Multidrug-Resistant Uropathogens in Companion Animals: A Comprehensive Study from Clinical Cases and a Genomic Analysis of a CTX-M-14-Producing Escherichia coli ST354,a Leading Cause of Urinary Tract Infections
Restricted accessResearch articleFirst published online April, 2025
Multidrug-Resistant Uropathogens in Companion Animals: A Comprehensive Study from Clinical Cases and a Genomic Analysis of a CTX-M-14-Producing Escherichia coli ST354,a Leading Cause of Urinary Tract Infections
Urinary tract infections (UTIs) are common in small animals, posing significant clinical challenges due to their recurrence and discomfort. This study investigated the bacterial causes and antimicrobial resistance patterns of UTIs in dogs and cats presented to an important Veterinary Teaching Hospital in São Paulo, Brazil, the largest city in Latin America. Samples were collected from 31 dogs and 9 cats via ultrasound-guided cystocentesis. Bacterial cultures were performed, species identification was accomplished with matrix-assisted laser desorption ionization-time of flight mass spectrometry, and antimicrobial susceptibility testing was done using the Kirby–Bauer method. Escherichia coli was the most frequently isolated pathogen, accounting for 27.9% of cases, followed by Staphylococcus pseudintermedius, Proteus mirabilis, and Klebsiella pneumoniae. Ampicillin resistance was observed in 70.4% of enterobacteria, with many E. coli strains exhibiting multidrug resistance. Whole-genome sequencing of an extended-spectrum beta-lactamase-producing uropathogenic Escherichia coli strain from a feline patient was performed; it was identified as ST354, a leading cause of UTIs worldwide in humans and animals, carrying the blaCTX-M-14 gene and other resistance determinants. Phylogenetic analysis indicated genetic proximity between this strain and others from Brazilian poultry and environmental sources. These findings emphasize the need for antimicrobial resistance surveillance in veterinary UTIs and advocate for stricter antibiotic stewardship to inform diagnostic and therapeutic approaches within a One Health perspective.
Get full access to this article
View all access options for this article.
References
1.
BarsantiJ. Genitourinary Infections. In: Infectious Diseases of the Dog and Cat W.B. Sauders: Philadelphia; 2006; pp. 626–646.
2.
JericóM, NetoJ, KogikaM. Tratado de Medicina Interna de Cães e Gatos. (JericóMM, NetoJPA, KogikaMM. eds). Roca: Rio de Janeiro; 2015.
3.
ByronJK. Urinary tract infection. Vet Clin North Am Small Anim Pract, 2019; 49(2):211–221; doi: 10.1016/j.cvsm.2018.11.005
4.
BienJ, SokolovaO, BozkoP. Role of uropathogenic Escherichia coli virulence factors in development of urinary tract infection and kidney damage. Int J Nephrol, 2012; 2012:681473; doi: 10.1155/2012/681473
5.
EtefiaE. Virulence factors of uropathogenic Escherichia coli. In: Escherichia Coli—Old and New Insights. IntechOpen; 2023; doi: 10.5772/intechopen.99891
6.
Lee VentolaC. The antibiotic resistance crisis part 1: Causes and threats. P T, 2015; 40(4):277–283.
7.
ThompsonMF, LitsterAL, PlatellJL, et al.Canine bacterial urinary tract infections: New developments in old pathogens. Vet J, 2011; 190(1):22–27; doi: 10.1016/J.TVJL.2010.11.013
8.
FayezM, ElmoslemanyA, Al RomaihiAA, et al.Prevalence and risk factors associated with multidrug resistance and extended-spectrum β-lactamase producing E. coli isolated from healthy and diseased cats. Antibiotics (Basel), 2023; 12(2); doi: 10.3390/antibiotics12020229
9.
Abad-FauA, SevillaE, OroA, et al.Multidrug resistance in pathogenic Escherichia coli isolates from urinary tract infections in dogs, Spain. Front Vet Sci, 2024; 11:1325072; doi: 10.3389/fvets.2024.1325072
10.
McEwenSA, CollignonPJ. Antimicrobial resistance: A one health perspective. Microbiol Spectr, 2018; 6(2); doi: 10.1128/microbiolspec.arba-0009-2017
11.
CaneschiA, BardhiA, BarbarossaA, et al.The use of antibiotics and antimicrobial resistance in veterinary medicine, a complex phenomenon: A narrative review. Antibiotics (Basel), 2023; 12(3); doi: 10.3390/antibiotics12030487
12.
ProcopGG, ChurchDL, HallGS, et al.Koneman’s Color Atlas and Textbook of Diagnostic Microbiology. 7th ed. Jones & Bartlett Learnin; 2020.
13.
BartgesJW. Diagnosis of urinary tract infections. Vet Clin North Am Small Anim Pract, 2004; 34(4):923–933, vi; doi: 10.1016/J.CVSM.2004.03.001
CLSI. Performance Standards for Antimicrobial Susceptibility Testing. 8th Ed. CLSI Supplement M100. Clinical and Laboratory Standards Institute. 2022. Available from: https://clsi.org/all-free-resources/ [Last accessed: October29, 2024].
17.
WickRR, JuddLM, GorrieCL, et al.Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol, 2017; 13(6):e1005595; doi: 10.1371/journal.pcbi.1005595
PalC, Bengtsson-PalmeJ, RensingC, et al.BacMet: Antibacterial biocide and metal resistance genes database. Nucleic Acids Res, 2014; 42(Database issue):D737–D743; doi: 10.1093/nar/gkt1252
20.
DosterE, LakinSM, DeanCJ, et al.MEGARes 2.0: A database for classification of antimicrobial drug, biocide and metal resistance determinants in metagenomic sequence data. Nucleic Acids Res, 2020; 48(D1):D561–D569; doi: 10.1093/nar/gkz1010
21.
ZankariE, HasmanH, CosentinoS, et al.Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother, 2012; 67(11):2640–2644; doi: 10.1093/jac/dks261
22.
AlcockBP, RaphenyaAR, LauTTY, et al.CARD 2020: Antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res, 2020; 48(D1):D517–D525; doi: 10.1093/nar/gkz935
23.
CarattoliA, ZankariE, García-FernándezA, et al.In silico detection and typing of plasmids using plasmidfinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother, 2014; 58(7):3895–3903; doi: 10.1128/AAC.02412-14
24.
Arredondo-AlonsoS, RogersMRC, BraatJC, et al.Corrigendum: Mlplasmids: A user-friendly tool to predict plasmid- and chromosome-derived sequences for single species. Microb Genom, 2019; 5(1); doi: 10.1099/mgen.0.000249
25.
RoerL, TchesnokovaV, AllesøeR, et al.Development of a web tool for Escherichia coli subtyping based on fimH Alleles. J Clin Microbiol, 2017; 55(8):2538–2543; doi: 10.1128/JCM.00737-17
26.
BeghainJ, Bridier-NahmiasA, Le NagardH, et al.ClermonTyping: An easy-to-use and accurate in silico method for Escherichia genus strain phylotyping. Microb Genom, 2018; 4(7); doi: 10.1099/mgen.0.000192
27.
PageAJ, CumminsCA, HuntM, et al.Roary: Rapid large-scale prokaryote pan genome analysis. Bioinformatics, 2015; 31(22):3691–3693; doi: 10.1093/bioinformatics/btv421
MagiorakosA-P, SrinivasanA, CareyRB, et al.Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect, 2012; 18(3):268–281; doi: 10.1111/j.1469-0691.2011.03570.x
30.
WHO. Critically Important Antimicrobials for Human Medicine: 6th Revision. WHO; 2018.
31.
KrzywinskiM, ScheinJ, Birolİ, et al.Circos: An information aesthetic for comparative genomics. Genome Res, 2009; 19(9):1639–1645; doi: 10.1101/gr.092759.109
32.
DorschR, Teichmann-KnorrnS, Sjetne LundH. Urinary tract infection and subclinical bacteriuria in cats: A clinical update. J Feline Med Surg, 2019; 21(11):1023–1038; doi: 10.1177/1098612X19880435
33.
Von Vopelius-FeldtC. Bakterielle Harnwegsinfektionen Bei Der Katze—Eine Retrospektive Tiber 10 Jahre. Doctoral thesis. Ludwig Maximilian University Munich: Munich; 2012.
34.
HernandoE, VilaA, D’IppolitoP, et al.Prevalence and characterization of urinary tract infection in owned dogs and cats from Spain. Top Companion Anim Med, 2021; 43:100512; doi: 10.1016/j.tcam.2021.100512
35.
OsuguiL, Pestana de CastroAF, IovineR, et al.Virulence genotypes, antibiotic resistance and the phylogenetic background of extraintestinal pathogenic Escherichia coli isolated from urinary tract infections of dogs and cats in Brazil. Vet Microbiol, 2014; 171(1–2):242–247; doi: 10.1016/J.VETMIC.2014.03.027
36.
FonsecaJD, MavridesDE, GrahamPA, et al.Results of urinary bacterial cultures and antibiotic susceptibility testing of dogs and cats in the UK. J Small Anim Pract, 2021; 62(12):1085–1091; doi: 10.1111/jsap.13406
37.
GarcêsA, LopesR, SilvaA, et al.Bacterial isolates from urinary tract infection in dogs and cats in Portugal, and their antibiotic susceptibility pattern: A retrospective study of 5 years (2017–2021). Antibiotics, 2022; 11(11):1520; doi: 10.3390/antibiotics11111520
38.
FlemingA. Sir Alexander Fleming Banquet Speech. The Nobel Foundation; 1945.
39.
JungWK, ShinS, ParkYK, et al.Distribution and antimicrobial resistance profiles of bacterial species in stray cats, hospital-admitted cats, and veterinary staff in South Korea. BMC Vet Res, 2020; 16(1):109; doi: 10.1186/s12917-020-02326-2
40.
Dastmalchi SaeiH, PanahiM. Genotyping and antimicrobial resistance of Staphylococcus aureus isolates from dairy ruminants: Differences in the distribution of clonal types between cattle and small ruminants. Arch Microbiol, 2020; 202(1):115–125; doi: 10.1007/s00203-019-01722-z
41.
Carrillo GaetaN, Cavalcante BritoJE, Nunes BatistaJM, et al.Bats are carriers of antimicrobial-resistant staphylococcaceae in their skin. Antibiotics (Basel), 2023; 12(2):331; doi: 10.3390/antibiotics12020331
42.
NoceraFP, PizzanoF, MasulloA, et al.Antimicrobial resistant staphylococcus species colonization in dogs, their owners, and veterinary staff of the veterinary teaching Hospital of Naples, Italy. Pathogens, 2023; 12(8):1016; doi: 10.3390/pathogens12081016
43.
SmoglicaC, EvangelistiG, FaniC, et al.Antimicrobial resistance profile of bacterial isolates from urinary tract infections in companion animals in central italy. Antibiotics (Basel), 2022; 11(10):1363; doi: 10.3390/antibiotics11101363
44.
DarwichL, SeminatiC, BurballaA, et al.Antimicrobial susceptibility of bacterial isolates from urinary tract infections in companion animals in Spain. Vet Rec, 2021; 188(9):e60; doi: 10.1002/vetr.60
45.
AurichS, Prenger-BerninghoffE, EwersC. Prevalence and antimicrobial resistance of bacterial uropathogens isolated from dogs and cats. Antibiotics (Basel), 2022; 11(12):1730; doi: 10.3390/antibiotics11121730
46.
KimES, HooperDC. Clinical importance and epidemiology of quinolone resistance. Infect Chemother, 2014; 46(4):226–238; doi: 10.3947/ic.2014.46.4.226
47.
RobicsekA, JacobyGA, HooperDC. The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect Dis, 2006; 6(10):629–640; doi: 10.1016/S1473-3099(06)70599-0
48.
ValverdeA, CantónR, Garcillán-BarciaMP, et al.Spread of blaCTX-M-14 is driven mainly by IncK plasmids disseminated among Escherichia coli phylogroups A, B1, and D in Spain. Antimicrob Agents Chemother, 2009; 53(12):5204–5212; doi: 10.1128/AAC.01706-08
49.
BonnetR. Growing group of extended-spectrum β-lactamases: The CTX-M enzymes. Antimicrob Agents Chemother, 2004; 48(1):1–14; doi: 10.1128/AAC.48.1.1-14.2004
50.
YoonE-J, ChoiYJ, KimD, et al.Amplification of the chromosomal blaCTX-M-14 gene in Escherichia coli expanding the spectrum of resistance under antimicrobial pressure. Microbiol Spectr, 2022; 10(3):e0031922; doi: 10.1128/spectrum.00319-22
51.
ArduinoSM, RoyPH, JacobyGA, et al.blaCTX-M-2 is located in an unusual class 1 integron (In35) which includes Orf513. Antimicrob Agents Chemother, 2002; 46(7):2303–2306; doi: 10.1128/AAC.46.7.2303-2306.2002
52.
LiaoX-P, XiaJ, YangL, et al.Characterization of CTX-M-14-producing Escherichia coli from food-producing animals. Front Microbiol, 2015; 6:1136; doi: 10.3389/fmicb.2015.01136
53.
HamamotoK, UedaS, ToyosatoT, et al.High prevalence of chromosomal blaCTX-M-14 in Escherichia coli isolates possessing bla CTX-M-14. Antimicrob Agents Chemother, 2016; 60(4):2582–2584; doi: 10.1128/AAC.00108-16
54.
RomeK, BordeC, TaherR, et al.The two-component system ZraPSR is a novel ESR that contributes to intrinsic antibiotic tolerance in Escherichia coli. J Mol Biol, 2018; 430(24):4971–4985; doi: 10.1016/j.jmb.2018.10.021
55.
Baker-AustinC, WrightMS, StepanauskasR, et al.Co-selection of antibiotic and metal resistance. Trends Microbiol, 2006; 14(4):176–182; doi: 10.1016/j.tim.2006.02.006
56.
PalC, AsianiK, AryaS, et al.Metal resistance and its association with antibiotic resistance. Adv Microb Physiol, 2017; 70:261–313; doi: 10.1016/bs.ampbs.2017.02.001
57.
SpurbeckRR, DinhPC, WalkST, et al.Escherichia coli isolates that carry vat, fyuA, chuA, and yfcV efficiently colonize the urinary tract. Infect Immun, 2012; 80(12):4115–4122; doi: 10.1128/IAI.00752-12
58.
BundukiGK, HeinzE, PhiriVS, et al.Virulence factors and antimicrobial resistance of uropathogenic Escherichia coli (UPEC) isolated from urinary tract infections: A systematic review and meta-analysis. BMC Infect Dis, 2021; 21(1):753; doi: 10.1186/s12879-021-06435-7
59.
LiuQ, ZhuJ, LiuN, et al.Type I fimbriae subunit fimA enhances Escherichia coli biofilm formation but affects L-threonine carbon distribution. Front Bioeng Biotechnol, 2022; 10:904636; doi: 10.3389/fbioe.2022.904636
60.
SpauldingC, HultgrenS. Adhesive pili in UTI pathogenesis and drug development. Pathogens, 2016; 5(1):30; doi: 10.3390/pathogens5010030
61.
HaganEC, MobleyHLT. Haem acquisition is facilitated by a novel receptor Hma and required by uropathogenic Escherichia coli for kidney infection. Mol Microbiol, 2009; 71(1):79–91; doi: 10.1111/j.1365-2958.2008.06509.x
62.
GuoS, WakehamD, BrouwersHJM, et al.Human-associated fluoroquinolone-resistant Escherichia coli clonal lineages, including ST354, isolated from canine feces and extraintestinal infections in Australia. Microbes Infect, 2015; 17(4):266–274; doi: 10.1016/j.micinf.2014.12.016
63.
MoraA, BlancoM, LópezC, et al.Emergence of clonal groups O1:HNM-D-ST59, O15:H1-D-ST393, O20:H34/HNM-D-ST354, O25b:H4-B2-ST131 and ONT:H21,42-B1-ST101 among CTX-M-14-producing Escherichia coli clinical isolates in Galicia, northwest Spain. Int J Antimicrob Agents, 2011; 37(1):16–21; doi: 10.1016/J.IJANTIMICAG.2010.09.012
64.
TamangMD, NamH-M, JangG-C, et al.Molecular characterization of extended-spectrum-β-lactamase-producing and plasmid-mediated AmpC β-Lactamase-producing Escherichia coli isolated from Stray Dogs in South Korea. Antimicrob Agents Chemother, 2012; 56(5):2705–2712; doi: 10.1128/AAC.05598-11
65.
Salgado-CaxitoM, BenavidesJA, MunitaJM, et al.Risk factors associated with faecal carriage of extended-spectrum cephalosporin-resistant Escherichia coli among dogs in Southeast Brazil. Prev Vet Med, 2021; 190:105316; doi: 10.1016/j.prevetmed.2021.105316
66.
VangchhiaB, AbrahamS, BellJM, et al.Phylogenetic diversity, antimicrobial susceptibility and virulence characteristics of phylogroup F Escherichia coli in Australia. Microbiology (Reading), 2016; 162(11):1904–1912; doi: 10.1099/mic.0.000367
67.
ZamparetteCP, SchornerM, CamposE, et al.IncX4 plasmid-mediated mcr-1.1 in polymyxin-resistant Escherichia coli from outpatients in Santa Catarina, Southern Brazil. Microb Drug Resist, 2020; 26(11):1326–1333; doi: 10.1089/mdr.2019.0203
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
