More than three decades after the first reported case of AIDS, sub-Saharan Africa continues to be the most heavily affected region in the world. East and southern Africa alone account for 56% of the global burden of HIV with eight countries having estimates of more than 1,000,000 persons living with HIV/AIDS . HIV prevalence in west Africa remains comparatively low, with the adult prevalence in the general population assessed at 2% or lower except for Côte d’Ivoire and Nigeria where adult prevalence is estimated at 3.4 and 3.5%, respectively . West Africa includes 14 countries, 3 landlocked and 11 with a coastline (Fig. 1), with the majority purporting French as their national language. The epidemic in west Africa is deemed to be heterosexually driven, but recent data suggest that sex between men may play a significant role in the spread of HIV infection [2,3]. Data from Senegal, The Gambia, Côte d’Ivoire, Ghana and Nigeria indicate that a substantial number of infections occur [4–7] among men who have sex with men (MSM), many of whom also report having sex with women .
The Joint United Nations Programme on HIV/AIDS defines epidemics as concentrated, low level, generalized and hyper endemic . The characterization of concentrated epidemics has been based on a threshold of HIV prevalence less than 1% in the general population and more than 5% in key populations – subpopulations at higher risk of HIV, such as female sex workers (FSW), MSM and persons who inject drugs (PWID). However, recent literature has examined transmission dynamics to document if HIV infection in the general population is self-sustaining or dependent on transmission from key populations [10▪,11]. Surveillance data indicate that west African countries have experienced concentrated HIV epidemics with elevated HIV prevalence among FSW and MSM [10▪]. Limited data are available for PWID in west Africa  and the role of injecting drugs in HIV transmission dynamics is unknown. Yet, reported drug use in this region has predominantly been noninjecting . Several studies document the disproportionate high rates of HIV among key populations in low-income countries [14▪,15▪▪,16]. However, national responses to the HIV/AIDS epidemic in most west African countries have historically focused on the general population, with little attention being paid to key populations. Key populations have rarely been part of surveillance activities in west Africa, resulting in important data gaps necessary to inform a broader public health response.
For this review, we included journal articles published during 2009–2014. During this period, some published articles report on studies and/or data collected over the past 15 years. We conducted a systematic search of publications using EMBASE and PubMed that either reported HIV seroprevalence data among key populations or included discussions on seroprevalence among key populations or MSM, FSW and PWID.
In this review, we will describe the HIV epidemic in FSW and MSM in west Africa and discuss challenges to expanding HIV prevention programs to key populations in the region.
Female sex workers
FSW and their clients are a critical group contributing to the spread of HIV infection worldwide . In west Africa, FSW carry a significant burden of HIV disease and are identified as a high-prevalence and incidence core group [18,19]. In selected cities in Ghana, Benin and Togo, 32–84% of prevalent cases among men had been attributed to sexual contact with FSW [1,18,20]. The percentage of HIV in the general women population that can be attributed to female sex work is estimated at 18% . A meta-analysis of FSW studies in low to middle-income countries indicated that FSW in sub-Saharan Africa had 12.4 times the odds of HIV compared with all women of reproductive age [15▪▪]. HIV prevalence in FSW varies within and across west African settings, with reported estimates over the past 5 years of 15.9% in The Gambia , 20% in Nigeria , 20.1% in Senegal , 25.7% in Bobo-Dioulasso, Burkina Faso , 26.6% in Côte d’Ivoire , 30.4% in Cotonou, Benin , 45.4% in Lome, Togo  and up to 68.6% in a study in Ghana and Benin  (Table 1). Although data are scarce for male and transgender sex workers, a study conducted among male sex workers in Côte d’Ivoire identified an HIV prevalence of 50% .
Although these estimates among FSW and male sex workers are relatively high, it is important to interpret them cautiously as these studies were largely conducted in urban areas, and were not nationally representative. Furthermore, population size estimations for key populations are available only for four (Sierra Leone, Côte d’Ivoire, Ghana and Nigeria) out of the 14 west African countries [28–30], which provides limited ability to effectively gauge the contribution of key populations to the HIV epidemic in the region. Trends recently reported from Benin, Côte d’Ivoire, Guinea and Nigeria show a temporal decline in HIV prevalence estimates among FSW [1,23,25,27].
The risk of HIV acquisition and/or transmission is usually determined by a combination of behavioral, biological and structural factors, such as the frequency of unprotected sexual intercourse, a high number of concurrent sexual partners, the presence of other sexually transmitted infections (STIs), limited access to prevention and treatment services, social stigma and discriminatory legal or regulatory policies [15▪▪]. In most studies on FSW, unprotected sexual intercourse was frequent with clients, with reported rates as high as 62% in Sierra Leone [31,32]. Similar rates of unprotected sex have been reported by FSW elsewhere with regular sexual partners . However, in two consecutive studies conducted in Nigeria, self-reported condom use among FSW was high with clients who pay for sex, ranging from 76.3 to 90.5%, but under 45% with regular, nonpaying sexual partners [23,33]. Unfortunately, there are no available data across the region to assess whether duration of sex work or early onset of sex work is associated with risk of infection.
STIs, especially genital ulcers, may play an important role in HIV transmission and acquisition [34–36]. FSW studies from Côte d’Ivoire, Ghana, Benin and Nigeria documented an elevated prevalence of curable bacterial STIs, denoting a higher risk for HIV infection among these FSW [17,18,26]. Structural factors that elevate risk among FSW include extreme poverty, concomitant lack of familial and social support, gender inequality, stigma, discrimination, physical and sexual violence and legal and regulatory policies penalizing sex work [15▪▪,37]. Sex work is illegal in most west African countries and FSW are criminalized, when arrested. Structural risk factors associated with arrest and incarceration indirectly heighten risk for HIV infection by restricting access to preventive HIV/ STIs care and treatment services . Although some localized education and prevention interventions have been launched for FSW in west Africa, they lack the scale to reach most FSW [10▪].
Men who have sex with men
Since the beginning of the epidemic, MSM have been disproportionately affected by HIV . Although the annual number of new HIV infections among all adults in sub-Saharan Africa has declined by 34% since 2001 , emerging data suggest that the situation among African MSM may mirror higher risk profiles documented among MSM elsewhere in the world [14▪]. Recent studies in Africa also indicate that MSM risk is higher than the general population . In Nigeria, consecutive assessments conducted in 2007 and 2010 among MSM documented an increase in HIV prevalence from 13.5 to 17.2% . Elsewhere in the region, HIV prevalence among MSM varies, with reported estimates over the past 3 years of 9.8% in Banjul, The Gambia , 18.0% in Abidjan, Côte d’Ivoire , 34.3% in Accra-Tema in Ghana , 34.9% in Abuja, Nigeria  and up to 50.0% among MSM engaging in sex work in Abidjan, Côte d’Ivoire  (Table 2).
As with FSW, risk factors for MSM bring in several contextual elements, such as illegality of same-sex behavior and poor quality service access that intensify individual-level risk . Individual risks include unprotected anal intercourse, high numbers of sexual partners and the presence of other STIs. Unprotected anal intercourse at last sex was reported by 43.4% of MSM enrolled in a cross-sectional survey conducted in three cities in Nigeria and by 57% of MSM in a study conducted in Douala, Cameroon [44,45], underscoring the high levels of risky behavior among these men. At the sexual network level, studies from Senegal and Nigeria have documented a substantial percentage of MSM who report having both male and female concurrent sex partners [8,46]. Bisexual concurrency may establish a bridge between male and female sexual networks and have implications for HIV transmission in the general population [47,48]. Furthermore, in some contexts, 25–50% of MSM engage in sex work based on recent studies in Nigeria, Côte d’Ivoire and Senegal [4,5,7,44,49], which may increase their vulnerability to HIV infection. The presence of bacterial STIs constitutes biological factors that may exacerbate risk of HIV infection and transmission . Studies of MSM in Côte d’Ivoire and Senegal documented a high prevalence of bacterial STIs [7,51]. Lastly, other important factors associated with higher risk sexual practices, such as excessive use of alcohol, injecting and noninjecting drugs (e.g., amphetamine-type stimulants) stigma, discrimination and human rights abuses have yet to be examined.
Although some estimates of risk factors for HIV infection are available for west African MSM, important data gaps remain. Donor-supported and national HIV surveillance and prevention activities are focused on the general heterosexual population; MSM prevalence data are not available for Liberia, Sierra Leone, Niger, Burkina Faso and Mali. Data on trends in HIV prevalence and incidence are even scarcer in the region. To fill these gaps, the President's Emergency Plan for AIDS Relief has over the past 5 years funded a plan to conduct a series of behavioral surveys, with biomarkers using respondent-driven sampling to assess HIV prevalence, risk behaviors and MSM population size estimates in Nigeria, Côte d’Ivoire, Ghana and Mali. The intent of these surveys is to create an evidence base on which HIV prevention programs may be developed for MSM in west Africa – a population that has historically been overlooked by HIV prevention programs. The majority of MSM in resource-limited countries has yet to be reached by prevention services . The Global Forum on MSM and HIV estimates the scale-up and delivery of basic strategies and interventions proven to reduce HIV transmission remains poor for MSM, particularly outside of high-income countries .
HIV PREVENTION CHALLENGES FOR KEY POPULATIONS IN WEST AFRICA
There is ample evidence that targeted HIV prevention programs aimed at reducing transmission of HIV and STIs are feasible and effective among FSW [21,54–56] and to a lesser extent among MSM [57,58]. However, major challenges hamper the delivery of effective prevention programs in these populations in west Africa. These challenges are linked to sociocultural, legal, political and economic issues and are often exacerbated by limited programmatic capacity and infrastructure within the public healthcare system.
Defining sex workers is difficult, as FSW often have multiple types of employment, are highly mobile and are often compelled to seek anonymity because of stigma. A qualitative study among FSW in Ghana concluded that stigma may deter FSW from getting tested, undermine condom use and prevent those who are HIV-positive from seeking treatment . Understanding motivations and barriers for seeking healthcare among those women could help inform interventions to reduce HIV transmission and its associated morbidity and mortality . Many MSM choose to remain closeted or to enter into sexual relationships or marriages with women because of sociocultural gender norms and a fear of stigmatization and discrimination. Adebajo et al. found a statistically significant association between internalized homophobia and HIV infection among MSM reporting bisexual practices in Nigeria, emphasizing the misconceptions of risk that often lead to riskier sexual practices . In general, unlike their peers from other countries, key populations in west Africa are not uniformly organized into peer-led or lesbian, gay, bisexual and transgender organizations . Consequently, key populations are unable to serve as social capital to assist and/or provide interventions to their peers. Several nascent lesbian, gay, bisexual and transgender groups or organizations in the region, such as the International Centre on Advocacy for the Right to health in Nigeria, the Center for Popular Education and Human Rights in Ghana or Alternative in Côte d’Ivoire, would benefit from greater regional and international support.
Legal and human rights challenges
Sex work is illegal in most west African countries with numerous punitive legal approaches but is unevenly enforced. Senegal is the lone exception, where prostitution has been legal and regulated since 1969 [61,62]. However, there is increasing evidence that many FSW in Senegal are no longer willing to be registered, and a significant number may be working outside legal sanction . Likewise, MSM are highly stigmatized as same-sex intercourse is criminalized across west Africa and may be punishable by lengthy prison terms or death [16,30,63]. A recent Nigerian law mandates a 14-year prison sentence for anyone entering a same-sex union and a 10-year term for ‘a person or group of persons who supports the registration, operation and sustenance of gay clubs, societies, organizations, processions or meetings’ . A rapid assessment conducted by Poteat et al. in Senegal concluded that enforcing laws criminalizing same-sex practices may significantly decrease uptake of HIV services among MSM. Furthermore, the assessment found that law enforcement officers often ignore or participate in antigay violence . In some countries, healthcare providers are pressured by governmental authorities to disclose the identities of their MSM clients, rendering this political environment a deterrent for seeking care and/or treatment services .
Despite the emerging evidence indicating a heavy HIV burden among key populations, the public health response in most west African countries is influenced by a moral debate. Largely because of political pressure, current HIV prevention and care policies do not call for an urgent scale-up of comprehensive initiatives among key populations . In most countries, government is reticent to engage with key populations stakeholders and to help expand and sustain successful programs even when programs are successfully jump-started by externally funded nongovernmental or community-based organizations. In recent years, a social justice movement has emerged in Africa  with strong advocacy by regional networks, such as the African Men for Sexual Health and Rights and substantive engagement by civil society to promote human rights of sexual minorities. The emergence of groups such as, African Men for Sexual Health and Rights, has helped mobilize or strengthen political will to offer services to key populations. But on several occasions public advocacy on behalf of MSM issues has contributed to a backlash or reenforcement of negative measures, namely in Senegal, Ghana and Core d’Ivoire . Nevertheless, FSW and MSM have been recognized as an HIV prevention priority in Nigeria, Ghana and Côte d’Ivoire's 5-year national strategic plans.
Over the last decade, several FSW interventions were implemented as part of epidemiologic research or demonstration projects in Burkina Faso, Togo, Benin and Nigeria [24,65], but were not designed to be sustainable projects. Other interventions, such as Project PAPO in Côte d’Ivoire, were initiated through President's Emergency Plan for AIDS Relief with country-based partners and gradually scaled up to successfully provide comprehensive services to FSW and MSM . However, these interventions remain dependent on external donor funding and have yet to transition into complete country-owned programs, either through a ministry of health or a sustainably funded civil society partner. Similarly, multicountry initiatives to promote HIV prevention strategies among FSW have been sponsored by development agencies and successfully rolled out in major west African cities over the last 10 years. These projects were specifically targeting FSW with a comprehensive package of services [10▪], but funding gaps resulted in extended interruptions of services in some countries . Inadequate financing for HIV prevention programming for key populations remains a primary reason why low coverage of HIV prevention services for key populations persists in west Africa [10▪].
In west Africa key populations engage in high-risk practices and live in a sociopolitical environment that increases vulnerability for HIV acquisition and transmission. Although the effectiveness of targeted HIV prevention interventions among FSW has been well recognized , fewer evidence-based achievements were noted among MSM globally . The challenge for implementing HIV/AIDS awareness education and prevention interventions in resource-limited countries is not a lack of ‘know how’, but rather an amalgamation of factors and barriers that include cultural and social norms, legal and human rights issues and economic commitment. Most west African countries have yet to engage key stakeholders, including government and political leaders, to define suitable key populations-friendly policies and to mobilize adequate technical and financial support for strong and viable key populations programmes, including service delivery. Services that address HIV prevention strategies, such as peer-led interventions, condom and condom-compatible lubricant promotion and use, STIs screening and treatment services, HIV testing and counseling and HIV care, treatment and support, have a better chance to impact transmission rates significantly, if delivered together. Sufficient resources combined with planning, political will and reforms to legal and structural frameworks will all be required to overcome the substantial social, political, economic, legal and psychosocial barriers that key populations face in west Africa. This review suggests that emerging evidence exists to justify concerns about the bridging role key populations may play in fueling the epidemic in the general population in west Africa and the need to mobilize new investments for HIV and other STIs prevention care and treatment programs for key populations throughout the region.
Disclaimer: The findings and conclusions in this article are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.
Conflicts of interest
There are no conflicts of interest.
REFERENCES AND RECOMMENDED READING
Papers of particular interest, published within the annual period of review, have been highlighted as:
- ▪ of special interest
- ▪▪ of outstanding interest
2. Samuelsen H, Norgaard O, Ostergaard LR. Social and cultural aspects of HIV and AIDS in West Africa
: a narrative review of qualitative research. SAHARA J 2012; 9:64–73.
3. De Cock KM, Jaffe HW, Curran JW. The evolving epidemiology of HIV/AIDS. AIDS 2012; 26:1205–1213.
4. Merrigan M, Azeez A, Afolabi B, et al. HIV prevalence and risk behaviours among men having sex with men in Nigeria. Sex Transm Infect 2011; 87:65–70.
5. Vu L, Adebajo S, Tun W, et al. High HIV prevalence among men who have sex with men in Nigeria: implications for combination prevention. J Acquir Immune Defic Syndr 2013; 63:221–227.
6. Mason K, Ketende S, Peitzmeier S, et al. A cross-sectional analysis of population demographics, HIV knowledge and risk behaviors, and prevalence and associations of HIV among men who have sex with men in The Gambia. AIDS Res Hum Retroviruses 2013; 29:1547–1552.
7. Vuylsteke B, Semde G, Sika L, et al. High prevalence of HIV and sexually transmitted infections among male sex workers in Abidjan, Côte d’Ivoire: need for services tailored to their needs. Sex Transm Infect 2012; 88:288–293.
8. Sheehy M, Tun W, Vu L, et al. High levels of bisexual behavior and factors associated with bisexual behavior among men having sex with men (MSM) in Nigeria. AIDS Care 2013; 26:116–122.
9. Joint United Nations Programme on HIV/AIDS (UNAIDS). Combination prevention: addressing the urgent need to reinvigorate HIV prevention responses globally by scaling up and achieving synergies to halt and begin to reverse the spread of AIDS epidemic. In: 30th Meeting of the UNAIDS coordinating board; 5–7 June 2012; Geneva, Switzerland.
10▪. Alary M, Lowndes CM, Van de Perre P, et al. Scale-up of combination prevention and antiretroviral therapy for female sex workers in West Africa
: time for action. AIDS 2013; 27:1369L 1374.
Review of prevention care and treatment interventions for sex workers over the past 10 years. The study indicates that a few interventions were initiated but were not designed to be sustainable and were dependent on external donor rather than country-owned programs. With an epidemic largely driven by at-risk populations in west Africa, it is essential to renew the interest in combination prevention strategies and expanded treatment services.
11. Drame FM, Peitzmeier S, Lopes M, et al. Gay men and other men who have sex with men in West Africa
: evidence from the field. Cult Health Sex 2013; 15 (Suppl 15):7–21.
12. Eluwa GI, Strathdee SA, Adebayo SB, et al. A profile on HIV prevalence and risk behaviors among injecting drug users in Nigeria: should we be alarmed? Drug Alcohol Depend 2013; 127:65–71.
14▪. Beyrer C, Baral SD, van Griensven F, et al. Global epidemiology of HIV infection in men who have sex with men. Lancet 2012; 380:367–377.
This is a comprehensive review of available data for HIV prevalence, incidence, risk factors and the molecular epidemiology of HIV in MSM from 2007 to 2011 with a modelling of transmission dynamics. There is a disproportionate disease burden among MSM worldwide. Prevention strategies that lower biological transmission and acquisition risks, such as antiretroviral therapy, offer promise for controlling the expanding epidemic in MSM, but potential effectiveness is limited by structural factors that contribute to low health-seeking behaviors in population of MSM in many parts of the world.
15▪▪. Baral S, Beyrer C, Muessig K, et al. Burden of HIV among female sex workers in low-income and middle-income countries: a systematic review and meta-analysis. Lancet Infect Dis 2012; 12:538–549.
Comprehensive review of 102 studies of 99 878 female sex workers in 50 low-income and middle-income countries published between 1 January 2007 and 25 June 2011. HIV risk data among female sex workers are scarce, but the burden of disease is disproportionately high. The data suggest an urgent need to scale-up access to quality HIV prevention programs. Considerations of the legal and policy environments in which sex workers operate and actions to address the important role of stigma, discrimination, and violence targeting female sex workers are needed.
16. Millett GA, Jeffries WL4th, Peterson JL, et al. Common roots: a contextual review of HIV epidemics in black men who have sex with men across the African diaspora. Lancet 2012; 380:411–423.
17. Vuylsteke B, Semde G, Sika L, et al. HIV and STI prevalence among female sex workers in Côte d’Ivoire: why targeted prevention programs should be continued and strengthened. PLoS One 2012; 7:e32627.
18. Labbe AC, Pepin J, Khonde N, et al. Periodical antibiotic treatment for the control of gonococcal and chlamydial infections among sex workers in Benin and Ghana: a cluster-randomized placebo-controlled trial. Sex Transm Dis 2012; 39:253–259.
19. Forbi JC, Entonu PE, Mwangi LO, Agwale SM. Estimates of human immunodeficiency virus incidence among female sex workers in north central Nigeria: implications for HIV clinical trials. Trans R Soc Trop Med Hyg 2011; 105:655–660.
20. Sobela F, Pepin J, Gbeleou S, et al. A tale of two countries: HIV among core groups in Togo. J Acquir Immune Defic Syndr 2009; 51:216–223.
21. Kane CT, Diawara S, Ndiaye HD, et al. Concentrated and linked epidemics of both HSV-2 and HIV-1/HIV-2 infections in Senegal: public health impacts of the spread of HIV. Int J STD AIDS 2009; 20:793–796.
22. Peitzmeier S, Mason K, Ceesay N, et al. A cross-sectional evaluation of the prevalence and associations of HIV among female sex workers in The Gambia. Int J STD AIDS 2013; 25:244–252.
23. Eluwa GI, Strathdee SA, Adebajo SB, et al. Sexual risk behaviors and HIV among female sex workers in Nigeria. J Acquir Immune Defic Syndr 2012; 61:507–514.
24. Konate I, Traore L, Ouedraogo A, 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.
25. Behanzin L, Diabate S, Minani I, 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; 63:126–134.
26. Ahoyo AB, Alary M, Ndour M, et al. HIV and sexually transmitted disease among female sex workers in Benin. Med Trop (Mars) 2009; 69:457–462.
27. Diallo BL, Alary M, Barry A, Rashed S. HIV epidemic among female sex workers in Guinea: prevalence, associated risk factors, vulnerability and trend from 2001 to 2007. Rev Epidemiol Sante Publique 2010; 58:245–254.
28. Ministere de la Sante et de la lutte contre le VIH/SIDA CdI. Etude sur le VIH et les facteurs de risque associes chez les hommes ayant des rapport sexuels avec des hommes a Abidjan, Côte d’Ivoire. 2012. [Ministry of Health and HIV/AIDS control. Survey on HIV-associated risk factors among men who have sex with men in Abidjan, Cô te d’Ivoire 2012]
29. Ghana AIDS Commission. HIV prevalence and correlates of infection among MSM: 4 areas in Ghana, the Ghana Men's Health Study, 2010–2011. http://www.avac.org/ht/display/ContentDetails/i/49517
. [Accessed 19 March 2014]
30. National HIV and AIDS Secretariat SL: population size estimation of key populations. 2013; Sierra Leone: 2013: Vol. 2014.
31. Larsen MM, Sartie MT, Musa T, et al. Changes in HIV/AIDS/STI knowledge, attitudes and practices among commercial sex workers and military forces in Port Loko, Sierra Leone. Disasters 2004; 28:239–254.
32. Aho J, Koushik A, Diakite SL, et al. Biological validation of self-reported condom use among sex workers in Guinea. AIDS Behav 2010; 14:1287–1293.
33. Federal Ministry of Health Nigeria. Nigeria integrated biological and behavioural surveillance survey 2010; 2010.
34. Celum C, Wald A, Hughes J, et al. HPTN 039 Protocol TeamEffect of aciclovir on HIV-1 acquisition in herpes simplex virus 2 seropositive women and men who have sex with men: a randomised, double-blind, placebo-controlled trial. Lancet 2008; 371:2109–2119.
35. Barnabas RV, Celum C. Infectious co-factors in HIV-1 transmission herpes simplex virus type-2 and HIV-1: new insights and interventions. Curr HIV Res 2012; 10:228–237.
36. Barnabas RV, Webb EL, Weiss HA, Wasserheit JN. The role of coinfections in HIV epidemic trajectory and positive prevention: a systematic review and meta-analysis. AIDS 2011; 25:1559–1573.
37. Ngugi EN, Roth E, Mastin T, et al. Female sex workers in Africa: epidemiology overview, data gaps, ways forward. SAHARA J 2012; 9:148–153.
38. Beyrer C, Sullivan P, Sanchez J, et al. The global HIV epidemics in MSM: time to act. AIDS 2013; 27:2665–2678.
39. SHARM study group, Hakim Avi, Aho J, Semde G, et al. HIV prevalence and associated risk factors among MSM: a respondent-driven sampling survey, Abidjan, Côte d’Ivoire. 20th Conference on Retroviruses and Opportunistic Infections; 2013; Atlanta, GA: 2013.
40. Aberle-Grasse J, McFarland W, El-Adas A. HIV prevalence and correlates of infection among MSM: 4 areas in Ghana, the Ghana Men's Health Study, 2010–2011. 20th Conference on Retroviruses and Opportunistic Infections; 3–6 March 2013 Atlanta, GA: 2013.
41. CB United Nations. The official United Nations Site for MDG indicators. Millenium Development GOAL Indicators; 2013; http://unstats.un.org/unsd/mdg/SeriesDetail.aspx?srid=747&crid=
42. Wade AS, Larmarange J, Diop AK, et al. Reduction in risk-taking behaviors among MSM in Senegal between 2004 and 2007 and prevalence of HIV and other STIs. ELIHoS Project, ANRS 12139. AIDS Care 2010; 22:409–414.
43. 2011; Poteat T, Diouf D, Drame FM, et al. HIV risk among MSM in Senegal: a qualitative rapid assessment of the impact of enforcing laws that criminalize same sex practicesJT PLoS One. 6:e28760.
44. Vu L, Andrinopoulos K, Tun W, Adebajo S. High levels of unprotected anal intercourse and never testing for HIV among men who have sex with men in Nigeria: evidence from a cross-sectional survey for the need for innovative approaches to HIV prevention. Sex Transm Infect 2013; 89:659–665.
45. Henry E, Marcellin F, Yomb Y, et al. Factors associated with unprotected anal intercourse among men who have sex with men in Douala, Cameroon. Sex Transm Infect 2010; 86:136–140.
46. Larmarange J, Wade AS, Diop AK, et al. ELIHoS GroupMen who have sex with men (MSM) and factors associated with not using a condom at last sexual intercourse with a man and with a woman in Senegal. PLoS One 2010; 5:e13189.
47. Smith AD, Tapsoba P, Peshu N, et al. Men who have sex with men and HIV/AIDS in sub-Saharan Africa. Lancet 2009; 374:416–422.
48. Beyrer C, Trapence G, Motimedi F, et al. Bisexual concurrency, bisexual partnerships, and HIV among Southern African men who have sex with men. Sex Transm Infect 2010; 86:323–327.
49. Ndiaye P, Fall A, Tal-Dia A, et al. Knowledge, attitudes and practices related to STD and HIV/AIDS: men having sex with men in Senegal. Rev Epidemiol Sante Publique 2011; 59:305–311.
50. Celum CL. Sexually transmitted infections and HIV: epidemiology and interventions. Top HIV Med 2010; 18:138–142.
51. Wade AS, Kane CT, Diallo PA, et al. HIV infection and sexually transmitted infections among men who have sex with men in Senegal. AIDS 2005; 19:2133–2140.
52. Beyrer C. Global prevention of HIV infection for neglected populations: men who have sex with men. Clin Infect Dis 2010; 50 (Suppl 3):S108–113.
53. The Global Forum on MSM and HIV (MSMGF). Access to HIV prevention services and attitudes about emerging strategies: a global survey of men who have sex with men (MSM) and their healthcare providers; 2011.
54. Steen R, Vuylsteke B, DeCoito T, et al. Evidence of declining STD prevalence in a South African mining community following a core-group intervention. Sex Transm Dis 2000; 27:1–8.
55. Ghys PD, Diallo MO, Ettiegne-Traore V, et al. Increase in condom use and decline in HIV and sexually transmitted diseases among female sex workers in Abidjan Côte d’Ivoire. AIDS 2002; 16:251–258.
56. World Health Organization (WHO). Prevention and treatment of HIV and other sexually transmitted infections for sex workers in low-and middle-income countries: recommendations for a public health approach; 2012.
57. Baral SD, Wirtz A, Sifakis F, et al. The highest attainable standard of evidence (HASTE) for HIV/AIDS interventions: toward a public health approach to defining evidence. Public Health Rep 2012; 127:572–584.
58. Lorimer K, Kidd L, Lawrence M, et al. Systematic review of reviews of behavioural HIV prevention interventions among men who have sex with men. AIDS Care 2013; 25:133–150.
59. Rosenheck R, Ngilangwa D, Manongi R, Kapiga S. Treatment-seeking behavior for sexually transmitted infections in a high-risk population. AIDS Care 2010; 22:1350–1358.
60. Nigeria FGo. Same sex marriage prohibition act, 2013. Edited by Assembly N; 2013.
61. Meda N, Ndoye I, M’Boup S, 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.
62. Laurent C, Seck K, Coumba N, et al. Prevalence of HIV and other sexually transmitted infections, and risk behaviours in unregistered sex workers in Dakar, Senegal. AIDS 2003; 17:1811–1816.
63. Beyrer C. Hidden yet happening: the epidemics of sexually transmitted infections and HIV among men who have sex with men in developing countries. Sex Transm Infect 2008; 84:410–412.
64. Beyrer C. LGBT Africa: a social justice movement emerges in the era of HIV. SAHARA J 2012; 9:177–179.
65. Huet C, Ouedraogo A, Konate I, 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.
66. Semini I, Batona G, Lafrance C, et al. Implementing for results: program analysis of the HIV/STI interventions for sex workers in Benin. AIDS Care 2013; 25 (Suppl 1):S30–39.