After sub-Saharan Africa and Asia, Latin America is the region most heavily affected by HIV infection. The Latin American HIV epidemic reflects diverse transmission patterns and epidemiology.1 In all countries of the Andean region, men who have sex with men (MSM) account for a substantial proportion of HIV infection2 and comprise a “bridge” group for spreading into the heterosexual population because of the high frequency of reported bisexuality.3,4
Different methods have been proposed to monitor the progress of the HIV epidemic.5 Second-generation HIV sentinel surveillance has the benefit that through monitoring risk behaviors and serving as an “early warning system” for incident HIV infection and sexually transmitted infections (STIs), it may detect changes in HIV epidemiology and risk behavior patterns.6
A nationwide general population-based survey of urban young adults conducted in 20 Peruvian cities during 2002 showed an overall HIV prevalence of 0.2% (0.4% for men and 0.1% for women).7 In comparison, a baseline second-generation HIV sentinel surveillance conducted among MSM in Lima in 1996 found prevalences of HIV and syphilis seroreactivity of 18.5% and 16.0%, respectively, and estimated HIV seroincidence as 11.2% per year.3 Subsequently, the Ministry of Health (MoH) of Peru implemented HIV prevention activities for MSM and other vulnerable populations, including “gay-friendly” clinics in Lima and Peru's larger cities that provided free condoms, voluntary counseling, and STI diagnosis and therapy. Since 1996, second-generation HIV sentinel surveillance has been conducted biannually in Lima among MSM to assist in resource allocation for HIV programs and assess the impact of public health interventions.6 More comprehensive understanding of longitudinal changes in HIV and STI epidemiology can identify appropriate populations and intervention strategies to reduce HIV transmission.8-10 To gain further insight into the HIV and STI epidemic dynamics among MSM in Lima, we assessed and estimated trends in HIV, STIs and sexual behavior among MSM between 1996 and 2002.
Study Population and Procedures
We conducted 4 different sentinel surveillance surveys in Lima, Peru over 3-month periods in 1996, 1998, 2000, and 2002. Men who were at least 18 years of age and had had sexual intercourse with at least 1 man during the previous year were eligible to participate, regardless of their history of HIV-1 testing, serostatus, or treatment. There was no effort to oversample HIV-infected persons during these survey periods. Survey protocols, informed consent, and recruitment materials were approved by the National AIDS and STD Control Program, MoH of Peru; US Navy Medical Research Center; University of Washington; Asociacion Via Libre; and Asociacion Civil Impacta Salud y Educacion Institutional Review Boards. Participants provided written informed consent for participation, HIV and STI testing, and specimen storage for future testing.
Recruitment and referral of participants were based on “snowball” techniques and outreach by peer educators representing diverse MSM subcultures in Lima at previously mapped venues. Approximately 800 different venues were identified for mapping activities every 2 years, including saunas, pornographic movie theaters, video arcades, areas frequented by sex workers and transvestites, discotheques, bars, beauty parlors, and sports areas. Recruitment strategies included the use of posters, distribution of flyers, and informational meetings.
Geographically, to cover Lima, which has more than 8 million inhabitants and encompasses 1750 square miles, different STI clinics from the MoH or private nongovernmental organizations (NGOs) served as sentinel sites during the study periods. At baseline in 1996, implementation of the surveys was piloted in an NGO-sponsored clinic located in a “high risk” area of downtown Lima. Since 1998, sentinel sites were increased to 4 in 1998 and 5 in 2000 and 2002, which are located in each of the most densely populated districts of Lima.
At each sentinel site, counselors explained the study objectives to potential participants and obtained informed consent (for their participation and for provision of blood samples for confidential HIV-1 and STI testing, storage for further testing, or contact for future studies). Men who agreed and provided informed consent underwent a structured interview to collect information about demographics, sexual risk behavior, previous HIV-1 testing and diagnosis, self-designated sexual identity, and number of male and female sexual partners. Questionnaires differentiated sex partners as a primary steady partner and nonprimary nonsteady partners or casual partners. During 1996, 1998, and 2000, interviews were conducted by trained counselors; in 2002, interviews were conducted by computer-assisted self-interview (CASI). Counselors assisted participants in case of illiteracy or computer unfamiliarity. Physicians obtained a medical history and a targeted physical examination, including the genitals, anus, lymph nodes, skin, and oropharynx.
All participants received confidential pre- and post-HIV test counseling, risk reduction counseling, and condoms. Participants with STIs were managed according to Peruvian STD treatment guidelines.11 Participant with a diagnosis of HIV-1 infection received standard health care following Peruvian HIV and AIDS health care management guidelines,12 which did not include antiretroviral therapy at the time these surveys were conducted.
A peripheral venous blood sample was obtained from all participants for detection of antibodies to HIV-1 by means of enzyme immunoassay (in 1996, Abbott Laboratories, Chicago, IL; since 1998, Vironostika, Organon Teknika, Durham, NC) and confirmed by Western blot (in 1996, Cambridge Biotech; Worcester, MA; since 1998, Biorad Laboratories, Hercules, CA). Presumptive recent acquired HIV-1 infection was categorized among HIV-1-infected participants who had an optical density signal-to-cutoff ratio <0.75 in sensitive/less-sensitive or “detuned” EIA testing (Vironostika, Organon Tecnica).13 Those HIV-infected participants with a reactive less-sensitive and sensitive EIA were considered as having chronic HIV infection.
Antibodies to Treponema pallidum were determined by a quantitative venereal disease research laboratory (VDRL, Biotec Laboratories Limited, Suffolk, England) in 1996 or by a rapid plasma reagin (RPR; Organon Teknika) since 1998, with confirmation by microhemagglutination assay (MHA-TP; Organon Teknika). Syphilis seroreactivity was defined by a VDRL or RPR titer ≥1:1 and a positive MHA-TP assay. A presumptive diagnosis of early syphilis was made for a VDRL or RPR titer ≥1:16 and a positive MHA-TP assay. In 2002, herpes simplex virus 2 (HSV-2) antibody testing was performed using a type-specific enzyme-linked immunoassay (ELISA; Focus Technology, Cypress, CA). HSV-2 seroreactivity was defined by a reactive ELISA with an index ratio ≥3.5 to improve specificity.14
Among participants who consented, rectal (from 1996-2000) and pharyngeal (only in 1998 and 2000) swabs were taken for Neisseria gonorrhoeae isolation following standard Thayer-Martin procedures.15 A first-void urine sample was obtained for a leukocyte esterase test (Multistix 2; Bayer, Elkhart, IN) or microscopy of spun urine for white blood cells. A presumptive diagnosis of urethritis was made for those with a positive leukocyte esterase test result or ≥5 leukocytes per high-power field. No further attempts were made to identify the cause of urethritis.
Data were entered into electronic databases, and statistical analyses were computed using Intercooled STATA 7.0 for Windows 98/95/NT (Stata Corporation, College Station, TX). Point prevalences and 95% confidence intervals (CIs) were computed using binomial approximation. HIV seroincidences and 95% CIs were estimated using the testing strategies described by Janssen et al.13 Bivariate comparisons of selected variables used the χ2 test for categoric variables or nonparametric tests as appropriate. Observed trends were analyzed through the extended Mantel-Haenszel χ2 procedure using Statcalc, Epi Info version 3.3.2 (Centers for Disease Control and Prevention, Atlanta, GA). Multivariate binary logistic regression analysis was used to compute annual odds ratios (ORs) for estimated trends of HIV, STI, and condom use among MSM in Lima. Variables for the multivariate model were selected using the single stepwise-forward method. All statistical tests were 2-tailed (P < 0.05).
A total of 4370 MSM met entry criteria, provided informed consent, and were enrolled in the sentinel surveillance surveys: 444 participated in 1996, 1211 in 1998, 1357 in 2000, and 1358 in 2002. Overall, age distribution varies by study year, with a higher proportion of older men in the later years and differences in educational level (Table 1). From 1996 through 2002, knowledge of current HIV-1 serostatus among participants increased from 41.3% to 71.5%, and knowledge of being HIV-positive also increased from 1.4% to 9.7% (P < 0.001 for each comparison). The study population composition based on self-reported sexual orientation varied in each survey (P < 0.001). Across all survey periods, the largest proportion (42.3%-66.7%) of participants self-identified as homosexuals/gays. The proportion of participants reporting any STI symptom during the last year significantly decreased from 34.1% to 29.1% between 1996 and 2002 (P < 0.001).
HIV and Sexually Transmitted Infection Trends
There was an increasing observed trend in the prevalence of HIV-1 infection from 18.5% (95% CI: 15.0% to 22.4%) in 1996 to 22.3% (95% CI: 20.1% to 24.6%) in 2002 (P = 0.006; Table 2). In contrast, there was a decreasing trend in the prevalence of bacterial STIs: syphilis decreased from 16.0% to 12.4% (P = 0.001), early syphilis decreased from 8.6% to 3.4% (P < 0.001), and rectal gonorrhea decreased from 5.1% to 0.2% (P < 0.001). A presumptive diagnosis of urethritis increased modestly from 6.2% in 1998 to 9.4% in 2002. Pharyngeal gonorrhea was diagnosed in 1.5% of participants in 1998 and in 0.7% of participants in 2000. A presumptive diagnosis of recently acquired HIV-1 infection was made in 15 participants in 1996, 17 participants in 1998, 50 participants in 2000, and 32 participants in 2002, providing estimated HIV seroincidence rates of 11.3% per year (95% CI: 4.8% to 23.6%) in 1996, 4.8% (95% CI: 2.1% to 9.6%) in 1998, 12.4% (95% CI: 7.4% to 20.3%) in 2000, and 8.3% (95% CI: 4.5% to 14.7%) in 2002, with no significant trend observed.
No significant trend was found in the prevalence of HIV among young men (18-20 years old) who self-identify as homosexuals/gays (8.0% in 1996, 10.1% in 1998, 8.1% in 2000, and 13.0% in 2002). No significant trend was present when the analysis included men between 18 and 24 years of age (14.3% in 1996, 12.9% in 1998, 16.0% in 2000, and 14.5% in 2002).
HIV and STI prevalence varied by self-reported sexual orientation and year, as shown in Table 3. Importantly, a statistically increasing trend for HIV infection was only observed among those who self-identify as homosexuals/gays (from 18.0% to 26.2%; P < 0.001), which coincided with an increasing proportion presumptively diagnosed with urethritis (from 4.5% to 9.2%; P < 0.001).
Although, overall, transvestites had the highest STI prevalences during the study period, significant decreasing trends for syphilis (from 51.1% to 24.3%; P < 0.001), early syphilis (from 28.9% to 4.3%; P < 0.001), and rectal gonorrhea (from 7.5% to 0.0%; P = 0.003) were observed in this group. Likewise, syphilis also seemed to decrease among those self-identifying as bisexuals (from 11.9% to 3.0%; P < 0.001), whereas early syphilis and rectal gonorrhea significantly decreased among those identifying as bisexuals and homosexuals (see Table 3).
In 2002, overall HSV-2 seroprevalence was 51.0%, with significant differences between groups: 22.4% in those self-identifying as heterosexuals, 26.0% in bisexuals, 57.3% in homosexuals, and 79.6% in transvestites (P < 0.001).
Sexual Behavior and Trends of Reported Condom Use
Self-reported identification as a sex worker was 14.4% in 1998, 10% in 2000, and 17.2% in 2002 (Table 4); however, over all study years, more than 30.2% of subjects reported receiving money or gifts in exchange for sex with other men. The proportion of men reporting sex with women varied from 26.4% in 1996 to 47.6% in 2000.
Condom use during last sexual intercourse with the most recent male steady partner significantly increased from 24.3% in 1996 to 54.1% in 2002 (P < 0.001). When stratified by participants' knowledge of their HIV serostatus, condom use increased significantly over time for those who did not know their HIV status (from 20.8% in 1996 to 51.9% in 2002; P < 0.001) and in HIV-uninfected men (from 27.8% in 1996 to 56.0% in 2002; P < 0.001) but not for those who knew they were HIV-positive. After stratifying by HIV diagnosis, reported condom use significantly increased from 25.7% to 54.2% among HIV-negative men (P < 0.001) and from 17.9% to 54.0% in 2002 among those with chronic HIV infection (P < 0.001). No significant trend was observed among those with recent HIV infection based on the less-sensitive EIA classification (see Table 4).
Notably, there is no clear indication that use of CASI in 2002 for behavioral data collection affected the reporting of sensitive behaviors; as shown in Table 4, for those variables resulting in statistical significant trends, trends remained significant even when data from the year 2002 survey were removed from the analyses (data not shown).
Condom use during last sexual intercourse with the most recent male casual partner did not statistically increase over time. After stratifying by participants' knowledge of their HIV serostatus previous to the survey and by HIV diagnosis made at each survey, no significant trends were observed over time.
Estimated HIV, Sexually Transmitted Infections, and Condom Use Trends
After adjustment for age, educational level, and self-reported sexual orientation, HIV seroprevalence significantly increased over the 8-year period, with an annual OR of 1.06 (95% CI: 1.02 to 1.11), indicating that the odds of having HIV infection among MSM in Lima increased by 6% compared with each previous year. The adjusted OR of syphilis decreased by 9% (OR = 0.91, 95% CI: 0.86 to 0.95) and that of early syphilis decreased by 18% (OR = 0.82, 95% CI: 0.77 to 0.88) each year. From 1996 to 2000, the adjusted odds of having rectal gonorrhea decreased by 64% each year. No changes were expected to occur in urethritis between 1998 and 2002 (Table 5). After including self-reported transactional sex (ie, self-defined sex worker) in the analysis (1998-2002), the adjusted ORs resulted in an increase of 10% in HIV prevalence (OR = 1.10, 95% CI: 1.04 to 1.16), a decrease in syphilis of 12% (OR = 0.88, 95% CI: 0.82 to 0.93), and a decrease in early syphilis of 19% (OR = 0.81, 95% CI: 0.73 to 0.90) each year.
After adjustment for age, educational level, self-reported sexual orientation, and knowledge of HIV serostatus, condom use during last sexual intercourse with the most recent steady partner increased by 26% each year (OR = 1.26, 95% CI: 1.18 to 1.36) over the 8-year study period (see Table 5). The inclusion of self-reported identification as a sex worker did not significantly change (OR = 1.27, 95% CI: 1.17 to 1.37) the trends in condom use between 1998 and 2002.
Since 1998 to 2002, among non-sex workers, condom use during last sexual intercourse with a casual partner significantly increased by 10% each year (OR = 1.11, 95% CI: 1.03 to 1.19) after adjustment for age, educational level, and self-reported sexual orientation (see Table 5), whereas among sex workers, condom use decreased by 25% (OR = 0.75, 95% CI: 0.63 to 0.88).
This first analysis of trends from data collected by second-generation HIV sentinel surveillance among MSM in Latin America involving collaborative efforts of the Peruvian government, NGOs, and US institutions indicates that between 1996 and 2002, HIV prevalence increased by 6% per year among MSM in Lima, whereas declines were observed in bacterial STIs, including syphilis (by 9% each year), early syphilis (by 18%), and rectal gonorrhea (by 64%). The behavioral data indicate that among MSM in Lima, condom use during last sexual intercourse increased by 26% each year with the most recent male steady partner and by 11% with the last male casual partner among non-sex workers.
These observed temporal increases in HIV prevalences, declines in bacterial STIs, and self-reported symptoms of STI in the past year may reflect increasing health-seeking behavior promoted by the MoH during the study period in public STI clinics, which provided free diagnosis and treatment for curable STIs. HSV-2 serologic testing in 2002 indicated an HSV-2 seroprevalence of approximately 50%. Possibly attributable to different compositions of study participants at each survey, a stratified evaluation by self-reported sexual orientation showed that HIV prevalence and presumptive urethritis increased only among those who self-identified as homosexuals/gays. Notably, although transvestites showed the highest STI prevalences over time among all MSM subgroups, consistent declines in the prevalences of bacterial STIs were also observed in this group. Transvestites in Peru are highly stigmatized, with poor access to health services before the implementation of the decentralized MoH-sponsored STI clinics.
Interestingly, knowledge of current HIV-1 status among study participants increased significantly over time, which may reflect success of the voluntary counseling and testing programs conducted by the MoH and different NGOs working in HIV prevention activities. Stratified analysis for those reporting sex with a steady partner showed that condom use during most recent sexual intercourse increased over time among those who did not know their HIV serostatus and HIV-negative men. When the analysis included participants' HIV diagnosis made at each survey, condom use substantially increased among those with no HIV diagnosis and among those with suspected chronic HIV infection. Importantly, high rates of sex with women were reported, with the highest (47.6%) in the 2000 survey.
Considering that, by definition, all sex workers always have sex with casual partners, the validity of the estimated condom use decline (by 25%) among sex workers is difficult to assess in the context that we failed to identify whether or not the last partner was a client, which has important methodologic and epidemiologic considerations.
Worldwide, data on STI and HIV trends before the introduction of antiretrovirals are scarce. Since the increased availability of highly active antiretroviral therapy (HAART), however, different patterns of STI and HIV trends among MSM have been reported worldwide, showing heterogeneity by geographic area and age over time. Most of these reports show stable or decreasing HIV incidences16 with corresponding increasing incidences of syphilis and gonorrhea,17-21 including the occurrence of STI outbreaks, which can be explained by antiretroviral-treated HIV-infected individuals resuming sexual activity.22 Increasing incidences of HIV and other STIs have been reported elsewhere, however.23
A limitation of this study is that sentinel surveillance surveys were convenience-based samples of the population of MSM in Lima every 2 years; MSM were recruited by experienced outreach workers but the composition of the population was not uniform across time. Although all surveys followed standard guidelines6 and recruited large samples of diverse participants representing the diverse MSM subcultures in Lima, the recruiters' knowledge of and access to different subgroups of MSM in Lima are reflected in the varying composition of the samples mainly based on self-reported sexual identity (see Table 1). By extending the sentinel sites in 1998, the composition of the population might have diversified and become more heterogeneous. Additionally, men who participated in these surveys represent the MSM in Lima who visited socialization venues where study recruitment was conducted, who were aware of the conduct of these surveys, and who voluntarily accepted participation. Likewise, MSM perceiving themselves to be at higher risk for HIV or STI acquisition may have been more willing to participate in later surveys, which would provide higher incidence estimates. This scenario would explain the high proportion of men who self-reported as sex workers, reaching as high as 18.3% in 2002.
Surveys were not implemented during the same 3-month period, which could have led to seasonal variations in high-risk behaviors24 and incidence of STIs,25 including HIV. Sexual behavior data are subject to recall bias and the participants' willingness to provide personal information to interviewers or even CASI. Use of CASI in 2002 could have increased the accuracy of responses to survey questions, however, especially those related to self-identification and sexual practices. Although different clinics and personnel participated in all surveys, no major changes over time occurred in the structure of study clinics and procedures followed by study personnel.
Recognizing these limitations, HIV prevalence significantly increased and STI prevalence significantly decreased over time (see Table 5), with the exception of urethritis, which was based on less-specific criteria (eg, leukocytes in first-void urine). Even with substantial declines in syphilis and early syphilis, prevalences remained high in 2002 (12.4% and 3.4%, respectively). The high prevalence of syphilis and HSV-2 may contribute to the 6% annual increase in HIV prevalence and indicate high HIV incidence.26 Our high estimated HIV incidence is corroborated by our longitudinal studies among MSM, which have shown high observed HIV incidences of 3.3 and 6.2 cases per 100 person-years between 1998 and 200027,28 and between 2002 and 2003,29 respectively. Incident HIV infection was associated with newly acquired STIs, which cause genital or anorectal ulcers, and unprotected receptive anal sex with casual male partners.27,28 The continued relatively low level of condom use (∼55% in 2002), the potential effect of role segregation,30 the lack of HSV-2 control measures, and high rates of sex partner concurrence31 may all contribute to high HIV incidence among MSM in Lima.
Given the high rates of new HIV infections, our data suggest that MSM in Lima constitute an important target population for intensified and innovative biomedical interventions. Clinical trials of HSV-2 suppression, pre-exposure chemoprophylaxis, HIV vaccines, and male circumcision among Peruvian MSM are warranted. While these trials are underway, behavioral changes, such as condom use, fewer sexual partners, and voluntary counseling and testing for HIV and STIs, should be promoted. The identification of recent HIV seroconverters would provide a unique opportunity to reduce secondary sexual transmission, given their high viremia and correspondent probabilities of sexual transmission of HIV.32
From 2004, the MoH of Peru and the Global Fund to Fight AIDS, Tuberculosis, and Malaria have scaled up antiretroviral therapy access in Peru. Accordingly, HIV prevalence is likely to increase regardless of changes in the incidence of HIV infection, and second-generation HIV sentinel surveillance methodology needs to be updated. An innovative approach is needed to capture the dynamic nature of the epidemic in the HAART era. Because it is critical to guide prevention and treatment programs, an innovative and integrated approach of community-based surveillance of sexual behavior in high-risk populations should be linked to monitoring HIV incidence, primary and secondary antiretroviral resistance, and phylogenetic diversity in third-generation HIV sentinel surveillance model programs.26
J. Sanchez, L. Suarez, J. L. Sanchez, and C. Celum are among the principal investigators of the HIV Sentinel Surveillance studies conducted among MSM in Peru. This article was conceived and written by J. Sanchez, J. R. Lama, and C. Celum. Statistical analyses were done by J. R. Lama and J. P. Hughes. All the authors participated in data interpretation and manuscript review.
The authors gratefully acknowledge the contributions of the staff of the participating health centers (Asociación Via Libre, Raul Patrucco Health Center, Alberto Barton Health Center, Surquillo Health Center, Tahuantinsuyo Bajo Health Center, Chorrillos I Health Center, and San Jose Health Center) and the men who gave their time to participate in this study.
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Members of the Peruvian HIV Sentinel Surveillance Working Group include the following: Luis Suarez and Monica Pun (Direction of General Epidemiology, MoH, Lima, Peru); César Cabezas and Patricia Caballero (National Institute of Health, MoH, Lima, Peru); Jorge Sanchez, Javier Lama, Juan Guanira, Aldo Lucchetti, Pedro Goicochea, and Jorge Vergara (Asociacion Civil Impacta Salud y Educacion, Lima, Peru); Martin Casapia and Juan Carlos Hinojosa (Asociacion Civil Selva Amazonica, Iquitos, Peru); Victoria Zamalloa (Instituto Sur Peruano de Infectologia, Arequipa, Peru); Abner Ortiz (Centro Medico Cayetano Heredia, Pucallpa, Peru); Nora Ojeda (Asociacion de Servicios Generales de Salud y Educacion, Sullana, Peru); Anabeli Tataje (Policlinico Daniel Alcides Carrion, Ica, Peru); Pablo Campos, Patricia Garcia, and Cesar Carcamo (Universidad Peruana Cayetano Heredia, Lima, Peru); Connie L. Celum, King K. Holmes, Joseph Zunt, William Whittington, and James P. Hughes (University of Washington, Seattle, WA); Jose L. Sánchez (past member); and Silvia Montano, Victor A. Laguna-Torres, and Tadeusz Kochel (US Naval Medical Research Center Detachment, Lima, Peru).