Hepatitis C Virus Infection: Prevalence, Risk Factors, and Prevention Opportunities among Young Injection Drug Users in Chicago,

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1 1588 Hepatitis C Virus Infection: Prevalence, Risk Factors, and Prevention Opportunities among Young Injection Drug Users in Chicago, Lorna E. Thorpe, 1,a Lawrence J. Ouellet, 1 Jennie R. Levy, 1 Ian T. Williams, 2 and Edgar R. Monterroso 3,a 1 Department of Epidemiology and Biostatistics, University of Illinois at Chicago, Chicago; 2 Hepatitis Branch, Division of Viral and Rickettsial Diseases, National Center for Infectious Diseases, and 3 Division of HIV/AIDS Prevention, Centers for Disease Control and Prevention, Atlanta Georgia The prevalence, risk factors, and prevention opportunities of hepatitis C virus (HCV) infection were studied in a large sample of 698 young adult injection drug users (IDUs) in Chicago, years old. Participants were recruited between 1997 and 1999 by using street outreach, targeted advertising, and chain-referral methods. HCV infection prevalence was 27% and was strongly associated with both age and duration of injecting ( P!.001). In multivariable analysis, sexual behaviors were unrelated to seropositivity. Independent drug-related risk factors included frequent injection, heavy crack smoking, injecting in a shooting gallery, and syringe-mediated sharing. Urban residents were more likely than suburban residents to be infected. Most research on hepatitis C has shown rapid spread of infection among IDUs, but these findings underscore that opportunities to identify IDUs uninfected with HCV may be greater than assumed and emphasize the need to target younger, newer IDUs. Injection drug users (IDUs) are at high risk for hepatitis C infection. Between 1992 and 1995, 43% of the persons in the United States with acute hepatitis C reported having injected drugs during the past 6 months, and 60% of those had a lifetime history of high-risk drug use [1 3]. The most common mode of hepatitis C virus (HCV) transmission among IDUs seems to be the multiperson use of contaminated syringes and other injection paraphernalia [1 3]. Surveys of adult, long-term IDUs in the United States consistently report seroprevalence levels of 70% 90% [4 8], signifying that HCV infection has reached saturation levels in this population [9]. The high rate of persistence of HCV infection and its ability to induce chronic liver disease indicate that current IDU populations will expe- Received 26 April 2000; revised 1 August 2000; electronically published 2 November Presented in part: 32d annual meeting of the Society for Epidemiologic Research, Baltimore, 10 June 1999 (abstract 340). Informed consent was obtained from all survey participants. Study protocols and consent agreements were approved by institutional review boards at the Centers for Disease Control and Prevention (CDC) and the University of Illinois at Chicago. No author has or had a commercial or other association that might pose a potential conflict of interest. Financial support: Funds from the CDC under Cooperative Agreement U64/CCU a Present affiliations: Division of Tuberculosis Elimination, CDC (L.E.T.), and Vaccine-Preventable Disease Eradication Division, National Immunization Program, CDC (E.R.M.). Reprints or correspondence: Dr. Lorna Thorpe, Division of Tuberculosis Elimination, Centers for Disease Control and Prevention, MS-E10, 1600 Clifton Rd., Atlanta, GA (lht2@cdc.gov). The Journal of Infectious Diseases 2000;182: by the Infectious Diseases Society of America. All rights reserved /2000/ $02.00 rience the bulk of future HCV-associated morbidity and mortality in this country. HCV infection seems to be acquired more rapidly after initiation into injection drug use than is infection with the human immunodeficiency virus (HIV) or the hepatitis B virus [3, 10, 11], but there is uncertainty about how quickly hepatitis C saturation occurs following injection initiation. A cross-sectional study of 2921 IDUs in Baltimore who were recruited in observed a prevalence of 85% in the total sample and 79% among those who reported having injected!2 years ( n p 135; median age, 28 years), indicating near-saturation 2 years after initiation into injection drug use [10, 12]. The only published study in the United States, to our knowledge, that has addressed HCV infection among young IDUs was also conducted in Baltimore. The authors reported a baseline HCV prevalence of 38% in 1994 among the 229 participants, most of whom were years old (median age, 24 years) [3]. Of the 135 participants who had injected for 2 years, only 21% tested positive for HCV. The wide disparity in prevalence levels between the 2 Baltimore studies indicates the need for further investigation. The feasibility of primary prevention activities to reduce the incidence of HCV infection among IDUs depends on the speed at which they become infected and the ability of prevention programming efforts to reach those who are uninfected [13]. With HCV prevalence having reached saturation levels among middle-aged, long-term injectors, researchers need to confirm trends in the development of infection in newer and younger IDUs. Our purpose was to use serological and survey data from a large and diverse sample of young adult IDUs in Chicago to examine the prevalence patterns of HCV infection and deter-

2 JID 2000;182 (December) Hepatitis C Infection Prevalence in Young IDUs 1589 Figure 1. Percentage of hepatitis C infection prevalence, by duration of injection drug use, in months, among young adult injection drug users, Chicago, mine the drug- and sex-related risk factors associated with infection. We paid specific attention to the relationships among prevalence, duration of injection drug use, and age, to extrapolate information on infection trends. We also examined, we believe for the first time, the different patterns of prevalence between suburban and urban young IDUs, on the basis of the substantial representation of suburban IDUs in the sample. Subjects and Methods Study population. The participants were IDUs, years old, who were recruited in Chicago and its suburbs. The study was conducted from storefront offices in 4 low-income neighborhoods, each selected for its high concentration of drug use and distinct racial and ethnic composition. The North Side storefront is in a multiethnic neighborhood, where the largest racial/ethnic group is white. The West Side office is in a largely African-American area, where extensive and easily accessed drug markets attract IDUs from across the city and suburbs. The Northwest Side office is in the heart of Chicago s Puerto Rican community, and the South Side site is in an area populated almost exclusively by African Americans. The cohort was developed as part of Collaborative Injection Drug Users Study II (CIDUS II), a multisite longitudinal study, focusing on initiates to drug injection, that was conducted under a cooperative agreement with the Centers for Disease Control and Prevention (CDC). Between August 1997 and April 1999, participants were recruited through street outreach, targeted advertising, and chain referral. Street recruiting by former IDUs was done in areas such as youth hangouts, shooting galleries (places where addicts gather to inject drugs and perhaps to be assisted in injecting), and illicit drug markets. Advertisements were placed in alternative magazines and newspapers and on college campuses. In a version of respondentdriven sampling [14], each newly interviewed participant received 3 6 coupons to distribute to eligible peers. When one of these numbered coupons was redeemed through enrollment in the study, the peer recruiter received an incentive fee of $10. Half (54%) of the participants were recruited by their peers using coupons, a method that, in preliminary analyses, proved to be more successful at recruiting suburban and white respondents than at recruiting urban minorities [15]. Persons were eligible for the study if they were years old, had proof of their birthdate, and reported having injected drugs in the 6 six months. Recent injection drug use was verified by inspecting for stigmata, such as scars or abscesses. Persons with old scars were questioned about their recent injection use. When stigmata were absent, we conducted an injection screening interview, a series of questions to ascertain familiarity with injection routines. This element of the screening was important, because new IDUs often have little physical evidence of injection use. To prevent coaching that would enable persons who had not injected drugs to pass the screening test and enroll in the study, we used 4 versions of our screening questionnaire and rotated them according to recruitment chains. Data collection. Trained interviewers administered a standardized face-to-face interview in a private room, after which phlebotomists provided pretest counseling about HIV, HCV, and other bloodborne pathogens and drew blood samples. Serological specimens were batch-shipped to the Hepatitis Branch at the CDC, to be tested by ELISA (Abbott HCV EIA 2.0; Abbott Laboratories, Abbott Park, IL). All positive samples were retested twice by ELISA, but no confirmatory testing was performed because of the study population s high risk for infection and high likelihood of

3 1590 Thorpe et al. JID 2000;182 (December) univariable and multivariable analyses were conducted by using Statistical Analysis Software (SAS; SAS Institute, Cary, NC). Results Figure 2. Percentage of hepatitis C infection prevalence, by duration of injection drug use, in years, and age group. testing positive if confirmatory assay methods were used (195% likelihood in a previous, similar study) [10]. Study protocols were explained to participants, and informed consent was obtained prior to data collection. All participants were compensated $25 for the interview. The survey instrument was developed by the CDC and principal investigators from each of the study sites. Respondents were asked about demographic characteristics, alcohol and other drug use, drug use in the past 6 months (i.e., frequency of drug use and types of drugs used, circumstances of initiation, recent injection practices, and needle exchange and needle acquisition practices), recent sexual behaviors, imprisonment, and medical and drug treatment. At the close of the interview, respondents were counseled about reducing their risk for HIV and hepatitis and were given information about drug treatment programs, an on-site hepatitis B vaccination program, and other services provided by trained staff members. All respondents were given appointments to return for their HCV test results and posttest counseling. Any clients screening positive for HCV antibodies were referred to 1 of 2 liver clinics for full diagnostic testing and possible treatment. Data analysis. We examined associations between seropositivity to HCV and study variables in both univariable and stratified analyses, using x 2 -based adjusted odds ratios (AORs) and 95% confidence intervals (95% CIs) to depict the magnitude and strength of associations. Independent variables were selected on the basis of findings from research on prevalent and incident viral infections in IDUs and included demographic characteristics, drug-use practices, and sexual behaviors. After identifying factors significantly associated with HCV infection at the univariable level, we performed a more detailed stratified analysis, adjusting for age and cumulative parenteral exposure (defined by duration and frequency of injecting drug use), to evaluate the effects of confounding and potential effect modification ( a p.05) and to identify risk and demographic variables with a sufficiently robust association to HCV infection to be considered for multivariable analysis. Multiple logistic regression models were then constructed, to identify independent predictors of HCV infection. The final model was confirmed, by backward selection techniques, to have the best fit. Both By December 1998, 700 IDUs, years old, had enrolled in the study and completed the interview, and all but 2 respondents had opted for a blood screening ( n p 698). Serolog- ical evidence of HCV infection was detected in 190 (27%) of the participants. Despite initiating our recruitment efforts in low-income, predominantly minority urban neighborhoods, 58% of the enrollees were white and 38% resided in suburbs. HCV infection was positively associated with age, female sex, Hispanic ethnicity, urban residence, and having been in prison and was negatively associated with having some college education and living with a parent (table 1). At study enrollment, 34% of respondents had injected for 1 year, median injection duration was 2 years (range,!1 20 years), and 75% of the sample had begun injecting within the past 4 years. Infection with HCV was strongly associated with duration of injection. The sharpest increases in HCV infection levels were observed to be at years 1 and 4 of injecting (figure 1). These breaks provided reasonable categories for summarizing risks associated with duration of use in stratified and multivariable models. Compared with those who had injected for!1 year, those who had injected for 1 4 years were nearly 3 times more likely to be infected with HCV; those who had injected for 14 years were 10 times as likely to be infected. Nearly half of the sample reported having injected on a daily basis for the past 6 months, and daily injectors were nearly 3 times more likely to be infected with HCV than were those who injected less often. Older IDUs showed a greater risk of infection in each stratum of injection drug use duration. Among study participants who began injecting in the past year, 21% of those years old tested positive for HCV infection, whereas prevalence was!10% in the 2 younger groups (figure 2). Similarly, among those who had injected for 4 years, prevalence was much lower among those years old. Heroin was overwhelmingly the drug used most often (198% of participants from each racial/ethnic group reported injecting heroin in the past 6 months), but polydrug use was common. In univariable analysis, HCV infection was positively associated with smoking crack 4 days per week and having injected cocaine during the past 6 months. Other drug-related risk variables positively associated with infection were a history of injecting in shooting galleries, practicing needle exchange in the past 6 months, engaging in backloading during the past 6 months (receiving drugs into one s syringe from another syringe for the purposes of measuring and dividing), and the age of the person who initiated the participant into injection drug use. Those initiated by persons 5 years older than themselves had

4 JID 2000;182 (December) Hepatitis C Infection Prevalence in Young IDUs 1591 a higher prevalence of HCV infection than those initiated by their age peers or someone younger than themselves. Other than backloading, measurements of syringe sharing or the multiperson use of nonsyringe paraphernalia in the past 6 months were not related to infection. Because this was an unusual finding, we examined the associations in more detail. All responses to questions on frequency of sharing paraphernalia in the prior 6 months were originally coded as one of the following: never, less than half the time, half the time, more than half the time, or always. We examined trend statistics across these responses and the association between different frequency levels of sharing for each type of paraphernalia. No increasing trend of HCV infection prevalence was observed with increased frequency of receptive syringe sharing, and a nonsignificant positive trend was observed between sharing nonsyringe paraphernalia (i.e., cotton filters, cookers, and rinse water) and HCV infection ( P p.148). This lack of association was not confounded or modified by age or by duration or frequency of injection. Only 9% of the sample reported no sexual activity in the past 6 months, and the median number of sex partners during that time was 1 (range, ). Sex-related risk factors associated with infection in the past 6 months were engaging in commercial sex or having a sex partner who was also an IDU. Sex-related risk factors found to be unrelated to HCV infection included number of sex partners in the past 6 months, sexual orientation, and self-reported history of a sexually transmitted disease (data not shown). All factors associated with HCV infection in univariable analyses were then re-examined after adjusting for duration and frequency of injection and for age. These analyses were performed to determine whether associations were independent of cumulative parenteral exposure. Among the drug-related risk factors, the association between prevalent HCV infection and the age of the initiator to injection drug use (AOR, 1.24; 95% CI, ) and the association between needle exchange program use and HCV infection (AOR, 1.34; 95% CI, ) were no longer significant in these models. Associations between sex-related risk variables and HCV infection were also not significant. We then submitted the factors that had remained associated with prevalent infection to multivariable modeling. In the final multiple logistic regression model, drug-related risk factors independently associated with HCV seropositivity were duration of injection drug use, frequency of injection, shooting gallery use, backloading, and heavy crack smoking (table 2). Urban residents were more likely than suburban residents to be infected, and age remained a strong positive predictor of infection. African-American participants in our sample had significantly lower prevalence levels of infection than either whites or Latinos, independent of the measured behavioral risk factors and the fact that 95% of all African-American respondents were urban residents. Last, participants with a minimum of a high Table 1. Demographic and risk-related characteristics of young adult injection drug users in Chicago, , by hepatitis C status. Variable Total sample (N p 698) Hepatitis C positive (n p 190) Odds ratio (95% CI) Age at enrollment, years (44) 40 (21) (25) 49 (26) 2.6 ( ) (31) 101 (53) 6.1 ( ) Race/ethnicity White 404 (58) 86 (45) 1.00 Hispanic 155 (22) 64 (34) 2.6 ( ) Black 118 (17) 34 (18) 1.5 ( ) Other 21 (3) 6 (3) 1.5 ( ) Sex Male 454 (65) 112 (59) 1.00 Female 244 (35) 78 (41) 1.4 ( ) Educational level, years! (43) 104 (55) or GED 240 (34) 63 (33) 0.7 ( ) (23) 23 (12) 0.3 ( ) Residence Urban 432 (62) 152 (80) 1.00 Suburban 266 (38) 38 (20) 0.3 ( ) Ever imprisoned No 152 (22) 20 (11) 1.00 Yes 546 (78) 170 (89) 3.0 ( ) Duration of injection drug use, years!1 201 (29) 20 (11) (44) 71 (37) 2.7 ( ) (27) 99 (52) 9.9 ( ) Frequency of injection, past 6 mo Less than daily 368 (53) 65 (34) 1.00 Once or more daily 330 (47) 125 (66) 2.8 ( ) Drugs injected, past 6 mo Heroin 691 (99) 186 (27) 0.3 ( ) Speedball 258 (37) 90 (35) 1.8 ( ) Cocaine 186 (27) 66 (35) 1.7 ( ) Crack use, past 6 mo None or low (!4 days/ 623 (89) 151 (79) 1.00 week) High ( 4 days/week) 75 (11) 39 (21) 3.4 ( ) Age of person initiating injection drug use!5 years older 447 (64) 96 (51) years older 251 (36) 94 (49) 2.2 ( ) Shared paraphernalia, past 6mo Needles 348 (50) 94 (27) 1.0 ( ) Any equipment 516 (74) 143 (28) 1.1 ( ) Backloading 196 (28) 69 (35) 1.7 ( ) Ever injected drugs in shooting gallery No 513 (74) 114 (60) 1.00 Yes 184 (26) 76 (40) 2.5 ( ) Used needle exchange program, past 6 mo No 453 (65) 109 (57) 1.00 Yes 245 (35) 81 (43) 1.6 ( ) Sex partners, past 6 mo (76) 138 (73) (25) 52 (27) 1.2 ( ) Commercial sex, past 6 mo No 587 (84) 147 (77) 1.00 Yes 111 (16) 43 (23) 1.9 ( ) NOTE. Data are no. (%), except where noted otherwise. CI, confidence interval; GED, general equivalency diploma; mo, months; speedball, simultaneous injection of heroin and cocaine.

5 1592 Thorpe et al. JID 2000;182 (December) Table 2. Multiple logistic regression analysis for factors associated with hepatitis C seropositivity among young injection drug users in Chicago, Characteristic Total sample (N p 698) Adjusted odds ratio a (95% CI) Duration of injection drug use, years! ( ) ( ) Frequency of injection Less than daily Once or more daily ( ) Backloading, past 6 mo No Yes ( ) Ever injected drugs in shooting gallery No Yes ( ) Crack use, past 6 mo None/low (!4 days/week) High ( 4 days/week) ( ) Residence Suburban Urban ( ) Education Didn t complete high school High school diploma, GED, or higher ( ) Race/ethnicity White Hispanic ( ) Black ( ) NOTE. CI, confidence interval; GED, general equivalency diploma; mo, months. a Adjusted for age and all other listed variables. school diploma or its equivalent were nearly 2 times less likely to be infected than those with a lower educational level. Discussion In this study of IDUs years old, the prevalence of HCV infection was 15% among those who had injected 2 years and 27% among the sample as a whole. Given that most research on hepatitis C has shown saturation among older, long-term IDUs, these findings underscore the need to target younger, newer IDUs for prevention efforts. During the late 1980s, researchers in Baltimore found that HCV infection developed quickly after initiating drug injection and that it reached near-saturation in only 2 years. These findings suggested that prevention resources should be concentrated on persons at high risk for beginning to inject. Our findings, which are based on a large sample, coupled with prevalence data from the recent Baltimore study [3], provide new evidence that, among young adult IDUs, sufficient time exists between the initiation of injection drug use and HCV infection to target them for prevention. Many of the identified risk factors for HCV infection in our study are similar to those previously reported. Duration of injection drug use [3, 4, 7, 10, 16 18] and frequency of injection [5, 10, 16, 18] are the 2 factors most often reported, and they most likely reflect a cumulative potential exposure to contaminated injection equipment [16]. Two other cited risk factors confirmed in our study include sharing needles in high-risk settings, such as shooting galleries [5], and backloading [6]. In IDU studies, a number of sexual risk factors have typically been crudely associated with hepatitis C prevalence, but, as found in our analysis, these associations tend to disappear when drug-related risk practices are accounted for in multivariable analyses [3, 5, 10, 18]. A significant new finding in this study was that over one third of the sample comprised young white suburban participants. The addition of peer-driven sampling methods in this study appeared to have increased enrollment of younger, nonurban IDUs, 87% of whom were white. Population estimates of heroin use from the 1997 National Household Survey on Drug Abuse indicated that 56% of persons using heroin in the previous year were non-hispanic white [19]. This estimate may not be reflective of recent heroin use in Chicago, but it does provide some indication that a sample with 58% enrollment of white IDUs may be within a reasonable range of the area s true distribution. We found a large difference in prevalence between the urban and suburban IDUs (35% vs. 14%, respectively), a finding that is partially explained by the younger age and shorter duration of injecting of suburban IDU participants. The varying background prevalence suggests that young urban IDUs who engage in high-risk practices have a greater likelihood of being exposed to persons already infected by HCV than do suburban IDUs engaging in the same behaviors. However, the potential for dramatic amplification of infection levels in the suburbs is cause for concern, given the high level of reported sharing practices by suburban IDUs (48% vs. 28% syringe sharing in the past 6 months among suburban vs. urban participants, respectively). Some studies have found higher rates of HCV infection in minority populations [4, 12, 20, 21]. In our study, differences in prevalence levels between whites and Hispanics largely disappeared after adjusting for age differences between the 2 groups. African Americans, however, remained significantly less likely to be infected than were other participants, despite multiple adjustments, suggesting that factors other than those examined might be important. Recent ethnographic research in Chicago has found that drug injection is more stigmatized among African-American heroin users than among whites and Hispanics [22]. A greater desire to hide injection from peers could result in young African-American IDUs having relatively small and isolated injection networks, thus reducing the spread of HCV. Although more research is needed to investigate these possibilities, it is noteworthy that non African-American race or ethnicity was also a significant predictor of HCV prevalence in the sample of young IDUs from Baltimore.

6 JID 2000;182 (December) Hepatitis C Infection Prevalence in Young IDUs 1593 This study has several limitations to consider when interpreting its findings. First, because the analysis was based on cross-sectional data, the temporal relationship of risk behaviors to the acquisition of HCV infection is uncertain. This may explain our inability to detect an association between infection and borrowing or sharing syringes or other injection paraphernalia in the past 6 months, either in univariable or in multivariable analysis. The apparent lack of association between reported sharing practices and HCV infection prevalence in this study is unusual but may be a function of the study population s characteristics. The sample was composed of young IDUs, many with short durations of injection and high levels of sharing practices. In this setting, recent risky sharing behaviors may not correlate greatly with prevalent infection, particularly when infection prevalence is low and risk behaviors are high. Second, behavioral data were self-reported and therefore were subject to biases associated with differences in the accuracy or completeness of reporting past behaviors or experiences. To minimize recall bias, most behavioral questions concerned the past 6 months, and interviewers asked about significant life circumstances during that time to help participants remember specific behaviors. Some participants may have responded with socially desirable answers, thereby reducing the data s validity. Such influences tend to occur if IDUs are interviewed in settings unfamiliar to them, where, they may fear, drug-related behaviors are more readily condemned [23]. By interviewing in storefront offices operated by staff with past experience in using injected drugs, participants may have been more likely to speak truthfully about their experiences. Risk reduction counseling, which could encourage socially desirable responses, was provided after the interview. Third, the sample was not randomly selected, due to the known difficulty in enumerating IDU populations and employing random sampling methods. Thus, the extent to which findings can be generalized to other young IDUs in Chicago and elsewhere is unknown. In this study, however, we used multiple recruiting sites and methods to reduce sample bias, and the study s large sample size is a particular strength in ensuring that our findings may apply to other groups. Our findings show that interventions to prevent HCV transmission among young, new drug injectors are needed and that sufficient time exists between the initiation of injection drug use and most HCV infections to implement prevention interventions. Given the moderately high levels of infection we observed, reductions in hepatitis C risk behaviors should substantially reduce the number of new infections. In our experience, most young IDUs are, at best, vaguely aware of the risk for HCV infection, but they are motivated to avoid infection as awareness increases. Prevention efforts should target both urban and suburban populations, should focus on reducing risky injection practices, and should include educational and motivational components, riskreduction materials, drug-treatment programs tailored to the needs of young IDUs, and promotion of hepatitis A and B vaccination [13]. Because injection drug use seems to be a highly efficient mode of transmitting HCV infection, particular effort should be directed toward helping young IDUs to stop injecting drugs and, if possible, cease engaging in illicit drug use altogether. Acknowledgments We thank the entire field staff of Community Outreach Intervention Projects for their dedication and tireless efforts in identifying, recruiting, and providing services to the respondents enrolled in this study. Special thanks goes to each of the project interviewers: Steven Diaz, Brenda Delgado, Maria Nieves, Cheryl Nix, Meshoun Doursey, Julio Garcia, Jesus Saenz, Oscar Tanner, and Jose Curiel. A number of colleagues provided early reviews of the manuscript, and we d like to thank them for their comments: Susan Bailey, Jack Goldberg, Ronald Hershow, and Michael Hansen. From the Centers for Disease Control and Prevention (CDC), we are grateful to Richard Garfein, Miriam Alter, and Steve Jones for their suggestions. 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