treatment services could continue by decentralising the services from health institutions involved in managing the pandemic (Villain et al., 2021). As the pandemic safety measures changed, stakeholders could play a proactive role in clarifying guidelines and protocols to ensure the continuity of services specifically for groups of women such as vaccinated women and high-risk women. In Bangladesh, the stakeholders operationalised the changing safe distancing measures during lockdowns with timely changes in screening protocols and provided mentorships to clarify guidelines with health care workers (Basu et al., 2021).

Other ways that multisectoral stakeholders could do to recover the cervical cancer prevention services included integrating screening with antiretroviral HIV therapy clinics for HIV-positive women, combining screening and HPV vaccination during postnatal visits or integrating HPV vaccination with other adolescent vaccination programs. (Watson-Jones et al., 2016) Previously, an HIV clinic in Zimbabwe integrated screening with antiretroviral therapy using Cervical Cancer Screening Cascade to provide women with a continuum of care from screening to treatment before the pandemic. (Taghavi et al., 2022) This recommendation improved referral for screen-positive women and helped retain women for follow-up care. Considerable economic returns of cervical cancer investment can be attained with a multisectoral approach regarding productivity and broader social benefits.

3.3. Strategies implemented during the pandemic

Of all the recommended recovery strategies mentioned above, three strategies were reported to have been successfully implemented. CRS EpiC3-90 Project in Zambia implemented staggered appointments to prevent overcrowding, social distancing measures, hand washing facilities and masking for both staff and women. The introduction of infection prevention measures gave women the confidence to return for cervical screening, and the program recorded an 83% improvement in the month following the lockdown (Murewanhema, 2021).

The most frequently recommended strategy reported by the eleven publications was to improve accessibility through outreach screening programs in rural areas or target areas with many women with HIV or overdue for screening (Toh et al., 2021, Gupta et al., 2021, Nakaganda et al., 2021, Villain et al., 2021, Chaila et al., 2021, Sormani et al., 2021, Murewanhema, 2021, Vázquez Rosas et al., 2021, Basu et al., 2021, Lozar et al., 2021, Yadav et al., 2021). Alternatively, the screening program could also reimburse women travelling costs to encourage them to travel to the screening sites. The northern part of Bangladesh reached the rural areas by setting up special clinics close to the community (Basu et al., 2021). The team had community workers in the hard-to-reach areas, so women did not have to travel to a health facility. This strategy enabled the team to have an overall 10% to 45% increase in the total number of women screened in 2020 compared to 2019 despite the restrictions on movement and limited access to health facilities.

For women already diagnosed with pre-invasive cervical lesions, strategies implemented in a few LMICs to ensure these women received timely treatment included covering travel costs to treatment facilities, providing treatment through mobile clinics, minimising repeat visits with screen-and-treat approach, and use of calls, texts and community health workers to encourage attendance for follow-up. Countries including Rwanda, Zambia, Bhutan and India provided free transport services for women to attend treatment facilities for patients diagnosed with cervical cancer (Villain et al., 2021). Furthermore, in India, youth volunteer teams were utilised to assist patients in reaching oncology centres. Bangladesh implemented screen-and-treat at outreach clinics to increase compliance of screen-positive women and reduce the number of referrals to colposcopy clinics by at least 20% compared to 2019. (Basu et al., 2021) In India, Rwanda and Zambia, teleconsultations were used to deliver cervical screening results and follow-up consultations (Villain et al., 2021, Gupta et al., 2021). The use of teleconsultations reduced the need for experts or women to travel. This reduces the geographical inequalities for women living in rural areas of LMICs, where the specialists were often concentrated in cities.

4. Sufficient and trained health workforce

Recommended recovery strategies for the health workforce included getting a (1) sufficient workforce (Chaila et al., 2021, Murewanhema, 2021) and (2) providing training (Chaila et al., 2021, Sormani et al., 2021, Vázquez Rosas et al., 2021, Budukh et al., 2021, Chargari et al., 2022, Lozar et al., 2021, Salcedo et al., 2021, Salcedo et al., 2020), and both have been implemented successfully during the pandemic. In the CRS EpiC3-90 Project, Zambia successfully provided 43 new providers with mentorship in their cervical program's documentation and technical support. (Chaila et al., 2021) The training program in Mozambique introduced blended virtual learning to overcome travel restrictions due to COVID-19 (Salcedo et al., 2021, Salcedo et al., 2020). The international faculty lectured and gave guidance virtually, while local gynaecologists provided on-site support. Overall, 98% of participants in the study stated that the blended virtual experience was the same or better than an in-person course. The other forms of training recommended included digital platforms and workshops for stakeholders, governments, academics and healthcare institutions to learn from each other.

5. Maintaining sufficient and equitable access to vaccines and screening tests

Recommended recovery strategies for the medical products and technologies were (1) a single-dose vaccination regimen (Toh et al., 2021, Vorsters et al., 2022), (2) maintaining the supplies of vaccines (Toh et al., 2021, Vorsters et al., 2022), (3) HPV self-sampling tests (Sormani et al., 2021, Budukh et al., 2021, Vorsters et al., 2022, Lozar et al., 2021, Woo et al., 2021, Gangopadhyay, 2022), and (4) research on products applicable to field conditions of LMICs (Vázquez Rosas et al., 2021, Chargari et al., 2022).

5.1. Single-dose vaccination

There was a recent WHO position paper recommending the optimisation of HPV schedule using alternative off-label single-dose schedule to improve access after disruptions, including school closure and the previous global shortage of HPV vaccines. (WHO Strategic Advisory Group of Experts on Immunization. Meeting of the Strategic Advisory Group of Experts on Immunization, 2022, World Health Organization. Human Papillomavirus Vaccines: WHO Position Paper, December, 2022) The single-dose HPV vaccination strategy eliminated the necessity to trace girls for their second dose. The single-dose schedule might facilitate male and catch-up vaccination for older girls as it reduces logistical and financial resources needed for vaccine delivery, fewer cold chain requirements and easier integration into routine immunisation services. Publications also recommended the local stakeholders to strengthen partnerships with ministries and international organisations to maintain the supplies of vaccines and maintain continuity of vaccination programs (Toh et al., 2021, Vorsters et al., 2022). Stakeholders could learn or leverage the COVID-19 vaccination program to resolve the cold chain logistics and storage issues related to vaccines.

5.2. Self-sampling for HPV tests

Publications recommended self-sampling for HPV tests as a cervical cancer screening recovery strategy (Sormani et al., 2021, Budukh et al., 2021, Vorsters et al., 2022, Lozar et al., 2021, Woo et al., 2021, Gangopadhyay, 2022). It had various successful pilot studies in terms of implementation and high patient acceptability and was an alternative to clinician-collected screening where countries were overloaded or overwhelmed with backlogs. Screening programs could leverage PCR testing infrastructure and technical expertise for HPV testing from what had been learned from screening for COVID-19 and reduce inertia on setup. HPV self-sampling testing could be built onto the existing registries and utilise other logistics from the COVID-19 pandemic in the follow-up of women, sending results via digital platforms and training the workforce to advise women of the results. The Netherlands attained higher cervical screening rates using self-sampling kits than office-based screening during COVID-19(Castanon et al., 2021). This strategy could reduce the reliance on health care professionals at clinics and increase the reach of cervical screening beyond the clinic setting with the self-sampling kits sent through posts (Basu et al., 2021, Lozar et al., 2021).

5.3. Research focus on treatments

To provide equitable access to treatments in rural areas of LMICs, the publications recommended a focus on researching products (radiographic testing techniques, surgical treatments) applicable to field conditions of LMICs (Chargari et al., 2022), particularly being portable and economically viable. Also, publications suggested researching technologies related to artificial intelligence interpretation of colposcopic Images and extending triage markers for the self-sampling kits (Vorsters et al., 2022).

6. Sustainable financing

Recommended recovery strategies for health financing were providing (1) equitable access to vaccines, screening kits and cancer treatments in LMICs (Vázquez Rosas et al., 2021, Vorsters et al., 2022, Chargari et al., 2022), (2) financial sustainability of vaccination and screening programs (Toh et al., 2021, Vorsters et al., 2022) and (3) setting up a database to understand the cost of cervical cancer for efficient use of resources (Vázquez Rosas et al., 2021).

6.1. Equitable access to vaccines, screening kits and cancer treatments

As countries prioritise national resources and efforts to counter the COVID-19 pandemic coupled with the economic effects of the pandemic, there might be a shift in projected government budgets for the prevention of cervical cancer, including HPV vaccination. The publications mentioned the importance of developing affordable vaccines, screening kits and cancer treatments for equitable access in LIMCs. International organisations such as GAVI have kept the price of HPV vaccines to US$ 4.50 per dose for LICs (Gavi. Gavi Annual Progress Report, 2020), while the same vaccines can cost more than US$ 100 in high-income countries. Each vaccine dose costs US$ 13 to US$ 64 for MIC not eligible for GAVI (World Health Organization. WHO HPV Vaccine Global Market Study, 2022). The pandemic brought about the COVID-19 Vaccines Global Access (COVAX) system (Roozen et al., 2022). COVAX showcased a new possibility in ensuring equity through a global pooled procurement mechanism, where international organisations pool buying power from participating economies and provide volume guarantees across a range of promising vaccine candidates to support participation from middle-income countries (Tatar and Wilson, 2021). Also, this strategy could be explored for countries not eligible for GAVI subsided vaccines to negotiate better prices. The Doha Declaration for antiretroviral treatment drugs was another example of making HPV vaccines, cervical screening or treatment options more affordable (Huddart et al., 2017). The declaration demonstrated how to make treatment affordable to the most vulnerable populations by affirming the right of countries to import and produce generic versions and give the license to another entity for the lower-cost generic vaccine, contributing to increasing the supply of drugs essential to HIV treatments (Taghavi et al., 2020, Hinman and Orenstein, 2021).

7. Establish health information for monitoring and tracking

Recommended recovery strategies for health information systems were to set up a (1) population-based cancer registry (Vázquez Rosas et al., 2021, Budukh et al., 2021, Nakaganda et al., 2021, Basu et al., 2021) and (2) to increase compliance to standards with monitoring and evaluation frameworks. Examples include setting up accreditation processes and having quality indicators (Murewanhema, 2021, Chargari et al., 2022).

7.1. Data-driven outreach programs

Many studies supported the importance of population-based cervical cancer screening registries to map underserved communities and track progress and quality of implementation (Vázquez Rosas et al., 2021, Budukh et al., 2021, Nakaganda et al., 2021, Basu et al., 2021). Stakeholders could also use a health information system to support them in making data-driven decisions through timely information on health determinants, cancer risk factors, and program performance. Bangladesh implemented population-based cervical cancer screening using District Health Information Software (DHIS2) and used the data for more targeted outreach programs during the pandemic (Basu et al., 2021). A population-based cancer registry or national screening registry provides an unbiased profile of the cancer burden in the population and how it is changing over time during pandemic or after a change in guidelines. It provides a more accurate view of gaps in the elimination efforts than a screening registry that operates independently, for example, a hospital-based registry.

During the pandemic, many countries had digital tools to contact and trace infected citizens to counter the COVID-19 virus spread and used as proof of vaccination status. Stakeholders from various sectors could share their learnings from COVID-19 and iterate on how to accelerate the implementation of a population-based cancer registry for cervical screening and vaccination services for a comprehensive profile of the cancer burden and vaccination coverage in the population and data-driven recovery strategies.

8. Conclusion

COVID-19 significantly impacted all three elimination pillars for cervical cancer, but it has also presented opportunities to instil resilience in prevention programs. Digital health technology plays a pivotal role during the COVID-19 pandemic by providing optimal access and improving service delivery, vaccination status and service tracking. The COVID-19 digital tool used to improve access could be adapted to scale up cervical screening and HPV vaccination services. The use of telemedicine has allowed the continuation of clinical care and patient management when and where access to service is limited. Telemedicine has also facilitated the continuity of medical education for healthcare practitioners and allowed the healthcare community to maintain clinical care services. Additionally, digital health technology allows for the development of population-base registries that can be repurposed into cancer registries to provide data-driven insights for continuous improvement of cancer screening and prevention services. The pandemic has expanded the PCR testing infrastructure and technical expertise, allowing for rapid mass COVID-19 testing. As the pandemic continues to improve, it opens up further opportunities for scaling up cervical cancer screening, particularly through HPV DNA testing, in each country. For financing, the COVAX system has showcased a new possibility for ensuring equity among countries not eligible for GAVI-subsidized vaccines by enabling them to negotiate better prices through a global pooled procurement mechanism. However, this paper has several limitations regarding the documented strategies. Firstly, the analysis only included publications in English, and there may be other recovery strategies published in other languages that were not considered. Secondly, some recovery strategies that have previously been successful in LMICs were not included in this review as they were challenging to implement during the pandemic, such as campaign mode vaccination. Lastly, this paper did not distinguish between other recommended strategies to address challenges that existed before the pandemic, as the strategies would have evolved to meet the current challenges during and after the pandemic.

There are many ways to recover cervical cancer elimination efforts, and there is no one strategy that does fit all LMICs. The implementation of recovery strategies for cervical cancer elimination efforts requires proactive involvement from stakeholders, who have played a crucial role in pushing for continuity and implementing recovery strategies during the pandemic. Zambia and Mozambique stakeholders' commitment to continue screening or training programs during the pandemic. In Bangladesh, the stakeholders operationalise the changing safe distancing measures during lockdowns with timely changes in protocols and mentorships to clarify guidelines. Leadership and governance were the drivers for recovery strategies in Fig. 2, marked with grey areas. The highlighted strategies, such as HPV self-sampling tests, and a population-based cancer registry, required multisectoral stakeholders’ support and collaboration for sustainable implementations. Hence, we suggested the next step is to understand the barriers and facilitators from the perspectives of stakeholders in order to support the decision-making processes and information required to implement the recovery strategies in LMICs.

Fig. 2.

Visual representations of the recommended strategies mapped to WHO health system building blocks. A column of dots represents a strategy, while each dot represents a publication. The dots with a black border represent the strategies that have been implemented in the 10 LMICs. Leadership and governance play a crucial role for strategies marked with grey areas.

Declaration of Competing Interest

This is a research project initiated by the research team and supported by Merck education grant. Merck has no financial interest, ownership, and intellectual property rights of the research project findings. SMG is supported by NHMRC APP1197951 Leadership Investigator grant level 3, a member of the advisory board for the nine valent HPV vaccine of Merck, received educational grant from Merck for study on HPV and young women through her institution and received Merck lecture fees. SK has served in advisory boards of both Merck & GSK and has received Merck lecture fees. IIP has received Roche lecture fees. DAM has received lecture fees from MSD. The other author reports no conflict of interest. The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Appendix A. Supplementary data

The following are the Supplementary data to this article:

Data availability

Data will be made available on request.