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Elevated Risk for HIV Infection among Men Who Have Sex with Men in Low- and Middle-Income Countries 2000–2006: A Systematic Review

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  • Stefan Baral
  • Frangiscos Sifakis
  • Farley Cleghorn
  • Chris Beyrer

Abstract

Background: Recent reports of high HIV infection rates among men who have sex with men (MSM) from Asia, Africa, Latin America, and the former Soviet Union (FSU) suggest high levels of HIV transmission among MSM in low- and middle-income countries. To investigate the global epidemic of HIV among MSM and the relationship of MSM outbreaks to general populations, we conducted a comprehensive review of HIV studies among MSM in low- and middle-income countries and performed a meta-analysis of reported MSM and reproductive-age adult HIV prevalence data. Methods and Findings: A comprehensive review of the literature was conducted using systematic methodology. Data regarding HIV prevalence and total sample size was sequestered from each of the studies that met inclusion criteria and aggregate values for each country were calculated. Pooled odds ratio (OR) estimates were stratified by factors including HIV prevalence of the country, Joint United Nations Programme on HIV/AIDS (UNAIDS)–classified level of HIV epidemic, geographic region, and whether or not injection drug users (IDUs) played a significant role in given epidemic. Pooled ORs were stratified by prevalence level; very low-prevalence countries had an overall MSM OR of 58.4 (95% CI 56.3–60.6); low-prevalence countries, 14.4 (95% CI 13.8–14.9); and medium- to high-prevalence countries, 9.6 (95% CI 9.0–10.2). Significant differences in ORs for HIV infection among MSM in were seen when comparing low- and middle-income countries; low-income countries had an OR of 7.8 (95% CI 7.2–8.4), whereas middle-income countries had an OR of 23.4 (95% CI 22.8–24.0). Stratifying the pooled ORs by whether the country had a substantial component of IDU spread resulted in an OR of 12.8 (95% CI 12.3–13.4) in countries where IDU transmission was prevalent, and 24.4 (95% CI 23.7–25.2) where it was not. By region, the OR for MSM in the Americas was 33.3 (95% CI 32.3–34.2); 18.7 (95% CI 17.7–19.7) for Asia; 3.8 (95% CI 3.3–4.3) for Africa; and 1.3 (95% CI 1.1–1.6) for the low- and middle-income countries of Europe. Conclusions: MSM have a markedly greater risk of being infected with HIV compared with general population samples from low- and middle-income countries in the Americas, Asia, and Africa. ORs for HIV infection in MSM are elevated across prevalence levels by country and decrease as general population prevalence increases, but remain 9-fold higher in medium–high prevalence settings. MSM from low- and middle-income countries are in urgent need of prevention and care, and appear to be both understudied and underserved. From a systematic review, Chris Beyrer and colleagues conclude that men who have sex with men in the Americas, Asia, and Africa have a markedly greater risk of being HIV-infected than does the general population. Background.: AIDS (acquired immunodeficiency syndrome) first emerged in the early 1980s among gay men living in New York and California. But, as the disease rapidly spread around the world, it became clear that AIDS also affected heterosexual men and women. Now, a quarter of a century later, 40 million people are infected with human immunodeficiency virus (HIV), the organism that causes AIDS. HIV is most often spread by having unprotected sex with an infected partner and in sub-Saharan Africa, the region most badly hit by HIV/AIDS, heterosexual transmission predominates. However, globally, 5%–10% of all HIV infections are thought to be in men who have sex with men (MSM, a term that encompasses gay, bisexual, transgendered, and heterosexual men who sometimes have sex with men), and in several high-income countries, including the US, male-to-male sexual contact remains the most important HIV transmission route. Why Was This Study Done?: In the US, the MSM population is visible and there is considerable awareness about the risks of HIV transmission associated with sex between men. In many other countries, MSM are much less visible. They remain invisible because they fear discrimination, stigmatization (being considered socially unacceptable), or arrest—sex between men is illegal in 85 countries. Consequently, MSM are often under-represented in HIV surveillance systems and in prevention and care programs. If the AIDS epidemic is going to be halted, much more needs to be known about HIV prevalence (the proportion of the population that is infected) among MSM. In this study, the researchers have done a systematic review (a type of research where the results of existing studies are brought together) on published reports of HIV prevalence among MSM in low- and middle-income countries to get a better picture of the global epidemic of HIV in this population. What Did the Researchers Do and Find?: The researchers found 83 published studies that reported HIV prevalence in 38 low- and middle-income countries in Asia, Africa, the Americas, and Eastern Europe. When the results were pooled—in what statisticians call a meta-analysis—MSM were found to have a 19.3-times greater chance of being infected with HIV than the general population. This is described as a pooled odds ratio (OR) of 19.3. The researchers also did several subgroup analyses where they asked whether factors such as injection drug use (another risk factor for HIV transmission), per capita income, geographical region, or the HIV prevalence in the general population were associated with differential risk (increase in odds) of HIV infection compared to the general population. They found, for example, that in countries where the prevalence of HIV in the general population was very low (less than 1 adult in 1,000 infected) the pooled OR for MSM compared to the general population was 58.4; where it was high (more than 1 adult in 20 infected), the pooled OR for MSM was 9.6. What Do These Findings Mean?: These findings indicate that MSM living in low- to middle-income countries have a greater risk of HIV infection than the general populations of these countries. The subgroup analyses indicate that the high HIV prevalence among MSM is not limited to any one region or income level or to countries with any specific HIV prevalence or injection drug use level. Although the small number and design of the studies included in the meta-analysis may affect the numerical accuracy of these findings, the clear trend toward a higher HIV prevalence of among MSM suggests that HIV surveillance efforts should be expanded to include MSM in those countries where they are currently ignored. Efforts should also be made to include MSM in HIV prevention programs and to improve the efficacy of these programs by investigating the cultural, behavioral, social, and public policy factors that underlie the high HIV prevalence among MSM. By increasing surveillance, research, and prevention among MSM in low- to middle-income countries, it should be possible to curb HIV transmission in this marginalized population and reduce the global burden of HIV. Additional Information.: Please access these Web sites via the online version of this summary at http://dx.doi.org/10.1371/journal.pmed.0040339.

Suggested Citation

  • Stefan Baral & Frangiscos Sifakis & Farley Cleghorn & Chris Beyrer, 2007. "Elevated Risk for HIV Infection among Men Who Have Sex with Men in Low- and Middle-Income Countries 2000–2006: A Systematic Review," PLOS Medicine, Public Library of Science, vol. 4(12), pages 1-11, December.
  • Handle: RePEc:plo:pmed00:0040339
    DOI: 10.1371/journal.pmed.0040339
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    1. Septime P H Hessou & Yolaine Glele-Ahanhanzo & Rhéda Adekpedjou & Clement Ahoussinou & Codjo D Djade & Alphonse Biaou & Christian R Johnson & Michel Boko & Michel Alary, 2020. "HIV incidence and risk contributing factors among men who have sex with men in Benin: A prospective cohort study," PLOS ONE, Public Library of Science, vol. 15(6), pages 1-17, June.
    2. Farisai Gamariel & Petros Isaakidis & Ivan Alejandro Pulido Tarquino & José Carlos Beirão & Lucy O’Connell & Nordino Mulieca & Heitor Pedro Gatoma & Vasco Francisco Japissane Cumbe & Emilie Venables, 2020. "Access to health services for men who have sex with men and transgender women in Beira, Mozambique: A qualitative study," PLOS ONE, Public Library of Science, vol. 15(1), pages 1-16, January.
    3. Jeffy G. Mattathil & Asisa Volz & Olusegun O. Onabajo & Sean Maynard & Sandra L. Bixler & Xiaoying X. Shen & Diego Vargas-Inchaustegui & Marjorie Robert-Guroff & Celia Lebranche & Georgia Tomaras & Da, 2023. "Direct intranodal tonsil vaccination with modified vaccinia Ankara vaccine protects macaques from highly pathogenic SIVmac251," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Eric P F Chow & David P Wilson & Lei Zhang, 2011. "HIV and Syphilis Co-Infection Increasing among Men Who Have Sex with Men in China: A Systematic Review and Meta-Analysis," PLOS ONE, Public Library of Science, vol. 6(8), pages 1-1, August.
    5. Catherine E Oldenburg & Amaya G Perez-Brumer & Sari L Reisner & Jason Mattie & Till Bärnighausen & Kenneth H Mayer & Matthew J Mimiaga, 2014. "Global Burden of HIV among Men Who Engage in Transactional Sex: A Systematic Review and Meta-Analysis," PLOS ONE, Public Library of Science, vol. 9(7), pages 1-1, July.
    6. Luh Putu Lila Wulandari & Rebecca Guy & John Kaldor, 2020. "The burden of HIV infection among men who purchase sex in low- and middle-income countries – a systematic review and meta-analysis," PLOS ONE, Public Library of Science, vol. 15(9), pages 1-23, September.
    7. Jing Wu & Yifei Hu & Yujiang Jia & Yingying Su & Huixia Cui & Huixin Liu & Ning Wang, 2014. "Prevalence of Unprotected Anal Intercourse among Men Who Have Sex with Men in China: An Updated Meta-Analysis," PLOS ONE, Public Library of Science, vol. 9(5), pages 1-1, May.
    8. Sarah E Stutterheim & Mart van Dijk & Haoyi Wang & Kai J Jonas, 2021. "The worldwide burden of HIV in transgender individuals: An updated systematic review and meta-analysis," PLOS ONE, Public Library of Science, vol. 16(12), pages 1-29, December.
    9. Persson, Asha & Ellard, Jeanne & Newman, Christy & Holt, Martin & de Wit, John, 2011. "Human rights and universal access for men who have sex with men and people who inject drugs: A qualitative analysis of the 2010 UNGASS narrative country progress reports," Social Science & Medicine, Elsevier, vol. 73(3), pages 467-474, August.

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