Background One third of the world's population is infected withMycobacterium tuberculosis, and in the developed countries immigrationis a major force that sustains the incidence of tuberculosis.We studied the effects of immigration on the epidemiology oftuberculosis and its recent resurgence in the United States.
Methods We analyzed data from the national tuberculosis reportingsystem of the Centers for Disease Control and Prevention. Since1986 reports of tuberculosis have included the patient's countryof origin. Population estimates for foreign-born persons werederived from special samples from the 1980 and 1990 censuses.
Results The proportion of persons reported to have tuberculosiswho were foreign-born increased from 21.6 percent (4925 cases)in 1986 to 29.6 percent (7346 cases) in 1993. For the entireeight-year period, most foreign-born patients with tuberculosiswere from Latin America (43.9 percent; 21,115 cases) and SoutheastAsia (34.6 percent; 16,643 cases). Among foreign-born personsthe incidence rate was almost quadruple the rate for nativeresidents of the United States (30.6 vs. 8.1 per 100,000 person-years),and 55 percent of immigrants with tuberculosis had the conditiondiagnosed in their first five years in the United States.
Conclusions Immigration has had an increasingly important effecton the epidemiology of tuberculosis in the United States. Itwill be difficult to eliminate tuberculosis without better effortsto prevent and control it among immigrants and greater effortsto control it in the countries from which they come.
The decades-long decline in the incidence of tuberculosis inthe United States was reversed during the late 1980s. The resurgencecontinued into the current decade, and despite a 5.1 percentrelative decline from 1992 to 1993, the number of reported casesin 1993 was 14 percent higher than in the nadir year of 1985.1A limited number of studies have examined the effects of increasesin immigration on the recent epidemiology of tuberculosis inthe United States.2,3,4,5,6 A study by Powell et al. from 1977to 1979 found that foreign-born persons accounted for 15 percentof the reported cases of tuberculosis in the 11 areas studied.2The national surveillance data show that the proportion of diagnosedcases of active tuberculosis in which the patient was foreign-bornincreased from 22 percent in 1986 to almost 30 percent in 1993.1
The increasing contribution of foreign-born persons to the incidenceof tuberculosis has been noted in a number of developed countrieswith substantial levels of immigration.7,8,9,10,11,12,13,14However, there have been no comprehensive epidemiologic studiesin the United States of the incidence rates of tuberculosisamong foreign-born residents. Previous analyses have presentedonly frequency counts or estimates of rates for a limited numberof subgroups of the foreign-born population.2,3,4,5,15 Accurateestimates of incidence rates are needed to develop cost-effectivestrategies for the prevention, control, and ultimate eliminationof tuberculosis.16 Therefore, we have investigated the recentinfluence of immigration on the epidemiology of tuberculosisusing data from the national reporting system for tuberculosisand from U.S. Census Bureau surveys of the foreign-born population.
Methods
Cases
All 50 states and the District of Columbia mandate the reportingof persons with clinically active tuberculosis to local or statehealth authorities.17 The data used in this analysis were derivedfrom the standardized case reports forwarded to the Centersfor Disease Control and Prevention (CDC) by these local or stateauthorities.1 Since 1986 all reports have included data on thepatient's country of origin. All patients with newly diagnoseddisease must be reported, regardless of their legal residencystatus, so long as they consider the community their home orplan to remain in the country for at least 90 days.18 The patient'slegal residency status, if it is ascertained, is not forwardedto the CDC.
The U.S. Census Bureau definition was used to classify personsas foreign-born.19 Anyone born in the United States or a territoryof the United States, as well as anyone born in a foreign countrybut having at least one American parent, was categorized asnative to the United States, or U.S.-born. Persons not meetingthe criteria for the native designation were considered foreign-born.
Information on the date of immigration was incomplete for 24percent of the foreign-born persons reported as having tuberculosis.Excluding patients with incomplete information would have resultedin gross underestimations of the incidence rates. Therefore,since age and world region of origin correlated strongly withlength of residence for patients with complete information,means for length of residence were imputed to those with missingdates on the basis of their ages and world regions of origin.
Population
The population estimates used in this analysis were derivedfrom a 5 percent sample of all U.S. households surveyed as partof the censuses conducted in 1980 and 1990.20 We calculatedintercensal estimates using linear interpolations between the1980 and 1990 censuses. Estimates beyond 1990 were developedby linear extrapolation. The sampling frame for the decennialestimates contained single households as well as group quarters,including homeless shelters, correctional facilities, campsfor migrant workers, and military installations. Data were collectedby the U.S. Census Bureau regardless of residency status, solegal immigrants as well as undocumented persons are includedin these estimates. Data on the number of legal immigrants,as well as estimates of the number of illegal immigrants andresidents, were obtained from reports published by the Immigrationand Naturalization Service.21
Census data may undercount certain minority subpopulations,possibly resulting in inflated disease-rate estimates for theforeign-born population.22,23 However, published estimates ofcensus undercounts suggest that for broad population groupingson a national level the magnitude of these biases would haveno substantial effect on our major findings.19,23
Regions of Origin
To obtain precise rate estimates, we categorized the foreigncountries of origin in eight groups according to geography andeconomic development, using a scheme devised by the World Bank.24The groups are sub-Saharan Africa; India; mainland China; otherAsian countries (excluding India, China, Japan, and countriesof the former Soviet Union); Latin America and the Caribbean;the Middle Eastern crescent; the formerly socialist economiesof Europe, including the countries of the former Soviet Unionas well as the eastern European countries with formerly communisteconomies; and the established market economies, including Canada,Western Europe, Australia, New Zealand, and Japan.
Statistical Analysis
All rates were adjusted for age by the direct method, with thedistribution in the 10-year age intervals in 1990 used as thestandard.24 Standard errors for age-adjusted rate ratios wereestimated with a simple approximation to the Poisson probabilitydistribution.25,26 We present 99 percent confidence intervalsbecause of the design effect associated with the complex samplingprocedures used to derive the population estimates.20,25,27Pearson correlation coefficients were calculated with two-sidedP values.
We used logistic regression to assess the effects of adjustmentfor multiple covariates other than age.28 We present the resultsfrom the model containing only main effects.29
Results
From 1986 through 1993, 195,186 persons were given a diagnosisof tuberculosis and were reported to the CDC. Only 1.2 percentof the reports had incomplete information about the countryof origin or age and were excluded from our analysis. The proportionof patients reported to have tuberculosis who were classifiedas foreign-born increased from 21.6 percent (4925) in 1986 to29.6 percent (7346) in 1993. The estimated rates of tuberculosisamong foreign-born persons also increased (Figure 1). From 1986to 1989 the average annual rate in the foreign-born populationwas 27.1 per 100,000 persons. After 1989 the number of documentedimmigrants increased greatly. This increase included previouslyillegal long-term residents who were allowed to adjust theirresidency status under provisions of the Immigration Reformand Control Act of 1986. Immigrants adjusting their status werealso screened for tuberculosis as part of this special admissionprocess. From 1990 to 1993 the incidence rate of tuberculosisin the foreign-born population increased to 33.6 per 100,000.During the entire eight-year period, the overall rate in theU.S.-born population remained relatively constant at about 8.1per 100,000.
Figure 1. Number of Legal Immigrants According to Year of Admission (Bars) and Tuberculosis Case Rates for U.S.-Born (Broken Line) and Foreign-Born (Solid Line) Persons.
The gray portions of the bars represent the numbers of illegal residents who were granted legal residence status under the provisions of the Immigration Reform and Control Act of 1986. The Immigration Act of 1990 liberalized the screening procedures for tuberculosis in legal immigrants (see the Discussion section). All rates are adjusted for age to the 1990 U.S. population distribution.
When people with tuberculosis were stratified according to age,the largest relative difference between those who were foreign-bornand those who were born in the United States was evident amongchildren less than 15 years of age (Table 1). The annual rateamong foreign-born children was so great that it exceeded thehighest age-specific rate among native persons by 54 percent.
Table 1. Tuberculosis Case Rates in the United States According to Place of Birth and Demographic Variables, 1986 to 1993.
There was substantial heterogeneity in the effect of foreignbirth on the rate of tuberculosis across racial and ethnic groups.The greatest difference was noted in the Asian population, whereasthere was relatively little difference in the rates betweenforeign-born and U.S.-born blacks or Hispanics (Table 1).
The incidence of tuberculosis in foreign-born persons residingin the western United States was almost twice the rate amongforeign-born persons in the rest of the country (Table 1). Incontrast, the highest rates of tuberculosis for U.S.-born personswere in the Northeast. There was little correlation betweenthe state-specific rates for foreign-born persons and thosefor U.S.-born persons (Figure 2).
Figure 2. Correlation between State-Specific Tuberculosis Case Rates for Foreign-Born Persons and U.S.-Born Persons in the United States, 1986 to 1993.
All rates are adjusted for age to the 1990 U.S. population distribution. The solid line is the best-fit regression line, and the correlation coefficient was calculated by the Pearson method.
The incidence of tuberculosis in foreign-born persons variedsubstantially according to the world region of origin (Table 2).People from Asian countries other than India, Japan, mainlandChina, and countries of the former Soviet Union had the highestrate. Of the 16,643 persons from this region with a diagnosisof tuberculosis, 92.2 percent were from five countries: thePhilippines (6286 cases); Vietnam (4941); South Korea (2262);Cambodia (977); and Laos (878). Although the rate of tuberculosiswas highest in those from Asia, there were more patients withtuberculosis from Latin America, and Mexico was the countryof origin for 56.8 percent of the 21,115 patients from LatinAmerica.
Table 2. Tuberculosis Case Rates According to the Length of Residence in the United States and the World Region of Origin for Foreign-Born Persons in the United States, 1986 to 1993.
The length of residence in the United States was strongly relatedto the rate of tuberculosis among foreign-born persons, withthe highest rates occurring in the first five years after arrival.Overall, 55 percent of the tuberculosis cases in the foreign-bornpopulation were diagnosed in the first five years of residencein the United States. Of the 35,399 foreign-born patients whoserecords contained complete information on the month and yearof immigration, 10,478 (29.6 percent) received diagnoses oftuberculosis less than one year after their entry into the UnitedStates. The highest average annual rate for the first five yearsafter arrival was among persons from the other-Asian-countriesregion. In contrast, the rate for recent arrivals from countrieswith established market economies was lower than the rate forU.S.-born Americans.
We used logistic regression to adjust simultaneously for thepotential confounding effects of selected demographic and geographicvariables. The major determinants of risk in the foreign-bornpopulation were the region of the world from which the personemigrated and the number of years in the United States (Table 3).The rate ratio for the incidence of tuberculosis among foreign-bornpersons in the western United States as compared with the incidencein foreign-born persons in the rest of the country decreasedsubstantially, from 1.7 to 1.3, after adjustment for other factors.
Table 3. Age-Adjusted and Multivariable Analysis of Rate Ratios for Tuberculosis among Foreign-Born Persons in the United States According to Selected Variables, 1986 to 1993.
Discussion
Recent reports from Canada, New Zealand, Britain, and westernEurope have documented that immigration from nations where tuberculosisis common has been largely responsible for slowing the decreasein morbidity rates in these developed countries.7,10,11,30 Inthe United States, approximately 8.2 million immigrants werelegally granted permanent residence from 1986 through 1993.There were 3 to 4 million illegal foreign-born residents bythe early 1990s.21 Therefore, between 1980 and 1990 the foreign-bornpopulation in this country increased by over 40 percent.19 Thetop five countries of origin during this period were Mexico,the Philippines, Vietnam, China, and Korea.21 The tuberculosisincidence rates in these countries are 10 to 30 times greaterthan the rate in the United States.31 Our findings suggest thatthe increase in immigration during the late 1980s and early1990s has profoundly affected the recent epidemiology of thisdisease in the United States.
National tuberculosis rates among people born in the UnitedStates did not vary substantially during the period of thisstudy. This general stability obscures the increases in someareas, particularly urban centers with large numbers of personsinfected with the human immunodeficiency virus (HIV).32 Thereare currently only limited national data on the proportion ofpatients with tuberculosis who are infected with HIV.1 Focusedseroprevalence studies from tuberculosis clinics indicate thatforeign-born patients from the countries that contribute thegreatest number of immigrants have substantially lower ratesof HIV infection than have patients born in the United States.33These data, in combination with the legal restriction that makesHIV infection a bar to immigration to the United States, suggestthere is little likelihood that HIV coinfection has contributedto recent increases in tuberculosis rates among foreign-bornpersons.34
The high relative rate of tuberculosis in foreign-born childrenindicates that there is substantial recent transmission eitherbefore or shortly after immigration.35 From our data it is difficultto determine the importance of active transmission within theforeign-born community after immigrants' arrival in the UnitedStates. However, a recent study from San Francisco using thetechnique of restriction-fragmentlength polymorphismconcluded that active tuberculosis in foreign-born persons wasmore likely to result from reactivation of remote infectionthan from recent transmission in the local community.36 Theabsence of correlation between state-specific disease ratesfor the foreign-born and those for the native population suggeststhat transmission to U.S.-born persons is probably not extensive.
The elevated rates among young foreign-born persons are consistentwith the results of studies that report positive tuberculin-skin-testreactions in 35 to 53 percent of young foreign-born personsfrom Southeast Asia and Latin America.36,37,38,39,40 Young foreign-bornpersons with latent tuberculosis infections represent a growingpool of immigrants in whom active disease will continue to developunless major efforts are mounted to screen for infection andprovide treatment.6,16,41
Several factors explain the finding that the highest rates oftuberculosis among foreign-born persons occur within a few yearsof their arrival in the United States.3,5 First, only immigrantsand refugees applying for permanent legal residence are screenedfor tuberculosis. Persons allowed to change their status fromillegal to legal under the provisions of the Immigration Reformand Control Act of 1986 were also screened. Applicants for immigrationwho have abnormal screening chest radiographs as well as positivesmears for acid-fast bacilli on sputum examinations must begintherapy that is effective in converting their sputum smearsto negative, and each must obtain a waiver from a responsiblehealth care provider in the United States before he or she canenter or remain in the country.34 Before implementation of theImmigration Act of 1990 (Figure 1), people with abnormal chestradiographs indicative of active tuberculosis but with negativesputum smears were also required to obtain waivers.6 However,the criteria for exclusion were liberalized to make it easierfor overseas immigrants who were considered noninfectious (i.e.,whose sputum smears were negative) to receive treatment in theUnited States. This was done to discourage such persons fromreceiving suboptimal treatment overseas that could promote theselection of resistant organisms.6,34
Studies in recent Southeast Asian immigrants have found thatsputum smears are relatively insensitive in detecting clinicallyactive Mycobacterium tuberculosis.6,9,42,43 There are currentlyno federal regulations prescribing follow-up procedures forthose with suspicious chest radiographs who have negative sputumsmears, although they are reported to local health departmentsby federal authorities. The number who are actually evaluatedis unknown, since many notification forms sent to state andlocal health departments are never returned to the CDC (TippleM, Division of Quarantine, CDC: personal communication). Hence,substantial numbers of persons undoubtedly enter the countrywith active disease but when they later come to the attentionof health care workers in the United States they are countedas representing new, previously unidentified cases.3,5,6
A second factor contributing to the high rates among recentarrivals is the decreased risk of tuberculosis with lengtheningtime after infection.12 The annual risk of infection in manyof the countries of origin is 100 to 200 times the rate in theUnited States.2,12,44,45 Therefore, the rate of disease amongimmigrants is greatest within the first few years after entry,because they are much more likely to be infected before departurethan after their arrival in the United States.
Another reason for high incidence rates among recent arrivalsis the more than 20 million nonimmigrant visitors and studentsand the estimated 200,000 undocumented immigrants who enterthe United States every year.21 People in these groups do notundergo a prescribed medical evaluation before entry, and somearrive with active disease that is then diagnosed and reportedin the United States. The impact of visitors and students andof undocumented residents on the rate of tuberculosis amongforeign-born persons is impossible to estimate from our surveillancedata. Local health departments are frequently reluctant to inquireabout legal status because illegal residents with infectiousdisease may delay seeking care if they suspect they will bereported to immigration authorities.46
Our analyses indicate that improvements are needed in screeningimmigrants and refugees overseas, as well as in communicatingthe results of screening examinations to responsible publichealth and medical officials.6,16,47 Physicians in the UnitedStates who care for foreign-born persons should be aware thattheir patients from developing countries are at increased riskfor tuberculosis even if they have been medically cleared duringthe legal immigration process, since that screening focusesexclusively on the identification of highly infectious persons(i.e., those whose sputum smears are positive for acid-fastbacilli). Also, programs that minimize barriers to appropriatescreening and chemoprophylaxis have to be available to foreign-bornresidents if progress is to be made in the control of tuberculosis.6,16,41,47
Finally, recent reports document that the treatment and controlof tuberculosis is one of the most cost-effective health interventionsfor developing countries.24,48 Future success in tuberculosiscontrol in this country will require greater efforts by theUnited States, in coordination with other countries and internationalorganizations, to upgrade the standards and quality of tuberculosis-controlprograms in developing countries.6,31,49 These endeavors maybe most efficiently pursued in Latin America and Southeast Asia,which supply the greatest numbers of immigrants to the UnitedStates.
We are indebted to state and local tuberculosis-control officialsin health departments throughout the United States who collectedand reported the data used in this analysis, and to the surveillancestaff at the Division of Tuberculosis Elimination, CDC, whohave maintained this information over time; to Dr. Nancy Binkinfrom the Division of Tuberculosis Elimination for comments onearly versions of the manuscript; to Dr. Margaret Tipple fromthe Division of Quarantine, CDC, for valuable assistance; andto Robert Pratt for his help with the computer programming.
Source Information
From the Division of Tuberculosis Elimination, Centers for Disease Control and Prevention, 1600 Clifton Rd. E-10, Atlanta, GA 30333, where reprint requests should be addressed to Dr. McKenna.
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