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Published in: BMC Infectious Diseases 1/2015

Open Access 01-12-2015 | Research article

Shiga toxin-producing escherichia coli infections in Norway, 1992–2012: characterization of isolates and identification of risk factors for haemolytic uremic syndrome

Authors: Lin T. Brandal, Astrid L. Wester, Heidi Lange, Inger Løbersli, Bjørn-Arne Lindstedt, Line Vold, Georg Kapperud

Published in: BMC Infectious Diseases | Issue 1/2015

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Abstract

Background

Shiga toxin-producing E. coli (STEC) infection is associated with haemolytic uremic syndrome (HUS). Therefore Norway has implemented strict guidelines for prevention and control of STEC infection. However, only a subgroup of STEC leads to HUS. Thus, identification of determinants differentiating high risk STEC (HUS STEC) from low risk STEC (non-HUS STEC) is needed to enable implementation of graded infectious disease response.

Methods

A national study of 333 STEC infections in Norway, including one STEC from each patient or outbreak over two decades (1992–2012), was conducted. Serotype, virulence profile, and genotype of each STEC were determined by phenotypic or PCR based methods. The association between microbiological properties and demographic and clinical data was assessed by univariable analyses and multiple logistic regression models.

Results

From 1992 through 2012, an increased number of STEC cases including more domestically acquired infections were notified in Norway. O157 was the most frequent serogroup (33.6 %), although a decrease of this serogroup was seen over the last decade. All 25 HUS patients yielded STEC with stx2, eae, and ehxA. In a multiple logistic regression model, age ≤5 years (OR = 16.7) and stx2a (OR = 30.1) were independently related to increased risk of HUS. eae and hospitalization could not be modelled since all HUS patients showed these traits. The combination of low age (≤5 years) and the presence of stx2a, and eae gave a positive predictive value (PPV) for HUS of 67.5 % and a negative predictive value (NPV) of 99.0 %. SF O157:[H7] and O145:H?, although associated with HUS in the univariable analyses, were not independent risk factors. stx1 (OR = 0.1) was the sole factor independently associated with a reduced risk of HUS (NPV: 79.7 %); stx2c was not so.

Conclusions

Our results indicate that virulence gene profile and patients’ age are the major determinants of HUS development.
Appendix
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Literature
1.
2.
go back to reference Ethelberg S, Olsen KE, Scheutz F, Jensen C, Schiellerup P, Enberg J, et al. Virulence factors for hemolytic uremic syndrome, Denmark. Emerg Infect Dis. 2004;10:842–7.CrossRefPubMedPubMedCentral Ethelberg S, Olsen KE, Scheutz F, Jensen C, Schiellerup P, Enberg J, et al. Virulence factors for hemolytic uremic syndrome, Denmark. Emerg Infect Dis. 2004;10:842–7.CrossRefPubMedPubMedCentral
3.
go back to reference Buvens G, De Gheldre Y, Dediste A, de Moreau AI, Mascart G, Simon A, et al. Incidence and virulence determinants of verocytotoxin-producing Escherichia coli infections in the Brussels-Capital Region, Belgium, in 2008–2010. J Clin Microbiol. 2012;50:1336–45.CrossRefPubMedPubMedCentral Buvens G, De Gheldre Y, Dediste A, de Moreau AI, Mascart G, Simon A, et al. Incidence and virulence determinants of verocytotoxin-producing Escherichia coli infections in the Brussels-Capital Region, Belgium, in 2008–2010. J Clin Microbiol. 2012;50:1336–45.CrossRefPubMedPubMedCentral
4.
go back to reference Mellmann A, Bielaszewska M, Kock R, Friedrich AW, Fruth A, Middendorf B, et al. Analysis of collection of hemolytic uremic syndrome-associated enterohemorrhagic Escherichia coli. Emerg Infect Dis. 2008;14:1287–90.CrossRefPubMedPubMedCentral Mellmann A, Bielaszewska M, Kock R, Friedrich AW, Fruth A, Middendorf B, et al. Analysis of collection of hemolytic uremic syndrome-associated enterohemorrhagic Escherichia coli. Emerg Infect Dis. 2008;14:1287–90.CrossRefPubMedPubMedCentral
5.
go back to reference Friedrich AW, Bielaszewska M, Zhang WL, Pulz M, Kuczius T, Ammon A, et al. Escherichia coli harboring Shiga toxin 2 gene variants: frequency and association with clinical symptoms. J Infect Dis. 2002;185:74–84.CrossRefPubMed Friedrich AW, Bielaszewska M, Zhang WL, Pulz M, Kuczius T, Ammon A, et al. Escherichia coli harboring Shiga toxin 2 gene variants: frequency and association with clinical symptoms. J Infect Dis. 2002;185:74–84.CrossRefPubMed
6.
go back to reference Bielaszewska M, Friedrich AW, Aldick T, Schurk-Bulgrin R, Karch H. Shiga toxin activatable by intestinal mucus in Escherichia coli isolated from humans: predictor for a severe clinical outcome. Clin Infect Dis. 2006;43:1160–7.CrossRefPubMed Bielaszewska M, Friedrich AW, Aldick T, Schurk-Bulgrin R, Karch H. Shiga toxin activatable by intestinal mucus in Escherichia coli isolated from humans: predictor for a severe clinical outcome. Clin Infect Dis. 2006;43:1160–7.CrossRefPubMed
7.
go back to reference Persson S, Olsen KE, Ethelberg S, Scheutz F. Subtyping method for Escherichia coli shiga toxin (verocytotoxin) 2 variants and correlations to clinical manifestations. J Clin Microbiol. 2007;45:2020–4.CrossRefPubMedPubMedCentral Persson S, Olsen KE, Ethelberg S, Scheutz F. Subtyping method for Escherichia coli shiga toxin (verocytotoxin) 2 variants and correlations to clinical manifestations. J Clin Microbiol. 2007;45:2020–4.CrossRefPubMedPubMedCentral
8.
go back to reference Scheutz F, Teel LD, Beutin L, Pierard D, Buvens G, Karch H, et al. Multicenter evaluation of a sequence-based protocol for subtyping Shiga toxins and standardizing Stx nomenclature. J Clin Microbiol. 2012;50:2951–63.CrossRefPubMedPubMedCentral Scheutz F, Teel LD, Beutin L, Pierard D, Buvens G, Karch H, et al. Multicenter evaluation of a sequence-based protocol for subtyping Shiga toxins and standardizing Stx nomenclature. J Clin Microbiol. 2012;50:2951–63.CrossRefPubMedPubMedCentral
9.
go back to reference Marejkova M, Blahova K, Janda J, Fruth A, Petras P. Enterohemorrhagic Escherichia coli as causes of hemolytic uremic syndrome in the Czech Republic. PLoS One. 2013;8:e73927.CrossRefPubMedPubMedCentral Marejkova M, Blahova K, Janda J, Fruth A, Petras P. Enterohemorrhagic Escherichia coli as causes of hemolytic uremic syndrome in the Czech Republic. PLoS One. 2013;8:e73927.CrossRefPubMedPubMedCentral
11.
go back to reference Melton-Celsa A, Mohawk K, Teel L, O'Brien A. Pathogenesis of Shiga-toxin producing escherichia coli. Curr Top Microbiol Immunol. 2012;357:67–103.PubMed Melton-Celsa A, Mohawk K, Teel L, O'Brien A. Pathogenesis of Shiga-toxin producing escherichia coli. Curr Top Microbiol Immunol. 2012;357:67–103.PubMed
12.
go back to reference Vally H, Hall G, Dyda A, Raupach J, Knope K, Combs B, et al. Epidemiology of Shiga toxin producing Escherichia coli in Australia, 2000–2010. BMC Public Health. 2012;12:63.CrossRefPubMedPubMedCentral Vally H, Hall G, Dyda A, Raupach J, Knope K, Combs B, et al. Epidemiology of Shiga toxin producing Escherichia coli in Australia, 2000–2010. BMC Public Health. 2012;12:63.CrossRefPubMedPubMedCentral
13.
go back to reference Rivero MA, Passucci JA, Rodriguez EM, Parma AE. Seasonal variation of HUS occurrence and VTEC infection in children with acute diarrhoea from Argentina. Eur J Clin Microbiol Infect Dis. 2012;31:1131–5.CrossRefPubMed Rivero MA, Passucci JA, Rodriguez EM, Parma AE. Seasonal variation of HUS occurrence and VTEC infection in children with acute diarrhoea from Argentina. Eur J Clin Microbiol Infect Dis. 2012;31:1131–5.CrossRefPubMed
14.
go back to reference Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, et al. Foodborne illness acquired in the United States--major pathogens. Emerg Infect Dis. 2011;17:7–15.CrossRefPubMedPubMedCentral Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, et al. Foodborne illness acquired in the United States--major pathogens. Emerg Infect Dis. 2011;17:7–15.CrossRefPubMedPubMedCentral
15.
go back to reference Locking ME, Pollock KG, Allison LJ, Rae L, Hanson MF, Cowden JM. Escherichia coli O157 infection and secondary spread, Scotland, 1999–2008. Emerg Infect Dis. 2011;17:524–7.CrossRefPubMedPubMedCentral Locking ME, Pollock KG, Allison LJ, Rae L, Hanson MF, Cowden JM. Escherichia coli O157 infection and secondary spread, Scotland, 1999–2008. Emerg Infect Dis. 2011;17:524–7.CrossRefPubMedPubMedCentral
16.
go back to reference Gould LH, Mody RK, Ong KL, Clogher P, Cronquist AB, Garman KN, et al. 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. 2013;10:453–60.CrossRefPubMed Gould LH, Mody RK, Ong KL, Clogher P, Cronquist AB, Garman KN, et al. 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. 2013;10:453–60.CrossRefPubMed
17.
go back to reference Beutin L, Krause G, Zimmermann S, Kaulfuss S, Gleier K. Characterization of Shiga toxin-producing Escherichia coli strains isolated from human patients in Germany over a 3-year period. J Clin Microbiol. 2004;42:1099–108.CrossRefPubMedPubMedCentral Beutin L, Krause G, Zimmermann S, Kaulfuss S, Gleier K. Characterization of Shiga toxin-producing Escherichia coli strains isolated from human patients in Germany over a 3-year period. J Clin Microbiol. 2004;42:1099–108.CrossRefPubMedPubMedCentral
18.
go back to reference Kappeli U, Hachler H, Giezendanner N, Beutin L, Stephan R. Human infections with non-O157 Shiga toxin-producing Escherichia coli, Switzerland, 2000–2009. Emerg Infect Dis. 2011;17:180–5.CrossRefPubMedPubMedCentral Kappeli U, Hachler H, Giezendanner N, Beutin L, Stephan R. Human infections with non-O157 Shiga toxin-producing Escherichia coli, Switzerland, 2000–2009. Emerg Infect Dis. 2011;17:180–5.CrossRefPubMedPubMedCentral
19.
go back to reference van Duynhoven YT, Friesema IH, Schuurman T, Roovers A, van Zwet AA, Sabbe LJ, et al. Prevalence, characterisation and clinical profiles of Shiga toxin-producing Escherichia coli in The Netherlands. Clin Microbiol Infect. 2008;14:437–45.CrossRefPubMed van Duynhoven YT, Friesema IH, Schuurman T, Roovers A, van Zwet AA, Sabbe LJ, et al. Prevalence, characterisation and clinical profiles of Shiga toxin-producing Escherichia coli in The Netherlands. Clin Microbiol Infect. 2008;14:437–45.CrossRefPubMed
20.
go back to reference European Food Safety Authority ECfDPaC: The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2011. EFSA Journal 2013,11:3129 [250 pp.]. doi:10.2903/j.efsa.2013.3129 2013. European Food Safety Authority ECfDPaC: The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2011. EFSA Journal 2013,11:3129 [250 pp.]. doi:10.​2903/​j.​efsa.​2013.​3129 2013.
21.
22.
go back to reference Norwegian Institute of Public Health: E. coli-enteritt (inkludert EHEC-infeksjon og HUS). Smittevernboka 2013 [In Norwegian], [http://www.fhi.no/eway/default.aspx?pid = 239&trg = Content_6493&Main_6157 = 6287:0:25,5499&MainContent_6287 = 6493:0:25,6833&Content_6493 = 6441:82709::0:6446:32:::0:0] Norwegian Institute of Public Health: E. coli-enteritt (inkludert EHEC-infeksjon og HUS). Smittevernboka 2013 [In Norwegian], [http://​www.​fhi.​no/​eway/​default.​aspx?​pid = 239&trg = Content_6493&Main_6157 = 6287:0:25,5499&MainContent_6287 = 6493:0:25,6833&Content_6493 = 6441:82709::0:6446:32:::0:0]
23.
go back to reference Wong CS, Mooney JC, Brandt JR, Staples AO, Jelacic S, Boster DR, et al. Risk factors for the hemolytic uremic syndrome in children infected with Escherichia coli O157:H7: a multivariable analysis. Clin Infect Dis. 2012;55:33–41.CrossRefPubMedPubMedCentral Wong CS, Mooney JC, Brandt JR, Staples AO, Jelacic S, Boster DR, et al. Risk factors for the hemolytic uremic syndrome in children infected with Escherichia coli O157:H7: a multivariable analysis. Clin Infect Dis. 2012;55:33–41.CrossRefPubMedPubMedCentral
24.
go back to reference Werber D, King LA, Muller L, Follin P, Buchholz U, Bernard H, et al. Associations of age and sex with the clinical outcome and incubation period of Shiga toxin-producing Escherichia coli O104:H4 infections, 2011. Am J Epidemiol. 2013;178:984–92.CrossRefPubMed Werber D, King LA, Muller L, Follin P, Buchholz U, Bernard H, et al. Associations of age and sex with the clinical outcome and incubation period of Shiga toxin-producing Escherichia coli O104:H4 infections, 2011. Am J Epidemiol. 2013;178:984–92.CrossRefPubMed
25.
go back to reference Zoufaly A, Cramer JP, Vettorazzi E, Sayk F, Bremer JP, Koop I, et al. Risk factors for development of hemolytic uremic syndrome in a cohort of adult patients with STEC 0104:H4 infection. PLoS One. 2013;8:e59209.CrossRefPubMedPubMedCentral Zoufaly A, Cramer JP, Vettorazzi E, Sayk F, Bremer JP, Koop I, et al. Risk factors for development of hemolytic uremic syndrome in a cohort of adult patients with STEC 0104:H4 infection. PLoS One. 2013;8:e59209.CrossRefPubMedPubMedCentral
26.
go back to reference Haugum K, Brandal LT, Lindstedt BA, Wester AL, Bergh K, Afset JE. PCR-Based Detection and Molecular Characterization of Shiga Toxin-Producing Escherichia coli Strains in a Routine Microbiology Laboratory over 16 years. J Clin Microbiol. 2014;52:3156–63.CrossRefPubMedPubMedCentral Haugum K, Brandal LT, Lindstedt BA, Wester AL, Bergh K, Afset JE. PCR-Based Detection and Molecular Characterization of Shiga Toxin-Producing Escherichia coli Strains in a Routine Microbiology Laboratory over 16 years. J Clin Microbiol. 2014;52:3156–63.CrossRefPubMedPubMedCentral
27.
go back to reference Haugum K, Lindstedt BA, Lobersli I, Kapperud G, Brandal LT. Identification of the anti-terminator qO111:H)- gene in Norwegian sorbitol-fermenting Escherichia coli O157:NM. FEMS Microbiol Lett. 2012;329:102–10.CrossRefPubMed Haugum K, Lindstedt BA, Lobersli I, Kapperud G, Brandal LT. Identification of the anti-terminator qO111:H)- gene in Norwegian sorbitol-fermenting Escherichia coli O157:NM. FEMS Microbiol Lett. 2012;329:102–10.CrossRefPubMed
28.
go back to reference Back E, Svennerholm AM, Holmgren J, Mollby R. Evaluation of a ganglioside immunosorbent assay for detection of Escherichia coli heat-labile enterotoxin. J Clin Microbiol. 1979;10:791–5.PubMedPubMedCentral Back E, Svennerholm AM, Holmgren J, Mollby R. Evaluation of a ganglioside immunosorbent assay for detection of Escherichia coli heat-labile enterotoxin. J Clin Microbiol. 1979;10:791–5.PubMedPubMedCentral
29.
go back to reference Brian MJ, Frosolono M, Murray BE, Miranda A, Lopez EL, Gomez HF, et al. Polymerase chain reaction for diagnosis of enterohemorrhagic Escherichia coli infection and hemolytic-uremic syndrome. J Clin Microbiol. 1992;30:1801–6.PubMedPubMedCentral Brian MJ, Frosolono M, Murray BE, Miranda A, Lopez EL, Gomez HF, et al. Polymerase chain reaction for diagnosis of enterohemorrhagic Escherichia coli infection and hemolytic-uremic syndrome. J Clin Microbiol. 1992;30:1801–6.PubMedPubMedCentral
30.
go back to reference Gannon VP, Rashed M, King RK, Thomas EJ. Detection and characterization of the eae gene of Shiga-like toxin-producing Escherichia coli using polymerase chain reaction. J Clin Microbiol. 1993;31:1268–74.PubMedPubMedCentral Gannon VP, Rashed M, King RK, Thomas EJ. Detection and characterization of the eae gene of Shiga-like toxin-producing Escherichia coli using polymerase chain reaction. J Clin Microbiol. 1993;31:1268–74.PubMedPubMedCentral
31.
go back to reference Wang G, Clark CG, Rodgers FG. Detection in Escherichia coli of the genes encoding the major virulence factors, the genes defining the O157:H7 serotype, and components of the type 2 Shiga toxin family by multiplex PCR. J Clin Microbiol. 2002;40:3613–9.CrossRefPubMedPubMedCentral Wang G, Clark CG, Rodgers FG. Detection in Escherichia coli of the genes encoding the major virulence factors, the genes defining the O157:H7 serotype, and components of the type 2 Shiga toxin family by multiplex PCR. J Clin Microbiol. 2002;40:3613–9.CrossRefPubMedPubMedCentral
32.
go back to reference Brandal LT, Lindstedt BA, Aas L, Stavnes TL, Lassen J, Kapperud G. Octaplex PCR and fluorescence-based capillary electrophoresis for identification of human diarrheagenic Escherichia coli and Shigella spp. J Microbiol Methods. 2007;68:331–41.CrossRefPubMed Brandal LT, Lindstedt BA, Aas L, Stavnes TL, Lassen J, Kapperud G. Octaplex PCR and fluorescence-based capillary electrophoresis for identification of human diarrheagenic Escherichia coli and Shigella spp. J Microbiol Methods. 2007;68:331–41.CrossRefPubMed
33.
go back to reference Brandal LT, Sekse C, Lindstedt BA, Sunde M, Lobersli I, Urdahl AM, et al. Norwegian sheep are an important reservoir for human-pathogenic Escherichia coli O26:H11. Appl Environ Microbiol. 2012;78:4083–91.CrossRefPubMedPubMedCentral Brandal LT, Sekse C, Lindstedt BA, Sunde M, Lobersli I, Urdahl AM, et al. Norwegian sheep are an important reservoir for human-pathogenic Escherichia coli O26:H11. Appl Environ Microbiol. 2012;78:4083–91.CrossRefPubMedPubMedCentral
34.
go back to reference Toma C, Lu Y, Higa N, Nakasone N, Chinen I, Baschkier A, et al. Multiplex PCR assay for identification of human diarrheagenic Escherichia coli. J Clin Microbiol. 2003;41:2669–71.CrossRefPubMedPubMedCentral Toma C, Lu Y, Higa N, Nakasone N, Chinen I, Baschkier A, et al. Multiplex PCR assay for identification of human diarrheagenic Escherichia coli. J Clin Microbiol. 2003;41:2669–71.CrossRefPubMedPubMedCentral
35.
go back to reference Bolin I, Wiklund G, Qadri F, Torres O, Bourgeois AL, Savarino S, et al. Enterotoxigenic Escherichia coli with STh and STp genotypes is associated with diarrhea both in children in areas of endemicity and in travelers. J Clin Microbiol. 2006;44:3872–7.CrossRefPubMedPubMedCentral Bolin I, Wiklund G, Qadri F, Torres O, Bourgeois AL, Savarino S, et al. Enterotoxigenic Escherichia coli with STh and STp genotypes is associated with diarrhea both in children in areas of endemicity and in travelers. J Clin Microbiol. 2006;44:3872–7.CrossRefPubMedPubMedCentral
36.
go back to reference Russmann H, Schmidt H, Heesemann J, Caprioli A, Karch H. Variants of Shiga-like toxin II constitute a major toxin component in Escherichia coli O157 strains from patients with haemolytic uraemic syndrome. J Med Microbiol. 1994;40:338–43.CrossRefPubMed Russmann H, Schmidt H, Heesemann J, Caprioli A, Karch H. Variants of Shiga-like toxin II constitute a major toxin component in Escherichia coli O157 strains from patients with haemolytic uraemic syndrome. J Med Microbiol. 1994;40:338–43.CrossRefPubMed
37.
go back to reference Jelacic JK, Damrow T, Chen GS, Jelacic S, Bielaszewska M, Ciol M, et al. Shiga toxin-producing Escherichia coli in Montana: bacterial genotypes and clinical profiles. J Infect Dis. 2003;188:719–29.CrossRefPubMed Jelacic JK, Damrow T, Chen GS, Jelacic S, Bielaszewska M, Ciol M, et al. Shiga toxin-producing Escherichia coli in Montana: bacterial genotypes and clinical profiles. J Infect Dis. 2003;188:719–29.CrossRefPubMed
38.
go back to reference Zheng J, Cui S, Teel LD, Zhao S, Singh R, O'Brien AD, et al. Identification and characterization of Shiga toxin type 2 variants in Escherichia coli isolates from animals, food, and humans. Appl Environ Microbiol. 2008;74:5645–52.CrossRefPubMedPubMedCentral Zheng J, Cui S, Teel LD, Zhao S, Singh R, O'Brien AD, et al. Identification and characterization of Shiga toxin type 2 variants in Escherichia coli isolates from animals, food, and humans. Appl Environ Microbiol. 2008;74:5645–52.CrossRefPubMedPubMedCentral
39.
go back to reference Lindstedt BA, Heir E, Gjernes E, Vardund T, Kapperud G. DNA fingerprinting of Shiga-toxin producing Escherichia coli O157 based on Multiple-Locus Variable-Number Tandem-Repeats Analysis (MLVA). Ann Clin Microbiol Antimicrob. 2003;2:12.CrossRefPubMedPubMedCentral Lindstedt BA, Heir E, Gjernes E, Vardund T, Kapperud G. DNA fingerprinting of Shiga-toxin producing Escherichia coli O157 based on Multiple-Locus Variable-Number Tandem-Repeats Analysis (MLVA). Ann Clin Microbiol Antimicrob. 2003;2:12.CrossRefPubMedPubMedCentral
40.
go back to reference Lindstedt BA, Brandal LT, Aas L, Vardund T, Kapperud G. Study of polymorphic variable-number of tandem repeats loci in the ECOR collection and in a set of pathogenic Escherichia coli and Shigella isolates for use in a genotyping assay. J Microbiol Methods. 2007;69:197–205.CrossRefPubMed Lindstedt BA, Brandal LT, Aas L, Vardund T, Kapperud G. Study of polymorphic variable-number of tandem repeats loci in the ECOR collection and in a set of pathogenic Escherichia coli and Shigella isolates for use in a genotyping assay. J Microbiol Methods. 2007;69:197–205.CrossRefPubMed
41.
go back to reference Lobersli I, Haugum K, Lindstedt BA. Rapid and high resolution genotyping of all Escherichia coli serotypes using 10 genomic repeat-containing loci. J Microbiol Methods. 2012;88:134–9.CrossRefPubMed Lobersli I, Haugum K, Lindstedt BA. Rapid and high resolution genotyping of all Escherichia coli serotypes using 10 genomic repeat-containing loci. J Microbiol Methods. 2012;88:134–9.CrossRefPubMed
43.
go back to reference Byrne L, Vanstone GL, Perry NT, Launders N, Adak GK, Godbole G, et al. The epidemiology and microbiology of Shiga-toxin producing Escherichia coli other than serogroup O157 in England 2009–2013. J Med Microbiol. 2014;63:1181–8.CrossRefPubMed Byrne L, Vanstone GL, Perry NT, Launders N, Adak GK, Godbole G, et al. The epidemiology and microbiology of Shiga-toxin producing Escherichia coli other than serogroup O157 in England 2009–2013. J Med Microbiol. 2014;63:1181–8.CrossRefPubMed
44.
go back to reference Boerlin P, McEwen SA, Boerlin-Petzold F, Wilson JB, Johnson RP, Gyles CL. Associations between virulence factors of Shiga toxin-producing Escherichia coli and disease in humans. J Clin Microbiol. 1999;37:497–503.PubMedPubMedCentral Boerlin P, McEwen SA, Boerlin-Petzold F, Wilson JB, Johnson RP, Gyles CL. Associations between virulence factors of Shiga toxin-producing Escherichia coli and disease in humans. J Clin Microbiol. 1999;37:497–503.PubMedPubMedCentral
45.
go back to reference Bielaszewska M, Middendorf B, Kock R, Friedrich AW, Fruth A, Karch H, et al. Shiga toxin-negative attaching and effacing Escherichia coli: distinct clinical associations with bacterial phylogeny and virulence traits and inferred in-host pathogen evolution. Clin Infect Dis. 2008;47:208–17.CrossRefPubMed Bielaszewska M, Middendorf B, Kock R, Friedrich AW, Fruth A, Karch H, et al. Shiga toxin-negative attaching and effacing Escherichia coli: distinct clinical associations with bacterial phylogeny and virulence traits and inferred in-host pathogen evolution. Clin Infect Dis. 2008;47:208–17.CrossRefPubMed
46.
go back to reference Bielaszewska M, Zhang W, Tarr PI, Sonntag AK, 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;43:4225–8.CrossRefPubMedPubMedCentral Bielaszewska M, Zhang W, Tarr PI, Sonntag AK, 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;43:4225–8.CrossRefPubMedPubMedCentral
47.
go back to reference Pradel N, Bertin Y, Martin C, Livrelli V. Molecular analysis of shiga toxin-producing Escherichia coli strains isolated from hemolytic-uremic syndrome patients and dairy samples in France. Appl Environ Microbiol. 2008;74:2118–28.CrossRefPubMedPubMedCentral Pradel N, Bertin Y, Martin C, Livrelli V. Molecular analysis of shiga toxin-producing Escherichia coli strains isolated from hemolytic-uremic syndrome patients and dairy samples in France. Appl Environ Microbiol. 2008;74:2118–28.CrossRefPubMedPubMedCentral
48.
go back to reference Kawano K, Ono H, Iwashita O, Kurogi M, Haga T, Maeda K, et al. stx genotype and molecular epidemiological analyses of Shiga toxin-producing Escherichia coli O157:H7/H- in human and cattle isolates. Eur J Clin Microbiol Infect Dis. 2012;31:119–27.CrossRefPubMed Kawano K, Ono H, Iwashita O, Kurogi M, Haga T, Maeda K, et al. stx genotype and molecular epidemiological analyses of Shiga toxin-producing Escherichia coli O157:H7/H- in human and cattle isolates. Eur J Clin Microbiol Infect Dis. 2012;31:119–27.CrossRefPubMed
49.
go back to reference Orth D, Grif K, Khan AB, Naim A, Dierich MP, Wurzner R. The Shiga toxin genotype rather than the amount of Shiga toxin or the cytotoxicity of Shiga toxin in vitro correlates with the appearance of the hemolytic uremic syndrome. Diagn Microbiol Infect Dis. 2007;59:235–42.CrossRefPubMed Orth D, Grif K, Khan AB, Naim A, Dierich MP, Wurzner R. The Shiga toxin genotype rather than the amount of Shiga toxin or the cytotoxicity of Shiga toxin in vitro correlates with the appearance of the hemolytic uremic syndrome. Diagn Microbiol Infect Dis. 2007;59:235–42.CrossRefPubMed
50.
go back to reference Luna-Gierke RE, Griffin PM, Gould LH, Herman K, Bopp CA, Strockbine N, et al. Outbreaks of non-O157 Shiga toxin-producing Escherichia coli infection: USA. Epidemiol Infect. 2014;1–11. Luna-Gierke RE, Griffin PM, Gould LH, Herman K, Bopp CA, Strockbine N, et al. Outbreaks of non-O157 Shiga toxin-producing Escherichia coli infection: USA. Epidemiol Infect. 2014;1–11.
51.
go back to reference Watahiki M, Isobe J, Kimata K, Shima T, Kanatani J, Shimizu M, et al. Characterization of enterohemorrhagic Escherichia coli O111 and O157 strains isolated from outbreak patients in Japan. J Clin Microbiol. 2014;52:2757–63.CrossRefPubMedPubMedCentral Watahiki M, Isobe J, Kimata K, Shima T, Kanatani J, Shimizu M, et al. Characterization of enterohemorrhagic Escherichia coli O111 and O157 strains isolated from outbreak patients in Japan. J Clin Microbiol. 2014;52:2757–63.CrossRefPubMedPubMedCentral
52.
go back to reference Rivero MA, Passucci JA, Rodriguez EM, Parma AE. Role and clinical course of verotoxigenic Escherichia coli infections in childhood acute diarrhoea in Argentina. J Med Microbiol. 2010;59:345–52.CrossRefPubMed Rivero MA, Passucci JA, Rodriguez EM, Parma AE. Role and clinical course of verotoxigenic Escherichia coli infections in childhood acute diarrhoea in Argentina. J Med Microbiol. 2010;59:345–52.CrossRefPubMed
53.
go back to reference Karch H, Tarr PI, Bielaszewska M. Enterohaemorrhagic Escherichia coli in human medicine. Int J Med Microbiol. 2005;295:405–18.CrossRefPubMed Karch H, Tarr PI, Bielaszewska M. Enterohaemorrhagic Escherichia coli in human medicine. Int J Med Microbiol. 2005;295:405–18.CrossRefPubMed
54.
go back to reference Alpers K, Werber D, Frank C, Koch J, Friedrich AW, Karch H, et al. Sorbitol-fermenting enterohaemorrhagic Escherichia coli O157:H- causes another outbreak of haemolytic uraemic syndrome in children. Epidemiol Infect. 2009;137:389–95.CrossRefPubMed Alpers K, Werber D, Frank C, Koch J, Friedrich AW, Karch H, et al. Sorbitol-fermenting enterohaemorrhagic Escherichia coli O157:H- causes another outbreak of haemolytic uraemic syndrome in children. Epidemiol Infect. 2009;137:389–95.CrossRefPubMed
55.
go back to reference Rosser T, Dransfield T, Allison L, Hanson M, Holden N, Evans J, et al. Pathogenic potential of emergent sorbitol-fermenting Escherichia coli O157:NM. Infect Immun. 2008;76:5598–607.CrossRefPubMedPubMedCentral Rosser T, Dransfield T, Allison L, Hanson M, Holden N, Evans J, et al. Pathogenic potential of emergent sorbitol-fermenting Escherichia coli O157:NM. Infect Immun. 2008;76:5598–607.CrossRefPubMedPubMedCentral
56.
go back to reference Nygård K VL, Heier BT, Bruun T, Kapperud G: Annual report: Foodborne infections and outbreaks in 2009. Reporting system for infectious diseases (MSIS) and web-based system for outbreak warning (Vesuv). 2010 [In Norwegian], [http://www.fhi.no/eway/default.aspx?pid = 239&trg = Content_6466&Main_6157 = 6263:0:25,6493&MainContent_6263 = 6466:0:25,6494&Content_6466 = 6259:84108::0:6184:2:::0:0] Nygård K VL, Heier BT, Bruun T, Kapperud G: Annual report: Foodborne infections and outbreaks in 2009. Reporting system for infectious diseases (MSIS) and web-based system for outbreak warning (Vesuv). 2010 [In Norwegian], [http://​www.​fhi.​no/​eway/​default.​aspx?​pid = 239&trg = Content_6466&Main_6157 = 6263:0:25,6493&MainContent_6263 = 6466:0:25,6494&Content_6466 = 6259:84108::0:6184:2:::0:0]
57.
go back to reference Preussel K, Hohle M, Stark K, Werber D. Shiga toxin-producing Escherichia coli O157 is more likely to lead to hospitalization and death than non-O157 serogroups--except O104. PLoS One. 2013;8:e78180.CrossRefPubMedPubMedCentral Preussel K, Hohle M, Stark K, Werber D. Shiga toxin-producing Escherichia coli O157 is more likely to lead to hospitalization and death than non-O157 serogroups--except O104. PLoS One. 2013;8:e78180.CrossRefPubMedPubMedCentral
58.
go back to reference Gerber A, Karch H, Allerberger F, Verweyen HM, Zimmerhackl LB. Clinical course and the role of shiga toxin-producing Escherichia coli infection in the hemolytic-uremic syndrome in pediatric patients, 1997–2000, in Germany and Austria: a prospective study. J Infect Dis. 2002;186:493–500.CrossRefPubMed Gerber A, Karch H, Allerberger F, Verweyen HM, Zimmerhackl LB. Clinical course and the role of shiga toxin-producing Escherichia coli infection in the hemolytic-uremic syndrome in pediatric patients, 1997–2000, in Germany and Austria: a prospective study. J Infect Dis. 2002;186:493–500.CrossRefPubMed
59.
go back to reference Pradel N, Livrelli V, De Champs C, Palcoux JB, Reynaud A, Scheutz F, et al. Prevalence and characterization of Shiga toxin-producing Escherichia coli isolated from cattle, food, and children during a one-year prospective study in France. J Clin Microbiol. 2000;38:1023–31.PubMedPubMedCentral Pradel N, Livrelli V, De Champs C, Palcoux JB, Reynaud A, Scheutz F, et al. Prevalence and characterization of Shiga toxin-producing Escherichia coli isolated from cattle, food, and children during a one-year prospective study in France. J Clin Microbiol. 2000;38:1023–31.PubMedPubMedCentral
60.
go back to reference Blanco JE, Blanco M, Alonso MP, Mora A, Dahbi G, Coira MA, et al. Serotypes, virulence genes, and intimin types of Shiga toxin (verotoxin)-producing Escherichia coli isolates from human patients: prevalence in Lugo, Spain, from 1992 through 1999. J Clin Microbiol. 2004;42:311–9.CrossRefPubMedPubMedCentral Blanco JE, Blanco M, Alonso MP, Mora A, Dahbi G, Coira MA, et al. Serotypes, virulence genes, and intimin types of Shiga toxin (verotoxin)-producing Escherichia coli isolates from human patients: prevalence in Lugo, Spain, from 1992 through 1999. J Clin Microbiol. 2004;42:311–9.CrossRefPubMedPubMedCentral
61.
go back to reference Mingle LA, Garcia DL, Root TP, Halse TA, Quinlan TM, Armstrong LR, et al. Enhanced identification and characterization of non-O157 Shiga toxin-producing Escherichia coli: a six-year study. Foodborne Pathog Dis. 2012;9:1028–36.CrossRefPubMed Mingle LA, Garcia DL, Root TP, Halse TA, Quinlan TM, Armstrong LR, et al. Enhanced identification and characterization of non-O157 Shiga toxin-producing Escherichia coli: a six-year study. Foodborne Pathog Dis. 2012;9:1028–36.CrossRefPubMed
62.
go back to reference Kappeli U, Hachler H, Giezendanner N, Cheasty T, Stephan R: Shiga toxin-producing Escherichia coli O157 associated with human infections in Switzerland, 2000–2009. Epidemiol Infect 2010:1–8. Kappeli U, Hachler H, Giezendanner N, Cheasty T, Stephan R: Shiga toxin-producing Escherichia coli O157 associated with human infections in Switzerland, 2000–2009. Epidemiol Infect 2010:1–8.
63.
go back to reference Hedican EB, Medus C, Besser JM, Juni BA, Koziol B, Taylor C, et al. Characteristics of O157 versus non-O157 Shiga toxin-producing Escherichia coli infections in Minnesota, 2000–2006. Clin Infect Dis. 2009;49:358–64.CrossRefPubMed Hedican EB, Medus C, Besser JM, Juni BA, Koziol B, Taylor C, et al. Characteristics of O157 versus non-O157 Shiga toxin-producing Escherichia coli infections in Minnesota, 2000–2006. Clin Infect Dis. 2009;49:358–64.CrossRefPubMed
65.
go back to reference Smith JL, Fratamico PM, Gunther NW. Shiga toxin-producing Escherichia coli. Adv Appl Microbiol. 2014;86:145–97.CrossRefPubMed Smith JL, Fratamico PM, Gunther NW. Shiga toxin-producing Escherichia coli. Adv Appl Microbiol. 2014;86:145–97.CrossRefPubMed
66.
go back to reference Vold L, Klungseth Johansen B, Kruse H, Skjerve E, Wasteson Y. Occurrence of shigatoxinogenic Escherichia coli O157 in Norwegian cattle herds. Epidemiol Infect. 1998;120:21–8.CrossRefPubMedPubMedCentral Vold L, Klungseth Johansen B, Kruse H, Skjerve E, Wasteson Y. Occurrence of shigatoxinogenic Escherichia coli O157 in Norwegian cattle herds. Epidemiol Infect. 1998;120:21–8.CrossRefPubMedPubMedCentral
67.
go back to reference LeJeune JT, Hancock D, Wasteson Y, Skjerve E, Urdahl AM. Comparison of E. coli O157 and Shiga toxin-encoding genes (stx) prevalence between Ohio, USA and Norwegian dairy cattle. Int J Food Microbiol. 2006;109:19–24.CrossRefPubMed LeJeune JT, Hancock D, Wasteson Y, Skjerve E, Urdahl AM. Comparison of E. coli O157 and Shiga toxin-encoding genes (stx) prevalence between Ohio, USA and Norwegian dairy cattle. Int J Food Microbiol. 2006;109:19–24.CrossRefPubMed
68.
go back to reference Urdahl AM, Beutin L, Skjerve E, Wasteson Y. Serotypes and virulence factors of Shiga toxin-producing Escherichia coli isolated from healthy Norwegian sheep. J Appl Microbiol. 2002;93:1026–33.CrossRefPubMed Urdahl AM, Beutin L, Skjerve E, Wasteson Y. Serotypes and virulence factors of Shiga toxin-producing Escherichia coli isolated from healthy Norwegian sheep. J Appl Microbiol. 2002;93:1026–33.CrossRefPubMed
70.
go back to reference Werber D, Behnke SC, Fruth A, Merle R, Menzler S, Glaser S, et al. Shiga toxin-producing Escherichia coli infection in Germany: different risk factors for different age groups. Am J Epidemiol. 2007;165:425–34.CrossRefPubMed Werber D, Behnke SC, Fruth A, Merle R, Menzler S, Glaser S, et al. Shiga toxin-producing Escherichia coli infection in Germany: different risk factors for different age groups. Am J Epidemiol. 2007;165:425–34.CrossRefPubMed
71.
go back to reference Schimmer B, Nygard K, Eriksen HM, Lassen J, Lindstedt BA, Brandal LT, et al. Outbreak of haemolytic uraemic syndrome in Norway caused by stx2-positive Escherichia coli O103:H25 traced to cured mutton sausages. BMC Infect Dis. 2008;8:41.CrossRefPubMedPubMedCentral Schimmer B, Nygard K, Eriksen HM, Lassen J, Lindstedt BA, Brandal LT, et al. Outbreak of haemolytic uraemic syndrome in Norway caused by stx2-positive Escherichia coli O103:H25 traced to cured mutton sausages. BMC Infect Dis. 2008;8:41.CrossRefPubMedPubMedCentral
72.
go back to reference Wahl E, Vold L, Lindstedt BA, Bruheim T, Afset JE. 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. 2011;11:238.CrossRefPubMedPubMedCentral Wahl E, Vold L, Lindstedt BA, Bruheim T, Afset JE. 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. 2011;11:238.CrossRefPubMedPubMedCentral
Metadata
Title
Shiga toxin-producing escherichia coli infections in Norway, 1992–2012: characterization of isolates and identification of risk factors for haemolytic uremic syndrome
Authors
Lin T. Brandal
Astrid L. Wester
Heidi Lange
Inger Løbersli
Bjørn-Arne Lindstedt
Line Vold
Georg Kapperud
Publication date
01-12-2015
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2015
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-015-1017-6

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