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Volume 69, Issue 4

Antimicrobial resistance prevalence in commensal from broilers, fattening turkeys, fattening pigs and veal calves in European countries and association with antimicrobial usage at country level Free

Abstract

The aim of this article is to report on antimicrobial resistance (AMR) in commensal from livestock from several European countries. The relationships with antimicrobial usage (AMU) at country level and harmonized indicators to cover the most relevant AMR aspects for human health in animal production were also investigated. were isolated in faeces from broilers and fattening pigs (from nine countries), and fattening turkeys and veal calves (from three countries) and screened against a fixed antimicrobial panel. AMU data were collected at farm and average treatment incidences stratified by antimicrobial class, country and livestock species were calculated. Associations between AMR and AMU at country level were analysed. Independent of animal species, the highest resistance was observed for ampicillin, sulphamethoxazole, tetracycline and trimethoprim. from broilers showed the highest resistance level for (fluoro)quinolones, and multidrug resistance peaked in broilers and fattening turkeys. Colistin resistance was observed at very low levels with the exception of fattening turkeys. High resistance to third- and fourth-generation cephalosporins was detected in broilers and fattening turkeys. The lowest levels of resistance were for meropenem, azithromycin and tigecycline (<1 %). Significant correlations between resistance and usage at country level were detected in broilers for polymyxins and aminoglycosides, and in fattening pigs for cephalosporins, amphenicols, fluoroquinolones and polymyxins. None of the correlations observed between AMR and AMU were statistically significant for fattening turkey and veal calves. The strength of the analysis performed here is the correlation of aggregated data from the same farms at country level for both AMU and AMR within antimicrobial classes.

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Keyword(s): antimicrobial resistance , antimicrobial usage , Escherichia coli , Europe , livestock and MIC
Funding
This study was supported by the:
  • European Commission Seventh Framework Programme (Award 613754)
© 2020 The Authors
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2020-03-18
2024-04-27
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References

  1. McDermott PF, Zhao S, Wagner DD, Simjee S, Walker RD et al. The food safety perspective of antibiotic resistance. Anim Biotechnol 2002; 13:71–84 [View Article][PubMed]
     [Google Scholar]
  2. Hoelzer K, Wong N, Thomas J, Talkington K, Jungman E et al. Antimicrobial drug use in food-producing animals and associated human health risks: what, and how strong, is the evidence?. BMC Vet Res 2017; 13:211 [View Article][PubMed]
     [Google Scholar]
  3. Scott AM, Beller E, Glasziou P, Clark J, Ranakusuma RW et al. Is antimicrobial administration to food animals a direct threat to human health? a rapid systematic review. Int J Antimicrob Agents 2018; 52:316–323 [View Article][PubMed]
     [Google Scholar]
  4. Szmolka A, Nagy B. Multidrug resistant commensal Escherichia coli in animals and its impact for public health. Front Microbiol 2013; 4:258 [View Article][PubMed]
     [Google Scholar]
  5. European Centre for Disease Control European Food Safety Authority - Panel on Biological Hazard (BIOHAZ), and European Medicines Agency - Committee for Medicinal Products for Veterinary Use (CVMP). ECDC, EFSA and EMA Joint Scientific Opinion on a list of outcome indicators as regards surveillance of antimicrobial resistance and antimicrobial consumption in humans and food‐producing animals. Efsa J 2017; 15:e05017
     [Google Scholar]
  6. Munk P, Knudsen BE, Lukjancenko O, Duarte ASR, Van Gompel L et al. Abundance and diversity of the faecal resistome in slaughter pigs and broilers in nine European countries. Nat Microbiol 2018; 3:898–908 [View Article][PubMed]
     [Google Scholar]
  7. European Food Safety Authority (EFSA) Report from the Task Force on Zoonoses Data Collection including guidance for harmonized monitoring and reporting of antimicrobial resistance in commensal Escherichia coli and Enterococcus spp. from food animals. EFSA Journal 2008; 6:141r [View Article]
     [Google Scholar]
  8. Kahlmeter G, Brown DFJ, Goldstein FW, MacGowan AP, Mouton JW et al. European harmonization of MIC breakpoints for antimicrobial susceptibility testing of bacteria. J Antimicrob Chemother 2003; 52:145–148 [View Article][PubMed]
     [Google Scholar]
  9. Joosten P, Sarrazin S, Van Gompel L, Luiken REC, Mevius DJ et al. Quantitative and qualitative analysis of antimicrobial usage at farm and flock level on 181 broiler farms in nine European countries. J Antimicrob Chemother 2019; 74:798–806 [View Article][PubMed]
     [Google Scholar]
  10. Sarrazin S, Joosten P, Van Gompel L, Luiken REC, Mevius DJ et al. Quantitative and qualitative analysis of antimicrobial usage patterns in 180 selected farrow-to-finish pig farms from nine European countries based on single batch and purchase data. J Antimicrob Chemother 2019; 74:807–816 [View Article][PubMed]
     [Google Scholar]
  11. Postma M, Sjölund M, Collineau L, Lösken S, Stärk KDC et al. Assigning defined daily doses animal: a European multi-country experience for antimicrobial products authorized for usage in pigs. J Antimicrob Chemother 2015; 70:294–302 [View Article][PubMed]
     [Google Scholar]
  12. R Core Team R: a language and environment for statistical computing. 2017, R foundation for statistical computing, Vienna, Austria. https://www.R-project.org/
  13. Hanon J-B, Jaspers S, Butaye P, Wattiau P, Méroc E et al. A trend analysis of antimicrobial resistance in commensal Escherichia coli from several livestock species in Belgium (2011–2014). Prev Vet Med 2015; 122:443–452 [View Article][PubMed]
     [Google Scholar]
  14. Wasyl D, Hoszowski A, Zając M, Szulowski K. Antimicrobial resistance in commensal Escherichia coli isolated from animals at slaughter. Front Microbiol 2013; 4:221 [View Article][PubMed]
     [Google Scholar]
  15. European Food Safety Authority European Centre for Disease Control The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017. EFSA J 2019; 17:5598278
     [Google Scholar]
  16. Grossman TH. Tetracycline antibiotics and resistance. Cold Spring Harb Perspect Med 2016; 6:a025387 [View Article][PubMed]
     [Google Scholar]
  17. European Commission Commission regulation (EC) NO 1430/94 amending annexes I, II, III and IV of Council regulation (EEC) NO 2377/90 laying down a community procedure for the establishment of maximum residue limits of veterinary medicinal products in foodstuffs of animal origin. OJ 1994L156/6
     [Google Scholar]
  18. Pournaras S, Koumaki V, Spanakis N, Gennimata V, Tsakris A. Current perspectives on tigecycline resistance in Enterobacteriaceae: susceptibility testing issues and mechanisms of resistance. Int J Antimicrob Agents 2016; 48:11–18 [View Article][PubMed]
     [Google Scholar]
  19. Nickell JS, White BJ. Metaphylactic antimicrobial therapy for bovine respiratory disease in stocker and feedlot cattle. Vet Clin North Am Food Anim Pract 2010; 26:285–301 [View Article][PubMed]
     [Google Scholar]
  20. European Medicines Agency Sales of veterinary antimicrobial agents in 30 European countries in 2016. Trends from 2010 to 2016. 8th ESVAC report 2018
     [Google Scholar]
  21. World Health Organization Advisory Group on Integrated Surveillance of Antimicrobial Resistance (WHO AGISAR Critically Important Antimicrobials for Human Medicine, 6th Revision (ed). Geneva: World Health Organization; 2019
     [Google Scholar]
  22. Randall LP, Lemma F, Rogers JP, Cheney TEA, Powell LF et al. Prevalence of extended-spectrum-β-lactamase-producing Escherichia coli from pigs at slaughter in the UK in 2013. J Antimicrob Chemother 2014; 69:2947–2950 [View Article][PubMed]
     [Google Scholar]
  23. Collignon PJ, Conly JM, Andremont A, McEwen SA, Aidara-Kane A et al. World Health organization ranking of antimicrobials according to their importance in human medicine: a critical step for developing risk management strategies to control antimicrobial resistance from food animal production. Clin Infect Dis 2016; 63:1087–1093 [View Article][PubMed]
     [Google Scholar]
  24. de Jong A, Stephan B, Silley P. Fluoroquinolone resistance of Escherichia coli and Salmonella from healthy livestock and poultry in the EU. J Appl Microbiol 2012; 112:239–245 [View Article][PubMed]
     [Google Scholar]
  25. Falgenhauer L, Imirzalioglu C, Ghosh H, Gwozdzinski K, Schmiedel J et al. Circulation of clonal populations of fluoroquinolone-resistant CTX-M-15-producing Escherichia coli ST410 in humans and animals in Germany. Int J Antimicrob Agents 2016; 47:457–465 [View Article][PubMed]
     [Google Scholar]
  26. Gosling RJ, Clouting CS, Randall LP, Horton RA, Davies RH. Ciprofloxacin resistance in E. coli isolated from turkeys in Great Britain. Avian Pathol 2012; 41:83–89 [View Article][PubMed]
     [Google Scholar]
  27. Jones EM, Snow LC, Carrique-Mas JJ, Gosling RJ, Clouting C et al. Risk factors for antimicrobial resistance in Escherichia coli found in GB turkey flocks. Vet Rec 2013; 173:422 [View Article][PubMed]
     [Google Scholar]
  28. Economou V, Gousia P. Agriculture and food animals as a source of antimicrobial-resistant bacteria. Infect Drug Resist 2015; 8:49–61 [View Article][PubMed]
     [Google Scholar]
  29. Magiorakos A-P, Srinivasan A, Carey RB, Carmeli Y, Falagas ME et al. Multidrug-Resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012; 18:268–281 [View Article][PubMed]
     [Google Scholar]
  30. Simoneit C, Burow E, Tenhagen B-A, Käsbohrer A. Oral administration of antimicrobials increase antimicrobial resistance in E. coli from chicken--a systematic review. Prev Vet Med 2015; 118:1–7 [View Article][PubMed]
     [Google Scholar]
  31. Luiken REC, Van Gompel L, Munk P, Sarrazin S, Joosten P et al. Associations between antimicrobial use and the faecal resistome on broiler farms from nine European countries. J Antimicrob Chemother 2019; 74:2596–2604 [View Article][PubMed]
     [Google Scholar]
  32. Van Gompel L, Luiken REC, Sarrazin S, Munk P, Knudsen BE et al. The antimicrobial resistome in relation to antimicrobial use and biosecurity in pig farming, a metagenome-wide association study in nine European countries. J Antimicrob Chemother 2019; 74:865–876 [View Article][PubMed]
     [Google Scholar]
  33. Dorado-García A, Mevius DJ, Jacobs JJH, Van Geijlswijk IM, Mouton JW et al. Quantitative assessment of antimicrobial resistance in livestock during the course of a nationwide antimicrobial use reduction in the Netherlands. J Antimicrob Chemother 2016; 71:3607–3619 [View Article][PubMed]
     [Google Scholar]
  34. Agency EM. European Centre for Disease Control European Food Safety Authority ECDC/EFSA/EMA second joint report on the integrated analysis of the consumption of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from humans and food-producing animals – joint Interagency antimicrobial consumption and resistance analysis (JIACRA) report. Efsa J 2017; 15:4872
     [Google Scholar]
  35. Chantziaras I, Boyen F, Callens B, Dewulf J. Correlation between veterinary antimicrobial use and antimicrobial resistance in food-producing animals: a report on seven countries. J Antimicrob Chemother 2014; 69:827–834 [View Article][PubMed]
     [Google Scholar]
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Antimicrobial resistance prevalence in commensal Escherichia coli from broilers, fattening turkeys, fattening pigs and veal calves in European countries and association with antimicrobial usage at country level
J. Med. Microbiol. 69, 537 (2020); https://doi.org/10.1099/jmm.0.001176
/content/journal/jmm/10.1099/jmm.0.001176
/content/journal/jmm/10.1099/jmm.0.001176
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