Antimicrobial Susceptibilities, Its Resistance Mechanisms, Virulence Determinants and Phylogenetic Groups of Escherichia coli Isolated From Different Clinical Animal Samples


Published: Apr 19, 2025
Keywords:
Antimicrobial Resistance Clermont’s phylogenetic typing Escherichia coli Virulence
Ö Aslantaş
https://orcid.org/0000-0003-0407-8633
F Sakin
M Bayırlı Nacaroğlu
Oktay Keskin
Ayfer Güllü Yücetepe
BG Celic
SA Şengül
Abstract

Escherichia coli is a versatile agent, as some are commensals, normally living in the intestines of both
humans and animals, while others are pathogenically responsible for a wide variety of intestinal and extra-intestinal infections
including urinary tract infections (UTIs), meningitis, septicemia, bovine mastitis and colibacillosis in poultry.
The present study aims to determine the antimicrobial susceptibilities, its underlying genetic resistance mechanisms,
distribution of phylogroups, and virulence determinants of 42 E. coli isolates from different clinical sources of animals.
Our results have revealed that phylogroup A1 (42.9%) and B1 (40.5%) were the most prevalent phylogenetic groups
with different virulence profiles and varying incidence of virulence determinants. High rates of resistance to different
categories of antimicrobial agents with high rate of MDR (59.5%). Phylogenetic analysis showcased remarkable diversity
among the tested isolates, with no discernible clustering based on antimicrobial resistance or virulence patterns.
Our research has demonstrated the significant phylogenetic diversity of E. coli isolated from different clinical samples.
E. coli isolates are endowed with various virulence factors that contribute to their pathogenesis in animals. The elevated
rates of antimicrobial resistance and emergence of MDR mirror the trend detected globally in recent years.

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References
Acik MN, Yurdakul NE, Cakici L, Onat N, Dogan O, Cetinkaya B (2004)
TraT and CNF2 genes of Escherichia coli isolated from milk of
healthy cows and sheep. Res Vet Sci 77: 17-21.
Aslantaş Ö (2020) High occurrence of CMY-2-type beta-lactamase-producing
Escherichia coli among broiler flocks in Turkey. Trop Anim
Health Prod 52(4):1681-1689.
Aslantaş Ö (2018) Antimicrobial resistance among commensal Escherichia
coli from broilers in Turkey. Isr J Vet Med 73(3):19-24.
Aslantaş Ö, Korkut AM, Bayırlı Nacaroğlu M (2023) Isolation and characterization
of cefotaxime and ciprofloxacin co-resistant Escherichia
coli in retail chicken carcasses. Harran Üniv Vet Fak Derg 12(2):228-
Awad WS, El-Sayed AA, Mohammed FF, Bakry NM, Abdou NMI, Kamel
MS (2020) Molecular characterization of pathogenic Escherichia coli
isolated from diarrheic and in-contact cattle and buffalo calves. Trop
Anim Health Prod 52(6):3173-3185.
Aworh MK, Kwaga JKP, Hendriksen RS, Okolocha EC, Thakur S (2021)
Genetic relatedness of multidrug resistant Escherichia coli isolated
from humans, chickens and poultry environments. Antimicrob
Resist Infect Control 10(1):58.
Azam M, Mohsin M, Johnson TJ, Smith EA, Johnson A, Umair M, Saleemi
MK, Sajjadur R (2020) Genomic landscape of multi-drug resistant
avian pathogenic Escherichia coli recovered from broilers. Vet
Microbiol 247:108766.
Börjesson S, Jernberg C, Brolund A, Edquist P, Finn M, Landén A,Olsson-
Liljequist B, Wisell KT, Bengtsson B, Englund S (2013) Characterization
of plasmid-mediated AmpC-producing E. coli from
Swedish broilers and association with human clinical isolates. Clin
Microbiol Infect 19:E309-E311.
Caneschi A, Bardhi A, Barbarossa A, Zaghini A (2023) The use of antibiotics
and antimicrobial resistance in veterinary medicine, a complex
phenomenon: a narrative review. Antibiotics (Basel) 12(3):487.
Cengiz S, Adıgüzel MC (2020) Determination of virulence factors and
antimicrobial resistance of E. coli isolated from calf diarrhea, part of
eastern Turkey. Ankara Univ Vet Fak Derg 67:365-371.
Chinemerem Nwobodo D, Ugwu MC, Oliseloke Anie C, Al-Ouqaili
MTS, Chinedu Ikem J, Victor Chigozie U, Saki M (2022) Antibiotic
resistance: The challenges and some emerging strategies for strategies
for tackling a global menace. J Clin Lab Anal 36(9):e24655.
Clermont O, Bonacorsi S, Bingen E (2000) Rapid and simple determination
of the Escherichia coli phylogenetic group. App Environ Microbiol
:4555-4558.
Clinical and Laboratory Standards Institute (CLSI): Performance standards
for antimicrobial susceptibility testing. CLSI Document:
M100-32, 2022. Wayne, PA, USA.
Dubreuil JD (2019) EAST1 toxin: an enigmatic molecule associated with
sporadic episodes of diarrhea in humans and animals. J Microbiol
(7):541-549.
El‑baz R, Said HS, Abdelmegeed ES, Barwa R (2022) Characterization
of virulence determinants and phylogenetic background of multiple
and extensively drug resistant Escherichia coli isolated from diferent
clinical sources in Egypt. Appl Microbiol Biotechnol 106:1279-1298.
El-Shaer S, Abdel-Rhman SH, Barwa R, Hassan R (2018) Virulence
Characteristics, serotyping and phylogenetic typing of clinical and
environmental Escherichia coli isolates. Jundishapur J Microbiol
(12):e82835.
Ewers C, Janssen T, Kiessling S, Philipp HC, Wieler LH (2005) Rapid detection
of virulence-associated genes in avian pathogenic Escherichia
coli by multiplex polymerase chain reaction. Avian Dis 49(2):269-73.
Fabbri A, Travaglione S, Fiorentini C (2010) Escherichia coli cytotoxic
necrotizing factor 1 (CNF1): toxin biology, in vivo applications and
therapeutic potential. Toxins 2(2): 283-296.
Guerra ST, Orsi H, Joaquim SF, Guimarães FF, Lopes BC, Dalanezi FM,
Leite DS, Langoni H, Pantoja JCF, Rall VLM, hernandes RT, Lucheis
SB, Ribeiro MG: Investigation of extra-intestinal pathogenic Escherichia
coli virulence genes, bacterial motility, and multidrug resistance
pattern of strains isolated from dairy cows with different severity
scores of clinical mastitis. J Dairy Sci 103(4): 3606-3614.
Harada K, Asai T, Kojima A, Ishihara K, Takahashi T (2006) Role of
coresistance in the development of resistance to chloramphenicol
in Escherichia coli isolated from sick cattle and pigs. Am J Vet Res
:230-235.
Joseph J, Jennings M, Barbieri N, Zhang L, Adhikari P, Ramachandran
R (2023) Characterization of avian pathogenic Escherichia coli isolated
from broiler breeders with colibacillosis in Mississippi. Poultry
:24-39.
Karczmarczyk M, Abbott Y, Walsh C, Leonard N, Fannin S (2011) Characterization
of multidrug-resistant Escherichia coli isolates from
animals presenting at a university veterinary hospital. Appl Environ
Microbiol 77(20):7104-7112.
Khalifa SM, Abd El-Aziz AM, Hassan R, Abdelmegeed ES (2021) β-lactam
resistance associated with β-lactamase production and porin alteration
in clinical isolates of E. coli and K. pneumoniae. PLoS One
(5):e0251594
Kızıl S, Aydın FE, Önel AU, Yıldırım M, Önlen Güneri C, Çeçen EM
(2024) Determination of subtypes, serogroups, and serotypes, virulence,
and/or toxigenic properties of Escherichia coli isolated from
cattle, sheep, and goat feces by multiplex PCR. Kafkas Univ Vet Fak
Derg, 30 (2), 155-160, 2024.
Kostakioti M, Stathopoulos C (2004) Functional analysis of the tsh autotransporter
from an avian pathogenic Escherichia coli strain. Infect
Immun 72(10):5548-5554.
Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske
CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson
DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber
JT, Monnet DL (2012) Multidrug-resistant, extensively drug-resistant
and pandrug-resistant bacteria: an international expert proposal for
interim standard definitions for acquired resistance. Clin Microbiol
Infect 18(3):268-281.
Maynard C, Bekal S, Sanschagrin F, Levesque RC, Brousseau R, Masson
L, Lariviére S, Harel J (2004) Heterogeneity among virulence and
antimicrobial resistance gene profiles of extraintestinal Escherichia
coli isolates of animal and human origin. J Clin Microbiol 42(12):
-5452.
Miajlovic H and Smith S (2014) Bacterial self-defence: How Escherichia
coli evades serum killing. FEMS Microbiol Lett 354:1-9.
Negeri AA, Mamo H, Gahlot DK, Gurung JM, Seyoum ET, Francis MS
(2023) Characterization of plasmids carrying blaCTX‑M genes among
extra‑intestinal Escherichia coli clinical isolates in Ethiopia. Sci Rep
:8595.
Ng LK, Martin I, Alfa M, Mulvey M (2001) Multiplex PCR for the detection
of tetracycline-resistant genes. Mol Cell Probes, 15:209-215.
Nichols KB, Totsika M, Moriel DG, Lo AW, Yang J, Wurpel DJ, Rossiter
AE, Strugnell RA, Henderson IR, Ulett GC (2016) Molecular characterization
of the vacuolating autotransporter toxin in uropathogenic
Escherichia coli. J Bacteriol 198(10):1487-1498.
Ochoa SA, Cruz-Córdova A, Luna-Pineda VM, Reyes-Grajeda JP,
Cázares-Domínguez V, Escalona G, Sepúlveda-González ME,
López-Montiel F, Arellano-Galindo J, López-Martínez B, Parra-Ortega
I, Giono-Cerezo S, Hernández-Castro R, de la Rosa-Zamboni
D, Xicohtencatl-Cortes J (2016) Multidrug- and extensively drug-resistant
uropathogenic Escherichia coli clinical strains: phylogenetic
groups widely associated with integrons maintain high genetic diversity.
Front Microbiol 7:2042.
O’Keefe A, Hutton TA, Schifferli DM, Rankin SC (2010) First detection
of CTX-M and SHV extended-spectrum beta-lactamases in Escherichia
coli urinary tract isolates from dogs and cats in the United
States. Antimicrob Agents Chemother 54(8):3489-92.
O’Neill L, Manzanilla EG, Ekhlas D, Leonard FC (2023) Antimicrobial
resistance in commensal Escherichia coli of the porcine gastrointestinal
tract. Antibiotics 12:1616.
Paixão AC, Ferreira AC, Fontes M, Themudo P, Albuquerque T, Soares
MC, Fevereiro M, Martins L, de Sá MIC (2016) Detection of virulence-
associated genes in pathogenic and commensal avian Escherichia coli isolates. Poult Sci, 95 (7), 1646-1652.
Pakbin B, Brück WM, Rossen JWA (2021) Virulence factors of enteric
pathogenic Escherichia coli: A Review. Int J Mol Sci 22(18):9922.
Persoons D, Dewulf J, Smet A, Herman L, Heyndrickx M, Martel A, Catry
B, Butaye P, Haesebrouck F (2010) Prevalence and persistence
of antimicrobial resistance in broiler indicator bacteria. Microb Drug
Resist 16:67-74.
Procop G, Church D, Hall G, Janda W, Koneman E, Schrekenberger P,
Woods GL: Koneman’s color atlas and textbook of diagnostic microbiology.
th ed. Lippincott Williams and Wilkins: Philadelphia; 2017.
-6 p.
Ramos S, Silva V, de Lurdes Enes Dapkevicius M, Caniça M, Tejedor-Junco
MT, Igrejas G, Poeta P (2020) Escherichia coli as commensal and
pathogenic bacteria among food-producing Animals: Health implications
of extended spectrum β-Lactamase (ESBL) production. Animals
:2239.
Rehman MU, Zhang H, Iqbal MK, Mehmood K, Huang S, Nabi F, Luo H,
Lan Y, Li J (2017) Antibiotic resistance, serogroups, virulence genes,
and phylogenetic groups of Escherichia coli isolated from yaks with
diarrhea in Qinghai Plateau. China Gut Pathog 9: 24.
Serwecińska L (2020) Antimicrobials and antibiotic-resistant bacteria: A
risk to the environment and to public health. Water 12:3313.Sobhy
NM, Yousef SGA, Aboubakr HA, Nisar M, Nagaraja KV, Mor SK,
Valeris-Chacin RJ, Goyal SM (2020) Virulence factors and antibiograms
of Escherichia coli isolated from diarrheic calves of Egyptian
cattle and water buffaloes. PLoS One 11(5):e0232890.
Sora VM, Meroni G, Martino PA, Soggiu A, Bonizzi L, Zecconi A
(2021) Extraintestinal pathogenic Escherichia coli: virulence factors
and antibiotic resistance. Pathogens 10(11):1355.
Wang H, Zhong Z, Luo Y, Cox E, Devriendt B (2019) Heat-stable enterotoxins
of enterotoxigenic Escherichia coli and their impact on host
immunity. Toxins 11(1):24.
Whelan S, Lucey B, Finn K (2023) Uropathogenic Escherichia coli (UPEC)-
associated urinary tract infections: The molecular basis for challenges
to effective treatment. Microorganisms 11(9):2169.
World Health Organization (WHO) Critically Important Antimicrobials
for Human Medicine, 6th Revision 2018. Geneva, Switzerland, 2019;
Licence: CC BY-NC-SA 3.0 IGO. Available online: https://iris.who.
int/bitstream/handle/10665/312266/9789241515528-eng.pdf.(accessed
on 13 Jan 2024).
Yassin AK, Gong J, Kelly P, Lu G, Guardabassi L, Wei L, Han X, Qiu H,
Price S, Cheng D, Wang C (2017) Antimicrobial resistance in clinical
Escherichia coli isolates from poultry and livestock, China. PLoS
One 12(9):e0185326.
Yılmaz EŞ, Aslantaş Ö (2019) Phylogenetic group/subgroups distributions,
virulence factors, and antimicrobial susceptibility of Escherichia
coli strains from urinary tract Infections in Hatay. Rev Soc Bras
Med Trop 7(53):e20190429.
Zamudio R, Boerlin P, Beyrouthy R, Madec JY, Schwarz S, Mulvey MR,
Zhanel GG, Cormier A, Chalmers G, Bonnet R, Haenni M, Eichhorn
I, Kaspar H, Garcia-Fierro R, Wood JLN, Mather A (2022) Dynamics
of extended-spectrum cephalosporin resistance genes in Escherichia
coli from Europe and North America. Nat Commun 13(1):7490.
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