Background The incidence of tuberculosis and drug resistanceis increasing in the United States, but it is not clear howmuch of the increase is due to reactivation of latent infectionand how much to recent transmission.
Methods We performed DNA fingerprinting using restriction-fragment-lengthpolymorphism (RFLP) analysis of at least one isolate from everypatient with confirmed tuberculosis at a major hospital in theBronx, New York, from December 1, 1989, through December 31,1992. Medical records and census-tract data were reviewed forrelevant clinical, social, and demographic data.
Results Of 130 patients with tuberculosis, 104 adults (80 percent)had complete medical records and isolates whose DNA fingerprintscould be evaluated. Isolates from 65 patients (62.5 percent)had unique RFLP patterns, whereas isolates from 39 patients(37.5 percent) had RFLP patterns that were identical to thoseof an isolate from at least 1 other study patient; the isolatesin the latter group were classified into 12 clusters. Patientswhose isolates were included in one of the clusters were inferredto have recently transmitted disease. Independent risk factorsfor having a clustered isolate included seropositivity for thehuman immunodeficiency virus (HIV) (odds ratio for Hispanicpatients, 4.31; P = 0.02; for non-Hispanic patients, 3.12; P= 0.07), Hispanic ethnicity combined with HIV seronegativity(odds ratio, 5.13; P = 0.05), infection with drug-resistanttuberculosis (odds ratio, 4.52; P = 0.005), and younger age(odds ratio, 1.59; P = 0.02). Residence in sections of the Bronxwith a median household income below $20,000 was also associatedwith having a clustered isolate (odds ratio, 3.22; P = 0.04).
Conclusions In the inner-city community we studied, recentlytransmitted tuberculosis accounts for approximately 40 percentof the incident cases and almost two thirds of drug-resistantcases. Recent transmission of tuberculosis, and not only reactivationof latent disease, contributes substantially to the increasein tuberculosis. .
After decades of decline, the incidence of tuberculosis in theUnited States began to increase in 1986, resulting in 52,000excess cases by 19921. New York City accounted for 14 percentof all cases of tuberculosis in the United States in 1992; thenumber of cases reported in the city has increased by over 150percent since 19792. This increase has been especially dramaticamong minorities and in specific areas.
The increase in tuberculosis has been attributed to coinfectionwith the human immunodeficiency virus (HIV),3,4 deteriorationof the public health infrastructure,5 social disruption includinghomelessness and drug abuse,5 and immigration6. A high reactivationrate of latent tuberculous infection in persons coinfected withHIV is thought to be the principal mechanism underlying thisphenomenon7. It is estimated that 90 percent of tuberculosiscases nationwide are due to the reactivation of latent, remoteinfection8. To reduce the risk of reactivation, tuberculosis-controlstrategies have emphasized preventive therapy in populationsat high risk for latent infection8.
Outbreaks of tuberculosis in a residence for patients with theacquired immunodeficiency syndrome (AIDS),9 in shelters,10,11and in hospitals12 show that transmission and rapid progressionto disease can occur in institutional settings. Increases intuberculosis among children13 indicate that transmission isoccurring in the community. There has been a growing recognitionthat social conditions in poor urban areas where tuberculosisremains prevalent, combined with high rates of HIV infection,may facilitate transmission of tuberculosis14. However, therelative contribution of recent transmission to the overallincidence of disease and the risk factors involved have notbeen established. In this study, we used molecular and epidemiologicmethods to assess these factors in one medical center in NewYork City.
The presence of repetitive genetic insertional elements in Mycobacteriumtuberculosis permits the identification of individual strainsby DNA fingerprinting with restriction-fragment-length polymorphism(RFLP) analysis and can be used to demonstrate the transmissionof particular M. tuberculosis strains in outbreaks9,15. Thistechnique, combined with medical-record review and analysisof census data, allowed us to investigate the microbiologic,clinical, social, and demographic factors associated with recentlytransmitted disease.
Methods
Patient Population
The study was performed at a 765-bed hospital that is the largestprovider of primary care to the 1.2 million residents of theBronx, a borough of New York City. The population served islargely poor, Hispanic, and black, but also includes middle-classwhites and minorities. The hospital also serves as a referralcenter for nearby counties. There have been no recognized outbreaksof nosocomially transmitted tuberculosis.
Accrual of Patients and Mycobacterial Samples
All patients who had at least one positive culture for M. tuberculosisfrom December 1, 1989, through December 31, 1992, were enrolledin the study. Each patient's medical records were reviewed witha standardized form, and one initial M. tuberculosis isolatewas selected for RFLP analysis and antimycobacterial-susceptibilitytesting. Thirteen isolates could not be subcultured: 11 werenonviable, 1 was contaminated, and 1 was lost. Patients wereconsidered to be infected with HIV only if they met the 1987definition of AIDS devised by the Centers for Disease Controland Prevention (CDC) or were documented to be seropositive,and they were considered to have AIDS only if they met the 1987CDC case definition. A patient's country of origin was not alwaysrecorded; consequently, patients were classified as either foreign-bornor not foreign-born (U.S.-born or of unknown origin). The hospital'smedical data base was used to provide a complete listing ofeach patient's previous hospitalizations at the institutionfrom mid-1984 until the end of the study period. The investigatorswere unaware of the individual RFLP patterns of the study patientswhen they reviewed the medical records. This study was approvedby the institutional review board of the hospital.
Analysis and Mapping of Census Blocks
Adults with tuberculosis who had confirmed Bronx addresses werelocated in specific census blocks and block groups (the smallestareas of census enumeration) with TIGER files, the comprehensivegeographic locator system developed by the U.S. Census and U.S.Geological Survey. Demographic, social, and household characteristicswere taken from the STF1 and STF3 reports, the major files ofthe 1990 U.S. Census. Mapping was done by the ATLAS/GIS mappingprogram. Fifteen patients were excluded from this analysis becausetheir medical records listed an address outside the Bronx, andone was excluded because the address given could not be confirmedas an existing street address.
Susceptibility Testing
Susceptibility testing was done with the CDC version of theproportion method16. Susceptibility data were not availablefor three isolates; this was reflected in the denominator usedin calculations involving drug resistance. A radiometric culturesystem (Bactec) was not used at the study hospital.
RFLP Analysis
RFLP analysis was performed according to previously describedmethods17. In brief, M. tuberculosis DNA was extracted, digestedwith PvuII, subjected to electrophoresis, and hybridized withSouthern blot techniques with a fragment of the insertion elementIS6110 measuring 245 base pairs and generated by the polymerasechain reaction. Images were generated by enhanced chemiluminescence(Amersham, Arlington Heights, Ill.). A subgroup of M. tuberculosisstrains was subjected to secondary RFLP analysis. The DNA wasdigested with AluI and probed in a similar manner with a 36-baseoligonucleotide homologous to the direct-repeat region of theM. tuberculosis genome18. Two investigators visually examinedthe RFLP fingerprints. A cluster was defined as a group of twoor more isolates from different patients whose RFLP fingerprintswere identical with respect to both the number and molecularsize of all bands. Isolates that had unique fingerprints weredeemed nonclustered. The isolates were divided into two groups:group 1 contained all nonclustered isolates, and group 2 containedall the clustered isolates.
Confirmatory Analysis
We have found that RFLP analysis based solely on hybridizationwith IS6110 may not distinguish between isolates with only twoapparently identical bands (data not shown). In order to confirmstrain identity among these isolates, we subjected most suchstrains to secondary RFLP analysis using a second enzyme anda different probe (see above). On this basis, we were able tosort strains with only two initially identical bands into threesmaller clusters. One such strain had a unique secondary fingerprintand was reclassified into group 1. Two other strains could notbe recultured for secondary RFLP analysis. One was placed inan established cluster of two-banded strains on the basis ofa shared unusual pattern of resistance, and the other strainwas excluded from the study. Two strains with only one apparentlyidentical band detected on primary RFLP fingerprinting werealso excluded to avoid a bias toward clustering.
Statistical Analysis
Chi-square tests (or Fisher's exact tests, when expected cellsizes were less than five) were performed to test the associationof clustering with categorical predictor variables. Wilcoxonnonparametric tests and t-tests were performed to determinewhether the distributions of the continuous variables differedbetween subjects with clustered strains and those with nonclusteredstrains. Predictor variables that were significantly associatedwith clustering (P<0.05) were included in a logistic-regressionmodel. Statistical interaction with HIV status was also investigated.Logistic-regression analysis was also performed on the dataon subjects who were Bronx residents to determine the independenteffects of household income on clustering.
Results
Study Population
Of 130 patients who had culture-proved tuberculosis during thestudy period, 117 had M. tuberculosis cultures available forRFLP fingerprinting. The medical records were reviewed for 114of the 117 patients (97 percent) with known RFLP fingerprints.Three patients with negative smears, a single positive culture,and no clinical or radiologic evidence of tuberculosis on chartreview were excluded because their culture results were thoughtto represent possible laboratory contamination or mislabeling.We also excluded three patients whose isolates had two or fewerbands on primary RFLP analysis and for which secondary RFLPanalysis was not done. For classification purposes, the remaining108 patients were assigned to group 1 or group 2 on the basisof their DNA fingerprints. For all other analyses, the fourchildren under 15 years of age were excluded, because many ofthe social variables evaluated in this study are not relevantto children. The final study population consisted of the 104adult patients for whom complete data were available. The demographicand clinical characteristics of the study population were comparedwith those of two series of patients with tuberculosis in NewYork City who were studied in 199119,20. The study populationwas similar to those in the two earlier studies in most respects,including sex, age, proportion of foreign-born subjects, andproportion seropositive for HIV, but there was a greater proportionof Hispanic subjects, reflecting the ethnic makeup of the Bronx,and somewhat fewer patients with AIDS and homeless patients.
Characterization of Patients According to Tuberculosis Strain
Of the 104 study patients, 65 (62.5 percent) had strains ofM. tuberculosis with unique RFLP fingerprints (group 1) and39 (37.5 percent) had strains whose RFLP patterns were identicalto those of 1 to 11 isolates from other patients, which we classifiedinto 12 clusters (group 2). A total of 77 RFLP patterns wereseen in 104 patients.
The clinical and epidemiologic characteristics of the groupsare shown in Table 1. The patients in group 2 were significantlymore likely than the patients in group 1 to be HIV-infected(67 percent vs. 31 percent, P<0.001) and to have drug-resistantisolates (49 percent vs. 16 percent, P<0.001), includingresistance to multiple drugs (24 percent vs. 5 percent, P =0.003). There was a significant association with Hispanic ethnicity(49 percent vs. 26 percent, P = 0.02); however, birth outsidethe United States and Puerto Rico was less common (8 percentvs. 28 percent, P = 0.01). The patients in group 2 were alsosignificantly younger than those in group 1 (mean age, 36 vs.46 years, P = 0.001). Other clinical and radiologic featuresof the two groups were similar. The patients in group 2 werenot more likely than the patients in group 1 to have been hospitalizedpreviously at the study hospital; before their disease developed,only three patients could possibly have been exposed to otherpatients infected with strains with identical RFLP fingerprints.
Table 1. Characteristics of the Two Groups of Patients with Tuberculosis.
Analysis of the Bronx residents according to census blocks andblock groups permitted us to assess the local economic and demographicenvironment in which each patient lived. Patients in group 2resided in block groups with lower median household incomesthan those in group 1 ($17,676 vs. $22,338, P = 0.02) and livedin more crowded conditions (percentage of households on theblock with more than one person per room, 22 percent vs. 17.8percent; P = 0.04). The difference in median incomes was significantonly among non-Hispanic patients ($17,713 vs. $24,480, P = 0.01)and HIV-seronegative patients ($14,977 vs. $23,476, P = 0.003).Hispanic patients as a whole lived in block groups with lowermedian incomes than non-Hispanic patients (mean income, $17,577vs. $22,224; P = 0.02), but there was no significant differencein this variable between group 1 and group 2.
Age Differences
Younger age and HIV seropositivity were strongly associatedwith having a clustered isolate (group 2). However, group 1also had young foreign-born and HIV-seropositive patients (Figure 1).The higher mean age of the patients in group 1 was due tothe large number of HIV-seronegative patients over the age of50 (21 of 45), as compared with group 2 (2 of 13, P = 0.04).Therefore, younger patients were at risk for both clusteredand nonclustered isolates, whereas older patients had predominantlynonclustered isolates.
Figure 1. Age Distribution of Patients in Group 1 and Group 2 According to HIV Status and Place of Birth.
Group 1 comprises at least three populations: an older population of HIV-seronegative patients and two younger populations, one HIV-seropositive and the other HIV-seronegative and foreign-born. Patients in group 2 are more homogeneous, with similar age distributions of HIV-seropositive and HIV-seronegative patients.
Multivariate Analysis of Differences between Groups
In the multivariate model (Table 2), resistance to one or moredrugs was strongly associated with clustering (adjusted oddsratio, 4.52; P = 0.005), as was younger age (adjusted odds ratiofor a difference of 10 years as a continuous variable, 1.59;P = 0.02). Conversely, subjects known to be foreign-born wereless likely to be in group 2 (adjusted odds ratio, 0.27; P =0.08). There was an interaction between HIV status and ethnicity.The odds of clustering were significantly increased among patientswho were Hispanic, HIV-seropositive, or both as compared withpatients who were HIV-seronegative and not Hispanic. However,HIV seropositivity did not increase the risk of having a clusteredisolate among the Hispanic patients, and conversely, being Hispanicdid not increase this risk among HIV-seropositive patients.
Table 2. Multivariate Analysis of the Association of Study Variables with Clustering of Tuberculosis.
Multivariate analysis was performed on data on Bronx residents,including block-group data on median household income. Crowdedliving conditions (more than 20 percent of households in thecensus block with more than one person per room) was not includedin the final model because it was correlated with median householdincome (R2 = 0.71, P<0.001). Previously noted associationswith clustering remained the same, although their statisticalsignificance was decreased as a result of the smaller numberof observations and increased number of variables in the model.A median household income of less than $20,000 per year wasassociated with clustering (adjusted odds ratio, 3.22; P = 0.04).The geographic concentration of patients in group 2 in predominantlylower-income block groups and the relation of this variableto HIV status and ethnic group are shown in Figure 2.
Figure 2. Map of the Bronx, Showing the Ethnicity, HIV Status, and Geographic Location of Patients in Group 1 and Group 2 in Relation to Lower-Income Block Groups.
Patients in group 2 lived more often in poor block groups (median household income in 1989, below $20,000). This association was independent of ethnicity or HIV status. The lower-income block groups represented identifiable geographic areas where cases of recently transmitted tuberculosis were common.
Analysis of Clustered Cases According to Date of Presentation and Pattern of Drug Resistance
Cases of tuberculosis due to clustered strains tended to appeartogether (Figure 3A). The first positive cultures from the patientsin each cluster were obtained over a limited period, a circumstanceconsistent with an episodic pattern of transmission. Strainsin cluster J, the largest cluster, were isolated throughoutthe study, but they were found predominantly in 1990 and 1992;only one case was seen in 1991. This same strain has been implicatedin an outbreak of tuberculosis at a men's shelter in northernManhattan21.
Figure 3. Temporal Distribution and Patterns of Drug Resistance of Strains of Tuberculosis Isolated from Patients in Group 2.
Panel A shows that most cases caused by clustered strains presented within a limited period. The date of the initial positive M. tuberculosis culture is shown for each patient (39 adults and 2 children, the latter indicated by asterisks). The initial isolates in clusters A through F, H, I, and L were all cultured within 11 months of each other. New isolates with identical RFLP fingerprints were not otherwise seen during the 37-month study period. Isolates from clusters G and K were identified 12 and 14 months apart, respectively. Cases caused by strains from cluster J, the largest cluster, occurred throughout the study but were found predominantly in 1990 and 1992; only one case was seen in 1991.
Panel B shows that the patterns of drug resistance were similar within each cluster. Each entry describes the resistance profile of one M. tuberculosis isolate. Resistance profiles are listed according to cluster and are shown in the order in which they presented (from left to right) during the study period. In four of eight clusters with drug resistance, all isolates with known susceptibility profiles were resistant to the same drugs. In two clusters, one isolate was drug-sensitive whereas the others were resistant to a single drug, and in one cluster all isolates were multidrug-resistant but one was resistant to an additional drug. In only one cluster did all three isolates have different susceptibility profiles. I denotes isoniazid, R rifampin, E ethambutol, S streptomycin, a dash no resistance, and a question mark an unknown pattern of resistance. There were a total of 12 drug-sensitive isolates in cluster J (marked with a dagger).
Nearly 50 percent of group 2 isolates were drug-resistant. Theisolates within an individual cluster had similar patterns ofresistance (Figure 3B); most clusters were identical, and inthree of four with different susceptibilities, the susceptibilitiesdiffered by only one drug. Five patients with drug-resistantstrains had a history of tuberculosis, but the susceptibilityof their previous isolate was unknown.
Discussion
We used DNA fingerprinting in conjunction with traditional epidemiologicmethods to investigate the pathogenesis of resurgent tuberculosisin a New York City community. Traditional teaching has heldthat the majority of the cases of tuberculosis in developedcountries result from reactivation during adulthood of an infectioncontracted decades before22,23. It is estimated that reactivationis responsible for up to 90 percent of the incident cases inthe United States8. Excess cases have largely been attributedto increases in tuberculosis contracted outside the United States1and to the high reactivation rate among persons infected withboth tuberculosis and HIV3,4. Recently transmitted tuberculosis(usually defined as disease occurring within two years of infection)was generally thought to have a minor role24. However, investigationsof institutional outbreaks caused by a single strain have clearlydemonstrated that transmission and rapid progression to diseasecan occur, particularly in persons with AIDS9,12. Some expertssuggest that recent transmission may have a substantial rolein the current spread of tuberculosis14. However, few data areavailable on the relative contributions of recent transmissionand reactivation to incident cases in the community or on riskfactors associated with transmission.
DNA fingerprinting provides a new tool for distinguishing recentlytransmitted from reactivated tuberculosis. Investigations ofnumerous outbreaks have demonstrated that epidemiologicallylinked strains of M. tuberculosis have identical RFLP patterns,whereas unrelated strains have differing patterns9,15. In theNetherlands, where the incidence of tuberculosis is declining,all epidemiologically unrelated M. tuberculosis isolates haveunique RFLP fingerprints25.
The substantial diversity of RFLP patterns among members ofthe study population suggests that the chance occurrence ofidentical RFLP fingerprints among unrelated cases would be unusual.We therefore infer that cases of tuberculosis caused by strainswith identical RFLP fingerprints (group 2) are due to recentlytransmitted disease and that cases caused by strains with uniqueRFLP fingerprints (group 1) are primarily due to the reactivationof infection. Several findings support this conclusion. Caseswithin each cluster occurred over a limited period, as wouldbe expected with new focal outbreaks of disease. Furthermore,almost half the clustered cases were drug-resistant, with similarpatterns of resistance within each cluster. Until recently,drug resistance was uncommon in New York City20; therefore,clustering of RFLP-identical, drug-resistant isolates must bedue to recently transmitted organisms. Conversely, many patientswith nonclustered strains had demographic characteristics consistentwith a finding of reactivated tuberculosis. Eighteen of 21 foreign-bornpatients were in group 1, as were 22 of 25 patients who were50 years of age or older.
Our analysis probably underestimates the true extent of recenttransmission. Some patients in group 1 might have been recentlyinfected by persons outside the study population. Conversely,if each cluster includes one reactivated index case, it couldoverestimate the incidence of recent transmission. The latterpossibility seems unlikely, since RFLP fingerprinting of strainsfrom other area hospitals has revealed isolates with patternsidentical to several of the clusters in this study,21,26,27demonstrating that the chain of transmission extends beyondour study population. Although it is possible that a bias towardclustering exists in any study performed at a single institution,our population was comparable in most respects to that of allpatients with tuberculosis in New York City in 1991.
Our study suggests that recently transmitted tuberculosis accountsfor almost 40 percent of the incident cases in an inner-citycommunity. The independent risk factors for recently transmitteddisease include younger age, Hispanic ethnicity in HIV-seronegativepatients, and infection with drug-resistant organisms. Livingin a lower-income block group was an additional risk factorfor recent transmission in some demographic groups. Forty-threepercent of the cases of tuberculosis in the HIV-seropositivepatients were in group 1 and can be attributed to the increasedreactivation rate with HIV coinfection. We believe that theremaining 57 percent are due to recent transmission. There wasno association between clustering and previous admissions, andonly three cases of possible nosocomial transmission at thestudy hospital; hence, nosocomial transmission is an unlikelyexplanation for our findings. We also found that most foreign-bornpatients did not have clustered strains, which implies thatimported cases are not a major cause of recent transmissionof tuberculosis in this area. The association between recenttransmission and HIV infection reflects both biologic and socialfactors. HIV-seropositive patients can have rapid disease progressionafter infection with tuberculosis12. HIV may modify or overwhelmother risk factors for transmission. For example, in this study,the impact of lower income was found to be greatest in the HIV-seronegativepopulation.
This study has several implications for the future control oftuberculosis. In this urban population, Hispanic ethnicity,HIV infection, and residence in lower-income block groups wererisk factors for recent transmission. The recently transmittedcases can be mapped to lower-income neighborhoods, thus identifyingan environment where there are other potential risk factorsfor transmission, such as crowding. In populations in whichmost cases of tuberculosis are due to reactivation, screeningwith the tuberculin test and selective use of preventive therapyoffer effective strategies for controlling disease. However,in communities with high rates of recent transmission, identificationof groups at high risk for transmission, early identificationof cases, reduction of institutional spread, and treatment untilthe disease is cured require more emphasis. In this study, almosthalf the isolates from patients with recently transmitted infectionswere drug-resistant, and one quarter were resistant to multipledrugs. Recently transmitted cases accounted for almost two thirdsof drug-resistant M. tuberculosis. In 1991, many of the drug-resistantcases in New York City were due to primary drug resistance20.The difficulty of treating drug-resistant tuberculosis untilit is cured may lead to a prolonged infectious state, increasingthe risk of selection for and transmission of drug-resistantstrains. Our study suggests that efforts to control the increasein drug-resistant tuberculosis must include a strategy to reducethe transmission of the disease. In addition to intensive inpatientand outpatient therapeutic programs, unconventional approaches,including active case finding in the areas of high transmissionand the option of immunization with bacille Calmette-Guerinfor persons at higher risk, merit serious consideration to protectthe community, health care workers, and hospitalized patientsfrom further transmission of drug-resistant disease.
Supported by training grants from the National Cancer Institute(2T32CA09173-16) and the National Institute of Allergy and InfectiousDiseases (T32AI07183-13 and T32AI07183-14), by the Henry J.Kaiser Foundation, and by the Howard Hughes Medical ResearchInstitute.
We are indebted to Mary Motyl, Ph.D., John McKitrick, Ph.D.,and William R. Jacobs, Jr., Ph.D., for their expertise and support;to Charles Lawson and Barry Shapiro of the Audio Visual Centerof the Albert Einstein College of Medicine for assistance withillustrations; and to Peter Alpert, M.D., for help with datacollection and analysis.
Source Information
From the Division of Infectious Diseases, Department of Medicine, Montefiore Medical Center-North Central Bronx Hospital (D.A., G.E.K.), the Department of Epidemiology and Social Medicine, Montefiore Medical Center (E.D.), and the Department of Microbiology and Immunology and the Howard Hughes Medical Institute (R.A.M., B.R.B.), Albert Einstein College of Medicine, Bronx, N.Y.; the Department of Epidemiology and Biostatistics, University of California, San Francisco, and the Division of Epidemiology and Medicine, San Francisco General Hospital, San Francisco (A.R.M., J.A.H.); and the Department of Political Science, Lehman College, City University of New York, Bronx, N.Y. (W.B.).
Address reprint requests to Dr. Alland at the Division of Infectious Diseases, Department of Medicine, Montefiore Medical Center, 111 East 210 St., Bronx, NY 10467.
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