Skip to main content
NCBI home page
Occupational and Environmental Medicine logoLink to Occupational and Environmental Medicine
. 2004 Feb;61(2):96–102. doi: 10.1136/oem.2003.008573

The transmission of tuberculosis in the light of new molecular biological approaches

A Seidler 1, A Nienhaus 1, R Diel 1
PMCID: PMC1740712  PMID: 14739374

Abstract

This review briefly summarises the recent achievements in tuberculosis epidemiology associated with the introduction of molecular methods, and considers the implications of these methods for the understanding of occupational tuberculosis transmission. Special attention is paid to the relative contribution of recently transmitted tuberculosis; risk factors for recent transmission; and the occurrence and frequency of exogenous reinfection. There is a need for occupational epidemiological studies, which should combine the methods of "classical" epidemiology with those of molecular epidemiology.

Full Text

The Full Text of this article is available as a PDF (234.1 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alland D., Kalkut G. E., Moss A. R., McAdam R. A., Hahn J. A., Bosworth W., Drucker E., Bloom B. R. Transmission of tuberculosis in New York City. An analysis by DNA fingerprinting and conventional epidemiologic methods. N Engl J Med. 1994 Jun 16;330(24):1710–1716. doi: 10.1056/NEJM199406163302403. [DOI] [PubMed] [Google Scholar]
  2. Bandera A., Gori A., Catozzi L., Degli Esposti A., Marchetti G., Molteni C., Ferrario G., Codecasa L., Penati V., Matteelli A. Molecular epidemiology study of exogenous reinfection in an area with a low incidence of tuberculosis. J Clin Microbiol. 2001 Jun;39(6):2213–2218. doi: 10.1128/JCM.39.6.2213-2218.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bauer J., Kok-Jensen A., Faurschou P., Thuesen J., Taudorf E., Andersen A. B. A prospective evaluation of the clinical value of nation-wide DNA fingerprinting of tuberculosis isolates in Denmark. Int J Tuberc Lung Dis. 2000 Apr;4(4):295–299. [PubMed] [Google Scholar]
  4. Bauer J., Yang Z., Poulsen S., Andersen A. B. Results from 5 years of nationwide DNA fingerprinting of Mycobacterium tuberculosis complex isolates in a country with a low incidence of M. tuberculosis infection. J Clin Microbiol. 1998 Jan;36(1):305–308. doi: 10.1128/jcm.36.1.305-308.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Behr M. A., Hopewell P. C., Paz E. A., Kawamura L. M., Schecter G. F., Small P. M. Predictive value of contact investigation for identifying recent transmission of Mycobacterium tuberculosis. Am J Respir Crit Care Med. 1998 Aug;158(2):465–469. doi: 10.1164/ajrccm.158.2.9801062. [DOI] [PubMed] [Google Scholar]
  6. Bennett Diane E., Onorato Ida M., Ellis Barbara A., Crawford Jack T., Schable Barbara, Byers Robert, Kammerer J. Steve, Braden Christopher R. DNA fingerprinting of Mycobacterium tuberculosis isolates from epidemiologically linked case pairs. Emerg Infect Dis. 2002 Nov;8(11):1224–1229. doi: 10.3201/eid0811.020420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Borgdorff M. W., Behr M. A., Nagelkerke N. J., Hopewell P. C., Small P. M. Transmission of tuberculosis in San Francisco and its association with immigration and ethnicity. Int J Tuberc Lung Dis. 2000 Apr;4(4):287–294. [PubMed] [Google Scholar]
  8. Borgdorff M. W., Nagelkerke N. J., de Haas P. E., van Soolingen D. Transmission of Mycobacterium tuberculosis depending on the age and sex of source cases. Am J Epidemiol. 2001 Nov 15;154(10):934–943. doi: 10.1093/aje/154.10.934. [DOI] [PubMed] [Google Scholar]
  9. Braden C. R., Templeton G. L., Cave M. D., Valway S., Onorato I. M., Castro K. G., Moers D., Yang Z., Stead W. W., Bates J. H. Interpretation of restriction fragment length polymorphism analysis of Mycobacterium tuberculosis isolates from a state with a large rural population. J Infect Dis. 1997 Jun;175(6):1446–1452. doi: 10.1086/516478. [DOI] [PubMed] [Google Scholar]
  10. Burgos M. V., Pym A. S. Molecular epidemiology of tuberculosis. Eur Respir J Suppl. 2002 Jul;36:54s–65s. doi: 10.1183/09031936.02.00400702. [DOI] [PubMed] [Google Scholar]
  11. Burman W. J., Reves R. R., Hawkes A. P., Rietmeijer C. A., Yang Z., el-Hajj H., Bates J. H., Cave M. D. DNA fingerprinting with two probes decreases clustering of Mycobacterium tuberculosis. Am J Respir Crit Care Med. 1997 Mar;155(3):1140–1146. doi: 10.1164/ajrccm.155.3.9117000. [DOI] [PubMed] [Google Scholar]
  12. Caminero J. A., Pena M. J., Campos-Herrero M. I., Rodríguez J. C., Afonso O., Martin C., Pavón J. M., Torres M. J., Burgos M., Cabrera P. Exogenous reinfection with tuberculosis on a European island with a moderate incidence of disease. Am J Respir Crit Care Med. 2001 Mar;163(3 Pt 1):717–720. doi: 10.1164/ajrccm.163.3.2003070. [DOI] [PubMed] [Google Scholar]
  13. Codecasa L. R., Porretta A. D., Gori A., Franzetti F., Degli Esposti A., Lizioli A., Carreri V., Di Proietto M. C., Perozziello F., Besozzi G. Tuberculosis among immigrants from developing countries in the province of Milan, 1993-1996. Int J Tuberc Lung Dis. 1999 Jul;3(7):589–595. [PubMed] [Google Scholar]
  14. Cronin Wendy A., Golub Jonathan E., Lathan Monica J., Mukasa Leonard N., Hooper Nancy, Razeq Jafar H., Baruch Nancy G., Mulcahy Donna, Benjamin William H., Magder Laurence S. Molecular epidemiology of tuberculosis in a low- to moderate-incidence state: are contact investigations enough? Emerg Infect Dis. 2002 Nov;8(11):1271–1279. doi: 10.3201/eid0811.020261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Diel Roland, Schneider Steffen, Meywald-Walter Karen, Ruf Christa-Maria, Rüsch-Gerdes Sabine, Niemann Stefan. Epidemiology of tuberculosis in Hamburg, Germany: long-term population-based analysis applying classical and molecular epidemiological techniques. J Clin Microbiol. 2002 Feb;40(2):532–539. doi: 10.1128/JCM.40.2.532-539.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dobbs K. G., Lok K. H., Bruce F., Mulcahy D., Benjamin W. H., Dunlap N. E. Value of Mycobacterium tuberculosis fingerprinting as a tool in a rural state surveillance program. Chest. 2001 Dec;120(6):1877–1882. doi: 10.1378/chest.120.6.1877. [DOI] [PubMed] [Google Scholar]
  17. Elizaga Jorge, Carrero Pablo, Iñigo Jesús, Chaves Fernando. Transmisión reciente de la tuberculosis en un área con baja incidencia: estudio epidemiológico y molecular. Med Clin (Barc) 2002 May 11;118(17):645–649. doi: 10.1016/s0025-7753(02)72484-6. [DOI] [PubMed] [Google Scholar]
  18. Ellis Barbara A., Crawford Jack T., Braden Christopher R., McNabb Scott J. N., Moore Marisa, Kammerer Steve, National Tuberculosis Genotyping and Surveillance Network Work Group Molecular epidemiology of tuberculosis in a sentinel surveillance population. Emerg Infect Dis. 2002 Nov;8(11):1197–1209. doi: 10.3201/eid0811.020403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Fernandez de la Hoz K., Iñigo J., Fernandez-Martín J. I., Arce A., Alonso-Sanz M., Gomez-Pintado P., Palenque E., Chaves F. The influence of HIV infection and imprisonment on dissemination of Mycobacterium tuberculosis in a large Spanish city. Int J Tuberc Lung Dis. 2001 Aug;5(8):696–702. [PubMed] [Google Scholar]
  20. Fine P. E., Small P. M. Exogenous reinfection in tuberculosis. N Engl J Med. 1999 Oct 14;341(16):1226–1227. doi: 10.1056/NEJM199910143411609. [DOI] [PubMed] [Google Scholar]
  21. Garzelli C., Lari N., Nguon B., Pistello M., Falcone G. DNA restriction fragments length polymorphism of Mycobacterium tuberculosis isolates in Pisa, Italy. Eur J Epidemiol. 1997 Oct;13(7):845–851. doi: 10.1023/a:1007337319454. [DOI] [PubMed] [Google Scholar]
  22. Genewein A., Telenti A., Bernasconi C., Mordasini C., Weiss S., Maurer A. M., Rieder H. L., Schopfer K., Bodmer T. Molecular approach to identifying route of transmission of tuberculosis in the community. Lancet. 1993 Oct 2;342(8875):841–844. doi: 10.1016/0140-6736(93)92698-s. [DOI] [PubMed] [Google Scholar]
  23. Geng Elvin, Kreiswirth Barry, Driver Cynthia, Li Jiehui, Burzynski Joseph, DellaLatta Phyllis, LaPaz Angel, Schluger Neil W. Changes in the transmission of tuberculosis in New York City from 1990 to 1999. N Engl J Med. 2002 May 9;346(19):1453–1458. doi: 10.1056/NEJMoa012972. [DOI] [PubMed] [Google Scholar]
  24. Glynn J. R., Bauer J., de Boer A. S., Borgdorff M. W., Fine P. E., Godfrey-Faussett P., Vynnycky E. Interpreting DNA fingerprint clusters of Mycobacterium tuberculosis. European Concerted Action on Molecular Epidemiology and Control of Tuberculosis. Int J Tuberc Lung Dis. 1999 Dec;3(12):1055–1060. [PubMed] [Google Scholar]
  25. Glynn J. R., Vynnycky E., Fine P. E. Influence of sampling on estimates of clustering and recent transmission of Mycobacterium tuberculosis derived from DNA fingerprinting techniques. Am J Epidemiol. 1999 Feb 15;149(4):366–371. doi: 10.1093/oxfordjournals.aje.a009822. [DOI] [PubMed] [Google Scholar]
  26. Gutiérrez M. C., Vincent V., Aubert D., Bizet J., Gaillot O., Lebrun L., Le Pendeven C., Le Pennec M. P., Mathieu D., Offredo C. Molecular fingerprinting of Mycobacterium tuberculosis and risk factors for tuberculosis transmission in Paris, France, and surrounding area. J Clin Microbiol. 1998 Feb;36(2):486–492. doi: 10.1128/jcm.36.2.486-492.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Haas W. H. Molekularbiologische Methoden in der Epidemiologie der Tuberkulose. Pneumologie. 1998 May;52(5):271–276. [PubMed] [Google Scholar]
  28. Hayward A. C., Goss S., Drobniewski F., Saunders N., Shaw R. J., Goyal M., Swan A., Uttley A., Pozniak A., Grace-Parker J. The molecular epidemiology of tuberculosis in inner London. Epidemiol Infect. 2002 Apr;128(2):175–184. doi: 10.1017/s0950268801006690. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Heldal E., Döcker H., Caugant D. A., Tverdal A. Pulmonary tuberculosis in Norwegian patients. The role of reactivation, re-infection and primary infection assessed by previous mass screening data and restriction fragment length polymorphism analysis. Int J Tuberc Lung Dis. 2000 Apr;4(4):300–307. [PubMed] [Google Scholar]
  30. Hernández-Garduño Eduardo, Kunimoto Dennis, Wang Lei, Rodrigues Mabel, Elwood R. Kevin, Black William, Mak Sunny, FitzGerald J. Mark. Predictors of clustering of tuberculosis in Greater Vancouver: a molecular epidemiologic study. CMAJ. 2002 Aug 20;167(4):349–352. [PMC free article] [PubMed] [Google Scholar]
  31. Iñigo Martínez J., Chaves Sánchez F., Arce Arnáez A., Alonso Sanz M., Palenque Mataix E., Jaén Herreros F., Martínez Martínez M. T., Gómez García M., Rodríguez Noriega A. Transmisión reciente de la tuberculosis en Madrid: utilidad de las técnicas moleculares. Med Clin (Barc) 2000 Sep 9;115(7):241–245. [PubMed] [Google Scholar]
  32. Kamerbeek J., Schouls L., Kolk A., van Agterveld M., van Soolingen D., Kuijper S., Bunschoten A., Molhuizen H., Shaw R., Goyal M. Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol. 1997 Apr;35(4):907–914. doi: 10.1128/jcm.35.4.907-914.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kulaga S., Behr M. A., Schwartzman K. Genetic fingerprinting in the study of tuberculosis transmission. CMAJ. 1999 Nov 2;161(9):1165–1169. [PMC free article] [PubMed] [Google Scholar]
  34. Kulaga Sophie, Behr Marcel, Musana Kenneth, Brinkman Jacquelyn, Menzies Dick, Brassard Paul, Kunimoto Dennis, Tannenbaum Terry-Nan, Thibert Louise, Joseph Lawrence. Molecular epidemiology of tuberculosis in Montreal. CMAJ. 2002 Aug 20;167(4):353–354. [PMC free article] [PubMed] [Google Scholar]
  35. Lillebaek T., Andersen A. B., Bauer J., Dirksen A., Glismann S., de Haas P., Kok-Jensen A. Risk of Mycobacterium tuberculosis transmission in a low-incidence country due to immigration from high-incidence areas. J Clin Microbiol. 2001 Mar;39(3):855–861. doi: 10.1128/JCM.39.3.855-861.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Magnani J., Mathema B., Berger J., Brown S., David M., Glatt A., Pujol F., Segal-Maurer S., Riley L. W., Kreiswirth B. N. Molecular epidemiology of tuberculosis among eight hospitals in New York City, 1996-1997. Int J Infect Dis. 2001;5(3):126–132. doi: 10.1016/s1201-9712(01)90086-4. [DOI] [PubMed] [Google Scholar]
  37. Maguire H., Dale J. W., McHugh T. D., Butcher P. D., Gillespie S. H., Costetsos A., Al-Ghusein H., Holland R., Dickens A., Marston L. Molecular epidemiology of tuberculosis in London 1995-7 showing low rate of active transmission. Thorax. 2002 Jul;57(7):617–622. doi: 10.1136/thorax.57.7.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Martinez A. N., Rhee J. T., Small P. M., Behr M. A. Sex differences in the epidemiology of tuberculosis in San Francisco. Int J Tuberc Lung Dis. 2000 Jan;4(1):26–31. [PubMed] [Google Scholar]
  39. Mazars E., Lesjean S., Banuls A. L., Gilbert M., Vincent V., Gicquel B., Tibayrenc M., Locht C., Supply P. High-resolution minisatellite-based typing as a portable approach to global analysis of Mycobacterium tuberculosis molecular epidemiology. Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):1901–1906. doi: 10.1073/pnas.98.4.1901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. McConkey Samuel J., Williams Michael, Weiss Don, Adams Hilda, Cave M. Donald, Yang Zhenhua, Lindner Tom, Bailey Thomas C. Prospective use of molecular typing of Mycobacterium tuberculosis by use of restriction fragment-length polymorphism in a public tuberculosis-control program. Clin Infect Dis. 2002 Jan 23;34(5):612–619. doi: 10.1086/338785. [DOI] [PubMed] [Google Scholar]
  41. Moro M. L., Salamina G., Gori A., Penati V., Sacchetti R., Mezzetti F., Infuso A., Sodano L. Two-year population-based molecular epidemiological study of tuberculosis transmission in the metropolitan area of Milan, Italy. Eur J Clin Microbiol Infect Dis. 2002 Feb;21(2):114–122. doi: 10.1007/s10096-001-0664-2. [DOI] [PubMed] [Google Scholar]
  42. Murray Megan, Alland David. Methodological problems in the molecular epidemiology of tuberculosis. Am J Epidemiol. 2002 Mar 15;155(6):565–571. doi: 10.1093/aje/155.6.565. [DOI] [PubMed] [Google Scholar]
  43. Murray Megan, Nardell Edward. Molecular epidemiology of tuberculosis: achievements and challenges to current knowledge. Bull World Health Organ. 2002;80(6):477–482. [PMC free article] [PubMed] [Google Scholar]
  44. Nastasi A., Mammina C. Epidemiological study of tuberculosis in Palermo, Italy: IS6110 fingerprinting of Mycobacterium tuberculosis strains isolated in the years 1994-1998. Infection. 1999 Nov-Dec;27(6):318–322. doi: 10.1007/s150100050036. [DOI] [PubMed] [Google Scholar]
  45. Niemann S., Rüsch-Gerdes S., Richter E. IS6110 fingerprinting of drug-resistant Mycobacterium tuberculosis strains isolated in Germany during 1995. J Clin Microbiol. 1997 Dec;35(12):3015–3020. doi: 10.1128/jcm.35.12.3015-3020.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Niemann S., Rüsch-Gerdes S., Richter E., Thielen H., Heykes-Uden H., Diel R. Stability of IS6110 restriction fragment length polymorphism patterns of Mycobacterium tuberculosis strains in actual chains of transmission. J Clin Microbiol. 2000 Jul;38(7):2563–2567. doi: 10.1128/jcm.38.7.2563-2567.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Pfyffer G. E., Strässle A., Rose N., Wirth R., Brändli O., Shang H. Transmission of tuberculosis in the metropolitan area of Zurich: a 3 year survey based on DNA fingerprinting. Eur Respir J. 1998 Apr;11(4):804–808. doi: 10.1183/09031936.98.11040804. [DOI] [PubMed] [Google Scholar]
  48. Poulet S., Cole S. T. Repeated DNA sequences in mycobacteria. Arch Microbiol. 1995 Feb;163(2):79–86. doi: 10.1007/BF00381780. [DOI] [PubMed] [Google Scholar]
  49. Rhee J. T., Tanaka M. M., Behr M. A., Agasino C. B., Paz E. A., Hopewell P. C., Small P. M. Use of multiple markers in population-based molecular epidemiologic studies of tuberculosis. Int J Tuberc Lung Dis. 2000 Dec;4(12):1111–1119. [PubMed] [Google Scholar]
  50. Safi H., Aznar J., Palomares J. C. Molecular epidemiology of Mycobacterium tuberculosis strains isolated during a 3-year period (1993 to 1995) in Seville, Spain. J Clin Microbiol. 1997 Oct;35(10):2472–2476. doi: 10.1128/jcm.35.10.2472-2476.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Samper S., Iglesias M. J., Rabanaque M. J., Lezcano M. A., Vitoria L. A., Rubio M. C., Gómez-Lus R., Gómez L. I., Otal I., Martín C. The molecular epidemiology of tuberculosis in Zaragoza, Spain: a retrospective epidemiological study in 1993. Int J Tuberc Lung Dis. 1998 Apr;2(4):281–287. [PubMed] [Google Scholar]
  52. Sepkowitz K. A., Friedman C. R., Hafner A., Kwok D., Manoach S., Floris M., Martinez D., Sathianathan K., Brown E., Berger J. J. Tuberculosis among urban health care workers: a study using restriction fragment length polymorphism typing. Clin Infect Dis. 1995 Nov;21(5):1098–1101. doi: 10.1093/clinids/21.5.1098. [DOI] [PubMed] [Google Scholar]
  53. Sharnprapai Sharon, Miller Ann C., Suruki Robert, Corkren Edward, Etkind Sue, Driscoll Jeffrey, McGarry Michael, Nardell Edward. Genotyping analyses of tuberculosis cases in U.S.- and foreign-born Massachusetts residents. Emerg Infect Dis. 2002 Nov;8(11):1239–1245. doi: 10.3201/eid0811.020370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Small P. M., Hopewell P. C., Singh S. P., Paz A., Parsonnet J., Ruston D. C., Schecter G. F., Daley C. L., Schoolnik G. K. The epidemiology of tuberculosis in San Francisco. A population-based study using conventional and molecular methods. N Engl J Med. 1994 Jun 16;330(24):1703–1709. doi: 10.1056/NEJM199406163302402. [DOI] [PubMed] [Google Scholar]
  55. Sudre P., Pfyffer G. E., Bodmer T., Prod'hom G., Furrer H., Bassetti S., Bernasconi E., Matter L., Telenti A., Strässle A. Molecular epidemiology of tuberculosis among HIV-infected persons in Switzerland: a countrywide 9-year cohort study. Swiss HIV Cohort Study. Infection. 1999 Nov-Dec;27(6):323–330. doi: 10.1007/s150100050037. [DOI] [PubMed] [Google Scholar]
  56. Suffys P. N., de Araujo M. E., Degrave W. M. The changing face of the epidemiology of tuberculosis due to molecular strain typing--a review. Mem Inst Oswaldo Cruz. 1997 May-Jun;92(3):297–316. doi: 10.1590/s0074-02761997000300001. [DOI] [PubMed] [Google Scholar]
  57. Tornieporth N. G., Ptachewich Y., Poltoratskaia N., Ravi B. S., Katapadi M., Berger J. J., Dahdouh M., Segal-Maurer S., Glatt A., Adamis R. Tuberculosis among foreign-born persons in New York City, 1992-1994: implications for tuberculosis control. Int J Tuberc Lung Dis. 1997 Dec;1(6):528–535. [PubMed] [Google Scholar]
  58. Vachée A., Vincent P., Savage C., Caillaux M., Pithoud L., Changeon C., Vérité E., De Decker L., Simonet M. Molecular epidemiology of tuberculosis in the Nord Department of France during 1995. Tuber Lung Dis. 1999;79(6):361–366. doi: 10.1054/tuld.1999.0224. [DOI] [PubMed] [Google Scholar]
  59. Van Soolingen D. Molecular epidemiology of tuberculosis and other mycobacterial infections: main methodologies and achievements. J Intern Med. 2001 Jan;249(1):1–26. doi: 10.1046/j.1365-2796.2001.00772.x. [DOI] [PubMed] [Google Scholar]
  60. Vynnycky E., Nagelkerke N., Borgdorff M. W., van Soolingen D., van Embden J. D., Fine P. E. The effect of age and study duration on the relationship between 'clustering' of DNA fingerprint patterns and the proportion of tuberculosis disease attributable to recent transmission. Epidemiol Infect. 2001 Feb;126(1):43–62. [PMC free article] [PubMed] [Google Scholar]
  61. Warren R. M., van der Spuy G. D., Richardson M., Beyers N., Borgdorff M. W., Behr M. A., van Helden P. D. Calculation of the stability of the IS6110 banding pattern in patients with persistent Mycobacterium tuberculosis disease. J Clin Microbiol. 2002 May;40(5):1705–1708. doi: 10.1128/JCM.40.5.1705-1708.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Yang Z. H., de Haas P. E., Wachmann C. H., van Soolingen D., van Embden J. D., Andersen A. B. Molecular epidemiology of tuberculosis in Denmark in 1992. J Clin Microbiol. 1995 Aug;33(8):2077–2081. doi: 10.1128/jcm.33.8.2077-2081.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Yeh R. W., Ponce de Leon A., Agasino C. B., Hahn J. A., Daley C. L., Hopewell P. C., Small P. M. Stability of Mycobacterium tuberculosis DNA genotypes. J Infect Dis. 1998 Apr;177(4):1107–1111. doi: 10.1086/517406. [DOI] [PubMed] [Google Scholar]
  64. de Boer A. S., Borgdorff M. W., Vynnycky E., Sebek M. M., van Soolingen D. Exogenous re-infection as a cause of recurrent tuberculosis in a low-incidence area. Int J Tuberc Lung Dis. 2003 Feb;7(2):145–152. [PubMed] [Google Scholar]
  65. de Boer A. S., Borgdorff M. W., de Haas P. E., Nagelkerke N. J., van Embden J. D., van Soolingen D. Analysis of rate of change of IS6110 RFLP patterns of Mycobacterium tuberculosis based on serial patient isolates. J Infect Dis. 1999 Oct;180(4):1238–1244. doi: 10.1086/314979. [DOI] [PubMed] [Google Scholar]
  66. van Deutekom H., Gerritsen J. J., van Soolingen D., van Ameijden E. J., van Embden J. D., Coutinho R. A. A molecular epidemiological approach to studying the transmission of tuberculosis in Amsterdam. Clin Infect Dis. 1997 Nov;25(5):1071–1077. doi: 10.1086/516072. [DOI] [PubMed] [Google Scholar]
  67. van Embden J. D., Cave M. D., Crawford J. T., Dale J. W., Eisenach K. D., Gicquel B., Hermans P., Martin C., McAdam R., Shinnick T. M. Strain identification of Mycobacterium tuberculosis by DNA fingerprinting: recommendations for a standardized methodology. J Clin Microbiol. 1993 Feb;31(2):406–409. doi: 10.1128/jcm.31.2.406-409.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. van Rie A., Warren R., Richardson M., Victor T. C., Gie R. P., Enarson D. A., Beyers N., van Helden P. D. Exogenous reinfection as a cause of recurrent tuberculosis after curative treatment. N Engl J Med. 1999 Oct 14;341(16):1174–1179. doi: 10.1056/NEJM199910143411602. [DOI] [PubMed] [Google Scholar]
  69. van Soolingen D., Borgdorff M. W., de Haas P. E., Sebek M. M., Veen J., Dessens M., Kremer K., van Embden J. D. Molecular epidemiology of tuberculosis in the Netherlands: a nationwide study from 1993 through 1997. J Infect Dis. 1999 Sep;180(3):726–736. doi: 10.1086/314930. [DOI] [PubMed] [Google Scholar]

Articles from Occupational and Environmental Medicine are provided here courtesy of BMJ Publishing Group

RESOURCES