Enterohemorrhagic Escherichia coli O26:H11/H-: a new virulent clone emerges in Europe.

BACKGROUND Enterohemorrhagic Escherichia coli (EHEC) O26 causes diarrhea and hemolytic uremic syndrome (HUS). Strains harboring the stx1a gene prevail, but strains with stx2a as the sole Shiga toxin-encoding gene are now emerging. The traits and virulence of the latter set of strains are unknown. We correlated stx genotypes of 272 EHEC O26 strains isolated in 7 European countries between 1996 and 2012 with disease phenotypes. We determined phylogeny, clonal structure, and plasmid gene profiles of the isolates and portray geographic and temporal distribution of the different subgroups. METHODS The stx genotypes and plasmid genes were identified using polymerase chain reaction, phylogeny was assigned using multilocus sequence typing, and clonal relatedness was established using pulsed-field gel electrophoresis. RESULTS Of the 272 EHEC O26 isolates, 107 (39.3%), 139 (51.1%), and 26 (9.6%) possessed stx1a, stx2a, or both genes, respectively. Strains harboring stx2a only were significantly associated with HUS (odds ratio, 14.2; 95% confidence interval, 7.9-25.6; P < .001) compared to other stx genotypes. The stx2a-harboring strains consist of 2 phylogenetically distinct groups defined by sequence type (ST) 21 and ST29. The ST29 strains are highly conserved and correspond by plasmid genes to the new virulent clone of EHEC O26 that emerged in Germany in the 1990s. This new clone occurred in 6 of the 7 countries and represented approximately 50% of all stx2a-harboring EHEC O26 strains isolated between 1996 and 2012. CONCLUSIONS A new highly virulent clone of EHEC O26 has emerged in Europe. Its reservoirs and sources warrant identification.

[1]  Stefano Morabito,et al.  Multicenter Evaluation of a Sequence-Based Protocol for Subtyping Shiga Toxins and Standardizing Stx Nomenclature , 2012, Journal of Clinical Microbiology.

[2]  Craig S. Wong,et al.  Risk factors for the hemolytic uremic syndrome in children infected with Escherichia coli O157:H7: a multivariable analysis. , 2012, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[3]  H. Karch,et al.  Need for long-term follow-up in enterohemorrhagic Escherichia coli-associated hemolytic uremic syndrome due to late-emerging sequelae. , 2012, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[4]  A. Caprioli,et al.  Pathogenic Potential to Humans of Bovine Escherichia coli O26, Scotland , 2012, Emerging infectious diseases.

[5]  J. Janda,et al.  Fatal case of diarrhea‐associated hemolytic uremic syndrome with severe neurologic involvement , 2012, Pediatrics international : official journal of the Japan Pediatric Society.

[6]  F. Scheutz,et al.  Incidence and Virulence Determinants of Verocytotoxin-Producing Escherichia coli Infections in the Brussels-Capital Region, Belgium, in 2008–2010 , 2012, Journal of Clinical Microbiology.

[7]  N. Ohashi,et al.  Serotype, Shiga toxin (Stx) type, and antimicrobial resistance of Stx-producing Escherichia coli isolated from humans in Shizuoka Prefecture, Japan (2003-2007). , 2012, Japanese journal of infectious diseases.

[8]  Valentina Rizzi,et al.  The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2010. , 2012, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[9]  Klaus Stark,et al.  Epidemic profile of Shiga-toxin-producing Escherichia coli O104:H4 outbreak in Germany. , 2011, The New England journal of medicine.

[10]  Craig S. Wong,et al.  Early volume expansion during diarrhea and relative nephroprotection during subsequent hemolytic uremic syndrome. , 2011, Archives of pediatrics & adolescent medicine.

[11]  T. Beattie,et al.  Highly Virulent Escherichia coli O26, Scotland , 2011, Emerging infectious diseases.

[12]  L. Beutin,et al.  Human Infections with Non-O157 Shiga Toxin–producing Escherichia coli, Switzerland, 2000–2009 , 2011, Emerging infectious diseases.

[13]  Efsa Journal,et al.  European Food Safety Authority, European Centre for Disease Prevention and Control; The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2009 , 2011 .

[14]  A. Mellmann,et al.  Enterohemorrhagic Escherichia coli O26:H11-Associated Hemolytic Uremic Syndrome: Bacteriology and Clinical Presentation. , 2010, Seminars in thrombosis and hemostasis.

[15]  F. Conraths,et al.  Analysis of the Clonal Relationship of Serotype O26:H11 Enterohemorrhagic Escherichia coli Isolates from Cattle , 2009, Applied and Environmental Microbiology.

[16]  J. Besser,et al.  Characteristics of O157 versus non-O157 Shiga toxin-producing Escherichia coli infections in Minnesota, 2000-2006. , 2009, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[17]  A. Mellmann,et al.  Intrahost genome alterations in enterohemorrhagic Escherichia coli. , 2009, Gastroenterology.

[18]  E. Nielsen,et al.  Outbreak of non-O157 Shiga toxin-producing Escherichia coli infection from consumption of beef sausage. , 2009, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[19]  A. Mellmann,et al.  Analysis of Collection of Hemolytic Uremic Syndrome–associated Enterohemorrhagic Escherichia coli , 2008, Emerging infectious diseases.

[20]  V. Vaillant,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 , 2008, The Pediatric infectious disease journal.

[21]  A. Mellmann,et al.  Shiga Toxin Gene Loss and Transfer In Vitro and In Vivo during Enterohemorrhagic Escherichia coli O26 Infection in Humans , 2007, Applied and Environmental Microbiology.

[22]  A. Friedrich,et al.  Shiga toxin activatable by intestinal mucus in Escherichia coli isolated from humans: predictor for a severe clinical outcome. , 2006, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[23]  B. Swaminathan,et al.  Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. , 2006, Foodborne pathogens and disease.

[24]  P. Griffin,et al.  Characterization and epidemiologic subtyping of Shiga toxin-producing Escherichia coli strains isolated from hemolytic uremic syndrome and diarrhea cases in Argentina. , 2006, Foodborne pathogens and disease.

[25]  J. Wells,et al.  Non-O157 Shiga toxin-producing Escherichia coli infections in the United States, 1983-2002. , 2005, The Journal of infectious diseases.

[26]  P. Tarr,et al.  Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome , 2005, The Lancet.

[27]  Steen Ethelberg,et al.  Virulence Factors for Hemolytic Uremic Syndrome, Denmark , 2004, Emerging infectious diseases.

[28]  J. Blanco,et al.  Serotypes, Virulence Genes, and Intimin Types ofShiga Toxin (Verotoxin)-Producing Escherichia coli Isolatesfrom Cattle in Spain and Identification of a New Intimin VariantGene(eae-ξ) , 2004, Journal of Clinical Microbiology.

[29]  R. Siegler Postdiarrheal Shiga toxin-mediated hemolytic uremic syndrome. , 2003, JAMA.

[30]  Gilbert S Chen,et al.  Shiga toxin-producing Escherichia coli in Montana: bacterial genotypes and clinical profiles. , 2003, The Journal of infectious diseases.

[31]  A. Caprioli,et al.  Hemolytic-uremic syndrome associated with enterohemorrhagic Escherichia coli O26:H infection and consumption of unpasteurized cow's milk. , 2003, International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases.

[32]  A. Edefonti,et al.  Shiga Toxin–Producing Escherichia coli Infections Associated with Hemolytic Uremic Syndrome, Italy, 1988–2000 , 2003, Emerging infectious diseases.

[33]  H. Karch,et al.  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. , 2002, The Journal of infectious diseases.

[34]  E. Elliott,et al.  Nationwide study of haemolytic uraemic syndrome: clinical, microbiological, and epidemiological features , 2001, Archives of disease in childhood.

[35]  R. Gryko,et al.  Isolation of verotoxigenic strains of Escherichia coli O26 in Poland. , 2000, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[36]  H. Karch,et al.  Molecular characteristics and epidemiological significance of Shiga toxin-producing Escherichia coli O26 strains. , 2000, Journal of clinical microbiology.

[37]  Antimicrobial Susceptibility Testing ( Agar Disk Diffusion Method ) , 2022 .