Current perspectives on detection of Staphylococcal enterotoxins

Journal of Food Protection

Volumn 60, Issue 2, 1997, Pages 195-202

  Yi Cheng, S U ^a   Lee Wong, Amy C ^a  

^a UNIVERSITY OF WISCONSIN   (United States)

Author keywords

enterotoxin detection; food poisoning; Staphylococcus aureus

Indexed keywords

STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; THEOBROMA CACAO;

EID: 0030945991     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028x-60.2.195     Document Type: Article

References (97)

1. Adesiyun, A. A., S. R. Tatini, and D. G. Hoover. 1984. Production of enterotoxin(s) by Stapltylococcus liyicus. Vet. Microbiol 9:487-495.
2. Anonymous. 1992. Outbreak that didn't seem right spread like butter. Food Prot. Rep. 8(7-8): 5-6.
3. Association of Official Analytical Chemists. 1984. Official methods of analysis, 14th ed. AOAC, Arlington, VA.
4. Avena, R. M., and M. S. Bergdoll. 1967. Purification and some physicochemical properties of enterotoxin C, Staphylococcus aureus strain 361. Biochemistry 6:1474-1480.
5. Bautista, L., P. Gaya, M. Medina, and M. Nunez. 1988. A quantitative study of enterotoxin production by sheep milk staphylococci. Appl. Environ. Microbiol. 54:4799-4806.
6. Bayles, K. W., and J. J. landolo. 1989. Genetic and molecular analyses of the gene encoding staphylococcal enterotoxin D. J. Bacteriol. 171:4799-4806.
7. Bennett, R. W., and F. McClure. 1994. Visual screening with enzyme immunoassay for staphylococcal enterotoxins in foods: collaborative study. J. AOAC Int. 77:357-364.
8. Bennett, R. W., S. Notermans, and S. R. Tatini. 1992. Staphylococcal enterotoxins, p. 551-592. In C. Vanderzant and D. F. Splittstoesser (ed.). Compendium of methods for the microbiological examination of foods, 3rd ed. American Public Health Association, Washington, D.C.
9. Bergdoll, M. S. 1972. The enterotoxins, p. 301-331. In J. O. Cohen (ed.). The staphylococci. John Wiley & Sons, Inc., New York.
10. Bergdoll, M. S. 1979. Staphylococcal intoxications, p. 443-494. In H. Riemann and F. C. Bryan (ed.), Food-borne infections and intoxications, 2nd ed. Academic Press, Inc., New York.
11. Bergdoll, M. S. 1983. Enterotoxins, p. 559-598. In C. Adlam and C. S. F. Easman (ed.), Staphylococci and staphylococcal infections, vol. 2. Academic Press, Inc., London.
12. Bergdoll, M. S. 1989. Staphylococcus aureus, p. 463-523. In M. P. Doyle (ed.), Foodbome bacterial pathogens. Marcel Dekker, Inc., New York.
13. Bergdoll, M. S. 1994. The AOAC official methods for detection of staphylococcal enterotoxins in foods. J. AOAC Int. 77:31 A.
14. Bergdoll, M. S. 1995. Importance of staphylococci that produce nanogram quantities of enterotoxin. Zentralbl. Bakteriol. 282:1-6.
15. Bergdoll, M. S., C. R. Borja, and R. M. Avena. 1965. Identification of a new enterotoxin as enterotoxin C. J. Bacteriol. 90:1481-1485.
16. Bergdoll, M. S., C. R. Borja, R. H. Robbins, and K. F. Weiss. 1971. Identification of enterotoxin E. Infect. Immun. 4:593-595.
17. Bergdoll, M. S., B. A. Crass, R. F. Reiser, R. N. Robbins, and J. P. Davis. 1981. A new staphylococcal enterotoxin, enterotoxin F, associated with toxic-shock-syndrome Staphylococcus aureus isolates. Lancet ii:1017-1021.
18. Bergdoll, M. S., M. J. Surgalla, and G. M. Dack. 1959. Staphylococcal enterotoxin-identification of a specific precipitating antibody with enterotoxin-neutralizing property. J. Immunol. 83:334-338.
19. Berry, P. R., A. A. Wieneke, J. C. Rodhouse, and R. J. Gilbert. 1987. Use of commercial kits for the detection of Clostridiiim perfringens and Staphylococcus aurais enterotoxins, p. 245-254. In J. M. Grange, A. Fox, and N. L. Morgan (ed.), Immunological techniques in microbiology. Blackwell Scientific Publications, London.
20. Betley, M. J., D. W. Borst, and L. B. Regassa. 1992. Staphylococcal enterotoxins, toxic shock syndrome toxin and streptococcal pyrogenic exotoxins: a comparative study of their molecular biology. Chem. Immunol.55:l-35.
21. Betley, M. J., and J. J. Mekalanos. 1988. Nucleotide sequence of the type A Staphylococcal enterotoxin gene. J. Bacteriol. 170:34-41.
22. Bhatti, A. R., Y. M. Siddiqui, and V. V. Micusan. 1994. Highly sensitive fluorogenic enzyme-linked immunosorbent assay: detection of Staphylococcal enterotoxin B. J. Microbiol. Methods 19:179-187.
23. Bohach.G.A., and P.M. Schlievert. 1987. Nucleotide sequence of the Staphylococcal enterotoxin C\ gene and relatedness to other pyrogenic toxins. Mol. Gen. Genet. 209:15-20.
24. Bohach, G. A., and P. M. Schlievert. 1989. Conservation of the biologically active portions of Staphylococcal enterotoxins C| and 2Infect. Immun. 57:2249-2252.
25. Borja, C. R., and M. S. Bergdoll. 1967. Purification and partial charactenzation of enterotoxin C produced by Staphylococcus aureus strain 137. Biochemistry 6:1467-1473.
26. Borja, C. R., E. Fanning, I-Y. Huang, and M. S. Bergdoll. 1972. Purification and some physicochemical properties of Staphylococcal enterotoxin E. J. Biol. Chem. 247:2456-2463.
27. Breckinridge, J. C., and M. S. Bergdoll. 1971. Outbreak of food-borne gastroenteritis due to a coagulase-negative enterotoxin-producing Staphylococcus. N. Engl. J. Med. 284:541-543.
28. Casman, E. P. 1960. Further serological studies of Staphylococcal enterotoxin. J. Bacteriol. 79:849-856.
29. Casman, E. P., R. W. Bennett, A. E. Dorsey, and J. A. Issa. 1967. Identification of a fourth Staphylococcal enterotoxin D. J. Bacteriol. 94:1875-1882.
30. Casman, E. P..R.W. Bennett.A. E. Dorsey, and J. E. Stone. 1969. The micro-slide gel double diffusion test for the detection and assay of Staphylococcal enterotoxins. Health Lab. Sei. 6:185-198.
31. Casman, E. P., M. S. Bergdoll, and J. Robinson. 1963. Designation of Staphylococcal enterotoxins. J. Bacteriol. 85:715-716.
32. Chang, H.-C, and M. S. Bergdoll. 1979. Purification and some ' physicochemical properties of Staphylococcal enterotoxin D. Biochemistry 18:1937-1942.
33. Collins, W. S., A. D. Johnson, J. F. Metzger, and R. W. Bennett. 1973. Rapid solid-phase radioimmunoassay for Staphylococcal enterotoxin A. Appl. Microbiol. 25:774-777.
34. Collins, W. S., II, J. F. Metzger, and A. D. Johnson. 1972. A rapid solid phase radioimmunoassay for Staphylococcal B enterotoxin. J. Immunol. 108:852-856. '
35. Couch, J. L., and M. J. Betley. 1989. Nucleotide sequence of the type C3 Staphylococcal enterotoxin gene suggests that intergenic recombination causes antigenic variation. J. Bacteriol. 171:4507-4510.
36. Couch, J. L., M. T. Soltis, and M. J. Betley. 1988. CIcning and nucleotide sequence of the type E Staphylococcal enterotoxin gene. J. Bacteriol. 170:2954-2960.
37. Davison, E., G. M. Dack, and W. E. Cary. 1938. Attempts to assay the enterotoxic substance produced by staphylococci by parenteral injection of monkeys and kittens. J. Infect. Dis. 62:219-223.
38. Devriese, L. A., V. Hajek, P. Oeding, S.A. Meyer. and K. H. Schleifer. 1978. Staphylococcus hyicus (Sompolinsky 1953) comb. nov. and Staphylococcus hyicus subsp. chromogenes subsp. nov. Int. J. Syst. Bacteriol. 28:482-190.
39. Dickie, N., and S. M. Akhtar. 1982. Improved radioimmunoassay of Staphylococcal enterotoxin A. J. Assoc. Off. Anal. Chem. 65:180-184.
40. Dolman, C. E., R. J. Wilson, and W. H. Cockcroft. 1936. A new method of detecting Staphylococcus enterotoxin. Can. Public Health J. 27:489-193.
41. Edwin, C, S. R. Tatini, R. S. Strobel, and S. K. Maheswaran. 1984. Production of monoclonal antibodies to Staphylococcal enterotoxin A. Appl. Environ. Microbiol. 48:1171-1175.
42. Evenson, M. L., M. W. Hinds, R. S. Bernstein, and M. S. Bergdoll. 1988. Estimation of human dose of Staphylococcal enterotoxin A from a large outbreak of Staphylococcal food poisoning involving chocolate milk. Int. J. Food Microbiol. 7:311-316.
43. Fey, H., H. Pfister, and O. Rüegg. 1984. Comparative evaluation of different enzyme-linked immunosorbent assay systems for the detec-lion of staphylococcal enterotoxins A, B, C and D. J. Clin. Microbiol. 19:34-38.
44. Food and Drug Administration. 1995. Bacteriological analytical manual, 8th éd. AOAC International, Arlington, VA.
45. Freed, R. C., M. L. Evenson, R. F. Reiser, and M. S. Bergdoll. 1982. Enzyme-linked immunosorbent assay for detection of staphylococcal enterotoxins in food. Appl. Environ. Microbiol. 44:1349-1355.
46. Fujikawa, H., and H. Igarashi. 1988. Rapid latex agglutination test for detection of staphylococcal enterotoxins A to E that uses high-density latex particles. Appl. Environ. Microbiol. 54:2345-2348.
47. Hahn, I. F., P. Pickenhahn, W. Lenz, and H. Brandis. 1986. An avidin-biotin ELISA for the detection of staphylococcal enterotoxin A and B. J. Immunol. Methods. 92:25-29.
48. Hâjek, V. 1976. Slaphylococcus intennedius, a new species isolated from animals. Int. J. Syst. Bacteriol. 26:401-408.
49. Hammon, W. M. 1941. Staphylococcus enterotoxin: an improved cat test, chemical and immunological studies. Am. J. Public Health. 31:1191-1198.
50. Holmberg, S. D., and P. A. Blake. 1984. Staphylococcal food poisoning in the United States: new facts and old misconceptions. JAM A 251:487-489.
51. Huang, I. Y., J. L. Hughes, M. S. Bergdoll, and E. J. Schantz. 1987. Complete amino acid sequence of staphylococcal enterotoxin A. J. Biol. Chem. 262:7006-7013.
52. Huang, I.-Y., T. Shih, C. R. Borja, R. M. Avena, and M. S. Bergdoll. 1967. Amino acid composition and terminal amino acids of staphylococcal enterotoxin C. Biochemistry 6:1480-1484.
53. Inganäs, M., S. G. O. Johansson, and H. H. Bennich. 1980. Interaction of human polyclonal IgE and IgG from different species with protein A from Staphylococcus aureus: demonstration of protein-A-reactive sites located in the Fab2 fragment of human IgG. Scand. J. Immunol. 12:23-31.
54. Jay, J. M. 1986. Staphylococcal gastroenteritis, p. 437-458. In J. M. Jay (ed.), Modem food microbiology, 3rd ed. Van Nostrand Reinhold Company Inc., New York.
55. Johnson'.'H. M., J. A. Bukovic, and P. E. Kauffmann. 1973. Staphylococcal enterotoxins A and B: solid-phase radioimmunoassay in food. Appl. Microbiol. 26:309-313.
56. Johnson, W. M., S. D. Tyler, E. P. Ewan, F. E. Ashton, D. R. Pollard, and K. R. Rozee. 1991. Detection of genes for enterotoxins, exfoliative toxins, and toxic shock syndrome toxin 1 in Staphylococcus aureus by the polymerase chain reaction. J. Clin. Microbiol. 29:426430.
57. Jones, C. L., and S. A. Khan. 1986. Nucleotide sequence of the enterotoxin B gene from Staphylococcus aureus. J. Bacteriol. 166: 29-33.
58. Kauffman, P. E. 1980. Enzyme immunoassay for staphylococcal enterotoxin A. J.Assoc. Off. Anal. Chem. 63:1138-1143.
59. Kokan, N. P., and M. S. Bergdoll. 1987. Detection of low-enterotoxinproducing Staphylococcus aureus strains. Appl. Environ. Microbiol. 53:2675-2676.
60. Koper, J. W., A. M. Hagenaars, and S. Notermans. 1980. Prevention of cross-reactions in the enzyme-linked immunosorbent assay (ELISA) for the detection of Slaphylococcus aureus enterotoxin type B in culture filtrates and foods. J. Food Safety 2:35-45.
61. Lampel, K. A., J. A. Jagow, M. Trucksess, and W. E. Hill. 1990. Polymerase chain reaction for detection of invasive Shigella flexneri in food. Appl. Environ. Microbiol. 56:1536-1540.
62. Lapeyre, C., F. Janin, and S. V. Kaveri. 1988. Indirect double sandwich ELISA using monoclonal antibodies for detection of staphylococcal enterotoxins A, B, C] and D in food samples. Food Microbiol. 5:25-31.
63. Lapeyre, C., S. V. Kaveri, F. Janin, and A. D. Strosberg. 1987. Production and characterization of monoclonal antibodies to staphylococcal enterotoxins: use in immunodetection and immunopurification. Mol. Immunol. 24:1243-1254.
64. Lindroth, S., and A. Niskanen. 1977. Double antibody solid-phase radioimmuno-assay for staphylococcal enterotoxin A. Eur. J. Appl. Microbiol. 4:137-143.
65. Meyer, R. F., L. Miller, R. W. Bennett, and J. D. Macmillan. 1984. Development of a monoclonal antibody capable of interacting with five serotypes of Slaphylococcus aureus enterotoxin. Appl. Environ. Microbiol. 47:283-287.
66. Meyer, R. F., and M. J. Palmieri. 1980. Single radial immunodiffusion method for screening staphylococcal isolates for enterotoxin. Appl. Environ. Microbiol. 40:1080-1085.
67. Miller, B. A., R. F. Reiser, and M. S. Bergdoll. 1978. Detection of staphylococcal enterotoxins A, B, C, D, and E in foods by radioimmunoassay, using staphylococcal cells containing protein A as immunoadsorbent. Appl. Environ. Microbiol. 36:421-126.
68. Munson, S. H., and M. J. Betley. 1991. Partial characterization of a new staphylococcal enterotoxin gene, abstr. B-36, p. 31. Abstr. 91st Annu. Meet. Am. Soc. Microbiol. 1991.
69. Notermans, S., P. Timmermans, and J. Nagel. 1982. Interaction of staphylococcal protein A in enzyme-linked immunosorbent assays for detecting staphylococcal antigens. J. Immunol. Methods 55:35-41.
70. Orden, J. A., J. Goyache, J. Hernandez, A. Domenech, G. Suarez, and E. Gomez-Lucia. 1992. Production of staphylococcal enterotoxins and TSST-1 by coagulase negative staphylococci isolated from ruminant mastitis. J. Vet. Med. B. 39:144-148.
71. Ouchterlony, 0. 1949. Antigen-antibody reactions in gels. Acta Path. Microbiol. Scand. 25:507-515.
72. Park, C. E., M. Akhtar, and M. K. Rayman. 1992. Nonspecific reactions of a commercial enzyme-linked immunosorbent assay kit (TECRA) for detection of staphylococcal enterotoxins in foods. Appl. Environ. Microbiol. 58:2509-2512.
73. Park, C. E., M. Akhtar, and M. K. Rayman. 1994. Evaluation of a commercial enzyme immunoassay kit (RIDASCREEN) for detection of staphylococcal enterotoxins A, B, C, D, and E in foods. Appl. Environ. Microbiol. 60:677-681.
74. Park, C. E., D. Warburton, P. J. Laffey, and Collaborators. 1996. A collaborative study on the detection of staphylococcal enterotoxins in foods with an enzyme immunoassay kit (TECRA). J. Food Prot. 59:390-397.
75. Reiser, R., D. Conaway, and M. S. Bergdoll. 1974. Detection of staphylococcal enterotoxin in foods. Appl. Microbiol. 27:83-85.
76. Reiser, R. F., R. N. Robbins, G. P. Khoe, and M. S. Bergdoll. 1983. Purification and some physicochemical properties of toxic-shock toxin. Biochemistry 22:3907-3912.
77. Reiser, R. F., R. N. Robbins, A. L. Noleto, G. P. Khoe, and M. S. Bergdoll. 1984. Identification, purification, and some physicochemical properties of staphylococcal enterotoxin C3. Infect. Immun. 45:625-630.
78. Ren, K., J. D. Bannan, V. Pancholi, A. L. Cheung, J. C. Robbins, V. A. Fischetti, and J. B. Zabriskie. 1994. Characterization and biological properties of a new staphylococcal exotoxin. J. Exp. Med. 180:16751683.
79. Robbins, R., S. Gould, and M. S. Bergdoll. 1974. Detecting the enterotoxigenicity of Staphylococcus aiireiis strains. Appl. Microbiol. 28:946-950.
80. Robem, H., M. Dighton, Y. Yano, and N. Dickie. 1975. Doubleantibody radioimmunoassay for staphylococcal enterotoxin C2. Appl. Microbiol. 30:525-529.
81. Saunders, G. C., and M. L. Bartlett. 1977. Double-antibody solidphase enzyme immunoassay for the detection of staphylococcal enterotoxin A. Appl. Environ. Microbiol. 34:518-522.
82. Schantz, E. J., W. G. Roessler, J. Wagman, L. Spero, D. A. Dunnery, and M. S. Bergdoll. 1965. Purification of staphylococcal enterotoxin B. Biochemistry 4:1011-1016.
83. Schantz, E. J., W. G. Roessler, M. J. Woodbum, J. M. Lynch, H. M. Jacoby, S. J. Silverman, J. C. German, and L. Spero. 1972. Purification and some chemical and physical properties of staphylococcal enterotoxin A. Biochemistry 11:360-366.
84. Scheuber, P. H., H. Mussmann, G. Beck, and D. K. Hammer. 1983. Direct skin test in highly sensitized guinea pigs for rapid and sensitive determination of staphylococcal enterotoxin B. Appl. Environ. Microbiol. 46:1351-1356.
85. Shingaki, M., H. Igarashi, H. Fujikawa, H. Ushioda, T. Terayama, and S. Sakai. 1981. Study on reversed passive latex agglutination for the detection of staphylococcal enterotoxins A-C. Ann. Rep. Tokyo Metr. Res. Lab. Public Health 32-1:128-131.
86. Sokari, T. G., and S. O. Anozie. 1989. Modified single radial immunodiffusion method for screening staphylococcal isolates for enterotoxin. Food Microbiol. 6:45-48.
87. Spero, L., D. Stefanye, P. I. Brecher, H. M. Jacoby, J. E. Dalidowicz, and E. J. Schantz. 1965. Amino acid composition and terminal amino acids of staphylococcal enterotoxin B. Biochemistry 4:1024-1030.
88. Stifïïer-Rosenberg, G., and H. Fey. 1978. Simple assay for staphylococcal enterotoxins A, B, and C: modification of enzyme-linked immunosorbent assay. J. Clin. Microbiol. 8:473-479.
89. Su, Y.-C., and A. C. Lee Wong. 1995. Identification and purification of a new staphylococcal enterotoxin, H. Appl. Environ. Microbiol. 61:1438-1443.
90. Su, Y.-C., and A. C. Lee Wong. 1996. Detection of staphylococcal enterotoxin H by an enzyme-linked immunosorbent assay. J. Food Prot. 59:327-330.
91. Surgalla, M. J., M. S. Bergdoll, and G. M. Dack. 1953. Some observations on the assay of staphylococcal enterotoxin by the monkey-feeding test. J. Lab. Clin. Med. 41:782-788.
92. Thompson, N. E., M. J. Ketterhagen, and M. S. Bergdoll. 1984. Monoclonal antibodies to staphylococcal enterotoxins B and C: cross-reactivity and localization of epitopes on tryptic fragments. Infect. Immun. 45:281-285.
93. Todd, E. C. D. 1989. Preliminary estimates of costs of foodborne disease in the United States. 1989. J. Food Prot. 52:595-601.
94. Tsen, H.-Y., and T.-R. Chen. 1992. Use of the polymerase chain reaction for specific detection of type A, D and E enterotoxigenic Staphylococcus aiireus in foods. Appl. Microbiol. Biotechnol. 37:685690.
95. Wieneke, A. A. 1991. Comparison of four kits for the detection of staphylococcal enterotoxin in foods from outbreaks of food poisoning. Int. J. Food Microbiol. 14:305-312.
96. Williams, R. E. O. 1963. Healthy carriage of Staphylococcus aiireus: its prevalence and importance. Bacteriol. Rev. 27:56-71.
97. Wilson, I. G., J. E. Cooper, and A. Gilmour. 1991. Detection of enterotoxigenic Staphylococcus aiireus in dried skimmed milk: use of the polymerase chain reaction for amplification and detection of staphylococcal enterotoxin genes entB and entC/ and the thermonuclease gene mtc. Appl. Environ. Microbiol. 57:1753-1798.