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Open Access 01-12-2017 | Research

Prevalence and characteristics of ST131 clone among unselected clinical Escherichia coli in a Chinese university hospital

Authors: Bin Li, Yanfang Lu, Fangjun Lan, Qingwen He, Chen Li, Yingping Cao

Published in: Antimicrobial Resistance & Infection Control | Issue 1/2017

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Abstract

Background

Escherichia coli clinical sequence type 131 (ST131) has emerged as an extensively antimicrobial resistant E. coli clonal group in recent years throughout the world. The aim of this study was to investigate the prevalence and molecular characteristics of ST131 among unselected E. coli clinical isolates in a Chinese university hospital.

Methods

Seven hundred consecutive E. coli isolates were collected at a Chinese university hospital between 2014 and 2015. Isolates belonging to ST131 were identified by PCR and multilocus sequence typing (MLST), and then characterized for antibiotic resistance, CTX-M-type extended-spectrum β-lactamase genes, fluoroquinolone resistance genes, O types, phylogenetic groups, virulence factors and PFGE patterns.

Results

Overall, 83 (11.6%) isolates were identified as ST131 group. The H30 lineage accounted for 53 (63.9%) of the ST131 isolates, including 13 H30-Rx and 40 H30 non-Rx. The remaining 30 isolates belonged to H41 lineage. Two O types were identified in this study: O25b (66.3%) and O16 (33.7%). Compared with O25b-B2-ST131 isolates, O16-B2-ST131 isolates harbored less virulence factors of adhesins. ST131 H30 Rx isolates had significantly higher virulence score than those of other isolates. O16-B2-ST131 isolates were shown to have a lower resistance to quinolones than O25b-B2-ST131 isolates. 5 nonsynonymous mutations (GyrA S83 L, D87N, ParC S80I, E84V and ParE I529L) were strongly associated with ST131 H30 and O25b isolates. Results of PFGE demonstrated that these isolates were classified into 68 pulsotypes and these subtypes were grouped into 23 different PFGE clusters using 70% similarity cut-off value.

Conclusions

This is the first study to reveal the prevalence and molecular characteristic of ST131 clonal group among consecutive clinical E. coli isolates in China. Our findings demonstrated that ST131 lineage accounts for a small proportion of clinical E. coli isolates in China, which included two major groups: O25b-B2-ST131 and O16-B2-ST131. Our results implies that O16-B2-ST131 subclone may be an important type of E. coli ST 131 in China, which suggests that future studies should not ignore such clone in this country.
Literature
2.
go back to reference Mathers AJ, Peirano G, Pitout JD. The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant Enterobacteriaceae. Clin MicrobioRev. 2015;28:565–91.CrossRef Mathers AJ, Peirano G, Pitout JD. The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant Enterobacteriaceae. Clin MicrobioRev. 2015;28:565–91.CrossRef
3.
go back to reference Johnson JR, Tchesnokova V, Johnston B, Clabots C, Roberts PL, Billig M, et al. Abrupt emergence of single dominant multidrug-resistant strain of Escherichia Coli. J Infect Dis. 2013;207:919–28.CrossRefPubMedPubMedCentral Johnson JR, Tchesnokova V, Johnston B, Clabots C, Roberts PL, Billig M, et al. Abrupt emergence of single dominant multidrug-resistant strain of Escherichia Coli. J Infect Dis. 2013;207:919–28.CrossRefPubMedPubMedCentral
4.
go back to reference Sauget M, Cholley P, Vannier A, Thouverez M, Nicolas-Chanoine MH, Hocquet D, et al. Trends of extended-spectrum β-lactamase-producing Escherichia Coli sequence type 131 and its H30 subclone in a French hospital over a 15-year period. Int J Antimicrob Agents. 2016;48:744–7.CrossRefPubMed Sauget M, Cholley P, Vannier A, Thouverez M, Nicolas-Chanoine MH, Hocquet D, et al. Trends of extended-spectrum β-lactamase-producing Escherichia Coli sequence type 131 and its H30 subclone in a French hospital over a 15-year period. Int J Antimicrob Agents. 2016;48:744–7.CrossRefPubMed
5.
go back to reference Matsumura Y, Johnson JR, Yamamoto M, Nagao M, Tanaka M, Takakura S, et al. CTX-M-27- and CTX-M-14-producing, ciprofloxacin-resistant Escherichia Coli of the H30 subclonal group within ST131 drive a Japanese regional ESBL epidemic. J Antimicrob Chemother. 2015;70:1639–49.PubMed Matsumura Y, Johnson JR, Yamamoto M, Nagao M, Tanaka M, Takakura S, et al. CTX-M-27- and CTX-M-14-producing, ciprofloxacin-resistant Escherichia Coli of the H30 subclonal group within ST131 drive a Japanese regional ESBL epidemic. J Antimicrob Chemother. 2015;70:1639–49.PubMed
6.
go back to reference Ben Zakour NL, Alsheikh-Hussain AS, Ashcroft MM, Khanh Nhu NT, Roberts LW, Stanton-Cook M, et al. Sequential Acquisition of Virulence and Fluoroquinolone Resistance has Shaped the evolution of Escherichia Coli ST131. MBio. 2016;7:e00347–16.PubMedPubMedCentral Ben Zakour NL, Alsheikh-Hussain AS, Ashcroft MM, Khanh Nhu NT, Roberts LW, Stanton-Cook M, et al. Sequential Acquisition of Virulence and Fluoroquinolone Resistance has Shaped the evolution of Escherichia Coli ST131. MBio. 2016;7:e00347–16.PubMedPubMedCentral
7.
go back to reference Wang LH, Liu PP, Wei DD, Liu Y, Wan LG, Xiang TX, et al. Clinical isolates of uropathogenic Escherichia Coli ST131 producing NDM-7 metallo-β-lactamase inChina. Int J Antimicrob Agents. 2016;48:41–5.CrossRefPubMed Wang LH, Liu PP, Wei DD, Liu Y, Wan LG, Xiang TX, et al. Clinical isolates of uropathogenic Escherichia Coli ST131 producing NDM-7 metallo-β-lactamase inChina. Int J Antimicrob Agents. 2016;48:41–5.CrossRefPubMed
8.
go back to reference Zhang F, Zhu D, Xie L, Guo X, Ni Y, Sun J. Molecular epidemiology of carbapenemase-producing Escherichia Coli and the prevalence of ST131 subclone H30 in shanghai, China. Eur J Clin Microbiol Infect Dis. 2015;34:1263–9.CrossRefPubMed Zhang F, Zhu D, Xie L, Guo X, Ni Y, Sun J. Molecular epidemiology of carbapenemase-producing Escherichia Coli and the prevalence of ST131 subclone H30 in shanghai, China. Eur J Clin Microbiol Infect Dis. 2015;34:1263–9.CrossRefPubMed
9.
go back to reference Wang S, Zhao SY, Xiao SZ, FF G, Liu QZ, Tang J, et al. Antimicrobial resistance and molecular epidemiology of Escherichia Coli causing bloodstream infections in three hospitals in shanghai, China. PLoS One. 2016;11:e0147740.CrossRefPubMedPubMedCentral Wang S, Zhao SY, Xiao SZ, FF G, Liu QZ, Tang J, et al. Antimicrobial resistance and molecular epidemiology of Escherichia Coli causing bloodstream infections in three hospitals in shanghai, China. PLoS One. 2016;11:e0147740.CrossRefPubMedPubMedCentral
10.
go back to reference Johnson JR, Menard M, Johnston B, Kuskowski MA, Nichol K, Zhanel GG. Epidemic clonal groups of Escherichia Coli as a cause of antimicrobial-resistant urinary tract infections in Canada, 2002 to 2004. Antimicrob Agents Chemother. 2009;53:2733–9.CrossRefPubMedPubMedCentral Johnson JR, Menard M, Johnston B, Kuskowski MA, Nichol K, Zhanel GG. Epidemic clonal groups of Escherichia Coli as a cause of antimicrobial-resistant urinary tract infections in Canada, 2002 to 2004. Antimicrob Agents Chemother. 2009;53:2733–9.CrossRefPubMedPubMedCentral
11.
go back to reference Colpan A, Johnston B, Porter S, Clabots C, Anway R, Thao L, et al. Escherichia coli sequence type 131 (ST131) subclone H30 as an emergent multidrug-resistant pathogen among US veterans. Clin Infect Dis. 2013;57:1256–65.CrossRefPubMedPubMedCentral Colpan A, Johnston B, Porter S, Clabots C, Anway R, Thao L, et al. Escherichia coli sequence type 131 (ST131) subclone H30 as an emergent multidrug-resistant pathogen among US veterans. Clin Infect Dis. 2013;57:1256–65.CrossRefPubMedPubMedCentral
12.
go back to reference Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; 24th Informational Supplement, M100-S26. PA: Wayne; 2016. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; 24th Informational Supplement, M100-S26. PA: Wayne; 2016.
13.
go back to reference Clermont O, Christenson JK, Denamur E, Gordon DM. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity anddetection of new phylo-groups. Environ Microbiol Rep. 2013;5:58–65.CrossRefPubMed Clermont O, Christenson JK, Denamur E, Gordon DM. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity anddetection of new phylo-groups. Environ Microbiol Rep. 2013;5:58–65.CrossRefPubMed
14.
go back to reference Li D, Liu B, Chen M, Guo D, Guo X, Liu F, et al. A multiplex PCR method to detect 14 Escherichia coli serogroups associated with urinary tract infections. J Microbiol Methods. 2010;82:71–7.CrossRefPubMed Li D, Liu B, Chen M, Guo D, Guo X, Liu F, et al. A multiplex PCR method to detect 14 Escherichia coli serogroups associated with urinary tract infections. J Microbiol Methods. 2010;82:71–7.CrossRefPubMed
15.
go back to reference Clermont O, Dhanji H, Upton M, Gibreel T, Fox A, Boyd D, et al. Rapid detection of the O25b-ST131 clone of Escherichia coli encompassing the CTX-M-15-producing strains. J Antimicrob Chemother. 2009;64:274–7.CrossRefPubMed Clermont O, Dhanji H, Upton M, Gibreel T, Fox A, Boyd D, et al. Rapid detection of the O25b-ST131 clone of Escherichia coli encompassing the CTX-M-15-producing strains. J Antimicrob Chemother. 2009;64:274–7.CrossRefPubMed
16.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
17.
go back to reference Oteo J, Gonzalez-Lopez JJ, Ortega A, Quintero-Zarate JN, Bou G, Cercenada E, et al. Inhibitor-resistant TEM- and OXA-1- producing Escherichia Coli isolates resistant to amoxicillin-clavulanate are more clonal and possess lower virulence gene content than susceptible clinical isolates. Antimicrob Agents Chemother. 2014;58:3874–81.CrossRefPubMedPubMedCentral Oteo J, Gonzalez-Lopez JJ, Ortega A, Quintero-Zarate JN, Bou G, Cercenada E, et al. Inhibitor-resistant TEM- and OXA-1- producing Escherichia Coli isolates resistant to amoxicillin-clavulanate are more clonal and possess lower virulence gene content than susceptible clinical isolates. Antimicrob Agents Chemother. 2014;58:3874–81.CrossRefPubMedPubMedCentral
18.
go back to reference Li B, Sun JY, Liu QZ, Han LZ, Huang XH, Ni YX. High prevalence of CTX-M β-lactamases in faecal Escherichia coli strains from healthy humans in Fuzhou, China. Scand J Infect Dis. 2011;43:170–4.CrossRefPubMed Li B, Sun JY, Liu QZ, Han LZ, Huang XH, Ni YX. High prevalence of CTX-M β-lactamases in faecal Escherichia coli strains from healthy humans in Fuzhou, China. Scand J Infect Dis. 2011;43:170–4.CrossRefPubMed
19.
go back to reference Komp Lindgren P, Karlsson A, Hughes D. Mutation rate and evolution of fluoroquinolone resistance in Escherichia Coli isolates from patients with urinary tract infections. Antimicrob Agents Chemother. 2003;47:3222–32.CrossRefPubMedPubMedCentral Komp Lindgren P, Karlsson A, Hughes D. Mutation rate and evolution of fluoroquinolone resistance in Escherichia Coli isolates from patients with urinary tract infections. Antimicrob Agents Chemother. 2003;47:3222–32.CrossRefPubMedPubMedCentral
20.
go back to reference Robicsek A, Strahilevitz J, Jacoby GA, Macielag M, Abbanat D, Park CH, et al. Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase. Nat Med. 2006;12:83–8.CrossRefPubMed Robicsek A, Strahilevitz J, Jacoby GA, Macielag M, Abbanat D, Park CH, et al. Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase. Nat Med. 2006;12:83–8.CrossRefPubMed
21.
go back to reference Yamane K, Wachino J, Suzuki S, Kimura K, Shibata N, Kato H, et al. New plasmid-mediated fluoroquinolone efflux pump, QepA, found in an Escherichia coli clinical isolate. Antimicrob Agents Chemother. 2007;51:3354–60.CrossRefPubMedPubMedCentral Yamane K, Wachino J, Suzuki S, Kimura K, Shibata N, Kato H, et al. New plasmid-mediated fluoroquinolone efflux pump, QepA, found in an Escherichia coli clinical isolate. Antimicrob Agents Chemother. 2007;51:3354–60.CrossRefPubMedPubMedCentral
22.
go back to reference Lafolie J, Nicolas-Chanoine MH, Grenouillet F, Hocquet D, Bertrand X. Prevalence of Escherichia coli sequence type 131 and its H30 subclone among E. coli isolates in a French hospital. Int J Antimicrob Agents. 2014;44:466–8.CrossRefPubMed Lafolie J, Nicolas-Chanoine MH, Grenouillet F, Hocquet D, Bertrand X. Prevalence of Escherichia coli sequence type 131 and its H30 subclone among E. coli isolates in a French hospital. Int J Antimicrob Agents. 2014;44:466–8.CrossRefPubMed
23.
go back to reference Kim SY, Park YJ, Johnson JR, JK Y, Kim YK, Kim YS. Prevalence and characteristics of Escherichia coli sequence type 131 and its H30 and H30Rx subclones: a multicenter study from Korea. Diagn Microbiol Infect Dis. 2016;84:97–101.CrossRefPubMed Kim SY, Park YJ, Johnson JR, JK Y, Kim YK, Kim YS. Prevalence and characteristics of Escherichia coli sequence type 131 and its H30 and H30Rx subclones: a multicenter study from Korea. Diagn Microbiol Infect Dis. 2016;84:97–101.CrossRefPubMed
24.
go back to reference Banerjee R, Johnson JRA. New clone sweeps clean: the enigmatic emergence of Escherichia coli sequence type 131. Antimicrob Agents Chemother. 2014;58:4997–5004.CrossRefPubMedPubMedCentral Banerjee R, Johnson JRA. New clone sweeps clean: the enigmatic emergence of Escherichia coli sequence type 131. Antimicrob Agents Chemother. 2014;58:4997–5004.CrossRefPubMedPubMedCentral
25.
go back to reference Zhong YM, Liu WE, Liang XH, Li YM, Jian ZJ, Hawkey PM. Emergence and spread of O16-ST131 and O25b-ST131 clones among faecal CTX-M-producing Escherichia Coli in healthy individuals in Hunan Province, China. J Antimicrob Chemother. 2015;70:2223–7.CrossRefPubMedPubMedCentral Zhong YM, Liu WE, Liang XH, Li YM, Jian ZJ, Hawkey PM. Emergence and spread of O16-ST131 and O25b-ST131 clones among faecal CTX-M-producing Escherichia Coli in healthy individuals in Hunan Province, China. J Antimicrob Chemother. 2015;70:2223–7.CrossRefPubMedPubMedCentral
26.
go back to reference Matsumura Y, Yamamoto M, Nagao M, Hotta G, Matsushima A, Ito Y, et al. Emergence and spread of B2-ST131-O25b, B2-ST131-O16 and D-ST405 clonal groups among extended-spectrum-β-lactamase-producing Escherichia coli in Japan. J Antimicrob Chemother. 2012;67:2612–20.CrossRefPubMed Matsumura Y, Yamamoto M, Nagao M, Hotta G, Matsushima A, Ito Y, et al. Emergence and spread of B2-ST131-O25b, B2-ST131-O16 and D-ST405 clonal groups among extended-spectrum-β-lactamase-producing Escherichia coli in Japan. J Antimicrob Chemother. 2012;67:2612–20.CrossRefPubMed
27.
go back to reference Peirano G, van der Bij AK, Freeman JL, Poirel L, Nordmann P, Costello M, et al. Characheristics of Escherichia Coli sequence type 131 isolates that produce extended-spectrum β-lactamases: global distribution of the H30-Rx sublineage. Antimicrob Agents Chemother. 2014;58:3762–7.CrossRefPubMedPubMedCentral Peirano G, van der Bij AK, Freeman JL, Poirel L, Nordmann P, Costello M, et al. Characheristics of Escherichia Coli sequence type 131 isolates that produce extended-spectrum β-lactamases: global distribution of the H30-Rx sublineage. Antimicrob Agents Chemother. 2014;58:3762–7.CrossRefPubMedPubMedCentral
30.
go back to reference Johnning A, Kristiansson E, Angelin M, Marathe N, Shouche YS, Johansson A, et al. Quinolone resistance mutations in the faecal microbiota of Swedish travellers to India. BMC Microbiol. 2015;15:235.CrossRefPubMedPubMedCentral Johnning A, Kristiansson E, Angelin M, Marathe N, Shouche YS, Johansson A, et al. Quinolone resistance mutations in the faecal microbiota of Swedish travellers to India. BMC Microbiol. 2015;15:235.CrossRefPubMedPubMedCentral
31.
go back to reference Johnson JR, Johnston B, Kuskowski MA, Sokurenko EV, Tchesnokova V. Intensity and mechanisms of fluoroquinolone resistance within the H30 and H30Rx subclones of Escherichia Coli sequence type 131 compared with other fluoroquinolone-resistant E. Coli. Antimicrob Agents Chemother. 2015;59:4471–80.CrossRefPubMedPubMedCentral Johnson JR, Johnston B, Kuskowski MA, Sokurenko EV, Tchesnokova V. Intensity and mechanisms of fluoroquinolone resistance within the H30 and H30Rx subclones of Escherichia Coli sequence type 131 compared with other fluoroquinolone-resistant E. Coli. Antimicrob Agents Chemother. 2015;59:4471–80.CrossRefPubMedPubMedCentral
32.
go back to reference Olesen B, Frimodt-Møller J, Leihof RF, Struve C, Johnston B, Hansen DS, et al. Temporal trends in antimicrobial resistance and virulence-associated traits within the Escherichia Coli sequence type 131 clonal group and its H30 and H30-Rx subclones, 1968 to 2012. Antimicrob Agents Chemother. 2014;58:6886–95.CrossRefPubMedPubMedCentral Olesen B, Frimodt-Møller J, Leihof RF, Struve C, Johnston B, Hansen DS, et al. Temporal trends in antimicrobial resistance and virulence-associated traits within the Escherichia Coli sequence type 131 clonal group and its H30 and H30-Rx subclones, 1968 to 2012. Antimicrob Agents Chemother. 2014;58:6886–95.CrossRefPubMedPubMedCentral
33.
go back to reference Farrell DJ, Morrissey I, De Rubeis D, Robbins M, Felmingham DAUK. Multicentre study and the antimicrobial susceptibility of bacterial pathogens causing urinary tract infection. J Inf Secur. 2003;46:94–100. Farrell DJ, Morrissey I, De Rubeis D, Robbins M, Felmingham DAUK. Multicentre study and the antimicrobial susceptibility of bacterial pathogens causing urinary tract infection. J Inf Secur. 2003;46:94–100.
34.
go back to reference Tarchouna M, Ferjani A, Ben-Selma W, Boukadida J. Distribution of uropathogenic virulence genes in Escherichia coli isolated from patients with urinary tract infection. Int J InfectDis. 2013;17:e450–3.CrossRef Tarchouna M, Ferjani A, Ben-Selma W, Boukadida J. Distribution of uropathogenic virulence genes in Escherichia coli isolated from patients with urinary tract infection. Int J InfectDis. 2013;17:e450–3.CrossRef
Metadata
Title
Prevalence and characteristics of ST131 clone among unselected clinical Escherichia coli in a Chinese university hospital
Authors
Bin Li
Yanfang Lu
Fangjun Lan
Qingwen He
Chen Li
Yingping Cao
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Antimicrobial Resistance & Infection Control / Issue 1/2017
Electronic ISSN: 2047-2994
DOI
https://doi.org/10.1186/s13756-017-0274-0

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