Prevalence and classification of toxigenic Staphylococcus aureus isolated from refrigerated ready-to-eat foods (sushi, kimbab and California rolls) in Korea

Journal of Applied Microbiology

Volumn 111, Issue 6, 2011, Pages 1456-1464

  Kim, N H ^a   Yun, A R ^b   Rhee, M S ^a  

^a Korea University   (South Korea)

^b Lotte R and D Center   (South Korea)

Author keywords

Food safety; Microbial contamination; Staphylococci; Toxigenicity

Indexed keywords

BACTERIA; CONTAMINATION; FOOD MICROBIOLOGY; FOOD PRODUCTS; GENES; TOXIC MATERIALS;

CALIFORNIA; FOOD-SAFETY; MICROBIAL CONTAMINATION; READY-TO-EAT; READY-TO-EAT FOODS; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; TOXIGENIC; TOXIGENICITY; TOXIN PRODUCTION;

FOOD SAFETY;

BACTERIUM; DATABASE; DISEASE PREVALENCE; FOOD CHAIN; FOOD MARKET; FOOD SAFETY; POLYMERASE CHAIN REACTION; SAMPLING; SPATIOTEMPORAL ANALYSIS; TOXIN;

ARTICLE; BACTERIUM ISOLATE; FOOD CONTAMINATION; FOOD FREEZING; GENETIC CODE; KOREA; NONHUMAN; PREVALENCE; STAPHYLOCOCCUS AUREUS; TOXICITY;

KOREA;

STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS;

EID: 81255153663     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2011.05168.x     Document Type: Article

References (60)

1. Adwan, G., Abu-Shanab, B. and Adwan, K. (2005) Enterotoxigenic Staphylococcus aureus in raw milk in the North of Palestine. Turk J Biol 29, 229-232.
2. Akineden, Ö., Hassan, A.A., Schneider, E. and Usleber, E. (2008) Enterotoxigenic properties of Staphylococcus aureus isolated from goats' milk cheese. Int J Food Microbiol 124, 211-216.
3. Argudin, M.A., Mendoza, M.C. and Fodicio, M.R. (2010) Food poisoning and Staphylococcus aureus enterotoxins. Toxins 2, 1751-1773.
4. Asao, T., Kumeda, T., Kawai, T., Shibata, T., Oda, H., Haruki, K., Nakazawa, H. and Kozaki, S. (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.
5. Atanassova, V., Meindl, A. and Ring, C. (2001) Prevalence of Staphylococcus aureus and staphylococcal enterotoxins in raw pork and uncooked smoked ham - a comparison of classical culturing detection and RFLP-PCR. Int J Food Microbiol 68, 105-113.
6. Atanassova, V., Reich, F. and Klein, G. (2008) Microbiological quality of sushi from sushi bars and retailers. J Food Protect 71, 860-864.
7. Aycicek, H., Cakiroglu, S. and Stevenson, T.H. (2005) Incidence of Staphylococcus aureus in ready-to-eat meals from military cafeterias in Ankara, Turkey. Food Control 16, 531-534.
8. Balaban, N. and Rasooly, A. (2000) Staphylococcal enterotoxins. Int J Food Microbiol 61, 1-10.
9. Bania, J., Dabrowska, A., Bystron, J., Korzekwa, K., Chrzanowska, J. and Molenda, J. (2006) Distribution of newly described enterotoxin-like genes in Staphylococcus aureus from food. Int J Food Microbiol 108, 36-41.
10. Bestor, T.C. (2000) How sushi went global. Foreign Policy 121, 54-63.
11. Betley, M.J. and Harris, T.O. (1994) Staphylococcal enterotoxins: genetic characterization and relationship between structure and emetic activity. Food Microbiol 11, 109-121.
12. Boynukara, B., Gulhan, T., Alisarli, M., Gurturk, K. and Solmaz, H. (2008) Classical enterotoxigenic characteristics of Staphylococcus aureus strains isolated from bovine subclinical mastitis in Van, Turkey. Int J Food Microbiol 125, 209-211.
13. Cha, J.O., Lee, J.K., Jung, Y.H., Yoo, J.I., Park, Y.K., Kim, B.S. and Lee, Y.S. (2006) Molecular analysis of Staphylococcus aureus isolates associated with staphylococcal food poisoning in South Korea. J Appl Microbiol 101, 864-871.
14. Chiang, Y.C., Liao, W.W., Fan, C.M., Pai, W.Y., Chiou, C.S. and Tsen, H.Y. (2008) PCR detection of Staphylococcal enterotoxins (SEs) N, O, P, Q, R, U, and survey of SE types in Staphylococcus aureus isolates form food-poisoning cases in Taiwan. Int J Food Microbiol 121, 66-73.
15. Diplock, K. (2003) The potential of Sushi rice to serve as a medium for bacterial growth. Environmental Health Review (Winter), 109-116.
16. Fang, T.J., Wei, Q.K., Liao, C.W., Hung, M.J. and Wang, T.H. (2003) Microbiological quality of 18°C ready-to-eat food products sold in Taiwan. Int J Food Microbiol 80, 241-250.
17. Fitzgerald, J.R., Monday, S.R., Foster, T.J., Bohach, G.A., Hartigan, P.J., Meaney, W.J. and Smyth, C.J. (2001) Characterization of a putative pathogenicity island from bovine Staphylcoccus aures encoding multiple superantigens. J Bacteriol 183, 63-70.
18. Hwang, S.Y., Kim, S.H., Jang, E.J., Kwon, N.H., Park, Y.K., Koo, H.C., Jung, W.K., Kim, J.M. et al. (2007) Novel multiplex PCR for the detection of the Staphylococcus aureus superantigen and its application to raw meat isolates in Korea. Int J Food Microbiol 117, 99-105.
19. Ikeda, T., Tamate, M., Yamaguchi, K. and Makino, S. (2005) Mass outbreak of food poisoning disease caused by small amounts of staphylococcal enterotoxins A and H. Appl Environ Microbiol 71, 2793-2795.
20. Issenberg, S. (ed.) (2007) Are you ready for rice sandwiches? (How Sushi became the favorite food of the capital of the twentieth century). In The Sushi Economy: Globalization and the Making of a Modern Delicacy, pp. 79-106. New York, NY: Gotham Books.
21. Jarraud, S., Cozon, G., Vandenesch, F., Bes, M., Etienne, J. and Lina, G. (1999) Involvement of enterotoxins G and I in staphylococcal toxic shock syndrome and staphylococcal scarlet fever. J Clin Microbiol 37, 2446-2449.
22. Jarraud, S., Peyrat, M.A., Lim, A., Tristan, A., Bes, M., Mougel, C., Etienne, J., Vandenesch, F. et al. (2001) egc, A highly prevalence operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus. J Immunol 166, 669-677.
23. Jett, M., Iomin, B., Das, R. and Neill, R. (2001) The staphylococcal enterotoxins. In Molecular Medical Microbiology ed. Sussman, M. pp. 1089-1116. San Diego, CA: Academic Press.
24. Johnson, W.M., Tyler, S.D., Ewan, E.P., Ashton, F.E., Pollard, D.R. and Rozee, K.R. (1991) Detection of genes for enterotoxins, exfoliative toxins, and toxic shock syndrome toxin 1 in Staphylococcus aureus by the polymerase chain reaction. J Clin Microbiol 29, 416-430.
25. Jørgensen, H.J., Mørk, T., Høgasen, H.R. and Rørvik, L.M. (2005) Enterotoxigenic Staphylococcus aureus in bulk milk in Norway. J Appl Microbiol 99, 158-166.
26. Jung, W.Y., Choi, Y.M. and Rhee, M.S. (2009) Potential use of supercritical carbon dioxide to decontaminate Escherichia coli O157:H7, Listeria monocytogenes, and Salmonella typhimurium in alfalfa sprouted seeds. Int J Food Microbiol 136, 66-70.
27. Kérouanton, A., Hennekinne, J.A., Letertre, C., Petit, L., Chesneau, O., Brisabois, A. and De Buyser, M.L. (2007) Characterization of Staphylococcus aureus strains associated with food poisoning outbreaks in France. Int J Food Microbiol 115, 369-375.
28. KFDA (Korea Food and Drug Administration). (2010) Food poisoning statistics system. Available at.
29. Kim, S.A., Kim, O.Y. and Rhee, M.S. (2010) Direct application of supercritical carbon dioxide for the reduction of Cronobacter spp. (Enterobacter sakazakii) in end products of dehydrated powdered infant formula. J Dairy Sci 93, 1854-1860.
30. KMA (Korea Meteorological Administration). (2010) Available at.
31. Kuroda, M., Ohta, T., Uchiyama, I., Baba, T., Yuzawa, H., Kobayashi, I., Cui, L., Oguchi, A. et al. (2001) Whole genome sequencing of methicillin-resistant Staphylococcus aureus. Lancet 357, 1225-1240.
32. Lee, S.Y., Dancer, G.I., Chang, S.S., Rhee, M.S. and Kang, D.H. (2006) Efficacy of chlorine dioxide gas against Alicyclobacillus acidoterrestris spores on apple surfaces. Int J Food Microbiol 108, 364-368.
33. Lee, G.Y., Jang, H.I., Hwang, I.G. and Rhee, M.S. (2009) Prevalence and classification of pathogenic Escherichia coli isolated from fresh beef, poultry and pork in Korea. Int J Food Microbiol 134, 196-200.
34. Letertre, C., Perelle, S., Dilasser, F. and Fach, P. (2003) Identification of a new putative enterotoxin SEU encoded by the egc cluster of Staphylococcus aureus. J Appl Microbiol 95, 38-43.
35. Lina, G., Bohach, G.A., Nair, S.P., Hiramatsu, K., Jouvin-Marche, E. and Mariuzza, R. (2004) Standard nomenclature for the superantigens expressed by Staphylococcus. J Infect Dis 189, 2334-2336.
36. Loir, Y.L., Baron, F. and Gautier, M. (2003) Staphylococcus aureus and food poisoning. Genet Mol Res 2, 63-76.
37. Marry, J.C., Lyon, J.D., Roberson, J.R., Lupher, M., Davis, W.C. and Bohach, G.A. (1993) Characterization of novel type C staphylococcal enterotoxins: biological and evolutionary implications. Infect Immun 61, 4254-4262.
38. Monday, S. and Bohach, G.A. (1999) Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in staphylococcal isolates. J Clin Microbiol 37, 3411-3414.
39. Morandi, S., Brasca, M., Lodi, R., Cremonesi, P. and Castiglioni, B. (2007) Detection of classical enterotoxins and identification of enterotoxin genes in Staphylococcus aureus from milk and dairy products. Vet Microbiol 124, 66-72.
40. Munson, S.H., Thremaine, M.T., Betley, M.J. and Welch, R.A. (1998) Identification and characterization of staphylococcal enterotoxin types G and I from Staphylococcus aureus. Infect Immun 66, 3337-3348.
41. NARSA (Network of Antimicrobial Resistance in Staphylococcus aureus). (2010) Available at.
42. Oh, S.K., Lee, N., Cho, Y.S., Shin, D.B., Choi, S.Y. and Koo, M. (2007) Occurrence of toxigenic Staphylococcus aureus in ready-to-eat food in Korea. J Food Protect 70, 1153-1158.
43. Omoe, K., Hu, D.L., Takahashi-Omoe, H., Nakane, A. and Shinagawa, K. (2003) Identification and characterization of a new staphylococcal enterotoxin-related putative toxin encoded by two kinds of plasmids. Infect Immun 71, 6088-6094.
44. Ono, H.K., Omoe, K., Imanishi, K., Iwakabe, Y., Hu, D.L., Kato, H., Saito, N., Nakane, A. et al. (2008) Identification and characterization of two novel staphylococcal enterotoxins, types S and T. Infect Immun 76, 4999-5005.
45. Orwin, P.M., Leung, D.Y., Donahue, H.L., Novick, R.P. and Schlievert, P.M. (2001) Biochemical and biological properties of staphylococcal enterotoxin K. Infect Immun 69, 360-366.
46. Orwin, P.M., Leung, D.Y., Tripp, T.J., Bohach, G.A., Earhart, C.A., Ohlendorf, D.H. and Schlievert, P.M. (2002) Characterization of a novel staphylococcal enterotoxin-like superantigen, a member of the group V subfamily of pyrogenic toxins. Biochemistry 41, 14033-14040.
47. Orwin, P.M., Fitzgerald, J.R., Leung, D.Y., Gutierrez, J.A., Bohach, G.A. and Schlievert, P.M. (2003) Characterization of Staphylococcus aureus enterotoxin L. Infect Immun 71, 2916-2919.
48. Rall, V.L.M., Vieira, F.P., Rall, R., Vieitis, R.L., Fernandes, A. Jr, Candeias, J.M.G., Cardoso, K.F.G. and Araújo, J.P. Jr (2008) PCR detection of staphylococcal enterotoxin genes in Staphylococcus aureus strains isolated from raw and pasteurized milk. Vet Microbiol 132, 408-413.
49. Ren, K., Bannan, J.D., Pancholi, V., Cheung, A.L., Robbins, J.C., Fischetti, V.A. and Zabriskie, J.B. (1994) Characterization and biological properties of a new staphylococcal exotoxin. J Exp Med 180, 1675-1683.
50. Sokari, T. (1991) Distribution of enterotoxigenic Staphylococcus aureus in ready-to-eat foods in eastern Nigeria. Int J Food Microbiol 12, 275-279.
51. Su, Y. and Wong, A. (1995) Identification and purification of a new staphylococcal enterotoxin, H. Appl Environ Microbiol 61, 1438-1443.
52. Thomas, D., Jarraud, S., Lemercier, B., Cozon, G., Echasserieau, K., Etienne, J., Gougeon, M., Lina, G. et al. (2006) Staphylococcal enterotoxin-like toxins U2 and V, two new staphylococcal superantigens arising from recombination within the enterotoxin gene cluster. Infect Immun 74, 4724-4734.
53. US FDA (United States Food and Drug Administration). (2009) Bad Bug Book: foodborne pathogenic microorganisms and natural toxins handbook Staphylococcus aureus. Available at.
54. Vandenbergh, M.F.Q. and Verbrugh, H.A. (1999) Carriage of Staphylococcus aureus: epidemiology and clinical relevance. J Lab Clin Med 133, 525-534.
55. Vandenesch, F., Naimi, T., Enright, M.C., Lina, G., Nimmo, G.R., Heffernan, H., Liassine, N., Bes, M. et al. (2003) Community-acquired methicillin resistant Staphylococcus aureus carrying panton-valentine leukocidin genes: worldwide emergence. Emerg Infect Dis 9, 978-984.
56. Veras, J.F., Carmo, L.S.D., Tong, L.C., Shupp, J.W., Cummings, D., Santos, D.A.D., Cerqueira, M.M.O.P., Cantini, A. et al. (2008) A study of the enterotoxigenicity of coagulase-negative and coagulase-positive staphylococcal isolates from food poisoning outbreaks in Minas Gerais, Brazil. Int J Infect Dis 12, 410-415.
57. Wang, S.C., Wu, C.M., Xia, S.C., Qui, T.H., Xia, L.N. and Shen, J.Z. (2009) Distribution of superantigenic toxin genes in Staphylococcus aureus isolates from milk samples of bovine subclinical mastitis cases in two major dairy production regions of China. Vet Microbiol 137, 276-281.
58. Wei, Q.K., Hwang, S.J. and Chen, T.R. (2006) Microbiological quality of ready-to-eat food products in Southern Taiwan. Yao Wu Shi Pin Fen Xi 14, 68-73.
59. Yarwood, J.M., McCormick, J.K., Paustian, M.L., Orwin, P.M., Kapur, V. and Schlievert, P.M. (2002) Characterization and expression analysis of Staphylococcus aureus pathogenicity island 3: implications of the evolution of staphylococcal pathogenicity islands. J Biol Chem 277, 13138-13147.
60. Zhang, S., Iandolo, J.J. and Stewart, G.C. (1998) The enterotoxin D plasmid of Staphylococcus aureus encodes a second entertotoxin determinant (sej). FEMS Microbiol Lett 168, 227-233.