Cross-protective effects of temperature, pH, and osmotic and starvation stresses in Escherichia coli O157:H7 subjected to pulsed electric fields in milk

International Dairy Journal

Volumn 21, Issue 12, 2011, Pages 953-962

  Rodríguez González, Oscar ^a   Walkling Ribeiro, Markus ^a   Jayaram, Shesha ^b   Griffiths, Mansel W ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF WATERLOO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL CELLS; COLD SHOCK; E.COLI O157:H7; EFFECTS OF TEMPERATURE; ESCHERICHIA COLI O157:H7; FIELD STRENGTHS; GOODNESS OF FIT; ONSET TEMPERATURE; OSMOTIC CONDITIONS; OSMOTIC STRESS; PULSED ELECTRIC FIELD; PULSED ELECTRIC FIELD TREATMENTS; STRESS RESPONSE; WEIBULL MODELS;

CELLS; ELECTRIC FIELDS; OSMOSIS; PH EFFECTS; SODIUM CHLORIDE; TEMPERATURE;

ESCHERICHIA COLI;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 80052883707     PISSN: 09586946     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.idairyj.2011.07.003     Document Type: Article

References (71)

1. Alvarez I., Mañas P., Condón S., Raso J. Resistance variation of Salmonella enterica serovars to pulsed electric fields treatments. Journal of Food Science 2003, 68:2316-2320.
2. Alvarez I., Pagán R., Condón S., Raso J. The influence of process parameters for the inactivation of Listeria monocytogenes by pulsed electric fields. International Journal of Food Microbiology 2003, 87:87-95.
3. Anderson I.C., Rhodes M., Kator H. Sublethal stress in Escherichia coli: a function of salinity. Applied and Environmental Microbiology 1979, 38:1147-1152.
4. Aronsson K., Borch E., Stenlöf B., Rönner U. Growth of pulsed electric field exposed Escherichia coli in relation to inactivation and environmental factors. International Journal of Food Microbiology 2004, 93:1-10.
5. Baranyi J., Roberts T.A., McClure P. A non-autonomous differential equation to model bacterial growth. Food Microbiology 1993, 10:43-59.
6. Baranyi J., Roberts T.A. A dynamic approach to predicting bacterial growth in food. International Journal of Food Microbiology 1994, 23:277-294.
7. Baranyi J., Roberts T.A. Mathematics of predictive food microbiology. International Journal of Food Microbiology 1995, 26:199-218.
8. Baranyi J., Pin C. Modelling the history effect on microbial growth and survival: deterministic and stochastic approaches. Modeling microbial responses in food 2004, 285-301. CRC Press, Boca Raton, FL, USA. R. McKellar, X. Lu (Eds.).
9. Bull M.K., Hayman M.M., Stewart C.M., Szabo E.A., Knabel S.J. Effect of prior growth temperature, type of enrichment medium, and temperature and time of storage on recovery of Listeria monocytogenes following high pressure processing of milk. International Journal of Food Microbiology 2005, 101:53-61.
10. Busch S.V., Donnelly C.W. Development of a repair-enrichment broth for resuscitation of heat-injured Listeria monocytogenes and Listeria innocua. Applied and Environmental Microbiology 1992, 58:14-20.
11. Campanella O.H., Peleg M. Theoretical comparison of a new and the traditional method to calculate Clostridium botulinum survival during thermal inactivation. Journal of the Science of Food and Agriculture 2001, 81:1069-1076.
12. Castro F.D., Tufenkji N. Relevance of nontoxigenic strains as surrogates for Escherichia coli O157:H7 in groundwater contamination potential: role of temperature and cell acclimation time. Environmental Science and Technology 2007, 41:4332-4338.
13. Cheville A.M., Arnold K.W., Buchrieser C., Cheng C.M., Kaspar C.W. rpoS regulation of acid, heat, and salt tolerance in Escherichia coli O157:H7. Applied and Environmental Microbiology 1996, 62:1822-1824.
14. Chung H.J., Bang W., Drake M.A. Stress response of Escherichia coli. Comprehensive Reviews in Food Science and Food Safety 2006, 5:52-64.
15. Corradini M.G., Peleg M. Dynamic model of heat inactivation kinetics for bacterial adaptation. Applied and Environmental Microbiology 2009, 75:2590-2597.
16. Couvert O., Gaillard S., Savy N., Mafart P., Leguerinel I. Survival curves of heated bacterial spores: effect of environmental factors on Weibull parameters. International Journal of Food Microbiology 2005, 101:73-81.
17. Dalgaard P., Ross T., Kamperman L., Neumeyer K., McMeekin T.A. Estimation of bacterial growth rates from turbidimetric and viable count data. International Journal of Food Microbiology 1994, 23:391-404.
18. Dalgaard P., Koutsoumanis K. Comparison of maximum specific growth rates and lag times estimated from absorbance and viable count data by different mathematical models. Journal of Microbiological Methods 2001, 43:183-196.
19. Desmond C., Stanton C., Fitzgerald G.F., Collins K., Ross R.P. Environmental adaptation of probiotic lactobacilli towards improvement of performance during spray drying. International Dairy Journal 2001, 11:801-808.
20. Faleiro M.L., Andrew P.W., Power D. Stress response of Listeria monocytogenes isolated from cheese and other foods. International Journal of Food Microbiology 2003, 84:207-216.
21. Fernández A., Salmerón C., Fernández P.S., Martínez A. Application of a frequency distribution model to describe the thermal inactivation of two strains of Bacillus cereus. Trends in Food Science and Technology 1999, 10:158-162.
22. García D., Gómez N., Raso J., Pagán R. Bacterial resistance after pulsed electric fields depending on the treatment medium pH. Innovative Food Science and Emerging Technologies 2005, 6:388-395.
23. García D., Mañas P., Gómez N., Raso J., Pagán R. Biosynthetic requirements for the repair of sublethal membrane damage in Escherichia coli cells after pulsed electric fields. Journal of Applied Microbiology 2006, 100:428-435.
24. Gawande P.V., Griffiths M.W. Growth history influences starvation-induced expression of uspA, grpE, and rpoS and subsequent cryotolerance in Escherichia coli O157:H7. Journal of Food Protection 2005, 68:1154-1158.
25. Gawande P.V., Griffiths M.W. Effects of environmental stresses on the activities of the uspA, grpE, and rpoS promoters of Escherichia coli O157:H7. International Journal of Food Microbiology 2005, 99:91-98.
26. Griffiths M.W. Predictive modelling: applications in the dairy industry. International Journal of Food Microbiology 1994, 23:305-315.
27. Guerrero-Beltrán J.A., Sepulveda D.R., Góngora-Nieto M.M., Swanson B., Barbosa-Cánovas G.V. Milk thermization by pulsed electric fields (PEF) and electrically induced heat. Journal of Food Engineering 2010, 100:56-60.
28. Hayman, M. (2007). Factors that influence barotolerance of Listeria monocytogenes and the mechanism of inactivation by high pressure processing. PhD thesis, State College, PA, USA: Pennsylvania State University.
29. Hayman M.M., Anantheswaran R.C., Knabel S.J. The effects of growth temperature and growth phase on the inactivation of Listeria monocytogenes in whole milk subject to high pressure processing. International Journal of Food Microbiology 2007, 115:230-236.
30. Hill C., Cotter P.D., Sleator R.D., Gahan C.G.M. Bacterial stress response in Listeria monocytogenes: jumping the hurdles imposed by minimal processing. International Dairy Journal 2002, 12:273-283.
31. Johnson E.A. Microbial adaptation and survival in foods. Microbial stress adaptation and food safety 2003, 75-103. CRC Press, Boca Raton, FL, USA. A.E. Yousef, V.K. Juneja (Eds.).
32. Juneja V.K., Klein P.G., Marmer B.S. Heat shock and thermotolerance of Escherichia coli O157:H7 in a model beef gravy system and ground beef. Journal of Applied Microbiology 1998, 84:677-684.
33. Juneja V.K., Novak J.S. Adaptation of foodborne pathogens to stress from exposure to physical intervention strategies. Microbial stress adaptation and food safety 2003, 31-53. CRC Press, Boca Raton, FL, USA. A.E. Yousef, V.K. Juneja (Eds.).
34. Juneja V.K., Valenzuela Melendres M., Huang L., Gumudavelli V., Subbiah J., Thippareddi H. Modeling the effect of temperature on growth of Salmonella in chicken. Food Microbiology 2007, 24:328-335.
35. Juneja V.K., Valenzuela Melendres M., Huang L., Subbiah J., Thippareddi H. Mathematical modeling of growth of Salmonella in raw ground beef under isothermal conditions from 10 to 45 °C. International Journal of Food Microbiology 2009, 131:106-111.
36. Kim W.S., Perl L., Park J.H., Tandianus J.E., Dunn N.W. Assessment of stress response of the probiotic Lactobacillus acidophilus. Current Microbiology 2001, 43:346-350.
37. Kumar M., Mora R., Kostrzynska M., Warriner K. Mode of Salmonella and Escherichia coli O157:H7 inactivation by a stabilized oxychloro-based sanitizer. Journal of Applied Microbiology 2006, 102:1427-1436.
38. Lado B., Yousef A.E. Characteristics of Listeria monocytogenes important to food processors. Listeria, listeriosis, and food safety 2007, 157-213. CRC Press, Boca Raton, FL, USA. 3rd ed. E.T. Ryser, E.H. Marth (Eds.).
39. Laird D.T., Gambrel-Lenarz S.A., Scher F.M., Graham T.E., Reddy R. Microbiological count methods. Standard methods for the examination of dairy products 2004, 153-186. American Public Health Association, Washington, DC, USA. 17th ed. H.M. Wehr, J.F. Frank (Eds.).
40. Leenanon B., Drake M.A. Acid stress, starvation, and cold stress after poststress behavior of Escherichia coli O157:H7 and nonpathogenic Escherichia coli. Journal of Food Protection 2001, 64:970-974.
41. López S., Prieto M., Dijkstra J., Dhanoa M.S., France J. Statistical evaluation of mathematical models for microbial growth. International Journal of Food Microbiology 2004, 96:289-300.
42. Lou Y., Yousef A.E. Resistance of Listeria monocytogenes to heat after adaptation to environmental stresses. Journal of Food Protection 1996, 59:465-471.
43. Mafart P., Couvert O., Gallard S., Leguerinei I. On calculating sterility in thermal preservation methods: application of the weibull frequency distribution model. International Journal of Food Microbiology 2002, 72:107-113.
44. McKellar R.C., Lu X. Primary models. Modeling microbial responses in food 2004, 21-62. CRC Press, Boca Raton, FL, USA. R.C. McKellar, X. Lu (Eds.).
45. Noci F., Walkling-Ribeiro M., Cronin D.A., Morgan D.J., Lyng J.G. Effect of thermosonication, pulsed electric field and their combination on inactivation of Listeria innocua in milk. International Dairy Journal 2009, 19:30-35.
46. Peleg M., Cole M.B. Estimating the survival of Clostridium botulinum spores during heat treatments. Journal of Food Protection 2000, 63:190-195.
47. Peleg M., Normand M.D. Calculating microbial survival parameters and predicting survival curves from non-isothermal inactivation data. Critical Reviews in Food Science and Nutrition 2004, 44:409-418.
48. Peleg M., Penchina C.M. Modeling microbial survival during exposure to a lethal agent with varying intensity. Critical Reviews in Food Science and Nutrition 2000, 40:159-172.
49. Pina-Pérez M.C., Rodrigo Aliaga D., Ferrer-Bernat C., Rodrigo Enguinados M., Martínez-López A. Inactivation of Enterobacter sakazakii by pulsed electric field in buffered peptone water and infant formula milk. International Dairy Journal 2007, 17:1441-1449.
50. Ravishankar S., Juneja V.K. Adaptation or resistance responses of microorganisms to stresses in the food processing environment. Microbial stress adaptation and food safety 2003, 105-158. CRC Press, Boca Raton, FL, USA. A.E. Yousef, V.K. Juneja (Eds.).
51. Rodrigo D., Barbosa-Cánovas G.V., Martínez A., Rodrigo M. Weibull distribution function based on an empirical mathematical model for inactivation of Escherichia coli by pulsed electric fields. Journal of Food Protection 2003, 66:1007-1012.
52. Rodríguez-Calleja J.M., Cebrián G., Condón S., Mañas P. Variation in resistance of natural isolates of Staphylococcus aureus to heat, pulsed electric field and ultrasound under pressure. Journal of Applied Microbiology 2006, 100:1054-1062.
53. Rodríguez-González O., Walkling-Ribeiro M., Jayaram S., Griffiths M.W. Factors affecting the inactivation of the natural microbiota of milk processed by pulsed electric fields and cross-flow microfiltration. Journal of Dairy Research 2011, 78:270-278.
54. Rodríguez-Romo L., Yousef A. Cross-protective effects of bacterial stress. Understanding pathogen behaviour: Virulence, stress response and resistance 2005, 128-151. CRC Press, Boca Raton, FL, USA. M.W. Griffiths (Ed.).
55. Rosso L., Lobry J.R., Bajard S., Flandrois J.P. Convenient model to describe the combined effects of temperature and pH on microbial growth. Applied and Environmental Microbiology 1995, 61:610-616.
56. Rowe M.T., Kirk R. An investigation into the phenomenon of cross-protection in Escherichia coli O157:H7. Food Microbiology 1999, 16:157-164.
57. Ryu J., Beuchat L.R. Influence of acid tolerance responses on survival, growth, and thermal cross-protection of Escherichia coli O157:H7 in acidified media and fruit juices. International Journal of Food Microbiology 1998, 45:185-193.
58. Sampedro F., Rodrigo M., Martínez A., Rodrigo D., Barbosa-Canovas G.V. Quality and safety aspects of PEF application in milk and milk products. Critical Reviews in Food Science and Nutrition 2005, 45:25-47.
59. Sampedro F., Rivas A., Rodrigo D., Martínez A., Rodrigo M. Effect of temperature and substrate on PEF inactivation of Lactobacillus plantarum in an orange juice-milk beverage. European Food Research and Technology 2006, 223:30-34.
60. Smith K., Mittal G.S., Griffiths M.W. Pasteurization of milk using pulsed electrical field and antimicrobials. Journal of Food Science 2002, 67:2304-2308.
61. Sobrino-López A., Martín-Belloso O. Review: potential of high-intensity pulsed electric field technology for milk processing. Food Engineering Reviews 2010, 2:17-27.
62. Sui Q., Roginski H., Williams R.P.W., Versteeg C., Wan J. Effect of pulsed electric field and thermal treatment on the physicochemical properties of lactoferrin with different iron saturation levels. International Dairy Journal 2010, 20:707-714.
63. Teo A.Y., Ziegler G.R., Knabel S.J. Optimizing detection of heat-injured Listeria monocytogenes in pasteurized milk. Journal of Food Protection 2001, 64:1000-1011.
64. Walkling-Ribeiro M., Noci F., Cronin D.A., Lyng J.G., Morgan D.J. Antimicrobial effect and shelf-life extension by combined thermal and pulsed electric field treatment of milk. Journal of Applied Microbiology 2009, 106:241-248.
65. Walkling-Ribeiro M., Rodríguez-González O., Jayaram S., Griffiths M.W. Microbial inactivation and shelf life comparison of 'cold' hurdle processing with pulsed electric fields and microfiltration, and conventional thermal pasteurisation in skim milk. International Journal of Food Microbiology 2011, 144:379-386.
66. Walkling-Ribeiro, M., Rodríguez-González, O., Jayaram, S. H., & Griffiths, M. W. Processing temperature, alcohol and carbonation levels and their impact on pulsed electric fields (PEF) mitigation of selected characteristic microorganisms in beer. Food Research International, in press. doi:10.1016/j.foodres.2011.01.046.
67. Wouters P.C., Bos A.P., Ueckert J. Membrane permeabilization in relation to inactivation kinetics of Lactobacillus species due to pulsed electric fields. Applied and Environmental Microbiology 2001, 67:3092-3101.
68. Zhang Q., Barbosa-Cánovas C.V., Swanson B.G. Engineering aspects of pulsed electric field pasteurization. Journal of Food Engineering 1995, 25:261-281.
69. Zhang Y., Griffiths M.W. Induced expression of the heat shock protein genes uspA and grpE during starvation at low temperatures and their influence on thermal resistance of Escherichia coli O157:H7. Journal of Food Protection 2003, 66:2045-2050.
70. Zimmerman U., Pilwat G., Riemann F. Dielectric breakdown in cell membranes. Biophysical Journal 1974, 14:881-889.
71. Zwietering M.H., De Koos J.T., Hasenack B.E., De Wit J.C., Van't Riet K. Modeling of bacterial growth as a function of temperature. Applied and Environmental Microbiology 1991, 57:1094-1101.