Public Health
Volume 120, Issue 8 , Pages 712-723 , August 2006

Balancing prevention and screening among international migrants with tuberculosis: Population mobility as the major epidemiological influence in low-incidence nations

  • D.W. MacPherson

      Affiliations

    • Migration Health Consultants Inc., Hartackerstrasse 77/21190 Vienna, Austria
    • Faculty of Health Sciences, McMaster University, Hamilton, Ontario, Canada
  • ,
  • B.D. Gushulak

      Affiliations

    • Migration Health Consultants Inc., Hartackerstrasse 77/21190 Vienna, Austria
    • Corresponding Author InformationCorresponding author.

Received 20 June 2005 ,Revised 4 February 2006 ,Accepted 5 April 2006.

References 

  1. Osler W. On the study of tuberculosis. The Philadelphia Med J 1900;1–5.
  2. Rieder HL. Epidemiologic basis of tuberculosis control. 1st ed. Paris: International Union against Tuberculosis and Lung Disease; 1999;
  3. WHO. The global plan to stop TB 2006–2015. Geneva: The World Health Organization, 2006. Available from http://www.who.int/tb/publications/global_plan_to_stop_tb/en/index.html. (accessed 3 May 2006).
  4. van Soolingen D, Borgdorff MW, de Haas PE, Sebek MM, Veen J, Dessens M, et al. Molecular epidemiology of tuberculosis in the Netherlands: a nationwide study from 1993 through 1997. J Infect Dis. 1999;180:726–736
  5. Committee on Migration, Refugees and Population, Parliamentary Assembly Council of Europe. Migration and integration: a challenge and an opportunity for Europe. Document 10453. February 2005. Available from url: http://assembly.coe.int/Documents/WorkingDocs/Doc05/EDOC10453.htm (accessed 3 May 2006).
  6. Diel R, Meywald-Walter K, Gottschalk R, Rusch-Gerdes S, Niemann S. Ongoing outbreak of tuberculosis in a low-incidence community: a molecular-epidemiological evaluation. Int J Tuberc Lung Dis. 2004;8:855–861
  7. Nguyen D, Proulx J- F, Westley J, Thibert L, Dery S, Behr MA. Tuberculosis in the nuit Community of Quebec, Canada. Am J Respir Crit Care Med. 2003;168:1353–1357
  8. Lutz W, O’Neill BC, Scherbov S. Europe's population at a turning point. Science. 2003;299:1991–1993
  9. Robinson WC. Terms of refuge: the Indochinese exodus and the international response. London: Zed Books; 1998;
  10. Vitkovskaya G. Post-Soviet migrations, the Geneva process, and civil society in Russia. Briefing Paper. Migration and Citizenship Program, volume 2, issue 08. Moscow: Carneigie Endowment for Inernational Peace, 2000, Available from http://www.carnegie.ru/en/pubs/briefings/48351.htm (accessed 3 May 2006).
  11. Castles S, Davidson A. Citizenship and migration: globalization and the politics of belonging. New York: Routledge; 2000;
  12. Public Health Agency of Canada. Tuberculosis in Canada 2002. Ottawa, 2004. Available from URL; http://www.phac-aspc.gc.ca/publicat/tbcan02/pdf/tbcan_2002_e.pdf (accessed 3 May 2006).
  13. CDC. Reported tuberculosis in the United States, 2004. Atlanta, GA: US Department of Health and Human Services, CDC; September 2005. Available from: http://www.cdc.gov/nchstp/tb/surv/surv2004/default.htm (accessed 3 May 2006)
  14. UK Health Protection Agency. Pulmonary and non-pulmonary notifications, England and Wales, 1982–2003. Available from htttp://www.hpa.org.uk/infections/topics_az/tb/epidemiology/figures/figure1.htm.
  15. Chemtob D, Leventhal A, Berlowitz Y, Weiler-Ravell D. The new National Tuberculosis Control Programme in Israel, a country of high immigration. Int J Tuberc Lung Dis. 2003;7:828–836
  16. Li J, Roche P, Spencer J, Bastian I, Christensen A, Hurwitz M, et al. National Tuberculosis Advisory Committee Communicable Disease Network Australia. Tuberculosis Notifications in Australia, 2003. Commun Dis Intell. 2004;28:464–473
  17. Anonymous. Technical instructions for medical examination of aliens in the United States. Atlanta, Georgia: US. Department of Health and Human Services, CDC, June 1991. Available from http://www.cdc.gov/ncidod/dq/technica.htm (accessed 3 May 2006).
  18. Citizenship and Immigration Canada. Conducting an immigration medical examination. In: Designated medical practitioner handbook, section 6. Available from http://www.cic.gc.ca/english/pub/dmp%2Dhandbook/index.html (accessed 3 May 2006).
  19. Australian Government. Department of Immigration and Multicultural and Indigenous Affairs. General visa issues. Health examination—frequently asked questions. Available from http://www.immi.gov.au/faq/general/general03.htm (accessed 3 May 2006).
  20. Moreno B. Encyclopaedia of Ellis Island. Connecticut: Greenwood Press; 2004;
  21. Binkin N, Zuber P, Wells C, Tipple M, Castro K. Overseas screening for tuberculosis in immigrants and refugees to the United States: current status. Clin Infect Dis. 1996;26:1226–1232
  22. Tala E, Liippo K. Still screening for pulmonary tuberculosis?. Eur Respir J. 1989;2:397–398
  23. Gordin FM, Slutkin G, Schecter G, Goodman PC, Hopewell PC. Presumptive diagnosis and treatment of pulmonary tuberculosis based on radiographic findings. Am Rev Respir Dis. 1989;139:1090–1093
  24. Rieder HL, Zellweger JP, Raviglione MC, Keizer ST, Miglori GB. Tuberculosis control in Europe and international migration. Eur Respir J. 1994;7:1545–1553
  25. Underwood BR, White VL, Baker T, Law M, Moore-Gillon JC. Contact tracing and population screening for tuberculosis: who should be assessed?. J Public Health Med. 2003;25:59–61
  26. Mandalakas A, Starke JR. Tuberculosis screening in immigrant children. Pediatr Infect Dis J. 2004;23:71–72
  27. Lewinsohn DA, Gennaro ML, Scholvinck L, Lewinsohn DM. Tuberculosis immunology in children: diagnostic and therapeutic challenges and opportunities. Int J Tuberc Lung Dis. 2004;8:658–674
  28. Phillips L, Carlile J, Smith D. Epidemiology of a tuberculosis outbreak in a rural Missouri high school. Pediatrics. 2004;113:514–519
  29. Feja K, Saiman L. Tuberculosis in children. Clin Chest Med. 2005;26:295–312
  30. World Health Organization. Global tuberculosis control: surveillance, planning, and financing. WHO Report 2005. WHO/HTM/TB/2005. Available from http://www.who.int/tb/publications/global_report/2005/en/ (accessed 3 May 2006).
  31. Recommendations for Prevention and Control of Tuberculosis Among Foreign-Born Persons Report of the Working Group on Tuberculosis Among Foreign-Born Persons. MMWR 1998; 47(RR16);1-26. Available from http://wonder.cdc.gov/wonder/prevguid/m0054855/m0054855.asp (accessed 3 May 2006).
  32. Lillebaek T, Andersen AB, Dirksen A, Smith E, Skovgaard LT, Kok-Jensen A. Persistent high incidence of tuberculosis in immigrants in a low-incidence country. Emerg Infect Dis. 2002;8:679–684
  33. Public Health Agency of Canada. Tuberculosis among the foreign-born in Canada. CCDR 2003; 29: January 15, 2003. Available from http://www.phac-aspc.gc.ca/publicat/ccdr-rmtc/03vol29/dr2902eb.html (accessed 3 May 2006).
  34. Li J, et al. Tuberculosis notifications in Australia, 2003. Commun Dis Intell. 2004;28:464–473
  35. Public Health Agency of Canada. Tuberculosis prevention and control. Surveillance Reports. Available from http://www.phac-aspc.gc.ca/tbpc-latb/surv_e.html (accessed 3 May 2006).
  36. Farah MG, Meyer HE, Selmer R, Heldal E, Bjune G. Long-term risk of tuberculosis among immigrants in Norway. Int J Epidemiol. 2005;34:1005–1011
  37. Borgdorff MW, van der Werf MJ, de Haas PE, Kremer K, van Soolingen D. Tuberculosis elimination in the Netherlands. Emerg Infect Dis. 2005;11:597–602
  38. CDC. Reported tuberculosis in the United States, 2002. Atlanta, GA: US Department of Health and Human Services, CDC; September 2003.
  39. Tuberculosis Section. Health Protection Agency Centre for Infections. London. Annual report on tuberculosis cases reported in England, Wales and Northern Ireland in 2003. December 2005. Available from http://www.hpa.org.uk/infections/topics_az/tb/menu.htm (accessed 3 May 2006).
  40. Rieder HL, Zellweger JP, Raviglione MC, Keizer ST, Miglori GB. Tuberculosis control in Europe and international migration. Eur Respir J. 1994;7:1545–1553
  41. Brassard P, Steensma C, Cadieux L, Lands LC. Evaluation of a school-based tuberculosis-screening program and associate investigation targeting recently immigrated children in a low-burden country. Pediatrics. 2006;117:148–156
  42. Breuss E, Helbling P, Altpeter E, Zellweger JP. Screening and treatment for latent tuberculosis infection among asylum seekers entering Switzerland. Swiss Med Wkly. 2002;132:197–200
  43. Carvalho AC, Saleri N, El-Hamad I, Tedoldi S, Capone S, Pezzoli MC, et al. Completion of screening for latent tuberculosis infection among immigrants. Epidemiol Infect. 2005;133:179–185
  44. Marks GB, Bai J, Stewart GJ, Simpson SE, Sullivan EA. Effectiveness of post-migration screening in controlling tuberculosis among refugees: a historical cohort study, 1984–1998. Am J Public Health. 2001;91:1797–1799
  45. Sterling TR, Thompson D, Stanley RL, McElroy PD, Madison A, Moore K, et al. A multi-state outbreak of tuberculosis among members of a highly mobile social network: implications for tuberculosis elimination. Int J Tuberc Lung Dis. 2000;4:1066–1073
  46. Diel R, Meywald-Walter K, Gottschalk R, Rusch-Gerdes S, Niemann S. Ongoing outbreak of tuberculosis in a low-incidence community: a molecular-epidemiological evaluation. Int J Tuberc Lung Dis. 2004;8:855–861
  47. Lemaitre N, Sougakoff W, Truffot-Pernot C, Cambau E, Derenne JP, Bricaire F, et al. Use of DNA fingerprinting for primary surveillance of nosocomial tuberculosis in a large urban hospital: detection of outbreaks in homeless people and migrant workers. Int J Tuberc Lung Dis. 1998;2:390–396
  48. Tomes N. The making of a germ panic, then and now. Am J Public Health. 2000;90:191–198
  49. CDC. Trends in tuberculosis: USA 2004. MMWR 2005;54:245–49. Available from http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5410a2.htm (accessed 3 May 2006).
  50. Heath T, Roberts C, Winks M, Capon A. The epidemiology of tuberculosis in New South Wales 1975–1995: the effects of immigration in a low prevalence population. Int J Tuberc Lung Dis. 1998;2:647–654
  51. Walker D, Stevens W. The economics of TB control in developing countries. Expert Opin Pharmacother. 2003;4:359–368
  52. Schwartzman K, Oxlade O, Barr RG, Grimard F, Acosta I, Baez J, et al. Domestic returns from investment in the control of tuberculosis in other countries. N Engl J Med. 2005;353:1008–1020
  53. Anonymous. Post-detention completion of tuberculosis treatment for persons deported or released from the custody of the Immigration and Naturalization Service: United States, 2003. MMWR Morb Mortal Wkly Rep. 2003;52:438–441
  54. Mitnick C, Furin J, Henry C, Ross J. Tuberculosis among the foreign born in Massachusetts, 1982–1994: a reflection of social and economic disadvantage. Int J Tuberc Lung Dis. 1998;2:S32–S40
  55. Houston HR, Harada N, Makinodan T. Development of a culturally sensitive educational intervention program to reduce the high incidence of tuberculosis among foreign-born Vietnamese. Ethn Health. 2002;7:255–265
  56. Hayward AC, Darton T, Van-Tam JN, Watson JM, Coker R, Schwoebel V. Epidemiology and control of tuberculosis in Western European cities. Int J Tuberc Lung Dis. 2003;7:751–757
  57. Anoymous. Increase in African immigrants and refugees with tuberculosis: Seattle, King County, Washington, 1998–2001. MMWR. 2002;51:882–883
  58. Espinal MA, Laszlo A, Simonsen L, Boulahbal F, Kim SJ, Reniero A, et al. Global trends in resistance to antituberculosis drugs. N Engl J Med. 2001;344:1294–1303
  59. Willcox PA. Drug resistant tuberculosis: worldwide trends, problems specific to Eastern Europe and other hotspots, and the threat to developing countries. Curr Opin Pulm Med. 2001;7:148–153
  60. Robert J, Trystram D, Truffot-Pernot C, Jarlier V. Multidrug-resistant tuberculosis: eight years of surveillance in France. Eur Respir J. 2003;22:833–837
  61. El Sahly HM, Adams GJ, Soini H, Teeter L, Musser JM, Graviss EA. Epidemiologic differences between United States- and foreign-born tuberculosis patients in-Houston, Texas. J Infect Dis. 2001;183:461–468
  62. Zencovich M, Kennedy K, MacPherson DW, Gushulak BD. Immigration medical screening, migration and human immuno-deficiency virus infection. Int J STD AIDS, in press.
  63. Pieterse S, Ismail S. Nutritional risk factors for older refugees. Disasters. 2003;27:16–36
  64. Kwara A, Flanigan TP, Carter EJ. Highly active antiretroviral therapy (HAART) in adults with tuberculosis: current status. Int J Tuberc Lung Dis. 2005;9:248–257
  65. Sharma SK, Mohan A, Kadhiravan T. HIV-TB co-infection: epidemiology, diagnosis and management. Indian J Med Res. 2005;121:550–567
  66. Lewden C, Sobesky M, Cabie A, Couppie P, Boulard F, Bissuel F, et al. Groupe d’etude “Mortalite 2000”. Causes of death among HIV infected adults in French Guyana and the French West Indies in the era of highly active antiretroviral therapy (HAART). Med Mal Infect. 2004;34:286–292[in French]
  67. Seyler C, Toure S, Messou E, Bonard D, Gabillard D, Anglaret X. Risk factors for active tuberculosis following antiretroviral treatment initiation in Abidjan. Am J Respir Crit Care Med 2005; [Epub ahead of print] PMID: 15805184.
  68. Limaye S, Quin J, Steele RH. HIV and tuberculosis co-infection in south-western Sydney: experience from a case series. Intern Med J. 2004;34:203–206
  69. Rieder HL, Zellweger JP, Raviglione MC, Keizer ST, Migliori GB. Tuberculosis control in Europe and international migration. Eur Respir J. 1994;7:1545–1553
  70. Coker J, Bell A, Pitman R, Hayward A, Watson J. Screening programmes for tuberculosis in new entrants across Europe. Int J Tuberc Lung Dis. 2004;8:1022–1026
  71. Johnsen NL, Steen TW, Meyer H, Heldal E, Skarpaas IJ, June GB. Cohort analysis of asylum seekers in Oslo, Norway, 1987–1995: effectiveness of screening at entry and TB incidence in subsequent years. Int J Tuberc Lung Dis. 2005;9:37–42
  72.  Floyd KCosts and effectiveness: the impact of economic studies on TB control. Tuberculosis (Edinb). 2003;83:187–200
  73. Dahle UR, Sandven P, Heldal E, Caugant DA. Continued low rates of transmission of Mycobacterium tuberculosis in Norway. J Clin Microbiol. 2003;41:2968–2973
  74. Department of Health. Stopping tuberculosis in England. An action plan from the Chief Medical Officer. London: Department of Health; October 2004.
  75. Callister ME, Barringer J, Thanabalasingam ST, Gair R, Davidson RN. Pulmonary tuberculosis among political asylum seekers screened at Heathrow Airport, London, 1995–9. Thorax. 2002;57:152–156
  76. The Home Office. Controlling our borders. Making migration work for Britain. Five year strategy for asylum and immigration. London: The Home Office; February 2005. Available from http://www.official-documents.co.uk/document/cm64/6472/6472.htm (accessed 3 May 2006).
  77. Coker R. Migration, public health and compulsory screening for TB and HIV. Asylum and Migration Working Paper 1. London: Institute for Public Policy Research; November 2003.
  78. UKVisas. Health screening: general Q&A. December 24, 2005. Available from http://www.ukvisas.gov.uk/servlet/Front?pagename=OpenMarket/Xcelerate/ShowPage&c=Page&cid=1134650060850 (accessed 3 May 2006).
  79. UKVisas. Health (tuberculosis) screening. December 24, 2005. Available from http://www.ukvisas.gov.uk/servlet/Front?pagename=OpenMarket/Xcelerate/ShowPage&c=Page&cid=1006977150250&a=KArticle&aid=1134650068984 (accessed 3 May 2006).
  80. Khan K, Muennig P, Behta M, Pharm D, Zivin JG. Global drug-resistance patterns and the management of latent tuberculosis infection in immigrants to the United States. N Engl J Med. 2002;347:1850–1859
  81. CDC. Controlling tuberculosis in the United States: recommendations from the American Thoracic Society, CDC, and the Infectious Diseases Society of America. MMWR. 2005;54:1–81
  82. Institute of Medicine, Committee on the Elimination of Tuberculosis in the United States. Ending neglect: the elimination of tuberculosis in the United States. Washington, DC: National Academy Press; 2000;
  83. Menzies D. Screening immigrants to Canada for tuberculosis: chest radiography or tuberculin skin testing?. CMAJ. 2003;169:1035–1036
  84. Foundation for Innovative New Diagnostics. Request for applications: novel TB diagnostic methods: point-of-care detection of TB RFA-FIND/TDR-2005-01. Available from http://www.finddiagnostics.org/activities/tb_2005.htm (accessed 3 May 2006).
  85. Rajalahti I, Ruokonen EL, Kotomaki T, Sintonen H, Nieminen MM. Economic evaluation of the use of PCR assay in diagnosing pulmonary TB in a low-incidence area. Eur Respir J. 2004;23:446–451
  86. Albert H. Economic analysis of the diagnosis of smear-negative pulmonary tuberculosis in South Africa: incorporation of a new rapid test, FASTPlaqueTB, into the diagnostic algorithm. Int J Tuberc Lung Dis. 2004;8:240–247
  87. Okuda Y, Maekura R, Hirotani A, Kitada S, Yoshimura K, Hiraga T, et al. Rapid serodiagnosis of active pulmonary Mycobacterium tuberculosis by analysis of results from multiple antigen-specific tests. J Clin Microbiol. 2004;42:1136–1141
  88. Kivihya-Ndugga LE, van Cleeff MR, Githui WA, Nganga LW, Kibuga DK, Odhiambo JA, et al. A comprehensive comparison of Ziehl–Neelsen and fluorescence microscopy for the diagnosis of tuberculosis in a resource-poor urban setting. Int J Tuberc Lung Dis. 2003;7:1163–1171
  89. Wang JY, Lee LN, Chou CS, Huang CY, Wang SK, Lai HC, et al. Performance assessment of a nested-PCR assay (the RAPID BAP-MTB) and the BD ProbeTec ET system for detection of Mycobacterium tuberculosis in clinical specimens. J Clin Microbiol. 2004;42:4599–4603
  90. Harada N, Higuchi K, Sekiya Y, Rothel J, Kitoh T, Mori T. Basic characteristics of a novel diagnostic method (QuantiFERON TB-2G) of latent tuberculosis infection with a use of Mycobacterium tuberculosis-specific antigens, ESAT-6 and CFP-10. Kekkaku. 2004;79:725–735[in Japanese]
  91. Villarino ME, Mazurek GH. Guidelines for using the QuantiFERON®-TB test for diagnosing latent Mycobacterium tuberculosis infection. MMWR. 2003;52:15–18
  92. DG News. FDA Approves QuantiFERON-TB GOLD for detection of immune responses to tuberculosis. Test could replace tuberculin skin test. Valencia, CA: December 3, 2004. Available from http://www.docguide.com/news/content.nsf/news/8525697700573E1885256F5F004F3B6F (accessed 3 May 2006).
  93. Mazurek GH, Jereb J, Lobue P, Iademarco MF, Metchock B, Vernon A. Division of tuberculosis elimination. National Center for HIV, STD, and TB Prevention, Centers for Disease Control and Prevention (CDC). Guidelines for using the QuantiFERON-TB Gold test for detecting Mycobacterium tuberculosis infection, United States. MMWR Recomm Rep. 2005;54:49–55
  94. Horwitz O, Wilbek E, Erickson PA. Epidemiological basis of tuberculosis eradication: longitudinal studies on the risk of tuberculosis in the general population of a low-prevalence area. Bull World Health Organ. 1969;51:95–113
  95. Styblo K. Epidemiology of tuberculosis. Development of bacillary pulmonary tuberculosis capable of transmitting bacilli following infection with M. tuberculosis (the disease ratio). Selected Papers of the Royal Netherlands Tuberculosis Association, vol. 24, 1991. p. 55–66.
  96. Uppaluri A, Naus M, Heywood N, Brunton J, Kerbel D, Wobeser W. Effectiveness of the Immigration Medical Surveillance Program for tuberculosis in Ontario. Can J Public Health. 2002;93:88–91
  97. Ho MJ. Sociocultural aspects of tuberculosis: a literature review and a case study of immigrant tuberculosis. Soc Sci Med. 2004;59:753–762
  98. Coreil J, Lauzardo M, Heurtelou M. Cultural feasibility assessment of tuberculosis prevention among persons of Haitian origin in South Florida. J Immigr Health. 2004;6:63–69
  99. Heywood N, Kawa B, Long R, Njoo H, Panaro L, Wobeser W. Immigration subcommittee of the Canadian Tuberculosis Committee. Guidelines for the investigation and follow-up of individuals under medical surveillance for tuberculosis after arriving in Canada: a summary. CMAJ. 2003;168:1563–1565
  100. Pediatric Tuberculosis Collaborative Group. Targeted tuberculin skin testing and treatment of latent tuberculosis infection in children and adolescents. Pediatrics. 2004;114:1175–1201
  101. Diel R, Rusch-Gerdes S, Niemann S. Molecular epidemiology of tuberculosis among immigrants in Hamburg, Germany. J Clin Microbiol. 2004;42:2952–2960
  102. Euro TB. Surveillance of tuberculosis in Europe. Available from http://www.eurotb.org/ (accessed 3 May 2006).
  103. LoBue PA, Moser KS. Screening of immigrants and refugees for pulmonary tuberculosis in San Diego County, California. Chest. 2004;126:1777–1782
  104. Schwartzman K. Latent tuberculosis infection: old problem, new priorities. CMAJ. 2002;166:759–761
  105. Enarson DA. Tberculosis: 12. Global disease and the role of international collaboration. CMAJ. 2000;162:57–61
  106. Fanning A. The impact of global tuberculosis in Canada: we are our brothers’ keepers. Can J Infect Dis. 1995;6:225–226
  107. Samaan G, Roche P, Spencer J, Bastian I, Christensen A, Hurwitz M, et al. National Tuberculosis Advisory Committee for the Communicable Diseases Network. Tuberculosis notifications in Australia, 2002. Commun Dis Intell. 2003;27:449–458
  108. Heywood N, Kawa B, Long R, Njoo H, Panaro L, Wobeser W. Immigration Subcommittee of the Canadian Tuberculosis Committee. Guidelines for the investigation and follow-up of individuals under medical surveillance for tuberculosis after arriving in Canada: a summary. CMAJ. 2003;168:1563–1565
  109. Chemtob D, Leventhal A, Weiler-Ravell D. Screening and management of tuberculosis in immigrants: the challenge beyond professional competence. Int J Tuberc Lung Dis. 2003;7:959–966
  110. Iademarco MF, Sodt D, Sutherland WM. Evaluation and epidemiological research in tuberculosis control: linking medical care and public health. Mayo Clin Proc. 2004;79:1110–1112
  111. Okeke IN, Edelman R. Dissemination of antibiotic-resistant bacteria across geographic borders Clin Infec Dis 2001;33:364-69.
  112. United Nations. Millennium development goals. Available from http://www.un.org/millenniumgoals/ (accessed 3 May 2006).
  113. Statistics Canada. Canada's ethnocultural portrait: The changing mosaic. Available from url: http://www12.statcan.ca/english/census01/products/analytic/companion/etoimm/canada.cfm#majority_newest_immigrants_working_age (accessed 3 May 2006).

PII: S0033-3506(06)00106-5

doi: 10.1016/j.puhe.2006.05.002

Public Health
Volume 120, Issue 8 , Pages 712-723 , August 2006