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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1990 Jan;87(1):225–229. doi: 10.1073/pnas.87.1.225

A single clone of Staphylococcus aureus causes the majority of cases of toxic shock syndrome.

J M Musser 1, P M Schlievert 1, A W Chow 1, P Ewan 1, B N Kreiswirth 1, V T Rosdahl 1, A S Naidu 1, W Witte 1, R K Selander 1
PMCID: PMC53234  PMID: 1967495

Abstract

Genetic relationships among 315 isolates of the bacterium Staphylococcus aureus expressing toxic shock syndrome toxin-1 (TSST-1) recovered primarily from humans with toxic shock syndrome (TSS) in five countries on two continents were determined by analyzing electrophoretically demonstrable allelic variation at 20 chromosomal enzyme loci. Forty-nine distinctive electrophoretic types (ETs), representing multilocus enzyme genotypes, were identified. Cluster analysis of the ETs revealed two major phylogenetic divisions separated at a genetic distance of 0.35 and seven branches diverging from one another at distances greater than or equal to 0.20. A single clone (ET 41) accounted for 88% of cases of TSS with a female urogenital focus and 53% of TSS cases involving nonurogenital (predominantly wound) infections. With few exceptions, strains representing different phylogenetic lines had characteristic TSST-1 gene (tst) restriction fragment length polymorphism patterns obtained by digestion of genomic DNA with Cla I. Strains recovered from ovine and bovine hosts with mastitis were genotypically distinct from the major human TSS clone. The expression of TSST-1 in cell lineages representing the total breadth of multilocus genotypic diversity in the species S. aureus as a whole is interpreted as evidence that the TSST-1 gene is evolutionarily old. The recovery of a single clone from the majority of individuals afflicted with TSS having a urogenital focus and from the genital tract of a large proportion of asymptomatic female carriers strongly suggests that this clone is especially well adapted for colonization of these anatomic sites.

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Selected References

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  1. Altemeier W. A., Lewis S. A., Bjornson H. S., Staneck J. L., Schlievert P. M. Staphylococcus in toxic shock syndrome and other surgical infections. Development of new bacteriophages. Arch Surg. 1983 Mar;118(3):281–284. doi: 10.1001/archsurg.1983.01390030013002. [DOI] [PubMed] [Google Scholar]
  2. Altemeier W. A., Lewis S. A., Schlievert P. M., Bergdoll M. S., Bjornson H. S., Staneck J. L., Crass B. A. Staphylococcus aureus associated with toxic shock syndrome: phage typing and toxin capability testing. Ann Intern Med. 1982 Jun;96(6 Pt 2):978–982. doi: 10.7326/0003-4819-96-6-978. [DOI] [PubMed] [Google Scholar]
  3. Altemeier W. A., Lewis S. A., Schlievert P. M., Bergdoll M. S., Bjornson H. S., Staneck J. L., Crass B. A. Staphylococcus aureus associated with toxic shock syndrome: phage typing and toxin capability testing. Ann Intern Med. 1982 Jun;96(6 Pt 2):978–982. doi: 10.7326/0003-4819-96-6-978. [DOI] [PubMed] [Google Scholar]
  4. Barbour A. G. Vaginal isolates of Staphylococcus aureus associated with toxic shock syndrome. Infect Immun. 1981 Aug;33(2):442–449. doi: 10.1128/iai.33.2.442-449.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bergdoll M. S., Crass B. A., Reiser R. F., Robbins R. N., Davis J. P. A new staphylococcal enterotoxin, enterotoxin F, associated with toxic-shock-syndrome Staphylococcus aureus isolates. Lancet. 1981 May 9;1(8228):1017–1021. doi: 10.1016/s0140-6736(81)92186-3. [DOI] [PubMed] [Google Scholar]
  6. Bergdoll M. S., Crass B. A., Reiser R. F., Robbins R. N., Lee A. C., Chesney P. J., Davis J. P., Vergeront J. M., Wand P. J. An enterotoxin-like protein in Staphylococcus aureus strains from patients with toxic shock syndrome. Ann Intern Med. 1982 Jun;96(6 Pt 2):969–971. doi: 10.7326/0003-4819-96-6-969. [DOI] [PubMed] [Google Scholar]
  7. Chu M. C., Kreiswirth B. N., Pattee P. A., Novick R. P., Melish M. E., James J. F. Association of toxic shock toxin-1 determinant with a heterologous insertion at multiple loci in the Staphylococcus aureus chromosome. Infect Immun. 1988 Oct;56(10):2702–2708. doi: 10.1128/iai.56.10.2702-2708.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chu M. C., Melish M. E., James J. F. Tryptophan auxotypy associated with Staphylococcus aureus that produce toxic-shock-syndrome toxin. J Infect Dis. 1985 Jun;151(6):1157–1158. doi: 10.1093/infdis/151.6.1157. [DOI] [PubMed] [Google Scholar]
  9. Clyne M., De Azavedo J., Carlson E., Arbuthnott J. Production of gamma-hemolysin and lack of production of alpha-hemolysin by Staphylococcus aureus strains associated with toxic shock syndrome. J Clin Microbiol. 1988 Mar;26(3):535–539. doi: 10.1128/jcm.26.3.535-539.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Garbe P. L., Arko R. J., Reingold A. L., Graves L. M., Hayes P. S., Hightower A. W., Chandler F. W., Broome C. V. Staphylococcus aureus isolates from patients with nonmenstrual toxic shock syndrome. Evidence for additional toxins. JAMA. 1985 May 3;253(17):2538–2542. [PubMed] [Google Scholar]
  11. Ho G., Campbell W. H., Carlson E. Ovine-associated Staphylococcus aureus protein with immunochemical similarity to toxic shock syndrome toxin 1. J Clin Microbiol. 1989 Jan;27(1):210–212. doi: 10.1128/jcm.27.1.210-212.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Koch A. L. The pertinence of the periodic selection phenomenon to prokaryote evolution. Genetics. 1974 May;77(1):127–142. doi: 10.1093/genetics/77.1.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kreiswirth B. N. Genetics and expression of toxic shock syndrome toxin 1: overview. Rev Infect Dis. 1989 Jan-Feb;11 (Suppl 1):S97–100. doi: 10.1093/clinids/11.supplement_1.s97. [DOI] [PubMed] [Google Scholar]
  14. Kreiswirth B. N., Löfdahl S., Betley M. J., O'Reilly M., Schlievert P. M., Bergdoll M. S., Novick R. P. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature. 1983 Oct 20;305(5936):709–712. doi: 10.1038/305709a0. [DOI] [PubMed] [Google Scholar]
  15. Kreiswirth B. N., O'Reilly M., Novick R. P. Genetic characterization and cloning of the toxic shock syndrome exotoxin. Surv Synth Pathol Res. 1984;3(1):73–82. [PubMed] [Google Scholar]
  16. Kreiswirth B. N., Projan S. J., Schlievert P. M., Novick R. P. Toxic shock syndrome toxin 1 is encoded by a variable genetic element. Rev Infect Dis. 1989 Jan-Feb;11 (Suppl 1):S83–S89. doi: 10.1093/clinids/11.supplement_1.s83. [DOI] [PubMed] [Google Scholar]
  17. Langmuir A. D., Worthen T. D., Solomon J., Ray C. G., Petersen E. The Thucydides syndrome. A new hypothesis for the cause of the plague of Athens. N Engl J Med. 1985 Oct 17;313(16):1027–1030. doi: 10.1056/NEJM198510173131618. [DOI] [PubMed] [Google Scholar]
  18. MacDonald K. L., Osterholm M. T., Hedberg C. W., Schrock C. G., Peterson G. F., Jentzen J. M., Leonard S. A., Schlievert P. M. Toxic shock syndrome. A newly recognized complication of influenza and influenzalike illness. JAMA. 1987 Feb 27;257(8):1053–1058. doi: 10.1001/jama.257.8.1053. [DOI] [PubMed] [Google Scholar]
  19. Musser J. M., Bemis D. A., Ishikawa H., Selander R. K. Clonal diversity and host distribution in Bordetella bronchiseptica. J Bacteriol. 1987 Jun;169(6):2793–2803. doi: 10.1128/jb.169.6.2793-2803.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Musser J. M., Hewlett E. L., Peppler M. S., Selander R. K. Genetic diversity and relationships in populations of Bordetella spp. J Bacteriol. 1986 Apr;166(1):230–237. doi: 10.1128/jb.166.1.230-237.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Musser J. M., Mattingly S. J., Quentin R., Goudeau A., Selander R. K. Identification of a high-virulence clone of type III Streptococcus agalactiae (group B Streptococcus) causing invasive neonatal disease. Proc Natl Acad Sci U S A. 1989 Jun;86(12):4731–4735. doi: 10.1073/pnas.86.12.4731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Peng H. L., Novick R. P., Kreiswirth B., Kornblum J., Schlievert P. Cloning, characterization, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus. J Bacteriol. 1988 Sep;170(9):4365–4372. doi: 10.1128/jb.170.9.4365-4372.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Quimby F., Nguyen H. T. Animal studies of toxic shock syndrome. Crit Rev Microbiol. 1985;12(1):1–44. doi: 10.3109/10408418509104424. [DOI] [PubMed] [Google Scholar]
  24. Rasheed J. K., Arko R. J., Feeley J. C., Chandler F. W., Thornsberry C., Gibson R. J., Cohen M. L., Jeffries C. D., Broome C. V. Acquired ability of Staphylococcus aureus to produce toxic shock-associated protein and resulting illness in a rabbit model. Infect Immun. 1985 Mar;47(3):598–604. doi: 10.1128/iai.47.3.598-604.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Reeves M. W., Arko R. J., Chandler F. W., Bridges N. B. Affinity purification of staphylococcal toxic shock syndrome toxin 1 and its pathologic effects in rabbits. Infect Immun. 1986 Feb;51(2):431–439. doi: 10.1128/iai.51.2.431-439.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Reeves M. W., Pine L., Feeley J. C., Wells D. E. Presence of toxic shock toxin in toxic shock and other clinical strains of Staphylococcus aureus. Infect Immun. 1984 Nov;46(2):590–597. doi: 10.1128/iai.46.2.590-597.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schlievert P. M., Osterholm M. T., Kelly J. A., Nishimura R. D. Toxin and enzyme characterization of Staphylococcus aureus isolates from patients with and without toxic shock syndrome. Ann Intern Med. 1982 Jun;96(6 Pt 2):937–940. doi: 10.7326/0003-4819-96-6-937. [DOI] [PubMed] [Google Scholar]
  28. Schlievert P. M., Shands K. N., Dan B. B., Schmid G. P., Nishimura R. D. Identification and characterization of an exotoxin from Staphylococcus aureus associated with toxic-shock syndrome. J Infect Dis. 1981 Apr;143(4):509–516. doi: 10.1093/infdis/143.4.509. [DOI] [PubMed] [Google Scholar]
  29. Schlievert P. M. Staphylococcal enterotoxin B and toxic-shock syndrome toxin-1 are significantly associated with non-menstrual TSS. Lancet. 1986 May 17;1(8490):1149–1150. doi: 10.1016/s0140-6736(86)91859-3. [DOI] [PubMed] [Google Scholar]
  30. Schutzer S. E., Fischetti V. A., Zabriskie J. B. Toxic shock syndrome and lysogeny in Staphylococcus aureus. Science. 1983 Apr 15;220(4594):316–318. doi: 10.1126/science.6220467. [DOI] [PubMed] [Google Scholar]
  31. See R. H., Adilman S., Bartlett K. H., Chow A. W. Colony immunoblot assay for the detection of staphylococcal toxic shock syndrome toxin 1 (TSST-1) with anti-TSST-1 F(ab')2 fragments. J Clin Microbiol. 1989 Sep;27(9):2050–2053. doi: 10.1128/jcm.27.9.2050-2053.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. See R. H., Chow A. W. Microbiology of toxic shock syndrome: overview. Rev Infect Dis. 1989 Jan-Feb;11 (Suppl 1):S55–S60. doi: 10.1093/clinids/11.supplement_1.s55. [DOI] [PubMed] [Google Scholar]
  33. Selander R. K., Caugant D. A., Ochman H., Musser J. M., Gilmour M. N., Whittam T. S. Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics. Appl Environ Microbiol. 1986 May;51(5):873–884. doi: 10.1128/aem.51.5.873-884.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Selander R. K., Levin B. R. Genetic diversity and structure in Escherichia coli populations. Science. 1980 Oct 31;210(4469):545–547. doi: 10.1126/science.6999623. [DOI] [PubMed] [Google Scholar]
  35. Shands K. N., Schmid G. P., Dan B. B., Blum D., Guidotti R. J., Hargrett N. T., Anderson R. L., Hill D. L., Broome C. V., Band J. D. Toxic-shock syndrome in menstruating women: association with tampon use and Staphylococcus aureus and clinical features in 52 cases. N Engl J Med. 1980 Dec 18;303(25):1436–1442. doi: 10.1056/NEJM198012183032502. [DOI] [PubMed] [Google Scholar]
  36. Todd J. K., Franco-Buff A., Lawellin D. W., Vasil M. L. Phenotypic distinctiveness of Staphylococcus aureus strains associated with toxic shock syndrome. Infect Immun. 1984 Aug;45(2):339–344. doi: 10.1128/iai.45.2.339-344.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Todd J., Fishaut M., Kapral F., Welch T. Toxic-shock syndrome associated with phage-group-I Staphylococci. Lancet. 1978 Nov 25;2(8100):1116–1118. doi: 10.1016/s0140-6736(78)92274-2. [DOI] [PubMed] [Google Scholar]
  38. Whittam T. S., Wachsmuth I. K., Wilson R. A. Genetic evidence of clonal descent of Escherichia coli O157:H7 associated with hemorrhagic colitis and hemolytic uremic syndrome. J Infect Dis. 1988 Jun;157(6):1124–1133. doi: 10.1093/infdis/157.6.1124. [DOI] [PubMed] [Google Scholar]
  39. de Azavedo J. C. Animal models for toxic shock syndrome: overview. Rev Infect Dis. 1989 Jan-Feb;11 (Suppl 1):S205–S209. doi: 10.1093/clinids/11.supplement_1.s205. [DOI] [PubMed] [Google Scholar]
  40. de Azavedo J. C., Arbuthnott J. P. Toxicity of staphylococcal toxic shock syndrome toxin 1 in rabbits. Infect Immun. 1984 Nov;46(2):314–317. doi: 10.1128/iai.46.2.314-317.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]

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