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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 A3

Drug resistance in Beijing and other genotypes of Mycobacterium tuberculosis among nonimmigrants*†

Study n % resistant to each drug (no.)
Any drug Isoniazid Rifampicin Streptomycin Ethambutol MDR
West Europe
Austria: western
Beijing 7 14.3 (1) 0.0 (0) 14.3 (1) 0.0 (0) 0.0 (0) 0.0 (0)
Other 647 6.7 (43) 2.9 (19) 2.2 (14) 3.9 (25) 0.78 (5) 0.93 (6)
Denmark
Beijing 16 12.5 (2) 12.5 (2) 6.3 (1) 12.5 (2) 6.3 (1) 6.3 (1)
Other 1,623 10.2 (165) 3.1 (50) 0.12 (2)‡ 3.6 (58) 0.0 (0)§ 0.0 (0)§
Finland
Beijing 13 15.4 (2) 7.7 (1) 7.7 (1) 16.7 (2) 0.0 (0) 7.7 (1)
Other 1,102 4.6 (51) 1.5 (17) 0.27 (3)‡ 1.2 (12)§ 0.73 (5) 0.0 (0)‡
The Netherlands
Beijing 199 9.1 (18) 3.5 (7) 0.50 (1) 7.0 (14) 0.50 (1)
Other 3,239 5.8 (189) 3.2 (105) 0.22 (7) 3.9 (125)‡ 0.15 (5)
Western Sweden
Beijing 3 33.3 (1) 33.3 (1) 0.0 (0) 33.3 (1) 0.0 (0) 0.0 (0)
Other 72 5.6 (4) 2.8 (2) 0.0 (0) 1.4 (1) 0.0 (0) 0.0 (0)
United Kingdom
Inner London
Beijing 5 0.0 (0) 0.0 (0) 0.0 (0) 0.0 (0)
Other 145 2.8 (4) 2.1 (3) 0.69 (1) 0.69 (1)
London
Beijing 10 20.0 (2) 20.0 (2) 0.0 (0) 10.0 (1) 0.0 (0) 0.0 (0)
Other 259 11.2 (29) 9.3 (24) 3.5 (9) 4.3 (11) 1.2 (3) 3.5 (9)
Eastern Europe
Estonia
Beijing 61 70.5 (43) 59.0 (36) 34.4 (21) 59.0 (36) 19.7 (12) 34.4 (21)
Other 148 14.2 (21)¶ 8.8 (13)¶ 2.7 (4)¶ 8.1 (12)¶ 1.4 (2)¶ 2.0 (3)¶
Russia
St. Petersburg
Beijing 133 90.2 (120) 74.4 (99) 67.7 (90) 86.5 (115) 12.0 (16) 60.2 (80)
Other 103 74.8 (77)§ 52.4 (54)¶ 47.6 (49)§ 70.9 (73)§ 2.9 (3)§ 42.7 (44)§
Archangel#
Beijing 54 79.6 (43) 64.8 (35) 46.3 (25) 75.9 (41) 44.4 (24) 46.3 (25)
Other 65 36.9 (24)¶ 30.8 (20)¶ 7.7 (5)¶ 23.1 (15)¶ 21.5 (14)§ 7.7 (5)
Sub-Saharan Africa
Malawi**
Beijing 43 0.0 (0) 0.0 (0) 0.0 (0) 0.0 (0) 0.0 (0) 0.0 (0)
Other 964 6.6 (64) 6.2 (60) 0.6 (6) 5.7 (24) 0.47 (2) 0.6 (6)
United States
San Francisco
Beijing 12 8.3 (1) 8.3 (1) 8.3 (1) 8.3 (1) 8.3 (1) 8.3 (1)
Other 96 16.7 (16) 2.1 (2) 3.1 (3) 11.5 (11) 1.0 (1) 0.0 (0)
Caribbean
Cuba
Outside Havana
Beijing 22 50.0 (11) 0.0 (0) 9.1 (2) 50.0 (11) 0.0 (0) 0.0 (0)
Other 136 6.6 (9)¶ 2.9 (4) 1.5 (2) 4.4 (6)¶ 0.7 (1) 1.5 (2)
Havana
Beijing 4 50.0 (2) 0.0 (0) 0.0 (0) 50.0 (2) 0.0 (0) 0.0 (0)
Other 47 4.3 (2)‡ 0.0 (0) 0.0 (0) 4.3 (2)‡ 0.0 (0) 0.0 (0)
Latin America
Argentina: Buenos Aires
Beijing 5 0.0 (0) 0.0 (0) 0.0 (0) 0.0 (0) 0.0 (0) 0.0 (0)
Other 548 29.0 (159) 22.5 (123) 15.0 (82) 18.3 (100) 9.1 (50) 14.6 (80)
Brazil: São Paulo
Beijing 4 50.0 (2)†† 50.0 (2) 50.0 (2) 50.0 (2) 0 (0.0) 50.0 (2)
Other 416 15.1 (63) 9.9 (41) 6.3 (26)‡ 3.4 (14)§ 2.4 (10) 4.8 (20)‡
Indian subcontinent
Bangladesh
Beijing 7 71.4 (5) 71.4 (5) 28.6 (2) 42.9 (3) 28.6 (2) 28.6 (2)
Other 89 20.2 (18)§ 14.6 (13)§ 4.5 (4) 12.4 (11) 1.1 (1)‡ 3.4 (3)‡
Southeast Asia
Indonesia: Jakarta
Beijing 28 35.7 (10) 35.7 (10) 7.1 (2) 14.3 (4) 3.6 (1) 7.1 (2)
Other 53 22.6 (12) 17.0 (9) 3.8 (2) 5.7 (3) 5.7 (3) 3.8 (2)
Malaysia
Beijing 64 6.3 (4) 3.1 (2) 3.1 (2) 4.7 (3) 3.1 (2) 3.1 (2)
Other 322 14.9 (48) 8.7 (28) 3.7 (12) 8.7 (28) 2.2 (7) 3.1 (10)
Thailand: Bangkok
Beijing 98 29.6 (29) 12.2 (12) 7.1 (7) 20.4 (20) 3.1 (3) 4.1 (4)
Other 106 31.1 (33) 5.7 (6) 5.7 (6) 18.9 (20) 6.6 (7) 0.9 (1)
Vietnam
Hanoi#
Beijing 33 60.6 (20) 60.6 (20) 36.4 (12) 39.4 (13) 21.2 (7) 36.4 (12)
Other 20 25.9 (7)§ 22.2 (6)§ 11.1 (3)‡ 7.4 (2)§ 3.7 (1) 7.4 (2)§
Ho Chi Minh 1#
Beijing 81 43.2 (35) 27.2 (22) 6.2 (5) 42.0 (34) 6.2 (5) 6.2 (5)
Other 87 26.4 (23)‡ 19.5 (17) 2.3 (2) 17.2 (15)¶ 2.3 (2) 2.3 (2)
Ho Chi Minh 2
Beijing 34 52.9 (18) 41.2 (14) 5.9 (2) 50.0 (17) 0.0 (0) 5.9 (2)
Other 41 34.2 (14) 22.0 (9) 4.9 (2) 24.4 (10)‡ 0.0 (0) 4.9 (2)
Tien Giang
Beijing 28 53.6 (15) 21.4 (6) 7.1 (2) 53.6 (15) 3.6 (1) 7.1 (2)
Other 32 34.4 (11) 15.6 (5) 0.0 (0) 28.1 (9)‡ 0.0 (0) 0.0 (0)
East Asia
China
Shanghai#
Beijing 25 44.0 (11) 28.0 (7) 16.0 (4) 30.4 (7) 0.0 (0) 16.0 (4)
Other 14 57.1 (8) 35.7 (5) 14.3 (2) 35.7 (5) 21.4 (3)‡ 14.3 (2)
Henan
Beijing 36 33.3 (12) 25.0 (9) 16.7 (6) 27.8 (10) 8.3 (3) 13.9 (5)
Other 16 31.3 (5) 18.9 (3) 6.3 (1) 25.0 (4) 0.0 (0) 6.3 (1)
Hong Kong
Beijing 356 13.5 (48) 5.3 (19) 0.6 (2) 9.3 (33) 1.1 (4) 0.6 (2)
Other 144 18.1 (26) 8.3 (12) 0.7 (1) 13.9 (20) 1.4 (2) 0.7 (1)
Mongolia
Beijing 97 48.5 (47) 27.8 (27) 2.1 (2) 39.2 (38) 4.1 (4) 2.1 (2)
Other 71 50.7 (36) 16.9 (12) 0.0 (0) 46.5 (33) 0.0 (0) 0.0 (0)
Taiwan#
Beijing 181 49.7 (90) 33.7 (61) 21.0 (38) 21.0 (38) 27.1 (49) 19.3 (35)
Other 172 35.5 (61)§ 24.4 (42) 15.7 (27) 19.8 (34) 16.9 (29)‡ 15.7 (27)

*Studies with >3 patients with Beijing genotype tuberculosis with known drug sensitivity included. In all but 3 of the included studies, >97% of patients were tested for drug resistance. The 3 exceptions were Argentina (95%), inner London (91%), and Jakarta (79%). In some studies, not all patients were tested for every drug. In some studies, "any drug" includes drugs not shown on the table (e.g., pyrazinamide). In Zimbabwe, 0/4 patients with Beijing genotype strains had drug- resistant strains; whether other strains were resistant is unknown.
†MDR, multidrug resistant, resistant to at least isoniazid and rifampin.
‡p<0.05.
§p<0.01.
¶p<0.001.
#Immigration status not known.
**Includes immigrants from neighboring countries.
††The 2 patients with drug-resistant Beijing strains in this study were brothers.

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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