The populations of Japanese deer and boar have increased dramatically and have a serious impact on farming and mountain villages. Although the Japanese government promotes the use of captured wild animals, game meat is not subject to sanitary control considering that it is not subject to meat inspection or quality control. Here, we have attempted to isolate Staphylococcus aureus, a typical foodborne pathogen, as a part of an investigation of contamination in the meats of wild animals and their processing stages. We examined 390 samples of deer feces, 117 samples of wild boar feces, and 75 samples of disemboweled deer meat for isolation of S. aureus; ultimately, 30 (positive rate: 7.7%), 2 (1.7%), and 21 (28.0%) strains were isolated, respectively, from the samples. The genome sequences of these isolates were analyzed and were subjected to multilocus sequence typing. We identified 12 new sequence types (STs) and a dominant population of S. aureus with a characteristic genetic background in wild animals, namely, the ST groups derived from CC121 (number of strains = 39). These strains did not harbor the enterotoxin gene or only harbored egc-related enterotoxin, which is of low involvement in Staphylococcal food poisoning. However, one ST2449 strain, which produces causative enterotoxins, was isolated from a deer's feces. Since there are several common STs isolated from feces and dismembered meat and because fecal contamination during dismemberment is suspected, continuous monitoring and guidance for improving sanitary management conditions during processing and handling of the meat are highly warranted with immediate effect.

Department of Microbiology Tokyo Metropolitan Institute of Public Health 3 24 1 Hyakunin Cho Shinjuku Ku Tokyo 169 0073 Japan

Department of Pathogenetic and Preventive Veterinary Science Joint Faculty of Veterinary Medicine Kagoshima University 1 21 24 Korimoto Kagoshima Kagoshima 890 0065 Japan

Division of Biomedical Food Research National Institute of Health Sciences 3 25 26 Tonomachi Kawasaki Ku Kawasaki Kanagawa 210 9501 Japan

Laboratory of Animal Hygiene Kitasato University School of Veterinary Medicine Higashi 23 35 1 Towada Aomori 034 8628 Japan

Laboratory of Veterinary Food Hygiene Department of Veterinary Medicine College of Bioresource Sciences Nihon University 1866 Kameino Fujisawa Kanagawa 252 0880 Japan

Laboratory of Veterinary Parasitic Diseases Department of Veterinary Sciences Faculty of Agriculture University of Miyazaki 1 1 Gakuen Kibanadai Nishi Miyazaki 889 2192 Japan

Laboratory of Zoonoses Kitasato University School of Veterinary Medicine Higashi 23 35 1 Towada Aomori 034 8628 Japan

Zobrazit více v PubMed

Argudín MÁ, Mendoza MC, Rodicio MR (2010) Food poisoning and Staphylococcus aureus enterotoxins. Toxins (Basel) 2:1751–1773 DOI

Asai T, Hiki M, Baba K et al (2012) Presence of Staphylococcus aureus ST398 and ST9 in Swine in Japan. Jpn J Infect Dis 65:551–552 DOI

Asao T, Kumeda Y, Kawai T et al (2003) An extensive outbreak of staphylococcal food poisoning due to low-fat milk in Japan: estimation of enterotoxin A in the incriminated milk and powdered skim milk. Epidemiol Infect 130:33–40 DOI

Bukowski M, Wladyka B, Dubin G (2010) Exfoliative toxins of Staphylococcus aureus. Toxins (Basel) 2:1148–1165 DOI

Dinges MM, Orwin PM, Schlievert PM (2000) Exotoxins of Staphylococcus aureus. Clin Microbiol Rev 13:16–34 DOI

Fisher EL, Otto M, Cheung GYC (2018) Basis of virulence in enterotoxin-mediated staphylococcal food poisoning. Front Microbiol 9:436 DOI

Gómez P, Lozano C, González-Barrio D et al (2015) High prevalence of methicillin-resistant Staphylococcus aureus (MRSA) carrying the mecC gene in a semi-extensive red deer (Cervus elaphus hispanicus) farm in Southern Spain. Vet Microbiol 177:326–331 DOI

Hata E, Katsuda K, Kobayashi H et al (2010) Genetic variation among Staphylococcus aureus strains from bovine milk and their relevance to methicillin-resistant isolates from humans. J Clin Microbiol 48:2130–2139 DOI

Hu DL, Nakane A (2014) Mechanisms of staphylococcal enterotoxin-induced emesis. Eur J Pharmacol 722:95–107 DOI

Hu DL, Omoe K, Shimoda Y et al (2003) Induction of emetic response to staphylococcal enterotoxins in the house musk shrew (Suncus murinus). Infect Immun 71:567–570 DOI

Kashif A, McClure JA, Lakhundi S et al (2019) Staphylococcus aureus ST398 virulence is associated with factors carried on prophage ϕSa3. Front Microbiol 10:2219 DOI

Luzzago C, Lauzi S, Ehricht R et al (2022) Survey of Staphylococcus aureus carriage by free-living red deer (Cervus elaphus): evidence of human and domestic animal lineages. Transbound Emerg Dis 69:e1659–e1669 DOI

Ménard G, Bonnaure-Mallet M, Donnio PY (2020) Adhesion of Staphylococcus aureus to epithelial cells: an in vitro approach to study interactions within the nasal microbiota. J Med Microbiol 69:1253–1261 DOI

Ministry of Health, Labour and Welfare. Guidelines for Hygienic Management of Wild Fowl and Wild Animal Meat. [Cited 3 February 2023] Available from URL: https://www.mhlw.go.jp/stf/seisakunitsuite/bunya/kenkou_iryou/shokuhin/syokuchu/01_00021.html (In Japanese)

Ministry of the Environment. Protection and management of wild birds and animals. [Cited 3 February 2023] Available from URL: https://www.env.go.jp/nature/choju/docs/docs4/index.html (In Japanese)

Monecke S, Gavier-Widén D, Hotzel H et al (2016) Diversity of Staphylococcus aureus Isolates in European Wildlife. PLoS ONE 11:e0168433 DOI

Munson SH, Tremaine MT, Betley MJ et al (1998) Identification and characterization of staphylococcal enterotoxin types G and I from Staphylococcus aureus. Infect Immun 66:3337–3348 DOI

Nascimento M, Sousa A, Ramirez M et al (2017) PHYLOViZ 2.0: providing scalable data integration and visualization for multiple phylogenetic inference methods. Bioinformatics 33:28–129 DOI

Omoe K, Hu DL, Ono HK et al (2013) Emetic potentials of newly identified staphylococcal enterotoxin-like toxins. Infect Immun 81:3627–3631 DOI

Omoe K, Ishikawa M, Shimoda Y et al (2002) Detection of seg, seh, and sei genes in Staphylococcus aureus isolates and determination of the enterotoxin productivities of S. aureus isolates Harboring seg, seh, or sei genes. J Clin Microbiol 40:857–862 DOI

Porrero MC, Mentaberre G, Sánchez S et al (2014) Carriage of Staphylococcus aureus by free-living wild animals in Spain. Appl Environ Microbiol 80:4865–4870 DOI

Rabello RF, Moreira BM, Lopes RMM et al (2007) Multilocus sequence typing of Staphylococcus aureus isolates recovered from cows with mastitis in Brazilian dairy herds. J Med Microbiol 56:1505–1511 DOI

Santos SCL, Saraiva MMS, Moreira Filho ALB et al (2021) Swine as reservoirs of zoonotic borderline oxacillin-resistant Staphylococcus aureus ST398. Comp Immunol Microbiol Infect Dis 79:101697 DOI

Sasaki T, Tsubakishita S, Tanaka Y et al (2012) Population genetic structures of Staphylococcus aureus isolates from cats and dogs in Japan. J Clin Microbiol 50:2152–2155 DOI

Sasaki Y, Yamanaka M, Nara K et al (2020) Isolation of ST398 methicillin-resistant Staphylococcus aureus from pigs at abattoirs in Tohoku region, Japan. J Vet Med Sci 82:1400–1403 DOI

Sato’o Y, Hisatsune J, Nagasako Y et al (2015) Positive regulation of staphylococcal enterotoxin H by rot (repressor of toxin) protein and its importance in clonal complex 81 subtype 1 lineage-related food poisoning. Appl Environ Microbiol 81:7782–7790 DOI

Schelin J, Wallin-Carlquist N, Cohn MT et al (2011) The formation of Staphylococcus aureus enterotoxin in food environments and advances in risk assessment. Virulence 2:580–592 DOI

Suzuki Y (2022) Current studies in staphylococcal food poisoning and its testing methods. J Clin Lab Med 66:64–72

Suzuki Y, Kubota H, Sato’o Y et al (2015) Identification and characterization of novel Staphylococcus aureus pathogenicity islands encoding staphylococcal enterotoxins originating from staphylococcal food poisoning isolates. J Appl Microbiol 118:1507–1520 DOI

Suzuki Y, Omoe K, Hu DL et al (2014) Molecular epidemiological characterization of Staphylococcus aureus isolates originating from food poisoning outbreaks that occurred in Tokyo, Japan. Microbiol Immunol 58:570–580 DOI

Suzuki Y, Ono HK, Shimojima Y et al (2020) A novel staphylococcal enterotoxin SE02 involved in a staphylococcal food poisoning outbreak that occurred in Tokyo in 2004. Food Microbiol 92:103588 DOI

Umeda K, Ono HK, Wada T et al (2021) High production of egc2-related staphylococcal enterotoxins caused a food poisoning outbreak. Int J Food Microbiol 357:109366 DOI