Plasmid-mediated quinolone resistance in Escherichia coli isolates from commercial broiler chickens in Semnan, Iran
,
Abstract
Background and Objectives: Antibiotic resistance within the poultry sector presents a considerable health concern due to treatment inefficacy and resistance transmission to humans and the environment. The investigation of plasmid-mediated quinolone resistance (PMQR) in Escherichia coli, acknowledged for its role in advancing resistance, remains inadequately studied in Iranian poultry. This study aimed to evaluate PMQR gene prevalence as well as to determine correlation between resistance phenotype and genotype in E. coli obtained from poultry colibacillosis.
Materials and Methods: A collection of 100 E. coli isolates from the viscera of broilers suspected to colibacillosis was assessed. Using the Kirby-Bauer disk diffusion method, antimicrobial susceptibility tests were conducted for ofloxacin, nalidixic acid, levofloxacin, ciprofloxacin, and ampicillin. Additionally, PCR was employed to screen for qnrS, qnrB, and aac(6)Ib-cr genes.
Results: Among the analyzed E. coli isolates, 51% demonstrated resistance to at least one of the tested antibiotics, with 17% exhibiting resistance to four different antibiotics. Nalidixic acid displayed the highest resistance rate at 48%, while ampicillin had the lowest at 16%. PMQR genes were detected in 28% of the E. coli isolates, with aac(6′)-Ib-cr being the most prevalent at 14%, followed by qnrB in 13%, and qnrS in 7%.
Conclusion: The study underscores the vital need for careful antibiotic usage in poultry to curb the emergence of antibiotic-resistant bacteria. The results illuminate the prevalence of PMQR genes and their association with resistance trends in Iranian poultry, forming a pivotal basis for forthcoming approaches to combat antibiotic resistance within the poultry sector.
1. Iskandar K, Molinier L, Hallit S, Sartelli M, Catena F, Coccolini F, et al. Drivers of antibiotic resistance transmission in low-and middle-income countries from a “one health” perspective-A review. Antibiotics (Basel) 2020; 9: 372.
2. Rahman MM, Husna A, Elshabrawy HA, Alam J, Runa NY, Badruzzaman ATM, et al. Isolation and molecular characterization of multidrug-resistant Escherichia coli from chicken meat. Sci Rep 2020; 10: 21999.
3. Panth Y. Colibacillosis in poultry: A review. J Agric Nat Resour 2019; 2: 301-311.
4. Niero G, Bortolaia V, Vanni M, Intorre L, Guardabassi L, Piccirillo A. High diversity of genes and plasmids encoding resistance to third-generation cephalosporins and quinolones in clinical Escherichia coli from commercial poultry flocks in Italy. Vet Microbiol 2018; 216: 93-98.
5. Röderova M, Halova D, Papousek I, Dolejska M, Masarikova M, Hanulik V, et al. Characteristics of quinolone resistance in Escherichia coli isolates from humans, animals, and the environment in the Czech Republic. Front Microbiol 2017; 7: 2147.
6. FarajzadehSheikh A, Veisi H, Shahin M, Getso M, Farahani A. Frequency of quinolone resistance genes among extended-spectrum β-lactamase (ESBL)-producing Escherichia coli strains isolated from urinary tract infections. Trop Med Health 2019; 47: 19.
7. Jacoby GA, Strahilevitz J, Hooper DC. Plasmid‐mediated quinolone resistance. Microbiol Spectr 2014; 2: 10.1128/microbiolspec.PLAS-0006-2013.
8. Li X-Z. Quinolone resistance in bacteria: emphasis on plasmid-mediated mechanisms. Int J Antimicrob Agents 2005; 25: 453-463.
9. Mohammadzadeh M, Montaseri M, Hosseinzadeh S, Majlesi M, Berizi E, Zare M, et al. Antibiotic residues in poultry tissues in Iran: A systematic review and meta-analysis. Environ Res 2022; 204: 112038.
10. Pouyan S, Kafshdouzan K, Jebelli A. Synergistic effect of cinnamomum camphora and origanum vulgare essential oils against blaCTX-M Producing Escherichia coli isolated from poultry colibacillosis. J Med Bacteriol 2021; 10: 20-29.
11. Ciesielczuk H, Hornsey M, Choi V, Woodford N, Wareham DW. Development and evaluation of a multiplex PCR for eight plasmid-mediated quinolone-resistance determinants. J Med Microbiol 2013; 62: 1823-1827.
12. Seo KW, Lee YJ. Prevalence and characterization of plasmid mediated quinolone resistance genes and class 1 integrons among multidrug-resistant Escherichia coli isolates from chicken meat. J Appl Poult Res 2019; 28: 761-770.
13. Literak I, Reitschmied T, Bujnakova D, Dolejska M, Cizek A, Bardon J, et al. Broilers as a source of quinolone-resistant and extraintestinal pathogenic Escherichia coli in the Czech Republic. Microb Drug Resist 2013; 19: 57-63.
14. Zahraei Salehi T, Farashi Bonab S. Antibiotics susceptibility pattern of Escherichia coli strains isolated from chickens with colisepticemia in Tabriz province, Iran. Int J Poult Sci 2006; 5: 677-684.
15. Bakhshi M, Fatahi Bafghi M, Astani A, Ranjbar VR, Zandi H, Vakili M. Antimicrobial resistance pattern of Escherichia coli isolated from chickens with colibacillosis in Yazd, Iran. J Food Qual Hazards Control 2017; 4: 74-78.
16. Rahimi E, Ameri M. Antimicrobial resistance patterns of Campylobacter spp. isolated from raw chicken, turkey, quail, partridge, and ostrich meat in Iran. Food Control 2011; 22: 1165-1170.
17. Gholami-Ahangaran M, Moravvej AH, Safizadeh Z, Sadeghi Nogoorani V, Zokaei M, Ghasemian SO. The evaluation of ESBL genes and antibiotic resistance rate in Escherichia coli strains isolated from meat and intestinal contents of turkey in Isfahan, Iran. Iran J Vet Res 2021; 22: 318-325.
18. Mousavinafchi SB, Rahimi E, Shakerian A. Campylobacter spp. isolated from poultry in Iran: Antibiotic resistance profiles, virulence genes, and molecular mechanisms. Food Sci Nutr 2022; 11: 1142-1153.
19. Khademi F, Sahebkar A. Prevalence of fluoroquinolone-resistant Campylobacter species in Iran: a systematic review and meta-analysis. Int J Microbiol 2020; 2020: 8868197.
20. Vaez H, Ghanbari F, Sahebkar A, Khademi F. Antibiotic resistance profiles of Salmonella serotypes isolated from animals in Iran: a meta-analysis. Iran J Vet Res 2020; 21: 188-197.
21. Yu T, Jiang X, Fu K, Liu B, Xu D, Ji S, et al. Detection of extended‐spectrum β‐lactamase and plasmid‐mediated quinolone resistance determinants in Escherichia coli isolates from retail meat in China. J Food Sci 2015; 80: M1039-M1043.
22. Ghorbani A, Khoshbakht R, Kaboosi H, Shirzad-Aski H, Ghadikolaii FP. Study on antibiotic resistance and phylogenetic comparison of avian-pathogenic Escherichia coli (APEC) and uropathogenic Escherichia coli (UPEC) isolates. Vet Res Forum 2022; 13: 569-576.
23. Zarei O, Shokoohizadeh L, Hossainpour H, Alikhani MY. The prevalence of Shiga toxin-producing Escherichia coli and enteropathogenic Escherichia coli isolated from raw chicken meat samples. Int J Microbiol 2021; 2021: 3333240.
24. Ghavidel M, Gholamhosseini-Moghadam T, Nourian K, Ghazvini K. Virulence factors analysis and antibiotic resistance of uropathogenic Escherichia coli isolated from patients in northeast of Iran. Iran J Microbiol 2020; 12: 223-230.
25. Rasoulinasab M, Shahcheraghi F, Feizabadi MM, Nikmanesh B, Hajihasani A, Aslani MM. Distribution of ciprofloxacin-resistance genes among ST131 and non-ST131 clones of Escherichia coli isolates with ESBL phenotypes isolated from women with urinary tract infection. Iran J Microbiol 2021; 13: 294-302.
26. Jomehzadeh N, Saki M, Ahmadi K, Zandi G. The prevalence of plasmid-mediated quinolone resistance genes among Escherichia coli strains isolated from urinary tract infections in southwest Iran. Mol Biol Rep 2022; 49: 3757-3763.
27. Ferreira JC, Penha Filho RAC, Kuaye APY, Andrade LN, Berchieri Junior A, Darini ALDC. Identification and characterization of plasmid-mediated quinolone resistance determinants in Enterobacteriaceae isolated from healthy poultry in Brazil. Infect Genet Evol 2018; 60: 66-70.
28. Pourhossein Z, Asadpour L, Habibollahi H, Shafighi T. Antimicrobial resistance in fecal Escherichia coli isolated from poultry chicks in northern Iran. Gene Rep 2020; 21: 100926.
29. Kenyon C. Positive association between the use of quinolones in food animals and the prevalence of fluoroquinolone resistance in E. coli and K. pneumoniae, A. baumannii and P. aeruginosa: A global ecological analysis. Antibiotics (Basel) 2021; 10: 1193.
2. Rahman MM, Husna A, Elshabrawy HA, Alam J, Runa NY, Badruzzaman ATM, et al. Isolation and molecular characterization of multidrug-resistant Escherichia coli from chicken meat. Sci Rep 2020; 10: 21999.
3. Panth Y. Colibacillosis in poultry: A review. J Agric Nat Resour 2019; 2: 301-311.
4. Niero G, Bortolaia V, Vanni M, Intorre L, Guardabassi L, Piccirillo A. High diversity of genes and plasmids encoding resistance to third-generation cephalosporins and quinolones in clinical Escherichia coli from commercial poultry flocks in Italy. Vet Microbiol 2018; 216: 93-98.
5. Röderova M, Halova D, Papousek I, Dolejska M, Masarikova M, Hanulik V, et al. Characteristics of quinolone resistance in Escherichia coli isolates from humans, animals, and the environment in the Czech Republic. Front Microbiol 2017; 7: 2147.
6. FarajzadehSheikh A, Veisi H, Shahin M, Getso M, Farahani A. Frequency of quinolone resistance genes among extended-spectrum β-lactamase (ESBL)-producing Escherichia coli strains isolated from urinary tract infections. Trop Med Health 2019; 47: 19.
7. Jacoby GA, Strahilevitz J, Hooper DC. Plasmid‐mediated quinolone resistance. Microbiol Spectr 2014; 2: 10.1128/microbiolspec.PLAS-0006-2013.
8. Li X-Z. Quinolone resistance in bacteria: emphasis on plasmid-mediated mechanisms. Int J Antimicrob Agents 2005; 25: 453-463.
9. Mohammadzadeh M, Montaseri M, Hosseinzadeh S, Majlesi M, Berizi E, Zare M, et al. Antibiotic residues in poultry tissues in Iran: A systematic review and meta-analysis. Environ Res 2022; 204: 112038.
10. Pouyan S, Kafshdouzan K, Jebelli A. Synergistic effect of cinnamomum camphora and origanum vulgare essential oils against blaCTX-M Producing Escherichia coli isolated from poultry colibacillosis. J Med Bacteriol 2021; 10: 20-29.
11. Ciesielczuk H, Hornsey M, Choi V, Woodford N, Wareham DW. Development and evaluation of a multiplex PCR for eight plasmid-mediated quinolone-resistance determinants. J Med Microbiol 2013; 62: 1823-1827.
12. Seo KW, Lee YJ. Prevalence and characterization of plasmid mediated quinolone resistance genes and class 1 integrons among multidrug-resistant Escherichia coli isolates from chicken meat. J Appl Poult Res 2019; 28: 761-770.
13. Literak I, Reitschmied T, Bujnakova D, Dolejska M, Cizek A, Bardon J, et al. Broilers as a source of quinolone-resistant and extraintestinal pathogenic Escherichia coli in the Czech Republic. Microb Drug Resist 2013; 19: 57-63.
14. Zahraei Salehi T, Farashi Bonab S. Antibiotics susceptibility pattern of Escherichia coli strains isolated from chickens with colisepticemia in Tabriz province, Iran. Int J Poult Sci 2006; 5: 677-684.
15. Bakhshi M, Fatahi Bafghi M, Astani A, Ranjbar VR, Zandi H, Vakili M. Antimicrobial resistance pattern of Escherichia coli isolated from chickens with colibacillosis in Yazd, Iran. J Food Qual Hazards Control 2017; 4: 74-78.
16. Rahimi E, Ameri M. Antimicrobial resistance patterns of Campylobacter spp. isolated from raw chicken, turkey, quail, partridge, and ostrich meat in Iran. Food Control 2011; 22: 1165-1170.
17. Gholami-Ahangaran M, Moravvej AH, Safizadeh Z, Sadeghi Nogoorani V, Zokaei M, Ghasemian SO. The evaluation of ESBL genes and antibiotic resistance rate in Escherichia coli strains isolated from meat and intestinal contents of turkey in Isfahan, Iran. Iran J Vet Res 2021; 22: 318-325.
18. Mousavinafchi SB, Rahimi E, Shakerian A. Campylobacter spp. isolated from poultry in Iran: Antibiotic resistance profiles, virulence genes, and molecular mechanisms. Food Sci Nutr 2022; 11: 1142-1153.
19. Khademi F, Sahebkar A. Prevalence of fluoroquinolone-resistant Campylobacter species in Iran: a systematic review and meta-analysis. Int J Microbiol 2020; 2020: 8868197.
20. Vaez H, Ghanbari F, Sahebkar A, Khademi F. Antibiotic resistance profiles of Salmonella serotypes isolated from animals in Iran: a meta-analysis. Iran J Vet Res 2020; 21: 188-197.
21. Yu T, Jiang X, Fu K, Liu B, Xu D, Ji S, et al. Detection of extended‐spectrum β‐lactamase and plasmid‐mediated quinolone resistance determinants in Escherichia coli isolates from retail meat in China. J Food Sci 2015; 80: M1039-M1043.
22. Ghorbani A, Khoshbakht R, Kaboosi H, Shirzad-Aski H, Ghadikolaii FP. Study on antibiotic resistance and phylogenetic comparison of avian-pathogenic Escherichia coli (APEC) and uropathogenic Escherichia coli (UPEC) isolates. Vet Res Forum 2022; 13: 569-576.
23. Zarei O, Shokoohizadeh L, Hossainpour H, Alikhani MY. The prevalence of Shiga toxin-producing Escherichia coli and enteropathogenic Escherichia coli isolated from raw chicken meat samples. Int J Microbiol 2021; 2021: 3333240.
24. Ghavidel M, Gholamhosseini-Moghadam T, Nourian K, Ghazvini K. Virulence factors analysis and antibiotic resistance of uropathogenic Escherichia coli isolated from patients in northeast of Iran. Iran J Microbiol 2020; 12: 223-230.
25. Rasoulinasab M, Shahcheraghi F, Feizabadi MM, Nikmanesh B, Hajihasani A, Aslani MM. Distribution of ciprofloxacin-resistance genes among ST131 and non-ST131 clones of Escherichia coli isolates with ESBL phenotypes isolated from women with urinary tract infection. Iran J Microbiol 2021; 13: 294-302.
26. Jomehzadeh N, Saki M, Ahmadi K, Zandi G. The prevalence of plasmid-mediated quinolone resistance genes among Escherichia coli strains isolated from urinary tract infections in southwest Iran. Mol Biol Rep 2022; 49: 3757-3763.
27. Ferreira JC, Penha Filho RAC, Kuaye APY, Andrade LN, Berchieri Junior A, Darini ALDC. Identification and characterization of plasmid-mediated quinolone resistance determinants in Enterobacteriaceae isolated from healthy poultry in Brazil. Infect Genet Evol 2018; 60: 66-70.
28. Pourhossein Z, Asadpour L, Habibollahi H, Shafighi T. Antimicrobial resistance in fecal Escherichia coli isolated from poultry chicks in northern Iran. Gene Rep 2020; 21: 100926.
29. Kenyon C. Positive association between the use of quinolones in food animals and the prevalence of fluoroquinolone resistance in E. coli and K. pneumoniae, A. baumannii and P. aeruginosa: A global ecological analysis. Antibiotics (Basel) 2021; 10: 1193.
| Files | ||
| Issue | Vol 16 No 2 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v16i2.15352 | |
| Keywords | ||
| Anti-bacterial agents; Drug resistance; Escherichia coli; Poultry diseases; Quinolones | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Javadi B, Kafshdouzan K, Emadi Chashmi SH, Pazhand O. Plasmid-mediated quinolone resistance in Escherichia coli isolates from commercial broiler chickens in Semnan, Iran. Iran J Microbiol. 2024;16(2):193-200.
