1887
  1. Home
  2. Eurosurveillance
  3. Volume 27, Issue 49, 08/Dec/2022
  4. Article
Research Open Access
Like 0
Download

Food as vehicle for AMR

Abstract

Introduction

Meat can be a vehicle for food-borne transmission of antimicrobial resistant bacteria and antimicrobial resistance genes. The occurrence of extended‐spectrum beta‐lactamase (ESBL) producing Enterobacterales has been observed in meat from livestock production but has not been well studied in meat from wild game.

Aim

We aimed to investigate, particularly in central Europe, to what extent ESBL-producing Enterobacterales may be present in wild game meat.

Methods

A total of 111 samples of different types of game meat supplied by butchers, hunters, retail stores and a large game-processing establishment in Europe were screened for ESBL-producing Enterobacterales using a selective culture medium. Isolates were genotypically and phenotypically characterised.

Results

Thirty-nine samples (35% of the total) yielded ESBL-producing Enterobacterales, with most (35/39) supplied by the game-processing establishment. Isolates included 32 , 18 and one . PCR screening identified (n = 31), (n = 8), (n = 4), (n = 3), (n = 1), (n = 1), (n = 1), and (n = 2). Most belonged to phylogenetic group A (n = 7) or B1 (n = 9), but several isolates belonged to extraintestinal pathogenic (ExPEC) sequence types (ST)58 (n = 4), ST68 (n = 1) and ST540 (n = 1). Whole genome sequencing of six selected isolates localised on megaplasmids in four and on IncN_1 plasmids in one and one . Forty-eight isolates (94%) exhibited a multidrug-resistance phenotype.

Conclusion

We found a high occurrence of ESBL-producing Enterobacterales in wild game meat, suggesting wildlife habitat pollution and possible microbial contamination events occurring during skinning or cutting carcasses.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2022.27.49.2200343
2022-12-08
2024-04-26
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2022.27.49.2200343
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/27/49/eurosurv-27-49-3.html?itemId=/content/10.2807/1560-7917.ES.2022.27.49.2200343&mimeType=html&fmt=ahah

References

  1. World Health Organization (WHO). Critically important antimicrobials for human medicine. 6th revision. Geneva: WHO; 2019. Available from: https://www.who.int/publications/i/item/9789241515528
  2. Peirano G, Pitout JDD. Extended-Spectrum β-lactamase-producing Enterobacteriaceae: update on molecular epidemiology and treatment options. Drugs. 2019;79(14):1529-41.  https://doi.org/10.1007/s40265-019-01180-3  PMID: 31407238 
  3. Aidara-Kane A, Angulo FJ, Conly JM, Minato Y, Silbergeld EK, McEwen SA, et al. , WHO Guideline Development Group. World Health Organization (WHO) guidelines on use of medically important antimicrobials in food-producing animals. Antimicrob Resist Infect Control. 2018;7(1):7.  https://doi.org/10.1186/s13756-017-0294-9  PMID: 29375825 
  4. 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 
  5. Gomes-Neves E, Abrantes AC, Vieira-Pinto M, Müller A. Wild game meat—a microbiological safety and hygiene challenge. Curr Clin Microbiol Rep. 2021;8(2):31-9.  https://doi.org/10.1007/s40588-021-00158-8 
  6. Marescotti ME, Caputo V, Demartini E, Gaviglio A. Discovering market segments for hunted wild game meat. Meat Sci. 2019;149:163-76.  https://doi.org/10.1016/j.meatsci.2018.11.019  PMID: 30557774 
  7. Mateus-Vargas RH, Atanassova V, Reich F, Klein G. Antimicrobial susceptibility and genetic characterization of Escherichia coli recovered from frozen game meat. Food Microbiol. 2017;63:164-9.  https://doi.org/10.1016/j.fm.2016.11.013  PMID: 28040165 
  8. Pitout JD, Thomson KS, Hanson ND, Ehrhardt AF, Moland ES, Sanders CC. beta-Lactamases responsible for resistance to expanded-spectrum cephalosporins in Klebsiella pneumoniae, Escherichia coli, and Proteus mirabilis isolates recovered in South Africa. Antimicrob Agents Chemother. 1998;42(6):1350-4.  https://doi.org/10.1128/AAC.42.6.1350  PMID: 9624474 
  9. Woodford N, Fagan EJ, Ellington MJ. Multiplex PCR for rapid detection of genes encoding CTX-M extended-spectrum (beta)-lactamases. J Antimicrob Chemother. 2006;57(1):154-5.  https://doi.org/10.1093/jac/dki412  PMID: 16284100 
  10. Geser N, Stephan R, Hächler H. Occurrence and characteristics of extended-spectrum β-lactamase (ESBL) producing Enterobacteriaceae in food producing animals, minced meat and raw milk. BMC Vet Res. 2012;8(1):21.  https://doi.org/10.1186/1746-6148-8-21  PMID: 22397509 
  11. Clinical and Laboratory Standards (CLSI). Performance standards for antimicrobial susceptibility testing. Thirty-first edition. Wayne, PA: CLSI; supplement M100. 2021.
  12. Clermont O, Christenson JK, Denamur E, Gordon DM. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep. 2013;5(1):58-65.  https://doi.org/10.1111/1758-2229.12019  PMID: 23757131 
  13. Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH, et al. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol. 2006;60(5):1136-51.  https://doi.org/10.1111/j.1365-2958.2006.05172.x  PMID: 16689791 
  14. Fukasawa Y, Ermini L, Wang H, Carty K, Cheung MS, Long QC. A quality control tool for third generation sequencing long read data. G3: Genes, Genomes. Genetics. 2020;10:1193-6. PMID: 32041730 
  15. Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34(17):i884-90.  https://doi.org/10.1093/bioinformatics/bty560  PMID: 30423086 
  16. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLOS Comput Biol. 2017;13(6):e1005595.  https://doi.org/10.1371/journal.pcbi.1005595  PMID: 28594827 
  17. Seemann T. Abricate. Available at: https://githubcom/tseemann/abricate 2021.
  18. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother. 2012;67(11):2640-4.  https://doi.org/10.1093/jac/dks261  PMID: 22782487 
  19. 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 
  20. Galata V, Fehlmann T, Backes C, Keller A. PLSDB: a resource of complete bacterial plasmids. Nucleic Acids Res. 2019;47(D1):D195-202.  https://doi.org/10.1093/nar/gky1050  PMID: 30380090 
  21. Athanasakopoulou Z, Sofia M, Giannakopoulos A, Papageorgiou K, Chatzopoulos DC, Spyrou V, et al. ESBL-producing Moellerella wisconsensis-the contribution of wild birds in the dissemination of a zoonotic pathogen. Animals (Basel). 2022;12(3):340.  https://doi.org/10.3390/ani12030340  PMID: 35158664 
  22. De Witte C, Vereecke N, Theuns S, De Ruyck C, Vercammen F, Bouts T, et al. Presence of broad-spectrum beta-lactamase-producing Enterobacteriaceae in zoo mammals. Microorganisms. 2021;9(4):834.  https://doi.org/10.3390/microorganisms9040834  PMID: 33919869 
  23. Wasyl D, Zając M, Lalak A, Skarżyńska M, Samcik I, Kwit R, et al. Antimicrobial resistance in Escherichia coli isolated from wild animals in Poland. Microb Drug Resist. 2018;24(6):807-15.  https://doi.org/10.1089/mdr.2017.0148  PMID: 29185858 
  24. Stephan R, Hächler H. Discovery of extended-spectrum beta-lactamase producing Escherichia coli among hunted deer, chamois and ibex. Schweiz Arch Tierheilkd. 2012;154(11):475-8.  https://doi.org/10.1024/0036-7281/a000390  PMID: 23117989 
  25. Mayrhofer S, Paulsen P, Smulders FJM, Hilbert F. Antimicrobial resistance in commensal Escherichia coli isolated from muscle foods as related to the veterinary use of antimicrobial agents in food-producing animals in Austria. Microb Drug Resist. 2006;12(4):278-83.  https://doi.org/10.1089/mdr.2006.12.278  PMID: 17227214 
  26. Literak I, Dolejska M, Radimersky T, Klimes J, Friedman M, Aarestrup FM, et al. Antimicrobial-resistant faecal Escherichia coli in wild mammals in central Europe: multiresistant Escherichia coli producing extended-spectrum beta-lactamases in wild boars. J Appl Microbiol. 2010;108(5):1702-11.  https://doi.org/10.1111/j.1365-2672.2009.04572.x  PMID: 19849769 
  27. Palmeira JD, Cunha MV, Carvalho J, Ferreira H, Fonseca C, Torres RT. Emergence and spread of cephalosporinases in wildlife: a review. Animals (Basel). 2021;11(6):1765.  https://doi.org/10.3390/ani11061765  PMID: 34204766 
  28. Alonso CA, González-Barrio D, Tenorio C, Ruiz-Fons F, Torres C. Antimicrobial resistance in faecal Escherichia coli isolates from farmed red deer and wild small mammals. Detection of a multiresistant E. coli producing extended-spectrum beta-lactamase. Comp Immunol Microbiol Infect Dis. 2016;45:34-9.  https://doi.org/10.1016/j.cimid.2016.02.003  PMID: 27012919 
  29. Poeta P, Radhouani H, Pinto L, Martinho A, Rego V, Rodrigues R, et al. Wild boars as reservoirs of extended-spectrum beta-lactamase (ESBL) producing Escherichia coli of different phylogenetic groups. J Basic Microbiol. 2009;49(6):584-8.  https://doi.org/10.1002/jobm.200900066  PMID: 19810044 
  30. Naseer U, Sundsfjord A. The CTX-M conundrum: dissemination of plasmids and Escherichia coli clones. Microb Drug Resist. 2011;17(1):83-97.  https://doi.org/10.1089/mdr.2010.0132  PMID: 21281129 
  31. Zheng XR, Sun YH, Zhu JH, Wu SL, Ping C, Fang LX, et al. Two novel blaNDM-1-harbouring transposons on pPrY2001-like plasmids coexisting with a novel cfr-encoding plasmid in food animal source Enterobacteriaceae. J Glob Antimicrob Resist. 2021;26:222-6.  https://doi.org/10.1016/j.jgar.2021.06.006  PMID: 34245899 
  32. Hutinel M, Fick J, Larsson DGJ, Flach CF. Investigating the effects of municipal and hospital wastewaters on horizontal gene transfer. Environ Pollut. 2021;276:116733.  https://doi.org/10.1016/j.envpol.2021.116733  PMID: 33631686 
  33. Woodford N, Turton JF, Livermore DM. Multiresistant Gram-negative bacteria: the role of high-risk clones in the dissemination of antibiotic resistance. FEMS Microbiol Rev. 2011;35(5):736-55.  https://doi.org/10.1111/j.1574-6976.2011.00268.x  PMID: 21303394 
  34. Hertz FB, Nielsen JB, Schønning K, Littauer P, Knudsen JD, Løbner-Olesen A, et al. Population structure of drug-susceptible,-resistant and ESBL-producing Escherichia coli from community-acquired urinary tract infections. BMC Microbiol. 2016;16:63.  https://doi.org/10.1186/s12866-016-0725-4  PMID: 27324943 
Finding of extended-spectrum beta-lactamase (ESBL)-producing Enterobacterales in wild game meat originating from several European countries: predominance of Moellerella wisconsensis producing CTX-M-1, November 2021
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Magdalena+N%C3%BCesch-Inderbinen&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Nüesch-Inderbinen Magdalena</a>, <a href="/search?value1=Silvan+Tresch&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Tresch Silvan</a>, <a href="/search?value1=Katrin+Zurfluh&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Zurfluh Katrin</a>, <a href="/search?value1=Nicole+Cernela&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Cernela Nicole</a>, <a href="/search?value1=Michael+Biggel&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Biggel Michael</a>, <a href="/search?value1=Roger+Stephan&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Stephan Roger</a></span>. Finding of extended-spectrum beta-lactamase (ESBL)-producing Enterobacterales in wild game meat originating from several European countries: predominance of Moellerella wisconsensis producing CTX-M-1, November 2021. <a href="/content/ecdc">Euro Surveill.</a> 2022;27(49):pii=2200343. <a href="https://doi.org/10.2807/1560-7917.ES.2022.27.49.2200343" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2022.27.49.2200343</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 18 Apr 2022;&nbsp;&nbsp; <span class="generated">Accepted</span>: 23 Oct 2022 </span> </p>
/content/10.2807/1560-7917.ES.2022.27.49.2200343
/content/10.2807/1560-7917.ES.2022.27.49.2200343
Loading

Data & Media loading...

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error