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. 2022 Aug 25;11(9):1152.
doi: 10.3390/antibiotics11091152.

Distribution and Genomic Characterization of Third-Generation Cephalosporin-Resistant Escherichia coli Isolated from a Single Family and Home Environment: A 2-Year Longitudinal Study

Yin-Chih Feng  1 , Ci-Hong Liou  2 , Wailap Victor Ng  3 , Feng-Jui Chen  2   4 , Chih-Hsin Hung  5 , Po-Yen Liu  1 , Yu-Chieh Liao  6 , Han-Chieh Wu  2 , Ming-Fang Cheng  1   7   8
Affiliations

Distribution and Genomic Characterization of Third-Generation Cephalosporin-Resistant Escherichia coli Isolated from a Single Family and Home Environment: A 2-Year Longitudinal Study

Yin-Chih Feng et al. Antibiotics (Basel). .

Abstract

Third-generation cephalosporin-resistant Escherichia coli (CREC), particularly strains producing extended-spectrum β-lactamases (ESBLs), are a global concern. Our study aims to longitudinally assemble the genomic characteristics of CREC isolates from fecal samples from an index patient with recurrent CREC-related urinary tract infections and his family and swabs from his home environment 12 times between 2019 and 2021 to investigate the distribution of antibiotic resistance genes. CREC identified using the VITEK 2 were subjected to nanopore whole-genome sequencing (WGS). The WGS of 27 CREC isolates discovered in 137 specimens (1 urine, 123 feces, and 13 environmental) revealed the predominance of ST101 and ST131. Among these sequence types, blaCTX-M (44.4%, n = 12) was the predominant ESBL gene family, with blaCTX-M-14 (n = 6) being the most common. The remaining 15 (55.6%) isolates harbored blaCMY-2 genes and were clonally diverse. All E. coli isolated from the index patient's initial urine and fecal samples belonged to O25b:H4-B2-ST131 and carried blaCTX-M-14. The results of sequence analysis indicate plasmid-mediated household transmission of blaCMY-2 or blaCTX-M-55. A strong genomic similarity was discovered between fecal ESBL-producing E. coli and uropathogenic strains. Furthermore, blaCMY-2 genes were widely distributed among the CREC isolated from family members and their home environment.

Keywords: AmpC β-lactamases; CMY-2; Escherichia coli; extended-spectrum β-lactamases; plasmid; third-generation cephalosporin-resistant Escherichia coli; whole-genome sequencing.

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Conflict of interest statement

The authors declare no conflict of interest. The funders did not play any role in the study design, data collection and interpretation, or discussion to submit the study for publications.

Figures

Figure 1
Figure 1
Multilocus sequence typing and phylogenetics traits of 27 third-generation cephalosporin-resistant Escherichia coli (CREC) isolates. (A) Phylogenetic tree of 27 CREC isolates produced through genome-wide phylogenetic analysis of the chromosomal sequences using the Type (Strain) Genome Server (https://tygs.dsmz.de/, accessed on 21 March 2022). (B) Proportions of sequence types (middle ring), phylogenetic groups (inner ring), and subclades (outer ring) of the pandemic ST131 strains predicted from the genome sequences of the 27 CREC isolates. a The S and U in isolation no. indicate the stool and urine origins, respectively.
Figure 2
Figure 2
Relative abundance of sequence types among CTX-M-14-producing and CMY-2-producing Escherichia coli. The majority of CTX-M-14-producing and CMY-2-producing isolates had ST131 and ST101, respectively. The β-lactamases and sequence types of the 27 third-generation cephalosporin-resistant E. coli isolates were determined using MLST 2.0.4 for sequence type identification and ResFinder 4.1 for CTX-M/AmpC β-lactamase gene detection.
Figure 3
Figure 3
Sequence types and third-generation cephalosporin resistance genes among third-generation cephalosporin-resistant Escherichia coli (CREC) isolates. Distribution of sequence types and blaESBL and blaAmpC genes in CREC isolated from family members and household environment from 12 collections between April 2020 and September 2021 after the index patient’s first urinary tract infection in December 2019. The isolate numbers are indicated in parentheses with the sequence types and antibiotic resistance genes. Characterization of β-lactamase-encoding genes and household transmission. Those β-lactamase-encoding genes with the same superscripts(a,b,c) are from similar plasmid sequences.
Figure 4
Figure 4
β-lactamase-encoding plasmids are highly similar among isolates. Concentric maps showing sequence similarities of (A) CMY-2 plasmid 1 among E-01, I-08-S, I-11-S, I-09-S, I-10-S, I-07-S; (B) CMY-2 plasmid 2 among I-06-S, I-05-S, C2-02-S; (C) CTX-M-55 plasmid among C2-03-S and A-04-S (innermost to outermost circles). Plasmid alignment was performed using the Basic Local Alignment Search Tool Ring Image Generator with the longest plasmid contigs as the reference sequence. The numbers 1–6 highlight the regions missing in some of the plasmids and comprise mobile elements (red arrow), antibiotic resistance genes (blue arrow), virulence factor–encoding genes (green arrow), and miscellaneous elements (white arrow). Colors and their shades indicate sequence similarities.
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