Biofilm formation by Gram-positive bacteria including Staphylococcus aureus, Mycobacterium avium and Enterococcus spp. in food processing environments

Biofilms in the Food and Beverage Industries

Volumn , Issue , 2009, Pages 250-269

  Langsrud, S ^a  

^a NORWEGIAN FOOD RESEARCH INSTITUTE   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84902633948     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1533/9781845697167.2.250     Document Type: Chapter

References (97)

1. Archuleta R.J., Mullens P., Primm T.P. The relationship of temperature to desiccation and starvation tolerance of the Mycobacterium avium complex. Archives of Microbiology 2002, 178:311-314.
2. Asao T., Kumeda Y., Kawai T., Shibata T., Oda H., Haruki K., Nakazawa H., Kozaki S. An extensive outbreak of staphylococcal food poisoning due to low-fat milk in Japan: estimation of enterotoxin A in the indiscriminated milk and powdered skim milk. Epidemiology and Infection 2003, 130:33-40.
3. Baird-Parker T.C. The microbiological safety and quality of food. Staphylococcus aureus 2000, Aspen Publishers, Gaithersburg. B.M. Lund, T.C. Baird-Parker, G.W. Gould (Eds.).
4. Boles B.R., Horswill A.R. agr-Mediated Dispersal of Staphylococcus aureus Biofilms: PLoS Pathogens 2008, v. 4, p. e1000052.
5. Bolton K.J., Dodd C.E.R., Mead G.C., Waites W.M. Chlorine resistance of strains of Staphylococcus aureus isolated from poultry processing plants. Letters in Applied Microbiology 1988, 6:31-34.
6. Boyce J.M. Environmental contamination makes an important contribution to hospital infection. Journal of Hospital Infection 2007, 65:50-54.
7. Cafiso V., Bertuccio T., Santagati M., Demelio V., Spina D., Nicoletti G., Stefani S. agr-Genotyping and transcriptional analysis of biofilm-producing Staphylococcus aureus. FEMS Immunology and Medical Microbiology 2007, 51:220-227.
8. Carpentier B., Chassaing D. Interactions in biofilms between Listeria monocytogenes and resident microorganisms from food industry premises. International Journal of Food Microbiology 2004, 97:111-122.
9. Cramton S.E. Anaerobic conditions induce expression of polysaccharide intercellular adhesin in Staphylococcus aureus and Staphylococcus epidermidis. Infection and Immunity 2001, 69:4079.
10. Cramton S.E., Gerke C., Schnell N.F., Nichols W.W., Gotz F. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infection and Immunity 1999, 67:5427-5433.
11. Cucarella C. Role of biofilm-associated protein bap in the pathogenesis of bovine Staphylococcus aureus. Infection and Immunity 2004, 72:2177.
12. Cucarella C., Solano C., Valle J., Amorena B., Lasa I., Penades J.R. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. Journal of Bacteriology 2001, 183:2888-2896.
13. Deza M.A., Araujo M., Garrido M.J. Inactivation of Escherichia coli, Listeria monocytogenes, Pseudomonas aeruginosa and Staphylococcus aureus on stainless steel and glass surfaces by neutral electrolysed water. Letters in Applied Microbiology 2005, 40:341-346.
14. Dodd C.E.R., Mead G.C., Waites W.M. Detection of the site of contamination by Staphylococcus aureus within the defeathering machinery of a poultry-processing plant. Letters in Applied Microbiology 1988, 7:63-66.
15. Dunowska M., Morley P.S., Hyatt D.R. The effect of Virkon®S fogging on survival of Salmonella enterica and Staphylococcus aureus on surfaces in a veterinary teaching hospital. Veterinary Microbiology 2005, 105:281-289.
16. Evans J.A., Russell S.L., James C., Corry J.E.L. Microbial contamination of food refrigeration equipment. Journal of Food Engineering 2004, 62:225-232.
17. Fitzpatrick F., Humphreys H., O'Gara J.P. Evidence for icaADBC-independent biofilm development mechanism in methicillin-resistant Staphylococcus aureus clinical isolates. Journal of Clinical Microbiology 2005, 43:1973-1976.
18. Fitzpatrick F., Humphreys H., O'Gara J.P. Environmental regulation of biofilm development in methicillin-resistant and methicillin-susceptible Staphylococcus aureus clinical isolates. Journal of Hospital Infection 2006, 62:120-122.
19. Fuster-Valls N., Hernadez-Herrero M., Marin-De-Mateo M., Rodriguez-Jerez J.J. Effect of different environmental conditions on the bacteria survival on stainless steel surfaces. Food Control 2008, 19:308-314.
20. Gelinas P., Goulet J., Tastayre G.M., Picard G.A. Effect of temperature and contact time on the activity of eight disinfectants - a classification. Journal of Food Protection 1984, 47:841-847.
21. Gibbs P.A., Patterson J.T., Thompson J.K. Distribution of Staphylococcus aureus in a poultry-processing plant. Journal of Applied Bacteriology 1978, 44:401-410.
22. Gibson H., Taylor J.H., Hall K.H., Holah J.T. Biofilms and their detection in the food industry 1995, Campden and Chorleywood Food Research Association (CCFRA), Gloucesterchire, UK.
23. Gibson H., Taylor J.H., Hall K.E., Holah J.T. Effectiveness of cleaning techniques used in the food industry in terms of removal of bacterial biofilms. Journal of Applied Microbiology 1999, 87:41-48.
24. Giraffa G. Enterococci from foods. FEMS Microbiology Reviews 2002, 26:163-171.
25. Gounadaki A.S., Skandamis P.N., Drosinos E.H., Nychas G.J.E. Microbial ecology of food contact surfaces and products of small-scale facilities producing traditional sausages. Food Microbiology 2008, 25:313-323.
26. Gross M. Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces. Infection and Immunity 2001, 69:3423.
27. Guzel-Seydim Z., Bever P.I., Greene A.K. Efficacy of ozone to reduce bacterial populations in the presence of food components. Food Microbiology 2004, 21:475-479.
28. Heir E., Sundheim G., Holck A.L. Identification and characterization of quaternary ammonium compound resistant staphylococci from the food industry. International Journal of Food Microbiology 1999, 48:211-219.
29. Heir E., Sundheim G., Holck A.L. The qacG gene on plasmid pST94 confers resistance to quaternary ammonium compounds in staphylococci isolated from the food industry. Journal of Applied Microbiology 1999, 86:378-388.
30. Herrera J.J.R., Cabo M.L., Gonzalez A., Pazos I., Pastoriza L. Adhesion and detachment kinetics of several strains of Staphylococcus aureus subsp aureus under three different experimental conditions. Food Microbiology 2007, 24:585-591.
31. Holmberg S.D., Blake P.A. Staphylococcal food poisoning in the United States - new facts and old misconceptions. Jama - Journal of the American Medical Association 1984, 251:487-489.
32. Izano E.A., Amarante M.A., Kher W.B., Kaplan J.B. Differential roles of Poly-N-acetylglucosamin surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Applied and Environmental Microbiology 2008, 74:470-476.
33. Johnson M., Cockayne A., Williams P.H., Morrissey J.A. Iron-responsive regulation of biofilm formation in Staphylococcus aureus involves Fur-dependent and Fur-independent mechanisms. Journal of Bacteriology 2005, 187:8211-8215.
34. Jones T.F., Kellum M.E., Porter S.S., Bell M., Schaffner W. An outbreak of community-acquired foodborne illness caused by methicillin-resistant Staphylococcus aureus. Emerging Infectious Diseases 2002, 8:82-84.
35. Jono K., Takayama T., Kuno M., Higashide E. Effect of alkyl chain length of benzalkonium chloride on the bactericidal activity and binding to organic materials. Chemical and Pharmaceutical Bulletin 1986, 34:4215-4224.
36. Jorgensen H.J., Mork T., Rorvik L.M. The occurrence of Staphylococcus aureus on a farm with small-scale production of raw milk cheese. Journal of Dairy Science 2005, 88:3810-3817.
37. Kennedy C.A. Contribution of culture media and chemical properties of polystyrene tissue culture plates to biofilm development by Staphylococcus aureus. Journal of Medical Microbiology 2004, 53:1171.
38. Kennedy J., Jackson V., Blair I.S., Mcdowell D.A., Cowan C., Bolton D.J. Food safety knowledge of consumers and the microbiological and temperature status of their refrigerators. Journal of Food Protection 2005, 68:1421-1430.
39. Kim J.H., Jo C., Rho Y.T., Lee C.B., Byun M.W. Comparison of gamma irradiation and sodium hypochlorite treatments to inactivate Staphylococcus aureus and Pseudomonas aeruginosa biofilms on stainless steel surfaces. Food Science and Biotechnology 2007, 16:315-319.
40. Kishimoto M., Hioki Y., Okano T., Konuma H., Takamizawa K., Kashio H., Kasuga F. Ribotyping and a study of transmission of Staphylococcus aureus collected from food preparation facilities. Journal of Food Protection 2004, 67:1116-1122.
41. Kleiss T., Van Schothorst M., Cordier J.-L., Untermann F. Staphylococci in a whey powder plant environment: an ecological survey as a contribution to HACCP studies. Food Control 1994, 5:196-199.
42. Kluytmans J., Vanleeuwen W., Goessens W., Hollis R., Messer S., Herwaldt L., Bruining H., Heck M., Rost J., Vanleeuwen N., Vanbelkum A., Verbrugh H. Food-initiated outbreak of methicillin-resistant Staphylococcus aureus analyzed by phenotyping and genotyping. Journal of Clinical Microbiology 1995, 33:1121-1128.
43. Kolawole D.O. Resistance mechanisms of mucoid-grown Staphylococcus aureus to the antibacterial action of some disinfectants and antiseptics. FEMS Microbiology Letters 1984, 25:205-209.
44. Kong K.F., Vuong C., Otto M. Staphylococcus quorum sensing in biofilm formation and infection. International Journal of Medical Microbiology 2006, 296:133-139.
45. Kristian S.A. The ability of biofilm formation does not influence virulence of Staphylococcus aureus and host response in a mouse tissue cage infection model. Microbial Pathogenesis 2004, 36:237.
46. Langsrud S., Sundheim G. Factors contributing to a suspension test method for antimicrobial activity of disinfectants. Journal of Applied Microbiology 1998, 85:1006-1012.
47. Langsrud S., Sidhu M.S., Heir E., Holck A.L. Bacterial disinfectant resistance - a challenge for the food industry. International Biodeterioration &Biodegradation 2003, 51:283-290.
48. Langsrud S., Seifert L., Møretrø T. Characterization of the microbial flora in disinfecting footbaths with hypochlorite. Journal of Food Protection 2006, 69:2193-2198.
49. Lasa I., Penades J.R. Bap: A family of surface proteins involved in biofilm formation. Research in Microbiology 2006, 157:99-107.
50. Lim Y. Control of glucose- and NaCI-induced biofilm formation by rbf in Staphylococcus aureus. Journal of Bacteriology 2004, 186:722.
51. Loir Y., Baron F., Gautier M. Staphylococcus aureus and food poisoning. Genetics and Molecular Research 2003, 2:63-76.
52. Luppens S.B.I., Reij M.W., Van Der Heijden R.W.L., Rombouts F.M., Abee T. Development of a standard test to assess the resistance of Staphylococcus aureus biofilm cells to disinfectants. Applied and Environmental Microbiology 2002, 68:4194-4200.
53. Mack D., Becker P., Chatterjee I., Dobinsky S., Knobloch J.K.M., Peters G., Rohde H., Herrmann M. Mechanisms of biofilm formation in Staphylococcus epidermidis and Staphylococcus aureus: functional molecules, regulatory circuits, and adaptive responses. International Journal of Medical Microbiology 2004, 294:203-212.
54. Mack D., Davies A.P., Harris L.G., Rohde H., Horstkotte M.A., Knobloch J.K.M. Microbial interactions in Staphylococcus epidermidis biofilms. Analytical and Bioanalytical Chemistry 2007, 387:399-408.
55. Mead G.C., Norris A.P., Bratchell N. Differentiation of Staphylococcus aureus from freshly slaughtered poultry and strains endemic to processing plants by biochemical and physiological tests. Journal of Applied Bacteriology 1989, 66:153-159.
56. Mead P.S., Slutsker L., Dietz V., Mccaig L.F., Bresee J.S., Shapiro C., Griffin P.M., Tauxe R.V. Food-related illness and death in the United States. Emerging Infectious Diseases 1999, 5:607-625.
57. Minei C.C., Gomes B.C., Ratti R.P., D'Angelis C.E.M., De Martinis E.C.P. Influence of peroxyacetic acid and nisin and coculture with Enterococcus faecium on Listeria monocytogenes biofilm formation. Journal of Food Protection 2008, 71:634-638.
58. Mohamed J.A., Huang D.B. Biofilm formation by enterococci. Journal of Medical Microbiology 2007, 56:1581-1588.
59. Moreno M.R.F., Sarantinopoulos P., Tsakalidou E., De Vuyst L. The role and application of enterococci in food and health. International Journal of Food Microbiology 2006, 106:1-24.
60. Moretro T., Hermansen L., Holck A.L., Sidhu M.S., Rudi K., Langsrud S. Biofilm formation and the presence of the intercellular adhesion locus ica, among staphylococci from food and food processing environments. Applied and Environmental Microbiology 2003, 69:5648-5655.
61. Morot-Bizot S.C., Leroy S., Talon R. Staphylococcal community of a small unit manufacturing traditional dry fermented sausages. International Journal of Food Microbiology 2006, 108:210-217.
62. Murray R.J. Recognition and management of Staphylococcus aureus toxin-mediated disease. International Medicine journal 2005, 35:S106-S119.
63. Normanno G., Firinu A., Virgilio S., Mula G., Dambrosio A., Poggiu A., Decastelli L., Mioni R., Scuota S., Bolzoni G., Di Giannatale E., Salinetti A.P., La Salandra G., Bartoli M., Zuccon F., Pirino T., Sias S., Parisi A., Quaglia N.C., Celano G.V. Coagulase-positive Staphylococci and Staphylococcus aureus in food products marketed in Italy. International Journal of Food Microbiology 2005, 98:73-79.
64. Notermans S., Dufrenne J., Vanleeuwen W.J. Contamination of broiler-chickens by Staphylococcus aureus during processing - incidence and origin. Journal of Applied Bacteriology 1982, 52:275-280.
65. O'Gara J.P. ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiology Letters 2007, 270:179-188.
66. Oie S. Efficacy of disinfectants against biofilm cells of methicillin-resistant Staphylococcus aureus. Microbios 1996, 85:223-230.
67. O'Neill E. Association between methicillin susceptibility and biofilm regulation in Staphylococcus aureus isolates from device-related infections. Journal of Clinical Microbiology 2007, 45:1379.
68. Orth R., Mrozeck H. Is the control of Listeria, Campylobacter and Yersinia a disinfection problem?. Fleischwirtsch 1989, 69:1575-1576.
69. Otter J.A., Cummins M., Ahmad F., Van Tonder C., Drabu Y.J. Assessing the biological efficacy and rate of recontamination following hydrogen peroxide vapour decontamination. Journal of Hospital Infection 2007, 67:182-188.
70. Oulahal N., Martial-Gros A., Bonneau M., Blum L.J. Removal of meat biofilms from surfaces by ultrasounds combined with enzymes and/or a chelating agent. Innovative Food Science &Emerging Technologies 2007, 8:192-196.
71. Oulahal N., Brice W., Martial A., Degraeve P. Quantitative analysis of survival of Staphylococcus aureus or Listeria innocua on two types of surfaces: Polypropylene and stainless steel in contact with three different dairy products. Food Control 2008, 19:178-185.
72. Pompermayer D.M.C., Gaylarde C.C. The influence of temperature on the adhesion of mixed cultures of Staphylococcus aureus and Escherichia coli to polypropylene. Food Microbiology 2000, 17:361-365.
73. Qin Z.Q., Ou Y.Z., Yang L.A., Zhu Y.L., Tolker-Nielsen T., Molin S., Qu D. Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology-Sgm 2007, 153:2083-2092.
74. Rice K.C., Mann E.E., Endres J.L., Weiss E.C., Cassat J.E., Smeltzer M.S., Bayles K.W. The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:8113-8118.
75. Rode T.M., Langsrud S., Holck A., MøRetrø T. Different patterns of biofilm formation in Staphylococcus aureus under food-related stress conditions. International Journal of Food Microbiology 2007, 116:372-383.
76. Rodgers J.D., Mccullagh J.J., Mcnamee P.T., Smyth J.A., Ball H.J. An investigation into the efficacy of hatchery disinfectants against strains of Staphylococcus aureus associated with the poultry industry. Veterinary Microbiology 2001, 82:131-140.
77. Rohde H. Polysaccharide intercellular adhesin or protein factors in biofilm accumulation of Staphylococcus epidermidis and Staphylococcus aureus isolated from prosthetic hip and knee joint infections. Biomaterials 2007, 28:1711.
78. Rossoni E.M.M., Gaylarde C.C. Comparison of sodium hypochlorite and peracetic acid as sanitising agents for stainless steel food processing surfaces using epifluorescence microscopy. International Journal of Food Microbiology 2000, 61:81-85.
79. Rowe M.T., Grant I.R. Mycobacterium avium spp. paratuberculosis and its potential survival tactics. Letters in Applied Microbiology 2006, 42:305-311.
80. Sagripanti J.L., Eklund C.A., Trost P.A., Jinneman K.C., Abeyta C., Kaysner C.A., Hill W.E. Comparative sensitivity of 13 species of pathogenic bacteria to seven chemical germicides. American Journal of Infection Control 1997, 25:335-339.
81. Shale K., Lues J.F.R., Venter P., Buys E.M. The distribution of Staphylococcus sp on bovine meat from abattoir deboning rooms. Food Microbiology 2005, 22:433-438.
82. Sharma M., Anand S.K. Characterization of constitutive microflora of biofilms in dairy processing lines. Food Microbiology 2002, 19:627-636.
83. Sidhu M., Heir E., K L., Wiger K., Holck A. Frequency of disinfectant resistance genes and genetic linkage with beta-lactamase transposon Tn552 among clinical staphylococci. Antimicrobial Agents and Chemotherapy 2002, 46:2797-2803.
84. Sidhu M.S., Heir E., Sorum H., Holck A. Genetic linkage between resistance to quaternary ammonium compounds and beta-lactam antibiotics in food-related Staphylococcus spp. Microbial Drug Resistance 2001, 7:363-371.
85. Skovgaard N. New trends in emerging pathogens. International Journal of Food Microbiology 2007, 120:217-224.
86. Sneed J., Strohbehn C., Gilmore S.A., Mendonca A. Microbiological evaluation of foodservice contact surfaces in Iowa assisted-living facilities. Journal of the American Dietetic Association 2004, 104:1722-1724.
87. Soriano J.M., Font G., Molto J.G., Manes J. Enterotoxigenic staphylococci and their toxins in restaurant foods. Trends in Food Science &Technology 2002, 13:60-67.
88. Steed K.A., Falkinham J.O. Effect of growth in biofilms on chlorine susceptibility of Mycobacterium avium and Mycobacterium intracellulare. Applied and Environmental Microbiology 2006, 72:4007-4011.
89. Toledo-Arana A., Merino N., Vergara-Irigaray M., Dearbouille M., Penades J.R., Lasa H. Staphylococcus aureus develops an alternative, ica-independent biofilm in the absence of the arlRS two-component system. Journal of Bacteriology 2005, 187:5318-5329.
90. Top J., Willems R., Bonten M. Emergence of CC17 Enterococcus faecium: from commensal to hospital-adapted pathogen. FEMS Immunology and Medical Microbiology 2008, 52:297-308.
91. Vaerevijck M.J.M., Huys G., Palomino J.C., Swings J., Portaels F. Mycobacteria in drinking water systems: ecology and significance for human health. FEMS Microbiology Reviews 2005, 29:911-934.
92. Valle J., Toledo-Arana A., Berasain C., Ghigo J.M., Amorena B., Penades J.R., Lasa I. SarA and not sigma(B) is essential for biofilm development by Staphylococcus aureus. Molecular Microbiology 2003, 48:1075-1087.
93. Vergara-Irigaray M., Maira-Litran T., Merino N., Pier G.B., Penades J.R., Lasa I. Wall teichoic acids are dispensable for anchoring the PNAG exopolysaccharide to the Staphylococcus aureus cell surface. Microbiology-Sgm 2008, 154:865-877.
94. Vuong C., Saenz H.L., Gotz F., Otto M. Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus. Journal of Infectious Diseases 2000, 182:1688-1693.
95. Yarwood J.M., Paquette K.M., Tikh I.B., Volper E.M., Greenberg E.P. Generation of virulence factor variants in Staphylococcus aureus biofilms. Journal of Bacteriology 2007, 189:7961-7967.
96. Zetola N., Francis J.S., Nuermberger E.L., Bishai W.R. Community-acquired meticillin-resistant Staphylococcus aureus: an emerging threat. Lancet Infectious Diseases 2005, 5:275-286.
97. Zhao T., Doyle M.P., Zhao P. Control of Listeria monocytogenes in a biofilm by competitive-exclusion microorganisms. Applied and Environmental Microbiology 2004, 70:3996-4003.