Prevalence of Fluoroquinolone-Resistant &lt;i&gt;Escherichia coli&lt;/i&gt; O25:H4-ST131 (CTX-M-15-Nonproducing) Strains Isolated in Japan

Yokota, Shinichi; Sato, Toyotaka; Okubo, Torahiko; Ohkoshi, Yasuo; Okabayashi, Tamaki; Kuwahara, Osamu; Tsutsumi, Yutaka; Fujii, Nobuhiro

doi:10.1159/000336129

Cited by 25 publications

(31 citation statements)

References 44 publications

(30 reference statements)

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“…One of the most prominent characteristics of ST131 is its fluoroquinolone resistance, to which this clonal group is the major contributor worldwide (9,(42)(43)(44)(45)(46)(47). We have recently demonstrated that this phenotype is predominantly associated with strains carrying an NA114-like fimH30 allele (48).…”

Section: Discussionmentioning

confidence: 99%

Role of Homologous Recombination in Adaptive Diversification of Extraintestinal Escherichia coli

et al. 2013

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The contribution of homologous exchange (recombination) of core genes in the adaptive evolution of bacterial pathogens is not well understood. To investigate this, we analyzed fully assembled genomes of two Escherichia coli strains from sequence type 131 (ST131), a clonal group that is both the leading cause of extraintestinal E. coli infections and the main source of fluoroquinolone-resistant E. coli. Although the sequences of each of the seven multilocus sequence typing genes were identical in the two ST131 isolates, the strains diverged from one another by homologous recombination that affected at least 9% of core genes. This was on a par with the contribution to genomic diversity of horizontal gene transfer and point gene mutation. The genomic positions of recombinant and mobile genetic regions were partially linked, suggesting their concurrent occurrence. One of the genes affected by homologous recombination was fimH, which encodes mannose-specific type 1 fimbrial adhesin, resulting in functionally distinct copies of the gene in ST131 strains. One strain, a uropathogenic isolate, had a pathoadaptive variant of fimH that was acquired by homologous replacement into the commensal strain background. Close examination of FimH structure and function in additional ST131 isolates revealed that recombination led to acquisition of several functionally distinct variants that, upon homologous exchange, were targeted by a variety of pathoadaptive mutations under strong positive selection. Different recombinant fimH strains also showed a strong clonal association with ST131 isolates that had distinct fluoroquinolone resistance profiles. Thus, homologous recombination of core genes plays a significant role in adaptive diversification of bacterial pathogens, especially at the level of clonally related groups of isolates.

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Section: Discussionmentioning

confidence: 99%

Role of Homologous Recombination in Adaptive Diversification of Extraintestinal Escherichia coli

et al. 2013

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“…First, we showed that several strains of certain populations of fluoroquinolone-resistant E. coli, including major extraintestinal pathogenic lineages O25b:H4-ST131-H30R and O1-ST648, show reduced susceptibility to TGC (1.0% and 3.6% of fluoroquinolone-resistant E. coli isolates were resistant or nonsusceptible to TGC, respectively). Considering the frequency of fluoroquinolone resistance (for example, the fluoroquinolone resistance rate in E. coli was 23.4% in our previous study [4]), approximately 0.8% or fewer of E. coli clinical isolates could be nonsusceptible or resistant to TGC. Indeed, previous large-scale surveillance studies indicated that fewer than 0.3% of the E. coli clinical isolates were nonsusceptible to TGC (10, 11).…”

mentioning

confidence: 83%

“…Two hundred seventy-seven fluoroquinolone-susceptible E. coli isolates (ciprofloxacin [CIP] MIC, Ͻ0.125 mg/liter) and 194 fluoroquinolone-resistant E. coli isolates (CIP MIC, Ͼ2 mg/liter) were isolated from human clinical specimens. Of these, 100 fluoroquinolone-susceptible E. coli isolates and 118 fluoroquinolone-resistant E. coli isolates (six strains were added for this study) were from human specimens collected in 2008 and 2009, as described previously (4). One hundred seventy-seven fluoroquinolone-susceptible E. coli isolates and 76 fluoroquinolone-resistant E. coli isolates were from human clinical specimens collected in 2015 and 2016 in Japan (Sapporo Medical University Hospital, Sapporo, Japan) and stored in the laboratory.…”

Section: Methodsmentioning

confidence: 99%

“…E. coli ATCC 25922 was used as a reference. The MIC values for CIP, cefpodoxime, cefepime, and gentamicin were obtained from previous studies of E. coli isolates from 2008 and 2009 (4,6,43). MICs for ceftazidime (GSK Japan, Tokyo, Japan), imipenem (MSD, Tokyo, Japan), amikacin (Wako Pure Chemical, Osaka, Japan), and fosfomycin (Meiji Seika Pharma, Tokyo, Japan) were also determined using the agar plate dilution method.…”

Section: Methodsmentioning

confidence: 99%

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Tigecycline Nonsusceptibility Occurs Exclusively in Fluoroquinolone-Resistant Escherichia coli Clinical Isolates, Including the Major Multidrug-Resistant Lineages O25b:H4-ST131-H 30 R and O1-ST648

Sato

Suzuki

Shiraishi

et al. 2017

Antimicrob Agents Chemother

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Tigecycline (TGC) is a last-line drug for multidrug-resistant Enterobacteriaceae. We investigated the mechanism(s) underlying TGC nonsusceptibility (TGC resistant/intermediate) in Escherichia coli clinical isolates. The MIC of TGC was determined for 277 fluoroquinolone-susceptible isolates (ciprofloxacin [CIP] MIC, Ͻ0.125 mg/liter) and 194 fluoroquinolone-resistant isolates (CIP MIC, Ͼ2 mg/liter). The MIC 50 and MIC 90 for TGC in fluoroquinolone-resistant isolates were 2-fold higher than those in fluoroquinolone-susceptible isolates (MIC 50 , 0.5 mg/liter versus 0.25 mg/liter; MIC 90 , 1 mg/liter versus 0.5 mg/liter, respectively). Two fluoroquinolone-resistant isolates (O25b:H4-ST131-H30R and O125:H37-ST48) were TGC resistant (MICs of 4 and 16 mg/liter, respectively), and four other isolates of O25b:H4-ST131-H30R and an isolate of O1-ST648 showed an intermediate interpretation (MIC, 2 mg/liter). No TGC-resistant/intermediate strains were found among the fluoroquinolone-susceptible isolates. The TGC-resistant/intermediate isolates expressed higher levels of acrA and acrB and had lower intracellular TGC concentrations than susceptible isolates, and they possessed mutations in acrR and/or marR. The MICs of acrAB-deficient mutants were markedly lower (0.25 mg/liter) than those of the parental strain. After continuous stepwise exposure to CIP in vitro, six of eight TGC-susceptible isolates had reduced TGC susceptibility. Two of them acquired TGC resistance (TGC MIC, 4 mg/liter) and exhibited expression of acrA and acrB and mutations in acrR and/or marR. In conclusion, a population of fluoroquinolone-resistant E. coli isolates, including major extraintestinal pathogenic lineages O25b:H4-ST131-H30R and O1-ST648, showed reduced susceptibility to TGC due to overexpression of the efflux pump AcrAB-TolC, leading to decreased intracellular concentrations of the antibiotics that may be associated with the development of fluoroquinolone resistance.

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“…This lineage is FQ resistant and often acquires ESBL genes, particularly the CTX-M-15 of group 1. In contrast, other ESBL genes, particularly CTX-M groups 9 (CTX-M-14 and 27) and 2 (CTX-M-2), are dominant in Japanese O25b:H4-ST131 strains [14,15]. However, CTX-M-15-producing O25b:H4-ST131 strains have been found in recent years in Japan [16].…”

Section: Introductionmentioning

confidence: 99%

High Prevalence of Cross-Resistance to Aminoglycosides in Fluoroquinolone-Resistant Escherichia coli Clinical Isolates

Tsukamoto¹,

Ohkoshi²,

Okubo³

et al. 2013

Chemotherapy

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Background: Multidrug-resistant Escherichia coli, especially a lineage of O25b:H4-ST131, has increased and spread worldwide. The surveillance of cross-resistance of E. coli is necessary. Methods: Cross-resistance to fluoroquinolones (FQs) and aminoglycosides (AGs) was examined in E. coli isolated in Hokkaido Prefecture, Japan, between 2008 and 2009. Results: Gentamicin (GEN) resistance was more common in FQ-resistant isolates (30/112 strains; 26.8%) than in FQ-susceptible isolates (2/100 strains; 2%). The frequency of GEN resistance was similar in two groups of FQ-resistant strains, O25b:H4-ST131 genotype (22/87 strains; 25.3%) and a group of other FQ-resistant genotypes (8/25 strains; 32.0%). The main AG resistance gene was aac(3)-II (87.5% of GEN-resistant strains). The only amikacin-resistant strain which was FQ resistant carried the aac(6')-Ib-cr gene. CTX-M type extended-spectrum β-lactamase (ESBL) genes were also found in FQ-resistant strains at a high frequency. However, the number of strains with both ESBL and AG-modifying enzyme genes was relatively low (8 strains). Conclusion: All FQ-resistant strains, not only O25b:H4-ST131, appeared to preferentially acquire ESBL genes and/or genes encoding AG-modifying enzymes; however, the acquisitions of these genes seemed to occur independently.

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Prevalence of Fluoroquinolone-Resistant <i>Escherichia coli</i> O25:H4-ST131 (CTX-M-15-Nonproducing) Strains Isolated in Japan

Cited by 25 publications

References 44 publications

Role of Homologous Recombination in Adaptive Diversification of Extraintestinal Escherichia coli

Role of Homologous Recombination in Adaptive Diversification of Extraintestinal Escherichia coli

Tigecycline Nonsusceptibility Occurs Exclusively in Fluoroquinolone-Resistant Escherichia coli Clinical Isolates, Including the Major Multidrug-Resistant Lineages O25b:H4-ST131-H 30 R and O1-ST648

High Prevalence of Cross-Resistance to Aminoglycosides in Fluoroquinolone-Resistant Escherichia coli Clinical Isolates

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