Predicting growth rates and growth boundary of Listeria monocytogenes - An international validation study with focus on processed and ready-to-eat meat and seafood

International Journal of Food Microbiology

Volumn 141, Issue 3, 2010, Pages 137-150

  Mejlholm, Ole ^a   Gunvig, Annemarie ^b   Borggaard, Claus ^b   Blom Hanssen, Jesper ^b   Mellefont, Lyndal ^c   Ross, Tom ^c   Leroi, Francoise ^d   Else, Tony ^e   Visser, Diana ^e   Dalgaard, Paw ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b DANISH MEAT RESEARCH INSTITUTE   (Denmark)

^c UNIVERSITY OF TASMANIA   (Australia)

^d IFREMER   (France)

^e PURAC biochem bv ^*  (Netherlands)

Author keywords

Bias and accuracy factors; Correct prediction percentage; Growth no growth predictions; Predictive models; Psi ( ) value

Indexed keywords

ACETIC ACID; ACETOACETIC ACID; CARBON DIOXIDE; LACTIC ACID; NITRITE;

ARTICLE; ENVIRONMENTAL PARAMETERS; EVALUATION; FOOD CONTROL; FOOD PROCESSING; FOOD STORAGE; GROWTH RATE AND GROWTH REGULATION; LISTERIA MONOCYTOGENES; MEAT; MICROBIAL GROWTH; NONHUMAN; SEA FOOD; VALIDATION STUDY; ANALYSIS; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; FAST FOOD; FOOD CONTAMINATION; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; KINETICS; MICROBIOLOGY;

ANIMALS; FAST FOODS; FOOD CONTAMINATION; KINETICS; LISTERIA MONOCYTOGENES; MEAT; MODELS, BIOLOGICAL; SEAFOOD;

LISTERIA MONOCYTOGENES;

EID: 77954311471     PISSN: 01681605     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2010.04.026     Document Type: Article

References (74)

1. Augustin J.-C., Carlier V. Mathematical modelling of the growth rate and lag time for Listeria monocytogenes. International Journal of Food Microbiology 2000, 56:29-51.
2. Augustin J.C., Zuliani V., Cornu M., Guillier L. Growth rate and growth probability of Listeria monocytogenes in dairy, meat and seafood products in suboptimal conditions. Journal of Applied Microbiology 2005, 99:1019-1042.
3. Barmpalia I.M., Koutsoumanis K.P., Geornaras I., Belk K.E., Scanga J.A., Kendall P.A., Smith G.C., Sofos J.N. Effect of antimicrobials as ingredients of pork bologna for Listeria monocytogenes control during storage at 4 and 10°C. Food Microbiology 2005, 22:205-211.
4. Bidlas E., Lambert R.J.W. Quantification of hurdles: predicting the combination of effects-interaction vs. non-interaction. International Journal of Food Microbiology 2008, 128:78-88.
5. Blom H., Nerbrink E., Dainty R., Hagtvedt T., Borch E., Nissen H., Nesbakken T. Addition of 2.5% lactate and 0.25% acetate controls growth of Listeria monocytogenes in vacuum-packed, sensory acceptable servelat sausage and cooked ham stored at 4°C. International Journal of Food Microbiology 1997, 38:71-76.
6. Burnett S.L., Mertz E.L., Bennie B., Ford T., Starobin A. Growth or survival of Listeria monocytogenes in ready-to-eat meat products and combination deli salads during refrigerated storage. Journal of Food Science 2005, 70:M301-M304.
7. CAC, 1999. Principles and Guidance for the Conduct of Microbiological Risk Assessment (CAC/GL-30). Codex Alimentarius Commission, Rome, Italy. accessed in October 2009. http://www.codexalimentarius.net/download/standards/357/CXG_030e.pdf.
8. Cardinal M., Gunnlaugsdottir H., Bjoernevik M., Ouisse A., Vallet J.L., Leroi F. Sensory characteristics of cold-smoked Atlantic salmon (Salmo salar) from European market and relationships with chemical, physical and microbiological measurements. Food Research International 2004, 37:181-193.
9. Chirife J., Resnik S.L. Unsaturated solutions of sodium chloride as reference sources of water activity at various temperatures. Journal of Food Science 1984, 49:1486-1488.
10. Combase, 2009. Combase Browser accessed in October 2009 at http://combase.arserrc.gov/BrowserHome/SearchOptions/Search.aspx.
11. Dalgaard P. Modelling of microbial activity and prediction of shelf life for packed fresh fish. International Journal of Food Microbiology 1995, 26:305-317.
12. Dalgaard P., Jørgensen L.V. Predicted and observed growth of Listeria monocytogenes in seafood challenge tests and in naturally contaminated cold-smoked salmon. International Journal of Food Microbiology 1998, 40:105-115.
13. Delignette-Muller M.L., Cornu M., Pouillot R., Denis J.-B. Use of Bayesian modelling in risk assessment: application to growth of Listeria monocytogenes and food flora in cold-smoked salmon. International Journal of Food Microbiology 2006, 106:195-208.
14. DRMI, 2007. Listeria model from Danish Meat Research Institute (DMRI). Available from (username: matmodel and password: listeria). http://1.test.dezone.dk/.
15. EC Commission regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. Official Journal of the European Union 2005, 338:1-25.
16. FAO/WHO, 2009. Proposed Draft Microbiological Criteria for Listeria monocytogenes in Ready-to-Eat Foods (ALINORM 09/32/13). Codex Alimentarius Commission, 32nd Session, Rome, Italy, 29 June-4 July 2009. accessed on 10 October 2009. http://www.codexalimentarius.net/web/archives.jsp.
17. FSIS, 2008. USDA Food Safety and Inspection Service. Supplementary guidance on the use of antimicrobial agents to control Listeria monocytogenes in post-lethality exposed ready-to-eat meat and poultry Products. Accessed on 24 November 2009. http://www.fsis.usda.gov/Significant_Guidance/index.asp.
18. Giménez B., Dalgaard P. Modelling and predicting the simultaneous growth of Listeria monocytogenes and spoilage micro-organisms in cold-smoked salmon. Journal of Applied Microbiology 2004, 96:96-109.
19. Giuffrida A., Valenti D., Ziino G., Spagnolo B., Panebianco A. A stochastic interspecific competition model to predict the behaviour of Listeria monocytogenes in the fermentation process of a traditional Sicilian salami. European Food Research and Technology 2009, 228:767-775.
20. Glass K.A., Doyle M.P. Fate of Listeria monocytogenes in processed meat products during refrigerated storage. Applied and Environmental Microbiology 1989, 55:1565-1569.
21. Glass K.A., Granberg D.A., Smith A.L., McNamara A.M., Hardin M., Mattias J., Ladwig K., Johnson E.A. Inhibition of Listeria monocytogenes by sodium diacetate and sodium lactate on wieners and cooked bratwurst. Journal of Food Protection 2002, 65:116-123.
22. Glass K., Preston D., Veesenmeyer J. Inhibition of Listeria monocytogenes in turkey and pork-beef bologna by combinations of sorbate, benzoate, and propionate. Journal of Food Protection 2007, 70:214-217.
23. Glass K.A., McDonnell L.M., Rassel R.C., Zierke K.L. Controlling Listeria monocytogenes on sliced ham and turkey products using benzoate, propionate, and sorbate. Journal of Food Protection 2007, 70:2306-2312.
24. Gougouli M., Angelidis A.S., Koutsoumanis K. A study on the kinetic behavior of Listeria monocytogenes in ice cream stored under static and dynamic chilling and freezing conditions. Journal of Dairy Science 2008, 91:523-530.
25. Gunvig A., Blom-Hanssen J., Jacobsen T., Hansen F., Borggaard C. A predictive model for growth of Listeria monocytogenes in meat products with seven hurdle variables. 5th Int. Conf. Predictive Modelling in Foods-Conference Proceedings 2007, 197-200. Agricultural University of Athens, Athens. G.J.E. Nychas (Ed.).
26. Hwang C.A. Development of predictive models for Listeria monocytogenes in selected refrigerated ready-to-eat foods. 6th Int. Conf. Predictive Modeling in Foods-Conference Proceedings 2009, http://www.icpmf.org/ accessed on 10 October.
27. Hwang C.A. The probability of growth of Listeria monocytogenes in cooked salmon and tryptic soy broth as affected by salt, smoke compound, and storage temperature. Food Microbiology 2009, 26:253-258.
28. Hwang C.A., Sheen S. Modeling the growth characteristics of Listeria monocytogenes and native microflora in smoked salmon. Journal of Food Science 2009, 74:M125-M130.
29. Hwang C.A., Tamplin M.L. Modeling the lag phase and growth rate of Listeria monocytogenes in ground ham containing sodium lactate and sodium diacetate at various storage temperatures. Journal of Food Science 2007, 72:M246-M253.
30. Jørgensen L.V., Huss H.H. Prevalence and growth of Listeria monocytogenes in naturally contaminated seafood. International Journal of Food Microbiology 1998, 42:127-131.
31. w when grown in suspension or on a solid surface. Food Microbiology 2004, 21:415-422.
32. Lakshmanan R., Dalgaard P. Effects of high-pressure processing on Listeria monocytogenes, spoilage microflora and multiple compound quality indices in chilled cold-smoked salmon. Journal of Applied Microbiology 2004, 96:398-408.
33. Le Marc Y., Huchet V., Bourgeois C.M., Guyonnet J.P., Mafart P., Thuault D. Modelling the growth kinetics of Listeria as a function of temperature, pH and organic acid concentration. International Journal of Food Microbiology 2002, 73:219-237.
34. Legan J.D., Seman D.L., Milkowski A.L., Hirschey J.A., Vandeven M.H. Modeling the growth boundary of Listeria monocytogenes in ready-to-eat cooked meat products as a function of the product salt, moisture, potassium lactate, and sodium diacetate concentrations. Journal of Food Protection 2004, 67:2195-2204.
35. Lustre A.O., Issenberg P. Phenolic components of smoked meat products. Journal of Agricultural and Food Chemistry 1970, 18:1056-1058.
36. McMeekin T.A., Baranyi J., Bowman J., Dalgaard P., Kirk M., Ross T., Schmid S., Zwietering M.H. Information systems in food safety management. International Journal of Food Microbiology 2006, 112:181-194.
37. Mejlholm O., Dalgaard P. Modeling and predicting the growth boundary of Listeria monocytogenes in lightly preserved seafood. Journal of Food Protection 2007, 70:70-84.
38. Mejlholm O., Dalgaard P. Modeling and predicting the growth of lactic acid bacteria in lightly preserved seafood and their inhibiting effect on Listeria monocytogenes. Journal of Food Protection 2007, 70:2485-2497.
39. Mejlholm O., Dalgaard P. Development and validation of an extensive growth and growth boundary model for Listeria monocytogenes in lightly preserved and ready-to-eat shrimp. Journal of Food Protection 2009, 72:2132-2143.
40. Mejlholm O., Bøknæs N., Dalgaard P. Shelf life and safety aspects of chilled cooked and peeled shrimps (Pandalus borealis) in modified atmosphere packaging. Journal of Applied Microbiology 2005, 99:66-76.
41. Mellefont L.A., Ross T. Effect of potassium lactate and a potassium lactate-sodium diacetate blend on Listeria monocytogenes growth in modified atmosphere packaged sliced ham. Journal of Food Protection 2007, 70:2297-2305.
42. Nerbrink E., Borch E., Blom H., Nesbakken T. A model based on absorbance data on the growth rate of Listeria monocytogenes and including the effects of pH, NaCl, Na-lactate and Na-acetate. International Journal of Food Microbiology 1999, 47:99-109.
43. Pal A., Labuza T.P., Diez-Gonzalez F. Evaluating the growth of Listeria monocytogenes in refrigerated ready-to-eat frankfurters: influence of strain, temperature, packaging, lactate and diacetate, and background microflora. Journal of Food Protection 2008, 71:1806-1816.
44. Pal A., Labuza T.P., Diez-Gonzalez F. Shelf life evaluation for ready-to-eat sliced uncured turkey breast and cured ham under probable storage conditions based on Listeria monocytogenes and psychrotroph growth. International Journal of Food Microbiology 2008, 126:49-56.
45. Panagou E.Z., Nychas G.J.E. Dynamic modeling of Listeria monocytogenes growth in pasteurized vanilla cream after postprocessing contamination. Journal of Food Protection 2008, 71:1828-1834.
46. Paranjpye R.N., Peterson M.E., Poysky F.T., Eklund M.W. Incidence, growth, and inactivation of Listeria monocytogenes in cooked and peeled cold-water shrimp. Journal of Aquatic Food Product Technology 2008, 17:266-284.
47. Pelroy G.A., Peterson M.E., Holland P.J., Eklund M.W. Inhibition of Listeria monocytogenes in cold-process (smoked) salmon by sodium lactate. Journal of Food Protection 1994, 57:108-113.
48. Pelroy G.A., Peterson M.E., Paranjpye R.N., Almond J., Eklund M.W. Inhibition of Listeria monocytogenes in cold-process (smoked) salmon by sodium nitrite and packaging method. Journal of Food Protection 1994, 57:114-119.
49. Peterson M.E., Pelroy G.A., Paranjpye R.N., Poysky F.T., Almond J.S., Eklund M.W. Parameters for control of Listeria monocytogenes in smoked fishery products - sodium-chloride and packaging method. Journal of Food Protection 1993, 56:938-943.
50. Peterson L.D., Faith N.G., Czuprynski C.J. Growth of L. monocytogenes strain F2365 on ready-to-eat turkey meat does not enhance gastrointestinal listeriosis in intragastrically inoculated A/J mice. International Journal of Food Microbiology 2008, 126:112-115.
51. Porto A.C.S., Franco B.D.G.M., Sant'Anna E.S., Call J.E., Piva A., Luchansky J.B. Viability of a five-strain mixture of Listeria monocytogenes in vacuum-sealed packages of frankfurters, commercially prepared with and without 2.0 or 3.0% added potassium lactate, during extended storage at 4 and 10 degrees C. Journal of Food Protection 2002, 65:308-315.
52. Pouillot R., Miconnet N., Afchain A.-L., Delignette-Muller M.L., Beaufort A., Rosso L., Denis J.-B., Cornu M. Quantitative risk assessment of Listeria monocytogenes in French cold-smoked salmon: I. Quantitative exposure assessment. Risk Analysis 2007, 27:683-700.
53. Powell M.R., Tamplin M., Marks B., Campos D.T. Bayesian synthesis of a pathogen growth model: Listeria monocytogenes under competition. International Journal of Food Microbiology 2006, 109:34-46.
54. Pradhan A.K., Ivanek R., Grohn Y.T., Geornaras I., Sofos J.N., Wiedemann M. Quantitative risk assessment for Listeria monocytogenes in selected categories of deli meats: impact of lactate and diacetate on Listeriosis Cases and Deaths. Journal of Food Protection 2009, 72:978-989.
55. PURAC, 2007. Opti.Form Listeria control 2007 model. http://www.purac.com/EN/Food/Contact.aspx. Accessed in October 2008. http://www.purac.com/EN/Food/Contact.aspx.
56. Rosenow E.M., Marth E.H. Growth of Listeria-monocytogenes in skim, whole and chocolate milk, and in whipping cream during incubation at 4°C, 8°C, 13°C, 21°C and 35°C. Journal of Food Protection 1987, 50:452-459.
57. Ross T. Indices for performance evaluation of predictive models in food microbiology. Journal of Applied Bacteriology 1996, 81:501-508.
58. Ross T. Predictive Food Microbiology Models in the Meat Industry 1999, Meat and Livestock Australia, North Sydney, Australia, pp. 196.
59. Ross T., Dalgaard P. Secondary models. Modeling Microbial Responses in Food 2004, 63-150. CRC Press, Boca Raton. R.C. McKellar, X. Lu (Eds.).
60. Seman D.L., Borger A.C., Meyer J.D., Hall P.A., Milkowski A.L. Modeling the growth of Listeria monocytogenes in cured ready-to-eat processed meat products by manipulation of sodium chloride, sodium diacetate, potassium lactate, and product moisture content. Journal of Food Protection 2002, 65:651-658.
61. Skandamis P.N., Stopforth J.D., Yoon Y., Kendall P.A., Sofos J.N. Modeling the effect of storage atmosphere on growth-no growth interface of Listeria monocytogenes as a function of temperature, sodium lactate, sodium diacetate, and NaCl. Journal of Food Protection 2007, 70:2329-2338.
62. SSSP, 2009. Seafood Spoilage and Safety Predictor (SSSP) software version 3.1 from august 2009, accessed in October 2009. http://sssp.dtuaqua.dk.
63. Stekelenburg F.K. Enhanced inhibition of Listeria monocytogenes in Frankfurter sausage by the addition of potassium lactate and sodium diacetate mixtures. Food Microbiology 2003, 20:133-137.
64. Stekelenburg F.K., Kant-Muermans M.L.T. Effects of sodium lactate and other additives in a cooked ham product on sensory quality and development of a strain of Lactobacillus curvatus and Listeria monocytogenes. International Journal of Food Microbiology 2001, 66:197-203.
65. Szabo E.A., Cahill M.E. Nisin and ALTA (TM) 2341 inhibit the growth of Listeria monocytogenes on smoked salmon packaged under vacuum or 100% CO2. Letters in Applied Microbiology 1999, 28:373-377.
66. Tamplin M. Accessible modelling software and databases. Bulletin of the International Dairy Federation 2009, 433:59-64.
67. te Giffel M.C., Zwietering M.H. Validation of predictive models describing the growth of Listeria monocytogenes. International Journal of Food Microbiology 1999, 46:135-149.
68. Theys T.E., Geeraerd A.H., Verhulst A., Poot K., Van Bree I., Devlieghere F., Moldenaers P., Wilson D., Brocklehurst T., Van Impe J.F. Effect of pH, water activity and gel micro-structure, including oxygen profiiles and rheological characterization, on the growth kinetics of Salmonella Thyphimurium. International Journal of Food Microbiology 2008, 128:67-77.
69. Thurette, J., 1995. Listeria et saumons fumes: Acquisition de donnees pour la microbiologie previsionelle, PhD thesis, Université des Sciences et Technologies de Lille, Lille, France. pp 248.
70. Tienungoon S., Ratkowsky D.A., McMeekin T.A., Ross T. Growth limits of Listeria monocytogenes as a function of temperature, pH, NaCl, and lactic acid. Applied and Environmental Microbiology 2000, 66:4979-4987.
71. Vermeulen A., Gysemans K.P.M., Bernaerts K., Geeraerd A.H., Van Impe J.F., Debevere J., Devlieghere F. Influence of pH, water activity and acetic acid concentration on Listeria monocytogenes at 7°C: data collection for the development of a growth/no growth model. International Journal of Food Microbiology 2007, 114:332-341.
72. Wederquist H.J., Sofos J.N., Schmidt G.R. Listeria monocytogenes inhibition in refrigerated vacuum-packaged turkey bologna by chemical additives. Journal of Food Science 1994, 59:498-516.
73. Yoon K.S., Burnette C.N., Abou-Zeid K.A., Whiting R.C. Control of growth and survival of Listeria monocytogenes on smoked salmon by combined potassium lactate and sodium diacetate and freezing stress during refrigeration and frozen storage. Journal of Food Protection 2004, 67:2465-2471.
74. Zuliani V., Lebert I., Augustin J.-C., Garry P., Vendeuvre J.-L., Lebert A. Modelling the behaviour of Listeria monocytogenes in ground pork as a function of pH, water activity, nature and concentration of organic acid salts. Journal of Applied Microbiology 2007, 103:536-550.