Enterotoxigenic profiling of emetic toxin- and enterotoxin-producing bacillus cereus, isolated from food, environmental, and clinical samples by multiplex PCR

Journal of Food Science

Volumn 79, Issue 11, 2014, Pages M2288-M2293

  Forghani, Fereidoun ^a   Kim, Jung Beom ^b   Oh, Deog Hwan ^a  

^a Kangwon National University   (South Korea)

^b Gyeonggi do Research Institute of Health and Environment   (South Korea)

Author keywords

Bacillus cereus; Enterotoxigenic profiling; Food poisoning; Multiplex PCR

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL TOXIN; ENTEROTOXIN; ENTEROTOXIN, BACILLUS CEREUS; NHEA PROTEIN, BACILLUS CEREUS;

ANALYSIS; BACILLUS CEREUS; BACILLUS THURINGIENSIS; BACTERIAL GENE; DIARRHEA; FOOD CONTAMINATION; FOOD CONTROL; FOOD POISONING; FOOD SAFETY; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MULTIPLEX POLYMERASE CHAIN REACTION;

BACILLUS CEREUS; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; BACTERIAL TOXINS; DIARRHEA; ENTEROTOXINS; FOOD CONTAMINATION; FOOD MICROBIOLOGY; FOOD SAFETY; FOODBORNE DISEASES; GENES, BACTERIAL; MULTIPLEX POLYMERASE CHAIN REACTION;

EID: 84910629442     PISSN: 00221147     EISSN: 17503841     Source Type: Journal    
DOI: 10.1111/1750-3841.12666     Document Type: Article

References (47)

1. Agata N, Mori M, Ohta M, Suwan S, Ohtani I, Isobe M. 1994. A novel dodecadepsipeptide, cereulide, isolated from Bacillus cereus vacuole formation in Hep-2 cells. FEMS Microbiol Lett 121:31-4.
2. Agata N, Ohta M, Mori M, Shibayama K. 1999. Growth conditions of and emetic toxin production by Bacillus cereus in a defined medium with amino acids. Microbiol Immunol 43:15-8.
3. Agata N, Ohta M, Yokoyama K. 2002. Production of Bacillus cereus emetic toxin (cereulide) in various foods. Int J Food Microbiol 73:23-7.
4. Altayar M, Sutherland AD. 2006. Bacillus cereus is common in the environment but emetic toxin producing strains are rare. J Appl Microbiol 100:7-14.
5. Ankolekar C, Rahmati T, Labbé RG. 2009. Detection of toxigenic Bacillus cereus and Bacillus thuringiensis spores in U.S. rice. Int J Food Microbiol 128:460-6.
6. Anonymous. 2004. ISO 7932:2004 microbiology of food and animal feeding stuffs horizontal method for the enumeration of presumptive Bacillus cereus: colony-count technique at 30 degrees C. Geneve, Switzerland: Intl. Organization for Standardization.
7. Anonymous. 2006. ISO 21871:2006 Microbiology of food and animal feeding stuffs: horizontal method for the determination of low numbers of presumptive Bacillus cereus-most probable number technique and detection method. Geneve, Switzerland: Intl. Organization for Standardization.
8. Bonerba E, Di Pinto A, Novello L, Montemurro F, Terio V, Colao V, Ciccarese G, Tantillo G. 2010. Detection of potentially enterotoxigenic food-related Bacillus cereus by PCR analysis. Int J Food Sci Technol 45:1310-5.
9. Brillard J, Lereclus D. 2004. Comparison of cytotoxin cytK promoters from Bacillus cereus strain ATCC 14579 and from a B. cereus food-poisoning strain. Microbiology 150: 2699-705.
10. Chon JW, Kim JH, Lee SJ, Hyeon JY, Seo KH. 2012. Toxin profile, antibiotic resistance, and phenotypic and molecular characterization of Bacillus cereus in sunsik. Food Microbiol 32:217-22.
11. Dierick K, Van Coillie E, Swiecicka I, Meyfroidt G, Devlieger H, Meulemans A, Hoedemaekers G, Fourie L, Heyndrickx M, Mahillon J. 2005. Fatal family outbreak of Bacillus cereus-associated food poisoning. J Clin Microbiol 43:4277-9.
12. Ehling-Schulz M, Fricker M, Siegfried S. 2004. Identification of emetic toxin producing Bacillus cereus strains by a novel molecular assay. FEMS Mirobiol Lett 232:189-95.
13. Ehling-Schulz M, Guinbretiere MH, Monthán A, Berge O, Fricker M, Svensson B. 2006. Toxin gene profiling of enterotoxic and emetic Bacillus cereus. FEMS Microbiol Lett 260:232-40.
14. Ehling-schulz M, Messelhäusser 2013. Bacillus "next generation" diagnostics: moving from detection toward subtyping and risk-related strain profiling. Front Microbiol 4(32):1-8.
15. Ehling-Schulz M, Svensson B, Guinebretiere MH, Lindbäck T, Andersson M, Schulz A, Fricker M, Christiansson A, Granum PE, Märtlbauer E, Nguyen-The C, Salkinoja-Salonen M, Scherer S. 2005. Emetic toxin formation of Bacillus cereus is restricted to a single evolutionary lineage of closely related strains. Microbiol 151:183-97.
16. Ellis RT, Stockhoff BA, Stamp L, Schnepf HE, Schwab GE, Knuth M, Russell J, Cardineau GA, Narva KE. 2002. Novel Bacillus thuringiensis binary insecticidal crystal proteins active on western corn rootworm, Diabrotica virgifera virgifera LeConte. Appl Environ Microbiol 68:1137-45.
17. Fernández-No IC, Guarddon M, Böhme K, Cepeda A, Calo-Mata P, Barros-Velázquez J. 2011. Detection and quantification of spoilage and pathogenic Bacillus cereus, Bacillus subtilis and Bacillus licheniformis by real-time PCR. Food Microbiol 28:605-10.
18. Fricker M, Messelhäußer U, Busch U, Scherer S, Ehking-Schulz M. 2007. Diagnostic real-time PCR assays for the detection of emetic Bacillus cereus strains in foods and recent food-borne outbreaks. Appl Environ Microbiol 73(6):1892-8.
19. Fricker M, Reissbrodt R, Ehling-Schulz M. 2008. Evaluation of standard and new chromogenic selective plating media for isolation and identification of Bacillus cereus. Int J Food Microbiol 121:27-34.
20. Gaviria Rivera AM, Granum PE, Priest FG. 2000. Common occurrence of enterotoxin genes and enterotoxicity in Bacillus thuringiensis. FEMS Microbiol Lett 190:151-5.
21. Granum PE, O'Sullivan K, Lund T. 1999. The sequence of the non-hemolytic enterotoxin operon from Bacillus cereus. FEMS Microbiol Lett 177:225-9.
22. Guinebretie`re M, Broussolle Y, Nguyen-The C. 2002. Enterotoxigenic profiles of food-poisoning and food-borne Bacillus cereus strains. J Clin Microbiol 40:3053-6.
23. Häggblom MM, Apetroaie C, Andersson MA, Salkinoja-Salonen MS. 2002. Quantitative analysis of cereulide, the emetic toxin of Bacillus cereus, produced under various conditions. Appl Environ Microbiol 68:2479-83.
24. Helgason E, Økstad OA, Caugant DA, Johansen HA, Fouet A, Mock M, Hegna I, KolstØ AB. 2000. Bacillus anthracis, Bacillus cereus and Bacillus thuringiensis: one species on the basis genetic evidence. Appl Environ Microbiol 66:2627-30.
25. Jiménez G, Blanch AR, Tamames J, Rosselló-Mora R. 2013. Complete genome sequence of Bacillus toyonensis BCT-7112T, the active ingredient of the feed additive preparation Toyocerin. Genome Announc 1(6):e01080-13. DOI:10.1128/genomeA.01080-13.
26. Kim JM, Forghani F, Kim JB, Park YB, Park MS, Wang J, Park JH, Oh DH. 2012. Improved multiplex PCR assay for simultaneous detection of Bacillus cereus emetic and enterotoxic strains. Food Sci Biotechnol 21(5):1439-44.
27. Kim JB, Kim JM, Cho SH, Oh SH, Choi NJ, Oh DH. 2011. The gene profiles and toxin production ability of Bacillus cereus isolated from clinical and food samples. J Food Sci 76(1):25-9.
28. Kim SK, Kim KP, Jang SS, Shin EM, Kim MJ, Oh S, Ryu S. 2009. Prevalence and toxigenic profiles of Bacillus cereus isolated from dried red peppers, rice and sunsik in Korea. J Food Prot 72(3):578-82.
29. Kim JB, Kim JM, Kim CH, Seo KS, Park YB, Choi NJ, Oh DH. 2010. Emetic toxin producing Bacillus cereus Korean isolates contain genes encoding diarrheal-related enterotoxins. Int J Food Microbiol 144:182-6.
30. Ladeuze S, Lents N, Delbrassinne L, Hu X, Kahillon J. 2011. Antifungal activity displayed by cereulide, the emetic toxin produced by Bacillus cereus. Appl Environ Microbiol 77(7):2555-8.
31. Lindbäck T, Fagerlund A, RØdland S, Granum PE. 2004. Characterization of Bacillus cereus Nhe enterotoxin. Microbiology 150:3959-67.
32. Lund T, De Buyser ML, Granum PE. 2000. A new cytotoxin from Bacillus cereus that may cause necrotic enteritis. Mol Microbiol 38:254-61.
33. Martínez-Blanch JF, Sánchez G, Garay E, Aznar R. 2009. Development of a real-time PCR assay for detection and quantification of enterotoxigenic members of Bacillus cereus group in food samples. Int J Food Microbiol 135:15-21.
34. McKillip JL. 2000. Prevalence and expression of enterotoxins in Bacillus cereus and other Bacillus spp., a literature review. Antonie van Leeuwenhoek 77:393-9.
35. Molva C, Sudagidan M, Okuklu B. 2009. Extracellular enzyme production and enterotoxigenic gene profiles of Bacillus cereus and Bacillus thuringiensis strains isolated from cheese in Turkey. Food Control 20:829-34.
36. Ngamwongsatit P, Buasri W, Pianariyanon P, Pulsrikarn C, Ohba M, Assavanig A, Panbangred W. 2008. Broad distribution of enterotoxin genes (hblCDA, nheABC, cytK and entFM) among Bacillus thuringiensis and bacillus cereus as shown by novel primers. Int J Food Microbiol 121:352-6.
37. Oh MH, Ham JS, Cox JM. 2012. Diversity and toxigenicity among members of the Bacillus cereus group. Int J Food Microbiol 152:1-8.
38. Park YB, Kim JB, Shin SW, Kim JC, Cho SH, Lee BK, Ahn J, Kim JM, Oh DH. 2009. Prevalence, genetic diversity, and antibiotic susceptibility of Bacillus cereus strains isolated from rice and cereals collected in Korea. J Food Prot 72(3):612-7.
39. Rahmati T, Labbé R. 2008. Levels and toxigenicity of Bacillus cereus and Clostridium perfringens from retail seafood. J Food Prot 71:1178-85.
40. Rosenquist H, Smidt L, Andersen SR, Jensen GB, Wilcks A. 2005. Occurrence and significance of Bacillus cereus and Bacillus thuringiensis in ready-to-eat food. FEMS Microbiol Lett 250:129-36.
41. Sandra A, Afsah-Hejri L, Tunung R, Tuan Zainazor TC, Tang JYH, Ghazali FM, Nakaguchi Y, Nishibuchi M, Son R. 2012. Bacillus cereus and Bacillus thuringiensis in ready-to-eat cooked rice in Malaysia. Int Food Res J 19(3):829-36.
42. Schoeni JL, Wong ACL. 2005. Bacillus cereus food poisoning and its toxins. J Food Prot 68:636-48.
43. Seong SJ, Lim JS, Lee KG, Lee SJ, Hong KW. 2008. Toxin gene profiling of Bacillus cereus food isolates by PCR. J Korean Soc Appl Biol Chem 51(4):263-8.
44. Tewari A, Singh SP, Rashmi S. 2013. Incidence and enterotoxigenic profile of Bacillus cereus in meat and meat products of Utarkhand, India. J Food Sci Technol DOI: 10.1007/s13197-013-1162-0.
45. Thorsen L, Hansen BM, Nielsen KF, Hendriksen NB, Phipps RK, Budde BB. 2006. Characterization of emetic Bacillus weihenstephanensis, a new cereulide producing bacterium. Appl Environ Microbiol 72:5118-21.
46. Tran SL, Guillemet E, Gohar M, lereclus D, Ramarao N. 2010. CwpFM (EntFM) is a Bacillus cereus potential cell wall peptidase implicated in adhesion, biofilm formation, and virulence. J Bacteriol 192(10):2638-42.
47. Wehrle E, Didier A, Moravek M, Dietrich R, Märtlbauer E. 2010. Detection of Bacillus cereus with enteropathogenic potential by multiplex real-time PCR based on SYBR Green I. Mol Cell Probes 24:124-30.