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The role of leptomeningeal collaterals in redistributing blood flow during stroke


Epp, Robert; Glück, Chaim; Binder, Nadine Felizitas; El Amki, Mohamad; Weber, Bruno; Wegener, Susanne; Jenny, Patrick; Schmid, Franca (2023). The role of leptomeningeal collaterals in redistributing blood flow during stroke. PLoS Computational Biology, 19(10):e1011496.

Abstract

Leptomeningeal collaterals (LMCs) connect the main cerebral arteries and provide alternative pathways for blood flow during ischaemic stroke. This is beneficial for reducing infarct size and reperfusion success after treatment. However, a better understanding of how LMCs affect blood flow distribution is indispensable to improve therapeutic strategies. Here, we present a novel in silico approach that incorporates case-specific in vivo data into a computational model to simulate blood flow in large semi-realistic microvascular networks from two different mouse strains, characterised by having many and almost no LMCs between middle and anterior cerebral artery (MCA, ACA) territories. This framework is unique because our simulations are directly aligned with in vivo data. Moreover, it allows us to analyse perfusion characteristics quantitatively across all vessel types and for networks with no, few and many LMCs. We show that the occlusion of the MCA directly caused a redistribution of blood that was characterised by increased flow in LMCs. Interestingly, the improved perfusion of MCA-sided microvessels after dilating LMCs came at the cost of a reduced blood supply in other brain areas. This effect was enhanced in regions close to the watershed line and when the number of LMCs was increased. Additional dilations of surface and penetrating arteries after stroke improved perfusion across the entire vasculature and partially recovered flow in the obstructed region, especially in networks with many LMCs, which further underlines the role of LMCs during stroke.

Abstract

Leptomeningeal collaterals (LMCs) connect the main cerebral arteries and provide alternative pathways for blood flow during ischaemic stroke. This is beneficial for reducing infarct size and reperfusion success after treatment. However, a better understanding of how LMCs affect blood flow distribution is indispensable to improve therapeutic strategies. Here, we present a novel in silico approach that incorporates case-specific in vivo data into a computational model to simulate blood flow in large semi-realistic microvascular networks from two different mouse strains, characterised by having many and almost no LMCs between middle and anterior cerebral artery (MCA, ACA) territories. This framework is unique because our simulations are directly aligned with in vivo data. Moreover, it allows us to analyse perfusion characteristics quantitatively across all vessel types and for networks with no, few and many LMCs. We show that the occlusion of the MCA directly caused a redistribution of blood that was characterised by increased flow in LMCs. Interestingly, the improved perfusion of MCA-sided microvessels after dilating LMCs came at the cost of a reduced blood supply in other brain areas. This effect was enhanced in regions close to the watershed line and when the number of LMCs was increased. Additional dilations of surface and penetrating arteries after stroke improved perfusion across the entire vasculature and partially recovered flow in the obstructed region, especially in networks with many LMCs, which further underlines the role of LMCs during stroke.

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Item Type:Journal Article, refereed, original work
Communities & Collections:04 Faculty of Medicine > University Hospital Zurich > Clinic for Neurology
04 Faculty of Medicine > Institute of Pharmacology and Toxicology
07 Faculty of Science > Institute of Pharmacology and Toxicology
Dewey Decimal Classification:610 Medicine & health
570 Life sciences; biology
Scopus Subject Areas:Life Sciences > Ecology, Evolution, Behavior and Systematics
Physical Sciences > Modeling and Simulation
Physical Sciences > Ecology
Life Sciences > Molecular Biology
Life Sciences > Genetics
Life Sciences > Cellular and Molecular Neuroscience
Physical Sciences > Computational Theory and Mathematics
Uncontrolled Keywords:Computational Theory and Mathematics, Cellular and Molecular Neuroscience, Genetics, Molecular Biology, Ecology, Modeling and Simulation, Ecology, Evolution, Behavior and Systematics
Language:English
Date:23 October 2023
Deposited On:18 Dec 2023 13:46
Last Modified:29 Jun 2024 01:40
Publisher:Public Library of Science (PLoS)
ISSN:1553-734X
OA Status:Gold
Free access at:Publisher DOI. An embargo period may apply.
Publisher DOI:https://doi.org/10.1371/journal.pcbi.1011496
PubMed ID:37871109
Project Information:
  • : FunderSNSF
  • : Grant ID166707
  • : Project TitleThe role of capillary diameter adaption on the cerebral microcirculation
  • : FunderSNSF
  • : Grant ID166707
  • : Project TitleThe role of capillary diameter adaption on the cerebral microcirculation
  • : FunderSNSF
  • : Grant ID166707
  • : Project TitleThe role of capillary diameter adaption on the cerebral microcirculation
  • : FunderEidgenössische Technische Hochschule Zürich
  • : Grant ID
  • : Project Title
  • : FunderEidgenössische Technische Hochschule Zürich
  • : Grant ID
  • : Project Title
  • : FunderEidgenössische Technische Hochschule Zürich
  • : Grant ID
  • : Project Title
  • : FunderSNSF
  • : Grant ID202192
  • : Project TitleEnergy Supply in Whole Brain Microvascular Networks in Health and Disease - Quantifying the Relevance of Small-Scale Disturbances
  • Content: Published Version
  • Language: English
  • Licence: Creative Commons: Attribution 4.0 International (CC BY 4.0)