Original Article
An Outbreak of Multidrug-Resistant Tuberculosis among Hospitalized Patients with the Acquired Immunodeficiency Syndrome
N Engl J Med 1992; 326:1514-1521June 4, 1992
- Abstract
- Abstract
Background
Since 1990 several clusters of multidrug-resistant tuberculosis have been identified among hospitalized patients with the acquired immunodeficiency syndrome (AIDS). We investigated one such cluster in a voluntary hospital in New York.
Methods.
We compared exposures among 18 patients with AIDS in whom tuberculosis resistant to isoniazid and streptomycin was diagnosed from January 1989 through April 1990 (the case patients) with exposures among 30 control patients who had AIDS and tuberculosis susceptible to isoniazid, streptomycin, or both. We also compared exposures among the 14 case patients hospitalized during the six months before the diagnosis of tuberculosis (the exposure period) with those among 44 control patients with AIDS matched for duration of hospitalization. Mycobacterium tuberculosis isolates were typed with analysis of restriction-fragment–length polymorphism (RFLP).
Results.
Case patients with drug-resistant tuberculosis were significantly more likely than controls with drugsusceptible tuberculosis to have been hospitalized during their exposure periods (14 of 18 vs. 10 of 30) (odds ratio, 7.0; 95 percent confidence interval, 1.6 to 36; P = 0.006). Case patients hospitalized during their exposure periods were significantly more likely to have been hospitalized on the same ward as a patient with infectious drug-resistant tuberculosis than were either controls with drug-susceptible tuberculosis hospitalized during their exposure periods or controls matched for duration of hospitalization (13 of 14 vs. 2 of 10 and 23 of 44) (odds ratio, 52; 95 percent confidence interval, 3.1 to 2474; P<0.001; and odds ratio, ∞; 95 percent confidence interval, 2.4 to ∞; P = 0.005, respectively). Among those hospitalized on the same ward, the rooms of case patients were closer to that of the nearest patient with infectious tuberculosis than were the rooms of controls matched for duration of hospitalization. M. tuberculosis isolates from 15 of 16 case patients had identical patterns on RFLP analysis. Of 16 patients' rooms tested with air-flow studies, only 1 had the recommended negative-pressure ventilation.
Conclusions.
Multidrug-resistant tuberculosis is readily transmitted among hospitalized patients with AIDS. Physicians must be alert to this danger and must enforce adherence to the measures recommended to prevent nosocomial transmission of tuberculosis. (N Engl J Med 1992; 326:1514–21.)
Media in This Article
Figure 1
Distribution of Patients with Tuberculosis According to Pattern of Drug Resistance, AIDS Diagnosis, and Month of Collection of First Culture-Positive Specimen.Figure 2
Hospitalizations of Case Patients According to Ward.Article Activity
- Article
TUBERCULOSIS is an increasing cause of morbidity among persons with human immunodeficiency virus (HIV) infection in the United States.1 As the number of patients hospitalized with HIV infection and tuberculosis increases, the risk of nosocomial transmission of tuberculosis may rise. Moreover, HIV-induced immunosuppression may amplify the spread of tuberculosis in hospitals because it greatly increases the risk of rapid progression to active, infectious tuberculosis.2
In 1990 the first recognized clusters of primary multidrug-resistant tuberculosis among hospitalized patients with the acquired immunodeficiency syndrome (AIDS) in the United States were reported to the Centers for Disease Control (CDC).3 Twelve such clusters have been reported to date. One of them was detected at Roosevelt Hospital, a voluntary hospital in New York, where primary multidrug-resistant tuberculosis developed in seven patients with AIDS during a seven-month period. Several features of the outbreak increased the suspicion of hospital-acquired infection. None of the patients belonged to groups traditionally at high risk for tuberculosis, such as alcoholics, drug users, the foreign born, the indigent, or the homeless. All had primary multidrug resistance — that is, none had previously received antituberculosis therapy. And all had been hospitalized previously for other reasons.
This report describes the findings of our investigation of this cluster, undertaken to determine risk factors for disease, assess the probability of nosocomial transmission, find evidence of possible routes of such transmission, and estimate attack rates and incubation periods.
Methods
Case–Control Study 1
A case patient was defined as a patient with AIDS in whom tuberculosis was diagnosed at Roosevelt Hospital between January 1, 1989, and April 30, 1990 (the study period), and who had a Mycobacterium tuberculosis isolate resistant to at least isoniazid and streptomycin. For case–control study 1, all patients with AIDS in whom tuberculosis was diagnosed at the hospital during the study period and whose isolates were susceptible to isoniazid, streptomycin, or both were selected as controls. The date of diagnosis was defined as the date of collection of the first specimen from which M. tuberculosis was grown in culture. Hospital laboratory records were reviewed to identify all the patients who met the definition of case patient or control. A patient with tuberculosis resistant to isoniazid and streptomycin was considered to have had infectious disease for two weeks before and two weeks after the collection of sputum or bronchoalveolar-lavage fluid in which acid-fast bacilli were seen microscopically. Because the temporal clustering of cases suggested that case patients had progressed rapidly from infection to clinical disease, we defined the exposure period for a case patient or control as the 6-month interval immediately preceding the diagnosis of tuberculosis, but excluding the last 14 days.
Case–Control Study 2
In case–control study 2, case patients who had been hospitalized during their exposure periods were compared with patients with AIDS (with or without tuberculosis) who were matched according to the number of days of hospitalization during the case patient's exposure period. Three or four controls were matched to each case patient. Those who had received antimycobacterial drugs (e.g., for M. avium infection) or who had tuberculosis resistant to isoniazid or streptomycin were excluded.
Data Sources
The medical records of the case patients and controls were reviewed for demographic, clinical, and microbiologic data. The patients' room numbers for each day between July 1988 and June 1990 were obtained from computerized hospital records.
Laboratory Investigation
M. tuberculosis isolates were tested by the hospital laboratory for susceptibility to isoniazid, rifampin, streptomycin, and ethambutol. All available isolates that were reported to be resistant to two or more drugs and all available isolates from patients with AIDS were tested again at the CDC for susceptibility to antimicrobial drugs4 and for genetic similarity by analysis of restriction-fragment–length polymorphism (RFLP).5 These tests were performed by workers blinded to the patients' case or control status.
Air-Flow Studies
Smoke tubes were used in six hospital rooms where patients with tuberculosis had been isolated to determine the direction of air flow between the rooms and the adjacent hallway. Air supply and exhaust in 2 of these rooms and in another 10 rooms were measured with velometers. For the purposes of this investigation, negative pressure was considered to be present when measured exhaust exceeded measured supply by at least 20 percent.
Statistical Analysis
Group distributions were compared by the Wilcoxon rank-sum test, and proportions by the chi-square test or Fisher's exact test. Because the time between the diagnosis of AIDS and the diagnosis of tuberculosis was longer in the case patients than in the controls with drug-susceptible tuberculosis, a proportional-hazards model was constructed to adjust for the duration of AIDS. The case patients and controls were analyzed together as a retrospective cohort, followed from the time of the diagnosis of AIDS; hospitalization was analyzed as a time-dependent covariate for its effect on survival without multidrug-resistant tuberculosis. For this model, data were analyzed with use of conditional logistic regression.6 Data on matched case patients and controls were analyzed with use of conditional logistic regression for matched sets.6
Results
M. tuberculosis was isolated from 240 patients at Roosevelt Hospital from 1986 to 1990 (Fig. 1Figure 1
Distribution of Patients with Tuberculosis According to Pattern of Drug Resistance, AIDS Diagnosis, and Month of Collection of First Culture-Positive Specimen.). The number of cases of tuberculosis increased from 8 per quarter in 1986 to 24 in the first quarter of 1990. Overall, 96 of the 240 patients (40 percent) had AIDS, and an increase among those with AIDS (from 3 per quarter in 1986 to 15 in the first quarter of 1990) accounted for most of the increase in cases of tuberculosis. Cases of tuberculosis with resistance to two or more drugs increased from 1 of 32 (3 percent) in 1986 to 8 of 27 (30 percent) in the first third of 1990. Patients with AIDS accounted for the majority of the cases of tuberculosis with resistance to two or more drugs in 1989 and 1990 (20 of 23 patients). Tuberculosis with resistance to at least isoniazid and streptomycin occurred among 18 patients with AIDS in 1989 and 1990, as compared with only 3 such patients in the preceding three years.Characteristics of the Case Patients
Of the 18 patients who met the case definition, 17 were men, 16 of whom were homosexual or bisexual, and 10 were white (Table 1Table 1
Characteristics of Case Patients and Controls with AIDS and Drug-Susceptible Tuberculosis.). Their median age was 32.5 years (range, 24 to 44), and their median CD4+ lymphocyte count was 11.5 per cubic millimeter (0.115×109 per liter). The case patients had had AIDS for a median of five months when tuberculosis was diagnosed. All 18 had pulmonary tuberculosis; 6 also had extrapulmonary tuberculosis. In all 18, chest radiographs revealed infiltrates (17 patients), hilar or mediastinal lymphadenopathy (12), or pleural effusions (8). (In one patient there were no infiltrates, but M. tuberculosis grew in a culture of his sputum.) In 16 patients, acid-fast bacilli were seen in smears of sputum (10 patients) or bronchoalveolar-lavage fluid (4), lung aspirate (2), lymph-node—biopsy specimens (2), or pleural fluid (1); in only 2 patients were all smears for acid-fast bacilli negative. In the 13 patients with positive smears of sputum or bronchoalveolar-lavage fluid, the median time between admission and the order to isolate the patient was 6 days; the median period of infectiousness was 32 days. M. tuberculosis isolates from 15 case patients were resistant to rifampin (1 patient), ethambutol (2), or both (12), as well as isoniazid and streptomycin. The median length of survival after a diagnosis of multidrug-resistant tuberculosis was 19 weeks; 7 of the 18 case patients died during the hospitalization in which their tuberculosis was diagnosed. Survival was longer among the 7 patients who received at least two antituberculosis drugs other than isoniazid, rifampin, streptomycin, and ethambutol within two weeks after diagnosis (6 of these 7 [86 percent] survived 20 weeks, as compared with 2 of the 11 [18 percent] who did not receive such drugs within the same period; P = 0.01). Fourteen case patients had been hospitalized at Roosevelt Hospital during the six months before their diagnosis of tuberculosis, and 13 had been hospitalized on the same ward as a patient with infectious multidrug-resistant tuberculosis for at least one day during that time (Fig. 2Figure 2Hospitalizations of Case Patients According to Ward.).Case–Control Study 1
The 18 case patients and the 30 controls with drug-susceptible tuberculosis were similar in age, sex, race or ethnic group, and CD4+ lymphocyte count (Table 1). As compared with the controls, however, the case patients were more likely to be homosexual men, to have had AIDS longer when their tuberculosis was diagnosed, and to have been hospitalized at Roosevelt Hospital in the six months before their tuberculosis was diagnosed. After adjustment for HIV risk group in a logistic-regression model, the case patients remained significantly more likely than the controls to have been hospitalized in the six months before their tuberculosis was diagnosed (adjusted odds ratio, 5.0; 95 percent confidence interval, 1.1 to 22). In a proportional-hazards model with control for the duration of AIDS, the case patients were still more likely than the controls to have been hospitalized during their exposure periods (hazard ratio, 18; 95 percent confidence interval, 4.5 to 68).
We further examined the 14 case patients and 10 controls who had been hospitalized during their exposure periods for their proximity in space and time to patients with infectious multidrug-resistant tuberculosis. The case patients were significantly more likely than the controls to have been hospitalized on the same ward on the same day as a patient with infectious disease (Table 1). Being a homosexual man was associated with both hospitalization on the same ward and drug resistance; when the analysis was restricted to homosexual men, the association between hospitalization on the same ward and drug resistance remained significant (13 of 14 vs. 2 of 6) (odds ratio, 26; 95 percent confidence interval, 1.3 to 1374; P = 0.01).
Case–Control Study 2
In case–control study 2, the 14 case patients with hospitalizations during their exposure periods and the 44 controls matched for duration of hospitalization were similar in age, sex, race or ethnic group, HIV risk factors, CD4+ lymphocyte count, and duration of AIDS (Table 2Table 2
Characteristics of Case Patients Hospitalized during the Exposure Period and Controls with AIDS Matched for Duration of Hospitalization.). However, the case patients were significantly more likely than the controls to have been hospitalized on the same ward as a patient with infectious tuberculosis during the exposure period. Among patients hospitalized on the same ward, the case patients occupied rooms that were significantly closer to the room of the nearest patient with infectious disease than were those of the controls (Table 2).Days of such exposure were categorized according to whether isolation precautions for tuberculosis had been ordered for the patient with infectious tuberculosis on that day (Table 2). Hospitalization on the same ward as a patient in isolation for tuberculosis was significantly more frequent among the case patients than among the controls. Such exposure to a patient who was not in isolation was also more frequent among the case patients than among the controls, but this difference was not statistically significant. The case patients' exposures to patients not in isolation for tuberculosis most often occurred within a few days before isolation was ordered.
Laboratory Investigation
M. tuberculosis isolates from 16 case patients were available for examination by RFLP analysis; 13 yielded an identical pattern (Fig. 3Figure 3
Autoradiographs of RFLP Patterns of M. tuberculosis Isolates from Case Patients (Arrows) and Other Patients at Roosevelt Hospital.). One patient's isolate yielded a distinct pattern. Isolates from the remaining two patients gave conflicting results; in each, one isolate yielded the common case pattern, whereas another isolate yielded a distinct pattern. (The 16 patients included 13 who had been hospitalized before the diagnosis of tuberculosis; isolates from 12 of these patients had identical patterns; isolates from the other gave conflicting results. The one patient whose only isolate yielded a distinct RFLP pattern had not been hospitalized before diagnosis.)Isolates from 18 other patients at Roosevelt Hospital yielded patterns distinct from those of the case patients' isolates (Fig. 3). These other patients included eight of the controls with AIDS and drug-susceptible tuberculosis, five patients with AIDS and drug-susceptible tuberculosis diagnosed after April 1990, and five patients without AIDS who had multidrug-resistant (but not isoniazid- and streptomycin-resistant) tuberculosis.
Air-Flow Studies
Patients with known or suspected active pulmonary tuberculosis were isolated in any available private room. Air ducts supplied air to convectors located under the windows in each room. Air was exhausted from vents in each patient's bathroom directly out of the building without recirculation. Smoke-tube testing demonstrated positive pressure (outward air flow from the room to the adjacent hall) through part or all of the doorway in all six rooms tested. In three rooms, the air flowed inward at the bottom of the doorway and outward at the top. The air supply, as measured with velometers, exceeded measured exhaust in 10 of the 12 patients' rooms tested; in the remaining 2, exhaust exceeded supply by 12 percent and 32 percent, respectively. Smoke-tube testing in the first of these latter two rooms demonstrated air flow from the room to the adjacent hall at the top of the doorway. In sum, only 1 of 16 patients' rooms evaluated by smoke-tube testing or velometric air-flow measurements had negative pressure.
Attack Rate
Three hundred forty-six patients with AIDS were hospitalized on the same ward as one or more patients with infectious tuberculosis during the study period. In 13 of these patients, tuberculosis resistant to isoniazid and streptomycin was diagnosed at the hospital during the study period (Table 2). In an additional eight, tuberculosis resistant to isoniazid and streptomycin was diagnosed between May and December 1990 (after the study period had ended). Thus, by December 1990 the calculated attack rate among these patients was 6.1 percent (21 of 346 patients). Among patients whose hospital rooms were two rooms or less away from the room of a patient with infectious disease, the attack rate was 9.5 percent (18 of 189 patients).
Interval between Exposure and Diagnosis of Tuberculosis (Incubation Period)
The case patients' exposures to patients with infectious tuberculosis lasted days or weeks (Fig. 2); the day on which transmission occurred was not known. However, for 9 of 13 case patients with such exposures (69 percent), all the exposures occurred 30 to 105 days (1 to 3 1/2 months) before tuberculosis was diagnosed. For all 13, there was at least one day of exposure during this period. The case patients' incubation periods were artifactually limited by the time of observation (which was truncated at the end of the study period). We therefore examined incubation periods among the eight additional patients with AIDS who had exposures on the same ward during the study period and in whom tuberculosis resistant to isoniazid and streptomycin developed after the study period (i.e., between May and December 1990). Their incubation periods were somewhat longer: for six of the eight (75 percent), all the exposures occurred 50 to 182 days (1 1/2 to 6 months) before the diagnosis of tuberculosis; all had at least 1 day of exposure during this period.
Discussion
The transmission of multidrug-resistant tuberculosis from one inpatient to another in this New York hospital is strongly suggested by several lines of epidemiologic and laboratory evidence. The case patients were more likely than the controls to have been hospitalized at Roosevelt Hospital in the six months before their tuberculosis was diagnosed. Among those who had been hospitalized, the case patients were more likely than the controls to have been hospitalized on the same ward as a patient with infectious multidrug-resistant tuberculosis. Among those on the same ward, the case patients occupied rooms that were closer than controls' rooms to the room of the nearest patient with infectious disease. Finally, strains of M. tuberculosis from 15 of 16 case patients had identical DNA fingerprints by RFLP analysis. The inconsistent RFLP results in two patients may have been due to infection with two different strains or to laboratory cross-contamination. The 18 cases could not be attributed through a chain of transmission to a single index case (Fig. 2); in fact, 4 case patients had not been hospitalized before their admission for multidrug-resistant tuberculosis, including 2 with RFLP fingerprints matching those of the other patients. Nonetheless, the epidemiologic and molecular genetic data, taken together, provide strong evidence of nosocomial transmission of a single multidrug-resistant strain of M. tuberculosis.
Tuberculosis in persons with HIV infection has been thought to represent chiefly the reactivation of remotely acquired infection.7 This outbreak highlights the potential importance of tuberculosis due to newly acquired infection (primary tuberculosis).2 Active tuberculosis will develop in an estimated 3.3 percent of immunocompetent persons within the first year after a positive tuberculin skin test8; this progression from infection to active disease occurred in a larger proportion of our immunocompromised cohort during a shorter period. Our calculated attack rate should be considered a minimal estimate, because we do not know the number of exposed patients who died, were lost to follow-up, or were treated with antituberculosis drugs for M. avium infection before multidrug-resistant tuberculosis was diagnosed.
Mycobacterial drug resistance and host immunodeficiency may interact synergistically to potentiate the transmission of tuberculosis among patients with HIV infection in hospitals. Unrecognized drug resistance may increase the risk of nosocomial transmission if patients have infectious disease for weeks or months while they receive ineffective therapy pending the results of drug-susceptibility tests, or if isolation precautions are discontinued before a clinical and bacteriologic response to therapy has been demonstrated. At the same time, persons with HIV infection who have tuberculosis are often hospitalized in settings where they are in close contact with other immunocompromised patients with HIV infection. If tuberculosis infection is transmitted in this setting, the high attack rates and rapid progression from infection to disease that characterize tuberculosis in patients with HIV infection may accelerate person-to-person spread and perpetuate transmission. Recent outbreaks of tuberculosis in prisons,9 10 11 drug-treatment facilities,12 residential facilities for persons with HIV infection,13 and homeless shelters14 15 16 emphasize the alarming potential of HIV-induced immunosuppression to amplify the person-to-person spread of tuberculosis.
Guidelines for preventing the transmission of tuberculosis in hospitals have been published.3 , 17 The outbreak described in this report highlights the particular importance of several of these recommendations. In this investigation, patients with infectious tuberculosis posed a risk to other patients with AIDS on their wards despite isolation for tuberculosis. Incomplete adherence to isolation protocols by patients or hospital personnel may have accounted for this finding. Airflow studies suggested another possible explanation, however. Published guidelines recommend that patients with known or suspected active pulmonary or laryngeal tuberculosis be isolated in rooms with negative air pressure relative to corridors or other adjacent areas.17 Equal or positive pressure, found in 15 of the 16 patients' rooms tested in this hospital, may have allowed the airborne spread of infectious droplet nuclei into the corridor. The use of negative-pressure isolation rooms, although costly, is an important tool in preventing the spread of tuberculosis in hospitals.
Hospitalization on the same ward as a patient with infectious disease who was not in isolation was more than three times more common among the case patients than among the controls, although the association was not statistically significant. The majority of these exposures occurred within a few days before the report of a positive smear for acid-fast bacilli prompted the patient's isolation. Thus, although smears for acid-fast bacilli provided a diagnosis in 16 of the 18 case patients, patients with infectious tuberculosis who were not yet isolated may have posed an additional risk to patients on the same ward. This underscores the need for heightened clinical suspicion of infectious tuberculosis, prompt isolation of potentially infectious cases, and rapid reporting of the results of smears for acid-fast bacilli.17
A tuberculin-skin-test survey conducted among health care workers during this outbreak revealed skin-test conversions in 18 percent of the workers with previously negative skin tests, and one worker had tuberculosis resistant to isoniazid and streptomycin with an RFLP pattern that matched that of the case isolates (unpublished data). The pattern of skin-test conversions suggested an ongoing risk over time, rather than a recent increase in risk during the outbreak period. Routine, periodic skin testing of health care workers is necessary to identify newly infected workers so they can be offered preventive therapy and to alert infection-control personnel to the nosocomial transmission of tuberculosis to health care workers.17 Preventing tuberculosis in health care workers is important, both for the workers themselves and to prevent the transmission of tuberculosis from workers to patients.
Finally, recent increases in the incidence of multidrug-resistant tuberculosis, described in this and other reports3 , 18 19 20 (and unpublished data), underscore the particular importance of three additional published recommendations.3 , 17 First, hospitals and health departments where recent M. tuberculosis isolates have been resistant to antituberculosis drugs should conduct surveillance for drug-resistant M. tuberculosis. New cases of tuberculosis should be periodically tabulated according to the pattern of drug resistance and according to epidemiologic factors that may influence the likelihood of drug resistance, such as the presence of AIDS or HIV infection and the patient's history of hospitalization, previous treatment for tuberculosis, and country of origin. Second, these data should be used to guide initial therapy for patients with newly diagnosed tuberculosis.21 , 22 Conventional initial regimens are no longer appropriate for patients in the groups in which multidrug-resistant tuberculosis has now appeared. Third, physicians treating patients with tuberculosis should carefully monitor their patients' clinical and bacteriologic response to therapy and be attentive to the possibility of drug resistance. The control of multidrug-resistant tuberculosis is severely hampered by the long time required for definitive determinations of antimicrobial susceptibility; conventional methods require three to eight weeks for colony growth and then three to eight additional weeks for incubation with antimicrobial agents. More rapid methods of susceptibility testing are needed; until they are available, suspicion of drug resistance on epidemiologic and clinical grounds will remain essential for the control of drug-resistant tuberculosis.
Nosocomial multidrug-resistant tuberculosis is a cause of serious morbidity and mortality. The outbreak described in this report occurred in the context of three contributing factors that are present in a large number of urban hospitals in the United States — a rising number of hospitalized patients with AIDS, rising rates of tuberculosis in these patients, and incomplete adherence to published guidelines for preventing the transmission of tuberculosis. To date, 12 clusters of multidrug-resistant tuberculosis among patients with HIV infection have been reported to the CDC, all since 19903 (and unpublished data). Unrecognized nosocomial transmission is probably occurring in other institutions. Although multidrug resistance serves as an epidemiologic marker for the identification of clusters, drug-susceptible tuberculosis is transmitted under the same conditions. Thus, nosocomial transmission of tuberculosis is likely to remain a serious problem until effective preventive measures are brought to bear. Increased alertness on the part of clinicians and careful adherence to published guidelines3 , 17 are needed to prevent further nosocomial spread of the disease.
Presented in part at the 31st Interscience Conference on Antimicrobial Agents and Chemotherapy, Chicago, September 30, 1991.
We are indebted to Dr. Glen A. Satten for statistical advice, Fred R. Ingram for assistance in computer programming, and Dr. Angela T. Walker and Marco Pardi for other technical assistance.
Source Information
From the Division of HIV/AIDS (B.R.E., K.G.C., S.D.H.), the Hospital Infections Program (J.I.T., W.R.J.), and the Divsion of Bacterial and Mycotic Diseases (J.T.C., J.O.K.), National Center for Infectious Diseases, and the Division of Tuberculosis Elimination, National Center for Preventive Services (S.W.D.), Centers for Disease Control, Atlanta; and St. Luke's–Roosevelt Hospital Center, Columbia University College of Physicians and Surgeons, New York (M.H.G., J.W., E.M.S., K.R.O.). Address reprint requests to Dr. Edlin at Mailstop E-45, Centers for Disease Control, Atlanta, GA 30333.
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