https://orcid.org/0000-0003-3847-7085
Figures
Abstract
Escherichia coli sequence type (ST) 131 is a globally disseminated multidrug-resistant clone that poses a substantial public health threat. This study investigated the prevalence, virulence characteristics, and antimicrobial resistance profiles of ST131 among companion-animal E. coli isolates. A total of 400 E. coli isolates obtained from dogs and cats diagnosed with urinary tract infections at the National Taiwan University Veterinary Hospital between 2011 and 2019 were analyzed. Phylogenetic grouping identified 192 isolates (48.0%) belonging to phylogroup B2, which is strongly associated with ST131. Among these, 26 isolates (13.5%) were confirmed as ST131 by single-nucleotide polymorphism screening and multilocus sequence typing, and 19 isolates were selected for detailed characterization. Virulence gene analysis by multiplex PCR showed that fyuA (100.0%), traT (94.7%), iutA (89.5%), and kpsMT II (84.2%) were the most prevalent genes. Antimicrobial susceptibility testing demonstrated universal susceptibility to meropenem, whereas all isolates were resistant to amoxicillin and ampicillin. Six canine-derived isolates produced extended-spectrum β-lactamases (ESBLs) or AmpC β-lactamases. Among ESBL producers, bla gene groups blaCTX-M-1, blaCTX-M-9, and blaTEM were detected, whereas blaCMY-178 was the only AmpC gene identified. Conjugation experiments demonstrated transferability for most bla genes, except blaTEM-102, blaTEM-12, and blaCTX-M-55. Plasmid replicon typing revealed IncF (100%) and IncB/O (69%) as the predominant plasmid groups. Only two O-antigen types, O25b and O16, were detected among ST131 isolates, which carried fimH variants fimH22, fimH27, fimH30, or fimH41 subclones. These findings demonstrate the circulation of virulent and multidrug-resistant ST131 strains in companion animals in Taiwan, highlighting their potential relevance within a One Health context.
Citation: Lin S-X, Yeh K-S (2026) Characteristics of Escherichia coli ST131 strains isolated from dogs and cats with urinary tract infections in a teaching hospital in Taiwan. PLoS One 21(5): e0350088. https://doi.org/10.1371/journal.pone.0350088
Editor: Gabriel Trueba, Universidad San Francisco de Quito, ECUADOR
Received: October 1, 2025; Accepted: May 10, 2026; Published: May 22, 2026
Copyright: © 2026 Lin, Yeh. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the manuscript and its Supporting Information files.
Funding: This work was supported by a grant from National Taiwan University (No. G049919) to KSY. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
E. coli is a common commensal bacterium of the intestinal tract but also an important opportunistic pathogen capable of causing both intestinal and extraintestinal infections [1]. While many strains are harmless members of the normal microbiota, pathogenic strains may acquire virulence determinants through horizontal gene transfer mediated by plasmids, bacteriophages, or chromosomal integration. Pathogenic E. coli are broadly classified into intestinal pathogenic E. coli, which cause diarrheal disease, and extraintestinal pathogenic E. coli (ExPEC), which cause infections outside the gastrointestinal tract [2]. ExPEC is a major cause of urinary tract infections (UTIs), septicemia, and meningitis, resulting in substantial clinical and economic burdens worldwide. In the United States alone, ExPEC infections are estimated to account for nearly USD 2 billion annually in direct medical costs [3]. The growing prevalence of antimicrobial resistance has further complicated treatment options. For example, trimethoprim–sulfamethoxazole, once widely used for UTIs, has increasingly been replaced by fluoroquinolones because of resistance; however, extensive fluoroquinolone use has subsequently driven the emergence of fluoroquinolone-resistant E. coli strains [4].
In addition to antimicrobial resistance, ExPEC strains possess numerous virulence factors that enhance their pathogenic potential [5]. Among these, E. coli sequence type (ST)131 has attracted global attention since its first recognition in North America, Europe, and Asia in 2008 [6–8]. ST131 is characterized by high virulence, multidrug resistance, and widespread international dissemination, posing important threats to both human and animal health [9]. E. coli ST131 is an important cause of UTIs in both humans and companion animals, particularly dogs and cats [10]. In 2009, ST131 carrying blaCTX-M-15 and fluoroquinolone resistance determinants including qnrB2 and aac(6’)-Ib-cr was reported from canine urine samples in Portugal [11]. Close contact between humans and pets may facilitate bidirectional transmission [11], and previous studies have shown that cohabiting dogs and cats can harbor indistinguishable ST131 strains [12]. Furthermore, ST131 has also been identified in livestock, wildlife, and environmental reservoirs, emphasizing its relevance within a One Health framework [9].
Although previous studies have reported extended-spectrum β-lactamase-producing E. coli from companion animals in Taiwan [13–15], detailed molecular characterization of ST131 isolates from veterinary clinical cases remains limited. Such information is important for understanding local epidemiology, tracking the dissemination of antimicrobial resistance, and supporting antimicrobial stewardship. Therefore, this study aimed to determine the prevalence and molecular characteristics of E. coli ST131 isolated from dogs and cats with urinary tract infections in a veterinary teaching hospital in Taiwan, including their antimicrobial susceptibility, virulence gene repertoire, β-lactamase genotypes, plasmid content, serotype–fimH associations, and transferability of resistance determinants.
Materials and methods
Sample collection
A total of 400 E. coli isolates were recovered from urine samples of dogs and cats diagnosed with UTIs at the National Taiwan University Veterinary Hospital between 2011 and 2019. Species identification was performed using the VITEK 2 Compact automated system (bioMérieux, Marcy-l'Étoile, France) with GN identification cards. All isolates were preserved in Microbank System cryovials (Pro-Lab Diagnostics, Richmond Hill, Ontario, Canada) and stored at −80 °C until analysis. The clinical samples used in this study were collected as part of routine diagnostic and therapeutic procedures. No animals were sampled specifically for research purposes; therefore, formal approval from an Institutional Animal Care and Use Committee (IACUC) was not required.
E. coli phylogenetic grouping
Heat-extracted lysates from all 400 isolates were prepared as previously described by Shaheen et al. [16] and used as DNA templates for polymerase chain reaction (PCR). Phylogenetic grouping was performed according to the revised Clermont quadruplex PCR method [17], which classifies E. coli into phylogroups A, B1, B2, C, D, E, F, and clade I based on the presence or absence of specific amplicons. Isolates showing the marker combinations (−, + , + , −), (−, + , + , +), or (−, + , − , +) for arpA, chuA, yjaA, and Tsp.E4.C2 were assigned to phylogroup B2. Primer sequences are listed in S1 Table.
Screening and confirmation of E. coli ST131
Among the phylogroup B2 isolates, screening for ST131 was performed using previously described single-nucleotide polymorphism (SNP)-based markers in the mdh and gyrB genes. Specifically, ST131-associated SNPs included C288T and C525T in mdh, and C621T, C729T, and T735C in gyrB. Target gene fragments were amplified by PCR and sequenced. The resulting sequences were compared with reference sequences available in the National Center for Biotechnology Information (NCBI) database [18]. Putative ST131 isolates were further confirmed by multilocus sequence typing (MLST), which was performed using seven housekeeping genes as previously described [19]. PCR products were sequenced commercially, and allele profiles were analyzed using the PubMLST (https://pubmlst.org/) and EnteroBase databases (http://enterobase.warwick.ac.uk/) for sequence type assignment. Primer sequences are listed in S2 Table.
Virulence gene detection
Virulence-associated genes were detected by multiplex PCR using the method of Johnson and Stell [20]. Twelve genes commonly associated with uropathogenic E. coli were examined, including adhesin genes (papAH, sfa/focDE, focG), siderophore genes (iutA, fyuA), toxin genes (cnf1, hlyA), capsule-associated genes (K1, kpsMT II, K5), and additional virulence-associated genes (ibeA and traT). Primer sequences are shown in S3 Table.
Antimicrobial Susceptibility Testing (AST)
Antimicrobial susceptibility testing was performed using the minimum inhibitory concentration (MIC) method according to Clinical and Laboratory Standards Institute (CLSI) guidelines [21]. Fifteen antimicrobial agents were evaluated: ceftiofur, cefotaxime (CTX), ceftazidime (CAZ), meropenem, amoxicillin, ampicillin, colistin, amikacin, kanamycin, gentamicin, doxycycline, tetracycline, ciprofloxacin, enrofloxacin, and trimethoprim–sulfamethoxazole.
Screening and confirmation of ESBL-producing E. coli ST131
ST131 isolates were initially screened for extended-spectrum β-lactamase (ESBL) production using CHROMagar ESBL selective medium (CHROMagar, Paris, France). Presumptive ESBL-positive isolates were further confirmed phenotypically using the CLSI combination disk diffusion method with ceftazidime, ceftazidime–clavulanic acid, cefotaxime, and cefotaxime–clavulanic acid disks. ESBL production was confirmed when the inhibition zone diameter increased by ≥5 mm in the presence of clavulanic acid. Klebsiella pneumoniae ATCC 700603 and E. coli ATCC 25922 were used as positive and negative controls, respectively.
AmpC-β-lactamase phenotype test
AmpC β-lactamase production was evaluated using cefotetan/cefotetan-cloxacillin gradient strips according to the method of Polsfuss et al. [22]. A ratio of the MIC of cefotetan alone to that of cefotetan plus cloxacillin of ≥8 was interpreted as positive for AmpC β-lactamase production. K. pneumoniae ATCC 700603 and strains previously confirmed as AmpC-β-lactamase producers served as the negative and positive controls, respectively.
Detection of β-lactamase genes of E. coli ST131
ESBL- or AmpC-producing ST131 isolates were screened by PCR for common β-lactamase genes. Target genes included blaTEM, blaSHV, blaCTX-M groups (blaCTX-M-1, −2, −8, −9, and −25) [23–27], and plasmid-mediated AmpC genes (blaCIT, blaDHA, blaMOX, blaCMY, blaEBC, and blaFOX) [28]. Amplicons of the expected size were sequenced, and sequences were compared with entries in the Beta-Lactamase Database and NCBI databases (https://www.ncbi.nlm.nih.gov/pathogens/beta-lactamase-data-resources/). The primers used for detecting β-lactamase genes are listed in S4 Table.
O-antigen and fimH subclone typing
O-antigen typing focused on the two serotypes most commonly associated with ST131, O25b and O16. Multiplex PCR targeting pabB (O25b) and trpA (O16) was performed as previously described [29,30]. fimH subclone typing was conducted by multiplex PCR to detect fimH22, fimH27, fimH30, fimH30Rx, fimH35, and fimH41 [31]. The primers used for these assays are listed in S5 Table.
Plasmid replicon typing
Plasmid replicon types were determined by multiplex PCR using the method of Johnson et al [32]. Detected plasmids were classified according to incompatibility (Inc) groups. S6 Table lists the primers for plasmid replicon typing.
Conjugation test
Conjugation experiments were performed to evaluate horizontal transfer of β-lactamase genes. ST131 isolates were used as donor strains, and sodium azide-resistant E. coli J53 (ATCC BAA-2730) served as the recipient strain. Donor and recipient cultures were mixed and incubated overnight, and transconjugants were selected on Mueller–Hinton agar containing cefotaxime (2 mg/L) and sodium azide (150 mg/L) [33]. Putative transconjugants were confirmed by PCR for the corresponding resistance genes.
Statistical analysis
This study primarily used descriptive statistics. The prevalence of phylogenetic groups, ST131 isolates, virulence genes, antimicrobial resistance phenotypes, β-lactamase genes, O-antigen types, fimH subclones, and plasmid replicon types was summarized as counts and percentages. No inferential statistical comparisons were performed because the study was designed to characterize the molecular features of ST131 isolates rather than to test predefined hypotheses between groups.
Results
E. coli phylogenetic grouping
A total of 400 E. coli isolates were recovered from urine samples of dogs and cats diagnosed with urinary tract infections at the National Taiwan University Veterinary Hospital between December 6, 2011, and November 13, 2019. Of these, 314 isolates (78.5%) were obtained from dogs and 86 (21.5%) from cats. Phylogenetic grouping showed that group B2 was the most prevalent group (192/400, 48.0%), including 144 isolates from dogs (75.0%) and 48 from cats (25.0%). The remaining isolates were assigned to group E (52/400, 13.0%), group B1 (39/400, 9.8%), group A (12/400, 3.0%), group D (7/400, 1.8%), group F (5/400, 1.3%), group C (4/400, 1.0%), and clade I (2/400, 0.5%). In addition, 87 isolates (21.8%) could not be assigned to any phylogenetic group. S1 Fig shows a representative agarose gel of E. coli phylogenetic grouping.
Screening and confirmation of E. coli ST131
Among the 192 phylogroup B2 isolates, 26 (13.5%) were positive for ST131-associated SNP markers. Most of these isolates were recovered from dogs (22/26, 84.6%), whereas four isolates (15.4%) were obtained from cats. Multilocus sequence typing confirmed that all 26 putative isolates belonged to sequence type 131. Seven isolates had been included in previous studies investigating ESBL-producing E. coli [14]; therefore, the remaining 19 ST131 isolates were selected for further characterization in the present study.
Detection of virulence genes
All 19 ST131 isolates carried fyuA (19/19, 100.0%). None were positive for focG (0/19, 0.0%). The prevalence of the remaining virulence genes was as follows: traT (18/19, 94.7%), iutA (17/19, 89.5%), kpsMT II (16/19, 84.2%), K5 (9/19, 47.4%), papAH (5/19, 26.3%), cnf1 (3/19, 15.8%), ibeA (3/19, 15.8%), K1 (2/19, 10.5%), hlyA (2/19, 10.5%), and sfa/focDE (1/19, 5.3%). Detailed virulence profiles of each isolate are presented in Table 1.
Antimicrobial susceptibility test
All ST131 isolates were resistant to amoxicillin and ampicillin, whereas all remained susceptible to meropenem. Resistance rates for the other tested antimicrobials were as follows: ceftiofur and ciprofloxacin (95%), cefotaxime and gentamicin (74%), trimethoprim–sulfamethoxazole (63%), enrofloxacin (58%), and tetracycline (53%). The proportions of susceptible, intermediate, and resistant isolates for each antimicrobial agent are shown in S2 Fig. Individual isolate profiles are summarized in Table 1.
O-antigen, fimH subclone, and plasmid replicon typing
Only two O-antigen types, O25b and O16, were identified among the ST131 isolates. Four fimH subtypes—fimH22, fimH27, fimH30, and fimH41—were detected. Notably, all O16 isolates belonged exclusively to the fimH41 subtype (Table 1). Plasmid replicon typing identified multiple incompatibility groups, with detailed results summarized in Table 2.
Detection of β-lactamase genes and conjugation test
Among the 19 ST131 isolates, five carried ESBL genes and one carried an AmpC gene; all six isolates were recovered from dogs. The only AmpC gene detected was blaCMY-178 (case 10), which was successfully transferred to the E. coli J53 recipient strain. The ESBL-producing isolates carried blaCTX-M-1-group (CTX-M-55), blaCTX-M-9-group (CTX-M-17 and CTX-M-27), and blaTEM group genes (TEM-12 and TEM-102). Notably, only blaCTX-M-9-group genes were successfully transferred in conjugation experiments, whereas blaCTX-M-55 and blaTEM variants were not transferred. Detailed results for donor strains, transconjugants, and plasmid replicon types are presented in Table 2.
Discussion
This study identified E. coli ST131 in 6.5% of urinary E. coli isolates recovered from companion animals in Taiwan. This prevalence was higher than that reported in previous studies from Germany (3.5%) [34] and from healthy dogs in Taiwan (2.3%) [13]. The higher prevalence observed in the present study may reflect differences in sampling populations, antimicrobial exposure, or regional epidemiological patterns.
Among the virulence-associated genes examined, fyuA was the most frequently detected and was present in all ST131 isolates. The fyuA gene encodes the receptor of the yersiniabactin iron-acquisition system, which enhances bacterial fitness in iron-limited host environments and has been widely associated with uropathogenic E. coli [35]. The distribution of virulence genes in ST131 isolates appears to vary geographically and across host species. Previous studies in Europe reported associations between companion-animal ST131 isolates and ibeA or kpsMT II, whereas only kpsMT II was highly prevalent in the present study and ibeA was detected less frequently [34]. Another study reported no significant correlations among the virulence genes traT, cnf1, and fyuA [34]. However, the detection rates of fyuA and traT in the present ST131 isolates were notably high—100.0% (19/19) and 94.8% (18/19), respectively. These findings suggest that the prevalence of virulence genes in ST131 isolates may vary across geographic regions. The prevalence of virulence genes in ST131 isolates also varies across studies. For example, in a study conducted in Iran, fyuA was detected in all ST131 isolates (100.0%), consistent with the findings of the present study. The detection rates of other genes—such as ibeA (1.4%), traT (95.7%), and K5 (49.3%)—were also similar to those observed in the present study. However, the detection rates of cnf1 (26.1%) and hlyA (29.0%) were higher than those reported in the present study [36].
The distribution and detection rates of ESBL and AmpC beta-lactamase genotypes in ST131 isolates also vary globally. Studies have shown that in most Asian countries—including Taiwan, China, and Japan, but excluding India—blaCTX-M-14 of the CTX-M-9 group is the most common ESBL genotype in ST131 isolates. blaCTX-M-15 of the CTX-M-1 group is also prevalent in ST131 isolates in Japan but relatively rare in those from Indonesia and China [37]. However, although blaCTX-M-15, which is predominantly detected in Europe, was not identified in the ST131 isolates analyzed in this study, the most frequently detected ESBL genes were blaCTX-M-17 (n = 3) and blaCTX-M-27 (n = 2), both belonging to the CTX-M-9 group. One strain carrying blaCTX-M-17 and another carrying blaCTX-M-27 also harbored blaCTX-M-55, a genotype belonging to the CTX-M-1 group. blaCTX-M-55 has been widely detected in food-producing and companion animals in China, and its geographic distribution is largely concentrated in Asia [27,38,39]. A study conducted in the United Kingdom reported that the detection rate of blaCTX-M-15, previously the dominant ESBL variant in Europe, has declined and has been increasingly replaced by blaCTX-M-55 [40]. Among the AmpC-related genotypes, blaCMY-178, a novel variant of blaCMY, was the only one identified in this study (carried by ST131 case 10). In both human and animal specimens, blaCMY-related genotypes are frequently detected in E. coli, with blaCMY-2 being the most prevalent variant. These genes are commonly located on IncA/C and IncI plasmids [41,42]. Studies have shown that blaCMY-178 confers higher resistance to ceftazidime–avibactam (CAZ–AVI) than blaCMY-172, another CAZ–AVI resistance gene [43].
In the conjugation test conducted in this study, ESBL/AmpC-producing strains carrying a single β-lactamase gene successfully transferred the gene to the recipient strain. In contrast, two strains harboring multiple β-lactamase genes (494 and 668) each transferred only one. Specifically, strain 494 (blaCTX-M-55+CTX-M-17+TEM-102) transferred only blaCTX-M-17, and strain 668 (blaCTX-M-55+CTX-M-27+TEM-12) transferred only blaCTX-M-27, both of which belong to the CTX-M-9 group. A possible explanation for this selective transfer is that the β-lactamase genes are located on different plasmids. Previous studies have further indicated that certain ESBL and AmpC genotypes are strongly associated with specific plasmid types [44–46]. This may indicate that different genes were located on distinct plasmids with variable transfer efficiencies, or that transfer conditions were suboptimal for certain plasmid types. Therefore, failure of transfer in vitro should not be interpreted as evidence of non-transferability in natural settings.
Among the ST131 isolates examined in this study, IncF (19/19, 100.0%) and IncB/O (15/19, 78.9%) were the most frequently detected plasmid types. IncF plasmids were identified in all ST131 isolates, consistent with previous reports showing strong associations between ST131 and IncF plasmid lineages [47]. These plasmids commonly carry antimicrobial resistance determinants and virulence-associated genes, thereby contributing to the successful global dissemination of ST131 [48,49].
A proportion of isolates could not be assigned to a phylogenetic group using the Clermont quadruplex PCR method. This may be attributable to sequence variation in primer-binding regions, inherent limitations of the PCR-based typing scheme, or variation in DNA quality among archived isolates. Future whole-genome sequencing studies may improve phylogenetic resolution. Capsule-associated virulence factors, including K1, have been reported in certain extraintestinal pathogenic E. coli (ExPEC) lineages, particularly those associated with invasive infections such as neonatal meningitis [5,20]. However, previous studies of ST131 have shown considerable variability in virulence gene profiles across subclones and host sources [9,31], and a consistent association between specific fimH subclones, including fimH22, and K1 capsule has not been clearly established. In the present study, only one of the three fimH22 isolates was K1-positive by PCR, suggesting heterogeneity among companion-animal-derived ST131 isolates. This variation may reflect differences in genetic background, host adaptation, or selective pressures across ecological niches.
This study has several limitations. First, the isolates were obtained from a single veterinary teaching hospital and may not fully represent the broader companion-animal population in Taiwan. Second, the number of confirmed ST131 isolates available for detailed characterization was limited. Third, whole-genome sequencing was not performed and could provide additional insights into clonality, resistance gene context, and transmission dynamics. Despite these limitations, the present study provides valuable baseline data on the prevalence, resistance characteristics, and virulence-associated profiles of E. coli ST131 from dogs and cats with urinary tract infections in Taiwan. Continued surveillance of this high-risk lineage is warranted under a One Health framework.
Conclusion
This study demonstrated the presence of E. coli ST131 among dogs and cats with urinary tract infections in Taiwan. Most isolates exhibited multidrug resistance and carried multiple virulence-associated genes, highlighting the clinical relevance of this lineage in companion animals. The detection of transferable β-lactamase genes and globally recognized ST131 subclones further underscores the potential public health importance of these isolates. Continued molecular surveillance and prudent antimicrobial stewardship in veterinary medicine are warranted within a One Health framework.
Supporting information
S1 Table. Primers used for E. coli phylogenetic grouping.
https://doi.org/10.1371/journal.pone.0350088.s001
(DOCX)
S3 Table. Primers used for virulence gene detection.
https://doi.org/10.1371/journal.pone.0350088.s003
(DOCX)
S4 Table. Primers used for detecting β-lactamase genes in E. coli.
https://doi.org/10.1371/journal.pone.0350088.s004
(DOCX)
S5 Table. Primers used for O-antigen and fimH subclone typing.
https://doi.org/10.1371/journal.pone.0350088.s005
(DOCX)
S6 Table. Primers used for plasmid replicon typing.
https://doi.org/10.1371/journal.pone.0350088.s006
(DOCX)
S1 Fig. Quadruplex PCR profiles for Clermont phylogenetic grouping.
https://doi.org/10.1371/journal.pone.0350088.s007
(JPG)
S2 Fig. Antimicrobial susceptibility profiles of E. coli ST131 isolates (n = 19).
https://doi.org/10.1371/journal.pone.0350088.s008
(JPG)
Acknowledgments
The authors gratefully acknowledge Dr. Lee-Jene Teng (Department of Clinical Laboratory Sciences and Medical Biotechnology, National Taiwan University) for kindly providing K. pneumoniae ATCC 700603. We also thank Dr. Chao-Tsai Liao (Department of Medical Laboratory Science and Biotechnology, Central Taiwan University of Science and Technology) for generously providing E. coli J53.
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