Advertisement

The Benefit of a Plant-Based Cattle Vaccine for Reducing Enterohemorrhagic Escherichia Coli Shedding and Improving Food Safety

  • Adam Chin-Fatt
  • Ed Topp
  • Rima Menassa
Chapter

Abstract

Upon ingestion, enterohemorrhagic Escherichia coli (EHEC) can colonize intestinal mucosa and cause hemorrhaging of nearby tissue. The failure to adequately control its contamination of food and water can consequently compromise the health of a population and incur economic losses to all stages of the food supply chain. EHEC is currently one of the foremost foodborne pathogenic threats worldwide because of its virulence across all age groups and demographics, a low infective dose, a relatively high resilience in diverse environments and its widespread prevalence across cattle herds. EHEC primarily colonizes the bovine digestive tract from which it can be transmitted via fecal shedding or during slaughter. Considering its threat to food security and in accord with the ‘One Health’ framework, the development of a bovine vaccine as a pre-harvest intervention strategy to curtail the transmission of EHEC is of great interest. Although two EHEC vaccines have already been developed using bacterial production platforms, their market penetrance has been markedly low. As an alternative, production in a plant platform may have the potential to redress the reasons for this low penetrance by providing a better economy of scale and a more convenient mode of delivery. This chapter summarizes the scope of the threat posed by EHEC and discusses the prospects for developing a commercial plant-based vaccine for EHEC within the framework of the North American beef industry.

Keywords

EHEC O157 VTEC STEC Shiga Cattle Vaccine 

References

  1. Amani J, Mousavi SL, Rafati S et al (2011) Immunogenicity of a plant-derived edible chimeric EspA, Intimin and Tir of Escherichia coli O157:H7 in mice. Plant science: an international journal of experimental plant biology 180:620–627CrossRefGoogle Scholar
  2. Baines D, Masson L, Mcallister T (2008) Escherichia coli O157: H7-secreted cytotoxins are toxic to enterocytes and increase Escherichia coli O157: H7 colonization of jejunum and descending colon in cattle. Can J Anim Sci 88:41–50CrossRefGoogle Scholar
  3. Bell BP, Goldoft M, Griffin PM et al (1994) A multistate outbreak of escherichia coli o157: h7—associated bloody diarrhea and hemolytic uremic syndrome from hamburgers: the washington experience. JAMA 272:1349–1353CrossRefPubMedGoogle Scholar
  4. Berry ED, Wells JE, Bono JL et al (2015) Effect of proximity to a cattle feedlot on Escherichia coli O157: H7 contamination of leafy greens and evaluation of the potential for airborne transmission. Appl Environ Microbiol 81:1101–1110CrossRefPubMedPubMedCentralGoogle Scholar
  5. Besser TE, Hancock DD, Pritchett LC et al (1997) Duration of detection of fecal excretion of Escherichia coli 0157: H7 in cattle. J Infect Dis 175:726–729CrossRefPubMedGoogle Scholar
  6. Best A, La Ragione RM, Sayers AR et al (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 73:1836–1846CrossRefPubMedPubMedCentralGoogle Scholar
  7. Beutin L, Geier D, Steinrück H et al (1993) Prevalence and some properties of verotoxin (Shiga-like toxin)-producing Escherichia coli in seven different species of healthy domestic animals. J Clin Microbiol 31:2483–2488PubMedPubMedCentralGoogle Scholar
  8. Boyd B, Lingwood C (1989) Verotoxin receptor glycolipid in human renal tissue. Nephron 51:207–210CrossRefPubMedGoogle Scholar
  9. Burkinshaw BJ, Deng W, Lameignère E et al (2015) Structural analysis of a specialized type III secretion system peptidoglycan-cleaving enzyme. J Biol Chem 290:10406–10417CrossRefPubMedPubMedCentralGoogle Scholar
  10. Büttner D (2012) Protein export according to schedule: architecture, assembly, and regulation of type III secretion systems from plant-and animal-pathogenic bacteria. Microbiol Mol Biol Rev 76:262–310CrossRefPubMedPubMedCentralGoogle Scholar
  11. CDC (2011) Vital signs: incidence and trends of infection with pathogens transmitted commonly through food–foodborne diseases active surveillance network, 10 US sites, 1996–2010. Morb Mortal Wkly Rep 60:749Google Scholar
  12. CDC (2017) Foodborne diseases active surveillance network (FoodNet): FoodNet 2015 Surveillance Report (Final Data). Atlanta, Georgia: U.S. Department of health and human services. https://www.cdc.gov/foodnet/pdfs/FoodNet-Annual-Report-2015-508c.pdf. Accessed 8 Jan 2018
  13. Charatan F (1999) New York outbreak of E coli poisoning affects 1000 and kills two. BMJ. British Medical Journal 319:873CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chong Y, Fitzhenry R, Heuschkel R et al (2007) Human intestinal tissue tropism in Escherichia coli O157: H7–initial colonization of terminal ileum and Peyer’s patches and minimal colonic adhesion ex vivo. Microbiology 153:794–802CrossRefPubMedGoogle Scholar
  15. Cleary TG (2004) The role of Shiga-toxin-producing Escherichia coli in hemorrhagic colitis and hemolytic uremic syndrome. In: Seminars in pediatric infectious diseases. Elsevier, p 260–265CrossRefPubMedGoogle Scholar
  16. Delahay RM, Knutton S, Shaw RK et al (1999) The Coiled-coil Domain of EspA Is Essential for the Assembly of the Type III Secretion Translocon on the Surface of Enteropathogenic Escherichia coli. J Biol Chem 274:35969–35974CrossRefPubMedGoogle Scholar
  17. Donnenberg MS, Tzipori S, Mckee ML 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 92:1418CrossRefPubMedPubMedCentralGoogle Scholar
  18. Doyle M, Archer J, Kaspar C et al (2006) FRI Briefing: human illness caused by E. coli O157: H7 from food and non-food sources. https://fri.wisc.edu/files/Briefs_File/FRIBrief_EcoliO157H7humanillness.pdf. Accessed 08 Jan 2018
  19. Dziva F, Van Diemen PM, Stevens MP et al (2004) Identification of Escherichia coli O157: H7 genes influencing colonization of the bovine gastrointestinal tract using signature-tagged mutagenesis. Microbiology 150:3631–3645CrossRefPubMedGoogle Scholar
  20. Endo Y, Tsurugi K, Lambert JM (1988) The site of action of six different ribosome-inactivating proteins from plants on eukaryotic ribosomes: the RNA N-glycosidase activity of the proteins. Biochem Biophys Res Commun 150:1032–1036CrossRefPubMedGoogle Scholar
  21. Eresearch Corporation NCWB (2012) Initiating Report for BioNiche life sciences Inc. http://www.baystreet.ca/articles/research_reports/eresearch/BNC_011712-I.pdf. Accessed 08 Jan 2018
  22. Fivaz M, Van Der Goot FG (1999) The tip of a molecular syringe. Trends Microbiol 7:341–343CrossRefPubMedGoogle Scholar
  23. Fukushima H, Hashizume T, Morita Y et al (1999) Clinical experiences in Sakai City Hospital during the massive outbreak of enterohemorrhagic Escherichia coli O157 infections in Sakai City, 1996. Pediatr Int 41:213–217CrossRefPubMedGoogle Scholar
  24. 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 6:1167–1183CrossRefPubMedGoogle Scholar
  25. Gill A, Gill CO (2010) Non-O157 verotoxigenic Escherichia coli and beef: a Canadian perspective. Can J Vet Res 74:161–169PubMedPubMedCentralGoogle Scholar
  26. Gould LH, Demma L, Jones TF et al (2009) Hemolytic uremic syndrome and death in persons with Escherichia coli O157: H7 infection, foodborne diseases active surveillance network sites, 2000–2006. Clin Infect Dis 49:1480–1485CrossRefPubMedGoogle Scholar
  27. Grier K, Schmidt C (2009) E. coli 0157 risk reduction: economic benefit to Canada. George Morris CentreGoogle Scholar
  28. Griffin P (1995) Escherichia coli O157: H7 and other enterohemorrhagic Escherichia coli. Infections of the gastrointestinal tract:739–761Google Scholar
  29. Griffin PM, Olmstead LC, Petras RE (1990) Escherichia coli O157: H7-associated colitis. Gastroenterology 99:142–149CrossRefPubMedGoogle Scholar
  30. 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 13:60–98CrossRefPubMedGoogle Scholar
  31. 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 51:1233–1249CrossRefPubMedGoogle Scholar
  32. Hale CR, Scallan E, Cronquist AB et al (2012) Estimates of enteric illness attributable to contact with animals and their environments in the United States. Clin Infect Dis 54:S472–S479CrossRefPubMedGoogle Scholar
  33. Heuvelink A, Van Heerwaarden C, Zwartkruis-Nahuis J et al (2002) Escherichia coli O157 infection associated with a petting zoo. Epidemiol Infect 129:295–302CrossRefPubMedPubMedCentralGoogle Scholar
  34. Hrudey S, Payment P, Huck P et al (2003) A fatal waterborne disease epidemic in Walkerton, Ontario: comparison with other waterborne outbreaks in the developed world. Water Sci Technol 47:7–14CrossRefPubMedGoogle Scholar
  35. Ismaili A, Philpott DJ, Dytoc MT et al (1995) Signal transduction responses following adhesion of verocytotoxin-producing Escherichia coli. Infect Immun 63:3316–3326PubMedPubMedCentralGoogle Scholar
  36. Jacewicz MS, Acheson D, Mobassaleh M et al (1995) Maturational regulation of globotriaosylceramide, the Shiga-like toxin 1 receptor, in cultured human gut epithelial cells. J Clin Invest 96:1328CrossRefPubMedPubMedCentralGoogle Scholar
  37. Jarvis KG, Giron JA, Jerse AE et al (1995) Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching and effacing lesion formation. Proc Natl Acad Sci 92:7996–8000CrossRefPubMedGoogle Scholar
  38. Jarvis KG, Kaper JB (1996) Secretion of extracellular proteins by enterohemorrhagic Escherichia coli via a putative type III secretion system. Infect Immun 64:4826–4829PubMedPubMedCentralGoogle Scholar
  39. Jiang X, Morgan J, Doyle MP (2002) Fate of Escherichia coli O157: H7 in manure-amended soil. Appl Environ Microbiol 68:2605–2609CrossRefPubMedPubMedCentralGoogle Scholar
  40. Judge NA, Mason HS, O’brien AD (2004) Plant cell-based intimin vaccine given orally to mice primed with intimin reduces time of Escherichia coli O157:H7 shedding in feces. Infect Immun 72:168–175CrossRefPubMedPubMedCentralGoogle Scholar
  41. Kandel G, Donohue-Rolfe A, Donowitz M et al (1989) Pathogenesis of Shigella diarrhea. XVI. Selective targetting of Shiga toxin to villus cells of rabbit jejunum explains the effect of the toxin on intestinal electrolyte transport. J Clin Invest 84:1509CrossRefPubMedPubMedCentralGoogle Scholar
  42. Karmali M, Petric M, Lim C et al (1983) Escherichia coli cytotoxin, haemolytic-uraemic syndrome, and haemorrhagic colitis. The Lancet 322:1299–1300CrossRefGoogle Scholar
  43. Karmali MA (2004) Prospects for preventing serious systemic toxemic complications of Shiga toxin–producing Escherichia coli infections using Shiga toxin receptor analogues. J Infect Dis 189:355–359CrossRefPubMedGoogle Scholar
  44. Kenny B, Devinney R, Stein M et al (1997) Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91:511–520CrossRefPubMedGoogle Scholar
  45. Kenny B, Finlay BB (1995) Protein secretion by enteropathogenic Escherichia coli is essential for transducing signals to epithelial cells. Proc Natl Acad Sci 92:7991–7995CrossRefPubMedGoogle Scholar
  46. 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 2:160–171CrossRefPubMedGoogle Scholar
  47. Knutton S, Baldwin T, Williams P et al (1989) Actin accumulation at sites of bacterial adhesion to tissue culture cells: basis of a new diagnostic test for enteropathogenic and enterohemorrhagic Escherichia coli. Infect Immun 57:1290–1298PubMedPubMedCentralGoogle Scholar
  48. Kolotilin I, Kaldis A, Devriendt B et al (2012) Production of a subunit vaccine candidate against porcine post-weaning diarrhea in high-biomass transplastomic tobacco. PLoS ONE 7:e42405CrossRefPubMedPubMedCentralGoogle Scholar
  49. Kwon K-C, Verma D, Singh ND et al (2013) Oral delivery of human biopharmaceuticals, autoantigens and vaccine antigens bioencapsulated in plant cells. Adv Drug Deliv Rev 65:782–799CrossRefPubMedGoogle Scholar
  50. La Ragione R, Ahmed NM, Best A et al (2005) Colonization of 8-week-old conventionally reared goats by Escherichia coli O157: H7 after oral inoculation. J Med Microbiol 54:485–492CrossRefPubMedGoogle Scholar
  51. La Ragione R, 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 55:819–828CrossRefPubMedGoogle Scholar
  52. Lai L-C, Wainwright LA, Stone KD et al (1997) A third secreted protein that is encoded by the enteropathogenic Escherichia coli pathogenicity island is required for transduction of signals and for attaching and effacing activities in host cells. Infect Immun 65:2211–2217PubMedPubMedCentralGoogle Scholar
  53. Lejeune JT, Besser TE, Hancock DD (2001) Cattle water troughs as reservoirs of Escherichia coli O157. Appl Environ Microbiol 67:3053–3057CrossRefPubMedPubMedCentralGoogle Scholar
  54. Lim JY, Li J, Sheng H et al (2007) Escherichia coli O157: H7 colonization at the rectoanal junction of long-duration culture-positive cattle. Appl Environ Microbiol 73:1380–1382CrossRefPubMedGoogle Scholar
  55. Louise CB, Tran MC, Obrig TG (1997) Sensitization of human umbilical vein endothelial cells to Shiga toxin: involvement of protein kinase C and NF-kappaB. Infect Immun 65:3337–3344PubMedPubMedCentralGoogle Scholar
  56. Macdonald J, Miletic S, Gaildry T et al (2017) Co-expression with the Type 3 Secretion Chaperone CesT from Enterohemorrhagic E. coli Increases Accumulation of Recombinant Tir in Plant Chloroplasts. Frontiers in Plant Science 8Google Scholar
  57. Majowicz SE, Scallan E, Jones-Bitton A et al (2014) Global incidence of human Shiga toxin–producing Escherichia coli infections and deaths: a systematic review and knowledge synthesis. Foodborne pathogens and disease 11:447–455CrossRefPubMedPubMedCentralGoogle Scholar
  58. Mathusa EC, Chen Y, Enache E et al (2010) Non-O157 Shiga toxin-producing Escherichia coli in foods. J Food Prot 73:1721–1736CrossRefPubMedGoogle Scholar
  59. Matthews L, Reeve R, Gally DL et al (2013) Predicting the public health benefit of vaccinating cattle against Escherichia coli O157. Proc Natl Acad Sci 110:16265–16270CrossRefPubMedGoogle Scholar
  60. Mckee ML, O’brien AD (1996) Truncated enterohemorrhagic Escherichia coli (EHEC) O157: H7 intimin (EaeA) fusion proteins promote adherence of EHEC strains to HEp-2 cells. Infect Immun 64:2225–2233PubMedPubMedCentralGoogle Scholar
  61. Miletic S, Hunerberg M, Kaldis A et al (2017) A Plant-produced candidate subunit vaccine reduces shedding of enterohemorrhagic Escherichia coli in Ruminants. Biotechnol J 12Google Scholar
  62. Montenegro MA, Bülte M, Trumpf T et al (1990) Detection and characterization of fecal verotoxin-producing Escherichia coli from healthy cattle. J Clin Microbiol 28:1417–1421PubMedPubMedCentralGoogle Scholar
  63. Moon H, Whipp S, Argenzio R et al (1983) Attaching and effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines. Infect Immun 41:1340–1351PubMedPubMedCentralGoogle Scholar
  64. Nart P, Naylor SW, Huntley JF et al (2008) Responses of cattle to gastrointestinal colonization by Escherichia coli O157:H7. Infect Immun 76:5366–5372CrossRefPubMedPubMedCentralGoogle Scholar
  65. Naylor SW, Low JC, Besser TE et al (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 71:1505–1512CrossRefPubMedPubMedCentralGoogle Scholar
  66. Ochieng’ BJ, Hobbs JE (2017) Factors affecting cattle producers’ willingness to adopt an Escherichia coli O157: H7 vaccine: a probit analysis. International Food and Agribusiness Management Review 20:347–363CrossRefGoogle Scholar
  67. Omisakin F, Macrae M, Ogden I et al (2003) Concentration and prevalence of Escherichia coli O157 in cattle feces at slaughter. Appl Environ Microbiol 69:2444–2447CrossRefPubMedPubMedCentralGoogle Scholar
  68. Pai C, Kelly J, Meyers G (1986) Experimental infection of infant rabbits with verotoxin-producing Escherichia coli. Infect Immun 51:16–23PubMedPubMedCentralGoogle Scholar
  69. Pelosi A, Piedrafita D, De Guzman G et al (2012) The effect of plant tissue and vaccine formulation on the oral immunogenicity of a model plant-made antigen in sheep. PLoS ONE 7:e52907CrossRefPubMedPubMedCentralGoogle Scholar
  70. Perna NT, Mayhew GF, Pósfai G et al (1998) Molecular evolution of a pathogenicity island from enterohemorrhagic Escherichia coli O157: H7. Infect Immun 66:3810–3817PubMedPubMedCentralGoogle Scholar
  71. Phillips A, Navabpour S, Hicks S et al (2000) Enterohaemorrhagic Escherichia coliO157: H7 target Peyer9 s patches in humans and cause attaching/effacing lesions in both human and bovine intestine. Gut 47:377–381CrossRefPubMedPubMedCentralGoogle Scholar
  72. Pruimboom-Brees IM, Morgan TW, Ackermann MR et al (2000) Cattle lack vascular receptors for Escherichia coli O157: H7 Shiga toxins. Proc Natl Acad Sci 97:10325–10329CrossRefPubMedGoogle Scholar
  73. Public Health Agency of Canada (2015) Foodnet Canada Short Report 2015. http://publications.gc.ca/site/eng/461265/publication.html. Accessed 08 Jan 2018
  74. Rangel JM, Sparling PH, Crowe C et al (2005a) Epidemiology of Escherichia coli O157: H7 outbreaks, United States, 1982–2002Google Scholar
  75. Rangel JM, Sparling PH, Crowe C et al (2005b) Epidemiology of Escherichia coli O157:H7 outbreaks, United States, 1982-2002. Emerg Infect Dis 11:603–609CrossRefPubMedPubMedCentralGoogle Scholar
  76. Riley LW, Remis RS, Helgerson SD et al (1983) Hemorrhagic colitis associated with a rare Escherichia coli serotype. N Engl J Med 308:681–685CrossRefPubMedGoogle Scholar
  77. Rybicki EP (2010) Plant-made vaccines for humans and animals. Plant Biotechnol J 8:620–637CrossRefPubMedGoogle Scholar
  78. Sanderson MW, Sargeant JM, Shi X et al (2006) Longitudinal emergence and distribution of Escherichia coli O157 genotypes in a beef feedlot. Appl Environ Microbiol 72:7614–7619CrossRefPubMedPubMedCentralGoogle Scholar
  79. Sargeant J, Amezcua M, Rajic A et al (2007) Pre-harvest interventions to reduce the shedding of E. coli O157 in the faeces of weaned domestic ruminants: a systematic review. Zoonoses Public Health 54:260–277CrossRefPubMedGoogle Scholar
  80. Slutsker L, Ries AA, Greene KD et al (1997) Escherichia coli O157: H7 diarrhea in the United States: clinical and epidemiologic features. Ann Intern Med 126:505–513CrossRefPubMedGoogle Scholar
  81. Smith DR, Moxley RA, Klopfenstein TJ et al (2009a) A randomized longitudinal trial to test the effect of regional vaccination within a cattle feedyard on Escherichia coli O157: H7 rectal colonization, fecal shedding, and hide contamination. Foodborne Pathogens and Disease 6:885–892CrossRefPubMedGoogle Scholar
  82. Smith DR, Moxley RA, Peterson RE et al (2009b) A two-dose regimen of a vaccine against type III secreted proteins reduced Escherichia coli O157: H7 colonization of the terminal rectum in beef cattle in commercial feedlots. Foodborne pathogens and disease 6:155–161CrossRefPubMedGoogle Scholar
  83. Snedeker K, Campbell M, Sargeant J (2012) A systematic review of vaccinations to reduce the shedding of Escherichia coli O157 in the faeces of domestic ruminants. Zoonoses Public Health 59:126–138CrossRefPubMedGoogle Scholar
  84. Stanford K, Stephens TP, Mcallister TA (2011) Use of model super-shedders to define the role of pen floor and hide contamination in the transmission of Escherichia coli O157:H7. J Anim Sci 89:237–244CrossRefPubMedGoogle Scholar
  85. Statistics Canada (2017) Livestock estimates. http://www.statcan.gc.ca/daily-quotidien/170818/dq170818e-eng.htm. Accessed 08 Jan 2018
  86. Stephens TP, Mcallister TA, Stanford K (2009) Perineal swabs reveal effect of super shedders on the transmission of Escherichia coli O157:H7 in commercial feedlots. J Anim Sci 87:4151–4160CrossRefPubMedGoogle Scholar
  87. Strachan NJ, Doyle MP, Kasuga F et al (2005) Dose response modelling of Escherichia coli O157 incorporating data from foodborne and environmental outbreaks. Int J Food Microbiol 103:35–47CrossRefPubMedGoogle Scholar
  88. Tobe T, Beatson SA, Taniguchi H et al (2006) An extensive repertoire of type III secretion effectors in Escherichia coli O157 and the role of lambdoid phages in their dissemination. Proc Natl Acad Sci 103:14941–14946CrossRefPubMedGoogle Scholar
  89. Tuttle J, Gomez T, Doyle M et al (1999) Lessons from a large outbreak of Escherichia coli O157: H7 infections: insights into the infectious dose and method of widespread contamination of hamburger patties. Epidemiol Infect 122:185CrossRefPubMedPubMedCentralGoogle Scholar
  90. Tzipori S, Gibson R, Montanaro J (1989) Nature and distribution of mucosal lesions associated with enteropathogenic and enterohemorrhagic Escherichia coli in piglets and the role of plasmid-mediated factors. Infect Immun 57:1142–1150PubMedPubMedCentralGoogle Scholar
  91. Tzipori S, Gunzer F, Donnenberg MS et al (1995) The role of the eaeA gene in diarrhea and neurological complications in a gnotobiotic piglet model of enterohemorrhagic Escherichia coli infection. Infect Immun 63:3621–3627PubMedPubMedCentralGoogle Scholar
  92. Unicef (2010) Diarrhoea: why children are still dying and what can be done. https://www.unicef.org/media/files/Final_Diarrhoea_Report_October_2009_final.pdf. Accessed 08 Jan 2018
  93. United States Department of Agriculture (2017) Cattle. http://usda.mannlib.cornell.edu/MannUsda/viewDocumentInfo.do?documentID=1017. Accessed 08 Jan 2018
  94. Vial PA, Robins-Browne R, Lior H et al (1988) Characterization of enteroadherent-aggregative Escherichia coli, a putative agent of diarrheal disease. J Infect Dis 158:70–79CrossRefPubMedGoogle Scholar
  95. Wagner PL, Waldor MK (2002) Bacteriophage control of bacterial virulence. Infect Immun 70:3985–3993CrossRefPubMedPubMedCentralGoogle Scholar
  96. Warawa J, Finlay BB, Kenny B (1999) Type III secretion-dependent hemolytic activity of enteropathogenic Escherichia coli. Infect Immun 67:5538–5540PubMedPubMedCentralGoogle Scholar
  97. Wen SX, Teel LD, Judge NA et al (2006a) Genetic toxoids of Shiga toxin types 1 and 2 protect mice against homologous but not heterologous toxin challenge. Vaccine 24:1142–1148CrossRefPubMedGoogle Scholar
  98. Wen SX, Teel LD, Judge NA et al (2006b) A plant-based oral vaccine to protect against systemic intoxication by Shiga toxin type 2. Proc Natl Acad Sci 103:7082–7087CrossRefPubMedGoogle Scholar
  99. Wendel AM, Johnson DH, Sharapov U et al (2009) Multistate outbreak of Escherichia coli O157: H7 infection associated with consumption of packaged spinach, August–September 2006: the Wisconsin investigation. Clin Infect Dis 48:1079–1086CrossRefPubMedGoogle Scholar
  100. Wheeler T, Kalchayanand N, Bosilevac JM (2014) Pre-and post-harvest interventions to reduce pathogen contamination in the US beef industry. Meat Sci 98:372–382CrossRefPubMedGoogle Scholar
  101. Williams MS, Withee JL, Ebel ED et al (2010) Determining relationships between the seasonal occurrence of Escherichia coli O157: H7 in live cattle, ground beef, and humans. Foodborne pathogens and disease 7:1247–1254CrossRefPubMedGoogle Scholar
  102. Wong AR, Pearson JS, Bright MD et al (2011) Enteropathogenic and enterohaemorrhagic Escherichia coli: even more subversive elements. Mol Microbiol 80:1420–1438CrossRefPubMedGoogle Scholar
  103. Woodward MJ, Best A, Sprigings KA et al (2003) Non-toxigenic Escherichia coli O157: H7 strain NCTC12900 causes attaching-effacing lesions and eae-dependent persistence in weaned sheep. Int J Med Microbiol 293:299–308CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Agriculture and Agri-Food CanadaLondonCanada
  2. 2.Biology DepartmentUniversity of Western OntarioLondonCanada

Personalised recommendations