Meta-analysis of D-values of proteolytic clostridium botulinum and its surrogate strain Clostridium sporogenes PA 3679

International Journal of Food Microbiology

Volumn 174, Issue , 2014, Pages 23-30

  Diao, Mamadou Moctar ^a,b   André, Stéphane ^c   Membré, Jeanne Marie ^a,b  

^a Ecole Nationale d'Ingenieurs des Techniques des Industries Agricoles et Alimentaires ENITIAA   (France)

^b LUNAM UNIVERSITÉ   (France)

^c Zone d'Activites l'Aeroport   (France)

Author keywords

Bayesian inference; Clostridium botulinum; Clostridium sporogenes PA 3679; Heat resistance; Mixed effect model; Z values

Indexed keywords

ARTICLE; BACTERIAL STRAIN; CLOSTRIDIUM BOTULINUM; CLOSTRIDIUM SPOROGENES; CULTURE MEDIUM; FOOD; HEAT TOLERANCE; HEAT TREATMENT; LIQUID CULTURE; MATHEMATICAL PARAMETERS; NONHUMAN; PH;

BAYESIAN INFERENCE; CLOSTRIDIUM BOTULINUM; CLOSTRIDIUM SPOROGENES PA 3679; HEAT RESISTANCE; MIXED EFFECT MODEL; Z-VALUES;

CLOSTRIDIUM; CLOSTRIDIUM BOTULINUM; FOOD MICROBIOLOGY; HOT TEMPERATURE; HYDROGEN-ION CONCENTRATION; LINEAR MODELS; SPORES, BACTERIAL;

EID: 84892630849     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2013.12.029     Document Type: Article

References (71)

1. Ababouch L., Busta F.F. Effect of thermal treatments in oils on bacterial spore survival. J. Appl. Bacteriol. 1987, 62:491-502.
2. Ababouch L., Dikra A., Busta F.F. Tailing of survivor curves of clostridial spores in edible oils. J. Appl. Bacteriol. 1987, 62:503-511.
3. Alderton G., Chen J.K., Ito K.A. Effect of lysozyne on the recovery of heated Clostridium botulinum spores. Appl. Microbiol. 1974, 27:613-615.
4. Alderton G., Ito K.A., Chen J.K. Chemical manipulation of the heat resistance of Clostridium botulinum spores. Appl. Environ. Microbiol. 1976, 31:492-498.
5. Anderson W.A., McClure P.J., Baird-Parker A.C., Cole M.B. The application of a log-logistic model to describe the thermal inactivation of Clostridium botulinum 213B at temperatures below 121.1° C. J. Appl. Bacteriol. 1996, 80:283-290.
6. Anderson N.M., Larkin J.W., Cole M.B., Skinner G.E., Whiting R.C., Gorris L.G.M., Rodriguez A., Buchanan R., Stewart C.M., Hanlin J.H., Keener L., Hall P.A. Food Safety Objective approach for controlling Clostridium botulinum growth and toxin production in commercially sterile foods. J. Food Prot. 2011, 74:1956-1989.
7. André S., Zuber F., Remize F. Thermophilic spore-forming bacteria isolated from spoiled canned food and their heat resistance. Results of a French ten-year survey. Int. J. Food Microbiol. 2013, 165:134-143.
8. Awuah G.B., Ramaswamy H.S., Economides A. Thermal processing and quality: principles and overview. Chem. Eng. Process. Process Intensif. 2007, 46:584-602.
9. Brown K.L., Martinez A. The heat resistance of spores of Clostridium botulinum 213B heated at 121-130° C in acidified mushroom extract. J. Food Prot. 1992, 55:913-915.
10. Brown J.L., Tran-Dinh N., Chapman B. Clostridium sporogenes PA 3679 and its uses in the derivation of thermal processing schedules for low-acid shelf-stable foods and as a research model for proteolytic Clostridium botulinum. J. Food Prot. 2012, 75:779-792.
11. Bull M.K., Olivier S.A., van Diepenbeek R.J., Kormelink F., Chapman B. Synergistic inactivation of spores of proteolytic Clostridium botulinum strains by high pressure and heat is strain and product dependent. Appl. Environ. Microbiol. 2009, 75:434-445.
12. Byun B., Cho H.-Y., Hwang H.-J., Mah J.-H., Liu Y., Tang J., Kang D.-H. Optimization and evaluation of heat-shock condition for spore enumeration being used in thermal-process verification: differential responses of spores and vegetative cells of Clostridium sporogenes to heat shock. Food Sci. Biotechnol. 2011, 20:751-757.
13. Cameron M.S., Leonard S.J., Barrett E.L. Effect of moderately acidic pH on heat resistance of Clostridium sporogenes spores in phosphate buffer and in buffered pea puree. Appl. Environ. Microbiol. 1980, 39:943-949.
14. Casolari A. Non-logarithmic inactivation of P.A. No. 3679 spores/inoculated in tunny, meat and cheese. Industria Conserve 1974, 49.
15. Dakins M.E., Toll J.E., Small M.J., Brand K.P. Risk-based environmental remediation: Bayesian Monte Carlo analysis and the expected value of sample information. Risk Anal. 1996, 16:67-79.
16. Dakins M.E., Toll J.E., Small M.J., Brand K.P. Risk-based environmental remediation: Bayesian Monte Carlo analysis and the expected value of sample information. Risk Anal. 1996, 16:67-79.
17. Deindoerfer F.H., Humphrey A.E. Analytical method for calculating heat sterilization times. Appl. Microbiol. 1959, 7:256-264.
18. Dixit A., Alam S.I., Dhaked R.K., Singh L. Sporulation and heat resistance of spores from a Clostridium sp. RKD. J. Food Sci. 2005, 70:m367-m373.
19. Doyle M.P. Foodborne bacterial pathogens 1989, Marcel Dekker Inc., New York and Basel.
20. Esselen W.B., Pflug I.J. Thermal resistance of putrefactive anaerobe N° 3679 spore in vegetables in the temperature range of 250-290°F. Food Technol. 1956, 11:557-560.
21. Esty J.R., Meyer K.F. The heat resistance of spore B. botulinus and allied anaerobes. J. Infect. Dis. 1922, 31:650-663.
22. Frank H.A., Campbell L.L. The influence of recovery media on thermal resistance values of spores of a putrefactive anaerobic bacterium. Appl. Microbiol. 1955, 3:300-302.
23. Frazier W.C. Food microbiology 1967, McGraw-Hill Inc., New York. 2nd ed.
24. Gaze J.E., Brown K.L. The heat resistance of spores of Clostridium botulinum 213B over the temperature range 120 to 140°C. Int. J. Food Sci. Technol. 1988, 23:373-378.
25. Gaze J.E., Brown K.L., Brown G.D., Food C., Association D.R. Comparative heat resistance studies on spores of Clostridium botulinum, Clostridium sporogenes and Bacillus stearothermophilus, thermoresistor studies and Bacillus datafile 1990, (Chipping Campden, UK). C. Food, D. Research Association (Eds.).
26. Gonzales Barron U., Bergin D., Butler F. A meta-analysis study of the effect of chilling on prevalence of Salmonella on pig carcasses. J. Food Prot. 2008, 71:1330-1337.
27. Gonzales-Barron U., Butler F. The use of meta-analytical tools in risk assessment for food safety. Food Microbiol. 2011, 28:823-827.
28. Hassan H.F., Ramaswamy H.S. Heat resistance of G. stearothermophilus and C. sporogenes in carrot and meat alginate purees. J. Food Process. Preserv. 2011, 35:376-385.
29. Holdsworth S.D. Optimisation of thermal processing - a review. J. Food Eng. 1985, 4:89-116.
30. ICMSF Microorganisms in foods 7: microbiological testing in food safety management 2002, Kluwer Academic/Plenum Publishers, New York.
31. Ito K.A., Seeger M.L., Bohrer C.W., Denny C.B., Bruch M.K. The thermal and germicidal resistance of Clostridium botulinum types A, B, and E spores. Proceedings of the first U.S.-Japan conference on toxic micro-organisms (Mycotoxins Botulism) 1970, 410-415. UJNR Joint Panels on toxic micro-organisms and the US Department of the Interior, Washington, D.C. H. Mendel (Ed.).
32. Jaloustre S., Guillier L., Morelli E., Noël V., Delignette-Muller M.L. Modeling of Clostridium perfringens vegetative cell inactivation in beef-in-sauce products: a meta-analysis using mixed linear models. Int. J. Food Microbiol. 2012, 154:44-51.
33. Kaplan A.M., Reynolds H., Lichtenstein H. Significance of variations in observed slopes of thermal death time curves for putrefactive anaerobes. J. Food Sci. 1954, 19:173-181.
34. Katzin L.I., Sandholzer L.A., Strong M.E. Application of the decimal reduction time principle to a study of the resistance of coliform bacteria to pasteurization. J. Bacteriol. 1943, 45:265-272.
35. Körmendy I., Mohácsi-Farkas C. Heat treatment and the defective units' ratio: surviving active spores in pea puree. J. Food Eng. 2000, 45:225-230.
36. Lambert R.J.W. A model for the thermal inactivation of micro-organisms. J. Appl. Microbiol. 2003, 95:500-507.
37. Leblanc F., Devlin K.A., Stumbo C.R. The influence of subtilin on the thermal resistance of spore Clostridium botulinum and the putrefactive anaerobe 3679. Food Technol. 1953, 7:181-184.
38. Leguerinel I., Mafart P. Modelling the influence of pH and organic acid types on thermal inactivation of Bacillus cereus spores. Int. J. Food Microbiol. 2001, 63:29-34.
39. Luechapattanaporn K., Wang Y., Wang J., Al-Holy M., Kang D.H., Tang J., Hallberg L.M. Microbial safety in radio-frequency processing of packaged foods. J. Food Sci. 2004, 69:201-206.
40. Lund B.M., Peck M.W. Clostridium botulinum. The Microbiological safety and quality of food 2000, 1057-1109. Aspen Publishers Inc., Gaithersburg, Maryland. B.M. Lund, T.C. Baird-Parker, G.W. Gould (Eds.).
41. Lynt R.K., Kautter D.A., Solomon H.M. Heat resistance of proteolytic Clostridium botulinurn Type F in phosphate buffer and crabmeat. J. Food Sci. 1982, 47:204-206.
42. Mah J.H., Kang D.H., Tang J. Comparison of viability and heat resistance of Clostridium sporogenes stored at different temperatures. J. Food Sci. 2008, 74:M23-M27.
43. Margosch D., Ehrmann M.A., Ganzle M.G., Vogel R.F. Comparison of pressure and heat resistance of Clostridium botulinum and other endospores in mashed carrots. J. Food Prot. 2004, 67:2530-2537.
44. Matsuda N., Komaki M., Matsunawa K. Heat resistance of spores of some Clostridium botulinum types A and B strains. J. Food Hyg. Soc. Jpn. 1980, 21:398-404.
45. Matsuda N., Komaki M., Matsunawa K. Heat resistance of Clostridium botulinum 62A spores in comminuted food substrates. Canners J. 1982, 61:1-7.
46. McClung L.S. Studies on anaerobic bacteria. X. Heat stable and heat labile antigens in the botulinus and related groups of spore-bearing anaerobes. J. Infect. Dis. 1937, 60:122-128.
47. Ocio M.J., Sanchez T., Fernandez P.S., Rodrigo M., Martinez A. Thermal resistance characteristics of PA 3679 in the temperature range of 110-121°C as affected by pH, type of acidulant and substrate. Int. J. Food Microbiol. 1994, 22:239-247.
48. Odlaug T.E., Pflug I.J. Recovery of spores of Clostridium botulinum in yeast extract agar and pork infusion agar after heat treatment. Appl. Environ. Microbiol. 1977, 34:377-381.
49. Odlaug T.E., Pflug I.J. Thermal destruction of Clostridium botulinum spores suspended in tomato juice in aluminum thermal death time tubes. Appl. Environ. Microbiol. 1977, 34:23-29.
50. Odlaug T.E., Pflug I.J., Kautter D.A. Heat resistance of Clostridium botulinum type B spores grown from isolates commercially canned mushrooms. J. Food Prot. 1978, 41:351-353.
51. Patil S., Cates S., Morales R. Consumer food safety knowledge, practices, and demographic differences: findings from a meta-analysis. J. Food Prot. 2005, 68:1884-1894.
52. Patwardhan A., Small M.J. Bayesian methods for model uncertainty analysis with application to future sea level rise. Risk Anal. 1992, 12:513-523.
53. Pflug I.J., Odlaug T.E. A review of z and F values used to ensure the safety of low-acid canned foods. Food Technol. 1978, 32:63-70.
54. Reynolds H., Kaplan A.M., Spencer F.B., Lichtenstein H. Thermal destruction of Cameron's putrefactive anaerobe 3679 in food substrates. J. Food Sci. 1952, 17:153-167.
55. Rigaux C., Denis J.-B., Albert I., Carlin F. A meta-analysis accounting for sources of variability to estimate heat resistance reference parameters of bacteria using hierarchical Bayesian modeling: estimation of D at 121.1°C and pH7, zT and zpH of Geobacillus stearothermophilus. Int. J. Food Microbiol. 2013, 161:112-120.
56. Rodrigo M., Martinez A. Determination of a process time for a new product: canned low acid artichoke hearts. Int. J. Food Sci. Technol. 1988, 23:31-41.
57. Rodrigo M., Martinez A., Sanchez T., Peris M.J., Safon J. Kinetics of Clostridium sporogenes PA3679 spore destruction using computer-controlled thermoresistometer. J. Food Sci. 1993, 58:649-652.
58. Rosnes J.T., Fernandez P.S., Periago P.M., Shara T. Microorganisms of relevance in thermally processed foods. Progress on Quantitative Approaches of Thermal Food Processing 2012, 1-37. Nova Science Publishers, New York. V. Valdramidis, J.F.M. Van Impe (Eds.).
59. Salgado D., Torres J.A., Welti-Chanes J., Velazquez G. Effect of input data variability on estimations of the equivalent constant temperature time for microbial inactivation by HTST and retort thermal processing. J. Food Sci. 2011, 76:E495-E502.
60. Santos M.H.S., Zarzo J.T. The effect of ethylenediaminetetraacetic acid on heat resistance and recovery of Clostridium sporogenes PA 3679 spores treated in HTST conditions. Int. J. Food Microbiol. 1997, 34:293-305.
61. Santos M.H.S., Kalasic H.N., Goti A.C., Enguidanos M.R. The effect of pH on the thermal resistance of Clostridium sporogenes (PA 3679) in asparagus purée acidified with citric acid and glucono-δ-lactone. Int. J. Food Microbiol. 1992, 16:275-281.
62. Secrist J.L.,., Stumbo C.R. Application of spores resistance in the newer methods of process evaluation. J. Food Sci. Technol. 1956, 10:543-545.
63. Stone G., Chapman B., Lovell D. Development of a log-quadratic model to describe microbial inactivation, illustrated by thermal inactivation of Clostridium botulinum. Appl. Environ. Microbiol. 2009, 75:6998-7005.
64. Stumbo C.R. A technique for studying resistance of bacterial spores to temperatures in the higher range. Food Technol. 1948, 2:228-240.
65. Stumbo C.R. Thermobacteriology in food processing 2nd ed 1973, Academic Press, Inc., New York.
66. Stumbo C.R., Murphy J.R., Cochran J. Nature of thermal death time curves for P.A. 3679 and Clostridium botulinum. Food Technol. 1950, 4:321-326.
67. 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.
68. Vialette M., Pinon A., Leporq B., Dervin C., Membré J.-M. Meta-analysis of food safety information based on a combination of a relational database and a predictive modeling tool. Risk Anal. 2005, 25:75-83.
69. Wallace M.J., Larson Nordsiden K., Wold I.D., Thompson D.R., Zottola E.A. Thermal inactivation of Clostridium sporogenes PA 3679 and Bacillus stearothermophillus 1518 in low-acid home-canned foods. J. Food Sci. 1978, 43:1738-1740.
70. Xezone J., Hutchings I.J. Thermal resistance of Clostridium botulinum (62A) spores as affected by fundamental food constituents. I. Effect of pH. Food Technol. 1965, 19:113-115.
71. Zhu S., Naim F., Marcotte M., Ramaswamy H., Shao Y. High-pressure destruction kinetics of Clostridium sporogenes spores in ground beef at elevated temperatures. Int. J. Food Microbiol. 2008, 126:86-92.