Modeling the recovery of heat-treated Bacillus licheniformis Ad978 and Bacillus weihenstephanensis KBAB4 spores at suboptimal temperature and pH using growth limits

Applied and Environmental Microbiology

Volumn 81, Issue 2, 2015, Pages 562-568

  Trunet, C ^a   Mtimet, N ^a,b   Mathot, A G ^a   Postollec, F ^a   Leguerinel, I ^a   Sohier, D ^a   Couvert, O ^a   Carlin, F ^a,c   Coroller, L ^a  

^a UNIVERSITÉ DE BREST   (France)

^b Université de Brest EA3882 Laboratoire Universitaire de Biodiversité et Ecologie Microbienne UMT1401 SPORE RISK ScInBioS ^*  (France)

^c UMR A 408 INRA University of Avignon   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOLOGY; RECOVERY; SPECIFIC HEAT; TEMPERATURE DISTRIBUTION;

BACILLUS LICHENIFORMIS; DECIMAL REDUCTION; INPUT PARAMETER; PH VALUE; RECOVERY TEMPERATURE;

HEAT RESISTANCE;

AGAR; BACTERIUM; GROWTH RATE; HEATING; NUMERICAL MODEL; PH; SPORULATION; TEMPERATURE GRADIENT;

BACILLUS LICHENIFORMIS; BACILLUS WEIHENSTEPHANENSIS;

BACILLUS; BACTERIAL SPORE; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; PH; RADIATION RESPONSE; TEMPERATURE; THEORETICAL MODEL;

BACILLUS; HYDROGEN-ION CONCENTRATION; MODELS, THEORETICAL; SPORES, BACTERIAL; TEMPERATURE;

EID: 84920747672     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02520-14     Document Type: Article

References (42)

1. Postollec F, Mathot A-G, Bernard M, Divanac'h M-L, Pavan S, Sohier D. 2012. Tracking spore-forming bacteria in food: from natural biodiversity to selection by processes. Int J Food Microbiol 158:1-8. http://dx.doi .org/10.1016/j.ijfoodmicro.2012.03.004.
2. Carlin F. 2011. Origin of bacterial spores contaminating foods. Food Microbiol 28:177-182. http://dx.doi.org/10.1016/j.fm.2010.07.008.
3. Abee T, Groot MN, Tempelaars M, Zwietering M, Moezelaar R, Voort M. 2011. Germination and outgrowth of spores of Bacillus cereus group members: diversity and role of germinant receptors. Food Microbiol 28: 199-208. http://dx.doi.org/10.1016/j.fm.2010.03.015.
4. Leguérinel I, Couvert O, Mafart P. 2006. Modelling the influence of the incubation temperature upon the estimated heat resistance of heated bacillus spores. Lett Appl Microbiol 43:17-21. http://dx.doi.org/10.1111/j .1472-765X.2006.01921.x.
5. Mafart P, Couvert O, Leguérinel I. 2001. Effect of pH on the heat resistance of spores: comparison of two models. Int J Food Microbiol 63:51-56. http://dx.doi.org/10.1016/S0168-1605(00)00397-4.
6. Augustin J-C. 2011. Challenges in risk assessment and predictive microbiology of foodborne spore-forming bacteria. Food Microbiol 28:209-213. http://dx.doi.org/10.1016/j.fm.2010.05.003.
7. Suzuki Y, Rode LJ. 1969. Effect of lysozyme on resting spores of Bacillus megaterium. J Bacteriol 98:238-245.
8. Setlow P. 2013. Summer meeting 2013-when the sleepers wake: the germination of spores of Bacillus species. J Appl Microbiol 115:1251-1268. http://dx.doi.org/10.1111/jam.12343.
9. Guinebretière M-H, Thompson FL, Sorokin A, Normand P, Dawyndt P, Ehling-Schulz M, Svensson B, Sanchis V, Nguyen-The C, Heyndrickx M, De Vos P. 2008. Ecological diversification in the Bacillus cereus group. Environ Microbiol 10:851-865. http://dx.doi.org/10.1111/j.1462-2920 .2007.01495.x.
10. Baril E, Coroller L, Couvert O, Leguérinel I, Postollec F, Boulais C, Carlin F, Mafart P. 2012. Modeling heat resistance of Bacillus weihenstephanensis and Bacillus licheniformis spores as function of sporulation temperature and pH. Food Microbiol 30:29-36. http://dx.doi.org/10 .1016/j.fm.2011.09.017.
11. Baril E, Coroller L, Postollec F, Leguerinel I, Boulais C, Carlin F, Mafart P. 2011. The wet-heat resistance of Bacillus weihenstephanensis KBAB4 spores produced in a two-step sporulation process depends on sporulation temperature but not on previous cell history. Int J Food Microbiol 146:57-62. http://dx.doi.org/10.1016/j.ijfoodmicro.2011.01.042.
12. Garcia D, van der Voort M, Abee T. 2010. Comparative analysis of Bacillus weihenstephanensis KBAB4 spores obtained at different temperatures. Int J Food Microbiol 140:146-153. http://dx.doi.org/10.1016/j .ijfoodmicro.2010.04.005.
13. Madslien EH, Granum PE, Blatny JM, Lindbäck T. 2014. L-alanineinduced germination in Bacillus licheniformis-the impact of native gerA sequences. BMC Microbiol 14:101. http://dx.doi.org/10.1186/1471-2180 -14-101.
14. Webb MD, Stringer SC, Le Marc Y, Baranyi J, Peck MW. 2012. Does proximity to neighbours affect germination of spores of non-proteolytic Clostridium botulinum? Food Microbiol 32:104-109. http://dx.doi.org/10 .1016/j.fm.2012.04.015.
15. 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 72:107-113. http://dx .doi.org/10.1016/S0168-1605(01)00624-9.
16. Valdramidis VP, van Impe JF. 2012. Progress on quantitative approaches of thermal food processing. Nova Science Publishers, Hauppauge, NY.
17. Fellows PJ. 2009. Food processing technology: principles and practice, 3rd ed. Woodhead Publishing, Boca Raton, FL.
18. Rosso L, Lobry JR, Bajard S, Flandrois J-P. 1995. Convenient model to describe the combined effects of temperature and pH on microbial growth. Appl Environ Microbiol 61:610-616.
19. Bigelow WD. 1921. The logarithmic nature of thermal death time curves. J Infect Dis 29:528-536. http://dx.doi.org/10.1093/infdis/29.5.528.
20. Huet S, Bouvier A, Poursat M-A, Jolivet E. 2010. Statistical tools for nonlinear regression, 2nd ed. A practical guide with S-PLUS and R examples. Springer, New York, NY.
21. Scherrer B, Legendre P, Beltangady M. 2009. Biostatistique, vol 2, 2nd ed. Gaetan Morin, Montreal, Canada.
22. Mafart P. 2000. Taking injuries of surviving bacteria into account for optimising heat treatments. Int J Food Microbiol 55:175-179. http://dx .doi.org/10.1016/S0168-1605(00)00160-4.
23. Baril E. 2011. Quantification de l'influence de l'environnement sur la formation et la thermo-résistance des spores bactériennes. Université de Bretagne Occidentale, Brest, France.
24. Mafart P, Leguérinel I. 1997. Modelling the heat stress and the recovery of bacterial spores. Int J Food Microbiol 37:131-135. http://dx.doi.org/10 .1016/S0168-1605(97)00061-5.
25. McMeekin TA. 1993. Predictive microbiology: theory and application. Research Studies Press Ltd., Taunton, United Kingdom.
26. Bajard S, Rosso L, Fardel G, Flandrois JP. 1996. The particular behaviour of Listeria monocytogenes under sub-optimal conditions. Int J Food Microbiol 29:201-211. http://dx.doi.org/10.1016/0168-1605(95)00031-3.
27. Ross T, Olley J, McMeekin TA, Ratkowsky DA. 2011. Some comments on Huang, L. (2010). Growth kinetics of Escherichia coli O157:H7 in mechanically- tenderized beef. International Journal of Food Microbiology, 140: 40-48. Int J Food Microbiol 147:78-80.
28. Gonzalez I, Lopez M, Mazas M, Gonzalez J, Bernardo A. 1995. The effect of recovery conditions on the apparent heat resistance of Bacillus cereus spores. J Appl Bacteriol 78:548-554. http://dx.doi.org/10.1111/j .1365-2672.1995.tb03098.x.
29. Daelman J, Sharma A, Vermeulen A, Uyttendaele M, Devlieghere F, Membré J-M. 2013. Development of a time-to-detect growth model for heat-treated Bacillus cereus spores. Int J Food Microbiol 165:231-240. http://dx.doi.org/10.1016/j.ijfoodmicro.2013.04.018.
30. Stringer SC, Webb MD, Peck MW. 2009. Contrasting effects of heat treatment and incubation temperature on germination and outgrowth of individual spores of nonproteolytic Clostridium botulinum bacteria. Appl Environ Microbiol 75:2712-2719. http://dx.doi.org/10.1128/AEM .02572-08.
31. Levinson HS, Hyatt MT. 1970. Effects of temperature on activation, germination, and outgrowth of Bacillus megaterium spores. J Bacteriol 101:58.
32. Peck MW. 2006. Clostridium botulinum and the safety of minimally heated, chilled foods: an emerging issue? J Appl Microbiol 101:556-570. http://dx.doi.org/10.1111/j.1365-2672.2006.02987.x.
33. Vary JC, Halvorson HO. 1965. Kinetics of germination of Bacillus spores. J Bacteriol 89:1340-1347.
34. Blocher JC, Busta FF. 1985. Multiple modes of inhibition of spore germination and outgrowth by reduced pH and sorbate. J Appl Bacteriol 59:469-478. http://dx.doi.org/10.1111/j.1365-2672.1985.tb03347.x.
35. Setlow P. 2003. Spore germination. Curr Opin Microbiol 6:550-556. http://dx.doi.org/10.1016/j.mib.2003.10.001.
36. Koutsoumanis K. 2008. A study on the variability in the growth limits of individual cells and its effect on the behavior of microbial populations. Int J Food Microbiol 128:116-121. http://dx.doi.org/10.1016/j.ijfoodmicro .2008.07.013.
37. Periago P, Fernández P, Salmerón M, Martínez A. 1998. Predictive model to describe the combined effect of pH and NaCl on apparent heat resistance of Bacillus stearothermophilus. Int J Food Microbiol 44:21-30. http://dx.doi.org/10.1016/S0168-1605(98)00111-1.
38. Zwietering MH, Wijtzes T, Rombouts FM, van't Riet K. 1992. A decision support system for prediction of microbial spoilage in foods. J Ind Microbiol 12:324-329.
39. Prentice GA, Clegg LFL. 1974. The effect of incubation temperature on the recovery of spores of Bacillus subtilis 8057. J Appl Bacteriol 37:501-513. http://dx.doi.org/10.1111/j.1365-2672.1974.tb00475.x.
40. Knaysi G. 1964. Effect of temperature on the rate of germination in Bacillus cereus. J Bacteriol 87:619-622.
41. Leguerinel I, Couvert O, Mafart P. 2000. Relationship between the apparent heat resistance of Bacillus cereus spores and the pH and NaCl concentration of the recovery medium. Int J Food Microbiol 55:223-227. http://dx.doi.org/10.1016/S0168-1605(00)00175-6.
42. Broussolle V, Gauillard F, Nguyen-The C, Carlin F. 2008. Diversity of spore germination in response to inosine and L-alanine and its interaction with NaCl andpHin the Bacillus cereus group. J Appl Microbiol 105:1081-1090. http://dx.doi.org/10.1111/j.1365-2672.2008.03847.x.