• Azhi Sarbast Abdalrahman Razga Company, Sulaimani City, 46001, Kurdistan Region, Iraq.
  • Khanda Abdullateef Anwar Department of Microbiology, College of Medicine, University of Sulaimani, Kurdistan Region, Iraq.



Cephalosporins, Extended-Spectrum β-Lactamase, ESBL, Enterobacteriaceae, UTI


Extended-Spectrum β-Lactamase are enzymes that provide resistance against third-and fourth generation Cephalosporins and Monobactams, and they are distributed among the Enterobacteriaceae family.

To describe the prevalence of Extended-Spectrum β-Lactamase among Enterobacteriaceae causing urinary tract infections in Sulaimani province.

Patients and Methods
One hundred bacterial isolates of Enterobacteriaceae from patients with urinary tract infections attending Smart Hospital (inpatients and outpatients). Urine samples were inoculated onto different culture media. Colony morphology, gram staining, and BD Phoenix™ system were used for bacterial identification. Antibiotic profile and Extended-Spectrum β-Lactamase were observed phenotypically by antibiotic profile results, double disk synergy test, and confirmed by combined disk test methods and BD Phoenix™ system.

Out of one hundred isolates of Enterobacteriaceae, Escherichia coli was the commonest isolate (89), followed by Klebsiella pneumoniae (10) and one isolate of Proteus mirabilis. According to the antibiotic profile, the most effective antibiotic among all three isolates was Imipenem and Nitrofurantoin, while the most resistant antibiotic was Nalidixic acid and third generation Cephalosporin. The prevalence rate of Extended-Spectrum β-Lactamase -producing Enterobacteriaceae was 69% by the screening tests and 48% by the confirmatory tests.

In this study, Extended-Spectrum β-Lactamase prevalence was shown to be at an alarming rate that must be considered. The high priority of public health justifies further investigation to properly establish annual surveillance systems that can aid in selecting an appropriate antibiotic upon ESBL detection.


Tan CW, Chlebicki MP. Urinary tract infections in adults. Singapore Med J. 2016 Sep;57(9):485–90. DOI:

Najar MS, Saldanha CL, Banday KA. Approach to urinary tract infections. Indian J Nephrol. 2009 Oct;19(4):129–39. DOI:

De Angelis G, Del Giacomo P, Posteraro B, Sanguinetti M, Tumbarello M. Molecular Mechanisms, Epidemiology, and Clinical Importance of β-Lactam Resistance in Enterobacteriaceae. Int J Mol Sci. 2020 Jul;21(14):5090. DOI:

Walsh C, Collyns T. The pathophysiology of urinary tract infections. Surg. 2017;35(6):293–8. DOI:

Waller TA, Pantin SAL, Yenior AL, Pujalte GGA. Urinary tract infection antibiotic resistance in the United States. Prim Care Clin Off Pract. 2018;45(3):455–66. DOI:

Ghafourian S, Sadeghifard N, Soheili S, Sekawi Z. Extended-spectrum beta-lactamases: definition, classification and epidemiology. Curr Issues Mol Biol. 2015;17(1):11–22.

Castanheira M, Simner PJ, Bradford PA. Extended-spectrum β-lactamases: an update on their characteristics, epidemiology and detection. JAC-antimicrobial Resist. 2021 Sep;3(3):dlab092. DOI:

Brolund A, Sandegren L. Characterization of ESBL disseminating plasmids. Infect Dis (Auckl). 2016;48(1):18–25. DOI:

Pietrucha-Dilanchian1 P, Hooton TM. Diagnosis, treatment, and prevention of urinary tract infection. Urin Tract Infect Mol Pathog Clin Manag. 2017;41–68. DOI:

Karah N, Rafei R, Elamin W, Ghazy A, Abbara A, Hamze M, et al. Guideline for urine culture and biochemical identification of bacterial urinary pathogens in low-resource settings. Diagnostics. 2020;10(10):832. DOI:

Majumder MI, Ahmed T, Sakib N, Khan AR, Saha CK. A follow-up study of bacteriology and antibiotic sensitivity pattern of urinary tract infection in a tertiary care hospital in Bangladesh. J Bacteriol Parasitol. 2018;9(334):2. DOI:

Feizabadi MM, Mahamadi-Yeganeh S, Mirsalehian A, Mirafshar S-M, Mahboobi M, Nili F, et al. Genetic characterisation of ESBL-producing strains of Klebsiella pneumoniae from Tehran hospitals. J Infect Dev Ctries. 2010;4(10):609–15. DOI:

Weinstein MP, Lewis JS. The Clinical and laboratory standards institute subcommittee on antimicrobial susceptibility testing: Background, organisation, functions, and Processes. J Clin Microbiol. 2020;58(3):e01864-19. DOI:

Kaur J, Chopra S, Sheevani GM. Modified double disc synergy test to detect ESBL production in urinary isolates of Escherichia coli and Klebsiella pneumoniae. J Clin Diagnostic Res JCDR. 2013;7(2):229. DOI:

Teklu DS. Comparison of Double Disk Synergy Test and Combination Disk Test Methods for detecting Extended-Spectrum Beta-Lactamase Production among Enterobacteriaceae. EC Microbiol. 2019;15(6):411–20.

Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol. 2015 May;13(5):269–84. DOI:

Aljanaby AAJ, Gafil FA-A. Effect of different antibiotics on aerobic pathogenic bacteria and urinary tract infection in Al-Manathera City, Iraq: a comparative study. Res Chem Intermed. 2013;39(8):3679–87. DOI:

Foxman B. The epidemiology of urinary tract infection. Nat Rev Urol. 2010 Dec;7(12):653–60. DOI:

Polse R, Yousif S, Assafi M. Prevalence and antimicrobial susceptibility patterns of uropathogenic E. coli among people in Zakho, Iraq. Int J Res Med Sci. 2016;4(4):1219–23. DOI:

Gatya Al-Mayahie SM, Al-Guranie DRT, Hussein AA, Bachai ZA. Prevalence of common carbapenemase genes and multidrug resistance among uropathogenic Escherichia coli phylogroup B2 isolates from outpatients in Wasit Province/Iraq. PLoS One. 2022;17(1):e0262984. DOI:

Hyun M, Lee JY, Kim HA, Ryu SY. Comparison of Escherichia coli and Klebsiella pneumoniae Acute Pyelonephritis in Korean Patients. Infect Chemother. 2019 Jun;51(2):130–41. DOI:

Erol B, Culpan M, Caskurlu H, Sari U, Cag Y, Vahaboglu H, et al. Changes in antimicrobial resistance and demographics of UTIs in pediatric patients in a single institution over six years. J Pediatr Urol. 2018;14(2):176-e1. DOI:

Ventola CL. The antibiotic resistance crisis: Part 1: Causes and threats. Pharm Ther. 2015;40(4):277.

Pishtiwan AH, Khadija KM. Prevalence of blaTEM, blaSHV, and blaCTX-M genes among ESBL-producing Klebsiella pneumoniae and Escherichia coli isolated from thalassemia patients in Erbil, Iraq. Mediterr J Hematol Infect Dis. 2019;11(1):e2019041. DOI:

Sakhi RJ. Isolation of Escherichia coli from diarrhoea and test their pathogenicity and susceptibility pattern for antibiotics. Internafional J Agric Sci Res. 2016;6(2):29–34.

R Kadhim S, M Hassan A, S Shoukat D. Antimicrobial susceptibility patterns against Escherichia coli and prevalence of extended–spectrum β-lactamases. Kerbala J Med. 2011;4(9):1019–23.

Frieri M, Kumar K, Boutin A. Antibiotic resistance. J Infect Public Health. 2017;10(4):369–78. DOI:

Murugan MS, Sinha DK, Kumar ORV, Yadav AK, Pruthvishree BS, Vadhana P, et al. Epidemiology of carbapenem-resistant Escherichia coli and first report of blaVIM carbapenemases gene in calves from India. Epidemiol Infect. 2019;147:E159. DOI:

Shams S, Hashemi A, Esmkhani M, Kermani S, Shams E, Piccirillo A. Imipenem resistance in clinical Escherichia coli from Qom, Iran. BMC Res Notes. 2018;11(1):1–5. DOI:

Naqid IA, Balatay AA, Hussein NR, Saeed KA, Ahmed HA, Yousif SH. Antibiotic Susceptibility Pattern of Escherichia coli Isolated from Various Clinical Samples in Duhok City, Kurdistan Region of Iraq. Int J Infect. 2020;7(3):e103740. DOI:

Denisuik AJ, Lagacé-Wiens PRS, Pitout JD, Mulvey MR, Simner PJ, Tailor F, et al. Molecular epidemiology of extended-spectrum β-lactamase-, AmpC β-lactamase-and carbapenemase-producing Escherichia coli and Klebsiella pneumoniae isolated from Canadian hospitals over five years: CANWARD 2007–11. J Antimicrob Chemother. 2013;68(suppl_1):i57–65. DOI:

Hussein AA, Al-Mayahie SMG. High distribution of AmpC-type ESBLs among Escherichia coli isolates from outpatients with urinary tract infection in Wasit Province, Iraq. Indian J Nat Sci. 2019;9(55):17545–54.

Yazdansetad S, Alkhudhairy MK, Najafpour R, Farajtabrizi E, Al-Mosawi RM, Saki M, et al. A preliminary survey of extended-spectrum β-lactamases (ESBLs) in nosocomial uropathogenic Klebsiella pneumoniae in north-central Iran. Heliyon. 2019;5(9):e02349. DOI:

Goudarzi M, Sabzehali F, Tayebi Z, Azad M, Boromandi S, Hashemi A, et al. Prevalence of blaCTX-M gene in multi-resistant Escherichia coli isolated from Urinary Tract Infections, Tehran, Iran. Nov Biomed. 2014;2(4):107–13.

Isikgoz Tasbakan M, Durusoy R, Pullukcu H, Sipahi OR, Ulusoy S. Hospital-acquired urinary tract infection point prevalence in Turkey: differences in risk factors among patient groups. Ann Clin Microbiol Antimicrob. 2013;12(1):1–8. DOI:

Rodriguez-Bano J, Alcalá JC, Cisneros JM, Grill F, Oliver A, Horcajada JP, et al. Community infections caused by extended-spectrum β-lactamase–producing Escherichia coli. Arch Intern Med. 2008;168(17):1897–902. DOI:

Luo Y, Ma Y, Zhao Q, Wang L, Guo L, Ye L, et al. Similarity and divergence of phylogenies, antimicrobial susceptibilities, and virulence factor profiles of Escherichia coli isolate causing recurrent urinary tract infections that persist or result from reinfection. J Clin Microbiol. 2012;50(12):4002–7. DOI:

Rawat D, Nair D. Extended-spectrum β-lactamases in Gram Negative Bacteria. J Glob Infect Dis. 2010 Sep;2(3):263–74. DOI:



How to Cite

Abdalrahman A, Anwar K. PREVALENCE RATE OF ESBL AMONG ENTEROBACTERIACEAE ISOLATED FROM UTI PATIENTS IN SULAIMANI PROVINCE. JSMC [Internet]. 2023 Jun. 21 [cited 2024 Jun. 13];13(2):8. Available from:

Similar Articles

1-10 of 32

You may also start an advanced similarity search for this article.