To review the current state of the art and future development of intracranial vessel wall imaging.
Methods
Recent literature review and expert opinion about intracranial arterial wall imaging.
Results
Intracranial large artery diseases represent an important cause of stroke and vascular cognitive impairment worldwide. Our traditional understanding of intracranial large artery diseases is based on the observation of luminal narrowing or occlusion with angiographic or ultrasound techniques. Recently, novel imaging techniques have made the intracranial artery wall accessible for noninvasive visualization. The main advantage of vessel-wall imaging as compared to conventional imaging techniques for visualization of intracranial arteries is the ability to detect vessel wall changes even before they get to cause any significant luminal stenosis. This diagnostic capacity is provoking a revolutionary change in the way we see the intracranial circulation. In this article, we will review the current state of magnetic resonance imaging and computed tomography-based intracranial arterial wall imaging, focusing on technical considerations and their clinical applicability. Moreover, we will provide the readers with our vision on the future development of vessel-wall imaging techniques.
Conclusion
Intracranial arterial wall imaging methods are gaining increasing potential to impact the diagnosis and treatment of patients with cerebrovascular diseases.
GorelickPWongKSLiuL. Epidemiology. Front Neurol Neurosci2017; 40: 34–46. .
2.
ArenillasJF. Intracranial atherosclerosis: current concepts. Stroke2011; 42: S20–S23.
3.
FanZYangQDengZ, et al.Whole-brain intracranial vessel wall imaging at 3 Tesla using cerebrospinal fluid–attenuated T1-weighted 3D turbo spin echo. Magn Reson Med2017; 77: 1142–1150.
4.
SkarpathiotakisMMandellDMSwartzRHTomlinsonGMikulisDJ. Intracranial atherosclerotic plaque enhancement in patients with ischemic stroke. AJNR Am J Neuroradiol2013; 34: 299–304.
5.
van der KolkAGHendrikseJZwanenburgJJMVisserFLuijtenPR. Clinical applications of 7 T MRI in the brain. Eur J Radiol2013; 82: 708–718.
6.
van der KolkAGZwanenburgJJMBrundelM, et al.Intracranial vessel wall imaging at 7.0-T MRI. Stroke2011; 42: 2478–2484.
7.
LindenholzAvan der KolkAGZwanenburgJJMHendrikseJ. The use and pitfalls of intracranial vessel wall imaging: how we do it. Radiology2018; 286: 12–28.
8.
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.
9.
EdelmanRRChienDKimD. Fast selective black blood MR imaging. Radiology1991; 181: 655–660.
10.
WangJYarnykhVLYuanC. Enhanced image quality in black-blood MRI using the improved motion-sensitized driven-equilibrium (iMSDE) sequence. J Magn Reson Imaging2010; 31: 1256–1263.
11.
LiLMillerKLJezzardP. DANTE-prepared pulse trains: a novel approach to motion-sensitized and motion-suppressed quantitative magnetic resonance imaging. Magn Reson Med2012; 68: 1423–1438.
12.
WangJHelleMZhouZBörnertPHatsukamiTSYuanC. Joint blood and cerebrospinal fluid suppression for intracranial vessel wall MRI. Magn Reson Med2016; 75: 831–838.
13.
ViessmannOLiLBenjaminPJezzardP. T2-weighted intracranial vessel wall imaging at 7 Tesla using a DANTE-prepared variable flip angle turbo spin echo readout (DANTE-SPACE). Magn Reson Med2017; 77: 655–663.
14.
ZhangLZhangNWuJLiuXChungYC. High resolution simultaneous imaging of intracranial and extracranial arterial wall with improved cerebrospinal fluid suppression. Magn Reson Imaging2017; 44: 65–71.
15.
XieYYangQXieGPangJFanZLiD. Improved black-blood imaging using DANTE-SPACE for simultaneous carotid and intracranial vessel wall evaluation. Magn Reson Med2016; 75: 2286–2294.
16.
DielemanNYangWAbrigoJM, et al.Magnetic resonance imaging of plaque morphology, burden, and distribution in patients with symptomatic middle cerebral artery stenosis. Stroke2016; 47: 1797–1802.
DielemanNVan Der KolkAGZwanenburgJJM, et al.Imaging intracranial vessel wall pathology with magnetic resonance imaging current prospects and future directions. Circulation2014; 130: 192–201.
19.
GutierrezJHonigLElkindMSV, et al.Brain arterial aging and its relationship to Alzheimer dementia. Neurology2016; 86: 1507–1515.
20.
HarteveldAADenswilNPVan HeckeW, et al.Ex vivo vessel wall thickness measurements of the human Circle of Willis using 7T MRI. Atherosclerosis2018; 273: 106–114.
21.
HarteveldAAvan der KolkAGvan der WorpHB, et al.High-resolution intracranial vessel wall MRI in an elderly asymptomatic population: comparison of 3T and 7T. Eur Radiol2017; 27: 1585–1595.
22.
de HavenonAMossa-BashaMShahL, et al.High-resolution vessel wall MRI for the evaluation of intracranial atherosclerotic disease. Neuroradiology2017; 59: 1193–1202.
23.
SwartzRHBhutaSSFarbRI, et al.Intracranial arterial wall imaging using high-resolution 3-tesla contrast-enhanced MRI. Neurology2009; 72: 627–634.
24.
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.
25.
KimJMJungKHSohnCH, et al.Intracranial plaque enhancement from high resolution vessel wall magnetic resonance imaging predicts stroke recurrence. Int J Stroke2016; 11: 171–179.
26.
TuranTNRumboldtZGranholmAC, et al.Intracranial atherosclerosis: correlation between in-vivo 3T high resolution MRI and pathology. Atherosclerosis2014; 237: 460–463.
27.
YangWJChenXYZhaoHL, et al.Postmortem study of validation of low signal on fat-suppressed T1-weighted magnetic resonance imaging as marker of lipid core in middle cerebral artery atherosclerosis. Stroke2016; 47: 2299–2304.
YuJHKwakHSChungGHHwangSBParkMSParkSH. Association of intraplaque hemorrhage and acute infarction in patients with basilar artery plaque. Stroke2015; 46: 2768–2772.
30.
PowersWJDerdeynCPBillerJ, et al.2015 American Heart Association/American stroke association focused update of the 2013 guidelines for the early management of patients with acute ischemic stroke regarding endovascular treatment: a guideline for healthcare professionals from the American. Stroke2015; 46: 3020–3035.
31.
NakamuraKGuizardNFonovVSNarayananSCollinsDLArnoldDL. Jacobian integration method increases the statistical power to measure gray matter atrophy in multiple sclerosis. NeuroImage Clin2014; 4: 10–17.
32.
AbrahamPScott PannellJSantiago-DieppaDR, et al.Vessel wall signal enhancement on 3-T MRI in acute stroke patients after stent retriever thrombectomy. Neurosurg Focus2017; 42: E20.
33.
LiYTuranTNChaudryI, et al.High-resolution magnetic resonance imaging evidence for intracranial vessel wall inflammation following endovascular thrombectomy. J Stroke Cerebrovasc Dis2017; 26: e96–e98.
34.
RenúALaredoCLopez-RuedaA, et al.Vessel wall enhancement and blood-cerebrospinal fluid barrier disruption after mechanical thrombectomy in acute ischemic stroke. Stroke2017; 48: 651–657.
35.
SeoWKOhKSuhSISeolHY. Clinical significance of wall changes after recanalization therapy in acute stroke: high-resolution vessel wall imaging. Stroke2017; 48: 1077–1080.
36.
PowerSMatoukCCasaubonLK, et al.Vessel wall magnetic resonance imaging in acute ischemic stroke: effects of embolism and mechanical thrombectomy on the arterial wall. Stroke2014; 45: 2330–2334.
37.
OwenDRJLindsayACChoudhuryRPFayadZA. Imaging of atherosclerosis. Annu Rev Med2011; 62: 25–40.
38.
SangiorgiGRumbergerJASeversonA, et al.Arterial calcification and not lumen stenosis is highly correlated with atherosclerotic plaque burden in humans: a histologic study of 723 coronary artery segments using nondecalcifying methodology. J Am Coll Cardiol1998; 31: 126–133.
39.
FisherCMGoreIOkabeNWhitePD. Calcification of the carotid siphon. Circulation1965; 32: 538–548.
40.
WoodcockRJGoldsteinJHKallmesDFCloftHJPhillipsCD. Angiographic correlation of CT calcification in the carotid siphon. Am J Neuroradiol1999; 20: 495–499.
41.
BosDVan Der RijkMJMGeeraedtsTEA, et al.Intracranial carotid artery atherosclerosis: prevalence and risk factors in the general population. Stroke2012; 43: 1878–1884.
42.
ChenXYLamWWMHoKNFanYHWongKS. The frequency and determinants of calcification in intracranial arteries in Chinese patients who underwent computed tomography examinations. Cerebrovasc Dis2006; 21: 91–97.
43.
BosDPortegiesMLPVan Der LugtA, et al.Intracranial carotid artery atherosclerosis and the risk of stroke in whites: the Rotterdam study. JAMA Neurol2014; 71: 405–411.
44.
TaylorAJCerqueiraMHodgsonJM, et al.ACCF/SCCT/ACR/AHA/ASE/ASNC/NASCI/SCAI/SCMR 2010 appropriate use criteria for cardiac computed tomography. J Am Coll Cardiol2010; 56: 1864–1894.
45.
VosAVan HeckeWSplietWGM, et al.Predominance of nonatherosclerotic internal elastic lamina calcification in the intracranial internal carotid artery. Stroke2016; 47: 221–223.
46.
KockelkorenRVosAVan HeckeW, et al.Computed tomographic distinction of intimal and medial calcification in the intracranial internal carotid artery. PLoS One2017; 12: e0168360.
47.
CompagneKCJClephasPRDMajoieCBLM, et al.Intracranial carotid artery calcification and effect of endovascular stroke treatment: Mr CLEAN subgroup analysis. Stroke2018; 49: 2961–2968.
48.
Pavlin-PremrlDSharmaRCampbellBCV, et al.Advanced imaging of intracranial atherosclerosis: lessons from interventional cardiology. Front Neurol2017; 8: 387.
PatelIJBezerraHGCostaMAFujinoYHsuDP. Novel use of optical coherence tomography. J Neurointerv Surg2013; 5: 10–13.
51.
MajidiSSeinJWatanabeM, et al.Intracranial-derived atherosclerosis assessment: an in vitro comparison between virtual histology by intravascular ultrasonography, 7T MRI, and histopathologic findings. AJNR Am J Neuroradiol2013; 34: 2259–2264.
52.
MeyersPMSchumacherHCGrayWA, et al.Intravascular ultrasound of symptomatic intracranial stenosis demonstrates atherosclerotic plaque with intraplaque hemorrhage: a case report. J Neuroimaging2009; 19: 266–270.
53.
WangXPeterK. Molecular imaging of atherothrombotic diseases: seeing is believing. Arterioscler Thromb Vasc Biol2017; 37: 1029–1040.
54.
GounisMJVan Der MarelKMarosfoiM, et al.Imaging inflammation in cerebrovascular disease. Stroke2015; 46: 2991–2997.
55.
MandellDMMatoukCCFarbRI, et al.Vessel wall MRI to differentiate between reversible cerebral vasoconstriction syndrome and central nervous system vasculitis: preliminary results. Stroke2012; 43: 860–862.
56.
BackesDHendrikseJvan der SchaafI, et al.Determinants of gadolinium-enhancement of the aneurysm wall in unruptured intracranial aneurysms. Neurosurgery2018; 83: 719–725.
57.
EdjlaliMGentricJCRégent-RodriguezC, et al.Does aneurysmal wall enhancement on vessel wall MRI Help to distinguish stable from unstable intracranial aneurysms?Stroke2014; 45: 3704–3706.
58.
QiaoYAnwarZIntrapiromkulJ, et al.Patterns and implications of intracranial arterial remodeling in stroke patients. Stroke2016; 47: 434–440.
59.
LeeWJChoiHSJangJ, et al.Non-stenotic intracranial arteries have atherosclerotic changes in acute ischemic stroke patients: a 3T MRI study. Neuroradiology2015; 57: 1007–1013.
60.
KimTHChoiJWRohHG, et al.Atherosclerotic arterial wall change of non-stenotic intracracranial arteries on high-resolution MRI at 3.0 T: correlation with cerebrovascular risk factors and white matter hyperintensity. Clin Neurol Neurosurg2014; 126: 1–6.
