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Annual Review of Food Science and Technology

Volume 9, 2018

Natural Diversity in Heat Resistance of Bacteria and Bacterial Spores: Impact on Food Safety and Quality

Abstract

Heat treatments are widely used in food processing often with the aim of reducing or eliminating spoilage microorganisms and pathogens in food products. The efficacy of applying heat to control microorganisms is challenged by the natural diversity of microorganisms with respect to their heat robustness. This review gives an overview of the variations in heat resistances of various species and strains, describes modeling approaches to quantify heat robustness, and addresses the relevance and impact of the natural diversity of microorganisms when assessing heat inactivation. This comparison of heat resistances of microorganisms facilitates the evaluation of which (groups of) organisms might be troublesome in a production process in which heat treatment is critical to reducing the microbial contaminants, and also allows fine-tuning of the process parameters. Various sources of microbiological variability are discussed and compared for a range of species, including spore-forming and non-spore-forming pathogens and spoilage organisms. This benchmarking of variability factors gives crucial information about the most important factors that should be included in risk assessments to realistically predict heat inactivation of bacteria and spores as part of the measures for controlling shelf life and safety of food products.

Keyword(s): D-value, pathogens, spoilage organisms, thermotolerance, variability, z-value
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2018-03-25
2024-04-23
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Literature Cited

  1. Ababouch L, Grimit L, Eddafry R, Busta F. 1995. Thermal inactivation kinetics of Bacillus subtilis spores suspended in buffer and in oils. J. Appl. Bacteriol. 78:6669–76 [Google Scholar]
  2. Abee T, Koomen J, Metselaar KI, Zwietering MH, den Besten HMW. 2016. Impact of pathogen population heterogeneity and stress-resistant variants on food safety. Annu. Rev. Food Sci. Technol. 7:439–56 [Google Scholar]
  3. Abhyankar W, Pandey R, Ter Beek A, Brul S, De Koning LJ, De Koster CG. 2015. Reinforcement of Bacillus subtilis spores by cross-linking of outer coat proteins during maturation. Food Microbiol 45:Pt. A54–62 [Google Scholar]
  4. André S, Zuber F, Remize F. 2013. Thermophilic spore-forming bacteria isolated from spoiled canned food and their heat resistance. Results of a French ten-year survey Int. J. Food Microbiol. 165:134–43 [Google Scholar]
  5. Aryani DC, den Besten HMW, Hazeleger WC, Zwietering MH. 2015. Quantifying variability and the effect of growth history on thermal resistance of Listeria monocytogenes. Int. J. Food Microbiol. 193:130–38 [Google Scholar]
  6. Aryani DC, den Besten HMW, Zwietering MH. 2016. Quantifying variability in growth and thermal inactivation kinetics of Lactobacillus plantarum. Appl. Environ. Microbiol. 82:164896–908 [Google Scholar]
  7. Ates MB, Skipnes D, Rode TM, Lekang OI. 2016. Comparison of spore inactivation with novel agitating retort, static retort and combined high pressure–temperature treatments. Food Control 60:484–92 [Google Scholar]
  8. Barbosa-Cánovas GV. 2005. Novel Food Processing Technologies Boca Raton, Fla: CRC Press
  9. Beaman TC, Gerhardt P. 1986. Heat resistance of bacterial spores correlated with protoplast dehydration, mineralization, and thermal adaptation. Appl. Environ. Microbiol. 52:61242–46 [Google Scholar]
  10. Beaman TC, Greenamyre JT, Corner TR, Pankratz HS, Gerhardt P. 1982. Bacterial spore heat resistance correlated with water content, wet density, and protoplast/sporoplast volume ratio. J. Bacteriol. 150:2870–77 [Google Scholar]
  11. Bean D, Bourdichon F, Bresnahan D, Davies A, Geeraerd A. et al. 2012. Risk assessment approaches to setting thermal processes in food manufacture ILSI Eur. Rep. Ser., ILSI Brussels, Belg:
  12. Berendsen EM, Boekhorst J, Kuipers OP, Wells-Bennik MHJ. 2016.a A mobile genetic element profoundly increases heat resistance of bacterial spores. ISME J 10:2633–42 [Google Scholar]
  13. Berendsen EM, Koning RA, Boekhorst J, de Jong A, Kuipers OP, Wells-Bennik MHJ. 2016.b High-level heat resistance of spores of Bacillus amyloliquefaciens and Bacillus licheniformis results from the presence of a spoVA operon in a Tn1546 transposon. Front. Microbiol. 7:1912 [Google Scholar]
  14. Berendsen EM, Zwietering MH, Kuipers OP, Wells-Bennik MHJ. 2015. Two distinct groups within the Bacillus subtilis group display significant different spore heat resistance properties. Food Microbiol 45:18–25 [Google Scholar]
  15. Bhattacharya S. 2014. Conventional and Advanced Food Processing Technologies Somerset, UK: Wiley
  16. Briggs A. 1966. The resistances of spores of the genus Bacillus to phenol, heat and radiation. J. Appl. Bacteriol. 29:3490–504 [Google Scholar]
  17. Briggs A, Yazdany S. 1970. Effect of sodium chloride on the heat and radiation resistance and on the recovery of heated or irradiated spores of the genus Bacillus. J. Appl. Bacteriol. 33:4621–32 [Google Scholar]
  18. Butler RR 3rd, Schill KM, Wang Y, Pombert JF. 2017. Genetic characterization of the exceptionally high heat resistance of the non-toxic surrogate Clostridium sporogenes PA 3679. Front. Microbiol. 8:545 [Google Scholar]
  19. Cazemier AE, Wagenaars SFM, Ter Steeg PF. 2001. Effect of sporulation and recovery medium on the heat resistance and amount of injury of spores from spoilage bacilli. J. Appl. Microbiol. 90:761–70 [Google Scholar]
  20. Cerf O. 1977. Tailing of survival curves of bacterial spores. J. Appl. Bacteriol. 42:1–19 [Google Scholar]
  21. Checinska A, Paszczynski A, Burbank M. 2015. Bacillus and other spore-forming genera: variations in responses and mechanisms for survival. Annu. Rev. Food Sci. Technol. 6:351–69 [Google Scholar]
  22. Cho HY, Yousef AE, Sastry SK. 1999. Kinetics of inactivation of Bacillus subtilis spores by continuous or intermittent ohmic and conventional heating. Biotechnol. Bioeng. 62:3368–72 [Google Scholar]
  23. Condon S, Bayarte M, Sala FJ. 1992. Influence of the sporulation temperature upon the heat resistance of Bacillus subtilis. J. Appl. Bacteriol. 73:3251–56 [Google Scholar]
  24. Condon S, Lopez P, Oria R, Sala FJ. 1989. Thermal death determination: design and evaluation of a thermoresistometer. J. Food Sci. 54:2451–57 [Google Scholar]
  25. Condón S, Palop A, Raso J, Sala FJ. 1996. Influence of the incubation temperature after heat treatment upon the estimated heat resistance values of spores of Bacillus subtilis. Lett. Appl. Microbiol. 22:2149–52 [Google Scholar]
  26. Conesa R, Periago PM, Esnoz A, López A, Palop A. 2003. Prediction of Bacillus subtilis spore survival after a combined non-isothermal-isothermal heat treatment. Eur. Food Res. Technol. 217:4319–24 [Google Scholar]
  27. Coton M, Denis C, Cadot P, Coton E. 2011. Biodiversity and characterization of aerobic spore-forming bacteria in surimi seafood products. Food Microbiol 28:2252–60 [Google Scholar]
  28. den Besten HMW, Berendsen EM, Wells-Bennik MHJ, Straatsma H, Zwietering MH. 2017. Two complementary approaches to quantify variability in heat resistance of spores of Bacillus subtilis. Int. J. Food Microbiol. 253:48–53 [Google Scholar]
  29. den Besten HMW, Mataragas M, Moezelaar R, Abee T, Zwietering MH. 2006. Quantification of the effects of salt stress and physiological state on thermotolerance of Bacillus cereus ATCC 10987 and ATCC 14579. Appl. Environ. Microbiol. 72:95884–94 [Google Scholar]
  30. den Besten HMW, Van der Mark EJ, Hensen L, Abee T, Zwietering MH. 2010. Quantification of the effect of culturing temperature on salt-induced heat resistance of Bacillus species. Appl. Environ. Microbiol. 76:134286–92 [Google Scholar]
  31. den Besten HMW, Zwietering MH. 2012. Meta-analysis for quantitative microbiological risk assessments and benchmarking data. Trends Food Sci. Technol. 25:134–39 [Google Scholar]
  32. Diao MM, André S, Membré JM. 2014. Meta-analysis of D-values of proteolytic Clostridium botulinum and its surrogate strain Clostridium sporogenes PA 3679. Int. J. Food Microbiol. 174:23–30 [Google Scholar]
  33. Eijlander RT, De Jong A, Krawczyk AO, Holsappel S, Kuipers OP. 2014. SporeWeb: an interactive journey through the complete sporulation cycle of Bacillus subtilis. Nucleic Acids Res 42:D1D685–91 [Google Scholar]
  34. Eijlander RT, Holsappel S, de Jong A, Ghosh A, Christie G, Kuipers OP. 2016. SpoVT: From fine-tuning regulator in Bacillus subtilis to essential sporulation protein in Bacillus cereus. Front. Microbiol 7:1607 [Google Scholar]
  35. Esteban MD, Conesa R, Huertas JP, Palop A. 2015. Effect of thymol in heating and recovery media on the isothermal and non-isothermal heat resistance of Bacillus spores. Food Microbiol 48:35–40 [Google Scholar]
  36. FDA/CFSAN. 2000. Kinetics of Microbial Inactivation for Alternative Food Processing Technologies Washington, DC: FDA https://www.fda.gov/downloads/Food/FoodborneIllnessContaminants/UCM545175.pdf
  37. Fellows PJ. 2016. Food Processing Technology. Principles and Practice Cambridge, UK: Woodhead Publ 4th ed
  38. Fox K, Eder BD. 1969. Comparison of survivor curves of Bacillus subtilis spores subjected to wet and dry heat. J. Food Sci. 34:6518–21 [Google Scholar]
  39. Geeraerd AH, Herremans CH, Van Impe JF. 2000. Structural model requirements to describe microbial inactivation during a mild heat treatment. Int. J. Food Microbiol. 59:185–209 [Google Scholar]
  40. Geeraerd AH, Valdramidis VP, Van Impe JF. 2005. GInaFiT, a freeware tool to assess non-log-linear microbial survivor curves. Int. J. Food Microbiol. 102:95–105. Erratum. 2016. Int. J. Food Microbiol 110:297–97 [Google Scholar]
  41. Georget E, Miller B, Aganovic K, Callanan M, Heinz V, Mathys A. 2014. Bacterial spore inactivation by ultra-high pressure homogenization. Innov. Food Sci. Emerg. Technol. 26:116–23 [Google Scholar]
  42. Gómez-Jódar I, Ros-Chumillas M, Palop A. 2015. Effect of heating rate on highly heat-resistant spore-forming microorganisms. Food Sci. Technol. Int. 22:2164–72 [Google Scholar]
  43. Gonzales-Barron U, Butler F. 2011. The use of meta-analytical tools in risk assessment for food safety. Food Microbiol 28:823–27 [Google Scholar]
  44. Guinebretière MH, Thompson FL, Sorokin A, Normand P, Dawyndt P. et al. 2008. Ecological diversification in the Bacillus cereus group. Environ. Microbiol. 10:851–65 [Google Scholar]
  45. Gunasekera TS, Csonka LN, Paliy O. 2008. Genome-wide transcriptional responses of Escherichia coli K-12 to continuous osmotic and heat stresses. J. Bacteriol. 190:103712–20 [Google Scholar]
  46. Gurtler JB, Hinton A Jr, Bailey RB, Cray WC Jr, Meinersmann RJ. et al. 2015. Salmonella isolated from ready-to-eat pasteurized liquid egg products: thermal resistance, biochemical profile, and fatty acid analysis. Int. J. Food Microbiol. 206:109–17 [Google Scholar]
  47. Härnulv B, Snygg B. 1972. Heat resistance of Bacillus subtilis spores at various water activities. J. Appl. Bacteriol. 35:4615–24 [Google Scholar]
  48. Hayrapetyan H, Boekhorst J, De Jong A, Kuipers OP, Nierop Groot MN, Abee T. 2016. Draft whole-genome sequences of 11 Bacillus cereus food isolates. Genome Announc 4:3e00485–16 [Google Scholar]
  49. Jagannath A, Tsuchido T. 2003. Validation of a polynomial regression model: the thermal inactivation of Bacillus subtilis spores in milk. Lett. Appl. Microbiol. 37:5399–404 [Google Scholar]
  50. Jagannath A, Tsuchido T, Membré JM. 2005. Comparison of the thermal inactivation of Bacillus subtilis spores in foods using the modified Weibull and Bigelow equations. Food Microbiol 22:2–3233–39 [Google Scholar]
  51. Janštová B, Lukášová J. 2001. Heat resistance of Bacillus spp. spores isolated from cow's milk and farm environment. Acta Vet. BRNO 70:2179–84 [Google Scholar]
  52. Jongenburger I, Bassett J, Jackson T, Gorris LGM, Jewell K, Zwietering MH. 2012. Impact of microbial distributions on food safety II. Quantifying impacts on public health and sampling. Food Control 26:546–54 [Google Scholar]
  53. Karatzas KA, Wouters JA, Gahan CG, Hill C, Abee T, Bennik MHJ. 2003. The CtsR regulator of Listeria monocytogenes contains a variant glycine repeat region that affects piezotolerance, stress resistance, motility and virulence. Mol. Microbiol. 49:51227–38 [Google Scholar]
  54. Khoury PH, Lombardi SJ, Slepecky RA. 1987. Perturbation of the heat resistance of bacterial spores by sporulation temperature and ethanol. Curr. Microbiol. 15:115–19 [Google Scholar]
  55. Khoury PH, Qoronfleh MW, Streips UN, Slepecky RA. 1990. Altered heat resistance in spores and vegetative cells of a mutant from Bacillus subtilis. Curr. Microbiol. 21:4249–53 [Google Scholar]
  56. Kort R, O'Brien AC, Van Stokkum IH, Oomes SJ, Crielaard W. et al. 2005. Assessment of heat resistance of bacterial spores from food product isolates by fluorescence monitoring of dipicolinic acid release. Appl. Environ. Microbiol. 71:73556–64 [Google Scholar]
  57. Krawczyk AO, De Jong A, Eijlander RT, Berendsen EM, Holsappel S. et al. 2015. Next-generation whole-genome sequencing of eight strains of Bacillus cereus, isolated from food. Genome Announc 3:6e01480–15 [Google Scholar]
  58. Lechowich R, Ordal ZJ. 1965. The influence of the sporulation temperature on the heat resistance and chemical composition of bacterial spores. Can. J. Microbiol. 8:3287–95 [Google Scholar]
  59. Lenz CA, Vogel RF. 2015. Differential effects of sporulation temperature on the high pressure resistance of Clostridium botulinum type E spores and the interconnection with sporulation medium cation contents. Food Microbiol 46:434–42 [Google Scholar]
  60. Li H, Xie G, Edmondson A. 2007. Evolution and limitations of primary models in predictive microbiology. Br. Food J. 109:608–26 [Google Scholar]
  61. Lianou A, Koutsoumanis KP. 2011. Effect of the growth environment on the strain variability of Salmonella enterica kinetic behavior. Food Microbiol 28:828–37 [Google Scholar]
  62. Lianou A, Koutsoumanis KP. 2013. Evaluation of the strain variability of Salmonella enterica acid and heat resistance. Food Microbiol 34:259–67 [Google Scholar]
  63. Lima LJR, Kamphuis HJ, Nout MJR, Zwietering MH. 2011. Microbiota of cocoa powder with particular reference to aerobic thermoresistant spore-formers. Food Microbiol 28:3573–82 [Google Scholar]
  64. Lücking G, Stoeckel M, Atamer Z, Hinrichs J, Ehling-Schulz M. 2013. Characterization of aerobic spore-forming bacteria associated with industrial dairy processing environments and product spoilage. Int. J. Food Microbiol. 166:2270–79 [Google Scholar]
  65. Luu-Thi H, Khadka DB, Michiels CW. 2014. Thermal inactivation parameters of spores from different phylogenetic groups of Bacillus cereus. Int. J. Food Microbiol. 189:183–88 [Google Scholar]
  66. Ma L, Zhang G, Gerner-Smidt P, Mantripragada V, Ezeoke I, Doyle MP. 2009. Thermal inactivation of Salmonella in peanut butter. J. Food Prot. 72:81596–601 [Google Scholar]
  67. Mafart P, Couvert O, Gaillard S, Leguerinel I. 2002. On calculating sterility in thermal preservation methods: application of the Weibull frequency distribution model. Int. J. Food Microbiol. 72:107–13 [Google Scholar]
  68. Melly E, Genest PC, Gilmore ME, Little S, Popham DL. et al. 2002. Analysis of the properties of spores of Bacillus subtilis prepared at different temperatures. J. Appl. Microbiol. 92:1105–15 [Google Scholar]
  69. Melly E, Setlow P. 2001. Heat shock proteins do not influence wet heat resistance of Bacillus subtilis spores. J. Bacteriol. 183:2779–84 [Google Scholar]
  70. Membré JM. 2016. Microbiological risk assessments in food industry. Food Hygiene and Toxicology in Ready-to-Eat Foods P Kotzekidou 337–50 Cambridge, MA: Acad. Press [Google Scholar]
  71. Membré JM, Amézquita A, Bassett J, Giavedoni P, de W Blackburn C, Gorris LGM. 2006. A probabilistic modeling approach in thermal inactivation: estimation of postprocess Bacillus cereus spore prevalence and concentration. J. Food Prot. 69:1118–29 [Google Scholar]
  72. Mercer RG, Walker BD, Yang X, McMullen LM, Gänzle MG. 2017. The locus of heat resistance (LHR) mediates heat resistance in Salmonella enterica, Escherichia coli and Enterobacter cloacae. Food Microbiol 64:96–103 [Google Scholar]
  73. Mercer RG, Zheng J, Garcia-Hernandez R, Ruan L, Gänzle MG, McMullen LM. 2015. Genetic determinants of heat resistance in Escherichia coli. Front. Microbiol. 6:932 [Google Scholar]
  74. Metselaar KI, Abee T, Zwietering MH, den Besten HMW. 2016. Modeling and validation of the ecological behavior of wild-type Listeria monocytogenes and stress-resistant variants. Appl. Environ. Microbiol. 82:175389–401 [Google Scholar]
  75. Metselaar KI, den Besten HMW, Abee T, Moezelaar R, Zwietering MH. 2013. Isolation and quantification of highly resistant variants of Listeria monocytogenes. Int. J. Food Microbiol. 166:508–14 [Google Scholar]
  76. Miller FA, Ramos B, Gil MM, Brandão TRS, Teixeira P, Silva CLM. 2009. Influence of pH, type of acid and recovery media on the thermal inactivation of Listeria innocua. Int. J. Food Microbiol. 133:1–2121–28 [Google Scholar]
  77. Molin N, Snygg BG. 1967. Effect of lipid materials on heat resistance of bacterial spores. Appl. Microbiol. 15:61422–26 [Google Scholar]
  78. Movahedi S, Waites W. 2000. A two-dimensional protein gel electrophoresis study of the heat stress response of Bacillus subtilis cells during sporulation. J. Bacteriol. 182:174758–63 [Google Scholar]
  79. Nakayama A, Yano Y, Kobayashi S, Ishikawa M, Sakai K. 1996. Comparison of pressure resistances of spores of six Bacillus strains with their heat resistances. Appl. Environ. Microbiol. 62:103897–900 [Google Scholar]
  80. Nguyen Thi Minh H, Durand A, Loison P, Perrier-Cornet J-M, Gervais P. 2011. Effect of sporulation conditions on the resistance of Bacillus subtilis spores to heat and high pressure. Appl. Microbiol. Biotechnol. 90:1409–17 [Google Scholar]
  81. Odlaug TE, Caputo RA, Graham GS. 1981. Heat resistance and population stability of lyophilized Bacillus subtilis spores. Appl. Environ. Microbiol. 41:61374–77 [Google Scholar]
  82. Peck MW, Van Vliet AH. 2016. Impact of Clostridium botulinum genomic diversity on food safety. Curr. Opin. Food Sci. 10:52–59 [Google Scholar]
  83. Penna TCV, Marques M, Machoshvili IA, Ishii M. 2002. The effect of composition of parenteral solution on the thermal resistance of Bacillus stearothermophilus and Bacillus subtilis spores. Appl. Biochem. Biotechnol. 98:1539–51 [Google Scholar]
  84. Put H, Aalbersberg W. 1967. Occurrence of Bacillus subtilis with high heat resistance. J. Appl. Bacteriol. 30:3411–19 [Google Scholar]
  85. Reineke K, Mathys A, Knorr D. 2011. The impact of high pressure and temperature on bacterial spores: inactivation mechanisms of Bacillus subtilis above 500 MPa. J. Food Sci. 76:3M189–97 [Google Scholar]
  86. Reineke K, Schottroff F, Meneses N, Knorr D. 2015. Sterilization of liquid foods by pulsed electric fields: an innovative ultra-high temperature process. Front. Microbiol. 6:400 [Google Scholar]
  87. Rigaux C, Denis JB, Albert I, Carlin F. 2013. 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 pH 7, zT and zpH of Geobacillus stearothermophilus. Int. J. Food Microbiol. 61:2112–20 [Google Scholar]
  88. Rodriguez J, Cousin M, Nelson P. 1993. Thermal resistance and growth of Bacillus licheniformis and Bacillus subtilis in tomato juice. J. Food Prot. 56:2165–68 [Google Scholar]
  89. Rose R, Setlow B, Monroe A, Mallozzi M, Driks A, Setlow P. 2007. Comparison of the properties of Bacillus subtilis spores made in liquid or on agar plates. J. Appl. Microbiol. 103:3691–99 [Google Scholar]
  90. Sala FJ, Ibarz P, Palop A, Raso J, Condon S. 1995. Sporulation temperature and heat resistance of Bacillus subtilis at different pH values. J. Food Prot. 58:3239–43 [Google Scholar]
  91. Sanchez-Salas J-L, Setlow B, Zhang P, Li Y-Q, Setlow P. 2011. Maturation of released spores is necessary for acquisition of full spore heat resistance during Bacillus subtilis sporulation. Appl. Environ. Microbiol. 77:196746–54 [Google Scholar]
  92. Schill KM, Wang Y, Butler RR 3rd, Pombert JF, Reddy NR. et al. 2015. Genetic diversity of Clostridium sporogenes PA 3679 isolates obtained from different sources as resolved by pulsed-field gel electrophoresis and high-throughput sequencing. Appl. Environ. Microbiol. 82:1384–93 [Google Scholar]
  93. Schumann W. 2016. Regulation of bacterial heat shock stimulons. Cell Stress Chaperones 21:6959–68 [Google Scholar]
  94. Senhaji AF. 1977. The protective effect of fat on the heat resistance of bacteria. Int. J. Food Sci. Technol. 12:3217–30 [Google Scholar]
  95. Serp D, Von Stockar U, Marison IW. 2002. Immobilized bacterial spores for use as bioindicators in the validation of thermal sterilization processes. J. Food Prot. 65:71134–41 [Google Scholar]
  96. Setlow P. 2006. Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. J. Appl. Microbiol. 101:3514–25 [Google Scholar]
  97. Smelt JPPM, Brul S. 2014. Thermal inactivation of microorganisms. Crit. Rev. Food Sci. Nutr. 54:101371–85 [Google Scholar]
  98. Stumbo CR. 1973. Thermal Bacteriology in Food Processing New York: Academic
  99. Van Asselt ED, Zwietering MH. 2006. A systematic approach to determine global thermal inactivation parameters for various food pathogens. Int. J. Food Microbiol. 107:173–82 [Google Scholar]
  100. Van Boeijen IKH, Francke C, Moezelaar R, Abee T, Zwietering MH. 2011. Isolation of highly heat-resistant Listeria monocytogenes variants by use of a kinetic modeling-based sampling scheme. Appl. Environ. Microbiol. 77:82617–24 [Google Scholar]
  101. Van Boekel MAJS. 2002. On the use of the Weibull model to describe thermal inactivation of microbial vegetative cells. Int. J. Food Microbiol. 74:139–59 [Google Scholar]
  102. Wachnicka E, Stringer SC, Barker GC, Peck MW. 2016. Systematic assessment of nonproteolytic Clostridium botulinum spores for heat resistance. Appl. Environ. Microbiol. 82:196019–29 [Google Scholar]
  103. Warda AK, Siezen RJ, Boekhorst J, Wells-Bennik MHJ, de Jong A. et al. 2016. Linking Bacillus cereus genotypes and carbohydrate utilization capacity. PLOS ONE 11:6e0156796 [Google Scholar]
  104. Warda AK, Xiao Y, Boekhorst J, Wells-Bennik MHJ, Nierop Groot MN, Abee T. 2017. Analysis of germination capacity and germinant receptor (sub)clusters of genome-sequenced Bacillus cereus environmental isolates and model strains. Appl. Environ. Microbiol. 83:4e02490–16 [Google Scholar]
  105. Warth A. 1978. Relationship between the heat resistance of spores and the optimum and maximum growth temperatures of Bacillus species. J. Bacteriol. 134:3699–705 [Google Scholar]
  106. Weibull W. 1951. A statistical distribution function of wide applicability. J. Appl. Mech. 18:293–97 [Google Scholar]
  107. Wells-Bennik MHJ, Eijlander RT, den Besten HMW, Berendsen EM, Warda AK. et al. 2016. Bacterial spores in food: survival, emergence, and outgrowth. Annu. Rev. Food Sci. Technol. 7:457–82 [Google Scholar]
  108. Wells-Bennik MHJ, Janssen O, Klaus V, Yang C, Zwietering MH. et al. 2018. Heat resistance of spores of 18 strains of Geobacillus stearothermophilus and impact of culturing conditions. Submitted
  109. Wu VC. 2008. A review of microbial injury and recovery methods in food. Food Microbiol 25:735–44 [Google Scholar]
  110. Xiao Y, Wagendorp A, Abee T, Wells-Bennik MHJ. 2015. Differential outgrowth potential of Clostridium perfringens food-borne isolates with various cpe-genotypes in vacuum-packed ground beef during storage at 12°C. Int. J. Food Microbiol. 94:40–45 [Google Scholar]
  111. Zwietering MH. 2009. Quantitative risk assessment: Is more complex always better? Simple is not stupid and complex is not always more correct. Int. J. Food Microbiol. 134:1–257–62 [Google Scholar]
  112. Zwietering MH. 2015. Risk assessment and risk management for safe foods: Assessment needs inclusion of variability and uncertainty, management needs discrete decisions. Int. J. Food Microbiol. 213:118–23 [Google Scholar]
  113. Zwietering MH, Jongenburger I, Rombouts FM, Van ’t Riet K. 1990. Modeling of the bacterial growth curve. Appl. Environ. Microbiol. 56:61875–81 [Google Scholar]
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Natural Diversity in Heat Resistance of Bacteria and Bacterial Spores: Impact on Food Safety and Quality
Annual Review of Food Science and Technology 9, 383 (2018); https://doi.org/10.1146/annurev-food-030117-012808
/content/journals/10.1146/annurev-food-030117-012808
/content/journals/10.1146/annurev-food-030117-012808
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