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Journal of Clinical Microbiology, May 2003, p. 1963-1970, Vol. 41, No. 5
0095-1137/03/$08.00+0     DOI: 10.1128/JCM.41.5.1963-1970.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Snapshot of Moving and Expanding Clones of Mycobacterium tuberculosis and Their Global Distribution Assessed by Spoligotyping in an International Study{dagger}

Ingrid Filliol,1 Jeffrey R. Driscoll,2 Dick van Soolingen,3 Barry N. Kreiswirth,4 Kristin Kremer,3 Georges Valétudie,1 Dang Duc Anh,5 Rachael Barlow,6 Dilip Banerjee,7 Pablo J. Bifani,4 Karine Brudey,1 Angel Cataldi,8 Robert C. Cooksey,9 Debby V. Cousins,10 Jeremy W. Dale,11 Odir A. Dellagostin,12 Francis Drobniewski,13 Guido Engelmann,14 Séverine Ferdinand,1 Deborah Gascoyne-Binzi,6 Max Gordon,1 M. Cristina Gutierrez,15 Walter H. Haas,16 Herre Heersma,3 Eric Kassa-Kelembho,17 Ho Minh Ly,5 Athanasios Makristathis,18 Caterina Mammina,19 Gerald Martin,20 Peter Moström,1 Igor Mokrousov,21 Valérie Narbonne,22 Olga Narvskaya,21 Antonino Nastasi,23 Sara Ngo Niobe-Eyangoh,15 Jean W. Pape,24 Voahangy Rasolofo-Razanamparany,25 Malin Ridell,26 M. Lucia Rossetti,27 Fritz Stauffer,28 Philip N. Suffys,29 Howard Takiff,30 Jeanne Texier-Maugein,31 Véronique Vincent,15 Jacobus H. de Waard,32 Christophe Sola,1* and Nalin Rastogi1*

Unité de la Tuberculose et des Mycobactéries, Institut Pasteur de Guadeloupe, Pointe-à-Pitre, Guadeloupe,1 Wadsworth Center, New York State Department Of Health, Albany New York,2 Public Health Research Institute, Tuberculosis Center, Newark, New Jersey,4 Diagnosis Laboratory for Infectious Diseases and Perinatal Screening RIVM, Bilthoven, The Netherlands,3 National Institute of Hygiene and Epidemiology, Hanoi, Vietnam,5 Department of Microbiology, Leeds General Infirmary, Leeds,6 Medical School, St Georges Hospital,7 Mycobacterium Reference Unit, PHLS, Dulwich Hospital, London,13 University of Surrey, Guildford, Surrey, United Kingdom,11 Instituto de Biotecnologia INTA, Moron, Argentina,8 Tuberculosis Mycobacteriology Branch, Centers for Disease Control and Prevention, Atlanta, Georgia,9 Australian Reference Laboratory for Bovine Tuberculosis, Department of Agriculture, South Perth, Australia,10 Centro de Biotecnologia, Universidade Federal de Pelotas, Pelotas,12 Universidade Federal do Rio Grande do Sul, Porto Alegre,27 Department of Biochemistry and Molecular Biology, Fiocruz, Oswaldo Cruz Institute, Rio de Janeiro, Brazil,29 University Childrens Hospital, Heidelberg,14 Infektions Epidemiology, Robert Koch Institute, Berlin,16 Bundesinstitut für Gesundheitlichen Verbraucherschutz und Veterinärmedizin, Jena, Germany,20 Centre National de Référence des Mycobactéries, Institut Pasteur, Paris,15 Laboratoire de Bactériologie, CHU de Brest, Brest,22 Laboratoire de Bactériologie, CHU de Bordeaux, Bordeaux, France,31 Institut Pasteur de Bangui, Bangui, Central African Republic,17 Klinische Mikrobiologie, Hygiene-Institut der Universität,18 Bundesstaatliche Bakteriologisch-Serologische Untersuchungsanstalt Wien, Vienna, Austria,28 Department of Hygiene and Microbiology, University of Palermo, Palermo,19 Department of Public Health, University of Florence, Florence, Italy,23 Laboratory of Molecular Microbiology, Saint Petersburg Pasteur Institute, Saint Petersburg, Russia,21 Les Centres Gheskio, INLR, Port au Prince, Haïti,24 Institut Pasteur de Madagascar, Tananarive, Madagascar,25 Institute of Medical Microbiology and Immunology, Göteborg University, Göteborg, Sweden,26 IVIC, Centro de Microbiología y Biología Celular, Laboratorio de Genética Molecular,30 Tuberculosis Laboratory, Instituto de Biomedicina, Caracas, Venezuela,32

Received 21 October 2002/ Returned for modification 6 January 2003/ Accepted 31 January 2003

The present update on the global distribution of Mycobacterium tuberculosis complex spoligotypes provides both the octal and binary descriptions of the spoligotypes for M. tuberculosis complex, including Mycobacterium bovis, from >90 countries (13,008 patterns grouped into 813 shared types containing 11,708 isolates and 1,300 orphan patterns). A number of potential indices were developed to summarize the information on the biogeographical specificity of a given shared type, as well as its geographical spreading (matching code and spreading index, respectively). To facilitate the analysis of hundreds of spoligotypes each made up of a binary succession of 43 bits of information, a number of major and minor visual rules were also defined. A total of six major rules (A to F) with the precise description of the extra missing spacers (minor rules) were used to define 36 major clades (or families) of M. tuberculosis. Some major clades identified were the East African-Indian (EAI) clade, the Beijing clade, the Haarlem clade, the Latin American and Mediterranean (LAM) clade, the Central Asian (CAS) clade, a European clade of IS6110 low banders (X; highly prevalent in the United States and United Kingdom), and a widespread yet poorly defined clade (T). When the visual rules defined above were used for an automated labeling of the 813 shared types to define nine superfamilies of strains (Mycobacterium africanum, Beijing, M. bovis, EAI, CAS, T, Haarlem, X, and LAM), 96.9% of the shared types received a label, showing the potential for automated labeling of M. tuberculosis families in well-defined phylogeographical families. Intercontinental matches of shared types among eight continents and subcontinents (Africa, North America, Central America, South America, Europe, the Middle East and Central Asia, and the Far East) are analyzed and discussed.

* Corresponding author. Mailing address: Unité de la Tuberculose et des Mycobactéries, Institut Pasteur de Guadeloupe, Morne Jolivière, BP 484, 97165 Pointe à Pitre-Cedex, Guadeloupe. Fax: 590 (590) 893 880. E-mail for Christophe Sola: csola{at}pasteur-guadeloupe.fr. E-mail for Nalin Rastogi: nrastogi{at}pasteur-guadeloupe.fr.

{dagger} This work is dedicated to the memories of Anne Devallois, who initiated the spoligotyping project in Guadeloupe in 1996 but died tragically at the age of 30 years, and Gerald Martin, coinvestigator, who also died tragically during the course of the present study.

Journal of Clinical Microbiology, May 2003, p. 1963-1970, Vol. 41, No. 5
0095-1137/03/$08.00+0     DOI: 10.1128/JCM.41.5.1963-1970.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



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