1887

Abstract

In recent years several new staphylococcal enterotoxins (SEs) have been described, which currently have largely unknown frequencies of occurrence and roles in human or animal disease. One hundred and ninety-one isolates from cows (99), goats (39), sheep (23), rabbits (15), chickens (15) and a cat (1) were screened for SE genes , and and for the gene encoding staphylococcal toxic shock syndrome toxin-1 using multiplex PCRs and individual PCRs for the and genes. One hundred and ten isolates tested positive for at least one of these 16 superantigen (SAg)-encoding genes. There were statistically significant differences in the frequencies of some of these SAg genes between isolates from different animals. No strain possessed either the or gene. The gene was present in 51 isolates, the gene in eight and the gene in one. The gene was found in four strains and the and genes together in one isolate. The most common combinations of genes were the cluster, bearing the , , , and genes, in 47 isolates, the , and gene combination typical of the SaPIbov pathogenicity island in 44 isolates, the cluster lacking the gene in 11 isolates, the and genes in nine isolates, and the and genes without the gene in seven isolates. The higher frequencies of the and genes together and the lower frequencies of the gene cluster among the SAg gene-positive sheep or goat isolates compared to bovine isolates were statistically significant. Of 36 bovine isolates that were mitogenic for human T lymphocytes, four were negative for the 16 SAg genes tested for, while a further 14 gave borderline results in the mitogenicity assay, 12 of which were SAg gene-negative. Twenty-nine strains lacking all the SAg genes did not induce T-cell proliferation. This survey indicates that novel SE genes , , , , and along with the and genes predominate in from animal hosts. The mitogenicity assays indicate that further uncharacterized SAgs may be present in bovine isolates.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.45863-0
2005-04-01
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/jmm/54/4/JM540415.html?itemId=/content/journal/jmm/10.1099/jmm.0.45863-0&mimeType=html&fmt=ahah

References

  1. Akineden Ö., Annemüller C., Hassan A. A., Lämmler C., Wolter W., Zschöck M. 2001; Toxin genes and other characteristics of Staphylococcus aureus isolates from milk of cows with mastitis. Clin Diagn Lab Immunol 8:959–964
    [Google Scholar]
  2. Alouf J. E., Müller-Alouf H. 2003; Staphylococcal and streptococcal superantigens: molecular, biological and clinical aspects. Int J Med Microbiol 292:429–440 [CrossRef]
    [Google Scholar]
  3. Balaban N., Rasooly A. 2000; Staphylococcal enterotoxins. Int J Food Microbiol 61:1–10 [CrossRef]
    [Google Scholar]
  4. Bautista L., Gaya P., Medina M., Nuñez M. 1988; A quantitative study of enterotoxin production by sheep milk staphylococci. Appl Environ Microbiol 54:566–569
    [Google Scholar]
  5. Beck H. S., Wise W. S., Dodd F. H. 1992; Cost benefit analysis of bovine mastitis in the UK. J Dairy Res 59:449–460 [CrossRef]
    [Google Scholar]
  6. Becker K., Friedrich A. W., 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 [CrossRef]
    [Google Scholar]
  7. Blaiotta G., Ercolini D., Pennacchia C., Fusco V., Casaburi A., Pepe O., Villani F. 2004; PCR detection of staphylococcal enterotoxin genes in Staphylococcus spp.strains isolated from meat and dairy products. Evidence for new variants of se G and se I in S. aureus AB-8802. J Appl Microbiol 97:719–730 [CrossRef]
    [Google Scholar]
  8. Cenci-Goga B. T., Karama M., Rossitto P. V., Morgante R. A., Cullor J. S. 2003; Enterotoxin production by Staphylococcus aureus isolated from mastitic cows. J Food Prot 66:1693–1696
    [Google Scholar]
  9. Chen T.-R., Chiou C.-S., Tsen H.-Y. 2004; Use of novel PCR primers specific to the genes of staphylococcal enterotoxin G, H, I for the survey of Staphylococcus aureus strains isolated from food-poisoning cases and food samples in Taiwan. Int J Food Microbiol 92:189–197 [CrossRef]
    [Google Scholar]
  10. Dinges M. M., Orwin P. M., Schlievert P. M. 2000; Exotoxins of Staphylococcus aureus . Clin Microbiol Rev 13:16–34 [CrossRef]
    [Google Scholar]
  11. Fitzgerald J. R., Meaney W. J., Hartigan P. J., Smyth C. J., Kapur V. 1997; Fine-structure molecular epidemiological analysis of Staphylococcus aureus recovered from cows. Epidemiol Infect 119:261–269 [CrossRef]
    [Google Scholar]
  12. Fitzgerald J. R., Hartigan P. J., Meaney W. J., Smyth C. J. 2000; Molecular population and virulence factor analysis of Staphylococcus aureus from bovine intramammary infection. J Appl Microbiol 88:1028–1037 [CrossRef]
    [Google Scholar]
  13. Fitzgerald J. R., Monday S., Foster T. J., Bohach G. A., Hartigan P. J., Meaney W. J., Smyth C. J. 2001; Characterization of a putative pathogenicity island from bovine Staphylococcus aureus encoding multiple superantigens. J Bacteriol 183:63–70 [CrossRef]
    [Google Scholar]
  14. Foschino R., Invernizzi A., Barucco R., Stradiotto K. 2002; Microbial composition, including the incidence of pathogens, of goat milk from the bergamo region of Italy during a lactation year. J Dairy Sci 69:213–225
    [Google Scholar]
  15. Gruet P., Maincent P., Berthelot X., Kaltsatos V. 2001; Bovine mastitis and intramammary drug delivery: review and perspectives. Adv Drug Deliv Rev 50:245–259 [CrossRef]
    [Google Scholar]
  16. Hazariwala A., Sanders Q., Hudson C. R., Hofacre C., Thayer S. G., Maurer J. J. 2002; Distribution of staphylococcal enterotoxin genes among Staphylococcus aureus isolates from poultry and humans with invasive staphylococcal disease. Avian Dis 46:132–136 [CrossRef]
    [Google Scholar]
  17. Hentschel U., Hacker J. 2001; Pathogenicity islands: the tip of the iceberg. Microbes Infect 3:545–548 [CrossRef]
    [Google Scholar]
  18. Herdt P. 2000; Differentiation between high and low virulence Staphylococcus aureus strains from rabbits by randomly amplified polymorphic DNA (RAPD) analysis. Vet Microbiol 72:311–319 [CrossRef]
    [Google Scholar]
  19. Hermans K., Haesebrouck F., Vaneechoutte M., Devriese L. A., Godard C., de Hermans K., Devriese L. A., Haesebrouck F. 2003; Rabbit staphylococcosis: difficult solutions for serious problems. Vet Microbiol 91:57–64 [CrossRef]
    [Google Scholar]
  20. Ho G., Campbell W. H., Carlson E. 1989; Ovine-associated Staphylococcus aureus protein with immunochemical similarity to toxic shock syndrome toxin 1. J Clin Microbiol 72:210–212
    [Google Scholar]
  21. Huff G. R., Huff W. E., Rath N. C., Balog J. M. 2000; Turkey osteomyelitis complex. Poult Sci 79:1050–1056 [CrossRef]
    [Google Scholar]
  22. Jablonski L. M., Bohach G. A. 2001; Staphylococcus aureus . In Fundamentals of Food Microbiology pp 410–434 Edited by Beuchat L., Doyle M., Montville T. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  23. Jarraud S., Peyrat M. A., Lim A. & 7 other authors; 2001; egc , a highly prevalent operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus . J Immunol 166:669–677 (erratum in J Immunol 166, following 4259 [CrossRef]
    [Google Scholar]
  24. Kenny K., Reiser R. F., Bastida-Corcuera F. D., Norcross N. L. 1993; Production of enterotoxins and toxic shock syndrome toxin by bovine mammary isolates of Staphylococcus aureus . J Clin Microbiol 31:706–707
    [Google Scholar]
  25. Kuroda M., Ohta T., Uchiyama I. & 34 other authors; 2001; Whole genome sequencing of methicillin-resistant Staphylococcus aureus . Lancet 357:1225–1240 [CrossRef]
    [Google Scholar]
  26. Kúzma K., Malinowski E., Lassa H., Kłossowska A. 2003; Detection of genes for enterotoxins and toxic shock syndrome toxin-1 in Staphylococcus aureus isolated from bovine mastitis. Bull Vet Inst Pulawy 47:419–426
    [Google Scholar]
  27. Larsen H. D., Huda A., Eriksen N. H. R., Jensen N. E. 2000; Differences between Danish bovine and human Staphylococcus aureus isolates in the possession of superantigens. Vet Microbiol 76:153–162 [CrossRef]
    [Google Scholar]
  28. Larsen H. D., Aarestrup F. M., Jensen N. E. 2002; Geographical variation in the presence of genes encoding superantigenic exotoxins and β-hemolysin among Staphylococcus aureus isolated from bovine mastitis in Europe and USA. Vet Microbiol 85:61–67 [CrossRef]
    [Google Scholar]
  29. Le Loir Y., Baron F., Gautier M. 2003; Staphylococcus aureus and food poisoning. Genet Mol Res 2:7–28
    [Google Scholar]
  30. Letertre C., Perelle S., Dilasser F., Fach P. 2003a; Identification of a new putative enterotoxin SEU encoded by the egc cluster of Staphylococcus aureus . J Appl Microbiol 95:38–43 [CrossRef]
    [Google Scholar]
  31. Letertre C., Perelle S., Dilasser F., Fach P. 2003b; Detection and genotyping by real-time PCR of the staphylococcal enterotoxin genes sea to sej . Mol Cell Probes 17:139–147 [CrossRef]
    [Google Scholar]
  32. Letertre C., Perelle S., Dilasser F., Fach P. 2003c; A strategy based on 5′-nuclease multiplex PCR to detect enterotoxin genes sea to sej of Staphylococcus aureus . Mol Cell Probes 17:227–235 [CrossRef]
    [Google Scholar]
  33. Linares J. A., Wigle W. L. 2001; Staphylococcus aureus pneumonia in turkey poults with gross lesions resembling aspergillosis. Avian Dis 45:1068–1072 [CrossRef]
    [Google Scholar]
  34. Lindsay I. A., Ruzin A., Ross H. F., Kurepina N., Novick R. P. 1998; The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus . Mol Microbiol 29:527–543 [CrossRef]
    [Google Scholar]
  35. Llewelyn M., Cohen J. 2002; Superantigens: microbial agents that corrupt immunity. Lancet Infect Dis 2:156–162 [CrossRef]
    [Google Scholar]
  36. Loncarevic S., Mathisen T. 2004 Characterisation of Staphylococcus aureus enterotoxin type H from a food outbreak. In Proceedings of the 5th World Congress on Foodborne Infections and Intoxications, Berlin, Germany; June 2004, abstract no. P-A10 p 118 Berlin: Berlin Federal Institute for Risk Assessement;
    [Google Scholar]
  37. Marr J. C., Lyon J. D., Roberson J. R., Lupher M., Davis W. C., Bohach G. A. 1993; Characterisation of novel type C staphylococcal enterotoxins: biological and evolutionary implications. Infect Immun 61:4254–4262
    [Google Scholar]
  38. Martín M. C., Fueyo J. M., González-Hevia M. A., Mendoza M. C. 2004; Genetic procedures for identification of enterotoxigenic strains of Staphylococcus aureus from three food poisoning outbreaks. Int J Food Microbiol 94:279–286 [CrossRef]
    [Google Scholar]
  39. Matsunaga T., Kamata S., Kakiichi N., Uchida K. 1993; Characteristics of Staphylococcus aureus isolated from peracute, acute and chronic bovine mastitis. J Vet Med Sci 55:297–300 [CrossRef]
    [Google Scholar]
  40. McCormick J. K., Yarwood J. M., Schlievert P. M. 2001; Toxic shock syndrome and bacterial superantigens: an update. Annu Rev Microbiol 55:77–104 [CrossRef]
    [Google Scholar]
  41. McCullagh J. J., McNamee P. T., Smyth J. A., Ball H. J. 1998; The use of pulsed field gel electrophoresis to investigate the epidemiology of Staphylococcus aureus infection in commercial broiler flocks. Vet Microbiol 63:275–281 [CrossRef]
    [Google Scholar]
  42. McNamee P. T., McCullagh J. J., Thorp B. H., Ball H. J., Graham D., McCullough S. J., McConaghy D., Smyth J. A. 1998; Study of leg weakness in two commercial broiler flocks. Vet Rec 143:131–135 [CrossRef]
    [Google Scholar]
  43. Mead P. S., Slutsker L., Dietz V., McCaig L. F., Bresee J. S., Shapiro C., Griffin P. M., Tauxe R. V. 1999; Food-related illness and death in the United States. Emerg Infect Dis 5:607–625 [CrossRef]
    [Google Scholar]
  44. Mehrotra M., Wang G., Johnson W. M. 2000; Multiplex PCR for detection of genes for Staphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1 and methicillin resistance. J Clin Microbiol 38:1032–1035
    [Google Scholar]
  45. Michie C. A., Cohen J. 1998; The clinical significance of T-cell superantigens. Trends Microbiol 6:61–65 [CrossRef]
    [Google Scholar]
  46. Miles H., Lesser W., Sears P. 1992; The economic implications of bioengineered mastitis control. J Dairy Sci 75:596–605 [CrossRef]
    [Google Scholar]
  47. Monday S. R., Bohach G. A. 1999; Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in staphylococcal isolates. J Clin Microbiol 37:3411–3414
    [Google Scholar]
  48. Nashev D., Toshkova K., Salasia S. I. O., Hassan A. A., Lämmler C., Zschöck M. 2004; Distribution of virulence genes of Staphylococcus aureus isolated from stable nasal carriers. FEMS Microbiol Lett 233:45–52 [CrossRef]
    [Google Scholar]
  49. Novick R. P. 2003; Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus . Plasmid 49:93–105 [CrossRef]
    [Google Scholar]
  50. Novick R. P., Schlievert P., Ruzin A. 2001; Pathogenicity and resistance islands of staphyloccci. Microbes Infect 3:585–594 [CrossRef]
    [Google Scholar]
  51. Omoe K., Hu D.-L., Takahashi-Omoe H., Nakane A., Shinagawa K. 2003; Identification and characterisation of a new staphylococcal enterotoxin-related putative toxin encoded by two kinds of plasmids. Infect Immun 71:6088–6094 [CrossRef]
    [Google Scholar]
  52. Orden J. A., Goyache J., Hernández J., Doménech A., Suárez G., Gómez-Lucia E. 1992; Detection of enterotoxins and TSST-1 secreted by Staphylococcus aureus isolated from ruminant mastitis.Comparison of ELISA and immunoblot. J Appl Bacteriol 72:486–489 [CrossRef]
    [Google Scholar]
  53. Orwin P. M., Leung D. Y. M., Donahue H. L., Novick R. P., Schlievert P. M. 2001; Biochemical and biological properties of staphylococcal enterotoxin K. Infect Immun 69:360–366 [CrossRef]
    [Google Scholar]
  54. Orwin P. M., Leung D. Y., Tripp T. J., Bohach G. A., Earhart C. A., Ohlendorf D. H., Schlievert P. M. 2002; Characterisation of a novel staphylococcal enterotoxin-like superantigen, a member of the group V subfamily of pyrogenic toxins. Biochemistry 41:14033–14040 [CrossRef]
    [Google Scholar]
  55. Orwin P. M., Fitzgerald J. R., Leung D. Y. M., Gutierrez J. A., Bohach G. A., Schlievert P. M. 2003; Characterization of Staphylococcus aureus enterotoxin L. Infect Immun 71:2916–2919 [CrossRef]
    [Google Scholar]
  56. Peacock S. J., Moore C. E., Justice A., Kantzanou M., Story L., Mackie K., O'Neill G., Day N. P. J. 2002; Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus . Infect Immun 70:4987–4996 [CrossRef]
    [Google Scholar]
  57. Petersson K., Forsberg G., Walse B. 2004; Interplay between superantigens and immunoreceptors. Scand J Immunol 59:345–355 [CrossRef]
    [Google Scholar]
  58. Poindexter N. J., Schlievert P. M. 1985; Toxic-shock-syndrome toxin 1-induced proliferation of lymphocytes: comparison of the mitogenic response of human, murine, and rabbit lymphocytes. J Infect Dis 151:65–72 [CrossRef]
    [Google Scholar]
  59. Proft T., Fraser J. D. 2003; Bacterial superantigens. Clin Exp Immunol 133:299–306 [CrossRef]
    [Google Scholar]
  60. Rodgers J. D., McCullagh J. J., McNamee P. T., Smyth J. A., Ball H. J. 1999; Comparison of Staphylococcus aureus recovered from personnel in a poultry hatchery and in broiler parent farms with those isolated from skeletal disease in broilers. Vet Microbiol 69:189–198 [CrossRef]
    [Google Scholar]
  61. Rosec J. P., Gigaud O. 2002; Staphylococcal enterotoxin genes of classical and new types detected by PCR in France. Int J Food Microbiol 77:61–70 [CrossRef]
    [Google Scholar]
  62. Sambrook J., Russell D. W. 2001 Molecular Cloning: a Laboratory Manual , 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  63. Scherrer D., Corti S., Muehlherr J. E., 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 [CrossRef]
    [Google Scholar]
  64. Schlievert P. M., Jablonski L. M., Roggiani M., Sadler I., Callantine S., Mitchell D. T., Ohlendorf D. H., Bohach G. A. 2000; Pyrogenic toxin superantigen site specificity in toxic shock syndrome and food poisoning in animals. Infect Immun 68:3630–3634 [CrossRef]
    [Google Scholar]
  65. Sergeev N., Volokhov D., Chizhikov V., Rasooly A. 2004; Simultaneous analysis of multiple staphylococcal enterotoxin genes by an oligonucleotide microarray assay. J Clin Microbiol 42:2134–2143 [CrossRef]
    [Google Scholar]
  66. Shimizu A., Fujita M., Igarashi H., Takagi M., Nagase N., Sasaki A., Kawano J. 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 38:3746–3749
    [Google Scholar]
  67. Stulberg D. L., Penrod M. A., Blatny R. A. 2002; Common bacterial skin infections. Am Fam Physician 66:119–124
    [Google Scholar]
  68. Takeuchi S., Matsunaga K., Inubushi S., Higuchi H., Imaizumi K., Kaidoh T. 2002; Structural gene and strain specificity of a novel cysteine protease produced by Staphylococcus aureus isolated from a diseased chicken. Vet Microbiol 89:201–210 [CrossRef]
    [Google Scholar]
  69. Thompson J. D., Higgins D. G., Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 [CrossRef]
    [Google Scholar]
  70. Webster K. A., Mitchell G. B. 1989; Experimental production of tick pyaemia. Vet Parasitol 34:129–133 [CrossRef]
    [Google Scholar]
  71. Wieneke A. A., Roberts D., Gilbert R. J. 1993; Staphylococcal food poisoning in the United Kingdom, 1969-90. Epidemiol Infect 110:519–531 [CrossRef]
    [Google Scholar]
  72. Woteki C. E., Kineman B. D. 2003; Challenges and approaches to reducing foodborne illness. Annu Rev Nutr 23:315–344 [CrossRef]
    [Google Scholar]
  73. Yarwood J. M., McCormick J. K., Paustian M. L., Orwin P. M., Kapur V., Schlievert P. M. 2002; Characterisation and expression analysis of Staphylococcus aureus pathogenicity island 3. J Biol Chem 277:13138–13147 [CrossRef]
    [Google Scholar]
  74. Zhang S., Iandolo J. J., Stewart G. C. 1998; The enterotoxin D plasmid of Staphylococcus aureus encodes a second enterotoxin determinant ( sej ). FEMS Microbiol Lett 168:227–233 [CrossRef]
    [Google Scholar]
  75. Zschöck M., Riße K., Sommerhäuser J. 2004; Occurrence and clonal relatedness of sec / tst -gene positive Staphylococcus aureus isolates of quartermilk samples of cows suffering with mastitis. Lett Appl Microbiol 38:493–498 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.45863-0
Loading
/content/journal/jmm/10.1099/jmm.0.45863-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error