India is the second most populous country in the world and has an estimated 2.5 million people living with HIV . The HIV epidemic is highly heterogeneous, with evidence of diminishing incidence in some areas while increasing in others . The majority of HIV infections occur through heterosexual transmission, with unprotected paid sex a major transmission route, particularly in the southern states . Mathematical modelling suggests that preventive interventions directed at female sex workers (FSW) could halt the spread of the epidemic in India if applied at sufficient quality and scale , and that they are cost-effective . There is, however, little published evidence demonstrating the efficacy of FSW preventive interventions in India [5–8]. Moreover, the processes required to bring about changes to FSW community norms in terms of practising safer sex and treatment of sexually transmitted infections (STI) are unclear [9–13]. The National AIDS Control Programme in India now recommends community mobilization and enhancing the enabling environment for FSW preventive interventions, but, with few exceptions , the effectiveness of such approaches has not been well documented.
Karnataka state in southern India has a population of approximately 55 million. In 2003, when the HIV prevention programme in Mysore city described in this paper was initiated, the mean HIV prevalence among antenatal clinic attenders was 1.5%, placing it among the top four states in India with regard to HIV epidemic severity . In 2003, Mysore was characterized by high levels of street-based female sex work and general non-availability of condoms (from mapping and enumeration data collected at project initiation: S. Reza-Paul, personal communication). In January 2004, an HIV preventive intervention programme was initiated among FSW, male and transgender sex workers, supported by the India AIDS Initiative (Avahan) of the Bill and Melinda Gates Foundation, as part of a similar intervention across six states in India [15,16]. The programme took a rights-based approach , with three key project foci: (1) community mobilization and peer-mediated outreach, including condom promotion and provision; (2) increased access to and utilization of sexual health services, expansion of condom accessibility through social marketing, and increased condom availability in non-traditional outlets; and (3) creating an enabling environment to support the programme. During the first 6 weeks of the project, a participatory mapping and enumeration exercise was conducted . During the next 6 weeks, peer-mediated outreach was established, which identified and addressed difficulties reported by sex workers, and promoted a sense of camaraderie and kinship among the community. Simultaneously, dedicated sexual health services were established, which offered STI identification and syndromic case management, routine speculum examination, treatment for syphilis, and periodic presumptive treatment every 3–6 months for chlamydial infection and gonorrhoea (supplied in ‘grey packs’ containing 1 g azithromycin and 400 mg cefixime). The health services provided by the clinics promoted a ‘positive health image’, whereby regular sexual health check-ups connoted ‘normal’ health maintenance, rather than merely treatment for symptomatic STI. Advocacy with key stakeholders, such as the police, local government officials, local shopkeepers, clients and partners of sex workers, was initiated, and a 24-h crisis response team was established to assist sex workers during crises. A drop-in centre was created to provide a welcoming safe space, promoting dialogue among the community, as well as providing services such as a community kitchen and literacy classes.
To assess and document the impact of this programme, we conducted two unlinked, anonymous, cross-sectional, integrated behavioural and biological assessments (IBBA) on samples of FSW, approximately 6 months after project initiation, and again 2.5 years later.
Study design and sampling framework
Mapping and enumeration conducted in January 2004 estimated that 1420 FSW sold sex in Mysore city, working in three main zones. Sample size calculations were designed to detect a 10–15% increase in condom use with 90% power and alpha error of 5%, assuming a baseline value for consistent condom use with commercial clients of 50%. It was thus estimated that 385 participants (rounded to 400) were required for each IBBA round. In each IBBA round, a variation of the time-location cluster (TLC) sampling method was used to sample FSW. Guides from the sex worker community identified the FSW working in a zone during the specified time segment, and the first five respondents who agreed to participate were selected. At baseline, the three zones were each divided into four time slots, and the sampling numbers required were proportionally allocated. At follow-up, the three zones were divided into 15 sites, and each site was divided into two to four time slots per day, generating 2240 TLC. Eighty-five TLC were randomly selected with equal probability. The sample size was fixed at the first five respondents who were eligible and agreed to participate per TLC. At both surveys, FSW who agreed to participate were asked to provide written informed consent, and were then interviewed in a venue close to the solicitation site.
Integrated behavioural and biological assessment
A behavioural questionnaire was designed in English and back translated into Kannada (the local language), pilot tested with peer educators, and redesigned to be culturally sensitive and context specific . It contained questions about demographic characteristics, sex work and migration, sexual history and sexual behaviour, condom and injection practices, and the use of the project drop-in centre and sexual health clinic. Interviewers were literate FSW who were not peer educators and were trained for one week. All interviews were conducted in Kannada and took between 30 and 50 minutes to complete. To ensure confidentiality, the names of participants were not recorded and cannot be linked to the data.
Blood and urine samples were taken to test for HIV, herpes simplex virus type 2 (HSV-2), syphilis, gonorrhoea, chlamydial infection and trichomonas infection. All samples were transported daily to a laboratory in Mysore, and syphilis testing was conducted on serum. All other tests were conducted in Bangalore. Serum for HIV testing was stored at −20°C, and urine aliquots and dried blood spots for HIV testing were stored at 4°C. Urine aliquots for chlamydia, gonorrhoea and trichomonas testing were stored at −20°C. HIV serological testing used a synthetic peptide enzyme immunoassay (Detect HIV 1/2 system; BioChem ImmunoSystems, Montreal, Canada), and positive tests were confirmed using a recombinant antigen enzyme immunoassay (Genedia HIV 1/2 ELISA 3.0; Green Cross Life Science Corporation, South Korea). When serum samples were not provided, a dried blood spot was performed on fingerprick blood using the same serological tests. When neither serum nor fingerprick samples were provided, urine samples were tested for HIV by enzyme immunoassay (Calypte Biomedical Corporation, Berkeley, California, USA) and confirmed by Western blot (Calypte Biomedical Corporation). BED testing was done on all HIV positive serological specimens (Calypte Biomedical Corporation). Serological testing for HSV-2 used an IgG enzyme immunoassay (Kalon Biological Ltd., Aldershot, UK). Serological testing for syphilis used the rapid plasma reagin (RPR) method (Span Diagnostics, Sachin, India), and if positive, confirmation was by the Treponema pallidum haemagluttination assay (TPHA) test (Omega Diagnostics Ltd., Alloa, Scotland). Syphilis infection was defined as being RPR positive (any titre) and TPHA positive. High-titre syphilis was defined as having an RPR titre of 1: 8 or greater and being TPHA positive. Urine samples were tested by polymerase chain reaction (PCR) for gonorrhoea and chlamydia using the Roche Amplicor system (Roche Molecular Diagnostics, Pleasanton, California, USA), and for trichomonas infection using a PCR assay developed specifically at the University of Manitoba. Biotin labelled PCR primers were used during amplification  and a modified Trichomonas vaginalis bovine serum albumin conjugated probe  was used to coat the detection plates. Positive trichomonas tests were re-run for confirmation. All positive specimens and 10% of negative specimens were sent to the National AIDS Research Institute (NARI) in Pune, India, for quality assurance.
Following the surveys, all participants were referred for a free health check-up and treatment. Following the unexpectedly high syphilis results found in the baseline IBBA, intensive community mobilization was undertaken to promote regular syphilis screening, and services were established at the project clinic.
Data were double-entered using Microsoft Access. All statistical analyses were performed using STATA version 9.0. Odds ratios (OR) were used as the measure of association, and the Wald chi-square test was the statistical test used. There were few missing data at either round, except for syphilis and HSV-2 results from 36 participants in round 1. Women who participated in both rounds were included in all analyses, because as a result of the unlinked, anonymous nature of the surveys it was not possible to know which individuals in round 1 also participated at follow-up. Primary outcomes were defined as condom use at last sex with regular and occasional clients and with regular partners; the number of episodes of unprotected sex in the previous month; and STI prevalence (infection with HIV, HSV-2, syphilis, chlamydia, gonorrhoea and trichomonas). In the multivariate models, age was included as a potential confounding variable. Other potential demographic confounders were added to the model using a stepwise approach, and those which caused the OR of the independent variables to change by 10% or more were included in the final model. All results presented are unweighted because weighted analyses, adjusting for sex worker typology and non-response, produced essentially the same results.
The study was approved by the institutional ethical review board of St John's Medical College, Bangalore, India, and the health research ethics board of the University of Manitoba, Winnipeg, Canada. The study was also approved by the health ministry screening committee, Government of India. Due to the unlinked and anonymous testing of samples, it was not possible to trace and treat participants who had an STI. Those willing to know their HIV status were referred to government testing centres for free HIV testing, and STI case management was provided to all participants. Community mobilization for syphilis testing and treatment was also carried out. At the follow-up IBBA, women also received a card through which they could follow up on their syphilis serology result and treatment.
Of the 431 women invited to participate at the baseline IBBA, 429 did so. All 425 invited women participated at the follow-up survey, and 175 women took part in both IBBA; as noted above, it was not possible to link their responses as a result of the surveys being anonymous.
The median age for both surveys was 30 years (range 18–45). The majority of sex workers were illiterate (unable to read or write), and most were either married or had previously been married but were now separated, deserted, divorced or widowed (Table 1). The median age of sexual debut was 16 years at baseline [range 2–27; interquartile range (IQR) 14, 18 years] and 15 years at follow-up (range 2–30; IQR 14, 18 years). The median age women started selling sex was 25 years in both surveys (baseline range 12–44; IQR 21, 29; follow-up range 12–43; IQR 20, 28), and women reported working as sex workers for a median of 3 years at baseline (range 0–38; IQR 1, 5), and 5 years at follow-up (range 0–30; IQR 2, 10). The majority of women were street-based sex workers, who entertain clients either in a lodge, at home or in a public place. The proportion of women who reported 10 or more sex clients per week fell between surveys, and the median charge per sex act increased from 100 rupees to 200 rupees (baseline range 3–1000; IQR 100, 200; follow-up range 20–700; IQR 100, 200; Table 1). Only a minority of women reported ever having had anal sex (7% at baseline and 4% at follow-up, P = 0.04), or having injected drugs (0.2% at baseline; 0.7% at follow-up, P = 0.3).
Exposure to the intervention programme
In both univariate and multivariate analyses, compared with baseline, being seen in the follow-up survey was strongly (P < 0.001) associated with exposure to the intervention programme (Table 2). There were substantial increases in the proportion of women who reported ever being visited by a peer educator, the proportion ever visiting the drop-in centre, ever visiting the project sexual health clinic, ever receiving the ‘grey pack’ at the clinic, ever witnessing a condom demonstration, and currently carrying a condom. In addition, there was a reduction in the proportion reporting condom breakage in the previous month (Table 2).
At baseline, reported condom use with clients and regular partners was relatively low (Table 3). In univariate and multivariate analysis, there was strong evidence of an association between the follow-up IBBA survey and increased condom use at last sex with both clients and regular partners (Table 3). Moreover, the proportion of FSW reporting zero unprotected sex acts per month with all clients increased from 20% to 58% at follow-up (Table 3).
Sexually transmitted infection prevalence
At the baseline IBBA survey, 36 FSW (8.4%) had missing HSV-2 and syphilis serology results, and 29 FSW (6.8%) did not provide a serum sample for HIV testing. Of these 29, 26 provided a dried blood spot for HIV testing, and a urine HIV test was performed for the remaining three. At the follow-up IBBA survey, all women provided serum for HIV and STI testing.
Compared with baseline, HIV prevalence at follow-up remained stable (26.1% versus 24.2%), but in multivariate analysis there was a reduction in HIV prevalence in sex workers who reported not having a regular partner (Table 3). BED testing was performed on all HIV-positive serum specimens, and the proportion of BED-positive specimens declined from 22.9% (24/105) to 14.9% (15/101) [OR 0.59, 95% confidence interval (CI) 0.29–1.20; P = 0.14]. HSV-2 prevalence increased at the follow-up survey and was strongly associated with HIV infection at both baseline and follow-up (HSV-2 prevalence: baseline 59.5% HIV-uninfected versus 78.8% HIV-infected, OR adjusted for age 2.6, 95% CI 1.5–4.4, P = 0.001; follow-up 73.2% HIV-uninfected versus 97.1% HIV-infected, OR adjusted for age 13.6, 95% CI 4.1–44.4; P < 0.001).
In both univariate and multivariate analyses, there were substantial reductions at follow-up in rates of syphilis, high-titre syphilis, trichomonas, chlamydia and gonorrhoea infections, compared with baseline (Table 3).
Causal pathway analysis
Having observed strong associations between the follow-up IBBA survey and both increased condom use and decreased curable STI prevalence, possible pathways through which the exposure could have been having an effect were suggested (Fig. 1).
After adjusting for demographic and sex work characteristics, and for survey round, there was strong evidence of an association between programme exposure and increased condom use with commercial clients (Table 4). Interestingly, despite the striking increases in condom use at last sex with regular partners, there was only a weak trend between increased condom use with regular partners and exposure to the intervention programme (Table 4), suggesting that other unmeasured factors may be involved.
Reductions in chlamydial infection were strongly associated with clinic indicators (Table 4). Likewise, reductions in gonorrhoea were associated with receiving the ‘grey pack’. Not being infected with trichomonas was associated with condom use at last sex with a regular partner, whereas there were no associations between the reductions in syphilis infection and any of the programme exposure variables (Table 4).
We have documented substantial increases in self-reported condom use with all sexual partners, and significant reductions in the prevalence of four curable STI (syphilis, trichomonas, chlamydia and gonorrhoea) among FSW following the initiation of a community-led HIV preventive intervention. Furthermore, unlike other FSW populations in India that have reported sharp increases in HIV prevalence rates over time [11,12], we have reported no increase in HIV prevalence, and a decline in HIV prevalence among those women without a regular partner. In addition, we have documented extremely high programme coverage among the target population, so that by the second survey conducted 2.5 years after programme initiation, more than 90% of FSW reported having been visited by a peer educator, having visited the drop-in centre, having visited the dedicated sexual health clinic, and having received presumptive STI treatment.
As the cross-sectional surveys were unlinked and anonymous, it is not possible to ascertain directly what the rate of new HIV infection acquisition was during the study period. We did not attempt to translate the BED test results  into incidence rates because of the difficulties reported previously in doing so , but there is a suggestion that the rate of new infections may have declined. Furthermore, as infection with STI has been shown to increase the likelihood of HIV transmission [23–26], it is hoped that the substantial reductions in STI prevalence in this population (with the exception of HSV-2), in conjunction with increased condom use, would contribute to reductions in new HIV transmission events [27–29]. It is unclear why the prevalence of HSV-2 was higher at follow-up compared with baseline, but it may be related to the strong associations seen between HSV-2 and HIV-1 prevalence, and thus enhanced transmission of HSV-2 in the presence of persistent HIV-1 infection [30,31]. Bacterial STI are, however, a better marker of recent changes in sexual behaviour compared with HIV and HSV-2, which are chronic infections.
Treatment for STI at the project clinic was associated with reductions in the prevalence of gonorrhoea and chlamydia. The reduction observed in syphilis infection is probably due to intensive community mobilization for syphilis testing and treatment following the baseline survey, which has been undertaken twice per year since then. In the context of accessing and utilizing health services, the members of the community have taken an active part in not only mobilizing their peers to use services, but in positioning the health services as their own.
HIV/STI preventive interventions with FSW in resource-poor settings elsewhere suggest that combining sexual risk reduction, condom promotion and improved access to STI treatment reduces HIV and STI acquisition. In addition, from the few studies available, there is some evidence that structural interventions, policy change or empowerment of sex workers can also reduce the prevalence of STI and HIV [7,32,33]. This is one of the first studies to evaluate rigorously the effect on HIV and STI rates of a preventive intervention that combines risk reduction, condom promotion and improved access to sexual health services with the empowerment of sex workers . Although we did not directly measure empowerment, the high response rates coupled with the extremely high rates of programme exposure in the second survey suggest effective community mobilization. Several studies in both FSW and other populations have reported increases in condom use following intervention programmes [9,11,12,34–45]. Interestingly, reported condom use was not generally associated with reductions in curable STI in our study , and it is possible that condom use may have been overreported. In any event, for individuals in high-risk populations with high rates of STI prevalence and multiple sexual partners, STI and HIV transmission may still occur despite high levels of reported condom use [25,27,46–51].
Negotiating condom use with repeat clients and regular partners is difficult and more complex than with occasional clients . Indeed, the increases seen in condom use with regular partners at follow-up were only weakly associated with programme parameters, suggesting that other unmeasured factors such as community mobilization, empowerment and increased self-esteem may have enabled condom use with regular partners to increase. Although visiting the drop-in-centre was a facilitating factor for increased condom use, it is unclear exactly how these visits were important. Discussions with FSW suggest that the drop-in centre has acted as a peg around which community members have mobilized themselves, reducing the feeling of isolation among FSW who are often scattered and solicit in different public places. In addition, the interpersonal and group exchanges at the drop-in centre regarding FSW life situations, as well as choices that they can exercise by utilizing their collective bargaining power, may have acted to elevate self-esteem, as well as provide positive affirmation of risk reduction behaviours.
The conversion of a hostile environment to a more facilitative enabling environment for sex work has been reported elsewhere as a contributing factor to improved condom use [7,53]. Programme monitoring data from Mysore have documented a marked reduction in violence by partners, the police, local thugs and shopkeepers. This has translated into sex workers accessing services more easily, as well as carrying condoms without fear of their being used as evidence of sex work. In addition, working in an environment less threatened by violence supports women to make choices based on their own volition. Advocacy with lodge and house owners (where sex work predominantly takes place) has resulted in these establishments stocking condoms, amplifying the possibility of condom use.
Community mobilization is probably another unmeasured contributing factor to programme success . The overall increase in the transactional ability of FSW may have enhanced their ability to introduce condoms in their sexual encounters, and may account for the increased rate charged per sex act. The median charge doubled in 30 months, which is far more than could be accounted for by inflation, which had run at approximately 5% per year in India . Discussions with FSW about the reduction in reported regular partners have highlighted that some psychosocial needs previously met by regular partners are now being fulfilled by the sex worker collective and their friends, suggesting that for some sex workers, not having a regular partner may be a proxy indicator for empowerment and collectivization.
There are a number of limitations with survey data such as these. This study comprised two cross-sectional surveys, rather than a randomized, controlled trial (RCT) design. Without a suitable control group, it is not possible to rule out the possibility that the results may have occurred independently of the intervention, instead reflecting natural trends in STI prevalence rates. The magnitude of the observed changes, however, makes this exceedingly unlikely. Furthermore, although a clustered RCT may have been the theoretical gold standard, the ethical provision of basic HIV preventive services to all study participants may have led to STI reductions and increased condom use in all enrolled, as was seen in a recent RCT in Kenya . In addition, the ‘baseline’ survey was conducted 6 months after programme initiation, by which time the programme may already have started to have an effect. The magnitude of changes in condom use and STI rates may thus have been underestimated. Finally, the programme exposure variables measured did not fully capture the complexities involved with risk reduction behaviours. We are undertaking some qualitative assessments to understand these issues better, and we also plan to include indicators related to empowerment, community mobilization and the enabling environment in subsequent surveys.
In conclusion, the results of this study suggest that the rapid implementation of a community-led HIV prevention programme among FSW, featuring community mobilization and empowerment through peer-led outreach, along with enhancing the enabling environment and increasing access to and utilization of health services, can have a positive impact in terms of increased condom use and decreased STI prevalence among the FSW community. While we await the results of studies modelling the impact of such a programme on STI and HIV prevalence rates in the wider community , the roll-out of programmes such as this are critical for STI and HIV prevention and control in similar urban settings across India and the subcontinent.
The authors would like to thank St John's Medical College and Hospital, Bangalore, TTK Blood Bank, Bangalore, and JSS Medical College and Hospital, Mysore, for their support with specimen collection, storage, transportation and testing. Sincere thanks are offered to Dr S. Sundararaman for his mentoring and support to this project and also to Dr S. Jana for his insights into the development of this project. Gratitude goes out to the members of Ashodaya Samithi (the sex workers' organization) and the project staff in Mysore for their tireless efforts in implementing the HIV prevention programme.
Sponsorship: This study was supported by the India AIDS Initiative (Avahan) and the Bill and Melinda Gates Foundation, grant no. 43136.
The views expressed herein are those of the authors and do not necessarily reflect the official policy or position of the Bill and Melinda Gates Foundation.
Conflicts of interest: James F. Blanchard receives funding from Canada Research Chairs, Health Canada.
All other authors declare no conflict of interest.
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