Potential of Escherichia coli O157:H7 to persist and form viable but non-culturable cells on a food-contact surface subjected to cycles of soiling and chemical treatment

International Journal of Food Microbiology

Volumn 144, Issue 1, 2010, Pages 96-103

  Marouani Gadri, Nesrine ^a   Firmesse, Olivier ^a   Chassaing, Danielle ^a   Sandris Nielsen, Dennis ^b   Arneborg, Nils ^b   Carpentier, Brigitte ^a  

^a Laboratoire de sécurité des aliments de Maisons Alfort   (France)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Cleaning and disinfection; E. coli O157:H7; EMA qPCR; FRIM; Persistence; Viable but non culturable

Indexed keywords

ETHIDIUM AZIDE; POLYURETHAN; REAGENT; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; BIOFILM; CELL SURVIVAL; CELL VIABILITY; CHEMICAL ANALYSIS; CLEANING; COLONY FORMING CELL; COMAMONAS TESTOSTERONI; DISINFECTION; ENVIRONMENT; ESCHERICHIA COLI O157; FOOD; FOOD CONTAMINATION; INCUBATION TIME; MEAT; NONHUMAN; PH; POLYMERASE CHAIN REACTION; SLAUGHTERHOUSE; SOILING;

BIOFILMS; COLONY COUNT, MICROBIAL; COMAMONAS TESTOSTERONI; DISINFECTANTS; DISINFECTION; EQUIPMENT CONTAMINATION; ESCHERICHIA COLI O157; FOOD MICROBIOLOGY; MEAT; MEAT-PACKING INDUSTRY; POLYVINYL CHLORIDE; TEMPERATURE; TIME FACTORS;

BACTERIA (MICROORGANISMS); COMAMONAS TESTOSTERONI; ESCHERICHIA COLI;

EID: 78149471512     PISSN: 01681605     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2010.09.002     Document Type: Article

References (45)

1. Ahmed S., Donaghy M. An outbreak of Escherichia coli O157:H7 in central Scotland. Escherichia coli O157:H7 and Other Shiga Toxin-Producing E. coli Strains 1998, American Society for Microbiology, Washington, D.C. J.B. Kaper, A.D. O'Brien (Eds.).
2. Asakura H., Igimi S., Kawamoto K., Yamamoto S., Makino S. Role of in vivo passage on the environmental adaptation of enterohemorrhagic Escherichia coli O157:H7: cross-induction of the viable but nonculturable state by osmotic and oxidative stresses. FEMS Microbiology Letters 2005, 253:243-249.
3. Asséré A., Oulahal N., Carpentier B. Comparative evaluation of methods for counting surviving biofilm cells adhering to a polyvinyl chloride surface exposed to chlorine or drying. Journal of Applied Microbiology 2008, 104:1692-1702.
4. Bagge-Ravn D., Ng Y., Hjelm M., Christiansen J.N., Johansen C., Gram L. The microbial ecology of processing equipment in different fish industries-analysis of the microflora during processing and following cleaning and disinfection. International Journal of Food Microbiology 2003, 87:239-250.
5. Banatvala N., Magnano A.R., Cartter M.L., Barrett T.J., Bibb W.F., Vasile L.L., Mshar P., Lambert-Fair M.A., Green J.H., Bean N.H., Tauxe R.V. Meat grinders and molecular epidemiology: two supermarket outbreaks of Escherichia coli O157:H7 infection. The Journal of Infectious Diseases 1996, 173:480-483.
6. Booth I.R. Regulation of cytoplasmic pH in bacteria. Microbiological Reviews 1985, 49:359-378.
7. Cawthorn D.M., Witthuhn R.C. Selective PCR detection of viable Enterobacter sakazakii cells utilizing propidium monoazide or ethidium bromide monoazide. Journal of Applied Microbiology 2008, 105:1178-1185.
8. Dunsmore D.G., Twomey A., Whittlestone W.G., Morgan H.W. Design and performance of systems for cleaning product-contact surfaces of food equipment: a review. Journal of Food Protection 1981, 44:220-240.
9. Frank J.F., Koffi R.A. Surface-adherent growth of Listeria monocytogenes is associated with increased resistance to surfactant sanitizers and heat. Journal of Food Protection 1990, 53:550-554.
10. Holah J.T., Taylor J.H., Dawson D.J., Hall K.E. Biocide use in the food industry and the disinfectant resistance of persistent strains of Listeria monocytogenes and Escherichia coli. Journal of Applied Microbiology 2002, 92(Suppl 1):111S-120S.
11. Hornbaek T., Brockhoff P.B., Siegumfeldt H., Budde B.B. Two subpopulations of Listeria monocytogenes occur at subinhibitory concentrations of leucocin 4010 and nisin. Applied and Environmental Microbiology 2006, 72:1631-1638.
12. Kolling G.L., Matthews K.R. Examination of recovery in vitro and in vivo of nonculturable Escherichia coli O157:H7. Applied and Environmental Microbiology 2001, 67:3928-3933.
13. Krysinski E., Brown L., Marchisello T. Effect of cleaners and sanitizers on Listeria monocytogenes attached to product contact surfaces. Journal of Food Protection 1992, 55:246-251.
14. Lechevallier M.W., Cawton C.D., Lee R.G. Factors promoting survival of bacteria in chlorinated water supplies. Applied and Environmental Microbiology 1988, 54:649-654.
15. Leriche V., Briandet R., Carpentier B. Ecology of mixed biofilms subjected daily to a chlorinated alkaline solution: spatial distribution of bacterial species suggests a protective effect of one species to another. Environmental Microbiology 2003, 5:64-71.
16. Makino S.I., Kii T., Asakura H., Shirahata T., Ikeda T., Takeshi K., Itoh K. Does enterohemorrhagic Escherichia coli O157:H7 enter the viable but nonculturable state in salted salmon roe?. Applied and Environmental Microbiology 2000, 66:5536-5539.
17. 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, 72:157-164.
18. Marouani-Gadri N., Chassaing D., Carpentier B. Comparative evaluation of biofilm formation and tolerance to a chemical shock of pathogenic and non-pathogenic Escherichia coli O157:H7 strains. Journal of Food Protection 2009, 72:157-164.
19. Maule A. Survival of verocytotoxigenic Escherichia coli O157 in soil, water and on surfaces. Symposium Series: Society for Applied Microbiology 2000, 71S-78S.
20. McKay A.M. Viable but non-culturable forms of potentially pathogenic bacteria in water. Letters in Applied Microbiology 1992, 14:129-135.
21. Mettler E., Carpentier B. Variations over time of microbial load and physicochemical properties of floor materials after cleaning in food industry premises. Journal of Food Protection 1998, 61:57-65.
22. Midelet G., Carpentier B. Transfer of microorganisms, including Listeria monocytogenes, from various materials to beef. Applied and Environmental Microbiology 2002, 68:4015-4024.
23. Mizunoe Y., Wai S.N., Takade A., Yoshida S. Restoration of culturability of starvation-stressed and low-temperature-stressed Escherichia coli O157 cells by using H2O2-degrading compounds. Archives of Microbiology 1999, 172:63-67.
24. Nataro J.P., Kaper J.B. Diarrheagenic Escherichia coli. Clinical Microbiology Reviews 1998, 11:142-201.
25. Nocker A., Camper A.K. Selective removal of DNA from dead cells of mixed bacterial communities by use of ethidium monoazide. Applied and Environmental Microbiology 2006, 72:1997-2004.
26. Nocker A., Cheung C.Y., Camper A.K. Comparison of propidium monoazide with ethidium monoazide for differentiation of live vs. dead bacteria by selective removal of DNA from dead cells. Journal of Microbiological Methods 2006, 67:310-320.
27. Nogva, H.K., Dromtorp, S.M., Nissen, H., Rudi, K. 2003. Ethidium monoazide for DNA-based differentiation of viable and dead bacteria by 5'-nuclease PCR. Biotechniques 34, 804-808, 810, 812-803.
28. Olsen K.N., Budde B.B., Siegumfeldt H., Rechinger K.B., Jakobsen M., Ingmer H. Noninvasive measurement of bacterial intracellular pH on a single-cell level with green fluorescent protein and fluorescence ratio imaging microscopy. Applied and Environmental Microbiology 2002, 68:4145-4147.
29. Padan E., Zilberstein D., Rottenberg H. The proton electrochemical gradient in Escherichia coli cells. European Journal of Biochemistry 1976, 63:533-541.
30. Penders J., Vink C., Driessen C., London N., Thijs C., Stobberingh E.E. Quantification of Bifidobacterium spp., Escherichia coli and Clostridium difficile in faecal samples of breast-fed and formula-fed infants by real-time PCR. FEMS Microbiology Letters 2005, 243:141-147.
31. Peneau S., Chassaing D., Carpentier B. First evidence of division and accumulation of viable but nonculturable Pseudomonas fluorescens cells on surfaces subjected to conditions encountered at meat processing premises. Applied and Environmental Microbiology 2007, 73:2839-2846.
32. Reissbrodt R., Rienaecker I., Romanova J.M., Freestone P.P., Haigh R.D., Lyte M., Tschape H., Williams P.H. Resuscitation of Salmonella enterica serovar typhimurium and enterohemorrhagic Escherichia coli from the viable but nonculturable state by heat-stable enterobacterial autoinducer. Applied and Environmental Microbiology 2002, 68:4788-4794.
33. Rigsbee W. Detection of the viable but non culturable state in Escherichia coli O157:H7. Journal of Food Safety 1997, 16:255-262.
34. 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.
35. Rudi K., Moen B., Dromtorp S.M., Holck A.L. Use of ethidium monoazide and PCR in combination for quantification of viable and dead cells in complex samples. Applied and Environmental Microbiology 2005, 71:1018-1024.
36. Siegumfeldt H., Bjorn Rechinger K., Jakobsen M. Dynamic changes of intracellular pH in individual lactic acid bacterium cells in response to a rapid drop in extracellular pH. Applied and Environmental Microbiology 2000, 66:2330-2335.
37. Tatchou-Nyamsi-Konig J.A., Moreau A., Federighi M., Block J.C. Behaviour of Campylobacter jejuni in experimentally contaminated bottled natural mineral water. Journal of Applied Microbiology 2007, 103:280-288.
38. Tilden J., Young W., McNamara A.M., Custer C., Boesel B., Lambert-Fair M.A., Majkowski J., Vugia D., Werner S.B., Hollingsworth J., Morris J.G. A new route of transmission for Escherichia coli: infection from dry fermented salami. American Journal of Public Health 1996, 86:1142-1145.
39. Tuttle J., Gomez T., Doyle M.P., Wells J.G., Zhao T., Tauxe R.V., Griffin P.M. Lessons from a large outbreak of Escherichia coli O157:H7 infections: insights into the infectious dose and method of widespread contamination of hamburger patties. Epidemiology and Infection 1999, 122:185-192.
40. Union European Directive 2000/54/EC of the European Parliament and of the Council of 18 September 2000 on the protection of workers from risks related to exposure to biological agents at work (seventh individual directive within the meaning of Article 16(1) of Directive 89/391/EEC). Official Journal of the European Union, L series 2000, 262:21-45.
41. Varma J.K., Greene K.D., Reller M.E., DeLong S.M., Trottier J., Nowicki S.F., DiOrio M., Koch E.M., Bannerman T.L., York S.T., Lambert-Fair M.-A., Wells J.G., Mead P.S. An outbreak of Escherichia coli O157 infection following exposure to a contaminated building. Journal of the American Medical Association 2003, 290:2709-2712.
42. Bilan des connaissances relatives aux Escherichia coli producteurs de Shiga-toxines (STEC) 2003, French Food Safety Agency, Maisons-Alfort (France), Available at http://www.afssa.fr/Documents/MIC-Ra-STEC.pdf. Accessed 5 February 2009. C. Vernozy-Rozand, S. Roze (Eds.).
43. Vernozy-Rozand C., Feng P., Montet M.P., Ray-Gueniot S., Villard L., Bavai C., Meyrand A., Mazuy C., Atrache V. Detection of Escherichia coli O157:H7 in heifers' faecal samples using an automated immunoconcentration system. Letters in Applied Microbiology 2000, 30:217-222.
44. Wang G., Zhao T., Doyle M. Fate of enterohemorrhagic Escherichia coli O157:H7 in bovine feces. Applied and Environmental Microbiology 1996, 62:2567-2570.
45. Wilks S.A., Michels H., Keevil C.W. The survival of Escherichia coli O157 on a range of metal surfaces. International Journal of Food Microbiology 2005, 105:445-454.