Leptomeningeal anastomoses: Mechanisms of pial collateral remodeling in ischemic stroke

Abstract

Arterial collateralization, as determined by leptomeningeal anastomoses or pial collateral vessels, is a well‐established vital player in cerebral blood flow restoration and neurological recovery from ischemic stroke. A secondary network of cerebral collateral circulation apart from the Circle of Willis, exist as remnants of arteriole development that connect the distal arteries in the pia mater. Recent interest lies in understanding the cellular and molecular adaptations that control the growth and remodeling, or arteriogenesis, of these pre‐existing collateral vessels. New findings from both animal models and human studies of ischemic stroke suggest a multi‐factorial and complex, temporospatial interplay of endothelium, immune and vessel‐associated cell interactions may work in concert to facilitate or thwart arteriogenesis. These valuable reports may provide critical insight into potential predictors of the pial collateral response in patients with large vessel occlusion and may aid in therapeutics to enhance collateral function and improve recovery from stroke. This article is categorized under: Neurological Diseases > Molecular and Cellular Physiology

Pial collaterals develop through mosaic colonization of capillaries by arterial and microvascular endothelial cells

“…Our confocal imaging of the entire pial surface enabled us to anatomically distinguish collaterals from neighboring arterioles. Mature collaterals are easily identifiable in the adult as the often tortuous connections between the neighboring arterioles of the highest branching order (Faber et al, 2014; Kaloss & Theus, 2022; Perovic et al, 2022). In the embryo, collateral connections show no tortuosity and resemble vascular loops (Fig.…”

“…Pial collaterals are thus a rare gem, as they represent a back-up feeding strategy. After ischemic blocking of the main feeding artery, collaterals undergo extensive remodeling in a matter of days, all while maintaining vascular integrity and function (Faber et al, 2014; Okyere et al, 2018; Kaloss and Theus, 2022; Maguida and Shuaib, 2023). Although collateral enhancement in patients has substantial clinical potential as an acute stroke therapy, collateral therapeutics remain a relatively uncharted therapeutic strategy (Winship, 2015; Iwasawa et al, 2016).…”

Pial collaterals develop through mosaic colonization of capillaries by arterial and microvascular endothelial cells

“…Pial collaterals are thus a rare gem, as they represent a back-up feeding strategy. After ischemic blocking of the main feeding artery, collaterals undergo extensive remodeling in a matter of days, all while maintaining vascular integrity and function (Faber et al, 2014 ;Okyere et al, 2018 ;Kaloss and Theus, 2022 ;Maguida and Shuaib, 2023 ). Although collateral enhancement in patients has substantial clinical potential as an acute stroke therapy, collateral therapeutics remain a relatively uncharted therapeutic strategy (Winship, 2015 ;Iwasawa et al, 2016 ).…”

“…Our confocal imaging of the entire pial surface enabled us to anatomically distinguish collaterals from neighboring arterioles. Mature collaterals are easily identifiable in the adult as the often tortuous connections between the neighboring arterioles of the highest branching order (Faber et al, 2014 ;Kaloss & Theus, 2022 ;Perovic et al, 2022 ). In the embryo, collateral connections show no tortuosity and resemble vascular loops (Fig.…”

Remodeling of the Neurovascular Unit Following Cerebral Ischemia and Hemorrhage

“…The collateral circulation is a unique blood vessel present in the microcirculation of most tissues connecting a small fraction of the outer branches of adjacent arterial trees [ 98 , 99 ]. Collateral circulation protects against ischemic brain injury through the alternate routes of perfusion [ 100 , 101 ]. Furthermore, endothelial and smooth muscle cells of collateral vessels have morphologic and functional differences from nearby similarly sized arterioles [ 102 ].…”