The differences and associations among acute and non-acute cerebral small vessel disease and the related imaging markers_West China Medical Journal

Authors：

XU Mangmang , JIANG Shuai , TAO Wendan ,  LIU Ming

Center of Cerebrovascular Diseases, Department of Neurology, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;

Corresponding author：

LIU Ming, Email: wyplmh@hotmail.com

Keywords：

Acute cerebral small vessel disease; Imaging markers of cerebral small vessel disease; Lacunar cerebral infarction; Cerebral hemorrhage; Cerebral amyloid angiopathy

DOI：

10.7507/1002-0179.202104269

Video：

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Abstract Full text Figures/Tables Video References Cited by

Cerebral small vessel disease is a common neurological disease, including acute and non-acute categories. With the development of neuroimaging, cerebral small vessel disease has attracted substantial attention in recent years. However, the categories and concepts of cerebral small vessel disease and the related imaging markers usually confuse people. The purpose of this study was to discuss the relationships among acute and non-acute cerebral small vessel disease and the imaging markers, so as to improve the understanding of cerebral small vessel disease, and to shed light on clinical practice and research.

Citation： XU Mangmang, JIANG Shuai, TAO Wendan, LIU Ming. The differences and associations among acute and non-acute cerebral small vessel disease and the related imaging markers. West China Medical Journal, 2021, 36(6): 725-730. doi: 10.7507/1002-0179.202104269 Copy

1.	Wardlaw JM, Smith C, Dichgans M. Small vessel disease: mechanisms and clinical implications. Lancet Neurol, 2019, 18(7): 684-696.
2.	严玉颖, 吴波, 张舒婷. 急性脑小血管病的定义和临床特征. 华西医学, 2019, 34(10): 1091-1095.
3.	吴波, 刘鸣. 重视急性脑小血管病的诊治与研究. 中华神经科杂志, 2021. doi: 10.3760/cma.j.cn113694-20210114-00037.
4.	Zhang X, Ding L, Yuan J, et al. Spatial relationship between acute lacunar infarction and white matter hyperintensities. Eur Neurol, 2015, 74(5-6): 259-266.
5.	Duering M, Csanadi E, Gesierich B, et al. Incident lacunes preferentially localize to the edge of white matter hyperintensities: insights into the pathophysiology of cerebral small vessel disease. Brain, 2013, 136(Pt 9): 2717-2726.
6.	Loos CMJ, Makin SDJ, Staals J, et al. Long-term morphological changes of symptomatic lacunar infarcts and surrounding white matter on structural magnetic resonance imaging. Stroke, 2018, 49(5): 1183-1188.
7.	中华医学会神经病学分会, 中华医学会神经病学分会脑血管病学组. 中国急性缺血性脑卒中诊治指南 2018. 中华神经科杂志, 2018, 51(9): 666-682.
8.	Barow E, Boutitie F, Cheng B, et al. Functional outcome of intravenous thrombolysis in patients with lacunar infarcts in the wake-up trial. JAMA Neurol, 2019, 76(6): 641-649.
9.	Pantoni L, Fierini F, Poggesi A. Thrombolysis in acute stroke patients with cerebral small vessel disease. Cerebrovasc Dis, 2014, 37(1): 5-13.
10.	Álvarez-Sabín J, Maisterra O, Santamarina E, et al. Factors influencing haemorrhagic transformation in ischaemic stroke. Lancet Neurol, 2013, 12(7): 689-705.
11.	Fluri F, Hatz F, Rutgers MP, et al. Intravenous thrombolysis in patients with stroke attributable to small artery occlusion. Eur J Neurol, 2010, 17(8): 1054-1060.
12.	Mustanoja S, Meretoja A, Putaala J, et al. Outcome by stroke etiology in patients receiving thrombolytic treatment: descriptive subtype analysis. Stroke, 2011, 42(1): 102-106.
13.	Appleton JP, Woodhouse LJ, Adami A, et al. Imaging markers of small vessel disease and brain frailty, and outcomes in acute stroke. Neurology, 2020, 94(5): e439-e452.
14.	Jiang J, Huang X, Zhang Y, et al. Total MRI burden of cerebral vessel disease correlates with the progression in patients with acute single small subcortical strokes. Brain Behav, 2019, 9(1): e01173.
15.	Gómez-Choco M, Mengual JJ, Rodríguez-Antigüedad J, et al. Pre-existing cerebral small vessel disease limits early recovery in patients with acute lacunar infarct. J Stroke Cerebrovasc Dis, 2019, 28(11): 104312.
16.	Tang WK, Chen YK, Lu JY, et al. Cerebral microbleeds and depression in lacunar stroke. Stroke, 2011, 42(9): 2443-2446.
17.	Zhang X, Tang Y, Xie Y, et al. Total magnetic resonance imaging burden of cerebral small-vessel disease is associated with post-stroke depression in patients with acute lacunar stroke. Eur J Neurol, 2017, 24(2): 374-380.
18.	Pasi M, Boulouis G, Fotiadis P, et al. Distribution of lacunes in cerebral amyloid angiopathy and hypertensive small vessel disease. Neurology, 2017, 88(23): 2162-2168.
19.	Schreiber S, Wilisch-Neumann A, Schreiber F, et al. Invited review: the spectrum of age-related small vessel diseases: potential overlap and interactions of amyloid and nonamyloid vasculopathies. Neuropathol Appl Neurobiol, 2020, 46(3): 219-239.
20.	Charidimou A, Perosa V, Frosch MP, et al. Neuropathological correlates of cortical superficial siderosis in cerebral amyloid angiopathy. Brain, 2020, 143(11): 3343-3351.
21.	Charidimou A, Linn J, Vernooij MW, et al. Cortical superficial siderosis: detection and clinical significance in cerebral amyloid angiopathy and related conditions. Brain, 2015, 138(Pt 8): 2126-2139.
22.	Charidimou A, Martinez-Ramirez S, Reijmer YD, et al. Total magnetic resonance imaging burden of small vessel disease in cerebral amyloid angiopathy: an imaging-pathologic study of concept validation. JAMA Neurol, 2016, 73(8): 994-1001.
23.	Pasi M, Sugita L, Xiong L, et al. Association of cerebral small vessel disease and cognitive decline after intracerebral hemorrhage. Neurology, 2021, 96(2): e182-e192.
24.	Charidimou A, Boulouis G, Xiong L, et al. Cortical superficial siderosis evolution. Stroke, 2019, 50(4): 954-962.
25.	Planton M, Pariente J, Nemmi F, et al. Interhemispheric distribution of amyloid and small vessel disease burden in cerebral amyloid angiopathy-related intracerebral hemorrhage. Eur J Neurol, 2020, 27(8): 1664-1671.
26.	Uniken Venema SM, Marini S, Brouwers HB, et al. Associations of radiographic cerebral small vessel disease with acute intracerebral hemorrhage volume, hematoma expansion, and intraventricular hemorrhage. Neurocrit Care, 2020, 32(2): 383-391.
27.	Boulouis G, van Etten ES, Charidimou A, et al. Association of key magnetic resonance imaging markers of cerebral small vessel disease with hematoma volume and expansion in patients with lobar and deep intracerebral hemorrhage. JAMA Neurol, 2016, 73(12): 1440-1447.
28.	Lou M, Al-Hazzani A, Goddeau RP Jr, et al. Relationship between white-matter hyperintensities and hematoma volume and growth in patients with intracerebral hemorrhage. Stroke, 2010, 41(1): 34-40.
29.	Lioutas VA, Wu B, Norton C, et al. Cerebral small vessel disease burden and functional and radiographic outcomes in intracerebral hemorrhage. J Neurol, 2018, 265(12): 2803-2814.
30.	Charidimou A, Imaizumi T, Moulin S, et al. Brain hemorrhage recurrence, small vessel disease type, and cerebral microbleeds: a meta-analysis. Neurology, 2017, 89(8): 820-829.
31.	Greenberg SM, Eng JA, Ning M, et al. Hemorrhage burden predicts recurrent intracerebral hemorrhage after lobar hemorrhage. Stroke, 2004, 35(6): 1415-1420.
32.	Roongpiboonsopit D, Charidimou A, William CM, et al. Cortical superficial siderosis predicts early recurrent lobar hemorrhage. Neurology, 2016, 87(18): 1863-1870.
33.	Xu M, Cheng Y, Song Q, et al. Total burden of cerebral small vessel disease in recurrent ICH versus first-ever ICH. Aging Dis, 2019, 10(3): 570-577.
34.	Xu M, Li B, Zhong D, et al. Cerebral small vessel disease load predicts functional outcome and stroke recurrence after intracerebral hemorrhage: a median follow-up of 5 years. Front Aging Neuroscie, 2021, 13: 628271.
35.	Arntz RM, van den Broek SM, van Uden IW, et al. Accelerated development of cerebral small vessel disease in young stroke patients. Neurology, 2016, 87(12): 1212-1219.
36.	Bivard A, Cheng X, Lin LT, et al. Global white matter hypoperfusion on CT predicts larger infarcts and hemorrhagic transformation after acute ischemia. CNS Neurosci Ther, 2016, 22(3): 238-243.
37.	Wei CC, Zhang ST, Wang YH, et al. Association between leukoaraiosis and hemorrhagic transformation after cardioembolic stroke due to atrial fibrillation and/or rheumatic heart disease. J Neurol Sci, 2017, 378: 94-99.
38.	El Nawar R, Yeung J, Labreuche J, et al. MRI-based predictors of hemorrhagic transformation in patients with stroke treated by intravenous thrombolysis. Front Neurol, 2019, 10: 897.
39.	Albo Z, Marino J, Nagy M, et al. Relationship of white matter lesion severity with early and late outcomes after mechanical thrombectomy for large vessel stroke. J Neurointerv Surg, 2021, 13(1): 19-24.
40.	Boulouis G, Bricout N, Benhassen W, et al. White matter hyperintensity burden in patients with ischemic stroke treated with thrombectomy. Neurology, 2019, 93(16): e1498-e1506.
41.	Henninger N, Kaesmacher J. Mechanical thrombectomy in acute stroke: paying attention to white matter hyperintensities. Neurology, 2019, 93(16): 691-692.
42.	Tsivgoulis G, Zand R, Katsanos AH, et al. Risk of symptomatic intracerebral hemorrhage after intravenous thrombolysis in patients with acute ischemic stroke and high cerebral microbleed burden: a meta-analysis. JAMA Neurol, 2016, 73(6): 675-683.
43.	Chacon-Portillo MA, Llinas RH, Marsh EB. Cerebral microbleeds shouldn’t dictate treatment of acute stroke: a retrospective cohort study evaluating risk of intracerebral hemorrhage. BMC Neurol, 2018, 18(1): 33.
44.	Charidimou A, Turc G, Oppenheim C, et al. Microbleeds, cerebral hemorrhage, and functional outcome after stroke thrombolysis. Stroke, 2017, 48(8): 2084-2090.
45.	Powers WJ, Rabinstein AA, Ackerson T, et al. Guidelines for the early management of patients with acute ischemic stroke: 2019 update to the 2018 guidelines for the early management of acute ischemic stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke, 2019, 50(12): e344-e418.
46.	Liang Y, Song Q, Jiao Y, et al. Cerebral microbleeds and the safety of anticoagulation in ischemic stroke patients: a systematic review and meta-analysis. Clin Neuropharmacol, 2018, 41(6): 202-209.
47.	Wilson D, Ambler G, Shakeshaft C, et al. Cerebral microbleeds and intracranial haemorrhage risk in patients anticoagulated for atrial fibrillation after acute ischaemic stroke or transient ischaemic attack (CROMIS-2): a multicentre observational cohort study. Lancet Neurol, 2018, 17(6): 539-547.
48.	Lovelock CE, Cordonnier C, Naka H, et al. Antithrombotic drug use, cerebral microbleeds, and intracerebral hemorrhage: a systematic review of published and unpublished studies. Stroke, 2010, 41(6): 1222-1228.
49.	Cheng Y, Liu J, Zhang S, et al. Prior antithrombotic therapy is associated with cerebral microbleeds in ischemic stroke patients with atrial fibrillation and/or rheumatic heart disease. Front Neurol, 2018, 9: 1184.
50.	Ryu WS, Woo SH, Schellingerhout D, et al. Stroke outcomes are worse with larger leukoaraiosis volumes. Brain, 2017, 140(1): 158-170.
51.	Baik M, Kim K, Yoo J, et al. Differential impact of white matter hyperintensities on long-term outcomes in ischemic stroke patients with large artery atherosclerosis. PLoS One, 2017, 12(12): e0189611.
52.	Liu J, Wang D, Li J, et al. High serum alkaline phosphatase levels in relation to multi-cerebral microbleeds in acute ischemic stroke patients with atrial fibrillation and/or rheumatic heart disease. Curr Neurovasc Res, 2016, 13(4): 303-308.
53.	Liu J, Wang D, Xiong Y, et al. Association between coagulation function and cerebral microbleeds in ischemic stroke patients with atrial fibrillation and/or rheumatic heart disease. Aging Dis, 2017, 8(2): 131-135.
54.	Liu J, Wang D, Xiong Y, et al. A cohort study of relationship between serum calcium levels and cerebral microbleeds (CMBs) in ischemic stroke patients with AF and/or RHD. Medicine (Baltimore), 2016, 95(26): e4033.
55.	Wei CC, Zhang ST, Liu JF, et al. Association between fibrinogen and leukoaraiosis in patients with ischemic stroke and atrial fibrillation. J Stroke Cerebrovasc Dis, 2017, 26(11): 2630-2637.
56.	Wei C, Zhang S, Liu J, et al. Relationship of cardiac biomarkers with white matter hyperintensities in cardioembolic stroke due to atrial fibrillation and/or rheumatic heart disease. Medicine(Baltimore), 2018, 97(33): e11892.
57.	Lei C, Lin S, Wu B, et al. Lipid levels are regionally associated with cerebral microbleeds in patients with intracerebral hemorrhage. J Stroke Cerebrovasc Dis, 2014, 23(5): 1195-1198.
58.	Xu M, Zhang S, Liu J, et al. Kidney dysfunction is associated with a high burden of cerebral small vessel disease in primary intracerebral hemorrhage. Curr Neurovasc Res, 2018, 15(1): 39-46.

1. Wardlaw JM, Smith C, Dichgans M. Small vessel disease: mechanisms and clinical implications. Lancet Neurol, 2019, 18(7): 684-696.
2. 严玉颖, 吴波, 张舒婷. 急性脑小血管病的定义和临床特征. 华西医学, 2019, 34(10): 1091-1095.
3. 吴波, 刘鸣. 重视急性脑小血管病的诊治与研究. 中华神经科杂志, 2021. doi: 10.3760/cma.j.cn113694-20210114-00037.
4. Zhang X, Ding L, Yuan J, et al. Spatial relationship between acute lacunar infarction and white matter hyperintensities. Eur Neurol, 2015, 74(5-6): 259-266.
5. Duering M, Csanadi E, Gesierich B, et al. Incident lacunes preferentially localize to the edge of white matter hyperintensities: insights into the pathophysiology of cerebral small vessel disease. Brain, 2013, 136(Pt 9): 2717-2726.
6. Loos CMJ, Makin SDJ, Staals J, et al. Long-term morphological changes of symptomatic lacunar infarcts and surrounding white matter on structural magnetic resonance imaging. Stroke, 2018, 49(5): 1183-1188.
7. 中华医学会神经病学分会, 中华医学会神经病学分会脑血管病学组. 中国急性缺血性脑卒中诊治指南 2018. 中华神经科杂志, 2018, 51(9): 666-682.
8. Barow E, Boutitie F, Cheng B, et al. Functional outcome of intravenous thrombolysis in patients with lacunar infarcts in the wake-up trial. JAMA Neurol, 2019, 76(6): 641-649.
9. Pantoni L, Fierini F, Poggesi A. Thrombolysis in acute stroke patients with cerebral small vessel disease. Cerebrovasc Dis, 2014, 37(1): 5-13.
10. Álvarez-Sabín J, Maisterra O, Santamarina E, et al. Factors influencing haemorrhagic transformation in ischaemic stroke. Lancet Neurol, 2013, 12(7): 689-705.
11. Fluri F, Hatz F, Rutgers MP, et al. Intravenous thrombolysis in patients with stroke attributable to small artery occlusion. Eur J Neurol, 2010, 17(8): 1054-1060.
12. Mustanoja S, Meretoja A, Putaala J, et al. Outcome by stroke etiology in patients receiving thrombolytic treatment: descriptive subtype analysis. Stroke, 2011, 42(1): 102-106.
13. Appleton JP, Woodhouse LJ, Adami A, et al. Imaging markers of small vessel disease and brain frailty, and outcomes in acute stroke. Neurology, 2020, 94(5): e439-e452.
14. Jiang J, Huang X, Zhang Y, et al. Total MRI burden of cerebral vessel disease correlates with the progression in patients with acute single small subcortical strokes. Brain Behav, 2019, 9(1): e01173.
15. Gómez-Choco M, Mengual JJ, Rodríguez-Antigüedad J, et al. Pre-existing cerebral small vessel disease limits early recovery in patients with acute lacunar infarct. J Stroke Cerebrovasc Dis, 2019, 28(11): 104312.
16. Tang WK, Chen YK, Lu JY, et al. Cerebral microbleeds and depression in lacunar stroke. Stroke, 2011, 42(9): 2443-2446.
17. Zhang X, Tang Y, Xie Y, et al. Total magnetic resonance imaging burden of cerebral small-vessel disease is associated with post-stroke depression in patients with acute lacunar stroke. Eur J Neurol, 2017, 24(2): 374-380.
18. Pasi M, Boulouis G, Fotiadis P, et al. Distribution of lacunes in cerebral amyloid angiopathy and hypertensive small vessel disease. Neurology, 2017, 88(23): 2162-2168.
19. Schreiber S, Wilisch-Neumann A, Schreiber F, et al. Invited review: the spectrum of age-related small vessel diseases: potential overlap and interactions of amyloid and nonamyloid vasculopathies. Neuropathol Appl Neurobiol, 2020, 46(3): 219-239.
20. Charidimou A, Perosa V, Frosch MP, et al. Neuropathological correlates of cortical superficial siderosis in cerebral amyloid angiopathy. Brain, 2020, 143(11): 3343-3351.
21. Charidimou A, Linn J, Vernooij MW, et al. Cortical superficial siderosis: detection and clinical significance in cerebral amyloid angiopathy and related conditions. Brain, 2015, 138(Pt 8): 2126-2139.
22. Charidimou A, Martinez-Ramirez S, Reijmer YD, et al. Total magnetic resonance imaging burden of small vessel disease in cerebral amyloid angiopathy: an imaging-pathologic study of concept validation. JAMA Neurol, 2016, 73(8): 994-1001.
23. Pasi M, Sugita L, Xiong L, et al. Association of cerebral small vessel disease and cognitive decline after intracerebral hemorrhage. Neurology, 2021, 96(2): e182-e192.
24. Charidimou A, Boulouis G, Xiong L, et al. Cortical superficial siderosis evolution. Stroke, 2019, 50(4): 954-962.
25. Planton M, Pariente J, Nemmi F, et al. Interhemispheric distribution of amyloid and small vessel disease burden in cerebral amyloid angiopathy-related intracerebral hemorrhage. Eur J Neurol, 2020, 27(8): 1664-1671.
26. Uniken Venema SM, Marini S, Brouwers HB, et al. Associations of radiographic cerebral small vessel disease with acute intracerebral hemorrhage volume, hematoma expansion, and intraventricular hemorrhage. Neurocrit Care, 2020, 32(2): 383-391.
27. Boulouis G, van Etten ES, Charidimou A, et al. Association of key magnetic resonance imaging markers of cerebral small vessel disease with hematoma volume and expansion in patients with lobar and deep intracerebral hemorrhage. JAMA Neurol, 2016, 73(12): 1440-1447.
28. Lou M, Al-Hazzani A, Goddeau RP Jr, et al. Relationship between white-matter hyperintensities and hematoma volume and growth in patients with intracerebral hemorrhage. Stroke, 2010, 41(1): 34-40.
29. Lioutas VA, Wu B, Norton C, et al. Cerebral small vessel disease burden and functional and radiographic outcomes in intracerebral hemorrhage. J Neurol, 2018, 265(12): 2803-2814.
30. Charidimou A, Imaizumi T, Moulin S, et al. Brain hemorrhage recurrence, small vessel disease type, and cerebral microbleeds: a meta-analysis. Neurology, 2017, 89(8): 820-829.
31. Greenberg SM, Eng JA, Ning M, et al. Hemorrhage burden predicts recurrent intracerebral hemorrhage after lobar hemorrhage. Stroke, 2004, 35(6): 1415-1420.
32. Roongpiboonsopit D, Charidimou A, William CM, et al. Cortical superficial siderosis predicts early recurrent lobar hemorrhage. Neurology, 2016, 87(18): 1863-1870.
33. Xu M, Cheng Y, Song Q, et al. Total burden of cerebral small vessel disease in recurrent ICH versus first-ever ICH. Aging Dis, 2019, 10(3): 570-577.
34. Xu M, Li B, Zhong D, et al. Cerebral small vessel disease load predicts functional outcome and stroke recurrence after intracerebral hemorrhage: a median follow-up of 5 years. Front Aging Neuroscie, 2021, 13: 628271.
35. Arntz RM, van den Broek SM, van Uden IW, et al. Accelerated development of cerebral small vessel disease in young stroke patients. Neurology, 2016, 87(12): 1212-1219.
36. Bivard A, Cheng X, Lin LT, et al. Global white matter hypoperfusion on CT predicts larger infarcts and hemorrhagic transformation after acute ischemia. CNS Neurosci Ther, 2016, 22(3): 238-243.
37. Wei CC, Zhang ST, Wang YH, et al. Association between leukoaraiosis and hemorrhagic transformation after cardioembolic stroke due to atrial fibrillation and/or rheumatic heart disease. J Neurol Sci, 2017, 378: 94-99.
38. El Nawar R, Yeung J, Labreuche J, et al. MRI-based predictors of hemorrhagic transformation in patients with stroke treated by intravenous thrombolysis. Front Neurol, 2019, 10: 897.
39. Albo Z, Marino J, Nagy M, et al. Relationship of white matter lesion severity with early and late outcomes after mechanical thrombectomy for large vessel stroke. J Neurointerv Surg, 2021, 13(1): 19-24.
40. Boulouis G, Bricout N, Benhassen W, et al. White matter hyperintensity burden in patients with ischemic stroke treated with thrombectomy. Neurology, 2019, 93(16): e1498-e1506.
41. Henninger N, Kaesmacher J. Mechanical thrombectomy in acute stroke: paying attention to white matter hyperintensities. Neurology, 2019, 93(16): 691-692.
42. Tsivgoulis G, Zand R, Katsanos AH, et al. Risk of symptomatic intracerebral hemorrhage after intravenous thrombolysis in patients with acute ischemic stroke and high cerebral microbleed burden: a meta-analysis. JAMA Neurol, 2016, 73(6): 675-683.
43. Chacon-Portillo MA, Llinas RH, Marsh EB. Cerebral microbleeds shouldn’t dictate treatment of acute stroke: a retrospective cohort study evaluating risk of intracerebral hemorrhage. BMC Neurol, 2018, 18(1): 33.
44. Charidimou A, Turc G, Oppenheim C, et al. Microbleeds, cerebral hemorrhage, and functional outcome after stroke thrombolysis. Stroke, 2017, 48(8): 2084-2090.
45. Powers WJ, Rabinstein AA, Ackerson T, et al. Guidelines for the early management of patients with acute ischemic stroke: 2019 update to the 2018 guidelines for the early management of acute ischemic stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke, 2019, 50(12): e344-e418.
46. Liang Y, Song Q, Jiao Y, et al. Cerebral microbleeds and the safety of anticoagulation in ischemic stroke patients: a systematic review and meta-analysis. Clin Neuropharmacol, 2018, 41(6): 202-209.
47. Wilson D, Ambler G, Shakeshaft C, et al. Cerebral microbleeds and intracranial haemorrhage risk in patients anticoagulated for atrial fibrillation after acute ischaemic stroke or transient ischaemic attack (CROMIS-2): a multicentre observational cohort study. Lancet Neurol, 2018, 17(6): 539-547.
48. Lovelock CE, Cordonnier C, Naka H, et al. Antithrombotic drug use, cerebral microbleeds, and intracerebral hemorrhage: a systematic review of published and unpublished studies. Stroke, 2010, 41(6): 1222-1228.
49. Cheng Y, Liu J, Zhang S, et al. Prior antithrombotic therapy is associated with cerebral microbleeds in ischemic stroke patients with atrial fibrillation and/or rheumatic heart disease. Front Neurol, 2018, 9: 1184.
50. Ryu WS, Woo SH, Schellingerhout D, et al. Stroke outcomes are worse with larger leukoaraiosis volumes. Brain, 2017, 140(1): 158-170.
51. Baik M, Kim K, Yoo J, et al. Differential impact of white matter hyperintensities on long-term outcomes in ischemic stroke patients with large artery atherosclerosis. PLoS One, 2017, 12(12): e0189611.
52. Liu J, Wang D, Li J, et al. High serum alkaline phosphatase levels in relation to multi-cerebral microbleeds in acute ischemic stroke patients with atrial fibrillation and/or rheumatic heart disease. Curr Neurovasc Res, 2016, 13(4): 303-308.
53. Liu J, Wang D, Xiong Y, et al. Association between coagulation function and cerebral microbleeds in ischemic stroke patients with atrial fibrillation and/or rheumatic heart disease. Aging Dis, 2017, 8(2): 131-135.
54. Liu J, Wang D, Xiong Y, et al. A cohort study of relationship between serum calcium levels and cerebral microbleeds (CMBs) in ischemic stroke patients with AF and/or RHD. Medicine (Baltimore), 2016, 95(26): e4033.
55. Wei CC, Zhang ST, Liu JF, et al. Association between fibrinogen and leukoaraiosis in patients with ischemic stroke and atrial fibrillation. J Stroke Cerebrovasc Dis, 2017, 26(11): 2630-2637.
56. Wei C, Zhang S, Liu J, et al. Relationship of cardiac biomarkers with white matter hyperintensities in cardioembolic stroke due to atrial fibrillation and/or rheumatic heart disease. Medicine(Baltimore), 2018, 97(33): e11892.
57. Lei C, Lin S, Wu B, et al. Lipid levels are regionally associated with cerebral microbleeds in patients with intracerebral hemorrhage. J Stroke Cerebrovasc Dis, 2014, 23(5): 1195-1198.
58. Xu M, Zhang S, Liu J, et al. Kidney dysfunction is associated with a high burden of cerebral small vessel disease in primary intracerebral hemorrhage. Curr Neurovasc Res, 2018, 15(1): 39-46.

West China Medical Journal

The differences and associations among acute and non-acute cerebral small vessel disease and the related imaging markers

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