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(Chest. 2004;126:1777-1782.)
© 2004 American College of Chest Physicians

Screening of Immigrants and Refugees for Pulmonary Tuberculosis in San Diego County, California*

Philip A. LoBue, MD, FCCP and Kathleen S. Moser, MD, MPH

* From the Centers for Disease Control and Prevention, National Center for HIV, STD and TB Prevention (Dr. LoBue), Division of Tuberculosis Elimination, Field Services Branch, Atlanta, GA; and Tuberculosis Control Program (Dr. Moser), County of San Diego Health and Human Services Agency, San Diego, CA.

Correspondence to: Philip A. LoBue, MD, FCCP, Centers for Disease Control and Prevention, National Center for HIV, STD and TB Prevention, Division of Tuberculosis Elimination, Field Services and Evaluation Branch, Mail Stop E-10, 1600 Clifton Rd, Atlanta, GA 30333; e-mail: pgl5{at}cdc.gov


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: To evaluate the outcomes of a tuberculosis (TB) screening program for recent immigrants to San Diego County, CA, and to compare the demographic and clinical characteristics of pulmonary TB cases occurring in recently arrived foreign-born persons detected through this screening with those of similar cases found through routine surveillance.

Design: Retrospective review of computer databases and medical records.

Setting: Local public health department.

Patients: Recent immigrants and refugees classified as TB suspects in their country of departure and foreign-born patients with active TB detected through routine surveillance.

Results: Five hundred seventy-one of 658 immigrants and refugees (87%) of completed screening. Thirty-nine subjects (7%) were found to have active TB, and 433 subjects (76%) were found to have latent TB. A diagnosis of active TB was associated with age of 25 to 44 years (odds ratio, 3.6; 95% confidence interval, 1.1 to 11.6) and A (odds ratio, 25.7; 95% confidence interval, 1.3 to 512.2) or B1 classifications (odds ratio, 4.3; 95% confidence interval, 1.5 to 12.5). Cases detected through screening comprised 12% of all reported foreign-born persons with active TB. Compared to other recently arrived foreign-born persons with active TB, those detected through immigrant screening were more likely to be Asian and born in the Philippines and less likely to have advanced disease.

Conclusions: Most immigrants and refugees classified as TB suspects by foreign screening completed the US screening process, which had a high yield for detecting active and latent TB. Only a minority of foreign-born persons (12%) with active TB were discovered through this program, however, and additional measures are needed to facilitate early case finding in other foreign-born populations.

Key Words: immigrant • refugee • screening • tuberculosis


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
In 2002, persons born outside of the United States accounted for at least half of tuberculosis (TB) cases reported in the United States for the first time.1 Between 1992 and 2002, the number of US states with > 50% of TB cases diagnosed in foreign-born persons increased from 4 to 22, with 5 states reporting > 70% of their cases occurring in persons born outside of the United States.1 Thus, expanded screening of immigrants for TB is a priority among the measures required to achieve TB elimination.2

Currently, all persons attempting to enter the United States as refugees or through application for an immigrant visa must undergo a medical examination that includes screening for active TB. The TB screening process, which has been described previously, occurs in two phases: it is initiated by panel physicians (selected by the US Department of State) in the country of departure and completed in the United States by state and local health departments.3 Briefly, all immigrants and refugees at least 15 years of age are required to have a chest radiograph (CXR). Based on the CXR results, the panel physician determines if the immigrant should submit three sputum specimens for acid-fast bacilli (AFB) smear staining. Using the CXR and sputum results, the immigrant is classified as class A (active TB; infectious [AFB smear positive]); class B1 (active TB; noninfectious [AFB smear negative]); or class B2 (inactive TB) or no TB infection. Individuals with active or inactive TB are required to report to the local or state health department for further evaluation after arriving in the United States. Those with infectious TB cannot enter the United States until they have received sufficient treatment to render them noninfectious. Immigrants < 15 years of age are not required to have a CXR routinely. If such individuals have had contact with a known TB case or are suspected of having TB for other reasons, they must undergo a tuberculin skin test (TST). If there is induration or erythema of any size, a CXR is required. Additional evaluation is conducted as it is for persons > 15 years old.

In San Diego County, CA, the local TB control program conducts the US phase of the TB screening for immigrants and refugees arriving in the county who are suspected of having TB based on their overseas evaluation. To determine the yield of our screening process, we reviewed outcomes of individuals undergoing examination. Data were not available as to the total number of immigrants and refugees who began the screening process in their countries of origin; therefore, our analysis was limited to individuals suspected of having TB who were referred by the Centers for Disease Control and Prevention (CDC) Division of Global Migration and Quarantine (DGMQ), the agency that administers the immigrant and refugee health screening program. We also compared demographic and clinical characteristics of pulmonary TB cases occurring in recently arrived foreign-born persons detected through this screening with those of similar cases found through routine surveillance.


   Materials and Methods
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 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
The County of San Diego TB Control Program has maintained a computer database since July 2001 for all immigrant and refugee notifications it received from the CDC DGMQ. To evaluate the outcomes of TB screening for these persons, data were extracted from the database and analyzed. Individuals were included if they were registered between July 1, 2001, and June 30, 2003, and they were not continuing the screening process at the time the analysis was performed. Review of medical records maintained within the TB Control Program was used to obtain missing information critical to the analysis.

Panel physicians performed the mandated medical examination in the country of departure. TB notifications were classified as A, B1, or B2 according to the instructions for medical examination provided to the panel physicians by DGMQ (Table 1 ).3 Applicants have up to 6 months to enter the United States after their TB status has been designated.


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  		Table 1.. TB Classifications

 
Initial testing for TB in San Diego included a CXR, TST (Mantoux method), and medical examination by a physician. Additional testing, such as sputum examination, was performed at the discretion of the evaluating physician. Screening outcomes were classified as no infection; latent TB infection (LTBI); old, healed TB; and active TB as defined in Table 2 . A patient with active pulmonary TB was considered sputum AFB smear positive if at least one sputum smear had AFB seen on microscopy.


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  		Table 2.. Screening Outcomes: Definitions and Results*

 
Data items extracted included sex, age, race/ethnicity, country of birth, immigration status (immigrant, refugee, or other visa type—eg, asylee, fiancé), TB notification class, sputum AFB smear results, mycobacterial culture results, outcome of US screening, and time elapsed between foreign and US evaluations. Race/ethnicity was self-reported and categorized as Hispanic; white, non-Hispanic; black, non-Hispanic; Asian-Pacific Islander; or other. The following additional items were extracted for patients with active TB: prior TB treatment history, CXR results (cavitary vs noncavitary), and antituberculous drug susceptibility results.

To compare the characteristics of patients with active pulmonary TB identified through immigration screening with those of recent foreign-born active pulmonary TB patients discovered through routine surveillance (ie, reported to the health department by local medical providers), identical data items were extracted from the local CDC Tuberculosis Information Management System database for all other foreign-born patients with active pulmonary TB who were reported during the same time period and who had been in the United States for ≤ 1 year.

Ratios were calculated and compared in a univariate analysis using the {chi}2 and Fisher exact tests. Multivariate logistic regression was performed to adjust for the effects of multiple explanatory variables in determining their association with one outcome of interest, specifically whether the immigrant was found to have active pulmonary TB. Explanatory variables were included in the model if they were associated with the outcome in the univariate analysis (p < 0.10). For explanatory variables with more than two categories, the category with the lowest rate of association was chosen as the reference category. Goodness of fit was adequate according to the Hosmer-Lemeshow test.4 There was no evidence of collinearity as measured by variance inflation factor analysis (< 2.5 for all independent variables).4 Associations between independent and dependent variables were considered significant at p < 0.05. Median days elapsed between foreign and US evaluations for different groups were compared using the Kruskal-Wallis test. Statistical analyses were performed using Statistical Package for the Social Sciences software (Version 11.0; SPSS; Chicago, IL).

This project was reviewed by the Office of the Associate Director of Science for the National Center for STD, HIV and TB Prevention, and considered not to be research involving human subjects. It was, therefore, not submitted to an institutional review board. To protect patient confidentiality, the database is password protected. In addition, after data were exported to SPSS for analysis, all specific identifiers (eg, name, medical record number) were removed.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
The County of San Diego TB Control Program was notified by the CDC of 658 immigrants and refugees who required screening during the 2-year period. Seventy-seven subjects (12%) did not complete the screening process (9 were never located, 55 moved outside the county prior to completing their evaluation, and 13 refused evaluation). Five hundred seventy-one immigrants and refugees (88%) underwent screening for TB. Demographic characteristics and immigration status of these individuals are shown in Table 3 .


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  		Table 3.. Demographic Characteristics and Immigration Status of Immigrants and Refugees Screened in San Diego County, July 2001–June 2003

 
Outcomes of screening are shown in Table 2. Active pulmonary TB was diagnosed in 39 patients (7%), 33 of whom (85%) had one or more sputum cultures positive for Mycobacterium tuberculosis. Ten patients (26% of patients with active TB or 2% of all persons screened) had one or more sputum smears with AFB seen on microscopy. Seven of the culture-positive patients (18%) had isoniazid-resistant TB, and one patient (3%) had multidrug-resistant TB. The patient with multidrug-resistant TB was AFB smear positive; all of the isoniazid-resistant patients were smear negative. A diagnosis of active TB was statistically significantly associated with the 25- to 44-year-old age group and A and B1 classifications (Table 4 ). The time elapsed, measured in median days (interquartile range), between foreign and US evaluations did not differ significantly (p = 0.62) based on a diagnosis of active TB and sputum AFB smear status (not active TB, 118 days [85 to 179 days]; active TB, AFB sputum smear negative, 109 days (62 to 188 days); and active TB (62 to 188 days, AFB sputum smear positive, 157 days [84 to 182 days]).


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  		Table 4.. Multivariate Analysis of Factors Associated With Diagnosis of Active Pulmonary TB

 
Between July 1, 2001 and June 30, 2003, 339 pulmonary TB cases occurring among foreign-born persons were reported in San Diego County. Of patients with active TB detected within 1 year of entering the United States, 39% (39 of 100 patients) were found through the immigrant/refugee screening process. Patients with active TB detected through immigration screening were more likely to be Asian-Pacific Islanders, born in the Philippines, while other recently arrived foreign-born TB patients were more likely to be Hispanic and born in Mexico (Table 5 ). TB patients discovered through immigration screening were less likely to have cavities on CXR and positive sputum AFB smears.


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  		Table 5.. Comparison of Pulmonary TB Cases Detected Through Immigration Screening and Other Pulmonary TB Cases Detected in Foreign-Born Patients in United States for < 1 Year

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
With regard to TB, the purpose of the mandated medical examination for immigrants and refugees is to prevent persons with highly infectious TB (ie, pulmonary sputum AFB-positive TB) from entering the United States.3 In addition, this program identifies persons who are at risk to progress to infectious TB, including individuals with active pulmonary TB, sputum AFB smear negative, and those with old, healed TB. In this context, we wanted to evaluate three aspects of the screening program from a local perspective: (1) how successful was it in preventing sputum AFB smear-positive patients from entering the United States, (2) what was the yield in finding persons with AFB smear-negative pulmonary TB and latent TB infection (with or without radiographic changes of old, healed TB), and (3) which recent immigrants did the screening program fail to detect.

Of the 571 immigrants and refugees screened locally, 10 subjects (2%) were found to have sputum AFB smear-positive TB. Compared to recently arrived foreign-born TB patients found through routine surveillance (ie, TB patients reported to the health department by local medical providers), patients discovered through screening tended to have less advanced disease as manifested by a lower percentage of patients with positive sputum AFB smears and cavities on CXR. A study5 conducted in California in from 1992 to 1995 had similar findings; many of the advanced, sputum AFB smear-positive cases were screened out in their country of departure, suggesting that the program was reasonably successful in this regard. Nevertheless, infectious TB cases did arrive in the United States. One possible explanation is that the patients had progression of their disease in the interval between their foreign evaluation and their arrival in San Diego. This explanation seems reasonable given that the median time elapsed between foreign and US examinations was > 5 months for sputum AFB smear-positive patients. Alternatively, specimen collection or laboratory techniques may have been suboptimal in the country of origin. Finally, one cannot exclude the possibility of intentional sputum substitution.

A number of studies have evaluated the yield of TB screening for persons immigrating to the United States. Examining cohorts of immigrants in the early 1990s, the rate of active TB was found to vary between 1% and 14%.35678 We found a rate of active TB in the middle of this range (7%). In addition to the high rate of case detection, > 75% of persons evaluated had LTBI, 60% of whom had radiographic evidence of prior TB. These findings are similar to those described for a cohort of immigrants examined in San Francisco from 1992 to 1993, and they demonstrate that new immigrant screening provides an excellent opportunity for TB prevention through LTBI treatment of a high-risk group.7 Because of their high yield for active and latent TB, immigrant-screening programs can be effective in improving TB control if recommendations for LTBI treatment are followed.9

Despite the high yield of such programs, they only detect a minority of foreign-born patients with active TB.10 In our study, 39% of pulmonary TB cases occurring in foreign-born persons residing in the United States for < 1 year (and 12% of all foreign-born pulmonary TB cases) were found through the screening process. Even more striking is the fact that only 3% of Mexican-born TB patients residing in the United States for < 1 year were discovered through immigrant screening. Given the location of San Diego on the United States/Mexico border, it is surprising that so few new immigrants from Mexico (16 total) were screened by the San Diego TB Control Program. This figure appears to be confirmed, however, by data extracted from the DGMQ database, showing that since 2001 only 23 persons immigrating from Mexico, designated as TB class A or B, listed San Diego County as their US destination (personal communication; C. Fan, CA; Department of Health Services, TB Control Branch; December 2003).

An analysis11 of foreign-born patients with TB in Tarrant County, TX, found that 59% of cases occurred in permanent residents (including legal immigrants and refugees), 25% occurred in undocumented immigrants, and 17% occurred in nonimmigrant visitors (eg, tourists, students) As in our study, these data reveal that a large fraction of reported cases among recent arrivals, especially TB occurring in tourists, students, temporary workers, and undocumented immigrants, are not detected through existing screening mechanisms, and among groups screened on entry into the United States (legal immigrants, refugees), TB reactivation more frequently occurred years after arrival. The latter cases could, in theory, be prevented if targeted tuberculin testing and LTBI treatment guidelines were followed closely and patients adhered to treatment.

Because of the gaps in the ability of current US immigrant screening practices to detect and prevent TB among foreign-born persons, additional measures have been advocated. Such measures might include the use of TST along with CXR for overseas screening of immigrants and refugees.2 This would increase the detection of LTBI in these groups, and allow for subsequent referral to local US health departments for LTBI treatment. The Institute of Medicine has also recommended TST for individuals from high TB incidence countries, already living in the United States, who are adjusting their immigration status (eg, applying for permanent residency).2 Another possible approach would be for local health departments to partner with primary medical providers to offer TB and LTBI screening and treatment for high-risk immigrants as part of routine health care. This approach can reach a wide variety of foreign-born persons, not just recent legal immigrants and refugees.

Our study has several limitations. First, approximately 12% of immigrants and refugees did not complete the screening process. This may have affected the rates of detection for active cases and latent TB. Additionally, we have no data on the number of immigrants and refugees that were screened in their country of departure, were (correctly or incorrectly) believed not to have any evidence of pulmonary TB and therefore were not referred for follow-up evaluation in the United States. The detection of some TB cases may be delayed for this reason.

In summary, we found that almost 90% of immigrants and refugees identified as high risk for TB during the initial overseas screening procedures completed the local health department TB screening process after arriving in the United States. The local screening program had a high yield for detecting active and latent TB. Immigrant and refugee screening, however, identified only a minority of TB cases in the foreign-born reported in San Diego County (12% of all foreign born cases reported and 39% of those residing in the United States for < 1 year). To maximize effectiveness, further emphasis should be placed on identifying and treating immigrants and refugees with LTBI. In addition, strategies are needed for earlier case finding in immigrants not currently screened prior to US entry.2


   Footnotes
 
Abbreviations: AFB = acid-fast bacillus; CDC = Centers for Disease Control and Prevention; CXR = chest radiograph; DGMQ = Division of Global Migration and Quarantine; LTBI = latent tuberculosis infection; TB = tuberculosis; TST = tuberculin skin test

Funding was provided by a Centers for Disease Control and Prevention Tuberculosis Elimination Cooperative Agreement (U52/CCU900452-20).

Received for publication March 11, 2004. Accepted for publication July 13, 2004.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. . Centers for Disease Control and Prevention (2003) Trends in tuberculosis morbidity—United States, 1992–2002. MMWR Morb Mortal Wkly Rep 52,217-222[Medline]
  2. Institute of Medicine. Ending neglect: the elimination of tuberculosis in the United States. 2000,87-97 National Academy Press. Washington, DC:
  3. Binkin, NJ, Zuber, PL, Wells, CD, et al Overseas screening for tuberculosis in immigrants and refugees to the United States: current status. Clin Infect Dis 1996;23,1226-1232[ISI][Medline]
  4. Armitage, P, Berry, G, Matthews, JNS Statistical methods in medical research 2002,358-359 Blackwell Science. Oxford, UK: 494–495
  5. Sciortino, S, Mohle-Boetani, J, Royce, SE, et al B notifications and the detection of tuberculosis among foreign-born recent arrivals in California. Int J Tuberc Lung Dis 1999;3,778-785[ISI][Medline]
  6. Zuber, PL, Binkin, NJ, Ignacio, AC, et al Tuberculosis screening for immigrants and refugees: Diagnostic outcomes in the state of Hawaii. Am J Respir Crit Care Med 1996;154,151-155[Abstract]
  7. DeRiemer, K, Chin, DP, Schecter, GF, et al Tuberculosis among immigrants and refugees. Arch Intern Med 1998;158,753-760[Abstract/Free Full Text]
  8. Centers for Disease Control and Prevention. Tuberculosis among foreign-born persons who had recently arrived in the United States—Hawaii, 1992–1993 and Los Angeles County, 1993. MMWR Morb Mortal Wkly Rep 1995;44,703-707[Medline]
  9. Schwartzman, K, Menzies, D Tuberculosis screening of immigrants to low-prevalence countries: a cost-effectiveness analysis. Am J Respir Crit Care Med 2000;161,780-789[Abstract/Free Full Text]
  10. Menzies, D Controlling tuberculosis among foreign born within industrialized countries: expensive band-aids. Am J Respir Crit Care Med 2001;164,914-915[Free Full Text]
  11. Weis, SE, Moonan, PK, Pogoda, JM, et al Tuberculosis in the foreign-born population of Tarrant county, Texas by immigration status. Am J Respir Crit Care Med 2001;164,953-957[Abstract/Free Full Text]



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