In the United States, up to 300 000 individuals are infected with both HIV and hepatitis C virus (HCV), representing 25–30% of all HIV-infected individuals and 5–10% of all HCV-infected individuals [1,2]. Co-infection complicates the management of each infection and appears to affect the clinical course of each infection adversely . In addition, co-infection often coexists with other conditions and patient factors, some of them related to shared risk factors, which further complicate the management of both infections. The use of highly active antiretroviral therapy has led to a marked decline in most HIV-related opportunistic illnesses and a marked decline in deaths from HIV [4–6]. With these improvements in HIV care, the remaining comorbidities, including drug abuse, alcohol abuse, and severe mental illness have emerged as continuing factors that make such co-infected patients particularly vulnerable to poor health outcomes.
The Department of Veterans Affairs (VA) is the largest single provider of healthcare services in the United States to individuals with HIV  and to those with HCV . Over 19 000 patients with HIV and over 180 000 with HCV received care in the VA in 2002. We present basic patient demographic and clinical characteristics of HIV-infected and HIV/HCV-co-infected patients receiving care in the VA, with a focus on those patient factors that may place such patients at an increased risk of poor health outcomes.
The data source is the Immunology Case Registry (ICR), which has been described in detail elsewhere . In brief, in 1992 the VA established the ICR as an active registry of identified HIV-positive patients who receive care in the VA system. Each HIV-positive patient is entered manually onto a local registry list by a designated ICR coordinator. For patients on the local list, the ICR software extracts designated data fields from the VA's electronic medical record and transmits the extract nightly to the national ICR. The designated fields pertain to all VA care, and include data on inpatient diagnoses, laboratory test results, outpatient diagnoses and outpatient prescriptions. Data are transmitted nightly from all VA healthcare medical centers that represent the VA's approximately 160 hospitals, 850 community clinics, 130 nursing homes, and 40 residential facilities. As of 2003, the ICR included data on more than 54 000 HIV-positive patients who have been treated in the VA since 1992.
For this analysis, patients who were entered into the ICR before October 2003 with healthcare utilization between 1 January 2002 and 31 December 2002 were evaluated.
Non-veterans occasionally receive care at the VA in the course of humanitarian care, research studies or special programs. They were excluded from this analysis because they fall outside the main VA mission of caring for veterans, and consequently tend to have sporadic or minimal follow-up care at the VA.
HCV serostatus was determined by the presence ever of a HCV enzyme immunoassay antibody test result that was interpretable as positive or negative. Patients who were never tested and patients who had uninterpretable test results, such as ‘indeterminate’ or ‘quantity not sufficient’ were excluded. Patients who had both positive and negative HCV antibody results were classified as HCV seropositive.
Patient age was determined as of 1 January 2002. Race/ethnicity was categorized as black, Hispanic, other/unknown or white. The first period of military service was measured as a patient's chronologically earliest period of military service using VA designations of military service eras. Patient entry into the ICR was defined as the date of the first transmission of the patient's data to the national registry. We identified the VA medical center caring for the patient at the initial entry into the ICR. On the basis of the state in which a medical center was located, the medical center was assigned to one of four regions of the country as defined by the Centers for Disease Control and Prevention (CDC): northcentral, northeast, south and west .
A patient was considered to have had clinical AIDS if the patient had a recorded date of an AIDS-defining opportunistic infection (OI) on or before 31 December 2002. Dates of the first AIDS OI for patients are manually entered into the ICR, with such illnesses defined in the 1993 CDC AIDS surveillance case definition . VA medical centers have an incentive to enter this information into the ICR as they are eligible for a higher level of reimbursement for patients who have clinical AIDS.
We examined the rates of five comorbidities (mental health illness, depression, alcohol abuse, substance abuse and hard drug abuse) that are common among patients with HCV and HIV and that make such patients particularly vulnerable to poor health outcomes. Indicators of the presence of these comorbidities were based on VA inpatient and outpatient International Classification of Diseases, 9th Revision (ICD9) codes. Computerized diagnosis coding of VA inpatient hospitalizations is available from 1992, whereas computerized diagnosis coding of VA outpatient visits began in 1996. A patient was categorized as having a mental health illness excluding alcohol abuse and substance abuse if the patient had been assigned a mental health ICD9 code (304 ICD9 codes) at any time to the end of 2002 (see the Appendix for lists of the specific ICD9 codes). Within this group, we also identified the subset of patients who had ever received any of 29 ICD9 codes indicating depression, including bipolar disorder with depressive features. A patient was categorized as having a history of alcohol abuse if the patient had an ICD9 code for alcohol abuse or for a complication of excess alcohol use such as alcoholic dementia (42 ICD9 codes). A patient was categorized as having a history of substance abuse excluding alcohol if the patient had any of 215 substance abuse codes related to amphetamine, antidepressant, barbiturate, cannabis, cocaine, hallucinogen, opioid, unspecified and mixed drug abuse. A patient was categorized as having a history of hard drug abuse if the patient had any of 82 ICD9 codes related to amphetamine, cocaine or opioid abuse.
Measures of comorbidities based on diagnoses, however, may not be independent of treatment, and the effect of treatment on health is likely to differ from the effect of the cofmorbidity itself. Mindful of this lack of independence, we also developed a measure of a history of injection drug use based on data on HIV risk behavior. This variable was not available for the entire cohort. HIV risk behavior was entered manually at patient entry onto the ICR until April 1999 using the exposure categories of the CDC . We collapsed these categories to identify those patients who reported injection drug use as a risk factor for HIV.
We developed two measures concerning pharmacological treatment for HIV and HCV, respectively. We developed an indicator for whether the patient had a VA prescription for any US Food and Drug Administration-approved HIV antiretroviral medication in 2002. We also investigated whether patients ever received medications active against HCV. We developed an indicator for whether a patient ever received a VA prescription for IFN-α, IFN-α combined with ribavirin, pegylated interferon or ribavirin. It is possible that patients received interferon for indications other than HCV, such as Kaposi's sarcoma and other hematological malignancies. We could not determine the indication for the prescription from the present data.
Our measure of mortality was death from any cause reported in the ICR. Deaths before 1 October 2003 were included in this report.
We used bivariate analyses to compare the characteristics of the HIV and HIV/HCV-co-infected groups. Categorical variables, such as sex and race/ethnicity, were compared using the Pearson chi-square test. Continuous variables, such as age, were compared using the Wilcoxon rank-sum test. All tests were two-sided, and P values less than 0.05 were considered to be statistically significant. Data were analysed using SAS software, version 8.2 (SAS Institute, Cary, NC, USA) and the S-PLUS version 6.1 (Insightful Corporation, Seattle, WA, USA).
Of 19 878 HIV patients who received VA healthcare in 2002, 19 576 (98.4%) were veterans. Of these HIV-infected veterans, 18 402 (94.0%) had a recorded HCV antibody test at any time and 18 349 (93.7%) had an interpretable result. The demographic characteristics of these 18 349 veteran patients are shown in Table 1. A total of 6782 (37.0%) were HCV seropositive. For most of the demographic and clinical variables investigated, the difference between the HIV/HCV-co-infected and the HIV-only-infected groups was statistically significant. With such a large sample size, however, small differences that may not be clinically meaningful are often statistically significant.
Compared with HIV-alone-infected patients, HIV/HCV-co-infected patients were slightly older, more likely to be male, more likely to be black or Hispanic, and more likely to have begun their military service in the Vietnam era. Co-infected patients were more likely to have received care in the northeast. Among the 8914 patients for whom the HIV exposure category was available, co-infected patients were much more likely to report intravenous drug use as a risk behavior for HIV acquisition compared with patients with HIV alone (73.3 and 9.5%, respectively, P < 0.0001).
The clinical comorbidities and other clinical characteristics of the 18 349 patients are shown in Table 2. HIV/HCV-co-infected patients were much more likely to have diagnoses of mental health illness, depression, alcohol abuse, substance abuse and hard drug abuse when compared with HIV-alone-infected patients. Co-infected patients were actually less likely to have had an AIDS OI compared with patients with HIV alone. Co-infected patients were also less likely to have received antiretroviral medications for their HIV infection from the VA in 2002. Of note was the fact that co-infected patients had on average been entered into the ICR earlier than HIV-alone patients, indicating that on average the co-infected patients had been in VA care for their HIV disease longer than those patients infected with HIV alone. HCV genotype data were available for 2611 (38.5%) of the HIV/HCV-co-infected patients who were in VA care in 2002: 86.6% had HCV genotype 1, 6.8% genotype 2, 5.8% genotype 3 and 0.8% genotype 4.
Finally, before 1 October 2003, of the 18 349 patients who had been in VA care at some point in 2002, 1322 (7.2%) had died. HIV/HCV-co-infected patients were more likely to have died than those patients infected with HIV alone.
The US VA is the largest single provider of integrated healthcare to individuals with HIV infection, HCV infection and HIV/HCV co-infection in the United States. Data from the VA ICR from 2002 showed a high rate of HCV co-infection among HIV patients. The VA HIV and HIV/HCV-co-infected population had very high rates of additional comorbid conditions that complicate both the pharmacological therapy and clinical course of both HIV and HCV infections.
Both the HIV and the HIV/HCV-co-infected population had very high rates of mental health illness, and particularly depression. Having mental health illness puts the HIV and the HIV/HCV-co-infected patient at an increased risk of poor health outcomes through both direct (e.g. suicide) and indirect (e.g. impaired medication adherence, provider reluctance to prescribe complex medication regimes) mechanisms. Mental health illness is thus associated with shortened survival in general [13,14].
In the case of HCV, the currently approved drug therapy to treat this infection includes IFN-α, which has depression and suicidal behavior as major side-effects (package inserts for IFN-α2a and 2b). Depression occurs in 16–29% of interferon-treated patients and anxiety or emotional lability occurs in 3–34% . In addition, several reports have suggested that patients with psychopathological symptoms before starting interferon therapy may have more severe adverse psychiatric effects in response to treatment [16,17], although other groups believed that patients with a psychiatric diagnosis can successfully complete interferon therapy [18,19]. The high prevalence of a psychiatric diagnosis, and particularly the high rate of depression in HCV-infected patients thus poses an additional challenge, because IFN-α products may exacerbate or precipitate mental health illness, particularly depression. In addition, given the controversy about the tolerability of interferon treatment in patients with mental health illness, providers may be reluctant to offer HCV treatment to such patients. The high rates of mental health illness might thus contribute to the observed low rate of pharmacological treatment for HCV in HIV/HCV-co-infected patients.
In addition, the HIV/HCV-co-infected population had markedly elevated rates of alcohol abuse compared with the HIV-alone-infected population. Alcohol abuse appears to speed the clinical course of HCV infection and thus makes such co-infected patients particularly vulnerable to poor health outcomes from HCV infection. The chronic consumption of moderate to large amounts of alcohol in HCV patients increases the rate of liver fibrosis [20,21], cirrhosis [22–25], hepatocellular carcinoma [22,23,26], and probably death [27,28]. Alcohol consumption appears to have the same negative effects on the clinical course of HCV in HIV/HCV-co-infected patients, in whom alcohol consumption increases the rate of liver fibrosis [29–31], cirrhosis [29,32], and death from liver disease .
Finally, the HIV/HCV-co-infected population had markedly elevated rates of substance abuse, and particularly hard drug abuse compared with the HIV-alone-infected population. Substance users are at high risk of poor health outcomes through a variety of mechanisms. Drug use itself places these patients at risk of overdose and other direct drug-related toxicities (e.g. endocarditis, skin and soft tissue infections). In addition, substance users are at a high risk of poor health outcomes through indirect mechanisms, such as reduced access to healthcare, poverty, and reluctance by providers to begin complex or lengthy medication regimes such as those required by effective HIV antiretroviral therapy or HCV antiviral therapy.
Interestingly, HIV/HCV-co-infected patients had been in VA care for their HIV disease longer than those patients infected with HIV alone, but were less likely to have had an AIDS OI documented and to have received HIV antiretroviral medications. One possible explanation for these findings is that co-infected patients enter VA HIV care earlier in the course of their HIV disease, before the development of an AIDS OI and before an indication for antiretroviral medications. This may occur because of the earlier detection of HIV infection in the HIV/HCV co-infected. Many alcohol and substance abuse treatment programs routinely screen for HIV infection. HIV/HCV-co-infected patients, with their high rates of alcohol abuse and substance abuse, are more likely to be enrolled in such programs, and thus may have their HIV infection detected earlier. Alternatively, given their high rates of comorbidity, HIV/HCV-co-infected patients may be less likely to have access to other sources of medical care, and thus, once diagnosed with HIV, may present to the VA earlier in the course of their HIV disease for continued HIV care. Future research is needed to try to explain these findings.
To complicate HCV management further, the VA co-infected population has high rates of HCV genotype 1. The currently recommended combination of pegylated interferon and ribavirin has a generally lower success rate in HIV/HCV-co-infected patients with this genotype [33,34]. Future pharmacological innovations for the treatment of HCV will thus hopefully both improve the side-effect profile so that the treatment can be tolerated by the co-infected population and improve the response rates of the dominant genotype 1.
Our very preliminary data on mortality suggests an increased death rate among the HIV/HCV co-infected compared with those patients infected with HIV alone. Similar findings have been noted by some [35,36], but not all, other groups that have examined this issue in various cohorts [37,38]. Determining the cause of any mortality difference will be complicated by the differences in multiple patient characteristics, each of which may contribute to increased mortality through a variety of means. As noted above, the higher rates of comorbidities among HIV/HCV-co-infected patients may account for any increased mortality through either the direct effects of the comorbidity such as drug overdose or through indirect effects such as impaired medication adherence. Clearly, this ultimate outcome warrants much more extensive analysis to try to understand the findings and the determinants.
Our analysis has several limitations related to the reliance on ICD9 codes. Some ICD9 diagnoses, such as alcohol abuse, do not specify criteria, so different providers may assign the code for differing levels of alcohol consumption. This lack of standard criteria, particularly for alcohol abuse, also means that we cannot determine how these patients’ levels of alcohol consumption compare with the categories of alcohol ingestion used in studies on the effect of alcohol on the clinical course of HCV. The assignment of an ICD9 code also does not necessarily indicate on-going behavior because of both provider practice and the present study design. Providers may assign a diagnosis code for past patient behavior. In addition, we used the record of an ICD9 code at any time to indicate a history of the disorder, which again may not reflect a current patient condition.
The very high rates of comorbidities observed in the VA population underscore the complexities in screening, testing, and treatment for HIV, HCV and HIV/HCV co-infection among individuals with alcohol abuse, substance use, and mental health diagnoses. Future clinical resources must be given to expanding and improving the treatment for substance use and mental health illness as part of HIV and HCV prevention, screening and testing. Aggressive approaches to risk reduction, prevention and testing for other chronic viral infections must be implemented for individuals with substance use and mental health co-morbidities who are mono-infected with either HIV or HCV to prevent new co-infections. Finally, research and resources need to be invested to minimize fragmented care for these separate but highly interrelated conditions. Optimal models of integrated care need to be developed for populations with HIV, HCV, and HIV/HCV co-infection and those who need substance abuse or mental healthcare.
Special thanks go to all the VA facility ICR coordinators without whom none of this work would be possible.
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Mental health illness ICD9 codes: 290.xx Senile and presenile organic psychotic conditions; 293.xx Transient organic psychotic conditions; 294.xx Other organic psychotic conditions (chronic); 295.xx Schizophrenic disorders; 296.xx Affective psychoses; 297.xx Paranoid states (delusional disorders); 298.xx Other non-organic psychoses; 300.xx Neurotic disorders; 301.xx Personality disorders; 302.xx Sexual deviations and disorders; 307.xx Special symptoms or syndromes, not elsewhere classified; 308.xx Acute reaction to stress; 309.xx Adjustment reaction; 310.xx Specific non-psychotic mental disorders caused by organic brain damage; 311 Depressive disorder, not elsewhere classified; 312.xx Disturbances of conduct, not elsewhere classified; 316.xx Psychic factors associated with diseases classified elsewhere.
Depression ICD9 codes: 296.2x Major depressive disorder, single episode; 296.3x Major depressive disorder, recurrent episode; 296.5x Bipolar affective disorder, depressed; 296.80 Manic-depressive psychosis, unspecified; 296.82 Atypical depressive disorder; 296.89 Manic-depressive psychosis, other; 298.0 Depressive-type psychosis; 300.4 Neurotic depression; 309.0 Adjustment reaction – brief depressive reaction; 309.1 Adjustment reaction – prolonged depressive reaction; and 311 Depressive disorder, not elsewhere classified.
Alcohol abuse ICD9 codes: 291.xx Alcoholic psychoses; 303.0x Acute alcoholic intoxication; 303.9x Other and unspecified alcohol dependence; 305.0x Alcohol abuse; 357.5 Alcoholic polyneuropathy; 425.5 Alcoholic cardiomyopathy; 535.3x Alcoholic gastritis; 571.0 Alcoholic fatty liver; 571.1 Acute alcoholic hepatitis; 571.2 Alcoholic cirrhosis of liver; 571.3 Alcoholic liver damage, unspecified; 790.3 Excessive blood level of alcohol; 980.0 Toxic effect of ethyl alcohol; 980.8 Toxic effect of other specified alcohols; 980.9 Toxic effect of unspecified alcohol; E860.0 Accidental poisoning by alcohol, not elsewhere classified – alcoholic beverages; E860.1 Accidental poisoning by alcohol, not elsewhere classified – other and unspecified ethyl alcohol and its products; E860.9 Accidental poisoning by alcohol, not elsewhere classified – unspecified alcohol, and V11.3 Personal history of alcoholism.
Substance abuse ICD9 codes: 292.xx Drug psychoses; 304.xx Drug dependence; 305.2x Cannabis abuse; 305.3x Hallucinogen abuse; 305.4x Barbiturate and similarly acting sedative or hypnotic abuse; 305.5x Opioid abuse; 305.6x Cocaine abuse; 305.7x Amphetamine or related acting sympathomimetic abuse; 305.8 Antidepressant-type abuse; and 305.9x Other, mixed, or unspecified drug abuse.
Hard drug abuse ICD9 codes: 304.0x Opioid-type dependence; 304.2x Cocaine dependence; 304.4x Amphetamine and other psychostimulant dependence; 304.7x Combinations of opioid-type drug with any other; 305.5x Opioid abuse; 305.6x Cocaine abuse; and 305.7x Amphetamine or related acting sympathomimetic abuse.
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