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AIDS:
doi: 10.1097/01.aids.0000432449.30239.fe
Editorial Review

The increase in global HIV epidemics in MSM

Beyrer, Chrisa; Sullivan, Patrickb; Sanchez, Jorgec; Baral, Stefan D.a; Collins, Chrisd; Wirtz, Andrea L.a,e; Altman, Dennisf; Trapence, Giftg; Mayer, Kennethh

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Author Information

aCenter for Public Health and Human Rights, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland

bRollins School of Public Health, Emory University, Atlanta, Georgia, USA

cImpacta, Lima, Peru

damfAR, The Foundation for AIDS Research, Washington DC

eDepartment of Emergency Medicine, Johns Hopkins Medical Institute, Baltimore, Maryland, USA

fLaTrobe University, Melbourne, Australia

gCenter for the Development and Education of People, Blantrye, Malawi

hFenway Community Health Center and Harvard University, Boston, Massachusetts, USA.

Correspondence to Chris Beyrer, MD, MPH, Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, 615 North Wolfe Street, E 7152, Baltimore, MD 21205, USA. Tel: +1 410 614 5247; fax: +1 410 614 8371; e-mail: cbeyrer@jhsph.edu

Received 6 May, 2013

Revised 30 May, 2013

Accepted 11 June, 2013

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Abstract

Epidemics of HIV in MSM continue to expand in most low, middle, and upper income countries in 2013 and rates of new infection have been consistently high among young MSM. Current prevention and treatment strategies are insufficient for this next wave of HIV spread. We conducted a series of comprehensive reviews of HIV prevalence and incidence, risks for HIV, prevention and care, stigma and discrimination, and policy and advocacy options. The high per act transmission probability of receptive anal intercourse, sex role versatility among MSM, network level effects, and social and structural determinants play central roles in disproportionate disease burdens. HIV can be transmitted through large MSM networks at great speed. Molecular epidemiologic data show marked clustering of HIV in MSM networks, and high proportions of infections due to transmission from recent infections. Prevention strategies that lower biological risks, including those using antiretrovirals, offer promise for epidemic control, but are limited by structural factors including, discrimination, criminalization, and barriers to healthcare. Subepidemics, including among racial and ethnic minority MSM in the United States and UK, are particularly severe and will require culturally tailored efforts. For the promise of new and combined bio-behavioral interventions to be realized, clinically competent healthcare is necessary and community leadership, engagement, and empowerment are likely to be key. Addressing the expanding epidemics of HIV in MSM will require continued research, increased resources, political will, policy change, structural reform, community engagement, and strategic planning and programming, but it can and must be done.
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Introduction

The global epidemiology of HIV-1 is changing in 2013 [1]. Encouraging declines in new infections in many high burden countries in sub-Saharan Africa, declining trends in AIDS morbidity and mortality, and advances in treatment access and prevention science, have led to a new optimism that control of the HIV pandemic may be an achievable goal [2]. But the available data on HIV prevalence and incidence, from low, middle, and high income countries suggest that the HIV epidemics among gay, bisexual, and other MSM are on markedly different, and expanding, trajectories [3,4]. In many high income country settings, HIV epidemics have expanded among MSM in the HAART era – and where access to HIV prevention, treatment, and care services is widespread, including in the United States, the UK, France, Australia, and the Netherlands [5,6]. In many low and middle income countries, MSM have many fewer resources, and may be much more hidden and stigmatized, compounding risks for HIV acquisition and transmission [7,8] and limiting access to the most basic of services, including condoms and lubricants [3]. Subepidemics of HIV in particularly marginalized subgroups of MSM, most notably among black MSM in the United States and UK, are particularly severe and underscore the complex challenges addressing HIV among stigmatized men will require [9,10]. Although much of the work on HIV acquisition and transmission between men has focused on individual level risks for HIV infection, these have been shown to be insufficient to explain the divergence of MSM epidemics from those in other populations. How then, can these consistent and disturbing trends for HIV among MSM be explained? And what prevention, treatment, policy, and program innovations might help address this ongoing component of global HIV/AIDS?

An international collaborative team conducted a series of comprehensive reviews of the global HIV epidemic for a special theme issue of The Lancet in 2012. A number of recent reports have added new incidence and prevalence data, geographic reach, and analytic insights, which suggest a new paradigm of HIV risk and protection is emerging which may help gay and other MSM, and their communities and providers, address what is tragically, the next wave of global HIV.

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Global burden of HIV in MSM

There has been a vigorous recent effort to measure HIV disease burdens among MSM globally, including in many settings in which, despite decades of HIV research and programs, no studies had been done with MSM. Recent first reports on HIV prevalence have come from Uganda [11], Cote d’Ivoire [12], Israel [13], and Taiwan [14]. Figure 1 shows the global burden of HIV among MSM by region. Very high prevalence burdens are found in the United States [15–19], the Caribbean [20], Peru [21–24], multiple African countries [11,12,25–29], Thailand [30], Burma (Myanmar) [31], and parts of China [32]. Data from China [33–38], Vietnam [39], Taiwan [14] published within the last year have moved regional HIV prevalence estimates in East Asia from 5.3%, reported by Beyrer et al. in 2012 [3], to 10.3% [95% confidence interval (CI) 10.1–10.5].

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HIV incidence data have been less available, but new reports from Kenya [28,40], Thailand [30], China [41,42], and among black MSM in several US cities show consistently high rates of new infection, with the highest rates among the youngest age groups [43]. Figure 2 shows available incidence data on MSM globally through 1 May 2013.

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Epidemic drivers and risks

Individual level risks for HIV infection, including numbers of sex partners, use of intoxicants during sex, self-reported condom use, rates of substance use, and others are informative but insufficient to explain HIV epidemics among networks of men, and to explain the marked disparities in subepidemics of MSM, wherein individual level risks may be modest, but cumulative acquisition probabilities high [9,10]. Findings from network level investigations and from the molecular epidemiology of HIV may be more informative of the differing dynamics of infection in these populations. Two biological factors are essential to understanding these dynamics. First, as Baggaley et al.[44] have reported, is the very high transmission efficiency of receptive anal intercourse – at an estimated 1.4% per act probability (95% CI 0.2–2.5%) and the very high per partner probability of 40.4% (95% CI 6.0–74.9), roughly 18-fold higher than for vaginal intercourse. These probabilities were derived from a meta-analysis that included available data on both heterosexual and male homosexual couples – the risk did not differ by gender of the receptive partner, but is a function of the high efficiency of HIV transmission across the rectal mucosa. Second, is the reality that unlike women in heterosexual networks, men can be both receptive (high risk for acquisition) and insertive (high risk for transmission) partners in anal sex with other men [3]. These two factors appear to explain, at least in part, the rapid and efficient spread of HIV through networks of MSM. The very high acquisition probability in receptive anal sex likely accounts for the lack of protection with circumcision seen in MSM.

Recent insights from molecular epidemiology have helped elucidate aspects of these transmission dynamics at network and population levels (Table 1) [16,45–48]. Yebra et al.[45] using phylogenetic approaches explored networks in Madrid and found that MSM were more likely than other persons living with HIV to be in networks of transmissions, and that most of the networks identified were among MSM. Ambrosioni et al.[46] investigated newly diagnosed HIV infections in the Swiss national cohort and reported that recent HIV infections accounted for some two-thirds of transmission in MSM, and that MSM were significantly more likely than other persons to be in transmission clusters of other recent infections. Leigh Brown et al. [47], investigating epidemic dynamics among some 14 560 B clade infections in the UK, found that the median time of onward transmission was 17 months, and that in large clusters of MSM, some 20% of new HIV infections occurred within 6 months of index acquisition. They concluded that the high infectiousness of recent infection played a marked role in accelerating HIV transmission within MSM networks. Elegant work by Oster et al.[16] using traditional epidemiologic methods and phylogenetic data explored networks of transmission among MSM in Mississippi. They found very marked insularity in high HIV transmission networks among the youngest group of black MSM. HIV infections in black men aged 24 and under clustered in networks with no HIV infections in women, no IDU, few men of other races, and no men aged over 24 years, suggesting highly assortative spread of HIV within this network.

Table 1
Table 1
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Taken together, these insights suggest that HIV spread in networks of MSM is rapid, efficient, and is driven by high onward transmission probability among recently infected men. These findings would, at least partially, explain why HIV spread among young MSM might be increasing in settings in which the epidemic is otherwise in decline. The consistent finding of rapid spread among young MSM, who may be the least likely to be in care and on HAART, may also explain the limited impact of treatment as prevention (TasP) on these epidemics.

In most parts of the world, denial, persecution, and refusal to include MSM within prevention programs intersects with individual behaviors to place MSM at heightened risk of infection. Individual level biological and behavioral risks among these populations are likely contextualized by higher order risk factors including size and density of social and sexual networks, and stigma [26,49,50]. Stigma targeting MSM has been shown to limit both the provision and uptake of HIV services [50]. Stigma can also limit funding for targeted research and programs, and stigma within health provider networks can limit uptake of services. Stigma programs have tended to focus on people living with HIV/AIDS (PLWHA) [51–55], but there are consistent results of the outcomes of multiple forms of stigma affecting MSM. Research in Senegal demonstrated that stigma affected provision and uptake of HIV prevention, treatment, and care services in the context of ongoing arrests of MSM [56]. Studies of MSM clients have shown that stigma limits uptake of HIV services [26,49,50].

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Health disparities and black MSM

Many of the elements driving HIV epidemics among MSM globally are also responsible for HIV infection disparities among black MSM in the United States. Surveillance data show that HIV prevalence and incidence disproportionately affect black MSM compared to all other US populations [4,57]. Young black are particularly affected. New HIV infections among young black MSM increased by 48% between 2006 and 2009 [4] and mathematical models based upon HIV incidence estimates of young black MSM show that as many as 60% within a given cohort may be HIV-positive by age 40 [58].

A 2006 review provided the first comprehensive examination of factors that likely contribute to HIV infection disparities among black MSM [59]. A year later, a meta-analysis of 56 studies confirmed that despite greater HIV and sexually transmitted infection (STI) burden, black MSM across various studies, regions, and demographics reported comparable unprotected anal intercourse (UAI), fewer sex partners, less substance use, but greater undiagnosed HIV infection and less access to antiretroviral therapy (ART) [60]. A more recent meta-analysis of 176 US studies affirmed the results of the first meta-analysis and also found that black MSM have a 40% greater odds than other MSM of engaging in any behavior protective of HIV transmission [9]. Scientific opinion explaining disproportionate HIV infection among black MSM has converged on the following explanations.

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Differences in clinical outcomes

Although HIV diagnosis and treatment have enormous potential to curb HIV transmission opportunities at the interpersonal [61] and population [62] levels, black MSM are least likely to be diagnosed with HIV or to be in care compared with other MSM [9,60]. In fact, a recent meta-analysis of studies of HIV-positive MSM found evidence of major disparities in clinical outcomes at each stage of the treatment cascade (Fig. 3). Black MSM were more likely than other MSM to have undiagnosed HIV infection and to be diagnosed with HIV, yet less likely to access ART, to begin ART at a non-AIDS-defining CD4+ cell count (>200 cells/μl), to adhere to ART, or to be virally suppressed [9]. Moreover, the analysis found that access to ART and viral suppression remains complicated for HIV-diagnosed black MSM because they are more likely than other MSM to have a low income, to be uninsured, or to attend clinical visits. A separate analysis of HIV surveillance data found that an additional 38 920 black MSM would need to be placed on treatment to raise viral suppression to a comparable level as white MSM [63], which may be difficult to achieve as some black MSM in high prevalence jurisdictions remain undiagnosed even when engaged in healthcare and informing their physicians about their homosexual behavior [64].

Fig. 3
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Differences in sexual networks/partner characteristics

An important analysis found that having older and black sex partners raised the probability of HIV infection among black MSM compared with other MSM [65]. Black MSM across US studies are 11 times more likely to have black partners compared with other MSM and 50% more likely to have older sex partners [9]. Because background prevalence of HIV is greater among both older and black MSM, and because black MSM are less likely to be virally suppressed than other MSM, various analyses show that the partner pool for black places them at risk for HIV infection despite less risk behavior than other MSM [9,16,66]. Thus, black MSM with only two UAI partners have as much as a 40% risk of HIV infection compared with a 20% risk for white MSM with the same number of partners [53]. Risk is further compounded by assortative sexual mixing beliefs. Black MSM who believe that ‘sex with a black man reduces HIV risk’ were more likely to have undiagnosed HIV infection than black MSM who did not subscribe to this belief [64].

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Differences in social and structural experiences

Meta-analyses show that black MSM are more likely than other MSM to have a low income, to be unemployed, to ever be incarcerated, or to have a low education. Each of these factors is associated with a greater likelihood of HIV infection [67–69], and they highlight the degree to which black MSM remain marginalized despite being at the epicenter of the US epidemic and, along with homophobia, help explain why few HIV prevention interventions [70,71] or HIV prevention resources [72] target black MSM compared to US populations at lower risk for HIV infection.

HIV-related disparities affect black MSM beyond the US borders. Black MSM in the UK are more likely to be HIV-positive despite comparable risk behaviors and less likely to access ART once diagnosed with HIV. Moreover, meta-analytic data show that black MSM across the Diaspora (Africa, Caribbean, Europe, North America) are at elevated risk for HIV compared with other MSM or black populations generally [9,10]. Given these similarities, the creation of effective HIV prevention and care interventions for black MSM in any of these regions may have implications for the health and well being of black MSM globally.

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Responses, prevention for MSM

A consideration of HIV prevention for MSM starts with an understanding of the epidemiology and biology of HIV epidemics among these men. Around the world, MSM epidemics continue to expand, even as co-located epidemics among heterosexuals stabilize or contract; this is likely driven by the high per-act HIV transmission risk for anal sex, sex role versatility, and network level factors as described in Table 1. Modeling studies reported in The Lancet MSM and HIV series illustrate that even high levels of behavioral change are insufficient to meaningfully curb growth in MSM epidemics, given the high biological force of infection [3], and that achieving sufficient coverage of prevention interventions – as high as 60–80% of eligible MSM – may be required to achieve impact in reducing HIV incidence [6]. Taken together, these observations support the conclusion that there may be a biologically ‘higher bar’ for HIV prevention for MSM, and that strategies to meet the prevention needs of MSM will need to address barriers to high coverage, such as stigma and lack of access to culturally competent care. For MSM, the packaging of comprehensive prevention services is not an attractive theoretical next step: it is an imperative.

A systematic review of HIV prevention interventions conducted in 2011–2012 revealed several key themes [6]. Dozens of theoretically based interventions to increase condom use and/or reduce sexual partner number have been developed and tested, mostly in the United States, and have demonstrated modest reductions in self-reported outcomes, but no effects on HIV incidence outcomes. More recently, interventions based on the provision of antiviral drugs to MSM – either before HIV infection, to prevent infection [73], or after HIV infection, to reduce risk of onward transmission [74] – have demonstrated efficacy against HIV. Other prevention tools, such as HIV vaccines and rectal microbicides [75], are in ongoing testing and development, and comprehensive prevention strategies for MSM should be constructed flexibly, with the hope and expectation that such technologies will eventually be available.

Combination HIV prevention for MSM must utilize a set of approaches that intervene at key vulnerable points in the HIV transmission cycle, that allow the provision of prevention services tailored to men's individual circumstances, and that allow broad uptake and coverage of packages. Practically, packages should be built around the primary technologies with the strongest evidence of the highest efficacy in prevention infections: early treatment of partners (96% efficacy among heterosexual couples) [74], condoms (∼70–80% efficacy) [76–78], and oral preexposure prophylaxis (46% efficacy) [73]. Other services, such as periodic HIV and STI testing, allow men to be provided with recommendations for primary interventions based on their HIV serostatus, and to corroborate self-reported levels of behavioral risk. Behavior change interventions promote effectiveness, for example, by supporting uptake of condom use and adherence to drug regimens and repeat HIV testing recommendations.

In many parts of the world, there are substantial barriers to achieving adequate coverage of prevention services for MSM. Both HIV-related stigma and MSM-related stigma operate to discourage men from disclosing to their healthcare providers that they have male sex partners, and from attending clinical services tailored for the needs of gay men [50]. Similarly, criminalization of HIV transmission and male-male sex make it risky for men to have frank conversations about their risks for HIV, and thereby reduce the extent to which the most appropriate recommendations for services can be made [79]. Negative experiences with medical providers can also discourage men from disclosing their risks and asking for appropriate prevention services and commodities [26]. Thus, policy work to support decriminalization of HIV transmission and male-male sex is needed. Training of providers to provide culturally competent care and to take sexual histories that allow discussion of male-male sex should be increased. Table 2 illustrates three examples of targets for HIV prevention interventions, primary interventions, coordinated behavioral interventions, and societal/policy interventions to promote coverage.

Table 2
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In the coming 5 years, we should anticipate the potential for new opportunities in HIV prevention for MSM. First, communication technologies, such as text messaging, smartphone applications, and increased global access to high speed internet, will offer increased opportunities for using technologies to bring prevention services to scale, at marginal increased costs [6,80]. There are promising pipelines for new primary prevention technologies, including rectal microbicides [81]. Additional data sources, and perhaps bridging studies, will help develop our understanding of the efficacy of treatment of HIV-positive anal sex partners, making clearer the relevance of HPTN 052 for MSM [82]. As experience with PrEP (pre-exposure prophylaxis) provision matures, the demand for PrEP and its niche in HIV prevention approaches will become clearer [83].

More than any time in the epidemic, prevention providers and public health practitioners have efficacious tools with which to address re-emerging HIV epidemics among MSM. Because of the high biological bar for preventing HIV transmission through anal sex, we will need to develop coordinated packages of interventions and services, tailored to the needs of groups of MSM that are specific to regions, countries, and communities. To achieve greatest impact, HIV prevention for MSM must comprise the work of clinicians, mental health professionals, policymakers, and peers.

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Provision of comprehensive clinical care

Although the AIDS epidemic raised awareness of unique health needs of MSM, many root causes of HIV vulnerability were not initially fully understood, or incorporated into care and prevention programs [84]. Following list presents key elements of comprehensive clinical care for MSM.

  1. Culturally competent healthcare workers
  2. Confidential HIV counseling and testing services
  3. Access to affordable primary care
  4. Access to screening for bacterial sexually transmitted diseases, including the following:
    1. Syphilis serology with confirmatory testing
    2. Nucleic amplification testing for gonorrhea and chlamydia, including extragenital sites
  5. Screening for viral hepatitis; hepatitis A and B vaccination for susceptibles
  6. Screening for hepatitis C, if HIV-infected; access to treatment, if indicated
  7. Vaccination against human papillomavirus for MSM youth less than 26 years
  8. Access to culturally competent mental health professionals
  9. Access to substance use treatment services
  10. Access to evidence-based prevention interventions, including individual and group counseling
  11. Access to preexposure prophylaxis, if appropriate.

Subsequent analyses of the life experiences of MSM suggest that proximate sources of psychological distress and sexual risk taking may stem from early childhood experiences, including physical and emotional abuse by family and/or peers [85]. Sexual and gender minority youth are often exposed to rejection, which may create internalized homophobia, low self-esteem, and emotional distress [86]. MSM adolescents may experience shame and become depressed when they recognize that their same sex attraction is not socially acceptable. Given that the age of sexual debut is decreasing for youth globally, earlier conflicts are emerging between young MSM's identities and societal norms, at times when they are most vulnerable [87,88]. MSM adolescents are also more likely than heterosexual peers to report substance abuse, transactional sex, and STIs, often in response to a hostile environment. Key institutions, like schools that create safe milieus report better outcomes [89].

Despite social challenges, the majority of MSM are HIV-uninfected and productive, and their resiliency in the face of homophobic adversity warrants further study [90]. Emerging evidence suggests that resolution of internalized homophobia results in improved health outcomes [91]. However, often in response to antecedent stressors, adult MSM have higher rates of mood and anxiety disorders than demographically similar heterosexual men [92]. Unsupportive environments or hostile local norms may increase the likelihood that MSM will ‘self-medicate’ their depression and anxiety, contributing to higher rates of use [93]; however, the majority of substance-using MSM do not become drug-dependent, and that many appear to manage their substance use with relatively few consequences, with the exception of tobacco, alcohol, popper, and/or stimulant use [94]. Methamphetamine, cocaine, and poppers use are consistently and independently associated with unprotected sex and HIV seroconversion [94]. Although studies have suggested that culturally tailored substance use interventions are most effective in decreasing substance abuse among MSM [95], among US federally funded substance treatment providers, only 7.4% offered services that were tailored for sexual and gender minority clients [96]. Health and substance use treatment providers should be sensitized to issues faced by MSM and other lesbian, gay, bisexual, transgender (LGBT) clients that influence access and health outcomes [97]. As noted above, unprotected anal sex puts MSM at increased risk for HIV and other STIs. MSM biological risks are greatly enhanced if they avoid accessing clinical services because of anticipated negative responses from medical providers. Health service avoidance may result in MSM presenting late to care, with increased HIV and STI burdens. Although anal sex may increase HIV risk, social frameworks that do not recognize gay marriage may be counterproductive, by discouraging long-term maintenance of stable relationships. Given the high prevalence of HIV, STI, and mental health concerns among MSM, integrated services and interventions are needed. Substance using MSM should be routinely screened for HIV and STIs, and MSM presenting for HIV or STI care should have comprehensive behavioral health assessments.

Historically, MSM have received inadequate, and often discriminatory, medical care in both resource-rich and resource-constrained environments [98]. Although MSM have diverse health needs, provider training is often limited, particularly in countries where punitive laws may result in invisibility, resulting in few healthcare settings wherein MSM may receive optimal care. The provision of culturally competent care requires training healthcare workers to recognize medical conditions, which are specific for MSM because of distinctive practices (e.g. anal STIs in MSM who are anally receptive), and behavioral health concerns, which may arise from internal or external homophobia (e.g. substance use and depression), as well as knowledge of community norms that require tailored approaches (e.g. same sex couples counseling) [99]. If trusting relationships can be developed, providers may play an important role in helping MSM make healthy choices. Many resources are now available online (e.g. www.glma.org, www.gmhc.org, www.thefenwayinstitute.org) and in print (e.g., The Fenway Guide to Lesbian, Gay, Bisexual and Transgender Health) [100]. Although many of these materials were produced in developed countries, recently, educational materials that are appropriate for use in diverse cultures and resource-constrained settings have been developed (www.health4men.co.za; www.msmgf.org). Optimal healthcare for sexual and gender minorities is essential if the AIDS epidemic is going to be controlled, but moreover, it is a fundamental human right, requiring health professionals as allies.

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Responses: social, structural, community, and human rights

The heavy burden of HIV among gay men and other MSM is a reality in virtually every country affected by HIV and for which data on MSM are available [101]. Gay people realized early on in the AIDS crisis that because of the way gay people are legally and socially marginalized, protecting personal health required community level action. To this day, gay men, lesbians, and their nongay allies continue to be central to the AIDS response – where it has been safe for them to do so, and in many places where it has not been safe [102]. Gay movements targeting HIV arose in different countries based on the local contexts and histories [103–107]. In many cases, it was inaction and blatant disregard by governments for the needs and rights of gay people that mobilized action. Gay people forged a style of AIDS activism that was political and confrontational. This activism has had tangible results, including speeding regulatory approval of products for expanded clinical research; lowering the price of licensed HIV medicines; and building support for research and program funding [108–110]. Yet, although the epidemic has been very important in mobilizing homosexual men, often in extremely hostile environments, it has simultaneously led to greater repression of MSM in some parts of the world, often in the name of ‘tradition, culture, and religion’ [8].

Ironically, three decades into the HIV pandemic, MSM are often excluded from the evidence-based services that they helped develop. However, it is in these challenging environments wherein MSM community members and groups can be among the most effective, and sometimes the only, actors willing to provide and advocate for their communities. The last three decades has witnessed gay men and other MSM working in the HIV response through advocacy, education, research, and design and delivery of prevention, treatment, and care programs benefiting all affected by HIV. For MSM in many settings, including many MSM of color in the United States, engaging in research has often been complicated by a history of neglect and mistreatment by researchers, healthcare systems, and government [111–113]. In addition, MSM community members can be the best persons to describe their own sexual practices and the social and sexual network dynamics that drive incident HIV infections, thereby informing the development of effective responses [114].

MSM continue to lead on HIV advocacy as core participants in the development of strategies, resource allocations, policy development, decision-making, and evaluations of the Global Fund, PEPFAR, WHO and other UNAIDS Co-sponsors, and other global initiatives such as the UN Commission on Human Rights and the Global Commission on HIV and the Law [115–117]. However, MSM remain excluded from official processes in many places where same-sex practices are criminalized or heavily stigmatized [118]. And while gay AIDS advocacy has had tangible impacts, it has come at real personal cost, with activists having been beaten, arrested, and killed [119].

Gay community advocacy and engagement remain essential to ensuring appropriate use of new technologies and benefit from scientific knowledge, to advocate strategic and equitable use of resources, and to address stigma. The third decade of HIV should witness the end of the paradox too often seen today: MSM exclusion from the services that they helped develop. Taking maximum advantage of new HIV technologies and growing recognition of the MSM epidemic, gay communities will require increased resources, support to develop capacity, and expanded opportunities to serve and lead.

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Discussion and conclusion

The goal of global control of the HIV pandemic is now a part of strategic thinking, planning, and research. Recent advances, perhaps most compellingly the findings from Tanser et al.[62] that achievable levels antiretroviral therapy care can reduce HIV incidence at population levels, have led to new optimism that the global pandemic of HIV can be controlled. Yet for MSM, in low, middle, and high income country settings, the epidemic trajectory is markedly different: available prevention and treatment tools are insufficient as single interventions, are reaching inadequate levels of coverage, and continue to be hampered by homophobia, stigma, and discrimination. Treatment for HIV has become a reality, and life-expectancy for HIV-positive persons where treatment is available has been extended by decades. Yet the lifetime acquisition probabilities for HIV in MSM are high, disproportionate compared to other populations and most marked in subepidemics of extraordinary intensity and severity. This must change if global control of the HIV pandemic is to be achieved. This will require policy, program, legal, funding and communications advances on several fronts (Table 3).

Table 3
Table 3
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Table 3
Table 3
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The U.S. PEPFAR guidance on MSM lays out the minimum requirements for programs for MSM [120]: first, community-based outreach and the distribution of condoms and condom-compatible lubricants; HIV counseling and testing in safety and dignity; active linkages to healthcare and ART; targeted information, education and communication (IEC); and finally STI prevention, screening in safety and dignity. Condom and lubricant promotion, commodities, and distribution are an essential minimum of services for HIV prevention in MSM, and lubricant, in particular, remains markedly limited in coverage for MSM in many low resource and high stigma settings [121]. To close the condom and lubricant gap for MSM globally, a modest cost of 136 million USD in 2012 was estimated.

These are essentials, but the available data suggest they will not be sufficient to control HIV epidemics among MSM. Combination preventive interventions will almost certainly be required. Three studies – in the Americas, China, and South Africa – are developing and modeling combination interventions for MSM [122].

A vigorous research agenda is called for to develop and test novel interventions that may reduce the biological, network, and social/structural risks for MSM. More granular and nuanced epidemiologic approaches that utilize the marked assortative nature of MSM epidemics may help target interventions. Both rectal microbicides and HIV vaccines hold promise for reduction of acquisition probabilities. TasP needs to be adapted to MSM epidemics and must be for younger and more recently infected men if its promise as a prevention tool is to be realized. For these interventions, and for PrEP, research on improving adherence and on the development of less-adherence dependent interventions will likely be key to success. Nevertheless, PrEP with Truvada has demonstrated efficacy in three randomized controlled trials (RCTs) in male populations, two in heterosexuals and one in MSM, and should be made much more widely available for MSM at risk who want it. The current pricing structure, particularly in industrialized countries, is a clear barrier to the use of this new intervention and must also be addressed. Structural interventions, including healthcare worker training in LGBT sensitivity, decriminalization of same-sex behavior between consenting adults, and reducing homophobia will likely also be essential to turn the tide for MSM and HIV.

These efforts are essential from a public health perspective, but they are also required to meet minimum international standards for human rights. The universality of human rights, regardless of sexual orientation or gender identity, has been reaffirmed by the UN Secretary General in 2012 [123]: ‘All human beings are born free and equal in dignity and rights. All human beings – not some, not most, but all. No one gets to decide who is entitled to human rights and who is not … lesbian, gay, bisexual, and transgender people are entitled to the same rights as everyone else. They, too, are born free and equal.’

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Acknowledgements

The co-authors express their gratitude to Gregorio Millett for his inputs to this paper and contribution to the field of research of HIV and health disparities among MSM.

C.B. conceived of the manuscript structure, and drafted the introduction, the sections on disease burden and risks, and the discussion and conclusions.

P.S. wrote the prevention section, drafted the research agenda, and reviewed and edited the full manuscript.

J.S. provided an overall review of the draft manuscript and contributed to the research agenda.

S.D.B. wrote the community section, contributed to the design and analysis of the comprehensive reviews, and contributed to the global burden of disease section.

C.C. drafted the policy and recommendations section and contributed to the community section.

A.W. contributed the epidemiology review and created the global burden figures and worked on the epidemiology section.

D.A. drafted the policy sections of the review, and did an overall review and edit of the manuscript.

G.T. worked on the community engagement section.

K.M. drafted the clinical section, and added substantively to the discussion.

This research was supported by grants to the Center for Public Health and Human Rights at Johns Hopkins from amfAR, The Foundation for AIDS Research, The Bill & Melinda Gates Foundation, the Johns Hopkins Center for AIDS Research (NIAID, 1P30AI094189-01A1) and the Partners HealthCare (Mass. General Hospital) and Fenway Community Health NIAID/Harvard CFAR (5P30AI06354-09).

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Conflicts of interest

There are no conflicts of interest.

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Keywords

epidemiology; global burden of disease; health disparities; HIV; human rights; MSM; prevention

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