Recruitment strategies to promote uptake of cervical cancer screening in West Cameroon

World Health Organization’s (WHO) global strategy for cervical cancer elimination has set for 2030 that all countries reach the target of 70% coverage screening rate. Communities’ sensitization through media is often used but community health workers’ (CHW) involvement may contribute to improve screening coverage. We aimed to assess effectiveness and costs of two cervical cancer screening recruitment strategies conducted in a low resource setting. The study was conducted in West region of Cameroon precisely in Dschang Health District, a community of 300’000 people. From September 2018 to February 2020, we recruited and screened women in a cervical cancer single-visit prevention campaign at Dschang District Hospital. For the rst nine months, recruitment was only based on Community Information Channels (CIC) (i.e. street banners). Since the tenth month, participation of CHW was added for recruitment in the community after training for cervical cancer counselling. Population recruitment was compared between the two strategies by assessing the number of recruited women, and direct costs (CHW costs include recruitment, teaching, certication, identication badge, yers, transport, and salary). Interventions’ cost-effectiveness is expressed using an incremental cost-effectiveness ratio (ICER). to zone 1 within CHW group. In the CIC-led intervention, women in zone 1 were more frequently employed (38.1%) and independent workers (33.1%), whereas in zone 2–4, women worked more as farmers (34.1%, 34.4% and 50% respectively). In the CHW-led intervention, most participants were independent workers in zone 1 (34.9%), and farmers in zones 2 (49.4%), 3 (92.3%) and 4 (76.2%). We also found that most unemployed women 0.7% lived in zone 1 and were recruited through CIC. Women coming from zone 1 and recruited through CIC had fewer children than in other zones. Indeed, 49.7% women in zone 1 had between 1–4 children and 45.51% had more than 4 children, while in other subgroups, between 62.5% and 80.95% of participants had more than 4 children. Within the CIC-recruited group, most women who used condoms were in zone 1 (15.2%,) and zone 2 (13.6%). Participants who smoked the most were recruited by CHW and live in zone 2 (7.9%) and in zone 3 (12.8%). Variance in previous CC screening was also shown between women living in urban zones compared to those in rural zones and depending on the recruitment method. Recruited through CIC, 25.45% of women living in zone 1 had a history of previous HPV screening, 15.9% in zone 2, 9.4% in zone 3 and 5.6% in zone 4 (p = 0.092). Rates of previous screening were generally lower in women recruited by CHW, where 7.8% of women in zone 1 had a previous CC screening, 1.2% in zone 2, 2.6% in zone 3 and 1.9% in zone 4 (p = 0.017).


Background
Nearly 90% of cervical cancer (CC) deaths worldwide occur in low-and middle-income countries with a mortality rate almost three times higher than in more economically developed countries. (1) Among countries with the highest CC burden, 19 of the top 20 are located in Sub-Saharan Africa. (2) A key reason for persistent high morbidity and mortality is the lack of su cient screening coverage. (3) The main challenges of introducing an e cient screening program in Sub-Saharan countries are limited resources and health infrastructure, shortage of caregivers, a low level of awareness, and insu cient attention to women's health, especially in rural populations. (4,5) The result is that the vast majority of women cannot access screening and treatment.
In response to this growing problem, the World Health Organization (WHO) has launched the 90-70-90 targets for 2030 with the aim to eliminate cervical cancer. (6) These targets include (i) a coverage of 90% of girls vaccinated, (ii) 70% of women screened, and (iii) treatment of 90% of women identi ed with cervical disease. To reach the second and third WHO target, the recommendation is to use high performance HPV tests and associate screening and immediate treatment if needed ("screen-and-treat" approach). (7,8) Dschang Health District (West Cameroun) is rural, urban and semi-urban community of over 300'000 inhabitant. (9) In September 2018, we implemented a screening and treatment program in Dschang District Hospital, based on a single visit approach called 3T (for Test, Triage and Treat). The program is scheduled for a ve-year period (2018-2023) and follows the WHO's recommendations to screen women between the ages 30-49 years at least once every ve years. According to the national census, we estimated that about 18'000 women should be screened in Dschang Health District to reach the 70% coverage following WHO's "90-70-90 targets" by 2030. (6) Therefore, an annual recruitment of 3'600 women should be obtained to reach the second WHO target.
The strategy includes self-sampling for primary screening with rapid HPV testing (Self-HPV), followed by VIA and Lugol's iodine (VIA/VILI) for triage of HPV-positive women and treatment with thermal ablation or large loop excision of the transitional zone (LLETZ) if required. (10,11) Performance of the program and ultimately its impact on cervical cancer prevention highly depends on the population screening coverage and on reaching the targeted population which may be substantially enhanced by raising awareness with educational interventions. Outreach strategies to encourage participation in prevention program may be viewed as low priority activities and may suffer from a lack of resources by competing with other healthcare issues such as infectious diseases. (12,13) Several challenges are raised regarding the optimal recruitment strategies to reach women about screening information and motivate them to participate. Screening intervention should also consider the large geographic expense and the dispersed population living in these areas and adapted to population needs.
Methods for improving awareness among the community for Community Information Channels (CIC) (advertising, radio, and television) are traditional choices for cervical cancer awareness having the potential to reach a large number of people within a short period of time. However, implication of community health workers' (CHW) living in the community may have contribute for education and motivation improvement in screening coverage. Community health workers' de nition varies according to different cultures and healthcare systems. In Cameroon, they are trusted community members, integrated into the community health system without any formal professional or paraprofessional medical training. (14)(15)(16)(17)(18)(19) The purpose of this study was to analyze and compare the recruitment rate and costs of the two different recruitment strategies.

Methods
Setting -Dschang Health District is divided into 22 health areas, which we separated into 4 zones based on accessibility to the district hospital (e.g. distances, roads, weather, and transportation means available). Zone 1 was de ned as the most accessible area (urban) and Zone 4 the least accessible area (rural).
CIC recruitment -From September 2018 to May 2019, recruitment was entirely based on announcements made in women's associations, churches, and integrated health centers (chief nurses of each center were informed of this project). Local Radio broadcasting was made twice a week for one month. Large street banners were hung at the entrance and exit of the district of Dschang for a few months. In Dschang District Hospital, the project was presented daily to women waiting for their gynecologist' consultation. Upon arrival to the screening unit, a one-hour health education was given by trained midwives.General information on sexual health, as well as precise explanations on HPV and CC, were given. We expected participants to spread information about this campaign to their relatives. The combination of these methods of recruitment is summarized as community information channels (CIC).
CHW recruitment -From June 2019 to February 2020, CHW recruitment strategy was added to CIC intervention. At district level, district health managers were informed about the campaign and invited to participate by recruiting CHW. Selection is based on volunteer application without any prerequisites. CHWs work in their village. They usually have a main job and act as CHW when called during public health activities. An incentive of 600 CFA (1 USD or 2.6 2021Int'l$) per woman recruited from June to September 2019 was given, which was then increased to 1000 CFA (1.68 USD or 4.3 2021Int'l$) since October 2019 to adequately cover cellphone and transportation fees. CHW were enrolled in a two-day multi-modal training based on the "WHO Toolkit for improving CWH Program and Service" (20,21) and adapted to local barriers by regional caregivers. To differentiate CHW recruitment from CIC, CHW were given invitation vouchers to distribute to each woman they approached. CHW's received their incentive according to their respective number of vouchers returned by participants attending screening.
Data collection -Before completing their HPV test, participants lled a sociodemographic questionnaire distributed by midwives.
Inclusion -We included for this analysis all women aged 30 to 49 years old living within Dschang's Health District or its surroundings who completed an HPV test and signed our consent form, from September 2018 to February 2020. Exclusion criteria for HPV screening were pregnancy, hysterectomy, and vaginal bleeding. To include women in the CHW recruitment group, they had to present a CHW invitation voucher.
Outcome measures -(i) A comparison of sociodemographic characteristics of women recruited by each method was performed with in-depth analysis for each zone of origin. (ii) The number of participants screened was assessed and costs for the implementation of CHW and CIC interventions compared and (iii) To assess the cost-effectiveness of CHW, the costs and screening recruitment outcomes associated with each intervention were compared to generate an incremental cost-effectiveness ratio (ICER). Costs of recruitment by CHW include workers recruitment, training supplies, certi cation, identi cation badges, vouchers, transportation, meals, accommodation, incentives, per diem, and miscellaneous materials. CIC costs include radio broadcasting, banners, and yers. Both groups include nancial aid for women's transportation to the screening center according to hospital accessibility from each health area. To highlight the actual eld situation and its margin of error, we decided to compare the real-life cost-effectiveness (actual expenses, including incorrect patient transport nancial aid), and the theoretical cost-effectiveness (expected expenses) generated by the CHW intervention to the cost-effectiveness of the CIC intervention. Costs are expressed in USD according to the exchange rate on March 1st, 2020 and, in international dollars to consider purchasing power parity.
Statistical analysis -Quantitative data were stored and analyzed using Stata Statistical Software Release 16 (StataCorp LP, College Station, TX, USA). A descriptive analysis was conducted; categorical variables were summarized with frequencies and percentages, and continuous variables were summarized with means and standard deviations (SD). P-values were estimated using Pearson's chi-squared test, Student's ttest, and ANOVA test as appropriate. All analyses were 2-sided and p-values < 0.05 were considered statistically signi cant. Women's sociodemographic and medical data were collected, stored, and managed by the secuTrial® online database. The calculated incremental costeffectiveness ratio (ICER) is determined as the additional cost per screened woman by CHW, calculated as the difference between CHW costs and CIC costs divided by the difference of the number of screened women between CHWs and CIC.

Results
Population -A total of 1940 women were included during the study period, with an HPV positive rate of 18.6% (n = 361), and 39 CIN2+ (2.0%) lesions were diagnosed. In the CIC group, 1356 women (69.9%) were recruited and 28 CIN2+ (2.1%) lesions were detected. In the CHW 584 women (30.1%) were recruited and 11 CIN2+ (1.8%) lesions identi ed. Two hundred sixteen participants living outside the Dschang health district were recruited in the CIC group, and nineteen patients in the CHW group. Among the 68 CHW trained, eight did not recruit any participant. The recruitment progress is depicted in Fig. 1 showing reuptake of recruitment trend when introducing CHW and an annual closing of the Dschang Screening Unit for the winter holiday and equipment shortage in December. Figure 2A-B includes participants living in the health district. The CIC method recruited 87.89% women in zone 1 (n = 1002), 7.72% in zone 2 (n = 88), 2.81% in zone 3 (n = 32) and 1.58% in zone 4 (n = 18). The CHW method recruited 38.58% women in zone 1 (n = 218); 29.03% in zone 2 (n = 164); 13.81% in zone 3 (n = 78); 18.58% in zone 4 (n = 105).  Recruitment breakdown by zone -Socio-demographic differences between women recruited by CIC and CHW in the four zones are described in Table 2. Mean participants' age varied between urban and rural areas, with women in zone 1 tending to be younger than those in zone 4 (p = < 0.001). In zone 1, primary education only was attended by 17.4% of women in the CIC group contrasting with 39.5% of women recruited in CHW group. When comparing the two groups, secondary level and higher was reached by more participants, in CIC group than in CHW-led intervention except for zone 4, 38.9% in CIC and 49.5% in CHW group. Tertiary education was attended by 25.6% in zone 1 recruited by CIC compared to only 7.8% to zone 1 within CHW group. In the CIC-led intervention, women in zone 1 were more frequently employed (38.1%) and independent workers (33.1%), whereas in zone 2-4, women worked more as farmers (34.1%, 34.4% and 50% respectively). In the CHW-led intervention, most participants were independent workers in zone 1 (34.9%), and farmers in zones 2 (49.4%), 3 (92.3%) and 4 (76.2%). We also found that most unemployed women 0.7% lived in zone 1 and were recruited through CIC. Women coming from zone 1 and recruited through CIC had fewer children than in other zones. Indeed, 49.7% women in zone 1 had between 1-4 children and 45.51% had more than 4 children, while in other subgroups, between 62.5% and 80.95% of participants had more than 4 children. Within the CIC-recruited group, most women who used condoms were in zone 1 (15.2%,) and zone 2 (13.6%). Participants who smoked the most were recruited by CHW and live in zone 2 (7.9%) and in zone 3 (12.8%). Variance in previous CC screening was also shown between women living in urban zones compared to those in rural zones and depending on the recruitment method. Recruited through CIC, 25.45% of women living in zone 1 had a history of previous HPV screening, 15.9% in zone 2, 9.4% in zone 3 and 5.6% in zone 4 (p = 0.092). Rates of previous screening were generally lower in women recruited by CHW, where 7.8% of women in zone 1 had a previous CC screening, 1.2% in zone 2, 2.6% in zone 3 and 1.9% in zone 4 (p = 0.017).
Screening rate -Figs. 2C shows recruitment method predominance is shown. Health areas in dark blue show that most screened women were recruited by CHW and in orange represent health areas where recruitment was predominantly done through CIC. White color indicates that half of the patients were recruited by CIC and half by CHW. In grey, two health areas were excluded (Mekouale and Lepoh) as no CHW participated. We observe a predominance for CHW recruitment in areas distant from the center. Cost-effectiveness analysis of recruitment is presented in Table 3. Cost analysis -A detailed breakdown of CHWs training costs for each session is presented in the supplemental table. The June session costed a total cost of 694.98 USD (cost per trained CHW is 33.09 USD for 21 CHW). The October session total cost was 1962.88 USD (cost per trained CHW is 37.75 USD for 52CHW). CIC costs include 33.62 USD for four radio broadcasts, banners 184.92 USD for two street banners, 42.03 USD for a thousand yers. Based on the onsite account book, the patients' transport aid was 1411.30 USD without distinction between the two intervention groups. To compare the two groups, the theoretical patients' transport aid is presented on Table 3. This was calculated based on the prede ned amount allocated for each participant's according to hospital accessibility from each health area health area 1845.87 USD for CHW-led intervention and 1345.74 USD for CIC-led intervention. The amount paid to CHW was calculated to be around 1141.57 USD (571.67 USD + theoretically calculated for missing receipt). Theoretical CHW incentive $ based on the number of women recruited were 870.40 USD. The average cost per CIC-recruited woman is 1.18 USD compared to 9.20 USD per CHW-recruited woman. Based on theoretical costs, the ICER is 6.45 USD or 16.61 2021Int'l$ per screened woman recruited by CHW. The average cost per CIN2 + lesion diagnosed is 57.37 USD in the CIC group compared to 488.56 USD in the CHW group.

Discussion
The global WHO strategy for cervical cancer elimination recommends that each country should meet by 2030 the 90-70-90 targets. (6) Achieving and sustaining the second target (70% of participation rate with a high-performance test) will be one of the most challenging issue for many LMCs countries. For example, in Cameroon, participation is very low, it is estimated that cervical cancer screening participation rate in a woman's lifetime is less than 10%. (22) This condition is one of the main reasons for the high cervical cancer incidence and death among middle-aged women in the country. (8) Our aim was to explore the effectiveness and costs of two different recruitment strategies in encouraging women to have a screening test.
Media-based information for public education about health-related issue are frequently used in many national campaigns in Cameroon. (23)(24)(25) However, according to the 2018 Demographic and Health Survey in Cameroon, within West Region, 38.1% of women were not exposed to any television, radio, or newspapers, 56.5% of women watch television and 22.4% listen to radio at least once a week. (22) This aspect is crucial for any decision making related to information spreading. Considering this data, radio broadcasting in our context is not the most e cient strategy compared to television-based intervention which also may be more expensive. Data is still limited about the impact of encouraging behavior changes in favor of effective health service and cost per person screened.
E ciency results for screening coverage must consider that CIC and oral communication within the community co-existed with CHW-led intervention during the second period under study and that several women recruited by CHW could have been screened without mentioning the CHW referral, which would lead to their misclassi cation. Community spread communication co-existed with CHW-led intervention and has probably also increased our recruitment in each group, thus CHW's impact could be greater than we assumed. At the screening center, warm welcome can lead to a positive experience and favor recruitment.
Involvement of CHW for health education and promotion around cervical cancer in the community constitute an important step to increase participation in program. CHW intervention contribute to optimize the participation as they use their cultural knowledge and ensure that message are delivered in a culturally appropriate fashion according to women's preferences and needs in rural areas who are rarely or never screened, which differ from those of women living closer to the city. (16, 26) As shown in Tables 1 and 2, women recruited by CHW tended to be less educated, have more children, use fewer condoms, and consume more tobacco. Participant knowledge about cervical cancer may not be the same as women living closer to the hospital. Studies have suggested that higher cervical cancer awareness is found among women within an urban environment due to internet and media access. (27) It has been established that a lack of information and awareness about screening centers' location, costs, available time, and geographical condition are the main barriers to CC screening. (28-31) In our study, CIC were used to convey an invitation to get screened. However, other studies have utilized media as an educational tool that appeared as effective as CHW intervention to recognize the importance of CC screening, although lay health workers were more effective to change screening behaviors through encouragement and logistical support. (32,33) CIC appear to be most suitable for women living close to the city center, while CHW improve recruitment coverage in rural areas. CHW not only enhanced recruitment outside urban areas, but they were also able to engage with and invite more women from a different sociodemographic population to be screened, including in zone 1. To avoid a Bottleneck effect due to limited capacities at the screening center, one strategy could be to start by using CIC, before gradually implementing CHW intervention.
A probable reason for a higher history of previous cervical cancer screening among participants from zone 1 in the CIC group is an increase of awareness and a built trust throughout a previous screening campaign in Dschang, in addition to the twenty years of collaboration of our research team in Cameroon. (11) Transportation and childcare were previously reported as screening barriers. (26) Our screening recruitment heavily depended on rain seasons as roads were impracticable. Moreover, nancial transport aid was an essential aspect of our strategy as women living in rural areas had to travel for many hours. CHW intervention helped to decrease these barriers as they recruited hard-to-reach women with multiple children and informed them about the nancial subsidies for transportation.
The cost per screened women and CIN2 + diagnosed was higher in the CHW group. However, the media campaign was most e cient in zone 1. The higher recruitment of women in rural areas by CHW highlights the importance of training, preparing, and deploying CHWs to screen hard-to-reach women, especially considering that almost 45% of the Cameroon population lives in a rural area. (34) Undetected cervical lesions potentially leading to cervical cancer also increase overall costs not only for the healthcare system but can cause direct and indirect costs for the woman and her family such as cancer management cost, or loss of income due to disease, disability or even death.
In Uganda, if the population screening coverage was increased, then a self-HPV community campaign was found more cost-effective than provider collection. (35) When possible, CHW selection should be based on abilities and long term motivation, and their work should be adequately compensated to avoid having inactive workers that need to be replaced by newly trained personnel, which increases the screening cost. (15,36) Training in October 2019 was more expensive in total than the rst session in June 2019; however, the investment is similar if we consider the expense per CHW trained. Improving CHW knowledge is a key factor to a successful recruitment intervention, (18) as was shown with the October session based on a multi-modal training, which was followed by an increase of screened women.
Strategies with multiple visits to get screened, treated, and follow-up can decrease screening effectiveness and can increase the overall cost of cancer prevention per woman due to loss to follow-up (14,37). In our setting, the 3T strategy led only to a 1.1% loss to follow-up and will probably increase program effectiveness as barriers for Cameroonian women include "low health literacy, poverty, lack of resources, and geographical conditions". (10) However, additional after-treatment visits may increase the need for CHW, as studies have shown that inperson follow-up could be a cost-effective approach to keep women in the screening process. (14) In this study, we only focused on the cost of screening recruitment; however, further studies will be needed to assess the full nancial and social burden and cost-bene t analysis of an HPV "screen and treat" program in Dschang. In Sub-Saharan Africa, most women dying from cervical cancer are around fty years old and DALYs caused by CC were estimated as 641 years per 100'000 women. (11,38) The large sample size and heterogeneity of the population regarding social and demographic characteristics are the major strengths of this study. Real-world conditions and thus the amount paid for equipment, supplies, and labor do not re ect theoretical costs. Health area attribution discordances and village overlap between two health areas/zones could have led to misclassi cation and inexact cost and recruitment rate estimates, in addition to some miscommunication that led to incorrect patient reimbursement cost. Moreover, measuring the success rate of CHW intervention could have allowed a more detailed analysis of the cost of CHW service. Indeed, the ratio of CHWapproached to screened women is currently unknown. Since recruitment strategies were not led simultaneously, CHW intervention might have enroll less participants as some women had already been informed through CIC. Another limitation is that some women recruited by CHW might have eventually attended screening without CHW intervention, at least we advanced their screening participation.

Conclusion
Combining both approaches appear as the most e cient strategy for improving recruitment among the target population according to regional context. CHW have a central role in building awareness and motivation for improving cervical cancer screening participation. Further studies are needed to explore innovative community-based intervention on effective way to improve recruitment of the target population.

Supplementary Files
This is a list of supplementary les associated with this preprint. Click to download. SupplementalTable.docx