High wall shear stress and spatial gradients in vascular pathology: a review

Jennifer M Dolan, John Kolega, Hui Meng, Jennifer M Dolan, John Kolega, Hui Meng

Abstract

Cardiovascular pathologies such as intracranial aneurysms (IAs) and atherosclerosis preferentially localize to bifurcations and curvatures where hemodynamics are complex. While extensive knowledge about low wall shear stress (WSS) has been generated in the past, due to its strong relevance to atherogenesis, high WSS (typically >3 Pa) has emerged as a key regulator of vascular biology and pathology as well, receiving renewed interests. As reviewed here, chronic high WSS not only stimulates adaptive outward remodeling, but also contributes to saccular IA formation (at bifurcation apices or outer curves) and atherosclerotic plaque destabilization (in stenosed vessels). Recent advances in understanding IA pathogenesis have shed new light on the role of high WSS in pathological vascular remodeling. In complex geometries, high WSS can couple with significant spatial WSS gradient (WSSG). A combination of high WSS and positive WSSG has been shown to trigger aneurysm initiation. Since endothelial cells (ECs) are sensors of WSS, we have begun to elucidate EC responses to high WSS alone and in combination with WSSG. Understanding such responses will provide insight into not only aneurysm formation, but also plaque destabilization and other vascular pathologies and potentially lead to improved strategies for disease management and novel targets for pharmacological intervention.

Figures

FIGURE 1
FIGURE 1
Examples of arterial geometries with different WSS characteristics. (a) Carotid bifurcation with disturbed flow in the sinus opposite the apex, characterized by low WSS, and prone to atherogenesis. (b) Cerebral bifurcation with apex experiencing high WSS and WSSG resulting from flow impingement are prone to aneurysm formation. (c) Arterial stenosis, with both high WSS (upstream shoulder) and low WSS (downstream, disturbed flow).
FIGURE 2
FIGURE 2
Hemodynamic-histology co-mapping in the canine de novo bifurcation model reveals specific hemodynamic conditions leading to different remodeling responses. (a) Overlay of flow velocity vectors on the corresponding histological section. (b) Plot of WSS (blue) and WSSG (red) vs. distance from the apex revealing 3 regions with distinct flow patterns and remodeling responses from (a). Region 1: the impingement region with hyperplastic responses; Region II: acceleration region with aneurysmlike remodeling; and Region III: decelerating flow and recovery to baseline flow with no morphological changes. From Meng et al. Reproduced with permission.
FIGURE 3
FIGURE 3
Hemodynamic conditions for aneurysm initiation at the basilar terminus in rabbits that received bilateral CCA ligation. (a) Histology (Van Gieson staining) at 5 days showing early aneurysmal damage in the form of IEL loss in two segments (ends are marked by arrows) flanking the apex. (b) Hemodynamics-histology co-mapping to determine the local hemodynamic conditions of initial aneurysmal damage. (c) WSS (blue) and WSSG (red) distribution along the wall, whereby IEL damage (yellow bands) localized in the flow acceleration zone. (d) “Point cloud” showing microsegments of intact IEL (black open circles) and damaged IEL (red solid dots) plotted against their local WSS and WSSG values. The red dots are clustered to the top right of the coordinate system, indicating that aneurysm-initiating conditions are positive WSSG and high WSS. Reproduced from Metaxa et al. with permission.
FIGURE 4
FIGURE 4
A marble-in-a-bowl metaphor for the role of hemodynamic insult in relation to other risk factors in aneurysm initiation. Homeostasis is represented by the marble at the bottom of the bowl and hemodynamic insult (white arrow) is represented by a push on the marble. (a) A gentle push results in a return to homeostasis. (b) A strong enough push causes the marble to fall out of the bowl causing a departure from homeostasis into pathogenesis. (c) Other risk factors (family history, female gender, genetic diseases, cigarette smoking and hypertension) lower the rim of the bowl, such that a gentle push can result in pathogenesis (i.e., aneurysm formation). Modified from Meng et al.
FIGURE 5
FIGURE 5
Alignment of bovine aortic ECs subjected to high WSS alone (a) or in combination with WSSG (b). (a) In vitro flow chamber subjecting EC monolayers to baseline WSS and high WSS. ECs align and elongate with their long axis parallel to the flow with a time course dependent on the WSS and display a transient perpendicular alignment when WSS is high. (b) In vitro flow system with converging and diverging-segments to produce positive and negative WSSG across EC monolayers. Positive WSSG hinders cell alignment to flow while negative WSS promotes it, even under the same range of WSS. Modified from Dolan et al., Reproduced with permission.
FIGURE 6
FIGURE 6
A conceptual picture of the mechanical forces on ECs in accelerating and decelerating flow: WSS from the flowing blood, net stretching/compression due to WSSG, and cyclic stretching from pulsatile pressure.

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