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Origanum vulgare ethanolic extracts as a promising source of compounds with antimicrobial, anti-biofilm, and anti-virulence activity against dental plaque bacteria

Dental caries and periodontal diseases remain a challenge for oral health, especially given the lack of effective and safe treatment options that are currently available. Against the backdrop of an ongoing antimicrobial resistance crisis, a renewed interest in traditional medicinal plants as a poten...

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Autores principales: Idir, Fouzia, Van Ginneken, Sybren, Coppola, Guglielmo A., Grenier, Daniel, Steenackers, Hans P., Bendali, Farida
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9668103/
https://www.ncbi.nlm.nih.gov/pubmed/36406439
http://dx.doi.org/10.3389/fmicb.2022.999839
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author Idir, Fouzia
Van Ginneken, Sybren
Coppola, Guglielmo A.
Grenier, Daniel
Steenackers, Hans P.
Bendali, Farida
author_facet Idir, Fouzia
Van Ginneken, Sybren
Coppola, Guglielmo A.
Grenier, Daniel
Steenackers, Hans P.
Bendali, Farida
author_sort Idir, Fouzia
collection PubMed
description Dental caries and periodontal diseases remain a challenge for oral health, especially given the lack of effective and safe treatment options that are currently available. Against the backdrop of an ongoing antimicrobial resistance crisis, a renewed interest in traditional medicinal plants as a potential source of new bioactive compounds has surfaced. In this context, we systematically screened the antimicrobial and anti-biofilm activities of both ethanolic and aqueous extracts of nine Algerian medicinal plants (Artemisia herba alba, Centaurium erythraea, Juglans regia, Laurus nobilis, Matricaria recutita, Mentha pulegium, Mentha piperita, Origanum vulgare and Taraxacum officinale). To evaluate the activity spectrum of the extracts, the screening was carried out against an extensive collection of Streptococcus, Enterococcus and Lacticaseibacillus isolates recovered from dental plaques of Algerian patients. Broad-spectrum antimicrobial and anti-biofilm properties were observed, especially among ethanolic extracts, which marks them as a promising source for bioactive compounds to control oral biofilms. The ethanolic extract of O. vulgare, which showed the most promising effects in the initial screening, was further characterized. We first verified the biocompatibility of this extract using human oral keratinocytes and selected a range of non-cytotoxic concentrations (0.195–0.781 mg/ml) to further validate its anti-biofilm and anti-virulence potential. At these concentrations, the extract not only prevented biofilm formation (10.04 ± 0.75–87.91 ± 9.08% of reduction) of most dental plaque isolates on a polystyrene surface, but also significantly reduced their adherence to hydroxyapatite (34.58 ± 9.09–62.77 ± 0.95%). Moreover, the extract showed curative potential against mature biofilms grown under conditions mimicking the oral niche. In addition to its anti-biofilm properties, we observed an inhibition of glucosyltransferase activity, a reduction in acidogenesis and a downregulation in the expression of multiple virulence-associated genes for extract-treated samples. Since anti-virulence properties are more robust to the development of resistance, they provide an attractive complementation to the antimicrobial activities of the extract. Thymol was identified as an important active compound of the extract using GC–MS analysis, but synergy with other compounds was also detected, suggesting a potential advantage of using the whole extract over purified thymol. Further research into the bioactive compounds of the O. vulgare ethanolic extract could yield novel products to fight dental caries.
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spelling pubmed-96681032022-11-17 Origanum vulgare ethanolic extracts as a promising source of compounds with antimicrobial, anti-biofilm, and anti-virulence activity against dental plaque bacteria Idir, Fouzia Van Ginneken, Sybren Coppola, Guglielmo A. Grenier, Daniel Steenackers, Hans P. Bendali, Farida Front Microbiol Microbiology Dental caries and periodontal diseases remain a challenge for oral health, especially given the lack of effective and safe treatment options that are currently available. Against the backdrop of an ongoing antimicrobial resistance crisis, a renewed interest in traditional medicinal plants as a potential source of new bioactive compounds has surfaced. In this context, we systematically screened the antimicrobial and anti-biofilm activities of both ethanolic and aqueous extracts of nine Algerian medicinal plants (Artemisia herba alba, Centaurium erythraea, Juglans regia, Laurus nobilis, Matricaria recutita, Mentha pulegium, Mentha piperita, Origanum vulgare and Taraxacum officinale). To evaluate the activity spectrum of the extracts, the screening was carried out against an extensive collection of Streptococcus, Enterococcus and Lacticaseibacillus isolates recovered from dental plaques of Algerian patients. Broad-spectrum antimicrobial and anti-biofilm properties were observed, especially among ethanolic extracts, which marks them as a promising source for bioactive compounds to control oral biofilms. The ethanolic extract of O. vulgare, which showed the most promising effects in the initial screening, was further characterized. We first verified the biocompatibility of this extract using human oral keratinocytes and selected a range of non-cytotoxic concentrations (0.195–0.781 mg/ml) to further validate its anti-biofilm and anti-virulence potential. At these concentrations, the extract not only prevented biofilm formation (10.04 ± 0.75–87.91 ± 9.08% of reduction) of most dental plaque isolates on a polystyrene surface, but also significantly reduced their adherence to hydroxyapatite (34.58 ± 9.09–62.77 ± 0.95%). Moreover, the extract showed curative potential against mature biofilms grown under conditions mimicking the oral niche. In addition to its anti-biofilm properties, we observed an inhibition of glucosyltransferase activity, a reduction in acidogenesis and a downregulation in the expression of multiple virulence-associated genes for extract-treated samples. Since anti-virulence properties are more robust to the development of resistance, they provide an attractive complementation to the antimicrobial activities of the extract. Thymol was identified as an important active compound of the extract using GC–MS analysis, but synergy with other compounds was also detected, suggesting a potential advantage of using the whole extract over purified thymol. Further research into the bioactive compounds of the O. vulgare ethanolic extract could yield novel products to fight dental caries. Frontiers Media S.A. 2022-11-02 /pmc/articles/PMC9668103/ /pubmed/36406439 http://dx.doi.org/10.3389/fmicb.2022.999839 Text en Copyright © 2022 Idir, Van Ginneken, Coppola, Grenier, Steenackers and Bendali. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Idir, Fouzia
Van Ginneken, Sybren
Coppola, Guglielmo A.
Grenier, Daniel
Steenackers, Hans P.
Bendali, Farida
Origanum vulgare ethanolic extracts as a promising source of compounds with antimicrobial, anti-biofilm, and anti-virulence activity against dental plaque bacteria
title Origanum vulgare ethanolic extracts as a promising source of compounds with antimicrobial, anti-biofilm, and anti-virulence activity against dental plaque bacteria
title_full Origanum vulgare ethanolic extracts as a promising source of compounds with antimicrobial, anti-biofilm, and anti-virulence activity against dental plaque bacteria
title_fullStr Origanum vulgare ethanolic extracts as a promising source of compounds with antimicrobial, anti-biofilm, and anti-virulence activity against dental plaque bacteria
title_full_unstemmed Origanum vulgare ethanolic extracts as a promising source of compounds with antimicrobial, anti-biofilm, and anti-virulence activity against dental plaque bacteria
title_short Origanum vulgare ethanolic extracts as a promising source of compounds with antimicrobial, anti-biofilm, and anti-virulence activity against dental plaque bacteria
title_sort origanum vulgare ethanolic extracts as a promising source of compounds with antimicrobial, anti-biofilm, and anti-virulence activity against dental plaque bacteria
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9668103/
https://www.ncbi.nlm.nih.gov/pubmed/36406439
http://dx.doi.org/10.3389/fmicb.2022.999839
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