Effect of povidone-iodine and propanol-based mecetronium ethyl sulphate on antimicrobial resistance and virulence in Staphylococcus aureus

Abstract Background Reports are available on cross-resistance between antibiotics and biocides. We evaluated the effect of povidone-iodine (PVP-I) and propanol-based mecetronium ethyl sulphate (PBM) on resistance development, antibiotics cross-resistance, and virulence in Staphylococcus aureus. Meth...

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Main Authors: Nada A. Barakat, Salwa A. Rasmy, Alaa El-Dien M. S. Hosny, Mona T. Kashef
Format: Article
Language:English
Published: BMC 2022-11-01
Series:Antimicrobial Resistance and Infection Control
Subjects:
Online Access:https://doi.org/10.1186/s13756-022-01178-9
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author Nada A. Barakat
Salwa A. Rasmy
Alaa El-Dien M. S. Hosny
Mona T. Kashef
author_facet Nada A. Barakat
Salwa A. Rasmy
Alaa El-Dien M. S. Hosny
Mona T. Kashef
author_sort Nada A. Barakat
collection DOAJ
description Abstract Background Reports are available on cross-resistance between antibiotics and biocides. We evaluated the effect of povidone-iodine (PVP-I) and propanol-based mecetronium ethyl sulphate (PBM) on resistance development, antibiotics cross-resistance, and virulence in Staphylococcus aureus. Methods The minimum inhibitory concentration (MIC) of PVP-I and PBM were determined against S. aureus ATCC 25923 using the agar-dilution method. Staphylococcus aureus ATCC 25923 was subjected to subinhibitory concentrations of the tested biocides in ten consecutive passages followed by five passages in a biocide-free medium; MIC was determined after each passage and after the fifth passage in the biocide-free medium. The developed resistant mutant was tested for cross-resistance to different antibiotics using Kirby-Bauer disk diffusion method. Antibiotic susceptibility profiles as well as biocides’ MIC were determined for 97 clinical S. aureus isolates. Isolates were categorized into susceptible and resistant to the tested biocides based on MIC distribution pattern. The virulence of the biocide-resistant mutant and the effect of subinhibitory concentrations of biocides on virulence (biofilm formation, hemolysin activity, and expression of virulence-related genes) were tested. Results PVP-I and PBM MIC were 5000 μg/mL and 664 μg/mL. No resistance developed to PVP-I but a 128-fold increase in PBM MIC was recorded, by repeated exposure. The developed PBM-resistant mutant acquired resistance to penicillin, cefoxitin, and ciprofloxacin. No clinical isolates were PVP-I-resistant while 48.5% were PBM-resistant. PBM-resistant isolates were more significantly detected among multidrug-resistant isolates. PVP-I subinhibitory concentrations (¼ and ½ of MIC) completely inhibited biofilm formation and significantly reduced hemolysin activity (7% and 0.28%, respectively). However, subinhibitory concentrations of PBM caused moderate reduction in biofilm activity and non-significant reduction in hemolysin activity. The ½ MIC of PVP-I significantly reduced the expression of hla, ebps, eno, fib, icaA, and icaD genes. The virulence of the biocide-resistant mutant was similar to that of parent strain. Conclusion PVP-I is a highly recommended antiseptic for use in healthcare settings to control the evolution of high-risk clones. Exposure to PVP-I causes no resistance-development risk in S. aureus, with virulence inhibition by subinhibitory concentrations. Also, special protocols need to be followed during PBM use in hospitals to avoid the selection of resistant strains.
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spelling doaj.art-d1562f3646dd4f7988a907339534ba442022-12-22T02:31:04ZengBMCAntimicrobial Resistance and Infection Control2047-29942022-11-0111111410.1186/s13756-022-01178-9Effect of povidone-iodine and propanol-based mecetronium ethyl sulphate on antimicrobial resistance and virulence in Staphylococcus aureusNada A. Barakat0Salwa A. Rasmy1Alaa El-Dien M. S. Hosny2Mona T. Kashef3Department of Microbiology and Immunology, Faculty of Pharmacy, Cairo UniversityDepartment of Microbiology and Immunology, Faculty of Pharmacy, Cairo UniversityDepartment of Microbiology and Immunology, Faculty of Pharmacy, Cairo UniversityDepartment of Microbiology and Immunology, Faculty of Pharmacy, Cairo UniversityAbstract Background Reports are available on cross-resistance between antibiotics and biocides. We evaluated the effect of povidone-iodine (PVP-I) and propanol-based mecetronium ethyl sulphate (PBM) on resistance development, antibiotics cross-resistance, and virulence in Staphylococcus aureus. Methods The minimum inhibitory concentration (MIC) of PVP-I and PBM were determined against S. aureus ATCC 25923 using the agar-dilution method. Staphylococcus aureus ATCC 25923 was subjected to subinhibitory concentrations of the tested biocides in ten consecutive passages followed by five passages in a biocide-free medium; MIC was determined after each passage and after the fifth passage in the biocide-free medium. The developed resistant mutant was tested for cross-resistance to different antibiotics using Kirby-Bauer disk diffusion method. Antibiotic susceptibility profiles as well as biocides’ MIC were determined for 97 clinical S. aureus isolates. Isolates were categorized into susceptible and resistant to the tested biocides based on MIC distribution pattern. The virulence of the biocide-resistant mutant and the effect of subinhibitory concentrations of biocides on virulence (biofilm formation, hemolysin activity, and expression of virulence-related genes) were tested. Results PVP-I and PBM MIC were 5000 μg/mL and 664 μg/mL. No resistance developed to PVP-I but a 128-fold increase in PBM MIC was recorded, by repeated exposure. The developed PBM-resistant mutant acquired resistance to penicillin, cefoxitin, and ciprofloxacin. No clinical isolates were PVP-I-resistant while 48.5% were PBM-resistant. PBM-resistant isolates were more significantly detected among multidrug-resistant isolates. PVP-I subinhibitory concentrations (¼ and ½ of MIC) completely inhibited biofilm formation and significantly reduced hemolysin activity (7% and 0.28%, respectively). However, subinhibitory concentrations of PBM caused moderate reduction in biofilm activity and non-significant reduction in hemolysin activity. The ½ MIC of PVP-I significantly reduced the expression of hla, ebps, eno, fib, icaA, and icaD genes. The virulence of the biocide-resistant mutant was similar to that of parent strain. Conclusion PVP-I is a highly recommended antiseptic for use in healthcare settings to control the evolution of high-risk clones. Exposure to PVP-I causes no resistance-development risk in S. aureus, with virulence inhibition by subinhibitory concentrations. Also, special protocols need to be followed during PBM use in hospitals to avoid the selection of resistant strains.https://doi.org/10.1186/s13756-022-01178-9AntibioticsBiocidesBiofilmHemolysinPovidone-iodinePropanol-based mecetronium ethyl sulphate
spellingShingle Nada A. Barakat
Salwa A. Rasmy
Alaa El-Dien M. S. Hosny
Mona T. Kashef
Effect of povidone-iodine and propanol-based mecetronium ethyl sulphate on antimicrobial resistance and virulence in Staphylococcus aureus
Antimicrobial Resistance and Infection Control
Antibiotics
Biocides
Biofilm
Hemolysin
Povidone-iodine
Propanol-based mecetronium ethyl sulphate
title Effect of povidone-iodine and propanol-based mecetronium ethyl sulphate on antimicrobial resistance and virulence in Staphylococcus aureus
title_full Effect of povidone-iodine and propanol-based mecetronium ethyl sulphate on antimicrobial resistance and virulence in Staphylococcus aureus
title_fullStr Effect of povidone-iodine and propanol-based mecetronium ethyl sulphate on antimicrobial resistance and virulence in Staphylococcus aureus
title_full_unstemmed Effect of povidone-iodine and propanol-based mecetronium ethyl sulphate on antimicrobial resistance and virulence in Staphylococcus aureus
title_short Effect of povidone-iodine and propanol-based mecetronium ethyl sulphate on antimicrobial resistance and virulence in Staphylococcus aureus
title_sort effect of povidone iodine and propanol based mecetronium ethyl sulphate on antimicrobial resistance and virulence in staphylococcus aureus
topic Antibiotics
Biocides
Biofilm
Hemolysin
Povidone-iodine
Propanol-based mecetronium ethyl sulphate
url https://doi.org/10.1186/s13756-022-01178-9
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