Quantifying variability on thermal resistance of Listeria monocytogenes

International Journal of Food Microbiology

Volumn 193, Issue , 2015, Pages 130-138

  Aryani, D C ^a,b   den Besten, H M W ^a,b   Hazeleger, W C ^b   Zwietering, M H ^a,b  

^a TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

D value; Heterogeneity; Modified Weibull model

Indexed keywords

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CONTROLLED STUDY; GROWTH CURVE; HEAT TOLERANCE; LISTERIA MONOCYTOGENES; LOW TEMPERATURE; NONHUMAN; REPRODUCTION; STRAIN DIFFERENCE; THERMAL ANALYSIS; FOOD CONTROL; GROWTH, DEVELOPMENT AND AGING; HEAT; MICROBIAL VIABILITY; PHYSIOLOGY; REPRODUCIBILITY; SPECIES DIFFERENCE; THEORETICAL MODEL;

LISTERIA MONOCYTOGENES;

FOOD MICROBIOLOGY; HOT TEMPERATURE; LISTERIA MONOCYTOGENES; MICROBIAL VIABILITY; MODELS, THEORETICAL; REPRODUCIBILITY OF RESULTS; SPECIES SPECIFICITY;

EID: 84910066638     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2014.10.021     Document Type: Article

References (40)

1. Álvarez-Ordóñez A., Fernández A., López M., Arenas R., Bernardo A. Modifications in membrane fatty acid composition of Salmonella Typhimurium in response to growth conditions and their effect on heat resistance. Int. J. Food Microbiol. 2008, 123:212-219.
2. Bajard S., Rosso L., Fardel G., Flandrois J.P. The particular behaviour of Listeria monocytogenes under sub-optimal conditions. Int. J. Food Microbiol. 1996, 29:201-211.
3. Bayles D.O., Tunick M.H., Foglia T.A., Miller A.J. Cold shock and its effect on ribosomes and thermal tolerance in Listeria monocytogenes. Appl. Environ. Microbiol. 2000, 66:4351-4355.
4. Benito A., Ventoura G., Casadei M., Robinson T., Mackey B. Variation in resistance of natural isolates of Escherichia coli O157 to high hydrostatic pressure, mild heat, and other stresses. Appl. Environ. Microbiol. 1999, 65:1564-1569.
5. Berendsen E.M., Zwietering M.H., Kuipers O.P., Wells-Bennik M.H.J. Two distinct groups within the Bacillus subtilis group display significantly different spore heat resistance properties. Food Microbiol. 2014, (in press). 10.1016/j.fm.2014.04.009.
6. Casadei M.A., Esteves de Matos R., Harrison S.T., Gaze J.E. Heat resistance of Listeria monocytogenes in dairy products as affected by the growth medium. J. Appl. Microbiol. 1998, 84:234-239.
7. Chen H., Hoover D.G. Modeling the combined effect of high hydrostatic pressure and mild heat on the inactivation kinetics of Listeria monocytogenes Scott A in whole milk. Innov. Food Sci. Emerg. Technol. 2003, 4:25-34.
8. Condon S., Garcia M.L., Otero A., Sala F.J. Effect of culture age, pre-incubation at low temperature and pH on the thermal resistance of Aeromonas hydrophila. J. Appl. Bacteriol. 1992, 72:322-326.
9. De Jesús A.J., Whiting R.C. Thermal inactivation, growth, and survival studies of Listeria monocytogenes strains belonging to three distinct genotypic lineages. J. Food Prot. 2003, 66:1611-1617.
10. 2. J. Gen. Microbiol. 1990, 136:2113-2118.
11. Den Besten H.M.W., Mataragas M., Moezelaar R., Abee T., Zwietering M.H. Quantification of the effects of salt stress and physiological state on thermotolerance of Bacillus cereus ATCC 10987 and ATCC 14579. Appl. Environ. Microbiol. 2006, 72:5884-5894.
12. Den Besten H.M.W., van der Mark E.-J., Hensen L., Abee T., Zwietering M.H. Quantification of the effect of culturing temperature on salt-induced heat resistance of Bacillus species. Appl. Environ. Microbiol. 2010, 76:4286-4292.
13. Doyle M.E., Mazzotta A.S., Wang T., Wiseman D.W., Scott V.N. Heat resistance of Listeria monocytogenes. J. Food Prot. 2001, 64:410-429.
14. Farber J.M., Pagotto F. The effect of acid shock on the heat resistance of Listeria monocytogenes. Lett. Appl. Microbiol. 1992, 15:197-201.
15. FDA Guidance for industry: recommendations to processors of apple juice or cider on the use of ozone for pathogen reduction purposes [online] Available at, (Accessed: 29 September 2014). http://www.fda.gov/Food/GuidanceRegulation/GuidanceDocumentsRegulatoryInformation/ucm072524.htm.
16. Gaze J.E., Brown G.D., Gaskell D.E., Banks J.G. Heat resistance of Listeria monocytogenes in homogenates of chicken, beef steak and carrot. Food Microbiol. 1989, 6:251-259.
17. Jørgensen F., Panaretou B., Stephens P.J., Knøchel S. Effect of pre- and post-heat shock temperature on the persistence of thermotolerance and heat shock-induced proteins in Listeria monocytogenes. J. Appl. Bacteriol. 1996, 80:216-224.
18. Kilstrup M., Jacobsen S., Hammer K., Vogensen F.K. Induction of heat shock proteins DnaK, GroEL, and GroES by salt stress in Lactococcus lactis. Appl. Environ. Microbiol. 1997, 63:1826-1837.
19. Leyer G.J., Johnson E.A. Acid adaptation induces cross-protection against environmental stresses in Salmonella Typhimurium. Appl. Environ. Microbiol. 1993, 59:1842-1847.
20. Lianou A., Koutsoumanis K.P. Evaluation of the strain variability of Salmonella enterica acid and heat resistance. Food Microbiol. 2013, 34:259-267.
21. Lou Y., Yousef A.E. Resistance of Listeria monocytogenes to heat after adaptation to environmental stresses. J. Food Prot. 1996, 59:465-471.
22. Luu-Thi H., Khadka D.B., Michiels C.W. Thermal inactivation parameters of spores from different phylogenetic groups of Bacillus cereus. Int. J. Food Microbiol. 2014, 189:183-188.
23. Mackey B.M., Pritchet C., Norris A., Mead G.C. Heat resistance of Listeria: strain differences and effects of meat type and curing salts. Lett. Appl. Microbiol. 1990, 10:251-255.
24. Martínez S., López M., Bernardo A. Thermal inactivation of Enterococcus faecium: effect of growth temperature and physiological state of microbial cells. Lett. Appl. Microbiol. 2003, 37:475-481.
25. Mazzotta A.S. Thermal inactivation of stationary-phase and acid-adapted Escherichia coli O157:H7, Salmonella, and Listeria monocytogenes in fruit juices. J. Food Prot. 2001, 64:315-320.
26. Metselaar K.I., den Besten H.M.W., Abee T., Moezelaar R., Zwietering M.H. Isolation and quantification of highly acid resistant variants of Listeria monocytogenes. Int. J. Food Microbiol. 2013, 166:508-514.
27. Meury J., Kohiyama M. Role of heat shock protein DnaK in osmotic adaptation of Escherichia coli. J. Bacteriol. 1991, 173:4404-4410.
28. Miller A.J., Bayles D.O., Eblen B.S. Cold shock induction of thermal sensitivity in Listeria monocytogenes. Appl. Environ. Microbiol. 2000, 66:4345-4350.
29. Ng H., Bayne H.G., Garibaldi J.A. Heat resistance of Salmonella: the uniqueness of Salmonella Senftenberg 775W. Appl. Microbiol. 1969, 17:78-82.
30. 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. J. Appl. Microbiol. 2006, 100:1054-1062.
31. Sörqvist S. Heat resistance of different serovars of Listeria monocytogenes. J. Appl. Bacteriol. 1994, 76:383-388.
32. Stephens P.J., Cole M.B., Jones M.V. Effect of heating rate on the thermal inactivation of Listeria monocytogenes. J. Appl. Bacteriol. 1994, 77:702-708.
33. Sumner S.S., Sandros T.M., Harmon M.C., Scott V.N., Bernard D.T. Heat resistance of Salmonella Typhimurium and Listeria monocytogenes in sucrose solutions of various water activities. J. Food Sci. 1991, 56:1741-1743.
34. Van Asselt E.D., Zwietering M.H. A systematic approach to determine global thermal inactivation parameters for various food pathogens. Int. J. Food Microbiol. 2006, 107:73-82.
35. Van Boeijen I.K.H., Francke C., Moezelaar R., Abee T., Zwietering M.H. Isolation of highly heat-resistant Listeria monocytogenes variants by use of a kinetic modeling-based sampling scheme. Appl. Environ. Microbiol. 2011, 77:2617-2624.
36. Van der Veen S., Hain T., Wouters J.A., Hossain H., de Vos W.M., Abee T., Chakraborty T., Wells-Bennik M.H.J. The heat-shock response of Listeria monocytogenes comprises genes involved in heat shock, cell division, cell wall synthesis, and the SOS response. Microbiology 2007, 153:3593-3607.
37. Van der Veen S., Moezelaar R., Abee T., Wells-Bennik M.H.J. The growth limits of a large number of Listeria monocytogenes strains at combinations of stresses show serotype- and niche-specific traits. J. Appl. Microbiol. 2008, 105:1246-1258.
38. Van Lieverloo J.H.M., de Roode M., Fox M.B., Zwietering M.H., Wells-Bennik M.H.J. Multiple regression model for thermal inactivation of Listeria monocytogenes in liquid food products. Food Control 2013, 29:394-400.
39. White H.R. The heat resistance of Streptococcus faecalis. J. Gen. Microbiol. 1953, 8:27-37.
40. Whiting R.C., Golden M.H. Variation among Escherichia coli O157:H7 strains relative to their growth, survival, thermal inactivation, and toxin production in broth. Int. J. Food Microbiol. 2002, 75:127-133.