Konate, Issouf MD*; Traore, lsidore MD*; Ouedraogo, Abdoulaye MD*; Sanon, Anselme MSc*; Diallo, Ramata MSc*; Ouedraogo, Jean-Louis MD*; Huet, Charlotte MD, PhD*; Millogo, Ines MSc*; Andonaba, Jean-Baptiste MD*; Mayaud, Philippe MD, PhD†; Van de Perre, Philippe MD, PhD‡§∥; NAGOT, Nicolas MD, PhD‡§∥
HIV transmission dynamics have been driven mainly by transactional sex in West Africa. HIV prevalence is more than 10 times higher in female sex workers (FSWs)1-5 than in the general adult population, which ranges from 1% to 3% in sentinel surveillance surveys.6 The estimated population attributable fraction for prevalent HIV infection related to sexual contact with FSWs was estimated at 84% and 76% in the male adult populations of Accra (Ghana) and Cotonou (Benin).1,7 During the 1990s, this situation has led to the development of specific programs targeting FSWs in West Africa, with an emphasis on sexually transmitted infections (STIs) control, information, education, and communication (IEC) activities.1,8,9
One decade later, the epidemiological and socioeconomic context of sex work has dramatically changed in the region in at least 3 following ways: (1) The prostitution scene was made almost exclusively of foreign professional sex workers in the past; nowadays young nonprofessional or part-time FSWs are predominant in the commercial sex milieu. These women comprise bar workers, mobile fruit sellers, or women working in the informal sector who have no alternative but to accept client solicitations for transactional sex to meet the basic life needs. They have little knowledge of their risk-taking, which result in high HIV prevalence5,10; (2) bacterial STIs have markedly decreased in the general population11 and among high-risk groups over the last 2 decades, thanks to the wide implementation of STI control based on the syndromic management approach; (3) Although antiretroviral therapy (ART) have been scaled up over the last decade in Africa, sex workers have not been targeted by the national programs, mainly because this marginalized population was deemed unable to achieve and maintain a minimum adherence to long-term therapy. More recently, the debate over the “Test and Treat” strategy toward the elimination of HIV transmission12 has the merit to focus attention to the potential role of secondary prevention targeted at persons most at risk of HIV transmission.
In light of these remarkable changes, the interventions targeting this core group of transmission had to be revisited, with 2 main objectives to reduce risk, mainly by sexual behavior changes (primary prevention), and to reduce infectiousness through access to HIV therapy (secondary prevention for HIV-infected women).
In this article, we describe an intervention package combining HIV prevention and care among high-risk women in Burkina Faso and assess its impact on HIV incidence and HIV treatment outcomes.
Study Settings and Population
The ANRS 1222 “Yerelon” (meaning “Know yourself” in vernacular Dioula language) research programme was initiated in 1998 in Bobo-Dioulasso, the second largest city of Burkina Faso. A 2-year phase of formative research consisted in an initial socioanthropological survey, which identified the most-at-risk women and proposed a peer-based strategy to reach these women.5 This phase also allowed to identify and train peer leaders and to develop the basic health care package that would be useful and acceptable to the study population.
The “Yerelon clinic” was set up within a public health centre, the “Service d'Hygiene”, which offers vaccinations and routine medical check-ups for the population of food handlers.
An open-cohort study of high-risk women aged 18 years and above was set up from 2000. In addition to professional sex workers, nonprofessional sex workers including bar waitresses, mobile fruit sellers, traditional beer sellers, and other women occasionally selling sex, as identified in our anthropological survey,5 were recruited by the peer network. All participants reported exchanging money, gifts, or other benefits for sex.
After an information session, eligible and consenting women answered a standardized questionnaire to collect sociodemographic and sexual behavior data, followed by a pretest HIV counselling with a clinical psychologist. Then, a physician examined the participants and collected genital and blood samples. Follow-up visits were planned every 4 months with the same procedures. Patients who missed follow-up visits were recalled by telephone and home visits were made by peer-educators and social workers.
We report here data collected when the cohort was fully operational in terms of both HIV prevention and HIV care, that is, between December 2003 and January 2005.
Study Intervention Package
Six “peer leaders”, supervised by a coordinator, were trained to lead group education sessions, which covered a wide range of topics including HIV and STI basic education, condom negotiation skills, and adherence to long-term therapy.
In addition, each “peer leader” supervised 5 “fieldworkers” peers (ie, 30 in total) who carried out more individually tailored IEC sessions at working sites day and night, identified potential participants, and maintained adherence to follow-up visits (through recall and home visits). Free condoms were distributed at each visit.
Medical Care and HIV Therapy
Provision of ART therapy started in August 2004 in our cohort, according to the WHO guidelines, that is, when CD4 count was below 200 cells per microliter or at WHO clinical stage 3 or worse.
Women who started ART were followed more closely with weekly visits during the first 2 weeks, and monthly visits thereafter. CD4+ cell count and HIV-1 plasma viral load (PVL) were measured every 6 months.
Before and after ART initiation, participants were interviewed by a clinical psychologist to evaluate, anticipate, or address any issue of drug adherence. Group education sessions on ART (including adherence issues, and how to handle long-term therapy) were organized regularly by peer-educators at the Yerelon clinic.
Evaluation of the Impact of the Intervention Package
As a control group would have been ethically unacceptable, we assessed our intervention on the evolution of HIV incidence over time, assuming that our HIV prevention package would take some time to be assimilated by the participants as reported earlier.13 We also analyzed behavioral changes over time, considering both clients and regular partners with whom condom use is generally very low. Finally, the efficacy of HIV therapy was based on undetectability of PVL, T-CD4 lymphocyte gain, and drug adherence measured by pill count.
Every 4 months, HIV14 and genital infections were diagnosed using classical methods.15 Every 6 months, CD4+ T-lymphocytes count was measured using FACScan (Becton Dickinson, Flatlands, NJ) and plasma HIV-1 RNA was quantified using a real-time polymerase chain reaction assay (Generic HIV Viral Load, Biocentric, France), with a lower limit of detection of 300 copies per millilitre.16
Follow-up of HIV-negative women was censored at the time of HIV seroconversion for the calculation of incidence and sexual behaviors among HIV-negative women.
Primary Prevention Outcomes
The crude HIV incidence was calculated by dividing the total number of seroconverters over the study period by the total number of person-years of follow-up.
Sexual Behavior Changes
Sexual behavior were compared between enrollment and subsequent follow-up visits. To assess any modification of sexual behaviors after the introduction of ART, we compared condom use at last sexual intercourse with different sexual partners, between the last visit before ART and the final follow-up visit for women who initiated ART during the study, using the McNemar χ2 test.
The proportion of women with undetectable HIV PVL and the CD4+ T-lymphocytes cell gain were assessed at 6, 18, and 36 months after initiation.
The data analysis was conducted using STATA v9 (Statacorp, College Station, TX).
This study was approved by the Ministry of Health of Burkina Faso and the national ethical committee for health research.
From December 2003, 658 high-risk women were enrolled. Their median age was 25 years [interquartile range (IQR): 21-32], and 169 (25.7%) were HIV-infected: 42 (35.9%) among professional sex workers and 127 (23.5%) among part- time sex workers. Nearly one-fifth of women were married or cohabiting. Sex work was the main source of income for 22.3% of the participants, and the median duration of transactional sex was 5 years (IQR: 2-9) (Table 1).
Overall, condom use at last sex with any partner was relatively high at the time of enrollment (Table 2), particularly among professional sex workers (89.7%) who had a median of 30 clients (IQR: 5-49) per week. Part-time sex workers had only 1 client per week on average, with 80.0% condom use at last sex with new clients.
The median follow-up time was 20.8 months (IQR: 19.7-23.5), and 98 women were lost to follow-up, mainly professional sex workers (25 of 117). The main reason of loss to follow-up was the moving out of the city.
Beside HIV counselling every 4 months, 856 education sessions (6 attendees on average) were carried out on working sites by field-peer educators, in addition to the 850 sessions organized at the study clinics during follow-up visits.
Among the 489 HIV-uninfected women at enrollment, 7 participants seroconverted yielding an HIV incidence of 0.9 per 100 person-years [95% confidence interval (CI): 0.24 to 1.58]. The HIV incidence was 2-fold higher during the first 8 months as opposed to later (1.43 vs. 0.39 per 100 person-years). The HIV incidence tended to be higher among professional than among part-time sex workers (2.05 vs 0.74; P = 0.48).
Condom use at last sex with regular partners (boyfriends, “protectors” from the milieu, bar owners, etc.) improved from 14.8% at enrollment to 41.4% at the last visit (P < 0.001). Similarly, a significant increase in condom use at last sex was achieved with regular clients (from 62.7% to 83.9%, P < 0.001) and with new clients (81.7% to 98.6%, P < 0.001) (Fig. 1).
Among HIV-infected women, ART initiation did not lead to negative changes in sexual behavior, with any type of sexual partner (Table 3).
During the study period, 47 women initiated ART and were followed for a median of 32 months (IQR: 20-41). At ART initiation, the median CD4+ count was 147 cells per microliter (IQR: 79-183) and the mean PVL was 4.94 log10 copies per milliliter (95% CI: 4.70 to 5.18). 70% of women were at WHO clinical stages III or IV.
Virological and Immunological Efficacy
Six months after ART initiation, 79.4% of 34 women had an undetectable PVL. This rate was sustained at 18 months (80%, n = 30), and 36 months (81.8%, n = 22). Only 2 women had secondary virological failures, not linked to any ART interruption.
Correspondingly, the median values for CD4+ count reached 234 cells per microliter (IQR: 180-327) 6 months after ART initiation, 306 cells per microliter (IQR: 249-382) after 12 months, and 343 cells per microliter (IQR: 230-553) after 36 months. The median cumulative increases in the CD4+ count were 132 cells per microliter (IQR: 41-196), 177 cells per microliter (IQR: 105-255), and 230 cells per microliter (IQR: 90-400), at 6, 12, and 36 months, respectively.
Six months after ART initiation, 83.3% (95% CI: 67.2 to 93.6) of women achieved adherence levels of 95% or higher. This good initial adherence even increased over time to 92.1% (95% CI: 78.6 to 98.3) at 12 months.
Two women who started ART were lost during follow-up and 4 women died (mortality rate: 1.7 per 100 person-years). The cumulative probability of death after HAART initiation was 0.06 (95% CI: 0.02 to 0.18) at 12 months and 0.09 (95% CI: 0.03 to 0.22) at 36 months, respectively.
We designed an HIV intervention package targeting high-risk women, based on a prevention and care continuum. Beside obvious individual benefits, this intervention aims at reducing the role of high-risk women in the local HIV dynamics. Informed by an initial socioanthropological survey, this peer-based intervention achieved good results in terms of positive changes in sexual behavior, low HIV incidence, and good and sustained virological control among women taking ART. Although no control group could be used, the low and decreasing HIV incidence over time is a clear testimony of the effectiveness of the intervention package. Similarly, the virological efficacy of ART in this population at high-risk of poor adherence, due to their marginalization and lack of social and familial support, compared with reports from the general population in Africa.17-20
We are confident that the low HIV incidence observed in our study population is not simply due to the enrollment of a low-risk population. The HIV prevalence in this group, including among part-time sex workers, was about 10 times higher than in the general population of the same age,21 and their reported sexual behaviors are far more risky than those reported in the general population.21 In addition, as very few women refused to participate in the study and/or withdrew from the cohort, our participants are likely representative of the high-risk women living in Bobo-Dioulasso.
To our knowledge, no similar combined intervention has been reported and evaluated in West Africa. In a recent HIV prevention intervention in Benin as part of a microbicide trial, the HIV incidence among sex workers with about 20 clients per week was around 4 per 100 person-years, based on the data provided in the article.22 This incidence rate is much higher than the one we observed in our subgroup of professional sex workers, whereas these 2 neighbouring countries have very similar HIV prevalence rates in the female general population, 1.9% in Burkina21 and 1.5% in Benin.23
As we reported earlier,15 bacterial STI were very uncommon among these high-risk women. Although STI control is an important element of HIV prevention in many settings, the cofactor role of STIs may decline as interventions have been effectively deployed or according to the stage of the epidemic.24,25 Thus, alternative form of HIV control need to be added. The suggestion that ART could curve the HIV epidemics, especially when initiated on high-risk groups, is based on observational studies.26 Although mathematical models designed for general populations27,28 cannot accurately predict what might happen when targeting high-risk core groups, they suggest that raising the CD4+ count threshold for ART eligibility and achieving high coverage might reduce transmission considerably.29
The unprecedented epidemiological trend observed in the last decade in most of Western Africa, whereby HIV epidemics moved back progressively from generalized to concentrated feature, add yet another argument to specifically target high-risk women, who remain a major core group of transmission in this new context.
Our study participants achieved a good rate of ART virological and immunological success in the cohort, similar to the general population of HIV-infected individuals in West Africa,17-20 suggesting that our strategy to tailor adherence support by in-depth interviews with a psychologist were useful.
Importantly, ART initiation did not negatively influence sexual behavior in this population, which could counter-balance the beneficial effects of ART on HIV transmission.30 There was a risk that successful HIV treatment led to reduced condom use given that sex without condom is negotiated at a much higher price.
Our study has a number of limitations. Sexual behavior data is prone to under-reporting bias, which may increase overtime. The number of women initiating ART was small, which limits the statistical power on ART efficacy. Finally, the lower than expected observed HIV incidence in our cohort is mainly responsible our low statistical power to detect significant difference in HIV incidence over time.
From Implementation Research to Policy
Our operational research was designed to inform national policy regarding the provision of effective interventions for high-risk groups in Burkina Faso, which could also be relevant for West Africa more generally.
Our strategy, combining HIV/STI prevention and care in an adapted public clinic, is now being adopted by the Ministry of Health of Burkina Faso. The Yerelon study site has recently become a formal unit of the Bobo-Dioulasso University Teaching Hospital, directly linked to its Department of Infectious Diseases. A local NGO of high-risk women (the “Association Yerelon”), born from this initiative, has now be allocated a budget to coordinate the peer-educator network and finance their activities within the clinic.
In conclusion, the integration of care services, including a strong emphasis on treatment adherence, with a peer-led primary prevention package is pivotal to reduce HIV incidence among high-risk women in West Africa and is likely to impact markedly the local HIV dynamics.
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