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Staphylococcus aureus reservoirs during traditional Austrian raw milk cheese production

Published online by Cambridge University Press:  29 September 2014

Georg Walcher
Affiliation:
Department for Farm Animals and Veterinary Public Health, Institute of Milk Hygiene, Milk Technology and Food Science, University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210 Vienna, Austria
Monika Gonano
Affiliation:
Department for Farm Animals and Veterinary Public Health, Institute of Milk Hygiene, Milk Technology and Food Science, University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210 Vienna, Austria Austrian Agency for Health and Food Safety (AGES), Institute for Veterinary Investigations Mödling, Robert Koch Gasse 17, 2340 Mödling, Austria
Judith Kümmel
Affiliation:
Department for Pathobiology, Institute of Bacteriology, Mycology and Hygiene, Functional Microbiology, University of Veterinary Medicine, Veterinärplatz 1, 1210 Vienna, Austria Clinic for Ruminants, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine, Veterinärplatz 1, 1210 Vienna, Austria
Gary C. Barker
Affiliation:
Institute of Food Research, Norwich Research Park, Colney, Norwich NR4 7UA, UK
Karin Lebl
Affiliation:
Department for Farm Animals and Veterinary Public Health, Institute for Veterinary Public Health, University of Veterinary Medicine, Vienna, Austria
Othmar Bereuter
Affiliation:
Department of Dairy, Chamber of Agriculture Vorarlberg, Montfortstraße 9-11, 6900 Bregenz, Austria
Monika Ehling-Schulz
Affiliation:
Department for Pathobiology, Institute of Bacteriology, Mycology and Hygiene, Functional Microbiology, University of Veterinary Medicine, Veterinärplatz 1, 1210 Vienna, Austria
Martin Wagner
Affiliation:
Department for Farm Animals and Veterinary Public Health, Institute of Milk Hygiene, Milk Technology and Food Science, University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210 Vienna, Austria
Beatrix Stessl*
Affiliation:
Department for Farm Animals and Veterinary Public Health, Institute of Milk Hygiene, Milk Technology and Food Science, University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210 Vienna, Austria
*
*For correspondence; e-mail: [email protected]

Abstract

Sampling approaches following the dairy chain, including microbiological hygiene status of critical processing steps and physicochemical parameters, contribute to our understanding of how Staphylococcus aureus contamination risks can be minimised. Such a sampling approach was adopted in this study, together with rapid culture-independent quantification of Staph. aureus to supplement standard microbiological methods. A regional cheese production chain, involving 18 farms, was sampled on two separate occasions. Overall, 51·4% of bulk milk samples were found to be Staph. aureus positive, most of them (34·3%) at the limit of culture-based detection. Staph. aureus positive samples >100 cfu/ml were recorded in 17·1% of bulk milk samples collected mainly during the sampling in November. A higher number of Staph. aureus positive bulk milk samples (94·3%) were detected after applying the culture-independent approach. A concentration effect of Staph. aureus was observed during curd processing. Staph. aureus were not consistently detectable with cultural methods during the late ripening phase, but >100 Staph. aureus cell equivalents (CE)/ml or g were quantifiable by the culture-independent approach until the end of ripening. Enterotoxin gene PCR and pulsed-field gel electrophoresis (PFGE) typing provided evidence that livestock adapted strains of Staph. aureus mostly dominate the post processing level and substantiates the belief that animal hygiene plays a pivotal role in minimising the risk of Staph. aureus associated contamination in cheese making. Therefore, the actual data strongly support the need for additional sampling activities and recording of physicochemical parameters during semi-hard cheese-making and cheese ripening, to estimate the risk of Staph. aureus contamination before consumption.

Type
Research Article
Copyright
Copyright © Proprietors of Journal of Dairy Research 2014 

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References

Aprodu, I, Walcher, G, Schelin, J, Hein, I, Norling, B, Radstrom, P, Nicolau, A & Wagner, M 2011 Advanced sample preparation for the molecular quantification of Staphylococcus aureus in artificially and naturally contaminated milk. International Journal of Food Microbiology 145(Suppl. 1) S61S65 CrossRefGoogle ScholarPubMed
Arcuri, EF, Angelo, FF, Guimarães, MF, Talon, R, Borges Mde, F, Leroy, S, Loiseau, G, Lange, CC, Andrade, NJ & Montet, D 2010 Toxigenic status of Staphylococcus aureus isolated from bovine raw milk and Minas frescal cheese in Brazil. Journal of Food Protection 73 22252231 CrossRefGoogle ScholarPubMed
Bernini, V, Sgarbi, E, Bove, CG, Gatti, M & Neviani, E 2010 A polyphasic approach to detect enterotoxigenic Staphylococcus aureus and diarrheagenic Escherichia coli in raw milk Italian cheeses by multiplex PCR. Journal of Food Protection 73 22812284 CrossRefGoogle ScholarPubMed
Brakstad, OG, Aasbakk, K & Maeland, JA 1992 Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. Journal of Clinical Microbiology 30 16541660 CrossRefGoogle ScholarPubMed
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 3039 CrossRefGoogle ScholarPubMed
Costa Sobrinho Pde, S, Marcal de Faria, CA, Silva Pinheiro, J, Goncalves de Almeida, H, Vieira Pires, C & Silva Santos, A 2012 Bacteriological quality of raw milk used for production of a Brazilian farmstead raw milk cheese. Foodborne Pathogens and Diseases 9 138144 CrossRefGoogle ScholarPubMed
D'Amico, DJ & Donnelly, CW 2011 Characterization of Staphylococcus aureus strains isolated from raw milk utilized in small-scale artisan cheese production. Journal of Food Protection 74 13531358 CrossRefGoogle ScholarPubMed
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 21612167 CrossRefGoogle ScholarPubMed
European Commission 2006 Regulation (EC) No. 1662/2006 of 6 November 2006 amending Regulation (EC) No. 853/2004 of the European Parliament and of the Council laying down specific hygiene rules for food of animal origin. Official Journal of the European Union L 320, 110. eur67440.pdf (Accessed on 17 May 2014)Google Scholar
European Commission 2007 Regulation (EC) No. 1441/2007 of 5 December 2007 amending Commission Regulation (EC) No. 2073/2005 on microbiological criteria for foodstuffs. Brussels: Official Journal of the European Communities L322, 1229. eur75857.pdf (Accessed on 17 May 2014)Google Scholar
Gonano, M, Hein, I, Zangerl, P, Rammelmayr, A & Wagner, M 2009 Phenotypic and molecular characterization of Staphylococcus aureus strains of veterinary, dairy and human origin. Epidemiology and Infection 137 688699 CrossRefGoogle ScholarPubMed
Giammanco, GM, Pepe, A, Aleo, A, D'Agostino, V, Milone, S & Mammina, C 2011 Microbiological quality of Pecorino Siciliano “primosale” cheese on retail sale in the street markets of Palermo, Italy. New Microbiologica 34 179185 Google ScholarPubMed
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 554563 CrossRefGoogle ScholarPubMed
ISO 6888-1 1999 Microbiology of food and animal feeding stuffs – Horizontal method for the enumeration of coagulase-positive staphylococci Staphylococcus aureus and other species – Part 1: Technique using Baird-Parker agar medium. Geneva, Switzerland Google Scholar
ISO 4833 2003 Microbiology of food and animal feeding stuffs – Horizontal method for the enumeration of microorganisms – Colony-count technique at 30 degrees C. Geneva, Switzerland Google Scholar
ISO 4832 2006 Microbiology of food and animal feeding stuffs – Horizontal method for the enumeration of coliforms – Colony-count technique. Geneva, Switzerland Google Scholar
Jakobsen, RA, Heggebo, R, Sunde, EB & Skjervheim, M 2011 Staphylococcus aureus and Listeria monocytogenes in Norwegian raw milk cheese production. Food Microbiology 28 492496 CrossRefGoogle ScholarPubMed
Jørgensen, HJ, Mørk, T & Rørvik, LM 2005 The occurrence of Staphylococcus aureus on a farm with small-scale production of raw milk cheese. Journal of Dairy Science 88 38103817 CrossRefGoogle ScholarPubMed
Kongo, JM, Gomes, AP & Malcata, FX 2008 Monitoring and identification of bacteria associated with safety concerns in the manufacture of São Jorge, a Portuguese traditional cheese from raw cow's milk. Journal of Food Protection 71 986992 CrossRefGoogle Scholar
Mayrl, E, Roeder, B, Mester, P, Wagner, M & Rossmanith, P 2009 Broad range evaluation of the matrix solubilization (matrix lysis) strategy for direct enumeration of foodborne pathogens by nucleic acids technologies. Journal of Food Protection 72 12251233 CrossRefGoogle ScholarPubMed
Murchan, S, Kaufmann, ME, Deplano, A, de Ryck, R, Struelens, M, Zinn, CE, Fussing, V, Salmenlinna, S, Vuopio-Varkila, J, El Solh, N, Cuny, C, Witte, W, Tassios, PT, Legakis, N, van Leeuwen, W, van Belkum, A, Vindel, A, Laconcha, I, Garaizar, J, Haeggman, S, Olsson-Liljequist, B, Ransjo, U, Coombes, G & Cookson, B 2003 Harmonization of pulsed-field gel electrophoresis protocols for epidemiological typing of strains of methicillin-resistant Staphylococcus aureus: a single approach developed by consensus in 10 European laboratories and its application for tracing the spread of related strains. Journal of Clinical Microbiology 41 15741585 CrossRefGoogle ScholarPubMed
Nakayama, A, Okayama, A, Hashida, M, Yamamoto, Y, Takebe, H, Ohnaka, T, Tanaka, T & Imai, S 2006 Development of a routine laboratory direct detection system of staphylococcal enterotoxin genes. Journal of Medical Microbiology 55 273277 CrossRefGoogle ScholarPubMed
Pexara, A, Solomakos, N, Sergelidis, D & Govaris, A 2012 Fate of enterotoxigenic Staphylococcus aureus and staphylococcal enterotoxins in Feta and Galotyri cheeses. Journal of Dairy Research 79 405413 CrossRefGoogle ScholarPubMed
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 Designationof Origin Italian cheese. Letters in Applied Microbiology 45 529534 CrossRefGoogle Scholar
Stessl, B & Wagner, M 2012 Real-time PCR Detection of Foodborne Pathogenic Staphylococcus aureus . In Real-Time PCR in Food Science: Current Technology and Applications, p. 150154 (Ed. Rodríguez-Lázaro, D) Norfolk: Caister Academic Press Google Scholar
Stessl, B, Hein, I, Wagner, M & Ehling-Schulz, M 2011 Staphylococcus aureus in the dairy chain. In Rapid Detection, Characterization and Enumeration of Food-Borne Pathogens, p. 291305 (Ed. Hoorfar, J). Washington, DC, USA: American Society of Microbiology Press Google Scholar
Syring, C, Boss, R, Reist, M, Bodmer, M, Hummerjohann, J, Gehrig, P & Graber, HU 2010 Bovine mastitis: the diagnostic properties of a PCR-based assay to monitor the Staphylococcus aureus genotype B status of a herd, using bulk tank milk. Journal of Dairy Science 95 36743682 CrossRefGoogle Scholar
The Austrian Federal Ministry of Agriculture, Forestry, Environment and Water Management 2011 Grüner Bericht (Green report). http://www.gruenerbericht.at/cm3/download/summary/113-gruener-bericht-vorarlberg/472-gruener-bericht-vorarlberg-2011.html (Accessed on 17 May 2014)Google Scholar
Vicosa, GN, Moraes, PM, Yamazi, AK & Nero, LA 2010 Enumeration of coagulase and thermonuclease-positive Staphylococcus spp in raw milk and fresh soft cheese: an evaluation of Baird-Parker agar, Rabbit Plasma Fibrinogen agar and the Petrifilm Staph Express count system. Food Microbiology 27 447452 CrossRefGoogle ScholarPubMed
Walsh, PS, Metzger, DA & Higuchi, R 1991 Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10 506513 Google ScholarPubMed