Attachment and biofilm formation by Escherichia coli O157:H7 at different temperatures, on various food-contact surfaces encountered in beef processing

International Journal of Food Microbiology

Volumn 149, Issue 3, 2011, Pages 262-268

  Dourou, Dimitra ^a,b   Beauchamp, Catherine Simpson ^a   Yoon, Yohan ^a   Geornaras, Ifigenia ^a   Belk, Keith E ^a   Smith, Gary C ^a   Nychas, George John E ^b   Sofos, John N ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b AGRICULTURAL UNIVERSITY OF ATHENS   (Greece)

Author keywords

Attachment; Beef fabrication surfaces; Biofilms; Escherichia coli O157:H7; Soiling substrates

Indexed keywords

POLYETHYLENE; RIFAMPICIN; STAINLESS STEEL;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL COUNT; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIUM ADHERENCE; BEEF; BIOFILM; COLONY FORMING UNIT; CULTURE MEDIUM; ESCHERICHIA COLI O157; FOOD PROCESSING; HOMOGENATE; INCUBATION TIME; NONHUMAN; PH; STORAGE TEMPERATURE; TEMPERATURE DEPENDENCE;

ANIMALS; BIOFILMS; CATTLE; COLONY COUNT, MICROBIAL; ESCHERICHIA COLI; ESCHERICHIA COLI O157; FOOD HANDLING; MEAT; POLYETHYLENE; STAINLESS STEEL; TEMPERATURE; WATER;

ESCHERICHIA COLI;

EID: 80051597505     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2011.07.004     Document Type: Article

References (45)

1. Allan J.T., Yan Z., Kornacki J.L. Surface material, temperature, and soil effects on the survival of selected foodborne pathogens in the presence of condensate. Journal of Food Protection 2004, 67:2666-2670.
2. Aslam M., Greer G.G., Nattress F.M., Gill C.O., McMullen L.M. Genotypic analysis of Escherichia coli recovered from product and equipment at a beef-packing plant. Journal of Applied Microbiology 2004, 97:78-86.
3. Bacon R.T., Sofos J.N. Characteristics of biological hazards in foods. Food Safety Handbook 2003, 157-196. John Wiley and Sons, Inc., Hoboken, NJ. R.H. Schmidt, G.E. Rodrick (Eds.).
4. Barkocy-Gallagher G.A., Arthur T.M., Siragusa G.R., Keen J.E., Elder R.O., Laegreid W.W., Koohmaraie M. Genotypic analyses of Escherichia coli O157:H7 and O157 nonmotile isolates recovered from beef cattle and carcasses at processing plants in the Midwestern states of the United States. Applied and Environmental Microbiology 2001, 67:3810-3818.
5. Carpentier B., Cerf O. Biofilms and their consequences, with particular reference to hygiene in the food industry. Journal of Applied Bacteriology 1993, 75:499-511.
6. 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.
7. Castonguay M.-H., van der Schaaf S., Koester W., Krooneman J., van der Meer W., Harmsen H., Landini P. Biofilm formation by Escherichia coli is stimulated by synergistic interactions and co-adhesion mechanisms with adherence-proficient bacteria. Research in Microbiology 2006, 157:471-478.
8. Chmielewski R.A.N., Frank J.F. Biofilm formation and control in food processing facilities. Comprehensive Reviews in Food Science and Food Safety 2003, 2:22-32.
9. Davies D.G., Parsek M.R., Pearson J.P., Iglewski B.H., Costerton J.W., Greenberg E.P. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 1998, 280:295-298.
10. Dewanti R., Wong A.C.L. Influence of culture conditions on biofilm formation by Escherichia coli O157:H7. International Journal of Food Microbiology 1995, 26:147-164.
11. Donlan R.M., Costerton J.W. Biofilms: survival mechanisms of clinically relevant microorganisms. Clinical Microbiology Reviews 2002, 15:167-193.
12. Giaouris E.D., Nychas G.-J.E. The adherence of Salmonella Enteritidis PT4 to stainless steel: the importance of the air-liquid interface and nutrient availability. Food Microbiology 2006, 23:747-752.
13. Gill C.O., McGinnis J.C. Contamination of beef trimmings with Escherichia coli during a carcass breaking process. Food Research International 2000, 33:125-130.
14. Gill C.O., McGinnis J.C., Bryant J. Contamination of beef chucks with Escherichia coli during carcass breaking. Journal of Food Protection 2001, 64:1824-1827.
15. Gun H., Yilmaz A., Turker S., Tanlasi A., Yilmaz H. Contamination of bovine carcasses and abattoir environment by Escherichia coli O157:H7 in Istanbul. International Journal of Food Microbiology 2003, 84:339-344.
16. Hood S.K., Zottola E.A. Biofilms in food processing. Food Control 1995, 6:9-18.
17. Hood S.K., Zottola E.A. Isolation and identification of adherent gram-negative microorganisms from four meat-processing facilities. Journal of Food Protection 1997, 60:1135-1138.
18. Irie Y., Parsek M.R. Quorum sensing and microbial biofilms. Book Series: Current Topics in Microbiology and Immunology 2008, vol. 322:67-84. Springer-Verlag, Heidelberg, Berlin. T. Romeo (Ed.).
19. James G.A., Beaudette L., Costerton J.W. Interspecies bacterial interactions in biofilms. Journal of Industrial Microbiology 1995, 15:257-262.
20. Kauppi K.L., Tatini S.R., Harrell F., Feng P. Influence of substrate and low temperature on growth and survival of verotoxigenic Escherichia coli. Food Microbiology 1996, 13:397-405.
21. Klayman B.J., Volden P.A., Stewart P.S., Camper A.K. Escherichia coli O157:H7 requires colonizing partner to adhere and persist in a capillary flow cell. Environmental Science & Technology 2009, 43:2105-2111.
22. Koutsoumanis K., Sofos J.N. Microbial contamination. Encyclopedia of Meat Sciences 2004, 727-737. Elsevier Academic Press, Amsterdam, The Netherlands. W.K. Jensen (Ed.).
23. Kumar C.G., Anand S.K. Significance of microbial biofilms in food industry: a review. International Journal of Food Microbiology 1998, 42:9-27.
24. Leriche V., Carpentier B. Limitation of adhesion and growth of Listeria monocytogenes on stainless steel surfaces by Staphylococcus sciuri biofilms. Journal of Applied Microbiology 2000, 88:594-605.
25. Mafu A.A., Roy D., Goulet J., Magny P. Attachment of Listeria monocytogenes to stainless steel, glass, polypropylene, and rubber surfaces after short contact times. Journal of Food Protection 1990, 53:742-746.
26. Marouani-Gadri N., Augier G., Carpentier B. Characterization of bacterial strains isolated from a beef-processing plant following cleaning and disinfection - influence of isolated strains on biofilm formation by Sakaï and EDL 933 E. coli O157:H7. International Journal of Food Microbiology 2009, 133:62-67.
27. Noah C.W., Shaw C.I., Ikeda J.S., Kreuzer K.S., Sofos J.N. Development of green fluorescent protein-expressing bacterial strains and evaluation for potential use as positive controls in sample analyses. Journal of Food Protection 2005, 68:680-686.
28. Norwood D.E., Gilmour A. The differential adherence capabilities of two Listeria monocytogenes strains in monoculture and multispecies biofilms as a function of temperature. Letters in Applied Microbiology 2001, 33:320-324.
29. Palumbo S.A., Call J.E., Schultz F.J., Williams A.C. Minimum and maximum temperatures for growth and verotoxin production by hemorrhagic strains of Escherichia coli. Journal of Food Protection 1995, 58:352-356.
30. Pasmore M., Todd P., Pfiefer B., Rhodes M., Bowman C.N. Effect of polymer surface properties on the reversibility of attachment of Pseudomonas aeruginosa in the early stages of biofilm development. Biofouling 2002, 18:65-71.
31. 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.
32. Rivas L., Fegan N., Dykes G.A. Attachment of Shiga toxigenic Escherichia coli to stainless steel. International Journal of Food Microbiology 2007, 115:89-94.
33. Rivera-Betancourt M., Shackelford S.D., Arthur T.M., Westmoreland K.E., Bellinger G., Rossman M., Reagan J.O., Koohmaraie M. Prevalence of Escherichia coli O157:H7, Listeria monocytogenes, and Salmonella in two geographically distant commercial beef processing plants in the United States. Journal of Food Protection 2004, 67:295-302.
34. Rodriguez A., Autio W.R., McLandsborough L.A. Effect of surface roughness and stainless steel finish on Listeria monocytogenes attachment and biofilm formation. Journal of Food Protection 2008, 71:170-175.
35. Ryu J.-H., Kim H., Beuchat L.R. Attachment and biofilm formation by Escherichia coli O157:H7 on stainless steel as influenced by exopolysaccharide production, nutrient availability, and temperature. Journal of Food Protection 2004, 67:2123-2131.
36. Sasahara K.C., Zottola E.A. Biofilm formation by Listeria monocytogenes utilizes a primary colonizing microorganism in flowing systems. Journal of Food Protection 1993, 56:1022-1028.
37. Skandamis P.N., Stopforth J.D., Ashton L.V., Geornaras I., Kendall P.A., Sofos J.N. Escherichia coli O157:H7 survival, biofilm formation and acid tolerance under simulated slaughter plant moist and dry conditions. Food Microbiology 2009, 26:112-119.
38. Stoodley P., Sauer K., Davies D.G., Costerton J.W. Biofilms as complex differentiated communities. Annual Review of Microbiology 2002, 56:187-209.
39. Stopforth J.D., Samelis J., Sofos J.N., Kendall P.A., Smith G.C. Biofilm formation by acid-adapted and nonadapted Listeria monocytogenes in fresh beef decontamination washings and its subsequent inactivation with sanitizers. Journal of Food Protection 2002, 65:1717-1727.
40. Stopforth J.D., Samelis J., Sofos J.N., Kendall P.A., Smith G.C. Influence of extended acid stressing in fresh beef decontamination runoff fluids on sanitizer resistance of acid-adapted Escherichia coli O157:H7 in biofilms. Journal of Food Protection 2003, 66:2258-2266.
41. Stopforth J.D., Samelis J., Sofos J.N., Kendall P.A., Smith G.C. Influence of organic acid concentration on survival of Listeria monocytogenes and Escherichia coli O157:H7 in beef carcass wash water and on model equipment surfaces. Food Microbiology 2003, 20:651-660.
42. Tutenel A.V., Pierard D., Van Hoof J., De Zutter L. Molecular characterization of Escherichia coli O157 contamination routes in a cattle slaughterhouse. Journal of Food Protection 2003, 66:1564-1569.
43. Uhlich G.A., Cooke P.H., Solomon E.B. Analyses of the red-dry-rough phenotype of an Escherichia coli O157:H7 strain and its role in biofilm formation and resistance to antimicrobial agents. Applied and Environmental Microbiology 2006, 72:2564-2572.
44. Van Houdt R., Michiels C.W. Role of bacterial cell surface structures in Escherichia coli biofilm formation. Research in Microbiology 2005, 156:626-633.
45. Wijman J.G.E., de Leeuw P.P.L.A., Moezelaar R., Zwietering M.H., Abee T. Air-liquid interface biofilms of Bacillus cereus: formation, sporulation, and dispersion. Applied and Environmental Microbiology 2007, 73:1481-1488.