Antimicrobial Resistance Profiles and Clonal Relationship among Non-ESBL Avian Pathogenic Escherichia coli Isolates and ESBL Producing E. coli Isolates from Human Urinary Tract Infections

  • Bahman ABDI-HACHESOO Department of Clinical Sciences, School of Veterinary Medicine, Shiraz University, Shiraz, Iran
  • Abdollah DERAKHSHANDEH Department of Pathobiology, School of Veterinary Medicine, Shiraz University, Shiraz, Iran
  • Mohammad MOTAMEDIFAR Department of Bacteriology and Virology, Shiraz University of Medical Science, Shiraz, Iran
  • Negar AZIMZADEH Department of Pathobiology, School of Veterinary Medicine, Shiraz University, Shiraz, Iran
Escherichia coli, Beta-lactamases, Avian colibacillosis, Urinary tract infection


Background: We aimed to investigate antimicrobial resistance and clonal relationships among poultry Escherichia coli isolates from different broiler farms and their relationships with Extended-Spectrum Beta-Lactamase (ESBL) producing urinary pathogenic E. coli (UPEC) isolates from the same geographical area.

Methods: Twenty four E. coli isolates from six broiler farms with colibacillosis and 97 ESBL producing human UPEC isolates were investigated for resistance to critically important antimicrobials in human medicine in Shiraz, central Iran in 2015-16. In addition, clonal relationships of these isolates were investigated with Pulse Field Gel Electrophoresis (PFGE).

Results: As expected, cephalosporins and imipenem resistance were significantly higher in ESBL producing human E. coli isolates in comparison with non-ESBL avian pathogenic E. coli (APEC) isolates. In addition, significantly higher percentages of gentamycin and trimethoprim-sulfamethoxazole resistance were seen in human isolates. In contrast, nitrofurantoin resistance was significantly higher in APEC isolates. Based on PFGE patterns, five clusters were identified in APEC isolates. Isolates from each farm were closely related to each other by PFGE patterns. However, different PFGE restriction profiles were seen among the E. coli isolates from different broiler farms. Comparison of PFGE patterns among APEC and UPEC isolates showed two closely related PFGE patterns.

Conclusion: There were clonally related E. coli isolates caused the outbreaks of colibacillosis within broiler farms. Some of these isolates had closely related PFGE patterns with human UPEC isolates which suggest avian pathogenic E. coli strains as a potential zoonosis.


1. Nolan LK, Vaillancourt JP, Nicolle L et al (2013). Colibacillosis. In: Diseases of Poultry. Eds, David E. et al. 14th ed. pp. 751-805. DOI:10.1002/9781119371199.
2. Dierikx C, van der Goot J, Fabri T et al (2013). Extended-spectrum-β-lactamase-and AmpC-β-lactamase-producing Esche-richia coli in Dutch broilers and broiler farmers. J Antimicrob Chemother, 68: 60-67.
3. Pasquali F, Lucchi A, Braggio S et al (2015). Genetic diversity of Escherichia coli isolates of animal and environmental origins from an integrated poultry production chain. Vet Microbiol, 178: 230-237.
4. Newell DG, La Ragione RM (2018). Enter-ohaemorrhagic and other Shiga toxin‐producing Escherichia coli (STEC): Where are we now regarding diagnostics and control strategies?. Transbound Emerg Dis,
5. Karve S, Ryan K, Peeters P et al (2018). The impact of initial antibiotic treatment fail-ure: Real-world insights in patients with complicated urinary tract infection. J Infect, 76: 121-131.
6. Kariyawasam S, Scaccianoce JA, Nolan LK (2007). Common and specific genomic sequences of avian and human extraintes-tinal pathogenic Escherichia coli as deter-mined by genomic subtractive hybridiza-tion. BMC microbiol, 7:81.
7. Moulin-Schouleur M, Répérant M, Laurent S et al (2007). Extraintestinal pathogenic Escherichia coli strains of avian and human origin: link between phylogenetic relation-ships and common virulence patterns. J Clin Microbiol, 45: 3366-3376.
8. Cunha MPV, Saidenberg AB, Moreno AM et al (2017). Pandemic extra-intestinal pathogenic Escherichia coli (ExPEC) clonal group O6-B2-ST73 as a cause of avian colibacillosis in Brazil. PLoS One, 12: e 0178970.
9. Graziani C, Luzzi I, Corrò M et al (2009). Phylogenetic background and virulence genotype of ciprofloxacin-susceptible and ciprofloxacin-resistant Escherichia coli strains of human and avian origin. J Infect Dis, 199: 1209-1217.
10. Johnson JR, Kuskowski MA, Smith K et al (2005). Antimicrobial-resistant and ex-traintestinal pathogenic Escherichia coli in retail foods. J Infect Dis, 191: 1040-1049.
11. Kariuki S, Gilks C, Kimari J et al (1999). Genotype Analysis of Escherichia coli Strains Isolated from Children and Chickens Living in Close Contact. Appl Environ Microbiol, 65: 472-476.
12. Maluta RP, Logue CM, Casas MRT et al (2014). Overlapped sequence types (STs) and serogroups of avian pathogenic (APEC) and human extra-intestinal path-ogenic (ExPEC) Escherichia coli isolated in Brazil. PLoS One, 9: e105016.
13. Vincent C, Boerlin P, Daignault D et al (2010). Food reservoir for Escherichia coli causing urinary tract infections. Emerg In-fect Dis, 16: 88-95.
14. Goering RV (2010). Pulsed field gel electro-phoresis: a review of application and in-terpretation in the molecular epidemiolo-gy of infectious disease. Infect Genet Evol, 10: 866-875.
15. Alevizakos M, Nasioudis D, Mylonakis E (2017). Urinary tract infections caused by ESBL‐producing Enterobacteriaceae in renal transplant recipients: A systematic review and meta‐analysis. Transpl Infect Dis, 19(6).
16. Flokas M. E, Detsis M, Alevizakos M, My-lonakis E (2016). Prevalence of ESBL-producing Enterobacteriaceae in paediat-ric urinary tract infections: A systematic review and meta-analysis. J Infect, 73: 547-557.
17. Saliu EM, Vahjen W, Zentek J (2017). Types and prevalence of extended–spectrum beta–lactamase producing Enterobacteri-aceae in poultry. Anim Health Res Rev, 18: 46-57.
18. Manges AR (2016). Escherichia coli and uri-nary tract infections: the role of poultry-meat. Clin Microbiol Infect, 22: 122-129.
19. Markey B, Leonard F, Archambault M et al (2013). Clinical Veterinary Microbiology. E-Book, Elsevier Health Sciences.
20. Clinical and Laboratory Standards Institute. Performance standards for antibiotic sus-ceptibility testing: twenty-fifth informa-tional supplement (2015). CLSI, Wayne, Pennsylvania.
21. Turnidge JD (2015). Susceptibility test meth-ods: general considerations. In: Manual of Clinical Microbiology, Eleventh Edition. American Society of Microbiology, pp. 1246-1252.
22. Centers for Disease Control and Prevention (2013). Standard Operating Procedure for PulseNet PFGE of Escherichia coli O157:H7, Escherichia coli non-O157 (STEC), Salmonella serotypes, Shigella sonnei and Shigella flexneri.
23. Abdi-Hachesoo B, Asasi K, Sharifiyazdi H (2017). Farm-level evaluation of enroflox-acin resistance in Escherichia coli isolated from broiler chickens during a rearing period. Comp Clin Path, 26: 471-476.
24. Hricová K, Röderová M, Pudová V et al (2017). Quinolone-resistant Escherichia coli in poultry farming. Cent Eur J Public Health, 25: 163-167.
25. Thorsteinsdottir TR, Haraldsson G, Fridriksdottir V et al (2010). Broiler chick-ens as source of human fluoroquinolone-resistant Escherichia coli, Iceland. Emerg Infect Dis, 16: 133-135.
26. Aalipour F, Mirlohi M, Jalali M (2014). De-termination of antibiotic consumption index for animal originated foods pro-duced in animal husbandry in Iran, 2010. J Environ Health Sci Eng, 12(1):42.
27. Faghihi SM, Rassouli A, Marandi MV (2017). A survey on antibacterial drug use in broiler chicken farms in Qum prov-ince, Iran. J Vet Res, 72: 1-6.
28. Bebora LC, Oundo JO, Yamamoto H (1994). Resistance of E. coli strains, recov-ered from chickens to antibiotics with particular reference to trimethoprim-sulfamethoxazole (septrin). East Afr Med J, 71: 624-627.
29. Ho PL, Wong RC, Chow KH, Que TL (2009). Distribution of integron‐associated trimethoprim–sulfamethoxazole resistance determinants among Escherichia coli from humans and food‐producing animals. Lett Appl Microbiol, 49: 627-634.
30. Mund MD, Khan UH, Tahir U et al (2017). Antimicrobial drug residues in poultry products and implications on public health: A review. Int J Food Prop, 20: 1433-1446.
31. Munoz-Davila MJ (2014). Role of old anti-biotics in the era of antibiotic resistance. Highlighted nitrofurantoin for the treat-ment of lower urinary tract infections. Antibiotics (Basel), 3: 39-48.
32. Saberfar E, Pourakbari B, Chabokdavan K, Dolatshahi FT (2008). Antimicrobial Sus-ceptibility of Escherichia coli Isolated from Iranian Broiler Chicken Flocks, 2005–2006. J Appl Poult Res, 17: 302-304.
33. Bagheri M, Ghanbarpour R, Alizade H (2014). Shiga toxin and beta-lactamases genes in Escherichia coli phylotypes isolated from carcasses of broiler chickens slaughtered in Iran. Int J Food Microbiol, 177: 16-20.
34. Doregiraee F, Alebouyeh M, Nayeri Fasaei B et al (2017). Changes in antimicrobial re-sistance patterns and dominance of ex-tended spectrum β-lactamase genes among faecal Escherichia coli isolates from broilers and workers during two rearing periods. Ital J Anim Sci, 17(3):815-824.
35. Leverstein‐van Hall MA, Dierikx CM, Co-hen Stuart J et al (2011). Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. Clin Microbiol Infect, 17: 873-880.
36. Norizuki C, Wachino JI, Suzuki M et al (2017). Specific blaCTX-M-8/IncI1 Plasmid Transfer among Genetically Di-verse Escherichia coli Isolates between Humans and Chickens. Antimicrob Agents Chemother, 24;61(6).
37. Ozawa M, Harada K, Kojima A et al (2008). Antimicrobial susceptibilities, serogroups, and molecular characterization of avian pathogenic Escherichia coli isolates in Japan. Avian Dis, 52: 392-397.
38. Poulsen LL, Thøfner I, Bisgaard M et al (2017). Longitudinal study of transmis-sion of Escherichia coli from broiler breed-ers to broilers. Vet Microbiol, 207: 13-18.
39. Solà-Ginés M, Cameron-Veas K, Badiola I et al (2015). Diversity of multi-drug re-sistant Avian Pathogenic Escherichia coli (APEC) causing outbreaks of colibacillo-sis in broilers during 2012 in Spain. PloS One, 10: e0143191.
40. Li J, Ma Y, Hu C, Jin S et al (2010). Dissem-ination of cefotaxime-M-producing Esche-richia coli isolates in poultry farms, but not swine farms, in China. Foodborne Pathog Dis, 7: 1387-1392.
41. Johnson JR, Kuskowski MA, Menard M et al (2006). Similarity between human and chicken Escherichia coli isolates in relation to ciprofloxacin resistance status. J Infect Dis, 194: 71-78.
42. Overdevest I, Willemsen I, Rijnsburger M et al (2011). Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, The Netherlands. Emerg In-fect Dis, 17: 1216-1222.
43. Giufre M, Graziani C, Accogli M et al (2012). Escherichia coli of human and avian origin: detection of clonal groups associated with fluoroquinolone and mul-tidrug resistance in Italy. ‎J Antimicrob Chemother, 67(4): 860-867.
44. Jakobsen L, Garneau P, Bruant G et al (2012). Is Escherichia coli urinary tract infec-tion a zoonosis? Proof of direct link with production animals and meat. Eur J Clin Microbiol Infect Dis, 31(6): 1121-1129.
How to Cite
ABDI-HACHESOO B, DERAKHSHANDEH A, MOTAMEDIFAR M, AZIMZADEH N. Antimicrobial Resistance Profiles and Clonal Relationship among Non-ESBL Avian Pathogenic Escherichia coli Isolates and ESBL Producing E. coli Isolates from Human Urinary Tract Infections. Iran J Public Health. 49(3):530-538.
Original Article(s)