Computational modeling of multiscale collateral blood supply in a whole-brain-scale arterial network

PLoS Comput Biol. 2023 Sep 8;19(9):e1011452. doi: 10.1371/journal.pcbi.1011452. eCollection 2023 Sep.

Abstract

The cerebral arterial network covering the brain cortex has multiscale anastomosis structures with sparse intermediate anastomoses (O[102] μm in diameter) and dense pial networks (O[101] μm in diameter). Recent studies indicate that collateral blood supply by cerebral arterial anastomoses has an essential role in the prognosis of acute ischemic stroke caused by large vessel occlusion. However, the physiological importance of these multiscale morphological properties-and especially of intermediate anastomoses-is poorly understood because of innate structural complexities. In this study, a computational model of multiscale anastomoses in whole-brain-scale cerebral arterial networks was developed and used to evaluate collateral blood supply by anastomoses during middle cerebral artery occlusion. Morphologically validated cerebral arterial networks were constructed by combining medical imaging data and mathematical modeling. Sparse intermediate anastomoses were assigned between adjacent main arterial branches; the pial arterial network was modeled as a dense network structure. Blood flow distributions in the arterial network during middle cerebral artery occlusion simulations were computed. Collateral blood supply by intermediate anastomoses increased sharply with increasing numbers of anastomoses and provided one-order-higher flow recoveries to the occluded region (15%-30%) compared with simulations using a pial network only, even with a small number of intermediate anastomoses (≤10). These findings demonstrate the importance of sparse intermediate anastomoses, which are generally considered redundant structures in cerebral infarction, and provide insights into the physiological significance of the multiscale properties of arterial anastomoses.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arteries
  • Brain
  • Computer Simulation
  • Humans
  • Infarction, Middle Cerebral Artery
  • Ischemic Stroke*

Grants and funding

This work was supported by MEXT as the “Program for Promoting Researches on the Supercomputer Fugaku” (hp220161 to SW and hp230208 to SI), the Japanese Society for the Promotion of Science for Grants-in-Aid for Scientific Research (No. 19H01175 to SW, 21K18037 to TO, 22H00190 to MO, 23K11830 to TO), and the Multidisciplinary Research Laboratory System for Future Developments, Osaka University Graduate School of Engineering Science (to TO). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.