Carotid and intracranial imaging play an essential role in the comprehensive evaluation and prevention for stroke patients. High-resolution vessel wall magnetic resonance imaging (HR VW-MRI) has been applied in carotid and intracranial arteries with optimal ability in displaying the features of various vascular diseases. Recent advanced MRI techniques can not only help in the differential diagnosis of vascular diseases but can also provide information on pathogenesis exploration of underlying mechanisms, follow-up monitoring, and determination of prognosis for patients with cerebral strokes. The aim of this article was to review the applications of HR VW-MRI in various pathologic conditions of carotid and intracranial arterial imaging.
El-KoussyMSchrothGBrekenfeldC, et al.
Imaging of acute ischemic stroke.Eur Neurol2014;
72:309–316.
2.
NederkoornPJvan der GraafY, andHuninkMG.Duplex ultrasound and magnetic resonance angiography compared with digital subtraction angiography in carotid artery stenosis: a systematic review.Stroke2003;
34:1324–1332.
3.
MarklMSchnellSWuC, et al.
Advanced flow MRI: emerging techniques and applications.Clin Radiol2016;
71:779–795.
4.
TanHWChenXMaingardJ, et al.
Intracranial vessel wall imaging with magnetic resonance imaging: current techniques and applications.World Neurosurg2018;
112:186–198.
5.
WatanabeYNagayamaMSugaT, et al.
Characterization of atherosclerotic plaque of carotid arteries with histopathological correlation: vascular wall MR imaging vs. color Doppler ultrasonography (US).J Magn Reson Imaging2008;
28:478–485.
6.
XiaZYangHYuanX, et al.
High-resolution magnetic resonance imaging of carotid atherosclerotic plaques - a correlation study with histopathology.Vasa2017;
46:283–290.
7.
YarnykhVLYuanC.T1-insensitive flow suppression using quadruple inversion-recovery.Magn Reson Med2002;
48:899–905.
8.
SabaLYuanCHatsukamiTS, et al.
Carotid artery wall imaging: perspective and guidelines from the ASNR Vessel Wall Imaging Study Group and Expert Consensus Recommendations of the American Society of Neuroradiology.Am J Neuroradiol2018;
39:E9–e31.
9.
Mossa-BashaMAlexanderMGaddikeriS, et al.
Vessel wall imaging for intracranial vascular disease evaluation.J Neurointerv Surg2016;
8:1154–1159.
10.
QiaoYSteinmanDAQinQ, et al.
Intracranial arterial wall imaging using three-dimensional high isotropic resolution black blood MRI at 3.0 Tesla.J Magn Reson Imaging2011;
34:22–30.
11.
FanZZhangZChungYC, et al.
Carotid arterial wall MRI at 3T using 3D variable-flip-angle turbo spin-echo (TSE) with flow-sensitive dephasing (FSD).J Magn Reson Imaging2010;
31:645–654.
12.
MakhijaniMKBaluNYamadaK, et al.
Accelerated 3D MERGE carotid imaging using compressed sensing with a hidden Markov tree model.J Magn Reson Imaging2012;
36:1194–1202.
13.
WangJZhaoHHippeDS, et al.
Simultaneous noncontrast angiography and intraplaque hemorrhage (SNAP) imaging for carotid atherosclerotic disease evaluation.Magn Reson Med2013;
69:337–345.
14.
OtaHYarnykhVLFergusonMS, et al.
Carotid intraplaque hemorrhage imaging at 3.0-T MR imaging: comparison of the diagnostic performance of three T1-weighted sequences.Radiology2010;
254:551–563.
15.
LiDZhaoHChenX, et al.
Identification of intraplaque haemorrhage in carotid artery by simultaneous non-contrast angiography and intraPlaque haemorrhage (SNAP) imaging: a magnetic resonance vessel wall imaging study.Eur Radiol2018;
28:1681–1686.
16.
HarteveldAADe CockerLJDielemanN, et al.
High-resolution postcontrast time-of-flight MR angiography of intracranial perforators at 7.0 Tesla.PLoS One2015;
10:e0121051.
17.
ConijnMMHendrikseJZwanenburgJJ, et al.
Perforating arteries originating from the posterior communicating artery: a 7.0-Tesla MRI study.Eur Radiol2009;
19:2986–2992.
18.
ChoZHKangCKHanJY, et al.
Observation of the lenticulostriate arteries in the human brain in vivo using 7.0T MR angiography.Stroke2008;
39:1604–1606.
19.
FairheadJFRothwellPM.The need for urgency in identification and treatment of symptomatic carotid stenosis is already established.Cerebrovasc Dis2005;
19:355–358.
20.
EliasziwMKennedyJHillMD, et al.
Early risk of stroke after a transient ischemic attack in patients with internal carotid artery disease.CMAJ2004;
170:1105–1109.
21.
GuptaABaradaranHSchweitzerAD, et al.
Carotid plaque MRI and stroke risk: a systematic review and meta-analysis.Stroke2013;
44:3071–3077.
22.
SabaLAnzideiMMarincolaBC, et al.
Imaging of the carotid artery vulnerable plaque.Cardiovasc Intervent Radiol2014;
37:572–585.
23.
Lopez GonzalezMRFooSYHolmesWM, et al.
Atherosclerotic carotid plaque composition: A 3T and 7T MRI-histology correlation study.J Neuroimaging2016;
26:406–413.
24.
FabianoSMancinoSStefaniniM, et al.
High-resolution multicontrast-weighted MR imaging from human carotid endarterectomy specimens to assess carotid plaque components.Eur Radiol2008;
18:2912–2921.
25.
TakayaNYuanCChuB, et al.
Association between carotid plaque characteristics and subsequent ischemic cerebrovascular events: a prospective assessment with MRI–initial results.Stroke2006;
37:818–823.
26.
ZhaoHZhaoXLiuX, et al.
Association of carotid atherosclerotic plaque features with acute ischemic stroke: a magnetic resonance imaging study.Eur J Radiol2013;
82:e465–470.
27.
SaamTHetterichHHoffmannV, et al.
Meta-analysis and systematic review of the predictive value of carotid plaque hemorrhage on cerebrovascular events by magnetic resonance imaging.J Am Coll Cardiol2013;
62:1081–1091.
28.
SpagnoliLGMaurielloASangiorgiG, et al.
Extracranial thrombotically active carotid plaque as a risk factor for ischemic stroke.JAMA2004;
292:1845–1852.
29.
RedgraveJNLovettJKGallagherPJ, et al.
Histological assessment of 526 symptomatic carotid plaques in relation to the nature and timing of ischemic symptoms: the Oxford plaque study.Circulation2006;
113:2320–2328.
30.
RaiSThalerDESalehiP, et al.
More to atherosclerosis than stenosis: symptomatic carotid artery with intraplaque hemorrhage.Stroke2017;
48:e104–e107.
31.
TreimanGSMcNallyJSKimSE, et al.
Correlation of carotid intraplaque hemorrhage and stroke using 1.5 T and 3 T MRI.Magn Reson Insights2015;
8:1–8.
32.
GaoPChenZQBaoYH, et al.
Correlation between carotid intraplaque hemorrhage and clinical symptoms: systematic review of observational studies.Stroke2007;
38:2382–2390.
33.
AltafNDanielsLMorganPS, et al.
Detection of intraplaque hemorrhage by magnetic resonance imaging in symptomatic patients with mild to moderate carotid stenosis predicts recurrent neurological events.J Vasc Surg2008;
47:337–342.
34.
BrinjikjiWLehmanVTHustonJ3rd, et al.
The association between carotid intraplaque hemorrhage and outcomes of carotid stenting: a systematic review and meta-analysis.J Neurointerv Surg2017;
9:837–842.
35.
SunJZhaoXQBaluN, et al.
Carotid plaque lipid content and fibrous cap status predict systemic CV outcomes: the MRI substudy in AIM-HIGH.JACC Cardiovasc Imaging2017;
10:241–249.
36.
KweeRMvan OostenbruggeRJMessWH, et al.
Carotid plaques in transient ischemic attack and stroke patients: one-year follow-up study by magnetic resonance imaging.Invest Radiol2010;
45:803–809.
37.
LinRChenSLiuG, et al.
Association between carotid atherosclerotic plaque calcification and intraplaque hemorrhage: a magnetic resonance imaging study.Arterioscler Thromb Vasc Biol2017;
37:1228–1233.
38.
YuWUnderhillHRFergusonMS, et al.
The added value of longitudinal black-blood cardiovascular magnetic resonance angiography in the cross sectional identification of carotid atherosclerotic ulceration.J Cardiovasc Magn Reson2009;
11:31.
39.
SitzerMMullerWSieblerM, et al.
Plaque ulceration and lumen thrombus are the main sources of cerebral microemboli in high-grade internal carotid artery stenosis.Stroke1995;
26:1231–1233.
40.
MitchellCCWilbrandSMKunduB, et al.
Transcranial Doppler and microemboli detection: relationships to symptomatic status and histopathology findings.Ultrasound Med Biol2017;
43:1861–1867.
41.
GrimmJMSchindlerAFreilingerT, et al.
Comparison of symptomatic and asymptomatic atherosclerotic carotid plaques using parallel imaging and 3 T black-blood in vivo CMR.J Cardiovasc Magn Reson2013;
15:44.
42.
ZhaoXHippeDSLiR, et al.
Prevalence and characteristics of carotid artery high-risk atherosclerotic plaques in Chinese patients with cerebrovascular symptoms: a Chinese Atherosclerosis Risk Evaluation II Study. J Am Heart Assoc2017;
6:e005831.
43.
MandellDMMossa-BashaMQiaoY, et al.
Intracranial vessel wall MRI: principles and expert consensus recommendations of the American Society of Neuroradiology.Am J Neuroradiol2017;
38:218–229.
44.
YangWJFisherMZhengL, et al.
Histological characteristics of intracranial atherosclerosis in a Chinese population: a postmortem study. Front Neurol2017;
8:488.
45.
ChenXYWongKSLamWW, et al.
Middle cerebral artery atherosclerosis: histological comparison between plaques associated with and not associated with infarct in a postmortem study.Cerebrovasc Dis2008;
25:74–80.
46.
YangWQHuangBLiuXT, et al.
Reproducibility of high-resolution MRI for the middle cerebral artery plaque at 3T.Eur J Radiol2014;
83:e49–55.
47.
ZhangXZhuCPengW, et al.
Scan-rescan reproducibility of high resolution magnetic resonance imaging of atherosclerotic plaque in the middle cerebral artery.PLoS One2015;
10:e0134913.
48.
XuWHLiMLGaoS, et al.
Middle cerebral artery intraplaque hemorrhage: prevalence and clinical relevance.Ann Neurol2012;
71:195–198.
49.
Sui B, Gao P, Lin Y, et al. Distribution and features of middle cerebral artery atherosclerotic plaques in symptomatic patients: a 3.0 T high-resolution MRI study. Neurol Res 2015; 37: 391–396.
50.
GuptaABaradaranHAl-DasuqiK, et al.
Gadolinium enhancement in intracranial atherosclerotic plaque and ischemic stroke: a systematic review and meta-analysis. J Am Heart Assoc2016;
5:e003816.
51.
RyuCWJahngGHShinHS.Gadolinium enhancement of atherosclerotic plaque in the middle cerebral artery: relation to symptoms and degree of stenosis.Am J Neuroradiol2014;
35:2306–2310.
52.
QiaoYZeilerSRMirbagheriS, et al.
Intracranial plaque enhancement in patients with cerebrovascular events on high-spatial-resolution MR images.Radiology2014;
271:534–542.
53.
SkarpathiotakisMMandellDMSwartzRH, et al.
Intracranial atherosclerotic plaque enhancement in patients with ischemic stroke.Am J Neuroradiol2013;
34:299–304.
54.
VakilPVranicJHurleyMC, et al.
T1 gadolinium enhancement of intracranial atherosclerotic plaques associated with symptomatic ischemic presentations.Am J Neuroradiol2013;
34:2252–2258.
55.
AbeASekineTSakamotoY, et al.
Contrast-enhanced high-resolution MRI for evaluating time course changes in middle cerebral artery plaques.J Nippon Med Sch2018;
85:28–33.
56.
van der KolkAGZwanenburgJJBrundelM, et al.
Distribution and natural course of intracranial vessel wall lesions in patients with ischemic stroke or TIA at 7.0 Tesla MRI.Eur Radiol2015;
25:1692–1700.
57.
KronerESvan VelzenJEBoogersMJ, et al.
Positive remodeling on coronary computed tomography as a marker for plaque vulnerability on virtual histology intravascular ultrasound.Am J Cardiol2011;
107:1725–1729.
58.
PhinikaridouAAndiaMEIndermuehleA, et al.
Vascular remodeling and plaque vulnerability in a rabbit model of atherosclerosis: comparison of delayed-enhancement MR imaging with an elastin-specific contrast agent and unenhanced black-blood MR imaging.Radiology2014;
271:390–399.
59.
XuWHLiMLGaoS, et al.
In vivo high-resolution MR imaging of symptomatic and asymptomatic middle cerebral artery atherosclerotic stenosis.Atherosclerosis2010;
212:507–511.
60.
ZhaoDLDengGXieB, et al.
High-resolution MRI of the vessel wall in patients with symptomatic atherosclerotic stenosis of the middle cerebral artery.J Clin Neurosci2015;
22:700–704.
61.
ChungGHKwakHSHwangSB, et al.
High resolution MR imaging in patients with symptomatic middle cerebral artery stenosis.Eur J Radiol2012;
81:4069–4074.
62.
Mossa-BashaMShibataDKHallamDK, et al.
Added value of vessel wall magnetic resonance imaging for differentiation of nonocclusive intracranial vasculopathies.Stroke2017;
48:3026–3033.
63.
DebetteSCompterALabeyrieMA, et al.
Epidemiology, pathophysiology, diagnosis, and management of intracranial artery dissection.Lancet Neurol2015;
14:640–654.
64.
BachmannRNassensteinIKooijmanH, et al.
High-resolution magnetic resonance imaging (MRI) at 3.0 Tesla in the short-term follow-up of patients with proven cervical artery dissection.Invest Radiol2007;
42:460–466.
65.
NaggaraOLouilletFTouzeE, et al.
Added value of high-resolution MR imaging in the diagnosis of vertebral artery dissection.Am J Neuroradiol2010;
31:1707–1712.
66.
HanMRimNJLeeJS, et al.
Feasibility of high-resolution MR imaging for the diagnosis of intracranial vertebrobasilar artery dissection.Eur Radiol2014;
24:3017–3024.
67.
ChoiJWHanMHongJM, et al.
Feasibility of improved motion-sensitized driven-equilibrium (iMSDE) prepared 3D T1-weighted imaging in the diagnosis of vertebrobasilar artery dissection.J Neuroradiol2018;
45:186–191.
68.
KimTWChoiHSKooJ, et al.
Intramural hematoma detection by susceptibility-weighted imaging in intracranial vertebral artery dissection.Cerebrovasc Dis2013;
36:292–298.
69.
NakagawaKTouhoHMorisakoT, et al.
Long-term follow-up study of unruptured vertebral artery dissection: clinical outcomes and serial angiographic findings.J Neurosurg2000;
93:19–25.
70.
ObusezECHuiFHajj-AliRA, et al.
High-resolution MRI vessel wall imaging: spatial and temporal patterns of reversible cerebral vasoconstriction syndrome and central nervous system vasculitis.Am J Neuroradiol2014;
35:1527–1532.
71.
KatoYTerashimaMOhigashiH, et al.
Vessel wall inflammation of Takayasu arteritis detected by contrast-enhanced magnetic resonance imaging: association with disease distribution and activity.PLoS One2015;
10:e0145855.
72.
SunYMaLJiZ, et al.
Value of whole-body contrast-enhanced magnetic resonance angiography with vessel wall imaging in quantitative assessment of disease activity and follow-up examination in Takayasu’s arteritis.Clin Rheumatol2016;
35:685–693.
73.
JiangLLiDYanF, et al.
Evaluation of Takayasu arteritis activity by delayed contrast-enhanced magnetic resonance imaging.Int J Cardiol2012;
155:262–267.
74.
MillerTRShivashankarRMossa-BashaM, et al.
Reversible cerebral vasoconstriction syndrome, part 1: epidemiology, pathogenesis, and clinical course.Am J Neuroradiol2015;
36:1392–1399.
75.
MandellDMMatoukCCFarbRI, et al.
Vessel wall MRI to differentiate between reversible cerebral vasoconstriction syndrome and central nervous system vasculitis: preliminary results.Stroke2012;
43:860–862.
76.
Mossa-BashaMHwangWDDe HavenonA, et al.
Multicontrast high-resolution vessel wall magnetic resonance imaging and its value in differentiating intracranial vasculopathic processes.Stroke2015;
46:1567–1573.
77.
ChenCYChenSPFuhJL, et al.
Vascular wall imaging in reversible cerebral vasoconstriction syndrome - a 3-T contrast-enhanced MRI study. J Headache Pain2018;
19:74.
78.
TakagiYHermantoYTakahashiJC, et al.
Histopathological characteristics of distal middle cerebral artery in adult and pediatric patients with Moyamoya disease.Neurol Med Chir (Tokyo)2016;
56:345–349.
79.
TakagiYKikutaKNozakiK, et al.
Histological features of middle cerebral arteries from patients treated for Moyamoya disease.Neurol Med Chir (Tokyo)2007;
47:1–4.
80.
KurodaSHoukinK.Moyamoya disease: current concepts and future perspectives.Lancet Neurol2008;
7:1056–1066.
81.
MikamiTNoshiroSKomatsuK, et al.
Vascular remodeling of the circle of Willis in moyamoya disease.Neurol Res2015;
37:880–885.
82.
KakuYMoriokaMOhmoriY, et al.
Outer-diameter narrowing of the internal carotid and middle cerebral arteries in moyamoya disease detected on 3D constructive interference in steady-state MR image: is arterial constrictive remodeling a major pathogenesis?Acta Neurochir (Wien)2012;
154:2151–2157.
83.
YuanMLiuZQWangZQ, et al.
High-resolution MR imaging of the arterial wall in moyamoya disease.Neurosci Lett2015;
584:77–82.
84.
KimJMJungKHSohnCH, et al.
High-resolution MR technique can distinguish moyamoya disease from atherosclerotic occlusion.Neurology2013;
80:775–776.
85.
YamashitaMOkaK, andTanakaK.Histopathology of the brain vascular network in moyamoya disease.Stroke1983;
14:50–58.
86.
RyooSChaJKimSJ, et al.
High-resolution magnetic resonance wall imaging findings of Moyamoya disease.Stroke2014;
45:2457–2460.
87.
FuQGuanSLiuC, et al.
Clinical significance of circumferential aneurysmal wall enhancement in symptomatic patients with unruptured intracranial aneurysms: a high-resolution MRI study.Clin Neuroradiol2018;
28:509–514.
88.
WangGXWenLLeiS, et al.
Wall enhancement ratio and partial wall enhancement on MRI associated with the rupture of intracranial aneurysms.J Neurointerv Surg2018;
10:566–570.
89.
LehmanVTBrinjikjiWMossa-BashaM, et al.
Conventional and high-resolution vessel wall MRI of intracranial aneurysms: current concepts and new horizons.J Neurosurg2018;
128:969–981.
