High pressure inactivation of Clostridium botulinum type E endospores in model emulsion systemsFootnote

^†This paper was presented at the 8th International Conference on High Pressure Bioscience & Biotechnology (HPBB 2014), in Nantes (France), 15-18 July 2014.

References

• Arnon SS, Schechter R, Inglesby TV, Henderson DA, Bartlett JG, Ascher MS, Eitzen E, Fine AD, Hauer J, Layton M, Lillibridge S, Osterholm MT, O'Toole T, Parker G, Perl TM, Russell PK, Swerdlow DL, Tonat K. Botulinum toxin as a biological weapon. Jama-J Am Med Assoc. 2001;285:1059–1070. doi: 10.1001/jama.285.8.1059
   PubMed Web of Science ®Google Scholar
• MacDonald TE, Helma CH, Shou Y, Valdez YE, Ticknor LO, Foley BT, Davis SW, Hannett GE, Kelly-Cirino CD, Barash JR, Arnon SS, Lindström M, Korkeala H, Smith LA, Smith TJ, Hill KK. Analysis of Clostridium botulinum serotype E strains by using multilocus sequence typing, amplified fragment length polymorphism, variable-number tandem-repeat analysis, and botulinum neurotoxin gene sequencing. Appl Environ Microbiol. 2011;77:8625–8634. doi: 10.1128/AEM.05155-11
   PubMed Web of Science ®Google Scholar
• Considine KM, Kelly AL, Fitzgerald GF, Hill C, Sleator RD. High-pressure processing – effects on microbial food safety and food quality. Fems Microbiol Lett. 2008;281:1–9. doi: 10.1111/j.1574-6968.2008.01084.x
   PubMed Web of Science ®Google Scholar
• Sale JH, Gould GW, Hamilton WA. Mechanisms of induction of germination of Bacillus subtilis spores by high pressure. J Gen Microbiol. 1970;60:323–334. doi: 10.1099/00221287-60-3-323
   PubMedGoogle Scholar
• Serment-MorenoV, Barbosa-Cánovas G, Torres JA, Welti-Chanes J. High-pressure processing: kinetic models for microbial and enzyme inactivation. Food Eng Rev. 2014;6:56–88. doi: 10.1007/s12393-014-9075-x
   Web of Science ®Google Scholar
• Simpson RK, Gilmour A. The effect of high hydrostatic pressure on Listeria monocytogenes in phosphate-buffered saline and model food systems. J Appl Microbiol. 1997;83:181–188. doi: 10.1046/j.1365-2672.1997.00215.x
   PubMed Web of Science ®Google Scholar
• Miller RJ. Verteilung und Inaktivierung von Mikroorganismen in binären Systemen (Öl-in-Wasser-Emulsionen) [dissertation]. Freising: Technischen Universität München/Weihenstephan; 2006.
   Google Scholar
• Morales P, Calzada J, Rodríguez B, de Paz M, Gaya P, Nuñez M. Effect of cheese water activity and carbohydrate content on the barotolerance of Listeria monocytogenes scott A. J Food Protect. 2006;69:1328–1333.
   PubMed Web of Science ®Google Scholar
• Ananta E, Heinz V, Schlüter O, Knorr D. Kinetic studies on high pressure inactivation of Bacillus stearothermophilus spores suspended in cocoa mass and broccoli. IFSET. 2001;2:261–272.
   Google Scholar
• Molin M, Snygg BG. Effect of lipid materials on heat resistance of bacterial spores. Appl Microbiol. 1967;15:1422–1426.
   PubMedGoogle Scholar
• Senhaji AF, Loncin M. The protective effect of fat on the heat resistance of bacteria (I)*. Int J Food Sci Tech. 1977;12:203–216. doi: 10.1111/j.1365-2621.1977.tb00102.x
   Google Scholar
• Senhaji AF. The protective effect of fat on the heat resistance of bacteria (II). Int J Food Sci Tech. 1977;12:217–230. doi: 10.1111/j.1365-2621.1977.tb00103.x
   Google Scholar
• Ababouch LH, Grimit L, Eddafry R, Busta FF. Thermal inactivation kinetics of Bacillus subtilis spores suspended in buffer and in oils. J Appl Bacteriol. 1995;78:669–676. doi: 10.1111/j.1365-2672.1995.tb03114.x
   PubMedGoogle Scholar
• Lekogo BM, Coroller L, Mathot AG, 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. Int J Food Microbiol. 2010;141:242–247. doi: 10.1016/j.ijfoodmicro.2010.05.023
   PubMed Web of Science ®Google Scholar
• Lenz CA, Vogel RF. Effect of sporulation medium and its divalent cation content on the heat and high pressure resistance of Clostridium botulinum type E spores. Food Microbiol. 2014;44:156–167. doi: 10.1016/j.fm.2014.05.010
   PubMed Web of Science ®Google Scholar
• Yang WW, Crow-Willard EN, Ponce A. Production and characterization of pure Clostridium spore suspensions. J Appl Microbiol. 2009;106:27–33. doi: 10.1111/j.1365-2672.2008.03931.x
   PubMed Web of Science ®Google Scholar
• Lerche D, Sobisch T, Detloff T. Determination of stability, consolidation and particle size distribution of liquid or semi-liquid food products by multisample analytical centrifugation. In: Fischer P, Erni P, Windhab EJ, editors. Proceedings 4th international symposium on food rheology and structure (ISFRS); 2006 Feb 19–26; Zürich, Switzerland. Zürich: Laboratory of Food Process Engineering; 2006.
   Google Scholar
• Badolato GG, Aguilar F, Schuchmann HP, Sobisch T, Lerche D. Evaluation of long term stability of model emulsions by multisample analytical centrifugation. Prog Coll Pol Sci S. 2008;134:66–73.
   Google Scholar
• Laflamme C, Lavigne S, Ho J, Duchaine C. Assessment of bacterial endospore viability with fluorescent dyes. J Appl Microbiol. 2004;96:684–692. doi: 10.1111/j.1365-2672.2004.02184.x
   PubMed Web of Science ®Google Scholar
• Knoerzer K, Buckow R, Versteeg C. Adiabatic compression heating coefficients for high-pressure processing – a study of some insulating polymer materials. J Food Eng. 2010;98:110–119. doi: 10.1016/j.jfoodeng.2009.12.016
   Web of Science ®Google Scholar
• Dickinson E, James JD. Rheology and flocculation of high-pressure-treated β-Lactoglobulin-stabilized emulsions: comparison with thermal treatment. J Agr Food Chem. 1998;46:2565–2571. doi: 10.1021/jf971096s
   Web of Science ®Google Scholar
• Anton M, Chapleau N, Beaumal V, Delépine S, de Lamballerie-Anton M. Effect of high-pressure treatment on rheology of oil-in-water emulsions prepared with hen egg yolk. Innov Food Sci Emerg. 2001;2:9–21. doi: 10.1016/S1466-8564(00)00036-9
   Google Scholar
• van de Ven C, Courvoisier C, Matser A. High pressure versus heat treatments for pasteurisation and sterilisation of model emulsions. Innov Food Sci Emerg Technol. 2007;8:230–236. doi: 10.1016/j.ifset.2006.12.001
   Web of Science ®Google Scholar
• Zhu X, Ye A, Teo HJ, Lim SJ, Singh S. Oxidative stability of fish oil-in-water emulsions under high-pressure treatment. Int J Food Sci Tech. 2014;49:1441–1448. doi: 10.1111/ijfs.12462
   Web of Science ®Google Scholar
• Karbstein H, Schubert H, Scigalla W, Ludwig, H. Sterilization of emulsions by means of high pressure. In: Blany C, Hayashi R, Hermans K, Masson P, editors. High pressure and biotechnology. London: John Libbey Eurotext; 1992. p. 345–347.
   Google Scholar
• Koshikawa T, Yamazaki M, Yoshimi M, Ogawa S, Yamada A, Watabe K, Torii M. Surface hydrophobicity of spores of Bacillus spp. J Gen Microbiol. 1989;135:2717–2722.
   PubMedGoogle Scholar
• Andersson A, Rönner U. Adhesion and removal of dormant, heat-activated, and germinated spores of three strains of Bacillus cereus. Biofouling. 1998;13:51–67. doi: 10.1080/08927019809378370
   Web of Science ®Google Scholar
• Wiencek KM, Klapes NA, Foegeding PM. Hydrophobicity of Bacillus and Clostridium spores. Appl Environ Microb. 1990;56:2600–2605.
   PubMed Web of Science ®Google Scholar
• Husmark U, Rönner U. The influence of hydrophobic, electrostatic and morphologic properties on the adhesion of Bacillus spores. Biofouling. 1992;5:335–344.
   Google Scholar
• Husmark U. Adhesion mechanisms of bacterial spores to solid surfaces [dissertation]. Göteborg: Chalmers University of Technology; 1993.
   Google Scholar
• Matz LL, Beaman TC, Gerhardt P. Chemical composition of exosporium from spores of Bacillus cereus. J Bacteriol. 1970;101:196–201.
   PubMed Web of Science ®Google Scholar
• Takumi K, Kinouchi T, Kawata T. Isolation and partial characterization of exosporium from spores of a highly sporogenic mutant of Clostridium botulinum type A. Microbiol Immunol. 1979;23:443–454. doi: 10.1111/j.1348-0421.1979.tb00484.x
   PubMed Web of Science ®Google Scholar
• Doyle RJ, Haiem-Nedjat F, Singh JS. Hydrophobic characteristics of Bacillus spores. Curr Microbiol. 1984;10:329–332. doi: 10.1007/BF01626560
   Web of Science ®Google Scholar
• Elowitz RB, Levine AJ, Siggia ED, Swain PS. Stochastic gene expression in a single cell. Science. 2002;297:1183–1186. doi: 10.1126/science.1070919
   PubMed Web of Science ®Google Scholar
• Melly E, Genest PC, Gilmore ME, Little S, Popham DL, Driks A, Setlow P. Analysis of the properties of spores of Bacillus subtilis prepared at different temperatures. Appl Environ Microb. 2002;92:1105–1115. doi: 10.1046/j.1365-2672.2002.01644.x
   Web of Science ®Google Scholar
• Margosch D, Gänzle MG, Ehrmann MA, Vogel RF. Pressure Inactivation of Bacillus Endospores. Appl Environ Microb. 2004;70:7321–7328. doi: 10.1128/AEM.70.12.7321-7328.2004
   PubMed Web of Science ®Google Scholar
• Hornstra LM, Beek AT, Smelt JP, Kallemeijn WW, Brul S. On the origin of heterogeneity in (preservation) resistance of Bacillus spores: input for a ‘systems’ analysis approach of bacterial spore outgrowth. Int J Food Microbiol. 2009;134:9–15. doi: 10.1016/j.ijfoodmicro.2009.02.011
   PubMed Web of Science ®Google Scholar
• Stecchini ML, Spaziani M, Del Torre M, Pacor S. Bacillus cereus cell and spore properties as influenced by the micro-structure of the medium. Appl Environ Microb. 2009;106:1838–1848. doi: 10.1111/j.1365-2672.2009.04162.x
   Web of Science ®Google Scholar
• Setlow P, Liu J, Faeder JR. Chapter 12: Heterogeneity in bacterial spore populations. In: Abel-Santos E, editor. Bacterial spores: current research and applications. Norfolk: Caister Academic Press; 2012. p. 199–214.
   Google Scholar
• Hodgkiss M, Ordal ZJ. Morphology of the spore of some strains of Clostridium botulinum type E. J Bacteriol. 1996;91:2031–2036.
   Google Scholar
• Escobar-Cortes K, Barra-Carrasco J, Paredes-Sabja D. Proteases and sonication specifically remove the exosporium layer of spores of Clostridium difficile strain 630. J Microbiol Method. 2013;93:25–31. doi: 10.1016/j.mimet.2013.01.016
   PubMed Web of Science ®Google Scholar
• Shigemoto M, Nakagawa K, Sakamoto JJ, Tsuchidoi T. Thermal death of Bacillus subtilis spores in oil-water systems. Biocontrol Sci. 2010;15:27–31. doi: 10.4265/bio.15.27
   PubMed Web of Science ®Google Scholar
• Gao YL, Ju XR. Modelling the effects of food ingredients and pH on high-pressure processing inactivation of Bacillus cereus spores: a laboratorial study. Int J Food Sci Technol. 2010;45:1862–1869. doi: 10.1111/j.1365-2621.2010.02350.x
   Web of Science ®Google Scholar
• Setlow P. Chapter 2: Germination of spores of Bacillus subtilis by high pressure. In: Doona CJ, Dunne CP, Florence EF, editors. High pressure processing of food. Chicago: IFT Press; 2007. p. 15–40.
   Google Scholar
• Paredes-Sabja D, Setlow P, Sarker MR. Germination of spores of Bacillales and Clostridiales species: mechanisms and proteins involved. Trends Microbiol. 2011;19:85–94. doi: 10.1016/j.tim.2010.10.004
   PubMed Web of Science ®Google Scholar
• Sarker MR, Akhtar S, Torres JA, Paredes-Sabja D. High hydrostatic pressure-induced inactivation of bacterial spores. Crit Rev Microbiol. Epub 2013 Apr 30.
   Google Scholar
• Dodds KL, Austin JW. Chapter 15: Clostridium botulinum. In: Doyle MP, Beuchat LR, Montville TJ, editors. Food microbiology: fundamentals and frontiers. Washington (DC): ASM Press; 1997. p. 228–304.
   Google Scholar
• Ting E, Balasubramaniam VM, Raghubeer E. Determining thermal effects in high pressure processing. Food Technol. 2002;56:31–35.
   Web of Science ®Google Scholar