Cervical Cancer Screening Cascade in Côte d’Ivoire: A Decade of Real-World Program Evaluation According to HIV Status

Abstract

PURPOSE

We assessed progress toward WHO 2030 Cervical Cancer (CC) elimination targets including 70% coverage for CC screening and 90% of precancerous lesions treated according to HIV status in Côte d’Ivoire during the 2010-2021 period.

METHODS

A national CC screening registry was initiated in Côte d’Ivoire since 2010, collecting individual-level data from all health facilities offering visual inspection with acetic acid (VIA). The CC screening coverage was estimated based on the 2021 population census and the HIV national database in women aged 25-49 years from the general population and in women with HIV (WLHIV). CC screening and care cascade indicators were documented over time and compared according to HIV status. Access to same-day cryotherapy and associated factors were analyzed through a logistic regression model.

RESULTS

A total of 66,268 women received CC screening, with 11,251 (17.0%) being WLHIV. The estimated CC screening coverage was 4.4% (2.6-5.2), rising to 13.9% (13.5-15.3) in WLHIV. Overall, VIA positivity was 6.4% (6.2-6.5) and was higher in WLHIV (9.1% [8.6-9.7]), P < .001. Among VIA-positive women, 3,500 (83.1%) were eligible for same-day cryotherapy. Access to cryotherapy was 59.1%, declining over time from 71.7% before 2015 to 51.9% in 2021. Access to cryotherapy was higher in WLHIV (aOR, 1.55 [95% CI, 1.32 to 1.84]) and women screened in secondary-level (aOR, 1.82 [95% CI, 1.49 to 2.23]) or tertiary-level facilities (aOR, 1.79 [95% CI, 1.54 to 2.09]) versus primary level.

CONCLUSION

Despite major achievements in this 11-year implementation of the CC screening program in Côte d’Ivoire, performances remained low regardless of HIV status and far from elimination targets in 2021. These findings underline the need to endorse new screening strategies based on HPV testing and thermal ablation treatment at a national level.

BACKGROUND

Cervical cancer (CC) is one of the most common cancers among women worldwide, particularly in low- and middle-income countries, with sub-Saharan Africa (SSA) bearing one of the highest burden.¹ Women living with HIV (WLHIV) are at a six-times higher risk of CC compared with their HIV-uninfected counterparts.² Despite a global reduction in new HIV infections and decline in HIV-related deaths achieved in recent years through the implementation of the WHO 95-95-95 strategies, CC incidence and mortality continue to be substantially high in WLHIV.³ In Côte d’Ivoire, CC remains the deadliest female cancer, and WHO predicts an increase of 47.5% in CC-related mortality rate by 2040.^1,4

CONTEXT

• Key Objective

• To report on progresses of an 11-year cervical cancer (CC) screening program implementation among women with or without HIV in Côte d’Ivoire.

• Knowledge Generated

• Women participation increased over time. Access to timely cryotherapy was suboptimal, higher in women with HIV, and higher in those screened in tertiary or secondary compared with primary-level facilities.

• Relevance

• Although CC screening programs are becoming more widely available, reflecting the efforts of clinical and community health workers, coverage estimates remain low. Effectively integrating screening into primary health care services must be improved. Limited access to same-day cryotherapy highlights a critical clinical gap, as delays in treatment increase the risk of loss to follow-up and disease progression. These findings emphasize the urgent need to improve investments in the health system, particularly at primary care level, to strengthen screening capacity and ensure timely treatment by promoting thermal ablation, which should be more logistically resilient than cryotherapy.

In 2021, the WHO published its global CC elimination initiative, relying on three pillars: 90% of girls are vaccinated before age 15; 70% of women are screened using a high-performance test at ages 35 and 45; and 90% of those with preinvasive or invasive lesions access appropriate care.⁵ In Côte d’Ivoire, several CC screening (CCS) initiatives have been launched in 2009 with initial pilot projects targeting WLHIV in selected health counties in Abidjan, the country’s economic capital.⁶ Since 2012, CCS programs progressively extended outside HIV clinics as well as outside Abidjan, targeting all women of age 25-55 years.⁷ This program based on Visual Inspection with Acetic acid (VIA) and cryotherapy was initially supported by international or implementing partners, and subsequently endorsed by the Ministry of Health (MoH) through the first national guidelines for CC prevention edited in 2013.⁸ A previous evaluation of this program demonstrated early successes in the scale-up of CCS in Abidjan but also pointed out potential challenges, especially the need to expand access to screening and the sustainability of the see and-treat approach.⁷

Similar to Côte d’Ivoire, a number of countries in SSA have implemented CCS services over the last decade through scaling up pilot project integrated in HIV care, at multifacility or subnational levels.^9,10 However in many contexts, the CCS uptake remains low.¹¹ Monitoring systems are weak, insufficient to provide evidence-based information on strategies to reduce the CC burden, overall as well as in highly affected population such as WLHIV.^12,13 The need to measure performance indicators of CCS programs is therefore a high priority, especially in West Africa, in view of the WHO CC elimination targets to be reached by 2030.

Here, we report successes and challenges according to HIV status in Côte d’Ivoire through one of a few national CCS registries in SSA. We aim at providing updated estimates of CCS coverage and access to precancerous lesions treatment according to HIV status, as well as their correlates in Côte d’Ivoire.

METHODS

Design and Settings

The CASCADE project is an initiative to build a CCS registry, collecting standardized individual-level data from all health facilities offering VIA.

Since 2010, all CCS visits at any health facility are documented through a standardized paper-based case report form (CRF) under the supervision of the National Cancer Control Program (NCCP). We undertook to digitalize retrospectively all patient-level data from the Ivorian national CCS program conducted over the 2010-2021 period. CCS registry was initiated, collecting standardized individual-level data from all health facilities offering VIA.

All women attending one of the CCS facilities in the administrative regions of Abidjan, Bouake, and Daloa (the three most inhabited cities) for an initial screening and eligible for a CCS according to the national guidelines were included.⁸ During the 2010-2021 period, all women age 25-55 years or adult (>18 years) WLHIV until 55 years attending health facilities for an initial VIA were included. In the event of a positive test result involving a nonextensive aceto-white lesion, a same-day cryotherapy was recommended. Otherwise, a referral system was implemented to enable women requiring loop electrosurgical excision procedure (LEEP) for extensive lesions or postponed cryotherapy to receive treatment at another facility within the three regions. The same CRF, also called individual screening form, has been used since 2010 to capture data on initial screening visits and the outcomes of subsequent visits.

Data Collection and Management

All health facilities identified by the NCCP, from both the public and private sectors, across all levels of health system, including those integrated into HIV care and maternal health services, were subsequently requested to provide their CRFs, as well as their registers of women attending for CCS in each region. All provided CRFs (irrespective of the eligibility criteria) were digitalized by trained staff, using a dedicated REDCap electronic data capture tool, a secure Web application for building and managing online surveys and databases.^14,15

The CRFs documented individual-level data, HIV status (Appendix), history of tobacco consumption, the purpose of the visit (initial screening, routine screening, postponed cryotherapy, and post-treatment surveillance), the screening method, and outcomes. Interestingly, VIA was the main screening method used throughout the health system, from primary- to tertiary-level care levels over time. However, tertiary-level hospitals continue to offer VIA to all eligible clients while recommending the Pap test to women during antenatal and fertility check-ups, or to those age over 55 years, not captured by the national screening program.

During CCS visits, a systematic HIV testing was recommended to be offered by health care providers in charge of documenting the result and linking clients to specialized or integrated HIV care for initiation of antiretroviral treatment therapy in cases of newly diagnosed HIV, as part of the national HIV guidelines. Among VIA-positive women, eligibility for cryotherapy or LEEP, procedure timing (same-day or referred), reasons for delay, and referral facility were recorded on the initial CRF. The CRF (Data Supplement, File S1) also captured the level of the health facility in the sanitary pyramid, its social status and level of integration regarding the health services (HIV care, sexual and reproductive care, maternal care, etc), and the quality of the provider.

To minimize missing data, a two-step procedure was applied. A primary tracking of duplicates was ensured at the facility level using individual information (name, age, residency) in the REDCap search function before any new entry within CCS facilities. When the tracking retrieved a proof of a previous visit, the purpose of the visit was updated accordingly (corrected to routine VIA or a post-treatment visit). A second automated electronic tracking process was used to identify and merge duplicate records where it was established that the same ID had been used for different purposes. Alternatively, the IDs were split into two electronic records when an identification error was formally noted. Perfect duplicates, defined as records for women with the same CCS visit purpose on the same day, were deleted. Ultimately, aberrant captured CRFs (age outside the guidelines or persistently incomplete records for key variables, despite multiple requests to providers) were deleted before the analysis.

The primary CCS visits were chained with follow-up visits using a probabilistic algorithm including information on name, age, home address, and mobile phone when available.

Data Analysis

For CCS coverage estimates, the 2021 National census of population and housing (RGPH 2021) was obtained from the National Institute of Statistics (INS) to estimate the number of eligible women living in three administrative regions. Using the cumulated number of women screened in these area since the initiation of the CCS, we estimated CCS coverage with their 95% CI. Additionally, an extraction from the national database of people living with HIV (SPECTRUM 2021) provided the number of adult WLHIV to specifically estimate the CCS coverage in that specific population.

Numerical variables were described as median and IQR, whereas categorical variables were described as frequencies with percentages. CCS and care cascade indicators were described as proportions and compared according to HIV status, using chi-square test. Results with a P value < .05 were considered statistically significant.

Access to same-day cryotherapy was calculated among women with a positive VIA test and eligible for cryotherapy (nonextensive aceto-white lesion). A logistic regression model was used to analyze factors associated with access to same-day cryotherapy. Independent variables were facility-level (health facility level in health pyramid, level of HIV care integration, provider, location) and patient-level data (age, educational level, number of living births, HIV status). In bivariate analysis, variables with a P value <.25 and/or HIV status were considered in multivariable analysis. Finally, those with a P value < .05 were independently associated with VIA positivity and access to same-day cryotherapy. STATA 16.0 (StataCorp, College Station, TX) was used for statistical analysis.

Ethical Aspects

An approval to conduct this study was obtained from the Ivorian National Ethics Committee (Ref 00069_24/MSHPCMU/CNESVS-km). The MoH through the NCCP gave an authorization to conduct the study and also took part in all stages of the project. The database was anonymized before analyses.

RESULTS

Population Characteristics

A total of 68,118 initial visits were recorded in the CC screening database. Finally, 66,268 women were effectively screened according to national guidelines including 11,251 (17.0%) WLHIV (Fig 1).

FIG 1.

Flow chart describing women inclusion, the CASCADE project, 2010-2021. CC, cervical cancer; VIA, visual inspection with acetic acid.

At their first screening, women were aged 34 years (IQR, 28-41) in median: 33 (IQR, 27-40) in HIV-uninfected/unknown women and 37 (IQR, 32-42) in WLHIV, P < .001 (Table 1).

TABLE 1.

Women Attending Cervical Cancer Screening and Facility Characteristics in Côte d’Ivoire, 2010-2021

Characteristic	Total (N = 66,268), No. (%)	HIV-Uninfected Women (N = 55,017), No. (%)	HIV-Infected Women (N = 11,251), No. (%)	P
Age, median (IQR)	34 (28.0-41.0)	33 (27.0-40.0)	37.0 (32.0-42.0)	<.001
<30	20,449 (30.9)	18,879 (34.3)	1,570 (14.0)
30-40	25,708 (38.8)	20,525 (37.3)	5,183 (46.1)
40-55	19,495 (29.4)	15,103 (27.5)	4,392 (39.0)
Missing	616 (0.9)	510 (0.9)	106 (0.9)
Residency				<.001
Abidjan	44,848 (67.7)	34,910 (63.5)	9,938 (88.3)
Bouake	7,460 (11.3)	6,715 (12.2)	745 (6.6)
Daloa	13,960 (21.0)	13,392 (24.3)	568 (5.1)
Educational level				<.001
No or primary level	13,112 (19.8)	12,303 (22.4)	809 (7.2)
Secondary level or university	14,091 (21.2)	13,496 (24.5)	595 (5.3)
Missinga	39,065 (59.0)	28,467 (53.1)	9,702 (87.5)
Number of living births				<.001
0-1	6,235 (9.4)	5,979 (10.9)	256 (2.3)
2-4	17,642 (26.6)	16,687 (30.3)	955 (8.5)
≥5	8,154 (12.3)	7,804 (14.2)	350 (3.1)
Missinga	34,237 (51.7)	24,547 (44.6)	9,690 (86.1)
Tobacco use				.007
No use	65,866 (99.4)	54,663 (99.4)	11,203 (99.6)
Current or former use	402 (0.6)	354 (0.6)	48 (0.4)
According to the health pyramid level				<.001
Primary	45,691 (69.0)	37,707 (68.5)	7,984 (71.0)
Secondary	8,040 (12.1)	7,469 (13.6)	571 (5.0)
Tertiary	12,537 (18.9)	9,841 (17.9)	2,696 (24.0)
Integration of health facility				<.001
Maternal and child clinic	17,175 (25.9)	16,509 (30.0)	666 (5.9)
HIV clinic	4,778 (7.2)	1,046 (1.9)	3,732 (33.1)
Integrated services	43,753 (66.0)	36,906 (67.1)	6,847 (60.9)
Private/NGO sector	562 (0.9)	556 (1.0)	6 (0.1)
Quality of health provider				<.001
Nurse/Midwife	57,952 (87.4)	49,675 (90.3)	8,277 (73.6)
Physician	8,316 (12.6)	5,342 (9.7)	2,974 (26.4)

Abbreviations: CRF, case report form; NGO, nongovernmental organization.

^a CRF was updated in 2015 by integrating education and number of living births, justifying missing data.

Of the 66,289 women, 45,691 (69%) were offered VIA in a primary health care facility. Screening was conducted in an integrated facility for 43,753 women (66.0%), within maternal and child care programs for 17,175 (25.9%), and in HIV clinics for 4,778 (7.2%). The main CCS providers were midwives (87.4%; Table 1).

CCS Coverage Estimates

The program began with 2,376 women screened in 2010 and increased to 4,624 in 2021. The proportion of WLHIV screened for CC ranged from 76.5% to 4.7% compared with HIV-uninfected/unknown women. The estimated CCS coverage (lifetime screening) was 4.4% (95% CI, 2.6 to 5.2), ranging from 3.5% (95% CI, 3.4 to 3.5), 4.9% (95% CI, 4.8 to 5.1), and 18.9 (95% CI, 18.6 to 19.2) in Abidjan, Bouake, and Daloa, respectively. In WLHIV, the estimated CCS coverage was 13.9% (95% CI, 13.5 to 15.3), including 14.5% (95% CI, 14.2 to 14.8) in Abidjan, 10.1% (95% CI, 12.4 to 14.0) in Bouake, and 14.1% (95% CI, 13.0 to 15.2) in Daloa.

VIA Positivity and Associated Factors

VIA positivity rate was 6.4% (95% CI, 6.2-6.5), and was higher in WLHIV (9.1% [95% CI, 8.6 to 9.7]) compared with their HIV-uninfected/unknown counterparts (5.8% [95% CI, 5.6 to 7.0]), P < .001. VIA positivity showed similar trends over years, being higher in WLHIV. The highest prevalence was found in 35-39 and 40-44 (7.2% and 6.9%, respectively). Among the 4,210 VIA-positive women, 3,500 (83.1%) were eligible for same-day cryotherapy overall and 83.9% in WLHIV (P = .007). Age groups (aOR, 1.42 [95% CI, 1.21 to 1.66]), HIV status (aOR, 2.37 [95% CI, 1.94 to 2.87]), and parity (aOR, 1.32 [95% CI, 1.14 to 1.54]) were independently associated with VIA positivity (Figs 2 and 3).

FIG 2.

Trend in initial Cervical Cancer screening program participation during the 2010-2021 period in Côte d’Ivoire, according to HIV status, the CASCADE Study.

FIG 3.

Trends in VIA positivity, eligibility for cryotherapy, and access to same-day cryotherapy over the 2010-2021 period according to HIV status, the CASCADE Study. VIA, visual inspection with acetic acid.

Access to Treatment and Associated Factors

Same-day cryotherapy rate was 59.1% (57.1%) in HIV-negative/unknown women and 65.2% in WLHIV, (P < .001) but declined over time from 71.7% before 2015 to 51.9% in 2021. In WLHIV, it decreased from 72.8% to 44.2% (P < .001), but was higher in those screened in HIV-specialized clinics (81.6%) versus HIV-integrated facilities (53.2%, P < .001). Access to same-day cryotherapy decreased over time regardless of HIV status but with major disruption observed over time in WLHIV. Reasons for delayed cryotherapy were lack of equipment or disruption of gas (97.9%), women refusal (1.4%), and the need to get consent from sexual partners (0.7%).

In multivariable analysis, access to same-day cryotherapy was higher in WLHIV (aOR, 1.49 [95% CI, 1.26 to 1.76]) and women screened at secondary-level (aOR, 2.04 [95% CI, 1.61 to 2.61]) or tertiary-level facilities (aOR, 1.62 [95% CI, 1.38 to 1.91]) compared with primary-level facilities, and in those age 30-40 years at screening (aOR, 1.27 [95% CI, 1.07 to 1.50]) compared with the youngest category (Table 2).

TABLE 2.

Factors Associated With Access to Same-Day Cryotherapy in VIA-Positive Women

Variable	Access to Same-Day Cryotherapy, No. (%)	Bivariate Model			Multivariable Model
		OR	(95% CI)	P	aOR	(95% CI)	P
Age at screening, years				.002			.010
<30	537 (56.0)	1
30-40	922 (62.0)	1.32	(1.12 to 1.56)		1.27	(1.07 to 1.50)
40-55	598 (58.0)	1.10	(0.92 to 1.31)		1.06	(0.88 to 1.27)
HIV status				<.001			<.001
Negative/Unknown	1,521 (57.0)	1			1
Positive	546 (65.0)	1.41	(1.20 to 1.66)		1.49	(1.26 to 1.76)
Health pyramid level				<.001			<.001
Primary	918 (53.0)	1			1
Secondary	364 (65.0)	1.67	(1.37 to 2.04)		2.04	(1.61 to 2.61)
Tertiary	785 (66.0)	1.73	(1.49 to 2.01)		1.62	(1.38 to 1.91)
Region				<.001			.004
Abidjan	1,583 (57.0)	1
Bouake	324 (69.0)	1.62	(1.32 to 2.00)		1.40	(1.12 to 1.75)
Daloa	160 (59.0)	1.07	(0.83 to 1.38)		0.79	(0.58 to 1.08)

Abbreviation: VIA, visual inspection with acetic acid.

DISCUSSION

This field evaluation showed low CCS coverage estimates and a suboptimal access to same-day cryotherapy in Côte d’Ivoire over the 2010-2021 period.

Our estimates of CCS coverage are in line with previous estimates that ranged from 2% to 6%.^11,16,17 Estimates from a Demographic and Health Survey (DHS) conducted in Côte d’Ivoire reported 5.6% of women of childbearing age declaring a previous lifetime CCS.¹⁶ However, the DHS approach may have overestimated CCS coverage as these assessments relied on declared attendance with no information on effective screening uptake. Reports from systematic reviews based on empirical data estimated that 2% of women received a lifetime CCS in Côte d’Ivoire.^11,17 Considering that the current scale-up of CCS covers around half of the targeted population, these last estimates support the 4% access to a lifetime CCS estimates in eligible women where VIA-based screening was available. Although SSA harbors a low CCS uptake coverage, estimated globally around 13%,¹⁸ Western and Central African countries performed significantly worse (6%) compared with Eastern (13%) and Southern Africa (51%).^11,16 These results highlight the substantial need for increased regional MoH investments in screening to close the gap towards elimination. It has been estimated that incremental costs needed to meet the 70% CCS target should be expanded by a factor 35 at a national level.¹⁷

The CCS coverage estimates were also low in WLHIV compared with reports from SSA,¹⁹ with up to a CCS coverage of 29.4% in western Kenya²⁰ or 25.3% in Zambia.²¹ Access to CSS over time also showed a stagnation in WLHIV, as seen in Kenya,²⁰ suggesting that WLHIV would become increasingly difficult to reach with traditional strategies. In this evaluation, seven of 10 women were screened in a primary health care facility. Screening of CC through primary facilities must be empowered to bring services closer to targeted women. The global aging of HIV cohorts, thanks to major improvement of life expectancy in people living with HIV over the last decade,²² could partly explain access to CCS at an older age for WLHIV compared with uninfected women.^23,24

Our study reports that two-thirds of women eligible to a see-and-treat approach received a same-day cryotherapy. This outcome varied over time, probably due to many structural barriers such as an insufficient investment to ensure a sustained access to cryotherapy equipment. Access to cryotherapy was globally low compared with the 84% reported treatment rate in SSA, particularly in Zambia (90%), Malawi (77%), Tanzania (90%), and Cape Verde (82%),¹¹ but was higher compared with Kenya’s experience (40%).¹⁰ Although access to treatment was higher in WLHIV as demonstrated earlier in Abidjan,⁷ it declined over time regardless of HIV status. A 20-point reduction was observed between the early period of the program, supported by implementing partners, and the latest period where funding support was progressively transferred to MoH.⁷ During this last period, the program was hampered by regular shortage of gas supply and cryotherapy logistical issue as well as a low maintenance system in regions. These issues were particularly common in primary care facilities already less equipped and far from maintenance institutions. Protective mechanisms should be developed for primary health care facilities. In addition, the referral mechanisms should be strengthened and monitored to ensure all women with postponed treatment effectively receive it.

Ultimately, our analysis paves the way for several perspectives. HPV-based screening program and treatment through thermal ablation are now the gold standard for SSA countries.⁵ The potential of HPV testing, with the advantage of self-sampling option, could be a key additional approach to enhance screening coverage.²⁵ The scale-up of this approach must overcome clear challenges, primarily related to the cost and logistic issues of HPV tests and machines. The implementation of monitoring/tracing strategies for positively screened women should be a priority, as the Ivorian NCCP is now recommending HPV tests as a preferred primary screening method.

The replacement of cryotherapy by thermal ablation in the 2024 national guidelines is an opportunity to improve the treatment rate among women with precancerous lesions, irrespective of their HIV status. Thermocoagulators should be provided in all health care facilities prioritizing those from primary and secondary care level.²⁶ The integration of CC secondary prevention strategies in the current universal health coverage could put the country on track to achieve both screening and treatment elimination targets by 2030. Finally, the CCS registry initiated must be consolidated to ensure sustained national monitoring of the program, timely data analysis for evidence-based policy, and the development of tailored interventions.

Our study has some limitations. Unfortunately, there is no yearly national census in Côte d’Ivoire and the HIV database was no longer available before 2016. Given that the population is predominantly young (75.6% are under age 35 years), and the increase in the adult female population between the two censuses was less than 10% (7.6%, from 1,228,020 in 2014 to 1,321,679 in 2021), we assumed that the proportion of women eligible for CCS would not significantly change throughout the study period.²⁷ Indeed, these estimates could inform policy makers on progress since the first evaluation (2010-2014) and the outcome of the implementation of future CCS strategies. Furthermore, a HIV clinic in Bouaké reported having lost 2 years' worth of CCS records, whereas another clinic in a university hospital was unable to provide screening records for a year due to refurbishments. Additionally, updates of the monitoring tools in 2015 resulted in missing data for new variables, limiting the full exploration of the patterns of key CCS outcomes. We were not also able to document missed opportunities of CCS among women attending health facilities for other purposes as the study was not designed in this way.

Nevertheless, this evaluation is one of the comprehensive evaluations in West Africa that explores the effect of HIV status on key performances of a subnational population-based CCS program over a large implementation period. The inclusion of almost all of the health facilities and campaign activities suggests a good capitalization of programmatic data.

In conclusion, this study demonstrated major achievements in building an 11-year-old real-life CCS program in Côte d'Ivoire. However, CCS program performances remained low, regardless of HIV status. Wider integration of screening strategies is needed to improve access to CCS. Access to treatment was suboptimal, but possibly within the reach of the 2030 target if new investments become effective. Overcoming delivery gaps and implementing monitoring/tracing strategies for positively screened women should be prioritized. The transition from screen-and-treat to HPV-based test, triage and treat approaches needs to be carefully negotiated to maximize current resources while making new progresses, in the view of achieving the WHO CC elimination targets.

APPENDIX

HIV Status in CASCADE Study

Per national guidelines, HIV testing algorithm relies on a primary rapid HIV diagnostic test (RDT) that provides accurate and instant results. In case of positive RDT, additional blood is sampled to run a confirmatory test. As CCS follow-up schedules relied on HIV status, all women attending CCS were counseled to disclose their status and/or take an HIV test (when consumables were available at the facility). The results of the HIV tests or the women's HIV status were reported on the CCS form on the same day.

Inclusion Criteria

Between 2010 and 2021, a total of 68,118 initial visits were recorded in the CC screening database. After exclusion of incomplete records for key data such as identifiers, VIA realization, and outcomes (0.5%), we subsequently excluded 30 records for follow-up visits. Indeed, the tracking process managed 67,791 CC screening records and retrieved 67,761 women attending the health facility for an initial CCS. Women who did not undergo VIA for any reasons (1.3%) and 0.9% women outside the recommended target (aged <18 or >55) were consecutively excluded. Among women recused for VIA, 212 were directly referred for a suspected cervical cancer. Finally, 66,268 women were effectively screened according to national guidelines including 11,251 (17.0%) WLHIV (Fig 1).

VIA Positivity

Our study did not focus on VIA positivity. Substantial evidence exists of a high VIA positivity rate in Africa (11.9%), as well as a higher risk among WLHIV compared with women without HIV,²⁹ and among 35- to 44-year-old women compared with younger age groups.³⁰ However, when considering particularly WLHIV, the overall rate of VIA positivity was quite similar to that reported earlier in Abidjan,⁷ but higher compared with the Eswatini prevalence of 2.6%.³⁰

Trends in CC Screening Visits

The CCS registry of Cote d’Ivoire also offers the opportunity to analyze trends over time. The participation in the CCS program has increased over time during the considered period, probably resulting from an increase of CC-related information concurrently given with breast cancer messages during national awareness events such as Pink October, as per the civil society mobilization. More screening providers were also trained in health counties, yielding new CCS facilities in the regions we evaluated. Unfortunately, the rapid scale-up of CCS facilities opened at the beginning of the program in the three administrative regions did not expand as expected over time. Worse still, of the 27 centers that contributed to the first evaluation of the program in Abidjan during the 2010-2014 period,⁷ six provided fewer than 100 screening visits per year due to irregular activity related to shortages in health care provider and/or closure of the health facility's screening unit. Efforts from national health authorities faced persistent barriers, including those probably specific to Ivorian context (ie, political events) and structural ones common to SSA contexts.

Variation in Same-Day Cryotherapy

A 20-point reduction was observed between the early period of the CC prevention program, supported by implementing partners, and the later period, when funding support was progressively transferred to local authorities.⁷ During this last period, performances of the screening program were hampered by regular shortage of gas supply and cryotherapy logistical issue as well as a low maintenance system in implementing regions. These issues were particularly common in primary care facilities already less equipped and far from maintenance institutions, generally at the regional and central office of the Ministry of Health. Finally, the lack of continued investment in equipping health facilities in treatment devices and ensuring regular maintenance of cryotherapy probes were the main barriers. The resilience of the program was tested, particularly during the withdrawal of funders (2016-2020). Globally, weaknesses of the health system response were observed during that period, except in few tertiary- or secondary-level screening units which succeeded in ensuring gas supply and maintaining cryotherapy probes. Protective mechanisms should be developed for primary health care facilities, already repositioned at frontline for accelerating CC elimination. The referral mechanisms should be strengthened and monitored to ensure all women with postponed treatment effectively receive cryotherapy/thermal ablation, even loop electrosurgical excision procedure.

Site Investigators and Cohorts

Adult cohorts: Marcel Djimon Zannou, CNHU, Cotonou, Benin; Armel Poda, CHU Souro Sanou, Bobo Dioulasso, Burkina Faso; Oliver Ezechi, National Institute of Medical Research (NIMR), Lagos, Nigeria. Eugene Messou, ACONDA CePReF, Abidjan, Cote d’Ivoire; Henri Chenal, CIRBA, Abidjan, Cote d’Ivoire; Kla Albert Minga, CMSDS, Abidjan, Cote d’Ivoire; Aristophane Tanon, CHU Treichville, Cote d’Ivoire; Moussa Seydi, CHNU de Fann, Dakar, Senegal; Ephrem Mensah, Clinique EVT, Lomé, Togo. Bem Tar, Federal Medical Center, Makurdi, Nigeria; James Samuel, Jos University Teaching Hospital, Nigeria; Muyiwa Ojo-osagie, University College Hospital, Ibadan, Nigeria; Azeez Ayotunde Federal Medical Center, Abeokuta, Nigeria; Sheriff, Bolanle Yemisi Alabi, State Specialist Hospital, Akure, Nigeria; Pediatric cohorts: Caroline Yonaba, CHU Yalgado Ouadraogo; Lehila Bagnan, CNHU, Cotonou, Benin; Jocelyn Dame, Joycelyn Assimeng Dame, Korle Bu Hospital, Accra, Ghana; Sylvie Marie N'Gbeche, ACONDA CePReF, Abidjan, Ivory Coast; Kouadio Kouakou, CIRBA, Abidjan, Cote d’Ivoire; Madeleine Amorissani Folquet, CHU de Cocody, Abidjan, Cote d’Ivoire; François Tanoh Eboua, CHU de Yopougon, Abidjan, Cote d’Ivoire; Mariam SYLLA, Hopital Gabriel Toure, Bamako, Mali; Oliver Ezchechi, Agatha David, Rosemary Audu, NIMR, Lagos, Nigeria; Elom Takassi, CHU Sylvanus Olympio, Lomé,Togo. Ahula David, Victor Ojeh Bazim, Federal Medical Center, Makurdi, Nigeria; Jos University Teaching Hospital, Nigeria; Olarenwaju Ogunyide, University College Hospital, Ibadan, Nigeria; Mariam Moji Ogundeyi, Federal Medical Center, Abeokuta, Nigeria; Olaseinde Bello, State Specialist Hospital, Akure, Nigeria.

Regional Coordination

Antoine Jaquet (PI), Didier Koumavi Ekouevi (PI), François Dabis, Charlotte Bernard, Sophie Labarriere, Karen Malateste, Olivier Marcy, Marie Kerbie Plaisy, Elodie Rabourdin, Thierry Tiendrebeogo. ADERA, University of Bordeaux, National Institute for Health and Medical Research (Inserm) UMR1219, Research Institute for Sustainable Development (IRD) EMR 271, Bordeaux Population Health Center, Bordeaux, France

Désiré Dahourou, Sophie Desmonde, Julie Jesson, Valeriane Leroy, Emile Sodenyessi. CERPOP, Inserm UMR1295, Toulouse, France

Raoul Moh, Jean-Claude Azani, Kadidja Diarra, Jean Jacques Koffi, Maika Bengali, Abdoulaye Cissé, Guy Gnepa, Eric Komena, Apollinaire Horo, Séverin Lenaud, Simon Boni, Eulalie Kangah, Corinne Moh, Jeanne Eliam, PAC-CI program, CHU Treichville, Abidjan, Côte d’Ivoire.

Partner Institutions

Case Western Reserve University: Igho Ofotokun (PI), Washington University: Noëlle Benzekri, Geoffrey Gottlieb, APIN Public Health Initiatives, Abuja, Nigeria: Prosper Okonkwo, Oluwaseun Olaifa, Uche Okezie.

DATA SHARING STATEMENT

The data for this study are available, and can be provided from NCCP Côte d’Ivoire (www.pnlca.org) upon reasonable request.

AUTHOR CONTRIBUTIONS

Conception and design: Simon Boni, Apollinaire Horo, Innocent Adoubi, Antoine Jaquet

Administrative support: Simon Boni, Mesmin Adie, Innocent Adoubi

Provision of study materials or patients: Simon Boni, David Goore, Mesmin Adie, Apollinaire Horo, Innocent Adoubi

Collection and assembly of data: Simon Boni, David Goore, Mesmin Adie, Franck Gnahatin, Denise Kpebo

Data analysis and interpretation: Simon Boni, Franck Gnahatin, Denise Kpebo, Innocent Adoubi, Antoine Jaquet

Manuscript writing: All authors

Final approval of manuscript: All authors

Accountable for all aspects of the work: All authors

AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

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No potential conflicts of interest were reported.