India currently has an estimated 2.5 million HIV-infected persons (though estimates have been as high as 5.7 million in the past years),1-3 the majority (63%) of whom reside in the 4 southern states of Maharashtra, Karnataka, Andhra Pradesh, and Tamil Nadu.4 The focus in India has been on the predominantly heterosexual epidemic (estimated 84% of infections)5 and its gradual dissemination over the years from sex workers to monogamous housewives.6 It is only in the northeastern region of India that injection drug users (IDUs) receive appreciable attention as the epidemic in this region is driven by injection drug use.7
It has increasingly been recognized that IDUs exist outside of the northeastern region of India, but these epidemics have been largely ignored. For example, Tamil Nadu is home to an estimated 10,000-15,000 IDUs8 and according to the 2006 sentinel surveillance report released by the National AIDS Control Organization, India, is the state with the highest HIV prevalence among IDUs in India.4 Yet, there are few community-based reports of HIV prevalence and risk behaviors among IDUs in Tamil Nadu. Furthermore, little is known about the prevalence of coinfection with hepatitis C virus (HCV) and hepatitis B virus (HBV) infection, which occur frequently among IDUs.9-12
The objective of this analysis was to characterize the baseline prevalence of HIV infection and associated coinfections (eg, HCV and HBV) among a cohort of IDUs in Chennai, India. We further characterize correlates of prevalent HIV infection and recent risk behaviors among HIV-positive and -negative IDUs.
In March 2005, a longitudinal cohort study aimed at measuring the incidence of HIV, HBV, and HCV among IDUs and examining the natural history of drug abuse in Chennai was initiated through the YR Gaitonde Centre for Substance Abuse-Related Research located in north Chennai. We report here on the baseline findings of this cohort. YR Gaitonde Centre for Substance Abuse-related Research was established in November 2004 to provide HIV counseling and testing services to marginalized populations such as IDUs. YR Gaitonde Centre for Substance Abuse-related Research is a branch of the YR Gaitonde Medical Education and Research Foundation, which includes the YR Gaitonde Centre for AIDS Research and Education, a nongovernmental, not-for-profit organization, which has been involved in HIV-related research since the mid-1990s and has provided medical and psychosocial care to more than 12,000 individuals living with HIV/AIDS. This study was approved by the YR Gaitonde Centre for AIDS Research and Education and the Johns Hopkins School of Public Health institutional review boards.
A convenience sample of IDUs from various regions of Chennai was recruited by field staff acquainted with IDUs in Chennai and their injection venues. To be eligible for the longitudinal study, IDUs had to (1) be able to provide written informed consent for screening, (2) be at least 18 years of age, and (3) have injected at least once in the prior 6 months. A total of 924 IDUs were screened for HIV between March 31, 2005, and March 10, 2006. All participants received pre- and post-test counseling. Participants also received information/counseling on safer injecting practices and sexual risk reduction counseling. Twelve participants withdrew after screening, leaving 912 of whom 272 tested positive for HIV and were referred to the on-site clinic for further medical evaluation.
Three trained interviewers administered standardized demographic and risk assessment questionnaires to participants at baseline. HIV serostatus was determined using double enzyme-linked immunosorbent assay testing (Murex HIV-1.2.O; Abbott Murex, United Kingdom, and Vironostika HIV Uni-form II Ag/Ab, BioMérieux, Boxtel, The Netherlands). If the results from the 2 tests were discrepant, participants were invited to return for further testing at 3 months. Hepatitis C serostatus was diagnosed by the presence of antibodies to HCV (anti-HCV) using the Murex Anti-HCV kit (Abbott Murex, Republic of South Africa), and chronic HBV infection was diagnosed by the presence of hepatitis B surface antigen (HBsAg; Hepanostika HBsAg Uniform II, BioMérieux).
The χ2 and Mann-Whitney tests were used to compare demographic variables for HIV-positive and -negative IDUs. Univariate and multivariate Poisson regression with robust variance estimates were used to estimate prevalence ratios (PRs) for correlates of prevalent HIV infection.13,14 Logistic regression was not performed, as odds ratios generally overestimate the association between a variable and an outcome if the outcome is common (>10%).15 We report the fully saturated multivariate model versus the parsimonious model to minimize bias in our estimates.16 We further compared the prevalence of current risk behaviors by HIV serostatus using χ2 tests. As there were only 3 female IDUs (of whom 1 was HIV positive), they were excluded from all analyses. A P value <0.05 was used to indicate statistical significance. All statistical analyses were performed using Intercooled STATA version 10.0 (College Station, TX).
Description of the Study Population
The median age of the 909 male participants was 35 years (interquartile range [IQR]: 30-40). Almost all (98.3%) participants were of Tamil ethnicity; 58% were married, 32.1% were single, 4% were separated, and the remaining were either widowed or divorced (Table 1). Compared with HIV-negative IDUs, HIV-positive IDUs were more often single (36.5% vs 30.3%) and separated (8.12% vs 2.66%) and less often married (50.2% vs 61.6%) (P value = 0.001). Twenty-eight percent reported no formal education. The majority of the participants worked for daily wages and earned less than USD 36 per month. The median age at first injection drug use for non-medicinal purposes was 25 years, with HIV-positive IDUs initiating drug use at a younger median age (24 vs 25 years; P < 0.001).
Prevalence of HIV, HBV, and HCV
Overall, 29.8% were infected with HIV, 62.1% were exposed to HCV (anti-HCV), and 11.1% were chronically infected with HBV (HBsAg). One in 4 IDUs (25.7%) screened positive for antibodies to both HIV and HCV. Nearly all (95.2%) HIV-positive IDUs also screened positive for anti-HCV compared with 48% of HIV-negative IDUs. The prevalence of chronic HBV infection in HIV-positive and -negative IDUs was 9% versus 11.7%, respectively. All IDUs who were chronically infected with HBV (HBsAg positive) were also positive for anti-HCV. Overall 25 persons (2.74%) were positive for HIV and anti-HCV and were chronically infected with HBV; among HIV-positive IDUs, the prevalence of anti-HCV and HBsAg was 9.19%.
Correlates of Prevalent HIV Infection
In univariate analysis, IDUs who were either single or separated, participants with a longer duration of injection, and those who reported having injected at a dealer's place in the past and having a tattoo had significantly higher HIV prevalence (P < 0.05; Table 2). Alcohol consumption was negatively associated with prevalent HIV infection (P < 0.05). Age and history of ever sharing needles were not associated with HIV prevalence.
In multivariate analysis, duration of injection drug use ≥11 years [PR: 3.02; 95% confidence interval (CI): 1.36 to 6.72] and 6-10 years (PR: 2.45; 95% CI: 1.11 to 5.44) was significantly associated with a higher prevalence of HIV (Table 2). Participants with a history of injecting at the dealer's place (PR: 1.57; 95% CI: 1.29 to 1.91) and a history of tattooing (PR: 1.78; 95% CI: 1.35 to 2.36) remained more likely to be HIV positive. Alcohol consumption more than once a week (PR: 0.48; 95% CI: 0.38 to 0.62) remained negatively associated with HIV prevalence.
Recent Risk Behaviors
HIV-positive IDUs were more likely to have injected in the prior month with 26% having injected more than 30 times compared with 17.4% of HIV-negative IDUs (P < 0.01). HIV-positive IDUs were also more likely to have injected only heroin in the prior month (84.5% vs 66.9%) compared with HIV-negative IDUs who were more likely to have injected buprenorphine (19.9% vs 5.8%) (P < 0.001). HIV-positive and -negative IDUs had similar needle cleaning (HIV positive vs HIV negative: 57.2% vs 54.4%) and sharing practices (HIV positive vs HIV negative: 29.2% vs 33.7%) and similar rates of non-injection drug use (HIV positive vs HIV negative: 83% vs 84.6%). HIV-positive IDUs were less likely to have had sexual intercourse in the prior 1 month (28.9% vs 46.1; P < 0.001).
We observed a high prevalence of HIV infection, HIV/HCV coinfection, and associated risk behaviors among this community-based cohort of IDUs in Chennai, India. Understanding the true burden of disease in a community and the prevalent risk behaviors are critical for designing effective prevention interventions to curtail the spread of HIV and other infectious diseases among IDUs and from IDUs to their sexual partners and the general population.
Our study represents one of the largest community-based efforts among IDUs in India. The majority of existing HIV prevalence data in India, including those among IDUs, are derived from sentinel surveillance, which has inherent limitations. By comparison with other risk groups, there are few IDU-specific sentinel surveillance sites and the estimates have varied dramatically from year to year. In Tamil Nadu, for example, between 2003 and 2006, estimates of HIV prevalence among IDUs varied from 18% to 64%.4,17 Thus, it is critical that sentinel surveillance estimates are supplemented with community-based estimates of disease prevalence. Our results are comparable with a prior community-based study conducted among a much smaller sample of 226 married IDUs in Chennai between April and July 2003 (HIV prevalence was 29.2%).18 This high prevalence translates into a large number of HIV-positive IDUs living in Chennai alone and more broadly in India, where an estimated 1.1 million IDUs live.19 Not surprisingly, all but 3 IDUs recruited to participate in this study were male, which is consistent with other reports from Chennai suggesting that there are few female IDUs in Chennai.20,21
The high prevalence of anti-HCV (86%) and both HBsAg and anti-HCV (9.2%) is analogous to IDUs in other settings and the limited reports from India9,11,12,21 and has multiple implications. First, coinfection with HIV and HCV has been associated with more rapid progression of liver disease and higher rates of mortality.22 Similar associations have been observed with hepatitis B as well.23 Treatments are available for all 3 infections, but they are rarely received by IDUs in India. At the end of 2004, only 400 of the 35,000 estimated to be on highly active antiretroviral therapy (HAART) in India are IDUs-all were from the northeast.24 Delivery of HAART in this population will be difficult as even in Western countries IDUs tend to have limited access to HAART compared with other groups, and they have also been shown to experience higher rates of treatment failure.25 Furthermore, in India, nevirapine is included in the preferred first-line HAART regimens at most treatment centers. However, severe hepatotoxicity has been observed at a higher frequency among persons coinfected with HBV/HCV receiving a nevirapine-containing HAART regimen compared with protease inhibitor- and efavirenz-based regimens, which are more expensive in India.26 Innovative methods of HAART delivery such as directly administered antiretroviral therapy27 and alternate regimens will need to be considered and evaluated among IDUs in the Indian setting given these high rates of coinfection with the hepatitis viruses.
Access to treatment will be critical for those who are already infected, but efforts also need to focus on preventing new infections, and thus, it is critical to understand what puts IDUs at risk for HIV. Evidence from developed countries have consistently observed that more frequent injection, needle sharing, attending shooting galleries, and high-risk sexual behavior are risk factors for HIV among IDUs.28-30 In this study, the association of some factors with HIV such as longer duration of injection and having ever injected drugs at a dealer's place are consistent with what has been observed by other Indian studies and those from the West.9,18,30 We also observed an association with a history of tattooing, which has been associated with HIV infection in developing countries.18,31 Interestingly, we observed that heavy alcohol use was associated with lower HIV prevalence. Of note, IDUs who reported the heaviest alcohol intake also reported lower frequency of injection. Furthermore, most drug users who combined alcohol with injection drugs (93%) identified insufficient intoxication from the injected drug as the primary reason for combining the 2, suggesting that those who drank were injecting less.
In addition to having a greater frequency of lifetime risk behaviors, HIV-positive IDUs were as or more risky compared with HIV-negative IDUs with respect to recent risk behaviors. They were significantly more likely to be injecting heroin and had a higher frequency of injection. It has been noted that in the Indian setting, heroin users tend to inject more frequently and more often at a dealer's place, are more likely to share equipment, and also are more likely to have larger needle-sharing networks.21 Furthermore, buprenorphine is a pharmaceutical agent that is usually purchased over-the-counter in liquid form by IDUs, whereas heroin is generally acquired from a dealer. During our interactions with the study participants, we learned that IDUs typically have arrangements with pharmacists in their locale wherein the pharmacist selling the IDU a vial of buprenorphine also compels the IDU to buy a sterile needle/syringe at the time of purchase to maximize profits.
There were no differences in reported recent needle sharing or cleaning of needles between HIV-positive and -negative IDUs. However, it is important to note that at least 30% of both HIV-negative and -positive IDUs reported sharing a needle in the prior month, suggesting that high-risk behaviors are common. Although more than 50% of both groups reported cleaning a needle at least once in the prior 1 month, the majority of IDUs used only tap water or parts of their clothing to clean injection equipment, a finding that is consistent with other studies in India.12,20,21 The majority of the IDUs in this study learned their HIV status for the first time through this study, which may explain the finding that HIV-positive IDUs were as or more risky than HIV-negative IDUs. Monitoring behaviors during follow-up visits will allow us to examine the impact of counseling and testing and the impact of knowledge of HIV serostatus on risky injection practices. The fact that most IDUs were diagnosed with HIV for the first time through this study also indicates the lack of perception of HIV risk and/or lack of access to voluntary and counseling testing services. Furthermore, few IDUs in this sample had any access to preventive services such as drug treatment or needle exchange. Finally, none of the HIV-positive IDUs were enrolled in HIV treatment or care programs.
Interestingly, HIV-positive IDUs were significantly less likely to report recent sexual intercourse and may reflect that they were more heavy injectors. However, it is important to note that 40.9% of this cohort reported a history of sexual intercourse in the month before their baseline assessment. Seventy-five IDUs reported having more than 1 female sexual partner in the prior 1 month, whereas 15 reported having sex with other men in the prior month. Thus, a sizable proportion is practicing high-risk sexual behaviors. It is often through these high-risk behaviors that HIV and/or HBV is transmitted from IDUs to their sexual partners as has been reported in Tamil Nadu18 and Manipur.32
The primary limitation of our study was the inability to ascertain the temporality of recent risk behaviors and prevalent HIV infection given our cross-sectional design. Another limitation was the use of HBsAg for the diagnosis of HBV infection and antibodies to HCV for the diagnosis of HCV infection. HBsAg is a marker of chronic HBV infection and thus underestimates the true lifetime prevalence of exposure to HBV infection among these IDUs. A core antigen study from Manipur by Saha et al11 detected antibodies to HBV (anti-HbC) among all IDUs in their sample, implying that almost all IDUs had been exposed to HBV. Nevertheless, disease progression is unlikely to occur in HBsAg-negative patients, so our data reflect the true disease burden of HBV.33 Conversely, we used an antibody test for the diagnosis of HCV infection, which reflects exposure rather than chronic infection. In most settings, approximately 15%-20% spontaneously clear virus34; therefore, our prevalence of HCV likely overestimates the true prevalence of chronic HCV infection by this factor.
The findings in this cohort of IDUs in Chennai, India, are very similar to the early HIV epidemics among IDUs in the United States and Europe in the late 1980s, both in terms of the prevalence of HIV, HBV, and HCV and their injecting practices.28-30,35 The incidence subsequently declined among these IDUs primarily due to interventions such as needle exchange, drug substitution/treatment programs, and health education of IDUs.36-38 However, despite some success among IDUs and men who have sex with men who were the focus of interventions in the early years of the HIV epidemic in the United States, new risk groups have emerged in recent years.39 For example, in the United States, HIV incidence is currently on the rise among minority women whose primary risk factor for infection is heterosexual sex. India may face a similar situation if they focus only on the well-described heterosexual epidemic and ignore emerging HIV epidemics, such as the epidemics among IDUs in regions of India besides the northeast, in their planning of prevention and treatment programs.
In conclusion, there is a large burden of HIV and other blood-borne infections among IDUs in Chennai coupled with high-risk behaviors. Interventions that helped curtail the HIV epidemic among IDUs in the West, such as education on safe injection practices, needle exchange programs, drug substitution, and treatment programs, need to be implemented and evaluated for use in India to prevent further spread of the epidemic among IDUs and from IDUs to their sexual partners. Furthermore, measures should be taken to ensure that the IDUs already infected with HIV have adequate access to care and support.
The authors thank the staff at YR Gaitonde Centre for Substance Abuse-Related Research and YR Gaitonde Centre for AIDS Research and Education who helped with the implementation of this study, especially Mr Jayakumar and Mr Guru who helped with the development of the database and data entry, and our field staff. We thank Joel E. Gallant, MD, MPH, for his guidance with the management of the HIV-infected IDUs. We would also like to thank Drs Padmanesan Narasimhan, Balachander, and Ramnath Subburaman who helped with the functioning of the on-site HIV clinic. Sunil S. Solomon had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Most importantly, we would like to thank the participants without whom this article would not have been possible.
1. Dandona L, Lakshmi V, Kumar GA, et al. Is the HIV burden in India being overestimated? BMC Public Health
4. National AIDS Control Organization (NACO), India. HIV Sentinel Surveillance and HIV Estimation, 2006. Available at: http://22.214.171.124/upload/Documents/HIV
%20Sentinel%20Surveillance%20and%20HIV%20Estimation,%202006.pdf. Accessed January 3, 2008.
6. Gangakhedkar RR, Bentley ME, Divekar AD, et al. Spread of HIV infection in married monogamous women in India. JAMA
7. Steinbrook R. HIV in India-a complex epidemic. N Engl J Med
8. Dorabjee J, Samson L. A multi-centre rapid assessment of injecting drug use in India. Int J Drug Policy
9. Eicher AD, Crofts N, Benjamin S, et al. A certain fate: spread of HIV among young injecting drug users in Manipur, north-east India. AIDS Care
10. Panda S, Chatterjee A, Bhattacharjee S, et al. HIV, hepatitis B and sexual practices in the street-recruited injecting drug users of Calcutta: risk perception versus observed risks. Int J STD AIDS
11. Saha MK, Chakrabarti S, Panda S, et al. Prevalence of HCV & HBV infection amongst HIV seropositive intravenous drug users & their non-injecting wives in Manipur, India. Indian J Med Res
12. Sarkar K, Bal B, Mukherjee R, et al. Epidemic of HIV coupled with hepatitis C virus among injecting drug users of Himalayan West Bengal, eastern India, bordering Nepal, Bhutan, and Bangladesh. Subst Use Misuse
13. Behrens T, Taeger D, Wellmann J, et al. Different methods to calculate effect estimates in cross-sectional studies. A comparison between prevalence odds ratio and prevalence ratio. Methods Inf Med
14. Zou G. A modified poisson regression approach to prospective studies with binary data. Am J Epidemiol
15. McNutt LA, Wu C, Xue X, et al. Estimating the relative risk in cohort studies and clinical trials of common outcomes. Am J Epidemiol
16. Robins JM, Greenland S. The role of model selection in causal inference from nonexperimental data. Am J Epidemiol
17. National AIDS Control Organization (NACO), India. HIV/AIDS Epidemiological Surveillance & Estimation Report for the Year 2005. Available at: http://nacoonline.org/fnlapil06rprt.pdf
. Accessed February22, 2007.
18. Panda S, Kumar MS, Lokabiraman S, et al. Risk factors for HIV infection in injection drug users and evidence for onward transmission of HIV to their sexual partners in Chennai, India. J Acquir Immune Defic Syndr
19. Aceijas C, Friedman SR, Cooper HL, et al. Estimates of injecting drug users at the national and local level in developing and transitional countries, and gender and age distribution. Sex Transm Infect
. 2006;82(Suppl 3):iii10-iii17.
20. AIDS Prevention and Control (APAC), India. HIV Risk Behavior Surveillance Survey in Tamil Nadu Wave X- 2005: Chennai, India. APAC-VHS; 2006.
21. Kumar MS, Mudaliar S, Thyagarajan SP, et al. Rapid assessment and response to injecting drug use in Madras, south India. Int J Drug Policy
22. Lumbreras B, Jarrin I, del Amo J, et al. Impact of hepatitis C infection on long-term mortality of injecting drug users from 1990 to 2002: differences before and after HAART. AIDS
23. Thio CL, Seaberg EC, Skolasky R Jr, et al. HIV-1, hepatitis B virus, and risk of liver-related mortality in the Multicenter Cohort Study (MACS). Lancet
24. Aceijas C, Oppenheimer E, Stimson GV, et al. Antiretroviral treatment for injecting drug users in developing and transitional countries 1 year before the end of the “Treating 3 million by 2005. Making it happen. The WHO strategy” (“3 by 5”). Addiction
25. Lucas GM, Cheever LW, Chaisson RE, et al. Detrimental effects of continued illicit drug use on the treatment of HIV-1 infection. J Acquir Immune Defic Syndr
26. Sulkowski MS, Thomas DL, Mehta SH, et al. Hepatotoxicity associated with nevirapine or efavirenz-containing antiretroviral therapy: role of hepatitis C and B infections. Hepatology
27. Lucas GM, Mullen BA, Weidle PJ, et al. Directly administered antiretroviral therapy in methadone clinics is associated with improved HIV treatment outcomes, compared with outcomes among concurrent comparison groups. Clin Infect Dis
28. Marmor M, Des Jarlais DC, Cohen H, et al. Risk factors for infection with human immunodeficiency virus among intravenous drug abusers in New York City. AIDS
29. Rezza G, Titti F, Tempesta E, et al. Needle sharing and other behaviours related to HIV spread among intravenous drug users. AIDS
30. Vlahov D, Munoz A, Anthony JC, et al. Association of drug injection patterns with antibody to human immunodeficiency virus type 1 among intravenous drug users in Baltimore, Maryland. Am J Epidemiol
31. Akeke VA, Mokgatle M, Oguntibeju OO. Tattooing and risk of transmitting HIV in Quthing prison, Lesotho. Int J STD AIDS
32. Panda S, Chatterjee A, Bhattacharya SK, et al. Transmission of HIV from injecting drug users to their wives in India. Int J STD AIDS
33. Giovanna F, Bortolotti F, Francesco D. Natural history of chronic hepatitis B: special emphasis on disease progression and prognostic factors. J Hepatol
34. Villano SA, Vlahov D, Nelson KE, et al. Persistence of viremia and the importance of long-term follow-up after acute hepatitis C infection. Hepatology
35. Van Ameijden EJ, Van den Hoek JA, Mientjes GH, et al. A longitudinal study on the incidence and transmission patterns of HIV, HBV and HCV infection among drug users in Amsterdam. Eur J Epidemiol
36. Des Jarlais DC, Perlis T, Arasteh K, et al. Reductions in hepatitis C virus and HIV infections among injecting drug users in New York City, 1990-2001. AIDS
. 2005;19(Suppl 3):S20-S25.
37. Kral AH, Lorvick J, Gee L, et al. Trends in human immunodeficiency virus seroincidence among street-recruited injection drug users in San Francisco, 1987-1998. Am J Epidemiol
38. Mehta SH, Galai N, Astemborski J, et al. HIV incidence among injection drug users in Baltimore, Maryland (1988-2004). J Acquir Immune Defic Syndr
39. Centers for Disease Control and Prevention. Epidemiology of HIV/AIDS-United States, 1981-2005. MMWR Morb Mortal Wkly Rep