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Prevalence of Hepatitis C Virus Infection among Injection Drug Users in the United States, 1994–2004

  1. Joseph J. Amon1,
  2. Richard S. Garfein2,3,
  3. Linda Ahdieh-Grant2,
  4. Gregory L. Armstrong1,
  5. Lawrence J. Ouellet6,
  6. Mary H. Latka7,
  7. David Vlahov7,
  8. Steffanie A. Strathdee3,
  9. Sharon M. Hudson4,
  10. Peter Kerndt5,
  11. Don Des Jarlais8, and
  12. Ian T. Williams1
  1. 1Divisions of Viral Hepatitis, New York
  2. 2HIV/AIDS, Centers for Disease Control and Prevention, Atlanta, Georgia, New York
  3. 3Department of Family and Preventive Medicine, University of California–San Diego, School of Medicine, San Diego, New York
  4. 4Health Research Association, Hollywood, New York
  5. 5Los Angeles County Department of Public Health, Los Angeles, California, New York
  6. 6Division of Epidemiology and Biostatistics, School of Public Health, University of Illinois at Chicago, Chicago, New York
  7. 7New York Academy of Medicine, New York
  8. 8Baron Edmond de Rothschild Chemical Dependency Institute at Beth Israel Medical Center, New York
  1. Reprints or correspondence: Dr. Joseph J. Amon, HIV/AIDS Program, Human Rights Watch, 350 Fifth Ave., 34th Fl., New York, NY 10118-3299 (amonj{at}hrw.org).
 
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Abstract

Objective. To examine hepatitis C virus (HCV) seroprevalence among injection drug users in 4 US cities from 1994 through 2004.

Methods. Demographic characteristics, behaviors, and prevalence of HCV antibody among 5088 injection drug users aged 18–40 years from Baltimore, Maryland; Chicago, Illinois; Los Angeles, California; and New York, New York, enrolled in 3 related studies—Collaborative Injection Drug User Study (CIDUS) I (1994–1996), CIDUS II (1997–1999), and CIDUS III/Drug User Intervention Trial (2002–2004)—were compared using the χ2 and Mantel-Haenszel tests of significance. Trends over time were assessed by logistic regression.

Results. Prevalence of HCV infection was 65%, 35%, and 35% in CIDUS I, CIDUS II, and CIDUS III, respectively. The adjusted prevalence odds ratio (OR) of being HCV antibody positive increased with the number of years of injection drug use (OR, 1.93 [95% confidence interval {CI}, 1.68–2.21] for each year of injecting within the first 2 years; OR, 1.09 [95% CI, 1.07–1.11] for each year of injecting beyond the first 2 years). Significant decreases were observed in the prevalence of HCV antibody between CIDUS I and CIDUS III in Baltimore (OR, 0.30; 95% CI, 0.20–0.43) and Los Angeles (OR, 0.17; 95% CI, 0.09–0.31) and among people of races other than black in Chicago (OR, 0.12; 95% CI, 0.08–0.17). No decrease in prevalence was seen in New York (OR, 1.04; 95% CI, 0.69–1.58) or among blacks in Chicago (OR, 0.55; 95% CI, 0.16–1.90).

Conclusion. Although regional differences exist, our data suggest that the incidence of HCV infection among injection drug users in the United States decreased from 1994 through 2004.

In the United States, hepatitis C virus (HCV) seroprevalence has been reported in 75%–90% of long-term injection drug users [1–5] and in 18%–38% of shorter-duration (<3 years) injection drug users [5–9]. Although the incidence of HIV infection was reported to have decreased among injection drug users in New York City [10,11] and Baltimore [12] in the 1990s, geographically diverse studies have continued to find a high incidence of HCV infection among injection drug users, in the range of 10%–35% per year [4, 8, 9, 13–15].

Because acute HCV has a low case-fatality rate and because antibodies to HCV are long lasting, the prevalence of HCV infection closely reflects the cumulative incidence of infection in a population. Thus, studies consistently report a direct correlation between the duration of injection drug use and HCV prevalence, suggesting that rates of change in prevalence by duration of injection drug use could provide insights into changes in risk of HCV infection at different points along the “injection career” of an injection drug user. The incidence of HCV infection among recently initiated injection drug users is also important in the consideration of the design of effective interventions to prevent transmission of HCV. A high incidence of HCV infection among recently initiated injection drug users argues for a greater effort to reach non-injection drug users before they transition to injection drug use [16], whereas a lower incidence could suggest the possibility of a “window of opportunity” for interventions to reach those who have recently begun injecting drugs, to prevent HCV infection [7] and other bloodborne infections (e.g., infection with HIV or hepatitis B virus) that typically follow [2].

Using data from 3 related studies conducted in the United States from 1994 through 2004 in 4 US cities, we examined HCV seroprevalence by site, race, and duration of injection drug use and identified factors associated with HCV infection.

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Methods

Data from 3 related, multisite studies—Collaborative Injection Drug User Study (CIDUS) I, CIDUS II, and CIDUS III/Drug User Intervention Trial—that share similar study methods were used for the analysis. Data from 4 sites (Baltimore, Maryland; Chicago, Illinois; Los Angeles, California; and New York, New York) that participated in all 3 studies were analyzed. Methods for each of these studies have been described in detail elsewhere [5, 15, 17–19]. Briefly, the objectives of the CIDUSs were to estimate the prevalence and incidence of bloodborne infections among injection drug users and to identify risk factors associated with infection and seroconversion. The first study, CIDUS I, enrolled injection drug users from 1994 through 1996. CIDUS II enrolled injection drug users from 1997 through 1999, and CIDUS III enrolled injection drug users from 2002 through 2004. A uniform protocol was followed with respect to community-based recruitment, eligibility criteria, interview procedures, and serum collection across all studies and sites. Participants were individuals who reported having injected drugs in the past 6 months. The age of participants varied slightly in each study; however, individuals aged 18–40 years were included in the present analysis. The studies were approved by institutional review boards at the Centers for Disease Control and Prevention and at each participating institution.

Interviews were administered by trained study staff or with computer-assisted interviewing software and were conducted before pretest counseling and venipuncture. Questions on current drug use (type and frequency) and injecting practices referred to the 6 months preceding the interview date for CIDUS I and CIDUS II and to the past 3 months for CIDUS III. Additional variables in the interview included sociodemographic data, sexual risk behaviors, duration of drug injection, and specific injecting practices.

Blood specimens were sent to the Centers for Disease Control and Prevention for serologic testing of HCV antibodies. Samples from CIDUS I and CIDUS III were tested using a third-generation EIA (ORTHO Hepatitis C Virus Version 3.0 ELISA; Ortho-Clinical Diagnostics). Positive samples having a signal-to-cutoff ratio of <3.8 were verified using a recombinant immunoblot assay (RIBA; Chiron Corporation) [20]. Samples from CIDUS II were tested twice by use of a second-generation EIA (Abbott Hepatitis C Virus ELISA 2.0; Abbott Laboratories), but no supplemental immunoblot testing was performed, on the basis of the high positive predictive value of repeat reactive ELISA testing in this population (a sample of 100 repeat reactive specimens were tested with a supplemental recombinant immunoblot assay [RIBA; Chiron Corporation], and all were found to be positive).

Demographic characteristics, behaviors, and the prevalence of HCV antibody among injection drug users were compared using the χ2 and Mantel-Haenszel tests of significance. The prevalence of HCV antibody for each study period was examined by site, race, and duration of injection drug use. Trends over time were further assessed by logistic regression. To adjust for differences in subject characteristics among the studies, a multivariate model was developed that controlled for age, sex, number of years injecting drugs, intensity of injection drug use, most frequently injected drug, race, and study site. All statistically significant terms identified through bivariate analyses were considered in the logistic model and were retained on the basis of a comparison of likelihood-ratio tests from nested models. Multiple potential interaction terms were evaluated for statistical significance on the basis of the significance of independent terms and their epidemiologic relevance, and plausibility and statistically significant (P<.05) interactions were maintained. Continuous variables were examined for linearity, and, when linear assumptions were not upheld, categorical variables were created.

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Results

From CIDUS I, 1079 participants aged 18–40 years with a determined HCV antibody status were included in the analysis. A total of 16% were non-Hispanic whites, and 69% had injected drugs for ⩾5 years. Most (61%) injected drugs ⩾1 time/day, and 48% most frequently injected heroin (table 1).

Figure 1
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Figure 1

Prevalence of hepatitis C virus antibody (Anti-HCV) and duration of injection by site, race, and study. Red lines, Collaborative Injection Drug User Study (CIDUS) I, 1994–1996. Blue lines, CIDUS II, 1997–1999. Green lines, CIDUS III, 2002–2004. Lines with and data n ! 20 points with n ! 4 were suppressed. LA, Los Angeles; NYC, New York City.

Table 1
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Table 1

Demographic characteristics, drug use behaviors, and prevalence of hepatitis C virus (HCV) antibody among injection drug users who participated in Collaborative Injection Drug User Study (CIDUS) I, CIDUS II, and CIDUS III.

From CIDUS II, 1424 individuals were included, 47% of whom were non-Hispanic whites and 27% of whom had injected drugs for ⩾5 years. A total of 42% of the study participants injected ⩾1 time/day, and 69% most frequently injected heroin (table 1).

From CIDUS III, 2585 individuals were included, 62% of whom were non-Hispanic whites. Just less than half (48%) had injected drugs for ⩾5 years. A total of 68% of study participants injected ⩾1 time/day, and 60% reported most frequently injecting heroin (table 1).

Within each study period, the prevalence of HCV antibody varied by race (P<.001), frequency of injecting drugs (P<.001), and type of drug injected (P<.001). The highest prevalence of HCV antibody was found among Hispanics (83%, 45%, and 41% for CIDUS I, CIDUS II, and CIDUS III, respectively), individuals injecting ⩾1 time/day (74%, 50%, and 41% for CIDUS I, CIDUS II, and CIDUS III, respectively), and those most frequently injecting heroin and cocaine together (74%, 74%, and 60% for CIDUS I, CIDUS II, and CIDUS III, respectively) (table 1).

Prevalence of HCV antibody also increased with age and number of years of injecting drugs (P<.001 for each study period). Differences between the distribution of response to all variables in table 1 by period were statistically significant (P<.01) by χ2 test (table 1).

The prevalence of HCV antibody increased with reported length of time of injecting in all 3 study periods and across all 4 sites, with some variation in rate of increase (figure 1). A multivariate model that included age, number of years injecting drugs, intensity of injection drug use, most frequently injected drug, race, and study site found similar results (table 2). Significant interactions were found between study period and site, and for 1 site (Chicago), a 3-way interaction was found among study period, site, and race/ethnicity. Sex was removed from the model because of a lack of statistical significance (P>.05).

Table 2
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Table 2

Adjusted prevalence ORs and 95% CIs for positivity for hepatitis C virus antibody among participants of Collaborative Injection Drug User Study (CIDUS) I (1994–1996), CIDUS II (1997– 1999), and CIDUS III (2002–2004).

The multivariate model found that the adjusted prevalence OR (hereafter, “OR”) of being HCV antibody positive increased with age (OR, 1.09 per year; 95% CI, 1.07–1.11), the number of years of injection drug use (OR, 1.93 [95% CI, 1.68–2.21] for each year of injecting drugs within the first 2 years; OR, 1.09 [95% CI, 1.07–1.11] for each year of injecting drugs beyond the first 2 years), and injection frequency (OR, 4.41 [95% CI, 2.87–6.77] for ⩾1 time/day, compared with never injecting during the recall period) (table 2).

Individuals injecting heroin and cocaine together had a higher odds of being HCV antibody positive (OR, 2.73; 95% CI, 1.87–3.98) than did those injecting heroin alone. The odds of being HCV antibody positive were highest among Hispanics (OR, 5.50; 95% CI, 4.15–7.29) and non-Hispanic whites (OR, 4.18; 95% CI, 3.23–5.41), compared with blacks. Injection drug users in Baltimore (OR, 2.16; 95% CI, 1.40–3.33) and Los Angeles (OR, 1.73; 95% CI, 0.99–3.04) were more likely to be HCV antibody positive, whereas injection drug users in New York were less likely (OR, 0.43; 95% CI, 0.28–0.65), compared with injection drugs users in Chicago.

Significant decreases in prevalence of HCV antibody were found between CIDUS I (1994–1996) and CIDUS III (2002–2004) in Baltimore (OR, 0.30; 95% CI, 0.20–0.43) and Los Angeles (OR, 0.17; 95% CI, 0.09–0.31) and among people of races other than black in Chicago (OR, 0.12; 95% CI, 0.08–0.17). No statistically significant change in prevalence of HCV antibody was seen in New York (OR, 1.04; 95% CI, 0.69–1.58) or among blacks in Chicago (OR, 0.55; 95% CI, 0.16–1.90).

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Discussion

The prevalence of HCV antibody among injection drug users continues to be extremely high in the United States, with >1 in 3 being infected within the first 5 years after initiation of injection drug use. Although previously reported data suggest that incidence of HCV infection among injection drug users in the United States decreased from the late 1980s through the mid 1990s and remained stable thereafter [21, 22], our data suggest that the incidence may have actually continued to decrease until 2002–2004, at least in some major metropolitan cities.

During the last study period (2002–2004), only 7% of injection drug users who reported injecting for <1 year and only 22% of those who reported injecting for 1–2 years were HCV antibody positive. These results are considerably lower than the prevalence of HCV antibody among injection drug users documented in the mid 1980s, when >50% of injection drug users were found to become infected within the first 6 months after injecting [2] and are lower than studies [5–9] from the 1990s that reported that 18%–38% of individuals injecting for <3 years were HCV antibody positive.

Despite overall lower prevalence of HCV antibody, our results were consistent with previous studies that have shown that prevalence of HCV antibody increases with age, years injecting, and intensity of injection drug use [1–5]. Although 1 study has reported that injection drug users who have been injecting for >5 years continued to be at a high risk for HCV infection [14], it has been more commonly reported [4, 5, 8, 9, 15] that injection drug users face higher rates of infection at initiation of injection drug use and that HCV incidence rates subsequently decrease. The present data, although cross-sectional, support that understanding, finding sharply higher odds of HCV antibody prevalence in the first 2 years of injection drug use and lower subsequent rates of increase in those odds.

Our data were also consistent with previous studies [6, 13, 23] that found, even after adjustment for multiple characteristics, racial and geographic differences in prevalence of HCV antibody. The reasons for these differences are unknown. They may represent regional differences in demographic factors (such as mobility of injection drug users), injecting practices (including the size and characteristics of injection drug user social networks and safer injection practices), or the intensity and success of interventions targeting injection drug users. Recent studies have indicated sharply decreased rates of injection drug use among non-Hispanic blacks [24, 25].

Our results support the idea of a “window of opportunity” for interventions to reach new injection drug users to prevent HCV infection [7, 26]. However, with >1 in 5 injection drug users infected with HCV within the first 2 years after initiation of injection drug use, this window is narrow, and there is a clear need to aggressively provide information on prevention of HCV infection and services to both injection drug users and non-injection drug users who are at risk of initiating injection. Although the focus of this research was on injection drug use characteristics, other research has documented the links between HCV infection and sexual violence, commercial sex, and unstable housing [27]. Although access to sterile injection equipment is a central component to reducing transmission of HCV, the contributions of these other factors to HCV vulnerability should not be ignored.

This study had several limitations. Although CIDUS I, CIDUS II, and CIDUS III had similar recruitment strategies and eligibility requirements, participants differed with respect to demographic and drug-use characteristics at individual sites across the 3 study periods. Although we have adjusted for these differences by using multivariate methods, it is possible that not all the potentially confounding factors were accounted for. For example, our experience suggests that, in chain-referral samples, the likelihood that a young injection drug user will be connected to an older injection drug user network is greater when injection drug users of all ages are sampled than when only young injection drug users are sampled, and individuals from different age ranges were recruited at different sites and study periods. Studies that recruit individuals from a wider range of ages, such as CIDUS I, are more likely to enroll young injection drug users referred by older injection drug users (who may be direct or indirect injection partners) and are less likely to find or enroll young injection drug users who only associate with other young injection drug users. Because HCV prevalence increases with injection duration and age is a strong proxy for injection duration, connections with older injection drug users, even at equivalent levels of risk behaviors or time since initiation of injection drug use, is an important factor in the risk of HCV infection in a young injection drug user. Estimation of the incidence of HCV infection among injection drug users with the use of serial cross-sectional studies has some inherent limitations. Because drug use can be discontinuous and drug users have high mortality rates, study participants cannot be considered as a cohort across the study period. Although prevalence by duration of injection is a proxy for incidence, true incidence might be different.

The epidemiology of HCV infection among injection drug users has changed markedly during the past 2 decades in the United States. Although 1 in 5 injection drug users is infected within the first 2 years after starting to inject drugs, this rate is considerably lower than that observed a decade ago and indicates that a window of opportunity exists to prevent HCV infection among injection drug users. Our data also indicate that there are regional differences in the epidemiology of HCV infection in the United States. An understanding of local trends in HCV infection is important for geographically tailoring strategies to target primary and secondary prevention activities.

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Acknowledgments

Financial support. Centers for Disease Control and Prevention.

Potential conflicts of interest. All authors: no conflicts.

  • Received October 1, 2007.
  • Accepted February 9, 2008.
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  1. Clin Infect Dis. (2008) 46 (12): 1852-1858. doi: 10.1086/588297
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