Characteristics of the Shiga-toxin-producing enteroaggregative Escherichia coli O104:H4 German outbreak strain and of STEC strains isolated in Spain

International Microbiology

Volumn 14, Issue 3, 2011, Pages 121-141

  Mora, Azucena ^a   Herrera, Alexandra ^a   López, Cecilia ^a   Dahbi, Ghizlane ^a   Mamani, Rosalia ^a   Pita, Julia M ^b   Alonso, María P ^b   Llovo, José ^c   Bernárdez, María I ^a,c   Blanco, Jesús E ^a   Blanco, Miguel ^a   Blanco, Jorge ^a  

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^b Hospital Lucus Augusti   (Spain)

^c HOSPITAL CLÍNICO UNIVERSITARIO   (Spain)

Author keywords

Enteroaggregative E. coli; Enterohemorrhagic escherichia coli; Serotypes O104:H4, O157:H7, O146:H21; Shiga toxin

Indexed keywords

EID: 82155171970     PISSN: 11396709     EISSN: 16181905     Source Type: Journal    
DOI: 10.2436/20.1501.01.142     Document Type: Article

References (85)

1. Aidar-Ugrinovich L, Blanco J, Blanco M, Blanco JE, Leomil L, Dahbi G, Mora A, Onuma DL, Silveira WD, Pestana de Castro AF (2007) Serotypes, virulence genes, and intimin types of Shiga toxin-producing Escherichia coli (STEC) and enteropathogenic E. coli (EPEC) isolated from calves in São Paulo, Brazil. Int J Food Microbiol 115:297-306
2. Alonso S, Mora A, Blanco M, et al. (2007) Fecal carriage of Escherichia coli O157:H7 and carcass contamination in cattle at slaughter in northern Italy. Int Microbiol 10:109-116
3. Bae WK, Lee YK, Cho MS, Ma SK, Kim SW, Kim NH, Choi KC (2006) Acase of hemolytic uremic syndrome caused by Escherichia coli O104:H4. Yonsei Med J 47:437-439
4. Beutin L, Krause G, Zimmermann S, Kaulfuss S, Gleier K (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
5. Bielaszewska M, Mellmann A, Zhang W, Köck R, Fruth A, Bauwens A, Peters G, Karch H (2011) Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany, 2011: a microbiological study. Lancet Infect Dis 11:671-676
6. Blanco J, Blanco M, Blanco JE, Alonso MP, Escribano A (1993) [Pathogenesis, epidemiology, and microbiologic diagnosis of infections caused by verotoxin-producing enterohemorrhagic Escherichia coli]. Enferm Infecc Microbiol Clin 11:324-334 (In Spanish)
7. Blanco M, Blanco JE, Mora A, et al. (2003) Serotypes, virulence genes, and intimin types of Shiga toxin (verotoxin)-producing Escherichia coli isolates from healthy sheep in Spain. J Clin Microbiol 41:1351-1365
8. Blanco J, Blanco M, Blanco JE, et al. (2003) Verotoxin-producing Escherichia coli in Spain: prevalence, serotypes, and virulence genes of O157:H7 and non-O157 VTEC in ruminants, raw beef products, and humans. Exp Biol Med (Maywood) 228:345-351
9. Blanco JE, Blanco M, Alonso MP, Mora A, Dahbi G, Coira MA, Blanco J (2004) 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
10. Blanco M, Blanco JE, Mora A, Dahbi G, Alonso MP, González EA, Bernárdez MI, Blanco J (2004) 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
11. Blanco M, Padola NL, Krüger A, et al. (2004) Virulence genes and intimin types of Shiga-toxin-producing Escherichia coli isolated from cattle and beef products in Argentina. Int Microbiol 7:269-276
12. Blanco M, Blanco JE, Dahbi G, et al. (2006) Identification of two new intimin types in atypical enteropathogenic Escherichia coli. Int Microbiol 9:103-110
13. Blanco M, Blanco JE, Dhabi G, Mora A, Alonso MP, Varela G, Gadea MP, Schelotto F, González EA, Blanco J (2006) Typing of intimin (eae) genes from enteropathogenic Escherichia coli (EPEC) isolatedfrom children with diarrhoea in Montevideo, Uruguay: identification of two novel intimin variants (μB and ξR/β2B). J Med Microbiol 55:1165-1174
14. Blanco M, Alonso MP, Nicolas-Chanoine MH, et al. (2009) Molecular epidemiology of Escherichia coli producing extended-spectrum β-lactamases in Lugo (Spain): dissemination of clone O25b:H4-ST131 producing CTX-M-15 J Antimicrob Chemother 63:1135-1141
15. Blanco J, Mora A, Mamani R, et al. (2011) National survey of Escherichia coli causing extraintestinal infections reveals the spread of drug-resistant clonal groups O25b:H4-B2-ST131, O15:H1-D-ST393 and CGA-D-ST69 with high virulence gene content in Spain. J Antimicrob Chemother 66:2011-2021
16. Brzuszkiewicz E, Thürmer A, Schuldes J, Leimbach A, Liesegang H, Meyer FD, Boelter J, Petersen H, Gottschalk G, Daniel R (2011) 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. DOI: 10.1007/s00203-011-0725-6
17. Caro I, Mateo J, García-Armesto MR (2007) Phenotypical characteristics of Shiga-like toxin Escherichia coli isolated from sheep dairy products. Lett Appl Microbiol 45:295-300
18. Chattaway MA, Dallman T, Okeke IN, Wain J (2011) Enteroaggregative E. coli O104 from an outbreak of HUS in Germany 2011, could it happen again? J Infect Dev Ctries 5:425-436
19. Cortés C, De la Fuente R, Blanco J, et al. (2005) Serotypes, virulence genes and intimin types of verotoxin-producing Escherichia coli and enteropathogenic E. coli isolated from healthy dairy goats in Spain. Vet Microbiol 110:67-76
20. Denamur E (2011) The 2011 Shiga toxin-producing Escherichia coli O104:H4 German outbreak: a lesson in genomic plasticity. Clin Microbiol Infect 17:1124-1125
21. Desmarchelier PM, Bilge SS, Fegan N, Mills L, Vary JC Jr, Tarr PI (1998) A PCR specific for Escherichia coli O157 based on the rfb locus encoding O157 lipopolysaccharide. J Clin Microbiol 36:1801-1804
22. Durso LM, Bono JL, Keen JE (2005) Molecular serotyping of Escherichia coli O26:H11. Appl Environ Microbiol 71:4941-4944
23. European Centre for Disease Prevention and Control and European Food Safety Authority (2011) 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. Stockholm: ECDC; 2011. DOI:10.2900/55055
24. European Food Safety Authority (2009) Technical specifications for the monitoring and reporting of verotoxigenic Escherichia coli (VTEC) on animals and food (VTEC surveys on animals and food) on request of EFSA. EFSA Journal 2009; 7(11):1366 [43 pp]. DOI:10.2903/ j.efsa.2009.1366
25. European Food Safety Authority (2011) Urgent advice on the public health risk of Shiga-toxin producing Escherichia coli in fresh vegetables. EFSA Journal 2011; 9(6):2274 [50 pp]. DOI:10.2903/ j.efsa.2011.2274
26. European Food Safety Authority (2011) Tracing seeds, in particular fenugreek (Trigonella foenum-graecum) seeds, in relation to the Shiga toxin-producing E. coli (STEC) O104:H4 2011 outbreaks in Germany and France.
27. Frank C, Werber D, Cramer JP, et al. (2011) Epidemic profile of Shigatoxin- producing Escherichia coli O104:H4 outbreak in Germany-Preliminary Report. N Engl J Med. 2011 Jun 22 DOI: 10.1056/ NEJMoa1106483
28. Friesema I, Sigmundsdottir G, van der Zwaluw K, et al. (2008) An international outbreak of Shiga toxin-producing Escherichia coli O157 infection due to lettuce, September-October 2007. Euro Surveill 13(50), pii:19065
29. Friesema IH, VAN DE Kassteele J, DE Jager CM, Heuvelink AE, VAN Pelt W (2010) Geographical association between livestock density and human Shiga toxin-producing Escherichia coli O157 infections. Epidemiol Infect 8:1-7
30. Gannon VP, D'Souza S, Graham T, King RK, Rahn K, Read S (1997) Use of the flagellar H7 gene as a target in multiplex PCR assays and improved specificity in identification of enterohemorrhagic Escherichia coli strains. J Clin Microbiol 35:656-662
31. García-Aljaro C, Muniesa M, Blanco JE, Blanco M, Blanco J, Jofre J, Blanch AR (2005) Characterization of Shiga toxin-producing Escherichia coli isolated from aquatic environments. FEMS Microbiol Lett 246:55-65
32. Garmendia J, Frankel G, Crepin VF (2005) Enteropathogenic and enterohemorrhagic Escherichia coli infections: translocation, translocation, translocation. Infect Immun 73:2573-2585
33. Garrido P, Blanco M, Moreno-Paz M, Briones C, Dahbi G, Blanco JE, Blanco J, Parro V (2006) STEC-EPEC oligonucleotide microarray: a new tool for typing genetic variants of the LEE pathogenicity island of human and animal Shiga toxin-producing Escherichia coli (STEC) and enteropathogenic E. coli (EPEC) strains. Clin Chem 52:192-201
34. Gault G, Weill F, Mariani-Kurkdjian P, et al. (2011) Outbreak of haemolytic uraemic syndrome and bloody diarrhoea due to Escherichia coli O104:H4, south-west France, June 2011. Euro Surveill. 16(26), pii: 19905
35. Gould LH, Bopp C, Strockbine N, et al. (2009) Recommendations for diagnosis of shiga toxin-producing Escherichia coli infections by clinical laboratories. MMWR Recomm Rep. 58:1-14
36. Gunzburg ST, Tornieporth NG, Riley LW (1995) Identification of enteropathogenic Escherichia coli by PCR-based detection of the bundle- forming pilus gene. J Clin Microbiol 33:1375-1377
37. Gyles CL (2007) Shiga toxin-producing Escherichia coli: an overview. J Anim Sci. 85(13 Suppl): E45-62
38. Imamovic L, Muniesa M (2011) Quantification and evaluation of infectivity of Shiga toxin-encoding bacteriophages in beef and salad. Appl Environ Microbiol 77:3536-3540
39. Itoh Y, Nagano I, Kunishima M, Ezaki T (1997) Laboratory investigation of enteroaggregative Escherichia coli O untypeable:H10 associated with a massive outbreak of gastrointestinal illness. J Clin Microbiol 35:2546-2550
40. Käppeli U, Hächler H, Giezendanner N, Beutin L, Stephan R (2011) Human infections with non-O157 Shiga toxin-producing Escherichia coli, Switzerland, 2000-2009. Emerg Infect Dis 17:180-185
41. Karmali MA, Mascarenhas M, Shen S, Ziebell K, Johnson S, Reid- Smith R, Isaac-Renton J, Clark C, Rahn K, Kaper JB (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
42. Kaspar C, Doyle ME, Archer J (2009) FRI Food Safety Review: non- O157:H7 Shiga toxin-producing E. coli from meat and non-meat sources. Food Research Institute, UW-Madison. Available at: http://fri.wisc.edu/docs/pdf/FRI_Brief_NonO157STEC_4_10.pdf
43. Khakria R, Duck D, Lior H (1990) Extended phage-typing scheme for Escherichia coli O157:H7. Epidemiol Infect 105:511-520
44. Martin A, Beutin L (2011) 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 146:99-104
45. Martinez-Medina M, Aldeguer X, López-Siles M, González-Huix F, López-Oliu C, Dahbi G, Blanco JE, Blanco J, Garcia-Gil LJ, Darfeuille- Michaud A (2009) Molecular diversity of Escherichia coli in the human gut: new ecological evidence supporting the role of adherent-invasive E. coli (AIEC) in Crohn's disease. Inflamm Bowel Dis 15:872-882
46. Mellmann A, Bielaszewska M, Köck R, Friedrich AW, Fruth A, Middendorf B, Harmsen D, Schmidt MA, Karch H (2008) Analysis of collection of hemolytic uremic syndrome-associated enterohemorrhagic Escherichia coli. Emerg Infect Dis 14:1287-1290
47. Mellmann A, Harmsen D, Cummings CA, et al. (2011) Prospective genomic characterization of the German enterohemorrhagic Escherichia coli O104:H4 outbreak by Rapid Next Generation Sequencing Technology. PLoS One. 6:e22751
48. Mendez-Arancibia E, Vargas M, Soto S, Ruiz J, Kahigwa E, Schellenberg D, Urassa H, Gascón J, Vila J (2008) Prevalence of different virulence factors and biofilm production in enteroaggregative Escherichia coli isolates causing diarrhea in children in Ifakara (Tanzania). Am J Trop Med Hyg 78:985-989
49. Michino H, Araki K, Minami S, Takaya S, Sakai N, Miyazaki M, Ono A, Yanagawa H (1999) Massive outbreak of Escherichia coli O157:H7 infection in schoolchildren in Sakai City, Japan, associated with consumption of white radish sprouts. Am J Epidemiol 150:787-796
50. Mira A, Martín-Cuadrado AB, D'Auria G, Rodríguez-Valera F (2010) The bacterial pan-genome: a new paradigm in microbiology. Int Microbiol 13:45-57
51. Mora A, Blanco M, Blanco JE, Alonso MP, Dhabi G, Thomson-Carter F, Usera MA, Bartolomé R, Prats G, Blanco J (2004) Phage types and genotypes of shiga toxin-producing Escherichia coli O157:H7 isolates from humans and animals in Spain: identification and characterization of two predominating phage types (PT2 and PT8). J Clin Microbiol 42:4007-4015
52. Mora A, Blanco JE, Blanco M, Alonso MP, Dhabi G, Echeita A, González EA, Bernárdez MI, Blanco J (2005) Antimicrobial resistance of Shiga toxin (verotoxin)-producing Escherichia coli O157:H7 and non-O157 strains isolated from humans, cattle, sheep and food in Spain. Res Microbiol 156:793-806
53. Mora A, Blanco M, Blanco JE, Dahbi G, López C, Justel P, Alonso MP, Echeita A, Bernárdez MI, González EA, Blanco J (2007) Serotypes, virulence genes and intimin types of Shiga toxin (verocytotoxin)-producing Escherichia coli isolates from minced beef in Lugo (Spain) from 1995 through 2003. BMC Microbiol 7:13
54. Mora A, León SL, Blanco M, Blanco JE, López C, Dahbi G, Echeita A, González EA, Blanco J (2007) Phage types, virulence genes and PFGE profiles of Shiga toxin-producing Escherichia coli O157:H7 isolated from raw beef, soft cheese and vegetables in Lima (Peru). Int J Food Microbiol 114:204-210
55. Mora A, Blanco M, Yamamoto D, et al. (2009) HeLa-cell adherence patterns and actin aggregation of enteropathogenic Escherichia coli (EPEC) and Shiga-toxin-producing E. coli (STEC) strains carrying different eae and tir alleles. Int Microbiol 12:243-251
56. Mora A, Herrera A, Mamani R, et al. (2010) Recent emergence of clonal group O25b:K1:H4-B2-ST131 ibeA strains among Escherichia coli poultry isolates, including CTX-M-9-producing strains, and comparison with clinical human isolates. Appl Environ Microbiol 76:6991-6997
57. Morabito S, Karch H, Mariani-Kurkdjian P, Schmidt H, Minelli F, Bingen E, Caprioli A (1998) Enteroaggregative, Shiga toxin-producing Escherichia coli O111:H2 associated with an outbreak of hemolyticuremic syndrome. J Clin Microbiol 36:840-842
58. Muniesa M, de Simon M, Prats G, Ferrer D, Pañella H, Jofre J (2003) Shiga toxin 2-converting bacteriophages associated with clonal variability in Escherichia coli O157:H7 strains of human origin isolated from a single outbreak. Infect Immun 71:4554-4562
59. Muniesa M, Blanco JE, De Simón M, Serra-Moreno R, Blanch AR, Jofre J (2004) Diversity of stx2 converting bacteriophages induced from Shiga-toxin-producing Escherichia coli strains isolated from cattle. Microbiology 150:2959-2971
60. Nielsen EM, Scheutz F, Torpdahl M (2006) Continuous surveillance of Shiga toxin-producing Escherichia coli infections by pulsed-field gel electrophoresis shows that most infections are sporadic. Foodborne Pathog Dis 3:81-87
61. Okeke IN, Wallace-Gadsden F, Simons HR, Matthews N, Labar AS, Hwang J, Wain J (2010) Multi-locus sequence typing of enteroaggregative Escherichia coli isolates from Nigerian children uncovers multiple lineages. PLoS One 5(11):e14093
62. Orden JA, Ruiz-Santa-Quiteria JA, Blanco M, Blanco JE, Mora A, Cid D, González EA, Blanco J, de la Fuente R (2003) Prevalence and characterization of Vero cytotoxin-producing Escherichia coli isolated from diarrhoeic and healthy sheep and goats. Epidemiol Infect 130:313-321
63. Orden JA, Cortés C, Horcajo P, et al. (2008) A longitudinal study of verotoxin-producing Escherichia coli in two dairy goat herds. Vet Microbiol 132:428-434
64. Pebody RG, Furtado C, Rojas A, et al. (1999) An international outbreak of Vero cytotoxin-producing Escherichia coli O157 infection amongst tourists; a challenge for the European infectious disease surveillance network. Epidemiol Infect 123:217-223
65. Pennington H (2010) Escherichia coli O157. Lancet 376:1428-1435
66. Piva IC, Pereira AL, Ferraz LR, Silva RS, Vieira AC, Blanco JE, Blanco M, Blanco J, Giugliano LG (2003) Virulence markers of enteroaggregative Escherichia coli isolated from children and adults with diarrhea in Brasília, Brazil. J Clin Microbiol. 41:1827-1832
67. Prats G, Frías C, Margall N, et al. (1996) [Hemorrhagic colitis caused by verotoxigenic Escherichia coli. Presentation of 9 cases]. Enferm Infecc Microbiol Clin. 14:7-15 [In Spanish]
68. Rasko DA, Webster DR, Sahl JW, et al. (2011) Origins of the E. coli strain causing an outbreak of hemolytic-uremic syndrome in Germany. N Engl J Med 365:709-717
69. Rey J, Sánchez S, Blanco JE, Hermoso de Mendoza J, Hermoso de Mendoza M, García A, Gil C, Tejero N, Rubio R, Alonso JM (2006) Prevalence, serotypes and virulence genes of Shiga toxin-producing Escherichia coli isolated from ovine and caprine milk and other dairy products in Spain. Int J Food Microbiol 107:212-217
70. Robert Koch Institute (RKI) EHEC/HUS O104:H4 - The outbreak is considered to be over. http://www.rki.de/cln_117/nn_217400/EN/Home/PM__EHEC.html
71. Rohde H, Qin J, Cui Y, et al. (2011) Open-source genomic analysis of Shiga-toxin-producing E. coli O104:H4. N Engl J Med 365:718-724
72. Sánchez S, García-Sánchez A, Martínez R, et al. (2009) Detection and characterisation of Shiga toxin-producing Escherichia coli other than Escherichia coli O157:H7 in wild ruminants. Vet J 180:384-388
73. Sánchez S, Martínez R, Rey J, et al. JM (2010) Pheno-genotypic characterisation of Escherichia coli O157:H7 isolates from domestic and wild ruminants. Vet Microbiol 142:445-449
74. Sánchez S, Martínez R, García A, et al. (2010) Detection and characterisation of O157:H7 and non-O157 Shiga toxin-producing Escherichia coli in wild boars. Vet Microbiol 143:420-423
75. Sánchez S, Martínez R, Alonso JM, Rey J (2010) [Clinical and pathogenic aspects of infections due to Escherichia coli O157:H7 and other verocytotoxigenic E. coli]. Enferm Infecc Microbiol Clin 28:370-374. [In Spanish]
76. Scheutz F, Moller Nielsen E, Frimodt-Moller J, Boisen N, Morabito S, Tozzoli R, Nataro J, Caprioli A (2011) 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 16(24), pii: 19889
77. Schmidt H, Knop C, Franke S, Aleksic S, Heesemann J, Karch H (1995) Development of PCR for screening of enteroaggregative Escherichia coli. J Clin Microbiol 33:701-705
78. Schultsz C, Pool GJ, van Ketel R, de Wever B, Speelman P, Dankert J (1994) Detection of enterotoxigenic Escherichia coli in stool samples by using nonradioactively labeled oligonucleotide DNA probes and PCR. J Clin Microbiol 32:2393-2397
79. Söderström A, Osterberg P, Lindqvist A, et al. (2008) A large Escherichia coli O157 outbreak in Sweden associated with locally produced lettuce. Foodborne Pathog Dis 5:339-349
80. Tornieporth NG, John J, Salgado K, de Jesus P, Latham E, Melo MC, Gunzburg ST, Riley LW (1995) Differentiation of pathogenic Escherichia coli strains in Brazilian children by PCR. J Clin Microbiol 33: 1371-1374
81. Torres AG, Blanco M, Valenzuela P, et al. (2009) Genes related to long polar fimbriae of pathogenic Escherichia coli strains as reliable markers to identify virulent isolates. J Clin Microbiol 47:2442-2451
82. Wendel AM, Johnson DH, Sharapov U, Grant J, Archer JR, Monson T, Koschmann C, Davis JP (2009) Multistate outbreak of Escherichia coli O157:H7 infection associated with consumption of packaged spinach, August-September 2006: the Wisconsin investigation. Clin Infect Dis 48:1079-1086
83. Werber D, Beutin L, Pichner R, Stark K, Fruth A (2008) Shiga toxinproducing Escherichia coli serogroups in food and patients, Germany. Emerg Infect Dis 14:1803-1806
84. Kim J, Oh K, Jeon S, et al. (2011) Escherichia coli O104:H4 from 2011 European outbreak and strain from South Korea. Emerg Infect Dis 17: 1755-1756
85. Scavia G, Morabito S, Tozzoli R, et al. (2011) Similarity of Shiga toxin-producing Escherichia coli O104:H4 strains from Italy and Germany. Emerg Infect Dis 17:1957-1958