Prevalence of Quinolone Resistance of Extended-Spectrum β-Lactamase-Producing Escherichia coli with ST131-fimH30 in a City Hospital in Hyogo, Japan
Abstract
:1. Introduction
2. Results
2.1. CH Typing
2.2. Antimicrobial Resistance
2.3. Antimicrobial Resistance Genes
2.4. Rep.-PCR
3. Discussion
4. Materials and Methods
4.1. Isolates
4.2. Antimicrobial Susceptibility Test
4.3. CH (fumC/fimH) Typing
4.4. QRDR Analysis
4.5. ESBL Genotyping
4.6. Repetitive-Sequence-Based PCR
4.7. Statistical Analysis Method
Supplementary Materials
Author Contributions
Acknowledgments
Conflicts of Interest
References
- Mathers, A.J.; Peirano, G.; Pitout, J.D. 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. [Google Scholar] [CrossRef] [PubMed]
- Japan Nosocomial Infections Surveillance. Available online: https://janis.mhlw.go.jp/report/kensa.html (accessed on 23 December 2018).
- Naas, T.; Oxacelay, C.; Nordman, P. Identification of CTX-M-Type extended-spectrum-β-lactamase genes using real-time PCR and pyrosequencing. Antimicrob. Agents Chemother. 2007, 51, 223–230. [Google Scholar] [CrossRef] [PubMed]
- Bevan, E.R.; Jones, A.M.; Hawkey, P.M. Global epidemiology of CTX-M β-lactamases: Temporal and geographical shifts in genotype. J. Antimicrob. Chemother. 2017, 72, 2145–2155. [Google Scholar] [CrossRef] [PubMed]
- Hawkey, P.M. Multidrug-resistant Gram-negative bacteria: A product of globalization. J. Hosp. Infect. 2015, 89, 241–247. [Google Scholar] [CrossRef]
- Rogers, B.A.; Sidjabat, H.E.; Paterson, D.L. Escherichia coli O25b-ST131: A pandemic, multiresistant, community-associated strain. J. Antimicrob. Chemother. 2011, 66, 1–14. [Google Scholar] [CrossRef]
- Clermont, O.; Bonacorsi, S.; Bingen, E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl. Environ. Microbiol. 2000, 66, 4555–4558. [Google Scholar] [CrossRef]
- Nicolas-Chanoine, M.H.; Bertrand, X.; Madec, J.Y. Escherichia coli ST131, an Intriguing clonal group. Clin. Microbiol. Rev. 2014, 27, 543–574. [Google Scholar] [CrossRef]
- Yano, H.; Uemura, M.; Endo, S.; Kanamori, H.; Inomata, S.; Kakuta, R.; Ichimura, S.; Ogawa, M.; Shimojima, M.; Ishibashi, N.; et al. Molecular characteristics of extended-spectrum β-lactamases in clinical isolates from Escherichia coli at a Japanese tertiary hospital. PLoS ONE 2013, 8, e64359. [Google Scholar] [CrossRef]
- Johnson, J.R.; Tchesnokova, V.; Johnston, B.; Clabots, C.; Roberts, P.L.; Billig, M.; Riddell, K.; Rogers, P.; Qin, X.; Butler-Wu, S.; et al. Abrupt emergence of a single dominant multidrug-resistant strain of Escherichia coli. J. Infect. Dis. 2013, 207, 919–928. [Google Scholar] [CrossRef]
- Peirano, G.; Pitout, J.D. 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. 2014, 58, 2699–2703. [Google Scholar] [CrossRef]
- Tchesnokova, V.L.; Rechkina, E.; Larson, L.; Ferrier, K.; Weaver, J.L.; Schroeder, D.W.; She, R.; Butler-Wu, S.M.; Aguero-Rosenfeld, M.E.; Zerr, D.; et al. Rapid and expansion in the United States of a new multidrug-resistant Escherichia coli clonal group, sequence type 1193. Clin. Infect. Dis. 2019, 68, 334–337. [Google Scholar] [CrossRef] [PubMed]
- Kim, S.Y.; Park, Y.J.; Johnson, J.R.; Yu, J.K.; Kim, Y.K.; Kim, Y.S. 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. [Google Scholar] [CrossRef] [PubMed]
- Matsumura, Y.; Johnson, J.R.; Yamamoto, M.; Nagao, M.; Tanaka, M.; Takakura, S. 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, 1639–1649. [Google Scholar] [CrossRef] [PubMed]
- Osawa, K.; Shigemura, K.; Shimuzu, R.; Kato, A.; Kusuki, M.; Jikimoto, T.; Nakamura, T.; Yoshida, H.; Arakawa, S.; Fujisawa, M.; et al. Molecular characteristics of extended-spectrum β-lactamase-producing Escherichia coli in a university teaching hospital. Microb. Drug Resist. 2015, 21, 130–139. [Google Scholar] [CrossRef]
- Yamagishi, J.; Shimizu, M. Genetic study of molecular mechanisms of quinolone resistance. Jpn. J. Chemother. 2001, 49, 469–484. [Google Scholar]
- Banejee, R.; Johnson, J.R. A new clone sweeps clean: The enigmatic emergence of Escherichia coli sequence type 131. Antimicrob. Agents Chemother. 2014, 58, 4997–5004. [Google Scholar] [CrossRef]
- Price, L.B.; Johnson, J.R.; Aziz, M.; Clabots, C.; Johnston, B.; Tchesnokova, V.; Nordstrom, L.; Billig, M.; Chattopadhyay, S.; Stegger, M.; et al. The epidemic of extended-spectrm-β-lactamase-producing Escherichia coli ST131 is driven by a single highly pathogenic subclone, H30-Rx. mBio 2013, 4, e00377-13. [Google Scholar] [CrossRef]
- Weissman, S.J.; Johnson, J.R.; Tchesnokova, V.; Billig, M.; Dykhuizen, D.; Riddell, K.; Rogers, P.; Qin, X.; Butler-Wu, S.; Cookson, B.T.; et al. High-resolution two-locus clonal typing of extraintestinal pathogenic Escherichia coli. Appl. Environ. Microbiol. 2012, 78, 1353–1360. [Google Scholar] [CrossRef]
- Shibata, N.; Kurokawa, H.; Doi, Y.; Yagi, T.; Yamane, K.; Wachino, J.; Suzuki, S.; Kimura, K.; Ishikawa, S.; Kato, H.; et al. PCR classification of CTX-M-type β-lactamase genes identified in clinically isolates gram-negative bacilli in Japan. Antimicrob. Agents Chemother. 2006, 50, 791–795. [Google Scholar] [CrossRef]
- Matsumura, Y.; Noguchi, T.; Tanaka, M.; Kanahashi, T.; Yamamoto, M.; Nagao, M.; Takakura, S.; Ichiyama, S. Population structure of Japanese extraintestinal pathogenic Escherichia coli and its relationship with antimicrobial resistance. J. Antimicrob. Chemother. 2017, 72, 1040–1049. [Google Scholar]
- Banerjee, R.; Johnston, B.; Lohse, C.; Chattopadhyay, S.; Tchesnokova, V.; Sokurenko, E.V.; Johnson, J.R. The clonal distribution and diversity of extraintestinal Escherichia coli isolates vary according to patient characteristics. Antimicrob. Agents Chemother. 2013, 57, 5912–5917. [Google Scholar] [CrossRef]
- Tzelepi, E.; Giakkoupi, P.; Sofianou, D.; Loukova, V.; Kemeroglou, A.; Tsakris, A. Detection of extended-spectrum β-lactamases in clinical isolates of Enterobacter cloacae and Enterobacter aerogenes. J. Clin. Microbiol. 2000, 38, 542–546. [Google Scholar]
- Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing: Twenty-second informational supplement M100-S22. 2012. [Google Scholar]
- Johnson, J.R.; Menard, M.; Johnston, B.; Kuskowski, M.A.; Nichol, K.; Zhanel, G.G. 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, 2733–2739. [Google Scholar] [CrossRef]
- Roer, L.; Tchesnokova, V.; Allesoe, R.; Muradova, M.; Chattopadhyay, S.; Ahrenfeldt, J.; Thomsen, M.C.F.; Lund, O.; Hansen, F.; Hammerum, A.M.; et al. Development of a web tool for Escherichia coli subtyping based on fimH alleles. J. Clin. Microbiol. 2017, 55, 2538–2543. [Google Scholar] [CrossRef]
- Banerjee, R.; Robicsek, A.; Kuskowski, M.A.; Porter, S.; Johnston, B.D.; Sokurenko, E.; Tchesnokova, V.; Price, L.B.; Johnson, J.R. Molecular epidemiology of Escherichia coli sequence type 131 and its H30 and H30-Rx subclones among extended-spectrum-β-lactamase-positive and -negative E. coli clinical isolates from the Chicago region, 2007 to 2010. Antimicrob. Agents Chemother. 2013, 57, 6385–6388. [Google Scholar] [CrossRef]
- Clermont, O.; Lavollay, M.; Vimont, S.; Deschamps, C.; Forestier, C.; Branger, C.; Denamur, E.; Arlet, G. The CTX-M-15-producing Escherichia coli diffusing clone belongs to a highly virulent B2 phylogenetic subgroup. J. Antimicrob. Chemother. 2008, 61, 1024–1028. [Google Scholar] [CrossRef]
- Ieda, T.; Kuwahara, K.; Morimoto, Y.; Hisasue, S.; Itou, T.; Horie, S.; Hiramatsu, K. The drug susceptibility of major causative urinary tract infection bacteria, and molecular characterization of the quinolone resistance-determining regions (QRDR) including gyrA and parC. Jpn. J. Chemother. 2015, 63, 343–349. [Google Scholar]
Antibiotics | Total n (%) | CH type a | |||||
---|---|---|---|---|---|---|---|
40-30 (n = 54) | 14-64 (n = 6) | 40-41 (n = 5) | 26-5 (n = 3) | 100-96 (n = 3) | Others (n = 12) | ||
LVFX | 66 (79.5) | 54 (100) | 6 (100) | 0 (0) | 1 (33.3) | 0 (0) | 5 (41.7) |
ABPC/SBT | 67 (80.7) | 42 (77.8) | 4 (66.7) | 4 (80.0) | 3 (100) | 3 (100) | 11 (91.7) |
PIPC/TAZ | 2 (2.4) | 1 (1.9) | 0 (0) | 1 (20.0) | 0 (0) | 0 (0) | 0 (0) |
CMZ | 1 (1.2) | 1 (1.9) | 0 (0) | 0 (0) | 0 (0) | 0 (0) | 0 (0) |
CTX | 83 (100) | 54 (100) | 6 (100) | 5 (100) | 3 (100) | 3 (100) | 12 (100) |
CAZ | 38 (45.8) | 27 (50.0) | 2 (33.3) | 2 (40.0) | 1 (33.3) | 2 (66.7) | 4 (33.3) |
CFPM | 74 (89.2) | 48 (88.9) | 5 (83.3) | 4 (80.0) | 3 (100) | 3 (100) | 11 (91.7) |
AZT | 71 (85.5) | 47 (87.0) | 5 (83.3) | 4 (80.0) | 3 (100) | 2 (66.7) | 10 (83.3) |
GM | 22 (26.5) | 9 (16.7) b | 3 (50.0) | 3 (60.0) | 2 (66.7) | 1 (33.3) | 4 (33.3) |
SXT | 23 (27.7) | 8 (14.8) b | 5 (83.3) | 1 (20.0) | 3 (100) | 0 (0) | 6 (50.0) |
CH type a | ||||||||
---|---|---|---|---|---|---|---|---|
QRDRs mutations b (number of mutations) | LVFX susceptibility | Total n (%) | 40-30 (n = 54) | 14-64 (n = 6) | 40-41 (n = 5) | 26-5 (n = 3) | 100-96 (n = 3) | others (n = 12) |
SDSE (0) | S | 7 (8.4) | 0 (0) | 0 (0) | 0 (0) | 0 (0) | 3 (100) | 4 (33.3) |
LDSE (1) | S | 9 (10.8) | 0 (0) | 0 (0) | 5 (100) | 1 (33.3) | 0 (0) | 3 (25.0) |
LDIE (2) | S | 1 (1.2) | 0 (0) | 0 (0) | 0 (0) | 1 (33.3) | 0 (0) | 0 (0) |
LYIE (3) | R | 1 (1.2) | 0 (0) | 0 (0) | 0 (0) | 1 (33.3) | 0 (0) | 0 (0) |
LNIE (3) | R | 10 (12.0) | 0 (0) | 6 (100) | 0 (0) | 0 (0) | 0 (0) | 4 (33.3) |
LNIG (4) | R | 1 (1.2) | 0 (0) | 0 (0) | 0 (0) | 0 (0) | 0 (0) | 1 (8.3) |
LNIV (4) | R | 54 (65.1) | 54 (100) | 0 (0) | 0 (0) | 0 (0) | 0 (0) | 0 (0) |
CTX-M-type | Total n (%) | fimH30-Rx (n = 14) | fimH30-non-Rx (n = 40) |
---|---|---|---|
CTX-M-15 | 15 (27.8) | 14 (100) | 1 (2.5) |
CTX-M-14 | 26 (48.1) | 0 (0) | 26 (65.0) |
CTX-M-27 | 12 (22.2) | 0 (0) | 12 (30.0) |
CTX-M-15+CTX-M-27 | 1 (1.9) | 0 (0) | 1 (2.5) |
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Teramae, M.; Osawa, K.; Shigemura, K.; Kitagawa, K.; Shirakawa, T.; Fujisawa, M.; Miyara, T. Prevalence of Quinolone Resistance of Extended-Spectrum β-Lactamase-Producing Escherichia coli with ST131-fimH30 in a City Hospital in Hyogo, Japan. Int. J. Mol. Sci. 2019, 20, 5162. https://0-doi-org.brum.beds.ac.uk/10.3390/ijms20205162
Teramae M, Osawa K, Shigemura K, Kitagawa K, Shirakawa T, Fujisawa M, Miyara T. Prevalence of Quinolone Resistance of Extended-Spectrum β-Lactamase-Producing Escherichia coli with ST131-fimH30 in a City Hospital in Hyogo, Japan. International Journal of Molecular Sciences. 2019; 20(20):5162. https://0-doi-org.brum.beds.ac.uk/10.3390/ijms20205162
Chicago/Turabian StyleTeramae, Masazumi, Kayo Osawa, Katsumi Shigemura, Koichi Kitagawa, Toshiro Shirakawa, Masato Fujisawa, and Takayuki Miyara. 2019. "Prevalence of Quinolone Resistance of Extended-Spectrum β-Lactamase-Producing Escherichia coli with ST131-fimH30 in a City Hospital in Hyogo, Japan" International Journal of Molecular Sciences 20, no. 20: 5162. https://0-doi-org.brum.beds.ac.uk/10.3390/ijms20205162