Francesca PEDONESE, Carlo D'ASCENZI, Beatrice TORRACCA, Clizia ZINGONI, Barbara TURCHI, Filippo FRATINI, Roberta NUVOLONI

Staphylococcus aureus growth and enterotoxin production in Italian caciotta cheese

To evaluate growth and enterotoxin production of Staphylococcus aureus in raw milk caciotta, an Italian soft cheese, experimental cheesemaking trials were carried out with and without a commercial starter. Two different inocula of selected enterotoxin-producing S. aureus strains were tested: high (mean value 5.03 log CFU/mL of milk) and low (mean value 3.22 log CFU/mL of milk). Uninoculated cheeses with milk containing 2.15 log CFU/mL mean value of coagulase-positive staphylococci were also examined. With higher inocul a coagulase-positive staphylococci counts reached 7.57 log CFU/g without starter and had significantly higher values after the acidification phase than those with starter (below 6.5 log CFU/g). Using an enzyme immunoassay, enterotoxins were detected in cheeses both without and with starter, but the latter showed significantly lower photometrical absorbance values than the former. In low inoculum and uninoculated cheeses without starter, coagulase-positive staphylococci maximum values were between 5 and 6 log CFU/g, without enterotoxin production. To enhance the safety of this cheese it is fundamental to strictly prevent coagulase-positive staphylococci contamination and multiplication, particularly at the primary production level, and to correctly acidify the curd by starter cultures, which can substantially limit total coagulase-positive staphylococci increase.

Anahtar Kelimeler:

Key words: Caciotta cheese, enterotoxin production, experimental cheesemaking process, Staphylococcus aureus

Staphylococcus aureus growth and enterotoxin production in Italian caciotta cheese

Keywords:

Key words: Caciotta cheese, enterotoxin production, experimental cheesemaking process, Staphylococcus aureus,

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Salvadori del Prato O. Trattato di Tecnologia Casearia. Bologna, Italy: Edagricole–Edizioni Agricole, 1998 (in Italian).
Halpin-Dohnalek M, Marth E. Staphylococcus aureus: production of extracellular compounds and behaviour in foods: a review. J Food Protect 1989; 52: 267–282.
Vasudevan P, Mohan Nair MK, Annamalai T, Venkitanarayanan KS. Phenotypic and genotypic characterization of bovine mastitis isolates of Staphylococcus aureus for biofilm formation. Vet Microbiol 2003; 92: 179–185.
Gill JJ, Pacan JC, Carson ME, Leslie KE, Griffiths MW, Sabour PM. Efficacy and pharmacokinetics of bacteriophage therapy in treatment of subclinical Staphylococcus aureus mastitis in lactating dairy cattle. Antimicrob Agents Chemother 2006; 50: 2912–2918.
De Buyser ML, Dufour B, Maire M, Lafarge V. Implication of milk and milk products in food-borne diseases in France and in different industrialised countries. Int J Food Microbiol 2001; 67: 1–17.
Kerouanton A, Hennekinne JA, Letertre C, Petit L, Chesneau O, Brisabois A, De Buyser ML. Characterization of Staphylococcus aureus strains associated with food poisoning outbreaks in France. Int J Food Microbiol 2007; 115: 369–375.
Cretenet M, Even S, Le Loir Y. Unveiling Staphylococcus aureus enterotoxin production in dairy products: a review of recent advances to face new challenges. Dairy Sci Technol 2011; 91: 127–150.
Tatini SR, Jezeski JJ, Morris HA, Olson JC, Casman EP. Production of staphylococcal enterotoxin A in Cheddar and Colby cheeses. J Dairy Sci 1971; 54: 815–825.
Gomez-Lucia E, Goyache J, Orden JA. Growth of Staphylococcus aureus and synthesis of enterotoxin during ripening of experimental Manchego-type cheese. J Dairy Sci 1992; 75: 19–26.
Bachmann HP, Spahr U. The fate of potentially pathogenic bacteria in Swiss hard and semihard cheeses made from raw milk. J Dairy Sci 1995; 78: 476–483.
Vernozy-Rozand C, Meyrand A, Mazuy C, Delignette-Muller ML, Jaubert G, Perrin G, Lapeyre C, Richard Y. Behaviour and enterotoxin production by Staphylococcus aureus during the manufacture and ripening of raw goats’ milk lactic cheeses. J Dairy Res 1998; 65: 273–281.
Daminelli P. Dynamics of the survival of Staphylococcus aureus in Crescenza and Italico cheeses artificially contaminated. Selezione Veterinaria 1999; 11: 819–829 (article in Italian with an English abstract).
Meyrand A, Vernozy-Rozand C, Gonthier A, Mazuy C, Ray-Gueniot S, Jaubert G, Perrin G, Lapeyre C, Richard Y. Main differences in behavior and enterotoxin production of Staphylococcus aureus in two different raw milk cheeses. Rev. Méd Vét 1999; 150: 271–278.
Delbes C, Alomar J, Chougui N, Martin JF, Montel MC. Staphylococcus aureus growth and enterotoxin production during the manufacture of uncooked, semihard cheese from cows’ raw milk. J Food Protect 2006; 69: 2161–2167.
Pexara A, Solomakos N, Sergelidis D, Govaris A. Fate of enterotoxigenic Staphylococcus aureus and staphylococcal enterotoxins in Feta and Galotyri cheeses. J Dairy Res 2012; 79: 405–413.
Kalorey DR, Shanmugam Y, Kurkure NV, Chousalkar KK, Barbuddhe SB. PCR-based detection of genes encoding virulence determinants in Staphylococcus aureus from bovine subclinical mastitis cases. J Vet Sci 2007; 8: 151–154.
Johnson WM, Tyler SD, Ewan EP, Ashton FE, Pollard DR, Rozee KR. Detection of genes for enterotoxins, exfoliative toxins and toxic shock syndrome toxin 1 in Staphylococcus aureus by the polymerase chain reaction. J Clin Microbiol 1991; 29: 426–430.
UNI EN ISO Standard 6888-1:2000. Microbiology of food and animal feeding stuffs. Horizontal method for the enumeration of coagulase-positive staphylococci (Staphylococcus aureus and other species). Technique using Baird-Parker agar medium (in Italian).
Intesa tra il Governo e le Regioni in materia di vendita di latte crudo per l’alimentazione umana n. 5 del 25-01-2007.
Supplemento alla Gazzetta Ufficiale della Repubblica Italiana n. 36 del 13-02-2007 (in Italian).
Commission Regulation EC No. 1441/2007 of 5 December 2007 amending Regulation (EC) No. 2073/2005 on microbiological criteria for foodstuffs. Official Journal of the European Union L322/12, 07-12-2007.
Meyrand A, Vernozy-Rozand C. Croissance et entérotoxinogenèse de Staphylococcus aureus dans différents fromages. Rev. Méd. Vét. 1999; 150: 601–616 (article in French with an English abstract).
Iandolo JJ, Clark CW, Bluhm L, Ordal ZJ. Repression of Staphylococcus aureus in associative culture. Appl Microbiol 1965; 13: 646–649.
Haines WC, Harmon LG. Effect of selected lactic acid bacteria on growth of Staphylococcus aureus and production of enterotoxin. Appl Microbiol 1973; 436–441.
Stadhouders J, Cordes MMO, Schouwenburg-van Foeken AWJ. The effect of manufacturing conditions on the development of staphylococci in cheese. Their inhibition by starter bacteria. Neth Milk Dairy J 1978; 32: 193–203.
Chordash RA, Potter NN. Stability of staphylococcal enterotoxin A to selected conditions encountered in foods. J Food Sci 1976; 41: 906–909.
Harris TO, Hufnagle WO, Betley MJ. Staphylococcal enterotoxin type A internal deletion mutants: serological activity and induction of T-cell proliferation. Infect Immun 1993; 61: 2059–2068.
Metzroth B, Marx T, Linnig M, Fleischer B. Concomitant loss of conformation and superantigenic activity of staphylococcal enterotoxin B deletion mutant proteins. Infect Immun 1993; 61: 2445–2452.