Isolation of Salmonella species of public health concern from commonly fed dried meat dog treats.
Salmonella
dog
dried treats
Journal
The Veterinary record
ISSN: 2042-7670
Titre abrégé: Vet Rec
Pays: England
ID NLM: 0031164
Informations de publication
Date de publication:
Apr 2023
Apr 2023
Historique:
revised:
24
12
2022
received:
17
10
2022
accepted:
11
01
2023
medline:
4
4
2023
pubmed:
31
1
2023
entrez:
30
1
2023
Statut:
ppublish
Résumé
Dried non-heat-treated meat treats, such as ears, skin and tails, are popular supplementary dog foods. Previous studies have demonstrated Salmonella spp. contamination on treats, particularly in pig ears and chicken products. This small, exploratory, cross-sectional study investigated Salmonella spp. presence in dried treats available in the UK. A selection of dried treats from local pet shops and online retailers underwent bacterial culture for Salmonella spp. and subsequent antimicrobial susceptibility testing, with Salmonella serotype determined by whole genome sequencing. Eighty-four samples were tested, with 16% being Salmonella spp. positive. Five Salmonella serotypes were identified, each associated with specific treat types. An antimicrobial-resistant phenotype was identified in 39% of isolates. All serotypes identified are known to cause human infection. This study was limited by a small sample size and limited number of retail sources. Salmonella spp. of public health concern were present in some dried dog treats in this study. Dog owners, pet food retailers and veterinary professionals should be aware of the potential zoonotic disease risk associated with these treats, and appropriate hygiene measures, including thorough hand washing, should be utilised if they are fed.
Sections du résumé
BACKGROUND
BACKGROUND
Dried non-heat-treated meat treats, such as ears, skin and tails, are popular supplementary dog foods. Previous studies have demonstrated Salmonella spp. contamination on treats, particularly in pig ears and chicken products. This small, exploratory, cross-sectional study investigated Salmonella spp. presence in dried treats available in the UK.
METHODS
METHODS
A selection of dried treats from local pet shops and online retailers underwent bacterial culture for Salmonella spp. and subsequent antimicrobial susceptibility testing, with Salmonella serotype determined by whole genome sequencing.
RESULTS
RESULTS
Eighty-four samples were tested, with 16% being Salmonella spp. positive. Five Salmonella serotypes were identified, each associated with specific treat types. An antimicrobial-resistant phenotype was identified in 39% of isolates. All serotypes identified are known to cause human infection.
LIMITATIONS
CONCLUSIONS
This study was limited by a small sample size and limited number of retail sources.
CONCLUSION
CONCLUSIONS
Salmonella spp. of public health concern were present in some dried dog treats in this study. Dog owners, pet food retailers and veterinary professionals should be aware of the potential zoonotic disease risk associated with these treats, and appropriate hygiene measures, including thorough hand washing, should be utilised if they are fed.
Substances chimiques
Anti-Infective Agents
0
Anti-Bacterial Agents
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2642Subventions
Organisme : University of Liverpool
Organisme : Veterinary Medicines Directorate
Informations de copyright
© 2023 The Authors. Veterinary Record published by John Wiley & Sons Ltd on behalf of British Veterinary Association.
Références
Dodd S, Cave N, Abood S, Shoveller A-K, Adolphe J, Verbrugghe A. An observational study of pet feeding practices and how these have changed between 2008 and 2018. Vet Rec. 2020;186(19):643.
Department for Environment Food and Rural Affairs. Using animal by-products to make pet food. Available from: https://www.gov.uk/guidance/using-animal-by-products-to-make-pet-food. Accessed March 2022.
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.
Wong TL, Thom K, Nicol C, Heffernan H, MacDiarmid S. Salmonella serotypes isolated from pet chews in New Zealand. J Appl Microbiol. 2007;103(4):803-10.
Lenz J, Joffe D, Kauffman M, Zhang Y, Lejeune J. Perceptions, practices, and consequences associated with foodborne pathogens and the feeding of raw meat to dogs. Can Vet J. 2009;50(6):637-43.
Morgan SK, Willis S, Shepherd ML. Survey of owner motivations and veterinary input of owners feeding diets containing raw animal products. PeerJ. 2017;2017(3):1-16.
Morelli G, Bastianello S, Catellani P, Ricci R. Raw meat-based diets for dogs: survey of owners’ motivations, attitudes and practices. BMC Vet Res. 2019;15(1):1-10.
Viegas FM, Ramos CP, Xavier RGC, Lopes EO, Junior CAO, Bagno RM, et al. Fecal shedding of Salmonella spp., Clostridium perfringens, and Clostridioides difficile in dogs fed raw meat-based diets in Brazil and their owners’ motivation. PLoS One. 2020;15(4):1-13.
Marx FR, Machado GS, Pezzali JG, Marcolla CS, Kessler AM, Ahlstrøm, et al. Raw beef bones as chewing items to reduce dental calculus in Beagle dogs. Aust Vet J. 2016;94(1-2):18-23.
Wales A, Davies R. How to talk to clients about giving raw food diets to their dogs and cats. In Pract. 2021;43(8):468-73.
Centers for Disease Control and Prevention (CDC). Human salmonellosis associated with animal-derived pet treats-United States and Canada, 2005. MMWR Morb Mortal Wkly Rep. 2006;55(25):702-5.
White DG, Datta A, McDermott P, Friedman S, Qaiyumi S, Ayers S, et al. Antimicrobial susceptibility and genetic relatedness of Salmonella serovars isolated from animal-derived dog treats in the USA. J Antimicrob Chemother. 2003;52(5):860-3.
Clark C, Cunningham J, Ahmed R, Woodward D, Fonseca K, Isaacs S, et al. Characterization of Salmonella associated with pig ear dog treats in Canada. J Clin Microbiol. 2001;39(11):3962-8.
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.
Yukawa S, Uchida I, Tamura Y, Ohshima S, Hasegawa T. Characterisation of antibiotic resistance of Salmonella isolated from dog treats in Japan. Epidemiol Infect. 2019;147:1-6.
Adley C, Dillon C, Morris CP, Delappe N, Cormican M. Prevalence of Salmonella in pig ear pet treats. Food Res Int.. 2011;44(1):193-7.
Willis C. Isolation of Salmonella species from imported dog chews. Vet Rec. 2001;149(14):426-7.
Finley R, Reid-Smith R, Ribble C, Popa M, Vandermeer M, Aramini J. The occurrence and anti-microbial susceptibility of Salmonellae isolated from commercially available pig ear pet treats. Zoonoses Public Health. 2008;55(8-10):455-61.
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114-20.
Tewolde R, Dallman T, Schaefer U, Sheppard CL, Ashton P, Pichon B, et al. MOST: a modified MLST typing tool based on short read sequencing. PeerJ. 2016;2016(8):1-10.
Achtman M, Wain J, Weill FX, Nair S, Zhou Z, Sangal V, et al. Multilocus sequence typing as a replacement for serotyping in Salmonella enterica. PLoS Pathog. 2012;8(6):e1002776.
Ashton PM, Nair S, Peters TM, Bale JA, Powell DG, Painset A, et al. Identification of Salmonella for public health surveillance using whole genome sequencing. PeerJ. 2016;2016(4):1-18.
Zhang S, den Bakker HC, Li S, Chen J, Dinsmore BA, Lane C, et al. SeqSero2: rapid and improved salmonella serotype determination using whole-genome sequencing data. Appl Environ Microbiol. 2019;85(23):e01746-19.
Chattaway MA, Chandra N, Painset A, Shah V, Lamb P, Acheampong E, et al. Genomic approaches used to investigate an atypical outbreak of Salmonella Adjame. Microb Genomics. 2019;5(1):e000248.
Zhou Z, Alikhan NF, Sergeant MJ, Luhmann N, Vaz C, Francisco AP, et al. Grapetree: visualization of core genomic relationships among 100,000 bacterial pathogens. Genome Res. 2018;28(9):1395-404.
Zhou Z, Alikhan NF, Mohamed K, Fan Y, Achtman M. The EnteroBase user's guide, with case studies on Salmonella transmissions, Yersinia pestis phylogeny, and Escherichia core genomic diversity. Genome Res. 2020;30(1):138-52.
Pearce ME, Alikhan NF, Dallman TJ, Zhou Z, Grant K, Maiden MCJ. Comparative analysis of core genome MLST and SNP typing within a European Salmonella serovar Enteritidis outbreak. Int J Food Microbiol. 2018;274:1-11.
Larkin L, de la Gandara MP, Hoban A, Pulford C, Da SilvaNJ, de Valk H, et al. Investigation of an international outbreak of multidrug-resistant monophasic Salmonella Typhimurium associated with chocolate products, EU/EEA and United Kingdom, February to April 2022. Eurosurveillance. 2022;27(15):1-6.
European Committee on Antimicrobial Susceptibility Testing (EUCAST). Breakpoint tables for interpretation of MICs and zone diameters, version 12.0. 2022. p. 15-20. Available from: http://www.eucast.org
Chattaway MA, Dallman TJ, Larkin L, Nair S, Mccormick J, Mikhail A, et al. The transformation of reference microbiology methods and surveillance for Salmonella with the use of whole genome sequencing in England and Wales. Front Public Heal. 2019;7:1-12.
Pitout JDD, Reisbig MD, Mulvey M, Chui L, Louie M, Crowe L, et al. Association between handling of pet treats and infection with Salmonella enterica serotype Newport expressing the AmpC β-lactamase, CMY-2. J Clin Microbiol. 2003;41(10):4578-82.
Ferrari RG, Rosario DKA, Cunha-Neto A, Mano SB, Figueiredo EES, Conte-Juniora CA. Worldwide epidemiology of Salmonella serovars in animal-based foods: a meta-analysis. Appl Environ Microbiol. 2019;85(14):1-21.
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.
Sévellec Y, Granier SA, Le Hello S, Weill F, Guillier L, Mistou M-Y, et al. Source attribution study of sporadic Salmonella Derby cases in France. Front Microbiol. 2020;11:889.
Simon S, Trost E, Bender J, Fuchs S, Malorny B, Rabsch W, et al. Evaluation of WGS based approaches for investigating a food-borne outbreak caused by Salmonella enterica serovar Derby in Germany. Food Microbiol. 2018;71:46-54.
Harvey RR, Friedman CR, Crim SM, Judd M, Barrett KA, Tolar B, et al. Epidemiology of Salmonella enterica serotype Dublin infections among humans, United States, 1968-2013. Emerg Infect Dis. 2018;23(9):1493-501.
Lowden P, Wallis C, Gee N, Hilton A. Investigating the prevalence of Salmonella in dogs within the Midlands region of the United Kingdom. BMC Vet Res. 2015;11(1):1-6.
Sanchez S, Hofacre CL, Lee MD, Maurer JJ, Doyle MP. Zoonosis update animal sources of salmonellosis in humans. J Am Vet Med Assoc. 2002;221(4):492-7.
Reimschuessel R, Grabenstein M, Guag J, Nemser SM, Song K, Qiu J, et al. Multilaboratory survey to evaluate Salmonella prevalence in diarrheic and nondiarrheic dogs and cats in the United States between 2012 and 2014. J Clin Microbiol. 2017;55(5):1350-68.
Usmael B, Abraha B, Alemu S, Mummed B, Hiko A, Abdurehman A. Isolation, antimicrobial susceptibility patterns, and risk factors assessment of non-typhoidal Salmonella from apparently healthy and diarrheic dogs. BMC Vet Res. 2022;18(1):1-12.
Bataller E, García-Romero E, Llobat L, Lizana V, Jiménez-Trigos E. Dogs as a source of Salmonella spp. in apparently healthy dogs in the Valencia Region. Could it be related with intestinal lactic acid bacteria? BMC Vet Res. 2020;16(1):1-9.
Lefebvre SL, Reid-Smith R, Boerlin P, Weese JS. Evaluation of the risks of shedding Salmonellae and other potential pathogens by therapy dogs fed raw diets in Ontario and Alberta. Zoonoses Public Health. 2008;55(8-10):470-80.
Leonard EK, Pearl DL, Janecko N, Finley RL, RJ Reid-smith, Weese JS, et al. Risk factors for carriage of antimicrobial-resistant Salmonella spp. and Escherichia coli in pet dogs from volunteer households in Ontario, Canada, in 2005 and 2006. Am J Vet Res. 2015;76(11):959-68.
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.
Morley PS, Strohmeyer RA, Tankson JD, Hyatt DR, Dargatz DA, Fedorka-Cray PJ. Evaluation of the association between feeding raw meat and Salmonella enterica infections at a Greyhound breeding facility. J Am Vet Med Assoc. 2006;228(10):1524-32.
Williams E, Towle HAM. A case of canine Salmonella spp. osteomyelitis with secondary fracture following dog bite. Vet Med Sci. 2021;7(5):1518-23.
Hertzer JN, Fujishiro M, Lawhon SD, Creevy KE. Treatment and management of Salmonella prostatitis in a heartworm-positive intact male dog: a case report. BMC Vet Res. 2021;17(1):1-7.
Andruzzi MN, Krath ML, Lawhon SD, Boudreau B. Salmonella enterica subspecies houtenae as an opportunistic pathogen in a case of meningoencephalomyelitis and bacteriuria in a dog. BMC Vet Res. 2020;16(1):1-6.
Thomas M, Feng Y. Risk of foodborne illness from pet food: assessing pet owners’ knowledge, behavior, and risk perception. J Food Prot. 2020;83(11):1998-2007.
Empert-Gallegos A, Hill S, Yam PS. Insights into dog owner perspectives on risks, benefits, and nutritional value of raw diets compared to commercial cooked diets. PeerJ. 2020;8:e10383.
Bulochova V, Evans EW. Raw meat-based pet feeding and food safety: netnography study of pet owner comments and review of manufacturers’ information provision. J Food Prot. 2021;84(12):2099-108.
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.