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Effect of a Culture-Based Screening Algorithm on Tuberculosis Incidence in Immigrants and Refugees Bound for the United States: A Population-Based Cross-sectional StudyTB Screening in Immigrants and Refugees Bound for the United States

Yecai Liu, MS; Drew L. Posey, MD, MPH; Martin S. Cetron, MD; and John A. Painter, DVM, MS
[+] Article, Author, and Disclosure Information

From Centers for Disease Control and Prevention, Atlanta, Georgia.

Disclaimer: The findings and conclusions of this article are those of the authors and do not necessarily represent the official position of the CDC.

Acknowledgment: The authors thank Mr. Wei-Lun Juang for computer programming support, Mr. Curtis Blanton for providing statistical consultation, and Ms. Zanju Wang for obtaining immigrant arrival data from the U.S. Department of Homeland Security. They also thank the staff of the CDC's EDN team for managing the notification system for TB in immigrants and refugees, the staff of the CDC's quarantine stations for collecting overseas medical examination forms at the ports of entry, panel physicians for performing overseas TB screening, the staff of the state and local health department for conducting follow-up evaluation, and Dr. Nancy Rytina of the U.S. Department of Homeland Security for providing summary data of immigrant arrivals.

Disclosures: Authors have disclosed no conflicts of interest. Forms can be viewed at www.acponline.org/authors/icmje/ConflictOfInterestForms.do?msNum=M14-2082.

Reproducible Research Statement:Study protocol and data set: Not available. Statistical code: Available from Mr. Liu (e-mail, yliu@cdc.gov).

Requests for Single Reprints: Yecai Liu, MS, Division of Global Migration and Quarantine, Centers for Disease Control and Prevention, 1600 Clifton Road, MS-E03, Atlanta, GA 30333; e-mail, yliu@cdc.gov.

Current Author Addresses: Mr. Liu and Drs. Posey, Cetron, and Painter: Division of Global Migration and Quarantine, Centers for Disease Control and Prevention, 1600 Clifton Road, MS-E03, Atlanta, GA 30333.

Author Contributions: Conception and design: Y. Liu, D.L. Posey, M.S. Cetron, J.A. Painter.

Analysis and interpretation of the data: Y. Liu, D.L. Posey, M.S. Cetron, J.A. Painter.

Drafting of the article: Y. Liu, M.S. Cetron, J.A. Painter.

Critical revision of the article for important intellectual content: Y. Liu, D.L. Posey, M.S. Cetron, J.A. Painter.

Final approval of the article: Y. Liu, D.L. Posey, M.S. Cetron, J.A. Painter.

Provision of study materials or patients: M.S. Cetron.

Statistical expertise: Y. Liu, M.S. Cetron, J.A. Painter.

Obtaining of funding: M.S. Cetron, J.A. Painter.

Administrative, technical, or logistic support: M.S. Cetron, J.A. Painter.

Collection and assembly of data: Y. Liu, M.S. Cetron, J.A. Painter.


Ann Intern Med. 2015;162(6):420-428. doi:10.7326/M14-2082
Text Size: A A A

Background: Before 2007, immigrants and refugees bound for the United States were screened for tuberculosis (TB) by a smear-based algorithm that could not diagnose smear-negative/culture-positive TB. In 2007, the Centers for Disease Control and Prevention implemented a culture-based algorithm.

Objective: To evaluate the effect of the culture-based algorithm on preventing the importation of TB to the United States by immigrants and refugees from foreign countries.

Design: Population-based, cross-sectional study.

Setting: Panel physician sites for overseas medical examination.

Patients: Immigrants and refugees with TB.

Measurements: Comparison of the increase of smear-negative/culture-positive TB cases diagnosed overseas among immigrants and refugees by the culture-based algorithm with the decline of reported cases among foreign-born persons within 1 year after arrival in the United States from 2007 to 2012.

Results: Of the 3 212 421 arrivals of immigrants and refugees from 2007 to 2012, a total of 1 650 961 (51.4%) were screened by the smear-based algorithm and 1 561 460 (48.6%) were screened by the culture-based algorithm. Among the 4032 TB cases diagnosed by the culture-based algorithm, 2195 (54.4%) were smear-negative/culture-positive. Before implementation (2002 to 2006), the annual number of reported cases among foreign-born persons within 1 year after arrival was relatively constant (range, 1424 to 1626 cases; mean, 1504 cases) but decreased from 1511 to 940 cases during implementation (2007 to 2012). During the same period, the annual number of smear-negative/culture-positive TB cases diagnosed overseas among immigrants and refugees bound for the United States by the culture-based algorithm increased from 4 to 629.

Limitation: This analysis did not control for the decline in new arrivals of nonimmigrant visitors to the United States and the decrease of incidence of TB in their countries of origin.

Conclusion: Implementation of the culture-based algorithm may have substantially reduced the incidence of TB among newly arrived, foreign-born persons in the United States.

Primary Funding Source: None.

Figures

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Appendix Figure 1.

The smear-based overseas TB screening algorithm.

TB = tuberculosis.

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Appendix Figure 2.

The culture-based overseas TB screening algorithm.

IGRA = interferon-γ release assay; TB = tuberculosis; TST = tuberculin skin test; WHO = World Health Organization.

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Figure 1.

Immigrants and refugees who were screened for TB overseas by the smear-based algorithm or the culture-based algorithm.

TB = tuberculosis.

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Figure 2.

Immigrants and refugees identified with class B1 or B2 TB by the smear-based algorithm and those identified with class B1 TB by the culture-based algorithm.

TB = tuberculosis.

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Figure 3.

TB cases diagnosed overseas among 1 561 460 immigrants and refugees who were screened by the culture-based algorithm.

TB = tuberculosis.

* 14 cases of TB were diagnosed in 2007: 2 (14.3%) cases of smear-positive/culture-positive TB, 1 (7.1%) case of smear-positive/culture-negative TB, 4 (28.6%) cases of smear-negative/culture-positive TB, and 7 (50.0%) cases of clinically diagnosed TB.

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Figure 4.

Comparison of reported TB cases among foreign-born persons within 1 y after arrival in the United States and smear-negative/culture-positive TB cases diagnosed overseas among immigrants and refugees by the culture-based algorithm.

TB = tuberculosis.

* Had the culture-based algorithm not been implemented, cases of smear-negative/culture-positive TB likely would have been imported to the United States and counted as reported cases among foreign-born persons within 1 y after arrival by the U.S. National Tuberculosis Surveillance System.

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Comments

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Computational approach to Mycobacterium tuberculosis
Posted on March 25, 2015
Carlos Polanco, Ph.D. (*,a), and Vladimir Uversky Ph.D. (b)
(*,a) Universidad Nacional Autonoma de Mexico, Mexico City, Mexico. (b) University of South Florida, Tampa Florida, US
Conflict of Interest: None Declared
To the editor,

Computational approach to Mycobacterium tuberculosis
We read with the great interest an article by Liu and colleagues emphasizing the use of population-Based cross-sectional study on Tuberculosis (TB) incidence (1) in light of the rise of the multidrug-resistant TB strains (2). Our group has developed a bioinformatics method named "polarity index method" (3) that can be used to differentiate and group proteins based on the peculiarities of polarity distribution within their sequences (4), and applied this tool to a set of proteins associated with TB (unpublished results). This analysis revealed that the TB-associated proteins are characterized by a specific polarity (or electronegativity) profile (5). We believe that this information can be used in the development of new drugs, and think that the effective bioinformatics tools represent crucial means that help eliminating one of the world's most persistent pathogens.

Sincerely,
Carlos Polanco, Ph.D., (*, a)
Vladimir N. Uversky, Ph.D., (b)


(a) Universidad Nacional Autonoma de Mexico, Mexico City, Mexico.
(b) University of South Florida, Tampa Florida, USA.



References

(1) Liu Y, Posey DL, Cetron MS, Painter JA. Effect of a Culture-Based Screening Algorithm on Tuberculosis Incidence in Immigrants and Refugees Bound for the United States: A Population-Based Cross-sectional Study. 2015:7;276fs8 Ann Intern Med. 2015 Mar 17;162(6):420-8. doi: 10.7326/M14-2082.

(2) Sougakoff W. Molecular epidemiology of multidrug-resistant strains of Mycobacterium tuberculosis. Clin Microbiol Infect. 2011;17:800-5. DOI: 10.1111/j.1469-0691.2011.03577

(3) Polanco C, Castanon-Gonzalez JA. Cross-sectional bioinformatics analysis on proteins associated to the Ebola virus Comment to: Hantel A, Olopade CO. Drug and Vaccine Access in the Ebola Epidemic: Advising Caution in Compassionate Use. Ann Intern Med. 2015;162:141-142. DOI:10.7326/M14-2002.

(4) Polanco C, Buhse T, Samaniego JL, Castanon-Gonzalez JA. Detection of selective antibacterial peptides by the Polarity Profile method. Acta Biochim Pol. 2013;60:183-189.

(5) Pauling L. General Chemistry 3rd edition W. H. Freeman & Company Publishers, 1955, pp. 227,621.
Alternative explanations for the decline in TB cases in newly arrived foreign-born perosns in the US
Posted on April 12, 2015
Azariyas A. Challa
Department of Medicine, UPMC, Pittsburgh, PA
Conflict of Interest: None Declared
Liu and colleagues (1) attribute the recent decline in TB cases among newly arrived, foreign-born persons in the US to the number of smear-negative/culture-positive TB cases diagnosed overseas among immigrants and refugees as a result of implementation of the culture-based algorithm by CDC. The observation seems plausible until one considers that in addition to immigrants and refugees who undergo obligatory tuberculosis screening before admittance to the US, foreign-born persons include visitors, students, temporary workers, and unauthorized aliens who are not required to have pre-entry screening (2). In fact, immigrants and refugees constitute only about a third of the estimated 1.3 million foreign-born persons who enter the US yearly for a long term stay (3). The study did not provide specific data about the number of reported TB cases in immigrants and refugees. It, therefore, cannot exclude with certainty the possibility that the observed decrease in the incidence of TB in newly arrived foreign-born persons during the period 2007-2012 was due to changes unrelated to overseas screening.

In recent years, increased attention has been given to TB control in foreign-born persons in US. For example, unlike earlier versions of guidelines for TB control, the 2005 guideline has designated foreign-born persons who have resided in US fewer than 5 years as a particularly high risk group (4). Consequently, several notable efforts at targeted screening and treatment of latent TB infection (LTBI) in foreign-born individuals are underway (5). Perhaps as a result of this enhanced focus, it is a possibility that more newly-arrived, foreign-born individuals received treatment for LTBI during 2007-2012 compared to 2002-2006.

Furthermore, during the period 2007-2012, the authors found that 4032 cases of TB were diagnosed overseas by the culture-based algorithm, of which 2195 were smear-negative/culture-positive and 480 were diagnosed clinically (1). However, the study does not provide similar data for the old smear-based algorithm, preventing evaluation of the effect of the new algorithm on the number of clinically diagnosed cases of tuberculosis by the panel physicians overseas. It is possible that, prior to the culture-based screening, there may have been more clinically diagnosed TB cases than the 480 reported for the period 2007-2012. If that was the case, the study would have overestimated the actual effect of culture-based screening in identifying cases of TB overseas.

In summary, the absence of data distinguishing new TB cases among immigrants and refugees from that found in other foreign-born individuals, and lack of details on the old smear-based algorithm make interpretation of the results less straightforward, and thus dampen the optimism claimed by the authors regarding the effect of the new culture-based screening on the incidence of tuberculosis among foreign-born persons in the United States.

References
1- Liu Y, Posey DL, Cetron MS, Painter JA. Effect of a Culture-Based Screening Algorithm on Tuberculosis Incidence in Immigrants and Refugees Bound for the United States: A Population-Based Cross-sectional Study. Ann Intern Med. 2015 Mar 17;162(6):420-8

2- Cain KP, Haley CA, Armstrong LR, Garman KN et al. Tuberculosis among foreign-born persons in the United States: achieving tuberculosis elimination. Am J Respir Crit Care Med (2007) 175: 75–9.

3- Elizabeth M. Grieco EM, Acosta YD, de la Cruz GP et-al. The Foreign-Born Population in the United States: 2010. American Community Survey Reports. Issued May 2012. ACS-19.

4- ATS, CDC, IDSA. Controlling Tuberculosis in the United States: Recommendations from the American Thoracic Society, CDC, and the Infectious Diseases Society of America. MMWR. 2005; 54 (RR-12); 1-81.

5- Cain KP, Garman KN, Laserson KF, et-al. Moving toward tuberculosis elimination: implementation of statewide targeted tuberculin testing in Tennessee. Am J Respir Crit Care Med. 2012 Aug 1;186(3):273-9

Author's Response
Posted on May 19, 2015
Yecai Liu, MS; Drew L Posey, MD, MPH; Martin S Cetron, MD; John A Painter, DVM, MS
Division of Global Migration and Quarantine, Centers for Disease Control and Prevention
Conflict of Interest: None Declared
Dr. Challa suggested several limitations of the data in our analysis, raising doubts of the effect of a newly implemented overseas culture-based tuberculosis (TB) screening algorithm on reducing the importation of TB to the United States. We discussed some of these limitations in our article, but have reached a different conclusion.

Newly arrived nonimmigrant visitors contribute to the TB burden in the United States (1). Compared to 2002-2006, the mean of annual admissions of nonimmigrant visitors during 2007-2012 decreased 8.5%, but during the same period, the mean of the annual number of reported TB cases among foreign-born persons within 1 year after arrival decreased 24.7% (2). The discrepancy in reductions indicates that the decrease in admissions of nonimmigrant visitors alone could not account for the overall decline of TB cases in the newly arrived foreign-born population.

Dr. Challa suggested that more foreign-born persons were likely to have received treatment for latent TB infection during 2007-2012, causing the decline of TB among newly arrived foreign-born persons. This assumption is not consistent with the results of previous studies. For example, within 1 year after arrival in the United States, only 5.8% of TB cases were likely due to reactivation of latent TB infection (3). Therefore, identifying and treating latent TB infection is unlikely to explain much of the observed decline in TB cases among foreign-born persons within 1 year after arrival.

Dr. Challa indicated that our analysis may not have adequately accounted for clinically diagnosed cases in the old algorithm and suggested a possibility that most smear-negative but culture-positive cases would have been identified by clinical assessment alone. We have not found any studies to support this assumption, and do not believe that, without M. tuberculosis culture, panel physicians could diagnose such large numbers of applicants with smear-negative but culture-positive TB. During post-arrival follow-up evaluation, active TB was diagnosed in 1.8% of persons with Class B1 TB identified by the culture-based algorithm, but in 3.5% of persons with Class B1/B2 TB by the smear-based algorithm (2). These results were consistent with other studies (4,5), suggesting that the culture-based algorithm is more effective.

Despite limitations, we believe our data indicate that implementation of the culture-based algorithm has a substantial effect on preventing the importation of TB to the United States.

Sincerely,

Yecai Liu, MS
Drew L Posey, MD, MPH
Martin S. Cetron, MD
John A. Painter, DVM, MS

1. Liu Y, Painter JA, Posey DL, et al. Estimating the impact of newly arrived foreign-born persons on tuberculosis in the United States. PLoS ONE. 2012. 7(2): e32158.

2. Liu Y, Posey DL, Cetron MS, Painter JA. Effect of a culture-based screening algorithm on tuberculosis incidence in immigrants and refugees bound for the United States: a population-based cross-sectional study. Ann Intern Med. 2015 Mar 17;162(6):420-8

3. Walter ND, Painter JA, Parker M, et al. Persistent latent tuberculosis reactivation risk in the United States immigrants. Am J Respir Crit Care Med. 2014. 189(1):88-95.

4. Lowenthal P, Westenhouse J, Moore M, Posey DL, Watt JP, Flood J. Reduced importation of tuberculosis after the implementation of an enhanced pre-immigration screening protocol. Int J Tuberc Lung Dis. 2011. 15:761-6.

5. Oeltmann JE, Varma JK, Ortega L, et al. Multidrug-resistant tuberculosis outbreak among US-bound Hmong refugees, Thailand, 2005. Emerg Infect Dis. 2008. 14(11):1715-21.
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