Persistence strategies of Bacillus cereus spores isolated from dairy silo tanks

Food Microbiology

Volumn 27, Issue 3, 2010, Pages 347-355

  Shaheen, Ranad ^a   Svensson, Birgitta ^b   Andersson, Maria A ^a   Christiansson, Anders ^c   Salkinoja Salonen, Mirja ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b Tetra Pak AB   (Sweden)

^c Swedish Dairy Association   (Sweden)

Author keywords

Adherence; Alkali tolerance; Bacillus cereus; Biofilm; Cereulide; Dairy silo tank; Psychrotrophic; Ribopattern; Spores

Indexed keywords

DISINFECTANT AGENT; STAINLESS STEEL;

ANIMAL; ARTICLE; BACILLUS CEREUS; BACTERIAL COUNT; BACTERIAL SPORE; BACTERIUM ADHERENCE; BIOFILM; CATTLE; DRUG EFFECT; FOOD CONTAMINATION; FOOD CONTROL; GENOTYPE; GERMINATION; GROWTH, DEVELOPMENT AND AGING; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; MILK; PH; PHENOTYPE; PHYSIOLOGY; RANDOM AMPLIFIED POLYMORPHIC DNA; SAFETY; TEMPERATURE;

ANIMALS; BACILLUS CEREUS; BACTERIAL ADHESION; BIOFILMS; CATTLE; COLONY COUNT, MICROBIAL; CONSUMER PRODUCT SAFETY; DISINFECTANTS; FOOD CONTAMINATION; FOOD MICROBIOLOGY; GENOTYPE; GERMINATION; HUMANS; HYDROGEN-ION CONCENTRATION; MILK; PHENOTYPE; RANDOM AMPLIFIED POLYMORPHIC DNA TECHNIQUE; SPORES, BACTERIAL; STAINLESS STEEL; TEMPERATURE;

BACILLUS CEREUS; BACTERIA (MICROORGANISMS);

EID: 77949328997     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2009.11.004     Document Type: Article

References (44)

1. Andersson A., Rönner U., and Granum P. What problems does the food industry have with the spore-forming pathogens Bacillus cereus and Clostridium perfringens?. International Journal of Food Microbiology 28 (1995) 145-155
2. Andersson M.A., Jääskeläinen E.L., Shaheen R., Pirhonen T., Wijnands L.M., and Salkinoja-Salonen M.S. Sperm bioassay for rapid detection of cereulide producing Bacillus cereus in food and related environments. International Journal of Food Microbiology 94 5 (2004) 1453-1457
3. Apetroaie C., Andersson M.A., Spröer C., Tsitko I., Shaheen R., Jääskeläinen E.L., Wijnands L.M., Heikkilä R., and Salkinoja-Salonen M.S. Cereulide producing strains of Bacillus cereus show diversity. Archives in Microbiology 184 (2005) 141-151
4. Banyko J., and Vyletelova M. Determining the source of Bacillus cereus and Bacillus licheniformis isolated from raw milk, pasteurized milk and yoghurt. Letters in Applied Microbiology 48 (2009) 318-323
5. Bartoszewicz M., Hansen B.M., and Swiecicka I. The members of the Bacillus cereus group are commonly present contaminants of fresh and heat-treated milk. Food Microbiology 25 (2008) 588-596
6. Bartoszewicz M., Dideshi D.K., Kraszewska A., Modzelewska E., and Swicicka I. Natural isolates of Bacillus thuringiensis display genetic and psychrotrophic properties characteristic of Bacillus weihenstephanensis. Journal of Applied Microbiology 106 (2009) 1967-1975
7. Becker H., Schaller G., Wiese W.v., and Terplan G. Bacillus cereus in infant foods and dried milk products. International Journal of Food Microbiology 23 (1994) 1-15
8. Branda S.S., Vik A., Friedman L., and Kolter R. Biofilms: the matrix revisited. Trends in Microbiology 13 1 (2005) 20-26
9. Carlin F., Fricker M., Pielaat A.-M., Shaheen R., Salkinoja Salonen M., Svensson B., Nguyen-the C., and Ehling-Schulz M. Emetic toxin-producing strains of Bacillus cereus show a distinct phenotype within the Bacillus cereus group. International Journal of Food Microbiology 109 (2006) 132-138
10. Christiansson A., Bertilsson J., and Svensson B. Bacillus cereus spores in raw milk: factors affecting the contamination of milk during the grazing period. Journal of Dairy Science 82 (1999) 305-314
11. Eaton A.D., Clesceri L.S., Rice E.W., and Greenberg A.E. Microbiological Examination. Standard Methods for the Examination of Water and Wastewater. 21st ed. (2005), American Public Health Association, Washington, DC 9-36 Part 9000, 9215
12. Ehling-Schulz M., Svensson B., Guinebretiere M.-H., Lindbäck T., Andersson M., Schulz A., Fricker M., Schirsitnasson A., Granum P.E., Märtlbauer E., Nguyen-The C., Salkinoja-Salonen M.S., and Scherer S. Emetic toxin formation of Bacillus cereus is restricted to a single evolutionary lineage of closely related strains. Microbiology 151 (2005) 183-197
13. Faille C., Fontaine F., and Bénézech T. Potential occurrence of adhering living Bacillus spores in milk product processing lines. Journal of Applied Microbiology 90 (2001) 892-900
14. Flint S.H., Bremer P.J., and Brooks J.D. Biofilms in dairy manufacturing plant description, current concerns and methods of control. Biofouling 11 (1997) 81-97
15. Francis K.P., Mayr R., von Stetten F., Stewart G.S., and Scherer S. Discrimination of psychrotrophic and mesophilic strains of the Bacillus cereus group by PCR targeting of major cold shock protein genes. Applied and Environmental Microbiology 64 9 (1998) 3525-3529
16. Helgason E., Økstad O.A., Caugant D.A., Johansen H.A., Fouet A., Mock M., Hegna I., and Kolstø A.B. Bacillus anthracis, Bacillus cereus and Bacillus thuringiensis - one species on the basis of genetic evidence. Applied and Environmental Microbiology 66 6 (2000) 2627-2630
17. Helke D.M., Somers E.B., and Wong A.C.L. Attachment of Listeria monocytogenes and Salmonella typhimurium to stainless steel and buna-N in the presence of milk and individual milk components. Journal of Food Protection 56 (1993) 479-484
18. Hornstra L.M., de Leeuw P.L.A., Moezelaar R., Wolbert E.J., De Vries Y.P., De Vos W.M., and Abee T. Germination of Bacillus cereus spores adhered to stainless steel. International Journal of Food Microbiology 116 (2007) 367-371
19. Hsueh Y.H., Somers E.B., Lereclus D., and Wong A.C.L. Biofilm formation by Bacillus cereus is influenced by PlcR a pleiotropic regulator. Applied and Environmental Microbiology 72 (2006) 5089-5092
20. Jääskeläinen E.L., Häggblom M.M., Andersson M.A., Vanne L., and Salkinoja-Salonen M.S. Potential of Bacillus cereus for producing an emetic toxin, cereulide, in bakery products: quantitative analysis by chemical and biological methods. Journal of Food Protection 66 (2003) 1047-1054
21. Kulikovsky A., Pankratz H.S., and Sadoff H.L. Ultrastructural and chemical changes in spores of Bacillus cereus after action of disinfectants. Journal of Applied Bacteriology 38 (1975) 39-46
22. Langsrud S., Baardsen B., and Sundheim G. Potentiation of the lethal effect of peroxygen on Bacillus cereus spores by alkali and enzyme wash. International Journal of Food Microbiology 56 (2000) 81-86
23. Lin S., Schraft H., Odumeru J.A., and Griffiths M.W. Identification of contamination sources of Bacillus cereus in pasteurized milk. International Journal of Food Microbiology 43 (1998) 159-171
24. Lopez F., Fischbach M.A., Chu F., Losick R., and Kolter R. Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis. Proceedings of the National Academy of Sciences of the USA 106 (2009) 280-285
25. Magnusson M., Christiansson A., Svensson B., and Kolstrup C. Effect of different premilking manual teat-cleaning methods on bacterial spores in milk. Journal of Dairy Science 89 (2006) 3866-3875
26. Nilsson J., Svensson B., Ekelund K., and Christiansson A. A RAPD-PCR method for large-scale typing of Bacillus cereus. Letters in Applied Microbiology 27 (1998) 168-172
27. Peng J.S., Tsai W.C., and Chou C.C. Inactivation and removal of Bacillus cereus by sanitizer and detergent. International Journal of Food Microbiology 77 (2002) 11-18
28. Pirttijärvi T.S.M., Andersson M.A., Scoging A.C., and Salkinoja-Salonen M. Evaluation of methods for recognizing strains of the Bacillus cereus group with food poisoning potential among industrial and environmental contaminants. Systematic and Applied Microbiology 22 (1999) 133-144
29. Ryu J.H., and Beuchat L. Biofilm Formation and sporulation by Bacillus cereus on a stainless steel surface and subsequent resistance of vegetative cells and spores to chlorine, chlorine dioxide and a peroxyacetic acid-based sanitizer. Journal of Food Protection 68 (2005) 2614-2622
30. Shaheen R., Andersson M.A., Apetroaie C., Schulz A., Ehling-Schulz M., Ollilainen V.-M., and Salkinoja-Salonen M.S. Potential of selected infant food formulas for production of Bacillus cereus emetic toxin, cereulide. International Journal of Food Microbiology 107 (2006) 287-294
31. Simmonds P., Mossel B.L., Intaraphan T., and Deeth H.C. Heat resistance of Bacillus spores when adhered to stainless steel and its relationship to spore hydrophobicity. Journal of Food Protection 66 11 (2003) 2070-2075
32. Stalheim T., and Granum P.E. Characterization of spore appendages from Bacillus cereus strains. Journal of Applied Microbiology 91 (2001) 839-845
33. Svensson B., Eneroth A., Brendehaug J., and Christiansson A. Investigation of Bacillus cereus contamination sites in a dairy plant with RAPD-PCR. International Dairy Journal 9 (1999) 903-912
34. Svensson B., Ekelund K., Ogura H., and Christiansson A. Characterisation of Bacillus cereus isolated from milk silo tanks at eight different dairy plants. International Dairy Journal 14 (2004) 17-27
35. Svensson B., Monthan A., Shaheen R., Andersson A., Salkinoja-Salonen M., and Christiansson A. Occurrence of emetic toxin producing Bacillus cereus in the dairy production chain. International Dairy Journal 16 7 (2006) 740-749
36. Tauveron G., Slomianny C., Henry C., and Faille C. Variability among Bacillus cereus strains in spore surface properties and influence on their ability to contaminate food surface equipment. International Journal of Food Microbiology 100 (2006) 254-262
37. Te Giffel M.C., Beumer R.R., Van Dam W.F., Slaghuis B.A., and Rombouts F.M. Sporicidal effect of disinfectants on Bacillus cereus isolated from the milk processing environment. International Biodeterioration & Biodegradation 36 (1995) 421-430
38. Te Giffel M.C., Beumer R.R., Granum P.E., and Rombouts F.M. Isolation and characterisation of Bacillus cereus from pasteurised milk in household refrigerators in the Netherlands. International Journal of Food Microbiology 34 (1997) 307-318
39. Te Giffel M.C., Wagendorp A., Herrewegh A., and Driehuis F. Bacterial spores in silage and milk. Antonie Van Leeuwenhoek 81 (2002) 625-630
40. Vissers M.M.M., Te Giffel M.C., Driehuis F., De Jong P., and Lankveld J.M.G. Predictive modeling of Bacillus cereus spores in farm tank milk during grazing and housing periods. Journal of Dairy Science 90 (2007) 281-282
41. Virtanen S.M., Roivainen M., Andersson M.A., Ylipaasto P., Hoornstra D., Mikkola R., and Salkinoja-Salonen M.S. In vitro toxicity of cereulide on porcine pancreatic Langerhans islets. Toxicon 51 (2008) 1029-1037
42. Wijman J.G.E., de Leeuw P.P.L.A., Moezelaar R., Zwietering M.H., and Abee T. Air-liquid interface biofilms of Bacillus cereus: formation, sporulation, and dispersion. Applied and Environmental Microbiology 73 (2007) 1481-1488
43. Wijnands L.M., Dufrenne J.B., Rombouts F.M., in t'Veld P.H., and Van Leusden F.M. Prevalence of potentially pathogenic Bacillus cereus in food commodities in the Netherlands. Journal of Food Protection 69 11 (2006) 2587-2594
44. Wong A.C.L. Biofilms in food processing environments. Journal of Dairy Science 81 (1998) 2765-2770