Follow-up of the Bacillus cereus emetic toxin production in penne pasta under household conditions using liquid chromatography coupled with mass spectrometry

Food Microbiology

Volumn 28, Issue 5, 2011, Pages 1105-1109

  Delbrassinne, Laurence ^a   Andjelkovic, Mirjana ^a   Rajkovic, Andreja ^b   Bottledoorn, Nadine ^a   Mahillon, Jacques ^c   Van Loco, Joris ^a  

^a SCIENTIFIC INSTITUTE OF PUBLIC HEALTH   (Belgium)

^b Faculty of Bioscience Engineering   (Belgium)

^c UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

B. cereus emetic strains; Cereulide; Food matrices; Household storage; LC MS

Indexed keywords

BACTERIAL TOXIN; CEREULIDE; DEPSIPEPTIDE;

ARTICLE; BACILLUS CEREUS; CHEMISTRY; EVALUATION; FOOD CONTAMINATION; FOOD CONTROL; FOOD HANDLING; ISOLATION AND PURIFICATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; METHODOLOGY;

BACILLUS CEREUS; BACTERIAL TOXINS; CHROMATOGRAPHY, LIQUID; DEPSIPEPTIDES; FOOD CONTAMINATION; FOOD HANDLING; FOOD MICROBIOLOGY; MASS SPECTROMETRY;

BACILLUS CEREUS; BACTERIA (MICROORGANISMS);

EID: 79955846034     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2011.02.014     Document Type: Article

References (39)

1. Agata N., Mori M., Ohta M., Suwan S., Ohtani I., Isobe M. A novel dodecadepsipeptide, cereulide, isolated from Bacillus cereus causes vacuole formation in HEp-2 cells. FEMS Microbiol. Lett. 1994, 121:31-34.
2. Agata N., Ohta M., Mori M., Isobe M. A novel dodecadepsipeptide, cereulide, is an emetic toxin of Bacillus cereus. FEMS Microbiol. Lett. 1995, 129:17-19.
3. Agata N., Ohta M., Mori M., Shibayama K. Growth conditions of an emetic toxin production by Bacillus cereus in a defined medium with amino acids. Microbiol. Immunol. 1999, 43:15-18.
4. Agata N., Ohta M., Yokoyama K. Production of Bacillus cereus emetic toxin (cereulide) in various foods. Int. J. Food Microbiol. 2002, 73:23-27.
5. Altayar M., Sutherland A.D. Bacillus cereus is common in the environment but emetic toxin producing isolates are rare. J. Appl. Microbiol. 2006, 100:7-14.
6. Andersson M.A., Mikkola R., Helin J., Andersson M.C., Salkinoja-Salonen M. A novel sensitive bioassay for detection of Bacillus cereus emetic toxin and related depsipeptide ionophores. Appl. Environ. Microbiol. 1998, 64:1338-1343.
7. Andersson M.A., Jääskeläinen E.L., Shaheen R., Pirhonen T., Wijnands L.M., Salkinoja-Salonen M.S. Sperm bioassay for rapid detection of cereulide-producing Bacillus cereus in food and related environments. Int. J. Food Microbiol. 2004, 94:175-183.
8. Andersson M.A., Hakulinen P., Honkalampi-Hämäläinen U., Hoornstra D., Lhuguenot J.C., Mäki-Paakkanen J., Savolainen M., Severin I., Stammati A.L., Turco L., Weber A., von Wright A., Zucco F., Salkinoja-Salonen M. Toxicological profile of cereulide, the Bacillus cereus emetic toxin, in functional assays with human, animal and bacterial cells. Toxicon 2007, 49:351-357.
9. Ankolekar C., Rahmati T., Labbé R.G. Detection of toxinogenic Bacillus cereus and Bacillus thuringiensis spores in U.S. rice. Int. J. Food Microbiol. 2009, 128:460-466.
10. Apetroaie-Constantin C., Shaheen R., Andrup L., Smidt L., Rita H., Salkinoja-Salonen M. Environment driven cereulide production by emetic strains of Bacillus cereus. Int. J. Food Microbiol. 2008, 127:60-67.
11. Bauer T., Stark T., Hofmann T., Ehling-Schulz M. Development of a stable isotope dilution analysis for the quantification of the Bacillus cereus toxin cereulide in foods. J. Agric. Food Chem. 2010, 58:1420-1428.
12. Beattie S.H., Williams A.G. Detection of toxigenic strains of Bacillus cereus and other Bacillus spp. with an improved cytotoxicity assay. Lett. Appl. Microbiol. 1999, 28:221-225.
13. 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.
14. Ehling-Schulz M., Fricker M., Scherer S. Identification of emetic toxin producing Bacillus cereus strains by a novel molecular assay. FEMS Microbiol. Lett. 2004, 232:189-195.
15. Ehling-Schulz M., Svensson B., Guinebretière M.H., Lindbäck T., Andersson M., Schulz A., Fricker M., Christiansson A., Granum P.E., Märtlbauer E., Nguyen-The C., Salkinoja-Salonen M., Scherer S. Emetic toxin formation of Bacillus cereus is restricted to a single evolutionary lineage of closely related strains. Microbiology 2005, 151:183-197.
16. Finlay W.J.J., Logan N.A., Sutherland A.D. Bacillus cereus produces most emetic toxin at lower temperatures. Lett. Appl. Microbiol. 2000, 31:385-389.
17. Häggblom M.M., Apetroaie C., Andersson M.A., Salkinoja-Salonen M. Quantitative analysis of cereulide, the emetic toxin of Bacillus cereus, produced under various conditions. Appl. Environ. Microbiol. 2002, 68:2479-2483.
18. Hoton F.M., Fornelos N., N'Guessan E., Hu X., Swiecicka I., Dierick K., Jääskeläinen E., Salkinoja-Salonen M., Mahillon J. Family portrait of Bacillus cereus and Bacillus weihenstephanensis cereulide-producing strains. Environ. Microbiol. Rep. 2009, 1:177-183.
19. Hughes S., Bartholomew B., Hardy J.C., Kramer J.M. Potential application of a HEp-2 cell assay in the investigation of Bacillus cereus emetic-syndrome food poisoning. FEMS Microbiol. Lett. 1988, 52:7-12.
20. In't Veld, P.H., Fitz-James, I.A., Nuppunen, M., Kankare, M., Johansson, T., 2010. Quantification of cereulide from food poisoning outbreaks caused by Bacillus cereus. In: Proceedings of FoodMicro Symposium.
21. Isobe M., Ishikawa T., Suwan S., Agata N., Ohta M. Synthesis and activity of cereulide, a cyclic dodecadepsipeptide ionophore as emetic toxin from Bacillus cereus. Bioorg. Med. Chem. Lett. 1995, 5:2855-2858.
22. Jääskeläinen E., Teplova V., Andersson M.A., Andersson L.C., Tammela P., Andersson M.C., Pirhonen T.I., Saris N.-E.L., Vuorela P., Salkinoja-Salonen M.S. In vitro assay for human toxicity of cereulide, the emetic mitochondrial toxin produced by food poisoning Bacillus cereus. Toxicol. in Vitro 2003, 17:737-744.
23. Jääskeläinen E., Häggblom M.M., Andersson M.A., Vanne L., Salkinoja-Salonen M.S. Potential of Bacillus cereus for producing an emetic toxin, cereulide, in bakery products: quantitative analysis by chemical and biological methods. J. Food Protect. 2003, 66:1047-1054.
24. Jääskeläinen E., Häggblom M.M., Andersson, Salkinoja-Salonen M.S. Atmospheric oxygen and other conditions affecting the production of cereulide by Bacillus cereus in food. Int. J. Food Microbiol. 2004, 96:75-83.
25. Kawamura-Sato K., Hirama Y., Agata N., Ito H., Torii K., Takeno A., Hasegawa T., Shimomura Y., Ohta M. Quantitative analysis of cereulide, an emetic toxin of Bacillus cereus, by using rat liver mitochondria. Microbiol. Immunol. 2005, 49:25-30.
26. Kim J.-B., Kim J.-M., Kim S.-Y., Kim J.-H., Park Y.-B., Choi N.-J., Oh D.-H. Comparison of enterotoxin production and phenotypic characteristics between emetic and enterotoxic Bacillus cereus. J. Food Protect. 2010, 73:1219-1224.
27. Kim J.-B., Kim J.-M., Park Y.-B., Han J.-A., Lee S.-H., Kwak H.-S., Hwang I.-G., Yoon M.-H., Lee J.-B., Oh D.-H. Evaluation of various PCR assays for the detection of emetic toxin producing Bacillus cereus. J. Microbiol. Biotechnol. 2010, 20:1107-1113.
28. Mahler H., Pasi A., Kramer J.M., Schulte P., Scoging A.C., Bär W., Krähenbühl S. Fulminant liver failure in association with the emetic toxin of Bacillus cereus. N. Engl. J. Med. 1997, 336:1142-1148.
29. Pirhonen T.I., Andersson M.A., Jääskeläinen E.L., Salkinoja-Salonen M.S., Honkanen-Buzalski T., Johansson T.M.L. Biochemical and toxic diversity of Bacillus cereus in a pasta and meat dish associated with a food-poisoning case. Food Microbiol. 2005, 22:87-91.
30. Pirttijärvi T.S.M., Andersson M.A., Salkinoja-Salonen M.S. Properties of Bacillus cereus and other bacilli contaminating biomaterial-based industrial processes. Int. J. Food Microbiol. 2000, 60:231-239.
31. Rajkovic A., Uyttendaele M., Ombregt S.A., Jääskeläinen E., Salkinoja-Salonen M., Debevere J. Influence of type of food on the kinetics and overall production of Bacillus cereus emetic toxin. J. Food Protect. 2006, 69:847-852.
32. Rajkovic A., Uyttendaele M., Deley W., Van Soom A., Rijsselaere T., Debevere J. Dynamics of boar semen motility inhibition as a semi-quantitative measurement of Bacillus cereus emetic toxin (cereulide). J. Microbiol. Meth. 2006, 65:525-534.
33. Rajkovic A., Uyttendaele M., Vermeulen A., Andjelkovic M., Fitz-James I., In't Veld P., Denon Q., Vérhe R., Debevere J. Heat resistance of Bacillus cereus emetic toxin, cereulide. Lett. Appl. Microbiol. 2008, 46:536-541.
34. Shaheen R., Andersson M.A., Apetroaie C., Schulz A., Ehling-Schulz M., Ollilainen V.M., Salkinoja-Salonen M.S. Potential of selected infant food formulas for production of Bacillus cereus emetic toxin, cereulide. Int. J. Food Microbiol. 2006, 107:287-294.
35. Shinagawa K., Konuma H., Sekita H., Sugii S. Emesis of rhesus monkeys induced by intragastric administration with the HEp-2 vacuolation factor (cereulide) produced by Bacillus cereus. FEMS Microbiol. Lett. 1995, 130:87-90.
36. Shinagawa K., Ueno Y., Hu D., Ueda S., Sugii S. Mouse lethal activity of a HEp-2 vacuolation factor, cereulide, produced by Bacillus cereus isolated from vomiting-type food poisoning. J. Vet. Med. Sci. 1996, 58:1027-1029.
37. Thorsen L., Hansen B.M., Nielsen K.F., Hendriksen N.B., Phipps R.K., Budde B.B. Characterization of emetic Bacillus weihenstephanensis, a new cereulide-producing bacterium. Appl. Environ. Microbiol. 2006, 72:5118-5121.
38. Thorsen L., Budde B.B., Henrichsen L., Martinussen T., Jakobsen M. Cereulide formation by Bacillus weihenstephanensis and mesophilic emetic Bacillus cereus at temperature abuse depends on pre-incubation conditions. Int. J. Food Microbiol. 2009, 134:133-139.
39. Wallin-Carlquist N., Marta D., Borch E., Radström P. Prolonged expression and production of Staphylococcus aureus enterotoxin A in processed pork meat. Int. J. Food Microbiol. 2010, 141:S69-S74.