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Food as vehicle for AMR

Abstract

Background

The pet industry is expanding worldwide, particularly raw meat-based diets (RMBDs). There are concerns regarding the safety of RMBDs, especially their potential to spread clinically relevant antibiotic-resistant bacteria or zoonotic pathogens.

Aim

We aimed to investigate whether dog food, including RMBD, commercially available in Portugal can be a source of and/or other strains resistant to last-line antibiotics such as colistin.

Methods

Fifty-five samples from 25 brands (21 international ones) of various dog food types from 12 suppliers were screened by standard cultural methods between September 2019 and January 2020. Isolates were characterised by phenotypic and genotypic methods, including whole genome sequencing and comparative genomics.

Results

Only RMBD batches were contaminated, with 10 of 14 containing polyclonal multidrug-resistant (MDR) and one MDR . One turkey-based sample contained MDR serotype 1,4,[5],12:i:- ST34/cgST142761 with similarity to human clinical isolates occurring worldwide. This exhibited typical antibiotic resistance ( +  +  + ) and metal tolerance profiles ( +  + ) associated with the European epidemic clone. Two samples (turkey/veal) carried globally dispersed MDR (ST3997-complexST10/cgST95899 and ST297/cgST138377) with colistin resistance (minimum inhibitory concentration: 4 mg/L) and gene on IncX4 plasmids, which were identical to other IncX4 circulating worldwide.

Conclusion

Some RMBDs from European brands available in Portugal can be a vehicle for clinically relevant MDR and pathogenic clones carrying genes encoding resistance to the last-line antibiotic colistin. Proactive actions within the One Health context, spanning regulatory, pet-food industry and consumer levels, are needed to mitigate these public health risks.

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/content/10.2807/1560-7917.ES.2024.29.18.2300561
2024-05-02
2024-11-16
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2024.29.18.2300561
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References

  1. Davies RH, Lawes JR, Wales AD. Raw diets for dogs and cats: a review, with particular reference to microbiological hazards. J Small Anim Pract. 2019;60(6):329-39.  https://doi.org/10.1111/jsap.13000  PMID: 31025713 
  2. Freeman LM, Chandler ML, Hamper BA, Weeth LP. Current knowledge about the risks and benefits of raw meat-based diets for dogs and cats. J Am Vet Med Assoc. 2013;243(11):1549-58.  https://doi.org/10.2460/javma.243.11.1549  PMID: 24261804 
  3. Runesvärd E, Wikström C, Fernström L-L, Hansson I. Presence of pathogenic bacteria in faeces from dogs fed raw meat-based diets or dry kibble. Vet Rec. 2020;187(9):e71.  https://doi.org/10.1136/vr.105644  PMID: 32054718 
  4. Solís D, Toro M, Navarrete P, Faúndez P, Reyes-Jara A. Microbiological quality and presence of foodborne pathogens in raw and extruded canine diets and canine fecal samples. Front Vet Sci. 2022;9:799710.  https://doi.org/10.3389/fvets.2022.799710  PMID: 35923819 
  5. Vecchiato CG, Schwaiger K, Biagi G, Dobenecker B. From nutritional adequacy to hygiene quality: A detailed assessment of commercial raw pet-food for dogs and cats. Animals (Basel). 2022;12(18):2395.  https://doi.org/10.3390/ani12182395  PMID: 36139257 
  6. European Pet Food Industry (FEDIAF). Guide to good practice for the manufacture of safe pet foods. Brussels: FEDIAF; 2018. Available from: http://europeanpetfood.org/wp-content/uploads/2022/03/FEDIAF_Safety_Guide_February_2018_online.pdf
  7. Europe Commission. Commission Regulation (EU) No 142/2011 implementing Regulation (EC) No 1069/2009 of the European Parliament and of the Council laying down health rules as regards animal by-products and derived products not intended for human consumption and implementing Council Directive 97/78/EC as regards certain samples and items exempt from veterinary checks at the border under that Directive. Official Journal of the European Union. 26.2.2011:L 54/1. Available from: http://www.eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2011:054:0001:0254:EN:PDF
  8. Rapid Alert System for Food and Feed (RASFF). RASFF Window. Brussels: European Commission. [Accessed: 12 Feb 2024]. Available from: https://webgate.ec.europa.eu/rasff-window/screen/search
  9. Kaindama L, Jenkins C, Aird H, Jorgensen F, Stoker K, Byrne L. A cluster of Shiga toxin-producing Escherichia coli O157:H7 highlights raw pet food as an emerging potential source of infection in humans. Epidemiol Infect. 2021;149(e124):e124.  https://doi.org/10.1017/S0950268821001072  PMID: 33955833 
  10. Russini V, Corradini C, Rasile E, Terracciano G, Senese M, Bellagamba F, et al. A familiar outbreak of monophasic Salmonella serovar Typhimurium (ST34) involving three dogs and their owner’s children. Pathogens. 2022;11(12):1500.  https://doi.org/10.3390/pathogens11121500  PMID: 36558834 
  11. Jones JL, Wang L, Ceric O, Nemser SM, Rotstein DS, Jurkovic DA, et al. Whole genome sequencing confirms source of pathogens associated with bacterial foodborne illness in pets fed raw pet food. J Vet Diagn Invest. 2019;31(2):235-40.  https://doi.org/10.1177/1040638718823046  PMID: 30663530 
  12. Hamame A, Davoust B, Cherak Z, Rolain JM, Diene SM. Mobile colistin resistance (mcr) genes in cats and dogs and their zoonotic transmission risks. Pathogens. 2022;11(6):698.  https://doi.org/10.3390/pathogens11060698  PMID: 35745552 
  13. Menezes J, Moreira da Silva J, Frosini SM, Loeffler A, Weese S, Perreten V, et al. mcr-1 colistin resistance gene sharing between Escherichia coli from cohabiting dogs and humans, Lisbon, Portugal, 2018 to 2020. Euro Surveill. 2022;27(44):2101144.  https://doi.org/10.2807/1560-7917.ES.2022.27.44.2101144  PMID: 36330821 
  14. Nüesch-Inderbinen M, Treier A, Zurfluh K, Stephan R. Raw meat-based diets for companion animals: a potential source of transmission of pathogenic and antimicrobial-resistant Enterobacteriaceae. R Soc Open Sci. 2019;6(10):191170.  https://doi.org/10.1098/rsos.191170  PMID: 31824726 
  15. Nilsson O. Hygiene quality and presence of ESBL-producing Escherichia coli in raw food diets for dogs. Infect Ecol Epidemiol. 2015;5(1):28758.  https://doi.org/10.3402/iee.v5.28758  PMID: 26490763 
  16. van Bree FPJ, Bokken GCAM, Mineur R, Franssen F, Opsteegh M, van der Giessen JWB, et al. Zoonotic bacteria and parasites found in raw meat-based diets for cats and dogs. Vet Rec. 2018;182(2):50.  https://doi.org/10.1136/vr.104535  PMID: 29326391 
  17. Finisterra L, Duarte B, Peixe L, Novais C, Freitas AR. Industrial dog food is a vehicle of multidrug-resistant enterococci carrying virulence genes often linked to human infections. Int J Food Microbiol. 2021;358(109284):109284.  https://doi.org/10.1016/j.ijfoodmicro.2021.109284  PMID: 34144837 
  18. International Organization for Standardization (ISO). ISO 6579–1:2017. Microbiology of the food chain Horizontal method for the detection, enumeration and serotyping of Salmonella. Part 1: Detection of Salmonella spp. Geneva: ISO; 2022. Available from: https://www.iso.org/standard/56712.html
  19. Mourão J, Rebelo A, Ribeiro S, Peixe L, Novais C, Antunes P. Atypical non-H2S-producing monophasic Salmonella Typhimurium ST3478 strains from chicken meat at processing stage are adapted to diverse stresses. Pathogens. 2020;9(9):701.  https://doi.org/10.3390/pathogens9090701  PMID: 32859122 
  20. Ribeiro S, Mourão J, Novais Â, Campos J, Peixe L, Antunes P. From farm to fork: Colistin voluntary withdrawal in Portuguese farms reflected in decreasing occurrence of mcr-1-carrying Enterobacteriaceae from chicken meat. Environ Microbiol. 2021;23(12):7563-77.  https://doi.org/10.1111/1462-2920.15689  PMID: 34327794 
  21. Mourão J, Ribeiro-Almeida M, Novais C, Magalhães M, Rebelo A, Ribeiro S, et al. From farm to fork: Persistence of clinically relevant multidrug-resistant and copper-tolerant Klebsiella pneumoniae long after colistin withdrawal in poultry production. Microbiol Spectr. 2023;11(4):e0138623.  https://doi.org/10.1128/spectrum.01386-23  PMID: 37428073 
  22. European Committee on Antimicrobial Susceptibility Testing (EUCAST). Recommendations for MIC determination of colistin (polymyxin E)—as recommended by the joint CLSI-EUCAST Polymyxin Breakpoints Working Group. Växjö: EUCAST. [Accessed: 5 Jan 2023]. Available from: https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/General_documents/Recommendations_for_MIC_determination_of_colistin_March_2016.pdf
  23. European Committee on Antimicrobial Susceptibility Testing (EUCAST). Breakpoint tables for interpretation of MICs and zone diameters, version 13.0. Växjö: EUCAST. [Accessed: 5 Jan 2022]. Available from: https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_13.0_Breakpoint_Tables.pdf
  24. Clinical and Laboratory Standards Institute (CLSI). M100. Performance standards for antimicrobial susceptibility testing. 32nd ed. Wayne: CLSI; 2022. Available from: https://clsi.org/media/wi0pmpke/m100ed32_sample.pdf
  25. Fujioka M, Otomo Y, Ahsan CR. A novel single-step multiplex polymerase chain reaction assay for the detection of diarrheagenic Escherichia coli. J Microbiol Methods. 2013;92(3):289-92.  https://doi.org/10.1016/j.mimet.2012.12.010  PMID: 23270615 
  26. Mourão J, Marçal S, Ramos P, Campos J, Machado J, Peixe L, et al. Tolerance to multiple metal stressors in emerging non-typhoidal MDR Salmonella serotypes: a relevant role for copper in anaerobic conditions. J Antimicrob Chemother. 2016;71(8):2147-57.  https://doi.org/10.1093/jac/dkw120  PMID: 27118781 
  27. Bottari B, Bancalari E, Barera A, Ghidini S, Gatti M. Evaluating the presence of human pathogens in commercially frozen, biologically appropriate raw pet food sold in Italy. Vet Rec. 2020;187(7):e50.  https://doi.org/10.1136/vr.105893  PMID: 32430390 
  28. Campos J, Mourão J, Peixe L, Antunes P. Non-typhoidal Salmonella in the pig production chain: a comprehensive analysis of its impact on human health. Pathogens. 2019;8(1):19.  https://doi.org/10.3390/pathogens8010019  PMID: 30700039 
  29. 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 2018/2019. EFSA J. 2021;19(4):e06490. PMID: 33868492 
  30. Zeng H, De Reu K, Gabriël S, Mattheus W, De Zutter L, Rasschaert G. Salmonella prevalence and persistence in industrialized poultry slaughterhouses. Poult Sci. 2021;100(4):100991.  https://doi.org/10.1016/j.psj.2021.01.014  PMID: 33610890 
  31. Finley R, Ribble C, Aramini J, Vandermeer M, Popa M, Litman M, et al. The risk of salmonellae shedding by dogs fed Salmonella-contaminated commercial raw food diets. Can Vet J. 2007;48(1):69-75. PMID: 17310625 
  32. Groat EF, Williams NJ, Pinchbeck G, Warner B, Simpson A, Schmidt VM. UK dogs eating raw meat diets have higher risk of Salmonella and antimicrobial-resistant Escherichia coli faecal carriage. J Small Anim Pract. 2022;63(6):435-41.  https://doi.org/10.1111/jsap.13488  PMID: 35191029 
  33. Centers for Disease Control and Prevention (CDC). Outbreak of multidrug-resistant Salmonella infections linked to contact with pig ear pet treats. Washington, D.C.: CDC; 2019. Available from: https://www.cdc.gov/salmonella/pet-treats-07-19/index.html
  34. Centers for Disease Control and Prevention (CDC). Multidrug-resistant salmonella infections linked to raw turkey products. Washington, D.C.: CDC; 2019. Available from: https://www.cdc.gov/salmonella/reading-07-18/index.html
  35. Bacci C, Vismarra A, Dander S, Barilli E, Superchi P. Occurrence and antimicrobial profile of bacterial pathogens in former foodstuff meat products used for pet diets. J Food Prot. 2019;82(2):316-24.  https://doi.org/10.4315/0362-028X.JFP-18-352  PMID: 30688534 
  36. Campos J, Gil J, Mourão J, Peixe L, Antunes P. Ready-to-eat street-vended food as a potential vehicle of bacterial pathogens and antimicrobial resistance: An exploratory study in Porto region, Portugal. Int J Food Microbiol. 2015;206:1-6.  https://doi.org/10.1016/j.ijfoodmicro.2015.04.016  PMID: 25910073 
  37. Hadjadj L, Riziki T, Zhu Y, Li J, Diene SM, Rolain J-M. Study of mcr-1 gene-mediated colistin resistance in Enterobacteriaceae isolated from humans and animals in different countries. Genes (Basel). 2017;8(12):394.  https://doi.org/10.3390/genes8120394  PMID: 29257080 
  38. Bulochova V, Evans EW. Exploring food safety perceptions and self-reported practices of pet owners providing raw meat–based diets to pets. J Food Prot. 2021;84(5):912-9.  https://doi.org/10.4315/JFP-20-338  PMID: 33428742 
Raw meat-based diet for pets: a neglected source of human exposure to Salmonella and pathogenic Escherichia coli clones carrying mcr, Portugal, September 2019 to January 2020
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Marisa+Ribeiro-Almeida&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ribeiro-Almeida Marisa</a>, <a href="/search?value1=Joana+Mour%C3%A3o&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Mourão Joana</a>, <a href="/search?value1=Mafalda+Magalh%C3%A3es&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Magalhães Mafalda</a>, <a href="/search?value1=Ana+R+Freitas&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Freitas Ana R</a>, <a href="/search?value1=Carla+Novais&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Novais Carla</a>, <a href="/search?value1=Lu%C3%ADsa+Peixe&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Peixe Luísa</a>, <a href="/search?value1=Patr%C3%ADcia+Antunes&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Antunes Patrícia</a></span>. Raw meat-based diet for pets: a neglected source of human exposure to Salmonella and pathogenic Escherichia coli clones carrying mcr, Portugal, September 2019 to January 2020. <a href="/content/ecdc">Euro Surveill.</a> 2024;29(18):pii=2300561. <a href="https://doi.org/10.2807/1560-7917.ES.2024.29.18.2300561" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2024.29.18.2300561</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 16 Oct 2023;&nbsp;&nbsp; <span class="generated">Accepted</span>: 04 Mar 2024 </span> </p>
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