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THE PRESENCE OF STAPHYLOCOCCUS AUREUS AND STAPHYLOCOCCAL ENTEROTOXINS IN READY-TO-COOK MEATBALLS AND WHITE PICKLED CHEESE

Year 2006, Volume: 32 Issue: 3, 31 - 39, 21.12.2012

Abstract

ABSTRACT

In this study 30 ready-to-cook meatball and 30 white pickled cheese samples, obtained from different sales outlets in Istanbul, were analysed for the presence of staphylococcal enterotoxins (SE) with the aid of the ELISA technique. Additionally, total Staphylococcus aureus count, DNase positive Staphylococcus aureus count and thermonuclease activity were determined. The meatball samples were found to contain between 3.0x101 and 5.2x104 cfu/g of Staphylococcus aureus while in the white cheese samples, the count varied between <10 - 9.2x103 cfu/g. In 9 meatball samples and 11 white cheese samples, no DNase positive bacteria growth could be detected. Despite these results, SE could not be identified in any of the samples of both food groups, and all samples gave negative results in the thermonuclease test. With respect to Staphylococcus aureus count, 63% of the white cheese samples and 43% of the meatball samples did not comply with Turkish Food Codex. The findings of this study indicate a low microbiological quality of the analysed meatballs and white cheese samples. However, none of the samples conteined staphylococcal enterotoxins.

Keywords: Staphylococcus aureus, enterotoxin, cheese, meatball

HAZIR KÖFTE VE BEYAZ PEYNİRLERDE STAPHYLOCOCCUS AUREUS VE STAFİLOKOKKAL ENTEROTOKSİNLERİN VARLIĞI

ÖZET

Bu çalışmada Staphylococcus aureus yönünden riskli gıdalar arasında yer alan hazır köftelerde (30 adet) ve beyaz peynirlerde (30 adet) ELISA tekniği ile stafilokokkal enterotoksinlerin (SE) varlığı araştırılmıştır. Çalışma materyali İstanbul'daki çeşitli satış noktalarından sağlanmıştır. Örneklerde aynı zamanda toplam Staphylococcus aureus sayısı, DNase pozitif Staphylococcus aureus sayısı ve termonukleaz aktivitesi de belirlenmiştir. Yapılan analizler sonucunda hazır köfte örneklerinde 3.0X101 - 5.2x104 kob/g; beyaz peynir örneklerinde <10 - 9.2x103 kob/g arasinda Staphylococcus aureus saptanmıştır. Hazır köftelerin 9'unda, beyaz peynirlerin 11'inde DNase pozitif bakteri üremesi kaydedilmemiştir. Buna rağmen, her iki gıda grubuna ait örneklerin hiçbirinde SE saptanmamış ve tamamında termonukleaz testi negatif sonuç vermiştir. Staphylococcus aureus sayısı bakımından peynir örneklerinin % 63'u, hazır köfte örneklerinin %43'ü Türk Gıda Kodeksi Yönetmeliği'ne uygunluk göstermemektedir. Bu çalışmada elde edilen bulgular; incelenen köfte ve peynir örneklerinin mikrobiyolojik kalitesi düşük olmakla birlikte stafilokokkal enterotoksinlerin bulundurmadığını göstermektedir.

Anahtar Kelimeler: Staphylococcus aureus, enterotoksin, peynir, köfte

References

  • Bergdoll, M.S.: Staphylococcus aureus. In: Foodborne bacterial pathogens. Ed. Doyle, M.P., New York, Marcel Decker, 1989, 463-523.
  • Chrife, J., Buera, M.P.: Water activity, water glass dynamics and the control of microbiological growth in foods. Crit. Rew. Food Sci. Nutr., 1996; 36(5): 465-513.
  • FDA.: Bacteriological Analytical Manual. Food and Drug Administration (6t h ed.) AOAC Int. Gaithersburg, 1995.
  • Gillespie, I.A., Little, C.L., Mitchell, R.T.: Microbiological examination of ready-to-eat quiche from retail establishments in the United Kingdom. Commun. Dis. Public. Health., 2001; 4(1):53-59.
  • Gomez-Lucia, E., Blanco, J.L., Goyache, J., de la Fuente, R., Vazquez, J.A., Ferri, E.F., Suarez, G.: Growth and enterotoxin A production by Staphylococcus aureus S6 in Manchego type cheese. J. Appl. Bacteriol., 1986; 61(6): 499-503.
  • Gomez-Lucia, E., Goyache, J., Orden, J.A. Domenech, A., Javier Hernandez, J., Ruiz- Santa Quiteria, J.A., Lopez, B., Blanco, J.L., Suarez, G.: Growth of Staphylococcus aureus and synthesis of enterotoxin during ripening of experimental Manchego-type cheese. J. Dairy Sci., 1992; 75(1): 19-26.
  • Göckler, L., Notermans, S., Kramer, J.: Production of enterotoxins and thermonuclease by Staphylococcus aureus in cooked egg-noodles. Int. J. Food Microbiol., 1988; 6(2):127-139.
  • Halpin-Dohnalek, M.I., Marth, E.H.: Staphylococcus aureus: Production of extracellular compounds and behavior in foods - a review. J. Food Prot., 1989; 52 (4): 267-282.
  • Harrigan, W.F.: Laboratory Methods in Food Microbiology. Academic Press, London, 1998.
  • Hobbs, B.C., Roberts, D.: Food Poisoning and Food Hygiene. 5t h ed. Edward Arnold, London, 1987.
  • Isigidi, B.K., Mathieu, A.M., Devriese, L.A., Godard, C., Van Hoof, J . : Enterotoxin production in different Staphylococcus aureus biotypes isolated from food and meat plants. J. Appl. Bacteriol., 1992; 72(1):16-20.
  • Jung, R., Terplan, G. (1993): Strip ELISA for detection for Staphylococcal enterotoxins in culture supernatants and foods. Food Agr. Immunol., 1993; 5, 107-114.
  • Meyrand, A., Boutrand-Loei, S., Ray-Gueniot, S., Mazuy, C., Gaspard, C.E., Jaubert, G., Perrin, G., Lapeyre, C., Vernozy-Rozand, C.: Growth and enterotoxin production of
  • Staphylococcus aureus during the manufacture and ripening of Camembert-type cheeses
  • from raw goats' milk. J. Appl. Microbiol., 1998; 85(3):537-544.
  • Morissette, C., Goulet, J., Lamoreux, G.: Rapid and sensitive sandwich enzyme-linked immunosorbent assay for detection of staphylococcal enterotoxin B in cheese. Appl. Environ. Microbiol., 1991; 57(3): 836-842.
  • Olarte, C., Sanz, S., Gonzalez-Fandos, E., Torre, P.: Microbiological and physicochemical characteristics of Cameros cheese. Food Microbiol., 1999; 16(6): 615-621
  • Park, C.E., Akhtar, M., Rayman, M.K.: Evaluation of a commercial enzyme immunoassay kit (RIDASCREEN) for detection of staphylococcus enterotoxins A, B, C, D and E in Foods.
  • Appl. Environ. Microbiol., 1994; 60: 677-681
  • Park, C.E., Warburton, D., Laffey, P.J.: A collaborative study on the detection of staphylococcal enterotoxins in foods by an enzyme immunoassay kit (RIDASCREEN). Int. J. Food Microbiol., 1996; 29 (2-3): 281-295.
  • Peeva, T., Gogov, I.: Presence of enterotoxin D in Staphylococcus aureus strains isolated from food products. Vet. Med. Nauki., 1983; 20 (8) :67-71.
  • Reibnitz, M.G., Tavares, L.B., Garcia, J.A.: Presence of fecal coliforms, Escherichia coli and DNAse- and coagulase-positive Staphylococcus aureus, in "colonial" cheese sold in the city of Blumenau, Estado de Santa Catarina, Brazil. Rev. Argent. Microbiol., 1998; 30 (1): 8-12.
  • Scheusner, D.L., Hood, L.L., Harmon, L.G.: Effect of temperature and pH on growth and enterotoxin production by Staphylococcus aureus. J. Milk Food Technol., 1973; 36 (5): 249ı 252.
  • Sokari, T.: Distribution of enterotoxigenic Staphylococcus aureus in ready-to-eat foods in eastern Nigeria. Int. J. Food Microbiol., 1991; 12(2-3): 275-279.
  • Tawfek, N.F., Sharaf, O.M., Hewedy, M.M.: Incidence of several pathogens and staphylococcal enterotoxins in Kariesh cheese. Offentl. Gesundheitswes., 1989; 51(1): 272ı 279.
  • Turantaş, F., Ünlütürk, A., Göktan, D.: Microbiological and compositional status of Turkish white cheese. Int.J. Food Microbiol.,1989; 8(1):19-24.
  • Türk Gıda Kodeksi Yönetmeliği.: Mikrobiyolojik Kriterler Tebliği, Resmi Gazete, Sayı: 24511, 2001.
  • Türk Gıda Kodeksi Yönetmeliği.: Taze Et, Hazırlanmış Et ve Hazırlanmış Et Karışımları Tebliği, Resmi Gazete, Sayı: 23960, 2000.
  • Vernozy-Rozand, C., Mazuy, C., Prevost, G., Lapeyre, C., Bes, M., Brun, Y., Fleurette, J.: Enterotoxin production by coagulase-negative staphylococci isolated from goats' milk and cheese. Int. J. Food Microbiol., 1996; 30(3): 271-280.
  • Waites, W.M., Arbuthnott,J.P.: Foodborne Illness. A lancet review. Edward Arnold, London, 1991.
  • Wieneke, A.A., Roberts, D., Gilbert, R.J.: Staphylococcal food poisoning in the United Kingdom, 1969-90. Epidemiol. Infect., 1993; 110(3): 519-531.
Year 2006, Volume: 32 Issue: 3, 31 - 39, 21.12.2012

Abstract

References

  • Bergdoll, M.S.: Staphylococcus aureus. In: Foodborne bacterial pathogens. Ed. Doyle, M.P., New York, Marcel Decker, 1989, 463-523.
  • Chrife, J., Buera, M.P.: Water activity, water glass dynamics and the control of microbiological growth in foods. Crit. Rew. Food Sci. Nutr., 1996; 36(5): 465-513.
  • FDA.: Bacteriological Analytical Manual. Food and Drug Administration (6t h ed.) AOAC Int. Gaithersburg, 1995.
  • Gillespie, I.A., Little, C.L., Mitchell, R.T.: Microbiological examination of ready-to-eat quiche from retail establishments in the United Kingdom. Commun. Dis. Public. Health., 2001; 4(1):53-59.
  • Gomez-Lucia, E., Blanco, J.L., Goyache, J., de la Fuente, R., Vazquez, J.A., Ferri, E.F., Suarez, G.: Growth and enterotoxin A production by Staphylococcus aureus S6 in Manchego type cheese. J. Appl. Bacteriol., 1986; 61(6): 499-503.
  • Gomez-Lucia, E., Goyache, J., Orden, J.A. Domenech, A., Javier Hernandez, J., Ruiz- Santa Quiteria, J.A., Lopez, B., Blanco, J.L., Suarez, G.: Growth of Staphylococcus aureus and synthesis of enterotoxin during ripening of experimental Manchego-type cheese. J. Dairy Sci., 1992; 75(1): 19-26.
  • Göckler, L., Notermans, S., Kramer, J.: Production of enterotoxins and thermonuclease by Staphylococcus aureus in cooked egg-noodles. Int. J. Food Microbiol., 1988; 6(2):127-139.
  • Halpin-Dohnalek, M.I., Marth, E.H.: Staphylococcus aureus: Production of extracellular compounds and behavior in foods - a review. J. Food Prot., 1989; 52 (4): 267-282.
  • Harrigan, W.F.: Laboratory Methods in Food Microbiology. Academic Press, London, 1998.
  • Hobbs, B.C., Roberts, D.: Food Poisoning and Food Hygiene. 5t h ed. Edward Arnold, London, 1987.
  • Isigidi, B.K., Mathieu, A.M., Devriese, L.A., Godard, C., Van Hoof, J . : Enterotoxin production in different Staphylococcus aureus biotypes isolated from food and meat plants. J. Appl. Bacteriol., 1992; 72(1):16-20.
  • Jung, R., Terplan, G. (1993): Strip ELISA for detection for Staphylococcal enterotoxins in culture supernatants and foods. Food Agr. Immunol., 1993; 5, 107-114.
  • Meyrand, A., Boutrand-Loei, S., Ray-Gueniot, S., Mazuy, C., Gaspard, C.E., Jaubert, G., Perrin, G., Lapeyre, C., Vernozy-Rozand, C.: Growth and enterotoxin production of
  • Staphylococcus aureus during the manufacture and ripening of Camembert-type cheeses
  • from raw goats' milk. J. Appl. Microbiol., 1998; 85(3):537-544.
  • Morissette, C., Goulet, J., Lamoreux, G.: Rapid and sensitive sandwich enzyme-linked immunosorbent assay for detection of staphylococcal enterotoxin B in cheese. Appl. Environ. Microbiol., 1991; 57(3): 836-842.
  • Olarte, C., Sanz, S., Gonzalez-Fandos, E., Torre, P.: Microbiological and physicochemical characteristics of Cameros cheese. Food Microbiol., 1999; 16(6): 615-621
  • Park, C.E., Akhtar, M., Rayman, M.K.: Evaluation of a commercial enzyme immunoassay kit (RIDASCREEN) for detection of staphylococcus enterotoxins A, B, C, D and E in Foods.
  • Appl. Environ. Microbiol., 1994; 60: 677-681
  • Park, C.E., Warburton, D., Laffey, P.J.: A collaborative study on the detection of staphylococcal enterotoxins in foods by an enzyme immunoassay kit (RIDASCREEN). Int. J. Food Microbiol., 1996; 29 (2-3): 281-295.
  • Peeva, T., Gogov, I.: Presence of enterotoxin D in Staphylococcus aureus strains isolated from food products. Vet. Med. Nauki., 1983; 20 (8) :67-71.
  • Reibnitz, M.G., Tavares, L.B., Garcia, J.A.: Presence of fecal coliforms, Escherichia coli and DNAse- and coagulase-positive Staphylococcus aureus, in "colonial" cheese sold in the city of Blumenau, Estado de Santa Catarina, Brazil. Rev. Argent. Microbiol., 1998; 30 (1): 8-12.
  • Scheusner, D.L., Hood, L.L., Harmon, L.G.: Effect of temperature and pH on growth and enterotoxin production by Staphylococcus aureus. J. Milk Food Technol., 1973; 36 (5): 249ı 252.
  • Sokari, T.: Distribution of enterotoxigenic Staphylococcus aureus in ready-to-eat foods in eastern Nigeria. Int. J. Food Microbiol., 1991; 12(2-3): 275-279.
  • Tawfek, N.F., Sharaf, O.M., Hewedy, M.M.: Incidence of several pathogens and staphylococcal enterotoxins in Kariesh cheese. Offentl. Gesundheitswes., 1989; 51(1): 272ı 279.
  • Turantaş, F., Ünlütürk, A., Göktan, D.: Microbiological and compositional status of Turkish white cheese. Int.J. Food Microbiol.,1989; 8(1):19-24.
  • Türk Gıda Kodeksi Yönetmeliği.: Mikrobiyolojik Kriterler Tebliği, Resmi Gazete, Sayı: 24511, 2001.
  • Türk Gıda Kodeksi Yönetmeliği.: Taze Et, Hazırlanmış Et ve Hazırlanmış Et Karışımları Tebliği, Resmi Gazete, Sayı: 23960, 2000.
  • Vernozy-Rozand, C., Mazuy, C., Prevost, G., Lapeyre, C., Bes, M., Brun, Y., Fleurette, J.: Enterotoxin production by coagulase-negative staphylococci isolated from goats' milk and cheese. Int. J. Food Microbiol., 1996; 30(3): 271-280.
  • Waites, W.M., Arbuthnott,J.P.: Foodborne Illness. A lancet review. Edward Arnold, London, 1991.
  • Wieneke, A.A., Roberts, D., Gilbert, R.J.: Staphylococcal food poisoning in the United Kingdom, 1969-90. Epidemiol. Infect., 1993; 110(3): 519-531.
There are 31 citations in total.

Details

Primary Language Turkish
Journal Section Research Article
Authors

Kamil Bostan

Ömer Çetin

Serkan Büyükünal This is me

Özer Ergün This is me

Publication Date December 21, 2012
Published in Issue Year 2006 Volume: 32 Issue: 3

Cite

APA Bostan, K., Çetin, Ö., Büyükünal, S., Ergün, Ö. (2012). THE PRESENCE OF STAPHYLOCOCCUS AUREUS AND STAPHYLOCOCCAL ENTEROTOXINS IN READY-TO-COOK MEATBALLS AND WHITE PICKLED CHEESE. İstanbul Üniversitesi Veteriner Fakültesi Dergisi, 32(3), 31-39. https://doi.org/10.16988/iuvfd.72724
AMA Bostan K, Çetin Ö, Büyükünal S, Ergün Ö. THE PRESENCE OF STAPHYLOCOCCUS AUREUS AND STAPHYLOCOCCAL ENTEROTOXINS IN READY-TO-COOK MEATBALLS AND WHITE PICKLED CHEESE. iuvfd. December 2012;32(3):31-39. doi:10.16988/iuvfd.72724
Chicago Bostan, Kamil, Ömer Çetin, Serkan Büyükünal, and Özer Ergün. “THE PRESENCE OF STAPHYLOCOCCUS AUREUS AND STAPHYLOCOCCAL ENTEROTOXINS IN READY-TO-COOK MEATBALLS AND WHITE PICKLED CHEESE”. İstanbul Üniversitesi Veteriner Fakültesi Dergisi 32, no. 3 (December 2012): 31-39. https://doi.org/10.16988/iuvfd.72724.
EndNote Bostan K, Çetin Ö, Büyükünal S, Ergün Ö (December 1, 2012) THE PRESENCE OF STAPHYLOCOCCUS AUREUS AND STAPHYLOCOCCAL ENTEROTOXINS IN READY-TO-COOK MEATBALLS AND WHITE PICKLED CHEESE. İstanbul Üniversitesi Veteriner Fakültesi Dergisi 32 3 31–39.
IEEE K. Bostan, Ö. Çetin, S. Büyükünal, and Ö. Ergün, “THE PRESENCE OF STAPHYLOCOCCUS AUREUS AND STAPHYLOCOCCAL ENTEROTOXINS IN READY-TO-COOK MEATBALLS AND WHITE PICKLED CHEESE”, iuvfd, vol. 32, no. 3, pp. 31–39, 2012, doi: 10.16988/iuvfd.72724.
ISNAD Bostan, Kamil et al. “THE PRESENCE OF STAPHYLOCOCCUS AUREUS AND STAPHYLOCOCCAL ENTEROTOXINS IN READY-TO-COOK MEATBALLS AND WHITE PICKLED CHEESE”. İstanbul Üniversitesi Veteriner Fakültesi Dergisi 32/3 (December 2012), 31-39. https://doi.org/10.16988/iuvfd.72724.
JAMA Bostan K, Çetin Ö, Büyükünal S, Ergün Ö. THE PRESENCE OF STAPHYLOCOCCUS AUREUS AND STAPHYLOCOCCAL ENTEROTOXINS IN READY-TO-COOK MEATBALLS AND WHITE PICKLED CHEESE. iuvfd. 2012;32:31–39.
MLA Bostan, Kamil et al. “THE PRESENCE OF STAPHYLOCOCCUS AUREUS AND STAPHYLOCOCCAL ENTEROTOXINS IN READY-TO-COOK MEATBALLS AND WHITE PICKLED CHEESE”. İstanbul Üniversitesi Veteriner Fakültesi Dergisi, vol. 32, no. 3, 2012, pp. 31-39, doi:10.16988/iuvfd.72724.
Vancouver Bostan K, Çetin Ö, Büyükünal S, Ergün Ö. THE PRESENCE OF STAPHYLOCOCCUS AUREUS AND STAPHYLOCOCCAL ENTEROTOXINS IN READY-TO-COOK MEATBALLS AND WHITE PICKLED CHEESE. iuvfd. 2012;32(3):31-9.