Imaging intracranial vessel wall pathology with magnetic resonance imaging current prospects and future directions

Circulation

Volumn 130, Issue 2, 2014, Pages 192-201

  Dieleman, Nikki ^a   Van Der Kolk, Anja G ^a   Zwanenburg, Jaco J M ^b   Harteveld, Anita A ^a   Biessels, Geert J ^a   Luijten, Peter R ^a   Hendrikse, Jeroen ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b Image Science Institute   (Netherlands)

Author keywords

Atherosclerotic; Infarction; Magnetic resonance imaging; Neuroimaging; Plaque; Stroke

Indexed keywords

BLOOD VESSEL INJURY; BLOOD VESSEL WALL; BRAIN ATHEROSCLEROSIS; BRAIN ISCHEMIA; CEREBROVASCULAR ACCIDENT; CLINICAL PRACTICE; CONTRAST ENHANCEMENT; HUMAN; INTRACRANIAL VESSEL WALL; MAGNETIC FIELD; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; REVIEW;

INFARCTION; MAGNETIC RESONANCE IMAGING; NEUROIMAGING; PLAQUE, ATHEROSCLEROTIC; STROKE;

ANIMALS; CEREBRAL ARTERIES; CEREBROVASCULAR CIRCULATION; CEREBROVASCULAR DISORDERS; FORECASTING; HUMANS; MAGNETIC RESONANCE IMAGING;

EID: 84903936681     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.113.006919     Document Type: Review

References (76)

1. Adams HP Jr, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, Marsh EE 3rd. 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. 1993; 24: 35-41. (Pubitemid 23014379)
2. Bash S, Villablanca JP, Jahan R, Duckwiler G, Tillis M, Kidwell C, Saver J, Sayre J. Intracranial vascular stenosis and occlusive disease: evaluation with CT angiography, MR angiography, and digital subtraction angiography. AJNR Am J Neuroradiol. 2005; 26: 1012-1021. (Pubitemid 43821943)
3. Kiechl S, Willeit J. The natural course of atherosclerosis, part II: vascular remodeling. Arterioscler Thromb Vasc Biol. 1999; 19: 1491-1498. (Pubitemid 29263019)
4. Glagov S, Weisenberg E, Zarins CK, Stankunavicius R, Kolettis GJ. Compensatory enlargement of human atherosclerotic coronary arteries. N Engl J Med. 1987; 316: 1371-1375. (Pubitemid 17079680)
5. Mandell DM, Shroff M. On MR imaging of the intracranial vessel wall. Can J Neurol Sci. 2011; 38: 4-5.
6. Mühlenbruch G, Das M, Mommertz G, Schaaf M, Langer S, Mahnken AH, Wildberger JE, Thron A, Günther RW, Krings T. Comparison of dualsource CT angiography and MR angiography in preoperative evaluation of intra- and extracranial vessels: a pilot study. Eur Radiol. 2010; 20: 469-476.
7. Arenillas JF. Intracranial atherosclerosis: current concepts. Stroke. 2011; 42(suppl): S20-S23.
8. Qureshi AI, Caplan LR. Intracranial atherosclerosis. Lancet. 2013; 6736: 1-15.
9. van der Kolk AG, Zwanenburg JJ, Brundel M, Biessels GJ, Visser F, Luijten PR, Hendrikse J. Intracranial vessel wall imaging at 7.0-T MRI. Stroke. 2011; 42: 2478-2484.
10. Lou X, Ma N, Ma L, Jiang WJ. Contrast-enhanced 3T high-resolution MR imaging in symptomatic atherosclerotic basilar artery stenosis. AJNR Am J Neuroradiol. 2013; 34: 513-517.
11. Ma N, Jiang WJ, Lou X, Ma L, Du B, Cai JF, Zhao TQ. Arterial remodeling of advanced basilar atherosclerosis: a 3-Tesla MRI study. Neurology. 2010; 75: 253-258.
12. Ma N, Lou X, Zhao TQ, Wong EH, Jiang WJ. Intraobserver and interobserver variability for measuring the wall area of the basilar artery at the level of the trigeminal ganglion on high-resolution MR images. AJNR Am J Neuroradiol. 2011; 32: E29-E32.
13. Park JK, Kim SH, Kim BS, Choi G, Jeong SY, Choi JC. Imaging of intracranial plaques with black-blood double inversion recovery MR imaging and CT. J Neuroimaging. 2011; 21: e64-e68.
14. Chung GH, Kwak HS, Hwang SB, Jin GY. High resolution MR imaging in patients with symptomatic middle cerebral artery stenosis. Eur J Radiol. 2012; 81: 4069-4074.
15. Kim JM, Jung KH, Sohn CH, Moon J, Han MH, Roh JK. Middle cerebral artery plaque and prediction of the infarction pattern. Arch Neurol. 2012; 69: 1470-1475.
16. Kim YS, Lim SH, Oh KW, Kim JY, Koh SH, Kim J, Heo SH, Chang DI, Lee YJ, Kim HY. The advantage of high-resolution MRI in evaluating basilar plaques: a comparison study with MRA. Atherosclerosis. 2012; 224: 411-416.
17. Mi Kim S, Ryu CW, Jahng GH, Jong Kim E, Suk Choi W. Two different morphologies of chronic unilateral middle cerebral artery occlusion: evaluation using high-resolution MRI [published online ahead of print January 16, 2013]. J Neuroimaging. doi: 10.1111/jon.12009. http://onlinelibrary. wiley.com/doi/10. 1111/jon.12009/abstract; jsessionid=3660FCB7B0B6D 764E13E30AC535D8BCA.f03t04. Accessed June 20, 2013.
18. Mandell DM, Matouk CC, Farb RI, Krings T, Agid R, terBrugge K, Willinsky RA, Swartz RH, Silver FL, Mikulis DJ. Vessel wall MRI to differentiate between reversible cerebral vasoconstriction syndrome and central nervous system vasculitis: preliminary results. Stroke. 2012; 43: 860-862.
19. Pfefferkorn T, Linn J, Habs M, Opherk C, Cyran C, Ottomeyer C, Straube A, Dichgans M, Nikolaou K, Saam T. Black blood MRI in suspected large artery primary angiitis of the central nervous system. J Neuroimaging. 2013; 23: 379-383.
20. Qiao Y, Steinman DA, Qin Q, Etesami M, Schär M, Astor BC, Wasserman BA. Intracranial arterial wall imaging using three-dimensional high isotropic resolution black blood MRI at 3.0 Tesla. J Magn Reson Imaging. 2011; 34: 22-30.
21. Ryu CW, Jahng GH, Kim EJ, Choi WS, Yang DM. High resolution wall and lumen MRI of the middle cerebral arteries at 3 Tesla. Cerebrovasc Dis. 2009; 27: 433-442.
22. Saam T, Habs M, Pollatos O, Cyran C, Pfefferkorn T, Dichgans M, Dietrich O, Glaser C, Reiser MF, Nikolaou K, Nikolauo K. High-resolution blackblood contrast-enhanced T1 weighted images for the diagnosis and follow- up of intracranial arteritis. Br J Radiol. 2010; 83: e182-e184.
23. Edelman RR, Chien D, Kim D. Fast selective black blood MR imaging. Radiology. 1991; 181: 655-660.
24. Koktzoglou I, Kirpalani A, Carroll TJ, Li D, Carr JC. Dark-blood MRI of the thoracic aorta with 3D diffusion-prepared steady-state free precession: initial clinical evaluation. AJR Am J Roentgenol. 2007; 189: 966-972. (Pubitemid 47479783)
25. Wang J, Yarnykh VL, Hatsukami T, Chu B, Balu N, Yuan C. Improved suppression of plaque-mimicking artifacts in black-blood carotid atherosclerosis imaging using a multislice motion-sensitized driven-equilibrium (MSDE) turbo spin-echo (TSE) sequence. Magn Reson Med. 2007; 58: 973-981. (Pubitemid 350074365)
26. Botnar RM, Stuber M, Kissinger KV, Kim WY, Spuentrup E, Manning WJ. Noninvasive coronary vessel wall and plaque imaging with magnetic resonance imaging. Circulation. 2000; 102: 2582-2587.
27. Aoki S, Shirouzu I, Sasaki Y, Okubo T, Hayashi N, Machida T, Hoshi E, Suzuki K, Funada N, Araki T. Enhancement of the intracranial arterial wall at MR imaging: relationship to cerebral atherosclerosis. Radiology. 1995; 194: 477-481.
28. Aoki S, Hayashi N, Abe O, Shirouzu I, Ishigame K, Okubo T, Nakagawa K, Ohtomo K, Araki T. Radiation-induced arteritis: thickened wall with prominent enhancement on cranial MR images report of five cases and comparison with 18 cases of Moyamoya disease. Radiology. 2002; 223: 683-688. (Pubitemid 34547583)
29. Klein IF, Lavallée PC, Mazighi M, Schouman-Claeys E, Labreuche J, Amarenco P. Basilar artery atherosclerotic plaques in paramedian and lacunar pontine infarctions: a high-resolution MRI study. Stroke. 2010; 41: 1405-1409.
30. Küker W, Gaertner S, Nagele T, Dopfer C, Schoning M, Fiehler J, Rothwell PM, Herrlinger U. Vessel wall contrast enhancement: a diagnostic sign of cerebral vasculitis. Cerebrovasc Dis. 2008; 26: 23-29. (Pubitemid 351931417)
31. Natori T, Sasaki M, Miyoshi M, Ohba H, Katsura N, Yamaguchi M, Narumi S, Kabasawa H, Kudo K, Ito K, Terayama Y. Evaluating middle cerebral artery atherosclerotic lesions in acute ischemic stroke using magnetic resonance T1-weighted 3-dimensional vessel wall imaging. J Stroke Cerebrovasc Dis. 2014; 23: 706-711.
32. Vakil P, Vranic J, Hurley MC, Bernstein RA, Korutz AW, Habib A, Shaibani A, Dehkordi FH, Carroll TJ, Ansari SA. T1 gadolinium enhancement of intracranial atherosclerotic plaques associated with symptomatic ischemic presentations. AJNR Am J Neuroradiol. 2013; 34: 2252-2258.
33. Klein IF, Lavallée PC, Touboul PJ, Schouman-Claeys E, Amarenco P. In vivo middle cerebral artery plaque imaging by high-resolution MRI. Neurology. 2006; 67: 327-329. (Pubitemid 44305427)
34. Klein IF, Lavallée PC, Schouman-Claeys E, Amarenco P. High-resolution MRI identifies basilar artery plaques in paramedian pontine infarct. Neurology. 2005; 64: 551-552. (Pubitemid 40189882)
35. Lam WW, Wong KS, So NM, Yeung TK, Gao S. Plaque volume measurement by magnetic resonance imaging as an index of remodeling of middle cerebral artery: correlation with transcranial color Doppler and magnetic resonance angiography. Cerebrovasc Dis. 2004; 17: 166-169. (Pubitemid 38529193)
36. Chen XY, Lam WW, Ng HK, Zhao HL, Wong KS. Diagnostic accuracy of MRI for middle cerebral artery stenosis: a postmortem study. J Neuroimaging. 2006; 16: 318-322. (Pubitemid 44521381)
37. Sparing R, Harrer JU, Spuentrup E, Krings T. MR-imaging of thrombus in extra- and intracranial arteries employing balanced fast-field echo MRI. Neuroradiology. 2004; 46: 973-977. (Pubitemid 40823321)
38. Chung JW, Kim BJ, Choi BS, Sohn CH, Bae HJ, Yoon BW, Lee SH. High-resolution magnetic resonance imaging reveals hidden etiologies of symptomatic vertebral arterial lesions. J Stroke Cerebrovasc Dis. 2014; 23: 293-302.
39. Matouk CC, Mandell DM, Günel M, Bulsara KR, Malhotra A, Hebert R, Johnson MH, Mikulis DJ, Minja FJ. Vessel wall magnetic resonance imaging identifies the site of rupture in patients with multiple intracranial aneurysms: proof of principle. Neurosurgery. 2013; 72: 492-496.
40. Shi M, Wang S, Zhou H, Cheng Y, Feng J, Wu J. Wingspan stenting of symptomatic middle cerebral artery stenosis and perioperative evaluation using high-resolution 3 Tesla MRI. J Clin Neurosci. 2012; 19: 912-914.
41. Skarpathiotakis M, Mandell DM, Swartz RH, Tomlinson G, Mikulis DJ. Intracranial atherosclerotic plaque enhancement in patients with ischemic stroke. AJNR Am J Neuroradiol. 2013; 34: 299-304.
42. Swartz RH, Bhuta SS, Farb RI, Agid R, Willinsky RA, Terbrugge KG, Butany J, Wasserman BA, Johnstone DM, Silver FL, Mikulis DJ. Intracranial arterial wall imaging using high-resolution 3-Tesla contrastenhanced MRI. Neurology. 2009; 72: 627-634.
43. Turan TN, Rumboldt Z, Brown TR. High-resolution MRI of basilar atherosclerosis: three-dimensional acquisition and FLAIR sequences. Brain Behav. 2013; 3: 1-3.
44. Xu WH, Li ML, Gao S, Ni J, Zhou LX, Yao M, Peng B, Feng F, Jin ZY, Cui LY. In vivo high-resolution MR imaging of symptomatic and asymptomatic middle cerebral artery atherosclerotic stenosis. Atherosclerosis. 2010; 212: 507-511.
45. Xu WH, Li ML, Gao S, Ni J, Zhou LX, Yao M, Peng B, Feng F, Jin ZY, Cui LY. Plaque distribution of stenotic middle cerebral artery and its clinical relevance. Stroke. 2011; 42: 2957-2959.
46. Vergouwen MD, Silver FL, Mandell DM, Mikulis DJ, Krings T, Swartz RH. Fibrous cap enhancement in symptomatic atherosclerotic basilar artery stenosis. Arch Neurol. 2011; 68: 676.
47. Vergouwen MD, Silver FL, Mandell DM, Mikulis DJ, Swartz RH. Eccentric narrowing and enhancement of symptomatic middle cerebral artery stenoses in patients with recent ischemic stroke. Arch Neurol. 2011; 68: 338-342.
48. Li ML, Xu WH, Song L, Feng F, You H, Ni J, Gao S, Cui LY, Jin ZY. Atherosclerosis of middle cerebral artery: evaluation with high-resolution MR imaging at 3T. Atherosclerosis. 2009; 204: 447-452.
49. Niizuma K, Shimizu H, Takada S, Tominaga T. Middle cerebral artery plaque imaging using 3-Tesla high-resolution MRI. J Clin Neurosci. 2008; 15: 1137-1141.
50. Zhu XJ, Du B, Lou X, Hui FK, Ma L, Zheng BW, Jin M, Wang CX, Jiang WJ. Morphologic characteristics of atherosclerotic middle cerebral arteries on 3T high-resolution MRI. AJNR Am J Neuroradiol. 2013; 34: 1717-1722.
51. Turan TN, Bonilha L, Morgan PS, Adams RJ, Chimowitz MI. Intraplaque hemorrhage in symptomatic intracranial atherosclerotic disease. J Neuroimaging. 2011; 21: e159-e161.
52. van der Kolk AG, Hendrikse J, Zwanenburg JJ, Visser F, Luijten PR. Clinical applications of 7 T MRI in the brain. Eur J Radiol. 2013; 82: 708-718.
53. Majidi S, Sein J, Watanabe M, Hassan AE, Van de Moortele PF, Suri MF, Clark HB, Qureshi AI. Intracranial-derived atherosclerosis assessment: an in vitro comparison between virtual histology by intravascular ultrasonography, 7T MRI, and histopathologic findings. AJNR Am J Neuroradiol. 2013; 34: 2259-2264.
54. Marinkovié S, Gibo H, Milisavljevié M. The surgical anatomy of the relationships between the perforating and the leptomeningeal arteries. Neurosurgery. 1996; 39: 72-83.
55. Kamath S. Observations on the length and diameter of vessels forming the circle of Willis. J Anat. 1981; 133(pt 3): 419-423. (Pubitemid 11022819)
56. Haacke M. Magnetic Resonance Imaging: Physical Principles and Sequence Design. New York, NY: Wiley-Liss; 1999.
57. Chen XY, Wong KS, Lam WW, Zhao HL, Ng HK. Middle cerebral artery atherosclerosis: histological comparison between plaques associated with and not associated with infarct in a postmortem study. Cerebrovasc Dis. 2008; 25: 74-80. (Pubitemid 351280378)
58. Duivenvoorden R, de Groot E, Elsen BM, Laméris JS, van der Geest RJ, Stroes ES, Kastelein JJ, Nederveen AJ. In vivo quantification of carotid artery wall dimensions: 3.0-Tesla MRI versus B-mode ultrasound imaging. Circ Cardiovasc Imaging. 2009; 2: 235-242.
59. Touboul PJ, Elbaz A, Koller C, Lucas C, Adraï V, Chédru F, Amarenco P. Common carotid artery intima-media thickness and brain infarction: the Etude du Profil Génétique de l'Infarctus Céré bral (GENIC) case-control study: the GENIC Investigators. Circulation. 2000; 102: 313-318. (Pubitemid 30457582)
60. Ravensbergen J, Ravensbergen JW, Krijger JK, Hillen B, Hoogstraten HW. Localizing role of hemodynamics in atherosclerosis in several human vertebrobasilar junction geometries. Arterioscler Thromb Vasc Biol. 1998; 18: 708-716. (Pubitemid 28267649)
61. Honye J, Mahon DJ, Jain A, White CJ, Ramee SR, Wallis JB, al-Zarka A, Tobis JM. Morphological effects of coronary balloon angioplasty in vivo assessed by intravascular ultrasound imaging. Circulation. 1992; 85: 1012-1025.
62. Sluimer JC, Kolodgie FD, Bijnens AP, Maxfield K, Pacheco E, Kutys B, Duimel H, Frederik PM, van Hinsbergh VW, Virmani R, Daemen MJ. Thin-walled microvessels in human coronary atherosclerotic plaques show incomplete endothelial junctions relevance of compromised structural integrity for intraplaque microvascular leakage. J Am Coll Cardiol. 2009; 53: 1517-1527.
63. Qiao Y, Etesami M, Astor BC, Zeiler SR, Trout HH 3rd, Wasserman BA. Carotid plaque neovascularization and hemorrhage detected by MR imaging are associated with recent cerebrovascular ischemic events. AJNR Am J Neuroradiol. 2012; 33: 755-760.
64. Saam T, Hatsukami TS, Takaya N, Chu B, Underhill H, Kerwin WS, Cai J, Ferguson MS, Yuan C. The vulnerable, or high-risk, atherosclerotic plaque: noninvasive MR imaging for characterization and assessment. Radiology. 2007; 244: 64-77. (Pubitemid 46981959)
65. Virmani R, Kolodgie FD, Burke AP, Finn AV, Gold HK, Tulenko TN, Wrenn SP, Narula J. Atherosclerotic plaque progression and vulnerability to rupture: angiogenesis as a source of intraplaque hemorrhage. Arterioscler Thromb Vasc Biol. 2005; 25: 2054-2061. (Pubitemid 41416300)
66. Edwards JH, Kricheff II, Riles T, Imparato A. Angiographically undetected ulceration of the carotid bifurcation as a cause of embolic stroke. Radiology. 1979; 132: 369-373. (Pubitemid 9215692)
67. Yuan C, Mitsumori LM, Beach KW, Maravilla KR. Carotid atherosclerotic plaque: noninvasive MR characterization and identification of vulnerable lesions. Radiology. 2001; 221: 285-299. (Pubitemid 33043408)
68. van der Kolk AG, Hendrikse J, Brundel M, Biessels GJ, Smit EJ, Visser F, Luijten PR, Zwanenburg JJ. Multi-sequence whole-brain intracranial vessel wall imaging at 7.0 Tesla. Eur Radiol. 2013; 23: 2996-3004.
69. Wardlaw JM, Dennis MS, Warlow CP, Sandercock PA. Imaging appearance of the symptomatic perforating artery in patients with lacunar infarction: occlusion or other vascular pathology? Ann Neurol. 2001; 50: 208-215. (Pubitemid 32738146)
70. Biessels GJ, Zwanenburg JJ, Visser F, Frijns CJ, Luijten PR. Hypertensive cerebral hemorrhage: imaging the leak with 7-T MRI. Neurology. 2010; 75: 572-573.
71. Furie KL, Kasner SE, Adams RJ, Albers GW, Bush RL, Fagan SC, Halperin JL, Johnston SC, Katzan I, Kernan WN, Mitchell PH, Ovbiagele B, Palesch YY, Sacco RL, Schwamm LH, Wassertheil-Smoller S, Turan TN, Wentworth D; American Heart Association Stroke Council, Council on Cardiovascular Nursing, Council on Clinical Cardiology, Interdisciplinary Council on Quality of Care and Outcomes Research. Guidelines for the prevention of stroke in patients with stroke or transient ischemic attack: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2011; 42: 227-276.
72. Hajj-Ali RA, Singhal AB, Benseler S, Molloy E, Calabrese LH. Primary angiitis of the CNS. Lancet Neurol. 2011; 10: 561-572.
73. Derdeyn CP, Chimowitz MI, Lynn MJ, Fiorella D, Turan TN, Janis LS, Montgomery J, Nizam A, Lane BF, Lutsep HL, Barnwell SL, Waters MF, Hoh BL, Hourihane JM, Levy EI, Alexandrov AV, Harrigan MR, Chiu D, Klucznik RP, Clark JM, McDougall CG, Johnson MD, Pride GL, Lynch JR, Zaidat OO, Rumboldt Z, Cloft HJ. Aggressive medical treatment with or without stenting in high-risk patients with intracranial artery stenosis (SAMMPRIS): the final results of a randomised trial. Lancet. 2013; 6736: 1-9.
74. Chimowitz MI, Lynn MJ, Howlett-Smith H, Stern BJ, Hertzberg VS, Frankel MR, Levine SR, Chaturvedi S, Kasner SE, Benesch CG, Sila CA, Jovin TG, Romano JG; Warfarin-Aspirin Symptomatic Intracranial Disease Trial Investigators. Comparison of warfarin and aspirin for symptomatic intracranial arterial stenosis. N Engl J Med. 2005; 352: 1305-1316.
75. Yuan C, Hatsukami TS, Obrien KD. High-resolution magnetic resonance imaging of normal and atherosclerotic human coronary arteries ex vivo: discrimination of plaque tissue components. J Investig Med. 2001; 49: 491-499. (Pubitemid 33104582)
76. den Hartog AG, Bovens SM, Koning W, Hendrikse J, Luijten PR, Moll FL, Pasterkamp G, de Borst GJ. Current status of clinical magnetic resonance imaging for plaque characterisation in patients with carotid artery stenosis. Eur J Vasc Endovasc Surg. 2013; 45: 7-21.