2019Frontiers in PhysiologyOpen access

Computational Network Modeling of Intranidal Hemodynamic Compartmentalization in a Theoretical Three-Dimensional Brain Arteriovenous Malformation

Mika Sarkin Jain, Huy M., Tarik F. Massoud

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Abstract

There are currently no in vivo techniques to accurately study dynamic equilibrium of blood flow within separate regions (compartments) of a large brain arteriovenous malformation (AVM) nidus. A greater understanding of this AVM compartmentalization, even if theoretical, would be useful for optimal planning of endovascular and multimodal AVM therapies. We aimed to develop a biomathematical AVM model for theoretical investigations of intranidal regions of increased mean intravascular pressure (Pmean) and flow representing hemodynamic compartments, upon simulated AVM superselective angiography (SSA). We constructed an AVM model as a theoretical electrical circuit containing four arterial feeders (AF1-AF4) and a three-dimensional nidus of 97 interconnected plexiform and fistulous components. We simulated SSA by increases in Pmean in each AF (with and without occlusion of all other AFs), and then used network analysis to establish resulting increases in Pmean and flow within each nidus vessel. We analyzed shifts in hemodynamic compartments consequent to increasing AF injection pressures. SSA simulated by increases of 10 mm Hg in AF1, AF2, AF3, or AF4 resulted in dissipation of Pmean over 38%, 66%, 76%, or 20% of the nidus, respectively, rising slightly with simultaneous occlusion of other AFs. We qualitatively analyzed shifting intranidal compartments consequent to varying injection pressures by mapping the hemodynamic changes onto the nidus network. Differences in extent of nidus filling upon SSA injections provide theoretical evidence that hemodynamic and angioarchitectural features help establish AVM nidus compartmentalization. This model will serve as a useful computational tool for further theoretical investigations of AVM embolotherapy strategies.

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There are currently no in vivo techniques to accurately study dynamic equilibrium of blood flow within separate regions (compartments) of a large brain arteriovenous malformation (AVM) nidus. A greater understanding of this AVM compartmentalization, even if theoretical, would be useful for optimal planning of endovascular and multimodal AVM therapies. We aimed to develop a biomathematical AVM model for theoretical investigations of intranidal regions of increased mean intravascular pressure (Pmean) and flow representing hemodynamic compartments, upon simulated AVM superselective angiography (SSA). We constructed an AVM model as a theoretical electrical circuit containing four arterial feeders (AF1-AF4) and a three-dimensional nidus of 97 interconnected plexiform and fistulous components. We simulated SSA by increases in Pmean in each AF (with and without occlusion of all other AFs), and then used network analysis to establish resulting increases in Pmean and flow within each nidus vessel. We analyzed shifts in hemodynamic compartments consequent to increasing AF injection pressures. SSA simulated by increases of 10 mm Hg in AF1, AF2, AF3, or AF4 resulted in dissipation of Pmean over 38%, 66%, 76%, or 20% of the nidus, respectively, rising slightly with simultaneous occlusion of other AFs. We qualitatively analyzed shifting intranidal compartments consequent to varying injection pressures by mapping the hemodynamic changes onto the nidus network. Differences in extent of nidus filling upon SSA injections provide theoretical evidence that hemodynamic and angioarchitectural features help establish AVM nidus compartmentalization. This model will serve as a useful computational tool for further theoretical investigations of AVM embolotherapy strategies.

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Available abstract

There are currently no in vivo techniques to accurately study dynamic equilibrium of blood flow within separate regions (compartments) of a large brain arteriovenous malformation (AVM) nidus. A greater understanding of this AVM compartmentalization, even if theoretical, would be useful for optimal planning of endovascular and multimodal AVM therapies. We aimed to develop a biomathematical AVM model for theoretical investigations of intranidal regions of increased mean intravascular pressure (Pmean) and flow representing hemodynamic compartments, upon simulated AVM superselective angiography (SSA). We constructed an AVM model as a theoretical electrical circuit containing four arterial feeders (AF1-AF4) and a three-dimensional nidus of 97 interconnected plexiform and fistulous components. We simulated SSA by increases in Pmean in each AF (with and without occlusion of all other AFs), and then used network analysis to establish resulting increases in Pmean and flow within each nidus vessel. We analyzed shifts in hemodynamic compartments consequent to increasing AF injection pressures. SSA simulated by increases of 10 mm Hg in AF1, AF2, AF3, or AF4 resulted in dissipation of Pmean over 38%, 66%, 76%, or 20% of the nidus, respectively, rising slightly with simultaneous occlusion of other AFs. We qualitatively analyzed shifting intranidal compartments consequent to varying injection pressures by mapping the hemodynamic changes onto the nidus network. Differences in extent of nidus filling upon SSA injections provide theoretical evidence that hemodynamic and angioarchitectural features help establish AVM nidus compartmentalization. This model will serve as a useful computational tool for further theoretical investigations of AVM embolotherapy strategies.

Key concepts: Medicine, Hemodynamics, Arteriovenous malformation, Compartmentalization (fire protection), Blood flow, Occlusion, Radiology, Cardiology

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