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

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Abstract
Objectives: To determine associations between farm-and flock-level antimicrobial usage (AMU), farmbiosecurity 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 classspecific 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 beta-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 beta-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.
Keywords
ESCHERICHIA-COLI, RISK-FACTORS, RESISTANCE, TRANSMISSION

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MLA
Luiken, Roosmarijn EC, et al. “Associations between Antimicrobial Use and the Faecal Resistome on Broiler Farms from Nine European Countries.” JOURNAL OF ANTIMICROBIAL CHEMOTHERAPY, vol. 74, no. 9, 2019, pp. 2596–604.
APA
Luiken, R. E., Van Gompel, L., Munk, P., Sarrazin, S., Joosten, P., Dorado-Garcia, A., … Stark, K. D. (2019). Associations between antimicrobial use and the faecal resistome on broiler farms from nine European countries. JOURNAL OF ANTIMICROBIAL CHEMOTHERAPY, 74(9), 2596–2604.
Chicago author-date
Luiken, Roosmarijn EC, Liese Van Gompel, Patrick Munk, Steven Sarrazin, Philip Joosten, Alejandro Dorado-Garcia, Rasmus Borup Hansen, et al. 2019. “Associations between Antimicrobial Use and the Faecal Resistome on Broiler Farms from Nine European Countries.” JOURNAL OF ANTIMICROBIAL CHEMOTHERAPY 74 (9): 2596–2604.
Chicago author-date (all authors)
Luiken, Roosmarijn EC, Liese Van Gompel, Patrick Munk, Steven Sarrazin, Philip Joosten, Alejandro Dorado-Garcia, Rasmus Borup Hansen, Berith E Knudsen, Alex Bossers, Jaap A Wagenaar, Frank M Aarestrup, Jeroen Dewulf, Dik J Mevius, Dick JJ Heederik, Lidwien AM Smit, Heike Schmitt, Haitske Graveland, Alieda van Essen, Bruno Gonzalez-Zorn, Gabriel Moyano, Pascal Sanders, Claire Chauvin, Julie David, Antonio Battisti, Andrea Caprioli, Thomas Blaha, Katharina Wadepohl, Maximiliane Brandt, Tine Hald, Ana Sofia Ribeiro Duarte, Dariusz Wasyl, Magdalena Skarzynska, Magdalena Zajac, Hristo Daskalov, Helmut W Saatkamp, and Katharina DC Stark. 2019. “Associations between Antimicrobial Use and the Faecal Resistome on Broiler Farms from Nine European Countries.” JOURNAL OF ANTIMICROBIAL CHEMOTHERAPY 74 (9): 2596–2604.
Vancouver
1.
Luiken RE, Van Gompel L, Munk P, Sarrazin S, Joosten P, Dorado-Garcia A, et al. Associations between antimicrobial use and the faecal resistome on broiler farms from nine European countries. JOURNAL OF ANTIMICROBIAL CHEMOTHERAPY. 2019;74(9):2596–604.
IEEE
[1]
R. E. Luiken et al., “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, 2019.
@article{8633080,
  abstract     = {Objectives: To determine associations between farm-and flock-level antimicrobial usage (AMU), farmbiosecurity 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 classspecific 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 beta-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 beta-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.},
  author       = {Luiken, Roosmarijn EC and Van Gompel, Liese and Munk, Patrick and Sarrazin, Steven and Joosten, Philip and Dorado-Garcia, Alejandro and Hansen, Rasmus Borup and Knudsen, Berith E and Bossers, Alex and Wagenaar, Jaap A and Aarestrup, Frank M and Dewulf, Jeroen and Mevius, Dik J and Heederik, Dick JJ and Smit, Lidwien AM and Schmitt, Heike and Graveland, Haitske and van Essen, Alieda and Gonzalez-Zorn, Bruno and Moyano, Gabriel and Sanders, Pascal and Chauvin, Claire and David, Julie and Battisti, Antonio and Caprioli, Andrea and Blaha, Thomas and Wadepohl, Katharina and Brandt, Maximiliane and Hald, Tine and Duarte, Ana Sofia Ribeiro and Wasyl, Dariusz and Skarzynska, Magdalena and Zajac, Magdalena and Daskalov, Hristo and Saatkamp, Helmut W and Stark, Katharina DC},
  issn         = {0305-7453},
  journal      = {JOURNAL OF ANTIMICROBIAL CHEMOTHERAPY},
  keywords     = {ESCHERICHIA-COLI,RISK-FACTORS,RESISTANCE,TRANSMISSION},
  language     = {eng},
  number       = {9},
  pages        = {2596--2604},
  title        = {Associations between antimicrobial use and the faecal resistome on broiler farms from nine European countries},
  url          = {http://dx.doi.org/10.1093/jac/dkz235},
  volume       = {74},
  year         = {2019},
}

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