The Prevalence of Fluoroquinolone-Resistant E. coli in Animals and Animal Products: A Systematic Review and Meta-Analysis
Fluoroquinolone-resistant E. coli in Iran
-
Hadi Sedigh Ebrahim-Saraie
,
Mohammad Esmaeil Amini
,
Meysam Hasannejad-Bibalan
,
Ervin Zadgari
,
Arash Bakhshi
Abstract
Background: Biological contamination of foods is a serious problem for human health. Animal and animal products may be contaminated by these biological and chemical contaminants. One of the most important causes of foodborne illness in humans is Escherichia coli. Fluoroquinolones can be used as a suitable treatment for enteric infections in food-producing livestock. We aimed to evaluate the current status of resistance of E. coli strains isolated from animals and animal products to fluoroquinolone in Iran.
Methods: A systematic search was conducted using the Web of Science, PubMed, Embase, Google Scholar, and Scopus databases from 2000 to Oct 2020. Nineteen studies were selected based on the inclusion criteria and analysis by Comprehensive Meta-Analysis.
Results: Based on the data analysis, The rates of antibiotic resistance in animal strains were as follows: Flumequine (75.1%), Enrofloxacin (55.2%), Danofloxacin (48.1%), Ciprofloxacin (48.4%), and Norfloxacin (52.9%). Next, the rates of quinolone resistance among E. coli strains isolated from animal products were Norfloxacin (45.5%), Ciprofloxacin (44.5%), and Enrofloxacin (60.9%). Based on the funnel plots and Egger's test, there was no significant publication bias.
Conclusion: We finally concluded that antibiotic resistance in commensal E. coli is related to the overuse of antibiotics in livestock, especially fluoroquinolones.
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2. Scallan E, Hoekstra RM, Angulo FJ, et al. Foodborne illness acquired in the United States--major pathogens. Emerg Infect Dis 2011; 17(1):7-15.
3. Salehi S, Nakhaei Moghadam M, Asgharian Rezaei Y, et al. Antibiotic resistance pattern and prevalence of tetA, tetB, tetR, OXA-10 and OXA-48 resistance genes among Escherichia coli isolates from toilets in Mashhad Azad University (Iran) in 2020. Iranian Journal of Medical Microbiology 2023; 17(2):167-75.
4. Gaschignard J, Levy C, Romain O, et al. Neonatal Bacterial Meningitis: 444 Cases in 7 Years. Pediatr Infect Dis J 2011; 30(3):212-7.
5. Momtaz H, Farzan R, Rahimi E, et al. Molecular characterization of Shiga toxin-producing Escherichia coli isolated from ruminant and donkey raw milk samples and traditional dairy products in Iran. Sci World J 2012;2012:231342.
6. van Duijn PJ, Dautzenberg MJ, Oostdijk EA. Recent trends in antibiotic resistance in European ICUs. Curr Opin Crit Care 2011; 17(6):658-65.
7. Suchi TA, Mishu ID, Akhter MZ, et al. Comparative antimicrobial efficacy, kinetic destruction pattern and microbial inactivation dynamics of extracted cinnamon essential oil and commercial cinnamaldehyde against foodborne pathogens. Iranian Journal of Medical Microbiology 2023; 17(2):230-42.
8. de Vrese M, Schrezenmeir J. Probiotics, prebiotics, and synbiotics. Adv Biochem Engin/Biotechnol 2008; 111:1-66.
9. Martinez JL, Baquero F. Interactions among strategies associated with bacterial infection: pathogenicity, epidemicity, and antibiotic resistance. Clin Microbiol Rev 2002; 15(4):647-79.
10. Miles TD, McLaughlin W, Brown PD. Antimicrobial resistance of Escherichia coli isolates from broiler chickens and humans. BMC Vet Res 2006; 2:7.
11. Redgrave LS, Sutton SB, Webber MA, et al. Fluoroquinolone resistance: mechanisms, impact on bacteria, and role in evolutionary success. Trends Microbiol 2014; 22(8):438-45.
12. Lesher GY, Froelich EJ, Gruett MD, et al. 1,8-Naphthyridine Derivatives. A New Class of Chemotherapeutic Agents. J Med Pharma Chem 1962; 91:1063-5.
13. Patrick G. Antibacterial agents in an introduction to medicinal chemistry. Oxford University Press, Oxford, New York; 2003.
14. Fao J. OIE/WHO Expert Workshop on Non-Human Antimicrobial Usage and Antimicrobial Resistance: scientific assessment (Geneva, 1-5 December 2003). Geneva. World Health Organisation. 2004.
15. Shokoohizadeh L, Rabiei M, Baharifar A, et al. Evaluation of the virulence genes in quinolone and fluoroquinolones-resistant uropathogenic Escherichia coli isolates. Iranian Journal of Medical Microbiology 2022; 16(6):581-6.
16. Pourhossein Z, Asadpour L, Habibollahi H, et al. Antimicrobial resistance in fecal Escherichia coli isolated from poultry chicks in northern Iran. Gene Rep 2020; 21:100926.
17. Dehdashti S, Ghanbarpour R, Hajikolaei MRH. Molecular detection of Shiga toxin–producing and antibiotic-resistant Escherichia coli isolates from buffaloes in southwest of Iran. Trop Anim Health Prod 2019; 51(6):1725-36.
18. Mohammadi V, Ghaniei A, Sepehrnia P. Antimicrobial resistance profile and prevalence of tetracycline resistance genes in Escherichia coli isolates from broiler chickens, Northwestern Iran. Bulg J Vet Med 2018; 21(2):169-75.
19. Ranjbar R, Safarpoor Dehkordi F, Sakhaei Shahreza MH, et al. Prevalence, identification of virulence factors, O-serogroups and antibiotic resistance properties of Shiga-toxin producing Escherichia coli strains isolated from raw milk and traditional dairy products. Antimicrob Resist Infect Control 2018; 7(1):1-11.
20. Boroomand Z, Jafari R, Gharibi D, et al. An investigation into enterobacteriaceae responsible for early mortality in japanese quail chicks and their antibiotic susceptibility patterns. Arch Razi Inst 2018; 73(4):277-85.
21. Bakhshi M, Fatahi Bafghi M, Astani A, et al. Antimicrobial resistance pattern of Escherichia coli isolated from chickens with colibacillosis in Yazd, Iran. J Food Qual Hazards Control 2017; 4(3):74-8.
22. Safavi EA, Shahbazi Y. Antimicrobial resistance in Escherichia coli isolated from different parts of the digestive tract of sheep. Bulg J Vet Med 2017; 20(3):271-5.
23. Chaleshtori FS, Arani NM, Aghadavod E, et al. Molecular characterization of Escherichia coli recovered from traditional milk products in Kashan, Iran. Vet World 2017; 10(10):1264.
24. Hasani B, Banani M, Nouri A, et al. Detection of three virulence genes and antibiotic resistance profiles in Escherichia coli isolates from commercial broilers with colibacillosis in Tabriz, Iran. Arch Razi Inst 2017; 72(1):1-8.
25. Kheiri R, Ranjbar R, Khamesipour F, et al. Role of antibiotic in drug resistance and integrons prevalence in Escherichia coli isolated from human and animal specimens. Mol Microbiol 2016; 1(3).
26. Bonyadian M, Moshtaghi H, Taheri MA, editors. Molecular characterization and antibiotic resistance of enterotoxigenic and entero-aggregative Escherichia coli isolated from raw milk and unpasteurized cheeses. Veterinary Research Forum: an International Quarterly Journal; 2014: Faculty of Veterinary Medicine, Urmia University, Urmia, Iran.
27. Talebiyan R, Kheradmand M, Khamesipour F, et al. Multiple antimicrobial resistance of Escherichia coli isolated from chickens in Iran. Vet Med Int 2014; 32(1):115-23.
28. Abdi-Hachesoo B, Asasi K, Sharifiyazdi H. Farm-level evaluation of enrofloxacin resistance in Escherichia coli isolated from broiler chickens during a rearing period. Comp Clin Path 2017; 26(2):471-6.
29. Rahimi M. Antibioresistance profile of avian pathogenic Escherichia coli isolates recovered from broiler chicken farms with colibacillosis in Kermanshah province, Iran. Glob Vet 2013; 10(4):447-52.
30. Seifi S, Shirzad M. Antimicrobial susceptibility of Escherichia coli isolated from free range poultry or wild birds at the southern Caspian Sea coast of Iran. J Hell Vet Med Soc 2013; 64(4):249-54.
31. Momtaz H, Jamshidi A. Shiga toxin-producing Escherichia coli isolated from chicken meat in Iran: Serogroups, virulence factors, and antimicrobial resistance properties. Poult Sci J 2013; 92(5):1305-13.
32. Rad M, Kooshan M, Mesgarani H. Quinolone resistance among Salmonella enterica and Escherichia coli of animal origin. Comp Clin Path 2012; 21(2):161-5.
33. Momtaz H, Rahimi E, Moshkelani S. Molecular detection of antimicrobial resistance genes in E. coli isolated from slaughtered commercial chickens in Iran. Vet Med 2012; 57(4):193-7.
34. Tabatabaei M, Marashi NF, Mokarizade A. Transferable plasmid mediating multi-antibiotic resistance in non-pathogenic Escherichia coli isolates from chicken flocks. Glob Vet 2010; 5(6):371-5.
35. Emery D, Nagaraja KV, Shaw D, et sl. Virulence factors of Escherichia coli associated with colisepticemia in chickens and turkeys. Avian Dis 1992; 504-11.
36. Hammerum AM, Heuer OE. Human health hazards from antimicrobial-resistant Escherichia coli of animal origin. Clin Infect Dis 2009; 48(7):916-21.
37. Mahmoud Farhan S, Mahmoud Abd El-Baky R, Abdalla M, et al. Efficacy of amikacin and imipenem against multi-drug resistant gram-negative bacteria isolated from wound Infections, Egypt. Iranian Journal of Medical Microbiology 2023; 17(2):218-29.
38. Fortini D, Fashae K, García-Fernández A, et al. Plasmid-mediated quinolone resistance and β-lactamases in Escherichia coli from healthy animals from Nigeria. J Antimicrob Chemother 2011; 66(6):1269-72.
39. Yang T, Zeng Z, Rao L, et al. The association between occurrence of plasmid-mediated quinolone resistance and ciprofloxacin resistance in Escherichia coli isolates of different origins. Vet Microbiol 2014; 170(1-2):89-96.
40. Seo KW, Lee YJ. Characterization of plasmid mediated quinolone resistance determinants in ciprofloxacin resistant-Escherichia coli from chicken meat produced by integrated broiler operations in Korea. Int J Food Microbiol 2019; 307:108274.
41. Van den Bogaard A, London N, Driessen C, et al. Antibiotic resistance of faecal Escherichia coli in poultry, poultry farmers and poultry slaughterers. J Antimicrob Chemother 2001; 47(6):763-71.
42. Fakhraddin Raheem T, Ahmed Hasan Ali S. Prevalence and multi-drug resistance patterns of uropathogenic E. coli isolated from women patients in Kirkuk city, Iraq. Iranian Journal of Medical Microbiology 2022; 16(6):609-14.
43. Gosling R, Clouting C, Randall L, et al. Ciprofloxacin resistance in E. coli isolated from turkeys in Great Britain. Avian Pathol 2012; 41(1):83-9.
2. Scallan E, Hoekstra RM, Angulo FJ, et al. Foodborne illness acquired in the United States--major pathogens. Emerg Infect Dis 2011; 17(1):7-15.
3. Salehi S, Nakhaei Moghadam M, Asgharian Rezaei Y, et al. Antibiotic resistance pattern and prevalence of tetA, tetB, tetR, OXA-10 and OXA-48 resistance genes among Escherichia coli isolates from toilets in Mashhad Azad University (Iran) in 2020. Iranian Journal of Medical Microbiology 2023; 17(2):167-75.
4. Gaschignard J, Levy C, Romain O, et al. Neonatal Bacterial Meningitis: 444 Cases in 7 Years. Pediatr Infect Dis J 2011; 30(3):212-7.
5. Momtaz H, Farzan R, Rahimi E, et al. Molecular characterization of Shiga toxin-producing Escherichia coli isolated from ruminant and donkey raw milk samples and traditional dairy products in Iran. Sci World J 2012;2012:231342.
6. van Duijn PJ, Dautzenberg MJ, Oostdijk EA. Recent trends in antibiotic resistance in European ICUs. Curr Opin Crit Care 2011; 17(6):658-65.
7. Suchi TA, Mishu ID, Akhter MZ, et al. Comparative antimicrobial efficacy, kinetic destruction pattern and microbial inactivation dynamics of extracted cinnamon essential oil and commercial cinnamaldehyde against foodborne pathogens. Iranian Journal of Medical Microbiology 2023; 17(2):230-42.
8. de Vrese M, Schrezenmeir J. Probiotics, prebiotics, and synbiotics. Adv Biochem Engin/Biotechnol 2008; 111:1-66.
9. Martinez JL, Baquero F. Interactions among strategies associated with bacterial infection: pathogenicity, epidemicity, and antibiotic resistance. Clin Microbiol Rev 2002; 15(4):647-79.
10. Miles TD, McLaughlin W, Brown PD. Antimicrobial resistance of Escherichia coli isolates from broiler chickens and humans. BMC Vet Res 2006; 2:7.
11. Redgrave LS, Sutton SB, Webber MA, et al. Fluoroquinolone resistance: mechanisms, impact on bacteria, and role in evolutionary success. Trends Microbiol 2014; 22(8):438-45.
12. Lesher GY, Froelich EJ, Gruett MD, et al. 1,8-Naphthyridine Derivatives. A New Class of Chemotherapeutic Agents. J Med Pharma Chem 1962; 91:1063-5.
13. Patrick G. Antibacterial agents in an introduction to medicinal chemistry. Oxford University Press, Oxford, New York; 2003.
14. Fao J. OIE/WHO Expert Workshop on Non-Human Antimicrobial Usage and Antimicrobial Resistance: scientific assessment (Geneva, 1-5 December 2003). Geneva. World Health Organisation. 2004.
15. Shokoohizadeh L, Rabiei M, Baharifar A, et al. Evaluation of the virulence genes in quinolone and fluoroquinolones-resistant uropathogenic Escherichia coli isolates. Iranian Journal of Medical Microbiology 2022; 16(6):581-6.
16. Pourhossein Z, Asadpour L, Habibollahi H, et al. Antimicrobial resistance in fecal Escherichia coli isolated from poultry chicks in northern Iran. Gene Rep 2020; 21:100926.
17. Dehdashti S, Ghanbarpour R, Hajikolaei MRH. Molecular detection of Shiga toxin–producing and antibiotic-resistant Escherichia coli isolates from buffaloes in southwest of Iran. Trop Anim Health Prod 2019; 51(6):1725-36.
18. Mohammadi V, Ghaniei A, Sepehrnia P. Antimicrobial resistance profile and prevalence of tetracycline resistance genes in Escherichia coli isolates from broiler chickens, Northwestern Iran. Bulg J Vet Med 2018; 21(2):169-75.
19. Ranjbar R, Safarpoor Dehkordi F, Sakhaei Shahreza MH, et al. Prevalence, identification of virulence factors, O-serogroups and antibiotic resistance properties of Shiga-toxin producing Escherichia coli strains isolated from raw milk and traditional dairy products. Antimicrob Resist Infect Control 2018; 7(1):1-11.
20. Boroomand Z, Jafari R, Gharibi D, et al. An investigation into enterobacteriaceae responsible for early mortality in japanese quail chicks and their antibiotic susceptibility patterns. Arch Razi Inst 2018; 73(4):277-85.
21. Bakhshi M, Fatahi Bafghi M, Astani A, et al. Antimicrobial resistance pattern of Escherichia coli isolated from chickens with colibacillosis in Yazd, Iran. J Food Qual Hazards Control 2017; 4(3):74-8.
22. Safavi EA, Shahbazi Y. Antimicrobial resistance in Escherichia coli isolated from different parts of the digestive tract of sheep. Bulg J Vet Med 2017; 20(3):271-5.
23. Chaleshtori FS, Arani NM, Aghadavod E, et al. Molecular characterization of Escherichia coli recovered from traditional milk products in Kashan, Iran. Vet World 2017; 10(10):1264.
24. Hasani B, Banani M, Nouri A, et al. Detection of three virulence genes and antibiotic resistance profiles in Escherichia coli isolates from commercial broilers with colibacillosis in Tabriz, Iran. Arch Razi Inst 2017; 72(1):1-8.
25. Kheiri R, Ranjbar R, Khamesipour F, et al. Role of antibiotic in drug resistance and integrons prevalence in Escherichia coli isolated from human and animal specimens. Mol Microbiol 2016; 1(3).
26. Bonyadian M, Moshtaghi H, Taheri MA, editors. Molecular characterization and antibiotic resistance of enterotoxigenic and entero-aggregative Escherichia coli isolated from raw milk and unpasteurized cheeses. Veterinary Research Forum: an International Quarterly Journal; 2014: Faculty of Veterinary Medicine, Urmia University, Urmia, Iran.
27. Talebiyan R, Kheradmand M, Khamesipour F, et al. Multiple antimicrobial resistance of Escherichia coli isolated from chickens in Iran. Vet Med Int 2014; 32(1):115-23.
28. Abdi-Hachesoo B, Asasi K, Sharifiyazdi H. Farm-level evaluation of enrofloxacin resistance in Escherichia coli isolated from broiler chickens during a rearing period. Comp Clin Path 2017; 26(2):471-6.
29. Rahimi M. Antibioresistance profile of avian pathogenic Escherichia coli isolates recovered from broiler chicken farms with colibacillosis in Kermanshah province, Iran. Glob Vet 2013; 10(4):447-52.
30. Seifi S, Shirzad M. Antimicrobial susceptibility of Escherichia coli isolated from free range poultry or wild birds at the southern Caspian Sea coast of Iran. J Hell Vet Med Soc 2013; 64(4):249-54.
31. Momtaz H, Jamshidi A. Shiga toxin-producing Escherichia coli isolated from chicken meat in Iran: Serogroups, virulence factors, and antimicrobial resistance properties. Poult Sci J 2013; 92(5):1305-13.
32. Rad M, Kooshan M, Mesgarani H. Quinolone resistance among Salmonella enterica and Escherichia coli of animal origin. Comp Clin Path 2012; 21(2):161-5.
33. Momtaz H, Rahimi E, Moshkelani S. Molecular detection of antimicrobial resistance genes in E. coli isolated from slaughtered commercial chickens in Iran. Vet Med 2012; 57(4):193-7.
34. Tabatabaei M, Marashi NF, Mokarizade A. Transferable plasmid mediating multi-antibiotic resistance in non-pathogenic Escherichia coli isolates from chicken flocks. Glob Vet 2010; 5(6):371-5.
35. Emery D, Nagaraja KV, Shaw D, et sl. Virulence factors of Escherichia coli associated with colisepticemia in chickens and turkeys. Avian Dis 1992; 504-11.
36. Hammerum AM, Heuer OE. Human health hazards from antimicrobial-resistant Escherichia coli of animal origin. Clin Infect Dis 2009; 48(7):916-21.
37. Mahmoud Farhan S, Mahmoud Abd El-Baky R, Abdalla M, et al. Efficacy of amikacin and imipenem against multi-drug resistant gram-negative bacteria isolated from wound Infections, Egypt. Iranian Journal of Medical Microbiology 2023; 17(2):218-29.
38. Fortini D, Fashae K, García-Fernández A, et al. Plasmid-mediated quinolone resistance and β-lactamases in Escherichia coli from healthy animals from Nigeria. J Antimicrob Chemother 2011; 66(6):1269-72.
39. Yang T, Zeng Z, Rao L, et al. The association between occurrence of plasmid-mediated quinolone resistance and ciprofloxacin resistance in Escherichia coli isolates of different origins. Vet Microbiol 2014; 170(1-2):89-96.
40. Seo KW, Lee YJ. Characterization of plasmid mediated quinolone resistance determinants in ciprofloxacin resistant-Escherichia coli from chicken meat produced by integrated broiler operations in Korea. Int J Food Microbiol 2019; 307:108274.
41. Van den Bogaard A, London N, Driessen C, et al. Antibiotic resistance of faecal Escherichia coli in poultry, poultry farmers and poultry slaughterers. J Antimicrob Chemother 2001; 47(6):763-71.
42. Fakhraddin Raheem T, Ahmed Hasan Ali S. Prevalence and multi-drug resistance patterns of uropathogenic E. coli isolated from women patients in Kirkuk city, Iraq. Iranian Journal of Medical Microbiology 2022; 16(6):609-14.
43. Gosling R, Clouting C, Randall L, et al. Ciprofloxacin resistance in E. coli isolated from turkeys in Great Britain. Avian Pathol 2012; 41(1):83-9.
| Files | ||
| Issue | Vol 12 No 4 (2024) | |
| Section | Review Articles | |
| Keywords | ||
| Fluoroquinolones Antimicrobial resistance Escherichia coli Animal products Iran | ||
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How to Cite
1.
Ebrahim-Saraie HS, Amini ME, Hasannejad-Bibalan M, Zadgari E, Bakhshi A. The Prevalence of Fluoroquinolone-Resistant E. coli in Animals and Animal Products: A Systematic Review and Meta-Analysis. J Med Bacteriol. 2024;:65-75.
