Effect of the food matrix on pressure resistance of Shiga-toxin producing Escherichia coli

Food Microbiology

Volumn 57, Issue , 2016, Pages 96-102

  Li, Hui ^a   Garcia Hernandez, Rigoberto ^a   Driedger, Darcy ^b   McMullen, Lynn M ^a   Gänzle, Michael ^a,c  

^a UNIVERSITY OF ALBERTA   (Canada)

^b Food Processing Development Centre   (Canada)

^c HUBEI UNIVERSITY OF TECHNOLOGY   (China)

Author keywords

Escherichia coli; Food matrix; High pressure; Membrane; Shiga toxin producing E. coli (STEC)

Indexed keywords

FOOD PRESERVATIVE; YOGHURT;

ANIMAL; BACTERIAL COUNT; BOVINE; CHEMISTRY; DEVICES; DRUG EFFECTS; EVALUATION STUDY; FOOD PRESERVATION; GROWTH, DEVELOPMENT AND AGING; HYDROSTATIC PRESSURE; MEAT; MICROBIOLOGY; PROCEDURES; SHIGA TOXIN PRODUCING ESCHERICHIA COLI;

ANIMALS; CATTLE; COLONY COUNT, MICROBIAL; FOOD PRESERVATION; FOOD PRESERVATIVES; HYDROSTATIC PRESSURE; MEAT; SHIGA-TOXIGENIC ESCHERICHIA COLI; YOGURT;

EID: 84958245770     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2016.02.002     Document Type: Article

References (50)

1. Aertsen A., Spiegeleer P.D., Vanoirbeek K., Lavilla M., Michiels C.W. Induction of oxidative stress by high hydrostatic pressure in Escherichia coli. Appl. Microbiol. Biotechnol. 2005, 71:2226-2231.
2. Aertsen A., Vanoirbeek K., De Spiegeleer P., Sermon J., Hauben K., Farewell A., Nyström T., Michiels C.W. Heat shock protein-mediated resistance to high hydrostatic pressure in Escherichia coli. Appl. Environ. Microbiol. 2004, 70:2660-2666.
3. Alpas H., Kalchayanand N., Bozoglu F., Ray B. Interactions of high hydrostatic pressure, pressurization temperature and pH on death and injury of pressure-resistant and pressure-sensitive strains of foodborne pathogens. Int. J. Food Microbiol. 2000, 60:33-42.
4. Balasubramaniam V.M., Martinez-Monteagudo S.I., Gupta R. Principles and application of high pressure - based technologies in the food industry. Ann. Rev. Food Sci. Technol. 2015, 6. 19.1-19.28.
5. Carmel-Harel O., Storz G. Roles of the Glutathione- and Thioredoxin- Dependent Reduction Systems in the Escherichia coli and Saccharomyces cerevisiae Responses to Oxidative Stress 2000.
6. Casadei M.A., Manas P., Nilven G., Needs E., Mackey B.M. Role of membrane fluidity in pressure resistance of Escherichia coli NCTC 8164. Appl. Environ. Microbiol. 2002, 68:5965-5972.
7. Charoenwong D., Andrews S., Mackey B. Role of RpoS in the development of cell envelope resilience and pressure resistance in stationary-phase Escherichia coli. Appl. Environ. Microbiol. 2011, 77:5220-5229.
8. Choi S.H., Gu M.B. Phenolic toxicity e detection and classification through the use of a recombinant bioluminescent Escherichia coli. Environ. Toxicol. Chem. 2001, 20:248-255.
9. Cueva C., Moreno-Arribas M.V., Martín-Álvarez P.J., Bills G., Vicente M.F., Basilio A., Rivas C.L., Requena T., Rodríguez J.M., Bartolomé B. Antimicrobial activity of phenolic acids against commensal, probiotic and pathogenic bacteria. Res. Microbiol. 2010, 161:372-382.
10. Dlusskaya E., McMullen L.M., Gänzle M.G. Characterization of an extremely heat resistant Escherichia coli obtained from a beef processing facility. J. Appl. Microbiol. 2011, 110:840-849.
11. Feehily C., Karatzas K.A.G. Role of glutamate metabolism in bacterial responses towards acid and other stresses. J. Appl. Microbiol. 2012, 114:11-24.
12. Feyaerts J., Rogiers G., Corthouts J., Michiels C.W. Thiol-reactive natural antimicrobials and high pressure treatment synergistically enhance bacterial inactivation. Innov. Food Sci. Emerg. Technol. 2015, 27:26-34.
13. Foster J.W. Escherichia coli acid resistance: tales of an amateur acidophile. Nat. Rev. Microbiol. 2004, 2:898-907.
14. Frenzen P.D., Drake A., Angulo F.J. Ecomomic cost of illness due to Escherichia coli O157 infections in the United States. J. Food Prot. 2005, 68:2623-2630. the Emerging Infections Program Foodnet Working Group.
15. Gänzle M.G., Vogel R.F. On-line fluorescence determination of pressure mediated outer membrane damage in Escherichia coli. Syst. Appl. Microbiol. 2001, 24:477-485.
16. Gänzle M.G., Liu Y. Mechanisms of pressure-mediated cell death and injury in Escherichia coli: from fundamentals to food applications. Front. Food Microbiol. 2015, 6:599.
17. Garcia-Graells C., Hauben K.J.A., Michiels C.W. High-pressure inactivation and sublethal injury of pressure-resistant Escherichia coli mutants in fruit juices. Appl. Environ. Microbiol. 1998, 64:1566-1568.
18. Garcia-Hernandez R., McMullen L., Gänzle M.G. Development and validation of a surrogate strain cocktail to evaluate bactericidal effects of pressure on verotoxigenic Escherichia coli. Int. J. Food Microbiol. 2015, 205:16-22.
19. Gayán E., Condó S., Álvarez I., Nabakabaya M., Bernard M. Effect of pressure-induced changes in the ionization equilibria of buffers on inactivation of Escherichia coli and Staphylococcus aureus by high hydrostatic pressure. Appl. Environ. Microbiol. 2013, 79:4041-4047.
20. Georget E., Sevenich R., Reineke K., Mathys A., Heinz V., Callanan M., Rauh C., Knorr D. Inactivation of microorganisms by high isostatic pressure processing in complex matrices: a review. Innov. Food Sci. Emerg. Technol. 2015, 27:1-14.
21. Govers S.K., Dutré P., Aertsen A. In vivo disassembly and reassembly of protein aggregates in Escherichia coli. J. Bacteriol. 2014, 196:2325-2332.
22. Hauben K.J., Bartlett D.H., Soontjens C.C., Cornelis K., Wuytack E.Y., Michiels C.W. Escherichia coli mutants resistant to inactivation by high hydrostatic pressure. Appl. Environ. Microbiol. 1997, 63:945-950.
23. Hauben K.J.A., Bernaerts K., Michiels C.W. Protective effect of calcium on inactivation of Escherichia coli by high hydrostatic pressure. J. Appl. Microbiol. 1998, 85:678-684.
24. Helander I.M., Mattila-Sandholm T. Fluorometric assessment of Gram-negative bacterial permeabilization. J. Appl. Microbiol. 2000, 88:213-219.
25. Hofstetter S., Winter R., McMullen L.M., Gänzle M.G. In situ determination of membrane fluidity of Clostridium spp. during pressure-assisted thermal processing in combination with nisin or reutericyclin. Appl. Environ. Microbiol. 2013, 79:2103-2106.
26. Huffer S., Clark M.E., Ning J.C., Blanch H.W., Clark D.S. Role of alcohols in growth, lipid composition, and membrane fluidity of yeasts, bacteria, and archaea. Appl. Environ. Microbiol. 2011, 77:6400-6408.
27. Jordan S.L., Pascual C., Bracey E., Mackey B.M. Inactivation and injury of [U+2028]pressure-resistant strains of Escherichia coli O157 and Listeria monocytogenes in fruit juices. J. Appl. Microbiol. 2001, 91:463-469.
28. Karch H., Tarr P.I., Bielaszewaka M. Enterohaemorrhagic Escherichia coli in human medicine. Int. J. Med. Microbiol. 2005, 295:405-418.
29. Keweloh H., Diefenbach R., Rehm H. Increase of phenol tolerance of Escherichia coli by alternations of the fatty acid composition of the membrane lipids. Arch. Microbiol. 1991, 157:49-53.
30. Kilimann K.V., Hartmann C., Vogel R.F., Gänzle M.G. Differential inactivation of glucose- and glutamate-dependent acid resistance of Escherichia coli TMW 2.497 by high pressure treatments. Syst. Appl. Microbiol. 2005, 28:663-671.
31. Lavinas F.C., Miguel M.A.L., Lopes M.L.M., Valente-Mesquita V.L. Effect of high hydrostatic pressure on cashew apple (Anacardium occidentale L.) juice preservation. J. Food Sci. 2008, 73:273-277.
32. Liu Y., Betti M., Gänzle M.G. High pressure inactivation of Escherichia coli, Campylobacter jejuni, and spoilage microbiota on poultry meat. J. Food Prot. 2012, 75:497-503.
33. Liu Y., Gill A., McMullen L., Gänzle M.G. Variation in heat and pressure resistance of verotoxigenic and non-toxigenic Escherichia coli. J. Food Prot. 2015, 78:111-120.
34. Lu P., Ma D., Chen Y., Guo Y., Chen G., Deng H., Shi Y. L-Glutamine provides acid resistance for Escherichia coli through enzymatic release of ammonia. Cell Res. 2013, 23:635-644.
35. Malone A.S., Chuang Y.-K., Yousef A.E. Genes of Escherichia coli O157:H7 that are involved in high-pressure resistance. Appl. Environ. Microbiol. 2006, 72:2661-2671.
36. Mercer R.G., Zheng J., Garcia-Hernandez R., Ruan L., Gänzle M.G., McMullen L.M. Genetic determinants of heat resistance in Escherichia coli. Front. Microbiol. 2015, 6:932.
37. Molina-Gutierrez A., Stippl V., Delgado A., Gänzle M.G., Vogel R.F. In situ determination of the intracellular pH of Lactococcus lactis and Lactobacillus plantarum during pressure treatment. Appl. Environ. Microbiol. 2002, 68:4399-4406.
38. Niven G.W., Miles C.A., Mackey B.M. The effects of hydrostatic pressure on ribosome conformation in Escherichia coli: an in vivo study using differential scanning calorimetry. Microbiology 1999, 145:419-425.
39. Omana D.A., Plastow G., Betti M. Effect of different ingredients on color and oxidative characteristics of high pressure processed chicken breast meat with special emphasis on use of β-glucan as a partial salt replacer. Innov. Food Sci. Emerg. Technol. 2011, 12:244-254.
40. Pagán R., Jordan S., Benito A., Mackey B. Enhanced acid sensitivity of pressure-damaged Escherichia coli O157 cells. Appl. Environ. Microbiol. 2001, 67:1983-1985.
41. Patterson M.F., Quinn M., Simpson R., Gilmour A. Sensitivity of vegetative pathogens to high hydrostatic pressure treatment in phosphate-buffered saline and foods. J. Food Prot. 1995, 58:524-529.
42. Reineke K., Sevenich R., Hertwig C., JanBen T., Fröhling A., Knorr D., Wieler L.H., Schlüter O. Comparative study on the high pressure inactivation behavior of the Shiga toxin-producing Escherichia coli O104:H4 and O157:H7 outbreak strains and a non-pathogenic surrogate. Food Microbiol. 2015, 46:184-194.
43. Ritz M., Feulet M., Orange N., Federighi M. Effects of high hydrostatic pressure [U+2028]on membrane proteins of Salmonella typhimurium. Int. J. Food Microbiol. 2000, 55:115-119.
44. Sánchez-Maldonado A.F., Schieber A., Gänzle M.G. Structure-function relationships of the antibacterial activity of phenolic acids and their metabolism by lactic acid bacteria. J. Appl. Microbiol. 2011, 111:1176-1184.
45. Tassou C.C., Panagou E.Z., Samaras F.J., Galiatsatou P., Mallidis C.G. Temperature-assisted high hydrostatic pressure inactivation of Staphylococcus aureus in a ham model system: evaluation in selective and nonselective medium. J. Appl. Microbiol. 2008, 104:1764-1773.
46. Teixeira J.S., Seeras A., Sanchez-Maldonado A.F., Zhang C., Su M.S., Gänzle M.G. Glutamine, glutamate, and arginine-based acid resistance in Lactobacillus reuteri. Food Microbiol. 2014, 42:172-180.
47. Ulmer H.M., Herberhold H., Fahsel S., Gänzle M.G., Winter R., Vogel R.F. Effects of pressure induced membrane phase transitions on HorA inactivation in Lactobacillus plantarum. Appl. Environ. Microbiol. 2002, 68:1088-1095.
48. Welch T.J., Bartlett D.H. Identification of a regulatory protein required for pressure-responsive gene expression in the deep-sea bacterium Photobacterium species strain SS9. Mol. Microbiol. 1998, 27:977-985.
49. Winter R. Synchrotron X-ray and neutron small-angle scattering of lyotropic lipid mesophases, model biomembranes and proteins in solution at high pressure. Biochim. Biophys. Acta 2002, 1595:160-184.
50. Wouters P.C., Glaasker E., Smelt J.P.P.M. Effects of high pressure on inactivation kinetics and events related to proton efflux in Lactobacillus plantarum. Appl. Environ. Microbiol. 1998, 64:509-514.