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Abstract

Objectives. To describe the prevalence, distribution and risk factors for hepatitis C virus (HCV) infection among homeless adults using eight Health Care for the Homeless (HCH) clinics nationally. Methods. Data were collected for 387 participants through blood draws, structured interviews, chart reviews. Results. Overall prevalence of HCV-antibody positivity was 31.0%, including 70.0% among injection drug users and 15.5% among reported non-injectors. Much HCV infection was hidden as the majority (53.3%) of HCV-antibody positive participants was unaware of their status. Independent risk factors for HCV among the total sample included injection drug use, prison, and tattoos; among injectors, risk factors included prison and three or more years of injection drug use; among reported non-injectors, risk factors included tattoos and prison. Conclusion. These HCH clinics serve high concentrations of HCV-infected injectors, making these and similar clinics priority intervention sites for aggressive screening, education, testing, and treatment for HCV and other blood-borne diseases.

Keywords

Homeless, hepatitis C, Health Care for the Homeless, tattoos, injection drug use, prison, risk factors, primary care clinics, blood borne disease, infectious disease, sexual risk

Hepatitis C (HCV) is a contagious virus that infects the liver, and it constitutes a serious public problem worldwide. In the U.S., HCV is transmitted primarily by exposure to infectious blood via injection drug use, although other sources may include transfusions before 1990, tattooing, non-injection drug use, accidental exposure to HCV-contaminated blood and blood products, and by exposure to an infected sexual partner (low risk).1-3 [End Page 811]

The U.S. prevalence of hepatitis C is estimated to be 1.6% (or 4.1 million).4 Most of these [an estimated 1.3% (or 2.7 to 3.9 million)] have chronic HCV.2,4 Although HCV-related diseases have a slow progression among people with chronic HCV, chronic HCV infection is the leading cause of cirrhosis and liver cancer.2,5-7 The prevalence of hepatitis C cirrhosis and its complications are expected to increase through 2020 in the U.S. due to infections acquired between 1970 and 1990.8-9 A disproportionate burden of HCV in the U.S. has been demonstrated for people who have low family income or a prison history; who are non-Hispanic Black males, HIV-infected, or Vietnam veterans; or who were born between 1945 and 1964.4,7

Recent U.S. prevalence estimates cited above are based on a national household survey, the National Health and Nutrition Examination Survey (NHANES) from 1999 through 2002.4 The NHANES estimates are based on a national household sample that included non-institutionalized people ages six and older.4 This figure likely understates the prevalence of HCV in the U.S. since it included many children at extremely low risk for HCV. Additionally, the NHANES did not include understudied populations such as homeless people or prison inmates, both of which have relatively high rates of HCV7,10-11 and low access to medical services where HCV might be diagnosed and treated.2,12 Higher rates of HCV have also been reported in U.S. mental health treatment institutions.13-14 Rates of newly acquired HCV infections appear to be declining,6,15-16 although interpretation of this trend is complicated by the failure to include many injection drug users and other high-risk groups in the current surveillance systems.2

Hepatitis C in homeless people.

Earlier studies of HCV in U.S. homeless adults report HCV rates that range widely between 26.5% and 69.1%,17-22 depending on each study's demographic profile and sample source. Studies have been based on diverse sampling sites11,18,20,23 and on very specific homeless sub-populations such as youth, veterans in domiciliary care, HIV-infected people, injectors, and people with serious mental illness or co-occurring substance use with major mental disorders.17-19,22 One study reported retrospective test results (i.e., based on self-reported results of prior HCV tests) with questionable validity.19 Several studies found severity of homelessness to be an independent factor for HCV, including Hall and colleagues who reported homelessness to be an independent risk factor for HCV among the urban poor in San Francisco.11,17

In the past decade, the National Institutes of Health (NIH) and the Centers for Disease Control and Prevention (CDC) have outlined a national agenda for HCV research that recommends continued epidemiological monitoring and studies on the specific modes of transmission among racial and ethnic minority people, low socioeconomic groups, and injection and intranasal drug users.24-25 The NIH and the CDC have emphasized that early detection and treatment, along with educational efforts for high-risk and infected people, are crucial elements of the national health agenda for preventing the spread and consequences of HCV. The Institute of Medicine's (IOM) 2010 Hepatitis and Liver Cancer: National Strategy for Prevention and Control of Hepatitis B and C concluded that reducing the rates of illness and death associated with hepatitis C will require improved identification of at-risk people and improved access to medical care.2

The NIH, CDC, and IOM Reports are pertinent to health care providers who serve homeless clients due to the high prevalence of HCV among homeless people who also [End Page 812] generally experience impaired health status and whose lives are already complicated by subsistence demands.2,24-25

In contrast to previous studies, the present study investigated the seroprevalence, distribution, and risk factors for HCV in a broader cross section of the homeless population; that is, homeless adults who attended one of eight Health Care for the Homeless Program (HCH) primary care clinics. The HCH is funded by the Bureau of Primary Health Care of the U.S. Health Resources and Services Administration. The federally funded HCH grantees serve about 700,000 people yearly. This study analyzed the extent, distribution and risk factors for HCV among 387 homeless clients systematically sampled from eight of 185 HCH clinics nationally. The results of this multi-site study will inform policymakers and health care providers about the extent and risk factors for HCV among a high-risk population of homeless adult clients of selected HCH clinics. Findings will support the ongoing national agenda for preventing the spread and consequences of HCV to homeless people and the broader community.

Methods

Design.

For this community-based study, the HCV Task Force of the Health Care for the Homeless Clinicians' Network (HCHCN, a membership group of the National Health Care for the Homeless Council, which included HCH clinicians and researchers), worked collaboratively to design and oversee this study from its inception, including development of the research questions, fieldwork protocol and data-collection instruments. Lead clinicians from the HCH Hepatitis C Task Force volunteered their clinics as study sites and agreed to lead their clinic's onsite data collection. Additional clinics were recruited to balance geographic distribution. A $500 incentive was provided to each participating clinic to offset partially staff time used for data collection.

A convenience sample of eight clinics was chosen from geographically diverse urban settings including Los Angeles, California; Phoenix, Arizona; Denver, Colorado; Albuquerque, New Mexico; Des Moines, Iowa; Milwaukee, Wisconsin; Birmingham, Alabama; and Providence, Rhode Island.

Study protocols were pilot-tested at three sites. Researchers and HCH project staff then worked with clinical teams at each clinic to tailor the standard research protocol to each site. Then each clinical team, which would be collecting all data for the study at their respective sites, also piloted data collection and fieldwork protocols at their own sites. The HCH Project Director and the researchers were available on-call throughout the piloting and data collection process to address emerging issues and concerns. Training in laboratory procedures was similarly carried out between the Project Director, individual site staffs, and the independent laboratory coordinator. The lab coordinator met with individual sites to discuss the lab protocol including blood testing, storage, and mailing procedures. All blood was tested at a centralized laboratory.

Sampling, screening, and recruitment.

The recruitment goal was 50 homeless adult clients randomly sampled from each of the eight study clinics for a total sample size of 400. Lead clinicians continued recruitment over a number of days until a sample size of 50 clients was completed for each clinic. [End Page 813]

At the beginning of the clinic day, an intake staff person systematically sampled potential subjects from the appointment list or intake roster, for example, by sampling every fifth client after a random start. In turn, each of these clients was orally screened for eligibility for the study based on two criteria: age (18 and older) and literal homelessness. Literal homelessness was based on a yes/no question to determine whether the client had spent the previous night in a shelter or on the streets.

You spent last night in a homeless shelter or "on the streets"? "On the streets" can include any place not designed for human habitation such as a vehicle, abandoned buildings, parking structures, buses or subways, public buildings (such as hospital emergency rooms), movie houses, and outside. (YES/NO)

Eligible clients were invited to complete an interview and blood draw to test for HCV and hepatitis B (HBV) infections. The clinician then obtained written informed consent to participate in the study. A separate consent form authorized subsequent access to each client's medical records to determine whether they returned for their test results.

Each client completed a 20-minute face-to-face interview with the lead clinician followed by tailored pre-test counseling for HBV and HCV and then a blood draw. Each client received an incentive of $10 cash or a $10-cash equivalent for completion of all three. Clients were then scheduled for an appointment in the same clinic about two weeks later to obtain the results of their blood tests.

Blood specimens, identified only by a case number, were sent to and tested by an independent central laboratory. Only HCV results were prepared for this paper. Blood samples were analyzed by Consolidated Laboratory Services, who identified cases with HCV antibody positivity using the DiaSorin's ETI-MAX-3000 Microtiter Analyzer. Based on the CDC suggested protocol, confirmation of HCV antibody positivity was conducted using the recombinant immunoblot assay (RIBA) test for cases in which the signal-to-cutoff ratio was less than 3.8 on the initial HCV antibody EIA test.26

Individual lab results were faxed back to respective clinics and affixed to each client's medical chart by clinic staff. Returning clients were notified of test results, and depending on results, they received tailored post-test counseling. Clients testing HCV positive received treatment or referral. The HCH Task Force provided written pre- and post-test counseling guidelines as a resource for the clinics.

Documenting HCV treatment that clients received at the clinics was not within the scope of the present study. Nevertheless, the treatment provided by each clinic was based on site-specific protocols. All clinics, as mandated by state licensure and HCH requirements, were to provide services as clinic resources would allow. This meant that after identification of HCV positivity and liver enzyme results, further evaluation or treatment would have been provided either by the individual clinics or through appropriate referrals. Clinics were expected to conduct further testing that may have included more specific HCV lab tests, such as viral loads, genotyping, phenotyping or liver biopsies. If individual clinics were unable to perform such testing due to lack of services or funds to pay for such services, clinics were to refer clients to appropriate specialty clinics for further evaluation or treatment. This was the standard of practice among HCH program services. Potential treatment or referral for care was included in the client's consent form. [End Page 814]

Data collection.

The structured interview included questions about demographic characteristics and background; homelessness history; detailed medical, psychiatric, and prison history; HCV-specific knowledge and prior testing; and recent alcohol use. Questions also included potential risk behaviors for HCV transmission including lifetime drug use [e.g., drugs used, modes of use (i.e., injection, intranasal, or smoked), and sharing of injection and other drug-use equipment]; tattoos; transfusions before 1990; and sexual risk behaviors (including number of lifetime sex partners, trading sex for cash or drugs, and lifetime anal sex). The instrument was adapted from a prior study of homeless and other indigent adults.27 Additional items were developed by the HCHCN HCV Task Force to address specific concerns of clinical staff.

The completion rates varied by site from 92% to 100%. Overall, 396 clients completed interviews, and among these, 387 had blood draws for an overall completion rate of 97.7%. In six clinics, lead clinicians reviewed medical records for 300 clients to determine whether each one returned for results. Among these, records indicated that 186 (62%) clients returned to the clinics during their respective 30-day follow-up periods.

The University of California Los Angeles (UCLA) Institutional Review Board (IRB) served as the multiple project assurance agency that approved the study. The study was also approved by the Federal Office of Management and Budget and individual clinic IRBs. Prior to data collection, all research and clinic personnel involved in the study completed an online UCLA IRB course in the protection of human subjects.

Data analysis.

Data from the eight clinics were merged into an aggregated dataset. Data analysis was performed using SAS® 9.0 software (SAS Institute Inc., Cary, NC, USA). Categorical variables were created for age (younger than 45 years and 45 years or older), number of lifetime sexual partners (fewer than 15 or 15 or more), chronic homelessness (one year or more accumulated since age 18 versus less than one year), tattoos, and years of injection drug use. Differences between sites were analyzed using chi-squared tests. At the bivariate level, associations between categorical variables and HCV infection were examined with odds ratios (OR) and 95% confidence intervals (CI).

Three logistic regression models were developed to identify variables independently associated with HCV infection for the total sample and for two mutually exclusive groups: i.e., those who reported injection of any illicit drugs in their lifetimes, and those who reported none. Each model initially included all variables that were at least marginally associated with HCV status in the bivariate analysis (p≤.10). Each model also controlled for age as a continuous variable, biological sex, and race. Variables were entered into stepwise backward logistic regression models to create a core model, and then each model was confirmed using stepwise forward analysis. Variables in each core model were examined and corrected for multicollinearity, defined as correlations greater than 0.5 and a variance inflation factor greater than or equal to four. Model fit was judged by the comparison of the -2 log-likelihood of model improvement and Wald statistics of the beta coefficients.

Results

HCV seroprevalence and distribution by site (Table 1).

Overall, 31% of the sample was HCV-antibody positive. The variation in HCV rates by site approached statistical [End Page 815] significance (18.0%-47.9%, p<.10). Injectors accounted for the great majority (nearly two-thirds) of all HCV-positive clients. In all sites, HCV was significantly associated with rates of IDU, and HCV ranged from 55.6% to 81.8% among injectors. HCV ranged from 7.1% to 21.4% among reported non-injectors.

Sample overview (Table 2).

The majority of the sample was male, non-White, and high school graduates with a median age of 44. Few self-identified as gay or bisexual (5.9%). Most experienced chronic homelessness (i.e., one year or longer cumulatively as an adult), and half (51.7%) were homeless for two years or longer. Sixteen percent of the sample (21% of men, not shown) were U.S. military veterans. During the 30 days prior to the interview, about half the sample had used alcohol at least once, and about one-third of the sample reported hazardous drinking (i.e., they drank four or more drinks on at least one of those days).

Regarding potential risk factors for HCV, more than one-third of the sample had ever been in prison. Two-fifths of the sample had at least one tattoo. Fourteen percent reported a transfusion of blood or blood products before 1990. About half reported

Table 1. Distribution of Hepatitis C Antibody for the Total Sample and by Site Stratified by Injection Drug Use History (N=387 Literally Homeless Adult Clients of Eight Health Care for the Homeless Clinics)a
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Table 1.

Distribution of Hepatitis C Antibody for the Total Sample and by Site Stratified by Injection Drug Use History (N=387 Literally Homeless Adult Clients of Eight Health Care for the Homeless Clinics)a

[End Page 816]

Table 2. Prevalence of Hepatitis C Antibody (HCV+) among Clients of Eight HCH Clinics by Background Characteristics and Potential Risk Behaviors (N=387 Literally Homeless Adults)
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Table 2.

Prevalence of Hepatitis C Antibody (HCV+) among Clients of Eight HCH Clinics by Background Characteristics and Potential Risk Behaviors (N=387 Literally Homeless Adults)

[End Page 818]

more than 15 sexual partners, and about one fifth had ever been paid for sex or been given drugs for sex. More than one-third (38.5%) of women and 3.3% of men reported lifetime anal sex.

Lifetime drug use was highly prevalent, with three-quarters reporting illicit drug use at least once. Many (28.4%) had ever injected illicit drugs, including heroin, cocaine and speed, and half of these had injected drugs during the previous 12 months. More than half (54.8%) of the sample had ever snorted cocaine.

Bivariate associations with HCV for the total sample (Table 2).

In bivariate analysis of the total sample, HCV rates were significantly higher among men, older people, and adults with more education. HCV was also higher among adults with time in prison, tattoos, recent hazardous drinking, 15 or more lifetime sexual partners, and a history of giving sex for drugs. HCV rates were significantly lower in African Americans. High-risk lifetime sexual practices such as anal sex or having been paid for sex were not significantly associated with HCV. Drug use history was associated with HCV antibody positivity including lifetime illicit drug use, intranasal use of cocaine, and injection drug use. We conducted a subgroup analysis by injection history. [End Page 819]

Bivariate associations with HCV for injectors (Table 3).

HCV prevalence among lifetime injection drug users was 70.0%. The injector subgroup was mostly male, White, and high school graduates, with a median age of 44. The majority had been in prison and had tattoos. The median time using injection drugs was 3.5 years, and HCV rates were strongly associated with total time injecting (i.e., HCV was 45.5% at less than one year, 60.0% at one to less than three years, and 81.4% at three years or more). More than two-thirds had been chronically homeless (homeless for one year or longer). Among injectors, HCV-antibody positivity was significantly higher among clients who were age 45 or older, were former prison inmates, had injected drugs for three years or longer, or had ever injected cocaine or injected heroin. HCV rates were only marginally higher for males compared to females, for Hispanics compared with non-Hispanic Whites, and for clients reporting 15 or more lifetime sexual partners.

Bivariate associations with HCV for non-injectors (Table 3).

In the subgroup that reported no history of injection drug use, 15.5% were HCV-antibody positive. The non-injector subgroup was predominantly male, non-White, and high school graduates with a median age of 45. One-third had ever been in prison or had tattoos. Two-thirds of the non-injector subset had used illicit drugs. Two-fifths had more than 15 lifetime sexual partners. In the non-injector subgroup, HCV positivity was significantly higher among men, Native Americans compared with non-Hispanic Whites, clients with tattoos, former prison inmates, and those who had ever been paid for sex. HCV rates were only marginally higher among more educated clients and those never given drugs for sex.

Multivariate associations with HCV for the total sample (Table 4).

Logistic regression analysis was used to identify significant independent risk factors for HCV antibody positivity in the total sample and then for the injector and non-injector subgroups, controlling for age (as a continuous variable), biological sex and White vs. non-White race. In the total sample, lifetime injection drug use, prison history, and having tattoos were significant independent predictors for HCV-antibody positivity. That is, injectors had 12.2 times greater odds of testing positive for HCV compared with the rest of the total sample. Clients with a prison history or tattoos had 2.9 and 2.7 times greater odds of testing positive for HCV respectively compared with the rest of the total sample.

Multivariate associations with HCV for the injector subsample (Table 4).

Among the injector subsample, prison history and three or more years of injection drug use were significant independent predictors of HCV-antibody positivity, with 3.7 and 3.3 times greater odds respectively of testing positive for HCV compared with other injectors.

Multivariate associations with HCV for the non-injector subsample (Table 4).

Among the non-injector subsample, having tattoos and a prison history were significant independent predictors of HCV-antibody positivity with 4.4 and 2.2 times greater odds respectively of testing positive for HCV compared with other non-injectors.

HCV testing history, knowledge, and hidden infection.

About 41.7% of the sample reported prior HCV testing. However, more than half (53.4%) of clients who actually tested HCV positive did not know they were currently HCV positive. While a great majority of the sample knew they could get infected with HCV from using a dirty or contaminated needle or syringe (90.2%), only about one-third knew that they could not get infected with HCV from contaminated food (35.2%) or that there was no vaccination against HCV (30.3%) (not shown). [End Page 820]

Table 3. Prevalence of Hepatitis C Antibody Positivity (HCV+) among Eight HCH Clinics by Background Characteristics and Potential Risk Behaviors, Stratified by History of Injection Drug Use (N=87 Literally Homeless Adults)
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Table 3.

Prevalence of Hepatitis C Antibody Positivity (HCV+) among Eight HCH Clinics by Background Characteristics and Potential Risk Behaviors, Stratified by History of Injection Drug Use (N=87 Literally Homeless Adults)

[End Page 825]

Table 4. Factors Independently Associated with Hepatitis C Antibody Positivity (HCV+) among Clients of Eight HCH Clinics for the Total Sample and Stratified by Drug Injection History (N=387 Literally Homeless Adults)a
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Table 4.

Factors Independently Associated with Hepatitis C Antibody Positivity (HCV+) among Clients of Eight HCH Clinics for the Total Sample and Stratified by Drug Injection History (N=387 Literally Homeless Adults)a

Discussion

This study reports the prevalence, distribution, and risk factors for HCV infection among homeless clients from eight Health Care for the Homeless Program primary care clinics nationally. The prevalence of HCV infection overall (31.0%), was in the lower range of estimates found in previous studies of homeless adults.11,19 HCV prevalence rates varied marginally by site and were strongly associated with the proportion of injection drug users at each site.

Overall, and in each of the clinics (ranging from 18.0%-47.9%), HCV rates were high relative to the estimated HCV rate for the U.S. general population (1.6%). Unfortunately, the U.S. estimate is calculated based on the general population ages six and older, which biases downward the national HCV estimate due to the large number of minors who have a minimal chance of HCV infection. Such a calculation exaggerates the difference in HCV rates between homeless adults and the general population. Although used widely as the U.S. prevalence rate for comparison in HCV studies, it has limited utility for comparison with the HCV prevalence reported here for the total sample of homeless adults.

Total sample.

Generally, the burden of HCV fell more heavily on males, older clients, and clients with time in prison, tattoos, recent hazardous drinking, 15 or more sexual partners, and a history of trading drugs for sex. HCV prevalence overall was significantly [End Page 826] lower for clients with lower education. Overall, non-Hispanic African Americans had significantly lower rates of HCV than non-Hispanic Whites. These findings for African Americans are surprising since they contrast with the U.S. general population among whom HCV rates were significantly higher among African Americans, based on NHANES.28 However, when disaggregated by injection sub-groups (in Table 3), we found that HCV rates among African American injectors were only slightly higher (not significantly higher) than White injectors, and African-American non-injectors were not significantly different from White non-injectors. Both aggregated and disaggregated findings contrast with the U.S. general population findings for African Americans.4

In bivariate analysis, important drug-use variables that were associated with HCV-antibody positivity included lifetime injection drug use (heroin, crack, and speed), lifetime illicit drug use, and intranasal use of cocaine. As reported here for the majority of HCV-positive homeless clients (53%), many high-risk populations in the U.S. similarly lack knowledge about HCV, including chronic HCV infection.2

Homeless injectors.

Consistent with the broader literature on HCV, the primary independent risk factor for HCV in this sample was injection of illicit drugs. More than one-quarter of the sample (28.4%) reported lifetime injection drug use compared with an estimated 2% in the U.S. general adult population.4

The HCV rates for homeless and general population adults are more similar when comparing by similar ages and behavioral risk factors. On point, homeless adult injectors (ages 18 and older) had a higher rate of HCV (70.0% reported here) compared with adult injectors in the general population (ages 20-59), which is estimated at 57.5% based on the NHANES data.4 Nearly two-thirds of homeless adults who were HCV-positive reported histories of injection drug use, while by contrast, only about half of HCV-positive adults in the general population reported injection histories.4 Rates for injectors in the eight clinics ranged from 55.6% to 81.8%. While injectors represented about one-quarter of the entire sample, they accounted for nearly two-thirds (64.2%) of HCV-positive cases. Injectors were 12 times more likely than non-injector clients to be HCV-positive. Overall, about one in five homeless adults in the sample (19.9%) was an injector who tested positive for HCV. Strikingly, HCV rates were strongly associated with duration of injection drug use: HCV rates were 45.5% at less than one year, 60.0% from one up to three years, and 81.4% for three years or longer. Similarly, the rate of HCV among injectors in our sample was similar to HCV rates found among longer-term injectors in other samples (65-90%),2 but higher than the rates among housed young injectors in Los Angeles (27%).2

Homeless non-injectors.

Reported non-injectors had significantly lower yet still noteworthy rates of HCV positivity (15.5%) compared with homeless injectors. HCV rates for homeless non-injectors were high relative to non-injectors in the general U.S. adult population, who ranged from 0.7%-3.5% based on the NHANES.4 Non-injectors accounted for more than one-third of the HCV-positive homeless clients (35.8%). In multivariate analysis, ever getting a tattoo or having a prison history were independent risk factors for HCV-positivity. Among non-injectors, clients with any histories of prison or tattoos were respectively two and four times more likely to test HCV-positive.

Altogether, there were 18 HCV-positive clients who reported neither injection drug use nor tattoos (15% of all HCV-positive clients). Since injection drug use is the [End Page 827] predominant mode of HCV transmission, it is possible that some of these 18 had a history of injection drug use that they did not report. Otherwise, they may have been exposed to contaminated blood through one of the less common possible modes of transmission including transfusion, non-injection drug use, or high-risk sexual behavior.

Specific risk factors for HCV.

Prison history.

As reported in previous studies, prison exposure was a significant independent risk factor for HCV infection for the total sample and the injector and non-injector subgroups, even after controlling for sex, race, and age. Strikingly, 37.9% of the sample reported time spent in prison, and about half these were HCV antibody positive (50.7%), a rate that is higher than the range found in incarcerated populations in the U.S. (12-35%).2,4 In contrast to findings here, population-based studies of homeless adults generally have reported higher rates of prison or incarceration (prison or jail) (51%-80%).

As prison is a potential site of HCV transmission due to injection drug use or tattoos with contaminated paraphernalia, improved prison-specific HCV screening and prevention strategies are needed.12,29-30 In one report, while 94% of all inmates are incarcerated in state facilities that have HCV testing polices, 69% of these facilities direct testing to high-risk groups or per patient request.31 While testing populations with high rates of injection drug use is efficient for identifying HCV-positive people, factors contributing to acceptance of testing and completion of treatment must also be identified.12

Tattoos.

Tattoos were a significant independent risk factor for HCV in the total sample and among non-injectors, even after controlling for prison exposure. This finding contributes to the larger body of evidence suggesting tattoos as a potential mode of HCV transmission.21 There is also evidence that tattoos, particularly those received in prison, may be a risk factor given reported sharing of tattoo-making equipment in a population with high HCV infection rates and other risk behaviors for HCV.32-33 It is possible that tattoos could serve as a surrogate marker for high-risk behavior among clients under-reporting injection drug use. However, while prior studies have demonstrated that survey data tends to under-estimate illicit drug use, there is no evidence to support that tattoos specifically are reported in lieu of drug use.34

No evidence of sexual risk for HCV.

Consistent with previous studies of homeless adults, we found no evidence of HCV risk associated independently with risky sexual behaviors.11 Although HCV was significantly higher in bivariate analysis among clients with two sexual risk behaviors (i.e., more than 15 sexual partners and giving sex for drugs), neither had an independent relationship to HCV infection once other variables were controlled for.

No evidence of intranasal drug use as a risk for HCV.

Although HCV was significantly higher in bivariate analysis among clients with a history of intranasal cocaine use, no intranasal drug use variables had an independent relationship to HCV infection after other variables were accounted for.

Severity of homelessness.

As reported elsewhere,21 marginally higher HCV prevalence was found among people who experienced chronic homelessness (i.e., one year or longer cumulatively).

Strengths.

Significantly, this study demonstrated the successful collaboration between a community-based interdisciplinary team of HCH clinicians and clinician-researchers with academic researchers. As a function of the project's organization, clinicians rather [End Page 828] than research staff conducted interviews at each site. Other strengths of this study include its multisite design, random patient selection within each site, and extensive information collected from structured interviews, blood tests, and medical chart reviews.

Limitations.

Most data (other than HCV-antibody status and medical record data) were self-reported and subject to bias (e.g., injection drug use or specific sexual behaviors may be underreported due to stigma). Although all eight clinics were in urban settings, and clients were randomly selected within each site, the clinic sites themselves were not randomly selected, which limits the generalizability of findings to these specific clinics. However, the demographic characteristics closely parallel figures for a nationally representative sample of homeless adults by Burt on gender, race and ethnicity, and education.35 Finally, clients were recruited and interviews were conducted by clinic staff, which may have enhanced response rates and influenced reliability of self-reported data on sensitive questions (e.g., injection drug use or specific sexual behaviors) due to social desirability, although the potential effects of using clinic staff as researchers were not evaluated.

Conclusion.

There were high concentrations of HCV-antibody positivity among homeless clients overall and in each of the eight HCH primary care clinics studied. Injection drug use was the strongest predictor of HCV-antibody positivity and continues to be the presumptive primary mode of HCV transmission. However, findings suggest that tattoos may also be a significant mode of transmission given that tattoos demonstrated a relationship with HCV that was independent of injection drug use, prison, and other risk factors. In particular, tattoos may help explain HCV among non-injectors.

Nearly one-third of homeless adults who presented at the eight HCH clinics during the study were already infected with HCV. The majority of these did not know that they had been infected. Many of the rest, although not infected, reported risk behaviors for HCV exposure including injection drug use, non-injection drug use, and having tattoos.

The high concentrations of HCV-infected clients along with clients engaged in high-risk behaviors make these and similar clinics opportune intervention sites for aggressive and comprehensive services that would include screening, testing, education, and treatment for HCV and other blood-borne diseases, as recommended by the NIH, IOM, CDC and others.2,7,25 Our findings support the explicit inclusion of homeless people in the national agenda on preventing and controlling HCV. The agenda emphasizes that early detection and treatment of infected people, along with educational efforts for those with high-risk behaviors, are crucial elements for preventing the spread and consequences of HCV. Given the array of proven and potential high-risk behaviors for exposure to HCV, our study also supports the inclusion of homeless adults in continued epidemiological monitoring and studies of specific modes of transmission.25 Effective HCV prevention, education, and treatment programs for homeless people could decrease transmission, improve morbidity and mortality rates, and potentially decrease health care costs from end stage liver disease.

Primary care and prevention.

Primary and secondary prevention strategies are the main findings from this study that service providers should incorporate into their clinical practices. Providers must assess client risk factors such as IDU, tattoos, prison history, non-injection drug use, and risky sexual behaviors, and provide specific education interventions to clients that address these matters and the facts about how lifestyle [End Page 829] patterns may place them at higher risk for HCV exposure and possible development of liver disease. Lastly, these findings may spark political action among primary health care providers to advocate for effective screening and treatment services for homeless individuals.

One concrete example of primary prevention is provided in the 2010 IOM report on the prevention and control of hepatitis B and C. The IOM recommended that federal and state governments reduce the risk of hepatitis C virus infection due to injection drug use by providing comprehensive HCV prevention programs for injectors in community health facilities. Such programs would include education on safer injection practices, access to sterile needles and syringes and drug-preparation equipment, and expansion of prevention and care services in settings that injectors and non-injection drug users are likely to use.2,37

Implications for treatment of HCV.

Recently approved by the Federal Drug Administration, new HCV therapies promise treatment response rates upwards of 85%.38-39 Yet, HCV treatment remains expensive and challenging for many service providers and their homeless clients. HCV treatment, including antiviral medications and laboratory monitoring, is expensive and often prohibitive for many primary care programs and their potential referral resources. Unstable housing is a major barrier to treatment continuity. In addition, mental health and substance use disorders, which are relatively common among homeless adults, are contraindications for treatment with current antiviral medications such as pegylated interferon and ribavirin. Ideally, antiviral treatment would include support for abstinence from substance use and monitoring of mental health disorders such as depression. Furthermore, the median age of homeless adults in the U.S. is increasing over time.36 Chronic health conditions such as hepatitis-related liver cancer and cirrhosis increase with age, and they will present challenges to traditional caregiving in an aging homeless population. Researchers warn that public systems of care should expect increasing costs related to HCV infection as homeless and other indigent individuals develop the serious medical sequelae of chronic HCV infection.8,18

The U.S. is now faced with a large reservoir of individuals untreated for HCV, including many homeless adults, for whom no strong treatment guidelines or recommendations exist. The IOM Report concluded that funding for preventive and other viral hepatitis services at community health centers, including homeless programs, had been inadequate.2 The IOM authors recommended that public agencies provide adequate resources to federally funded treatment facilities, including primary care sites, to provide comprehensive viral hepatitis services for homeless and other at-risk indigent clients.2 Failure to screen, educate, and treat these populations will lead to unnecessary human suffering related to HCV infection and associated end stage liver disease. As a consequence, health care expenditures will likely increase, and failure to tailor treatment programs to under-served populations such as homeless adults may lead to less effective treatment programs that can result in non-adherence to medical protocols, which in some cases can lead to drug resistance.40

It is time to fund and work with primary care centers in the U.S. that serve populations with the highest burden of HCV to develop prevention, screening, and treatment programs tailored to these high-risk populations. The literature on homeless people is limited with regard to effective HCV treatment studies. Research is needed to help [End Page 830] reduce risk behaviors, identify barriers to services, and improve treatment strategies that may eventually prevent, delay, and significantly reduce HCV and related liver disease among homeless and other high-risk populations.

Aaron J. Strehlow, Marjorie J. Robertson, Suzanne Zerger, Catherine Rongey, Lisa Arangua, Ed Farrell, Adele O'Sullivan, and Lillian Gelberg

The authors are affiliated with the UCLA School of Nursing (AJS), the Alcohol Research Group (MJR), the Center for Social Innovation (SZ), San Francisco Veterans Affairs Medical Center and the University of California, San Francisco (CR), UCLA (LA), Clinical Family Health Services in Thornton, Colorado (EF), Circle The City in Phoenix (AO'S), and UCLA David Geffen School of Medicine (LG).

Please address correspondence to Aaron J Strehlow, RN, PhD, FNP-BC, FNP-C, NPNP, 1228 N La Cienega Blvd., #102, West Hollywood, CA 90069-2485; (310) 659-7761; astrehlo@ucla.edu.

Acknowledgments

We are grateful for the selfless effort of the lead clinicians and their teams who implemented the research protocols at the following HCH sites: Albuquerque HCH, Inc. in Albuquerque, NM (Sarah Langwell,); Birmingham HCH Coalition, Inc. in Birmingham, AL (Zakir Khan); Stout Street Clinic, Colorado Coalition for the Homeless in Denver, CO (Ed Farrell); The Outreach Project, Primary Health Care, Broadlawns Medical Center in Des Moines, IA (Lorna Hines); UCLA School of Nursing Health Center at the Union Rescue Mission in Los Angeles, CA (Aaron Strehlow); St. Ben's Clinic for the Homeless, St. Mary's Hospital in Milwaukee, WI (Carol Sejda); HCH Program, Maricopa County DPH in Phoenix, AZ (Adele O'Sullivan); and Crossroads Rhode Island in Providence, RI (Gloria Rose). We gratefully acknowledge the support of Jean Hochron, Chief, Amy M. Taylor, Deputy Chief, of the Health Care for the Homeless Branch, HRSA, of the U.S. Department of Health and Human Services and the National Health Care for the Homeless Council.

Primary funding for this project was provided by the Homeless Branch, Division of Programs for Special Populations, Bureau of Primary Health Care, HRSA, HHS. Additional support for Robertson and Gelberg was provided by the National Institute on Drug Abuse (RO1-DA14294, "Hepatitis B and C Among Homeless Adults"). Robertson was also supported by the NIAAA National Alcohol Research Center at the Alcohol Research Group of the Public Health Institute in Emeryville, CA.

Notes

1. Ghany MG, Strader DB, Thomas DL, et al. Diagnosis, management, and treatment of hepatitis C: an update. Hepatology. 2009 Apr;49(4):1335-74.

2. Institute of Medicine. Hepatitis and liver cancer: a national strategy for prevention and control of hepatitis B and C. Washington, DC: The National Academies Press, 2010. Available at: http://books.nap.edu/openbook.php?record_id=12793.

3. Terrault NA. Sexual activity as a risk factor for hepatitis C. Hepatology. 2002 Nov;36(5 Suppl 1):S99-105.

4. Armstrong GL, Wasley A, Simard EP, et al. The prevalence of hepatitis C virus infection in the United States, 1999 through 2002. Ann Intern Med. 2006 May 16;144(10):705-14.

5. Di Bisceglie AM. Natural history of hepatitis C: its impact on clinical management. Hepatology. 2000 Apr;31(4):1014-8.

6. Seeff LB, Hoofnagle JH. National Institutes of Health Consensus Development Conference management of hepatitis C: 2002. Hepatology. 2002 Nov;36(5 Suppl 1):S1-2.

7. Kuehn BM. Silent epidemic of viral hepatitis may lead to boom in serious liver disease. JAMA. 2009 Nov 11;302(18):1949-50, 1954.

8. Davis GL, Alter MJ, El-Serag H, et al. Aging of hepatitis C virus (HCV)-infected people in the United States: a multiple cohort model of HCV prevalence and disease progression. Gastroenterology. 2010 Feb;138(2):513-21, 521 e1-6.

9. Armstrong GL, Alter MJ, McQuillan GM, et al. The past incidence of hepatitis C virus [End Page 831] infection: implications for the future burden of chronic liver disease in the United States. Hepatology. 2000 Mar;31(3):777-82.

10. Ruiz JD, Molitor F, Plagenhoef JA. Trends in hepatitis C and HIV infection among inmates entering prisons in California, 1994 versus 1999. AIDS. 2002 Nov 8;16(16): 2236-8.

11. Nyamathi AM, Dixon EL, Robbins W, et al. Risk factors for hepatitis C virus infection among homeless adults. J Gen Intern Med. 2002 Feb;17(2):134-43.

12. Weinbaum C, Lyerla R, Margolis HS. Prevention and control of infections with hepatitis viruses in correctional settings. MMWR Recomm Rep. 2003 Jan 24;52(RR-1):1-36; quiz CE1-4.

13. Al Jurdi RK, Burruss JW. Prevalence of hepatitis C in psychiatric institutions. Psychosomatics. 2003 Sep-Oct;44(5):439-40.

14. Dominitz JA, Boyko EJ, Koepsell TD, et al. Elevated prevalence of hepatitis C infection in users of United States veterans medical centers. Hepatology. 2005 Jan;41(1):88-96.

15. Vajdic CM, Grulich AE, Kaldor JM, et al. Specific infections, infection-related behavior, and risk of non-Hodgkin lymphoma in adults. Cancer Epidemiol Biomarkers Prev. 2006 Jan;15(6):1102-8.

16. Rustgi VK. The epidemiology of hepatitis C infection in the United States. J Gastroenterol. 2007 Jul;42(7):513-21.

17. Hall CS, Charlebois ED, Hahn JA, et al. Hepatitis C virus infection in San Francisco's HIV-infected urban poor. J Gen Intern Med. 2004 Apr;19(4):357-65.

18. Desai RA, Rosenheck RA, Agnello V. Prevalence of Hepatitis C virus infection in a sample of homeless veterans. Soc Psychiatry Psychiatr Epidemiol. 2003 Jul;38(7):396-401.

19. Cheung RC, Hanson AK, Maganti K, et al. Viral hepatitis and other infectious diseases in a homeless population. J Clin Gastroenterol. 2002 Apr;34(4):476-80.

20. Schwarz KB, Garrett B, Alter MJ, et al. Seroprevalence of HCV infection in homeless Baltimore families. J Health Care Poor Underserved. 2008 May;19(2):580-7.

21. Stein JA, Nyamathi A. Correlates of hepatitis C virus infection in homeless men: a latent variable approach. Drug Alcohol Depend. 2004 Jul 15;75(1):89-95.

22. Klinkenberg WD, Caslyn RJ, Morse GA, et al. Prevalence of human immunodeficiency virus, hepatitis B, and hepatitis C among homeless people with co-occurring severe mental illness and substance use disorders. Compr Psychiatry. 2003 Jul-Aug; 44(4):293-302.

23. Sherriff LC, Mayon-White RT. A survey of hepatitis C prevalence amongst the homeless community of Oxford. J Public Health Med. 2003 Dec;25(4):358-61.

24. Alter MJ. Integrating risk history screening and HCV testing into clinical and public health settings. Am Fam Physician. 2005 Aug;72(4):576, 579.

25. NIH Consensus Statement on Management of Hepatitis C: 2002. NIH Consens State Sci Statements. 2002 Jun 10-12;19(3):1-46.

26. Alter MJ, Kuhnert WL, Finelli L. Guidelines for laboratory testing and result reporting of antibody to hepatitis C virus. MMWR Recomm Rep. 2003 Feb 7;52(RR-3):1-13, 15; quiz CE1-4.

27. Robertson MJ, Clark RA, Charlebois ED, et al. HIV seroprevalence among homeless and marginally housed adults in San Francisco. Am J Public Health. 2004 Jul; 94(7):1207-17.

28. Howell C, Jeffers L, Hoofnagle JH. Hepatitis C in African Americans: summary of a workshop. Gastroenterology. 2000 Nov;119(5):1385-96. [End Page 832]

29. Fox RK, Currie SL, Evans J, et al. Hepatitis C virus infection among prisoners in the California state correctional system. Clin Infect Dis. 2005 Jul 15;41(2):177-86.

30. Spaulding AC, Weinbaum CM, Lau DT, et al. A framework for management of hepatitis C in prisons. Ann Intern Med. 2006 May 16;144(10):762-9.

31. U.S. Department of Justice, Office of Justice Programs. Hepatitis testing and treatment in state prisons. (April 2004, NCJ 199173C.) Washington, DC: U.S. Department of Justice, 2004. Available at: http://bjs.ojp.usdoj.gov/content/pub/pdf/httsp.pdf.

32. Hellard ME, Aitken CK, Hocking JS. Tattooing in prisons—not such a pretty picture. Am J Infect Control. 2007 Sep;35(7):477-80.

33. Kushel MB, Hahn JA, Evans JL, et al. Revolving doors: imprisonment among the homeless and marginally housed population. Am J Public Health. 2005 Oct;95(10):1747-52.

34. Magura S. Validating self-reports of illegal drug use to evaluate National Drug Control Policy: a reanalysis and critique. Eval Program Plann. 2010 Aug;33(3):234-7.

35. Burt MR, Aron LY, Douglas T, et al. Homelessness: programs and the people they serve. Washington, DC: The Urban Institute, 1999. Available at: http://www.urban.org/uploadedpdf/homelessness.pdf.

36. Hahn JA, Kushel MB, Bangsberg DR, et al. Brief report: the aging of the homeless population: fourteen-year trends in San Francisco. J Gen Intern Med. 2006 Jul;21(7): 775-8.

37. Badiaga S, Raoult D, Brouqui P. Preventing and controlling emerging and reemerging transmissible diseases in the homeless. Emerg Infect Dis. 2008 Sep;14(9):1353-9.

38. Pawlotsky JM. The results of Phase III clinical trials with telaprevir and boceprevir presented at the Liver Meeting 2010: a new standard of care for hepatitis C virus genotype 1 infection, but with issues still pending. Gastroenterology. 2011 Mar;140(3):746-54.

39. Marcellin P, Forns X, Goeser T, et al. Telaprevir is effective given every 8 or 12 hours with ribavirin and peginterferon alfa-2a or -2b to patients with chronic hepatitis C. Gastroenterology. 2011 Feb;140(2):459-68 e1; quiz e14.

40. Sylvestre D. Perspective: recognizing resistance. Nature. 2011 Jun;474(7350):S11. [End Page 833]

Additional Information

ISSN
1548-6869
Print ISSN
1049-2089
Pages
811-833
Launched on MUSE
2012-04-25
Open Access
No
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