DOI QR코드

DOI QR Code

Targeting the culprit: vessel wall magnetic resonance imaging for evaluating stroke

  • Kim, Seung Min (Department of Neurology, Veterans Health Service Medical Center) ;
  • Ha, Sang Hee (Department of Neurology, Asan Medical Center) ;
  • Kwon, Hanim (Department of Neurology, Asan Medical Center) ;
  • Kim, Yeon Jung (Department of Neurology, Asan Medical Center) ;
  • Ahn, Sung Ho (Department of Neurology, Pusan National University Yangsan Hospital) ;
  • Kim, Bum Joon (Department of Neurology, Asan Medical Center)
  • Received : 2021.02.02
  • Accepted : 2021.02.24
  • Published : 2021.04.30

Abstract

The pathogenesis of many strokes originates in the vessel wall. Despite this, most traditional imaging focuses on the vascular lumen. Vessel-wall magnetic resonance imaging (VWMRI) is useful for establishing the etiology of intracranial stenosis. It also provides information regarding atherosclerotic plaque composition and thus plaque vulnerability, which is an indication of its potential to cause a stroke. In this review we focus on the characteristics of VWMRI findings in various arteriopathies related to intracranial artery stenosis, and discuss the clinical implications of these findings.

Keywords

Acknowledgement

This research was supported by the Brain Convergence Research Program of the National Research Foundation (NRF) funded by the Korean government (MSIT; No. 2020M3E5D2A01084576).

References

  1. Kim BJ, Kim JS. Ischemic stroke subtype classification: an asian viewpoint. J Stroke 2014;16:8-17. https://doi.org/10.5853/jos.2014.16.1.8
  2. Kim BJ, Kang HG, Kim HJ, Ahn SH, Kim NY, Warach S, et al. Magnetic resonance imaging in acute ischemic stroke treatment. J Stroke 2014;16:131-145. https://doi.org/10.5853/jos.2014.16.3.131
  3. Kim SM, Kim YJ, Kim K, Kim BJ. Usefulness of carotid ultrasonography and treatment of carotid disease. J Korean Med Assoc 2020;63:342-353. https://doi.org/10.5124/jkma.2020.63.6.342
  4. Kim JS, Nah HW, Park SM, Kim SK, Cho KH, Lee J, et al. Risk factors and stroke mechanisms in atherosclerotic stroke: intracranial compared with extracranial and anterior compared with posterior circulation disease. Stroke 2012;43:3313-3318. https://doi.org/10.1161/STROKEAHA.112.658500
  5. Kim JS, Bonovich D. Research on intracranial atherosclerosis from the East and west: why are the results different? J Stroke 2014;16:105-113. https://doi.org/10.5853/jos.2014.16.3.105
  6. Kim BJ, Lee KM, Lee SH, Kim HG, Kim EJ, Heo SH, et al. Ethnic differences in intracranial artery tortuosity: a possible reason for different locations of cerebral atherosclerosis. J Stroke 2018;20:140-141. https://doi.org/10.5853/jos.2017.02915
  7. Kim YS, Kim BJ, Noh KC, Lee KM, Heo SH, Choi HY, et al. Distal versus proximal middle cerebral artery occlusion: different mechanisms. Cerebrovasc Dis 2019;47:238-244. https://doi.org/10.1159/000500947
  8. Ha SH, Chang JY, Lee SH, Lee KM, Heo SH, Chang DI, et al. Mechanism of stroke according to the severity and location of atherosclerotic middle cerebral artery disease. J Stroke Cerebrovasc Dis 2021;30:105503. https://doi.org/10.1016/j.jstrokecerebrovasdis.2020.105503
  9. Mandell DM, Mossa-Basha M, Qiao Y, Hess CP, Hui F, Matouk C, et al. Intracranial vessel wall MRI: Principles and Expert Consensus Recommendations of the American Society of Neuroradiology. AJNR Am J Neuroradiol 2017;38:218-229. https://doi.org/10.3174/ajnr.A4893
  10. Kim BJ, Yoon Y, Lee DH, Kang DW, Kwon SU, Kim JS. The shape of middle cerebral artery and plaque location: high-resolution MRI finding. Int J Stroke 2015;10:856-860. https://doi.org/10.1111/ijs.12497
  11. Fuster V, Moreno PR, Fayad ZA, Corti R, Badimon JJ. Atherothrombosis and high-risk plaque: part I: evolving concepts. J Am Coll Cardiol 2005;46:937-954. https://doi.org/10.1016/j.jacc.2005.03.074
  12. Dieleman N, Yang W, Abrigo JM, Chu WC, van der Kolk AG, Siero JC, et al. Magnetic resonance imaging of plaque morphology, burden, and distribution in patients with symptomatic middle cerebral artery stenosis. Stroke 2016;47:1797-1802. https://doi.org/10.1161/STROKEAHA.116.013007
  13. Xu WH, Li ML, Gao S, Ni J, Zhou LX, Yao M, et al. In vivo high-resolution MR imaging of symptomatic and asymptomatic middle cerebral artery atherosclerotic stenosis. Atherosclerosis 2010;212:507-511. https://doi.org/10.1016/j.atherosclerosis.2010.06.035
  14. Kim JM, Jung KH, Sohn CH, Moon J, Shin JH, Park J, et al. Intracranial plaque enhancement from high resolution vessel wall magnetic resonance imaging predicts stroke recurrence. Int J Stroke 2016;11:171-179. https://doi.org/10.1177/1747493015609775
  15. Vakil P, Vranic J, Hurley MC, Bernstein RA, Korutz AW, Habib A, et al. T1 gadolinium enhancement of intracranial atherosclerotic plaques associated with symptomatic ischemic presentations. AJNR Am J Neuroradiol 2013;34:2252-2258. https://doi.org/10.3174/ajnr.A3606
  16. 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. https://doi.org/10.1159/000111525
  17. Portanova A, Hakakian N, Mikulis DJ, Virmani R, Abdalla WM, Wasserman BA. Intracranial vasa vasorum: insights and implications for imaging. Radiology 2013;267:667-679. https://doi.org/10.1148/radiol.13112310
  18. Parma L, Baganha F, Quax PHA, de Vries MR. Plaque angiogenesis and intraplaque hemorrhage in atherosclerosis. Eur J Pharmacol 2017;816:107-115. https://doi.org/10.1016/j.ejphar.2017.04.028
  19. Chu B, Kampschulte A, Ferguson MS, Kerwin WS, Yarnykh VL, O'Brien KD, et al. Hemorrhage in the atherosclerotic carotid plaque: a high-resolution MRI study. Stroke 2004;35:1079-1084. https://doi.org/10.1161/01.STR.0000125856.25309.86
  20. Kim BJ, Kim HY, Jho W, Kim YS, Koh SH, Heo SH, et al. Asymptomatic basilar artery plaque distribution and vascular geometry. J Atheroscler Thromb 2019;26:1007-1014. https://doi.org/10.5551/jat.47365
  21. Yang WJ, Fisher M, Zheng L, Niu CB, Paganini-Hill A, Zhao HL, et al. Histological characteristics of intracranial atherosclerosis in a Chinese population: a postmortem study. Front Neurol 2017;8:488. https://doi.org/10.3389/fneur.2017.00488
  22. Yang WJ, Chen XY, Zhao HL, Niu CB, Xu Y, Wong KS, et al. In vitro assessment of histology verified intracranial atherosclerotic disease by 1.5T magnetic resonance imaging: concentric or eccentric? Stroke 2016;47:527-530. https://doi.org/10.1161/STROKEAHA.115.011086
  23. 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. https://doi.org/10.1016/j.ejrad.2012.07.001
  24. Qiao Y, Anwar Z, Intrapiromkul J, Liu L, Zeiler SR, Leigh R, et al. Patterns and implications of intracranial arterial remodeling in stroke patients. Stroke 2016;47:434-440. https://doi.org/10.1161/STROKEAHA.115.009955
  25. Pasterkamp G, Schoneveld AH, van der Wal AC, Hijnen DJ, van Wolveren WJ, Plomp S, et al. Inflammation of the atherosclerotic cap and shoulder of the plaque is a common and locally observed feature in unruptured plaques of femoral and coronary arteries. Arterioscler Thromb Vasc Biol 1999;19:54-58. https://doi.org/10.1161/01.ATV.19.1.54
  26. Shi MC, Wang SC, Zhou HW, Xing YQ, Cheng YH, Feng JC, et al. Compensatory remodeling in symptomatic middle cerebral artery atherosclerotic stenosis: a high-resolution MRI and microemboli monitoring study. Neurol Res 2012;34:153-158. https://doi.org/10.1179/1743132811Y.0000000065
  27. Watanabe Y, Nagayama M. MR plaque imaging of the carotid artery. Neuroradiology 2010;52:253-274. https://doi.org/10.1007/s00234-010-0663-z
  28. Suzuki J, Takaku A. Cerebrovascular "moyamoya" disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 1969;20:288-299. https://doi.org/10.1001/archneur.1969.00480090076012
  29. Bang OY, Ryoo S, Kim SJ, Yoon CH, Cha J, Yeon JY, et al. Adult moyamoya disease: a burden of intracranial stenosis in East Asians? PLoS One 2015;10:e0130663. https://doi.org/10.1371/journal.pone.0130663
  30. Kim JS. Moyamoya disease: epidemiology, clinical features, and diagnosis. J Stroke 2016;18:2-11. https://doi.org/10.5853/jos.2015.01627
  31. Kaku Y, Morioka M, Ohmori Y, Kawano T, Kai Y, Fukuoka H, 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. https://doi.org/10.1007/s00701-012-1472-4
  32. Takagi Y, Kikuta K, Nozaki K, Hashimoto N. Histological features of middle cerebral arteries from patients treated for Moyamoya disease. Neurol Med Chir (Tokyo) 2007;47:1-4. https://doi.org/10.2176/nmc.47.1
  33. Kim YJ, Lee DH, Kwon JY, Kang DW, Suh DC, Kim JS, et al. High resolution MRI difference between moyamoya disease and intracranial atherosclerosis. Eur J Neurol 2013;20:1311-1318. https://doi.org/10.1111/ene.12202
  34. Burke GM, Burke AM, Sherma AK, Hurley MC, Batjer HH, Bendok BR. Moyamoya disease: a summary. Neurosurg Focus 2009;26:E11.
  35. Choi YJ, Jung SC, Lee DH. Vessel wall imaging of the intracranial and cervical carotid arteries. J Stroke 2015;17:238-255. https://doi.org/10.5853/jos.2015.17.3.238
  36. Debette S, Compter A, Labeyrie MA, Uyttenboogaart M, Metso TM, Majersik JJ, et al. Epidemiology, pathophysiology, diagnosis, and management of intracranial artery dissection. Lancet Neurol 2015;14:640-654. https://doi.org/10.1016/S1474-4422(15)00009-5
  37. Kwon JY, Kim NY, Suh DC, Kang DW, Kwon SU, Kim JS. Intracranial and extracranial arterial dissection presenting with ischemic stroke: lesion location and stroke mechanism. J Neurol Sci 2015;358:371-376. https://doi.org/10.1016/j.jns.2015.09.368
  38. Maruyama H, Nagoya H, Kato Y, Deguchi I, Fukuoka T, Ohe Y, et al. Spontaneous cervicocephalic arterial dissection with headache and neck pain as the only symptom. J Headache Pain 2012;13:247-253. https://doi.org/10.1007/s10194-012-0420-2
  39. Lee SH, Kim KY, Jung JM. High-resolution magnetic resonance imaging for the follow-up of intracranial arterial dissections. Acta Neurol Belg 2020 Jul 10. [Epub]. DOI:10.1007/s13760-020-01432-0. Online ahead of print.
  40. Lee SH, Jung JM, Kim KY, Kim BJ. Intramural hematoma shape and acute cerebral infarction in intracranial artery dissection: a high-resolution magnetic resonance imaging study. Cerebrovasc Dis 2020;49:269-276. https://doi.org/10.1159/000508027
  41. Patel RR, Adam R, Maldjian C, Lincoln CM, Yuen A, Arneja A. Cervical carotid artery dissection: current review of diagnosis and treatment. Cardiol Rev 2012;20:145-152. https://doi.org/10.1097/CRD.0b013e318247cd15
  42. Wu Y, Wu F, Liu Y, Fan Z, Fisher M, Li D, et al. High-resolution magnetic resonance imaging of cervicocranial artery dissection: imaging features associated with stroke. Stroke 2019;50:3101-3107. https://doi.org/10.1161/STROKEAHA.119.026362
  43. Wang Y, Lou X, Li Y, Sui B, Sun S, Li C, et al. Imaging investigation of intracranial arterial dissecting aneurysms by using 3 T high-resolution MRI and DSA: from the interventional neuroradiologists' view. Acta Neurochir (Wien) 2014;156:515-525. https://doi.org/10.1007/s00701-013-1989-1
  44. Redekop GJ. Extracranial carotid and vertebral artery dissection: a review. Can J Neurol Sci 2008;35:146-152. https://doi.org/10.1017/S0317167100008556
  45. Calabrese LH, Dodick DW, Schwedt TJ, Singhal AB. Narrative review: reversible cerebral vasoconstriction syndromes. Ann Intern Med 2007;146:34-44. https://doi.org/10.7326/0003-4819-146-1-200701020-00007
  46. Miller TR, Shivashankar R, Mossa-Basha M, Gandhi D. Reversible cerebral vasoconstriction syndrome, part 1: epidemiology, pathogenesis, and clinical course. AJNR Am J Neuroradiol 2015;36:1392-1399. https://doi.org/10.3174/ajnr.A4214
  47. Miller TR, Shivashankar R, Mossa-Basha M, Gandhi D. Reversible cerebral vasoconstriction syndrome, part 2: diagnostic work-up, imaging evaluation, and differential diagnosis. AJNR Am J Neuroradiol 2015;36:1580-1588. https://doi.org/10.3174/ajnr.A4215
  48. Swartz RH, Bhuta SS, Farb RI, Agid R, Willinsky RA, Terbrugge KG, et al. Intracranial arterial wall imaging using high-resolution 3-tesla contrast-enhanced MRI. Neurology 2009;72:627-634. https://doi.org/10.1212/01.wnl.0000342470.69739.b3
  49. Hajj-Ali RA, Calabrese LH. Diagnosis and classification of central nervous system vasculitis. J Autoimmun 2014;48-49:149-152. https://doi.org/10.1016/j.jaut.2014.01.007
  50. Jung SC, Kang DW, Turan TN. Vessel and vessel wall imaging. Front Neurol Neurosci 2016;40:109-123. https://doi.org/10.1159/000448308
  51. Lindenholz A, van der Kolk AG, Zwanenburg JJM, Hendrikse J. The use and pitfalls of intracranial vessel wall imaging: how we do it. Radiology 2018;286:12-28. https://doi.org/10.1148/radiol.2017162096
  52. Power S, Matouk C, Casaubon LK, Silver FL, Krings T, Mikulis DJ, et al. Vessel wall magnetic resonance imaging in acute ischemic stroke: effects of embolism and mechanical thrombectomy on the arterial wall. Stroke 2014;45:2330-2334. https://doi.org/10.1161/STROKEAHA.114.005618