Scale-up of combination prevention and antiretroviral therapy for female sex workers in West Africa: time for action
Alary, Michela,b,c; Lowndes, Catherine M.a,d,e; Van de Perre, Philippef; Béhanzin, Luca,b; Batona, Georgesa,g; Guédou, Fernand A.a,g; Konate, Issoufh; Traore, Isidorei; Asamoah-Adu, Comfortj; Akinocho, Evelynek; Nagot, Nicolasf
aURESP, Centre de recherche du CHU de Québec
bDépartement de médecine sociale et préventive, Université Laval
cInstitut national de santé publique du Québec, Québec, Canada
dHealth Protection Agency
eLondon School of Hygiene and Tropical Medicine, London, UK
fINSERM U 1058, Université Montpellier I, Montpellier, France
gDispensaire IST, Cotonou, Bénin
hCentre Muraz, Bobo-Dioulasso
iCentre de recherche international pour la santé, Université de Ouagadougou, Burkina Faso
jGhana West Africa Project to Combat AIDS and STI, Accra, Ghana
kProgramme National de lutte contre le Sida et les IST, Cotonou, Bénin.
Correspondence to Dr Michel Alary, CHU de Québec, Hôpital du Saint-Sacrement, 1050 Chemin Ste-Foy; G1S 4L8, Québec (Québec), Canada. Tel: +1418 682 7387; fax: +418 682 7949; e-mail: email@example.com
Received 16 October, 2012
Revised 4 January, 2013
Accepted 5 February, 2013
HIV epidemiology in West Africa
Surveillance data indicate that most West African countries have experienced concentrated HIV epidemics. Whereas HIV prevalence in the general population was less than 2% in nine of the 11 West African countries where such data were available in 2008, it was more than eight times higher among female sex workers (FSWs) in 10 of these countries . Analysis of HIV transmission dynamics also indicates largely concentrated HIV epidemics in these 10 countries. For example, in Accra, Ghana, and Cotonou, Benin, over 75% of prevalent cases of HIV among men were related to sexual intercourse with FSWs, with onwards transmission from clients of FSWs accounting for most infections in women of the general population [2–4].
In contrast, the WHO/UNAIDS classification of the HIV epidemic as generalized in 12 of the 15 West African countries  was largely due to the use of the numerical proxy of at least 1% prevalence among women attending antenatal care (ANC), as proposed in 2000 . Interestingly, this numerical proxy was dropped from the recently published updated definitions, which are now based solely on HIV transmission dynamics , that is, whether transmission in the general population is self-sustaining or dependent on outwards transmission from high-risk groups.
Response to the HIV epidemic in West Africa
As a result of the inconsistent classification of epidemic states, most West African countries have focused the response to the epidemic on the general population and relatively low-risk groups, with little budget allocated to the most vulnerable populations, including FSWs . A notable exception is Senegal, where the HIV epidemic has always been considered as concentrated, with ANC HIV prevalence less than 1%, a situation attributed largely to the early national response, including prevention programmes specifically targeting FSWs, in a context in which sex work is legalized .
A regional project funded by the Canadian International Development Agency (CIDA) implemented interventions targeting FSWs in major cities in nine West African countries from 2001 to 2006. Following CIDA disengagement, these interventions were mainly discontinued, except in Ghana and Benin. In Ghana, the CIDA-funded project staff set up a donor-funded NGO, the Ghana West-Africa Project to Combat AIDS and STI, which influenced the National AIDS Commission in its decision to implement interventions targeting FSWs and other high-risk groups throughout the country . In Benin, FSW interventions were scaled up to cover the whole country by the National AIDS Control Programme, a process which faced major difficulties, largely because of structural issues hampering the integration of the different components of the interventions, and timely disbursement .
In Côte d’Ivoire, the PAPO-HV project, mainly funded by PEPFAR and based on the successful project RETRO-CI in Abidjan , was initiated in 2004 and progressively scaled-up its activities to cover 13 sites throughout the country by 2008. After a brief interruption in 2010 , the project resumed under the name of Impact-CI . In Burkina Faso, FSW interventions were implemented as part of a research project initiated in 1998 in Bobo-Dioulasso and 2008 in Ouagadougou . However, these interventions have not yet been integrated into sustainable national programmes.
Thus, for FSW-targeted programmes in most West African countries, the present is sobering and the future uncertain. There is however some hope for improvement, as the 2011–2015 UNAIDS strategic framework recognizes the under-development of programmes targeting FSWs, the necessity for their expansion with the involvement of FSWs themselves, and the need to fight to improve the human rights of marginalized populations .
Effectiveness of prevention and treatment interventions targeting female sex workers
Early into the HIV epidemic, the central role of the most at-risk populations (then called core groups) – including FSWs – in the spread of the HIV epidemic was recognized . Early studies in Nairobi, Kenya, showed that health education and condom promotion were successful at increasing condom use among FSWs . Complementary modelling exercises suggested that this intervention covering 1000 FSWs could prevent 6000–10 000 HIV cases per year among clients of FSWs and their contacts in the general population, and were highly cost-effective . In Zaire and Thailand, similar interventions, augmented by screening and treatment of curable sexually transmitted infections (STIs), were successful at decreasing HIV and/or other STIs in both FSWs  and the general population . Subsequent observational studies in West Africa demonstrated similarly favourable postintervention HIV/STI trends among FSWs. In Abidjan, Côte d’Ivoire, between 1992 and 1998, there was a decrease in HIV, gonorrhea and genital ulcer prevalence, from 89 to 32%, 33 to 11% and 21 to 4%, respectively . In Cotonou, Benin, HIV prevalence decreased from 53 to 33% between 1993 and 2005; and gonorrhoea prevalence from 43 to 3% [21,22]. Mathematical modelling studies indicated that as a result, about 50% of HIV infections were prevented in the general population in Cotonou , and a recent empirical study showed that the FSW intervention could be linked to a decrease in HIV prevalence among men aged less than 30 years, from 3.0% in 1998 to 0.5% in 2008 . A recent systematic review concluded that, despite a lack of randomized controlled trial data, available evidence supported the effectiveness of comprehensive combination prevention – including behavioural interventions, improved access to STI treatment and structural measures – in reducing HIV and STI acquisition among FSWs .
The strength of evidence supporting the effectiveness of comprehensive interventions targeting FSWs was considered adequate for their replication and scale-up to a level never before achieved by Avahan, the India AIDS Initiative of the Bill & Melinda Gates Foundation, starting in 2004 . Around 350 000 FSWs were reached by the programme, with monthly intervention coverage of over 75% of identified FSWs in the areas targeted . The evaluation of Avahan, based on triangulation of multiple approaches, provides further compelling evidence that comprehensive interventions can significantly curb the HIV epidemic not only among FSWs, but also in the general population, in a country with a concentrated HIV epidemic, with an estimated more than 100 000 HIV cases averted by the intervention [28–30].
Small-scale demonstration projects, mainly carried out in West Africa, indicate that antiretroviral therapy (ART) can be successfully implemented among FSWs, with satisfactory immunological and virological responses [14,31–33], good treatment compliance levels [31,32], and maintenance or even improvement of safe sex behaviour [14,34–36]. Some of these studies underline the importance of strongly linking prevention with care through the integration of HIV/STI care services and community-based prevention packages [14,34]. Scaling-up treatment programmes for marginalized, hard-to-reach populations, such as FSWs, will undoubtedly be challenging. Nevertheless, in addition to the health equity issues related to access to ART for FSWs, the application of ‘test and treat’ strategies in this population could substantially impact HIV prevention at the general population level , given recent trial data showing that the implementation of this strategy among serodiscordant couples led to a 96% reduction in HIV transmission . Such a strategy should however be carefully evaluated in the target population before implementation and scale-up, and would require specific adherence support and community involvement.
The way forward
With an epidemic largely driven by the most at-risk populations, especially FSWs, and a renewed interest in interventions targeting these populations, it is time to move forward to successfully curtail the HIV epidemic in West Africa, as has been achieved in several Asian countries with concentrated epidemics. Table 1 details the components of the comprehensive, integrated prevention and treatment interventions that we propose.
Table 1-a Elements o...Image Tools
Generation of the political will and financial support necessary to implement, scale up and sustain the integration of national HIV care and prevention services targeting FSWs will be key , particularly at a time when the sustainability of donor programs for HIV control is debated . In a context of scarce resources, wherein high-impact actions should take precedence, United Nations agencies, such as UNAIDS and the World Bank, will need to strongly advocate the prioritisation of such interventions with the national authorities. As is already the case in Benin  and Côte d’Ivoire , units responsible for coordinating targeted interventions should be created within the government structures in charge of the fight against HIV/AIDS. These units will be essential to link and integrate the clinical, community and structural components of the interventions, as well as their monitoring and evaluation, to fully realize the benefits of combination prevention [42,43] and expanded treatment services. Interventions should also target clients and other male sexual partners of FSWs as in the West African context, they constitute the main bridge population for HIV transmission to the general population [2–4,44] and can be targeted successfully by preventive interventions . To achieve sustainability, it will be important that all donors adhere to the national programmes by supporting the targeted intervention units.
Table 1-b Elements o...Image Tools
Finally, with the recent decrease in HIV prevalence in many countries of Southern and East Africa , a ‘reversed’ epidemiological transition from generalized to concentrated epidemics is likely to occur in many settings. In this context, the targeted interventions that we propose for West Africa will also be essential for effective HIV control in these countries.
M.A., C.M.L. and N.N. conceptualized the article. Its content was discussed with all the other co-authors who brought their respective expertise to the content (epidemiologic research and prevention program design for LB and FG, field work and program evaluation for GB, clinical research for PVDP, IK and IT, program management at the government level for EA and program management at the NGO level for CAA). M.A. drafted the article and all authors contributed edits to the article and approved its final content.
Conflicts of interest
All authors declare that they have no conflict of interest.
2. Alary M, Lowndes CM. The central role of clients of female sex workers in the dynamics of heterosexual HIV transmission in sub-Saharan Africa
. AIDS 2004; 18:945–947.
3. Cote AM, Sobela F, Dzokoto A, Nzambi K, Asamoah-Adu C, Labbe AC, et al. Transactional sex is the driving force in the dynamics of HIV in Accra, Ghana
. AIDS 2004; 18:917–925.
4. Lowndes CM, Alary M, Meda H, Gnintoungbe CA, 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 1):i69–i77.
7. UNAIDS/WHO Working Group on Global HIV/AIDS and sexually transmitted infections Surveillance. Guidelines for second generation HIV surveillance: an update: know your epidemic. 2011. Geneva: World Health Organization;
8. Meda N, Ndoye I, M’Boup S, Wade A, Ndiaye S, Niang C, et al. Low and stable HIV infection rates in Senegal: natural course of the epidemic or evidence for success of prevention?
. AIDS 1999; 13:1397–1405.
10. Batona G, Lafrance C, Kessou L, Gbedji E, Anani H, Semini I, et al.Analyse de l’efficacité des programmes de santé et de lutte contre les IST/VIH ciblant les travailleuses du sexe et leurs partenaires sexuels au Bénin. 2012. Washington, DC:The World Bank, CNLS Benin, CHA Université Laval;
11. Ghys PD, Diallo MO, Ettiegne-Traore V, Kale K, Tawil O, Carael M, et al. Increase in condom use and decline in HIV and sexually transmitted diseases among female sex workers in Abidjan, Cote d’Ivoire, 1991–1998
. AIDS 2002; 16:251–258.
12. Vuylsteke B, Semde G, Sika L, Crucitti T, Ettiegne Traore V, Buve A, et al. HIV and STI prevalence among female sex workers in Cote d’Ivoire: why targeted prevention programs should be continued and strengthened
. PLoS One 2012; 7:e32627.
14. Konate I, Traore L, Ouedraogo A, Sanon A, Diallo R, Ouedraogo JL, et al. Linking HIV prevention and care for community interventions among high-risk women in Burkina Faso: the ARNS 1222 ‘Yerelon’ cohort
. J Acquir Immune Defic Syndr 2011; 57 (Suppl 1):S50–S54.
16. Plummer FA, Nagelkerke NJ, Moses S, Ndinya-Achola JO, Bwayo J, Ngugi E. The importance of core groups in the epidemiology and control of HIV-1 infection
. AIDS 1991; 5 (Suppl 1):S169–S176.
17. Ngugi EN, Plummer FA, Simonsen JN, Cameron DW, Bosire M, Waiyaki P, et al. Prevention of transmission of human immunodeficiency virus in Africa: effectiveness of condom promotion and health education among prostitutes
. Lancet 1988; ii:887–890.
18. Moses S, Plummer FA, Ngugi EN, Nagelkerke NJ, Anzala AO, Ndinya-Achola JO. Controlling HIV in Africa: effectiveness and cost of an intervention in a high-frequency STD transmitter core group
. AIDS 1991; 5:407–411.
19. Laga M, Alary M, Nzila N, Manoka AT, Tuliza M, Behets F, et al. Condom promotion, sexually transmitted diseases treatment, and declining incidence of HIV-1 infection in female Zairian sex workers
. Lancet 1994; 344:246–248.
20. Hanenberg RS, Rojanapithayakorn W, Kunasol P, Sokal DC. Impact of Thailand's HIV-control programme as indicated by the decline of sexually transmitted diseases
. Lancet 1994; 344:243–245.
21. 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, 1993-1999
. AIDS 2002; 16:463–470.
22. Béhanzin L, Diabaté S, Minani I, Boily MC, Labbe AC, Ahoussinou C, et al.Decline in the prevalence of HIV and sexually transmitted infections among female sex workers in Benin over 15 years of targeted interventions.
J Acquir Immune Defic Syndr 2013 [Epub ahead of print]
23. 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 1):i78–i90.
24. Behanzin L, Diabate S, Minani I, Lowndes CM, Boily MC, Labbe AC, et al. Decline in HIV prevalence among young men in the general population of Cotonou, Benin, 1998-2008
. PLoS One 2012; 7:e43818.
25. Shahmanesh M, Patel V, Mabey D, Cowan F. Effectiveness of interventions for the prevention of HIV and other sexually transmitted infections in female sex workers in resource poor setting: a systematic review
. Trop Med Int Health 2008; 13:659–679.
26. Chandrasekaran P, Dallabetta G, Loo V, Mills S, Saidel T, Adhikary R, et al. Evaluation design for large-scale HIV prevention programmes: the case of Avahan, the India AIDS initiative
. AIDS 2008; 22 (Suppl 5):S1–S15.
27. Verma R, Shekhar A, Khobragade S, Adhikary R, George B, Ramesh BM, et al. Scale-up and coverage of Avahan: a large-scale HIV-prevention programme among female sex workers and men who have sex with men in four Indian states
. Sex Transm Infect 2010; 86 (Suppl 1):i76–i82.
28. Moses S, Ramesh BM, Nagelkerke NJ, Khera A, Isac S, Bhattacharjee P, et al. Impact of an intensive HIV prevention programme for female sex workers on HIV prevalence among antenatal clinic attenders in Karnataka state, south India: an ecological analysis
. AIDS 2008; 22 (Suppl 5):S101–S108.
29. Ng M, Gakidou E, Levin-Rector A, Khera A, Murray CJ, Dandona L. Assessment of population-level effect of Avahan, an HIV-prevention initiative in India
. Lancet 2011; 378:1643–1652.
30. Pickles M, Foss AM, Vickerman P, Deering K, Verma S, Demers E, et al. Interim modelling analysis to validate reported increases in condom use and assess HIV infections averted among female sex workers and clients in southern India following a targeted HIV prevention programme
. Sex Transm Infect 2010; 86 (Suppl 1):i33–i43.
31. Diabaté S, Zannou DM, Geraldo N, Chamberland A, Akakpo J, Ahouada C, et al. Antiretroviral therapy among HIV-1 infected female sex workers in Benin: a comparative study with patients from the general population
. World J AIDS 2011; 1:94–99.
32. Huet C, Ouedraogo A, Konate I, Traore I, Rouet F, Kabore A, et al. Long-term virological, immunological and mortality outcomes in a cohort of HIV-infected female sex workers treated with highly active antiretroviral therapy in Africa
. BMC Public Health 2011; 11:700.
33. McKinnon LR, Kimani M, Wachihi C, Nagelkerke NJ, Muriuki FK, Kariri A, et al. Effect of baseline HIV disease parameters on CD4+ T cell recovery after antiretroviral therapy initiation in Kenyan women
. PLoS One 2010; 5:e11434.
34. Braunstein SL, Umulisa MM, Veldhuijzen NJ, Kestelyn E, Ingabire CM, Nyinawabega J, et al. HIV diagnosis, linkage to HIV care, and HIV risk behaviors among newly diagnosed HIV-positive female sex workers in Kigali, Rwanda
. J Acquir Immune Defic Syndr 2011; 57:e70–e76.
35. Diabaté S, Chamberland A, Nassirou G, Zannou DM, Massinga Loembé M, Anagonou S, et al. Condom use during work time among female sex workers in Benin
. Sex Transm Infect 2011; 87 (Suppl 1):A41–A42.
36. McClelland L, Wanje G, Kashonga F, Kibe L, McClelland RS, Kiarie J, et al. Understanding the context of HIV risk behavior among HIV-positive and HIV-negative female sex workers and male bar clients following antiretroviral therapy rollout in Mombasa, Kenya
. AIDS Educ Prev 2011; 23:299–312.
37. Delva W, Eaton JW, Meng F, Fraser C, White RG, Vickerman P, et al. HIV treatment as prevention: optimising the impact of expanded HIV treatment programmes
. PLoS Med 2012; 9:e1001258.
38. Cohen MS, Chen YQ, McCauley M, Gamble T, Hosseinipour MC, Kumarasamy N, et al. Prevention of HIV-1 infection with early antiretroviral therapy
. N Engl J Med 2011; 365:493–505.
39. Montague BT, Vuylsteke B, Buve A. Sustainability of programs to reach high risk and marginalized populations living with HIV in resource limited settings: implications for HIV treatment and prevention
. BMC Public Health 2011; 11:701.
40. Bennett S, Singh S, Ozawa S, Tran N, Kang JS. Sustainability of donor programs: evaluating and informing the transition of a large HIV prevention program in India to local ownership
. Glob Health Action 2011; 4:7360.
41. [Accessed 2 January 2013] Conseil national de la lutte contre le sida, République de Côte d’Ivoire. Le programme de lutte contre le Sida chez les personnes hautement vulnérables (PLS-PHV). http://www.mlsida.gouv.ci/index.php/faq?start=1
42. Hankins CA, de Zalduondo BO. Combination prevention: a deeper understanding of effective HIV prevention
. AIDS 2010; 24 (Suppl 4):S70–S80.
43. Merson M, Padian N, Coates TJ, Gupta GR, Bertozzi SM, Piot P, et al. Combination HIV prevention
. Lancet 2008; 372:1805–1806.
44. Lowndes CM, Alary M, Gnintoungbe CA, Bedard E, Mukenge L, Geraldo N, et al. Management of sexually transmitted diseases and HIV prevention in men at high risk: targeting clients and nonpaying sexual partners of female sex workers in Benin
. AIDS 2000; 14:2523–2534.
45. Lowndes CM, Alary M, Labbe AC, Gnintoungbe C, Belleau M, Mukenge L, et al. Interventions among male clients of female sex workers in Benin, West Africa: an essential component of targeted HIV preventive interventions
. Sex Transm Infect 2007; 83:577–581.
female sex workers; HIV; prevention; treatment; West Africa
© 2013 Lippincott Williams & Wilkins, Inc.
Highlight selected keywords in the article text.