Injecting drug use is the predominant mode of HIV transmission in eastern Europe . In Russia, as well as in some other newly independent states of the former Soviet Union (FSU), the vast majority, over 90%, of HIV cases are estimated to be associated with injecting drug use [2,3]. Current estimates of HIV spread in Russia and the FSU are based on national case reports derived from large screening programmes among populations at risk. These do not provide accurate estimates of HIV prevalence among injecting drug users (IDU).
The spread of HIV associated with injecting drug use can be ‘explosive’ . This has been well documented among IDU in south and south-east Asia . Since 1995, a decade after the rapid spread of HIV was reported among IDU in Asia, and a decade after HIV transmission had peaked in western Europe, new epidemics of HIV have been reported among IDU in Russia, Ukraine, Moldova, Belarus and Kazakhstan [5,6]. Before 1995, there was little evidence of HIV transmission associated with injecting drug use in these countries. The rate of increase in new cases of HIV in Russia recorded by the Ministry of Health has been exponential, with 56 630 new cases recorded in 2000, almost twice the cumulative number of cases recorded since 1987, and a further 82 852 new cases in 2001 .
The diffusion of HIV outbreaks among IDU within Russia suggests that by the end of 2000, epidemics had occurred in over 30 cities and in 82 of the 89 Oblasts (regions) of the Federation. Outbreaks have been observed, for example, in: Kaliningrad (since January 1996); Krasnodar (February 1996); Nizhny Novgorod (March 1996); Tumen (April 1996); Rostov (June 1996); Tver (January 1997); Tula (April 1997); Irkutsk (since 1998); and Moscow (since 1999) [3,6]. In Kaliningrad, for instance, new HIV cases were reported to have increased from less than one to more than 100 per month between August and September 1996, with 80% of cases associated with injecting drug use . In Moscow, the increase in reported new cases associated with injecting drug use in the past 2 years has been particularly dramatic .
There are no published studies of HIV prevalence among large community-recruited or non-treatment samples of IDU in Russia. These would appear to be a priority. This paper reports on the findings from one of the first studies of HIV prevalence among IDU in Russia.
A cross-sectional anonymous survey of IDU recruited from community settings was conducted during a 4-week period between September and October 2001 in Togliatti City, Samara Oblast, Russian Federation. All participants reported injecting in the previous 4 weeks, provided informed consent, and gave oral fluid specimens for HIV testing. The study was undertaken with ethical approval from the Riverside Research Ethics Committee (Chelsea and Westminster Hospitals), and with the support of the Togliatti City Department of Health and City Narcological Services.
Survey data collection
The survey used a 30 min structured questionnaire, developed from comparable surveys and informed by a qualitative study and piloting among IDU . Sections included demographic characteristics, drug use, injecting and sharing behaviours, sexual behaviour and HIV testing history. Checks across demographic data identified no duplicates within the study population.
All IDU were recruited in the community. The survey was administered by two teams of trained fieldworkers (n = 22), each working in pairs across the three districts of the city. Fieldworkers were employed on the basis of their ‘indigenous’ or ‘privileged’ access to IDU, and included outreach workers as well as former and current drug users. A 4-day fieldwork training course focused on research and interviewing techniques, recruitment and outreach, ethics, safety, and relapse prevention. Measures to ensure data quality and the minimization of social network or geographical bias included: placing limits on the numbers of interviews permitted per fieldworker; undertaking daily monitoring of fieldwork contacts and completed interviews; and undertaking observations and spot-checks in the field. Fieldworker safety was ensured by daily supervision and through issuing mobile telephones to maintain contact during fieldwork. A signed agreement for the study was made with the City Departments of Internal Affairs and City Narcological Clinic.
No financial incentives were offered to IDU for their participation. Instead, IDU received a pack containing syringes, condoms, information booklets, referral cards, as well as cigarettes and condensed milk.
Anti-HIV antibody testing
Oral fluid specimens were obtained using the OraSure device (Epitope Inc., Oregon, USA) and were screened for antibodies to HIV (anti-HIV) employing the GACELISA HIV 1+2 enzyme immunoassay (VK61, Abbott Laboratories, Maidenhead, UK). Detailed laboratory methods have been published elsewhere [9,10]. Specimens that were reactive on initial testing were subjected to confirmatory testing using alternative methods. The GACELISA has been shown in multiple studies to be 100% sensitive [9–11], and the use of validated supplemental tests excluded false positives, such that specificity was also close to 100%. All anti-HIV testing took place in Togliatti City in collaboration between the Togliatti Fifth City Hospital Laboratory – Diagnostic Centre, Togliatti City AIDS Centre and the UK Central Public Health Laboratory.
Associations between antibody prevalence and covariates were explored using the likelihood ratio statistic and Stata 6.0 (Stata Corp, College Station, TX, USA). Factors reaching P < 0.05 in univariate analysis were subsequently entered in a multivariate logistic regression model.
The city of Togliatti covers a territory of 224 square kilometres, divided into three geographically separated administrative districts or raions; Tsentralnii, Komsomolksii (the smallest), and Avtozavodskoi (the largest). As of January 2001, the registered population was 753 819, although the true number is estimated to be nearer 1 000 000 if non-registered (ne propisanno) residents are included. Togliatti is a relatively young city, with 66% of the total population of working age and 23% younger than 17 years. At the time of writing, there were 5981 registered drug users or potrebitelii (individuals registered as using drugs for non-medical purposes, including non-injectors). Of these, 4535 were registered as narkomanii (addicts) and 4419 as IDU. The true number of IDU is likely to be between five and 10 times higher .
A total of 426 IDU were recruited over 4 weeks, of whom 55% were recruited from Avtozavodskoi, 30% from Tsentralnii, and 15% from Komsomolksii (Table 1). Two-thirds (64%) were male and half (47%) were aged under 25 years. Over a quarter of the sample (29%) had been in prison at some point in the past, while 53% reported having had an overdose, and 35% reported having previously received treatment for their drug use (detoxification or residential rehabilitation).
In terms of drug use and injecting risk behaviour, there was a substantial proportion of recent initiates to injecting, with one-fifth of the sample having commenced injecting in the past 2 years, and 27% in the past 3–5 years (Table 1). Nearly 60% of the sample reported injecting drugs that had been ‘home produced', including ‘jeff’ (ephedrine-based stimulant extracted from ‘Solutan', a cough syrup), ‘hanka’ (a liquid derivative of opium poppy) and ‘vint’ (an ephedrine-based methamphetamine, also derived from ‘Solutan’ or ephedrine-based tablets). The most commonly injected drug in the 4 weeks before the interview was heroin (98%), and three-fifths of the sample (58%) injected on a daily basis.
The majority of the sample (86%) reported pharmacies and shops as their main source of new needles and syringes in the previous 4 weeks, and just over a third (36%) had injected with used needles in this time period (Table 1). Only 16% of the sample reported never having injected with a used needle or syringe, and for the rest, the median number of days since the last sharing event was five, ranging from one day to 8 years. Two-fifths of the sample reported ‘backloading’ or ‘frontloading’ in the past 4 weeks [the practice whereby a drug solution is squirted from a donor syringe into another, either by removing the plunger (backloading) or needle (frontloading) from the receiving syringe]. In the same time period, 63% had used filters and 58% rinse water previously used by someone else, and 82% had drawn up their drug from a solution from which someone else had previously drawn. Seven per cent had ever injected with needles and syringes previously used by someone they knew had HIV infection. A quarter of the respondents (27%) had been registered as IDU at the Narcological Dispensary.
The overall prevalence of anti-HIV was 56% (234/418). A third (141/418) had received a negative test result in 2000 or 2001, of whom 41% were now positive for anti-HIV. Only 29 (26%) of those found to be anti-HIV positive, self-reported that they were positive. Moreover, eight of those who reported that they were positive in fact tested anti-HIV negative. Univariate associations between key risk factors and anti-HIV are shown in Table 1. Neither sex, age, or duration of injecting were associated with anti-HIV. For example, for duration of injecting, the prevalence was 48% among those injecting for 2 years or less, 63% for those injecting for between 3 and 5 years, 51% for those injecting for between 6 and 9 years, and 59% for those injecting for 10 years or more (P = 0.097).
Seventy per cent of those recruited from Komsomolksii were HIV positive, compared with 48% for Tsentralnii and 56% for Avtozavodskoi (P = 0.016, Table 1). The prevalence of HIV was higher among those who had injected home-produced drugs in the past (64%) than among those who had not (45%, P < 0.001). Injectors whose main source of new needles and syringes in the past 4 weeks had been buying them on the streets, or being given them by a sexual partner, friend, other drug user or a drug dealer had a higher prevalence of HIV than those whose main source was pharmacies, shops, needle exchange or outreach workers (P = 0.032). Those who had injected with used needles and syringes in the past 4 weeks had a higher prevalence of HIV than their counterparts (64 versus 51%, P = 0.007).
In a multivariate model (Table 2), IDU in Komsomolksii had twice the odds of being HIV positive compared with those recruited from Avtozavodskoi [odds ratio (OR) 1.9; 95% confidence interval (CI) 1.3–3.0]. IDU who had injected home-produced drugs had twice the odds of being HIV positive than those who had not (OR 2.0; 95% CI 1.3–3.0). Those who had injected with used needles and syringes in the past 4 weeks had nearly twice the odds of being HIV positive than their counterparts (OR 1.7; 95% CI 1.1–2.6). However, the relationship between the main source of new needles and syringes and HIV was weakened (P = 0.170).
The prevalence of HIV among IDU in this study was extremely high, at 56% of the whole sample. The lack of association between prevalence and the duration of injecting or age, and the high prevalence of HIV among individuals who had reported a negative test result in the past 2 years, suggest that the epidemic is both recent and explosive. This is supported by evidence of a rapid increase in the proportion of screening tests in Togliatti testing positive since 2000 . Approximately 100 000 HIV antibody tests are undertaken annually in the city from various populations at risk in over 140 health facilities. In 1998, only two out of 91 377 tests proved to be HIV positive, and in 1999, only 10 out of 97 710 tests were positive . However, in 2000, 3680 new cases were identified (out of 116 777 tests). Of the 4890 cumulative cases of HIV registered by the City AIDS Centre as of May 2001, 99% were attributed to injecting drug use.
Taken together, these findings suggest that the HIV epidemic in Togliatti has been explosive, reaching 50% prevalence among IDU in under 2 years. Moreover, despite extensive screening in the city, the survey suggested that three-quarters of IDU were unaware of their positive status.
It is important to recognize that similar trends in HIV spread associated with injecting drug use have been reported elsewhere in the FSU, including in Belarus, Moldova, Kazakhstan, and the Ukraine [4,6]. In the Ukraine, for example, two small studies of HIV prevalence [6,12], conducted in the south of the country, estimated that in Odessa HIV prevalence among IDU rose from 1.4% in January 1995, to 13% in August 1995, to 31% by January 1996; and in Nykolayev, from 0.3% in 1994, to 17% in early 1995, to 57% by January 1996. A similar pattern of spread to that in Togliatti is currently being observed in neighbouring Samara City, the capital of the Oblast [3,8].
IDU who had injected home-produced drugs had twice the odds of being HIV positive. Qualitative accounts point to the diffusion of heroin occurring in Togliatti since 1997, before which time the injection of home-produced hanka was the norm, alongside vint and jeff. In the case of hanka and vint, it has been posited that HIV may enter the production process via containers and mixers used to collect up, decant and mix the solution ingredients, and via injecting equipment used to test or distribute the liquid directly from containers , although heating during the production process may inactivate HIV . Of arguably more importance, we speculate that the increased risk related to the injection of home-produced drugs may be associated with the distribution of home-produced drugs, which commonly takes place in a group situation, often involving the collective use of injecting equipment [8,14]. These situational risk factors, as well as potential differences in injecting practices associated with home-produced liquid drugs and non-home produced powder drugs, merit further exploration.
IDU had almost twice the odds of being HIV positive if they had injected with used needles and syringes in the 4 weeks before the interview. Research in Togliatti and elsewhere highlights the critical importance of situational factors influencing syringe distribution and exchange practices [8,15]. Most notably, there is a reported reluctance among IDU to carry needles and syringes for fear of detainment by police, which in turn may encourage receptive needle and syringe sharing at the point of drug sale, most commonly in a dealer's house, wherein mixing between different social networks of IDU may occur .
Although useful in targeting HIV prevention, it is unclear to us why IDU in Komsomolksii, part of the old city, had twice the odds of being HIV positive than IDU living in Tsentralnii, a neighbouring district in the old city, or Avtozavodskoi, the new town wherein a greater proportion of the population are in factory or other employment. Given no strong evidence of interactions between the city district and other predictors, further research is required, including an exploration of potential area differences in the structure of drug injecting, dealing and injecting equipment networks.
HIV prevention in an epidemic of high prevalence
Explosive and highly prevalent HIV epidemics among IDU have been documented elsewhere [2,5,17]. The reconstruction of HIV diffusion in south and south-east Asia showed HIV prevalence among IDU rising to over 40% within one year of detection in Bangkok and Chiang Rai (1987–1988), Mytkyina, Mandalay and Yangon in Myanmar (1989), Ruili (Yunnan Province) in south-west China (1989), and Manipur in north-east India (1989–1990) . In Bangkok, for example, rapid HIV spread among IDU in 1987 and 1988 was followed by prevalence stabilizing between 1989 and 1997, with large surveys showing prevalence rates between 33 and 38% among IDU during this period [18,19]. The same studies highlighted declining levels of injecting risk behaviour among a high proportion (over 90%) of IDU since 1989, with reduced HIV incidence associated with stopping needle and syringe sharing. Behaviour change may have prevented saturation of the epidemic within IDU in Bangkok, but moderate levels of continued risk behaviour were nonetheless found to maintain a ‘moderate to high’ rate of HIV incidence .
Once HIV prevalence among a high-risk IDU population reaches 20%, HIV epidemics can become self-perpetuating, with even modest levels of risk behaviour leading to substantial rates of infection [20,21]. Explosive spread may further exacerbate the risk in these conditions, given high levels of unreported positivity and the possibility that HIV infection diffuses faster than behavioural change. The situation in Togliatti would appear to mimic other highly prevalent epidemics among IDU in this respect .
One of the best documented examples to date of declining HIV prevalence in a large epidemic among IDU is the epidemic in New York City, where HIV spread rapidly in the late 1970s and early 1980s, stabilized through the mid-1980s, and declined after 1991 . Declines in prevalence and incidence in the New York epidemic were simultaneous with declines in risk behaviour, and suggested a ‘causal effect’ between the expansion of HIV prevention services and reductions in risk . The reversal of the epidemic was closely associated with the legalization, funding and expansion of a community-based syringe exchange . These finding are consistent with international evidence supporting the protective effect of syringe exchange [25,26], as well as community outreach and low-threshold drug treatment [27,28] against HIV transmission among IDU.
In Russia, HIV prevention coverage appears woefully inadequate. Approximately 40 syringe exchange programmes have been established across 89 Oblasts. The development of syringe exchange and outreach in Russian cities has typically occurred after or during periods of explosive spread, and often without the levels of coverage necessary to avert or reverse epidemic outbreaks . In Togliatti, there are two syringe exchanges (one in Avtozavodskoi, and one in Tsentralnii), with the first established in late 2000, and legal access to the purchase of needles and syringes at pharmacies. A minority (8%) of those surveyed used the exchanges, with the majority (86%) relying instead on pharmacies. Our findings have urgent implications for maximizing the distribution of sterile injecting equipment among IDU in Togliatti City via a combination of pharmacy outlets, syringe exchange and outreach, with the aim of achieving community-wide HIV prevention coverage. There is also the need for the rapid introduction of such measures in other cities in advance of explosive outbreaks of HIV. A public health initiative such as this clearly requires city and Oblast support, including among law enforcement and policing agencies. It also requires strategies that foster the development of low-threshold drug treatment, ideally substitution treatment, in combination with low-threshold voluntary HIV counselling and testing services [27,28].
A finding of high prevalence also underscores the need for a simultaneous focus on sexual risk reduction, especially among IDU involved in sex work . Explosive HIV epidemics of high prevalence among IDU elsewhere point to the potential for onward sexual transmission towards non-injecting populations . Recent molecular studies in Russia are suggestive of sexual transmission between IDU and their non-injecting sexual partners .
These data indicate a high prevalence of HIV among IDU in Togliatti City, suggesting that a rapid spread of HIV has occurred since 1999. Current HIV prevention coverage among IDU is inadequate. There is an urgent need to maximize the distribution and exchange of sterile injecting equipment, as well as to promote sexual risk reduction among IDU and their partners. We recommend the enhancement of existing syringe exchange and the development of community-wide HIV prevention for IDU supported by city and state policies oriented towards harm reduction.
The authors are grateful for the support of the UK Department for International Development, who provided funds for this study as part of a wider project to enhance HIV prevention services for IDU in the Russian Federation associated with the DfID Programme ‘Knowledge for Action in HIV/AIDS'. The authors would also like to express gratitude to the Togliatti City Department of Health, to the Togliatti Harm Reduction Project Coordination Group, to the Togliatti Narcology Outreach Workers, and to the following individuals for their comments on an earlier draft of this paper: Dave Burrows, Andrew Ball, Jean-Paul Grund, Lucy Platt, Elvira Zhukova, Veronica Petrova, Yuri Pevzner, Alexander Shakhov, and Olga Bogdanova.
1. UNAIDS/WHO. AIDS Epidemic Update.
Geneva: UNAIDS/WHO, December 2001.
2. Rhodes T, Stimson GV, Crofts N, Ball A, Dehne K, Khodakevich L. Drug injecting, rapid HIV spread and the ‘risk environment'
. AIDS 1999, 13 (Suppl. A) : S259–S269.
3. Federal AIDS Centre. HIV infection: informational bulletin
, No. 20. Moscow; 2001.
4. Crofts N, Reid G, Deany P. Injecting drug use and HIV infection in Asia
. AIDS 1998, 12 (Suppl. B): S69–S78.
5. Rhodes T, Ball A, Stimson GV. et al
. HIV infection associated with drug injecting in the newly independent states, eastern Europe
. Addiction 1999, 94: 1323–1336.
6. Dehne KL, Khodakevich L, Hamers FF, Schwartlander B. The HIV/AIDS epidemic in eastern Europe: recent patterns and trends and their implication for policy-making. AIDS 1999, 13: 741–749.
7. Liitsola K, Tashinova I, Laukkanen T. et al
. HIV-1 genetic subtype A/B recombinant strain causing an explosive epidemic in injecting drug users in Kaliningrad
. AIDS 1998, 12: 1907–1919.
8. Rhodes T, Mikhailova LA, Lowndes C. et al
. Preventing HIV infection among injecting drug users in Togliatti City, Samara Oblast, Russia.
London: Imperial College; 2001.
9. Connell JA, Parry JV, Mortimer PP, Duncan J. Novel assay for the detection of immunoglobulin G anti-human immunodeficiency virus in untreated saliva and urine
. J Med Virol 1993, 41: 159–164.
10. Connell JA, Parry JV. Detection of anti-HIV in saliva and urine at the time of seroconversion
. Clin Diagnost Virol 1994, 1: 299–311.
11. Tamashiro N, Constantine N. Serological diagnosis of HIV infection using oral fluid samples
. Bull WHO 1994, 72: 135–143.
12. Khodakevich L, Kobyshcha Y, Shcherbinskaya AM. Development of HIV epidemics in Belarus, Moldova and Ukraine
. In:8th International Conference on the Reduction of Drug Related Harm.
Paris, 1997 [Abstract].
13. Clatts MC, Heimer R, Abdala N. et al
. Iliicit drug injection and HIV-1 transmission: heating drug solutions may inactivate HIV-1
. J Acquired Immune Defic Syndr 1999, 22: 194–199.
14. Grund JPC, Kobzev D, Melnikov V, et al.Drug use patterns and HIV risk behaviors of Russian syringe exchange participants
. In:12th International Conference on the Reduction of Drug-Related Harm.
New Delhi, 2001 [Abstract].
15. Grund JPC. A candle lit from both ends: the epidemic of HIV infection in central and eastern Europe
. In:HIV and AIDS: international comparisons.
McElrath K (editor). Westport, CT: Greenwood Press.
16. Rhodes T, Mikhailova L, Lowndes CM, et al.Situational factors influencing drug injecting and syringe exchange practices in Togliatti City, Russian Federation
. In:13th International Conference on the Reduction of Drug-Related Harm.
Ljubljana, Slovenia, 2002 [Abstract, 203].
17. Stimson GV. Reconstruction of the subregional diffusion of HIV infection among injecting drug users in south-east Asia. AIDS 1994, 8: 1630–1632.
18. Vanichseni S, Choopanya K, Des Jarlais DC. et al
. HIV among injecting drug users in Bangkok: the first decade. Int J Drug Policy 2002, 13: 39–44.
19. Des Jarlais DC, Choopanya K, Vanichseni S. et al
. AIDS risk reduction and reduced HIV seroconversion among injection drug users in Bangkok. Am J Public Health 1994, 84: 452–455.
20. Des Jarlais DC, Marmor M, Friedmann P. et al
. HIV incidence among injection drug users in New York City, 1992–1997: evidence for a declining epidemic. Am J Public Health 2000, 90: 352–359.
21. Holberg S. The estimated prevalence and incidence of HIV in 96 large US metropolitan areas. Am J Public Health 1996, 86: 642–654.
22. Friedman SR, Jose B, Deren S, Des Jarlais DC, Neaigus A, and the National AIDS Consortium. Risk factors for HIV seroconversion among out-of-treatment drug injectors in high- and low-seroprevalence cities. Am J Epidemiol 1999, 142: 864–874.
23. Des Jarlais DC, Perlis T, Freidman SR. et al
. Behavioral risk reduction in a declining HIV epidemic: injection drug users in New York City, 1990–1997. Am J Public Health 2000, 90: 1112–1116.
24. Des Jarlais DC, Marmor M, Paone D. et al
. HIV incidence among injection drug users in New York City syringe-exchange programmes. Lancet 1996, 348: 987–991.
25. Gibson DR, Flynn NM, Perales D. Effectiveness of syringe exchange programs in reducing HIV risk behavior and HIV seroconversion among injecting drug users. AIDS 2001, 15: 1329–1341.
26. Hurley SF, Jolley DJ, Kaldor JM. Effectiveness of needle-exchange programmes for prevention of HIV infection
. Lancet 1997, 349: 1797–1800.
27. Coyle SL, Needle RH, Normand J. Outreach-based HIV prevention
for injecting drug users: a review of published outcomes data. Pub Health Rep 1998, 113 (Suppl. 1) : 19–30.
28. Drucker E, Lurie P, Wodak A, Alcabes P. Measuring harm reduction
: the effects of needle and syringe exchange programs and methadone maintenance on the ecology of HIV. AIDS 1998, 12 (Suppl. A) : S217–S230.
29. Dallabetta G, Diomi MC. Treating sexually transmitted diseases to control HIV transmission. Curr Opin Infect Dis 1997, 10: 22–25.
30. Panda S, Chatterjee A, Sarkar S. et al
. Injection drug use in Calcutta: a potential focus for an explosive HIV epidemic. Drug Alcohol Rev 1997, 16: 17–23.
31. Ladnaya NN, Pokrovsky VV, Bobkov A, et al.Correlation between risk factors for HIV infection in Russia and HIV-1 subtypes isolated in Russia, 1994–1997.
In:12th World AIDS Conference
, Geneva, 1998 [Abstract 14191].