The evaluation of ESBL genes and antibiotic resistance rate in Escherichia coli strains isolated from meat and intestinal contents of turkey in Isfahan, Iran

Document Type : Full paper (Original article)


1 Department of Clinical Sciences, Faculty of Veterinary Medicine, Shahrekord Branch, Islamic Azad University, Shahrekord, Iran

2 Undergraduate in Faculty of Veterinary Medicine, Sanandaj Branch, Islamic Azad University, Sanandaj, Iran

3 Undergraduate in Faculty of Veterinary Medicine, Shahid Bahonar University of Kerman, Kerman, Iran

4 Graduated from Faculty of Veterinary Medicine, Shahrekord Branch, Islamic Azad University, Shahrekord, Iran

5 Department of Food Science and Technology, Faculty of Nutrition Science, Food Science and Technology/National Nutrition and Food Technology Research Institute, Shahid Beheshti University of Medical Sciences, Tehran, Iran

6 Department of Veterinary, Behbahan Branch, Islamic Azad University, Behbahan, Iran


Background: Extended spectrum beta-lactamase (ESBL) has been described in Escherichia coli strains that have been isolated from humans and animals; it has induced a main concern with antibiotic resistance in serious bacterial infections. Aims: This study aimed to investigate the frequency of ESBL-producing E. coli (EPE) strains in meat and intestinal contents of turkey, and to compare the antibiotic resistance profile between EPE and non-EPE strains. Methods: Totally, 70 and 110 E. coli strains were isolated from turkey meat and turkey intestinal content samples, respectively. To determine EPE strains, double disc synergy test was applied by that 20 and 22 EPE strains were finally identified in meats and intestinal contents of the turkeys, respectively. Antibiotic susceptibility was exerted using disc diffusion method. Escherichia coli isolates were then characterized for virulence genes (stx-1 and stx-2) and ESBL genes (TEM, SHV, and CTX-M). Results: None of the E. coli strains harbored stx genes. The EPE strains in comparison with non-EPE strains were significantly more resistant to ciprofloxacin (47.6 vs 26.5%), tetracycline (80.9 vs 67.3%), ampicillin (47.6 vs 22.4%), penicillin (23.8 vs 10.2%), ceftazidime (57.1 vs 16.3%), ceftriaxone (38.1 vs 18.4%), and cefotaxime (47.6 vs 8.2%). The majority of EPE strains carried CTX-M gene. SHV showed the lowest frequency and it was not detected in EPE strains isolated from the intestinal contents. In this study, 75% of TEM-producing E. coli strains and 33% of SHV-producing E. coli strains were resistant to ampicillin. In addition, 41.7% of TEM-producing E. coli strains were resistant to penicillin, and 76.9% of CTX-producing E. coli were resistant to cefotaxime. Furthermore, 4.7% of EPE strains isolated from turkey meat were imipenem resistant. Conclusion: The resistance to cefotaxime and imipenem in EPE strains induces a concern in growing antibiotic resistance against broad spectrum antibiotics in E. coli strains.


Main Subjects

Acikgoz, ZC; Koseoglu, EO and Kocagoz, S (2007). CTX-M-3 Beta lactamase produsing Shigella sonnei isolated from pediatric bacillary dysentery cases. Jpn. J. Infect. Dis., 61: 135-137.
Badri, A; Ibrahim, I; Mohamed, S; Garbi, M; Kabbashi, A and Arbab, M (2017). Prevalence of extended-spectrum beta-lactamase (ESBL) producing Escherichia coli and Klebsiella pneumoniae isolated from raw milk samples in Al Jazirah State; Sudan. Mol. Biol., 7: 201-209.
Ben Slama, K; Jouini, A; Ben Sallem, R; Somalo, S; Sáenz, Y; Estepa, V and Torres, C (2010). Prevalence of broad-spectrum cephalosporin-resistant Escherichia coli isolates in food samples in Tunisia; and characterization of integrons and antimicrobial resistance mechanisms implicated. Int. J. Food Microbiol., 137: 281-286.
Bezabih, YM; Sabiiti, W; Alamneh, E; Bezabih, A; Peterson, GM; Bezabhe, WM and Roujeinikova, A (2021). The global prevalence and trend of human intestinal carriage of ESBL-producing Escherichia coli in the community. J. Antimicrob. Chemother., 76: 22-29.
Birgand, G; Castro-Sánchez, E; Hansen, S; Gastmeier, P; Lucet, J; Ferlie, E; Holmes, A and Ahmed, R (2018). Comparison of governance approaches for the control of antimicrobial resistance: Analysis of three European countries. Antimicrob. Resist. Infect. Control. 7: 1-12.
Botelho, LAB; Kraychete, GB; Costa e Silva, JL; Regis, DVV; Picão, RC; Moreira, BM and Bonelli, RR (2015). Widespread distribution of CTX-M and plasmid-mediated AmpC β-lactamases in Escherichia coli from Brazilian chicken meat. Mem. I. Oswaldo. Cruz., 110: 249-254.
Carvalho, I; Alonso, CA; Silva, V; Pimenta, P; Cunha, R; Martins, C and Poeta, P (2020). Extended-spectrum beta-lactamase-producing Klebsiella pneumoniae isolated from healthy and sick dogs in Portugal. Microb. Drug Resist., 26: 709-715.
Chopra, I and Roberts, M (2001). Tetracycline antibiotics: mode of action; applications; molecular biology; and epidemiology of bacterial resistance. Mic. Mol. Biol. Rev., 65: 232-260.
CLSI (2018). Performance standards for antimicrobial susceptibility testing. 28th Edn., Wayne, Pennsylvania, Clinical and Laboratory Standards Institute. PP: 1-258.
Costa, D; Vinue, L; Poeta, P; Coelho, AC; Matos, M; Sáenz, Y and Torres, C (2009). Prevalence of extended-spectrum beta-lactamase-producing Escherichia coli isolates in fecal samples of broilers. Vet. Microbiol., 138: 339-344.
Dierikx, C; Van der Goot, J; Fabri, T; van Essen-Zandbergen, A; Smith, H and Mevius, D (2013). Extended-spectrum β-lactamase and Ampc β-lactamase-producing Escherichia coli in Dutch broilers and broiler farmers. J. Antimicrob. Chemother., 68: 60-67.
Falgenhauer, L; Imirzalioglu, C; Oppong, K; Akenten, CW; Hogan, B; Krumkamp, R and Eibach, D (2019). Detection and characterization of ESBL-producing Escherichia coli from humans and poultry in Ghana. Front. Microbiol., 9: 3358-3366.
Gholami-Ahangaran, M; Ahmadi-Dastgerdi, A; Azizi, S; Basiratpour, A; Zokaei, M and Derakhshan, M (2021a). Thymol and carvacrol supplementation in poultry health and performance. Vet. Med. Sci., doi: 10.1002/vms3.663.
Gholami-Ahangaran, M and ZiaJahromi, N (2014). Identification of shiga toxin and intimin genes in Escherichia coli detected from canary (Serinus canaria domestica). Toxicol. Ind. Health. 30: 724-727.
Gholami-Ahangaran, M; Zinsaz, P; Pourmahdi, O; Ahmadi-Dastgerdi, A; Ostadpour, M and Soltani M (2021b). Tetracycline resistance genes in Escherichia coli strains isolated from biofilm of drinking water system in poultry farms. Acta Vet. Euracia. doi: 10.5152/actavet. 2021.20070.
Haeggman, S; Löfdahl, S; Paauw, A; Verhoef, J and Brisse, S (2004). Diversity and evolution of the class A chromosomal beta-lactamase gene in Klebsiella pneumoniae. Antimicrob. Agents Chemother., 48: 2400-2408.
Jafari, RA; Motamedi, H; Maleki, E; Ghanbarpour, R and Mayahi, M (2016). Phylogenetic typing and detection of extended-spectrum β-lactamases in Escherichia coli isolates from broiler chickens in Ahvaz; Iran. Vet. Res. Forum. 7: 227-232.
Junyoung, K; Semi, J; Hogeun, R; Bokkwon, L; Misun, P; Hoanjong, L; Jina, L and Seonghan, K (2009). Rapid detection of extended spectrum β-lactamase (ESBL) for Enterobacteriaceae by use of a multiplex PCR-based method. Infect. Chemother., 41: 181-184.
Kar, D; Bandyopadhyay, S; Bhattacharyya, D; Samanta, I; Mahanti, A; Nanda, PK and Singh, RK (2015). Molecular and phylogenetic characterization of multidrug resistant extended spectrum beta-lactamase producing Escherichia coli isolated from poultry and cattle in Odisha; India. Infect. Genet. Evol., 29: 82-90.
Khezri, A; Avershina, E and Ahmad, R (2021). Plasmid identification and plasmid-mediated antimicrobial gene detection in Norwegian isolates. Microorganisms. 9: 52-65.
Kuralayanapalya, SP; Patil, SS; Hamsapriya, S; Shinduja, R and Roy, P (2019). Amachawadi RG. Prevalence of extended-spectrum beta-lactamase producing bacteria from animal origin: A systematic review and meta-analysis report from India. PloS One. 14: e0221771.
Leverstein-van Hall, MA; Dierikx, CM; Cohen Stuart, J; Voets, GM; Van Den Munckhof, MP and van Essen-Zandbergen, A (2011). Dutch patients; retail chicken meat and poultry share the same ESBL genes; plasmids and strains. Clin. Microbiol. Infect., 17: 873-880.
Li, J; Ma, Y; Hu, C; Jin, S; Zhang, Q; Ding, H and Cui, S (2010). Dissemination of cefotaxime-M-producing Escherichia coli isolates in poultry farms; but not swine farms; in China. Foodborne Pathog. Dis., 7: 1387-1392.
Mobasseri, G; The, CSJ; Ooi, PT; Tan, SC and Thong, KL (2019). Molecular characterization of multidrug-resistant and extended-spectrum beta-lactamase-producing Klebsiella pneumoniae isolated from swine farms in Malaysia. Microb. Drug Resist., 25: 1087-1098.
Momtaz, H; Rahimi, E and Moshkelani, S (2012). Molecular detection of antimicrobial resistance genes in E. coli isolated from slaughtered commercial chickens in Iran. Vet. Med., 57: 193-197.
Overdevest, I; Willemsen, I; Rijnsburger, M; Eustace, A; Xu, L; Hawkey, P and Kluytmans, J (2011). Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans; The Netherlands. Emerg. Infect. Dis., 17: 1216-1222.
Pehlivanlar Önen, S; Aslantaş, Ö; Şebnem Yılmaz, E and Kürekci, C (2015). Prevalence of β-lactamase producing Escherichia coli from retail meat in Turkey. J. Food Sci., 80: M2023-M2029.
Rahimi, E; Hormozipoor, H; Gholami Ahangaran, M and Yazdi F (2012). Prevalence of Arcobacter species on chicken carcasses during processing in Iran. J. Appl. Poult. Res., 21: 407-412.
Rahman, SU; Ahmad, S and Khan, I (2019). Incidence of ESBL-producing Escherichia coli in poultry farm environment and retail poultry meat. Pak. Vet. J., 39: 116-120.
Reich, F; Atanassova, V and Klein, G (2013). Extended-spectrum β-lactamase and Ampc-producing Enterobacteria in healthy broiler chickens; Germany. Emerg. Infect. Dis., 19: 1253-1259.
Roberts, MC (1996). Tetracycline resistance determinants: mechanisms of action; regulation of expression; genetic mobility; and distribution. FEMS Mic. Rev., 19: 1-24.
Sabat, G; Rose, P; Hickey, WJ and Harkin, JM (2000). Selective and sensitive method for PCR amplification of
Escherichia coli 16S rRNA genes in soil. Appl. Environ. Microbiol., 66: 844-849.
Samanta, A; Mahanti, A; Chatterjee, S; Joardar, SN; Bandyopadhyay, S; Sar, TK and Samanta, I (2018). Pig farm environment as a source of beta-lactamase or AmpC-producing Klebsiella pneumoniae and Escherichia coli. Ann. Microbiol., 68: 781-791.
Sengeløv, G; Halling-Sørensen, B and Aarestrup, FM (2003). Susceptibility of Escherichia coli and Enterococcus faecium isolated from pigs and broiler chickens to tetracycline degradation products and distribution of tetracycline resistance determinants in E. coli from food animals. Vet. Mic., 95: 91-101.
Smet, A; Martel, A; Persoons, D; Dewulf, J; Heyndrickx, M; Catry, B and Butaye, P (2008). Diversity of extended-spectrum β-lactamases and class C β-lactamases among cloacal Escherichia coli isolates in Belgian broiler farms. Antimicrob. Agents Chemother., 52: 1238-1243.
Teimuri, S; Gholami-Ahangaran, M and Shakerian, A (2008). The comparison of enrofloxacin residue in chicken and turkey meat; by high performance liquid chromatography in Isfahan province. Iran. Food Hyg., 8: 95-100.
Xu, L; Shabir, S; Bodah, T; McMurray, C; Hardy, K; Hawkey, P and Nye, K (2011). Regional survey of CTX-M type extended-spectrum β-lactamses among Entero-bacteriaceae reveals heterogenecity in the distribution of the ST131 clone. J. Antimicrob. Chemother., 66: 505-511.
Yazdi, M; Nazemi, A; Mirinargasi, M; Khataminejad, MR; Sharifi, S and Babaikochkaksaraei, M (2010). Prevalence of SHV/CTXM/TEM (ESBL) beta-lactamase resistance genes in Escherichia coli isolated from urinary tract infections in Tehran; Iran. Iran. Med. Lab. J., 4: 67-73 (persian).