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Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage

Author

Listed:
  • Rene S. Hendriksen

    (Technical University of Denmark)

  • Patrick Munk

    (Technical University of Denmark)

  • Patrick Njage

    (Technical University of Denmark)

  • Bram Bunnik

    (University of Edinburgh)

  • Luke McNally

    (University of Edinburgh)

  • Oksana Lukjancenko

    (Technical University of Denmark)

  • Timo Röder

    (Technical University of Denmark)

  • David Nieuwenhuijse

    (Viroscience, Erasmus Medical Center)

  • Susanne Karlsmose Pedersen

    (Technical University of Denmark)

  • Jette Kjeldgaard

    (Technical University of Denmark)

  • Rolf S. Kaas

    (Technical University of Denmark)

  • Philip Thomas Lanken Conradsen Clausen

    (Technical University of Denmark)

  • Josef Korbinian Vogt

    (Technical University of Denmark)

  • Pimlapas Leekitcharoenphon

    (Technical University of Denmark)

  • Milou G. M. Schans

    (RIKILT Wageningen University and Research)

  • Tina Zuidema

    (RIKILT Wageningen University and Research)

  • Ana Maria Roda Husman

    (National Institute for Public Health and the Environment (RIVM))

  • Simon Rasmussen

    (Technical University of Denmark)

  • Bent Petersen

    (Technical University of Denmark)

  • Clara Amid

    (European Bioinformatics Institute)

  • Guy Cochrane

    (European Bioinformatics Institute)

  • Thomas Sicheritz-Ponten

    (AIMST University)

  • Heike Schmitt

    (National Institute for Public Health and the Environment (RIVM))

  • Jorge Raul Matheu Alvarez

    (World Health Organization)

  • Awa Aidara-Kane

    (World Health Organization)

  • Sünje J. Pamp

    (Technical University of Denmark)

  • Ole Lund

    (Technical University of Denmark)

  • Tine Hald

    (Technical University of Denmark)

  • Mark Woolhouse

    (University of Edinburgh)

  • Marion P. Koopmans

    (Viroscience, Erasmus Medical Center)

  • Håkan Vigre

    (Technical University of Denmark)

  • Thomas Nordahl Petersen

    (Technical University of Denmark)

  • Frank M. Aarestrup

    (Technical University of Denmark)

Abstract

Antimicrobial resistance (AMR) is a serious threat to global public health, but obtaining representative data on AMR for healthy human populations is difficult. Here, we use metagenomic analysis of untreated sewage to characterize the bacterial resistome from 79 sites in 60 countries. We find systematic differences in abundance and diversity of AMR genes between Europe/North-America/Oceania and Africa/Asia/South-America. Antimicrobial use data and bacterial taxonomy only explains a minor part of the AMR variation that we observe. We find no evidence for cross-selection between antimicrobial classes, or for effect of air travel between sites. However, AMR gene abundance strongly correlates with socio-economic, health and environmental factors, which we use to predict AMR gene abundances in all countries in the world. Our findings suggest that global AMR gene diversity and abundance vary by region, and that improving sanitation and health could potentially limit the global burden of AMR. We propose metagenomic analysis of sewage as an ethically acceptable and economically feasible approach for continuous global surveillance and prediction of AMR.

Suggested Citation

  • Rene S. Hendriksen & Patrick Munk & Patrick Njage & Bram Bunnik & Luke McNally & Oksana Lukjancenko & Timo Röder & David Nieuwenhuijse & Susanne Karlsmose Pedersen & Jette Kjeldgaard & Rolf S. Kaas & , 2019. "Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-08853-3
    DOI: 10.1038/s41467-019-08853-3
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    Cited by:

    1. Patrick Munk & Christian Brinch & Frederik Duus Møller & Thomas N. Petersen & Rene S. Hendriksen & Anne Mette Seyfarth & Jette S. Kjeldgaard & Christina Aaby Svendsen & Bram Bunnik & Fanny Berglund & , 2022. "Genomic analysis of sewage from 101 countries reveals global landscape of antimicrobial resistance," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    2. Ágnes Becsei & Alessandro Fuschi & Saria Otani & Ravi Kant & Ilja Weinstein & Patricia Alba & József Stéger & Dávid Visontai & Christian Brinch & Miranda Graaf & Claudia M. E. Schapendonk & Antonio Ba, 2024. "Time-series sewage metagenomics distinguishes seasonal, human-derived and environmental microbial communities potentially allowing source-attributed surveillance," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    3. Aguiar, Raphael & Keil, Roger & Wiktorowicz, Mary, 2024. "The urban political ecology of antimicrobial resistance: A critical lens on integrative governance," Social Science & Medicine, Elsevier, vol. 348(C).
    4. Zhenyan Zhang & Qi Zhang & Tingzhang Wang & Nuohan Xu & Tao Lu & Wenjie Hong & Josep Penuelas & Michael Gillings & Meixia Wang & Wenwen Gao & Haifeng Qian, 2022. "Assessment of global health risk of antibiotic resistance genes," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    5. Visanu Thamlikitkul & Surapee Tiengrim & Narisara Thamthaweechok & Preeyanuch Buranapakdee & Wilai Chiemchaisri, 2019. "Contamination by Antibiotic-Resistant Bacteria in Selected Environments in Thailand," IJERPH, MDPI, vol. 16(19), pages 1-11, October.
    6. Kihyun Lee & Sebastien Raguideau & Kimmo Sirén & Francesco Asnicar & Fabio Cumbo & Falk Hildebrand & Nicola Segata & Chang-Jun Cha & Christopher Quince, 2023. "Population-level impacts of antibiotic usage on the human gut microbiome," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    7. Qi Dang & Wei Zhang & Jiqing Liu & Liting Wang & Deli Wu & Dejin Wang & Zhendong Lei & Liang Tang, 2023. "Bias-free driven ion assisted photoelectrochemical system for sustainable wastewater treatment," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    8. Andrea Butcher & Jose A. Cañada & Salla Sariola, 2021. "How to make noncoherent problems more productive: Towards an AMR management plan for low resource livestock sectors," Palgrave Communications, Palgrave Macmillan, vol. 8(1), pages 1-10, December.
    9. Peter J. Diebold & Matthew W. Rhee & Qiaojuan Shi & Nguyen Vinh Trung & Fayaz Umrani & Sheraz Ahmed & Vandana Kulkarni & Prasad Deshpande & Mallika Alexander & Ngo Hoa & Nicholas A. Christakis & Najee, 2023. "Clinically relevant antibiotic resistance genes are linked to a limited set of taxa within gut microbiome worldwide," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

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