High rates of intestinal colonisation with fluoroquinolone-resistant ESBL-harbouring Enterobacteriaceae in hospitalised patients with antibiotic-associated diarrhoea

  • J. Vervoort
  • M. Gazin
  • M. Kazma
  • T. Kotlovsky
  • C. Lammens
  • Y. Carmeli
  • H. Goossens
  • S. Malhotra-Kumar
  • on behalf of the SATURN WP1 and MOSAR WP2 study groups


The purposes of this study were to investigate the intestinal carriage of extended-spectrum β-lactamase-harbouring Enterobacteriaceae (ESBL-EN) and associated fluoroquinolone resistance (FQ-R) in 120 hospitalised patients with antibiotic-associated diarrhoea, and to investigate a correlation between Clostridium difficile (C. difficile) infection and intestinal colonisation with ESBL-EN in these patients. Stool samples were screened for C. difficile infection by toxin A/B enzyme-linked immunosorbent assay (ELISA) and for the presence of enterobacterial isolates producing β-lactamases by plating on β-lactamase screening (BLSE) agar. Recovered isolates were confirmed pheno- and genotypically for the presence of ESBL genes (bla CTX-M, bla TEM, bla SHV) by the double-disc synergy test and polymerase chain reaction (PCR) sequencing, and tested for the presence of topoisomerase mutations (gyrA, parC) and plasmid-mediated quinolone resistance (PMQR) determinants [qnrA, qnrB, qnrS, qepA, aac(6′)-Ib-cr] by PCR sequencing. ESBL-EN were detected in 44/120 (37 %) stool samples. C. difficile-infected patients showed a significantly higher frequency of intestinal colonisation with ESBL-EN compared to C. difficile non-infected patients (62 % vs. 31 %, p = 0.008). Of the 73 ESBL-EN recovered, 46 (63 %) showed high-level FQ-R [ciprofloxacin minimum inhibitory concentration (MIC) ≥32 mg/L]. The largest group consisted of 21 bla CTX-M-15-harbouring Enterobacteriaceae (ciprofloxacin MIC ≥64 mg/L) with multiple topoisomerase mutations in gyrA and parC, in combination with co-carriage of aac(6′)-Ib-cr. Most of them were Escherichia coli isolates belonging to sequence types ST131 and ST410. We found remarkably high rates of intestinal colonisation with high-level FQ-R ESBL-EN in hospitalised patients with antibiotic-associated diarrhoea, especially among C. difficile-infected patients. These data underscore the need for stringent infection control to contain this potentially infectious and multidrug-resistant reservoir.


Stool Sample Intestinal Colonisation ESBL Gene Sequence Type ST131 PMQR Gene 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Funding and role of the funding source

This work, JV and MG are supported by funding from the European Community (MOSAR network contract LSHP-CT-2007-037941; SATURN network contract FP7-HEALTH-2009-SINGLE STAGE-N°241796). The sponsor had no role in the study design, data collection, data analysis, data interpretation or writing of the report.

Transparency declarations

None to declare.

Conflict of interest

We declare that we have no conflict of interest.

Supplementary material

10096_2014_2193_MOESM1_ESM.doc (40 kb)
ESM1 (DOC 39 kb).


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Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • J. Vervoort
    • 1
  • M. Gazin
    • 1
  • M. Kazma
    • 2
  • T. Kotlovsky
    • 2
  • C. Lammens
    • 1
  • Y. Carmeli
    • 2
  • H. Goossens
    • 1
  • S. Malhotra-Kumar
    • 1
    • 3
  • on behalf of the SATURN WP1 and MOSAR WP2 study groups
  1. 1.Department of Medical Microbiology, Vaccine & Infectious Disease InstituteUniversity of AntwerpAntwerpBelgium
  2. 2.Division of Epidemiology and Laboratory for Molecular Epidemiology and Antibiotic Research, Tel Aviv Sourasky Medical Center, Sackler Faculty of MedicineTel Aviv UniversityTel AvivIsrael
  3. 3.Department of Medical Microbiology, Campus Drie EikenUniversity of AntwerpWilrijkBelgium

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