Skip to main content
Log in

Non-O157:H7 Shiga toxin (verocytotoxin)-producing Escherichia coli strains: epidemiological significance and microbiological diagnosis

  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Shiga toxin (Stx)-producing Escherichia coli (STEC) are important causes of diarrhoea and the haemolytic uremic syndrome (HUS). The most common STEC serotype implicated worldwide is E. coli O157:H7 that is diagnosed using procedures based on its typical phenotypic feature, the lack of sorbitol fermentation. In addition to E. coli O157:H7, a variety of non-O157:H7 STEC strains that usually ferment sorbitol and are thus missed by using the diagnostic protocol for E.coli O157:H7 have been isolated from patients. Among these sorbitol-fermenting (SF) non-O157:H7 STEC, SF E. coli O157:H and non-O157 STEC strains of serogroups O26, O103, O111 and O145 have emerged as significant causes of HUS and diarrhoea in continental Europe and have been associated with human disease in other parts of the world. Microbiological diagnosis of non-O157:H7 STEC strains is difficult due to their serotype diversity and the absence of a simple biochemical property that distinguishes such strains from the physiological intestinal microflora. Screening for non-O157:H7 STEC and their isolation from stools is presently based on the detection of Stx production or stx genes that are common characteristics of such strains. Molecular subtyping of the most frequent non-O157 STEC demonstrated that strains of serogroups O26, O103 and O111 belong to their own clonal lineages and show unique virulence profiles. SF STEC O157:H strains that have been isolated mostly in Central Europe represent a new clone within E. coli O157 serogroup which has its own typical combination of virulence factors.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Acheson, D.W.K. & Keusch, G.T. 1995 Which Shiga toxin-producing types of E. coli are important? American Society for Microbiology (ASM) News 62, 302–306.

    Google Scholar 

  • Acheson, D.W.K., Wolf, L.E. & Park, C.H. 1997 Escherichia coli and the hemolytic uremic syndrome. New England Journal of Medicine 336, 515.

    Article  CAS  Google Scholar 

  • Allerberger, F., Rossboth, D., Dierich, M.P., Aleksic, S., Schmidt, H. & Karch, H. 1996 Prevalence and clinical manifestation of Shigalike toxin-producing Escherichia coli infections in Austrian children. European Journal of Clinical Microbiology and Infectious Diseases 15, 545–550.

    Article  CAS  Google Scholar 

  • Ammon, A., Peterson, L. R. & Karch, H. 1999 A large outbreak of hemolytic uremic syndrome caused by an unusual sorbitol-fermenting strain E. coli O157:H¯. Journal of Infectious Diseases 179, 1274–1277.

    Article  CAS  Google Scholar 

  • Bégué, R.E., Neill, M.A., Papa, E.F., Dennehy, P.H. 1994 A prospective study of Shiga-like toxin-associated diarrhoea in a pediatric population. Journal of Pediatrics and Gastroenterology Nutrition 19, 164-169.

    Article  Google Scholar 

  • Beutin, L., Montenegro, M.A., Orskov, I., Orskov, F., Prada, J., Zimmermann, S. & Stephan, R. 1989 Close association of verotoxin (Shiga-like toxin) production with enterohemolysin production in strains of Escherichia coli. Journal of Clinical Microbiology 27, 2559–2564.

    CAS  Google Scholar 

  • Bielaszewska, M., Janda, J., Blahova, K., Sramkova, L., Havlik, J. & Potuznik, V. 1994 Verocytotoxin-producing Escherichia coli in children with hemolytic uremic syndrome and diarrhea in the Czech Republic. In Recent Advances in Verocytotoxin-Producing Escherichia coli Infections; Proceedings of the 2nd International Symposium and Workshop on Verocytotoxin (Shiga-like toxin)-producing Escherichia coli infections, Bergamo, Italy, 27-30 June 1994, eds. Karmali, M.A. & Goglio, A.G. pp. 37–40. Amsterdam: Elsevier Science B.V. ISBN 0-444-81840-5.

    Google Scholar 

  • Bielaszewska, M., Janda, J., Blahova, K., Feber, J., Potuznik, V. & Souckova, A. 1996 Verocytotoxin-producing Escherichia coli in children with hemolytic uremic syndrome in the Czech Republic. Clinical Nephrology 46, 42–44.

    CAS  Google Scholar 

  • Bielaszewska, M., Schmidt, H., Karmali, M.A., Khakhria, R., Janda, J., Blahova, K. & Karch, H. 1998 Isolation and characterization of sorbitol-fermenting Shiga toxin-producing Escherichia coli O157:H) strains in the Czech Republic. Journal of Clinical Microbiology 36, 2135–2137.

    CAS  Google Scholar 

  • Bitzan, M., Moebius, E., Ludwig, K., Muller Wiefel, D.E., Heesemann, J. & Karch, H. 1991 High incidence of serum antibodies to Escherichia coli O157 lipopolysaccharide in children with hemolytic-uremic syndrome. Journal of Pediatrics 119, 380–385.

    Article  CAS  Google Scholar 

  • Blanco, J.E., Blanco, M., Molinero, M.E., Peiro, E., Mora, A. & Blanco, J. 1996 Brote de gastroenteritis asociado con un Escherichia coli verotoxigenico O111:H-VT1+ eae+. Alimentaria 275, 109–113.

    Google Scholar 

  • Bockemühl, J. & Karch, H. 1996 Zur aktuellen Bedeutung der enterohämorrhagischen Escherichia coli (EHEC) in Deutschland (1994–1995). Bundesgesundheitsblatt 8, 290–296.

    Google Scholar 

  • Bockemühl, J., Karch, H. & Tschäpe, H. 1997 Infektionen des Menschen durch enterohämorrhagische Escherichia coli (EHEC) in Deutschland, 1996. Bundesgesundheitsblatt 6, 194–197.

    Google Scholar 

  • Bockemühl, J., Karch, H. & Tschäpe, H. 1998 Zur Situation der Infektionen des Menschen durch enterohämorrhagische Escherichia coli (EHEC) in Deutschland, 1997. Bundesgesundheitsblatt October (Suppl.), 2–5.

  • Bokete, T.N., O'Callahan, C.M., Clausen, C.R., Tang, N.M., Tran, N., Moseley, S.L., Fritsche, T.R. & Tarr, P.I. 1993 Shiga-like toxin-producing Escherichia coli in Seattle children: a prospective study. Gastroenterology 105, 1724–1731.

    CAS  Google Scholar 

  • Boudaillez, B., Berquin, P., Mariani-Kurkdjian, P., Bef, D., Cuvelier, B., Capek, I., Tribout, B., Bingen, E. & Piussan, C. 1996 Possible person-to-person transmission of Escherichia coli O111-associated hemolytic uremic syndrome. Pediatric Nephrology 11, 36-39.

    Article  Google Scholar 

  • Burnens, A.P., Boss, P., Orskov, F., Orskov, I., Schaad, U.B., Muller, F., Heinzle, R. & Nicolet, J. 1992 Occurence and phenotypic properties of verotoxin-producing Escherichia coli in sporadic cases of gastroenteritis. European Journal of Clinical Microbiology and Infectious Diseases 11, 631–634.

    Article  CAS  Google Scholar 

  • Caprioli, A., Luzzi, I., Rosmini, F., Resti, C., Edefonti, A., Perfumo, F., Farina, C., Goglio, A., Gianviti, A. & Rizzoni, G. 1994. Community-wide outbreak of hemolytic-uremic syndrome associated with non-O157 verocytotoxin-producing Escherichia coli. Journal of Infectious Diseases 169, 208-211.

    CAS  Google Scholar 

  • Caprioli, A., Tozzi, A.E., Rizzoni, G. & Karch, H. 1997 Non-O157 Shiga toxin-producing Escherichia coli infections in Europe. Emerging Infectious Diseases 3, 578–579.

    CAS  Google Scholar 

  • Caprioli, A. & Tozzi, A.E. 1998 Epidemiology of Shiga toxin-producing Escherichia coli infections in continental Europe. In Escherichia coli O157:H7 and Other Shiga Toxin-Producing E. coli Strains, eds. Kaper, J.B. & O'Brien, A.D. pp. 38-48. Washington, DC: American Society for Microbiology. ISBN 1-55581-129-9.

    Google Scholar 

  • Cebula, T.A., Payne, W.L. & Feng, P. 1995 Simultaneous identification of strains of Escherichia coli serotype O157:H7 and their Shiga-like toxin type by mismatch amplification mutation assay-multiplex PCR. Journal of Clinical Microbiology 33, 248–250.

    CAS  Google Scholar 

  • Centers for Disease Control and Prevention. 1995 Outbreak of acute gastroenteritis attributable to Escherichia coli serotype O104:H21 -Helena, Montana, 1994. Morbidity and Mortality Weekly Reports 44, 501-503.

    Google Scholar 

  • Cobeljic, M., Lepsanovic, Z. & Velimirovic S. 1995 Infrequent finding of verotoxin-producing Escherichia coli in diarrheal stools in Belgrade, Serbia. Scandinavian Journal of Infectious Diseases 27, 427–428.

    CAS  Google Scholar 

  • Decludt, B., Bouvet, P., Mariani-Kurkdjian, P., Grimont, F., Grimont, P.A.D., Hubert, B., Loirat, C. & The Societe de Nephrologie Pediatrique. 2000 Haemolytic uraemic syndrome and Shiga toxin-producing Escherichia coli infection in children in France. Epidemiology and Infection 124, 215–220.

    Article  CAS  Google Scholar 

  • Deschenes, G., Casenave, C., Grimont, F., Desenclos, J.C., Benoit, S., Collin, M., Baron, S., Mariani, P., Grimont, P.A. & Nivet, H. 1996 Cluster of cases of haemolytic uraemic syndrome due to unpasteurised cheese. Pediatric Nephrology 10, 203-205.

    CAS  Google Scholar 

  • Franke, S., Harmsen, D., Caprioli, A., Pierard, D., Wieler, L.H. & Karch, H. 1995a. Clonal relatedness of Shiga-like toxin-producing Escherichia coli O101 strains of human and porcine origin. Journal of Clinical Microbiology 33, 3174–3178.

    CAS  Google Scholar 

  • Franke, S., Gunzer, F., Wieler, L.H., Baljer, G. & Karch, H. 1995b Construction of recombinant Shiga-like toxin IIv (SLT-IIv) and its use in monitoring the SLT-IIv antibody status of pigs. Veterinary Microbiology 43, 41–52.

    Article  CAS  Google Scholar 

  • Fürst, S., Scheef, J., Bielaszewska, M., Rüssmann, H., Schmidt, H. & Karch, H. 2000 Identification and characterisation of Escherichia coli strains if O157 and non-O157 serogroups containing three distinct Shiga toxin genes. Journal of Medical Microbiology 49, 383–386.

    Google Scholar 

  • Goldwater, P.N. & Bettelheim, K.A. 1995a The role of enterohaemorrhagic Escherichia coli serotypes other than O157:H7 as causes of disease. Communicable Disease Intelligence 19, 2-4.

    Google Scholar 

  • Goldwater, P.N. & Bettelheim, K.A. 1995b Hemolytic uremic syndrome due to Shiga-like toxin-producing Escherichia coli O48:H21 in South Australia. Emerging Infectious Diseases 1, 132–133.

    Article  CAS  Google Scholar 

  • Griffin, P.M. 1998 Epidemiology of Shiga toxin-producing Escherichia coli infections in humans in the United States. In Escherichia coli O157:H7 and Other Shiga Toxin-Producing E. coli Strains, eds. Kaper, J.B. & O'Brien, A.D. pp. 15–22. Washington, DC: American Society for Microbiology. ISBN 1-55581-129-9.

    Google Scholar 

  • Gunzer, F., Böhm, H., Rüssmann, H., Bitzan, M., Aleksic, S. & Karch, H. 1992 Molecular detection of sorbitol-fermenting Escherichia coli O157 in patients with hemolytic-uremic syndrome. Journal of Clinical Microbiology 30, 1807-1810.

    CAS  Google Scholar 

  • Hull, A.E., Acheson, D.W., Echeverria, P., Donohue Rolfe, A. & Keusch, G.T. 1993 Mitomycin immunoblot colony assay for detection of Shiga-like toxin-producing Escherichia coli in fecal samples: comparison with DNA probes. Journal of Clinical Microbiololgy 31, 1167-1172.

    CAS  Google Scholar 

  • Huppertz, H.I., Busch, D., Schmidt, H., Aleksic, S. & Karch, H. 1996 Diarrhea in young children associated with Escherichia coli non-O157 organisms that produce Shiga-like toxin. Journal of Pediatrics 128, 341–346.

    Article  CAS  Google Scholar 

  • Johnson, R.P., Clarke, R.C., Wilson, J.B., Read, S.C., Rahn, K., Renwick, S.A., Sandhu, K.A., Alves, D., Karmali, M.A., Lior, H., McEwen, S.A., Spika, J.S. & Gyles, C.L. 1996 Growing concerns and recent outbreaks involving non-O157:H7 serotypes of verotoxigenic Escherichia coli. Journal of Food Protection 59, 1112-1122.

    Google Scholar 

  • Karch, H., Strockbine, N.A. & O'Brien, A.D. 1986 Growth of Escherichia coli in the presence of trimethoprim-sulfamethoxazole facilitates detection of Shiga-like toxin producing strains by colony blot assay. FEMS Microbiology Letters 35, 141–145.

    Article  CAS  Google Scholar 

  • Karch, H. & Meyer, T. 1989 Evaluation of oligonucleotide probes for identification of Shiga-like-toxin-producing Escherichia coli. Journal of Clinical Microbiology 27, 1180–1186.

    CAS  Google Scholar 

  • Karch, H., Wiss, R., Glonning, H., Emmrich, P., Aleksic, S. & Bockemühl, J. 1990 Hämolytisch-urämisches Syndrom bei Kleinkindern durch Verotoxin-produzierende Escherichia coli. Deutsche Medizinische Wochenschrifft 115, 485-495.

    Google Scholar 

  • Karch, H., Böhm, H., Schmidt, H., Gunzer, F., Aleksic, S. & Heesemann, J. 1993 Clonal structure and pathogenicity of Shiga-like toxin-producing, sorbitol-fermenting Escherichia coli O157:H¯. Journal of Clinical Microbiology 31, 1200–1205.

    CAS  Google Scholar 

  • Karch, H., Huppertz, H.-I., Bockemühl, J., Schmidt, H., Schwarzkopf, A. & Lissner, R. 1997 Shiga toxin-producing Escherichia coli infections in Germany. Journal of Food Protection 11, 1454–1457.

    Google Scholar 

  • Karch, H., Bielaszewska, M., Bitzan, M. & Schmidt, H. 1999 Epidemiology and diagnosis of Shiga toxin-producing Escherichia coli infections. Diagnostic Microbiology and Infectious Disease 34, 229-243.

    Article  CAS  Google Scholar 

  • Karmali, M.A., Petric, M., Lim, C., Fleming, P.C., Arbus, G.S. & Lior, H. 1985 The association between idiopathic hemolytic uremic syndrome and infection by verotoxin-producing Escherichia coli. Journal of Infectious Diseases 151, 775–782.

    CAS  Google Scholar 

  • Keskimäki, M., Saari, M., Heiskanen, T. & Siitonen, A. 1998 Shiga toxin-producing Escherichia coli in Finland from 1990 through 1997: prevalence and characteristics of isolates. Journal of Clinical Microbiology 36, 3641–3646.

    Google Scholar 

  • Kudoh, Y., Kai, A., Obata, H., Kusunoki, J., Monma, C., Shingaki, M., Yanagawa, Y., Yamada, S., Matsushita, S., Itoh, T. & Ohta, T. 1994 Epidemiological surveys on verocytotoxin-producing Escherichia coli in Japan. In Recent advances in Verocytotoxin-Producing Escherichia coli Infections; Proceedings of the 2nd International Symposium and Workshop on Verocytotoxin (Shiga-like Toxin)-Producing Escherichia coli Infections, Bergamo, Italy, 27-30 June 1994, eds. Karmali, M.A. & Goglio A.G. pp. 53-56. Amsterdam: Elsevier Science B.V. ISBN 0-444-81840-5.

    Google Scholar 

  • Lopez, E.L., Diaz, M., Grinstein, S., Devoto, S., Mendilaharz, F., Murray, B.E., Askhenazi, S., Rubeglio, E., Woloj, M., Vasquez, M., Turco, M., Pickering, L.K. & Cleary, T.G. 1989 Hemolytic uremic syndrome and diarrhoea in Argentine children: the role of Shiga-like toxins. Journal of Infectious Diseases 160, 469–475.

    CAS  Google Scholar 

  • March, S.B. & Ratnam, S. 1986 Sorbitol-MacConkey medium for detection of Escherichia coli O157: H7 associated with hemorrhagic colitis. Journal of Clinical Microbiology 23, 869-872.

    CAS  Google Scholar 

  • Mariani-Kurkdjian, P., Denamur, E., Milon, A., Picard, B., Cave, H., Lambert Zechovsky, N., Loirat, C., Goullet, P., Sansonetti, P.J. & Elion, J. 1993 Identification of a clone of Escherichia coli O103:H2 as a potential agent of hemolytic-uremic syndrome in France. Journal of Clinical Microbiology 31, 296–301.

    CAS  Google Scholar 

  • Michino, H., Araki, H., Minami, S., Nakayama, T., Ejiama, Y., Hiroe, K., Tanaka, H., Fujita, N., Usami, S., Yonekawa, M., Sadamoto, K., Takaya, S. & Sakai, N. 1998 Recent outbreaks of infections caused by Escherichia coli O157:H7 in Japan. In Escherichia coli O157:H7 and other Shiga Toxin-Producing E. coli strains, eds. Kaper, J.B. & O'Brien, A.D. pp. 73–81. Washington, DC: American Society for Microbiology. ISBN 1-55581-129-9.

    Google Scholar 

  • Pai, C., Ahmed, N., Lior, H., Johnson, W.J., Sims, H.V. & Woods, D.E. 1988 Epidemiology of sporadic diarrhea due to verocytotox-in-producing Escherichia coli: a two-year prospective study. Journal of Infectious Diseases 157, 1954-1057.

    Google Scholar 

  • Park, C.H., Gates, K.M., Vandel, N.M. & Hixon, D.L. 1996 Isolation of Shiga-like toxin producing Escherichia coli (O157 and non-O157) in a community hospital. Diagnostic Microbiology and Infectious Disease 26, 69-72.

    Article  CAS  Google Scholar 

  • Paton, A.W., Ratcliff, R.M., Doyle, R.M., Seymour Murray, J., Davos, D., Lanser, J.A. & Paton, J.C. 1996 Molecular microbiological investigation of an outbreak of hemolytic-uremic syndrome caused by dry fermented sausage contaminated with Shiga-like toxin-producing Escherichia coli. Journal of Clinical Microbiology 34, 1622–1627.

    CAS  Google Scholar 

  • Piérard, D., Huyghens, L., Lauwers, S. & Lior, H. 1991 Diarrhoea associated with Escherichia coli producing porcine oedema disease verotoxin. Lancet 338, 762.

    Article  Google Scholar 

  • Piérard, D., Stevens, D., Moriau, L., Lior, H. & Lauwers, S. 1997 Isolation and virulence factors of verocytotoxin-producing Escherichia coli in human stool samples. Clinical Microbiology and Infection 3, 531–540.

    Article  Google Scholar 

  • Piéard, D., Muyldermans, G., Moriau, L., Stevens, D. & Lauwers, S. 1998 Identification of a new verocytotoxin type 2 variant B-subunit genes in human and animal Escherichia coli isolates. Journal of Clinical Microbiology 36, 3317-3322.

    Google Scholar 

  • Rowe, P.C., Orrbine, E., Lior, H., Wells, G.A. & McLaine, P.N. 1993 A prospective study of exposure to verotoxin-producing Escherichia coli among Canadian children with haemolytic uraemic syndrome. Epidemiology and Infection 110, 1–7.

    Article  CAS  Google Scholar 

  • Schmidt, H., Rüssmann, H., Schwarzkopf, A., Aleksic, S., Heesemann, J. & Karch, H. 1994 Prevalence of attaching and effacing Escherichia coli in stool samples from patients and controls. Zentralblatt für Bakteriologie. International Journal of Medical Microbiology, Virology, Parasitology and Infectious Diseases 281, 201–213.

    CAS  Google Scholar 

  • Schmidt, H., Beutin, L. & Karch, H. 1995 Molecular analysis of the plasmid-encoded hemolysin of Escherichia coli O157:H7 strain EDL 933. Infection and Immunity 63, 1055-1061.

    CAS  Google Scholar 

  • Schmidt, H., Geitz, C., Tarr, P.I., Frosch, M. & Karch, H. 1999 Non-O157 pathogenic Shiga toxin-producing Escherichia coli: phenotypic and genetic profiling of virulence traits and evidence for clonality. Journal of Infectious Diseases 179, 115–123.

    Article  CAS  Google Scholar 

  • Schmidt, H., Scheef, J., Morabito, S., Caprioli, A., Wieler, L. & Karch, H. 2000 A new Shiga toxin variant (Stx2f) from Escherichia coli isolated from pigeons. Applied and Environmental Microbiology 66, 1205–1208.

    Article  CAS  Google Scholar 

  • Smith, H.R., Rowe, B., Adak, G.K. & Reilly, W.J. 1998 Shiga toxin (verocytotoxin)-producing Escherichia coli in the United Kingdom. In Escherichia coli O157:H7 and Other Shiga Toxin-Producing E. coli Strains, eds. Kaper, J.B. & O'Brien, A.D. pp. 49–58. Washington, DC: American Society for Microbiology. ISBN 1-55581-129-9.

    Google Scholar 

  • Tarr, P.I. 1995 Escherichia coli O157:H7: clinical, diagnostic, and epidemiological aspects of human infection. Clinical Infectious Diseases 20, 1-8.

    CAS  Google Scholar 

  • Tarr, P.I. & Neill, M.A. 1996 Perspective: the problem of non-O157 Shiga toxin (verocytotoxin)-producing Escherichia coli. Journal of Infectious Diseases 174, 1136-1139.

    CAS  Google Scholar 

  • van de Kar, N.C.A.J., Roelofs, H.G.R., Muytjens, H.L., Tolboom, J.J.M., Chart, H. & Monnens, L.A. 1994 Verocytotoxin-producing Escherichia coli infections in patients with hemolytic uremic syndrome and their family members in the Netherlands. In Recent advances in Verocytotoxin-Producing Escherichia coli Infections; Proceedings of the 2nd International Symposium and Workshop on Verocytotoxin (Shiga-like Toxin)-Producing Escherichia coli Infections, Bergamo, Italy, 27-30 June 1994, eds. Karmali, M.A. & Goglio A.G. pp. 45–48. Amsterdam: Elsevier Science B. V. ISBN 0-444-81840-5.

    Google Scholar 

  • World Health Organization. 1999 Zoonotic non-O157 Shiga toxin-producing Escherichia coli (STEC). Report of a WHO Scientific Working Group Meeting, Berlin, Germany, 23-26 June, 1998.

  • Zhang, W.-L., Bielaszewska, M., Liesegang, A., Tschäpe, H., Schmidt, H., Bitzan, M. & Karch, H. 2000 Molecular characterization and epidemiological significance of Shiga toxin-producing Escherichia coli O26 strains. Journal of Clinical Microbiology 38, 2134-2140.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bielaszewska, M., Karch, H. Non-O157:H7 Shiga toxin (verocytotoxin)-producing Escherichia coli strains: epidemiological significance and microbiological diagnosis. World Journal of Microbiology and Biotechnology 16, 711–718 (2000). https://doi.org/10.1023/A:1008972605514

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1008972605514

Navigation