Progress on the correlation between circle of Willis and cerebral large and small vessel diseases

doi:10.3969/j.issn.1672-6731.2023.11.003

Abstract

Abstract:

The circle of Willis constitutes the primary collateral circulation of the brain, exerting a significant influence on the distribution of intracranial blood flow. Variations of the circle of Willis can impact the cerebrovascular diseases by diminishing collateral compensation capacity and altering the stability of intracranial hemodynamics. This paper reviews the research progress on the association between circle of Willis and cerebral large vessel disease [such as intracranial arterial dolichoectasia (IADE) and intracranial atherosclerotic stenosis (ICAS)], as well as cerebral small vessel disease (CSVD), so as to provide new ideas for the diagnosis and treatment for these diseases.

Key words: Cerebrovascular disorders, Circle of Willis, Review

摘要：

Willis环构成大脑初级侧支循环，对脑血流分布具有重要影响。Willis环变异通过降低侧支循环代偿功能、改变脑血流动力学稳定性影响脑血管病发生与发展。本文对Willis环变异与脑大血管病（如颅内动脉延长扩张和颅内动脉粥样硬化性狭窄）及小血管病相关性研究进展进行综述，以为疾病的诊断与治疗提供新思路。

关键词: 脑血管障碍, 大脑动脉环, 综述

Lu FENG, Yi-cheng ZHU. Progress on the correlation between circle of Willis and cerebral large and small vessel diseases[J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2023, 23(11): 966-971.

冯璐, 朱以诚. Willis环变异与脑大血管病及小血管病相关性研究进展[J]. 中国现代神经疾病杂志, 2023, 23(11): 966-971.

/ / Recommend / Download Citations

URL: http://journal11.magtechjournal.com/cjcnn/EN/10.3969/j.issn.1672-6731.2023.11.003

http://journal11.magtechjournal.com/cjcnn/EN/Y2023/V23/I11/966

Figures/Tables 1

References 38

1	Duering M , Biessels GJ , Brodtmann A , Chen C , Cordonnier C , de Leeuw FE , Debette S , Frayne R , Jouvent E , Rost NS , Ter Telgte A , Al-Shahi Salman R , Backes WH , Bae HJ , Brown R , Chabriat H , De Luca A , deCarli C , Dewenter A , Doubal FN , Ewers M , Field TS , Ganesh A , Greenberg S , Helmer KG , Hilal S , Jochems ACC , Jokinen H , Kuijf H , Lam BYK , Lebenberg J , MacIntosh BJ , Maillard P , Mok VCT , Pantoni L , Rudilosso S , Satizabal CL , Schirmer MD , Schmidt R , Smith C , Staals J , Thrippleton MJ , van Veluw SJ , Vemuri P , Wang Y , Werring D , Zedde M , Akinyemi RO , Del Brutto OH , Markus HS , Zhu YC , Smith EE , Dichgans M , Wardlaw JM . Neuroimaging standards for research into small vessel disease: advances since 2013. Lancet Neurol, 2023, 22: 602- 618. doi: 10.1016/S1474-4422(23)00131-X
2	Pasi M , Cordonnier C . Clinical relevance of cerebral small vessel diseases. Stroke, 2020, 51: 47- 53. doi: 10.1161/STROKEAHA.119.024148
3	Gutierrez J , Turan TN , Hoh BL , Chimowitz MI . Intracranial atherosclerotic stenosis: risk factors, diagnosis, and treatment. Lancet Neurol, 2022, 21: 355- 368. doi: 10.1016/S1474-4422(21)00376-8
4	Zhang DP , Yin S , Zhang HL , Li D , Song B , Liang JX . Association between intracranial arterial dolichoectasia and cerebral small vessel disease and its underlying mechanisms. J Stroke, 2020, 22: 173- 184. doi: 10.5853/jos.2019.02985
5	Lopez-Navarro ER , Gutierrez J . Metalloproteinases and their inhibitors in neurological disease. Naunyn Schmiedebergs Arch Pharmacol, 2022, 395: 27- 38. doi: 10.1007/s00210-021-02188-x
6	Marquez-Romero JM , Díaz-Molina R , Hernández-Curiel BC , Bonifacio-Delgadillo DM , Prado-Aguilar CA . Matrix metalloproteinase-2 and matrix metalloproteinase-9 serum levels in patients with vertebrobasilar dolichoectasia with and without stroke: case-control study. Neuroradiology, 2022, 64: 1187- 1193. doi: 10.1007/s00234-021-02869-7
7	Nixon AM , Gunel M , Sumpio BE . The critical role of hemodynamics in the development of cerebral vascular disease. J Neurosurg, 2010, 112: 1240- 1253. doi: 10.3171/2009.10.JNS09759
8	Wang J , Ji J , Qiu J , Wang Y . Incompleteness of circle of Willis and silent brain infarction in patients with internal carotid artery stenosis. J Clin Neurosci, 2022, 98: 73- 77. doi: 10.1016/j.jocn.2022.02.001
9	Ye H , Wu X , Yan J , Wang J , Qiu J , Wang Y . Completeness of circle of Willis and white matter hyperintensities in patients with severe internal carotid artery stenosis. Neurol Sci, 2019, 40: 509- 514. doi: 10.1007/s10072-018-3683-9
10	Bertulli L , Robert T . Embryological development of the human cranio-facial arterial system: a pictorial review. Surg Radiol Anat, 2021, 43: 961- 973. doi: 10.1007/s00276-021-02684-y
11	Leng X , Leung TW . Collateral flow in intracranial atherosclerotic disease. Transl Stroke Res, 2023, 14: 38- 52. doi: 10.1007/s12975-022-01042-3
12	Qiao X , Duan J , Zhang N , Duan Y , Wang X , Pei Y , Xu Z , Yang B , Qi M , Li J . Risk factors of impaired perfusion in patients with symptomatic internal carotid artery steno-occlusive disease. Front Neurol, 2022, 13: 801413. doi: 10.3389/fneur.2022.801413
13	Zhang B , Wang G , Gao Y , Tan H , Wang P . Influence of the integrity of circle of Willis on asymptomatic or mild patients with first diagnosed chronic internal carotid artery occlusion. Eur J Radiol, 2023, 165: 110954. doi: 10.1016/j.ejrad.2023.110954
14	Hendrikse J , Eikelboom BC , van der Grond J . Magnetic resonance angiography of collateral compensation in asymptomatic and symptomatic internal carotid artery stenosis. J Vasc Surg, 2002, 36: 799- 805. doi: 10.1067/mva.2002.127346
15	Zarrinkoob L , Wåhlin A , Ambarki K , Birgander R , Eklund A , Malm J . Blood flow lateralization and collateral compensatory mechanisms in patients with carotid artery stenosis. Stroke, 2019, 50: 1081- 1088. doi: 10.1161/STROKEAHA.119.024757
16	Hendrikse J , van Raamt AF , van der Graaf Y , Mali WP , van der Grond J . Distribution of cerebral blood flow in the circle of Willis. Radiology, 2005, 235: 184- 189. doi: 10.1148/radiol.2351031799
17	Zheng R , Han Q , Hong W , Yi X , He B , Liu Y . Hemodynamic characteristics and mechanism for intracranial aneurysms initiation with the circle of Willis anomaly. Comput Methods Biomech Biomed Engin, 2023, 20: 1- 9.
18	Xu J , Yu Y , Wu X , Wu Y , Jiang C , Wang S , Huang Q , Liu J . Morphological and hemodynamic analysis of mirror posterior communicating artery aneurysms. PLoS One, 2013, 8: e55413. doi: 10.1371/journal.pone.0055413
19	Muskat JC , Rayz VL , Goergen CJ , Babbs CF . Hemodynamic modeling of the circle of Willis reveals unanticipated functions during cardiovascular stress. J Appl Physiol (1985), 2021, 131: 1020- 1034. doi: 10.1152/japplphysiol.00198.2021
20	Hindenes LB , Håberg AK , Johnsen LH , Mathiesen EB , Robben D , Vangberg TR . Variations in the Circle of Willis in a large population sample using 3D TOF angiography: the Tromsø study. PLoS One, 2020, 15: e0241373. doi: 10.1371/journal.pone.0241373
21	van den Brink H , Doubal FN , Duering M . Advanced MRI in cerebral small vessel disease. Int J Stroke, 2023, 18: 28- 35. doi: 10.1177/17474930221091879
22	Gaidzik F , Pathiraja S , Saalfeld S , Stucht D , Speck O , Thévenin D , Janiga G . Hemodynamic data assimilation in a subject-specific circle of Willis geometry. Clin Neuroradiol, 2021, 31: 643- 651. doi: 10.1007/s00062-020-00959-2
23	Zhou S, Qiao Y, Zhou X, Wasserman BA, Caughey MC. Detection of dolichoectasia and atherosclerosis by automated MRA tortuosity metrics in a population-based study[J]. J Magn Reson Imaging, 2023. [Epub ahead of print]
24	Dumais F , Caceres MP , Janelle F , Seifeldine K , Arès-Bruneau N , Gutierrez J , Bocti C , Whittingstall K . eICAB: a novel deep learning pipeline for Circle of Willis multiclass segmentation and analysis. Neuroimage, 2022, 260: 119425. doi: 10.1016/j.neuroimage.2022.119425
25	Yu L , Xinmiao Z , Yawei W , Wentao F , Jing J , Zhunjun S , Bitian W , Yongjun W , Yubo F . Effects of abnormal vertebral arteries and the circle of Willis on vertebrobasilar dolichoectasia: a multi-scale simulation study. Clin Biomech (Bristol, Avon), 2023, 101: 105853. doi: 10.1016/j.clinbiomech.2022.105853
26	Wu TC , Chen TY , Ko CC , Chen JH , Lin CP . Correlation of internal carotid artery diameter and carotid flow with asymmetry of the circle of Willis. BMC Neurol, 2020, 20: 251. doi: 10.1186/s12883-020-01831-z
27	Gutierrez J , Sultan S , Bagci A , Rundek T , Alperin N , Elkind MS , Sacco RL , Wright CB . Circle of Willis configuration as a determinant of intracranial dolichoectasia. Cerebrovasc Dis, 2013, 36: 446- 453. doi: 10.1159/000356347
28	Takeuchi M , Miwa K , Tanaka M , Zhou Y , Todo K , Sasaki T , Sakaguchi M , Kitagawa K , Mochizuki H . A 9-year longitudinal study of basilar artery diameter. J Am Heart Assoc, 2019, 8: e011154. doi: 10.1161/JAHA.118.011154
29	Omran SS , Khasiyev F , Zhang C , Rundek T , Sacco RL , Wright CB , Elkind MSV , Gutierrez J . Anatomical effects on the relationship between brain arterial diameter and length: the Northern Manhattan Study. J Neuroimaging, 2022, 32: 735- 743. doi: 10.1111/jon.12969
30	Sho E , Sho M , Singh TM , Nanjo H , Komatsu M , Xu C , Masuda H , Zarins CK . Arterial enlargement in response to high flow requires early expression of matrix metalloproteinases to degrade extracellular matrix. Exp Mol Pathol, 2002, 73: 142- 153. doi: 10.1006/exmp.2002.2457
31	Li J , Zheng L , Yang WJ , Sze-To CY , Leung TW , Chen XY . Plaque wall distribution pattern of the atherosclerotic middle cerebral artery associates with the circle of Willis completeness. Front Neurol, 2021, 11: 599459. doi: 10.3389/fneur.2020.599459
32	Wang H , Shen L , Zhao C , Liu S , Wu G , Wang H , Wang B , Zhu J , Du J , Gong Z , Chai C , Xia S . The incomplete circle of Willis is associated with vulnerable intracranial plaque features and acute ischemic stroke. J Cardiovasc Magn Reson, 2023, 25: 23. doi: 10.1186/s12968-023-00931-2
33	Xu M , Guo W , Rascle L , Mechtouff L , Nighoghossian N , Eker O , Wang L , Henninger N , Mikati AG , Zhang S , Wu B , Liu M . Leukoaraiosis distribution and cerebral collaterals: a systematic review and meta-analysis. Front Neurol, 2022, 13: 869329. doi: 10.3389/fneur.2022.869329
34	Feng L , Zhai FF , Li ML , Zhou LX , Ni J , Yao M , Jin ZY , Cui LY , Zhang SY , Han F , Zhu YC . Association between anatomical variations of the circle of Willis and covert vascular brain injury in the general population. Cerebrovasc Dis, 2023, 52: 480- 486. doi: 10.1159/000527432
35	Miyazawa N , Shinohara T , Yamagata Z . Association of incompleteness of the anterior part of the circle of Willis with the occurrence of lacunes in the basal ganglia. Eur J Neurol, 2011, 18: 1358- 1360. doi: 10.1111/j.1468-1331.2011.03400.x
36	Xu M , Wu Q , Cheng Y , Zhang S , Tao W , Zhang S , Wang D , Liu M , Wu B . Circle of Willis morphology in primary intracerebral hemorrhage. Transl Stroke Res, 2022, 13: 736- 744. doi: 10.1007/s12975-022-00997-7
37	Del Brutto OH , Mera RM , Zambrano M , Lama J . Incompleteness of the Circle of Willis correlates poorly with imaging evidence of small vessel disease: a population-based study in rural Ecuador (the Atahualpa project). J Stroke Cerebrovasc Dis, 2015, 24: 73- 77. doi: 10.1016/j.jstrokecerebrovasdis.2014.07.036
38	Aminuddin N , Achuthan A , Ruhaiyem NIR , Che Mohd Nassir CMN , Idris NS , Mustapha M . Reduced cerebral vascular fractal dimension among asymptomatic individuals as a potential biomarker for cerebral small vessel disease. Sci Rep, 2022, 12: 11780. doi: 10.1038/s41598-022-15710-9

[1]	Ming-sheng LIU. Application of peripheral nerve and muscle ultrasound in neuromuscular diseases [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2023, 23(9): 771-774.
[2]	Ya-lan WAN, Jia-xi YU, Jian-wen DENG, Dao-jun HONG, Zhao-xia WANG. Clinical and mechanism research progress on short tandem repeat-related neuromuscular diseases [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2023, 23(9): 775-781.
[3]	Shu-hua LI, Wen SU, Hai-bo CHEN. Diagnosis and treatment of functional dystonia [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2023, 23(9): 844-849.
[4]	Ya-wei WANG, Feng TIAN. Research progress on the difference of atherosclerosis between different sexes [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2023, 23(9): 864-871.
[5]	Rong XUE, Xuan ZHANG. Impact of sleep disorders on cerebrovascular diseases [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2023, 23(8): 659-662.
[6]	Peng ZHANG, Tao CHEN, Li XU. Key techniques in cognitive behavioral therapy for insomnia in adults and recommendations for workflow improvements [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2023, 23(8): 663-667.
[7]	Xuan ZHANG, Rong XUE. Progress on biomarkers of idiopathic rapid eye movement sleep behavior disorder conversion to neurodegenerative diseases [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2023, 23(8): 668-673.
[8]	Yin LIU, Yong-hong TANG, Jin-xia ZHAI, Yuan QIU. Research progress of chronic low-grade inflammation and sleep disorders [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2023, 23(8): 674-677.
[9]	Jie-yang YU, Ya-nan ZHANG, Hui-min LI, Zhen-can HUANG, Wan-ru LI, Zan WANG. Progress on narcolepsy and anxiety [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2023, 23(8): 678-682.
[10]	Cheng-xin KU, Li-ying DENG, Liang XIE. Progress on excessive daytime sleepiness secondary to ischemic stroke [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2023, 23(8): 683-686.
[11]	Jia-feng JIANG, Lian-hua ZHAO, Wei ZHAO. Role of melatonin in pathological injury mechanism of Alzheimer's disease [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2023, 23(8): 687-692.
[12]	Pei HUANG, Gang WANG. Progress on diagnosis and treatment of functional parkinsonism [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2023, 23(8): 738-741.
[13]	Tao HONG, Bin TANG. How to become an excellent skull base surgeon [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2023, 23(7): 571-574.
[14]	Qing-shuo ZHANG, Dan-dan SONG, Shi-yue ZHOU, Jin-lu ZHANG, Xiao-xu HAN, Shun-liang XU. Diagnosis and treatment of functional gait disorder [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2023, 23(7): 604-609.
[15]	Xi-juan PAN, Ying-qi XING, Yu-mei LIU. Imaging scoring methods for cerebral small vessel disease [J]. Chinese Journal of Contemporary Neurology and Neurosurgery, 2023, 23(7): 633-637.

Please choose a citation manager

Content to export