Cerebral Hemodynamics Underlying Artery-to-Artery Embolism in Symptomatic Intracranial Atherosclerotic Disease

Xueyan Feng; Hui Fang; Bonaventure Y M Ip; Ka Lung Chan; Shuang Li; Xuan Tian; Lina Zheng; Yuying Liu; Linfang Lan; Haipeng Liu; Jill Abrigo; Sze Ho Ma; Florence S Y Fan; Vincent H L Ip; Yannie O Y Soo; Vincent C T Mok; Bo Song; Thomas W Leung; Yuming Xu; Xinyi Leng

doi:10.1007/s12975-023-01146-4

Cerebral Hemodynamics Underlying Artery-to-Artery Embolism in Symptomatic Intracranial Atherosclerotic Disease

Xueyan Feng, Hui Fang, Bonaventure Y M Ip, Ka Lung Chan, Shuang Li, Xuan Tian, Lina Zheng, Yuying Liu, Linfang Lan, Haipeng Liu, Jill Abrigo, Sze Ho Ma, Florence S Y Fan, Vincent H L Ip, Yannie O Y Soo, Vincent C T Mok, Bo Song, Thomas W Leung, Yuming Xu, Xinyi Leng

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Abstract

Artery-to-artery embolism (AAE) is a common stroke mechanism in intracranial atherosclerotic disease (ICAD), associated with a considerable risk of recurrent stroke. We aimed to investigate cerebral hemodynamic features associated with AAE in symptomatic ICAD. Patients with anterior-circulation, symptomatic ICAD confirmed in CT angiography (CTA) were recruited. We classified probable stroke mechanisms as isolated parent artery atherosclerosis occluding penetrating artery, AAE, hypoperfusion, and mixed mechanisms, largely based on infarct topography. CTA-based computational fluid dynamics (CFD) models were built to simulate blood flow across culprit ICAD lesions. Translesional pressure ratio (PR = Pressure /Pressure ) and wall shear stress ratio (WSSR = WSS /WSS ) were calculated, to reflect the relative, translesional changes of the two hemodynamic metrics. Low PR (PR ≤ median) and high WSSR (WSSR ≥ 4th quartile) respectively indicated large translesional pressure and elevated WSS upon the lesion. Among 99 symptomatic ICAD patients, 44 had AAE as a probable stroke mechanism, 13 with AAE alone and 31 with coexisting hypoperfusion. High WSSR was independently associated with AAE (adjusted OR = 3.90; P = 0.022) in multivariate logistic regression. There was significant WSSR-PR interaction on the presence of AAE (P for interaction = 0.013): high WSSR was more likely to associate with AAE in those with low PR (P = 0.075), but not in those with normal PR (P = 0.959). Excessively elevated WSS in ICAD might increase the risk of AAE. Such association was more prominent in those with large translesional pressure gradient. Hypoperfusion, commonly coexisting with AAE, might be a therapeutic indicator for secondary stroke prevention in symptomatic ICAD with AAE. [Abstract copyright: © 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.]

Original language	English
Pages (from-to)	572-579
Number of pages	8
Journal	Translational Stroke Research
Volume	15
Issue number	3
Early online date	10 Mar 2023
DOIs	https://doi.org/10.1007/s12975-023-01146-4
Publication status	Published - Jun 2024

Bibliographical note

The final publication is available at Springer via http://dx.doi.org/10.1007/s12975-023-01146-4

Copyright © and Moral Rights are retained by the author(s) and/ or other copyright owners. A copy can be downloaded for personal non-commercial research or study, without prior permission or charge. This item cannot be reproduced or quoted extensively from without first obtaining permission in writing from the copyright holder(s). The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the copyright holders.

This document is the author’s post-print version, incorporating any revisions agreed during the peer-review process. Some differences between the published version and this version may remain and you are advised to consult the published version if you wish to cite from it.

Funder

This study was funded by the General Research Fund (Reference No. 14106019 & 14138416), Hong Kong Research Grants Council; Health and Medical Research Fund (Reference No. 07180366), Hong Kong Food and Health Bureau; the NHC Key Laboratory of Prevention and treatment of Cerebrovascular Disease, Henan Key Laboratory of Cerebrovascular Diseases (Zhengzhou University), the Non-profit Central Research Institute and Major Science to Yuming Xu (Grant No. 2020-PT310-01).

Keywords

Stroke
Intracranial Atherosclerosis
Prognosis
Embolism
Hemodynamics

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10.1007/s12975-023-01146-4

Liu2023AAM Accepted author manuscript, 1.04 MB

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Feng, X., Fang, H., Ip, B. Y. M., Chan, K. L., Li, S., Tian, X., Zheng, L., Liu, Y., Lan, L., Liu, H., Abrigo, J., Ma, S. H., Fan, F. S. Y., Ip, V. H. L., Soo, Y. O. Y., Mok, V. C. T., Song, B., Leung, T. W., Xu, Y., & Leng, X. (2024). Cerebral Hemodynamics Underlying Artery-to-Artery Embolism in Symptomatic Intracranial Atherosclerotic Disease. Translational Stroke Research, 15(3), 572-579. https://doi.org/10.1007/s12975-023-01146-4

Feng, X, Fang, H, Ip, BYM, Chan, KL, Li, S, Tian, X, Zheng, L, Liu, Y, Lan, L, Liu, H, Abrigo, J, Ma, SH, Fan, FSY, Ip, VHL, Soo, YOY, Mok, VCT, Song, B, Leung, TW, Xu, Y & Leng, X 2024, 'Cerebral Hemodynamics Underlying Artery-to-Artery Embolism in Symptomatic Intracranial Atherosclerotic Disease', Translational Stroke Research, vol. 15, no. 3, pp. 572-579. https://doi.org/10.1007/s12975-023-01146-4

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abstract = "Artery-to-artery embolism (AAE) is a common stroke mechanism in intracranial atherosclerotic disease (ICAD), associated with a considerable risk of recurrent stroke. We aimed to investigate cerebral hemodynamic features associated with AAE in symptomatic ICAD. Patients with anterior-circulation, symptomatic ICAD confirmed in CT angiography (CTA) were recruited. We classified probable stroke mechanisms as isolated parent artery atherosclerosis occluding penetrating artery, AAE, hypoperfusion, and mixed mechanisms, largely based on infarct topography. CTA-based computational fluid dynamics (CFD) models were built to simulate blood flow across culprit ICAD lesions. Translesional pressure ratio (PR = Pressure /Pressure ) and wall shear stress ratio (WSSR = WSS /WSS ) were calculated, to reflect the relative, translesional changes of the two hemodynamic metrics. Low PR (PR ≤ median) and high WSSR (WSSR ≥ 4th quartile) respectively indicated large translesional pressure and elevated WSS upon the lesion. Among 99 symptomatic ICAD patients, 44 had AAE as a probable stroke mechanism, 13 with AAE alone and 31 with coexisting hypoperfusion. High WSSR was independently associated with AAE (adjusted OR = 3.90; P = 0.022) in multivariate logistic regression. There was significant WSSR-PR interaction on the presence of AAE (P for interaction = 0.013): high WSSR was more likely to associate with AAE in those with low PR (P = 0.075), but not in those with normal PR (P = 0.959). Excessively elevated WSS in ICAD might increase the risk of AAE. Such association was more prominent in those with large translesional pressure gradient. Hypoperfusion, commonly coexisting with AAE, might be a therapeutic indicator for secondary stroke prevention in symptomatic ICAD with AAE. [Abstract copyright: {\textcopyright} 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.]",

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author = "Xueyan Feng and Hui Fang and Ip, {Bonaventure Y M} and Chan, {Ka Lung} and Shuang Li and Xuan Tian and Lina Zheng and Yuying Liu and Linfang Lan and Haipeng Liu and Jill Abrigo and Ma, {Sze Ho} and Fan, {Florence S Y} and Ip, {Vincent H L} and Soo, {Yannie O Y} and Mok, {Vincent C T} and Bo Song and Leung, {Thomas W} and Yuming Xu and Xinyi Leng",

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N1 - The final publication is available at Springer via http://dx.doi.org/10.1007/s12975-023-01146-4 Copyright © and Moral Rights are retained by the author(s) and/ or other copyright owners. A copy can be downloaded for personal non-commercial research or study, without prior permission or charge. This item cannot be reproduced or quoted extensively from without first obtaining permission in writing from the copyright holder(s). The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the copyright holders. This document is the author’s post-print version, incorporating any revisions agreed during the peer-review process. Some differences between the published version and this version may remain and you are advised to consult the published version if you wish to cite from it.

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N2 - Artery-to-artery embolism (AAE) is a common stroke mechanism in intracranial atherosclerotic disease (ICAD), associated with a considerable risk of recurrent stroke. We aimed to investigate cerebral hemodynamic features associated with AAE in symptomatic ICAD. Patients with anterior-circulation, symptomatic ICAD confirmed in CT angiography (CTA) were recruited. We classified probable stroke mechanisms as isolated parent artery atherosclerosis occluding penetrating artery, AAE, hypoperfusion, and mixed mechanisms, largely based on infarct topography. CTA-based computational fluid dynamics (CFD) models were built to simulate blood flow across culprit ICAD lesions. Translesional pressure ratio (PR = Pressure /Pressure ) and wall shear stress ratio (WSSR = WSS /WSS ) were calculated, to reflect the relative, translesional changes of the two hemodynamic metrics. Low PR (PR ≤ median) and high WSSR (WSSR ≥ 4th quartile) respectively indicated large translesional pressure and elevated WSS upon the lesion. Among 99 symptomatic ICAD patients, 44 had AAE as a probable stroke mechanism, 13 with AAE alone and 31 with coexisting hypoperfusion. High WSSR was independently associated with AAE (adjusted OR = 3.90; P = 0.022) in multivariate logistic regression. There was significant WSSR-PR interaction on the presence of AAE (P for interaction = 0.013): high WSSR was more likely to associate with AAE in those with low PR (P = 0.075), but not in those with normal PR (P = 0.959). Excessively elevated WSS in ICAD might increase the risk of AAE. Such association was more prominent in those with large translesional pressure gradient. Hypoperfusion, commonly coexisting with AAE, might be a therapeutic indicator for secondary stroke prevention in symptomatic ICAD with AAE. [Abstract copyright: © 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.]

AB - Artery-to-artery embolism (AAE) is a common stroke mechanism in intracranial atherosclerotic disease (ICAD), associated with a considerable risk of recurrent stroke. We aimed to investigate cerebral hemodynamic features associated with AAE in symptomatic ICAD. Patients with anterior-circulation, symptomatic ICAD confirmed in CT angiography (CTA) were recruited. We classified probable stroke mechanisms as isolated parent artery atherosclerosis occluding penetrating artery, AAE, hypoperfusion, and mixed mechanisms, largely based on infarct topography. CTA-based computational fluid dynamics (CFD) models were built to simulate blood flow across culprit ICAD lesions. Translesional pressure ratio (PR = Pressure /Pressure ) and wall shear stress ratio (WSSR = WSS /WSS ) were calculated, to reflect the relative, translesional changes of the two hemodynamic metrics. Low PR (PR ≤ median) and high WSSR (WSSR ≥ 4th quartile) respectively indicated large translesional pressure and elevated WSS upon the lesion. Among 99 symptomatic ICAD patients, 44 had AAE as a probable stroke mechanism, 13 with AAE alone and 31 with coexisting hypoperfusion. High WSSR was independently associated with AAE (adjusted OR = 3.90; P = 0.022) in multivariate logistic regression. There was significant WSSR-PR interaction on the presence of AAE (P for interaction = 0.013): high WSSR was more likely to associate with AAE in those with low PR (P = 0.075), but not in those with normal PR (P = 0.959). Excessively elevated WSS in ICAD might increase the risk of AAE. Such association was more prominent in those with large translesional pressure gradient. Hypoperfusion, commonly coexisting with AAE, might be a therapeutic indicator for secondary stroke prevention in symptomatic ICAD with AAE. [Abstract copyright: © 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.]

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Cerebral Hemodynamics Underlying Artery-to-Artery Embolism in Symptomatic Intracranial Atherosclerotic Disease

Abstract

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Keywords

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