In Cameroon, female sex workers (FSW) are a key population for HIV prevention and control; they experience a high burden of HIV augmented by structural barriers to HIV prevention, testing, and care services.1,2 A review of data from 1991 to 2009 estimated that HIV prevalence among FSW in Cameroon is 23.6%.3 One included study from 2009—the most recent primary data to date—reported national HIV prevalence of 37% among FSW, with pronounced regional variation.4 In comparison, HIV prevalence was 4.3% among all adults in Cameroon in 2011,5 and updated to 3.7% in 2018.6 Sub-Saharan Africa (SSA) is typically known for having a generalized HIV epidemic; yet, this classification masks the diversity of HIV epidemics seen in subregions of SSA, as well as within countries and populations. West and Central Africa (WCA) generally has lower HIV prevalence (range 0.5%–4.5%) among reproductive-aged adults compared with Southern and East Africa3; yet, the stark disproportionate burden of HIV among FSW observed in Cameroon is also reflected more broadly in WCA3 and SSA, wherein the pooled HIV prevalence is 36.9% among FSW in SSA compared with background prevalence of 7.4%.7 Evidentially, prevention and treatment programs that appropriately target and reach FSW are fundamental to HIV control in the region.
Identification of appropriate indicators to both target and gauge the success of FSW prevention, care, and treatment interventions can be challenging. Cross-sectional data are most readily available but are limited to assessing HIV prevalence, which is a lagging indicator of epidemic progress. HIV incidence is more responsive to changes in transmission and thus ideal for monitoring local HIV epidemics, evaluating the effectiveness of interventions and understanding the drivers of disease,8–10 but it is difficult to measure.11 Although multiple studies have estimated HIV prevalence among FSW in Cameroon, to date, there have been no studies that have allowed for estimation of HIV incidence. An understanding of incidence and risks of new infections is particularly important to inform new interventions such as pre-exposure prophylaxis (PrEP), which is prioritized for population groups and individuals with substantial risk of HIV.12
Characterizing the behavioral, health, structural, and social factors linked to HIV acquisition and transmission has been shown to be relevant when considering the implementation of HIV prevention and treatment programs intended to specifically address those needs.13 The contribution of structural factors, including legal barriers, stigma, discrimination, and violence, to the burden of HIV among FSW internationally has been well documented.7 In Cameroon, sex work remains criminalized and the prevalence of physical and sexual violence experienced among FSW is high1; previous work has demonstrated associations between experience of violence with reduced ability to negotiate condom use, inconsistent condom use, fear of health services, and lack of law enforcement protection.1,14 It is thus conceivable that these factors will also be related to HIV acquisition. However, no previous work has examined the risks and contextual factors associated with newly acquired HIV. Assessing associations with HIV infection based on prevalence data can result in reverse causality, whereby correlates such as income, condom use, service access, or experience of stigma and violence may be affected by awareness of HIV-positive status rather than a determinant of infection.15,16 Analyses that exclude known prevalent infections can limit these biases. Furthermore, previous work has demonstrated the importance of undiagnosed infection to the onward transmission of HIV.17–19 An understanding of characteristics associated with undiagnosed HIV may help target testing strategies to reduce undiagnosed infection and prevent new HIV infections.
Subsequently, a measure of new HIV diagnoses was devised to assess the prevalence and determinants of new HIV diagnoses among FSW, recruited through an integrated biobehavioural survey (IBBS) conducted in 2016. These findings will help improve targeting of interventions to reduce HIV transmission, prevent HIV, and reduce undiagnosed infection among FSW in Cameroon.
Study Design and Setting
A cross-sectional study was conducted among FSW recruited for the 2016 IBBS as part of the Continuum of Prevention, Care and Treatment (CoPCT) of HIV/AIDS with Most-at-risk Populations (CHAMP) project in Cameroon, implemented by CARE. Recruitment was conducted in 5 cities across Cameroon from December 2015–October 2016: Bamenda, Bertoua, Douala, Kribi, and Yaounde.
FSW were defined as women who reported sex work as their principal source of income in the past year. Other inclusion criteria were the following: born female, aged 18 years or older, speaks and understands French or English, and resided in the city of recruitment for at least 3 months before recruitment.
FSW were recruited through respondent-driven sampling (RDS). Six initial recruits, known as seeds, were purposively selected through formative research and mapping with consideration of their understanding of the recruitment process, ability to recruit peers, knowing many other peers, and interest in being recruited. Seeds and subsequent FSW recruited in the study (nodes) were provided with 3 referral coupons and asked to recruit up to 3 members of their social network who met the study's eligibility criteria. Sampling continued in waves until the desired sample size (n = 2250) was met.20
Study staff explained the study to potential participants, screened them for eligibility, and obtained informed consent. Willing participants completed an interviewer-assisted behavioral questionnaire and underwent serological testing for HIV and syphilis. Questionnaires took 45–60 minutes to complete and covered multiple domains, including sexual behavior, stigma and discrimination, health care access, and history and knowledge of HIV and syphilis. Then, serological testing was completed based on a venous blood draw and following national testing protocol, included pre- and post-test counseling. HIV testing used dual rapid testing through first-line testing with Alere Determine TM HIV-1/2 antigen/antibody combo test and where first result was positive or indeterminate, second-line testing with OraQuick ADVANCE Rapid HIV-1/2 antibody test. Results were available 20–40 minutes after testing. Syphilis infection was detected using a rapid non-treponemal Venereal Disease Reference Laboratory (VDRL) test and Treponema pallidum hemagglutination assay (TPHA) except at one site (n = 574) where only TPHA testing was completed due to unavailability of VDRL testing facilities. Past or current syphilis infection was defined as TPHA-positive or VDRL-positive. Individuals with a VDRL-positive test were considered to have active syphilis and were treated; where VDRL results were not available, all individuals who were TPHA-positive were treated. Participants who tested positive for HIV and/or syphilis were referred to health facilities for care and treatment; other participants were referred to a community-based center, supported by the CHAMP program, for prevention services and routine HIV and sexually transmitted infection (STI) testing. All participants were reimbursed 2000 FCFA (∼4 USD) for their time and transportation and received an additional 1000 FCFA (∼2 USD) for each person they referred who was successfully recruited into the study.
Self-reported HIV status was derived from HIV testing history (“Have you ever been tested for HIV infection?”), receipt of results (“Did you receive your last HIV test?”), and result of the last HIV test (positive, negative, unknown). We defined new HIV diagnosis as self-reporting HIV-negative or status unknown with a serological HIV-positive result.
Covariates of Interest
Key covariates were selected to include individual measures widely shown to be associated with HIV infection in existing literature (such as age, unprotected sex, HIV knowledge, and STI infection) as well as broader measures of sex work, health, service engagement, and structural and social measures that are implicated in a socioecological model of HIV infection.21 An overview of measures considered for inclusion in the model is presented in Supplemental Digital Content 1, https://links.lww.com/QAI/B252.
Monthly income from formal and informal work, assessed in 50,000 FCFA brackets, was reclassified based on minimum wage in Cameroon (36,270 FCFA/mo)22 and in 100,000 FCFA brackets.
Sex work was defined as sex in exchange for money or other goods. Frequency of condom use was assessed for individual partner types and, in analysis, was dichotomized as always and less than always. Consistent condom use (CCU) was defined as always using a condom with the indicated partner type. In addition to standard behavioral risk variables, we defined protected sex with regular nonpaying partners as meeting one of the following criteria based on past 12 months: CCU with all regular nonpaying partners; only one regular partner in the past year who is known HIV-negative; only one regular partner in the past year who is known HIV-positive and on ART; and no vaginal or anal sex with a regular partner.
Experience of STI symptoms was dichotomized based on self-reported presence of any of the following STI symptoms in the previous 12 months: genital/anal blisters or sores; pain or burning with urination; vaginal discharge; irregular vaginal bleeding; genital/anal warts; or abnormal mass or swelling around the genital organs.
Mental health was assessed using the Patient Health Questionnaire (PHQ9) scale,23,24 which generates a score from 0 to 27 based on frequency of depressive symptoms in the previous 2 weeks. Individuals with more than one item missing were excluded from the scale. Depressive symptoms were categorized as none (<5), mild (≥5 & <10), and moderate or severe (≥10). This was then dichotomized for analysis.
Social capital was assessed using a modified scale developed in Brazil for measuring social cohesion among FSW25 and validated in Swaziland.26 Nine items were used to assess agreement to statements about the ability to count on other FSW for particular needs (eg, to help you deal with a difficult client), trust, and friendship, with a 5-point scale of agreement. Each item was scored from 0 (strongly disagree) to 4 (strongly agree). The 9 items were summed to create a continuous score from 0 to 36. Overall, 118/2255 FSW had a least one item missing. Individuals with less than 4 missing items were included in the scale, with missing data treated as zero. Those with 4 or more missing items were excluded from the scale. The overall score was categorized based on the 25th percentile (16) and 75th percentile (27), with 3 ordinal categories for low (0–16), medium (17–26), and high (27–36) social cohesion; these were dichotomized for inclusion in the model. These methods were adapted from previous work examining the associations between social capital and HIV.26,27
First, we assessed self-reported HIV status in relation to actual HIV status and determined the prevalence of newly diagnosed HIV infection. Participants self-reporting a previous positive HIV test (ie, previously diagnosed) or an indeterminate HIV result at the time of testing were excluded from the subsequent analyses to limit biases associated with a prior HIV diagnosis.
Second, associations between key covariates and a new HIV diagnosis, versus HIV-negative status, were assessed using Poisson regression with robust variance.28,29 Prevalence ratios and adjusted prevalence ratios were assessed to 0.05 significance. This method was chosen given that prevalence of the outcome was over 10%. A full multivariable Poisson regression model was developed using all key covariates. Covariates were manually dropped from the model based on a combination of conceptual framework and high nonsignificant P-value (>0.1); variables included a priori according to conceptual framework are indicated in Supplemental Digital Content 1, https://links.lww.com/QAI/B252.
To control for RDS, sampling weights were computed using RDS Analyst based on the whole study sample.30 RDS-adjusted HIV prevalence of the entire sample was assessed by calculating the average point estimate and upper and lower confidence limits from individual sites. Poisson regression models were corrected for sampling weights and clustering by seed. Seed participants (n = 6) were included in statistical models.
All analyses on the subsample were conducted using Stata version 14.31
Ethical approval was obtained from the National Research Ethics Committee in Cameroon alongside administrative clearance from the Ministry of Public Health. All data collected were nonidentifiable.
Overall, 2255 FSW were recruited. The median age was 28 years and ranged from 18 to 70 years. The crude HIV prevalence was 24.5% (550/2248) and ranged from 15.1% to 33.8% by site (Table 1). RDS-adjusted HIV prevalence was 25.8% (95% confidence interval: 21.7% to 30.4%) overall. HIV serostatus in relation to self-reported HIV status is reported in Table 2. Among participants testing HIV-positive, 53% (290/550) self-reported living with HIV and 47% (260/550) were newly diagnosed with HIV based on self-reported status. An additional 7 participants self-reported to be living with HIV but tested HIV-negative, of whom 2 (29%) reported being on ART. The final sample excluded participants who self-reported HIV-positive status (n = 297) and those with indeterminate test results (n = 7); of the remaining participants, 13.3% (260/1951) of women were newly diagnosed with HIV.
Characteristics and Experiences of FSW Self-Reporting HIV-Negative or Unknown HIV Status
Additional characteristics of the 1951 FSW included in the analysis are described in Table 3.
The median age was 27 years [interquartile range (IQR): 23–34]. Most women (78.1%; n = 1524) reported being single and never married and 1632 (83.7) participants reported any biological children. The proportion of FSW newly diagnosed with HIV was similar between cities.
The median age of first selling sex in exchange for goods, money, or favors was 22 years (IQR: 19–27). Participants reported having sex in exchange for money or goods for a median of 3 years (IQR: 2–5). Half (49%) of the participants reported at least 5 clients on a normal day, and the median number of clients per month was 72 (IQR: 36–125). The majority of women (71.2%) earned at least 50,000 FCFA (∼USD 90) per month. The most common settings reported for meeting clients were: the street (64.5%); bar/club (61.1%); hotel/guest house (26.2%); and brothels (22.3%). The most common settings reported for having sex with clients were: hotel/guest house (84.6%); brothel (37.7%); and a private residence (50.0%).
Where participants reported vaginal and/or anal sex with the relevant partner type, the proportion reporting CCU was 75% (1499/1935) with clients, 52% (18/351) with casual nonpaying partners, and 17% (236/1371) with regular nonpaying partners. Considering other risk-reduction strategies (CCU with all regular nonpaying partners; only one regular partner in the past year who is known HIV-negative; only one regular partner in the past year who is known HIV-positive and on ART; and no vaginal or anal sex with a regular partner), the proportion reporting protected sex with regular nonpaying partners increased to 65% (930/1434), where relevant.
Overall, 1725 (88.6%) participants reported ever testing for HIV, and 1056 (54.2%) participants reported having completed an HIV test in the past year. Of women tested in the past year, the median time since last test was 110 days (IQR: 64–186.5). Among women newly diagnosed with HIV, 40% (103/260) reported an HIV test in the past year (median 112 days, IQR: 51–203), 42% (110/260) reported an HIV test more than 1 year before, and 18% (47/260) reported never previously testing for HIV.
In the previous 6 months, 1256 (63.9%) participants reported receiving any information on HIV; only 100 (5.1%) women reported knowing that anal sex posed the highest sexual risk, and 682 (35.0%) women knew that the safest lubricant is water based. Overall, 847 (43.1%) participants reported experiencing any STI symptoms in the previous 12 months. Based on serological testing, 227 (11.7%) participants had past or current syphilis infection. A total of 34 (1.7%) women reported ever taking antiretrovirals (ARVs, off-label) to prevent HIV.
Experience of stigmatization was high: 1403 (71.9%) participants reported any stigma; an additional 469 (24.1%) women reported ever being physically harassed or hurt due to sex work, including 232 (11.9%) who reported recent violence; and 612 (31.4%) had ever been forced to have sex against their will, including 202 (10.4%) who reported this recently within the past 6 months. In addition, 783 (40.1%) participants had ever been arrested and 45 (2.3%) participants had ever been arrested and incarcerated. Most (79.8%) participants demonstrated self-stigmatization due to sex work. Based on the PHQ9, 614 (31.6%) women reported mild and 317 (16.3%) women reported moderate to severe depressive symptoms. A total of 346 (17.8%) FSW reported suicidal ideation in the previous 2 weeks. The majority of participants reported medium to high social capital (75.2%).
Associations With Newly Diagnosed HIV
Table 3 presents results from Poisson regression with robust variance estimation. In multivariable analysis, the following variables were significantly associated with new HIV diagnosis when adjusting for other variables: primary school education or less compared with any secondary or higher education, 5 or more dependents compared with none, 5 or more years involved in sex work compared with <1 year, history of incarceration, and low social capital. Higher income (>250,000 CFA compared to <50,000 CFA per month) was associated with lower prevalence of new HIV diagnosis.
HIV remains highly prevalent among FSW in Cameroon, with 1 in 4 FSW estimated to be living with HIV. Although stark declines in HIV prevalence and new infections among FSW have been observed in other parts of WCA,3,32–34 the same declines have not been observed in Cameroon when accounting for differences in sampling frame and recruitment.3,4 Results from this study demonstrate that HIV is frequently undiagnosed and may include both delayed diagnoses and new infections. There is evidential need to expand prevention tools and service delivery for women at high risk of acquiring HIV. Moreover, these data suggest the importance of interventions that address social and structural risks for HIV and for engagement in health care services among FSW. Supporting frequent HIV testing among key populations remains essential to ensure prompt diagnosis and linkage to treatment.
Beyond individual-level behavioral factors, findings from this study reiterate the importance and role of economic factors, policing and incarceration,1,35–37 and social capital25,26 on HIV risk and delayed diagnosis among FSW. Tools that effectively address these risks are integral to reducing HIV incidence among FSW in Cameroon.13 Although the majority of FSW earned above the national minimum monthly wage,22 we still detected a protective relationship between income and education attainment with new HIV diagnosis, which is consistent with observations among FSW from other settings.38–41 Elsewhere, this has been attributed to degree of economic dependence on sex work, negotiating power and threat of violence, self-efficacy, affordability of condoms, and work environment.38–41 Even where HIV testing is free, auxiliary and indirect costs may be a barrier to testing42 and thus delay diagnosis. Strategies to reduce economic power imbalances and the threat of violence, promote skills in handling difficult clients and negotiating condom use, and strengthen police and legal protection of FSW will support HIV prevention and testing among FSW, particularly those with low income and low level of education. Although there is inadequate evidence for income-generation and microfinance schemes for HIV prevention,43,44 where there is suitable demand and buy-in from FSW, these may help to reduce economic pressure and empower FSW. Community-based HIV testing remains important to reduce costs and times associated with HIV testing.45 Interventions focused on increasing awareness among uniformed officers on the needs and specific vulnerabilities among FSW, including physical and sexual violence, may further promote a supportive environment for more effective HIV prevention services in Cameroon.38 Community empowerment initiatives for FSW, which promote ownership of programs, foster social capital, and support HIV prevention, are highly regarded, although there are recognized challenges to implementing them.46 Further work is needed to understand how best to strengthen social capital among FSW in Cameroon.
National guidelines in Cameroon advise at least annual testing for FSW,47 and more frequent testing where indicated by risk or HIV exposure. Gaps in recent testing resulting in undiagnosed infections were highly evident among FSW and may impede progress in achieving 90-90-90 goals for knowledge of status, access to ART, and viral suppression.48 Regular HIV testing may be supported through the continued availability of community and outreach testing, as well as new strategies such as HIV self-testing.45 HIV self-testing is demonstrated to increase recent testing,49 but not necessarily correct knowledge of HIV status,50 and further work is needed to ascertain how to optimize the distribution and utilization of HIV self-tests in the local context.
Based on self-reported HIV testing history, approximately 2 in 5 study participants newly diagnosed with HIV may have acquired HIV in the past year. Current HIV prevention interventions for FSW in Cameroon are focused on education, condom promotion and distribution, and HIV testing.47,51 The possible contribution of newly acquired infections to a portion of new HIV diagnoses confirms that PrEP may be a valuable prevention commodity in this setting to complement existing services. Although structural issues delaying diagnosis may similarly affect PrEP uptake and need to be addressed,52–55 PrEP provides a means for individual-controlled prevention to circumvent some social and structurally driven HIV acquisition risks. Of note, although PrEP is not currently available in Cameroon, there was a small minority of FSW who reported using ARV for prevention, which may indicate acceptability and demand of this form of biomedical prevention. However, the nature and consequences of nonsupervised use of ARVs in Cameroon, and how this may affect PrEP programming, are not yet known. Further research is needed to assess the acceptability and feasibility of rolling out PrEP to key populations in Cameroon.
Targeting interventions toward a subpopulation considered most at risk is a common means for promoting efficient resource allocation and ensuring referral to appropriate services based on individual needs, including for identifying PrEP candidates.56 The present findings indicate that common indicators for risk assessment, such as condom use, are insufficient for predicting undiagnosed HIV infection. Based on findings reported in relation to key populations in other settings,57 individual behavior factors are also unlikely to be sufficient for predicting risk of new HIV infection in this population. Screening tools that consider the social, demographic, and structural determinants of newly diagnosed HIV, as well as network-level factors,57 may support targeting HIV interventions among FSW locally.
A number of limitations for these results should be considered. All indicators are based on self-reported interview data and may be subject to reporting bias. The derivation of the analysis sample was dependent on self-reported HIV status. Individuals may have underreported being HIV-positive due to stigma, social desirability bias, or poor comprehension of diagnosis,58,59 and thus may have been incorrectly classified as newly diagnosed. In addition, individuals on ART may have received a false-negative test result; thus, all participants who self-reported living with HIV were excluded from analysis, regardless of test result. Furthermore, our designation of newly diagnosed HIV is not synonymous with newly infected. Ongoing research is needed to assess HIV incidence and determinants among FSW based on serological measures. Recent primary syphilis may have been misclassified as never infected at one site due to unavailability of VDRL testing. FSW were recruited from 5 urban localities in Cameroon, and results cannot be generalized to all FSW nationally. However, the use of RDS is considered a best practice for surveying hard-to-reach populations,60,61 and within the cities sampled, it is likely to have recruited a more representative sample than previous surveys in Cameroon that used venue-based sampling.1,4,62 Finally, typical of cross-sectional studies, causality cannot be determined. In a population where half of the women living with HIV had been previously diagnosed, there is high potential for known status to influence behavior and bias associations. However, in this analysis, we enhanced the cross-sectional design through exclusion of previously diagnosed cases, thus minimizing the impact of behavior change, service access, or experiences related to known status. In the absence of HIV incidence data, these results provide insights into ongoing HIV acquisition risks among FSW across Cameroon.
Taken together, these data reinforce the importance of social and structural factors in sustained HIV acquisition and delayed diagnosis among FSW in Cameroon. Although there is increasing evidence supporting the efficacy of HIV prevention and treatment interventions, the impact of criminalization, law enforcement, financial resources, stigma, and social capital on the rollout of these interventions needs to be closely considered to avoid widening the gap in service access. Ultimately, moving forward necessitates concerted and collaborative approaches to leverage all evidence available to implement evidence-based and human rights–affirming interventions.
The authors thank all study team members, advisors, and study participants for their time and contributions to the study. This study was implemented through the CHAMP project, which was funded by the U.S. President's Emergency Plan for AIDS Relief (PEPFAR) through the U.S. Agency for International Development (USAID) from 2014 to 2019. Partners in CHAMP and involved in the implementation of this study included CARE Cameroon, CARE USA, Johns Hopkins School of Public Health, Metabiota, Moto Action, the National AIDS Control Committee (NACC), National Institute of Statistics, Horizons Femmes, Humanity First Cameroon, Alternatives Cameroon, Alcondoms, Cameroon Medical Women's Association (CMWA), CAMNAFAW, La Direction de la Recherche Operationnelle en Santé (DROS), L'institut Nationale de Statistique (INS) and L'Observatoire National de la Santé Publique du Cameroun (ONSP). The authors also appreciate the collaborating health facilities: Yaounde Military Hospital; Biyem-Assi District Hospital; Laquintinie Hospital; Douala Military Hospital; Nylon District Hospital; CMA Soboum; Bertoua Regional Hospital; Bamenda Regional Hospital; and Kribi District Hospital. The authors extend their gratitude to the Cameroon Government and, in particular, the Minister of Public Health, the Permanent Secretary of NACC, and their collaborators.
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