Development of a real-time PCR assay for detection and quantification of enterotoxigenic members of Bacillus cereus group in food samples

International Journal of Food Microbiology

Volumn 135, Issue 1, 2009, Pages 15-21

  Martinez Blanch J F ^a,b   Sanchez G ^b   Garay, E ^a   Aznar, R ^a,b  

^a UNIVERSITY OF VALENCIA   (Spain)

^b INSTITUTO DE AGROQUÍMICA Y TECNOLOGÍA DE ALIMENTOS CSIC   (Spain)

Author keywords

Bacillus cereus; Food; Quantification; Real time PCR

Indexed keywords

GENOMIC DNA; PHOSPHOLIPASE C;

ARTICLE; ARTIFICIAL MILK; BACILLUS; BACILLUS CEREUS; BACTERIAL STRAIN; BACTERIUM DETECTION; BACTERIUM ISOLATE; CALIBRATION; CONTROLLED STUDY; DILUTION; EGG; FOOD CONTAMINATION; INTERMETHOD COMPARISON; NONHUMAN; NUCLEOTIDE SEQUENCE; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSITIVITY AND SPECIFICITY;

BACILLUS CEREUS; CALIBRATION; COLONY COUNT, MICROBIAL; DNA, BACTERIAL; EGGS; ENTEROTOXINS; FOOD CONTAMINATION; FOOD MICROBIOLOGY; HUMANS; INFANT; INFANT FORMULA; INFANT, NEWBORN; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

BACILLUS CEREUS; BACILLUS CEREUS GROUP;

EID: 68949116175     PISSN: 01681605     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2009.07.013     Document Type: Article

References (53)

1. Abriouel H., Ben O.N., Lucas L.R., Martinez C.M., Ortega E., and Galvez A. Differentiation and characterization by molecular techniques of Bacillus cereus group isolates from poto poto and degue, two traditional cereal-based fermented foods of Burkina Faso and Republic of Congo. Journal of Food Protection 70 (2007) 1165-1173
2. Agata N., Ohta M., and Yokoyama K. Production of Bacillus cereus emetic toxin (cereulide) in various foods. International Journal of Food Microbiology 73 (2002) 23-27
3. Anonymous. ISO 16140:2003 microbiology of food and animal feeding stuffs - protocol for the validation of alternative methods (2003), International Organization for Standardization, Geneve Switzerland
4. Anonymous. 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 (2004), International Organization for Standardization, Geneve Switzerland
5. Anonymous. 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 (2006), International Organization for Standardization, Geneve Switzerland
6. Asano S.I., Nukumizu Y., Bando H., Iizuka T., and Yamamoto T. Cloning of novel enterotoxin genes from Bacillus cereus and Bacillus thuringiensis. Applied Environmental Microbiology 63 (1997) 1054-1057
7. Aznar R., and Alarcon B. PCR detection of Listeria monocytogenes: a study of multiple factors affecting sensitivity. Journal of Applied Microbiology 95 (2003) 958-966
8. Beattie S.H., and Williams A.G. Detection of toxigenic strains of Bacillus cereus and other Bacillus spp. with an improved cytotoxicity assay. Letters in Applied Microbiology 28 (1999) 221-225
9. Becker H., Schaller G., von W.W., and Terplan G. Bacillus cereus in infant foods and dried milk products. International Journal of Food Microbiology 23 (1994) 1-15
10. Beecher D.J., Schoeni J.L., and Wong A.C. Enterotoxic activity of hemolysin BL from Bacillus cereus. Infection and Immunity 63 (1995) 4423-4428
11. De Clerck E., Van M.K., Jannes G., Rossau R., and De V.P. Design of a 5' exonuclease-based real-time PCR assay for simultaneous detection of Bacillus licheniformis, members of the 'B. cereus group' and B. fumarioli in gelatine. Letters in Applied Microbiology 39 (2004) 109-115
12. De Santis E.P.L., Foddai A., Virdis S., Marongiu P., Pilo A.L., and Scarano C. Toxin gene pattern in Bacillus cereus group strains isolated from sheep ricotta cheese. Veterinary research communications 32 (2008) S323-S326
13. Dierick K., Van Coillie E., Swiecicka I., Meyfroidt G., Devlieger H., Meulemans A., Hoedemaekers G., Fourie L., Heyndrickx M., and Mahillon J. Fatal family outbreak of Bacillus cereus-associated food poisoning. Journal of Clinical Microbiology 43 (2005) 4277-4279
14. Ehling-Schulz M., Fricker M., and Scherer S. Bacillus cereus, the causative agent of an emetic type of food-borne illness. Molecular Nutrition & Food Research 48 (2004) 479-487
15. Ehling-Schulz M., Vukov N., Schulz A., Shaheen R., Andersson M., Martlbauer E., and Scherer S. Identification and partial characterization of the nonribosomal peptide synthetase gene responsible for cereulide production in emetic Bacillus cereus. Applied and Environmental Microbiology 71 (2005) 105-113
16. Ehling-Schulz M., Guinebretiere M.H., Monthan A., Berge O., Fricker M., and Svensson B. Toxin gene profiling of enterotoxic and emetic Bacillus cereus. FEMS Microbiology Letters 260 (2006) 232-240
17. Elizaquivel P., Chenoll E., and Aznar R. A TaqMan-based real-time PCR assay for the specific detection and quantification of Leuconostoc mesenteroides in meat products. FEMS Microbiology Letters 278 (2008) 62-71
18. European Food Safety Authority. The community summary report on trends and sources of Zoonoses, Zoonotic agents, antimicrobial resistance and foodborne outbreaks in the European Union in 2006. The EFSA Journal 130 (2007) 3-352
19. Fricker M., Messelhausser U., Busch U., Scherer S., and Ehling-Schulz M. Diagnostic real-time PCR assays for the detection of emetic Bacillus cereus strains in foods and recent food-borne outbreaks. Applied and Environmental Microbiology 73 (2007) 1892-1898
20. Fricker M., Reissbrodt R., and Ehling-Schulz M. Evaluation of standard and new chromogenic selective plating media for isolation and identification of Bacillus cereus. International Journal of Food Microbiology 121 (2008) 27-34
21. Fukushima H., Tsunomori Y., and Seki R. Duplex real-time SYBR green PCR assays for detection of 17 species of food- or waterborne pathogens in stools. Journal of Clinical Microbiology 41 (2003) 5134-5146
22. Fykse E.M., Olsen J.S., and Skogan G. Application of sonication to release DNA from Bacillus cereus for quantitative detection by real-time PCR. Journal of Microbiology Methods 55 (2003) 1-10
23. Gaviria Rivera A.M., Granum P.E., and Priest F.G. Common occurrence of enterotoxin genes and enterotoxicity in Bacillus thuringiensis. FEMS Microbiology Letters 190 (2000) 151-155
24. Gilbert R.J., de L.J., Donovan T., Little C., Nye K., Ribeiro C.D., Richards J., Roberts D., and Bolton F.J. Guidelines for the microbiological quality of some ready-to-eat foods sampled at the point of sale. PHLS Advisory Committee for Food and Dairy Products. Communicable disease and public health 3 (2000) 163-167
25. Goto M., Takahashi H., Segawa Y., Hayashidani H., Takatori K., and Hara-Kudo Y. Real-time PCR method for quantification of Staphylococcus aureus in milk. Journal of Food Protection 70 (2007) 90-96
26. Granum P.E. Bacillus cereus and food poisoning. In applications and systematics of Bacillus and relatives. In: Berkeley R., Heyndrickx M., Logan N., and De Vos P. (Eds) (2002), Blackwell Publishing, Oxford 37-46
27. Granum P.E., O'Sullivan K., and Lund T. The sequence of the non-haemolytic enterotoxin operon from Bacillus cereus. FEMS Microbiology Letters 177 (1999) 225-229
28. Guttmann D.M., and Ellar D.J. Phenotypic and genotyogypic comparisons of 23 strains from the Bacillus cereus complex for a selection of known and putative B. thuringiensis virulence factors. FEMS Microbiology Letters 188 (2000) 7-13
29. Hansen B.M., Leser T.D., and Hendriksen N.B. Polymerase chain reaction assay for the detection of Bacillus cereus group cells. FEMS Microbiology Letters 2002 (2001) 209-213
30. Hendriksen N.B., Hansen B.M., and Johansen J.E. Occurrence and pathogenic potential of Bacillus cereus group bacteria in a sandy loam. Antonie Van Leeuwenhoek 89 (2006) 239-249
31. Ivanova N., Sorokin A., Anderson I., Galleron N., Candelon B., Kapatral V., Bhattacharyya A., Reznik G., Mikhailova N., Lapidus A., Chu L., Mazur M., Goltsman E., Larsen N., D'Souza M., Walunas T., Grechkin Y., Pusch G., Haselkorn R., Fonstein M., Ehrlich S.D., Overbeek R., and Kyrpides N. Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature 423 (2003) 87-91
32. Kim Y.R., Czajka J., and Batt C.A. Development of a fluorogenic probe-based PCR assay for detection of Bacillus cereus in nonfat dry milk. Applied and Environmental Microbiology 66 (2000) 1453-1459
33. Knutsson R., Lofstrom C., Grage H., Hoorfar J., and Radstrom P. Modeling of 5' nuclease real-time responses for optimization of a high-throughput enrichment PCR procedure for Salmonella enterica. Journal of Clinical Microbiology 40 (2002) 52-60
34. Lopez-Enriquez L., Rodriguez-Lazaro D., and Hernandez M. Quantitative detection of Clostridium tyrobutyricum in milk by real-time PCR. Applied and Environmental Microbiology 73 (2007) 3747-3751
35. Ludwig W., Strunk O., Westram R., Richter L., Meier H., Yadhukumar B.A., Lai T., Steppi S., Jobb G., Forster W., Brettske I., Gerber S., Ginhart A.W., Gross O., Grumann S., Hermann S., Jost R., Konig A., Liss T., Lussmann R., May M., Nonhoff B., Reichel B., Strehlow R., Stamatakis A., Stuckmann N., Vilbig A., Lenke M., Ludwig T., Bode A., and Schleifer K.H. ARB: a software environment for sequence data. Nucleic Acids Research 32 (2004) 1363-1371
36. Lund T., De Buyser M.L., and Granum P.E. A new cytotoxin from Bacillus cereus that may cause necrotic enteritis. Molecular Microbiology 38 (2000) 254-261
37. Manzano M., Cocolin L., Cantoni C., and Comi G. Bacillus cereus, Bacillus thuringiensis and Bacillus mycoides differentiation using a PCR-RE technique. International Journal of Food Microbiology 81 (2003) 249-254
38. Pitcher D.G., Saunders N.A., and Owen R.J. Rapid extraction of bacterial genomic DNA with guanidium thiocyanate. Letters in Applied Microbiology 8 (1989) 151-156
39. Priha O., Hallamaa K., Saarela M., and Raaska L. Detection of Bacillus cereus group bacteria from cardboard and paper with real-time PCR. Journal of Industrial Microbiology & Biotechnology 31 (2004) 161-169
40. Prüss B.M., Francis K.P., von Stetten F., and Scherer S. Correlation of 16 S Ribosomal DNA Signature Sequences with Temperature-Dependent Growth Rates of Mesophilic and Psychrotolerant Strains of the Bacillus cereus Group. Journal of Bacteriology 181 (1999) 2624-2630
41. Radhika B., Padmapriya B.P., Chandrashekar A., Keshava N., and Varadaraj M.C. Detection of Bacillus cereus in foods by colony hybridization using PCR-generated probe and characterization of isolates for toxins by PCR. International Journal of Food Microbiology 74 (2002) 131-138
42. Rajkovic A., Uyttendaele M., Vermeulen A., Andjelkovic M., Fitz-James I., in't Veld P., Denon Q., Vérhe R., and Debevere J. Heat resistance of Bacillus cereus emetic toxin, cereulide. Letters in Applied Microbiology 46 (2008) 536-541
43. Reekmans R., Stevens P., Vervust T., and De V.P. An alternative real-time PCR method to detect the Bacillus cereus group in naturally contaminated food gelatine: a comparison study. Letters in Applied Microbiology 48 (2009) 97-104
44. Reyes J.E., Bastías J.M., Gutiérrez M.R., and Rodríguez M. Prevalence of Bacillus cereus in dried milk products used by Chilean School Feeding Program. Food Microbiology 24 (2007) 1-6
45. Rowan N.J. Viable but non-culturable forms of food and waterborne bacteria: Quo Vadis?. Trends in Food Science & Technology 15 (2004) 462-467
46. Rusul G., and Yaacob N.H. Prevalence of Bacillus cereus in selected foods and detection of enterotoxin using TECRA-VIA and BCET-RPLA. International Journal of Food Microbiology 25 (1995) 131-139
47. Schraft H., and Griffiths M.W. Specific oligonucleotide primers for detection of lecithinase-positive Bacillus spp. by PCR. Applied and Environmental Microbiology 61 (1995) 98-102
48. Stenfors Arnesen L.P., Fagerlund A., and Granum P.E. From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbioloy Reviews 32 (2008) 579-606
49. Turbull P.C.B., Jackson P.J., Hill K.K., Keim P., Kolsto A.B., and Beecher D.J. Longstanding taxonomic enigmas within the 'Bacillus Cereus Group' are on the verge of being resolved by far-reaching molecular developments: forecasts on the possible outcome by an ad hoc team. In: Berkeley R., Heyndrickx M., Logan N., and De Vos P. (Eds). In Applications and Systematics of Bacillus and Relatives (2002), Wiley-Blackwell 100-122
50. Vilas-Boas G.T., Peruca A.P., and Arantes O.M. Biology and taxonomy of Bacillus cereus, Bacillus anthracis, and Bacillus thuringiensis. Canadian Journal of Microbiology 53 (2007) 673-687
51. Wang R.F., Cao W.W., and Cerniglia C.E. A universal protocol for PCR detection of 13 species of foodborne pathogens in foods. Journal of Applied Microbiology 83 (1997) 727-736
52. Yang I.C., Shih D.Y., Huang T.P., Huang Y.P., Wang J.Y., and Pan T.M. Establishment of a novel multiplex PCR assay and detection of toxigenic strains of the species in the Bacillus cereus group. Journal of Food Protection 68 (2005) 2123-2130
53. Yang I.C., Shih D.Y., Wang J.Y., and Pani T.M. Development of rapid real-time PCR and most-probable-number real-time PCR assays to quantify enterotoxigenic strains of the species in the Bacillus cereus group. Journal of Food Protection 70 (2007) 2774-2781