Articles
Burden of HIV among female sex workers in low-income and middle-income countries: a systematic review and meta-analysis

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Summary

Background

Female sex workers are a population who are at heightened risk of HIV infection secondary to biological, behavioural, and structural risk factors. However, three decades into the HIV pandemic, understanding of the burden of HIV among these women remains limited. We aimed to assess the burden of HIV in this population compared with that of other women of reproductive age.

Methods

We searched PubMed, Embase, Global Health, SCOPUS, PsycINFO, Sociological Abstracts, CINAHL (Cumulative Index to Nursing and Allied Health Literature), Web of Science, and POPLine for studies of female sex workers in low-income and middle-income countries published between Jan 1, 2007, and June 25, 2011. Studies of any design that measured the prevalence or incidence of HIV among female sex workers, even if sex workers were not the main focus of the study, were included. Meta-analyses were done with the Mantel-Haenszel method with a random-effects model characterising an odds ratio for the prevalence of HIV among female sex workers compared with that for all women of reproductive age.

Findings

Of 434 selected articles and surveillance reports, 102 were included in the analyses, representing 99 878 female sex workers in 50 countries. The overall HIV prevalence was 11·8% (95% CI 11·6–12·0) with a pooled odds ratio for HIV infection of 13·5 (95% CI 10·0–18·1) with wide intraregional ranges in the pooled HIV prevalence and odds ratios for HIV infection. In 26 countries with medium and high background HIV prevalence, 30·7% (95% CI 30·2–31·3; 8627 of 28 075) of sex workers were HIV-positive and the odds ratio for infection was 11·6 (95% CI 9·1–14·8).

Interpretation

Although data characterising HIV risk among female sex workers is scarce, the burden of disease is disproportionately high. These data suggest an urgent need to scale up access to quality HIV prevention programmes. Considerations of the legal and policy environments in which sex workers operate and actions to address the important role of stigma, discrimination, and violence targeting female sex workers is needed.

Funding

The World Bank, UN Population Fund.

Introduction

Epidemiological surveillance data have shown declines in the rate of spread of HIV from an estimated 3·1 million (95% CI 3·0–3·3) new infections in 2002 to 2·7 million (95% CI 2·4–2·9) new infections in 2010.1 UNAIDS estimates that over the past decade, 33 countries—including 22 sub-Saharan African countries—have achieved declines in HIV incidence of more than 25%.2 These decreases highlight overall advances in the fight against HIV, but might mask sustained or expanding spread among populations who are most at risk including sex workers, men who have sex with men (MSM), and people who use drugs.2 In much of the world, HIV epidemics are most concentrated in populations who are most at risk,1 and where HIV epidemics occur in general populations, largely in sub-Saharan Africa, these populations might still have very high disease burdens relative to others.3, 4, 5, 6 Unfortunately, our understanding of the burden of HIV in populations who are most at risk is poor, largely because these populations are poorly represented in national HIV surveillance systems and are hidden and stigmatised in many settings. Female sex workers have been reported to be at high risk for HIV infection in nearly every setting where they have been studied, yet in 2012 we still have limited understanding of the relative burden of HIV in these women.

Sex work—defined here as the exchange of sex for money—and the structure of sex work vary substantially around the world. Those who sell sex might work with or without a controller (eg, pimp, manager) through establishments such as bars, brothels, or saunas, or in more public spaces such as parks, streets, or festivals. Additionally, a growing portion of sex work is arranged through the internet.7, 8 Most sex workers worldwide are women; however, substantial populations of male and transgender sex workers exist in many countries.9 The dynamics of HIV transmission among male and transgender sex workers could be further complicated by the heightened biological risks of anal intercourse, high prevalence of HIV in some subgroups of MSM, and the large proportion of male and transgender sex workers who report bisexual practices.9

HIV infection in female sex workers varies by geographical epidemic typology, structure of sex work, and overlapping nature of HIV-risk behaviours such as injection drug use. Yet the heightened risk for HIV acquisition and transmission among sex workers operates through a similar variety of behavioural, biological or biomedical, and structural risks.10, 11 Behavioural risk factors act at the level of the individual, with sex workers experiencing high-risk sexual exposures through high numbers of sexual partners and high concurrency of these partners. Biologically, the high prevalence of bacterial sexually transmitted infections (STIs) in sex workers12 and the synergistic relation between HIV and STIs13 compounds their risks and could lead to complications around reproductive health and childbearing.14, 15, 16 In some settings, protective sexual practices including consistent condom use and HIV testing are higher among sex workers than among women in the general population,2, 7 although these rates remain low in many areas.17 HIV transmission among sex workers might also be driven, or exacerbated, by the intersection of injection drug use and sex work through increased parenteral exposures from shared injection equipment, sex with more HIV-positive partners, low condom use, and increased risk of other STIs such as syphilis and hepatitis C.17, 18, 19

Structural risk factors indirectly heighten risk for HIV infection among sex workers by restricting access to preventive health and HIV and STI services and treatment.7, 20, 21 Structural factors also include the limiting influences of poverty, discrimination, and gender inequality as well as the damaging effects of physical and sexual violence, stigma, and social exclusion.22, 23, 24, 25 Finally, structural factors such as the organisation and power dynamics of sex work and legal and regulatory policies regarding sex work have also been shown to contribute to sex workers' increased risk of HIV infection by limiting their ability to negotiate safer sex.26, 27, 28, 29 Health enabling environments, including safer work spaces, structural support for condom promotion and distribution, and community empowerment for sex workers have been shown to reduce structural risks for HIV infection.22, 30, 31, 32, 33, 34

Interventions targeting behavioural and structural-level risk factors for HIV among sex workers have proven successful for increasing protective behaviours and decreasing HIV and STI transmission.35, 36, 37 In fact, 44 of 87 countries with available data report that over 80% of sex workers used condoms with their last client.2 Despite these promising results and increasing number of initiatives, UNAIDS estimates that less than 50% of sex workers worldwide are covered by ongoing HIV prevention programmes.2 In view of this urgent need for HIV prevention and treatment among sex workers, there is still a lack of crucial information to guide global resource investment because most meta-analyses are limited to a single country or area.38, 39, 40, 41 Systematic reviews and meta-analyses have been undertaken in other populations who are most at risk, including MSM and people who use drugs, to better characterise the relative burden of HIV to background rates.3, 4 To date, however, such a review has not been completed for female sex workers, which is needed to better characterise the relative level of HIV risk among these women and to guide the allocation of resources and content of HIV prevention programmes and policies. The aim of this study is to characterise current burdens of HIV in female sex workers.

Section snippets

Search strategy and selection criteria

We searched PubMed, EMBASE, Global Health, SCOPUS, PsycINFO, Sociological Abstracts, CINAHL (Cumulative Index to Nursing and Allied Health Literature), Web of Science, and POPLine for studies published between Jan 1, 2007, and June 25, 2011. Articles and citations were downloaded, organised, and reviewed using the QUOSA information management software package (version 8.05) and EndNote (version X4). The search included MeSH terms for HIV or AIDS, and terms associated with sex work (prostitute

Results

Our search criteria identified 19 180 citations, of which 2240 were unique records (figure 1). Of 434 selected articles and surveillance reports, data from 102 met inclusion criteria. These studies included 91 articles and 11 surveillance reports representing 99 878 female sex workers in 50 countries: 14 countries in Asia, four in the eastern Europe, 11 in Latin America and the Caribbean, five in the Middle East and north Africa, and 16 countries in sub-Saharan Africa (figure 1, table 1).

The

Discussion

We identified consistent evidence of substantially higher levels of HIV among female sex workers compared with all women of reproductive age in low-income and middle-income countries in all regions with data. Although female sex workers have long been understood to be a key affected population, the scope and breadth of their disproportionate risk for HIV infection had to date not been systematically documented.

The largest sample size was available from Asia (table 1), where we reported the

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