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

Nature Microbiology volume 3, pages 898–908 (2018)Cite this article

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An Author Correction to this article was published on 21 August 2018

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.

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Fig. 1: Overview of AMR abundance and composition.
Fig. 2: Resistome clustering is influenced by both host animal and country.
Fig. 3: AMR genes differ in abundance between countries.
Fig. 4: Resistome alpha diversity and richness differ between animal host and countries.
Fig. 5: Taxonomic variation explains resistome variation.
Fig. 6: National veterinary AMU is associated with total metagenomic AMR.

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Acknowledgements

We thank all of the anonymous pig and poultry herd owners who agreed to participate in the study and especially everyone involved in sampling and laboratory work: M. Schlepers (Belgium); T. Ivanova, N. Cholakov, E. Gurova-Mehmedova and K. Penchev (Bulgaria); F. Nienhaus (Germany); C. L. Nielsen, P. Ryt-Hansen, B. Hølstad, B. Rasmussen and K. Nielsen (Denmark); C. Jenna, D. Virginie, E. Florent, E. Eric, S. Le Bouquin, L. Denis and T. Rodolphe (France); M. Gherpelli, M. Pegoraro and V. Carfora (Italy); D. de Vries (the Netherlands); B. Gawlik, D. Krasucka and A. Hoszowski (Poland). The EFFORT project (www.effort-against-amr.eu) and the work presented here is supported by the European Union, FP7-KBBE-2013-7, grant agreement 613754.

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Author notes

  1. A list of participants and their affiliations appears at the end of the paper.

Authors and Affiliations

  1. Research Group for Genomic Epidemiology, National Food Institute, Technical University of Denmark, Kongens Lyngby, Denmark

    Patrick Munk, Berith Elkær Knudsen, Oksana Lukjancenko, Ana Sofia Ribeiro Duarte, Thomas Nordahl Petersen, Ole Lund, Tine Hald, Sünje Johanna Pamp, Håkan Vigre & Frank M. Aarestrup

  2. Institute for Risk Assessment Sciences, Utrecht University, Utrecht, the Netherlands

    Liese Van Gompel, Roosmarijn E. C. Luiken, Lidwien A. M. Smit, Heike Schmitt, Alejandro Dorado Garcia, Alex Bossers, Haitske Graveland & Dick Heederik

  3. Intomics A/S. Diplomvej 377, Kongens Lyngby, Denmark

    Rasmus Borup Hansen

  4. Wageningen Bioveterinary Research, Lelystad, the Netherlands

    Alex Bossers, Alieda van Essen, Helmut W. Saatkamp, Jaap A. Wagenaar & Dik Mevius

  5. Genomic Research Laboratory, Hôpitaux Universitaires de Genève, Geneva, Switzerland

    Etienne Ruppé

  6. Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, the Netherlands

    Jaap A. Wagenaar & Dik Mevius

  7. Department of Animal Health and Health Surveillance Center (VISAVET), Complutense University of Madrid, Madrid, Spain

    Bruno Gonzalez-Zorn & Gabriel Moyano

  8. Fougeres Laboratory, French Agency for Food, Environmental and Occupational Health & Safety, Fougères, France

    Pascal Sanders, Claire Chauvin & Julie David

  9. Istituto Zooprofilattico Sperimentale del Lazio e della Toscana, Department of General Diagnostics, National Reference Laboratory for Antimicrobial Resistance, Rome, Italy

    Antonio Battisti & Andrea Caprioli

  10. Department of Reproduction, Obstetrics and Herd Health, Ghent University, Merelbeke, Belgium

    Jeroen Dewulf

  11. University of Veterinary Medicine Hannover, Bakum, Germany

    Thomas Blaha, Katharina Wadepohl & Maximiliane Brandt

  12. National Veterinary Research Institute, Pulawy, Poland

    Dariusz Wasyl, Magdalena Skarzyńska & Magdalena Zajac

  13. National Diagnostic Research Veterinary Institute, Sofia, Bulgaria

    Hristo Daskalov

  14. SAFOSO AG, Liebefeld, Switzerland

    Katharina D. C. Stärk

Authors
  1. Patrick Munk
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  2. Berith Elkær Knudsen
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  3. Oksana Lukjancenko
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  6. Roosmarijn E. C. Luiken
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  14. Ole Lund
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Consortia

EFFORT Group

  • 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

Contributions

F.M.A., D.H., J.A.W., T.H., D.M. and the EFFORT group designed the study. F.M.A. and B.E.K. detailed the sampling and sequencing. A.S.R.D. and the EFFORT group carried out the sampling. B.E.K. and S.J.P. conducted the DNA purification and, with P.M., organized the sequencing. R.B.H., O.Lund. and T.N.P. created the read-mapping pipeline. E.R. created the FRD. P.M., O.Lukjacenko., R.E.C.L., L.V.G., L.A.M.S., H.S., A.B., A.D.G. and H.V. carried out the bioinformatics and statistical analysis. P.M. created the figures and drafted the manuscript. All authors helped review, edit and complete the manuscript.

Corresponding author

Correspondence to Frank M. Aarestrup.

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The authors declare no competing interests.

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Supplementary Information

Supplementary Figures 1–17, Supplementary Table legends and Supplementary Methods.

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Munk, P., Knudsen, B.E., Lukjancenko, O. et al. Abundance and diversity of the faecal resistome in slaughter pigs and broilers in nine European countries. Nat Microbiol 3, 898–908 (2018). https://doi.org/10.1038/s41564-018-0192-9

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