Skip to main content
Journal of Clinical Microbiology logoLink to Journal of Clinical Microbiology
. 1996 Dec;34(12):3101–3107. doi: 10.1128/jcm.34.12.3101-3107.1996

O serogroups, biotypes, and eae genes in Escherichia coli strains isolated from diarrheic and healthy rabbits.

J E Blanco 1, M Blanco 1, J Blanco 1, A Mora 1, L Balaguer 1, M Mouriño 1, A Juarez 1, W H Jansen 1
PMCID: PMC229466  PMID: 8940455

Abstract

A total of 305 Escherichia coli strains isolated from diarrheic and healthy rabbits in 10 industrial fattening farms from different areas of Spain were serotyped, biotyped, and tested for the presence of the eae gene and toxin production. The characteristics found in strains isolated from healthy rabbits were generally different from those observed in E. coli strains associated with disease. Thus, strains with the eae gene (74% versus 22%); strains belonging to serogroups O26, O49, O92, O103, and O128 (64% versus 12%); rhamnose-negative strains (51% versus 5%); and rhamnose-negative O103 strains with eae genes present (41% versus 1%) were significantly (P < 0.001 in all cases) more frequently detected in isolates from diarrheic animals than in those from healthy rabbits. Whereas a total of 35 serogroups and 17 biotypes were distinguished, the majority of the strains obtained from diarrheic rabbits belonged to only four serobiotypes, which in order of frequency were O103:B14 (72 strains), O103:B6 (16 strains), O26:B13 (12 strains), and O128:B30 (12 strains). These four serobiotypes accounted for 48% (112 of 231) and 5% (4 of 74) of the E. coli strains isolated from diarrheic and healthy rabbits, respectively. Only six strains were toxigenic (three CNF1+, two CNF2+, and one VT1+). We conclude that enteropathogenic E. coli strains that possess the eae gene are a common cause of diarrhea in Spanish rabbit farms and that the rhamnose-negative highly pathogenic strains of serotype O103:K-:H2 and biotype B14 are especially predominant. Detection of the eae gene is a useful method for the identification of enteropathogenic E. coli strains from rabbits. However, a combination of serogrouping and biotyping may be sufficient to accurately identify the highly pathogenic strains for rabbits.

Full Text

The Full Text of this article is available as a PDF (218.2 KB).

Selected References

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

  1. Blanco J. E., Blanco M., Blanco J., Rioja L., Ducha J. Serotypes, toxins and antibiotic resistance of Escherichia coli strains isolated from diarrhoeic and healthy rabbits in Spain. Vet Microbiol. 1994 Jan;38(3):193–201. doi: 10.1016/0378-1135(94)90001-9. [DOI] [PubMed] [Google Scholar]
  2. Blanco J., Blanco M., Alonso M. P., Blanco J. E., González E. A., Garabal J. I. Characteristics of haemolytic Escherichia coli with particular reference to production of cytotoxic necrotizing factor type 1 (CNF1). Res Microbiol. 1992 Nov-Dec;143(9):869–878. doi: 10.1016/0923-2508(92)90074-x. [DOI] [PubMed] [Google Scholar]
  3. Blanco J., Blanco M., González E. A., Alonso M. P., Garabal J. I. Comparative evaluation of three tests for the detection of Escherichia coli cytotoxic necrotizing factors (CNF1 and CNF2) using filtrates of cultures treated with mitomycin C. FEMS Microbiol Lett. 1990 Jun 1;57(3):311–316. doi: 10.1016/0378-1097(90)90086-6. [DOI] [PubMed] [Google Scholar]
  4. Blanco M., Blanco J., Blanco J. E., González E. A., Gomes T. A., Zerbini L. F., Yano T., de Castro A. F. Genes coding for Shiga-like toxins in bovine verotoxin-producing Escherichia coli (VTEC) strains belonging to different O:K:H serotypes. Vet Microbiol. 1994 Nov;42(2-3):105–110. doi: 10.1016/0378-1135(94)90010-8. [DOI] [PubMed] [Google Scholar]
  5. Blanco M., Blanco J., Blanco J. E., Ramos J. Enterotoxigenic, verotoxigenic, and necrotoxigenic Escherichia coli isolated from cattle in Spain. Am J Vet Res. 1993 Sep;54(9):1446–1451. [PubMed] [Google Scholar]
  6. Camguilhem R., Milon A. Biotypes and O serogroups of Escherichia coli involved in intestinal infections of weaned rabbits: clues to diagnosis of pathogenic strains. J Clin Microbiol. 1989 Apr;27(4):743–747. doi: 10.1128/jcm.27.4.743-747.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cantey J. R., Blake R. K. Diarrhea due to Escherichia coli in the rabbit: a novel mechanism. J Infect Dis. 1977 Mar;135(3):454–462. doi: 10.1093/infdis/135.3.454. [DOI] [PubMed] [Google Scholar]
  8. De Rycke J., González E. A., Blanco J., Oswald E., Blanco M., Boivin R. Evidence for two types of cytotoxic necrotizing factor in human and animal clinical isolates of Escherichia coli. J Clin Microbiol. 1990 Apr;28(4):694–699. doi: 10.1128/jcm.28.4.694-699.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Echeverria P., Orskov F., Orskov I., Knutton S., Scheutz F., Brown J. E., Lexomboon U. Attaching and effacing enteropathogenic Escherichia coli as a cause of infantile diarrhea in Bangkok. J Infect Dis. 1991 Sep;164(3):550–554. doi: 10.1093/infdis/164.3.550. [DOI] [PubMed] [Google Scholar]
  10. Gannon V. P., Rashed M., King R. K., Thomas E. J. Detection and characterization of the eae gene of Shiga-like toxin-producing Escherichia coli using polymerase chain reaction. J Clin Microbiol. 1993 May;31(5):1268–1274. doi: 10.1128/jcm.31.5.1268-1274.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Giammanco A., Maggio M., Giammanco G., Morelli R., Minelli F., Scheutz F., Caprioli A. Characteristics of Escherichia coli strains belonging to enteropathogenic E. coli serogroups isolated in Italy from children with diarrhea. J Clin Microbiol. 1996 Mar;34(3):689–694. doi: 10.1128/jcm.34.3.689-694.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jerse A. E., Kaper J. B. The eae gene of enteropathogenic Escherichia coli encodes a 94-kilodalton membrane protein, the expression of which is influenced by the EAF plasmid. Infect Immun. 1991 Dec;59(12):4302–4309. doi: 10.1128/iai.59.12.4302-4309.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jerse A. E., Yu J., Tall B. D., Kaper J. B. A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. Proc Natl Acad Sci U S A. 1990 Oct;87(20):7839–7843. doi: 10.1073/pnas.87.20.7839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Karmali M. A. Infection by verocytotoxin-producing Escherichia coli. Clin Microbiol Rev. 1989 Jan;2(1):15–38. doi: 10.1128/cmr.2.1.15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Leroy-Setrin S., Lesage M. C., Chaslus-Dancla E., Lafont J. P. Clonal diffusion of EPEC-like Escherichia coli from rabbits as detected by ribotyping and random amplified polymorphic DNA assays. Epidemiol Infect. 1995 Feb;114(1):113–121. doi: 10.1017/s0950268800051967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Leroy S. M., Lesage M. C., Chaslus-Dancla E., Lafont J. P. Presence of eaeA sequences in pathogenic and nonpathogenic Escherichia coli strains isolated from weaned rabbits. J Med Microbiol. 1994 Feb;40(2):90–94. doi: 10.1099/00222615-40-2-90. [DOI] [PubMed] [Google Scholar]
  17. Levine M. M. Escherichia coli that cause diarrhea: enterotoxigenic, enteropathogenic, enteroinvasive, enterohemorrhagic, and enteroadherent. J Infect Dis. 1987 Mar;155(3):377–389. doi: 10.1093/infdis/155.3.377. [DOI] [PubMed] [Google Scholar]
  18. Licois D. Escherichia coli entéropathogènes du lapin. Ann Rech Vet. 1992;23(1):27–48. [PubMed] [Google Scholar]
  19. Licois D., Guillot J. F., Mouline C., Reynaud A. Susceptibility of the rabbit to an enteropathogenic strain of Escherichia coli 0103: effect of animals' age. Ann Rech Vet. 1992;23(3):225–232. [PubMed] [Google Scholar]
  20. Licois D., Reynaud A., Federighi M., Gaillard-Martinie B., Guillot J. F., Joly B. Scanning and transmission electron microscopic study of adherence of Escherichia coli O103 enteropathogenic and/or enterohemorrhagic strain GV in enteric infection in rabbits. Infect Immun. 1991 Oct;59(10):3796–3800. doi: 10.1128/iai.59.10.3796-3800.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Okerman L., Devriese L. A. Biotypes of enteropathogenic Escherichia coli strains from rabbits. J Clin Microbiol. 1985 Dec;22(6):955–958. doi: 10.1128/jcm.22.6.955-958.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Okerman L. Enteric infections caused by non-enterotoxigenic Escherichia coli in animals: occurrence and pathogenicity mechanisms. A review. Vet Microbiol. 1987 May;14(1):33–46. doi: 10.1016/0378-1135(87)90050-2. [DOI] [PubMed] [Google Scholar]
  23. Peeters J. E., Charlier G. J., Halen P. H. Pathogenicity of attaching effacing enteropathogenic Escherichia coli isolated from diarrheic suckling and weanling rabbits for newborn rabbits. Infect Immun. 1984 Dec;46(3):690–696. doi: 10.1128/iai.46.3.690-696.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Peeters J. E., Charlier G. J., Raeymaekers R. Scanning and transmission electron microscopy of attaching effacing Escherichia coli in weanling rabbits. Vet Pathol. 1985 Jan;22(1):54–59. doi: 10.1177/030098588502200109. [DOI] [PubMed] [Google Scholar]
  25. Peeters J. E., Geeroms R., Orskov F. Biotype, serotype, and pathogenicity of attaching and effacing enteropathogenic Escherichia coli strains isolated from diarrheic commercial rabbits. Infect Immun. 1988 Jun;56(6):1442–1448. doi: 10.1128/iai.56.6.1442-1448.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Peeters J. E., Pohl P., Okerman L., Devriese L. A. Pathogenic properties of Escherichia coli strains isolated from diarrheic commercial rabbits. J Clin Microbiol. 1984 Jul;20(1):34–39. doi: 10.1128/jcm.20.1.34-39.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Percy D. H., Muckle C. A., Hampson R. J., Brash M. L. The enteritis complex in domestic rabbits: A field study. Can Vet J. 1993 Feb;34(2):95–102. [PMC free article] [PubMed] [Google Scholar]
  28. Pohl P. H., Peeters J. E., Jacquemin E. R., Lintermans P. F., Mainil J. G. Identification of eae sequences in enteropathogenic Escherichia coli strains from rabbits. Infect Immun. 1993 May;61(5):2203–2206. doi: 10.1128/iai.61.5.2203-2206.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Prohászka L. Antibacterial effect of volatile fatty acids in enteric E. coli-infections of rabbits. Zentralbl Veterinarmed B. 1980;27(8):631–639. doi: 10.1111/j.1439-0450.1980.tb01726.x. [DOI] [PubMed] [Google Scholar]
  30. Robins-Browne R. M., Tokhi A. M., Adams L. M., Bennett-Wood V., Moisidis A. V., Krejany E. O., O'Gorman L. E. Adherence characteristics of attaching and effacing strains of Escherichia coli from rabbits. Infect Immun. 1994 May;62(5):1584–1592. doi: 10.1128/iai.62.5.1584-1592.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Varga J., Pesti L. Serological and some pathological characteristics of Escherichia coli strains isolated from rabbits. Zentralbl Veterinarmed B. 1982 Mar;29(2):145–152. doi: 10.1111/j.1439-0450.1982.tb01209.x. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Clinical Microbiology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES