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J. Food Qual. Hazards Control 2026, 13(1): 40-46 |
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Bagheri M, Ghanbarpour R, Amirpoorsaid Z, Mohseni P, Hesam-Arefi M, Jajarmi M. Turkey (Meleagris gallopavo f. domestica) Meat as a Potential Reservoir for Dissemination of Antimicrobial Resistant and Shigatoxigenic Escherichia coli Strains. J. Food Qual. Hazards Control 2026; 13 (1) :40-46
URL: http://jfqhc.ssu.ac.ir/article-1-1247-en.html
URL: http://jfqhc.ssu.ac.ir/article-1-1247-en.html
Department of Food Science and Technology, Bardsir Faculty of Agriculture, Shahid Bahonar University of Kerman, Kerman, Iran , ma.bagheri@uk.ac.ir
Keywords: Shiga-Toxigenic Escherichia coli, Beta-Lactamase, Antibiotic Resistance, Phylogeny, Turkeys, Abattoirs
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Turkey (Meleagris gallopavo f. domestica) Meat as a Potential
Reservoir for Dissemination of Antimicrobial Resistant and
Shigatoxigenic Escherichia coli Strains
M. Bagheri 1** , R. Ghanbarpour 2, Z. Amirpoorsaid 1, P. Mohseni 3, M. Hesam-Arefi 3, M. Jajarmi 3
1. Department of Food Science and Technology, Bardsir Faculty of Agriculture, Shahid Bahonar University of Kerman, Kerman, Iran
2. Molecular Microbiology Research Group, Shahid Bahonar University of Kerman, Kerman, Iran
3. Department of Pathobiology, Faculty of Veterinary Medicine, Shahid Bahonar University of Kerman, Kerman, Iran
HIGHLIGHTS
Table 1: Sequences of primers used in this study
Table 2: Prevalence of antimicrobial resistance phenotype among Escherichia coli isolates
Table 3: Phenotypic antimicrobial resistance profiles and their distribution pattern among phylo-groups
*This strain is the only Extended-Spectrum Beta-Lactamase-producing Escherichia coli isolate.
C=chloramphenicol; CAZ=ceftazidime; CIP=ciprofloxacin; CTX=Cefotaxime; FF=florfenicol; NA=nalidixic acid; NFX=enrofloxacin
.PNG)
Figure 1: Heat map of phenotypic antimicrobial resistance patterns, phylogenetic background, virulence genes, and antimicrobial resistance genes.
C=chloramphenicol; CAZ=ceftazidime; CIP=ciprofloxacin; CTX=Cefotaxime; FF=florfenicol; NA=nalidixic acid; NFX=enrofloxacin
Table 4: Prevalence of antimicrobial resistance genotype and distribution pattern of phylogenetic groups among Escherichia coli isolates
Table 5: Prevalence of virulence gene and distribution pattern of phylogenetic groups among Escherichia coli isolates
Reservoir for Dissemination of Antimicrobial Resistant and
Shigatoxigenic Escherichia coli Strains
M. Bagheri 1**
1. Department of Food Science and Technology, Bardsir Faculty of Agriculture, Shahid Bahonar University of Kerman, Kerman, Iran
2. Molecular Microbiology Research Group, Shahid Bahonar University of Kerman, Kerman, Iran
3. Department of Pathobiology, Faculty of Veterinary Medicine, Shahid Bahonar University of Kerman, Kerman, Iran
- Escherichia coli was detected in 75.78% of turkey carcasses, with 52.7% of isolates being multidrug-resistant.
- A significant resistance to chloramphenicol (63.89%), nalidixic acid (59.72%), and florfenicol (56.94%) was detected.
- The virulence genes stx1 (4.17%), stx2 (1.39%), and eae (2.77%) were identified in the isolates.
- The E. coli isolates were assigned to phylotypes A, B1, C, D, and E, while 9.72% remained unclassified.
- The findings highlighted the public health risks associated with antibiotic-resistant STEC and EPEC strains in turkey meat.
| Article type Original article |
ABSTRACT Background: Enteropathogenic and Shiga toxin-producing Escherichia coli (E. coli) are the two main pathotypes capable of causing serious human infections, especially when resistant to antibiotics. Methods: In this work, 95 turkey carcasses were swabbed in slaughterhouse over four months (June–September 2023). Antibiotic resistance was evaluated by a disk diffusion method named Kirby–Bauer against nine antimicrobial agents. Three virulence genes including stx1, stx2, eae, three resistance genes including blaTEM, blaSHV, blaCTX-M, and four phylogenetic markers (arpA, chuA, yjaA, TspE4.C2) were screened by Polymerase Chain Reaction (PCR) method. Data were analyzed using Microsoft Excel and SPSS (version 24), with the chi-square test at a significance level of p≤0.05. Results: Out of 95 carcasses, 72 (75.78%) were E. coli-positive. Among the E. coli isolates, 63.89% were resistant to chloramphenicol, 59.72% to nalidixic acid, and 56.94% to florfenicol. One isolate, classified as extended-spectrum beta-lactamase positive, belonged to phylogroup D and showed simultaneous resistance to four antibiotics without harboring the resistance genes studied. Overall, 52.7% of the E. coli isolates were recognized as Multi-Drug Resistant (MDR). Profiles of resistance genes included blaTEM (23.61%), blaTEM/blaSHV (2.77%), and blaCTX-M (1.38%). Virulence genes were detected in six isolates: stx1 (4.17%), stx2 (1.39%), and eae (2.77%). Phylogenetic analysis revealed five groups: A (19.44%), B1 (36.11%), C (5.55%), D (13.8%), and E (15.27%), while 9.72% remained unclassified. Conclusion: The occurrence of E. coli isolates harboring virulence and antibiotic-resistance genes in turkey carcasses underscores serious public health risks. The significant frequency of Multi-Drug Resistant (MDR) E. coli isolates highlights the need for improved monitoring and control measures throughout the food chain. © 2026, Shahid Sadoughi University of Medical Sciences. This is an open access article under the Creative Commons Attribution 4.0 International License. |
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| Keywords Shiga-Toxigenic Escherichia coli Beta-Lactamase Antibiotic Resistance Phylogeny Turkeys Abattoirs |
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| Article history Received: 17 Jul 2024 Revised: 30 Aug 2025 Accepted: 15 Sep 2025 |
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| Abbreviations AMR=Antimicrobial-Resistant CLSI=Clinical and Laboratory Standards Institute EHEC=Enterohemorrhagic Escherichia coli EPEC=Enteropathogenic Escherichia coli ESBL=Extended-Spectrum Beta-Lactamase MDR=Multi-Drug Resistant PCR=Polymerase Chain Reaction STEC=Shiga Toxin-Producing Escherichia Coli |
To cite: Bagheri, M., Ghanbarpour, R., Amirpoorsaid, Z., Mohseni, P., Hesam-Arefi, M. and Jajarmi, M. (2026) 'Turkey (Meleagris gallopavo f. domestica) meat as a potential reservoir for dissemination of antimicrobial resistant and shigatoxigenic Escherichia coli strains', Journal of Food Quality and Hazards Control, 13(1), pp. 40-49.
Introduction
Turkey meat (Meleagris gallopavo f. domestica) is one the most consumed meat worldwide, following chicken meat
E. coli is mainly commensal, but some strains exhibit pathogenicity due to distinct virulence factors(Pakbin, Brück and Rossen, 2021) . Among the different pathotypes used to classify pathogenic E. coli strains, Shiga toxin-producing (STEC) and enteropathogenic E. coli (EPEC) are regarded as the most relevant to public health (Pakbin, Brück and Rossen, 2021) . STECs produce two types of Shiga toxins named Stx1 and Stx2, which are encoded by stx1 and stx2 genes, whereas A distinctive feature of EPEC is its ability to cause attaching and effacing lesions, mediated by the outer membrane protein intimin, encoded by the eae gene (Pakbin, Brück and Rossen, 2021) . The co-occurrence of intimin and stx1 and/or stx2 in E. coli strains defines the clinically significant pathotype called Enterohemorrhagic E. coli (EHEC; Zarei et al., 2021) . Stx is a major virulence factor produced by STEC and EHEC, contributing to HC (hemorrhagic colitis) and HUS (Hemolytic Uremic Syndrome) (Freedman, Van De Kar and Tarr, 2023) . Intimate adherence of bacteria to gut epithelial cells, causes disruption of the microvilli and formation of pedestal-like structures (Mare et al., 2021; Sokolovic et al., 2022) .
One of the major challenges in infections caused by EPEC, STEC, and EHEC is the presence of antibiotic resistance in E. coli strains(Bouzari et al., 2018) . The emergence of Antimicrobial-Resistant (AMR) E. coli in some food-producing animals, including poultry, has been increasingly reported worldwide (Van Boeckel et al., 2019) . Studies have identified AMR E. coli isolates in meat products of turkey and other poultry, raising concerns about their potential foodborne transmission to humans (Khaitsa et al., 2008) . These AMR strains may be resistant to fluoroquinolones and cephalosporins, which are essential for the treatment of severe human infections (Shrestha et al., 2022) . The global health implications of AMR E. coli are significant, as these strains not only compromise treatment efficacy but also serve as reservoirs of resistance genes that may disseminate to other pathogenic/non-pathogenic bacteria (Martinez, 2009) . Factors contributing to the emergence of AMR E. coli include improper antibiotic use, administration without prior antimicrobial susceptibility testing, and the utilization of counterfeit drugs; such practices exert selective pressure, favoring resistant bacteria while disadvantaging antibiotic-susceptible strains. Addressing this issue is crucial to public health, as it underscores the need for monitoring AMR E. coli prevalence in poultry and implementing more stringent antimicrobial stewardship practices (Endale, Mathewos and Abdeta, 2023) .
E. coli populations are clonal and can be assigned to distinct phylogroups including A, B1, B2, D, C, E, F, G, and Escherichia cryptic clade I based on screening of four genetic markers: arpA, TspE4.C2, yjaA and chuA(Beghain et al., 2018) . These phylogenetic groups reflect the virulence, evolutionary history, ecological niche and both genotypic/phenotypic characteristics of E. coli strains (Stoppe et al., 2017) . Understanding the phylogroup is crucial, as certain groups are more commonly associated with virulence and antibiotic resistance features, thereby influencing the pathogenic potential and clinical outcomes of E. coli infections characteristics (Tenaillon et al., 2010) .
Therefore, this study aims to investigate the prevalence of virulence genes and antimicrobial resistance factors among various phylogenetic groups of E. coli isolates from turkey meat. The results of this study may shed light on the contribution of turkey meat to the epidemiology of virulent and AMR E. coli strains.
E. coli is mainly commensal, but some strains exhibit pathogenicity due to distinct virulence factors
One of the major challenges in infections caused by EPEC, STEC, and EHEC is the presence of antibiotic resistance in E. coli strains
E. coli populations are clonal and can be assigned to distinct phylogroups including A, B1, B2, D, C, E, F, G, and Escherichia cryptic clade I based on screening of four genetic markers: arpA, TspE4.C2, yjaA and chuA
Therefore, this study aims to investigate the prevalence of virulence genes and antimicrobial resistance factors among various phylogenetic groups of E. coli isolates from turkey meat. The results of this study may shed light on the contribution of turkey meat to the epidemiology of virulent and AMR E. coli strains.
Materials and methods
Collection of samples and isolation of E. coli
In total, 95 swab samples were collected from the carcasses of 95 turkeys in the slaughterhouse after chilling during four months (June to September 2023), before any secondary processing; Samples were taken by swabbing the interior surface of the turkey carcasses at the end of the slaughter line, prior to carcass cutting and packaging. A sterile swab was used to thoroughly swab the internal cavity of each carcass, moving from one end to the other 5 to 10 times to ensure sufficient sample collection. The swab was then placed into a transport medium for subsequent microbiological analysis. This standardized approach was aimed to ensure consistency and reproducibility across all samples. The sample size was estimated based on the formula:
Collection of samples and isolation of E. coli
In total, 95 swab samples were collected from the carcasses of 95 turkeys in the slaughterhouse after chilling during four months (June to September 2023), before any secondary processing; Samples were taken by swabbing the interior surface of the turkey carcasses at the end of the slaughter line, prior to carcass cutting and packaging. A sterile swab was used to thoroughly swab the internal cavity of each carcass, moving from one end to the other 5 to 10 times to ensure sufficient sample collection. The swab was then placed into a transport medium for subsequent microbiological analysis. This standardized approach was aimed to ensure consistency and reproducibility across all samples. The sample size was estimated based on the formula:
Z value for the 95% confidence interval [error level (α): 0.05] = 1.96; Z2 = 3.84
p [the projected proportion based on earlier research(Nwankwo et al., 2021) ]
1- p
d (the error rate chosen by the investigators in this work) = 0.1 (or 10%); d2 = 0.01
The swab samples were collected using aseptic techniques, stored in sterile tubes containing transport medium (Cary Blair; Himedia, India) under controlled temperature conditions (4°C), and immediately handled to laboratory mostly within 2 h and sometimes up to the 12 h. The swabs were transferred to the laboratory within 12 h. The samples were streaked on MacConkey agar (Merck, Germany) and incubated at 37 °C (Memmert, Germany) for 24 h. The lactose-positive colonies were biochemically confirmed by IMViC biochemical tests, including indole, methyl red, Voges-Proskauer, and citrate as E. coli strains(Markey et al., 2013) . Then, one strain from each bird was considered for virulence, antimicrobial resistance, and phylogenetic assessments.
Phenotypic evaluation of the E. coli isolates
Antimicrobial resistance was determined in this work via the Kirby-Bauer disc diffusion method, performed in accordance with the Clinical and Laboratory Standards Institute (CLSI) guidelines (CLSI, 2021); the antibiotics used (Padtan Teb co., Iran) included ceftazidime, cefotaxime, cefotaxime clavulanate, ceftazidime clavulanate, florfenicol, chloramphenicol, enrofloxacin, nalidixic acid, and ciprofloxacin. The reference strain E. coli ATCC 25922 was used as the quality control strain, and the inhibition zone diameters were interpreted according to CLSI guidelines (CLSI, 2021). Isolates showing an increase of ≥ 5 mm in the inhibition zone for cefotaxime-clavulanate relative to cefotaxime alone, or for ceftazidime-clavulanate relative to ceftazidime alone, were considered Extended-Spectrum β-Lactamase-producing E. coli (ESBL; CLSI, 2021).
p [the projected proportion based on earlier research
d (the error rate chosen by the investigators in this work) = 0.1 (or 10%); d2 = 0.01
The swab samples were collected using aseptic techniques, stored in sterile tubes containing transport medium (Cary Blair; Himedia, India) under controlled temperature conditions (4°C), and immediately handled to laboratory mostly within 2 h and sometimes up to the 12 h. The swabs were transferred to the laboratory within 12 h. The samples were streaked on MacConkey agar (Merck, Germany) and incubated at 37 °C (Memmert, Germany) for 24 h. The lactose-positive colonies were biochemically confirmed by IMViC biochemical tests, including indole, methyl red, Voges-Proskauer, and citrate as E. coli strains
Phenotypic evaluation of the E. coli isolates
Antimicrobial resistance was determined in this work via the Kirby-Bauer disc diffusion method, performed in accordance with the Clinical and Laboratory Standards Institute (CLSI) guidelines (CLSI, 2021); the antibiotics used (Padtan Teb co., Iran) included ceftazidime, cefotaxime, cefotaxime clavulanate, ceftazidime clavulanate, florfenicol, chloramphenicol, enrofloxacin, nalidixic acid, and ciprofloxacin. The reference strain E. coli ATCC 25922 was used as the quality control strain, and the inhibition zone diameters were interpreted according to CLSI guidelines (CLSI, 2021). Isolates showing an increase of ≥ 5 mm in the inhibition zone for cefotaxime-clavulanate relative to cefotaxime alone, or for ceftazidime-clavulanate relative to ceftazidime alone, were considered Extended-Spectrum β-Lactamase-producing E. coli (ESBL; CLSI, 2021).
Polymerase Chain Reaction (PCR) for virulence, antimicrobial resistance, and phylogenetic genes
DNA extraction was carried out using boiling lysis method. In brief, E. coli colonies were suspended in 400 µl water (distilled and sterile) and heated at 98-100 °C for 10 min in boiling water. The lysates were then placed on (10 min) and centrifuged (13,000 × g; 1 min). The supernatant, containing the released DNA, was collected and used as the template for subsequent reactions. DNA yield and purity were evaluated with NanoDrop (BioTek Epoch, USA) by measuring absorbance at 260/280 nm.
The occurrence of the genes including stx1, stx2, and eae were screened(Paton and Paton, 2002 ) by PCR (Bio-Rad, USA). Sakaï strain of E. coli (eae+, stx1+, and stx2+) was used as a control+ while E. coli strain MG1655 (eae−, stx1−, and stx2−) was employed as a control−, sourced from Shahid Bahonar University of Kerman. Additionally, the E. coli strains were screened for blaCTX-M, blaTEM, and blaSHV as antibiotic resistance genes (Roschanski et al., 2014) (Table 1).
DNA extraction was carried out using boiling lysis method. In brief, E. coli colonies were suspended in 400 µl water (distilled and sterile) and heated at 98-100 °C for 10 min in boiling water. The lysates were then placed on (10 min) and centrifuged (13,000 × g; 1 min). The supernatant, containing the released DNA, was collected and used as the template for subsequent reactions. DNA yield and purity were evaluated with NanoDrop (BioTek Epoch, USA) by measuring absorbance at 260/280 nm.
The occurrence of the genes including stx1, stx2, and eae were screened
Detection of four sequences (arpA, chuA, yjaA, and TspE4.C2) using PCR (multiplex) (Clermont et al., 2013) led to phylogenetic grouping of E. coli into 7 groups and some clades. Isolates that were arpA positive but chuA, yjaA, and TspE4.C2 negative were allocated to phylogroup A, whereas those that were arpA positive, chuA and yjaA negative, but TspE4.C2 positive were classified as B1. Phylogroup B2 included isolates that were arpA negative, chuA positive, and positive for at least one of yjaA or TspE4.C2. Isolates with the profile arpA positive, chuA negative, yjaA positive, and TspE4.C2 negative were subjected to C-specific PCR; if this reaction was positive, they were assigned to C, otherwise they were reclassified as A. Strains that were arpA positive and chuA positive but yjaA negative (with TspE4.C2 either negative or positive) were tested using E-specific primers; isolates yielding a positive result were designated as E, and those testing negative were placed in D. Isolates showing arpA positive, chuA positive, yjaA positive, and TspE4.C2 negative were similarly screened with E-specific primers: E-positive strains were classified as E, whereas E-negative ones were assigned to Escherichia cryptic clade I and confirmed using cryptic clade-specific primers. Strains that were arpA negative, chuA positive, yjaA negative, and TspE4.C2 negative were grouped as F, and isolates displaying arpA negative, chuA negative, yjaA positive, and TspE4.C2 negative were assigned to Escherichia cryptic clade I or II after confirmation with cryptic clade-specific primers (Table 1). Other genotypes were considered as unknown phylogroups.
A 1.5% agarose gel in a horizontal electrophoresis unit was used to resolve the PCR products at 100 V for 45 minutes (Cleaver Scientific, United Kingdom) and then visualized by fluorescence staining using Greenview dye (Parstous Biotechnology, Iran) and gel documentation system (Vilber Lourmat co., Quantum software version ST4, France). Amplicon sizes were determined using two types of DNA marker including 50 bp and 100 bp (Parstous Biotechnology, Iran) as a reference.(Connolly and Campbell, 2023) . Meat products of turkey may be one of the putative reservoirs for several key foodborne pathogens, such as Escherichia coli, Staphylococcus spp., Salmonella spp., Clostridium spp., Campylobacter spp., Listeria spp., and Arcobacter spp. (Silva, Vidal and Junior, 2017) . E. coli is of particular significance due to its predominant presence within the gastrointestinal microbiota in warm-blooded animals (Foster-Nyarko and Pallen, 2022) .
A 1.5% agarose gel in a horizontal electrophoresis unit was used to resolve the PCR products at 100 V for 45 minutes (Cleaver Scientific, United Kingdom) and then visualized by fluorescence staining using Greenview dye (Parstous Biotechnology, Iran) and gel documentation system (Vilber Lourmat co., Quantum software version ST4, France). Amplicon sizes were determined using two types of DNA marker including 50 bp and 100 bp (Parstous Biotechnology, Iran) as a reference.
Table 1: Sequences of primers used in this study
| Gene | Sequence (5'–3') | PCR condition | Product size(bp) |
Reference |
| stx1 | F-ATAAATCGCCATTCGTTGACTAC R-AGAACGCCCACTGAGATCATC |
35 cycles: 94°C (90 s), 60°C (90 s), 72°C (90 s) | 348 | |
| stx2 | F-GGCACTGTCTCTCTGAAACTGCTCC R-TCGCCAGTTATCTGACATTCTG |
35 cycles: 94°C (90 s), 60°C (90 s), 72°C (90 s) | 584 | |
| eae | F-GACCCGGCACAAGCATAAGC R-CCACCTGCAGCAACAAGAGG |
35 cycles: 94°C (90 s), 60°C (90 s), 72°C (90 s) | 482 | |
| arpA | F-AACGCTATTCGCCAGCTTGC R-TCTCCCCATACCGTACGCTA |
30 cycles: 94°C (5 s), 59°C (20 s) and 1 cycle 72°C (5 min) | 400 | |
| chuA | F-ATGGTACCGGACGAACCAAC R-TGCCGCCAGTACCAAAGACA |
30 cycles: 94°C (5 s), 59°C (20 s) and 1 cycle 72°C (5 min) | 288 | |
| yjaA | F-CAAACGTGAAGTGTCAGGAG R-AATGCGTTCCTCAACCTGTG |
30 cycles: 94°C (5 s), 59°C (20 s) and 1 cycle 72°C (5 min) | 211 | |
| TspE4.C2 | F-CACTATTCGTAAGGTCATCC R-AGTTTATCGCTGCGGGTCGC |
30 cycles: 94°C (5 s), 59°C (20 s) and 1 cycle 72°C (5 min) | 152 | |
| blaTEM | Fa -GCGGAACCCCTATTTG Rb -ACCAATGCTTAATCAGTGAG |
35 cycles: 95°C (30 s), 52°C (30 s), 72°C (60 s) | 963 | |
| blaSHV | F-TTATCTCCCTGTTAGCCACC R-GATTTGCTGATTTCGCTCGG |
35 cycles: 95°C (30 s), 54°C (30 s), 72°C (30 s) | 795 | |
| blaCTX-M | F-CGATGTGCAGTACCAGTAA R-TTAGTGACCAGAATCAGCGG |
35 cycles: 95°C (30 s), 60°C (30 s), 72°C (60 s) | 585 |
Statistical analysis
To minimize potential confounding factors and biases, sampling was carried out over a 16-week period (4 months). During each sampling session, 5 to 10 samples were collected, and carcasses were selected in an alternating pattern (every other carcass) to ensure randomness and reduce selection bias. For each isolate, information on phylogroup status and antimicrobial resistance was compiled in Microsoft Excel 2016 and subsequently analyzed in SPSS version 24 (IBM) to obtain prevalence percentages through descriptive statistics. The chi-square test was applied to assess differences in frequencies and associations between variables, and a p-value of ≤ 0.05 was taken as the threshold for statistical significance.
To minimize potential confounding factors and biases, sampling was carried out over a 16-week period (4 months). During each sampling session, 5 to 10 samples were collected, and carcasses were selected in an alternating pattern (every other carcass) to ensure randomness and reduce selection bias. For each isolate, information on phylogroup status and antimicrobial resistance was compiled in Microsoft Excel 2016 and subsequently analyzed in SPSS version 24 (IBM) to obtain prevalence percentages through descriptive statistics. The chi-square test was applied to assess differences in frequencies and associations between variables, and a p-value of ≤ 0.05 was taken as the threshold for statistical significance.
Results and discussion
Prevalence of E. coli strains
E. coli was detected in 72 out of 95 turkey carcasses (75.78%). The presence of E. coli on turkey carcasses suggests shortcomings in slaughterhouse hygiene, including possible fecal cross-contamination or improper carcass handling. Such contamination represents a potential public health risk. E. coli may contribute substantially to the spread of virulence factors and antimicrobial resistance determinants.
Prevalence of phenotypic antimicrobial resistance
Antimicrobial resistance to seven widely used antibiotics was investigated; these antibiotics belonged to three different classes and were tested using the disc diffusion method. For amphenicols, 46 (63.89%) isolates showed resistance against chloramphenicol, and 41 (56.94%) isolates were resistant to florfenicol. For quinolones, resistance against enrofloxacin, nalidixic acid, and ciprofloxacin was detected in 23 (31.94%), 43 (59.72%), and 17 (23.61%) isolates, respectively. The lowest level of resistance was identified to β-lactams (p≤0.05); only four strains were resistant against cefotaxime (5.56%), one was ceftazidime-resistant (1.38%), and only one isolate was ESBL-positive (1.38%) (Table 2). No differences were significantly observed in the frequency of antibiotic resistance among the phylogenetic groups (p>0.05).
Prevalence of E. coli strains
E. coli was detected in 72 out of 95 turkey carcasses (75.78%). The presence of E. coli on turkey carcasses suggests shortcomings in slaughterhouse hygiene, including possible fecal cross-contamination or improper carcass handling. Such contamination represents a potential public health risk. E. coli may contribute substantially to the spread of virulence factors and antimicrobial resistance determinants.
Prevalence of phenotypic antimicrobial resistance
Antimicrobial resistance to seven widely used antibiotics was investigated; these antibiotics belonged to three different classes and were tested using the disc diffusion method. For amphenicols, 46 (63.89%) isolates showed resistance against chloramphenicol, and 41 (56.94%) isolates were resistant to florfenicol. For quinolones, resistance against enrofloxacin, nalidixic acid, and ciprofloxacin was detected in 23 (31.94%), 43 (59.72%), and 17 (23.61%) isolates, respectively. The lowest level of resistance was identified to β-lactams (p≤0.05); only four strains were resistant against cefotaxime (5.56%), one was ceftazidime-resistant (1.38%), and only one isolate was ESBL-positive (1.38%) (Table 2). No differences were significantly observed in the frequency of antibiotic resistance among the phylogenetic groups (p>0.05).
Table 2: Prevalence of antimicrobial resistance phenotype among Escherichia coli isolates
| Antimicrobial family | Antimicrobial resistance phenotype | Number | Percentage | 95% CI |
| β-lactams | ||||
| Cefotaxime | 4 | 5.56 | 0.26-10.85% | |
| Ceftazidime | 1 | 1.38 | 0-4.09% | |
| Extended-Spectrum Beta-Lactamase-positive | 1 | 1.38 | 0-4.09% | |
| Amphenicols | ||||
| Florfenicol | 41 | 56.94 | 45.51-68.38% | |
| Chloramphenicol | 46 | 63.89 | 52.79-74.98% | |
| Quinolones | ||||
| Enrofloxacin | 23 | 31.94 | 21.17-42.71% | |
| Nalidixic acid | 43 | 59.72 | 48.39-71.05% | |
| Ciprofloxacin | 17 | 23.61 | 13.80-33.42% |
The elevated levels of resistance to chloramphenicol, nalidixic acid, and florfenicol found in this study are consistent with previous findings in E. coli strains recovered from turkey meat and intestinal contents in Iran (Gholami-Ahangaran et al., 2021) ; furthermore, the low levels of resistance to cefotaxime and ceftazidime observed in our study agreed with those reported previously in Germany, (Kaesbohrer et al., 2012) , Poland (Wasyl et al., 2013) , and Iran (Mousavi, Rahimi and Shakerian, 2020) .
Lowest resistance level was against the β-lactams. The rate of antibiotic resistance for cefotaxime in this study was lower than study in Egypt(AbdelRahman et al., 2020; Moawad et al., 2018; Younis, Awad, and Mohamed, 2017) , China (Wang et al., 2021) , and India (Sebastian et al., 2021) ; only one isolate of our study was ESBL-positive. The lower levels of resistance against β-lactams in turkey meat, compared to florfenicol and chloramphenicol, may reflect differences in antibiotic usage practices in turkey production.
Antibiotic usage in veterinary medicine is a widespread approach either as a preventive measure or as additives to promote growth in livestock(Vázquez-Villanueva et al., 2023) . Unfortunately, this has resulted in the appearance of bacterial strains that exhibit resistance to multiple antibiotics, including florfenicol, chloramphenicol, cefotaxime, and ceftazidime. The present study demonstrates a considerable presence of AMR strains, suggesting a lack of adherence to recommended guidelines and an overuse of antibiotics.
Resistance patterns and their distribution among phylogroups are shown in Table 3 and Figure 1. Twenty antimicrobial resistance profiles were observed in which florfenicol-chloramphenicol was the most prevalent AMR profile (12 isolates; 16.67%). Thirty-eight (52.7%) isolates were recognized as Multi-Drug Resistant (MDR; a strain, resistant to at least one antibiotic from three different antimicrobial classes); this finding is comparable to the results reported from the USA(Davis et al., 2018) . Six strains were susceptible to all tested antimicrobials. The most common resistance pattern was related to FF, C profile (12 isolates, 16.69%). In Egypt, a work on E. coli strains isolated from turkey showed 100% of the isolates were MDR (Eid and Samir, 2019) . The global dissemination of MDR strains as a consequence of excessive and uncontrolled use of antimicrobials has caused a serious problem, indicating the high prevalence of MDR isolates among poultry farms.
Detection of β-lactamase genes
The most frequent antimicrobial resistance genotypic pattern was blaTEM (17 isolates; 23.61%), followed by blaTEM/blaSHV (2 isolates; 2.77%), and blaCTX-M (1 isolate; 1.38%). Fifty-two isolates (72.22%) possessed none of the screened antimicrobial resistance genes. The phylogenetic distribution pattern of the positive isolates is revealed in Table 4.
Lowest resistance level was against the β-lactams. The rate of antibiotic resistance for cefotaxime in this study was lower than study in Egypt
Antibiotic usage in veterinary medicine is a widespread approach either as a preventive measure or as additives to promote growth in livestock
Resistance patterns and their distribution among phylogroups are shown in Table 3 and Figure 1. Twenty antimicrobial resistance profiles were observed in which florfenicol-chloramphenicol was the most prevalent AMR profile (12 isolates; 16.67%). Thirty-eight (52.7%) isolates were recognized as Multi-Drug Resistant (MDR; a strain, resistant to at least one antibiotic from three different antimicrobial classes); this finding is comparable to the results reported from the USA
Detection of β-lactamase genes
The most frequent antimicrobial resistance genotypic pattern was blaTEM (17 isolates; 23.61%), followed by blaTEM/blaSHV (2 isolates; 2.77%), and blaCTX-M (1 isolate; 1.38%). Fifty-two isolates (72.22%) possessed none of the screened antimicrobial resistance genes. The phylogenetic distribution pattern of the positive isolates is revealed in Table 4.
Table 3: Phenotypic antimicrobial resistance profiles and their distribution pattern among phylo-groups
| Antimicrobial resistance profiles | Phylo-group (no.) | ||||||
| A | B1 | C | D | E | U | No. (%) | |
| C | 1 | 2 | 3 (4.17) | ||||
| FF | 1 | 1 | 1 | 1 | 4 (5.57) | ||
| NA | 1 | 2 | 3 | 1 | 7 (9.73) | ||
| CTX | 1 | 1 (1.38) | |||||
| FF, C | 5 | 3 | 1 | 3 | 12 (16.69) | ||
| C, NA | 1 | 1 (1.38) | |||||
| FF, NA | 1 | 1 (1.38) | |||||
| C, CTX | 1 | 1 (1.38) | |||||
| NA, CIP | 1 | 1 (1.38) | |||||
| FF, CTX | 1 | 1 (1.38) | |||||
| NA, NFX | 1 | 1 | 2 (2.77) | ||||
| FF, C, NA | 3 | 3 | 2 | 8 (11.12) | |||
| FF, C, CIP | 1 | 1 (1.38) | |||||
| C, NA, NFX | 1 | 1 (1.38) | |||||
| NA, NFX, CIP | 1 | 1 | 1 | 3 (4.17) | |||
| FF, C, NA, CIP | 1 | 1 (1.38) | |||||
| FF, C, NA, NFX | 2 | 3 | 1 | 6 (8.34) | |||
| C, NA, NFX, CIP | 1 | 1 | 1* | 1 | 4 (5.57) | ||
| C, NA, CTX, CAZ | 1 | 1 (1.38) | |||||
| FF, C, NA, NFX, CIP | 2 | 4 | 1 | 7 (9.73) | |||
| Non-resistant isolates | 1 | 4 | 1 | 6 (8.34) | |||
| Total (%) | 15 (20.83) | 26 (36.11) | 3 (4.17) | 10 (13.89) | 11 (15.28) | 7 (9.72) | 72 (100) |
C=chloramphenicol; CAZ=ceftazidime; CIP=ciprofloxacin; CTX=Cefotaxime; FF=florfenicol; NA=nalidixic acid; NFX=enrofloxacin
Figure 1: Heat map of phenotypic antimicrobial resistance patterns, phylogenetic background, virulence genes, and antimicrobial resistance genes.
C=chloramphenicol; CAZ=ceftazidime; CIP=ciprofloxacin; CTX=Cefotaxime; FF=florfenicol; NA=nalidixic acid; NFX=enrofloxacin
Table 4: Prevalence of antimicrobial resistance genotype and distribution pattern of phylogenetic groups among Escherichia coli isolates
| Variables | Phylo-group | No. (%) | 95% confidence interval | |||||
| A | B1 | C | D | E | U | |||
| blaTEM | 7 | 3 | 1 | 1 | 4 | 1 | 17 (23.61) | 13.8%-33.42% |
| blaTEM/blaSHV | 1 | 1 | 2 (2.77) | 0%-6.57% | ||||
| blaCTX-M | 1 | 1 (1.38) | 0%-4.09% | |||||
| No resistance gene | 8 | 23 | 1 | 8 | 6 | 6 | 52 (72.22) | 61.88%-82.57% |
| Total | 15 | 26 | 3 | 10 | 11 | 7 | 72 (100) | - |
Higher frequency of bla gene-positive strains in poultry and turkey has been reported in Egypt (AbdelRahman et al., 2020) , Ghana (Eibach et al., 2018) , Türkiye (Baran, Adıgüzel and Yüksel, 2020), and Brazil (Hoepers et al., 2018) . These studies are relevant as they demonstrate the widespread occurrence of bla genes in poultry across diverse geographic regions. The present study’s results on the blaCTX-M closely align with finding from Canada (Sheikh et al., 2012) and Egypt (Moawad et al., 2018) .
It is also important to recognize the potential for horizontal transfer of ESBL genes to other bacteria. Such transfer events may promote the dissemination of resistance features to otherwise susceptible bacterial populations, thereby increasing the likelihood of therapeutic failure and making infection control more difficult.
Prevalence of virulence genes
In the current study, six strains carried at least one of the three virulence genes under investigation; stx1 (3 isolates; 4.17%), stx2 (1 isolate; 1.39%) and eae (2 isolates; 2.77%). No virulence genes were detected in 66 isolates (91.67%). Details are presented in table 5.
Furthermore, six strains harbored at least one of the three virulence genes analyzed, which are known to be associated with STEC, EPEC, and EHEC pathotypes; the prevalence of VG-positives was less than 5%. Comparable frequencies of stx1, stx2, and eae were found by Mousavi, Rahimi and Shakerian (2020) in Iran. However, some studies in Saudi Arabia(Hessain et al., 2015) , Austria (Mayrhofer et al., 2004) , and Canada (Bohaychuk et al., 2006) did not detect virulence genes related to STEC, EPEC, and EHEC.
It is also important to recognize the potential for horizontal transfer of ESBL genes to other bacteria. Such transfer events may promote the dissemination of resistance features to otherwise susceptible bacterial populations, thereby increasing the likelihood of therapeutic failure and making infection control more difficult.
Prevalence of virulence genes
In the current study, six strains carried at least one of the three virulence genes under investigation; stx1 (3 isolates; 4.17%), stx2 (1 isolate; 1.39%) and eae (2 isolates; 2.77%). No virulence genes were detected in 66 isolates (91.67%). Details are presented in table 5.
Furthermore, six strains harbored at least one of the three virulence genes analyzed, which are known to be associated with STEC, EPEC, and EHEC pathotypes; the prevalence of VG-positives was less than 5%. Comparable frequencies of stx1, stx2, and eae were found by Mousavi, Rahimi and Shakerian (2020) in Iran. However, some studies in Saudi Arabia
Table 5: Prevalence of virulence gene and distribution pattern of phylogenetic groups among Escherichia coli isolates
| Variables | Phylo-group | No. (%) | 95% confidence interval | |||||
| A | B1 | C | D | E | U | |||
| eae | 1 | 1 | 2 (2.77) | 0%-6.57% | ||||
| stx1 | 1 | 1 | 1 | 3 (4.17) | 0%-8.78% | |||
| stx2 | 1 | 1 (1.39) | 0%-4.09% | |||||
| No virulence gene | 14 | 25 | 3 | 8 | 10 | 6 | 66 (91.67) | 82.74%-96.88% |
| Total | 15 | 26 | 3 | 10 | 11 | 7 | 72 (100) | - |
The variation in sample size between studies may be one reason for the observed differences in findings. The lower prevalence of the virulence genes in turkey meat compared to other food sources such as beef can be attributed to biological and husbandry-related factors. It is well-established that ruminants, rather than birds, serve as the primary reservoirs of STEC. Therefore, the presence of these virulence genes is generally higher in ruminant-derived products. However, in traditional turkey farming systems, especially where turkeys are raised in close proximity to ruminants, the likelihood of STEC contamination may increase due to potential cross-contamination or environmental exposure.
Available evidence suggests that food animals might function as a reservoir for human infection. Also, retail meats could potentially serve as a vehicle for the transmission of these strains. Although the frequency of pathogenic E. coli isolates in turkey carcasses is low, their potential role in spreading virulent strains should not be overlooked, especially considering vulnerable populations such as immunocompromised individuals, for whom even minimal exposure may pose significant health risks.
Prevalence of phylogenetic groups
Totally, among the 72 strains, seven phylogroups including A, B1, B2, C, D, E, and F were identified, while some isolates remained unassigned and were categorized as unknown (U); from high to low prevalence, 26 isolates (36.11%) belonged to B1, 14 isolates (19.44%) to A, 11 (15.27%) isolates to E, 10 isolates (13.8%) to D, 4 isolates (5.55%) to C, and 7 isolates (9.72%) didn’t belong to any of the phylogenetic groups (U) (Table 3-5). A heat map of phenotypic antimicrobial resistance patterns and associated phylogenetic background, virulence genes, and antimicrobial resistance genotypic profile has been provided in Figure 1.
The dominance of B1 in our study is consistent with another work in Türkiye(Baran, Adıgüzel and Yüksel, 2020) . The most prevalent phylotypes in China (Wang et al., 2021), Spain (Egea et al., 2012) , and Iran (Asadi et al., 2018) have been related to phylotype A. Various variables, for example body mass, age, diet, species, sex, type of nutrition, types of pollution, environment (geographic location and climate), bacteria (pathogenicity and resistance), method, sample size, and study time, account for differences in phylotypes across studies.
Most positive strains for β-lactam were found in A and B1, the phylogroups known as commensal phylogroups of E. coli. Therefore, commensal strains may represent a potential threat to public health because of their role in the transmission of antibiotic resistance. among different hosts and pathogens. Strains classified within phylogroup D were all negative for virulence genes. This finding is interesting because, in many studies, D has been introduced as a phylogroup related to pathogenic strains of E. coli. Although B2 and D are traditionally considered more pathogenic in humans and other hosts, some studies have reported that strains belonging to these groups may exhibit lower virulence potential. This observation suggests that phylogenetic grouping alone may not fully predict the pathogenicity of E. coli bacterium.
Phylogroups of E. coli may be associated with distinct antibiotic resistance patterns; however, this relationship is complex and influenced by multiple factors. The transfer of genes encoding resistance factors through mobile genetic elements can modify resistance patterns among different phylogroups(Xie, Ogura and Suzuki, 2022) .
Conclusion
The findings of this study indicate a high prevalence of E. coli in turkey carcasses. turkey carcasses, with a substantial proportion of isolates identified as multidrug-resistant and harboring the genetic determinants related to virulence and antibiotic resistance. Occurrence of virulent and AMR E. coli isolates from turkey meat highlights significant public health concerns, particularly in relation to food safety and antibiotic stewardship.
The results highlight the attention to regular surveillance of antimicrobial resistance patterns in poultry meat, as well as the implementation of effective hygiene practices throughout the slaughtering process. Improved slaughterhouse hygiene, personnel training, and adherence to international standards, including Hazard Analysis and Critical Control Points (HACCP), are essential for minimizing microbial contamination.
Given the limitations of the present study, small sample size and the selection of only one isolate per bird, further research is recommended to better capture the heterogeneity and dynamics of E. coli bacterium in poultry.
Future studies should involve larger and geographically diverse sampling, comparison with other poultry species, and an expanded panel of virulence genes to gain a better understanding of the pathogenic ability and antimicrobial resistance profiles of E. coli in turkey meat.
Available evidence suggests that food animals might function as a reservoir for human infection. Also, retail meats could potentially serve as a vehicle for the transmission of these strains. Although the frequency of pathogenic E. coli isolates in turkey carcasses is low, their potential role in spreading virulent strains should not be overlooked, especially considering vulnerable populations such as immunocompromised individuals, for whom even minimal exposure may pose significant health risks.
Prevalence of phylogenetic groups
Totally, among the 72 strains, seven phylogroups including A, B1, B2, C, D, E, and F were identified, while some isolates remained unassigned and were categorized as unknown (U); from high to low prevalence, 26 isolates (36.11%) belonged to B1, 14 isolates (19.44%) to A, 11 (15.27%) isolates to E, 10 isolates (13.8%) to D, 4 isolates (5.55%) to C, and 7 isolates (9.72%) didn’t belong to any of the phylogenetic groups (U) (Table 3-5). A heat map of phenotypic antimicrobial resistance patterns and associated phylogenetic background, virulence genes, and antimicrobial resistance genotypic profile has been provided in Figure 1.
The dominance of B1 in our study is consistent with another work in Türkiye
Most positive strains for β-lactam were found in A and B1, the phylogroups known as commensal phylogroups of E. coli. Therefore, commensal strains may represent a potential threat to public health because of their role in the transmission of antibiotic resistance. among different hosts and pathogens. Strains classified within phylogroup D were all negative for virulence genes. This finding is interesting because, in many studies, D has been introduced as a phylogroup related to pathogenic strains of E. coli. Although B2 and D are traditionally considered more pathogenic in humans and other hosts, some studies have reported that strains belonging to these groups may exhibit lower virulence potential. This observation suggests that phylogenetic grouping alone may not fully predict the pathogenicity of E. coli bacterium.
Phylogroups of E. coli may be associated with distinct antibiotic resistance patterns; however, this relationship is complex and influenced by multiple factors. The transfer of genes encoding resistance factors through mobile genetic elements can modify resistance patterns among different phylogroups
Conclusion
The findings of this study indicate a high prevalence of E. coli in turkey carcasses. turkey carcasses, with a substantial proportion of isolates identified as multidrug-resistant and harboring the genetic determinants related to virulence and antibiotic resistance. Occurrence of virulent and AMR E. coli isolates from turkey meat highlights significant public health concerns, particularly in relation to food safety and antibiotic stewardship.
The results highlight the attention to regular surveillance of antimicrobial resistance patterns in poultry meat, as well as the implementation of effective hygiene practices throughout the slaughtering process. Improved slaughterhouse hygiene, personnel training, and adherence to international standards, including Hazard Analysis and Critical Control Points (HACCP), are essential for minimizing microbial contamination.
Given the limitations of the present study, small sample size and the selection of only one isolate per bird, further research is recommended to better capture the heterogeneity and dynamics of E. coli bacterium in poultry.
Future studies should involve larger and geographically diverse sampling, comparison with other poultry species, and an expanded panel of virulence genes to gain a better understanding of the pathogenic ability and antimicrobial resistance profiles of E. coli in turkey meat.
Author contributions
M.B. conceptualized and administrated the project and wrote, reviewed and edited the manuscript; R.G. supervised the research and reviewed the manuscript; Z.A., P.M., M.H.A., and M.J. performed the sampling, laboratory procedures, and data analysis. All authors read and approved the final manuscript.
Acknowledgments
The authors gratefully acknowledge the support of the manager and staff of Bardsir Industrial Poultry Slaughterhouse for their assistance in sampling for the present projects.
Conflicts of interest
The authors declare that there is no conflict of interest.
Funding
This research received no specific grant from any funding agency in the public, commercial, or non-profit sectors.
Ethical consideration
Not applicable.
M.B. conceptualized and administrated the project and wrote, reviewed and edited the manuscript; R.G. supervised the research and reviewed the manuscript; Z.A., P.M., M.H.A., and M.J. performed the sampling, laboratory procedures, and data analysis. All authors read and approved the final manuscript.
Acknowledgments
The authors gratefully acknowledge the support of the manager and staff of Bardsir Industrial Poultry Slaughterhouse for their assistance in sampling for the present projects.
Conflicts of interest
The authors declare that there is no conflict of interest.
Funding
This research received no specific grant from any funding agency in the public, commercial, or non-profit sectors.
Ethical consideration
Not applicable.
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Xie, H., Ogura, Y. and Suzuki, Y. (2022) 'Persistence of antibiotic-resistant Escherichia coli strains belonging to the B2 phylogroup in municipal wastewater under aerobic conditions', Antibiotics, 11(2), p. 202. Available at: https://doi.org/10.3390/antibiotics11020202
Younis, G., Awad, A. and Mohamed, N. (2017) 'Phenotypic and genotypic characterization of antimicrobial susceptibility of avian pathogenic Escherichia coli isolated from broiler chickens', Veterinary World, 10(10), pp. 1167–1172. Available at: https://doi.org/10.14202/vetworld.2017.1167-1172
Zarei, O., Shokoohizadeh, L., Hossainpour, H. and Alikhani, M.Y. (2021) 'The prevalence of Shiga toxin-producing Escherichia coli and enteropathogenic Escherichia coli isolated from raw chicken meat samples', International Journal of Microbiology, 2021, p. 3333240. Available at: https://doi.org/10.1155/2021/3333240
AbdelRahman, M.A.A., Roshdy, H., Samir, A.H. and Hamed, E.A. (2020) 'Antibiotic resistance and extended-spectrum β-lactamase in Escherichia coli isolates from imported 1-day-old chicks, ducklings, and turkey poults', Veterinary World, 13(6), pp. 1037-1044. Available at: https://doi.org/10.14202/vetworld.2020.1037-1044
Asadi, A., Salehi, T.Z., Jamshidian, M. and Ghanbarpour, R. (2018) 'ECOR phylotyping and determination of virulence genes in Escherichia coli isolates from pathological conditions of broiler chickens in poultry slaughter-houses of southeast of Iran', Veterinary Research Forum, 9(3), pp. 211-216. Available at: https://doi.org/10.30466/vrf.2018.30827
Baran, A., Adıgüzel, M. and Yüksel, M. (2020) 'Prevalence of antibiotic-resistant and extended-spectrum beta-lactamase-producing Escherichia coli in chicken meat from eastern Turkey', Pakistan Veterinary Journal, 40(3), pp. 355-359. Available at: https://doi.org/10.29261/pakvetj/2020.047
Beghain, J., Bridier-Nahmias, A., Le Nagard, H., Denamur, E. and Clermont, O. (2018) 'ClermonTyping: an easy-to-use and accurate in silico method for Escherichia genus strain phylotyping', Microbial Genomics, 4(7), p. e000192. Available at: https://doi.org/10.1099/mgen.0.000192
Bohaychuk, V.M., Gensler, G.E., King, R.K., Manninen, K.I., Sorensen, O., Wu, J.T., Stiles, M.E. and McMullen, L.M. (2006) 'Occurrence of pathogens in raw and ready-to-eat meat and poultry products collected from the retail marketplace in Edmonton, Alberta, Canada', Journal of Food Protection, 69(9), pp. 2176–2182. Available at: https://doi.org/10.4315/0362028X-69.9.2176
Bouzari, S., Farhang, E., Hosseini, S.M. and Alikhani, M.Y. (2018) 'Prevalence and antimicrobial resistance of Shiga toxin-producing Escherichia coli and enteropathogenic Escherichia coli isolated from patients with acute diarrhea', Iranian Journal of Microbiology, 10(3), pp. 151–157.
Clermont, O., Christenson, J.K., Denamur, E. and Gordon, D.M. (2013) 'The Clermont Escherichia coli phylo-typing method revisited: Improvement of specificity and detection of new phylo-groups', Environmental Microbiology Reports, 5(1), pp. 58–65. Available at: https://doi.org/10.1111/1758-2229.12019
Clinical and Laboratory Standards Institute (CLSI) (2021) Performance Standards for Antimicrobial Susceptibility Testing. 31st edn. CLSI supplement M100. Wayne, Pennsylvania, USA: Clinical and Laboratory Standards Institute.
Connolly, G. and Campbell, W.W. (2023) 'Poultry consumption and human cardiometabolic health-related outcomes: A narrative review', Nutrients, 15(16), p. 3550. Available at: https://doi.org/10.3390/nu15163550
Davis, G.S., Waits, K., Nordstrom, L., Grande, H., Weaver, B., Papp, K., Horwinski, J., Koch, B., Hungate, B.A., Liu, C.M. and Price, L.B. (2018) 'Antibiotic-resistant Escherichia coli from retail poultry meat with different antibiotic use claims', BMC Microbiology, 18, p. 174. Available at: https://doi.org/10.1186/s12866-018-1322-5
Egea, P., López-Cerero, L., Torres, E., Del Carmen Gómez-Sánchez, M., Serrano, L., Sánchez-Ortiz, M.D.N., Rodriguez-Baño, J. and Pascual, A. (2012) 'Increased raw poultry meat colonization by extended spectrum beta-lactamase-producing Escherichia coli in the south of Spain', International Journal of Food Microbiology, 159(2), pp. 69–73. Available at: https://doi.org/10.1016/j.ijfoodmicro.2012.08.002
Eibach, D., Dekker, D., Boahen, K.G., Akenten, C.W., Sarpong, N., Campos, C.B., Berneking, L., Aepfelbacher, M., Krumkamp, R., Owusu-Dabo, E. and May, J. (2018) 'Extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in local and imported poultry meat in Ghana', Veterinary Microbiology, 217, pp. 7–12. Available at: https://doi.org/10.1016/j.vetmic.2018.02.023
Eid, S. and Samir, A.H. (2019) 'Extended-spectrum beta-lactamase and Class 1 integrons in multidrug-resistant Escherichia coli isolated from turkeys', Veterinary World, 12(7), pp. 1167–1174. Available at: https://doi.org/10.14202/vetworld.2019.1167-1174
Endale, H., Mathewos, M. and Abdeta, D. (2023) 'Potential causes of spread of antimicrobial resistance and preventive measures in one health perspective-a review', Infection and Drug Resistance, 16, pp. 7515–7545. Available at: https://doi.org/10.2147/IDR.S428837
Foster-Nyarko, E. and Pallen, M.J. (2022) 'The microbial ecology of Escherichia coli in the vertebrate gut', FEMS Microbiology Reviews, 46(3), p. fuac008. Available at: https://doi.org/10.1093/femsre/fuac008
Freedman, S.B., Van De Kar, N.C.A.J. and Tarr, P.I. (2023) 'Shiga toxin–producing Escherichia coli and the hemolytic–uremic syndrome', New England Journal of Medicine, 389(15), pp. 1402-1414. Available at: https://doi.org/10. 1056/NEJMra2108739
Gholami-Ahangaran, M., Moravvej, A.H., Safizadeh, Z., Sadeghi Nogoorani, V., Zokaei, M. and Ghasemian, S.O. (2021) 'The evaluation of ESBL genes and antibiotic resistance rate in Escherichia coli strains isolated from meat and intestinal contents of turkey in Isfahan, Iran', Iranian Journal of Veterinary Research, 22(4), pp. 318–325. Available at: https://doi.org/10.22099/ijvr.2021.39493.5737
Hessain, A.M., Al-Arfaj, A.A., Zakri, A.M., El-Jakee, J.K., Al-Zogibi, O.G., Hemeg, H.A. and Ibrahim, I.M. (2015) 'Molecular characterization of Escherichia coli O157: H7 recovered from meat and meat products relevant to human health in Riyadh, Saudi Arabia', Saudi Journal of Biological Sciences, 22(6), pp. 725–729. Available at: https://doi.org/10.1016/j.sjbs.2015.06.009
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Kaesbohrer, A., Schroeter, A., Tenhagen, B.-A., Alt, K., Guerra, B. and Appel, B. (2012) 'Emerging antimicrobial resistance in commensal Escherichia coli with public health relevance', Zoonoses and Public Health, 59, pp. 158–165. Available at: https://doi.org/10.1111/j.1863-2378.2011.01451.x
Khaitsa, M.L., Oloya, J., Doetkott, D. and Kegode, R. (2008) 'Antimicrobial resistance and association with class 1 integrons in Escherichia coli isolated from turkey meat products', Journal of Food Protection, 71(8), pp. 1679–1684. Available at: https://doi.org/10.4315/0362-028X-71.8.1679
Mare, A.D., Ciurea, C.N., Man, A., Tudor, B., Moldovan, V., Decean, L. and Toma, F. (2021) 'Enteropathogenic Escherichia coli—a Summary of the literature', Gastroenterology Insights, 12(1), pp. 28–40. Available at: https://doi.org/10.3390/gastroent12010004
Markey, B., Leonard, F., Archambault, M., Cullinane, A. and Maguire, D. (2013) Clinical Veterinary Microbiology. 2nd edn. London, UK: Elsevier Health Sciences.
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Moawad, A.A., Hotzel, H., Neubauer, H., Ehricht, R., Monecke, S., Tomaso, H., Hafez, H.M., Roesler, U. and El-Adawy, H. (2018) 'Antimicrobial resistance in Enterobacteriaceae from healthy broilers in Egypt: emergence of colistin-resistant and extended-spectrum β-lactamase-producing Escherichia coli', Gut Pathogens, 10, p. 39. Available at: https://doi.org/10.1186/s13099-018-0266-5
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Wang, M., Jiang, M., Wang, Z., Chen, R., Zhuge, X. and Dai, J. (2021) 'Characterization of antimicrobial resistance in chicken-source phylogroup F Escherichia coli: similar populations and resistance spectrums between E. coli recovered from chicken colibacillosis tissues and retail raw meats in Eastern China', Poultry Science, 100(9), p. 101370. Available at: https://doi.org/10.1016/j.psj.2021.101370
Wasyl, D., Hoszowski, A., Zając, M. and Szulowski, K. (2013) 'Antimicrobial resistance in commensal Escherichia coli isolated from animals at slaughter', Frontiers in Microbiology, 4, p. 221. Available at: https://doi.org/10.3389/fmicb.2013.00221
Xie, H., Ogura, Y. and Suzuki, Y. (2022) 'Persistence of antibiotic-resistant Escherichia coli strains belonging to the B2 phylogroup in municipal wastewater under aerobic conditions', Antibiotics, 11(2), p. 202. Available at: https://doi.org/10.3390/antibiotics11020202
Younis, G., Awad, A. and Mohamed, N. (2017) 'Phenotypic and genotypic characterization of antimicrobial susceptibility of avian pathogenic Escherichia coli isolated from broiler chickens', Veterinary World, 10(10), pp. 1167–1172. Available at: https://doi.org/10.14202/vetworld.2017.1167-1172
Zarei, O., Shokoohizadeh, L., Hossainpour, H. and Alikhani, M.Y. (2021) 'The prevalence of Shiga toxin-producing Escherichia coli and enteropathogenic Escherichia coli isolated from raw chicken meat samples', International Journal of Microbiology, 2021, p. 3333240. Available at: https://doi.org/10.1155/2021/3333240
*Corresponding author (M. Bagheri)
E-mail: ma.bagheri@uk.ac.ir
ORCID ID: https://orcid.org/0000-0003-0522-9747
E-mail: ma.bagheri@uk.ac.ir
ORCID ID: https://orcid.org/0000-0003-0522-9747
Type of Study: Original article |
Subject:
Special
Received: 24/07/17 | Accepted: 25/09/15 | Published: 26/03/20
Received: 24/07/17 | Accepted: 25/09/15 | Published: 26/03/20
References
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