Skip to main content
SpringerLink
Log in

Shiga Toxin-Producing E. coli in Animals: Detection, Characterization, and Virulence Assessment

  • Protocol
  • First Online:
Shiga Toxin-Producing E. coli

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2291))

Abstract

Cattle and other ruminants are primary reservoirs for Shiga toxin-producing Escherichia coli (STEC) strains which have a highly variable, but unpredictable, pathogenic potential for humans. Domestic swine can carry and shed STEC, but only STEC strains producing the Shiga toxin (Stx) 2e variant and causing edema disease in piglets are considered pathogens of veterinary medical interest. In this chapter, we present general diagnostic workflows for sampling livestock animals to assess STEC prevalence, magnitude, and duration of host colonization. This is followed by detailed method protocols for STEC detection and typing at genetic and phenotypic levels to assess the relative virulence exerted by the strains.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 99.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 129.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Karmali MA (1989) Infection by verocytotoxin-producing Escherichia coli. Clin Microbiol Rev 2(1):15–38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Moxley RA (2004) Escherichia coli O157:H7: an update on intestinal colonization and virulence mechanisms. Anim Health Res Rev 5(1):15–33. https://doi.org/10.1079/ahr200463

    Article  CAS  PubMed  Google Scholar 

  3. Brooks JT, Sowers EG, Wells JG, Greene KD, Griffin PM, Hoekstra RM, Strockbine NA (2005) Non-O157 Shiga toxin-producing Escherichia coli infections in the United States, 1983–2002. J Infect Dis 192(8):1422–1429. https://doi.org/10.1086/466536

    Article  PubMed  Google Scholar 

  4. Luna-Gierke RE, Griffin PM, Gould LH, Herman K, Bopp CA, Strockbine N, Mody RK (2014) Outbreaks of non-O157 Shiga toxin-producing Escherichia coli infection: USA. Epidemiol Infect 142(11):2270–2280. https://doi.org/10.1017/S0950268813003233

    Article  CAS  PubMed  Google Scholar 

  5. Baker CA, Rubinelli PM, Park SH, Carbonero F, Ricke SC (2016) Shiga toxin-producing Escherichia coli in food: incidence, ecology, and detection strategies. Food Control 59:407–419. https://doi.org/10.1016/j.foodcont.2015.06.011

    Article  CAS  Google Scholar 

  6. Tseng M, Fratamico PM, Manning SD, Funk JA (2014) Shiga toxin-producing Escherichia coli in swine: the public health perspective. Anim Health Res Rev 15(1):63–75. https://doi.org/10.1017/S1466252313000170

    Article  PubMed  PubMed Central  Google Scholar 

  7. Wieler LH, Franke S, Menge C, Rose M, Bauerfeind R, Karch H, Baljer G (1995) Untersuchungen zur Immunantwort bei der Ödemkrankheit von Absetzferkeln mit einer rekombinanten B-Untereinheit des Shiga-like-Toxins-IIe. Dtsch Tierärztl Wochenschr 102(1):40–43

    CAS  PubMed  Google Scholar 

  8. Barth S, Schwanitz A, Bauerfeind R (2011) Polymerase chain reaction-based method for the typing of F18 fimbriae and distribution of F18 fimbrial subtypes among porcine Shiga toxin-encoding Escherichia coli in Germany. J Vet Diagn Investig 23(3):454–464. https://doi.org/10.1177/1040638711403417

    Article  Google Scholar 

  9. Frydendahl K, Kare Jensen T, Strodl Andersen J, Fredholm M, Evans G (2003) Association between the porcine Escherichia coli F18 receptor genotype and phenotype and susceptibility to colonisation and postweaning diarrhoea caused by E. coli O138:F18. Vet Microbiol 93(1):39–51

    Article  PubMed  Google Scholar 

  10. Beutin L, Kruger U, Krause G, Miko A, Martin A, Strauch E (2008) Evaluation of major types of Shiga toxin 2e-producing Escherichia coli bacteria present in food, pigs, and the environment as potential pathogens for humans. Appl Environ Microbiol 74(15):4806–4816. https://doi.org/10.1128/Aem.00623-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Barth S, Tscholchiew A, Menge C, Weiss R, Baljer G, Bauerfeind R (2007) Virulence and fitness gene patterns of Shiga toxin-encoding Escherichia coli isolated from pigs with edema disease or diarrhea in Germany. Berl Münch Tierärztl Wochenschr 120(7–8):307–316

    CAS  PubMed  Google Scholar 

  12. Gyles CL, Fairbrother JM (2010) Escherichia coli. In: Gyles CL, Prescott JF, Songer G, Thoen CO (eds) Pathogenesis of bacterial infections in animals, 4th edn. Blackwell Publishing, Ames, IA

    Chapter  Google Scholar 

  13. Moxley RA (2000) Edema disease. Vet Clin North Am Food Anim Pract 16(1):175–185

    Article  CAS  PubMed  Google Scholar 

  14. Osek J (1999) Prevalence of virulence factors of Escherichia coli strains isolated from diarrheic and healthy piglets after weaning. Vet Microbiol 68(3–4):209–217

    Article  CAS  PubMed  Google Scholar 

  15. Wray C, Woodward MJ (1997) Escherichia coli infections in farm animals. In: Sussmann M (ed) Escherichia coli – mechanisms of virulence. Cambridge University Press, Cambridge, pp 95–104

    Google Scholar 

  16. Fairbrother JM, Nadeau E (2019) Colibacillosis. In: Zimmerman JJ, Karriker LA, Ramirez A, Schwartz KJ, Stevenson GW, Zhang J (eds) Diseases of swine, 11th edn. Wiley-Blackwell, Hoboken, NJ, pp 807–834

    Chapter  Google Scholar 

  17. Gyles CL (2020) Overview of edema disease. Merck Sharp and Dohme Corp, Kenilworth, NJ. https://www.msdvetmanual.com. Accessed 28 Jan 2020

    Google Scholar 

  18. Bertschinger HU, Nief V, Tschäpe H (2000) Active oral immunization of suckling piglets to prevent colonization after weaning by enterotoxigenic Escherichia coli with fimbriae F18. Vet Microbiol 71(3–4):255–267

    Article  CAS  PubMed  Google Scholar 

  19. Nadeau É, Fairbrother JM, Zentek J, Bélanger L, Tremblay D, Tremblay CL, Rohe I, Vahjen W, Brunelle M, Hellmann K, Cveji D, Brunner B, Schneider C, Bauer K, Wolf R, Hidalgo A (2017) Efficacy of a single oral dose of a live bivalent E. coli vaccine against post-weaning diarrhea due to F4 and F18-positive enterotoxigenic E. coli. Vet J 226:32–39. https://doi.org/10.1016/j.tvjl.2017.07.004

    Article  CAS  PubMed  Google Scholar 

  20. Bosworth BT, Samuel JE, Moon HW, O’Brien AD, Gordon VM, Whipp SC (1996) Vaccination with genetically modified Shiga-like toxin IIe prevents edema disease in swine. Infect Immun 64(1):55–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. EMA (2020) European Medicines Agency. https://www.ema.europa.eu. Accessed 25 Jan 2020

  22. Geue L, Segura-Alvarez M, Conraths FJ, Kuczius T, Bockemühl J, Karch H, Gallien P (2002) A long-term study on the prevalence of Shiga toxin-producing Escherichia coli (STEC) on four German cattle farms. Epidemiol Infect 129(1):173–185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Besser TE, Richards BL, Rice DH, Hancock DD (2001) Escherichia coli O157:H7 infection of calves: infectious dose and direct contact transmission. Epidemiol Infect 127(3):555–560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. 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 Microbiol 68(5):2269–2277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Geue L, Segura-Alvarez M, Conraths FJ, Kuczius T, Bockemuhl J, Karch H, Gallien P (2002) A long-term study on the prevalence of shiga toxin-producing Escherichia coli (STEC) on four German cattle farms. Epidemiol Infect 129(1):173–185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Naylor SW, Low JC, Besser TE, Mahajan A, Gunn GJ, Pearce MC, McKendrick IJ, Smith DG, 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(3):1505–1512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Pohlenz JF, Dean-Nystrom EA (2004) Colonisation of Escherichia coli O157:H7 on squamous epithelial cells at the rectal-anal junction. Vet Rec 155(8):248

    PubMed  Google Scholar 

  28. Stevens MP, van Diemen PM, Dziva F, Jones PW, Wallis TS (2002) Options for the control of enterohaemorrhagic Escherichia coli in ruminants. Microbiology 148(Pt 12):3767–3778

    Article  CAS  PubMed  Google Scholar 

  29. Shaw DJ, Jenkins C, Pearce MC, Cheasty T, Gunn GJ, Dougan G, Smith HR, Woolhouse ME, Frankel G (2004) Shedding patterns of verocytotoxin-producing Escherichia coli strains in a cohort of calves and their dams on a Scottish beef farm. Appl Environ Microbiol 70(12):7456–7465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Moxley RA, Francis DH (1986) Natural and experimental infection with an attaching and effacing strain of Escherichia coli in calves. Infect Immun 53(2):339–346. https://doi.org/10.1128/Iai.53.2.339-346.1986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. 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(6):897–901

    CAS  PubMed  Google Scholar 

  32. Smith DG, Naylor SW, Gally DL (2002) Consequences of EHEC colonisation in humans and cattle. Int J Med Microbiol 292(3–4):169–183

    Article  CAS  PubMed  Google Scholar 

  33. Jonsson ME, Aspan A, Eriksson E, Vagsholm I (2001) Persistence of verocytotoxin-producing Escherichia coli O157:H7 in calves kept on pasture and in calves kept indoors during the summer months in a Swedish dairy herd. Int J Food Microbiol 66(1–2):55–61

    Article  CAS  PubMed  Google Scholar 

  34. Liebana E, Smith RP, Batchelor M, McLaren I, Cassar C, Clifton-Hadley FA, Paiba GA (2005) Persistence of Escherichia coli O157 isolates on bovine farms in England and Wales. J Clin Microbiol 43(2):898–902. https://doi.org/10.1128/JCM.43.2.898-902.2005

    Article  PubMed  PubMed Central  Google Scholar 

  35. Cray WC Jr, Moon HW (1995) Experimental infection of calves and adult cattle with Escherichia coli O157:H7. Appl Environ Microbiol 61(4):1586–1590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Pirro F, Wieler LH, Failing K, Bauerfeind R, Baljer G (1995) Neutralizing antibodies against Shiga-like toxins from Escherichia coli in colostra and sera of cattle. Vet Microbiol 43(2–3):131–141

    Article  CAS  PubMed  Google Scholar 

  37. Hoffman MA, Menge C, Casey TA, Laegreid W, Bosworth BT, Dean-Nystrom EA (2006) Bovine immune response to shiga-toxigenic Escherichia coli O157:H7. Clin Vaccine Immunol 13(12):1322–1327. https://doi.org/10.1128/CVI.00205-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Matthews L, McKendrick IJ, Ternent H, Gunn GJ, Synge B, Woolhouse ME (2006) Super-shedding cattle and the transmission dynamics of Escherichia coli O157. Epidemiol Infect 134(1):131–142. https://doi.org/10.1017/S0950268805004590

    Article  CAS  PubMed  Google Scholar 

  39. Robinson SE, Brown PE, Wright EJ, Hart CA, French NP (2009) Quantifying within- and between-animal variation and uncertainty associated with counts of Escherichia coli O157 occurring in naturally infected cattle faeces. J R Soc Interface 6(31):169–177. https://doi.org/10.1098/rsif.2008.0183

    Article  CAS  PubMed  Google Scholar 

  40. Matthews L, Reeve R, Gally DL, Low JC, Woolhouse ME, McAteer SP, Locking ME, Chase-Topping ME, Haydon DT, Allison LJ, Hanson MF, Gunn GJ, Reid SW (2013) Predicting the public health benefit of vaccinating cattle against Escherichia coli O157. Proc Natl Acad Sci U S A 110(40):16265–16270. https://doi.org/10.1073/pnas.1304978110

    Article  PubMed  PubMed Central  Google Scholar 

  41. EFSA and ECDC (European Food Safety Authority and European Centre for Disease Prevention and Control) (2019) The European Union one health 2018 zoonoses report. EFSA J 17(12):5926. https://doi.org/10.2903/j.efsa.2019.5926

    Article  Google Scholar 

  42. Rashid RA, Tabata TA, Oatley MJ, Besser TE, Tarr PI, Moseley SL (2006) Expression of putative virulence factors of Escherichia coli O157:H7 differs in bovine and human infections. Infect Immun 74(7):4142–4148. https://doi.org/10.1128/IAI.00299-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. 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(2):1059–1066. https://doi.org/10.1128/aem.69.2.1059-1066.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Lejeune JT, Abedon ST, Takemura K, Christie NP, Sreevatsan S (2004) Human Escherichia coli O157:H7 genetic marker in isolates of bovine origin. Emerg Infect Dis 10(8):1482–1485. https://doi.org/10.3201/eid1008.030784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Lupolova N, Dallman TJ, Matthews L, Bono JL, Gally DL (2016) Support vector machine applied to predict the zoonotic potential of E. coli O157 cattle isolates. Proc Natl Acad Sci U S A 113(40):11312–11317. https://doi.org/10.1073/pnas.1606567113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Bielaszewska M, Mellmann A, Zhang W, Kock R, Fruth A, Bauwens A, Peters G, Karch H (2011) Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany, 2011: a microbiological study. Lancet Infect Dis 11(9):671–676. https://doi.org/10.1016/S1473-3099(11)70165-7

    Article  CAS  PubMed  Google Scholar 

  47. Rasko DA, Webster DR, Sahl JW, Bashir A, Boisen N, Scheutz F, Paxinos EE, Sebra R, Chin CS, Iliopoulos D, Klammer A, Peluso P, Lee L, Kislyuk AO, Bullard J, Kasarskis A, Wang S, Eid J, Rank D, Redman JC, Steyert SR, Frimodt-Moller J, Struve C, Petersen AM, Krogfelt KA, Nataro JP, Schadt EE, Waldor MK (2011) Origins of the E. coli strain causing an outbreak of hemolytic-uremic syndrome in Germany. N Engl J Med 365(8):709–717. https://doi.org/10.1056/NEJMoa1106920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Stalb S, Barth SA, Sobotta K, Liebler-Tenorio E, Geue L, Menge C (2018) Pro-inflammatory capacity of Escherichia coli O104:H4 outbreak strain during colonization of intestinal epithelial cells from human and cattle. Int J Med Microbiol 308(7):899–911. https://doi.org/10.1016/j.ijmm.2018.06.003

    Article  CAS  PubMed  Google Scholar 

  49. Hamm K, Barth SA, Stalb S, Geue L, Liebler-Tenorio E, Teifke JP, Lange E, Tauscher K, Kotterba G, Bielaszewska M, Karch H, Menge C (2016) Experimental infection of calves with Escherichia coli O104:H4 outbreak strain. Sci Rep 6. https://doi.org/10.1038/srep32812

  50. Cabal A, Geue L, Gomez-Barrero S, Barth S, Barcena C, Hamm K, Porrero MC, Valverde A, Canton R, Menge C, Gortazar C, Dominguez L, Alvarez J (2015) Detection of virulence-associated genes characteristic of intestinal Escherichia coli pathotypes, including the enterohemorrhagic/enteroaggregative O104:H4 in bovines from Germany and Spain. Microbiol Immunol. https://doi.org/10.1111/1348-0421.12275

  51. Arimizu Y, Kirino Y, Sato MP, Uno K, Sato T, Gotoh Y, Auvray F, Brugere H, Oswald E, Mainil JG, Anklam KS, Dopfer D, Yoshino S, Ooka T, Tanizawa Y, Nakamura Y, Iguchi A, Morita-Ishihara T, Ohnishi M, Akashi K, Hayashi T, Ogura Y (2019) Large-scale genome analysis of bovine commensal Escherichia coli reveals that bovine-adapted E. coli lineages are serving as evolutionary sources of the emergence of human intestinal pathogenic strains. Genome Res 29(9):1495–1505. https://doi.org/10.1101/gr.249268.119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Nataro JP, Kaper JB (1998) Diarrheagenic Escherichia coli. Clin Microbiol Rev 11(1):142–201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Sonntag AK, Bielaszewska M, Mellmann A, Dierksen N, Schierack P, Wieler LH, Schmidt MA, Karch H (2005) Shiga toxin 2e-producing Escherichia coli isolates from humans and pigs differ in their virulence profiles and interactions with intestinal epithelial cells. Appl Environ Microbiol 71(12):8855–8863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. 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 153(Pt 4):959–967. https://doi.org/10.1099/mic.0.2006/003467-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Stamm I, Mohr M, Bridger PS, Schröpfer E, König M, Stoffregen WC, Dean-Nystrom EA, Baljer G, Menge C (2008) Epithelial and mesenchymal cells in the bovine colonic mucosa differ in their responsiveness to Escherichia coli Shiga toxin 1. Infect Immun 76(11):5381–5391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Sansonetti PJ (2004) War and peace at mucosal surfaces. Nat Rev Immunol 4(12):953–964

    Article  CAS  PubMed  Google Scholar 

  57. Schmidt N, Barth SA, Frahm J, Meyer U, Danicke S, Geue L, Menge C (2018) Decreased STEC shedding by cattle following passive and active vaccination based on recombinant Escherichia coli Shiga toxoids. Vet Res 49. https://doi.org/10.1186/s13567-018-0523-0

  58. Fröhlich J, Baljer G, Menge C (2009) Maternally and naturally acquired antibodies to Shiga toxins in a cohort of calves shedding Shiga-toxigenic Escherichia coli. Appl Environ Microbiol 75(11):3695–3704

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Segura-Alvarez M, Richter H, Conraths FJ, Geue L (2003) Evaluation of enzyme-linked immunosorbent assays and a PCR test for detection of shiga toxins for shiga toxin-producing Escherichia coli in cattle herds. J Clin Microbiol 41(12):5760–5763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Clinical and Laboratory Standards Institute (CLSI) (2018) Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. CLSI standard VET01, 5th edn. Clinical and Laboratory Standards Institute, Pittsburgh, PA

    Google Scholar 

  61. Bridger PS, Mohr M, Stamm I, Fröhlich J, Follmann W, Birkner S, Metcalfe H, Werling D, Baljer G, Menge C (2010) Primary bovine colonic cells: a model to study strain-specific responses to Escherichia coli. Vet Immunol Immunopathol 137(1–2):54–63. https://doi.org/10.1016/j.vetimm.2010.04.010

    Article  CAS  PubMed  Google Scholar 

  62. Cray WC Jr, Moon HW (1995) Experimental infection of calves and adult cattle with Escherichia coli O157:H7. Appl Environ Microbiol 61(4):1586–1590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Lee MS, Koo S, Jeong DG, Tesh VL (2016) Shiga toxins as multi-functional proteins: induction of host cellular stress responses, role in pathogenesis and therapeutic applications. Toxins 8(3). https://doi.org/10.3390/toxins8030077

  64. Matthias D (1969) Investigations on localisation of beta-hemolytic E. coli in several organs of swine with edema disease. Zentbl Bakteriolog 212(1):103

    CAS  Google Scholar 

  65. Menge C (2020) Molecular biology of Escherichia coli Shiga toxins’ effects on mammalian cells. Toxins 12(5). https://doi.org/10.3390/toxins12050345

  66. Lee MS, Tesh VL (2019) Roles of Shiga toxins in immunopathology. Toxins 11(4). https://doi.org/10.3390/toxins11040212

  67. Barth SA, Menge C, Eichhorn I, Semmler T, Wieler LH, Pickard D, Belka A, Berens C, Geue L (2016) The accessory genome of Shiga toxin-producing Escherichia coli defines a persistent colonization type in cattle. Appl Environ Microbiol 82(17):5455–5464. https://doi.org/10.1128/AEM.00909-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Kaper JB (1998) The locus of enterocyte effacement pathogenicity island of shiga toxin-producing Escherichia coli O157:H7 and other attaching and effacing E. coli. Jpn J Med Sci Biol 51:S101–S107. https://doi.org/10.7883/yoken1952.51.Supplement1_S101

    Article  PubMed  Google Scholar 

  69. Monteiro R, Ageorges V, Rojas-Lopez M, Schmidt H, Weiss A, Bertin Y, Forano E, Jubelin G, Henderson IR, Livrelli V, Gobert AP, Rosini R, Soriani M, Desvaux M (2016) A secretome view of colonisation factors in Shiga toxin-encoding Escherichia coli (STEC): from enterohaemorrhagic E. coli (EHEC) to related enteropathotypes. FEMS Microbiol Lett 363(16). https://doi.org/10.1093/femsle/fnw179

  70. Hazen TH, Michalski J, Luo Q, Shetty AC, Daugherty SC, Fleckenstein JM, Rasko DA (2017) Comparative genomics and transcriptomics of Escherichia coli isolates carrying virulence factors of both enteropathogenic and enterotoxigenic E. coli. Sci Rep 7(1):3513. https://doi.org/10.1038/s41598-017-03489-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Soysal N, Mariani-Kurkdjian P, Smail Y, Liguori S, Gouali M, Loukiadis E, Fach P, Bruyand M, Blanco J, Bidet P, Bonacorsi S (2016) Enterohemorrhagic Escherichia coli hybrid pathotype O80:H2 as a new therapeutic challenge. Emerg Infect Dis 22(9):1604–1612. https://doi.org/10.3201/eid2209.160304

    Article  PubMed  PubMed Central  Google Scholar 

  72. Vygen-Bonnet S, Rosner B, Wilking H, Fruth A, Prager R, Kossow A, Lang C, Simon S, Seidel J, Faber M, Schielke A, Michaelis K, Holzer A, Kamphausen R, Kalhofer D, Thole S, Mellmann A, Flieger A, Stark K (2017) Ongoing haemolytic uraemic syndrome (HUS) outbreak caused by sorbitol-fermenting (SF) Shiga toxin-producing Escherichia coli (STEC) O157, Germany, December 2016 to May 2017. Euro Surveill 22(21). https://doi.org/10.2807/1560-7917.ES.2017.22.21.30541

  73. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM (2011) Foodborne illness acquired in the United States—major pathogens. Emerg Infect Dis 17(1):7–15. https://doi.org/10.3201/eid1701.P11101

    Article  PubMed  PubMed Central  Google Scholar 

  74. Zweifel C, Schumacher S, Beutin L, Blanco J, Stephan R (2006) Virulence profiles of Shiga toxin 2e-producing Escherichia coli isolated from healthy pig at slaughter. Vet Microbiol 117(2–4):328–332. https://doi.org/10.1016/j.vetmic.2006.06.017

    Article  CAS  PubMed  Google Scholar 

  75. Wieler LH, Tigges M, Ebel F, Schaferkordt S, Djafari S, Schlapp T, Baljer G, Chakraborty T (1996) The enterohemolysin phenotype of bovine Shiga-like toxin-producing Escherichia coli (SLTEC) is encoded by the EHEC-hemolysin gene. Vet Microbiol 52(1–2):153–164

    Article  CAS  PubMed  Google Scholar 

  76. Wieler LH, Bauerfeind R, Baljer G (1992) Characterization of Shiga-like toxin producing Escherichia coli (SLTEC) isolated from calves with and without diarrhoea. Zentralbl Bakteriol [Orig] 276(2):243–253

    Article  CAS  Google Scholar 

  77. Wieler LH, Bauerfeind R, Weiß R, Pirro F, Baljer G (1995) Association of enterohemolysin and non-fermentation of rhamnose and sucrose with Shiga-like toxin genes in Escherichia coli from calves. Zentralbl Bakteriol [Orig] 282(3):265–274

    Article  CAS  Google Scholar 

  78. Beutin L, Montenegro MA, Ørskov I, Ørskov F, Prada J, Zimmermann S, Stephan R (1989) Close association of verotoxin (Shiga-like toxin) production with enterohemolysin production in strains of Escherichia coli. J Clin Microbiol 27(11):2559–2564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Mainil JG, Fairbrother JM (2014) Pathogenic Escherichia coli in domestic mammals and birds. In: Morabito S (ed) Pathogenic Escherichia coli – molecular and cellular microbiology. caister. Academic, Norfolk, pp 19–43

    Google Scholar 

  80. Bertschinger HU, Pohlenz J (1983) Bacterial colonization and morphology of the intestine in porcine Escherichia coli enterotoxemia (edema disease). Vet Pathol 20(1):99–110

    Article  CAS  PubMed  Google Scholar 

  81. Luppi A (2017) Swine enteric colibacillosis: diagnosis, therapy and antimicrobial resistance. Porcine Health Manag 3:16. https://doi.org/10.1186/s40813-017-0063-4

    Article  PubMed  PubMed Central  Google Scholar 

  82. Pedersen KS, Okholm E, Johansen M, Angen O, Jorsal SE, Nielsen JP, Baekbo P (2015) Clinical utility and performance of sock sampling in weaner pig diarrhoea. Prev Vet Med 120(3–4):313–320. https://doi.org/10.1016/j.prevetmed.2015.04.015

    Article  PubMed  Google Scholar 

  83. Bjustrom-Kraft J, Christopher-Hennings J, Daly R, Main R, Torrison J, Thurn M, Zimmerman J (2018) The use of oral fluid diagnostics in swine medicine. J Swine Health Prod 26(5):262–269

    Google Scholar 

  84. Wieler LH, Bauerfeind R (2003) STEC as a veterinary problem. Diagnostics and prophylaxis in animals. Methods Mol Med 73:75–89

    CAS  PubMed  Google Scholar 

  85. Casey TA, Bosworth BT (2009) Design and evaluation of a multiplex polymerase chain reaction assay for the simultaneous identification of genes for nine different virulence factors associated with Escherichia coli that cause diarrhea and edema disease in swine. J Vet Diagn Investig 21(1):25–30

    Article  Google Scholar 

  86. Kaper JB, O’Brien AD (2014) Overview and historical perspectives. Microbiol Spectr 2(6). https://doi.org/10.1128/microbiolspec.EHEC-0028-2014

  87. Scheutz F, Teel LD, Beutin L, Pierard D, Buvens G, Karch H, Mellmann A, Caprioli A, Tozzoli R, Morabito S, Strockbine NA, Melton-Celsa AR, Sanchez M, Persson S, O’Brien AD (2012) Multicenter evaluation of a sequence-based protocol for subtyping Shiga toxins and standardizing Stx nomenclature. J Clin Microbiol 50(9):2951–2963. https://doi.org/10.1128/JCM.00860-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Blanco M, Blanco JE, Blanco J, Gonzalez EA, Alonso MP, Maas H, Jansen WH (1996) Prevalence and characteristics of human and bovine verotoxigenic Escherichia coli strains isolated in Galicia (north-western Spain). Eur J Epidemiol 12(1):13–19. https://doi.org/10.1007/BF00144422

    Article  CAS  PubMed  Google Scholar 

  89. Blanco M, Blanco JE, Blanco J, Mora A, Prado C, Alonso MP, Mourino M, Madrid C, Balsalobre C, Juarez A (1997) Distribution and characterization of faecal verotoxin-producing Escherichia coli (VTEC) isolated from healthy cattle. Vet Microbiol 54(3–4):309–319. https://doi.org/10.1016/s0378-1135(96)01292-8

    Article  CAS  PubMed  Google Scholar 

  90. Richter H, Klie H, Timm M, Gallien P, Steinrück H, Perlberg KW, Protz D (1997) Verotoxin-bildende E coli (VTEC) im Kot von Schlachtrindern aus Deutschland Berl Münch. Tierärztl Wochenschr 110(4):121–127

    CAS  Google Scholar 

  91. Weber A, Klie H, Richter H, Gallien P, Timm M, Perlberg KW (1997) Uber die derzeitigen Probleme zum Auffinden von Infektionsquellen und Infektionsketten beim enterohamorrhagischen E coli (EHEC) Berl Münch. Tierärztl Wochenschr 110(6):211–213

    CAS  Google Scholar 

  92. Ball HJ, Finlay D, Burns L, Mackie DP (1994) Application of monoclonal antibody-based sandwich ELISAs to detect verotoxins in cattle faeces. Res Vet Sci 57(2):225–232. https://doi.org/10.1016/0034-5288(94)90062-0

    Article  CAS  PubMed  Google Scholar 

  93. Heuvelink AE, van den Biggelaar FL, Zwartkruis-Nahuis J, Herbes RG, Huyben R, Nagelkerke N, Melchers WJ, Monnens LA, de Boer E (1998) Occurrence of verocytotoxin-producing Escherichia coli O157 on Dutch dairy farms. J Clin Microbiol 36(12):3480–3487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Callaway TR, Carr MA, Edrington TS, Anderson RC, Nisbet DJ (2009) Diet, Escherichia coli O157:H7, and cattle: a review after 10 years. Curr Issues Mol Biol 11(2):67–79

    CAS  PubMed  Google Scholar 

  95. Kudva IT, Hatfield PG, Hovde CJ (1995) Effect of diet on the shedding of Escherichia coli O157:H7 in a sheep model. Appl Environ Microbiol 61(4):1363–1370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Aslam M, Stanford K, McAllister TA (2010) Characterization of antimicrobial resistance and seasonal prevalence of Escherichia coli O157:H7 recovered from commercial feedlots in Alberta, Canada. Lett Appl Microbiol 50(3):320–326. https://doi.org/10.1111/j.1472-765X.2010.02798.x

    Article  CAS  PubMed  Google Scholar 

  97. Schneider LG, Lewis GL, Moxley RA, Smith DR (2018) A four-season longitudinal study of enterohaemorrhagic Escherichia coli in beef cow-calf herds in Mississippi and Nebraska. Zoonoses Public Health 65(5):552–559. https://doi.org/10.1111/zph.12465

    Article  CAS  PubMed  Google Scholar 

  98. Stanford K, Reuter T, Bach SJ, Chui L, Ma A, Conrad CC, Tostes R, McAllister TA (2017) Effect of severe weather events on the shedding of Shiga toxigenic Escherichia coli in slaughter cattle and phenotype of serogroup O157 isolates. FEMS Microbiol Ecol 93(9). https://doi.org/10.1093/femsec/fix098

  99. McPherson AS, Dhungyel OP, Ward MP (2015) Comparison of recto-anal mucosal swab and faecal culture for the detection of Escherichia coli O157 and identification of super-shedding in a mob of Merino sheep. Epidemiol Infect 143(13):2733–2742. https://doi.org/10.1017/S0950268815000011

    Article  CAS  PubMed  Google Scholar 

  100. ISO TS 13136:2012 (revised 2019) Microbiology of food and animal feed – real-time polymerase chain reaction (PCR)-based method for the detection of food-borne pathogens – horizontal method for the detection of Shiga toxin-producing Escherichia coli (STEC) and the determination of O157, O111, O26, O103 and O145 serogroups

    Google Scholar 

  101. Gunn GJ, McKendrick IJ, Ternent HE, Thomson-Carter F, Foster G, Synge BA (2007) An investigation of factors associated with the prevalence of verocytotoxin producing Escherichia coli O157 shedding in Scottish beef cattle. Vet J 174(3):554–564. https://doi.org/10.1016/j.tvjl.2007.08.024

    Article  CAS  PubMed  Google Scholar 

  102. Pearce MC, Chase-Topping ME, McKendrick IJ, Mellor DJ, Locking ME, Allison L, Ternent HE, Matthews L, Knight HI, Smith AW, Synge BA, Reilly W, Low JC, Reid SW, Gunn GJ, Woolhouse ME (2009) Temporal and spatial patterns of bovine Escherichia coli O157 prevalence and comparison of temporal changes in the patterns of phage types associated with bovine shedding and human E. coli O157 cases in Scotland between 1998–2000 and 2002–2004. BMC Microbiol 9:276. https://doi.org/10.1186/1471-2180-9-276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Paiba GA, Wilesmith JW, Evans SJ, Pascoe SJ, Smith RP, Kidd SA, Ryan JB, McLaren IM, Chappell SA, Willshaw GA, Cheasty T, French NP, Jones TW, Buchanan HF, Challoner DJ, Colloff AD, Cranwell MP, Daniel RG, Davies IH, Duff JP, Hogg RA, Kirby FD, Millar MF, Monies RJ, Nicholls MJ, Payne JH (2003) Prevalence of faecal excretion of verocytotoxigenic Escherichia coli O157 in cattle in England and Wales. Vet Rec 153(12):347–353. https://doi.org/10.1136/vr.153.12.347

    Article  CAS  PubMed  Google Scholar 

  104. Ellis-Iversen J, Smith RP, Snow LC, Watson E, Millar MF, Pritchard GC, Sayers AR, Cook AJ, Evans SJ, Paiba GA (2007) Identification of management risk factors for VTEC O157 in young-stock in England and Wales. Prev Vet Med 82(1–2):29–41. https://doi.org/10.1016/j.prevetmed.2007.05.004

    Article  PubMed  Google Scholar 

  105. Henry MK, Tongue SC, Evans J, Webster C, Mc KI, Morgan M, Willett A, Reeves A, Humphry RW, Gally DL, Gunn GJ, Chase-Topping ME (2017) British Escherichia coli O157 in cattle study (BECS): to determine the prevalence of E. coli O157 in herds with cattle destined for the food chain. Epidemiol Infect 145(15):3168–3179. https://doi.org/10.1017/S0950268817002151

    Article  CAS  PubMed  Google Scholar 

  106. Stephens TP, McAllister TA, Stanford K (2008) Development of an experimental model to assess the ability of Escherichia coli O157:H7-inoculated fecal pats to mimic a super shedder within a feedlot environment. J Food Prot 71(3):648–652. https://doi.org/10.4315/0362-028x-71.3.648

    Article  CAS  PubMed  Google Scholar 

  107. Halliday JE, Chase-Topping ME, Pearce MC, McKendrick IJ, Allison L, Fenlon D, Low C, Mellor DJ, Gunn GJ, Woolhouse ME (2006) Herd-level risk factors associated with the presence of phage type 21/28 E coli O157 on Scottish cattle farms. BMC Microbiol 6:99. https://doi.org/10.1186/1471-2180-6-99

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Chase-Topping ME, McKendrick IJ, Pearce MC, MacDonald P, Matthews L, Halliday J, Allison L, Fenlon D, Low JC, Gunn G, Woolhouse ME (2007) Risk factors for the presence of high-level shedders of Escherichia coli O157 on Scottish farms. J Clin Microbiol 45(5):1594–1603. https://doi.org/10.1128/JCM.01690-06

    Article  PubMed  PubMed Central  Google Scholar 

  109. Dixon A, Cernicchiaro N, Amachawadi RG, Shi X, Cull CA, Renter DG (2020) Longitudinal characterization of prevalence and concentration of Shiga toxin-producing Escherichia coli serogroups in feces of individual feedlot cattle. Foodborne Pathog Dis. https://doi.org/10.1089/fpd.2019.2777

  110. 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(1):237–244. https://doi.org/10.2527/jas.2010-3088

    Article  CAS  PubMed  Google Scholar 

  111. Wang GD, Zhao T, Doyle MP (1996) Fate of enterohemorrhagic Escherichia coli O157:H7 in bovine feces. Appl Environ Microbiol 62(7):2567–2570. https://doi.org/10.1128/Aem.62.7.2567-2570.1996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Arthur TM, Nou XW, Kalchayanand N, Bosilevac JM, Wheeler T, Koohmaraie M (2011) Survival of Escherichia coli O157:H7 on cattle hides. Appl Environ Microbiol 77(9):3002–3008. https://doi.org/10.1128/Aem.02238-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Smith DR, Moxley RA, Clowser SL, Folmer JD, Hinkley S, Erickson GE, Klopfenstein TJ (2005) Use of rope devices to describe and explain the feedlot ecology of Escherichia coli O157:H7 by time and place. Foodborne Pathog Dis 2(1):50–60. https://doi.org/10.1089/fpd.2005.2.50

    Article  CAS  PubMed  Google Scholar 

  114. Hahn N, Failing K, Eisenberg T, Schlez K, Zschock PM, Donat K, Einax E, Kohler H (2017) Evaluation of different diagnostic methods for the detection of Mycobcterium avium subsp. paratuberculosis in boot swabs and liquid manure samples. BMC Vet Res 13(1):259. https://doi.org/10.1186/s12917-017-1173-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Roschanski N, Friese A, von Salviati-Claudius C, Hering J, Kaesbohrer A, Kreienbrock L, Roesler U (2017) Prevalence of carbapenemase producing Enterobacteriaceae isolated from German pig-fattening farms during the years 2011–2013. Vet Microbiol 200:124–129. https://doi.org/10.1016/j.vetmic.2015.11.030

    Article  CAS  PubMed  Google Scholar 

  116. Eisenberg T, Wolter W, Lenz M, Schlez K, Zschock M (2013) Boot swabs to collect environmental samples from common locations in dairy herds for Mycobacterium avium ssp. paratuberculosis (MAP) detection. J Dairy Res 80(4):485–489. https://doi.org/10.1017/S002202991300040X

    Article  CAS  PubMed  Google Scholar 

  117. Donat K, Hahn N, Eisenberg T, Schlez K, Kohler H, Wolter W, Rohde M, Putzschel R, Rosler U, Failing K, Zschock PM (2016) Within-herd prevalence thresholds for the detection of Mycobacterium avium subspecies paratuberculosis-positive dairy herds using boot swabs and liquid manure samples. Epidemiol Infect 144(2):413–424. https://doi.org/10.1017/S0950268815000977

    Article  CAS  PubMed  Google Scholar 

  118. Stanford K, Bach SJ, Marx TH, Jones S, Hansen JR, Wallins GL, Zahiroddini H, McAllister TA (2005) Monitoring Escherichia coli O157:H7 in inoculated and naturally colonized feedlot cattle and their environment. J Food Prot 68(1):26–33. https://doi.org/10.4315/0362-028x-68.1.26

    Article  CAS  PubMed  Google Scholar 

  119. Barth S, Duncker S, Hempe J, Breves G, Baljer G, Bauerfeind R (2009) Escherichia coli Nissle 1917 for probiotic use in piglets: evidence for intestinal colonization. J Appl Microbiol 107(5):1697–1710. https://doi.org/10.1111/j.1365-2672.2009.04361.x

    Article  CAS  PubMed  Google Scholar 

  120. Conrad CC, Stanford K, Narvaez-Bravo C, Callaway T, McAllister T (2017) Farm fairs and petting zoos: a review of animal contact as a source of zoonotic enteric disease. Foodborne Pathog Dis 14(2):59–73. https://doi.org/10.1089/fpd.2016.2185

    Article  PubMed  Google Scholar 

  121. Chase-Topping ME, Rosser T, Allison LJ, Courcier E, Evans J, McKendrick IJ, Pearce MC, Handel I, Caprioli A, Karch H, Hanson MF, Pollock KG, Locking ME, Woolhouse ME, Matthews L, Low JC, Gally DL (2012) Pathogenic potential to humans of bovine Escherichia coli O26, Scotland. Emerg Infect Dis 18(3):439–448. https://doi.org/10.3201/eid1803.111236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Sharma R, Stanford K, Louie M, Munns K, John SJ, Zhang YX, Gannon V, Chui L, Read R, Topp E, McAllister T (2009) Escherichia coli O157:H7 lineages in healthy beef and dairy cattle and clinical human cases in Alberta, Canada. J Food Prot 72(3):601–607. https://doi.org/10.4315/0362-028x-72.3.601

    Article  PubMed  Google Scholar 

  123. Tostes R, Goji N, Amoako K, Chui L, Kastelic J, DeVinney R, Stanford K, Reuter T (2017) Subtyping Escherichia coli virulence genes isolated from feces of beef cattle and clinical cases in Alberta. Foodborne Pathog Dis 14(1):35–42. https://doi.org/10.1089/fpd.2016.2199

    Article  CAS  PubMed  Google Scholar 

  124. Smith KE, Stenzel SA, Bender JB, Wagstrom E, Soderlund D, Leano FT, Taylor CM, Belle-Isle PA, Danila R (2004) Outbreaks of enteric infections caused by multiple pathogens associated with calves at a farm day camp. Pediatr Infect Dis J 23(12):1098–1104. https://doi.org/10.1097/01.inf.0000145409.74116.e5

    Article  PubMed  Google Scholar 

  125. Barth S, Geue L, Hinsching A, Jenckel M, Schlosser J, Eiden M, Pietschmann J, Menge C, Beer M, Groschup M, Jori F, Etter E, Blome S (2017) Experimental evaluation of faecal Escherichia coli and hepatitis E virus as biological indicators of contacts between domestic pigs and Eurasian wild boar. Transbound Emerg Dis 64(2):487–494. https://doi.org/10.1111/tbed.12389

    Article  CAS  PubMed  Google Scholar 

  126. Geue L, Klare S, Schnick C, Mintel B, Meyer K, Conraths FJ (2009) Analysis of the clonal relationship of serotype O26:H11 enterohemorrhagic Escherichia coli isolates from cattle. Appl Environ Microbiol 75(21):6947–6953. https://doi.org/10.1128/AEM.00605-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Treacy J, Jenkins C, Paranthaman K, Jorgensen F, Mueller-Dobliess D, Anjum M, Kaindama L, Hartman H, Kirchner M, Carson T, Kar-Purkayastha I (2019) Outbreak of Shiga toxin-producing Escherichia coli O157:H7 linked to raw drinking milk resolved by rapid application of advanced pathogen characterisation methods, England, August to October 2017. Euro Surveill 24(16):7–13. https://doi.org/10.2807/1560-7917.Es.2019.24.16.1800191

    Article  Google Scholar 

  128. Hussein HS, Sakuma T (2005) Prevalence of shiga toxin-producing Escherichia coli in dairy cattle and their products. J Dairy Sci 88(2):450–465

    Article  CAS  PubMed  Google Scholar 

  129. Menrath A, Wieler LH, Heidemanns K, Semmler T, Fruth A, Kemper N (2010) Shiga toxin producing Escherichia coli: identification of non-O157:H7-super-shedding cows and related risk factors. Gut Pathogens 2. https://doi.org/10.1186/1757-4749-2-7

  130. Naylor SW, Gally DL, Low JC (2005) Enterohaemorrhagic E. coli in veterinary medicine. Int J Med Microbiol 295(6–7):419–441

    Article  CAS  PubMed  Google Scholar 

  131. Caprioli A, Morabito S, Brugere H, Oswald E (2005) Enterohaemorrhagic Escherichia coli: emerging issues on virulence and modes of transmission. Vet Res 36(3):289–311

    Article  CAS  PubMed  Google Scholar 

  132. Callaway TR, Anderson RC, Edrington TS, Genovese KJ, Harvey RB, Poole TL, Nisbet DJ (2004) Recent pre-harvest supplementation strategies to reduce carriage and shedding of zoonotic enteric bacterial pathogens in food animals. Anim Health Res Rev 5(1):35–47. https://doi.org/10.1079/ahr200462

    Article  CAS  PubMed  Google Scholar 

  133. Snedeker KG, Campbell M, Sargeant JM (2012) A systematic review of vaccinations to reduce the shedding of Escherichia coli O157 in the faeces of domestic ruminants. Zoonoses Public Health 59(2):126–138. https://doi.org/10.1111/j.1863-2378.2011.01426.x

    Article  CAS  PubMed  Google Scholar 

  134. Vande Walle K, Vanrompay D, Cox E (2013) Bovine innate and adaptive immune responses against Escherichia coli O157:H7 and vaccination strategies to reduce faecal shedding in ruminants. Vet Immunol Immunopathol 152(1–2):109–120

    Article  PubMed  CAS  Google Scholar 

  135. Hoffman MA, Menge C, Casey TA, Laegreid W, Bosworth BT, Dean-Nystrom EA (2006) Bovine immune response to shiga-toxigenic Escherichia coli O157:H7. Clin Vaccine Immunol 13(12):1322–1327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Fitzgerald SF, Beckett AE, Palarea-Albaladejo J, McAteer S, Shaaban S, Morgan J, Ahmad NI, Young R, Mabbott NA, Morrison L, Bono JL, Gally DL, McNeilly TN (2019) Shiga toxin sub-type 2a increases the efficiency of Escherichia coli O157 transmission between animals and restricts epithelial regeneration in bovine enteroids. PLoS Pathog 15(10). https://doi.org/10.1371/journal.ppat.1008003

  137. Stanford K, Hannon S, Booker CW, Jim GK (2014) Variable efficacy of a vaccine and direct-fed microbial for controlling Escherichia coli O157:H7 in feces and on hides of feedlot cattle. Foodborne Pathog Dis 11(5):379–387. https://doi.org/10.1089/fpd.2013.1693

    Article  CAS  PubMed  Google Scholar 

  138. Cahill EE, Glantz PJ (1978) Demonstration of K88ac and K88ab antigens of Escherichia coli by means of immunoelectrophoresis and immunodiffusion. Infect Immun 20(3):811–815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Woodward MJ, Wray C (1990) Nine DNA probes for detection of toxin and adhesin genes in Escherichia coli isolated from diarrhoeal disease in animals. Vet Microbiol 25(1):55–65

    Article  CAS  PubMed  Google Scholar 

  140. Franck SM, Bosworth BT, Moon HW (1998) Multiplex PCR for enterotoxigenic, attaching and effacing, and Shiga toxin-producing Escherichia coli strains from calves. J Clin Microbiol 36(6):1795–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH, Karch H, Reeves PR, Maiden MC, Ochman H, Achtman M (2006) Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 60(5):1136–1151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Cravioto A, Tello A, Navarro A, Ruiz J, Villafan H, Uribe F, Eslava C (1991) Association of Escherichia coli HEp-2 adherence patterns with type and duration of diarrhoea. Lancet 337(8736):262–264

    Article  CAS  PubMed  Google Scholar 

  143. Scotland SM, Gross RJ, Rowe B (1985) Laboratory tests for enterotoxin production, enteroinvasion and adhesion in diarrhoeagenic E. coli. In: Sussman M (ed) The virulence of Escherichia coli. Reviews and methods. Academic, New York, NY, pp 359–405

    Google Scholar 

  144. Knutton S, Baldwin T, Williams PH, McNeish AS (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(4):1290–1298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Dibb-Fuller MP, Allen-Vercoe E, Thorns CJ, Woodward MJ (1999) Fimbriae- and flagella-mediated association with and invasion of cultured epithelial cells by Salmonella enteritidis. Microbiology 145(Pt 5):1023–1031. https://doi.org/10.1099/13500872-145-5-1023

    Article  CAS  PubMed  Google Scholar 

  146. Sasaki M, Sitaraman SV, Babbin BA, Gerner-Smidt P, Ribot EM, Garrett N, Alpern JA, Akyildiz A, Theiss AL, Nusrat A, Klapproth JM (2007) Invasive Escherichia coli are a feature of Crohn’s disease. Lab Investig 87(10):1042–1054. https://doi.org/10.1038/labinvest.3700661

    Article  CAS  PubMed  Google Scholar 

  147. Föllmann W, Weber S, Birkner S (2000) Primary cell cultures of bovine colon epithelium: isolation and cell culture of colonocytes. Toxicol In Vitro 14(5):435–445. https://doi.org/10.1016/S0887-2333(00)00033-3

    Article  PubMed  Google Scholar 

  148. Eisel D, Seth O, Grünewald-Janho S, Kruchen B, Rüger B (2008) DIG application manual for filter hybridization. Roche Diagnostics GmbH, Mannheim

    Google Scholar 

  149. Zhou YH, Zhang XP, Ebright RH (1991) Random mutagenesis of gene-sized DNA molecules by use of PCR with Taq DNA polymerase. Nucleic Acids Res 19(21):6052. https://doi.org/10.1093/nar/19.21.6052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Müller D, Greune L, Heusipp G, Karch H, Fruth A, Tschäpe H, Schmidt MA (2007) Identification of unconventional intestinal pathogenic Escherichia coli isolates expressing intermediate virulence factor profiles by using a novel single-step multiplex PCR. Appl Environ Microbiol 73(10):3380–3390. https://doi.org/10.1128/AEM.02855-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Levine MM, Prado V, Robins-Browne R, Lior H, Kaper JB, Moseley SL, Gicquelais K, Nataro JP, Vial P, Tall B (1988) Use of DNA probes and HEp-2 cell adherence assay to detect diarrheagenic Escherichia coli. J Infect Dis 158(1):224–228. https://doi.org/10.1093/infdis/158.1.224

    Article  CAS  PubMed  Google Scholar 

  152. Blumer C, Kleefeld A, Lehnen D, Heintz M, Dobrindt U, Nagy G, Michaelis K, Emody L, Polen T, Rachel R, Wendisch VF, Unden G (2005) Regulation of type 1 fimbriae synthesis and biofilm formation by the transcriptional regulator LrhA of Escherichia coli. Microbiol SGM 151:3287–3298. https://doi.org/10.1099/mic.0.28098-0

    Article  CAS  Google Scholar 

  153. Al Safadi R, Abu-Ali GS, Sloup RE, Rudrik JT, Waters CM, Eaton KA, Manning SD (2012) Correlation between in vivo biofilm formation and virulence gene expression in Escherichia coli O104:H4. PLoS One 7(7):e41628. https://doi.org/10.1371/journal.pone.0041628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Herold S, Paton JC, Srimanote P, Paton AW (2009) Differential effects of short-chain fatty acids and iron on expression of iha in Shiga-toxigenic Escherichia coli. Microbiology 155(Pt 11):3554–3563. https://doi.org/10.1099/mic.0.029454-0

    Article  CAS  PubMed  Google Scholar 

  155. Zhang W, Bielaszewska M, Bauwens A, Fruth A, Mellmann A, Karch H (2012) Real-time multiplex PCR for detecting Shiga toxin 2-producing Escherichia coli O104:H4 in human stools. J Clin Microbiol 50(5):1752–1754. https://doi.org/10.1128/JCM.06817-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Friedrich-Loeffler-Institut/Federal Research Institute for Animal Health, Institute of Molecular Pathogenesis, Jena, Germany

    Stefanie A. Barth, Christian Berens & Christian Menge

  2. Institute for Hygiene and Infectious Diseases of Animals, Justus Liebig University Gießen, Gießen, Germany

    Rolf Bauerfeind

Authors
  1. Stefanie A. Barth
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rolf Bauerfeind
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christian Berens
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christian Menge
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christian Menge .

Editor information

Editors and Affiliations

  1. University of East Anglia, Norwich Medical School, Norwich, UK

    Stephanie Schüller

  2. National Reference Laboratory for E. coli and Shigellae, National Institute of Public Health, Prague, Czech Republic

    Martina Bielaszewska

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Barth, S.A., Bauerfeind, R., Berens, C., Menge, C. (2021). Shiga Toxin-Producing E. coli in Animals: Detection, Characterization, and Virulence Assessment. In: Schüller, S., Bielaszewska, M. (eds) Shiga Toxin-Producing E. coli . Methods in Molecular Biology, vol 2291. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-1339-9_2

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-1339-9_2

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-1338-2

  • Online ISBN: 978-1-0716-1339-9

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation