Computational and Experimental Investigation of Biofilm Disruption Dynamics Induced by High-Velocity Gas Jet Impingement

ABSTRACT Experimental data showed that high-speed microsprays can effectively disrupt biofilms on their support substratum, producing a variety of dynamic reactions such as elongation, displacement, ripple formation, and fluidization. However, the mechanics underlying the impact of high-speed turbul...

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Autores principales:	Lledó Prades, Stefania Fabbri, Antonio D. Dorado, Xavier Gamisans, Paul Stoodley, Cristian Picioreanu
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	non-Newtonian fluid flow computational fluid dynamics turbulence high-velocity air jets ripples Streptococcus mutans Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/cde9335f70764002afbaa9eaaab1cac7
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spelling	oai:doaj.org-article:cde9335f70764002afbaa9eaaab1cac72021-11-15T15:56:57ZComputational and Experimental Investigation of Biofilm Disruption Dynamics Induced by High-Velocity Gas Jet Impingement10.1128/mBio.02813-192150-7511https://doaj.org/article/cde9335f70764002afbaa9eaaab1cac72020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02813-19https://doaj.org/toc/2150-7511ABSTRACT Experimental data showed that high-speed microsprays can effectively disrupt biofilms on their support substratum, producing a variety of dynamic reactions such as elongation, displacement, ripple formation, and fluidization. However, the mechanics underlying the impact of high-speed turbulent flows on biofilm structure is complex under such extreme conditions, since direct measurements of viscosity at these high shear rates are not possible using dynamic testing instruments. Here, we used computational fluid dynamics simulations to assess the complex fluid interactions of ripple patterning produced by high-speed turbulent air jets impacting perpendicular to the surface of Streptococcus mutans biofilms, a dental pathogen causing caries, captured by high-speed imaging. The numerical model involved a two-phase flow of air over a non-Newtonian biofilm, whose viscosity as a function of shear rate was estimated using the Herschel-Bulkley model. The simulation suggested that inertial, shear, and interfacial tension forces governed biofilm disruption by the air jet. Additionally, the high shear rates generated by the jet impacts coupled with shear-thinning biofilm property resulted in rapid liquefaction (within milliseconds) of the biofilm, followed by surface instability and traveling waves from the impact site. Our findings suggest that rapid shear thinning under very high shear flows causes the biofilm to behave like a fluid and elasticity can be neglected. A parametric sensitivity study confirmed that both applied force intensity (i.e., high jet nozzle air velocity) and biofilm properties (i.e., low viscosity and low air-biofilm surface tension and thickness) intensify biofilm disruption by generating large interfacial instabilities. IMPORTANCE Knowledge of mechanisms promoting disruption though mechanical forces is essential in optimizing biofilm control strategies which rely on fluid shear. Our results provide insight into how biofilm disruption dynamics is governed by applied forces and fluid properties, revealing a mechanism for ripple formation and fluid-biofilm mixing. These findings have important implications for the rational design of new biofilm cleaning strategies with fluid jets, such as determining optimal parameters (e.g., jet velocity and position) to remove the biofilm from a certain zone (e.g., in dental hygiene or debridement of surgical site infections) or using antimicrobial agents which could increase the interfacial area available for exchange, as well as causing internal mixing within the biofilm matrix, thus disrupting the localized microenvironment which is associated with antimicrobial tolerance. The developed model also has potential application in predicting drag and pressure drop caused by biofilms on bioreactor, pipeline, and ship hull surfaces.Lledó PradesStefania FabbriAntonio D. DoradoXavier GamisansPaul StoodleyCristian PicioreanuAmerican Society for Microbiologyarticlenon-Newtonian fluid flowcomputational fluid dynamicsturbulencehigh-velocity air jetsripplesStreptococcus mutansMicrobiologyQR1-502ENmBio, Vol 11, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	non-Newtonian fluid flow computational fluid dynamics turbulence high-velocity air jets ripples Streptococcus mutans Microbiology QR1-502
spellingShingle	non-Newtonian fluid flow computational fluid dynamics turbulence high-velocity air jets ripples Streptococcus mutans Microbiology QR1-502 Lledó Prades Stefania Fabbri Antonio D. Dorado Xavier Gamisans Paul Stoodley Cristian Picioreanu Computational and Experimental Investigation of Biofilm Disruption Dynamics Induced by High-Velocity Gas Jet Impingement
description	ABSTRACT Experimental data showed that high-speed microsprays can effectively disrupt biofilms on their support substratum, producing a variety of dynamic reactions such as elongation, displacement, ripple formation, and fluidization. However, the mechanics underlying the impact of high-speed turbulent flows on biofilm structure is complex under such extreme conditions, since direct measurements of viscosity at these high shear rates are not possible using dynamic testing instruments. Here, we used computational fluid dynamics simulations to assess the complex fluid interactions of ripple patterning produced by high-speed turbulent air jets impacting perpendicular to the surface of Streptococcus mutans biofilms, a dental pathogen causing caries, captured by high-speed imaging. The numerical model involved a two-phase flow of air over a non-Newtonian biofilm, whose viscosity as a function of shear rate was estimated using the Herschel-Bulkley model. The simulation suggested that inertial, shear, and interfacial tension forces governed biofilm disruption by the air jet. Additionally, the high shear rates generated by the jet impacts coupled with shear-thinning biofilm property resulted in rapid liquefaction (within milliseconds) of the biofilm, followed by surface instability and traveling waves from the impact site. Our findings suggest that rapid shear thinning under very high shear flows causes the biofilm to behave like a fluid and elasticity can be neglected. A parametric sensitivity study confirmed that both applied force intensity (i.e., high jet nozzle air velocity) and biofilm properties (i.e., low viscosity and low air-biofilm surface tension and thickness) intensify biofilm disruption by generating large interfacial instabilities. IMPORTANCE Knowledge of mechanisms promoting disruption though mechanical forces is essential in optimizing biofilm control strategies which rely on fluid shear. Our results provide insight into how biofilm disruption dynamics is governed by applied forces and fluid properties, revealing a mechanism for ripple formation and fluid-biofilm mixing. These findings have important implications for the rational design of new biofilm cleaning strategies with fluid jets, such as determining optimal parameters (e.g., jet velocity and position) to remove the biofilm from a certain zone (e.g., in dental hygiene or debridement of surgical site infections) or using antimicrobial agents which could increase the interfacial area available for exchange, as well as causing internal mixing within the biofilm matrix, thus disrupting the localized microenvironment which is associated with antimicrobial tolerance. The developed model also has potential application in predicting drag and pressure drop caused by biofilms on bioreactor, pipeline, and ship hull surfaces.
format	article
author	Lledó Prades Stefania Fabbri Antonio D. Dorado Xavier Gamisans Paul Stoodley Cristian Picioreanu
author_facet	Lledó Prades Stefania Fabbri Antonio D. Dorado Xavier Gamisans Paul Stoodley Cristian Picioreanu
author_sort	Lledó Prades
title	Computational and Experimental Investigation of Biofilm Disruption Dynamics Induced by High-Velocity Gas Jet Impingement
title_short	Computational and Experimental Investigation of Biofilm Disruption Dynamics Induced by High-Velocity Gas Jet Impingement
title_full	Computational and Experimental Investigation of Biofilm Disruption Dynamics Induced by High-Velocity Gas Jet Impingement
title_fullStr	Computational and Experimental Investigation of Biofilm Disruption Dynamics Induced by High-Velocity Gas Jet Impingement
title_full_unstemmed	Computational and Experimental Investigation of Biofilm Disruption Dynamics Induced by High-Velocity Gas Jet Impingement
title_sort	computational and experimental investigation of biofilm disruption dynamics induced by high-velocity gas jet impingement
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/cde9335f70764002afbaa9eaaab1cac7
work_keys_str_mv	AT lledoprades computationalandexperimentalinvestigationofbiofilmdisruptiondynamicsinducedbyhighvelocitygasjetimpingement AT stefaniafabbri computationalandexperimentalinvestigationofbiofilmdisruptiondynamicsinducedbyhighvelocitygasjetimpingement AT antonioddorado computationalandexperimentalinvestigationofbiofilmdisruptiondynamicsinducedbyhighvelocitygasjetimpingement AT xaviergamisans computationalandexperimentalinvestigationofbiofilmdisruptiondynamicsinducedbyhighvelocitygasjetimpingement AT paulstoodley computationalandexperimentalinvestigationofbiofilmdisruptiondynamicsinducedbyhighvelocitygasjetimpingement AT cristianpicioreanu computationalandexperimentalinvestigationofbiofilmdisruptiondynamicsinducedbyhighvelocitygasjetimpingement
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Computational and Experimental Investigation of Biofilm Disruption Dynamics Induced by High-Velocity Gas Jet Impingement

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