The central role of clients of female sex workers in the dynamics of heterosexual HIV transmission in sub-Saharan Africa

Alary, Michela; Lowndes, Catherine Mb

Editorial Comment
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From the aPopulation Health Research Unit, Centre Hospital affiliated with the Universities of Québec and Laval, Québec, Canada and the bHealth Protection Agency, Communicable Disease Surveillance Centre, London, UK.

Correspondence to Dr M. Alary, Population Health Research Unit, Centre hospitalier affilié universitaire de Québec – Hôpital du Saint-Sacrement, 1050 Chemin Ste-Foy, Québec, Qc G1S 4L8, Canada.

Received: 4 December 2003; accepted: 23 December 2003.

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In this issue, Côté et al. present the results of a very interesting study on clients of female sex workers (FSW) in Accra, Ghana [1], which adds weight to the growing body of evidence demonstrating the importance of core and bridging groups in the HIV epidemic in sub-Saharan Africa. Quantitative analyses demonstrating the central role of clients of FSW as a bridging population in the transmission dynamics of HIV in a West African setting have been previously published [2]. Côté et al. have extended this work by estimating the population attributable fraction (PAF) of sexual contact with FSW in prevalent HIV infections among adult men. The results of this analysis confirm the central role of transactional sex in the HIV epidemic in Accra, with a best estimate of 84% for this PAF, and a range of 47 to 100% according to a sensitivity analysis where the level of uncertainty of the parameters used for the PAF estimation has been taken into account. Interestingly, in Cotonou (Benin), a setting where the differential in HIV prevalence between clients of FSW and the general population of men is higher than in Accra but where the estimated proportion of adult men having sex with FSW is lower, a recent estimation of the PAF for prevalent male HIV infections related to sexual exposure to FSW was 76% [3].

There are several limitations to the use of such an approach. First, there is potential misclassification of the exposure that is relevant to HIV acquisition among men in Accra. On the one hand, especially since it is impossible to delineate precisely when infection occurred, the PAF may be overestimated, since some of the clients may have acquired their infection from another type of sexual partner or, less likely, through a different mode of transmission. Given the relatively low general population HIV prevalence in Accra, however, this is unlikely to make a significant difference to the estimated PAF. On the other hand, the estimate of the size of the client population in Accra used in the PAF calculation corresponds to the number of men who visited a FSW in the last year. Since prevalent HIV reflects lifetime risk, many men who had previously visited a FSW (but had not done so during the year preceding the study) will not be counted in the client population, thus leading to an underestimation of the PAF.

Second, as pointed out by Côté et al., the method of estimation employed is quite sensitive to uncertainties in the measures of the parameters needed to compute the PAF. This level of uncertainty is exacerbated by the fact that most of these parameters (size of the FSW population, number of client-contacts reported by FSW, number of visits to FSW reported by clients, HIV prevalence in the general population) are obtained from different sources.

Third, the clients’ studies in both Accra [1] and Cotonou [2-4] were carried out using similar methodology in the overt transactional sex milieu, where prostitution can be described as ‘professional'. As such, they do not take into account more clandestine forms of prostitution, which are often practised in different settings on a part-time basis by women whose male clientele may be quite different to that of professional FSW. This would result in an underestimation of the PAF.

Finally, the method of PAF estimation used is static and does not take into account HIV transmission dynamics: it will not, for example, count as a case attributable to transactional sex a non-client infected man who acquired HIV from a regular female partner, who herself acquired it from a man infected through sexual contact with a FSW.

Despite these limitations, which could lead either to underestimation or to overestimation of the PAF, the data from Accra and Cotonou strongly suggest that transactional sex is the driving force of the epidemic, accounting for the majority of HIV cases among adult men, in settings where overall HIV prevalence is still moderate in the general population, such as the many West African countries where HIV prevalence remains under 5% in the general population. Such men then act as a bridging population, transmitting HIV from the core group of FSW to their other, non-FSW sexual partners [2]. In situations such as these, where there is a significant differential between HIV prevalence in sex workers, their clients, and the general population, interventions targeted at FSW and their clients could substantially delay the onset and reduce the magnitude of a widespread epidemic in the general population [5]. A recent study from Dakar, Senegal, also in West Africa, similarly demonstrated a higher HIV prevalence among clients of FSW than among the general population [6]. But what about the role of transactional sex in countries where the HIV epidemic is more explosive and still on the rise, as in the countries of Southern Africa, and in settings with more mature epidemics, as in East Africa and some West African countries?

A study carried out in 1999 among truck drivers visiting FSW in KwaZulu-Natal, South Africa showed an HIV prevalence of 56% in this population [7]. The differential between this and the HIV prevalence in the general population of this region at the time of the survey (20–25%) suggests that, even in explosive epidemics, interaction between FSW and their clients, and subsequently between these men and other non-FSW women, may be of importance in the dynamics of HIV transmission. Interestingly, in this study, HIV prevalence was exactly the same (56%) among FSW and their clients [7], whereas it was five- to tenfold higher in FSW than in their clients in both Cotonou [4,8] and Accra [1,9]. This could be partly because most Beninese and Ghanaian men are circumcised, which is not the case in South Africa. Indeed, circumcision has been convincingly shown to be protective for HIV transmission [10], to the point where, in a study carried out among HIV-discordant couples in Rakai district, Uganda, there was no case of female-to-male transmission in 50 circumcised men followed-up for a total of 106 person-years, compared with an HIV incidence of 16.7/100 person-years among 137 uncircumcised men [11]. This could explain the relatively slow spread of HIV from FSW to their clients and subsequently to the general population observed in both Cotonou and Accra.

In Abidjan, Côte d'Ivoire, the epidemic is more mature, with an HIV prevalence that has been stable for several years at approximately 10%. Here, HIV prevalence among clients of FSW was 13.4% in 1999, a figure quite close to that of the general population [12]. However, only 25% of these men were older than 30 years and prevalence in this older group was 26.6%. As young men starting their sexual life have a very low HIV prevalence and may, in some cases, have some of their earliest sexual experiences with FSW, prevention of HIV transmission in transactional sex settings could make a significant difference for the next generation in countries with currently mature epidemics, which could then possibly die out if the basic reproductive rate (R0) of HIV transmission were kept < 1 in young people.

Some studies in West Africa have shown that it is possible to implement successful preventive interventions targeting FSW [8,13]. More recently, it has been shown that clients of FSW are also a reachable population [1,4,6,12] and that interventions targeting these men can also be successful in terms of increasing condom use and decreasing rates of sexually transmitted infections [3,14]. Given the convincing evidence accumulating about the central role of transactional sex in the HIV epidemic, scaling up of interventions targeting FSW, both in intensity and geographical coverage, is urgently required, and these interventions should simultaneously target the men who have sex with them, in all settings where heterosexual HIV transmission is predominant.

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1. Côté AM, Sobela F, Dzokoto A, Nzambi K, Asamoah-Adu C, Labbé AC, et al. Transactional sex is the driving force in the dynamics of HIV in Accra, Ghana. AIDS 2004, 18:000–000.
2. Lowndes CM, Alary M, Meda H, Gnintoungbé CAB, Mukenge-Tshibaka L, Adjovi C, et al. Role of core and bridging groups in the transmission dynamics of HIV and STIs in Cotonou, Benin, West Africa. Sex Transm Infect 2002, 78(suppl i):i69-i77.
3. Lowndes CM, Alary M, Labbé AC, Gnintoungbé C, Belleau M, Mukenge-Tshibaka L, et al. Male clients of female sex workers in Cotonou, Benin (West Africa): contributions to the HIV epidemic and effect of targeted interventions. 15th Biennial Congress of the International Society for Sexually Transmitted Diseases Research, Ottawa, July 2003 [abstract 0729].
4. Lowndes CM, Alary M, Gnintoungbé CAB, Bédard E, Mukenge L, Geraldo N, et al. Management of sexually transmitted diseases and HIV prevention in men at high risk: targeting clients and non-paying sexual partners of female sex workers in Benin. AIDS 2000, 14:2523-2534.
5. Boily MC, Lowndes C, Alary M. The impact of HIV epidemic phases on the effectiveness of core group interventions: insights from mathematical models. Sex Transm Infect 2002, 78(suppl i): i78-i90.
6. Gomes do Espirito Santo ME, Etheredge GD. How to reach clients of female sex workers: a survey by surprise in brothels in Dakar, Senegal. Bull World Health Organ 2002, 80:709-713.
7. Ramjee G, Gouws E. Prevalence of HIV among truck drivers visiting sex workers in KwaZulu-Natal, South Africa. Sex Transm Dis 2002, 29:44-49.
8. Alary M, Mukenge-Tshibaka L, Bernier F, Geraldo N, Lowndes CM, Meda H, et al. Decline in the prevalence of HIV and sexually transmitted diseases among female sex workers in Cotonou, Benin, 1993–99. AIDS 2002, 16:463-470.
9. Asamoah-Adu C, Khonde N, Avorkliah M, Bekoe V, Alary M, Mondor M, et al. HIV infection among sex workers in Accra: need to target new recruits entering the trade. J Acquir Immune Defic Syndr 2001, 28:358-366.
10. Weiss HA, Quigley MA, Hayes RJ. Male circumcision and risk of HIV infection in sub-Saharan Africa: a systematic review and meta-analysis. AIDS 2000, 24:2361-2370.
11. Quinn TC, Wawer MJ, Sewankambo N, Serwadda D, Li C, Wabwire-Mangen F, et al. Viral load and heterosexual transmission of human immunodeficiency virus type 1. Rakai Project Study Group. N Engl J Med 2000, 342:921-929.
12. Vuylsteke BL, Ghys PD, Traoré M, Konan Y, Mah-Bi G, Maurice C, et al. HIV prevalence and risk behaviour among clients of female sex workers in Abidjan, Côte d'Ivoire. AIDS 2003, 17:1691-1694.
13. Ghys PD, Diallo MO, Ettiègne-Traoré V, Kalé K, Tawil O, Caraël M, et al. Increase in condom use and decline in HIV and sexually transmitted diseases among female sex workers in Abidjan, Côte d'Ivoire, 1991–1998. AIDS 2002, 16:251-258.
14. Lowndes CM, Alary M, Belleau M, Batona G, Gnintoungbé CAB, Meda H. Interventions directed at male clients of female sex workers in Cotonou, Benin, West Africa. Int J STD & AIDS 2001, 12 (suppl 2):81.

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transactional sex; clients of sex workers; HIV prevention; core groups; bridging groups; population attributable fraction; Africa

© 2004 Lippincott Williams & Wilkins, Inc.