Volume 12, Number 5—May 2006
THEME ISSUE
Tuberculosis Special Section
Research
Beijing/W Genotype Mycobacterium tuberculosis and Drug Resistance
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.
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).