Original Article
An Outbreak of Tuberculosis with Accelerated Progression among Persons Infected with the Human Immunodeficiency Virus — An Analysis Using Restriction-Fragment—Length Polymorphisms
N Engl J Med 1992; 326:231-235January 23, 1992
- Abstract
- Abstract
Background.
Tuberculosis typically develops from a reactivation of latent infection. Clinical tuberculosis may also arise from a primary infection, and this is thought to be more likely in persons infected with the human immunodeficiency virus (HIV). However, the relative importance of these two pathogenetic mechanisms in this population is unclear.
Methods.
Between December 1990 and April 1991, tuberculosis was diagnosed in 12 residents of a housing facility for HIV-infected persons. In the preceding six months, two patients being treated for tuberculosis had been admitted to the facility. We investigated this outbreak using standard procedures plus analysis of the cultured organisms with Restriction-Fragment Length polymorphisms (RFLPs).
Results.
Organisms isolated from all 11 of the culturepositive residents had similar RFLP patterns, whereas the isolates from the 2 patients treated for tuberculosis in the previous six months were different strains. This implicated the first of the 12 patients with tuberculosis as the source of this outbreak. Among the 30 residents exposed to possible infection, active tuberculosis developed in 11 (37 percent), and 4 others (13 percent) had newly positive tuberculin skin tests. Of 28 staff members with possible exposure, at least 6 had positive tuberculin-test reactions, but none had tuberculosis.
Conclusions.
Newly acquired tuberculous infection in HIV-infected patients can spread readily and progress rapidly to active disease. There should be heightened surveillance for tuberculosis in facilities where HIV-infected persons live, and investigation of contacts must be undertaken promptly and be focused more broadly than is usual. (N Engl J Med 1992;326:231–5.)
Media in This Article
Figure 1
Sequence of the Tuberculosis Outbreak in a Residential Facility for HIV-infected Patients.Figure 2
RFLPs of M. bovis BCG, M. intracellulare, and Clinical Mycobacterial Isolates from Residents of the HIV Congregate-Living Site.Article Activity
- Article
INFECTION with the human immunodeficiency virus (HIV) has had a substantial impact on the global epidemiology of tuberculosis.1 , 2 By causing a progressive and ultimately profound reduction in cell-mediated immunity, HIV infection increases the risk of tuberculosis through two pathogenetic mechanisms, both of which have been suggested by earlier reports.3 , 4 First, in persons previously infected with Mycobacterium tuberculosis, the immunologic mechanisms that contain the infection are sufficiently impaired to allow the organisms to proliferate and cause clinical disease. Second, whether or not there has been a previous infection, HIV-infected persons who are exposed to infectious tuberculosis may not be able to control a new infection; thus, clinical disease may develop quickly after exposure to M. tuberculosis. Because prevention strategies differ according to the sequence with which tuberculosis develops in HIV-infected populations, determining the mechanisms involved is important. If, for example, tuberculosis occurs in HIV-infected persons predominantly as a reactivation of latent infection, as it does in persons without HIV infection, the greatest emphasis should be placed on the identification of persons with latent infection and on their preventive treatment with isoniazid. Alternatively, if most cases of tuberculosis among persons with HIV infection are a consequence of the accelerated progression of new tuberculous infection, targeted surveillance of high-risk groups and prompt evaluation of contacts, together with preventive therapy, would have a larger overall epidemiologic impact. If both sequences occur, as is likely, preventive measures should be geared to both patterns of disease transmission and pathogenesis.
This report describes an outbreak of tuberculosis in a residential facility for HIV-infected persons. We used analysis of restriction-fragmentlength polymorphisms (RFLPs) to identify the strains of M. tuberculosis in the index patient and 11 subsequent patients with rapidly developing tuberculosis. The features of the outbreak provide insight into the pathogenesis of the disease in HIV-infected persons and raise a number of important issues concerning the control of tuberculosis in HIV-infected populations.
Methods
Review of Cases
The available medical records and the records of the Tuberculosis Case Registry related to the patients with tuberculosis were reviewed. Standard demographic data, information on methods of diagnosis, and results of laboratory investigations were abstracted.
Investigation of Tuberculosis Contacts
All patients with newly diagnosed tuberculosis were interviewed by disease-control investigators trained and experienced in the investigation of tuberculosis contacts. The information collected included the names of persons with whom the index patient had been in contact and the duration and circumstances of the exposure. In addition, patterns of air circulation within the facility were examined.
The residents and staff of the facility were given tuberculin skin tests by the Mantoux method, with 5 tuberculin units of commercial purified protein derivative of tuberculin (Aplisol, Parke-Davis, Morris Plains, N.J.). Intradermal tests for both mumps (40 colonyforming units per milliliter; Connaught, Swiftwater, Pa.) and candida (Dermatophyton "O" 1:100; Miles, West Haven, Conn.) were administered to residents of the facility (all of whom were known to be infected with HIV). For persons whose initial tuberculin skin tests were negative, the tests were repeated approximately 10 weeks after the discovery of the 11th secondary case of tuberculosis in the facility. For each of the antigens, a reaction ≥5 mm of induration was considered positive.
The residents of the facility were also evaluated with standard frontal- and lateral-view chest radiographs. The staff members of the facility underwent chest radiography only if they had positive tuberculin reactions.
Persons with abnormal findings on chest radiographs were evaluated in a standard fashion, with specimens from the respiratory tract being submitted for acid-fast staining and mycobacterial culture as well as for the identification of other respiratory pathogens. Standard laboratory procedures were used for the mycobacterial cultures, the determination of species, and testing of any organisms isolated for drug susceptibility.
A patient was considered to have tuberculosis if M. tuberculosis was isolated from any specimen or if there were symptoms and radiographic abnormalities of undetermined cause that responded to antituberculosis chemotherapy.
RFLP Analysis
M. tuberculosis strains isolated from the patients and from other, randomly selected patients during the time of the outbreak were obtained from Lowenstein—Jensen slant cultures from the laboratory of the San Francisco Department of Public Health. Reference strains from the American Type Culture Collection (ATCC) (Rockville, Md.) included the bacille Calmette–Guérin (BCG) strain of M. bovis (A. Jespersen strain, ATCC 27291), M. intracellulare (ATCC 13590), and M. avium (ATCC 25291). The organisms were grown for two to three weeks at 37°C in 15 ml of Middlebrook 7H9 broth supplemented with Tween 80, glycerol, and albumin—dextrose complex (Becton Dickinson, Cockeysville, Md.). Bacteria were collected by centrifugation, and chromosomal DNA was extracted with the method developed by van Soolingen et al. 5 Reaction mixtures containing 1 μg of genomic DNA were digested with 10 units of PvuII and electrophoresed on 1 percent agarose gels. After blotting, the membranes were hybridized with a 245-base-pair (bp) fragment of the insertion element IS986, and developed with use of enhanced chemoluminescence (ECL gene-detection kit, Amersham, Arlington Heights, Ill.).6
The Outbreak
The outbreak occurred in a congregate-living facility subsidized by the Department of Housing and Urban Development for HIV-infected persons in San Francisco. The facility was a 2 1/2-story structure with 32 private rooms and 8 shared bathrooms or lavatories. Two communal meeting rooms and a shared kitchen were located on the first floor. The structure was centrally heated by four forced-air residential-type gas furnaces with recirculation ducts. The furnaces had disposable filters of relatively low efficiency. Each bedroom had a heater vent; there were no exhaust inlets in the rooms. A return register was located in the corridor on each floor.
The periods during which the patients with tuberculosis resided in the facility and the time of their diagnoses are shown in Figure 1.Figure 1
Sequence of the Tuberculosis Outbreak in a Residential Facility for HIV-infected Patients. The first patient known to have tuberculosis (Patient 1) came to the facility in early July 1990. Pulmonary tuberculosis had been diagnosed on June 15, and the patient had been receiving antituberculosis treatment for approximately two weeks when he entered the site. A second patient with tuberculosis (Patient 2) entered the facility in November, having received antituberculosis chemotherapy since September, when pulmonary tuberculosis was diagnosed.Between December 1990 and April 1991, 12 additional residents were found to have tuberculosis. The first of these (Patient 3) entered the facility on November 1, 1990, and was hospitalized on December 19 after approximately three weeks of progressive respiratory symptoms. Acid-fast organisms were found by microscopical examination of a sputum sample, and M. tuberculosis was isolated from the same specimen. The patient did not return to the facility after his hospitalization.
After residing at the facility for 1/2 years, Patient 4 was hospitalized on January 19, 1991; for 1 week he had had nonproductive cough, fever, chills, and shortness of breath. Acid-fast bacilli were found in an induced-sputum specimen, and antituberculosis chemotherapy was begun. M. tuberculosis was isolated from the sputum, blood, and pleural fluid. The patient returned to the facility on February 5 but did not take his medications. He was hospitalized again on February 15; acid-fast organisms were again detected in his sputum, from which M. tuberculosis was subsequently isolated. Although his tuberculosis improved with treatment, Patient 4 died of sepsis involving Pseudomonas aeruginosa on March 10.
Between February 21 and March 4, three additional residents (Patients 5, 6, and 7) were found to have active pulmonary tuberculosis. Their infections were diagnosed in the course of hospitalizations for respiratory conditions.
Results
Investigation of Contacts
Thirty-one other residents were living in the facility when Patients 3 and 4 were living there. Of these 31, 18 were still living in the facility and had not yet been identified as having tuberculosis when the investigation of contacts took place. These 18 residents had tuberculin tests performed, of which 7 were positive and 1 was negative with positive control antigens. The remaining 10 residents were anergic. In addition, all the residents had chest radiography. Three of those with positive tuberculin reactions and two who were anergic were found to have tuberculosis (Patients 8, 9, 10, 11, and 12). None of the remaining 13 residents who were evaluated had evidence of active tuberculosis. All 13 were offered isoniazid, and 11 accepted this therapy.
Eight of the 31 residents were not evaluated in the investigation because they had moved from the facility. Of these, one was known to have had tuberculosis (Patient 13), one was dead of an unknown cause, three were alive with no evidence of tuberculosis, and no information was available for three.
The final patient with tuberculosis (Patient 14) was identified on April 4. In the course of the investigation he was found to be anergic and to have a normal chest radiograph. Although preventive therapy with isoniazid was recommended, in consultation with his physician he decided not to take the drug, because of markedly abnormal liver-function tests.
Each of the M. tuberculosis isolates was sensitive to all the primary antituberculosis agents.
Fourteen of the 28 staff members who had potentially been exposed to 1 or more of the 14 patients were evaluated in the outbreak investigation, and 4 had positive tuberculin reactions, one of which was a documented conversion. Five staff members had previously documented positive tuberculin tests and were not tested. The remaining 19 staff members had negative tuberculin reactions (9 were tested by private physicians). No cases of tuberculosis were found among them.
Repeat tuberculin testing was performed in early June 1991 for the residents and staff who had negative reactions on initial testing. There were no new reactions among the residents, but five of the staff members tested positive, whereas 10 weeks earlier they had been negative. No new cases of tuberculosis were identified.
RFLP Analysis
The RFLP patterns of the genomic DNA of M. bovis BCG, M. avium, M. intracellulare, and clinical mycobacterial isolates are shown in Figure 2Figure 2
RFLPs of M. bovis BCG, M. intracellulare, and Clinical Mycobacterial Isolates from Residents of the HIV Congregate-Living Site. (for Patients 1 through 7 and 9 through 14; Patient 8 had negative cultures) and Figure 3Figure 3
RFLPs of M. bovis BCG, M. avium, and Random Clinical Isolates of M. tuberculosis Obtained from Patients Identified in San Francisco at the Time of the Outbreak and Used as Controls. (random clinical isolates). The M. bovis BCG strain tested yielded an RFLP pattern containing two bands. However, other BCG strains have yielded from one to three bands under the same conditions.6 No M. avium or M. intracellulare restriction fragments hybridized with the M. tuberculosis probe. The mycobacteria isolated from the treated patients (Patients 1 and 2) had unique RFLP patterns, whereas those from the residents in whom tuberculosis was diagnosed between December and April had very similar patterns (Patients 3 to 14). The RFLP patterns of nine of the strains are identical. The slight difference in the patterns in Patients 9 and 11, as compared to the other nine patients starting with Patient 3, appears to be due to the movement of the insertion element. In contrast, all 13 randomly selected isolates of M. tuberculosis from San Francisco were found to have unique patterns (Fig. 3).Demographic and Clinical Data
The mean age of Patients 3 through 14 was 37.2 years (range, 26 to 49). Eleven patients were men; 8 were white, and 4 were black; and 11 were homosexual or bisexual, 3 of whom also used intravenous drugs. Injection drug use was the only HIV risk factor in the one woman. The results of tuberculin skin tests, CD4+ lymphocyte counts, acid-fast smears, and mycobacterial cultures for Patients 3 through 14 are shown in Table 1.Table 1
Immunologic and Microbiologic Data on the Patients with Tuberculosis.* No patient was known to have had a positive tuberculin skin test before the diagnosis, and six patients had had negative reactions documented previously. Three of these six had positive reactions at the time tuberculosis was diagnosed.In summary, tuberculosis developed in 10 of 29 residents (34 percent) who were exposed to Patient 3 or Patient 4. Beginning with Patient 3, the rate of new infections was 37 percent (11 of 30 residents). Tuberculosis did not develop in any of 28 staff members with exposures, although there were 6 with documented tuberculin conversions and 8 others had positive tuberculin reactions of unknown duration. Eight of the 12 cases occurred among the residents of the 15 rooms on the second floor. However, no specific features of the building's heating and ventilation system or of the residents' patterns of socialization were found to correlate with the risk of acquiring M. tuberculosis.
Discussion
The outbreak of tuberculosis described in this report shows that in HIV-infected patients, recently acquired tuberculosis infections can progress rapidly to cause tuberculosis. This pathogenetic sequence can be inferred from the report by DiPerri and coworkers,4 who examined a nosocomial outbreak of tuberculosis among 18 HIV-infected inpatients, 7 of whom had active disease within 60 days of exposure to the index patient. In the outbreak reported here, however, RFLP analysis was used to provide positive identification of strains and thus confirm that 11 patients had disease caused by a single strain. The contention that this outbreak represented a spread of infection from Patient 3 is strengthened by the failure to identify the same strain or similar strains among isolates from patients with tuberculosis selected at random from San Francisco at approximately the time of the outbreak. It is reassuring to note that isolates from the first two patients (Patients 1 and 2), who were being treated for tuberculosis when they entered the facility, bore no similarity to the strain associated with the outbreak. The finding that these two patients had unique RFLP patterns served to exclude them from consideration as sources and focused the investigation on Patient 3.
The usefulness of RFLP analysis as an epidemiologic tool has been suggested by work with other pathogens as well as with M. tuberculosis. 6 , 7 Because this method yields a kind of "fingerprint," strains can be tracked accurately. In the patients described in this report, nearly identical RFLP patterns were obtained with DNA probes derived from the insertion element IS986 (essentially the same as IS61lO).8 , 9 The similarity of the RFLP patterns, the temporal association of the onset of disease, or both clearly indicate that Patients 3 through 14 were epidemiologically connected. The slightly different patterns in Patients 9 and 11, thought to be due to movement of the insertion element, could have been caused by the transposition of the insertion element in a proportion of the organisms, resulting in a more weakly hybridizing 6-kb band.
Two features of this outbreak were striking. The first was the extraordinarily large number of tuberculous infections resulting from the exposure. In the United States, approximately 30 percent of the close contacts of newly identified patients with tuberculosis have positive tuberculin skin tests, indicative of infection with M. tuberculosis, presumably acquired from the index patient.10 In this outbreak in which all residents and staff members could be considered to be close contacts, the incidence of new, active tuberculosis, not just quiescent infection, was 37 percent among the HIV-infected residents, whereas no cases were identified among the staff members. The number of new infections among residents in whom the disease did not develop cannot be determined, because previous tuberculin-test results were generally not known. Given the high rate of anergy among the residents who did not have the disease (55 percent), it is likely that not all tuberculous infections were detected. However, 4 of the 18 people in whom tuberculosis did not develop had positive reactions to purified protein derivative detected during the course of the outbreak investigation, for a minimal overall rate of tuberculous infection among exposed HIV-infected patients of 50 percent (15 of 30). Among the 28 staff members, 6 had tuberculin-test conversions, 3 were tuberculin-positive without previous testing, and 5 were known to have had previous positive reactions, for an overall prevalence of positive reactions of 50 percent by the end of the outbreak. On the basis of these data, and assuming an artifactually low rate of positive skin-test reactions because of anergy, the acquisition of the organism by HIV-infected residents seems to have been facilitated.
The second striking feature of this outbreak was the high percentage of exposed people in whom tuberculosis developed and the rapidity with which it did so. Usually, new tuberculous infections are quiescent, with clinically evident tuberculosis developing within the first year after infection in only 3 to 5 percent of persons who acquire new infections.11 It is estimated that another 3 to 5 percent of the infected persons in whom disease does not develop in the first year will become ill with tuberculosis at some point in their lives. The total duration of this outbreak (from Patient 3 to Patient 14) was 106 days, and in one patient (Patient 7) disease developed within 4 weeks of exposure. This rapid progression suggests that the organisms proliferated very rapidly without the usual inhibition from specific cell-mediated immunity. Although the data are not presented, the clinical manifestations of tuberculosis in this outbreak were essentially those of primary tuberculosis. These features have commonly been described among HIV-infected patients with tuberculosis and have generally been ascribed to the lack of an immune response in the host rather than to the actual presence of progressive primary infection.
This outbreak presents a number of implications for the control of tuberculosis in HIV-infected populations. Clearly, prompt and thorough investigation of contacts is exceedingly important when tuberculosis is diagnosed in a person who is in contact with HIV-infected persons, whether or not the source patient is HIV-infected. The usual criteria for judging an exposed person's risk for acquiring tuberculous infection should be modified when that person is known or thought to be infected with HIV. In general, this will enlarge the scope of contact investigations.
In evaluating persons who are known or suspected to be infected with HIV and who are exposed to infectious tuberculosis, the value of skin testing with either tuberculin or control antigens is questionable. In this outbreak, little information was gained by skin testing. Among the patients, all the possible combinations of reaction patterns were found. Given a substantial exposure history, all the persons who have been in contact with the source patient, regardless of their skin-test reactions, should be offered preventive therapy with isoniazid if they have no clinical or chest radiographic evidence of tuberculosis. In view of the rapid progression from infection to disease, however, HIV-infected contacts must be carefully evaluated before preventive therapy with isoniazid is begun. If active tuberculosis has developed, treatment with isoniazid alone would be a major error. Besides the usual first step of tuberculin testing, persons with possible exposure should be asked about their symptoms and a chest radiograph should be obtained in those with HIV infection or at risk for it. If there is even suggestive evidence of active tuberculosis, therapy with multiple drugs should be initiated until the situation is clarified. It is noteworthy that Patients 1 and 2 came to the facility after receiving antituberculous therapy for a relatively short time, but they caused no secondary cases.
There should be heightened concern about the screening for tuberculosis of persons who are admitted to HIV care facilities, as well as the screening of employees. Moreover, surveillance for tuberculosis in such facilities should be maintained, and persons with suspicious symptoms should be evaluated promptly. The risks of acquisition of tuberculous infection should be made known to HIV-infected health care workers, and surveillance should be extended to them as well.
In patients with both tuberculous infection and HIV infection, limited data suggest that preventive therapy with isoniazid is effective.3 During this outbreak, tuberculosis did not develop in any of the residents taking isoniazid chemoprophylaxis. However, pulmonary tuberculosis did subsequently develop in one of the two patients who did not take isoniazid. At least in this outbreak, isoniazid seemed to be effective in preventing the rapid progression to tuberculosis.
Supported in part by an Institutional National Research Service Award (HL 07185), by a grant (AIZ6170) from the National Institutes of Health, and by the Howard Hughes Medical Institute.
We are indebted to Antonio Paz, Houmpheng Banouvong, Carlos Balladares, and Octavio Lumba for conducting the investigation of contacts; to Marilyn Girodo and Arthur Back for providing clinical isolates; to William Charney and Leonard Fisher for assessing the ventilation system; to Jack Crawford and Barry Bloom for their thoughtful comments; and to Peter W.M. Hermans and Jan van Embden for providing pAL5000 DNA, as well as technical assistance and guidance with the RFLP analysis.
Note added in proof: One staff member whose tuberculin reaction had been negative on initial testing but was positive on retesting in June has been found to have pulmonary tuberculosis with positive sputum cultures. The RFLP pattern of the organisms has not been determined as of this writing.
Source Information
From the Medical Service, San Francisco General Hospital Medical Center, and the Department of Medicine, University of California, San Francisco (C.L.D., G.F.S.. P.C.H.); the Howard Hughes Medical Institute and the Division of Geographic Medicine, Department of Medicine, Stanford University School of Medicine, Stanford, Calif. (P.M.S., G.K.S.); the Department of Public Health, City and County of San Francisco (G.F.S.); and the Howard Hughes Medical Institute and the Department of Microbiology and Immunology, Albert Einstein College of Medicine, New York (R.A.M., W.R.J.). Address reprint requests to Dr. Daley at the Chest Service, Rm. 5K1, San Francisco General Hospital, San Francisco, CA 94110.
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