Escherichia coli O157:H7 strains that persist in feedlot cattle are genetically related and demonstrate an enhanced ability to adhere to intestinal epithelial cells

Applied and Environmental Microbiology

Volumn 75, Issue 18, 2009, Pages 5927-5937

  Carlson, Brandon A ^a   Nightingale, Kendra K ^a   Mason, Gary L ^a   Ruby, John R ^b   Choat, W Travis ^c   Loneragan, Guy H ^d   Smith, Gary C ^a   Sofos, John N ^a   Belk, Keith E ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b JBS Packerland Inc   (United States)

^c ELANCO ANIMAL HEALTH   (United States)

^d WEST TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DATA SUPPORT; E. COLI; E.COLI O157:H7; ESCHERICHIA COLI O157:H7; FEEDLOT CATTLES; GENE FRAGMENTS; GENETIC DIVERGENCE; INTESTINAL EPITHELIAL CELLS; INTESTINAL EPITHELIUM; LONGITUDINAL STUDY; MULTIPLEX PCR; PULSED FIELD GEL ELECTROPHORESIS; SAMPLE POPULATION; VIRULENCE GENE;

ANIMALS; CELLS; ELECTROPHORESIS; MULTIPLEXING;

ESCHERICHIA COLI;

BACTERIOLOGY; CATTLE; COLONIZATION; DIVERGENCE; E REGION; ELECTROKINESIS; FECAL PELLET; GEL; GENE EXPRESSION; GENOTYPE; POLYMERASE CHAIN REACTION; VIRULENCE;

ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BACTERIUM DETECTION; CATTLE; CELL ADHESION; CONTROLLED STUDY; ESCHERICHIA COLI O157; GENE INSERTION; GENOTYPE; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; NONHUMAN; POLYMERASE CHAIN REACTION; PULSED FIELD GEL ELECTROPHORESIS;

ANIMALS; BACTERIAL ADHESION; BACTERIAL TYPING TECHNIQUES; CATTLE; CATTLE DISEASES; CELL LINE, TUMOR; CLUSTER ANALYSIS; DNA FINGERPRINTING; DNA, BACTERIAL; ELECTROPHORESIS, GEL, PULSED-FIELD; EPITHELIAL CELLS; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI O157; ESCHERICHIA COLI PROTEINS; GENOTYPE; HUMANS; LONGITUDINAL STUDIES; POLYMERASE CHAIN REACTION; RECTUM; VIRULENCE FACTORS;

ANIMALIA; BOS; ESCHERICHIA COLI;

EID: 70249140622     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00972-09     Document Type: Article

References (58)

1. Bach, S. J., L. J. Selinger, K. Stanford, and T. A. McAllister. 2005. Effect of supplementing corn- or barley-based feedlot diets with canola oil on faecal shedding of Escherichia coli O157:H7 by steers. J. Appl. Microbiol. 98:464-475.
2. Barham, A. R., B. L. Barham, A. K. Johnson, D. M. Allen, J. R. Blanton, J. R., and M. F. Miller. 2002. Effects of the transportation of beef cattle from the feedyard to the packing plant on prevalence levels of Escherichia coli O157 and Salmonella spp. J. Food Prot. 65:280-283.
3. Barkocy-Gallagher, G. A., E. D. Berry, M. Rivera-Betancourt, T. M. Arthur, X. Nou, and M. Koohmaraie. 2002. Development of methods for the recovery of Escherichia coli O157 and Salmonella from beef carcass sponge samples and bovine fecal and hide samples. J. Food Prot. 65:1527-1534.
4. Barkocy-Gallagher, G. A., T. M. Arthur, M. Rivera-Betancourt, X. Nou, S. D. Shackelford, T. M. Wheeler, and M. Koohmaraie. 2003. Seasonal prevalence of Shiga toxin-producing Escherichia coli, including O157:H7 and non-O157 serotypes, and Salmonella in commercial beef processing plants. J. Food Prot. 66:1978-1986.
5. Barkocy-Gallagher, G. A., K. K. Edwards, X. Nou, J. M. Bosilevac, T. M. Arthur, S. D. Shackelford, and M. Koohmaraie. 2005. Methods for recovering Escherichia coli O157:H7 from cattle fecal, hide, and carcass samples: sensitivity and improvements. J. Food Prot. 68:2264-2268.
6. Besser, T. E., D. D. Hancock, L. C. Pritchett, E. M. McRae, D. H. Rice, and P. I. Tarr. 1997. Duration of detection of fecal excretion of Escherichia coli O157:H7 in cattle. J. Infect. Dis. 175:726-729.
7. Besser, T. E., B. L. Richards, D. H. Rice, and D. D. Hancock. 2001. Escherichia coli O157:H7 infection of calves: infectious dose and direct contact transmission. Epidemiol. Infect. 127:555-560.
8. Brown, C. A., B. G. Harmon, T. Zhao, and M. P. Doyle. 1997. Experimental Escherichia coli O157:H7 carriage in calves. Appl. Environ. Microbiol. 63:27-32.
9. Buchko, S. J., R. A. Holley, W. O. Olsen, V. P. J. Gannon, and D. M. Veira. 2000. The effects of different grain diets on fecal shedding of Escherichia coli O157:H7 by steers. J. Food Prot. 63:1467-1474.
10. Centers for Disease Control and Prevention. 2001. One-day (24-28 h) standardized laboratory protocol for molecular subtyping of Escherichia coli O157:H7 by pulsed-field gel electrophoresis (PFGE). Centers for Disease Control and Prevention, Atlanta, GA.
11. Childs, K. D., C. A. Simpson, W. Warren-Serna, G. Bellinger, B. Centrella, R. A. Bowling, J. Ruby, J. Stefanek, D. J. Vote, T. Choat, J. A. Scanga, J. N. Sofos, G. C. Smith, and K. E. Belk. 2006. Molecular characterization of Escherichia coli O157:H7 hide contamination routes: feedlot to harvest. J. Food Prot. 69:1240-1247.
12. Cobbold, R. N., D. D. Hancock, D. H. Rice, J. Berg, R. Stilborn, C. J. Hovde, and T. E. Besser. 2007. Rectoanal junction colonization of feedlot cattle by Escherichia coli O157:H7 and its association with supershedders and excretion dynamics. Appl. Environ. Microbiol. 73:1563-1568.
13. Cookson, A. L., and M. J. Woodward. 2003. The role of intimin in the adherence of enterohemorrhagic Escherichia coli (EHEC) O157:H7 to HEp-2 tissue culture cells and to bovine gut explants tissues. Int. J. Med. Microbiol. 292:547-553.
14. Cornick, N. A., S. L. Booher, and H. W. Moon. 2002. Intimin facilitates colonization by Escherichia coli O157:H7 in adult ruminants. Infect. Immun. 70:2704-2707.
15. Cray, Jr., W. C., and H. W. Moon. 1995. Experimental infection of calves and adult cattle with Escherichia coli O157:H7. Appl. Environ. Microbiol. 61:1586-1590.
16. Dean-Nystrom, E. A., B. T. Bosworth, W. C. Cray, Jr., and H. W. Moon. 1997. Pathogenicity of Escherichia coli O157:H7 in the intestines of neonatal calves. Infect. Immun. 65:1842-1848.
17. Dean-Nystrom, E. A., B. T. Bosworth, and H. W. Moon. 1999. Pathogenesis of Escherichia coli O157:H7 in weaned calves. Adv. Exp. Med. Biol. 473:173-177.
18. Echeverry, A., G. H. Loneragan, B. A. Wagner, and M. M. Brashears. 2005. Effect of intensity of fecal pat sampling on estimates of E. coli O157 prevalence. Am. J. Vet. Res. 66:2023-2027.
19. Elder, R. O., J. E. Keen, G. R. Siragusa, G. A. Barkocy-Gallagher, M. Koohmaraie, and W. W. Laegreid. 2000. Correlation of enterohemorrhagic Escherichia coli O157 prevalence in feces, hides, and carcass of beef cattle during processing. Proc. Natl. Acad. Sci. USA 97:2999-3003.
20. Food and Drug Administration, United States Department of Health and Human Services. 2001. Bacteriological analytical manual. http://vm.cfsan.fda. gov/~ebam/bam-toc.html. Accessed 20 September 2006.
21. Food Safety Inspection Service, United States Department of Agriculture. 2008. Detection, isolation and identification of Escherichia coli O157:H7 from meat products. http://www.fsis.usda.gov/PDF/MLG-5-04.pdf. Accessed 13 May 2008.
22. Galland, J. C., D. R. Hyatt, S. S. Crupper, and D. W. Acheson. 2001. Prevalence, antibiotic susceptibility, and diversity of Escherichia coli O157:H7 isolates from a longitudinal study of beef cattle feedlots. Appl. Environ. Microbiol. 67:1619-1627.
23. Girard, F., F. Dziva, P. van Diemen, A. D. Phillips, M. P. Stevens, and G. Frankel. 2007. Adherence of enterohemorrhagic Escherichia coli O157, O26, and O111 strains to bovine intestinal explants ex vivo. Appl. Environ. Microbiol. 73:3084-3090.
24. Grauke, L. J., I. T. Kudva, J. W. Yoon, C. W. Hunt, C. J. Williams, and C. J. Hovde. 2002. Gastrointestinal tract location of Escherichia coli O157:H7 in ruminants. Appl. Environ. Microbiol. 68:2269-2277.
25. Gyles, C. L. 2007. Shiga toxin-producing Escherichia coli: an overview. J. Anim. Sci. 85:E45-E62.
26. Hu, Y., Q. Zhang, and J. C. Meitzler. 1999. Rapid and sensitive detection of Escherichia coli O157:H7 in bovine faeces by a multiplex PCR. J. Appl. Microbiol. 87:867-876.
27. Hunter, S. B., P. Vauterin, M. A. Lambert-Fair, M. S. Van Duyne, K. Kubota, L. Graves, D. Wrigley, T. Barrett, and E. Ribot. 2005. Establishment of a universal size strain for use with the PulseNet standardized pulsed-field gel electrophoresis protocols: converting the national databases to the new size standard. J. Clin. Microbiol. 43:1045-1050.
28. Hussein, H. S. 2007. Prevalence and pathogenicity of Shiga toxin-producing Escherichia coli in beef cattle and their products. J. Anim. Sci. 85(Suppl. E):E63-E72.
29. Hussein, H. S., and L. M. Bollinger. 2005. Prevalence of Shiga toxin-producing Escherichia coli in beef cattle. J. Food Prot. 68:2224-2241.
30. Kaper, J. B., J. P. Nataro, and H. L. T. Mobley. 2004. Pathogenic Escherichia coli. Nat. Rev. 2:123-140.
31. Khaitsa, M. L., D. R. Smith, J. A. Stoner, A. M. Parkhurst, S. Hinkley, T. J. Klopfenstein, and R. A. Moxley. 2003. Incidence, duration, and prevalence of Escherichia coli O157:H7 fecal shedding by feedlot cattle during the finishing period. J. Food Prot. 66:1972-1977.
32. Laven, R. A., A. Ashmore, and C. S. Stewart. 2003. Escherichia coli in the rumen and colon of slaughter cattle, with particular reference to E. coli O157. Vet. J. 165:78-83. (Pubitemid 37555037)
33. LeJeune, J. T., T. E. Besser, D. H. Rice, J. L. Berg, R. P. Stillborn, and D. D. Hancock. 2004. Longitudinal study of fecal shedding of Escherichia coli O157:H7 in feedlot cattle: predominance and persistence of specific clonal types despite massive cattle turnover. Appl. Environ. Microbiol. 70:377-384.
34. Low, J. C., I. J. McKendrick, C. McKechnie, D. Fenlon, S. N. Naylor, C. Currie, D. G. E. Smith, L. Allison, and D. L. Gally. 2005. Rectal carriage of enterohemorrhagic Escherichia coli O157 in slaughtered cattle. J. Appl. Microbiol. 71:93-97.
35. Matthews, L., I. J. McKendrick, H. Ternent, G. J. Gunn, B. Synge, and M. E. J. Woolhouse. 2006. Super-shedding cattle and the transmission dynamics of Escherichia coli O157. Epidemiol. Infect. 134:131-142
36. Matthews, L., J. C. Low, D. L. Gally, M. C. Pearce, D. J. Mellor, J. A. P. Heesterbeek, M. Chase-Topping, S. W. Naylor, D. J. Shaw, S. W. J. Reid, G. J. Gunn, and M. E. J. Woolhouse. 2006. Heterogeneous shedding of Escherichia coli O157 in cattle and its implications for control. Proc. Natl. Acad. Sci. USA 103:547-552.
37. Mead, P. S., and P. M. Griffin. 1998. Escherichia coli O157:H7. Lancet 352:1207-1212.
38. Mead, P. S., L. Slutsker, V. Dietz, L. F. McCraig, J. S. Bresee, C. Shapiro, P. M. Griffin, and R. V. Tauxe. 1999. Food-related illnesses and death in the United States. Emerg. Infect. Dis. 5:607-625.
39. Minihan, D., M. O'Mahony, P. Whyte, and J. D. Collins. 2003. An investigation on the effect of transport and lairage on the fecal shedding prevalence of Escherichia coli O157 in cattle. J. Vet. Med. 50:378-382.
40. Naylor, S. W., J. C. Low, T. E. Besser, A. Mahajan, G. J. Gunn, M. C. Pearce, I. J. McKendrick, G. E. Smith, and D. L. Gally. 2003. Lymphoid follicle-dense mucosa at the terminal rectum is the principal site of colonization of enterhemorrhagic Escherichia coli O157:H7 in the bovine host. Infect. Immun. 71:1505-1512.
41. Rasmussen, M. A., W. C. Cray, T. A. Casey, and S. C. Whipp. 1993. Rumen contents as a reservoir of enterohemorrhagic Escherichia coli serotype O157: H7. FEMS Microbiol. Lett. 114:79-84.
42. Ray, P. E., and X. H. Lui. 2001. Pathogenesis of Shiga toxin-induced hemolytic uremic syndrome. Pediatr. Nephrol. 16:823-839.
43. Riley, L. W., R. S. Remis, S. D. Helgerson, H. B. McGee, J. G. Wells, B. R. Davis, R. J. Hebert, E. S. Olcott, L. M. Johnson, N. T. Hargrett, P. A. Blake, and M. L. Cohen. 1983. Hemorrhagic colitis associated with a rare Escherichia coli serotype. N. Engl. J. Med. 308:681-685.
44. Robinson, S. E., E. J. Wright, C. A. Hart, M. Bennett, and N. P. French. 2004. Intermittent and persistent shedding of Escherichia coli O157 in cohorts of naturally infected calves. J. Appl. Microbiol. 97:1045-1053.
45. Sanderson, M. W., T. E. Besser, J. M. Gay, C. C. Gay, and D. D. Hancock. 1999. Fecal Escherichia coli O157:H7 shedding patterns of orally inoculated calves. Vet. Microbiol. 69:199-205.
46. Scott, L., P. McGee, D. Minihan, J. J. Sheridan, B. Earley, and N. Leonard. 2006. The characterization of E. coli O157:H7 isolates from cattle faeces and feedlot environment using PFGE. Vet. Microbiol. 114:331-336.
47. Sheng, H., M. A. Davis, H. J. Knecht, and C. J. Hovde. 2004. Rectal administration of Escherichia coli O157:H7: novel model for colonization of ruminants. Appl. Environ. Microbiol. 70:4588-4595.
48. Sheng, H., J. Y. Lim, H. J. Knecht, J. Li, and C. J. Hovde. 2006. Role of Escherichia coli O157:H7 virulence factors in colonization at the bovine terminal rectal mucosa. Infect. Immun. 74:4685-4693.
49. Shere, J. A., K. J. Bartlett, and C. W. Kaspar. 1998. Longitudinal study of Escherichia coli O157:H7 dissemination on four dairy farms in Wisconsin. Appl. Environ. Microbiol. 64:1390-1399.
50. Reference deleted.
51. Stanford, K., D. Croy, S. J. Bach, G. L. Williams, H. Zahiroddini, and T. A. McAllister. 2005a. Ecology of Escherichia coli O157:H7 in commercial dairies in southern Alberta. J. Dairy Sci. 88:4441-4451.
52. Stanford, K., S. J. Bach, T. H. Marx, S. Jones, J. R. Hansen, G. L. Wallins, H. Zahiroddini, and T. A. McAllister. 2005b. Monitoring Escherichia coli O157:H7 in inoculated and naturally colonized feedlot cattle and their environment. J. Food Prot. 68:26-33.
53. Stoffregen, W. C., J. F. L. Pohlenz, and E. A. Dean-Nystrom. 2004. Escherichia coli O157:H7 in the gall bladders of experimentally infected calves. J. Vet. Diagn. Investig. 16:79-84.
54. Tenover, F. C., R. D. Arbeit, R. V. Goering, P. A. Mickelson, B. A. Murray, D. A. Persing, and B. Swaminathan. 1995. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J. Clin. Microbiol. 33:2233-2239.
55. Tkalcic, S., C. A. Brown, B. G. Harmon, A. V. Jain, E. P. Mueller, A. Parks, K. L. Jacobsen, S. A. Martin, T. Zhao, and M. P. Doyle. 2000. Effects of diet on rumen proliferation and fecal shedding of Escherichia coli O157:H7 in calves. J. Food Prot. 63:1630-1636.
56. Van Donkersgoed, J., T. Graham, and V. Gannon. 1999. The prevalence of verotoxins, Escherichia coli O157:H7, and Salmonella in the feces and rumen of cattle at processing. Can. Vet. J. 40:332-338.
57. Van Donkersgoed, J., J. Berg, A. Potter, D. Hancock, T. Besser, D. Rice, J. LeJeune, and S. Klashinsky. 2001. Environmental sources and transmission of Escherichia coli O157 in feedlot cattle. Can. Vet. J. 42:714-720.
58. Woerner, D. R., J. R. Ransom, J. N. Sofos, G. A. Dewell, G. C. Smith, M. D. Salman, and K. E. Belk. 2006. Determining the prevalence of Escherichia coli O157 in cattle and beef from the feedlot to the cooler. 2006. J. Food Prot. 69:2824-2827.