Influence of food matrix on outgrowth heterogeneity of heat damaged Bacillus cereus spores

International Journal of Food Microbiology

Volumn 201, Issue , 2015, Pages 27-34

  Warda, Alicja K ^a,b   den Besten, Heidy M W ^b   Sha, Na ^b   Abee, Tjakko ^a,b   Nierop Groot, Masja N ^a,b  

^a TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Bacillus cereus; Damage; Food matrix; Population heterogeneity; Sporeformers; Thermal treatment

Indexed keywords

ARTICLE; BACILLUS CEREUS; BACTERIAL SPORE; BROCCOLI; CELL DIVISION; CELL GROWTH; CONTROLLED STUDY; FOOD; GERMINATION; HEAT TREATMENT; NONHUMAN; OSMOTIC STRESS; PH; RICE; SPORE GERMINATION; SUSPENSION; BRASSICA; FOOD CONTROL; GROWTH, DEVELOPMENT AND AGING; HEAT; MEAT; MICROBIOLOGY; PHYSIOLOGY;

BACILLUS CEREUS; BACILLUS CEREUS ATCC 14579; BRASSICA OLERACEA VAR. ITALICA;

BACILLUS CEREUS; BRASSICA; FOOD MICROBIOLOGY; HOT TEMPERATURE; HYDROGEN-ION CONCENTRATION; MEAT; ORYZA SATIVA; SPORES, BACTERIAL;

EID: 84923632373     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2015.02.010     Document Type: Article

References (45)

1. Abee T., Groot M.N., Tempelaars M., Zwietering M., Moezelaar R., van der Voort M. Germination and outgrowth of spores of Bacillus cereus group members: diversity and role of germinant receptors. Food Microbiol. 2011, 28:199-208.
2. Aguirre J.S., Ordonez J.A., Garcia de Fernando G.D. A comparison of the effects of E-beam irradiation and heat treatment on the variability of Bacillus cereus inactivation and lag phase duration of surviving cells. Int. J. Food Microbiol. 2012, 153:444-452.
3. Andersson A., Rönner U., Granum P.E. What problems does the food industry have with the spore-forming pathogens Bacillus cereus and Clostridium perfringens?. Int. J. Food Microbiol. 1995, 28:145-155.
4. Carlin F., Girardin H., Peck M.W., Stringer S.C., Barker G.C., Martinez A., Fernandez A., Fernandez P., Waites W.M., Movahedi S., van Leusden F., Nauta M., Moezelaar R., Del Torre M., Litman S. Research on factors allowing a risk assessment of spore-forming pathogenic bacteria in cooked chilled foods containing vegetables: a FAIR collaborative project. Int. J. Food Microbiol. 2000, 60:117-135.
5. Cazemier A.E., Wagenaars S.F.M., ter Steeg P.F. Effect of sporulation and recovery medium on the heat resistance and amount of injury of spores from spoilage bacilli. J. Appl. Microbiol. 2001, 90:761-770.
6. Choma C., Guinebretière M.H., Carlin F., Schmitt P., Velge P., Granum P.E., Nguyen-The C. Prevalence, characterization and growth of Bacillus cereus in commercial cooked chilled foods containing vegetables. J. Appl. Microbiol. 2000, 88:617-625.
7. Cronin U.P., Wilkinson M.G. The use of flow cytometry to study the germination of Bacillus cereus endospores. Cytom. A 2007, 71:143-153.
8. Cronin U.P., Wilkinson M.G. Bacillus cereus endospores exhibit a heterogeneous response to heat treatment and low-temperature storage. Food Microbiol. 2008, 25:235-243.
9. den Besten H.M.W., Ingham C.J., van Hylckama Vlieg J.E.T., Beerthuyzen M.M., Zwietering M.H., Abee T. Quantitative analysis of population heterogeneity of the adaptive salt stress response and growth capacity of Bacillus cereus ATCC 14579. Appl. Environ. Microbiol. 2007, 73:4797-4804.
10. den Besten H.M.W., Garcia D., Moezelaar R., Zwietering M.H., Abee T. Direct-imaging-based quantification of Bacillus cereus ATCC 14579 population heterogeneity at a low incubation temperature. Appl. Environ. Microbiol. 2010, 76:927-930.
11. den Besten H.M.W., van Melis C.C.J., Sanders J.W., Nierop Groot M.N., Abee T. Impact of sorbic acid on germination and outgrowth heterogeneity of Bacillus cereus ATCC 14579 spores. Appl. Environ. Microbiol. 2012, 78:8477-8480.
12. Dierick K., Van Coillie E., Swiecicka I., Meyfroidt G., Devlieger H., Meulemans A., Hoedemaekers G., Fourie L., Heyndrickx M., Mahillon J. Fatal family outbreak of Bacillus cereus - associated food poisoning. J. Clin. Microbiol. 2005, 43:4277-4279.
13. Ehling-Schulz M., Fricker M., Scherer S. Bacillus cereus, the causative agent of an emetic type of food-borne illness. Mol. Nutr. Food Res. 2004, 48:479-487.
14. Faille C., Lebret V., Gavini F., Maingonnat J.-F. Injury and lethality of heat treatment of Bacillus cereus spores suspended in buffer and in poultry meat. J. Food Prot. 1997, 60:544-547.
15. Gaillard S., Leguerinel I., Savy N., Mafart P. Quantifying the combined effects of the heating time, the temperature and the recovery medium pH on the regrowth lag time of Bacillus cereus spores after a heat treatment. Int. J. Food Microbiol. 2005, 105:53-58.
16. Garcia D., van der Voort M., Abee T. Comparative analysis of Bacillus weihenstephanensis KBAB4 spores obtained at different temperatures. Int. J. Food Microbiol. 2010, 140:146-153.
17. Ghosh S., Setlow P. The preparation, germination properties and stability of superdormant spores of Bacillus cereus. J. Appl. Microbiol. 2010, 108:582-590.
18. González I., López M., Mazas M., Gonzalez J., Bernardo A. The effect of recovery conditions on the apparent heat resistance of Bacillus cereus spores. J. Appl. Bacteriol. 1995, 78:548-554.
19. González I., López M., Mazas M., Bernardo A., Martin R. Effect of pH of the recovery medium on the apparent heat resistance of three strains of Bacillus cereus. Int. J. Food Microbiol. 1996, 31:341-347.
20. Granum P.E. Bacillus cereus. Foodborne Pathogens: Microbiology and Molecular Biology 2005, Caister Academic Press. P.M. Fratamico, A.K. Bhunia, J.L. Smith (Eds.).
21. Hornstra L.M., de Vries Y.P., de Vos W.M., Abee T., Wells-Bennik M.H.J. gerR, a novel ger operon involved in L-alanine- and inosine-initiated germination of Bacillus cereus ATCC 14579. Appl. Environ. Microbiol. 2005, 71:774-781.
22. Hornstra L.M., de Vries Y.P., Wells-Bennik M.H.J., de Vos W.M., Abee T. Characterization of germination receptors of Bacillus cereus ATCC 14579. Appl. Environ. Microbiol. 2006, 72:44-53.
23. Johnson K.M., Nelson C.L., Busta F.F. Influence of temperature on germination and growth of spores of emetic and diarrheal strains of Bacillus cereus in a broth medium and in rice. J. Food Sci. 1983, 48:286-287.
24. Kotiranta A., Lounatmaa K., Haapasalo M. Epidemiology and pathogenesis of Bacillus cereus infections. Microbes Infect. 2000, 2:189-198.
25. Løvdal I.S., Hovda M.B., Granum P.E., Rosnes J.T. Promoting Bacillus cereus spore germination for subsequent inactivation by mild heat treatment. J. Food Prot. 2011, 74:2079-2089.
26. Mazas M., López M., Martinez S., Bernardo A., Martin R. Heat resistance of Bacillus cereus spores: effects of milk constituents and stabilizing additives. J. Food Prot. 1999, 62:410-413.
27. Moussa-Boudjemaa B., Gonzalez J., Lopez M. Heat resistance of Bacillus cereus spores in carrot extract acidified with different acidulants. Food Control 2006, 17:819-824.
28. Nordstokke D.W., Zumbo B.D. A new nonparametric levene test for equal variances. Psicologica 2010, 31:401.
29. Nordstokke D.W, Zumbo B.D., Cairns S.L., Saklofske D.H. The operating characteristics of the nonparametric Levene test for equal variances with assessment and evaluation data. Pract. Assess. Res. Eval. 2011, 16:1-8.
30. Pandey R., Ter Beek A., Vischer N.O.E., Smelt J.P.P.M., Brul S., Manders E.M.M. Live cell imaging of germination and outgrowth of individual bacillus subtilis spores; the effect of heat stress quantitatively analyzed with SporeTracker. PLoS ONE 2013, 8:e58972.
31. Rajkovic A., Smigic N., Devlieghere F. Contemporary strategies in combating microbial contamination in food chain. Int. J. Food Microbiol. 2010, 141(Suppl. 1):S29-S42.
32. Ramirez-Peralta A., Zhang P., Li Y.Q., Setlow P. Effects of sporulation conditions on the germination and germination protein levels of Bacillus subtilis spores. Appl. Environ. Microbiol. 2012, 78:2689-2697.
33. Rodriguez-Palacios A., LeJeune J.T. Moist-heat resistance, spore aging, and superdormancy in Clostridium difficile. Appl. Environ. Microbiol. 2011, 77:3085-3091.
34. Samapundo S., Heyndrickx M., Xhaferi R., de Baenst I., Devlieghere F. The combined effect of pasteurization intensity, water activity, pH and incubation temperature on the survival and outgrowth of spores of Bacillus cereus and Bacillus pumilus in artificial media and food products. Int. J. Food Microbiol. 2014, 181:10-18.
35. Schoeni J.L., Wong A.C.L. Bacillus cereus food poisoning and its toxins. J. Food Prot. 2005, 68:636-648.
36. Setlow P. Spore germination. Curr. Opin. Microbiol. 2003, 6:550-556.
37. Shah I.M., Laaberki M.H., Popham D.L., Dworkin J. A eukaryotic-like Ser/Thr kinase signals bacteria to exit dormancy in response to peptidoglycan fragments. Cell 2008, 135:486-496.
38. Smelt J.P.P.M., Bos A.P., Kort R., Brul S. Modelling the effect of sub(lethal) heat treatment of Bacillus subtilis spores on germination rate and outgrowth to exponentially growing vegetative cells. Int. J. Food Microbiol. 2008, 128:34-40.
39. Stenfors Arnesen L.P., Fagerlund A., Granum P.E. From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol. Rev. 2008, 32:579-606.
40. Stringer S.C., Webb M.D., Peck M.W. Contrasting effects of heat treatment and incubation temperature on germination and outgrowth of individual spores of nonproteolytic Clostridium botulinum bacteria. Appl. Environ. Microbiol. 2009, 75:2712-2719.
41. Stringer S.C., Webb M.D., Peck M.W. Lag time variability in individual spores of Clostridium botulinum. Food Microbiol. 2011, 28:228-235.
42. Ter Beek A., Hornstra L.M., Pandey R., Kallemeijn W.W., Smelt J.P.P.M., Manders E.M.M., Brul S. Models of the behaviour of (thermally stressed) microbial spores in foods: tools to study mechanisms of damage and repair. Food Microbiol. 2011, 28:678-684.
43. van der Voort M., Garcia D., Moezelaar R., Abee T. Germinant receptor diversity and germination responses of four strains of the Bacillus cereus group. Int. J. Food Microbiol. 2010, 139:108-115.
44. van Melis C.C.J., den Besten H.M.W., Nierop Groot M.N., Abee T. Quantification of the impact of single and multiple mild stresses on outgrowth heterogeneity of Bacillus cereus spores. Int. J. Food Microbiol. 2014, 177:57-62.
45. Wang G., Paredes-Sabja D., Sarker M.R., Green C., Setlow P., Li Y.Q. Effects of wet heat treatment on the germination of individual spores of Clostridium perfringens. J. Appl. Microbiol. 2012, 113:824-836.