Escherichia coli O157:H7 colonization in small domestic ruminants

FEMS Microbiology Reviews

Volumn 33, Issue 2, 2009, Pages 394-410

  La Ragione, Roberto M ^a   Best, Angus ^a   Woodward, Martin J ^a   Wales, Andrew D ^a  

^a VETERINARY LABORATORIES AGENCY   (United Kingdom)

Author keywords

Colonization; Escherichia coli O157:H7; Goats; Persistence; Sheep

Indexed keywords

BACTERIAL COLONIZATION; BOVIDS; CRYPTOSPORIDIUM; ESCHERICHIA COLI; FLAGELLUM; IMMUNOMAGNETIC SEPARATION; NONHUMAN; REVIEW;

ANIMALS; CATTLE; CATTLE DISEASES; DISEASE RESERVOIRS; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI O157; GOAT DISEASES; GOATS; HUMANS; RUMINANTS; SHEEP DISEASES; SHEEP, DOMESTIC;

BOS; BOVINAE; CAPRA HIRCUS; ESCHERICHIA COLI; OVIS ARIES;

EID: 60149090846     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1111/j.1574-6976.2008.00138.x     Document Type: Review

References (196)

1. Acres SD, Saunders JR Radostits OM (1977) Acute undifferentiated neonatal diarrhea of beef calves - prevalence of enterotoxigenic E. coli, reo-like (rota) virus and other enteropathogens in cow-calf herds. Can Vet J 18 : 113 121.
2. Agin TS, Cantey JR, Boedeker EC Wolf MK (1996) Characterisation of the eaeA gene from rabbit enteropathogenic Escherichia coli strain RDEC-1 and comparison to other eaeA genes from bacteria that cause attaching-effacing lesions. FEMS Microbiol Lett 144 : 249 258.
3. Aktan I, Sprigings KA, La Ragione RM, Faulkner LM, Paiba GA Woodward MJ (2004) Characterisation of attaching-effacing Escherichia coli isolated from animals at slaughter in England and Wales. Vet Microbiol 102 : 43 53.
4. Aktan I, La Ragione RM Woodward MJ (2007) Colonization, persistence, and tissue tropism of Escherichia coli O26 in conventionally reared weaned lambs. Appl Environ Microb 73 : 691 698.
5. Allen-Vercoe E Woodward MJ (1999) The role of flagella, but not fimbriae, in the adherence of Salmonella enterica serotype Enteritidis to chick gut explant. J Med Microbiol 48 : 771 780.
6. Allen-Vercoe E, Waddell B, Toh MC DeVinney R (2006) Amino acid residues within enterohemorrhagic Escherichia coli O157:H7 Tir involved in phosphorylation, alpha-actinin recruitment, and Nck-independent pedestal formation. Infect Immun 74 : 6196 6205.
7. Altmann K Mukkur TKS (1983) Passive immunization of neonatal lambs against infection with enteropathogenic Escherichia coli via colostrum of ewes immunized with crude and purified K99 pili. Res Vet Sci 35 : 234 239.
8. Angus KW, Tzipori S Gray EW (1982) Intestinal lesions in specific-pathogen-free lambs associated with a cryptosporidium from calves with diarrhea. Vet Pathol 19 : 67 78.
9. Anon (2007) Enter-Net Annual Report: 2005 - Surveillance of Enteric Pathogens in Europe and Beyond. Enter-net surveillance hub. HPA Centre for Infections, Colindale, London, UK.
10. 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 Microb 73 : 7338 7346.
11. Barlow AM, Wales AD, Burch AA, Woodward MJ Pearson GR (2004) Attaching and effacing lesions in the intestines of an adult goat associated with natural infection with Escherichia coli O145. Vet Rec 155 : 807 808.
12. Battisti A, Lovari S, Franco A, Di Egidio A, Tozzoli R, Caprioli A Morabito S (2006) Prevalence of Escherichia coli O157 in lambs at slaughter in Rome, central Italy. Epidemiol Infect 134 : 415 419.
13. Bäumler AJ, Tsolis RM Heffron F (1996) The lpf fimbrial operon mediates adhesion of Salmonella typhimurium to murine Peyer's patches. P Natl Acad Sci USA 93 : 279 283.
14. Berin MC, Darfeuille-Michaud A, Egan LJ, Miyamoto Y Kagnoff MF (2002) Role of EHEC O157:H7 virulence factors in the activation of intestinal epithelial cell NF-kappaB and MAP kinase pathways and the upregulated expression of interleukin 8. Cell Microbiol 4 : 635 648.
15. Besser RE, Lett SM, Weber JT, Doyle MP, Barrett TJ, Wells JG Griffin PM (1993) An outbreak of diarrhea and hemolytic uremic syndrome from Escherichia coli O157:H7 in fresh-pressed apple cider. JAMA 269 : 2217 2220.
16. Best A, La Ragione RM, Sayers AR Woodward MJ (2005) Role for flagella but not intimin in the persistent infection of the gastrointestinal tissues of specific-pathogen-free chicks by shiga toxin-negative Escherichia coli O157:H7. Infect Immun 73 : 1836 1846.
17. Best A, La Ragione RM, Clifford D, Cooley WA, Sayers AR Woodward MJ (2006) A comparison of Shiga-toxin negative Escherichia coli O157 aflagellate and intimin deficient mutants in porcine in vitro and in vivo models of infection. Vet Microbiol 113 : 63 72.
18. Best A, Clifford D, Crudgington B, Cooley WA, Nunez A, Carter B, Weyer U, Woodward MJ La Ragione RM (2008) Intermittent Escherichia coli O157:H7 colonisation at the terminal rectum mucosa of conventionally-reared lambs. Vet Res 40 : 09. DOI :.
19. Bielaszewska M, Janda J, Blahova K et al 1997) Human Escherichia coli O157:H7 infection associated with the consumption of unpasteurized goat's milk. Epidemiol Infect 119 : 299 305.
20. 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 1356.
21. Bonardi S, Foni E, Chiapponi C, Salsi A Brindani F (2007) Detection of verocytotoxin-producing Escherichia coli serogroups O157 and O26 in the cecal content and lymphatic tissue of cattle at slaughter in Italy. J Food Protect 70 : 1493 1497.
22. Bopp CA, Greene KD, Downes FP, Sowers EG, Wells JG Wachsmuth IK (1987) Unusual verotoxin-producing Escherichia coli associated with hemorrhagic colitis. J Clin Microbiol 25 : 1486 1489.
23. Borczyk AA, Karmali MA, Lior H Duncan LMC (1987) Bovine reservoir for verotoxin-producing Escherichia coli O157:H7. Lancet 1 : 98.
24. Bretschneider G, Berberov EM Moxley RA (2007) Reduced intestinal colonization of adult beef cattle by Escherichia coli O157:H7 tir deletion and nalidixic-acid-resistant mutants lacking flagellar expression. Vet Microbiol 125 : 381 386.
25. Campellone KG, Rankin S, Pawson T, Kirschner MW, Tipper DJ Leong JM (2004a) Clustering of Nck by a 12-residue Tir phosphopeptide is sufficient to trigger localized actin assembly. J Cell Biol 164 : 407 416.
26. Campellone KG, Robbins D Leong JM (2004b) EspF(U) is a translocated EHEC effector that interacts with Tir and N-WASP and promotes Nck-independent actin assembly. Dev Cell 7 : 217 228.
27. Centers for Disease Control and Prevention (2006) Annual listing of foodborne disease outbreaks, United States. Available at, accessed August 25, 2008.
28. Centers for Disease Control and Prevention (2008) Summary of notifiable diseases - United States, 2006. MMWR 55 : 1 94.
29. Cerqueira AMF, Guth BEC, Joaquim RM Andrade JRC (1999) High occurrence of Shiga toxin-producing Escherichia coli (STEC) in healthy cattle in Rio de Janeiro State, Brazil. Vet Microbiol 70 : 111 121.
30. Chapman PA, Siddons CA, Wright DJ, Norman P, Fox J Crick E (1993) Cattle as a possible source of verocytotoxin-producing Escherichia coli O157 infections in man. Epidemiol Infect 111 : 439 447.
31. Chapman PA, Siddons CA, Cerdan Malo AT Harkin MA (1997) A 1-year study of Escherichia coli O157 in cattle, sheep, pigs and poultry. Epidemiol Infect 119 : 245 250.
32. Chapman PA, Cornell J Green C (2000) Infection with verocytotoxin- producing Escherichia coli O157 during a visit to an inner city open farm. Epidemiol Infect 125 : 531 536.
33. Cobbold R Desmarchelier P (2000) A longitudinal study of Shiga-toxigenic Escherichia coli (STEC) prevalence in three Australian dairy herds. Vet Microbiol 71 : 125 137.
34. Cobbold RN, Hancock DD, Rice DH, Berg J, Stilborn R, Hovde CJ Besser TE (2007) Rectoanal junction colonization of feedlot cattle by Escherichia coli O157:H7 and its association with supershedders and excretion dynamics. Appl Environ Microb 73 : 1563 1568.
35. Cookson AL, Hayes CM, Pearson GR, Roe JM, Wales AD Woodward MJ (2002a) Isolation from a sheep of an attaching-effacing E. coli O115:H- with a novel combination of virulence factors. J Med Microbiol 51 : 1041 1049.
36. Cookson AL, Wales AD, Roe JM, Hayes CM, Pearson GR Woodward MJ (2002b) Variation in the persistence of Escherichia coli O157:H7 in experimentally inoculated six-week-old conventional lambs. J Med Microbiol 51 : 1032 1040.
37. Cookson AL, Taylor SCS, Bennett J, Thomson-Carter F Attwood GT (2006) Serotypes and analysis of distribution of Shiga toxin-producing Escherichia coli from cattle and sheep in the lower North Island, New Zealand. New Zeal Vet J 54 : 78 84.
38. Cookson AL, Bennett J, Thomson-Carter F Attwood GT (2007) Intimin subtyping of Escherichia coli: concomitant carriage of multiple intimin subtypes from forage-fed cattle and sheep. FEMS Microbiol Lett 272 : 163 171.
39. Cornick NA VuKhac H (2008) Indirect transmission of Escherichia coli O157:H7 occurs readily among swine but not among sheep. Appl Environ Microb 74 : 2488 2491.
40. Cornick NA, Booher SL Moon HW (2002) Intimin facilitates colonization by Escherichia coli O157:H7 in adult ruminants. Infect Immun 70 : 2704 2707.
41. Cornick NA, Helgerson AF Sharma V (2007) Shiga toxin and Shiga toxin-encoding phage do not facilitate Escherichia coli O157:H7 colonization in sheep. Appl Environ Microb 73 : 344 346.
42. Cortes 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.
43. Creuzburg K Schmidt H (2007) Molecular characterization and distribution of genes encoding members of the type III effector NleA family among pathogenic Escherichia coli strains. J Clin Microbiol 45 : 2498 2507.
44. Cryan B (1990) Enterohaemorrhagic Escherichia coli. Scand J Infect Dis 22 : 1 4.
45. Dahan S, Wiles S, La Ragione RM et al 2005) EspJ is a prophage-carried type III effector protein of attaching and effacing pathogens that modulates infection dynamics. Infect Immun 73 : 679 686.
46. Dean-Nystrom EA, Bosworth BT Moon HW (1997) Pathogenesis of O157:H7 Escherichia coli infection in neonatal calves. Adv Exp Med Biol 412 : 47 51.
47. Dean-Nystrom EA, Bosworth BT, O'Brien AD Moon HW (1999) Bovine infection with Escherichia coli O157:H7. E. coli O157 in Farm Animals (Stewart CS Flint HJ, eds), pp. 51 58. CAB International, Wallingford, UK.
48. de la Fuente R, Luzon M, Ruiz-Santa-Quiteria JA, Garcia A, Cid D, Orden JA, Garcia S, Sanz R Gomez-Bautista M (1999) Cryptosporidium and concurrent infections with other major enteropathogens in 1 to 30-day-old diarrheic dairy calves in central Spain. Vet Parasitol 80 : 179 185.
49. Dibb-Fuller MP, Best A, Stagg DA, Cooley WA Woodward MJ (2001) An in-vitro model for studying the interaction of Escherichia coli O157:H7 and other enteropathogens with bovine primary cell cultures. J Med Microbiol 50 : 759 769.
50. Dipineto L, Santaniello A, Fontanella M, Lagos K, Fioretti A Menna LF (2006) Presence of Shiga toxin-producing Escherichia coli O157:H7 in living layer hens. Lett Appl Microbiol 43 : 293 295.
51. Djordjevic SP, Hornitzky MA, Bailey G, Gill P, Vanselow B, Walker K Bettelheim KA (2001) Virulence properties and serotypes of Shiga toxin-producing Escherichia coli from healthy Australian slaughter-age sheep. J Clin Microbiol 39 : 2017 2021.
52. Dobbin HS, Hovde CJ, Williams CJ Minnich SA (2006) The Escherichia coli O157 flagellar regulatory gene flhC and not the flagellin gene fliC impacts colonization of cattle. Infect Immun 74 : 2894 2905.
53. Donnenberg MS, Tzipori S, McKee ML, O'Brien AD, Alroy J Kaper JB (1993) The role of the eae gene of enterohemorrhagic Escherichia coli in intimate attachment in vitro and in a porcine model. J Clin Invest 92 : 1418 1424.
54. Dons L, Eriksson E, Jin Y, Rottenberg ME, Kristensson K, Larsen CN, Bresciani J Olsen JE (2004) Role of flagellin and the two-component CheA/CheY system of Listeria monocytogenes in host cell invasion and virulence. Infect Immun 72 : 3237 3244.
55. Doyle MP Schoeni JL (1987) Isolation of Escherichia coli O157:H7 from retail fresh meats and poultry. Appl Environ Microb 53 : 2394 2396.
56. Drolet R, Fairbrother JM Vaillancourt D (1994) Attaching and effacing Escherichia coli in a goat with diarrhea. Can Vet J 35 : 122 123.
57. Duhamel GE, Moxley RA, Maddox CW Erickson ED (1992) Enteric infection of a goat with enterohemorrhagic Escherichia coli (O103:H2). J Vet Diagn Invest 4 : 197 200.
58. Dziva F, Vlisidou I, Crepin VF, Wallis TS, Frankel G Stevens MP (2007) Vaccination of calves with EspA, a key colonisation factor of Escherichia coli O157:H7, induces antigen-specific humoral responses but does not confer protection against intestinal colonisation. Vet Microbiol 123 : 254 261.
59. Elliott SJ, Krejany EO, Mellies JL, Robins-Browne RM, Sasakawa C Kaper JB (2001) EspG, a novel type III system-secreted protein from enteropathogenic Escherichia coli with similarities to VirA of Shigella flexneri. Infect Immun 69 : 4027 4033.
60. Erdem AL, Avelino F, Xicohtencatl-Cortes J Giron JA (2007) Host protein binding and adhesive properties of H6 and H7 flagella of attaching and effacing Escherichia coli. J Bacteriol 189 : 7426 7435.
61. Eriksson E, Nerbrink E, Borch E, Aspan A Gunnarsson A (2003) Verocytotoxin-producing Escherichia coli O157:H7 in the Swedish pig population. Vet Rec 152 : 712 717.
62. Espie E, Vaillant V, Mariani-Kurkdjian P, Grimont F, Martin-Schaller R, De Valk H Vernozy-Rozand C (2006) Escherichia coli O157 outbreak associated with fresh unpasteurized goats' cheese. Epidemiol Infect 134 : 143 146.
63. Faith NG, Shere JA, Brosch R, Arnold KW, Ansay SE, Lee MS, Luchansky JB Kaspar CW (1996) Prevalence and clonal nature of Escherichia coli O157:H7 on dairy farms in Wisconsin. Appl Environ Microb 62 : 1519 1525.
64. Fegan N Desmarchelier P (1999) Shiga toxin-producing Escherichia coli in sheep and pre-slaughter lambs in eastern Australia. Lett Appl Microbiol 28 : 335 339.
65. Feldman M, Bryan R, Rajan S, Scheffler L, Brunnert S, Tang H Prince A (1998) Role of flagella in pathogenesis of Pseudomonas aeruginosa pulmonary infection. Infect Immun 66 : 43 51.
66. Ferguson DD, Scheftel J, Cronquist A, Smith K, Woo-Ming A, Anderson E, Knutsen J, De AK Gershman K (2005) Temporally distinct Escherichia coli O157 outbreaks associated with alfalfa sprouts linked to a common seed source - Colorado and Minnesota, 2003. Epidemiol Infect 133 : 439 447.
67. Fitzhenry R, Dahan S, Torres AG, Chong Y, Heuschkel R, Murch SH, Thomson M, Kaper JB, Frankel G Phillips AD (2006) Long polar fimbriae and tissue tropism in Escherichia coli O157:H7. Microbes Infect 8 : 1741 1749.
68. Fitzhenry RJ, Pickard DJ, Hartland EL, Reece S, Dougan G, Phillips AD Frankel G (2002) Intimin type influences the site of human intestinal mucosal colonisation by enterohaemorrhagic Escherichia coli O157:H7. Gut 50 : 180 185.
69. Foster G, Evans J, Knight HI, Smith AW, Gunn GJ, Allison LJ, Synge BA Pennycott TW (2006) Analysis of feces samples collected from a wild-bird garden feeding station in Scotland for the presence of verocytotoxin-producing Escherichia coli O157. Appl Environ Microb 72 : 2265 2267.
70. Fox JT, Corrigan M, Drouillard JS, Shi X, Oberst RD Nagaraja TG (2007) Effects of concentrate level of diet and pen configuration on prevalence of Escherichia coli O157 in finishing goats. Small Ruminant Res 72 : 45 50.
71. Fukushima H Seki R (2004) High numbers of Shiga toxin-producing Escherichia coli found in bovine faeces collected at slaughter in Japan. FEMS Microbiol Lett 238 : 189 197.
72. Fukushima H, Hashizume T, Morita Y, Tanaka J, Azuma K, Mizumoto Y, Kaneno M, Matsuura M, Konma K Kitani T (1999) Clinical experiences in Sakai City Hospital during the massive outbreak of enterohemorrhagic Escherichia coli O157 infections in Sakai City, 1996. Pediatr Int 41 : 213 217.
73. Galiero G, Conedera G, Alfano D Caprioli A (2005) Isolation of verocytotoxin-producing Escherichia coli O157 from water buffaloes (Bubalus bubalis) in southern Italy. Vet Rec 156 : 382 383.
74. Gansheroff LJ O'Brien AD (2000) Escherichia coli O157:H7 in beef cattle presented for slaughter in the US: higher prevalence rates than previously estimated. P Natl Acad Sci USA 97 : 2959 2961.
75. Garcia-Sanchez A, Sanchez S, Rubio R, Pereira G, Alonso JM, Hermoso de Mendoza J Rey J (2007) Presence of Shiga toxin-producing E. coli O157:H7 in a survey of wild artiodactyls. Vet Microbiol 121 : 373 377.
76. Garmendia J, Phillips AD, Carlier MF et al 2004) TccP is an enterohaemorrhagic Escherichia coli O157:H7 type III effector protein that couples Tir to the actin-cytoskeleton. Cell Microbiol 6 : 1167 1183.
77. Giron JA, Torres AG, Freer E Kaper JB (2002) The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol Microbiol 44 : 361 379.
78. Goosney DL, DeVinney R, Pfuetzner RA, Frey EA, Strynadka NC Finlay BB (2000) Enteropathogenic E. coli translocated intimin receptor, Tir, interacts directly with alpha-actinin. Curr Biol 10 : 735 738.
79. Grauke LJ, Kudva IT, Yoon JW, Hunt CW, Williams CJ Hovde CJ (2002) Gastrointestinal tract location of Escherichia coli O157:H7 in ruminants. Appl Environ Microb 68 : 2269 2277.
80. Griffin PM Tauxe RV (1991) The epidemiology of infections caused by Escherichia coli O157:H7, other enterohemorrhagic E. coli, and the associated hemolytic uremic syndrome. Epidemiol Rev 13 : 60 98.
81. Gruenheid S, DeVinney R, Bladt F, Goosney D, Gelkop S, Gish GD, Pawson T Finlay BB (2001) Enteropathogenic E. coli Tir binds Nck to initiate actin pedestal formation in host cells. Nat Cell Biol 3 : 856 859.
82. Gruenheid S, Sekirov I, Thomas NA et al 2004) Identification and characterization of NleA, a non-LEE-encoded type III translocated virulence factor of enterohaemorrhagic Escherichia coli O157:H7. Mol Microbiol 51 : 1233 1249.
83. Gunzer F, Hennig-Pauka I, Waldmann KH, Sandhoff R, Grone HJ, Kreipe HH, Matussek A Mengel M (2002) Gnotobiotic piglets develop thrombotic microangiopathy after oral infection with enterohemorrhagic Escherichia coli. Am J Clin Pathol 118 : 364 375.
84. Hancock DD, Rice DH, Herriott DE, Besser TE, Ebel ED Carpenter LV (1997) Effects of farm manure-handling practices on Escherichia coli O157 prevalence in cattle. J Food Protect 60 : 363 366.
85. Hayashi T, Makino K, Ohnishi M et al 2001) Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12. DNA Res 8 : 11 22 (Erratum in DNA Res 8, 96).
86. Heuvelink AE, van den Biggelaar FL, de Boer E, Herbes RG, Melchers WJ, Huis in 't Veld JH Monnens LA (1998) Isolation and characterization of verocytotoxin-producing Escherichia coli O157 strains from Dutch cattle and sheep. J Clin Microbiol 36 : 878 882.
87. Heuvelink AE, van Heerwaarden C, Zwartkruis-Nahuis JT, van Oosterom R, Edink K, van Duynhoven YT de Boer E (2002) Escherichia coli O157 infection associated with a petting zoo. Epidemiol Infect 129 : 295 302.
88. Ho TD Waldor MK (2007) Enterohemorrhagic Escherichia coli O157:H7 gal mutants are sensitive to bacteriophage P1 and defective in intestinal colonization. Infect Immun 75 : 1661 1666.
89. Hoey DE, Currie C, Else RW, Nutikka A, Lingwood CA, Gally DL Smith DG (2002) Expression of receptors for verotoxin 1 from Escherichia coli O157 on bovine intestinal epithelium. J Med Microbiol 51 : 143 149.
90. Iida K, Mizunoe Y, Wai SN Yoshida S (2001) Type 1 fimbriation and its phase switching in diarrheagenic Escherichia coli strains. Clin Diagn Lab Immun 8 : 489 495.
91. Iino T, Komeda Y, Kutsukake K, Macnab RM, Matsumura P, Parkinson JS, Simon MI Yamaguchi S (1988) New unified nomenclature for the flagellar genes of Escherichia coli and Salmonella typhimurium. Microbiol Rev 52 : 533 535.
92. Inglis TJ, Robertson T, Woods DE, Dutton N Chang BJ (2003) Flagellum-mediated adhesion by Burkholderia pseudomallei precedes invasion of Acanthamoeba astronyxis. Infect Immun 71 : 2280 2282.
93. Janke BH, Francis DH, Collins JE, Libal MC, Zeman DH Johnson DD (1989) Attaching and effacing Escherichia coli infections in calves, pigs, lambs, and dogs. J Vet Diagn Invest 1 : 6 11.
94. Janke BH, Francis DH, Collins JE, Libal MC, Zeman DH, Johnson DD Neiger RD (1990) Attaching and effacing Escherichia coli infection as a cause of diarrhea in young calves. J Am Vet Med Assoc 196 : 897 901.
95. Jordan DM, Cornick N, Torres AG, Dean-Nystrom EA, Kaper JB Moon HW (2004) Long polar fimbriae contribute to colonization by Escherichia coli O157:H7 in vivo. Infect Immun 72 : 6168 6171.
96. Kalchayanand N, Arthur TM, Bosilevac JM, Brichta-Harhay DM, Guerini MN, Shackelford SD, Wheeler TL Koohmaraie M (2007) Microbiological characterization of lamb carcasses at commercial processing plants in the United States. J Food Protect 70 : 1811 1819.
97. Kaper JB, Elliott S, Sperandio V, Perna NT, Mayhew GF Blattner FR (1998) Attaching-and-effacing intestinal histopathology and the locus of enterocyte effacement. Escherichia coli O157:H7 and Other Shiga Toxin-Producing E. coli Strains (O'Brien AD Kaper JB, eds), pp. 163 182. ASM Press, Washington, DC.
98. Karmali MA, Steele BT, Petric M Lim C (1983) Sporadic cases of haemolytic-uraemic syndrome associated with faecal cytotoxin and cytotoxin-producing Escherichia coli in stools. Lancet 1 : 619 620.
99. Keen JE, Wittum TE, Dunn JR, Bono JL Durso LM (2006) Shiga-toxigenic Escherichia coli O157 in agricultural fair livestock, United States. Emerg Infect Dis 12 : 780 786.
100. Kelleher SL Lonnerdal B (2001) Immunological activities associated with milk. Advances in Nutritional Research, Vol. 10. Kluwer Academic/Plenum Publishing, New York, pp. 39 65.
101. Kim J, Thanabalasuriar A, Chaworth-Musters T et al 2007) The bacterial virulence factor NleA inhibits cellular protein secretion by disrupting mammalian COPII function. Cell Host, Microbe 2 : 160 171.
102. Kirov SM, Castrisios M Shaw JG (2004) Aeromonas flagella (polar and lateral) are enterocyte adhesins that contribute to biofilm formation on surfaces. Infect Immun 72 : 1939 1945.
103. Knutton S, Lloyd DR McNeish AS (1987) Adhesion of enteropathogenic Escherichia coli to human intestinal enterocytes and cultured human intestinal mucosa. Infect Immun 55 : 69 77.
104. Kudva IT, Hatfield PG Hovde CJ (1996) Escherichia coli O157:H7 in microbial flora of sheep. J Clin Microbiol 34 : 431 433.
105. Lane MC Mobley HL (2007) Role of P-fimbrial-mediated adherence in pyelonephritis and persistence of uropathogenic Escherichia coli (UPEC) in the mammalian kidney. Kidney Int 72 : 19 25.
106. La Ragione RM, Cooley WA Woodward MJ (2000) The role of fimbriae and flagella in the adherence of avian strains of Escherichia coli O78:K80 to tissue culture cells and tracheal and gut explants. J Med Microbiol 49 : 327 338.
107. La Ragione RM, Best A, Sprigings KA, Cooley WA, Jepson MA Woodward MJ (2004) Interaction between attaching and effacing Escherichia coli serotypes O157:H7 and O26:K60 in cell culture. Vet Microbiol 104 : 119 124.
108. La Ragione RM, Ahmed NM, Best A, Clifford D, Weyer U, Cooley WA, Johnson L, Pearson GR Woodward MJ (2005a) Colonization of 8-week-old conventionally reared goats by Escherichia coli O157:H7 after oral inoculation. J Med Microbiol 54 : 485 492.
109. La Ragione RM, Ahmed NM, Best A, Clifford D, Weyer U Woodward MJ (2005b) Failure to detect transmission of Escherichia coli O157:H7 from orally dosed nannies to sucking kids at foot. Vet Rec 157 : 659 661.
110. La Ragione RM, Best A, Clifford D et al 2006) Influence of colostrum deprivation and concurrent Cryptosporidium parvum infection on the colonization and persistence of Escherichia coli O157:H7 in young lambs. J Med Microbiol 55 : 819 828.
111. Laven RA, Ashmore A Stewart CS (2003) Escherichia coli in the rumen and colon of slaughter cattle, with particular reference to E. coli O157. Vet J 165 : 78 83.
112. Levine MM (1987) Escherichia coli that cause diarrhea: enterotoxigenic, enteropathogenic, enteroinvasive, enterohemorrhagic, and enteroadherent. J Infect Dis 155 : 377 389.
113. Licence K, Oates KR, Synge BA Reid TMS (2001) An outbreak of E. coli O157 infection with evidence of spread from animals to man through contamination of a private water supply. Epidemiol Infect 126 : 135 138.
114. Liu X Matsumura P (1994) The FlhD/FlhC complex, a transcriptional activator of the Escherichia coli flagellar class II operons. J Bacteriol 176 : 7345 7351.
115. Locking ME, O'Brien SJ, Reilly WJ, Wright EM, Campbell DM, Coia JE, Browning LM Ramsay CN (2001) Risk factors for sporadic cases of Escherichia coli O157 infection: the importance of contact with animal excreta. Epidemiol Infect 127 : 215 220.
116. Logan EF, Stenhous A, Ormrod DJ Penhale WJ (1974) Role of colostral immunoglobulins in intestinal immunity to enteric colibacillosis in calf. Res Vet Sci 17 : 290 301.
117. Low AS, Dziva F, Torres AG et al 2006) Cloning, expression, and characterization of fimbrial operon F9 from enterohemorrhagic Escherichia coli O157:H7. Infect Immun 74 : 2233 2244.
118. Low JC, McKendrick IJ, McKechnie C, Fenlon D, Naylor SW, Currie C, Smith DG, Allison L Gally DL (2005) Rectal carriage of enterohemorrhagic Escherichia coli O157 in slaughtered cattle. Appl Environ Microb 71 : 93 97.
119. Maki DG (2006) Don't eat the spinach - controlling foodborne infectious disease. New Engl J Med 355 : 1952 1955.
120. Marchès O, Ledger TN, Boury M et al 2003) Enteropathogenic and enterohaemorrhagic Escherichia coli deliver a novel effector called Cif, which blocks cell cycle G2/M transition. Mol Microbiol 50 : 1553 1567.
121. Marchès O, Wiles S, Dziva F et al 2005) Characterization of two non-locus of enterocyte effacement-encoded type III-translocated effectors, NleC and NleD, in attaching and effacing pathogens. Infect Immun 73 : 8411 8417.
122. Marchès O, Covarelli V, Dahan S, Cougoule C, Bhatta P, Frankel G Caron E (2008) EspJ of enteropathogenic and enterohaemorrhagic Escherichia coli inhibits opsono-phagocytosis. Cell Microbiol 10 : 1104 1115.
123. Martin ML, Shipman LD, Wells JG, Potter ME, Hedberg K, Wachsmuth IK, Tauxe RV, Davis JP, Arnoldi J Tilleli J (1986) Isolation of Escherichia coli O157:H7 from dairy cattle associated with two cases of haemolytic uraemic syndrome. Lancet 2 : 1043.
124. McIntyre L, Fung J, Paccagnella A, Isaac-Renton J, Rockwell F, Emerson B Preston T (2002) Escherichia coli O157 outbreak associated with the ingestion of unpasteurized goat's milk in British Columbia, 2001. Can Commun Dis Rep 28 : 6 8.
125. McNeilly TN, Naylor SW, Mitchell MC, McAteer S, Mahajan A, Smith DGE, Gally DL, Low JC Huntley JF (2007) Simple methods for measurement of bovine mucosal antibody responses in vivo. Vet Immunol Immunop 118 : 160 167.
126. Meng J, Zhao S Doyle MP (1998) Virulence genes of Shiga toxin-producing Escherichia coli isolated from food, animals and humans. Int J Food Microbiol 45 : 229 235.
127. Menge C, Stamm I, Blessenohl M, Wieler LH Baljer G (2003) Verotoxin 1 from Escherichia coli affects Gb(3)/CD77(+) bovine lymphocytes independent of interleukin-2, tumor necrosis factor-alpha, and interferon-alpha. Exp Biol Med 228 : 377 386.
128. Midgley J, Fegan N Desmarchelier P (1999) Dynamics of Shiga toxin-producing Escherichia coli (STEC) in feedlot cattle. Lett Appl Microbiol 29 : 85 89.
129. Milnes AS, Stewart I, Clifton-Hadley FA et al 2008) Intestinal carriage of verocytotoxigenic Escherichia coli O157, Salmonella, thermophilic Campylobacter and Yersinia enterocolitica, in cattle, sheep and pigs at slaughter in Great Britain during 2003. Epidemiol Infect 136 : 739 751.
130. Miyao Y, Kataoka T, Nomoto T, Kai A, Itoh T Itoh K (1998) Prevalence of verotoxin-producing Escherichia coli harbored in the intestine of cattle in Japan. Vet Microbiol 61 : 137 143.
131. Monday SR, Minnich SA Feng PC (2004) A 12-base-pair deletion in the flagellar master control gene flhC causes nonmotility of the pathogenic German sorbitol-fermenting Escherichia coli O157:H- strains. J Bacteriol 186 : 2319 2327.
132. Mundy R, Jenkins C, Yu J, Smith H Frankel G (2004a) Distribution of espl among clinical enterohaemorrhagic and enteropathogenic Escherichia coli isolates. J Med Microbiol 53 : 1145 1149.
133. Mundy R, Petrovska L, Smollett K et al 2004b) Identification of a novel Citrobacter rodentium Type III secreted protein, EspI, and roles of this and other secreted proteins in infection. Infect Immun 72 : 2288 2302.
134. Mundy R, Schuller S, Girard F, Fairbrother JM, Phillips AD Frankel G (2007) Functional studies of intimin in vivo and ex vivo: implications for host specificity and tissue tropism. Microbiology (SGM) 153 : 959 967.
135. Munoz M, Alvarez M, Lanza I Carmenes P (1996) Role of enteric pathogens in the aetiology of neonatal diarrhoea in lambs and goat kids in Spain. Epidemiol Infect 117 : 203 211.
136. Müsken A, Bielaszewska M, Greune L, Schweppe CH, Muething J, Schmidt H, Schmidt MA, Karch H Zhang W (2008) Anaerobic conditions promote expression of Sfp fimbriae and adherence of sorbitol-fermenting enterohemorrhagic Escherichia coli O157:NM to human intestinal epithelial cells. Appl Environ Microb 74 : 1087 1093.
137. Nataro JP Kaper JB (1998) Diarrheagenic Escherichia coli. Clin Microbiol Rev 11 : 142 201.
138. Naylor SW, Low JC, Besser TE, Mahajan A, Gunn GJ, Pearce MC, McKendrick IJ, Smith DGE Gally DL (2003) Lymphoid follicle-dense mucosa at the terminal rectum is the principal site of colonization of enterohemorrhagic Escherichia coli O157:H7 in the bovine host. Infect Immun 71 : 1505 1512.
139. Naylor SW, Roe AJ, Nart P, Spears K, Smith DG, Low JC Gally DL (2005) Escherichia coli O157:H7 forms attaching and effacing lesions at the terminal rectum of cattle and colonization requires the LEE4 operon. Microbiology (SGM) 151 : 2773 2781.
140. Nougayrede JP, Boury M, Tasca C, Marches O, Milon A, Oswald E De Rycke J (2001) Type III secretion-dependent cell cycle block caused in HeLa cells by enteropathogenic Escherichia coli O103. Infect Immun 69 : 6785 6795.
141. Ogden ID, MacRae M Strachan NJ (2004) Is the prevalence and shedding concentrations of E. coli O157 in beef cattle in Scotland seasonal? FEMS Microbiol Lett 233 : 297 300.
142. Ogden ID, MacRae M Strachan NJ (2005) Concentration and prevalence of Escherichia coli O157 in sheep faeces at pasture in Scotland. J Appl Microbiol 98 : 646 651.
143. Omisakin F, MacRae M, Ogden ID Strachan NJ (2003) Concentration and prevalence of Escherichia coli O157 in cattle feces at slaughter. Appl Environ Microb 69 : 2444 2447.
144. Ooka T, Vieira MA, Ogura Y et al 2007) Characterization of tccP2 carried by atypical enteropathogenic Escherichia coli. FEMS Microbiol Lett 271 : 126 135.
145. Oporto B, Esteban JI, Aduriz G, Juste RA Hurtado A (2008) Escherichia coli O157:H7 and non-O157 Shiga toxin-producing E. coli in healthy cattle, sheep and swine herds in northern Spain. Zoonoses Public Health 55 : 73 81.
146. Pai CH, Gordon R, Sims HV Bryan LE (1984) Sporadic cases of hemorrhagic colitis associated with Escherichia coli O157:H7. Clinical, epidemiologic, and bacteriologic features. Ann Intern Med 101 : 738 742.
147. Paiba GA, Gibbens JC, Pascoe SJ et al 2002) Faecal carriage of verocytotoxin-producing Escherichia coli O157 in cattle and sheep at slaughter in Great Britain. Vet Rec 150 : 593 598.
148. Paiba GA, Wilesmith JW, Evans SJ et al 2003) Prevalence of faecal excretion of verocytotoxigenic Escherichia coli O157 in cattle in England and Wales. Vet Rec 153 : 347 353.
149. Payne CJ, Petrovic M, Roberts RJ et al 2003) Vero cytotoxin-producing Escherichia coli O157 gastroenteritis in farm visitors, North Wales. Emerg Infect Dis 9 : 526 530.
150. Perna NT, Plunkett G, Burland V et al 2001) Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409 : 529 533.
151. Potter AA, Klashinsky S, Li YL et al 2004) Decreased shedding of Escherichia coli O157:H7 by cattle following vaccination with type III secreted proteins. Vaccine 22 : 362 369.
152. Pritchard GC, Willshaw GA, Bailey JR, Carson T Cheasty T (2000) Verocytotoxin-producing Escherichia coli O157 on a farm open to the public: outbreak investigation and longitudinal bacteriological study. Vet Rec 147 : 259 264.
153. Pritchard GC, Williamson S, Carson T, Bailey JR, Warner L, Willshaw G Cheasty G (2001) Wild rabbits - a novel vector for verocytotoxigenic Escherichia coli O157. Vet Rec 149 : 567.
154. Pruimboom-Brees IM, Morgan TW, Ackermann MR, Nystrom ED, Samuel JE, Cornick NA Moon HW (2000) Cattle lack vascular receptors for Escherichia coli O157:H7 Shiga toxins. P Natl Acad Sci USA 97 : 10325 10329.
155. Rey J, Sanchez S, Blanco JE, Hermoso de Mendoza J, Hermoso de Mendoza M, Garcia A, Gil C, Tejero N, Rubio R Alonso JM (2006) Prevalence, serotypes and
156. Rice DH, Sheng HQ, Wynia SA Hovde CJ (2003) Rectoanal mucosal swab culture is more sensitive than fecal culture and distinguishes Escherichia coli O157:H7-colonized cattle and those transiently shedding the same organism. J Clin Microbiol 41 : 4924 4929.
157. Richards MS, Corkish JD, Sayers AR, McLaren IM, Evans SJ Wray C (1998) Studies of the presence of verocytotoxic Escherichia coli O157 in bovine faeces submitted for diagnostic purposes in England and Wales and on beef carcases in abattoirs in the United Kingdom. Epidemiol Infect 120 : 187 192.
158. Richardson SE, Karmali MA, Becker LE Smith CR (1988) The histopathology of the hemolytic uremic syndrome associated with verocytotoxin-producing Escherichia coli infections. Hum Pathol 19 : 1102 1108.
159. Riley LW (1987) The epidemiologic, clinical, and microbiologic features of hemorrhagic colitis. Annu Rev Microbiol 41 : 383 407.
160. Riley LW, Remis RS, Helgerson SD et al 1983) Hemorrhagic colitis associated with a rare Escherichia coli serotype. New Engl J Med 308 : 681 685.
161. Roe AJ, Currie C, Smith DGE Gally DL (2001) Analysis of type 1 fimbriae expression in verotoxigenic Escherichia coli: a comparison between serotypes O157 and O26. Microbiology (SGM) 147 : 145 152.
162. Rugbjerg H, Nielsen EM Andersen JS (2003) Risk factors associated with faecal shedding of verocytotoxin-producing Escherichia coli O157 in eight known-infected Danish dairy herds. Prev Vet Med 58 : 101 113.
163. Ryan CA, Tauxe RV, Hosek GW, Wells JG, Stoesz PA, McFadden HW Jr., Smith PW, Wright GF Blake PA (1986) Escherichia coli O157:H7 diarrhea in a nursing home: clinical, epidemiological, and pathological findings. J Infect Dis 154 : 631 638.
164. Scaife HR, Cowan D, Finney J, Kinghorn-Perry SF Crook B (2006) Wild rabbits (Oryctolagus cuniculus) as potential carriers of verocytotoxin-producing Escherichia coli. Vet Rec 159 : 175 178.
165. Schimmer B, Nygard K, Eriksen HM, Lassen J, Lindstedt BA, Brandal LT, Kapperud G Aavitsland P (2008) Outbreak of haemolytic uraemic syndrome in Norway caused by stx(2)-positive Escherichia coli O103:H25 traced to cured mutton sausages. BMC Infect Dis 8 : 41, DOI :.
166. Shaw RK, Smollett K, Cleary J, Garmendia J, Straatman-Iwanowska A, Frankel G Knutton S (2005) Enteropathogenic Escherichia coli type III effectors EspG and EspG2 disrupt the microtubule network of intestinal epithelial cells. Infect Immun 73 : 4385 4390.
167. Sheng H, Davis MA, Knecht HJ Hovde CJ (2004) Rectal administration of Escherichia coli O157:H7: novel model for colonization of ruminants. Appl Environ Microb 70 : 4588 4595.
168. Shukla R, Slack R, George A, Cheasty T, Rowe B Scutter J (1995) Escherichia coli O157 infection associated with a farm visitor centre. Commun Dis Rep CDR Rev 5 : R86 R90.
169. Solecki O, MacRae M, Ogden I Strachan N (2007) Can the high levels of human verocytotoxigenic Escherichia coli O157 infection in rural areas of NE Scotland be explained by consumption of contaminated meat? J Appl Microbiol 103 : 2616 2621.
170. Sperandio V, Mellies JL, Nguyen W, Shin S Kaper JB (1999) Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. P Natl Acad Sci USA 96 : 15196 15201.
171. Sperandio V, Torres AG, Giron JA Kaper JB (2001) Quorum sensing is a global regulatory mechanism in enterohemorrhagic Escherichia coli O157:H7. J Bacteriol 183 : 5187 5197.
172. Sperandio V, Torres AG Kaper JB (2002) Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli. Mol Microbiol 43 : 809 821.
173. Sperandio V, Torres AG, Jarvis B, Nataro JP Kaper JB (2003) Bacteria-host communication: the language of hormones. P Natl Acad Sci USA 100 : 8951 8956.
174. Steen M, Hedin G, Hokeberg I, Eriksson E, Wallden B Nagelhus O (2001) EHEC from goat milk as the cause of severe diarrhoea in a young woman. Svensk Vet Tidn 53 : 861 865.
175. Stevens MP, van Diemen PM, Frankel G, Phillips AD Wallis TS (2002) Efa1 influences colonization of the bovine intestine by Shiga toxin-producing Escherichia coli serotypes O5 and O111. Infect Immun 70 : 5158 5166.
176. Stevens MP, Roe AJ, Vlisidou I, van Diemen PM, La Ragione RM, Best A, Woodward MJ, Gally DL Wallis TS (2004) Mutation of toxB and a truncated version of the efa-1 gene in Escherichia coli O157:H7 influences the expression and secretion of locus of enterocyte effacement-encoded proteins but not intestinal colonization in calves or sheep. Infect Immun 72 : 5402 5411.
177. Stirling J, Griffith M, Dooley JSG et al 2008) Zoonoses associated with petting farms and open zoos. Vector-Borne Zoonot 8 : 85 92.
178. Strachan NJ, Dunn GM, Locking ME, Reid TM Ogden ID (2006) Escherichia coli O157: burger bug or environmental pathogen? Int J Food Microbiol 112 : 129 137.
179. Strachan NJC, Fenlon DR Ogden ID (2001) Modelling the vector pathway and infection of humans in an environmental outbreak of Escherichia coli O157. FEMS Microbiol Lett 203 : 69 73.
180. Synge B Paiba G (2000) Verocytotoxin-producing E. coli O157. Vet Rec 147 : 27.
181. Tasteyre A, Barc MC, Collignon A, Boureau H Karjalainen T (2001) Role of FliC and FliD flagellar proteins of Clostridium difficile in adherence and gut colonization. Infect Immun 69 : 7937 7940.
182. Tominaga K, Nakazawa M, Haritani M Hirata K (1989) Bio-chemical characteristics and pathogenicity of attaching and effacing Escherichia coli (AEEC) isolated from calves with diarrhoea. Nippon Juishikai Zasshi (J Jpn Vet Med Assoc) 42 : 775 779.
183. Torres AG, Giron JA, Perna NT, Burland V, Blattner FR, Avelino-Flores F Kaper JB (2002) Identification and characterization of lpfABCC'DE, a fimbrial operon of enterohemorrhagic Escherichia coli O157:H7. Infect Immun 70 : 5416 5427.
184. Torres AG, Milflores-Flores L, Garcia-Gallegos JG, Patel SD, Best A, La Ragione RM, Martinez-Laguna Y Woodward MJ (2007) Environmental regulation and colonization attributes of the long polar fimbriae (LPF) of Escherichia coli O157:H7. Int J Med Microbiol 297 : 177 185.
185. Tutenel AV, Pierard D, Uradzinski J et al 2002) Isolation and characterization of enterohaemorrhagic Escherichia coli O157:H7 from cattle in Belgium and Poland. Epidemiol Infect 129 : 41 47.
186. Vlisidou I, Lyte M, van Diemen PM, Hawes P, Monaghan P, Wallis TS Stevens MP (2004) The neuroendocrine stress hormone norepinephrine augments Escherichia coli O157:H7-induced enteritis and adherence in a bovine ligated ileal loop model of infection. Infect Immun 72 : 5446 5451.
187. Vlisidou I, Dziva F, La Ragione RM et al 2006) Role of intimin-Tir interactions and the Tir-cytoskeleton coupling protein in the colonization of calves and lambs by Escherichia coli O157:H7. Infect Immun 74 : 758 764.
188. Wales AD, Pearson GR, Best A, Cookson AL, Hayes CM, La Ragione RM, Roe JM Woodward MJ (2005a) Naturally-acquired attaching and effacing Escherichia coli in sheep. Res Vet Sci 78 : 109 115.
189. Wales AD, Pearson GR, Roe JM, Hayes CM Woodward MJ (2005b) Attaching-effacing lesions associated with Escherichia coli O157:H7 and other bacteria in experimentally inoculated conventional neonatal goat kids. J Comp Pathol 132 : 185 194.
190. Wales AD, Woodward MJ Pearson GR (2005c) Attaching-effacing bacteria in animals. J Comp Pathol 132 : 1 26.
191. Woodward MJ, Best A, Sprigings KA, Pearson GR, Skuse AM, Wales A, Hayes CM, Roe JM, Low CJ La Ragione RM (2003) Non-toxigenic Escherichia coli O157:H7 strain NCTC12900 causes attaching-effacing lesions and eae-dependent persistence in weaned sheep. Int J Med Microbiol 293 : 299 308.
192. Wright KJ, Seed PC Hultgren SJ (2005) Uropathogenic Escherichia coli flagella aid in efficient urinary tract colonization. Infect Immun 73 : 7657 7668.
193. Xicohtencati-Cortes J, Monteiro-Neto V, Ledesma MA, Jordan DM, Francetic O, Kaper JB, Puente JL Giron JA (2007) Intestinal adherence associated with type IV pili of enterohemorrhagic Escherichia coli O157:H7. J Clin Invest 117 : 3519 3529.
194. 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, DOI :.
195. Zhao T, Doyle MP, Shere J Garber L (1995) Prevalence of enterohemorrhagic Escherichia coli O157:H7 in a survey of dairy herds. Appl Environ Microb 61 : 1290 1293.
196. Zhou X, Giron JA, Torres AG, Crawford JA, Negrete E, Vogel SN Kaper JB (2003) Flagellin of enteropathogenic Escherichia coli stimulates interleukin-8 production in T84 cells. Infect Immun 71 : 2120 2129.