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Epidemiology of Human Immunodeficiency Virus, Viral Hepatitis (B and C), Treponema pallidum, and Human T-Cell Lymphotropic I/II Virus Among Men Who Have Sex With Men in Buenos Aires, Argentina

Pando, María A. PhD*; Bautista, Christian T. MSc; Maulen, Sergio MD; Duranti, Ricardo MD; Marone, Ruben BS; Rey, Jorge MD§; Vignoles, Moira BS*; Eirin, Maria E. BS*; Biglione, Mirna M. MD, PhD*; Griemberg, Gloria BS; Montano, Silvia M. MD, MPH; Carr, Jean K. MHS, PhD**; Sanchez, José L. MD, MPH††; Ávila, María M. PhD*

Sexually Transmitted Diseases: May 2006 - Volume 33 - Issue 5 - p 307-313
doi: 10.1097/01.olq.0000194578.06795.2d
Article

Background: Human immunodeficiency virus (HIV) and sexually transmitted infections (STI) are prevalent among men who have sex with men (MSM).

Goal: To estimate the prevalence of HIV and STIs in this group.

Study: A total of 694 MSM were tested for HIV, hepatitis B (HBV), hepatitis C (HCV), human T-cell lymphotropic (HTLV-I/II) viruses and Treponema pallidum infection.

Results: HIV, HBV, and T pallidum were detected in 13.8%, 37.7%, and 16.9% of subjects, respectively. Prevalences of 1.9% and 0.3% were detected for HCV and HTLV-I/II. A prior history of STI was the most predictor for HIV, HBV, and T pallidum. Use of illegal drugs, blood transfusion history, and multiple sexual partners were associated with HCV. The 2 most common coinfections were HBV/T pallidum and HIV/HBV.

Conclusions: Infection with HIV, HBV, and T pallidum was elevated among MSM. Routine testing, education, vaccine-based prevention, and control programs need to be implemented in this high-risk population.

A cross-sectional study of 694 men who have sex with men was conducted in Buenos Aires, Argentina, to estimate the prevalence of human immunodeficiency virus (HIV) and sexually transmitted infections. This study showed a high prevalence of hepatitis B (37.7%), Treponema pallidum, (16.9%), and HIV (13.8%).

From the *Centro Nacional de Referencia para el SIDA, Departamento de Microbiología, Parasitología e Inmunología, Facultad de Medicina, Universidad de Buenos Aires, Buenos Aires, Argentina; †US Military HIV Research Program at the Walter Reed Army Institute of Research, the Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc., Rockville, Maryland; ‡Nexo, Asociación Civil, Buenos Aires, Argentina; §Laboratorio de Hemoterapia, Hospital de Clínicas “José de San Martín,” Buenos Aires, Argentina; ∥Laboratorio de Inmunología Clínica, Facultad de Farmacia y Bioquímica, Universidad de Buenos Aires, Buenos Aires, Argentina; the ¶US Naval Medical Research Center Detachment, Lima, Perú; **Division of Epidemiology, Institute of Human Virology, University of Maryland Biotechnology Institute, Baltimore, Maryland; and ††Anteon Corporation, Frederick, Maryland

The authors want to thank Wiener Laboratorios of Rosario, Argentina, for the supply of the reagents used for HBV and HCV diagnosis, as well as the technical assistance provided by Sebastian A.

Financial Support: This study was supported by the US Military HIV Research Program at the Walter Reed Army Institute of Research, Rockville, MD, (WRAIR 914) and by the US Naval Medical Research Command, Silver Spring, MD (Work Unit No. 62787A 873 H B0002).

Correspondence: María M. Avila, PhD, Centro Nacional de Referencia para el SIDA, Departamento de Microbiología, Parasitología e Inmunología, Facultad de Medicina, Universidad de Buenos Aires, Paraguay 2155, Piso 11, C1121ABG, Buenos Aires, Argentina. E-mail: mavila@fmed.uba.ar.

Human Use Statement: The study was approved by institutional review boards and scientific ethical committees at the University of Buenos Aires, at the US Naval Medical Research Center, and at the Walter Reed Army Institute of Research in the United States.

Disclaimer: The opinions and assertions contained herein do not reflect the official position of the Argentinean Ministry of Health, of the Department of Defense, of the US Department of the Navy or Army, of the Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc., or of Anteon Corporation.

Portions of the results contained in this manuscript have been presented at the XIV International AIDS Conference, July 2002, Barcelona, Spain (Abstract ThPeC7526); at the 8th World STI/AIDS Congress, December 2003, Punta del Este, Uruguay (Abstract 349); and at the XV International AIDS Conference, July 2004, Bangkok, Thailand (Abstract C12256).

Conflicts of interest: none reported.

HIGH PREVALENCES OF INFECTION with human immunodeficiency virus type 1 (HIV) have been reported among men who have sex with men (MSM) in South America.1,2 Hepatitis B virus (HBV), hepatitis C virus (HCV) and Treponema pallidum infections are found among HIV-infected MSM due to shared modes of transmission.3–6 A marked worldwide geographic variability in the distribution of these sexually transmitted infections (STI) has also been noted.7–9

Since the advent of blood donor screening and universal childhood HBV vaccination in the mid- to late 1980s, HBV infection rates have declined sharply in many developed countries such as Taiwan and the United States.10 However, high HBV infection rates among MSM are still reported in countries where vaccination coverage levels are less than 10%.11–12

HCV infection has been found to be more prevalent among persons who have had sexual contact with an HCV-infected partner, who reported multiple sexual partners, or among those of a younger age at first sexual encounter and among MSM and heterosexual men who do not routinely use condoms.13 However, the importance of person-to-person contact and sexual activity in the transmission of this disease has not been well defined. Most HCV cases (approximately two-thirds) in the United States have been associated with injecting drug use (IDU) behavior. Other studies conducted in the United States14 and Australia15 have documented that IDU was the prevailing risk factor associated with HCV infection among MSM.

Human T-cell lymphotropic virus type I (HTLV-I) has a worldwide distribution; however, it appears to be endemic in the southwestern islands of Japan, the Caribbean, and in some areas of Africa and Latin America.16 By contrast, human T-cell lymphotropic virus type II (HTLV-II) has been reported to mainly affect Amerindians17 and some communities where IDU is prevalent.18,19

Increases in high-risk sexual behavior, such as unprotected anal intercourse with more than 1 sexual partner and unsafe sex under the influence of alcohol or recreational drugs, have also accounted for an increase in T pallidum and HIV infections among MSM in the United States20,21 and in certain countries in Europe.5,6 In addition, loss of fear of acquiring and transmitting HIV and lower levels of condom use may also represent contributing factors to STI transmission.22

To better guide future STI-specific prevention strategies, a cross-sectional epidemiological study was conducted to estimate the prevalence of HIV, HBV, HCV, HTLV-I/II, and T pallidum infection, as well as to examine the potential role that high-risk behavior factors may have in their transmission among MSM in Buenos Aires, Argentina.

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Materials and Methods

Study Population and Enrollment Procedures

MSM who resided in the Buenos Aires city area, who reported sustaining sexual relations with at least 1 other man in the preceding 6 months, and who were 18 years of age or older were invited to participate during the period of March 2000 through March 2001. Participants were recruited by means of informational leaflets, which were distributed in gay nightclubs, porno cinemas, gymnasiums, and streets. Direct referral to study investigators was made to Nexo Asociación Civil, a large, gay-supporting, nongovernmental organization. HIV and other STI prevention pre- and posttest counseling was conducted at the Nexo offices in a confidential manner by trained interviewers, who explained the study objectives and procedures and obtained written informed consent. Only those subjects who were willing to participate and provided written informed consent were enrolled.

Study participants provided clinic-epidemiologic data using a standardized questionnaire that outlined the following: (1) subjects’ demographic characteristics (such as age, nationality, educational level, and employment status); (2) current sexual practices (such as prior history of STI, previous HIV testing, weekly number of sexual partners, use of condoms with steady and casual partners); (3) history of exchange of sex for money or goods (drugs or food); (4) use of drugs (such as cocaine, marijuana, or other illegal drugs); (5) sexual contact with foreigners; and (6) blood transfusion history.

All participants found to be infected with any agent infected were subsequently referred for medical follow-up at local designated medical centers, as well as for evaluation by a social worker.

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Serology

HIV infection was diagnosed by means of enzyme-linked immunosorbent assay (ELISA) (SERODIA-HIV 1/2, Fujirebio, Tokyo, Japan). HBV infection was screened for by ELISA; reactivity to HBV surface antigen (HBsAg) and/or anticore antibodies (anti-HBc) (Wiener Laboratorios S.A.I.C., Rosario, Argentina) was considered evidence of previous HBV infection. HCV infection (anti-HCV) was screened for by ELISA (anti-HCV ELISA, Wiener Laboratorios, SAIC, Rosario, Argentina). Antibody screening for HTLV-I/II was performed by particle agglutination technique (SERODIA-HTLV-I, Fujirebio, Tokyo, Japan) and by ELISA (Platelia HTLV-I, New BioRad, Marnes la Coquette, France). Serum samples that were found to be reactive by particle agglutination and/or ELISA were confirmed by Western blot assay for HIV (Novapath HIV-1 Immunoblot, BioRad, Marnes la Coquette, France) and for HTLV-I/II (HTLV blot 2.4, Genelabs Diagnostics, Science Park, Singapore). Past T pallidum infection was screened for by VDRL (Wiener Laboratorios, SAIC, Rosario, Argentina); confirmatory testing was conducted by T pallidum hemagglutination assay (TPHA Biosystems, Barcelona, Spain) and by indirect immunofluorescence test (FTA-Abs, Inmunofluor Biocientifica SA, Argentina). T pallidum infection was diagnosed if the serum sample was reactive by VDRL and reactive by either the TPHA or FTA-Abs methods.

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Statistical Analyses

χ2 and Fisher exact test were used to compare proportions. Student’s t test or Mann-Whitney U test was used to compare continuous variables. Associations of risk factors with HIV, HBV, HCV, and T pallidum infections were expressed as odds ratios (ORs) with 95% CI. ORs were adjusted (AOR) for age and education. Potential risk factors with a P value <0.25 were selected for possible inclusion in stepwise forward logistic regression analysis, with thresholds of P = 0.10 for entry into to and removal from the model. All reported P values were 2 sided. Analyses were carried out using Stata v. 8.0 (Stata Corporation, College Station, TX).

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Results

Study Population

A total of 694 (98%) MSM subjects who were approached for participation were enrolled; details of enrollment have been published elsewhere.23 At entry, the mean age ± SD of the study participants was 30.9 years ± 8.9 (range = 18–66 years). Almost one-half (47.3%) of participants reported a university-level education, 593 (85.4%) were employed in professional positions, and most of them (95.2%) were Argentinean born. Only 11 (1.6%) subjects identified themselves as sex workers, and 47 (6.8%) participants reported exchange of sex for money, drugs, or food. A prior history of STI or use of illegal drugs was reported by 171 (24.6%) subjects and 126 (18.2%) of subjects, respectively. An IDU behavior was reported by only 3 (0.4%) subjects; 16.6% and 6.5% reported marijuana or cocaine use. Almost one-quarter (22%) of participants reported 2 or more sexual partners per week, and one-third (35.4%) reported sexual contacts with foreigners. A high frequency of irregular condom use was observed (e.g., never or sometimes) with steady partners (61.2%) and with casual partners (53.0%).23

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Prevalences

Infections with HIV, HBV, and T pallidum were detected in 96 (13.8%), 257 (37.7%), and 112 (16.9%) of study participants, respectively (Table 1). In contrast, prevalences of 1.9% and 0.3%, respectively, were noted for HCV and HTLV-I/II. A pattern of increasing prevalence with age was found for HBV and T pallidum (P <0.001, χ2 for trend), but not for other agents (Fig. 1). The mean age of HBV-positive subjects (33.7 years) was significantly older than for HBV-negative ones (30.1 years, P <0.001). Likewise, subjects with past T pallidum infections were also noted to be older than those who were negative (34.1 versus 30.1, P <0.001).

TABLE 1

TABLE 1

Fig. 1

Fig. 1

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).

TABLE 2

TABLE 2

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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.

TABLE 3

TABLE 3

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.

TABLE 4

TABLE 4

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.

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Coinfections

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).

Fig. 2

Fig. 2

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Discussion

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.

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