Am. J. Trop. Med. Hyg., 74(6), 2006, pp. 1111-1116
Copyright © 2006 by The American Society of Tropical Medicine and Hygiene
HEPATITIS C INFECTION AMONG DRUG USERS IN NORTHERN THAILAND
JAROON JITTIWUTIKARN,
SATAWAT THONGSAWAT,
VINAI SURIYANON,
NIWAT MANEEKARN,
DAVID CELENTANO,
MYAT HTOO RAZAK,
NAMTIP SRIRAK,
TASSANAI VONGCHAK,
SURINDA KAWICHAI,
DAVID THOMAS,
TEERADA SRIPAIPAN,
DALE NETSKI,
ASHWIN ANANTHAKRISHNAN, AND
KENRAD E. NELSON*
Faculty of Medicine and Research Institute for Health Sciences, Chiang Mai University, Chiang Mai, Thailand; Northern Drug Dependence Treatment Center, Chiang Mai, Thailand; Departments of Medicine, and Epidemiology, Johns Hopkins Medical Institutions, Baltimore, Maryland
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ABSTRACT
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Illicit drug users are commonly infected with hepatitis C virus (HCV) and human immunodeficiency virus (HIV). We evaluated the prevalence, incidence, and risk behaviors associated with HCV infection in 1,859 drug users in northern Thailand. The HCV prevalence was 27.3%: 86.0% among drug injectors (IDUs) and 5.3% among those who did not inject. Sexual behavior was not significantly associated with HCV among IDUs or drug users who used but didn’t inject illicit drugs; only injection behaviors were independently associated with HCV in multivariate analysis. Among men, a history and increasing frequency of injecting drugs, older age, and a history of incarceration were associated with HCV infection. Among 514 opiate users who were HCV and HIV seronegative at baseline, 41 incident HCV infections and 6 HIV infections occurred on follow-up; the HCV incidence was 5.43/100 person-years; it was 44.3/100 person-years in IDUs and 1.9/100 person-years in non-injectors. HCV and HIV among drug users in Thailand are common and primarily associated with injection behavior.
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INTRODUCTION
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It has been estimated that as many as 170 million persons worldwide have chronic infections with hepatitis C virus (HCV).1 While many persons who are infected remain asymptomatic, HCV is an important cause of chronic active hepatitis, cirrhosis, liver failure, and hepatocellular carcinoma.2 In the United States, persons with cirrhosis from HCV infection constitute the majority of patients undergoing liver transplantation.3
HCV infections are primarily acquired parenterally, through contaminated injections, blood transfusions, or illicit injection drug use.4 Sexual transmission and perinatal transmission occur but are less common.5 The risk of acquisition of infection by blood transfusion has decreased substantially in recent years because of the screening of donors using serological or nucleic acid amplification methods to identify infected donors and exclusion of donors at highest risk.6,7
Several studies of injection drug users (IDUs) have found HCV prevalence rates between 60% and 90% in these populations.4 The overall prevalence of HCV infections in Thailand may have increased in recent years. The prevalence of HCV among persons screened as potential blood donors in northern Thailand increased from 1.5% in 1992 to 2.8% in 1998.8 Other studies of volunteer blood donors throughout Thailand have found HCV prevalence rates between 1.5% and 5.0%.8–11
The population injecting heroin and other opiates in Thailand also may have increased in the past two decades. In the 1980s, the cultivation of poppies in Thailand was dramatically reduced by the Thai government’s crop substitution program.12 This resulted in increased trafficking of processed opium and heroin from neighboring countries and an increase in the population injecting these illicit drugs.13 A study of temporal trends in the injection of illicit drugs among 21-year-old men randomly conscripted for military service in Thailand found the prevalence of a history of injecting illicit drugs to have increased from 1% in 1991 to 4% in 1997.14
Another factor influencing the recognition and importance of chronic HCV infections in Thailand is the continued high HIV prevalence among IDUs.15 Drug users who are co-infected with HCV and HIV have been reported to have increased liver-related morbidity and mortality.16,17 Since the mid-1990s, a dramatic increase has occurred in Thailand in the trafficking of amphetamines, which has been manufactured in Myanmar and Laos.18 Methamphetamine is known in Thai as "Ya Ba," meaning "crazy medicine," for its dramatic effect on behavior, with agitation, anxiety, insomnia, and personality changes.19
To evaluate the prevalence and risk factors for HCV and associations with HIV infection in drug users in northern Thailand, we studied a population of IDUs and non-IDUs who sought treatment at a government drug treatment center.
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MATERIALS AND METHODS
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The study population was enrolled from persons admitted to the Northern Drug Dependence Treatment Center (NDTC) in Mae Rim, Chiang Mai province in Thailand between February 1999 and March 2000. A total of 1,859 subjects were enrolled who consented to be tested for HIV and HCV and receive their test results with counseling. Opiate users (N = 514) who were HIV seronegative who did not live in a remote area and who agreed to be followed were seen at 6-month intervals for another 2 years to detect incident HIV and HCV infections. A detailed description of the enrollment procedure has been published previously.18
After obtaining informed consent, a risk factor questionnaire was administered by an interviewer. The data obtained included sociodemographic information, detailed history of injection and non-injection drug use, incarceration in a prison, cigarette and alcohol use, and sexual behavior history. We also collected information on the route of administration of the drugs (i.e. by injection, orally, smoking, or other routes) and the types of drugs used. For drug users who began using drugs by a non-parenteral route, the time of transition to injection of drugs was ascertained. The age of initiation of drug use and injection practices, including sharing of injection equipment, was determined.
To estimate the possible role of sexual transmission of HCV, we inquired about sexual behavior. We asked the age at initiation of sexual intercourse, lifetime number of sex partners, use of commercial sex workers (CSWs), condom use with CSWs and regular partners, history of sexually transmitted diseases (STDs), treatment of STDs, exchange of money or drugs for sex, and male homosexual sex.
A blood specimen was obtained and tested for antibodies to HCV using a licensed third-generation enzyme immunoassay (EIA; Abbott Laboratories, Abbott Park, IL). Initially reactive specimens were repeated in duplicate. Repeatedly reactive sera were tested for HCV RNA by nucleic acid amplification using polymerase chain reaction (PCR) amplification of the 5'-untranslated region of HCV.20 A total of 204 HCV EIA-positive samples were tested for HCV RNA using the COBAS Amplicor HCV test version 2.0 (Roche Molecular Systems, Branchburg, NJ). Samples that were PCR positive were genotyped by direct sequencing of the reverse transcriptase (RT)-PCR products.20 Nucleotide sequences of purified PCR amplicons were determined by use of a PRISM Version 3100 automatic sequencer. Genotypes were assigned based on homogeneity with consensus reference sequences in GenBank. Selected EIA-positive, PCR-negative samples were tested by RIBA-3 (Ortho Pharmaceutical, Raritan, NJ). Antibodies to HIV were detected using a licensed EIA (Vironostica HIV Uni-form II plus O; Organon Teknika, Durham, NC). Specimens reactive by EIA were tested using the gel-particle agglutination (GPA) test for antibodies to HIV (Serodia-HIV, Fujirebio, Tokyo, Japan). Specimens reactive on both EIA and GPA were considered to be HIV-positive. EIA-positive, GPA-negative samples were tested by HIV Western blot using licensed reagents (HIV Blot 2.2: Gene Laboratories Diagnostics, Singapore). Syphilis antibodies were detected by a rapid plasma reagin (RPR) test (Syph Screen; Shield Diagnostics, Dundee, Scotland, UK), and reactive specimens were confirmed by a TPHA test (passive particle agglutination test for antibodies to T. pallidum; Serodia TP-PA; Fujirebio, Tokyo, Japan). Chlamydia trachomatis and Neisseria gonorrhea were detected using the PCR method (Amplicor PCR Diagnostics; Roche Diagnostic Systems).
The data were analyzed using the 
2 test and multiple logistic regressions to estimate the unadjusted and adjusted odds ratios (ORs) and 95% confidence limits of the association of risk factors with prevalent HCV infection. Stratified analyses were done for participants with and without a history of the use of drugs by injection. For prospective follow-up to detect incident HCV and HIV infections, we used person-time methods to estimate incidence per person year and assumed that new cases of HCV infection occurred midway between the last negative and first positive test. An analysis of the HIV prevalence and associated risk factors has been published.18 The study was reviewed and approved by the institutional review boards at Johns Hopkins University, Chiang Mai University, and the Ministry of Public Health of Thailand.
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RESULTS
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Overall, a total of 1,859 participants, including 1,659 men and 200 women, were enrolled in the cross-sectional component of the study. The prevalence of HCV infection in the population, including IDUs and non-IDUs, was 27.3%. Overall, 168 (82.4%) of 204 specimens that were tested by PCR had detectable HCV RNA, of which 96% were typeable as genotype 3 (39%), 1 (31%), or 6 (26%) by nested RT-PCR of the core/E1 regions of the genome.20
Several sociodemographic characteristics were found to be associated with HCV infection. Men were more than twice (OR = 2.29) as likely to be HCV positive (Table 1
). Persons 20–39 years of age were more likely to be HCV infected than younger or older subjects (Table 1). There was no difference in infection rates between single and married persons, but those who were separated/widowed/or divorced had significantly higher prevalence of HCV infection (Table 1). There was no association of HCV with the level of formal education. Being a trader or laborer was significantly associated with HCV infection. A history of both cigarette smoking and alcohol use were associated with HCV infection (Table 2).
The type of illicit drug used before admission to the NDTC was associated with the HCV infection prevalence. Subjects who had used heroin had significantly greater HCV prevalence than those who had used opium, amphetamines, or another drug (Table 2
). Persons who had used both heroin and another drug had an intermediate risk. Among persons who had only used amphetamine, the HCV prevalence was 4.5% (Table 2). The HCV prevalence among subjects who had injected drugs was 86.0% compared with 5.3% among non-injectors (Table 2). Those who had injected drugs in the past year had a higher prevalence (88.0%) than those with a history of injecting drugs who had not injected in the past year (73.1%; OR = 2.69). Those who reported ever sharing injection equipment with another drug user or sharing in the past 3 months had a higher HCV prevalence than those who denied ever sharing (Table 2). However, the HCV prevalence was 79.5% among those with a history of injecting drugs who denied sharing injection equipment. There was no association between HCV infection prevalence and the interval between initiating illicit drug use and first injecting drugs.
Sexual risk factors were evaluated for their association with HCV prevalence. In univariate analysis, persons who were sexually experienced had a significantly greater HCV prevalence compared with those who reported never having had sex (Table 3). The age of first sex, among those who reported having had sex, was not associated with HCV infection. The HCV prevalence did not increase significantly among IDUs (Table 3) or non-IDUs (Table 4) with increased numbers of sex partners. No significant differences in HCV prevalence occurred among persons reporting a history of sex with a female sex worker (FSW) or among men who had sex with another man when the population was stratified by parenteral and non-injection drug use (Tables 3 and 4). A lifetime history of an STD was associated with an increased HCV prevalence among IDUs (Table 3) but not among non-IDUs (Table 4). There was a significant association between HIV and HCV seroprevalence among both IDUs and drug users without an injection history, although the latter group had a lower prevalence of both HIV and HCV (Table 5).
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TABLE 5 Association of HIV and HCV infections by drug users, who inject (IDUs) or not (non-IDUs) northern Thailand
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Several multivariate logistic regression models were constructed to evaluate the independent association of various risk behaviors for HCV prevalence. Among all men (N = 1,659), a history of injection of illicit drugs, increasing age, and incarceration in a jail or prison were independently significant (Table 6). However, in the same model, the number of sex partners (< 5 versus 
5), sex for money, or male to male sex (MSM) were not significant.
In multivariate models restricted to sexually active IDUs (N = 508), older age, incarceration in a jail, and daily injection in the past 3 months were significantly associated with HCV (Table 7). However, increased number of sex partners, sex for money, or MSM was not significantly associated with HCV infection in this model. In a multivariate model restricted to sexually active men who did not inject drugs (N = 958), increased age over 20 years was significantly associated with HCV, but incarceration and number of sex partners were not (Table 8).
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TABLE 8 Multivariate logistic regression model for HCV prevalence among all sexually active male non-IDUs (N = 958)
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Overall, 41 incident HCV infections were detected on follow-up of 514 HCV-negative, HIV-negative drug users at baseline. This is an incidence of 5.43/100 person-years; among IDUs, the incidence was 44.3/100 person-years, and in non-IDUs, the HCV incidence was 1.9/100 person-years. There were 6 HIV seroconverters; 5 occurred among the 41 HCV seroconverters and 1 among the 473 drug users who remained HCV negative.
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DISCUSSION
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Among drug users in northern Thailand, HCV infection is nearly universal in those who inject illicit drugs, but it is much less frequent among those without an injection history. The prevalence of HIV infection in this population has also been reported to be strongly associated with injection of drugs.18 Studies of injection drug users in other areas of Thailand have also detected a very high prevalence of HCV in these populations.21–25
In addition to a history of injection of drugs, HCV prevalence was found to be higher in men, in older subjects, in those who injected daily, and in those with a history of incarceration. These individual risk factors could all be associated with an increased likelihood of exposure to contaminated injection equipment from another HCV-infected person. IDUs had higher levels of sexual risk behavior than drug users who did not inject drugs (non-IDUs). However, the number of sex partners or a history of sex with an FSW or MSM was not significant when the analysis was stratified by the method of drug use. These data indicate that HCV infection in this population is primarily determined by drug use behavior. Although the HCV prevalence among non-IDUs was somewhat higher than that reported among blood donors, we found no good evidence that high-risk sexual behavior could have accounted for the higher HCV prevalence in this population. However, amphetamine use by the non-injection route could have influenced sexual and other behaviors.19 Analysis of HIV prevalence in this population also pointed to the importance of injection behavior as determinants of infection and failed to identify sexual behaviors as a significant risk for HIV prevalence.18
Some studies of populations of IDUs have found sexual behavior to be associated with HIV transmission.26,27 However, sexual activity is less efficient in the transmission of HCV than HIV in these populations. Nevertheless, we found evidence of the sexual transmission of HCV among the sexual partners of (non-drug using) blood donors in northern Thailand.28 Therefore, some emphasis probably should be given to counseling HCV-positive IDUs about the potential risks of the sexual transmission of the virus, especially those who are co-infected with HIV.5,29
In follow-up of HIV and HCV seronegative users who injected drugs, the HCV incidence was nearly 10-fold higher than the HIV incidence among those who did not inject; nearly one half of the IDUs who were HCV negative at baseline seroconverted per year of follow-up.
The high prevalence and incidence of both HIV and HCV among IDUs in Thailand is a substantial public health problem. Although the epidemic of sexually transmitted HIV has been brought under some control by an effective national program to reduce infection acquired through commercial sex and other programs targeted at reducing sexual transmission,30 the epidemic among IDUs has not been controlled.14,15,18
The Thai government has recently embarked on a program of expanded access to highly active anti-retroviral therapy (HAART) with a goal of providing 50,000 HIV/AIDS patients with HAART. Persons who are co-infected with HCV and HIV are likely to challenge the success of this expanded HAART program, because persons with HCV may be more difficult to treat because of liver-related co-morbidity.16,17
Received January 20, 2005.
Accepted for publication February 8, 2006.
Financial support: This research was supported in part by Grants DA-11333 and U01 DA-13032 from the National Institute of Drug Abuse, National Institutes of Health. None of the authors has a conflict of interest.
* Address correspondence to Kenrad E. Nelson, Department of Epidemiology, Johns Hopkins University, Bloomberg School of Public Health, 615 N. Wolfe Street, Baltimore, MD 21205. E-mail: kenelson{at}jhsph.edu 
Authors’ addresses: Jaroon Juttiwutikarn, Northern Drug Dependence Treatment Center, Mae Rim, Thailand. Satawat Thongsawat, Vinai Suriyanon, Niwat Maneekarn, Namtip Srirak, Tassanai Vongchak, and Surinda Kawichai, Faculty of Medicine and Research Institute for Health Sciences, Chiang Mai University, Chiang Mai, Thailand. David D. Celentano, David L. Thomas, Teerada Sripaipan, Dale Netski, Ashwin Ananthakrishnan, and Kenrad E. Nelson, Johns Hopkins Medical Institutions, Baltimore, MD, E-mails: kenelson{at}jhsph.edu. Myatt Htoo Razak, Medical officer (HIV/AIDS), World Health Organization, Thailand, Permanent Secretary Building 3, 4th Flr., Ministry of Public Health, Bangkok, Thailand.
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ABSTRACT
INTRODUCTION
