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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 airbiofilm 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.

Experimental data showed that high-speed micro-sprays can effectively disrupt biofilms on their support substratum, producing a variety of dynamic reactions such as elongation, displacement, ripples formation and fluidization. However, the mechanics underlying the impact of high-speed turbulent flows on biofilm structure is complex in 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 travelling waves from the impact site. Our findings suggest that rapid shear-thinning in the biofilm reproduces dynamics under very high shear flows that elasticity can be neglected under these conditions, behaving the biofilm as a Newtonian fluid. A parametric sensitivity study confirmed that both applied force intensity (i.e. high jet-nozzle air velocity) and biofilm properties (i.e. low viscosity, low air-biofilm surface tension and thickness) intensify biofilm disruption, by generating large interfacial instabilities.IMPORTANCEKnowledge 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 ripples formation and fluid-biofilm mixing. These findings have important implications for the rational design of new biofilms 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.