Changes in HIV Prevalence and Risk Among New Injecting Drug Users in a Russian City of High HIV Prevalence

Platt, Lucy PhD*; Rhodes, Tim PhD*; Hickman, Matthew PhD†; Mikhailova, Larissa PhD‡; Lisetsky, Konstantin PhD§; Sarang, Anya∥; Lewis, Kim MSc¶; Parry, John PhD¶

JAIDS Journal of Acquired Immune Deficiency Syndromes: 15 April 2008 - Volume 47 - Issue 5 - pp 623-631
doi: 10.1097/QAI.0b013e318165dbf7
Epidemiology and Social Science

Objective: To measure HIV prevalence and associated risk factors among recent initiates into drug injecting in 2001 and 2004 in Togliatti City, Russian Federation.

Design: Two unlinked, anonymous, cross-sectional, community-recruited surveys of injecting drug users (IDUs) with oral fluid samples for anti-HIV testing.

Methods: IDUs completed an interviewer-administered questionnaire, and oral fluid samples were tested for antibodies to HIV. Demographic characteristics and injecting risk behaviors were compared between subsamples of IDUs who reported injecting for 3 years or less in each of the survey years, 2001 (n = 138) and 2004 (n = 96). Univariable and multivariable analyses explored risk factors with anti-HIV among these new injectors.

Results: Among IDUs overall, although HIV prevalence was high, a lower prevalence was found in 2004 (38.5%, 95% confidence interval [CI]: 34.1 to 42.9) than in 2001 (56%, 95% CI: 51.2 to 60.8). A significantly lower prevalence of HIV was found among new injectors in 2004 (11.5%, 95% CI: 5.0 to 17.9) than in 2001 (55.2%, 95% CI: 46.7 to 63.8). Proportionally, fewer new injectors reported injecting daily, injecting with used needles/syringes, and frontloading in 2004 compared with 2001. Decreased odds of anti-HIV were associated with being recruited in 2004 and with a history of drug treatment. Increased odds of HIV were associated with exchanging sex, duration of injection, and frontloading.

Conclusions: Findings indicate a decrease in HIV prevalence among new injectors between 2001 and 2004 and emphasize the role of provision of needle/syringes through pharmacies and providing access to voluntary HIV testing. These findings have implications for other cities in which explosive HIV outbreaks have occurred.

From the *Centre for Research on Drugs and Health Behaviour, Public and Environmental Health Research Unit, Department of Public Health and Policy, London School of Hygiene and Tropical Medicine, London, United Kingdom; †Department of Social Medicine, University of Bristol, Bristol, United Kingdom; ‡City Narcological Services and NGO Parents Against Drugs, Togliatti City, Samara Oblast, Russian Federation; §Samara State University, Samara Oblast, Russian Federation; ∥Russian Harm Reduction Network, Ilimskaya Street 4-1-38, 127576 Moscow, Russia; and the ¶Health Protection Agency and Department of Public Health and Policy London School of Hygiene and Tropical Medicine, London, United Kingdom.

Received for publication August 17, 2007; accepted December 19, 2007.

Funded by the Department for International Development.

Correspondence to: Lucy Platt, PhD, Centre for Research on Drugs and Health Behaviour, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, United Kingdom (e-mail:

Article Outline

Evidence points to an HIV epidemic in the Russian Federation contained primarily among injecting drug users (IDUs) that has occurred rapidly with explosive outbreaks at a city level.1-4 Evidence from a cohort study of IDUs recruited between 2001 and 2002 reports a high prevalence of 30% and an incidence of 4.5 per 100 person-years indicative of a rapid onset of HIV.5 Documented research showing a reduction in the prevalence of HIV among IDUs in high-prevalence settings is limited. The available evidence suggests that prevalence can take many years to stabilize, as is illustrated in the cases of New York, Edinburgh, and Bangkok, which have all witnessed epidemics of HIV among IDUs.6-8

The World Health Organization recommends the use of enhanced or second-generation surveillance, drawing on behavioral and biologic data in targeted population groups, to monitor the dynamics of risk and changing epidemics and emphasizes the importance of sampling young populations as measures of incidence.9,10 Some research has also shown that new injectors tend to engage in riskier injecting practices than IDUs with longer injecting careers11,12 Other research has shown that newer injectors adopt the reduced risk injection practices of longer term injectors in the context of outbreaks of HIV, however.13

Monitoring HIV infections and risk behaviors among recent initiates into injection is important, because the perpetuation of HIV is determined by the number of people who start injecting, their injecting and sexual risk behaviors, and the prevalence and incidence within this population. There is increasing evidence of the potential for sexual transmission of HIV among IDUs and their sexual partners in Russia and the former Soviet Union, which is partially related to a close interplay between sex work and drug injecting.5,14-17 There is evidence of sexual transmission between IDUs and their noninjecting sexual partners.14,17-19 A recent multicity Russian study found elevated odds of syphilis associated with sex work among IDUs, indicating the potential for sexual transmission.20 Among IDUs attending a syringe exchange in St. Petersburg, a higher prevalence of syphilis was found among sex workers compared with non-sex workers (odds ratio [OR] = 8.6, 95% confidence interval [CI]: 2.5 to 31).21 The proportion of new HIV diagnoses in Russia attributed to sexual transmission has increased from 6% in 2001 to 32% in 2004, whereas over the same period, the proportion attributed to injection drug use has decreased from 94% to 67%.22 If sexual mixing is sufficient, there is a risk that the HIV epidemic in Russia may become less concentrated among IDUs and more generalized, which is of particular concern, given the high population prevalence of syphilis in many Russian cities.23,24

We undertook a community sample survey of HIV prevalence and risk behavior among IDUs in a high-prevalence Russian city and compared our findings with those of a similar study conducted in the same city 3 years previously.3,25,26 We measured changes in HIV prevalence and associated risk factors among IDUs reporting injecting 3 years or less from the 2 surveys and examined how the surveys contribute to second-generation surveillance.

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Alongside an analysis of new HIV case reports collated since 2000, we conducted an unlinked anonymous cross-sectional survey in 2004 of 476 IDUs recruited from nontreatment settings in Togliatti City (Samara Region, Russia), designed to replicate as closely as possible a baseline community-recruited survey of 426 IDUs conducted in 2001.3,25 To be eligible for either study, participants had injected drugs in the previous 4 weeks and consented to provide oral fluid samples for testing for anti-HIV-1 or anti-HIV-2 antibodies. Ethical approval was granted by the Riverside Research Ethics Committee, United Kingdom, with the support of the Togliatti City Department of Health. Only IDUs who reported injecting for 3 years or less were included in the analysis, which included 138 IDUs in 2001 and 96 in 2004.

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Sampling and Data Collection

The methods used in the 2001 survey are reported elsewhere.3,25,26 For the 2004 survey, IDUs were recruited through respondent-driven sampling (RDS), a methodology that combines chain referral sampling with a mathematic model that adjusts for nonrandom recruitment of the sample to provide population estimates of the characteristics of IDUs.27-29 Sampling begins with a set of initial subjects who serve as “seeds” for an expanding chain of referrals, with respondents from each chain or wave referring respondents from subsequent waves. The RDS method uses information on estimated network size to allow for the calculation of selection probabilities.28 To increase comparability with the 2001 sample,3 the RDS 2004 sample is treated as a standard chain referral sample in this analysis. Field workers (researchers from Samara State University and trained outreach workers) conducted structured survey interviews at fixed-site syringe exchanges and in community settings. In addition to the survey, we collated routine new HIV case reports between 2000 and 2005 by gender and risk factor.

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Anti-HIV Antibody Testing

Oral fluid specimens were collected from participants using the OraSure device (Orasure Technologies, Bethlehem, PA). All specimens were tested for the presence of human IgG, and those that had a concentration of >0.1 mg/L were tested for anti-HIV-1 and anti-HIV-2 antibodies. Specimens with insufficient levels of total IgG (<0.1 mg/L) were not tested for anti-HIV. Specimens were screened for HIV antibody using an IgG class-specific antibody-capture anti-HIV enzyme immunoassay (GACELISA), and the specificity of the reaction was initially confirmed by testing using the Oral Fluid Vironostika HIV-1 MicroElisa System (bioMérieux [UK] Ltd, Basingstoke, United Kingdom).30-33 Specimens nonreactive by the GACELISA were considered to be anti-HIV-negative, whereas specimens that tested reactive by GACELISA and Vironostika were considered to be anti-HIV-positive. Specimens that showed discordant results between the 2 tests were further tested by Western blot analysis, thereby resolving indeterminate results. When Western Blot tests could not resolve indeterminate enzyme immunoassay (EIA) results, such specimens were considered indeterminate and were removed from the final calculations. All anti-HIV testing took place at the Togliatti Fifth City Hospital Laboratory in collaboration with the UK Health Protection Agency.

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Statistical Analysis

First, we compared risk behaviors and characteristics between the 2001 and 2004 samples, limiting the analysis to IDUs who were recent initiates into injecting or new injectors, defined as injecting for 3 years or less. Pearson χ2 tests were used for categoric variables, and t tests with equal variance were used for continuous variables. Second, associations between antibodies to HIV (the outcome of interest) and covariables were explored univariably and by multiple logistic regression for the 2001 and 2004 samples combined but, again, limiting the analysis to IDUs who had injected for 3 years or less. Multivariable analysis followed a conceptual framework approach described previously.34-37 Analyses were conducted using STATA 7 (Stata Corp., College Station, TX). The effect of time was explored univariably and multivariably by fitting a dummy variable (2001 vs. 2004) univariably and within each group of the conceptual framework. A dummy variable for time was also fitted as an interaction with covariates. Interactions with P values <0.01 were taken to be strong evidence of interaction.

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City Context

Togliatti City is divided into 3 geographically distinct districts, Centralnii, Avtozavodskii (the largest), and Komsomolskii (the smallest). Census data suggest that the population of registered citizens was 740,636 in 2001, although the true number, including unregistered citizens, was more likely to be nearer to 1,000,000. Population size had scarcely increased by 2004, increasing slightly to 743,239. Evidence suggested a large population of IDUs in the city of 20,226 (95% CI: 16,971 to 24,749) in 2001, which corresponds to a population prevalence of 5.4% (95% CI: 4.5 to 6.6) of the registered population and 2.7% (95% CI: 2.4 to 3.5) of the total population, including unregistered citizens.38 Data using similar methods to estimate the IDU population in 2004 are not available.

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In 2001, a total of 426 IDUs were sampled, of whom 138 were recent initiates into injecting.3 In 2004, a total of 476 IDUs were sampled, of whom 96 were recent initiates into injecting. Table 1 compares the characteristics and injecting risk behaviors of recent initiates into injecting between 2001 and 2004.

Similar proportions of both samples were male, and the median age was 20 years in 2001 and 19 years in 2004. There was some evidence of a different distribution of injectors across the 3 districts of Togliatti. In 2001, proportionally more injectors were recruited from Avtozavodskaya (55.5%) compared with Centralni (19.2%) and Komsomolskii (15.3%), and in 2004, 64.6% were recruited from Avtozavodskii compared with 15.6% from Centralnii and 19.8% from Komsomolskii. There was no difference in the proportion of IDUs reporting attending higher education or main source of income between the 2 samples.

There was some difference in drug use behavior, with a significantly lower proportion of new injectors in 2004 (4.2%) reporting injecting daily compared with 2001 (43.8%; P < 0.001). The main drug injected in the past 4 weeks remained heroin, and similar proportions reported ever injecting homemade drugs (opiates or amphetamines). There were significant differences in reported injecting risk behaviors in the past 4 weeks over the 2 time frames. In 2004, proportionally fewer injectors reported injecting with a used needle/syringe (8.3% vs. 31.9%; P < 0.001), using a filter in which someone had previously put their needle/syringe to draw up drugs (18.7% vs. 60.9%; P < 0.001), frontloading (whereby a drug solute is squirted from a donor syringe into another by removing the needle; 6.3% vs. 33%; P < 0.001), or reusing the same needle more than once for injection (22.6% vs. 69.7%; P < 0.001) than in 2001. In 2004, however, proportionally more IDUs reported injecting with a prefilled syringe (14.6%) than in 2001 (4.3%; P < 0.01).

Similar proportions across the 2 time frames reported exchanging sex for money, drugs, or goods in the past 4 weeks. The proportions reporting ever having a sexually transmitted infection had decreased in 2004 (9.4%) compared with 2001 (20.3%; P = 0.03). In terms of environmental risk factors, similar proportions across the 2 samples reported a history of prison (∼6%) and being arrested by the police in the past 12 months (∼63%).

In terms of health service utilization, the main source of obtaining new needles/syringes continued to be pharmacies across the 2 times. Proportionally fewer IDUs reported having any contact with drug treatment or harm reduction services in 2004 compared with 2001, including experience of a state-provided drug treatment service (2.1% in 2004 vs. 18.8% in 2001; P < 0.001); ever visiting a syringe exchange (0% in 2004 vs. 6.7% in 2001; P = 0.01), or receiving clean needles or syringes from an outreach worker (1.1% in 2004 vs. 11.9% in 2001; P < 0.001). Proportionally more IDUs in 2004 reported ever having been tested for HIV than in 2001 (56.3% vs. 39.7%; P = 0.01).

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In the 2001 sample, overall HIV prevalence was 56.0% (95% CI: 51.2 to 60.8) and remained high among the subsample of recent initiates at 55.2% (95% CI: 46.7 to 63.8). In the 2004 sample, the overall prevalence of HIV among IDUs was 38.5% (95% CI: 34.1 to 42.9), and among recent initiates, it was 11.5% (95% CI: 5.0 to 17.9).

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Risk for Anti-HIV

Table 2 summarizes univariable and multivariable risk factors for anti-HIV among recent initiates into injecting recruited from the 2001 and 2004 samples. In the univariable analysis, decreased odds of anti-HIV were associated with being recruited in 2004 (OR = 0.1, 95% CI: 0.05 to 0.21) and with ever being tested for HIV compared with those who had not been tested (OR = 0.5, 95% CI: 0.30 to 0.91). Increased odds of anti-HIV were associated with being female versus male (OR = 2.1, 95% CI: 1.21 to 3.72) and with injecting drugs daily versus less than daily (OR = 1.9, 95% CI: 1.04 to 3.41). In terms of injecting risk behaviors, increased odds of anti-HIV were associated with injecting with a used needle/syringe in the past 4 weeks (OR = 2.4, 95% CI: 1.35 to 4.42), using a filter in which someone had previously put their needle/syringe to draw up drugs (OR = 2.6, 95% CI: 1.52 to 4.56), frontloading (OR = 4.7, 95% CI: 2.44 to 9.08), and reusing the same needle more than once for injecting (OR = 2.4, 95% CI: 1.29 to 4.44). Increased odds of anti-HIV were also associated with exchanging sex for money, drugs, or goods in the past 4 weeks (OR = 3.02, 95% CI: 1.44 to 6.33). Odds of anti-HIV increased by each year of injection (OR = 1.5, 95% CI: 1.14 to 2.00) but not with age (OR = 1.0, 95% CI: 0.92 to 1.06).

After adjustment, 5 variables remained associated with anti-HIV in the multivariable model. Decreased odds of anti-HIV remained associated with IDUs recruited in 2004 compared with 2001 (OR = 0.1, 95% CI: 0.05 to 0.25). Odds of HIV increased per year of injection (OR = 1.4, 95% CI: 1.01 to 2.0) and were higher among IDUs who reported frontloading in the past 4 weeks compared with those who had not (OR = 3.1, 95% CI: 1.44 to 6.79). Increased odds of anti-HIV were higher among IDUs who reported exchanging sex in the past 4 weeks compared with those who had not (OR = 2.5, 95% CI: 1.01 to 6.28). Decreased odds of anti-HIV were associated with IDUs who reported ever experiencing drug treatment compared with those with no experience (OR = 0.4, 95% CI: −0.14 to 0.95). There was no evidence of an interaction between time and any covariates.

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Routine HIV Case Reports

Table 3 presents routine surveillance data from the Togliatti City AIDS Center on all HIV-positive cases reported between 2000 and 2005 and their main attributed risk factor. In 2000, almost all new cases (97%) were associated with injection drug use. By 2005, this had decreased to 56.4%. In 2000, most HIV cases were among men (80%), but the distribution of new cases among men and women had equalized by 2005.

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Togliatti City is a setting characterized historically by an explosive outbreak of HIV and high HIV prevalence among injectors.3 Our findings indicate a large decrease in HIV prevalence among new injectors between 2001 and 2004, from 55% to 11.5% prevalence. These findings are indicative of a reduction in HIV prevalence among new injectors. This is supported by city HIV case reports, which show a decrease in the absolute number of new HIV cases in the same time frame and a decrease in the proportion of new cases associated with injection drug use.

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Risk Associated With HIV

In the multivariable analysis, new injectors reporting frontloading had 3 times the odds of HIV infection. There is evidence of HIV transmission linked to paraphernalia and indirect sharing practices, such as frontloading and backloading, but this remains limited.39,40 We also interpret the association between frontloading and increased odds of HIV as important because such a measure may be acting as a proxy of risk for injecting risk behavior, including direct needle and syringe sharing. Surveys of IDUs may be underreporting direct needle and syringe sharing.41 Qualitative studies have also emphasized that user interpretations of what constitutes “sharing” in relation to injecting risk may be different from that assumed by survey measures.42

We found elevated odds of HIV associated with sex work across the 2 samples. Studies among IDU sex workers suggest that the primary route of HIV transmission remains drug injecting and not sexual transmission and that IDU sex workers have a greater risk of infection related to injection than nonsex workers because of higher rates of borrowing injecting equipment and injecting in higher risk environments.25,43,44 It is nonetheless important to note recent evidence indicative of HIV seroconversion associated with sexual behavior among community-recruited IDU sex workers.45,46 City HIV case report data presented here show an increase since 2001 in the proportion of new HIV cases among women compared with men and a shift in the main attributed risk factor from injecting to sexual transmission. IDUs, and IDUs involved in sex work specifically, should be targets for sexual risk reduction interventions. After adjustment by sex work and duration of injection, new injectors engaged in drug treatment had decreased odds of HIV.

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Declining HIV Prevalence

A reduction in injecting risk behaviors was observed across the 2 time frames, providing some evidence to support the supposition that the observed decline in HIV prevalence between 2001 and 2004 is real. IDUs in 2004 were less likely to inject daily or with used needles or syringes and were less likely to practice frontloading or to inject using a communal filter. They were, however, more likely to inject drugs from a prefilled syringe. The explanation for this is unclear. Purchasing drugs in prefilled syringes is most likely associated with the distribution of home-produced drug solutes (eg, the opiate “mak,” the methamphetamine “vint”), and there were only nonsignificant increases in mak or vint being injected as primary drugs in 2004 compared with 2001. Taken together, our findings suggest that new injectors in 2004 were engaging in less injecting risk behavior than new injectors in 2001. New injectors in 2004 would have started injecting at a time when there was generalized awareness among injectors in Togliatti City that explosive HIV spread had occurred, reaching a high prevalence among injectors, including new injectors.3,25,47 Patterns of injecting may therefore have changed in the intervening period, and for those new to injection after 2001, involved much less frequent injection and related risk exposure despite a high background HIV prevalence among established injectors. Evidence from other Russian cities suggests that the frequency of injection may have decreased in recent years, with studies undertaken between 1999 and 2001 reporting higher proportions of IDUs injecting daily of up to 68%,48,49 whereas later studies indicated lower proportions of approximately 18%.36

We found decreases in the proportions of new injectors reached by the city needle and syringe exchange program (NSEP), outreach, and drug treatment. The decline in attendance at the state-provided drug treatment services is most likely attributable to an increase in the availability of private treatment centers over the period. There is also an increasing reluctance on the part of drug users to use these services because of their emphasis on detoxification and maintaining abstinence, lack of emphasis on confidentiality, and tendency to exchange patient information with police services for surveillance purposes; in addition, drug treatment attendance leads to official registration as an addict, which affects the ability to find employment.38,50

In both time periods, most IDUs (near 90% in 2001 and more than 90% in 2004) relied on pharmacies as their main source of sterile injecting equipment. The coverage achieved through dedicated needle and syringe exchange or outreach projects in the city is clearly limited relative to the potential role played by pharmacies. The low coverage achieved by the NSEP relative to pharmacies is not unusual for projects in the Russian Federation. Evidence from other cities has shown that the geographic location of outlets and strict program regulations, such as demand for 1-for-1 exchange rather than unconditional provision of syringes, make pharmacies a far more accessible source of new needles/syringes than NSEPs, especially given their ubiquity and more accessible opening times.51 The observed decline in HIV prevalence among new injectors is therefore unlikely to be directly linked to the introduction of needle and syringe or outreach projects in 2001 but is more likely to be a consequence of more generalized shifts in risk awareness and patterns of injection. A higher proportion of IDUs in 2004 reported ever having been tested for HIV in 2004 than in 2001, and this was associated with decreased odds of anti-HIV univariably. We emphasize the need for increasing access to voluntary and confidential HIV testing in combination with increasing the accessibility of sterile injecting equipment through pharmacies, including through pilot pharmacy-based exchange schemes.

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Limits and Interpretation

Aside from some difference in geographic distribution of injectors across the 3 districts, the demographic and environmental indicators of the populations sampled in the 2 time frames are similar and suggest that the observed decline is unlikely to be an artifact of sampling bias alone. In the 2001 survey, however, increased odds of anti-HIV were associated with injectors residing in Komsomolskii, raising the possibility that this sample had tapped into a network of HIV-positive IDUs from this district. The implementation of future repeat community-recruited cross-sectional surveys would substantiate the validity of the observed differences in HIV risk factors and shifts in HIV transmission case reports reported here and the extent to which sampling variation or misclassification of behavioral data may play a role.

We must recognize that any inferences made about the underlying risk factors driving HIV transmission and changes since 2001 are limited by the fact that the behavioral data are drawn from self-reports, although the potential bias associated with socially desirable responses was limited by the use of a field work team involving current or former drug users.52 Newer evidence suggests that risk behavior reported to indigenous field workers may be of poorer quality than that collected through computer-assisted survey interviewing (CASI) programs, however.41 Any inferences about causality between risk factors and anti-HIV is unavoidably limited by the cross-sectional nature of the study, and in respect to sexual risk behavior, this was compounded by the lack of standardized sexual risk indicators collected between 2001 and 2004.

Our analysis was predicated on the assumption that our sample of new injectors was HIV-negative before initiation into injection. This assumption is plausible considering other international evidence, but the ability to test this assumption explicitly was limited by 3 factors: first, by lack of biologic indicators on other sexually transmitted infections; second, by lack of use of detuned assays to verify that the HIV infections were new infections; and third, by lack of standardized data on sexual risk behaviors collected from the 2 time points. Additionally, data on the extent to which the population size of IDUs had changed by 2004 would have enabled us to explore whether the decline in HIV prevalence among new injectors was influenced by changes in the size of the IDU population.

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These studies highlight the potential role of cross-sectional surveys as a method of second-generation surveillance in conjunction with HIV case reporting for monitoring trends in HIV and in pinpointing key intervention targets of risk and behavior change. Our findings also highlight the importance of sampling recent initiates into injecting to predict changing incidence.9,10 Findings suggest a reduction in HIV prevalence among populations of new injectors in a city having witnessed explosive HIV spread and high HIV prevalence. Despite this, HIV remains of epidemic proportions among new injectors in Togliatti City. Findings emphasized the importance of HIV testing in maximizing risk awareness and opportunities for behavior change and of piloting pharmacy-based needle and syringe exchange, given low levels of coverage linked to expanding dedicating needle and syringe exchange. These findings have relevance for other cities in Russia and Eastern Europe, which were witness to rapid or explosive HIV outbreaks occurring among IDUs in the past decade.

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The authors are grateful for the support of the UK Department for International Development, which supported this study through program grants, and to the UK Department of Health, which provided core funding to the Centre for Research on Drugs and Health Behaviour. They also thank the study participants and the following individuals: Sergei Belikh, Irina Berezhnova, Dimitry Blagov, Natalia Bobrova, Elvira Demyanyenko, Alexander Fillipov, Nadezhda Gorshkhova, Elena Kudravtseva, Peter Madden, Olga Mikhailova, Adrian Renton, Nelly Savelevna, Lenar Sultanov, Grigoryev Svyatoslav, Mikhail Tichonov, Venyamin Volnov, Konstantin Vyshinsky, and Martin Wall. This article is dedicated to the memories of our colleagues and friends, Andrei Rylkov and Nadezhda Zabotina.

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HIV prevention; injecting drug use; new injectors; Russia; sexual risk behavior

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