|
|
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 Tuberculosis1
|
Appendix Table 1. 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
|
(1)
|
|
Finland: entire
|
2000–2002
|
Central laboratory for entire country
|
Pulm/Extra
|
?
|
RFLP, spoligo
|
(2)
|
| France |
| |
Paris area
|
1995
|
All patients from 10 hospitals
|
Pulm/Extra
|
88
|
RFLP, spoligo
|
(3)
|
|
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
|
(4)
|
|
Italy
|
| |
Verona
|
1996–1997
|
Reference laboratory for area
|
Pulm/Extra
|
?
|
Spoligo on all
|
(5)
|
|
Sardinia
|
1997–1998
|
Patients at 1 hospital
|
Pulm/Extra
|
73
|
RFLP, spoligo
|
|
Tuscany
|
2002
|
All patients in area
|
Pulm/Extra
|
83
|
RFLP, spoligo
|
(6)
|
|
Netherlands: entire
|
1993–2002
|
All patients in area
|
Pulm/Extra
|
96
|
RFLP, spoligo
|
(7)
|
|
Spain
|
| |
Elche
|
1993–1999
|
Sample of patients in area
|
Pulm/Extra
|
90
|
RFLP, spoligo
|
(8)
|
|
Madrid
|
1992–2001
|
All patients in area
|
Pulm/Extra
|
71
|
RFLP, spoligo
|
|
Zaragoza
|
1993–1995
|
All patients in area
|
Pulm/Extra
|
?
|
RFLP, spoligo
|
(9)
|
|
Sweden: western
|
1999–2002
|
Laboratory for all patients in area
|
Pulm/Extra
|
87
|
Spoligo on all
|
(10)
|
|
United Kingdom
|
| |
Inner London
|
1993
|
Laboratories for all patients in
area
|
Pulm/Extra
|
89
|
Spoligo on all
|
(11)
|
|
London
|
1995–1997
|
Laboratories for all patients in
area
|
Pulm/Extra
|
88
|
RFLP
|
(12)
|
|
Central and Eastern Europe
|
| |
Czech Republic: Prague and South Moravia
|
1998
|
Laboratories for all patients in
areas
|
Pulm/Extra
|
?
|
Spoligo on all
|
(13)
|
|
Estonia: entire
|
1994
|
All new pulmonary TB patients
in area
|
Pulm
|
100
|
RFLP, spoligo
|
(14)
|
|
Russia
|
| |
St. Petersburg
|
1999–2002
|
All patients in area with data
|
Pulm/Extra
|
59
|
RFLP, spoligo
|
(15,16)
|
|
Archangel
|
1998–1999
|
All patients at TB clinic
|
Pulm
|
75
|
Spoligo on all
|
(17)
|
|
North Africa and Middle East
|
| |
Iran: several areas
|
1995–1997
|
All smear-positive patients from
Shiraz plus random others
|
Pulm/Extra
|
79
|
RFLP, spoligo
|
(18)
|
|
Sub-Saharan Africa
|
| |
Cameroon: western region
|
1997–1998
|
All patients from all hospitals in
region
|
Pulm
|
79
|
Spoligo on all
|
(19,20)
|
|
Ethiopia: Addis Ababa
|
1996
|
Patients at 1 hospital
|
Pulm
|
85
|
RFLP, spoligo
|
(21)
|
|
Guinea Bissau: Bissau
|
1989–1993
|
All patients in area
|
Pulm
|
100
|
RFLP, spoligo
|
(22)
|
|
Malawi: Karonga District
|
1996–2003
|
All patients in area
|
Pulm/Extra
|
93
|
RFLP, spoligo
|
(23)
|
|
South Africa: Cape Town
|
1992–1998
|
All patients from 2 clinics
|
Pulm/Extra
|
91
|
RFLP, spoligo
|
(24)
|
|
Sudan: Khartoum
|
1998–1999
|
Patients from 2 clinics
|
Pulm
|
54
|
Spoligo on all
|
(25)
|
|
Zimbabwe: Harare
|
1997
|
All patients from 1 hospital
|
Pulm
|
93
|
Spoligo on all
|
(26)
|
|
North America
|
|
|
United States
|
| |
New Jersey
|
1999
|
All patients in area
|
Pulm/Extra
|
99
|
RFLP, spoligo, region A
|
(27)
|
|
San Francisco
|
1998–2000
|
All patients in area
|
Pulm/Extra
|
92
|
RFLP
|
(28)
|
|
Caribbean
|
|
|
Cuba
|
| |
Outside Havana
|
1994–1995
|
Isolates sent from regional laboratories
|
Pulm
|
94
|
RFLP, spoligo
|
(29)
|
|
Havana
|
1997–1998
|
Isolates sent to reference laboratory
|
Pulm
|
86
|
RFLP
|
(30)
|
|
Latin America
|
| |
Argentina: Buenos Aires
|
1998–2001
|
All patients in 1 hospital
|
Pulm/Extra
|
82
|
Spoligo on all
|
|
|
Brazil: Săo 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
|
(31)
|
|
Bangladesh: Mymensingh
|
2001–2003
|
Hospitalized patients, 3 hospitals
|
Pulm
|
1
|
Spoligo on all
|
(32)
|
|
Southeast Asia
|
| |
Indonesia: Jakarta
|
1998–1999
|
All patients from outpatient TB clinic
|
Pulm
|
75
|
RFLP,spoligo
|
(33)
|
|
Malaysia: entire
|
1993–1994
|
Random sample from reference laboratory
|
Pulm/Extra
|
89
|
RFLP
|
(34)
|
|
Thailand: Bangkok
|
1998–2000
|
All patients in single hospital
|
Pulm/Extra
|
Spoligo on all
|
(35)
|
|
Vietnam
|
| |
Hanoi, Ho Chi Minh City
|
1998–1999
|
All new smear-positive patients at
2 centers
|
Pulm
|
?
|
Spoligo on all
|
(36)
|
|
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
|
(37)
|
|
Japan: Okayama
|
2000–2002
|
All patients in area with data
|
Pulm/Extra
|
99
|
RFLP, spoligo
|
(38)
|
|
Mongolia: entire
|
1998–1999
|
Random sample of patients in
area
|
Pulm
|
100
|
Spoligo on all
|
(39)
|
|
Taiwan: entire
|
2002
|
Random sample from laboratory
|
Pulm/Extra
|
?
|
Spoligo on all
|
(40)
|
|
|
*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 (Universitŕ di Verona); Leonardo A Sechi,
Stephania Zanetti (Universitŕ di Sassari); Carlo Garzelli (Universitŕ
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).
|
Appendix
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J Clin Microbiol. 1999;37:3872–8.
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et al. Transmission
of a multidrug-resistant Mycobacterium tuberculosis strain resembling
"strain W" among noninstitutionalized, human immunodeficiency
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molecular epidemiologic analysis of tuberculosis trends in San Francisco,
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al. 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;2:743–50.
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IS6110 restriction fragment length polymorphism typing. Mem Inst
Oswaldo Cruz. 2001;96:437–43.
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to treatment. Emerg Infect Dis. 2001,7:880–3.
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epidemiology of tuberculosis in Malaysia. J Clin Microbiol. 1999;37:1265–8.
- Prodinger WM, Bunyaratvej P, Prachaktam R, Pavlic M. Mycobacterium
tuberculosis isolates of Beijing genotype in Thailand. Emerg
Infect Dis. 2001;7:483–4.
- Anh DD, Borgdorff M, Van LN, Lan NTN, van Gorkom T, Kremer K, et al.
Mycobacterium
tuberculosis Beijing genotype emerging in Vietnam. Emerg Infect
Dis. 2000;6:302–5.
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Seventy
percent of the Mycobacterium tuberculosis isolates in Hong Kong
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- Ohata R, Tada A.
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in Taiwan. J Clin Microbiol. 2005;43:95–100.
|
Appendix Table 2. Proportion
of tuberculosis cases caused by the Beijing genotype in different
studies
|
|
|
Study
|
Period
|
Overall Beijing/total (%)
|
Excluding immigrants,*
Beijing/total (%)
|
|
|
Western Europe
|
|
|
Austria: western
|
1993–2004
|
12/895 (1.3)
|
7/673 (1.0)
|
|
Denmark: entire
|
1992–2001
|
96/3,844 (2.5)
|
17/1,659 (1.0)
|
|
Finland: entire
|
2000–2002
|
23/1,246 (1.9)
|
13/1,119 (1.2)
|
|
France
|
|
Paris area
|
1995
|
3/272 (1.1)
|
0/91 (0.0)
|
|
Paris
|
2001–2003
|
5/66 (7.6)
|
1/22 (4.6)
|
|
Lyon
|
2003
|
3/85 (3.5)
|
1/31 (3.2)
|
|
Germany: Hamburg
|
2001
|
6/178 (3.4)
|
1/80 (1.3)
|
|
Italy
|
|
Verona
|
1996–1997
|
2/158 (1.3)
|
0/131 (0.0)
|
|
Sardinia
|
1997–1998
|
2/350 (0.6)
|
0/28 (0.0)
|
|
Tuscany
|
2002
|
7/245 (2.9)
|
2/153 (1.2)
|
|
Netherlands: entire
|
1993–2002
|
522/8,510 (6.1)
|
202/3,469 (5.8)
|
|
Spain
|
|
Elche
|
1993–1999
|
0/146 (0.0)
|
|
Madrid
|
1992–2001
|
0/507 (0.0)
|
0/484 (0.0)
|
|
Zaragoza
|
1993–1995
|
2/569 (0.4)
|
0/544 (0.0)
|
|
Sweden: western
|
1999–2002
|
11/212 (5.2)
|
3/77 (3.9)
|
|
United Kingdom
|
|
Inner London
|
1993
|
18/547 (3.3)
|
5/164 (3.0)
|
|
London
|
1995–1997
|
108/2,490 (4.3)
|
10/273 (3.7)
|
|
Central and Eastern Europe
|
| |
Czech Republic |
|
Prague
|
1998
|
2/111 (1.8)
|
1/104 (1.0)
|
|
South Moravia
|
1998
|
5/120 (4.2)
|
0/114 (0.0)
|
|
Estonia: entire
|
1994
|
61/209 (29.2)
|
61/209 (29.2)
|
|
Russia
|
|
St. Petersburg
|
1999–2001
|
133/236 (56.4)
|
133/236 (56.4)
|
|
Archangel
|
1998–1999
|
54/119 (45.4)
|
|
North Africa and Middle East
|
| |
Iran: several areas
|
1995–1997
|
10/101 (9.9)
|
6/81 (7.4)
|
|
Sub-Saharan Africa
|
| |
Cameroon†: western region
|
1997–1998
|
0/456 (0.0)
|
0/456 (0.0)
|
|
Ethiopia: Addis Ababa
|
1996
|
0/121 (0.0)
|
0/121 (0.0)
|
|
Guinea Bissau: Bissau
|
1989–1993
|
1/229 (0.4)
|
1/221 (0.5)
|
|
Malawi: Karonga District
|
1996–2003
|
44/1,030 (4.3)
|
38/785 (4.8)
|
|
South Africa: Cape Town
|
1992–1998
|
140/847 (16.5)
|
140/847 (16.5)
|
|
Sudan: Khartoum
|
1998–1999
|
0/49 (0.0)
|
0/48 (0.0)
|
|
Zimbabwe: Harare
|
1997
|
4/214 (1.9)
|
4/212 (1.9)
|
|
North America
|
| |
United States
|
|
New Jersey
|
1999
|
29/382 (7.6)
|
15/151 (9.9)
|
|
San Francisco
|
1998–2000
|
135/492 (27.4)
|
12/109 (11.0)
|
|
Caribbean
|
| |
Cuba
|
|
Outside Havana
|
1994–1995
|
22/160 (13.8)
|
22/160 (13.8)
|
|
Havana
|
1997–1998
|
4/51 (7.8)
|
4/51 (7.8)
|
|
Latin America
|
| |
Argentina: Buenos Aires
|
1998–2001
|
5/612 (0.8)
|
5/582 (0.9)
|
|
Brazil: Săo Paulo
|
2000–2001
|
4/420 (1.0)
|
3/382 (0.8)
|
|
Indian subcontinent
|
| |
India: Delhi
|
1995–1996
|
1/83 (1.2)
|
|
|
Bangladesh: Mymensingh
|
2000–2002
|
7/97 (7.2)
|
|
Southeast Asia
|
| |
Indonesia: Jakarta
|
1998–1999
|
32/91 (35.2)
|
32/91 (35.2)
|
|
Malaysia: Sample
|
1993–1994
|
71/426 (16.7)
|
65/388 (16.8)
|
|
Thailand: Bangkok
|
1998–2000
|
98/204 (48.0)
|
98/204 (48.0)
|
|
Vietnam
|
|
Hanoi
|
1998–1999
|
37/64 (57.8)
|
|
|
Ho Chi Minh City
|
1998–1999
|
263/499 (52.7)
|
|
Ho Chi Minh City
|
1998–2000
|
34/75 (45.3)
|
34/75 (45.3)
|
|
Tien Giang
|
2003
|
28/60 (46.7)
|
28/60 (46.7)
|
|
East Asia
|
| |
China
|
|
|
Shanghai and other areas
|
1994–1995
|
40/59 (67.8)
|
|
Henan
|
2000–2001
|
36/52 (69.2)
|
36/52 (69.2)
|
|
Hong Kong: Hong Kong
|
1998–1999
|
356/500 (71.2)
|
|
Japan: Okayama
|
2000–2002
|
103/142 (72.5)
|
103/142 (72.5)
|
|
Mongolia: entire
|
1998–1999
|
97/168 (57.7)
|
97/168 (57.7)
|
|
Taiwan: entire
|
2002
|
187/421 (44.4)
|
|
|
*Immigration status not known for all patients.
|
|
†The spoligotype of 1 isolate in this study had
only spacers 40–43, but other genetic markers showed it to be Mycobacterium
africanum.
|
|
Appendix Table 3. 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: Săo 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.
|
