Thermal inactivation and sublethal injury kinetics of Salmonella enterica and Listeria monocytogenes in broth versus agar surface

International Journal of Food Microbiology

Volumn 243, Issue , 2017, Pages 70-77

  Wang, Xiang ^a   Devlieghere, Frank ^a   Geeraerd, Annemie ^b   Uyttendaele, Mieke ^a  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

D value; Heat resistance; Meta analysis; Model agar system; Surface pasteurization

Indexed keywords

AGAR;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CELL DAMAGE; CELL MEMBRANE; COMPARATIVE STUDY; CONTROLLED STUDY; HEAT TOLERANCE; LISTERIA MONOCYTOGENES; NONHUMAN; SALMONELLA ENTERICA; SURFACE PROPERTY; TEMPERATURE; TEMPERATURE SENSITIVITY; BACTERIAL COUNT; FOOD CONTROL; GROWTH, DEVELOPMENT AND AGING; HEAT; HEATING; KINETICS; MICROBIAL VIABILITY; PROCEDURES;

AGAR; COLONY COUNT, MICROBIAL; FOOD MICROBIOLOGY; HEATING; HOT TEMPERATURE; KINETICS; LISTERIA MONOCYTOGENES; MICROBIAL VIABILITY; SALMONELLA ENTERICA;

EID: 85006792242     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2016.12.008     Document Type: Article

References (64)

1. Adams, M., Detecting Sublethally Damaged Cells. Understanding Pathogen Behaviour. 2005, Woodhead Publishing Limited, Cambridge, England, 199–212.
2. Aguirre, J., Pin, C., Rodríguez, M., de Fernando, G.G., Analysis of the variability in the number of viable bacteria after mild heat treatment of food. Appl. Environ. Microbiol. 75 (2009), 6992–6997.
3. Aljarallah, K.M., Adams, M.R., Mechanisms of heat inactivation in Salmonella serotype typhimurium as affected by low water activity at different temperatures. J. Appl. Microbiol. 102 (2007), 153–160.
4. 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. 123 (2008), 212–219.
5. Ariefdjohan, M.W., Nelson, P.E., Singh, R.K., Bhunia, A.K., Balasubramaniam, V.M., Singh, N., Efficacy of high hydrostatic pressure treatment in reducing Escherichia coli O157 and Listeria monocytogenes in alfalfa seeds. J. Food Sci. 69 (2004), M117–M120.
6. Arroyo, C., Condon, S., Pagan, R., Thermobacteriological characterization of Enterobacter sakazakii. Int. J. Food Microbiol. 136 (2009), 110–118.
7. Aryani, D.C., den Besten, H.M.W., Hazeleger, W.C., Zwietering, M.H., Quantifying variability on thermal resistance of Listeria monocytogenes. Int. J. Food Microbiol. 193 (2015), 130–138.
8. Baird-Parker, T.C., Gould, G.W., Lund, B.M., The Microbiological Safety and Quality of Food. 2000, Aspen Publishers, Inc, Gaithersburg, Maryland.
9. Balasubramaniam, V., Ting, E., Stewart, C., Robbins, J., Recommended laboratory practices for conducting high-pressure microbial inactivation experiments. Innovative Food Sci. Emerg. Technol. 5 (2004), 299–306.
10. Bermúdez-Aguirre, D., Corradini, M.G., Inactivation kinetics of Salmonella spp. under thermal and emerging treatments: a review. Food Res. Int. 45 (2012), 700–712.
11. Besse, N.G., Influence of various environmental parameters and of detection procedures on the recovery of stressed L. monocytogenes: a review. Food Microbiol. 19 (2002), 221–234.
12. Brocklehurst, T., Mitchell, G., Smith, A., A model experimental gel-surface for the growth of bacteria on foods. Food Microbiol. 14 (1997), 303–311.
13. Buchanan, R.L., Golden, M.H., Whiting, R.C., Differentiation of the effects of pH and lactic or acetic-acid concentration on the kinetics of Listeria monocytogenes inactivation. J. Food Prot. 56 (1993), 474–478.
14. Casadei, M.A., Ingram, R., Hitchings, E., Archer, J., Gaze, J.E., Heat resistance of Bacillus cereus, Salmonella typhimurium and Lactobacillus delbrueckii in relation to pH and ethanol. Int. J. Food Microbiol. 63 (2001), 125–134.
15. Chiruta, J., Davey, K.R., Thomas, C.J., Thermal inactivation kinetics of three vegetative bacteria as influenced by combined temperature and pH in a liquid medium. Food Bioprod. Process. 75 (1997), 174–180.
16. den Besten, H.M.W., Aryani, D.C., Metselaar, K.I., Zwietering, M.H., Microbial variability in growth and heat resistance of a pathogen and a spoiler: All variabilities are equal but some are more equal than others. Int. J. Food Microbiol. 240 (2017), 24–31.
17. Devlieghere, F., Vermeiren, L., Debevere, J., New preservation technologies: possibilities and limitations. Int. Dairy J. 14 (2004), 273–285.
18. Doyle, M.E., Mazzotta, A.S., Review of studies on the thermal resistance of Salmonellae. J. Food Prot. 63 (2000), 779–795.
19. Doyle, M.E., Mazzotta, A.S., Wang, T., Wiseman, D.W., Scott, V.N., Heat resistance of Listeria monocytogenes. J. Food Prot. 64 (2001), 410–429.
20. Dykes, G.A., Physical and metabolic causes of sub-lethal damage in Listeria monocytogenes after long-term chilled storage at 4 °C. Int. J. Food Microbiol. 87 (1999), 915–922.
21. EFSA (European Food Safety Authority), ECDC (European Centre for Disease Prevention and Control), The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2014. EFSA J., 13(12), 2015, 4329 (2015).
22. Fujikawa, H., Morozumi, S., Modeling surface growth of Escherichia coli on agar plates. Appl. Environ. Microbiol. 71 (2005), 7920–7926.
23. Geeraerd, A.H., Herremans, C.H., Van Impe, J.F., Structural model requirements to describe microbial inactivation during a mild heat treatment. Int. J. Food Microbiol. 59 (2000), 185–209.
24. Geeraerd, A.H., Valdramidis, V.P., Van Impe, J.F., GInaFiT, a freeware tool to assess non-log-linear microbial survivor curves. Int. J. Food Microbiol. 102 (2005), 95–105.
25. Geeraerd, A.H., Valdramidis, V.P., Van Impe, J.F., Erratum to “GInaFiT, a freeware tool to assess non-log-linear microbial survivor curves”. Int. J. Food Microbiol. 102:2005 (2006), 95–105 (Int. J. Food Microbiol. 110, 297).
26. Harris, L.J., Farber, J.N., Beuchat, L.R., Parish, M.E., Suslow, T.V., Garrett, E.H., Busta, F.F., Outbreaks associated with fresh produce: incidence, growth, and survival of pathogens in fresh and fresh-cut produce. Compr. Rev. Food Sci. Food Saf. 2 (2003), 78–141.
27. Hornstra, L.M., Ter Beek, A., Smelt, J.P., Kallemeijn, W.W., Brul, S., On the origin of heterogeneity in (preservation) resistance of Bacillus spores: input for a ‘systems’ analysis approach of bacterial spore outgrowth. Int. J. Food Microbiol. 134 (2009), 9–15.
28. Huang, L., Thermal resistance of Listeria monocytogenes, Salmonella Heidelberg, and Escherichia coli O157:H7 at elevated temperatures. J. Food Prot. 67 (2004), 1666–1670.
29. Humpeson, L., Adams, M.R., Anderson, W.A., Cole, M.B., Biphasic thermal inactivation kinetics in Salmonella enteritidis PT4. Appl. Environ. Microbiol. 64 (1998), 459–464.
30. Jasson, V., Uyttendaele, M., Rajkovic, A., Debevere, J., Establishment of procedures provoking sub-lethal injury of Listeria monocytogenes, Campylobacter jejuni and Escherichia coli O157 to serve method performance testing. Int. J. Food Microbiol. 118 (2007), 241–249.
31. Jasson, V., Baert, L., Uyttendaele, M., Detection of low numbers of healthy and sub-lethally injured Salmonella enterica in chocolate. Int. J. Food Microbiol. 145 (2011), 488–491.
32. Jemmi, T., Stephan, R., Listeria monocytogenes: food-borne pathogen and hygiene indicator. Rev. Off. Int. Epizoot. 25 (2006), 571–580.
33. Juneja, V.K., Extrinsic and intrinsic factors that influence microbial heat resistance. Bull. Int. Dairy Fed. No 392/2004, 2004, 16–30.
34. Juneja, V.K., Eblen, B., Ransom, G., Thermal inactivation of Salmonella spp. in chicken broth, beef, pork, turkey, and chicken: determination of D-and Z-values. J. Food Sci. 66 (2001), 146–152.
35. Juneja, V.K., Huang, L., Marks, H., Approaches for Modeling Thermal Inactivation of Food Borne Pathogens, ACS symposium series. 2006, Oxford University Press, 235–251.
36. Juneja, V.K., Mukhopadhyay, S., Marks, H., Mohr, T.B., Warning, A., Datta, A., Predictive thermal inactivation model for effects and interactions of temperature, NaCl, sodium pyrophosphate, and sodium lactate on Listeria monocytogenes in ground beef. Food Bioproc. Tech. 7 (2014), 437–446.
37. w when grown in suspension or on a solid surface. Food Microbiol. 21 (2004), 415–422.
38. Lianou, A., Koutsoumanis, K.P., Evaluation of the strain variability of Salmonella enterica acid and heat resistance. Food Microbiol. 34 (2013), 259–267.
39. McCann, M.S., McGovern, A.C., McDowell, D.A., Blair, I.S., Sheridan, J.J., Effects of storage and the presence of a beef microflora on the thermal resistance of Salmonella typhimurium DT104 in beef and broth systems. Int. J. Food Microbiol. 102 (2007), 1561–1569.
40. McKellar, R., Butler, G., Stanich, K., Modelling the influence of temperature on the recovery of Listeria monocytogenes from heat injury. Food Microbiol. 14 (1997), 617–626.
41. Metselaar, K.I., den Besten, H.M., Abee, T., Moezelaar, R., Zwietering, M.H., Isolation and quantification of highly acid resistant variants of Listeria monocytogenes. Int. J. Food Microbiol. 166 (2013), 508–514.
42. Miller, A.J., Bayles, D.O., Eblen, B.S., Cold shock induction of thermal sensitivity in Listeria monocytogenes. Appl. Environ. Microbiol. 66 (2000), 4345–4350.
43. Miller, F.A., Brandao, T.R.S., Teixeira, P., Silva, C.L.M., Recovery of heat-injured Listeria innocua. Int. J. Food Microbiol. 112 (2006), 261–265.
44. Miller, F.A., Gil, M.M., Brandao, T.R.S., Teixeira, P., Silva, C.L.M., Sigmoidal thermal inactivation kinetics of Listeria innocua in broth: Influence of strain and growth phase. Food Control 20 (2009), 1151–1157.
45. Miller, F.A., Ramos, B., Brandao, T.R.S., Teixeira, P., Silva, C.L.M., Comparison of recovery methods for the enumeration of injured Listeria innocua cells under isothermal and non-isothermal treatments. Food Microbiol. 27 (2010), 1112–1120.
46. Moats, W.A., Dabbah, R., Edwards, V.M., Interpretation of nonlogarithmic survivor curves of heated bacteria. J. Food Sci. 36 (1971), 523–526.
47. Murphy, R.Y., Marks, B.P., Johnson, E.R., Johnson, M.G., Inactivation of Salmonella and Listeria in ground chicken breast meat during thermal processing. J. Food Prot. 62 (1999), 980–985.
48. Murphy, R.Y., Marks, B.P., Johnson, E.R., Johnson, M.G., Thermal inactivation kinetics of Salmonella and Listeria in ground chicken breast meat and liquid medium. J. Food Sci. 65 (2000), 706–710.
49. Ng, H., Bayne, H.G., Garibaldi, J.A., Heat resistance of Salmonella: the uniqueness of Salmonella Senftenberg 775W. Appl. Microbiol. 17 (1969), 78–82.
50. Noriega, E., Velliou, E., Van Derlinden, E., Mertens, L., Van Impe, J.F.M., Effect of cell immobilization on heat-induced sublethal injury of Escherichia coli, Salmonella typhimurium and Listeria innocua. Food Microbiol. 36 (2013), 355–364.
51. Rajkowski, K.T., Thermal inactivation of Escherichia coli O157:H7 and Salmonella on catfish and tilapia. Food Microbiol. 30 (2012), 427–431.
52. Rawson, A., Patras, A., Tiwari, B.K., Noci, F., Koutchma, T., Brunton, N., Effect of thermal and non thermal processing technologies on the bioactive content of exotic fruits and their products: Review of recent advances. Food Res. Int. 44 (2011), 1875–1887.
53. Rose, B.E., Hill, W.E., Umholtz, R., Ransom, G.M., James, W.O., Testing for Salmonella in raw meat and poultry products collected at federally inspected establishments in the United States, 1998 through 2000. J. Food Prot. 65 (2002), 937–947.
54. Silva, A., Genovés, S., Martorell, P., Zanini, S.F., Rodrigo, D., Martinez, A., Sublethal injury and virulence changes in Listeria monocytogenes and Listeria innocua treated with antimicrobials carvacrol and citral. Food Microbiol. 50 (2015), 5–11.
55. Skandamis, P.N., Yoon, Y., Stopforth, J.D., Kendall, P.A., Sofos, J.N., Heat and acid tolerance of Listeria monocytogenes after exposure to single and multiple sublethal stresses. Food Microbiol. 25 (2008), 294–303.
56. Smith, J.L., Archer, D.L., Heat-induced injury in Listeria monocytogenes. J. Ind. Microbiol. 3 (1988), 105–110.
57. Sorqvist, S., Heat resistance in liquids of Enterococcus spp., Listeria spp., Escherichia coli, Yersinia enterocolitica, Salmonella spp. and Campylobacter spp. Acta Vet. Scand. 44 (2003), 1–19.
58. Stopforth, J.D., Suhalim, R., Kottapalli, B., Hill, W.E., Samadpour, M., Thermal inactivation D- and z-values of multidrug-resistant and non-multidrug-resistant Salmonella serotypes and survival in ground beef exposed to consumer-style cooking. J. Food Prot. 71 (2008), 509–515.
59. Stringer, S.C., George, S.M., Peck, M.W., Thermal inactivation of Escherichia coli O157:H7. Symp. Ser. (Soc. Appl. Microbiol.) 88 (2000), 79S–89S.
60. 2 on the resuscitation of Listeria monocytogenes injured by various bactericidal treatments. Int. J. Food Microbiol. 123 (2008), 67–73.
61. Walsh, C., Duffy, G., Sheridan, J., Fanning, S., Blair, I., McDowell, D., Thermal resistance of antibiotic-resistant and antibiotic-sensitive Salmonella spp. on chicken meat. J. Food Saf. 25 (2005), 288–302.
62. Wu, V.C.H., A review of microbial injury and recovery methods in food. Food Microbiol. 25 (2008), 735–744.
63. Xavier, I.J., Ingham, S.C., Increased D-values for Salmonella enteritidis following heat shock. J. Food Prot. 60 (1997), 181–184.
64. Zwietering, M., Cuppers, H., De Wit, J., Van't Riet, K., Evaluation of data transformations and validation of a model for the effect of temperature on bacterial growth. Appl. Environ. Microbiol. 60 (1994), 195–203.