Populations at higher risk for HIV infection are often the most difficult to reach and this is particularly true of men who have sex with men (MSM) in sub-Saharan Africa [1–3]. Research on MSM in Africa has been largely neglected because male-to-male sex is illegal in many countries, has been publicly denied by some heads of state and remains a matter of religious controversy . In addition, researchers have not formally assessed the role of anal intercourse in the epidemiology of AIDS in Africa [5,6]. As a consequence homosexual behaviour remains stigmatized, MSM fear legal authorities, and virtually no health services in Kenya are tailored towards diagnosis and treatment of sexually transmitted infections in MSM . HIV prevention counselling services targeted towards MSM do not exist in Coastal Kenya.
There has been little research on MSM in Kenya's coastal region, although the existence of men who sell sex has been documented . In 2002, formative research with 25 MSM who sell sex was conducted in Mombasa; they reported risky sexual behaviours, low condom use, and vulnerability to discrimination and violence . Since late 2005, MSM who sell sex have been recruited into an ongoing cohort study of persons at higher risk for HIV infection, in an urban area adjacent to Mombasa district. HIV prevalence at screening was 38% [23/60, 95% confidence interval (CI), 26–52%] and three sero-conversions were captured in 37 HIV-negative MSM (HIV incidence = 20.9 per 100 person years observation; 95% CI, 6.7–64.9) .
Preliminary study findings from the 2002 formative research and ongoing cohort study were communicated to district and provincial health authorities, and a study working group was formed to advise the Provincial Medical Office on the health needs of MSM who sell sex around Mombasa. This report presents the results of a collaborative effort to enumerate MSM who sell sex in and around Mombasa, to prepare for HIV prevention interventions.
Since July 2005, key populations at higher risk for HIV infections have been recruited at a research clinic for sexually transmitted diseases (STD) in an urban location north of Mombasa. This cohort includes mostly female sex workers (FSW), male sex workers (MSW) who have paid sex with women, and MSM, the majority of whom also engage in sex work . Ongoing recruitment of MSM (including those who do not sell sex) is facilitated by 10 trained MSM peer leaders who provide information about the cohort study, including the benefit of counselling and testing for HIV, and screening and treatment of STD. Prospective study volunteers are invited to the drop-in centre, located next to the STD clinic, to receive further information about research participation. The study was granted approval by the National Ethical Review Committee under Kenya Medical Research Institute (KEMRI).
Contact locations for men who have sex with men in and around Mombasa
In the formative stage of this study, the Population Council and the International Centre for Reproductive Health mapped over 50 key contact locations where MSM are known to search or wait for clients. During the enumeration training, additional sites were found, and a total of 77 locations were categorized geographically and assigned to 12 zones in and around Mombasa District. These locations included bars (23 locations), nightclubs/discos (eight locations), beach areas and beach bars (five locations), other private brothels, businesses, and estates (32 locations), and public streets and parks (nine locations; Table 1).
Training of enumerators
A total of seven training sessions were conducted, from 24 April to 26 May 2006. In the first two sessions 14 MSM peer leaders were trained and helped to design a recruitment leaflet. This group was gradually enriched with 23 enumerators identified by the peer leaders, many of whom had been recruited themselves in the ongoing cohort study.
Peak hours of contact were determined for each contact location and an enumeration scheme was established for each team, allowing for a defined observation period per location. It was agreed that Saturday afternoons and evenings would provide the largest probability to capture MSM who sell sex. To minimize security risks to the enumerators, most outdoor sites were only surveyed during daylight hours until about 1900 h and most enumerators were instructed to stop after midnight.
Enumerators were supported by three surveillance teams conducting periodic site checks to ensure that enumerators were present at the assigned times, and to answer questions and resolve issues (e.g. shortage of recruitment flyers). Each enumerator was given enough money to provide for a safe taxi ride to their homes at the end of the evening.
Identification of men who have sex with men who sell sex
Given that both prostitution and sex between men is illegal in Kenya, approaching and confirming contacts as MSM who sell sex presented a unique challenge to the enumerators. Participatory discussion and role-playing revealed, however, that MSM consider themselves to be very good at visually identifying other MSM by evaluating a man's appearance, body language, and/or clothing. Other ethnographic research on MSM in Senegal supports this . An enumerator would first visually identify, then approach and start casual conversation with the suspected MSM contact. Once the enumerator was confident that the contact's MSM status was confirmed, he would ask if the captured MSM was ‘seeking clients, or currently willing to sell sex in exchange for money and/or goods’, that is, if he was ‘on the market’. Spoken in Swahili, sokoni refers literally to a local market.
After it was established that an MSM was ‘on the market’, and therefore an MSM who sells sex, the enumerator would introduce himself as a peer educator with KEMRI, and offer an A5-size recruitment leaflet containing information in both Swahili and English about MSM, the risk of anal transmission of STD, including HIV, the benefits of regular HIV counselling and testing, and the location of the research clinic. Designed to be colourful and eye-catching, accepting the leaflet would effectively ‘tag’, or capture each contact. The enumerators were further instructed to show contacts their identity badge, and, if necessary, a signed letter from the Provincial Medical Officer providing explanation and justification of the research activity. MSM contacts who had previously received a leaflet elsewhere were asked if the leaflet was given by an official numerator (with badge) or by a peer contact. Data were recorded for each contact, using tick boxes and requiring minimal writing (Fig. 1).
Estimation of population of men who have sex with men who sell sex
To estimate the total population of MSM who sell sex, we applied a ‘capture–recapture’ formula described in detail elsewhere [12,13]:
In brief, c1 (capture 1) was the first sample of individuals captured from the population n of MSM who sell sex. One week later at the same places and times, the second sample c2 (capture 2) was captured. Some of c2 captured in the second count comprised recaptures, or matches m, (i.e. those who were also captured during the first count). The formula assumes that the proportion or second count matches (m) to second count captures (c2), equals the proportion of those captured in the first count (c1) to the total population (n). Therefore, n can be calculated as:
To estimate the 95% confidence interval for n, the following formula was used:
Capture 1 included 284 men (following the removal of 15 duplicates); 89 men refused to participate. Capture 2 included 484 men (following the removal of 35 duplicates); 75 men refused to participate. Of the 484 men in capture 2, 186 (recaptures) were also included in capture 1. These men were considered matches. Hence, the estimate of the population size is:
We used a two-sample capture–recapture calculation to estimate that 739 MSM sell sex in and around Mombasa. In total, 582 MSM who sell sex were contacted through trained peer enumerators and an information leaflet about reducing HIV and STD transmission extended. Of these, 484 were contacted in a single day, offering avenues for HIV prevention.
Despite high community stigma and legal concerns, trust was established with a core group of MSM sex workers, who currently benefit from regular HIV counselling and testing, STD screening, and provision of comprehensive care at a research STD-clinic . Self-selection of the majority of enumerators from this MSM cohort, participatory development of the recruitment leaflet, endorsement of the outreach activity by national health authorities, and formative research conducted by two collaborative groups , allowed us to draw two samples of MSM who were selling sex in and around Mombasa at 77 locations, on two consecutive Saturdays.
Four assumptions underlie the capture–recapture methodology [12,13]: the population must be closed, the capture history of each member accurate, capture sources independent, and the probability of being captured during both rounds equal. In the current study, the MSM population was not completely closed, but little change would have been expected over the period of 1 week; training and supervision of enumerators helped to ensure capture accuracy. High mobility of recaptures to new locations documented in the second count supports the case for independence of many of the capture sources, although, for organizational and safety reasons, enumerators visited the same locations on both days.
Due to familiarity with the enumerators and the project, some men counted in capture 1 may have been more likely to be included in capture 2. However, this effect on the capture–recapture estimate (i.e. an increase in the matches, and therefore a reduction of the estimate) may have been balanced by men included in capture 2 who refused a leaflet the previous week, thereby failing to be recorded as matches.
During the second round we almost doubled MSM contacts, with an almost equal number of new contacts, a large number of recaptures, and an overall decrease in the rate of refusals. Possible explanations for this include: the second count was done near the month-end, following a Friday when many Kenyans received their salaries – hence an increase of MSM who sell sex in the study area looking for clients; the sites documenting most recaptures were a popular public park area and adjacent nightclub where increased public traffic was observed during the second count; and, finally, enumerators reported an improvement in skills and confidence following the successful first count a week earlier. These factors may have affected the probability of capture in the second count.
Our estimate of 739 MSM who sell sex in and around Mombasa is likely to be conservative. Thirty-seven enumerators could not provide permanent coverage at 77 locations, some felt that the time limits were too restrictive, and MSM working in private brothels or homes were not contacted efficiently.
This study limited the enumeration to MSM who sell sex, because it was assumed that commercial MSM are more likely to congregate at key areas to seek clients. However, it seems likely that MSM who sell sex make up only a part of the larger population of MSM in this community, highlighting the potential importance of homosexual contact as a means of HIV transmission. Further investigation to collect information on the clients of MSM who sell sex as well as MSM who do not engage in commercial sex is clearly needed. A large study of behaviour characteristics of approximately 400 MSM who sell sex in and around Mombasa is currently ongoing.
Targeting MSM for HIV prevention and STD treatment challenges established AIDS control options in Kenya, as messages promoting male condoms do not generally address anal sex. If HIV prevalence, risk behaviour, and HIV incidence in the larger group is similar to the group recruited in the cohort , then the epidemiologic impact of MSM on HIV transmission in the Mombasa area may be substantial, particularly as the sexual networks of MSM in Kenya extend to women, and are not isolated from the general population . This concern and the results of this study have been presented to the Coast Provincial Medical Officer and the National AIDS Control Council of Kenya, with the view towards implementing ‘positive prevention’ . Reaching out and contacting MSM who sell sex with a view to reducing HIV transmission is recommended as an HIV public health intervention but would not necessarily require capture–recapture methodology.
In summary, we documented a group of MSM selling sex in and around Mombasa, at both public and private locations. Targeting HIV prevention strategies towards MSM is urgently needed.
We wish to commend the commitment and effort of 37 MSM enumerators. We thank Dr A. Kahindi, Provincial Medical Officer, Coast Province, for his administrative support and advice. Dr Ronald Geskus, Municipal Health Service, Amsterdam; Dr Pat Fast, International AIDS Vaccine Initiative, New York, and Chris Castle, UNESCO, Paris, for useful comments on the manuscript. We also acknowledge Agnes Rinyiru of ICRH, and Theresia Mumbia of KEMRI for their contributions in the field. Eka Esu-Williams, Leila Wangari and Waimar Tun of the Population Council and W. Onyango-Ouma of the Institute of African Studies at the University of Nairobi for technical assistance. This paper was published with permission of Dr Davy Koech, Director of KEMRI.
Sponsorship: Financial support for this study was provided by the International AIDS Vaccine Initiative (IAVI), New York, US, and the President's Emergency Plan for AIDS Relief through the Office of HIV/AIDS, Bureau of Global Health, US Agency for International Development (USAID), through the Population Council's Horizons Program cooperative agreement of Award No. HRN-A-00-97-00012-00. The opinions expressed herein are those of the authors and do not necessarily reflect the views of USAID.
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