Chapter 8 : Staphylococcal Food Poisoning

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This chapter focuses predominantly on staphylococcal food poisoning (SFP), another toxin-mediated illness. SFP, also known as staphylococcal gastroenteritis, is not an infection but is a foodborne intoxication caused by one or more staphylococcal enterotoxins (SEs). It appears to have been initially reported in 1894 as a family outbreak due to undercooked meat from a sick cow that became contaminated with . Staphylococci are often divided into coagulasepositive staphylococci and coagulase-negative staphylococci (CNS), on the basis of coagulase production or the presence of a coagulase gene. Staphylococcal osmotolerance is problematic for food safety since blocked growth of competing bacteria can result in a more likely overgrowth of . Staphylococci are ubiquitous in air, dust, sewage, water, milk, and many foods and on food equipment, environmental surfaces, humans, and animals. SE production is affected by temperature, pH, and osmotic conditions and is also regulated at the molecular level. The oligonucleotideoligosaccharide- binding fold containing a β-barrel structure capped with an α-helix comprises much of one domain and is present in other toxins including cholera toxin, pertussis toxin, and Shiga toxin. Recent studies demonstrated that staphylococcal pathogenicity island (SaPI) is mobilized by staphylococcal bacteriophages and endogenous prophages, suggesting that SE genes might be transferred horizontally. The identification of novel toxins and improved methods of detection have also indicated that SE production is much more widespread than originally thought and includes species of staphylococci other than .

Citation: Seok Seo K, Bohach G. 2010. Staphylococcal Food Poisoning, p 119-130. In Juneja V, Sofos J (ed), Pathogens and Toxins in Foods. ASM Press, Washington, DC. doi: 10.1128/9781555815936.ch8

Key Concept Ranking

Toxic Shock Syndrome Toxin 1
Major Histocompatibility Complex Class II
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Image of Figure 1.
Figure 1.

Ribbon diagram of SEC3. The figure is oriented with domain 1 containing the oligonucleotide-oligosaccharide-binding fold on the right and the N and C termini on the left. Major features including the TCR-cell receptor binding site, MHC II binding site, and cysteine loop are indicated.

Citation: Seok Seo K, Bohach G. 2010. Staphylococcal Food Poisoning, p 119-130. In Juneja V, Sofos J (ed), Pathogens and Toxins in Foods. ASM Press, Washington, DC. doi: 10.1128/9781555815936.ch8
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1. Angelotti, R.,, M. J. Foter, and, K. H. Lewis. 1961. Time-temperature effects on salmonellae and staphylococci in foods. I. Behavior in refrigerated foods. II. Behavior at warm holding temperatures. Am. J. Public Health Nations Health 51:7688.
2. Asao, T.,, Y. Kumeda,, T. Kawai,, T. Shibata,, H. Oda,, K. Haruki,, H. Nakazawa, and, S. Kozaki. 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. 130:3340.
3. Atanassova, V.,, A. Meindl, and, C. Ring. 2001. Prevalence of Staphylococcus aureus and staphylococcal enterotoxins in raw pork and uncooked smoked ham—a comparison of classical culturing detection and RFLP-PCR. Int. J. Food Microbiol. 68:105113.
4. Baba, T.,, F. Takeuchi,, M. Kuroda,, H. Yuzawa,, K. Aoki,, A. Oguchi,, Y. Nagai,, N. Iwama,, K. Asano,, T. Naimi,, H. Kuroda,, L. Cui,, K. Yamamoto, and K. Hiramatsu. 2002. Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359:18191827.
5. Baker, M. D.,, and K. R. Acharya. 2004. Superantigens: structure-function relationships. Int. J. Med. Microbiol. 293:529537.
6. Balaban, N.,, and A. Rasooly. 2000. Staphylococcal enterotoxins. Int. J. Food Microbiol. 61:110.
7. Barber, M. A. 1914. Milk poisoning due to a type of Staphylococcus albus occurring in the udder of a healthy cow. Philipp. J. Sci. 9:515519.
8. Bautista, L.,, P. Gaya,, M. Medina, and, M. Nunez. 1988. A quantitative study of enterotoxin production by sheep milk staphylococci. Appl. Environ. Microbiol. 54:566569.
9. Bayles, K. W.,, and J. J. Iandolo. 1989. Genetic and molecular analyses of the gene encoding staphylococcal enterotoxin D. J. Bacteriol. 171:47994806.
10. Becker, K.,, D. Harmsen,, A. Mellmann,, C. Meier,, P. Schumann,, G. Peters, and, C. von Eiff. 2004. Development and evaluation of a quality-controlled ribosomal sequence database for 16S ribosomal DNA-based identification of Staphylococcus species. J. Clin. Microbiol. 42:49884995.
11. Bennett, R. W.,, and M. R. Berry, Jr. 1987. Serological reactivity and in vivo toxicity of Staphylococcus aureus enterotoxin A and D in selected canned foods. J. Food Sci. 52:416418.
12. Bergdoll, M. S. 1967. The staphylococccal enterotoxin, p. 1–25. In R. I. Mateles, and G. N. Wogan (ed.), Biochemistry of Some Foodborne Microbial Toxins, MIT Press, Cambridge, MA.
13. Bergdoll, M. S. 1988. Monkey feeding test for staphylococcal enterotoxin. Methods Enzymol. 165:324333.
14. Bergdoll, M. S. 1995. Importance of staphylococci that produce nanogram quantities of enterotoxin. Zentralbl. Bakteriol. 282:16.
15. Betley, M. J.,, and J. J. Mekalanos. 1988. Nucleotide sequence of the type A staphylococcal enterotoxin gene. J. Bacteriol. 170:3441.
16. Borja, C. R.,, and M. S. Bergdoll. 1967. Purification and partial characterization of enterotoxin C produced by Staphylococcus aureus strain 137. Biochemistry 6:14671473.
17. Branen, J. R.,, M. J. Hass,, E. R. Douthit,, W. C. Maki, and, A. L. Branen. 2007. Detection of Escherichia coli O157, Salmonella enterica serovar Typhimurium, and staphylococcal enterotoxin B in a single sample using enzymatic bio-nanotransduction. J. Food Prot. 70:841850.
18. Breckinridge, J. C.,, and M. S. Bergdoll. 1971. Outbreak of foodborne gastroenteritis due to a coagulase-negative enterotoxin-producing staphylococcus. N. Engl. J. Med. 284:541543.
19. Cavett, J. J. 1962. The microbiology of vacuum packed sliced bacon. J. Appl. Bacteriol. 25:282289.
20. CDC. 1983. Staphylococcal food poisoning on a cruise ship. MMWR Morb. Mortal. Wkly. Rep. 32:294295.
21. CDC. 1998. FoodNet:What We Are, Where We Are, and What We’re Doing in 1998. http://www.cdc.gov/ncidod/dbmd/food-net/foodnet.htm.
22. Chen, T. R.,, M. H. Hsiao,, C. S. Chiou, and, H. Y. Tsen. 2001. Development and use of PCR primers for the investigation of C1, C2 and C3 enterotoxin types of Staphylococcus aureus strains isolated from food-borne outbreaks. Int. J. Food Microbiol. 71:6370.
23. Chiang, Y. C.,, W. W. Liao,, C. M. Fan,, W. Y. Pai,, C. S. Chiou, and, H. Y. Tsen. 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. 121:6673.
24. Clarridge, J. E., III. 2004. Impact of 16S rRNA gene sequence analysis for identification of bacteria on clinical microbiology and infectious diseases. Clin. Microbiol. Rev. 17:840862.
25. Couch, J. L.,, M. T. Soltis, and, M. J. Betley. 1988. Cloning and nucleotide sequence of the type E staphylococcal enterotoxin gene. J. Bacteriol. 170:29542960.
26. Crass, B. A.,, and M. S. Bergdoll. 1986. Involvement of coagulase-negative staphylococci in toxic shock syndrome. J. Clin. Microbiol. 23:4345.
27. De Buyser, M. L.,, B. Lombard,, S. M. Schulten,, P. H. In’t Veld,, S. L. Scotter,, P. Rollier, and, C. Lahellec. 2003. Validation of EN ISO standard methods 6888 part 1 and part 2: 1999—enumeration of coagulase-positive staphylococci in foods. Int. J. Food Microbiol. 83:185194.
28. Denny, C. B.,, P. L. Tan, and, C. W. Bohrer. 1996. Heat inactivation of staphylococcal enterotoxin. J. Food Sci. 31:762767.
29. Denys, J. 1894. Empoisonnement par la viande contenant le Staphylocoque pyogène. Sem. Méd. 14:441.
30. De Paulis, A. N.,, S. C. Predari,, C. D. Chazarreta, and, J. E. Santoianni. 2003. Five-test simple scheme for species-level identification of clinically significant coagulase-negative staphylococci. J. Clin. Microbiol. 41:12191224.
31. Deringer, J. R.,, R. J. Ely,, S. R. Monday,, C. V. Stauffacher, and, G. A. Bohach. 1997. Vβ-dependent stimulation of bovine and human T cells by host-specific staphylococcal enterotoxins. Infect. Immun. 65:40484054.
32. Dinges, M. M.,, P. M. Orwin, and, P. M. Schlievert. 2000. Exotoxins of Staphylococcus aureus. Clin. Microbiol. Rev. 13:1634.
33. Do Carmo, L. S.,, C. Cummings,, V. R. Linardi,, R. S. Dias,, J. M. De Souza,, M. J. De Sena,, D. A. Dos Santos,, J. W. Shupp,, R. K. Pereira, and, M. Jett. 2004. A case study of a massive staphylococcal food poisoning incident. Foodborne Pathog. Dis. 1:241246.
34. 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. 7:311316.
35. Fitzgerald, J. R.,, P. J. Hartigan,, W. J. Meaney, and, C. J. Smyth. 2000. Molecular population and virulence factor analysis of Staphylococcus aureus from bovine intramammary infection. J. Appl. Microbiol. 88:10281037.
36. Fox, L. K.,, T. E. Besser, and, S. M. Jackson. 1996. Evaluation of a coagulase-negative variant of Staphylococcus aureus as a cause of intramammary infections in a herd of dairy cattle. J. Am. Vet. Med. Assoc. 209:11431146.
37. Futagawa-Saito, K.,, M. Suzuki,, M. Ohsawa,, S. Ohshima,, N. Sakurai,, W. Ba-Thein, and, T. Fukuyasu. 2004. Identification and prevalence of an enterotoxin-related gene, se-int, in Staphylococcus intermedius isolates from dogs and pigeons. J. Appl. Microbiol. 96:13611366.
38. Gardini, F.,, R. Tofalo, and, G. Suzzi. 2003. A survey of antibiotic resistance in Micrococcaceae isolated from Italian dry fermented sausages. J. Food Prot. 66:937945.
39. Genigeorgis, C.,, H. Riemann, and, W. W. Sadler. 1969. Production of enterotoxin B in cured meats. J. Food Sci. 32:6268.
40. Genigeorgis, C. A. 1989. Present state of knowledge on staphylococcal intoxication. Int. J. Food Microbiol. 9:327360.
41. Guthertz, L. S.,, J. T. Fruin,, R. L. Okoluk, and, J. L. Fowler. 1977. Microbial quality of frozen comminuted turkey meat. J. Food Sci. 42:13441347.
42. Harvey, J.,, and A. Gilmour. 2000. Staphylococcus aureus, p. 2066–2071. In C. A. Batt, and R. D. Patel (ed.), Encyclopedia of Food Microbiology, 1st ed. Academic Press, London, United Kingdom.
43. Heikens, E.,, A. Fleer,, A. Paauw,, A. Florijn, and, A. C. Fluit. 2005. Comparison of genotypic and phenotypic methods for species-level identification of clinical isolates of coagulase-negative staphylococci. J. Clin. Microbiol. 43:22862290.
44. Holley, R. A. 1985. Beef jerky: fate of Staphylococcus aureus in marinated and corned beef during jerky manufacture and 2.5°C storage. J. Food Prot. 48:107111.
45. Holtfreter, S.,, K. Bauer,, D. Thomas,, C. Feig,, V. Lorenz,, K. Roschack,, E. Friebe,, K. Selleng,, S. Lovenich,, T. Greve,, A. Greinacher,, B. Panzig,, S. Engelmann,, G. Lina, and, B. M. Broker. 2004. egc-encoded superantigens from Staphylococcus aureus are neutralized by human sera much less efficiently than are classical staphylococcal enterotoxins or toxic shock syndrome toxin. Infect. Immun. 72:40614071.
46. Hoover, D. G.,, S. R. Tatini, and, J. B. Maltais. 1983. Characterization of staphylococci. Appl. Environ. Microbiol. 46:649660.
47. Hu, D. L.,, G. Zhu,, F. Mori,, K. Omoe,, M. Okada,, K. Wakabayashi,, S. Kaneko,, K. Shinagawa, and, A. Nakane. 2007. Staphylococcal enterotoxin induces emesis through increasing serotonin release in intestine and it is downregulated by cannabinoid receptor 1. Cell. Microbiol. 9:22672277.
48. Jarraud, S.,, M. A. Peyrat,, A. Lim,, A. Tristan,, M. Bes,, C. Mougel,, J. Etienne,, F. Vandenesch,, M. Bonneville, and, G. Lina. 2001. egc, a highly prevalent operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus. J. Immunol. 166:669677.
49. Jay, J. M.,, M. J. Loessner, and, D. A. Golden. 2005. Staphylococcal gastroenteritis, p. 544–566. In D. R. Heldman (ed.), Modern Food Microbiology, 7th ed. Springer Science and Business Inc., New York, NY.
50. Jones, T. F.,, M. E. Kellum,, S. S. Porter,, M. Bell, and, W. Schaffner. 2002. An outbreak of community-acquired foodborne illness caused by methicillin-resistant Staphylococcus aureus. Emerg. Infect. Dis. 8:8284.
51. Jousson, O.,, D. Di Bello,, M. Vanni,, G. Cardini,, G. Soldani,, C. Pretti, and, L. Intorre. 2007. Genotypic versus phenotypic identification of staphylococcal species of canine origin with special reference to Staphylococcus schleiferi subsp. coagulans. Vet. Microbiol. 123:238244.
52. Kappler, J.,, B. Kotzin,, L. Herron,, E. W. Gelfand,, R. D. Bigler,, A. Boylston,, S. Carrel,, D. N. Posnett,, Y. Choi, and, P. Marrack. 1989. V beta-specific stimulation of human T cells by staphylococcal toxins. Science 244:811813.
53. Kerouanton, A.,, J. A. Hennekinne,, C. Letertre,, L. Petit,, O. Chesneau,, A. Brisabois, and, M. L. De Buyser. 2007. Characterization of Staphylococcus aureus strains associated with food poisoning outbreaks in France. Int. J. Food Microbiol. 115:369375.
54. Khambaty, F. M.,, R. W. Bennett, and, D. B. Shah. 1994. Application of pulsed-field gel electrophoresis to the epidemiological characterization of Staphylococcus intermedius implicated in a food-related outbreak. Epidemiol. Infect. 113:7581.
55. Kloos, W. E.,, K. H. Schleifer, and, R. Götz. 1991. The genus Staphylococcus, p. 1369–1420. In A. Balows,, H. G. Trüper,, M. Dworkin,, W. Harder,, and K. H. Schleifer (ed.), The Prokaryotes. A Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications, 2nd ed., vol. 2. Springer, New York, NY.
56. Kullik, I. I.,, and P. Giachino. 1997. The alternative sigma factor sigmaB in Staphylococcus aureus: regulation of the sigB operon in response to growth phase and heat shock. Arch. Microbiol. 167:151159.
57. Kwon, N. H.,, S. H. Kim,, K. T. Park,, W. K. Bae,, J. Y. Kim,, J. Y. Lim,, J. S. Ahn,, K. S. Lyoo,, J. M. Kim,, W. K. Jung,, K. M. Noh,, G. A. Bohach, and, Y. H. Park. 2004. Application of extended single-reaction multiplex polymerase chain reaction for toxin typing of Staphylococcus aureus isolates in South Korea. Int. J. Food Microbiol. 97:137145.
58. Lawrynowicz-Paciorek, M.,, M. Kochman,, K. Piekarska,, A. Grochowska, and, B. Windyga. 2007. The distribution of enterotoxin and enterotoxin-like genes in Staphylococcus aureus strains isolated from nasal carriers and food samples. Int. J. Food Microbiol. 117:319323.
59. Le Loir, Y.,, F. Baron, and, M. Gautier. 2003. Staphylococcus aureus and food poisoning. Genet. Mol. Res. 2:6376.
60. Letertre, C.,, S. Perelle,, F. Dilasser, and, P. Fach. 2003a. Detection and genotyping by real-time PCR of the staphylococcal enterotoxin genes sea to sej. Mol. Cell. Probes 17:139147.
61. Letertre, C.,, S. Perelle,, F. Dilasser, and, P. Fach. 2003b. Identification of a new putative enterotoxin SEU encoded by the egc cluster of Staphylococcus aureus. J. Appl. Microbiol. 95:3843.
62. Lina, G.,, G. A. Bohach,, S. P. Nair,, K. Hiramatsu,, E. Jouvin-Marche, and, R. Mariuzza. 2004. Standard nomenclature for the superantigens expressed by Staphylococcus. J. Infect. Dis. 189:23342336.
63. Lindsay, J. A.,, A. Ruzin,, H. F. Ross,, N. Kurepina, and, R. P. Novick. 1998. The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Mol. Microbiol. 29:527543.
64. Luczak-Kadlubowska, A.,, J. Krzyszton-Russjan, and, W. Hryniewicz. 2006. Characteristics of Staphylococcus aureus strains isolated in Poland in 1996 to 2004 that were deficient in species-specific proteins. J. Clin. Microbiol. 44:40184024.
65. Marshall, B. J.,, D. F. Ohye, and, J. H. Christian. 1971. Tolerance of bacteria to high concentrations of NaCl and glycerol in the growth medium. Appl. Microbiol. 21:363364.
66. Martin, M. C.,, J. M. Fueyo,, M. A. Gonzalez-Hevia, and, M. C. Mendoza. 2004. Genetic procedures for identification of enterotoxigenic strains of Staphylococcus aureus from three food poisoning outbreaks. Int. J. Food Microbiol. 94:279286.
67. Matthews, K. R.,, S. P. Oliver, and, S. H. King. 1990. Comparison of Vitek gram-positive identification system with API Staph-Trac system for species identification of staphylococci of bovine origin. J. Clin. Microbiol. 28:16491651.
68. McCormick, J. K.,, J. M. Yarwood, and, P. M. Schlievert. 2001. Toxic shock syndrome and bacterial superantigens: an update. Annu. Rev. Microbiol. 55:77104.
69. McNamara, P. J.,, K. C. Milligan-Monroe,, S. Khalili, and, R. A. Proctor. 2000. Identification, cloning, and initial characterization of rot, a locus encoding a regulator of virulence factor expression in Staphylococcus aureus. J. Bacteriol. 182:31973203.
70. Mead, P. S.,, L. Slutsker,, V. Dietz,, L. F. McCaig,, J. S. Bresee,, C. Shapiro,, P. M. Griffin, and, R. V. Tauxe. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5:607625.
71. Monday, S. R.,, and G. A. Bohach. 1999. Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in staphylococcal isolates. J. Clin. Microbiol. 37:34113414.
72. Moon, J. S.,, A. R. Lee,, S. H. Jaw,, H. M. Kang,, Y. S. Joo,, Y. H. Park,, M. N. Kim, and, H. C. Koo. 2007. Comparison of antibiogram, staphylococcal enterotoxin productivity, and coagulase genotypes among Staphylococcus aureus isolated from animal and vegetable sources in Korea. J. Food Prot. 70:25412548.
73. Munson, S. H.,, M. T. Tremaine,, M. J. Betley, and, R. A. Welch. 1998. Identification and characterization of staphylococcal enterotoxin types G and I from Staphylococcus aureus. Infect. Immun. 66:33373348.
74. Nedelkov, D.,, A. Rasooly, and, R. W. Nelson. 2000. Multitoxin biosensor-mass spectrometry analysis: a new approach for rapid, real-time, sensitive analysis of staphylococcal toxins in food. Int. J. Food Microbiol. 60:113.
75. Noleto, A. L.,, and M. S. Bergdoll. 1982. Production of enterotoxin by a Staphylococcus aureus strain that produces three identifiable enterotoxins. J. Food Prot. 45:10961097.
76. Oh, S. K.,, N. Lee,, Y. S. Cho,, D. B. Shin,, S. Y. Choi, and, M. Koo. 2007. Occurrence of toxigenic Staphylococcus aureus in ready-to-eat food in Korea. J. Food Prot. 70:11531158.
77. Olsen, S. J.,, L. C. MacKinnon,, J. S. Goulding,, N. H. Bean, and, L. Slutsker. 2000. Surveillance for foodborne-disease outbreaks—United States, 1993–1997. MMWR Surveill. Summ. 49:162.
78. Olsvik, O.,, K. Fossum, and, B. P. Berdal. 1982. Staphylococcal enterotoxin A, B, and C produced by coagulase-negative strains within the family Micrococcaceae. Acta Pathol. Microbiol. Immunol. Scand. Sect. B 90:441444.
79. Omoe, K.,, D. L. Hu,, H. Takahashi-Omoe,, A. Nakane, and, K. Shinagawa. 2005a. Comprehensive analysis of classical and newly described staphylococcal superantigenic toxin genes in Staphylococcus aureus isolates. FEMS Microbiol. Lett. 246:191198.
80. Omoe, K.,, K. Imanishi,, D. L. Hu,, H. Kato,, Y. Fugane,, Y. Abe,, S. Hamaoka,, Y. Watanabe,, A. Nakane,, T. Uchiyama, and, K. Shinagawa. 2005b. Characterization of novel staphylococcal enterotoxin-like toxin type P. Infect. Immun. 73:55405546.
81. Omoe, K.,, K. Imanishi,, D. L. Hu,, H. Kato,, H. Takahashi-Omoe,, A. Nakane,, T. Uchiyama, and, K. Shinagawa. 2004. Biological properties of staphylococcal enterotoxin-like toxin type R. Infect. Immun. 72:36643667.
82. Omoe, K.,, M. Ishikawa,, Y. Shimoda,, D. L. Hu,, S. Ueda, and, K. Shinagawa. 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. 40:857862.
83. Orwin, P. M.,, J. R. Fitzgerald,, D. Y. Leung,, J. A. Gutierrez,, G. A. Bohach, and, P. M. Schlievert. 2003. Characterization of Staphylococcus aureus enterotoxin L. Infect. Immun. 71:29162919.
84. Orwin, P. M.,, D. Y. Leung,, H. L. Donahue,, R. P. Novick, and, P. M. Schlievert. 2001. Biochemical and biological properties of staphylococcal enterotoxin K. Infect. Immun. 69:360366.
85. Orwin, P. M.,, D. Y. Leung,, T. J. Tripp,, G. A. Bohach,, C. A. Earhart,, D. H. Ohlendorf, and, P. M. Schlievert. 2002. Characterization of a novel staphylococcal enterotoxin-like superantigen, a member of the group V subfamily of pyrogenic toxins. Biochemistry 41:1403314040.
86. Pereira, J. L.,, S. P. Salzberg, and, M. S. Bergdoll. 1982. Effect of temperature, pH and sodium chloride concentrations on production of staphylococcal enterotoxin A and B. J. Food Prot. 45:13061309.
87. Petersson, K.,, H. Pettersson,, N. J. Skartved,, B. Walse, and, G. Forsberg. 2003. Staphylococcal enterotoxin H induces V alpha-specific expansion of T cells. J. Immunol. 170:41484154.
88. Phillips, D.,, D. Jordan,, S. Morris,, I. Jenson, and, J. Sumner. 2006. A national survey of the microbiological quality of beef carcasses and frozen boneless beef in Australia. J. Food Prot. 69:11131117.
89. Portocarrero, S. M.,, M. Newman, and, B. Mikel. 2002. Staphylococcus aureus survival, staphylococcal enterotoxin production and shelf stability of country-cured hams manufactured under different processing procedures. Meat Sci. 62:267273.
90. Poyart, C.,, G. Quesne,, C. Boumaila, and, P. Trieu-Cuot. 2001. Rapid and accurate species-level identification of coagulase-negative staphylococci by using the sodA gene as a target. J. Clin. Microbiol. 39:42964301.
91. Raj, H. D.,, and M. S. Bergdoll. 1969. Effect of enterotoxin B on human volunteers. J. Bacteriol. 98:833834.
92. Ranelli, D. M.,, C. L. Jones,, M. B. Johns,, G. J. Mussey, and, S. A. Khan. 1985. Molecular cloning of staphylococcal enterotoxin B gene in Escherichia coli and Staphylococcus aureus. Proc. Natl. Acad. Sci. USA 82:58505854.
93. Regassa, L. B.,, J. L. Couch, and, M. J. Betley. 1991. Steady-state staphylococcal enterotoxin type C mRNA is affected by a product of the accessory gene regulator (agr) and by glucose. Infect. Immun. 59:955962.
94. Rodriguez, M.,, F. Nunez,, J. J. Cordoba,, E. Bermudez, and, M. A. Asensio. 1996. Gram-positive, catalase-positive cocci from dry cured Iberian ham and their enterotoxigenic potential. Appl. Environ. Microbiol. 62:18971902.
95. Sanjeev, S.,, T. S. Gopalakrishna Iyer,, P. R. Varma,, C. C. Panduranga Rao, and, K. Mahadeva Iyer. 1987. Carriage of enterotoxigenic staphylococci in workers of fish processing factories. Indian J. Med. Res. 85:262265.
96. Schantz, E. J.,, W. G. Roessler,, M. J. Woodburn,, J. M. Lynch,, H. M. Jacoby,, S. J. Silverman,, J. C. Gorman, and, L. Spero. 1972. Purification and some chemical and physical properties of staphylococcal enterotoxin A. Biochemistry 11:360366.
97. Schleifer, K. H. 1986. Gram positive cocci, p. 999–1100. In P. A. Sneath (ed.), Bergey’s Manual of Systematic Bacteriology, 1st ed., vol. 2. Williams & Wilkins Co., Baltimore, MD.
98. Schmidt, K. A.,, N. P. Donegan,, W. A. Kwan, Jr.,, and A. Cheung. 2004. Influences of sigmaB and agr on expression of staphylococcal enterotoxin B (seb) in Staphylococcus aureus. Can. J. Microbiol. 50:351360.
99. Seo, K. S.,, S. U. Lee,, Y. H. Park,, W. C. Davis,, L. K. Fox, and, G. A. Bohach. 2007. Long-term staphylococcal enterotoxin C1 exposure induces soluble factor-mediated immunosuppression by bovine CD4+ and CD8+ T cells. Infect. Immun. 75:260269.
100. Sergeev, N.,, D. Volokhov,, V. Chizhikov, and, A. Rasooly. 2004. Simultaneous analysis of multiple staphylococcal enterotoxin genes by an oligonucleotide microarray assay. J. Clin. Microbiol. 42:21342143.
101. Shimizu, A.,, M. Fujita,, H. Igarashi,, M. Takagi,, N. Nagase,, A. Sasaki, and, J. Kawano. 2000. Characterization of Staphylococcus aureus coagulase type VII isolates from staphylococcal food poisoning outbreaks (1980–1995) in Tokyo, Japan, by pulsed-field gel electrophoresis. J. Clin. Microbiol. 38:37463749.
102. Skow, A.,, K. A. Mangold,, M. Tajuddin,, A. Huntington,, B. Fritz,, R. B. Thomson, Jr.,, and K. L. Kaul. 2005. Species-level identification of staphylococcal isolates by real-time PCR and melt curve analysis. J. Clin. Microbiol. 43:28762880.
103. Spero, L.,, B. Y. Griffin,, J. L. Middlebrook, and, J. F. Metzger. 1976. Effect of single and double peptide bond scission by trypsin on the structure and activity of staphylococcal enterotoxin C. J. Biol. Chem. 251:55805588.
104. Srinivasan, V.,, A. A. Sawant,, B. E. Gillespie,, S. J. Headrick,, L. Ceasaris, and, S. P. Oliver. 2006. Prevalence of enterotoxin and toxic shock syndrome toxin genes in Staphylococcus aureus isolated from milk of cows with mastitis. Foodborne Pathog. Dis. 3:274283.
105. State of Alaska. 1975. Staphylococcal foodborne outbreak. State Alaska Epidemiol. Bull. 4:12.
106. Stewart, C. M.,, M. B. Cole,, J. D. Legan,, L. Slade,, M. H. Vandeven, and, D. W. Schaffner. 2002. Staphylococcus aureus growth boundaries: moving towards mechanistic predictive models based on solute-specific effects. Appl. Environ. Microbiol. 68:18641871.
107. Sugiyama, H.,, and T. Hayama. 1965. Abdominal viscera as site of emetic action for staphylococcal enterotoxin in the monkey. J. Infect. Dis. 115:330336.
108. Summer, S. S.,, J. A. Albrecht, and, D. L. Peters. 1993. Occurrence of enterotoxigenic strains of Staphylococcus aureus and enterotoxin production in bakery products. J. Food Prot. 56:722724.
109. Swartzentruber, A.,, A. H. Schwab,, A. P. Duran,, B. A. Wentz, and, R. B. Read, Jr. 1980. Microbiological quality of frozen shrimp and lobster tail in the retail market. Appl. Environ. Microbiol. 40:765769.
110. Taponen, S.,, H. Simojoki,, M. Haveri,, H. D. Larsen, and, S. Pyorala. 2006. Clinical characteristics and persistence of bovine mastitis caused by different species of coagulase-negative staphylococci identified with API or AFLP. Vet. Microbiol. 115:199207.
111. Thaikruea, L.,, J. Pataraarechachai,, P. Savanpunyalert, and, U. Naluponjiragul. 1995. An unusual outbreak of food poisoning. Southeast Asian J. Trop. Med. Public Health 26:7885.
112. Tonge, R. J.,, A. C. Baird-Parker, and, J. J. Cavett. 1964. Chemical and microbiological changes during storage of vacuum packed sliced bacon. J. Appl. Bacteriol. 27:252264.
113. Townsend, D. E.,, and B. J. Wilkinson. 1992. Proline transport in Staphylococcus aureus: a high-affinity system and a low-affinity system involved in osmoregulation. J. Bacteriol. 174:27022710.
114. Tremaine, M. T.,, D. K. Brockman, and, M. J. Betley. 1993. Staphylococcal enterotoxin A gene (sea) expression is not affected by the accessory gene regulator (agr). Infect. Immun. 61:356359.
115. Udo, E. E.,, M. A. Al-Bustan,, L. E. Jacob, and, T. D. Chugh. 1999. Enterotoxin production by coagulase-negative staphylococci in restaurant workers from Kuwait City may be a potential cause of food poisoning. J. Med. Microbiol. 48:819823.
116. USDA. 1996. Nationwide federal plant raw ground beef microbiological survey. U.S. Department of Agriculture, Washington, DC.
117. USFDA. 1992. Staphylococcus aureus. Bad Bug Book, Foodborne Pathogenic Microorganisms and Natural Toxins Handbook. U.S. Food and Drug Administration, Washington, DC. http://vm.cfsan.fda.gov/~mow/chap3.html.
118. Valle, J.,, E. Gomez-Lucia,, S. Piriz,, J. Goyache,, J. A. Orden, and, S. Vadillo. 1990. Enterotoxin production by staphylococci isolated from healthy goats. Appl. Environ. Microbiol. 56:13231326.
119. Vandenbosch, L. L.,, D. Y. Fung, and, M. Widomski. 1973. Optimum temperature for enterotoxin production by Staphylococcus aureus S-6 and 137 in liquid medium. Appl. Microbiol. 25:498500.
120. Vandenesch, F.,, C. Lebeau,, M. Bes,, D. McDevitt,, T. Greenland,, R. P. Novick, and, J. Etienne. 1994. Coagulase deficiency in clinical isolates of Staphylococcus aureus involves both transcriptional and post-transcriptional defects. J. Med. Microbiol. 40:344349.
121. Vernozy-Rozand, C.,, C. Mazuy,, G. Prevost,, C. Lapeyre,, M. Bes,, Y. Brun, and, J. Fleurette. 1996. Enterotoxin production by coagulase-negative staphylococci isolated from goats’ milk and cheese. Int. J. Food Microbiol. 30:271280.
122. Warren, J. R.,, L. Spero, and, J. F. Metzger. 1974. Stabilization of native structure by the closed disulfide loop of staphylococcal enterotoxin B. Biochim. Biophys. Acta 359:351363.
123. WHO Surveillance Programme. 2000. 7th Report (1993–1998), p. 13–393. In K. Schmidt, and C. Tirado (ed.), WHO Surveillance Programme 7th Report. WHO, Berlin, Germany.
124. Yamashita, K.,, A. Shimizu,, J. Kawano,, E. Uchida,, A. Haruna, and, S. Igimi. 2005. Isolation and characterization of staphylococci from external auditory meatus of dogs with or without otitis externa with special reference to Staphylococcus schleiferi subsp. coagulans isolates. J. Vet. Med. Sci. 67:263268.
125. Yeh, K. S.,, S. P. Chen, and, J. H. Lin. 2005. One-year (2003) nationwide pork carcass microbiological baseline data survey in Taiwan. J. Food Prot. 68:458461.
126. Yugueros, J.,, A. Temprano,, B. Berzal,, M. Sanchez,, C. Hernanz,, J. M. Luengo, and, G. Naharro. 2000. Glyceraldehyde-3-phosphate dehydrogenase-encoding gene as a useful taxonomic tool for Staphylococcus spp. J. Clin. Microbiol. 38:43514355.
127. Zhang, S.,, J. J. Iandolo, and, G. C. Stewart. 1998. The enterotoxin D plasmid of Staphylococcus aureus encodes a second enterotoxin determinant (sej). FEMS Microbiol. Lett. 168:227233.


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Table 1.

Prevalence of in several foods

Citation: Seok Seo K, Bohach G. 2010. Staphylococcal Food Poisoning, p 119-130. In Juneja V, Sofos J (ed), Pathogens and Toxins in Foods. ASM Press, Washington, DC. doi: 10.1128/9781555815936.ch8
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Table 2.

Biochemical and functional properties of SEs and SEls (grouped according to sequence and functional similarities)

Citation: Seok Seo K, Bohach G. 2010. Staphylococcal Food Poisoning, p 119-130. In Juneja V, Sofos J (ed), Pathogens and Toxins in Foods. ASM Press, Washington, DC. doi: 10.1128/9781555815936.ch8
Generic image for table
Table 3.

Large outbreaks of SFP

Citation: Seok Seo K, Bohach G. 2010. Staphylococcal Food Poisoning, p 119-130. In Juneja V, Sofos J (ed), Pathogens and Toxins in Foods. ASM Press, Washington, DC. doi: 10.1128/9781555815936.ch8

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