Enterohaemorrhagic Escherichia coli O26:H11/H-: A human pathogen in emergence

Berliner und Munchener Tierarztliche Wochenschrift

Volumn 120, Issue 7-8, 2007, Pages 279-287

  Bielaszewska, Martina ^a   Zhang, Wenlan ^a   Mellmann, Alexander ^a   Karch, Helge ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Enterohaemorrhagic Escherichia coli O26; Epidemiology; Evolution; Haemolytic uraemic syndrome; Outbreak; Virulence

Indexed keywords

SHIGA TOXIN; VIRULENCE FACTOR;

ANIMAL; BIOSYNTHESIS; ENTEROBACTER INFECTION; EPIDEMIC; ESCHERICHIA COLI; FOOD CONTROL; GENETICS; HEMOLYTIC UREMIC SYNDROME; HUMAN; METABOLISM; MICROBIOLOGY; PATHOGENICITY; REVIEW; VIRULENCE;

ANIMALS; DISEASE OUTBREAKS; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FOOD MICROBIOLOGY; HEMOLYTIC-UREMIC SYNDROME; HUMANS; SHIGA TOXINS; VIRULENCE; VIRULENCE FACTORS;

BOS; ESCHERICHIA COLI;

EID: 34447515550     PISSN: 00059366     EISSN: None     Source Type: Journal    
DOI: 10.2376/0005-9366-120-279     Document Type: Review

References (91)

1. Abu-Median A. B., P. M. van Diemen, F. Dziva, I. Vlisidou, T. S. Wallis, M. P. Stevens (2006): Functional analysis of lymphostatin homologues in enterohaemorrhagic Escherichia coli. FEMS Microbiol. Lett. 258, 43-49.
2. Aldick T., M. Bielaszewska, W. Zhang, J. Brockmeyer, H. Schmidt A. W. Friedrich, K. S. Kim, M. A. Schmidt, H. Karch (2007): Hemolysin from Shiga toxin-negative Escherichia coli O26 strains injures microvascular endothelium. Microb. Infect. doi:10.1016/j.micinf.2006.12.001.
3. - infection and consumption of unpasteurized cow's milk. Int. J. Infect. Dis. 7, 42-45.
4. Anjum M. F., S. Lucchini, A. Thompson, J. C. Hinton, and M. J. Woodward (2003): Comparative genomic indexing reveals the phylogenomics of Escherichia coli pathogens. Infect. Immun. 71, 4674-4683.
5. Beutin L., G. Krause, S. Zimmermann, S. Kaulfuss, K. Gleier (2004): Characterization of Shiga toxin-producing Escherichia coli strains isolated from human patients in Germany over a 3-year period. J. Clin. Microbiol. 42, 1099-1108.
6. Bielaszewska M., J. Janda, K. Blahova, J. Feber, V. Potuznik, A. Souckova (1996): Verocytotoxin-producing Escherichia coli in children with hemolytic uremic syndrome in the Czech Republic. Clin. Nephrol. 46, 42-44.
7. Bielaszewska M., H. Karch (2005): Consequences of enterohaemorrhagic Escherichia coli infection for the vascular endothelium. Thromb. Haemost. 94, 312-318.
8. Bielaszewska M., W. Zhang, P. I. Tarr, A.-K. Sonntag, H. Karch (2005a): Molecular profiling and phenotype analysis of Escherichia coli O26:H11 and O26:NM: Secular and geographic consistency of enterohemorrhagic and enteropathogenic isolates. J. Clin. Microbiol. 43, 4225-4228.
9. Bielaszewska M., P. I. Tarr, H. Karch, W. Zhang, W. Mathys (2005b): Phenotypic and molecular analysis of tellurite resistance among enterohemorrhagic Escherichia coli O157:H7 and sorbitolfermenting O157:NM clinical isolates. J. Clin. Microbiol. 43, 452-454.
10. Bielaszewska M., A. W. Friedrich, T. Aldick, R. Schurk-Bulgrin, H. Karch (2006): Shiga toxin activatable by intestinal mucus in Escherichia coli isolated from humans: predictor for a severe clinical outcome. Clin. Infect. Dis. 43, 1160-1167.
11. Bielaszewska M., A.-K. Sonntag, M. A. Schmidt, H. Karch (2007): Presence of virulence and fitness gene modules of enterohemorrhagic Escherichia coli in atypical enteropathogenic Escherichia coli O26. Microb. Infect., in press.
12. Blanco J. E., M. Blanco, M. P. Alonso, A. Mora, G. Dahbi, M. A. Coira, J. Blanco (2004a): Serotypes, virulence genes, and intimin types of Shiga toxin (verotoxin)-producing Escherichia coli isolates from human patients: prevalence in Lugo, Spain, from 1992 through 1999. J. Clin. Microbiol. 42, 311-319.
13. Blanco M., J. E. Blanco, A. Mora, G. Dahbi, M. P. Alonso, E. A. Gonzalez, M. I. Bernardez, J. Blanco (2004b): Serotypes, virulence genes, and intimin types of Shiga toxin (verotoxin)-producing Escherichia coli isolates from cattle in Spain and identification of a new intimin variant gene (eae-xi). J. Clin. Microbiol. 42, 645-651.
14. Bokete T. N., T. S. Whittam, R. S. Wilson, C. R. Clausen, C. M. O'Callahan, S.L. Moseley, T.R. Fritsche, P.I. Tarr (1997): Genetic and phenotypic analysis of Escherichia coli with enteropathogenic characteristics isolated from Seattle children. J. Infect.Dis. 175, 1382-1389.
15. Brooks J.T., E.G. Sowers, J.G. Wells, K.D. Greene, P M. Griffin, R.M. Hoekstra, N.A. Strockbine (2005): Non-O157 Shiga toxin-producing Escherichia coli infections in the United States, 1983-2002. J. Infect. Dis. 192, 1422-1429.
16. Buchrieser C., R. Brosch, S. Bach, A. Guiyoule, E. Carniel (1998): The high pathogenicity island of Yersinia pseudotuberculosis can be inserted into any of the three chromosomal asn tRNA genes. Mol. Microbiol. 30, 965-978.
17. Carniel E (2001): The Yersinia high-pathogenicity island: an iron-uptake island. Microbes Infect. 3, 561-569.
18. Cobbold R., P. Desmarchelier (2001): Characterisation and clonal relationships of Shiga-toxigenic Escherichia coli (STEC) isolated from Australian dairy cattle. Vet. Microbiol. 79, 323-335.
19. Dobrindt U., F. Agerer, K. Michaelis, A. Janka, C. Buchrieser, M. Samuelson, C. Svanborg, G. Gottschalk, H. Karch, J. Hacker (2003): Analysis of genome plasticity in pathogenic and commensal Escherichia coli isolates by use of DNA arrays. J. Bacteriol. 185, 1831-1840.
20. Donnenberg M., T. S. Whittam (2001): Pathogenesis and evolution of virulence in enteropathogenic and enterohemorrhagic Escherichia coli. J. Clin. Invest. 107, 539-548.
21. Eklund M., F. Scheutz, A. Siitonen (2001): Clinical isolates of non-O157 Shiga toxin-producing Escherichia coli: serotypes, virulence characteristics, and molecular profiles of strains of the same serotype. J. Clin. Microbiol. 39, 2829-2834.
22. Elliott E. J., R. M. Robins-Browne, E. V. O'Loughlin, V. Bennett-Wood, J. Bourke, P. Henning, G. G. Hogg, J. Knight, H. Powell, D. Redmond (2001): Nationwide study of haemolytic uraemic syndrome: clinical, microbiological, and epidemiological features. Arch. Dis. Child. 85, 125-131.
23. Ethelberg S., K. E. Olsen, F. Scheutz, C. Jensen, P. Schiellerup, J. Enberg, A. M. Petersen, B. Olesen, P. Gerner-Smidt, K. Molbak (2004): Virulence factors for hemolytic uremic syndrome, Denmark. Emerg. Infect. Dis. 10, 842-847.
24. Feng P., K. A. Lampel, H. Karch, T. S. Whittam (1998): Genotypic and phenotypic changes in the emergence of Escherichia coli O157:H7. J. Infect. Dis. 177, 1750-1753.
25. Friedrich A. W., M. Bielaszewska, W.-L. Zhang, M. Pulz, T. Kuczius, A. Ammon, H. Karch (2002): Escherichia coli harboring Shiga toxin 2 gene variants: frequency and association with clinical symptoms. J. Infect. Dis. 185, 74-84.
26. Friedrich A.W., J. Borell, M. Bielaszewska, A. Fruth, H. Tschäpe, H. Karch (2003): Shiga toxin 1c-producing Escherichia coli strains: Phenotypic and genetic characterization and association with human disease. J. Clin. Microbiol. 41, 2448-2453.
27. Friedrich A.W., R. Lukas, A. Mellmann, R. Köck, W. Zhang, W. Mathys, M. Bielaszewska, H. Karch (2006): Urease genes in non-O157 Shiga toxin-producing Escherichia coli: mostly silent but valuable markers for pathogenicity. Clin. Microbiol. Infect. 12, 483-486.
28. Gerber A., H. Karch, F. Allerberger, H.M. Verweyen, L.B. Zimmerhackl (2002): Clinical course and the role of Shiga toxin-producing Escherichia coli infection in the hemolytic-uremic syndrome in pediatric patients, 1997-2000, in Germany and Austria: A prospective study. J. Infect. Dis. 186, 493-500.
29. Geue L., M. Segura-Alvarez, F.J. Conraths, T. Kuczius, J. Bockemühl, H. Karch, P. Gallien (2002): A long-term study on the prevalence of Shiga toxin-producing Escherichia coli (STEC) on four German cattle farms. Epidemiol. Infect. 129, 173-185.
30. Gilmour M. W., T. Cote, J. Munro, L. Chui, J. Wylie, J. Isaac-Renton, G. Horsman, D. M. Tracz, A. Andrysiak, L. K. Ng (2005): Multilocus sequence typing of Escherichia coli O26:H11 isolates carrying stx in Canada does not identify genetic diversity. J. Clin. Microbiol. 43, 5319-5323.
31. Herold S., H. Karch, H. Schmidt (2004): Shiga toxin-encoding bacteriophages - genomes in motion. Int. J. Med. Microbiol. 294, 115-121.
32. Hiramatsu R., M. Matsumoto, Y. Miwa, Y. Suzuki, M. Saito, Y. Miyazaki (2002): Characterization of Shiga toxin-producing Escherichia coli O26 strains and establishment of selective isolation media for these strains. J. Clin. Microbiol. 40, 922-925.
33. Hornitzky M. A., K. Mercieca, K. A. Bettelheim, S. P. Djordjevic (2005): Bovine feces from animals with gastrointestinal infections are a source of serologically diverse atypical enteropathogenic Escherichia coli and Shiga toxin-producing E. coli strains that commonly possess intimin. Appl. Environ. Microbiol. 71, 3405-3412.
34. Hoshina K., A. Itagaki, R. Seki, K. Yamamoto, S. Masuda, T. Muku, N. Okada (2001): Enterohemorrhagic Escherichia coli O26 outbreak caused by contaminated natural water supplied by facility owned by local community. Jpn. J. Infect. Dis. 54, 247-248.
35. -. Int. J. Med. Microbiol. 292; 207-214.
36. Jelacic J. K., T. Damrow, G. S. Chen, S. Jelacic, M. Bielaszewska, M. Ciol, H. M. Carvalho, A. R. Melton-Celsa, A. D. O'Brien, P. I. Tarr (2003): Shiga toxin-producing Escherichia coli in Montana: bacterial genotypes and clinical profiles. J. Infect. Dis. 188, 719-729.
37. Jenkins C., M. C. Pearce, A. W. Smith, H. I. Knight, D. J. Shaw, T. Cheasty, G. Foster, G. J. Gunn, G. Dougan, H. R. Smith, G. Frankel (2003): Detection of Escherichia coli serogroups O26, O103, O111 and O145 from bovine faeces using immunomagnetic separation and PCR/DNA probe techniques. Lett. Appl. Microbiol. 37, 207-212.
38. Kaper J. B., J. P. Nataro, H. L. Mobley (2004): Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2, 123-140.
39. Karch H., S. Schubert, D. Zhang, W. Zhang, H. Schmidt, T. Ölschläger, J. Hacker (1999): A genomic island, termed high pathogenicity island, is present in certain non-O157 Shiga toxin-producing Escherichia coli clonal lineages. Infect. Immun. 67, 5994-6001.
40. Karch H., P. I. Tarr, M. Bielaszewska (2005): Enterohaemorrhagic Escherichia coli in human medicine. Int. J. Med. Microbiol., 295, 405-418.
41. Karch H., A. W. Friedrich, A. Gerber, L. B. Zimmerhackl, M. A. Schmidt, M. Bielaszewska (2006): New aspects in the pathogenesis of enteropathic hemolytic uremic syndrome. Semin. Thromb. Hemost. 32, 105-112.
42. Karmali M. A., B. T. Steele, M. Petric, C. Lim (1983): Sporadic cases of haemolytic-uraemic syndrome associated with faecal cytotoxin and cytotoxin-producing Escherichia coli in stools. Lancet 1, 619-620.
43. Karmali, M. A., M. Petric, C. Lim, P. C. Fleming, G. S. Arbus, H. Lior (1985): The association between idiopathic hemolytic uremic syndrome and infection by verotoxin-producing Escherichia coli. J. Infect. Dis. 151, 775-782.
44. Karmali, M. A., M. Mascarenhas, S. Shen, K. Ziebell, S. Johnson, R. Reid-Smith, J. Isaac-Renton, C. Clark, K. Rahn, J. B. Kaper (2003): Association of genomic O island 122 of Escherichia coli EDL 933 with verocytotoxin-producing Escherichia coli seropathotypes that are linked to epidemic and/or serious disease. J. Clin. Microbiol. 41, 4930-4940.
45. Kijima-Tanaka M., K. Ishihara, A. Kojima, A. Morioka, R. Nagata, M. Kawanishi, M. Nakazawa, Y. Tamura, T. Takahashi (2005): A national surveillance of Shiga toxin-producing Escherichia coli in food-producing animals in Japan. J. Vet. Med. B. Infect. Dis. Vet. Public Health 52, 230-237.
46. Klapproth J. M., I. C. Scaletsky, B. P. McNamara, L. C. Lai, C. Malstrom, S. P. James, M. S. Donnenberg (2000): A large toxin from pathogenic Escherichia coli strains that inhibits lymphocyte activation. Infect. Immun. 68, 2148-2155.
47. Konowalchuk J., J. I. Speirs, S. Stavric (1977): Vero response to a cytotoxin of Escherichia coli. Infect. Immun. 18, 775-779.
48. Kuczius T., M. Bielaszewska, A. W. Friedrich, W. Zhang (2004): A rapid method for the discrimination of genes encoding classical Shiga toxin (Stx) 1 and its variants, Stx1c and Stx1d, in Escherichia coli. Mol. Nutr. Food Res. 48, 515-521.
49. Levine M. M., R. Edelmann (1984): Enteropathogenic Escherichia coli of classic serotypes associated with infantile diarrhea: Epidemiology and pathogenesis. Epidemiol. Rev. 8, 31-51.
50. Levine M. M., J. G. Xu, J. B. Kaper, H. Lior, V. Prado, B. Tall, J. Nataro, H. Karch, K. Wachsmuth (1987): A DNA probe to identify enterohemorrhagic Escherichia coli of O157:H7 and other serotypes that cause hemorrhagic colitis and hemolytic uremic syndrome. J. Infect. Dis. 156, 175-182.
51. McDaniel T. K., K. G. Jarvis, M. S. Donnenberg, J. B. Kaper (1995): A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc. Natl. Acad. Sci. USA 92, 1664-1668.
52. McDaniel T. K., J. B. Kaper (1997): A cloned pathogenicity island from enteropathogenic Escherichia coli confers the attaching and effacing phenotype on E. coli K-12. Mol. Microbiol. 23, 399-107
53. McMaster C., E. A. Roch, G. A. Willshaw, A. Doherty, W. Kinnear, T. Cheasty (2001): Verocytotoxin-producing Escherichia coli serotype O26:H11 outbreak in an Irish creche. Eur. J. Clin. Microbiol. Infect. Dis. 20, 430-432.
54. Mellmann A., M. Bielaszewska, L. B. Zimmerhackl, R. Prager, D. Harmsen, H. Tschäpe, H. Karch (2005): Enterohemorrhagic Escherichia coli during human infection: in vivo evolution of a bacterial pathogen. Clin. Infect. Dis. 41, 785-792.
55. Misselwitz J., H. Karch, M. Bielazewska, U. John, F. Ringelmann, G. Ronnefarth, L. Patzer (2003): Cluster of hemolytic-uremic syndrome caused by Shiga toxin-producing Escherichia coli O26:H11. Pediatr. Infect. Dis. J. 22, 349-354.
56. Muniesa M., M.A. Schembri, N. Hauf, T. Chakraborty (2006): Active genetic elements present in the locus of enterocyte effacement in Escherichia coli O26 and their role in mobility. Infect. Immun. 74, 4190-1199.
57. Nicholls L., T. H. Grant, R. M. Robins-Browne (2000): Identification of a novel genetic locus that is required for in vitro adhesion of a clinical isolate of enterohaemorrhagic Escherichia coli to epithelial cells. Mol. Microbiol. 35, 275-288.
58. Orth D., R. Würzner (2006): What makes an enterohemorrhagic Escherichia coli? Clin. Infect. Dis. 43, 1168-1169.
59. Orth D., K. Grif, M. P. Dierich, R. Würzner (2006): Prevalence, structure and expression of urease genes in Shiga toxin-producing Escherichia coli from humans and the environment. Int. J. Hyg. Environ. Health 209, 513-520.
60. Perna N. T., G. F. Mayhew, G. Posfai, S. Elliott, M. S. Donnenberg, J. B. Kaper, F. R. Blattner (1998): Molecular evolution of a pathogenicity island from enterohemorrhagic Escherichia coli O157:H7. Infect. Immun. 66, 3810-3817.
61. Perna N. T., G. Plunkett, V. Burland, B. Mau, J. D. Glasner, D. J. Rose, G. F. Mayhew, P. S. Evans, J. Gregor, H. A. Kirkpatrick, G. Posfai, J. Hackett, S. Klink, A. Boutin, Y. Shao, L. Miller, E. J. Grotbeck, N. W. Davis, A. Lim, E. T. Dimalanta, K. D. Potamousis, J. Apodaca, T. S. Anantharaman, J. Lin, G. Yen, D. C. Schwartz, R. A. Welch, F. R. Blattner (2001): Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409, 529-533.
62. - in Germany. Infect. Genet. Evol. 1, 265-275.
63. Reid S. D., C. J. Herbelin, A. C. Bumbaugh, R. K. Selander, T. S. Whittam (2000): Parallel evolution of virulence in pathogenic Escherichia coli. Nature 406, 64-67.
64. Rivas M., E. Miliwebsky, I. Chinen, C. D. Roldan, L. Balbi, B. Garcia, G. Fiorilli, S. Sosa-Estani, J. Kincaid, J. Rangel, P. M. Griffin (2006): The Case-Control Study Group. Characterization and epidemiologic subtyping of Shiga toxin-producing Escherichia coli strains isolated from hemolytic uremic syndrome and diarrhea cases in Argentina. Foodborne Pathog. Dis. 3, 88-96.
65. Rumer L., J. Jores, P. Kirsch, Y. Cavignac, K. Zehmke, L. H. Wieler (2003): Dissemination of pheU- and pheV-located genomic islands among enteropathogenic (EPEC) and enterohemorrhagic (EHEC) E. coli and their possible role in the horizontal transfer of the locus of enterocyte effacement (LEE). Int. J. Med. Microbiol. 292, 463-475.
66. Schmidt H., L. Beutin, H. Karch (1995): Molecular analysis of the plasmid-encoded hemolysin of Escherichia coli O157:H7 strain EDL 933. Infect. Immun. 63, 1055-1061.
67. Schmidt H., C. Kernbach, H. Karch (1996): Analysis of the EHEC hly operon and its location in the physical map of the large plasmid of enterohaemorrhagic Escherichia coli O157:H7. Microbiology 142, 907-914.
68. Schmidt H., C. Geitz, P. I. Tarr, M. Frosch, H. Karch (1999): Non-O157 pathogenic Shiga toxin-producing Escherichia coli: Phenotypic and genetic profiling of virulence traits and evidence for clonality. J. Infect. Dis. 179, 115-123.
69. Smith H.W., P. Green, Z. Parsell (1983): Vero cell toxins in Escherichia coli and related bacteria: transfer by phage and conjugation and toxic action in laboratory animals, chickens and pigs. J. Gen. Microbiol. 129, 3121-3137.
70. Sonntag A.-K., R. Prager, M. Bielaszewska, W. Zhang, A. Fruth, H. Tschäpe, H. Karch (2004): Phenotypic and genotypic analyses of enterohemorrhagic Escherichia coli O145 strains from patients in Germany. J. Clin. Microbiol. 42, 954-962.
71. Sonntag A. K., M. Bielaszewska, A. Mellmann, N. Dierksen, P. Schierack, L. H. Wieler, M. A. Schmidt, H. Karch (2005a): Shiga toxin 2e-producing Escherichia coli isolates from humans and pigs differ in their virulence profiles and interactions with intestinal epithelial cells. Appl. Environ. Microbiol. 71, 8855-8863.
72. Sonntag A. K., E. Zenner, H. Karch, M. Bielaszewska (2005b): Pigeons as a possible reservoir of Shiga toxin 2f-producing Escherichia coli pathogenic to humans. Berl. Munch. Tierarztl. Wochenschr. 118, 464-470.
73. Stevens M. P., P. M. van Diemen, G. Frankel, A. D. Phillips, T. S. Wallis (2002): Efa1 influences colonization of the bovine intestine by Shiga-toxin producing Escherichia coli serotypes O5 and O111. Infect. Immun., 5158-5166.
74. Tarr P .I., C. A. Gordon, W. L. Chandler (2005): Shiga toxin-producing Escherichia coli and the haemolytic uraemic syndrome. Lancet 365, 1073-1086.
75. Tozzi E., A. Caprioli, F. Minelli, A. Gianviti, L. De Petris, A. Edefonti, G. Montini, A. Ferretti, T. De Palo, M. Gaido, G. Rizzoni, Hemolytic Uremic Syndrome Study Group (2003): Shiga toxin-producing Escherichia coli infections associated with hemolytic uremic syndrome in Italy 1988-2000. Emerg. Infect. Dis. 9, 106-108.
76. Vali L., A. Hamouda, D. V. Hoyle, M. C. Pearce, L. H. Whitaker, C. Jenkins, H. I. Knight, A. W. Smith, S. G. Amyes (2007): Antibiotic resistance and molecular epidemiology of Escherichia coli O26, O103 and O145 shed by two cohorts of Scottish beef cattle. J. Antimicrob. Chemother. doi:10.1093/jac/dk1491.
77. - genes required for intestinal colonization in calves. Infect. Immun. 73, 1735-1743.
78. Vaz T. M.I., K. Irino, M. A. M. F. Kato, A. M. G. Dias, T. A. T. Gomes, M. I. C. Medeiros, M. M. M. Rocha, B. E. C. Guth (2004): Virulence properties and characteristics of Shiga toxin-producing Escherichia coli in Sao Paulo, Brazil, from 1976 through 1999. J. Clin. Microbiol. 42, 903-905.
79. Watanabe H., J. Terajima, H. Izumiya, A. Wada, K. Tamura (1999): Molecular analysis of enterohemorrhagic Escherichia coli isolates in Japan and its application to epidemiological investigation. Pediatr. Int. 41, 202-208.
80. Wells J. G., L. D. Shipman, K. D. Greene, E. G. Sowers, J. H. Green, D. N. Cameron, F. P. Downes, M. L. Martin, P .M. Griffin, S.M. Ostroff (1991): Isolation of Escherichia coli serotype O157:H7 and other Shiga-like-toxin-producing E. coli from dairy cattle. J. Clin. Microbiol., 985-989.
81. Werber D., A. Fruth, A. Liesegang, M. Littmann, U. Buchholz, R. Prager, H. Karch, T. Breuer, H. Tschäpe, A. Ammon (2002): A multistate outbreak of Shiga toxin-producing Escherichia coli O26:H11 infections in Germany, detected by molecular subtyping surveillance, J. Infect. Dis. 186, 419-422.
82. Whittam T. S., M. L. Wolfe, I. K. Wachsmuth, F. Orskov, I. Orskov, R. Wilson (1993): Clonal relationships among Escherichia coli strains that cause hemorrhagic colitis and infantile diarrhea. Infect. Immun. 61, 1619-1629.
83. Wickham M., C. Lupp, M. Mascarenhas, A. Vazquez, B.K. Coombes, N.F. Brown, B.A. Coburn, W. Deng, J.L. Puento, M.A. Karmali, B.B. Finlay (2006): Bacterial genetic determinants of non-O157 STEC outbreaks and hemolytic uremic syndrome after infection. J. Infect. Dis. 194, 819-827.
84. Wieler L. H., M. Tigges, F. Ebel, S. Schäferkordt, S. Djafari, T. Schlapp, G. Baljer, T. Chakraborty (1996a): The enterohemolysin phenotype of Shiga-like toxin-producing Escherichia coli (SLTEC) is encoded by the EHEC-hemolysin gene. Vet. Microbiol. 52, 153-164.
85. Wieler L. H., E. Vieler, C. Erpenstein, T. Schlapp, H. Steinrück, R. Bauerfeind, A. Byomi, G. Baljer (1996b): Shiga toxin-producing Escherichia coli strains from bovines: association of adhesion with carriage of eae and other genes. J. Clin. Microbiol. 34, 2980-2984.
86. Wieler L. H., T. K. McDaniel, T. S. Whittam, J. B. Kaper (1997): Insertion site of the locus of enterocyte effacement in enteropathogenic and enterohemorrhagic Escherichia coli differs in relation to the clonal phytogeny of the strains. FEMS Microbiol. Lett. 156, 49-53.
87. Wirth T., D. Falush, R. Lan, F. Colles, P. Mensa, L. H. Wieler, H. Karch, P. R. Reeves, M. C. Maiden, H. Ochman, M. Achtman (2006): Sex and virulence in Escherichia coli: an evolutionary perspective. Mol. Microbiol. 60, 1136-1151.
88. Zhang W.-L., M. Bielaszewska, A. Liesegang, H. Tschäpe, H. Schmidt, M. Bitzan, H. Karch (2000a): Molecular characteristics and epidemiological significance of Shiga toxin-producing Escherichia coli O26. J. Clin. Microbiol. 38, 2134-2140.
89. Zhang, W.-L., M. Bielaszewska, J. Bockemühl, H. Schmidt, F. Scheutz, H. Karch (2000b): Molecular analysis of H antigens reveals that human diarrheagenic Escherichia coli O26 strains that carry the eae gene belong to the H11 clonal complex. J. Clin. Microbiol. 38, 2989-2933.
90. Zhang W., M. Bielaszewska, A. W. Friedrich, T. Kuczius, H. Karch (2005): Transcriptional analysis of genes encoding Shiga toxin 2 and its variants in Escherichia coli. Appl. Environ. Microbiol. 71, 558-561.
91. Zhang W., A. Mellmann, A.-K. Sonntag, L. Wieler, M. Bielaszewska, H. Tschape, H. Karch, A.W. Friedrich (2007): Structural and functional differences between disease-associated genes of enterohaemorrhagic Escherichia coli O111. Int. J. Med. Microbiol. 297, 17-26.