Volume 9, Issue 3 (2023)                   IEM 2023, 9(3): 209-218 | Back to browse issues page

XML Print

Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:

Qasim Raheem H, Al-Maliki L, Alaa Abdolzahra M, Shafi Hussein T. Prevalence of Extended-Spectrum B-Lactamase (ESBL) and Quinolone Resistance (qnr) Genes among Cytotoxic Necrotizing Factor-1-Producing Uropathogenic Escherichia coli in Babylon, Iraq. IEM 2023; 9 (3) :209-218
URL: http://iem.modares.ac.ir/article-4-69926-en.html
1- DNA Research center, University of Babylon, Al-Karameh Street-51001, Babylon state, Iraq , haiderbio412@gmail.com
2- Department of Molecular and Medical biotechnology, college of Biotechnology Al-Nahrain University
3- Department of Pharmacy, Al-Amal College For Medical Specialized Sciences, Karbala-56001, Iraq
Abstract:   (607 Views)
Background: Pathogenic Escherichia coli (E. coli) is usually known as the principal agent of hospital-acquired infections, particularly those related to urinary tract infections (UTIs). The purpose of tThis study aimedwas to determine ESBL (extended-spectrum B-lactamase) production and quinolone resistance (qnr) genes in cytotoxic necrotizing factor 1 (CNF-1)- producing E. coli isolatesd from UTIs in Iraq.
Materials & Methods: A total of 996 E. coli isolates were obtained from UTIs infections in two general hospitals in Hillah, Babylon, Iraq (during 2014-2022), and 100 uropathogenic E. coli (UPEC) were cnf-1 gene carriers. ESBL production was evaluated using the double-disk synergy -test. The qnr genes were detected using polymerase chain reaction (PCR).
Findings: Nalidixic acid and chloramphenicol resistance wasincluded 70% and 30%, respectively. ESBL production was observed among 46% of cnf-1 -carriers isolates. The qnrA, qnrB, and qnrS genes were detected in 18%, 21%, and 11% of the isolates, respectively. ESBL-producing isolates mainly carried the qnrB gene and showedhad the highest resistance levels to quinolones. Major risk factors of pathogenic E. coli isolation included older age (68%, p= 0.031), previous hospitalization (76%, p= 0.021), and urinary catheter (83%, p= 0.018).
Conclusion: Although the prevalenceexistence of the cnf-1 gene was not high among UPEC isolates, its prevalencerate was high among quinolone-resistant and ESBL-producing isolates. The cContinuous investigation of virulence and resistance genes is essential tfor monitoring and controlling the infections and facilitate their control. ItMore investigation is necessary to determine the virulence  traits factors and resistance genes among UPEC in Iraq and to take in timely measures action to hinder the spread of resistance genes from spreading to other nosocomial isolates.
Full-Text [PDF 807 kb]   (123 Downloads)    
Article Type: Original Research | Subject: Bacteriology
Received: 2023/06/19 | Accepted: 2023/10/4 | Published: 2023/10/18

1. References
2. McDanel J, Schweizer M, Crabb V, Nelson R, Samore M, Khader K, et al. Incidence of Extended-Spectrum β-Lactamase (ESBL)-Producing Escherichia coli and Klebsiella Infections in the United States: A Systematic Literature Review. Infect Control Hosp Epidemiol 2017; 38(10):1209-1215. [DOI:10.1017/ice.2017.156] [PMID]
3. Jiang X, Yu T, Wu N, Meng H, Shi L. Detection of qnr, aac(6')-Ib-cr and qepA genes in Escherichia coli isolated from cooked meat products in Henan, China. Int J Food Microbiol 2014; 187:22-25. [DOI:10.1016/j.ijfoodmicro.2014.06.026] [PMID]
4. Rodríguez-Martínez JM, Cano ME, Velasco C, Martínez-Martínez L, Pascual A. Plasmid-mediated quinolone resistance: an update. J Infect Chemother 2011; 17(2):149-182. [DOI:10.1007/s10156-010-0120-2] [PMID]
5. Ezzeroug Ezzraimi A, Hannachi N, Mariotti A, Rolain JM, Camoin-Jau L. Platelets and Escherichia coli: A Complex Interaction. Biomedicines 2022; 10(7). [DOI:10.3390/biomedicines10071636] [PMID] []
6. Ramuta T, Tratnjek L, Janev A, Seme K, Starčič Erjavec M, Kreft ME. The Antibacterial Activity of Human Amniotic Membrane against Multidrug-Resistant Bacteria Associated with Urinary Tract Infections: New Insights from Normal and Cancerous Urothelial Models. Biomedicines 2021; 9(2). [DOI:10.3390/biomedicines9020218] [PMID] []
7. Shah C, Baral R, Bartaula B, Shrestha LB. Virulence factors of uropathogenic Escherichia coli (UPEC) and correlation with antimicrobial resistance. BMC Microbiol 2019; 19(1):204. [DOI:10.1186/s12866-019-1587-3] [PMID] []
8. Kaur H, Modgil V, Chaudhary N, Mohan B, Taneja N. Computational Guided Drug Targets Identification against Extended-Spectrum Beta-Lactamase-Producing Multi-Drug Resistant Uropathogenic Escherichia coli. Biomedicines 2023; 11(7). [DOI:10.3390/biomedicines11072028] [PMID] []
9. Holmbom M, Möller V, Kristinsdottir L, Nilsson M, Rashid MU, Fredrikson M, et al. Risk factors and outcome due to extended-spectrum β-lactamase-producing uropathogenic Escherichia coli in community-onset bloodstream infections: A ten-year cohort study in Sweden. PLoS One 2022; 17(11):e0277054. [DOI:10.1371/journal.pone.0277054] [PMID] []
10. 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:10.1371/journal.pone.0262984] [PMID] []
11. Tseng C-H, Liu C-W, Liu P-Y. Extended-Spectrum β-Lactamases (ESBL) Producing Bacteria in Animals. Antibiotics 2023; 12(4):661. [DOI:10.3390/antibiotics12040661] [PMID] []
12. Karlowsky JA, Lob SH, DeRyke CA, Siddiqui F, Young K, Motyl MR, et al. Prevalence of ESBL non-CRE Escherichia coli and Klebsiella pneumoniae among clinical isolates collected by the SMART global surveillance programme from 2015 to 2019. Int J Antimicrob Agents 2022; 59(3):106535. [DOI:10.1016/j.ijantimicag.2022.106535] [PMID]
13. Palmeira JD, Ferreira HMN. Extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae in cattle production-a threat around the world. Heliyon 2020; 6(1). [DOI:10.1016/j.heliyon.2020.e03206] [PMID] []
14. Ortiz-Díez G, Mengíbar RL, Turrientes M-C, Artigao M-RB, Gallifa RL, Tello AM, et al. Prevalence, incidence and risk factors for acquisition and colonization of extended-spectrum beta-lactamase-and carbapenemase-producing Enterobacteriaceae from dogs attended at a veterinary hospital in Spain. Comparative Immunology, Microbiology and Infectious Diseases 2023; 92:101922. [DOI:10.1016/j.cimid.2022.101922] [PMID]
15. Lima LS, Proietti-Junior AA, Rodrigues YC, da Silva Vieira MC, Lima L, de Oliveira Souza C, et al. High Genetic Diversity and Antimicrobial Resistance in Escherichia coli Highlight Arapaima gigas (Pisces: Arapaimidae) as a Reservoir of Quinolone-Resistant Strains in Brazilian Amazon Rivers. Microorganisms 2022; 10(4). [DOI:10.3390/microorganisms10040808] [PMID] []
16. Briales A, Rodríguez-Martínez JM, Velasco C, de Alba PD, Rodríguez-Baño J, Martínez-Martínez L, et al. Prevalence of plasmid-mediated quinolone resistance determinants qnr and aac(6')-Ib-cr in Escherichia coli and Klebsiella pneumoniae producing extended-spectrum β-lactamases in Spain. Int J Antimicrob Agents 2012; 39(5):431-434. [DOI:10.1016/j.ijantimicag.2011.12.009] [PMID]
17. Kariuki K, Diakhate MM, Musembi S, Tornberg-Belanger SN, Rwigi D, Mutuma T, et al. Plasmid-mediated quinolone resistance genes detected in Ciprofloxacin non-susceptible Escherichia coli and Klebsiella isolated from children under five years at hospital discharge, Kenya. BMC Microbiol 2023; 23(1):129. [DOI:10.1186/s12866-023-02849-2] [PMID] []
18. Jacoby GA, Strahilevitz J, Hooper DC. Plasmid-mediated quinolone resistance. Microbiol Spectr 2014; 2(5). [DOI:10.1128/microbiolspec.PLAS-0006-2013] [PMID] []
19. Akshay SD, Nayak S, Deekshit VK, Rohit A, Maiti B. Differential expression of outer membrane proteins and quinolone resistance determining region mutations can lead to ciprofloxacin resistance in Salmonella Typhi. Arch Microbiol 2023; 205(4):136. [DOI:10.1007/s00203-023-03485-0] [PMID]
20. Rodríguez-Martínez JM, Machuca J, Cano ME, Calvo J, Martínez-Martínez L, Pascual A. Plasmid-mediated quinolone resistance: Two decades on. Drug Resist Updat 2016; 29:13-29. [DOI:10.1016/j.drup.2016.09.001] [PMID]
21. Aldred KJ, Kerns RJ, Osheroff N. Mechanism of quinolone action and resistance. Biochemistry 2014; 53(10):1565-1574. [DOI:10.1021/bi5000564] [PMID] []
22. Doma AO, Popescu R, Mitulețu M, Muntean D, Dégi J, Boldea MV, et al. Comparative evaluation of qnrA, qnrB, and qnrS genes in Enterobacteriaceae ciprofloxacin-resistant cases, in swine units and a hospital from Western Romania. Antibiotics 2020; 9(10):698. [DOI:10.3390/antibiotics9100698] [PMID] []
23. Amador P, Fernandes R, Prudêncio C, Duarte I. Prevalence of Antibiotic Resistance Genes in Multidrug-Resistant Enterobacteriaceae on Portuguese Livestock Manure. Antibiotics (Basel) 2019; 8(1). [DOI:10.3390/antibiotics8010023] [PMID] []
24. Aworh MK, Kwaga JK, Hendriksen RS, Okolocha EC, Harrell E, Thakur S. Quinolone-resistant Escherichia coli at the interface between humans, poultry and their shared environment-a potential public health risk. One Health Outlook 2023; 5(1):1-16. [DOI:10.1186/s42522-023-00079-0] [PMID] []
25. Ruiz E, Sáenz Y, Zarazaga M, Rocha-Gracia R, Martínez-Martínez L, Arlet G, et al. qnr, aac(6')-Ib-cr and qepA genes in Escherichia coli and Klebsiella spp.: genetic environments and plasmid and chromosomal location. J Antimicrob Chemother 2012; 67(4):886-897. [DOI:10.1093/jac/dkr548] [PMID]
26. Mohamed Ali I, Duman C, Bozdağ İ, Artan Abdi A, Nor Abdi M, Karakurt SE, et al. Microbiology and Drug Susceptibility Pattern of Bacterial Isolates from Patients with Chronic Suppurative Otitis Media at a Tertiary Care Hospital in Somalia. Infect Drug Resist 2022; 15:7733-7739. [DOI:10.2147/IDR.S390886] [PMID] []
27. Sora VM, Meroni G, Martino PA, Soggiu A, Bonizzi L, Zecconi A. Extraintestinal pathogenic Escherichia coli: Virulence factors and antibiotic resistance. Pathogens 2021; 10(11):1355. [DOI:10.3390/pathogens10111355] [PMID] []
28. Raimondi S, Righini L, Candeliere F, Musmeci E, Bonvicini F, Gentilomi G, et al. Antibiotic resistance, virulence factors, phenotyping, and genotyping of E. coli isolated from the feces of healthy subjects. Microorganisms 2019; 7(8):251. [DOI:10.3390/microorganisms7080251] [PMID] []
29. Wang MH, Kim KS. Cytotoxic necrotizing factor 1 contributes to Escherichia coli meningitis. Toxins (Basel) 2013; 5(11):2270-2280. [DOI:10.3390/toxins5112270] [PMID] []
30. Li XZ. Quinolone resistance in bacteria: emphasis on plasmid-mediated mechanisms. Int J Antimicrob Agents 2005; 25(6):453-463. [DOI:10.1016/j.ijantimicag.2005.04.002] [PMID]
31. Herrera-Vázquez A, Arellano-Aranda R, Hernández-Cueto D, Rodríguez-Miranda E, López-Briones S, Hernández-Luna MA. Detection of Cyclomodulin CNF-1 Toxin-Producing Strains of Escherichia coli in Pig Kidneys at a Slaughterhouse. Microorganisms 2023; 11(8). [DOI:10.3390/microorganisms11082065] [PMID] []
32. Alhadidi HA, Al-Qaysi SA, Al-Halbosiy MM. Prevalence and Cytotoxic Effects of Some Colibactin and cnf Genes among Escherichia coli Isolated from Urinary Tract Infections. 2022. [DOI:10.48022/mbl.2203.03005]
33. Chat H, Dalmasso G, Godfraind C, Bonnin V, Beyrouthy R, Bonnet M, et al. Cytotoxic necrotizing factor 1 hinders colon tumorigenesis induced by colibactin-producing Escherichia coli in ApcMin/+ mice. Gut Microbes 2023; 15(1):2229569. [DOI:10.1080/19490976.2023.2229569] [PMID] []
34. Harwalkar A, Gupta S, Rao A, Srinivasa H. Lower prevalence of hlyD, papC and cnf-1 genes in ciprofloxacin-resistant uropathogenic Escherichia coli than their susceptible counterparts isolated from southern India. Journal of infection and public health 2014; 7(5):413-419. [DOI:10.1016/j.jiph.2014.04.002] [PMID]
35. Da Silva GJ, Mendonça N. Association between antimicrobial resistance and virulence in Escherichia coli. Virulence 2012; 3(1):18-28. [DOI:10.4161/viru.3.1.18382] [PMID]
36. Marin J, Clermont O, Royer G, Mercier-Darty M, Decousser JW, Tenaillon O, et al. The Population Genomics of Increased Virulence and Antibiotic Resistance in Human Commensal Escherichia coli over 30 Years in France. Appl Environ Microbiol 2022; 88(15):e0066422. [DOI:10.1128/aem.00664-22] [PMID] []
37. Biggel M, Moons P, Nguyen MN, Goossens H, Van Puyvelde S. Convergence of virulence and antimicrobial resistance in increasingly prevalent Escherichia coli ST131 papGII+ sublineages. Commun Biol 2022; 5(1):752. [DOI:10.1038/s42003-022-03660-x] [PMID] []
38. Jia Y, Mao W, Liu B, Zhang S, Cao J, Xu X. Study on the drug resistance and pathogenicity of Escherichia coli isolated from calf diarrhea and the distribution of virulence genes and antimicrobial resistance genes. Frontiers in Microbiology 2022; 13:992111. [DOI:10.3389/fmicb.2022.992111] [PMID] []
39. Guiral E, Bosch J, Vila J, Soto SM. Prevalence of Escherichia coli among samples collected from the genital tract in pregnant and nonpregnant women: relationship with virulence. FEMS Microbiol Lett 2011; 314(2):170-173. [DOI:10.1111/j.1574-6968.2010.02160.x] [PMID]
40. Sfeir MM. Adoption of the updated CLSI fluoroquinolone breakpoints for Gram-negative bacteria in microbiology laboratories. Clin Microbiol Infect 2021; 27(2):308-310. [DOI:10.1016/j.cmi.2020.07.027] [PMID]
41. Quesada MD, Giménez M, Molinos S, Fernández G, Sánchez MD, Rivelo R, et al. Performance of VITEK-2 Compact and overnight MicroScan panels for direct identification and susceptibility testing of Gram-negative bacilli from positive FAN BacT/ALERT blood culture bottles. Clin Microbiol Infect 2010; 16(2):137-140. [DOI:10.1111/j.1469-0691.2009.02907.x] [PMID]
42. Cattoir V, Poirel L, Rotimi V, Soussy CJ, Nordmann P. Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J Antimicrob Chemother 2007; 60(2):394-397. [DOI:10.1093/jac/dkm204] [PMID]
43. Azam MW, Zarrilli R, Khan AU. Updates on the Virulence Factors Produced by Multidrug-Resistant Enterobacterales and Strategies to Control Their Infections. Microorganisms 2023; 11(8). [DOI:10.3390/microorganisms11081901] [PMID] []
44. Akiyama T, Khan AA. Molecular characterization of strains of fluoroquinolone-resistant Salmonella enterica serovar Schwarzengrund carrying multidrug resistance isolated from imported foods. J Antimicrob Chemother 2012; 67(1):101-110. [DOI:10.1093/jac/dkr414] [PMID]
45. Chong Y, Shimoda S, Shimono N. Current epidemiology, genetic evolution and clinical impact of extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae. Infect Genet Evol 2018; 61:185-188. [DOI:10.1016/j.meegid.2018.04.005] [PMID]
46. Onishi R, Shigemura K, Osawa K, Yang YM, Maeda K, Tanimoto H, et al. Impact on quinolone resistance of plasmid-mediated quinolone resistance gene and mutations in quinolone resistance-determining regions in extended spectrum beta lactamase-producing Klebsiella pneumoniae isolated from urinary tract infection patients. Pathog Dis 2022; 80(1). [DOI:10.1093/femspd/ftac030] [PMID]
47. Rahn DD. Urinary tract infections: contemporary management. Urol Nurs 2008; 28(5):333-341; quiz 342.
48. Rippere-Lampe KE, O'Brien AD, Conran R, Lockman HA. Mutation of the gene encoding cytotoxic necrotizing factor type 1 (cnf 1) attenuates the virulence of uropathogenic Escherichia coli. Infection and immunity 2001; 69(6):3954-3964. [DOI:10.1128/IAI.69.6.3954-3964.2001] [PMID] []
49. Morgan RN, Saleh SE, Farrag HA, Aboulwafa MM. Prevalence and pathologic effects of colibactin and cytotoxic necrotizing factor-1 (Cnf 1) in Escherichia coli: experimental and bioinformatics analyses. Gut pathogens 2019; 11:1-18. [DOI:10.1186/s13099-019-0304-y] [PMID] []
50. Dolejska M, Papagiannitsis CC. Plasmid-mediated resistance is going wild. Plasmid 2018; 99:99-111. [DOI:10.1016/j.plasmid.2018.09.010] [PMID]
51. Alawi M, Torrijos TV, Walsh F. Plasmid-mediated antimicrobial resistance in drinking water. Environmental Advances 2022:100191. [DOI:10.1016/j.envadv.2022.100191]
52. Meng M, Li Y, Yao H. Plasmid-mediated transfer of antibiotic resistance genes in soil. Antibiotics 2022; 11(4):525. [DOI:10.3390/antibiotics11040525] [PMID] []
53. Azargun R, Sadeghi MR, Soroush Barhaghi MH, Samadi Kafil H, Yeganeh F, Ahangar Oskouee M, et al. The prevalence of plasmid-mediated quinolone resistance and ESBL-production in Enterobacteriaceae isolated from urinary tract infections. Infect Drug Resist 2018; 11:1007-1014. [DOI:10.2147/IDR.S160720] [PMID] []
54. Liang H, Zhang J, Hu J, Li X, Li B. Fluoroquinolone Residues in the Environment Rapidly Induce Heritable Fluoroquinolone Resistance in Escherichia coli. Environmental Science & Technology 2023; 57(12):4784-4795. [DOI:10.1021/acs.est.2c04999] [PMID]
55. Allou N, Cambau E, Massias L, Chau F, Fantin B. Impact of low-level resistance to fluoroquinolones due to qnrA1 and qnrS1 genes or a gyrA mutation on ciprofloxacin bactericidal activity in a murine model of Escherichia coli urinary tract infection. Antimicrobial Agents and Chemotherapy 2009; 53(10):4292-4297. [DOI:10.1128/AAC.01664-08] [PMID] []
56. Firoozeh F, Zibaei M, Soleimani-Asl Y. Detection of plasmid-mediated qnr genes among the quinolone-resistant Escherichia coli isolates in Iran. The Journal of Infection in Developing Countries 2014; 8(07):818-822. [DOI:10.3855/jidc.3746] [PMID]
57. Ghasemian A, Mobarez AM, Peerayeh SN, Abadi AB. The association of surface adhesin genes and the biofilm formation among Klebsiella oxytoca clinical isolates. New microbes and new infections 2019; 27:36-39. [DOI:10.1016/j.nmni.2018.07.001] [PMID] []
58. Al Hamdan AS, Alghamdi AA, Alyousif GF, Hamza FA, Shafey MM, AlAmri AM, et al. Evaluating the prevalence and the risk factors of gram-negative multi-drug resistant bacteria in Eastern Saudi Arabia. Infection and Drug Resistance 2022:475-490. [DOI:10.2147/IDR.S350048] [PMID] []
59. Yalew GT, Muthupandian S, Hagos K, Negash L, Venkatraman G, Hagos YM, et al. Prevalence of bacterial vaginosis and aerobic vaginitis and their associated risk factors among pregnant women from northern Ethiopia: A cross-sectional study. PloS one 2022; 17(2):e0262692. [DOI:10.1371/journal.pone.0262692] [PMID] []
60. San Millan A. Evolution of Plasmid-Mediated Antibiotic Resistance in the Clinical Context. Trends Microbiol 2018; 26(12):978-985. [DOI:10.1016/j.tim.2018.06.007] [PMID]
61. DelaFuente J, Toribio-Celestino L, Santos-Lopez A, León-Sampedro R, Alonso-Del Valle A, Costas C, et al. Within-patient evolution of plasmid-mediated antimicrobial resistance. Nat Ecol Evol 2022; 6(12):1980-1991. [DOI:10.1038/s41559-022-01908-7] [PMID] []

Add your comments about this article : Your username or Email:

Send email to the article author

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.