Semin Thromb Hemost 2010; 36(6): 586-593
DOI: 10.1055/s-0030-1262880
© Thieme Medical Publishers

Enterohemorrhagic Escherichia coli O26:H11–Associated Hemolytic Uremic Syndrome: Bacteriology and Clinical Presentation

Lothar-Bernd Zimmerhackl1 , Alejandra Rosales1 , Johannes Hofer1 , Magdalena Riedl1 , Therese Jungraithmayr1 , Alexander Mellmann2 , Martina Bielaszewska2 , Helge Karch2
  • 1Department of Pediatrics, Medical University of Innsbruck, Innsbruck, Austria
  • 2Institute of Hygiene, University of Münster, Münster, Germany
Further Information

Publication History

Publication Date:
23 September 2010 (online)

ABSTRACT

Infection by enterohemorrhagic Escherichia coli (EHEC) is the most frequent cause of hemolytic uremic syndrome (HUS) in childhood. During a 6-year period, all patients with the clinical diagnosis of HUS were registered in a prospective multicenter study in Austria and Germany. EHEC O26:H11 was the second most frequent detected serotype, accounting for 15.4% of all EHEC isolates. The presence of EHEC O26:H11 was significantly associated with young age at the disease onset (p < 0.001). Patients infected with this serotype were not different in their clinical presentation than those infected with other serotypes. This study underlines the importance of EHEC serotypes other than O157 in the etiology of HUS and emphasizes the importance of implementation of appropriate diagnostic methods to identify the whole spectrum of EHEC associated with HUS.

REFERENCES

  • 1 Siegler R L. The hemolytic uremic syndrome.  Pediatr Clin North Am. 1995;  42(6) 1505-1529
  • 2 Karmali M A, Steele B T, Petric M, Lim C. Sporadic cases of haemolytic-uraemic syndrome associated with faecal cytotoxin and cytotoxin-producing Escherichia coli in stools.  Lancet. 1983;  1(8325) 619-620
  • 3 Levine M M, Xu J G, Kaper J B et al. 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. 1987;  156(1) 175-182
  • 4 Chandler W L, Jelacic S, Boster D R et al. Prothrombotic coagulation abnormalities preceding the hemolytic-uremic syndrome.  N Engl J Med. 2002;  346(1) 23-32
  • 5 Bell B P, Goldoft M, Griffin P M et al. A multistate outbreak of Escherichia coli O157:H7-associated bloody diarrhea and hemolytic uremic syndrome from hamburgers. The Washington experience.  JAMA. 1994;  272(17) 1349-1353
  • 6 Brandt J, Wong C, Mihm S et al. Invasive pneumococcal disease and hemolytic uremic syndrome.  Pediatrics. 2002;  110(2 Pt 1) 371-376
  • 7 Loirat C, Noris M, Frémeaux-Bacchi V. Complement and the atypical hemolytic uremic syndrome in children.  Pediatr Nephrol. 2008;  23(11) 1957-1972
  • 8 Noris M, Remuzzi G. Atypical hemolytic-uremic syndrome.  N Engl J Med. 2009;  361(17) 1676-1687
  • 9 Zimmerhackl L B. Epidemiology, pathogenesis and therapeutic modalities in hemolytic-uremic syndrome.  Kidney Blood Press Res. 1998;  21(2–4) 290-292
  • 10 Banatvala N, Griffin P M, Greene K D Hemolytic Uremic Syndrome Study Collaborators et al. The United States National Prospective Hemolytic Uremic Syndrome Study: microbiologic, serologic, clinical, and epidemiologic findings.  J Infect Dis. 2001;  183(7) 1063-1070
  • 11 Ethelberg S, Smith B, Torpdahl M et al. Outbreak of non-O157 Shiga toxin-producing Escherichia coli infection from consumption of beef sausage.  Clin Infect Dis. 2009;  48(8) e78-e81
  • 12 Werber D, Behnke S C, Fruth A et al. Shiga toxin-producing Escherichia coli infection in Germany: different risk factors for different age groups.  Am J Epidemiol. 2007;  165(4) 425-434
  • 13 Banatvala N, Debeukelaer M M, Griffin P M et al. Shiga-like toxin-producing Escherichia coli O111 and associated hemolytic-uremic syndrome: a family outbreak.  Pediatr Infect Dis J. 1996;  15(11) 1008-1011
  • 14 Brooks J T, Bergmire-Sweat D, Kennedy M et al. Outbreak of Shiga toxin-producing Escherichia coli O111:H8 infections among attendees of a high school cheerleading camp.  Clin Infect Dis. 2004;  38(2) 190-198
  • 15 Caprioli A, Luzzi I, Rosmini F et al. Community-wide outbreak of hemolytic-uremic syndrome associated with non-O157 verocytotoxin-producing Escherichia coli .  J Infect Dis. 1994;  169(1) 208-211
  • 16 Elliott E J, Robins-Browne R M, O'Loughlin E V Contributors to the Australian Paediatric Surveillance Unit et al. Nationwide study of haemolytic uraemic syndrome: clinical, microbiological, and epidemiological features.  Arch Dis Child. 2001;  85(2) 125-131
  • 17 Fey P D, Wickert R S, Rupp M E, Safranek T J, Hinrichs S H. Prevalence of non-O157:H7 shiga toxin-producing Escherichia coli in diarrheal stool samples from Nebraska.  Emerg Infect Dis. 2000;  6(5) 530-533
  • 18 Werber D, Fruth A, Liesegang A et al. A multistate outbreak of Shiga toxin-producing Escherichia coli O26:H11 infections in Germany, detected by molecular subtyping surveillance.  J Infect Dis. 2002;  186(3) 419-422
  • 19 Karch H, Tarr P I, Bielaszewska M. Enterohaemorrhagic Escherichia coli in human medicine.  Int J Med Microbiol. 2005;  295(6-7) 405-418
  • 20 Jenkins C, Evans J, Chart H, Willshaw G A, Frankel G. Escherichia coli serogroup O26—a new look at an old adversary.  J Appl Microbiol. 2008;  104(1) 14-25
  • 21 Tozzi A E, Caprioli A, Minelli F Hemolytic Uremic Syndrome Study Group et al. Shiga toxin-producing Escherichia coli infections associated with hemolytic uremic syndrome, Italy, 1988–2000.  Emerg Infect Dis. 2003;  9(1) 106-108
  • 22 Brooks J T, Sowers E G, Wells J G et al. Non-O157 Shiga toxin-producing Escherichia coli infections in the United States, 1983–2002.  J Infect Dis. 2005;  192(8) 1422-1429
  • 23 Hedican E B, Medus C, Besser J M et al. Characteristics of O157 versus non-O157 Shiga toxin-producing Escherichia coli infections in Minnesota, 2000–2006.  Clin Infect Dis. 2009;  49(3) 358-364
  • 24 Jelacic J K, Damrow T, Chen G S et al. Shiga toxin-producing Escherichia coli in Montana: bacterial genotypes and clinical profiles.  J Infect Dis. 2003;  188(5) 719-729
  • 25 Rivas M, Miliwebsky E, Chinen I Case-Control Study Group et al. Characterization and epidemiologic subtyping of Shiga toxin-producing Escherichia coli strains isolated from hemolytic uremic syndrome and diarrhea cases in Argentina.  Foodborne Pathog Dis. 2006;  3(1) 88-96
  • 26 Rivero M A, Passucci J A, Rodriguez E M, Parma A E. Role and clinical course of verotoxigenic Escherichia coli infections in childhood acute diarrhea in Argentina.  J Med Microbiol. 2010;  59 345-352
  • 27 Hoshina K, Itagaki A, Seki R et al. Enterohemorrhagic Escherichia coli O26 outbreak caused by contaminated natural water supplied by facility owned by local community.  Jpn J Infect Dis. 2001;  54(6) 247-248
  • 28 Bielaszewska M, Köck R, Friedrich A W et al. Shiga toxin-mediated hemolytic uremic syndrome: time to change the diagnostic paradigm?.  PLoS One. 2007;  2(10) e1024
  • 29 Gerber A, Karch H, Allerberger F, Verweyen H M, Zimmerhackl L B. 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. 2002;  186(4) 493-500
  • 30 Mellmann A, Bielaszewska M, Köck R et al. Analysis of collection of hemolytic uremic syndrome-associated enterohemorrhagic Escherichia coli .  Emerg Infect Dis. 2008;  14(8) 1287-1290
  • 31 McMaster C, Roch E A, Willshaw G A, Doherty A, Kinnear W, Cheasty T. Verocytotoxin-producing Escherichia coli serotype O26:H11 outbreak in an Irish crèche.  Eur J Clin Microbiol Infect Dis. 2001;  20(6) 430-432
  • 32 Misselwitz J, Karch H, Bielazewska M et al. Cluster of hemolytic-uremic syndrome caused by Shiga toxin-producing Escherichia coli O26:H11.  Pediatr Infect Dis J. 2003;  22(4) 349-354
  • 33 Sonoda C, Tagami A, Nagatomo D et al. An enterohemorrhagic Escherichia coli O26 outbreak at a nursery school in Miyazaki, Japan.  Jpn J Infect Dis. 2008;  61(1) 92-93
  • 34 Allerberger F, Friedrich A W, Grif K et al. Hemolytic-uremic syndrome associated with enterohemorrhagic Escherichia coli O26:H infection and consumption of unpasteurized cow's milk.  Int J Infect Dis. 2003;  7(1) 42-45
  • 35 Bielaszewska M, Zhang W, Tarr P I, Sonntag A K, Karch H. 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. 2005;  43(8) 4225-4228
  • 36 Friedrich A W, Bielaszewska M, Zhang W L et al. Escherichia coli harboring Shiga toxin 2 gene variants: frequency and association with clinical symptoms.  J Infect Dis. 2002;  185(1) 74-84
  • 37 Bitzan M, Moebius E, Ludwig K, Müller-Wiefel D E, Heesemann J, Karch H. High incidence of serum antibodies to Escherichia coli O157 lipopolysaccharide in children with hemolytic-uremic syndrome.  J Pediatr. 1991;  119(3) 380-385
  • 38 Espié E, Grimont F, Mariani-Kurkdjian P et al. Surveillance of hemolytic uremic syndrome in children less than 15 years of age, a system to monitor O157 and non-O157 Shiga toxin-producing Escherichia coli infections in France, 1996–2006.  Pediatr Infect Dis J. 2008;  27(7) 595-601
  • 39 Caprioli A, Tozzi A E, Rizzoni G, Karch H. Non-O157 Shiga toxin-producing Escherichia coli infections in Europe.  Emerg Infect Dis. 1997;  3(4) 578-579
  • 40 Loirat C, Sonsino E, Varga Moreno A et al. Hemolytic-uremic syndrome: an analysis of the natural history and prognostic features.  Acta Paediatr Scand. 1984;  73(4) 505-514
  • 41 Siegler R L, Milligan M K, Burningham T H, Christofferson R D, Chang S Y, Jorde L B. Long-term outcome and prognostic indicators in the hemolytic-uremic syndrome.  J Pediatr. 1991;  118(2) 195-200
  • 42 Siegler R L, Pavia A T, Christofferson R D, Milligan M K. A 20-year population-based study of postdiarrheal hemolytic uremic syndrome in Utah.  Pediatrics. 1994;  94(1) 35-40
  • 43 Siegler R L, Pavia A T, Hansen F L, Christofferson R D, Cook J B. Atypical hemolytic-uremic syndrome: a comparison with postdiarrheal disease.  J Pediatr. 1996;  128(4) 505-511
  • 44 Tönshoff B, Sammet A, Sanden I, Mehls O, Waldherr R, Schärer K. Outcome and prognostic determinants in the hemolytic uremic syndrome of children.  Nephron. 1994;  68(1) 63-70
  • 45 Gianviti A, Tozzi A E, De Petris L et al. Risk factors for poor renal prognosis in children with hemolytic uremic syndrome.  Pediatr Nephrol. 2003;  18(12) 1229-1235
  • 46 Ogura Y, Ooka T, Iguchi A et al. Comparative genomics reveal the mechanism of the parallel evolution of O157 and non-O157 enterohemorrhagic Escherichia coli .  Proc Natl Acad Sci U S A. 2009;  106(42) 17939-17944
  • 47 Mellmann A, Bielaszewska M, Karch H. Intrahost genome alterations in enterohemorrhagic Escherichia coli .  Gastroenterology. 2009;  136(6) 1925-1938
  • 48 Zhang W, Mellmann A, Sonntag A K et al. Structural and functional differences between disease-associated genes of enterohaemorrhagic Escherichia coli O111.  Int J Med Microbiol. 2007;  297(1) 17-26
  • 49 Aldick T, Bielaszewska M, Zhang W et al. Hemolysin from Shiga toxin-negative Escherichia coli O26 strains injures microvascular endothelium.  Microbes Infect. 2007;  9(3) 282-290
  • 50 Aldick T, Bielaszewska M, Uhlin B E, Humpf H U, Wai S N, Karch H. Vesicular stabilization and activity augmentation of enterohaemorrhagic Escherichia coli haemolysin.  Mol Microbiol. 2009;  71(6) 1496-1508
  • 51 Brockmeyer J, Bielaszewska M, Fruth A et al. Subtypes of the plasmid-encoded serine protease EspP in Shiga toxin-producing Escherichia coli: distribution, secretion, and proteolytic activity.  Appl Environ Microbiol. 2007;  73(20) 6351-6359
  • 52 Tarr P I, Bilge S S, Vary Jr J C et al. Iha: a novel Escherichia coli O157:H7 adherence-conferring molecule encoded on a recently acquired chromosomal island of conserved structure.  Infect Immun. 2000;  68(3) 1400-1407
  • 53 Toma C, Martínez Espinosa E, Song T et al. Distribution of putative adhesins in different seropathotypes of Shiga toxin-producing Escherichia coli .  J Clin Microbiol. 2004;  42(11) 4937-4946
  • 54 Bielaszewska M, Sonntag A K, Schmidt M A, Karch H. Presence of virulence and fitness gene modules of enterohemorrhagic Escherichia coli in atypical enteropathogenic Escherichia coli O26.  Microbes Infect. 2007;  9(7) 891-897
  • 55 Karch H, Schubert S, Zhang D et al. A genomic island, termed high-pathogenicity island, is present in certain non-O157 Shiga toxin-producing Escherichia coli clonal lineages.  Infect Immun. 1999;  67(11) 5994-6001
  • 56 Orth D, Grif K, Dierich M P, Würzner R. Variability in tellurite resistance and the ter gene cluster among Shiga toxin-producing Escherichia coli isolated from humans, animals and food.  Res Microbiol. 2007;  158(2) 105-111
  • 57 Mellmann A, Bielaszewska M, Zimmerhackl L B et al. Enterohemorrhagic Escherichia coli in human infection: in vivo evolution of a bacterial pathogen.  Clin Infect Dis. 2005;  41(6) 785-792
  • 58 Bielaszewska M, Middendorf B, Köck R et al. Shiga toxin-negative attaching and effacing Escherichia coli: distinct clinical associations with bacterial phylogeny and virulence traits and inferred in-host pathogen evolution.  Clin Infect Dis. 2008;  47(2) 208-217
  • 59 Bielaszewska M, Prager R, Köck R et al. Shiga toxin gene loss and transfer in vitro and in vivo during enterohemorrhagic Escherichia coli O26 infection in humans.  Appl Environ Microbiol. 2007;  73(10) 3144-3150
  • 60 Bielaszewska M, Prager R, Zhang W et al. Chromosomal dynamism in progeny of outbreak-related sorbitol-fermenting enterohemorrhagic Escherichia coli O157:NM.  Appl Environ Microbiol. 2006;  72(3) 1900-1909
  • 61 Mellmann A, Lu S, Karch H et al. Recycling of Shiga toxin 2 genes in sorbitol-fermenting enterohemorrhagic Escherichia coli O157:NM.  Appl Environ Microbiol. 2008;  74(1) 67-72

Lothar-Bernd ZimmerhacklM.D. Ph.D. 

Medical University of Innsbruck, Anichstrasse 35

6020 Innsbruck, Austria

Email: lothar-bernd.zimmerhackl@uki.at

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