Elsevier

The Lancet

Volume 380, Issue 9839, 28 July–3 August 2012, Pages 367-377
The Lancet

Series
Global epidemiology of HIV infection in men who have sex with men

https://doi.org/10.1016/S0140-6736(12)60821-6 Get rights and content

Summary

Epidemics of HIV in men who have sex with men (MSM) continue to expand in most countries. We sought to understand the epidemiological drivers of the global epidemic in MSM and why it continues unabated. We did a comprehensive review of available data for HIV prevalence, incidence, risk factors, and the molecular epidemiology of HIV in MSM from 2007 to 2011, and modelled the dynamics of HIV transmission with an agent-based simulation. Our findings show that the high probability of transmission per act through receptive anal intercourse has a central role in explaining the disproportionate disease burden in MSM. HIV can be transmitted through large MSM networks at great speed. Molecular epidemiological data show substantial clustering of HIV infections in MSM networks, and higher rates of dual-variant and multiple-variant HIV infection in MSM than in heterosexual people in the same populations. Prevention strategies that lower biological transmission and acquisition risks, such as approaches based on antiretrovirals, offer promise for controlling the expanding epidemic in MSM, but their potential effectiveness is limited by structural factors that contribute to low health-seeking behaviours in populations of MSM in many parts of the world.

Introduction

In 2012, men who have sex with men (MSM) are at substantial risk for HIV infection in virtually every context studied (panel 1).1, 3, 4 This risk has been present since the syndrome now known as AIDS was first described in previously healthy homosexual men in Los Angeles (CA, USA) in 1981.5, 6, 7 Despite decades of research and community, medical, and public health efforts, high HIV prevalence and incidence burdens have been reported in MSM throughout the world.8 In many high-income settings—including Australia, France, the UK, and the USA—overall HIV epidemic trends are in decline except in MSM, where they have been expanding in the era of highly active antiretroviral therapy (HAART) in what have been described as re-emergent epidemics in MSM.9, 10 In the USA, HIV infections in MSM are estimated to be increasing at roughly 8% per year since 2001.9 And in much of Africa, Asia, and Latin America, the highest rates of HIV infection in any risk group are in these men.8

However, our understanding of worldwide epidemiology is far from complete. By the end of 2011, 93 of 196 countries had not reported on HIV prevalence in MSM in the previous 5 years.11 In several regions, notably the Middle East, north Africa, and sub-Saharan Africa, data for HIV infections in MSM are only emerging.12, 13 Data gaps and challenges to HIV research, surveillance, and epidemiological characterisation in MSM are largely the result of the hidden and stigmatised nature of MSM populations in much of the world, and of ongoing criminalisation of homosexuality and other forms of same-sex behaviour.11 These structural realities have limited our understanding, and might also have crucial roles in the vulnerability of MSM to HIV.14, 15 We review the global epidemiology and disease burden of HIV infection in MSM; individual-level, couple, and network-level risks for HIV acquisition and transmission; biological aspects of anorectal HIV transmission; and molecular epidemiology advances, with the aim of understanding why MSM continue to bear such disproportionate burdens of HIV. We also developed and report on stochastic agent-based simulation models of HIV transmission to further clarify the drivers of HIV spread in MSM.16 Finally, we discuss the public health importance of our emerging understanding of the epidemiology of HIV in MSM.

Section snippets

Disease burden of HIV in MSM

We did a comprehensive search for HIV burden and risks in MSM from Jan 1, 2007, to June 30, 2011 (search criteria in the appendix). We retrieved 2105 unique citations, and we identified and reviewed 68 additional surveillance studies in the public domain. We included country progress reports submitted to the UN General Assembly Special Session on HIV/AIDS (UNGASS). We obtained data from 82 peer-reviewed publications on disease burden of HIV in MSM, from 12 of the 68 surveillance reports, and

Risks for HIV infection

Individual-level risks for HIV acquisition in MSM have been well documented, and include unprotected receptive anal intercourse, high frequency of male partners, high number of lifetime male partners, injection drug use, high viral load in the index partner, African-American ethnic origin (in the USA), and non-injection-drug use, including use of amphetamine-type stimulants (ATS).33, 34, 35 Recent data suggest individual-level risks might be insufficient to explain the high transmission

Biological factors

The biology of anal sex, the gut tropism of HIV-1,74 and the practices and behaviours associated with anal sex, might at least partly explain the high transmission efficiency of HIV infection for this practice. A recent systematic review and meta-analysis of HIV transmission risks in anal sex24 reported a 1·4% per-act probability (95% CI 0·2–2·5) of transmission for anal sex and a 40·4% per-partner probability (6·0–74·9).24 Per-act probabilities did not differ for MSM or heterosexual anal sex.

Molecular epidemiology of HIV-1 in MSM

Recent reports from molecular epidemiology, phylodynamic studies, and HIV virology are providing insights into transmission and acquisition risks for MSM, transmission dynamics in MSM networks, and challenges to HIV prevention for these men. In a 2008 report on HIV transmission dynamics across the city of London,38 episodic bursts of transmission in large linked clusters were identified as characteristics of transmission within MSM populations.38 About 25% of all HIV infections in MSM were

Modelling HIV risk in MSM

We developed a stochastic agent-based network simulation model of HIV transmission to show the size of some key drivers of HIV epidemics for MSM discussed above (details given in the appendix). These drivers include the high per-act transmission rate for anal sex relative to vaginal sex; the unique ability for MSM to be role versatile within high-transmission acts; and the existence of high numbers of partners within a subset of the population. The model thus shares some goals of previous work

Public health significance

Our findings on the epidemiology of HIV in MSM have many implications for HIV prevention, treatment, and care. The second101 and third102 reports in this Series will address these implications in detail and propose a targeted set of interventions for prevention for these men. First, the high transmission probability, high force of infection, and the potent effect of prevalent HIV infections in networks clearly suggest that interventions to reduce infectiousness, such as HAART for HIV-positive

References (105)

  • F van Griensven et al.

    The global epidemic of HIV infection among men who have sex with men

    Curr Opin HIV AIDS

    (2009)
  • CDC

    Follow-up on Kaposi's sarcoma and Pneumocystis pneumonia

    MMWR Morb Mortal Wkly Rep

    (1981)
  • CDC

    Kaposi's sarcoma and Pneumocystis pneumonia among homosexual men—New York City and California

    MMWR Morb Mortal Wkly Rep

    (1981)
  • CDC

    Pneumocystis pneumonia—Los Angeles

    MMWR Morb Mortal Wkly Rep

    (1981)
  • C Beyrer et al.

    The expanding epidemics of HIV-1 among men who have sex with men in low and middle income countries: diversity and consistency

    Epidemiol Rev

    (2010)
  • CDC

    Prevalence and awareness of HIV infection among men who have sex with men—21 cities, United States, 2008

    MMWR Morb Mortal Wkly Rep

    (2010)
  • C Beyrer et al.

    The global HIV epidemics among men who have sex with men

    (2011)
  • G Mumtaz et al.

    HIV-1 molecular epidemiology evidence and transmission patterns in the Middle East and north Africa

    Sex Transm Infect

    (2011)
  • G Mumtaz et al.

    Are HIV epidemics among men who have sex with men emerging in the Middle East and north Africa?: a systematic review and data synthesis

    PLoS Med

    (2010)
  • R Luan et al.

    A study on methods of estimating the population size of MSM in southwest China

    Eur J Epi

    (2005)
  • U Marcus et al.

    The denominator problem: estimating MSM-specific incidence of STI and prevalence of HIV using population sizes of MSM derived from Internet surveys

    BMC Public Health

    (2009)
  • S Cassels et al.

    Mathematical models for HIV transmission dynamics: tools for social and behavioral science research

    J Acquir Immune Defic Syndr

    (2008)
  • UNAIDS

    Report on the global AIDS epidemic—2010. Geneva: UNAIDS, 2010

  • SM McAllister et al.

    Unlinked anonymous HIV prevalence among New Zealand sexual health clinic attenders: 2005–2006

    Int J STD AIDS

    (2008)
  • Sanders EJ, Okuku HS, Mwangome M, et al. Risk factors for HIV-1 infection among MSM in coastal Kenya. 18th Conference...
  • WHO

    HIV/AIDS: data and statistics

  • UNAIDS

    Data and analysis

  • J Faugier et al.

    Sampling hard to reach populations

    J Adv Nurs

    (1997)
  • S Semaan

    Time-space sampling and respondent driven sampling with hard-to-reach populations

    Methodological Innov Online

    (2010)
  • R Baggaley et al.

    HIV transmission risk through anal intercourse: systematic review, meta-analysis and implications for HIV prevention

    Int J Epidemiol

    (2010)
  • D Heckathorn

    Respondent-driven sampling: a new approach to the study of hidden populations

    Soc Probl

    (1997)
  • D Heckathorn

    Respondent-driven sampling II: deriving valid population estimates from chain-referral samples of hidden populations

    Soc Probl

    (2002)
  • Y Guo et al.

    A comparison of four sampling methods among men having sex with men in China: implications for HIV/STD surveillance and prevention

    AIDS Care

    (2011)
  • AR Evans et al.

    Central and east European migrant men who have sex with men in London: a comparison of recruitment methods

    BMC Med Res Methodol

    (2011)
  • PS Sullivan et al.

    Bias in online recruitment and retention of racial and ethnic minority men who have sex with men

    J Med Internet Res

    (2011)
  • LG Johnston et al.

    Efficacy of convenience sampling through the internet versus respondent driven sampling among males who have sex with males in Tallinn and Harju County, Estonia: challenges reaching a hidden population

    AIDS Care

    (2009)
  • S Lieb et al.

    Men who have sex with men: estimated population sizes and mortality rates by race/ethnicity, Miami-Dade County, Florida

    J Acquir Immune Defic Syndr

    (2007)
  • CA McGarrigle et al.

    Estimating adult HIV prevalence in the UK in 2003: the direct method of estimation

    Sex Transm Infect

    (2006)
  • D German et al.

    Persistently high prevalence and unrecognized HIV infection among men who have sex with men in Baltimore: the BESURE Study

    J Acquir Immune Defic Syndr

    (2011)
  • ES Rosenberg et al.

    Number of casual male sexual partners and associated factors among men who have sex with men: results from the National HIV Behavioral Surveillance system

    BMC Public Health

    (2011)
  • B Koblin et al.

    Risk factors for HIV infection among men who have sex with men

    AIDS

    (2006)
  • SM Goodreau et al.

    Biological and demographic causes of high HIV and sexually transmitted disease prevalence in men who have sex with men

    Sex Transm Infect

    (2007)
  • C Beyrer

    Global prevention of HIV infection for neglected populations: men who have sex with men

    Clin Infect Dis

    (2010)
  • F Lewis et al.

    Episodic sexual transmission of HIV revealed by molecular phylodynamics

    PLoS Med

    (2008)
  • ED Charlebois et al.

    The effect of expanded antiretroviral treatment strategies on the HIV epidemic among men who have sex with men in San Francisco

    Clin Infect Dis

    (2011)
  • C Beyrer et al.

    Bisexual concurrency, bisexual partnerships, and HIV among southern African men who have sex with men

    Sex Transm Infect

    (2010)
  • EJ Sanders et al.

    HIV-1 infection in high risk men who have sex with men in Mombasa, Kenya

    AIDS

    (2007)
  • CF Caceres et al.

    New populations at high risk of HIV/STIs in low-income, urban coastal Peru

    AIDS Behav

    (2008)
  • KA Konda et al.

    High rates of sex with men among high-risk, heterosexually-identified men in low-income, coastal Peru

    AIDS Behav

    (2008)
  • F van Griensven et al.

    Trends in HIV prevalence, estimated HIV incidence, and risk behavior among men who have sex with men in Bangkok, Thailand, 2003–2007

    J Acquir Immune Defic Syndr

    (2009)
  • Cited by (0)

    View full text