Detection of Carbapenemase-Producing Klebsiella pneumoniae and Escherichia coli Recovered from Clinical Specimens in Erbil City Kurdistan Region of Iraq


  • Heshu Jalal Ahmed MSc Student, Hawler Medical University
  • Aryan R. Ganjo Department of Pharmacognosy, College of Pharmacy, Hawler Medical University, Erbil, Kurdistan.



Carbapenemase, Escherichia coli, EDTA-combination disk test, Klebsiella pneumoniae, Modified Hodge test, Multi-drug resistant.


Background: Carbapenems are usually the choice of antimicrobial agents in infections produced by Enterobacteriaceae bacteria-producing ESBL (extended spectrum β-lactamases). Carbapenemase production among clinical isolates of Enterobacteriaceae has been widely reported and Resistance to carbapenems group is generally due to production of Carbapenemases. Phenotypic determination and distinction of Carbapenemases in drug-resistant gram-negative is crucial for appropriate infection control. Materials and Methods: Carbapenemase production among Enterobacteriaceae isolates was identified phenotypically using a commercially available EDTA-combined disc diffusion test containing inhibitors to the various carbapenemase classes and Modified Hodge test (MHT). Results: A total of 98 Enterobacteriaceae isolates were included, 42(42.8%) were Multi-drug resistant (MDR), 27(27.5%) were XDR while 8(8.2%) exhibited pan-drug resistance (PDR). Of the 74 isolates of Escherichia coli and 24 Klebsiella pneumoniae that were positive for carbapenemase production, 12 (16.2%) and 9 (37.5%) were Metallo beta-lactamase (MBL) producers respectively, Hence, the overall prevalence of carbapenemase-producing Escherichia coli and Klebsiella pneumoniae in this study were 47.3% and 87.5%. Conclusion: Carbapenemase-producing Enterobacteriaceae was indeed recognized in our hospitals. The EDTA-combination disk test was a rapid, cost-effective and suitable method which will be able to identify and distinguish the carbapenem-resistant bacterial isolates within the hospitals especially when molecular detection techniques are not available.


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N. Girish, K. Saileela, and S. Mohanty, "Extended Spectrum β-Lactamase producing Klebsiella pneumoniae and Escherichia coli in neonatal intensive care unit," J Bacteriol Parasitol, vol. 3, pp. 1-3, 2012.

A. Poulou, E. Grivakou, G. Vrioni, V. Koumaki, T. Pittaras, S. Pournaras, et al., "Modified CLSI extended-spectrum β-lactamase (ESBL) confirmatory test for phenotypic detection of ESBLs among Enterobacteriaceae producing various β-lactamases," Journal of clinical microbiology, vol. 52, pp. 1483-1489, 2014. [

">Crossref] [PubMed ID: 24574283 PMCid:PMC3993656]

P. Nordmann, T. Naas, and L. Poirel, "Global spread of carbapenemase-producing Enterobacteriaceae," Emerging infectious diseases, vol. 17, p. 1791, 2011. [

">Crossref] [PubMed ID: 22000347 PMCid:PMC3310682]

J. Rolain, P. Parola, and G. Cornaglia, "New Delhi metallo‐beta‐lactamase (NDM‐1): towards a new pandemia?," Clinical Microbiology and Infection, vol. 16, pp. 1699-1701, 2010. [

">Crossref] [PubMed ID: 20874758]

D. L. Paterson, "Resistance in gram-negative bacteria: Enterobacteriaceae," American journal of infection control, vol. 34, pp. S20-S28, 2006. [

">Crossref] [PubMed ID: 16813978]

P. A. Bradford, "Extended-spectrum β-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat," Clinical microbiology reviews, vol. 14, pp. 933-951, 2001. [

">Crossref] [PubMed ID: 11585791 PMCid:PMC89009]

S. Pottumarthy, E. S. Moland, S. Juretschko, S. R. Swanzy, K. S. Thomson, and T. R. Fritsche, "NmcA carbapenem-hydrolyzing enzyme in Enterobacter cloacae in North America," Emerging infectious diseases, vol. 9, p. 999, 2003. [

">Crossref] [PubMed ID: 12967501 PMCid:PMC3020613]

M. Kaur, S. Gupte, and T. Kaur, "Detection of carbapenem resistant gram-negative bacteria in clinical isolates from a tertiary care hospital," J Bacteriol Mycol Open Access, vol. 2, p. 00011, 2016. [


R. Dahab, A. M. Ibrahim, and H. N. Altayb, "Phenotypic and genotypic detection of carbapenemase enzymes producing gram-negative bacilli isolated from patients in Khartoum State," F1000Research, vol. 6, 2017. [


V. Miriagou, G. Cornaglia, M. Edelstein, I. Galani, C. Giske, M. Gniadkowski, et al., "Acquired carbapenemases in Gram-negative bacterial pathogens: detection and surveillance issues," Clinical microbiology and infection, vol. 16, pp. 112-122, 2010. [

">Crossref] [PubMed ID: 20085605]

I. Galani, P. D. Rekatsina, D. Hatzaki, D. Plachouras, M. Souli, and H. Giamarellou, "Evaluation of different laboratory tests for the detection of metallo-β-lactamase production in Enterobacteriaceae," Journal of antimicrobial chemotherapy, vol. 61, pp. 548-553, 2008. [Crossref] [PubMed ID: 18222954]

K. Lee, Y. Chong, H. Shin, Y. Kim, D. Yong, and J. Yum, "Modified Hodge and EDTA‐disk synergy tests to screen metallo‐β‐lactamase‐producing strains of Pseudomonas and Acinetobacter species," Clinical microbiology and infection, vol. 7, pp. 88-91, 2001. [

">Crossref] [PubMed ID: 11298149]

P. Wayne, "Clinical and Laboratory Standards Institute: Performance standards for antimicrobial susceptibility testing: Twenty-fourth informational supplement, M100-S24," Clinical and Laboratory Standards Institute (CLSI), vol. 34, 2014.

R. Adrizain, F. Suryaningrat, A. Alam, and D. Setiabudi, "Incidence of multidrug-resistant, extensively drug-resistant and pan-drug-resistant bacteria in children hospitalized at Dr. Hasan Sadikin general hospital Bandung Indonesia," in IOP Conference Series: Earth and Environmental Science, 2018, p. 012077. [


C. f. D. Control and Prevention, "Modified Hodge test for carbapenemase detection in Enterobacteriaceae," ed, 2013.

S. R. Schlesinger, M. J. Lahousse, T. O. Foster, and S.-K. Kim, "Metallo-β-lactamases and aptamer-based inhibition," Pharmaceuticals, vol. 4, pp. 419-428, 2011. [

">Crossref] [PubMed ID: PMC4053962]

K. A. Anoar, F. A. Ali, and S. A. Omer, "Phenotypic detection of metallo-lactamase enzyme among Gram-negative bacteria isolated from burn patients in Sulaimani, Iraq," Int J Curr Microbiol Appl Sci, vol. 3, pp. 315-325, 2014.

S. van Burgh, D. M. Maghdid, A. R. Ganjo, I. Y. Mansoor, D. J. Kok, M. H. Fatah, et al., "PME and Other ESBL-Positive Multiresistant Pseudomonas aeruginosa Isolated from Hospitalized Patients in the Region of Kurdistan, Iraq," Microbial Drug Resistance, 2018. [

">Crossref] [PubMed ID: 30067166]

A. H. Al-Charrakh, S. J. Al-Awadi, and A. S. Mohammed, "Detection of metallo-β-lactamase producing Pseudomonas aeruginosa isolated from public and private hospitals in Baghdad, Iraq," Acta Medica Iranica, vol. 54, pp. 107-113, 2016.

L. Romero, L. Lopez, J. Rodriguez-Bano, J. R. Hernandez, L. Martinez-Martinez, and A. Pascual, "Long-term study of the frequency of Escherichia coli and Klebsiella pneumoniae isolates producing extended-spectrum β-lactamases," Clinical microbiology and infection, vol. 11, pp. 625-631, 2005. [

">Crossref] [PubMed ID: 16008614]

P. E. Akpaka and W. H. Swanston, "Phenotypic detection and occurrence of extended-spectrum beta-lactamases in clinical isolates of Klebsiella pneumoniae and Escherichia coli at a tertiary hospital in Trinidad & Tobago," Brazilian Journal of Infectious Diseases, vol. 12, pp. 516-520, 2008. [

">Crossref] [PubMed ID: 19287841]

S. Ahmad, N. F. Al-Juaid, F. Q. Alenzi, E. H. Mattar, and O. E.-S. Bakheet, "Prevalence, Antibiotic Susceptibility Pattern and Production of Extended-Spectrum ββ-Lactamases Amongst Clinical Isolates of Klebsiella pneumoniae at Armed Forces Hospital in Saudi Arabia," J Coll Physicians Surg Pak, vol. 19, pp. 264-5, 2009.

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



F. Ghanbari, F. Khademi, S. Saberianpour, M. Shahin, N. Ghanbari, K. Naderi, et al., "An Epidemiological Study on the Prevalence and Antibiotic Resistance Patterns of Bacteria Isolated from Urinary Tract Infections in Central Iran," Avicenna Journal of Clinical Microbiology and Infection, vol. 4, 2017. [


L. Folgori, S. Livadiotti, M. Carletti, J. Bielicki, G. Pontrelli, M. L. C. Degli Atti, et al., "Epidemiology and clinical outcomes of multidrug-resistant, gram-negative bloodstream infections in a European tertiary pediatric hospital during a 12-month period," The Pediatric infectious disease journal, vol. 33, pp. 929-932, 2014. [

">Crossref] [PubMed ID: 24642515]

S. Basak, P. Singh, and M. Rajurkar, "Multidrug resistant and extensively drug resistant bacteria: A study," Journal of pathogens, vol. 2016, 2016. [

">Crossref] [PubMed ID: 26942013 PMCid:PMC4749793]

A. Birgy, P. Bidet, N. Genel, C. Doit, D. Decré, G. Arlet, et al., "Phenotypic screening of carbapenemases and associated beta-lactamases in carbapenem-resistant Enterobacteriaceae," Journal of clinical microbiology, pp. JCM. 06131-11, 2012. [

">Crossref] [PubMed ID: 22259214 PMCid:PMC3318498]

J.-J. Yan, J.-J. Wu, S.-H. Tsai, and C.-L. Chuang, "Comparison of the double-disk, combined disk, and Etest methods for detecting metallo-β-lactamases in gram-negative bacilli," Diagnostic microbiology and infectious disease, vol. 49, pp. 5-11, 2004. [

">Crossref] [PubMed ID: 15135493]

M. A. D. Fakhuruddin, I. Bakar, R. Ahmed, and M. Kumar, "ONLINE SUBMISSION."


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How to Cite

H. J. Ahmed and A. R. Ganjo, “Detection of Carbapenemase-Producing Klebsiella pneumoniae and Escherichia coli Recovered from Clinical Specimens in Erbil City Kurdistan Region of Iraq”, Al-Mustansiriyah Journal of Science, vol. 30, no. 2, pp. 10–18, Sep. 2019, doi: 10.23851/mjs.v30i2.612.

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