Czech J. Food Sci., 2008, 26(5):309-323 | DOI: 10.17221/1128-CJFS

Biofilms and hygiene on dairy farms and in the dairy industry: sanitation chemical products and their effectiveness on biofilms - a review

Hana Vlková1, Vladimír Babák1, Růžena Seydlová2, Ivo Pavlík1, Jarmila Schlegelová1
1 Department of Food and Feed Safety, Veterinary Research Institute, Brno, Czech Republic
2 Dairy Research Institute, Prague, Czech Republic

Microbial biofilms which form on all types of surfaces of technological systems in the dairy industry and on dairy farms adversely affect the quality and safety of final products, i.e. both foodstuffs and raw materials used for their production. The fact that a number of microorganisms are alimentary pathogens, e.g. Staphylococcus aureus or Listeria monocytogenes, makes a serious problem directly affecting human health. Biofilms are usually formed by various species of microorganism, which protect each other against the effects of biocidal (antibacterial) agents and are resistant to these agents. The colonisation of surfaces of the open and closed piping systems, floors, waste, walls and ceilings of the production halls becomes a major problem in the selection of effective sanitation agents for their control. Based on the existing model studies, practical methods for testing the effectiveness of sanitation procedures should be evaluated, including the selection of biocides and comparison of the physical parameters of the sanitation procedures. Testing the effectiveness of the sanitation agents should be performed with the use of standardised tests, which consider microbial, structural, and chemical characteristics of the living microbial communities on specific contact surfaces in the food-processing industry.

Keywords: microbial communities; food process surfaces; mechanisms of resistance; food safety

Published: October 31, 2008  Show citation

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Vlková H, Babák V, Seydlová R, Pavlík I, Schlegelová J. Biofilms and hygiene on dairy farms and in the dairy industry: sanitation chemical products and their effectiveness on biofilms - a review. Czech J. Food Sci.. 2008;26(5):309-323. doi: 10.17221/1128-CJFS.
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    References

    1. Aarnisalo K., Salo S., Miettinen H., Suihko M.L., Wirtanen G., Autio T., Lundén J., Korkeala H., Sjöberg A.M. (2000): Bactericidal efficiencies of commercial disinfectants against Listeria monocytogenes on surfaces. Journal of Food Safety, 20: 237-250. Go to original source...
    2. Arciola C.R., Balsdassarri L., Montanaro L. (2001): Presence of icaA and icaD genes and slime production in a collection of staphylococcal strains from catheterassociated infections. Journal of Clinical Microbiology, 39: 2151-2156. Go to original source... Go to PubMed...
    3. Asao T., Kumeda Y., Kawai T., Shibata T., Oda H., Haruki K., Nakazawa H., Kozaki S. (2003): An extensive outbreak of staphylococcal food poisoning due to low-fat milk in Japan: estimation of enterotoxin A in the incriminated milk and powdered skim milk. Epidemiology and Infection, 130: 33-40. Go to original source... Go to PubMed...
    4. Austin J.W., Bergeron G. (1995): Development of bacterial biofilms in dairy processing lines. Journal of Dairy Research, 62: 509-519. Go to original source... Go to PubMed...
    5. Bessems E. (1998): The effect of practical conditions on the efficacy of disinfectants. International Biodeterioration and Biodegradation, 41: 177-183. Go to original source...
    6. Bjorland J., Steinum T., Kvitle B., Waage S., Sunde M., Heir E. (2005): Widespread distribution of disinfectant resistance genes among staphylococci of bovine and caprine origin in Norway. Journal of Clinical Microbiology, 43: 4363-4368. Go to original source... Go to PubMed...
    7. Bloomfield S.F., Arthur M., Begun K., Patel H. (1993): Comparative testing of disinfectants using proposed European surface test methods. Letters in Applied Microbiology, 17: 119-125. Go to original source...
    8. Bremer P.J., Fillery S., McQuillan A.J. (2006): Laboratory scale Clean-In-Place (CIP) studies on the effectiveness of different caustic and acid wash steps on the removal of dairy biofilms. International Journal of Food Microbiology, 106: 254-262. Go to original source... Go to PubMed...
    9. Bylund G. (1995): Dairy Processing Handbook. Tetra Pak Processing Systems AB, Lund: 436.
    10. Cafiso V., Bertuccio T., Santagati M., Campanile F., Amicosante G., Perilli M.G., Selan L., Arttini M., Nicoletti G., Stefani S. (2004): Presence of the ica operon in clinical isolates of Staphylococcus epidermidis and its role in biofilm production. Clinical Microbiology and Infection, 10: 1081-1088. Go to original source... Go to PubMed...
    11. Capita R., Alonso-Calleja C., Rodriguez-Perez R., Moreno B., Garcia-Fernandez M.C. (2002): Influence of poultry carcass skin sample site on the effectiveness of trisodium phosphate against Listeria monocytogenes. Journal of Food Protection, 65: 853-856. Go to original source... Go to PubMed...
    12. Carpentier B., Cerf O. (1993): Biofilms and their consequences, with particular reference to hygiene in the food industry. Journal of Applied Bacteriology, 75: 499-511. Go to original source... Go to PubMed...
    13. Chick H. (1908): An investigation into the laws of disinfection. Journal of Hygiene, 8: 92-158. Go to original source... Go to PubMed...
    14. Chmielewski R., Frank J.F. (2003): Biofilm formation and control in food processing facilities. Comprehensive Reviews in Food Science and Food Safety, 2: 22-32. Go to original source... Go to PubMed...
    15. Commission regulation (EC) No 1048/2005 of 13 June 2005 amending Regulation (EC) No 2032/2003 on the second phase of the 10-year work programme referred to in Article 16(2) of Directive 98/8/EC of the European Parliament and of the Council concerning the placing of biocidal products on the market. Official Journal of the European Union, No L 178, 09/07/2005: 1-98.
    16. Commission regulation (EC) No 1687/2002 of 25 September 2002 on an additional period for notification of certain active substances already on the market for biocidal use as established in Article 4(1) of Regulation (EC) No 1896/2000. Official Journal of the European Communities, No L 258, 26/09/2002: 15-16.
    17. Commission regulation (EC) No 1896/2000 of 7 September 2000 on the first phase of the programme referred to in the Article 16(2) of Directive 98/8/EC of the European Parliament and of the Council on biocidal products. Official Journal of the European Communities, No L 228, 08/09/2000: 6-17.
    18. Commission regulation (EC) No 2032/2003 of 4 November 2003 on the second phase of the 10-year work programme referred to in Article 16(2) of Directive 98/8/EC of the European Parliament and of the Council concerning the placing of biocidal products on the market, and amending Regulation (EC) No 1896/2000. Official Journal of the European Union, No L 307, 24/11/2003: 1-96.
    19. Costerton J.W., Geesey G.G., Cheng K.J. (1978): How bacteria stick. Scientific American, 238: 86-95. Go to original source... Go to PubMed...
    20. Costerton J.W., Stewart P.S., Greenberg E.P. (1999): Bacterial biofilms: a common cause of persistent infections. Science, 284: 1318-1322. Go to original source... Go to PubMed...
    21. Czechowski M.H., Banner M. (1992): Control of biofilms in breweries through cleaning and sanitizing. Technical Quarterly Master Brewers Association of the Americas, 29: 86-88.
    22. Dankert J., Hogt A.H., Feijen J. (1986): Biomedical polymers: bacterial adhesion, colonization, and identification. Critical Reviews in Biocompatibility, 2: 219-301.
    23. Davies D.G., Parsek M.R., Pearson J.P., Iglewski B.H., Costerton J.W., Greenberg E.P. (1998): The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science, 280: 295-298. Go to original source... Go to PubMed...
    24. De Silva G.D.I., Kantzanou M., Justice A., Massey R.C., Wilkinson A.R., Day N.P.J., Peacock S.J. (2002): The ica operon and biofilm production in coagulasenegative staphylococci associated with carriage and disease in neonatal intensive care unit. Journal of Clinical Microbiology, 40: 382-388. Go to original source... Go to PubMed...
    25. Directive 98/8/EC of the European Parliament and of the Council of 16 February 1998 concerning the placing of biocidal products on the market. Official Journal of the European Communities, No L 123, 24/04/1998: 1-63.
    26. Donlan R.M. (2001): Biofilm formation: a clinically relevant microbiological process. Clinical Infectious Diseases, 33: 1387-1392. Go to original source... Go to PubMed...
    27. Dunsmore D.G., Twomey A., Whittlestone W.G., Morgan H.W. (1981): Design and performance of systems for cleaning product-contact surfaces of food equipment: a review. Journal of Food Protection, 44: 220-240. Go to original source... Go to PubMed...
    28. EHEDG Document No. 8 (1993): Hygienic equipment design criteria. European Hygienic Engineering & Design Group, Frankfurt/Main.
    29. EHEDG Document No. 2 (2000): A method for the assessment of in-place cleanability of food processing equipment. European Hygienic Engineering & Design Group, Frankfurt/Main.
    30. EN 1040:2005: Chemical disinfectants and antiseptics. Quantitative suspension test for the evaluation of basic bactericidal activity of chemical disinfectants and antiseptics. Test method and requirements (phase 1).
    31. EN 12353:2006: Chemical disinfectants and antiseptics. Preservation of test organisms used for the determination of bactericidal, mycobactericidal, sporicidal and fungicidal activity.
    32. EN 1276:1997: Chemical disinfectants and antiseptics. Quantitative suspension test for the evaluation of bactericidal activity of chemical disinfectants and antiseptics used in food, industrial, domestic, and institutional areas. Test method and requirements (phase 2, step 1).
    33. EN 13697:2001: Chemical disinfectants and antiseptics. Quantitative non-porous surface test for the evaluation of bactericidal and/or fungicidal activity of chemical disinfectants used in food, industrial, domestic and institutional areas. Test method and requirements without mechanical action (phase 2, step 2).
    34. EN 13704:2002: Chemical disinfectants. Quantitative suspension test for the evaluation of sporicidal activity of chemical disinfectants used in food, industrial, domestic and institutional areas. Test method and requirements (phase 2, step 1).
    35. EN 1656:2000: Chemical disinfectants and antiseptics. Quantitative suspension test for the evaluation of bactericidal activity of chemical disinfectants and antiseptics used in veterinary field. Test method and requirements (phase 2, step 1).
    36. EN 1672-2:2005: Food processing machinery. Basic concepts. Part 2: Hygiene requirements.
    37. EN ISO 14159:2004: Safety of machinery. Hygiene requirements for the design of machinery.
    38. Flint S.H., Bremer P.J., Brooks J.D. (1997): Biofilms in dairy manufacturing plant - description, current concerns and methods of control. Biofouling, 11: 81-97. Go to original source...
    39. Frank J.F. (2001): Microbial attachment to food and food contact surfaces. Advances in Food and Nutrition Research, 43: 319-370. Go to original source... Go to PubMed...
    40. Gibson H., Taylor J.H., Hall K.E., Holah J.T. (1999): Effectiveness of cleaning techniques used in the food industry in terms of the removal of bacterial biofilms. Journal of Applied Microbiology, 87: 41-48. Go to original source... Go to PubMed...
    41. Gilbert P., Allison D.G., McBain A.J. (2002): Biofilms in vitro and in vivo: do singular mechanisms imply cross-resistance? Journal of Applied Microbiology, 92 (Suppl. 1): 98-110. Go to original source...
    42. Guðbjörnsdóttir B., Einarsson H., Thorkelsson G. (2005): Microbial adhesion to processing lines for fish fillets and cooked shrimp: influence of stainless steel surface finish and presence of gram-negative bacteria on the attachment of Listeria monocytogenes. Food Technology and Biotechnology, 43: 56-61.
    43. Hilbert L.R., Bagge-Ravn D., Kold J., Gram, L. (2003): Influence of surface roughness of stainless steel on microbial adhesion and corrosion resistance. International Biodeterioration and Biodegradation, 52: 175-185. Go to original source...
    44. Holah J.T. (1992): Industrial monitoring: Hygiene in food processing. In: Melo L.F., Bott T.R., Fletcher M., Capdeville B. (eds): Biofilms - Science and Technology. Springer, New York: 645-659. Go to original source...
    45. Holah J.T., Gibson H. (1999): Biofouling: Cleanability problems in food processing? In: Wirtanen G., Salo S., Mikkola A. (eds): Proceedings of 30th R3 - Nordic Contamination Control Symposium, VTT Symposium 193, Espoo: 177-186.
    46. Jang A., Szabo J., Hosni A.A., Coughlin M., Bishop P.L. (2006): Measurement of chlorine dioxide penetration in dairy process pipe biofilms during disinfection. Applied Microbiology and Biotechnology, 72: 368-376. Go to original source... Go to PubMed...
    47. Johnston M.D., Simons E.A., Lambert R.J. (2000): One explanation for the variability of the bacterial suspension test. Journal of Applied Microbiology, 88: 237-242. Go to original source... Go to PubMed...
    48. Jones M.B., Miller J.J., Brown W.E. (1986): Effectiveness of a quaternary ammonium compound in the presence of hard water and organic soil. Developments in Industrial Microbiology, 25: 771-777.
    49. Keener K.M., Bashor M.P., Curtis P.A., Sheldon B.W., Kathariou S. (2004): Comprehensive review of Campylobacter and poultry processing. Comprehensive Reviews. Food Science and Food Safety, 3: 105-116. Go to original source... Go to PubMed...
    50. Krönig B., Paul T. (1897): Die chemischen Grundlagen der Lehre von der Giftwirkung und Desinfection. Zeitschrift für Hygiene, 25: 1-112. Go to original source...
    51. Kumar C.G., Anand S.K. (1998): Significance of microbial biofilms in food industry: a review. International Journal of Food Microbiology, 42: 9-27. Go to original source... Go to PubMed...
    52. Langsrud S., Sidhu M.S., Heir E., Holck A.L. (2003): Bacterial disinfectant resistance - a challenge for the food industry. International Biodeterioration and Biodegradation, 51: 283-290. Go to original source...
    53. Larson E.L., Morton H.E. (1991): Alcohols. In: Block S.S. (ed.): Disinfection, Sterilization, and Preservation. 4th Ed. Lea & Febiger, London: 204-224.
    54. Lawrence J.R., Korber D.R., Hoyle B.D., Costerton J.W., Caldwell D.E. (1991): Optical sectioning of microbial biofilms. The Journal of Bacteriology, 173: 6558-6567. Go to original source... Go to PubMed...
    55. Le Chevallier M.W., Cawthon C.D., Lee R.G. (1988): Factors promoting survival of bacteria in chlorinated water supplies. Applied and Environmental Microbiology, 54: 649-654. Go to original source... Go to PubMed...
    56. Lelieveld H.L.M. (1985): Hygienic design and test methods. Journal of the Society of Dairy Technology, 38: 14-16. Go to original source...
    57. Lomander A., Schreuders P., Russek-Cohen E., Ali L. (2004): Evaluation of chlorines impact on biofilms on scratched stainless steel surfaces. Bioresource Technology, 94: 275-283. Go to original source... Go to PubMed...
    58. Luppens S.B.I., Reij M.W., van Der Heijden R.W.L., Rombouts F.M., Abee T. (2002): Development of a standard test to assess the resistance of Staphylococcus aureus biofilms cells to disinfectants. Applied and Environmental Microbiology, 68: 4194-4200. Go to original source... Go to PubMed...
    59. Mafu A.A., Roy D., Goulet J., Magny P. (1990): Attachment of Listeria monocytogenes to stainless steel, glass, polypropylene, and rubber surfaces after short contact times. Journal of Food Protection, 53: 742-746. Go to original source... Go to PubMed...
    60. Mattila-Sandholm T., Wirtanen G. (1992): Biofilm formation in the food industry: a review. Food Reviews International, 8: 573-603. Go to original source...
    61. Mettler E., Carpentier B. (1998): Variations over time of microbial load and physicochemical properties of floor materials after cleaning in food industry premises. Journal of Food Protection, 61: 57-65. Go to original source... Go to PubMed...
    62. Møretrø T., Hermansen L., Holck A.L., Sidhu M.S., Rudi K., Langsrud S. (2003): Biofilm formation and the presence of the intercellular adhesion locus ica among staphylococci from food and food processing environments. Applied and Environmental Microbiology, 69: 5648-5655. Go to original source... Go to PubMed...
    63. Morwood K. (2006): Step by step disinfectant evaluation. Cleanroom Technology Magazine (The European Journal of Contamination Control), 16 th February 2006. Available at http://www.cleanroom-technology.co.uk/story.asp?storyCode=38475
    64. Ntsama-Essomba C., Bouttier S., Ramaldes M., Dubois-Brissonet F., Fourniat J. (1997): Resistance of Escherichia coli growing as biofilms to disinfectants. Veterinary Research, 28: 353-363.
    65. Oulahal N., Martial-Gros A., Bonneau M., Blum L.J. (2004): Combined effect of chelating agents and ultrasound on biofilm removal from stainless steel surfaces. Application to Escherichia coli milk and Staphylococcus aureus milk biofilms. Biofilms, 1: 65-73. Go to original source...
    66. Peng J.S., Tsai W.C., Chou C.C. (2001): Surface characteristics of Bacillus cereus and its adhesion to stainless steel. International Journal of Food Microbiology, 65: 105-111. Go to original source... Go to PubMed...
    67. Peters A. (2003): Control of biofilm in the food industry: a microbiological survey of high-risk processing facilities. In: Lens P., O'Flaherty V., Moran A.P., Stoodley P., Mahony T. (eds): Biofilms in Medicine, Industry and Environmental Biotechnology: Characteristics, Analysis and Control. IWA Publishing, Cornwall: 554-567.
    68. Phelps E.B. (1911): The application of certain laws of physical chemistry in the standardization of disinfectants. The Journal of Infectious Diseases, 8: 27-38. Go to original source...
    69. Rayner J., Veeh R., Flood J. (2004): Prevalence of microbial biofilms on selected fresh produce and household surfaces. International Journal of Food Microbiology, 95: 29-39. Go to original source... Go to PubMed...
    70. Regulation (EC) No 178/2002 of the European Parliament and of the Council of 28 January 2002 laying down the general principles and requirements of food law, establishing the European Food Safety Authority and laying down procedures in matters of food safety. Official Journal of the European Communities, No L 31, 01/02/02: 1-24.
    71. Regulation (EC) No 852/2004 of the European Parliament and of the Council of 29 April 2004 on the hygiene of foodstuffs. Official Journal of the European Union, No L 226, 25/06/2004: 3-21.
    72. Regulation (EC) No 853/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules for food of animal origin. Official Journal of the European Union, No L 226, 25/06/2004: 22-82.
    73. Regulation (EC) No 854/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific rules for the organisation of official control on products of animal origin intended for human consumption. Official Journal of the European Union, No L 226, 25/06/2004: 83-127.
    74. Rodgers M., Zhan X.M. (2003): Moving-medium biofilm reactors. Reviews in Environmental Science and Biotechnology, 2: 213-224. Go to original source...
    75. Salo S., Mattila-Sandholm T., Wirtanen G. (2001): Do we need enhanced low pressure cleaning procedures for open process surfaces? In: Proceedings of 32nd R3 - Nordic Symposium on Contamination Control: 185-193.
    76. Sequiera C.A.C., Carrasquinho P.M.N.A., Cebola C.M. (1988): Control of microbial corrosion in cooling water systems by the use of biocides. In: Sequiera C.A.C., Tiller A.K. (eds): Microbial Corrosion 1. Elsevier Applied Science, Essex: 240-255.
    77. Sharma M., Anand S.K. (2002): Characterization of constitutive microflora of biofilms in dairy processing lines. Food Microbiology, 19: 627-636. Go to original source...
    78. Sidhu M.S., Langsrud S., Holck A. (2001): Disinfectant and antibiotic resistance of lactic acid bacteria isolated from food industry. Microbial Drug Resistance, 7: 73-83. Go to original source... Go to PubMed...
    79. Somers E.B., Wong A.C. (2004): Efficacy of two cleaning and sanitizing combinations on Listeria monocytogenes biofilms formed at low temperature on a variety materials in the presence of ready-to-eat meat residue. Journal of Food Protection, 67: 2218-2229. Go to original source... Go to PubMed...
    80. Springthorpe S. (2000): Disinfection of surfaces and equipment. Journal of the Canadian Dental Association, 66: 58-60.
    81. Stewart P.S., Rayner J., Roe F., Rees W.M. (2001): Biofilm penetration and disinfection efficacy of alkaline hypochlorite and chlorosulfamates. Journal of Applied Microbiology, 91: 523-532. Go to original source... Go to PubMed...
    82. Stoodley P., Hall-Stoodley L., Lappin-Scott H.M. (2001a): Detachment, surface migration, and other dynamic behavior in bacterial biofilms revealed by digital time-lapse imaging. Methods in Enzymology, 337: 306-319. Go to original source... Go to PubMed...
    83. Stoodley P., Wilson S., Hall-Stoodley L., Boyle J.D., Lappin-Scott H.M, Costerton J.W. (2001b): Growth and detachment of cell clusters from mature mixed- species biofilms. Applied and Environmental Microbiology, 67: 5608-5613. Go to original source... Go to PubMed...
    84. Suihko M.L., Salo S., Niclasen O., Guðbjörnsdóttir B., Torkelsson G., Bredholt S., Sjöberg A.M., Gustavsson P. (2002): Characterization of Listeria monocytogenes isolates from meat, poultry and seafood industries by automated ribotyping. International Journal of Food Microbiology, 72: 137-146. Go to original source... Go to PubMed...
    85. Tamine A.Y., Robinson R.K. (1999): Yoghurt: Science and Technology. Woodhead Publishing Ltd, Cambridge.
    86. Templeton C. (2005): Choosing the right cleaning and disinfection program for your operation. In: Proceedings of the 5th London Swine Conference - Production at the Leading Edge. 6-7 April 2005.
    87. Troller J.A. (1986): Water relations of foodborne bacterial pathogens - an update review. Journal of Food Protection, 49: 656-670. Go to original source... Go to PubMed...
    88. Troller J.A. (1993): Sanitation in food Processing. Academic Press, San Diego: 30-70, 263-286. Go to original source...
    89. Türetgen I. (2004): Comparison of the efficacy of free residual chlorine and monochloramine against biofilms in model and full scale cooling towers. Biofouling, 20: 81-85. Go to original source... Go to PubMed...
    90. Van Loosdrecht M.C.M., Lyklema J., Norde W., Zehnder A.J.B. (1989): Bacterial adhesion: A physicochemical approach. Microbial Ecology, 17: 1-15. Go to original source... Go to PubMed...
    91. Vidal D.R., Ragot C., Thibault F. (1997): Bacterial biofilms and resistance to disinfectants. Annales Pharmaceutiques Françaises, 55: 49-54. Go to PubMed...
    92. Watson H.E. (1908): A note on the variation of the rate of disinfection with change in the concentration of the disinfectant. Journal of Hygiene, 8: 536-542. Go to original source... Go to PubMed...
    93. Wirtanen G. (1995): Biofilm Formation and its Elimination from Food Processing Equipment. VTT Publications 251, Espoo: 106.
    94. Wirtanen G., Husmark U., Mattila-Sandholm T. (1996): Microbial evaluation of the biotransfer potential from surfaces with Bacillus biofilms after rinsing and cleaning procedures in closed food-processing systems. Journal of Food Protection, 59: 727-733. Go to original source... Go to PubMed...
    95. Wirtanen G., Juvonen R. (2002): Disinfectant efficacy on spoilage yeasts isolated from various food processes. In: Wilson D.I., Fryer P.J., Hastings A.P.M. (eds.): Fouling, Cleaning and Disinfection in Food Processing. City Services Design and Print, Cambridge: 189-196.
    96. Wirtanen G., Langsrud S., Salo S., Olofson U., Alnås H., Neuman M., Homeid J.P., Mattila-Sandholm T. (2002): Evaluation of Sanitation Procedures for Use in Daires. VTT Publication 481, Espoo: 96.
    97. Wirtanen G., Saarela M., Mattila-Sandholm T. (2000): Biofilms - Impact on hygiene in food industries. In: Bryers J. (ed.): Biofilms II: Process Analysis and Aplication. John Wiley - Liss, New York: 327-372.
    98. Wirtanen G., Salo S., Allison D.G., Mattila-Sandholm T., Gilbert P. (1998): Performance evaluation of disinfectant formulations using poloxamer-hydrogel biofilm-constructs. Journal of Applied Microbiology, 85: 965-971. Go to original source... Go to PubMed...
    99. Wirtanen G., Salo S. (2003): Disinfection in food processing - Efficacy testing of disinfectants. Reviews in Environmental Science and Biotechnology, 2: 293-306. Go to original source...
    100. Wirtanen G., Salo S. (2005): Improper dairy hygiene - Case studies on poor microbial ecology in the Nordic DairyNET project. In: 36th R3 - Nordic Symposium and 5th European Parenteral Conference of ESPC, 23-25 May 2005, Linköping: 171-182.
    101. Wirthlin M.R., Chen P.K., Hoover C.I. (2005): A laboratory model biofilm fermenter: design and initial trial on a single species biofilm. Journal of Periodontology, 9: 1443-1449. Go to original source... Go to PubMed...
    102. Zoltai P.T., Zottola E.A., McKay L.L. (1981): Scanning electron microscopy of microbial attachment to milk contact surfaces. Journal of Food Protection, 44: 204-208. Go to original source... Go to PubMed...
    103. Zottola E.A., Sasahara K.C. (1994): Microbial biofilms in the food processing industry - Should they be a concern? International Journal of Food Microbiology, 23: 125-148. Go to original source... Go to PubMed...

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