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Transcontinental spread and evolution of Mycobacterium tuberculosis W148 European/Russian clade toward extensively drug resistant tuberculosis

Author

Listed:
  • Matthias Merker

    (Research Center Borstel
    Partner site Hamburg-Lübeck-Borstel-Riems
    Research Center Borstel)

  • Jean-Philippe Rasigade

    (EPHE, PSL University
    Muséum national d’Histoire naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles
    Université Lyon 1, ENS de Lyon)

  • Maxime Barbier

    (EPHE, PSL University
    Muséum national d’Histoire naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles)

  • Helen Cox

    (University of Cape Town)

  • Silke Feuerriegel

    (Research Center Borstel
    Partner site Hamburg-Lübeck-Borstel-Riems)

  • Thomas A. Kohl

    (Research Center Borstel
    Partner site Hamburg-Lübeck-Borstel-Riems)

  • Egor Shitikov

    (Federal Research and Clinical Centre of Physical-Chemical Medicine)

  • Kadri Klaos

    (SA TUH United Laboratories, Mycobacteriology)

  • Cyril Gaudin

    (Genoscreen)

  • Rudy Antoine

    (Univ. Lille, CNRS, Inserm, CHU Lille, Institut Pasteur de Lille, U1019 - UMR 9017 - CIIL - Centre d’Infection et d’Immunité de Lille)

  • Roland Diel

    (Schleswig-Holstein University Hospital
    Lung Clinic Grosshansdorf, German Center for Lung Research (DZL), Airway Research Center North (ARCN))

  • Sonia Borrell

    (Swiss Tropical and Public Health Institute
    University of Basel)

  • Sebastien Gagneux

    (Swiss Tropical and Public Health Institute
    University of Basel)

  • Vladyslav Nikolayevskyy

    (Imperial College London)

  • Sönke Andres

    (Research Center Borstel)

  • Valeriu Crudu

    (National TB Reference Laboratory, Institute of Phthisiopneumology)

  • Philip Supply

    (Univ. Lille, CNRS, Inserm, CHU Lille, Institut Pasteur de Lille, U1019 - UMR 9017 - CIIL - Centre d’Infection et d’Immunité de Lille)

  • Stefan Niemann

    (Research Center Borstel
    Partner site Hamburg-Lübeck-Borstel-Riems)

  • Thierry Wirth

    (EPHE, PSL University
    Muséum national d’Histoire naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles)

Abstract

Transmission-driven multi-/extensively drug resistant (M/XDR) tuberculosis (TB) is the largest single contributor to human mortality due to antimicrobial resistance. A few major clades of the Mycobacterium tuberculosis complex belonging to lineage 2, responsible for high prevalence of MDR-TB in Eurasia, show outstanding transnational distributions. Here, we determined factors underlying the emergence and epidemic spread of the W148 clade by genome sequencing and Bayesian demogenetic analyses of 720 isolates from 23 countries. We dated a common ancestor around 1963 and identified two successive epidemic expansions in the late 1980s and late 1990s, coinciding with major socio-economic changes in the post-Soviet Era. These population expansions favored accumulation of resistance mutations to up to 11 anti-TB drugs, with MDR evolving toward additional resistances to fluoroquinolones and second-line injectable drugs within 20 years on average. Timescaled haplotypic density analysis revealed that widespread acquisition of compensatory mutations was associated with transmission success of XDR strains. Virtually all W148 strains harbored a hypervirulence-associated ppe38 gene locus, and incipient recurrent emergence of prpR mutation-mediated drug tolerance was detected. The outstanding genetic arsenal of this geographically widespread M/XDR strain clade represents a “perfect storm” that jeopardizes the successful introduction of new anti-M/XDR-TB antibiotic regimens.

Suggested Citation

  • Matthias Merker & Jean-Philippe Rasigade & Maxime Barbier & Helen Cox & Silke Feuerriegel & Thomas A. Kohl & Egor Shitikov & Kadri Klaos & Cyril Gaudin & Rudy Antoine & Roland Diel & Sonia Borrell & S, 2022. "Transcontinental spread and evolution of Mycobacterium tuberculosis W148 European/Russian clade toward extensively drug resistant tuberculosis," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32455-1
    DOI: 10.1038/s41467-022-32455-1
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    References listed on IDEAS

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    1. Maha R. Farhat & Luca Freschi & Roger Calderon & Thomas Ioerger & Matthew Snyder & Conor J. Meehan & Bouke de Jong & Leen Rigouts & Alex Sloutsky & Devinder Kaur & Shamil Sunyaev & Dick van Soolingen , 2019. "GWAS for quantitative resistance phenotypes in Mycobacterium tuberculosis reveals resistance genes and regulatory regions," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    2. Vegard Eldholm & Johana Monteserin & Adrien Rieux & Beatriz Lopez & Benjamin Sobkowiak & Viviana Ritacco & Francois Balloux, 2015. "Four decades of transmission of a multidrug-resistant Mycobacterium tuberculosis outbreak strain," Nature Communications, Nature, vol. 6(1), pages 1-9, November.
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    1. Melanie H. Chitwood & Caroline Colijn & Chongguang Yang & Valeriu Crudu & Nelly Ciobanu & Alexandru Codreanu & Jaehee Kim & Isabel Rancu & Kyu Rhee & Ted Cohen & Benjamin Sobkowiak, 2024. "The recent rapid expansion of multidrug resistant Ural lineage Mycobacterium tuberculosis in Moldova," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    2. Xin Fan & Rong-Chen Dai & Shu Zhang & Yuan-Yuan Geng & Mei Kang & Da-Wen Guo & Ya-Ning Mei & Yu-Hong Pan & Zi-Yong Sun & Ying-Chun Xu & Jie Gong & Meng Xiao, 2023. "Tandem gene duplications contributed to high-level azole resistance in a rapidly expanding Candida tropicalis population," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    3. Chloé Loiseau & Etthel M. Windels & Sebastian M. Gygli & Levan Jugheli & Nino Maghradze & Daniela Brites & Amanda Ross & Galo Goig & Miriam Reinhard & Sonia Borrell & Andrej Trauner & Anna Dötsch & Ru, 2023. "The relative transmission fitness of multidrug-resistant Mycobacterium tuberculosis in a drug resistance hotspot," Nature Communications, Nature, vol. 14(1), pages 1-11, December.

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