An important feature of the HIV/AIDS epidemic in India is its remarkable heterogeneity. Whereas HIV prevalence among antenatal clinic (ANC) attenders in most Indian states is well under 1% , several states in the southern and northeastern areas of India have more severe epidemics, with mean HIV prevalence approaching or exceeding 2% among antenatal women in some districts in those states . Not surprisingly, given the large population size and sociocultural differences, there is also an uneven geographical distribution of HIV within states and even within districts . The concentration of the epidemic in a relatively small number of states and districts, and in specific high-risk populations within them, particularly female sex workers (FSW), men who have sex with men and injection drug users , offers an important window of opportunity for prevention. In particular, effective and intensive prevention programmes directed to those areas and populations that are at highest risk of HIV transmission could significantly curtail the expansion of the HIV epidemic .
Using behavioural parameters from studies in India, mathematical modelling has suggested that an intervention that effectively increases condom use to 80% of sexual encounters between FSW and clients would be sufficient to curtail and ultimately virtually eliminate the epidemic in India . An intervention that improves the control of curable sexually transmitted infections (STI) would also significantly curtail the epidemic. Studies from Kenya have indicated that a combination of these two strategies has resulted in dramatic declines in curable STI, and is associated with a declining trend in HIV prevalence in the general population . The challenge for India, and many other countries, is to take these preventive interventions to a scale that is sufficient to arrest the HIV epidemic.
The state of Karnataka in south India, with a population of approximately 55 million, is divided into 27 administrative districts, including Bangalore, the state capital. The first individuals with AIDS in Karnataka were identified in 1988. Since then, there is evidence that the HIV epidemic has advanced substantially within the state. In the general population, data from ANC attender surveillance suggest that the overall mean prevalence of HIV in the adult population at the beginning of the current decade was relatively high: 1.4% in 2001 and 1.7% in 2002 , although ANC attender surveillance in those years did not cover all districts. At that time, Karnataka had the third highest HIV prevalence in ANC attenders among the four large states in south India, the region in India with the highest HIV prevalence . In addition, the prevalence of HIV among STI clinic attenders in all but one sentinel site throughout the state was over 10%. HIV prevalence data from FSW populations were not available until later on, but in studies undertaken from 2004 to 2006, HIV prevalence ranged from 10% to 34% in five districts of Karnataka , suggesting a serious epidemic in the higher risk segments of the population.
In Karnataka, as elsewhere in India, female sex work is an important component of HIV transmission dynamics. Sex work is widely distributed in Karnataka . Unlike major Indian urban centres such as Kolkata and Mumbai, brothel-based sex work is relatively uncommon, with brothel-based FSW representing only approximately 3.4% of the overall total . Instead, most sex work is either home based or is initiated in public places [8,9]. In the northern, mostly rural, districts of Karnataka, home-based sex work predominates and tends to be geographically dispersed, manifesting itself in a high proportion of villages . Female sex work in that context is embedded within the social and cultural traditions in those areas .
In 2003, the Karnataka state government's State AIDS Prevention Society (KSAPS) and the University of Manitoba established a partnership through the Karnataka Health Promotion Trust, in order to intensify and expand the response to the HIV epidemic in the state. With support from the Bill and Melinda Gates Foundation's India AIDS Initiative (Avahan), a project was designed to reduce HIV transmission in Karnataka through focused preventive interventions among FSW and their clients . Activities have been implemented in 18 priority districts. These districts were selected on the basis of the severity of the epidemic as measured by HIV prevalence, and on an assessment of vulnerability based on information regarding known vulnerable groups, particularly FSW. Districts where there were few existing prevention programmes in place were also preferentially selected for the programme. Four critical activities were implemented in an integrated fashion in each of the priority districts: focused HIV and STI prevention education outreach, with emphasis on condom promotion, using a peer-mediated education approach ; behaviour change programmes for HIV and STI risk reduction among regular partners of FSW; improved quality and accessibility of high-quality STI management services for FSW; and enhancement of the enabling environment to support the programme, including efforts to reduce stigma and discrimination, reduce violence and harassment, and promote social equity.
A strategic and population-based approach was used in the design and implementation of programmes and services. First, a comprehensive situation assessment was conducted to determine the nature, location and size of the FSW populations and to understand high-risk sexual behaviour. This was done through rapid social mapping, behavioural surveys, and epidemiological assessment of the population distribution of HIV and STI. On the basis of this assessment, preventive interventions for FSW were tailored to the local situation and needs. For FSW, these interventions included both individual/cognitive interventions for behavioural risk reduction through peer education, access to STI services, and structural interventions to reduce vulnerability through creating an enabling environment for behaviour change, such as establishing crisis-response programmes, and advocacy with police and media outlets. By the middle of 2005, FSW programmes had been scaled up in most of the 18 districts, as well as within subdistrict locations, implemented by various non-governmental and community-based organizations . At present, we estimate a total programme coverage of over 60 000 FSW in the urban centres in the 18 districts, as well as in rural areas of several districts, where the rural epidemic was felt to be substantial . Project reach now includes 178 cities or towns and over 200 village clusters, covering over 2500 sex work sites. Counselling and medical (STI) services are provided through 175 drop-in centres, 93 programme-run clinics, 110 outreach clinics and 157 referral clinics. Approximately 80% of all FSW are contacted on a regular basis (monthly) by programme peer educators or outreach workers, and approximately 20% of FSW attend a programme-linked STI clinic or STI referral clinic each month. Mean reported condom use at last sex by FSW, as measured through annual surveys using a polling booth methodology  has increased from very low levels before programme initiation to between 70% and 90% in all sites . In the other nine districts in the state, several non-governmental organizations have been funded to execute targeted interventions among FSW, also using a peer educator-mediated approach to behavioural risk reduction, including condom distribution. Coverage has, however, generally been restricted to a few large towns in each district and a smaller number of sex work sites, access to STI services has been more limited, and less emphasis has been placed on vulnerability reduction measures. In addition, the regularity of contact of FSW by the programmes in the other nine districts is probably not as frequent, although data are sparse. In this paper, the 18 districts covered by the Avahan-supported programme are therefore referred to as intensive preventive intervention (IPI) districts. In the 18 IPI districts, the average number of condoms distributed directly by the programme to FSW contacted in 2007 was approximately 435 per FSW (range 96–1784); the corresponding figure in the other districts was 215 (range 53–507), consistent with the notion of a less intensive programmatic approach in the non-IPI districts. To assess the impact of the IPI programme at an ecological level, we examined trends in HIV prevalence among ANC attenders over time, and compared trends in the IPI districts with those in the non-IPI districts.
Since 2001, annual sentinel surveillance of ANC populations has been conducted in Karnataka by the Karnataka State AIDS Prevention Society (KSAPS), under the guidance of the Indian National AIDS Control Organisation (NACO). Each year, usually between July and September, 400 consecutive ANC attenders are sampled from government ANC throughout the state, are administered a brief questionnaire, and have blood samples tested for HIV in an anonymous, unlinked fashion . In 2001 and 2002, surveillance was conducted in only a small number of districts. From 2003 onwards, surveillance has been undertaken in all 27 districts in Karnataka, and in two sites per district: one is the ANC at the district headquarters city or town; the other is an ANC at a subdistrict (taluka) headquarters town, referred to as a first referral unit (FRU). Four hundred ANC attenders from each of the two ANC in all of Karnataka's 27 districts were sampled each year between 2003 and 2007 inclusive. Although it has been suggested that HIV prevalence among ANC attenders in India may overestimate HIV prevalence in the general population , the fact that the same sites and populations were sampled over a period of many years allows for an examination of trends over time .
The information collected from the ANC attenders includes age, rural/urban location, education level, district where the ANC is situated, and whether the clinic is located at the district headquarters or at an FRU. HIV testing is done by enzyme-linked immunosorbent assay at government voluntary counselling and testing (VCT) centres, and if an initial test is positive, a second test is performed for confirmation. If both tests are positive, the result is considered positive. All positive samples and 10% of negative samples are re-tested at the National Institute of Mental Health and Neurological Sciences (NIMHANS) in Bangalore for quality control.
We examined overall trends over time in HIV prevalence from 2003 to 2007, stratified by age and by the other parameters noted above. We were particularly interested in young ANC attenders (under the age of 25 years), as HIV infections in these women are more likely to represent recent infections, and are thus more likely to mirror recent changes in HIV transmission . Crude trends in HIV prevalence were tested using conditional logistic regression, with individual HIV infection as the dependent variable and year of survey as the independent variable, stratifying for district, district headquarters/FRU, urban/rural residence, literacy and age. As the 18 IPI districts were not assigned randomly from the total of 27 districts, to compare trends between the 18 IPI districts and the nine other districts, we also constructed a random effects (multilevel) logistic regression model, using STATA version 10.0 (xtmelogit command), with HIV infection as the dependent variable. This differs from standard logistic regression in that individuals are assumed to belong to larger units (districts, or more specifically the set of surveillance sites belonging to specific districts), and that there exists variation among these units that impacts on the outcome of individual subjects. All records were included from all women at the 54 ANC sites from 2003 to 2007. As HIV prevalence in 2003 varied substantially among districts, district HIV prevalence in 2003 (baseline HIV prevalence) was entered in the model as a potential confounder, as was its interaction with subsequent survey year (counted from 2003). The other variables entered into the model were the type of site (district headquarters clinic or FRU), rural/urban location, literacy, age, district HIV prevention programme (IPI or non-IPI district), and the interaction between year of survey and the variable IPI/non-IPI district. The estimated regression coefficient of the latter variable was used as the main outcome measure. Differences in HIV prevalence among districts at baseline, as well as heterogeneity in trends over time among districts, were included as random effects in the model (i.e. random intercept and slope). Standardized HIV prevalence rates by year for the IPI and non-IPI districts were calculated using direct standardization methods (i.e. they were not based on a statistical model), standardized for district, district headquarters/FRU clinic, urban/rural location, age and literacy.
Table 1 shows the number of ANC sentinel surveillance sites in Karnataka and the distribution of ANC attenders among district headquarters and FRU sites, from 2001 to 2007. As indicated above, only data from 2003 onwards have been used in this analysis. Figure 1 shows HIV prevalence among ANC attenders participating in the ANC sentinel surveillance from 2003 to 2007, stratified by age. Overall, HIV prevalence was approximately 1.5% in 2003 and 2004, and declined steadily from 2005 to 2007, reaching a prevalence of 0.86% in 2007 (P < 0.001 by conditional logistic regression). As would be expected with a chronic infection, HIV prevalence was higher in women aged 25 years or older than among women under 25 years of age, but the declines in HIV prevalence over time in both age groups were similar, and both trends were statistically significant (P < 0.001 and P = 0.003 for ages <25 and ≥25 years, respectively). Overall, approximately 68% of the ANC attenders between 2003 and 2007 were under the age of 25 years.
Figure 2 shows HIV prevalence among ANC attenders under the age of 25 years participating in the ANC sentinel surveillance from 2003 to 2007, stratified by IPI districts versus other districts. HIV prevalence among women in the IPI districts was higher in 2003, reflecting the selection of higher risk districts for the intensive intervention, as noted above. By 2005, HIV prevalence in the IPI districts was comparable to that in the other districts, but was much lower in 2006 and 2007. In the IPI districts, HIV prevalence in 2003 was 1.49%, and declined steadily to 0.61% in 2007, representing a crude overall decline of approximately 59%. In the non-IPI districts, HIV prevalence in 2003 was 1.21% and 1.11% in 2007, a crude decline of 8.3%.
In the random effects logistic regression model described above, age, year of survey, and the interaction between baseline HIV prevalence and survey year were not statistically significant predictors of HIV infection. We therefore ran the model again without age, but retained survey year and the interaction between baseline HIV prevalence and survey year, in the event that confounding involving these variables might still occur. In addition to baseline (2003) HIV prevalence, attending an FRU ANC, reporting rural residence and being illiterate remained significant predictors of HIV infection (Table 2). In addition, the average annual decline in HIV prevalence per year in the IPI districts was 12% greater per year [95% confidence interval (CI) 3–21%; P = 0.01], compared with the non-IPI districts (where the decline was not significant). Table 3 shows the standardized HIV prevalence rates per year, broken down by IPI and non-IPI districts. Between 2003 and 2007, there was a standardized overall decline in HIV prevalence among ANC attenders under the age of 25 years of approximately 56% in IPI districts, compared with approximately 5% in the non-IPI districts.
We have observed a marked decline in HIV prevalence among ANC attenders in Karnataka state from 2003 to 2007. This decline occurred in all age groups, and is statistically significant, but was particularly marked in women under the age of 25 years, declining from 1.40% in 2003 to 0.77% in 2007. HIV infections in young antenatal women are more likely to represent recent infections, and therefore reflect recent trends in HIV transmission dynamics. We have also seen that the majority of the decline occurred in the IPI districts. The multivariate statistical model showed that the average annual decline in HIV prevalence among ANC attenders in the IPI districts was approximately 12% greater than in the non-IPI districts. It is a tenet of the intensive intervention programme that the prevention of HIV transmission from FSW to their clients, largely through increased condom use, as well as treatment and prevention of other STI, will result in lower rates of HIV infection in male clients, and therefore less HIV transmission to their other sexual contacts, including their spouses . This should then be reflected in lower HIV prevalence rates among ANC attenders, particularly those in younger age groups, who are more likely to have recently become sexually active. Our findings are consistent with this hypothesis, although the magnitude of the decline was somewhat greater, and occurred over a shorter period of time than might have been expected from the intervention alone . As the intensive intervention was not assigned randomly to districts, however, it cannot be ruled out that different epidemic phases in the districts, or unmeasured systematic differences between IPI and non-IPI districts in behavioural or other population-level factors, may have contributed to the differential declines, and thereby biased our findings.
Over the past two decades, HIV surveillance among ANC attenders has been used as a principal method for analysing and monitoring trends in HIV transmission in the general population [22–28]. It has generally been the only source of HIV prevalence data that is readily available, involves a large segment of the population, and is collected on a regular basis. In different countries and time periods, such prevalence trends have been shown generally to increase during the early years of HIV epidemics, followed by stabilization of prevalence levels, and in more recent years, by declining trends in many countries. It is unclear, however, whether stabilizing or declining prevalence trends reflect real stabilizing or declining HIV incidence rates, or rather reflect other factors, such as high levels of mortality or migration. Indeed, cohort studies from Uganda and Tanzania have suggested the latter [29,30]. In other settings, however, declines in HIV prevalence do seem to have been associated with reductions in HIV incidence, largely through reductions in sexual risk behaviour [31–34], and this notion has been supported by mathematical modelling studies .
The extent to which HIV prevalence among ANC attenders reflects HIV prevalence in the general population of adult women, or adult men for that matter, is not always clear. Over 30 countries have now undertaken population-based demographic and health surveys, in which representative samples of the adult population are sampled, and tested for HIV . In countries with concentrated epidemics, such as India, these population-based surveys have generally shown lower HIV prevalence rates than seen in sentinel surveillance data from ANC attenders. The Joint United Nations Joint Programme on HIV/AIDS (UNAIDS) now estimates that HIV prevalence estimates from general population surveys are approximately 80% of those observed among ANC attenders in the same locations . Studies from a number of African countries have, however, shown that HIV prevalence in ANC attenders can also underestimate HIV prevalence in the general adult female population, because of reduced fertility among HIV-infected women, patterns of contraception use, mobility patterns, age of marriage, age-specific parity and the age distribution of ANC attenders [38–41]. In a recent study from South Africa, population-based estimates of HIV prevalence among all women and pregnant women were significantly lower than that those among ANC attenders, but it was unclear which estimates were more reflective of reality in the general population . The authors concluded that in areas where antenatal care coverage and contraceptive use are relatively high, HIV prevalence is underestimated in population-based surveys because of the unrepresentativeness of the population-based sample, according to age, residence and probably HIV status; whereas HIV prevalence in surveys of ANC attenders generally overestimates the true prevalence because of selection bias in terms of age of sexual debut and contraceptive use. Population-based surveys may also undersample high-risk populations, leading to the underestimation of HIV prevalence .
In India, HIV prevalence estimates in the general population have recently been revised downwards, largely as a result of data from the population-based National Family Health Survey, round 3 (NFHS-3) carried out in 2006 . NFHS-3 found infection rates among adults to be considerably lower than those observed in ANC attender surveillance, which had been one of the major inputs used to derive previous estimates. The figures from NFHS-3 for HIV prevalence in Karnataka state were 0.69% overall (0.85% among men and 0.54% among women) . This compares with the ANC attender sentinel surveillance figure of 1.13% for 2006, i.e. 39% lower overall, and 52% lower compared with all women. In a population-based survey in the Guntur district of neighbouring Andhra Pradesh state conducted in 2004–2005, HIV prevalence overall was 1.72% (1.74% among men and 1.72% among women), compared with 3% observed in ANC attender sentinel surveillance . This differential was attributed to the preferential use of public hospitals by people in lower socioeconomic strata (who are also at higher risk of HIV infection), as well as the selective referral of HIV-positive individuals to public hospitals. In a general population-based survey undertaken in Bagalkot district in northern Karnataka in 2003, HIV prevalence was 2.9% overall (2.5% among women and 3.3% among men), which was similar to that seen in ANC attender sentinel surveillance for the district (3.1%) . Similarly, a general population-based survey in Mysore district in southern Karnataka in 2005–2006 found an overall HIV prevalence in the general population of 0.8%, just less than the prevalence of 1.0% found among ANC attenders in Mysore in 2006 of 1% .
Declining trends in HIV prevalence in India, as determined from sentinel surveillance among ANC attenders under the age of 25 years, have been reported from four states in south India, using sentinel surveillance data from 2000–2004 [18,47]. Karnataka state was included in this analysis, although the decline in Karnataka was small, and as indicated above, sentinel surveillance coverage before 2003 was incomplete and sampling sites changed each year. A declining trend in HIV prevalence has also been reported recently from Pune, in neighbouring Maharashtra state . The Pune study was conducted among young, recently married, monogamous primigravid women attending ANC, so HIV infections in this group are likely to be recent infections, and HIV incidence was approximated through estimates of person-time exposure. Between 2002 and 2006, HIV incidence declined from 2.2 to 0.73 per 100 person-years, paralleling declines observed in HIV prevalence among ANC attenders during that period. The authors attributed this decline to decreased high-risk sexual behaviour among young, recently married men, contributing to a decreasing risk of HIV transmission to their wives.
There are limitations to analysing and comparing data obtained from sentinel surveillance, and attributing trend differentials on an ecological basis to specific activities or events. It is difficult to measure district-level variability precisely in programme coverage or quality, and changes in intervention intensity over time, although we have shown that condom distribution per FSW was much greater in the IPI districts. The intervention districts were also not chosen randomly, but districts that were felt a priori to be associated with a higher risk of HIV tended to be selected for the intensive intervention programme, although this was not always the case. We tried to control for variability in HIV risk among districts by including HIV prevalence per district at baseline (2003) in the statistical model, but there may be other, unknown factors that are important in determining HIV prevalence, which we could not capture. For example, it may be that the higher prevalence districts that were overrepresented among the IPI districts were in a later epidemic phase than the other districts, and that the decline in ANC attender prevalence had already begun before the intervention programme was put in place.
Whatever the reasons for the decline in HIV prevalence observed in sentinel surveillance among ANC attenders in Karnataka, there seems little doubt now that the decline has been real, and it seems likely that at least one of the major reasons for the decline has been the intensive HIV preventive programmes that have been undertaken over the past 5 years, within both the governmental and non-governmental sectors. An added benefit of the decline in HIV prevalence among pregnant women, whatever the cause, is the prevention of maternal to child transmission. There are approximately 1.2 million births each year in Karnataka, so a reduction in HIV prevalence among pregnant women of 0.6%, as has occurred between 2003 and 2007, translates into 7200 fewer HIV-infected pregnant women in 2007. Approximately 30% of infants born to these women would have been HIV infected, unless covered by programmes for the prevention of maternal to child transmission of HIV. The reduced HIV prevalence in the population of pregnant women would thus result in over 2000 HIV infections among newborns having been prevented in 2007. This compares to less than 200 such infections having been prevented in Karnataka in 2007 through screening for HIV in pregnancy and providing HIV-positive pregnant women and their newborns with antiretroviral therapy to prevent HIV transmission, as estimated from prevention of parent to child transmission programme data (Karnataka State AIDS Prevention Society, personal communication). In 2007, just over 202 000 pregnant women were screened for HIV in Karnataka, of which 2599 tested positive, and 858 were treated with nevirapine to prevent maternal to child HIV transmission. If 30% of the 858 women (257) would have had positive newborns without treatment, and if two-thirds of those were prevented by nevirapine, that would amount to approximately 172 cases of HIV prevented in newborns.
In conclusion, this study supports the notion that scaled-up, intensive, targeted HIV preventive interventions among high-risk groups can have a measurable and relatively rapid impact on HIV transmission in the general population, as represented by young ANC attenders. Such focused intervention programmes should be rapidly taken to scale in all HIV epidemics, and especially in concentrated epidemics such as is being experienced in India.
Sponsorship: Support for this study was provided by the Bill and Melinda Gates Foundation.
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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