Skip to main content
Top
Published in: European Radiology 9/2022

02-04-2022 | Cerebral Small Vessel Disease | Head and Neck

Carotid vulnerable plaque coexisting with cerebral small vessel disease and acute ischemic stroke: a Chinese Atherosclerosis Risk Evaluation study

Authors: Jin Li, Hengqu Wu, Hailun Hang, Beibei Sun, Huilin Zhao, Zengai Chen, Yan Zhou, Jianrong Xu, Jinmei Chen, Dan Zhou, Xihai Zhao, Chun Yuan

Published in: European Radiology | Issue 9/2022

Login to get access

Abstract

Objectives

We aimed to investigate the associations between carotid vulnerable plaque features coexisting with cerebral small vessel diseases (CSVDs) and acute ischemic stroke (AIS) and, furthermore, to determine whether coexisting diseases had a stronger association with AIS than a single disease.

Methods

Patients with cerebrovascular symptoms and carotid plaque were recruited from the cross-sectional, multicenter CARE-II study. The population was divided into two groups (AIS and transient ischemic stroke (TIA)). MRI features of carotid plaques (including luminal stenosis and plaque vulnerabilities) and CSVDs (such as white matter hyperintensities (WMHs) and lacunes) were evaluated. Coexisting diseases were defined as the presence of at least one carotid plaque features and one or more CSVDs feature. Multivariate logistic regression was performed to examine the associations between coexisting diseases and AIS.

Results

Of the recruited 634 patients (mean age: 59.1 ± 11.3 years; 429 males), 312 (49.2%) patients had AIS. These subjects had a higher prevalence of carotid vulnerable plaques, lacunes, and moderate-to-severe WMHs (a total Fazekas score of 3–6) than those with TIA (42.6% vs. 29.5%, 59.6% vs. 26.4%, 69.9% vs. 60.6%, respectively, all p < 0.05). Multivariate analysis revealed that carotid plaque features coexisting with lacunes or moderate-to-severe WMHs had a stronger association with AIS compared to carotid lesions alone (all p < 0.05) (i.e., vulnerable plaque coexisting with lacunes vs. vulnerable plaque alone, adjusted odds ratio: 3.67 vs. 1.62).

Conclusions

Carotid vulnerable plaque features coexisting with CSVDs, particularly lacunes, had a stronger association with AIS compared to carotid lesions alone in a large, symptomatic, cohort.

Trial registration

Clinical trial registration URL: http://​www.​clinicaltrials.​gov, unique identifier: NCT02017756

Key Points

• Carotid vulnerable plaque features coexisting with cerebral small vessel diseases, such as lacunes, had a stronger association with acute ischemic stroke compared to single diseases in symptomatic patients.
• A comprehensive assessment of coexisting cerebrovascular diseases may help stratify the risk of acute ischemic stroke.
Literature
1.
go back to reference GBD 2016 Neurology Collaborators (2019) Global, regional, and national burden of stroke, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol 18:439–458 GBD 2016 Neurology Collaborators (2019) Global, regional, and national burden of stroke, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol 18:439–458
2.
go back to reference Adams HP Jr, Bendixen BH, Kappelle LJ et al (1993) Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of Org 10172 in Acute Stroke Treatment. Stroke 24:35–41CrossRef Adams HP Jr, Bendixen BH, Kappelle LJ et al (1993) Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of Org 10172 in Acute Stroke Treatment. Stroke 24:35–41CrossRef
3.
go back to reference Saba L, Saam T, Jäger HR et al (2019) Imaging biomarkers of vulnerable carotid plaques for stroke risk prediction and their potential clinical implications. Lancet Neurol 18:559–572CrossRef Saba L, Saam T, Jäger HR et al (2019) Imaging biomarkers of vulnerable carotid plaques for stroke risk prediction and their potential clinical implications. Lancet Neurol 18:559–572CrossRef
4.
go back to reference Li J, Li D, Yang D et al (2020) Irregularity of carotid plaque surface predicts subsequent vascular event: a MRI study. J Magn Reson Imaging 52:185–194CrossRef Li J, Li D, Yang D et al (2020) Irregularity of carotid plaque surface predicts subsequent vascular event: a MRI study. J Magn Reson Imaging 52:185–194CrossRef
5.
go back to reference Pantoni L (2010) Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 9:689–701CrossRef Pantoni L (2010) Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 9:689–701CrossRef
6.
go back to reference Cannistraro RJ, Badi M, Eidelman BH, Dickson DW, Middlebrooks EH, Meschia JF (2019) CNS small vessel disease: a clinical review. Neurology 92:1146–1156CrossRef Cannistraro RJ, Badi M, Eidelman BH, Dickson DW, Middlebrooks EH, Meschia JF (2019) CNS small vessel disease: a clinical review. Neurology 92:1146–1156CrossRef
7.
go back to reference Rensma SP, van Sloten TT, Launer LJ, Stehouwer CDA (2018) Cerebral small vessel disease and risk of incident stroke, dementia and depression, and all-cause mortality: a systematic review and meta-analysis. Neurosci Biobehav Rev 90:164–173CrossRef Rensma SP, van Sloten TT, Launer LJ, Stehouwer CDA (2018) Cerebral small vessel disease and risk of incident stroke, dementia and depression, and all-cause mortality: a systematic review and meta-analysis. Neurosci Biobehav Rev 90:164–173CrossRef
8.
go back to reference Buyck JF, Dufouil C, Mazoyer B et al (2009) Cerebral white matter lesions are associated with the risk of stroke but not with other vascular events: the 3-City Dijon Study. Stroke 40:2327–2331CrossRef Buyck JF, Dufouil C, Mazoyer B et al (2009) Cerebral white matter lesions are associated with the risk of stroke but not with other vascular events: the 3-City Dijon Study. Stroke 40:2327–2331CrossRef
9.
go back to reference Altaf N, Morgan PS, Moody A, MacSweeney ST, Gladman JR, Auer DP (2008) Brain white matter hyperintensities are associated with carotid intraplaque hemorrhage. Radiology 248:202–209CrossRef Altaf N, Morgan PS, Moody A, MacSweeney ST, Gladman JR, Auer DP (2008) Brain white matter hyperintensities are associated with carotid intraplaque hemorrhage. Radiology 248:202–209CrossRef
10.
go back to reference Altaf N, Daniels L, Morgan PS et al (2006) Cerebral white matter hyperintense lesions are associated with unstable carotid plaques. Eur J Vasc Endovasc Surg 31:8–13CrossRef Altaf N, Daniels L, Morgan PS et al (2006) Cerebral white matter hyperintense lesions are associated with unstable carotid plaques. Eur J Vasc Endovasc Surg 31:8–13CrossRef
11.
go back to reference Conijn MM, Kloppenborg RP, Algra A et al (2011) Cerebral small vessel disease and risk of death, ischemic stroke, and cardiac complications in patients with atherosclerotic disease: the Second Manifestations of ARTerial disease-Magnetic Resonance (SMART-MR) study. Stroke 42:3105–3109CrossRef Conijn MM, Kloppenborg RP, Algra A et al (2011) Cerebral small vessel disease and risk of death, ischemic stroke, and cardiac complications in patients with atherosclerotic disease: the Second Manifestations of ARTerial disease-Magnetic Resonance (SMART-MR) study. Stroke 42:3105–3109CrossRef
12.
go back to reference Gerdes VE, Kwa VI, ten Cate H et al (2006) Cerebral white matter lesions predict both ischemic strokes and myocardial infarctions in patients with established atherosclerotic disease. Atherosclerosis 186:166–172CrossRef Gerdes VE, Kwa VI, ten Cate H et al (2006) Cerebral white matter lesions predict both ischemic strokes and myocardial infarctions in patients with established atherosclerotic disease. Atherosclerosis 186:166–172CrossRef
13.
go back to reference Zhao X, Li R, Hippe DS et al (2017) Chinese Atherosclerosis Risk Evaluation (CARE II) study: a novel cross-sectional, multicentre study of the prevalence of high-risk atherosclerotic carotid plaque in Chinese patients with ischaemic cerebrovascular events-design and rationale. Stroke Vasc Neurol 2:15–20CrossRef Zhao X, Li R, Hippe DS et al (2017) Chinese Atherosclerosis Risk Evaluation (CARE II) study: a novel cross-sectional, multicentre study of the prevalence of high-risk atherosclerotic carotid plaque in Chinese patients with ischaemic cerebrovascular events-design and rationale. Stroke Vasc Neurol 2:15–20CrossRef
14.
go back to reference Underhill HR, Yarnykh VL, Hatsukami TS et al (2008) Carotid plaque morphology and composition: initial comparison between 1.5- and 3.0-T magnetic field strengths. Radiology 248:550–560CrossRef Underhill HR, Yarnykh VL, Hatsukami TS et al (2008) Carotid plaque morphology and composition: initial comparison between 1.5- and 3.0-T magnetic field strengths. Radiology 248:550–560CrossRef
15.
go back to reference Yuan C, Mitsumori LM, Ferguson MS et al (2001) In vivo accuracy of multispectral magnetic resonance imaging for identifying lipid-rich necrotic cores and intraplaque hemorrhage in advanced human carotid plaques. Circulation 104:2051–2056CrossRef Yuan C, Mitsumori LM, Ferguson MS et al (2001) In vivo accuracy of multispectral magnetic resonance imaging for identifying lipid-rich necrotic cores and intraplaque hemorrhage in advanced human carotid plaques. Circulation 104:2051–2056CrossRef
16.
go back to reference Hatsukami TS, Ross R, Polissar NL, Yuan C (2000) Visualization of fibrous cap thickness and rupture in human atherosclerotic carotid plaque in vivo with high-resolution magnetic resonance imaging. Circulation 102:959–964CrossRef Hatsukami TS, Ross R, Polissar NL, Yuan C (2000) Visualization of fibrous cap thickness and rupture in human atherosclerotic carotid plaque in vivo with high-resolution magnetic resonance imaging. Circulation 102:959–964CrossRef
17.
go back to reference Chu B, Ferguson MS, Underhill H et al (2005) Images in cardiovascular medicine. Detection of carotid atherosclerotic plaque ulceration, calcification, and thrombosis by multicontrast weighted magnetic resonance imaging. Circulation 112:e3–e4CrossRef Chu B, Ferguson MS, Underhill H et al (2005) Images in cardiovascular medicine. Detection of carotid atherosclerotic plaque ulceration, calcification, and thrombosis by multicontrast weighted magnetic resonance imaging. Circulation 112:e3–e4CrossRef
18.
go back to reference Saba L, Anzidei M, Marincola BC et al (2014) Imaging of the carotid artery vulnerable plaque. Cardiovasc Intervent Radiol 37:572–585CrossRef Saba L, Anzidei M, Marincola BC et al (2014) Imaging of the carotid artery vulnerable plaque. Cardiovasc Intervent Radiol 37:572–585CrossRef
19.
go back to reference Chimowitz MI, Lynn MJ, Howlett-Smith H et al (2005) Comparison of warfarin and aspirin for symptomatic intracranial arterial stenosis. N Engl J Med 352:1305–1316CrossRef Chimowitz MI, Lynn MJ, Howlett-Smith H et al (2005) Comparison of warfarin and aspirin for symptomatic intracranial arterial stenosis. N Engl J Med 352:1305–1316CrossRef
20.
go back to reference Inzitari D, Eliasziw M, Gates P et al (2000) The causes and risk of stroke in patients with asymptomatic internal-carotid-artery stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med 342:1693–1700CrossRef Inzitari D, Eliasziw M, Gates P et al (2000) The causes and risk of stroke in patients with asymptomatic internal-carotid-artery stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med 342:1693–1700CrossRef
21.
go back to reference Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA (1987) MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol 149:351–356CrossRef Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA (1987) MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol 149:351–356CrossRef
22.
go back to reference Kim GM, Park KY, Avery R et al (2014) Extensive leukoaraiosis is associated with high early risk of recurrence after ischemic stroke. Stroke 45:479–485CrossRef Kim GM, Park KY, Avery R et al (2014) Extensive leukoaraiosis is associated with high early risk of recurrence after ischemic stroke. Stroke 45:479–485CrossRef
23.
go back to reference Patti J, Helenius J, Puri AS, Henninger N (2016) White matter hyperintensity-adjusted critical infarct thresholds to predict a favorable 90-day outcome. Stroke 47:2526–2533CrossRef Patti J, Helenius J, Puri AS, Henninger N (2016) White matter hyperintensity-adjusted critical infarct thresholds to predict a favorable 90-day outcome. Stroke 47:2526–2533CrossRef
24.
go back to reference Wardlaw JM, Smith EE, Biessels GJ et al (2013) Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol 12:822–838CrossRef Wardlaw JM, Smith EE, Biessels GJ et al (2013) Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol 12:822–838CrossRef
25.
go back to reference Klarenbeek P, van Oostenbrugge RJ, Rouhl RP, Knottnerus IL, Staals J (2013) Ambulatory blood pressure in patients with lacunar stroke: association with total MRI burden of cerebral small vessel disease. Stroke 44:2995–2999CrossRef Klarenbeek P, van Oostenbrugge RJ, Rouhl RP, Knottnerus IL, Staals J (2013) Ambulatory blood pressure in patients with lacunar stroke: association with total MRI burden of cerebral small vessel disease. Stroke 44:2995–2999CrossRef
26.
go back to reference Takaya N, Yuan C, Chu B et al (2006) Association between carotid plaque characteristics and subsequent ischemic cerebrovascular events: a prospective assessment with MRI—initial results. Stroke 37:818–823CrossRef Takaya N, Yuan C, Chu B et al (2006) Association between carotid plaque characteristics and subsequent ischemic cerebrovascular events: a prospective assessment with MRI—initial results. Stroke 37:818–823CrossRef
27.
go back to reference Zhao H, Zhao X, Liu X et al (2013) Association of carotid atherosclerotic plaque features with acute ischemic stroke: a magnetic resonance imaging study. Eur J Radiol 82:e465–e470CrossRef Zhao H, Zhao X, Liu X et al (2013) Association of carotid atherosclerotic plaque features with acute ischemic stroke: a magnetic resonance imaging study. Eur J Radiol 82:e465–e470CrossRef
28.
go back to reference Gupta A, Giambrone AE, Gialdini G et al (2016) Silent brain infarction and risk of future stroke: a systematic review and meta-analysis. Stroke 47:719–725CrossRef Gupta A, Giambrone AE, Gialdini G et al (2016) Silent brain infarction and risk of future stroke: a systematic review and meta-analysis. Stroke 47:719–725CrossRef
29.
go back to reference Ryu WS, Schellingerhout D, Hong KS et al (2019) White matter hyperintensity load on stroke recurrence and mortality at 1 year after ischemic stroke. Neurology 93:e578–e589CrossRef Ryu WS, Schellingerhout D, Hong KS et al (2019) White matter hyperintensity load on stroke recurrence and mortality at 1 year after ischemic stroke. Neurology 93:e578–e589CrossRef
30.
go back to reference Nam KW, Kwon HM, Lim JS, Han MK, Nam H, Lee YS (2017) The presence and severity of cerebral small vessel disease increases the frequency of stroke in a cohort of patients with large artery occlusive disease. PLoS One 12:e0184944CrossRef Nam KW, Kwon HM, Lim JS, Han MK, Nam H, Lee YS (2017) The presence and severity of cerebral small vessel disease increases the frequency of stroke in a cohort of patients with large artery occlusive disease. PLoS One 12:e0184944CrossRef
31.
go back to reference Shi H, Shao S, Wang G et al (2020) Bilaterally asymmetric associations between extracranial carotid artery atherosclerosis and ipsilateral middle cerebral artery stenosis in symptomatic patients: a CARE-II study. Arterioscler Thromb Vasc Biol 40:2965–2974. Shi H, Shao S, Wang G et al (2020) Bilaterally asymmetric associations between extracranial carotid artery atherosclerosis and ipsilateral middle cerebral artery stenosis in symptomatic patients: a CARE-II study. Arterioscler Thromb Vasc Biol 40:2965–2974.
32.
go back to reference Akoudad S, Portegies ML, Koudstaal PJ et al (2015) Cerebral microbleeds are associated with an increased risk of stroke: the Rotterdam study. Circulation 132:509–516. Akoudad S, Portegies ML, Koudstaal PJ et al (2015) Cerebral microbleeds are associated with an increased risk of stroke: the Rotterdam study. Circulation 132:509–516.
33.
go back to reference Lau KK, Li L, Lovelock CE et al (2017) Clinical correlates, ethnic differences, and prognostic implications of perivascular spaces in transient ischemic attack and ischemic stroke. Stroke 48:1470–1477. Lau KK, Li L, Lovelock CE et al (2017) Clinical correlates, ethnic differences, and prognostic implications of perivascular spaces in transient ischemic attack and ischemic stroke. Stroke 48:1470–1477.
Metadata
Title
Carotid vulnerable plaque coexisting with cerebral small vessel disease and acute ischemic stroke: a Chinese Atherosclerosis Risk Evaluation study
Authors
Jin Li
Hengqu Wu
Hailun Hang
Beibei Sun
Huilin Zhao
Zengai Chen
Yan Zhou
Jianrong Xu
Jinmei Chen
Dan Zhou
Xihai Zhao
Chun Yuan
Publication date
02-04-2022
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 9/2022
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-022-08757-9

Other articles of this Issue 9/2022

European Radiology 9/2022 Go to the issue