Effect of Mentha longifolia essential oil on oqxA efflux pump gene expression and biofilm formation in ciprofloxacin-resistant Klebsiella pneumoniae strains
Abstract
Background and Objectives: Today, medicinal plants and their derivatives are considered to reduce the prevalence of antibiotic resistance. The aim of this study was to investigate the effect of Mentha longifolia essential oil on oqxA efflux pump gene expression and biofilm formation in ciprofloxacin-resistant Klebsiella pneumoniae strains.
Materials and Methods: A total of 50 clinical strains of K. pneumoniae resistant to ciprofloxacin were studied. The minimum inhibitory concentration (MIC) of M. longifolia essential oil and its synergistic effect with ciprofloxacin were determined using the microbroth dilution method and the fractional inhibitory concentration (FIC) method. Minimum biofilm inhibition concentration (MBIC) of M. longifolia essential oil was detected. The effect of essential oils on the expression level of the oqxA gene was detected by Real-time PCR.
Results: M. longifolia essential oil showed inhibitory activity against ciprofloxacin-resistant strains of K. pneumoniae. When M. longifolia essential oil was combined with ciprofloxacin, the MIC was reduced 2-4 times. In 28% of the strains, M. longifolia with ciprofloxacin showed a synergistic effect. M. longifolia essential oil reduces the strength of biofilm formation and alters the biofilm phenotype. A significant decrease in oqxA gene expression was observed in all isolates after treatment with M. longifolia essential oil.
Conclusion: Based on the results of this study, it was observed that supplementing M. longifolia essential oil can help reduce ciprofloxacin resistance and inhibit biofilm formation in fluoroquinolone-resistant K. pneumoniae strains.
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13. Gulluce M, Sahin F, Sokmen M, Ozer H, Daferera D, Sokmen A, et al. Antimicrobial and antioxidant properties of the essential oils and methanol extract from Mentha longifolia L. ssp. longifolia. Food Chem 2007; 103: 1449-1456.
14. Farzaei MH, Bahramsoltani R, Ghobadi A, Farzaei F, Najafi F. Pharmacological activity of Mentha longifolia and its phytoconstituents. J Tradit Chin Med 2017; 37: 710-720.
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20. Ashraf SA, Al-Shammari E, Hussain T, Tajuddin S, Panda BP. In-vitro antimicrobial activity and identification of bioactive components using GC–MS of commercially available essential oils in Saudi Arabia. J Food Sci Technol 2017; 54: 3948-3958.
21. Ghavam M, Bacchetta G, Castangia I, Manca ML. Evaluation of the composition and antimicrobial activities of essential oils from four species of Lamiaceae Martinov native to Iran. Sci Rep 2022; 12: 17044.
22. Ghafari O, Sharifi A, Ahmadi A, Nayeri Fasaei B. Antibacterial and anti‐PmrA activity of plant essential oils against fluoroquinolone‐resistant Streptococcus pneumoniae clinical isolates. Lett Appl Microbiol 2018; 67: 564-569.
23. O'Toole GA. Microtiter dish biofilm formation assay. J Vis Exp 2011; (47): 2437.
24. Martínez A, Manrique-Moreno M, Klaiss-Luna MC, Stashenko E, Zafra G, Ortiz C. Effect of essential oils on growth inhibition, biofilm formation and membrane integrity of Escherichia coli and Staphylococcus aureus. Antibiotics (Basel) 2021; 10: 1474.
25. Rodríguez-Martínez JM, Díaz de Alba P, Briales A, Machuca J, Lossa M, Fernández-Cuenca F, et al. Contribution of OqxAB efflux pumps to quinolone resistance in extended-spectrum-β-lactamase-producing Klebsiella pneumoniae. J Antimicrob Chemother 2013; 68: 68-73.
26. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C(T)) Method. Methods 2001; 25: 402-408.
27. Makvandi M, Shokoohizadeh L, Mirzaee M. Antibacterial and drug synergistic activities of mentha longifolia essential Oil against Shigella flexneri and Shigella sonnei. Int J Enteric Pathog 2017; 5: 92-95.
28. Seasotiya L, Dalal S. Screening of Indian medicinal plants as efflux pump inhibitors of fluoroquinolones. J Pharmacogn Phytochem 2014; 3: 235-241.
29. Iman Islamieh D, Goudarzi H, Khaledi A, Afshar D, Esmaeili D. Reduced efflux pumps expression of Pseudomonas aeruginosa with Satureja khuzistanica essential oil. Iran J Med Sci 2020; 45: 463-468.
30. Pazarci O, Tutar U, Kilinc S. Investigation of the antibiofilm effects of Mentha longifolia essential oil on titanium and stainless steel orthopedic implant surfaces. Eurasian J Med 2019; 51: 128-132.
31. Al-Shuneigat J, Al-Sarayreh S, Al-Saraireh Y, Al-Qudah M, Al-Tarawneh I. Effects of wild Thymus vulgaris essential oil on clinical isolates biofilm-forming bacteria. J Dent Med Sci 2014; 13: 62-66.
2. Russo TA, Marr CM. Hypervirulent Klebsiella pneumoniae. Clin Microbiol Rev 2019; 32 (3): e00001-19.
3. Shadkam S, Goli HR, Mirzaei B, Gholami M, Ahanjan M. Correlation between antimicrobial resistance and biofilm formation capability among Klebsiella pneumoniae strains isolated from hospitalized patients in Iran. Ann Clin Microbiol Antimicrob 2021; 20: 13.
4. Bengoechea JA, Sa Pessoa J. Klebsiella pneumoniae infection biology: living to counteract host defences. FEMS Microbiol Rev 2019; 43: 123-144.
5. 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.
6. Hooper DC, Jacoby GA. Mechanisms of drug resistance: quinolone resistance. Ann N Y Acad Sci 2015; 1354: 12-31.
7. Amereh F, Arabestani MR, Shokoohizadeh L. Relationship of OqxAB efflux pump to antibiotic resistance, mainly fluoroquinolones in Klebsiella pneumoniae, isolated from hospitalized patients. Iran J Basic Med Sci 2023; 26: 93-98.
8. Perez F, Rudin SD, Marshall SH, Coakley P, Chen L, Kreiswirth BN, et al. OqxAB, aquinolone and olaquindox efflux pump, is widely distributed among multidrug-resistant Klebsiella pneumoniae isolates of human origin. Antimicrob Agents Chemother 2013; 57: 4602-4603.
9. Li J, Zhang H, Ning J, Sajid A, Cheng G, Yuan Z, et al. The nature and epidemiology of OqxAB, a multidrug efflux pump. Antimicrob Resist Infect Control 2019; 8: 44.
10. Hernando-Amado S, Blanco P, Alcalde-Rico M, Corona F, Reales-Calderon JA, Sanchez MB, et al. Multidrug efflux pumps as main players in intrinsic and acquired resistance to antimicrobials. Drug Resist Updat 2016; 28: 13-27.
11. Sharma A, Gupta VK, Pathania R. Efflux pump inhibitors for bacterial pathogens: From bench to bedside. Indian J Med Res 2019; 149: 129-145.
12. Stavri M, Piddock LJ, Gibbons S. Bacterial efflux pump inhibitors from natural sources. J Antimicrob Chemother 2007; 59: 1247-1260.
13. Gulluce M, Sahin F, Sokmen M, Ozer H, Daferera D, Sokmen A, et al. Antimicrobial and antioxidant properties of the essential oils and methanol extract from Mentha longifolia L. ssp. longifolia. Food Chem 2007; 103: 1449-1456.
14. Farzaei MH, Bahramsoltani R, Ghobadi A, Farzaei F, Najafi F. Pharmacological activity of Mentha longifolia and its phytoconstituents. J Tradit Chin Med 2017; 37: 710-720.
15. Chouhan S, Sharma K, Guleria S. Antimicrobial activity of some essential oils-present status and future perspectives. Medicines (Basel) 2017; 4: 58.
16. Mahon CR, Lehman DC, Manuselis G (2014). Textbook of Diagnostic Microbiology, Elsevier, Amsterdam, Netherlands, 5th Edidtion edition.
17. Amereh F, Arabestani MR, Hosseini SM, Shokoohizadeh L. Association of qnr Genes and OqxAB efflux pump in Fluoroquinolone-resistant Klebsiella pneumoniae strains. Int J Microbiol 2023; 2023: 9199108.
18. CLSI. Performance, “Standards for antimicrobial susceptibility testing,” CLSI Supplement M100, Clinical and Laboratory Standards Institute, 31st edition, 2021.
19. Mahmoudi H, Shokoohizadeh L, Zare Fahim N, Mohamadi Bardebari A, Moradkhani S, Alikhani MY. Detection of adeABC efllux pump encoding genes and antimicrobial effect of Mentha longifolia and Menthol on MICs of imipenem and ciprofloxacin in clinical isolates of Acinetobacter baumannii. BMC Complement Med Ther 2020; 20: 92.
20. Ashraf SA, Al-Shammari E, Hussain T, Tajuddin S, Panda BP. In-vitro antimicrobial activity and identification of bioactive components using GC–MS of commercially available essential oils in Saudi Arabia. J Food Sci Technol 2017; 54: 3948-3958.
21. Ghavam M, Bacchetta G, Castangia I, Manca ML. Evaluation of the composition and antimicrobial activities of essential oils from four species of Lamiaceae Martinov native to Iran. Sci Rep 2022; 12: 17044.
22. Ghafari O, Sharifi A, Ahmadi A, Nayeri Fasaei B. Antibacterial and anti‐PmrA activity of plant essential oils against fluoroquinolone‐resistant Streptococcus pneumoniae clinical isolates. Lett Appl Microbiol 2018; 67: 564-569.
23. O'Toole GA. Microtiter dish biofilm formation assay. J Vis Exp 2011; (47): 2437.
24. Martínez A, Manrique-Moreno M, Klaiss-Luna MC, Stashenko E, Zafra G, Ortiz C. Effect of essential oils on growth inhibition, biofilm formation and membrane integrity of Escherichia coli and Staphylococcus aureus. Antibiotics (Basel) 2021; 10: 1474.
25. Rodríguez-Martínez JM, Díaz de Alba P, Briales A, Machuca J, Lossa M, Fernández-Cuenca F, et al. Contribution of OqxAB efflux pumps to quinolone resistance in extended-spectrum-β-lactamase-producing Klebsiella pneumoniae. J Antimicrob Chemother 2013; 68: 68-73.
26. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C(T)) Method. Methods 2001; 25: 402-408.
27. Makvandi M, Shokoohizadeh L, Mirzaee M. Antibacterial and drug synergistic activities of mentha longifolia essential Oil against Shigella flexneri and Shigella sonnei. Int J Enteric Pathog 2017; 5: 92-95.
28. Seasotiya L, Dalal S. Screening of Indian medicinal plants as efflux pump inhibitors of fluoroquinolones. J Pharmacogn Phytochem 2014; 3: 235-241.
29. Iman Islamieh D, Goudarzi H, Khaledi A, Afshar D, Esmaeili D. Reduced efflux pumps expression of Pseudomonas aeruginosa with Satureja khuzistanica essential oil. Iran J Med Sci 2020; 45: 463-468.
30. Pazarci O, Tutar U, Kilinc S. Investigation of the antibiofilm effects of Mentha longifolia essential oil on titanium and stainless steel orthopedic implant surfaces. Eurasian J Med 2019; 51: 128-132.
31. Al-Shuneigat J, Al-Sarayreh S, Al-Saraireh Y, Al-Qudah M, Al-Tarawneh I. Effects of wild Thymus vulgaris essential oil on clinical isolates biofilm-forming bacteria. J Dent Med Sci 2014; 13: 62-66.
| Files | ||
| Issue | Vol 16 No 4 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v16i4.16315 | |
| Keywords | ||
| Klebsiella pneumoniae; Ciprofloxacin; Biofilm; Efflux pump inhibitor | ||
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How to Cite
1.
Keyhani S, Alikhani MY, Doosti-Irani A, Shokoohizadeh L. Effect of Mentha longifolia essential oil on oqxA efflux pump gene expression and biofilm formation in ciprofloxacin-resistant Klebsiella pneumoniae strains. Iran J Microbiol. 2024;16(4):552-559.
