Thermosonication versus thermal processing of skim milk and beef slurry: Modeling the inactivation kinetics of psychrotrophic Bacillus cereus spores

Food Research International

Volumn 67, Issue , 2015, Pages 67-74

  Evelyn, ^a   Silva, Filipa V M ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF RIAU   (Indonesia)

Author keywords

Bacteria; Modeling; Sonication; Survival; Thermal; Ultrasonics

Indexed keywords

BACILLUS CEREUS; BACTERIA; BACTERIOLOGY; BEEF; ENERGY CONSERVATION; FOOD PRESERVATION; HEAT TREATMENT; MODELS; SONICATION; ULTRASONICS;

BACILLUS CEREUS SPORES; INACTIVATION KINETICS; LOG-LOGISTIC MODEL; LOWER TEMPERATURES; SURVIVAL; THERMAL; THERMO SONICATIONS; ULTRASOUND TECHNOLOGY;

THERMAL PROCESSING (FOODS);

BACILLUS CEREUS;

EID: 84912016365     PISSN: 09639969     EISSN: 18737145     Source Type: Journal    
DOI: 10.1016/j.foodres.2014.10.028     Document Type: Article

References (76)

1. Ahmed A. Incidence of Bacillus cereus in milk and some milk products. Journal of Food Protection 1983, 46:126-128.
2. Ahmed F., Russell C. Synergism between ultrasonic waves and hydrogen peroxide in the killing of microorganisms. Journal of Applied Microbiology 1975, 39:31-40.
3. Awad T., Moharram H., Shaltout O., Asker D., Youssef M. Applications of ultrasound in analysis, processing and quality control of food: A review. Food Research International 2012, 48:410-427.
4. Barbano D.M., Ma Y., Santos M.V. Influence of raw milk quality on fluid milk shelf life. Journal of Dairy Science 2006, 89:E15-E19.
5. Bassen M., Gupta L., Jolly L., Tewari R. Thermal resistance of Bacillus cereus spores in custard preparations. MIRCEN Journal of Applied Microbiology and Biotechnology 1989, 5:511-516.
6. Burgos J., Ordonez J., Sala F. Effect of ultrasonic waves on the heat resistance of Bacillus cereus and Bacillus licheniformis spores. Journal of Applied Microbiology 1972, 24:497-498.
7. Butz P., Tauscher B. Emerging technologies: Chemical aspects. Food Research International 2002, 35:279-284.
8. Byrne B., Dunne G., Bolton D. Thermal inactivation of Bacillus cereus and Clostridium perfringens vegetative cells and spores in pork luncheon roll. Food Microbiology 2006, 23:803-808.
9. Carlin F., Girardin H., Peck M.W., Stringer S.C., Barker G.C., Martinez A., et al. Research on factors allowing a risk assessment of spore-forming pathogenic bacteria in cooked chilled foods containing vegetables: a FAIR collaborative project. International Journal of Food Microbiology 2000, 60:117-135.
10. Carlin F., Guinebretiere M.H., Choma C., Pasqualini R., Braconnier A., Nguyen-the C. Spore-forming bacteria in commercial cooked, pasteurised and chilled vegetable purees. Food Microbiology 2000, 17:153-165.
11. Chen D. Applications of ultrasound in water and wastewater treatment. Handbook on application of ultrasound: Sonochemistry for sustainability 2012, 373-406. CRC Press, USA. D. Chen, S.K. Sharma, A. Mudhoo (Eds.).
12. Chen H., Hoover D.G. Modeling the combined effect of high hydrostatic pressure and mild heat on the inactivation kinetics of Listeria monocytogenes Scott A in whole milk. Innovative Food Science & Emerging Technologies 2003, 4:25-34.
13. Choma C., Guinebretiere M., Carlin F., Schmitt P., Velge P., Granum P. Prevalence, characterization and growth of Bacillus cereus in commercial cooked chilled foods containing vegetables. Journal of Applied Microbiology 2000, 88:617-625.
14. Christiansson A., Naidu A.S., Nilsson I., Wadström T., Pettersson H. Toxin production by Bacillus cereus dairy isolates in milk at low temperatures. Applied Environmental Microbiology 1989, 55:2595-2600.
15. Collado J., Fernández A., Rodrigo M., Martinez A. Modelling the effect of a heat shock and germinant concentration on spore germination of a wild strain of Bacillus cereus. International Journal of Food Microbiology 2006, 106:85-89.
16. Collins E.B. Heat resistant psychrotrophic microorganisms. Journal of Dairy Science 1981, 64:157-160.
17. Daryaei H., Balasubramaniam V.M. Kinetics of Bacillus coagulans spore inactivation in tomato juice by combined pressure-heat treatment. Food Control 2013, 30:168-175.
18. Daryaei H., Balasubramaniam V.M., Legan J.D. Kinetics of Bacillus cereus spore inactivation in cooked rice by combined pressure-heat treatment. Journal of Food Protection 2013, 76:616-623.
19. Desai S.V., Varadaraj M.C. Behavioural pattern of vegetative cells and spores of Bacillus cereus as affected by time-temperature combinations used in processing of Indian traditional foods. Journal of Food Science and Technology 2010, 47:549-556.
20. Dierick K., Van Coillie E., Swiecicka I., Meyfroidt G., Devlieger H., Meulemans A., et al. Fatal family outbreak of Bacillus cereus-associated food poisoning. Journal of Clinical Microbiology 2005, 43:4277-4279.
21. Dufrenne J., Bijwaard M., Te Giffel M., Beumer R., Notermans S. Characteristics of some psychrotrophic Bacillus cereus isolates. International Journal of Food Microbiology 1995, 27:175-183.
22. EFSA Bacillus cereus and other Bacillus spp in foodstuffs. Journal of European Food Safety Authority (EFSA) 2005, 175:1-48.
23. Evreux F., Delaporte B., Leret N., Buffet-Janvresse C., Morel A. A case of fatal neonatal Bacillus cereus meningitis. Archives de Pédiatrie: Organe Officiel de la Sociéte Française de Pédiatrie 2007, 14:365.
24. Fellows P.J. Food processing technology: Principles and practice 2000, CRC Press, USA, (Chapter 2).
25. Feng, H., Pearlstein, A., & Zhou, B. (2009). Continuous-flow bacterial disinfection of fruit, vegetables, fresh cut produce and leafy greens using high intensity ultrasound. US Patent 61/245 382.
26. Feng H., Yang W. Ultrasonic processing. Nonthermal processing technologies for food 2011, 135-154. Wiley-Blackwell, USA. J.P. Clark, C. Ritson, G.W. Smithers, M.A. Augustin, W. Ellefson, L. Zach, F. Shahidi (Eds.).
27. Fernández A., Ocio M., Fernández P., Martínez A. Effect of heat activation and inactivation conditions on germination and thermal resistance parameters of Bacillus cereus spores. International Journal of Food Microbiology 2001, 63:257-264.
28. FSANZ Agents of foodborne illness: A technical series summarising key information on microorganisms associated with foodborne illness (Accessed 14 of March 2014). http://www.foodstandards.govt.nz/publications/Documents/FSANZ_FoodborneIllness_2013_WEB.pdf.
29. Gao S., Lewis G.D., Ashokkumar M., Hemar Y. Inactivation of microorganisms by low-frequency high-power ultrasound: 1. Effect of growth phase and capsule properties of the bacteria. Ultrasonics Sonochemistry 2014, 21:446-453.
30. Garcia M.L., Burgos J., Sanz B., Ordonez J. Effect of heat and ultrasonic waves on the survival of two strains of Bacillus subtilis. Journal of Applied Bacteriology 1989, 67:619-628.
31. Gera N., Doores S. Kinetics and mechanism of bacterial inactivation by ultrasound waves and sonoprotective effect of milk components. Journal of Food Science 2011, 76:M111-M119.
32. Ghelardi E., Celandroni F., Salvetti S., Barsotti C., Baggiani A., Senesi S. Identification and characterization of toxigenic Bacillus cereus isolates responsible for two food-poisoning outbreaks. FEMS Microbiology Letters 2002, 208:129-134.
33. Gogate P.R. Application of hydrodynamic cavitation for food and bioprocessing. Ultrasound technologies for food and bioprocessing 2011, 141-173. Springer, New York. H. Feng, G. Barbosa-Cánovas, J. Weiss (Eds.).
34. González I., López M., Martinez S., Bernardo A., González J. Thermal inactivation of Bacillus cereus spores formed at different temperatures. International Journal of Food Microbiology 1999, 51:81-84.
35. Granum P.E., Lund T. Bacillus cereus and its food poisoning toxins. FEMS Microbiology Letters 1997, 157:223-228.
36. Harvey E.N., Loomis A.L. The destruction of luminous bacteria by high frequency sound waves. Journal of Bacteriology 1929, 17:373.
37. Hielscher-Ultrasonic Ultrasonic homogenizers for liquid processing: Ultrasonic lab devices and industrial processors (Accessed 21 April 2014). http://www.hielscher.com/products.htm.
38. Jenson I., Moir C., Hocking A. Bacillus cereus and other Bacillus species. Foodborne microorganisms of public health significance 2003, 445-478. Australian Institute of Food Science and Technology (NSW Branch), Sydney. A. Hocking (Ed.).
39. Joyce E., Phull S., Lorimer J., Mason T. The development and evaluation of ultrasound for the treatment of bacterial suspensions: A study of frequency, power and sonication time on cultured Bacillus species. Ultrasonics Sonochemistry 2003, 10:315-318.
40. Lekogo B.M., Coroller L., Mathot A.G., Mafart P., Leguerinel I. Modelling the influence of palmitic, palmitoleic, stearic and oleic acids on apparent heat resistance of spores of Bacillus cereus NTCC 11145 and Clostridium sporogenes Pasteur 79.3. International Journal of Food Microbiology 2010, 141:242-247.
41. López-Malo A., Jimenez-Fernandez M., Palou E. Penicillium digitatum spores inactivation by combining thermoultrasonication treatments and antimicrobial agents. IFT 2001 annual meeting technical program abstracts 2001, 151.
42. López-Malo A., Palou E., Jiménez-Fernández M., Alzamora S.M., Guerrero S. Multifactorial fungal inactivation combining thermosonication and antimicrobials. Journal of Food Engineering 2005, 67:87-93.
43. Luby S., Jones J., Dowda H., Kramer J., Horan J. A large outbreak of gastroenteritis caused by diarrheal toxin-producing Bacillus cereus. Journal of Infectious Diseases 1993, 167:1452-1455.
44. Luu-Thi H., Khadka D.B., Michiels C.W. Thermal inactivation parameters of spores from different phylogenetic groups of Bacillus cereus. International Journal of Food Microbiology 2014, 189:183-188.
45. Mason T.J., Paniwnyk L., Lorimer J.P. The uses of ultrasound in food technology. Ultrasonics Sonochemistry 1996, 3:253-260.
46. Novak J.S., Call J., Tomasula P., Luchansky J.B. An assessment of pasteurization treatment of water, media, and milk with respect to Bacillus spores. Journal of Food Protection 2005, 68:751-757.
47. Ordonez J., Burgos J. Effect of ultrasonic waves on the heat resistance of Bacillus spores. Applied Environmental Microbiology 1976, 32:183-184.
48. Ortega-Rivas E. Ultrasound in food preservation. Non-thermal food engineering operations 2012, 251-262. Springer, US. G.V. Barbosa-Carnovas (Ed.).
49. Palacios P., Burgos J., Hoz L., Sanz B., Ordóñez J.A. Study of substances released by ultrasonic treatment from Bacillus stearothermophilus spores. Journal of Applied Bacteriology 1991, 71:445-451.
50. Peng J.S., Tsai W.C., Chou C.C. Surface characteristics of Bacillus cereus and its adhesion to stainless steel. International Journal of Food Microbiology 2001, 65:105-111.
51. Pina-Pérez M., Silva-Angulo A., Rodrigo D., Martínez-López A. Synergistic effect of Pulsed Electric Fields and CocoanOX 12% on the inactivation kinetics of Bacillus cereus in a mixed beverage of liquid whole egg and skim milk. International Journal of Food Microbiology 2009, 130:196-204.
52. Piyasena P., Mohareb E., McKellar R. Inactivation of microbes using ultrasound: A review. International Journal of Food Microbiology 2004, 87:207-216.
53. Riesz P., Kondo T. Free radical formation induced by ultrasound and its biological implications. Free Radical Biology and Medicine 1992, 13:247-270.
54. Ross T. Indices for performance evaluation of predictive models in food microbiology. Journal of Applied Microbiology 1996, 81:501-508.
55. Røssland E., Langsrud T., Granum P.E., Sørhaug T. Production of antimicrobial metabolites by strains of Lactobacillus or Lactococcus co-cultured with Bacillus cereus in milk. International Journal of Food Microbiology 2005, 98:193-200.
56. Russell A. The destruction of bacterial spores. Inhibition and destruction of the microbial cell 1971, Academic Press, London and New York. W.B. Hugo (Ed.).
57. Sagong H.G., Cheon H.L., Lee S.Y., Park K.H., Chung M.S., Ryu S., et al. Combined effects of ultrasound and surfactants to reduce Bacillus cereus spores on lettuce and carrots. International Journal of Food Microbiology 2012, 160:367-372.
58. Sala F.J., Burgos J., Condon S., Lopez P., Raso J. Effect of heat and ultrasounds on microorganisms and enzymes. New methods of food preservation 1995, 176-204. Blackie, Glasgow. G.W. Gould (Ed.).
59. Samapundo S., Everaert H., Wandutu J.N., Rajkovic A., Uyttendaele M., Devlieghere F. The influence of headspace and dissolved oxygen level on growth and haemolytic BL enterotoxin production of a psychrotolerant Bacillus weihenstephanensis isolate on potato based ready-to-eat food products. Food Microbiology 2011, 28:298-304.
60. Santamaria L., Castellani A., Levi F.A. Hyaluronidase inactivation by ultrasonic waves and its mechanism. Enzymologia 1952, 15:285-295.
61. Sanz B., Palacios P., Lopez P., Ordogez J.A. Effect of ultrasonic waves on the heat resistance of Bacillus stearothermophilus spores. Fundamental and applied aspects of bacterial spores 1985, 251-259. Academic Press, London. G.J. Dring, D.J. Ellar, G.W. Gould (Eds.).
62. Schoeni J.L. Bacillus cereus food poisoning and its toxins. Journal of Food Protection 2005, 68:636-648.
63. Senhaji A.F., Loncin M. The protective effect of fat on the heat resistance of bacteria. International Journal of Food Science & Technology 1977, 12:203-216.
64. Shehata T.E., Collins E.B. Sporulation and heat resistance of psychrophilic strains of Bacillus. Journal of Dairy Science 1973, 55:1405-1409.
65. Sierra G., Boucher R.M. Ultrasonic synergistic effects in liquid-phase chemical sterilization. Applied Microbiology 1971, 22:160-164.
66. Silva F.M., Gibbs P., Vieira M.C., Silva C.L.M. Thermal inactivation of Alicyclobacillus acidoterrestris spores under different temperature, soluble solids and pH conditions for the design of fruit processes. International Journal of Food Microbiology 1999, 51:95-103.
67. Silva F.V.M., Gibbs P.A. Non-proteolytic Clostridium botulinum spores in low-acid cold-distributed foods and design of pasteurization processes. Trends in Food Science and Technology 2010, 21:95-105.
68. Silva F.V.M., Gibbs P.A., Nunez H., Almonacid S., Simpson R. Thermal processes: Pasteurization. Encyclopedia of food microbiology 2014, 577-595. Elsevier, Amsterdam. C.A. Batt, M.L. Tortorello (Eds.).
69. Slaten D.D., Oropeza R.I., Werner S.B. An outbreak of Bacillus cereus food poisoning-Are caterers supervised sufficiently. Public Health Reports 1992, 107:477.
70. Stumbo C.R. Thermal resistance of bacteria. Thermobacteriology in food processing 1965, 79-104. Academic Press Inc., New York. M.L. Anson, E.M. Mark, C.O. Chichestor, G.F. Stewart (Eds.).
71. USFDA Bad bug book: Foodborne pathogenic microorganisms and natural toxins handbook 2012, (http://www.fda.gov/food/foodborneillnesscontaminants/causesofillnessbadbugbook/default.htm. Accessed 28 March 2014). 2nd ed.
72. USFDA Bacteriological Analytical Manual (BAM): Bacillus cereus (Chapter 14), (Accessed 25 March 2014). http://www.fda.gov/food/foodscienceresearch/laboratorymethods/ucm070875.htm.
73. Valero M., Hernandez-Herrero L., Giner M. Survival, isolation and characterization of a psychrotrophic Bacillus cereus strain from a mayonnaise-based ready-to-eat vegetable salad. Food Microbiology 2007, 24:671-677.
74. Villamiel M., Hamersveld V., De Jong P. Review: Effect of ultrasound processing on the quality of dairy products. Milchwissenschaft 1999, 54:69-73.
75. Wimalaratne S.K. Pressure assisted thermal sterilization: A novel means of processing foods 2009, (PhD Thesis), The University of Auckland, New Zealand.
76. Wu T.Y., Guo N., Teh C.Y., Hay J.X.W. Theory and fundamentals of ultrasound. Advances in ultrasound technology for environmental remediation 2013, 5-11. Springer, New York.