Prevalence of toxicogenic bacteria in some foods and detection of Bacillus cereus and Staphylococcus aureus enterotoxin genes using multiplex PCR

Annals of Microbiology

Volumn 62, Issue 2, 2012, Pages 569-580

  Abdou, Mohamed A ^a   Awny, Nadia Mohammed ^a   Abozeid, Azza Abl Elaziz M ^a  

^a Zagazig University   (Egypt)

Author keywords

Bacillus cereus; Enterotoxin genes; Food borne pathogens; Protein profile; Staphylococcus aureus; Virulence factors

Indexed keywords

BACILLUS CEREUS; BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

EID: 84863845304     PISSN: 15904261     EISSN: 18692044     Source Type: Journal    
DOI: 10.1007/s13213-011-0293-7     Document Type: Article

References (72)

1. Agata N, Ohta M, Yokoyama K (2002) Production of Bacillus cereus emetic toxin (cerulide) in various foods. Int J Food Microbiol 73:23-27 (Pubitemid 34143082)
2. American Public Health Association (1992) Compendium ofmethods for the microbiological examination, 3rd edn. APHA, Washington D.C.
3. Argudin M, Mendoza M, Rodicio M (2010) Food poisoning and Staphylococcus aureus enterotoxins. Toxins 2(7):1751-1773
4. Balaban N, Rasooly A (2000) Staphylococcal enterotoxins. Int J Food Microbiol 61:1-10
5. Becker K, Roth R, Peters G (1998) Rapid and specific detection of toxigenic Staphylococcus aureus: use of two multiplex PCR enzyme immunoassays for amplification and hybridization of staphylococcal enterotoxin genes, exfoliative toxin genes, and toxic shock syndrome toxin 1 gene. J Clin Microbiol 36:2548-2553 (Pubitemid 28380953)
6. Beecher DJ, MacMillan JD (1990) A novel bicomponent haemolysin from Bacillus cereus. Infect Immun 58:2220-2227 (Pubitemid 20212299)
7. Beecher DJ, MacMillan JD (1991) Characterization of the components of haemolysin BL from Bacillus cereus. Infect Immun 59:1778-1784
8. Beecher DJ, Wong AC (1994) Identification of heamolysin Bl producing Bacillus cereus isolates by a discontinuous haemolytic pattern in blood agar. Appl Environ Microbiol 60:1646-1651 (Pubitemid 24144828)
9. Beecher DJ, Wong AC (2000) Cooperative, synergistic and antagonistic haemolytic interactions between haemolysin BL, phosphatidylcholine phospholipase C and sphingomyelinase from Bacillus cereus. Microbiology 146:3033-3039 (Pubitemid 32040811)
10. Bergdoll MS (1989) Staphylococcus aureus. In: Doyle MP (ed) Foodborne bacterial pathogens. Marcel Dekker, New York, pp 463-523
11. Bergdoll MS, Huang IY, Schantz EJ (1974) Chemistry of the staphylococcal enterotoxins. J Agric Food Chem 22(1):9-13
12. Boerema JA, Clemens R, Brightwel G (2006) Evaluation of molecular methods to determine enterotoxigenic status and molecular genotype of bovine, ovine, human and food isolates of Staphylococcus aureus. Int J Food Microbiol 107:192-201 (Pubitemid 43339778)
13. Callegan MC, Cochran DC, Kane ST, Gilmore MS, Gominet M, Lereclus D (2002) Contribution of membrane-damaging toxins to Bacillus endophthalmitis pathogenesis. Infect Immun 70:5381-5389
14. Difco Laboratories (1994) Difco manual: dehydrated culture media reagents for microbial, 10th edn. Difco Laboratories, Detroit
15. Dinges MM, Orwin PM, Schlievert PM (2000) Exotoxins of Staphylococcus aureus. Clin Microbiol Rev13:16-34 (Pubitemid 30039341)
16. Do Carmo LS, Cummings C, Linardi VR, Dias RS, De Souza JM, De Sena MJ, Dos Santos DA, Shupp JW, Peres Pereira RK, Jett M (2004) A case study of a massive staphylococcal food poisoning incident. Food Borne Pathogens Dis 1(4):241-246
17. Doyle MP (ed) (1989) Food borne bacterial pathogens. Marcel Dekker, New York
18. Drobniewski F (1993) Bacillus cereus and related species. Clin Microbiol Rev 4:324-338 (Pubitemid 23306590)
19. Duc LH, Dong TC, Logan NA, Sutherland AD, Taylor J, Cutting SM (2005) Cases of emesis associated with bacterial contamination of an infant breakfast cereal product. Int J Food Microbiol 102:245-251 (Pubitemid 40898130)
20. Federal Drug Administration (2001) Food and Drug Administration bacteriological analytical manual. FDA, Washington D.C.
21. FDA/CFSAN (2007) Bacillus cereus and other Bacillus spp. In: Food Borne pathogenic microorganisms and natural toxins handbook. Center for Food Safety and Applied Nutrition, U.S. Food and Drug Administration, Washington D.C. Available at: mow/las/dav/ear
22. Fernandez MM, De Marzi MC, Berguer P, Burzyn D, Langley RJ, Piazzon I, Mariuzza RA, Malchiodi EL (2006) Binding of natural variants of staphylococcal superantigens SEG and SEI to TCR and MHC class II molecule. Mol Immunol 43(7):927-938 (Pubitemid 41814410)
23. Fueyo JM, Martin MC, Gonzalez-Hevia MA, Mendoza MC (2001) Enterotoxin production and DNA fingerprinting in Staphylococcus aureus isolated from human and food samples. Relations between genetic types and enterotoxins. Int J Food Microbiol 67:139-145 (Pubitemid 32631422)
24. Granum PE (2001) Bacillus cereus. In: Doyle MP (ed) food microbiology fundamentals and frontiers. ASM Press, Washington D.C., pp 373-381
25. Granum PE, Baird-Parker TC (2000) Bacillus species. In: Lund B, Baird-Parker T, Gould G (eds) The microbiological safety and quality of food. Aspen Publ, Gaitherburg, pp 1029-1039
26. Granum PE, Lund T (1997) Bacillus cereus and its food poisoning toxins. FEMS Microbiol Lett 157:223-228 (Pubitemid 28248203)
27. Gravet A, Rondeau M, Harf-Monteil C, Grunenberger F, Monteil H, Scheftel JM, Prevost G (1999) Predominant Staphylococcus aureus isolated from antibiotic-associated diarrhea is clinically relevant and produces enterotoxin A and the bicomponent toxin LukE-LukD. J Clin Microbiol 37:4012-4019
28. Guinebretiere M, Fagerlund A, Granum PE, Nguyen-The C (2006) Rapid discrimination of cytK-1 and cytK-2 genes in Bacillus cereus strains by a novel PCR system. FEMS Microbiol Lett 59 (1):74-80
29. Hill WE (1996) The polymerase chain reaction: application for the detection of food borne pathogens. Crit Rev Food Sci Nutr 36:123-173
30. Hill WE, Keasler SP (1991) Identification of food borne pathogens by nucleic acid hybridization. Int J Food Microbiol 12:67-76
31. Jett M, Neill R, Welch C, Boyle T, Bernton E, Hoover D, Lowell G, Hunt RE, Chatterjee S, Gemski P (1994) Identification of staphylococcal enterotoxin B sequences important for induction of lymphocyte proliferation by using synthetic peptide fragments of toxin. Infect Immun 62(8):3408-3415 (Pubitemid 24232127)
32. Kenny K, Reiser RF, Bastida-Corcucra FD, Norcross NL (1993) Production of enterotoxins and toxic shock syndrome toxin by bovine mammary isolates of Staphylococcus aureus. J Clin Microbiol 31:706-707 (Pubitemid 23059895)
33. King NJ, Whyte R, Hudson JA (2007) Presence and significance of Bacillus cereus in dehydrated potatoes. J Food Protect 70 (2):514-520
34. Klotz M, Opper S, Heeg K, Zimmermann S (2003) Detection of Staphylococcus aureus Enterotoxins A to D by real-time Fluorescence PCR assay. J Clin Microbiol 41(10):4683-4687 (Pubitemid 37259777)
35. Kotiranta A, Lounatmaa K, Haapasalo M (2000) Epidemiology and pathogenesis of Bacillus cereus infections. Microbiol Infect 2:189-198 (Pubitemid 30154708)
36. Krieg NR, Holt JG (1984) Bergey's manual of systematic bacteriology, 9th edn, vol. 1, 2. Williams & Wilkins, Baltimore
37. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685
38. Letertre C, Perelle S, Dilasser F, Fach P (2003) Identification of a new putative enterotoxin SEU encoded by the egc cluster of Staphylococcus aureus. J Appl Microbiol 95:38-43 (Pubitemid 36791864)
39. Lindback T, Fagerlund A, Rodland MS, Granum PE (2004) Characterization of the Bacillus cereus Nhe enterotoxin. Microbiology 150:3959-3967 (Pubitemid 40045325)
40. LKB Application note (1997) SDS-PAGE. LKB, Sweden
41. Llewelyn M, Cohen J (2002) Superantigens: Microbial agents corrupt immunity. Lancet Infect Dis 2:156-162 (Pubitemid 34462450)
42. Lund T, Granum PE (1997) Comparison of biological effect of the two different enterobtoxin complexes isolated from three different strains of Bacilus cereus. Microbiology 143:3329-3336 (Pubitemid 27470182)
43. Lund T, Buyser ML De, Granum PE (2000) A new cytoxin from Bacillus cereus that may causenecrotic enteritis. Mol Microbiol 38: 254-261
44. Mahler H, Pasi A, Kramer JM, Schulte P, Scoging AC, Bar W, Krahenbuhl S (1997) Fulminant liver failure in association with emetic toxin of Bacillus cereus. N Engl J Med 336:1142-1148
45. Martin MC, Fueyo JM, Gonzalez-Hevia MA, Mendoza MC (2004) Genetic procedures for identification of enterotoxigenic strains of Staphylococcus aureus from three food poisoning outbreaks. Int J Food Microbiol 94(3):279-286 (Pubitemid 38891353)
46. Matsunaga T, Kamata S, Kakiichi N, Uccida A (1993) Characteristics of Staphylococcus aureus isolated from peracute, acute and chronic bovine mastitis. J Vet Med Sci 55:297-300
47. McKillip JL (2000) Prevalence and expression of enterotoxins in B. cereus and other B. spp., a literature review. Antonie van Leeuwenhoek 77:393-399 (Pubitemid 30614232)
48. McLauchlin J, Narayanan GL, Mithani V, O'Neill G (2000) The detection of enterotoxins and toxic shock syndrome toxin genes in Staphylococcus aureus by polymerase chain reaction. JFood Protect 63(4):479-488 (Pubitemid 30208700)
49. Miethke T, Wahl K, Heeg B, Echtenacher PH, Krammer HW (1992) T cell-mediated lethal shock triggered in mice by the superantigen staphylococcal enterotoxin B: critical role of tumor necrosis factor. J Exp Med 175:91-98
50. Misra AK, Kuila RK (1992) Use of Bifidobacterium bifidum in the manufacture of bifidus milk and its antibacterial activity. Lait 72 (2):213-220
51. Ngamwongsatit P, Busari W, Pianariyanon P, Pulsrikarn C, Ohba M, Assavanig A, Panbangred W (2008) Broad distribution of entertoxin genes (hblCDA, nheABC, cytK, and entFM) among Bacillus thuringiensis and Bacillus cereus as shown by novel primers. Int J Food Microbiol 121:352-356
52. Olsen JE (2000) DNA-based methods for detection of food-borne bacterial pathogens. Food Res Int 33(3-4):257-266
53. Olsen JE, Aabo S, Rasmussen OF, Rossen L (1995) Oligo-nucleotide probes specific for the genus Salmonella and for S. typhimurium. Lett Appl Microbiol 20:160-166
54. Ombui JN, Gitahi N, Gicheru M (2008) Direct detection of Bacillus cereus enterotoxin genes in food by multiplex polymerase chain reaction. Int J Integr Biol 2(3):172
55. Oxoid Ltd. (1990) Culture media, including in gradients and other laboratory services. Oxoid, London
56. Pinto B, Chenoll E, Aznar R (2005) Identification and typing of food borne Staphylococcus aureus by PCR-based techniques. Syst Appl Microbiol 37:4012-4019
57. Reinheimer JA, Demkow MR, Canditi MC, Austr B (1990) J Dairy Technol 45:5-9
58. Rhodehamel EJ, Harmon SM (2001) Bacteriological analytical manual online: chapter 14, Bacillus cereus. Center for Food Safety & Applied Nutrition, FDA, Washington D.C.
59. Schneider KR, Parish ME, Goodrich RM, Cookingham T (2004) Preventing food borne illness: Bacillus cereus and Bacillus anthracis. University of Florida, IFAS Extension. FSHNO04-05. Available at: http://edis.ifas.ufl.edu
60. Schoeni JL, Wong ACL (2005) B. cereus food poisoning and its toxins. J Food Protect 68:636-648 (Pubitemid 40346789)
61. Shaheen R, Andersson MA, Apetroaie C, Schulz V, Salkinoja-Salonen MS (2006) Potential of selected infant food formulas for production of Bacillus cereus emetic toxin, cerulide. Int J Food Microbiol 107(3):287-294
62. Smith BJ (1997) SDS polyacrylamide gel electrophoresis for Nterminal protein sequencing In: Smith BJ (ed) Methodsin molecular biology: protein sequencing protocols. Humana Press-Totowa
63. Smyth DS, Hartigan PJ, Meaney WJ, Fitzgerald JR, Deobald CF, Bohach GA, Smyth J (2005) Superantigen genes encoded by the egc cluster and SaPIbov are predominant among Staphylococcus aureus isolates from cows, goats, sheep, rabbits and poultry. J Med Microbiol 54(4):401-411 (Pubitemid 40489549)
64. Soriano JM, Font G, Molto JC, Manes J (2002) Enterotoxigenic staphylococci and their toxins in restaurant foods. Trends Food Sci Technol 13(2):60-67 (Pubitemid 35240917)
65. Su YC, Wong AL (1997) Current perspectives on detection of staphylococcal enterotoxins. J Food Protect 60:195-202
66. Svensson B, Monthan A, Guinebretiere HM, Nguyen C, Christiansson A (2007) Toxin production potential and the detection of toxin genes among strains of Bacillus cereus group isolated along the dairy production chain. Int Dairy J 17:1201-1208 (Pubitemid 47103258)
67. Todar K (2005) Textbook of bacteriology. The Genus Bacillus. Available at: http://www.textbookofbacteriology.net/Bacillus.html
68. Wolcott MJ (1991) DNA-based rapid methods for the detection of food borne pathogens. Journal Food Protect 54:387-401
69. Wooldridge K (2009) Secretory mechanisms and role pathogenesis. In: Wooldridge K (ed) bacterial secreted proteins. Caister Academic Press, London
70. Wong KKY, Hancock REW (2000) Insertion mutagenesis and membrane topology model of the Pseudomonasae ruginosa outer membrane protein OprM. J Bacteriol 182: 2402-2410 (Pubitemid 30212895)
71. Wu HJ, Wang AHJ, Jennings PM (2008) Discovery of virulence factors of pathogenic bacteria. Curr Opin Chem Biol 12:93-101
72. Yokoyama K, Ito M, Agata N, Isobe M, Shibayama K, Horii T, Ohta M (1999) Pathological effect of synthetic cerulide, an emetic toxin of Bacillus cereus, is reversible in mice. FEMS Immunol Med Microbiol 24:115-120 (Pubitemid 29189224)