Differential virulence of clinical and bovine-biased enterohemorrhagic Escherichia coli O157:H7 genotypes in piglet and dutch belted rabbit models

Infection and Immunity

Volumn 80, Issue 1, 2012, Pages 369-380

  Shringi, Smriti ^a   García, Alexis ^b   Lahmers, Kevin K ^a   Potter, Kathleen A ^a   Muthupalani, Sureshkumar ^b   Swennes, Alton G ^b   Hovde, Carolyn J ^c   Call, Douglas R ^a   Fox, James G ^b   Besser, Thomas E ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF IDAHO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; STX 2 PROTEIN; STX 2C PROTEIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR; BACTERIAL DNA; SHIGA TOXIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM CULTURE; CELL INFILTRATION; CONTROLLED STUDY; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; GENETIC VARIABILITY; GENOTYPE; HISTOPATHOLOGY; INTESTINE; KIDNEY; LEUKOCYTE; NONHUMAN; PIGLET; PRIORITY JOURNAL; RABBIT; ANIMAL; ANIMAL DISEASE; CATTLE; DISEASE MODEL; ESCHERICHIA COLI O157; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; NEWBORN; PATHOGENICITY; PROPHAGE; SURVIVAL; SWINE; VIRULENCE;

ANIMALS; ANIMALS, NEWBORN; CATTLE; DISEASE MODELS, ANIMAL; DNA, BACTERIAL; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI O157; GENOTYPE; HUMANS; PROPHAGES; RABBITS; SHIGA TOXINS; SURVIVAL ANALYSIS; SWINE; VIRULENCE;

EID: 84857093909     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05470-11     Document Type: Article

References (76)

1. Abu-Ali GS, et al. 2010. Increased adherence and expression of virulence genes in a lineage of Escherichia coli O157:H7 commonly associated with human infections. PLoS One 5:e10167.
2. Bach SJ, McAllister TA, Veira DM, Gannon VPJ, Holley RA. 2002. Transmission and control of Escherichia coli O157:H7-a review. Can. J. Anim. Sci. 82:475- 490.
3. Baker DR, et al. 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.
4. Besser RE, Griffin PM, Slutsker L. 1999. Escherichia coli O157:H7 gastroenteritis and the hemolytic uremic syndrome: an emerging infectious disease. Annu. Rev. Med. 50:355-367.
5. Besser TE, et al. 2007. Greater diversity of Shiga toxin-encoding bacteriophage insertion sites among Escherichia coli O157:H7 isolates from cattle than in those from humans. Appl. Environ. Microbiol. 73:671- 679.
6. Borczyk AA, Karmali MA, Lior H, Duncan LM. 1987. Bovine reservoir for verotoxin-producing Escherichia coli O157:H7. Lancet i:98.
7. Centers for Disease Control and Prevention. 1999. One-day (24-28 h) standardized laboratory protocol for molecular subtyping of Escherichia coli serotype O157 by pulsed field gel electrophoresis (PFGE). PulseNet, the National Molecular Subtyping Network for Foodborne Disease Surveillance, Centers for Disease Control and Prevention, Atlanta, GA.
8. Centers for Disease Control and Prevention. 2009. Preliminary FoodNet data on the incidence of infection with pathogens transmitted commonly through food-10 states, 2008. MMWR Morb. Mortal. Wkly. Rep. 58: 333-337.
9. Centers for Disease Control and Prevention. 2010. Surveillance for foodborne disease outbreaks-United States, 2007. MMWR Morb. Mortal. Wkly. Rep. 59:973-979.
10. Centers for Disease Control and Prevention. 2009. Surveillance for foodborne disease outbreaks-United States, 2006. MMWR Morb. Mortal. Wkly. Rep. 58:609-615.
11. Cornick NA, Vukhac H. 2008. Indirect transmission of Escherichia coli O157:H7 occurs readily among swine but not among sheep. Appl. Environ. Microbiol. 74:2488 -2491.
12. Creuzburg K, et al. 2005. Genetic structure and chromosomal integration site of the cryptic prophage CP-1639 encoding Shiga toxin 1. Microbiology 151:941-950.
13. Davis MA, Hancock DD, Besser TE, Call DR. 2003. Evaluation of pulsed-field gel electrophoresis as a tool for determining the degree of genetic relatedness between strains of Escherichia coli O157:H7. J. Clin. Microbiol. 41:1843-1849.
14. Dean-Nystrom EA, Pohlenz JF, Moon HW, O'Brien AD. 2000. Escherichia coli O157:H7 causes more-severe systemic disease in suckling piglets than in colostrum-deprived neonatal piglets. Infect. Immun. 68: 2356-2358.
15. 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.
16. Donnenberg MS, et al. 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.
17. 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.
18. 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.
19. Fuller CA, Pellino CA, Flagler MJ, Strasser JE, Weiss AA. 2011. Shiga toxin subtypes display dramatic differences in potency. Infect. Immun. 79:1329 -1337.
20. García A, et al. 2006. Renal injury is a consistent finding in Dutch Belted rabbits experimentally infected with enterohemorrhagic Escherichia coli. J. Infect. Dis. 193:1125-1134.
21. García A, Fox JG, Besser TE. 2010. Zoonotic enterohemorrhagic Escherichia coli: a one health perspective. ILAR J. 51:221-232.
22. Gentry PA. 1999. Acute phase proteins, p 336-398. In Loeb WF, Quimby FW (ed), The clinical chemistry of laboratory animals, 2nd ed. Taylor and Francis, Philadelphia, PA.
23. 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.
24. Gunzer F, et al. 2002. Gnotobiotic piglets develop thrombotic microangiopathy after oral infection with enterohemorrhagic Escherichia coli. Am. J. Clin. Pathol. 118:364 -375.
25. Hayashi T, 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.
26. Hintzee J. 2007. NCSS 2007. NCSS, LLC. Kaysville, UT.
27. Ikeda K, et al. 2000. Predictors for the development of haemolytic uraemic syndrome with Escherichia coli O157:H7 infections: with focus on the day of illness. Epidemiol. Infect. 124:343-349.
28. Kailasan Vanaja S, Bergholz TM, Whittam TS. 2009. Characterization of the Escherichia coli O157:H7 Sakai GadE regulon. J. Bacteriol. 191: 1868-1877.
29. Karmali MA. 2004. Infection by Shiga toxin-producing Escherichia coli: an overview. Mol. Biotechnol. 26:117-122.
30. Karmali MA, Petric M, Bielaszewska M. 1999. Evaluation of a microplate latex agglutination method (Verotox-F assay) for detecting and characterizing verotoxins (Shiga toxins) in Escherichia coli. J. Clin. Microbiol. 37: 396-399.
31. Karmali MA, et al. 1985. The association between idiopathic hemolytic uremic syndrome and infection by verotoxin-producing Escherichia coli. J. Infect. Dis. 151:775-782.
32. 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 i:619-620.
33. 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. U. S. A. 96:13288 -13293.
34. Kim J, et al. 2001. Ancestral divergence, genome diversification, and phylogeographic variation in subpopulations of sorbitol-negative, betaglucuronidase- negative enterohemorrhagic Escherichia coli O157. J. Bacteriol. 183:6885- 6897.
35. Koch C, Hertwig S, Appel B. 2003. Nucleotide sequence of the integration site of the temperate bacteriophage 6220, which carries the Shiga toxin gene stx(1ox3). J. Bacteriol. 185:6463- 6466.
36. Kotewicz ML, Mammel MK, LeClerc JE, Cebula TA. 2008. Optical mapping and 454 sequencing of Escherichia coli O157:H7 isolates linked to the US 2006 spinach-associated outbreak. Microbiology 154:3518 -3528.
37. Laing CR, et al. 2009. In silico genomic analyses reveal three distinct lineages of Escherichia coli O157:H7, one of which is associated with hypervirulence. BMC Genomics 10:287.
38. Law D. 2000. Virulence factors of Escherichia coli O157 and other Shiga toxin-producing E. coli. J. Appl. Microbiol. 88:729 -745.
39. Lefebvre B, Diarra MS, Vincent C, Moisan H, Malouin F. 2009. Relative cytotoxicity of Escherichia coli O157:H7 isolates from beef cattle and humans. Foodborne Pathog. Dis. 6:357-364.
40. Liu B, et al. 2010. Verotoxin 2 enhances adherence of enterohemorrhagic Escherichia coli O157:H7 to intestinal epithelial cells and expression of {beta}1-integrin by IPEC-J2 cells. Appl. Environ. Microbiol. 76: 4461-4468.
41. Manning SD, et al. 2008. Variation in virulence among clades of Escherichia coli O157:H7 associated with disease outbreaks. Proc. Natl. Acad. Sci. U. S. A. 105:4868-4873.
42. Mead PS, Griffin PM. 1998. Escherichia coli O157:H7. Lancet 352: 1207-1212.
43. Muniesa M, et al. 2003. Shiga toxin 2-converting bacteriophages associated with clonal variability in Escherichia coli O157:H7 strains of human origin isolated from a single outbreak. Infect. Immun. 71:4554-4562.
44. Nathanson S, et al. 2010. Acute neurological involvement in diarrheaassociated hemolytic uremic syndrome. Clin. J. Am. Soc. Nephrol. 5:1218 -1228.
45. Naylor SW, et al. 2005. Escherichia coli O157:H7 forms attaching and effacing lesions at the terminal rectum of cattle and colonization requires the LEE4 operon. Microbiology 151:2773-2781.
46. Oakes RS, Siegler RL, McReynolds MA, Pysher T, Pavia AT. 2006. Predictors of fatality in postdiarrheal hemolytic uremic syndrome. Pediatrics 117:1656 -1662.
47. Ohnishi M, et al. 2002. Genomic diversity of enterohemorrhagic Escherichia coli O157 revealed by whole genome PCR scanning. Proc. Natl. Acad. Sci. U. S. A. 99:17043-17048.
48. Orth D, et al. 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.
49. Paton JC, Paton AW. 1998. Pathogenesis and diagnosis of Shiga toxinproducing Escherichia coli infections. Clin. Microbiol. Rev. 11:450-479.
50. Perna NT, et al. 1998. Molecular evolution of a pathogenicity island from enterohemorrhagic Escherichia coli O157:H7. Infect. Immun. 66: 3810-3817.
51. Perna NT, et al. 2001. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409:529 -533.
52. Pohlenz JF, Winter KR, Dean-Nystrom EA. 2005. Shiga-toxigenic Escherichia coli-inoculated neonatal piglets develop kidney lesions that are comparable to those in humans with hemolytic-uremic syndrome. Infect. Immun. 73:612- 616.
53. Rangel JM, Sparling PH, Crowe C, Griffin PM, Swerdlow DL. 2005. Epidemiology of Escherichia coli O157:H7 outbreaks, United States, 1982-2002. Emerg. Infect. Dis. 11:603- 609.
54. 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.
55. Ritchie JM, Thorpe CM, Rogers AB, Waldor MK. 2003. Critical roles for stx2, eae, and tir in enterohemorrhagic Escherichia coli-induced diarrhea and intestinal inflammation in infant rabbits. Infect. Immun. 71: 7129-7139.
56. Ritchie JM, Wagner PL, Acheson DW, Waldor MK. 2003. Comparison of Shiga toxin production by hemolytic-uremic syndrome-associated and bovine-associated Shiga toxin-producing Escherichia coli isolates. Appl. Environ. Microbiol. 69:1059 -1066.
57. Robinson CM, Sinclair JF, Smith MJ, O'Brien AD. 2006. Shiga toxin of enterohemorrhagic Escherichia coli type O157:H7 promotes intestinal colonization. Proc. Natl. Acad. Sci. U. S. A. 103:9667-9672.
58. Robson WL, Leung AK, Montgomery MD. 1991. Causes of death in hemolytic uremic syndrome. Child Nephrol. Urol. 11:228 -233.
59. Scallan E, et al. 2011. Foodborne illness acquired in the United States-major pathogens. Emerg. Infect. Dis. 17:7-15.
60. Shaikh N, Tarr PI. 2003. Escherichia coli O157:H7 Shiga toxin-encoding bacteriophages: integrations, excisions, truncations, and evolutionary implications. J. Bacteriol. 185:3596 -3605.
61. Sheng H, Lim JY, Knecht HJ, Li J, Hovde CJ. 2006. Role of Escherichia coli O157:H7 virulence factors in colonization at the bovine terminal rectal mucosa. Infect. Immun. 74:4685- 4693.
62. Shimizu K, et al. 2003. Development of a lethal Shiga toxin-producing Escherichia coli-infection mouse model using multiple mitomycin C treatment. Microb. Pathog. 35:1-9.
63. Shin S, et al. 2001. An activator of glutamate decarboxylase genes regulates the expression of enteropathogenic Escherichia coli virulence genes through control of the plasmid-encoded regulator, Per. Mol. Microbiol. 41:1133-1150.
64. Tarr PI, Gordon CA, Chandler WL. 2005. Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet 365:1073-1086.
65. Tatsuno I, et al. 2003. Increased adherence to Caco-2 cells caused by disruption of the yhiE and yhiF genes in enterohemorrhagic Escherichia coli O157:H7. Infect. Immun. 71:2598 -2606.
66. Tenover FC, et al. 1995. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J. Clin. Microbiol. 33:2233-2239.
67. Tzipori S, Chow CW, Powell HR. 1988. Cerebral infection with Escherichia coli O157:H7 in humans and gnotobiotic piglets. J. Clin. Pathol. 41:1099 -1103.
68. Vanaja SK, Springman AC, Besser TE, Whittam TS, Manning SD. 2010. Differential expression of virulence and stress fitness genes between Escherichia coli O157:H7 strains with clinical or bovine-biased genotypes. Appl. Environ. Microbiol. 76:60-68.
69. Watanabe M, et al. 2004. Oral therapeutic agents with highly clustered globotriose for treatment of Shiga toxigenic Escherichia coli infections. J. Infect. Dis. 189:360 -368.
70. Whitworth J, et al. 2010. Diverse genetic markers concordantly identify bovine origin Escherichia coli O157 genotypes underrepresented in human disease. Appl. Environ. Microbiol. 76:361-365.
71. Whitworth JH, et al. 2008. International comparison of clinical, bovine, and environmental Escherichia coli O157 isolates on the basis of Shiga toxin-encoding bacteriophage insertion site genotypes. Appl. Environ. Microbiol. 74:7447-7450.
72. Wick LM, Qi W, Lacher DW, Whittam TS. 2005. Evolution of genomic content in the stepwise emergence of Escherichia coli O157:H7. J. Bacteriol. 187:1783-1791.
73. Wieler LH, et al. 1996. Shiga toxin-producing Escherichia coli strains from bovines: association of adhesion with carriage of eae and other genes. J. Clin. Microbiol. 34:2980 -2984.
74. Yang Z, et al. 2004. Identification of common subpopulations of nonsorbitol- fermenting, beta-glucuronidase-negative Escherichia coli O157:H7 from bovine production environments and human clinical samples. Appl. Environ. Microbiol. 70:6846-6854.
75. Yoshii N, et al. 2009. Pulsed-field gel electrophoresis profile changes resulting from spontaneous chromosomal deletions in enterohemorrhagic Escherichia coli O157:H7 during passage in cattle. Appl. Environ. Microbiol. 75:5719 -5726.
76. Zhang Y, et al. 2007. Genome evolution in major Escherichia coli O157:H7 lineages. BMC Genomics 8:121.