1887
Research Open Access
Like 1

Abstract

Background

The epidemiology of carriage of extended-spectrum beta-lactamase-producing (ESBL-E) and carbapenemase-producing Enterobacteriaceae (CPE) in the general population is unknown.

Aim

In this observational study, the prevalence and risk factors for intestinal ESBL-E and CPE carriage in the Dutch general population were determined. ESBL-E were characterised.

Methods

From 2014 to 2016, ca 2,000 residents were invited monthly to complete a questionnaire and provide a faecal sample, which was tested for ESBL-E. The first 1,758 samples were also tested for CPE. Risk factors for ESBL-E carriage were identified by multivariable logistic regression analysis. ESBL-E isolates underwent whole genome sequencing.

Results

Of 47,957 individuals invited, 4,177 (8.7%) completed the questionnaire and provided a faecal sample. ESBL-E were detected in 186 (4.5%) individuals, resulting in an adjusted prevalence of 5.0% (95% confidence interval (CI):3.4–6.6%). Risk factors were: born outside the Netherlands (odds ratio (OR): 1.99; 95% CI: 1.16−4.54), eating in restaurants > 20 times/year (OR: 1.70; 95% CI: 1.04−2.76), antibiotic use < 6 months ago (OR: 2.05; 95% CI: 1.05−4.03), swimming in sea/ocean < 12 months ago (OR: 1.63; 95% CI: 1.11−2.39), travelling to Africa (OR: 3.03; 95% CI: 1.23−7.46) or Asia (OR: 2.00; 95% CI: 1.02−3.90) < 12 months ago, and not changing kitchen towels daily (OR: 2.19; 95% CI: 1.24−3.87). The last had the largest population attributable risk (PAR) (47.5%). Eighty-four of 189 (44.4%) ESBL-E isolates carried . isolates belonged to 70 different sequence types (ST)s, of which ST131 (42/178 isolates; 23.6%) was most prevalent. Associations were observed between IncFIA plasmids and ST131 and , and between IncI1 and ST88 and . No CPE were detected.

Conclusions

The prevalence of ESBL-E carriage in the Netherlands’ community-dwelling population is 5.0%. Identified risk factors were mostly travelling (particularly to Asia and Africa) and kitchen hygiene. CPE were not detected.

Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2019.24.41.1800594
2019-10-10
2019-12-06
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2019.24.41.1800594
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/24/41/eurosurv-24-41-4.html?itemId=/content/10.2807/1560-7917.ES.2019.24.41.1800594&mimeType=html&fmt=ahah

References

  1. Hordijk J, Schoormans A, Kwakernaak M, Duim B, Broens E, Dierikx C, et al. High prevalence of fecal carriage of extended spectrum β-lactamase/AmpC-producing Enterobacteriaceae in cats and dogs. Front Microbiol. 2013;4:242.  https://doi.org/10.3389/fmicb.2013.00242  PMID: 23966992 
  2. Blaak H, de Kruijf P, Hamidjaja RA, van Hoek AHAM, de Roda Husman AM, Schets FM. Hamidjaja R a, van Hoek AH a M, de Roda Husman AM, Schets FM. Prevalence and characteristics of ESBL-producing E. coli in Dutch recreational waters influenced by wastewater treatment plants. Vet Microbiol. 2014;171(3-4):448-59.  https://doi.org/10.1016/j.vetmic.2014.03.007 
  3. Blaak H, van Hoek AH, Veenman C, Docters van Leeuwen AE, Lynch G, van Overbeek WM, et al. Extended spectrum ß-lactamase- and constitutively AmpC-producing Enterobacteriaceae on fresh produce and in the agricultural environment. Int J Food Microbiol. 2014;168-169:8-16.  https://doi.org/10.1016/j.ijfoodmicro.2013.10.006  PMID: 24211774 
  4. Overdevest I, Willemsen I, Rijnsburger M, Eustace A, Xu L, Hawkey P, et al. Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, The Netherlands. Emerg Infect Dis. 2011;17(7):1216-22.  https://doi.org/10.3201/eid1707.110209  PMID: 21762575 
  5. ISISweb. ISIS-AR data. Bilthoven: RIVM. [Accessed 22 Jan 2018]. Dutch. Available from: https://www.isis-web.nl/interactieve_rapporten/bezoekvraag/
  6. Dohmen W, Bonten MJM, Bos MEH, van Marm S, Scharringa J, Wagenaar JA, et al. Carriage of extended-spectrum β-lactamases in pig farmers is associated with occurrence in pigs. Clin Microbiol Infect. 2015;21(10):917-23.  https://doi.org/10.1016/j.cmi.2015.05.032  PMID: 26033669 
  7. Paltansing S, Vlot JA, Kraakman MEM, Mesman R, Bruijning ML, Bernards AT, et al. Extended-spectrum β-lactamase-producing enterobacteriaceae among travelers from the Netherlands. Emerg Infect Dis. 2013;19(8):1206-13.  https://doi.org/10.3201/eid1908.130257  PMID: 23885972 
  8. von Wintersdorff CJH, Penders J, Stobberingh EE, Oude Lashof AM, Hoebe CJ, Savelkoul PH, et al. High rates of antimicrobial drug resistance gene acquisition after international travel, The Netherlands. Emerg Infect Dis. 2014;20(4):649-57.  https://doi.org/10.3201/eid2004.131718  PMID: 24655888 
  9. Reuland EA, Overdevest IT, Al Naiemi N, Kalpoe JS, Rijnsburger MC, Raadsen SA, et al. High prevalence of ESBL-producing Enterobacteriaceae carriage in Dutch community patients with gastrointestinal complaints. Clin Microbiol Infect. 2013;19(6):542-9.  https://doi.org/10.1111/j.1469-0691.2012.03947.x  PMID: 22757622 
  10. van den Bunt G, Liakopoulos A, Mevius DJ, Geurts Y, Fluit AC, Bonten MJ, et al. ESBL/AmpC-producing Enterobacteriaceae in households with children of preschool age: prevalence, risk factors and co-carriage. J Antimicrob Chemother. 2017;72(2):589-95.  https://doi.org/10.1093/jac/dkw443  PMID: 27789683 
  11. Reuland EA, Al Naiemi N, Kaiser AM, Heck M, Kluytmans JA, Savelkoul PH, et al. Prevalence and risk factors for carriage of ESBL-producing Enterobacteriaceae in Amsterdam. J Antimicrob Chemother. 2016;71(4):1076-82.  https://doi.org/10.1093/jac/dkv441  PMID: 26755493 
  12. Huijbers PMC, de Kraker M, Graat EA, van Hoek AH, van Santen MG, de Jong MC, et al. Prevalence of extended-spectrum β-lactamase-producing Enterobacteriaceae in humans living in municipalities with high and low broiler density. Clin Microbiol Infect. 2013;19(6):E256-9.  https://doi.org/10.1111/1469-0691.12150  PMID: 23397953 
  13. Wielders CCH, van Hoek AHAM, Hengeveld PD, Veenman C, Dierikx CM, Zomer TP, et al. Extended-spectrum β-lactamase- and pAmpC-producing Enterobacteriaceae among the general population in a livestock-dense area. Clin Microbiol Infect. 2017;23(2):120.e1-8.  https://doi.org/10.1016/j.cmi.2016.10.013  PMID: 27773759 
  14. Mughini Gras L, Smid JH, Wagenaar JA, de Boer AG, Havelaar AH, Friesema IH, et al. Risk factors for campylobacteriosis of chicken, ruminant, and environmental origin: a combined case-control and source attribution analysis. PLoS One. 2012;7(8):e42599.  https://doi.org/10.1371/journal.pone.0042599  PMID: 22880049 
  15. Doorduyn Y, Van Pelt W, Havelaar AH. The burden of infectious intestinal disease (IID) in the community: a survey of self-reported IID in The Netherlands. Epidemiol Infect. 2012;140(7):1185-92.  https://doi.org/10.1017/S0950268811001099  PMID: 21943704 
  16. Carattoli A, Bertini A, Villa L, Falbo V, Hopkins KL, Threlfall EJ. Identification of plasmids by PCR-based replicon typing. J Microbiol Methods. 2005;63(3):219-28.  https://doi.org/10.1016/j.mimet.2005.03.018  PMID: 15935499 
  17. 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(11):2640-4.  https://doi.org/10.1093/jac/dks261  PMID: 22782487 
  18. Joensen KG, Scheutz F, Lund O, Hasman H, Kaas RS, Nielsen EM, et al. Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J Clin Microbiol. 2014;52(5):1501-10.  https://doi.org/10.1128/JCM.03617-13  PMID: 24574290 
  19. Carattoli A, Zankari E, García-Fernández A, Voldby Larsen M, Lund O, Villa L, et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother. 2014;58(7):3895-903.  https://doi.org/10.1128/AAC.02412-14  PMID: 24777092 
  20. Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H, Marvig RL, et al. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol. 2012;50(4):1355-61.  https://doi.org/10.1128/JCM.06094-11  PMID: 22238442 
  21. Korndewal MJ, Mollema L, Tcherniaeva I, van der Klis F, Kroes AC, Oudesluys-Murphy AM, et al. Cytomegalovirus infection in the Netherlands: seroprevalence, risk factors, and implications. J Clin Virol. 2015;63:53-8.  https://doi.org/10.1016/j.jcv.2014.11.033  PMID: 25600606 
  22. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc. 1995;57:289-300.
  23. van Buuren S, Groothuis-oudshoorn K. mice: multivariate imputation by chained equations in R. J Stat Softw. 2011;45(3):1-67.  https://doi.org/10.18637/jss.v045.i03 
  24. Rockhill B, Newman B, Weinberg C. Use and misuse of population attributable fractions. Am J Public Health. 1998;88(1):15-9.  https://doi.org/10.2105/AJPH.88.1.15  PMID: 9584027 
  25. Dean AG, Sullivan KM, Soe MM. Open Source Epidemiologic Statistics for Public Health. Atlanta: Emory University; 2013. Available from: https://www.openepi.com/SampleSize/SSCC.htm
  26. Ny S, Löfmark S, Börjesson S, Englund S, Ringman M, Bergström J, et al. Community carriage of ESBL-producing Escherichia coli is associated with strains of low pathogenicity: a Swedish nationwide study. J Antimicrob Chemother. 2017;72(2):582-8.  https://doi.org/10.1093/jac/dkw419  PMID: 27798205 
  27. van Hoek AHAM, Schouls L, van Santen MG, Florijn A, de Greeff SC, van Duijkeren E. Molecular characteristics of extended-spectrum cephalosporin-resistant Enterobacteriaceae from humans in the community. PLoS One. 2015;10(6):e0129085.  https://doi.org/10.1371/journal.pone.0129085  PMID: 26029910 
  28. Wielders CCH, van Hoek AHAM, Hengeveld PD, Veenman C, Dierikx CM, Zomer TP, et al. Extended-spectrum β-lactamase- and pAmpC-producing Enterobacteriaceae among the general population in a livestock-dense area. Clin Microbiol Infect. 2017;23(2):120.e1-8.  https://doi.org/10.1016/j.cmi.2016.10.013  PMID: 27773759 
  29. Platteel TN, Leverstein-van Hall MA, Cohen Stuart JW, Thijsen SF, Mascini EM, van Hees BC, et al. Predicting carriage with extended-spectrum beta-lactamase-producing bacteria at hospital admission: a cross-sectional study. Clin Microbiol Infect. 2015;21(2):141-6.  https://doi.org/10.1016/j.cmi.2014.09.014  PMID: 25658554 
  30. Cassini A, Högberg LD, Plachouras D, Quattrocchi A, Hoxha A, Simonsen GS, et al. Burden of AMR Collaborative Group. Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: a population-level modelling analysis. Lancet Infect Dis. 2019;19(1):56-66.  https://doi.org/10.1016/S1473-3099(18)30605-4  PMID: 30409683 
  31. Nethmap/Maran. Nethmap/Maran 2018. 2018.
  32. European Centre for Disease Prevention and Control (ECDC). Summary of the latest data on antibiotic consumption in the European Union. Stockholm: ECDC; 2017. Available from: https://ecdc.europa.eu/en/publications-data/summary-latest-data-antibiotic-consumption-eu-2017
  33. Arcilla MS, van Hattem JM, Haverkate MR, Bootsma MCJ, van Genderen PJJ, Goorhuis A, et al. Import and spread of extended-spectrum β-lactamase-producing Enterobacteriaceae by international travellers (COMBAT study): a prospective, multicentre cohort study. Lancet Infect Dis. 2017;17(1):78-85.  https://doi.org/10.1016/S1473-3099(16)30319-X  PMID: 27751772 
  34. Reuland EA, Sonder GJB, Stolte I, Al Naiemi N, Koek A, Linde GB, et al. Travel to Asia and traveller’s diarrhoea with antibiotic treatment are independent risk factors for acquiring ciprofloxacin-resistant and extended spectrum β-lactamase-producing Enterobacteriaceae-a prospective cohort study. Clin Microbiol Infect. 2016;22(8):731.e1-7.  https://doi.org/10.1016/j.cmi.2016.05.003  PMID: 27223840 
  35. von Wintersdorff CJH, Penders J, Stobberingh EE, Oude Lashof AM, Hoebe CJ, Savelkoul PH, et al. High rates of antimicrobial drug resistance gene acquisition after international travel, The Netherlands. Emerg Infect Dis. 2014;20(4):649-57.  https://doi.org/10.3201/eid2004.131718  PMID: 24655888 
  36. Koningstein M, Leenen MA, Mughini-Gras L, Scholts RM, van Huisstede-Vlaanderen KW, Enserink R, et al. Prevalence and Risk Factors for Colonization With Extended-Spectrum Cephalosporin-Resistant Escherichia coli in Children Attending Daycare Centers: A Cohort Study in the Netherlands. J Pediatric Infect Dis Soc. 2015;4(4):e93-9. PMID: 26407274 
  37. Huizinga P, Kluytmans-van den Bergh-Kl M, van Rijen M, Willemsen I, van ’t Veer N, Kluytmans J. Proton Pump Inhibitor use is associated with Extended- Spectrum β-Lactamase–producing Enterobacteriaceae rectal carriage at hospital admission: a cross-sectional study. Clin Infect Dis. 2016;702:5-7. PMID: 27965302 
  38. Johnson JR, Johnston B, Clabots C, Kuskowski MA, Castanheira M. Escherichia coli sequence type ST131 as the major cause of serious multidrug-resistant E. coli infections in the United States. Clin Infect Dis. 2010;51(3):286-94.  https://doi.org/10.1086/653932  PMID: 20572763 
  39. McNally A, Kallonen T, Connor C, et al. Signatures of negative frequency dependent selection in colonisation factors and the evolution of a multi-drug resistant lineage of. bioRxiv. 2018.
  40. 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(8):1437-49.  https://doi.org/10.1101/gr.216606.116  PMID: 28720578 
/content/10.2807/1560-7917.ES.2019.24.41.1800594
Loading

Data & Media loading...

Supplementary data

Comment has been disabled for this content
Submit comment
Close
Comment moderation successfully completed
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