1887

Abstract

The resistance to quinolone reported in uropathogenic (UPEC) is commonly caused by mutations in the target site encoding genes such as the gene. Bacterial plasmids carrying resistance genes such as genes can also transfer resistance. Biofilms produced by UPEC can further aid the development of resistant urinary tract infections (UTIs).

Biofilm production is associated with higher prevalence of quinolones resistance genetic determinants.

To detect the prevalence of genes and gene mutation among quinolone-resistant UPEC and to investigate the relation between these genetic resistance determinants and biofilm production.

Catheterized urine samples were collected from 420 patients with evidence of UTIs and processed using standard techniques. Isolated UPEC were screened for quinolone resistance using an antimicrobial susceptibility test. Biofilm production among quinolone-resistant isolates was detected using the tissue culture plate method. All quinolone-resistant isolates were screened for genes ( and ) by multiplex PCR and for gene mutation by PCR-RFLP.

Two hundred and sixty-four UPEC isolates were detected from 420 processed urine samples. Out of the identified 264 UPEC 123 (46.6 %) isolates were found to be quinolone-resistant, showing resistance to 1 or more of the tested quinolones. Of the 123 quinolone-resistant UPEC detected, 71(57.7 %) were biofilm producers. The genes were detected among 62.6 % of the quinolone-resistant UPEC, with an estimated prevalence of 22.8 32.5 and 37.4 % for and genes, respectively. Additionally, the gene mutation was identified among 53.7 % of the quinolone-resistant isolates. We reported a significant association between biofilm production and the presence of , and genes. Furthermore, the gene mutation was significantly associated with biofilm-producing isolates. The coexistence of genes, gene mutation and biofilm production was demonstrated in almost 40 % of the quinolone-resistant isolates.

A significantly higher prevalence of genes ( and ) as well as the gene mutation was found among biofilm-forming UPEC. The reported coexistence of these different resistance mechanisms could aggravate quinolone resistance. Therefore, monitoring of resistance mechanisms and a proper stewardship programme are necessary.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001432
2021-10-19
2024-04-19
Loading full text...

Full text loading...

References

  1. Aldred KJ, Kerns RJ, Osheroff N. Mechanism of quinolone action and resistance. Biochemistry 2014; 53:1565–1574 [View Article] [PubMed]
    [Google Scholar]
  2. Dalhoff A. Resistance surveillance studies: a multifaceted problem--the fluoroquinolone example. Infection 2012; 40:239–262 [View Article] [PubMed]
    [Google Scholar]
  3. Redgrave LS, Sutton SB, Webber MA, Piddock LJ. Fluoroquinolone resistance: mechanisms, impact on bacteria, and role in evolutionary success. Trends Microbiol 2014; 22:438–445 [View Article] [PubMed]
    [Google Scholar]
  4. Drlica K, Malik M, Kerns RJ, Zhao X. Quinolone-mediated bacterial death. Antimicrob Agents Chemother 2008; 52:385–392 [View Article] [PubMed]
    [Google Scholar]
  5. Drlica K, Hiasa H, Kerns R, Malik M, Mustaev A et al. Quinolones: action and resistance updated. Curr Top Med Chem 2009; 9:981–998 [View Article] [PubMed]
    [Google Scholar]
  6. Livermore DM, Hope R, Reynolds R, Blackburn R, Johnson AP et al. Declining cephalosporin and fluoroquinolone non-susceptibility among bloodstream Enterobacteriaceae from the UK: links to prescribing change?. J Antimicrob Chemother 2013; 68:2667–2674 [View Article] [PubMed]
    [Google Scholar]
  7. Aldred KJ, McPherson SA, Turnbough CL, Kerns RJ, Osheroff N. Topoisomerase IV-quinolone interactions are mediated through a water-metal ion bridge: mechanistic basis of quinolone resistance. Nucleic Acids Res 2013; 41:4628–4639 [View Article] [PubMed]
    [Google Scholar]
  8. Strahilevitz J, Jacoby GA, Hooper DC, Robicsek A. Plasmid-mediated quinolone resistance: a multifaceted threat. Clin Microbiol Rev 2009; 22:664–689 [View Article] [PubMed]
    [Google Scholar]
  9. Rodríguez-Martínez JM, Cano ME, Velasco C, Martínez-Martínez L, Pascual A. Plasmid-mediated quinolone resistance: an update. J Infect Chemother 2011; 17:149–182 [View Article] [PubMed]
    [Google Scholar]
  10. Aparna MS, Yadav S. Biofilms: microbes and disease. Braz J Infect Dis 2008; 12:526–530S1413-86702008000600016 [View Article] [PubMed]
    [Google Scholar]
  11. Pelling H, Nzakizwanayo J, Milo S. Bacterial biofilm formation on indwelling urethral catheters. Lett Appl Microbiol 2019; 68:277–293 [View Article] [PubMed]
    [Google Scholar]
  12. Sultan AM. Yasmin Nabiel: Tube method and Congo red agar versus tissue culture plate method for detection of biofilm production by uropathogens isolated from midstream urine: Which one could be better?. African J Clin Exp Microbiol 2019; 20:60–66 [View Article]
    [Google Scholar]
  13. Clinical and Laboratory Standards Institute Performance Standards for Antimicrobial Susceptibility Testing, 28th ed. CLSI supplement M100. Wayne, PA: Clinical and Laboratory Standards Institute; 2018
    [Google Scholar]
  14. Bakir SH, Ali FA. Comparison of different methods for detection of biofilm production in multi-drug resistance bacteria causing pharyngotonsillitis. IJRPB 2016; 3:13–22
    [Google Scholar]
  15. Panda PS, Chaudhary U, Dube SK. Comparison of four different methods for detection of biofilm formation by uropathogens. Indian J Pathol Microbiol 2016; 59:177–179 [View Article] [PubMed]
    [Google Scholar]
  16. Sadeghi A, Halaji M, Fayyazi A, Havaei SA. Characterization of plasmid-mediated quinolone resistance and serogroup distributions of uropathogenic Escherichia coli among Iranian kidney transplant patients. Biomed Res Int 2020; 2020:2850183 [View Article] [PubMed]
    [Google Scholar]
  17. Yousefi S, Mojtahedi A, Shenagari M. A Survey of gyrA Target-Site Mutation and qnr Genes among Clinical Isolates of Escherichia coli in the North of Iran. Jundishapur J Microbiol 2018; 11:e67293 [View Article]
    [Google Scholar]
  18. Ruiz J. Mechanisms of resistance to quinolones: target alterations, decreased accumulation and DNA gyrase protection. J Antimicrob Chemother 2003; 51:1109–1117 [View Article] [PubMed]
    [Google Scholar]
  19. FarajzadehSheikh A, Veisi H, Shahin M, Getso M, Farahani A. Frequency of quinolone resistance genes among extended-spectrum β-lactamase (ESBL)-producing Escherichia coli strains isolated from urinary tract infections. Trop Med Health 2019; 47:19 [View Article] [PubMed]
    [Google Scholar]
  20. Malekzadegan Y, Rastegar E, Moradi M, Heidari H, Sedigh Ebrahim-Saraie H. Prevalence of quinolone-resistant uropathogenic Escherichia coli in a tertiary care hospital in south Iran [Response to letter]. Infect Drug Resist 2019; 12:2175–2176 [View Article] [PubMed]
    [Google Scholar]
  21. Guessennd N, Bremont S, Gbonon V et al. Résistance aux quinolones de type qnr chez les entérobactéries productrices de bêta-lactamases à spectre élargi à Abidjan en Côte d’Ivoire [Qnr-type quinolone resistance in extended-spectrum beta-lactamase producing enterobacteria in Abidjan, Ivory Coast]. Pathol Biol 2008; 56:439–446 [View Article]
    [Google Scholar]
  22. Tarchouna M, Ferjani A, Marzouk M, Guedda I, Boukadida J. Prevalence of plasmid-mediated quinolone resistance detrminants among clinical isolates of Escherichia coli in a Tunisian hospitals. Int J Curr Microbiol App Sci 2015; 4:195–206
    [Google Scholar]
  23. Moumouni A, Diagbouga S, Nadembèga C, Metuor Dabire A, Ouattara K et al. Quinolone resistance (qnr) genes in fecal carriage of extended Spectrum beta-lactamases producing Enterobacteria isolated from children in Niger. Curr Res Microbiol Biotechnol 2017; 5:953–957
    [Google Scholar]
  24. Salah FD, Soubeiga ST, Ouattara AK. Distribution of quinolone resistance gene (qnr) in ESBL-producing Escherichia coli and Klebsiella spp. in Lomé, Togo. Antimicrob Resist Infect Control 2019; 8:104 [View Article] [PubMed]
    [Google Scholar]
  25. Abbasi H, Ranjbar R. The prevalence of quinolone resistance genes of A, B, S in Escherichia coli strains isolated from three major hospitals in Tehran, Iran. Cent European J Urol 2018; 71:129–133 [View Article] [PubMed]
    [Google Scholar]
  26. Düzgün , Okumuş F, Saral A, Çiçek , Cinemre S. Determination of antibiotic resistance genes and virulence factors in Escherichia coli isolated from Turkish patients with urinary tract infection. Rev Soc Bras Med Trop 2019; 52:e20180499 [View Article]
    [Google Scholar]
  27. Minarini LA, Darini AL. Mutations in the quinolone resistance-determining regions of gyrA and parC in Enterobacteriaceae isolates from Brazil. Braz J Microbiol 2012; 43:1309–1314 [View Article] [PubMed]
    [Google Scholar]
  28. Sharma M, Aparna YS, Chaudhary U. Biofilm production in uropathogenic Escherichia coli. Indian J Pathol Microbiol 2009; 52:294 [View Article] [PubMed]
    [Google Scholar]
  29. Niveditha S, Pramodhini S, Umadevi S, Kumar S, Stephen S. The isolation and the biofilm formation of uropathogens in the patients with catheter associated Urinary Tract Infections (UTIs). J Clin Diagn Res 2012; 6:1478–1482 [View Article] [PubMed]
    [Google Scholar]
  30. Santos-Lopez A, Marshall CW, Scribner MR, Snyder DJ, Cooper VS. Evolutionary pathways to antibiotic resistance are dependent upon environmental structure and bacterial lifestyle. elife 2019; 8:e47612 [View Article] [PubMed]
    [Google Scholar]
  31. Penesyan A, Nagy SS, Kjelleberg S, Gillings MR, Paulsen IT. Rapid microevolution of biofilm cells in response to antibiotics. NPJ Biofilms Microbiomes 2019; 5:34 [View Article] [PubMed]
    [Google Scholar]
  32. Lynch AS, Robertson GT. Bacterial and fungal biofilm infections. Annu Rev Med 2008; 59:415–428 [View Article] [PubMed]
    [Google Scholar]
  33. Conibear TC, Collins SL, Webb JS. Role of mutation in Pseudomonas aeruginosa biofilm development. PLoS One 2009; 4:e6289 [View Article] [PubMed]
    [Google Scholar]
  34. Ryder VJ, Chopra I, O’Neill AJ. Increased mutability of Staphylococci in biofilms as a consequence of oxidative stress. PLoS One 2012; 7:e47695 [View Article] [PubMed]
    [Google Scholar]
  35. Steenackers HP, Parijs I, Dubey A, Foster KR, Vanderleyden J. Experimental evolution in biofilm populations [published correction appears in FEMS Microbiol Rev. 2016 Nov 1;40(6):980. Dubey, Akanksha [added]]. FEMS Microbiol Rev 2016; 40:373–397 [View Article]
    [Google Scholar]
  36. Stalder T, Cornwell B, Lacroix J. Evolving populations in biofilms contain more persistent plasmids. Mol Biol Evol 2020; 37:1563–1576 [View Article] [PubMed]
    [Google Scholar]
  37. Azizi O, Shakibaie MR, Modarresi F, Shahcheraghi F. Molecular detection of class-D OXA carbapenemase genes in biofilm and non-biofilm forming clinical isolates of Acinetobacter baumannii. Jundishapur J Microbiol 2015; 8:e21042 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001432
Loading
/content/journal/jmm/10.1099/jmm.0.001432
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error