Background From 1978 through 1992, the number of patients withtuberculosis in New York City nearly tripled, and the proportionof such patients who had drug-resistant isolates of Mycobacteriumtuberculosis more than doubled.
Methods We reviewed, confirmed, and analyzed data obtained duringthe surveillance of patients with tuberculosis.
Results From 1992 through 1994, there was a 21 percent decreasein reported cases of tuberculosis in New York City. An evaluationof the surveillance system revealed very few unreported cases.The number of cases decreased by more than 20 percent amongblacks and Hispanics, persons with documented human immunodeficiencyvirus infection, homeless persons, and patients with multidrug-resistanttuberculosis; in all these groups, tuberculosis is likely toresult from recent transmission. In contrast, the number ofcases of tuberculosis increased among elderly and foreign-bornpersons, in whom the disease is likely to result from the reactivationof an infection acquired many years earlier. Enrollment in aprogram of directly observed therapy, in which health workerswatch patients take their medications, increased from fewerthan 100 patients to nearly 1300, with more than 32,000 patient-monthsof observation from 1992 through 1994.
Conclusions Epidemiologic patterns strongly suggest that thedecrease in cases resulted from an interruption in the ongoingspread of M. tuberculosis infection, primarily because of betterrates of completion of treatment and expanded use of directlyobserved therapy. Another contributing factor may have beenefforts to reduce the spread of tuberculosis in institutionalsettings, such as hospitals, shelters, and jails. Expansionof measures to prevent and control tuberculosis and supportof international control efforts are needed to ensure continuedprogress.
Since before the turn of the century, New York City has beena center for both tuberculosis and its control. In 1889, HermannBiggs of the New York City Department of Health recommendeda comprehensive program of tuberculosis control1 that eventuallyincluded systematic surveillance, nursing follow-up of individualpatients, public education, isolation of infectious patients,and free laboratory testing of sputum samples. Until the discoveryof specific antituberculous medications, these were the onlyavailable methods of disease control; even now, all remain important.
Programs to control tuberculosis became victims of their ownsuccess. In 1960, New York City had more than 2400 beds forpatients with tuberculosis in hospitals and sanitariums anda comprehensive system of treatment.2 But as the incidence ofthe disease declined, so did programs to control it. By 1988,the staff of the Bureau of Tuberculosis Control had been reducedto approximately 140, the number of clinics had declined from24 to 8, and combined public health and chest clinics in municipaland voluntary hospitals had been disbanded.3 As a result, in1989 less than half of patients who began treatment were cured.The human immunodeficiency virus (HIV) epidemic, diminishedpublic health efforts to control tuberculosis, rising povertyand homelessness, overcrowded conditions in congregate settings,and immigration from countries with a high prevalence of tuberculosisall led to a resurgence of the disease in the 1980s.3
As a result of inadequate treatment, the proportion of patientswith drug-resistant isolates of Mycobacterium tuberculosis increased.Drug resistance among patients who had never been treated increasedfrom 10 percent in 1983 to 23 percent in 1991.4 Such resistanceincreases the likelihood of treatment failure and relapse andgreatly complicates the control of the disease.5 By 1992, thesituation in New York City looked bleak. The number of casesof tuberculosis had nearly tripled in 15 years.6 In centralHarlem, the case rate of 222 per 100,000 people exceeded thatof many Third World countries.7 Outbreaks of multidrug-resistanttuberculosis had been documented in more than half a dozen majorhospitals, with case fatality rates greater than 80 percent,and health care workers were becoming ill and dying of thisdisease.8,9,10,11 Nearly one in five patients with tuberculosisin New York City had multidrug-resistant strains, and the proportionof new patients with multidrug resistance had more than doubledin seven years.4 In the first quarter of 1991, with 3 percentof the country's population, New York City accounted for a remarkable61 percent of cases of multidrug-resistant tuberculosis in theUnited States.12
Just two years later, however, the city announced a substantialdecrease in new cases — a reduction of 15 percent, from3811 in 1992 to 3235 in 1993. This decline continued through1994 (to 2995 cases), with the decrease reported over the two-yearperiod exceeding 21 percent; the trend appears to be continuingin 1995. The decrease in 1993 was the first substantial declinein New York City in 15 years, accounting for 42 percent of thedecrease in the number of cases of tuberculosis in the nationthat year.13 In this article we analyze the accuracy of reportingof tuberculosis cases, as well as the epidemiologic patternsof and reasons for this decrease.
Methods
To confirm the accuracy of surveillance data, we conducted fourinvestigations. First, all mycobacteriology laboratories inNew York City were audited. Second, we reviewed all 1992 and1993 death certificates that listed tuberculosis as the underlyingcause of death. Third, we reviewed the records of all patientsreported to the Department of Health for whom no bacteriologicconfirmation of disease was available, to see whether they metthe clinical case definition of tuberculosis.14 Fourth, we evaluatedthe possibility that patients with the acquired immunodeficiencysyndrome (AIDS) who also had tuberculosis were being reportedto the AIDS surveillance program in New York City, but not tothe tuberculosis surveillance system.
Results
The audits of death certificates yielded only two previouslyunreported cases of tuberculosis. Both were culture-negative,with tuberculosis diagnosed at autopsy, and both were includedin the 1994 case count. As a result of intensive review, 382patients who met the clinical case definition of tuberculosiswere included in the 1993 case count, and 515 were includedin the 1994 count. The proportion of clinically confirmed casesrose steadily, from 4.2 percent in 1990 to 17.2 percent in 1994.Thus, the decrease in culture-confirmed cases from 1992 to 1994was even greater — 27.9 percent — than the overalldecrease. Because verification of clinically confirmed casesof tuberculosis has improved, in this article we analyze trendsamong cases with positive cultures only. One hundred forty-ninepatients were reported to the AIDS surveillance system as havingtuberculosis, but they were not reported to the Bureau of TuberculosisControl. On review, only one of these patients, who had beencared for at a Veterans Affairs hospital, met the surveillancecriteria for tuberculosis. Thus, the decrease in the numberof cases does not appear to be an artifact of surveillance.
There are revealing patterns in the decreasing number of cases.Recent evidence based on the analysis of M. tuberculosis isolatesusing restriction-fragment–length polymorphisms suggeststhat in New York City, San Francisco, and possibly elsewhere,at least one quarter of cases of tuberculosis result from recentlytransmitted infection.15,16 Patients likely to have acquiredM. tuberculosis recently include the poor, some racial and ethnicminorities, patients with multidrug-resistant tuberculosis,and patients with HIV infection or AIDS.15,16 Foreign-born andelderly patients are substantially less likely than U.S.-bornor young patients to be infected with organisms that had beentransmitted recently. It can be expected, then, that if thedecrease in the number of cases of tuberculosis was real andwas the result of improved treatment, the groups most likelyto have recently transmitted infections would have the greatestreductions in disease. This is precisely what occurred.
As compared with 1991–1992, the number of culture-confirmedcases in New York City in 1993–1994 decreased by 44 percentamong children under the age of 10 years, by 30 percent amongadults 20 to 40 years old, by 24 percent among persons withdocumented HIV infection, by 24 percent among non-Hispanic blacks,and by 21 percent among Hispanics. Even more dramatic were thedecreases in the number (44 percent) and proportion (30 percent)of these patients who had multidrug-resistant tuberculosis.In contrast, the number of cases increased by 22 percent amongforeign-born persons and by 4 percent among those more than60 years of age — patients in whom a case of tuberculosisis likely to represent a reactivation of infection acquiredyears earlier (Table 1). The increase in cases in the Asianpopulation in New York City was observed entirely among foreign-bornpersons; the number of cases declined slightly among Asiansborn in the United States.
Table 1. Patients with Culture-Confirmed Tuberculosis in New York City during Two Two-Year Periods.
Discussion
These epidemiologic patterns strongly suggest that the decreasein the number of cases resulted from an interruption of theongoing spread of M. tuberculosis infection. Several programmaticimprovements are likely to have contributed.
Directly Observed Therapy
First, public health programs to control tuberculosis have recentlyexpanded, particularly those that provide directly observedtherapy, in which patients are observed as they take each doseof their medicine (Figure 1). With support from the Centersfor Disease Control and Prevention as well as the city and stategovernments of New York, the staff of the Bureau of TuberculosisControl of the New York City Department of Health increasedfrom 144 to more than 600 between 1988 and 1994; in the sameperiod, the bureau's budget increased from $4 million to morethan $40 million. Outreach workers traveled to patients' homesand workplaces, as well as to street corners, bridges, subwaystations, park benches, and even "crack dens" in abandoned buildings,to ensure that patients were appropriately treated. By the endof 1994, more than 1200 patients were receiving directly observedtherapy, as compared with fewer than 50 in 1983. Most receivedtheir therapy through the city Department of Health with federaland local funding, and some were in programs supported by thestate Department of Health, Medicaid funds, and funding grantedunder the Ryan White Care Act.
Figure 1. Number of Patients with Tuberculosis in New York City (Solid Line) and Number Receiving Directly Observed Therapy at the End of Each Year (Shaded Bars), 1978 through 1994.
Data are from the New York City Department of Health.
From January 1, 1992, through December 31, 1994, more than 32,000patient-months of directly observed therapy were administered.In a typical month during this period, only 3 percent of patientswho received the therapy were infectious, as indicated by sputumsmears positive for acid-fast bacilli and M. tuberculosis onculture. We estimate that, without directly observed therapy,at least 15 to 20 percent of patients would have been infectious.A single infectious patient infects approximately one personper month.17 Since more than 40 percent of patients with tuberculosisin New York City have HIV infection,4 many contacts (perhaps20 percent) who would have become infected with M. tuberculosiswere also HIV-infected. Among HIV-infected persons with newtuberculosis infections, the rate of progression to active tuberculosisis likely to be at least 30 percent in the first year18,19;among HIV-negative patients, it is approximately 3 to 5 percent.20On the basis of these figures, directly observed therapy mayhave prevented at least 4000 tuberculosis infections and atleast 800 cases of active tuberculosis by preventing patientsfrom either becoming or remaining infectious.
The proportion of patients who completed treatment increasedfrom less than 50 percent in 1989 to approximately 90 percentamong patients with tuberculosis diagnosed in 1994, with mostof the improvement occurring from 1992 to 1994. In additionto directly observed therapy and intensive case management,involuntary in-hospital confinement was instituted for the smallproportion of patients (approximately 1 percent) in whom allother treatment approaches failed. The most important effectof the detention program was probably as a deterrent; giventhe credible threat of detention, adherence to directly observedtherapy by some patients undoubtedly increased.
Infection-Control Measures
There has also been improvement in infection control. The NewYork State Department of Health has documented that tuberculosis-controlefforts in New York City hospitals improved substantially fromJuly 1992 to July 1994 (Stricof RL: personal communication).Measures carried out at hospitals where an outbreak has occurredcan halt the spread of multidrug-resistant tuberculosis.21 Therewere 115 cases in 1991 for which there was epidemiologic evidenceof nosocomial transmission, 103 cases in 1992, and fewer than30 cases annually in 1993 and 1994. We recently found that morethan 4 percent of all cases of tuberculosis in New York Cityin April 1991 appeared to have been associated with a hospitalstay (unpublished data). Thus, improved infection control islikely to have substantially decreased the number of cases citywide.
A further factor that may have contributed to the decrease incases is the downsizing of large shelters for single adults.In the 1980s, as many as 50,000 different people passed throughshelters for homeless adult men in New York City in a singleyear, with more than 5000 housed on any given night.22 In theearly 1990s, non-congregate housing began to be provided tohomeless patients with AIDS. This policy had the dual effectof removing most patients with tuberculosis from the sheltersystem and of removing many patients with AIDS — thosewho are at highest risk for tuberculosis. Also, the large sheltersthat had housed 800 or more men in a single room in the late1980s and early 1990s were phased out. This change may haveaffected the transmission of tuberculosis among the homelesspersons who remained in the system, by reducing the opportunitiesfor exposure to the disease as well as decreasing the intensityof such exposure. The number of patients with tuberculosis whowere listed on the computerized registry of the shelter systemdecreased from 748 in 1991 to 293 in 1994.
In addition, improved practices for screening, isolation, andfollow-up of incarcerated persons in New York City probablyreduced the transmission of M. tuberculosis infection. The RikersIsland Correctional Facility holds more than 120,000 prisonersannually and has a daily census of more than 15,000.23 Therewere no effective facilities for isolation at Rikers Islanduntil May 1992, when a communicable-disease unit with effectiverespiratory isolation was constructed. There is evidence thattuberculosis was transmitted among patients incarcerated atRikers Island in 198524; it is likely that subsequent improvementsin screening and isolation to prevent the airborne spread ofM. tuberculosis reduced such transmission. In 1992, all patientswith suspected or confirmed active tuberculosis at Rikers Islandwere enrolled in a program of directly observed therapy. Anexpanded outreach program and the use of incentives increasedthe proportion of patients who kept follow-up appointments aftertheir release from less than 20 percent to 92 percent (BaileyV, Larkin C: personal communication).
These factors — the use of directly observed therapy andimproved infection control in hospitals, shelters for the homeless,and correctional facilities — are related. Programs ofdirectly observed therapy for outpatients greatly reduced thenumber of infectious patients entering hospitals, shelters,and jails. Improved infection control limited the spread ofdisease by infectious persons who entered those facilities.
Changes in Treatment Regimens
Other factors may have contributed to the recent decrease inthe number of cases of tuberculosis in New York City. In November1991 the Department of Health recommended an initial regimenof at least four drugs (isoniazid, rifampin, pyrazinamide, andethambutol) for all patients with active tuberculosis. By July1993, one survey found that 89 percent of patients with suspectedtuberculosis were being treated with at least four antituberculousdrugs (Stricof RL: personal communication). This drug regimennot only reduced the likelihood that the treatment of drug-resistanttuberculosis would be ineffective, but also shortened the timerequired for patients to become noninfectious.25 Improved laboratorymethods, broader use of drug-susceptibility testing, and a higherindex of suspicion for the disease (leading to more rapid diagnosisand initiation of treatment) probably all played a part.
The expanded use of preventive therapy in high-risk groups,such as persons with HIV infection, and the use of rifabutinas prophylaxis against disease caused by M. avium complex mayalso have contributed to the decrease. This cannot be demonstrated,however, because there is no systematic monitoring of the numberof patients who complete preventive therapy. The chest clinicsof the New York City Department of Health provided such therapyto more than 4000 people annually from 1992 through 1994, asubstantial increase from prior years.
Finally, the number of severely immunosuppressed HIV-infectedpersons may have decreased slightly in New York City in recentyears.26 The fact that the number of cases of tuberculosis decreasedless rapidly among women — in whom AIDS has been increasing,when a constant case definition is used — suggests thatthe epidemiologic features of AIDS may have played some partin this change.27,28 However, even among women 20 to 40 yearsof age, the number of cases of tuberculosis fell 22 percent.
The decrease in resistance to drugs is perhaps the most convincingevidence linking the reduced numbers of tuberculosis cases withprogrammatic improvements. The incidence of drug-resistant tuberculosishas been shown to decline with improved rates of completionof treatment and with the use of directly observed therapy,29,30but presumably it would not be decreased by either the use ofisoniazid prophylaxis or changes in the pattern of the HIV epidemic.
Implications
There is an important and complex lesson to be learned fromthe rapid decrease in the number of cases of tuberculosis. Ithad been believed that 90 percent of cases could be attributedto the reactivation of earlier infection,31 but at least inthe era of HIV, 30 percent or more of cases may result fromthe recent transmission of M. tuberculosis.15,16 It is comparativelyeasy to prevent transmission by ensuring that patients withrecently acquired disease are treated promptly, appropriately,and completely — ideally, with directly observed therapy.But after these cases have been prevented, the challenge becomesmuch greater. Preventive treatment must be given to many peoplewho are not ill, who are unaware that they are infected, andfor whom preventive therapy may be only a low priority; at thesame time, effective directly observed therapy and high ratesof completion of treatment among patients with active diseasemust be maintained. Thus, it is critical that control programscontinue and expand, or another surge in tuberculosis may welloccur.
New York City has not yet controlled tuberculosis. In 1994,2995 cases were reported, far more than in any other city inthe United States. The case rate was more than four times thenational average, and there were more patients with multidrug-resistanttuberculosis than in the rest of the country combined. Nevertheless,the recent substantial decrease confirms that this disease canbe prevented and cured, even in persons with HIV infection.32
The costs of the resurgence of tuberculosis have been phenomenal.From 1979 through 1994, there were more than 20,000 excess casesof the disease in New York City — cases that would nothave occurred if previous downward trends had continued. Eachcase cost more than $20,000 in 1990 dollars, for a total exceeding$400 million.33 In addition, as many as one third of patientswith tuberculosis were rehospitalized because of inadequatefollow-up, and thousands of people were hospitalized in orderto rule out the diagnosis. There were additional expendituresfor renovation at Rikers Island (more than $60 million); therenovation of hospitals; and preventive therapy for those whobecame infected during the resurgence. Care will be requiredfor those who become ill, some of them with multidrug-resistantdisease, in the years and decades to come. These costs easilyexceed $1 billion and may reach several times that amount. Thus,despite their cost, efforts to control tuberculosis in the UnitedStates are likely to be highly cost effective.
Tuberculosis is a preventable and curable disease, and the waragainst it can be won. New York City's experience demonstratesthat tuberculosis can be controlled even in populations in whichimmunosuppression is common and the prevalence of drug-resistantorganisms is high. The challenge in the years ahead will beto continue to focus on treating the disease and to expand theuse of preventive treatment for people at high risk, such asclose contacts of patients with tuberculosis, people with HIVinfection, and persons from countries where tuberculosis remainscommon. Because foreign-born persons account for an increasingproportion of cases in the United States, we need to improvescreening and services for immigrants and support internationalprograms to control tuberculosis, which are important, effective,and woefully underfunded.34,35 By doing so, we can ensure thatthe recent decrease in incidence becomes not simply a blip ona curve, but the resumption of a consistent drive to eliminatetuberculosis as a serious threat to public health in the UnitedStates.
We are indebted to the staff members of the Bureau of TuberculosisControl, New York City Department of Health, and to health careworkers throughout New York City for their dedication and commitmentin caring for patients with tuberculosis, and to Ms. DeborahLew for assistance in the preparation of the manuscript.
Source Information
From the New York City Department of Health, New York (T.R.F., P.I.F., R.M.W., M.A.H.); and the Division of Tuberculosis Elimination, National Center for Prevention Services (T.R.F., P.I.F.), and the Division of Field Epidemiology, Epidemiology Program Office (R.M.W.), Centers for Disease Control and Prevention, Atlanta.
Address reprint requests to Dr. Frieden at the Bureau of Tuberculosis Control, 125 Worth St., Box 74, New York, NY 10013.
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