Predictive Modeling for the Growth of Listeria monocytogenes as a Function of Temperature, NaCl, and pH

  • PARK SHIN YOUNG (Department of Food Science and Technology, Chung-Ang University) ;
  • CHOI JIN-WON (Department of Food Science and Technology, Chung-Ang University) ;
  • YEON JIHYE (Department of Food Science and Technology, Chung-Ang University) ;
  • LEE MIN JEONG (Department of Food Science and Technology, Chung-Ang University) ;
  • CHUNG DUCK HWA (Division of Applied Life Science, Gyeongsang National University) ;
  • KIM MIN-GON (Laboratory of Integrative Biotechnology, Korea Research Institute of Bioscience and Biotechnology) ;
  • LEE KYU-HO (Department of Environmental Engineering and Biotechnology, Hankuk University of Foreign Studies) ;
  • KIM KEUN-SUNG (Department of Food Science and Technology, Chung-Ang University) ;
  • LEE DONG-HA (Korea Food and Drug Administration) ;
  • BAHK GYUNG-JIN (Korea Health Industry Development Institute) ;
  • BAE DONG-HO (Department of Applied Biology & Chemistry, Konkuk University) ;
  • KIM KWANG-YUP (Department of Food Science and Technology, Chungbuk University) ;
  • KIM CHEOL-HO (Department of Biochemistry and Molecular Biology, College of Oriental Medicine, Dongguk University)
  • Published : 2005.12.01

Abstract

A mathematical model was developed for predicting the growth kinetics of Listeria monocytogenes in tryptic soy broth (TSB) as a function of combined effects of temperature, pH, and NaCl. The TSB containing four different concentrations of NaCl (2, 4, 5, and $10\%$) was initially adjusted to six different pH levels (pH 5, 6, 7, 8, 9, and 10) and incubated at 4, 10, 25, or 37$^{circ}C$. In all experimental variables, the primary growth curves were well fitted ($r^{2}$=0.982 to 0.998) to a Gompertz equation to obtain the lag time (LT) and specific growth rate (SGR). Surface response models were identified as appropriate secondary models for LT and SGR on the basis of coefficient determination ($r^{2}$=0.907 for LT, 0.964 for SGR), mean square error (MSE=3.389 for LT, 0.018 for SGR), bias factor ($B_{1}$B,=0.706 for LT, 0.836 for SGR), and accuracy factor ($A_{f}$=1.567 for LT, 1.213 for SGR). Therefore, the developed secondary model proved reliable predictions of the combined effect of temperature, NaCl, and pH on both LT and SGR for L. monocytogenes in TSB.

Keywords

References

  1. Adair, C., D. C. Kilsby, and P. T. Whittall. 1989. Comparison of the Schoolfield (non-linear Arrhenius) model and the square root model for predicting bacterial growth in foods. Food Microbiol. 6: 7-18 https://doi.org/10.1016/S0740-0020(89)80033-4
  2. Ahn, C., C. H. Kim, H. K. Shin, Y. M. Lee, Y. S. Lee, and G. E. Ji. 2003. Antibiosis of pediocin-producing Pediococcus sp. KCA1303-10 against Listeria monocytogenes in mixed cultures. J. Microbiol. Biotechnol. 13: 429-436
  3. Bhaduri, S., C. Turner-Jones, R. L. Buchanan, and J. G. Phillips. 1994. Response surface models of the effect of pH, sodium chloride and sodium nitrite on growth of Yersinia enterocolitica at low temperatures. Int. J. Food Microbiol. 23: 333-343 https://doi.org/10.1016/0168-1605(94)90161-9
  4. Buchanan, R. L., L. K. Bagi, R. V. Goins, and J. G. Phillips. 1993. Response surface model for the growth kinetics of Escherichia coli O157:H7. Food Microbiol. 10: 303-315 https://doi.org/10.1006/fmic.1993.1035
  5. 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 https://doi.org/10.4315/0362-028X-56.6.474
  6. Buchanan, R. L. and J. G. Phillips. 1990. Response surface model for predicting the effects of temperature, pH, sodium chloride content, sodium nitrite concentration and atmosphere on the growth of Listeria monocytogenes. J. Food Prot. 53: 370-376 https://doi.org/10.4315/0362-028X-53.5.370
  7. Buchanan, R. L., H. G. Stahl, and R. C. Whiting. 1989. Effects and interactions of temperature, pH, atmosphere, sodium chloride, and sodium nitrite on the growth of Listeria monocytogenes. J. Food Prot. 52: 844-851 https://doi.org/10.4315/0362-028X-52.12.844
  8. Cheroutre-Vialette, M., I. Lebert, M. Hebraud, J. C. Labadie, and A. Lebert. 1998. Effects of pH or a(w) stress on growth of Listeria monocytogenes. Int. J. Food Microbiol. 42: 71- 77 https://doi.org/10.1016/S0168-1605(98)00064-6
  9. Cho, S. Y., B. K. Park, K. D. Moon, and D. H. Oh. 2004. Prevalence of Listeria monocytogenes and related species in minimally processed vegetables. J. Microbiol. Biotechnol. 14: 515-519
  10. Cole, M. B., M. V. Jones, and C. Holyoak. 1990. The effect of pH, salt concentration and temperature on the survival and growth of Listeria monocytogenes. J. Appl. Bacteriol. 69: 63-72 https://doi.org/10.1111/j.1365-2672.1990.tb02912.x
  11. Davey, K. R. and B. J. Daughtry. 1995. Validation of a model for predicting the combined effect of three environmental factors on both exponential and lag phases of bacterial growth: Temperature, salt concentration and pH. Food Res. Int. 28: 223-237
  12. Duh, Y. B. and D. W. Schaffner. 1993. Modelling the effect of temperature on the growth rate and lag time of Listeria innocua and Listeria monocytogenes. J. Food Prot. 56: 205-210 https://doi.org/10.4315/0362-028X-56.3.205
  13. Duffy, L. L., P. B. Vanderlinde, and F. H. Grau. 1994. Growth of Listeria monocytogenes on vacuum-packed cooked meats: Effects of pH, a, nitrite and ascorbate. Int. J. Food Microbiol. 23: 377-390 https://doi.org/10.1016/0168-1605(94)90164-3
  14. Farber, J. M. and P. I. Peterkin. 1991. Listeria monocytogenes, a food-borne pathogen. Microbiol. Rev. 55: 476-511
  15. Farber, J. M., G. W. Sanders, S. Dunfield, et al. 1989. The effect of various acidulants on the growth of Listeria monocytogenes. Lett. Appl. Microbiol. 9: 181-183 https://doi.org/10.1111/j.1472-765X.1989.tb00319.x
  16. Fernandez, P. S., S. M. George, C. C. Sills, and M. W. Peck. 1997. Predictive model of the effect of $CO_2$, pH, temperature and NaCl on the growth of Listeria monocytogenes. Int. J. Food Microbiol. 37: 37-45 https://doi.org/10.1016/S0168-1605(97)00043-3
  17. Gibson, A. M., N. Bratchell, and T. A. Roberts. 1988. Predicting microbial growth: Growth responses of salmonellae in a laboratory medium as affected by pH, sodium chloride and storage temperature. Int. J. Food Microbiol. 6: 155-178 https://doi.org/10.1016/0168-1605(88)90051-7
  18. Gibson, A. M., N. Bratchell, and T. A. Roberts. 1987. The effect of sodium chloride and temperature on the rate and extent of growth of Clostridium botulinum type A in pasteurized pork slurry. J. Appl. Bacteriol. 62: 479-490 https://doi.org/10.1111/j.1365-2672.1987.tb02680.x
  19. Grau, F. H. and P. B. Vanderlinede. 1993. Aerobic growth of Listeria monocytogenes on beef lean and fatty tissue: Equations describing the effects of temperature and pH. J. Food Prot. 56: 96-101 https://doi.org/10.4315/0362-028X-56.2.96
  20. Kim, H. J., H. B. Bennetto, and M. A. Halabi. 2004. Application of flow cytometry to monitoring of liposomal restructing induced by Listeria monocytogenes. J. Microbiol. Biotechnol. 14: 1099-1102
  21. Kim, S. Y., Y. M. Lee, S. Y. Lee, Y. S. Lee, J. H. Kim, C. Ahn, B. C. Kang, and G. E. Ji. 2001. Synergistic effect of citric acid and pediocin K1, a bacteriocin produced by Pediococcus sp. K1 on inhibition of Listeria monocytogenes. J. Microbiol. Biotechnol. 11: 831-837
  22. 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 https://doi.org/10.1016/S0168-1605(01)00640-7
  23. Lee, J. H., M. J. Kim, D. W. Jeong, M. J. Kim, J. H. Kim, H. C. Chang, D. K. Chung, H. Y. Kim, K. H. Kim, and H. J. Lee. 2005. Identification of bacteriocin-producing Lactobacillus paraplantarum first isolated from Kimchi. J. Microbiol. Biotechnol. 15: 428-433
  24. Lin, J. Q., S. M. Lee, and Y. M. Koo. 2005. Modeling and simulation of simultaneous saccharification and fermentation of paper mill sludge to lactic acid. J. Microbiol. Biotechnol. 15: 40-47
  25. Lin, J.-Q., S.-M. Lee, and Y.-M. Koo. 2004. Model development for lactic acid fermentation and parameter optimization using genetic algorithm. J. Microbiol. Biotechnol. 14: 1163-1169
  26. Marth, E. H. 1993. Growth and survival of Listeria monocytogenes, Salmonella species, and Staphylococcus aureus in the presence of sodium chloride: A review. Dairy Food Environ. Sanit. 13: 14-18
  27. McClure, P. J., A. L. Beaumont, J. P. Sutherland, and T. A. Roberts. 1997. Predictive modeling of growth of Listeria monocytogenes. The effects on growth of NaCl, pH, storage temperature and $NaNO_2$. Int. J. Food Microbiol. 34: 221- 232 https://doi.org/10.1016/S0168-1605(96)01193-2
  28. Mendonca, A. F., T. L. Amoroso, and S. J. Knabel. 1994. Destruction of gram-negative food-borne pathogens by high pH involves disruption of the cytoplasmic membrane. Appl. Environ. Microbiol. 60: 4009-4014
  29. Nolan, D. A., D. C. Champlin, and J. A. Troller. 1992. Minimal water activity levels for growth and survival of Listeria monocytogenes and Listeria innocua. Int. J. Food Microbiol. 16: 323-335 https://doi.org/10.1016/0168-1605(92)90034-Z
  30. Palumbo, S. A., A. C. Williams, R. L. Buchanan, and J. G. Phillips. 1991. Model for the aerobic growth of Aeromonas hydrophila K144. J. Food Prot. 55: 429-435
  31. Patil, N. K., U. Sharanagouda, J. H. Niazi, C.-K. Kim, and T. B. Karegoudar. 2003. Degradation of salicylic acid by free and immobilized cells of Pseudomonas sp. strain NGK1. J.Microbiol. Biotechnol. 13: 29-34
  32. Ross, T. 1996. Indices for performance evaluation of predictive models in food microbiology. J. Appl. Bacteriol. 81: 501-508
  33. Ross, T. 1999. Meat and Livestock Australia, Sydney, Australia. Predictive Food Microbiology Models in the Meat Industry
  34. Ross, T., P. Dalgaard, and S. Tienungoon. 2000. Predictive modelling of the growth and survival of Listeria in fishery products. Int. J. Food Microbiol. 62: 231-245 https://doi.org/10.1016/S0168-1605(00)00340-8
  35. SAS Institute Inc. 2002. SAS User's Guide. Statistical Analysis Systems Institute, Cary, NC, U.S.A
  36. Sutherland, J. P., A. J. Bayliss, and T. A. Roberts. 1994. Predictive modeling of growth of Staphylococcus aureus: The effects of temperature, pH, and sodium chloride. Int. J. Food Microbiol. 21: 217-236 https://doi.org/10.1016/0168-1605(94)90029-9
  37. Walker, S. J., P. Archer, and J. G. Banks. 1990. Growth of Listeria monocytogenes at refrigeration temperatures. J. Appl. Bacteriol. 68: 157-162 https://doi.org/10.1111/j.1365-2672.1990.tb02561.x
  38. Wijtzes, T., P. J. McClure, M. H. Zwietering, and T. A. Roberts. 1993. Modelling bacterial growth of Listeria monocytogenes as a function of water activity, pH and temperature. Int. J. Food Microbiol. 18: 139-149 https://doi.org/10.1016/0168-1605(93)90218-6
  39. Yoon, K. S., C. N. Butnette, and T. P. Oscar. 2004. Development of predictive models for the survival of Campylobacter jejuni (ATCC 43051) on cooked chicken breast patties and in broth as a function of temperature. J. Food Prot. 67: 64-70 https://doi.org/10.4315/0362-028X-67.1.64