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Understanding development of jugular bulb stenosis in vein of galen malformations: identifying metrics of complex flow dynamics in the cerebral venous vasculature of infants

Introduction: Computational fluid dynamics (CFD) assess biological systems based on specific boundary conditions. We propose modeling more advanced hemodynamic metrics, such as core line length (CL) and critical points which characterize complexity of flow in the context of cerebral vasculature, and...

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Autores principales: Hadad, Sara, Rangwala, Shivani D., Stout, Jeffrey N., Mut, Fernando, Orbach, Darren B., Cebral, Juan R., See, Alfred P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10236198/
https://www.ncbi.nlm.nih.gov/pubmed/37275225
http://dx.doi.org/10.3389/fphys.2023.1113034
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author Hadad, Sara
Rangwala, Shivani D.
Stout, Jeffrey N.
Mut, Fernando
Orbach, Darren B.
Cebral, Juan R.
See, Alfred P.
author_facet Hadad, Sara
Rangwala, Shivani D.
Stout, Jeffrey N.
Mut, Fernando
Orbach, Darren B.
Cebral, Juan R.
See, Alfred P.
author_sort Hadad, Sara
collection PubMed
description Introduction: Computational fluid dynamics (CFD) assess biological systems based on specific boundary conditions. We propose modeling more advanced hemodynamic metrics, such as core line length (CL) and critical points which characterize complexity of flow in the context of cerebral vasculature, and specifically cerebral veins during the physiologically evolving early neonatal state of vein of Galen malformations (VOGM). CFD has not been applied to the study of arteriovenous shunting in Vein of Galen Malformations but could help illustrate the pathophysiology of this malformation. Methods: Three neonatal patients with VOGM at Boston Children’s Hospital met inclusion criteria for this study. Structural MRI data was segmented to generate a mesh of the VOGM and venous outflow. Boundary condition flow velocity was derived from PC-MR sequences with arterial and venous dual velocity encoding. The mesh and boundary conditions were applied to model the cerebral venous flow. We computed flow variables including mean wall shear stress (WSSmean), mean OSI, CL, and the mean number of critical points (nCrPointsmean) for each patient specific model. A critical point is defined as the location where the shear stress vector field is zero (stationary point) and can be used to describe complexity of flow. Results: The division of flow into the left and right venous outflow was comparable between PC-MR and CFD modeling. A high complexity recirculating flow pattern observed on PC-MR was also identified on CFD modeling. Regions of similar WSSmean and OSImean (<1.3 fold) in the left and right venous outflow channels of a single patient have several-fold magnitude difference in higher order hemodynamic metrics (> 3.3 fold CL, > 1.7 fold nCrPointsmean). Specifically, the side which developed JBS in each model had greater nCrPointsmean compared to the jugular bulb with no stenosis (VOGM1: 4.49 vs. 2.53, VOGM2: 1.94 vs. 0, VOGM3: 1 vs. 0). Biologically, these regions had subsequently divergent development, with increased complexity of flow associating with venous stenosis. Discussion: Advanced metrics of flow complexity identified in computational models may reflect observed flow phenomena not fully characterized by primary or secondary hemodynamic parameters. These advanced metrics may indicate physiological states that impact development of jugular bulb stenosis in VOGM.
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spelling pubmed-102361982023-06-03 Understanding development of jugular bulb stenosis in vein of galen malformations: identifying metrics of complex flow dynamics in the cerebral venous vasculature of infants Hadad, Sara Rangwala, Shivani D. Stout, Jeffrey N. Mut, Fernando Orbach, Darren B. Cebral, Juan R. See, Alfred P. Front Physiol Physiology Introduction: Computational fluid dynamics (CFD) assess biological systems based on specific boundary conditions. We propose modeling more advanced hemodynamic metrics, such as core line length (CL) and critical points which characterize complexity of flow in the context of cerebral vasculature, and specifically cerebral veins during the physiologically evolving early neonatal state of vein of Galen malformations (VOGM). CFD has not been applied to the study of arteriovenous shunting in Vein of Galen Malformations but could help illustrate the pathophysiology of this malformation. Methods: Three neonatal patients with VOGM at Boston Children’s Hospital met inclusion criteria for this study. Structural MRI data was segmented to generate a mesh of the VOGM and venous outflow. Boundary condition flow velocity was derived from PC-MR sequences with arterial and venous dual velocity encoding. The mesh and boundary conditions were applied to model the cerebral venous flow. We computed flow variables including mean wall shear stress (WSSmean), mean OSI, CL, and the mean number of critical points (nCrPointsmean) for each patient specific model. A critical point is defined as the location where the shear stress vector field is zero (stationary point) and can be used to describe complexity of flow. Results: The division of flow into the left and right venous outflow was comparable between PC-MR and CFD modeling. A high complexity recirculating flow pattern observed on PC-MR was also identified on CFD modeling. Regions of similar WSSmean and OSImean (<1.3 fold) in the left and right venous outflow channels of a single patient have several-fold magnitude difference in higher order hemodynamic metrics (> 3.3 fold CL, > 1.7 fold nCrPointsmean). Specifically, the side which developed JBS in each model had greater nCrPointsmean compared to the jugular bulb with no stenosis (VOGM1: 4.49 vs. 2.53, VOGM2: 1.94 vs. 0, VOGM3: 1 vs. 0). Biologically, these regions had subsequently divergent development, with increased complexity of flow associating with venous stenosis. Discussion: Advanced metrics of flow complexity identified in computational models may reflect observed flow phenomena not fully characterized by primary or secondary hemodynamic parameters. These advanced metrics may indicate physiological states that impact development of jugular bulb stenosis in VOGM. Frontiers Media S.A. 2023-05-10 /pmc/articles/PMC10236198/ /pubmed/37275225 http://dx.doi.org/10.3389/fphys.2023.1113034 Text en Copyright © 2023 Hadad, Rangwala, Stout, Mut, Orbach, Cebral and See. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Hadad, Sara
Rangwala, Shivani D.
Stout, Jeffrey N.
Mut, Fernando
Orbach, Darren B.
Cebral, Juan R.
See, Alfred P.
Understanding development of jugular bulb stenosis in vein of galen malformations: identifying metrics of complex flow dynamics in the cerebral venous vasculature of infants
title Understanding development of jugular bulb stenosis in vein of galen malformations: identifying metrics of complex flow dynamics in the cerebral venous vasculature of infants
title_full Understanding development of jugular bulb stenosis in vein of galen malformations: identifying metrics of complex flow dynamics in the cerebral venous vasculature of infants
title_fullStr Understanding development of jugular bulb stenosis in vein of galen malformations: identifying metrics of complex flow dynamics in the cerebral venous vasculature of infants
title_full_unstemmed Understanding development of jugular bulb stenosis in vein of galen malformations: identifying metrics of complex flow dynamics in the cerebral venous vasculature of infants
title_short Understanding development of jugular bulb stenosis in vein of galen malformations: identifying metrics of complex flow dynamics in the cerebral venous vasculature of infants
title_sort understanding development of jugular bulb stenosis in vein of galen malformations: identifying metrics of complex flow dynamics in the cerebral venous vasculature of infants
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10236198/
https://www.ncbi.nlm.nih.gov/pubmed/37275225
http://dx.doi.org/10.3389/fphys.2023.1113034
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