Staphylococcal food poisoning: A current review

Archiv fur Lebensmittelhygiene

Volumn 61, Issue 6, 2010, Pages 220-228

  Johler, Sophia ^a   Stephan, Roger ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Food poisoning; Outbreak; Regulatory mechanisms; Staphylococcal enterotoxins; Superantigen

Indexed keywords

EID: 78651275662     PISSN: 0003925X     EISSN: None     Source Type: Journal    
DOI: 10.2376/0003-925X-61-220     Document Type: Article

References (69)

1. Asao T, Kumeda Y, Kawai T, Shibata T, Oda H, Haruki K, Nakazawa H, Kozaki S (2003): An extensive outbreak of staphylococcal food poisoning due to low-fat milk in Japan: estimation of enterotoxin A in the incriminated milk and powdered skim milk. Epidemiol Infect 130: 33-40.
2. Balaban N, Rasooly A (2000): Staphylococcal enterotoxins. Int J Food Microbiol 61: 1-10.
3. Bania J, Dabrowska A, Bystron J, Korzekwa K, Chrzanowska J, Molenda J (2006): Distribution of newly described enterotoxinlike genes in Staphylococcus aureus from food. Int J Food Microbiol 108: 36-41.
4. Bania J, Dabrowska A, Korzekwa K, Zarczynska A, Bystron J, Chrzanowska J, Molenda J (2006): The profiles of enterotoxin genes in Staphylococcus aureus from nasal carriers. Lett Appl Microbiol 42: 315-320.
5. Becker H, Bürk C, Märtlbauer E (2007): Staphylokokken- Enterotoxine: Bildung, Eigenschaften und Nachweis. JVL 2: 171-189.
6. Becker K, Friedrich AW, Lubritz G, Weilert M, Peters G, Von Eiff C (2003): Prevalence of genes encoding pyrogenic toxin superantigens and exfoliative toxins among strains of Staphylococcus aureus isolated from blood and nasal specimens. J Clin Microbiol 41: 1434-1439.
7. Bennett RW (2005): Staphylococcal enterotoxin and its rapid identification in foods by enzyme-linked immunosorbent assaybased methodology. J Food Prot 68: 1264-1270.
8. Betley M, Schlievert P, Bergdoll M, Bohach G, Iandolo J, Khan S, Pattee P, Reiser R (1990): Staphylococcal gene nomenclature. Am Soc Microbiol News 56: 182.
9. Bronner S, Monteil H, Prevost G (2004): Regulation of virulence determinants in Staphylococcus aureus: complexity and applications. FEMS Microbiol Rev 28:183-200.
10. Buzby J, Roberts T, Lin C, MacDonald J (1996): Bacterial foodborne disease: medical costs & productivity losses. USDA Agricultural Economic Report No 741.
11. Gasman E (1960): Further serological studies of staphylococcal enterotoxin. J Bacteriol 79: 849.
12. Casman E, Bergdoll M, Robinson J (1963): Designation of staphylococcal enterotoxins. J Bacteriol 85: 715.
13. Cheung AL, Bayer AS, Zhang G, Gresham H, Xiong YQ (2004): Regulation of virulence determinants in vitro and in vivo in Staphylococcus aureus. FEMS Immunol Med Microbiol 40: 1-9.
14. Chiang YC, Liao WW, Fan CM, Pai WY, Chiou CS, Tsen HY (2008): PCR detection of Staphylococcal enterotoxins (SEs) N, O, P, Q, R, U, and survey of SE types in Staphylococcus aureus isolates from food-poisoning cases in Taiwan. Int J Food Microbiol 121: 66-73.
15. Colombari V, Mayer MD, Laicini ZM, Mamizuka E, Franco BD, Destro MT, Landgraf M (2007): Foodborne outbreak caused by Staphylococcus aureus: phenotypic and genotypic characterization of strains of food and human sources. J Food Prot 70: 489-493.
16. Cowell NA, Hansen MT, Langley AJ, Graham TM, Bates JR (2002): Outbreak of staphylococcal enterotoxin food poisoning. Commun Dis Intell 26: 574-575.
17. de Jong JT, ten Brinke JM, van Ouwerkerk IM, Siebbeles MF, Fitz-James IA, in "t Veld PH (2004): [Large-scale, acute, bacterial gastroenteritis caused by the enterotoxin of Staphylococcus aureus after a barbecue]. Ned Tijdschr Geneeskd 148: 2136-2140.
18. Derzelle S, Dilasser F, Duquenne M, Deperrois V (2009): Differential temporal expression of the staphylococcal enterotoxins genes during cell growth. Food Microbiol 26: 896-904.
19. Dinges MM, Orwin PM, Schlievert PM (2000): Exotoxins of Staphylococcus aureus. Clin Microbiol Rev 13: 16-34.
20. Do Carmo L, Cummings C, Roberto Linardi V, Souza Dias R, Maria De Souza J, De Sena M, Aparecida Dos Santos D, Shupp J, Karla Peres Pereira R, Jett M (2004): A case study of a massive staphylococcal food poisoning incident. Foodborne Pathog Dis 1: 241-246.
21. Doyle M, Beuchat L (2007): Food Microbiology: Fundamentals and Frontiers. ASM Press Washington, DC.
22. Fueyo JM, Mendoza MC, Martin MC (2005): Enterotoxins and toxic shock syndrome toxin in Staphylococcus aureus recovered from human nasal carriers and manually handled foods: epidemiological and genetic findings. Microb Infect 7: 187-194.
23. Giezendanner N, Meyer B, Gort M, Muller P, Zweifel C (2009): [Raw milk-associated Staphylococcus aureus intoxication in children]. Schweiz Arch Tierheilkd 151: 329-331.
24. Harris TO, Grossman D, Kappler JW, Marrack P, Rich RR, Betley MJ (1993): Lack of complete correlation between emetic and T-cell-stimulatory activities of staphylococcal enterotoxins. Infect Immun 61: 3175-3183.
25. Holmberg SD, Blake PA (1984): Staphylococcal food poisoning in the United States. New facts and old misconceptions. J Am Med Assoc 251: 487-489.
26. Hu DL, Omoe K, Shimoda Y, Nakane A, Shinagawa K (2003): Induction of emetic response to staphylococcal enterotoxins in the house musk shrew (Suncus murinus). Infect Immun 71: 567-570.
27. Ikeda T, Tamate N, Yamaguchi K, Makino S (2005): Mass outbreak of food poisoning disease caused by small amounts of staphylococcal enterotoxins A and H. Appl Environ Microbiol 71: 2793-2795.
28. Jarraud S, Peyrat MA, Lim A, Tristan A, Bes M, Mougel C, Etienne J, Vandenesch F, Bonneville M, Lina G (2001): egc, a highly prevalent Operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus. J Immunol 166: 669-677.
29. Jay J, Loessner M, Golden D (2005): Modern food microbiology. Springer Verlag.
30. Jergensen HJ, Mathisen T, Lovseth A, Omoe K, Qvale KS, Loncarevic S (2005): An outbreak of staphylococcal food poisoning caused by enterotoxin H in mashed potato made with raw milk. FEMS Microbiol Lett 252: 267-272.
31. Katsuda K, Hata E, Kobayashi H, Kohmoto M, Kawashima K, Tsunemitsu H, Eguchi M (2005): Molecular typing of Staphylococcus aureus isolated from bovine mastitic milk on the basis of toxin genes and coagulase gene polymorphisms. Vet Microbiol 105: 301-305.
32. Kérouanton A, Hennekinne JA, Letertre C, Petit L, Chesneau O, Brisabois A, De Buyser ML (2007): Characterization of Staphylococcus aureus strains associated with food poisoning outbreaks in France. Int J Food Microbiol 115: 369-375.
33. Kitamoto M, Kito K, Niimi Y, Shoda S, Takamura A, Hiramatsu T, Akashi T, Yokoi Y, Hirano H, Hosokawa M, Yamamoto A, Agata N, Hamajima N (2009): Food poisoning by Staphylococcus aureus at a university festival. Jpn J Infect Dis 62: 242-243.
34. Kohler R, Krause G, Beutin L, Stephan R, Zweifel C (2008): Shedding of food-borne pathogens and microbiological carcass contamination in rabbits at slaughter. Vet Microbiol 132: 149-157.
35. Larkin EA, Carman RJ, Krakauer T, Stiles BG (2009): Staphylococcus aureus: the toxic presence of a pathogen extraordinaire. Curr Med Chem 16: 4003-4019.
36. Le Loir Y, Baron F, Gautier M (2003): Staphylococcus aureus and food poisoning. Gen Mol. Res 2: 63-76.
37. Lee YD, Moon BY, Park JH, Chang HI, Kim WJ (2007): Expression of enterotoxin genes in Staphylococcus aureus isolates based on mRNA analysis. J Microbiol Biotechnol 17: 461-467.
38. Lina G, Bohach G, Nair S, Hiramatsu K, Jouvin-Marche E, Mariuzza R (2004): Standard nomenclature for the superantigens expressed by Staphylococcus. J Infect Dis 189: 2334-2336.
39. McLauchlin J, Narayanan G, Mithani V, O'Neill G (2000): The detection of enterotoxins and toxic shock syndrome toxin genes in staphylococcus aureus by polymerase chain reaction. J Food Prot 63: 479-488.
40. Mitchell DT, Levitt DG, Schlievert PM, Ohlendorf DH (2000): Structural evidence for the evolution of pyrogenic toxin superantigens. J Mol. Evol 51: 520-531.
41. Miwa N, Kawamura A, Masuda T, Akiyama M (2001): An outbreak of food poisoning due to egg yolk reaction-negative Staphylococcus aureus. Int J Food Microbiol 64: 361-366.
42. Morandi S, Brasca M, Lodi R, Cremonesi P, Castiglioni B (2007): Detection of classical enterotoxins and identification of enterotoxin genes in Staphylococcus aureus from milk and dairy products. Vet Microbiol 124: 66-72.
43. Munson SH, Tremaine MT, Betley MJ, Welch RA (1998): Identification and characterization of staphylococcal enterotoxin types G and I from Staphylococcus aureus. Infect Immun 66: 3337-3348.
44. Nema V, Agrawal R, Kamboj DV, Goel AK, Singh L (2007): Isolation and characterization of heat resistant enterotoxigenic Staphylococcus aureus from a food poisoning outbreak in Indian subcontinent. Int J Food Microbiol 117: 29-35.
45. Nitzsche S, Zweifel C, Stephan R (2007): Phenotypic and genotypic traits of Staphylococcus aureus strains isolated from pig carcasses. Vet Microbiol 120: 292-299.
46. Novick R (2003): Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol. Microbiol 48: 1429-1449.
47. Novick R (2003): Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus. Plasmid 49: 93-105.
48. Omoe K, Hu DL, Takahashi-Omoe H, Nakane A, Shinagawa K (2005): Comprehensive analysis of classical and newly described staphylococcal superantigenic toxin genes in Staphylococcus aureus isolates. FEMS Microbiol Lett 246: 191-198.
49. Omoe K, Ishikawa M, Shimoda Y, Hu DL, Ueda S, Shinagawa K (2002): Detection of seg, seh, and sei genes in Staphylococcus aureus isolates and determination of the enterotoxin productivities of S. aureus isolates Harboring seg, seh, or sei genes. J Clin Microbiol 40: 857-862.
50. Orwin PM, Fitzgerald JR, Leung DY, Gutierrez JA, Bohach GA, Schlievert PM (2003): Characterization of Staphylococcus aureus enterotoxin L. Infect Immun 71: 2916-2919.
51. Orwin PM, Leung DY, Tripp TJ, Bohach GA, Earhart CA, Ohlendorf DH, Schlievert PM (2002): Characterization of a novel staphylococcal enterotoxin-like superantigen, a member of the group V subfamily of pyrogenic toxins. Biochemistry (Mose) 41: 14033-14040.
52. Ostyn A, De Buyser ML, Guillier F, Groult J, Felix B, Salah S, Delmas G, Hennekinne JA (2010): First evidence of a food poisoning outbreak due to staphylococcal enterotoxin type E, France, 2009. Euro Surveill 15.
53. Peles F, Wagner M, Varga L, Hein I, Rieck P, Gutser K, Kereszturi P, Kardos G, Turcsanyi I, Beri B, Szabo A (2007): Characterization of Staphylococcus aureus strains isolated from bovine milk in Hungary. Int J Food Microbiol 118: 186-193.
54. Pereira ML, DoCarmo LS, dosSantos EJ, Pereira JL, Bergdoll MS (1996): Enterotoxin H in staphylococcal food poisoning. J Food Prot 59: 559-561.
55. Rail VL, Vieira FP, Rail R, Vieitis RL, Fernandes A, Jr., Candeias JM, Cardoso KF, Araújo JP, Jr. (2008): PCR detection of staphylococcal enterotoxin genes in Staphylococcus aureus strains isolated from raw and pasteurized milk. Vet Microbiol 132: 408-413.
56. Ko̊zicková V, Karpísková R, Panto̊cek R, Pospíšilová M, Cerníková P, Doskar J (2008): Genotype analysis of enterotoxin Hpositive Staphylococcus aureus strains isolated from food samples in the Czech Republic. Int J Food Microbiol 121: 60-65.
57. Scherrer D, Corti S, Muehlherr JE, Zweifel C, Stephan R (2004): Phenotypic and genotypic characteristics of Staphylococcus aureus isolates from raw bulk-tank milk samples of goats and sheep. Vet Microbiol 101: 101-107.
58. Schmid D, Fretz R, Winter P, Mann M, Hoger G, Stoger A, Ruppitsch W, Ladstatter J, Mayer N, de Martin A, Allerberger F (2009): Outbreak of staphylococcal food intoxication after consumption of pasteurized milk products, June 2007, Austria. Wien Klin Wochenschr 121: 125-131.
59. Schmid D, Gschiel E, Mann M, Huhulescu S, Ruppitsch W, Bohm G, Pichler J, Lederer I, Hoger G, Heuberger S, Allerberger F (2007): Outbreak of acute gastroenteritis in an Austrian boarding school, September 2006. Euro Surveill 12: 224.
60. Srinivasan V, Sawant AA, Gillespie BE, Headrick SJ, Ceasaris L, Oliver SP (2006): Prevalence of enterotoxin and toxic shock syndrome toxin genes in Staphylococcus aureus isolated from milk of cows with mastitis. Foodborne Pathog Dis 3: 274-283.
61. Stephan R, Annemulier C, Hassan AA, Lammler C (2001): Characterization of enterotoxigenic Staphylococcus aureus strains isolated from bovine mastitis in north-east Switzerland. Vet Microbiol 78: 373-382.
62. Su YC, Wong AC (1995): Identification and purification of a new staphylococcal enterotoxin, H. Appl Environ Microbiol 61: 1438-1443.
63. Thomas D, Chou S, Dauwalder O, Lina G (2007): Diversity in Staphylococcus aureus enterotoxins. Chem Immunol Allergy 93: 24-41.
64. Tseng CW, Stewart GC (2005): Rot repression of enterotoxin B expression in Staphylococcus aureus. J Bacteriol 187: 5301-5309.
65. Tseng CW, Zhang S, Stewart GC (2004): Accessory gene regulator control of staphyloccoccal enterotoxin D gene expression. J Bacteriol 186: 1793-1801.
66. Ward K, Hammond R, Katz D, Hallman D (1997): Outbreak of staphylococcal food poisoning associated with precooked ham - Florida, 1997. Morb Mortal Weekly Rep 46: 1189-1191.
67. Wieneke AA (1974): Enterotoxin production by strains of Staphylococcus aureus isolated from foods and human beings. J Hyg 73: 255-262.
68. Zhang S, Stewart GC (2000): Characterization of the promoter elements for the staphylococcal enterotoxin D gene. J Bacteriol 182: 2321-2325.
69. Zschöck M, Kloppert B, Wolter W, Hamann HP, Lammler C (2005): Pattern of enterotoxin genes seg, seh, sci and sej positive Staphylococcus aureus isolated from bovine mastitis. Vet Microbiol 108: 243-249.