Pre-treatments of Milk and their Effect on the Food Safety of Cheese

  • Elisabeth Eugster
  • Ernst Jakob
Keywords: cheesemaking, food safety, milk treatment, pasteurization, thermization, bactofugation, microfiltration


In the manufacture of traditional cheese varieties, processing fresh milk that has been treated as little as possible is crucial. Preserving the microbiome and the activity of the original enzymes in the raw milk to the greatest extent possible allows these cheeses to retain their original character. This objective conflicts with the growing demands placed on products in terms of food safety. The present literature search addresses the influence of the pre-treatment of cheesemaking milk on the food safety and quality of ripened cheeses, with particular focus on heat treatment, bactofugation, and microfiltration.


Union Suisse des Paysans. Statistique laitière de la Suisse, 2017; 2018 [cited 2019 Oct 14]. Available from: URL:

Ministère de l’Agriculture et de l’Alimentation Secrétariat général Service de la Statistique et de la Prospective. Enquête annuelle laitière 2017; 2018. Available from: URL:

Hartmann K, Licitra G, Eugster-Meier E, Fröhlich-Wyder M-T, Jakob E, Wechsler D et al. Hard cheeses. In: Papademas P, Bintsis T, editors. Global cheesemaking technology. Chichester: John Wiley & Sons. Ltd.; 2017. p. 204–46.

López Morales MB, Ardö Y, Berthier F, Karatzas K-A, Bintis T. Blue-veined cheeses. In: Papademas P, Bintsis T, editors. Global cheesemaking technology. Chichester: John Wiley & Sons. Ltd.; 2017. p. 415–35.

Consorzio Tutela Taleggio: Official website for Taleggio PDO; 2019 [cited 2019 Aug 9]. Available from: URL:

Ardö Y, Berthier F, Harmann K, Eugster-Meier E, Fröhlich-Wyder M-T, Jakob E et al. Bacterial surface-ripened (smear) cheeses. In: Papademas P, Bintsis T, editors. Global cheesemaking technology. Chichester: John Wiley & Sons. Ltd.; 2017. p. 397–414.

Bintsis T, Alichanidis E, Uzonoy I, Özer B, Papademas P, Radulovic Z et al. White-brined cheeses. In: Papademas P, Bintsis T, editors. Global cheesemaking technology. Chichester: John Wiley & Sons. Ltd.; 2017. p. 349–67.

Anne VI. Pourquoi la future AOP Camembert de Normandie est-elle critiquée par certains producteurs ? Le Monde [cited 2019 Oct 14]. Available from: URL:

Sperat-Czar A, Sainte Marie C de. Cru-pasteurisé, à qui profite la coexistence? Profession fromager [cited 2019 Oct 14]:27–8. Available from: URL:

Licitra G, Caccamo M, Lortal S. Artisanal Products Made With Raw Milk. In: Nero LA, Carvalho AF de, editors. Raw Milk. London: Academic Press; 2019. p. 175–221.

Hartmann K, Maubois JL. Mould surface-ripened cheeses. In: Papademas P, Bintsis T, editors. Global cheesemaking technology. Chichester: John Wiley & Sons. Ltd.; 2017. p. 392–6.

Food and Agriculture Organization of the United Nations (FAO). Codex Alimentarius: General Principles of Food Hygiene [CXC 1-1969 ; CAC/RCP 1-1969]; 1969 [cited 2019 Oct 14]. Available from: URL:

European Union (EU). Regulation (EC) No 852/2004 of the European Parliament and of the Council of 29 April 2004 on the hygiene of foodstuffs; 2004 [cited 2019 Oct 14]. Available from: URL:

Mayo B, Rachid CTCC, Alegría A, Leite AMO, Peixoto RS, Delgado S. Impact of next generation sequencing techniques in food microbiology. Curr Genomics 2014; 15(4):293–309.

Quigley L, O'Sullivan O, Stanton C, Beresford TP, Ross RP, Fitzgerald GF et al. The complex microbiota of raw milk. FEMS Microbiol Rev 2013; 37(5):664–98.

Masoud W, Vogensen FK, Lillevang S, Abu Al-Soud W, Sørensen SJ, Jakobsen M. The fate of indigenous microbiota, starter cultures, Escherichia coli, Listeria innocua and Staphylococcus aureus in Danish raw milk and cheeses determined by pyrosequencing and quantitative real time (qRT)-PCR. Int J Food Microbiol 2012; 153(1-2):192–202.

Quigley L, O'Sullivan O, Beresford TP, Ross RP, Fitzgerald GF, Cotter PD. High-Throughput Sequencing for Detection of Subpopulations of Bacteria Not Previously Associated with Artisanal Cheeses. Appl. Environ. Microbiol. 2012; 78(16):5717–23.

Bergère JL, Le Bars D, Commissaire J. La bactofugation du lait et l'élimination des spores de Clostridium tyrobutyricum. Lait 1969; 49(488):507–19.

Robinson RK, Scott R, Wilbey RA. Cheesemaking practice. 3. ed. Gaithersburg, Md: Aspen Publishers; 1998.

Richard J, Desmazeaud M. The microbial flora of milk intended for cheesemaking. In: Eck A, Gillis J-C, editors. Cheesemaking: From science to quality assurance. 2nd ed. London: Intercept; 2000. p. 189–98.

Baumgartner A, Kueffer M, Rohner P. Occurrence and antibiotic resistance of enterococci in various ready-to-eat foods. Archiv für Lebensmittelhygiene 2001; 52:1–24.

McAuley CM, Britz ML, Gobius KS, Craven HM. Prevalence, seasonality, and growth of enterococci in raw and pasteurized milk in Victoria, Australia. J Dairy Sci 2015; 98(12):8348–58.

Top J, Willems R, Bonten M. Emergence of CC17 Enterococcus faecium: from commensal to hospital-adapted pathogen. FEMS Immunol Med Microbiol 2008; 52(3):297–308.

Teuber M, Meile L, Schwarz F. Acquired antibiotic resistance in lactic acid bacteria from food. Antonie Van Leeuwenhoek 1999; 76(1-4):115–37.

Franz CMAP, Huch M, Abriouel H, Holzapfel W, Gálvez A. Enterococci as probiotics and their implications in food safety. Int J Food Microbiol 2011; 151(2):125–40.

Wechsler D, Walther B, Jakob E, Winkler H. Bedeutung biogener Amine in der Ernährung und deren Vorkommen in Schweizer Käsesorten [ALP forum]: Agroscope; 2009 [cited 2019 Oct 14]. Available from: URL:

Leuschner RGK, Kurihara R, Hammes WP. Formation of biogenic amines by proteolytic enterococci during cheese ripening. J. Sci. Food Agric. 1999; 79(8):1141–4.

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(3):476–83.

Spahr U, Schafroth K. Fate of Mycobacterium avium subsp. paratuberculosis in Swiss Hard and Semihard Cheese Manufactured from Raw Milk. Applied and Environmental Microbiology 2001; 67(9):4199–205.

Food and Drug Administration. Cheeses and related cheese products: Code of Federal Regulations 21 [Subchapter B - Food for Human Consumption]; 2015 [cited 2019 Oct 14]. Available from: URL:

Reitsma CJ, Henning DR. Survival of Enterohemorrhagic Escherichia coli O157:H7 During the Manufacture and Curing of Cheddar Cheese. J Food Prot 1996; 59(5):460–4.

Schlesser JE, Gerdes R, Ravishankar S, Madsen K, Mowbray J, Teo AYL. Survival of a five-strain cocktail of Escherichia coli O157:H7 during the 60-day aging period of cheddar cheese made from unpasteurized milk. J Food Prot 2006; 69(5):990–8.

Peng S, Schafroth K, Jakob E, Stephan R, Hummerjohann J. Behaviour of Escherichia coli strains during semi-hard and hard raw milk cheese production. International Dairy Journal 2013; 31(2):117–20.

Rusch M. Untersuchungen zu verschiedenen mikrobiologischen Parametern in Rohmilch und Rohmilchkäse einer Biokäsereigenossenschaft über den Zeitraum eines Jahres: Doctoral Thesis, University of Zurich; 2005 [cited 2019 Oct 16]. Available from: URL:

Menéndez González S, Hartnack S, Berger T, Doherr M, Breidenbach E. A qualitative risk assessment approach for Swiss dairy products: opportunities and limitations. Zoonoses Public Health 2011; 58(3):209–19.

Verraes C, Vlaemynck G, van Weyenberg S, Zutter L de, Daube G, Sindic M et al. A review of the microbiological hazards of dairy products made from raw milk. International Dairy Journal 2015 [cited 2019 Oct 14]; 50:32–44. Available from: URL:

Fröhlich-Wyder MT. Bedeutung des Arginin Deiminase Stoffwechsels von Starterkulturen und Milchsäurebakterien aus der Rohmilch für die Qualität und Reifung von Käse. Ansbach; 2016. (Ansbacher Fachgespräche).

Imhof R, Schwendimann L. Prevalence of pathogenic bacteria in raw milk in Switzerland. Nantes; 2014. (International ICMFH conference).

Ascone P, Maurer J, Haldemann J, Irmler S, Berthoud H, Portmann R et al. Prevalence and diversity of histamine-forming Lactobacillus parabuchneri strains in raw milk and cheese – A case study. International Dairy Journal 2017; 70:26–33.

European Union (EU). Regulation (EC) No 853/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules on the hygiene of foodstuffs.; 2004 [cited 2019 Oct 14]. Available from: URL:

Leporq B, Membré J-M, Dervin C, Buche P, Guyonnet JP. The "Sym'Previus" software, a tool to support decisions to the foodstuff safety. Int J Food Microbiol 2005; 100(1-3):231–7.

Lenoir J, Remeuf F, Schneid N. Rennetability of milk. In: Eck A, Gillis J-C, editors. Cheesemaking: From science to quality assurance. 2nd ed. London: Intercept; 2000. p. 213–38.

Deeth HC. Lipoprotein lipase and lipolysis in milk. International Dairy Journal 2006; 16(6):555–62.

Food and Drug Administration. Grade “A” Pasteurized Milk Ordinance: Includes provisions from the Grade “A” Condensed and Dry Milk Products and Condensed and Dry Whey--Supplement I to the Grade “A” PMO; 2017 [cited 2019 Oct 14]. Available from: URL:

European Union (EU). Regulation (EC) No 1662/2006 amending Regulation (EC) No 853/2004 [Official Journal of the European Union]; 2006. Available from: URL:

Cerf O, Condron R. Coxiella burnetii and milk pasteurization: an early application of the precautionary principle? Epidemiol Infect 2006; 134(5):946–51.

Sörqvist S. Heat resistance in liquids of Enterococcus spp., Listeria spp., Escherichia coli, Yersinia enterocolitica, Salmonella spp. and Campylobacter spp. Acta Vet Scand 2003; 44(1-2):1–19.

Sung N, Collins MT. Thermal tolerance of Mycobacterium paratuberculosis. Applied and Environmental Microbiology 1998; 64(3):999–1005.

Hammer P, Richter E, Rüsch-Gerdes S, Walte H-GC, Matzen S, Kiesner C. Inactivation of Mycobacterium bovis ssp. caprae in high-temperature, short-term pasteurized pilot-plant milk. J Dairy Sci 2015; 98(3):1634–9.

Firstenberg-Eden R, Rosen B, Mannheim CH. Death and injury of Staphylococcus aureus during thermal treatment of milk. Can. J. Microbiol. 1977; 23(8):1034–7.

Rukke EO, Sørhaug T, Stepaniak L. Heat treatment of milk: Thermization of milk. In: Fuquay JW, Fox FP, McSweeney PHL, editors. Encyclopedia of Dairy Sciences. 2nd ed. Oxford UK: Elsevier; 2011. p. 693–8.

Franklin JG, Sharpe ME. The incidence of bacteria in cheese milk and Cheddar cheese and their association with flavour. Journal of Dairy Research 1963; 30(1):87–99.

Grappin R, Beuvier E. Possible implications of milk pasteurization on the manufacture and sensory quality of ripened cheese. International Dairy Journal 1997; 7(12):751–61.

Foulquié Moreno MR, Sarantinopoulos P, Tsakalidou E, Vuyst L de. The role and application of enterococci in food and health. Int J Food Microbiol 2006; 106(1):1–24.

Hickey DK, Kilcawley KN, Beresford TP, Wilkinson MG. Lipolysis in cheddar cheese made from raw, thermized, and pasteurized milks. J Dairy Sci 2007; 90(1):47–56.

Jakob E, Menéndez Gonzâlez S. Guideline for the milk production and dairy products on alpine farms [Leitlinie für die gute Verfahrenspraxis bei der Milchgewinnung und -verarbeitung in Sömmerungsbetrieben]. Bern: Schweizerischer Alpwirtschaftlicher Verband (SAV); 2015.

Jacobsson L, Thurell KE. Bactofugation of cheese milk. Svenska Mejeritidn 1970; 62(22):405–7.

Invernizzi GB. Esperienze Alfa Laval nell’applicazione della bactofugazione per la produzione di formaggio Grana. Latte 1984; 9:465–73.

Walstra P, Geurts TJ, Noomen A, Jellema A, van Boekel MAJS. Dairy Technology: Principles of Milk Properties and Processes: CRC Press; 1999.

Deeth HC, Datta N. Non-thermal Technologies: Introduction. In: Fuquay JW, Fox FP, McSweeney PHL, editors. Encyclopedia of Dairy Sciences. 2nd ed. Oxford UK: Elsevier; 2011. p. 725–31.

Spreer E. Technologie der Milchverarbeitung. 10., vollst. überarb. Aufl. Hamburg: Behr; 2011.

Te Giffel MC, van der Horst, H. C. Comparison between bactofugation and microfiltration regarding efficiency of somatic cell and bacteria removal. Bulletin of the IDF 2004; (389):49–53.

GEA Westfalia Separator GmbH. Separators from GEA Westfalia: Separator for milk clarification and bacteria removal; 2015 [cited 2019 Oct 14]. Available from: URL:

Torres-Anjel MJ, Hedrick TI. Spore removal by centrifugation and its effect on ultra-high temperature commercial sterilization of milk. J Dairy Sci 1971; 54(3):326–30.

Faccia M, Mastromatteo M, Conte A, Del Nobile MA. Influence of the Milk Bactofugation and Natural Whey Culture on the Microbiological and Physico-Chemical Characteristics of Mozzarella Cheese. J Food Process Technol 2013; 04(04):1–7.

Kosikowski FV, Fox PF. Low Heat, Hydrogen Peroxide, and Bactofugation Treatments of Milk to Control Coliforms in Cheddar Cheese. J Dairy Sci 1968; 51(7):1018–22.

Grant IR. Occurrence of Mycobacterium avium subsp. paratuberculosis in foods and the impact of milk processing on its survival. In: Proceedings of the 8th International Colloquium on Paratuberculosis. Madison; 2005. p. 271–7.

Fragnière C, Bütikofer U. Comparaison de différents traitements du lait (bactofugation, thermisation) pour la fabrication de Vacherin Fribourgeois. Liebefeld Posieux; 2006. (ALPinterne 204; vol 204).

Mc Carthy OJ. Centrifuges and Separators: Applications in the Dairy Industry. Encyclopedia of Dairy Sciences 2011; 4:175–81.

Kessler HG. Lebensmittel- und Bioverfahrenstechnik: Molkereitechnologie. 3. neubearb. u. erw. Aufl. Freising: Verlag A. Kessler; 1988.

Gillot J, Brinkman G, Garcera D. Nouveaux médias filtrants céramiques pour la microfiltration tangentielle et ultrafiltration: Société Française de Filtration; 1984.

Holm S, Malmerg R, Svensson K, inventors. Method and plant for producing milk with a low bacterial count. WO1986001687A1.

Uhl M. Bactocatch – Ein neues Verfahren zur Verbesserung der Milchqualität. DMZ, Lebensmittelindustrie und Milchwirtschaft 1990; 110(40):1272–6.

Fritsch J, Moraru CI. Development and optimization of a carbon dioxide-aided cold microfiltration process for the physical removal of microorganisms and somatic cells from skim milk. J Dairy Sci 2008; 91(10):3744–60.

Griep ER, Cheng Y, Moraru CI. Efficient removal of spores from skim milk using cold microfiltration: Spore size and surface property considerations. J Dairy Sci 2018; 101(11):9703–13.

Trouvé E, Maubois JL, Piot M, Madec MN, Fauquant J, Rouault A et al. Rétention de différentes espèces microbiennes lors de l'épuration du lait par microfiltration en flux tangentiel. Lait 1991; 71(1):1–13.

Klantschitsch T. Influence of microfiltration on the quality of semi-hard cheese from raw milk with particular emphasis on Clostridium tyrobutyricum spores [Dissertation ETH Zürich Nr. 13233]; 1999.

Saboya LV, Maubois J-L. Current developments of microfiltration technology in the dairy industrie. Lait 2000; (80):541–53.

Elwell MW, Barbano DM. Use of microfiltration to improve fluid milk quality. J Dairy Sci 2006; 89:E20-30.

Hartung M, Tenhagen B-A, Käsbohrer A. Erreger von Zoonosen in Deutschland im Jahr 2013. Bundesinstitut für Risikobewertung BfR 2015 [cited 2019 Oct 14]; (2). Available from: URL:

Zweifel C, Giezendanner N, Corti S, Krause G, Beutin L, Danuser J et al. Characterisics of Shiga Toxin-Producing Escherichia coli isolated from Swiss raw-milk cheese within a 3-Year monitoring program. J Food Prot 2010; 73(1):88–91.

Jay JM, Loessner MJ, Golden DA. Modern food microbiology [Food Science Text Series]. 7. ed. New York, NY: Springer Science + Business Media Inc.; 2005.

Mukhopadhyay S, Gorris LGM. Hurdle Technology. In: Batt CA, Tortorello ML, editors. Encyclopedia of Food Microbiology. 2nd ed. London: Academic Press; 2014. p. 221–7 (vol. 2).

Raynal K, Remeuf F. Effect of storage at 4 degrees C on the physicochemical and renneting properties of milk: a comparison of caprine, ovine and bovine milks. J Dairy Res 2000; 67(2):199–207.

Beuvier E, Berthaud K, Cegarra S, Dasen A, Pochet S, Buchin S et al. Ripening and quality of Swiss-type cheese made from raw, pasteurized or microfiltered milk. International Dairy Journal 1997; 7(5):311–23.

Bérard L, Marchenay P. Les produits de terroir - Entre cultures et règlements. Paris: CNRS Éditions; 2004 [cited 2019 Oct 14]. Available from: URL:

Majdi A. Séminaire sur les fromages AOP et IGP; 2009 [cited 2019 Oct 14]. Available from: URL:

FACE network. European Guide for Good Hygiene Practices in the production of artisanal cheese and dairy products; 2016. Available from: URL:

European Union (EU). Regulation (EC) No 2073/2005 of November 2005 on microbiological criteria for foodstuffs.; 2005 [cited 2019 Oct 14]. Available from: URL: