Hemodynamic significance of intracranial atherosclerotic disease and ipsilateral imaging markers of cerebral small vessel disease

Lina Zheng; Xuan Tian; Jill Abrigo; Hui Fang; Bonaventure YM Ip; Yuying Liu; Shuang Li; Yu  Liu; Linfang Lan; Haipeng Liu; Hing Lung Ip; Florence SY Fan; Sze Ho Ma; Karen Ma; Alexander Y Lau; Yannie OY Soo; Howan Leung; Vincent CT Mok; Lawrence KS  Wong; Yuming Xu; Liping Liu; Xinyi Leng; Thomas W Leung

doi:10.1177/23969873231205669

Hemodynamic significance of intracranial atherosclerotic disease and ipsilateral imaging markers of cerebral small vessel disease

Lina Zheng, Xuan Tian, Jill Abrigo, Hui Fang, Bonaventure YM Ip, Yuying Liu, Shuang Li, Yu Liu, Linfang Lan, Haipeng Liu, Hing Lung Ip, Florence SY Fan, Sze Ho Ma, Karen Ma, Alexander Y Lau, Yannie OY Soo, Howan Leung, Vincent CT Mok, Lawrence KS Wong , Yuming XuLiping Liu, Xinyi Leng, Thomas W Leung

Centre for Intelligent Healthcare

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Abstract

Introduction: Cerebral small vessel disease (CSVD) commonly exists in patients with symptomatic intracranial atherosclerotic disease (sICAD). We aimed to investigate the associations of hemodynamic features of sICAD lesions with imaging markers and overall burden of CSVD. Patients and methods: Patients with anterior-circulation sICAD (50%–99% stenosis) were analyzed in this cross-sectional study. Hemodynamic features of a sICAD lesion were quantified by translesional pressure ratio (PR = Pressurepost-stenotic/Pressurepre-stenotic) and wall shear stress ratio (WSSR = WSSstenotic-throat/WSSpre-stenotic) via CT angiography-based computational fluid dynamics modeling. PR ⩽median was defined as low (“abnormal”) PR, and WSSR ⩾ fourth quartile as high (“abnormal”) WSSR. For primary analyses, white matter hyperintensities (WMHs), lacunes, and cortical microinfarcts (CMIs) were assessed in MRI and summed up as overall CSVD burden, respectively in ipsilateral and contralateral hemispheres to sICAD. Enlarged perivascular spaces (EPVSs) and cerebral microbleeds (CMBs) were assessed for secondary analyses. Results: Among 112 sICAD patients, there were more severe WMHs, more lacunes and CMIs, and more severe overall CSVD burden ipsilaterally than contralaterally (all p < 0.05). Abnormal PR and WSSR (vs normal PR and WSSR) was significantly associated with moderate-to-severe WMHs (adjusted odds ratio = 10.12, p = 0.018), CMI presence (5.25, p = 0.003), and moderate-to-severe CSVD burden (12.55; p = 0.033), ipsilaterally, respectively independent of contralateral WMHs, CMI(s), and CSVD burden. EPVSs and CMBs were comparable between the two hemispheres, with no association found with the hemodynamic metrics. Discussion and conclusion: There are more severe WMHs and CMI(s) in the hemisphere ipsilateral than contralateral to sICAD. The hemodynamic significance of sICAD lesions was independently associated with severities of WMHs and CMI(s) ipsilaterally.

Original language	English
Pages (from-to)	144-153
Number of pages	10
Journal	European Stroke Journal
Volume	9
Issue number	1
Early online date	6 Oct 2023
DOIs	https://doi.org/10.1177/23969873231205669
Publication status	Published - Mar 2024

Bibliographical note

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

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by Direct Grant for Research, Chinese University of Hong Kong (Reference No. 2020.033); General Research Fund (Reference No. 14106019); and Early Career Scheme (Reference No. 24103122), Research Grants Council of Hong Kong; and Li Ka Shing Institute of Health Sciences.

Funding

We would like to thank all the participants and investigators who participated in the study. The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by Direct Grant for Research, Chinese University of Hong Kong (Reference No. 2020.033); General Research Fund (Reference No. 14106019); and Early Career Scheme (Reference No. 24103122), Research Grants Council of Hong Kong; and Li Ka Shing Institute of Health Sciences. The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by Direct Grant for Research, Chinese University of Hong Kong (Reference No. 2020.033); General Research Fund (Reference No. 14106019); and Early Career Scheme (Reference No. 24103122), Research Grants Council of Hong Kong; and Li Ka Shing Institute of Health Sciences.

Funders	Funder number
Research Grants Council, University Grants Committee
Chinese University of Hong Kong
Shanghai Normal University	24103122, 14106019
Chinese University of Hong Kong	2020.033

Keywords

Cerebral small vessel disease
hemodynamics
intracranial atherosclerotic disease
white matter hyperintensity
cortical microinfarct

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Zheng, L., Tian, X., Abrigo, J., Fang, H., Ip, B. YM., Liu, Y., Li, S., Liu, Y., Lan, L., Liu, H., Ip, H. L., Fan, F. SY., Ma, S. H., Ma, K., Lau, A. Y., Soo, Y. OY., Leung, H., Mok, V. CT., Wong , L. KS., ... Leung, T. W. (2024). Hemodynamic significance of intracranial atherosclerotic disease and ipsilateral imaging markers of cerebral small vessel disease. European Stroke Journal, 9(1), 144-153. https://doi.org/10.1177/23969873231205669

Zheng, L, Tian, X, Abrigo, J, Fang, H, Ip, BYM, Liu, Y, Li, S, Liu, Y, Lan, L, Liu, H, Ip, HL, Fan, FSY, Ma, SH, Ma, K, Lau, AY, Soo, YOY, Leung, H, Mok, VCT, Wong , LKS, Xu, Y, Liu, L, Leng, X & Leung, TW 2024, 'Hemodynamic significance of intracranial atherosclerotic disease and ipsilateral imaging markers of cerebral small vessel disease', European Stroke Journal, vol. 9, no. 1, pp. 144-153. https://doi.org/10.1177/23969873231205669

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title = "Hemodynamic significance of intracranial atherosclerotic disease and ipsilateral imaging markers of cerebral small vessel disease",

abstract = "Introduction: Cerebral small vessel disease (CSVD) commonly exists in patients with symptomatic intracranial atherosclerotic disease (sICAD). We aimed to investigate the associations of hemodynamic features of sICAD lesions with imaging markers and overall burden of CSVD. Patients and methods: Patients with anterior-circulation sICAD (50%–99% stenosis) were analyzed in this cross-sectional study. Hemodynamic features of a sICAD lesion were quantified by translesional pressure ratio (PR = Pressurepost-stenotic/Pressurepre-stenotic) and wall shear stress ratio (WSSR = WSSstenotic-throat/WSSpre-stenotic) via CT angiography-based computational fluid dynamics modeling. PR ⩽median was defined as low (“abnormal”) PR, and WSSR ⩾ fourth quartile as high (“abnormal”) WSSR. For primary analyses, white matter hyperintensities (WMHs), lacunes, and cortical microinfarcts (CMIs) were assessed in MRI and summed up as overall CSVD burden, respectively in ipsilateral and contralateral hemispheres to sICAD. Enlarged perivascular spaces (EPVSs) and cerebral microbleeds (CMBs) were assessed for secondary analyses. Results: Among 112 sICAD patients, there were more severe WMHs, more lacunes and CMIs, and more severe overall CSVD burden ipsilaterally than contralaterally (all p < 0.05). Abnormal PR and WSSR (vs normal PR and WSSR) was significantly associated with moderate-to-severe WMHs (adjusted odds ratio = 10.12, p = 0.018), CMI presence (5.25, p = 0.003), and moderate-to-severe CSVD burden (12.55; p = 0.033), ipsilaterally, respectively independent of contralateral WMHs, CMI(s), and CSVD burden. EPVSs and CMBs were comparable between the two hemispheres, with no association found with the hemodynamic metrics. Discussion and conclusion: There are more severe WMHs and CMI(s) in the hemisphere ipsilateral than contralateral to sICAD. The hemodynamic significance of sICAD lesions was independently associated with severities of WMHs and CMI(s) ipsilaterally.",

keywords = "Cerebral small vessel disease, hemodynamics, intracranial atherosclerotic disease, white matter hyperintensity, cortical microinfarct",

author = "Lina Zheng and Xuan Tian and Jill Abrigo and Hui Fang and Ip, {Bonaventure YM} and Yuying Liu and Shuang Li and Yu Liu and Linfang Lan and Haipeng Liu and Ip, {Hing Lung} and Fan, {Florence SY} and Ma, {Sze Ho} and Karen Ma and Lau, {Alexander Y} and Soo, {Yannie OY} and Howan Leung and Mok, {Vincent CT} and Wong, {Lawrence KS} and Yuming Xu and Liping Liu and Xinyi Leng and Leung, {Thomas W}",

note = "Copyright {\textcopyright} 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{\textquoteright}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. ",

year = "2024",

month = mar,

doi = "10.1177/23969873231205669",

language = "English",

volume = "9",

pages = "144--153",

journal = "European Stroke Journal",

issn = "2396-9873",

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TY - JOUR

T1 - Hemodynamic significance of intracranial atherosclerotic disease and ipsilateral imaging markers of cerebral small vessel disease

AU - Zheng, Lina

AU - Tian, Xuan

AU - Abrigo, Jill

AU - Fang, Hui

AU - Ip, Bonaventure YM

AU - Liu, Yuying

AU - Li, Shuang

AU - Liu, Yu

AU - Lan, Linfang

AU - Liu, Haipeng

AU - Ip, Hing Lung

AU - Fan, Florence SY

AU - Ma, Sze Ho

AU - Ma, Karen

AU - Lau, Alexander Y

AU - Soo, Yannie OY

AU - Leung, Howan

AU - Mok, Vincent CT

AU - Wong , Lawrence KS

AU - Xu, Yuming

AU - Liu, Liping

AU - Leng, Xinyi

AU - Leung, Thomas W

N1 - 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.

PY - 2024/3

Y1 - 2024/3

N2 - Introduction: Cerebral small vessel disease (CSVD) commonly exists in patients with symptomatic intracranial atherosclerotic disease (sICAD). We aimed to investigate the associations of hemodynamic features of sICAD lesions with imaging markers and overall burden of CSVD. Patients and methods: Patients with anterior-circulation sICAD (50%–99% stenosis) were analyzed in this cross-sectional study. Hemodynamic features of a sICAD lesion were quantified by translesional pressure ratio (PR = Pressurepost-stenotic/Pressurepre-stenotic) and wall shear stress ratio (WSSR = WSSstenotic-throat/WSSpre-stenotic) via CT angiography-based computational fluid dynamics modeling. PR ⩽median was defined as low (“abnormal”) PR, and WSSR ⩾ fourth quartile as high (“abnormal”) WSSR. For primary analyses, white matter hyperintensities (WMHs), lacunes, and cortical microinfarcts (CMIs) were assessed in MRI and summed up as overall CSVD burden, respectively in ipsilateral and contralateral hemispheres to sICAD. Enlarged perivascular spaces (EPVSs) and cerebral microbleeds (CMBs) were assessed for secondary analyses. Results: Among 112 sICAD patients, there were more severe WMHs, more lacunes and CMIs, and more severe overall CSVD burden ipsilaterally than contralaterally (all p < 0.05). Abnormal PR and WSSR (vs normal PR and WSSR) was significantly associated with moderate-to-severe WMHs (adjusted odds ratio = 10.12, p = 0.018), CMI presence (5.25, p = 0.003), and moderate-to-severe CSVD burden (12.55; p = 0.033), ipsilaterally, respectively independent of contralateral WMHs, CMI(s), and CSVD burden. EPVSs and CMBs were comparable between the two hemispheres, with no association found with the hemodynamic metrics. Discussion and conclusion: There are more severe WMHs and CMI(s) in the hemisphere ipsilateral than contralateral to sICAD. The hemodynamic significance of sICAD lesions was independently associated with severities of WMHs and CMI(s) ipsilaterally.

AB - Introduction: Cerebral small vessel disease (CSVD) commonly exists in patients with symptomatic intracranial atherosclerotic disease (sICAD). We aimed to investigate the associations of hemodynamic features of sICAD lesions with imaging markers and overall burden of CSVD. Patients and methods: Patients with anterior-circulation sICAD (50%–99% stenosis) were analyzed in this cross-sectional study. Hemodynamic features of a sICAD lesion were quantified by translesional pressure ratio (PR = Pressurepost-stenotic/Pressurepre-stenotic) and wall shear stress ratio (WSSR = WSSstenotic-throat/WSSpre-stenotic) via CT angiography-based computational fluid dynamics modeling. PR ⩽median was defined as low (“abnormal”) PR, and WSSR ⩾ fourth quartile as high (“abnormal”) WSSR. For primary analyses, white matter hyperintensities (WMHs), lacunes, and cortical microinfarcts (CMIs) were assessed in MRI and summed up as overall CSVD burden, respectively in ipsilateral and contralateral hemispheres to sICAD. Enlarged perivascular spaces (EPVSs) and cerebral microbleeds (CMBs) were assessed for secondary analyses. Results: Among 112 sICAD patients, there were more severe WMHs, more lacunes and CMIs, and more severe overall CSVD burden ipsilaterally than contralaterally (all p < 0.05). Abnormal PR and WSSR (vs normal PR and WSSR) was significantly associated with moderate-to-severe WMHs (adjusted odds ratio = 10.12, p = 0.018), CMI presence (5.25, p = 0.003), and moderate-to-severe CSVD burden (12.55; p = 0.033), ipsilaterally, respectively independent of contralateral WMHs, CMI(s), and CSVD burden. EPVSs and CMBs were comparable between the two hemispheres, with no association found with the hemodynamic metrics. Discussion and conclusion: There are more severe WMHs and CMI(s) in the hemisphere ipsilateral than contralateral to sICAD. The hemodynamic significance of sICAD lesions was independently associated with severities of WMHs and CMI(s) ipsilaterally.

KW - Cerebral small vessel disease

KW - hemodynamics

KW - intracranial atherosclerotic disease

KW - white matter hyperintensity

KW - cortical microinfarct

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JF - European Stroke Journal

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Hemodynamic significance of intracranial atherosclerotic disease and ipsilateral imaging markers of cerebral small vessel disease

Abstract

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