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SDG 3: Antimicrobial resistance

Abstract

Background

Antimicrobial resistance (AMR) is a global threat. Monitoring using an integrated One Health approach is essential to detect changes in AMR occurrence.

Aim

We aimed to detect AMR genes in pathogenic and commensal collected 2013–2020 within monitoring programmes and research from food animals, food (fresh retail raw meat) and humans in six European countries, to compare vertical and horizontal transmission.

Methods

We whole genome sequenced (WGS) 3,745 isolates detected AMR genes using ResFinder and performed phylogenetic analysis to determine isolate relatedness and transmission. A BLASTn-based bioinformatic method compared draft IncI1 genomes to conserved plasmid references from Europe.

Results

Resistance genes to medically important antimicrobials (MIA) such as extended-spectrum cephalosporins (ESC) were widespread but predicted resistance to MIAs authorised for human use (carbapenem, tigecycline) was detected only in two human and three cattle isolates. Phylogenetic analysis clustered according to phylogroups; commensal animal isolates showed greater diversity than those from human patients. Only 18 vertical animal-food and human-animal transmission events of clones were detected. However, IncI1 plasmids from different sources and/or countries carrying resistance to ESCs were conserved and widely distributed, although these variants were rarely detected in human pathogens.

Conclusion

Using WGS we demonstrated AMR is driven vertically and horizontally. Human clinical isolates were more closely related, but their IncI1 plasmids were more diverse, while animal or food isolates were less similar with more conserved IncI1 plasmids. These differences likely arose from variations in selective pressure, influencing AMR evolution and transmission.

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This work is licensed under a Creative Commons Attribution 4.0 International License.
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2024-11-21
2024-12-24
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References

  1. World Health Organization (WHO). WHO List of Medically Important Antimicrobials: a risk management tool for mitigating antimicrobial resistance due to non-human use. Geneva; WHO: 8 Feb 2024. Available from: https://cdn.who.int/media/docs/default-source/gcp/who-mia-list-2024-lv.pdf?sfvrsn=3320dd3d_2
  2. Mendelson M, Sharland M, Mpundu M. Antibiotic resistance: calling time on the ‘silent pandemic’. JAC Antimicrob Resist. 2022;4(2):dlac016.  https://doi.org/10.1093/jacamr/dlac016  PMID: 35310572 
  3. Ludden C, Raven KE, Jamrozy D, Gouliouris T, Blane B, Coll F, et al. One health genomic surveillance of Escherichia coli demonstrates distinct lineages and mobile genetic elements in isolates from humans versus livestock. MBio. 2019;10(1):e02693-18.  https://doi.org/10.1128/mBio.02693-18  PMID: 30670621 
  4. Peng Z, Maciel-Guerra A, Baker M, Zhang X, Hu Y, Wang W, et al. Whole-genome sequencing and gene sharing network analysis powered by machine learning identifies antibiotic resistance sharing between animals, humans and environment in livestock farming. PLOS Comput Biol. 2022;18(3):e1010018.  https://doi.org/10.1371/journal.pcbi.1010018  PMID: 35333870 
  5. European Commission (EC). Commission Implementing Decision (EU) 2020/1729 of 17 November 2020 on the monitoring and reporting of antimicrobial resistance in zoonotic and commensal bacteria and repealing Implementing Decision 2013/652/EU. Brussels: EC; 19 Nov 2020. Available from: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=uriserv:OJ.L_.2020.387.01.0008.01.ENG
  6. Velazquez-Meza ME, Galarde-López M, Carrillo-Quiróz B, Alpuche-Aranda CM. Antimicrobial resistance: One Health approach. Vet World. 2022;15(3):743-9.  https://doi.org/10.14202/vetworld.2022.743-749  PMID: 35497962 
  7. Veterinary Medicines Directorate (VMD). UK Veterinary Antibiotic Resistance and Sales Surveillance Report (UK-VARSS 2021). Addlestone: VMD; 8 Nov 2022. Available from: https://assets.publishing.service.gov.uk/media/63a41fd78fa8f53915365431/FOR_PUBLICATION_-_UK-VARSS_2021_Main_Report__Final_v3_-accessible.pdf
  8. European Commission (EC). Regulation 1831/2003/EC on additives for use in animal nutrition, Brussels: EC; 22 Sep 2003. Available from: https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2003:268:0029:0043:EN:PDF
  9. European Centre for Disease Prevention and Control (ECDC), European Food Safety Authority (EFSA) and European Medicines Agency (EMA). Antimicrobial consumption and resistance in bacteria from humans and animals: third joint inter-agency report on integrated analysis of antimicrobial agent consumption and occurrence of antimicrobial resistance in bacteria from humans and food-producing animals in the EU/EEA: JIACRA III 2016-2018.Stockholm: ECDC, Parma: EFSA and Amsterdam: EMA; 2021. Available from: https://data.europa.eu/doi/10.2900/056892
  10. European Centre for Disease Prevention and Control (ECDC). Antimicrobial resistance in the EU/EEA (EARS-Net) - Annual Epidemiological Report for 2021. Stockholm: ECDC; 17 Nov 2022. Available from: https://www.ecdc.europa.eu/en/publications-data/surveillance-antimicrobial-resistance-europe-2021
  11. Martelli F, AbuOun M, Cawthraw S, Storey N, Turner O, Ellington M, et al. Detection of the transferable tigecycline resistance gene tet(X4) in Escherichia coli from pigs in the United Kingdom. J Antimicrob Chemother. 2022;77(3):846-8.  https://doi.org/10.1093/jac/dkab439  PMID: 34897485 
  12. Duggett NA, Randall LP, Horton RA, Lemma F, Kirchner M, Nunez-Garcia J, et al. Molecular epidemiology of isolates with multiple mcr plasmids from a pig farm in Great Britain: the effects of colistin withdrawal in the short and long term. J Antimicrob Chemother. 2018;73(11):3025-33.  https://doi.org/10.1093/jac/dky292  PMID: 30124905 
  13. Duggett N, AbuOun M, Randall L, Horton R, Lemma F, Rogers J, et al. The importance of using whole genome sequencing and extended spectrum beta-lactamase selective media when monitoring antimicrobial resistance. Sci Rep. 2020;10(1):19880.  https://doi.org/10.1038/s41598-020-76877-7  PMID: 33199763 
  14. Nunez-Garcia J, AbuOun M, Storey N, Brouwer MS, Delgado-Blas JF, Mo SS, et al. Harmonisation of in-silico next-generation sequencing based methods for diagnostics and surveillance. Sci Rep. 2022;12(1):14372.  https://doi.org/10.1038/s41598-022-16760-9  PMID: 35999234 
  15. Duggett N, Ellington MJ, Hopkins KL, Ellaby N, Randall L, Lemma F, et al. Detection in livestock of the human pandemic Escherichia coli ST131 fimH30(R) clone carrying blaCTX-M-27. J Antimicrob Chemother. 2021;76(1):263-5.  https://doi.org/10.1093/jac/dkaa407  PMID: 33068401 
  16. Zamudio R, Boerlin P, Beyrouthy R, Madec JY, Schwarz S, Mulvey MR, et al. Dynamics of extended-spectrum cephalosporin resistance genes in Escherichia coli from Europe and North America. Nat Commun. 2022;13(1):7490.  https://doi.org/10.1038/s41467-022-34970-7  PMID: 36509735 
  17. Shaw LP, Chau KK, Kavanagh J, AbuOun M, Stubberfield E, Gweon HS, et al. Niche and local geography shape the pangenome of wastewater- and livestock-associated Enterobacteriaceae. Sci Adv. 2021;7(15):eabe3868.  https://doi.org/10.1126/sciadv.abe3868  PMID: 33837077 
  18. Arredondo-Alonso S, Willems RJ, van Schaik W, Schürch AC. On the (im)possibility of reconstructing plasmids from whole-genome short-read sequencing data. Microb Genom. 2017;3(10):e000128.  https://doi.org/10.1099/mgen.0.000128  PMID: 29177087 
  19. Johnson TJ, Nolan LK. Plasmid Replicon Typing. In: Caugant DA (editor). Molecular Epidemiology of Microorganisms. Dordrecht: Springer; 2009. p. 27-35. Available from: http://link.springer.com/10.1007/978-1-60327-999-4_3
  20. One Health European Joint Programme (OH-EJP). The Project ARDIG. 2024. Available from: https://onehealthejp.eu/jrp-ardig
  21. Gonzalez TJB, Marcato F, de Freitas Costa E, van den Brand H, Hoorweg FA, Wolthuis-Fillerup M, et al. Longitudinal study on the prevalence of extended spectrum cephalosporins-resistant Escherichia coli colonization in Dutch veal farms. Vet Microbiol. 2022;273:109520.  https://doi.org/10.1016/j.vetmic.2022.109520  PMID: 35939860 
  22. Storey N, Cawthraw S, Turner O, Rambaldi M, Lemma F, Horton R, et al. Use of genomics to explore AMR persistence in an outdoor pig farm with low antimicrobial usage. Microb Genom. 2022;8(3):000782.  https://doi.org/10.1099/mgen.0.000782  PMID: 35344479 
  23. Mo SS, Norström M, Slettemeås JS, Urdahl AM, Telke AA, Sunde M. Longitudinal sampling reveals persistence of and genetic diversity in extended-spectrum cephalosporin-resistant Escherichia coli from Norwegian broiler production. Front Microbiol. 2021;12:795127.  https://doi.org/10.3389/fmicb.2021.795127  PMID: 34956163 
  24. Mo SS, Telke AA, Osei KO, Sekse C, Slettemeås JS, Urdahl AM, et al. blaCTX-M-1/IncI1-Iγ Plasmids Circulating in Escherichia coli From Norwegian Broiler Production Are Related, but Distinguishable. Front Microbiol. 2020;11:333.  https://doi.org/10.3389/fmicb.2020.00333  PMID: 32194533 
  25. European Food Safety AuthorityEuropean Centre for Disease Prevention and Control. The European Union Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2019-2020. EFSA J. 2022;20(3):e07209. PMID: 35382452 
  26. Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S, Cattoir V, et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother. 2020;75(12):3491-500.  https://doi.org/10.1093/jac/dkaa345  PMID: 32780112 
  27. Carattoli A, Zankari E, García-Fernández A, Voldby Larsen M, Lund O, Villa L, et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother. 2014;58(7):3895-903.  https://doi.org/10.1128/AAC.02412-14  PMID: 24777092 
  28. Seemann T. mlst. Available from: https://github.com/tseemann/mlst
  29. Tonkin-Hill G, MacAlasdair N, Ruis C, Weimann A, Horesh G, Lees JA, et al. Producing polished prokaryotic pangenomes with the Panaroo pipeline. Genome Biol. 2020;21(1):180.  https://doi.org/10.1186/s13059-020-02090-4  PMID: 32698896 
  30. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32(1):268-74.  https://doi.org/10.1093/molbev/msu300  PMID: 25371430 
  31. Kaspersen H, Fiskebeck EZ. ALPPACA - A tooL for prokaryotic phylogeny and clustering analysis. J Open Source Softw. 2022;7(79):4677.  https://doi.org/10.21105/joss.04677 
  32. Smith H, Bossers A, Harders F, Wu G, Woodford N, Schwarz S, et al. Characterization of epidemic IncI1-Iγ plasmids harboring ambler class A and C genes in Escherichia coli and Salmonella enterica from animals and humans. Antimicrob Agents Chemother. 2015;59(9):5357-65.  https://doi.org/10.1128/AAC.05006-14  PMID: 26100710 
  33. AbuOun M, Jones H, Stubberfield E, Gilson D, Shaw LP, Hubbard ATM, et al. A genomic epidemiological study shows that prevalence of antimicrobial resistance in Enterobacterales is associated with the livestock host, as well as antimicrobial usage. Microb Genom. 2021;7(10):000630.  https://doi.org/10.1099/mgen.0.000630  PMID: 34609275 
  34. Katz LS, Griswold T, Morrison SS, Caravas JA, Zhang S, den Bakker HC, et al. Mashtree: a rapid comparison of whole genome sequence files. J Open Source Softw. 2019;4(44):1762.  https://doi.org/10.21105/joss.01762  PMID: 35978566 
  35. Ramírez-Castillo FY, Guerrero-Barrera AL, Avelar-González FJ. An overview of carbapenem-resistant organisms from food-producing animals, seafood, aquaculture, companion animals, and wildlife. Front Vet Sci. 2023;10:1158588.  https://doi.org/10.3389/fvets.2023.1158588  PMID: 37397005 
  36. Jakobsen L, Garneau P, Kurbasic A, Bruant G, Stegger M, Harel J, et al. Microarray-based detection of extended virulence and antimicrobial resistance gene profiles in phylogroup B2 Escherichia coli of human, meat and animal origin. J Med Microbiol. 2011;60(Pt 10):1502-11.  https://doi.org/10.1099/jmm.0.033993-0  PMID: 21617024 
  37. Micenková L, Bosák J, Štaudová B, Kohoutová D, Čejková D, Woznicová V, et al. Microcin determinants are associated with B2 phylogroup of human fecal Escherichia coli isolates. MicrobiologyOpen. 2016;5(3):490-8.  https://doi.org/10.1002/mbo3.345  PMID: 26987297 
  38. Sabaté M, Prats G, Moreno E, Ballesté E, Blanch AR, Andreu A. Virulence and antimicrobial resistance profiles among Escherichia coli strains isolated from human and animal wastewater. Res Microbiol. 2008;159(4):288-93.  https://doi.org/10.1016/j.resmic.2008.02.001  PMID: 18434099 
  39. Reeves PR, Liu B, Zhou Z, Li D, Guo D, Ren Y, et al. Rates of mutation and host transmission for an Escherichia coli clone over 3 years. PLoS One. 2011;6(10):e26907.  https://doi.org/10.1371/journal.pone.0026907  PMID: 22046404 
  40. de Been M, Lanza VF, de Toro M, Scharringa J, Dohmen W, Du Y, et al. Dissemination of cephalosporin resistance genes between Escherichia coli strains from farm animals and humans by specific plasmid lineages. PLoS Genet. 2014;10(12):e1004776.  https://doi.org/10.1371/journal.pgen.1004776  PMID: 25522320 
  41. Treacy J, Jenkins C, Paranthaman K, Jorgensen F, Mueller-Doblies D, Anjum M, et al. Outbreak of Shiga toxin-producing Escherichia coli O157:H7 linked to raw drinking milk resolved by rapid application of advanced pathogen characterisation methods, England, August to October 2017. Euro Surveill. 2019;24(16):1800191.  https://doi.org/10.2807/1560-7917.ES.2019.24.16.1800191  PMID: 31014418 
  42. European Food Safety Authority (EFSA)Aerts M, Battisti A, Hendriksen R, Kempf I, Teale C, et al. Technical specifications on harmonised monitoring of antimicrobial resistance in zoonotic and indicator bacteria from food-producing animals and food. EFSA J. 2019;17(6):e05709. PMID: 32626332 
  43. Tavaré S. Some probabilistic and statistical problems in the analysis of DNA sequences. Lect Math Life Sci. 1986;17:57-86.
Escherichia coli from six European countries reveals differences in profile and distribution of critical antimicrobial resistance determinants within One Health compartments, 2013 to 2020
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=H%C3%A5kon+P+Kaspersen&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Kaspersen Håkon P</a>, <a href="/search?value1=Michael+SM+Brouwer&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Brouwer Michael SM</a>, <a href="/search?value1=Javier+Nunez-Garcia&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Nunez-Garcia Javier</a>, <a href="/search?value1=Ingrid+C%C3%A1rdenas-Rey&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Cárdenas-Rey Ingrid</a>, <a href="/search?value1=Manal+AbuOun&option1=author&noRedirect=true" class="nonDisambigAuthorLink">AbuOun Manal</a>, <a href="/search?value1=Nicholas+Duggett&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Duggett Nicholas</a>, <a href="/search?value1=Nicholas+Ellaby&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ellaby Nicholas</a>, <a href="/search?value1=Jose+Delgado-Blas&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Delgado-Blas Jose</a>, <a href="/search?value1=Jens+A+Hammerl&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Hammerl Jens A</a>, <a href="/search?value1=Maria+Getino&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Getino Maria</a>, <a href="/search?value1=Carlos+Serna&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Serna Carlos</a>, <a href="/search?value1=Thierry+Naas&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Naas Thierry</a>, <a href="/search?value1=Kees+T+Veldman&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Veldman Kees T</a>, <a href="/search?value1=Alex+Bossers&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bossers Alex</a>, <a href="/search?value1=Marianne+Sunde&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Sunde Marianne</a>, <a href="/search?value1=Solveig+S+Mo&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Mo Solveig S</a>, <a href="/search?value1=Silje+B+J%C3%B8rgensen&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Jørgensen Silje B</a>, <a href="/search?value1=Matthew+Ellington&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ellington Matthew</a>, <a href="/search?value1=Bruno+Gonzalez-Zorn&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Gonzalez-Zorn Bruno</a>, <a href="/search?value1=Roberto+La+Ragione&option1=author&noRedirect=true" class="nonDisambigAuthorLink">La Ragione Roberto</a>, <a href="/search?value1=Philippe+Glaser&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Glaser Philippe</a>, <a href="/search?value1=Muna+F+Anjum&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Anjum Muna F</a></span>. Escherichia coli from six European countries reveals differences in profile and distribution of critical antimicrobial resistance determinants within One Health compartments, 2013 to 2020. <a href="/content/ecdc">Euro Surveill.</a> 2024;29(47):pii=2400295. <a href="https://doi.org/10.2807/1560-7917.ES.2024.29.47.2400295" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2024.29.47.2400295</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 14 May 2024;&nbsp;&nbsp; <span class="generated">Accepted</span>: 07 Oct 2024 </span> </p>
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