Determination of growth and toxin production potential of Staphylococcus aureus and Clostridium perfringens during döner production process

Determination of growth and toxin production potential of Staphylococcus aureus and Clostridium perfringens during döner production process

Döner is a traditional meat meal that is commonly consumed in Turkey. Although it receives heat treatment during processing,some microorganisms including pathogens may remain alive. Therefore, this study was carried out to determine the changes in thenumber of microorganisms (total aerobic mesophilic bacteria, Enterobacteriaceae, Escherichia coli, aerobic mesophilic spore-formingbacteria, Staphylococcus-Micrococcus spp.) and survival potential of some pathogenic bacteria (Staphylococcus aureus and Clostridiumperfringens) during the cooking period. Experimentally prepared döner kebabs were cooked continuously or intermittently. This processresulted in a reduction of microorganisms depending on the species and the use of low quality raw materials, and a number of bacteriasurvived at significant levels after cooking. The remaining bacteria multiplied and reached unacceptable levels with interrupted heattreatment over a long period of time. However, staphylococcal enterotoxins were not detected in intentionally contaminated samplesthat were kept at room temperature for 18 h after cooking. On the other hand, no significant microbiological changes appeared in rawsections of döner during cooking when the heat source was turned off.

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  • 1. Bartholoma A, Hildebrandt G, Stenzel WR, Erol I. A preliminary investigation of doner kebab in the German market. Fleischwirtschaft 1997; 77: 913-915.
  • 2. Stolle A, Eisgruber H, Kerschhofer D, Krausse G. Döner Kebap: Untersuchungen zur Verkehrsauffassung und mikrobiologischhygienischen Beschaffenheit im Raum München. Fleischwirtschaft 1993; 73: 938-948 (in German).
  • 3. Anar Ş. Döner ve döner üretimi. In: Anar Ş, editor. Et ve Et Ürünleri Teknolojisi. Bursa, Turkey: Dora Press; 2010. pp. 393- 399.
  • 4. Özden E. Effects of tumbling and sodium tripolyphosphate on nutritional quality and yield of döner kebap. MSc, Ankara University, Ankara, Turkey, 2009.
  • 5. Turkish Food Codex. Raw and Processed Meat Compounds. Notification No: 2006/31. Ankara, Turkey: Turkish Food Codex; 2009.
  • 6. Ergezer H, Gökçe R. Kanatlı etlerinin marinasyon tekniği ile işlenmesi. Pamukkale University Journal of Engineering Science 2004; 10: 227-233 (in Turkish).
  • 7. Parks SS, Reynolds AE, Wider L. Aqueous flavoring in breast muscle has physical, chemical and sensory properties similar to those phosphate marinated controls. Poultry Sci 2000; 79: 1183- 1188.
  • 8. Bostan K, Yılmaz F, Muratoğlu K, Aydın A. Pişmiş döner kebaplarda mikrobiyolojik kalite ve mikrobiyel gelişim üzerine bir araştırma. Kafkas Univ Vet Fak 2011; 17: 781-786 (in Turkish).
  • 9. Cebirbay MA. Research on changes in microbiological quality of döner during consumption time. MSc, Selcuk University, Konya, Turkey, 2007.
  • 10. Todd CDE, Szabo R, Spring F. Donairs (Gyros)-potential hazards and control. J Food Protect 1986; 49: 369-377.
  • 11. Dığrak M, Gür S, Özçelik S. Elazığ’da tüketime sunulan dönerlerin mikrobiyolojik kalitesi. Kükem Dergisi 1995; 18: 76 (in Turkish).
  • 12. Elmali M, Ulukanli Z, Tuzcu M, Yaman H, Cavli P. Microbiological quality of beef doner kebabs in Turkey. Arch Lebensmittelhyg 2005; 56: 25-48.
  • 13. Harakeh S, Yassine H, Gharios M, Barbour E, Hajjar S, El-Fadel M, Toufeili I, Tannous R. Isolation, molecular characterization and antimicrobial resistance patterns of Salmonella and Escherichia coli isolates from meat-based fast food in Libanon. Sci Total Environ 2005; 341: 33-44.
  • 14. Jockel J, Stengel G. Döner kebap-Unterschung und Beurteilung einer Turkischen Spezialitat. Fleischwirthschaft 1984; 64: 527- 540 (in German).
  • 15. Kayisoglu S, Yilmaz I, Demirci M, Yetim H. Chemical composition and microbiological quality of the doner kebabs sold in Tekirdağ market. Food Control 2003; 14: 469-474.
  • 16. Küpeli Gençer V, Kaya M. Yaprak dönerlerin mikrobiyolojik kalitesi ve kimyasal bileşimi. Turk J Vet Anim Sci 2004; 28: 1097- 1103 (in Turkish).
  • 17. Topçu S. Antibiotic resistance and isolation of Listeria monocytogenes, Staphylococcus aureus, Aeromonas hydrophila from ‘doner kebap’ varieties offered for consumption in Ankara. MSc, Gazi University, Ankara, Turkey, 2006.
  • 18. Ulukanlı Z, Çavlı P, Tuzcu M. Detection of Escherichia coli O157:H7 from beef doner kebabs sold in Kars. Gazi University Journal of Science 2006; 19: 99-104.
  • 19. Lopašovský L, Terentjeva M, Kunová S, Zeleňáková L, Kačániová M. Microbiological quality of ready-to-eat foods produced in Slovakia. J Microbiol Biotechnol Food Sci 2016; 5: 31-35.
  • 20. Smith JL, Buchanan RL, Palumbo SA. Effect of food environment on staphylococcal enterotoxin synthesis: a review. J Food Prot 1982; 46: 545-555.
  • 21. Loir YL, Baron F, Gautier M. Staphylococcus aureus and food poisoning. Genet Mol Res 2003; 2: 63-76.
  • 22. Bremer PJ, Fletcher GC, Osborne C. Staphylococcus aureus. Auckland, New Zealand: New Zealand Institute for Crop and Food Research Limited; 2004.
  • 23. Fueyo JM, Mendoza MC, Martin MC. Enterotoxins and toxic shock syndrome toxin in Staphylococcus aureus recovered from human nasal carriers and manually handled foods: epidemiological and genetic findings. Microbes Infect 2005; 7: 187-194.
  • 24. Erol İ. Escherichia coli. In: Erol İ, editor. Gıda Hijyeni ve Mikrobiyolojisi. Ankara, Turkey: Pozitif Press; 2007. pp. 78-92.
  • 25. Üzümcüoğlu U. A research on the döner kebaps sold in Ankara markets. MSc, Ankara University, Ankara, Turkey, 2001.
  • 26. Gibbs P. Characteristics of spore-forming bacteria. In: Blackburn CV, McClure PJ, editors. Foodborne Pathogens: Hazards, Risk Analysis and Control. Boca Raton, FL, USA: CRC Press; 2002. pp. 417-435.
  • 27. Tunail N. Clostridium perfringens. In: Tunail N, editor. Gıda Mikrobiyolojisi ve Uygulamaları. Ankara, Turkey: Sim Matbaası; 2000. pp. 1-3.
  • 28. Kamber U, Gökçe HI, Elmalı M. Clostridium perfringens and its toxins in minced meat from Kars, Turkey. Food Addit Contam 2007; 24: 673-678.
  • 29. Vazgecer B, Ulu H, Oztan A. Microbiological and chemical qualities of chicken doner kebab retailed on the Turkish restaurants. Food Control 2004; 15: 261-264.
  • 30. Turkish Food Codex. Communique on Microbiological Criteria, Notification No: 2009/68. Ankara, Turkey: Turkish Food Codex; 2010.
  • 31. Maturin LJ, Peeler JT. Bacteriological Analytical Manual. 8th Edition, Revision A. Rockville, MD, USA: AOAC; 2001.
  • 32. International Organization for Standardization. Microbiology of Food and Animal Feeding Stuffs - Horizontal Method for the Detection and Enumeration of Enterobacteriaceae. Part 2, Colony-Count Technique, 21528-2. Geneva, Switzerland: ISO; 2004.
  • 33. International Organization for Standardization. Horizontal Method for the Enumeration of β-Glucuronidase-Positive Escherichia coli. Part 2, Colony-Count Technique at 44°C using 5-Bromo-4-chloro-3-indoyl-beta-D-glucuronide, 16649. Geneva, Switzerland: ISO; 2001.
  • 34. Harrigan WF. Laboratory Methods in Food Microbiology. London, UK: Academic Press; 1998.
  • 35. Speck MC. Compendium of Methods for the Microbiological Examination of Foods. Washington, DC, USA: American Public Health Association;1976.
  • 36. International Organization for Standardization. Microbiology of Food and Animal Feeding Stuffs-Horizontal Method for the Enumeration of Coagulase-Positive Staphylococci (Staphylococcus aureus and the Species). Part 1, Technique Using Baird Parker Agar Medium, 6888-1. Geneva, Switzerland: ISO; 2003.
  • 37. Baird-Parker AC. The staphylococci: an introduction. J Appl Bacteriol 1990; 69: 1-8.
  • 38. Koneman EW, Allen SD, Janda WM, Schreckenberger PC, Winn WC. Medical bacteriology: taxonomy, morphology, physiology and virulence. In: Procop GW, editor. Color Atlas and Textbook of Diagnostic Microbiology. 6th ed. Philadelphia, PA, USA: Lippincott-Raven Publishers, Philadelphia; 2006. pp. 167-210.
  • 39. International Organization for Standardization. Microbiology of Food and Animal Feeding Stuffs-Horizontal Method for the Enumeration of Clostridium perfringens-Colony-Count Technique, 7937. Geneva, Switzerland: ISO; 2004.
  • 40. SPSS Inc. SPSS for Windows. Rel. 11.0.1. Chicago, IL, USA: SPSS Inc.; 2001.
  • 41. Çoksöyler N, Avşaroğlu MD. Isıl işlemlerle gıdaların korunması. In: Erkmen O, editor. Gıda Mikrobiyolojisi. Ankara, Turkey: Efil Press; 2010. pp. 207-232.
  • 42. Montville TJ, Matthews KR. Principles which influence microbial growth, survival, and death in foods. In: Doyle MP, Beuchat LR, Montville TJ, editors. Food Microbiology: Fundamentals and Frontiers. 2nd ed. Washington, DC, USA: ASM Press; 2001. pp. 13-32.
  • 43. Kolter R, Siegele DA, Tormo A. The stationary phase of the bacterial life cycle. Annu Rev Microbiol 1993; 47: 855-874.
  • 44. Gonulalan Z, Yetim H, Kose A. Quality characteristics of doner kebab made from sucuk dough which is a dry fermented Turkish sausage. Meat Sci 2004; 67: 669-674.
  • 45. Acar MS, Çiftçioğlu GR. Kasaplık hayvan etleri ve tavuk etinden yapılan döner kebapların mikrobiyolojik kalitesi üzerinde bir araştırma. Journal of the Faculty of Veterinary Medicine of İstanbul University 1997; 23: 395-404 (in Turkish).
  • 46. Easa SMH. Microorganisms found in fast and traditional fast food. J Am Sci 2010; 6: 515-531.
  • 47. Nemati M, Ghorbanpour Razavieh SV, Hoseini M. Chemical composition and microbiological quality of the bona kebabs sold in Tabriz market. J Food Safety 2008; 28: 315-323.
  • 48. Yuksek N, Evrensel SS, Temelli S, Anar S, Sen MKC. A microbiological evaluation on the ready-to-eat red meat and chicken donair kebabs from a local catering company in Bursa. J Environ Biol 2009; 3: 7-10.
  • 49. Jay JM. Bacterial biota (flora) in foods. In: Hui YH, Pierson MD, Gorham JR, editors. Foodborne Disease Handbook, Revised and Expanded, Volume 1: Bacterial Pathogens Science Technology System. 2nd ed. New York, NY, USA: Marcel Dekker; 2001. pp. 23-34.
  • 50. Ismail SA. Microbiological quality of hawawshy consumed in Ismailia. J Food Safety 2006; 26: 251-263.
  • 51. Kruger J, Schulz V, Kuntzer J. Doner kebab Unterschungen zum Handelsbrauch in Stuttgart. Fleischwirthsch 1993; 73: 1242- 1248 (in German).
  • 52. Lancette GA, Bennett RW. Staphylococcus aureus and staphylococcal enterotoxins. In: Downes FP, Ito K, editors. Compendium of Methods for the Microbiological Examination of Foods. Washington, DC, USA: American Public Health Association; 2001. pp. 387-400.
  • 53. Uğur M, Nazlı B, Bostan K. Escherichia coli. In: Uğur M, Nazlı B, Bostan K, editors. Gıda Hijyeni. İstanbul, Turkey: Teknik Yayınları; 2003. pp. 41-44.
  • 54. Jay JM. Intrinsic and extrinsic parameters of foods that affect microbial growth. In: Jay JM, editor. Modern Food Microbiology. Gaithersburg, MD, USA: Aspen; 2000. pp. 35-56.
  • 55. Yilmaz I, Arici M, Gumus T. Changes of microbiological quality in meatballs after heat treatment. Eur Food Res Technol 2005; 221: 281-283.
  • 56. Hampikyan H, Ulusoy B, Bingöl EB, Çolak H, Akhan M. İstanbul’da tüketime sunulan bazı ızgara tipi gıdalar ile salata ve mezelerin mikrobiyolojik kalitelerinin belirlenmesi. Türk Mikrobiyoloji Cemiyeti Dergisi 2008; 38: 87-94 (in Turkish).
  • 57. Jansson E, Bird P, Saputra T, Arnold G. Food safety survey of retail doner kebabs in NSW. Food Australia 2008; 60: 95-98.
  • 58. Bergdoll MS. Staphylococcus aureus. In: Doyle MP, editor. Foodborne Bacterial Pathogens. New York, NY, USA: Marcel Dekker; 1989. pp. 463-523.
  • 59. Jay JM. Staphylococcal gastroenteritis. In: Jay JM, editor. Modern Food Microbiology. Gaithersburg, MD, USA: Aspen; 2000. pp. 441-459.
  • 60. Mossel DAA, Van Nette P. Staphylococcus aureus and related staphylococci in foods: ecology, proliferation, toxinogenesis, control and monitoring. J Appl Bacteriol, Symp Sup 1990; 69: 123-145.
  • 61. Uğur M, Nazli B, Bostan K. Staphylococcus aureus. In: Uğur M, Nazlı B, Bostan K, editors. Gıda Hijyeni. İstanbul, Turkey: Teknik Yayınları; 2003. pp. 52-55.
  • 62. Murmann D, Lenz FC, Maydell AV. “Gyros” ein Erzeugnis aus Rohem und zerkleinertem Schweinefleisch. Fleischwirthschaft 1985; 65: 685-690 (in German).
  • 63. Corzo-Martinez M, Corzo N, Villamiel M. Biological properties of onions and garlic. Trends Food Sci Technol 2007; 18: 609- 625.
  • 64. Wilson EA, Demmig Adams B. Antioxidant, anti-inflammatory and antimicrobial properties of garlic and onions. Nutrition & Food Science 2007; 37: 178-183.
  • 65. Hughey VL, Johnson EA. Antimicrobial activity of lysozyme against bacteria involved in food spoilage and food-borne disease. J Appl Environ Microbiol 1987; 53: 2165-2170.
  • 66. Gill AO, Holley RA. Surface applications of lysozyme, nisin, and EDTA to inhibit spoilage and pathogenic bacteria on ham and bologna. J Food Protect 2000; 63: 1338-1346.
  • 67. Ibrahim HR, Matsuzaki T, Aoki T. Genetic evidence that antibacterial activity of lysozyme is independent of its catalytic function. FEBS Lett 2001; 506: 27-32.
  • 68. Brady D, Gaines S, Fenelon L, McPartlin J, O’Farrelly CA. A lipoprotein derived antimicrobial factor from hen-egg yolk is active against Streptococcus species. J Food Sci 2002; 67: 3096- 3103.
  • 69. International Commission on Microbiological Specifications for Foods. Microorganisms in Foods 6: Microbial Ecology of Food Commodities. 2nd ed. New York, NY, USA: Kluwer Academic/Plenum Publishers; 2005.
  • 70. Bryan FL, Standley SR, Henderson WC. Time-temperature conditions of gyros. J Food Protect 1980; 43: 346-353.
  • 71. Adams MR, Moss MO. Staphylococcus aureus. In: Adams MR, Moss MO, editors. Food Microbiology. 2nd ed. Cambridge, UK: Royal Society of Chemistry; 2000. pp. 205-210.
  • 72. Crouch EA, Labarre D, Golden NJ, Kause JR, Dearfield KL. Application of quantitative microbial risk assessments for estimation of risk management metrics: Clostridium perfringens in ready-to-eat and partially cooked meat and poultry products as an example. J Food Prot 2009; 72: 2151- 2161.
  • 73. McClane BA. Clostridium perfringens. In: Doyle MP, Beuchat LR, Montville TJ, editors. Food Microbiology: Fundamentals and Frontiers. 2nd ed. Washington, DC, USA: ASM Press; 2001. pp. 351-372.
  • 74. Labbe RG, Juneja VK. Clostridium perfringens gastroenteritis. In: Riemann HP, Cliver DO, editors. Foodborne Infections and Intoxications. 3rd ed. Oxford, UK: Academic Press; 2006. pp. 137-164.
  • 75. Wrigley DM. Clostridium perfringens. In: Hui YH, Pierson MD, Gorham JR, editors. Foodborne Disease Handbook, Revised and Expanded Volume 1: Bacterial Pathogens Science Technology System. 2nd ed. New York, NY, USA: Marcel Dekker; 2001. pp 139-168.
  • 76. Jablonski LM, Bohach GA. Staphylococcus aureus. In: Doyle MP, Beuchat LR, Montville TJ, editors. Food Microbiology: Fundamentals and Frontiers. 2nd ed. Washington, DC, USA: ASM Press; 2001. pp. 411-434.
  • 77. Qi Y, Miller KJ. Effect of low water activity on staphylococcal enterotoxin A and B biosynthesis. J Food Protect 2000; 63: 473- 478.
  • 78. Batish VK, Nataraj B, Grover S. Variation in the behaviour of enterotoxigenic Staphylococcus aureus after heat stress in milk. J Applied Bacteriol 1989; 66: 27-35.