Original Article
The Emergence of Drug-Resistant Tuberculosis in New York City
N Engl J Med 1993; 328:521-526February 25, 1993
- Abstract
Background
In the past decade the incidence of tuberculosis has increased nationwide and more than doubled in New York City, where there have been recent nosocomial outbreaks of multidrug-resistant tuberculosis.
Methods
We collected information on every patient in New York City with a positive culture for Mycobacterium tuberculosis during April 1991. Drug-susceptibility testing was performed at the Centers for Disease Control and Prevention.
Results
Of the 518 patients with positive cultures, 466 (90 percent) had isolates available for testing. Overall, 33 percent of these patients had isolates resistant to one or more antituberculosis drugs, 26 percent had isolates resistant to at least isoniazid, and 19 percent had isolates resistant to both isoniazid and rifampin. Of the 239 patients who had received antituberculosis therapy, 44 percent had isolates resistant to one or more drugs and 30 percent had isolates resistant to both isoniazid and rifampin. Among the patients who had never been treated, the proportion with resistance to one or more drugs increased from 10 percent in 1982 through 1984 to 23 percent in 1991 (P = 0.003). Patients who had never been treated and who were infected with the human immunodeficiency virus (HIV) or reported injection-drug use were more likely to have resistant isolates. Among patients with the acquired immunodeficiency syndrome, those with resistant isolates were more likely to die during follow-up through January 1992 (80 percent vs. 47 percent, P = 0.02). A history of antituberculosis therapy was the strongest predictor of the presence of resistant organisms (odds ratio, 2.7; P<0.001).
Conclusions
There has been a marked increase in drug-resistant tuberculosis in New York City. Previously treated patients, those infected with HIV, and injection-drug users are at increased risk for drug resistance. Measures to control and prevent drug-resistant tuberculosis are urgently needed.
Media in This Article
Figure 1
Survival among Patients Who Had Not Previously Received Antituberculosis Medications and Who Had Cultures That Grew M. tuberculosis in April 1991.Figure 2
Percentages of Patients in New York City Who Had Never Been Treated for Tuberculosis and Who Had Isolates Resistant to One or More Antituberculosis Medications, 1953 to 1991.Article Activity
- Article
After declining throughout the 20th century, the incidence of tuberculosis in the United States began to increase in the late 1980s1,2. The acquired immunodeficiency syndrome (AIDS) epidemic is believed to have had a central role in this rise3. In addition, homelessness, poverty, immigration, lack of an effective public health infrastructure, and limited access to medical care probably contributed to the increase4.
In New York City, the incidence of reported tuberculosis increased 132 percent from 1980 to 1990,5 and New York City reported 14 percent of all cases in the United States in 19902. In addition to an increasing incidence, there have been nosocomial outbreaks of tuberculosis caused by organisms resistant to multiple drugs6 and reports of increasing proportions of patients with drug-resistant Mycobacterium tuberculosis at two New York City hospitals7,8.
Drug resistance complicates efforts to control tuberculosis. Patients infected with organisms resistant to rifampin have a high rate of treatment failure when given the short course (six months) of therapy now standard in much of the United States9,10. Patients infected with organisms resistant to both isoniazid and rifampin require at least 18 months of therapy; some die of tuberculosis or continue to have active tuberculosis despite optimal therapy11,12. The effectiveness of preventive therapy in patients infected with drug-resistant M. tuberculosis organisms is unknown13.
Surveillance of drug resistance in the United States suggested stable or declining proportions of patients infected with resistant organisms from 1950 through 1986,14-17 but there are no national data for the years since 1986. We conducted a systematic survey of M. tuberculosis isolates to measure drug resistance among all patients in New York City who had a positive culture for M. tuberculosis in April 1991. We compared our results with those of earlier surveys in this city.
Methods
All patients in New York City with specimens from any anatomical site that grew M. tuberculosis in April 1991 were included in the survey. We included patients with previously positive cultures, those without such cultures, and patients whose specimens were collected in New York City but submitted or forwarded to laboratories outside the city. Only one isolate was included per patient; if a patient had more than one specimen that grew M. tuberculosis during April 1991, the isolate from the first positive specimen was collected.
Specimens for mycobacterial culture were collected at several hundred facilities in New York City, including municipal, voluntary, and proprietary hospitals; Department of Health clinics; and private physicians' offices. Such specimens were routinely sent to 1 of 71 laboratories that performed mycobacterial cultures, and when M. tuberculosis was identified, the isolates were forwarded to 1 of 24 laboratories that performed mycobacterial susceptibility testing. We contacted or visited every laboratory performing mycobacterial cultures to ensure that all cultures were collected; all mycobacteriology laboratories licensed to process specimens from New York City patients participated in the survey.
Laboratories submitted specimens on Lowenstein-Jensen medium to the New York City Department of Health laboratory, where they were coded and sent to the Centers for Disease Control and Prevention (CDC). At the CDC, species identification was confirmed by high-performance liquid chromatography,18 and susceptibility testing was performed by the proportion method with Middlebrook 7H10 medium19.
Clinical and demographic information on patients was obtained from multiple sources: laboratories submitting specimens, the New York City Department of Health Tuberculosis Control Bureau, the public-shelter registry, the New York City Health and Hospitals Corporation, and the New York City death-certificate registry. In addition to standard case investigations, additional medical-record reviews were performed by one of the authors or a trained investigator for all patients with no previous history of tuberculosis (to confirm that they had not previously received antituberculosis medications) and for patients with a history of taking antituberculosis medications who had drug-resistant isolates (to identify the date of their first treatment for tuberculosis and the results of susceptibility testing of their first isolate). Patients were considered either to have never been treated or to have received antituberculosis medications before their study culture was collected. Patients who were classified as having received antituberculosis medications before the culture was collected included those with relapses, patients who had recently begun treatment with antituberculosis drugs, inappropriately treated patients, and patients who did not comply with the treatment regimen. Patients were considered to have documented human immunodeficiency virus (HIV) infection only if they met the 1987 CDC case definition for AIDS or were documented to be HIV-seropositive. To determine the initial pattern of susceptibility among the patients with a history of antituberculosis treatment, we reviewed hospital laboratory records, Department of Health laboratory records, medical records, and the records of the Tuberculosis Control Bureau and reinterviewed all surviving patients who could be located. We assumed that every previously treated patient whose April 1991 specimen was susceptible to all drugs had an isolate that was initially susceptible. Reliable information on the patients' compliance with therapy was not available.
To obtain information on the date of death, we reviewed the tuberculosis and death registries for the period from April 1, 1991, through January 31, 1992. In an analysis of survival, we censored data on patients on the last documented date before they were lost to follow-up or died or at the end of the study period.
We compared the results of the current study with historical data, including a nationwide survey in which New York City participated during 1982 through 1984 (CDC: unpublished data). In that survey, cultures were forwarded to the CDC monthly from the New York City Department of Health laboratory, whereas in the current survey cultures were obtained from the Department of Health laboratory and all other New York City laboratories for the month of April 1991.
Categorical data were compared with the Mantel-Haenszel chi-square test or Fisher's exact two-tailed test. To compare continuous data, Student's t-test was used for normally distributed data; otherwise, the Wilcoxon two-sample test was used. Univariate and stratified analyses were performed with the Epi Info computer program, version 5.01b20. Multivariate analyses of the correlates of drug resistance (logistic regression) and risk factors for death (Cox proportional hazards) were performed21; the survival curves of different groups of patients with tuberculosis were compared with the Wilcoxon test. The results of multivariate analysis did not differ substantially from those of univariate analysis; the results of univariate analysis are presented here.
Results
Patients' Characteristics
During April 1991, 518 patients were identified as having positive cultures for M. tuberculosis in New York City (range, 0 to 77 patients per laboratory; median, 6). Among the 518 patients, isolates were available from 466. Of the 52 patients whose isolates were not available, 30 had isolates that could not be recovered by local laboratories, 18 had isolates that were nonviable, and 4 had isolates that were found to be contaminated on arrival at the CDC, including 1 that contained both M. tuberculosis and M. avium complex.
Clinical and demographic data were obtained for every patient and are summarized in Table 1Table 1
Characteristics of Patients with Culture-Documented Tuberculosis in New York City in April 1991.. Among the 242 patients with available isolates who were 30 to 44 years of age, HIV infection was documented in 61 of the 112 black men (54 percent), 28 of the 41 Hispanic men (68 percent), and 14 of the 21 white men (67 percent). The HIV status was documented to be negative in less than 10 percent of all patients. Among the patients with a history of antituberculosis treatment, one third had been treated for less than 2 months, one third for 2 to 14 months, and one third for more than 14 months. Fourteen patients had completed treatment for a previous episode of tuberculosis (i.e., they had relapses).Drug Resistance
Table 2Table 2
Proportion of Patients with Culture-Positive Tuberculosis in New York City in April 1991 Who Had Isolates Resistant to Antituberculosis Drugs. presents the proportion of patients with organisms resistant to antituberculosis medications. Overall, 33 percent had organisms resistant to one or more antituberculosis medications, 26 percent had organisms resistant to at least isoniazid, and 19 percent had organisms resistant to both isoniazid and rifampin. A history of treatment with antituberculosis medications was strongly associated with an increased risk of resistance. Rifabutin showed substantial cross-resistance with rifampin, with 65 percent of rifampin-resistant strains also showing resistance to rifabutin; no strain susceptible to rifampin was resistant to rifabutin.Isolates from the 18 patients with nonviable cultures were more likely to be resistant to one or more antituberculosis medications on testing in a local laboratory than were cultures from the 466 patients whose specimens were tested at the CDC (71 percent vs. 34 percent, P = 0.002).
Factors Associated with Drug Resistance
A history of antituberculosis treatment was the strongest predictor of drug resistance (Table 3Table 3
Factors Associated with Resistance to Antituberculosis Drugs among Patients with Positive Cultures for M. tuberculosis in New York City in April 1991.). Among the 227 patients who had not received antituberculosis therapy previously, resistance was more common in patients with documented HIV infection, with or without documented AIDS, and in patients with a reported history of injection-drug use. None of the following factors substantially altered the risk of drug resistance: the country of birth, immigration to the United States within the past 10 years, sex, area of residence, homelessness, race or ethnicity, or the presence of cavitary lung disease.Among the 239 patients who had received antituberculosis therapy, the susceptibility of the first isolate was established for 225; in the case of the remaining patients, either susceptibility testing was not performed or the records could not be retrieved. Of the 225 previously treated patients for whom information on initial susceptibility was available, 91 (40 percent) had resistant isolates in April 1991. Of these 91 patients, 55 (60 percent) had isolates resistant to one or more antituberculosis medications on their initial susceptibility test. (Of these 55 patients, 28 were alive and 24 were located and confirmed in an interview that the resistant isolate was from their first episode of tuberculosis.) Among the 170 patients with documented initial susceptibility to all antibiotics, drug resistance was found in 36 (21 percent). Acquired drug resistance was present in 7 percent of the patients who had been treated for tuberculosis for less than 2 months, 19 percent of the patients treated for 2 to 14 months, and 39 percent of the patients treated for more than 14 months (chi-square for linear trend, 18.34; P<0.001). Of the 14 patients with relapses, 11 had susceptible organisms. Cavitary lung disease was much more common in patients who had been treated with antituberculosis medications and was not independently associated with drug resistance.
Case Fatality Rate
Overall, 125 of the 466 patients (27 percent) died during the follow-up period, including 26 percent of the patients who had been treated previously and 27 percent of the patients who had never been treated. The presence of AIDS, increasing age (among patients without documented AIDS), and the presence of drug resistance (among patients with AIDS) were the most important predictors of mortality (Figure 1Figure 1
Survival among Patients Who Had Not Previously Received Antituberculosis Medications and Who Had Cultures That Grew M. tuberculosis in April 1991.). Among the cohort of patients who had never been treated, those with documented AIDS were more likely to die than were patients without documented AIDS (59 percent vs. 15 percent; relative risk, 4.0; 95 percent confidence interval, 2.6 to 6.0; P<0.001). Among patients without AIDS (including those who were HIV-seropositive), increasing age was associated with an increased case fatality rate (chi-square for linear trend, 7.66; P = 0.006); patients who were 35 years of age or older were 3.4 times more likely to die than those younger than 35 (20 percent vs. 6 percent; 95 percent confidence interval, 1.2 to 9.4; P = 0.01). Among patients with AIDS, those with resistant M. tuberculosis organisms were 1.7 times more likely to die than were those with drug-susceptible organisms (80 percent vs. 47 percent; 95 percent confidence interval, 1.1 to 2.5; P = 0.02). The case fatality rate was 91 percent (10 of 11 patients) among the patients with AIDS who were infected with organisms resistant to both isoniazid and rifampin.Discussion
For more than 30 years -- from 1950 through 1986 -- surveys documented stable or declining proportions of patients with drug-resistant tuberculosis in the United States14-17. In contrast, our 1991 survey documented both a high proportion of patients with tuberculosis caused by resistant organisms and a dramatic (130 percent) increase since the last survey eight years earlier in the proportion of patients in New York City who had never been treated for tuberculosis and who had resistant isolates (Figure 2Figure 2
Percentages of Patients in New York City Who Had Never Been Treated for Tuberculosis and Who Had Isolates Resistant to One or More Antituberculosis Medications, 1953 to 1991.). This trend is similar to that documented in parts of the developing world22-25 and reflects the lack of effective mechanisms to ensure that patients who begin treatment complete treatment.The most directly comparable historical data for untreated patients are from 1982 through 1984. Among such patients, the proportion with isolates resistant to one or more antituberculosis medications increased from 10 percent in 1982 through 1984 to 23 percent in 1991 (P = 0.003), the proportion with isolates resistant to isoniazid increased from 9 percent to 15 percent (P = 0.13), the proportion with isolates resistant to rifampin increased from 3 percent to 9 percent (P = 0.02), and the proportion with isolates resistant to both isoniazid and rifampin increased from 3 percent to 7 percent (P = 0.07).
Previous treatment,26,27 recent immigration to the United States,28 and cavitary lung disease29,30 have been associated with drug resistance. Previous treatment was by far the most important predictor of drug resistance in our study. This highlights the critical importance of obtaining a thorough history of previous treatment from all patients suspected of having tuberculosis and of having physicians contact local health authorities to determine patients' treatment status. Although the proportion of immigrants with tuberculosis who had drug resistance in our study was similar to that in Barnes' survey,28 the proportion was comparable to that for nonimmigrants in New York City; therefore, we did not find that recent immigration increased the risk of drug resistance. In our series, cavitary lung disease was a marker for previous treatment but not an independent risk factor for resistance.
We found that documented HIV infection was associated with a higher proportion of drug resistance in patients who had never been treated, a connection suggested previously in several reports31,32. However, few patients had documented negative HIV serologic results, and some patients without documented HIV infection may actually have been HIV-seropositive. There are at least three possible explanations for this increased risk. First, HIV-infected patients may be more likely to be exposed to infectious patients with resistant isolates and therefore to be infected, or reinfected, with resistant organisms. For example, HIV-seropositive injection-drug users may be infected with M. tuberculosis by other injection-drug users who have tuberculosis and in whom drug resistance has developed because of noncompliance with the treatment regimen. Second, HIV-seropositive patients infected with resistant M. tuberculosis organisms may be more likely to have progression to active disease than immunocompetent patients infected with resistant organisms (i.e., resistant organisms may be less likely than susceptible organisms to cause clinical disease in immunocompetent patients). Third, the higher proportion of drug resistance in HIV-infected persons may reflect more recent infection in these patients, in whom the disease progresses more rapidly after infection than in persons without HIV infection33. Thus, the patterns of drug resistance in HIV-seropositive patients may be a harbinger of future patterns in all patients with tuberculosis.
A surprisingly high proportion (51 percent) of patients had received antituberculosis medications, suggesting that current treatment strategies may be ineffective. Although some studies have assumed that previously treated patients with resistant isolates had acquired drug resistance, we found that the high proportion of previously treated patients with drug-resistant isolates represented a combination of patients with acquired drug resistance and those initially infected with resistant isolates. In fact, approximately 60 percent of the patients who had been treated before and whose isolates were drug-resistant had a drug-resistant first isolate. Although all drug resistance can ultimately be traced to inappropriate medical therapy or noncompliance with the treatment regimen, in April 1991, most patients with drug-resistant isolates in New York City had drug resistance because they were initially infected with resistant organisms.
The demographic profile of the patients in this survey was similar to that of all patients with tuberculosis in New York City5. The high prevalence of documented HIV infection (42 percent) is consistent with epidemiologic data that suggest that the HIV and tuberculosis epidemics are closely interrelated in New York City and elsewhere34,35.
Our study has several limitations. First, we studied only patients with documented positive cultures, not those with negative cultures or those from whom no culture was obtained. Second, nonviable specimens were more likely to be resistant than viable specimens on testing in a local laboratory. Thus, there may have been a slight selection bias against resistant isolates; the actual proportion of patients with resistant isolates may be 1 to 2 percent higher than the one reported in this investigation. Third, some patients identified as never having been treated may have had previous therapy that was not identified. However, our investigation of each case was at least as thorough as that done in previous studies. Since earlier studies may have misclassified some previously treated patients as never having been treated, the observed increase in drug resistance in untreated patients is probably a minimal estimate of the magnitude of this increase. Finally, the isolate we considered to be the initial isolate of previously treated patients may not have been their first, despite our extensive efforts to document this.
More than 25 percent of the patients with tuberculosis in this survey died in less than 12 months of follow-up. Patients with AIDS were more likely to be infected with resistant organisms and were also more likely to die if infected with these organisms. The high case fatality rate among patients not documented to have AIDS may reflect unrecognized HIV infection. The higher risk of death among patients with AIDS and resistant organisms suggests that tuberculosis may have been an important causal factor in many of these deaths. However, not all deaths in patients with tuberculosis are caused by tuberculosis; this investigation did not control for the degree of immunosuppression in these patients and was not designed to determine the mortality attributable to tuberculosis. An additional study to address this question is under way.
Increased transmission of drug-resistant M. tuberculosis has major public health implications. More than 25 percent of the patients with infectious tuberculosis in New York City with a documented positive culture in April 1991 could transmit isoniazid-resistant organisms, and nearly 20 percent could transmit organisms with resistance to both isoniazid and rifampin. These high proportions may change the risk-benefit ratio of preventive therapy with isoniazid in some cases36. The increasing incidence of resistance to rifampin is particularly troubling, since rifampin is essential to short-course therapy for tuberculosis9,10.
Patients with drug-resistant tuberculosis may have infectious disease for prolonged periods after treatment has begun and may therefore be more likely to infect others. This risk may be most apparent in facilities housing many immunocompromised persons, such as hospitals,37,38 prisons,39 homeless shelters,40 and residential drug-treatment programs41.
In response to the findings of this study, the New York City Department of Health has undertaken a series of control measures. It established ongoing mandatory surveillance of drug susceptibility, mandated timely laboratory testing of M. tuberculosis isolates for drug resistance, and recommended a four-drug treatment regimen (isoniazid, rifampin, pyrazinamide, and ethambutol) for all patients with newly diagnosed tuberculosis in New York City. Most importantly, the department is increasing efforts to ensure that patients complete therapy and is now recommending and implementing directly observed therapy, whereby patients are watched while they take each dose of medication,42 for patients with tuberculosis.
Tuberculosis is closely related to social factors such as substance abuse, poverty, and crowded living conditions. Similarly, a patient's ability to complete an antituberculosis regimen is affected by housing status, drug use, employment status, level of literacy, and other psychological and social phenomena43. Improvements in tuberculosis-control programs and in social and economic conditions are urgently needed and can promote the control of both tuberculosis and the emergence of drug-resistant organisms.
We are indebted to Gail Gerena, M.D., Kelly J. Henning, M.D., Robert A. Gunn, M.D., M.P.H., Robert C. Good, Ph.D., Lawrence Geiter, M.P.H., Laura J. Fehrs, M.D., Anite Mathieu, M.D., Irene Weitzman, Ph.D., Eduardo Netto, M.D., Kenneth R. Ong, M.D., Karen Brudney, M.D., Yelena Schuster, M.S., Jacques Mathieu, M.D., M.P.H., Craig Studer, M.A., Rebecca Tudryn, B.A., Jerine Gadsden, B.A., Michael Williams, B.A., David Karp, M.T., and Eric Mayr, M.T.; to the public health advisors of the New York City Tuberculosis Control Bureau; and to the technologists and laboratory directors in every mycobacteriology laboratory in New York City.
Source Information
From the Division of Field Epidemiology, Epidemiology Program Office (T.R.F.), the Division of Mycotic and Bacterial Diseases, National Center for Infectious Diseases (J.O.K.), and the Division of Tuberculosis Elimination, National Center for Prevention Services (G.M.C., S.W.D.), Centers for Disease Control and Prevention, Atlanta; the Division of Disease Intervention, New York City Department of Health, New York (T.R.F.); and Columbia-Presbyterian Medical Center, New York (T.S., A.P.-M.).
Address reprint requests to Dr. Frieden at 125 Worth St., Box 74, New York, NY 10013.
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