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Volume 12, Number 5—May 2006
THEME ISSUE
Tuberculosis Special Section
Research

Beijing/W Genotype Mycobacterium tuberculosis and Drug Resistance

European Concerted Action on New Generation Genetic Markers and Techniques for the Epidemiology and Control of Tuberculosis
Author affiliations: *RIVM, Bilthoven, the Netherlands

Main Article

Table A1

Included studies on Beijing/W genotype Mycobacterium tuberculosis and drug resistance*

Country Period Source Type of TB No previous TB % Typing method Reference†
Western Europe
Austria: western 1993–2004 Laboratory receiving from nearly all hospitals in area Pulm/Extra ? Spoligo on all
Denmark: entire 1992–2001 Central laboratory for entire country Pulm/Extra 97 RFLP, spoligo (37)
Finland: entire 2000–2002 Central laboratory for entire country Pulm/Extra ? RFLP, spoligo (38)
France
Paris area 1995 All patients from 10 hospitals Pulm/Extra 88 RFLP, spoligo (39)
Paris 2001–2003 Patients at 1 hospital Pulm/Extra ? Spoligo on all
Lyon 2003 Central laboratory for area Pulm/Extra 77 Spoligo on all
Germany: Hamburg 2001 Notified patients in area ? 99 RFLP, spoligo (40)
Italy
Verona 1996–1997 Reference laboratory for area Pulm/Extra ? Spoligo on all (41)
Sardinia 1997–1998 Patients at 1 hospital Pulm/Extra 73 RFLP, spoligo
Tuscany 2002 All patients in area Pulm/Extra 83 RFLP, spoligo (42)
Netherlands: entire 1993–2002 All patients in area Pulm/Extra 96 RFLP, spoligo (43)
Spain
Elche 1993–1999 Sample of patients in area Pulm/Extra 90 RFLP, spoligo (44)
Madrid 1992–2001 All patients in area Pulm/Extra 71 RFLP, spoligo
Zaragoza 1993–1995 All patients in area Pulm/Extra ? RFLP, spoligo (45)
Sweden: western 1999–2002 Laboratory for all patients in area Pulm/Extra 87 Spoligo on all (46)
United Kingdom
Inner London 1993 Laboratories for all patients in area Pulm/Extra 89 Spoligo on all (47)
London 1995–1997 Laboratories for all patients in area Pulm/Extra 88 RFLP (48)
Central and Eastern Europe
Czech Republic: Prague and South Moravia 1998 Laboratories for all patients in areas Pulm/Extra ? Spoligo on all (49)
Estonia: entire 1994 All new pulmonary TB patients in area Pulm 100 RFLP, spoligo (50)
Russia
St. Petersburg 1999–2002 All patients in area with data Pulm/Extra 59 RFLP, spoligo (51,52)
Archangel 1998–1999 All patients at TB clinic Pulm 75 Spoligo on all (53)
North Africa and Middle East
Iran: several areas 1995–1997 All smear-positive patients from Shiraz plus random others Pulm/Extra 79 RFLP, spoligo (54)
Sub-Saharan Africa
Cameroon: western region 1997–1998 All patients from all hospitals in region Pulm 79 Spoligo on all (55,56)
Ethiopia: Addis Ababa 1996 Patients at 1 hospital Pulm 85 RFLP, spoligo (57)
Guinea Bissau: Bissau 1989–1993 All patients in area Pulm 100 RFLP, spoligo (58)
Malawi: Karonga District 1996–2003 All patients in area Pulm/Extra 93 RFLP, spoligo (59)
South Africa: Cape Town 1992–1998 All patients from 2 clinics Pulm/Extra 91 RFLP, spoligo (60)
Sudan: Khartoum 1998–1999 Patients from 2 clinics Pulm 54 Spoligo on all (61)
Zimbabwe: Harare 1997 All patients from 1 hospital Pulm 93 Spoligo on all (62)
North America
United States
New Jersey 1999 All patients in area Pulm/Extra 99 RFLP, spoligo, region A (63)
San Francisco 1998–2000 All patients in area Pulm/Extra 92 RFLP (64)
Caribbean
Cuba
Outside Havana 1994–1995 Isolates sent from regional laboratories Pulm 94 RFLP, spoligo (65)
Havana 1997–1998 Isolates sent to reference laboratory Pulm 86 RFLP (66)
Latin America
Argentina: Buenos Aires 1998–2001 All patients in 1 hospital Pulm/Extra 82 Spoligo on all
Brazil: São Paulo 2000–2002 All patients in area Pulm 72 RFLP
Indian subcontinent
India: Delhi 1995–1996 Patients from 2 male wards + clinic ? 57 RFLP, spoligo (67)
Bangladesh: Mymensingh 2001–2003 Hospitalized patients, 3 hospitals Pulm 1 Spoligo on all (68)
Southeast Asia
Indonesia: Jakarta 1998–1999 All patients from outpatient TB clinic Pulm 75 RFLP,spoligo (69)
Malaysia: entire 1993–1994 Random sample from reference laboratory Pulm/Extra 89 RFLP (70)
Thailand: Bangkok 1998–2000 All patients in single hospital Pulm/Extra Spoligo on all (71)
Vietnam
Hanoi, Ho Chi Minh City 1998–1999 All new smear-positive patients at 2 centers Pulm ? Spoligo on all (72)
Ho Chi Minh City 1998–2000 HIV stratified random sample (1/3 HIV positive) Pulm 100 RFLP, spoligo
Tiet Giang Province 2003 Age stratified sample from laboratory (1/2 patients <40 y) Pulm 93 RFLP, spoligo
East Asia
China
Shanghai and other areas 1994–1995 Random sample from laboratory ? ? Spoligo on all
Henan 2001–2002 All patients in 1 hospital (severe cases) Pulm 87 RFLP
Hong Kong: Hong Kong 1998–1999 Random sample from laboratory ? 100 Spoligo on all (73)
Japan: Okayama 2000–2002 All patients in area with data Pulm/Extra 99 RFLP, spoligo (74)
Mongolia: entire 1998–1999 Random sample of patients in area Pulm 100 Spoligo on all (75)
Taiwan: entire 2002 Random sample from laboratory Pulm/Extra ? Spoligo on all (76)

*TB, tuberculosis; Pulm, pulmonary; extra, extrapulmonary; spoligo, spoligotyping; RFLP, restriction fragment length polymorphism, IS6110 fingerprinting; region A, characteristic insertion in region A.
†The references given describe the studies from which the data came. In many cases, the analysis of Beijing strains has been carried out specifically for this collaborative study. The key contacts who contributed the data are listed as follows: Austria: Wolfgang Prodinger (Medizinische Universität Innsbruck); Denmark: Troels Lillebaek (Statens Serum Institut, Copenhagen); Finland: Hanna Soini, Petri Ruutu, (National Public Health Institute, Helsinki); France: Cristina Gutierrez, Veronique Vincent (Institut Pasteur, Paris); Beate Heym, Veronique Friocourt (Hôpital Ambroise Paré, Boulogne-Billancourt); Isabelle Fredenucci, Jean-Pierre Flandrois (Centre Hospitalier Lyon-Sud, Lyon); Germany: Stefan Niemann (National Reference Centre for Mycobacteria, Forschungszentrum Borstel, Hamburg), Roland Diel (School of Public Health, University of Düsseldorf); Italy: Stefano Bonora (Università di Verona); Leonardo A Sechi, Stephania Zanetti (Università di Sassari); Carlo Garzelli (Università di Pisa); the Netherlands: Martien Borgdorff (KNCV Tuberculosis Foundation) Petra de Haas, Kristin Kremer, Dick van Soolingen (RIVM); Spain: Montserrat Ruiz, Juan Carlos Rodríguez, Gloria Royo (Universidad Miguel Hernández, Elche); Ana Pérez Meixeira, Jenaro Astray (Public Health Institute Getafe, Madrid), Juana Cacho, Amador Ramos (Hospital Universitario de Getafe); Maria Jose Iglesias (University of Zaragoza), Sofia Samper (Hospital Universitario Miguel Servet, Zaragoza); United Kingdom: Andrew Hayward, John Watson, Francis Drobniewski (Health Protection Agency, London); Jeremy Dale (University of Surrey) on behalf of the Steering Committee, Molecular Epidemiology of Tuberculosis in London; Sweden: Malin Ridell, Liselott Svensson (Institute of Medical Microbiology and Immunology, Göteborg University); Czech Republic: Milan Kubin (Institute of Hygiene of the City of Prague); Estonia: Annika Krüüner (Tartu University, Estonia, and Karolinska Institute, Stockholm, Sweden); Russia: Olga Toungoussova (University of Oslo, Norway), Dominique Caugant (Norwegian Institute of Public Health, Oslo, Norway), Andrey Mariandyshev (Northern State Medical University, Archangel): Olga Narvaskaya, Igor Mokrousov (St. Petersburg Pasteur Institute), Tatjana Otten, Boris Vyshnevskiy (Research Institute of Phthisiopulmonology, St. Petersburg); Iran: Mehrnoosh Doroudchi (Shiraz University of Medical Sciences); Cameroon: Sara Ngo Niobe-Eyangoh (Centre Pasteur du Cameroun, Yaoundé); Ethiopia: Judith Bruchfeld (Swedish Institute for Infectious Disease Control, Solna); Guinea Bissau: Tuija Koivula, Gunilla Kallenius (Swedish Institute for Infectious Disease Control, Solna); Malawi: Amelia Crampin, Judith Glynn (London School of Hygiene and Tropical Medicine, UK) on behalf of The Karonga Prevention Study (Chilumba, Malawi); South Africa: Madalene Richardson, Paul van Helden, Rob Warren, Nulda Beyers (Stellenbosch University, Cape Town); Sudan: Ghada Sharaf-Eldin (National Health Laboratory, Khartoum); Zimbabwe: Philippa Easterbrook, Shahed Murad, Francis Drobniewski (King’s College London, UK); Cuba: Raul Diaz (Instituto Pedro Kourí, Havana); United States: Barry Kreiswirth (International Center for Public Health, Newark, NJ); Midori Kato-Maeda, Elizabeth Fair, Sebastien Gagneux, Peter Small (Stanford University, Stanford, CA); Argentina: Nora Morcillo (Reference Laboratory of Buenos Aires Tuberculosis Control Program) Angel Cataldi (National Institute of Agricultural Technology); Brazil: Lucilaine Ferrazoli (Instituto Adolfo Lutz, Sao Paulo); India: Kristin Kremer (RIVM), P. Seth (All India Institute of Medical Sciences, New Delhi); Bangladesh: Leen Rigouts, Isdore Chola Shamputa (Institute of Tropical Medicine, Antwerp, Belgium); Indonesia: Reinout van Crevel (University Medical Center Nijmegen, the Netherlands); Malaysia: Jeremy Dale (University of Surrey, Guildford, UK); Thailand: Wolfgang Prodinger (Medizinische Universität Innsbruck, Austria), Porntip Bunyaratevej (Mahidol University, Bangkok); China: James Douglas (University of Hawaii); Li Weimin (Beijing Tuberculosis and Chest Tumor Institution), Kristin Kremer (RIVM); K.M. Kam (Tuberculosis Reference Laboratory, Hong Kong); Japan: Ritsuko Ohata (Okayama Prefectural Institute for Environmental Science and Public Health); Mongolia: N. Naranbat (National Center for Communicable Diseases, Ulaanbaatar); Vietnam: Dang Duc Anh (National Institute of Hygiene and Epidemiology, Hanoi); Mai Huyen, Nguyen Thi Ngoc Lan (Ho Chi Minh City); Taiwan: Ruwen Jou (Center for Disease Control, Taipei).

Main Article

References
  1. Bifani  PJ, Mathema  B, Kurepina  NE, Kreiswirth  BN. Global dissemination of the Mycobacterium tuberculosis W-Beijing family strains. Trends Microbiol. 2002;10:4552. DOIPubMedGoogle Scholar
  2. Glynn  JR, Whiteley  J, Bifani  PJ, Kremer  K, van Soolingen  D. Worldwide occurrence of Beijing/W strains of Mycobacterium tuberculosis: a systematic review. Emerg Infect Dis. 2002;8:8439.PubMedGoogle Scholar
  3. Filliol  I, Driscoll  JR, van Soolingen  D, Kreiswith  BN, Kremer  K, Valetudie  G, Snapshot of moving and expanding clones of Mycobacterium tuberculosis and their global distribution assessed by spoligotyping in an international study. J Clin Microbiol. 2003;41:196370. DOIPubMedGoogle Scholar
  4. Van Soolingen  D, Qian  L, de Haas  PE, Douglas  JT, Traore  H, Portaels  F, Predominance of a single genotype of Mycobacterium tuberculosis in countries of East Asia. J Clin Microbiol. 1995;33:32348.PubMedGoogle Scholar
  5. Rad  ME, Bifani  P, Martin  C, Kremer  K, Samper  S, Rauzier  J, Mutations in putative mutator genes of Mycobacterium tuberculosis strains of the W-Beijing family. Emerg Infect Dis. 2003;9:83845.PubMedGoogle Scholar
  6. Lopez  B, Aguilar  D, Orozco  H, Burger  M, Espitia  C, Ritacco  V, A marked difference in pathogenesis and immune response induced by different Mycobacterium tuberculosis genotypes. Clin Exp Immunol. 2003;133:307. DOIPubMedGoogle Scholar
  7. Kamerbeek  J, Schouls  L, Kolk  A, van Agterveld  M, van Soolingen  D, Kuijper  S, Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol. 1997;35:90714.PubMedGoogle Scholar
  8. van Embden  JDA, Cave  MD, Crawford  JT, Dale  JW, Eisenach  KD, Gicquel  B, Strain identification of Mycobacterium tuberculosis by DNA fingerprinting: recommendations for a standardized methodology. J Clin Microbiol. 1993;31:4069.PubMedGoogle Scholar
  9. Kurepina  NE, Sreevatsan  S, Plikaytis  BB, Bifani  PJ, Connell  ND, Donnelly  RJ, Characterization of the phylogenetic distribution and chromosomal insertion sites of five IS6110 elements in Mycobacterium tuberculosis: non-random integration in the dnaA-dnaN region. Tuber Lung Dis. 1998;79:3142. DOIPubMedGoogle Scholar
  10. Kremer  K, Glynn  JR, Lillebaek  T, Niemann  S, Kurepina  NF, Kreiswirth  BN, Definition of the Beijing/W lineage of Mycobacterium tuberculosis on the basis of genetic markers. J Clin Microbiol. 2004;42:40409. DOIPubMedGoogle Scholar
  11. Farnia  P, Mohammadi  F, Masjedi  MR, Varnerot  A, Zarifi  AZ, Tabatabee  J, Evaluation of tuberculosis transmission in Tehran: using RFLP and spoligotyping methods. J Infect. 2004;49:94101. DOIPubMedGoogle Scholar
  12. Qian  L, van Embden  JD, van Der Zanden  AG, Weltevreden  EF, Duanmu  H, Douglas  JT. Retrospective analysis of the Beijing family of Mycobacterium tuberculosis in preserved lung tissues. J Clin Microbiol. 1999;37:4714.PubMedGoogle Scholar
  13. Drobniewski  F, Balabanova  Y, Ruddy  M, Weldon  L, Jeltkova  K, Brown  T, Rifampin- and multidrug-resistant tuberculosis in Russian civilians and prison inmates: dominance of the Beijing strain family. Emerg Infect Dis. 2002;8:13206.PubMedGoogle Scholar
  14. Singh  UB, Suresh  N, Bhanu  NV, Arora  J, Pant  H, Sinha  S, Predominant tuberculosis spoligotypes, Delhi, India. Emerg Infect Dis. 2004;10:113842.PubMedGoogle Scholar
  15. Almeida  D, Rodrigues  C, Ashavaid  TF, Lalvani  A, Udwadia  ZF, Mehta  A. High incidence of the Beijing genotype among multidrug-resistant isolates of Mycobacterium tuberculosis in a tertiary care center in Mumbai, India. Clin Infect Dis. 2005;40:8816. DOIPubMedGoogle Scholar
  16. Bifani  PJ, Mathema  B, Liu  Z, Moghazeh  SL, Shopsin  B, Tempalski  B, Identification of a W variant outbreak of Mycobacterium tuberculosis via population-based molecular epidemiology. JAMA. 1999;282:23217. DOIPubMedGoogle Scholar
  17. Bifani  PJ, Plikaytis  BB, Kapur  V, Stockbauer  K, Pan  X, Lutfey  ML, Origin and interstate spread of a New York City multidrug-resistant Mycobacterium tuberculosis clone family. JAMA. 1996;275:4527. DOIPubMedGoogle Scholar
  18. Moss  AR, Alland  D, Telzak  E, Hewlett  D Jr, Sharp  V, Chiliade  P, A city-wide outbreak of a multiple-drug-resistant strain of Mycobacterium tuberculosis in New York. Int J Tuberc Lung Dis. 1997;1:11521.PubMedGoogle Scholar
  19. Agerton  TB, Valway  SE, Blinkhorn  RJ, Shilkret  KL, Reves  R, Schluter  WW, Spread of strain W, a highly drug-resistant strain of Mycobacterium tuberculosis, across the United States. Clin Infect Dis. 1999;29:8592. DOIPubMedGoogle Scholar
  20. Barnes  PF, Yang  Z, Preston-Martin  S, Pogoda  MJ, Jones  BE, Otaya  M, Patterns of tuberculosis transmission in central Los Angeles. JAMA. 1997;278:115963. DOIPubMedGoogle Scholar
  21. Yang  Z, Barnes  PF, Chaves  F, Eisenach  KD, Weis  SE, Bates  JH, Diversity of DNA fingerprints of Mycobacterium tuberculosis isolates in the United States. J Clin Microbiol. 1998;36:10037.PubMedGoogle Scholar
  22. Soini  H, Pan  X, Amin  A, Graviss  EA, Siddiqui  A, Musser  JM. Characterization of Mycobacterium tuberculosis isolates from patients in Houston, Texas, by spoligotyping. J Clin Microbiol. 2000;38:66976.PubMedGoogle Scholar
  23. Cowan  LS, Crawford  JT. Genotype analysis of Mycobacterium tuberculosis isolates from a sentinel surveillance population. Emerg Infect Dis. 2002;8:1294302.PubMedGoogle Scholar
  24. Caminero  JA, Pena  MJ, Campos-Herrero  MI, Rodriguez  JC, Garcia  I, Cabrera  P. al. Epidemiological evidence of the spread of a Mycobacterium tuberculosis strain of the Beijing genotype on Gran Canaria Island. Am J Respir Crit Care Med. 2001;164:116570.PubMedGoogle Scholar
  25. Zhang  M, Gong  J, Yang  Z, Samten  B, Cave  MD, Barnes  PF. Enhanced capacity of a widespread strain of Mycobacterium tuberculosis to grow in human macrophages. J Infect Dis. 1999;179:12137. DOIPubMedGoogle Scholar
  26. Dormans  J, Burger  M, Aguilar  D, Hernandex-Pando  R, Kremer  K, Roholl  P, Correlation of virulence, lung pathology, bacterial load and delayed type hypersensitivity responses after infection with different Mycobacterium tuberculosis genotypes in a BALB/c mouse model. Clin Exp Immunol. 2004;137:4608. DOIPubMedGoogle Scholar
  27. Lan  NT, Lien  HT. Tung le B, Borgdorff MW, Kremer K, van Soolingen D. Mycobacterium tuberculosis Beijing genotype and risk for treatment failure and relapse, Vietnam. Emerg Infect Dis. 2003;9:16335.PubMedGoogle Scholar
  28. van Crevel  R, Nelwan  RHH, de Lenne  W, Veeraragu  Y, van der Aznden  AG, Armin  Z, Mycobacterium tuberculosis Beijing genotype strains associated with febrile response to treatment. Emerg Infect Dis. 2001;7:14. DOIPubMedGoogle Scholar
  29. Borgdorff  MW, van Deutekom  H, de Haas  PE, Kremer  K, van Soolingen  D. Mycobacterium tuberculosis, Beijing genotype strains not associated with radiological presentation of pulmonary tuberculosis. Tuberculosis (Edinb). 2004;84:33740. DOIPubMedGoogle Scholar
  30. Glynn  JR, Crampin  AC, Traore  H, Yates  MD, Mwaungulu  FD, Mgwira  BM, Mycobacterium tuberculosis Beijing genotype, northern Malawi. Emerg Infect Dis. 2005;11:1503.PubMedGoogle Scholar
  31. Pfyffer  GE, Strassle  A, van Gorkom  T, Portaels  F, Rigouts  L, Mathieu  C, Multidrug-resistant tuberculosis in prison inmates, Azerbaijan. Emerg Infect Dis. 2001;7:85561. DOIPubMedGoogle Scholar
  32. Toungoussova  OS, Mariandyshev  A, Bjune  G, Sandven  P, Caugant  DA. Molecular epidemiology and drug resistance of Mycobacterium tuberculosis isolates in the Archangel prison in Russia: predominance of the W-Beijing clone family. Clin Infect Dis. 2003;37:66572. DOIPubMedGoogle Scholar
  33. van Helden  PD, Warren  RM, Victor  TC, van der Spuy  G, Richardson  M, Hoal-van Helden  E. Strain families of Mycobacterium tuberculosis. Trends Microbiol. 2002;10:1678. DOIPubMedGoogle Scholar
  34. Kubica  T, Rusch-Gerdes  S, Niemann  S. The Beijing genotype is emerging among multidrug-resistant Mycobacterium tuberculosis strains from Germany. Int J Tuberc Lung Dis. 2004;8:110713.PubMedGoogle Scholar
  35. Werngren  J, Hoffner  SE. Drug-susceptible Mycobacterium tuberculosis Beijing genotype does not develop mutation-conferred resistance to rifampin at an elevated rate. J Clin Microbiol. 2003;41:15204. DOIPubMedGoogle Scholar
  36. Toungoussova  OS, Caugant  DA, Sandven  P, Mariandyshev  AO, Bjune  G. Impact of drug resistance on fitness of Mycobacterium tuberculosis strains of the W-Beijing genotype. FEMS Immunol Med Microbiol. 2004;42:28190. DOIPubMedGoogle Scholar
  37. Lillebaek  T, Andersen  AB, Dirksen  A, Glynn  JR, Kremer  K. Mycobacterium tuberculosis Beijing genotype. Emerg Infect Dis. 2003;9:15537.PubMedGoogle Scholar
  38. Puustinen  K, Marjamaki  M, Rastogi  N, Sola  C, Filliol  I, Ruutu  P, Characterization of Finnish Mycobacterium tuberculosis isolates by spoligotyping. J Clin Microbiol. 2003;41:15258. DOIPubMedGoogle Scholar
  39. Gutierrez  MC, Vincent  V, Aubert  D, Bizet  J, Gaillot  O, Lebrun  L, Molecular fingerprinting of Mycobacterium tuberculosis and risk factors for tuberculosis transmission in Paris, France, and surrounding area. J Clin Microbiol. 1998;36:48692.PubMedGoogle Scholar
  40. Diel  R, Schneider  S, Meywald-Walter  K, Ruf  CM, Rusch-Gerdes  S, Niemann  S. Epidemiology of tuberculosis in Hamburg, Germany: long-term population-based analysis applying classical and molecular epidemiological techniques. J Clin Microbiol. 2002;40:5329. DOIPubMedGoogle Scholar
  41. Bonora  S, Gutierrez  MC, Di Perri  G, Brunello  F, Allegranzi  B, Ligozzi  M, Comparative evaluation of ligation-mediated PCR and spoligotyping as screening methods for genotyping of Mycobacterium tuberculosis strains. J Clin Microbiol. 1999;37:311823.PubMedGoogle Scholar
  42. Lari  N, Rindi  L, Bonanni  D, Tortoli  E, Garzelli  C. Beijing/W Mycobacterium tuberculosis in Italy. Emerg Infect Dis. 2004;10:9589.PubMedGoogle Scholar
  43. Borgdorff  MW, de Haas  P, Kremer  K, van Soolingen  D. Mycobacterium tuberculosis Beijing genotype, the Netherlands. Emerg Infect Dis. 2003;9:13103.PubMedGoogle Scholar
  44. Ruiz Garcia  M, Rodriguez  JC, Navarro  JF, Samper  S, Martin  C, Royo  G. Molecular epidemiology of tuberculosis in Elche, Spain: a 7-year study. J Med Microbiol. 2002;51:2737.PubMedGoogle Scholar
  45. Samper  S, Iglesias  MJ, Rabanaque  MJ, Lezcano  MA, Vitoria  LA, Rubio  MC, The molecular epidemiology of tuberculosis in Zaragoza, Spain: a retrospective epidemiological study in 1993. Int J Tuberc Lung Dis. 1998;2:2817.PubMedGoogle Scholar
  46. Brudey  K, Gordon  M, Mostrom  P, Svensson  L, Jonsson  B, Sola  C, Molecular epidemiology of Mycobacterium tuberculosis in western Sweden. J Clin Microbiol. 2004;42:304651. DOIPubMedGoogle Scholar
  47. Hayward  AC, Goss  S, Drobniewski  F, Saunders  N, Shaw  RJ, Goyal  M, The molecular epidemiology of tuberculosis in inner London. Epidemiol Infect. 2002;128:17584. DOIPubMedGoogle Scholar
  48. Maguire  H, Dale  JW, McHugh  TD, Butcher  PD, Gillespie  SH, Costetsos  A, Molecular epidemiology of tuberculosis in London 1995–7 showing low rate of active transmission. Thorax. 2002;57:61722. DOIPubMedGoogle Scholar
  49. Kurepina  NE, Kreiswirth  BN, Shaskina  E, Driscoll  JR, Polanecky  V, Kozakova , Molecular epidemiology of tuberculosis in Prague and South Moravia, Czech Republic: genetic analysis of Mycobacterium tuberculosis isolates by IS6110-RFLP fingerprinting and spoligotyping. Cent Eur J Public Health. 2004;12:14150.PubMedGoogle Scholar
  50. Kruuner  A, Hoffner  SE, Sillastu  H, Danilovits  M, Levina  K, Svenson  SB, Spread of drug-resistant pulmonary tuberculosis in Estonia. J Clin Microbiol. 2001;39:333945. DOIPubMedGoogle Scholar
  51. Narvskaya  O, Mokrousov  I, Limeschenko  E, Otten  T, Steklova  L, Graschenkova  O, Molecular characterisation of Mycobacterium tuberculosis strains from the northwest region of Russia. EpiNorth. 2000 [cited 2006 Mar 27]. Available from http://www.epinorth.org/eway/default0.asp?pid=230&oid=0&e=0&trg=MainArea_5260&MainArea_5260=5263:0:15,2930:1:0:0:5260;::0:0:0
  52. Mokrousov  I, Otten  T, Vyshnevskiy  B, Narvskaya  O. Detection of embB306 mutations in ethambutol-susceptible clinical isolates of Mycobacterium tuberculosis from Northwestern Russia: implications for genotypic resistance testing. J Clin Microbiol. 2002;40:38103. DOIPubMedGoogle Scholar
  53. Toungoussova  OS, Sandven  P, Mariandyshev  AO, Nizovtseva  NI, Bjune  G, Caugant  DA. Spread of drug-resistant Mycobacterium tuberculosis strains of the Beijing genotype in the Archangel Oblast, Russia. J Clin Microbiol. 2002;40:19307. DOIPubMedGoogle Scholar
  54. Doroudchi  M, Kremer  K, Basiri  EA, Kadivar  MR, Van Soolingen  D, Ghaderi  AA. IS6110-RFLP and spoligotyping of Mycobacterium tuberculosis isolates in Iran. Scand J Infect Dis. 2000;32:6638. DOIPubMedGoogle Scholar
  55. Niobe-Eyangoh  SN, Kuaban  C, Sorlin  P, Cunin  P, Thonnon  J, Sola  C, Genetic biodiversity of Mycobacterium tuberculosis complex strains from patients with pulmonary tuberculosis in Cameroon. J Clin Microbiol. 2003;41:254753. DOIPubMedGoogle Scholar
  56. Kuaban  C, Bercion  R, Noeske  J, Cunin  P, Nkamsse  P, Ngo Niobe  S. Anti-tuberculosis drug resistance in the West Province of Cameroon. Int J Tuberc Lung Dis. 2000;4:35660.PubMedGoogle Scholar
  57. Bruchfeld  J, Aderaye  G, Palme  IB, Bjorvatn  B, Ghebremichael  S, Hoffner  S, Molecular epidemiology and drug resistance of Mycobacterium tuberculosis isolates from Ethiopian pulmonary tuberculosis patients with and without human immunodeficiency virus infection. J Clin Microbiol. 2002;40:163643. DOIPubMedGoogle Scholar
  58. Kallenius  G, Koivula  T, Ghebremichael  S, Hoffner  SE, Norberg  R, Svensson  E, Evolution and clonal traits of Mycobacterium tuberculosis complex in Guinea-Bissau. J Clin Microbiol. 1999;37:38728.PubMedGoogle Scholar
  59. Glynn  JR, Crampin  AC, Traore  H, Yates  MD, Mwaungulu  F, Ngwira  B, Mycobacterium tuberculosis Beijing genotype, northern Malawi. Emerg Infect Dis. 2005;11:1503.PubMedGoogle Scholar
  60. van Rie  A, Warren  RM, Beyers  N, Gie  RP, Classen  CN, Richardson  M, Transmission of a multidrug-resistant Mycobacterium tuberculosis strain resembling "strain W" among noninstitutionalized, human immunodeficiency virus-seronegative patients. J Infect Dis. 1999;180:160815. DOIPubMedGoogle Scholar
  61. Sharaf-Eldin  GS, Saeed  NS, Hamid  ME, Jordaan  AM, Van der Spuy  GD, Warren  RM, Molecular analysis of clinical isolates of Mycobacterium tuberculosis collected from patients with persistent disease in the Khartoum region of Sudan. J Infect. 2002;44:24451. DOIPubMedGoogle Scholar
  62. Easterbrook  PJ, Gibson  A, Murad  S, Lamprecht  D, Ives  N, Ferguson  A, High rates of clustering of tuberculosis strains in Harare, Zimbabwe: a molecular epidemiological study. J Clin Microbiol. 2004;42:453644. DOIPubMedGoogle Scholar
  63. Bifani  PJ, Mathema  B, Liu  Z, Moghazeh  S, Shopsin  B, Tempalski  B, Identification of a W variant outbreak of Mycobacterium tuberculosis via population-based molecular epidemiology. JAMA. 1999;282:23217. DOIPubMedGoogle Scholar
  64. Jasmer  RM, Hahn  JA, Small  PM, Daley  CL, Behr  MA, Moss  AR, A molecular epidemiologic analysis of tuberculosis trends in San Francisco, 1991-1997. Ann Intern Med. 1999;130:9718.PubMedGoogle Scholar
  65. Diaz  R, Kremer  K, de Haas  PE, Gomez  RI, Marrero  A, Valdivia  JA, Molecular epidemiology of tuberculosis in Cuba outside of Havana, July 1994-June 1995: utility of spoligotyping versus IS6110 restriction fragment length polymorphism. Int J Tuberc Lung Dis. 1998;2:74350.PubMedGoogle Scholar
  66. Diaz  R, Gomez  R, Restrepo  E, Rumbaut  R, Sevy-Court  J, Valdivia  JA, Transmission of tuberculosis in Havana, Cuba: a molecular epidemiological study by IS6110 restriction fragment length polymorphism typing. Mem Inst Oswaldo Cruz. 2001;96:43743. DOIPubMedGoogle Scholar
  67. Bhanu  NV, van Soolingen  D, van Embden  JD, Dar  L, Pandey  RM, Seth  P. Predominace of a novel Mycobacterium tuberculosis genotype in the Delhi region of India. Tuberculosis (Edinb). 2002;82:10512. DOIPubMedGoogle Scholar
  68. Shamputa  IC, Rigouts  L, Eyongeta  LA, El Aila  NA, Van Deun  A, Salim  AH, Genotypic and phenotypic heterogeneity among single M tuberculosis isolates from pulmonary tuberculosis patients. J Clin Microbiol. 2004;42:552836. DOIPubMedGoogle Scholar
  69. van Crevel  R, Nelwan  RHH, de Lenne  W, Veeraragu  Y, van der Zanden  AG, Amin  Z, Mycobacterium tuberculosis Beijing genotype strains associated with febrile response to treatment. Emerg Infect Dis. 2001;7:8803. DOIPubMedGoogle Scholar
  70. Dale  JW, Nor  RM, Ramayah  S, Tang  TH, Zainuddin  ZF. Molecular epidemiology of tuberculosis in Malaysia. J Clin Microbiol. 1999;37:12658.PubMedGoogle Scholar
  71. Prodinger  WM, Bunyaratvej  P, Prachaktam  R, Pavlic  M. Mycobacterium tuberculosis isolates of Beijing genotype in Thailand. Emerg Infect Dis. 2001;7:4834.PubMedGoogle Scholar
  72. Anh  DD, Borgdorff  M, Van  LN, Lan  NTN, van Gorkom  T, Kremer  K, Mycobacterium tuberculosis Beijing genotype emerging in Vietnam. Emerg Infect Dis. 2000;6:3025. DOIPubMedGoogle Scholar
  73. Chan  MY, Borgdorff  M, Yip  CW, de Haas  PE, Wong  WS, Kam  KM, Seventy percent of the Mycobacterium tuberculosis isolates in Hong Kong represent the Beijing genotype. Epidemiol Infect. 2001;127:16971. DOIPubMedGoogle Scholar
  74. Ohata  R, Tada  A. IS6110 restriction fragment length polymorphism analysis of Mycobacterium tuberculosis isolated in Okayama Prefecture [in Japanese]. Kekkaku. 2002;77:62937.PubMedGoogle Scholar
  75. Naranbat  N, Kremer  K, Nymadawa  P, Van Soolingen  D. Abstract 101: Distribution the Beijing genotype of Mycobacterium strains isolated in Mongolia. In: 22nd International Union Against Tuberculosis and Lung Disease Eastern Region Conference, Kathmandu, Nepal, 2003 Sept 23–25. Abstract 101.
  76. Jou  R, Chiang  C-Y, Huang  W-L. Distribution of the Bejing family genotypes of Mycobacterium tuberculosis in Taiwan. J Clin Microbiol. 2005;43:95100. DOIPubMedGoogle Scholar

Main Article

1Analysis and writing committee: Judith R. Glynn, London School of Hygiene and Tropical Medicine, London, UK; Kristin Kremer, RIVM, Bilthoven, the Netherlands; Martien W. Borgdorff, Royal Netherlands Tuberculosis Association (KNCV) Tuberculosis Foundation, The Hague, the Netherlands; Mar Pujades Rodriguez, London School of Hygiene and Tropical Medicine, London, UK; and Dick van Soolingen, RIVM, Bilthoven, the Netherlands.

2The key contacts who contributed the data are listed as follows: Austria: Wolfgang Prodinger (Medizinische Universität Innsbruck); Denmark: Troels Lillebaek (Statens Serum Institut, Copenhagen); Finland: Hanna Soini, Petri Ruutu, (National Public Health Institute, Helsinki); France: Cristina Gutierrez, Veronique Vincent (Institut Pasteur, Paris); Beate Heym, Veronique Friocourt (Hôpital Ambroise Paré, Boulogne-Billancourt); Isabelle Fredenucci, Jean-Pierre Flandrois (Centre Hospitalier Lyon-Sud, Lyon); Germany: Stefan Niemann (National Reference Centre for Mycobacteria, Forschungszentrum Borstel, Hamburg), Roland Diel (School of Public Health, University of Düsseldorf); Italy: Stefano Bonora (Università di Verona); Leonardo A Sechi, Stephania Zanetti (Università di Sassari); Carlo Garzelli (Università di Pisa); the Netherlands: Martien Borgdorff (KNCV Tuberculosis Foundation) Petra de Haas, Kristin Kremer, Dick van Soolingen (RIVM); Spain: Montserrat Ruiz, Juan Carlos Rodríguez, Gloria Royo (Universidad Miguel Hernández, Elche); Ana Pérez Meixeira, Jenaro Astray (Public Health Institute Getafe, Madrid), Juana Cacho, Amador Ramos (Hospital Universitario de Getafe); Maria Jose Iglesias (University of Zaragoza), Sofia Samper (Hospital Universitario Miguel Servet, Zaragoza); United Kingdom: Andrew Hayward, John Watson, Francis Drobniewski (Health Protection Agency, London); Jeremy Dale (University of Surrey) on behalf of the Steering Committee, Molecular Epidemiology of Tuberculosis in London; Sweden: Malin Ridell, Liselott Svensson (Institute of Medical Microbiology and Immunology, Göteborg University); Czech Republic: Milan Kubin (Institute of Hygiene of the City of Prague); Estonia: Annika Krüüner (Tartu University, Estonia, and Karolinska Institute, Stockholm, Sweden); Russia: Olga Toungoussova (University of Oslo, Norway), Dominique Caugant (Norwegian Institute of Public Health, Oslo, Norway), Andrey Mariandyshev (Northern State Medical University, Archangel): Olga Narvaskaya, Igor Mokrousov (St. Petersburg Pasteur Institute), Tatjana Otten, Boris Vyshnevskiy (Research Institute of Phthisiopulmonology, St. Petersburg); Iran: Mehrnoosh Doroudchi (Shiraz University of Medical Sciences); Cameroon: Sara Ngo Niobe-Eyangoh (Centre Pasteur du Cameroun, Yaoundé); Ethiopia: Judith Bruchfeld (Swedish Institute for Infectious Disease Control, Solna); Guinea Bissau: Tuija Koivula, Gunilla Kallenius (Swedish Institute for Infectious Disease Control, Solna); Malawi: Amelia Crampin, Judith Glynn (London School of Hygiene and Tropical Medicine, UK) on behalf of The Karonga Prevention Study (Chilumba, Malawi); South Africa: Madalene Richardson, Paul van Helden, Rob Warren, Nulda Beyers (Stellenbosch University, Cape Town); Sudan: Ghada Sharaf-Eldin (National Health Laboratory, Khartoum); Zimbabwe: Philippa Easterbrook, Shahed Murad, Francis Drobniewski (King’s College London, UK); Cuba: Raul Diaz (Instituto Pedro Kourí, Havana); United States: Barry Kreiswirth (International Center for Public Health, Newark, NJ); Midori Kato-Maeda, Elizabeth Fair, Sebastien Gagneux, Peter Small (Stanford University, Stanford, CA); Argentina: Nora Morcillo (Reference Laboratory of Buenos Aires Tuberculosis Control Program) Angel Cataldi (National Institute of Agricultural Technology); Brazil: Lucilaine Ferrazoli (Instituto Adolfo Lutz, Sao Paulo); India: Kristin Kremer (RIVM), P. Seth (All India Institute of Medical Sciences, New Delhi); Bangladesh: Leen Rigouts, Isdore Chola Shamputa (Institute of Tropical Medicine, Antwerp, Belgium); Indonesia: Reinout van Crevel (University Medical Center Nijmegen, the Netherlands); Malaysia: Jeremy Dale (University of Surrey, Guildford, UK); Thailand: Wolfgang Prodinger (Medizinische Universität Innsbruck, Austria), Porntip Bunyaratevej (Mahidol University, Bangkok); China: James Douglas (University of Hawaii); Li Weimin (Beijing Tuberculosis and Chest Tumor Institution), Kristin Kremer (RIVM); K.M. Kam (Tuberculosis Reference Laboratory, Hong Kong); Japan: Ritsuko Ohata (Okayama Prefectural Institute for Environmental Science and Public Health); Mongolia: N. Naranbat (National Center for Communicable Diseases, Ulaanbaatar); Vietnam: Dang Duc Anh (National Institute of Hygiene and Epidemiology, Hanoi); Mai Huyen, Nguyen Thi Ngoc Lan (Ho Chi Minh City); Taiwan: Ruwen Jou (Center for Disease Control, Taipei).

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