Molecular epidemiology of antibiotic-resistant Escherichia coli among clinical samples isolated in Azerbaijan, Iran
-
Reza Ghotaslou
,
Shabnam Baghbani
,
Pardis Ghotaslou
,
Solmaz Mirmahdavi
,
Hamed Ebrahimzadeh Leylabadlo
Abstract
Background and Objectives: The immediate emergence of resistant bacteria poses an increasingly growing problem to human society and the increasing prevalence of antibiotic resistance in Escherichia coli strains is one of the most important health problems. This study aimed to review the molecular epidemiology of drug resistance among clinical isolates of E. coli in north-west portion of Iran Azerbaijan.
Materials and Methods: A complete of 219 clinical isolates of E. coli had been collected from the various clinical samples. The disk diffusion and agar dilution assays were used to determine antimicrobial susceptibility. The presence of antibiotics resistance genes was carried out by the PCR method.
Results: The highest susceptibility was shown to imipenem (3%) and fosfomycin (3%), and the most antibiotic resistance was presented to ampicillin (99%). The highest frequent ESBL gene among isolates was blaCTXM-15 in 70% followed by blaCMY-2 in 67%, and blaTEM-1 in 46%. The most common fluoroquinolone (FQ) resistance genes were oqxB (34%), followed by oqxA (25%), and qnrB (18%). The frequency of tetracycline resistance genes (tetA, tetB, tetC, and tetD) were detected in 24.8%, 31.6%, 1.8%, and 4.2%, respectively. The highest frequent genes to fosfomycin were fosA 10%, fosA3 30%, fosC 40%, and fosX 20%. The dominant founded aminoglycosides resistant genes were armA (12.96%) and npmA (4.93%).
Conclusion: The prevalence of antibiotics resistance in the tested E. coli isolates was high in Azerbaijan, Iran and these findings showed that E. coli is one of the major drug-resistant pathogens.
1. Martinson JN, Walk ST. Escherichia coli residency in the gut of healthy human adults. EcoSal Plus 2020; 9: 10.1128/ecosalplus.ESP-0003-2020.
2. Manges AR, Geum HM, Guo A, Edens TJ, Fibke CD, Pitout JD. Global extraintestinal pathogenic Escherichia coli (ExPEC) lineages. Clin Microbiol Rev 2019; 32(3): e00135-18.
3. Kaye KS, Pogue JM. Infections caused by resistant gram‐negative bacteria: epidemiology and management. Pharmacotherapy 2015; 35: 949-962.
4. Etemadi S, Leylabadlo HE, Ghotaslou R. AmpC β-lactamase among Enterobacteriaceae: a new insight. Gene Rep 2020; 19: 100673.
5. Leylabadlo HE, Kafil HS, Yousefi M, Aghazadeh M, Asgharzadeh M. Persistent infection with metallo-beta-lactamase and extended spectrum β-lactamase producer Morganella morganii in a patient with urinary tract infection after kidney transplantation. J Nat Sci Biol Med 2016; 7: 179-181.
6. Azargun R, Sadeghi V, Leylabadlo HE, Alizadeh N, Ghotaslou R. Molecular mechanisms of fluoroquinolone resistance in Enterobacteriaceae clinical isolates in Azerbaijan, Iran. Gene Rep 2020; 21: 100924.
7. Guan X, He L, Hu B, Hu J, Huang X, Lai G, et al. Laboratory diagnosis, clinical management and infection control of the infections caused by extensively drug-resistant Gram-negative bacilli: a Chinese consensus statement. Clin Microbiol Infect 2016; 22 Suppl 1: S15-25.
8. Reygaert WC. An overview of the antimicrobial resistance mechanisms of bacteria. AIMS Microbiol 2018; 4: 482-501.
9. Eichenberger EM, Thaden JT. Epidemiology and mechanisms of resistance of extensively drug resistant Gram-negative bacteria. Antibiotics (Basel) 2019; 8: 37.
10. Pitout JD. Extraintestinal pathogenic Escherichia coli: a combination of virulence with antibiotic resistance. Front Microbiol 2012; 3: 9.
11. Krueger WA, Lenhart F-P, Neeser G, Ruckdeschel G, Schreckhase H, Eissner H-J, et al. Influence of combined intravenous and topical antibiotic prophylaxis on the incidence of infections, organ dysfunctions, and mortality in critically ill surgical patients: a prospective, stratified, randomized, double-blind, placebo-controlled clinical trial. Am J Respir Crit Care Med 2002; 166: 1029-1037.
12. Slama TG. Gram-negative antibiotic resistance: there is a price to pay. Crit Care 2008; 12 Suppl 4(Suppl 4): S4.
13. Liang C, Zhang X, Zhou L, Meng G, Zhong L, Peng P. Trends and correlation between antibacterial consumption and carbapenem resistance in gram-negative bacteria in a tertiary hospital in China from 2012 to 2019. BMC Infect Dis 2021; 21: 444.
14. Azad MAR, Rahman MM, Amin R, Begum MIA, Fries R, Husna A, et al. Susceptibility and multidrug resistance patterns of Escherichia coli isolated from cloacal swabs of live broiler chickens in Bangladesh. Pathogens 2019; 8: 118.
15. CLSI. Performance standards for antimicrobial susceptibility testing. CLSI 2016.
16. Kuti JL, Pettit RS, Neu N, Cies JJ, Lapin C, Muhlebach MS, et al. Microbiological activity of ceftolozane/tazobactam, ceftazidime, meropenem, and piperacillin/tazobactam against Pseudomonas aeruginosa isolated from children with cystic fibrosis. Diagn Microbiol Infect Dis 2015; 83: 53-55.
17. Akhi MT, Khalili Y, Ghotaslou R, Kafil HS, Yousefi S, Nagili B, et al. Carbapenem inactivation: a very affordable and highly specific method for phenotypic detection of carbapenemase-producing Pseudomonas aeruginosa isolates compared with other methods. J Chemother 2017; 29: 144-149.
18. Zahra R, Javeed S, Malala B, Babenko D, Toleman MA. Analysis of Escherichia coli STs and resistance mechanisms in sewage from Islamabad, Pakistan indicates a difference in E. coli carriage types between South Asia and Europe. J Antimicrob Chemother 2018; 73: 1781-1785.
19. Chen X, Zhang W, Pan W, Yin J, Pan Z, Gao S, et al. Prevalence of qnr, aac (6′)-Ib-cr, qepA, and oqxAB in Escherichia coli isolates from humans, animals, and the environment. Antimicrob Agents Chemother 2012; 56: 3423-3427.
20. Aminov R, Chee-Sanford J, Garrigues N, Teferedegne B, Krapac I, White B, et al. Development, validation, and application of PCR primers for detection of tetracycline efflux genes of gram-negative bacteria. Appl Environ Microbiol 2002; 68: 1786-1793.
21. Gündoğdu A, Long YB, Vollmerhausen TL, Katouli M. Antimicrobial resistance and distribution of sul genes and integron-associated intI genes among uropathogenic Escherichia coli in Queensland, Australia. J Med Microbiol 2011; 60: 1633-1642.
22. Ghotaslou R, Yeganeh Sefidan F, Akhi MT, Asgharzadeh M, Mohammadzadeh Asl Y. Dissemination of genes encoding aminoglycoside-modifying enzymes and armA among Enterobacteriaceae isolates in Northwest Iran. Microb Drug Resist 2017; 23: 826-832.
23. Kerrn M, Klemmensen T, Frimodt-Møller N, Espersen F. Susceptibility of Danish Escherichia coli strains isolated from urinary tract infections and bacteraemia, and distribution of sul genes conferring sulphonamide resistance. J Antimicrob Chemother 2002; 50: 513-516.
24. Voets GM, Fluit AC, Scharringa J, Cohen Stuart J, Leverstein-van Hall MA. A set of multiplex PCRs for genotypic detection of extended-spectrum β-lactamases, carbapenemases, plasmid-mediated AmpC β-lactamases and OXA β-lactamases. Int J Antimicrob Agents 2011; 37: 356-359.
25. Dallenne C, Da Costa A, Decré D, Favier C, Arlet G. Development of a set of multiplex PCR assays for the detection of genes encoding important β-lactamases in Enterobacteriaceae. J Antimicrob Chemother 2010; 65: 490-495.
26. Pirouzi A, Foruozandeh H, Farahani A, Shamseddin J, Mohseni H, Abdollahi A, et al. Investigation of antimicrobial resistance pattern among Escherichia coli strains isolated from patients referred to Amir Al-Momenin Hospital, Gerash, Iran. Gene Cell Tissue 2019; 7(1): e97554.
27. Mansouri S, Neyestanaki DK, Shokoohi M, Halimi S, Beigverdi R, Rezagholezadeh F, et al. Characterization of AmpC, CTX-M and MBLs types of β-lactamases in clinical isolates of Klebsiella pneumoniae and Escherichia coli producing extended spectrum β-lactamases in Kerman, Iran. Jundishapur J Microbiol 2014; 7(2): e8756.
28. Arabi H, Pakzad I, Nasrollahi A, Hosainzadegan H, Jalilian FA, Taherikalani M, et al. Sulfonamide resistance genes (sul) M in extended spectrum beta lactamase (ESBL) and non-ESBL producing Escherichia coli isolated from Iranian hospitals. Jundishapur J Microbiol 2015; 8(7): e19961.
29. Pouladfar G, Basiratnia M, Anvarinejad M, Abbasi P, Amirmoezi F, Zare S. The antibiotic susceptibility patterns of uropathogens among children with urinary tract infection in Shiraz. Medicine (Baltimore) 2017; 96(37): e7834.
30. Soleimani N, Aganj M, Ali L, Shokoohizadeh L, Sakinc T. Frequency distribution of genes encoding aminoglycoside modifying enzymes in uropathogenic E. coli isolated from Iranian hospital. BMC Res Notes 2014; 7: 842.
31. Sohail M, Khurshid M, Saleem HGM, Javed H, Khan AA. Characteristics and antibiotic resistance of urinary tract pathogens isolated from Punjab, Pakistan. Jundishapur J Microbiol 2015; 8(7): e19272.
32. Abdi S, Ranjbar R, Vala MH, Jonaidi N, Bejestany OB, Bejestany FB. Frequency of blaTEM, blaSHV, blaCTX-M, and qnrA among Escherichia coli isolated from urinary tract infection. Arch Clin Infect Dis 2014; 9(1): e18690.
33. Leylabadlo HE, Pourlak T, Bialvaei AZ, Aghazadeh M, Asgharzadeh M, Kafil HS. Extended-spectrum beta-lactamase producing gram negative bacteria In Iran: A review. Afr J Infect Dis 2017; 11: 39-53.
34. Bajaj P, Singh NS, Kanaujia PK, Virdi JS. Distribution and molecular characterization of genes encoding CTX-M and AmpC β-lactamases in Escherichia coli isolated from an Indian urban aquatic environment. Sci Total Environ 2015; 505: 350-356.
35. Rezai MS, Salehifar E, Rafiei A, Langaee T, Rafati M, Shafahi K, et al. Characterization of multidrug resistant extended-spectrum beta-lactamase-producing Escherichia coli among uropathogens of pediatrics in North of Iran. Biomed Res Int 2015; 2015: 309478.
36. Grossman TH. Tetracycline antibiotics and resistance. Cold Spring Harb Perspect Med 2016; 6: 025387.
37. Sheykhsaran E, Bannazadeh Baghi H, Soroush Barhaghi MH, Alizadeh N, Memar MY, Etemadi S, et al. The rate of resistance to tetracyclines and distribution of tetA, tetB, tetC, tetD, tetE, tetG, tetJ and tetY genes in Enterobacteriaceae isolated from Azerbaijan, Iran during 2017. Physiol Pharmacol 2018; 22: 205-212.
38. Loras C, Mendes AC, Peixe L, Novais Â, Alós J-I. Escherichia coli resistant to fosfomycin from urinary tract infections: detection of the fosA3 gene in Spain. J Glob Antimicrob Resist 2020; 21: 414-416.
39. Malekpour Kolbadinezhad S, Fozouni L. Molecular monitoring of Fosfomycin resistance in Escherichia coli strains isolated from patients with urinary catheters in north-east of Iran. JoMMID 2018; 6: 112-117.
40. Zaniani FR, Savari M, Montazeri EA, Nejad RM, Khoshnood S. Distribution of fosfomycin and AmpC β-lactamase resistance genes in urinary Escherichia coli isolates obtained from patients admitted to an educational hospital in Ahvaz, southwest Iran. Gene Rep 2019; 17: 100533.
41. Lalehzadeh A, Soroush MH, Sadeghi J, Ahangarzadeh Rezaee M, Pirzadeh T, Yeganeh Sefidan F, et al. Determination of fosfomycin resistant enterobacteriaceae in isolates and frequency of fos genes in Tabriz Hospitals during 2018. J Biochem Tech 2019; 2: 143-148.
42. Azargun R, Soroush Barhaghi MH, Samadi Kafil H, Ahangar Oskouee M, Sadeghi V, Memar MY, et al. Frequency of DNA gyrase and topoisomerase IV mutations and plasmid-mediated quinolone resistance genes among Escherichia coli and Klebsiella pneumoniae isolated from urinary tract infections in Azerbaijan, Iran. J Glob Antimicrob Resist 2019; 17: 39-43.
43. Mirzaii M, Jamshidi S, Zamanzadeh M, Marashifard M, Hosseini SAAM, Haeili M, et al. Determination of gyrA and parC mutations and prevalence of plasmid-mediated quinolone resistance genes in Escherichia coli and Klebsiella pneumoniae isolated from patients with urinary tract infection in Iran. J Glob Antimicrob Resist 2018; 13: 197-200.
44. Varughese LR, Rajpoot M, Goyal S, Mehra R, Chhokar V, Beniwal V. Analytical profiling of mutations in quinolone resistance determining region of gyrA gene among UPEC. PLoS One 2018; 13(1): e0190729.
45. El-Mahdy RH, Saleh MA, Aboelnour A. GyrA mutations in nosocomial ciprofloxacin-resistant Escherichia coli isolates associated with urinary tract infections. Int J Curr Microbiol App Sci 2017; 6: 1902-1907.
46. Yuan J, Xu X, Guo Q, Zhao X, Ye X, Guo Y, et al. Prevalence of the oqxAB gene complex in Klebsiella pneumoniae and Escherichia coli clinical isolates. J Antimicrob Chemother 2012; 67: 1655-1659.
47. Kim HB, Wang M, Park CH, Kim E-C, Jacoby GA, Hooper DC. oqxAB encoding a multidrug efflux pump in human clinical isolates of Enterobacteriaceae. Antimicrob Agents Chemother 2009; 53: 3582-3584.
48. Benaicha H, Barrijal S, Ezzakkioui F, Elmalki F. Prevalence of PMQR genes in E. coli and Klebsiella spp. isolated from North-West of Morocco. J Glob Antimicrob Resist 2017; 10: 321-325.
49. Wu Q, Zhang Y, Han L, Sun J, Ni Y. Plasmid-mediated 16S rRNA methylases in aminoglycoside-resistant Enterobacteriaceae isolates in Shanghai, China. Antimicrob Agents Chemother 2009; 53: 271-272.
50. Bogaerts P, Galimand M, Bauraing C, Deplano A, Vanhoof R, De Mendonca R, et al. Emergence of ArmA and RmtB aminoglycoside resistance 16S rRNA methylases in Belgium. J Antimicrob Chemother 2007; 59: 459-464.
51. Berçot B, Poirel L, Nordmann P. Plasmid-mediated 16S rRNA methylases among extended-spectrum β-lactamase-producing Enterobacteriaceae isolates. Antimicrob Agents Chemother 2008; 52: 4526-4527.
52. Yang J, Ye L, Wang W, Luo Y, Zhang Y, Han L. Diverse prevalence of 16S rRNA methylase genes armA and rmtB amongst clinical multidrug-resistant Escherichia coli and Klebsiella pneumoniae isolates. Int J Antimicrob Agents 2011; 38: 348-351.
53. Rezaei-Tavirani M, Ghafourian S, Sayehmiri F, Pakzad R, Safiri S, Pakzad I. Prevalence of cotrimoxazole resistance uropathogenic bacteria in Iran: a systematic review and meta-analysis. Arch Clin Infect Dis 2018;13(5): e63256.
54. Japoni A, Gudarzi M, Farshad S, Basiri E, Ziyaeyan M, Alborzi A, et al. Assay for integrons and pattern of antibiotic resistance in clinical Escherichia coli strains by PCR-RFLP in Southern Iran. Jpn J Infect Dis 2008;61: 85-88.
55. Kozak GK, Pearl DL, Parkman J, Reid-Smith RJ, Deckert A, Boerlin P. Distribution of sulfonamide resistance genes in Escherichia coli and Salmonella isolates from swine and chickens at abattoirs in Ontario and Quebec, Canada. Appl Environ Microbiol 2009; 75: 5999-6001.
56. Bean DC, Livermore DM, Hall LM. Plasmids imparting sulfonamide resistance in Escherichia coli: implications for persistence. Antimicrob Agents Chemother 2009; 53: 1088-1093.
2. Manges AR, Geum HM, Guo A, Edens TJ, Fibke CD, Pitout JD. Global extraintestinal pathogenic Escherichia coli (ExPEC) lineages. Clin Microbiol Rev 2019; 32(3): e00135-18.
3. Kaye KS, Pogue JM. Infections caused by resistant gram‐negative bacteria: epidemiology and management. Pharmacotherapy 2015; 35: 949-962.
4. Etemadi S, Leylabadlo HE, Ghotaslou R. AmpC β-lactamase among Enterobacteriaceae: a new insight. Gene Rep 2020; 19: 100673.
5. Leylabadlo HE, Kafil HS, Yousefi M, Aghazadeh M, Asgharzadeh M. Persistent infection with metallo-beta-lactamase and extended spectrum β-lactamase producer Morganella morganii in a patient with urinary tract infection after kidney transplantation. J Nat Sci Biol Med 2016; 7: 179-181.
6. Azargun R, Sadeghi V, Leylabadlo HE, Alizadeh N, Ghotaslou R. Molecular mechanisms of fluoroquinolone resistance in Enterobacteriaceae clinical isolates in Azerbaijan, Iran. Gene Rep 2020; 21: 100924.
7. Guan X, He L, Hu B, Hu J, Huang X, Lai G, et al. Laboratory diagnosis, clinical management and infection control of the infections caused by extensively drug-resistant Gram-negative bacilli: a Chinese consensus statement. Clin Microbiol Infect 2016; 22 Suppl 1: S15-25.
8. Reygaert WC. An overview of the antimicrobial resistance mechanisms of bacteria. AIMS Microbiol 2018; 4: 482-501.
9. Eichenberger EM, Thaden JT. Epidemiology and mechanisms of resistance of extensively drug resistant Gram-negative bacteria. Antibiotics (Basel) 2019; 8: 37.
10. Pitout JD. Extraintestinal pathogenic Escherichia coli: a combination of virulence with antibiotic resistance. Front Microbiol 2012; 3: 9.
11. Krueger WA, Lenhart F-P, Neeser G, Ruckdeschel G, Schreckhase H, Eissner H-J, et al. Influence of combined intravenous and topical antibiotic prophylaxis on the incidence of infections, organ dysfunctions, and mortality in critically ill surgical patients: a prospective, stratified, randomized, double-blind, placebo-controlled clinical trial. Am J Respir Crit Care Med 2002; 166: 1029-1037.
12. Slama TG. Gram-negative antibiotic resistance: there is a price to pay. Crit Care 2008; 12 Suppl 4(Suppl 4): S4.
13. Liang C, Zhang X, Zhou L, Meng G, Zhong L, Peng P. Trends and correlation between antibacterial consumption and carbapenem resistance in gram-negative bacteria in a tertiary hospital in China from 2012 to 2019. BMC Infect Dis 2021; 21: 444.
14. Azad MAR, Rahman MM, Amin R, Begum MIA, Fries R, Husna A, et al. Susceptibility and multidrug resistance patterns of Escherichia coli isolated from cloacal swabs of live broiler chickens in Bangladesh. Pathogens 2019; 8: 118.
15. CLSI. Performance standards for antimicrobial susceptibility testing. CLSI 2016.
16. Kuti JL, Pettit RS, Neu N, Cies JJ, Lapin C, Muhlebach MS, et al. Microbiological activity of ceftolozane/tazobactam, ceftazidime, meropenem, and piperacillin/tazobactam against Pseudomonas aeruginosa isolated from children with cystic fibrosis. Diagn Microbiol Infect Dis 2015; 83: 53-55.
17. Akhi MT, Khalili Y, Ghotaslou R, Kafil HS, Yousefi S, Nagili B, et al. Carbapenem inactivation: a very affordable and highly specific method for phenotypic detection of carbapenemase-producing Pseudomonas aeruginosa isolates compared with other methods. J Chemother 2017; 29: 144-149.
18. Zahra R, Javeed S, Malala B, Babenko D, Toleman MA. Analysis of Escherichia coli STs and resistance mechanisms in sewage from Islamabad, Pakistan indicates a difference in E. coli carriage types between South Asia and Europe. J Antimicrob Chemother 2018; 73: 1781-1785.
19. Chen X, Zhang W, Pan W, Yin J, Pan Z, Gao S, et al. Prevalence of qnr, aac (6′)-Ib-cr, qepA, and oqxAB in Escherichia coli isolates from humans, animals, and the environment. Antimicrob Agents Chemother 2012; 56: 3423-3427.
20. Aminov R, Chee-Sanford J, Garrigues N, Teferedegne B, Krapac I, White B, et al. Development, validation, and application of PCR primers for detection of tetracycline efflux genes of gram-negative bacteria. Appl Environ Microbiol 2002; 68: 1786-1793.
21. Gündoğdu A, Long YB, Vollmerhausen TL, Katouli M. Antimicrobial resistance and distribution of sul genes and integron-associated intI genes among uropathogenic Escherichia coli in Queensland, Australia. J Med Microbiol 2011; 60: 1633-1642.
22. Ghotaslou R, Yeganeh Sefidan F, Akhi MT, Asgharzadeh M, Mohammadzadeh Asl Y. Dissemination of genes encoding aminoglycoside-modifying enzymes and armA among Enterobacteriaceae isolates in Northwest Iran. Microb Drug Resist 2017; 23: 826-832.
23. Kerrn M, Klemmensen T, Frimodt-Møller N, Espersen F. Susceptibility of Danish Escherichia coli strains isolated from urinary tract infections and bacteraemia, and distribution of sul genes conferring sulphonamide resistance. J Antimicrob Chemother 2002; 50: 513-516.
24. Voets GM, Fluit AC, Scharringa J, Cohen Stuart J, Leverstein-van Hall MA. A set of multiplex PCRs for genotypic detection of extended-spectrum β-lactamases, carbapenemases, plasmid-mediated AmpC β-lactamases and OXA β-lactamases. Int J Antimicrob Agents 2011; 37: 356-359.
25. Dallenne C, Da Costa A, Decré D, Favier C, Arlet G. Development of a set of multiplex PCR assays for the detection of genes encoding important β-lactamases in Enterobacteriaceae. J Antimicrob Chemother 2010; 65: 490-495.
26. Pirouzi A, Foruozandeh H, Farahani A, Shamseddin J, Mohseni H, Abdollahi A, et al. Investigation of antimicrobial resistance pattern among Escherichia coli strains isolated from patients referred to Amir Al-Momenin Hospital, Gerash, Iran. Gene Cell Tissue 2019; 7(1): e97554.
27. Mansouri S, Neyestanaki DK, Shokoohi M, Halimi S, Beigverdi R, Rezagholezadeh F, et al. Characterization of AmpC, CTX-M and MBLs types of β-lactamases in clinical isolates of Klebsiella pneumoniae and Escherichia coli producing extended spectrum β-lactamases in Kerman, Iran. Jundishapur J Microbiol 2014; 7(2): e8756.
28. Arabi H, Pakzad I, Nasrollahi A, Hosainzadegan H, Jalilian FA, Taherikalani M, et al. Sulfonamide resistance genes (sul) M in extended spectrum beta lactamase (ESBL) and non-ESBL producing Escherichia coli isolated from Iranian hospitals. Jundishapur J Microbiol 2015; 8(7): e19961.
29. Pouladfar G, Basiratnia M, Anvarinejad M, Abbasi P, Amirmoezi F, Zare S. The antibiotic susceptibility patterns of uropathogens among children with urinary tract infection in Shiraz. Medicine (Baltimore) 2017; 96(37): e7834.
30. Soleimani N, Aganj M, Ali L, Shokoohizadeh L, Sakinc T. Frequency distribution of genes encoding aminoglycoside modifying enzymes in uropathogenic E. coli isolated from Iranian hospital. BMC Res Notes 2014; 7: 842.
31. Sohail M, Khurshid M, Saleem HGM, Javed H, Khan AA. Characteristics and antibiotic resistance of urinary tract pathogens isolated from Punjab, Pakistan. Jundishapur J Microbiol 2015; 8(7): e19272.
32. Abdi S, Ranjbar R, Vala MH, Jonaidi N, Bejestany OB, Bejestany FB. Frequency of blaTEM, blaSHV, blaCTX-M, and qnrA among Escherichia coli isolated from urinary tract infection. Arch Clin Infect Dis 2014; 9(1): e18690.
33. Leylabadlo HE, Pourlak T, Bialvaei AZ, Aghazadeh M, Asgharzadeh M, Kafil HS. Extended-spectrum beta-lactamase producing gram negative bacteria In Iran: A review. Afr J Infect Dis 2017; 11: 39-53.
34. Bajaj P, Singh NS, Kanaujia PK, Virdi JS. Distribution and molecular characterization of genes encoding CTX-M and AmpC β-lactamases in Escherichia coli isolated from an Indian urban aquatic environment. Sci Total Environ 2015; 505: 350-356.
35. Rezai MS, Salehifar E, Rafiei A, Langaee T, Rafati M, Shafahi K, et al. Characterization of multidrug resistant extended-spectrum beta-lactamase-producing Escherichia coli among uropathogens of pediatrics in North of Iran. Biomed Res Int 2015; 2015: 309478.
36. Grossman TH. Tetracycline antibiotics and resistance. Cold Spring Harb Perspect Med 2016; 6: 025387.
37. Sheykhsaran E, Bannazadeh Baghi H, Soroush Barhaghi MH, Alizadeh N, Memar MY, Etemadi S, et al. The rate of resistance to tetracyclines and distribution of tetA, tetB, tetC, tetD, tetE, tetG, tetJ and tetY genes in Enterobacteriaceae isolated from Azerbaijan, Iran during 2017. Physiol Pharmacol 2018; 22: 205-212.
38. Loras C, Mendes AC, Peixe L, Novais Â, Alós J-I. Escherichia coli resistant to fosfomycin from urinary tract infections: detection of the fosA3 gene in Spain. J Glob Antimicrob Resist 2020; 21: 414-416.
39. Malekpour Kolbadinezhad S, Fozouni L. Molecular monitoring of Fosfomycin resistance in Escherichia coli strains isolated from patients with urinary catheters in north-east of Iran. JoMMID 2018; 6: 112-117.
40. Zaniani FR, Savari M, Montazeri EA, Nejad RM, Khoshnood S. Distribution of fosfomycin and AmpC β-lactamase resistance genes in urinary Escherichia coli isolates obtained from patients admitted to an educational hospital in Ahvaz, southwest Iran. Gene Rep 2019; 17: 100533.
41. Lalehzadeh A, Soroush MH, Sadeghi J, Ahangarzadeh Rezaee M, Pirzadeh T, Yeganeh Sefidan F, et al. Determination of fosfomycin resistant enterobacteriaceae in isolates and frequency of fos genes in Tabriz Hospitals during 2018. J Biochem Tech 2019; 2: 143-148.
42. Azargun R, Soroush Barhaghi MH, Samadi Kafil H, Ahangar Oskouee M, Sadeghi V, Memar MY, et al. Frequency of DNA gyrase and topoisomerase IV mutations and plasmid-mediated quinolone resistance genes among Escherichia coli and Klebsiella pneumoniae isolated from urinary tract infections in Azerbaijan, Iran. J Glob Antimicrob Resist 2019; 17: 39-43.
43. Mirzaii M, Jamshidi S, Zamanzadeh M, Marashifard M, Hosseini SAAM, Haeili M, et al. Determination of gyrA and parC mutations and prevalence of plasmid-mediated quinolone resistance genes in Escherichia coli and Klebsiella pneumoniae isolated from patients with urinary tract infection in Iran. J Glob Antimicrob Resist 2018; 13: 197-200.
44. Varughese LR, Rajpoot M, Goyal S, Mehra R, Chhokar V, Beniwal V. Analytical profiling of mutations in quinolone resistance determining region of gyrA gene among UPEC. PLoS One 2018; 13(1): e0190729.
45. El-Mahdy RH, Saleh MA, Aboelnour A. GyrA mutations in nosocomial ciprofloxacin-resistant Escherichia coli isolates associated with urinary tract infections. Int J Curr Microbiol App Sci 2017; 6: 1902-1907.
46. Yuan J, Xu X, Guo Q, Zhao X, Ye X, Guo Y, et al. Prevalence of the oqxAB gene complex in Klebsiella pneumoniae and Escherichia coli clinical isolates. J Antimicrob Chemother 2012; 67: 1655-1659.
47. Kim HB, Wang M, Park CH, Kim E-C, Jacoby GA, Hooper DC. oqxAB encoding a multidrug efflux pump in human clinical isolates of Enterobacteriaceae. Antimicrob Agents Chemother 2009; 53: 3582-3584.
48. Benaicha H, Barrijal S, Ezzakkioui F, Elmalki F. Prevalence of PMQR genes in E. coli and Klebsiella spp. isolated from North-West of Morocco. J Glob Antimicrob Resist 2017; 10: 321-325.
49. Wu Q, Zhang Y, Han L, Sun J, Ni Y. Plasmid-mediated 16S rRNA methylases in aminoglycoside-resistant Enterobacteriaceae isolates in Shanghai, China. Antimicrob Agents Chemother 2009; 53: 271-272.
50. Bogaerts P, Galimand M, Bauraing C, Deplano A, Vanhoof R, De Mendonca R, et al. Emergence of ArmA and RmtB aminoglycoside resistance 16S rRNA methylases in Belgium. J Antimicrob Chemother 2007; 59: 459-464.
51. Berçot B, Poirel L, Nordmann P. Plasmid-mediated 16S rRNA methylases among extended-spectrum β-lactamase-producing Enterobacteriaceae isolates. Antimicrob Agents Chemother 2008; 52: 4526-4527.
52. Yang J, Ye L, Wang W, Luo Y, Zhang Y, Han L. Diverse prevalence of 16S rRNA methylase genes armA and rmtB amongst clinical multidrug-resistant Escherichia coli and Klebsiella pneumoniae isolates. Int J Antimicrob Agents 2011; 38: 348-351.
53. Rezaei-Tavirani M, Ghafourian S, Sayehmiri F, Pakzad R, Safiri S, Pakzad I. Prevalence of cotrimoxazole resistance uropathogenic bacteria in Iran: a systematic review and meta-analysis. Arch Clin Infect Dis 2018;13(5): e63256.
54. Japoni A, Gudarzi M, Farshad S, Basiri E, Ziyaeyan M, Alborzi A, et al. Assay for integrons and pattern of antibiotic resistance in clinical Escherichia coli strains by PCR-RFLP in Southern Iran. Jpn J Infect Dis 2008;61: 85-88.
55. Kozak GK, Pearl DL, Parkman J, Reid-Smith RJ, Deckert A, Boerlin P. Distribution of sulfonamide resistance genes in Escherichia coli and Salmonella isolates from swine and chickens at abattoirs in Ontario and Quebec, Canada. Appl Environ Microbiol 2009; 75: 5999-6001.
56. Bean DC, Livermore DM, Hall LM. Plasmids imparting sulfonamide resistance in Escherichia coli: implications for persistence. Antimicrob Agents Chemother 2009; 53: 1088-1093.
| Files | ||
| Issue | Vol 15 No 3 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v15i3.12898 | |
| Keywords | ||
| Escherichia coli; Antibiotic resistance; Epidemiology | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Ghotaslou R, Baghbani S, Ghotaslou P, Mirmahdavi S, Ebrahimzadeh Leylabadlo H. Molecular epidemiology of antibiotic-resistant Escherichia coli among clinical samples isolated in Azerbaijan, Iran. Iran J Microbiol. 2023;15(3):383-391.
