Phenotypic and Molecular Study of Extended-Spectrum β-lactamases Producing Enterobacteriaceae from Urinary Tract Infection in Zakho city, Kurdistan Region/Iraq.


  • Dalia L. Hasan Department of Biology, Faculty of Science, University of Zakho, Duhok, Iraq
  • Haval M. Khalid Department of Biology, Faculty of Science, University of Zakho, Duhok, Iraq
  • Wijdan M. S. Mero Department of Biology, Faculty of Science, University of Zakho, Kurdistan Region, Iraq (Scientific Research Center, Nawroz University, Kurdistan Region –Iraq)




The prevalence of ESBLs producing Enterobacteriaceae are increasing locally and globally. This study aimed to investigate the antibiotic susceptibility profile of Enterobacteriaceae causing urinary tract infection and to record the prevalence of ESBLs genes among enterobacterial isolates. A total of 454 urine specimens were collected from outpatients with UTIs from two major hospitals in Zakho city; The Zakho General hospital and Emergency hospital. The enterobacterial isolates were identified using the phenotypic and conventional biochemical tests. The antibiotic susceptibility of the isolated organisms was determined using the disk diffusion method, and ESBL production was detected by a double-disk synergy test. The suspected ESBL producers were further confirmed by the amplification of specific primers using PCR assay. Out of 454 specimens, 239 enterobacterial isolates were identified. The most common detected isolates and their rates were: Escherichia coli (65.20 %) and Klebsiella pneumoniae (25.49 %). Imipenem was the most effective antibiotic used while, amoxicillin and ampicillin were the most resistant. The highest level of ESBL production was determined in E. coli (66.3 %) followed by K.  pneumoniae (30.43%). The predominant detected gene were both CTX-M and SHV equally followed by TEM. In conclusion, this study indicated that member of Enterobacteriaceae in particular E. coli and K. pneumoniae are the predominant species causing UTI. The isolated bacteria were resistant to most of used antibiotics except imipenem which was effective. These bacteria are becoming multidrug-resistant due to the absence of restriction in antibiotics uses, in addition to their abuse and overuse.


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Abdulrahman, I. S. (2018). Antimicrobial Susceptibility Pattern of Pathogenic Bacteria Causing Urinary Tract Infections at Azadi Hospital In Duhok CityKurdistan Region of Iraq. Science Journal of University of Zakho. 6(2): 46-50.‏

Ali, T., Ali, I., Khan, N. A., Han, B. and Gao, J. (2018). The growing genetic and functional diversity of extended spectrum beta-lactamases. BioMed research international, 2018: 1-14.

Assafi, M. S., Ali, F. F., Polis, R. F., Sabaly, N. J. and Qarani, S. M. (2022). An Epidemiological and Multidrug Resistance Study for E. coli Isolated from Urinary Tract Infection (Three Years of Study). Baghdad Science Journal.19(1):0007-0015.

Auda, J. G. and Al-Grawi, I. G. (2009). Isolation, Identification, and Antimicrobial Susceptibility of Uropathogenic Morganella Morganii. Al-Kindy College Medical Journal.5(1):28-32.‏

Chandel, D. S., Johnson, J. A., Chaudhry, R., Sharma, N., Shinkre, N., Parida, S., and Panigrahi, P. (2011). Extended-spectrum β-lactamase-producing Gram-negative bacteria causing neonatal sepsis in India in rural and urban settings. Journal of Medical Microbiology. 60( 4): 500-507.‏

den Heijer, C. D., Beerepoot, M. A., Prins, J. M., Geerlings, S. E.and Stobberingh, E. E. (2012). Determinants of antimicrobial resistance in Escherichia coli strains isolated from faeces and urine of women with recurrent urinary tract infections. PLoS One. 7(11): e49909 (1-4).

Eiamphungporn, W., Schaduangrat, N., Malik, A. A. And Nantasenamat, C. (2018). Tackling the antibiotic resistance caused by class A β-lactamases through the use of β-lactamase inhibitory protein. International Journal of Molecular Sciences.19(8): 2222-2227.‏

Engelkirk, P. G., & Duben-Engelkirk, J. L. (2008). Laboratory diagnosis of infectious diseases: essentials of diagnostic microbiology. Lippincott Williams & Wilkins.‏

Foxman, B. (2010). The epidemiology of urinary tract infection. Nature Reviews Urology.7(12): 653-660.‏

Gharavi, M. J., Zarei, J., Roshani-Asl, P., Yazdanyar, Z., Sharif, M., & Rashidi, N. (2021). Comprehensive study of antimicrobial susceptibility pattern and extended spectrum beta-lactamase (ESBL) prevalence in bacteria isolated from urine samples. Scientific Reports, 11(1), 1-11.‏

Habeeb, N.R., Hussein, M.S., Assafi .S.and Al-Dabbagh, S.A.(2014) Methicillin resistant staphylococcus aureus nasal colonization among secondary school students at duhok city-iraq. Journal of Microbiology and Infectious Diseases.4(2014): 59-63.

Haji, S. H., Jalal, S. T., Omer, S. A. and Mawlood, A. H. (2018). Molecular detection of SHV-Type ESBL in E. coli and K. pneumoniae and their antimicrobial resistance profile. Zanco Journal of Medical Sciences. 22(2):262-272.‏

Hudzicki, J. (2009). Kirby-Bauer disk diffusion susceptibility test protocol. American society for microbiology.703(15):55-63.‏

Ibrahim, M. S., Khalid, H. M., and Mero, W. M. (2020). Molecular Characterization of Some Virulence Genes and Antibiotic Susceptibility Pattern among Uropathogenic Escherichia coli Isolated from Patient in Zakho City/Iraq. Zanco Journal of Pure and Applied Sciences. 32(2):167-177.‏

Jarlier, V., Nicolas, M. H., Fournier, G., & Philippon, A. (1988). Extended broad-spectrum β-lactamases conferring transferable resistance to newer β-lactam agents in Enterobacteriaceae: hospital prevalence and susceptibility patterns. Clinical Infectious Diseases, 10(4), 867-878.‏

Khalid, H. M. andYassin, N. A. (2017). Distribution of extended spectrum β-lactamase genes among Proteus mirabilis isolated from clinical specimens in Duhok city, Kurdistan region, Iraq. Science Journal of University of Zakho. 5(1): 1-6.‏

Kim, Y. T., Kim, T. U., & Baik, H. S. (2006). Characterization of extended spectrum $beta $-lactamase genotype TEM, SHV, and CTX-M producing Klebsiella pneumoniae isolated from clinical specimens in Korea. Journal of microbiology and biotechnology, 16(6), 889-895.‏

Livermore, D. M. And Brown, D. F. (2001). Detection of β-lactamase-mediated resistance. Journal of antimicrobial chemotherapy.48(suppl-1): 59-64.‏

McNulty, C. A., Lecky, D. M., Xu-McCrae, L., Nakiboneka-Ssenabulya, D., Chung, K. T., Nichols, T., ... & Hawkey, P. M. (2018). CTX-M ESBL-producing Enterobacteriaceae: estimated prevalence in adults in England in 2014. Journal of Antimicrobial Chemotherapy, 73(5), 1368-1388.‏

Moustafa, A., Li, W., Singh, H., Moncera, K. J., Torralba, M. G., Yu, Y. and Telenti, A. (2018). Microbial metagenome of urinary tract infection. Scientific reports. 8(1): 1-12.‏

Osman, A. A. (2019). Antibiotic Resistance of Bacteria isolated in Urinary Tract Infections in Erbil City. Zanco Journal of Pure and Applied Sciences.31(4):42-49.‏

Patel, M. P., Hu, L., Brown, C. A., Sun, Z., Adamski, C. J., Stojanoski, V.and Palzkill, T. (2018). Synergistic effects of functionally distinct substitutions in β-lactamase variants shed light on the evolution of bacterial drug resistance. Journal of Biological Chemistry.293(46):17971-17984.‏

Pitout, J. D., Nordmann, P., Laupland, K. B., and Poirel, L. (2005). Emergence of Enterobacteriaceae producing extended-spectrum β-lactamases (ESBLs) in the community. Journal of antimicrobial chemotherapy. 56(1): 52-59.‏

Polse, R. F., Yousif, S. Y., & Assafi, M. S. (2016). Prevalence and molecular characterization of extended spectrum beta-Lactamases-producing uropathogenic Escherichia coli isolated in Zakho, Iraq. Journal of Microbiology and Infectious Diseases, 6(4), 163-167.‏

Rawat, D., & Nair, D. (2010). Extended-spectrum β-lactamases in Gram Negative Bacteria. Journal of global infectious diseases, 2(3), 263.‏

Rupp, M. E. and Fey, P. D. (2003). Extended spectrum β-lactamase (ESBL)-producing Enterobacteriaceae Drugs. Journal of Infrastructure Preservation and Resilience. 63(4):353-365.‏

Sana, T.,Rami, K.,Racha, B, Fouad, D., Marcel, A. and Hassan, M. (2011). Detection of genes TEM, OXA, SHV and CTX-M in 73 clinical isolates of Escherichia coli producers of extended spectrum Beta-lactamases and determination of their susceptibility to antibiotics. International Arabic Journal of Antimicrobial Agents. 1(1): 1-6.

Schwaber, M. J., Navon-Venezia, S., Schwartz, D. and Carmeli, Y. (2005). High levels of antimicrobial coresistance among extended-spectrum-β-lactamase-producing Enterobacteriaceae. Antimicrobial agents and chemotherapy.49(5): 2137-2139.‏

Shabeeb, B. T., Alghanimi, Y. K. and Ahmed, M. M. (2018). Molecular and Bacteriologic Study of â-lactam Resistance Proteus mirabilis associated with Urinary Tract Infection in Holy Karbala province, Iraq. Journal of Pharmaceutical Sciences and Research. 10(3):549-555.‏

Shakya, P., Shrestha, D., Maharja, E., Sharma, V. K., & Paudyal, R. (2017). Extended-spectrum βlactamase producing among Escherichia coli and Klebsiella spp causing urinary tract infections; a hospital-based study. Open Microbiol J, 11, 23-30.‏

Shrestha, A., Manandhar, S., Pokharel, P., Panthi, P. And Chaudhary, D. K. (2016). Prevalence of extended spectrum beta-Lactamase (ESBL) producing multidrug resistance gram-negative isolates causing urinary tract infection. EC Microbiol. 4(5): 749-755.‏

Suravaram, S., Hada, V. And Siddiqui, I. A. (2021). Comparison of antimicrobial susceptibility interpretation among Enterobacteriaceae using CLSI and EUCAST breakpoints. Indian journal of medical microbiology. 39(3): 315-319.‏

Tayh, G., Al Laham, N., Ben Yahia, H., Ben Sallem, R., Elottol, A. E.and Ben Slama, K. (2019). Extended-spectrum β-lactamases among Enterobacteriaceae isolated from urinary tract infections in Gaza strip, Palestine. BioMed research international. (2019): 4041801-11 p.

Teklu, D. S., Negeri, A. A., Legese, M. H., Bedada, T. L., Woldemariam, H. K., & Tullu, K. D. (2019). Extended-spectrum beta-lactamase production and multi-drug resistance among Enterobacteriaceae isolated in Addis Ababa, Ethiopia. Antimicrobial Resistance & Infection Control, 8(1), 1-12.‏

Tewari, R., Mitra, S. D., Ganaie, F., Venugopal, N., Das, S., Shome, R. And Shome, B. R. (2018). Prevalence of extended spectrum β-lactamase, AmpC β-lactamase and metallo β-lactamase mediated resistance in Escherichia coli from diagnostic and tertiary healthcare centers in south Bengaluru, India.‏ International Journal of Research in Medical Sciences.6(4):1308-1313.

Ye, Q., Wu, Q., Zhang, S., Zhang, J., Yang, G., Wang, J. And Chen, M. (2018). Characterization of extended-spectrum β-lactamase-producing Enterobacteriaceae from retail food in China. Frontiers in microbiology.9(1709):1-12.‏

Aljanaby, A. A. J., & Alhasnawi, H. M. R. J. (2017). Research article phenotypic and molecular characterization of multidrug resistant Klebsiella pneumoniae isolated from different clinical sources in Al-Najaf Province-Iraq. Pak. J. Biol. Sci, 20(5), 217-232.‏

Al-Hashimy, A. B., & Al-Musawy, W. K. (2020, November). Molecular Study and Antibiotic susceptibility patterns of some Extended Spectrum Beta-Lactamase Genes (ESBL) of Klebsiella pneumpniae in Urinary Tract Infections. In Jo urnal of Physics: Conference Series (Vol. 1660, No. 1, p. 012017).



How to Cite

L. Hasan, D., M. Khalid, H., & M. S. Mero, W. (2022). Phenotypic and Molecular Study of Extended-Spectrum β-lactamases Producing Enterobacteriaceae from Urinary Tract Infection in Zakho city, Kurdistan Region/Iraq. Academic Journal of Nawroz University, 11(3), 305–313.