The Epidemiology of Tuberculosis in San Francisco -- A Population-Based Study Using Conventional and Molecular Methods
Peter M. Small, Philip C. Hopewell, Samir P. Singh, Antonio Paz, Julie Parsonnet, Delaney C. Ruston, Gisela F. Schecter, Charles L. Daley, and Gary K. Schoolnik
Background The epidemiology of tuberculosis in urban populationsis changing. Combining conventional epidemiologic techniqueswith DNA fingerprinting of Mycobacterium tuberculosis can improvethe understanding of how tuberculosis is transmitted.
Methods We used restriction-fragment-length polymorphism (RFLP)analysis to study M. tuberculosis isolates from all patientsreported to the tuberculosis registry in San Francisco during1991 and 1992. These results were interpreted along with clinical,demographic, and epidemiologic data. Patients infected withthe same strains were identified according to their RFLP patterns,and patients with identical patterns were grouped in clusters.Risk factors for being in a cluster were analyzed.
Results Of 473 patients studied, 191 appeared to have activetuberculosis as a result of recent infection. Tracing of patients'contacts with the use of conventional methods identified linksamong only 10 percent of these patients. DNA fingerprinting,however, identified 44 clusters, 20 of which consisted of only2 persons and the largest of which consisted of 30 persons.In patients under 60 years of age, Hispanic ethnicity (oddsratio, 3.3; P = 0.02), black race (odds ratio, 2.3; P = 0.02),birth in the United States (odds ratio, 5.8; P<0.001), anda diagnosis of the acquired immunodeficiency syndrome (oddsratio, 1.8; P = 0.04) were independently associated with beingin a cluster. Further study of patients in clusters confirmedthat poorly compliant patients with infectious tuberculosishave a substantial adverse effect on the control of this disease.
Conclusions Despite an efficient tuberculosis-control program,nearly a third of new cases of tuberculosis in San Franciscoare the result of recent infection. Few of these instances oftransmission are identified by conventional contact tracing..
Tuberculosis and its recent resurgence are predominantly urbanphenomena in the United States, where case rates in large citiesare almost two and a half times higher than the national average1.A combination of biologic and social factors has been postulatedto account for this situation. In many cities, the number ofpersons who are immunosuppressed by infection with the humanimmunodeficiency virus (HIV) and the prevalence of drug-resistanttuberculosis have increased in the face of deteriorating socioeconomicconditions and public systems of health care delivery2. As aresult, important changes seem to have occurred in the patternsof Mycobacterium tuberculosis transmission. In particular, thelong-held assumption that only 10 percent of tuberculosis casesare the result of recent infection needs to be reconsidered3.
The combination of molecular fingerprinting of M. tuberculosisstrains and conventional epidemiologic investigation has improvedunderstanding of the transmission of tuberculosis. Molecularfingerprinting by restriction-fragment-length polymorphism (RFLP)analysis yields a unique, strain-specific pattern of bands (the"fingerprint") that is stable for at least two years4,5,6,7,8.Comparison of M. tuberculosis fingerprints from tuberculosisstrains isolated during circumscribed outbreaks has demonstratedmatching patterns among persons who were clearly infected froma common source4,8,9,10,11,12,13,14,15,16,17,18,19. By showingthat patients with no obvious epidemiologic relation are infectedwith the same strain, molecular fingerprinting has revealedthat M. tuberculosis can be transmitted during brief contactbetween persons who do not live or work together18,20,21. Takentogether, these studies suggest that patients with the sameM. tuberculosis RFLP pattern constitute an epidemiologicallylinked cluster. Furthermore, because tuberculosis developedduring a relatively short period in patients in a cluster, clusteringindicates recent infection and rapid progression to clinicalillness22.
We conducted a population-based molecular epidemiologic studyof tuberculosis in San Francisco. In addition to providing anestimate of the incidence of tuberculosis that results fromrecently transmitted infection, we identified some of the riskfactors for the transmission of M. tuberculosis. Our resultssuggest that current tuberculosis-control strategies have importantlimitations in contemporary urban environments.
Methods
Patient Identification and Routine Data Collection
The population studied included all patients with tuberculosiswho were reported to the San Francisco Department of PublicHealth, Division of Tuberculosis Control, between January 1,1991, and December 31, 1992. The routine demographic data collectedincluded age, sex, race or ethnicity, country of birth, numberof years of residency in the United States, and address at thetime of diagnosis. Specific information concerning tuberculosisincluded the date of diagnosis, site or sites of disease, resultsof chest radiographs, and results of microbiologic studies.
The registries for tuberculosis and the acquired immunodeficiencysyndrome (AIDS) maintained by the San Francisco Department ofPublic Health were cross-matched to identify all patients reportedto have both tuberculosis and AIDS as of September 1993. Confidentialitywas ensured by having health department personnel remove allidentifying information before the data analysis. The subjects'socioeconomic status was estimated by matching patients' addressesat the time of diagnosis to census-tract data (including indexesof unemployment, income, poverty level, education level, crowding,immigration status, and racial or ethnic distribution). Census-tractinformation was not included for 14 homeless persons.
Collection of M. tuberculosis Isolates and RFLP Analysis
Lowenstein-Jensen slant cultures used for mycobacterial identificationand drug-susceptibility testing were prospectively collectedfor all microbiologically confirmed new cases of tuberculosisin San Francisco. RFLP analysis was performed with an internationallystandardized method with internal molecular-weight standards23.The resulting autoradiographs were compared with the Bio ImageWhole Band Analyzer, version 3.0 (Millipore, Ann Arbor, Mich.).All lanes that were found by computer analysis to have similarpatterns were compared visually and classified as having matchingRFLP patterns if the number and molecular weights of the bandswere identical. Microbiology records were scrutinized for allpatients who had only a single positive culture for which asmear for acid-fast bacilli was negative. These cultures wereconsidered to be false positive if they were processed in themicrobiology laboratory on the same day as a specimen with apositive smear from another patient with the same RFLP pattern24.
Epidemiologic Investigations
For all patients treated by the Department of Tuberculosis Control,an investigation of contacts was conducted by trained, multilingualdisease-control investigators using standard methods25. Forpatients whose care was not managed by the Division of TuberculosisControl, contact investigation was conducted either by the treatingphysician or by Tuberculosis Control personnel. In additionto the routine contact investigation, selected groups of patientsinfected with organisms with identical RFLP patterns were studiedfurther by a more intensive review of the Division of TuberculosisControl records. For patients in the largest cluster, all availableclinic and hospital records were reviewed and the patients wereinterviewed.
Statistical Analysis
Data were entered and analyzed with FoxPro 2.5 (Microsoft, Redmond,Wash.), EpiInfo (Centers for Disease Control and Prevention,Atlanta), Egret (Statistics and Epidemiology Research Corporation,Seattle), and PC SAS (SAS Institute, Cary, N.C.) computer programs.A cluster was defined as two or more patients with identicalRFLP patterns. Patients with unmatched RFLP patterns were considerednonclustered.
Student's t-test and the chi-square test were used to assessunivariate risk factors for being in a cluster. Risk factorsfor clustering identified by univariate analysis were then includedin multivariate logistic-regression models, with clustered andnonclustered as the dependent outcomes. Because age appearedto be related to clustering in a nonlinear fashion, with a markeddecrease in risk at the age of 60 years, age was categorizedas either less than 60 years or 60 years or older. Odds ratioswere calculated from regression estimates based on the chi-squaredapproximation for the likelihood-ratio statistic; 95 percentconfidence intervals were based on the estimated variance ofthe regression coefficients26. The likelihood-ratio statisticswere also used to contrast the relative goodness of fit betweencompeting logistic-regression models. Tests for interactionwere conducted for all likely interacting variables. Age, sex,and factors that remained significant after adjustment for relatedvariables were included in a final model.
Results
Patient Population and RFLP Patterns Obtained
During 1991 and 1992, 688 cases of tuberculosis were reportedto the Division of Tuberculosis Control, 585 of which were confirmedby the isolation of M. tuberculosis. Viable isolates of M. tuberculosiswere not available from 89 patients. These patients were similarto the 496 patients included in this study except that theywere slightly older (median age, 46 years; P = 0.02) and morelikely to be Asian (RFLP data were not available on 20 percentof Asian patients, P = 0.003).
Nine of the 496 patients were excluded from further study becausetheir culture results fulfilled the criteria for laboratorycross-contamination. RFLP analysis of the strains isolated fromthe remaining 487 patients identified 326 distinct patterns,282 of which were found in only 1 patient.
Previously published molecular biologic and epidemiologic studieshave concluded that a clonal relation cannot be inferred toexist between strains of M. tuberculosis that have only onecopy of IS611027,28. Accordingly, the 12 M. tuberculosis strainswith only one copy of IS6110 were not included in the epidemiologicanalysis. Consequently, the statistical analysis was based on473 patients (Table 1) and 324 RFLP patterns, of which 44 werefound to be shared by at least 2 patients (i.e., they were inclusters). The 44 shared RFLP patterns were obtained from 191patients (Table 2). The RFLP patterns of strains isolated fromclusters containing three or more patients are shown in Figure 1.Thus, 191 of the 473 patients (40 percent) were in 1 of the44 clusters; the clusters ranged in size from 2 to 30 patients.
Figure 1. Results of RFLP Analysis of M. tuberculosis Strains Isolated from Three or More Patients.
The number of patients with M. tuberculosis isolates with a shared RFLP pattern is shown at the bottom of the figure. Twenty patterns, each found in two patients, are not shown. The 12 patients in the column at the left were excluded from analysis as described in the Results section.
Identification of Risk Factors
To identify risk factors for recent infection with M. tuberculosis,the 191 patients in clusters were compared with the 282 patientsnot in clusters. Univariate analysis (Table 1) showed that patientsin clusters were more likely to be male, young (mean age, 40.8years, vs. 48.4 years for patients not in clusters; P<0.001),black or Hispanic, and born in the United States; to have AIDS;to have received care at the Division of Tuberculosis Controlclinic; and to reside in a census tract with a poverty rateof more than 20 percent. In contrast, a history of tuberculosisand Asian race were associated with a significantly decreasedrisk of being in a cluster. Infection with drug-resistant M.tuberculosis and the level of crowding and education in thecensus tract were not associated with clustering (data not shown).
Multivariate analysis of the risk factors for clustering revealedsignificant differences between younger and older patients (Table 3).For patients younger than 60 years, risk factors for clusteringincluded Hispanic ethnicity (odds ratio, 3.3; P = 0.02), blackrace (odds ratio, 2.3; P = 0.02), birth in the United States(odds ratio, 5.8; P<0.001), and AIDS (odds ratio, 1.8; P= 0.04). In contrast, for patients 60 years of age or older,the only significant risk factor was having been cared for atthe Division of Tuberculosis Control clinic (odds ratio, 5.7;P = 0.008). In the older age group, Asian race was again associatedwith a reduced risk of being in a cluster.
Table 3. Analysis of Risk Factors for Clustering after Adjustment for Sex and Age at Diagnosis.
Epidemiologic Investigation of RFLP Clusters
Intensive epidemiologic investigations were conducted of the3 largest clusters and the 20 clusters composed of only twopatients. Thus, 23 of the 44 clusters (52 percent), or 108 ofthe 191 patients (56 percent) with isolates with identical RFLPpatterns, were included in this analysis.
Routine investigation had established that 12 patients in thelargest cluster (Table 2) were living in or employed by a residentialfacility for patients with AIDS12. Our RFLP analysis identifiedan additional 18 patients with isolates with the same fingerprintwho were not previously known to have any association with thefacility. Seven of these patients were available for interview,eight had died, and three could not be located or refused tobe interviewed.
The apparent index patient in this cluster was a 38-year-oldwhite man with AIDS who was receiving general assistance, wasnot compliant with antituberculous therapy, and had had positivesputum smears for approximately six months. Specific transmissionlinks could be established among nine of the patients who werenot associated with the residential facility (Figure 2): twonamed one another as contacts, three were on the same hospitalward, and four were in the same general medical clinic at atime when it was reasonable to assume that transmission hadoccurred. Although seven additional patients were homeless,homosexual, or substance abusers, they were not otherwise linkedepidemiologically. Three patients had no discernible connectionwith any of the other patients.
Figure 2. Transmission Links Identified between Patients with Isolates in the Largest Cluster.
Each dot represents a patient. Solid lines indicate links between patients who were residents or employees of the same residential facility, dashed lines links between patients who were identified as contacts of other patients, and dotted lines links between patients who were in the same hospital ward, clinic, or homeless shelter at a time when transmission was likely to have occurred. Dots not connected to a line represent the seven patients for whom no specific epidemiologic connection could be discerned. Squares denote patients with cavitary tuberculosis and positive smears, circles patients with tuberculosis who had documented conversions of tuberculin skin tests within two years, and triangles patients for whom there was no discernible connection with any of the other patients.
The second-largest cluster contained 23 patients who were primarilyyoung (average age, 33 years), born in the United States (18patients), and male (19 patients); 13 had AIDS, and 8 were substanceabusers. The index patient was a 28-year-old white HIV-infectedtranssexual man who was an intravenous drug user and a prostitute.He had been found to have tuberculosis, with a positive sputumsmear, shortly after moving to San Francisco and was noncompliantwith therapy. The M. tuberculosis strain found in this patientwas next isolated from four other young homeless HIV-infectedintravenous drug users over a three-month period and subsequentlyfrom a more diverse group of patients.
The apparent index patient in the third-largest cluster (15patients) was a 36-year-old HIV-seronegative black alcoholicman with cavitary pulmonary tuberculosis. He frequently usedpublic facilities, including homeless shelters, detoxificationcenters, public clinics, and hospitals. This patient also wasnoncompliant with therapy and had had positive sputum smearsfor nine months. Most of the other patients in this clusterwere also black (12 patients) and alcoholic (8 patients); only5 of the 15 patients were recorded as having AIDS.
Efficacy of Contact Tracing
A conventional investigation of the patients' contacts identifiedconnections among only 19 of the 191 patients (10 percent) foundto be connected by RFLP analysis. Of the three largest clusters,contact tracing identified only the outbreak in the AIDS facility.
To examine further the relation between the patients' characteristicsand the accuracy of conventional contact tracing, we studiedthe 20 clusters that contained only two patients each. Conventionalcontact tracing conducted before the RFLP results were availablepredicted transmission in only four of these clusters, all ofthem involving contact between an older patient who presumablyhad reactivated tuberculosis and a younger person in a traditionalhousehold setting. No instances of transmission between immigrants,transients, or patients with AIDS were predicted from the contactinvestigation.
Discussion
We used a systematic, population-based RFLP analysis of M. tuberculosisisolates in conjunction with conventional epidemiologic methodsto describe the contemporary pattern of tuberculosis transmissionin San Francisco. The information produced by this approachis consistent with that yielded by traditional reporting practicesin that it enumerates and characterizes the cases that occurredduring a given period in a single public health jurisdiction.However, our data provide considerably more information abouttuberculosis transmission in this urban area, including evidencethat an important factor in the resurgence of tuberculosis,despite an efficient tuberculosis-control program, is the ongoingtransmission of a few strains of M. tuberculosis in specificsubgroups of the population.
The use of RFLP analysis to identify the pathways of tuberculosistransmission within a community is based on the premise thatepidemiologically unrelated cases will have occurred as a resultof the reactivation of latent infection and thus have uniqueRFLP patterns, whereas cases that are linked as a consequenceof recent infection will have the same patterns (i.e., appearin a defined cluster). In this study, the first contention issupported by the vast diversity of RFLP patterns in San Francisco:326 distinct patterns among the 487 strains analyzed. The secondis supported by the congruence of the molecular-fingerprintingdata and results of the epidemiologic study of tuberculosisoutbreaks4,8,9,10,11,12,13,14,15,16,17,18,19,20,21.
We found that 191 of the 473 patients (40 percent) had 1 of44 clustered RFLP patterns and thus may have been epidemiologicallylinked. Assuming that a typical cluster of n persons comprisesone index patient with reactivated disease and n - 1 patientswith recently acquired disease, we estimate that at least 31percent (191 - 44) of the 473 cases were due to recent infectionthat had progressed to active disease during the two-year studyperiod. Because RFLP analysis can only be used to analyze microbiologicallyconfirmed cases, patients who became infected but whose infectionremained latent during the course of the study were not identified.Reactivation of infection in these latently infected personswill continue to produce overt disease for decades. As a result,the true magnitude of the increased burden of tuberculosis dueto recent M. tuberculosis infection in San Francisco is probablygreater than our estimate of 31 percent.
A principal objective of this study was the identification ofrisk factors for recent infection. Because we focused only oncases reported during a two-year period, our analysis of riskfactors encompassed only the subgroup of recently infected patientswhose infection progressed to active disease during this interval.As a result, epidemiologic risk factors for transmission arenecessarily combined with biologic risk factors that are associatedwith rapid progression.
For patients less than 60 years of age, a diagnosis of AIDS,birth in the United States, black race, and Hispanic ethnicitywere found by multivariate analysis to be significant, independentrisk factors. HIV seropositivity itself was not a significantrisk factor for clustering in the patients for whom HIV serologicdata were available (data not shown), probably reflecting theimportance of the degree of immunosuppression in the developmentof tuberculosis. In contrast, patients with AIDS and severeimmunosuppression are at increased risk of being in a cluster.This probably reflects the combined effects of a shortened intervalbetween infection and active disease and the tendency for patientswith AIDS to be brought together in common medical or livingfacilities.
Being born in the United States also might act as a risk factorthrough a biologic mechanism, since most such persons will havea negative tuberculin test and thus lack the relative immunityassociated with latent tuberculosis. In younger subjects, birthoutside the United States protected against newly acquired infection.Even after adjustment for race and ethnicity, the immigrantpopulation was significantly more likely to have reactivateddisease (and was less likely to be in a cluster) than personsborn in the United States. This may reflect the high rate oflatent tuberculosis infection in children born in developingcountries. If so, our results suggest that childhood infectionboth protects immigrants from new infection and places themat risk for reactivation.
Strikingly different risk factors were found for persons 60years of age or older. In this age group, treatment at the municipaltuberculosis clinic was the only variable identified as a riskfactor for clustering. Because most patients cared for in thisclinic have already been given a diagnosis of tuberculosis,the clinic itself is unlikely to have been a locus for transmission.Instead, its use may be a proxy for the use of other socialand medical facilities where transmission may have occurred.In the older age group, being Asian was a significant negativerisk factor for clustering, probably because many older patientshave latent infection that may become reactivated.
Epidemiologic investigation of the three largest clusters reconfirmsthat a single patient with highly infectious disease can havea major impact on urban programs of tuberculosis control. Eachof the index patients had positive smears and was poorly compliantin taking the prescribed antimicrobial therapy. In the largestcluster the putative index patient, one of the few patientsnot treated successfully by the San Francisco Tuberculosis ControlProgram, apparently infected 29 additional patients. Thus, thisone patient accounted for 6 percent of the cases evaluated inSan Francisco during the study period. Data collected by theCenters for Disease Control and Prevention show that such noncompliantpatients are uncommon in San Francisco, where during the studyperiod at least 95 percent of patients completed their regimensof antituberculous drugs. The cumulative contribution of suchpersons may be much greater in areas where compliance ratesare lower and multidrug-resistant tuberculosis is prevalent.
Overall, conventional contact tracing, conducted by an efficienttuberculosis-control program, identified only 10 percent ofthe patients in clusters. This low level of efficacy is bestexplained by the overrepresentation in clusters of unemployedand homeless persons, who may have become infected in settingsdetermined primarily by lifestyle and by social subgroups. Contactsof this kind may have been multiple, transient, and difficultto reconstruct by routine tracing techniques. The overrepresentationof patients with AIDS may also have reduced the efficacy ofcontact tracing in this group, since the presumably increasedsusceptibility of such persons to tuberculosis may have permittedtransmission to occur in settings where exposure is neitherprolonged nor intense. Casual transmission of this kind is hardto detect with current techniques of contact tracing.
This study has three major implications for urban tuberculosiscontrol. First, because more cases of tuberculosis are arisingas a result of recent infection with M. tuberculosis than hasbeen heretofore appreciated, increased emphasis should be placedon the identification of sites of transmission and the applicationof environmental controls. Second, because a single infectiouspatient may have devastating effects on tuberculosis control,the treatment of patients with infectious tuberculosis mustbe prompt and effective. Third, because only 10 percent of thepatients in clusters were identified by a conventional investigationof contacts, novel approaches to contact tracing may need tobe developed and targeted to specific populations.
Supported in part by the Howard Hughes Medical Institute, grantsfrom the National Institutes of Health (K08 AI01137-01 and R01AI34238-01), and a grant from the Centers for Disease Controland Prevention (U52-CCU 900454).
We are indebted to the personnel of the San Francisco Departmentof Public Health Division of Tuberculosis Control, whose highquality of service and cooperation have made this work possible;to Aimee LaPerriere-Hunt for diligent research assistance; toArthur Back (deceased), Anna Babst of the San Francisco PublicHealth Laboratory, Arthur Reingold, Gretchen Anderson, and theWestern Consortium for Public Health, Bacterial and MycoticSurveillance Project for assistance with the collection of M.tuberculosis; to Kevan Gross and Eric Preston for essentialassistance with computer-software design; to Karl Reich formany thoughtful discussions regarding the molecular biologyof M. tuberculosis; to Lorene Nelson and Jerry Halpern of theStanford University Department of Health Research and Policyfor important advice about statistical analysis; and to Dr.Nancy Krieger, Kaiser Permanente Division of Research, Oakland,Calif., for San Francisco County census-tract information.
Source Information
From the Division of Infectious Disease and Geographic Medicine, Department of Medicine (P.M.S., J.P., D.C.R., G.K.S.), and Howard Hughes Medical Institute (S.P.S., G.K.S.), Stanford Medical School, Stanford, Calif.; the Medical Service, San Francisco General Hospital, and the University of California, San Francisco (P.C.H., G.F.S., C.L.D.); and the Division of Tuberculosis Control, San Francisco Department of Public Health, San Francisco (A.P., G.F.S.).
Address reprint requests to Dr. Small at Beckman Center, Rm. 251, Stanford University, Stanford, CA 94305.
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Transmission of Tuberculosis
McKenna M., Williams M. H., Pollen R. H., Joy M., Small P. M., Hopewell P. C., Schoolnik G. K., Kalkut G. E., Alland D., Bloom B. R., Frieden T. R., Hamburg M. A.
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331:1093-1096, Oct 20, 1994.
Correspondence
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