Section I: Vulnerable populations
Hepatitis C virus and HIV co-infection in people with severe mental illness and substance use disorders
Rosenberg, Stanley D; Drake, Robert E; Brunette, Mary F; Wolford, George L; Marsh, Bryan J
Dartmouth Medical School and Dartmouth College, Lebanon, NH 03756, USA.
Correspondence to Stanley D. Rosenberg, PhD, Dartmouth Trauma Research Interventions Center, 1 Medical Center Drive, Lebanon, NH 03756, USA. Tel: +1 603 653 0740; fax: +1 603 653 0737; e-mail: email@example.com
Objectives: The 5–7% of adults in the United States with severe mental illness (SMI), especially the 50% who are ‘dually diagnosed’ with co-occurring substance use disorders (SUD), are at an elevated risk of HIV and hepatitis C virus (HCV). However, little is known about HIV/HCV co-infection in this population. This paper examines the prevalence and correlates of HIV, hepatitis C, and HIV/HCV co-infection in a large, multisite sample of SMI clients.
Design: We conducted a re-analysis of data on prevalence and correlates of blood-borne infections in a multisite sample of SMI clients.
Methods: In 1997–1998, 755 SMI clients were tested for HIV, hepatitis B virus and HCV, and assessed for demographic, illness-related and other behavioral risk factors for blood-borne infections. The prevalence and correlates of co-infection were examined, as well as the knowledge, attitudes and risk behaviors of individuals with HCV mono-infection.
Results: Of the 755 participants, 623 (82.5%) were negative for both HIV and HCV, 23 (3.0%) were positive for HIV, 109 (14.4%) were positive for HCV, and 13 (1.7%) were co-infected with HIV and HCV. Overall, 2.5% of dually diagnosed participants were co-infected, whereas only 0.6% of SMI participants without a comorbid SUD diagnosis were co-infected. Co-infection was associated with psychiatric illness severity, ongoing drug abuse, poverty, homelessness, incarceration, urban residence and minority status. HCV-mono-infected clients continued to engage in high levels of risk behavior for HIV.
Conclusion: In addition to efforts to identify and treat SMI patients with HIV/HCV co-infection, HCV-mono-infected clients should be targeted for prevention interventions.
Between 5 and 7% of adults in the United States suffer from severe mental illness (SMI) . SMI is defined by a diagnosis of a major mental illness, disability in important life spheres (e.g. school, work or family function), and persistence of illness and disability. The major diagnostic groups making up the SMI population include schizophrenia, schizoaffective disorder, bipolar disorder, and major depressive disorder. These psychiatric disorders are also associated with a heightened risk of substance use disorders (SUD), and individuals with both SMI and SUD, sometimes called ‘dually diagnosed’, are at a highly elevated risk of both HIV and hepatitis C virus (HCV) infection [2–8]. Current estimates of HIV infection for the SMI population range from 3.1 to 8%, and infection prevalence for dually diagnosed clients is generally estimated at more than twice these rates . However, before 2001, there were no published data on HCV co-infection  in the SMI population, and there are still virtually no available data on how co-infected clients differ from uninfected and HIV-mono-infected clients.
Co-infection in this group is of concern not only because it is associated with increased morbidity and mortality [10–12], but also because dually diagnosed, co-infected clients pose unique issues and challenges to providers in relation to detection, assessment and treatment.
Individuals with SMI are at high risk of HIV, hepatitis B and hepatitis C for a variety of reasons: injection drug use, multiple high-risk sexual partners, infrequent condom use, trading sex for material gain, and engaging in sex while using psychoactive substances [13–16]. Elevated rates of infectious hepatitis in psychiatric patients in other countries have been reported [17,18], but there has been a dearth of published information on HCV or HIV/HCV co-infection among individuals with SMI in the United States.
A recent, multisite study, which included urban, small metropolitan and rural sites, found that HIV/HCV co-infection was common in this group . The site-weighted HIV prevalence was 3.1% and HCV prevalence was 19.6%. The metropolitan prevalence of HCV was 25.4%, whereas the non-metropolitan prevalence was 10.6%. Approximately half of the dually diagnosed clients were seropositive for at least one of these infections. Of those clients who acknowledged injecting drugs even once in their lifetimes, closer to two-thirds tested positive for HCV. Two additional recent studies reported the prevalence of HCV among dually diagnosed clients in the range of 30–38% [19,20]. It is thus becoming more evident that many dually diagnosed clients living in high seroprevalence communities, especially injection drug users (IDU), already have chronic HCV infection (prevalence > 60%) .
Given the elevation in risk for both HIV and HCV associated with SUD, it is important to understand this phenomenon better in the SMI population. The Epidemiologic Catchment Area (ECA) study reported a lifetime prevalence of 47% for SUD in individuals with schizophrenia, 56% in individuals with bipolar disorder, and 27% in individuals with major depression . Although alcohol is the most commonly abused substance in patients with SMI [23–25], high-risk drug-related behaviors are frequent. For example, Osher et al.  reported that more than 20% of a large SMI sample reported lifetime intravenous drug use, 14% reported needle sharing, and 57% acknowledged sniffing or snorting cocaine.
SUD complicate the course of illness and treatment of patients with SMI , and are associated with treatment non-adherence, suicidality, hospitalization, homelessness, victimization, violence, jail or prison time, increased risk behaviors for HIV, hepatitis B, and hepatitis C infection, and lower functioning in general [23,28–34]. Moreover, co-occurring SUD are often underdetected and undertreated in mental health settings [35,36], so that clients at risk of blood-borne infection are not generally counseled regarding risk reduction, testing or medical evaluation. This problem is particularly relevant for the high percentage of dually diagnosed clients with chronic HCV, who seem largely unaware of their infection, and who are not receiving regular medical care [8,37].
We re-analysed data from a recently completed risk and seroprevalence study of a large, multisite sample of SMI clients [14,21,26,37,38]. The analyses reported here focused on the subset of participants in the larger study for whom serological testing was available for three blood-borne infections: HIV, hepatitis B virus (HBV), and HCV. This criterion excluded a subset of participants included in reports of the parent study: those receiving non-Department of Veterans Affairs outpatient services in North Carolina. For the present analyses, we also included some subjects for whom data were not yet available at the time of the original reports. The current analysis does not weight data by site, but rather reports absolute frequencies. The data therefore probably underestimate overall infection rates for the target population, because the rural sites had low base rates of HIV and HCV and, compared with national census data, were overrepresented in the sample.
Between June 1997 and December 1998, 777 patients with SMI in Connecticut, Maryland, New Hampshire, and North Carolina were recruited to participate in a risk and seroprevalence study of HIV, HBV and HCV. Participants were between the ages of 18 and 60 years, were fluent in English, and met common criteria for SMI. All participants were recipients of inpatient or outpatient treatment through the public mental health systems of Connecticut (158), Maryland (133), New Hampshire (288), or the Durham, NC, Department of Veterans Affairs (185).
The Connecticut and Maryland samples were drawn from large metropolitan areas known to have a high prevalence of HIV/AIDS and HCV, whereas the New Hampshire and North Carolina participants were drawn from rural and small metropolitan areas, which had much lower estimated population rates of these infections. In North Carolina, subjects were residents of the Piedmont area, where the population was primarily African-American; in New Hampshire, the state population and study participants were more than 95% Caucasian.
Sample demographics and diagnoses (Table 1) are typical of other samples of adults with SMI.
Following informed consent, subjects responded to standardized interviews regarding sociodemographic characteristics, substance use, risk behavior for HIV, HBV and HCV, knowledge and attitudes regarding HIV, history of infectious diseases, healthcare and other illness-related variables. Subjects also received pre-test counseling for HIV/AIDS, and provided blood specimens. The following serological tests were performed by a common laboratory (accredited by the College of American Pathologists): enzyme-linked immunosorbent assays, confirmed by Western blot, for HIV; Abbott Corzyme test (Abbott Laboratories, Abbott Park, IL, USA) for HBV core and Abbott HCV 2 enzyme-linked immunosorbent assays for HCV antibodies, confirmed by recombinant immunoblot assay (RIBA) on a random subset of reactives. Details regarding laboratory analyses of bloods can be found in Rosenberg et al. . All subjects were paid a participation fee of US$35, and were provided with test results and post-test counseling. All subjects with positive serology screens were referred for follow-up testing and treatment with appropriate providers. These procedures were approved by the relevant internal review boards at each participating site.
Details of the measures, including reliability and validity data, have previously been reported [39,40]. To recapitulate briefly, interviewers used standardized questionnaires to elicit information on background characteristics, including sex, age, race, marital status, poverty level, employment status, recent homelessness, and psychiatric/substance abuse diagnoses. We defined ‘homelessness’ as having no regular residence, or living in a shelter or on the street at some point in the past 6 months. To determine the poverty status, we used the 1999 poverty guidelines of the Department of Health and Human Services (based on the 1998 census; Federal Register, 1999) , which take into account income, marital status, and number of children.
Lifetime alcohol and drug use disorders were assessed through the use of the Structured Clinical Interview for Diagnostic and Statistical Manual of Mental Disorders, version IV , or through chart diagnosis. Current alcohol and drug use disorders were identified using the Dartmouth Assessment of Lifestyle Instrument , an 18-item screening tool for SUD (abuse or dependence) specifically developed and validated for patients with SMI. The Dartmouth Assessment of Lifestyle Instrument has high classification accuracy for current SUD of alcohol, cannabis and cocaine in this population.
To assess risk behaviors associated with HIV, HBV and HCV, we used the AIDS Risk Inventory (ARI), a structured interview for assessing risk behaviors associated with acquiring and transmitting these infections [44,45]. The ARI measures risky sexual practices such as unprotected sex (nine items) and risky drug practices (15 items) such as needle sharing. The total risk score is the combined number of risk items endorsed, so that scores can range from 0 to 23 (one item is shared by the sex and drug risk subscales). The ARI also includes items on knowledge and misconceptions regarding HIV/AIDS (eight items), and concerns about the respondent's own risk of infection and intentions to reduce risk (four items).
Clinical, health, and service utilization variables were obtained from The Short Form-12 Health Survey (SF-12) [46,47] and from the Piedmont Health Survey used in the Epidemiologic Catchment Area Survey . The SF-12 assesses two components of health-related quality of life: a mental component summary score and a physical component summary score. The SF-12 is reliable and valid among individuals with SMI . Clinical and physical health indices on the Piedmont Health Survey included the self-reported number of psychiatric hospitalizations in the past year, age of first psychiatric hospitalization, chronic health problems, doctor visits for physical health problems, and days hospitalized for physical health.
We examined rates, risk factors and correlates of HIV and HCV infection and co-infection. These included poverty, homelessness, urban residence, minority status, psychiatric illness-related variables (e.g. diagnosis), specific sexual and drug-related risk behaviors, knowledge of and attitudes towards HIV risk, SUD, healthcare utilization and incarceration [14,26]. As the initial reports from this dataset focused primarily on the rates and correlates of mono-infection, the focus of the analyses reported here is on characterizing the co-infected clients compared with the uninfected, and with the HIV and HCV-mono-infected participants. In addition, because those with chronic HCV infection are at continuing risk of developing superinfection if they contract HBV, potentially leading to fulminant liver failure or an accelerated rate of progression to liver disease, we report on HBV infection. Because the numbers are small and the cell sizes skewed, we report frequencies and descriptive data, but do not test group differences for statistical significance. We estimate that a sample of at least two to five times larger (depending on the specific variable) than the current dataset would be required for adequate power for hypothesis testing. Given the small number of co-infected individuals in this study, the results serve as a basis for preliminary description and hypothesis generation rather than a source of conclusions on the problem of co-infection in individuals with SMI and dual disorders.
From the total sample of 777 participants, 22 records had one or more missing laboratory result for HIV, HCV or both. We thus had complete serostatus data on 755 individuals for analyses. Approximately 87% of patients approached consented to participate in the assessments. The prevalence results were as follows: neither HIV nor HCV infection: 623 (82.5%); HIV infection: 23 (3%); HCV infection only: 109 (14%); co-infection of HIV and HCV: 13 (1.7%); HBV infection: 141 (19%); co-infection of HBV and HCV: 56 (7.4%).
Of those with HIV infection, 13 (57%) were also co-infected with HCV, and 10 of these co-infected participants also tested positive for HBV. This compares with an estimated rate of HCV co-infection of 25% for all HIV-positive individuals living in the United States, and an estimated rate of 70–90% of HIV-positive IDU.
Key demographic, diagnostic, substance abuse and other risk variables are shown in Table 1.
Table 1 shows that the HIV/HCV co-infected group appear to be characterized, compared with the sample as a whole, by female gender, urban residence, and minority status. Ten of the 13 co-infected participants were recruited from the two largest cities in the sample, even though these sites provided less than one third of the participants. In addition, the co-infected have many characteristics indicative of psychiatric illness severity and chronicity, including: a higher percentage had schizophrenia diagnoses (the most severe and disorganizing of psychiatric disorders); a young average age of onset; a higher number of previous hospitalizations; by far the lowest reported income of any subgroup; higher reported rates of homelessness; more limited average educational level; higher rates of incarceration; the higher rates of current and lifetime drug use disorders; and more ongoing drug risk behaviors. Again, we did not test these differences for statistical significance.
An alternative way of looking at the relationship between substance abuse and co-infection is as follows: 2.5% of the dually diagnosed participants (n = 448) were co-infected with HIV and HCV, whereas among the SMI participants with no SUD (n = 329), only 0.6% were co-infected. The co-infected participants reported the poorest physical health of any group, and appeared to be less likely to have a regular doctor or source of medical care than HIV-mono-infected participants. Somewhat surprisingly, co-infected individuals were similar to the other subgroups in their use of medical inpatient services during the previous 6 months. Finally, the co-infected clients had the worst scores regarding knowledge about HIV of any sub-group, and the most misconceptions about the infection.
The HIV-mono-infected clients contrasted with the co-infected in a number of ways. This group is more male dominated, younger, and less urban. Like the co-infected they tended to be of ethnic minority status (70%) in comparison with the sample as a whole (47.7%). In terms of psychiatric illness indicators, they are characterized by less severe diagnoses, the highest age of onset, the lowest number of previous hospitalizations, much higher income than the co-infected (close to the sample average), by far the lowest rates of homelessness, better educational backgrounds, much lower rates of current and lifetime drug use disorders, and lower current drug risk behaviors. In most respects, they seem to have the least psychiatric morbidity of any subgroup.
The HCV-infection-only group is of interest because they are by far the largest infection group, and the group at highest risk of developing co-infection. As shown in Table 1, clients with HCV mono-infection share many characteristics with currently co-infected clients and contrast sharply in a number of ways with the HIV mono-infected. They are the oldest subgroup, are predominantly urban, but (in contrast with the currently co-infected) are largely a male-dominated group. HCV mono-infected clients have relatively high rates of schizophrenia diagnoses, multiple previous psychiatric hospitalizations, high rates of homelessness and incarceration (over 90% lifetime), as well as current and lifetime drug use disorders. Despite the health risks inherent in such behavior, they also have high rates of current alcohol use disorder. Perhaps equally critical, they have relatively low levels of AIDS concern, and show the highest overall level of risky behaviors for HIV.
Clients with HCV mono-infection reported the following high-risk sexual behaviors for HIV in the previous 6 months: 38.3% reported engaging in unprotected sex; 10.8% reported engaging in unprotected anal sex; 10.8% reported having two or more sexual partners; 5.6% reported unprotected sex with known IDU; and 3.8% reported trading sex for drugs without condom use. Risky drug practices, including acts that put others at risk of contracting HCV, were also fairly common in the previous 6 months. Of the HCV-mono-infected clients, 8.3% reported needle use, 4.6% reported sharing needles (including the use of dirty needles), and 49.3% reported engaging in two or more risky sex or drug behaviors.
The data presented in this paper must be interpreted with caution because of the nature of the sampling procedure (non-random, geographically limited) and the small number of participants in two key groups: the co-infected and the HIV mono-infected. The latter factor did not permit statistical analyses, and delimits confidence in the generalizability of our findings. Clearly, larger studies employing nationally representative, random sampling procedures with SMI and dually diagnosed participants will be needed to gain greater clarity.
These caveats notwithstanding, the HIV/HCV-co-infected individuals in this study were extremely disadvantaged, disorganized, and ill. They were impaired by the most severe psychiatric and drug problems, and were highly likely to be dually diagnosed with both schizophrenia and drug use disorders. Women may have been overrepresented in the co-infected group because drug-dependent women with SMI must often resort to sex trading for drugs and housing, and are at high risk of sexual victimization . For both men and women with dual disorders, their low levels of education, income, psychosocial supports, and insight suggest that they will be difficult to engage and treat successfully [50–55].
Whereas there are almost no systematic published data on patients with both dual disorders (SMI plus substance abuse) and HIV/HCV co-infection, available findings suggest that dually disordered individuals with HCV infection are also less likely than those without HCV to receive regular medical care . In general, patients with dual disorders do not adhere to treatment, or do not engage in care at all when both the mental illness and the SUD are not addressed together. Patient-related barriers to medical care include cognitive, social support, transportation access and social skills deficits, symptoms of disorganization, avoidance or paranoia [57,58], as well as minority status and residence in poor neighborhoods. In addition, medical providers often consider individuals with mental illness difficult to treat and poor risks for treatment . An inability to pay for care as a result of unemployment, poverty, and poor insurance further reduces access to medical care . The net result is that this group receives little or inadequate medical attention [59,61].
Integrated mental health and substance abuse treatment, developed in response to these barriers and disparities, involves treatment by the same team in the same location [62–64]. Integrated dual diagnosis treatment is recommended by numerous federal and professional organizations. More recently, systematic efforts to integrate physical healthcare with mental health and substance abuse treatment have also been tested. The approach that has demonstrated the greatest effectiveness for improving access to medical care for individuals with SMI involves integrating a primary medical care provider within the mental health agency , or alternatively, integrating a mental health specialist within the primary care setting . In the integrated treatment model, the medical provider becomes part of the mental health team and handles screening, prevention, routine medical care, referral to specialists, and medical follow-up for all non-psychiatric medical conditions. The available evidence thus suggests that special programs of outreach, (including emphasis on tailoring outreach to minority communities), integrated mental health, substance abuse, and public health services; and perhaps special residential programs, will probably be needed for successful medical intervention with dually diagnosed co-infected patients.
The results presented here are congruent with the suggestion of Graham and Koziel  that being positive for both HIV and HCV is likely to be a marker for multiple problems and treatment barriers associated with injection drug use. The issues include poor access to medical care and a chaotic lifestyle, which may both delay access to care as well as affect the type of care received. Such problems are likely to be compounded in clients with pre-existing SMI and co-occurring substance abuse, and may have a significant impact on disease progression in co-infected patients. It has already been shown in the general population that injection drug use itself is a predictor of progression to an AIDS-defining illness . Furthermore, in a study comparing disease progression in HIV-positive/HCV-positive individuals versus HIV-positive individuals , co-infected individuals initiated highly active antiretroviral therapy later and had lower CD4 cell counts at initiation than mono-infected patients. Although it is vital to treat these clients, they currently fail even to access a consistent source of medical care. Clearly, the first steps for these clients will include more effective education about blood-borne infections; enhanced risk-reduction interventions, including interventions to reduce secondary risks, interventions directed at alcohol and drug abuse, and motivational enhancement to participate in and adhere to medical care. In reality, the service delivery system in this country is not well prepared to manage and treat these clients, with few providers being optimistic or comfortable with combining treatments for HIV and HCV, particularly when such contraindications as current alcohol or drug use and persistent psychiatric symptoms are present. Medical providers also have difficulty accessing necessary psychiatric consultation and collaboration in managing these patients .
In general, issues of illness management, costs, and provider burden for co-infected SMI and dually diagnosed clients are currently unknowns. However, they represent potentially daunting barriers to care. For example, recent findings suggest that annual service costs for Medicaid recipients with SMI and HIV mono-infection (excluding pharmacy costs) are US$13 800, versus US$5800 for comparable, uninfected clients with SMI . Changes in policy, funding, provider training and in the organization and coordination of services will be necessary to address the needs of these complex patients, and will require new models of disciplinary collaboration.
In terms of overall numbers and the potential to prevent co-infection and expensive treatments, the HCV infection group appears to be a critically important target. These individuals not only have multiple impairments and disadvantages, like the co-infected group, but they are also highly involved in behaviors that put them at risk of acquiring HIV co-infections. The results presented in this report are also consistent with findings from another recently completed study with similar participants (unpublished data). In that study, SMI respondents with HCV mono-infection reported the least concern of any sub-group about contracting HIV infection, and low intentions to increase personal safety. Despite their high-risk lifestyles, the majority reported never having been tested for HIV, having been tested only once, or not knowing if they had ever been tested. The data from this study suggest that dually diagnosed clients who are currently HCV mono-infected are at high risk of progressing to co-infection status, and that, in continuing their abuse of drugs and alcohol, they are also at risk of more rapid illness progression and liver deterioration. It thus appears important to provide these clients with integrated mental health, substance abuse, and public health treatments, residential supports, and HIV prevention interventions.
The authors acknowledge the contributions of the members of the 5 Site Health and Risk Study Research Committee. Connecticut: Susan M. Essock, Jerilynn Lamb-Pagone; Duke: Marvin Swartz, Jeffrey Swanson, Barbara J. Burns; Durham: Marian I. Butterfield, Keith G. Meador, Hayden B. Bosworth, Mary E. Becker, Richard Frothingham, Ronnie D. Homer, Lauren M. McIntyre, Patricia M. Spivey, Karen M. Stechuchak; Maryland: Fred C. Osher, Lisa A. Goodman, Lisa J. Miller, Jean S. Gearon, Richard W. Goldberg, John D. Herron, Raymond S. Hoffman, Corina L. Riismandel; New Hampshire: Patricia C. Auciello, Kim Mueser, Mark C. Iber, Ravindra Luckoor, Gemma R. Skillman, Rosemarie S. Wolfe, Robert M. Vidaver, Michelle P. Salyers.
Sponsorship: This research was supported by NIMH Grant R01-MH50094-03S2, Identifying Substance Abuse Disorders in the Mentally Ill (HIV supplement); NIMH Grant P50-MH43703, Center for Research on Services for Severe Mental Illness; NIMH Grant R01-MH48103-05, Effectiveness of Involuntary Outpatient Commitment; NIMH Grant P 50-MH51410-02, UNC-CHJ Duke Program on Services Research for People with Severe Mental Disorders; NIMH Grant R24-MH54446-05, CT DMH-Yale Medication Effectiveness Research Program; NIMH Grant R01-MH52872, Assertive Community Treatment for Dually Diagnosed Clients; and V A ERIC Grant EPP97-022 HIV Seroprevalence and Risks in Veterans with Severe Mental Illness.
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Co-infection; dual disorders; hepatitis C virus; HIV; severe mental illness
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