Background
Due to its large population, India is a major contributor to the South Asian HIV epidemic [
1,
2]. Six Indian states have consistently reported relatively high HIV prevalence: four in the south (Karnataka, Maharashtra, Andhra Pradesh and Tamil Nadu) and two in the northeast (Manipur and Nagaland). The state of Nagaland is located in northeast India, a geographically isolated region of the country characterised by a history of political unrest and under-development. The people of Nagaland are ethnically, culturally and linguistically distinct from the rest of India. Approximately 90% of Nagas (local residents) are Christian [
3], and consequently, the Church is very influential in both the public and private spheres creating a socially conservative context in which public health issues are discussed and responded to [
4]. Geographical isolation, fear of discrimination and lack of confidentiality are some of the barriers that inhibit access to standard health care services for groups at high risk of being infected with HIV such as female sex workers (FSWs).
Nagaland is consistently listed as one of the high HIV prevalence states in India [
5]; adult HIV prevalence in 2009 was 0.78% compared with 0.31% nationally [
6]. Based on prevention of parent to child transmission (PPTCT) testing data, Nagaland has the highest HIV prevalence among pregnant women in the country (0.89% compared with 0.19% nationally) [
6]. Between 2003 and 2008 the HIV prevalence among female sex workers (FSWs) increased from 4.4% to 14.1% (compared with 4.9% nationally) [
6,
7]. The prevalence of STIs among sex workers is high, indicating that unsafe sex is occurring. For example, in 2009, 12.7% of FSWs in Dimapur, the commercial hub, had reactive syphilis serology (down from 22.1% in 2006) [
8].
The HIV response in Nagaland is led by the Nagaland State AIDS Control Society (NSACS). In some districts the response is provided alongside government by the Avahan-funded Project ORCHID (Avahan is the India AIDS initiative of Bill & Melinda Gates Foundation in India). Most targeted HIV prevention services in Nagaland are implemented by non-government organisations (NGOs) funded by NSACS and/or Project ORCHID. The targeted interventions working with FSWs offer a range of services including safe sex promotion, condom distribution, and testing and treatment of sexually transmitted infections (STIs).
The HIV prevention services targeting FSWs in Dimapur, the commercial hub of Nagaland, have been primarily (although not exclusively) provided by Project ORCHID-funded NGOs since 2004. Dimapur is a commercial hub and an important transportation node that draws people from outside and inside Nagaland. It is the only town in Nagaland with an airport and a rail head. Dimapur hosts a concentration of FSWs; there are an estimated 1800 to 3500 FSWs in the city [
9] who most commonly work in hotels (as opposed to more structured brothel-based sex-work), ‘booze joints’ (illegal bars), at home and on the street. While there are known hotspots for sex-work, there is no red light district as such. FSWs in Nagaland report substantial harassment from police, local gangsters and conservative religious and insurgent groups [
10]. Consequently, from a public health perspective, these women remain hard to reach.
A major component of Avahan’s evaluation strategy for their HIV initiatives in India is the Integrated Behavioural and Biological Assessment (IBBA), comprising repeated cross-sectional surveys of target groups in selected districts. Two rounds of IBBA have been administered to FSWs in Dimapur, the commercial capital of Nagaland, in 2006 (Round 1) and 2009 (Round 2). Evidence for the effectiveness of HIV prevention programmes is essential given the importance of controlling HIV, and the considerable cost of the investment. Central to HIV prevention effectiveness is condom use and HIV testing among high-risk group members such as FSWs [
11,
12].
This paper reports on comparative analysis of Round 1 and Round 2 IBBA data in order to address the following questions in relation to FSWs in Dimapur: 1) Has condom use and the uptake of HIV testing improved? 2) Has programme coverage and intensity improved? 3) Are key vulnerable FSW sub-groups being reached by the programme? and 4) Is programme exposure associated with condom use and participation in HIV testing?
Discussion
This paper presents an assessment of the HIV prevention programme for FSWs in Dimapur, Nagaland, Northeast India using IBBA data from round 1 (2006) and round 2 (2009). The analysis provides evidence of a substantial increase in condom use and HIV testing between round 1 and round 2, and an association that links exposure to programme services with a greater likelihood of condom use and HIV testing reaffirming the importance of the harm reduction programme in reducing HIV risk behaviours. However, our analysis provides evidence that programme coverage remained far too low between round 1 and round 2 and that there is a pressing need to scale-up services. This suggests that the increases in condom use and HIV testing can only be partially attributed to the programme. We found that younger FSWs, those newer to sex work, and those who were more mobile were less likely to have been exposed to programme services.
There was a marked improvement in condom use at last sex between round 1 and round 2 with both occasional and regular types of clients, and with main non-paying partners. Reports of consistent condom use also increased. Despite this strong progress, the proportion of FSWs using condoms at last sex with commercial clients is considerably lower than that observed among FSWs elsewhere in India. For example, condom use with occasional clients is approaching, or exceeds, 90% in Karnataka (88.0%) [
23], Mysore (89.9%) [
24], Tamil Nadu (98.1%) [
25], and Maharashtra (99.7%) [
26]. Regardless of the higher condom use among FSWs elsewhere, condom use among FSWs in Dimapur has clearly improved substantially from a very low base.
There was an encouraging improvement in the uptake of HIV testing. Importantly, there was a decrease in the proportion of HIV positive FSWs who had never had an HIV test. Despite the improvement in HIV testing uptake among these FSWs, it is still a relatively and unacceptably low level of uptake. In comparison, IBBA data from elsewhere in India revealed that FSWs having undergone an HIV test ranged from 50.0% to 86.0% in Andhra Pradesh; 56.0% to 96.0% in Maharashtra; 60.0% to 77.0% in Karnataka; and 67.0% to 84.0% in Tamil Nadu [
8].
We found no clear evidence of an improvement in programme coverage between round 1 and round 2. We did however find a consistent and strong association between programme exposure and both HIV testing and condom use with a range of partners in both rounds suggesting the programme was having a positive impact on those FSWs who had received services. The associations between programme exposure and both condom use and HIV testing were comparable to those in other parts of India where FSWs are also serviced by the Avahan-funded India AIDS Initiative [
19,
25,
26]. Importantly, there was a very strong association between programme exposure and having undergone an HIV test. In round 2, those FSWs who were exposed to the programme were 9 times more likely to have had an HIV test; 57.1% of those exposed to the programme had undergone an HIV test compared to 12.9% of those who had not been exposed. The effect of programme exposure on HIV testing was pronounced among FSWs who tested positive for HIV; the proportion of HIV positive FSWs exposed to the programme who had previously undergone an HIV test increased markedly from 20.0% in round 1 to 60.0% in round 2.
The lack of progress with regard to programme coverage and the relatively lower use of condoms and uptake of HIV testing among FSWs in Dimapur, in comparison to FSWs from other parts of India, may be partly explained by the challenges associated with mobilising the local FSW community. Effective community mobilisation has been seen to be associated with improved condom use among other FSW populations [
27]. However, sex work in Dimapur has historically been hidden with some known hotspots but few brothels and no red light district. FSWs fears of harassment from police, gangsters and conservative religious groups has meant that public disclosure as a sex worker is personally risky [
10]. As a result, these women remain hard to reach and difficult to mobilise as a community, unlike FSWs in other parts of India [
27,
28]. The low, but increasing, rates of FSW attendance at NGO meetings seen in this study suggests that mobilising the FSW community in Dimapur will take more time and concerted effort.
Furthermore, previous research revealed considerable ethnic, cultural, religious and linguistic diversity among sex workers in Dimapur, with varying pathways to sex work, which can contribute to polarisation between local women and those from outside the state [
10]. A high level of socio-cultural diversity may present a barrier to community mobilisation activities that seek to building unity and a sense of commonality within the FSW community in Dimapur.
Particular FSW sub-groups were more or less likely to have been exposed to the NGO programme interventions. FSWs who tested positive for an STI were more likely to have had contact with programme services. The higher exposure to programs among FSWs who had STI symptoms suggests that their exposure was related to seeking treatment for perceived STI symptoms, or that FSWs with an STI are riskier and more deeply engaged in sex work and thus more easily identified by programme services and more willing to use them. The study of Ketkesone et al. [
29] in Laos suggests that FSWs prefer to seek treatment at drop-in-centres compared to public or private hospitals/clinics in order to maintain confidentiality. Subsequently, perhaps those who are exposed to programs due to perceived STI symptoms may also be exposed to other services such as HIV testing and condom distribution.
Younger FSWs (i.e. those under 20), those new to sex work, and those more mobile FSWs who had sold sex outside of Dimapur were all less likely to have been exposed to programme services. It is unsurprising that programme reach is lower among younger and newer FSWs, and this result has been found elsewhere in India [
19]. They may be less likely to identify as sex workers, less connected to the sex work community, and less aware and/or trusting of NGOs, thus making them more hidden in their sex work and harder to identify and approach. Given their young age and that they are new to sex work, they may also have less knowledge of STIs/HIV and less skill and experience in negotiating a safer work environment including condom use.
Having sold sex outside of Dimapur could be interpreted as a proxy for being a more mobile sex worker, and/or having migrated from outside Dimapur; previous research on a sample of FSWs in Dimapur found that approximately 40% were born outside Nagaland. By definition, more mobile FSWs can be harder to identify and engage depending on the frequency and scope of their mobility. Analysis of data on FSWs from four high HIV prevalence states (Andhra Pradesh, Karnataka, Tamil Nadu and Maharashtra) identified that highly mobile FSWs (i.e. having sold sex in three or more places) were approximately three times more likely to be inconsistent in using condoms with either paying or non-paying partners [
30], highlighting mobile FSWs as a key group of interest. FSWs who were born outside Nagaland may present additional challenges given there are likely to be barriers such as literacy in the local language and knowledge of local services that may be impeding access to services.
Overall, the results of our analyses highlight that NGO programmes in Dimapur are making a substantial contribution to the use of condoms and the uptake of HIV testing at least among the FSWs they are in contact with, including improved participation in HIV testing by HIV positive women, thereby facilitating their access to treatment services. However, coverage is far too low for effective HIV prevention, and there remains a clear and pressing need to scale-up services. This may require the development of interventions that specifically target the more difficult to reach groups such as the young and mobile FSWs. For example, younger FSWs who are new to sex work, and who do not yet identify with the FSW community, may be more likely to respond to younger peer educators, or more attracted to a less conspicuous HIV prevention service such as a beauty parlour that is strategically placed close to sex work hotspots, and that provides a range of services in addition to beauty services. The programme coverage needs to be broadened, without compromising quality, so that it can have the same impact on a larger pool of the FSWs working in Dimapur.
These study findings are subject to several limitations. The use of RDS methods to recruit participants creates limitations for multivariate analysis; guidelines for multivariate analysis of RDS data are still under development and require validation. Despite this limitation, RDSAT provides probability-based estimates of programme coverage, condom use and HIV testing, and weights were generated for multivariate analysis to best account for having used the RDS sampling methodology. Reporting of certain behaviours may have been influenced by recall and social desirability bias. As with all cross-sectional study designs, causal relationships cannot be firmly established.
Despite these limitations, the analysis in this paper presents results that have significant programming implications and improves our assessment of NGO-delivered HIV prevention services in Dimapur.
Competing interests
The authors declare that they have no competing interests.
Authors’ contributions
GA and GKM conceptualized the analysis in this paper. GA undertook the data analysis presented in the paper with inputs from MK, GKM and PG. GA and MK wrote the first draft of the paper. GKM, JM and RSP were involved in designing and coordinating the data collection. RSP, JM and PG provided a strong review and edit of the final draft. All authors read and approved the final manuscript.