Epidemiology of hepatitis B, hepatitis C and HIV infections among intravenous drug users in Jerusalem, Israel

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1 International Public Health Journal ISSN: Volume 2, Issue 3-Special Issue pp Nova Science Publishers, Inc. Epidemiology of hepatitis B, hepatitis C and HIV infections among intravenous drug users in Jerusalem, Israel Daniel Chemtob, MD, MPH, DEA 1, Maxim Gurevitz, MD 2, Shabtai Levitt, MSW 3, Niva Basudo-Manor, MPH 1, Emmy Shufman, MD 4 and Shlomo Maayan, MD 2 1 Department of Tuberculosis and AIDS, Public Health Services, Ministry of Health, 2 AIDS center of Jerusalem, Department of Clinical Microbiology and Infectious diseases, Hadassah University Hospital, Ein Kerem, 3 The Jerusalem Methadone clinic (MAMI) and 4 The Jerusalem Institute for Treatment of Substance Abuse, Jerusalem, Israel Abstract The demography and drug use practices in Israel are changing partly due to immigration. Objectives: Study the prevalence of blood borne viruses among intravenous drug users (IDU) and non-idu and compare to previous surveys done at the same centers. Methods: A cross-sectional survey of all 233 illicit drug users attending two drug rehabilitation centers in Jerusalem. Antibodies to HBV, HCV and HIV were measured and questionnaires related to drug use and sexual practices given. Results: 200 (85.8%) were males. Most cases (210-90%) were of Mediterranean origin, 23 (10%) of East European origin. 87 (37.3%) were IDU and more frequent in individual from East European origin (78.3%) than Mediterranean origin (32.9%) (p<0.0001). East European origin drug users comprised 20.6% of all injectors, but only 3.4 % of non-injectors (p<0.001). Compared to an earlier survey, the fraction of IDU almost doubled. We found an HCV prevalence of 24.5% (55.5% among IDU, 6.3% in non-idu, p<0.001); HBV: 32.2% (38.3% among IDU, 29.1% in non-idu - NS); HIV: 1.3% (3.4% among IDU, 0% in non-idu). Exposure to HCV and HBV was significantly related to the intensity of drug injections (p<0.0002). Conclusion: Despite that the number of IDU almost doubled between the studies, the level of blood born viruses (HBV and HCV) stayed alsmost similar. Drug use patterns in Jerusalem in suggested a shift towards IDU, mostly among individuals of East European origin. This may contribute to high rates of HCV and HBV infections in the future within this population group. Keywords: Intravenous drug use, Israel, Former Soviet Union, HCV infection, HBV infection, HIV infection. Introduction Correspondence: Professor Shlomo Maayan, The AIDS Center, Department of Clinical Microbiology and Infectious Diseases, Hadassah University Hospital, Jerusalem 91000, Israel. Tel: ; Fax: ; shlomo_m@netvision.net.il Injection drug use is a well recognized risk factor for the acquisition of the blood borne viruses such as hepatitis C, hepatitis B, HIV and HTLV-1 and 2 (1-7). In a previous survey conducted in Jerusalem in 1989 among all 300 drug users followed at two drug

2 346 Daniel Chemtob, Maxim Gurevitz, Shabtai Levitt et al. treatment centers, a prevalence of 54% of HCV and 26% of HBV antibodies was detected among intravenous drug users (IDU). HIV infection was not found (8,9). The starter for the current study, conducted six years later in the same treatment centers, was the recent influx to Israel of immigrant drug users from the former Soviet Union (FSU), the paucity of information from Israel about drug abuse patterns in this population and the emergence of a major HIV epidemic among IDU in the FSU (10). Results from this local survey were analysed in the framework of establishing a pilot syringe exchange program in Israel, which is described elsewhere (11). Intensity of injections Intensity of injections was defined as the number of injections/day X years of injections, expressed in years (injection years). Statistical analysis Data were analyzed using the SPSS 9 statistical package. Student s t-test was used for univariate analysis. Logistic regression was used for multivariate analysis. Methods A cross-sectional survey of all 233 illicit drug users who attended two drug rehabilitation centers in Jerusalem in the period January 1995-March 1996 was performed. One center is a drug free program, the other a Methadone maintenance program center. Most IDU (some 80%) were treated at the Methodone center. 52.9% of those who ever injected drugs and 92.9% of those who were currently injecting drug were treated at the drug free program. A questionaire of 36 variables (questionaire available upon request) was elaborated. Demographic, drug habit and sexual information were collected throught a directed and supervised interview from all the participants, following informed consent. Laboratory methods Hepatitis B seropositivity was defined as positive anti HBs and/or anti HBc on Elisa assays (Sorin). HCV seropositivity was defined as a positive sample obtained by two commercial Elisa assays (Sorin and Abbott). HIV antibodies were detected by a third generation commercial Elisa assay (Abbott) (tested positive twice) and confirmed by a Western Blot. HCV seropositivity was measured by commercial assays (Amplicor, Roche). HCV infectivity was defined as a positive reaction by HCV PCR in HCV sero-positive samples. Results Out of the 233 individuals, 200 (86%) were males and 33 (14%) females. The mean age for the group was 38.4 years (range years; SD= 7.6). Israeli Jews comprised 79% and Arabs (Israelis and non-israelis) comprised 21%. Most of the individuals (90%) originated from North Africa (and other Mediterranean countries) or from Middle East (Israel and Arab Palestinian Authority). The remaining 10% originated from East Europe (Russia, Ukraine, Poland). Demographic and blood born viruses data were almost similar between the two cohorts (1989 versus 1995), excepted an almost doubling of the fraction of IDU in the 1995 compared with the 1989 cohort (19% to 37%, see table 1) and the presence of three HIV positive cases in the 1995 cohort study. Of the 233 subjects, 87 (37.3%) were intravenous drug users. Most East European descendants (18/23, 83.3%) were IDU, compared to only 33.5% (69/210) of individuals of Mediterranean origin ( p<0.0001). Male/female ratio in the group of IDU was similar to the one in the group of non-idu. Similarity between these two groups was also found concerning the age of starting drug abuse (16.6 years old in IDU versus 16.1 years old in non-idu; p=ns). Risky sexual behaviour was common in both groups (IDU vs. non- IDU): Extra-marital encounters were reported by 66.7% and 48%, respectively (p=ns). Bisexual relations or frequenting prostitutes were reported by 27.6% and 12.3%, respectively (p=0.03).

3 Epidemiology of hepatitis B, hepatitis C and HIV infections 347 Table 1. Demographic of patients and exposure to blood borne viruses: 1989 and 1995 surveys in Jerusalem drug rehabilitation clinics, Israel 1989 survey 1995 survey No. (%) No. (%) Total Numbers Males 169 (90) 200 (86) Females 19 (10) 33 (14) IDU 57 (19) 87 (37) Non IDU 243 (81) 146 (63) Mediterranean origin 284 (95) 210 (90) European origin 16 (5) 23 (10) (15/18, 83%) vs. Mediterraneans (42/69, 61%) (p=ns). IDU with HBV positive or HCV positive had a significantly higher intensity of injection than IDU HBV negative or HCV negative (see table 2). Concerning HBV positive individuals, they were older than the HBV seronegatives (p<0.02) (see table 3). This was also correct when only non-idu were analyzed (p< 0.001). We did not find age strong correlation in HCV seropositive drug abusers (see table 4). Table 2. Intensity of onjections and exposure to blood borne viruses (N=87) HBV HCV HIV1 Injection/ day x years Injection/ day x years Injection /day x years 15.2 y. 7.0 y y. Seronegative HIV+ 0 ( of 181) * 3 (1.3) HBV+ 31%(of 181) * 72 (32) HCV+ 18%(of 181) * 54 (24) HCV+ among IDU 54% 55% IDU: Intravenous Drug Users. Intensity of injections (in injection years; IY) were not significantly different when comparing between males and females (28.6 IY vs IY), between individuals from Mediterranean and European origins (29.1 IY vs IY), nor between Jews and Arabs (30.8 IY vs IY). Exposure to blood borne viruses: HCV antibodies were detected among 54 individuals (out of 223 tested; 24.2% : 55.5% among IDU, 6.3% in non-idu; p<0.0001). HCV PCR + was detected in 50% of all HCV seropositives individuals. HBV antibodies were detected in 72 individuals (out of 222 tested; 32.4% : 38.3% among IDU, 29.1% in non-idu; p=ns). HIV antibody were detected in 3 individuals (out of 233 tested, 1.28%, all among IDU). This prevalence figures were similar to those detected in the 1989 cohort (see table 1). HBV was most significantly higher when considering IDU vs. non IDU. Among IDU, HCV was not significantly higher when considering the country of origin: East Europeans 47.1 y y. 105 y. Seropositive NA* *cannot be calculated p values Table 3. Age of patients and the risk of HBV infection HBV serology No. of patients Age, mean ( + ) ( - ) Total P value <0.02 Table 4. Multivaried analysis: Risk factors for infection by Hepatitis C & B among Jerusalem drug users , Israel Variable Hepatitis C sero+:or (95%CI) Age 1.05 ( ) Sex (F/M) 1.04 ( ) Hepatitis B sero+:or (95% CI) 1.14 ( ) 0.6 ( ) Ever injecting drugs 0.1 ( ) 0.8 ( ) Intensity of drug injections 6.2 ( ) 3.1 ( ) Unsafe sexual encounters NA NA Geographic origin (Mediterranean/E.Europe) NA 0.6 ( ) NA: Risk estimates statistics can not be compute.

4 348 Daniel Chemtob, Maxim Gurevitz, Shabtai Levitt et al. Concerning HBV, no gender difference was observed. The intensity of drug injections was strongly associated as a separate risk factor for HCV and HBV (OR of 6.2 and 3.1, retrrospectively (see table 4). Discussion The aim of this survey was to characterize a population of illicit drug users in Jerusalem, its drug abuse patterns and exposure to blood borne viruses and to compare results with a similar survey done some six years earlier. The impetus for the survey was the mass immigration to Israel from the FSU (12) and the major outbreak of HIV infection among IDU in the FSU (10). With this in mind we analysed exposure to blood borne viruse, both according to the pattern of drug abuse and to the geographical origin of the patients. The main result of this study was that the level of blood born viruses stayed almost the same when comparing the two cohorts, despite that the number of IDU cases almost double between the two studies. The second important result was that the increase in IDU cases was almost only among individuals originated from FSU. Still a high level of HBV was found. Therefore, the demographic data of the present survey are of high value, due to the known risk of blood born viruses transmission. It was therefore recommended to stay vigilant and to closely follow this high risk group population (IDU originated from FSU). Lastly, limitation exist, and these data are probably not reflecting the national data. The lack of generalisibility is due to the fact that in Jerusalem, the population mix is different than the national mix. Secondly, these data came from drug centers, and may not represent the overall population of IDU. However, when considering the establishement of a pilot syringe exchange program in Israel (11), these (yet) unpublished data were also taken into consideration. The demographics of the present cohort is quite similar to the sample from Then and in the current survey, a close association between IDU and HCV infection was noted (see table 1) with no increase in the prevalence of HCV among IDUs over the span of six years. High HCV prevalence among IDU may be taken in the context of published reports on HCV infection among IDU (13-16) and does not therefore represent a new epidemic among Israeli IDU s. We however noted that the fraction of IDU of the total cohort has increased from 19% in the 1989 (8,9) to 37% in 1995 with most IDUs of East European origin. An increase in the number of IDUs originating in the FSU has been consistently reported in recent years by a large drug rehabilitation center in Northern Israel (.17) Similar pattern has been observed in NYC, a popular site for FSU immigration (18). In Israel, FSU immigrants have also been implicated in the changing pattern of alcohol abuse (19,20). High prevalence of HCV has been detected in a group of alcoholics in Northern Israel, suggesting the coexistance of IDU and alcoholism in at least a part of that group (21). Such a coexistance alcoholism/idu has been demonstrated in the Bronx alcoholics (United States), where the prevalence of HCV has been high (22). Yet, further data and analysis are needed in order to correctly approximate the issue of alcohol consumption among IDU in Israel. The current report, although including only a small number of East European drug users (n=23), points to the extremely high prevalence of IDU in that group and to the associated high prevalence (83%) of infection by HCV. Such a high prevalence of HCV infection has also been reported among IDU in the FSU itself (23,24). We found three cases of HIV positivity among the 1995 population sample, compared to none in the previous survey. This may be an indicative of an early phase of the HIV epidemic among the drug injectors tested. Considering the concomittent HIV epidemic among IDU in FSU (25), it is strongly suggested to closely monitore the HIV epidemic in Israel, in particular among IDU (26,27). Thus, although not yet supported by our cohort, further spread of HIV is likely to occur among injection drug users if the current immigration pattern to Israel from the FSU continues. Repeated surveys in the same drug treatment centers in Jerusalem are needed to monitor the evolving HIV epidemic among IDUs. Unlike HCV and HIV, HBV is endemic in the Mediterranean region (28,29) and as observed in the current group of non- IDUs and in 1989 (8,9)(see

5 Epidemiology of hepatitis B, hepatitis C and HIV infections 349 table 2) HBV exposure can reach a substantial prevalence among Mediterranian descendants. This high prevalence may actually be due to perinatal acquisition of the virus rather than to contact with contaminated blood (28). As such, the HBV prevalence observed among the injection drug users (30.2%) can either be due to acquisition by injections or by the perinatal route or to both. In summary, despite that the number of IDU almost doubled between the two studies, the level of blood born viruses (HBV and HCV) stayed almost similar. Nevertheless, IDU started to be extremely common among drug addicts originating from FSU. In our survey, few HIV positive cases have been found. Nevertheless, considering the recent HIV epidemic among IDU in FSU, it is suggested to closely monitor individuals at risk for HIV, especially IDU. Acknowledgments This project was supported financially by a grant of the Israeli Antidrug Authrity. We are indebted to Mrs Orna First and Ms Michelle Houzi for technical support. The opinions expressed in this article are those of the authors and do not purport to represent the opinions of the agencies with which they are associated. References [1] Friedland GH. Infections in injection drug users. In: Harrison s principles of internal medicine, 14 th ed. New York: McGraw Hill, 1998: [2] Love A., Sigurdsson JR, Stanzeit B, et al. Characteristics of hepatitis C virus among intravenous drug users in Iceland. Am J Epidemiol 1996;143(6): [3] Francisci D., Baldelli F., Papili R. et al. Prevalence of HBV, HDV and HCV hepatitis markers in HIV-positive patients. Eur J Epidemiol 1995; 11(2): [4] Alcabes P, Friedland GH. Injection drug use and HIV1. Clin Infect Dis 1995;20:1467. [5] Stonebruner RL, et al. A larger spectrum of HIV related disease in intravenous drug users in NYC. Science 1988;242:916. [6] Battjes RJ, Pickens RW, Sloboda Z, et al. HIV risk factors among injecting drug users in five US cities. AIDS 1994;8: [7] Des Jarlais DC, Friedman SR, Stonebruner RL. HIV infection and intravenous drug use: Critical issues in transmission dynamics, infection outcomes and prevention. Rev Infect Des 1988;10: [8] Shufman E, Engelhard D, Bar-El CY, et al. Pattern of drug abuse and prevalence of antibodies to HIV in heroin addicts in Jerusalem, Isr J Med Sci 1990;26: [9] Maayan S, Shufman EN, Engelhard D, et al. Exposure to hepatitis B and C and to HTLV-1 and 2 among Israeli drug abusers in Jerusalem. Addiction 1994;89: [10] Epidemiological fact sheets by country. Russian Republic and the Ukraine. Accessed 2009 Oct 20. URL: [11] Chemtob D, Levit S, Mell H, Margolis A, Levy A, Leventhal A. Injecting clean or being clean? The International and Israeli experiences of syringe exchange program among injecting drug users. HaRefuah 2008;147(7): [Hebrew] [12] Russian immigration to Israel. URL: [13] Wormser GP, Forseter G, Joline C. Hepatitis C in HIVinfected intravenous drug users and Homosexual in Suburban New York City. JAMA 1991;265(22):2958. [14] Thomas DL, Vlahov D, Solomon L, et al. Correlates of hepatitis C virus infections among injection drug users. Medicine-Baltimore 1995;74(4): [15] Esteban JI, Esteban R, Viladomiu L, et al. Hepatitis C virus antibodies among risk groups in Spain. Lancet 1989;2(8658): [16] Miller CL, Johnston C, Spittal PM, Li K, Laliberte N, Montaner JS, Schechter MT. Opportunities for prevention: hepatitis C prevalence and incidence in a cohort of young injection drug users. Hepatology 2002;36(3): [17] Leventhal E. Summary of activity, Haifa: Hagefen Center, [18] Hamid A, Curtis B, McCoy K, et al. The heroin epidemic in New York City. Current status. J Psychoactive Drugs 1997;29: [19] Rahav G, Hasin D, Paykin A. Drinking pattern of recent russian immigrants and other Israelis:1995 national survey results. Am J Public Health 1999;89; [20] Hasin D, Rahev G, Meydan J, Neumark Y. The drinking of earlier and more recent Russian immigrants to Israel: comparison to other Israelis. J Subst Abuse 1998;10(4): [21] Srugo I, Shinar E, Bar-Shany S, Amos L. Hepatitis B and C markers among alcoholics in Israel: high incidence of HCV infection. Eur J Epidemiol 1998;14(4): [22] Rosman AS, Waraich A, Galvin K, Casiano J, Paronetto F, Lieber CS. Alcoholism is associated with hepatitis C but not hepatitis B in an urban population. Am J Gastroenterol 1996;91(3):

6 350 Daniel Chemtob, Maxim Gurevitz, Shabtai Levitt et al. [23] Lvov DK, Samokhvalov EI, Tsuda F, et al. Prevalence of hepatitis C virus and distribution of its genotypes in Northern Eurasia. Arch Virol 1996;141(9): [24] Naoumov NV. Hepatitis C virus infection in Eastern Europe. J Hepatol 1999;31(Suppl 1):84-7. [25] Hamers FF, Downs AM. HIV in central and eastern Europe. Lancet 2003;361(9362): [26] Chemtob D. Epidemiology of HIV/AIDS among intravenous drug users in Israel, Int Soc Addict Med (ISAM) Conf, Tel Aviv, 2001:81. [27] Chemtob D, Grossman Z. The epidemiology of adult and adolescent HIV infection in Israel, a country of immigration. Int J STD AIDS 2004:15(10): [28] Sherif MM, Abou-Aita BA, Abou-Elew MH, et al. Hepatitis B virus infection in upper and lower Egypt. J Med Virol 1985;15(2): [29] Said S, Larouze B, Biaud JM, et al. Seroepidemiology of hepatitis B in a population of a children in central Tunisia. Int J Epidemiol 1985;14(2): Submitted: December 19, Revised: January 28, Accepted: February 11, 2010.

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