Multicenter evaluation of a sequence-based protocol for subtyping Shiga toxins and standardizing Stx nomenclature

Journal of Clinical Microbiology

Volumn 50, Issue 9, 2012, Pages 2951-2963

  Scheutz, Flemming ^a   Teel, Louise D ^b   Beutin, Lothar ^c   Piérard, Denis ^d   Buvens, Glenn ^d   Karch, Helge ^e   Mellmann, Alexander ^e   Caprioli, Alfredo ^f   Tozzoli, Rosangela ^f   Morabito, Stefano ^f   Strockbine, Nancy A ^g   Melton Celsa, Angela R ^b   Sanchez, Maria ^b   Persson, Søren ^a   O'Brien, Alison D ^b  

^a STATENS SERUM INSTITUT   (Denmark)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^c FEDERAL INSTITUTE FOR RISK ASSESSMENT   (Germany)

^d UNIVERSITY HOSPITAL BRUSSELS   (Belgium)

^e UNIVERSITY OF MÜNSTER   (Germany)

^f ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^g NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HOLOTOXIN PROTEIN; SHIGA TOXIN; UNCLASSIFIED DRUG; VEROTOXIN 1; VEROTOXIN 2;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM EXAMINATION; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; GENE SEQUENCE; GENETIC VARIABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY; SEQUENCE ANALYSIS; SHIGA TOXIN PRODUCING ESCHERICHIA COLI; SPECIES DIFFERENCE; STX GENE;

GENOTYPE; HUMANS; POLYMERASE CHAIN REACTION; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; SHIGA TOXINS; SHIGA-TOXIGENIC ESCHERICHIA COLI; TERMINOLOGY AS TOPIC;

EID: 84865192343     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.00860-12     Document Type: Article

References (68)

1. Asakura H, et al. 1998. Detection and long-term existence of Shiga toxin (Stx)-producing Escherichia coli in sheep. Microbiol. Immunol. 42:683-688. (Pubitemid 28485455)
2. Asakura H, et al. 2001. Phylogenetic diversity and similarity of active sites of Shiga toxin (Stx) in Shiga toxin-producing Escherichia coli (STEC) isolates from humans and animals. Epidemiol. Infect. 127:27-36. (Pubitemid 32825637)
3. Bastian SN, Carle I, Grimont F. 1998. Comparison of 14 PCR systems for the detection and subtyping of stx genes in Shiga-toxin-producing Escherichia coli. Res. Microbiol. 149:457-472. (Pubitemid 28393835)
4. Bellin T, Pulz M, Matussek A, Hempen HG, Gunzer F. 2001. Rapid detection of enterohemorrhagic Escherichia coli by real-time PCR with fluorescent hybridization probes. J. Clin. Microbiol. 39:370-374. (Pubitemid 32059624)
5. Bertin Y, Boukhors K, Pradel N, Livrelli V, Martin C. 2001. Stx2 subtyping of Shiga toxin-producing Escherichia coli isolated from cattle in France: detection of a new Stx2 subtype and correlation with additional virulence factors. J. Clin. Microbiol. 39:3060-3065. (Pubitemid 32830294)
6. 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. (Pubitemid 38332832)
7. Beutin L, et al. 2007. 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. 73:4769-4775. (Pubitemid 47237224)
8. Beutin L, et al. 2007. Comparative evaluation of the Ridascreen Vero-toxin enzyme immunoassay for detection of Shiga-toxin producing strains of Escherichia coli (STEC) from food and other sources. J. Appl. Microbiol. 102:630-639.
9. Beutin L, Strauch E, Fischer I. 1999. Isolation of Shigella sonnei lysogenic for a bacteriophage encoding gene for production of Shiga toxin. Lancet 353:1498. (Pubitemid 29204377)
10. Bielaszewská M, Friedrich AW, Aldick T, Schurk-Bulgrin R, Karch H. 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. (Pubitemid 44632799)
11. Bürk C, et al. 2003. Identification and characterization of a new variant of Shiga toxin 1 in Escherichia coli ONT:H19 of bovine origin. J. Clin. Microbiol. 41:2106-2112. (Pubitemid 36576542)
12. Calderwood SB, et al. 1996. Proposed new nomenclature for SLT (VT) family. ASM News 62:118-119.
13. De Baets L, et al. 2004. Genetic typing of Shiga toxin 2 variants of Escherichia coli by PCR-restriction fragment length polymorphism analysis. Appl. Environ. Microbiol. 70:6309-6314. (Pubitemid 39471885)
14. de Sablet T, et al. 2008. Differential expression of stx2 variants in Shiga toxin-producing Escherichia coli belonging to seropathotypes A and C. Microbiology 154:176-186. (Pubitemid 351201397)
15. Franke S, et al. 1995. Clonal relatedness of Shiga-like toxin-producing Escherichia coli O101 strains of human and porcine origin. J. Clin. Microbiol. 33:3174-3178.
16. Friedrich AW, et al. 2002. Escherichia coli harboring Shiga toxin 2 gene variants: frequency and association with clinical symptoms. J. Infect. Dis. 185:74-84. (Pubitemid 34043019)
17. Friedrich AW, et al. 2003. Shiga toxin 1c-producing Escherichia coli strains: phenotypic and genetic characterization and association with human disease. J. Clin. Microbiol. 41:2448-2453. (Pubitemid 36712450)
18. Gannon VP, Teerling C, Masri SA, Gyles CL. 1990. Molecular cloning and nucleotide sequence of another variant of the Escherichia coli Shiga-like toxin II family. J. Gen. Microbiol. 136:1125-1135. (Pubitemid 20209267)
19. Garcia-Aljaro C, et al. 2005. Characterization of Shiga toxin-producing Escherichia coli isolated from aquatic environments. FEMS Microbiol. Lett. 246:55-65. (Pubitemid 40616284)
20. Gilmour MW, et al. 2007. Isolation and genetic characterization of a coinfection of non-O157 Shiga toxin-producing Escherichia coli. J. Clin. Microbiol. 45:3771-3773. (Pubitemid 350156881)
21. Gobius KS, Higgs GM, Desmarchelier PM. 2003. Presence of activatable Shiga toxin genotype (stx2d) in Shiga toxigenic Escherichia coli from livestock sources. J. Clin. Microbiol. 41:3777-3783. (Pubitemid 36994715)
22. Ito H, Terai A, Kurazono H, Takeda Y, Nishibuchi M. 1990. Cloning and nucleotide sequencing of Vero toxin 2 variant genes from Escherichia coli O91:H21 isolated from a patient with hemolytic uremic syndrome. Microb. Pathog. 8:47-60. (Pubitemid 20222891)
23. Iwasa M, Makino S, Asakura H, Kobori H, Morimoto Y. 1999. Detection of Escherichia coli O157:H7 from Musca domestica (Diptera: Muscidae) at a cattle farm in Japan. J. Med. Entomol. 36:108-112. (Pubitemid 129559019)
24. Jackson MP, Neill RJ, O'Brien AD, Holmes RK, Newland JW. 1987. Nucleotide sequence analysis and comparison of the structural genes for Shiga-like toxin I and Shiga-like toxin II encoded by bacteriophages from Escherichia coli 933. FEMS Microbiol. Lett. 44:109-114.
25. Jackson MP, Newland JW, Holmes RK, O'Brien AD. 1987. Nucleotide sequence analysis of the structural genes for Shiga-like toxin I encoded by bacteriophage 933J from Escherichia coli. Microb. Pathog. 2:147-153. (Pubitemid 17039513)
26. Jelacic JK, et al. 2003. Shiga toxin-producing Escherichia coli in Montana: bacterial genotypes and clinical profiles. J. Infect. Dis. 188:719-729. (Pubitemid 37115185)
27. Karmali MA, Lingwood CA, Petric M, Brunton J, Gyles C. 1996. Maintaining the existing phenotype nomenclatures for E. coli cytotoxins. ASM News 62:167-169.
28. Kauffmann F. 1966. The bacteriology of Enterobacteriaceae, 2nd ed. Munksgaard, Copenhagen, Denmark.
29. Koch C, Hertwig S, Lurz R, Appel B, Beutin L. 2001. Isolation of a lysogenic bacteriophage carrying the stx1OX3 gene, which is closely associated with Shiga toxin-producing Escherichia coli strains from sheep and humans. J. Clin. Microbiol. 39:3992-3998. (Pubitemid 33029773)
30. Konowalchuk J, Speirs JI, Stavric S. 1977. Vero response to a cytotoxin of Escherichia coli. Infect. Immun. 18:775-779. (Pubitemid 8247697)
31. Kusumoto M, Nishiya Y, Kawamura Y, Shinagawa K. 1999. Identification of an insertion sequence, IS1203 variant, in a Shiga toxin 2 gene of Escherichia coli O157:H7. J. Biosci. Bioeng. 87:93-96. (Pubitemid 29162237)
32. Lee JE, et al. 2007. Phylogenetic analysis of Shiga toxin 1 and Shiga toxin 2 genes associated with disease outbreaks. BMC Microbiol. 7:109.
33. Leung PHM, et al. 2003. A newly discovered verotoxin variant, VT2g, produced by bovine verocytotoxigenic Escherichia coli. Appl. Environ. Microbiol. 69:7549-7553. (Pubitemid 38585416)
34. Lindgren SW, Melton-Celsa AR, O'Brien AD. 1993. Virulence of enterohemorrhagic Escherichia coli O91:H21 clinical isolates in an orally infected mouse model. Infect. Immun. 61:3832-3842. (Pubitemid 23260057)
35. Mellmann A, et al. 2008. Analysis of collection of hemolytic uremic syndrome-associated enterohemorrhagic Escherichia coli. Emerg. Infect. Dis. 14:1287-1290.
36. Melton-Celsa AR, Darnell SC, O'Brien AD. 1996. Activation of Shiga-like toxins by mouse and human intestinal mucus correlates with virulence of enterohemorrhagic Escherichia coli O91:H21 isolates in orally infected, streptomycin-treated mice. Infect. Immun. 64:1569-1576. (Pubitemid 26129817)
37. Melton-Celsa AR, Kokai-Kun JF, O'Brien AD. 2002. Activation of Shiga toxin type 2d (Stx2d) by elastase involves cleavage of the C-terminal two amino acids of the A2 peptide in the context of the appropriate B pentamer. Mol. Microbiol. 43:207-215. (Pubitemid 34212202)
38. Melton-Celsa AR, O'Brien AD. 1998. Structure, biology, and relative toxicity of Shiga toxin family members for cells and animals, p 121-128. In Escherichia coli O157:H7 and other Shiga toxin-producing E. coli strains. American Society for Microbiology, Washington, DC.
39. Meyer T, Karch H, Hacker J, Bocklage H, Heesemann J. 1992. Cloning and sequencing of a Shiga-like toxin II-related gene from Escherichia coli O157:H7 strain 7279. Zentralbl. Bakteriol. 276:176-188.
40. Muniesa M, et al. 2004. Diversity of stx2 converting bacteriophages induced from Shiga-toxin-producing Escherichia coli strains isolated from cattle. Microbiology 150:2959-2971. (Pubitemid 39317797)
41. Muniesa M, Recktenwald J, Bielaszewská M, Karch H, Schmidt H. 2000. Characterization of a Shiga toxin 2e-converting bacteriophage from an Escherichia coli strain of human origin. Infect. Immun. 68:4850-4855.
42. O'Brien AD, Karmali MA, Scotland SM. 1994. A proposal for rationalization of the Escherichia coli cytotoxins, p 147-149. In Recent advances in verocytotoxin-producing Escherichia coli infections, Elsevier Science, B. V., Amsterdam, Netherlands.
43. O'Brien AD, et al. 1984. Shiga-like toxin-converting phages from Escherichia coli strains that cause hemorrhagic colitis or infantile diarrhea. Science 226:694-696. (Pubitemid 15202147)
44. Ohmura-Hoshino M, et al. 2003. Genetic and immunological analysis of a novel variant of Shiga toxin 1 from bovine Escherichia coli strains and development of bead-ELISA to detect the variant toxin. Microbiol. Immunol. 47:717-725. (Pubitemid 37288248)
45. Ooka T, et al. 2012. Clinical significance of Escherichia albertii. Emerg. Infect. Dis. 18:488-492.
46. Ørskov F, Ørskov I. 1984. Serotyping of Escherichia coli. Methods Microbiol. 14:43-112.
47. Paton AW, Beutin L, Paton JC. 1995. Heterogeneity of the amino-acid sequences of Escherichia coli Shiga-like toxin type-I operons. Gene 153:71-74.
48. Paton AW, Paton JC, Goldwater PN, Heuzenroeder MW, Manning PA. 1993. Nucleotide sequence of a variant Shiga-like toxin type-I operon of Escherichia coli O111:H-. Gene 129:87-92. (Pubitemid 23208076)
49. Paton AW, Paton JC, Heuzenroeder MW, Goldwater PN, Manning PA. 1992. Cloning and nucleotide sequence of a variant Shiga-like toxin II gene from Escherichia coli OX3:H21 isolated from a case of sudden infant death syndrome. Microb. Pathog. 13:225-236.
50. Persson S, Olsen KEP, Ethelberg S, Scheutz F. 2007. Subtyping method for Escherichia coli Shiga toxin (verocytotoxin) 2 variants and correlations to clinical manifestations. J. Clin. Microbiol. 45:2020-2024. (Pubitemid 46933951)
51. Piérard D, Muyldermans G, Moriau L, Stevens D, Lauwers S. 1998. Identification of new verocytotoxin type 2 variant B-subunit genes in human and animal Escherichia coli isolates. J. Clin. Microbiol. 36:3317-3322. (Pubitemid 28476185)
52. Reischl U, et al. 2002. Real-time fluorescence PCR assays for detection and characterization of Shiga toxin, intimin, and enterohemolysin genes from Shiga toxin-producing Escherichia coli. J. Clin. Microbiol. 40:2555-2565. (Pubitemid 34747362)
53. Scheutz F. 1997. Vero cytotoxin producing Escherichia coli (VTEC) isolated from Danish patients. Statens Serum Institut, Copenhagen, Denmark.
54. Scheutz F, Beutin L, Piérard D, Smith HR. 2001. Nomenclature of verocytotoxins, p 447-452. In Verocytotoxigenic E. coli. Food & Nutrition Press, Inc., Trumbull, CT.
55. Scheutz F, Cheasty T, Woodward D, Smith HR. 2004. Designation of O174 and O175 to temporary O groups OX3 and OX7, and six new E. coli O groups that include verocytotoxin-producing E. coli (VTEC): O176, O177, O178, O179, O180 and O181. APMIS 112:569-584. (Pubitemid 40040184)
56. Scheutz F, Ethelberg S. 2008. Nordic Meeting on detection and surveillance of VTEC infections in humans. http://www.ssi.dk/English/ HealthdataandICT/National%20Reference%20Laboratories/~/media/Indhold/ EN%20-%20engelsk/Public%20Health/National%20Reference%20Laboratories/ Nordic%20VTEC%20Report.ashx.
57. Scheutz F, Morabito S, Tozzoli R, Caprioli A. 2012. Identification of three vtx1 and seven vtx2 subtypes of verocytotoxin encoding genes of Escherichia coli by conventional PCR amplification. http://www.ssi.dk/English/ HealthdataandICT/National%20Reference%20Laboratories/~/media/Indhold/ EN%20-%20engelsk/Public%20Health/National%20Reference%20Laboratories/ vtx%20detection%20%20subtyping%20protocol-EQA-2010-11-rev4.ashx.
58. Scheutz F, Strockbine NA. 2005. Escherichia. The gammaproteobacteria, p 607-624. In Bergey's manual of systematic bacteriology, Vol 2, Part B. Springer, New York, NY.
59. Schmidt H, et al. 2000. A new Shiga toxin 2 variant (Stx2f) from Escherichia coli isolated from pigeons. Appl. Environ. Microbiol. 66:1205-1208. (Pubitemid 30130048)
60. - strain E32511. Infect. Immun. 59:1065-1073.
61. Strockbine NA, Jackson MP, Sung LM, Holmes RK, O'Brien AD. 1988. Cloning and sequencing of the genes of Shiga toxin from Shigella dysenteriae type 1. J. Bacteriol. 170:1116-1122. (Pubitemid 18079057)
62. Thomas A, Smith HR, Willshaw GA, Rowe B. 1991. Non-radioactively labelled polynucleotide oligonucleotide DNA probes for selectively detecting Escherichia coli strains producing Vero cytotoxins VT1, VT2 and VT2 variant. Mol. Cell. Probes 5:129-135.
63. Weinstein DL, Jackson MP, Samuel JE, Holmes RK, O'Brien AD. 1988. Cloning and sequencing of a Shiga-like toxin type II variant from Escherichia coli strain responsible for edema disease of swine. J. Bacteriol. 170:4223-4230.
64. Willshaw GA, Smith HR, Scotland SM, Rowe B. 1985. Cloning of genes determining the production of Vero cytotoxin by Escherichia coli. J. Gen. Microbiol. 131:3047-3053. (Pubitemid 16202279)
65. Zhang W, Bielaszewská M, Friedrich AW, Kuczius T, Karch H. 2005. Transcriptional analysis of genes encoding Shiga toxin 2 and its variants in Escherichia coli. Appl. Environ. Microbiol. 71:558-561. (Pubitemid 40116316)
66. 1c) in Escherichia coli strains isolated from humans. J. Clin. Microbiol. 40:1441-1446.
67. Zhang WL, et al. 2007. Structural and functional differences between disease-associated genes of enterohaemorrhagic Escherichia coli O111. Int. J. Med. Microbiol. 297:17-26.
68. Ziebell KA, Read SC, Johnson RP, Gyles CL. 2002. Evaluation of PCR and PCR-RFLP protocols for identifying Shiga toxins. Res. Microbiol. 153:289-300. (Pubitemid 34626787)