Genotypes and virulence characteristics of Shiga toxin-producing Escherichia coli O104 strains from different origins and sources

International Journal of Medical Microbiology

Volumn 303, Issue 8, 2013, Pages 410-421

  Miko, Angelika ^a   Delannoy, Sabine ^b   Fach, Patrick ^b   Strockbine, Nancy A ^c   Lindstedt, Björn Arne ^d   Mariani Kurkdjian, Patricia ^e   Reetz, Jochen ^a   Beutin, Lothar ^a  

^a FEDERAL INSTITUTE FOR RISK ASSESSMENT   (Germany)

^b French Agency for Food   (France)

^c CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^d NORWEGIAN INSTITUTE OF PUBLIC HEALTH   (Norway)

^e HÔPITAL ROBERT DEBRÉ   (France)

Author keywords

Cell adhesion; E. coli O104; Enteroaggregative E. coli; Genotyping; PFGE; Real time PCR; Shiga toxins; Virulence

Indexed keywords

VEROTOXIN 1; VEROTOXIN 2;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; DIARRHEAGENIC ESCHERICHIA COLI; EHXA GENE; ENTEROAGGREGATIVE ESCHERICHIA COLI; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI; ESPP GENE; GENE EXPRESSION; GENETIC POLYMORPHISM; GENOTYPE; HUMAN; HUMAN CELL; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PULSED FIELD GEL ELECTROPHORESIS; SEROTYPE; SHIGA TOXIN PRODUCING ESCHERICHIA COLI;

CELL-ADHESION; E. COLI O104; ENTEROAGGREGATIVE E. COLI; GENOTYPING; PFGE; REAL TIME PCR; SHIGA-TOXINS; VIRULENCE;

ANIMALS; CLUSTER ANALYSIS; ELECTROPHORESIS, GEL, PULSED-FIELD; ENVIRONMENTAL MICROBIOLOGY; ESCHERICHIA COLI INFECTIONS; EUROPE; GENOTYPE; HUMANS; MOLECULAR TYPING; SEROTYPING; SHIGA-TOXIGENIC ESCHERICHIA COLI; UNITED STATES; VIRULENCE FACTORS;

EID: 84887615077     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2013.05.006     Document Type: Article

References (66)

1. Abu-Ali G.S., Ouellette L.M., Henderson S.T., Whittam T.S., Manning S.D. Differences in adherence and virulence gene expression between two outbreak strains of enterohaemorrhagic Escherichia coli O157:H7. Microbiology 2010, 156:408-419.
2. Adolphs J., Alt K., Bandick N., et al. EHEC Outbreak 2011: Investigation of the Outbreak Along the Food Chain 2012, 1-154. Federal Institute for Risk Assessment, Berlin, Germany, http://www.bfr.bund.de/cm/350/ehec-outbreak-2011-investigation-of-the-outbreak-along-the-food-chain.pdf. B. Appel, G. Fleur-Böl, M. Greiner, M. Lahrssen-Wiederholt, A. Hensel (Eds.).
3. Ahmed S.A., Awosika J., Baldwin C., Bishop-Lilly K.A., Biswas B., Broomall S., Chain P.S., Chertkov O., Chokoshvili O., Coyne S., Davenport K., Detter J.C., Dorman W., Erkkila T.H., Folster J.P., Frey K.G., George M., Gleasner C., Henry M., Hill K.K., Hubbard K., Insalaco J., Johnson S., Kitzmiller A., Krepps M., Lo C.C., Luu T., McNew L.A., Minogue T., Munk C.A., Osborne B., Patel M., Reitenga K.G., Rosenzweig C.N., Shea A., Shen X., Strockbine N., Tarr C., Teshima H., van G.E., Verratti K., Wolcott M., Xie G., Sozhamannan S., Gibbons H.S. Genomic comparison of Escherichia coli O104:H4 isolates from 2009 and 2011 reveals plasmid, and prophage heterogeneity, including shiga toxin encoding phage Stx2. PLoS ONE 2012, 7:e48228.
4. Alexander D.C., Hao W., Gilmour M.W., Zittermann S., Sarabia A., Melano R.G., Peralta A., Lombos M., Warren K., Amatnieks Y., Virey E., Ma J.H., Jamieson F.B., Low D.E., Allen V.G. Escherichia coli O104:H4 infections and international travel. Emerg. Infect. Dis. 2012, 18:473-476.
5. Beutin L., Hammerl J.A., Strauch E., Reetz J., Dieckmann R., Kelner-Burgos Y., Martin A., Miko A., Strockbine N.A., Lindstedt B.A., Horn D., Monse H., Huettel B., Muller I., Stuber K., Reinhardt R. Spread of a distinct Stx2-encoding phage prototype among E. coli O104:H4 strains from outbreaks in Germany, Norway and Georgia. J. Virol. 2012, 86(10444):55.
6. Beutin L., Marches O., Bettelheim K.A., Gleier K., Zimmermann S., Schmidt H., Oswald E. HEp-2 cell adherence, actin aggregation, and intimin types of attaching and effacing Escherichia coli strains isolated from healthy infants in Germany and Australia. Infect. Immun. 2003, 71:3995-4002.
7. Beutin L., Martin A. Outbreak of Shiga Toxin-Producing Escherichia coli (STEC) O104:H4 Infection in Germany Causes a Paradigm Shift with Regard to Human Pathogenicity of STEC Strains. J. Food Prot. 2012, 75:408-418.
8. Beutin L., Miko A., Krause G., Pries K., Haby S., Steege K., Albrecht N. Identification of human-pathogenic strains of Shiga toxin-producing Escherichia coli from food by a combination of serotyping and molecular typing of Shiga toxin genes. Appl. Environ. Microbiol. 2007, 73:4769-4775.
9. Beutin L., Zimmermann S., Gleier K. Rapid detection and isolation of Shiga-like toxin (verocytotoxin)-producing Escherichia coli by direct testing of individual enterohemolytic colonies from washed sheep blood agar plates in the VTEC-RPLA assay. J. Clin. Microbiol. 1996, 34:2812-2814.
10. Bielaszewska M., Mellmann A., Zhang W., Kock R., Fruth A., Bauwens A., Peters G., Karch H. Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany, 2011: a microbiological study. Lancet Infect. Dis. 2011, 11:671-676.
11. Blanco J., Blanco M., Blanco J., Mora A., Alonso M.P., Gonzalez E.A., Bernardez M.I. Epidemiology of Verocytotoxigenic Escherihcia coli (VTEC) in ruminants. Verocytotoxigenic E. coli 2001, 113-148. Food & Nutrition Press, Inc., Trumbull. G. Duffy, P. Garvey, D.A. McDowell (Eds.).
12. Brunder W., Schmidt H., Karch H. EspP, a novel extracellular serine protease of enterohaemorrhagic Escherichia coli O157:H7 cleaves human coagulation factor V. Mol. Microbiol. 1997, 24:767-778.
13. Brzuszkiewicz E., Thurmer A., Schuldes J., Leimbach A., Liesegang H., Meyer F.D., Boelter J., Petersen H., Gottschalk G., Daniel R. Genome sequence analyses of two isolates from the recent Escherichia coli outbreak in Germany reveal the emergence of a new pathotype: Entero-Aggregative-Haemorrhagic Escherichia coli (EAHEC). Arch. Microbiol. 2011, 193:883-891.
14. Bugarel M., Beutin L., Fach P. Low-density macroarray targeting non-locus of enterocyte effacement effectors (nle genes) and major virulence factors of Shiga toxin-producing Escherichia coli (STEC): a new approach for molecular risk assessment of STEC isolates. Appl. Environ. Microbiol. 2010, 76:203-211.
15. Bugarel M., Martin A., Fach P., Beutin L. Virulence gene profiling of enterohemorrhagic (EHEC) and enteropathogenic (EPEC) Escherichia coli strains: a basis for molecular risk assessment of typical and atypical EPEC strains. BMC Microbiol. 2011, 11:142.
16. Burland V., Shao Y., Perna N.T., Plunkett G., Sofia H.J., Blattner F.R. The complete DNA sequence and analysis of the large virulence plasmid of Escherichia coli O157:H7. Nucleic Acids Res. 1998, 26:4196-4204.
17. Cassar C.A., Ottaway M., Paiba G.A., Futter R., Newbould S., Woodward M.J. Absence of enteroaggregative Escherichia coli in farmed animals in Great Britain. Vet. Rec. 2004, 154:237-239.
18. CDC Outbreak of acute gastroenteritis attributable to Escherichia coli Serotype O104:H21 - Helena, Montana, 1994. MMWR 1995, 44:501-503.
19. CDC Investigation Update: Outbreak of Shiga toxin-producing E. coli O104 (STEC O104:H4) Infections Associated with Travel to Germany 2011, Centers for Disease Control Prevention, Atlanta, USA, http://www.cdc.gov/ecoli/2011/ecolio104/.
20. Chassaing B., Etienne-Mesmin L., Bonnet R., Darfeuille-Michaud A. Bile salts induce long polar fimbriae expression favouring Crohn's disease-associated adherent-invasive Escherichia coli interaction with Peyer's patches. Environ. Microbiol. 2012, 15:355-371.
21. Delannoy S., Beutin L., Burgos Y.K., Fach P. Specific detection of enteroaggregative hemorrhagic Escherichia coli O104:H4 strains using the CRISPR locus as target for a diagnostic real-time PCR. J. Clin. Microbiol. 2012, 50:3485-3492.
22. Delannoy S., Beutin L., Fach P. Use of clustered regularly interspaced short palindromic repeat sequence polymorphisms for specific detection of enterohemorrhagic Escherichia coli strains of serotypes O26:H11, O45:H2, O103:H2, O111:H8, O121:H19, O145:H28, and O157:H7 by real-time PCR. J. Clin. Microbiol. 2012, 50:4035-4040.
23. European Centre for Disease Prevention and Control, European Food Safety Authority, 2011. In: ECDC, EFSA (Eds.), Shiga Toxin/verotoxin-Producing Escherichia coli in Humans, Food and Animals in the EU/EEA, With Special Reference to the German Outbreak Strain STEC O104. http://www.ecdc.europa.eu/en/publications/Publications/1106_TER_EColi_joint_EFSA.pdf.
24. European Food Safety Authority Shiga toxin-producing E. coli (STEC) O104:H4 2011 outbreaks in Europe: taking stock. EFSA J. 2011, 9:2390.
25. Farfan M.J., Torres A.G. Molecular mechanisms that mediate colonization of Shiga toxin-producing Escherichia coli strains. Infect. Immun. 2012, 80:903-913.
26. Frank C., Werber D., Cramer J.P., Askar M., Faber M., Heiden M.A., Bernard H., Fruth A., Prager R., Spode A., Wadl M., Zoufaly A., Jordan S., Kemper M.J., Follin P., Müller L., King L.A., Rosner B., Bucholz U., Stark K., Krause G. Epidemic profile of shiga-toxin-producing Escherichia coli O104:H4 outbreak in Germany - preliminary report. N. Engl. J. Med. 2011, 365:1771-1780.
27. Gault G., Weill F., Mariani-Kurkdjian P., Jourdan-da S.N., King L., Aldabe B., Charron M., Ong N., Castor C., Mace M., Bingen E., Noel H., Vaillant V., Bone A., Vendrely B., Delmas Y., Combe C., Bercion R., d'Andigne E., Desjardin M., de V.H., Rolland P. Outbreak of haemolytic uraemic syndrome and bloody diarrhoea due to Escherichia coli O104:H4, south-west France, June 2011. Euro Surveill. 2011, 16.(26).
28. Germani Y., Soro B., Vohito M., Morel O., Morvan J. Enterohaemorrhagic Escherichia coli in Central African Republic. Lancet 1997, 349:1670.
29. Gerner-Smidt P., Scheutz F. Standardized pulsed-field gel electrophoresis of Shiga toxin-producing Escherichia coli: the PulseNet Europe Feasibility Study. Foodborne Pathog. Dis. 2006, 3:74-80.
30. Gilmour M.W., Olson A.B., Andrysiak A.K., Ng L.K., Chui L. Sequence-based typing of genetic targets encoded outside of the O-antigen gene cluster is indicative of Shiga toxin-producing Escherichia coli serogroup lineages. J. Med. Microbiol. 2007, 56:620-628.
31. Grad Y.H., Lipsitch M., Feldgarden M., Arachchi H.M., Cerqueira G.C., Fitzgerald M., Godfrey P., Haas B.J., Murphy C.I., Russ C., Sykes S., Walker B.J., Wortman J.R., Young S., Zeng Q., Abouelleil A., Bochicchio J., Chauvin S., Desmet T., Gujja S., McCowan C., Montmayeur A., Steelman S., Frimodt-Moller J., Petersen A.M., Struve C., Krogfelt K.A., Bingen E., Weill F.X., Lander E.S., Nusbaum C., Birren B.W., Hung D.T., Hanage W.P. Genomic epidemiology of the Escherichia coli O104:H4 outbreaks in Europe, 2011. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:3065-3070.
32. Hauri A., Gotsch U., Strotmann I., Krahn J., Bettge-Weller G., Westbrock H., Bellinger O., Uphoff H. Secondary transmissions during the outbreak of Shiga toxin-producing Escherichia coli O104 in Hesse, Germany, 2011. Euro Surveill. 2011, 16(31).
33. Hussein H.S. Prevalence and pathogenicity of Shiga toxin-producing Escherichia coli in beef cattle and their products. J. Anim. Sci. 2007, 85:E63-E72.
34. International Organization for Standardization Microbiology of food and animal feed - real-time polymerase chain reaction (PCR)-based method for the detection of food-borne pathogens - horizontal method for the detection of Shiga toxin-producing Escherichia coli (STEC) and the determination of O157, O111, O26, O103 and O145 serogroups 2012, 1-23. ISO, Geneva. ISO copyright office (Ed.).
35. Kaper J.B., Nataro J.P., Mobley H.L. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2004, 2:123-140.
36. Makino K., Ishii K., Yasunaga T., Hattori M., Yokoyama K., Yutsudo C.H., Kubota Y., Yamaichi Y., Iida T., Yamamoto K., Honda T., Han C.G., Ohtsubo E., Kasamatsu M., Hayashi T., Kuhara S., Shinagawa H. Complete nucleotide sequences of 93-kb and 3.3-kb plasmids of an enterohemorrhagic Escherichia coli O157:H7 derived from Sakai outbreak. DNA Res. 1998, 5:1-9.
37. Mariani-Kurkdjian P., Bingen E., Gault G., Jourdan-da S.N., Weill F. Escherichia coli O104:H4 south-west France, June 2011. Lancet 2011, 732-733.
38. Martin A., Beutin L. Characteristics of Shiga toxin-producing Escherichia coli from meat and milk products of different origins and association with food producing animals as main contamination sources. Int. J. Food Microbiol. 2011, 146:99-104.
39. Mellmann A., Bielaszewska M., Kock R., Friedrich A.W., Fruth A., Middendorf B., Harmsen D., Schmidt M.A., Karch H. Analysis of collection of hemolytic uremic syndrome-associated enterohemorrhagic Escherichia coli. Emerg. Infect. Dis. 2008, 14:1287-1290.
40. Mellmann A., Harmsen D., Cummings C.A., Zentz E.B., Leopold S.R., Rico A., Prior K., Szczepanowski R., Ji Y., Zhang W., McLaughlin S.F., Henkhaus J.K., Leopold B., Bielaszewska M., Prager R., Brzoska P.M., Moore R.L., Guenther S., Rothberg J.M., Karch H. Prospective genomic characterization of the German enterohemorrhagic Escherichia coli O104:H4 outbreak by rapid next generation sequencing technology. PLoS ONE 2011, 6:e22751.
41. Melton-Celsa A., Mohawk K., Teel L., O'Brien A. Pathogenesis of Shiga-toxin producing Escherichia coli. Curr. Top. Microbiol. Immunol. 2012, 357:67-103.
42. Monecke S., Mariani-Kurkdjian P., Bingen E., Weill F.X., Baliere C., Slickers P., Ehricht R. Presence of enterohemorrhagic Escherichia coli ST678/O104:H4 in France prior to 2011. Appl. Environ. Microbiol. 2011, 77:8784-8786.
43. Mora A., Herrera A., Lopez C., Dahbi G., Mamani R., Pita J.M., Alonso M.P., Llovo J., Bernardez M.I., Blanco J.E., Blanco M., Blanco J. Characteristics of the Shiga-toxin-producing enteroaggregative Escherihcia coli O104:H4 German outbreak strain and of STEC strains isolated in Spain. Int. Microbiol. 2011, 14:121-141.
44. Nataro J.P., Steiner T., Guerrant R.L. Enteroaggregative Escherichia coli. Emerg. Infect. Dis. 1998, 4:251-261.
45. Okeke I.N. Diarrheagenic Escherichia coli in sub-Saharan Africa: status, uncertainties and necessities. J. Infect. Dev. Ctries 2009, 3:817-842.
46. Okhuysen P.C., Dupont H.L. Enteroaggregative Escherichia coli (EAEC): a cause of acute and persistent diarrhea of worldwide importance. J. Infect. Dis. 2010, 202:503-505.
47. Orskov F., Orskov I. Serotyping of Escherichia coli. Methods in Microbiology 1984, 43-112. Academic Press, London, United Kingdom. T. Bergan (Ed.).
48. Paton A.W., Srimanote P., Talbot U.M., Wang H., Paton J.C. A New Family of Potent AB5 Cytotoxins Produced by Shiga Toxigenic Escherichia coli. J. Exp. Med. 2004, 200:35-46.
49. Paton A.W., Srimanote P., Woodrow M.C., Paton J.C. Characterization of Saa, a Novel Autoagglutinating Adhesin Produced by Locus of Enterocyte Effacement-Negative Shiga-Toxigenic Escherichia coli Strains That Are Virulent for Humans. Infect. Immun. 2001, 69:6999-7009.
50. Persson S., Olsen K.E., Ethelberg S., Scheutz F. Subtyping method for Escherichia coli shiga toxin (verocytotoxin) 2 variants and correlations to clinical manifestations. J. Clin. Microbiol. 2007, 45:2020-2024.
51. Rashid R.A., Tarr P.I., Moseley S.L. Expression of the Escherichia coli IrgA homolog adhesin is regulated by the ferric uptake regulation protein. Microb. Pathog. 2006, 41:207-217.
52. Rasko D.A., Webster D.R., Sahl J.W., Bashir A., Boisen N., Scheutz F., Paxinos E.E., Sebra R., Chin C.S., Iliopoulos D., Klammer A., Peluso P., Lee L., Kislyuk A.O., Bullard J., Kasarskis A., Wang S., Eid J., Rank D., Redman J.C., Steyert S.R., Frimodt-Moller J., Struve C., Petersen A.M., Krogfelt K.A., Nataro J.P., Schadt E.E., Waldor M.K. Origins of the E. coli strain causing an outbreak of hemolytic-uremic syndrome in Germany. N. Engl. J. Med. 2011, 365:709-717.
53. Robert Koch-Institut Final presentation and evaluation of epidemiological findings in the EHEC O104:H4 Outbreak, Germany 2011 2011, RKI, Department for Infectious Disease Epidemiology, Division 35, Berlin, Germany, http://www.rki.de/EN/Home/EHEC_final_report.pdf?__blob=publicationFile. Robert Koch-Institut (Ed.).
54. Rohde H., Qin J., Cui Y., Li D., Loman N.J., Hentschke M., Chen W., Pu F., Peng Y., Li J., Xi F., Li S., Li Y., Zhang Z., Yang X., Zhao M., Wang P., Guan Y., Cen Z., Zhao X., Christner M., Kobbe R., Loos S., Oh J., Yang L., Danchin A., Gao G.F., Song Y., Li Y., Yang H., Wang J., Xu J., Pallen M.J., Wang J., Aepfelbacher M., Yang R. Open-source genomic analysis of shiga-toxin-producing E. coli O104:H4. N. Engl. J. Med. 2011, 365:718-724.
55. Rump L.V., Bodeis-Jones S., Abbott J., Zhao S., Kase J., Lorenz S., Fischer M., Brown E., Meng J. Genetic characterization of Escherichia coli O104 isolates from different sources in the United States. Appl. Environ. Microbiol. 2012, 78:1615-1618.
56. Scheutz F., Moller N.E., Frimodt-Moller J., Boisen N., Morabito S., Tozzoli R., Nataro J., Caprioli A. Characteristics of the enteroaggregative Shiga toxin/verotoxin-producing Escherichia coli O104:H4 strain causing the outbreak of haemolytic uraemic syndrome in Germany, May to June 2011. Euro Surveill. 2011, 16(24).
57. Scheutz F., Strockbine N.A. Genus I. Escherichia. Bergey's Manual of Systematic Bacteriology 2005, 607-624. Springer, New York, NY. G.M. Garrity, D.J. Brenner, N.R. Krieg, J.T. Staley (Eds.).
58. Scheutz F., Teel L.D., Beutin L., Pierard D., Buvens G., Karch H., Mellmann A., Caprioli A., Tozzoli R., Morabito S., Strockbine N.A., Melton-Celsa A.R., Sanchez M., Persson S., O'Brien A.D. Multicenter evaluation of a sequence-based protocol for subtyping shiga toxins and standardizing stx nomenclature. J. Clin. Microbiol. 2012, 50:2951-2963.
59. Schubert S., Rakin A., Karch H., Carniel E., Heesemann J. Prevalence of the "high-pathogenicity island" of Yersinia species among Escherichia coli strains that are pathogenic to humans. Infect. Immun. 1998, 66:480-485.
60. Tzschoppe M., Martin A., Beutin L. A rapid procedure for the detection and isolation of enterohaemorrhagic Escherichia coli (EHEC) serogroup O26, O103, O111, O118, O121, O145 and O157 strains and the aggregative EHEC O104:H4 strain from ready-to-eat vegetables. Int. J. Food Microbiol. 2012, 152:19-30.
61. Uber A.P., Trabulsi L.R., Irino K., Beutin L., Ghilardi A.C., Gomes T.A., Liberatore A.M., de Castro A.F., Elias W.P. Enteroaggregative Escherichia coli from humans and animals differ in major phenotypical traits and virulence genes. FEMS Microbiol. Lett. 2006, 256:251-257.
62. Wang L., Briggs C.E., Rothemund D., Fratamico P., Luchansky J.B., Reeves P.R. Sequence of the E. coli O104 antigen gene cluster and identification of O104 specific genes. Gene 2001, 270:231-236.
63. Welinder-Olsson C., Badenfors M., Cheasty T., Kjellin E., Kaijser B. Genetic profiling of enterohemorrhagic Escherichia coli strains in relation to clonality and clinical signs of infection. J. Clin. Microbiol. 2002, 40:959-964.
64. Whitfield C., Roberts I.S. Structure, assembly and regulation of expression of capsules in Escherichia coli. Mol. Microbiol. 1999, 31:1307-1319.
65. Wieler L.H., Semmler T., Eichhorn I., Antao E.M., Kinnemann B., Geue L., Karch H., Guenther S., Bethe A. No evidence of the Shiga toxin-producing E. coli O104:H4 outbreak strain or enteroaggregative E. coli (EAEC) found in cattle faeces in northern Germany, the hotspot of the 2011 HUS outbreak area. Gut Pathog. 2011, 3:17.
66. Wong A.R., Pearson J.S., Bright M.D., Munera D., Robinson K.S., Lee S.F., Frankel G., Hartland E.L. Enteropathogenic and enterohaemorrhagic Escherichia coli: even more subversive elements. Mol. Microbiol. 2011, 80:1420-1438.