Six Serogroups of Non-O157 Shiga toxin-producing E. coli: Comparison
Please note this is a comparison between Version 3 by Catherine Yang and Version 2 by RASHAD R. AL-HINDI.

Non-O157 Shiga toxin-producing Escherichia coli (STEC) are emerging serogroups that often result in diseases ranging from diarrhea to severe hemorrhagic colitis in humans. The most common non-O157 STEC are O26, O45, O103, O111, O121, and O145. These serogroups are known by the name “big six” because they cause severe illness and death in humans and the United States Department of Agriculture declared these serogroups as food contaminants.

  • Escherichia coli
  • non-O157
  • foodborne

1. E. coli Serogroup O26

Serogroup O26 E. coli possesses both EPEC and STEC strains. STEC O26 is the most common non-O157 serogroup related to HUS and HC in humans [71][1], while EPEC O26 is responsible for less-severe enteritis [72][2]. The human isolates of E. coli O26 mostly express the flagellar (H) antigen (e.g., H11) or are nonmotile (NM/H-) if the antigen is not encoded by their genome. Nevertheless, based on the molecular assessment, it has been proven that the H-serogroup is also classified under the H11 clonal complex [73][3]. EPEC O26:H11 does not comprise the EAF plasmid and is hence categorized as aEPEC [74][4]. However, classifying O26 serogroup into pathogroups, such as STEC and aEPEC, may be misleading, since aEPEC could be STEC which lacks stx and the reverse [75][5].
O26 serogroup has been isolated from both healthy as well as diarrheic animals [76,77,78][6][7][8]. Even though myriad studies on O26 have been performed, most of these investigations have been inadequate, with limited sample sizes, or have centered on STEC O26 rather than non-STEC O26 serotypes. Besides, most studies have been conducted on cattle [79[9][10],80], and research on O26 in sheep is scarce [77,81][7][11]. Among the STEC serogroups, O26 is the second most reported serogroup in several countries, including Ireland, Italy, France, and Denmark, and clinical O26 cases presently exceed cases caused by O157 [82][12]. Non-O157 infections were found to be clinically relevant in pediatric patients, in whom the disease severity is comparable to that of O157 [83,84][13][14]. Current outbreaks of eae and stx2 positive O26:H11 serogroup have caused severe HUS infections in young individuals, particularly in some countries, including France, Italy, and Romania [85,86,87,88][15][16][17][18]. To date, in European countries, the O26:H11 serogroup is accountable for more HUS infections than O157 STEC serogroup and is of emerging importance [82][12].

2. E. coli Serogroup O45

STEC O45 serogroup is one of the top six non-O157 STEC that have been recognized as a cause of sporadic BD in humans [89][19]. During the first outbreak of STEC O45 in 2005, 52 inmates in New York City became ill with diarrhea or BD, probably because they had been exposed to an ill food worker [90][20]. In addition to these outbreaks, two other outbreaks caused by O45:H2 serogroup have occurred in which 18 illnesses were reported, and contaminated smoked goat and game meat was implicated as the source of contamination in both outbreaks [91][21]. In a different study, two O145:H28 strains (RM13716 and RM13714) caused ice cream and lettuce-associated outbreaks in Belgium and US, respectively. These strains shared a common ancestor with 5 different STEC O157:H7 strains, including the Japanese E. coli Sakai strain [92,93][22][23].

3. E. coli Serogroup O103

Among the other STEC serogroups of E. coli, O103 has caused a few outbreaks worldwide. STEC O103:H2 is one of the most prevalent STEC serotypes isolated from humans in Europe [94][24]. E. coli O103:H11 has been reported in Japan and Canada as a sporadic cause of human infections in addition to E. coli O103:H2 [95][25].
An E. coli outbreak caused by O103 occurred in Norway in the spring of 2006. Among the 17 cases identified, 10 children experienced HUS and one died. The outbreak was traced to a cured sheep sausage product from one brand [96][26]. Stx-producing E. coli O103 H2 was first isolated in Brazil from sheep in 2004 and re-emerged in 2005 [97][27]. During the period 1997–2000, STEC E. coli O103 H2/H (-) ranked third among the most repeatedly isolated EHEC types in Germany [98][28]. The pathogen has also been reported in sporadic outbreaks at nursery facilities in Japan between 2010 and 2013 [99][29]. Recent outbreaks of E. coli O103 have been reported in Germany following school-led trips to Austria [100][30]. In this case, raw cow’s milk was implicated as the source of the infection, and international collaboration played an essential role in preventing outbreaks and responding appropriately.

4. E. coli Serogroup O111

Serogroup O111 causes enteropathogenic and enterohemorrhagic sickness in humans [32][31]. EPEC O111 serogroup is the leading cause of diarrhea in infants, predominantly in developing nations. Among the non-O157 E. coli serovars, stx-producing EHEC O111 is one of the frequent causes of BD and HUS across the world [101,102][32][33]. Many outbreaks have been correlated to this pathogen [89,101][19][32].
Research on the O111 serogroup that has originated from different sources indicated that there is a substantial phenotypic and genetic diversity among this E. coli O serogroup. Even though motile O111 serotypes isolated from children’s diarrhea usually expressed flagella antigens (H2, H12, or H21), in several cases NM isolates have been encountered. Serogroup O111:H and O111:H2 characteristically carry the EAF plasmid that facilitates localized attachment (LA) of bacteria to cultured cells which is a feature of the classic EPEC serogroups.
The O111 clone was the first STEC serogroup of E. coli that cause gastroenteritis outbreaks in humans [103][34]. The flagellar type O111:H12, O111:H8, O111:H2, and the non-flagellated O111: NM has been recognized as pathogenic clones. The O111 antigen has been classically linked to the enteropathogenic serogroup and now has also been recognized as an O antigen of EHEC and EAEC E. coli [32][31]. Due to the lack of facilities for proper diagnosis of O111 serotype of E. coli, the burden of the public health illness caused by these clones is underestimated. However, several O111 serotypes have been reported as they caused serious enteric illness in humans, including 28% of 50 outbreaks of child diarrhea in the US from 1934 to 1987 [104][35], 33% of infantile diarrhea cases in Brazil [105][36], a huge outbreak affecting >700 infected individuals in Finland [106][37], and currently, documented HUS outbreaks in Italy [107][38] and Australia [108][39].

5. E. coli Serogroup O121

Stx-producing O121 E. coli serogroups have been mainly isolated from individuals who developed HUS or HC, and consequently they are categorized as EHEC [109,110,111][40][41][42]. Moreover, these serogroups having virulence factors like those of enteroinvasive Shigella and E. coli, have resulted in shigellosis-like sicknesses [112][43]. In 1999, an HUS outbreak caused by O121:H19 serogroup was reported and the source of the infection was related to the lake in Connecticut [109][40]. Tarr et al. identified 24 isolates of O121:H19 serogroup and H- (NM) variants using multilocus sequencing and enzyme electrophoresis and the results indicated that the isolates were determined as a single bacterial clone. These isolates comprised a virulence gene that is specific for EHEC clones; nevertheless, the sequence analysis indicated that the O121:H19 clone was not classified under either EPEC E. coli or classical EHEC groups. Tarr et al. indicated that O121:H19 serogroup gained virulence genes and denotes a typical EHEC clone [113][44].

6. E. coli Serogroup O145

O145 is a crucial cause of HUS and HC worldwide. Ruminants are the main reservoir of this serogroup, which carry the agent in their hind GIT system and shed it in the manure. Fecal matter is the major source of carcass and hide contamination which leads to O145-associated foodborne infections in humans. Several outbreaks have been reported associated with O145 infection in the US and other countries, including Argentina [114][45], Germany [115][46], and Belgium [116][47]. In 1999, two O145-associated illnesses were reported in a daycare center in Minnesota, US [22][48]. This serogroup has also been reported as the cause of a waterborne infection in humans in 2005, in Oregon, US [117][49], and in 2010, the consumption of contaminated romaine lettuce resulted in a multistate outbreak, causing 45% hospitalization, associated with HUS in 10% of cases [118][50].

References

  1. Carbonari, C.C.; Miliwebsky, E.S.; Zolezzi, G.; Deza, N.L.; Fittipaldi, N.; Manfredi, E.; Baschkier, A.; D’Astek, B.A.; Melano, R.G.; Schesi, C. The Importance of Shiga Toxin-Producing Escherichia coli O145: NM /H28 Infections in Argentina, 1998–2020. Microorganisms 2022, 10, 582.
  2. Bielaszewska, M.; Zhang, W.; Tarr, P.I.; Sonntag, A.-K.; Karch, H. Molecular profiling and phenotype analysis of Escherichia coli O26: H11 and O26: NM: Secular and geographic consistency of enterohemorrhagic and enteropathogenic isolates. J. Clin. Microbiol. 2005, 43, 4225–4228.
  3. Zhang, W.-L.; Bielaszewska, M.; Bockemühl, J.; Schmidt, H.; Scheutz, F.; Karch, H. Molecular analysis of H antigens reveals that human diarrheagenic Escherichia coli O26 strains that carry the eae gene belong to the H11 clonal complex. J. Clin. Microbiol. 2000, 38, 2989–2993.
  4. Jenkins, C.; Evans, J.; Chart, H.; Willshaw, G.; Frankel, G. Escherichia coli serogroup O26–a new look at an old adversary. J. Appl. Microbiol. 2008, 104, 14–25.
  5. Anjum, M.F.; Lucchini, S.; Thompson, A.; Hinton, J.C.; Woodward, M.J. Comparative genomic indexing reveals the phylogenomics of Escherichia coli pathogens. Infect. Immun. 2003, 71, 4674–4683.
  6. Cid, D.; Ruiz-Santa-Quiteria, J.; Marın, I.; Sanz, R.; Orden, J.; Amils, R.; De La Fuente, R. Association between intimin (eae) and EspB gene subtypes in attaching and effacing Escherichia coli strains isolated from diarrhoeic lambs and goat kids. Microbiology 2001, 147, 2341–2353.
  7. Fröhlicher, E.; Krause, G.; Zweifel, C.; Beutin, L.; Stephan, R. Characterization of attaching and effacing Escherichia coli (AEEC) isolated from pigs and sheep. BMC Microbiol. 2008, 8, 144.
  8. Krause, G.; Zimmermann, S.; Beutin, L. Investigation of domestic animals and pets as a reservoir for intimin-(eae) gene positive Escherichia coli types. Vet. Microbiol. 2005, 106, 87–95.
  9. Pearce, M.; Evans, J.; McKendrick, I.; Smith, A.; Knight, H.; Mellor, D.; Woolhouse, M.; Gunn, G.; Low, J. Prevalence and virulence factors of Escherichia coli serogroups O26, O103, O111, and O145 shed by cattle in Scotland. Appl. Environ. Microbiol. 2006, 72, 653–659.
  10. Blanco, M.; Schumacher, S.; Tasara, T.; Zweifel, C.; Blanco, J.E.; Dahbi, G.; Blanco, J.; Stephan, R. Serotypes, intimin variants and other virulence factors of eae positive Escherichia coli strains isolated from healthy cattle in Switzerland. Identification of a new intimin variant gene (eae-η2). BMC Microbiol. 2005, 5, 23.
  11. Evans, J.; Knight, H.; McKendrick, I.J.; Stevenson, H.; Barbudo, A.V.; Gunn, G.J.; Low, J.C. Prevalence of Escherichia coli O157: H7 and serogroups O26, O103, O111 and O145 in sheep presented for slaughter in Scotland. J. Med. Microbiol. 2011, 60, 653–660.
  12. Hoyle, D.V.; Keith, M.; Williamson, H.; Macleod, K.; Mathie, H.; Handel, I.; Currie, C.; Holmes, A.; Allison, L.; McLean, R. Prevalence and epidemiology of non-O157 Escherichia coli serogroups O26, O103, O111, and O145 and Shiga toxin gene carriage in Scottish cattle, 2014–2015. Appl. Environ. Microbiol. 2021, 87, e03142-03120.
  13. Hermos, C.R.; Janineh, M.; Han, L.L.; McAdam, A.J. Shiga toxin-producing Escherichia coli in children: Diagnosis and clinical manifestations of O157: H7 and non-O157: H7 infection. J. Clin. Microbiol. 2011, 49, 955–959.
  14. Pollock, K.G.; Bhojani, S.; Beattie, T.J.; Allison, L.; Hanson, M.; Locking, M.E.; Cowden, J.M. Highly virulent Escherichia coli O26, Scotland. Emerg. Infect. Dis. 2011, 17, 1777.
  15. Bruyand, M.; Mariani-Kurkdjian, P.; Le Hello, S.; King, L.-A.; Van Cauteren, D.; Lefevre, S.; Gouali, M.; Jourdan-da Silva, N.; Mailles, A.; Donguy, M.-P. Paediatric haemolytic uraemic syndrome related to Shiga toxin-producing Escherichia coli, an overview of 10 years of surveillance in France, 2007 to 2016. Eurosurveillance 2019, 24, 1800068.
  16. Jones, G.; Lefèvre, S.; Donguy, M.-P.; Nisavanh, A.; Terpant, G.; Fougère, E.; Vaissière, E.; Guinard, A.; Mailles, A.; de Valk, H. Outbreak of Shiga toxin-producing Escherichia coli (STEC) O26 paediatric haemolytic uraemic syndrome (HUS) cases associated with the consumption of soft raw cow’s milk cheeses, France, March to May 2019. Eurosurveillance 2019, 24, 1900305.
  17. Severi, E.; Vial, F.; Peron, E.; Mardh, O.; Niskanen, T.; Takkinen, J. Community-wide outbreaks of haemolytic uraemic syndrome associated with Shiga toxin-producing Escherichia coli O26 in Italy and Romania: A new challenge for the European Union. Eurosurveillance 2016, 21, 30420.
  18. Loconsole, D.; Giordano, M.; Centrone, F.; Accogli, M.; Casulli, D.; De Robertis, A.L.; Morea, A.; Quarto, M.; Parisi, A.; Scavia, G. Epidemiology of Shiga toxin-producing Escherichia coli infections in Southern Italy after implementation of symptom-based surveillance of bloody diarrhea in the pediatric population. Int. J. Environ. Res. Public Health 2020, 17, 5137.
  19. Brooks, J.T.; Bergmire-Sweat, D.; Kennedy, M.; Hendricks, K.; Garcia, M.; Marengo, L.; Wells, J.; Ying, M.; Bibb, W.; Griffin, P.M. Outbreak of Shiga toxin—Producing Escherichia coli O111: H8 infections among attendees of a high school cheerleading camp. Clin. Infect. Dis. 2004, 38, 190–198.
  20. Schaffzin, J.; Coronado, F.; Dumas, N.; Root, T.; Halse, T.; Schoonmaker-Bopp, D.; Lurie, M.; Nicholas, D.; Gerzonich, B.; Johnson, G. Public health approach to detection of non-O157 Shiga toxin-producing Escherichia coli: Summary of two outbreaks and laboratory procedures. Epidemiol. Infect. 2012, 140, 283–289.
  21. Luna-Gierke, R.; Griffin, P.; Gould, L.; Herman, K.; Bopp, C.; Strockbine, N.; Mody, R. Outbreaks of non-O157 Shiga toxin-producing Escherichia coli infection: USA. Epidemiol. Infect. 2014, 142, 2270–2280.
  22. Cooper, K.K.; Mandrell, R.E.; Louie, J.W.; Korlach, J.; Clark, T.A.; Parker, C.T.; Huynh, S.; Chain, P.S.; Ahmed, S.; Carter, M.Q. Comparative genomics of enterohemorrhagic Escherichia coli O145: H28 demonstrates a common evolutionary lineage with Escherichia coli O157: H7. BMC Genom. 2014, 15, 17.
  23. Michino, H.; Araki, K.; Minami, S.; Takaya, S.; Sakai, N.; Miyazaki, M.; Ono, A.; Yanagawa, H. Massive outbreak of Escherichia coli O157: H7 infection in schoolchildren in Sakai City, Japan, associated with consumption of white radish sprouts. Am. J. Epidemiol. 1999, 150, 787–796.
  24. Sekse, C.; Sunde, M.; Hopp, P.; Bruheim, T.; Cudjoe, K.S.; Kvitle, B.; Urdahl, A.M. Occurrence of potentially human-pathogenic Escherichia coli O103 in Norwegian sheep. Appl. Environ. Microbiol. 2013, 79, 7502–7509.
  25. Spika, J.; Khakhria, R.; Michel, P.; Milley, D.; Wilson, J.; Waters, J. Shiga toxin-producing Escherichia coli infections in Canada. Escherichia coli O 1998, 157, 23–29.
  26. Sekse, C.; O’Sullivan, K.; Granum, P.E.; Rørvik, L.M.; Wasteson, Y.; Jørgensen, H.J. An outbreak of Escherichia coli O103: H25—Bacteriological investigations and genotyping of isolates from food. Int. J. Food Microbiol. 2009, 133, 259–264.
  27. Martins, F.H.; Guth, B.E.; Piazza, R.M.; Blanco, J.; Pelayo, J.S. First description of a Shiga toxin-producing Escherichia coli O103: H2 strain isolated from sheep in Brazil. J. Infect. Dev. Ctries. 2014, 8, 126–128.
  28. Miko, A.; Pries, K.; Haby, S.; Steege, K.; Albrecht, N.; Krause, G.; Beutin, L. Assessment of Shiga toxin-producing Escherichia coli isolates from wildlife meat as potential pathogens for humans. Appl. Environ. Microbiol. 2009, 75, 6462–6470.
  29. Kanayama, A.; Yahata, Y.; Arima, Y.; Takahashi, T.; Saitoh, T.; Kanou, K.; Kawabata, K.; Sunagawa, T.; Matsui, T.; Oishi, K. Enterohemorrhagic Escherichia coli outbreaks related to childcare facilities in Japan, 2010–2013. BMC Infect. Dis. 2015, 15, 539.
  30. Mylius, M.; Dreesman, J.; Pulz, M.; Pallasch, G.; Beyrer, K.; Claußen, K.; Allerberger, F.; Fruth, A.; Lang, C.; Prager, R. Shiga toxin-producing Escherichia coli O103: H2 outbreak in Germany after school trip to Austria due to raw cow milk, 2017–The important role of international collaboration for outbreak investigations. Int. J. Med. Microbiol. 2018, 308, 539–544.
  31. Nataro, J.P.; Kaper, J.B. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 1998, 11, 142–201.
  32. Jeon, B.-W.; Jeong, J.-M.; Won, G.-Y.; Park, H.; Eo, S.-K.; Kang, H.-Y.; Hur, J.; Lee, J.H. Prevalence and characteristics of Escherichia coli O26 and O111 from cattle in Korea. Int. J. Food Microbiol. 2006, 110, 123–126.
  33. Kato, K.; Shimoura, R.; Nashimura, K.; Yoshifuzi, K.; Shiroshita, K.; Sakurai, N.; Kodama, H.; Kuramoto, S. Outbreak of enterohemorrhagic Escherichia coli O111 among high school participants in excursion to Korea. Jpn. J. Infect. Dis. 2005, 58, 332.
  34. Kauffmann, F.; Dupont, A. Escherichia Strains from Infantile Epidemic Gastro-Enterltis. Acta Pathol. et Microbiol. Scand. 1950, 27, 552–564.
  35. Moyenuddin, M.; Wachsmuth, I.; Moseley, S.; Bopp, C.; Blake, P. Serotype, antimicrobial resistance, and adherence properties of Escherichia coli strains associated with outbreaks of diarrheal illness in children in the United States. J. Clin. Microbiol. 1989, 27, 2234–2239.
  36. Regua, A.H.; Bravo, V.; Leal, M.d.C.; Lobo Leite, M. Epidemiological survey of the enteropathogenic Escherichia coli isolated from children with diarrhoea. J. Trop. Pediatr. 1990, 36, 176–179.
  37. Viljanen, M.; Peltola, T.; Kuistila, M.; Huovinen, P.; Junnila, S.; Olkkonen, L.; Järvinen, H. Outbreak of diarrhoea due to Escherichia coli 0111: B4 in schoolchildren and adults: Association of Vi antigen-like reactivity. Lancet 1990, 336, 831–834.
  38. Caprioli, A.; Luzzi, I.; Rosmini, F.; Resti, C.; Edefonti, A.; Perfumo, F.; Farina, C.; Goglio, A.; Gianviti, A.; Rizzoni, G. Communitywide outbreak of hemolytic-uremic syndrome associated with non-O157 verocytotoxin-producing Escherichia coli. J. Infect. Dis. 1994, 169, 208–211.
  39. Paton, A.W.; Ratcliff, R.M.; Doyle, R.M.; Seymour-Murray, J.; Davos, D.; Lanser, J.A.; Paton, J.C. 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. 1996, 34, 1622–1627.
  40. McCarthy, T.A.; Barrett, N.L.; Hadler, J.L.; Salsbury, B.; Howard, R.T.; Dingman, D.W.; Brinkman, C.D.; Bibb, W.F.; Cartter, M.L. Hemolytic-uremic syndrome and Escherichia coli O121 at a lake in Connecticut, 1999. Pediatrics 2001, 108, e59.
  41. Stock, K.J.; Scott, M.A.; Davis, S.F.; Pierson Iii, R.N.; Dummer, J.S. Hemorrhagic colitis due to a novel Escherichia coli serotype (O121: H19) in a transplant patient. Transpl. Int. 2001, 14, 44–47.
  42. Cornu, G.; Proesmans, W.; Dediste, A.; Jacobs, F.; Van De Walle, J.; Mertens, A.; Ramet, J.; Lauwers, S. Hemolytic uremic syndrome in Belgium: Incidence and association with verocytotoxin-producing Escherichia coli infection. Clin. Microbiol. Infect. Off. Publ. Eur. Soc. Clin. Microbiol. Infect. Dis. 1999, 5, 16–22.
  43. Hiruta, N.; Himori, M.; Habutsu, M.; Okamura, N.; Ogawa, M.; Matsushita, S.; Kudoh, Y. Enteroinvasive Escherichia coli O121: H-isolated from travellers’ diarrhea. Kansenshogaku Zasshi. J. Jpn. Assoc. Infect. Dis. 1991, 65, 537–539.
  44. Tarr, C.L.; Large, T.M.; Moeller, C.L.; Lacher, D.W.; Tarr, P.I.; Acheson, D.W.; Whittam, T.S. Molecular characterization of a serotype O121: H19 clone, a distinct Shiga toxin-producing clone of pathogenic Escherichia coli. Infect. Immun. 2002, 70, 6853–6859.
  45. Rivero, M.A.; Passucci, J.A.; Rodriguez, E.M.; Parma, A.E. Role and clinical course of verotoxigenic Escherichia coli infections in childhood acute diarrhoea in Argentina. J. Med. Microbiol. 2010, 59, 345–352.
  46. Beutin, L.; Zimmermann, S.; Gleier, K. Human infections with Shiga toxin-producing Escherichia coli other than serogroup O157 in Germany. Emerg. Infect. Dis. 1998, 4, 635.
  47. De Schrijver, K.; Buvens, G.; Possé, B.; Van den Branden, D.; Oosterlynck, O.; De Zutter, L.; Eilers, K.; Piérard, D.; Dierick, K.; Van Damme-Lombaerts, R. Outbreak of verocytotoxin-producing E. coli O145 and O26 infections associated with the consumption of ice cream produced at a farm, Belgium, 2007. Eurosurveillance 2008, 13, 9–10.
  48. Luna, R.; Mody, R.; Griffin, P. Non-O157 Shiga toxin-producing E. coli (STEC) outbreaks, United States. Dep. Health Hum. Serv. CfDCaPC Ed. Cent. Dis. Control Prev. Atlanta 2010. Available online: http://blogs.cdc.gov/publichealthmatters/files/2010/05/nono157stec_obs_052110 (accessed on 15 November 2011).
  49. Yoder, J.; Roberts, V.; Craun, G.F.; Hill, V.; Hicks, L.A.; Alexander, N.T.; Radke, V.; Calderon, R.L.; Hlavsa, M.C.; Beach, M.J. Surveillance for waterborne disease and outbreaks associated with drinking water and water not intended for drinking—United States, 2005–2006. Morb. Mortal. Wkly. Report. Surveill. Summ. 2008, 57, 39–62.
  50. Taylor, E.; Nguyen, T.; Machesky, K.; Koch, E.; Sotir, M.; Bohm, S.; Folster, J.; Bokanyi, R.; Kupper, A.; Bidol, S. Multistate outbreak of Escherichia coli O145 infections associated with romaine lettuce consumption, 2010. J. Food Prot. 2013, 76, 939–944.
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