Pulsatile cerebral paraarterial flow by peristalsis, pressure and directional resistance

Abstract Background A glymphatic system has been proposed that comprises flow that enters along cerebral paraarterial channels between the artery wall and the surrounding glial layer, continues through the parenchyma, and then exits along similar paravenous channels. The mechanism driving flow throu...

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Main Author: M. Keith Sharp
Format: Article
Language:English
Published: BMC 2023-06-01
Series:Fluids and Barriers of the CNS
Subjects:
Online Access:https://doi.org/10.1186/s12987-023-00445-0
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author M. Keith Sharp
author_facet M. Keith Sharp
author_sort M. Keith Sharp
collection DOAJ
description Abstract Background A glymphatic system has been proposed that comprises flow that enters along cerebral paraarterial channels between the artery wall and the surrounding glial layer, continues through the parenchyma, and then exits along similar paravenous channels. The mechanism driving flow through this system is unclear. The pulsatile (oscillatory plus mean) flow measured in the space surrounding the middle cerebral artery (MCA) suggests that peristalsis created by intravascular blood pressure pulses is a candidate for the paraarterial flow in the subarachnoid spaces. However, peristalsis is ineffective in driving significant mean flow when the amplitude of channel wall motion is small, as has been observed in the MCA artery wall. In this paper, peristalsis in combination with two additional mechanisms, a longitudinal pressure gradient and directional flow resistance, is evaluated to match the measured MCA paraarterial oscillatory and mean flows. Methods Two analytical models are used that simplify the paraarterial branched network to a long continuous channel with a traveling wave in order to maximize the potential effect of peristalsis on the mean flow. The two models have parallel-plate and annulus geometries, respectively, with and without an added longitudinal pressure gradient. The effect of directional flow resistors was also evaluated for the parallel-plate geometry. Results For these models, the measured amplitude of arterial wall motion is too large to cause the small measured amplitude of oscillatory velocity, indicating that the outer wall must also move. At a combined motion matching the measured oscillatory velocity, peristalsis is incapable of driving enough mean flow. Directional flow resistance elements augment the mean flow, but not enough to provide a match. With a steady longitudinal pressure gradient, both oscillatory and mean flows can be matched to the measurements. Conclusions These results suggest that peristalsis drives the oscillatory flow in the subarachnoid paraarterial space, but is incapable of driving the mean flow. The effect of directional flow resistors is insufficient to produce a match, but a small longitudinal pressure gradient is capable of creating the mean flow. Additional experiments are needed to confirm whether the outer wall also moves, as well as to validate the pressure gradient.
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spelling doaj.art-974a7b4fb1f04b4483d4324e19b959022023-06-11T11:23:01ZengBMCFluids and Barriers of the CNS2045-81182023-06-012011910.1186/s12987-023-00445-0Pulsatile cerebral paraarterial flow by peristalsis, pressure and directional resistanceM. Keith Sharp0Department of Mechanical Engineering, University of LouisvilleAbstract Background A glymphatic system has been proposed that comprises flow that enters along cerebral paraarterial channels between the artery wall and the surrounding glial layer, continues through the parenchyma, and then exits along similar paravenous channels. The mechanism driving flow through this system is unclear. The pulsatile (oscillatory plus mean) flow measured in the space surrounding the middle cerebral artery (MCA) suggests that peristalsis created by intravascular blood pressure pulses is a candidate for the paraarterial flow in the subarachnoid spaces. However, peristalsis is ineffective in driving significant mean flow when the amplitude of channel wall motion is small, as has been observed in the MCA artery wall. In this paper, peristalsis in combination with two additional mechanisms, a longitudinal pressure gradient and directional flow resistance, is evaluated to match the measured MCA paraarterial oscillatory and mean flows. Methods Two analytical models are used that simplify the paraarterial branched network to a long continuous channel with a traveling wave in order to maximize the potential effect of peristalsis on the mean flow. The two models have parallel-plate and annulus geometries, respectively, with and without an added longitudinal pressure gradient. The effect of directional flow resistors was also evaluated for the parallel-plate geometry. Results For these models, the measured amplitude of arterial wall motion is too large to cause the small measured amplitude of oscillatory velocity, indicating that the outer wall must also move. At a combined motion matching the measured oscillatory velocity, peristalsis is incapable of driving enough mean flow. Directional flow resistance elements augment the mean flow, but not enough to provide a match. With a steady longitudinal pressure gradient, both oscillatory and mean flows can be matched to the measurements. Conclusions These results suggest that peristalsis drives the oscillatory flow in the subarachnoid paraarterial space, but is incapable of driving the mean flow. The effect of directional flow resistors is insufficient to produce a match, but a small longitudinal pressure gradient is capable of creating the mean flow. Additional experiments are needed to confirm whether the outer wall also moves, as well as to validate the pressure gradient.https://doi.org/10.1186/s12987-023-00445-0BrainGlymphatic flowPeristaltic flowPerivascularParavascular
spellingShingle M. Keith Sharp
Pulsatile cerebral paraarterial flow by peristalsis, pressure and directional resistance
Fluids and Barriers of the CNS
Brain
Glymphatic flow
Peristaltic flow
Perivascular
Paravascular
title Pulsatile cerebral paraarterial flow by peristalsis, pressure and directional resistance
title_full Pulsatile cerebral paraarterial flow by peristalsis, pressure and directional resistance
title_fullStr Pulsatile cerebral paraarterial flow by peristalsis, pressure and directional resistance
title_full_unstemmed Pulsatile cerebral paraarterial flow by peristalsis, pressure and directional resistance
title_short Pulsatile cerebral paraarterial flow by peristalsis, pressure and directional resistance
title_sort pulsatile cerebral paraarterial flow by peristalsis pressure and directional resistance
topic Brain
Glymphatic flow
Peristaltic flow
Perivascular
Paravascular
url https://doi.org/10.1186/s12987-023-00445-0
work_keys_str_mv AT mkeithsharp pulsatilecerebralparaarterialflowbyperistalsispressureanddirectionalresistance