Worldwide occurrence of Beijing/W strains of Mycobacterium tuberculosis: a systematic review. (Synopsis).Strains of the Beijing Beijing (bā-jĭng) or Peking (pē-kĭng, pā–), city (1994 est. urban pop. 6,093,300; 1994 est. total pop. 7,240,700), capital of the People's Republic of China./W genotype family of Mycobacterium anonymous mycobacteria , atypical mycobacteria nontuberculous mycobacteria. Group I–IV mycobacteria see nontuberculous mycobacteria. nontuberculous mycobacteria mycobacteria other than Mycobacterium tuberculosis Mycobacterium tuberculosis
tuberculosis have caused large outbreaks of tuberculosis, sometimes
involving multidrug resistance. This genetically highly conserved family
of M. tuberculosis strains predominates in some geographic areas. We
have conducted a systematic review of the published reports on these
strains to determine their worldwide distribution, spread, and
association with drug resistance drug resistance, condition in which infecting bacteria can resist the destructive effects of drugs such as antibiotics and sulfa drugs. Drug resistance has become a serious public health problem, since many disease-causing bacteria are no longer susceptible to previously effective drug therapies.. Sixteen studies reported prevalence of
Beijing strains defined by spoligotyping; another 10 used other
definitions. Beijing strains were most prevalent in Asia but were found
worldwide. Associations with drug resistance varied: in New York, Cuba,
Estonia, and Vietnam, Beijing strains were strongly associated with drug
resistance, but elsewhere the association was weak or absent. Although
few reports have measured trends in prevalence, the ubiquity of the
Beijing strains and their frequent association with outbreaks and drug
resistance underline their importance.n. or M. bovis ; they are divided into four groups, I–IV, on the basis of several physical characteristics. Tubercic bacillus. ********** In the early 1990s, a multidrug-resistant Mycobacterium tuberculosis strain was identified in New York (1). This strain, designated "W," which was associated with large institutional outbreaks of tuberculosis (TB) and many deaths, was later identified in other parts of the United States (2,3). In 1995, a large proportion of the M. tuberculosis strains in the Beijing area of China was reported to have mutually highly similar multi-banded IS6110 restriction fragment-length polymorphism (RFLP) patterns; these "Beijing" strains were also present in many other populations (4). The New York City multidrug-resistant "W" strain was, in the second half of the 1990s, recognized as a member of the "Beijing" genotype family of M. tuberculosis strains (5-7). The W strain is recognized by a specific IS6110 fingerprint pattern, by multiplex polymerase chain reaction (PCR) targeted at specific insertions, or both (2,3). W family strains have IS6110 patterns closely related to that of W, although the degree of similarity in different studies has not always been specified. Beijing strains, including the W variants, have an insertion of IS6110 in the genomic dnaA-dnaN locus (5,7). All W family strains have a characteristic spoligotype that is shared with the whole Beijing family of strains and seems to be specific for this family (4,8,9). Spoligotyping is based on DNA polymorphism DNA polymorphism n. in
the direct repeat region, and "Beijing" spoligotypes only
contain spacers 35-43. A condition in which one of two different but normal nucleotide sequences can exist at a particular site in a DNA molecule. The combination of a widespread family of strains and, in some situations, the association with multidrug resistance has led to concern that these strains may be spreading and may have a predilection for acquiring drug resistance. Many recent studies have recorded "Beijing-like" or "W-like" strains. We have conducted a systematic review of published reports to assess how widespread the family of strains is, whether there is any evidence that it is spreading, and whether it is associated with drug resistance. Methods Relevant studies were identified through computerized searches of Medline (January 1, 1990-November 1, 2001) and PubMed (January 1, 2000-November 1, 2001), manually searching key journals, searching the Internet, and crosschecking references with collections of articles on Beijing strains compiled by researchers in the field. The computerized searches used both thesaurus and free-text terms to search for tuberculosis and any of the following: molecular epidemiology, DNA fingerprinting, DNA [fingerprint.sup.*], typing, type, types, restriction fragment length polymorphism, RFLP, spoligotyping, [spoligotyp.sup.*], strain, and strains. The International Journal of Tuberculosis and Lung Disease, its predecessor Tuberculosis and Lung Disease, and the Journal of Clinical Microbiology were searched manually back to January 1990. A request for relevant articles was sent to all 32 participants in the European Union Concerted Action project on New Generation Genetic Markers and Techniques for the Epidemiology and Control of Tuberculosis. An Internet search, using Google, used the term "Beijing strain tuberculosis." The reference lists of all included articles were searched for additional relevant studies. Articles were included if they contained information allowing estimation of the proportion of TB patients included with the Beijing or W strains. Articles were excluded if they were limited to a particular outbreak, if they included only drug-resistant strains, or if <30 TB patients were included. Identified articles were subdivided into those that used spoligotyping to identify Beijing family strains and those that used other methods. Where spoligotypes were shown, estimates based on the spoligotype were used rather than any estimate given in the papers, using the proportion with spacers 35-43. Studies identifying only W strains or other W-like strains with a single IS6110 fingerprint pattern will underestimate the prevalence of Beijing strains, since they identify only part of the family of strains. The method of patient selection was recorded when stated. In all studies, any evidence of changes over time or by age group or of any association between strain type and drug resistance was recorded. Results Five thousand nineteen articles were selected from the initial search of Medline and PubMed. The titles and abstracts of these articles were scanned for relevant information, and 4,909 articles were rejected, leaving 110 articles for full text review. No further articles were identified by manual searching, but one recently published article was identified in the article collections that had not yet been indexed in the databases (10). One additional article was identified from reference list checking that was published in a Vietnamese journal not indexed by Medline, EMBASE, or Web of Science, and we have been unable to locate it. Another article was found from an Internet search, in an electronic journal (11). Of the 112 articles reviewed in full, 26 fulfilled the inclusion criteria of this review, including 16 that gave results based on spoligotyping and several that reported results from more than one area (Tables 1,2; Figure). Studies that described patients who were apparently included in other reports have been excluded (31,32). [FIGURE OMITTED] The Beijing strain was most common in the Beijing area of China, accounting for 92% of strains (4,12). The strain was common in all the Asian studies (4,8,12-15,23-25) and also in Houston, Texas (25%), and Estonia (29%) (18,20). Some examples of the Beijing family were seen in almost all the populations studied (Tables 1 and 2). Two studies looked at trends over time (Table 1). In China, the proportion of TB due to Beijing family strains in stored specimens going back to the 1950s was similar to the proportion among more recent specimens (12). In Gran Canaria, a dramatic increase was seen from 1992 to 1996, traced to an outbreak originating from a noncompliant patient with laryngeal TB (19). In studies over a short period, variations with age can be studied as a proxy for time trends. In Vietnam, among new cases of TB, the proportion due to Beijing strains was 71% in those <25 years of age, decreasing to 41% in those [greater than or equal to] 55 years (p < 0.001, chi square test for trend) (14). In Bangkok, little difference was seen with age in two studies (15,24). In Hong Kong (13), Jakarta, Indonesia (8), and Estonia (18), there was no association between age and disease due to the Beijing strain. In New Jersey, among those with tuberculosis due to W-like strains, 70% of patients were <50 years old, compared with 63% of those with other strains (p=0.2) (9). In Gran Canaria, the median age of cases with the Beijing strain was similar to that of all cases (19). No other studies have presented results by age. Several studies reported associations with drug resistance (Table 3). Some studies found high rates of drug resistance among Beijing strains, but others found no difference in drug resistance profiles between Beijing and the other local strains. An association between the successful spread of Beijing strains and BCG vaccination has been suggested (4). In Jakarta, Indonesia (8), 26% of those with Beijing strains and 23% of other patients had a BCG scar. In Vietnam, although a higher proportion of those with Beijing strains than with other strains had a BCG scar, this association was no longer apparent after the data were adjusted for age (14). Discussion This review has confirmed the ubiquity of the Beijing family of strains. Only a few of the smaller studies (in Martinique and French Guiana) found no examples, and the proportion of TB due to Beijing strains in several Asian studies was >50%. However, studies could only be included in the review if they mentioned the Beijing strain or strain W or presented data showing spoligotypes. Some of the excluded studies may have found Beijing strains but not reported them as such (33,34). Others may have looked for Beijing strains but not reported negative findings. The only articles identified that reported not finding Beijing strains were studies including more than one study site. It is not known how unusual it is for a genotype family of M. tuberculosis to be as widespread as this. Comparable data are not available for other strains, although they are beginning to be gathered, and some other strains have also been found in several distinct settings (35). In many studies, the true proportion of TB attributable to the Beijing family of strains is hard to assess. Difficulties arise due to the variable strain definitions used and the way patients were selected for inclusion. Spoligotyping seems to be both sensitive and specific for the Beijing family and is also easily compared between studies (6). Although IS6110 fingerprinting can also be used to detect this genotype family, with results that correlate closely with the spoligotypes, most published studies have used narrow definitions, based on a single strain or a few closely related strains defined by IS6110 fingerprinting; such studies are thus likely to underestimate the prevalence of Beijing strains. Studies including drug resistance in the definition (2) and those that appear to have defined the strains after grouping by drug resistance (26) may also underestimate the prevalence. Some of the studies (those in the Netherlands, New Jersey, Houston, Texas, Gran Canaria, and French Guiana and the Caribbean islands) included information on all TB patients in the population and thus provide reliable estimates of prevalence. Others were less representative, and many did not state how the patients were selected (Table 1 and 2). Studies that included patients from particular hospitals may be representative of an area, but referral hospitals may be biased if they accept a high proportion of drug-resistant or complex cases. Similarly, convenience samples may not be representative of the community of TB patients, particularly if the samples were kept because they were interesting in some way (e.g., drug resistant or from epidemiologically related cases). TB patients in prison (10) may not have the same strains as those in the community. Some studies included only new patients, and others included both new patients and recurrent cases. This distinction, which was often not clear in the reports, could influence the results if relapse rates differ between strains. In many studies, some culture-positive specimens are not typed because they are nonviable. IS6110 RFLP typing relies on large quantities of DNA and hence on viable strains, and theoretically some genotypes may survive better than others in vitro. Spoligotyping is PCR-based so does not require viable isolates, but it is sometimes used only as a secondary method in specimens that have already been typed by IS6110 RFLP. Associations with drug resistance were variable (Table 3): of the 12 studies with data available, only 4 found statistically significant increases in the proportions of drug resistance among those with Beijing strains. Of the Asian studies, only one found a statistically significant increase in drug resistance in Beijing strains (14), and in Hong Kong the Beijing strains were less likely than the others to be isoniazid isoniazid /iso·ni·a·zid/ (-ni´ah-zid) an antibacterial used as a tuberculostatic. i·so·ni·a·zid (   s resistant (13). In contrast, Beijing strains were strongly
associated with drug resistance in New York, Cuba, and Estonia
(3,18,21). In New York, the spread of the W strain, which was mainly
nosocomial and institutional, has been attributed in part to drug
resistance. Once a strain has become multidrug resistant, treatment is
more complicated so patients may remain infectious for a longer period.
Whether the Beijing family has a particularly high probability of
acquiring drug resistance is not known but is suggested by the fact that
these associations with the same strain family have been found in widely
distributed areas.The published studies provided little direct evidence that the Beijing strain has been increasing. Of the two studies that included time trends, one found no increase in a population with a very high prevalence for many decades (12), and in the other the increase may be attributable to the characteristics of the index patient in the outbreak (19,36). In Vietnam, the proportion of new TB patients with the Beijing strain decreased with age, suggesting an increase in Beijing strains in the communities studied (14). No association with age was found anywhere else (8,9,13,15,18,19,24), including the two other studies restricted to new patients (13,18). On the other hand, the ubiquity of the Beijing strain and its frequent appearance in outbreaks, particularly of drug-resistant TB, suggest that it may have the potential to spread. In Estonia, although there was no association between Beijing strains and age, TB and particularly multidrug-resistant (MDR) TB have been increasing, and most MDR TB was found to be due to Beijing strains (18). The limited amount of information available from most areas of the world and the possible biases in many of the studies make definite conclusions about the extent of spread and associations with drug resistance impossible. Through the European Concerted Action on New Generation Genetic Markers and Techniques for the Epidemiology and Control of Tuberculosis, a standard definition of the Beijing genotype is being finalized, by comparisons of large collections of strains typed with spoligotyping, IS6110 RFLP, and Region A RFLP, which visualizes insertion of IS6110 in the genomic dnaA-dnaN locus (ms. in preparation). Studies are planned to reanalyze available data worldwide by using standard definitions and approaches. Further studies are also needed to include more areas in an unbiased way, to study historical specimens if possible, and to investigate the virulence (8) and transmissibility of this potentially important family of M. tuberculosis strains. The question to be answered is if and to what extent Beijing genotype strains have selective advantages over other M. tuberculosis genotypes in the ability to gain resistance and to interact with the host immune defense system. If Beijing genotype strains represent a higher level of evolutionary development of M. tuberculosis being selected for as a result of the introduction of tuberculostatics, which inhibit the growth of M. tuberculosis, then consequences for the treatment of tuberculosis will be serious.
Table 1. Prevalence of Beijing family strains in studies that have used
spoligotyping (a)
Reference Setting Yrs Population
Asia
12 Beijing and 1956-1960 Stored lung biopsy
Hebei province, samples from pneumo-
China nectomies
1969-1970
1979-1980
1989-1990
1956-1990
4 Beijing, China 1992-1994 ? Selection method
13 Hong Kong 1998-1999 Random sample
14 Ho Chi Minh 1998-1999 ? All patients
City, and
Hanoi, Vietnam
15 Bangkok, 1999-2000 One hospital
Thailand ? Selection method
8 Jakarta, 1998-1999 Consecutive patients
Indonesia one clinic
Africa
16 Senegal 1994-1995 ? Selection method
(all Beijing were
relapses)
Middle East
17 Fars Province 1995-1996 All from Shiraz;
and Tehran, ? random for others
Iran
Europe
11 Northwest 1997-1998 ? Selection method
region, Russia
10 Azerbaijan 1995-1996 Prison
? Selection method
18 Estonia 1994 Two hospitals,
pulmonary TB
4 Netherlands 1993-1994 Whole population
19 Gran Canaria, 1991-1992 Whole island
Spain 1993
1994
1995
1996
1999
USA
9 New Jersey 1996-1998 Whole population
20 Houston, Texas 1994-1999 Whole population
Caribbean
21 Cuba, outside 1994-1995 Whole population
Havana
22 Guadeloupe 1994-1996 Whole island
22 Martinique 1995-1996 Whole island
South
America
22 French Guiana 1995-1996 Whole country
Prevalence
New TB or Beijing
Reference Setting Yrs new + old strain N/N (%)
Asia
12 Beijing and 1956-1960 ? Both 9/10 (90)
Hebei province,
China
1969-1970 8/9 (89)
1979-1980 18/18 (100)
1989-1990 10/12 (83)
1956-1990 45/49 (92)
4 Beijing, China 1992-1994 ? Both 45/49 (92)
13 Hong Kong 1998-1999 ? New 337/500 (67)
14 Ho Chi Minh 1998-1999 New 301/563 (53)
City, and
Hanoi, Vietnam
15 Bangkok, 1999-2000 ? Both 90/204 (44)
Thailand
8 Jakarta, 1998-1999 ? Both 31/92 (34)
Indonesia
Africa
16 Senegal 1994-1995 Both 8/69 (12)
Middle East
17 Fars Province 1995-1996 Both 10/97 (10)
and Tehran,
Iran
Europe
11 Northwest 1997-1998 Both 22/100 (22)
region, Russia
10 Azerbaijan 1995-1996 Both 46/65 (71)
18 Estonia 1994 New 61/209 (29)
4 Netherlands 1993-1994 Both 82/2,594 (3)
19 Gran Canaria, 1991-1992 ? Both 0/85 (0)
Spain 1993 10/179 (5.5)
1994 12/148 (8.1)
1995 18/110 (16)
1996 35/129 (27)
1999 9/40 (23)
USA
9 New Jersey 1996-1998 Both 68/1,207 (6)
20 Houston, Texas 1994-1999 ? Both 326/1,283 (25)
Caribbean
21 Cuba, outside 1994-1995 ? Both 20/157 (13)
Havana
22 Guadeloupe 1994-1996 ? Both 1/95 (1)
22 Martinique 1995-1996 ? Both 0/31 (0)
South
America
22 French Guiana 1995-1996 ? Both 0/76 (0)
(a) N/N, number with Beijing strain/total number of patients;
?, not clear from report.
Table 2. Prevalence of Beijing and W-like strains in studies not based
on spoligotyping (a)
Reference Setting Yrs Population
Asia
23 Henan Province, ? No information given
China
23 Philippines ? No information given
23 Hanoi, Vietnam ? No information given
23 Korea 1995 No information given
23 Thailand ? No information given
24 Bangkok 1994-1995 Patients from 3
Nonthaburi, Thailand hospitals ? how
selected. Half extrapul-
monary
23 Malaysia ? No information given
25 Malaysia 1993-1994 Random 3% sample from
whole population
Africa
26 Cape Town, South 1993-1997 Whole population
Africa
USA
27 New York City 1992-1994 Patients from 5
hospitals
3 New York City 1990-1995 ? selection method
28 Central Los Angeles 1994-1996 Consecutive patients
29 California 1992-1995 All cases from specific
locations
29 Texas 1993-1995 All cases from specific
locations
29 Colorado 1989-1994 All cases from specific
locations
2 United States 1992-1997 All notified cases
(excluding NY) and
Puerto Rico
South
America
30 Buenaventura, 1997-1998 34 treatment failure +
Colombia 73 new ? selection
method
New TB or Typing methods and
Reference Setting new + old definitions used
Asia
23 Henan Province, ? RFLP +3.6kb Pvu II
China fragment
23 Philippines ? RFLP +3.6kb Pvu II
fragment
23 Hanoi, Vietnam ? RFLP +3.6kb Pvu II
fragment
23 Korea ? RFLP +3.6kb Pvu II
fragment
23 Thailand ? RFLP +3.6kb Pvu II
fragment
24 Bangkok ? Both RFLP + comparison
Nonthaburi, Thailand with Dutch database
23 Malaysia ? RFLP +3.6kb Pvu II
fragment
25 Malaysia ? Both RFLP "similar" to
Beijing family
Africa
26 Cape Town, South Both RFLP "strain U",
Africa (W-like) Two closely
related patterns only
USA
27 New York City ? Both RFLP, strain W only
3 New York City ? Both RFLP, "W-like"
28 Central Los Angeles ? Both RFLP, strain 210
(W-related)
29 California ? Both RFLP, strain 210
(W-related)
29 Texas ? Both RFLP, strain 210
(W-related)
29 Colorado ? Both RFLP, strain 210
(W-related)
2 United States Both RFLP and/or PCR probe.
(excluding NY) and Multidrug resistant W
Puerto Rico only
South
America
30 Buenaventura, Both RFLP + PCR probe.
Colombia "Similar" to W
Prevalence of
Beijing strain
Reference Setting N/N (%)
Asia
23 Henan Province, 59/64 (92)
China
23 Philippines 34/34 (100)
23 Hanoi, Vietnam 20/50 (40)
23 Korea 99/138 (72)
23 Thailand 31/49 (63)
24 Bangkok 80/211 (37)
Nonthaburi, Thailand
23 Malaysia 17/48 (35)
25 Malaysia 83/439 (19)
Africa
26 Cape Town, South 17/650 (2.6)
Africa
USA
27 New York City 6/302 (2.0)
3 New York City 273/1,953 (14)
28 Central Los Angeles 43/162 (27)
29 California 39/522 (7)
29 Texas 16/546 (3)
29 Colorado 2/256 (0.8)
2 United States 23/104,549 (0.02)
(excluding NY) and
Puerto Rico
South
America
30 Buenaventura, 11/107 (10)
Colombia (? 8 in new)
(a) N/N, number with Beijing strain/total number of patient;
?, not clear from report; the different typing methods are described in
the introduction.
RFLP; restriction fragment length polymorphism using IS6110.
PCR; Polymerase chain reaction probe is a multiplex PCR probe targeted
at specific insertions. The 3.6 kb pvuII fragment was identified by
IS1081 fingerprinting.
Table 3. Association between Beijing family strains of Mycobacterium
tuberculosis and drug resistance (a)
% Drug resistance
Strain Any
Non- Non-
Reference Place, yr Beijing Beijing Beijing Beijing
13 Hong Kong, 310 181
1998-1999
14 Ho Chi 264 235
Minh City,
1998-1999
15 Bangkok, 90 114
1999-2000
8 Jakarta, 27 56 41 25
1998-1999
16 Senegal, 8 61
1994-1995
11 NW Russia, 22 78
1997-1998
10 Azerbaijan, 46 19 89 68
1995-1996
18 Estonia, 61 148 70 14
1994
19 Gran 75 576 0 ?
Canaria,
1991-1996
3 New York, 273 1,680
1990-1995 (W- (not W
like) like)
21 (d) Cuba, 20 137 55-65 4-5
1994-1995
30 Colombia, 11 70
1997-1998
% Drug resistance
I S
Non- Non-
Reference Place, yr Beijing Beijing Beijing Beijing
13 Hong Kong, 6 12 10 13
1998-1999
14 Ho Chi 28 19 42 19
Minh City,
1998-1999
15 Bangkok,
1999-2000
8 Jakarta, 37 20 15 5
1998-1999
16 Senegal,
1994-1995
11 NW Russia,
1997-1998
10 Azerbaijan, 80 68 83 58
1995-1996
18 Estonia,
1994
19 Gran
Canaria,
1991-1996
3 New York,
1990-1995
21 (d) Cuba, 55-60 4 0-10 0.7-2
1994-1995
30 Colombia,
1997-1998
% Drug resistance
MDR
Comparison of Beijing
Non- vs. non-Beijing by drug
Reference Place, yr Beijing Beijing (b) RR 95% CI (b)
13 Hong Kong, I 0.54 (0.30 to 0.97)
1998-1999 S 0.76 (0.46 to 1.3)
14 Ho Chi 3 2 I 1.5 (1.1 to 2.0)
Minh City, S 2.2 (1.6 to 3.0)
1998-1999 MDR 1.4 (0.47 to 4.3)
15 Bangkok, No assoc
1999-2000
8 Jakarta, Any 1.6 (0.86 to 3.1)
1998-1999 I 1.9 (0.92 to 3.9)
S 2.8 (0.67 to 11.5)
16 Senegal, No assoc
1994-1995
11 NW Russia, 77 58 MDR 1.3 (1.0 to 1.8)
1997-1998
10 Azerbaijan, 61 32 Any 1.3 (0.94 to 1.8)
1995-1996 I 1.2 (0.84 to 1.6)
S 1.4 (0.95 to 2.1)
MDR 1.9 (0.96 to 3.9)
18 Estonia, 34 2 Any 5.0 (3.2 to 7.6)
1994 MDR 17.0 (5.3 to 54.9)
19 Gran
Canaria,
1991-1996
3 New York, 93 (c) ?0 p <0.001
1990-1995
21 (d) Cuba, 0 0.7 Any 10.8 (4.7 to 24.5)
1994-1995 I 15.1 (5.8 to 38.9)
30 Colombia, 27 23 MDR 1.2 (0.41 to 3.4)
1997-1998
(a) I, isoniazid; S, streptomycin; MDR, multidrug resistant (at least
isoniazid and rifampicin); blank spaces indicate that data are not
available.
(b) Relative risks (RR) were calculated when possible from the data
presented. These are shown with 95% confidence intervals.
(c) Resistant to at least four drugs. Includes 206 W strains and 40 W1
strains. Identified by RFLP, not spoligotyping.
(d) Exact numbers not clear since drug resistance data only given by
strain number for IS6110 defined clusters, and two Beijing strains were
not clustered. For the relative risk calculation, the minimum proportion
resistant among the Beijing strains was used.
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Transmission of a multidrug-resistant Mycobacterium tuberculosis strain resembling "strain W" among noninstitutionalized, human immunodeficiency virus-seronegative patients. J Infect Dis 1999;180:1608-15. (27.) Tornieporth NG, Ptachewich Y, Poltoratskaia N, Ravi BS, Katapadi M, Berger JJ, et al. Tuberculosis among foreign-born persons in New York City, 1992-1994: implications for tuberculosis control. Int J Tuberc Lung Dis 1997;1:528-35. (28.) Barnes PF, Yang Z, Preston-Martin S, Pogoda JM, Jones BE, Otaya M, et al. Patterns of tuberculosis transmission in Central Los Angeles. JAMA 1997;278:1159-63. (29.) Yang Z, Barnes PF, Chaves F, Eisenach Eisenach (ī`zənäkh), city (1994 pop. 42,580), Thuringia, central Germany. It is an industrial center and rail junction. Industries include tourism, the manufacture of machinery, metal and wood products, chemicals, and electrical goods. KD, Weis SE, Bates JH, Cave MD. 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Tuber Lung Dis 2000;80:75-83. (34.) Torrea G, Levee G, Grimont P, Martin C, Chanteau S, Gicquel B. Chromosomal DNA fingerprinting analysis using the insertion sequence IS6110 and the repetitive element DR as strain-specific markers for epidemiological study of tuberculosis in French Polynesia. J Clin Microbiol 1995;33:1899-904. (35.) Sola C, Filliol I, Gutierrez MC, Mokrousov I, Vincent V, Rastogi N. Spoligotype database of Mycobacterium tuberculosis: biogeographic distribution of shared types and epidemiologic and phylogenetic perspectives. Emerg Infect Dis 2001,7:390-6. (36.) Bishai W. Tuberculosis transmission--rogue pathogen or rogue patient? Am J Respir Crit Care Med 2001;164:1104-5. Dr. Glynn is a senior lecturer in epidemiology at the London School of Hygiene and Tropical Medicine, London, United Kingdom. Her research interests include tuberculosis, HIV, and molecular epidemiology. Address for correspondence: Judith Glynn, Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK; fax: 44-(0)-20-7636-8739; e-mail: judith.glynn@lshtm.ac.uk Judith R. Glynn, * Jennifer Whiteley, * Pablo J. Bifani, ([dagger]) Kristin Kremer, ([double dagger]) and Dick van Soolingen ([double dagger]) * London School of Hygiene and Tropical Medicine, London, UK; ([dagger]) Institut Pasteur de Lille, France; and ([double dagger]) National Institute of Public Health and the Environment (RIVM), Bilthoven, the Netherlands |
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