Anti-microbial Resistance of Salmonella Isolates from Raw Meat-based Dog Food in Japan

Overview

Journal Vet Med Sci

Specialty Veterinary Medicine

Date 2022 Jan 25

PMID 35077028

Authors

Shoichiro Yukawa

Ikuo Uchida

Hiroshi Takemitsu

Asako Okamoto

Motomi Yukawa

Seinosuke Ohshima

Yutaka Tamura

Affiliations

Soon will be listed here.

Abstract

Background: Salmonella contamination of raw meat-based diets (RMBDs) for pets poses a major public health concern but has not been investigated in Japan.

Objective: To investigate Salmonella contamination in RMBDs for dogs marketed in Japan and the anti-microbial resistance profiles of the Salmonella isolates.

Methods: Sixty commercial RMBD samples were collected in the Okayama and Osaka Prefectures, Japan, between December 2016 and March 2017. The obtained Salmonella isolates were serotyped, their anti-microbial resistance patterns were determined, and the anti-microbial-resistant isolates were screened for the presence of resistance genes by polymerase chain reaction.

Results: Salmonella enterica subsp. enterica was detected in seven of the 60 RMBD samples. Among them, five isolates were identified as S. Infantis (n = 3), S. Typhimurium (n = 1) and S. Schwarzengrund (n = 1), while the serotypes of two isolates were unable to be identified. All isolates were susceptible to ampicillin, cefazolin, cefotaxime and gentamycin. Two isolates were resistant to more than one anti-microbial agent; one of the S. Infantis isolates was resistant to streptomycin, kanamycin, tetracycline and trimethoprim, while the S. Typhimurium isolate was resistant to nalidixic acid, ciprofloxacin and chloramphenicol. The S. Schwarzengrund isolate was resistant to tetracycline. Additionally, the S. Typhimurium isolate harboured the anti-microbial resistance gene gyrA with a mutation corresponding to Ser-83→Phe amino acid substitution.

Conclusion: The study findings suggest that RMBDs for dogs marketed in Japan can be a potential source of Salmonella infection for dogs and humans including infections caused by quinolone-resistant isolates.

Citing Articles

Multi-locus sequence typing of Salmonella enterica isolates from dog treats and raw meat-based dog food in Japan.

Yukawa S, Morita M BMC Res Notes. 2024; 17(1):366.

PMID: 39702536 PMC: 11660974. DOI: 10.1186/s13104-024-07014-0.

Salmonella Presence and Risk Mitigation in Pet Foods: A Growing Challenge with Implications for Human Health.

Dhakal J, Cancio L, Deliephan A, Chaves B, Tubene S Compr Rev Food Sci Food Saf. 2024; 23(6):e70060.

PMID: 39530630 PMC: 11605167. DOI: 10.1111/1541-4337.70060.

Microflora, Contents of Polyamines, Biogenic Amines, and TVB-N in Bovine Offal and Game Meat for the Raw-Feeding of Adult Dogs.

Lindinger S, Bauer S, Dicakova Z, Pilz B, Paulsen P Animals (Basel). 2023; 13(12).

PMID: 37370497 PMC: 10295124. DOI: 10.3390/ani13121987.

A Combination of Virulent and Non-Productive Phages Synergizes the Immune System against Typhimurium Systemic Infection.

Liang L, Huang J, Cui K, Li P, Shi W, Lin F Int J Mol Sci. 2022; 23(21).

PMID: 36361621 PMC: 9654417. DOI: 10.3390/ijms232112830.

Anti-microbial resistance of Salmonella isolates from raw meat-based dog food in Japan.

Yukawa S, Uchida I, Takemitsu H, Okamoto A, Yukawa M, Ohshima S Vet Med Sci. 2022; 8(3):982-989.

PMID: 35077028 PMC: 9122446. DOI: 10.1002/vms3.739.

References

Cavallo S, Daly E, Seiferth J, Nadeau A, Mahoney J, Finnigan J . Human outbreak of Salmonella Typhimurium associated with exposure to locally made chicken jerky pet treats, New Hampshire, 2013. Foodborne Pathog Dis. 2015; 12(5):441-6. PMC: 6517674. DOI: 10.1089/fpd.2014.1889. View

Lambertini E, Buchanan R, Narrod C, Pradhan A . Transmission of Bacterial Zoonotic Pathogens between Pets and Humans: The Role of Pet Food. Crit Rev Food Sci Nutr. 2015; 56(3):364-418. DOI: 10.1080/10408398.2014.902356. View

Yamane K, Wachino J, Suzuki S, Arakawa Y . Plasmid-mediated qepA gene among Escherichia coli clinical isolates from Japan. Antimicrob Agents Chemother. 2008; 52(4):1564-6. PMC: 2292543. DOI: 10.1128/AAC.01137-07. View

Antunes P, Mourao J, Campos J, Peixe L . Salmonellosis: the role of poultry meat. Clin Microbiol Infect. 2015; 22(2):110-121. DOI: 10.1016/j.cmi.2015.12.004. View

Stogdale L . BARF: "bones and raw foods" or "biologically appropriate raw foods"--fad, fiction or fanatical?. Can Vet J. 2001; 42(7):498-9. PMC: 1476634. View

Viegas F, Ramos C, Xavier R, Lopes E, Oliveira Junior C, Bagno R . 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):e0231275. PMC: 7156072. DOI: 10.1371/journal.pone.0231275. View

Duc V, Nakamoto Y, Fujiwara A, Toyofuku H, Obi T, Chuma T . Prevalence of Salmonella in broiler chickens in Kagoshima, Japan in 2009 to 2012 and the relationship between serovars changing and antimicrobial resistance. BMC Vet Res. 2019; 15(1):108. PMC: 6454760. DOI: 10.1186/s12917-019-1836-6. View

Wojdat E, Kwiatek K, Zasadny R . Microbiological quality of petfood in Poland. Pol J Vet Sci. 2004; 7(3):207-9. View

Sato Y, Mori T, Koyama T, Nagase H . Salmonella virchow infection in an infant transmitted by household dogs. J Vet Med Sci. 2000; 62(7):767-9. DOI: 10.1292/jvms.62.767. View

10.

Bolton L, Kelley L, Lee M, Fedorka-Cray P, Maurer J . Detection of multidrug-resistant Salmonella enterica serotype typhimurium DT104 based on a gene which confers cross-resistance to florfenicol and chloramphenicol. J Clin Microbiol. 1999; 37(5):1348-51. PMC: 84772. DOI: 10.1128/JCM.37.5.1348-1351.1999. View

11.

Noda T, Murakami K, Etoh Y, Okamoto F, Yatsuyanagi J, Sera N . Increase in resistance to extended-spectrum cephalosporins in Salmonella isolated from retail chicken products in Japan. PLoS One. 2015; 10(2):e0116927. PMC: 4314076. DOI: 10.1371/journal.pone.0116927. View

12.

Hara-Kudo Y, Konuma H, Kamata Y, Miyahara M, Takatori K, Onoue Y . Prevalence of the main food-borne pathogens in retail food under the national food surveillance system in Japan. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 2012; 30(8):1450-8. DOI: 10.1080/19440049.2012.745097. View

13.

Furukawa I, Ishihara T, Teranishi H, Saito S, Yatsuyanagi J, Wada E . Prevalence and Characteristics of Salmonella and Campylobacter in Retail Poultry Meat in Japan. Jpn J Infect Dis. 2016; 70(3):239-247. DOI: 10.7883/yoken.JJID.2016.164. View

14.

Freeman L, Michel K . Evaluation of raw food diets for dogs. J Am Vet Med Assoc. 2001; 218(5):705-9. DOI: 10.2460/javma.2001.218.705. View

15.

Yukawa S, Uchida I, Takemitsu H, Okamoto A, Yukawa M, Ohshima S . Anti-microbial resistance of Salmonella isolates from raw meat-based dog food in Japan. Vet Med Sci. 2022; 8(3):982-989. PMC: 9122446. DOI: 10.1002/vms3.739. View

16.

Matayoshi M, Kitano T, Sasaki T, Nakamura M . Resistance phenotypes and genotypes among multiple-antimicrobial-resistant Salmonella enterica subspecies enterica serovar Choleraesuis strains isolated between 2008 and 2012 from slaughter pigs in Okinawa Prefecture, Japan. J Vet Med Sci. 2015; 77(6):705-10. PMC: 4488408. DOI: 10.1292/jvms.14-0683. View

17.

Tauni M, Osterlund A . Outbreak of Salmonella typhimurium in cats and humans associated with infection in wild birds. J Small Anim Pract. 2000; 41(8):339-41. DOI: 10.1111/j.1748-5827.2000.tb03214.x. View

18.

Mizoguchi Y, Suzuki E, Tsuchida H, Tsuda T, Yamamoto E, Nakase K . Outbreak of Salmonella Braenderup infection originating in boxed lunches in Japan in 2008. Acta Med Okayama. 2011; 65(2):63-9. DOI: 10.18926/AMO/45264. View

19.

Sato Y, Kobayash C, Ichikawa K, Kuwamoto R, Matsuura S, Koyama T . An occurrence of Salmonella typhimurium infection in sika deer (Cervus nippon). J Vet Med Sci. 2000; 62(3):313-5. DOI: 10.1292/jvms.62.313. View

20.

Hoelzer K, Moreno Switt A, Wiedmann M . Animal contact as a source of human non-typhoidal salmonellosis. Vet Res. 2011; 42:34. PMC: 3052180. DOI: 10.1186/1297-9716-42-34. View