1887

Chapter 2 : Taxonomy Meets Public Health: The Case of Shiga Toxin-Producing

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in
Zoomout

Taxonomy Meets Public Health: The Case of Shiga Toxin-Producing , Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818791/9781555818784_Chap02-1.gif /docserver/preview/fulltext/10.1128/9781555818791/9781555818784_Chap02-2.gif

Abstract:

The term enteropathogenic was originally used to refer to strains belonging to a limited number of O groups epidemiologically associated with infantile diarrhea ( ). Subsequently, strains isolated from intestinal diseases have been grouped into at least six main categories on the basis of epidemiological evidence, phenotypic traits, clinical features of the disease they produce, and specific virulence factors. The well-described intestinal pathotypes or categories of diarrheagenic groups are enteropathogenic (EPEC), Shiga toxin-producing (STEC) or verocytotoxin-producing (VTEC) (including enterohemorrhagic [EHEC]), enterotoxigenic (ETEC), enteroaggregative (EAEC), enteroinvasive , and diffusely adherent . The general definition of an pathotype as “a group of strains of a single species that cause a common disease using a common set of virulence factors” ( ) has been further refined for STEC to help assess the clinical and public health risks associated with different STEC strains ( ). An empirical classification scheme was used to classify STEC serotypes into five “seropathotypes” (A through E) according to the reported association of serotypes with human intestinal disease, outbreaks, and hemolytic-uremic syndrome (HUS) ( ). This classification system uses a gradient ranging from seropathotype A (high risk) to seropathotypes D and E (minimal risk). This definition has been of considerable value in cases of human infection but is also problematic because the majority of isolates from STEC infections are not fully characterized and coupled to reliable clinical information. Although the definition of HUS is distinct, the spectrum of diarrheal disease varies considerably and may include a range of symptoms from nonbloody to scanty blood to true hemorrhagic colitis. Additionally, the use of A through E adds confusion because Shiga toxin subtypes are also named alphabetically. Most importantly, the concept of (sero)-pathotypes collides with the requirements of a good taxonomy, which separates elements of each group into subgroups that are mutually exclusive, unambiguous, and, together, include all possibilities. In practice, a good taxonomy should be simple to apply, easy to remember, and easy to use. The need to define human pathogenic STEC and to identify factors of STEC that absolutely predict the potential to cause human disease is obvious in terms of clinical management, supportive or antibiotic treatment, quarantine measurements, risk assessment, surveillance, and outbreak investigations and management. This chapter presents a brief history of the concept of pathotypes and describes the possible alternatives for categorizing STEC based on phenotypic or molecular typing.

Citation: Scheutz F. 2015. Taxonomy Meets Public Health: The Case of Shiga Toxin-Producing , p 17-36. In Sperandio V, Hovde C (ed), Enterohemorrhagic and Other Shiga Toxin-Producing . ASM Press, Washington, DC. doi: 10.1128/microbiolspec.EHEC-0019-2013
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1
Figure 1

Stx subtypes and variants. Parsimony tree of 107 variants: nine variants of Stx1a (including Shiga toxin from ), four variants of Stx1c, one variant of Stx1d, and subtypes of Stx2, including 21 Stx2a, 16 Stx2b, 18 Stx2c, 18 Stx2d, 14 Stx2e, two Stx2f, and four Stx2g variants. Data from reference and updated by the author.

Citation: Scheutz F. 2015. Taxonomy Meets Public Health: The Case of Shiga Toxin-Producing , p 17-36. In Sperandio V, Hovde C (ed), Enterohemorrhagic and Other Shiga Toxin-Producing . ASM Press, Washington, DC. doi: 10.1128/microbiolspec.EHEC-0019-2013
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Stx bacteriophage insertion sites in LEE-positive STEC include , , , , , , , and . Data from references , and . In LEE-negative STEC genomes additional insertion sites are often different and include , , , , and . Data from references , and . Big circles indicate the preferred bacteriophage integration site.

Citation: Scheutz F. 2015. Taxonomy Meets Public Health: The Case of Shiga Toxin-Producing , p 17-36. In Sperandio V, Hovde C (ed), Enterohemorrhagic and Other Shiga Toxin-Producing . ASM Press, Washington, DC. doi: 10.1128/microbiolspec.EHEC-0019-2013
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555818791.chap2
1. Neter E,, Westphal O,, Lüderitz O,, Gino RM,, Gorzynski EA . 1955. Demonstration of antibodies against enteropathogenic Escherichia coli in sera of children of various ages. Pediatrics 16 : 801 807.[PubMed]
2. Kaper JB,, Nataro JP,, Mobley HL . 2004. Pathogenic Escherichia coli . Nat Rev Microbiol 2 : 123 140.[PubMed] [CrossRef]
3. Karmali MA,, Mascarenhas M,, Shen S,, Ziebell KA,, 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.[PubMed] [CrossRef]
4. Konowalchuk J,, Speirs JI,, Stavric S . 1977. Vero response to a cytotoxin of Escherichia coli . Infect Immun 18 : 775 779.[PubMed]
5. O’Brien AD,, LaVeck GD,, Thompson MR,, Formal SB . 1982. Production of Shigella dysenteria type 1-like cytotoxin by Escherichia coli . J Infect Dis 146 : 763 769.[PubMed] [CrossRef]
6. O’Brien AD,, La Veck GF . 1983. Purification and characterization of a Shigella dysenteria 1-like toxin produced by Escherichia coli . Infect Immun 40 : 675 683.[PubMed]
7. Karmali MA,, Petric M,, Louie S,, Cheung R . 1986. Antigenic heterogeneity of Escherichia coli verotoxins. Lancet i : 164 165.[PubMed] [CrossRef]
8. Scotland SM,, Smith HR,, Rowe B . 1985. Two distinct toxins active on Vero cells from Escherichia coli O157. Lancet ii : 885 886.[PubMed] [CrossRef]
9. O’Brien AD,, Newland JW,, Miller SF,, Holmes RK,, Smith HW,, Formal SB . 1984. Shiga-like toxin-converting phages from Escherichia coli strains that cause hemorrhagic colitis or infantile diarrhea. Science 226 : 694 696.[PubMed] [CrossRef]
10. Scotland SM,, Smith HR,, Willshaw GA,, Rowe B . 1983. Vero cytotoxin production in strain of Escherichia coli is determined by genes carried on bacteriophage. Lancet ii : 216. (Letter).[PubMed] [CrossRef]
11. Smith HR,, Day NP,, Scotland SM,, Gross RJ,, Rowe B . 1984. Phage-determined production of Vero cytotoxin in strains of Escherichia coli serogroup O157. Lancet i : 1242 1243. (Letter).[PubMed] [CrossRef]
12. Smith HW,, Green P,, Parsell Z . 1983. Vero cell toxins in Escherichia coli and related bacteria: transfer by phage and conjugation and toxic action in laboratory animals, chickens and pigs. J Gen Microbiol 129 : 3121 3137.[PubMed]
13. Riley LW,, Remis RS,, Helgerson SD,, McGee HB,, Wells JG,, Davis BR,, Herbert RJ,, Olcott ES,, Johnson LM,, Hargret NT,, Blake PA,, Cohen ML . 1983. Hemorrhagic colitis associated with a rare Escherichia coli serotype. N Engl J Med 308 : 681 685.[PubMed] [CrossRef]
14. Johnson WM,, Lior H,, Bezanson GS . 1983. Cytotoxic Escherichia coli O157:H7 associated with hemorrhagic colitis in Canada. Lancet i : 76. [PubMed] [CrossRef]
15. O’Brien AD,, Lively TA,, Chen ME,, Rothman SW,, Formal SB . 1983. Escherichia coli O157:H7 strains associated with haemorrhagic colitis in the United States produce a Shigella dysenteriae 1 (Shiga) like cytotoxin. Lancet i : 702. [PubMed] [CrossRef]
16. Karmali MA,, Steele BT,, Petric M,, Lim CB . 1983. Sporadic cases of haemolytic-uraemic syndrome associated with faecal cytotoxin and cytotoxin-producing Escherichia coli in stools. Lancet i : 619 620.[PubMed] [CrossRef]
17. Karmali MA,, Petric M,, Lim C,, Fleming PC,, Steele BT . 1983. Escherichia coli cytotoxin haemolytic-uraemic syndrome, and haemorrhagic colitis. Lancet ii : 1299 1300.[CrossRef]
18. Levine MM,, Edelman R . 1984. Enteropathogenic Escherichia coli of classic serotypes associated with infant diarrhea: epidemiology and pathogenesis. Epidemiol Rev 6 : 31 51.[PubMed]
19. Levine MM,, Xu J-G,, Kaper JB,, Lior H,, Prado V,, Nataro JP,, Karch H,, Wachsmuth IK . 1987. 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 156 : 175 182.[PubMed] [CrossRef]
20. Wade WG,, Thom BT,, Evans N . 1979. Cytotoxic enteropathogenic Escherichia coli . Lancet ii : 1235 1236.[PubMed] [CrossRef]
21. Scotland SM,, Day NP,, Willshaw GA,, Rowe B . 1980. Cytotoxic enteropathogenic Escherichia coli . Lancet 1 : 90. [PubMed] [CrossRef]
22. Scheutz F,, Strockbine NA, . 2005. Escherichia , p 607 624. In Garrity GM,, Brenner DJ,, Krieg NR,, Staley JT (ed), Bergey’s Manual of Systematic Bacteriology, vol 2, part B, The Gammaproteobacteria. Springer, New York, NY.
23. Bosilevac JM,, Koohmaraie M . 2011. Prevalence and characterization of non-O157 Shiga toxin-producing Escherichia coli isolates from commercial ground beef in the United States. Appl Environ Microbiol 77 : 2103 2112.[PubMed] [CrossRef]
24. Buvens G,, Pierard D . 2012. Virulence profiling and disease association of verocytotoxin-producing Escherichia coli O157 and non-O157 isolates in Belgium. Foodborne Pathog Dis 9 : 530 535.[PubMed] [CrossRef]
25. EFSA Panel on Biological Hazards (BIOHAZ) . 2013. Scientific opinion on VTEC-seropathotype and scientific criteria regarding pathogenicity assessment. EFSA J 11 : 3138. 1106. 7-3-2013. European Food Safety Authority, Parma, Italy.
26. Centers for Disease Control and Prevention . 1995. Outbreak of acute gastroenteritis attributable to Escherichia coli serotype O104:H21—Helena, Montana. Morb Mortal Wkly Rep 44 : 501503.[PubMed]
27. Paton AW,, Woodrow MC,, Doyle RM,, Lanser JA,, Paton JC . 1999. Molecular characterization of a Shiga toxigenic Escherichia coli O113:H21 strain lacking eae responsible for a cluster of cases of hemolytic-uremic syndrome. J Clin Microbiol 37 : 3357 3361.[PubMed]
28. Mora A,, Herrera A,, Lopez C,, Dahbi G,, Mamani R,, Pita JM,, Alonso MP,, Llovo J,, Bernardez MI,, Blanco JE,, Blanco M,, Blanco J . 2011. Characteristics of the Shiga-toxin-producing enteroaggregative Escherichia coli O104:H4 German outbreak strain and of STEC strains isolated in Spain. Int Microbiol 14 : 121 141.[PubMed]
29. European Food Safety Authority and European Centre for Disease Prevention and Control . 2013. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2011. EFSA J 11 : 3129. 1250. 4-9-2013. European Food Safety Authority, Parma, Italy.
30. Kawano K,, Okada M,, Haga T,, Maeda K,, Goto Y . 2008. Relationship between pathogenicity for humans and stx genotype in Shiga toxin-producing Escherichia coli serotype O157. Eur J Clin Microbiol Infect Dis 27 : 227 232.[PubMed] [CrossRef]
31. Pai CH,, Ahmed N,, Lior H,, Johnson WM,, Sims HV,, Woods DE . 1988. Epidemiology of sporadic diarrhea due to verocytotoxin-producing Escherichia coli: a two-year prospective study. J Infect Dis 157 : 1054 1057.[PubMed] [CrossRef]
32. Boerlin P,, Mcewen SA,, Boerlin-Petzold F,, Wilson JB,, Johnson RP,, Gyles CL . 1999. Associations between virulence factors of Shiga toxin-producing Escherichia coli and disease in humans. J Clin Microbiol 37 : 497 503.[PubMed]
33. Gyles CL . 2007. Shiga toxin-producing Escherichia coli: an overview. J Anim Sci 85 : E45 E62. [PubMed] [CrossRef]
34. Ethelberg S,, Olsen KEP,, Scheutz F,, Jensen C,, Schiellerup P,, Engberg J,, Petersen AM,, Olesen B,, Gerner-Smidt P,, Mølbak K . 2004. Virulence factors for hemolytic uremic syndrome, Denmark. Emerg Infect Dis 10 : 842 847.[PubMed] [CrossRef]
35. Cookson AL,, Bennett J,, Thomson-Carter F,, Attwood GT . 2007. Molecular subtyping and genetic analysis of the enterohemolysin gene ( ehxA) from Shiga toxin-producing Escherichia coli and atypical enteropathogenic E. coli . Appl Environ Microbiol 73 : 6360 6369.[PubMed] [CrossRef]
36. Schmidt H,, Karch H . 1996. Enterohemolytic phenotypes and genotypes of Shiga toxin-producing Escherichia coli O111 strains from patients with diarrhea and hemolytic-uremic syndrome. J Clin Microbiol 34 : 2364 2367.[PubMed]
37. Mundy R,, Jenkins C,, Yu J,, Smith H,, Frankel G . 2004. Distribution of espI among clinical enterohaemorrhagic and enteropathogenic Escherichia coli isolates. J Med Microbiol 53 : 1145 1149.[PubMed] [CrossRef]
38. Bettelheim KA . 2007. The non-O157 shiga-toxigenic (verocytotoxigenic) Escherichia coli; under-rated pathogens. Crit Rev Microbiol 33 : 67 87.[PubMed] [CrossRef]
39. Lukjancenko O,, Wassenaar TM,, Ussery DW . 2010. Comparison of 61 sequenced Escherichia coli genomes. Microb Ecol 60 : 708 720.[PubMed] [CrossRef]
40. Mellmann A,, Harmsen D,, Cummings CA,, Zentz EB,, Leopold SR,, Rico A,, Prior K,, Szczepanowski R,, Ji Y,, Zhang W,, McLaughlin SF,, Henkhaus JK,, Leopold B,, Bielaszewska M,, Prager R,, Brzoska PM,, Moore RL,, Guenther S,, Rothberg JM,, Karch H . 2011. Prospective genomic characterization of the German enterohemorrhagic Escherichia coli O104:H4 outbreak by rapid next generation sequencing technology. PloS One 6 : e22751. [PubMed] [CrossRef]
41. Kim J,, Nietfeldt J,, Benson AK . 1999. Octamer-based genome scanning distinguishes a unique subpopulation of Escherichia coli O157:H7 strains in cattle. Proc Natl Acad Sci USA 96 : 13288 13293.[PubMed] [CrossRef]
42. Yang Z,, Kovar J,, Kim J,, Nietfeldt J,, Smith DR,, Moxley RA,, Olson ME,, Fey PD,, Benson AK . 2004. Identification of common subpopulations of non-sorbitol-fermenting, beta-glucuronidase-negative Escherichia coli O157:H7 from bovine production environments and human clinical samples. Appl Environ Microbiol 70 : 6846 6854.[PubMed] [CrossRef]
43. Zhang Y,, Laing C,, Steele M,, Ziebell K,, Johnson R,, Benson AK,, Taboada E,, Gannon VP . 2007. Genome evolution in major Escherichia coli O157:H7 lineages. BMC Genomics 8 : 121. [PubMed] [CrossRef]
44. Bono JL,, Smith TP,, Keen JE,, Harhay GP,, McDaneld TG,, Mandrell RE,, Jung WK,, Besser TE,, Gerner-Smidt P,, Bielaszewska M,, Karch H,, Clawson ML . 2012. Phylogeny of Shiga toxin-producing Escherichia coli O157 isolated from cattle and clinically ill humans. Mol Biol Evol 29 : 2047 2062.[PubMed] [CrossRef]
45. Manning SD,, Motiwala AS,, Springman AC,, Qi W,, Lacher DW,, Ouellette LM,, Mladonicky JM,, Somsel P,, Rudrik JT,, Dietrich SE,, Zhang W,, Swaminathan B,, Alland D,, Whittam TS . 2008. Variation in virulence among clades of Escherichia coli O157:H7 associated with disease outbreaks. Proc Natl Acad Sci USA 105 : 4868 4873.[PubMed] [CrossRef]
46. Centers for Disease Control and Prevention . 2006. Ongoing multistate outbreak of Escherichia coli serotype O157:H7 infections associated with consumption of fresh spinach—United States, September 2006. Morb Mortal Wkly Rep 55 : 10451046.[PubMed]
47. Grant J,, Wendelboe AM,, Wendel A,, Jepson B,, Torres P,, Smelser C,, Rolfs RT . 2008. Spinach-associated Escherichia coli O157:H7 outbreak, Utah and New Mexico, 2006. Emerg Infect Dis 14 : 1633 1636.[PubMed] [CrossRef]
48. Abu-Ali GS,, Ouellette LM,, Henderson ST,, Whittam TS,, Manning SD . 2010. Differences in adherence and virulence gene expression between two outbreak strains of enterohaemorrhagic Escherichia coli O157:H7. Microbiology 156 : 408 419.[PubMed] [CrossRef]
49. Whittam TS, . 1998. Evolution of Eschericia coli O157:H7 and other Siga toxin-producing E. coli strains, p 195 209. In Kaper JB,, O’Brien AD (ed), Escherichia coli O157:H7 and Other Shiga Toxin-Producing E. coli. Strains, 1st ed. ASM Press, Washington, DC.
50. Tarr CL,, Large TM,, Moeller CL,, Lacher DW,, Tarr PI,, Acheson DW,, Whittam TS . 2002. Molecular characterization of a serotype O121:H19 clone, a distinct Shiga toxin-producing clone of pathogenic Escherichia coli . Infect Immun 70 : 6853 6859.[PubMed] [CrossRef]
51. Abu-Ali GS,, Lacher DW,, Wick LM,, Qi W,, Whittam TS . 2009. Genomic diversity of pathogenic Escherichia coli of the EHEC 2 clonal complex. BMC Genomics 10 : 296. [PubMed] [CrossRef]
52. Hazen TH,, Sahl JW,, Fraser CM,, Donnenberg MS,, Scheutz F,, Rasko DA . 2013. Refining the pathovar paradigm via phylogenomics of the attaching and effacing Escherichia coli . Proc Natl Acad Sci USA 110 : 12810 12815.[PubMed] [CrossRef]
53. Steyert SR,, Sahl JW,, Fraser CM,, Teel LD,, Scheutz F,, Rasko DA . 2012. Comparative genomics and stx phage characterization of LEE-negative Shiga toxin-producing Escherichia coli . Front Cell Infect Microbiol 2 : 133. [PubMed] [CrossRef]
54. Scheutz F,, Teel LD,, Beutin L,, Pierard D,, Buvens G,, Karch H,, Mellmann A,, Caprioli A,, Tozzoli R,, Morabito S,, Strockbine NA,, Melton-Celsa AR,, Sanchez M,, Persson S,, O’Brien AD . 2012. Multicenter evaluation of a sequence-based protocol for subtyping shiga toxins and standardizing Stx nomenclature. J Clin Microbiol 50 : 2951 2963.[PubMed] [CrossRef]
55. Asakura H,, Makino SI,, Kobori H,, Watarai M,, Shirahata T,, Ikeda T,, Takeshi K . 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.[PubMed] [CrossRef]
56. 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.[PubMed] [CrossRef]
57. De Baets L,, Van der Taelen I,, De Filette M,, Piérard D,, Allison L,, De Greve H,, Hernalsteens JP,, Imberechts H . 2004. Genetic typing of shiga toxin 2 variants of Escherichia coli by PCR-restriction fragment length polymorphism analysis. Appl Environ Microbiol 70 : 6309 6314.[PubMed] [CrossRef]
58. 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.[PubMed]
59. Lee JE,, Reed J,, Shields MS,, Spiegel KM,, Farrell LD,, Sheridan PP . 2007. Phylogenetic analysis of Shiga toxin 1 and Shiga toxin 2 genes associated with disease outbreaks. BMC Microbiol 7 : 109. [PubMed] [CrossRef]
60. 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.[PubMed]
61. 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.[PubMed] [CrossRef]
62. Friedrich AW,, Bielaszewská M,, Zhang WL,, Pulz M,, Kuczius T,, Ammon A,, Karch H . 2002. Escherichia coli harboring Shiga toxin 2 gene variants: frequency and association with clinical symptoms. J Infect Dis 185 : 74 84.[PubMed] [CrossRef]
63. 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.[PubMed] [CrossRef]
64. Eklund M,, Leino K,, Siitonen A . 2002. Clinical Escherichia coli strains carrying stx genes: stx variants and stx-positive virulence profiles. J Clin Microbiol 40 : 4585 4593.[PubMed] [CrossRef]
65. Pedersen MG,, Hansen C,, Riise E,, Persson S,, Olsen KE . 2008. Subtype-specific suppression of Shiga toxin 2 released from Escherichia coli upon exposure to protein synthesis inhibitors. J Clin Microbiol 46 : 2987 2991.[PubMed] [CrossRef]
66. Rivas M,, Miliwebsky E,, Chinen I,, Roldan CD,, Balbi L,, Garcia B,, Fiorilli G,, Sosa-Estani S,, Kincaid J,, Rangel J,, Griffin PM . 2006. Characterization and epidemiologic subtyping of Shiga toxin-producing Escherichia coli strains isolated from hemolytic uremic syndrome and diarrhea cases in Argentina. Foodborne Pathog Dis 3 : 88 96.[PubMed] [CrossRef]
67. Bonnet R,, Souweine B,, Gauthier G,, Rich C,, Livrelli V,, Sirot J,, Joly B,, Forestier C . 1998. Non-O157:H7 Stx2-producing Escherichia coli strains associated with sporadic cases of hemolytic-uremic syndrome in adults. J Clin Microbiol 36 : 1777 1780.[PubMed]
68. Keskimäki M,, Ikaheimo R,, Karkkainen P,, Scheutz F,, Ratiner Y,, Puohiniemi R,, Siitonen A . 1997. Shiga toxin-producing Escherichia coli serotype OX3:H21 as a cause of hemolytic-uremic syndrome. Clin Infect Dis 24 : 1278 1279.[PubMed] [CrossRef]
69. Keskimäki M,, Ratiner Y,, Oinonen S,, Leijala E,, Nurminen M,, Saari M,, Siitonen A . 1999. Haemolytic-uraemic syndrome caused by vero toxin-producing Escherichia coli serotype Rough:K-:H49. Scand J Infect Dis 31 : 141 144.[PubMed] [CrossRef]
70. Rasko DA,, Webster DR,, Sahl JW,, Bashir A,, Boisen N,, Scheutz F,, Paxinos EE,, Sebra R,, Chin CS,, Iliopoulos D,, Klammer A,, Peluso P,, Lee L,, Kislyuk AO,, Bullard J,, Kasarskis A,, Wang S,, Eid J,, Rank D,, Redman JC,, Steyert SR,, Frimodt-Moller J,, Struve C,, Petersen AM,, Krogfelt KA,, Nataro JP,, Schadt EE,, Waldor MK . 2011. Origins of the E. coli strain causing an outbreak of hemolytic-uremic syndrome in Germany. N Engl J Med 365 : 709 717.[PubMed] [CrossRef]
71. Fuller CA,, Pellino CA,, Flagler MJ,, Strasser JE,, Weiss AA . 2011. Shiga toxin subtypes display dramatic differences in potency. Infect Immun 79 : 1329 1337.[PubMed] [CrossRef]
72. Baker DR,, Moxley RA,, Steele MB,, LeJeune JT,, Christopher-Hennings J,, Chen DG,, Hardwidge PR,, Francis DH . 2007. Differences in virulence among Escherichia coli O157:H7 strains isolated from humans during disease outbreaks and from healthy cattle. Appl Environ Microbiol 73 : 7338 7346.[PubMed] [CrossRef]
73. Zhang Y,, Laing C,, Zhang Z,, Hallewell J,, You C,, Ziebell K,, Johnson RP,, Kropinski AM,, Thomas JE,, Karmali M,, Gannon VP . 2010. Lineage and host source are both correlated with levels of Shiga toxin 2 production by Escherichia coli O157:H7 strains. Appl Environ Microbiol 76 : 474 482.[PubMed] [CrossRef]
74. Neupane M,, Abu-Ali GS,, Mitra A,, Lacher DW,, Manning SD,, Riordan JT . 2011. Shiga toxin 2 overexpression in Escherichia coli O157:H7 strains associated with severe human disease. Microb Pathog 51 : 466 470.[PubMed] [CrossRef]
75. Uhlich GA,, Sinclair JR,, Warren NG,, Chmielecki WA,, Fratamico P . 2008. Characterization of Shiga toxin-producing Escherichia coli isolates associated with two multistate food-borne outbreaks that occurred in 2006. Appl Environ Microbiol 74 : 1268 1272.[PubMed] [CrossRef]
76. Søborg B,, Lassen SG,, Muller L,, Jensen T,, Ethelberg S,, Molbak K,, Scheutz F . 2013. A verocytotoxin-producing E. coli outbreak with a surprisingly high risk of haemolytic uraemic syndrome, Denmark, September–October 2012. Euro Surveill 18 : ii, 20350. [PubMed]
77. Shringi S,, Garcia A,, Lahmers KK,, Potter KA,, Muthupalani S,, Swennes AG,, Hovde CJ,, Call DR,, Fox JG,, Besser TE . 2012. Differential virulence of clinical and bovine-biased enterohemorrhagic Escherichia coli O157:H7 genotypes in piglet and Dutch belted rabbit models. Infect Immun 80 : 369 380.[PubMed] [CrossRef]
78. Kawano K,, Ono H,, Iwashita O,, Kurogi M,, Haga T,, Maeda K,, Goto Y . 2012. stx genotype and molecular epidemiological analyses of Shiga toxin-producing Escherichia coli O157:H7/H- in human and cattle isolates. Eur J Clin Microbiol Infect Dis 31 : 119 127.[PubMed] [CrossRef]
79. Nishikawa Y,, Zhou Z,, Hase A,, Ogasawara J,, Cheasty T,, Haruki K . 2000. Relationship of genetic type of shiga toxin to manifestation of bloody diarrhea due to enterohemorrhagic Escherichia coli serogroup O157 isolates in Osaka City, Japan. J Clin Microbiol 38 : 2440 2442.[PubMed]
80. Orth D,, Grif K,, Khan AB,, Naim A,, Dierich MP,, Wurzner R . 2007. The Shiga toxin genotype rather than the amount of Shiga toxin or the cytotoxicity of Shiga toxin in vitro correlates with the appearance of the hemolytic uremic syndrome. Diagn Microbiol Infect Dis 59 : 235 242.[PubMed] [CrossRef]
81. Mariani-Kurkdjian P,, Denamur E,, Milon A,, Picard B,, Cave H,, Lambert-Zechovsky N,, Loirat C,, Goullet P,, Sansonetti PJ,, Elion J . 1993. Identification of a clone of Escherichia coli O103:H2 as a potential agent of hemolytic-uremic syndrome in France. J Clin Microbiol 31 : 296 301.[PubMed]
82. 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.[PubMed] [CrossRef]
84. Franke S,, Harmsen D,, Caprioli A,, Piérard D,, Wieler LH,, Karch H . 1995. Clonal relatedness of Shiga-like toxin-producing Escherichia coli O101 strains of human and porcine origin. J Clin Microbiol 33 : 3174 3178.[PubMed]
85. Ogura Y,, Ooka T,, Asadulghani,, Terajima J,, Nougayrede JP,, Kurokawa K,, Tashiro K,, Tobe T,, Nakayama K,, Kuhara S,, Oswald E,, Watanabe H,, Hayashi T . 2007. Extensive genomic diversity and selective conservation of virulence-determinants in enterohemorrhagic Escherichia coli strains of O157 and non-O157 serotypes. Genome Biol 8 : R138. [PubMed] [CrossRef]
86. Ogura Y,, Ooka T,, Iguchi A,, Toh H,, Asadulghani M,, Oshima K,, Kodama T,, Abe H,, Nakayama K,, Kurokawa K,, Tobe T,, Hattori M,, Hayashi T . 2009. Comparative genomics reveal the mechanism of the parallel evolution of O157 and non-O157 enterohemorrhagic Escherichia coli . Proc Natl Acad Sci USA 106 : 17939 17944.[PubMed] [CrossRef]
87. Shringi S,, Schmidt C,, Katherine K,, Brayton KA,, Hancock DD,, Besser TE . 2012. Carriage of stx2a differentiates clinical and bovine-biased strains of Escherichia coli O157. PLoS One 7: e51572. doi:10.1371/journal.pone.0051572.[PubMed] [CrossRef]
88. Garcia-Aljaro C,, Muniesa M,, Jofre J,, Blanch AR .. 2009. Genotypic and phenotypic diversity among induced, stx2-carrying bacteriophages from environmental Escherichia coli strains. Appl Environ Microbiol 75 : 329 336.[PubMed] [CrossRef]
89. Serra-Moreno R,, Jofre J,, Muniesa M . 2007. Insertion site occupancy by stx 2 bacteriophages depends on the locus availability of the host strain chromosome. J Bacteriol 189 : 6645 6654.[PubMed] [CrossRef]
90. Shringi S,, Schmidt C,, Katherine K,, Brayton KA,, Hancock DD,, Besser TE . 2012. Carriage of stx2a differentiates clinical and bovine-biased strains of Escherichia coli O157. PLoS One 7 : e51572. doi:10.1371/journal.pone.0051572.[PubMed] [CrossRef]
91. Clawson ML,, Keen JE,, Smith TP,, Durso LM,, McDaneld TG,, Mandrell RE,, Davis MA,, Bono JL .. 2009. Phylogenetic classification of Escherichia coli O157:H7 strains of human and bovine origin using a novel set of nucleotide polymorphisms. Genome Biol 10 : R56. [PubMed] [CrossRef]
92. Brüssow H,, Canchaya C,, Hardt WD . 2004. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68 : 560 602.[PubMed] [CrossRef]
93. Herold S,, Karch H,, Schmidt H . 2004. Shiga toxin-encoding bacteriophages—genomes in motion. Int J Med Microbiol 294 : 115 121.[PubMed] [CrossRef]
94. Waldor MK,, Friedman DI . 2005. Phage regulatory circuits and virulence gene expression. Curr Opin Microbiol 8 : 459 465. [PubMed] [CrossRef]
95. Wagner PL,, Neely MN,, Zhang XP,, Acheson DWK,, Waldor MK,, Friedman DI . 2001. Role for a phage promoter in Shiga toxin 2 expression from a pathogenic Escherichia coli strain. J Bacteriol 183 : 2081 2085.[PubMed] [CrossRef]
96. Fortier LC,, Sekulovic O . 2013. Importance of prophages to evolution and virulence of bacterial pathogens. Virulence 4: 354 365.[PubMed] [CrossRef]
97. Wagner PL,, Livny J,, Neely MN,, Acheson DW,, Friedman DI,, Waldor MK . 2002. Bacteriophage control of Shiga toxin 1 production and release by Escherichia coli . Mol Microbiol 44 : 957 970.[PubMed] [CrossRef]
98. Plunkett G,, Rose DJ,, Durfee TJ,, Blattner FR . 1999. Sequence of Shiga toxin 2 phage 933W from Escherichia coli O157:H7: Shiga toxin as a phage late-gene product. J Bacteriol 181 : 1767 1778.[PubMed]
99. Guo HC,, Kainz M,, Roberts JW . 1991. Characterization of the late-gene regulatory region of phage 21. J Bacteriol 173 : 1554 1560.[PubMed]
100. Strauch E,, Schaudinn C,, Beutin L . 2004. First-time isolation and characterization of a bacteriophage encoding the Shiga toxin 2c variant, which is globally spread in strains of Escherichia coli O157. Infect Immun 72 : 7030 7039.[PubMed] [CrossRef]
101. Strauch E,, Hammerl JA,, Konietzny A,, Schneiker-Bekel S,, Arnold W,, Goesmann A,, Puhler A,, Beutin L . 2008. Bacteriophage 2851 is a prototype phage for dissemination of the Shiga toxin variant gene 2c in Escherichia coli O157:H7. Infect Immun 76 : 5466 5477.[PubMed] [CrossRef]
102. Makino K,, Yokoyama K,, Kubota Y,, Yutsudo CH,, Kimura S,, Kurokawa K,, Ishii K,, Hattori M,, Tatsuno I,, Abe H,, Iida T,, Yamamoto K,, Onishi M,, Hayashi T,, Yasunaga T,, Honda T,, Sasakawa C,, Shinagawa H . 1999. Complete nucleotide sequence of the prophage VT2-Sakai carrying the verotoxin 2 genes of the enterohemorrhagic Escherichia coli O157:H7 derived from the Sakai outbreak. Genes Genet Syst 74 : 227 239.[PubMed] [CrossRef]
103. Yokoyama K,, Makino K,, Kubota Y,, Watanabe M,, Kimura S,, Yutsudo CH,, Kurokawa K,, Ishii K,, Hattori M,, Tatsuno I,, Abe H,, Yoh M,, Iida T,, Ohnishi M,, Hayashi T,, Yasunaga T,, Honda T,, Sasakawa C,, Shinagawa H . 2000. Complete nucleotide sequence of the prophage VT1-Sakai carrying the Shiga toxin 1 genes of the enterohemorrhagic Escherichia coli O157:H7 strain derived from the Sakai outbreak. Gene 258 : 127 139.[PubMed] [CrossRef]
104. Sato T,, Shimizu T,, Watarai M,, Kobayashi M,, Kano S,, Hamabata T,, Takeda Y,, Yamasaki S . 2003. Genome analysis of a novel Shiga toxin 1 (Stx1)-converting phage which is closely related to Stx2-converting phages but not to other Stx1-converting phages. J Bacteriol 185 : 3966 3971.[PubMed] [CrossRef]
105. Jacobsen A . 2012. M.Sc. thesis. Statens Serum Institut, Technical University of Denmark, Copenhagen, Denmark.
106. Perna NT,, Plunkett G 3rd,, Burland V,, Mau B,, Glasner JD,, Rose DJ,, Mayhew GF,, Evans PS,, Gregor J,, Kirkpatrick HA,, Posfai G,, Hackett J,, Klink S,, Boutin A,, Shao Y,, Miller L,, Grotbeck EJ,, Davis NW,, Lim A,, Dimalanta ET,, Potamousis KD,, Apodaca J,, Anantharaman TS,, Lin J,, Yen G,, Schwartz DC,, Welch RA,, Blattner FR . 2001. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409 : 529 533.[PubMed] [CrossRef]
107. Blanco M,, Blanco JE,, Dahbi G,, Alonso MP,, Mora A,, Coira MA,, Madrid C,, Juarez A,, Bernardez MI,, Gonzalez EA,, Blanco J . 2006. Identification of two new intimin types in atypical enteropathogenic Escherichia coli . Int Microbiol 9 : 103 110.[PubMed]
108. Garrido P,, Blanco M,, Moreno-Paz M,, Briones C,, Dahbi G,, Blanco J,, 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.[PubMed] [CrossRef]
109. Mora A,, Blanco M,, Yamamoto D,, Dahbi G,, Blanco JE,, Lopez C,, Alonso MP,, Vieira MA,, Hernandes RT,, Abe CM,, Piazza RM,, Lacher DW,, Elias WP,, Gomes TA,, Blanco J . 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.[PubMed]
110. Garmendia J,, Frankel G,, Crepin VF . 2005. Enteropathogenic and enterohemorrhagic Escherichia coli infections: translocation, translocation, translocation. Infect Immun 73 : 2573 2585.[PubMed] [CrossRef]
111. Bono JL,, Keen JE,, Clawson ML,, Durso LM,, Heaton MP,, Laegreid WW . 2007. Association of Escherichia coli O157:H7 tir polymorphisms with human infection. BMC Infect Dis 7 : 98. [PubMed] [CrossRef]
112. Haugum K,, Brandal LT,, Lobersli I,, Kapperud G,, Lindstedt BA . 2011. Detection of virulent Escherichia coli O157 strains using multiplex PCR and single base sequencing for SNP characterization. J Appl Microbiol 110 : 1592 1600.[PubMed] [CrossRef]
113. Badea L,, Doughty S,, Nicholls L,, Sloan J,, Robins-Browne RM,, Hartland EL . 2003. Contribution of Efa1/LifA to the adherence of enteropathogenic Escherichia coli to epithelial cells. Microb Pathog 34 : 205 215.[PubMed] [CrossRef]
114. Klapproth JA,, Scaletsky ICA,, McNamara BP,, Lai LC,, Malstrom C,, James SP,, Donnenberg MS . 2000. A large toxin from pathogenic Escherichia coli strains that inhibits lymphocyte activation. Infect Immun 68 : 2148 2155.[PubMed] [CrossRef]
115. Wickham ME,, Lupp C,, Mascarenhas M,, Vazquez A,, Coombes BK,, Brown NF,, Coburn BA,, Deng W,, Puente JL,, Karmali MA,, Finlay BB . 2006. Bacterial genetic determinants of non-O157 STEC outbreaks and hemolytic-uremic syndrome after infection. J Infect Dis 194 : 819 827.[PubMed] [CrossRef]
116. Newton HJ,, Pearson JS,, Badea L,, Kelly M,, Lucas M,, Holloway G,, Wagstaff KM,, Dunstone MA,, Sloan J,, Whisstock JC,, Kaper JB,, Robins-Browne RM,, Jans DA,, Frankel G,, Phillips AD,, Coulson BS,, Hartland EL . 2010. The type III effectors NleE and NleB from enteropathogenic E. coli and OspZ from Shigella block nuclear translocation of NF-kappaB p65. PLoS Pathog 6 : e1000898. doi:10.1371/journal.ppat.1000898 [doi]. [CrossRef]
117. Tree JJ,, Wolfson EB,, Wang D,, Roe AJ,, Gally DL . 2009. Controlling injection: regulation of type III secretion in enterohaemorrhagic Escherichia coli . Trends Microbiol 17 : 361 370.[PubMed] [CrossRef]
118. Shaikh N,, Tarr PI . 2003. Escherichia coli O157:H7 Shiga toxin-encoding bacteriophages: integrations, excisions, truncations, and evolutionary implications. J Bacteriol 185 : 3596 3605.[CrossRef]
119. Recktenwald J,, Schmidt H . 2002. The nucleotide sequence of Shiga toxin (Stx) 2e-encoding phage phiP27 is not related to other Stx phage genomes, but the modular genetic structure is conserved. Infect Immun 70 : 1896 1908.[CrossRef]

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error