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Incidence and characterization of Staphylococcus aureus strains isolated from food markets

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Abstract

Staphylococcus aureus is a major foodborne pathogen. The primary purpose of this research was to evaluate S. aureus contamination levels and distribution characteristics in various kinds of food. A total of 121 samples of 11 kinds of food were collected from different food markets in the summer season according to their availability and popularity, and 103 (85.1 %) samples were found to be contaminated with S. aureus. Raw meat, meat products, soybean products, and pickled vegetables are highly contaminated food. For enterotoxin genes analysis, among all the isolates, 20 (19.4 %) possessed sea gene, 2 (1.9 %) with sed gene, 8 (7.8 %) with seg gene, 4 (3.8 %) with seh gene, 24 (23.3 %) with sei gene, 5 (4.8 %) with selj gene, 24 (23.3 %) with selk gene, 44 (42.7 %) with seln gene, and 8 (7.8 %) with ser gene. The seb, sec, see, selm, and selu genes were not found in any of the isolates. For the antibiotic resistance genes tests, most isolates from the food samples were positive for at least 1 of 6 antibiotic resistance genes. The most prevalent resistance genes in samples were ermA (85/103, 82.5 %), followed by tetA (61/103, 59.2 %), chlA (60/103, 58.2 %), norA (56/103, 54.3 %), mecA (10/103, 9.7 %), and blaZ (7/103, 6.8 %). Our results showed that most isolates harbored enterotoxins-producing genes and antibiotic resistance genes, indicating the risk of foodborne S. aureus outbreaks, which drew urgent attention to the great need to improve hygienic conditions in food processing, in order to enhance the safety of food products.

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References

  • Alcorn T, Ouyang YD (2012) China's invisible burden of foodborne illness. Lancet 379(9818):789–790

    Article  PubMed  Google Scholar 

  • Argudín MÁ, Mendoza MC, Rodicio MR (2010) Food poisoning and Staphylococcus aureus enterotoxins. Toxins (Basel) 2(7):1751–1773

    Article  Google Scholar 

  • Argudín MA, Mendoza MC, González-Hevia MA, Bances M, Guerra B, Rodicio MR (2012) Genotypes, exotoxin gene content, and antimicrobial resistance of Staphylococcus aureus strains recovered from foods and food handlers. Appl Environ Microbiol 78(8):2930–2935

    Article  PubMed Central  PubMed  Google Scholar 

  • Aydin A, Muratoglu K, Sudagidan M, Bostan K, Okuklu B, Harsa S (2011) Prevalence and antibiotic resistance of foodborne Staphylococcus aureus isolates in Turkey. Foodborne Pathog Dis 8(1):63–69

    Article  CAS  PubMed  Google Scholar 

  • Bania J, Dabrowska A, Bystron J, Korzekwa K, Chrzanowska J, Molenda J (2006) Distribution of newly described enterotoxin-like genes in Staphylococcus aureus from food. Int J Food Microbiol 108(1):36–41

    Article  CAS  PubMed  Google Scholar 

  • Bennett SD, Walsh KA, Gould LH (2013) Foodborne disease outbreaks caused by Bacillus cereus, Clostridium perfringens, and Staphylococcus aureus–United States, 1998–2008. Clin Infect Dis 57(3):425–433

    Article  PubMed  Google Scholar 

  • Chen Y, Guo YC, Wang ZT, Liu XM, Liu H, Dai Y, Tang ZZ, Wen J (2010) Foodborne disease outbreaks in 2006-report of the National Food borne Disease Surveillance Network, China. J Hyg Res (In Chinese) 39(3):331–334

    Google Scholar 

  • Cliver DO, Riemann H (2002) Foodborne Diseases. Staphylococcal Food Poisoning (Chapter 16), 2nd Edition, Academic, London

  • DeLeo FR, Chambers HF (2009) Reemergence of antibiotic-resistant Staphylococcus aureus in the genomics era. J Clin Invest 119(9):2464–2474

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Doyle ME, Hartmann FA, Wong ACL (2011) White Paper on Sources of Methicillin-Resistant Staphylococcus aureus (MRSA) and Other Methicillin-Resistant Staphylococci: Implications for Our Food Supply? Food Research Institute, UW–Madison, www.fri.wisc.edu/

  • Gao J, Ferreri M, Yu FQ, Liu XQ, Chen LB, Su JL, Han B (2012) Molecular types and antibiotic resistance of Staphylococcus aureus isolates from bovine mastitis in a single herd in China. Vet J 192(3):550–552

    Article  CAS  PubMed  Google Scholar 

  • Gücükoğlu A, Cadirci O, Terzi G, Kevenk TO, Alişarli M (2013) Determination of enterotoxigenic and methicillin resistant Staphylococcus aureus in ice cream. J Food Sci 78(5):M738–M741

    Article  PubMed  Google Scholar 

  • Gutiérrez D, Delgado S, Vázquez-Sánchez D, Martínez B, Cabo ML, Rodríguez A, Herrera JJ, García P (2012) Incidence of Staphylococcus aureus and analysis of associated bacterial communities on food industry surfaces. Appl Environ Microbiol 78(24):8547–8554

    Article  PubMed Central  PubMed  Google Scholar 

  • Güven K, Mutlu MB, Gulbandilar A, Çakir P (2010) Occurrence and characterization of Staphylococcus aureus isolated from meat and dairy products consumed in Turkey. J Food Saf 30(1):196–212

    Article  Google Scholar 

  • Hennekinne JA, De Buyser ML, Dragacci S (2012) Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. FEMS Microbiol Rev 36(4):815–836

    Article  CAS  PubMed  Google Scholar 

  • Hu SK, Liu SY, Hu WF, Zheng TL, Xu JG (2013) Molecular biological characteristics of Staphylococcus aureus isolated from food. Eur Food Res Technol 236(2):285–291

    Article  CAS  Google Scholar 

  • Jiang L, Hu X, Xu T, Zhang H, Sheng D, Yin D (2013) Prevalence of antibiotic resistance genes and their relationship with antibiotics in the Huangpu River and the drinking water sources, Shanghai, China. Sci Total Environ 458–460:267–272

    Article  PubMed  Google Scholar 

  • Kotzekidou P (2013) Microbiological examination of ready-to-eat foods and ready-to-bake frozen pastries from university canteens. Food Microbiol 34(2):337–343

    Article  PubMed  Google Scholar 

  • Kreausukon K, Fetsch A, Kraushaar B, Alt K, Müller K, Krömker V, Zessin KH, Käsbohrer A, Tenhagen BA (2012) Prevalence, antimicrobial resistance, and molecular characterization of methicillin-resistant Staphylococcus aureus from bulk tank milk of dairy herds. J Dairy Sci 95(8):4382–4388

    Article  CAS  PubMed  Google Scholar 

  • Le Loir Y, Baron F, Gautier M (2003) Staphylococcus aureus and food poisoning. Genet Mol Res 2(1):63–76

    PubMed  Google Scholar 

  • Lina G, Bohach GA, Nair SP, Hiramatsu K, Jouvin-Marche E, Mariuzza R (2004) Standard nomenclature for the superantigens expressed by Staphylococcus. J Infect Dis 189(12):2334–2336

    Article  PubMed  Google Scholar 

  • Meemken D, Blaha T, Hotzel H, Strommenger B, Klein G, Ehricht R, Monecke S, Kehrenberg C (2013) Genotypic and phenotypic characterization of Staphylococcus aureus isolates from wild boars. Appl Environ Microbiol 79(5):1739–1742

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Morandi S, Brasca M, Lodi R, Cremonesi P, Castiglioni B (2007) Detection of classical enterotoxins and identification of enterotoxin genes in Staphylococcus aureus from milk and dairy products. Vet Microbiol 124(1–2):66–72

    Article  CAS  PubMed  Google Scholar 

  • Peles F, Wagner M, Varga L, Hein I, Rieck P, Gutser K, Keresztúri P, Kardos G, Turcsányi I, Béri B, Szabó A (2007) Characterization of Staphylococcus aureus strains isolated from bovine milk in Hungary. Int J Food Microbiol 118(2):186–193

    Article  CAS  PubMed  Google Scholar 

  • Rosec JP, Gigaud O (2002) Staphylococcal enterotoxin genes of classical and new types detected by PCR in France. Int J Food Microbiol 77(1–2):61–70

    Article  CAS  PubMed  Google Scholar 

  • Shittu AO, Okon K, Adesida S, Oyedara O, Witte W, Strommenger B, Layer F, Nübel U (2011) Antibiotic resistance and molecular epidemiology of Staphylococcus aureus in Nigeria. BMC Microbiol 11:92

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Su YC, Wong AC (1995) Identification and purification of a new staphylococcal enterotoxin, H. Appl Environ Microbiol 61(4):1438–1443

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sudagidan M, Aydin A (2013) Presence of inducible clindamycin resistance phenotype and erm genes in foodborne Staphylococcus aureus isolates. Foodborne Pathog Dis 10(6):555–558

    Article  CAS  PubMed  Google Scholar 

  • Tang JN, Shi XM, Shi CL, Chen HC (2006) Characterization of a duplex PCR assay for the detection of enterotoxigenic strains of Staphylococcus aureus. J Rapid Meth Aut Mic 14(3):201–217

    Article  CAS  Google Scholar 

  • Tang J, Tang C, Chen J, Du Y, Yang XN, Wang C, Zhang H, Yue H (2011) Phenotypic characterization and prevalence of enterotoxin genes in Staphylococcus aureus isolates from outbreaks of illness in Chengdu City. Foodborne Pathog Dis 8(12):1317–1320

    Article  CAS  PubMed  Google Scholar 

  • Vázquez-Sánchez D, Habimana O, Holck A (2013) Impact of food-related environmental factors on the adherence and biofilm formation of natural Staphylococcus aureus isolates. Curr Microbiol 66(2):110–121

    Article  PubMed  Google Scholar 

  • WHO (2002) Food safety and food borne illness. In World health Organization Fact sheet. World Health Organization, Geneva

    Google Scholar 

  • Zhao X, Li Y, Park M, Wang J, Zhang Y, He X, Forghani F, Wang L, Yu G, Oh DH (2013) Loop-mediated isothermal amplification assay targeting the femA gene for rapid detection of Staphylococcus aureus from clinical and food samples. J Microbiol Biotechnol 23(2):246–250

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was jointly supported by the National Natural Science Foundation of China (No. 31371781), the New Century Excellent Talents in University (NCET-11-0847), the National Science and Technology Major Project of the Ministry of Science and Technology of China (201203009).

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Correspondence to Junni Tang or Jian Li.

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Tang, J., Zhang, R., Chen, J. et al. Incidence and characterization of Staphylococcus aureus strains isolated from food markets. Ann Microbiol 65, 279–286 (2015). https://doi.org/10.1007/s13213-014-0859-2

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