Phenotypic Adaptation to Antiseptics and Effects on Biofilm Formation Capacity and Antibiotic Resistance in Clinical Isolates of Early Colonizers in Dental Plaque

Despite the wide-spread use of antiseptics in dental practice and oral care products, there is little public awareness of potential risks associated with antiseptic resistance and potentially concomitant cross-resistance. Therefore, the aim of this study was to investigate potential phenotypic adapt...

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Main Authors: David L. Auer, Xiaojun Mao, Annette Carola Anderson, Denise Muehler, Annette Wittmer, Christiane von Ohle, Diana Wolff, Cornelia Frese, Karl-Anton Hiller, Tim Maisch, Wolfgang Buchalla, Elmar Hellwig, Ali Al-Ahmad, Fabian Cieplik
Format: Article
Language:English
Published: MDPI AG 2022-05-01
Series:Antibiotics
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Online Access:https://www.mdpi.com/2079-6382/11/5/688
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author David L. Auer
Xiaojun Mao
Annette Carola Anderson
Denise Muehler
Annette Wittmer
Christiane von Ohle
Diana Wolff
Cornelia Frese
Karl-Anton Hiller
Tim Maisch
Wolfgang Buchalla
Elmar Hellwig
Ali Al-Ahmad
Fabian Cieplik
author_facet David L. Auer
Xiaojun Mao
Annette Carola Anderson
Denise Muehler
Annette Wittmer
Christiane von Ohle
Diana Wolff
Cornelia Frese
Karl-Anton Hiller
Tim Maisch
Wolfgang Buchalla
Elmar Hellwig
Ali Al-Ahmad
Fabian Cieplik
author_sort David L. Auer
collection DOAJ
description Despite the wide-spread use of antiseptics in dental practice and oral care products, there is little public awareness of potential risks associated with antiseptic resistance and potentially concomitant cross-resistance. Therefore, the aim of this study was to investigate potential phenotypic adaptation in 177 clinical isolates of early colonizers of dental plaque (<i>Streptococcus</i>, <i>Actinomyces</i>, <i>Rothia</i> and <i>Veillonella</i> spp.) upon repeated exposure to subinhibitory concentrations of chlorhexidine digluconate (CHX) or cetylpyridinium chloride (CPC) over 10 passages using a modified microdilution method. Stability of phenotypic adaptation was re-evaluated after culture in antiseptic-free nutrient broth for 24 or 72 h. Strains showing 8-fold minimal inhibitory concentration (MIC)-increase were further examined regarding their biofilm formation capacity, phenotypic antibiotic resistance and presence of antibiotic resistance genes (ARGs). Eight-fold MIC-increases to CHX were detected in four <i>Streptococcus</i> isolates. These strains mostly exhibited significantly increased biofilm formation capacity compared to their respective wild-type strains. Phenotypic antibiotic resistance was detected to tetracycline and erythromycin, consistent with the detected ARGs. In conclusion, this study shows that clinical isolates of early colonizers of dental plaque can phenotypically adapt toward antiseptics such as CHX upon repeated exposure. The underlying mechanisms at genomic and transcriptomic levels need to be investigated in future studies.
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spelling doaj.art-21f895d1c2024931a33d696a06b49ab82023-11-23T09:49:43ZengMDPI AGAntibiotics2079-63822022-05-0111568810.3390/antibiotics11050688Phenotypic Adaptation to Antiseptics and Effects on Biofilm Formation Capacity and Antibiotic Resistance in Clinical Isolates of Early Colonizers in Dental PlaqueDavid L. Auer0Xiaojun Mao1Annette Carola Anderson2Denise Muehler3Annette Wittmer4Christiane von Ohle5Diana Wolff6Cornelia Frese7Karl-Anton Hiller8Tim Maisch9Wolfgang Buchalla10Elmar Hellwig11Ali Al-Ahmad12Fabian Cieplik13Department of Conservative Dentistry and Periodontology, University Hospital Regensburg, 93053 Regensburg, GermanyDepartment of Conservative Dentistry and Periodontology, University Hospital Regensburg, 93053 Regensburg, GermanyDepartment of Operative Dentistry and Periodontology, Center for Dental Medicine, Faculty of Medicine, University of Freiburg, 79085 Freiburg im Breisgau, GermanyDepartment of Conservative Dentistry and Periodontology, University Hospital Regensburg, 93053 Regensburg, GermanyInstitute of Medical Microbiology and Hygiene, Faculty of Medicine, University of Freiburg, 79085 Freiburg im Breisgau, GermanyDepartment of Conservative Dentistry, Periodontology and Endodontology, University Hospital Tübingen, 72076 Tübingen, GermanyDepartment of Conservative Dentistry, University Hospital Heidelberg, 69120 Heidelberg, GermanyDepartment of Conservative Dentistry, University Hospital Heidelberg, 69120 Heidelberg, GermanyDepartment of Conservative Dentistry and Periodontology, University Hospital Regensburg, 93053 Regensburg, GermanyDepartment of Dermatology, University Hospital Regensburg, 93053 Regensburg, GermanyDepartment of Conservative Dentistry and Periodontology, University Hospital Regensburg, 93053 Regensburg, GermanyDepartment of Operative Dentistry and Periodontology, Center for Dental Medicine, Faculty of Medicine, University of Freiburg, 79085 Freiburg im Breisgau, GermanyDepartment of Operative Dentistry and Periodontology, Center for Dental Medicine, Faculty of Medicine, University of Freiburg, 79085 Freiburg im Breisgau, GermanyDepartment of Conservative Dentistry and Periodontology, University Hospital Regensburg, 93053 Regensburg, GermanyDespite the wide-spread use of antiseptics in dental practice and oral care products, there is little public awareness of potential risks associated with antiseptic resistance and potentially concomitant cross-resistance. Therefore, the aim of this study was to investigate potential phenotypic adaptation in 177 clinical isolates of early colonizers of dental plaque (<i>Streptococcus</i>, <i>Actinomyces</i>, <i>Rothia</i> and <i>Veillonella</i> spp.) upon repeated exposure to subinhibitory concentrations of chlorhexidine digluconate (CHX) or cetylpyridinium chloride (CPC) over 10 passages using a modified microdilution method. Stability of phenotypic adaptation was re-evaluated after culture in antiseptic-free nutrient broth for 24 or 72 h. Strains showing 8-fold minimal inhibitory concentration (MIC)-increase were further examined regarding their biofilm formation capacity, phenotypic antibiotic resistance and presence of antibiotic resistance genes (ARGs). Eight-fold MIC-increases to CHX were detected in four <i>Streptococcus</i> isolates. These strains mostly exhibited significantly increased biofilm formation capacity compared to their respective wild-type strains. Phenotypic antibiotic resistance was detected to tetracycline and erythromycin, consistent with the detected ARGs. In conclusion, this study shows that clinical isolates of early colonizers of dental plaque can phenotypically adapt toward antiseptics such as CHX upon repeated exposure. The underlying mechanisms at genomic and transcriptomic levels need to be investigated in future studies.https://www.mdpi.com/2079-6382/11/5/688chlorhexidinecetylpyridinium chlorideantisepticbiocideresistanceadaptation
spellingShingle David L. Auer
Xiaojun Mao
Annette Carola Anderson
Denise Muehler
Annette Wittmer
Christiane von Ohle
Diana Wolff
Cornelia Frese
Karl-Anton Hiller
Tim Maisch
Wolfgang Buchalla
Elmar Hellwig
Ali Al-Ahmad
Fabian Cieplik
Phenotypic Adaptation to Antiseptics and Effects on Biofilm Formation Capacity and Antibiotic Resistance in Clinical Isolates of Early Colonizers in Dental Plaque
Antibiotics
chlorhexidine
cetylpyridinium chloride
antiseptic
biocide
resistance
adaptation
title Phenotypic Adaptation to Antiseptics and Effects on Biofilm Formation Capacity and Antibiotic Resistance in Clinical Isolates of Early Colonizers in Dental Plaque
title_full Phenotypic Adaptation to Antiseptics and Effects on Biofilm Formation Capacity and Antibiotic Resistance in Clinical Isolates of Early Colonizers in Dental Plaque
title_fullStr Phenotypic Adaptation to Antiseptics and Effects on Biofilm Formation Capacity and Antibiotic Resistance in Clinical Isolates of Early Colonizers in Dental Plaque
title_full_unstemmed Phenotypic Adaptation to Antiseptics and Effects on Biofilm Formation Capacity and Antibiotic Resistance in Clinical Isolates of Early Colonizers in Dental Plaque
title_short Phenotypic Adaptation to Antiseptics and Effects on Biofilm Formation Capacity and Antibiotic Resistance in Clinical Isolates of Early Colonizers in Dental Plaque
title_sort phenotypic adaptation to antiseptics and effects on biofilm formation capacity and antibiotic resistance in clinical isolates of early colonizers in dental plaque
topic chlorhexidine
cetylpyridinium chloride
antiseptic
biocide
resistance
adaptation
url https://www.mdpi.com/2079-6382/11/5/688
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