• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of jcmPermissionsJournals.ASM.orgJournalJCM ArticleJournal InfoAuthorsReviewers
J Clin Microbiol. Feb 1993; 31(2): 296–301.
PMCID: PMC262753

Identification of a clone of Escherichia coli O103:H2 as a potential agent of hemolytic-uremic syndrome in France.


In a French multicenter study, six verocytotoxin-producing Escherichia coli strains were isolated from the stools of 6 of 69 children suffering from hemolytic-uremic syndrome. All strains belonged to serotype O103:H2, a serotype commonly associated with diarrhea in weaned rabbits in France. To determine whether the strains from humans and rabbits were genetically related, they were compared by analyzing their esterase electropherotypes and the restriction fragment length polymorphisms of the ribosomal DNA regions. A common clonal origin of these pathogenic strains was suggested by their identical esterase electropherotypes and their identical ribotypes, in addition to their identical serotypes. However, strains from humans, which are cytotoxic for HeLa cells through the production of verocytotoxin type 1, do not show adhesion in vitro to HeLa 229 cells and cannot infect rabbits. On the other hand, strains from rabbits do not carry the verocytotoxin type 1 gene, are not cytotoxic for Hela cells, and adhere to ileal villi and HeLa 229 cells because of the expression of their 32-kDa adhesin. Our results therefore identify a clone of verocytotoxin-producing E. coli O103:H2 as a potential agent of hemolytic uremic syndrome in France. They further suggest that clones from humans and rabbits probably have a common origin but that adaptation to the two species occurred by different mechanisms. Thus, they eliminate the hypothesis that the species is horizontally transmitted between rabbits and humans.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (1.3M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Images in this article

Click on the image to see a larger version.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Bingen EH, Denamur E, Lambert-Zechovsky NY, Bourdois A, Mariani-Kurkdjian P, Cezard JP, Navarro J, Elion J. DNA restriction fragment length polymorphism differentiates crossed from independent infections in nosocomial Xanthomonas maltophilia bacteremia. J Clin Microbiol. 1991 Jul;29(7):1348–1350. [PMC free article] [PubMed]
  • Birnboim HC, Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. [PMC free article] [PubMed]
  • 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. [PMC free article] [PubMed]
  • de Graaf FK, Klemm P, Gaastra W. Purification, characterization, and partial covalent structure of Escherichia coli adhesive antigen K99. Infect Immun. 1981 Sep;33(3):877–883. [PMC free article] [PubMed]
  • Denamur E, Sayada C, Souriau A, Orfila J, Rodolakis A, Elion J. Restriction pattern of the major outer-membrane protein gene provides evidence for a homogeneous invasive group among ruminant isolates of Chlamydia psittaci. J Gen Microbiol. 1991 Nov;137(11):2525–2530. [PubMed]
  • Dorn CR, Scotland SM, Smith HR, Willshaw GA, Rowe B. Properties of Vero cytotoxin-producing Escherichia coli of human and animal origin belonging to serotypes other than O157:H7. Epidemiol Infect. 1989 Aug;103(1):83–95. [PMC free article] [PubMed]
  • Fong JS, de Chadarevian JP, Kaplan BS. Hemolytic-uremic syndrome. Current concepts and management. Pediatr Clin North Am. 1982 Aug;29(4):835–856. [PubMed]
  • Fontaine A, Arondel J, Sansonetti PJ. Role of Shiga toxin in the pathogenesis of bacillary dysentery, studied by using a Tox- mutant of Shigella dysenteriae 1. Infect Immun. 1988 Dec;56(12):3099–3109. [PMC free article] [PubMed]
  • Gentry MK, Dalrymple JM. Quantitative microtiter cytotoxicity assay for Shigella toxin. J Clin Microbiol. 1980 Sep;12(3):361–366. [PMC free article] [PubMed]
  • Goullet P, Picard B. Comparative electrophoretic polymorphism of esterases and other enzymes in Escherichia coli. J Gen Microbiol. 1989 Jan;135(1):135–143. [PubMed]
  • Goullet P, Picard B. Characterization of enterobacteria by esterase specific-activity profiles. J Gen Microbiol. 1990 Mar;136(3):431–440. [PubMed]
  • Gransden WR, Damm MA, Anderson JD, Carter JE, Lior H. Further evidence associating hemolytic uremic syndrome with infection by Verotoxin-producing Escherichia coli O157:H7. J Infect Dis. 1986 Sep;154(3):522–524. [PubMed]
  • Grimont F, Grimont PA. Ribosomal ribonucleic acid gene restriction patterns as potential taxonomic tools. Ann Inst Pasteur Microbiol. 1986 Sep-Oct;137B(2):165–175. [PubMed]
  • Gurwith MJ, Williams TW. Gastroenteritis in children: a two-year review in Manitoba. I. Etiology. J Infect Dis. 1977 Aug;136(2):239–247. [PubMed]
  • Hall GA, Dorn CR, Chanter N, Scotland SM, Smith HR, Rowe B. Attaching and effacing lesions in vivo and adhesion to tissue culture cells of Vero-cytotoxin-producing Escherichia coli belonging to serogroups O5 and O103. J Gen Microbiol. 1990 Apr;136(4):779–786. [PubMed]
  • Kaplan BS, Cleary TG, Obrig TG. Recent advances in understanding the pathogenesis of the hemolytic uremic syndromes. Pediatr Nephrol. 1990 May;4(3):276–283. [PubMed]
  • Karmali MA. Infection by verocytotoxin-producing Escherichia coli. Clin Microbiol Rev. 1989 Jan;2(1):15–38. [PMC free article] [PubMed]
  • Karmali MA, Petric M, Lim C, Fleming PC, Arbus GS, Lior H. The association between idiopathic hemolytic uremic syndrome and infection by verotoxin-producing Escherichia coli. J Infect Dis. 1985 May;151(5):775–782. [PubMed]
  • Kleanthous H, Smith HR, Scotland SM, Gross RJ, Rowe B, Taylor CM, Milford DV. Haemolytic uraemic syndromes in the British Isles, 1985-8: association with verocytotoxin producing Escherichia coli. Part 2: Microbiological aspects. Arch Dis Child. 1990 Jul;65(7):722–727. [PMC free article] [PubMed]
  • Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. [PubMed]
  • Licois D, Reynaud A, Federighi M, Gaillard-Martinie B, Guillot JF, 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. [PMC free article] [PubMed]
  • Milon A, Esslinger J, Camguilhem R. Adhesion of Escherichia coli strains isolated from diarrheic weaned rabbits to intestinal villi and HeLa cells. Infect Immun. 1990 Aug;58(8):2690–2695. [PMC free article] [PubMed]
  • Mullis KB. The polymerase chain reaction in an anemic mode: how to avoid cold oligodeoxyribonuclear fusion. PCR Methods Appl. 1991 Aug;1(1):1–4. [PubMed]
  • Picard B, Picard-Pasquier N, Krishnamoorthy R, Goullet P. Characterization of highly virulent Escherichia coli strains by ribosomal DNA restriction fragment length polymorphism. FEMS Microbiol Lett. 1991 Aug 1;66(2):183–188. [PubMed]
  • Pollard DR, Johnson WM, Lior H, Tyler SD, Rozee KR. Rapid and specific detection of verotoxin genes in Escherichia coli by the polymerase chain reaction. J Clin Microbiol. 1990 Mar;28(3):540–545. [PMC free article] [PubMed]
  • Reynaud A, Federighi M, Licois D, Guillot JF, Joly B. R plasmid in Escherichia coli O103 coding for colonization of the rabbit intestinal tract. Infect Immun. 1991 Jun;59(6):1888–1892. [PMC free article] [PubMed]
  • Scaletsky IC, Silva ML, Trabulsi LR. Distinctive patterns of adherence of enteropathogenic Escherichia coli to HeLa cells. Infect Immun. 1984 Aug;45(2):534–536. [PMC free article] [PubMed]
  • Southern EM. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. [PubMed]
  • Strockbine NA, Marques LR, Newland JW, Smith HW, Holmes RK, O'Brien AD. Two toxin-converting phages from Escherichia coli O157:H7 strain 933 encode antigenically distinct toxins with similar biologic activities. Infect Immun. 1986 Jul;53(1):135–140. [PMC free article] [PubMed]
  • Strockbine NA, Parsonnet J, Greene K, Kiehlbauch JA, Wachsmuth IK. Molecular epidemiologic techniques in analysis of epidemic and endemic Shigella dysenteriae type 1 strains. J Infect Dis. 1991 Feb;163(2):406–409. [PubMed]
  • Tarr PI, Neill MA, Clausen CR, Watkins SL, Christie DL, Hickman RO. Escherichia coli O157:H7 and the hemolytic uremic syndrome: importance of early cultures in establishing the etiology. J Infect Dis. 1990 Aug;162(2):553–556. [PubMed]
  • Uriel J. Méthode d'électrophorèse dans des gels d'acrylamide-agarose. Bull Soc Chim Biol (Paris) 1966;48(8):969–982. [PubMed]
  • Whittam TS, Wachsmuth IK, Wilson RA. 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. [PubMed]

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


Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...


Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...