Global phylogeography and evolutionary history of Shigella dysenteriae type 1

Elisabeth Njamkepo; Nizar Fawal; Alicia Tran-Dien; Jane Hawkey; Nancy Strockbine; Claire Jenkins; Kaisar A Talukder; Raymond Bercion; Konstantin Kuleshov; Renáta Kolínská; Julie E Russell; Lidia Kaftyreva; Marie Accou-Demartin; Andreas Karas; Olivier Vandenberg; Alison E Mather; Carl J Mason; Andrew J Page; Thandavarayan Ramamurthy; Chantal Bizet; Andrzej Gamian; Isabelle Carle; Amy Gassama Sow; Christiane Bouchier; Astrid Louise Wester; Monique Lejay-Collin; Marie-Christine Fonkoua; Simon Le Hello; Martin J Blaser; Cecilia Jernberg; Corinne Ruckly; Audrey Mérens; Anne-Laure Page; Martin Aslett; Peter Roggentin; Angelika Fruth; Erick Denamur; Malabi Venkatesan; Hervé Bercovier; Ladaporn Bodhidatta; Chien-Shun Chiou; Dominique Clermont; Bianca Colonna; Svetlana Egorova; Gururaja P Pazhani; Analia V Ezernitchi; Ghislaine Guigon; Simon R Harris; Hidemasa Izumiya; Agnieszka Korzeniowska-Kowal; Anna Lutyńska; Malika Gouali; Francine Grimont; Céline Langendorf; Monika Marejková; Lorea A M Peterson; Guillermo Perez-Perez; Antoinette Ngandjio; Alexander Podkolzin; Erika Souche; Mariia Makarova; German A Shipulin; Changyun Ye; Helena Žemličková; Mária Herpay; Patrick A D Grimont; Julian Parkhill; Philippe Sansonetti; Kathryn E Holt; Sylvain Brisse; Nicholas R Thomson; François-Xavier Weill

doi:10.1038/NMICROBIOL.2016.27

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Global phylogeography and evolutionary history of Shigella dysenteriae type 1

Journal article

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Global phylogeography and evolutionary history of Shigella dysenteriae type 1

Elisabeth Njamkepo, Nizar Fawal, Alicia Tran-Dien, Jane Hawkey, Nancy Strockbine, Claire Jenkins, Kaisar A Talukder, Raymond Bercion, Konstantin Kuleshov, Renáta Kolínská, …

Nature microbiology, Vol.1(4), pp.16027-16027

03/21/2016

DOI: https://doi.org/10.1038/NMICROBIOL.2016.27

PMID: 27572446

Abstract

Drug Resistance, Bacterial

Dysentery, Bacillary - epidemiology

Dysentery, Bacillary - history

Dysentery, Bacillary - microbiology

Evolution, Molecular

Genome, Bacterial

History, 19th Century

History, 20th Century

History, 21st Century

Humans

Phylogeography

Sequence Analysis, DNA

Serogroup

Shigella dysenteriae - classification

Shigella dysenteriae - genetics

Shigella dysenteriae - isolation & purification

Global Health

Molecular Epidemiology

Together with plague, smallpox and typhus, epidemics of dysentery have been a major scourge of human populations for centuries(1). A previous genomic study concluded that Shigella dysenteriae type 1 (Sd1), the epidemic dysentery bacillus, emerged and spread worldwide after the First World War, with no clear pattern of transmission(2). This is not consistent with the massive cyclic dysentery epidemics reported in Europe during the eighteenth and nineteenth centuries(1,3,4) and the first isolation of Sd1 in Japan in 1897(5). Here, we report a whole-genome analysis of 331 Sd1 isolates from around the world, collected between 1915 and 2011, providing us with unprecedented insight into the historical spread of this pathogen. We show here that Sd1 has existed since at least the eighteenth century and that it swept the globe at the end of the nineteenth century, diversifying into distinct lineages associated with the First World War, Second World War and various conflicts or natural disasters across Africa, Asia and Central America. We also provide a unique historical perspective on the evolution of antibiotic resistance over a 100-year period, beginning decades before the antibiotic era, and identify a prevalent multiple antibiotic-resistant lineage in South Asia that was transmitted in several waves to Africa, where it caused severe outbreaks of disease.

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Title: Global phylogeography and evolutionary history of Shigella dysenteriae type 1
Creators: Elisabeth Njamkepo - Institut Pasteur, Unité des Bactéries Pathogènes Entériques, 75724 Paris Cedex 15, France
Nizar Fawal - Institut Pasteur, Unité des Bactéries Pathogènes Entériques, 75724 Paris Cedex 15, France
Alicia Tran-Dien - Institut Pasteur, Unité des Bactéries Pathogènes Entériques, 75724 Paris Cedex 15, France
Jane Hawkey - School of Agriculture and Veterinary Science, University of Melbourne, Parkville, Victoria 3010, Australia
Nancy Strockbine - Centers for Disease Control and Prevention, Escherichia and Shigella Reference Unit, Atlanta, Georgia 30333, USA
Claire Jenkins - Public Health England, Gastrointestinal Bacteria Reference Unit, Colindale NW9 5HT, UK
Kaisar A Talukder - icddr,b, Enteric and Food Microbiology Laboratory, Dhaka 1212, Bangladesh
Raymond Bercion - Institut Pasteur de Dakar, BP 220, Dakar, Senegal
Konstantin Kuleshov - Federal Budget Institute of Science, Central Research Institute for Epidemiology, Moscow 111123, Russia
Renáta Kolínská - Czech National Collection of Type Cultures (CNCTC), National Institute of Public Health, Prague 10, Czech Republic
Julie E Russell - Public Health England, National Collection of Type Cultures, Porton Down SP4 0JG, UK
Lidia Kaftyreva - Pasteur Institute of St Petersburg, St Petersburg 197101, Russia
Marie Accou-Demartin - Institut Pasteur, Unité des Bactéries Pathogènes Entériques, 75724 Paris Cedex 15, France
Andreas Karas - Department of Medical Microbiology, University of KwaZulu-Natal, Durban 4041, South Africa
Olivier Vandenberg - Environmental Health Research Centre, Public Health School, Université Libre de Bruxelles, 1070 Brussels, Belgium
Alison E Mather - Department of Veterinary Medicine, University of Cambridge, Cambridge CB3 0ES, UK
Carl J Mason - Armed Forces Research Institute of Medical Sciences (AFRIMS), Bangkok 10400, Thailand
Andrew J Page - Wellcome Trust Sanger Institute, Cambridge CB10 1SA, UK
Thandavarayan Ramamurthy - National Institute of Cholera and Enteric Diseases (NICED), Kolkata, West Bengal 700010, India
Chantal Bizet - Institut Pasteur, Collection de l'Institut Pasteur (CIP), 75724 Paris Cedex 15, France
Andrzej Gamian - Polish Collection of Microorganisms, Institute of Immunology and Experimental Therapy, 53-114 Wroclaw, Poland
Isabelle Carle - Institut Pasteur, Unité des Bactéries Pathogènes Entériques, 75724 Paris Cedex 15, France
Amy Gassama Sow - Institut Pasteur de Dakar, BP 220, Dakar, Senegal
Christiane Bouchier - Institut Pasteur, Plate-forme Génomique (PF1), 75724 Paris Cedex 15, France
Astrid Louise Wester - Department of Foodborne Infections, Norwegian Institute of Public Health, Nydalen 0403, Oslo, Norway
Monique Lejay-Collin - Institut Pasteur, Unité des Bactéries Pathogènes Entériques, 75724 Paris Cedex 15, France
Marie-Christine Fonkoua - Centre Pasteur du Cameroun, BP 1274, Yaoundé, Cameroon
Simon Le Hello - Institut Pasteur, Unité des Bactéries Pathogènes Entériques, 75724 Paris Cedex 15, France
Martin J Blaser - Departments of Medicine and Microbiology, New York University Langone Medical Center, New York, New York 10016, USA
Cecilia Jernberg - Public Health Agency of Sweden, 17182 Solna, Sweden
Corinne Ruckly - Institut Pasteur, Unité des Bactéries Pathogènes Entériques, 75724 Paris Cedex 15, France
Audrey Mérens - Biology Department and Infection Control Unit, Bégin Military Hospital, 94160 Saint-Mandé, France
Anne-Laure Page - Epicentre, 75011 Paris, France
Martin Aslett - Wellcome Trust Sanger Institute, Cambridge CB10 1SA, UK
Peter Roggentin - Institut für Hygiene und Umwelt, 20539 Hamburg, Germany
Angelika Fruth - Divison of Enteropathogenic Bacteria and Legionella, Robert Koch Institut, 38855 Wernigerode, Germany
Erick Denamur - INSERM, IAME, UMR 1137, Univ. Paris Diderot, IAME, UMR 1137, Sorbonne Paris Cité, 75018 Paris, France
Malabi Venkatesan - Bacterial Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland 20910, USA
Hervé Bercovier - Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem 91120, Israel
Ladaporn Bodhidatta - Armed Forces Research Institute of Medical Sciences (AFRIMS), Bangkok 10400, Thailand
Chien-Shun Chiou - Center of Research and Diagnostics, Centers for Disease Control, Taichung 40855, Taiwan
Dominique Clermont - Institut Pasteur, Collection de l'Institut Pasteur (CIP), 75724 Paris Cedex 15, France
Bianca Colonna - Istituto Pasteur-Fondazione Cenci Bolognetti, Dipartimento di Biologia e Biotecnologie C Darwin, Sapienza Università di Roma, 00185, Roma, Italy
Svetlana Egorova - Pasteur Institute of St Petersburg, St Petersburg 197101, Russia
Gururaja P Pazhani - National Institute of Cholera and Enteric Diseases (NICED), Kolkata, West Bengal 700010, India
Analia V Ezernitchi - Central Laboratories, Ministry of Health, Jerusalem 91342, Israel
Ghislaine Guigon - Institut Pasteur, Genotyping of Pathogens and Public Health Platform, 75724 Paris Cedex 15, France
Simon R Harris - Wellcome Trust Sanger Institute, Cambridge CB10 1SA, UK
Hidemasa Izumiya - Department of Bacteriology I, National Institute of Infectious Diseases, Tokyo, 162-8640, Japan
Agnieszka Korzeniowska-Kowal - Polish Collection of Microorganisms, Institute of Immunology and Experimental Therapy, 53-114 Wroclaw, Poland
Anna Lutyńska - Department of Sera and Vaccines Evaluation, National Institute of Public Health-National Institute of Hygiene, 00-791 Warsaw, Poland
Malika Gouali - Institut Pasteur, Unité des Bactéries Pathogènes Entériques, 75724 Paris Cedex 15, France
Francine Grimont - Institut Pasteur, Unité des Bactéries Pathogènes Entériques, 75724 Paris Cedex 15, France
Céline Langendorf - Epicentre, 75011 Paris, France
Monika Marejková - National Reference Laboratory for E. coli and Shigella, National Institute of Public Health, Prague 10, Czech Republic
Lorea A M Peterson - National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, Manitoba R3E 3R2, Canada
Guillermo Perez-Perez - Departments of Medicine and Microbiology, New York University Langone Medical Center, New York, New York 10016, USA
Antoinette Ngandjio - Centre Pasteur du Cameroun, BP 1274, Yaoundé, Cameroon
Alexander Podkolzin - Federal Budget Institute of Science, Central Research Institute for Epidemiology, Moscow 111123, Russia
Erika Souche - Institut Pasteur, Bioinformatics platform, 75724 Paris Cedex 15, France
Mariia Makarova - Pasteur Institute of St Petersburg, St Petersburg 197101, Russia
German A Shipulin - Federal Budget Institute of Science, Central Research Institute for Epidemiology, Moscow 111123, Russia
Changyun Ye - State Key Laboratory of Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, China CDC, Beijing 102206, China
Helena Žemličková - Department of Clinical Microbiology, Faculty of Medicine and University Hospital, Charles University, 500 05, Hradec Kralove, Czech Republic
Mária Herpay - Hungarian National Collection of Medical Bacteria, National Center for Epidemiology, H-1097 Budapest, Hungary
Patrick A D Grimont - Institut Pasteur, Unité des Bactéries Pathogènes Entériques, 75724 Paris Cedex 15, France
Julian Parkhill - Wellcome Trust Sanger Institute, Cambridge CB10 1SA, UK
Philippe Sansonetti - Institut Pasteur, Unité de Pathogénie Microbienne Moléculaire, 75724 Paris Cedex 15, France
Kathryn E Holt - Department of Biochemistry and Molecular Biology, Bio21 Molecular Science and Biotechnology Institute, University of Melbourne, Parkville, Victoria 3010, Australia
Sylvain Brisse - CNRS, UMR 3525, 75015 Paris, France
Nicholas R Thomson - London School of Hygiene and Tropical Medicine, London WC1E 7HT, UK
François-Xavier Weill - Wellcome Trust Sanger Institute, Cambridge CB10 1SA, UK
Publication Details: Nature microbiology, Vol.1(4), pp.16027-16027
Date published: 03/21/2016
Academic Unit: Center for Advanced Biotechnology and Medicine
Language: English
Resource Type: Journal article
Identifiers: 991031664415204646