Associations between antimicrobial use and the faecal resistome on broiler farms from nine European countries

Roosmarijn E C Luiken*, Liese Van Gompel, Patrick Munk, Steven Sarrazin, Philip Joosten, Alejandro Dorado-García, Rasmus Borup Hansen, Berith Elkær Knudsen, Alex Bossers, Jaap A Wagenaar, Frank Møller Aarestrup, Jeroen Dewulf, Dik J Mevius, Dick J J Heederik, Lidwien A M Smit, Heike Schmitt, EFFORT consortium

*Corresponding author for this work

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Abstract

Objectives
To determine associations between farm- and flock-level antimicrobial usage (AMU), farm biosecurity status and the abundance of faecal antimicrobial resistance genes (ARGs) on broiler farms.
Methods
In the cross-sectional pan-European EFFORT study, conventional broiler farms were visited and faeces, AMU information and biosecurity records were collected. The resistomes of pooled faecal samples were determined by metagenomic analysis for 176 farms. A meta-analysis approach was used to relate total and class-specific ARGs (expressed as fragments per kb reference per million bacterial fragments, FPKM) to AMU (treatment incidence per DDD, TIDDDvet) per country and subsequently across all countries. In a similar way, the association between biosecurity status (Biocheck.UGent) and the resistome was explored.
Results
Sixty-six (38%) flocks did not report group treatments but showed a similar resistome composition and roughly similar ARG levels to antimicrobial-treated flocks. Nevertheless, we found significant positive associations between β-lactam, tetracycline, macrolide and lincosamide, trimethoprim and aminoglycoside antimicrobial flock treatments and ARG clusters conferring resistance to the same class. Similar associations were found with purchased products. In gene-level analysis for β-lactams and macrolides, lincosamides and streptogramins, a significant positive association was found with the most abundant gene clusters blaTEM and erm(B). Little evidence was found for associations with biosecurity.
Conclusions
The faecal microbiome in European broilers contains a high diversity of ARGs, even in the absence of current antimicrobial selection pressure. Despite this, the relative abundance of genes and the composition of the resistome is positively related to AMU in European broiler farms for several antimicrobial classes.
Original languageEnglish
JournalJournal of Antimicrobial Chemotherapy
Volume74
Issue number9
Pages (from-to)2596–2604
ISSN0305-7453
DOIs
Publication statusPublished - 2019

Cite this

Luiken, R. E. C., Van Gompel, L., Munk, P., Sarrazin, S., Joosten, P., Dorado-García, A., ... consortium, EFFORT. (2019). Associations between antimicrobial use and the faecal resistome on broiler farms from nine European countries. Journal of Antimicrobial Chemotherapy, 74(9), 2596–2604. https://doi.org/10.1093/jac/dkz235
Luiken, Roosmarijn E C ; Van Gompel, Liese ; Munk, Patrick ; Sarrazin, Steven ; Joosten, Philip ; Dorado-García, Alejandro ; Borup Hansen, Rasmus ; Knudsen, Berith Elkær ; Bossers, Alex ; Wagenaar, Jaap A ; Aarestrup, Frank Møller ; Dewulf, Jeroen ; Mevius, Dik J ; Heederik, Dick J J ; Smit, Lidwien A M ; Schmitt, Heike ; consortium, EFFORT. / Associations between antimicrobial use and the faecal resistome on broiler farms from nine European countries. In: Journal of Antimicrobial Chemotherapy. 2019 ; Vol. 74, No. 9. pp. 2596–2604.
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title = "Associations between antimicrobial use and the faecal resistome on broiler farms from nine European countries",
abstract = "ObjectivesTo determine associations between farm- and flock-level antimicrobial usage (AMU), farm biosecurity status and the abundance of faecal antimicrobial resistance genes (ARGs) on broiler farms.MethodsIn the cross-sectional pan-European EFFORT study, conventional broiler farms were visited and faeces, AMU information and biosecurity records were collected. The resistomes of pooled faecal samples were determined by metagenomic analysis for 176 farms. A meta-analysis approach was used to relate total and class-specific ARGs (expressed as fragments per kb reference per million bacterial fragments, FPKM) to AMU (treatment incidence per DDD, TIDDDvet) per country and subsequently across all countries. In a similar way, the association between biosecurity status (Biocheck.UGent) and the resistome was explored.ResultsSixty-six (38{\%}) flocks did not report group treatments but showed a similar resistome composition and roughly similar ARG levels to antimicrobial-treated flocks. Nevertheless, we found significant positive associations between β-lactam, tetracycline, macrolide and lincosamide, trimethoprim and aminoglycoside antimicrobial flock treatments and ARG clusters conferring resistance to the same class. Similar associations were found with purchased products. In gene-level analysis for β-lactams and macrolides, lincosamides and streptogramins, a significant positive association was found with the most abundant gene clusters blaTEM and erm(B). Little evidence was found for associations with biosecurity.ConclusionsThe faecal microbiome in European broilers contains a high diversity of ARGs, even in the absence of current antimicrobial selection pressure. Despite this, the relative abundance of genes and the composition of the resistome is positively related to AMU in European broiler farms for several antimicrobial classes.",
author = "Luiken, {Roosmarijn E C} and {Van Gompel}, Liese and Patrick Munk and Steven Sarrazin and Philip Joosten and Alejandro Dorado-Garc{\'i}a and {Borup Hansen}, Rasmus and Knudsen, {Berith Elk{\ae}r} and Alex Bossers and Wagenaar, {Jaap A} and Aarestrup, {Frank M{\o}ller} and Jeroen Dewulf and Mevius, {Dik J} and Heederik, {Dick J J} and Smit, {Lidwien A M} and Heike Schmitt and EFFORT consortium",
year = "2019",
doi = "10.1093/jac/dkz235",
language = "English",
volume = "74",
pages = "2596–2604",
journal = "Journal of Antimicrobial Chemotherapy",
issn = "0305-7453",
publisher = "Oxford University Press",
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Luiken, REC, Van Gompel, L, Munk, P, Sarrazin, S, Joosten, P, Dorado-García, A, Borup Hansen, R, Knudsen, BE, Bossers, A, Wagenaar, JA, Aarestrup, FM, Dewulf, J, Mevius, DJ, Heederik, DJJ, Smit, LAM, Schmitt, H & consortium, EFFORT 2019, 'Associations between antimicrobial use and the faecal resistome on broiler farms from nine European countries', Journal of Antimicrobial Chemotherapy, vol. 74, no. 9, pp. 2596–2604. https://doi.org/10.1093/jac/dkz235

Associations between antimicrobial use and the faecal resistome on broiler farms from nine European countries. / Luiken, Roosmarijn E C; Van Gompel, Liese; Munk, Patrick; Sarrazin, Steven; Joosten, Philip; Dorado-García, Alejandro; Borup Hansen, Rasmus; Knudsen, Berith Elkær; Bossers, Alex; Wagenaar, Jaap A; Aarestrup, Frank Møller; Dewulf, Jeroen; Mevius, Dik J; Heederik, Dick J J; Smit, Lidwien A M; Schmitt, Heike; consortium, EFFORT.

In: Journal of Antimicrobial Chemotherapy, Vol. 74, No. 9, 2019, p. 2596–2604.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Associations between antimicrobial use and the faecal resistome on broiler farms from nine European countries

AU - Luiken, Roosmarijn E C

AU - Van Gompel, Liese

AU - Munk, Patrick

AU - Sarrazin, Steven

AU - Joosten, Philip

AU - Dorado-García, Alejandro

AU - Borup Hansen, Rasmus

AU - Knudsen, Berith Elkær

AU - Bossers, Alex

AU - Wagenaar, Jaap A

AU - Aarestrup, Frank Møller

AU - Dewulf, Jeroen

AU - Mevius, Dik J

AU - Heederik, Dick J J

AU - Smit, Lidwien A M

AU - Schmitt, Heike

AU - consortium, EFFORT

PY - 2019

Y1 - 2019

N2 - ObjectivesTo determine associations between farm- and flock-level antimicrobial usage (AMU), farm biosecurity status and the abundance of faecal antimicrobial resistance genes (ARGs) on broiler farms.MethodsIn the cross-sectional pan-European EFFORT study, conventional broiler farms were visited and faeces, AMU information and biosecurity records were collected. The resistomes of pooled faecal samples were determined by metagenomic analysis for 176 farms. A meta-analysis approach was used to relate total and class-specific ARGs (expressed as fragments per kb reference per million bacterial fragments, FPKM) to AMU (treatment incidence per DDD, TIDDDvet) per country and subsequently across all countries. In a similar way, the association between biosecurity status (Biocheck.UGent) and the resistome was explored.ResultsSixty-six (38%) flocks did not report group treatments but showed a similar resistome composition and roughly similar ARG levels to antimicrobial-treated flocks. Nevertheless, we found significant positive associations between β-lactam, tetracycline, macrolide and lincosamide, trimethoprim and aminoglycoside antimicrobial flock treatments and ARG clusters conferring resistance to the same class. Similar associations were found with purchased products. In gene-level analysis for β-lactams and macrolides, lincosamides and streptogramins, a significant positive association was found with the most abundant gene clusters blaTEM and erm(B). Little evidence was found for associations with biosecurity.ConclusionsThe faecal microbiome in European broilers contains a high diversity of ARGs, even in the absence of current antimicrobial selection pressure. Despite this, the relative abundance of genes and the composition of the resistome is positively related to AMU in European broiler farms for several antimicrobial classes.

AB - ObjectivesTo determine associations between farm- and flock-level antimicrobial usage (AMU), farm biosecurity status and the abundance of faecal antimicrobial resistance genes (ARGs) on broiler farms.MethodsIn the cross-sectional pan-European EFFORT study, conventional broiler farms were visited and faeces, AMU information and biosecurity records were collected. The resistomes of pooled faecal samples were determined by metagenomic analysis for 176 farms. A meta-analysis approach was used to relate total and class-specific ARGs (expressed as fragments per kb reference per million bacterial fragments, FPKM) to AMU (treatment incidence per DDD, TIDDDvet) per country and subsequently across all countries. In a similar way, the association between biosecurity status (Biocheck.UGent) and the resistome was explored.ResultsSixty-six (38%) flocks did not report group treatments but showed a similar resistome composition and roughly similar ARG levels to antimicrobial-treated flocks. Nevertheless, we found significant positive associations between β-lactam, tetracycline, macrolide and lincosamide, trimethoprim and aminoglycoside antimicrobial flock treatments and ARG clusters conferring resistance to the same class. Similar associations were found with purchased products. In gene-level analysis for β-lactams and macrolides, lincosamides and streptogramins, a significant positive association was found with the most abundant gene clusters blaTEM and erm(B). Little evidence was found for associations with biosecurity.ConclusionsThe faecal microbiome in European broilers contains a high diversity of ARGs, even in the absence of current antimicrobial selection pressure. Despite this, the relative abundance of genes and the composition of the resistome is positively related to AMU in European broiler farms for several antimicrobial classes.

U2 - 10.1093/jac/dkz235

DO - 10.1093/jac/dkz235

M3 - Journal article

VL - 74

SP - 2596

EP - 2604

JO - Journal of Antimicrobial Chemotherapy

JF - Journal of Antimicrobial Chemotherapy

SN - 0305-7453

IS - 9

ER -