Systematic review of HIV prevalence studies among key populations in Latin America and the Caribbean

Revisión sistemática de estudios de prevalencia del VIH en poblaciones clave de mayor riesgo en América Latina y el Caribe

William Meihack Miller, MPH^I; Lindsay Buckingham, BA^II; Mario Salvador Sánchez-Domínguez, MvD, MSc^III; Sonia Morales-Miranda, MVD, MSc^I; Gabriela Paz-Bailey, MD, MSc, PhD.^{I, II, IV}

^IUniversidad del Valle de Guatemala. Guatemala
^IISchool of Medicine, University of North Carolina at Chapel Hill. North Carolina, USA ]]> ^IIIInstituto Nacional de Salud Pública. Cuernavaca, Morelos, México
^IVTephinet, Inc. Guatemala

Corresponding author

ABSTRACT

OBJECTIVE: This systematic review aims to synthesize articles, abstracts and reports of HIV prevalence studies conducted among men who have sex with men (MSM) and female sex workers (FSW) in Latin America and the Caribbean (LAC).
MATERIALS AND METHODS: Authors searched online databases and collected gray literature on HIV prevalence among MSM and FSW from LAC. Year, location, sampling methodology, study design, sample size, HIV prevalence and confidence intervals were abstracted.
RESULTS: A total of 73 studies, dating from 1986 to 2010 were included.The median prevalences for MSM and FSW were 10.6% (interquartile range: 7.4- 17.4) and 2.6% (IQR: 0.6 -4.2), respectively. Variability was high, especially for MSM. The majority of studies recruited participants using convenience methods.
CONCLUSION: HIV prevalence among MSM was higher than that among FSW. Sampling techniques should be standardized for future studies, prioritizing probability methods.

RESUMEN

OBJETIVO: Esta revisión sistemática tiene el objetivo de sintetizar artículos, resúmenes y reportes de estudios de prevalencia de VIH en hombres que tienen sexo con hombres (HSH) y mujeres trabajadoras sexuales (MTS) en América Latina y el Caribe (ALC).
MATERIAL Y MÉTODOS: Se realizaron búsquedas en bases de datos electrónicas y se recopiló literatura gris sobre la prevalencia de VIH en HSH y MTS de América Latina y el Caribe. Los datos recolectados fueron año, lugar, metodología de muestreo, diseño del estudio, tamaño muestral, prevalencia de VIH e intervalos de confianza.
RESULTADOS: Se incluyó un total de 73 estudios, realizados de 1986 a 2010. La mediana de la prevalencia para HSH y MTS fue 10.6% (rango intercuartil: 7.4- 17.4) y 2.6% (RIC: 0.6-4.2), respectivamente. La variabilidad de las prevalencias estimadas fue alta, especialmente para HSH. La mayoría de estudios usaron muestras por conveniencia.
CONCLUSIONES: La prevalencia de VIH entre HSH es superior a MTS. Los métodos muestrales deben ser estandarizados para estudios futuros, priorizando métodos probabilísticos.

Palabras clave: VIH; poblaciones vulnerables; América Latina; región del Caribe

HIV/AIDS continues to be a pressing public health problem around the world. The Joint United Nations Programme on HIV/AIDS (UNAIDS) recently reported that in 2010 33.3 million people were infected, while in 2009 1.8 million deaths occurred as a result of HIV worldwide. Since new infections peaked in 1999, UNAIDS estimates a 19% decrease in new infections globally, with increases witnessed principally in several countries in Eastern Europe and Central Asia. Based on data from 120 countries, 2.6 million new infections were estimated to have occurred in 2009.^1,2

Data on the incidence and prevalence of HIV and other STI among MSM are very poor in most of the developing world.⁶ Even in countries where more information is available, the contribution of homosexual behavior to the HIV/AIDS epidemic is not fully appreciated, in part due to either a lack of data or lack of analysis of the available data.⁷ A number of more detailed epidemiological studies have shown that same sex behavior is more common and the HIV prevalence among MSM is higher than previously thought.^8-10 In urban centers of Latin America, HIV prevalence has remained high among MSM, even as the epidemic has expanded to other populations.¹¹

FSW have lower reported HIV prevalence than MSM but are still one of the key populations for HIV and STI transmission in Latin America and the Caribbean due to the large proportion of men who visit sex workers (2.5%-6.5%).¹² Clients of FSW have sex with members of both high risk (FSW) and low risk (wives, regular partners) female populations.¹³ HIV/STI transmission networks are thus formed between populations at higher and those at lower risk, allowing for transmission of HIV and other STI between FSW and their partners, as well as transmission of STI among FSW. Given their central role in the epidemiology of HIV and other STI in Latin America, FSW must also be a major focus of HIV/STI surveillance and control efforts.

In response to differentiated epidemiological characteristics of the pandemic, UNAIDS recommends differentiated national strategic plans attuned to the situation in each country.¹⁴ A principal difficulty in creating such proposals, however, is the availability of accurate information on different sub-populations or widely varying estimates for the same country.¹⁵ Considering the mix of available information, we conducted a systematic review of the HIV prevalence among different key populations in Latin America and the Caribbean to gain a greater understanding of the epidemiologic profile in the region and help inform strategies in response to the HIV epidemic.

Materials and methods

This systematic review aims to synthesize articles, abstracts and reports of HIV prevalence studies conducted among key populations in Latin America and the Caribbean. From May to October, 2010, two independent investigators conducted searches of the PubMed and National Library of Medicine's meeting abstract databases for published articles and abstracts using the following key words: highrisk groups; female sex workers; men who have sex with men; homosexual men; HIV; prevalence; Latin America; and individual country names. Reference listings from previous reviews and papers were also used to identify original articles, conference proceedings and reports. "Gray literature," most often in the form of study reports, was included based on the knowledge of coauthors. We considered peerreviewed articles, abstracts and documents published up to September 2010.

Eligibility criteria

Publications were assessed based on target population, location, year, sampling methodology, sample size and language. Inclusion criteria for studies were determined a priori to be: studies including HIV prevalence data among MSM or FSW; publication in a peer-reviewed journal, country report or an abstract at a conference with peer-reviewed blinded abstract selection process; studies from the Latin American and Caribbean regions. Inclusion criteria for studies among FSW included ex-changing sex for money or goods in different periods (i.e.: last month, last six months and last year). Inclusion criteria for MSM included anal or oral sex with another man, recall periods varying (i.e.: last month, last six months and last year). Studies in English, Spanish and Portuguese published between 1986 and 2010 were included in the review.

Exclusion criteria were studies with 100 or fewer participants and studies that combined participants from the target populations with other populations such as clients of FSW. When multiple reports existed for a single study, one paper was chosen based on completeness of the information. Only original research articles and reports were taken into account for this study, ex-cluding those reported in a review for which we could not locate the abstract, original paper or report. Authors kept records of all excluded publications.

We created a master table in Microsoft Excel (Redmond, WA, USA), extracted key information from included surveys, and entered data into the table. We extracted 1) the first author; 2) the year of the study; 3) survey location; 4) sampling methodology; 5) study design; 6) inclusion criteria; 7) sample size; 8) HIV prevalence; and 9) respective confidence intervals. When unavailable in the selected publications, confidence intervals were calculated assuming a simple random sample: this included 48 studies among MSM and 38 studies among FSW.

City estimates were reported as separate data points if the study presented the prevalence disaggregated by city. We originally arranged sampling methodologies into seven categories: unspecified convenience; snow-ball convenience; institutional convenience; cluster sampling including time-location sampling (TLS); stratified random sampling; census; and respondent-driven sampling (RDS). Institutional samples included those recruited at HIV testing, sexual/reproductive health, STI treatment and community centers. Institutional samples were presented as convenience samples in tables I, II and III. More recent data from 2000 to 2010 were summarized in a graph (figure 2).

Results

A total of 2 566 conference abstracts and 3 983 articles abstracts were originally identified. Of those, 2 539 conference proceedings and 3 876 articles were excluded because they were not from Latin America or the Caribbean, were out of scope or because they lacked an HIV prevalence estimate. One hundred and thirty-four records were deemed relevant by any reviewer and marked for full-text retrieval. Of those, 84 more were excluded due to duplicated data or sample size less than 100 (figure 1). Twenty- three studies considered gray literature were added to relevant peer-reviewed studies and conference papers for a total of 73 studies.

Men who have sex with men

Forty-eight studies screened 60 421 MSM (sample size range 102-7 041; median 306) and provided 78 population-and city- specific data points. Studies were published between 1988 and 2010. Data points were available from 19 countries. Most sites were large metropolitan centers. Studies were mostly cross-sectional, with the exception of six prospective cohort studies in four cities in South America and one Caribbean island. Recruitment venues included HIV testing clinics, medical and community-based organizations serving MSM, street locations, and social and workplace venues. The majority (77.1%) of studies was conducted using convenience sampling, and often a combination of techniques (advertising, active recruitment, HIV/STI testing centers, snowball, etc.) was used to reach the desired sample size. There were seven (14.6%) that used RDS, most of these in Central America, three (6.3%) cluster designs and one (2.1%) stratified random sample (table I). RDS studies were first reported in 2008. In countries where both RDS studies and convenience samples were conducted, there was a tendency for RDS studies to report lower HIV prevalence, though differences were not statistically significant based on confidence intervals.

A few studies reported HIV incidence. In Brazil, three cohort studies were implemented in the cities of Rio de Janeiro, Sao Paulo and Belo Horizonte which found incidence rates of 3.1, 1.5 and 2.0 per 100 person years, respectively.^18,19 In Peru, 1 140 men followed up between 1998 and 2000 yielded a seroincidence rate of 3.5 per 100 person years.²⁰ The BED assay has also been used to estimate incidence in cross-sectional studies reporting a range of 2.1-14.4% (95%CI: 5.4-29.7) in Central America⁴ and 11.2% in Peru.²¹

Female sex workers

Forty-three prevalence studies surveyed 76 416 female sex workers (sample size range 101-24 500; median 265) and included 86 data points. Studies were published between 1986 and 2010 from 18 countries. Sites included capitals, ports and other tourist and commercial centers. The highest sample size, 24 500 was reached in Mexico (0.3% HIV prevalence), where women were recruited from HIV testing sites at health units across the country.²² Cross-sectional studies predominated with the exception of one prospective cohort study. Recruitment venues included HIV testing clinics, medical and community-based organizations serving FSW, street locations, and social and workplace venues. Most studies (77.3%) used convenience sampling with the exception of six (13.3%) cluster designs, four (8.9%) RDS and one (2.2%) census (not exclusive; some studies used different sampling methods in different cities).

RDS studies were first reported for FSW in 2009. Studies from Central America were more often conducted using RDS than those from other regions. FSW were sampled using probability methods more frequently than MSM, though the difference was small.

HIV prevalence ranged from 0% in parts of Honduras, Nicaragua, Panama, Uruguay, Chile, Bolivia, Peru and Venezuela (conducted between 1986 and 2006)*^,23-30,121 to 12.4% in Haiti (1987-1988)³¹ with a median of 2.6% (IQR: 0.6-4.2) (table III). HIV prevalence among FSW by region and country from 2000-2010 are presented in figure 2. The data points showed lower prevalence and less variability than for MSM.

Discussion

Traditionally, the highest HIV prevalence among MSM have been reported in Mexico and the Andean countries. However, in the last 10 years the prevalence in Mexico appears to have decreased or studies have recruited a more heterogeneous sample and recent levels are similar to those reported in Central America. For FSW, the disease burden was greatest overall in Brazil, though recent rates were also lower than those from a decade ago. Taking into account the studies in this review, HIV prevalence among MSM was five times higher than among sex workers. HIV seroprevalence studies of other potentially key populations from Latin America and the Caribbean were lacking, and based on previous reviews men who have sex with men and female sex workers have proven to be the populations most affected by the HIV epidemic in countries across the region.^3,32-36

One of most apparent characteristics regarding the prevalence among MSM, especially evident in the Andean region, was the high degree of variability among studies from different countries but also from the same country. This could be due to the different sampling methods used to recruit MSM. Few studies with probabilistic sampling methodologies had been carried out in the region. Furthermore, it is possible that researchers chose probability methods to sample female sex workers more often than for MSM on the assumption that the entire FSW population works from establishments that can be mapped and cluster sampled. In the U.S. venue based sampling has been used to conduct ongoing HIV behavioral surveillance among MSM,³⁷ but in Latin America researchers have not opted for venue-based methods. In fact, the majority of articles were based on convenience methods, often combining snowball recruitment, out-reach referrals or advertisement methods. There are several possible explanations for this observation. MSM in Latin American countries might have been more difficult to recruit in venues compared to the U.S. due to lower social tolerance of sexual diversity and higher levels of stigma and discrimination. This could have resulted in insufficient number of MSM venues and safety concerns for field staff operating in dangerous areas. The high degree of convenience sampling and inclusion of larger proportions of MSM sub-populations at even higher risk such as male sex workers could have caused the large degree of variability on HIV prevalence among the MSM studies. Another explanation for the variability among studies is that RDS has been thought to produce lower seroprevalence estimates than other methods assuming that it reaches hidden segments of the target population, individuals who may have been sheltered from a lifestyle propitious to high rates of transmission.

Several approaches have been proposed to balance the need for recruitment efficiency and inclusiveness in representation. Snowball sampling increases efficiency, identification, and inclusion of hidden populations by having members of the target population recruit other members.⁴⁵ However, snowball sampling suffers from sampling bias and leads to a group that is not representative of the population. Facility-based sampling is also not generalizable as those who obtain services are different from those who do not. Targeted sampling involves an ethnographic mapping of the target population to later sample subgroups as strata. The magnitude of the bias in targeted sampling depends on the thoroughness of the ethnographic assessment. Time-location sampling involves an ethnographic mapping of sites where the target population meets or works and random selection of participants at randomly selected sites, days and times. Time-location sampling is a probability sampling method but as with targeted sampling, its representativeness depends on the exhaustiveness of the mapping and assistance of all population subgroups at selected sites. Nevertheless, TLS has worked well with more visible populations including female sex workers and their clients,^46,47 and MSM in gay-identified areas of urban centers.^48,49

Respondent-driven sampling has been used for surveillance of populations most at risk for HIV/AIDS in the United States and in more than 83 countries worldwide since 1994.^50,51 In theory, weighted estimates generated from RDS generalize to the population as a whole. However, recent assessments of the RDS sampling methodology have documented limitations in the RDS assumptions.^52,53 Despite these limitations, RDS is currently one of the only methods available to reach highly hidden populations that provides methodological rigor.

This review has several limitations. The use of different sampling methodologies diminished the validity of pooled prevalence estimates and only medians were presented as summary estimates in this paper. Calculated asymptotic confidence intervals were tighter than the true intervals, limiting the interpretability of the data. More recent studies may not have been included due to the lag time between data collection and publication of results. The inclusion of gray literature may also have been biased by the authors' geographical expertise or familiarity. Different types of laboratory tests were used to diagnosis HIV, including rapid tests, ELISA, and Western Blot among others. Information on the types of tests, specific tests or diagnostic algorithms was not always available for the included studies. This variability and lack of information limited the ability to compare the results from different studies. Medians and interquartile ranges (IQR) were reported and should be interpreted with care due to the different recruitment methodologies. For the same reason, trend analyses have not been presented in this article.

High prevalence rates among MSM and moderate rates among FSW have been detected in countries across Latin America and the Caribbean. A toolbox of standardized sampling techniques and data collection practices is urgently needed to clear up the varied picture presented by studies in this review. While many researchers continue to question the generalizability of RDS and TLS samples, it is encouraging that researchers are employing probability sampling methods more often than in the past. The implications of this study for prevention include recognizing that in Latin America and the Caribbean sufficient resources should be dedicated to HIV programs for men who have sex with men and sex workers to slow or stop transmission. Historical stigma attached to these key populations and their perceived or estimated population size in comparison to other populations influence decision makers. Widespread efforts are needed to ensure that leaders are aware of the results and that resources are allocated based on burden of disease and prevention needs.⁵⁴ Periodic surveillance of MSM, FSW and other populations important to the HIV epidemic should continue.

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Corresponding author: ]]> William Miller. 6 Jordan Dr., Pittsboro, NC 27312 USA
E-mail: meihackmiller@gmail.com

Received on: February 11, 2011
Accepted on: July 10, 2012