J Clin Neurol.  2016 Apr;12(2):129-136. 10.3988/jcn.2016.12.2.129.

Considerations When Subtyping Ischemic Stroke in Asian Patients

Affiliations
  • 1Department of Neurology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea. ohyoung.bang@samsung.com

Abstract

Both the incidence and prevalence of stroke in Asia are steadily increasing, and the burden of stroke is particularly high in Asian countries. Although strokes in Asians and Caucasians share many common features, there are some differences that are probably due to differences in lifestyle and genetic background. While there have been advances in the stroke classification system, the assignment of Asian stroke patients to etiological categories has received little attention. The current classification system may not be well suited to Asian patients with ischemic stroke because the proportions and relative importance of stroke subtypes may differ with race and ethnicity. This review addresses concerns about the use of the current stroke classification system in Asian patients with ischemic stroke, and proposes a classification system that is more specific to the Asian population, in conjunction with discussing advances in diagnostic techniques.

Keyword

stroke; ischemic stroke; subtype; Asian; classification

MeSH Terms

Asia
Asian Continental Ancestry Group*
Classification
Continental Population Groups
Humans
Incidence
Life Style
Prevalence
Stroke*

Figure

  • Fig. 1 Stroke subtypes by racial and ethnic groups. *Data from southern Californians (Modified from Bang et al.8), †Data from South Koreans. AF: atrial fibrillation.

  • Fig. 2 Recurrent infarcts with progression of intracranial stenosis. A 32-year-old female experienced recurrent left middle cerebral artery (MCA) infarcts (three times) within 2 years. Serial time-of-flight magnetic resonance angiography (MRA) showed the progression of stenosis in the left MCA. Transfemoral cerebral angiography (TFCA) showed no stenosis in the distal internal carotid artery or basal collaterals suggestive of moyamoya disease (MMD) (arrow). However, high-resolution (HR) MRI revealed a smaller outer diameter, concentric enhancement, and the absence of focal plaques in the stenotic segment (circle). A genetic investigation revealed that the RNF213 mutation was associated with MMD (p.Arg4810Lys). CE: contrast enhanced.

  • Fig. 3 Subcortical infarction but no significant stenosis. A 48-year-old female experienced left hemiparesis. Diffusion-weighted imaging (DWI) shows a deep infarct in the right basal ganglia and corona radiata. MRA shows no significant stenosis in the relevant vessels. TFCA and high-resolution (HR) MRA show a small plaque in the superior half of the middle cerebral artery (arrow). CE: contrast enhanced, MRA: magnetic resonance angiography, PD: proton density, TFCA: transfemoral cerebral angiography, TOF: time of flight, 3D: three dimensional.

  • Fig. 4 A 59-year-old male presented with right hemiparesis. Diffusion-weighted imaging shows a small acute lacunar infarct in the left corona radiata. The magnetic resonance angiography findings were normal. Gradient-echo imaging shows multiple cerebral microbleeds in deep regions bilaterally. Two years later he was readmitted to the Department of Neurosurgery due to intracranial bleeding while taking dual antiplatelet agents.

  • Fig. 5 Typical cases of atrial fibrillation (AF)-related stroke (A), AF-unrelated stroke (B), and no-AF stroke (C). Left panel, DWI. Middle panel, MRA. Right panel, multidetector cardiac computed tomography. A: AF-related stroke with a larger left atrial appendage (LAA) orifice diameter (32.1 mm) and larger LAA volume (16.8 mL). This patient had an infarction and occlusion in the right MCA territory, but no stenosis or occlusion in other intra- and extracranial vessels was noted. B: AF-unrelated stroke with a smaller LAA diameter (23.1 mm) and smaller LAA volume (9.8 mL). This patient had a rightsided border zone infarction with severe right cervical carotid occlusion. C: No-AF stroke with a smaller LAA orifice diameter (22.9 mm) and smaller LAA volume (4.6 mL). This patient had left cortical small infarcts with left MCA stenosis. DWI: diffusion-weighted imaging, MCA: middle cerebral artery, MRA: magnetic resonance angiography.


Cited by  2 articles

Association between Stroke Status and Depression in a Community Setting: The 2014 Korea National Health and Nutrition Examination Survey
Mina Kim, Gyung-Jae Oh, Young-Hoon Lee
J Clin Neurol. 2017;13(1):55-61.    doi: 10.3988/jcn.2017.13.1.55.

Cerebral Arterial Stenosis in Patients with Spontaneous Intracerebral Hemorrhage
Pil-Wook Chung, Yu Sam Won
J Korean Neurosurg Soc. 2017;60(5):511-517.    doi: 10.3340/jkns.2016.1011.003.


Reference

1. Bamford J, Sandercock P, Dennis M, Burn J, Warlow C. Classification and natural history of clinically identifiable subtypes of cerebral infarction. Lancet. 1991; 337:1521–1526.
Article
2. Gross CR, Shinar D, Mohr JP, Hier DB, Caplan LR, Price TR, et al. Interobserver agreement in the diagnosis of stroke type. Arch Neurol. 1986; 43:893–898.
Article
3. Bogousslavsky J, Van Melle G, Regli F. The Lausanne Stroke Registry: analysis of 1,000 consecutive patients with first stroke. Stroke. 1988; 19:1083–1092.
Article
4. Adams HP Jr, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, et al. 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.
Article
5. Ay H, Furie KL, Singhal A, Smith WS, Sorensen AG, Koroshetz WJ. An evidence-based causative classification system for acute ischemic stroke. Ann Neurol. 2005; 58:688–697.
Article
6. Amarenco P, Bogousslavsky J, Caplan LR, Donnan GA, Hennerici MG. New approach to stroke subtyping: the A-S-C-O (phenotypic) classification of stroke. Cerebrovasc Dis. 2009; 27:502–508.
Article
7. Krishnamurthi RV, Feigin VL, Forouzanfar MH, Mensah GA, Connor M, Bennett DA, et al. Global and regional burden of first-ever ischaemic and haemorrhagic stroke during 1990-2010: findings from the Global Burden of Disease Study 2010. Lancet Glob Health. 2013; 1:e259–e281.
Article
8. Bang OY, Saver JL, Liebeskind DS, Pineda S, Yun SW, Ovbiagele B. Impact of metabolic syndrome on distribution of cervicocephalic atherosclerosis: data from a diverse race-ethnic group. J Neurol Sci. 2009; 284:40–45.
Article
9. White H, Boden-Albala B, Wang C, Elkind MS, Rundek T, Wright CB, et al. Ischemic stroke subtype incidence among whites, blacks, and Hispanics: the Northern Manhattan Study. Circulation. 2005; 111:1327–1331.
Article
10. Kim BJ, Kim JS. Ischemic stroke subtype classification: an asian viewpoint. J Stroke. 2014; 16:8–17.
Article
11. Mehndiratta MM, Khan M, Mehndiratta P, Wasay M. Stroke in Asia: geographical variations and temporal trends. J Neurol Neurosurg Psychiatry. 2014; 85:1308–1312.
Article
12. Kim AS, Johnston SC. Global variation in the relative burden of stroke and ischemic heart disease. Circulation. 2011; 124:314–323.
Article
13. Gorelick PB, Wong KS, Bae HJ, Pandey DK. Large artery intracranial occlusive disease: a large worldwide burden but a relatively neglected frontier. Stroke. 2008; 39:2396–2399.
14. Wong LK. Global burden of intracranial atherosclerosis. Int J Stroke. 2006; 1:158–159.
Article
15. Sacco RL, Kargman DE, Zamanillo MC. Race-ethnic differences in stroke risk factors among hospitalized patients with cerebral infarction: the Northern Manhattan Stroke Study. Neurology. 1995; 45:659–663.
Article
16. 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.
Article
17. Xu WH, Li ML, Gao S, Ni J, Yao M, Zhou LX, et al. Middle cerebral artery intraplaque hemorrhage: prevalence and clinical relevance. Ann Neurol. 2012; 71:195–198.
Article
18. Majidi S, Sein J, Watanabe M, Hassan AE, Van de Moortele PF, Suri MF, et al. 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.
Article
19. Kamada F, Aoki Y, Narisawa A, Abe Y, Komatsuzaki S, Kikuchi A, et al. A genome-wide association study identifies RNF213 as the first Moyamoya disease gene. J Hum Genet. 2011; 56:34–40.
Article
20. Liu W, Morito D, Takashima S, Mineharu Y, Kobayashi H, Hitomi T, et al. Identification of RNF213 as a susceptibility gene for moyamoya disease and its possible role in vascular development. PLoS One. 2011; 6:e22542.
Article
21. Fujimura M, Sonobe S, Nishijima Y, Niizuma K, Sakata H, Kure S, et al. Genetics and biomarkers of Moyamoya disease: significance of RNF213 as a susceptibility gene. J Stroke. 2014; 16:65–72.
Article
22. Liu W, Hashikata H, Inoue K, Matsuura N, Mineharu Y, Kobayashi H, et al. A rare Asian founder polymorphism of Raptor may explain the high prevalence of Moyamoya disease among East Asians and its low prevalence among Caucasians. Environ Health Prev Med. 2010; 15:94–104.
Article
23. Liu W, Hitomi T, Kobayashi H, Harada KH, Koizumi A. Distribution of moyamoya disease susceptibility polymorphism p.R4810K in RNF213 in East and Southeast Asian populations. Neurol Med Chir (Tokyo). 2012; 52:299–303.
Article
24. Bang OY, Lee PH, Yoon SR, Lee MA, Joo IS, Huh K. Inflammatory markers, rather than conventional risk factors, are different between carotid and MCA atherosclerosis. J Neurol Neurosurg Psychiatry. 2005; 76:1128–1134.
Article
25. Bang OY, Kim JW, Lee JH, Lee MA, Lee PH, Joo IS, et al. Association of the metabolic syndrome with intracranial atherosclerotic stroke. Neurology. 2005; 65:296–298.
Article
26. López-Cancio E, Galán A, Dorado L, Jiménez M, Hernández M, Millán M, et al. Biological signatures of asymptomatic extra- and intracranial atherosclerosis: the Barcelona-AsIA (Asymptomatic Intracranial Atherosclerosis) study. Stroke. 2012; 43:2712–2719.
Article
27. Akins PT, Pilgram TK, Cross DT 3rd, Moran CJ. Natural history of stenosis from intracranial atherosclerosis by serial angiography. Stroke. 1998; 29:433–438.
Article
28. Ryoo S, Park JH, Kim SJ, Kim GM, Chung CS, Lee KH, et al. Branch occlusive disease: clinical and magnetic resonance angiography findings. Neurology. 2012; 78:888–896.
Article
29. Bang OY. Intracranial atherosclerosis: current understanding and perspectives. J Stroke. 2014; 16:27–35.
Article
30. Mazighi M, Labreuche J, Gongora-Rivera F, Duyckaerts C, Hauw JJ, Amarenco P. Autopsy prevalence of intracranial atherosclerosis in patients with fatal stroke. Stroke. 2008; 39:1142–1147.
Article
31. Xu WH, Li ML, Gao S, Ni J, Zhou LX, Yao M, et al. Plaque distribution of stenotic middle cerebral artery and its clinical relevance. Stroke. 2011; 42:2957–2959.
Article
32. Nah HW, Kang DW, Kwon SU, Kim JS. Diversity of single small subcortical infarctions according to infarct location and parent artery disease: analysis of indicators for small vessel disease and atherosclerosis. Stroke. 2010; 41:2822–2827.
Article
33. Turan TN, Derdeyn CP, Fiorella D, Chimowitz MI. Treatment of atherosclerotic intracranial arterial stenosis. Stroke. 2009; 40:2257–2261.
Article
34. Jackson C, Sudlow C. Comparing risks of death and recurrent vascular events between lacunar and non-lacunar infarction. Brain. 2005; 128(Pt 11):2507–2517.
Article
35. Gouw AA, Seewann A, van der Flier WM, Barkhof F, Rozemuller AM, Scheltens P, et al. Heterogeneity of small vessel disease: a systematic review of MRI and histopathology correlations. J Neurol Neurosurg Psychiatry. 2011; 82:126–135.
Article
36. Charidimou A, Kakar P, Fox Z, Werring DJ. Cerebral microbleeds and recurrent stroke risk: systematic review and meta-analysis of prospective ischemic stroke and transient ischemic attack cohorts. Stroke. 2013; 44:995–1001.
37. Gouw AA, van der Flier WM, Fazekas F, van Straaten EC, Pantoni L, Poggesi A, et al. Progression of white matter hyperintensities and incidence of new lacunes over a 3-year period: the Leukoaraiosis and Disability study. Stroke. 2008; 39:1414–1420.
Article
38. Conklin J, Silver FL, Mikulis DJ, Mandell DM. Are acute infarcts the cause of leukoaraiosis? Brain mapping for 16 consecutive weeks. Ann Neurol. 2014; 76:899–904.
Article
39. Park JH, Ryoo S, Kim SJ, Kim GM, Chung CS, Lee KH, et al. Differential risk factors for lacunar stroke depending on the MRI (white and red) subtypes of microangiopathy. PLoS One. 2012; 7:e44865.
Article
40. Liu W, Liu R, Sun W, Peng Q, Zhang W, Xu E, et al. Different impacts of blood pressure variability on the progression of cerebral microbleeds and white matter lesions. Stroke. 2012; 43:2916–2922.
Article
41. Shoamanesh A, Preis SR, Beiser AS, Vasan RS, Benjamin EJ, Kase CS, et al. Inflammatory biomarkers, cerebral microbleeds, and small vessel disease: Framingham Heart Study. Neurology. 2015; 84:825–832.
Article
42. Vernooij MW, Haag MD, van der Lugt A, Hofman A, Krestin GP, Stricker BH, et al. Use of antithrombotic drugs and the presence of cerebral microbleeds: the Rotterdam Scan Study. Arch Neurol. 2009; 66:714–720.
Article
43. Soo YO, Yang SR, Lam WW, Wong A, Fan YH, Leung HH, et al. Risk vs benefit of anti-thrombotic therapy in ischaemic stroke patients with cerebral microbleeds. J Neurol. 2008; 255:1679–1686.
Article
44. Kim SJ, Ryoo S, Kwon S, Park YK, Kim JP, Lee GY, et al. Is atrial fibrillation always a culprit of stroke in patients with atrial fibrillation plus stroke? Cerebrovasc Dis. 2013; 36:373–382.
Article
45. Bang OY, Ovbiagele B, Kim JS. Evaluation of cryptogenic stroke with advanced diagnostic techniques. Stroke. 2014; 45:1186–1194.
Article
46. Ryoo S, Cha J, Kim SJ, Choi JW, Ki CS, Kim KH, et al. High-resolution magnetic resonance wall imaging findings of Moyamoya disease. Stroke. 2014; 45:2457–2460.
Article
47. 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.
Article
48. Ahn SH, Lee J, Kim YJ, Kwon SU, Lee D, Jung SC, et al. Isolated MCA disease in patients without significant atherosclerotic risk factors: a high-resolution magnetic resonance imaging study. Stroke. 2015; 46:697–703.
Article
49. 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.
Article
50. 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.
Article
51. Wysokinski WE, Ammash N, Sobande F, Kalsi H, Hodge D, McBane RD. Predicting left atrial thrombi in atrial fibrillation. Am Heart J. 2010; 159:665–671.
Article
52. Okuyama H, Hirono O, Liu L, Takeishi Y, Kayama T, Kubota I. Higher levels of serum fibrin-monomer reflect hypercoagulable state and thrombus formation in the left atrial appendage in patients with acute ischemic stroke. Circ J. 2006; 70:971–976.
Article
53. Rodríguez-Yáñez M, Arias-Rivas S, Santamaría-Cadavid M, Sobrino T, Castillo J, Blanco M. High pro-BNP levels predict the occurrence of atrial fibrillation after cryptogenic stroke. Neurology. 2013; 81:444–447.
Article
54. Jickling GC, Stamova B, Ander BP, Zhan X, Liu D, Sison SM, et al. Prediction of cardioembolic, arterial, and lacunar causes of cryptogenic stroke by gene expression and infarct location. Stroke. 2012; 43:2036–2041.
Article
55. Di Biase L, Santangeli P, Anselmino M, Mohanty P, Salvetti I, Gili S, et al. Does the left atrial appendage morphology correlate with the risk of stroke in patients with atrial fibrillation? Results from a multicenter study. J Am Coll Cardiol. 2012; 60:531–538.
Article
56. Lee JM, Shim J, Uhm JS, Kim YJ, Lee HJ, Pak HN, et al. Impact of increased orifice size and decreased flow velocity of left atrial appendage on stroke in nonvalvular atrial fibrillation. Am J Cardiol. 2014; 113:963–969.
Article
57. Jeong WK, Choi JH, Son JP, Lee S, Lee MJ, Choe YH, et al. Volume and morphology of left atrial appendage as determinants of stroke subtype in patients with atrial fibrillation. Heart Rhythm. 2015.
Article
Full Text Links
  • JCN
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr