Despite the effectiveness of penicillin and its ubiquitous use over the last half-century, infection with Treponema pallidum, the causative agent of syphilis, remains elusive to elimination.1–2 Reemergence of syphilis at alarming proportions among at-risk populations in high-income countries is raising issues of prevention, treatment, and control once again—with a focus on increased screening as a mainstay of public health programs.1–3 Indeed, early diagnosis is paramount, as syphilis is most transmissible within 2 years of inoculation, especially in the presence of a primary chancre and during secondary syphilis.4 It is estimated that of the 9.4 million incident primary and congenital cases of syphilis acquired globally each year, 2.5 million occur in South and Southeast Asia.5 In India, the prevalence of syphilis in sentinel surveillance, as measured by RPR positivity among antenatal clinic attenders, was 1.5% in 2005. This suggests, when projected to the general population, that an estimated 6.9 million people may have had a prevalent syphilis infection that year, although RPR positivity does somewhat overestimate true syphilis prevalence.6,7 Among female sex workers (FSWs), syphilis prevalence is decidedly higher, often well over 20%.8–10 In addition to risky sexual behavior, related lifestyle factors such as mobility, violence, and alcohol abuse within the often marginalized communities of FSWs heighten their vulnerability to syphilis.11–16 Limited physical and social access to medical care can also impede individual treatment,17–20 thereby indirectly facilitating transmission within the population.1
Because of its wide spectrum of clinical presentation, including a painless (and often silent) primary stage, the diagnosis of syphilis can easily be missed. Primary lesions, which occur in the anogenital and oral mucosa, may reside undetected,21–23 the lack of symptoms obviating an infected individual’s perception of the need for treatment, use of condoms, or cessation of sexual intercourse. The presence of genital ulcers because of syphilis can facilitate the transmission of HIV and increase the risk of acquiring HIV.24,25 Moreover, even in the absence of self-reported genital ulcers, a recent study from Pune, in western India, has shown that within 6 months after an incident syphilis infection, individuals are 4 times as likely as those without syphilis to become infected with HIV.26 This epidemiologic synergy necessitates integration of syphilis treatment into HIV prevention programs.27,28 To implement effective strategies for the prevention, diagnosis, and treatment of individuals at highest risk of acquiring syphilis, it is essential to determine the prevalence of infection and understand the socio-demographic characteristics, behavioral risk factors, treatment seeking behaviors, and existing health services accessed by FSWs.
As part of the Bill & Melinda Gates Foundation’s India AIDS Initiative (Avahan), an HIV preventive intervention program directed at high-risk populations in India,29 integrated biologic and behavioral assessment (IBBA) surveys of FSWs were conducted in 5 districts in the state of Karnataka from 2004 to 2006. These surveys were conducted near the beginning of program implementation within each district, to provide baseline data to inform, monitor, and evaluate program initiatives. Examples of initiatives directed at reducing risk for HIV infection among FSWs include condom demonstration and distribution by peer educators and outreach workers; technical assistance for community and self-help group formation to support risk reduction behaviors; and provision of clinical and laboratory services in STI clinics. Clinical services at the time of the IBBAs consisted of syndromic management for STIs (including administration of benzathine penicillin for nonherpes like genital ulcers) and asymptomatic (presumptive) treatment for N. gonorrhoeae and C. trachomatis with a one-time dose of oral azithromycin 1 g and cefixime 400 mg.30 Interventions targeting syphilis control had not yet been put into place. In the absence of staging information, syphilis serology may be approximated to help distinguish active versus lifetime infection,31 differences that may be due to treatment-related factors. This study reviews the prevalence of and risk factors associated with syphilis infection, as well as specific treatment-seeking behavior among FSWs working in urban Karnataka, that subsequently directed programmatic strategies for HIV and STI risk reduction within the state.
Study Sites and Population Sampling
Data used in this study were drawn from cross-sectional IBBA surveys of urban FSWs in 5 districts of Karnataka. The districts selected were ones with large numbers of sex workers, and were selected to reflect the state’s geographic heterogeneity (Table 1). The first district to undergo an IBBA was Mysore in August 2004. Subsequent to that experience, modifications were made and additional questions were included in the questionnaire. Although these surveys were the first in a planned 3-series IBBA and constructed as a baseline assessment, considerable program infrastructure was in place at the time of each survey, as shown in Table 1.
The target sample size was 400 FSWs per district, with the exception of Bangalore Urban (800 participants), and was calculated based on published guidelines.32 The sampling methodology used for the survey in Mysore was slightly different, as the survey was undertaken earlier than the others, before the sampling methodology was standardized. Mysore was divided into 3 zones, which in turn were divided into 4 time-segments, and FSWs were randomly and proportionately selected from each time-segment. In the remaining districts, two-stage cluster sampling was utilized. For nonpublic places of solicitation, conventional cluster sampling was used to obtain random samples of respondents, whereas for public-places, time-based cluster sampling was used. For the latter, within each cluster, 5 respondents were randomly selected and invited to participate, with replacement in the case of nonresponse.
Institutional Review Boards at St. John’s Medical College (Bangalore, India) and the University of Manitoba (Winnipeg, Canada) approved the study. The study was also approved by the Health Ministry Screening Committee, Government of India.
Data Collection and Laboratory Testing
After providing informed written or oral (witnessed) consent, participants were administered a 20-minute face-to-face questionnaire by a trained interviewer in the local language (Kannada, Hindi, Tamil, or Telegu), and thereafter were invited to provide a venous blood and a urine sample. The reasons for declining to participate were not collected. In Mysore, all participants were referred for a free health check-up and treatment. In the remaining districts, women reporting symptoms of an STI were referred for assessment, and received a card through which they could follow-up on their syphilis test. Participants were encouraged to undergo HIV testing at a voluntary counseling and testing centre, and referred to the nearest centre. Venous blood samples were tested at St. John’s Medical College, Bangalore, for RPR (Span Diagnostics, Sachin, India); TPHA (Treponema pallidum Hemagluttination Assay test, Omega Diagnostics Ltd., Alloa, Scotland); HSV-2 (on Mysore specimens by Kalon Biological HSV2 IgG ELISA, Kalon Biological Ltd, Aldershot, United Kingdom, and on other specimens by HerpeSelect ELISA, Focus Diagnostics, Cypress, CA); and HIV antibody (Detect HIV 1/2 system, BioChem ImmunoSystems, Montreal, Canada), with positive ELISA samples confirmed using a recombinant antigen enzyme immunoassay (Genedia HIV 1/2 ELISA 3.0, Green Cross Life Science Corporation, South Korea). Aliquots from urine samples were transported in cold packs to TTK Blood Bank, Bangalore, where testing for N. gonorrhoeae and C. trachomatis was carried out (on Mysore specimens by Amplicor Duplex NG/CT PCR, Roche Molecular Diagnostics, Pleasanton, CA, and on other specimens by APTIMA-Combo 2 PCR, Gen-Probe Inc., San Diego, CA).
Socio-demographic characteristics, sexual behavior, treatment seeking patterns, and program-related exposures are reported using cluster-adjusted descriptive statistics. Outcomes of interest in this study were lifetime syphilis infection (positive TPHA) and active syphilis infection (positive RPR and TPHA). Typologies of sex work were defined as home based (soliciting at home or rented room, and having sex in the same place); brothel based (soliciting at a brothel or lodge and having sex in the same place); public to brothel or lodge based (soliciting in a public place and having sex in a brothel or lodge); public to home based (soliciting in a public place and having sex at home or rented room); and public based (soliciting and having sex in a public place). Univariate and multivariate logistic regression (Stata 9.0, StataCorp) was used to identify risk factors for lifetime and active syphilis infection, with adjustment for possible within-cluster homogeneity.
Socio-Demographic and Behavioral Characteristics
Of the 2741 women invited to participate, 2213 (80.7%) agreed to the interview, and 2208 (80.6%) also provided biologic samples. The prevalence of N. gonorrhoeae, C. trachomatis, HSV-2, and HIV is presented in Table 2. The prevalence of syphilis and socio-behavioral features of the respondents is shown in Table 3. Of the 211 women who had active syphilis, 128 (60.7%) had an RPR titre ≥1:8. Although the majority of women solicited clients in public places, nearly two-thirds of them moved to a home, or to a brothel or lodge, to have sex. Most women had a regular, noncommercial partner, with whom reported condom use at last sex was low, compared to use at last sex with paying clients (30.3% vs. 79.6%, P <0.001). The use of recreational injection drugs was reported by only 0.32% of women.
Among women who recalled having symptoms of an STI in the past year (N = 976), 70.0% stated that they used condoms or ceased to have sex while symptomatic with the last episode. There was near equal distribution in the selection of available physician-based services (government, NGO-affiliated, or private clinics; P = 0.88) between the districts. Sixty-one percent of women waited more than 1 month to seek treatment. Women who sought treatment were also more likely to engage in protective behavior or remain abstinent while symptomatic [odds ratio (OR): 2.1, 95% confidence interval (CI): 1.4–3.3]. Providing a history of recent genital ulcers was a poor predictor of lifetime or active syphilis.
Most women had already been contacted by at least 1 peer educator or outreach worker, and 74.1% had received education on condom use (condom demonstration or condom distribution by peer/outreach workers). Two-thirds of respondents had visited a program clinic, and over half had received a single dose of azithromycin and cefixime as presumptive treatment for cervical infection from the clinic.
Determinants of Syphilis
The overall prevalence of lifetime and active syphilis were 25.3% (95% CI: 23.1–27.5) and 9.6% (95% CI: 8.2–10.9), respectively. Several factors were significantly associated with syphilis on univariate analysis (Table 3). On multivariate analysis (Table 4), independent socio-demographic and behavioral risk factors for lifetime syphilis were older age, being illiterate, longer duration of sex work, client volume, solicitation in public places followed by sex in a brothel or lodge-based venue, and engaging in sex work in more than 1 city. With active infection, predictive factors on multivariate analysis included illiteracy, client volume, being divorced, widowed or deserted by a spouse, and public place solicitation to brothel or lodge-based sex work. Women working in Mysore and Bangalore urban districts had nearly 4× the odds of lifetime syphilis compared to FSWs in Shimoga (reference district). Although these 2 southern districts had a comparable burden of lifetime syphilis (OR: 0.89, 95% CI: 0.65–1.2), there was a higher proportion of active infection among FSWs in Mysore (OR: 1.8, 95% CI: 1.2–2.8). Among women who had a main, noncommercial partner (N = 1498), lack of condom use during last sex was independently associated with increased risk of lifetime syphilis (OR: 1.4, 95% CI: 1.1–1.9), but not active infection (OR: 1.2, 95% CI: 0.64–2.0), after controlling for the significant predictors noted above.
Treatment-seeking behavior was assessed for women who recalled STI symptoms in the last 1 year (N = 976). After controlling for significant socio-behavioral predictors identified on univariate analysis, having visited a physician or pharmacist remained protective against lifetime syphilis (OR: 0.61, 95% CI: 0.40–0.95) and active syphilis (OR: 0.53, 95% CI: 0.28–0.97), yet did not fully explain the variance between districts in this subset of patients.
A separate multivariate analysis (excluding Mysore, where alcohol consumption was not ascertained) was conducted using the same significant variables as above, and revealed that alcohol consumption was an independent risk factor for lifetime syphilis (OR: 2.0, 95% CI: 1.5–2.6) and active syphilis (OR: 2.4, 95% CI: 1.4–4.0). As shown in Table 5, syphilis coinfection with other STIs was common. HIV-infected women were significantly more likely to have a lifetime or active syphilis infection. In addition to HIV, HSV-2 sero-positivity and infection with N. gonorrhoeae was strongly associated with syphilis.
We found high prevalences of both active syphilis and lifetime syphilis in this population of female sex workers in South India. Elucidating the determinants of syphilis in core groups can be challenging, as both acquisition-related and treatment-associated behaviors need to be examined. In a cross-sectional study, positive treponemal-specific tests (TPHA) could represent an infection acquired at any time (usually past or treated), whereas a positive nontreponemal test (RPR), with confirmation, may reflect active disease, but may remain positive for some time after effective treatment.21 In the absence of a detailed clinical evaluation to approximate the stage of syphilis and long-term follow-up to monitor for seroconversion, we have made assumptions (acknowledging the limitations) regarding the timing of disease to facilitate our understanding of risks and treatment in this population. Discrepancy between the prevalence of lifetime and active infection was presumed to result from measured and unmeasured treatment. As would be expected, the overall prevalences of the other curable STIs and active syphilis were lower than the prevalences of HIV, HSV-2, and lifetime syphilis. Although the risk of acquisition of different STIs is not uniform, this finding may reflect treatment-related factors, and emphasizes the need to promote consistent condom use and other risk-reduction behaviors, in addition to enhancing treatment of the treatable STIs.
A striking finding in our study was the marked variability in the prevalence of syphilis between the districts, differences that could not fully be accounted for by the socio-behavioral determinants identified. This variability may be due to heterogeneity in sexual networks and bridging populations.33,34 For example, in a related IBBA conducted among clients of FSWs (unpublished data, IBBA of clients of FSWs, Karnataka Health Promotion Trust), a large number of men in Bangalore Urban reported having had sex with a man or hijra (a male to female transgender) (Table 1), implying a complex network between core groups in this district. At an ecologic level, general treatment seeking behavior and physician practices may differ between districts and contribute to the variation in active syphilis (at an individual level), and thus, incident syphilis infection (at a population level).15 We found a similar prevalence of lifetime syphilis infection in Bangalore Urban and Mysore districts. However, the prevalence of active infection was notably higher in the latter, suggesting that specific and general treatment practices between the 2 districts may underlie this divergence. FSWs from Mysore were less likely to seek out specific treatment and to report direct program exposures, possibly because the IBBA in Mysore was undertaken much closer to program initiation than in the other sites. General treatment seeking behavior among FSWs was assessed in the Bangalore Urban survey, revealing that 79% of FSWs had received at least 1 medical injection in the last 12 months, of which 91% were for an infection or a condition related to HIV/AIDS. Nearly all (96%) of medications provided were prescribed by a medical professional, suggesting that antibiotics may have been given. There was insufficient power to assess receipt of medical injections as it relates to active syphilis, but its protective effect has been shown in a previous study in India.26 There has been speculation that in the northern Karnataka districts, physicians prescribe a high frequency of medical injections as compared to the southern districts. If data from the general population may be projected to the treatment-seeking behavior of FSWs and concomitant physician practices, then as shown in Table 1, there is a large difference between the representative northern Karnataka district (Belgaum), where 75% of the population had received a medical injection in the previous year, and the representative southern Karnataka district (Mysore), where only 55% of the population had undergone such treatment [unpublished data, General Population Community-Based STI and HIV Prevalence Study, Mysore (2006) and Belgaum (2007) Districts, Karnataka Health Promotion Trust and Charme Project, Centre hospitalier affilié universitaire de Québec, Québec, Canada]. In both regions, 98% of the treatments were administered by a medical doctor.
A limitation of this study was in combining baseline surveys conducted over a two-year time period, and as indicated above, the varying durations of times that programs were in place before IBBAs being conducted could account for some of the variation in prevalence of syphilis. Potential contributing factors to variability in syphilis prevalence, such as heterogeneity in sexual networks and generalized treatment patterns between the districts, warrant further study.
We categorized sex work typology based on place of solicitation and subsequent place of sex, and discovered that women who solicited in public places and had sex in a lodge or brothel- based venue were at highest risk of both lifetime and active syphilis. Compared with FSWs who do not move locations to have sex or who move to a home-based site, these women may have limited condom access and negotiation power, and were identified as a group at significant risk. Furthermore, although having similar risks of lifetime acquisition, women who were divorced, deserted, or widowed were more likely to have active infection, implying either higher rates of repeat infection or lower treatment provision among this subgroup. This risk profiling has allowed programs to enhance program and service outreach to the most at-risk FSWs using a targeted approach, and focusing efforts on women soliciting in public places but having sex in brothels or lodges and on women exhibiting the other risk factors identified. Alcohol use was associated with syphilis infection, and there was a trend toward increased risk of lifetime syphilis among women who had experienced sexual violence.11–15 In conjunction with directed intervention programs, these lifestyle-related issues are also being addressed by programs.
The majority (78.8%) of women had accessed health-care facilities (physician or pharmacist) to address symptoms of STIs, which is comparable to the 2001 and 2006 findings from national surveys of FSWs (86.5% and 92.4%, respectively), and higher than in the general population (56.4% and 58.8%, respectively).35,36 Two-thirds of respondents had visited a program clinic, suggesting an opportunity for intervention: implementation of systematic syphilis screening in all program clinics caring for FSWs within the state. With less than half of women having recalled STI symptoms in the past year, including less than 10% having reported a previous genital ulcer, the findings highlight the need for screening asymptomatic individuals if syphilis control is to be achieved. Scaling-up of this initiative has been underway, and in the first follow-up IBBA survey conducted in Mysore in December 2006, the prevalence of active syphilis had declined from 24.9% to 12.0%.37 In our study, syphilis was associated with key behavioral indicators (low condom use, high client volumes, and poor treatment-seeking behavior for STI symptoms). Prevalent active syphilis, if treated appropriately, will generally sero-revert to RPR negative; thus, a lower prevalence over time would reflect one or a combination of decreased acquisition of syphilis because of behavioral change and increased appropriate treatment.
In summary, we observed considerable heterogeneity in the prevalence of syphilis among FSWs surveyed in different districts, confirmed the risk profile of urban FSWs, and found that there was a high level of treatment seeking and good program accessibility. There was opportunity therefore to enhance the capacities of clinics to screen and treat for syphilis, and in addition to existing syndromic and asymptomatic N. gonorrhoeae and C. trachomatis treatment programs, the scale-up of syphilis screening services is now well underway. Specific gaps in program coverage have been identified and are being addressed. As noted above, having been infected with syphilis was associated with a two-fold increased probability of being HIV-positive. Conversely, nearly 40% of women with HIV infection had lifetime syphilis infection, and 15.7% had syphilis at the time of the surveys. Addressing risk behavior and treatment to achieve good syphilis control therefore should help not only to reduce syphilis incidence, but also HIV infection, among FSWs, their clients, and the general population in India.
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