Variability in the Incidence of Human Immunodeficiency Virus, Hepatitis B Virus, and Hepatitis C Virus Infection among Young Injecting Drug Users in New York City

Don C. Des Jarlais1,2,, Theresa Diaz3, Theresa Perlis2, David Vlahov3, Carey Maslow2, Mary Latka3, Russell Rockwell2, Vincent Edwards3, Samuel R. Friedman2, Edgar Monterroso4, Ian Williams4 and Richard S. Garfein4

1 Baron Edmond de Rothschild Chemical Dependency Institute, Beth Israel Medical Center, New York, NY.
2 National Development and Research Institutes, Center for AIDS Research, New York, NY.
3 New York Academy of Medicine, Center for Urban Epidemiologic Studies, New York, NY.
4 Thailand–United States Collaboration, Centers for Disease Control and Prevention, Atlanta, GA.

Received for publication July 17, 2001; accepted for publication September 24, 2002.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Cohort studies of young (aged 18–30 years) injecting drug users recruited in 1997–1999 in the Harlem and Lower East Side areas of New York City, New York, were used to assess the incidence of human immunodeficiency virus (HIV), hepatitis B virus (HBV), and hepatitis C virus (HCV). The authors found that HIV incidence was low at both sites: 0.8/100 person-years at the Harlem site and 0/100 person-years at the Lower East Side site. In contrast, HBV incidence was moderate (12.2/100 person-years) at the Harlem site and high (30.7/100 person-years) at the Lower East Side site. Similarly, HCV incidence was moderate (9.3/100 person-years) at the Harlem site and high (34.0/100 person-years) at the Lower East Side site. Results show that high rates of HBV and HCV transmission do not imply high rates of HIV transmission, even within an area of high HIV seroprevalence.

cohort studies; hepatitis B virus; hepatitis C-like viruses; HIV; injections, intravenous; substance-related disorders

Abbreviations: Abbreviations: HBV, hepatitis B virus; HCV, hepatitis C virus; HIV, human immunodeficiency virus.


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Injecting drug users are at high risk of infection with blood-borne viruses such as human immunodeficiency virus (HIV), hepatitis B virus (HBV), and hepatitis C virus (HCV) (1, 2). The microtransfusions that occur when two or more persons inject with the same needle and syringe are an efficient method of transmitting these blood-borne viruses, and unprotected sexual activities are important in transmitting HIV and HBV (3, 4). The broad similarities in transmission of HIV, HBV, and HCV have led to suggestions that HBV and HCV should be used as outcome measures for evaluating programs to prevent HIV infection among injecting drug users (5).

There are also important differences with respect to the transmission dynamics of these three viruses in populations of injecting drug users. HBV and HCV are more environmentally stable and more readily transmitted than HIV (6). The prevalence of persons chronically infected with HCV is often much higher than the prevalence of persons infected with HIV in populations of injecting drug users. Incidence rates are also typically much higher for HBV and HCV infection than for HIV infection. The incidence of HCV infection can be extremely high among persons who have recently begun injecting drugs, with estimated rates of from 32 to more than 70 per 100 person-years at risk (7, 8).

We report here on the incidence of HIV, HBV, and HCV infection in two cohorts of young drug injectors from New York City, New York. We found substantial variability in incidence, both among the viruses and across the two study sites.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Study framework
Subjects were recruited during 1997–1999 as part of the Centers for Disease Control and Prevention (Atlanta, Georgia) Second Collaborative Injection Drug Users Studies (CIDUS II). Two New York City sites were included in these studies: one located in the Lower East Side (conducted by Beth Israel Medical Center and the National Development and Research Institutes) and one in central and east Harlem (conducted by the Center for Urban Epidemiologic Studies, New York Academy of Medicine). Eligibility criteria and the core questionnaire were the same for both sites, and community-based recruiting was used at both sites.

Eligibility
Study participants were persons between the ages of 18 and 30 years who reported injecting drugs during the previous 6 months. Questions to assess eligibility were asked within a series of unrelated questions (e.g., Do you have siblings?). The eligibility criteria were not advertised, because knowledge of these criteria might have led persons to falsely represent themselves in order to enter the study.

Sites
The Harlem study, known as Harlem Outreach Prevention and Education (HOPE), was conducted from a building in central Harlem. Recruitment took place in both central (predominantly African American) and east (predominantly Latino/Latina) Harlem.

For the Lower East Side, the study was conducted in a research storefront office in that neighborhood. The storefront has been in continuous operation since 1989 and is well known among drug users in the community. The Lower East Side is an ethnically diverse neighborhood with a large transient population of young White persons from the rest of the United States.

Recruitment procedures
Ethnographic interviews, health and law enforcement statistics, and direct observation were used to map central and east Harlem and the Lower East Side to determine specific areas in which young drug injectors congregated. Recruiters then approached young persons in these areas, engaged them in conversation, and formally assessed eligibility by asking structured questions, inviting those who were eligible to participate in the study. Persons who agreed to participate were escorted to the study office to receive information about the study and to provide informed consent. After completing an interview, they were given a small honorarium ($25) for their time and travel.

Data collection
At baseline and at 6 and 12 months postbaseline, eligible and consenting participants underwent standardized face-to-face interviews conducted by trained interviewers in private rooms. Participants received pretest counseling for HIV, HBV, and HCV infection, and serum samples were collected. After data collection, participants were given risk-reduction counseling and referral information for services such as drug treatment and social services. At post-test counseling (approximately 2–4 weeks after the interviews), participants whose test results were positive were offered referrals for follow-up medical evaluation. Those without evidence of HBV infection were offered referral for hepatitis B vaccination.

The study received institutional review board approval from Beth Israel Medical Center, the National Development and Research Institutes, the New York City Department of Health, and the Centers for Disease Control and Prevention.

Interviews
The interview included questions on sociodemographics, injecting behaviors, risk networks, and sexual behaviors. Most drug use and sexual behavior questions focused on the 6 months prior to the baseline interview, and then on the periods between successive interviews.

Laboratory analyses
Serum from blood specimens was analyzed for HIV-1 antibodies by using standard techniques at local laboratories. Specimens repeatedly reactive on enzyme-linked immunosorbent assay were confirmed with Western blot.

Blood specimens were sent to the Centers for Disease Control and Prevention for testing for serologic markers of HBV and HCV infection. Samples were tested for antibody to HBV core antigen (CORAB; Abbott Laboratories, Chicago, Illinois) and antibody to HCV (Abbott HCV EIA (enzyme immunoassay) 2.0; Abbott Laboratories). A sample of 100 specimens repeatedly reactive for HCV based on enzyme immunoassay received supplemental testing (EIA 2.0 and HCV MATRIX; Abbott Laboratories); all were found to be positive. Because of the high positive predictive value of repeat reactive enzyme immunoassay testing in this population, no further supplemental HCV testing was performed. Seroconversion was defined as a negative anti-HIV, anti-HCV, or antibody to HBV core antigen test at one data collection point followed by a corresponding positive anti-HIV, anti-HCV, or antibody to HBV core antigen test at the next data collection point. Time of seroconversion was estimated as the midpoint between the dates of serum collection of the last negative antibody test and the first positive antibody test.

Follow-up procedures
Follow-up visits were scheduled for 6 and 12 months after the baseline visit. Standard follow-up procedures were conducted at each site, including collecting detailed locator and contact information; maintaining telephone, mail, or in-person street contact with subjects; and providing honoraria for participation in follow-up interviews, with bonus incentives for subject-initiated appointments. For subjects who did not provide usable contact telephone numbers or addresses, recruiters conducted street searches of initial recruitment locations and typical "hangout" locations.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Table 1 presents selected sociodemographic characteristics, drug use and sexual behaviors, and baseline seroprevalence of HIV, HBV, and HCV infection among subjects recruited at the two sites. Substantial differences were found between sites concerning race/ethnicity, homelessness in the 6 months preceding the interview, and receipt of drug treatment in the previous 6 months. The Lower East Side subjects were more likely to be engaging in a variety of injection and sexual risk behaviors. The Harlem subjects were more likely to have antibodies against HIV, HBV, and HCV at baseline.


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TABLE 1. Sociodemographic characteristics, drug use and sexual risk behaviors,* and baseline seroprevalence of human immunodeficiency virus, hepatitis B virus, and hepatitis C virus among injecting drug users aged 18–30 years, Lower East Side and east Harlem, New York, 1997–1999
 
The follow-up rate for the 6-month interview was moderate for subjects from Harlem (67 percent) and low (31 percent) for subjects recruited at the Lower East Side site. Follow-up rates were lower for the 12-month interview—41 percent for Harlem and 10 percent for the Lower East Side. (A supplemental study (7) indicated that a large number of Lower East Side subjects had left the city during the follow-up period.) Additional information showed that many of the Harlem subjects were incarcerated during follow-up (T. Diaz, unpublished data).

We examined possible differences in baseline variables (those listed in table 1) between subjects for whom follow-up data were or were not available. In general, very few differences were found in baseline risk behaviors between subjects who were or were not followed up successfully. In particular, there were very few differences for the Lower East Side site, which had the lower follow-up rate (data not presented but are available from the first author).

Table 2 presents the incidence rates for HIV, HBV, and HCV infection for the two sites and for the combined sample. HIV incidence was similar at both sites and was low for areas in which HIV seroprevalence was high (approximately 30 percent among injecting drug users as a whole at each site (9) at the time of the study). At the Harlem site, the incidence of both HBV and HCV infection was approximately 10 per 100 person-years at risk, and the incidence of both HBV and HCV infection was approximately 30 per 100 person-years at risk at the Lower East Side site.


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TABLE 2. Human immunodeficiency virus, hepatitis B virus, and hepatitis C virus seroincidence rates among injecting drug users aged 18–30 years, Lower East Side and east Harlem, New York, 1997–1999
 
Given the three different blood-borne viruses, the two different sites, the variable follow-up rates across sites and across the 6- and 12-month follow-up periods, and the modest numbers of incident infections at each site, analyses of risk factors for seroconversion are not presented here.


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In this study, we found considerable variability in the incidence of HIV, HBV, and HCV infection among the young drug injectors at the two sites. The incidence rates of HIV versus HBV and HCV varied; HIV incidence was much lower than either HBV or HCV incidence. Incidence rates of HBV and HCV were significantly higher at the Lower East Side site, whereas HIV incidence was almost identical at the two sites. Note also that the difference in HBV and HCV incidence at the two sites was in the opposite direction of the baseline prevalences for these two viruses (table 1).

The incidence of HIV among these young injecting drug users at both sites is consistent with that found in other recent HIV incidence studies from New York City. A meta-analysis of 12 studies that included 6,000 person-years at risk found a weighted average incidence of 0.7 per 100 person-years at risk (10)—similar to the incidence rates of 0 per 100 person-years and 0.8 per 100 person-years found in the two samples of young injectors in this study. Indeed, given the other recent HIV incidence studies (10) among injecting drug users in New York, a high HIV incidence rate at either site would be unexpected and would require special explanation.

Low HIV incidence and moderate-to-high HCV/HBV incidence has been reported in studies from other areas, for example, those by van Beek et al. and Hagen et al. (8, 12). To the best of our knowledge, however, these other studies showing a low HIV and a high HCV/HBV incidence among injecting drug users were conducted in geographic areas in which the HIV prevalence was very low. The low prevalence of HIV may be a sufficient explanation for the differences in HIV versus HBV/HCV incidence in these other areas. However, this explanation would not apply to the New York City data reported here, because HIV prevalence in both the Harlem and Lower East Side areas was approximately 30 percent when the data were collected (10).

These follow-up samples can be considered convenience subsamples of the original convenience samples from the cohorts. Thus, these incidence rates should not be generalized to other young drug injectors in New York City, nor necessarily even to other young drug injectors from the two neighborhoods. However, our results do demonstrate that considerable variability can occur in the incidence rates of the three viruses in different groups of injecting drug users.

These data raise the question of how so many of the follow-up subjects became infected with HBV and HCV without becoming infected with HIV. As shown in table 2, among the follow-up subjects, there were 32 incident HBV infections and 25 incident HCV infections but only one incident HIV infection. We suggest two possible mechanisms for the differences between HBV and HCV versus HIV incidence. First, recent studies suggest that HBV and/or HCV frequently may be transmitted by sharing drug preparation equipment (cottons, cookers, rinse water) (11, 12), while it does not appear that HIV is often transmitted by sharing such drug preparation equipment. In the baseline data for this study, prevalent HCV infection was associated with the sharing of drug preparation equipment (13). Thus, HBV and HCV but not HIV may have been transmitted because young drug injectors in New York shared drug preparation equipment.

Second, the great majority of injecting drug users in New York have been tested for HIV, and injecting drug users who know that they are HIV seropositive are much less likely to pass on used needles and syringes compared with injecting drug users who know that they are HIV seronegative (Des Jarlais et al., unpublished manuscript). We doubt whether most injecting drug users in New York know 1) whether they are infected with and are capable of transmitting HBV and/or HCV infection and 2) the possible outcomes of chronic HBV and HCV infection; and whether those who know that they are capable of transmitting HBV and HCV are substantially reducing their transmission behaviors (passing on used needles and syringes).

There are two implications of the variability in the incidence of HIV, HBV, and HCV in these two groups of new drug injectors in New York. First, great caution is needed before either HBV incidence or HCV incidence is used as an outcome measure to assess HIV prevention programs. High HBV or high HCV incidence need not imply high HIV incidence and may not even imply a potential for high HIV incidence (although we think that low HBV/HCV incidence probably does imply low HIV incidence).

Second, it is likely that new methods of preventing HBV and HCV transmission among injecting drug users are needed. Vaccinating drug users against HBV is likely to be the most effective way to prevent HBV infection, but, at present, efforts to vaccinate drug users for HBV in the United States and many other countries are clearly inadequate. Reducing HCV transmission may be quite difficult. It is likely that further reductions in the sharing of both needles and syringes and of drug preparation equipment will be needed. We suggest that new efforts to reduce HCV transmission among injecting drug users should be developed in consultation with the injecting drug users themselves.

Reducing HIV, HBV, and HCV transmission among injecting drug users is an important public health goal. Clearly, additional research is needed on the transmission dynamics of HIV, HBV, and HCV in this population. Although there are broad similarities in how these three viruses are transmitted, important differences in the design and evaluation of programs may be needed to achieve this goal.


    NOTES
 
Correspondence to Dr. Don C. Des Jarlais, Baron Edmond de Rothschild Chemical Dependency Institute, Beth Israel Medical Center, 1st Avenue and East 16th Street, New York, NY 10003 (e-mail: dcdesjarla{at}aol.com). Back


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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  9. Des Jarlais DC, Perlis T, Friedman SR, et al. Declining seroprevalence in a very large HIV epidemic: injecting drug users in New York City, 1991–1996. Am J Public Health 1998;88:1801–6.[Abstract]
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