Individual and combined effects of pH and lactic acid concentration on Listeria innocua inactivation: Development of a predictive model and assessment of experimental variability

Applied and Environmental Microbiology

Volumn 73, Issue 5, 2007, Pages 1601-1611

  Janssen, M ^a   Geeraerd, A H ^a   Cappuyns, A ^a   Garcia Gonzalez, L ^a   Schockaert, G ^a   Van Houteghem, N ^b   Vereecken, K M ^a,d   Debevere, J ^b   Devlieghere, F ^b   Van Impe, J F ^a,c  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c Department of Chemical Engineering ^*  (Belgium)

^d Federal Agency for the Safety of the Food Chain   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCENCE MICROSCOPY; FOOD PRESERVATIVES; FOOD TECHNOLOGY; LACTIC ACID; PH EFFECTS;

INACTIVATION PROCESS; LISTERIA INNOCUA INACTIVATION; TAILING PHASE; TIME RANGE;

BACTERIA;

LACTIC ACID;

BACTERIUM; EXPERIMENTAL STUDY; GROWTH RESPONSE; MICROBIAL COMMUNITY; ORGANIC ACID; PH;

ARTICLE; BACTERIAL GROWTH; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; LISTERIA INNOCUA; MATHEMATICAL MODEL; NONHUMAN; PH; PREDICTION;

FOOD PRESERVATIVES; HYDROGEN-ION CONCENTRATION; INDUSTRIAL MICROBIOLOGY; LACTIC ACID; LISTERIA; MODELS, BIOLOGICAL;

LISTERIA INNOCUA;

EID: 33947207308     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.02198-06     Document Type: Article

References (50)

1. Abee, T., and J. A. Wouters. 1999. Microbial stress response in minimal processing. Int. J. Food Microbiol. 50:65-91.
2. Albert, I., and P. Mafart. 2005. A modified Weibull model for bacterial inactivation. Int. J. Food Microbiol. 100:197-211.
3. Anonymous. 2000. Kinetics of microbial inactivation for alternative food processing technologies-IFTs response to Task Order 1. US Food and Drug Administration: how to quantify the destruction kinetics of alternative processing technologies. J. Food Sci. 65(Suppl.):4-108.
4. Ben Amor, K., P. Breeuwer, P. Verbaarschot, F. M. Rombouts, A. D. L. Akkermans, W. M. De Vos, and T. Abee. 2002. Multiparamctric flow cytometry and cell sorting for the assessment of viable, injured, and dead bifidobacterium cells during bile salt stress. Appl. Environ. Microbiol. 68:5209-5216.
5. Bereksi, N., F. Gavini, T. Bénézech, and C. Faille. 2002. Growth, morphology and surface properties of Listeria monocytogenes Scott A and LO28 under saline and acid environments. J. Appl. Microbiol. 92:556-565.
6. Breeuwer, P., and T. Abee. 2000. Assessment of viability of microorganisms employing fluorescence techniques. Int. J. Food Microbiol. 55:193-200.
7. Breidt, F., Jr., J. S. Hayes, and R. F. McFeeters. 2004. Independent effects of acetic acid and pH on survival of Escherichia coli in simulated acidified pickle products. J. Food Prot. 67:12-18.
8. Brul, S., F. M. Klis, D. Knorr, T. Abee, and S. Notermans. 2003. Food preservation and the development of microbial resistance, p. 524-551. In P. Zeuthen and L. Bøgh-Sørensen (ed.), Food preservation techniques. CRC Press, Boca Raton, FL.
9. Buchanan, R. L., M. H. Golden, and R. C. Whiting. 1993. Differentiation of the effects of pH and lactic or acetic acid concentration on the kinetics of Listeria monocytogenes inactivation. J. Food Prot. 56:474-478, 484.
10. Cerf, O. 1977. Tailing of survival curves of bacteria! spores. J. Appl. Bacteriol. 42:1-19.
11. Cole, M. B., K. W. Davies, G. Munro, C. D. Holyoak, and D. C. Kilsby. 1993. A vitalistic model to describe the thermal inactivation of Listeria monocytogenes. J. Ind. Microbiol. 12:232-239.
12. Decker, E.-M. 2001. The ability of direct fluorescence-based, two-colour assays to detect different physiological states of oral streptococci. Lett. Appl. Microbiol. 33:188-192.
13. Geeraerd, A. H., C. H. Herremans, and J. F. Van Impe. 2000. Structural model requirements to describe microbial inactivation during a mild heat treatment. Int. J. Food Microbiol. 59:185-209.
14. Geeraerd, A. H., V. P. Valdramidis, and J. F. Van Impe. 2005. GlnaFiT, a freeware tool to assess non-loglinear microbial survivor curves. Int. J. Food Microbiol. 102:95-105.
15. Hazeleger, W. C., M. Dalvoorde, and R. R. Beumer. 2006. Fluorescence microscopy of NaCl-stressed, elongated Salmonella and Liberia cells reveals the presence of septa in filaments. Int. J. Food Microbiol. 112:288-290.
16. Hill, C., P. D. Cotter, R. D. Sleator, and C. G. M. Gahan. 2002. Bacterial stress response in Listeria monocytogenes: jumping the hurdles imposed by minimal processing. Int. Dairy J. 12:273-283.
17. Humpheson, L., M. R. Adams, W. A. Anderson, and M. B. Cole. 1998. Diphasic thermal inactivation kinetics in Salmonella enteritidis PT4. Appl. Environ. Microbiol. 64:459-464.
18. ICMSF. 1998. Microorganisms in foods 6. Microbial ecology of food commodities. Blackie Academic & Professional, London, United Kingdom.
19. Janssen, M., A. H. Geeraerd, F. Logist, Y. De Visscher, K. M. Vereecken, J. Debevere, F. Devlieghere, and J. F. Van Impe. 2006. Modelling Yersinia enterocolitica inactivation in coculture experiments with Lactobacillus sakei as based on pH and lactic acid profiles. Int. J. Food Microbiol. 111:59-72.
20. Kelly, A. F., and R. A. Patchett. 1996. Lactate and acetate production in Listeria innocua. Lett. Appl. Microbiol. 23:125-128.
21. Le Marc, Y., V. Huchet, C. M. Bourgeois, J. P. Guyonnet, P. Mafart, and D. Thuault. 2002. Modelling the growth kinetics of Listeria as a function of temperature, pH and organic acid concentration. Int. J. Food Microbiol. 73:219-237.
22. Leroy, F., K. Lievens, and L. De Vuyst. 2005. Interactions of meat-associated bacteriocin-producing lactobacilli with Listeria innocua under stringent sausage fermentation conditions. J. Food Prot. 68:2078-2084.
23. Lund, B. M., and T. Eklund. 2000. Control of pH and use of organic acids, p. 175-199. In B. M. Lund, T. C. Baird-Parker, and G. W. Gould (ed.). The microbiological safety and quality of food, vol. 1. Aspen Publishers, Inc., Gaithersburg, MD.
24. Mafart, P., O. Couvert, S. Gaillard, and I. Leguerinel. 2002. On calculating sterility in thermal preservation methods: application of the Weibull frequency distribution model. Int. J. Food Microbiol. 72:107-113.
25. McClure, P. J., C. de W. Blackburn, M. B. Cole, P. S. Curtis, J. E. Jones, J. D. Legan, I. D. Ogden, M. W. Peck, T. A. Roberts, J. P. Sutherland, and S. J. Walker. 1994. Modelling the growth, survival and death of microorganisms in foods: the UK Food Micromodel approach. Int. J. Food Microbiol. 23:265-275.
26. McMeekin, T. A., J. N. Olley, T. Ross, and D. A. Ratkowsky. 1993. Predictive microbiology: theory and application. John Wiley and Sons Inc., New York, NY.
27. McMeekin, T. A., and T. Ross. 1996. Shelf life prediction: status and future possibilities. Int. J. Food Microbiol. 33:65-83.
28. Neter, J., M. H. Kutner, C. J. Nachtsheim, and W. Wasserman. 1996. Applied linear statistical models. McGraw-Hill, Boston, MA.
29. Paulsen, P., and F. J. M. Smulders. 2003. Combining natural antimicrobial systems with other preservation techniques: the case of meat, p. 71-89. In P. Zeuthen and L. Bøgh-Sørensen (ed.), Food preservation techniques. CRC Press, Boca Raton, FL.
30. Peleg, M. 2000. Microbial survivor curves-the reality of flat "shoulders" and absolute thermal death times. Food Res. Int. 33:531-538.
31. Presser, K. A., D. A. Ratkowsky, and T. Ross. 1997. Modelling the growth rate of Escherichia coli as a function of pH and lactic acid concentration. Appl. Environ. Microbiol. 63:2355-2360.
32. Ratkowsky, D. A., T. Ross, T. A. McMeekin, and J. Olley. 1991. Comparison of Arrhenius-type and Bèlchrâdek-type models for prediction of bacterial growth in foods. J. Appl. Bacteriol. 71:452-459.
33. Ratkowsky, D. A. 2004. Model fitting and uncertainty, p. 151-196. In R. C. McKellar and X. Lu (ed.), Modeling microbial responses in food. CRC Press, Boca Raton, FL.
34. Ross, R. P., S. Morgan, and C. Hill. 2002. Preservation and fermentation: past, present and future. Int. J. Food Microbiol. 79:3-16.
35. Russell, J. B. 1992. Another explanation for the toxicity of fermentation acids at low pH: anion accumulation versus uncoupling. J. Appl. Bacteriol. 73:363-370.
36. Shabala, L., B. Budde, T. Ross, H. Siegumfeldt, and T. McMeekin. 2002. Responses of Listeria monocytogenes to acid stress and glucose availability monitored by measurements of intracellular pH and viable counts. Int. J. Food Microbiol. 75:89-97.
37. Shabala, L., T. McMeekin, B. B. Budde, and H. Siegumfeldt. 2006. Listeria innocua and Lactobacillus delbrueckii subsp. bulgaricus employ different strategies to cope with acid stress. Int. J. Food Microbiol. 110:1-7.
38. Shadbolt, C. T., T. Ross, and T. A. McMeekin. 1999. Nonthermal death of Escherichia coli. Int. J. Food Microbiol. 49:129-138.
39. Siegumfeldt, H., K. B. Rechinger, and M. Jakobsen. 2000. Dynamic changes of intracellular pH in individual lactic acid bacterium cells in response to a rapid drop in extracellular pH. Appl. Environ. Microbiol. 66:2330-2335.
40. Skandamis, P. N., and G.-J. E. Nychas. 2003. Modeling the microbial interaction and the death of Escherichia coli O157:H7 during the fermentation of Spanish-style green table olives. J. Food Prot. 66:1166-1175.
41. Stumbo, C. R. 1973. Thermobacteriology in food processing. Academic Press, Inc., Orlando, FL.
42. Thylin, I., P. Schuisky, S. Lindgren, and J. C. Gottschal. 1995. Influence of pH and lactic acid concentration on Clostridium tyrobutyricum during continuous growth in a pH-auxostat. J. Appl. Bacteriol. 79:663-670.
43. Van Impe, J. F., B. M. Nicolai, T. Martens, J. De Baerdemaeker, and J. Vandewalle. 1992. Dynamic mathematical model to predict microbial growth and inactivation during food processing. Appl. Environ. Microbiol. 58:2901-2909.
44. Van Impe, J. F., K. Bernaerts, A. H. Geeraerd, F. Poschet, and K. J. Versyck. 2001. Modelling and prediction in an uncertain environment, p. 156-179. In L. M. M. Tijskens, M. L. A. T. M. Hertog, and B. M. Nicolaï (ed.). Food process modelling. Woodhead Publishing Limited, Cambridge, United Kingdom.
45. Vereecken, K. M., M. Antwi, M. Janssen, A. Holvoet, F. Devlieghere, J. Debevere, and J. F. Van Impe. 2002. Biocontrol of microbial pathogens with lactic acid bacteria: evaluation through predictive modelling, p. 163-166. In Proceedings & Abstracts of the 18th International ICFMH Symposium, Matforsk. Norwegian Food Research Institute, Matforsk, Norway.
46. Vereecken, K. M., F. Devlieghere, A. Bockstaele, J. Debevere, and J. F. Van Impe. 2003. A model for lactic acid induced inhibition of Yersinia enterocolitica in mono- and coculture with Lactobacillus sakei. Food Microbiol. 20:701-713.
47. Virto, R., D. Sanz, I. Álvarez, S. Condon, and J. Raso. 2004. Relationship between inactivation kinetics of a Liberia monocytogenes suspension by chlorine and its chlorine demand. J. Appl. Microbiol. 97:1281-1288.
48. Virto, R., D. Sanz, I. Álvarez, S. Condon, and J. Raso. 2005. Inactivation kinetics of Yersinia enterocolitica by citric and lactic acid at different temperatures. Int. J. Food Microbiol. 103:251-257.
49. Zaika, L. L., and J. S. Fanelli. 2003. Growth kinetics and cell morphology of Listeria monocytogenes Scott A as affected by temperature, NaCl and EDTA. J. Food Prot. 66:1208-1215.
50. Zwietering, M. H., I. Jongenburger, F. M. Rombouts, and K. van't Riet. 1090. Modeling of the bacterial growth curve. Appl. Environ. Microbiol. 56:1875-1881.