Aerobactin and other virulence factor genes among strains of Escherichia coli causing urosepsis: association with patient characteristics (original) (raw)

Abstract

To assess the role of aerobactin as a virulence factor among uropathogenic Escherichia coli, we determined the prevalence, location, and phenotypic expression of aerobactin determinants among 58 E. coli strains causing bacteremic urinary tract infections. We correlated the presence of the aerobactin system with antimicrobial-agent resistance, the presence and phenotypic expression of other uropathogenic virulence factor determinants (P fimbriae, hemolysin, and type 1 fimbriae), and characteristics of patients. Colony and Southern hybridization of total and plasmid DNA with DNA probes for each virulence factor showed that aerobactin determinants were present in 78% of the strains and were plasmid associated in 21%, whereas P fimbria, hemolysin, and type 1 fimbria determinants were present in 74, 43, and 98% of the strains, respectively, and were always chromosomal. Chromosomal aerobactin, P fimbria, and hemolysin determinants occurred together on the chromosome more often in strains from patients without predisposing urological or medical conditions (P = 0.04). Strains with plasmid-encoded aerobactin lacked determinants for P fimbriae (P = 0.004) and hemolysin (P = 0.0004), were resistant to multiple antimicrobial agents (P = 0.0001), and were found only in compromised patients. Mating experiments demonstrated that some aerobactin plasmids also encoded antimicrobial-agent resistance. These findings suggest that the determinants for aerobactin, P fimbriae, and hemolysin are conserved on the chromosome of the antimicrobial-agent-susceptible uropathogenic strains of E. coli which invade noncompromised patients. In contrast, these chromosomal virulence factors are often absent from E. coli strains causing urosepsis in compromised hosts; these strains may acquire plasmid aerobactin in conjunction with antimicrobial-agent resistance genes.

405

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Blumenstock E., Jann K. Adhesion of piliated Escherichia coli strains to phagocytes: differences between bacteria with mannose-sensitive pili and those with mannose-resistant pili. Infect Immun. 1982 Jan;35(1):264–269. doi: 10.1128/iai.35.1.264-269.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bradley D. E., Taylor D. E., Cohen D. R. Specification of surface mating systems among conjugative drug resistance plasmids in Escherichia coli K-12. J Bacteriol. 1980 Sep;143(3):1466–1470. doi: 10.1128/jb.143.3.1466-1470.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brauner A., Leissner M., Wretlind B., Julander I., Svenson S. B., Källenius G. Occurrence of P-fimbriated Escherichia coli in patients with bacteremia. Eur J Clin Microbiol. 1985 Dec;4(6):566–569. doi: 10.1007/BF02013396. [DOI] [PubMed] [Google Scholar]
  4. Brenner D. J., Fanning G. R., Johnson K. E., Citarella R. V., Falkow S. Polynucleotide sequence relationships among members of Enterobacteriaceae. J Bacteriol. 1969 May;98(2):637–650. doi: 10.1128/jb.98.2.637-650.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Carbonetti N. H., Boonchai S., Parry S. H., Väisänen-Rhen V., Korhonen T. K., Williams P. H. Aerobactin-mediated iron uptake by Escherichia coli isolates from human extraintestinal infections. Infect Immun. 1986 Mar;51(3):966–968. doi: 10.1128/iai.51.3.966-968.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Carbonetti N. H., Williams P. H. A cluster of five genes specifying the aerobactin iron uptake system of plasmid ColV-K30. Infect Immun. 1984 Oct;46(1):7–12. doi: 10.1128/iai.46.1.7-12.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Felmlee T., Pellett S., Welch R. A. Nucleotide sequence of an Escherichia coli chromosomal hemolysin. J Bacteriol. 1985 Jul;163(1):94–105. doi: 10.1128/jb.163.1.94-105.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hull R., Bieler S., Falkow S., Hull S. Chromosomal map position of genes encoding P adhesins in uropathogenic Escherichia coli. Infect Immun. 1986 Feb;51(2):693–695. doi: 10.1128/iai.51.2.693-695.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hull S. I., Hull R. A., Minshew B. H., Falkow S. Genetics of hemolysin of Escherichia coli. J Bacteriol. 1982 Aug;151(2):1006–1012. doi: 10.1128/jb.151.2.1006-1012.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Johnson J. R., Roberts P. L., Stamm W. E. P fimbriae and other virulence factors in Escherichia coli urosepsis: association with patients' characteristics. J Infect Dis. 1987 Jul;156(1):225–229. doi: 10.1093/infdis/156.1.225. [DOI] [PubMed] [Google Scholar]
  11. Kado C. I., Liu S. T. Rapid procedure for detection and isolation of large and small plasmids. J Bacteriol. 1981 Mar;145(3):1365–1373. doi: 10.1128/jb.145.3.1365-1373.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Knapp S., Hacker J., Then I., Müller D., Goebel W. Multiple copies of hemolysin genes and associated sequences in the chromosomes of uropathogenic Escherichia coli strains. J Bacteriol. 1984 Sep;159(3):1027–1033. doi: 10.1128/jb.159.3.1027-1033.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Linggood M. A., Ingram P. L. The role of alpha haemolysin in the virulence of Escherichia coli for mice. J Med Microbiol. 1982 Feb;15(1):23–30. doi: 10.1099/00222615-15-1-23. [DOI] [PubMed] [Google Scholar]
  14. Linggood M. A., Roberts M., Ford S., Parry S. H., Williams P. H. Incidence of the aerobactin iron uptake system among Escherichia coli isolates from infections of farm animals. J Gen Microbiol. 1987 Apr;133(4):835–842. doi: 10.1099/00221287-133-4-835. [DOI] [PubMed] [Google Scholar]
  15. Lomberg H., Hanson L. A., Jacobsson B., Jodal U., Leffler H., Edén C. S. Correlation of P blood group, vesicoureteral reflux, and bacterial attachment in patients with recurrent pyelonephritis. N Engl J Med. 1983 May 19;308(20):1189–1192. doi: 10.1056/NEJM198305193082003. [DOI] [PubMed] [Google Scholar]
  16. Low D., David V., Lark D., Schoolnik G., Falkow S. Gene clusters governing the production of hemolysin and mannose-resistant hemagglutination are closely linked in Escherichia coli serotype O4 and O6 isolates from urinary tract infections. Infect Immun. 1984 Jan;43(1):353–358. doi: 10.1128/iai.43.1.353-358.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Maas R. An improved colony hybridization method with significantly increased sensitivity for detection of single genes. Plasmid. 1983 Nov;10(3):296–298. doi: 10.1016/0147-619x(83)90045-8. [DOI] [PubMed] [Google Scholar]
  18. Minshew B. H., Jorgensen J., Counts G. W., Falkow S. Association of hemolysin production, hemagglutination of human erythrocytes, and virulence for chicken embryos of extraintestinal Escherichia coli isolates. Infect Immun. 1978 Apr;20(1):50–54. doi: 10.1128/iai.20.1.50-54.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Montgomerie J. Z., Bindereif A., Neilands J. B., Kalmanson G. M., Guze L. B. Association of hydroxamate siderophore (aerobactin) with Escherichia coli isolated from patients with bacteremia. Infect Immun. 1984 Dec;46(3):835–838. doi: 10.1128/iai.46.3.835-838.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Normark S., Lark D., Hull R., Norgren M., Båga M., O'Hanley P., Schoolnik G., Falkow S. Genetics of digalactoside-binding adhesin from a uropathogenic Escherichia coli strain. Infect Immun. 1983 Sep;41(3):942–949. doi: 10.1128/iai.41.3.942-949.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. O'Hanley P., Low D., Romero I., Lark D., Vosti K., Falkow S., Schoolnik G. Gal-Gal binding and hemolysin phenotypes and genotypes associated with uropathogenic Escherichia coli. N Engl J Med. 1985 Aug 15;313(7):414–420. doi: 10.1056/NEJM198508153130704. [DOI] [PubMed] [Google Scholar]
  22. Orndorff P. E., Falkow S. Organization and expression of genes responsible for type 1 piliation in Escherichia coli. J Bacteriol. 1984 Aug;159(2):736–744. doi: 10.1128/jb.159.2.736-744.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sansonetti P. J., Hale T. L., Dammin G. J., Kapfer C., Collins H. H., Jr, Formal S. B. Alterations in the pathogenicity of Escherichia coli K-12 after transfer of plasmid and chromosomal genes from Shigella flexneri. Infect Immun. 1983 Mar;39(3):1392–1402. doi: 10.1128/iai.39.3.1392-1402.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Silverblatt F. J., Dreyer J. S., Schauer S. Effect of pili on susceptibility of Escherichia coli to phagocytosis. Infect Immun. 1979 Apr;24(1):218–223. doi: 10.1128/iai.24.1.218-223.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Svanborg Edén C., Bjursten L. M., Hull R., Hull S., Magnusson K. E., Moldovano Z., Leffler H. Influence of adhesins on the interaction of Escherichia coli with human phagocytes. Infect Immun. 1984 Jun;44(3):672–680. doi: 10.1128/iai.44.3.672-680.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Uhlin B. E., Båga M., Göransson M., Lindberg F. P., Lund B., Norgren M., Normark S. Genes determining adhesin formation in uropathogenic Escherichia coli. Curr Top Microbiol Immunol. 1985;118:163–178. doi: 10.1007/978-3-642-70586-1_9. [DOI] [PubMed] [Google Scholar]
  27. Valvano M. A., Crosa J. H. Aerobactin iron transport genes commonly encoded by certain ColV plasmids occur in the chromosome of a human invasive strain of Escherichia coli K1. Infect Immun. 1984 Oct;46(1):159–167. doi: 10.1128/iai.46.1.159-167.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Valvano M. A., Silver R. P., Crosa J. H. Occurrence of chromosome- or plasmid-mediated aerobactin iron transport systems and hemolysin production among clonal groups of human invasive strains of Escherichia coli K1. Infect Immun. 1986 Apr;52(1):192–199. doi: 10.1128/iai.52.1.192-199.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Väisänen-Rhen V., Elo J., Väisänen E., Siitonen A., Orskov I., Orskov F., Svenson S. B., Mäkelä P. H., Korhonen T. K. P-fimbriated clones among uropathogenic Escherichia coli strains. Infect Immun. 1984 Jan;43(1):149–155. doi: 10.1128/iai.43.1.149-155.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Väisänen V., Elo J., Tallgren L. G., Siitonen A., Mäkelä P. H., Svanborg-Edén C., Källenius G., Svenson S. B., Hultberg H., Korhonen T. Mannose-resistant haemagglutination and P antigen recognition are characteristic of Escherichia coli causing primary pyelonephritis. Lancet. 1981 Dec 19;2(8260-61):1366–1369. doi: 10.1016/s0140-6736(81)92796-3. [DOI] [PubMed] [Google Scholar]
  31. Williams P. H., Warner P. J. ColV plasmid-mediated, colicin V-independent iron uptake system of invasive strains of Escherichia coli. Infect Immun. 1980 Aug;29(2):411–416. doi: 10.1128/iai.29.2.411-416.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]