IJE Advance Access originally published online on March 31, 2005
International Journal of Epidemiology 2005 34(3):593-599; doi:10.1093/ije/dyi059
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Article |
Seroprevalence of hepatitis C virus and associated risk behaviours: a population-based study in San Juan, Puerto Rico
1 Department of Biostatistics and Epidemiology, Graduate School of Public Health, Medical Sciences Campus, University of Puerto Rico, PO Box 365067, San Juan, Puerto Rico 00936-5067
2 Department of Medicine, School of Medicine, Medical Sciences Campus, University of Puerto Rico, PO Box 365067, San Juan, Puerto Rico 00936-5067
* Corresponding author. Department of Biostatistics and Epidemiology, Graduate School of Public Health, PO Box 365067, San Juan, Puerto Rico 00936-5067. E-mail: cperez{at}rcm.upr.edu
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Abstract |
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Background Limited information about the epidemiology of hepatitis C virus (HCV) infection is available in Puerto Rico, one of the areas hardest hit by the human immunodeficiency virus/acquired immune deficiency syndrome (HIV/AIDS) epidemic. We estimated the prevalence of HCV infection and identified correlates of seropositivity in the municipality of San Juan, Puerto Rico.
Methods A probability cluster design was employed to select a sample of households representative of the population aged 21–64 years in San Juan during 2001–2002. All 964 subjects completed a face-to-face interview to gather data on demographics and self-reported risk behaviours followed by venipuncture for HCV antibody testing. Variables that were at least marginally associated with HCV seroprevalence (P < 0.10) in the bivariate analyses were considered for inclusion into the multiple logistic regression model to estimate the adjusted prevalence odds ratio (POR).
Results Overall weighted prevalence of HCV infection was 6.3% (95% CI 3.6–10.9%). A significant (P < 0.05) higher prevalence was observed among subjects with the following characteristics: age 30–49 (9.5%), male sex (10.6%), 
12 years of education (9.6%), no health coverage (12.6%), lifetime heroin use (39.2%), lifetime cocaine use (39.6%), tattooing practices (34.2%), history of imprisonment (32.8%), and self-reported histories of hepatitis B virus infection (30.4%) and HIV/AIDS (92.1%). Multivariate logistic regression revealed that tattooing practices (POR = 8.9; 95% CI 1.7–44.7), lifetime cocaine use (POR = 5.5; 95% CI 2.2–13.5), blood transfusions prior to 1992 (POR = 4.0; 95% CI 1.6–10.1), lifetime heroin use (POR = 3.3; 95% CI 1.4–7.8), and history of imprisonment (POR = 2.3; 95% CI 1.1–4.9) remained significantly associated with HCV seropositivity.
Conclusions The large prevalence of HCV infection observed in Puerto Rican adults residing in San Juan suggest that HCV infection is an emerging public health concern and merits further investigation.
Keywords Hepatitis C, epidemiology, prevalence, risk behaviours, Puerto Rico, Hispanics
Accepted 15 February 2005
Studies investigating the seroprevalence of hepatitis C virus (HCV) have been carried out in diverse populations, showing an estimated worldwide prevalence of 3% and a marked geographical variation.1,2 According to a large-scale epidemiologic survey of the non-institutionalized, civilian population aged 
6 years in the US, 1.8% or 3.9 million persons have been infected with HCV.3 Serologic surveys conducted in Puerto Rico have been limited to blood donors, haemodialysis patients, and women attending publicly funded prenatal clinics in San Juan, reporting HCV prevalence estimates within values found for the US population.4–6 However, the prevalence of HCV infection among 11 530 inmates in the island (78% of the correctional population) who consented to HCV testing in 1998 was 49.3%,7 a higher estimate than that found in other correctional facilities in the US and the UK.8–11
One would expect a higher prevalence of HCV infection in settings where rates of AIDS and risk behaviours are high. Puerto Rico has been disproportionately affected by the human immunodeficiency virus/acquired immune deficiency syndrome (HIV/AIDS) epidemic, ranking fourth in the incidence rate of AIDS in 2001 (32.3 per 100 000 population) among all US states and territories, with injecting drug use as the main route of exposure.12,13 Adults and adolescents of both sexes in Puerto Rico had the third and the sixth largest AIDS rate per 100 000 inhabitants (65.4 and 21.1, respectively) in 2001 among all US states and territories.12 San Juan continues to be one of the hardest hit regions, ranking eighth among large metropolitan areas (with 500 000 or more population) in the US, with an AIDS rate of 35.3 per 100 000 population during 2001.12 A study that compared Puerto Rican drug users residing in New York City with drug users residing in Puerto Rico found a higher HIV seroconversion rate among those residing in Puerto Rico (0.9 per 100 person-years and 3.4 per 100 person-years, respectively), suggesting a higher prevalence of risk behaviours in Puerto Rico than in the US.14 Limited information about the epidemiology of HCV infection is available in Puerto Rico; therefore, the present study estimated the seroprevalence of HCV infection and identified correlates of seropositivity in the adult population of San Juan, Puerto Rico.
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Materials and methods |
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Sample
A community-based study of the non-institutionalized population aged 21–64 years residing in the municipality of San Juan was conducted during 2001–2002 using a three-stage cluster design. In the first stage, a systematic selection of census block groups sorted by median age and household value, according to the Census 2000, was made with a probability proportional to the number of occupied households in the census block group. The second stage consisted of a random selection of one block within each selected census block group. In the third stage, a segment of 15 consecutive households was randomly selected from each block, and all eligible adults in this segment were invited to participate in the study.
Data collection
After obtaining written informed consent, all subjects completed a structured face-to-face interview followed by venipuncture for HCV antibody testing. Participants received a small economic incentive, educational material on hepatitis C, and test results. The questionnaire covered demographics, drug use and sexual risk practices measured over the lifetime, tattooing practices, body piercing, history of blood transfusions, imprisonment history, health-related occupations, and self-reported histories of hepatitis B virus (HBV) infection and HIV/AIDS. The Institutional Review Board at the University of Puerto Rico Medical Sciences Campus approved the study protocol.
Laboratory analysis
Blood specimens were collected from participants by certified phlebotomists and shipped to a local reference laboratory accredited by the Clinical Laboratory Improvement Amendments Program. Serum samples were tested for the HCV antibody by means of a third generation enzyme-linked immunosorbent assay following the manufacturer's specifications (Ortho® HCV EIA 3.0, Ortho-Clinical Diagnostics, Inc., Raritan, NJ). Samples that were repeatedly reactive on initial testing were subjected to supplemental testing via a third generation recombinant immunoblot assay following the manufacturer's specifications (Chiron® RIBA HCV 3.0 SIA, Chiron Corporation, Emeryville, CA). Samples that were reactive on both assays were classified as positive for the HCV antibody. Samples that were negative on EIA and those that were positive on EIA but negative on RIBA were both considered negative. Samples that were reactive on EIA and indeterminate on RIBA were classified as indeterminate. Individuals who tested positive or indeterminate for hepatitis C were counselled and referred for immediate follow-up medical evaluation.
Statistical analysis
Overall and subgroup-specific HCV antibody prevalences were estimated, and differences between subgroups were assessed using the Wald test statistic.15 To evaluate the association between high-risk behaviours and HCV infection, unadjusted prevalence odds ratios (POR) were computed. High-risk behaviours were considered for inclusion into the multiple logistic regression model to estimate the adjusted POR based on the following criteria: variables at least marginally associated (P < 0.10) with HCV seroprevalence and having an adequate number of seropositive individuals (ni > 10) in each variable category. All possible first-order interactions were assessed in the model. All unadjusted and adjusted parameters were estimated using generalized estimating equations method to control for the adjusted intra-class correlation (
) between subjects of the same household or subjects selected from the same segment.15 A robust variance estimator was used to determine the standard errors of the logistic regression parameters.15 In order to take into account the number of participants in each block (ni) and the number of adults aged 21–64 years old in the block (Ni), a weighting factor [wi = Ni/ni] was included in the logistic regression model. Extension of the Hosmer and Lemeshow goodness-of-fit test statistic indicated no evidence of lack-of-fit of the model to the data (P > 0.10).15 Data management and all statistical analyses were performed using the statistical package Stata (Version 8.0, College Station, TX, USA).
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Results |
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A total of 970 adults participated in the face-to-face interview and provided blood samples suitable for hepatitis C testing, attaining an overall response rate of 85.7%. The distribution of sex (female:male ratio is 1.28) and age group (20–29 years: 25.3%; 30–49 years: 45.1%; 50–64 years: 26.6%) was similar to that of the adult population of San Juan according to the Census 2000 (Table 1). Nearly 19% of the participants did not report health coverage at the time of the interview. Of the sample, <10% reported lifetime heroin (6.2%) and cocaine (8.0%) use, 12.4% reported tattooing practices, 50.1% reported first sexual intercourse before age 18, and 61.6% reported two or more sexual partners over their lifetime. Blood transfusions prior to 1992 were reported by only 5%, 9.6% reported ever working in health-related occupations, 9.7% reported a history of imprisonment, and 25.9% reported a history of ear or other body piercing. Of the sample, <1% self-reported a history of HBV infection (0.8%) and HIV/AIDS (0.6%).
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Of the adults, 59 (6.1%) were positive to HCV infection, 905 (93.3%) were negative, and six (0.6%) were indeterminate. Participants with indeterminate results were excluded from further analyses. Overall weighted prevalence of HCV infection was 6.3% (95% CI 3.6–10.9%). Among the 59 seropositive individuals, 55 (93.2%) were unaware of their infection status, and only two (3.4%) did not report potential exposures to HCV.
HCV seroprevalence was significantly higher (P < 0.05) for subjects with the following characteristics: age 30–49 (9.5%), male sex (10.6%), <12 years of education (9.6%), no health coverage (12.6%), lifetime heroin use (39.2%), lifetime cocaine use (39.6%), tattooing practices (34.2%), history of imprisonment (32.8%), and self-reported histories of HBV infection (30.4%) and HIV/AIDS (92.1%) (Table 2). Individuals who reported first sexual intercourse before age 18, two or more sexual partners over their lifetime, and blood transfusions prior to 1992 had a marginally (0.05 P < 0.10) higher seroprevalence of HCV. Those who ever worked in a health-related occupation or had a history of ear or other body piercing had a similar seroprevalence of HCV compared with individuals without such a history (P > 0.10).
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The following variables were significantly associated with HCV seropositivity in bivariate analysis: lifetime heroin use (POR = 18.4; 95% CI 8.5–40.2), lifetime cocaine use (POR = 19.1; 95% CI 11.7–31.3), tattooing practices (POR = 13.7; 95% CI 5.7–32.8), and history of imprisonment (POR = 13.6; 95% CI 8.7–21.3) (Table 3). Lifetime number of sexual partners (POR = 2.9; 95% CI 0.9–2.8), age at first sexual intercourse (POR = 3.1; 95% CI 1.0–9.4), and blood transfusions prior to 1992 (POR = 2.2; 95% CI 0.9–5.8) were marginally associated with HCV seropositivity. Ear or other body piercing (POR = 0.6; 95% CI 0.2–2.2) and ever worked in a health-related occupation (POR = 1.4; 95% CI 0.3–7.4) were not significantly associated with HCV seropositivity. In the multivariate analysis, tattooing practices (POR = 8.9; 95% CI 1.7–44.7), lifetime cocaine use (POR = 5.5; 95% CI 2.2–13.5), blood transfusions prior to 1992 (POR = 4.0; 95% CI 1.6–10.1), lifetime heroin use (POR = 3.3; 95% CI 1.4–7.8), and history of imprisonment (POR = 2.3; 95% CI 1.1–4.9) remained significantly associated with HCV seropositivity.
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Of our 59 seropositive participants, 49 (83.1%) reported at least one of these significant exposures for HCV: lifetime cocaine (29) or heroin use (28), tattooing practices (29), history of imprisonment (30), and blood transfusions prior to 1992 (8).
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Discussion |
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This is the first epidemiological study that assessed the seroprevalence of HCV among adults randomly selected from the municipality of San Juan, Puerto Rico. Our data reveal a higher prevalence of HCV infection in San Juan compared with estimates obtained from other metropolitan areas.16–18 Community-based studies conducted in Spain, France, and northern Italy have reported prevalences ranging from 1.2 to 3.3%. The higher prevalence in San Juan might be partially explained by a consistently higher frequency of drug injection (4–8 times daily) among Puerto Rican injection drug users than among other groups of injection drug users in the US, often in settings in which sterile injecting equipment and cleaning materials are scarce.19–21 Further support for this idea is provided by other studies showing that drug injectors in Puerto Rico are less likely to enter and complete drug treatment programmes, to use methadone maintenance treatment centres, and have less access to syringe exchange programmes than their counterparts in New York City.22,23
In spite of the evidence supporting the role of drug treatment in HIV prevention and recommendations of the NIH Consensus Statement on Management of Hepatitis C to institute measures to reduce transmission of HCV among injection drug users,24 a recent study of availability of drug treatment services in Puerto Rico revealed a 34.7% reduction in total treatment capacity from 1998 to 2002, even though the need for treatment had not decreased.25 The scarcity of preventive options in Puerto Rico regarding HIV/AIDS and drug abuse is likely to increase the burden of hepatitis C substantially in the future, unless effective prevention and treatment strategies among injecting drug users are implemented promptly.
Not surprisingly, a history of drug use was strongly associated with HCV seropositivity and is consistent with previous reports.1,2,8–11,16–18,24,26 We did not directly measure drug injecting practices. Thus, the associations of heroin and cocaine use with HCV seropositivity found in our study are likely to be surrogate markers for injecting drug use practices. HCV seropositivity was associated with tattooing practices, a finding consistent with the results of a community-based seroepidemiological survey of hepatitis C in Catalonia, Spain that found that tattoos were significantly associated with infection.16 Although previous reports have found significant associations between tattooing and HCV infection in highly selected populations, it is not known if these results can be inferred to the general population.27,28 Tattooing in prison is emerging as a potential risk factor for HCV infection.29,30 Although we did not ask participants if their tattooing practices occurred in prison, Reyes and colleagues studied 400 street-recruited injection drug users in San Juan, Puerto Rico and found that body piercing or tattooing in prison (POR = 4.1; 95% CI 1.5–10.9) was the most important risk factor associated with HCV infection.30
History of imprisonment was also associated with HCV seropositivity. This finding is consistent with other studies that have found that prisons are places where drug users, who continue to inject, are at high risk of HIV, HBV, and HCV infections.8–11 The Centers for Disease Control and Prevention have published new guidelines for prevention and control of infections with hepatitis viruses in correctional settings including an integrated health education and risk reduction programmes for hepatitis A, hepatitis B, and hepatitis C.8 Further research is needed to determine the extent to which these types of exposures and the settings in which they occur increase the risk of HCV infection. Exposure to blood transfusions prior to 1992 was also associated with HCV seropositivity, a well-established risk factor that has been documented in early studies of HCV prevalence among transfusion recipients.31,32
Evidence for transmission of HCV through sexual risk practices has been controversial. The role of sexual activity has been evaluated in diverse populations, and prevalence appears to be high for individuals at high risk for sexually transmitted infections and low for monogamous heterosexual couples.33 After adjusting for demographics and other high-risk behaviours, the present study did not find that HCV seropositivity was significantly associated with lifetime number of sexual partners or early age at first sexual intercourse. This observation is consistent with other studies, including those that have performed virological analyses that suggest that the risk of sexual transmission of HCV within heterosexual monogamous couples is extremely low or even null.34,35 Although a history of multiple sexual partners may indicate non-disclosure of injecting drug use or a marker for other potential exposures for HCV infection, further research into the role of sexual risk practices is required. These studies must include detailed virological analyses of antibody-concordant and genotype-concordant sexual partners.35
Our study found a high prevalence of HCV infection among individuals who self-reported HBV infection and HIV/AIDS. The high HCV seroprevalence observed, especially among individuals who self-reported HIV/AIDS, might probably be attributed to the fact that they all reported lifetime heroin or cocaine use and history of imprisonment, possible surrogate markers of injecting drug use. If drug users or individuals with a history of imprisonment are more likely to have been tested for HIV and HBV, misclassification due to differential history of testing may lead to overestimation of the association with HCV infection and partly explain these findings. Although we did not document HBV infection and HIV/AIDS by laboratory evidence, the finding is consistent with observations from other studies that have shown that an estimated 50–90% of the persons who acquired HIV infection from injecting drug use already have hepatitis C.36
Caution must be exercised in interpreting our results as generalizable to the adult population of San Juan since we excluded incarcerated and homeless individuals, who have been found to have high rates of HCV infection.8–11,37,38 Second, the cross-sectional nature of the investigation limits our ability to attribute a temporal relation between high-risk behaviours and prevalent HCV infection. Third, drug use, sexual behaviours, and HIV and HBV serostatus were self-reported and therefore potentially subject to measurement error. Although no toxicological tests were performed to detect cocaine, opiates, or other residues as validation methods of the self-reported information on drug use patterns, the available evidence about the validity of drug use self-reports in Puerto Rico suggests that the extent of under-reporting in personal interviews is similar to that found in studies conducted in the US.39
Notwithstanding these limitations, the high incidence of AIDS in Puerto Rico, the large prevalence of HCV infection observed in the inmate population and in adults residing in the municipality of San Juan, and the large group of infected individuals unaware of their HCV serostatus suggests that hepatitis C is an emerging public health concern and merits further investigation. A national serologic survey in Puerto Rico aimed at examining geographical differences in seroprevalence of HCV infection and assessing detailed high-risk behaviours and patterns of co-infections that might promote transmission will be underway to assess the public health impact of this infection. This study will contribute to provide a broader picture of the relative need for hepatitis C management, to define targets for intervention, and to define public health strategies for Puerto Rican adults who reside in the island.
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Disclosure of potential conflict of interest |
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The sponsors did not have any role in the study conception and design, data collection, data analysis and interpretation, writing and critical review of the report, and submission for publication to the International Journal of Epidemiology. Moreover, the authors have not received nor do they anticipate receiving any benefit in connection with this work.
KEY MESSAGES
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Acknowledgments |
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The authors are grateful to the subjects for their participation in this study and the registered nurses for conducting the face-to-face interviews and venipuncture procedures. The authors wish to acknowledge Dr Héctor Colón for his helpful suggestions on the manuscript. This project was supported by a grant from the Division of Medical Affairs of Schering-Plough del Caribe, Inc.
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References |
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