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Microbiology 144 (1998), 3049-3060; DOI  10.1099/00221287-144-11-3049
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A multilocus sequence typing scheme for Streptococcus pneumoniae: identification of clones associated with serious invasive disease

Mark C. Enright1 and Brian G. Spratt1,2

Wellcome Trust Centre for the Epidemiology of Infectious Disease, Department of Zoology, University of Oxford, Oxford OX1 3PS, UK

2Author for correspondence: Brian G. Spratt. Tel: +44 1865 281301. Fax: +44 1865 310447 e-mail: brian.spratt@zoology.oxford.ac.uk

ABSTRACT

SUMMARY: The population biology of Streptococcus pneumoniae is poorly understood. Most of the important issues could be addressed by the molecular characterization of large, well sampled populations from carriage and from the different manifestations of pneumococcal disease. The authors have therefore developed a pneumococcal multilocus sequence typing scheme and database by sequencing - 450 bp fragments of seven housekeeping loci from 295 isolates. The combination of alleles at the seven loci provided an allelic profile, or sequence type (ST), and the relatedness between isolates was obtained by constructing a dendrogram from the matrix of paiwvise differences between STs. The typing scheme was validated using pneumococci of known genetic relatedness and could resolve 6 billion STs. Among 274 isolates from recent cases of invasive pneumococcal disease in eight countries,143 STs were resolved, but 12 STs contained at least five isolates (range 5-21 isolates). The repeated recovery of indistinguishable isolates from invasive disease in different countries implies that these STs define strains with an increased capacity to cause invasive disease. The relationship between STs and serotypes suggested that, in the longer term, capsular genes have been distributed horizontally within the pneumococcal population, but in the short term, expansion of clones occurs with only occasional changes of serotype. The multilocus sequence typing scheme provides a powerful new approach to the characterization of pneumococci, since it provides molecular typing datathat are electronically portable between laboratories, and which can be used to probe aspects of the population and evolutionary biology of these organisms. A Web sitefor themolecular characterization of pneumococci by MLST is available (http://mlst.zoo.ox.ac.uk).

Keywords: molecular typing, virulent clones, serotype stability, housekeeping genes, World Wide Web




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S. C. Clarke, J. M. C. Jefferies, A. J. Smith, J. McMenamin, T. J. Mitchell, and G. F. S. Edwards
Pneumococci causing invasive disease in children prior to the introduction of pneumococcal conjugate vaccine in Scotland.
J. Med. Microbiol., August 1, 2006; 55(Pt 8): 1079 - 1084.
[Abstract] [Full Text] [PDF]

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 Clin. Microbiol. Rev.Home page
A. Singh, R. V. Goering, S. Simjee, S. L. Foley, and M. J. Zervos
Application of Molecular Techniques to the Study of Hospital Infection
Clin. Microbiol. Rev., July 1, 2006; 19(3): 512 - 530.
[Abstract] [Full Text] [PDF]

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 Infect. Immun.Home page
M. M. Pettigrew, K. P. Fennie, M. P. York, J. Daniels, and F. Ghaffar
Variation in the Presence of Neuraminidase Genes among Streptococcus pneumoniae Isolates with Identical Sequence Types.
Infect. Immun., June 1, 2006; 74(6): 3360 - 3365.
[Abstract] [Full Text] [PDF]

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 Infect. Immun.Home page
N. A. Silva, J. McCluskey, J. M. C. Jefferies, J. Hinds, A. Smith, S. C. Clarke, T. J. Mitchell, and G. K. Paterson
Genomic Diversity between Strains of the Same Serotype and Multilocus Sequence Type among Pneumococcal Clinical Isolates.
Infect. Immun., June 1, 2006; 74(6): 3513 - 3518.
[Abstract] [Full Text] [PDF]

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 J Med MicrobiolHome page
H. Zemlickova, O. Melter, and P. Urbaskova
Epidemiological relationships among penicillin non-susceptible Streptococcus pneumoniae strains recovered in the Czech Republic.
J. Med. Microbiol., April 1, 2006; 55(Pt 4): 437 - 442.
[Abstract] [Full Text] [PDF]

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 J. Clin. Microbiol.Home page
W. P. Hanage, T. Kaijalainen, A. Saukkoriipi, J. L. Rickcord, and B. G. Spratt
A successful, diverse disease-associated lineage of nontypeable pneumococci that has lost the capsular biosynthesis locus.
J. Clin. Microbiol., March 1, 2006; 44(3): 743 - 749.
[Abstract] [Full Text] [PDF]

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 J. Clin. Microbiol.Home page
B. Beall, M. C. McEllistrem, R. E. Gertz Jr., S. Wedel, D. J. Boxrud, A. L. Gonzalez, M.-J. Medina, R. Pai, T. A. Thompson, L. H. Harrison, et al.
Pre- and postvaccination clonal compositions of invasive pneumococcal serotypes for isolates collected in the United States in 1999, 2001, and 2002.
J. Clin. Microbiol., March 1, 2006; 44(3): 999 - 1017.
[Abstract] [Full Text] [PDF]

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 Appl. Environ. Microbiol.Home page
T. J. Coffey, G. D. Pullinger, R. Urwin, K. A. Jolley, S. M. Wilson, M. C. Maiden, and J. A. Leigh
First Insights into the Evolution of Streptococcus uberis: a Multilocus Sequence Typing Scheme That Enables Investigation of Its Population Biology
Appl. Envir. Microbiol., February 1, 2006; 72(2): 1420 - 1428.
[Abstract] [Full Text] [PDF]

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 MicrobiologyHome page
R. Camilli, E. Pettini, M. D. Grosso, G. Pozzi, A. Pantosti, and M. R. Oggioni
Zinc metalloproteinase genes in clinical isolates of Streptococcus pneumoniae: association of the full array with a clonal cluster comprising serotypes 8 and 11A
Microbiology, February 1, 2006; 152(2): 313 - 321.
[Abstract] [Full Text] [PDF]

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 MicrobiologyHome page
A. J. Smith, J. Jefferies, S. C. Clarke, C. Dowson, G. F. S. Edwards, and T. J. Mitchell
Distribution of epidemic antibiotic-resistant pneumococcal clones in Scottish pneumococcal isolates analysed by multilocus sequence typing
Microbiology, February 1, 2006; 152(2): 361 - 365.
[Abstract] [Full Text] [PDF]

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 MicrobiologyHome page
R. Sa-Leao, A. S. Simoes, S. Nunes, N. G. Sousa, N. Frazao, and H. de Lencastre
Identification, prevalence and population structure of non-typable Streptococcus pneumoniae in carriage samples isolated from preschoolers attending day-care centres
Microbiology, February 1, 2006; 152(2): 367 - 376.
[Abstract] [Full Text] [PDF]

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 J. Clin. Microbiol.Home page
M. Enersen, I. Olsen, A. J. van Winkelhoff, and D. A. Caugant
Multilocus Sequence Typing of Porphyromonas gingivalis Strains from Different Geographic Origins
J. Clin. Microbiol., January 1, 2006; 44(1): 35 - 41.
[Abstract] [Full Text] [PDF]

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 Infect. Immun.Home page
K. Shen, J. Gladitz, P. Antalis, B. Dice, B. Janto, R. Keefe, J. Hayes, A. Ahmed, R. Dopico, N. Ehrlich, et al.
Characterization, Distribution, and Expression of Novel Genes among Eight Clinical Isolates of Streptococcus pneumoniae
Infect. Immun., January 1, 2006; 74(1): 321 - 330.
[Abstract] [Full Text] [PDF]

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 J. Clin. Microbiol.Home page
L.-A. S. Kirkham, J. M. C. Jefferies, A. R. Kerr, Y. Jing, S. C. Clarke, A. Smith, and T. J. Mitchell
Identification of Invasive Serotype 1 Pneumococcal Isolates That Express Nonhemolytic Pneumolysin
J. Clin. Microbiol., January 1, 2006; 44(1): 151 - 159.
[Abstract] [Full Text] [PDF]

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 MicrobiologyHome page
B. de las Rivas, A. Marcobal, and R. Munoz
Development of a multilocus sequence typing method for analysis of Lactobacillus plantarum strains
Microbiology, January 1, 2006; 152(1): 85 - 93.
[Abstract] [Full Text] [PDF]

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 CVIHome page
E. Sadowy, A. Skoczynska, J. Fiett, M. Gniadkowski, and W. Hryniewicz
Multilocus sequence types, serotypes, and variants of the surface antigen PspA in Streptococcus pneumoniae isolates from meningitis patients in Poland.
Clin. Vaccine Immunol., January 1, 2006; 13(1): 139 - 144.
[Abstract] [Full Text] [PDF]

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 Antimicrob. Agents Chemother.Home page
I. Cochetti, M. Vecchi, M. Mingoia, E. Tili, M. R. Catania, A. Manzin, P. E. Varaldo, and M. P. Montanari
Molecular Characterization of Pneumococci with Efflux-Mediated Erythromycin Resistance and Identification of a Novel mef Gene Subclass, mef(I)
Antimicrob. Agents Chemother., December 1, 2005; 49(12): 4999 - 5006.
[Abstract] [Full Text] [PDF]

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 Appl. Environ. Microbiol.Home page
A. Gibson, T. Brown, L. Baker, and F. Drobniewski
Can 15-Locus Mycobacterial Interspersed Repetitive Unit-Variable-Number Tandem Repeat Analysis Provide Insight into the Evolution of Mycobacterium tuberculosis?
Appl. Envir. Microbiol., December 1, 2005; 71(12): 8207 - 8213.
[Abstract] [Full Text] [PDF]

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 Appl. Environ. Microbiol.Home page
M. Scally, E. L. Schuenzel, R. Stouthamer, and L. Nunney
Multilocus Sequence Type System for the Plant Pathogen Xylella fastidiosa and Relative Contributions of Recombination and Point Mutation to Clonal Diversity
Appl. Envir. Microbiol., December 1, 2005; 71(12): 8491 - 8499.
[Abstract] [Full Text] [PDF]

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 J. Clin. Microbiol.Home page
M. A. P. van Bergen, K. E. Dingle, M. C. J. Maiden, D. G. Newell, L. van der Graaf-Van Bloois, J. P. M. van Putten, and J. A. Wagenaar
Clonal Nature of Campylobacter fetus as Defined by Multilocus Sequence Typing
J. Clin. Microbiol., December 1, 2005; 43(12): 5888 - 5898.
[Abstract] [Full Text] [PDF]

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 J. Clin. Microbiol.Home page
R. R. Reinert, M. R. Jacobs, P. C. Appelbaum, S. Bajaksouzian, S. Cordeiro, M. van der Linden, and A. Al-Lahham
Relationship between the Original Multiply Resistant South African Isolates of Streptococcus pneumoniae from 1977 to 1978 and Contemporary International Resistant Clones
J. Clin. Microbiol., December 1, 2005; 43(12): 6035 - 6041.
[Abstract] [Full Text] [PDF]

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 J. Clin. Microbiol.Home page
R. Pai, R. E. Gertz, C. G. Whitney, B. Beall, and the Active Bacterial Core Surveillance Team
Clonal Association between Streptococcus pneumoniae Serotype 23A, Circulating within the United States, and an Internationally Dispersed Clone of Serotype 23F
J. Clin. Microbiol., November 1, 2005; 43(11): 5440 - 5444.
[Abstract] [Full Text] [PDF]

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 J Antimicrob ChemotherHome page
M. Sangvik, P. Littauer, G. S. Simonsen, A. Sundsfjord, and K. H. Dahl
mef(A), mef(E) and a new mef allele in macrolide-resistant Streptococcus spp. isolates from Norway
J. Antimicrob. Chemother., November 1, 2005; 56(5): 841 - 846.
[Abstract] [Full Text] [PDF]

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 Antimicrob. Agents Chemother.Home page
M. J. Stanhope, S. L. Walsh, J. A. Becker, M. J. Italia, K. A. Ingraham, M. N. Gwynn, T. Mathie, J. A. Poupard, L. A. Miller, J. R. Brown, et al.
Molecular Evolution Perspectives on Intraspecific Lateral DNA Transfer of Topoisomerase and Gyrase Loci in Streptococcus pneumoniae, with Implications for Fluoroquinolone Resistance Development and Spread
Antimicrob. Agents Chemother., October 1, 2005; 49(10): 4315 - 4326.
[Abstract] [Full Text] [PDF]

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 J Med MicrobiolHome page
M A Diggle and S C Clarke
Truncated xpt gene present in invasive Streptococcus pneumoniae may have implications for MLST schemes
J. Med. Microbiol., October 1, 2005; 54(10): 909 - 912.
[Abstract] [Full Text] [PDF]

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 J. Clin. Microbiol.Home page
A. Baldwin, E. Mahenthiralingam, K. M. Thickett, D. Honeybourne, M. C. J. Maiden, J. R. Govan, D. P. Speert, J. J. LiPuma, P. Vandamme, and C. G. Dowson
Multilocus Sequence Typing Scheme That Provides Both Species and Strain Differentiation for the Burkholderia cepacia Complex
J. Clin. Microbiol., September 1, 2005; 43(9): 4665 - 4673.
[Abstract] [Full Text] [PDF]

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 J. Clin. Microbiol.Home page
N. G. Sousa, R. Sa-Leao, M. I. Crisostomo, C. Simas, S. Nunes, N. Frazao, J. A. Carrico, R. Mato, I. Santos-Sanches, and H. de Lencastre
Properties of Novel International Drug-Resistant Pneumococcal Clones Identified in Day-Care Centers of Lisbon, Portugal
J. Clin. Microbiol., September 1, 2005; 43(9): 4696 - 4703.
[Abstract] [Full Text] [PDF]

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 J. Bacteriol.Home page
W. P. Hanage, T. Kaijalainen, E. Herva, A. Saukkoriipi, R. Syrjanen, and B. G. Spratt
Using Multilocus Sequence Data To Define the Pneumococcus
J. Bacteriol., September 1, 2005; 187(17): 6223 - 6230.
[Abstract] [Full Text] [PDF]

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 J. Bacteriol.Home page
S. R. Nallapareddy, H. Wenxiang, G. M. Weinstock, and B. E. Murray
Molecular Characterization of a Widespread, Pathogenic, and Antibiotic Resistance-Receptive Enterococcus faecalis Lineage and Dissemination of Its Putative Pathogenicity Island
J. Bacteriol., August 15, 2005; 187(16): 5709 - 5718.
[Abstract] [Full Text] [PDF]

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 Antimicrob. Agents Chemother.Home page
R. R. Reinert, M. van der Linden, and A. Al-Lahham
Molecular Characterization of the First Telithromycin-Resistant Streptococcus pneumoniae Isolate in Germany
Antimicrob. Agents Chemother., August 1, 2005; 49(8): 3520 - 3522.
[Abstract] [Full Text] [PDF]

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 Antimicrob. Agents Chemother.Home page
N. Wolter, A. M. Smith, D. J. Farrell, W. Schaffner, M. Moore, C. G. Whitney, J. H. Jorgensen, and K. P. Klugman
Novel Mechanism of Resistance to Oxazolidinones, Macrolides, and Chloramphenicol in Ribosomal Protein L4 of the Pneumococcus
Antimicrob. Agents Chemother., August 1, 2005; 49(8): 3554 - 3557.
[Abstract] [Full Text] [PDF]

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 J. Bacteriol.Home page
S. J. King, A. M. Whatmore, and C. G. Dowson
NanA, a Neuraminidase from Streptococcus pneumoniae, Shows High Levels of Sequence Diversity, at Least in Part through Recombination with Streptococcus oralis
J. Bacteriol., August 1, 2005; 187(15): 5376 - 5386.
[Abstract] [Full Text] [PDF]

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 Antimicrob. Agents Chemother.Home page
L. Chesnel, R. Carapito, J. Croize, O. Dideberg, T. Vernet, and A. Zapun
Identical Penicillin-Binding Domains in Penicillin-Binding Proteins of Streptococcus pneumoniae Clinical Isolates with Different Levels of {beta}-Lactam Resistance
Antimicrob. Agents Chemother., July 1, 2005; 49(7): 2895 - 2902.
[Abstract] [Full Text] [PDF]

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 Antimicrob. Agents Chemother.Home page
R. R. Reinert, S. Reinert, M. van der Linden, M. Y. Cil, A. Al-Lahham, and P. Appelbaum
Antimicrobial Susceptibility of Streptococcus pneumoniae in Eight European Countries from 2001 to 2003
Antimicrob. Agents Chemother., July 1, 2005; 49(7): 2903 - 2913.
[Abstract] [Full Text] [PDF]

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 Antimicrob. Agents Chemother.Home page
M. J. Ferrandiz, C. Ardanuy, J. Linares, J. M. Garcia-Arenzana, E. Cercenado, A. Fleites, A. G. de la Campa, and the Spanish Pneumococcal Infection Study Network
New Mutations and Horizontal Transfer of rpoB among Rifampin-Resistant Streptococcus pneumoniae from Four Spanish Hospitals
Antimicrob. Agents Chemother., June 1, 2005; 49(6): 2237 - 2245.
[Abstract] [Full Text] [PDF]

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 J. Clin. Microbiol.Home page
L. M. Schouls, A. van der Ende, I. van de Pol, C. Schot, L. Spanjaard, P. Vauterin, D. Wilderbeek, and S. Witteveen
Increase in Genetic Diversity of Haemophilus influenzae Serotype b (Hib) Strains after Introduction of Hib Vaccination in The Netherlands
J. Clin. Microbiol., June 1, 2005; 43(6): 2741 - 2749.
[Abstract] [Full Text] [PDF]

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 MicrobiologyHome page
N. Bisharat, N. Jones, D. Marchaim, C. Block, R. M. Harding, P. Yagupsky, T. Peto, and D. W. Crook
Population structure of group B streptococcus from a low-incidence region for invasive neonatal disease
Microbiology, June 1, 2005; 151(6): 1875 - 1881.
[Abstract] [Full Text] [PDF]


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