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; 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

doi:10.1038/s41564-018-0192-9

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 DavidAntonio 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 language	English
Journal	Nature Microbiology
Volume	3
Issue number	8
Pages (from-to)	898-908
ISSN	2058-5276
DOIs	https://doi.org/10.1038/s41564-018-0192-9
Publication status	Published - 1 Aug 2018

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Using metagenomic sequencing for monitoring antimicrobial resistance in livestock animals
Munk, P., 2018, Springer Nature.
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Munk, P., Knudsen, B. E., Lukjacenko, O., Duarte, A. S. R., Van Gompel, L., Luiken, R. E. C., Smit, L. A. M., Schmitt, H., Garcia, A. D., Hansen, R. B., Petersen, T. N., Bossers, A., Ruppé, E., Graveland, H., van Essen, A., Gonzalez-Zorn, B., Moyano, G., Sanders, P., Chauvin, C., ... EFFORT Group (2018). Abundance and diversity of the faecal resistome in slaughter pigs and broilers in nine European countries. Nature Microbiology, 3(8), 898-908. https://doi.org/10.1038/s41564-018-0192-9

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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 Skarzy{\'n}ska 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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doi = "10.1038/s41564-018-0192-9",

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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

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

C2 - 30038308

SN - 2058-5276

VL - 3

SP - 898

EP - 908

JO - Nature Microbiology

JF - Nature Microbiology

IS - 8

ER -

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

Abstract

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Using metagenomic sequencing for monitoring antimicrobial resistance in livestock animals

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