How should staphylococcal food poisoning outbreaks be characterized?

Toxins

Volumn 2, Issue 8, 2010, Pages 2106-2116

  Hennekinne, Jacques Antoine ^a   Ostyn, Annick ^a   Guillier, Florence ^a   Herbin, Sabine ^a   Prufer, Anne Laure ^a   Dragacci, Sylviane ^a  

^a French Agency for Food   (France)

Author keywords

Enzyme immunoassay; Food poisoning; Mass spectrometry; Molecular tools; Staphylococcal enterotoxin

Indexed keywords

STAPHYLOCOCCUS ENTEROTOXIN;

ANTIGENICITY; ARTICLE; BACTERIAL GROWTH; BACTERIUM IDENTIFICATION; BIOASSAY; CLINICAL FEATURE; COAGULASE NEGATIVE STAPHYLOCOCCUS; ENZYME IMMUNOASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIDEMIC; FOOD ANALYSIS; FOOD CONTAMINATION; FOOD INTAKE; FOOD PROCESSING; FOOD STORAGE; GENE IDENTIFICATION; HEALTH HAZARD; HUMAN; IMMUNODETECTION; MASS SPECTROMETRY; MICROBIOLOGICAL EXAMINATION; MOLECULAR BIOLOGY; NONHUMAN; POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STAPHYLOCOCCAL FOOD POISONING; STAPHYLOCOCCUS AUREUS; TOXIN ANALYSIS; VOMITING;

BIOLOGICAL ASSAY; DISEASE OUTBREAKS; ENTEROTOXINS; HUMANS; IMMUNOENZYME TECHNIQUES; MASS SPECTROMETRY; POLYMERASE CHAIN REACTION; STAPHYLOCOCCAL FOOD POISONING; STAPHYLOCOCCUS AUREUS;

STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS;

EID: 79952085112     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins2082106     Document Type: Article

References (55)

1. Rosenbach, F.J. Microorganismen bei den Wund-Infections-Krankheiten des Menschen; Bergmann, J.F., Ed.; Wiesbaden, Germany, 1884; pp. 1-122.
2. De la Fuente, R.; Suarez, G.; Schleifer, K.H. Staphylococcus aureus subsp. Anaerobius subsp. nov., the causal agent of abscess disease of sheep. Int. J. Syst. Bacteriol. 1985, 35, 99-102.
3. Hajek, V. Staphylococcus intermedius, a New Species Isolated from Animals. Int. J. Syst. Bacteriol. 1976, 26, 401-408.
4. Devriese, L.A.; Hajek, K.; Oeding, P.; Meyer, S.A.; Schleifer, K.H. Staphylococcus hyicus (Sompolinsky 1953) comb. nov. and Staphylococcus hyicus subsp. chromogenes subsp. nov. Int. J. Syst. Bacteriol. 1978, 28, 482-490.
5. Varaldo, P.E.; Kilpper-Balz, R.; Biavasco, F.; Satta, G.; Scheifer, K.H. Staphylococcus delphini sp. nov., a coagulase-positive species isolated from dolphins. Int. J. Syst. Bacteriol. 1988, 38, 436-439.
6. Igimi, S.; Takahashi, E.; Mitsouka, T. Staphylococcus schleiferi subsp. coagulans subsp. nov., isolated from the external auditory meatus of dogs with external ear otitis. Int. J. Syst. Bacteriol. 1990, 40, 409-411.
7. Foster, G.; Ross, H.M.; Hutson, R.A.; Collins, M.D. Staphylococcus lutrae sp. nov., a new coagulase-positive species isolated from otters. Int. J. Syst. Bacteriol. 1997, 47, 724-726.
8. Balaban, N.; Rasooly, A. Staphylococcal enterotoxins. Int. J. Food Microbiol. 2000, 61, 1-10.
9. Orwin, P.M.; Leung, D.Y.; Donahue, H.L.; Novick, R.P.; Schlievert, P.M. Biochemical and Biological Properties of Staphylococcal Enterotoxin K. Infect. Immun. 2001, 69, 360-366.
10. Jarraud, S.; Peyrat, M.A.; Lim, A.; Tristan, A.; Bes, M.; Mougel, C.; Etienne, J.; Vandenesch, F.; Bonneville, M.; Lina, G. egc, a highly prevalent operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus. J. Immunol. 2001, 166, 669-677.
11. Omoe, K.; Imanishi, K.; Hu, D.L.; Kato, H.; Fugane, Y.; Abe, Y.; Hamaoka, S.; Watanabe, Y.; Nakane, A.; Uchiyama, T.; Shinagawa, K. Characterization of novel staphylococcal enterotoxin-like toxin type P. Infect. Immun. 2005, 73, 5540-5546.
12. Orwin, P.M.; Leung, D.Y.M.; Tripp, T.J.; Bohach, G.A.; Earhart, C.A.; Ohlendorf, D.H.; Schlievert, P.M. Characterization of a novel staphylococcal enterotoxin-like superantigen, a member of the group V subfamily of pyrogenic toxins. Biochemistry 2002, 41, 14033-14040.
13. Omoe, K.; Hu, D.L.; Takahashi-Omoe, H.; Nakane, A.; Shinagawa, K. Identification and characterization of a new staphylococcal enterotoxin-related putative toxin encoded by two kinds of plasmids. Infect. Immun. 2003, 71, 6088-6094.
14. Ono, H.K.; Omoe, K.; Imanishi, K.; Iwakabe, Y.; Hu, D.L.; Kato, H.; Saito, N.; Nakane, A.; Uchiyama, T.; Shinagawa, K. Identification and characterization of two novel staphylococcal enterotoxins types S and T. Infect. Immun. 2008, 76, 4999-5005.
15. Letertre, C.; Perelle, S.; Dilasser, F.; Fach, P. Identification of a new putative enterotoxin SEU encoded by the egc cluster of Staphylococcus aureus. J. Appl. Microbiol. 2003, 95, 38-43.
16. Thomas, D.Y.; Jarraud, S.; Lemercier, B.; Cozon, G.; Echasserieau, K.; Etienne, J.; Gougeon, M.L.; Lina, G.; Vandenesch, F. Staphylococcal enterotoxin-like toxins U2 and V, two new staphylococcal superantigens arising from recombination within the enterotoxin gene cluster. Infect. Immun. 2006, 74, 4724-4734.
17. Betley, M.J.; Mekalanos, J.J. Staphylococcal enterotoxin A is encoded by a phage. Science 1985, 229, 185-187.
18. Bayles, K.W.; Iandolo, J.J. Genetic and molecular analysis of gene encoding staphylococcal enterotoxin D. J. Bacteriol. 1989, 171, 4799-4806.
19. Yarwood, J.M; McCormick, J.K.; Paustian, M.L.; Orwin, P.M.; Kapur, V.; Schlievert, P.M. Characterization and expression analysis of Staphylococcus aureus pathogenicity island 3. Implications for the evolution of staphylococcal pathogenicity islands. Biol. Chem. 2002, 277, 13138-13147.
20. Papageorgiou, A.; Acharya, K. Microbial superantigens: from structure to function. Trends Microbiol. 2000, 8, 369-375.
21. Dinges, M.M.; Orwin, P.M.; Schlievert, P.M. Exotoxins of Staphylococcus aureus. Clin. Microbiol. Rev. 2000, 13, 16-34.
22. Papageorgiou, A.C.; Tranter, H.S.; Acharya, H.K. Crystal structure of microbial superantigen staphylococcal enterotoxin B at 1.5 Å resolution: Implications for superantigen recognition by MHC class II molecules and T-cell receptors. J. Mol. Biol. 1998, 277, 61-79.
23. Jablonski, L.; Bohach, G.A. Staphylococcus aureus. In Food microbiology fundamentals and frontiers; Doyle, M.P., Beuchat, L.R., Montville, T.J., Eds.; America society of Microbiology Press: Washington, DC, USA, 2001; pp. 411-434.
24. Asao, T.; Kumeda, Y.; Kawai, T.; Shibata, T.; Oda, H.; Haruki, K.; Nakazawa, H.; Kozaki, S. 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. 2003, 130, 33-40.
25. Pereira, M.L.; Do Carmo, L.; Dos Santos, E.J.; Pereira, J.L.; Bergdoll, M.S. Enterotoxin H in staphylococcal food poisoning. J. Food Prot. 1996, 59, 559-561.
26. The Community Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and food-borne outbreaks in the European Union in 2008. EFSA J. 2010, 1496. Available online: http://www.efsa.europa.eu/en/scdocs/doc/s1496.pdf (accessed on 6 August 2010).
27. Bryan, F.L.; Guzewich, J.J.; Todd, E.C.D. Surveillance of foodborne disease II. Summary and presentation of descriptive data and epidemiologic patterns; their value and limitations. J. Food Prot. 1997, 60, 567-578.
28. Surgalla, M.; Bergdoll, M.S.; Dack, G.M. Some observations on the assay of staphylococcal enterotoxin by the monkey feeding test. J. Lab. Clin. Med. 1953, 41, 782-788.
29. Bergdoll, M.S. Staphylococcal intoxications. In Food-borne Infections and Intoxications; Riemann, H., Bryan, F.L., Eds.; Academic press: New York, NY, USA, 1979; pp. 443-494.
30. Ikeda, T.; Tamate, N.; Yamaguchi, K.; Makino, S. Mass outbreak of food poisoning disease caused by small amounts of staphylococcal enterotoxins A and H. Appl. Environ. Microbiol. 2005, 71, 2793-2795.
31. Hawryluk, T.; Hirshfield, I. A super antigen bioassay to detect staphylococcal enterotoxin A. J. Food Prot. 2002, 65, 1183-1187.
32. Lee, Y.D.; Moon, B.Y.; Park, J.H.; Chang, H.I.; Kim, W.J. Expression of enterotoxin genes in Staphylococcus aureus isolates based on mRNA analysis. J. Microbiol. Biotechnol. 2007, 17, 461-467.
33. Akineden, O.; Hassan, A.A.; Schneider, E.; Usleber, E. Enterotoxigenic properties of Staphylococcus aureus isolated from goats' milk cheese. Int. J. Food Microbiol. 2008, 124, 211-216.
34. Derzelle, S.; Dilasser, F.; Duquenne, M.; Deperrois, V. Differential temporal expression of the staphylococcal enterotoxins genes during cell growth. Food Microbiol. 2009, 26, 896-904.
35. Duquenne, M.; Fleurot, I.; Aigle, M.; Darrigo, C.; Borezée-Dupont, E.; Derzelle, S.; Bouix, M.; Deperrois-Lafarge, V.; Delacroix-Buchet, A. Tool for Quantification of Staphylococcal Enterotoxin Gene Expression in Cheese. Appl. Environ. Microbiol. 2010, 76, 1367-1374.
36. Schlievert, P.M.; Case, L.C. Molecular analysis of staphylococcal superantigens. Methods Mol. Biol. 2007, 391, 113-126.
37. Park, C.E.; Akhtar, M. Rayman, M.K. Nonspecific reactions of a commercial enzyme-linked immunosorbent assay kit (TECRA) for detection of staphylococcal enterotoxins in foods. Appl. Environ. Microbiol. 1992, 58, 2509-2512.
38. Wieneke, A.A. Comparison of four kits for the detection of staphylococcal enterotoxin in foods from outbreaks of food poisoning. Int. J. Food Microbiol. 1991, 14, 305-312.
39. Macaluso, L.; Lapeyre, C.; Dragacci, S. Determination of influential factors during sample preparation for staphylococcal enterotoxin detection in dairy products. Analusis 1998, 26, 300-304.
40. Meyrand, A.; Atrache, V.; Bavai, C.; Montet, M.P.; Vernozy-Rozand, C. Evaluation of an alternative extraction procedure for enterotoxin determination in dairy products. Lett. Appl. Microbiol. 1999, 28, 411-415.
41. Lapeyre, C.; Maire, T.; Messio, S.; Dragacci, S. Enzyme immunoassay of staphylococcal enterotoxins in dairy products with cleanup and concentration by immunoaffinity column. J. AOAC Int. 2001, 84, 1587-1592.
42. European Community. Commission Regulation. No. 1441/2007 of 5 December 2007. Off. J. Eur. Union. 2007, L322, 12-29.
43. Bennett, R.W. Staphylococcal enterotoxin and its rapid identification in foods by enzyme-linked immunosorbent assay-based methodology. J. Food Prot. 2005, 68, 1264-1270.
44. Hennekinne, J.A.; Ostyn, A.; Guillier, F.; Gohier, M.; Messio, S.; Dragacci, S.; Krys, S.; Lombard, B. Interlaboratory validation of the Vidas SET2 detection kit for an use in official controls of staphylococcal enterotoxins detection in milk products especially low-fat cheeses. J. AOAC Int. 2007, 90, 756-764.
45. Lapeyre, C.; Janin, F.; Kaveri, S.V. Indirect double sandwich ELISA using monoclonal antibodies for detection of staphylococcal enterotoxins A, B, C1 and D in food samples. Food Microbiol. 1988, 5, 25-31.
46. Mamone, G.; Picariello, S.; Caira, F.; Addeo, P. Ferranti, P. Analysis of food proteins and peptides by mass spectrometry based techniques. J. Chromatogr. A 2009, 1216, 7130-7142.
47. Norrgran, J.; Williams, T.L.; Woolfitt, A.R.; Solano, M.I.; Pirkle, J.L.; Barr, J.R. Optimization of digestion parameters for protein quantification. Anal. Biochem. 2009, 393, 48-55.
48. Oeljeklaus, S.; Meyer, H.E.; Warscheid, B. New dimensions in the study of protein complexes using quantitative mass spectrometry. FEBS Lett. 2009, 583, 1674-1683.
49. Bernardo, K.; Pakulat, N.; Macht, M.; Krut, O.; Seifert, H.; Fleer, S.; Hunger F.; Kronke, M. Identification and discrimination of Staphylococcus aureus strains using matrix-assisted laser desorption/ionization-time of flight mass spectrometry. Proteomics 2002, 2, 747-753.
50. Callahan, J.H.; Shefcheck, K.J.; Williams, T.L.; Musser, S.M. Detection, confirmation, and quantification of staphylococcal enterotoxin B in food matrixes using liquid chromatography-mass spectrometry. Anal. Chem. 2006, 78, 1789-1800.
51. Brun, V.; Dupuis, A.; Adrait, A.; Marcellin, M.; Thomas, D.; Court, M.; Vandenesch, F.; Garin, J. Isotope-labeled protein standards: toward absolute quantitative proteomics. Mol. Cell Proteomics 2007, 6, 2139-2149.
52. Dupuis, A.; Hennekinne, J.A.; Garin, J.; Brun, V. Protein Standard Absolute Quantification (PSAQ) for improved investigation of staphylococcal food poisoning outbreaks. Proteomics 2008, 8, 4633-4636.
53. Kerouanton, A.; Hennekinne, J.A.; Letertre, C.; Petit, L.; Chesneau, O.; Brisabois, A.; De Buyser, M.L. Characterization of Staphylococcus aureus strains associated with food poisoning outbreaks in France. Int. J. Food Microbiol. 2007, 115, 369-375.
54. Ostyn, A.; De Buyser, M.L.; Guillier, F.; Groult, J.; Félix, B.; Salah, S.; Delmas, G.; Hennekinne, J.A. First evidence of a food poisoning outbreak due to staphylococcal enterotoxin type E, France, 2009. EuroSurveillance 2010, 15, 19528. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19528 (accessed on 13 July 2010).
55. Hennekinne, J.A.; Brun, V.; De Buyser, M.L.; Dupuis, A.; Ostyn, A.; Dragacci, S. Innovative contribution of mass spectrometry to characterise staphylococcal enterotoxins involved in food outbreaks. Appl. Environ. Microbiol. 2009, 75, 882-884.