JAIDS Journal of Acquired Immune Deficiency Syndromes:
Epidemiology and Social Science
Trends in Hepatitis C Virus Infection Among Patients in the HIV Outpatient Study, 1996–2007
Spradling, Philip R MD*; Richardson, James T MPH†; Buchacz, Kate PhD‡; Moorman, Anne C BSN, MPH‡; Finelli, Lyn DrPH, MS*; Bell, Beth P MD, MPH*; Brooks, John T MD‡; and the HIV Outpatient Study Investigators1
From the *Division of Viral Hepatitis, National Center for HIV, Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention, Atlanta, GA; †Cerner Corporation, Vienna, VA; and ‡Division of HIV/AIDS Prevention, National Center for HIV, Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention, Atlanta, GA.
Received for publication March 2, 2009; accepted June 30, 2009.
Supported by Contract 200-2001-00133 and 200-2006-2879-Centers for Disease Control and Prevention.
Prevalence of hepatitis C (HCV) infection in the HIV Outpatient Study (HOPS), 1996-2005: More Testing, Less Prevalence (abstract 905). Presented at the 45th Annual Meeting of the Infectious Diseases Society of America, October 4-7, 2007, San Diego, CA.
Conflicts of interest: none.
The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.
The investigation followed the guidelines of the US Department of Health and Human Services regarding protection of human subjects. The study protocol was approved and renewed annually by each participating institutions' ethical review board. All study participants provided written informed consent.
1The HOPS Investigators are listed in the Appendix.
Correspondence to: Philip R. Spradling, MD, Division of Viral Hepatitis, National Center for HIV, Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention, Mailstop G37, 1600 Clifton Road, NE, Atlanta, GA 30333 (e-mail: email@example.com).
Background: Coinfection with hepatitis C virus (HCV) contributes increasingly to the morbidity and mortality of persons infected with HIV. We assessed HCV infection screening practices and determined trends in the prevalence of HCV infection in the HIV Outpatient Study (HOPS) from 1996 to 2007.
Methods: We calculated the proportion of patients eligible to be tested for HCV infection (i.e., never tested or previously tested negative) and the prevalence of HCV infection annually from 1996 to 2007 by sociodemographic, clinical, and HIV risk category characteristics. We used multiple logistic regression analyses to evaluate factors independently associated with HCV testing.
Results: A total of 7618 patients were active in the HOPS from 1996 through 2007. The proportion of eligible patients tested for HCV infection increased from 10.7% in 1996 to 76.6% in 2007 and increased among all demographic and risk groups. Overall HCV prevalence decreased from 36.7% in 1996 to 19.7% in 2007; decreases in prevalence occurred among all groups except for injection drug users (IDUs). In multivariable analysis, age older than 35 years, nonwhite race, Hispanic ethnicity, high-risk heterosexual and IDU risk categories, and at least 3 years of enrollment in the HOPS were associated with increased odds of having been tested for HCV infection.
Conclusions: Screening for HCV infection in the HOPS has improved, although a sizable fraction of patients remain unscreened. The decline in overall HCV infection prevalence from 1996 to 2007 resulted primarily from a decline in the fraction of all prevalent infections in the cohort attributable to IDU patients.
Chronic liver disease caused by hepatitis C virus (HCV) coinfection contributes increasingly to the morbidity and mortality of persons infected with HIV.1-11 Based on large serosurveys and on mathematical modeling, the prevalence of chronic HCV infection in the general population has stabilized and is expected to decline over the ensuing decades.12-16 It is unclear, however, whether such a trend is occurring in the HCV/HIV-coinfected population. Many surveys of HCV/HIV-coinfected persons have had limited generalizability: they have provided point prevalence estimates from cohorts enriched in unique and differing patient groups [e.g., injection drug users (IDUs), hemophiliacs, urban surgical patients, pregnant women, active military personnel, and veterans]17-26 and were usually conducted in a single city, region, or clinic. The few studies from geographically diverse and nationally representative cohorts have reported cross-sectional data.27,28
The objective of this analysis was to determine trends in the prevalence of HCV infection from 1996 to 2007-for the period and by year-in the HIV Outpatient Study (HOPS), a multisite, heterogeneous prospective cohort of HIV-infected patients in the United States with long-term outpatient follow-up, approximately 50-60% of whom are men who have sex with men (MSM). Although data collected in the HOPS are not population based, patients under care in the HOPS are followed in several urban HIV clinics around the country and constitute a mixture of persons with various demographic and risk characteristics. We also sought to assess HCV infection screening practices in the HOPS over this period and how they may have been affected by the release of US Public Health Service guidelines recommending HCV infection screening for HIV-infected persons in 1999.
The HIV Outpatient Study
The HOPS is an ongoing, prospective observational cohort study of HIV-infected adults receiving care at 10 participating public and private HIV clinics in 8 US cities (Chicago, IL; Denver, CO; Long Island, NY; Oakland and San Leandro, CA; Philadelphia, PA; Tampa, FL; and Washington, DC) since 1993.29,30 The HOPS is an open cohort: patients may enter the study at any point after a diagnosis of HIV infection, irrespective of treatment history, and may leave the study at any point for a variety of reasons (e.g., patient request, death, and lost to follow-up). Patient data, including sociodemographic characteristics, diagnoses, treatments, and laboratory values, are abstracted from medical charts and entered into an electronic database (Clinical Practice Analyst; Cerner Corporation, Vienna, VA) by trained staff. These data are reviewed for quality and analyzed centrally. Through 2007, the HOPS has collected sociodemographic and clinical data abstracted from medical charts of over 8500 patients at over 305,000 clinical encounters. The ethical conduct of the study undergoes annual review by the institutional review boards of the Centers for Disease Control and Prevention (Atlanta, GA) and each local site. Appropriate informed consent was obtained from all participants. The US Department of Health and Human Services' guidelines for human experimentation were followed in the conduct of this clinical research.
Selection of Persons for Analysis
All patients enrolled in the HOPS for any period of time between January 1, 1996, and December 31, 2007, were eligible for analysis. For a particular year, a patient was considered active and was included in the analysis if that patient had at least 1 HOPS-related clinic visit in that calendar year. For the period 1996-2007, patients were included in the analysis if they had at least 1 HOPS-related clinic visit during that entire interval, irrespective of the year in which it occurred.
Calculation of Prevalence of HCV Infection
Patients were classified as having HCV infection based on the 2005 Centers for Disease Control and Prevention/Council of State and Territorial Epidemiologists case definition of “past or present” HCV infection (formerly termed, “chronic or resolved” HCV infection) [http://www.cdc.gov/ncphi/disss/nndss/casedef/hepatitisccurrent.htm], from here on simply referred to as HCV infection. Accordingly, patients testing positive for any of the following laboratory criteria were classified as having HCV infection: antibody to HCV (anti-HCV) by enzyme immunoassay (EIA), recombinant immunoblot assay for anti-HCV, nucleic acid test for HCV RNA, or a determination of an HCV genotype. We defined prevalence as the number of patients with HCV infection (positive) divided by the number of persons tested for HCV (tested). For the calculation of annual prevalence, we considered patients positive for HCV infection if they had a positive serologic test or measurable qualitative or quantitative virologic test or a record of a specific HCV genotype in the current calendar year or any prior year of study enrollment; testing positive in a prior year could include the year before HOPS enrollment. For the calculation of annual prevalence, patients contributed to the numerator value of “positive” for the year in which they tested HCV positive and for each subsequent year that they remained under observation in the cohort. Patients contributed to the denominator value of “tested” for the year in which their first HCV test was performed and for each subsequent year that they remained under observation in the cohort. Patients entering the cohort as known positive for HCV infection contributed to the numerator and denominator in all years they remained under observation. For example, if a patient entered the HOPS in May 1999 and tested negative for HCV infection in April 2001, then tested positive for HCV infection in May 2002, and had a final HOPS visit in June 2004, this person would be counted in the numerator as a “positive” for 2002, 2003, and 2004 and contributed to the denominator of “tested” for the years 2001, 2002, 2003, and 2004. Active patients were considered eligible for testing during a calendar year if they had never been tested for HCV infection or had tested negative for HCV infection in the past. Our method for annual HCV prevalence estimation, whereby cases of HCV infection in numerator counted and “carried forward,” as long as the patient had been HCV tested and was in active HOPS follow-up in a particular year, allowed for various scenarios of patient entry, exit, and sometimes reentry into the study, consistent with the open cohort design of the HOPS.
We performed univariate analyses using the Pearson χ2 test for categorical data and the Wilcoxon rank sum test for continuous variable. P values <0.05 were considered significant. We performed univariate and multivariable multiple logistic regression analyses to examine factors associated with HCV testing during the study period. The Cochran-Armitage test for trend was used to assess trends in HCV prevalence over time. All analyses were performed using SAS, version 10.1 (SAS Institute Inc, Cary, NC).
The HOPS Cohort
From January 1, 1996, through December 31, 2007, there were a total of 7618 active patients in the HOPS (Table 1). The number of active patients in the study per year ranged from 2595 in 1996, increasing annually thereafter, to a maximum of 3380 patients in 2002, after which it decreased annually to 2662 patients in 2007. This trend was similar among the 3 age strata (age at HOPS entry <35, 35-44, and ≥45 years).
Trends in Testing for HCV Infection
Table 1 shows the demographic and HIV risk category characteristics of patients who were active (n = 7618) and HCV tested (n = 4606) in the HOPS cohort from 1996 through 2007. During the study period, the proportions of females and high-risk heterosexuals (HRH) enrolled in the HOPS increased, whereas the proportions of men, whites, IDUs, and MSM decreased. Whereas most shifts in the demographics of the HOPS patient population occurred in the earlier portion of the observation period, the proportion of IDU patients decreased steadily over time from 15.2% (395/2595) in 1996 to 11.6% (393/3380) in 2002 to 8.6% (229/2662) in 2007. The median age of the entire HOPS cohort increased from 38.6 years in 1996 to 44.6 years in 2007, as did the median age among all demographic and risk category groups. The increase in the median age was most substantial, however, for IDU patients (39.2 years in 1996 and 50.0 years in 2007).
Among the 7618 active patients, 310 patients were known to have HCV infection before study enrollment, resulting in 7308 patients who were eligible for subsequent HCV testing during the observation period (i.e., had either no record of prior testing or had had a negative test before enrollment). Overall, 4296 (58.8%) of these eligible patients were tested for HCV infection during observation. From 1996 to 2007, the absolute number and the proportion of eligible patients ever tested for HCV infection increased from 269 (10.7% of the eligible population in 1996) to 1733 (76.6% of the eligible population in 2007, Fig. 1); increases were observed in all sociodemographic groups (Fig. 2).
Although there was no consistent trend in the number of tests performed each year for HCV infection in the HOPS, the proportion of all HCV infection tests performed that were follow-up tests for patients with documented HCV-negative serostatus increased dramatically from 2.4% (3/124) in 1996 to 75.0% (417/556) in 2007.
Factors Associated With HCV Infection Testing
In multivariable analysis, the following groups were more likely (P < 0.05) to be tested for HCV infection (Table 2): patients aged 35-44 years compared with those aged <35 years at HOPS entry; patients of black race, Hispanic ethnicity, and other or unknown race compared with white patients; HRH and IDU patients compared with MSM patients; and patients with >3 years of enrollment and follow-up in the HOPS compared with those with ≤3 years. Patient gender, age ≥45 years at HOPS entry, insurance payer status at HOPS entry, or nadir CD4+ cell count at HOPS entry were not associated with the likelihood of being tested for HCV infection over the study period.
Trends in Prevalence of HCV Infection
From 1996 to 2007, there were a total of 1115 HCV infections identified among 4606 patients ever tested for HCV infection for an overall period prevalence of 24.2%. Among these 1115 infections, 805 were identified among patients whose HCV status was negative or unknown at HOPS enrollment and 310 represented patients known to have HCV infection at enrollment. The prevalence of HCV infection decreased from 36.7% in 1996 to 19.7% in 2007 (Fig. 1). Significant decreases (P < 0.01) were observed within most demographic and risk group strata from 1996 to 2000, with the exception of IDU (P = 0.32) and HRH (P = 0.36) patients (Fig. 3). Across the study period, prevalence of HCV infection remained consistently greater among patients ≥45 years old at HOPS entry compared with those aged 35-44 years and those aged <35 years at HOPS entry (41.5% vs. 40.3% and 31.9%, respectively, in 1996 and 24.2% vs. 22.0% and 13.8% in 2007), among females compared with males (29.9% vs. 22.5% for period 1996-2007), among blacks and Hispanics compared with whites (30.2% and 28.6% vs. 18.9% for 1996-2007), among IDU compared with HRH and MSM (80.8% vs. 18.1% and 10.2% for 1996-2007), and among publicly insured patients compared with privately insured patients (31.9% vs. 14.3% for 1996-2007).
Figure 4 shows the number of active patients with HCV infection by risk group and year, from 1996 to 2007, and the proportion of HCV-infected patients in each risk group. The number and relative proportion of HCV-infected HRH and MSM patients in the cohort was stable or increased slightly over the study observation period, but the number and resulting relative proportion of IDU patients with HCV infection in the HOPS decreased, changing from a peak of 59.7% (138/231) in 1997 to a period low of 41.9% (176/420) of all HCV infections in the HOPS in 2007.
To our knowledge, this study is the largest recent evaluation of trends in testing for and prevalence of HCV infection among a heterogeneous cohort of HIV-infected persons with long-term follow-up in the United States. We found that among patients active in the HOPS anytime from 1996 to 2007, the proportion of patients tested for HCV infection increased approximately 8-fold (from 10.7% to 76.6%) and the prevalence of HCV infection decreased almost 50% (from 36.7% to 19.7%). Patients were more likely to be tested for HCV infection if they were older than 35 years, were of nonwhite race or Hispanic ethnicity, were classified IDU or HRH, or had been followed more than 3 years in the HOPS. The increase in testing for HCV infection between 1996 and 2001 coincided with the 1999 release of guidelines that recommended universal testing of all HIV-infected persons; however, much of the increase actually occurred before their publication.31 Although recommendations for retesting known HCV-seronegative HIV-infected patients are not established, the fraction of all HCV tests performed annually in the HOPS for patients who had previously tested negative steadily increased from 1996 to 2007.
It remained concerning, however, that even in 2007, long after publication of the guidelines, nearly 1 of 4 HOPS patients went untested for HCV infection. As HOPS patients from sociodemographic groups traditionally at greater risk for HCV infection were more likely to be tested (e.g., IDU and blacks), it is possible that providers did not test some patients because they considered them at low risk for exposure to HCV (e.g., non-IDU MSM), although we have no definitive data to support this assertion. Recent data do suggest, however, that extensive sexual HCV transmission among HIV-infected MSM occurs.32,33 Regardless of perceived risk, it is important that all HIV-infected persons are tested for HCV infection so that coinfection can be identified as early as possible and prompt referral for treatment can occur.
In most serosurveys, the prevalence of HCV infection is driven primarily by the proportion of IDU in the cohort under study; the greater the fraction of IDU in the cohort, the greater the prevalence of HCV infection both in the general population13,34-37 and among HIV-infected persons.16,27,38,39 Whereas a recent study reported a decline in the incidence of HCV infection among IDUs from 1994 to 2004,40 we found that the prevalence of HCV infection among IDU patients did not decrease, in contrast to the pattern among the other demographic groups (Table 1, Fig. 2), and was consistently elevated at all time points. However, the fraction of all prevalent infections in the cohort attributable to IDU patients declined (Fig. 4), and that attributable to HRH and MSM patients increased, during the observation period.
The HOPS has seen an increase in median age across all demographic and risk groups; the increase was greatest among IDU patients (by 11 years compared with 6 years for other HIV risk groups). Our findings of relative aging of the IDU population are consistent with those in the national data and have been attributed to a cohort effect that coincided with the epidemic of IDU that began in the 1960s, peaked in the 1970s and 1980s, and decreased since then.41 Other surveys demonstrate that this age cohort, born between 1940 and 1960, is at greatest risk for HCV infection and that HCV infection incidence peaked in the mid-1980s and has been decreasing since then.12,14,42 The disproportionate increase in the median age of IDU patients in the HOPS suggests that, relative to patients from other risk groups, fewer young IDU patients were entering and/or more young IDUs were leaving the study. Nonetheless, the aging of the entire HOPS cohort is consistent with improvements in survival afforded by HAART, regardless of risk group. The relative reduction in the fraction of IDU patients and increase in the fraction of HRH and MSM patients among all prevalent HCV infections in the HOPS are consistent with the findings from the national surveillance data.43,44
Since 1996, proportionate mortality because of chronic liver disease has been increasing in the HOPS. In an analysis of 823 HOPS patients with and without HCV coinfection from 1996 to 2001, Tedaldi et al11 found disproportionately more deaths among HCV/HIV-coinfected patients, although HCV infection was not significantly associated with decreased survival. In other analyses, however, infection with HIV has been associated with higher HCV RNA viral load and more rapid progression of cirrhosis, liver failure, and hepatocellular carcinoma.2,45 Indeed, a recent analysis of mortality in the HOPS found that despite overall dramatic declines in mortality between 1996 and 2004, hepatic disease was the only reported cause of death for which absolute rates increased over time.46 The disproportionate liver-related mortality among patients coinfected with HCV may contribute to the reductions in HCV prevalence we observed over time.
Our findings are subject to limitations. First, data collected in the HOPS are not population based; therefore, trends and estimates derived from the study might not be representative of all HCV/HIV-coinfected persons in the United States. Second, we required only a single positive anti-HCV test for inclusion in the analyses because HCV confirmatory test results were not uniformly available or abstracted during the earlier part of the study period. Consequently, the true prevalence of chronic HCV infection in the HOPS is probably lower, given that 5-10% of HIV-infected persons seem to resolve HIV infection,47-49 although chronic seronegative HCV infection has been reported in as many as 13% of HIV-infected patients with advanced immunosuppression.50,51 Nonetheless, the effect of these factors should be modest and stable over time. The specificity of HCV EIA tests, however, has improved over time. Therefore, HCV EIA tests performed on HOPS patients in the 1990s were more likely to result in a false-positive test result than were such tests performed more recently.52 This may have lead to some overestimation of HCV prevalence in the earlier years of our observation period. Third, because subgroups of HOPS patients who were more likely to be tested (e.g., IDU, HRH, and patients of black and Hispanic ethnicity) also tended to have higher HCV coinfection rates, disparities in testing may have led us to overestimate the HCV prevalence in the HOPS population as a whole. Finally, because less than half of active patients in the cohort were tested for HCV infection before 2000, HCV infection prevalence estimates for earlier years may be less accurate, and some degree of bias in the temporal trends in HCV infection prevalence in HOPS over the study period cannot be ruled out.
In summary, we observed an overall decrease in the prevalence of HCV infection in the HOPS in recent years, associated with the reduction in the fraction of participating IDU patients, among whom HCV infection rates remained high and stable over time. Despite declining HCV prevalence, the overall rates we observed in the HOPS remained approximately 15-fold higher than HCV prevalence rates in the general US population (1.6%) estimated from the National Health and Nutrition Examination Survey (NHANES) during 1999 through 2002.14 Although the fraction of patients in the HOPS being tested (and retested) for HCV infection increased, a sizable portion of patients remained untested even in 2007. Testing all HIV-infected persons-irrespective of perception of risk-for HCV coinfection is imperative both to optimize patient management and to maximize opportunities to treat this potentially eradicable infection.
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APPENDIX: THE HOPS INVESTIGATORS
The HOPS Investigators currently include the following investigators and sites: John T. Brooks, Kate Buchacz, and Marcus Durham, Division of HIV/AIDS Prevention, National Center for HIV, STD, and TB Prevention, Centers for Disease Control and Prevention, Atlanta, GA; Kathleen C. Wood, Rose K. Baker, James T. Richardson, Darlene Hankerson, and Carl Armon, Cerner Corporation, Vienna, VA; Frank J. Palella, Joan S. Chmiel, Carolyn Studney, and Onyinye Enyia, Feinberg School of Medicine, Northwestern University, Chicago, IL; Kenneth A. Lichtenstein and Cheryl Stewart, National Jewish Medical and Research Center, Denver, CO; John Hammer, Benjamin Young, Kenneth S. Greenberg, Barbara Widick, and Joslyn D. Axinn, Rose Medical Center, Denver, CO; Bienvenido G. Yangco and Kalliope Halkias, Infectious Disease Research Institute, Tampa, FL; Douglas J. Ward and Jay Miller, Dupont Circle Physicians Group, Washington, DC; Jack Fuhrer, Linda Ording-Bauer, Rita Kelly, and Jane Esteves, State University of New York (SUNY), Stony Brook, NY; Ellen M. Tedaldi, Ramona A. Christian, Faye Ruley, and Dania Beadle, Temple University School of Medicine, Philadelphia, PA; and Richard M. Novak and Andrea Wendrow, University of Illinois at Chicago, Chicago, IL. Cited Here...
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