Background In the past decade the incidence of tuberculosishas increased nationwide and more than doubled in New York City,where there have been recent nosocomial outbreaks of multidrug-resistanttuberculosis.
Methods We collected information on every patient in New YorkCity with a positive culture for Mycobacterium tuberculosisduring April 1991. Drug-susceptibility testing was performedat the Centers for Disease Control and Prevention.
Results Of the 518 patients with positive cultures, 466 (90percent) had isolates available for testing. Overall, 33 percentof these patients had isolates resistant to one or more antituberculosisdrugs, 26 percent had isolates resistant to at least isoniazid,and 19 percent had isolates resistant to both isoniazid andrifampin. Of the 239 patients who had received antituberculosistherapy, 44 percent had isolates resistant to one or more drugsand 30 percent had isolates resistant to both isoniazid andrifampin. Among the patients who had never been treated, theproportion with resistance to one or more drugs increased from10 percent in 1982 through 1984 to 23 percent in 1991 (P = 0.003).Patients who had never been treated and who were infected withthe human immunodeficiency virus (HIV) or reported injection-druguse were more likely to have resistant isolates. Among patientswith the acquired immunodeficiency syndrome, those with resistantisolates were more likely to die during follow-up through January1992 (80 percent vs. 47 percent, P = 0.02). A history of antituberculosistherapy was the strongest predictor of the presence of resistantorganisms (odds ratio, 2.7; P<0.001).
Conclusions There has been a marked increase in drug-resistanttuberculosis in New York City. Previously treated patients,those infected with HIV, and injection-drug users are at increasedrisk for drug resistance. Measures to control and prevent drug-resistanttuberculosis are urgently needed.
After declining throughout the 20th century, the incidence oftuberculosis in the United States began to increase in the late1980s1,2. The acquired immunodeficiency syndrome (AIDS) epidemicis believed to have had a central role in this rise3. In addition,homelessness, poverty, immigration, lack of an effective publichealth infrastructure, and limited access to medical care probablycontributed to the increase4.
In New York City, the incidence of reported tuberculosis increased132 percent from 1980 to 1990,5 and New York City reported 14percent of all cases in the United States in 19902. In additionto an increasing incidence, there have been nosocomial outbreaksof tuberculosis caused by organisms resistant to multiple drugs6and reports of increasing proportions of patients with drug-resistantMycobacterium tuberculosis at two New York City hospitals7,8.
Drug resistance complicates efforts to control tuberculosis.Patients infected with organisms resistant to rifampin havea 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 isoniazidand rifampin require at least 18 months of therapy; some dieof tuberculosis or continue to have active tuberculosis despiteoptimal therapy11,12. The effectiveness of preventive therapyin patients infected with drug-resistant M. tuberculosis organismsis unknown13.
Surveillance of drug resistance in the United States suggestedstable or declining proportions of patients infected with resistantorganisms from 1950 through 1986,14,15,16,17 but there are nonational data for the years since 1986. We conducted a systematicsurvey of M. tuberculosis isolates to measure drug resistanceamong all patients in New York City who had a positive culturefor M. tuberculosis in April 1991. We compared our results withthose of earlier surveys in this city.
Methods
All patients in New York City with specimens from any anatomicalsite that grew M. tuberculosis in April 1991 were included inthe survey. We included patients with previously positive cultures,those without such cultures, and patients whose specimens werecollected in New York City but submitted or forwarded to laboratoriesoutside the city. Only one isolate was included per patient;if a patient had more than one specimen that grew M. tuberculosisduring April 1991, the isolate from the first positive specimenwas collected.
Specimens for mycobacterial culture were collected at severalhundred facilities in New York City, including municipal, voluntary,and proprietary hospitals; Department of Health clinics; andprivate physicians' offices. Such specimens were routinely sentto 1 of 71 laboratories that performed mycobacterial cultures,and when M. tuberculosis was identified, the isolates were forwardedto 1 of 24 laboratories that performed mycobacterial susceptibilitytesting. We contacted or visited every laboratory performingmycobacterial cultures to ensure that all cultures were collected;all mycobacteriology laboratories licensed to process specimensfrom New York City patients participated in the survey.
Laboratories submitted specimens on Lowenstein-Jensen mediumto the New York City Department of Health laboratory, wherethey were coded and sent to the Centers for Disease Controland Prevention (CDC). At the CDC, species identification wasconfirmed by high-performance liquid chromatography,18 and susceptibilitytesting was performed by the proportion method with Middlebrook7H10 medium19.
Clinical and demographic information on patients was obtainedfrom multiple sources: laboratories submitting specimens, theNew York City Department of Health Tuberculosis Control Bureau,the public-shelter registry, the New York City Health and HospitalsCorporation, and the New York City death-certificate registry.In addition to standard case investigations, additional medical-recordreviews were performed by one of the authors or a trained investigatorfor all patients with no previous history of tuberculosis (toconfirm that they had not previously received antituberculosismedications) and for patients with a history of taking antituberculosismedications who had drug-resistant isolates (to identify thedate of their first treatment for tuberculosis and the resultsof susceptibility testing of their first isolate). Patientswere considered either to have never been treated or to havereceived antituberculosis medications before their study culturewas collected. Patients who were classified as having receivedantituberculosis medications before the culture was collectedincluded those with relapses, patients who had recently beguntreatment with antituberculosis drugs, inappropriately treatedpatients, and patients who did not comply with the treatmentregimen. Patients were considered to have documented human immunodeficiencyvirus (HIV) infection only if they met the 1987 CDC case definitionfor AIDS or were documented to be HIV-seropositive. To determinethe initial pattern of susceptibility among the patients witha history of antituberculosis treatment, we reviewed hospitallaboratory records, Department of Health laboratory records,medical records, and the records of the Tuberculosis ControlBureau and reinterviewed all surviving patients who could belocated. We assumed that every previously treated patient whoseApril 1991 specimen was susceptible to all drugs had an isolatethat was initially susceptible. Reliable information on thepatients' compliance with therapy was not available.
To obtain information on the date of death, we reviewed thetuberculosis and death registries for the period from April1, 1991, through January 31, 1992. In an analysis of survival,we censored data on patients on the last documented date beforethey were lost to follow-up or died or at the end of the studyperiod.
We compared the results of the current study with historicaldata, including a nationwide survey in which New York City participatedduring 1982 through 1984 (CDC: unpublished data). In that survey,cultures were forwarded to the CDC monthly from the New YorkCity Department of Health laboratory, whereas in the currentsurvey cultures were obtained from the Department of Healthlaboratory and all other New York City laboratories for themonth of April 1991.
Categorical data were compared with the Mantel-Haenszel chi-squaretest or Fisher's exact two-tailed test. To compare continuousdata, Student's t-test was used for normally distributed data;otherwise, the Wilcoxon two-sample test was used. Univariateand stratified analyses were performed with the Epi Info computerprogram, version 5.01b20. Multivariate analyses of the correlatesof drug resistance (logistic regression) and risk factors fordeath (Cox proportional hazards) were performed21; the survivalcurves of different groups of patients with tuberculosis werecompared with the Wilcoxon test. The results of multivariateanalysis did not differ substantially from those of univariateanalysis; the results of univariate analysis are presented here.
Results
Patients' Characteristics
During April 1991, 518 patients were identified as having positivecultures for M. tuberculosis in New York City (range, 0 to 77patients per laboratory; median, 6). Among the 518 patients,isolates were available from 466. Of the 52 patients whose isolateswere not available, 30 had isolates that could not be recoveredby local laboratories, 18 had isolates that were nonviable,and 4 had isolates that were found to be contaminated on arrivalat the CDC, including 1 that contained both M. tuberculosisand M. avium complex.
Clinical and demographic data were obtained for every patientand are summarized in Table 1. Among the 242 patients with availableisolates who were 30 to 44 years of age, HIV infection was documentedin 61 of the 112 black men (54 percent), 28 of the 41 Hispanicmen (68 percent), and 14 of the 21 white men (67 percent). TheHIV status was documented to be negative in less than 10 percentof all patients. Among the patients with a history of antituberculosistreatment, one third had been treated for less than 2 months,one third for 2 to 14 months, and one third for more than 14months. Fourteen patients had completed treatment for a previousepisode of tuberculosis (i.e., they had relapses).
Table 1. Characteristics of Patients with Culture-Documented Tuberculosis in New York City in April 1991.
Drug Resistance
Table 2 presents the proportion of patients with organisms resistantto antituberculosis medications. Overall, 33 percent had organismsresistant to one or more antituberculosis medications, 26 percenthad organisms resistant to at least isoniazid, and 19 percenthad organisms resistant to both isoniazid and rifampin. A historyof treatment with antituberculosis medications was stronglyassociated with an increased risk of resistance. Rifabutin showedsubstantial cross-resistance with rifampin, with 65 percentof rifampin-resistant strains also showing resistance to rifabutin;no strain susceptible to rifampin was resistant to rifabutin.
Table 2. Proportion of Patients with Culture-Positive Tuberculosis in New York City in April 1991 Who Had Isolates Resistant to Antituberculosis Drugs.
Isolates from the 18 patients with nonviable cultures were morelikely to be resistant to one or more antituberculosis medicationson testing in a local laboratory than were cultures from the466 patients whose specimens were tested at the CDC (71 percentvs. 34 percent, P = 0.002).
Factors Associated with Drug Resistance
A history of antituberculosis treatment was the strongest predictorof drug resistance (Table 3). Among the 227 patients who hadnot received antituberculosis therapy previously, resistancewas more common in patients with documented HIV infection, withor without documented AIDS, and in patients with a reportedhistory of injection-drug use. None of the following factorssubstantially altered the risk of drug resistance: the countryof birth, immigration to the United States within the past 10years, sex, area of residence, homelessness, race or ethnicity,or the presence of cavitary lung disease.
Table 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 239 patients who had received antituberculosis therapy,the susceptibility of the first isolate was established for225; in the case of the remaining patients, either susceptibilitytesting was not performed or the records could not be retrieved.Of the 225 previously treated patients for whom informationon initial susceptibility was available, 91 (40 percent) hadresistant isolates in April 1991. Of these 91 patients, 55 (60percent) had isolates resistant to one or more antituberculosismedications on their initial susceptibility test. (Of these55 patients, 28 were alive and 24 were located and confirmedin an interview that the resistant isolate was from their firstepisode of tuberculosis.) Among the 170 patients with documentedinitial susceptibility to all antibiotics, drug resistance wasfound in 36 (21 percent). Acquired drug resistance was presentin 7 percent of the patients who had been treated for tuberculosisfor less than 2 months, 19 percent of the patients treated for2 to 14 months, and 39 percent of the patients treated for morethan 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 hadbeen treated with antituberculosis medications and was not independentlyassociated with drug resistance.
Case Fatality Rate
Overall, 125 of the 466 patients (27 percent) died during thefollow-up period, including 26 percent of the patients who hadbeen treated previously and 27 percent of the patients who hadnever been treated. The presence of AIDS, increasing age (amongpatients without documented AIDS), and the presence of drugresistance (among patients with AIDS) were the most importantpredictors of mortality (Figure 1). Among the cohort of patientswho had never been treated, those with documented AIDS weremore likely to die than were patients without documented AIDS(59 percent vs. 15 percent; relative risk, 4.0; 95 percent confidenceinterval, 2.6 to 6.0; P<0.001). Among patients without AIDS(including those who were HIV-seropositive), increasing agewas associated with an increased case fatality rate (chi-squarefor linear trend, 7.66; P = 0.006); patients who were 35 yearsof age or older were 3.4 times more likely to die than thoseyounger than 35 (20 percent vs. 6 percent; 95 percent confidenceinterval, 1.2 to 9.4; P = 0.01). Among patients with AIDS, thosewith resistant M. tuberculosis organisms were 1.7 times morelikely 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 infectedwith organisms resistant to both isoniazid and rifampin.
Figure 1. Survival among Patients Who Had Not Previously Received Antituberculosis Medications and Who Had Cultures That Grew M. tuberculosis in April 1991.
The follow-up period ended January 31, 1992. Among the patients without documented AIDS (according to the 1987 CDC definition), those who were at least 35 years of age were more likely to die than those who were younger than 35 (P = 0.05). Among the patients with AIDS, those with drug-resistant isolates were more likely to die than those with drug-susceptible isolates (P = 0.002).
Discussion
For more than 30 years -- from 1950 through 1986 -- surveysdocumented stable or declining proportions of patients withdrug-resistant tuberculosis in the United States14,15,16,17.In contrast, our 1991 survey documented both a high proportionof patients with tuberculosis caused by resistant organismsand a dramatic (130 percent) increase since the last surveyeight years earlier in the proportion of patients in New YorkCity who had never been treated for tuberculosis and who hadresistant isolates (Figure 2). This trend is similar to thatdocumented in parts of the developing world22,23,24,25 and reflectsthe lack of effective mechanisms to ensure that patients whobegin treatment complete treatment.
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.
Data for 1953 include patients treated for up to six months14; data for 1980 and 1983 (CDC: unpublished data) are from CDC surveys that used the same laboratory for all analyses and the same criteria for resistance.
The most directly comparable historical data for untreated patientsare from 1982 through 1984. Among such patients, the proportionwith isolates resistant to one or more antituberculosis medicationsincreased from 10 percent in 1982 through 1984 to 23 percentin 1991 (P = 0.003), the proportion with isolates resistantto isoniazid increased from 9 percent to 15 percent (P = 0.13),the proportion with isolates resistant to rifampin increasedfrom 3 percent to 9 percent (P = 0.02), and the proportion withisolates resistant to both isoniazid and rifampin increasedfrom 3 percent to 7 percent (P = 0.07).
Previous treatment,26,27 recent immigration to the United States,28and cavitary lung disease29,30 have been associated with drugresistance. Previous treatment was by far the most importantpredictor of drug resistance in our study. This highlights thecritical importance of obtaining a thorough history of previoustreatment from all patients suspected of having tuberculosisand of having physicians contact local health authorities todetermine patients' treatment status. Although the proportionof immigrants with tuberculosis who had drug resistance in ourstudy was similar to that in Barnes' survey,28 the proportionwas comparable to that for nonimmigrants in New York City; therefore,we did not find that recent immigration increased the risk ofdrug resistance. In our series, cavitary lung disease was amarker for previous treatment but not an independent risk factorfor resistance.
We found that documented HIV infection was associated with ahigher proportion of drug resistance in patients who had neverbeen treated, a connection suggested previously in several reports31,32.However, few patients had documented negative HIV serologicresults, and some patients without documented HIV infectionmay actually have been HIV-seropositive. There are at leastthree possible explanations for this increased risk. First,HIV-infected patients may be more likely to be exposed to infectiouspatients with resistant isolates and therefore to be infected,or reinfected, with resistant organisms. For example, HIV-seropositiveinjection-drug users may be infected with M. tuberculosis byother injection-drug users who have tuberculosis and in whomdrug resistance has developed because of noncompliance withthe treatment regimen. Second, HIV-seropositive patients infectedwith resistant M. tuberculosis organisms may be more likelyto have progression to active disease than immunocompetent patientsinfected with resistant organisms (i.e., resistant organismsmay be less likely than susceptible organisms to cause clinicaldisease in immunocompetent patients). Third, the higher proportionof drug resistance in HIV-infected persons may reflect morerecent infection in these patients, in whom the disease progressesmore rapidly after infection than in persons without HIV infection33.Thus, the patterns of drug resistance in HIV-seropositive patientsmay be a harbinger of future patterns in all patients with tuberculosis.
A surprisingly high proportion (51 percent) of patients hadreceived antituberculosis medications, suggesting that currenttreatment strategies may be ineffective. Although some studieshave assumed that previously treated patients with resistantisolates had acquired drug resistance, we found that the highproportion of previously treated patients with drug-resistantisolates represented a combination of patients with acquireddrug resistance and those initially infected with resistantisolates. In fact, approximately 60 percent of the patientswho had been treated before and whose isolates were drug-resistanthad a drug-resistant first isolate. Although all drug resistancecan ultimately be traced to inappropriate medical therapy ornoncompliance with the treatment regimen, in April 1991, mostpatients with drug-resistant isolates in New York City had drugresistance because they were initially infected with resistantorganisms.
The demographic profile of the patients in this survey was similarto 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 theHIV and tuberculosis epidemics are closely interrelated in NewYork City and elsewhere34,35.
Our study has several limitations. First, we studied only patientswith documented positive cultures, not those with negative culturesor those from whom no culture was obtained. Second, nonviablespecimens were more likely to be resistant than viable specimenson testing in a local laboratory. Thus, there may have beena slight selection bias against resistant isolates; the actualproportion of patients with resistant isolates may be 1 to 2percent higher than the one reported in this investigation.Third, some patients identified as never having been treatedmay have had previous therapy that was not identified. However,our investigation of each case was at least as thorough as thatdone in previous studies. Since earlier studies may have misclassifiedsome previously treated patients as never having been treated,the observed increase in drug resistance in untreated patientsis probably a minimal estimate of the magnitude of this increase.Finally, the isolate we considered to be the initial isolateof 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 thissurvey died in less than 12 months of follow-up. Patients withAIDS were more likely to be infected with resistant organismsand were also more likely to die if infected with these organisms.The high case fatality rate among patients not documented tohave AIDS may reflect unrecognized HIV infection. The higherrisk of death among patients with AIDS and resistant organismssuggests that tuberculosis may have been an important causalfactor in many of these deaths. However, not all deaths in patientswith tuberculosis are caused by tuberculosis; this investigationdid not control for the degree of immunosuppression in thesepatients and was not designed to determine the mortality attributableto tuberculosis. An additional study to address this questionis under way.
Increased transmission of drug-resistant M. tuberculosis hasmajor public health implications. More than 25 percent of thepatients with infectious tuberculosis in New York City witha documented positive culture in April 1991 could transmit isoniazid-resistantorganisms, and nearly 20 percent could transmit organisms withresistance to both isoniazid and rifampin. These high proportionsmay change the risk-benefit ratio of preventive therapy withisoniazid in some cases36. The increasing incidence of resistanceto rifampin is particularly troubling, since rifampin is essentialto short-course therapy for tuberculosis9,10.
Patients with drug-resistant tuberculosis may have infectiousdisease for prolonged periods after treatment has begun andmay therefore be more likely to infect others. This risk maybe most apparent in facilities housing many immunocompromisedpersons, such as hospitals,37,38 prisons,39 homeless shelters,40and residential drug-treatment programs41.
In response to the findings of this study, the New York CityDepartment of Health has undertaken a series of control measures.It established ongoing mandatory surveillance of drug susceptibility,mandated timely laboratory testing of M. tuberculosis isolatesfor drug resistance, and recommended a four-drug treatment regimen(isoniazid, rifampin, pyrazinamide, and ethambutol) for allpatients with newly diagnosed tuberculosis in New York City.Most importantly, the department is increasing efforts to ensurethat patients complete therapy and is now recommending and implementingdirectly observed therapy, whereby patients are watched whilethey take each dose of medication,42 for patients with tuberculosis.
Tuberculosis is closely related to social factors such as substanceabuse, poverty, and crowded living conditions. Similarly, apatient's ability to complete an antituberculosis regimen isaffected by housing status, drug use, employment status, levelof literacy, and other psychological and social phenomena43.Improvements in tuberculosis-control programs and in socialand economic conditions are urgently needed and can promotethe control of both tuberculosis and the emergence of drug-resistantorganisms.
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., LawrenceGeiter, M.P.H., Laura J. Fehrs, M.D., Anite Mathieu, M.D., IreneWeitzman, 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., JerineGadsden, B.A., Michael Williams, B.A., David Karp, M.T., andEric Mayr, M.T.; to the public health advisors of the New YorkCity Tuberculosis Control Bureau; and to the technologists andlaboratory directors in every mycobacteriology laboratory inNew 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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A correction has been published: N Engl J Med 1993;329(2):148.
