Abstract
Enterohemorrhagic Escherichia coli (EHEC) are a pathogenic subgroup of Shiga toxin-producing E. coli (STEC), and have demonstrated ability to cause severe intestinal disease and the hemolytic uremic syndrome (HUS). Cattle are the major reservoir of EHEC, where the bacteria can persist asymptomatically for years. Of particular concern are a small percentage of animals in herds that shed extremely high numbers of EHEC, termed ‘supershedders’, and are responsible for the majority of EHEC spread and contamination. Another transmission route is through the environment where EHEC can survive for weeks to many months, remaining viable in bovine feces, soil and water. EHEC contamination of meat during slaughter or processing, or contamination of plants via EHEC-containing water or manure are major routes of entry into the food chain. Several hundred outbreaks caused by EHEC O157 as well as non-O157 strains have been identified in industrialized countries worldwide. Current and future research efforts are focused on rapid outbreak identification, development of therapeutics, and implementation of preventative measures.
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1 Introduction
Most members of the species E. coli are part of the physiological flora in the gastrointestinal tracts of humans and animals. In addition to these commensal bacteria, there are pathogenic E. coli that cause extraintestinal and intestinal disease. Intestinal pathogenic E. coli presently include seven pathogroups: enterotoxigenic E. coli (ETEC), enteroinvasive E. coli (EIEC), enteroaggregative E. coli (EAEC), enteropathogenic E. coli (EPEC), adherent invasive E. coli (AIEC), diffusely adherent E. coli (DAEC) and enterohemorrhagic E. coli (EHEC) (Croxen et al. 2013). Each pathotype is associated with unique epidemiology and specific pathological diseases that cause significant morbidity and mortality. Zoonotic E. coli, of which EHEC are the prototype, pose many challenges to the food industry and public health and are intensively studied in human and veterinary medicine. Ongoing investigations are concerned with both ecology of EHEC in animals and persistence and survival in the environment, and how these factors affect entry into or dissemination along the food chain. Other areas of research are the epidemiology of EHEC infections in humans, diagnostics, pathogenic mechanisms of these bacteria and treatment as there is currently no specific therapy.
EHEC can cause a broad clinical spectrum of disease including watery or bloody diarrhea, and the hemolytic uremic syndrome (HUS), which is an important cause of acute renal failure in children (Tarr et al. 2005). Since the first isolation of an EHEC serotype O157:H7 outbreak strain in the USA in 1982 (Riley et al. 1983), and subsequent identification of involvement of this pathogen in outbreaks of hemorrhagic colitis and HUS (Wells et al. 1983), EHEC has emerged as an important public health concern worldwide. The large EHEC O104:H4 outbreak in Germany in 2011 with 3842 cases, 855 HUS patients and 53 deaths demonstrates the significant impact of an EHEC outbreak on human health (RKI 2011) .
2 Expression of Shiga Toxins in EHEC
A key characteristic of the EHEC pathotype is the presence of Shiga toxins (Stx). Stx, also known as verocytotoxins (VTs) , are members of a large family of cytotoxins that are characterized by a high degree of sequence diversity. The Stx family is divided into two major branches, Stx1 and Stx2, and many toxin subtypes and variants have been described in both branches (Karch et al. 2009; Bergan et al. 2012; Scheutz et al. 2012). Classification of Stx subtypes is used not only for taxonomic purposes, but also serves as an important predictor for the various clinically relevant Stxs found in strains associated with HUS versus other Stx subtypes that are carried by strains causing a milder course of disease (Scheutz et al. 2012). A sequence-based protocol for characterization of the Stx genes has been recently described (Scheutz et al. 2012), and includes three levels of classification: Types, subtypes and variants (see Table 9.1).
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1.
Types
The two major branches Stx1 and Stx2 share structure and function but are not cross neutralized with heterologous antibodies. The terms Stx1 and Stx2 should only be used when the subtype is unknown.
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2.
Subtypes
Currently the antigenically related members of Stx1 (Stx1a, Stx1c, and Stx1d) and Stx2 (Stx2a, Stx2b, Stx2c, Stx2d, Stx2e, Stx2f, and Stx2g) are distinguished.
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3.
Variants
Variants include the subtype-specific prototypic toxins or related toxins within a subtype (that differ by one or more amino acids from the prototype). The variants are designated by toxin subtype, O-antigen group of the host E. coli strain, followed by the strain name or number from which that toxin was described, e.g. Stx1a-O157-EDL933 or Stx2a-O104-G5506 (Scheutz et al. 2012, see Table 9.1). Nucleotide variants within a given Stx subtype are italicized.
All Stx consist of a single A and five B subunits. The A subunit represents the enzymatically active component. The Stx B pentamer binds to the high and less effective cellular ligand glycosphingolipids (GSLs), globotriaosylceramide (Gb3Cer) and globotetraosylceramide (Gb4Cer), respectively (Müthing et al. 2009). Stx1 and Stx2 share identical binding specificity (Müthing et al. 2009). After binding to the cell surface, the AB5-Gb3Cer complex is internalized by various endocytic mechanisms and routed from the early endosomes through the trans-Golgi-network and the Golgi stacks to the endoplasmic reticulum (Sandvig et al. 2010; Bauwens et al. 2013). Moreover, evidence suggests that Stxs (like other ribosome-inactivating proteins) remove adenine moieties not only from rRNA, but also efficiently depurinate DNA. Stx genes are found within the genomes of temperate bacteriophages, which are mobile elements that can easily integrate at specific sites in the bacterial chromosome. In vitro and in vivo studies have demonstrated that most EHEC can lose the Stx-encoding gene by bacteriophage excision during infection, isolation, or subculture, resulting in stx-negative isolates (Mellmann et al. 2009).
3 Epidemiology of EHEC in Animals
Several studies have demonstrated that cattle are the main reservoir of human pathogenic EHEC O157:H7, in addition to many pathogenic non-O157 EHEC serotypes (Naylor et al. 2005a) . These bacteria have adapted to an oral-fecal cycle in cattle, where EHEC colonization begins with ingestion and subsequent entrance to the rumen and gastrointestinal tract, but they generally do not have a pathogenic effect on adult animals. EHEC has been reported to cause disease in young calves, however, in particular certain non-O157 serogroups (O26, O111, O118) (Naylor et al. 2005a). Prevalence among cattle varies widely, and may be due to several circumstances including the geographical region, animal age, or the specific farm conditions (Ferens and Hovde 2011). Published prevalence rates vary dramatically, from 0 to 36 % among animals studied in different countries and farm types (Naylor et al. 2005a). Studies have also shown that EHEC prevalence is related to the type of farm (e.g. beef, dairy) and may be influenced by factors such as cattle movement, hygiene management, diet, and husbandry (Menrath et al. 2010; Cobbaut et al. 2009; Ferens and Hovde 2011). While cattle are the major known reservoir of EHEC, other minor reservoirs include sheep, goats , pigs, horses , dogs, poultry , and deer (Naylor et al. 2005a) .
The persistence of EHEC O157:H7 in cattle may be due to its ability to colonize a particular niche within the lower gastrointestinal tract (Grauke et al. 2002). Tissue tropism for the colon has been demonstrated by immunofluorescent detection of microcolonies at the lymphoid follicle-dense mucosa at the terminal rectum within 3–5 cm proximal to the rectoanal junction (Grauke et al. 2002; Naylor et al. 2003, 2005b). This rectoanal junction colonization is hypothesized to be responsible for a highlevel of EHEC O157:H7 shedding (104 CFU/g of feces) in a minor subset of cattle which are termed ‘supershedders’ and are thought to be responsible for most of the pathogen spread in a farm environment (Menrath et al. 2010). In support of this theory, an association between rectoanal junction colonization and supershedding status has been described (Cobbold et al. 2007; Low 2005). Furthermore, EHEC O157 and non-O157 strains express several fimbrial and afimbrial proteins that likely play a role in ruminant reservoir persistence (Farfan and Torres 2012). In studies that used bovine terminal rectal primary epithelial cells, the H7 flagellum was demonstrated to act as an adhesin to bovine intestinal epithelium, supporting its involvement in the initiating step for colonization of the cattle reservoir (Mahajan 2009). Stx may also play a role in colonization and persistence by blocking the activation of bovine lymphocytes and thus supressing the bovine host’s immune response to the intestinal colonization (Moussay et al. 2006) .
4 EHEC in the Environment
EHEC can survive in bovine feces long-term, making this a likely vehicle for transmission to cattle, food and the environment. Survival in feces can range from 1 to 18 weeks depending on the temperature (5, 15 and 25 °C were tested) (Fukushima et al.1999). Entry of EHEC to the environment may occur through direct deposit of feces onto land or through drainage runoff of fecal material in soil, especially after heavy rainfalls (Thurston-Enriquez et al. 2005). Moreover, under experimental conditions, EHEC can survive for more than 1 year in various manure-amended soils at different temperatures (Fremaux et al. 2008). Long-term survival of EHEC in lake water (13 weeks) and in cold river water has also been demonstrated (Wang and Doyle 1998; Maule 2000). This extended persistence in the environment likely plays a significant role in the colonization of cattle and subsequent human infection (Fremaux et al. 2008).
EHEC O157:H7 is also able to colonize various types of plants and fruits. For example, EHEC O157:H7 has been shown to form bacterial aggregates on apples (Janes et al. 2005) as well as on the surface of lettuce leaves (Seo and Frank 1999; Auty et al. 2005). Furthermore, studies have found EHEC in the internal inner tissues of plants, including radishes, carrots and lettuce (Itoh et al. 1998; Solomon et al. 2002). These subsurface localizations may be protective to the bacteria as they are inaccessible to other competitive bacteria as well as surface treatments and washing.
5 EHEC Infections in Humans
After ingestion of EHEC, a 3–12 day incubation period is typically followed by development of watery diarrhea accompanied with abdominal cramping and pain. Most patients will subsequently suffer from bloody diarrhea. About 1 week after the initial onset of diarrhea, HUS develops in a variable proportion of cases, depending on the serotype of the causative EHEC strain and the Stx subtype (Tarr et al. 2005). HUS patients present with widespread thrombotic microvascular lesions in the kidneys, the gastrointestinal tract, and other organs (Richardson et al. 1988). Since EHEC infections are rarely bacteremic, i.e. bacteria do not penetrate the circulatory system and are not found in patient blood cultures (Bielaszewska and Karch 2005), it is hypothesized that HUS results from vascular endothelial injury by circulating Stx. According to the generally accepted model of HUS pathogenesis, Stx is released by EHEC in the intestine, absorbed across the gut epithelium into the circulation (Hurley et al. 2001; Müthing et al. 2009), and transported to small vessel endothelial cells.
HUS is the most common cause of acute renal failure in children. The mortality rate can be up to 3 % (Karch et al. 2005). While 70 % of EHEC-infected patients were fully recovered within 5 years after diagnosis, the remaining 30 % still experienced persistent hypertension (9 %), neurological symptoms (4 %), decreased glomerular filtration rate (7 %), and/or proteinuria (18 %) (Rosales et al. 2012). There is currently no effective causative therapy, and antibiotic treatment appears to be ineffective if not harmful (Wong et al. 2000; Davis et al. 2013). In contrast to cattle, EHEC O157:H7 colonizes humans only for a limited time of about 4 weeks (Fig. 9.1; Karch et al. 1995). Moreover, whereas in cattle many different EHEC O157:H7 PFGE subtypes can co-exist in a single animal (Jacob et al. 2011), human patients are infected mostly by a distinct O157:H7 PFGE subtype.
EHEC O157:H7 is the most prevalent EHEC serotype identified as a cause of sporadic HUS cases (Tarr et al. 2005; Karch et al. 2005). Still, non-O157:H7 EHEC (especially O26:H11, O103:H2, O111:H8, O145:H28/H25 and sorbitol-fermenting (SF) O157:H−) represent a significant portion of EHEC infections leading to HUS complications (Karch et al. 2005; Mellmann et al. 2008; Bielaszewska et al. 2013). Though EHEC strains are often considered as a pathogroup, there may be important differences between serotypes.
SF EHEC O157:H− represent a significant serotype in Europe which has not yet been detected in North America. These strains are characterized by a specific combination of their phenotypic and virulence characteristics that differentiates them from classical non-SF EHEC O157:H7 (Karch and Bielaszewska 2001). This combination includes the ability to ferment sorbitol overnight and to produce β-D-glucuronidase. A gene cluster termed sfp, which encodes fimbriae and mediates mannose-resistant hemagglutination, has been identified on the large plasmid of SF STEC O157:H− (Brunder et al. 2001). Notably, Sfp-encoding genes are absent in EHEC O157:H7.
The minimum infectious dose of EHEC in humans is extremely low, with approximately 10–50 bacteria needed for colonization (Teunis et al. 2004). In meat implicated as an outbreak source in the USA in 1993 there were less than 700 EHEC O157:H7 bacterial cells per hamburger patty prior to cooking (Tuttle et al. 1999). Moreover, a high degree of tolerance to acid and drying enables EHEC to survive in food items, the consumption of which had been previously considered safe with respect to the ability to cause foodborne illness (e.g., apple cider, semi-dry fermented sausage). Three principal routes of transmission of EHEC infection have been identified: (1) contaminated food and contaminated water used for drinking or swimming, (2) person-to-person transmission, and (3) animal contact, for example in petting zoos housing domesticated sheep, goats and other small animals or (occupational) farm exposure (Crump et al. 2002; Karch et al. 2005).
6 EHEC Outbreaks
EHEC is the cause of hundreds of outbreaks worldwide (Griffin et al. 1988; Michino et al. 1999; Karch et al. 1999). Examples of large outbreaks, including clinical impact and source, caused by EHEC O157:H7 and non-O157 are described in Tables 9.2 and 9.3, respectively. Consumption of raw or undercooked food items of bovine origin, particularly ground beef (hamburger), are common modes of EHEC O157:H7 transmission (Table 9.2). Moreover, contaminated radish sprouts, lettuce, spinach, strawberries, and contaminated water have been implicated in transmitting EHEC O157:H7 (Table 9.2).
One of the largest outbreaks to date occurred in Japan, in Sakai City, in 1996 (Watanabe et al. 1996; Michino et al. 1999), where thousands were affected, mostly school children. White radish sprouts served during school lunches were the most probable vehicle of the infection. In the winter 1992–1993, the largest outbreak of EHEC O157:H7 infection in the United States affected 501 persons in four western states including Washington, Idaho, Nevada and California (Bell et al. 1994) where 45 persons, mostly children, developed HUS and three children died. Hamburgers from a single fast-food restaurant chain were identified as the vehicle of the infection (Bell et al. 1994). The largest outbreak caused by contaminated drinking water occurred in Canada in 2000. Approximately 2300 people became seriously ill and seven died from exposure to drinking water contaminated with EHEC O157:H7. In Europe, a large EHEC O157:H7 outbreak occurred in Central Scotland in 1996; 345 people contracted an infection after consuming meat from a single butcher’s shop, and 16 died (Dundas et al. 2001).
Table 9.3 describes several examples of large outbreaks caused by non-O157 EHEC strains. These include a wide range of serotypes, with the largest non-O157 outbreak occurring in Germany in 2011 associated with the contamination of fenugreek sprouts by EHEC O104:H4 (RKI 2011; Karch et al. 2012).
7 Future Strategies and Unresolved Issues
Advances in rapid alert systems for the early detection of EHEC outbreaks have created greater awareness for both the public as well as the clinical community. Moreover, an increasing number of clinical microbiological laboratories routinely screen for EHEC by detection of Stx genes and/or toxin production. Diagnosed cases are now legally required to be reported in nearly every country. New high resolution techniques including next generation sequencing (NGS) are becoming more accessible and widely used, which enable the rapid identification of outbreaks at the earliest stages (Mellmann et al. 2011). In the future, databases and nationwide reporting systems could be in place to facilitate outbreak prevention and public health. The value of such strain linkage analysis is obvious. Common sources of infection can be identified accurately and rapidly. This is especially important considering the emerging epidemiology of foodborne infections. In particular, foodborne outbreaks nowadays less frequently follow the “church picnic” model, in which small isolated clusters of illness can easily be identified with case interviews. Instead, current outbreaks now more frequently result from the dissemination of vehicles that are contaminated by relatively low levels of pathogens. Such outbreaks can occur across state lines and international borders.
Another area where considerable efforts are being expended to bring improvement are the farming practices and environmental factors that affect infection of animals with EHEC. EHEC transmits readily between ruminants in the farm setting and wild animals can represent important vectors. For many years, the cattle industry and researchers have focused on improving the safety of meat products after slaughter. Postslaughter antimicrobial treatments of carcasses and HACCP policies in slaughter plants have been shown to significantly reduce meat contamination (Elder et al. 2000).
Due to the widespread distribution of EHEC O157 and non-O157 in farm cattle, its control will require intervention at the individual farm level. Recently, two vaccines against EHEC O157:H7 that are designed for use in cattle have been developed. While use of these vaccines could reduce the risk of EHEC in cattle by 50 %, which translates to approximately 85 % reduction in human cases, these vaccines have not yet been widely accepted by farmers due to several factors including burden of responsibility and economic factors (Matthews et al. 2013). An alternative route for the control of EHEC in cattle may be the feeding of probiotic bacteria, which can compete and interfere with pathogenic strains by producing metabolites that are inhibitory to EHEC. Still, more research is needed to develop viable strategies targeting the different levels (cattle, food, person-to-person spread, etc.) to control EHEC.
Further research is also needed to address effective therapies for humans after EHEC infection. Ongoing investigations are focused on topics such as toxin binders and Stx neutralizing immunoglobulin preparations.
References
Auty M, Duffy G, O’Beirne D, McGovern A, Gleeson E, Jordan K (2005) In situ localization of Escherichia coli O157:H7 in food by confocal scanning laser microscopy. J Food Prot 68(3):482–486
Bauwens A, Betz J, Meisen I, Kemper B, Karch H, Müthing J (2013) Facing glycosphingolipid-Shiga toxin interaction: dire straits for endothelial cells of the human vasculature. Cell Mol Life Sci 70(3):425–457. doi:10.1007/s00018-012-1060-z
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):1349–1353
Bergan J, Dyve Lingelem AB, Simm R, Skotland T, Sandvig K (2012) Shiga toxins. Toxicon 60(6):1085–1107. doi:10.1016/j.toxicon.2012.07.016
Bielaszewska M, Karch H (2005) Consequences of enterohaemorrhagic Escherichia coli infection for the vascular endothelium. Thromb Haemost 94(2):312–318. doi:10.1267/THRO05020312
Bielaszewska M, Mellmann A, Bletz S, Zhang W, Köck R, Kossow A, Prager R, Fruth A, Orth-Holler D, Marejkova M, Morabito S, Caprioli A, Pierard D, Smith G, Jenkins C, Curova K, Karch H (2013) Enterohemorrhagic Escherichia coli O26:H11/H-: a new virulent clone emerges in Europe. Clin Infect Dis 56(10):1373–1381. doi:10.1093/cid/cit055
Brooks JT, Bergmire-Sweat D, Kennedy M, Hendricks K, Garcia M, Marengo L, Wells J, Ying M, Bibb W, Griffin PM, Hoekstra RM, Friedman CR (2004) Outbreak of Shiga toxin-producing Escherichia coli O111:H8 infections among attendees of a high school cheerleading camp. Clin Infect Dis 38(2):190–198. doi:10.1086/380634
Brunder W, Khan AS, Hacker J, Karch H (2001) Novel type of fimbriae encoded by the large plasmid of sorbitol-fermenting enterohemorrhagic Escherichia coli O157:H(−). Infect Immun 69(7):4447–4457. doi:10.1128/IAI.69.7.4447-4457.2001
CDC (1994) Outbreak of Acute Gastroenteritis Attributable to Escherichia coli Serotype O104:H21–Helena, Montana, 1994. http://www.cdc.gov/mmwr/preview/mmwrhtml/00038146.htm. Accessed 14 July 1995
CDC (2006) Update on Multi-State Outbreak of E. coli O157:H7 Infections From Fresh Spinach, October 6, 2006 http://www.cdc.gov/ecoli/2006/september/updates/100606.htm. Accessed 6 Oct 2006
CDC (2010) Investigation Update: Multistate Outbreak of Human E. coli O145 Infections Linked to Shredded Romaine Lettuce from a Single Processing Facility, http://www.cdc.gov/ecoli/2010/ecoli_o145/index.html?s_cid=ccu051010_006. Accessed Oct 4 2014
Cobbaut K, Berkvens D, Houf K, De Deken R, De Zutter L (2009) Escherichia coli O157 prevalence in different cattle farm types and identification of potential risk factors. J Food Prot 72(9):1848–1853
Cobbold RN, Hancock DD, Rice DH, Berg J, Stilborn R, Hovde CJ, Besser TE (2007) Rectoanal junction colonization of feedlot cattle by Escherichia coli O157:H7 and its association with supershedders and excretion dynamics. Appl Environ Microbiol 73(5):1563–1568. doi:10.1128/AEM.01742-06
Croxen MA, Law RJ, Scholz R, Keeney KM, Wlodarska M, Finlay BB (2013) Recent Advances in Understanding Enteric Pathogenic Escherichia coli. Clin Microbiol Rev 26(4):822–880. doi:10.1128/CMR.00022-13
Crump JA, Sulka AC, Langer AJ, Schaben C, Crielly AS, Gage R, Baysinger M, Moll M, Withers G, Toney DM, Hunter SB, Hoekstra RM, Wong SK, Griffin PM, Van Gilder TJ (2002) An outbreak of Escherichia coli O157:H7 infections among visitors to a dairy farm. N Engl J Med 347(8):555–560. doi:10.1056/NEJMoa020524
Davis TK, McKee R, Schnadower D, Tarr PI (2013) Treatment of Shiga Toxin-Producing Escherichia coli Infections. Infect Dis Clin North Am 27(3):577–597. doi:10.1016/j.idc.2013.05.010
De Schrijver K, Buvens G, Posse B, Van den Branden D, Oosterlynck O, De Zutter L, Eilers K, Pierard D, Dierick K, Van Damme-Lombaerts R, Lauwers C, Jacobs R (2008) Outbreak of verocytotoxin-producing E. coli O145 and O26 infections associated with the consumption of ice cream produced at a farm, Belgium, 2007. Euro Surveill 13(7):pii: 8041
Dundas S, Todd WT, Stewart AI, Murdoch PS, Chaudhuri AK, Hutchinson SJ (2001) The central Scotland Escherichia coli O157:H7 outbreak: risk factors for the hemolytic uremic syndrome and death among hospitalized patients. Clin Infect Dis 33(7):923–931. doi:10.1086/322598
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):2999–3003. doi:10.1073/pnas.060024897
Ethelberg S, Smith B, Torpdahl M, Lisby M, Boel J, Jensen T, Nielsen EM, Molbak K (2009) Outbreak of non-O157 Shiga toxin-producing Escherichia coli infection from consumption of beef sausage. Clin Infect Dis 48(8):e78–81. doi:10.1086/597502
Farfan MJ, Torres AG (2012) Molecular mechanisms that mediate colonization of Shiga toxin-producing Escherichia coli strains. Infect Immun 80(3):903–913. doi:10.1128/IAI.05907-11
Ferens WA, Hovde CJ (2011) Escherichia coli O157:H7: animal reservoir and sources of human infection. Foodborne Pathog Dis 8(4):465–487. doi:10.1089/fpd.2010.0673
Fremaux B, Prigent-Combaret C, Vernozy-Rozand C (2008) Long-term survival of Shiga toxin-producing Escherichia coli in cattle effluents and environment: an updated review. Vet Microbiol 132(1–2):1–18. doi:10.1016/j.vetmic.2008.05.015
Fukushima H, Hoshina K, Gomyoda M (1999) Long-term survival of shiga toxin-producing Escherichia coli O26, O111, and O157 in bovine feces. Appl Environ Microbiol 65(11):5177–5181
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
Griffin PM, Ostroff SM, Tauxe RV, Greene KD, Wells JG, Lewis JH, Blake PA (1988) Illnesses associated with Escherichia coli O157:H7 infections. A broad clinical spectrum. Ann Intern Med 109(9):705–712
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):7–14
Hurley BP, Thorpe CM, Acheson DW (2001) Shiga toxin translocation across intestinal epithelial cells is enhanced by neutrophil transmigration. Infect Immun 69(10):6148–6155. doi:10.1128/IAI.69.10.6148-6155.2001
Itoh Y, Sugita-Konishi Y, Kasuga F, Iwaki M, Hara-Kudo Y, Saito N, Noguchi Y, Konuma H, Kumagai S (1998) Enterohemorrhagic Escherichia coli O157:H7 present in radish sprouts. Appl Environ Microbiol 64(4):1532–1535
Jacob ME, Almes KM, Shi X, Sargeant JM, Nagaraja TG (2011) Escherichia coli O157:H7 genetic diversity in bovine fecal samples. J Food Prot 74(7):1186–1188. doi:10.4315/0362-028X.JFP-11-022
Janes ME, Kim KS, Johnson MG (2005) Transmission electron microscopy study of enterohemorrhagic Escherichia coli O157:H7 in apple tissue. J Food Prot 68(2):216–224
Karch H, Bielaszewska M (2001) Sorbitol-fermenting Shiga toxin-producing Escherichia coli O157:H(−) strains: epidemiology, phenotypic and molecular characteristics, and microbiological diagnosis. J Clin Microbiol 39(6):2043–2049. doi:10.1128/JCM.39.6.2043-2049.2001
Karch H, Russmann H, Schmidt H, Schwarzkopf A, Heesemann J (1995) Long-term shedding and clonal turnover of enterohemorrhagic Escherichia coli O157 in diarrheal diseases. J Clin Microbiol 33(6):1602–1605
Karch H, Bielaszewska M, Bitzan M, Schmidt H (1999) Epidemiology and diagnosis of Shiga toxin-producing Escherichia coli infections. Diagn Microbiol Infect Dis 34(3):229–243
Karch H, Tarr PI, Bielaszewska M (2005) Enterohaemorrhagic Escherichia coli in human medicine. Int J Med Microbiol 295(6–7):405–418. doi:10.1016/j.ijmm.2005.06.009
Karch H, Mellmann A, Bielaszewska M (2009) Epidemiology and pathogenesis of enterohaemorrhagic Escherichia coli. Berl Munch Tierarztl Wochenschr 122(11–12):417–424
Karch H, Denamur E, Dobrindt U, Finlay BB, Hengge R, Johannes L, Ron EZ, Tonjum T, Sansonetti PJ, Vicente M (2012) The enemy within us: lessons from the 2011 European Escherichia coli O104:H4 outbreak. EMBO Mol Med 4(9):841–848. doi:10.1002/emmm.201201662
Laidler MR, Tourdjman M, Buser GL, Hostetler T, Repp KK, Leman R, Samadpour M, Keene WE (2013) Escherichia coli O157:H7 infections associated with consumption of locally grown strawberries contaminated by deer. Clin Infect Dis 57(8):1129–1134. doi:10.1093/cid/cit468
Low JC, McKendrick IJ, McKechnie C, Fenlon D, Naylor SW, Currie C, Smith DG, Allison L, Gally DL (2005) Rectal carriage of enterohemorrhagic Escherichia coli O157 in slaughtered cattle. Appl Environ Microbiol 71(1):93–97. doi:10.1128/AEM.71.1.93-97.2005
Mahajan A, Currie CG, Mackie S, Tree J, McAteer S, McKendrick I, McNeilly TN, Roe A, La Ragione RM, Woodward MJ, Gally DL, Smith DG (2009) An investigation of the expression and adhesin function of H7 flagella in the interaction of Escherichia coli O157:H7 with bovine intestinal epithelium. Cell Microbiol 11 (1):121–137. doi:10.1111/j.1462-5822.2008.01244.x
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. doi:10.1073/pnas.1304978110
Maule A (2000) Survival of verocytotoxigenic Escherichia coli O157 in soil, water and on surfaces. Symp Ser Soc Appl Microbiol 29:71S–78S
Mellmann A, Bielaszewska M, Köck R, Friedrich AW, Fruth A, Middendorf B, Harmsen D, Schmidt MA, Karch H (2008) Analysis of collection of hemolytic uremic syndrome-associated enterohemorrhagic Escherichia coli. Emerg Infect Dis 14(8):1287–1290. doi:10.3201/eid1408.071082
Mellmann A, Bielaszewska M, Karch H (2009) Intrahost genome alterations in enterohemorrhagic Escherichia coli. Gastroenterology 136(6):1925–1938
Mellmann A, Harmsen D, Cummings CA, Zentz EB, Leopold SR, Rico A, Prior K, Szczepanowski R, Ji Y, Zhang W, McLaughlin SF, Henkhaus JK, Leopold B, Bielaszewska M, Prager R, Brzoska PM, Moore RL, Guenther S, Rothberg JM, Karch H (2011) Prospective genomic characterization of the German enterohemorrhagic Escherichia coli O104:H4 outbreak by rapid next generation sequencing technology. PloS ONE 6(7):e22751. doi:10.1371/journal.pone.0022751
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 Pathog 2(1):7. doi:10.1186/1757-4749-2-7
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):787–796
Moussay E, Stamm I, Taubert A, Baljer G, Menge C (2006) Escherichia coli Shiga toxin 1 enhances il-4 transcripts in bovine ileal intraepithelial lymphocytes. Vet Immunol Immunopathol 113(3–4):367–382. doi:10.1016/j.vetimm.2006.06.007
Müthing J, Schweppe CH, Karch H, Friedrich AW (2009) Shiga toxins, glycosphingolipid diversity, and endothelial cell injury. Thromb Haemost 101(2):252–264
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
Naylor SW, Gally DL, Low JC (2005a) Enterohaemorrhagic E. coli in veterinary medicine. Int J Med Microbiol 295(6–7):419–441
Naylor SW, Roe AJ, Nart P, Spears K, Smith DG, Low JC, Gally DL (2005b) Escherichia coli O157:H7 forms attaching and effacing lesions at the terminal rectum of cattle and colonization requires the LEE4 operon. Microbiology 151(Pt 8):2773–2781. doi:10.1099/mic.0.28060-0
Paton AW, Ratcliff RM, Doyle RM, Seymour-Murray J, Davos D, Lanser JA, Paton JC (1996) Molecular microbiological investigation of an outbreak of hemolytic-uremic syndrome caused by dry fermented sausage contaminated with Shiga-like toxin-producing Escherichia coli. J Clin Microbiol 34(7):1622–1627
Richardson SE, Karmali MA, Becker LE, Smith CR (1988) The histopathology of the hemolytic uremic syndrome associated with verocytotoxin-producing Escherichia coli infections. Hum Pathol 19(9):1102–1108
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):681–685. doi:10.1056/NEJM198303243081203
RKI (2011) Abschlussbericht zum EHEC/HUS-Ausbruch. Available via Robert-Koch-Institute. http://www.rki.de/DE/Content/InfAZ/E/EHEC/EHEC-Abschlussbericht.html. Accessed 9 Sept 2011
Rosales A, Hofer J, Zimmerhackl LB, Jungraithmayr TC, Riedl M, Giner T, Strasak A, Orth-Höller D, Würzner R, Karch H (2012) German-Austrian HUS Study Group. Clin Infect Dis 54(10):1413–1421. doi:10.1093/cid/cis196. Epub 2012 Mar 12
Sandvig K, Bergan J, Dyve AB, Skotland T, Torgersen ML (2010) Endocytosis and retrograde transport of Shiga toxin. Toxicon 56(7):1181–1185. doi:10.1016/j.toxicon.2009.11.021
Schaffzin JK, Coronado F, Dumas NB, Root TP, Halse TA, Schoonmaker-Bopp DJ, Lurie MM, Nicholas D, Gerzonich B, Johnson GS, Wallace BJ, Musser KA (2012) Public health approach to detection of non-O157 Shiga toxin-producing Escherichia coli: summary of two outbreaks and laboratory procedures. Epidemiol Infect 140(2):283–289. doi:10.1017/S0950268811000719
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. doi:10.1128/JCM.00860-12
Schimmer B, Nygard K, Eriksen HM, Lassen J, Lindstedt BA, Brandal LT, Kapperud G, Aavitsland P (2008) Outbreak of haemolytic uraemic syndrome in Norway caused by stx2-positive Escherichia coli O103:H25 traced to cured mutton sausages. BMC Infect Dis 8:41. doi:10.1186/1471-2334-8-41
Seo KH, Frank JF (1999) Attachment of Escherichia coli O157:H7 to lettuce leaf surface and bacterial viability in response to chlorine treatment as demonstrated by using confocal scanning laser microscopy. J Food Prot 62(1):3–9
Söderström 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):339–349. doi:10.1089/fpd.2007.0065
Sodha SV, Lynch M, Wannemuehler K, Leeper M, Malavet M, Schaffzin J, Chen T, Langer A, Glenshaw M, Hoefer D, Dumas N, Lind L, Iwamoto M, Ayers T, Nguyen T, Biggerstaff M, Olson C, Sheth A, Braden C (2011) Multistate outbreak of Escherichia coli O157:H7 infections associated with a national fast-food chain, 2006: a study incorporating epidemiological and food source traceback results. Epidemiol Infect 139(2):309–316. doi:10.1017/S0950268810000920
Solomon EB, Yaron S, Matthews KR (2002) Transmission of Escherichia coli O157:H7 from contaminated manure and irrigation water to lettuce plant tissue and its subsequent internalization. Appl Environ Microbiol 68(1):397–400
Tarr PI, Gordon CA, Chandler WL (2005) Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet 365(9464):1073–1086. doi:10.1016/S0140-6736(05)71144-2
Teunis P, Takumi K, Shinagawa K (2004) Dose response for infection by Escherichia coli O157:H7 from outbreak data. Risk Anal 24(2):401–407. doi:10.1111/j.0272-4332.2004.00441.x
Thurston-Enriquez JA, Gilley JE, Eghball B (2005) Microbial quality of runoff following land application of cattle manure and swine slurry. J Water Health 3(2):157–171
Tuttle J, Gomez T, Doyle MP, Wells JG, Zhao T, Tauxe RV, Griffin PM (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(2):185–192
Wahl E, Vold L, Lindstedt BA, Bruheim T, Afset JE (2011) Investigation of an Escherichia coli O145 outbreak in a child day-care centre–extensive sampling and characterization of eae- and stx1-positive E. coli yields epidemiological and socioeconomic insight. BMC Infect Dis 11:238. doi:10.1186/1471-2334-11-238
Wang G, Doyle MP (1998) Survival of enterohemorrhagic Escherichia coli O157:H7 in water. J Food Prot 61(6):662–667
Watanabe H, Wada A, Inagaki Y, Itoh K, Tamura K (1996) Outbreaks of enterohaemorrhagic Escherichia coli O157:H7 infection by two different genotype strains in Japan, 1996. Lancet 348(9030):831–832
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):512–520
Werber D, Fruth A, Liesegang A, Littmann M, Buchholz U, Prager R, Karch H, Breuer T, Tschape H, Ammon A (2002) A multistate outbreak of Shiga toxin-producing Escherichia coli O26:H11 infections in Germany, detected by molecular subtyping surveillance. J Infect Dis 186(3):419–422. doi:10.1086/341457
Wong CS, Jelacic S, Habeeb RL, Watkins SL, Tarr PI (2000) The risk of the hemolytic-uremic syndrome after antibiotic treatment of Escherichia coli O157:H7 infections. N Engl J Med 342(26):1930–1936. doi:10.1056/NEJM200006293422601
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Karch, H., Leopold, S., Kossow, A., Mellmann, A., Köck, R., Bauwens, A. (2015). Enterohemorrhagic E. coli (EHEC): Environmental-Vehicle-Human Interface. In: Sing, A. (eds) Zoonoses - Infections Affecting Humans and Animals. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9457-2_9
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