Conditions of staphylococcal enterotoxin production in milk and milk products
Résumé
The authors reviewed the existing scientific data, concerning the ability of Staphylococcus aureus to grow and produce enterotoxins in milk and in dairy products particularly in cheeses. S. aureus can grow well in liquid raw or pasteurized milks and produce enterotoxins if the product is stored in favorable for the pathogen temperature. Cream also supports growth of S. aureus and enterotoxin production, but butter as well as fermented products like yogurt and buttermilk are not favorable substrates for the production of enterotoxins. Cheeses represent a complex environment, due to their great variety in processing technology and environment. Fresh cheeses, soft cheeses and semi-hard and hard cheeses can support growth of S. aureus during the first stages of production up to 48 hours. Normally, the pathogen, if it is present in the milk, will multiply for 3-4 logs and after that, when acidity develops, the populations of S. aureus decrease and usually disappear by the end of the ripening period. However, if enterotoxins are produced during the multiplication phase of the pathogen, it will remain active in the cheese for a long time. Internal mould ripened cheeses (e.g. blue cheese), pasta filata cheeses or the processed cheeses do not represent favorable substrates for the multiplication of S. aureus and enterotoxin production. On the contrary, whey cheeses form a very favorable environment for the enterotoxins' production, because of their high pH and the absence of antagonistic bacterial flora.
Article Details
- Comment citer
-
MANTIS (Α.Ι. ΜΑΝΤΗΣ) A. J., & PAPAGEORGIOU (Δ.Κ. ΠΑΠΑΓΕΩΡΓΙΟΥ) D. K. (2017). Conditions of staphylococcal enterotoxin production in milk and milk products. Journal of the Hellenic Veterinary Medical Society, 54(3), 242–252. https://doi.org/10.12681/jhvms.15267
- Numéro
- Vol. 54 No 3 (2003)
- Rubrique
- Review Articles
Authors who publish with this journal agree to the following terms:
· Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution Non-Commercial License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
· Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g. post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
· Authors are permitted and encouraged to post their work online (preferably in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.
Téléchargements
Les données relatives au téléchargement ne sont pas encore disponibles.
Références
Adesiyun ΑΑ, Tatini SR, Hoover DG (1984). Production of enterotoxins by Staphylococcus hyicus. Vet. Microbiol. 9:487-495.
Ahmed A A-H, Mustafa MK, Marth EH (1983). Growth and survival of Staphylococcus aureus in Egyptian Domiati cheese. J. Food Prot. 46:412-415.
Anifantakis FM (1991). Greek cheese: A tradition of centuries. National Dairy Committee of Greece. Athens.
Anonymous (2001). Staphylococcus food poisoning in Japan. IARS, 22,185-186.
Anunciacao LLC, Linardi WR, Docarnco LS, Bergdoll MS (1994). Production of Staphyloccocal enterotoxin in a white cheese. Revista de Microbiologia 25:68-71.
Asao Τ, Kumeda Y, Kawai Τ, Shibata Τ, Oda Η, Haruki Κ, Nakazawa H, Kozaki S (2003). An extendive 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.
Asperger H (1994). Staphylococcus aureus. In "The significance of pathogenic microorganisms in raw milk" Int. Dairy Federation, Bulletin 9405 (S.I.)•
Asperger H, Zangerl Ρ (2002). Staphylococcus aureus. In Encyclopedia of Dairy Sciences (eds. Roginski, H., Fuquay, J.W., Fox, P.) Academic press, Elsevier Science, London, p. 2563-2569.
Batish VK, Chander Η (1987). Occurrence of Staphylococcus aureus and their preformed enterotoxins in frozen dairy desserts. Aust J. Dairy Technol. 42:22-24.
Becker K, Keller B, Von Eiff C, Brück M, Lubritz G, Etienne J, Petrs G (2001). Enterotoxigenic potential of Staphylococcus intermedius. Appi. Environ. Microbiol. 67,12,5551-5557.
Bennet RW, Amos WT (1983). Staphylococcus aureus growth and toxin production in Imitation cheeses. J. Food Sci. 48:1670-1673.
Boer E, KM D (1987). A survey of the microbiological quality of blue veined cheeses. Neth. Milk dairy L. 41:227-237.
Buia CJ, Bolle J, Glausez MP (1995). An epidemic of foodborne listeriosis in Western Switzerland: description of 57 cases involving adults. Clin. Inf. Dis. 20-66.
CDC (Center for Disease Control) (1970). Staphylococcal food poisoning traced to butter. Alabama. Morb. Mort. Weekly Rep. 19:217.
Chopin A, Mocquot G, Le Great Τ (1977). Destruction de Microbacterium lacticum, Escherichia coli et Staphylococcus aureus au cours du lait par atomization. IL Influence des conditions de séchage. Can J. Microbiol 23:755-763.
Chopin A, Tesone S, Vila J-P, Le Graet Y, Mocquot G (1978). Survie de Staphylococcus aureus au cours de la preparation et de la conservation de lait ecreme en poudre. Problèmes poses par le dénombrement des survivants. Can J. Microbiol. 24:1371.
Clark WS and Nelson FE (1961). Multiplication of coagulase positive staphylococci in grade A raw milk samples. J. Dairy Sci. 44:232-236.
Daminelli Ρ, (1999). Dinamica della sopravivenza di Staphylococcus aureus in fromaggi tipo crescenza ed Italico artificialmente contaminati. Le Selezione Veterinaria, 11/815-829.
De Buyser ML et Lapeyre C (1995). Inventane des souches isolées de 5 types de fromages au lait cru: le méthodes d' analyse, le dénombrement de Staphylococcus aureus, le détection des toxines. In "Compte-rendu de la journée Thématique Staphylocoques". ARILAIT-Recherches, 30 Mars 1995. Paris. pp.67-72.
Dengremeont E, Vincent JP, Catteau M (1995). Comportement de souches de Staphylococcus aureus en expérimentation planifiée. Croissance et production de toxins. In "Compte-rendu de la journée Thématique Staphylocoques". ARILAIT-Recherches, 30 Mars 1995. Paris, pp.73-87.
Donnelly CB, Lesli JE, Black LA (1968). Production of enterotoxin A in milk. Appi. Microbiol. 16:917-924.
Erkmen Ο (1995). Behavior of Staphylococcus aureus in Turkish feta cheese during manufacturing and ripening. J. Food Prot. 58:1201-1205
Evenson ML, Hinds, MW, Berstein RS, Bergdoll MS (1988). Estimation of human dose of staphylococcal enterotoxin A from a large outbreak of staphylococcal food poisoning, involving
chocolate milk. Int. J. Food Microbiol., 7, 311-316.
FAO/WHO (1973). Code of principles concerning milk and milk products. International standard and standard methods of sampling and analysis for milk products. 7th Edit. FAO, CAC/M-1,1973. Rome.
Fonteca J, Pelaez C, Juarem M, Requena T, Gomez C, Ramos M (1990). Biochemical and microbiological characteristics of artisanal hard goat's cheese. J. Dairy Sci. 73:1150-1157.
Galesloot TE, Stadhouders J (1968). The microbiology of spray dried milk products with special reference to Staphylococcus aureus and Salmonella. Neth. Milk. Dairy J. 22:158-172.
Genigeorgis CA (1989). Present state of knowledge on staphylococcal intoxication. Int. J. Food Microbiol., 9, 327-360.
Glass KA, Kaufman KM, Johnson EA (1998). Survival of bacterial pathogens in pasteurized process cheese slices stored at 30oC. J. Food Prot. 61:290-294.
Gogov Y, Slavchev G, Peeva Τ (1984). Cold resistance of S. aureus and A and C2 staphylococcus enterotoxins in ice cream. Vet. Sci. (Sofia), 21:46.
Gomez-Lucia E, Goyache J, Orden JA, Domenech A, Hernandez FJ, Quiteria JAR, Lopez B, Blanco JL, Suarez Q (1992). Growth of Staphylococcus aureus and synthesis of enterotoxin during ripening of experimental Manchego-type cheese. J. Dairy Sci. 75:19-26.
Halpin MI, Marth EH (1986). Growth and enterotoxin production by Staphylococcus aureus in cream with various amounts of milk fat. J. Food Prot. 49:851.
Hamama A, El Hankouri N, El Ay adi M, (2002). Fate of enterotoxigenic Staphylococcus aureus in the presence of nisin producing Lactococcus lactis strain during manufacture of Iben, Maroccan traditional fresh cheese. Int. Dairy J. 12:933-938.
Hoffner F (1996). Staphylococcus aureus en fabrication de Reblochon. Thèse de Doctorat Vétérinaire. Nantes.
Ibrahim GF, Baldock AK, Radford DR, Ireland LB (1981a). Inhibition of Staphylococcus aureus growth and enterotoxin A production in Cheddar cheese produced with variable starter activity. J. Food Prot. 44:263-267.
Ibrahim GF, Radford DR, Baldock AK, Ireland LB (1981b). Inhibition of growth of Staphylococcus aureus and enterotoxin A production in Cheddar cheese produced with induced starter failure. J. Food Prot. 44:189-193.
ICMSF (International Commission on Microbiological Specifications for Foods) (1996). Microorganisms in Food 5: Characteristics of Microbial Pathogens. Blackie Academic and Professional, London. Klwers Academic/Plenum Publishers, New York.
Staphylococcus aureus, Ch. 17, pp. 299-333.
Ikram M, Leudecke Ο (1977). Growth and enterotoxin A production by Staphylococcus aureus in fluid dairy products. J. Food Prot. 40:769-771.
Johnson EA, Nelson JH, Johnson M (1990). Microbiological safely of cheese made from heat treated milk, part II. Microbiology. J. Food Prot. 53:519-540.
Karaioannoglou Pr, Koidis P, Mantis A (1983). Growth and enterotoxin production by Staphylococcus aureus in whey cheese Manouri. Acta Microbiologica Hellenica 28:86-95.
Koening S, Marth EH (1982). Behavior of Staphylococcus aureus in Cheddar cheese made with sodium chloride or mixture of sodium chloride and potassium chloride. J. Food Prot. 45:996-1002.
Kosikowski FW, Mistry VV (1997). Cheese and fermented milk foods (F.V. Kosikowski, L.L.C., Pubis, Westport. Conn). Letondeur-Lafarge V, Lahellec C (1997). Aspects hygiénique. (In "Le
Fromage". Techn. Et Doc. Lavoisier, Paris, pp. 741-755.
Lodi R, Malaspina P, Brasca M, (1994). Lactic acid bacteria: a quality parameter for fresh cheese. Industria del latte. 30:3-16.
Lopez-Diaz TM, Santos JA, Gonzales CJ, Moreno B, Garcia M (1995). Bacteriological quality of a traditional Spanish Blue cheese. Milchwissenschaft, 50:503-505.
Mantis A (1973). Production of staphylococcal enterotoxins in whitebrined cheese Feta. Docent-Doctoral Thesis. School of Vet. Med. Univ. Thessaloniki (in Greek).
Massa S, Poda G, Cesaroni D, Trovatelli LD, (1989). A bacteriological survey of ice-cream. Food Microbiol. 6:129.
Medina M, Gaya P, Nunez M (1992). Gredos goat's milk cheese: microbiological and chemical changes throughout ripening. J. Dairy Res. 59:563-566.
Meyrand A, Boutrand-Loei S, Ray-Gueniot S, Mazuy C, Gaspard CE, Jaubert G, Perrin G, Lapeyre C, Vernory-Rozand C (1998). Growth and enterotoxin production of Staphylococcus aureus during the manufacture and ripening of Camembert type cheeses from raw goat's milk. J. Appi. Microb. 85:537-544.
Meyrand A, Vernozy-Rozand (1999). Croissance et enterotoxinogenese de Staphylococcus aureus dans different fromages. Revue Med. Vet. 150:601-616.
Minor TE, Marth EH (1970). Growth of Staphylococcus aureus in acidified pasteurized milk. J. Milk Food Technol. 33:516.
Minor TE, Marth EH (1972). Fate of Staphylococcus aureus in cultured buttermilk, sour cream and yogurt during storage. J. Milk and Food Technol. 35:302-306.
Minor TE, Marth EH (1972a). Loss of viability by Staphylococcus aureus in acidified media. Inactivation by several acids, mixtures of acids and salts of acids. J. Milk Food Technol. 35:191-196.
Minor TE, Marth EH (1972b). Staphylococcus aureus and enterotoxin A in cream and butter. J. Dairy Sci. 55:1410-1414.
Mueller M, Hahn G, Heeschen W (1996). Multiplication and production of enterotoxin by Staphylococcus aureus during the experimental manufacture of Camenbert cheese. Kieler Milchwirt-schaftliche-ferschungsberichte, 48:195-207.
Naguib MM, Nour MA, Noaman AA (1979). Survival of Staphylococcus aureus in Ras cheese. Arch. Lebensmittelhygiene, 30:227-228.
Nunez M, Medina M (1980). Les microcoques et les staphylocoques dans le fromage blue de Cabrabes. Le Lait, 60:171-183.
Papageorgiou DK, Abrahim A, Bori M, Doudounakis S (1998). Chemical and bacteriological characteristics of Pichtogalo Chanion cheese and mesophilic starter cultures for its production. J. Food Prot. 61:688-692.
Provent C (1986). Contribution a Γ étude de Γ origine et de la maîtrise de la contamination du fromage Mont d' Or par Staphylococcus aureus. Thèse de Doctorat Vétérinaire, Lyon, 1986.
Reiter B, Fewins BG, Fryer TF, Sharpe ME (1964). Factors affecting the multiplication and survival of coagulase positive staphylococci in Cheddar cheese. J. Dairy Res. 31:261-272.
Ryser ET (1998). Public Health Concerns. In "Applied Dairy Microbiology". E.H. Marth and J.L. Steele, eds. Marcel Dekker. Inc. New York.
Santos EC, Genigeorgis C (1981). Survival and growth of Staphylococcus aureus in commercially manufactured Minas cheese. J. Food Prot. 44:177-184.
Scott R (1986). Cheesemaking proctice. 2nd Edition. Elsevier Appi. Sci. Publisher. London, 1986.
Tamminga SK, Beumer RR, Kampelmacher EH (1980). Bacteriological examination of ice-cream in the Netherlands. Comperative studies on methods. J. Appi. Bacteriol. 49:239-253.
Tatini SP, Jezeski JJ, Olson JC, Casman EP (1971b). Factors influencing the production of staphylococcal enterotoxin A in milk. J. Dairy Sci., 54,312-320.
Tatini SR (1973). Influence of food environments on growth of Staphylococcus aureus and production of various enterotoxins. J. Milk Food TechnoL, 36,559-563.
Tatini SR, Jezeski JJ, Morris HA, Oslon JCJr, and Casman EP (1971a). Production of Staphylococcus enterotoxin A in Cheddar and Colby cheeses. J. Dairy Sci. 54:815-825.
Tatini SR, Soo HM, Cords BR, Bennett RW (1975). Heat stable nuclease for assessment of staphylococcal growth and likely presence of enterotoxins in foods. J. Food Sci. 40:352-356.
Tatini SR, Wesala WD, Jejeski JJ, Morris HA (1973). Production of Staphylococcal enterotoxin A in Blue, Brick, Mozzarella and Swiss cheeses. J. Dairy Sci. 56:429-435.
Tham WA, Hadju LJ, Danielson-Tham V (1990). Bacteriological quality of farm manufactured goat cheese. Epidemiol. Infect. 104:87-100.
Van Schouwenburg-Van Foeken AW, Stadhouders JJ, Witsenburg WW (1978). The number of enterotoxigenic Staphylococcus aureus reached in Gouda cheese made under normal acedification conditions and the amount of enterotoxin produced. Neth. Milk Dairy J. 33:49-59.
Vernozy-Rozand C, Meyrand A, Mazny C, Delignette-Muller ML, Jaubert G, Perrzin G, Lapeyer C, Richard Y (1998). Behaviour and enterotoxin production by Staphylococcus aureus during the
manufacture and ripening of raw goat's milk lactic cheeses. J. Dairy Res. 65:273-281.
WHO Surveillance programme for control of foodborn infections and intoxications in Europe 1993-1998. 7th report.
Zarate V, Belda F, Perez C, Cardell E (1997). Changes in the microbial flora of Tenerife goats milk cheese during ripening. Int. Dairy J. 7:635-641.
