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Journal of the International Association of Physicians in AIDS Care - Vol. 1, No. 1, January/March 2002
Renslow Sherer, MD;*† Joseph Pulvirenti, MD;* Kim Stieglitz, RN, DNSc;* Jyothi Narra, MD;* John Jasek;* Lynn Green, BA;* Billie Moore;* Susan Shott, PhD;† and Mardge Cohen, MD*
The CORE Center (formerly The Cook County HIV Primary Care Center), Cook County Hospital, and Rush Medical College, Chicago, Illinois
Supported in part by Contract # 250-OA-13(8), US Health Resource and Service Administration, March 13, 2000.
Background: Reduction in HIV-related morbidity and mortality in the highly active antiretroviral therapy (HAART) era has been unevenly distributed in the United States, and its impact on hospitalizations in urban minority populations in the public sector has been poorly characterized.
Methods: We conducted a retrospective analysis of clinical and administrative data sets of an urban public hospital HIV clinic from 1997 and 1998 to identify the correlates of hospitalization early in the HAART era.
Results: 2,647 unduplicated HIV-infected patients were seen in 1997 and 1998 at the CORE Center. There were 31.7 percent women, 71 percent African-Americans and 12 percent Hispanics, and the mean age was 38 years. Men who had sex with men (MSM), injection drug users (IDU), and heterosexuals each made up one third of the population. A majority of the patients had no health insurance, and 27 percent had Medicaid. The median CD4 T cell count was 266 cells/µL, and the median viral load was 1,901 copies/ml. Hospitalizations declined significantly from 1997 (1,579) to 1998 (1,160). Admissions were confined to 25 percent of clinic patients, and 16 patients (range 8-15) had eight or more admissions. African-Americans and Hispanics had significantly more and longer hospitalizations than whites, but there was no difference by gender. IDUs had significantly more admissions than non-IDUs (28 percent vs. 21 percent respectively). On multivariate analysis, lower CD4 T cell count and higher viral load predicted risk of admission in all periods. Unexpectedly, hospitalization rates were high in patients in the highest baseline CD4 T cell stratum, >500 cells/ml (45 of 353, 13 percent), and lowest viral load stratum, <500 copies/ml (103 of 675, 15 percent), and rose from 1997 to 1998. HAART (ie, 1 or 2 drug regimens) predicted fewer hospitalizations compared to 1 or 2 drug regimens. In a subset of patients who filled prescriptions on site, HAART increased from 72 percent to 85 percent and 1-2 drug regimens fell from 28 percent to 15 percent from 1997 to 1998. Regular care was associated with more frequent hospitalization and more hospital days per admission than no regular care. Hospitalized patients had significantly higher mortality than patients not hospitalized (12 percent vs. 2 percent respectively).
Conclusion: HIV-related hospitalizations were frequent in the HAART era and decreased over time. Older age, lack of HAART, lower CD4 T cell count, higher viral load, and minority race predicted hospitalization, while gender did not. However, patients with extremely favorable CD4 T cell and viral load counts also had higher than expected hospitalization rates. Three quarters of patients had no hospitalizations, and clustering of hospitalizations in a small number of patients may enable targeted programs to reduce recidivism.
Reduction in human immunodeficiency virus (HIV)-related morbidity and mortality in the era of highly active antiretroviral therapy (HAART), or the concomitant use of three or more drugs, has been unevenly distributed in the United States, with fewer gains in women, minorities, injection drug users, and persons without health insurance.1 Similar disparities have been reported in HIV ambulatory care outcomes in primary care settings in the US.2,3 In contrast, mortality from acquired immunodeficiency syndrome (AIDS) in Chicago declined 65 percent overall from 1995-1997 with no significant difference by race, gender, age, or history of drug use.4
The impact of the reduction in morbidity and mortality on hospitalizations in urban minority populations has been incompletely characterized to date. Progress in HIV care in the pre-HAART era may be an important consideration in this regard. Sherer et al reported marked reduction in hospitalizations and in-hospital mortality at Cook County Hospital from 1992 to 1997.5 Notably, the observed decline began in 1994, two years before the HAART era. Decline in mortality which preceded the HAART era was also reported in 1998 by the New York City Health Department.6 Between 1996 and 1998, several reports from the HAART era have shown dramatic reduction in overall hospitalizations as well as reduction in HIV-related morbidity and mortality.7,8 More recently, several groups have noted a plateau effect due to relative increase in hospitalizations for non-HIV related reasons, such as drug toxicity, chronic liver disease, and non-HIV associatedneoplasia.9 For example, Ahmad et al recently reported that, at Cook County Hospital from 1998 to 2000, 38 percent of deaths in in-patients were from non-HIV related causes, and one half of the deaths occurred while plasma viral load was undetectable.10 Other groups have reported a disproportionate increase in hospitalizations from non-HIV related causes in women and minorities.11
It is clear that the interactions of morbidity, mortality, and hospitalizations due to HIV disease remain complex in the HAART era and vary across various demographic groups. In order to identify predictors of public hospitalization in the HAART era, we investigated hospitalizations during 1997 and 1998, a period of well-documented decline in HIV-related morbidity and mortality in Chicago, in a cohort of patients who receive primary care at Cook County Hospital, the only public hospital in Chicago.
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We examined databases of the HIV Primary Care Center, now named the CORE Center, in order to conduct an observational, retrospective study of all patients enrolled in HIV primary care in 1997 and 1998. This setting will be referred to as the Center. Data collected included patient related information, primary care attendance, and whether they received ancillary services. The methodology used has been described previously.12 The study population consisted of all adults served by the Center in 1997 and 1998, including those new to care during this time. Unique patient identification unit numbers were used to identify the cohort across all services and databases. From January 1997 through September 1998, the Center was located at the Human Retroviral Disease Clinic (HRD), a 2,000 square foot portion of the Radiation Center of the Fantus Health Center of Cook County Hospital. From October 1998, it was located at the CORE Center, a 74,000 square foot freestanding ambulatory facility for HIV and related infectious diseases.
Outcome variables were mortality, hospitalizations, clinic visits, CD4 T cell counts, and viral loads. For patients enrolled in care prior to 1997, baseline CD4 cell counts were used from the last two months of 1996. Hospitalization data were limited to admissions to Cook County Hospital, as data on admissions to other hospitals were not available for the whole cohort. Data on reasons for discharge and discharge diagnoses were not available for this analysis.
All patients were analyzed in six-month time periods (periods 1-4) from their entry into care, or from January 1, 1997 for patients enrolled in care before 1997. Follow up for clinical care was through December 31, 1998, while follow up for mortality and retention in care was extended through December 31, 1999. This study was approved by the Cook County Scientific Committee, which is the Institutional Review Board of Cook County Hospital.
Pharmacy records were analyzed for the subset of patients who regularly filled prescriptions at the Cook County Hospital Pharmacy during 1997-8. Patients on three or more antiretroviral drugs were categorized as receiving HAART, and those on one or two drugs as receiving antiretroviral therapy (ART). Aggregate data on treatment for the entire cohort, including patients on no therapy, were not available for this analysis.
SPSS for Windows (V 7.5) was used for data management and statistical analyses. Bivariate relationships between variables were investigated using the chi-square test of association for nominal variables and non-parametric Spearman correlations for non-nominal, statistically non-normal variables. Comparisons of groups with respect to non-nominal, statistically non-normal variables were done with the nonparametric Kruskal-Wallis and Mann-Whitney tests. A 0.05 significance level was used for all statistical tests.
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Cohort: 2,647 adults aged 19 and above received primary care at the HIV Center/CORE Center in 1997 and 1998, of whom 32 percent were women. Table 1 shows the baseline characteristics of the cohort according to gender, age, race, payer status, and HIV risk behavior. The majority of patients were African-American, and the median age was 38 years. Two thirds of patients had no insurance at entry into care, 27 percent had Medicaid, and 1.7 percent had private insurance. Significantly more women than men had any form of health insurance (p<0.0005). Approximately one third of patients were men who have sex with men (MSM), one third were injection drug users (IDU), and one third acquired HIV heterosexually.
Of the 2,647 HIV-infected persons at baseline, ie, in period one, 715 (27 percent) persons had AIDS. The median CD4 T cell count at baseline was 266 cells/µL, with a range of 1-3,069 cells/µL. The median viral load at baseline was 1,901 copies/ml, with a range of <500 copies/ml to 800,000+ copies/ml. Women had significantly higher CD4 T cell counts at baseline than men. Disposition: On follow up through December 1999, 139 (5.2 percent) patients had died. 1,188 (45 percent) of patients met the definition of lost to follow up, ie, they had no primary care visits in two consecutive six-month periods. Excluding deaths and patients with return visits in 1999, 688 (29 percent) patients were lost to follow up in 1997 and 1998.
Clinical Outcomes: Demographics and Clinic Visits: 2,528 patients (95.5 percent) had at least one visit in 1997, and 1,457 patients (55 percent) had regular care during 1997, ie, at least one primary care visit in each six-month period. The median follow up interval was 23 months. The median number of primary care visits was five per year, with a standard deviation of 3.9 visits. 616 (23.3 percent) clients had two or fewer visits, and 1,174 (31.1 percent) had eight or more visits in 1997 and 1998. With older age, the likelihood of receiving any care or regular care, and the total number of visits, increased in both years. African-American and Hispanic patients had more visits than whites in both years (mean visits 8.5 and 8.9 vs. 7.5 respectively, p= 0.045 and 0.012 respectively). Patients with no insurance had fewer primary care visits in periods 1-3 than patients with insurance (mean 7.8 vs. 9.7, p=0.004). Patients with regular clinic care (greater than one visit per six months) had significantly lower viral loads in all periods than those with irregular care.
Hospitalizations: During 1997 there were 1,579 hospitalizations in 623 patients, of which 1,132 (72 percent) were men and 447 (28 percent) were women. There was no statistically significant relationship between gender and hospitalizations or hospital days. Total hospitalizations significantly declined from period 1 (868) to period 4 (585) and from 1997 (1,579) to 1998 (1,160) (p=0.0005). Table 2 shows the frequency of hospital admissions for the cohort. 76 percent of patients had no admissions. Of the 24 percent with hospital admissions, 245 (11 percent) patients had one admission, 295 (11 percent) patients had two to four admissions, and 83 (3 percent) patients had five or more admissions. 16 (0.6 percent) patients had eight to 15 admissions during the two years.
Older age was associated with increased admissions and hospital days (p<0.001). As shown in Table 3, whites had significantly fewer admissions and shorter hospital stays per period than Hispanics or African-Americans. As expected, there were negative, statistically significant correlations between the mean number of admissions and average number of hospital days, and CD4 T cell counts in each period. Similarly, a positive correlation was observed between admissions and total days, and viral load in each period. These results are shown in Table 4.
Hospital admissions during the study period by baseline CD4 T cell count and viral load strata are shown in Tables 5 and 6 respectively. In general, there was a linear increase in admissions among patients in strata with lower CD4 T cell counts and higher viral load. 117 of 266 patients (44 percent) with baseline CD4 T cell counts below 50 cells/µL were admitted at least once, compared with 45 of 353 patients (13 percent) with CD4 T cell counts above 500 cells/µL. Similarly, 68 of 185 patients (37 percent) with baseline viral loads above 100,000 copies/ml were admitted compared to 103 of 675 patients (15 percent) with viral loads below 500 copies/ml. Nonetheless, admissions among patients with low viral loads and high CD4 T cell counts were high in number, with 10.7 percent (45 of 422) of patients with CD4 T cell counts above 500 cells/µL being admitted, and 28.6 percent (103 of 360) of patients with viral loads below 500 copies/ml being admitted. As a proportion of all admissions, admissions in patients with CD4 cells above 500 cells/µL increased from 10.7 percent to 16 percent from period 1 to period 4, and admissions in patients with viral load below detection increased from 28 percent to 41 percent (data not shown).
Patients with regular care in both years had more hospital admissions and more hospital days than other patients (p=0.0005). Hospitalizations varied by form of therapy received; patients on HAART had significantly fewer hospitalizations than patients on ART after controlling for CD4 T cell count and viral load (mean 0.21 vs. 0.26, p=0.034, Mann- Whitney test). The proportion of treated patients on HAART and ART from 1997 to 1998 is shown in Table 7. Patients on HAART, or three or more drugs, rose from 70 percent in period 1 to 82 percent in period 4, and the percent on two drug regimens fell from 30 percent to 18 percent during the study period.
On studying interaction between support services and hospitalization, patients who needed and received case management, mental health services, and transportation assistance were found to have significantly fewer hospitalizations than patients in whom the support service need was unmet (p<0.015, Mann-Whitney test for each support service, data not shown).
Mortality was significantly higher in patients who were hospitalized than in other clinic patients. 36 of 2,023 patients (1.8 percent) who were not hospitalized died during the study period compared with 76 of 623 hospitalized patients (12.2 percent, p<0.0005).
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We found that HIV-related hospitalizations in the only public hospital in Chicago were frequent in the HAART era and decreased over time. Importantly, three quarters of patients living with HIV did not require hospitalization during this two year period. Multiple hospitalizations were clustered in fifteen percent of patients. Older age, lack of HAART, regular clinic care, lower CD4 T cell count, higher viral load, history of IDU, and minority race predicted hospitalization, while female gender did not. Predictably, we found a linear relationship between baseline CD4 T cell count and viral load, and hospitalization. However, we also found a high proportion of admissions occurred in patients with low viral load and high CD4 T cell counts, and the percent of admissions in these two groups increased significantly during the study period. These data are consistent with other studies of predictors of HIV disease progression13 and several recent reports of increasing hospitalization rates among patients with co-morbid conditions such as hepatitis C and chronic liver disease, drug toxicity, and mental illness.14,15
The significant racial disparity in hospitalization rates in the HAART era was unexpected. We observed higher rates of hospitalization and total hospital days in African-Americans and Hispanics compared with whites after adjustment for CD4 T cell count and viral load. Similar observations have been made in other disease states such as heart disease, asthma, and cancer.16 Possible explanations have included poor and delayed access to primary care for minority populations, and poorer overall health status in minorities due to a variety of factors, such as inadequate nutrition and greater exposure to environmental pollutants.
Due to the design of the analysis, our data cannot be explained simply by variations in access to regular primary care, to HAART, or to racial disparities in other predictors of HIV disease outcome such as baseline CD4 T cell count and viral load. All patients in the analysis were receiving ambulatory care at no cost with an equal opportunity for regularcare. The multivariate analysis adjusted for CD4 T cell count and viral load. In addition, we have already reported thefinding of no racial disparities in overall clinical outcomes such as mortality or disease progression as measured by trends in CD4 T cell counts and viral load.17 Indeed, in this analysis, as in others, lower viral load correlated significantly with lower hospitalization rates and lower mortality, and lower CD4 cell count correlated significantly with higher hospitalization rates and higher mortality, and in both cases these findings were independent of race.
The other unexpected finding of this analysis is the association between regular ambulatory care and a greater risk of hospitalization.
The most probable explanations for this observation are selection bias and missing data in patients with irregular care and follow up. Patients in regular care have more opportunity for the identification of medical problems necessitating hospitalization. One limitation of this study is the inability to trace patients who are lost to follow up. The hospitalization data in patients with irregular outpatient care are limited by missing data due to hospitalizations outside of the Cook County Hospital network of which we are unaware. Also, one quarter of the cohort had a baseline CD4 T cell count less than 200 cells/µL. Short-term morbidity in this group might not be responsive to short-term interventions, and thus regular care would be expected to increase hospitalizations due simply to selection bias. Finally, public hospitalization is often a short-term remedy to other problems. In addition to medical problems, social ills such as homelessness, domestic violence, acute drug binging or withdrawal, depression, and malnutrition are known to commonly occur in persons with HIV. As shown in other studies, women with HIV are particularly vulnerable to non-HIV related mortality.18,19 Further evaluation of disparities and commonalities in causes of hospitalization is needed to better assess their relative contribution to the observations in this study.
A comparison of these data to previously reported hospitalization data at Cook County Hospital from 1992 to 1996 is of interest.5 During that period, hospitalizations ranged from 1,575 to 1,781 persons per year with no apparent diminution over time. However, the average length of stay decreased from 13.3 days to 8.5 days, and the average daily census fell from 58 to 33 patients. During the same period, in-patient deaths fell from 116 in 1992 to 74 in 1996. It is noteworthy that these trends preceded the HAART era by several years, and suggest as others have also shown,6,8 that receiving regular medical care and prophylaxis for opportunistic infections may also have contributed substantially to the reduction in morbidity and mortality associated with the HAART era. In the current study hospitalizations declined significantly between 1997 and 1998, suggesting a delay in the impact of HAART on hospitalizations in the public sector.
These findings are compatible with numerous reports showing marked reduction in morbidity and mortality from 1996 to 1999.3,4,6,14 Most relevant to this analysis is the report from Whitman et al from the Chicago Department of Health that showed a 65 percent reduction in mortality between 1996 and 1998 in the city of Chicago. This reduction was equally distributed in men and women, and in African-Americans, Hispanics, and whites. Our data on hospitalizations and mortality provide a sobering counterpoint to these trends. Although declining, hospitalizations and mortality remain commonplace in the HAART era, and the number of hospital admissions is increasing in patients with well-controlled HIV disease.
The difference in our observations and others between hospitalizations and HIV primary care outcomes is of interest. In related analyses of this data set, IDUs, patients with no insurance, and younger patients were less likely to receive regular primary care.12 These data are comparable to the national HCSUS data, which showed that women, IDUs, and people of color were less likely to have any care, regular care, access to HAART, and improved morbidity and mortality compared to men, non-IDUs, whites, patients with insurance, and older patients.2 Unlike HCSUS, we saw no difference in primary care outcomes, mortality, or CD4 T cell counts and viral load between racial groups. Finally, we found that hospitalizations were concentrated in a relatively small fraction of the total ambulatory population, as has been seen among HIV positive patients in the private sector.3 In particular, we found that 16 (0.6 percent) individuals had eight or more admissions during the study period. These data provide some hope for targeted programs designed to help such highly hospitalization-prone individuals with the intent of reducing their contribution to the inpatient burden in public institutions. With the success of direct observed therapy (DOT) for tuberculosis, and preliminary success of DOT in HIV-infected populations, DOT-like programs for admission-prone individuals may offer an opportunity to blunt the recidivism rate. Similarly, a related analysis of this cohort found that outreach improved regular clinic care.12 Targeted programs to improve clinic attendance, adherence to medication, or management of co-morbidities such as chemical dependency, homelessness, or mental illness can substantially improve regular care, and reduce hospitalizations for interval medical or social crises. Although 16 of 2,647 patients may be a proportionately small number for targeted programs, the small number of patients increases the feasibility of beneficial targeted interventions, and the potential benefits in terms of cost and service utilization are large.
There are some limitations to this retrospective observational study. Missing data were common, despite efforts to complete the data set. In particular, one third of patients were lacking viral load and CD4 T cell count data, and complete treatment data for the entire cohort are lacking. Fortunately, the large numbers in the cohort allows for trend analysis of evaluable patients and provides some compensation for this shortcoming. Losses to follow up were common, with about one quarter of the cohort lost to follow up by the end of the study period. These losses explain much of the missing data, and their numbers are comparable to other cohorts in urban public hospitals. This defines the need for better outreach programs, and better strategies to retain patients once they are enrolled. The magnitude of missing data is discouraging, for it has occurred despite extensive efforts to create a "one-stop shopping" model that is convenient for patients with disrupted lives. As noted above, the statistical implications of the losses to follow up are mitigated by the large size of the cohort. Finally, documentation of certain data elements, particularly need for services, was incomplete and not standardized. As a result, more patients received services than were identified with a specific need for the service.
In conclusion, we found that HIV-related hospitalizations were frequent in the HAART era and decreased over time. However, three quarters of patients living with HIV and in care at an urban public hospital HIV clinic did not require hospitalization during this two-year period. Older age, lack of HAART (i.e., one or two drug regimens), lower CD4 T cell count, higher viral load, history of IDU, and minority race predicted hospitalization, while female gender did not. Admissions in patients with well-controlled HIV disease were higher than expected and increased over time. The clustering of hospitalizations in a small number of patients may enable the development of support programs targeted towards these "hospitalization-prone" patients to reduce recidivism.
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16. Sherer R and Goldberg D. "HIV Disease and Access to Care," in It Just Ain't Fair: The Ethics of Health Care for African Americans. Eds. Dula A & Goering S. Praeger Press, Westport, Connecticut, 1994, pp 149-165; ISBN: 0275944948.
17. Sherer R, Cohen M, Stieglitz K, et al. HIV Outcomes at the CORE Center 1997-8: Low median viral load and mortality. Int Conf AIDS. 2000 Jul 9-14;13 [Abstract TuPeC3316].
. Melnick SL, Sherer R, Louis TA, et al. Survival and Disease Progression According to Gender of Patients Enrolled in the Terry Beirn Community Programs for Clinical Research on AIDS (CPCRA). JAMA 1994 Dec 28;272(24):1915-21.
19. Cohen M, Moore B, Williamson M et al. The first 120 deaths in women with AIDS at Cook County Hospital. Program and Abstracts of the First National Conference on Women and HIV, Washington DC, 1997. Abstract 232.
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The Authors gratefully acknowledge the contributions of the following individuals to this work: Bonnie Lubin, PhD, Grants Administrator, Hektoen Institute; Aaron Rothenberg, Data and Computer Consultant; Patty Magana, Administrative Assistant; Kathi Braswell, RN, Executive Director, the CORE Center; and Robert A. Weinstein, MD, Chief Operating Officer, The CORE Center for the Prevention, Care, and Research of Infectious Disease.
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