Impact of mucus and biofilm on antimicrobial photodynamic therapy: Evaluation using Ruthenium(II) complexes

The biofilm lifestyle of bacterial pathogens is a hallmark of chronic lung infections such as in cystic fibrosis (CF) patients. Bacterial adaptation to the complex conditions in CF-affected lungs and repeated antibiotherapies lead to increasingly tolerant and hard-to-treat biofilms. In the context o...

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Main Authors: Raphaëlle Youf, Rosy Ghanem, Adeel Nasir, Gilles Lemercier, Tristan Montier, Tony Le Gall
Format: Article
Language:English
Published: Elsevier 2023-12-01
Series:Biofilm
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2590207523000102
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author Raphaëlle Youf
Rosy Ghanem
Adeel Nasir
Gilles Lemercier
Tristan Montier
Tony Le Gall
author_facet Raphaëlle Youf
Rosy Ghanem
Adeel Nasir
Gilles Lemercier
Tristan Montier
Tony Le Gall
author_sort Raphaëlle Youf
collection DOAJ
description The biofilm lifestyle of bacterial pathogens is a hallmark of chronic lung infections such as in cystic fibrosis (CF) patients. Bacterial adaptation to the complex conditions in CF-affected lungs and repeated antibiotherapies lead to increasingly tolerant and hard-to-treat biofilms. In the context of growing antimicrobial resistance and restricted therapeutic options, antimicrobial photodynamic therapy (aPDT) shows great promise as an alternative to conventional antimicrobial modalities. Typically, aPDT consists in irradiating a non-toxic photosensitizer (PS) to generate reactive oxygen species (ROS), which kill pathogens in the surrounding environment. In a previous study, we reported that some ruthenium (II) complexes ([Ru(II)]) can mediate potent photodynamic inactivation (PDI) against planktonic cultures of Pseudomonas aeruginosa and Staphylococcus aureus clinical isolates. In the present work, [Ru(II)] were further assayed to evaluate their ability to photo-inactivate such bacteria under more complex experimental conditions better recapitulating the microenvironment in lung infected airways. Bacterial PDI was tentatively correlated with the properties of [Ru(II)] in biofilms, in mucus, and following diffusion across the latter. Altogether, the results obtained demonstrate the negative impacting role of mucus and biofilm components on [Ru(II)]-mediated PDT, following different possible mechanisms of action. Technical limitations were also identified that may be overcome, making this report a pilot for other similar studies. In conclusion, [Ru(II)] may be subjected to specific chemical engineering and/or drug formulation to adapt their properties to the harsh micro-environmental conditions of the infected respiratory tract.
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spelling doaj.art-082d4da7cf9c4997b8e1783f53de0bed2023-06-19T04:29:32ZengElsevierBiofilm2590-20752023-12-015100113Impact of mucus and biofilm on antimicrobial photodynamic therapy: Evaluation using Ruthenium(II) complexesRaphaëlle Youf0Rosy Ghanem1Adeel Nasir2Gilles Lemercier3Tristan Montier4Tony Le Gall5Inserm, Univ Brest, EFS, UMR 1078, GGB, F-29200, Brest, FranceInserm, Univ Brest, EFS, UMR 1078, GGB, F-29200, Brest, France; CHU de Brest, Service de Génétique Médicale et de Biologie de la Reproduction, 29200, Brest, FranceInserm, Univ Brest, EFS, UMR 1078, GGB, F-29200, Brest, FranceUniversité de Reims Champagne-Ardenne, UMR CNRS 7312, BP 1039, CEDEX 2, 51687, Reims, FranceInserm, Univ Brest, EFS, UMR 1078, GGB, F-29200, Brest, France; CHU de Brest, Service de Génétique Médicale et de Biologie de la Reproduction, 29200, Brest, France; CHU de Brest, Centre de Référence des Maladies Rares Maladies Neuromusculaires, 29200, Brest, FranceInserm, Univ Brest, EFS, UMR 1078, GGB, F-29200, Brest, France; Corresponding author. Inserm, UMR 1078, Génétique, Génomique fonctionnelle et Biotechnologies, GTCA Team, Faculté de Médecine (UBO), 22 avenue Camille Desmoulins, 29238, Brest, France.The biofilm lifestyle of bacterial pathogens is a hallmark of chronic lung infections such as in cystic fibrosis (CF) patients. Bacterial adaptation to the complex conditions in CF-affected lungs and repeated antibiotherapies lead to increasingly tolerant and hard-to-treat biofilms. In the context of growing antimicrobial resistance and restricted therapeutic options, antimicrobial photodynamic therapy (aPDT) shows great promise as an alternative to conventional antimicrobial modalities. Typically, aPDT consists in irradiating a non-toxic photosensitizer (PS) to generate reactive oxygen species (ROS), which kill pathogens in the surrounding environment. In a previous study, we reported that some ruthenium (II) complexes ([Ru(II)]) can mediate potent photodynamic inactivation (PDI) against planktonic cultures of Pseudomonas aeruginosa and Staphylococcus aureus clinical isolates. In the present work, [Ru(II)] were further assayed to evaluate their ability to photo-inactivate such bacteria under more complex experimental conditions better recapitulating the microenvironment in lung infected airways. Bacterial PDI was tentatively correlated with the properties of [Ru(II)] in biofilms, in mucus, and following diffusion across the latter. Altogether, the results obtained demonstrate the negative impacting role of mucus and biofilm components on [Ru(II)]-mediated PDT, following different possible mechanisms of action. Technical limitations were also identified that may be overcome, making this report a pilot for other similar studies. In conclusion, [Ru(II)] may be subjected to specific chemical engineering and/or drug formulation to adapt their properties to the harsh micro-environmental conditions of the infected respiratory tract.http://www.sciencedirect.com/science/article/pii/S2590207523000102Antimicrobial photodynamic therapyBiofilmMucusPhotodynamic inactivationPhotosensitizerPulmonary infection
spellingShingle Raphaëlle Youf
Rosy Ghanem
Adeel Nasir
Gilles Lemercier
Tristan Montier
Tony Le Gall
Impact of mucus and biofilm on antimicrobial photodynamic therapy: Evaluation using Ruthenium(II) complexes
Biofilm
Antimicrobial photodynamic therapy
Biofilm
Mucus
Photodynamic inactivation
Photosensitizer
Pulmonary infection
title Impact of mucus and biofilm on antimicrobial photodynamic therapy: Evaluation using Ruthenium(II) complexes
title_full Impact of mucus and biofilm on antimicrobial photodynamic therapy: Evaluation using Ruthenium(II) complexes
title_fullStr Impact of mucus and biofilm on antimicrobial photodynamic therapy: Evaluation using Ruthenium(II) complexes
title_full_unstemmed Impact of mucus and biofilm on antimicrobial photodynamic therapy: Evaluation using Ruthenium(II) complexes
title_short Impact of mucus and biofilm on antimicrobial photodynamic therapy: Evaluation using Ruthenium(II) complexes
title_sort impact of mucus and biofilm on antimicrobial photodynamic therapy evaluation using ruthenium ii complexes
topic Antimicrobial photodynamic therapy
Biofilm
Mucus
Photodynamic inactivation
Photosensitizer
Pulmonary infection
url http://www.sciencedirect.com/science/article/pii/S2590207523000102
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