Objective This cross-sectional study investigates HIV, other sexually transmitted infections (STI), and risk behaviours among men who have sex with men (MSM) in two cities in El Salvador.
Methods Respondent-driven sampling (RDS) was used to recruit MSM in the cities of San Salvador and San Miguel, El Salvador. Participants responded to questions about HIV risk behaviours; and blood, urine and anal swabs were collected. Blood samples were tested for herpes simplex type 2, syphilis and HIV infection. Urine and anal samples were tested by polymerase chain reaction (PCR) for Chlamydia trachomatis, Neisseria gonorrhoeae, Trichomonas vaginalis, and Mycoplasma genitalium. HIV-positive samples were tested with the BED capture enzyme immunoassay to distinguish recent from longstanding HIV infection. We estimated population-adjusted prevalence of behavioural variables, STI and HIV, and identified risk factors for HIV.
Results The final sample included 596 and 195 MSM in San Salvador and San Miguel, respectively. Consistent condom use was low across all partner types as was recent HIV testing. RDS-adjusted HIV prevalence was 10.8% (95% CI 7.4% to 14.7%) in San Salvador, and 8.8% (95% CI 4.2% to 14.5%) in San Miguel. The proportion of recent testing among HIV-positive samples was 20%. Prevalence of any bacterial STI by PRC testing was 12.7% (95% CI 8.2% to 17.5%) in San Salvador, and 9.6% (95% CI 4.9% to 15.4%) in San Miguel.
Conclusions We found a high prevalence of HIV, high levels of recent infection, and low condom usage. In El Salvador, targeted interventions towards MSM are needed to promote condom use, as well as to diagnose, treat and prevent HIV and other STIs.
- Sexual Behaviour
- Latin America
- Gay Men
- Infectious Diseases
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In El Salvador, as in most of Latin America, the prevalence of HIV has remained below 1% among the general population. For instance, among pregnant women tested in antenatal clinics across El Salvador from 2003 to 2007, HIV prevalence was 0.16%.1 Conversely, the HIV epidemic disproportionately affects high-risk groups, such as female sex workers and men who have sex with men (MSM).2 However, in many countries in the region, there are few representative data on these most at-risk populations. The only study of HIV/sexually transmitted infections (STI), prevalence and behavioural indicators among MSM in El Salvador was conducted in 2002, and has been used as a baseline estimate for HIV-related indicators for the country since then. The study found a high prevalence of HIV and other STIs among a convenience-based sample of MSM in which 15.3% tested positive for HIV, and 10.9% for syphilis infections.3 The study documented that MSM in El Salvador had the highest rates of HIV in Central America with rates similar to those in some large cities in South America.4 ,5 Some of the challenges to an effective response to the HIV epidemic in El Salvador are the same found throughout the region, high levels of poverty, migration, homophobia and HIV-related discrimination.6
In 2008, we conducted a study on HIV and other STIs, and risk behaviours among MSM in two cities in El Salvador. The study was designed to provide representative data on socially networked MSM in these cities using respondent-driven sampling (RDS). This paper presents the main results of the study.
The study was conducted from March to September 2008 in San Salvador and San Miguel using RDS methods to recruit males, 18 years and older, who had engaged in anal sex with another biological man in the previous year, and who lived and/or worked in their respective study sites. San Salvador is the capital city and has the highest HIV rates in the country, while San Miguel is the second most important economic centre.1 Prior to the study, we conducted a formative assessment of MSM and transgender persons in both cities in close collaboration with local organisations working with MSM, to ensure that social networks were strong enough to support the RDS methodology, to inform the questionnaire development, and to identify proper study-site locations and hours of operation, as well as possible RDS ‘seeds’.7 The sample sizes for each city were based on the estimated numbers of MSM who could be reached in the different cities after this assessment. Sample sizes of 600 MSM in San Salvador and 200 for San Miguel were proposed to detect at least an 11% and 19% change, respectively, on a dichotomous behavioural indicator, between the current survey and the next behavioural surveillance round, using a conservative estimate of a baseline 50% prevalence rate, 80% power, and an assumed survey design effect of 2.0.
To initiate RDS recruitment of MSM peers, various ‘seeds’, diversified with respect to age, self-identification of sexual orientation and income levels were located through local organisations working with MSM. Eleven seeds were used in San Salvador and five in San Miguel. All the seeds, as well as each successive participant, received three coupons to recruit other MSM. The data collection sites were either private dwellings or locales rented for the study without any identifying information, in order to ensure privacy. Recruits who presented a valid coupon to a study site were screened for eligibility and were provided information about the study. They were then asked to provide written informed consent. They responded to questions in a computer-based as well as a face-to-face interview, and were asked to submit blood, urine and anal swab samples. All participants received promotional materials, condoms and a choice of other incentives (T-shirt, towel, make-up kit, lubricants, and additional condoms) for each recruited peer they referred (up to three). Recruitment was tracked using RDS coupon numbers, as names were not collected.
Urine was screened by PCR for bacterial STIs, including Chlamydia trachomatis, Neisseria gonorrhoeae, Trichomonas vaginalis, and Mycoplasma genitalium. Anal swabs were tested for C trachomatis and N gonorrhoeae. Blood samples were tested for HIV, syphilis and HSV-2 infections. Syphilis seropositivity was estimated based on reactive rapid plasma reagin (RPR) and positive Treponema particle-hemagglutination assay (TPHA) results. Active syphilis was defined as an RPR titre ≥1 : 8 and a reactive TPHA result. HSV-2 serology was performed with the HerpeSelect (Focus Technologies, Cypress, California, USA). STI test results and free treatment to participants with symptoms of STI, or a laboratory-diagnosed STI, were provided through the participating government health centres. HIV testing was performed on-site with two rapid HIV tests (Determine HIV-1/2 and OraQuick Rapid HIV-1 Antibody Test). Participants received post-test counselling, and received their HIV test results 30 min after testing.
All HIV-positive specimens, confirmed by ELISA at the El Salvador MOH's National Reference Laboratory, were tested to distinguish recent from longstanding HIV infection, using methods described in detail by Parekh and colleagues8 for the BED-capture enzyme immunoassay (BED-CEIA), which assumed a mean duration of recency of 197 days (95% CI 193 to 220) for recent infection.8 ,9 Specimens that classified as a recent infection on the BED-CEIA, but originated from participants who reported a duration of HIV infection >12 months, were redefined as longstanding HIV. We estimated the level of recent infection in the sample by calculating the proportion recent among HIV-infected samples, stratified by age, to assess the relative differences in the level of recent infection across younger (aged 15–24 years) and older (aged 25 years and older) MSM. HIV-positive specimens that were not tested on the incidence assay, were assumed to be missing at random. Given the lack of standardised guidance for estimating recent HIV infection in RDS surveys, estimation of the recent proportion in the sample was restricted to the specimen level, and not adjusted for study design effect or sampling weights.
Exposure to behaviour-change interventions was defined as the proportion reporting participation in HIV or risk-reduction counselling, or educational lecture sessions on HIV prevention in the previous 12 months. Consistent condom use was defined according to partner type, as always using a condom with that partner during the previous 12 months.
Proportion estimates and 95% CI for each city were calculated using the RDS Analysis Tool V.6.0.1 (RDSAT).10 All variables analysed were assessed for equilibrium with convergence radius set at two percentage points.11 Bivariate analysis with HIV positivity was also conducted using RDSAT to determine prevalence estimates and 95% CI. The bivariate analysis excluded those who had a previous HIV diagnosis or positive test result (n=18 from San Salvador, n=2 from San Miguel). For statistical evaluation of the results, overlaps in RDSAT-derived 95% CI were compared. In addition, univariate logistic regression analysis incorporating individual weights generated by RDSAT was employed to determine significance using the outcome variable. These weights reflected adjustments for any biases as a result of differential network sizes or recruitment patterns. Multivariate results are not presented due to small sample sizes, our preliminary analysis being hypothesis generating, and our focus being risk markers rather than identifying causality. The ethical review board of the Rosales National Hospital in San Salvador, and the US Centers for Disease Control and Prevention's Division of Global HIV/AIDS Chief of Science Office, reviewed and approved the study protocol.
The 11 seeds in San Salvador recruited 596 participants with an average of eight waves per seed, while in San Miguel, the five seeds averaged seven waves and recruited 195 participants. Unadjusted results are presented in table 1 along with the RDS-adjusted data, and only RDS-adjusted results are presented below. The majority of MSM in San Salvador (60%) and San Miguel (73%) were estimated to be <24 years of age (table 1). In both cities, over 40% of MSM were estimated to self-identify as heterosexual or bisexual; however, far fewer MSM in San Miguel (22%) than in San Salvador (46%) were identified as being gay or homosexual. The proportion of MSM selling sex in the previous 12 months was estimated to be 19% in San Salvador and 14% in San Miguel, while nearly 60% in both cities had had a casual partner during the 12 months prior to the study.
Consistent condom use was low with all partner types. In San Salvador and San Miguel, respectively, an estimated 35% and 30% of MSM with stable male partners consistently used condoms with them, while 76% and 66% of MSM who had exchanged sex for money in the previous 12 months had used condoms consistently with their clients. For MSM with casual partners, an estimated 44% in San Salvador and 35% in San Miguel, consistently used condoms. A total of 26% and 48% of MSM had sex with both men and women in the previous 12 months in San Salvador and San Miguel, respectively. Consistent condom use among MSM with female partners was 5% and 16%, respectively.
Exposure to behaviour change interventions was slightly higher in San Salvador (64%) compared with San Miguel (51%). Only 58% of MSM in San Salvador were estimated ever to have had an HIV test, and 30% had been tested in the year prior to the study. In San Miguel, the figures were estimated to be 41% and 22%, respectively.
In total, 87%, of recruited MSM submitted specimens for HIV testing in San Salvador, and 94% in San Miguel. HIV prevalence was 10.8% (95% CI 7.4% to 14.7%) in San Salvador, and 8.8% (95% CI 4.2% to 14.5%) in San Miguel. Among all HIV-positive specimens, 85.3% in San Salvador and 78.9% in San Miguel were available for BED-CEIA testing. Of 24 specimens that classified as recent on the BED-CEIA, 3 (13%) were from participants who reported a duration of HIV infection >12 months and subsequently redefined as a longstanding HIV infection in the analysis. The proportion of HIV-positive specimens testing recently on the assay was 21.4% overall, 34.8% among participants in the youngest age group (18–24 years), and 9.6% among participant aged 25 years and older. The proportion of recent infections was significantly higher among MSM in the youngest age group compared with those aged 25 years and older (p<0.01).
Among HIV-positive MSM, only 23% and 11%, in San Salvador and San Miguel, respectively, had received a previous HIV-positive test result or diagnosis. Individuals unaware of being HIV/infected (reporting HIV-negative or unknown status, but testing positive for HIV as part of the survey) were most prevalent among men 18–24 years of age (33/36, 92% and 9/9, 100% in San Salvador and San Miguel, respectively) compared with men 25 years of age and older (14/39 36% and 2/10, 20%, respectively).
Syphilis seropositivity was 12.1% (95% CI 8.4% to 16.2%) in San Salvador and 8.1% (95% CI 3.8% to 13.9%) in San Miguel. Active syphilis was prevalent in 4.4% (95% CI 2.6% to 6.7%) and 0.7% (95% CI 0% to 1.7%) of MSM in the two sites, respectively. The prevalence of other STI is shown in table 1.
In bivariate analysis (table 2), we found HIV infection was associated in both cities with self-identification as gay or homosexual, HSV-2 seropositivity, and not having had vaginal sex in the previous 12 months. In San Salvador, HIV infection was also associated with testing positive for any bacterial STIs in the urine, being >24 years of age, and having sold sex in the previous 12 months; in San Miguel it was associated with anal sex debut by age 15 years.
This study was successful in recruiting large numbers of MSM through the use of RDS in El Salvador. The study documents high HIV prevalence and a high proportion of recent infections among younger MSM. Most HIV-positive men in this population are unaware of their status. HIV testing and coverage of HIV prevention interventions is suboptimal, and the impact of these interventions is small, as demonstrated by the low levels of condom use with both male and female partners.
Alarmingly, the level of recent infection among young MSM (aged 15–24 years) was three times higher than levels observed among older MSM, highlighting the heightened vulnerability of young MSM in El Salvador to HIV infection. In comparison, the level of recent infection observed among older MSM (aged 25 years and older) was similar to expected levels of recent infection among the general population in mature epidemics, where approximately one in 10 HIV infections are expected to be recently acquired.12
Compared with the findings of the 2002 survey of MSM in San Salvador, we found slightly lower HIV prevalence, slightly higher rates of HIV testing, and better exposure to behavioural change interventions.3 We also found similar rates of syphilis and similarly low condom use across partner types. Although the earlier study used convenience sampling and the two cannot be compared, it is apparent that more action is needed to improve health behaviours and outcomes.
In bivariate analysis, HIV infection was associated with HSV-2 infection in both cities as well as with urethritis in San Salvador. The association between HIV and STI has been documented previously.13 ,14 Currently, there is no national strategy in El Salvador to improve management of STIs among MSM, but the high rates of syphilis, HSV-2 and Chlamydia underscore the need for a strategy that will address integrating STI management into primary healthcare, improving services for minority populations, strengthening STI syndromic management, and improving laboratory screening for syphilis and other STIs.
HIV prevalence is high among MSM in San Salvador and San Miguel, with many unaware of their HIV-positive status. The high level of unrecognised HIV infections among MSM is a public health concern. Persons aware of their HIV infection often take steps to reduce their risk behaviours, which could reduce HIV transmission.15 ,16 To increase the proportion of HIV-positive persons who know they are infected, sexually active MSM should be encouraged to have an HIV test at least annually and more often if they have multiple partners or engage in illicit drug use; and the test should be actively offered by health workers.17–19 Corresponding initiatives should be developed to identify and address barriers to testing, and to increase the availability of testing in both clinical and non-clinical settings. Those aware of their HIV infection would have the opportunity to be linked to care and treatment. El Salvador has good antiretroviral therapy coverage,20 and in light of the recent findings of the HIV Prevention Trials Network, improving the number of individuals on treatment in El Salvador may help reduce the likelihood of HIV transmission.21
This study has some limitations. It is believed that weighted estimates generated from RDS generalise to the population as a whole. However, recent assessments suggest that variance may be underestimated, particularly in the presence of tightly linked subgroups which are poorly connected to the rest of the social network (ie, ‘bottlenecks’).22 Others suggest that biases in under-representation of certain groups cannot be reduced by RDS inference methods.23 In this study, for variables such as age, place of work, self-identification and educational level, we observed relatively large numbers of recruitments from each variable category to the remaining categories (ie, no zero cells in the recruitment matrix), suggesting that network bottlenecks were not a major concern with respect to these variables (data not shown). Evaluations of the RDS recruitment strategy also suggest that bias may be introduced if too few waves are included, or if recruitment is preferential.24 In our study, of the 16 seeds, 10 resulted in long chains reaching at least five waves of recruitment. The longest recruitment chain included 19 waves. Finally, in RDS, estimates are based on a with-replacement random-walk model, while the actual sampling is without replacement. When a substantial fraction of the target population is sampled, this approximation can lead to bias in the resulting estimators.24 Based on a recent population size estimation of MSM in El Salvador, the RDS study sample represented less than 5%–12% of the estimated population.25 The sample covers only two cities in El Salvador; however, the cities account for almost half the population of El Salvador and concentrate 63.5% of HIV notifications.26
In settings like El Salvador, where the HIV epidemic is concentrated in high-risk populations, incidence assays represent an important attempt to provide up-to-date information on new infections, and identify groups at highest risk for acquiring HIV, in order to evaluate the impact of prevention programmes. Due to concerns about the accuracy of incidence assays in distinguishing recent from long-standing HIV infection, it is likely that the BED-CEIA misclassified some true longstanding infection as recent infection. We were able to address this to some degree by comparing cases that were tested recently on the assay with individual level data collected on duration of HIV infection in the survey. It is still possible that some longstanding infections remained classified as recent cases in the analysis, resulting in an overestimation of the level of recent infection in the sample. Though the level of false-recent misclassification is unknown if the assay was applied correctly and consistently, we do not expect assay misclassification to have significantly impacted the relative difference we observed in the level of recent infection across age strata. Data on recent infection were not adjusted for sampling weights and survey design effect in this analysis. Therefore, the level of recent infection, and the relative differences observed across age strata, should not be generalised to the broader population of MSM in El Salvador. As improved assays are developed, and more countries consider use of incidence assays in different settings, guidance is needed on how to effectively and accurately utilise this tool for informing and directing the HIV response in concentrated epidemic settings.
El Salvador has made great strides in the prevention of HIV transmission among certain non-MSM groups.27 Mother-to-child transmission decreased by more than 80% from 2003 to 2007; and in 2006, over 40% of the 241 146 HIV tests conducted at public facilities were for pregnant women where the total number of attended births was 69 511,28 and HIV prevalence was 0.16%.1 Rates in MSM are dozens of times higher for a population that is estimated in San Salvador at over 12 000, and will be higher on a national level.25 The same energy and resources that made these achievements possible should now be focused on those most at risk for HIV infection in El Salvador, who may constitute more important drivers of the HIV/AIDS epidemic. A recent study showed that funding for prevention of HIV targeted to MSM was just over US$80 000 in 2007, or 0.76% of all prevention money spent by the public sector in El Salvador.29 These findings reflect a tendency in Latin America, as well as globally, not to allocate HIV prevention resources based on the local epidemiology, but rather to be influenced by the social stigma and homophobia prevalent in the region.27 ,30 MSM in El Salvador, especially the youngest, are highly vulnerable to HIV. There is an urgent need for focused and improved HIV prevention strategies that are culturally and contextually appropriate for this population.
High prevalence of HIV, high levels of recent infection, and low condom usage were found among MSM in two cities in El Salvador.
Targeted interventions towards Salvadoran MSM should promote condom use, at least annual HIV testing, appropriate linkage to HIV care and treatment and STI diagnosis and treatment.
We would like to express our gratitude to the study participants and study staff, and to the Ministry of Health of El Salvador for leading this study. Furthermore, we have to thank Ron Ballard and Lisa Steele for providing quality control for laboratory testing at the Centres for Disease Control and Prevention STD Laboratory; to Nelly Arguera from the National Laboratory of the Ministry of Health in El Salvador for processing all serological tests; and Juan Pascale and Juan Castillo at the Gorgas Memorial Institute, Panama City, Panama, for conducting the testing for STIs by PCR. Thanks to Julio Armero, Guillermo Garay, and Rodrigo Siman from the Ministry of Health, Elizabeth Rodriguez from the World Bank, and Mari Carmen Estrada from the US Agency for International Development, for their contribution to the protocol, and valuable support during data collection. Special thanks to Gerardo Lara from PASMO, William Hernandez from Entre Amigos, and Monica Hernandez from Arcoiris for their support and guidance for planning and supporting the project. We thank Pamela Scofield for thoroughly and thoughtfully editing the manuscript. Finally, our appreciation to the two anonymous reviewers whose comments contributed to improving the final version of this manuscript.
Contributors GPB, JC and EM designed the study and wrote the protocol. JC, MG, GPB and AK contributed to development of survey instruments and procedures. JC, MG and AIN coordinated data collection. JC, GPB, AK and JL drafted the manuscript. JL, MG and AK conducted data analysis. All authors helped to conceptualise ideas, interpret findings and to review drafts of the manuscript.
Funding Funding for this study has been provided by the US Centers for Disease Control and Prevention, US Agency for International Development, the US Centers for Disease Control and Prevention, the Ministry of Health of El Salvador, the World Bank, the Training Programmes in Epidemiology and Public Health Interventions Network and the Network for Research and Training in Tropical Diseases in Central America (NeTropica) under the project No 06-R-2010.
Disclaimer The findings and conclusions in this paper are those of the authors, and do not necessarily represent those of the US Centers for Disease Control and Prevention.
Ethics approval Ethical review board of the Rosales National Hospital in San Salvador, and the US Centers for Disease Control and Prevention's Division of Global HIV/AIDS Chief of Science Office.
Provenance and peer review Not commissioned; externally peer reviewed.
Correction notice This article has been corrected since it was published Online First. The author name ‘Gabriela Paz Bailey’ has been corrected to ‘Gabriela Paz-Bailey’.
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