Outbreaks of Shiga Toxin-Related Poisoning

  • Christopher J. Silva
  • David L. Brandon
  • Craig B. Skinner
  • Xiaohua He
Chapter
Part of the Food Microbiology and Food Safety book series (FMFS)

Abstract

Foodborne outbreaks of Shiga toxin-producing bacteria occur with disturbing regularity. The two most common Shiga toxin-producing bacteria are Shigella spp. and the Shiga toxin-producing Escherichia coli (STEC). Among foodborne pathogens, they result in a disproportionately large share of hospitalizations, serious sequelae, and deaths. In 1982 the first reported outbreak of STEC was caused by an E. coli O157:H7 serotype in undercooked hamburger, but by 2008 it was estimated that most foodborne STEC disease was caused by other serotypes. As the food service industry has adopted more stringent cooking practices and as diets have changed, the sources of outbreaks have shifted as well. The two largest outbreaks on record were caused by consumption of uncooked radish and fenugreek sprouts. There are at least 200 different known strains of STEC found in farm animals, where they can propagate “below the radar” because farm animals lack the receptors that would make them vulnerable to Shiga toxins. Future outbreaks are likely to involve other uncooked foods and different strains of STEC, and they may be triggered by the agricultural practices, food processing and transportation conditions, and ecological factors that bring them together.

Keywords

Shiga toxin poisoning Quick serve restaurant Effective dose Pathogenic Escherichia coli Shigellosis Escherichia coli O157:H7 Escherichia coli O104:H4 Shigella sppFoodborne illness, Sakai, Japan STEC outbreak, Germany 

References

  1. Ackers ML, Mahon BE, Leahy E, Goode B, Damrow T, Hayes PS, Bibb WF, Rice DH, Barrett TJ, Hutwagner L, Griffin PM, Slutsker L (1998) An outbreak of Escherichia coli O157:H7 infections associated with leaf lettuce consumption. J Infect Dis 177(6):1588–1593CrossRefPubMedGoogle Scholar
  2. Adams NL, Byrne L, Smith GA, Elson R, Harris JP, Salmon R, Smith R, O’Brien SJ, Adak GK, Jenkins C (2016) Shiga toxin-producing Escherichia coli O157, England and Wales, 1983–2012. Emerg Infect Dis 22(4):590–597CrossRefPubMedPubMedCentralGoogle Scholar
  3. Almanza AV (2012) Department of agriculture. Food safety and inspection service. 9 CFR Parts 416, 417, and 430. [Docket No. FSIS–2010–0023]. Shiga toxin-producing Escherichia coli in certain raw beef products. Fed Regist 77(105):31975–31981Google Scholar
  4. Alteri CJ, Mobley HL (2012) Escherichia coli physiology and metabolism dictates adaptation to diverse host microenvironments. Curr Opin Microbiol 15(1):3–9CrossRefPubMedGoogle Scholar
  5. Anonymous (1982) Isolation of E. coli O157:H7 from sporadic cases of hemorrhagic colitis–United States. MMWR Morb Mortal Wkly Rep 31(43):580–585Google Scholar
  6. Anonymous (2000) Waterborne outbreak of gastroenteritis associated with a contaminated municipal water supply, Walkerton, Ontario, May–June 2000. Can Commun Dis Rep 26(20):170–173Google Scholar
  7. Anonymous (2001) Outbreaks of Escherichia coli O157:H7 infections among children associated with farm visits—Pennsylvania and Washington, 2000. MMWR Morb Mortal Wkly Rep 50(15):293–297Google Scholar
  8. Anonymous (2002) Multistate outbreak of Escherichia coli O157:H7 infections associated with eating ground beef—United States, June–July 2002. MMWR Morb Mortal Wkly Rep 51(29):637–639Google Scholar
  9. Anonymous (2006) Ongoing multistate outbreak of Escherichia coli serotype O157:H7 infections associated with consumption of fresh spinach—United States, September 2006. MMWR Morb Mortal Wkly Rep 55(38):1045–1046Google Scholar
  10. Anonymous (2009) Outbreak of Shiga toxin-producing Escherichia coli O157 infection associated with a day camp petting zoo—Pinellas County, Florida, May–June 2007. MMWR Morb Mortal Wkly Rep 58(16):426–428Google Scholar
  11. Anonymous (2013) Surveillance for foodborne disease outbreaks—United States, 2009–2010. MMWR Morb Mortal Wkly Rep 62:41–47Google Scholar
  12. Anonymous (2016) Multistate Outbreaks of Shiga toxin-producing Escherichia coli O26 Infections Linked to Chipotle Mexican Grill Restaurants (Final Update). http://www.cdc.gov/ecoli/2015/o26-11-15/index.html
  13. Arnade C, Calvin L, Kuchler F (2009) Consumer response to a food safety shock: the 2006 food-borne illness outbreak of E. coli O157:H7 linked to Spinach. Rev Agric Econ 31(4):734–750CrossRefGoogle Scholar
  14. Auld H, MacIver D, Klaassen J (2004) Heavy rainfall and waterborne disease outbreaks: the Walkerton example. J Toxicol Environ Health A 67(20–22):1879–1887CrossRefPubMedGoogle Scholar
  15. Bell BP, Goldoft M, Griffin PM, Davis MA, Gordon DC, Tarr PI, Bartleson CA, Lewis JH, Barrett TJ, Wells JG 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(17):1349–1353CrossRefPubMedGoogle Scholar
  16. Besser RE, Lett SM, Weber JT, Doyle MP, Barrett TJ, Wells JG, Griffin PM (1993) An outbreak of diarrhea and hemolytic uremic syndrome from Escherichia coli O157:H7 in fresh-pressed apple cider. JAMA 269(17):2217–2220CrossRefPubMedGoogle Scholar
  17. 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):671–676CrossRefPubMedGoogle Scholar
  18. Bolduc D, Srour LF, Sweet L, Neatby A, Galanis E, Isaacs S, Lim G (2004) Severe outbreak of Escherichia coli O157:H7 in health care institutions in Charlottetown, Prince Edward Island, fall, 2002. Can Commun Dis Rep 30(9):81–88PubMedGoogle Scholar
  19. Bopp DJ, Sauders BD, Waring AL, Ackelsberg J, Dumas N, Braun-Howland E, Dziewulski D, Wallace BJ, Kelly M, Halse T, Musser KA, Smith PF, Morse DL, Limberger RJ (2003) Detection, isolation, and molecular subtyping of Escherichia coli O157:H7 and Campylobacter jejuni associated with a large waterborne outbreak. J Clin Microbiol 41(1):174–180CrossRefPubMedPubMedCentralGoogle Scholar
  20. Breuer T, Benkel DH, Shapiro RL, Hall WN, Winnett MM, Linn MJ, Neimann J, Barrett TJ, Dietrich S, Downes FP, Toney DM, Pearson JL, Rolka H, Slutsker L, Griffin PM (2001) A multistate outbreak of Escherichia coli O157:H7 infections linked to alfalfa sprouts grown from contaminated seeds. Emerg Infect Dis 7(6):977–982CrossRefPubMedPubMedCentralGoogle Scholar
  21. Brzuszkiewicz E, Thurmer A, Schuldes J, Leimbach A, Liesegang H, Meyer FD, Boelter J, Petersen H, Gottschalk G, Daniel R (2011) Genome sequence analyses of two isolates from the recent Escherichia coli outbreak in Germany reveal the emergence of a new pathotype: Entero-Aggregative-Haemorrhagic Escherichia coli (EAHEC). Arch Microbiol 193(12):883–891CrossRefPubMedPubMedCentralGoogle Scholar
  22. Buchholz U, Bernard H, Werber D, Bohmer MM, Remschmidt C, Wilking H, Delere Y, an der Heiden M, Adlhoch C, Dreesman J, Ehlers J, Ethelberg S, Faber M, Frank C, Fricke G, Greiner M, Hohle M, Ivarsson S, Jark U, Kirchner M, Koch J, Krause G, Luber P, Rosner B, Stark K, Kuhne M (2011) German outbreak of Escherichia coli O104:H4 associated with sprouts. N Engl J Med 365(19):1763–1770CrossRefPubMedGoogle Scholar
  23. Caprioli A, Scavia G, Morabito S (2014) Public health microbiology of Shiga toxin-producing Escherichia coli. Microbiol Spectr 2(6). doi: 10.1128/microbiolspec.EHEC-0014-2013
  24. Cieslak PR, Barrett TJ, Griffin PM, Gensheimer KF, Beckett G, Buffington J, Smith MG (1993) Escherichia coli O157:H7 infection from a manured garden. Lancet 342(8867):367CrossRefPubMedGoogle Scholar
  25. Cody SH, Glynn MK, Farrar JA, Cairns KL, Griffin PM, Kobayashi J, Fyfe M, Hoffman R, King AS, Lewis JH, Swaminathan B, Bryant RG, Vugia DJ (1999) An outbreak of Escherichia coli O157:H7 infection from unpasteurized commercial apple juice. Ann Intern Med 130(3):202–209CrossRefPubMedGoogle Scholar
  26. Cooley M, Carychao D, Crawford-Miksza L, Jay MT, Myers C, Rose C, Keys C, Farrar J, Mandrell RE (2007) Incidence and tracking of Escherichia coli O157:H7 in a major produce production region in California. PLoS One 2(11):e1159CrossRefPubMedPubMedCentralGoogle Scholar
  27. Council of State and Territorial Epidemiologists (CSTE). CSTE position statement #4: national surveillance of Escherichia coli O157:H7: Atlanta: Council of State and Territorial Epidemiologists, June 1993Google Scholar
  28. Dev VJ, Main M, Gould I (1991) Waterborne outbreak of Escherichia coli O157. Lancet 337(8754):1412CrossRefPubMedGoogle Scholar
  29. DuPont HL, Levine MM, Hornick RB, Formal SB (1989) Inoculum size in shigellosis and implications for expected mode of transmission. J Infect Dis 159(6):1126–1128CrossRefPubMedGoogle Scholar
  30. Elder RO, Keen JE, Siragusa GR, Barkocy-Gallagher GA, Koohmaraie M, Laegreid WW (2000) Correlation of enterohemorrhagic Escherichia coli O157 prevalence in feces, hides, and carcasses of beef cattle during processing. Proc Natl Acad Sci U S A 97(7):2999–3003CrossRefPubMedPubMedCentralGoogle Scholar
  31. Foodborne Disease Outbreak Surveillance System (FDOSS) http://www.cdc.gov/foodsafety/fdoss/surveillance/index.html
  32. Ferguson DD, Scheftel J, Cronquist A, Smith K, Woo-Ming A, Anderson E, Knutsen J, De AK, Gershman K (2005) Temporally distinct Escherichia coli 0157 outbreaks associated with alfalfa sprouts linked to a common seed source—Colorado and Minnesota, 2003. Epidemiol Infect 133(3):439–447CrossRefPubMedPubMedCentralGoogle Scholar
  33. The Foodborne Outbreak Online Database (FOODTool) http://wwwn.cdc.gov/foodborneoutbreaks/
  34. Frank C, Werber D, Cramer JP, Askar M, Faber M, an der Heiden M, Bernard H, Fruth A, Prager R, Spode A, Wadl M, Zoufaly A, Jordan S, Kemper MJ, Follin P, Muller L, King LA, Rosner B, Buchholz U, Stark K, Krause G (2011) Epidemic profile of Shiga-toxin-producing Escherichia coli O104:H4 outbreak in Germany. N Engl J Med 365(19):1771–1780CrossRefPubMedGoogle Scholar
  35. Frenzen PD, Drake A, Angulo FJ (2005) Economic cost of illness due to Escherichia coli O157 infections in the United States. J Food Prot 68(12):2623–2630CrossRefPubMedGoogle Scholar
  36. Friedman MS, Roels T, Koehler JE, Feldman L, Bibb WF, Blake P (1999) Escherichia coli O157:H7 outbreak associated with an improperly chlorinated swimming pool. Clin Infect Dis 29(2):298–303CrossRefPubMedGoogle Scholar
  37. Friesema I, Sigmundsdottir G, van der Zwaluw K, Heuvelink A, Schimmer B, de Jager C, Rump B, Briem H, Hardardottir H, Atladottir A, Gudmundsdottir E, van Pelt W (2008) An international outbreak of Shiga toxin-producing Escherichia coli O157 infection due to lettuce, September–October 2007. Euro Surveill 13(50)Google Scholar
  38. Fuller CA, Pellino CA, Flagler MJ, Strasser JE, Weiss AA (2011) Shiga toxin subtypes display dramatic differences in potency. Infect Immun 79(3):1329–1337CrossRefPubMedPubMedCentralGoogle Scholar
  39. Goode B, O'Reilly C, Dunn J, Fullerton K, Smith S, Ghneim G, Keen J, Durso L, Davies M, Montgomery S (2009) Outbreak of Escherichia coli O157: H7 infections after Petting Zoo visits, North Carolina State Fair, October–November 2004. Arch Pediatr Adolesc Med 163(1):42–48Google Scholar
  40. Gould LH, Mody RK, Ong KL, Clogher P, Cronquist AB, Garman KN, Lathrop S, Medus C, Spina NL, Webb TH, White PL, Wymore K, Gierke RE, Mahon BE, Griffin PM (2013) Increased recognition of non-O157 Shiga toxin-producing Escherichia coli infections in the United States during 2000–2010: epidemiologic features and comparison with E. coli O157 infections. Foodborne Pathog Dis 10(5):453–460CrossRefPubMedGoogle Scholar
  41. Grant J, Wendelboe AM, Wendel A, Jepson B, Torres P, Smelser C, Rolfs RT (2008) Spinach-associated Escherichia coli O157:H7 outbreak, Utah and New Mexico, 2006. Emerg Infect Dis 14(10):1633–1636CrossRefPubMedPubMedCentralGoogle Scholar
  42. Haley MM (2001) Changing Consumer Demand for Meat: The US Example, 1970–2000. In: Regmi A (ed) Changing Structure of Global Food Consumption and Trade. Economic Research Service of the United States Department of Agriculture, Washington, DC, pp 41–48 http://www.ers.usda.gov/media/293605/wrs293011g_293601_pdf
  43. Heiman KE, Mody RK, Johnson SD, Griffin PM, Gould LH (2015) Escherichia coli O157 Outbreaks in the United States, 2003–2012. Emerg Infect Dis 21(8):1293–1301CrossRefPubMedPubMedCentralGoogle Scholar
  44. Heuvelink AE, van Heerwaarden C, Zwartkruis-Nahuis JT, van Oosterom R, Edink K, van Duynhoven YT, de Boer E (2002) Escherichia coli O157 infection associated with a petting zoo. Epidemiol Infect 129(2):295–302CrossRefPubMedPubMedCentralGoogle Scholar
  45. Hilborn ED, Mermin JH, Mshar PA, Hadler JL, Voetsch A, Wojtkunski C, Swartz M, Mshar R, Lambert-Fair MA, Farrar JA, Glynn MK, Slutsker L (1999) A multistate outbreak of Escherichia coli O157:H7 infections associated with consumption of mesclun lettuce. Arch Intern Med 159(15):1758–1764CrossRefPubMedGoogle Scholar
  46. Hoffmann S, Maculloch B, Batz M (2015) Economic Burden of Major Foodborne Illnesses Acquired in the United States. Economic Information Bulletin EIB-140, 59 pp. http://www.ers.usda.gov/media/1837791/eib140.pdf
  47. Hrudey SE, Huck PM, Payment P, Gillham RW, Hrudey EJ (2002) Walkerton: lessons learned in comparison with waterborne outbreaks in the developed world. J Environ Eng Sci 1:397–407CrossRefGoogle Scholar
  48. Hrudey SE, Payment P, Huck PM, Gillham RW, Hrudey EJ (2003) A fatal waterborne disease epidemic in Walkerton, Ontario: comparison with other waterborne outbreaks in the developed world. Water Sci Technol 47(3):7–14PubMedGoogle Scholar
  49. Hussein HS, Bollinger LM (2005) Prevalence of Shiga toxin-producing Escherichia coli in beef cattle. J Food Prot 68(10):2224–2241CrossRefPubMedGoogle Scholar
  50. Hynds PD, Thomas MK, Pintar KD (2014) Contamination of groundwater systems in the US and Canada by enteric pathogens, 1990–2013: a review and pooled-analysis. PLoS One 9(5):e93301CrossRefPubMedPubMedCentralGoogle Scholar
  51. Jay MT, Cooley M, Carychao D, Wiscomb GW, Sweitzer RA, Crawford-Miksza L, Farrar JA, Lau DK, O'Connell J, Millington A, Asmundson RV, Atwill ER, Mandrell RE (2007) Escherichia coli O157:H7 in feral swine near spinach fields and cattle, central California coast. Emerg Infect Dis 13(12):1908–1911CrossRefPubMedPubMedCentralGoogle Scholar
  52. Karmali MA, Gannon V, Sargeant JM (2010) Verocytotoxin-producing Escherichia coli (VTEC). Vet Microbiol 140(3–4):360–370CrossRefPubMedGoogle Scholar
  53. Karmali MA, Steele BT, Petric M, Lim C (1983) Sporadic cases of haemolytic-uraemic syndrome associated with faecal cytotoxin and cytotoxin-producing Escherichia coli in stools. Lancet 1(8325):619–620CrossRefPubMedGoogle Scholar
  54. Kassenborg HD, Hedberg CW, Hoekstra M, Evans MC, Chin AE, Marcus R, Vugia DJ, Smith K, Ahuja SD, Slutsker L, Griffin PM (2004) Farm visits and undercooked hamburgers as major risk factors for sporadic Escherichia coli O157:H7 infection: data from a case-control study in 5 FoodNet sites. Clin Infect Dis 38(Suppl 3):S271–S278CrossRefPubMedGoogle Scholar
  55. Keene WE, McAnulty JM, Hoesly FC, Williams LP Jr, Hedberg K, Oxman GL, Barrett TJ, Pfaller MA, Fleming DW (1994) A swimming-associated outbreak of hemorrhagic colitis caused by Escherichia coli O157:H7 and Shigella sonnei. N Engl J Med 331(9):579–584CrossRefPubMedGoogle Scholar
  56. Kozak GK, MacDonald D, Landry L, Farber JM (2013) Foodborne outbreaks in Canada linked to produce: 2001 through 2009. J Food Prot 76(1):173–183CrossRefPubMedGoogle Scholar
  57. Lascowski KM, Guth BE, Martins FH, Rocha SP, Irino K, Pelayo JS (2013) Shiga toxin-producing Escherichia coli in drinking water supplies of north Parana State, Brazil. J Appl Microbiol 114(4):1230–1239CrossRefPubMedGoogle Scholar
  58. McGrath J (2009) 10 Costy Food Recalls. HowStuffWorks. http://money.howstuffworks.com/10-food-recalls.htm/printable
  59. Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, Shapiro C, Griffin PM, Tauxe RV (1999) Food-related illness and death in the United States. Emerg Infect Dis 5(5):607–625CrossRefPubMedPubMedCentralGoogle Scholar
  60. Michino H, Araki K, Minami S, Takaya S, Sakai N, Miyazaki M, Ono A, Yanagawa H (1999) Massive outbreak of Escherichia coli O157:H7 infection in schoolchildren in Sakai City, Japan, associated with consumption of white radish sprouts. Am J Epidemiol 150(8):787–796CrossRefPubMedGoogle Scholar
  61. Miszczycha SD, Thevenot J, Denis S, Callon C, Livrelli V, Alric M, Montel MC, Blanquet-Diot S, Thevenot-Sergentet D (2014) Survival of Escherichia coli O26:H11 exceeds that of Escherichia coli O157:H7 as assessed by simulated human digestion of contaminated raw milk cheeses. Int J Food Microbiol 172:40–48CrossRefPubMedGoogle Scholar
  62. Miyata K, Yoneyama T, Suzuki T, Kouguchi H, Inui K, Niwa K, Watanabe T, Ohyama T (2009) Expression and stability of the nontoxic component of the botulinum toxin complex. Biochem Biophys Res Commun 384(1):126–130CrossRefPubMedGoogle Scholar
  63. Morbidity and Mortality Weekly Report (MMWR) http://www.cdc.gov/mmwr/index.html
  64. Mohle-Boetani JC, Farrar JA, Werner SB, Minassian D, Bryant R, Abbott S, Slutsker L, Vugia DJ (2001) Escherichia coli O157 and Salmonella infections associated with sprouts in California, 1996–1998. Ann Intern Med 135(4):239–247CrossRefPubMedGoogle Scholar
  65. Morgan GM, Newman C, Palmer SR, Allen JB, Shepherd W, Rampling AM, Warren RE, Gross RJ, Scotland SM, Smith HR (1988) First recognized community outbreak of haemorrhagic colitis due to verotoxin-producing Escherichia coli O 157.H7 in the UK. Epidemiol Infect 101(1):83–91CrossRefPubMedPubMedCentralGoogle Scholar
  66. Muto T, Matsumoto Y, Yamada M, Ishiguro Y, Kitazume H, Sasaki K, Toba M (2008) Outbreaks of enterohemorrhagic Escherichia coli O157 infections among children with animal contact at a dairy farm in Yokohama City, Japan. Jpn J Infect Dis 61(2):161–162PubMedGoogle Scholar
  67. Nataro JP, Kaper JB (1998) Diarrheagenic Escherichia coli. Clin Microbiol Rev 11(1):142–201PubMedPubMedCentralGoogle Scholar
  68. Neil KP, Biggerstaff G, MacDonald JK, Trees E, Medus C, Musser KA, Stroika SG, Zink D, MJ S (2012) A novel vehicle for transmission of Escherichia coli O157:H7 to humans: multistate outbreak of E. coli O157:H7 infections associated with consumption of ready-to-bake commercial prepackaged cookie dough—United States, 2009. Clin Infect Dis 54(4):511–518CrossRefPubMedGoogle Scholar
  69. National Outbreak Reporting System (NORS) http://www.cdc.gov/nors/
  70. Olsen SJ, Miller G, Breuer T, Kennedy M, Higgins C, Walford J, McKee G, Fox K, Bibb W, Mead P (2002) A waterborne outbreak of Escherichia coli O157:H7 infections and hemolytic uremic syndrome: implications for rural water systems. Emerg Infect Dis 8(4):370–375CrossRefPubMedPubMedCentralGoogle Scholar
  71. Paddock ZD, Bai J, Shi X, Renter DG, Nagaraja TG (2013) Detection of Escherichia coli O104 in the feces of feedlot cattle by a multiplex PCR assay designed to target major genetic traits of the virulent hybrid strain responsible for the 2011 German outbreak. Appl Environ Microbiol 79(11):3522–3525CrossRefPubMedPubMedCentralGoogle Scholar
  72. Paunio M, Pebody R, Keskimaki M, Kokki M, Ruutu P, Oinonen S, Vuotari V, Siitonen A, Lahti E, Leinikki P (1999) Swimming-associated outbreak of Escherichia coli O157:H7. Epidemiol Infect 122(1):1–5CrossRefPubMedPubMedCentralGoogle Scholar
  73. Persad AK, LeJeune JT (2014) Animal reservoirs of Shiga toxin-producing Escherichia coli. Microbiol Spectr 2(4):EHEC-0027-2014CrossRefPubMedGoogle Scholar
  74. Pollack SL (2001) Consumer demand for fruit and vegetables: the U.S. example. Economic Research Service of United States Department of Agriculture, Washington, DCGoogle Scholar
  75. Renwick SA, Wilson JB, Clarke RC, Lior H, Borczyk AA, Spika J, Rahn K, McFadden K, Brouwer A, Copps A et al (1993) Evidence of direct transmission of Escherichia coli O157:H7 infection between calves and a human. J Infect Dis 168(3):792–793CrossRefPubMedGoogle Scholar
  76. Riley LW, Remis RS, Helgerson SD, McGee HB, Wells JG, Davis BR, Hebert RJ, Olcott ES, Johnson LM, Hargrett NT, Blake PA, Cohen ML (1983) Hemorrhagic colitis associated with a rare Escherichia coli serotype. N Engl J Med 308(12):681–685CrossRefPubMedGoogle Scholar
  77. Rowell S, King C, Jenkins C, Dallman TJ, Decraene V, Lamden K, Howard A, Featherstone CA, Cleary P (2016) An outbreak of Shiga toxin-producing Escherichia coli serogroup O157 linked to a lamb-feeding event. Epidemiol Infect 144(12):2494–2500CrossRefPubMedGoogle Scholar
  78. Russo LM, Melton-Celsa AR, Smith MA, Smith MJ, O’Brien AD (2014) Oral intoxication of mice with Shiga toxin type 2a (Stx2a) and protection by anti-Stx2a monoclonal antibody 11E10. Infect Immun 82(3):1213–1221CrossRefPubMedPubMedCentralGoogle Scholar
  79. Samadpour M, Stewart J, Steingart K, Addy C, Louderback J, McGinn M, Ellington J, Newman T (2002) Laboratory investigation of an E. coli O157:H7 outbreak associated with swimming in Battle Ground Lake, Vancouver, Washington. J Environ Health 64(10):16–20 , 26, 25PubMedGoogle Scholar
  80. 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):7–15CrossRefPubMedPubMedCentralGoogle Scholar
  81. Shridhar PB, Noll LW, Shi X, Cernicchiaro N, Renter DG, Bai J, Nagaraja TG (2016) Escherichia coli O104 in feedlot cattle feces: prevalence, isolation and characterization. PLoS One 11(3):e0152101CrossRefPubMedPubMedCentralGoogle Scholar
  82. Sivapalasingam S, Friedman CR, Cohen L, Tauxe RV (2004) Fresh produce: a growing cause of outbreaks of foodborne illness in the United States, 1973 through 1997. J Food Prot 67(10):2342–2353CrossRefPubMedGoogle Scholar
  83. Skinner C, McMahon S, Rasooly R, Carter JM, He X (2013) Purification and characterization of shiga toxin 2f, an immunologically unrelated subtype of shiga toxin 2. PLoS One 8(3):e59760. doi: 10.51371/journal.pone.0059760 CrossRefPubMedPubMedCentralGoogle Scholar
  84. Soderstrom A, Osterberg P, Lindqvist A, Jonsson B, Lindberg A, Blide Ulander S, Welinder-Olsson C, Lofdahl S, Kaijser B, De Jong B, Kuhlmann-Berenzon S, Boqvist S, Eriksson E, Szanto E, Andersson S, Allestam G, Hedenstrom I, Ledet Muller L, Andersson Y (2008) A large Escherichia coli O157 outbreak in Sweden associated with locally produced lettuce. Foodborne Pathog Dis 5(3):339–349CrossRefPubMedGoogle Scholar
  85. Stirling J, Griffith M, Dooley JS, Goldsmith CE, Loughrey A, Lowery CJ, McClurg R, McCorry K, McDowell D, McMahon A, Millar BC, Rao J, Rooney PJ, Snelling WJ, Matsuda M, Moore JE (2008) Zoonoses associated with petting farms and open zoos. Vector Borne Zoonotic Dis 8(1):85–92CrossRefPubMedGoogle Scholar
  86. Swerdlow DL, Woodruff BA, Brady RC, Griffin PM, Tippen S, Donnell HD Jr, Geldreich E, Payne BJ, Meyer A Jr, Wells JG et al (1992) A waterborne outbreak in Missouri of Escherichia coli O157:H7 associated with bloody diarrhea and death. Ann Intern Med 117(10):812–819CrossRefPubMedGoogle Scholar
  87. Taormina PJ, Beuchat LR, Slutsker L (1999) Infections associated with eating seed sprouts: an international concern. Emerg Infect Dis 5(5):626–634CrossRefPubMedPubMedCentralGoogle Scholar
  88. Tarr PI, Gordon CA, Chandler WL (2005) Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet 365(9464):1073–1086PubMedGoogle Scholar
  89. Taylor CM, White RH, Winterborn MH, Rowe B (1986) Haemolytic-uraemic syndrome: clinical experience of an outbreak in the West Midlands. Br Med J (Clin Res Ed) 292(6534):1513–1516CrossRefGoogle Scholar
  90. Terajima J, Iyoda S, Ohnishi M, Watanabe H (2014) Shiga toxin (verotoxin)-producing Escherichia coli in Japan. Microbiol Spectr 2(5)Google Scholar
  91. Tesh VL, Burris JA, Owens JW, Gordon VM, Wadolkowski EA, O'Brien AD, Samuel JE (1993) Comparison of the relative toxicities of Shiga-like toxins type I and type II for mice. Infect Immun 61(8):3392–3402PubMedPubMedCentralGoogle Scholar
  92. Tilden J Jr, Young W, McNamara AM, Custer C, Boesel B, Lambert-Fair MA, Majkowski J, Vugia D, Werner SB, Hollingsworth J, Morris JG Jr (1996) A new route of transmission for Escherichia coli: infection from dry fermented salami. Am J Public Health 86(8):1142–1145CrossRefPubMedPubMedCentralGoogle Scholar
  93. Tozzoli R, Scheutz F (2014) Diarrhoeagenic Escherichia coli infections in humans. In: Morabito S (ed) Pathogenic Escherichia coli: molecular and cellular microbiology. Caister Academic Press, Norfolk, UK, pp 1–18Google Scholar
  94. U.S. Food and Drug Administration (US-FDA) (2006). FDA statement on foodborne E. coli O157:H7 outbreak in spinach. http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/2006/ucm108761.htm. Accessed 31 Aug 2016
  95. Varma JK, Greene KD, Reller ME, DeLong SM, Trottier J, Nowicki SF, DiOrio M, Koch EM, Bannerman TL, York ST, Lambert-Fair MA, Wells JG, Mead PS (2003) An outbreak of Escherichia coli O157 infection following exposure to a contaminated building. JAMA 290(20):2709–2712CrossRefPubMedGoogle Scholar
  96. Verma A, Bolton FJ, Fiefield D, Lamb P, Woloschin E, Smith N, McCann R (2007) An outbreak of E. coli O157 associated with a swimming pool: an unusual vehicle of transmission. Epidemiol Infect 135(6):989–992CrossRefPubMedPubMedCentralGoogle Scholar
  97. Vojdani JD, Beuchat LR, Tauxe RV (2008) Juice-associated outbreaks of human illness in the United States, 1995 through 2005. J Food Prot 71(2):356–364CrossRefPubMedGoogle Scholar
  98. Waterborne Disease & Outbreak Surveillance & Reporting (WDOSR) http://www.cdc.gov/healthywater/surveillance/index.html
  99. Weissman JB, Craun GF, Lawrence DN, Pollard RA, Saslaw MS, Gangarosa EJ (1976) An epidemic of gastroenteritis traced to a contaminated public water supply. Am J Epidemiol 103(4):391–398CrossRefPubMedGoogle Scholar
  100. Wells JG, Davis BR, Wachsmuth IK, Riley LW, Remis RS, Sokolow R, Morris GK (1983) Laboratory investigation of hemorrhagic colitis outbreaks associated with a rare Escherichia coli serotype. J Clin Microbiol 18(3):512–520PubMedPubMedCentralGoogle Scholar
  101. Wieler LH, Semmler T, Eichhorn I, Antao EM, Kinnemann B, Geue L, Karch H, Guenther S, Bethe A (2011) No evidence of the Shiga toxin-producing E. coli O104:H4 outbreak strain or enteroaggregative E. coli (EAEC) found in cattle faeces in northern Germany, the hotspot of the 2011 HUS outbreak area. Gut Pathog 3(1):17CrossRefPubMedPubMedCentralGoogle Scholar
  102. Wikswo ME, Hall AJ (2012) Outbreaks of acute gastroenteritis transmitted by person-to-person contact—United States, 2009–2010. MMWR Surveill Summ 61(9):1–12PubMedGoogle Scholar
  103. Wilson JB, Clarke RC, Renwick SA, Rahn K, Johnson RP, Karmali MA, Lior H, Alves D, Gyles CL, Sandhu KS, McEwen SA, Spika JS (1996) Vero cytotoxigenic Escherichia coli infection in dairy farm families. J Infect Dis 174(5):1021–1027CrossRefPubMedGoogle Scholar
  104. Yarze JC, Chase MP (2000) E. coli O157:H7—another waterborne outbreak! Am J Gastroenterol 95(4):1096PubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Christopher J. Silva
    • 1
  • David L. Brandon
    • 1
  • Craig B. Skinner
    • 1
  • Xiaohua He
    • 1
  1. 1.United States Department of Agriculture, Agricultural Research ServiceWestern Regional Research CenterAlbanyUSA

Personalised recommendations