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A Short History of HIV Prevention Programs for Female Sex Workers in Ghana: Lessons Learned Over 3 Decades

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Background: Female sex workers (FSWs) in Ghana have a 10-fold greater risk for acquiring HIV than the general adult population, and they contribute a substantial proportion of the new HIV infections in the country. Although researchers have conducted
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  S UPPLEMENT  A RTICLE  A Short History of HIV Prevention Programs for Female Sex Workers in Ghana: Lessons Learned Over 3 Decades  Peter Wondergem, MSc, *  Kimberly Green, PhD, †   Samuel Wambugu, MPH, †  Comfort Asamoah-Adu, MA,  ‡  Nana Fosua Clement, MA, †   Richard Amenyah, MD,§  Kyeremeh Atuahene, MA, k  and Michael Szpir, PhD †  Background:  Female sex workers (FSWs) in Ghana havea 10-fold greater risk for acquiring HIV than the general adult  population, and they contribute a substantial proportion of the newHIV infections in the country. Although researchers have con-ducted behavioral and biological surveys, there has been noreview of the contextual, programmatic, and epidemiologicalchanges over time. Methods:  The authors conducted a historical review of HIV prevention programs in Ghana. We reviewed the use of different interventions for HIV prevention among FSWs and data from program monitoring and Integrated Biological and BehavioralSurveillance Surveys. In particular, we looked at changes inservice access and coverage, the use of HIV testing and counselingservices, and the changing prevalence of HIV and other sexuallytransmitted infections. Results:  HIV prevention interventions among FSWs increased greatly between 1987 and 2013. Only 72 FSWs were reached ina pilot program in 1987, whereas 40,508 FSWs were reached duringa national program in 2013. Annual condom sales and the proportionof FSWs who used HIV testing and counseling services increased signi 󿬁 cantly, whereas the prevalence of gonorrhea and chlamydiadecreased. The representation of FSWs in national HIV strategic plans and guidelines also improved. Conclusions:  Ghana offers an important historical example of an evolving HIV prevention program that   —  despite periods of inactivity  —  grew in breadth and coverage over time. The preventionof HIV infections among sex workers has gained momentum inrecent years through the efforts of the national government and its partners  —  a trend that is critically important to Ghana ’ s future. Key Words:  female sex workers, HIV prevention programs,Ghana, history(  J Acquir Immune De   󿬁 c Syndr   2015;68:S138  –  S145) BACKGROUND Female sex work has a long history on the  “ Gold Coast  ”  of Africa (now modern Ghana). Records from the 17thand early 18th centuries describe the existence of a community- based institution of   “  public women ”  in the southern part of thecountry. These women were slaves  —  acquired by the politicalelite from local communities  —  who were compelled to providesexual services to local bachelors. 1 Public women were generallyaccepted as playing an important social role in the community.The institution has evolved over the centuries, and sexwork is no longer socially acceptable in Ghana. Indeed, thelaw prohibits sexual solicitations, and the possession of condoms is considered as evidence in the prosecution of female sex workers (FSWs). FSWs are also exposed to highlevels of abuse and extortion by the authorities; a recent human rights report based on a convenience sample notes that 34% of the respondents had been raped by a police of  󿬁 cer. 2 Despite the repressive social and legal environment for FSWs in Ghana, 52,000 FSWs were counted across thecountry in 2011; nearly 20,000 resided in the Greater AccraRegion, 3,4 where the capital city is located. The number of sexworkers has increased considerably in the past few decades: Asrecently as the 1950s, only 213 FSWs were known in the cityof Accra. 5 Signi 󿬁 cant economic development, populationgrowth, and migration may have been important factorsthat contributed to the dramatic increase of FSWs. One of the events that might have been especially in 󿬂 uential was theconstruction of the Akosombo hydroelectric dam in the 1960s.The dam- 󿬂 ooded land, northeast of Accra, was inhabited bythe Krobo people, who consequently faced severe economichardships. In the wake of these dif  󿬁 culties, countless youngKrobo women left Ghana in the following 3 decades to seek work in Cote d  ’ Ivoire and other neighboring countries  —  all of which had a higher prevalence of HIV than did Ghana. 6,7 These migrations may have played an important role inthe rise of the HIV epidemic in Ghana. During the late 1980s,FSWs in Accra (who had recently worked in Cote d  ’ Ivoire)were the primary population diagnosed with HIV. 8,9 Sincethat time, the prevalence of HIV among pregnant women indistricts where those sex workers srcinated has consistently been signi 󿬁 cantly higher than the national average. 3 Morerecently, a booming economy in the southern part of thecountry, and unemployment and poor education in the north,may have augmented the  “  push-and-pull ”  factors for paid sex.This could explain the rising numbers of FSWs from the From the *United States Agency for International Development, Yaounde,Cameroon;  † FHI 360, Accra, Ghana and Durham, NC;  ‡ West AfricaProgram to Combat AIDS and STI, Accra, Ghana; §UNAIDS-TSF,Ouagadougou, Burkina Faso; and   k Accra, Ghana AIDS Commission.Supported by United States Agency for International Development and FHI 360.The authors have no con 󿬂 icts of interest to disclose.Correspondence to: Peter Wondergem, MSc, United States Agency for International Development, US Embassy, Rosa Parks Avenue, P.O. Box817, Yaounde, Cameroon (e-mail: pwondergem@usaid.gov).Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved. S138  | www.jaids.com  J Acquir Immune Defic Syndr     Volume 68, Supplement 2, March 1, 2015 Copyright © 201 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. 5  north in southern urban slums and increases in transactionalsex among young women and older men. 10 Whatever the causes, FSWs in Ghana are currently 10times more likely to be HIV positive than the general population. 3 They also contribute a substantial proportionof the new HIV infections in the country. A 2004 studyreported that 84% of the HIV infections among males inAccra are attributable to interactions with FSWs. 11 A 2010modeling study of the HIV epidemic in West Africasuggested that 31% of new HIV infections in Ghana arerelated to sex work, either directly (sex workers and clients)or indirectly (partners of clients). 12,13 The history and the data suggest that FSWs shoulder a signi 󿬁 cant burden of the HIV infections in Ghana. Here, wedescribe 3 historical phases of HIV prevention interventionsamong FSWs  —  recounting the results, the missed opportuni-ties, and the nation ’ s need to adapt to a rapidly changingepidemic. We explore the evolution of these interventions between 1987 and 2013, focusing on the coverage of the keyinterventions and the sociopolitical dynamics during that  period. We also describe behavioral changes among FSWsassociated with seeking health services and HIV preventionservices between 1997 and 2011. METHODS Our historical review of FSWs in Ghana explored thedifferences between HIV prevention interventions throughtime, changes in service access and coverage, and the use of HIV testing and counseling (HTC) services. We alsoinvestigated the median time of involvement in sex work and the changing prevalence of HIV and other sexuallytransmitted infections (STIs), namely chlamydia and gonor-rhea. Comparisons are disaggregated by FSW type:  “ seater  ” or   “ roamer. ”  Seaters are home-based sex workers, whereasroamers are street-based or venue-based sex workers. 3 We conducted 3 stages of data review. In March 2013,we conducted a literature search on several databases  —  PubMed, Embase, CINAHL Journal Search, Global Health,PsycINFO, POPLINE, and the International AIDS Societyconference abstracts  —  using the search terms  “ female sexworker  ”  or   “  prostitute, ”  or   “ transactional sex ”  or   “ sex trade ” or   “ sexual exchange, ”  and   “ HIV ”  or   “ AIDS ”  or   “ STI, ”  and  “ Ghana. ”  We searched the literature for original researcharticles in the English language dating between 1987 and March 2013. A total of 133 articles were identi 󿬁 ed. Onlyarticles that described the design and results of HIV preventioninterventions among FSWs in Ghana were included (n = 17).Second, we identi 󿬁 ed and reviewed project reports of HIV prevention interventions among FSWs in Ghana that took place between 1987 and 2013. The review focused onreports from organizations involved in HIV preventionservices design and delivery: the Ghana AIDS Commission(GAC), West Africa Program to Combat AIDS and STI(WAPCAS), United States Agency for International Devel-opment (USAID), and FHI 360. We extracted information onthe design, implementation, and lessons learned related tothese FSW HIV prevention services and service delivery dataincluding the number of FSWs reached, the number of FSWsthat accessed HTC, and the number of FSWs that werescreened for STIs.Third, we compared data from published cross-sectional Integrated Biological and Behavioral SurveillanceSurveys of FSWs in Ghana, including the median time of involvement in sex work and the prevalence of HIV,chlamydia, and gonorrhea. The authors reviewed these datato identify any trends or patterns in the implementation of HIV prevention programs to describe the interventions and their results and to explore changes in the prevalence of HIV,chlamydia, and gonorrhea over time. First Phase: Early Experiments in an EvolvingEpidemic (1987 to 1996) In 1985, before the identi 󿬁 cation of Ghana ’ s  󿬁 rst case of AIDS in 1986, the National Committee on AIDS was formed under the leadership of Professor A. R. Neequaye of the GhanaMedical School. Neequaye was the principal investigator of Africa ’ s  󿬁 rst intervention that involved peer education for sexworkers, which was initiated in May 1987. 8,14 Private founda-tions  —  especially the American Foundation for AIDSResearch, championed by the American actress ElisabethTaylor   —  were the  󿬁 rst to provide funds to Family HealthInternational (now FHI 360) that implemented a pilot programfor work that was considered to be controversial at the time. 15 The small pilot project involved 6 sex worker leaderswho were identi 󿬁 ed, recruited, and trained about HIV and its prevention. The leaders educated their peers on safer sexual practices and received a small stipend for their efforts.Condoms and spermicidal foaming tablets were also distrib-uted at no charge by the peer educators.The program documented some encouraging outcomes.The proportion of FSWs who understood that HIV could betransmitted from a healthy-looking man increased from 1 in 3 (inJune 1987) to 9 in 10 women (in January 1988). 16 The reported regular use of condoms or spermicides increased signi 󿬁 cantlyfrom 13% to 89%. Similar programs were later expanded toMali, Cameroon, and Mexico with similar results. 16 In 1988, USAID cofunded the Ghana peer education program when the AIDSTECH Project was awarded to FHI360. 16 A follow-on program would later attempt to expand coverage in Accra. Other programs initiated at this timeincluded attempts to provide home-based care and alterna-tive sources of income for returning sex workers in Krobo. 17 This period also saw the  󿬁 rst handbook on HIV interven-tions for FSWs, which described the  “ targeting of pre-vention programs in Africa. ”  No account of these programsexists beyond 1990, when the national focus shifted to thegeneral population.These brief pilot programs provided evidence that   “  peer education may be an effective way to provide HIV/AIDSinformation to commercial sex workers, and it results inreports of increased condom use. ” 17 But, the opportunity toscale-up and achieve a meaningful impact during the earliest stages of the HIV epidemic was lost. It would be 6 years before interventions for HIV prevention among sex workerswould start again in Ghana.  J Acquir Immune Defic Syndr     Volume 68, Supplement 2, March 1, 2015  Female Sex Workers and HIV Prevention in Ghana  Copyright     2015 Wolters Kluwer Health, Inc. All rights reserved.  www.jaids.com  | S139 Copyright © 201 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. 5  Second Phase: A Clinical Approach toPrevention Interventions for Sex Workers(1996 to 2006) In 1996, the WAPCAS was initiated to control HIV and other STIs among most-at-risk populations, especiallyFSWs. 18 Between 1996 and 2006, the Canadian InternationalDevelopment Association (CIDA) provided   󿬁 nancial and technical support for WAPCAS through the  Center Hospi-talier Universitaire de Sherbrooke . During this period,WAPCAS was part of a regional project that was implemented in 9 West African countries: Togo, Cote d  ’ Ivoire, BurkinaFaso, Mali, Senegal, Guinea, Benin, Niger, and Ghana. 18 The CIDA and the Ministry of Health (MOH) agreed that WAPCAS should use a  “ low-key ”  approach to its program activities because of the controversial nature of thetarget population. A 1996 memorandum of understandingrequired CIDA, the MOH, and WAPCAS to conduct annualmeetings to review progress and to plan subsequent year  ’ sactivities (which had to be approved by the MOH). Theseannual meetings were sustained throughout the project years.After the initial agreement, a social scientist wascontracted to study the operation of sex work in Ghana.The study identi 󿬁 ed 2 types of sex workers: home-based sexworkers and mobile sex workers. 19 The home-based sexworkers, called   “ seaters, ”  typically sit in front of their dwellings, waiting for clients. The mobile sex workers, called  “ roamers, ”  can be found along the streets, in bars, hotels, and  brothels. Seaters mostly live in urban and semi-urban settingswhere there is security and protection by the landlords and  “ queen mothers. ”  Seaters are typically older than roamers(with an average age of 35 years versus 24 years for roamers). 3 They usually have more clients per day (as manyas 20) and charge less per sexual act. 3,19 The WAPCASintervention was initiated among the seaters in Accra becausethey were more organized and easier to reach than roamers.Several HIV prevention strategies were eventuallydeployed, but clinical approaches (STI screening and treat-ment) were emphasized during the early years. WAPCAStried to ensure sustainability and access to services bysupporting the development of STI clinics within the MOHhealth facilities. The project began in 1996 with a single STIclinic in Accra. 18 In 1997, the Minister of Health recommended theexpansion of the program to other parts of the country. Bythe end of 2003, 15 clinics had been established nationwide,with priority given to locations with at least 50 seater sexworkers. The STI clinics were also open to the general population with the hope that this would reduce anystigmatization of the clinics or the clients. A wide varietyof clinical services were offered, including STI screening and case management based on a syndromic approach, thetreatment of minor ailments, HIV counseling, prophylaxisfor opportunistic infections (OIs), STI prevalence monitoring,and STI education. Several operational research studies werealso conducted to inform the design of the interventions. 20  –  22 Drugs for STIs were not readily available at govern-ment facilities at this time. WAPCAS initially procured STI drugs and later facilitated the inclusion of the STIdrugs into Ghana ’ s essential drug list. Tools were devel-oped to monitor STI treatment and to capture clinical datafrom the  󿬁 eld. Program monitoring tools were eventuallyadapted by the National AIDS Control Program and are currently used by Ghana ’ s Health Management Infor-mation System. 23 Outreach activities were a critical part of WAPCAS ’ swork. Community health nurses, and at a later stage, peer educators visited the seater and roamer communities, pro-moted the sale of condoms and lubricants, and provided information about STI-related and HIV-related issues. Theyalso mobilized sex workers for periodic medical checks.Between 1997 and 2003, more than 38,000 outreach visitswere made to seaters and roamers [18]. And nearly 4000seaters and more than 6700 roamers attended the clinics [18].During this period, more than 9000 FSWs were screened for STIs and nearly 11,000 STIs were diagnosed and treated (Fig. 1). Because HIV testing was a cumbersome process  —  rapid HIV test kits did not yet exist   —  HIV testing was not emphasized by the program. Among the 1352 FSWs tested,526 (41%) were seropositive for HIV. 23 WAPCAS sold condoms at a low cost rather thanoffering them for free to increase their desirability and toensure affordability. WAPCAS negotiated and acquired several brands of condoms on credit from various sources,including the Ghana Health Service Family Planning clinicsand the Ghana Social Marketing Foundation. Water-based lubricating gels and female condoms were also introduced for the  󿬁 rst time. Condom promotion and sales increased over theyears, and by the end of December 2003, more than 10million male and female condoms had been sold to sexworkers (Fig. 2). 24 In 2003, when nearly all of the seaters in Ghana had  been reached by the program, WAPCAS received anadditional year of support from USAID to intensify its focuson roamers in 4 of the 10 regions in Ghana. It was duringthis time that WAPCAS transitioned from the use of  public health nurses to the use of social of  󿬁 cers with backgrounds in the social sciences for the outreach activities.The project also greatly increased the number of peer educators who were used for this work. Nurses continued to provide clinical services to the sex workers at Ghana HealthService (GHS) facilities. 24 The second phase of HIV interventions is notable because it suggests that an intervention can be initiated and sustained within government structures (through the MOH),although the cultural and political milieu is very hostile whenthe program begins. The sharp reduction in gonorrhea and chlamydia among seaters in Accra and Kumasi between 1997and 2002 could also be a result of the WAPCAS project,which was at that time the only STI reduction initiative that focused on FSWs in Ghana.After 10 years (1996  –  2006) of   󿬁 nancial and technicalsupport to the WAPCAS FSW intervention, CIDA withdrewits funding rather suddenly and without a plan for sustain-ability. Before the closure of the project, WAPCAS had registered as a local organization and had secured   󿬁 nancialsupport from USAID, the Danish government (DANIDA),and much later, the Global Fund. Wondergem et al   J Acquir Immune Defic Syndr     Volume 68, Supplement 2, March 1, 2015 S140  | www.jaids.com  Copyright     2015 Wolters Kluwer Health, Inc. All rights reserved. Copyright © 201 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. 5  Third Phase: Scaling up and ImprovingQuality (2006 to 2013) Although surveillance data in the early 2000s indicated that the prevalence of HIV was higher among FSWs than it was in the general population, Ghana ’ s national HIV pre-vention program did not focus on this population. 25 A budget analysis as part of the Modes of Transmission study found that less than 2% of the annual HIV budget was allocated to prevention programs for FSWs or their clients. 12 The GAC,which was established in 2000 as a prerequisite for World Bank funding, prioritized interventions for the general population during its  󿬁 rst 10 years. 26  –  28 These interventionstargeted miners, truck drivers, formal-sector workplace pro-grams, school children, and teachers. At the same time,USAID ’ s funds were largely used for the social marketing of condoms for the general population, workplace programs, and the national  “ Love Life ”  HIV education campaign. 26,27,29 The National Strategic Framework for 2001 (NSF I) and for 2006(NSF II) had few references to FSWs, an indication of the low priority given to this population for HIV-related informationand services. 26,27 FSWs started to receive more attention in 2002, whena then-controversial study by WAPCAS revealed that sexwork was the primary driver of the HIV epidemic in Accra. 11 Based on this information, USAID Ghana issued its  󿬁 rst large-scale request for applications for HIV prevention amongFSWs, men who have sex with men (MSM), and peopleliving with HIV (PLHIV). 25 In 2004, the Strengthening HIV/AIDS Response Partner-ships (SHARP) project was awarded to the Academy for Educational Development (now FHI 360) with USAID funds.Between 2004 and 2009, with some delays, the project attempted to increase healthy behaviors and access to HIV services amongFSWs, their intimate partners, MSM, and PLHIV. The project marked an important shift in the delivery of HIV services toFSWs. It was the  󿬁 rst time that peer education techniques werescaled up as the mainstay of HIV prevention. SHARP was alsothe  󿬁 rst national outreach project that speci 󿬁 cally targeted roamers and the intimate partners of FSWs. 30 Under SHARP, the delivery of HIV services to FSWswas anchored by the brand,  “ I am someone ’ s hope. ”  The heart of the campaign promoted 10 key behaviors for HIV prevention, and it included a program called   “ Peer EducationPlus ”—  an effort to improve the consistency of peer messag-ing, peer educator skills, mentoring, and supervision. SHARPalso provided access to affordable condoms and lubricants,drop-in centers, referrals to testing and counseling services,and STI services  —  an agreed-on minimum package of services. 30 By the end of the project, SHARP and its 16implementing partners had reached more than 25,000 FSWs,nearly half of the estimated number of FSWs in Ghana. 3,30 At around this time, the national  “ ownership ”  of HIV prevention strategies for FSWs became more apparent. A Modesof Transmission study 12 and Academy for Educational Develop-ment  ’ s integrated biological and behavioral survey amongFSWs in 2006 and 2009 provided the evidence that was needed for Ghana ’ s AIDS Commission to include FSWs in the NationalStrategic Plan (2011 to 2015). 30  –  32 These events opened the door for the development of the national strategy for key populations,which was consisted of best practice approaches in HIV prevention, care, and treatment among FSWs and the formationof the national technical working group for key populations. 33 This would allow the largest HIV donor in country, The GlobalFund, to initiate funding for FSW interventions.In 2010, USAID awarded FHI 360 with the SHARPER (Strengthening HIV/AIDS Response Partnerships with FIGURE 1.  Prevalence of gonorrhea among female sex workers in Accra and Kumasi: 1998 to 2011.  J Acquir Immune Defic Syndr     Volume 68, Supplement 2, March 1, 2015  Female Sex Workers and HIV Prevention in Ghana  Copyright     2015 Wolters Kluwer Health, Inc. All rights reserved.  www.jaids.com  | S141 Copyright © 201 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. 5  Evidence-based Results) project. SHARPER built on themomentum of SHARP, but on a greater scale, reaching FSWsin all regions of Ghana. SHARPER expanded the essential package of services to FSWs by providing greater access tosafe spaces through discreet drop-in centers that offered sexual and reproductive health and basic health care support.It added anonymous counseling through telephone-based crisis counseling and weekly short message service (SMS)messages that reinforced the following 10 key behaviors: (1)use condoms consistently and correctly, (2) use non-oil  –   based lubricants properly, (3) get tested and know HIV status, (4)disclose HIV status to regular partners, (5) promptly seek appropriate and effective treatment for STIs, HIV, and OIs, (6)adhere to treatment [STI, OI, antiretroviral therapy (ART)], (7)reduce the number of multiple and concurrent sexual partners,(8) eat healthy, (9) protect against other infectious diseases suchas tuberculosis, malaria, and diarrhea, and (10) actively participate in program design and implementation. Linkageswith care were strengthened during this time with the aid of several interventions, including peer-led referrals, support from “ Models of Hope ”  (HIV-positive peer educators based in clinics)and PLHIV case managers, increased access to PLHIV support groups, and daily ART adherence reminders through the SMS “ LifeLine ”  service. The impact of these interventions onadherence and survival of those enrolled in ART is not known.In light of the impact of violence on the lives of FSWs  —   perpetrated by police, intimate partners, and clients  —  the SHARPER project adapted an emergency responsesystem from Avahan in India. 2,3 The network involves “ M-Friends ”  and   “ M-Watchers, ”  people in the communitywho address sexual and gender-based violence and rightsviolations against key HIV-affected populations. Individualsin positions of power who are  “ key population friendly ”  areidenti 󿬁 ed and trained as M-Friends. They include lawyers,human rights advocates, police, and members of the localgovernment and health care workers. M-Watchers are leading peer educators (FSWs or MSM) who identify and report abuses (within 2 hours of being noti 󿬁 ed) to the local USAID-implementing partner. Networks have been established in all10 regions of Ghana, with 350 M-Friends and M-Watchersdeployed within their communities. 34,35 Given the level of institutionalized police violence against FSWs, SHARPER,and other USAID partners secured an agreement to train police. A unique aspect of the training involves a mandatory preservice education and testing of recruits as part of their certi 󿬁 cation process.In 2010, the Global Fund provided   󿬁 nancial support toGAC and the Adventist Development and Relief Agency to provide comprehensive HIV prevention services to FSWs inlocations where no interventions were in place. A 2011integrated behavioral and biological surveillance study amongFSWs measured an HIV prevalence of 11.1%. 3 Figure 3depicts the decline in HIV prevalence among seaters and roamers in Accra and Kumasi between 1998 and 2011.The third phase of interventions saw a number of measurable successes. In 2011, 72.2% of the roamers in Accra FIGURE 2.  Condoms sales to female sex workers by sex worker projects in Ghana: 1997 to 2012. Wondergem et al   J Acquir Immune Defic Syndr     Volume 68, Supplement 2, March 1, 2015 S142  | www.jaids.com  Copyright     2015 Wolters Kluwer Health, Inc. All rights reserved. Copyright © 201 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited. 5
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