Abstract
This study aims to evaluate condom use, sexually transmitted infection (STI) screening, and knowledge of STI symptoms among female sex workers in Peru associated with sex work venues and a community randomised trial of STI control. One component of the Peru PREVEN intervention conducted mobile-team outreach to female sex workers to reduce STIs and increase condom use and access to government clinics for STI screening and evaluation. Prevalence ratios were calculated using multivariate Poisson regression models with robust standard errors, clustering by city. As-treated analyses were conducted to assess outcomes associated with reported exposure to the intervention. Care-seeking was more frequent in intervention communities, but differences were not statistically significant. Female sex workers reporting exposure to the intervention had a significantly higher likelihood of condom use, STI screening at public health clinics, and symptom recognition compared to those not exposed. Compared with street- or bar-based female sex workers, brothel-based female sex workers reported significantly higher rates of condom use with last client, recent screening exams for STIs, and HIV testing. Brothel-based female sex workers also more often reported knowledge of STIs and recognition of STI symptoms in women and in men. Interventions to promote STI detection and prevention among female sex workers in Peru should consider structural or regulatory factors related to sex work venues.
Introduction
Female sex workers (FSWs) are a vulnerable population at high risk for acquisition of sexually transmitted infections (STIs). 1 They have also been considered a bridge group in terms of transmission of STIs from high-risk to general populations.2–5 They represent a key target population for promotion of health care-seeking for STI diagnosis, treatment, and prevention interventions. However, FSWs are often marginalised, isolated, and difficult to reach for intervention in many settings because sex work is illegal and covert in most countries, and sex workers are not always readily identifiable as such. Many FSWs are reluctant to self-identify for fear of violence or persecution by authorities.6–8
There is an increasing body of evidence that demonstrates that multi-component interventions including peer support, condom promotion, and access to STI screening services are associated with decreased STI prevalence and improved condom use among sex workers.9–14 While clinic-based screening interventions are effective, engaging FSWs to access clinic-based services in the context of fear of persecution, lack of knowledge and stigma is a challenge. 15 And while outreach sites may engage FSWs outside of clinics, they often lack the scope to address the diversity of reproductive health issues experienced by FSWs. 14 Few studies address FSWs’ linkage to and engagement in formal health care services. Furthermore, among community-based intervention studies, few are randomised trials.
Interventions that promote health care-seeking behavior as a component of a causal pathway toward improving biological endpoints can be placed within a broad conceptual framework that includes processes and factors operating at individual, socio-cultural, geographical, demographic, economic, and other structural levels.16,17 While individual factors such as higher education and knowledge of STIs are protective against HIV/STI acquisition, 18 structural interventions such as community mobilisation, venue-based support, or empowerment efforts have been identified as being promising mechanisms for decreasing FSW STI risk and improving linkage to health services.14,19 It is important, therefore, to understand not only individual knowledge and demographic factors related to health-seeking behavior, but to also assess the association between structural factors and STI-related health care-seeking behaviors.
The present analysis was undertaken as a component of the Peru PREVEN Study, in which 20 cities with populations >50,000 underwent pair-wise randomisation to a multi-component STI intervention that included mobile team-based FSW outreach. 20 Pre-intervention baseline analyses for the PREVEN study demonstrated that self-medication, or treating oneself in the absence of medical advice, for symptomatic STIs was less likely among FSWs who reported being aware of STI services and those based at brothel venues. 21 This present analysis further aims to evaluate uptake of health screening and HIV/STI preventive behaviors among FSWs in mid-sized cities in Peru, regardless of symptoms, associated with the community-randomised trial intervention. A second analysis further assesses screening outcomes associated with sex work venues.
Methods
Study design
The Peru PREVEN study was a community randomised trial conducted between 2003 and 2006 in medium-sized cities in Peru. Trial methods have been previously described elsewhere.20,22 The primary study endpoints determined in 2006 were combined prevalence of the major curable STIs in the general population and among FSWs. 20 The PREVEN multi-component HIV/STI intervention consisted of three key components: strengthened STI syndromic management for the general population; mobile team outreach to FSWs; and condom promotion among the general population and FSWs. Training of clinicians and pharmacy workers, and a health communication campaign on STI recognition and care-seeking, were implemented in the general population in 2005 to support syndromic management.
The mobile team component aimed to increase condom use and increase care-seeking for screening, diagnosis, and treatment of STIs among FSWs. 23 Each outreach team was led by a health professional and an FSW peer educator, and later visit cycles included a counsellor. Intervention sites including brothels, bars, and street venues were identified continuously via key informant interviews. Each intervention cycle was eight weeks long, during which the mobile team visited every identified sex work venue in the city. In addition to presumptive periodic treatment with metronidazole 2 g orally every two months for trichomoniasis and/or bacterial vaginosis, counselling was provided at each visit and included promotion of condom use, information on STI symptom recognition, and information about available government-provided health services.
Ethical considerations
This study was approved by the Institutional Review Boards at the University of Washington (16764), Universidad Peruana Cayetano Heredia (99084), and the United States Naval Medical Research Center Detachment in Peru (NMRCD.2002.0016). The clinical trial registration number is ISRCTN43722548.
Data collection
Cross-sectional surveys were conducted among FSWs in intervention and control cities at baseline in 2002–2003, during 2005, and at the end of the intervention in late 2006. Interviews were conducted among women found offering sex services at increasing numbers of venues identified over the three-year intervention. These venues included street, brothel, and bar-based settings. FSWs who were 14 years of age or older and were willing and able to provide informed consent were included. Participation in previous surveys, including prior Peru-PREVEN surveys, did not preclude participation. Trained fieldworkers administered questionnaires through face-to-face interviews.
Definitions
For this analysis, outcomes of interest included seeking a periodic STI screening exam from a government health facility during the prior six months, HIV testing within the last year, and ability to describe symptoms of STIs in women and in men. Perceived risk of HIV is also included as it has frequently been included in conceptual models of health care-seeking behavior in terms of perceived threat of disease and need for medical support.16,24–26 Symptoms were free-listed by participants and recorded where answered correctly. The median number of correctly identified symptoms was summarised, and a binary variable denoting report equal to or more than median number of reported symptoms was computed. Symptoms included lower abdominal pain, vaginal discharge, foul-smelling discharge, burning or pain on urination, genital ulcers or sores, swelling in the groin, genital itching, and genital warts among women; and urethral discharge, burning or pain on urination, genital sores or ulcers, swelling in the groin, and genital warts among men. Self-reported condom use outcomes with most recent client and non-client were also assessed. Uptake of services for STI treatment among symptomatic FSWs will be presented in a separate manuscript.
Statistical analysis
Statistical analyses used data from the 2006 FSW surveys, adjusting for city-specific baseline values from the 2002 surveys in measurement of intervention effects. Descriptive categorical variables were presented as frequencies and continuous variables as medians and interquartile ranges (IQR). FSW characteristics associated with sex work venues were tested using Chi square analysis and non-parametric tests of the equality of medians. 27 Prevalence ratios for behavioral outcomes associated with the intervention were calculated using non-paired, multivariate generalised linear models (STATACorp, College Station, TX), utilising Poisson family with robust standard errors and accounting for clustering by city. Intervention analyses were adjusted for city-specific 2002–2003 baseline responses, age, and brothel venue, as there were a higher proportion of brothels in intervention than in control cities, and FSWs in control cities were significantly older. 20 A secondary ‘as treated’ analysis was conducted using report of receiving services or participating in activities with the PREVEN mobile team as an exposure variable. Analyses of outcomes associated with brothel venues used similar statistical methods, though did not control for baseline, but rather for hypothesised confounders of age, marital/cohabitation status, geographical region, alcohol use, education, randomisation arm, and city cluster.
Results
Population and sample
In all, 4156 FSWs were enrolled in 20 cities; 2063 from control and 2093 from intervention cities. Key demographic characteristics of the sample are described elsewhere. 22 Of the 4156 participants, 44% were located in coastal cities, 36% in highlands cities, and 20% in jungle cities. 21% of FSWs were brothel-based, 23% street-based, and 56% were bar- or nightclub-based. Median age at first paid sex was 21 years and median duration of sex work was 20 months. Sex work was relatively frequent, with a median of six days worked in the last week, four weeks in the last month and eight months in the last year. Frequency of sex work increased with age (p < 0.001). FSWs reported a median of nine paying sex partners within the last week and two clients on the last day of work. Approximately 30% reported a source of income other than sex work.
FSW characteristics and venue of sex work
Characteristics of female sex workers (FSWs) by venue of sex work (2006 Survey).
Intervention arm and reported exposure to intervention
Sexually transmitted infection (STI) screening and knowledge of STI symptoms associated with Peru PREVEN intervention (2006 Survey).
Adjusted for 2002 baseline city proportions, age, brothel venue, and clustering by city.
Recoded as zero if skipped out of parent question.
Not adjusted for baseline, not asked in 2002 surveys.
Condom use, sexually transmitted infection (STI) screening, and knowledge of STI symptoms associated with reported exposure to Peru PREVEN intervention (2006 Survey).
FSW survey asked: Have you received services from (or participated in activities of) the PREVEN Mobile Team?
Adjusted for baseline city proportions, age, brothel venue, education, cohabitation, randomisation arm, and region. Cluster by city.
Recoded as zero if skipped out of parent question.
Sex work venue, condom use, and uptake of STI screening services
Condom use, sexually transmitted infection (STI) screening, and knowledge of STI symptoms associated with venue of sex work (2006 Peru PREVEN Survey).
Adjusted for age, education, cohabitation, region, randomisation arm, and alcohol use. Cluster by city.
Recoded as zero if skipped out of parent question.
Discussion
Despite significantly greater reductions in prevalence of curable STIs among FSWs from intervention cities than in control cities during the Peru PREVEN community randomised trial, we did not find statistically significant increases in uptake of STI screening services when comparing intervention and control cities after adjusting for baseline. One possible explanation is the mobility of FSWs, diffusion of the intervention across units of analysis (cities). Outcome surveys were performed at the city-level and enrolled FSWs separately from the intervention, thus one-quarter of the women completing outcome surveys in the intervention cities had not participated in the intervention. Furthermore, the mobile teams reported high turn-over among participants; after the fifth cycle of the intervention, more than half of FSWs were identified as first-time participants. 23 This is supported by consistent associations between increased health screening behaviors and reported exposure to the intervention. Another explanation could be the presence of social desirability bias in reporting sexual behaviors. In this study for example, more than 90% of participants in both cities reported condom use with their last client, numbers remarkably higher than most studies in other settings. Follow-up qualitative work revealed that participants were reluctant to admit non-condom use not only to research teams but also among their peers, especially in brothel settings where condom use was strictly enforced (C. Mejia, personal communication, 2012). However sex workers still acknowledged less condom use with non-clients than with clients and somewhat less condom use among FSWs not exposed to the intervention.
Another possible explanation is related to decreased statistical power when accounting for clustering by city.28,29 In our study, the design was powered for STI endpoints, which were less frequent than reported uptake of health services. Similar studies reporting statistically significant outcomes have been critiqued for failing to account for clustering in study design or analysis. 9 Finally, it is possible that reductions in curable STI rates were a result of periodic presumptive treatment for vaginal trichomoniasis, and testing and specific treatment for STIs, in addition to the moderate behavior change brought about by the counselling aspects of the intervention.
A recent systematic review of HIV risk among FSWs suggests an iterative and dynamic interaction between individual sex worker, client, work environment, community organization, and macrostructural factors. 30 An interesting finding in our analysis was that although street-based and brothel-based sex workers were more similar to each other than bar-based workers in demographic profiles, it was bar-based and street-based workers who had similar health-seeking behaviors, suggesting that structural factors operating in brothels could ‘override’ individual demographic risk characteristics. Similar findings were noted among injection drug-using FSWs in another semi-regulated setting in Tijuana, where policy environment and micro-social factors, such as having syringes confiscated by police, predominately drove increased HIV risk more so than individual level factors. 7 In the Philippines, structural factors including trafficking or managerial practices of having condoms available in sex work venues were independently associated with FSWs’ ability to negotiate condom use with clients. 31
In the context of Peru, as in many countries, prostitution has essentially had a quasi-legal status, in which sex work is generally not penalised, though efforts to promote it, especially with children, are considered criminal. Government health clinics in Peru offer free STI screening and treatment for FSWs, and regularly provided FSWs with documentation ‘carnets’ in order to verify health status. Although operation of brothels is not legal, they often operate and pay taxes under the auspices of a legally licensed establishment such as a bar or hotel. Outdated regulations required brothel-based FSWs to provide ‘carnet’ documentation of health status. Although these regulations were no longer enforced during the period of the study, many brothel owners continued to require condom use and health card documentation as a matter of practice.
Reported STI rates among FSWs have varied throughout the world by geographic location and type of sex work venue. However, which venues are of highest risk in any given setting has also varied tremendously. Bar-based or nightlife workers in Tijuana, Mexico, were characterised as at higher risk due to alcohol use and absence of regulatory enforcement, 32 while street-based sex workers in Bangkok, Thailand, had higher HIV and syphilis prevalences than other sex workers. 33 In Queensland, Australia, sex workers employed at licensed brothels were less likely to report gonorrhea than illegal street-based workers, 34 but brothel-based workers in Karnataka State in India were found to have higher rates of HIV infection and lower risk-reduction behaviors than street- and home-based FSWs. 10 The regulatory practices associated with the type of sex venue such as 100% condom use ‘house-rules’ or requirement of regular STI screening, more so than the venue type per se, may be a predominant driver of health-seeking and STI preventive behaviors among FSWs and should be examined further.
Modeling analyses suggest that decriminalisation of sex work could avert 33–46% of HIV infections over the next decade. 30 While regulation of sex work may promote positive health-seeking behaviors among FSWs, there is also concern that regulations have the potential to push the most vulnerable sex workers, such as those who are already HIV-infected, into less-protected settings.35–37 In our study only 21% of the 4156 women identified were brothel-based. In general it has been more difficult to identify and access sex workers in bars, nightclubs, or streets than in brothels.8,32 Our findings suggest that mobile teams that include FSW peers may be an effective method in reaching out to provide STI prevention, diagnosis, and treatment services to socially marginalised FSWs in all settings and to foster subsequent engagement in formal public health services.
These findings contribute to a body of evidence suggesting a role for health promotion interventions for sex workers utilising mobile outreach and peer services. Sex work venue is significantly associated with the health care-seeking and STI preventive behaviors of sex workers, thus health promotion interventions to increase STI prevention and detection among FSWs should consider structural factors related to all types of sex work venue.
Footnotes
Acknowledgments
Authors acknowledge the Peru PREVEN Study Team and the partnership of numerous local institutions including the Ministry of Health & local health directorates, and the National HIV/STI Program.
