CTX-M-27- and CTX-M-14-producing, ciprofloxacin-resistant <i>Escherichia coli</i> of the <i>H</i>30 subclonal group within ST131 drive a Japanese regional ESBL epidemic

Matsumura, Yasufumi; Johnson, James R.; Yamamoto, Masaki; Nagao, Miki; Tanaka, Michio; Takakura, Shunji; Ichiyama, Satoshi; Fujita, Naohisa; Komori, Toshiaki; Yamada, Yukiji; Shimizu, Takeshi; Hayashi, Akihiko; Ono, Tamotsu; Watanabe, Hiroki; Fujihara, Noború; Higuchi, Takeshi; Moro, Kunihiko; Shigeta, Masayo; Kida, Kaneyuki; Terada, Hiromi; Tsuboi, Fusayuki; Sugimoto, Yukihiko; Fukumoto, Chiyoko

doi:10.1093/jac/dkv017

Cited by 120 publications

(110 citation statements)

References 57 publications

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“…The bla CTX-M-14 gene was the most prevalent ESBL gene. Interestingly, this gene was also reported to be a common ESBL gene in clinical E. coli isolates collected in adjacent regions in Japan (25). The bla CMY-2 gene, which is the most common plasmid-mediated ampC ␤-lactamase gene worldwide (26), was the only acquired ampC ␤-lactamase gene detected in this study.…”

Section: Resultssupporting

confidence: 57%

Whole-Genome Analysis of Antimicrobial-Resistant and Extraintestinal Pathogenic Escherichia coli in River Water

Gomi

Matsuda

Matsumura

et al. 2017

Appl Environ Microbiol

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Contamination of surface waters by antimicrobial-resistant bacteria and pathogenic bacteria is a great concern. In this study, 531 Escherichia coli isolates obtained from the Yamato River in Japan were evaluated phenotypically for resistance to 25 antimicrobials. Seventy-six isolates (14.3%) were multidrug resistant (MDR), 66 (12.4%) were nonsusceptible to one or two classes of agents, and 389 (73.3%) were susceptible. We performed whole-genome sequencing of selected strains by using Illumina technology. In total, the genome sequences of 155 strains were analyzed for antibiotic resistance determinants and phylogenetic characteristics. More than 50 different resistance determinants, including acquired resistance genes and chromosomal resistance mutations, were detected. Among the sequenced MDR strains (n ϭ 66), sequence type 155 (ST155) complex (n ϭ 9), ST10 complex (n ϭ 9), and ST69 complex (n ϭ 7) were prevalent. Among extraintestinal pathogenic E. coli (ExPEC) strains (n ϭ 58), clinically important clonal groups, namely, ST95 complex (n ϭ 18), ST127 complex (n ϭ 8), ST12 complex (n ϭ 6), ST14 complex (n ϭ 6), and ST131 complex (n ϭ 6), were prevalent, demonstrating the clonal distribution of environmental ExPEC strains. Typing of the fimH (type 1 fimbrial adhesin) gene revealed that ST131 complex strains carried fimH22 or fimH41, and no strains belonging to the fimH30 subgroup were detected. Fine-scale phylogenetic analysis and virulence gene content analysis of strains belonging to the ST95 complex (one of the major clonal ExPEC groups causing community-onset infections) revealed no significant differences between environmental and clinical strains. The results indicate contamination of surface waters by E. coli strains belonging to clinically important clonal groups.IMPORTANCE The prevalence of antimicrobial-resistant and pathogenic E. coli strains in surface waters is a concern because surface waters are used as sources for drinking water, irrigation, and recreational purposes. In this study, MDR and ExPEC strains in river water were characterized by genomic sequencing and analysis. We detected more than 50 resistance determinants and identified clonal groups specific to MDR and ExPEC strains. This study showed contamination of surface waters by E. coli strains belonging to clinically important clonal groups. Overall, this study advances our understanding of environmental MDR and ExPEC strains.KEYWORDS antimicrobial resistance, Escherichia coli, ExPEC, whole-genome sequencing E scherichia coli is a commensal member of the gastrointestinal tract of humans and other warm-blooded animals. Consequently, E. coli, as well as Enterococcus spp., has long been used as an indicator of fecal contamination to assess the microbial quality of surface waters. Although most E. coli strains are harmless, some strains are pathogenic

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Section: Resultssupporting

confidence: 57%

Whole-Genome Analysis of Antimicrobial-Resistant and Extraintestinal Pathogenic Escherichia coli in River Water

Gomi

Matsuda

Matsumura

et al. 2017

Appl Environ Microbiol

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“…In this study, most of the CG131 strains produced CTX-M-14. CTX-M-14 is a prevalent CTX-M type in Japan, and the prevalence of CTX-M-14-producing E. coli ST131 increased from 2002 through 2012 (50). It is likely that the O25: H4/CG131 clone acquired both a plasmid harboring bla CTX-M- 14 and an EAEC virulence plasmid in the intestines of people in our district.…”

Section: Discussionmentioning

confidence: 96%

Phylogenetic Analysis of Enteroaggregative Escherichia coli (EAEC) Isolates from Japan Reveals Emergence of CTX-M-14-Producing EAEC O25:H4 Clones Related to Sequence Type 131

et al. 2016

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f Enteroaggregative Escherichia coli (EAEC) causes acute or persistent diarrhea. The aggR gene is widely used as a marker for typical EAEC. The heterogeneity of EAEC is well known; however, there are few reports on the phylogenetic relationships of EAEC. Recently, CTX-M extended-spectrum ␤-lactamase (ESBL)-producing EAEC strains have been reported worldwide. To characterize EAEC strains in Japan, we investigated the population structure of EAEC. A total of 167 aggR-positive strains isolated from stool specimens from diarrheal patients in Kagoshima (139 strains) and Osaka (28 strains), Japan, between 1992 and 2010 were examined for the prevalence of EAEC virulence markers, the bla CTX-M gene, and the capacity to form biofilms. Multilocus sequence typing was also conducted. EAEC strains were widely distributed across four major E. coli phylogroups. Strains of O111: H21/clonal group 40 (CG40) (30 strains), O126:H27/CG200 (13 strains), and O86a:H27/CG3570 (11 strains) in phylogroup B1 are the historical EAEC clones in Japan, and they exhibited strong biofilm formation. Twenty-nine strains of EAEC O25:H4/ CG131 were identified in phylogroup B2, 79% of which produced CTX-M-14. This clone has emerged since 2003. The clone harbored plasmid-encoded EAEC virulence genes but not chromosomal virulence genes and had lower biofilm-forming capacity than historical EAEC strains. This clone most likely emerged from a pandemic uropathogenic O25:H4/sequence type 131 clone by acquiring an EAEC virulence plasmid from canonical EAEC. Surveillance of the horizontal transfer of both virulence and ESBL genes among E. coli strains is important for preventing a worldwide increase in antimicrobial drug resistance. Enteroaggregative Escherichia coli (EAEC) causes acute or persistent diarrhea in children and adults, in both developing (1) and industrialized (2, 3) countries. Several outbreaks of gastroenteritis linked to EAEC have been reported (4, 5). EAEC is also the second most common cause of travelers' diarrhea (6). EAEC is defined by its characteristic aggregative adherence (AA) to HEp-2 cells in culture (7). Although detection of the AA phenotype in the HEp-2 cell adherence assay is still the gold standard for EAEC identification, the transcriptional regulator AggR, which controls the expression of multiple EAEC virulence genes, is also used as a typical EAEC marker for PCR detection (8).The pathogenesis of EAEC infection involves the adherence of the bacterium to the intestinal mucosa, followed by the secretion of one or more enterotoxins and/or cytotoxins that induce mucosal inflammation (9). EAEC adherence to the mucosa is characterized by the formation of a thick biofilm (10), which may promote persistent infection. The majority of EAEC strains carry a large (ϳ100-kb) plasmid, which encodes most putative EAEC virulence factors, such as AggR, aggregative adherence fimbriae (AAF), the dispersin protein Aap (11), its transporter Aat (12), the plasmid-encoded toxin Pet (13), enteroaggregative heat-stable toxin 1 (EAST-1) (14), and the...

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“…In addition, one TGC-nonsusceptible strain belonged to another major fluoroquinolone-resistant linage, O1-ST648, that is also distributed worldwide and which frequently expresses ␤-lactamases, CTX-M type ESBLs or CMY-2, and as reported in one study, NDM-5 (24)(25)(26). Thus, these clones are often resistant to multiple drugs (e.g., penicillins, cephalosporins, and aminoglycosides) (5,7,(24)(25)(26). Similarly, most TGC-nonsusceptible isolates belonging to O25b:H4-ST131-H30R and O1-ST648 were resistant to 2 to 4 of the five classes of antimicrobials (cephalosporins, carbapenems, aminoglycosides, fluoroquinolones, and fosfomycin).…”

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confidence: 87%

“…The seven TGC-nonsusceptible isolates were derived from various clinical specimens and patient backgrounds ( Table 1). Five of the seven isolates belonged to a specific lineage, O25b:H4-ST131-H30R, which is a known fluoroquinolone-resistant lineage identified frequently in clinical settings worldwide (Table 1) (5,7). In addition, one TGC-nonsusceptible strain belonged to another major fluoroquinolone-resistant linage, O1-ST648, that is also distributed worldwide and which frequently expresses ␤-lactamases, CTX-M type ESBLs or CMY-2, and as reported in one study, NDM-5 (24)(25)(26).…”

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confidence: 99%

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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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

Abstract: This Japanese regional ESBL-producing E. coli epidemic is closely associated with newly identified CTX-M-27- and CTX-M-14-producing ST131 H30R subclonal groups and with mobile elements IS26, ISEcp1 and IS903D.

Cited by 120 publications

References 57 publications

Whole-Genome Analysis of Antimicrobial-Resistant and Extraintestinal Pathogenic Escherichia coli in River Water

Whole-Genome Analysis of Antimicrobial-Resistant and Extraintestinal Pathogenic Escherichia coli in River Water

Phylogenetic Analysis of Enteroaggregative Escherichia coli (EAEC) Isolates from Japan Reveals Emergence of CTX-M-14-Producing EAEC O25:H4 Clones Related to Sequence Type 131

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

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