1887

Journal of Medical Microbiology logo

Volume 70, Issue 12

Prevalence of genotypic antimicrobial resistance in clinical Shiga toxin-producing in Norway, 2018 to 2020 Open Access

Abstract

Shiga toxin-producing (STEC) can cause severe to fatal disease in humans. Antimicrobial treatment is sometimes necessary, but contraindicated due to undesirable clinical outcome. However, recent studies have shown promising outcomes following antimicrobial treatment. Before the establishment of a possible antimicrobial treatment strategy for STEC infections, the prevalence of antimicrobial resistance in STEC needs to be determined.

The resistance status of Norwegian clinical STEC is not known and should be assessed.

We aim to characterize genotypic antimicrobial resistance determinants in clinical STEC in Norway, and determine the prevalence of genotypic resistance in order to inform possible antimicrobial treatment options for STEC infections.

We included all clinical STEC submitted to the Norwegian Reference Laboratory from March 2018 to April 2020. All samples were whole-genome sequenced and screened for genotypic antimicrobial resistance,virulence determinants and plasmid incompatibility groups. We performed phylogenetic clustering of STEC by core-genome multi-locus sequence typing, and statistical association analyses between isolate characteristics and genotypic resistance.

A total of 459 STEC were analysed. For 385 (83.9 %) STEC we did not identify any antimicrobial resistance determinants. Seventy-four STEC (16.1 %) harboured antimicrobial resistance determinants against one or more antimicrobial classes. The most frequent genotypic resistance was identified against aminoglycosides (10.5 %). Thirty-nine STEC (8.5 %) had a multi-drug resistance (MDR) genotype. Genotypic resistance was more prevalent in non-O157 than O157 STEC (=0.02). A positive association was seen between genotypic resistance and the low-virulent STEC O117:H7 phylogenetic cluster (no. 14) (<0.001). Genotypic resistance was not significantly associated to high-virulent STEC. STEC O146:H28 and isolates harbouring the plasmid replicon type IncQ1 were positively associated with MDR.

The overall prevalence of genotypic resistance in clinical STEC in Norway is low (16.1 %). Genotypic resistance is more prevalent in non-O157 strains compared to O157 strains, and not significantly associated to high-virulent STEC. Resistance to antimicrobials suggested for treatment, especially azithromycin is low and may present an empiric treatment alternative for severe STEC infections.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): antimicrobial treatment , antimicrobials , genotypic resistance determinants , Shiga toxin-producing Escherichia coli and whole-genome sequencing
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001454
2021-12-06
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/jmm/70/12/jmm001454.html?itemId=/content/journal/jmm/10.1099/jmm.0.001454&mimeType=html&fmt=ahah

References

  1. Karch H, Tarr PI, Bielaszewska M. Enterohaemorrhagic Escherichia coli in human medicine. Int J Med Microbiol 2005; 295:405–418 [View Article] [PubMed]
     [Google Scholar]
  2. Mayer CL, Leibowitz CS, Kurosawa S, Stearns-Kurosawa DJ. Shiga toxins and the pathophysiology of hemolytic uremic syndrome in humans and animals. Toxins (Basel) 2012; 4:1261–1287 [View Article] [PubMed]
     [Google Scholar]
  3. Bruyand M, Mariani-Kurkdjian P, Gouali M, de Valk H, King LA et al. Hemolytic uremic syndrome due to Shiga toxin-producing Escherichia coli infection. Med Mal Infect 2018; 48:167–174 [View Article] [PubMed]
     [Google Scholar]
  4. Kim J-S, Lee M-S, Kim JH. Recent updates on outbreaks of shiga toxin-producing Escherichia coli and its potential reservoirs. Front Cell Infect Microbiol 2020; 10:273 [View Article] [PubMed]
     [Google Scholar]
  5. European Food Safety Authority, European Centre for Disease Prevention Control The European Union One Health 2018 Zoonoses Report. Report No.: 1831-4732 Contract No.: 12; 2019
  6. Wong CS, Jelacic S, Habeeb RL, Watkins SL, Tarr PI. The risk of the hemolytic-uremic syndrome after antibiotic treatment of Escherichia coli O157:H7 infections. N Engl J Med 2000; 342:1930–1936 [View Article] [PubMed]
     [Google Scholar]
  7. Smith KE, Wilker PR, Reiter PL, Hedican EB, Bender JB et al. Antibiotic treatment of Escherichia coli O157 infection and the risk of hemolytic uremic syndrome, Minnesota. Pediatr Infect Dis J 2012; 31:37–41 [View Article] [PubMed]
     [Google Scholar]
  8. Menne J, Nitschke M, Stingele R, Abu-Tair M, Beneke J et al. Validation of treatment strategies for enterohaemorrhagic Escherichia coli O104:H4 induced haemolytic uraemic syndrome: case-control study. BMJ 2012e4565 [PubMed]
     [Google Scholar]
  9. Geerdes-Fenge HF, Löbermann M, Nürnberg M, Fritzsche C, Koball S et al. Ciprofloxacin reduces the risk of hemolytic uremic syndrome in patients with Escherichia coli O104:H4-associated diarrhea. Infection 2013; 41:669–673 [View Article] [PubMed]
     [Google Scholar]
  10. Agger M, Scheutz F, Villumsen S, Mølbak K, Petersen AM. Antibiotic treatment of verocytotoxin-producing Escherichia coli (VTEC) infection: a systematic review and a proposal. J Antimicrob Chemother 2015; 70:2440–2446 [View Article] [PubMed]
     [Google Scholar]
  11. Nitschke M, Sayk F, Härtel C, Roseland RT, Hauswaldt S et al. Association between azithromycin therapy and duration of bacterial shedding among patients with Shiga toxin-producing enteroaggregative Escherichia coli O104:H4. JAMA 2012; 307:1046–1052 [View Article] [PubMed]
     [Google Scholar]
  12. Kakoullis L, Papachristodoulou E, Chra P, Panos G. Shiga toxin-induced haemolytic uraemic syndrome and the role of antibiotics: a global overview. J Infect 2019; 79:75–94 [View Article] [PubMed]
     [Google Scholar]
  13. Tajiri H, Nishi J, Ushijima K, Shimizu T, Ishige T et al. A role for fosfomycin treatment in children for prevention of haemolytic-uraemic syndrome accompanying Shiga toxin-producing Escherichia coli infection. Int J Antimicrob Agents 2015; 46:586–589 [View Article] [PubMed]
     [Google Scholar]
  14. Bielaszewska M, Idelevich EA, Zhang W, Bauwens A, Schaumburg F et al. Effects of antibiotics on Shiga toxin 2 production and bacteriophage induction by epidemic Escherichia coli O104:H4 strain. Antimicrob Agents Chemother 2012; 56:3277–3282 [View Article] [PubMed]
     [Google Scholar]
  15. Corogeanu D, Willmes R, Wolke M, Plum G, Utermöhlen O et al. Therapeutic concentrations of antibiotics inhibit Shiga toxin release from enterohemorrhagic E. coli O104:H4 from the 2011 German outbreak. BMC Microbiol 2012; 12:160 [View Article] [PubMed]
     [Google Scholar]
  16. Ramstad SN, Taxt AM, Naseer U, Wasteson Y, Bjørnholt JV et al. Effects of antimicrobials on Shiga toxin production in high-virulent Shiga toxin-producing Escherichia coli. Microb Pathog 2021; 152:104636 [View Article] [PubMed]
     [Google Scholar]
  17. Mir RA, Kudva IT. Antibiotic-resistant Shiga toxin-producing Escherichia coli: An overview of prevalence and intervention strategies. Zoonoses Public Health 2019; 66:1–13 [View Article] [PubMed]
     [Google Scholar]
  18. Gentle A, Day MR, Hopkins KL, Godbole G, Jenkins C. Antimicrobial resistance in Shiga toxin-producing Escherichia coli other than serotype O157 : H7 in England, 2014-2016. J Med Microbiol 2020; 69:379–386 [View Article] [PubMed]
     [Google Scholar]
  19. Mukherjee S, Mosci RE, Anderson CM, Snyder BA, Collins J et al. Antimicrobial drug–resistant shiga toxin–producing Escherichia coli Infections, Michigan, USA. Emerg Infect Dis 2017; 23:1609–1611 [View Article]
     [Google Scholar]
  20. Buvens G, Bogaerts P, Glupczynski Y, Lauwers S, Piérard D. Antimicrobial resistance testing of verocytotoxin-producing Escherichia coli and first description of TEM-52 extended-spectrum β-lactamase in serogroup O26. Antimicrob Agents Chemother 2010; 54:4907–4909 [View Article] [PubMed]
     [Google Scholar]
  21. Schroeder CM, Zhao C, DebRoy C, Torcolini J, Zhao S et al. Antimicrobial resistance of Escherichia coli O157 isolated from humans, cattle, swine, and food. Appl Environ Microbiol 2002; 68:576–581 [View Article] [PubMed]
     [Google Scholar]
  22. Hendriksen RS, Bortolaia V, Tate H, Tyson GH, Aarestrup FM et al. Using genomics to track global antimicrobial resistance. Front Public Health 2019; 7:242 [View Article] [PubMed]
     [Google Scholar]
  23. World Health Organization GLASS whole-genome sequencing for surveillance of antimicrobial resistance. Geneva: World Health Organization; 2020
  24. Pan Y, Hu B, Bai X, Yang X, Cao L et al. Antimicrobial resistance of Non-O157 shiga toxin-producing Escherichia coli isolated from humans and domestic animals. Antibiotics (Basel) 2021; 10:74 [View Article] [PubMed]
     [Google Scholar]
  25. Day M, Doumith M, Jenkins C, Dallman TJ, Hopkins KL et al. Antimicrobial resistance in Shiga toxin-producing Escherichia coli serogroups O157 and O26 isolated from human cases of diarrhoeal disease in England, 2015. J Antimicrob Chemother 2017; 72:145–152 [View Article] [PubMed]
     [Google Scholar]
  26. Jenssen GR, Veneti L, Lange H, Vold L, Naseer U et al. Implementation of multiplex PCR diagnostics for gastrointestinal pathogens linked to increase of notified Shiga toxin-producing Escherichia coli cases in Norway, 2007-2017. Eur J Clin Microbiol Infect Dis 2019; 38:801–809 [View Article] [PubMed]
     [Google Scholar]
  27. Norwegian Institute of Public Health E. coli-enteritt (inkludert EHEC-infeksjon og HUS) - veileder for helsepersonell; 2021 https://www.fhi.no/nettpub/smittevernveilederen/sykdommer-a-a/e.-coli-enteritt-inkludert-ehec-inf/
  28. Thomsen MCF, Ahrenfeldt J, Cisneros JLB, Jurtz V, Larsen MV et al. A bacterial analysis platform: an integrated system for analysing bacterial whole genome sequencing data for clinical diagnostics and surveillance. PLoS One 2016; 11:e0157718 [View Article]
     [Google Scholar]
  29. Magiorakos A-P, Srinivasan A, Carey RB, Carmeli Y, Falagas ME et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012; 18:268–281 [View Article] [PubMed]
     [Google Scholar]
  30. Li G-L, Duo L-B, Luan Y, Wang C-Y, Wang W-P et al. Identification of genotypes of plasmid-encoded AmpC beta-lactamases from clinical isolates and characterization of mutations in their promoter and attenuator regions. Gene Expr 2012; 15:215–223 [View Article] [PubMed]
     [Google Scholar]
  31. NORM/NORM-VET 2019 Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromsø / Oslo 2020. Report No.: ISSN: 1502-2307 (print) / 1890-9965 2020
     [Google Scholar]
  32. Gulesen R, Levent B, Demir T, Akgeyik M, Kuran S. Characterization of shiga toxin-producing Escherichia coli isolated from humans between 2011 and 2014. Jpn J Infect Dis 2016; 69:390–394 [View Article] [PubMed]
     [Google Scholar]
  33. Baker KS, Dallman TJ, Thomson NR, Jenkins C. An outbreak of a rare Shiga-toxin-producing Escherichia coli serotype (O117:H7) among men who have sex with men. Microb Genom 2018; 4: [View Article]
     [Google Scholar]
  34. Soysal N, Mariani-Kurkdjian P, Smail Y, Liguori S, Gouali M et al. Enterohemorrhagic Escherichia coli hybrid pathotype O80:H2 as a new therapeutic challenge. Emerg Infect Dis 2016; 22:1604–1612 [View Article] [PubMed]
     [Google Scholar]
  35. Nüesch-Inderbinen M, Cernela N, Wüthrich D, Egli A, Stephan R. Genetic characterization of Shiga toxin producing Escherichia coli belonging to the emerging hybrid pathotype O80:H2 isolated from humans 2010-2017 in Switzerland. Int J Med Microbiol 2018; 308:534–538 [PubMed]
     [Google Scholar]
  36. Gigliucci F, van Hoek AHAM, Chiani P, Knijn A, Minelli F et al. Genomic characterization of hlyF-positive shiga toxin-producing Escherichia coli, Italy and the Netherlands, 2000-2019. Emerg Infect Dis 2021; 27:853–861 [View Article] [PubMed]
     [Google Scholar]
  37. Jensen C, Schiellerup P, Olsen K, Scheutz F, Petersen E et al. Antimicrobial treatment of asymptomatic carriers of verocytotoxin-producing Escherichia coli: An empiric study. Scand J Infect Dis 2005; 37:61–63 [View Article] [PubMed]
     [Google Scholar]
  38. Villa L, García-Fernández A, Fortini D, Carattoli A. Replicon sequence typing of IncF plasmids carrying virulence and resistance determinants. J Antimicrob Chemother 2010; 65:2518–2529 [View Article] [PubMed]
     [Google Scholar]
  39. Loftie-Eaton W, Rawlings DE. Diversity, biology and evolution of IncQ-family plasmids. Plasmid 2012; 67:15–34 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001454
Loading
Prevalence of genotypic antimicrobial resistance in clinical Shiga toxin-producing Escherichia coli in Norway, 2018 to 2020
J. Med. Microbiol. 70, 001454 (2021); https://doi.org/10.1099/jmm.0.001454
/content/journal/jmm/10.1099/jmm.0.001454
/content/journal/jmm/10.1099/jmm.0.001454
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error