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Horizontal antimicrobial resistance transfer drives epidemics of multiple Shigella species

Author

Listed:
  • Kate S. Baker

    (University of Liverpool
    Wellcome Trust Sanger Institute)

  • Timothy J. Dallman

    (Gastrointestinal Bacterial Reference Unit, National Infection Service, Public Health England)

  • Nigel Field

    (Institute for Global Health, UCL)

  • Tristan Childs

    (Public Health England)

  • Holly Mitchell

    (Institute for Global Health, UCL)

  • Martin Day

    (Gastrointestinal Bacterial Reference Unit, National Infection Service, Public Health England)

  • François-Xavier Weill

    (Unité des Bactéries Pathogènes Entériques)

  • Sophie Lefèvre

    (Unité des Bactéries Pathogènes Entériques)

  • Mathieu Tourdjman

    (the French Public Health Agency)

  • Gwenda Hughes

    (Public Health England)

  • Claire Jenkins

    (Gastrointestinal Bacterial Reference Unit, National Infection Service, Public Health England)

  • Nicholas Thomson

    (Wellcome Trust Sanger Institute
    London School of Hygiene and Tropical Medicine)

Abstract

Horizontal gene transfer has played a role in developing the global public health crisis of antimicrobial resistance (AMR). However, the dynamics of AMR transfer through bacterial populations and its direct impact on human disease is poorly elucidated. Here, we study parallel epidemic emergences of multiple Shigella species, a priority AMR organism, in men who have sex with men to gain insight into AMR emergence and spread. Using genomic epidemiology, we show that repeated horizontal transfer of a single AMR plasmid among Shigella enhanced existing and facilitated new epidemics. These epidemic patterns contrasted with slighter, slower increases in disease caused by organisms with vertically inherited (chromosomally encoded) AMR. This demonstrates that horizontal transfer of AMR directly affects epidemiological outcomes of globally important AMR pathogens and highlights the need for integration of genomic analyses into all areas of AMR research, surveillance and management.

Suggested Citation

  • Kate S. Baker & Timothy J. Dallman & Nigel Field & Tristan Childs & Holly Mitchell & Martin Day & François-Xavier Weill & Sophie Lefèvre & Mathieu Tourdjman & Gwenda Hughes & Claire Jenkins & Nicholas, 2018. "Horizontal antimicrobial resistance transfer drives epidemics of multiple Shigella species," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-03949-8
    DOI: 10.1038/s41467-018-03949-8
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    Cited by:

    1. Shaofu Qiu & Kangkang Liu & Chaojie Yang & Ying Xiang & Kaiyuan Min & Kunpeng Zhu & Hongbo Liu & Xinying Du & Mingjuan Yang & Ligui Wang & Yong Sun & Haijian Zhou & Muti Mahe & Jiayong Zhao & Shijun L, 2022. "A Shigella sonnei clone with extensive drug resistance associated with waterborne outbreaks in China," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. Sophie Lefèvre & Elisabeth Njamkepo & Sarah Feldman & Corinne Ruckly & Isabelle Carle & Monique Lejay-Collin & Laëtitia Fabre & Iman Yassine & Lise Frézal & Maria Pardos de la Gandara & Arnaud Fontane, 2023. "Rapid emergence of extensively drug-resistant Shigella sonnei in France," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    3. George E. Stenhouse & Karen H. Keddy & Rebecca J. Bengtsson & Neil Hall & Anthony M. Smith & Juno Thomas & Miren Iturriza-Gómara & Kate S. Baker, 2023. "The genomic epidemiology of shigellosis in South Africa," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Vincenzo Torraca & Myrsini Kaforou & Jayne Watson & Gina M Duggan & Hazel Guerrero-Gutierrez & Sina Krokowski & Michael Hollinshead & Thomas B Clarke & Rafal J Mostowy & Gillian S Tomlinson & Vanessa , 2019. "Shigella sonnei infection of zebrafish reveals that O-antigen mediates neutrophil tolerance and dysentery incidence," PLOS Pathogens, Public Library of Science, vol. 15(12), pages 1-26, December.
    5. Lewis C. E. Mason & David R. Greig & Lauren A. Cowley & Sally R. Partridge & Elena Martinez & Grace A. Blackwell & Charlotte E. Chong & P. Malaka Silva & Rebecca J. Bengtsson & Jenny L. Draper & Andre, 2023. "The evolution and international spread of extensively drug resistant Shigella sonnei," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    6. Ying Xiang & Kunpeng Zhu & Kaiyuan Min & Yaowen Zhang & Jiangfeng Liu & Kangkang Liu & Yiran Han & Xinge Li & Xinying Du & Xin Wang & Ying Huang & Xinping Li & Yuqian Peng & Chaojie Yang & Hongbo Liu , 2024. "Characterization of a Salmonella enterica serovar Typhimurium lineage with rough colony morphology and multidrug resistance," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    7. Iman Yassine & Sophie Lefèvre & Elisabeth E. Hansen & Corinne Ruckly & Isabelle Carle & Monique Lejay-Collin & Laëtitia Fabre & Rayane Rafei & Dominique Clermont & Maria Pardos Gandara & Fouad Dabbous, 2022. "Population structure analysis and laboratory monitoring of Shigella by core-genome multilocus sequence typing," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

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