Abstract

Antimicrobial resistance (AMR) is a global threat. A better understanding of how antibiotic use and between-ward patient transfers (or connectivity) impact population-level AMR in hospital networks can help optimize antibiotic stewardship and infection control strategies. Here, we used a metapopulation framework to explain variations in the incidence of infections caused by 7 major bacterial species and their drug-resistant variants in a network of 357 hospital wards. We found that ward-level antibiotic consumption volume had a stronger influence on the incidence of the more resistant pathogens, while connectivity had the most influence on hospital-endemic species and carbapenem-resistant pathogens. Piperacillin-tazobactam consumption was the strongest predictor of the cumulative incidence of infections resistant to empirical sepsis therapy. Our data provide evidence that both antibiotic use and connectivity measurably influence hospital AMR. Finally, we provide a ranking of key antibiotics by their estimated population-level impact on AMR that might help inform antimicrobial stewardship strategies.

Data availability

All data and software code that support the findings of this study are available at: https://github.com/rasigadelab/metapop.

Article and author information

Author details

  1. Julie Teresa Shapiro

    CIRI INSERM U1111, University of Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Gilles Leboucher

    Département de Pharmacie, Hospices Civils de Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7043-9834
  3. Anne-Florence Myard-Dury

    Pôle de Santé Publique, Département d'Information Médicale, Hospices Civils de Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Pascale Girardo

    Institut des Agents Infectieux, Hospices Civils de Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Anatole Luzzati

    Institut des Agents Infectieux, Hospices Civils de Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Melissa Mary

    Institut des Agents Infectieux, Hospices Civils de Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Jean-François Sauzon

    Institut des Agents Infectieux, Hospices Civils de Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Bénédicte Lafay

    Laboratoire de Biométrie et Biologie Evolutive, CNRS, Villeurbanne, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5783-5269
  9. Olivier Dauwalder

    Institut des Agents Infectieux, Hospices Civils de Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  10. Frederic Laurent

    CIRI INSERM U1111, University of Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  11. Gerard Lina

    CIRI INSERM U1111, University of Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  12. Christian Chidiac

    Service des Maladies Infectieuses et Tropicales, Hospices Civils de Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  13. Sandrine Couray-Targe

    Pôle de Santé Publique, Département d'Information Médicale, Hospices Civils de Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  14. François Vandenesch

    CIRI INSERM U1111, University of Lyon, Lyon, France
    Competing interests
    The authors declare that no competing interests exist.
  15. Jean-Pierre Flandrois

    Laboratoire de Biométrie et Biologie Evolutive, CNRS, Villeurbanne, France
    Competing interests
    The authors declare that no competing interests exist.
  16. Jean-Philippe Rasigade

    CIRI INSERM U1111, University of Lyon, Lyon, France
    For correspondence
    jean-philippe.rasigade@univ-lyon1.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8264-0452

Funding

Fondation Innovations en Infectiologie (R18037CC)

  • Jean-Philippe Rasigade

French Laboratory of Excellence project ECOFECT (ANR-11-LABX-0048)

  • Julie Teresa Shapiro
  • Gilles Leboucher
  • François Vandenesch
  • Jean-Philippe Rasigade

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Ben S Cooper, Mahidol University, Thailand

Publication history

  1. Received: December 30, 2019
  2. Accepted: October 12, 2020
  3. Accepted Manuscript published: October 27, 2020 (version 1)
  4. Version of Record published: November 26, 2020 (version 2)

Copyright

© 2020, Shapiro et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Julie Teresa Shapiro
  2. Gilles Leboucher
  3. Anne-Florence Myard-Dury
  4. Pascale Girardo
  5. Anatole Luzzati
  6. Melissa Mary
  7. Jean-François Sauzon
  8. Bénédicte Lafay
  9. Olivier Dauwalder
  10. Frederic Laurent
  11. Gerard Lina
  12. Christian Chidiac
  13. Sandrine Couray-Targe
  14. François Vandenesch
  15. Jean-Pierre Flandrois
  16. Jean-Philippe Rasigade
(2020)
Metapopulation ecology links antibiotic resistance, consumption, and patient transfers in a network of hospital wards
eLife 9:e54795.
https://doi.org/10.7554/eLife.54795

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