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Published in: European Journal of Clinical Microbiology & Infectious Diseases 12/2014

01-12-2014 | Article

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

Authors: 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

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 12/2014

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Abstract

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.
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Literature
1.
go back to reference Pitout JD, Laupland KB (2008) Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis 8(3):159–166CrossRefPubMed Pitout JD, Laupland KB (2008) Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis 8(3):159–166CrossRefPubMed
2.
3.
go back to reference Vervoort J, Baraniak A, Gazin M, Sabirova J, Lammens C, Kazma M, Grabowska A, Izdebski R, Carmeli Y, Kumar-Singh S, Gniadkowski M, Goossens H, Malhotra-Kumar S (2012) Characterization of two new CTX-M-25-group extended-spectrum beta-lactamase variants identified in Escherichia coli isolates from Israel. PLoS One 7(9):e46329CrossRefPubMedPubMedCentral Vervoort J, Baraniak A, Gazin M, Sabirova J, Lammens C, Kazma M, Grabowska A, Izdebski R, Carmeli Y, Kumar-Singh S, Gniadkowski M, Goossens H, Malhotra-Kumar S (2012) Characterization of two new CTX-M-25-group extended-spectrum beta-lactamase variants identified in Escherichia coli isolates from Israel. PLoS One 7(9):e46329CrossRefPubMedPubMedCentral
4.
go back to reference Robicsek A, Jacoby GA, Hooper DC (2006) The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect Dis 6(10):629–640CrossRefPubMed Robicsek A, Jacoby GA, Hooper DC (2006) The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect Dis 6(10):629–640CrossRefPubMed
5.
go back to reference Bartlett JG, Chang TW, Gurwith M, Gorbach SL, Onderdonk AB (1978) Antibiotic-associated pseudomembranous colitis due to toxin-producing clostridia. N Engl J Med 298(10):531–534CrossRefPubMed Bartlett JG, Chang TW, Gurwith M, Gorbach SL, Onderdonk AB (1978) Antibiotic-associated pseudomembranous colitis due to toxin-producing clostridia. N Engl J Med 298(10):531–534CrossRefPubMed
6.
go back to reference Gazin M, Paasch F, Goossens H, Malhotra-Kumar S (2012) Current trends in culture-based and molecular detection of extended-spectrum-beta-lactamase-harboring and carbapenem-resistant Enterobacteriaceae. J Clin Microbiol 50(4):1140–1146CrossRefPubMedPubMedCentral Gazin M, Paasch F, Goossens H, Malhotra-Kumar S (2012) Current trends in culture-based and molecular detection of extended-spectrum-beta-lactamase-harboring and carbapenem-resistant Enterobacteriaceae. J Clin Microbiol 50(4):1140–1146CrossRefPubMedPubMedCentral
7.
go back to reference Drieux L, Brossier F, Sougakoff W, Jarlier V (2008) Phenotypic detection of extended-spectrum beta-lactamase production in Enterobacteriaceae: review and bench guide. Clin Microbiol Infect 14(Suppl 1):90–103CrossRefPubMed Drieux L, Brossier F, Sougakoff W, Jarlier V (2008) Phenotypic detection of extended-spectrum beta-lactamase production in Enterobacteriaceae: review and bench guide. Clin Microbiol Infect 14(Suppl 1):90–103CrossRefPubMed
8.
go back to reference Malhotra-Kumar S, Wang S, Lammens C, Chapelle S, Goossens H (2003) Bacitracin-resistant clone of Streptococcus pyogenes isolated from pharyngitis patients in Belgium. J Clin Microbiol 41(11):5282–5284CrossRefPubMedPubMedCentral Malhotra-Kumar S, Wang S, Lammens C, Chapelle S, Goossens H (2003) Bacitracin-resistant clone of Streptococcus pyogenes isolated from pharyngitis patients in Belgium. J Clin Microbiol 41(11):5282–5284CrossRefPubMedPubMedCentral
9.
go back to reference Boyd DA, Tyler S, Christianson S, McGeer A, Muller MP, Willey BM, Bryce E, Gardam M, Nordmann P, Mulvey MR (2004) Complete nucleotide sequence of a 92-kilobase plasmid harboring the CTX-M-15 extended-spectrum beta-lactamase involved in an outbreak in long-term-care facilities in Toronto, Canada. Antimicrob Agents Chemother 48(10):3758–3764CrossRefPubMedPubMedCentral Boyd DA, Tyler S, Christianson S, McGeer A, Muller MP, Willey BM, Bryce E, Gardam M, Nordmann P, Mulvey MR (2004) Complete nucleotide sequence of a 92-kilobase plasmid harboring the CTX-M-15 extended-spectrum beta-lactamase involved in an outbreak in long-term-care facilities in Toronto, Canada. Antimicrob Agents Chemother 48(10):3758–3764CrossRefPubMedPubMedCentral
10.
go back to reference Mabilat C, Goussard S, Sougakoff W, Spencer RC, Courvalin P (1990) Direct sequencing of the amplified structural gene and promoter for the extended-broad-spectrum beta-lactamase TEM-9 (RHH-1) of Klebsiella pneumoniae. Plasmid 23(1):27–34CrossRefPubMed Mabilat C, Goussard S, Sougakoff W, Spencer RC, Courvalin P (1990) Direct sequencing of the amplified structural gene and promoter for the extended-broad-spectrum beta-lactamase TEM-9 (RHH-1) of Klebsiella pneumoniae. Plasmid 23(1):27–34CrossRefPubMed
11.
go back to reference Paterson DL, Hujer KM, Hujer AM, Yeiser B, Bonomo MD, Rice LB, Bonomo RA (2003) Extended-spectrum beta-lactamases in Klebsiella pneumoniae bloodstream isolates from seven countries: dominance and widespread prevalence of SHV- and CTX-M-type beta-lactamases. Antimicrob Agents Chemother 47(11):3554–3560CrossRefPubMedPubMedCentral Paterson DL, Hujer KM, Hujer AM, Yeiser B, Bonomo MD, Rice LB, Bonomo RA (2003) Extended-spectrum beta-lactamases in Klebsiella pneumoniae bloodstream isolates from seven countries: dominance and widespread prevalence of SHV- and CTX-M-type beta-lactamases. Antimicrob Agents Chemother 47(11):3554–3560CrossRefPubMedPubMedCentral
12.
go back to reference Chmelnitsky I, Carmeli Y, Leavitt A, Schwaber MJ, Navon-Venezia S (2005) CTX-M-2 and a new CTX-M-39 enzyme are the major extended-spectrum beta-lactamases in multiple Escherichia coli clones isolated in Tel Aviv, Israel. Antimicrob Agents Chemother 49(11):4745–4750CrossRefPubMedPubMedCentral Chmelnitsky I, Carmeli Y, Leavitt A, Schwaber MJ, Navon-Venezia S (2005) CTX-M-2 and a new CTX-M-39 enzyme are the major extended-spectrum beta-lactamases in multiple Escherichia coli clones isolated in Tel Aviv, Israel. Antimicrob Agents Chemother 49(11):4745–4750CrossRefPubMedPubMedCentral
13.
go back to reference Jeong SH, Bae IK, Kwon SB, Lee JH, Song JS, Jung HI, Sung KH, Jang SJ, Lee SH (2005) Dissemination of transferable CTX-M-type extended-spectrum beta-lactamase-producing Escherichia coli in Korea. J Appl Microbiol 98(4):921–927CrossRefPubMed Jeong SH, Bae IK, Kwon SB, Lee JH, Song JS, Jung HI, Sung KH, Jang SJ, Lee SH (2005) Dissemination of transferable CTX-M-type extended-spectrum beta-lactamase-producing Escherichia coli in Korea. J Appl Microbiol 98(4):921–927CrossRefPubMed
14.
go back to reference Pallecchi L, Riccobono E, Mantella A, Bartalesi F, Sennati S, Gamboa H, Gotuzzo E, Bartoloni A, Rossolini GM (2009) High prevalence of qnr genes in commensal enterobacteria from healthy children in Peru and Bolivia. Antimicrob Agents Chemother 53(6):2632–2635CrossRefPubMedPubMedCentral Pallecchi L, Riccobono E, Mantella A, Bartalesi F, Sennati S, Gamboa H, Gotuzzo E, Bartoloni A, Rossolini GM (2009) High prevalence of qnr genes in commensal enterobacteria from healthy children in Peru and Bolivia. Antimicrob Agents Chemother 53(6):2632–2635CrossRefPubMedPubMedCentral
15.
go back to reference Clinical and Laboratory Standards Institute (CLSI) (2014) Performance standards for antimicrobial susceptibility testing—24th informational supplement. CLSI document M100-S24. CLSI, Wayne, PA, USA Clinical and Laboratory Standards Institute (CLSI) (2014) Performance standards for antimicrobial susceptibility testing—24th informational supplement. CLSI document M100-S24. CLSI, Wayne, PA, USA
16.
go back to reference Dashti AA, Paton R, Amyes SG (2006) Linkage of ciprofloxacin resistance with a single genotypic cluster of Klebsiella pneumoniae. Int J Antimicrob Agents 27(1):73–76CrossRefPubMed Dashti AA, Paton R, Amyes SG (2006) Linkage of ciprofloxacin resistance with a single genotypic cluster of Klebsiella pneumoniae. Int J Antimicrob Agents 27(1):73–76CrossRefPubMed
17.
go back to reference Mouneimné H, Robert J, Jarlier V, Cambau E (1999) Type II topoisomerase mutations in ciprofloxacin-resistant strains of Pseudomonas aeruginosa. Antimicrob Agents Chemother 43(1):62–66PubMedPubMedCentral Mouneimné H, Robert J, Jarlier V, Cambau E (1999) Type II topoisomerase mutations in ciprofloxacin-resistant strains of Pseudomonas aeruginosa. Antimicrob Agents Chemother 43(1):62–66PubMedPubMedCentral
18.
go back to reference Rodríguez-Martínez JM, Velasco C, Pascual A, García I, Martínez-Martínez L (2006) Correlation of quinolone resistance levels and differences in basal and quinolone-induced expression from three qnrA-containing plasmids. Clin Microbiol Infect 12(5):440–445CrossRefPubMed Rodríguez-Martínez JM, Velasco C, Pascual A, García I, Martínez-Martínez L (2006) Correlation of quinolone resistance levels and differences in basal and quinolone-induced expression from three qnrA-containing plasmids. Clin Microbiol Infect 12(5):440–445CrossRefPubMed
19.
go back to reference Weigel LM, Anderson GJ, Tenover FC (2002) DNA gyrase and topoisomerase IV mutations associated with fluoroquinolone resistance in Proteus mirabilis. Antimicrob Agents Chemother 46(8):2582–2587CrossRefPubMedPubMedCentral Weigel LM, Anderson GJ, Tenover FC (2002) DNA gyrase and topoisomerase IV mutations associated with fluoroquinolone resistance in Proteus mirabilis. Antimicrob Agents Chemother 46(8):2582–2587CrossRefPubMedPubMedCentral
20.
go back to reference Kim HB, Park CH, Kim CJ, Kim EC, Jacoby GA, Hooper DC (2009) Prevalence of plasmid-mediated quinolone resistance determinants over a 9-year period. Antimicrob Agents Chemother 53(2):639–645CrossRefPubMedPubMedCentral Kim HB, Park CH, Kim CJ, Kim EC, Jacoby GA, Hooper DC (2009) Prevalence of plasmid-mediated quinolone resistance determinants over a 9-year period. Antimicrob Agents Chemother 53(2):639–645CrossRefPubMedPubMedCentral
21.
go back to reference Wu JJ, Ko WC, Tsai SH, Yan JJ (2007) Prevalence of plasmid-mediated quinolone resistance determinants QnrA, QnrB, and QnrS among clinical isolates of Enterobacter cloacae in a Taiwanese hospital. Antimicrob Agents Chemother 51(4):1223–1227CrossRefPubMedPubMedCentral Wu JJ, Ko WC, Tsai SH, Yan JJ (2007) Prevalence of plasmid-mediated quinolone resistance determinants QnrA, QnrB, and QnrS among clinical isolates of Enterobacter cloacae in a Taiwanese hospital. Antimicrob Agents Chemother 51(4):1223–1227CrossRefPubMedPubMedCentral
22.
go back to reference Park CH, Robicsek A, Jacoby GA, Sahm D, Hooper DC (2006) Prevalence in the United States of aac(6′)-Ib-cr encoding a ciprofloxacin-modifying enzyme. Antimicrob Agents Chemother 50(11):3953–3955CrossRefPubMedPubMedCentral Park CH, Robicsek A, Jacoby GA, Sahm D, Hooper DC (2006) Prevalence in the United States of aac(6′)-Ib-cr encoding a ciprofloxacin-modifying enzyme. Antimicrob Agents Chemother 50(11):3953–3955CrossRefPubMedPubMedCentral
23.
go back to reference Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH, Karch H, Reeves PR, Maiden MC, Ochman H, Achtman M (2006) Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 60(5):1136–1151CrossRefPubMedPubMedCentral Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH, Karch H, Reeves PR, Maiden MC, Ochman H, Achtman M (2006) Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 60(5):1136–1151CrossRefPubMedPubMedCentral
24.
go back to reference Friedmann R, Raveh D, Zartzer E, Rudensky B, Broide E, Attias D, Yinnon AM (2009) Prospective evaluation of colonization with extended-spectrum beta-lactamase (ESBL)-producing enterobacteriaceae among patients at hospital admission and of subsequent colonization with ESBL-producing enterobacteriaceae among patients during hospitalization. Infect Control Hospital Epidemiol 30(6):534–542CrossRef Friedmann R, Raveh D, Zartzer E, Rudensky B, Broide E, Attias D, Yinnon AM (2009) Prospective evaluation of colonization with extended-spectrum beta-lactamase (ESBL)-producing enterobacteriaceae among patients at hospital admission and of subsequent colonization with ESBL-producing enterobacteriaceae among patients during hospitalization. Infect Control Hospital Epidemiol 30(6):534–542CrossRef
25.
go back to reference Vidal-Navarro L, Pfeiffer C, Bouziges N, Sotto A, Lavigne JP (2010) Faecal carriage of multidrug-resistant Gram-negative bacilli during a non-outbreak situation in a French university hospital. J Antimicrob Chemother 65(11):2455–2458CrossRefPubMed Vidal-Navarro L, Pfeiffer C, Bouziges N, Sotto A, Lavigne JP (2010) Faecal carriage of multidrug-resistant Gram-negative bacilli during a non-outbreak situation in a French university hospital. J Antimicrob Chemother 65(11):2455–2458CrossRefPubMed
26.
go back to reference Adler A, Gniadkowski M, Baraniak A, Izdebski R, Fiett J, Hryniewicz W, Malhotra-Kumar S, Goossens H, Lammens C, Lerman Y, Kazma M, Kotlovsky T, Carmeli Y (2012) Transmission dynamics of ESBL-producing Escherichia coli clones in rehabilitation wards at a tertiary care centre. Clin Microbiol Infect 18(12):E497–E505CrossRefPubMed Adler A, Gniadkowski M, Baraniak A, Izdebski R, Fiett J, Hryniewicz W, Malhotra-Kumar S, Goossens H, Lammens C, Lerman Y, Kazma M, Kotlovsky T, Carmeli Y (2012) Transmission dynamics of ESBL-producing Escherichia coli clones in rehabilitation wards at a tertiary care centre. Clin Microbiol Infect 18(12):E497–E505CrossRefPubMed
27.
go back to reference Peirano G, Richardson D, Nigrin J, McGeer A, Loo V, Toye B, Alfa M, Pienaar C, Kibsey P, Pitout JD (2010) High prevalence of ST131 isolates producing CTX-M-15 and CTX-M-14 among extended-spectrum-beta-lactamase-producing Escherichia coli isolates from Canada. Antimicrob Agents Chemother 54(3):1327–1330CrossRefPubMedPubMedCentral Peirano G, Richardson D, Nigrin J, McGeer A, Loo V, Toye B, Alfa M, Pienaar C, Kibsey P, Pitout JD (2010) High prevalence of ST131 isolates producing CTX-M-15 and CTX-M-14 among extended-spectrum-beta-lactamase-producing Escherichia coli isolates from Canada. Antimicrob Agents Chemother 54(3):1327–1330CrossRefPubMedPubMedCentral
28.
go back to reference Colodner R, Samra Z, Keller N, Sprecher H, Block C, Peled N, Lazarovitch T, Bardenstein R, Schwartz-Harari O, Carmeli Y (2007) First national surveillance of susceptibility of extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella spp. to antimicrobials in Israel. Diagn Microbiol Infect Dis 57(2):201–205CrossRefPubMed Colodner R, Samra Z, Keller N, Sprecher H, Block C, Peled N, Lazarovitch T, Bardenstein R, Schwartz-Harari O, Carmeli Y (2007) First national surveillance of susceptibility of extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella spp. to antimicrobials in Israel. Diagn Microbiol Infect Dis 57(2):201–205CrossRefPubMed
29.
go back to reference Schwaber MJ, Navon-Venezia S, Schwartz D, Carmeli Y (2005) High levels of antimicrobial coresistance among extended-spectrum-beta-lactamase-producing Enterobacteriaceae. Antimicrob Agents Chemother 49(5):2137–2139CrossRefPubMedPubMedCentral Schwaber MJ, Navon-Venezia S, Schwartz D, Carmeli Y (2005) High levels of antimicrobial coresistance among extended-spectrum-beta-lactamase-producing Enterobacteriaceae. Antimicrob Agents Chemother 49(5):2137–2139CrossRefPubMedPubMedCentral
30.
go back to reference Karah N, Poirel L, Bengtsson S, Sundqvist M, Kahlmeter G, Nordmann P, Sundsfjord A, Samuelsen Ø (2010) Plasmid-mediated quinolone resistance determinants qnr and aac(6′)-Ib-cr in Escherichia coli and Klebsiella spp. from Norway and Sweden. Diagn Microbiol Infect Dis 66(4):425–431CrossRefPubMed Karah N, Poirel L, Bengtsson S, Sundqvist M, Kahlmeter G, Nordmann P, Sundsfjord A, Samuelsen Ø (2010) Plasmid-mediated quinolone resistance determinants qnr and aac(6′)-Ib-cr in Escherichia coli and Klebsiella spp. from Norway and Sweden. Diagn Microbiol Infect Dis 66(4):425–431CrossRefPubMed
31.
go back to reference Ruiz E, Sáenz Y, Zarazaga M, Rocha-Gracia R, Martínez-Martínez L, Arlet G, Torres C (2012) qnr, aac(6′)-Ib-cr and qepA genes in Escherichia coli and Klebsiella spp.: genetic environments and plasmid and chromosomal location. J Antimicrob Chemother 67(4):886–897CrossRefPubMed Ruiz E, Sáenz Y, Zarazaga M, Rocha-Gracia R, Martínez-Martínez L, Arlet G, Torres C (2012) qnr, aac(6′)-Ib-cr and qepA genes in Escherichia coli and Klebsiella spp.: genetic environments and plasmid and chromosomal location. J Antimicrob Chemother 67(4):886–897CrossRefPubMed
32.
go back to reference Robicsek A, Strahilevitz J, Sahm DF, Jacoby GA, Hooper DC (2006) qnr prevalence in ceftazidime-resistant Enterobacteriaceae isolates from the United States. Antimicrob Agents Chemother 50(8):2872–2874CrossRefPubMedPubMedCentral Robicsek A, Strahilevitz J, Sahm DF, Jacoby GA, Hooper DC (2006) qnr prevalence in ceftazidime-resistant Enterobacteriaceae isolates from the United States. Antimicrob Agents Chemother 50(8):2872–2874CrossRefPubMedPubMedCentral
33.
go back to reference Dahmen S, Poirel L, Mansour W, Bouallègue O, Nordmann P (2010) Prevalence of plasmid-mediated quinolone resistance determinants in Enterobacteriaceae from Tunisia. Clin Microbiol Infect 16(7):1019–1023CrossRefPubMed Dahmen S, Poirel L, Mansour W, Bouallègue O, Nordmann P (2010) Prevalence of plasmid-mediated quinolone resistance determinants in Enterobacteriaceae from Tunisia. Clin Microbiol Infect 16(7):1019–1023CrossRefPubMed
34.
go back to reference Szabó D, Kocsis B, Rókusz L, Szentandrássy J, Katona K, Kristóf K, Nagy K (2008) First detection of plasmid-mediated, quinolone resistance determinants qnrA, qnrB, qnrS and aac(6′)-Ib-cr in extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae in Budapest, Hungary. J Antimicrob Chemother 62(3):630–632CrossRefPubMed Szabó D, Kocsis B, Rókusz L, Szentandrássy J, Katona K, Kristóf K, Nagy K (2008) First detection of plasmid-mediated, quinolone resistance determinants qnrA, qnrB, qnrS and aac(6′)-Ib-cr in extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae in Budapest, Hungary. J Antimicrob Chemother 62(3):630–632CrossRefPubMed
35.
go back to reference Mavroidi A, Miriagou V, Liakopoulos A, Tzelepi E, Stefos A, Dalekos GN, Petinaki E (2012) Ciprofloxacin-resistant Escherichia coli in Central Greece: mechanisms of resistance and molecular identification. BMC Infect Dis 12:371CrossRefPubMedPubMedCentral Mavroidi A, Miriagou V, Liakopoulos A, Tzelepi E, Stefos A, Dalekos GN, Petinaki E (2012) Ciprofloxacin-resistant Escherichia coli in Central Greece: mechanisms of resistance and molecular identification. BMC Infect Dis 12:371CrossRefPubMedPubMedCentral
36.
go back to reference Novais Â, Viana D, Baquero F, Martínez-Botas J, Cantón R, Coque TM (2012) Contribution of IncFII and broad-host IncA/C and IncN plasmids to the local expansion and diversification of phylogroup B2 Escherichia coli ST131 clones carrying blaCTX-M-15 and qnrS1 genes. Antimicrob Agents Chemother 56(5):2763–2766CrossRefPubMedPubMedCentral Novais Â, Viana D, Baquero F, Martínez-Botas J, Cantón R, Coque TM (2012) Contribution of IncFII and broad-host IncA/C and IncN plasmids to the local expansion and diversification of phylogroup B2 Escherichia coli ST131 clones carrying blaCTX-M-15 and qnrS1 genes. Antimicrob Agents Chemother 56(5):2763–2766CrossRefPubMedPubMedCentral
37.
go back to reference Peirano G, Pitout JD (2014) Fluoroquinolone-resistant Escherichia coli sequence type 131 isolates causing bloodstream infections in a Canadian region with a centralized laboratory system: rapid emergence of the H30-Rx sublineage. Antimicrob Agents Chemother 58(5):2699–2703CrossRefPubMedPubMedCentral Peirano G, Pitout JD (2014) Fluoroquinolone-resistant Escherichia coli sequence type 131 isolates causing bloodstream infections in a Canadian region with a centralized laboratory system: rapid emergence of the H30-Rx sublineage. Antimicrob Agents Chemother 58(5):2699–2703CrossRefPubMedPubMedCentral
38.
Metadata
Title
High rates of intestinal colonisation with fluoroquinolone-resistant ESBL-harbouring Enterobacteriaceae in hospitalised patients with antibiotic-associated diarrhoea
Authors
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
Publication date
01-12-2014
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Clinical Microbiology & Infectious Diseases / Issue 12/2014
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI
https://doi.org/10.1007/s10096-014-2193-9

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