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(Chest. 2000;117:380-384.)
© 2000 American College of Chest Physicians

Nosocomial Tuberculosis Prevention Measures Among Two Groups of US Hospitals, 1992 to 1996*

Lilia P. Manangan, RN, MPH; Charles L. Bennett, MD, PhD; Nicole Tablan, BS; Dawn N. Simonds, BS; Gina Pugliese, RN, MS; Edgar Collazo, MD and William R. Jarvis, MD

* From the Hospital Infections Program (Mss. Manangan, Tablan, Simonds, and Drs. Collazo and Jarvis), National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA; Lakeside Veterans Affairs Hospital (Dr. Bennett), Chicago, IL; and the American Hospital Association (Ms. Pugliese), Chicago, IL.

Correspondence to: Lilia Manangan, RN, MPH, Investigation and Prevention Branch, Centers for Disease Control and Prevention, Mailstop E-69, 1600 Clifton Rd, Atlanta, GA 30333; e-mail: lpm2{at}cdc.gov


    Abstract
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Objective: To compare trends in nosocomial tuberculosis (TB) prevention measures and health-care worker (HCW) tuberculin skin test (TST) conversion of hospitals with HIV-related Pneumocystis carinii pneumonia (PCP) patients and other US hospitals from 1992 through 1996.

Design and setting: Surveys in 1992 and 1996 of 38 hospitals with PCP patients in four high-HIV-incidence cities and 136 other US hospitals from the American Hospital Association membership list.

Participants: Twenty-seven hospitals with PCP patients and 103 other US hospitals.

Results: In 1992, 63% of PCP hospitals and other US hospitals had rooms meeting Centers for Disease Control and Prevention (CDC) criteria (ie, negative air pressure, six or more air exchanges per hour, and air directly vented to the outside) for acid-fast bacilli isolation; in 1996, almost 100% had such isolation rooms. Similarly, in 1992, nonfitted surgical masks were used by HCWs at 60% of PCP hospitals and 68% at other US hospitals, while N95 respirators were used at 90% of PCP hospitals and 83% of other US hospitals in 1996. There was a significant decreasing trend in TST conversion rates among HCWs at both PCP and other US hospitals; however, this trend varied among all hospitals. HCWs at PCP hospitals had a higher risk of TST conversion than those at other US hospitals (relative risk, 1.71; p < 0.0001).

Conclusion: From 1992 through 1996, PCP and other US hospitals have made similar improvements in their nosocomial TB prevention measures and decreased their HCW TST conversion rate. These data show that most hospitals are compliant with CDC TB guidelines even before the enactment of an Occupational Safety and Health Administration TB standard.

Key Words: infection control • nosocomial • prevention • transmission • tuberculosis


    Introduction
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Since the resurgence of tuberculosis (TB) in the United States in 1985, numerous outbreaks of nosocomially transmitted Mycobacterium tuberculosis (MTB) have been investigated by the Hospital Infections Program, in conjunction with other Centers for Disease Control and Prevention (CDC) components, state and local health officials, and hospital personnel.1 2 3 4 Almost all of these outbreaks involved multidrug-resistant (MDR) strains of MTB and patients with HIV infection.5 The earliest episodes of nosocomial spread of MDR TB occurred in the late 1980s at several hospitals that provided care for large numbers of HIV and TB patients. In 1994 and 1995, a nosocomial outbreak of MDR TB occurred at a hospital that provided care for a large number of HIV patients and relatively few TB patients.6 7 Investigations1 2 3 have shown that incomplete implementation and/or compliance with CDC TB guidelines8 9 resulted in serious morbidity and mortality among patients and health-care workers (HCWs).

Although the reported number of persons with TB in the United States declined from 1992 through 1997,10 the transmission of MTB to patients and HCWs in hospitals is still a recognized risk. In 1997, the Occupational Safety and Health Administration (OSHA) published a proposed set of rules to prevent occupational MTB exposure because of concern that HCWs were not adequately protected.11 The objective of our study was to compare trends in nosocomial TB prevention measures and HCW tuberculin skin test (TST) conversion of hospitals with HIV-related Pneumocystis carinii pneumonia (PCP) patients and other US hospitals.


    Materials and Methods
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
In April 1992, we mailed questionnaires to the department of infection control of a 50% random sample (n = 38) of 76 hospitals that specialized in providing care to HIV patients in four high-HIV-incidence cities (New York, Chicago, Los Angeles, and Miami). These 76 hospitals had been providing care to patients with HIV-related PCP since 1987 and were randomly selected to participate in a separate study to investigate variations in quality of care for hospitalized patients with HIV-related PCP.12 These hospitals will be referred to as the "PCP hospitals."

To evaluate US hospitals without a specialized focus of HIV-patient care, we took a 50% random sample (n = 136) of 272 US hospitals at which six or more TB patient admissions were reported in 1991. We used six TB patient admissions as the cutoff because this number has been used in the CDC TB guidelines to classify facilities that had greater risk of nosocomial MTB transmission. These hospitals will be referred to as the "other US hospitals." These hospitals had participated in a larger survey conducted by the American Hospital Association and CDC in 1992, when questionnaires were mailed to the department of infection control of all public US hospitals (city, county, Veterans Administration, and primary medical school affiliated; n = 632) and a 20% random sample of all private hospitals with >= 100 beds (n = 444). This larger sample was derived from a 1990 American Hospital Association database of all US hospitals (including Puerto Rico).

In 1996, we mailed a questionnaire to the infection control practitioner of both PCP and other US hospitals who had responded to the 1992 survey. We followed up the nonresponding hospitals by telephone, fax, and/or mail three or more times.

In the surveys, we assessed the following two major areas of TB infection control measures: (1) engineering controls to facilitate the dilution and removal of infectious TB droplet nuclei and to prevent their spread; and (2) personnel health, ie, respiratory protection and TST programs for HCWs, including data on HCW TST conversion rates. In the questionnaire, we specifically asked whether TST results were recorded in a central registry, and we verified the validity of the TST data by calling the infection control personnel of hospitals that reported an unusual number of TSTs and/or TST conversions.

We also evaluated rates of HCW TST conversion among low TB and high TB caseload hospitals in the 27 PCP and the 103 other US hospital samples. In these analyses, we defined low TB caseload hospitals as those with fewer than six TB patient admissions in a specified year and high-TB caseload hospitals as those with six or more TB patients in a specified year.

Statistical Methods
All data were collected on standardized forms and analyzed using appropriate software (SAS Release 6.03 Edition; SAS Institute; Cary, NC and Epi Info; CDC; Atlanta, GA). We compared categorical variables using the Fisher’s Exact Test or likelihood ratio test as appropriate, and the continuous variables with Student’s t test or the Wilcoxon rank sum test. In calculating rates, we used the number of hospitals that provided a response to a specific question as the denominator.


    Results
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 Abstract
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 Materials and Methods
 Results
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Hospital Characteristics
The response rate was 71% for PCP hospitals (27/38) and 76% for the other US hospitals (103/136). Of the 130 respondents, 28 (22%) had <= 199 adult acute-care beds, 53 (41%) had 200 to 399 beds, and 42 (32%) had >= 400 beds; 43 were university-affiliated (33%), 30 were community teaching (23%), and 48 were community nonteaching hospitals (37%).

TB Admissions
The number of hospitals to which TB patients were admitted remained stable from 1989 to 1996. While the median number of annual TB patient admissions ranged from 9 to 10 for PCP hospitals during the 8-year period, among the other US hospitals, the median decreased from 9 in 1989 to 4 in 1996. Sixty-four percent of the surveyed hospitals had fewer than six TB patient admissions in 1996.

From 1992 through 1996, probable patient-to-patient nosocomial MTB transmission was reported by 2 of 92 hospitals (2%). During that same period, 2 of 77 hospitals (3%) reported possible nosocomial MTB transmission to HCWs.

Engineering Controls and Respiratory Protection Programs
In 1992, 64% of the hospitals had rooms that met CDC criteria for acid-fast bacillus (AFB) isolation (ie, negative air pressure, six or more air exchanges per hour, and air directly vented to the outside; Table 1 ). The median number of AFB isolation rooms was 4 (range, 0 to 45 rooms). By 1996, the availability of rooms that met CDC criteria for AFB isolation had improved to 97%. In addition, the number of isolation rooms increased to a median of 10 rooms (range, 0 to 74 rooms). Other engineering controls also increased, including use of high-efficiency particulate air (HEPA) filters and routine checks of air pressure (Table 1) . Routine checks of air pressure ranged from ongoing (when a suspect or confirmed TB patient was in the room) to monthly (when no such patients were in the room).


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Table 1.. Comparison of PCP Hospitals and Other US Hospitals by Use of Engineering Controls and Respiratory Protection of HCWs, 1992 and 1996*

 
In 1992, nonfitted surgical masks were the primary means of respiratory protection for HCWs entering AFB isolation rooms at both groups of hospitals. By 1996, N95 respirators were the primary respiratory protective device used by HCWs (Table 1) .

TST Programs
All hospitals in our study had some form of TST screening for HCWs; 100% included nurses while 57% included attending physicians. From 1992 to 1996, there was a 30% increase in the number of hospitals that had TST programs maintaining yearly reports on TST results. Of these, 89% of PCP and 69% of other US hospitals provided data on TST conversions among HCWs. In 1996, HCWs in 68% of responding PCP hospitals (13/19) and 79% of responding other US hospitals (77/98) had two-step TST (ie, a second TST, 1 to 3 weeks after the first test, is administered to newly employed personnel without a documented negative TST during the 12 months before employment).

Between 1992 and 1996, there was a higher risk of TST conversion among HCWs at PCP hospitals than at other US hospitals (relative risk, 71; p < 0.0001) and a significant decreasing trend of HCW TST conversion rates at PCP hospitals (from 1.2% in 1992 to 0.43% in 1996; p < 0.001) and other US hospitals (from 0.43% in 1992 to 0.26% in 1996; p < 0.001; Table 2 ). The number of HCW TST conversions per hospital increased at the PCP hospitals with low TB caseloads, while this number decreased at the PCP hospitals with high TB caseloads. In contrast, the number of TST conversions per hospital decreased at other US hospitals with low TB caseloads, while this number increased at other US hospitals with high TB caseloads (Table 3 ).


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Table 2.. Comparison of PCP Hospitals and Other US Hospitals By TST Conversions Among HCWs, 1992 to 1996

 

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Table 3.. Comparison of PCP Hospitals and Other US Hospitals That Reported TST Conversions Among HCWs by Low and High TB Caseloads, 1992 to 1996*

 

    Discussion
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Nosocomial transmission of MTB remains a great threat to public health. The 1997 publication of the proposed TB standard by OSHA has heightened this awareness among HCWs, especially those at hospitals with TB patient admissions. Various ways to prevent nosocomial transmission of and occupational exposure to MTB have been published8 9 11 since the resurgence of TB in 1985. The efficacy of these guideline recommendations have been documented in several studies.13 14 15 However, the reports of several hospitals with large numbers of HIV patients experiencing outbreaks of MDR TB5 over the past decade raise concern that TB infection-control practices vary according to factors such as hospital caseloads of HIV and TB.

Other investigators have reported that, in 1994 and 1995, poor infection control practices at a hospital with a large number of HIV patients and a low TB caseload led to the first report of a severe outbreak of MDR TB in the United States since the late 1980s.6 7 TST conversions occurred in six nurses, four house-staff physicians, and one ward secretary, with one HCW (who had previously become HIV infected following an inhospital needle-stick injury) dying from MDR TB.6 7 The outbreak was attributed to various factors such as poor engineering controls and a failure to suspect TB in an HIV-infected patient with MDR TB who had new pulmonary symptoms and a normal chest radiograph at the time of admission.

The results of our study indicate that improvements in nosocomial TB prevention measures have been accompanied by a significant overall decrease in TST conversion rates among HCWs at PCP and other US hospitals. However, our study also suggests that the improvements in HCW TST conversion rate have not occurred uniformly. We found an increase in the number of TST conversions among HCWs at PCP hospitals with low TB caseloads between 1992 and 1996, an increase that was three times more than among other PCP and US hospitals. This finding highlights the difficulty in evaluating low HCW TST rates over time. These differences may be due to false-positive reactions, prevalence of Bacille of Calmette and Guerin use in HCWs, community exposure to TB, or exposure to TB patients in hospitals. The fact that this increase occurred at PCP hospitals with low TB caseloads suggest that it may be secondary to nonhospital exposures. On the other hand, it is possible that in these hospitals some TB patients may not be identified promptly as at high risk for TB and therefore not placed in AFB isolation. It has been documented that the key to preventing transmission of nosocomial MTB in hospitals is promptly placing suspected TB patients in proper isolation rooms.13 14 15

Our study had several limitations. First, our results are based on responses from hospital personnel at a sample of PCP hospitals in four high-HIV-incidence cities and other US hospitals with low HIV caseloads. Although these respondents may be representative of other hospitals with high or low HIV-patient caseloads, regional or other differences may exist. Second, while improvements have occurred in our study hospitals, it is not known how effective some of these improvements are. For example, of all the changes in TB-prevention engineering controls, one of the most marked was the increasing use of portable HEPA filter systems, which increased threefold among PCP hospitals and twofold at the other US hospitals. Such systems have been viewed as alternative and less costly ways to produce negative pressure in a room; however, although they were routinely used in one hospital, they were not effective in protecting against MTB transmission during the most recent nosocomial outbreak of MDR TB.16 Further studies are needed to assess the efficacy of portable HEPA filters in preventing MTB transmission to patients or HCWs. Third, the changes in TST conversion rates from 1992 through 1996 also have been accompanied by decreased numbers of TB patients in the general population, fewer inpatients with TB, and expansion of TST programs to include hospital personnel who have a lower risk of acquiring TB. Nonetheless, improved compliance with CDC TB guidelines almost certainly played a role in the decreased HCW TST conversion rates identified at PCP hospitals with high TB caseloads and at the other US hospitals in our study.

In summary, between 1992 and 1996, PCP and other US hospitals have made similar improvements in preventing transmission of nosocomial TB, even before completion of the new OSHA TB standard. This is consistent with findings of a similar study that most US hospitals are making progress in implementing the 1994 CDC TB guidelines.17 These improvements have contributed to a safer workplace for HCWs and to the decreasing trend in TB patients in the United States. However, further studies are needed to accurately assess the risk factors of continued TST conversions among HCWs in hospitals and to assess the role nonhospital exposures play in HCW TST conversion.


    Footnotes
 
Abbreviations: AFB = acid-fast bacillus; CDC = Centers for Disease Control and Prevention; HCW = health-care worker; HEPA = high-efficiency particulate air; MDR = multidrug-resistant; MTB = Mycobacterium tuberculosis; OSHA = Occupational Safety and Health Administration; PCP = Pneumocystis carinii pneumonia; TB = tuberculosis; TST = tuberculin skin test

Received for publication May 4, 1999. Accepted for publication August 10, 1999.


    References
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Edlin, BR, Tokars, JI, Grieco, MH, et al (1992) An outbreak of multi-drug resistant tuberculosis among hospitalized patients with the acquired immunodeficiency syndrome. N Engl J Med 326,1514-1521[Abstract]
  2. Pearson, ML, Jereb, JA, Frieden, TR, et al (1992) Nosocomial transmission of multidrug-resistant Mycobacterium tuberculosis: a risk to patients and health-care workers. Ann Intern Med 117,191-196
  3. Beck-Sague, C, Dooley, SW, Hutton, MD, et al (1992) Hospital outbreak of multidrug-resistant Mycobacterium tuberculosis infections: factors in transmission to staff and HIV-infected patients. JAMA 268,1280-1286[Abstract]
  4. Coronado, VG, Beck-Sague, CM, Hutton, MD, et al (1993) 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 168,1052-1055[ISI][Medline]
  5. Jarvis, WR (1995) Nosocomial transmission of multidrug-resistant Mycobacterium tuberculosis. Am J Infect Control 23,146-151[CrossRef][ISI][Medline]
  6. Kenyon, TA, Rizdon, R, Luskin-Hawk, R, et al (1997) A nosocomial outbreak of multi-drug resistant tuberculosis. Ann Intern Med 127,32-36[Abstract/Free Full Text]
  7. Ridzon, R, Kenyon, T, Luskin-Hawk, R, et al (1997) Nosocomial transmission of human immunodeficiency virus and subsequent transmission of multi-drug resistant tuberculosis in a healthcare worker. Infect Control Hosp Epidemiol 18,422-423[ISI][Medline]
  8. . Centers for Disease Control and Prevention (1990) Guidelines for preventing the transmission of tuberculosis in health-care settings, with special focus on HIV-related issues. MMWR Morb Mortal Wkly Rep 39,RR-17
  9. . Centers for Disease Control and Prevention (1994) Guidelines for preventing the transmission of Mycobacterium tuberculosis in health-care facilities, 1994. MMWR Morb Mortal Wkly Rep 43,RR-13
  10. . Centers for Disease Control, and Prevention (1998) Tuberculosis morbidity–United States, 1997. MMWR Morb Mortal Wkly Rep 47,253-257[Medline]
  11. Occupational Safety, and Health Administration, Department of Labor. 29CFR Part 1910. Occupational exposure to tuberculosis: proposed rule. Federal Register 1997; 54160–54308
  12. Oken C, Archibald N, Cvitanic M, et al. Multi-city study of care for HIV-related Pneumocystis carinii pneumonia: successfully collecting highly sensitive information. Clin Perform Qual Health Care 1995; 140–146
  13. Maloney, SA, Pearson, ML, Gordon, MT, et al (1995) Efficacy of control measures in preventing nosocomial transmission of multidrug-resistant tuberculosis to patients and health care workers. Ann Intern Med 122,90-95[Abstract/Free Full Text]
  14. Wenger, PN, Otten, J, Breeden,, et al (1995) Control of nosocomial transmission of multidrug-resistant Mycobacterium tuberculosis among health care workers and HIV-infected patients. Lancet 345,235-240[CrossRef][ISI][Medline]
  15. Stroud, LA, Tokars, JI, Grieco, MH, et al (1995) Evaluation of infection control measures in preventing the nosocomial transmission of multidrug-resistant Mycobacterium tuberculosis in a New York City hospital. Infect Control Hosp Epidemiol 16,141-147[ISI][Medline]
  16. Bennett, CL, Schwartz, D, Lane, DR, et al (1999) Variations in inpatient care for HIV-related TB patients during a recent nosocomial outbreak of MDRTB. J Acquir Immune Defic Syndr Hum Retrovirol 21,348-349
  17. Manangan, LP, Simonds, DN, Pugliese, G, et al (1998) Are US hospitals making progress in implementing guidelines for prevention of Mycobacterium tuberculosis transmission? Arch Intern Med 158,1440-1444[Abstract/Free Full Text]



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