Abstract

Introduction

Achieving cervical cancer (CC) elimination requires monitoring access to and quality of prevention and care services, particularly for women at high risk of disease, like women living with HIV (WLHIV). We assessed implementation practices in HIV clinics across sub-Saharan Africa (SSA) and present CC prevention and care cascades for WLHIV.

Methods

We conducted a two-level facility-based survey in 30 HIV clinics participating in the International epidemiology Databases to Evaluate AIDS (IeDEA) consortium across SSA between November 2020 and July 2021. At site-level, we performed a qualitative assessment of CC prevention and care services. At patient-level, we analysed data from routine care offered to WLHIV in SSA.

Results

 HPV vaccination was uncommon across sites (33%). Referral for CC diagnosis (68%) and treatment (70%) was common and these services often came at a cost (55%) to the patient. Almost all sites had electronic health information systems (90%). However, routinely-collected data to inform indicators to monitor global targets for CC elimination in WLHIV were rare: data for monitoring were available in 36.4% of sites offering HPV vaccination, in 33.3% of sites offering cervical screening and in 20% of sites offering pre-cancer and CC treatment.

Conclusion

Although CC prevention and care services have been available in several HIV clinics across SSA for about a decade, patient and programme monitoring remain inadequate. While improving access to services, countries should consider leveraging existing health information systems, using guidance from World Health Organization tools for monitoring to improve these programmes, and track progress towards CC elimination globally.

 Keywords: Cervical cancer prevention, WLHIV, prevention and care cascades, sub-Saharan Africa, monitoring, elimination targets.

Introduction

Cervical cancer (CC) remains a leading cause of cancer-related mortality in Sub-Saharan Africa (SSA), although it is a highly preventable disease through early screening and treatment of cervical pre-cancer, coupled with high-risk human papillomavirus (HPV) vaccination. In 2020, there were an estimated 604 000 new cases and 342 000 CC-related deaths globally, with 90% of these occurring in low- and middle-income countries (LMICs).[1] HIV infection compounds the CC burden, contributing to huge disparities across countries and regions.[2] Whereas one in five CC cases in Africa was attributable to HIV in 2018, the population attributable fraction for HIV was less than 2% in all other regions.[3] Addressing CC prevention needs for WLHIV is crucial in significantly reducing the CC burden and regional disparities. Several countries across SSA have been implementing CC screening for about a decade, yet few studies report CC implementation practices and outcomes for WLHIV.

The World Health Organization’s (WHO) strategy to accelerate the elimination of CC within a century defines the 90-70-90 targets to be achieved by 2030: 90% of girls need to be vaccinated with an HPV vaccine by 15 years of age, 70% of women screened using a high performance test by the age of 35 years and by 45 years, and 90% of women identified with cervical pre-cancer or cancer are treated.[4] For these targets to be achieved, CC prevention strategies for girls living with HIV and WLHIV need to be tailored to suit their specific needs, as they are more susceptible to disease compared to HIV-negative women.[5, 6] For example, WHO recommends a screen-triage-treat approach starting at age 25. Also, integrating preventive HIV and CC services according to women’s needs over time and across different health system levels is strongly recommended.[6-9] This model has been shown to improve both uptake of screening services and clinical outcomes.[10]

With these recommendations and goals for CC elimination, it is important to assess currently available services and track progress towards CC elimination. Several countries in SSA have integrated CC prevention and care within HIV clinics.[11-14] However, these programs are opportunistic with low coverage and may not effectively reduce CC incidence and mortality over time as observed in high-income countries.[15] Cervical cancer control services need to be coupled with robust quality assurance and monitoring mechanisms.[4] Previous studies report pre-cancer treatment rates of 25.6% in WLHIV in a public hospital in Johannesburg, South Africa, 76.2% in women regardless of HIV status in Zambia, and 78% in WLHIV in one clinic in Zimbabwe.[16-18] A systematic review in 2017 summarised cervical screening practices for WLHIV in SSA.[5] These studies, however, do not report on all three WHO elimination targets as well as other aspects of a comprehensive CC prevention and control programme. A commitment to eliminating CC requires reform both internal and external to the health sector, including expanding community awareness, biomedical and clinical interventions, improving quality assurance and monitoring mechanisms, as well as financial and technical resources for programme implementation.[19] Patient–level and facility-level indicators with robust surveillance systems for monitoring CC prevention activities are critical to assess the progress, identify gaps, and facilitate change.[4]

Although cervical screening services are commonly available in HIV clinics across SSA, implementation practices are rarely described and routinely collected data to monitor global WHO targets for CC elimination in WLHIV are rarely reported. To address this gap, we qualitatively assessed the implementation of CC prevention services at the facility/site level. In addition, using patient-level data we populated steps in the prevention and care cascade for WLHIV attending HIV clinics with fairly evolved CC prevention programmes across SSA.

Methods

Study design and setting

We conducted a facility-based survey between November 2020 and July 2021. The study sites were selected HIV clinics in four African regions participating in the International epidemiology Databases to Evaluate AIDS (IeDEA). The IeDEA is a global network gathering and analysing routinely collected clinical data from children, adolescents and adults living with HIV across 240 HIV treatment and care sites (https://www.iedea.org/ ). We included 30 clinics offering CC prevention services on- or off-site. The IeDEA regional principal investigators identified sites that had fairly evolved CC screening programmes for participation in the survey.

Study participants

We collected patient- and site-level data for HPV vaccination and cervical screening in four populations as described below:

a) HPV vaccination

i) Girls and adolescents/young women in care: girls aged 9-14 years and/or adolescents or young women aged 15-26 years living with HIV who had at least one HIV medical care visit in the ART clinic during the index year (the year data was reported for).

ii) Girls and/or adolescents and young women living with HIV eligible for HPV vaccination: according to site's eligibility criteria

b) Cervical screening

iii) Women in care: Women living with HIV 15 years old or older, who had at least one HIV medical care visit during the index year

iv) Women eligible for cervical screening: Women living with HIV who met the site-specific CC screening eligibility criteria

These harmonised definitions of girls and women in care allowed for data comparisons across sites in different countries.

Survey development

We constructed a two-level survey based on the International Agency for Research on Cancer CANscreen5 tool (https://canscreen5.iarc.fr/) and the WHO Toolkit for Cervical Cancer prevention and control programmes.[20] Firstly, we organised a meeting with the IeDEA principal investigators, data managers, the CANscreen5 and WHO toolkit development team members, to discuss: the scope of the study, study population, site eligibility, and index years for data collection. Secondly, the lead author (SLA) visited six of the 30 participating sites to discuss the survey objectives and questions with CC control programme teams, and revised the survey based on their input. The revised survey was programmed into Research Electronic Data Capture (REDCap 9.8.2), a web-based application used to create databases and projects. We offered the survey in English and French.

At the site-level, we performed a qualitative assessment of CC prevention and care services. We assessed the availability of HPV vaccination and CC prevention services and organized the selected indicators into six domains: 1) respondent and site characteristics (e.g. facility location); 2) HPV vaccination (e.g. cost of vaccination); 3) CC screening, diagnosis and treatment (e.g. screening guideline availability); 4) data collection and aggregation systems (e.g. electronic system availability); 5) evaluations and audits (e.g. assessment of health information system within the last ten years); and 6) decision and referral support systems (e.g. availability of monitoring and evaluation plan).

At the patient-level, we analysed data from routine care offered to WLHIV in these sites. We obtained aggregated CC prevention data for girls and women receiving care at HIV clinics. We prioritised reporting of WHO global indicators [20], and included HPV vaccination rate, which is one of the key indicators for monitoring the WHO targets for CC elimination.

Survey piloting and data collection

Between May and August 2020, we piloted the survey at two sites in West and East Africa and revised following feedback. Target respondents for the site-level survey were CC prevention and control programme managers or health personnel directly involved in CC screening activities. For the survey of patient-level data, the data manager was the preferred respondent. We invited respondents via email using automatically generated links to survey forms. Sites with challenges using REDCap 9.8.2 printed the forms, filled them in and submitted scanned copies through a secured email server. One researcher (SLA) manually entered scanned responses into REDCap 9.8.2 and another (MD) checked the entries. Site investigators were also able to check accuracy of their site data and communicated any queries to the lead author.

Statistical analyses

The primary outcomes of interest for our analysis were: availability and use of CC prevention services, proportion of girls and women vaccinated, screened, treated for cervical pre-cancer and CC. We used descriptive statistics to report site characteristics. We calculated percentages for reported indicators. We used a changing-denominator, also called target approach, to calculate the CC prevention and care cascade, where all women reaching a given step comprise the denominator for the subsequent step. This approach highlights retention gaps at various points of the CC prevention and care cascade.[21] We reported outcomes of patient-level analyses for sites with data disaggregated by HIV status. We reported data for sites that included 10 or more eligible girls or women in care. This cut-off was guided by low data availability across sites, particularly those offering HPV vaccination. Due to the relatively few number of sites with evolved CC programmes included per region, we typically reported data for the total number of sites (column percentages in bold on tables 1-4 and supplementary tables 1-4).  The complete data for girls eligible for HPV vaccination, cervical screening, diagnosis, treatment, and referral are reported in Supplementary tables 5-10. All analyses were performed using Stata 16 SE (Stata Corp., College Station, TX, USA).

Ethical considerations

The local ethics committees in participating countries all approved the use of routine (aggregated) data for research within the IeDEA collaboration. We also received an ethics waiver from the Ethics Committee of the Canton of Bern, BASEG-Nr: Req-2019- 00695.

Results

Sites and respondent characteristics

We included 30 sites across the following 14 countries in four SSA IeDEA regions: Burundi and Rwanda in Central Africa (7 sites); Kenya, Tanzania, and Uganda in East Africa (8 sites); Lesotho, Malawi, Mozambique, South Africa, Zambia, and Zimbabwe in Southern Africa (9 sites); and Burkina Faso, Nigeria, and Côte d’Ivoire in West Africa (6 sites; Figure 1, Supplementary table 11). We had a 100% response rate to the survey. Most of the respondents were either data managers (30%), physicians (30%) or programme managers (27%). The majority of the sites were public sector facilities (73%) and were located in urban areas (83%; Table 1).

 Table 1: Site and respondent characteristics

Site-level data: qualitative indicators

HPV vaccination

Seventeen out of 30 sites (57%) offered HPV vaccination either currently (n=10, 33%) or in the past (n=7, 23%), see Supplement Table 1. Reasons for the discontinuation of HPV vaccination services included lack of funding (43%), low community acceptance and COVID-19 (n=1, 14%), completion of pilot/research study (14%). The quadrivalent (n=10, 59%) and bivalent (n=4, 24%) vaccines were the most commonly used HPV vaccines and were delivered mostly through a combination of school- and community-based (n=6, 20%) strategies. Of the 10 sites currently providing HPV vaccination, one site in Zimbabwe targeted both girls and boys between 8 and 18 years old while the other nine sites targeted only girls less than 15 years old. Services were free of charge in all sites either currently or previously offering HPV vaccination.

Organisation of cervical screening, demand generation and programme financing

About a quarter of CC screening programmes were supported as pilot programmes (n=2, 7%) or research studies (n=5, 17%). Integration of cervical screening services was mainly within the HIV clinic using existing staff (47%) or in another unit in the facility where the HIV clinic is located (43%) (Table 1). Mass media campaigns (78%) and group education (74%) were the most common approaches for demand generation. Although Non-Governmental Organisation (NGO) financial support to sites was common (83%), less than half of the sites (43%) received NGO support specifically for CC prevention. Clients in half of the sites paid either the total cost (43%) or partial cost (7%) for diagnosis and either the total cost (33%) or partial cost (20%) for pre-cancer and cancer treatment.

Table 2: Organisation of screening, demand generation and financing

Cervical screening and pre-cancer treatment

Cervical screening was provided on-site (93%) or off-site (7%). There was an equal distribution in the number of sites screening women regardless of age (40%), and those screening women between 15 and 65 years of age. Visual inspection with acetic acid (VIA) was the most common screening method (83%). HPV/DNA testing and triage was performed in less than half of the sites (40%). Histopathology (37%) and colposcopy (30%) were the most commonly used tools for pre-cancer diagnosis and these procedures mainly occurred off-site (53%). Cryotherapy (63%), thermocoagulation (43%) and Loop Electrosurgical Excision Procedure (57%) were the most common pre-cancer treatment methods. Follow-up of screened negative women and women treated for pre-cancer was common practice, with 12 months being the most common follow-up interval for both groups (Table 3).

Diagnosis and management of invasive cervical cancer

Invasive CC diagnosis (73%) and treatment (67%) services were available in about two thirds of the sites, see Supplement Table 2. Histopathology was the most common invasive CC diagnostic tool (40%). Simple hysterectomy (37%), radical hysterectomy (53%), chemotherapy (43%) radiation therapy (40%), and intra-cavitary radiation therapy (13%) were used in combination across sites. Access to opioids was very limited, with only six (20%) sites reporting consistent availability.

Table 3: Screening, triage and treatment of pre-cancerous lesions

Laboratory testing and quality assurance

Laboratory testing was done in 17 (57%) sites either for pre-cancer only (29%), invasive CC diagnosis only (12%), or both (58%); see Supplement Table 3. Time-to sample arrival at the laboratory was mostly within one day (41%) or between 2 and 7 days (41%). Results turnaround time varied between one and four weeks (65%) in most sites. Quality assurance coordinators were available in a little over half of the sites (59%); and corresponding guidelines in 70% of these sites and 48% of all sites. Accreditation systems were available in about a third of sites offering HPV/DNA testing (33%) and pathology services (20%).

Referral and tracking

Referral for CC screening was quite common across sites either always (23%) or sporadically (60%), see Supplement Table 4. Off-site referral was mainly for diagnosis (42%), and tracking of referred women through phone calls (48%) was common. Twenty-five sites referred women for pre-cancer treatment either systematically (40%) or occasionally (43%) for large lesions/suspect cancer (n=12, 40%), or absence of treatment infrastructure (n=9, 30%). Following referral, approximately a third of the sites (23%) never contacted women for follow-up after pre-cancer treatment and about half (43%) after invasive CC management.

Surveillance systems and data collection

All sites had data systems that were mostly electronic (90%), Table 4. Seven of the ten sites offering HPV vaccination collected related data, and half of the surveyed sites collected some data on CC screening. Several sites had at least one of the WHO global monitoring indicators for CC elimination in place: number of girls vaccinated by age 15 years, (n=10; 70%), number of women screened (n=30; 70%), and number of women treated (n=30; 50%). About one third of the sites (37%) specifically linked HIV status to existing indicators. A few sites systematically collected data on cancer stage (37%) and survival (23%).

 Table 4: Surveillance systems and data collection

Patient-level data: monitoring indicators reported for girls eligible for HPV vaccination and women in care at ART clinics

Of the 30 sites assessed, 11 (37%) collected data for the patient-level assessment specifically for girls living with HIV and WLHIV, including HPV vaccination, CC screening, pre-cancer and CC treatment. About a third of the sites 11 (37%) had some data, yet without disaggregation by HIV status.

HPV vaccination

Of the 10 sites offering HPV vaccination at the time of the survey, two reported HPV vaccination proportions for 10 girls or more living with HIV and eligible for HPV vaccination at their facility (Supplement Table 5). At these sites, vaccination proportions were 21% in Newlands Clinic, Zimbabwe, and 88% in Kisesa, Tanzania.

Cervical screening

Of the 15 sites that reported collecting data on cervical screening, only 11 reported indicators disaggregated by HIV status (Table 4). Cervical screening proportions ranged from 4.3% in “Hôpital de Jour du CHU Souro Sanou”, Burkina Faso to 78% in Newlands Clinic, Zimbabwe (Figure 2, Panel A).

Pre-cancer and cervical cancer management

Pre-cancer treatment proportions were reported in 10 sites and ranged from 14% in Kanyama hospital in Zambia to 100% in George health centre in Zambia (Figure 2, Panel B). There were wide disparities in attrition (proportion of women who did not attain the next necessary cascade step) observed across sites between women screened positive and those who received treatment for pre-cancer ranging from 0% in George health centre to 86% in Kanyama hospital (Supplement table 7). Only two sites reported data on the number of WLHIV who initiated treatment for CC; three women in Newlands Clinic in Zimbabwe, and one woman in “Hôpital de Jour du CHU Souro Sanou” in Burkina Faso, Supplement Table 8.

Discussion

We surveyed 30 HIV clinics across 14 countries in four SSA IeDEA regions to assess implementation practices for CC prevention and care and to populate indicators using routinely collected patient-level data. Programs for HPV vaccination were ongoing in only one third of investigated sites. Referral for pre-cancer and invasive CC diagnosis and treatment was common and women had to pay a fee for these services in about two thirds of the sites. Almost all sites used electronic systems for data collection, although only half collected CC data routinely, including data needed to inform WHO global monitoring indicators for CC elimination.

Comparison of findings with recent evidence and WHO guidelines

HPV vaccination is recommended by WHO for primary prevention of CC. By the end of 2019, 41% of WHO member states in the African region had introduced HPV vaccination in their national immunisation programmes.[22] At the time of our study, some sites had stopped HPV vaccination due to financial constraints and the COVID-19 pandemic which aligns with previous identified barriers to HPV vaccination.[23, 24] Financial barriers have partly been tackled by GAVI, the Vaccine Alliance for over a decade but our study shows that funding challenges persist. Although the GAVI model has been beneficial, countries will need to sustain financing for HPV vaccination as they mature. The repercussions of the COVID19 pandemic are yet to be completely measured. However, few reports show significant interruptions in vaccination programmes including HPV due to the COVID 19 pandemic.[25, 26] Innovative approaches for vaccine delivery within pandemic preparedness and response plans could be considered by countries. Data on HPV vaccination for girls living with HIV were rare and we found no previous published studies reporting HPV vaccination rates in girls living with HIV. Few studies report data on HPV vaccination rates for the general population, and data from countries in SSA remain scanty.[22, 27] Collecting HPV vaccination data is challenging particularly, for girls living with HIV. This might be partly because several vaccination programmes are school-based, and the associated stigma during administration of a second and third vaccine dose for these girls in school is problematic. Innovative strategies for vaccine delivery and data capture are needed for this underserved population.

WHO strongly recommends HPV/DNA testing and triaging as a cervical screening strategy for WLHIV.[6] Due to the sub-optimal specificity of the HPV/DNA test, triage tests are essential to distinguish between those who need immediate treatment and those who can be followed up. Although these recommendations were launched at the end of data collection for our study, a few sites already implemented HPV/DNA testing, while maintaining other visual methods for screening and triage. However, inadequate local infrastructure and lack of financing pose challenges for implementation of screen-triage-treat strategies for WLHIV in health facilities. In these settings, VIA-based screening is still very common as highlighted by findings from our study and previous studies.[17, 28, 29] Visual testing is less resource-intensive and women are more likely to receive same-day treatment improving retention in care.[10] Transitioning to HPV/DNA testing requires efforts to strengthen local laboratory infrastructure, quality assurance systems and financing.

In 2019, an estimated 40%-70% of healthcare facilities in the public sector in LMICs had services for cancer diagnosis and treatment.[4] Methods for invasive CC diagnosis and treatment used across sites studied have been efficient in improving outcomes for women in high-income countries.[30] However, access remains limited to many women in SSA. Women referred for CC diagnosis and treatment were tracked mostly through phone calls/messaging. Using mobile phones for text messaging follow-up reminders to women is a feasible solution in these settings.[31, 32] At the time of our survey, pre-cancer and CC diagnosis and treatment services were free in only about a third of the surveyed sites. Financial barriers to CC diagnosis and care services have been reported in previous studies and the cost of diagnostic tests, medication and travel were the key financial challenges reported by many women.[33, 34]

Routinely collected patient-level data disaggregated by HIV status was rare at sites included in our study. Previous reports have highlighted the limited availability of patient-level data as a shortcoming for integrated health programmes partly explained by fragmented funding and data systems [35, 36]. We identified high variation in attrition rates across different steps of the CC prevention and care cascade across sites. For example, between women screened positive and those treated for pre-cancer, attrition rates ranged between 0% in George health centre, Zambia, and 86% in Kanyama, Zambia. High attrition rates were also reported in a South African study; about 70% across cascade steps.[16] In contrast, a similar study carried out in the Newlands clinic in Zimbabwe showed attrition rates of less than 20% across cascade steps.[18] This clinic receives funding specifically for CC prevention, and invests in human resources for programme monitoring which may explain high screening rates and relatively low attrition rates.

Addressing financial barriers will further improve access to CC prevention and care services, hence outcomes for women. In our study, only half of the sites received Government or NGO financial support for CC screening. Keeping the long-term benefits of investing in CC prevention in mind, Governments may need to consider other innovative ways to sustain finance beyond grants.

Quality assurance and monitoring are indispensable for any effective CC prevention programme. The majority of sites studied had quality assurance plans, with accreditation systems for HPV tests. For monitoring to be feasible, data systems that collect data for pre-defined indicators in a consistent fashion are crucial. CC prevention facility-based indicators developed specifically for WLHIV[37] (Davidović M., unpublished) may be considered in these settings. Monitoring CC occurrence and outcomes, including incidence and survival requires population-based cancer registries. Where electronic records exist, record linkage of cancer registries and death registries with HIV data may help to fill gaps in HIV status and survival data respectively.[10] Although almost all sites studied had electronic data systems which have been shown to be more efficient in programme monitoring,[38] only half of them collected data on CC prevention and care, and less than half linked these data to population and hospital based cancer registries.

Strengths and weaknesses of the study

The main strength of our study is that we co-developed the survey with country representatives using internationally standardised tools, which improved the validity for each context. Our focus on WLHIV highlights existing prevention and monitoring efforts for this population and gaps across the continuum of CC prevention and care. Besides the site-level assessment, we also analyzed routinely collected data at patient-level, which reflects closely the real situation in these sites.

However, we acknowledge some limitations. The facilities included in our study are part of the IeDEA consortium receiving some research funding, and may not necessarily reflect the general CC prevention and care environment in sites in these countries. We also selected only 30 sites with fairly advanced CC prevention programmes, further reducing representativeness. In addition, the service delivery and monitoring landscape for CC may have changed since the time of data collection in some sites studied.

Conclusion

Facility-based data have contributed significantly to national and global monitoring of other diseases like HIV. Several efforts have been made by governments and partners to provide CC prevention and care for WLHIV across SSA. However, infrastructure and financial challenges persist, hindering access to vital vaccination, diagnostic and treatment services and proper monitoring mechanisms. Our findings illustrate the need for implementation strategies to improve monitoring of CC prevention among girls and WLHIV. Governments should consider leveraging existing electronic data systems to strengthen CC data collection in the short-to medium term, and improving access to specialised care platforms in the long term, which contribute to the majority of referrals. Data collected and analysed are crucial to assist governments and stakeholders to better plan, target, tailor, and scale-up CC prevention and care interventions and also to track progress towards the WHO 2030 CC elimination targets. All these approaches should be customised by each country, while allowing for comparability and taking into consideration readiness to implement prevention, to ensure sustainability.

Conflicts of interest

None declared

Authors’ contributions

SLA, MD, KT, AJ, KA, KWK, PB, MY, SPB, SB, AM, AS, CC and JB conceived the study, wrote the concept and drafted the survey. TD supported data curation and analysis, BM, CT, GM, HT, JM, OE, OO, MJ, KT coordinated data collection in all sites. SLA and JB wrote the first draft of the manuscript. All co-authors reviewed and approved the final manuscript.

Acknowledgements

We thank all the survey respondents, Dr Sharon Kapambwe, Ms Misinzo Moono, Mr Lweendo Muletambo, Ms Jane Matambo, Mr Mwansa Lumpa, Ms Ardele Mandiriri, Mr Athanase Munyaneza, Mr Claude Azani, Dr Jaqueline Huwa, Dr Eliane Rohner, Dr Zaidat Musa and the Clinical Trials Unit of the University of Bern REDCap team for their valuable contributions to this work.

Data availability statement

The supplementary files contain most of the data that support the findings of our study. Further information is available from the corresponding author upon reasonable request.

Ethics

The local ethics committees in participating countries all approved the use of routine data for research within the IeDEA collaboration. We also received an ethics waiver from the Ethics Committee of the Canton of Bern, BASEG-Nr: Req-2019- 00695.

Disclaimer

Where authors are identified as personnel of the International Agency for Research on Cancer/World Health Organization, the authors alone are responsible for the views expressed in this article and they do not necessarily represent the decisions, policy or views of the International Agency for Research on Cancer /World Health Organization.

Funding

This research was funded by the Swiss National Science Foundation (SNSF), under funding scheme: r4d (Swiss Programme for Research on Global Issues for Development), grant number 177319. The International Epidemiology Databases to Evaluate AIDS (IeDEA) is supported by the U.S. National Institutes of Health’s National Institute of Allergy and Infectious Diseases, the Eunice Kennedy Shriver National Institute of Child Health and Human Development, the National Cancer Institute, the National Institute of Mental Health, the National Institute on Drug Abuse, the National Heart, Lung, and Blood Institute, the National Institute on Alcohol Abuse and Alcoholism, the National Institute of Diabetes and Digestive and Kidney Diseases, and the Fogarty International Center, Central Africa, U01AI096299; East Africa, U01AI069911; Southern Africa, U01AI069924; West Africa, U01AI069919. Informatics resources are supported by the Harmonist project, R24AI24872. This work is solely the responsibility of the authors and does not necessarily represent the official views of any of the institutions mentioned above. SLA also received the Swiss Government Excellence Scholarship, number 2019.0741. Three authors (SLA, MD and TD) received the SSPH+ Global PhD Fellowship Program in Public Health Sciences funded by the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement No 801076.

ABBREVIATIONS AND ACRONYMS

ART – Antiretroviral Therapy

CanScreen5- Cancer Screening in Five continents

CC – Cervical Cancer

CKC – Cold Knife Conization

COVID-19- Coronavirus Disease-19

DNA- Deoxyribonucleic Acid

FBO – Faith Based Organisation

GAVI- Gavi, the Vaccine Alliance

HIV – Human Immunodeficiency Virus

HPV – Human Papillomavirus

IeDEA – The International Epidemiology Databases to Evaluate AIDS

NGO- Non-Governmental Organisation

PBCR – Population Based Cancer Registry

PIs – Principal Investigators

REDCap- Research Electronic Data Capture

SSA – Sub-Saharan African

VIA – Visual Inspection with Acetic Acid

VIAC – Visual Inspection with Acetic Acid and Cervicography

VILI – Visual Inspection with Lugol’s Iodine

WHO – World Health Organization

WLHIV – Women living with HIV

References

1.           Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin. 2021;71(3):209-49.

2.           Denslow SA, Rositch AF, Firnhaber C, Ting J, Smith JS. Incidence and progression of cervical lesions in women with HIV: a systematic global review. Int J STD AIDS. 2014;25(3):163-77.

3.           Stelzle D, Tanaka LF, Lee KK, Ibrahim Khalil A, Baussano I, Shah ASV, et al. Estimates of the global burden of cervical cancer associated with HIV. The Lancet Global Health. 2021;9(2):e161-e9.

4.           World Health O. Global strategy to accelerate the elimination of cervical cancer as a public health problem. Geneva: World Health Organization; 2020.

5.           Viviano M, DeBeaudrap P, Tebeu PM, Fouogue JT, Vassilakos P, Petignat P. A review of screening strategies for cervical cancer in human immunodeficiency virus-positive women in sub-Saharan Africa. Int J Womens Health. 2017;9:69-79.

6.           WHO guideline for screening and treatment of cervical pre-cancer lesions for cervical cancer prevention, second edition. Geneva: World Health Organization; 2021. Licence: CC BY-NC-SA 3.0 IGO.

7.           UNAIDS. Global-AIDS-strategy- End Inequalities. End AIDS. 2021-2026_en(1).pdf>.

8.           Huchko MJ, Maloba M, Nakalembe M, Cohen CR. The time has come to make cervical cancer prevention an essential part of comprehensive sexual and reproductive health services for HIV-positive women in low-income countries. J Int AIDS Soc. 2015 Dec 1;18(Suppl 5):20282. doi: 10.7448/IAS.18.6.20282. PMID: 26643456; PMCID: PMC4672400.

9.           World Health Organization. (‎2018)‎. Integrating health services: brief. World Health Organization. https://apps.who.int/iris/handle/10665/326459. License: CC BY-NC-SA 3.0 IGO

10.         UICC/IARC/AFCRN. Cervical cancer elimination in Africa: where we are now and where we need to be? 2022. http://globalink.uicc.org/resources/cervical-cancer-elimination-africa-where-are-we-now-and-where-do-we-need-be.

11.         Sigfrid L, Murphy G, Haldane V, Chuah FLH, Ong SE, Cervero-Liceras F, et al. Integrating cervical cancer with HIV healthcare services: A systematic review. PLoS One. 2017;12(7):e0181156.

12.         Sarah Maria N, Olwit C, Kaggwa MM, Nabirye RC, Ngabirano TD. Cervical cancer screening among HIV-positive women in urban Uganda: a cross sectional study. BMC Womens Health. 2022;22(1):148.

13.         Korn AK, Muzingwani L, O'Bryan G, Ensminger A, Boylan AD, Kafidi EL, et al. Cervical cancer screening and treatment, HIV infection, and age: Program implementation in seven regions of Namibia. PLoS One. 2022;17(2):e0263920.

14.         Afzal O, Lieber M, Dottino P, Beddoe AM. Cervical cancer screening in rural South Africa among HIV-infected migrant farm workers and sex workers. Gynecol Oncol Rep. 2017;20:18-21.

15.         Jansen EEL, Zielonke N, Gini A, Anttila A, Segnan N, Vokó Z, Ivanuš U, McKee M, de Koning HJ, de Kok IMCM; EU-TOPIA consortium. Effect of organised cervical cancer screening on cervical cancer mortality in Europe: a systematic review. Eur J Cancer. 2020 Mar;127:207-223. doi: 10.1016/j.ejca.2019.12.013. Epub 2020 Jan 21. PMID: 31980322.

16.         Rohner E, Mulongo M, Pasipamire T, Oberlin AM, Goeieman B, Williams S, et al. Mapping the cervical cancer screening cascade among women living with HIV in Johannesburg, South Africa(a). Int J Gynaecol Obstet. 2021;152(1):53-9.

17.         Pry JM, Manasyan A, Kapambwe S, Taghavi K, Duran-Frigola M, Mwanahamuntu M, et al. Cervical cancer screening outcomes in Zambia, 2010–19: a cohort study. The Lancet Global Health. 2021;9(6):e832-e40.

18.         Taghavi K, Mandiriri A, Shamu T, Rohner E, Bütikofer L, Asangbeh S, et al. Cervical Cancer Screening Cascade for women living with HIV: A cohort study from Zimbabwe. PLOS Global Public Health. 2022;2(2):e0000156.

19.         World Health Organization. Monitoring national cervical cancer prevention and control programmes: quality control and quality assurance for visual inspection with acetic acid (VIA)-based programmes. World Health Organisation, 2013.

20.         World Health Organization. Improving data for decision-making: a toolkit for cervical cancer prevention and control programmes. Geneva: World Health Organization; 2018. Licence: CC BY-NC-SA 3.0 IGO.

21.         World Health Organization. (‎2018)‎. HIV strategic information for impact: cascade data use manual: to identify gaps in HIV and health services for programme improvement: user manual. World Health Organization. https://apps.who.int/iris/handle/10665/273119. Lizenz: CC BY-NC-SA 3.0 IGO

22.         Bruni L, Saura-Lazaro A, Montoliu A, Brotons M, Alemany L, Diallo MS, et al. HPV vaccination introduction worldwide and WHO and UNICEF estimates of national HPV immunization coverage 2010-2019. Prev Med. 2021;144:106399.

23.         Amponsah-Dacosta E, Kagina BM, Olivier J. Health systems constraints and facilitators of human papillomavirus immunization programmes in sub-Saharan Africa: a systematic review. Health Policy Plan. 2020;35(6):701-17.

24.         Zheng L, Wu J, Zheng M. Barriers to and Facilitators of Human Papillomavirus Vaccination Among People Aged 9 to 26 Years: A Systematic Review. Sexually Transmitted Diseases. 2021;48(12):e255-e62.

25.         Toor J, Li X, Jit M, Trotter CL, Echeverria-Londono S, Hartner AM, et al. COVID-19 impact on routine immunisations for vaccine-preventable diseases: Projecting the effect of different routes to recovery. Vaccine. 2022;40(31):4142-9.

26.         Shet A, Carr K, Danovaro-Holliday MC, Sodha SV, Prosperi C, Wunderlich J, et al. Impact of the SARS-CoV-2 pandemic on routine immunisation services: evidence of disruption and recovery from 170 countries and territories. Lancet Glob Health. 2022;10(2):e186-e94.

27.         Spayne J, Hesketh T. Estimate of global human papillomavirus vaccination coverage: analysis of country-level indicators. BMJ Open. 2021;11(9).

28.         Taghavi K, Mandiriri A, Shamu T, Rohner E, Bütikofer L, et al. Cervical Cancer Screening Cascade for women living with HIV: A cohort study from Zimbabwe. PLOS Global Public Health 2022 2(2): e0000156. https://doi.org/10.1371/journal.pgph.0000156

29.         Lee H, Kang Y, Ju W. Cervical Cancer Screening in Developing Countries: Using Visual Inspection Methods. Clin J Oncol Nurs. 2016;20(1):79-83.

30.         Marth C, Landoni F, Mahner S, McCormack M, Gonzalez-Martin A, Colombo N, et al. Cervical cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2017;28(suppl_4):iv72-iv83.

31.         Erwin E, Aronson KJ, Day A, Ginsburg O, Macheku G, Feksi A, et al. SMS behaviour change communication and eVoucher interventions to increase uptake of cervical cancer screening in the Kilimanjaro and Arusha regions of Tanzania: a randomised, double-blind, controlled trial of effectiveness. BMJ Innov. 2019;5(1):28-34.

32.         Wanyoro AK, Kabiru EW. Use of Mobile Phone Short Text Message Service to Enhance Cervical Cancer Screening at Thika Level 5 Hospital, Kiambu County, Kenya: A Randomised Controlled Trial. Journal of Obstetrics and Gynaecology Research. 2017; 10.5923.j.rog.20170501.03.

33.         Adedimeji A, Ajeh R, Pierz A, Nkeng R, Ndenkeh JJ, Fuhngwa N, et al. Challenges and opportunities associated with cervical cancer screening programs in a low income, high HIV prevalence context. BMC Womens Health. 2021;21(1):74.

34.         Owenga JA, Nyambedha EO. Perception of Cervical Cancer Patients on their Financial Challenges in Western Kenya. BMC Health Serv Res. 2018;18(1):261.

35.         Drummond JL, Were MC, Arrossi S, Wools-Kaloustian K. Cervical cancer data and data systems in limited-resource settings: Challenges and opportunities. Int J Gynaecol Obstet. 2017;138 Suppl 1:33-40.

36.         White HL, Meglioli A, Chowdhury R, Nuccio O. Integrating cervical cancer screening and preventive treatment with family planning and HIV-related services. Int J Gynaecol Obstet. 2017;138 Suppl 1:41-6.

37.         Davidović M, Asangbeh SL, Taghavi K, Dhokothera T, Jaquet A, Musick B, Schwappach D, Wools-Kaloustian K, Anastos K, et al. Facility-based Indicators to Manage and Scale Up Cervical Cancer Prevention And Care Services For Women Living With HIV In Sub-Saharan Africa: Three-Round Modified Delphi Consensus Method. 2022 Unpublished.

38.         Walther B, Hossin S, Townend J, Abernethy N, Parker D, Jeffries D. Comparison of electronic data capture (EDC) with the standard data capture method for clinical trial data. PLoS One. 2011;6(9):e25348. doi: 10.1371/journal.pone.0025348. Epub 2011 Sep 23. PMID: 21966505; PMCID: PMC3179496.