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(Chest. 2004;126:1079-1086.)
© 2004 American College of Chest Physicians

Hospitalizations for Tuberculosis in the United States in 2000*

Predictors of In-Hospital Mortality

Nadia N. Hansel, MD, MPH; Barry Merriman, MA; Edward F. Haponik, MD, FCCP and Gregory B. Diette, MD, MHS

* From the Department of Medicine, School of Medicine, Johns Hopkins University, Baltimore, MD.

Correspondence to: Nadia N. Hansel, MD, MPH, Division of Pulmonary and Critical Care Medicine, Johns Hopkins University, Room 577, 1830 East Monument St, Baltimore, MD 21205; e-mail: nhansel1{at}mail.jhmi.edu


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: Despite curative therapy, mortality remains high for hospitalized patients with tuberculosis (TB) in the United States. The purpose of this study was to describe the characteristics of hospitalized patients with TB and to identify patient characteristics associated with in-hospital mortality.

Design, setting, and patients: Using the 2000 Nationwide Inpatient Sample, representing 20% of US hospital admissions, we identified 2,279 hospital admissions with a primary diagnosis of TB (International Classification of Diseases, ninth revision, codes, 010.xx to 018.xx).

Measurements and results: Mortality was the main outcome measure. Logistic regression analyses were performed including age, gender, race, insurance status, income, Deyo-adapted Charlson comorbidity index (DCI), HIV status, hospital admission source, and hospital characteristics as explanatory variables. A disproportionate number of patients hospitalized with TB were men (64%), nonwhite (72%), lived in areas with median incomes of < $35,000 (50%), and had publicly funded health insurance (49%) or no health insurance (17%). The mortality rate for patients hospitalized for TB was greater than that for non-TB hospital admissions (4.9% vs 2.4%, respectively; p < 0.001). Patients with TB who died during hospitalization were older (mean age, 65.1 vs 49.4 years, respectively; p < 0.001), had greater comorbid illness (DCI, 1.1 vs 0.55, respectively; p < 0.001), required longer hospitalizations (19.9 vs 13.9 days, respectively; p < 0.001), and accumulated substantially higher charges ($79,585 vs $31,610, respectively; p < 0.001) than did patients with TB who were alive at hospital discharge. In a multivariable analysis, older age, comorbid illnesses, and emergency department admissions were independently associated with mortality. The total charges for TB hospitalizations in the United States in 2000 exceeded $385 million.

Conclusions: Despite public health efforts, patients who are hospitalized with TB are frequently admitted through emergency care settings, have a high risk of in-hospital mortality, and incur substantial hospital charges. To improve TB health outcomes, more vigorous clinical management and prevention strategies should especially target older patients and those with comorbid medical conditions.

Key Words: epidemiology • health-care costs • hospitalization • Mycobacterium • outcomes • tuberculosis


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Tuberculosis (TB) is an infectious disease caused by Mycobacterium tuberculosis and transmitted by aerosolized droplet nuclei, infecting approximately one third of the world population.1 In 1997, it was estimated that almost 2 million people died of TB worldwide, with a case fatality rate as high as 23%.1 In the United States, active TB disease usually can be treated successfully, with an extended therapeutic course of a combination of antibiotics, often using directly observed therapy (DOT). According to a recent expert consensus statement,2 "it is well established that appropriate therapy of TB rapidly renders the patient noninfectious... minimizes the risk of disability or death from TB and nearly eliminates the possibility of relapse." Despite the availability of curative therapy, TB affects the quality of life of the people infected.3 A large proportion of patients with TB are being hospitalized, and in-hospital mortality remains high, with estimates of mortality rates ranging widely from 2 to 12%.4567 Some studies891011 have examined the costs of TB hospitalizations, however, few investigations have addressed the poor outcomes of hospitalized patients with TB.

Comorbidity, including high rates of HIV, and delayed treatment have been implicated as the causes for the high mortality rates of hospitalized patients with TB in international or regional studies in the United States.47 To our knowledge, previous studies have not examined a nationally representative sample of hospitalized patients with TB. The purpose of this investigation was to characterize the patients hospitalized with TB in the United States in year 2000 and to identify the predictors of in-hospital mortality.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Study Design and Population
Using an administrative database, we conducted a cross-sectional study characterizing hospitalizations for TB in the United States in 2000. Patients selected for this study had a primary discharge diagnosis of TB, using the International Classification of Diseases, ninth revision (ICD-9), hospital discharge codes 010.xx to 018.xx.

Database
We used the 2000 Nationwide Inpatient Sample (NIS), a database of hospital inpatient stays, developed by the Healthcare Cost and Utilization Project. As the largest all-payer inpatient care database that is publicly available in the United States, the NIS data set represents 20% of non-federal US hospitals. These data include a stratified random sample of 994 hospitals in 28 states, encompassing approximately 7.5 million inpatient stays. (More information on the NIS is available at the web site http://www.ahcpr.gov/data/hcup/nisintro.htm.)

Outcome and Predictor Variables
The primary outcome for this study was the in-hospital mortality rate. Secondary outcomes included total charges and length of stay. The independent variables studied included demographic characteristics (ie, age, gender, race, median income of zip code of residence, and health insurance status), comorbidity, HIV status, hospital admission source, and hospital characteristics (ie, region, location, and teaching status). All independent variables were examined as categoric variables, except for age, which was used as a continuous variable.

We assessed comorbidity in this sample by using the Deyo-adapted Charlson comorbidity index (DCI), a method that is used to estimate the risk of death from comorbid disease12 using ICD-9, clinical modification, administrative databases.13 Patients with three or more comorbid illnesses were categorized as one group due to the small number of patients with comorbidities in this range. Patients were considered to have HIV if any of the 15 hospital discharge diagnoses had an ICD-9 code of 042.

Statistical Analysis
We used weighted descriptive statistics to characterize the patient sample, using proportions or means with SDs where appropriate. The means and SDs of continuous variables were compared using the Student two-tailed t test. Differences for categoric variables were determined by {chi}2 test or the Cochran-Mantel-Haenszel test for trend. A p value of < 0.01 was considered to be statistically significant.

Logistic regression models were developed to evaluate the mortality outcome. Unweighted and weighted distributions for independent variables were similar, thus unweighted values were used in logistic models for simplicity. Bivariate analyses were conducted to determine the association of potential predictors of in-hospital mortality. The following multivariate models were used to adjust for potential confounding and interaction: (1) patient characteristics; (2) patient characteristics and hospital admission source; and (3) patient characteristics and hospital characteristics. The goodness of fit of the multiple logistic regression models was assessed using the Hosmer-Lemeshow test.14 Data from the logistic regression analyses are presented as crude and adjusted odds ratios (ORs), with corresponding 95% confidence intervals (CIs) and p values. Statistical analyses were performed using a statistical software package (Stata, version 6.0; Stata Corp; College Station, TX).


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
In this 20% sample of US hospitalizations, representing 7,450,992 hospital admissions, there were 2,279 hospitalizations with a primary hospital discharge diagnosis of TB. The mean patient age on hospital admission was 50.2 years. Demographic characteristics of these patients, compared to all other hospital admissions (7,448,713 hospital admissions), are shown in Table 1 . Unlike hospital admissions for primary reasons other than TB, the majority of hospital admissions for TB were in men (64%) and minorities (black, 27%; Hispanic, 25%; Asian or Pacific Islander, 14%; other, 7%). Additionally, half of the people admitted to the hospital for TB resided in zip code areas with a median income of < $35,000, and most had publicly funded health insurance or no documented health insurance (66%).


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  		Table 1. Characteristics of Hospitalized Patients, NIS, United States, 2000*

 
Comorbid illness was common in patients with TB, with 29% having a DCI score of 1, 9% having a score of 2, and 4% having a score of ≥ 3. Seventy-five patients (3.3%) were identified as having HIV infection.

Over half of the patients with TB (57%) were admitted to the hospital through the emergency department, and Table 2 shows the characteristics of the hospitals to which TB patients were admitted. Compared to non-TB patients, those with TB were more likely to be admitted to urban hospitals (92% vs 84%, respectively; p < 0.001) and those designated as teaching hospitals (61% vs 43%, respectively; p < 0.001).


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  		Table 2. Admission Source and Hospital Characteristics, NIS, United States, 2000*

 
Outcomes
The length of hospital stay was considerably longer for hospital admissions for TB compared to other hospital admissions (mean, 14.2 ± 18.8 vs 4.6 ± 6.7 days, respectively; p < 0.001; median, 9 vs 3 days, respectively). Additionally, the total charges were almost 2.5 times higher for hospital admissions for TB compared to all other hospital admissions (mean total charges, $33,985 ± 52,414 vs $13,770 ± 29,336, respectively; p < 0.001; median total charges, $18,975 vs $7,123, respectively). While two thirds of the patients (69.5%) were routinely discharged to home, 4.9% of those with a primary diagnosis of TB died during the hospitalization, compared to 2.4% of non-TB patients (relative mortality risk, 2.08; 95% CI, 1.74 to 2.49) [Table 3 ].


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  		Table 3. Outcomes of Hospitalized Patients With and Without TB*

 
Compared to patients with TB who were alive at hospital discharge, patients who died during hospitalization were older (mean age, 65.1 ± 16.5 years vs 49.4 ± 20.8 years, respectively; p < 0.001), had a higher level of comorbid illness (mean DCI, 1.1 ± 1.0 vs 0.55 ± 0.81, respectively; p < 0.001), required longer hospitalizations (mean length of stay, 19.9 ± 20.5 days vs 13.9 ± 18.7 days, respectively; p < 0.001), and accumulated substantially higher charges (mean charges, $79,585 ± 107,873 vs $31,610 ± 46,578, respectively; p < 0.001) [Fig 1 ].



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  		Figure 1. Comparison of patients with TB who died or were alive at hospital discharge. Comparison of age, DCI, length of stay (LOS), and total charges for patients with TB who died in the hospital (112 patients; black columns) and for those who were alive at hospital discharge (2,163 patients; white columns). p < 0.001 for all comparisons.

 
Logistic regression analyses estimating the unadjusted and adjusted ORs of risk of in-hospital mortality are presented in Table 4 . The Hosmer-Lemeshow test showed that the multivariate models demonstrated a good fit, and there was no evidence for collinearity among the independent variables. Increasing age, comorbidity, and having Medicare insurance were statistically significant predictors of mortality in bivariate analyses. In multivariate analyses, age (OR, 1.03 per year of age increase; p = 0.001) and comorbidity (OR, 1.59; p < 0.001) remained strong predictors of mortality. Medicare insurance status was no longer a statistically significant predictor of mortality, after adjustment. Similarly, HIV status, gender, race, and income did not significantly predict mortality.


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  		Table 4. Predictors of In-Hospital Mortality Among Patients Hospitalized for TB*

 
When hospital admission source was added to the multivariate model, the associations with patient characteristics and mortality were not significantly changed. However, patients admitted to the hospital through the emergency department were more than twice as likely to die during their hospitalization compared to those with routine hospital admissions (OR, 2.38; p = 0.001). Hospital characteristics were not significant in multivariate analysis and, when included in the multivariate model, did not significantly change the results (data not shown).


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
This is the largest study, to date, to provide nationally representative estimates of outcomes of hospitalized patients with TB in the United States. Since the observations in this study are not limited to specific geographic areas or subgroups of patients, the external validity of these results is increased. Using a national database, we identified patients hospitalized with TB in the United States in 2000 along with predictors of in-hospital mortality. There were 2,279 TB hospitalizations in our sample, representing 20% of US hospitalizations. Extrapolating from this finding (using hospital discharge weights), we estimate that there were > 11,000 TB hospital admissions in the United States in 2000. Although one patient may be hospitalized more than once, there were only 16,377 TB cases reported to the Centers for Disease Control and Prevention in 2000.15 Thus, it is likely that a high proportion of people with TB are being hospitalized, and they experience a high in-hospital mortality rate of 4.9%. In addition, based on these findings in 2000, there were > 160,000 hospital days and > $385 million in hospital charges estimated for TB patients. These observations are intriguing, for while TB is often considered a vanishing disease in the United States, there is still a substantial burden on the US health system.

While all people are susceptible to infection with TB, the majority of cases occur in men, minorities, and the socially disadvantaged.161718 Our results are consistent with these previous epidemiologic data. This study extends previous insights, and shows that men continue to be at greater risk and that most of the patients admitted to the hospital with TB were racial minorities, residents of regions with low household incomes, and had publicly funded or no health insurance.

Despite available effective therapy, people hospitalized for TB in the present study had an unacceptably high mortality rate. The in-hospital mortality rate for TB hospital admissions (4.9%) was more than double the mortality rate for all other hospital admissions (2.4%), including those for other chronic illnesses, such as COPD (2.5%),19 cystic fibrosis (1.6%), or asthma (0.4%).20 We identified several predictors of in-hospital mortality in a multivariate regression analysis, including emergency department admissions, older age, and comorbid illness.

The source of admission to the hospital is an indicator of access to continuity care and also an indicator of acuity of illness. We expected that patients who had been admitted to the hospital through the emergency department were likely to be sicker at time of presentation, and to have experienced delayed treatment and/or had limited access to primary care. Despite public health efforts and DOT, patients with TB were admitted to the hospital through the emergency department 57% of the time. Although we have accounted for several factors that are associated with limited access to care such as health insurance status, race, and income, the hospital admission source remained a significant predictor of mortality. In a previous study,21 unemployment, concern about cost, uncertainty about where to get care, anticipated long waiting time in the physician’s office or a long wait for an appointment, fear of immigration authorities, and belief in the efficacy of self-treatment were shown to be significantly associated with delays in seeking care among symptomatic patients with TB. Furthermore, individuals who are homeless, mentally disturbed, or alcoholic may lack the motivation or concern about their health status and may seek medical care too late to be cured.22 In fact, delayed treatment has been linked previously to higher mortality rates in patients with TB.72324 Thus, actual or perceived access barriers to health care may play a significant role in high TB mortality. Public health policy aimed at decreasing these barriers and encouraging patients to seek care early in their illness should be intensified. Because urban and teaching hospitals carry most of the burden of hospital care, and because publicly funded health-care programs (ie, Medicare and Medicaid) provide care for almost half of patients hospitalized for TB, the expansion of governmental programs that are aimed at education about, prevention of, and early identification of TB seems to be justified.

Older age was a strong, independent predictor of mortality. Given the aging of the American population,25 mortality from TB in the elderly is an enormous concern. Mortality may be higher in older adults because they may receive less vigorous care,26 or older persons may have more severe disease because of a decreased immunologic status and decreased baseline functional status.27 Older people with TB have been shown2829 to have more extensive disease, based on chest radiograph findings at presentation. Importantly, age may have a modifying effect on TB illness itself, making the diagnosis of TB more difficult. Older TB patients have a higher prevalence of nonspecific symptoms, a lower prevalence of fever, and less frequently manifest a positive tuberculin skin test.29 This less classic presentation may contribute to the longer delay in presentation and initiation of treatment, and may lead to a higher risk of death.28

Comorbid illness has substantial influence on patient outcomes.3031 Comorbidity indexes, utilizing ICD-9, clinical modification, codes from hospital discharge records, have been shown323334 to predict the survival of patients with various health conditions. In our study, comorbidity, measured by the DCI, was similarly found to be a significant predictor of mortality. Specifically, diseases such as renal failure and liver disease may cause difficulties in TB treatment given the increased risk of toxicity of first line TB drug therapies.2 Although HIV status is included in the measure of DCI, we also examined it separately because of its previously demonstrated relevance to TB outcomes.3536 A diagnosis of HIV in our study was not associated with higher mortality. Previous studies2437 that have examined the relationship suggest that the severity of immunodeficiency, or CD4 count depletion, is an independent predictor of mortality in TB patients with HIV. Clinical laboratory data, such as CD4 count, were not available in this database, so we were unable to assess the severity of HIV disease in these patients, which may explain why it was not predictive of death.

The prevalence of HIV in our study population of hospitalized TB patients was 3.3%, which is lower than the national estimate of the HIV-TB coinfectivity rate of 10% published by the Centers for Disease Control and Prevention.38 This finding may be due to a tendency to list HIV as the primary diagnosis when TB and HIV were coincident. In fact, this appears to be a plausible explanation, as the prevalence of HIV-TB coinfectivity reached 11.3% when we included patients with a primary diagnosis of HIV and a secondary diagnosis of TB. We focused on TB as a primary diagnosis in order to capture outcomes that are most likely attributable to TB illness. Nevertheless, in a secondary analysis (data not presented) we calculated the mortality rate of patients with a primary diagnosis of HIV and a secondary diagnosis of TB to assess whether they had different mortality rates than those patients in our study. The mortality rate was 4.8%, which is similar to that for patients with a primary diagnosis of TB. Thus, we do not believe that including these patients in our analysis would have changed our results significantly.

We have shown that TB is a disease that disproportionately affects minority populations in the United States. In many illnesses for which there are racial disparities in outcome, there is concern about the quality of care.39 For instance, minorities are less likely to undergo invasive cardiac procedures.40 However, our study showed that, once hospitalized for TB, minority patients had similar mortality outcomes as whites. These results should provide some optimism concerning potential racial disparities in the care of patients with TB, and they suggest that there may not be large differences in the hospital care of TB patients of different races and ethnicities.

Certain methodological limitations of the study must be considered. Several important factors that have been suggested as risk factors for TB mortality, such as homelessness, history of incarceration, injection drug use, multidrug-resistant TB, compliance with DOT, and delay in diagnosis,724 could not be ascertained directly by this administrative database. Specifically, missed diagnosis and delayed treatment after hospitalization have been shown to occur more often in hospitals with low TB hospital admission rates and were strongly associated with in-hospital death in Canada.7 The measure of income was an ecologic rather than patient-specific measure, which can lead to the misclassification of income status. Given that persons with TB tend to have relatively lower socioeconomic status (SES) than their demographic or geographic counterparts, assigning SES values to individuals based on geographic means may actually overestimate their income and, in turn, underestimate the association between SES and TB outcomes.17 In addition, the results of this study rely on the accuracy of the diagnosis codes. The NIS database does not include patient identifiers, thus validation of the accuracy of the hospital discharge records was not feasible. However, several studies194142 have successfully assessed patient outcomes using the NIS database.

Despite these limitations, the results of this study have major implications for public health programs, health-care providers, and patients. While curative therapy is seemingly readily available in the United States, TB hospitalization rates and the burden on the US health-care system remain substantial. Additionally, the risk of mortality once patients with TB are hospitalized is high and is unlikely to be explained by the HIV epidemic. Patients with older age and a greater number of comorbid illnesses, and patients admitted to the hospital through the emergency department have the highest risk of death. This underscores the importance of the need for improved clinical management strategies that are targeted for high-risk populations, including older patients and those with comorbid disease. Furthermore, it highlights the importance of intensifying public health efforts that are aimed at screening and detecting cases, decreasing barriers to seeking care, and increasing public awareness of the importance of TB and receiving early treatment. Much progress has been made in decreasing the prevalence of TB in the United States,43 but the disease is far from being eliminated, and larger strides are needed to decrease the suffering of those affected.


   Footnotes
 
Abbreviations: CI = confidence interval; DCI = Deyo-adapted Charlson comorbidity index; DOT = directly observed therapy; ICD-9 = International Classification of Diseases, ninth revision; NIS = Nationwide Inpatient Sample; OR = odds ratio; SES = socioeconomic status; TB = tuberculosis

Received for publication December 23, 2003. Accepted for publication March 9, 2004.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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