Abundance and diversity of the faecal resistome in slaughter pigs and broilers in nine European countries

Patrick Munk, Berith Elkær Knudsen, Oksana Lukjacenko, Ana Sofia Ribeiro Duarte, Liese Van Gompel, Roosmarijn E.C. Luiken, Lidwien A.M. Smit, Heike Schmitt, Alejandro Dorado Garcia, Rasmus Borup Hansen, Thomas Nordahl Petersen, Alex Bossers, Etienne Ruppé, Haitske Graveland, Alieda van Essen, Bruno Gonzalez-Zorn, Gabriel Moyano, Pascal Sanders, Claire Chauvin, Julie David & 21 others Antonio Battisti, Andrea Caprioli, Jeroen Dewulf, Thomas Blaha, Katharina Wadepohl, Maximiliane Brandt, Dariusz Wasyl, Magdalena Skarzyńska, Magdalena Zajac, Hristo Daskalov, Helmut W. Saatkamp, Katharina D.C. Stärk, Ole Lund, Tine Hald, Sünje Johanna Pamp, Håkan Vigre, Dick Heederik, Jaap A. Wagenaar, Dik Mevius, Frank Møller Aarestrup*, EFFORT Group

*Corresponding author for this work

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Abstract

Antimicrobial resistance (AMR) in bacteria and associated human morbidity and mortality is increasing. The use of antimicrobials in livestock selects for AMR that can subsequently be transferred to humans. This flow of AMR between reservoirs demands surveillance in livestock and in humans. We quantified and characterized the acquired resistance gene pools (resistomes) of 181 pig and 178 poultry farms from nine European countries, sequencing more than 5,000 Gb of DNA using shotgun metagenomics. We quantified acquired AMR using the ResFinder database and a second database constructed for this study, consisting of AMR genes identified through screening environmental DNA. The pig and poultry resistomes were very different in abundance and composition. There was a significant country effect on the resistomes, more so in pigs than in poultry. We found higher AMR loads in pigs, whereas poultry resistomes were more diverse. We detected several recently described, critical AMR genes, including mcr-1 and optrA, the abundance of which differed both between host species and between countries. We found that the total acquired AMR level was associated with the overall country-specific antimicrobial usage in livestock and that countries with comparable usage patterns had similar resistomes. However, functionally determined AMR genes were not associated with total drug use.

Original languageEnglish
JournalNature Microbiology
Volume3
Issue number8
Pages (from-to)898-908
ISSN2058-5276
DOIs
Publication statusPublished - 1 Aug 2018

Cite this

Munk, Patrick ; Knudsen, Berith Elkær ; Lukjacenko, Oksana ; Duarte, Ana Sofia Ribeiro ; Van Gompel, Liese ; Luiken, Roosmarijn E.C. ; Smit, Lidwien A.M. ; Schmitt, Heike ; Garcia, Alejandro Dorado ; Hansen, Rasmus Borup ; Petersen, Thomas Nordahl ; Bossers, Alex ; Ruppé, Etienne ; Graveland, Haitske ; van Essen, Alieda ; Gonzalez-Zorn, Bruno ; Moyano, Gabriel ; Sanders, Pascal ; Chauvin, Claire ; David, Julie ; Battisti, Antonio ; Caprioli, Andrea ; Dewulf, Jeroen ; Blaha, Thomas ; Wadepohl, Katharina ; Brandt, Maximiliane ; Wasyl, Dariusz ; Skarzyńska, Magdalena ; Zajac, Magdalena ; Daskalov, Hristo ; Saatkamp, Helmut W. ; Stärk, Katharina D.C. ; Lund, Ole ; Hald, Tine ; Pamp, Sünje Johanna ; Vigre, Håkan ; Heederik, Dick ; Wagenaar, Jaap A. ; Mevius, Dik ; Møller Aarestrup, Frank ; EFFORT Group. / Abundance and diversity of the faecal resistome in slaughter pigs and broilers in nine European countries. In: Nature Microbiology. 2018 ; Vol. 3, No. 8. pp. 898-908.
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title = "Abundance and diversity of the faecal resistome in slaughter pigs and broilers in nine European countries",
abstract = "Antimicrobial resistance (AMR) in bacteria and associated human morbidity and mortality is increasing. The use of antimicrobials in livestock selects for AMR that can subsequently be transferred to humans. This flow of AMR between reservoirs demands surveillance in livestock and in humans. We quantified and characterized the acquired resistance gene pools (resistomes) of 181 pig and 178 poultry farms from nine European countries, sequencing more than 5,000 Gb of DNA using shotgun metagenomics. We quantified acquired AMR using the ResFinder database and a second database constructed for this study, consisting of AMR genes identified through screening environmental DNA. The pig and poultry resistomes were very different in abundance and composition. There was a significant country effect on the resistomes, more so in pigs than in poultry. We found higher AMR loads in pigs, whereas poultry resistomes were more diverse. We detected several recently described, critical AMR genes, including mcr-1 and optrA, the abundance of which differed both between host species and between countries. We found that the total acquired AMR level was associated with the overall country-specific antimicrobial usage in livestock and that countries with comparable usage patterns had similar resistomes. However, functionally determined AMR genes were not associated with total drug use.",
author = "Patrick Munk and Knudsen, {Berith Elk{\ae}r} and Oksana Lukjacenko and Duarte, {Ana Sofia Ribeiro} and {Van Gompel}, Liese and Luiken, {Roosmarijn E.C.} and Smit, {Lidwien A.M.} and Heike Schmitt and Garcia, {Alejandro Dorado} and Hansen, {Rasmus Borup} and Petersen, {Thomas Nordahl} and Alex Bossers and Etienne Rupp{\'e} and Haitske Graveland and {van Essen}, Alieda and Bruno Gonzalez-Zorn and Gabriel Moyano and Pascal Sanders and Claire Chauvin and Julie David and Antonio Battisti and Andrea Caprioli and Jeroen Dewulf and Thomas Blaha and Katharina Wadepohl and Maximiliane Brandt and Dariusz Wasyl and Magdalena Skarzyńska and Magdalena Zajac and Hristo Daskalov and Saatkamp, {Helmut W.} and St{\"a}rk, {Katharina D.C.} and Ole Lund and Tine Hald and Pamp, {S{\"u}nje Johanna} and H{\aa}kan Vigre and Dick Heederik and Wagenaar, {Jaap A.} and Dik Mevius and {M{\o}ller Aarestrup}, Frank and {EFFORT Group}",
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Munk, P, Knudsen, BE, Lukjacenko, O, Duarte, ASR, Van Gompel, L, Luiken, REC, Smit, LAM, Schmitt, H, Garcia, AD, Hansen, RB, Petersen, TN, Bossers, A, Ruppé, E, Graveland, H, van Essen, A, Gonzalez-Zorn, B, Moyano, G, Sanders, P, Chauvin, C, David, J, Battisti, A, Caprioli, A, Dewulf, J, Blaha, T, Wadepohl, K, Brandt, M, Wasyl, D, Skarzyńska, M, Zajac, M, Daskalov, H, Saatkamp, HW, Stärk, KDC, Lund, O, Hald, T, Pamp, SJ, Vigre, H, Heederik, D, Wagenaar, JA, Mevius, D, Møller Aarestrup, F & EFFORT Group 2018, 'Abundance and diversity of the faecal resistome in slaughter pigs and broilers in nine European countries', Nature Microbiology, vol. 3, no. 8, pp. 898-908. https://doi.org/10.1038/s41564-018-0192-9

Abundance and diversity of the faecal resistome in slaughter pigs and broilers in nine European countries. / Munk, Patrick; Knudsen, Berith Elkær; Lukjacenko, Oksana; Duarte, Ana Sofia Ribeiro; Van Gompel, Liese; Luiken, Roosmarijn E.C.; Smit, Lidwien A.M.; Schmitt, Heike; Garcia, Alejandro Dorado; Hansen, Rasmus Borup; Petersen, Thomas Nordahl; Bossers, Alex; Ruppé, Etienne; Graveland, Haitske; van Essen, Alieda; Gonzalez-Zorn, Bruno; Moyano, Gabriel; Sanders, Pascal; Chauvin, Claire; David, Julie; Battisti, Antonio; Caprioli, Andrea; Dewulf, Jeroen; Blaha, Thomas; Wadepohl, Katharina; Brandt, Maximiliane; Wasyl, Dariusz; Skarzyńska, Magdalena; Zajac, Magdalena; Daskalov, Hristo; Saatkamp, Helmut W.; Stärk, Katharina D.C.; Lund, Ole; Hald, Tine; Pamp, Sünje Johanna; Vigre, Håkan; Heederik, Dick; Wagenaar, Jaap A.; Mevius, Dik; Møller Aarestrup, Frank ; EFFORT Group.

In: Nature Microbiology, Vol. 3, No. 8, 01.08.2018, p. 898-908.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Abundance and diversity of the faecal resistome in slaughter pigs and broilers in nine European countries

AU - Munk, Patrick

AU - Knudsen, Berith Elkær

AU - Lukjacenko, Oksana

AU - Duarte, Ana Sofia Ribeiro

AU - Van Gompel, Liese

AU - Luiken, Roosmarijn E.C.

AU - Smit, Lidwien A.M.

AU - Schmitt, Heike

AU - Garcia, Alejandro Dorado

AU - Hansen, Rasmus Borup

AU - Petersen, Thomas Nordahl

AU - Bossers, Alex

AU - Ruppé, Etienne

AU - Graveland, Haitske

AU - van Essen, Alieda

AU - Gonzalez-Zorn, Bruno

AU - Moyano, Gabriel

AU - Sanders, Pascal

AU - Chauvin, Claire

AU - David, Julie

AU - Battisti, Antonio

AU - Caprioli, Andrea

AU - Dewulf, Jeroen

AU - Blaha, Thomas

AU - Wadepohl, Katharina

AU - Brandt, Maximiliane

AU - Wasyl, Dariusz

AU - Skarzyńska, Magdalena

AU - Zajac, Magdalena

AU - Daskalov, Hristo

AU - Saatkamp, Helmut W.

AU - Stärk, Katharina D.C.

AU - Lund, Ole

AU - Hald, Tine

AU - Pamp, Sünje Johanna

AU - Vigre, Håkan

AU - Heederik, Dick

AU - Wagenaar, Jaap A.

AU - Mevius, Dik

AU - Møller Aarestrup, Frank

AU - EFFORT Group

PY - 2018/8/1

Y1 - 2018/8/1

N2 - Antimicrobial resistance (AMR) in bacteria and associated human morbidity and mortality is increasing. The use of antimicrobials in livestock selects for AMR that can subsequently be transferred to humans. This flow of AMR between reservoirs demands surveillance in livestock and in humans. We quantified and characterized the acquired resistance gene pools (resistomes) of 181 pig and 178 poultry farms from nine European countries, sequencing more than 5,000 Gb of DNA using shotgun metagenomics. We quantified acquired AMR using the ResFinder database and a second database constructed for this study, consisting of AMR genes identified through screening environmental DNA. The pig and poultry resistomes were very different in abundance and composition. There was a significant country effect on the resistomes, more so in pigs than in poultry. We found higher AMR loads in pigs, whereas poultry resistomes were more diverse. We detected several recently described, critical AMR genes, including mcr-1 and optrA, the abundance of which differed both between host species and between countries. We found that the total acquired AMR level was associated with the overall country-specific antimicrobial usage in livestock and that countries with comparable usage patterns had similar resistomes. However, functionally determined AMR genes were not associated with total drug use.

AB - Antimicrobial resistance (AMR) in bacteria and associated human morbidity and mortality is increasing. The use of antimicrobials in livestock selects for AMR that can subsequently be transferred to humans. This flow of AMR between reservoirs demands surveillance in livestock and in humans. We quantified and characterized the acquired resistance gene pools (resistomes) of 181 pig and 178 poultry farms from nine European countries, sequencing more than 5,000 Gb of DNA using shotgun metagenomics. We quantified acquired AMR using the ResFinder database and a second database constructed for this study, consisting of AMR genes identified through screening environmental DNA. The pig and poultry resistomes were very different in abundance and composition. There was a significant country effect on the resistomes, more so in pigs than in poultry. We found higher AMR loads in pigs, whereas poultry resistomes were more diverse. We detected several recently described, critical AMR genes, including mcr-1 and optrA, the abundance of which differed both between host species and between countries. We found that the total acquired AMR level was associated with the overall country-specific antimicrobial usage in livestock and that countries with comparable usage patterns had similar resistomes. However, functionally determined AMR genes were not associated with total drug use.

U2 - 10.1038/s41564-018-0192-9

DO - 10.1038/s41564-018-0192-9

M3 - Journal article

VL - 3

SP - 898

EP - 908

JO - Nature Microbiology

JF - Nature Microbiology

SN - 2058-5276

IS - 8

ER -