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(Chest. 2005;127:205-212.)
© 2005 American College of Chest Physicians

Delays in Suspicion and Isolation Among Hospitalized Persons With Pulmonary Tuberculosis at Public and Private US Hospitals During 1996 to 1999*

Julia Rozovsky-Weinberger, MD; Jorge P. Parada, MD, MPH; Laura Phan, MPH; David G. Droller, MD; Maria Deloria-Knoll, PhD; Joan S. Chmiel, PhD and Charles L. Bennett, MD, PhD, MPP

* From the Division of Pulmonary and Critical Care Medicine (Dr. Rozovsky-Weinberger), John H. Stroger Hospital of the Cook County, Chicago, IL; the Midwest Center for Health Services and Policy Research (Dr. Parada), Hines VA Hospital, Hines, IL; the Institute for Health Services Research and Policy Studies (Ms. Phan), and the Department of Preventative Medicine (Drs. Deloria-Knoll and Chmiel), Northwestern University Chicago, IL; the Division of Infectious Diseases (Dr. Droller), Broward General Medical Center, Ft. Lauderdale, FL; and the Midwest Center for Health Services and Policy Research (Dr. Bennett), Chicago, IL.

Correspondence to: Charles L. Bennett, MD, PhD, MPP, Jesse Brown VA Medical Center, 333 East Huron, Suite 277, Chicago, IL 60611; e-mail: cbenne{at}northwestern.edu.


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Background: While prior studies have shown that public and private hospitals differ in their rates of suspicion and isolation of patients who are at risk for tuberculosis (TB), no study has investigated whether this variation is due to differences in the impact of patient case-mix on hospitals or to variations attributable to specific hospital practice patterns.

Objective: To investigate patient-level and hospital-level factors associated with delays in TB suspicion and isolation among inpatients with pulmonary TB disease.

Design: Retrospective cohort study of patients hospitalized with culture-positive pulmonary TB during 1996 to 1999.

Setting: Patients with culture-proven pulmonary TB treated at three public hospitals (765 patients) and seven not-for-profit private hospitals (172 patients) in Chicago, Los Angeles, and southern Florida that provided care for five or more patients with TB per year during the study period.

Measurements: Two-day rates (within 48 h from admission) of acid-fast bacilli (AFB) smear orders and 1-day rates (within 24 h from admission) of TB isolation.

Results: Two-day rates of ordering AFB smears were > 80% at three public and two private hospitals vs 65 to 75% at five private hospitals. One-day rates of TB isolation at the three public hospitals were 64%, 79%, and 86%, respectively, vs 39 to 58% at the seven private hospitals. Delays of > 2 days in ordering AFB smears were associated with patient-level factors: absence of cough (adjusted odds ratio [AOR], 6.02; 95% confidence interval [CI], 3.82 to 9.52), cavitary lung lesion (AOR, 5.17; 95% CI, 1.98 to 13.50), night sweats (AOR, 3.38; 95% CI, 1.90 to 5.99), chills (AOR, 1.70; 95% CI, 1.01 to 2.88), and female gender (AOR, 1.66; 95% CI, 1.06 to 2.60). Delays of > 1 day in ordering pulmonary isolation were associated with patient-level factors: absence of cough (AOR, 3.40; 95% CI, 2.31 to 5.03), cavitary lung lesion (AOR, 2.66; 95% CI, 1.57 to 4.50), night sweats (AOR, 1.98; 95% CI, 1.35 to 2.92), and history of noninjecting drug use (AOR, 1.86; 95% CI, 1.16 to 2.99) and one hospital-level factor: receiving care at a nonpublic hospital. Even after adjustment for patient-level factors, TB patients at private hospitals were half as likely as those at public hospitals to be placed in pulmonary isolation (AOR, 0.47; 95% CI, 0.30 to 0.72), while odds of suspecting TB in these same patients were similar at both hospitals.

Conclusion: Private hospitals should order TB isolation for all patients for whom AFB smears are ordered, a policy that has been instituted previously at public hospitals in our study.

Key Words: nosocomial outbreak of tuberculosis • patterns of care • quality of care


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Tuberculosis (TB) reemerged as an important public health problem shortly after the AIDS epidemic began.123 Factors attributed to this resurgence include a decline in support for the public health infrastructure, co-infection with HIV, an increasing immigrant population, and nosocomial outbreaks of TB in prisons, nursing homes, hospitals, and shelters.45678 Several studies569101112131415 in the mid-1980s identified problems in hospital care such as delayed recognition and management of tuberculosis. In several instances, these were followed by nosocomial outbreaks of multidrug-resistant TB (MDR-TB). In a 1990-to-1993 evaluation from New York conducted following outbreaks of MDR-TB, Frieden et al13 identified 267 TB patients with isolates resistant to isoniazid, rifampin, ethambutol, streptomycin, and rifabutin. Remarkably, 67% of these patients had acquired their disease through nosocomial transmission. Many patients remained infectious from disease onset to death, did not survive the hospitalization, and were located on wards with other individuals with HIV infection. In a 1988-to-1996 evaluation of 206 TB inpatients in eight hospitals in St. Louis, 25% experienced delays in TB suspicion and in the implementation of standard infection control practices.11 In 1994 and 1996, recommendations for the prevention of nosocomial transmission were published by the Centers for Disease Control and Prevention (CDC) and the American Thoracic Society (ATS).1617 These recommendations included early identification of patients who may have infectious TB and prompt implementation of TB infection control precautions for such patients.1617

Even after publication of these recommendations, problems in the quality of inpatient TB care persisted.18192021 In a 1995-to-1997 evaluation of 1,227 HIV-infected patients with pneumonia who received care at 44 hospitals in New York, Chicago, or Los Angeles, only 66%, 63%, and 24% of the patients in the three study regions, respectively, were placed in pulmonary isolation during the first 2 hospital days.18 Rates of ordering TB isolation were highest at public vs private hospitals, despite rates of TB suspicion being similar at the two types of hospitals.1819 In a study of TB care at four hospitals in Chicago during 1994 to 1996, TB patients as well as HIV-infected patients with pneumonia who received care at a county vs a private hospital were significantly more likely to have been placed in pulmonary isolation.21 Moreover, a nosocomial outbreak of MDR-TB occurred at one private hospital with low rates of use of pulmonary isolation rooms for TB patients.21

While hospitals vary in TB practices, it is not known if these variations are primarily due to higher rates of high-risk TB patients at certain hospitals (case-mix or patient-level effects) or to variations in hospital-specific practices (hospital-level effects). In this study, we evaluated patient-level and hospital-level factors associated with delays in suspicion and isolation of TB patients during the years from 1996 to 1999 at three public and seven private hospitals in Los Angeles, Chicago, and Miami, three cities with large numbers of cases of TB.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Data
Thirty-one randomly selected public, for-profit, or not-for-profit hospitals in Chicago, Los Angeles, and Miami have participated in a series of studies of Pneumocystis carinii pneumonia and community-acquired pneumonia over the past decade.222324 From these 31 hospitals, a random sample of 12 hospitals were selected for consideration for this study. Of these 12 hospitals, 10 hospitals that treated five or more patients with culture-confirmed TB per year (for the years 1996 to 1999) agreed to participate in this study. Medical records for all patients with TB who received care at the study hospitals during 1996 to 1999 were reviewed. Cases were identified from reviews of hospital microbiology logbooks. All patients > 18 years of age with a positive culture finding for Mycobacterium tuberculosis were entered into the study database. The study was approved by the Institutional Review Board at Northwestern University and at each of the study hospitals prior to initiation of data collection. Hospital, patient, and physician confidentiality were maintained throughout the study.

Nurses reviewed inpatient medical records of each patient using a standardized data collection form. Standard risk factors, as defined by the ATS and the CDC,8 for tuberculous infection and for development of tuberculous disease after infection were sought from the medical record. The following presenting signs and symptoms at the time of hospitalization were recorded: cough, fever, night sweats, chills, shortness of breath, wheezing, chest pain, and weight loss. The findings from chest radiography done at hospital admission were also recorded. The type of pulmonary tuberculous disease was recorded by using the following descriptors: smear-positive sputum, cavitary, and others. Factors associated with high-risk for TB were recorded: HIV infection, drug use, homelessness, foreign birth, incarceration, and/or cavitary lung lesion.

Statistical Analysis
A low-TB-risk patient was operationally defined by the following factors: absence of cavitary lung lesions on chest radiograph, HIV negative, nonuser of illicit drugs, not homeless, and not having been incarcerated. Two time intervals were operationally defined, based on an extensive review of the literature, and the expert opinion resultant from the input from nine infectious disease or pulmonary specialists. The suspicion interval was defined as the time from hospital admission to the first ordering of acid-fast bacilli (AFB) sputum, and the isolation interval was the time from the admission to placement in respiratory isolation rooms. Intervals for suspicion that exceeded 48 h and isolation that exceeded 24 h were considered indicative of a delay in the management of the patient. The differences in these intervals were in large part attributable to the conclusion that any delay in the isolation of a patient with pulmonary TB represented a potential period conducive to the nosocomial spread of TB, or MDR-TB, and therefore was a break in optimal infection control practices. In order to overcome difficulties in assessing the exact timing of isolation, in light of limitations in the documentation of timing in the charts, and issues regarding direct admissions to a nursing unit vs admissions via emergency department and transfers, we operationalized this concept as proof that the patient was placed in respiratory isolation on the (first) day of admission. In contrast, it was believed that some delay in diagnostic workup, while not recommended, was certainly tolerable. Therefore, a 2-day window for obtaining an AFB sputum was selected in order to permit delays attributable to events such as coverage of patients by other physicians, need to arrange for an induced or bronchoscopic sputum collection, holidays, and weekend slowdowns. Finally, preferential isolation was defined as the practice of placing high-risk patients in TB isolation at a higher rate (≥ 25% difference) than low-risk patients.

Hospital-Level Analyses
Two-day rates (within 48 h of admission) of AFB orders and 1-day rates (within 24 h of admission) of pulmonary isolation were calculated for each hospital. The denominator was the total number of patients with pulmonary TB in each hospital. Hospital rates were compared using the {chi}2 test. Hospital practice patterns were also looked at by hospital type (public vs private) and to see if preferential isolation was used.

Patient-Level Analyses
All tests of significance were two tailed. Continuous variables were analyzed using Student t test or Wilcoxon rank-sum test. The {chi}2 test or Fisher Exact Test were used to analyze categorical variables, as appropriate. The primary data analysis compared patients who experienced an overall delay in TB isolation with those who had not experienced such delays. All values are expressed as the median (continuous variables) or as a percentage of the group from which they were derived (categorical variables), along with 5th and 95th percentiles; p ≤ 0.05 was considered statistically significant. Multiple logistic regression analysis was used to identify predictor variables that were significantly related to the likelihood of having a delay in ordering sputum for AFB examination or in ordering pulmonary isolation. Odds ratios and their 95% confidence intervals (CIs) were calculated by using standard methods. Baseline covariates were included in models that were judged a priori to be clinically sound. This was prospectively determined to be necessary to avoid producing spuriously significant results due to multiple comparisons. Potential predictor variables for model entry were identified by using univariate analysis, in which p = 0.05 was used to determine entry into the logistic regression model. Results of the logistic regression analysis are reported as adjusted odds ratios (AORs) with 95% CIs. A statistical software package (SAS, version 6.0; SAS Institute; Cary, NC) was used for all analyses.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Hospital-Level Results
Of the 10 hospitals, 3 were public hospitals and 7 were not-for-profit university and community hospitals in Chicago, Los Angeles, and southern Florida during 1996 to 1999. All hospitals had experience with diagnosis and treatment of TB. Each hospital in our study provided care for five or more cases of culture-positive pulmonary TB per year during from 1996 to 1999.

During the first 2 hospital days, all three public hospitals and two private hospitals ordered AFB smears for ≥ 80% of their pulmonary TB patients, while five other private hospitals ordered AFB smears for 65 to 75% of their pulmonary TB patients. During the first hospital day, two of the three public hospitals isolated 79% and 86% of the TB patients, respectively, and the third public hospital isolated 64% of the pulmonary TB patients. The seven private hospitals isolated 39 to 58% of the pulmonary TB patients. One public hospital and all seven private hospitals had 1-day pulmonary isolation placement rates and 2-day rates of sputum ordered for AFB smears that differed by ≥ 10% (Fig 1 ). Further evaluation of this figure reveals three hospital-level practice patterns, or groups, characterized by rates of ordering AFB smears in the first 2 days of hospitalization and rates of isolating pulmonary TB patients in the first day of hospitalization. Of note, group 2 consists solely of the three public hospitals, each of which had relatively high 2-day rates of TB suspicion (86 to 89%) and high-to-moderate 1-day rates of TB isolation (64 to 86%). All private hospitals were either in groups 1 or 3, characterized by high 2-day TB suspicion rates/low 1-day TB isolation rates (group 1: TB suspicion rates, 95%; TB isolation rates, 43%) and moderate-to-low 2-day TB suspicion rates/moderate-to-low 1-day TB isolation rates (group 3: TB suspicion rates, 65 to 77%; TB isolation rates, 39 to 57%). Table 1 details these findings as well as showing the hospital-level practice patterns for high-risk vs low-risk TB patients. Overall, TB isolation rates were lower for patients at low risk for TB infection. All seven private hospitals and two of the three public hospitals had 1-day TB isolation rates ranging from 0 to 58%. Of note, foreign-born and HIV-infected patients had high rates of timely TB isolation and diagnostic workup. However, this was primarily a patient-level effect, as regardless of the hospital type, these patients underwent prompt isolation and workup.



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  		Figure 1. Rates of AFB smear within 48 h of hospital admission and TB isolation within 24 h of admission by hospitals. The first number in the parenthesis indicates the number of patients at the respective hospital who were considered to have high TB risk; while the second number represents the number of patients at the respective hospital who were considered to have low TB risk. The total number of pulmonary TB patients at a hospital during from 1996 to 1999 equals the addition of the two numbers in the respective parenthesis.

 

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  		Table 1. Hospital Type and TB Practice Patterns With Regard to Rates of Institution of TB Respiratory Isolation and AFB Smears

 
Patient-Level Results
Nine hundred thirty-seven patients with culture-positive pulmonary TB received care for TB at the 10 study hospitals during 1996 to 1999. The mean age of the patients was 43 years (SD, 14 years). Table 2 shows additional sociodemographic data, such as gender, ethnicity, HIV status, elicit drug use, foreign-born status, homelessness, and history of incarceration. Table 3 also delineates pertinent clinical and radiographic findings, such as night sweats, weight loss, cough, and cavitary lung lesion.


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  		Table 2. Demographic Characteristics and Factors Associated With Delays in Ordering AFB Smears or Placement Into TB Isolation Rooms Among Patients Hospitalized With Culture-Confirmed TB*

 

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  		Table 3. Logistic Regression Analysis Identifying Variables Associated With Delays > 48 h From Hospital Admission in Ordering an AFB Smear Among Patients With Culture-Confirmed TB and Variables Associated With the Presence of Delay in Placement of Patients With Culture-Confirmed TB Into TB Isolation Rooms*

 
A delay of > 2 days in ordering sputum for AFB smears occurred in 137 patients (14.6%). Univariate analysis identified several demographic factors and disease characteristics that were associated with a delay in ordering sputum for AFB examination (Table 2). Of note, age, gender, elicit drug use, and homelessness were all found to be statistically significant (all with p < 0.05) for both delay in AFB smear (or TB diagnostic testing) and TB (or respiratory) isolation, and ethnicity approached statistical significance (p = 0.061) only for delay in instituting TB isolation. Neither HIV nor foreign-born status were found to be significant risk factors for delay in instituting TB isolation infection control measures, or obtaining an AFB sputum sample. Multiple logistic regression analysis showed that the following five patient-level characteristics were associated with increased likelihood of delay in obtaining sputum for AFB smear (Table 3): absence of cough (AOR, 6.02; 95% CI, 3.82 to 9.52); absence of cavitary lung lesion (AOR, 5.17; 95% CI, 1.98 to 13.50); absence of night sweats (AOR, 3.38; 95% CI, 1.90 to 5.99); absence of chills (AOR, 1.70; 95% CI, 1.01 to 2.88); and female gender (AOR, 1.66; 95% CI, 1.06 to 2.60).

Most patients were placed in TB isolation at hospital admission (the median interval from hospital admission to placement in a respiratory isolation room was 0 days; 5th and 95th percentiles, 0 days and 6 days, respectively). Among the 674 patients with sputum smears that were positive for AFB, respiratory isolation occurred later > 1 day after admission for 172 patients (25.5%). The median time until placement into respiratory isolation for individuals with smear-positive sputum was 0 days (5th and 95th percentiles, 0 days and 7 days). Factors associated with a delay of ≥ 1 day in ordering pulmonary isolation for all TB patients included four patient-level characteristics: absence of cough (AOR, 3.40; 95% CI, 2.31 to 5.03), absence of cavitary lung lesion (AOR, 2.66; 95% CI, 1.57 to 4.50), absence of night sweats (AOR, 1.98; 95% CI, 1.35 to 2.92), and absence of noninjecting drug use (AOR, 1.86; 95% CI, 1.16 to 2.99), and one hospital-level characteristic: nonpublic hospital ownership (AOR, 2.11; 95% CI, 1.38 to 3.24) [Table 3].


   Discussion
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Despite recent advances in microbiological techniques, it frequently takes ≥ 6 weeks to obtain microbiological confirmation of TB infection. Hospitalized TB patients who are not suspected as having this diagnosis are potential sources of secondary, nosocomial spread throughout the hospital environment during this period. In this study of 937 persons with culture-proven pulmonary TB disease who received care at ten hospitals in Chicago, Los Angeles, or southern Florida, 15% were not placed in respiratory isolation rooms on the first day of hospital admission. Even after adjustment for clinical and sociodemographic characteristics, TB patients treated at public hospitals were twice as likely as those treated at private hospitals to be placed in pulmonary isolation, despite the fact that the odds of suspecting TB were similar. In interpreting our findings, several factors should be considered.

First, studies from the 1980s and early 1990s found that 30 to 40% of patients hospitalized with pulmonary TB were not placed in respiratory isolation rooms early in the hospitalization.15 Delays in isolation were attributed primarily to subtle disease presentations on chest radiographs. Similar rates of nonuse of pulmonary isolation rooms were noted in our study of TB care during 1996 to 1999. Moreover, 13% of TB patients with cavitary lung lesions on their admission chest radiograph, and 25% of TB patients who were AFB smear positive were not placed in pulmonary isolation rooms in the first hospital day. Our findings raise concern that nosocomial outbreaks of TB could recur in this recent era.

Second, we found that in comparison to private hospitals, public hospitals continued to have better rates of TB isolation, even though as a whole the rates of TB suspicion were similar for the two types of hospitals. All public hospitals in this study had high rates of TB suspicion and high-to-moderate TB isolation rates (Table 1). Private hospitals tended to have a more lax approach to TB isolation, even when TB suspicion rates were very high (as characterized by group 1 types of hospitals). These finding persisted even for high-risk patients. While two thirds of public hospitals had high rates of TB isolation, and none had low rates of TB isolation for high-risk patients, only one of seven private hospitals (14%) had high rates of TB isolation for these patients, and most private hospitals (57%) had low rates of TB isolation for high-risk patients (Table 1). We recognize that public hospitals provide care for the largest numbers of high-TB-risk individuals, individuals who are HIV infected, drug users, homeless, and/or who are from foreign countries. In the late-1980s, public hospitals, with high TB caseloads and more TB experience than the nonpublic hospitals, were the setting for the majority of nosocomial outbreaks of MDR-TB.456710 However, even after adjustment for high-risk clinical characteristics, the odds of early use of TB isolation for inpatients with pulmonary TB were twice as great at public vs private hospitals.

Third, variations in hospital practices, rather than case-mix differences, appear to account for our findings. The infection control program at one public hospital in our study established policies of ordering pulmonary isolation for all HIV-infected individuals with an abnormal chest radiograph finding, obtaining chest radiographs for all adults admitted through the emergency department, and subsequently placing into pulmonary isolation all persons with suspicious radiographic findings who were admitted from the emergency department. Concurrent capital allocation expenditures allowed the hospital to build more negative-pressure isolation rooms. Following these changes, staff purified protein derivative conversion rates were < 0.5% vs the 1.6% rate noted in the early 1990s; 77 to 100% of potential TB exposures were limited to the emergency department vs 0 to 13% in the early 1990s; and TB suspicion and isolation rates were > 90%, the highest of any hospital in our study (D. Droller, MD; personal communication; August 5, 2002). At the other two public hospitals in our study, infection control programs, in addition to the use of pulmonary isolation rooms, also closely monitored AFB sputum orders. In contrast, although the private hospitals in our study cities reported high numbers of properly ventilated pulmonary isolation rooms and that hospital personnel used type N95 TB respirators when providing care for individuals with suspected TB, no specific infection control AFB monitoring programs were in effect during the study period. We have previously reported that between 1992 and 1996 at these private hospitals, on average the rates of TB skin conversions of hospital personnel had tripled at one of the private hospitals, a nurse acquired pulmonary TB with a multidrug-resistant isolate during a nosocomial outbreak of TB.2122 Our findings raise concern that, at private hospitals in cities with large numbers of TB cases, the absence of specific AFB monitoring efforts and a failure to place many individuals in pulmonary isolation for whom AFB smears had been ordered may have important adverse consequences for both hospital personnel and patients.

Fourth, our findings suggest hospital-level TB practice patterns are influenced by resource limitations. In a perfect world, TB suspicion and TB isolation for patients subsequently shown to have culture-proven TB would be timely, and best practices would call for TB isolation for all patients undergoing diagnostic evaluation for TB. In this study, the three county hospitals come closest to this ideal, and as a group would be expected to have low risk for nosocomial transmission of TB. We hypothesize that resource limitations impact on the ability of a hospital to approximate best practices, and recognize that preferential isolation of high-risk patients is likely to be the more cost-effective approach to TB evaluation at these hospitals. Hospital E, a public hospital with by far the greatest TB caseload, epitomizes this practice. It maintains a high TB suspicion rate and an overall high rate of TB isolation for all cases, yet preferentially uses TB isolation for the high-risk patients.

The limitations of our study should be noted. First, the study is based on a sample of medical records from 10 hospitals in three regions of the United States. While these regions have large number of cases of TB in the United States, additional studies from other hospitals and regions are needed. Second, we reported rates of TB isolation and AFB sputum evaluation among patients identified by discharge diagnosis of TB, rather than among persons identified by admission characteristics. However, similar results have been reported from patients in these study regions who were discharged with other pulmonary diagnoses.18

In conclusion, our data suggest that low rates of early use of TB isolation rooms at private hospitals continued into the late 1990s and raise concern that private hospitals may need a wake-up call. In particular, as recommended by the ATS and the CDC, all patients admitted to hospitals with a diagnosis other than TB, but for whom TB is an etiologic concern, should undergo prompt assessment of their risk for active TB. Our findings suggest that it is the "low-risk" culture-positive patients who are least likely to be placed in TB isolation. Therefore, we advocate that all patients in whom TB is suspected should be placed in respiratory isolation, and diagnostic studies, including chest radiography, collection of sputum for AFB smear and culture, and tuberculin skin testing, should be performed.1617 Good infection control practices and continued heightened vigilance are essential to the prevention of nosocomial TB outbreaks.


   Acknowledgements
 
The authors thank the staffs of each of the hospitals who assisted with retrieval of TB data from microbiology records and identification of medical records for review.


   Footnotes
 
Abbreviations: AFB = acid-fast bacilli; AOR = adjusted odds ratio; ATS = American Thoracic Society; CDC = Centers for Disease Control and Prevention; CI = confidence interval; MDR-TB = multidrug-resistant tuberculosis; TB = tuberculosis

This study was supported in part by grants from the Chicago Community Trust and the National Institute of Drug Abuse (5RO1DA10628–02). Dr. Parada is a VA Career Development Award recipient.

Received for publication December 30, 2002. Accepted for publication August 19, 2004.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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  10. Fischl, MA, Uttamchandani, RB, Dalkos, GL, et al An outbreak of tuberculosis caused by multiple drug resistant tubercle bacilli among patients with HIV infection. Ann Intern Med 1992;117,177-183[CrossRef][ISI][Medline]
  11. Rao, VK, Iademarco, EP, Fraser, VJ, et al Delays in the suspicion and treatment of tuberculosis among hospitalized patients. Ann Intern Med 1999;130,404-411[Abstract/Free Full Text]
  12. Coronado, VG, Beck-Sague, C, Hutton, MD, et al Transmission of multidrug-resistant Mycobacterium tuberculosis among persons with human immunodeficiency virus infection in an urban hospital: epidemiologic and restriction fragment length polymorphism analysis. J Infect Dis 1993;168,1052-1055[ISI][Medline]
  13. Frieden, TR, Sherman, LF, Maw, KL, et al A multi-institutional outbreak of highly drug resistant tuberculosis: epidemiology and clinical outcomes. JAMA 1996;276,1229-1235[Abstract]
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  16. Centers for Disease Control and Prevention. Guidelines for preventing the transmission of Mycobacterium tuberculosis in health care facilities, 1994. Available at: www.cdc.gov/mmwr/preview/mmwrhtml/00035909.htm. Accessed October 26, 2004
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  19. Bennett, CL, Hounshell, JB, Chmiel, JS Hospital measures for prevention of tuberculosis transmission in U.S. cities with and without previous nosocomial tuberculosis outbreaks [letter]. Ann Intern Med 2000;133,486[Free Full Text]
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  21. Bennett, CL, Schwartz, D, Lane, DR, et al Variations in inpatient care for HIV-related tuberculosis patients during a recent nosocomial outbreak of multidrug-resistant tuberculosis [letter]. J AIDS 1999;21,348-349
  22. Horner, RD, Bennett, CL, Achenbach, C, et al Predictors of resource utilization for hospitalized patients with PCP: a summary of effects from the multi-city study of quality of PCP care. J AIDS 1996;12,379-385
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  24. Kim, B, Lyons, TM, Parada, JP, et al HIV-related Pneumocystis carinii pneumonia in older patients hospitalized in the early HAART era. J Gen Intern Med 2001;16,583-589[CrossRef][ISI][Medline]




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