In univariate analysis, the following variables were found to be statistically different for HIV or any of the infections: age group, level of education, employment, place of birth, a prior history of STI, previous HIV testing, to be a sex worker, weekly number of sexual partners, to have a steady partner, to exchange sex for money or goods, use of illegal drugs (cocaine or marijuana), as well as for sexual contacts with foreigners and blood transfusion history. By contrast, use of condom with steady or casual partner was found not to be associated (Table 2).
Risk Factor Analysis
Risk factors for HIV infection were being 30 to 39 years of age, unemployed, and a prior history of STI (Table 3). For HBV-infection, risk factors included participants older than 30 years of age, non-Argentineans, a prior history of STI, previous HIV testing, illegal drugs use, especially cocaine and marijuana, and sexual contact with foreigners. Although the prevalence of HCV was found to be low (1.9%), a greater number of potential risk factors were associated with this infection. Among them were being 30 to 39 years of age, sex workers, weekly number of sexual partners (≥2), sex exchange for money or goods, use illegal drugs, especially cocaine or marijuana, and blood transfusion history. Risk factors for T pallidum infection included older age, less formal education, unemployment, non-Argentineans, a prior history of STI, sex work, weekly number of sexual partners (2–5 partners), no steady partner, and sexual contact with foreigners.
A prior history of STI was associated with HIV, HBV, and T pallidum (ORs = 1.8–4.3). Unemployment was associated with HIV (OR = 2.4) and T pallidum (OR = 2.0) only. Study participants 30 to 39 years of age (OR = 2.5) were also a predictor for HIV infection. Sexual contact with foreigners (OR = 1.6), participants older than 30 years of age (ORs = 2.2–4.2), and non-Argentinean nationality (OR = 4.4) were correlated with an increased risk for HBV infection (Table 4). On the contrary, those who reported a blood transfusion history (OR = 9.7), weekly number of sexual partners (≥2, ORs = 7.0–8.9), and use of illegal drugs (OR = 5.9) remained independently associated with HCV infection.
No risk factors were found to be associated with HTLV I/II. Of the 2 HTLV-I cases found, the first case reported a previous sexual partner who was born in Japan, and the second case was diagnosed in a Peruvian sex worker.
Analysis for coinfections was performed in the 651 (93.8%) subjects in whom full serologic data were available. Almost one-half (48.8%) of participants reported at least 1 infection. Of these 318 subjects, 199, 103, and 16 were diagnosed with 1, 2, 3 or more infections, respectively. The distribution of coinfections is shown in Figure 2. A total of 132 (20.3%), 34 (5.2%), and 29 (4.5%) participants were diagnosed only with HBV, T pallidum, and HIV infection, respectively. The most common coinfections were HBV/T pallidum (8.1%) and HBV/HIV (6.1%). Three risk factors were associated with at least 1 infection: (1) participants of older age (increasing risk with 10-year age intervals for those older than 30 years, OR = 1.6, 95% CI = 1.3–2.0, P <0.001); (2) non-Argentinean nationality (OR = 4.2, 95% CI = 1.3–13.3, P = 0.14); and (3) a prior history of STI (OR = 2.4, 95% CI = 1.6–3.6, P <0.001). HBV was correlated with HIV (OR = 2.8, 95% CI = 1.8–4.5, P <0.001). No significant associations were found between HIV and HCV or T pallidum infections in univariate or multiple logistic regression analysis (data not shown).
To our knowledge, this is the first cross-sectional study to document the prevalence of and risk factors associated with HIV, viral hepatitis (B and C), T pallidum, and HTLV I/II among MSM in Argentina. Our findings indicate that approximately 1 in 7 subjects was infected with HIV or T pallidum, whereas as many as one-third were found to have sustained previous HBV infection. Moreover, we estimated that one-half of MSM in our study had sustained a previous STI. Such high rates of severe, potentially immunocompromising STI are worrisome from a public health standpoint.
The high prevalence of HIV infection found in Buenos Aires correlates well with similar prevalences noted among MSM groups in other major cities of South America, such as in Montevideo, Uruguay (16.9%); La Paz, Bolivia (20.6%); Asuncion, Paraguay (21.8%)2; and among inner city MSM in the United States.21 A prior history of STI appears to correlate well with a history of HIV, HBV, and T pallidum in our study population. Thus, previous HIV infection may be accounted for by increased transmissibility or increased susceptibility to HIV infection, as reported elsewhere.24 It has been documented previously that the odds of HIV infection are increased from 2 to 5 times among individuals who report a previous STI (e.g., via sexual contact).25
HBV infection was the most prevalent STI found in this study. High levels of HBV infection have also been found in other MSM communities in Canada (41%),26 Italy (34%),27 Brazil (37%),28 the United States (28%),29 and New Zealand (8%).30
Sexual contact with an infected person and IDU with needle sharing are the 2 most common ways in which HBV is transmitted. Our results suggest that the transmission of HBV infection was through sexual intercourse due to the low percentage (0.4%) of injecting drug users reported. Of the total HBV infections diagnosed, about 62% occurred among participants aged 30 years or older; a strong linear association of increasing of HBV infection with age in years was also found (OR = 1.06, 95% CI = 1.04–1.08, P <0.001). This association corroborates age as a strong risk factor associated with HBV infection in our study population. However, although age has been also found to be an important risk factor in previous studies, age dependence is probably related to duration of the history of homosexual activity.3
Preexposure vaccination is one of the most effective methods to prevent HBV infection. Vaccination for HBV infection has been available since 198231 and highly recommended for all persons at high risk of acquiring HBV, especially core groups, such as MSM, IDU, heterosexuals with multiple sex partners or with STI, and sex partners of HBV carriers. Recently, in Argentina vaccination for HBV infection has become mandatory for children and preadolescents; however, the adult population has no access to this vaccine for free. Information about a prior HBV immunization was not collected in this study. However, a recent cohort study performed among 327 MSM subjects in Buenos Aires in 2003–2004 reported that only 7% of the participants had received HBV immunization (Avila MM and others, unpublished data). Therefore, due to the high transmission rate of HBV and the unvaccinated adult population in Argentina, it is advisable to provide the vaccine to the MSM population, as well as to recommend HBV vaccination to the adult population. In addition, HBV infection was significantly associated with an HIV-positive serostatus in which the risk of HIV infection increased almost threefold in HBV-infected subjects. This association may be because both viruses share similar routes of transmission. Evidence of the correlation of HIV status and markers for hepatitis B has also been reported among 200 MSM in Uruguay in 1999.32
The HCV prevalence (1.9%) found in this study was similar to that previously described in other MSM communities in countries such as New Zealand (1.8%)33 and the United States (1.2%).14 Acquisition of HCV has been associated with sexual contact, use of illegal drugs, particularly with a history of IDU and syringe/needle sharing.34 Although sexual activity in the transmission of this disease has not been well defined, the high AORs noted for sex work and a greater number of sexual partners strongly suggest that sexual transmission seems to be the most common route of transmission associated to HCV infection.
Outbreaks of T pallidum infection among MSM have been recently reported in the United States in 1998–200220 and in Denmark in 2003–2004.35 A recent study conducted among 451 MSM in Peru reported a T pallidum prevalence of 16%,36 similar to that detected in this study (16.9%). The different risk factors associated with T pallidum infection in our study population clearly indicate the presence of high-risk sexual behaviors among MSM in Argentina. As a genital ulcerative disease, T pallidum infection increases the risk of transmitting and acquiring HIV by three- to fivefold37; this may drive changes in the HIV epidemic in this country. However, it must be pointed out that T pallidum infections have only been retrospectively investigated, therefore reflecting cumulative exposures. It suffers from lack of data related to clinical manifestations. In addition, the percentage of T pallidum/HIV coinfection (21%, 20/94 HIV-infected people) noted in our population was similar to that stated in other large urban regions.38
In Argentina, there is a lack of information regarding the prevalence of HTLV-I/II among MSM. In our study, only 2 cases of HTLV-I infections were detected, and these were individuals from HTLV-endemic countries (Japan and Peru). Further studies are necessary to better understand the real impact of HTLV-I/II infections in this country.
Our study suffered from a number of limitations. First, because of its cross-sectional nature, the associations reported herein between infections and related risk factors may not be related in a cause-effect manner. Second, the nonrepresentativeness of the sample population may narrow the external validity of the findings (true prevalence). Third, this study was conducted only in Buenos Aires, the capital city of Argentina. Thus, we were unable to evaluate any geographical variability among MSM high-risk groups across the country. However, we strongly believe that our study population constitutes a representative sample of inner city MSM in Buenos Aires, thus we believe strongly that we could estimate actual prevalences and associated risk factors in a reliable manner.
In summary, the results from this study reveal an MSM population with high prevalence of HBV, T pallidum, and HIV infection. A prior history of STI was the most common risk factor associated with these infections. Thus, efforts to control the spread of other STIs can help prevent the spread of HIV infection. High-risk sexual behavior associated with STI indicates an urgent need to implement effective and innovative programs for STI/HIV prevention among MSM in Argentina.
1. Caceres CF. HIV among gay and other men who have sex with men in Latin America and the Caribbean: a hidden epidemic? AIDS 2002; 16:S23–S33.
2. Bautista CT, Sanchez JL, Montano SM, et al. Seroprevalence of and risk factors for HIV-1 infection among South American men who have sex with men. Sex Transm Infect 2004; 80:498–504.
3. Kahn J. Preventing hepatitis A and hepatitis B virus infections among men who have sex with men. Clin Infect Dis 2002; 35:1382–1387.
4. Macdonald N, Dougan S, McGarrigle CA, et al. Recent trends in diagnoses of HIV and other sexually transmitted infections in England and Wales among men who have sex with men. Sex Transm Infect 2004; 80:492–497.
5. Gilleece Y, Sullivan A. Management of sexually transmitted infections in HIV positive individuals. Curr Opin Infect Dis 2005; 18:43–47.
6. van der Bij AK, Stolte IG, Coutinho RA, et al. Increase of sexually transmitted infections, but not HIV, among young homosexual men in Amsterdam: are STIs still reliable markers for HIV transmission? Sex Transm Infect 2005; 81:34–37.
7. Gerbase AC, Rowley JT, Mertens TE. Global epidemiology of sexually transmitted diseases. Lancet
. 1998; 351:2–4.
8. Stolte IG, Coutinho RA. Risk behaviour and sexually transmitted diseases are on the rise in gay men, but what is happening with HIV? Curr Opin Infect Dis 2002; 15:37–41.
9. Fenton KA, Lowndes CM. Recent trends in the epidemiology of sexually transmitted infections in the European Union. Sex Transm Infect 2004; 80:255–263.
10. Poland GA, Jacobson RM. Clinical practice: prevention of hepatitis B with the hepatitis B vaccine. N Engl J Med 2004; 351:2832–2838.
11. MacKellar DA, Valleroy LA, Secura GM, et al. Two decades after vaccine license: hepatitis B immunization and infection among young men who have sex with men. Am J Public Health 2001; 91:965–971.
12. Centers for Disease Control and Prevention. Incidence of acute hepatitis B: United States, 1990–2002. MMWR Morb Mortal Wkly Rep 2004; 52:1252–1254.
13. Alter MJ. Prevention of spread of hepatitis C. Hepatology 2002; 36:S93–98.
14. Diamond C, Thiede H, Perdue T, et al. Viral hepatitis among young men who have sex with men: prevalence of infection, risk behaviors, and vaccination. Sex Transm Dis 2003; 30:425–432.
15. Bodsworth NJ, Cunningham P, Kaldor J, et al. Hepatitis C virus infection in a large cohort of homosexually active men: independent associations with HIV-1 infection and injecting drug use but not sexual behaviour. Genitourin Med 1996; 72:118–122.
16. Mueller N. The epidemiology of HTLV-I infection. Cancer Causes Control 1991; 2:37–52.
17. Lairmore MD, Jacobson S, Gracia F, et al. Isolation of human T-cell lymphotropic virus type 2 from Guaymi Indians in Panama. Proc Natl Acad Sci U S A 1990; 87:8840–8844.
18. Lee H, Swanson P, Shorty VS, et al. High rate of HTLV-II infection in seropositive IV drug abusers in New Orleans. Science 1989; 244:471–475.
19. Khabbaz RF, Onorato IM, Cannon RO, et al. Seroprevalence of HTLV-1 and HTLV-2 among intravenous drug users and persons in clinics for sexually transmitted diseases. N Engl J Med 1992; 326:375–380.
20. Centers for Disease Control and Prevention. Primary and secondary syphilis among men who have sex with men: New York City, 2001. MMWR Morb Mortal Wkly Rep 2002; 51:853–856.
21. Centers for Disease Control and Prevention. HIV prevalence, unrecognized infection, and HIV testing among men who have sex with men: five U.S. cities, June 2004–April 2005. MMWR Morb Mortal Wkly Rep 2005; 54:597–601.
22. Ciesielski CA. Sexually transmitted diseases in men who have sex with men: an epidemiologic review. Curr Infect Dis Rep 2003; 5:145–152.
23. Pando M de L, Maulen S, Weissenbacher M, et al. High human immunodeficiency virus type 1 seroprevalence in men who have sex with men in Buenos Aires, Argentina: risk factors for infection. Int J Epidemiol 2003; 32:735–740.
24. Centers for Disease Control and Prevention. Consultation on recent trends in STD and HIV morbidity and risk behaviors among MSM. Atlanta, GA. October 30–31, 2000. Meeting Report.
25. Wasserheit JN. Epidemiological synergy: interrelationships between human immunodeficiency virus infection and other sexually transmitted diseases. Sex Transm Dis 1992; 19:61–77.
26. Remis RS, Dufour A, Alary M, et al. Association of hepatitis B virus infection with other sexually transmitted infections in homosexual men: Omega Study Group. Am J Public Health 2000; 90:1570–1574.
27. Osella AR, Massa MA, Joekes S, et al. Hepatitis B and C virus sexual transmission among homosexuals. Am J Gastroenterol 1998; 93:49–52.
28. Sutmoller F, Penna TL, de Souza CT, et al. Human immunodeficiency virus incidence and risk behavior in the “Projeto Rio”: results of the first 5 years of the Rio de Janeiro open cohort of homosexual and bisexual men, 1994–98. Int J Infect Dis 2002; 6:259–265.
29. Choi KH, McFarland W, Neilands TB, et al. High level of hepatitis B infection and ongoing risk among Asian/Pacific Islander men who have sex with men, San Francisco, 2000–2001. Sex Transm Dis 2005; 32:44–48.
30. Saxton PJ, Hughes AJ, Robinson EM. Sexually transmitted diseases and hepatitis in a national sample of men who have sex with men in New Zealand. N Z Med J 2002; 26:U106.
31. Centers for Disease Control and Prevention. Recommendation of the Immunization Practices Advisory Committee (ACIP) inactivated hepatitis B virus vaccine. MMWR Morb Mortal Wkly Rep 1982; 31:317–328.
32. Russi JC, Serra M, Vinoles J, et al. Sexual transmission of hepatitis B virus, hepatitis C virus, and human immunodeficiency virus type 1 infections among male transvestite commercial sex workers in Montevideo, Uruguay. Am J Trop Med Hyg 2003; 68:716–720.
33. Staples CT, Rimland D, Dudas D. Hepatitis C in the HIV (human immunodeficiency virus) Atlanta V.A. (Veterans Affairs Medical Center) Cohort Study (HAVACS): the effect of coinfection on survival. Clin Infect Dis 1999; 29:150–154.
34. Soriano V, Rodriguez-Rosado R, Garcia-Samaniego J. Management of chronic hepatitis C in HIV-infected patients. AIDS 1999; 13:539–546.
35. Cowan S. Syphilis in Denmark: outbreak among MSM in Copenhagen, 2003–2004. Euro Surveill 2004; 9:25–27.
36. Tabet S, Sanchez J, Lama J, et al. HIV, syphilis and heterosexual bridging among Peruvian men who have sex with men. AIDS 2002; 16:1271–1277.
37. Holmes K, Mardh P, Sparling P, et al. Sexually Transmitted Diseases. 3rd ed. New York: McGraw-Hill, 1999:
© Copyright 2006 American Sexually Transmitted Diseases Association
38. Chan DJ. Syphilis and HIV co-infection: when is lumbar puncture indicated? Curr HIV Res 2005; 3:95–98.