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

Rene S. Hendriksen, Patrick Munk, Patrick Murigu Kamau Njage, Bram van Bunnik, Luke McNally, Oksana Lukjancenko, Timo Röder, David Nieuwenhuijse, Susanne Karlsmose Pedersen, Jette Sejer Kjeldgaard, Rolf Sommer Kaas, Philip Thomas Lanken Conradsen Clausen, Josef Korbinian Vogt, Pimlapas Leekitcharoenphon, Milou G M van de Schans, Tina Zuidema, Ana Maria de Roda Husman, Simon Rasmussen, Bent Petersen, Sewage Surveillance project consortium Global & 14 others Clara Amid, Guy Cochrane, Thomas Sicheritz-Pontén, Heike Schmitt, Jorge Raul Matheu Alvarez, Awa Aidara-Kane, Sünje Johanna Pamp, Ole Lund, Tine Hald, Mark Woolhouse, Marion P Koopmans, Håkan Vigre, Thomas Nordahl Petersen, Frank Møller Aarestrup*

*Corresponding author for this work

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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.
Original languageEnglish
Article number1124
JournalNature Communications
Volume10
Number of pages12
ISSN2041-1723
DOIs
Publication statusPublished - 2019

Keywords

  • Antimicrobial resistance
  • Ecological epidemiology
  • Metagenomics
  • Water microbiology

Cite this

Hendriksen, Rene S. ; Munk, Patrick ; Njage, Patrick Murigu Kamau ; van Bunnik, Bram ; McNally, Luke ; Lukjancenko, Oksana ; Röder, Timo ; Nieuwenhuijse, David ; Karlsmose Pedersen, Susanne ; Kjeldgaard, Jette Sejer ; Kaas, Rolf Sommer ; Clausen, Philip Thomas Lanken Conradsen ; Vogt, Josef Korbinian ; Leekitcharoenphon, Pimlapas ; van de Schans, Milou G M ; Zuidema, Tina ; de Roda Husman, Ana Maria ; Rasmussen, Simon ; Petersen, Bent ; Global, Sewage Surveillance project consortium ; Amid, Clara ; Cochrane, Guy ; Sicheritz-Pontén, Thomas ; Schmitt, Heike ; Alvarez, Jorge Raul Matheu ; Aidara-Kane, Awa ; Pamp, Sünje Johanna ; Lund, Ole ; Hald, Tine ; Woolhouse, Mark ; Koopmans, Marion P ; Vigre, Håkan ; Petersen, Thomas Nordahl ; Aarestrup, Frank Møller. / Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage. In: Nature Communications. 2019 ; Vol. 10.
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title = "Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage",
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.",
keywords = "Antimicrobial resistance, Ecological epidemiology, Metagenomics, Water microbiology",
author = "Hendriksen, {Rene S.} and Patrick Munk and Njage, {Patrick Murigu Kamau} and {van Bunnik}, Bram and Luke McNally and Oksana Lukjancenko and Timo R{\"o}der and David Nieuwenhuijse and {Karlsmose Pedersen}, Susanne and Kjeldgaard, {Jette Sejer} and Kaas, {Rolf Sommer} and Clausen, {Philip Thomas Lanken Conradsen} and Vogt, {Josef Korbinian} and Pimlapas Leekitcharoenphon and {van de Schans}, {Milou G M} and Tina Zuidema and {de Roda Husman}, {Ana Maria} and Simon Rasmussen and Bent Petersen and Global, {Sewage Surveillance project consortium} and Clara Amid and Guy Cochrane and Thomas Sicheritz-Pont{\'e}n and Heike Schmitt and Alvarez, {Jorge Raul Matheu} and Awa Aidara-Kane and Pamp, {S{\"u}nje Johanna} and Ole Lund and Tine Hald and Mark Woolhouse and Koopmans, {Marion P} and H{\aa}kan Vigre and Petersen, {Thomas Nordahl} and Aarestrup, {Frank M{\o}ller}",
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doi = "10.1038/s41467-019-08853-3",
language = "English",
volume = "10",
journal = "Nature Communications",
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Hendriksen, RS, Munk, P, Njage, PMK, van Bunnik, B, McNally, L, Lukjancenko, O, Röder, T, Nieuwenhuijse, D, Karlsmose Pedersen, S, Kjeldgaard, JS, Kaas, RS, Clausen, PTLC, Vogt, JK, Leekitcharoenphon, P, van de Schans, MGM, Zuidema, T, de Roda Husman, AM, Rasmussen, S, Petersen, B, Global, SSPC, Amid, C, Cochrane, G, Sicheritz-Pontén, T, Schmitt, H, Alvarez, JRM, Aidara-Kane, A, Pamp, SJ, Lund, O, Hald, T, Woolhouse, M, Koopmans, MP, Vigre, H, Petersen, TN & Aarestrup, FM 2019, 'Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage', Nature Communications, vol. 10, 1124. https://doi.org/10.1038/s41467-019-08853-3

Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage. / Hendriksen, Rene S.; Munk, Patrick; Njage, Patrick Murigu Kamau; van Bunnik, Bram; McNally, Luke; Lukjancenko, Oksana; Röder, Timo; Nieuwenhuijse, David; Karlsmose Pedersen, Susanne; Kjeldgaard, Jette Sejer; Kaas, Rolf Sommer; Clausen, Philip Thomas Lanken Conradsen; Vogt, Josef Korbinian; Leekitcharoenphon, Pimlapas; van de Schans, Milou G M; Zuidema, Tina; de Roda Husman, Ana Maria; Rasmussen, Simon; Petersen, Bent; Global, Sewage Surveillance project consortium; Amid, Clara; Cochrane, Guy; Sicheritz-Pontén, Thomas; Schmitt, Heike; Alvarez, Jorge Raul Matheu; Aidara-Kane, Awa; Pamp, Sünje Johanna; Lund, Ole; Hald, Tine; Woolhouse, Mark; Koopmans, Marion P; Vigre, Håkan; Petersen, Thomas Nordahl; Aarestrup, Frank Møller.

In: Nature Communications, Vol. 10, 1124, 2019.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage

AU - Hendriksen, Rene S.

AU - Munk, Patrick

AU - Njage, Patrick Murigu Kamau

AU - van Bunnik, Bram

AU - McNally, Luke

AU - Lukjancenko, Oksana

AU - Röder, Timo

AU - Nieuwenhuijse, David

AU - Karlsmose Pedersen, Susanne

AU - Kjeldgaard, Jette Sejer

AU - Kaas, Rolf Sommer

AU - Clausen, Philip Thomas Lanken Conradsen

AU - Vogt, Josef Korbinian

AU - Leekitcharoenphon, Pimlapas

AU - van de Schans, Milou G M

AU - Zuidema, Tina

AU - de Roda Husman, Ana Maria

AU - Rasmussen, Simon

AU - Petersen, Bent

AU - Global, Sewage Surveillance project consortium

AU - Amid, Clara

AU - Cochrane, Guy

AU - Sicheritz-Pontén, Thomas

AU - Schmitt, Heike

AU - Alvarez, Jorge Raul Matheu

AU - Aidara-Kane, Awa

AU - Pamp, Sünje Johanna

AU - Lund, Ole

AU - Hald, Tine

AU - Woolhouse, Mark

AU - Koopmans, Marion P

AU - Vigre, Håkan

AU - Petersen, Thomas Nordahl

AU - Aarestrup, Frank Møller

PY - 2019

Y1 - 2019

N2 - 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.

AB - 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.

KW - Antimicrobial resistance

KW - Ecological epidemiology

KW - Metagenomics

KW - Water microbiology

U2 - 10.1038/s41467-019-08853-3

DO - 10.1038/s41467-019-08853-3

M3 - Journal article

VL - 10

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

M1 - 1124

ER -