Biofilm formation by Staphylococcus aureus on food contact surfaces: Relationship with temperature and cell surface hydrophobicity

Food Control

Volumn 50, Issue , 2015, Pages 930-936

  Di Ciccio, P ^a   Vergara, A ^b   Festino, A R ^b   Paludi, D ^b   Zanardi, E ^a   Ghidini, S ^a   Ianieri, A ^a  

^a UNIVERSITY OF PARMA   (Italy)

^b UNIVERSITY OF TERAMO   (Italy)

Author keywords

Biofilm; Hydrophobicity; Polystyrene; Stainless steel; Staphylococcus aureus

Indexed keywords

EID: 84910660241     PISSN: 09567135     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodcont.2014.10.048     Document Type: Article

References (52)

1. Abdallah M., Benoliel C., Drider D., Dhulster P., Chihib N.E. Biofilm formation and persistence on abiotic surfaces in the context of food and medical environments. Archives of Microbiology 2014, 196:453-472.
2. Almeida R.R., Oliver S.P. Interaction of coagulase-negative Staphylococcus species with bovine mammary epithelial cells. Microbial Pathogenesis 2001, 31:205-212.
3. Archer N.K., Mazaitis M.J., Costerton J.W., Leid J.G., Powers M.E., Shirtliff M.E. Staphylococcus aureus biofilms Properties, regulation and roles in human disease. Virulence 2011, 2(5):445-459.
4. Arnold J.W., Bailey G.W. Surface finishes on stainless steel reduce bacterial attachment and early biofilm formation: scanning electron and atomic force microscopy study. Poultry Science 2000, 79:1839-1845.
5. Atshan S.S., Shamsudin M.N., Lung L.T., Sekawi Z., Ghaznavi-Rad E., Pei C.P. Comparative characterisation of genotypically different clones of MRSA in the production of biofilms. Journal of Biomedicine and Biotechnology 2012, 7. Article ID 417247.
6. Balaban M.S., Rasooly A. Staphylococcal enterotoxins. International Journal of Food Microbiology 2000, 61:1-10.
7. Braga L.C., Shupp J.W., Cummings C., Jett M., Takahashi J.A., Carmo L.S., et al. Pomegranate extract inhibits Staphylococcus aureus growth and subsequent enterotoxin production. Journal of Ethnopharmacology 2005, 96:335-339.
8. Cerca N., Jefferson K.K. Effect of growth conditions on poly-N-acetylglucosamine expression and biofilm formation in Escherichia coli. FEMS Microbiology Letters 2008, 283:36-41.
9. Cerca N., Pier G.B., Vilanova M., Oliveira R., Azeredo J. Quantitative analysis of adhesionn and biofilm formation on hydrophylic and hydrophobyc surfaces of clinical isolates of Staphylococcus epidermidis. Research in Microbiology 2005, 156:506-514.
10. Choi N.Y., Kim B.R., Bae Y.M., Lee S.Y. Biofilm formation, attachment, and cell hydrophobicity of foodborne pathogens under varied environmental conditions. Journal of the Korean Socety for Applied Biological Chemistry 2013, 56:207-220.
11. Costerton J.W. Introduction to biofilm. International Journal of Antimicrobial Agents 1999, 11:217-221.
12. Costerton J.W., Geesey G.G., Cheng K.J. How bacteria stick. Scientific American 1978, 238:86-95.
13. Cramton S.E., Gerke C., Schnell N.F., Nichols W.W., Götz F. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for bioilm formation. Infection and Immunity 1999, 67:5427-5433.
14. Cucarella C., Tormo M.A., Knecht E., Amorena B., Lasa I., Foster T.J., et al. Expression of the biofilm-associated protein interferes with host protein receptors of Staphylococcus aureus and alters the infective process. Infection and Immunity 2002, 70:3180-3186.
15. De Jesus Pimentel-Filho N.de F., Martins M.C., Bicalho Nogueira G., Cuquetto Mantovani H., Dantas Vanetti M.C. Bovicin HC5 and nisin reduce Staphylococcu aureus adhesion to polydtyrene and change the hydrophobicity profile and Gibbs free Energy of adhesion. International Journal of Food Microbiology 2014, 190:1-8.
16. Di Bonaventura G., Piccolomini R., Paludi D., D'Orio V., Vergara A., Conter M., et al. Influence of temperature on biofilm formation by Listeria monocytogenes on various food-contact surfaces: relationship with motility and cell surface hydrophobicity. Journal of Applied Microbiology 2008, 104:1552-1561.
17. Di Ciccio P., Conter M., Zanardi E., Ghidini S., Vergara A., Paludi D., et al. Listeria monocytogenes: biofilm in food processing. Italian Journal of Food Science 2012, 24(3):203-213.
18. Donlan R.M. Biofilms and device-associated infections. Emerging Infectious Diseases 2001, 7:277-281.
19. Donlan R.M., Costerton J.W. Biofilms: survival mechanisms of clinically relevant microorganisms. Clinical Microbiology Reviews 2002, 15:167-193.
20. Flemming H.C., Meier M., Schild T. Mini-review: microbial problems in paper production. Biofouling 2013, 29:683-696.
21. Fox L.K., Zadoks R.N., Gaskins C.T. Biofilm production by Staphylococcus aureus associated with intramammary infection. Veterinary Microbiology 2005, 107:295-299.
22. Giaouris E., Chorianopoulos N., Nychas G.J. Effect of temperature, pH, and water activity on biofilm formation by Salmonella enterica enteritidis PT4 on stainless steel surfaces as indicated by the bead vortexing method and conductance measurements. Journal of Food Protection 2005, 68:2149-2154.
23. Giaouris E., Heir E., Hébraud M., Chorianopoulos N., Langsrud S., Møretrø T., et al. Attachment and biofilm formation by foodborne bacteria in meat processing environments: causes, implications, role of bacterial interactions and control by alternative novel methods. Meat Science 2014, 97:298-309.
24. Gibson H., Taylor J.H., Hall K.E., Holah J.T. Effectiveness of cleaning techniques used in the food industry in terms of the removal of bacterial biofilms. Journal of Applied Microbiology 1999, 87(1):41-48.
25. Gounadaki A.S., Skandamis P.N., Drosinos E.H., Nychas G.J. Microbial ecology of food contact surfaces and products of small-scale facilities producing traditional sausages. Food Microbiology 2008, 25:313-323.
26. Gutiérrez D., Delgado S., Vázquez-Sánchez D., Martínez B., López Cabo M., Rodríguez A., et al. Incidence of Staphylococcus aureus and analysis of associated bacterial communities on food Industry surfaces. Applied and Environmental Microbiology 2012, 78(24):8547-8554.
27. Hamadi F., Asserne F., Elabed S., Bensouda S., Mabrouki M., Latrache H. Adhesion of Staphylococcus aureus on stainless steel treated with three types of milk. Food Control 2014, 38:104-108.
28. Hamadi F., Latrache H., Mabrrouki M., Elchmari A., Outzourhit A., Ellouali M., et al. Effect of pH on distribution and adhesion of Staphylococcus aureus to glass. Journal of Adhesion and Science of Technology 2005, 19:73-85.
29. Katsikogianni M., Spiliopoulou I., Dowling D.P., Missirlis Y.F. Adhesion of slime producing Staphylococcus epidermidis strains to PVC and diamond-like carbon/silver/fluorinated coatings. Journal of Materials Science: Materials in Medicine 2006, 17:679-689.
30. Kusumaningrum H.D., Riboldi G., Hazeleger W.C., Beumer R.R. Survival of foodborne pathogens on stainless steel surfaces and cross-contamination to foods. International Journal of Food Microbiology 2003, 85:227-236.
31. Lee S.H.I., Mangolin B.L.C., Gonçalves J., Neeff D.V., Silva M.P., Cruz A.G., et al. Biofilm-producing ability of Staphylococcus aureus isolates from Brazilian dairy farms. Journal of Dairy Science 2013, 97:1812-1816.
32. Leite de Souza E., Silva Meira Q.G., de Medeiros Barbosa I., Alves Aguiar Athayde A.J., da Conceição M.L., de Siqueira Júnior J.P. Biofilm formation by Staphylococcus aureus from food contact surfaces in a meat-based broth and sensitivity to sanitizers. Brazilian Journal of Microbiology 2014, 45:67-75.
33. Malheiros P.S., Passos C.T., Casarin L.S., Serraglio L., Tondo E.C. Evaluation of growth and transfer of Staphylococcus aureus from poultry meat to surfaces of stainless steel and polyethylene and their disinfection. Food Control 2010, 21:298-301.
34. Marques S.C., Rezende J.D.G.O.S., Aparecida de Freitas Alves L., Silva B.C., Alves E., Ronaldo de Abreu L., et al. Formation of biofilms by Staphylococcus aureus on stainless steel and glass surface and its resistance to some selected chemical sanitizers. Brazilian Journal of Microbiology 2007, 38:538-543.
35. Mattila Sandholm T., Wirtanen G. Biofilm formation in the industry: a review. Food Reviews International 1992, 8(4):573-603.
36. Mattos-Guaraldi A.L., Formiga L.C.D., Andrade A.F.B. Cell surface hydrophobicity of sucrose fermenting and nonfermenting Corynebacterium diphtheriae strains evaluated by different methods. Current Microbiology 1999, 38:37-42.
37. Nilsson R.E., Ross T., Bowman J.P. Variability in biofilm production by Listeria monocytogenes correlated to strain origin and growth conditions. International Journal of Food Microbiology 2011, 150:14-24.
38. Nostro A., Blanco A.R., Cannatelli M.A., Enea V., Flamini G., Morelli I., et al. Susceptibility of methicillin-resistant staphylococci to oregano essential oil, carvacrol and thymol. FEMS Microbiology Letters 2004, 230:191-195.
39. 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.
40. Pagedar A., Singh J. Influence of physiological cell stages on biofilm formation by Bacillus cereus of dairy origin. International Dairy Journal 2012, 23:30-35.
41. Pagedar A., Singh J., Batish V.K. Surface hydrophobicity, nutritional contents affect Staphylococcus aureus biofilms and temperature influences its survival in preformed biofilms. Journal of Basic Microbiology 2010, 50:S98-S106.
42. Regulation (EC) n.853/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules for on the hygiene of foodstuffs. G.U.L. n.139 del 30/04/2004.
43. Rode T.M., Langsrud S., Holck A., Moretto T. Different patterns of biofilm formation in Staphylococcus aureus under food-related stress conditions. International Journal of Food Microbiology 2007, 116:372-383.
44. Seidl K., Stucki M., Ruegg M., Goerke C., Wolz C., Harris L., et al. Staphylococcus aureus CcpA affects biofilm formation. Infection and Immunity 2008, 76:2044-2050.
45. Silva-Meira Q.G., Medeiros-Barbosa I., Athayde A.J.A.A., Siqueira-Júnior J.P., Souza E.L. Influence of temperature and surface kind on biofilm formation by Staphylococcus aureus from food-contact surfaces and sensitivity to sanitizers. Food Control 2012, 25:469-475.
46. Simões M., Simões L.C., Vieira M.J. Areview of current and emergent biofilm control strategies. LWT-Food Science Technology 2010, 43:573-583.
47. Tang L., Pillai S., Revesbech N.P., Schramm A., Bischoff C., Meyer R.L. Biofilm retention on surfaces with variable roughness and hydrophobicity. Biofouling 2011, 27:111-121.
48. Vasudevan P., Nair M.K., Annamalai T., Venkitanarayanan K.S. Phenotypic and genotypic characterization of bovine mastitis isolates of Staphylococcus aureus for biofilm formation. Veterinary Microbiology 2003, 92:179-185.
49. Vázquez-Sánchez D., Cabo M.L., Ibusquiza P.S., Rodríguez-Herrera J.J. Biofilm-forming ability and resistance to industrial disinfectants of Staphylococcus aureus isolated from fishery products. Food Control 2014, 39:8-16.
50. Vázquez-Sánchez D., Habimana O., Holck A. Impact of food-related environmental factors on the adherence and biofilm formation of natural Staphylococcus aureus isolates. Current Microbiology 2013, 66:110-121.
51. Vlkova H., Babak V., Seydlova R., Pavlik I., Schlegelova J. Biofilms and hygiene on dairy farms and in the dairy industry: sanitation chemical products and their effectiveness on biofilms-a Review. Czech Journal of Food Science 2008, 26:309-323.
52. Wirtanen G., Husmark U., Matilla-Sandholm T. 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 1996, 59(7):727-733.