Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-27T04:21:24.438Z Has data issue: false hasContentIssue false
  • English
  • Français

Fate of enterotoxigenic Staphylococcus aureus and staphylococcal enterotoxins in Feta and Galotyri cheeses

Published online by Cambridge University Press:  31 July 2012

Andreana Pexara ,
Nikolaos Solomakos ,
Daniil Sergelidis  and
Alexandros Govaris
Andreana Pexara
Affiliation:
Laboratory of Hygiene of Foods of Animal Origin, Faculty of Veterinary Medicine, University of Thessaly, 224 Trikalon Street, 43100 Karditsa, Greece
Nikolaos Solomakos
Affiliation:
Laboratory of Hygiene of Foods of Animal Origin, Faculty of Veterinary Medicine, University of Thessaly, 224 Trikalon Street, 43100 Karditsa, Greece
Daniil Sergelidis
Affiliation:
Laboratory of Hygiene of Foods of Animal Origin, Department of Hygiene and Technology of Foods of Animal Origin, Faculty of Veterinary Medicine, Aristotle University of Thessaloniki, Thessaloniki, Greece
Alexandros Govaris*
Affiliation:
Laboratory of Hygiene of Foods of Animal Origin, Faculty of Veterinary Medicine, University of Thessaly, 224 Trikalon Street, 43100 Karditsa, Greece Institute of Technology and Management of Agricultural Ecosystems (ITEMA), Center for Research and Technology, Thessaly (CERETETH), Karditsa, Greece
*
*For correspondence; e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

In this study the fate of enterotoxigenic Staphylococcus aureus and staphylococcal enterotoxins in Feta and Galotyri cheeses were studied. Initially, the enterotoxigenic abilities of four Staph. aureus LHA, LHB, LHC and LHD strains isolated from raw ovine milk were examined in both BHI broth and ovine milk. In BHI broth, the Staph. aureus LHA, LHB, LHC and LHD strains were found toxigenic at 37 °C producing the staphylococcal enterotoxins (SEs) serotypes SEA, SEB, SEC and SED, respectively, whereas in ovine milk at 37 °C, Staph. aureus LHD was found to produce only SED, while no SE production was observed for the other examined strains. Thus, the fate of only Staph. aureus LHD and SED were examined in Feta and Galotyri cheeses. The cheeses were made from raw ovine toxic milk with preformed SED or raw ovine milk contaminated with high (ca 6 log cfu/ml) and low inocula (ca 3 log cfu/ml) of Staph. aureus LHD. Results showed that the pathogen was eliminated at slower rate in Galotyri cheese than in Feta cheese, for the high (5 d vs. 16 d) or the low (1 d vs. 12 d) inoculum trials. In both cheeses produced from the toxic milk, SED was detected during manufacturing and storage. SED was also detected in the curd (2 h), when Staph. aureus LHD populations had reached ca 7 log cfu/g, and up to the end of storage for the high inoculum trials of both cheeses. No SED was observed for the low inoculum trials of either cheese.

Keywords

CheesesFetaGalotyristaphylococcal enterotoxinsStaphylococcus aureus
Type
Research Article
Information
Journal of Dairy Research , Volume 79 , Issue 4 , November 2012 , pp. 405 - 413
Copyright
Copyright © Proprietors of Journal of Dairy Research 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Akineden, O, Hassan, AA, Schneider, E & Usleber, E 2008 Enterotoxigenic properties of Staphylococcus aureus isolated from goats’ milk cheese. International Journal of Food Microbiology 124 211–216Google Scholar
Akkaya, L & Sancak, YC 2007 Growth abilities and enterotoxin production of Staphylococcus aureus strains in Herby cheese. Bulletin of the Veterinary Institute in Pulawy 51 401–406Google Scholar
Alomar, J, Loubiere, P, Delbes, C, Nouaille, S & Montel, MC 2008 Effect of Lactococcus garvieae, Lactococcus lactis and Enterococcus faecalis on the behaviour of Staphylococcus aureus in microfiltered milk. Food Microbiology 25 502–508CrossRefGoogle ScholarPubMed
APHA 2004 Standard Methods for the Examination of Dairy Products, 17th Edition p. 570 (Eds Michael Wehr, H & Frank, JF). Washington, DC: American Public Health Association.CrossRefGoogle Scholar
Balaban, N & Rasooly, A 2000 Staphylococcal enterotoxins. International Journal of Food Microbiology 61 1–8Google Scholar
Charlier, C, Cretenet, M, Even, S & Le Loir, Y 2009 Interactions between Staphylococcus aureus and lactic acid bacteria: an old story with new perspectives. International Journal of Food Microbiology 131 30–39CrossRefGoogle ScholarPubMed
Charlier, C, Even, S, Gautier, M & Le Loir, Y 2008 Acidification is not involved in the early inhibition of Staphylococcus aureus growth by Lactococcus lactis in milk. International Dairy Journal 18 197–203Google Scholar
Cremonesi, P, Perez, G, Pisoni, G, Moroni, P, Morandi, S, Luzzana, M, Brasca, M & Castiglioni, B 2007 Detection of enterotoxigenic Staphylococcus aureus isolates in raw milk cheese. Letters in Applied Microbiology 45 586–591Google Scholar
Delbes, C, Alomar, J, Chougui, N, Martin, JF & Montel, MC 2006 Staphylococcus aureus growth and enterotoxin production during the manufacture of uncooked, semihard cheese from cows’ raw milk. Journal of Food Protection 69 2161–2167Google Scholar
Donnelly, CB, Leslie, JE & Black, LA 1968 Production of enterotoxin A in milk. Applied Microbiology 16 917–924Google Scholar
El-Sharoud, WH & Spano, G 2008 Diversity and enterotoxigenicity of Staphylococcus spp. associated with domiati cheese. Journal of Food Protection 71 2567–2571Google Scholar
Gomez-Lucia, E, Goyache, J, Orden, JA, Domenech, A, Hernandez, FJ, Quiteria, JAR, Lopez, B, Blanco, JL & Suarez, G 1992 Growth of Staphylococcus aureus and synthesis of enterotoxin during ripening of experimental Manchego-type cheese. Journal of Dairy Science 75 19–26CrossRefGoogle ScholarPubMed
Govaris, A, Papageorgiou, D & Papatheodorou, K 2002 Behaviour of Escherichia coli O157:H7 during the manufacture and ripening of Feta and Telemes cheese. Journal of Food Protection 65 609–615Google Scholar
Greek Codex Alimentarius 2003 Official Journal of the Republic of Greece (Vol. B, Article 83). Athens: National Printing Office.Google Scholar
Hamama, A, El Hankouri, N & El Ayadi, M 2002 Fate of enterotoxigenic Staphylococcus aureus in the presence of nisin-producing Lactococcus lactis strain during manufacture of Jben, a Moroccan traditional fresh cheese. International Dairy Journal 12 933–938CrossRefGoogle Scholar
Hein, I, Jorgensen, HJ, Loncarevic, S & Wagner, M 2005 Quantification of Staphylococcus aureus in unpasteurised bovine and caprine milk by real-time PCR. Research in Microbiology 156 554–563Google Scholar
International Dairy Federation 1990 Milk and Milk Products. Counting of Staphylococcus aureus. Brussels: IDF (FIL-IDF Standard no. 145).Google Scholar
Jelastopulu, E, Venieri, D, Komninou, G, Kolokotronis, T, Constantinidis, TC & Bantias, C 2006 Outbreak of acute gastroenteritis in an air force base in Western Greece. BMC Public Health 6 254–261Google Scholar
Johnson, WM, Tyler, SD, Ewan, EP, Ashton, FE, Pollard, DR & Rozee, KR 1991 Detection of genes for enterotoxins, exfoliative toxins, and toxic shock syndrome toxin 1 in Staphylococcus aureus by the polymerase chain reactions. Journal of Clinical Microbiology 29 426–430Google Scholar
Kondyli, E, Katsiari, MC & Voutsinas, LP 2008 Chemical and sensory characteristics of Galotyri-type cheese made using different procedures. Food Control 19 301–307Google Scholar
Le Loir, Y, Baron, F & Gautier, M 2003 Staphylococcus aureus and food poisoning. Genetics and Molecular Research 2 63–67Google ScholarPubMed
Le Marc, Y, Valík, L & Medvedova, A 2009 Modelling the effect of the starter culture on the growth of Staphylococcus aureus in milk. International Journal of Food Microbiology 129 306–311Google Scholar
Lindqvist, R, Sylven, S & Vagsholm, I 2002 Quantitative microbial risk assessment exemplified by Staphylococcus aureus in unripened cheese made from raw milk. International Journal of Food Microbiology 78 155–170CrossRefGoogle ScholarPubMed
Loncarevic, S, Jorgensen, HJ, Lovseth, A, Mathisen, T & Rorvik, LM 2005 Diversity of Staphylococcus aureus enterotoxin types within single samples of raw milk and raw milk products. Journal of Applied Microbiology 98 443–453.Google Scholar
Medvedova, A, Valik, L, Sirotna, Z & Liptakova, D 2009a Growth characterisation of Staphylococcus aureus in milk: a quantitative approach. Czech Journal of Food Science 27 443–453Google Scholar
Medvedova, A, Valik, L & Studenicova, A 2009b The effect of temperature and water activity on the growth of Staphylococcus aureus. Czech Journal of Food Science 27 S228–S235Google Scholar
Meyrand, A, Boutrand-Loei, S, Ray-Gueniot, S, Mazuy, C, Gaspard, CE, Jaubert, G, Perrin, G, Lapeyre, C & Vernozy-Rozand, C 1998 Growth and enterotoxin production of Staphylococcus aureus during the manufacture and ripening of Camembert-type cheeses from raw goats’ milk. Journal of Applied Microbiology 85 537–544Google Scholar
Millette, M, Luquet, FM & Lacroix, M 2007 In vitro growth control of selected pathogens by Lactobacillus acidophilus- and Lactobacillus casei-fermented milk. Letters in Applied Microbiology 44 314–319Google Scholar
Morandi, S, Brasca, M, Lodi, R, Cremonesi, P & Castiglioni, B 2007 Detection of classical enterotoxins and identification of enterotoxin genes in Staphylococcus aureus from milk and dairy products. Veterinary Microbiology 124 66–72Google Scholar
Nicolaou, N, Xu, Y & Goodacre, R 2011 Fourier transform infrared and raman spectroscopies for the rapid detection, enumeration, and growth nteraction of the bacteria Staphylococcus aureus and Lactococcus lactis ssp. cremoris in milk. Analytical Chemistry 83 5681–5687Google Scholar
Normanno, G, La Salandra, G, Quaglia, NC, Corrente, M, Parisi, A, Santagada, G, Firinu, A, Crisetti, E & Celano, GV 2007 Occurrence, characterization and antimicrobial resistance of enterotoxigenic Staphylococcus aureus isolated from meat and dairy products. International Journal of Microbiology 115 290–296Google Scholar
Olarte, C, Sanz, S, Gonzalez-Fandos, E & Torre, P 2000 The effect of a commercial starter culture addition on the ripening of an artisanal goat's cheese (Cameros cheese). Journal of Applied Microbiology 88 421–429CrossRefGoogle ScholarPubMed
Pereira, G, Graca, JA, Ogando, NS, Gomes, AMP & Malcata, X 2009 Bacterial dynamics in model cheese systems, aiming at safety and quality of Portuguese-style traditional ewe's cheeses. Journal of Food Protection 72 2243–2251Google Scholar
Pereira, JL, Salzberg, SP & Bergdoll, MS 1991 Production of staphylococcal enterotoxin D in foods by low-enterotoxin-producing staphylococci. International Journal of Food Microbiology 14 19–26Google Scholar
Poli, A, Guglielmini, E, Sembeni, S, Spiazzi, M, Dellaglio, F, Rossi, F & Torriani, S 2007 Detection of Staphylococcus aureus and enterotoxin genotype diversity in Monte Veronese, a Protected Designation of Origin Italian cheese. Letters in Applied Microbiology 45 529–534Google Scholar
Rilla, N, Martinez, B & Rodriguez, A 2004 Inhibition of a methicillin-resistant Staphylococcus aureus strain in Afuega'l Pitu Cheese by the Nisin Z-producing strain Lactococcus lactis subsp. lactis IPLA 729. Journal of Food Protection 67 928–933Google Scholar
Tsen, HY & Chen, TR 1992 Use of the polymerase chain reaction for specific detection of type A, D and E enterotoxigenic Staphylococcus aureus in foods. Applied Microbiology and Biotechnology 37 685–690Google Scholar
Vernozy-Rozand, C, Meyrand, A, Mazuy, C, Delignette-Muller, ML, Jaubert, G, Perrin, G, Lapeyre, C & Richard, Y 1998 Behaviour and enterotoxin production by Staphylococcus aureus during the manufacture and ripening of raw goats’ milk lactic cheeses. Journal of Dairy Research 65 273–281Google Scholar