Shahmanesh M, Patel V, Mabey D, Cowan F. Effectiveness of interventions for the prevention of HIV and other sexually transmitted infections in female sex workers in resource poor setting: a systematic review. Trop Med Int Health 2008 May;13(5):659-79.
To systematically review the evidence for the effectiveness of HIV and sexually transmitted infection (STI) prevention interventions among female sex workers (SWs) in resource-poor settings
Published and unpublished studies were identified by searching electronic databases, doing hand searches, and contacting experts. Databases and dates searched included Cochrane controlled trial register and Cochrane database of systematic reviews (1998-2006); Medline (1966-2006); Embase (1980-2006); and Web of Science (1984-2006). Medline and Embase were searched using the Key Mesh terms and text words (in italics): (Prostitution OR prostitut* OR sex work*') AND (HIV OR HIV infection OR HIV seroprevalence OR HIV OR sexually transmitted disease OR sexually transmitted infection). The text words were used to search the other databases. A key non-indexed journal "Research for Sex Work" and references of review articles and selected studies were hand searched. Web sites of agencies involved in HIV prevention (UNAIDS, Family Health International, and Population Council) and conference abstracts found through Gateway and National Library of Medicine were searched. First authors and experts in the field were contacted to obtain information on unpublished work, forthcoming manuscripts, and research in progress. Unpublished studies and studies published in non-English language journals were considered for inclusion. Inclusion criteria were any intervention that intended to prevent HIV and STIs through targeting female SWs in resource-poor settings, and which was evaluated in an experimental (RCT) or quasi-experimental (controlled but without randomly assigned control groups, or time-series) study. Studies were excluded if they targeted male and transsexual SWs, were conducted prior to the advent of HIV, were based in resource-rich industrial countries, focused on harm reduction for injection drug users (IDUs), did not describe the intervention adequately, or had less than 6 months of follow-up.
Twenty-eight studies were included in the review, 25 individual interventions and three structural interventions, of which 26 were published and two were unpublished. Of 6,788 articles and 1,318 abstracts (including duplicates) identified across databases, plus 22 studies found by hand searching, searching websites and conferences, and contacting experts, 272 were potentially relevant. Only 75 of these 1,272 studies were HIV or STI interventions in female SWs in resource-poor settings. Inclusion criteria reduced the number to the 28 studies: 25 were conducted with SWs; one with couples (transactional and non-transactional sex partners) visiting a motel; two of interventions with high-risk women associated with mines and truck stops. Four studies evaluated the effect on clients. Sixteen (57%) of the studies were in Africa and the remainder were in Asia (n=8) and Latin America (n=5). Eleven (39%) studies were in dedicated SW clinics; the remainder were conducted in brothels (n=7), communities (n=7), motels (n=1) or truck stops (n=1). Eleven studies (39%) were RCTs, three of which were cluster RCTs. Seventeen (61%) studies were quasi-experimental, including uncontrolled before-and-after studies (n=11), studies with a non-randomized control arm (n=3), or a combination of both types of study (n=3).
Study participants were limited to female SWs, defined as women who exchange sex for money or other gifts and commodities. The studies included a total of 49,807 participants: 27,445 female SWs; 1,779 clients; 37 brothel owners; 6,463 couples; 330 high-risk women; 1,668 community men, women, and miners; 1,536 miners; and 4,086 military conscripts.
Seven studies (25%) evaluated interventions to increase condom use. Four (14%) evaluated the efficacy of the vaginal microbicide nonoxinol-9 (N-9). Fourteen (50%) evaluated a combination of a behavioral intervention and STI treatment, six of which were able to separate out the effectiveness of adding the STI treatment component. Three (11%) structural interventions were multifaceted, with improved STI care and an enabling atmosphere for risk reduction, either through community mobilization or political or legal sanction.
Studies were included only if they reported at least one outcome measure that could be externally validated, such as biological outcomes (HIV incidence and/or STI incidence/prevalence), or measurable health outcomes (e.g., condom disposal, health service utilization). Twenty-six (93%) studies assessed changes in incident or prevalent HIV or STIs, of which 12 measured HIV incidence. Other outcomes were verifiable measures of condom use, such as provision, disposal, or use with simulated clients (n=4), and service utilization (n=2). Self-reported condom use measures were not included. The heterogeneity of the interventions precluded a formal meta-analysis with a single summary outcome measure.
Four broad categories of interventions were identified: behavioral interventions with condom promotion, addition of vaginal microbicide, addition of STI treatment, and structural interventions. The evidence suggested that behavioral interventions with condom promotion had some effectiveness, that vaginal microbicides were not effective or increased risk, that periodic STI screening did not show evidence of effectiveness, and that structural interventions (policy and legal changes) showed some evidence of effectiveness.
Risk reduction counseling coupled with condom promotion reduced HIV or STI risk or increased condom use in all of the five studies that tested this hypothesis. Only two were RCTs of the combined effect of behavioral intervention with condom promotion. Only one study that was not a random-cluster clinical trial found a reduction in incident HIV. Despite the methodological limitations of these studies, the consistency of the direction of change; the dose response; the association among participation in the intervention, self-reported condom use, and reduced infection rates; and biological plausibility suggest that this is an effective strategy. Two studies assessed female condom promotion and showed an increase in female condom uptake.
Four placebo-controlled RCTs of the vaginal microbicide N-9 showed either no effect or an increased risk of HIV.
Three RCTs tested different STI treatment strategies. The two studies with an HIV incidence outcome, one with presumptive periodic treatment (PPT) and the other with regular screening, found no effect, although follow-up was less than 50% in one study. The third RCT, which used PPT, showed a significant reduction in bacterial STIs. That study detected a sample size problem from declining rates in both treatment arms and lengthened the enrollment period accordingly. One quasi-experimental study suggested that increasing the interval between rounds of PPT may lessen its effect on STI prevalence.
Seven structural interventions were included from Thailand, India, and the Dominican Republic. These interventions involved government-supported condom programs, media campaigns, sanctions or cost-benefit for brothels, STI treatment, peer educators, and empowerment through collective bargaining, self-organization, legal advice, and other services. Thailand's 100% condom use program was a countrywide, multi-component intervention that sought to increase condom use, reduce the number of commercial sexual encounters, and improve provision for STI treatment. Although reductions in STIs were observed in men and new military recruits, it is impossible to disentangle the effect of the different components of the intervention from each other or from secular trends. The only controlled study among the seven was the Dominican Republic's comparison of a regional policy change with sanctions against brothels for not enforcing 100% condom use, with SW empowerment, improved STI care, and self-regulation of brothels. Brothels were more likely to adhere to 100% condom use in the policy change area.
Over half of the studies that followed SWs reported attrition rates as high as 75%, compromising the validity of the outcomes.
Given the small number of effective studies, the authors were unable to explore the relationship between phase of the epidemic and effectiveness of the intervention. Given the complexity and multifaceted nature of the interventions, indicators of exposure to the intervention would have assisted interpretation. Unfortunately, the indicators to measure exposure commonly reported, such as number of clinic visits or educational events attended, also are measures of adherence. In the absence of controls, finding an association between these measures of exposure and outcomes may be confounded by other factors associated with being an "adherent" participant in disease prevention. Few of the cluster-controlled trials accounted for intercluster correlation in either the power calculation or the analysis stage, possibly resulting in a greater measure of effect than if clustering had been considered.
The authors concluded that none of the RCTs showed an effect on HIV incidence. However, the observational data suggest some evidence for the effectiveness of risk reduction counseling, condom promotion, and regular access to improved STI management in SWs. The methodological challenges to conducting studies in such a clandestine and mobile group suggest that caution should be exercised when interpreting the results. There is no unequivocal evidence that intensive STI management in SWs has any additional benefit in HIV prevention. The lack of effect on HIV from the RCTs of STI treatment could be due to a loss of power from reductions of STI rates in both arms of the studies (type II error). Innovative STI delivery methods, such as vouchers, may improve coverage. There is some evidence that policy support for SW interventions as well as strategies that empower the women improve coverage, acceptability, and adherence to the intervention.
The authors conducted a comprehensive search of the international literature by searching databases, contacting authors, and searching the "gray literature." Using the QUOROM checklist for systematic reviews, this was a well-conducted and thorough systematic review. However, the authors did not describe the data abstraction process (e.g., whether data abstraction was conducted independently and in duplicate) nor the criteria and process used to assess validity. Heterogeneity of the studies did not allow the authors to conduct a meta-analysis nor to construct a funnel plot to assess publication bias, yet it is likely that there was such bias. Although some RCTs were unable to show an effect, almost all quasi-experimental studies reported statistically significant findings in favor of the intervention being tested. Even within the gray literature there is potential for selection bias, as interventions funded or sanctioned by the larger donors are more likely to be accessed through UNAIDS, FHI, or Population Council reports and best practice publications. As in all systematic reviews, despite extensive hand searching, there is still the possibility of indexing bias. The review was restricted to evaluated interventions that had externally validated outcome measures. This may have excluded less rigorously evaluated but nevertheless important and potentially effective interventions. A limitation of this systematic review is that only interventions that involved women who exchange sex for gifts or money could be included. This criterion means that potentially effective interventions with high-risk women, such as bar workers, who were not explicit about the transactional nature of their sexual behavior, were excluded.
This is the first systematic review of HIV and STI prevention interventions in female SWs in resource-poor countries. Two important position papers have sought to summarize key strategies for HIV prevention in SWs. One approached HIV as an occupational hazard, advocating harm reduction strategies such as empowering SWs to use condoms and removing structural barriers to safety.(1) The other examined strategies to provide STI treatment for SWs and concluded that using presumptive periodic treatment with single dose antibiotics, followed by regular algorithm-driven screening, was likely to be the most effective strategy.(2) The effectiveness of either approach for SWs has not been assessed systematically. A systematic review of STI prevention interventions not specifically targeting SWs found that just over half of 41 interventions identified were effective at reducing STIs.(3) Authors of a systematic review of structural facilitators and barriers to HIV prevention suggested addressing macro-social determinants of risk, such as economic policy, migration, gender inequality, and sex work legislation.(4)
Mathematical models indicate that targeting core groups such as SWs is an effective way to reduce HIV transmission, particularly in the early and accelerated phase of the epidemic. Given the scale of sex work, with incomes equivalent to 2-14% of Southeast Asia's gross domestic product, there is an urgent need to identify which interventions are effective in reducing HIV in SWs. Overall, the evidence to show a reduction in HIV transmission was largely lacking, although a number of observational studies found that combining sexual risk reduction, condom promotion, and improved access to STI treatment showed improvements in condom use and STI prevalence or incidence that should lead to reduced HIV transmission. Strong evidence that regular STI screening or periodic treatment of STIs confers additional protection against HIV was lacking. There is still uncertainty about what is the best STI treatment strategy for SWs and the efficacy of STI treatment in HIV prevention. It appears that structural interventions, policy change, or empowerment of SWs may reduce the prevalence of STIs and HIV, but what components of structural interventions work and the potential negative ramifications of targeting SWs (e.g., stigma, violence, driving sex work underground) are not known. In addition, there is limited data available on the wider public health benefits of targeting SWs. There is a need to explore the effectiveness of comprehensive HIV care packages for SWs, new microbicides, HSV-2 prophylaxis, and pre-exposure prophylaxis. Evaluations of interventions that reach community-based SWs who work outside brothel-based settings and "red-light" districts also are required.
- Rekart ML. Sex-work harm reduction. Lancet 2005;366:2123-34.
- Steen R, Dallabetta G. Sexually transmitted infection control with sex workers: regular screening and presumptive treatment augment efforts to reduce risk and vulnerability. Reprod Health Mat 2003;11:74-90.
- Manhart LE, Holmes KK. Randomized controlled trials of individual-level, population-level, and multilevel interventions for preventing sexually transmitted infections: what has worked? J Infect Dis 2005;191(Suppl. 1):S7-S24.
- Parker RG, Easton D, Klein CH. Structural barriers and facilitators in HIV prevention: a review of international research. AIDS 2000;14(Suppl. 1):S22-32.