Extended-spectrum beta-lactamase (ESBL)-producing and non-ESBL-producing Escherichia coli isolates causing bacteremia in the Netherlands (2014 – 2016) differ in clonal distribution, antimicrobial resistance gene and virulence gene content


Autoři: Denise van Hout aff001;  Tess D. Verschuuren aff001;  Patricia C. J. Bruijning-Verhagen aff001;  Thijs Bosch aff002;  Anita C. Schürch aff003;  Rob J. L. Willems aff003;  Marc J. M. Bonten aff001;  Jan A. J. W. Kluytmans aff001
Působiště autorů: Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, University Utrecht, Utrecht, The Netherlands aff001;  Center for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, The Netherlands aff002;  Department of Medical Microbiology, University Medical Center Utrecht, University Utrecht, Utrecht, The Netherlands aff003;  Microvida Laboratory for Medical Microbiology and Department of Infection Control, Amphia Hospital, Breda, The Netherlands aff004
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0227604

Souhrn

Background

Knowledge on the molecular epidemiology of Escherichia coli causing E. coli bacteremia (ECB) in the Netherlands is mostly based on extended-spectrum beta-lactamase-producing E. coli (ESBL-Ec). We determined differences in clonality and resistance and virulence gene (VG) content between non-ESBL-producing E. coli (non-ESBL-Ec) and ESBL-Ec isolates from ECB episodes with different epidemiological characteristics.

Methods

A random selection of non-ESBL-Ec isolates as well as all available ESBL-Ec blood isolates was obtained from two Dutch hospitals between 2014 and 2016. Whole genome sequencing was performed to infer sequence types (STs), serotypes, acquired antibiotic resistance genes and VG scores, based on presence of 49 predefined putative pathogenic VG.

Results

ST73 was most prevalent among the 212 non-ESBL-Ec (N = 26, 12.3%) and ST131 among the 69 ESBL-Ec (N = 30, 43.5%). Prevalence of ST131 among non-ESBL-Ec was 10.4% (N = 22, P value < .001 compared to ESBL-Ec). O25:H4 was the most common serotype in both non-ESBL-Ec and ESBL-Ec. Median acquired resistance gene counts were 1 (IQR 1–6) and 7 (IQR 4–9) for non-ESBL-Ec and ESBL-Ec, respectively (P value < .001). Among non-ESBL-Ec, acquired resistance gene count was highest among blood isolates from a primary gastro-intestinal focus (median 4, IQR 1–8). Median VG scores were 13 (IQR 9–20) and 12 (IQR 8–14) for non-ESBL-Ec and ESBL-Ec, respectively (P value = .002). VG scores among non-ESBL-Ec from a primary urinary focus (median 15, IQR 11–21) were higher compared to non-ESBL-Ec from a primary gastro-intestinal (median 10, IQR 5–13) or hepatic-biliary focus (median 11, IQR 5–18) (P values = .007 and .04, respectively). VG content varied between different E. coli STs.

Conclusions

Non-ESBL-Ec and ESBL-Ec blood isolates from two Dutch hospitals differed in clonal distribution, resistance gene and VG content. Also, resistance gene and VG content differed between non-ESBL-Ec from different primary foci of ECB.

Klíčová slova:

Antimicrobial resistance – Bacteremia – Blood – Blood counts – Escherichia coli – Genetic epidemiology – Netherlands – Vaccines


Zdroje

1. Abernethy JK, Johnson AP, Guy R, Hinton N, Sheridan EA, Hope RJ. Thirty day all-cause mortality in patients with Escherichia coli bacteraemia in England. Clin Microbiol Infect. 2015;21: 251.e1–8. doi: 10.1016/j.cmi.2015.01.001 25698659

2. Fitzpatrick JM, Biswas JS, Edgeworth JD, Islam J, Jenkins N, Judge R, et al. Gram-negative bacteraemia; a multi-centre prospective evaluation of empiric antibiotic therapy and outcome in English acute hospitals. Clin Microbiol Infect. 2016;22: 244–251. doi: 10.1016/j.cmi.2015.10.034 26577143

3. Vihta K-D, Stoesser N, Llewelyn MJ, Quan TP, Davies T, Fawcett NJ, et al. Trends over time in Escherichia coli bloodstream infections, urinary tract infections, and antibiotic susceptibilities in Oxfordshire, UK, 1998–2016: a study of electronic health records. Lancet Infect Dis. 2018;18: 1138–1149. doi: 10.1016/S1473-3099(18)30353-0 30126643

4. de Kraker MEA, Jarlier V, Monen JCM, Heuer OE, van de Sande N, Grundmann H. The changing epidemiology of bacteraemias in Europe: trends from the European Antimicrobial Resistance Surveillance System. Clin Microbiol Infect. 2013;19: 860–868. doi: 10.1111/1469-0691.12028 23039210

5. Van Der Steen M, Leenstra T, Kluytmans JAJW, Van Der Bij AK. Trends in expanded-spectrum cephalosporin-resistant Escherichia coli and Klebsiella pneumoniae among Dutch clinical isolates, from 2008 to 2012. PLoS One. 2015;10: e0138088. doi: 10.1371/journal.pone.0138088 26381746

6. Schlackow I, Stoesser N, Walker AS, Crook DW, Peto TEA, Wyllie DH. Increasing incidence of Escherichia coli bacteraemia is driven by an increase in antibiotic-resistant isolates: electronic database study in Oxfordshire 1999–2011. J Antimicrob Chemother. 2012;67: 1514–1524. doi: 10.1093/jac/dks082 22438437

7. Abernethy J, Guy R, Sheridan EA, Hopkins S, Kiernan M, Wilcox MH, et al. Epidemiology of Escherichia coli bacteraemia in England: results of an enhanced sentinel surveillance programme. J Hosp Infect. 2017;95: 365–375. doi: 10.1016/j.jhin.2016.12.008 28190700

8. Huttner A, Hatz C, van den Dobbelsteen G, Abbanat D, Hornacek A, Frolich R, et al. Safety, immunogenicity, and preliminary clinical efficacy of a vaccine against extraintestinal pathogenic Escherichia coli in women with a history of recurrent urinary tract infection: a randomised, single-blind, placebo-controlled phase 1b trial. Lancet Infect Dis. 2017;17: 528–537. doi: 10.1016/S1473-3099(17)30108-1 28238601

9. Overdevest ITMA, Bergmans AMC, Verweij JJ, Vissers J, Bax N, Snelders E, et al. Prevalence of phylogroups and O25/ST131 in susceptible and extended-spectrum β-lactamase-producing Escherichia coli isolates, the Netherlands. Clin Microbiol Infect. 2015;21: 570.e1-e4. doi: 10.1016/j.cmi.2015.02.020 25749563

10. Van Der Bij AK, Peirano G, Goessens WHF, Van Der Vorm ER, Van Westreenen M, Pitout JDD. Clinical and molecular characteristics of extended-spectrum-β-lactamase-producing Escherichia coli causing bacteremia in the Rotterdam Area, Netherlands. Antimicrob Agents Chemother. 2011;55: 3576–3578. doi: 10.1128/AAC.00074-11 21502612

11. van Hout D, Verschuuren TD., Bruijning-Verhagen PCJ., Bosch T., Reuland EA., Fluit AC., et al. Design of the EPIGENEC Study: Assessing the EPIdemiology and GENetics of Escherichia coli in the Netherlands. Preprints. 2019; 2019020066. doi:10.20944/preprints201902.0066.v1

12. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013;29: 1072–1075. doi: 10.1093/bioinformatics/btt086 23422339

13. Simpson EH. Measurement of diversity. Nature. 1949;163.

14. Joensen KG, Tetzschner AMM, Iguchi A, Aarestrup FM, Scheutz F. Rapid and Easy In Silico Serotyping of Escherichia coli Isolates by Use of Whole-Genome Sequencing Data. J Clin Microbiol. 2015;53: 2410–2426. doi: 10.1128/JCM.00008-15 25972421

15. Geurtsen J, Weerdenburg E, Davies T, Go O, Spiessens B, Geet G Van, et al. Extraintestinal pathogenic Escherichia coli surveillance study to determine O-serotype prevalence and antibiotic resistance in blood isolates collected in Europe, 2011–2017. ECCMID Conf #P1451.

16. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother. 2012;67: 2640–2644. doi: 10.1093/jac/dks261 22782487

17. Liu B, Zheng D, Jin Q, Chen L, Yang J. VFDB 2019: a comparative pathogenomic platform with an interactive web interface. Nucleic Acids Res. 2019;47: D687–D692. doi: 10.1093/nar/gky1080 30395255

18. Johnson JR, Stell AL. Extended Virulence Genotypes of Escherichia coli Strains from Patients with Urosepsis in Relation to Phylogeny and Host Compromise. J Infect Dis. 2000;181: 261–72. doi: 10.1086/315217 10608775

19. Johnson JR, Johnston BD, Porter S, Thuras P, Aziz M, Price LB. Accessory Traits and Phylogenetic Background Predict Escherichia coli Extraintestinal Virulence Better Than Does Ecological Source. J Infect Dis. 2019;219: 121–132. doi: 10.1093/infdis/jiy459 30085181

20. Johnson JR, Porter S, Johnston B, Kuskowski MA, Spurbeck RR, Mobley HLT, et al. Host Characteristics and Bacterial Traits Predict Experimental Virulence for Escherichia coli Bloodstream Isolates From Patients With Urosepsis. Open Forum Infect Dis. 2015;2: ofv083. doi: 10.1093/ofid/ofv083 26199950

21. Dale AP, Woodford N. Extra-intestinal pathogenic Escherichia coli (ExPEC): Disease, carriage and clones. J Infect. 2015;71: 615–626. doi: 10.1016/j.jinf.2015.09.009 26409905

22. Dale AP, Pandey AK, Hesp RJ, Belogiannis K, Laver JR, Shone CC, et al. Genomes of Escherichia coli bacteraemia isolates originating from urinary tract foci contain more virulence-associated genes than those from non-urinary foci and neutropaenic hosts. J Infect. 2018;77: 534–543. doi: 10.1016/j.jinf.2018.10.011 30391630

23. Leimbach A. ecoli_VF_collection: V.0.1. Zenodo. 2016. Available: https://doi.org/10.5281/zenodo.56686

24. Frenck RW, Ervin J, Chu L, Abbanat D, Spiessens B, Go O, et al. Safety and immunogenicity of a vaccine for extra-intestinal pathogenic Escherichia coli (ESTELLA): a phase 2 randomised controlled trial. Lancet Infect Dis. 2019;19: 631–640. doi: 10.1016/S1473-3099(18)30803-X 31079947

25. Mathers AJ, Peirano G, Pitout JDD. The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant Enterobacteriaceae. Clin Microbiol Rev. 2015;28: 565–591. doi: 10.1128/CMR.00116-14 25926236

26. Hertz FB, Nielsen JB, Schonning K, Littauer P, Knudsen JD, Lobner-Olesen A, et al. “Population structure of drug-susceptible,-resistant and ESBL-producing Escherichia coli from community-acquired urinary tract”. BMC Microbiol. 2016;16: 63. doi: 10.1186/s12866-016-0681-z 27067536

27. Manges AR, Geum HM, Guo A, Edens TJ, Fibke CD, Pitout JDD. Global Extraintestinal Pathogenic Escherichia coli (ExPEC) Lineages. Clin Microbiol Rev. 2019;32. doi: 10.1128/CMR.00135-18 31189557

28. Kallonen T, Brodrick HJ, Harris SR, Corander J, Brown NM, Martin V, et al. Systematic longitudinal survey of invasive Escherichia coli in England demonstrates a stable population structure only transiently disturbed by the emergence of ST131. Genome Res. 2017;27: 1437–1449. doi: 10.1101/gr.216606.116 28720578

29. Nicolas-Chanoine M-H, Bertrand X, Madec J-Y. Escherichia coli ST131, an intriguing clonal group. Clin Microbiol Rev. 2014;27: 543–574. doi: 10.1128/CMR.00125-13 24982321

30. Alhashash F, Wang X, Paszkiewicz K, Diggle M, Zong Z, McNally A. Increase in bacteraemia cases in the East Midlands region of the UK due to MDR Escherichia coli ST73: high levels of genomic and plasmid diversity in causative isolates. J Antimicrob Chemother. 2015;71: 339–343. doi: 10.1093/jac/dkv365 26518049

31. McNally A, Oren Y, Kelly D, Pascoe B, Dunn S, Sreecharan T, et al. Combined Analysis of Variation in Core, Accessory and Regulatory Genome Regions Provides a Super-Resolution View into the Evolution of Bacterial Populations. PLoS Genet. 2016;12: e1006280. doi: 10.1371/journal.pgen.1006280 27618184

32. McNally A, Kallonen T, Connor C, Abudahab K, Aanensen DM, Horner C, et al. Diversification of Colonization Factors in a Multidrug-Resistant Escherichia coli Lineage Evolving under Negative Frequency-Dependent Selection. MBio. 2019;10: e00644–19. doi: 10.1128/mBio.00644-19 31015329

33. Dunn SJ, Connor C, McNally A. The evolution and transmission of multi-drug resistant Escherichia coli and Klebsiella pneumoniae: the complexity of clones and plasmids. Curr Opin Microbiol. 2019;51: 51–56. doi: 10.1016/j.mib.2019.06.004 31325664

34. Goswami C, Fox S, Holden M, Connor M, Leanord A, Evans TJ. Genetic analysis of invasive Escherichia coli in Scotland reveals determinants of healthcare-associated versus community-acquired infections. Microb genomics. 2018;4. doi: 10.1099/mgen.0.000190 29932391

35. Velasco M, Horcajada JP, Mensa J, Moreno-Martinez A, Vila J, Martinez JA, et al. Decreased invasive capacity of quinolone-resistant Escherichia coli in patients with urinary tract infections. Clin Infect Dis. 2001;33: 1682–1686. doi: 10.1086/323810 11595990

36. Vila J, Simon K, Ruiz J, Horcajada JP, Velasco M, Barranco M, et al. Are quinolone-resistant uropathogenic Escherichia coli less virulent? J Infect Dis. 2002;186: 1039–1042. doi: 10.1086/342955 12232848

37. Johnson JR, van der Schee C, Kuskowski MA, Goessens W, van Belkum A. Phylogenetic background and virulence profiles of fluoroquinolone-resistant clinical Escherichia coli isolates from the Netherlands. J Infect Dis. 2002;186: 1852–1856. doi: 10.1086/345767 12447775

38. Johnson JR, Kuskowski MA, Owens K, Gajewski A, Winokur PL. Phylogenetic origin and virulence genotype in relation to resistance to fluoroquinolones and/or extended-spectrum cephalosporins and cephamycins among Escherichia coli isolates from animals and humans. J Infect Dis. 2003;188: 759–768. doi: 10.1086/377455 12934193

39. Horcajada JP, Soto S, Gajewski A, Smithson A, Jiménez de Anta MT, Mensa J, et al. Quinolone-resistant uropathogenic Escherichia coli strains from phylogenetic group B2 have fewer virulence factors than their susceptible counterparts. J Clin Microbiol. 2005;43: 2962–2964. doi: 10.1128/JCM.43.6.2962-2964.2005 15956432

40. Moreno E, Prats G, Sabaté M, Pérez T, Johnson JR, Andreu A. Quinolone, fluoroquinolone and trimethoprim/sulfamethoxazole resistance in relation to virulence determinants and phylogenetic background among uropathogenic Escherichia coli. J Antimicrob Chemother. 2006;57: 204–211. doi: 10.1093/jac/dki468 16390858

41. Johnson JR, Porter S, Thuras P, Castanheira M. Epidemic Emergence in the United States of Escherichia coli Sequence Type 131-H30 (ST131-H30), 2000 to 2009. Antimicrob Agents Chemother. 2017;61: e00732–17. doi: 10.1128/AAC.00732-17 28533233

42. Johnson JR, Porter S, Thuras P, Castanheira M. The Pandemic H30 Subclone of Sequence Type 131 (ST131) as the Leading Cause of Multidrug-Resistant Escherichia coli Infections in the United States (2011–2012). Open forum Infect Dis. 2017;4: ofx089–ofx089. doi: 10.1093/ofid/ofx089 28638846

43. Johnson JR, Russo TA. Molecular Epidemiology of Extraintestinal Pathogenic Escherichia coli. EcoSal Plus. 2018;8: doi: 10.1128/ecosalplus.ESP-0004–2017

44. Ciesielczuk H, Jenkins C, Chattaway M, Doumith M, Hope R, Woodford N, et al. Trends in ExPEC serogroups in the UK and their significance. Eur J Clin Microbiol Infect Dis. 2016;35: 1661–1666. doi: 10.1007/s10096-016-2707-8 27329302


Článek vyšel v časopise

PLOS One


2020 Číslo 1