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Published in: Journal of Neurology 10/2019

01-10-2019 | Review

Cerebral small vessel disease: neuroimaging markers and clinical implication

Authors: Xiaodong Chen, Jihui Wang, Yilong Shan, Wei Cai, Sanxin Liu, Mengyan Hu, Siyuan Liao, Xuehong Huang, Bingjun Zhang, Yuge Wang, Zhengqi Lu

Published in: Journal of Neurology | Issue 10/2019

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Abstract

Cerebral small vessel disease (CSVD) is a broad category of cerebrovascular diseases which primarily affect the perforating arterioles, capillaries and venules with multiple distinct etiologies. In spite of distinctive pathogenesis, CSVD shares similar neuroimaging markers, including recent small subcortical infarct, lacune of presumed vascular origin, white matter hyperintensity of presumed vascular origin, perivascular space and cerebral microbleeds. The radiological features of neuroimaging markers are indicative for etiological analysis. Furthermore, in sporadic arteriosclerotic pathogenesis associated CSVD, the total CSVD burden is a significant predictor for stroke events, global cognitive impairment, psychiatric disorders and later life quality. This review aims to summarize the radiological characteristics as well as the clinical implication of CSVD markers and neuroimaging interpretation for CSVD symptomatology.
Literature
1.
go back to reference Pantoni L (2010) Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 9:689–701PubMed Pantoni L (2010) Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 9:689–701PubMed
2.
go back to reference Wardlaw JM, Smith EE, Biessels GJ, Cordonnier C, Fazekas F, Frayne R, Lindley RI, O’Brien JT, Barkhof F, Benavente OR, Black SE, Brayne C, Breteler M, Chabriat H, Decarli C, de Leeuw FE, Doubal F, Duering M, Fox NC, Greenberg S, Hachinski V, Kilimann I, Mok V, Oostenbrugge R, Pantoni L, Speck O, Stephan BC, Teipel S, Viswanathan A, Werring D, Chen C, Smith C, van Buchem M, Norrving B, Gorelick PB, Dichgans M (2013) Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol 12:822–838PubMedPubMedCentral Wardlaw JM, Smith EE, Biessels GJ, Cordonnier C, Fazekas F, Frayne R, Lindley RI, O’Brien JT, Barkhof F, Benavente OR, Black SE, Brayne C, Breteler M, Chabriat H, Decarli C, de Leeuw FE, Doubal F, Duering M, Fox NC, Greenberg S, Hachinski V, Kilimann I, Mok V, Oostenbrugge R, Pantoni L, Speck O, Stephan BC, Teipel S, Viswanathan A, Werring D, Chen C, Smith C, van Buchem M, Norrving B, Gorelick PB, Dichgans M (2013) Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol 12:822–838PubMedPubMedCentral
3.
go back to reference Staals J, Makin SD, Doubal FN, Dennis MS, Wardlaw JM (2014) Stroke subtype, vascular risk factors, and total MRI brain small-vessel disease burden. Neurology 83:1228–1234PubMedPubMedCentral Staals J, Makin SD, Doubal FN, Dennis MS, Wardlaw JM (2014) Stroke subtype, vascular risk factors, and total MRI brain small-vessel disease burden. Neurology 83:1228–1234PubMedPubMedCentral
4.
go back to reference Li Y, Li M, Zuo L, Shi Q, Qin W, Yang L, Jiang T, Hu W (2018) Compromised blood–brain barrier integrity is associated with total magnetic resonance imaging burden of cerebral small vessel disease. Front Neurol 9:221PubMedPubMedCentral Li Y, Li M, Zuo L, Shi Q, Qin W, Yang L, Jiang T, Hu W (2018) Compromised blood–brain barrier integrity is associated with total magnetic resonance imaging burden of cerebral small vessel disease. Front Neurol 9:221PubMedPubMedCentral
5.
go back to reference Pavlovic AM, Pekmezovic T, Zidverc Trajkovic J, Svabic Medjedovic T, Veselinovic N, Radojicic A, Mijajlovic M, Tomic G, Jovanovic Z, Norton M, Sternic N (2016) Baseline characteristic of patients presenting with lacunar stroke and cerebral small vessel disease may predict future development of depression. Int J Geriatr Psychiatry 31:58–65PubMed Pavlovic AM, Pekmezovic T, Zidverc Trajkovic J, Svabic Medjedovic T, Veselinovic N, Radojicic A, Mijajlovic M, Tomic G, Jovanovic Z, Norton M, Sternic N (2016) Baseline characteristic of patients presenting with lacunar stroke and cerebral small vessel disease may predict future development of depression. Int J Geriatr Psychiatry 31:58–65PubMed
6.
go back to reference Zhang X, Tang Y, Xie Y, Ding C, Xiao J, Jiang X, Shan H, Lin Y, Li C, Hu D, Li T, Sheng L (2017) 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 24:374–380PubMed Zhang X, Tang Y, Xie Y, Ding C, Xiao J, Jiang X, Shan H, Lin Y, Li C, Hu D, Li T, Sheng L (2017) 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 24:374–380PubMed
7.
go back to reference Liang Y, Chen YK, Deng M, Mok VCT, Wang DF, Ungvari GS, Chu CW, Kamiya A, Tang WK (2017) Association of cerebral small vessel disease burden and health-related quality of life after acute ischemic stroke. Front Aging Neurosci 9:372PubMedPubMedCentral Liang Y, Chen YK, Deng M, Mok VCT, Wang DF, Ungvari GS, Chu CW, Kamiya A, Tang WK (2017) Association of cerebral small vessel disease burden and health-related quality of life after acute ischemic stroke. Front Aging Neurosci 9:372PubMedPubMedCentral
8.
go back to reference Sacco S, Marini C, Totaro R, Russo T, Cerone D, Carolei A (2006) A population-based study of the incidence and prognosis of lacunar stroke. Neurology 66:1335–1338PubMed Sacco S, Marini C, Totaro R, Russo T, Cerone D, Carolei A (2006) A population-based study of the incidence and prognosis of lacunar stroke. Neurology 66:1335–1338PubMed
9.
go back to reference Moran C, Phan TG, Srikanth VK (2012) Cerebral small vessel disease: a review of clinical, radiological, and histopathological phenotypes. Int J Stroke 7:36–46PubMed Moran C, Phan TG, Srikanth VK (2012) Cerebral small vessel disease: a review of clinical, radiological, and histopathological phenotypes. Int J Stroke 7:36–46PubMed
10.
go back to reference Arboix A, Estevez S, Rouco R, Oliveres M, Garcia-Eroles L, Massons J (2015) Clinical characteristics of acute lacunar stroke in young adults. Exp Rev Neurother 15:825–831 Arboix A, Estevez S, Rouco R, Oliveres M, Garcia-Eroles L, Massons J (2015) Clinical characteristics of acute lacunar stroke in young adults. Exp Rev Neurother 15:825–831
11.
go back to reference Rutten-Jacobs LCA, Markus HS (2017) Vascular risk factor profiles differ between magnetic resonance imaging-defined subtypes of younger-onset lacunar stroke. Stroke 48:2405–2411PubMedPubMedCentral Rutten-Jacobs LCA, Markus HS (2017) Vascular risk factor profiles differ between magnetic resonance imaging-defined subtypes of younger-onset lacunar stroke. Stroke 48:2405–2411PubMedPubMedCentral
12.
go back to reference Zhu S, McClure LA, Lau H, Romero JR, White CL, Babikian V, Nguyen T, Benavente OR, Kase CS, Pikula A (2015) Recurrent vascular events in lacunar stroke patients with metabolic syndrome and/or diabetes. Neurology 85:935–941PubMedPubMedCentral Zhu S, McClure LA, Lau H, Romero JR, White CL, Babikian V, Nguyen T, Benavente OR, Kase CS, Pikula A (2015) Recurrent vascular events in lacunar stroke patients with metabolic syndrome and/or diabetes. Neurology 85:935–941PubMedPubMedCentral
13.
go back to reference Klarenbeek P, van Oostenbrugge RJ, Rouhl RP, Knottnerus IL, Staals J (2013) Ambulatory blood pressure in patients with lacunar stroke: association with total MRI burden of cerebral small vessel disease. Stroke 44:2995–2999PubMed Klarenbeek P, van Oostenbrugge RJ, Rouhl RP, Knottnerus IL, Staals J (2013) Ambulatory blood pressure in patients with lacunar stroke: association with total MRI burden of cerebral small vessel disease. Stroke 44:2995–2999PubMed
14.
go back to reference Benavente OR, Coffey CS, Conwit R, Hart RG, McClure LA, Pearce LA, Pergola PE, Szychowski JM (2013) Blood-pressure targets in patients with recent lacunar stroke: the SPS3 randomised trial. Lancet 382:507–515PubMed Benavente OR, Coffey CS, Conwit R, Hart RG, McClure LA, Pearce LA, Pergola PE, Szychowski JM (2013) Blood-pressure targets in patients with recent lacunar stroke: the SPS3 randomised trial. Lancet 382:507–515PubMed
15.
go back to reference Arboix A, Font A, Garro C, Garcia-Eroles L, Comes E, Massons J (2007) Recurrent lacunar infarction following a previous lacunar stroke: a clinical study of 122 patients. J Neurol Neurosurg Psychiatry 78:1392–1394PubMedPubMedCentral Arboix A, Font A, Garro C, Garcia-Eroles L, Comes E, Massons J (2007) Recurrent lacunar infarction following a previous lacunar stroke: a clinical study of 122 patients. J Neurol Neurosurg Psychiatry 78:1392–1394PubMedPubMedCentral
16.
go back to reference Traylor M, Bevan S, Baron JC, Hassan A, Lewis CM, Markus HS (2015) Genetic architecture of lacunar stroke. Stroke 46:2407–2412PubMedPubMedCentral Traylor M, Bevan S, Baron JC, Hassan A, Lewis CM, Markus HS (2015) Genetic architecture of lacunar stroke. Stroke 46:2407–2412PubMedPubMedCentral
17.
go back to reference Neurology Working Group of the Cohorts for Heart and Aging Research in Genomic Epidemiology (CHARGE) Consortium tSGNS, and the International Stroke Genetics Consortium (ISGC) (2016) Identification of additional risk loci for stroke and small vessel disease: a meta-analysis of genome-wide association studies. Lancet Neurol 15:695–707 Neurology Working Group of the Cohorts for Heart and Aging Research in Genomic Epidemiology (CHARGE) Consortium tSGNS, and the International Stroke Genetics Consortium (ISGC) (2016) Identification of additional risk loci for stroke and small vessel disease: a meta-analysis of genome-wide association studies. Lancet Neurol 15:695–707
18.
go back to reference Traylor M, Rutten-Jacobs LC, Thijs V, Holliday EG, Levi C, Bevan S, Malik R, Boncoraglio G, Sudlow C, Rothwell PM, Dichgans M, Markus HS (2016) Genetic associations with white matter hyperintensities confer risk of lacunar stroke. Stroke 47:1174–1179PubMedPubMedCentral Traylor M, Rutten-Jacobs LC, Thijs V, Holliday EG, Levi C, Bevan S, Malik R, Boncoraglio G, Sudlow C, Rothwell PM, Dichgans M, Markus HS (2016) Genetic associations with white matter hyperintensities confer risk of lacunar stroke. Stroke 47:1174–1179PubMedPubMedCentral
19.
go back to reference Fisher CM (1991) Lacunar infarct: a review. Cerebrovasc Dis 1:311–320 Fisher CM (1991) Lacunar infarct: a review. Cerebrovasc Dis 1:311–320
20.
go back to reference Arboix A, Lopez-Grau M, Casasnovas C, Garcia-Eroles L, Massons J, Balcells M (2006) Clinical study of 39 patients with atypical lacunar syndrome. J Neurol Neurosurg Psychiatry 77:381–384PubMedPubMedCentral Arboix A, Lopez-Grau M, Casasnovas C, Garcia-Eroles L, Massons J, Balcells M (2006) Clinical study of 39 patients with atypical lacunar syndrome. J Neurol Neurosurg Psychiatry 77:381–384PubMedPubMedCentral
21.
go back to reference Grau-Olivares M, Arboix A, Bartres-Faz D, Junque C (2007) Neuropsychological abnormalities associated with lacunar infarction. J Neurol Sci 257:160–165PubMed Grau-Olivares M, Arboix A, Bartres-Faz D, Junque C (2007) Neuropsychological abnormalities associated with lacunar infarction. J Neurol Sci 257:160–165PubMed
22.
go back to reference Blanco-Rojas L, Arboix A, Canovas D, Grau-Olivares M, Oliva Morera JC, Parra O (2013) Cognitive profile in patients with a first-ever lacunar infarct with and without silent lacunes: a comparative study. BMC neurology 13:203PubMedPubMedCentral Blanco-Rojas L, Arboix A, Canovas D, Grau-Olivares M, Oliva Morera JC, Parra O (2013) Cognitive profile in patients with a first-ever lacunar infarct with and without silent lacunes: a comparative study. BMC neurology 13:203PubMedPubMedCentral
23.
go back to reference Bonnin-Vilaplana M, Arboix A, Parra O, Garcia-Eroles L, Montserrat JM, Massons J (2009) Sleep-related breathing disorders in acute lacunar stroke. J Neurol 256:2036–2042PubMed Bonnin-Vilaplana M, Arboix A, Parra O, Garcia-Eroles L, Montserrat JM, Massons J (2009) Sleep-related breathing disorders in acute lacunar stroke. J Neurol 256:2036–2042PubMed
24.
go back to reference Arboix A, Marti-Vilalta JL (2004) New concepts in lacunar stroke etiology: the constellation of small-vessel arterial disease. Cerebrovasc Dis 17(Suppl 1):58–62PubMed Arboix A, Marti-Vilalta JL (2004) New concepts in lacunar stroke etiology: the constellation of small-vessel arterial disease. Cerebrovasc Dis 17(Suppl 1):58–62PubMed
25.
go back to reference Arboix A, Blanco-Rojas L, Marti-Vilalta JL (2014) Advancements in understanding the mechanisms of symptomatic lacunar ischemic stroke: translation of knowledge to prevention strategies. Expert Rev Neurother 14:261–276PubMed Arboix A, Blanco-Rojas L, Marti-Vilalta JL (2014) Advancements in understanding the mechanisms of symptomatic lacunar ischemic stroke: translation of knowledge to prevention strategies. Expert Rev Neurother 14:261–276PubMed
26.
go back to reference Benavente OR, Pearce LA, Bazan C, Roldan AM, Catanese L, Bhat Livezey VM, Vidal-Pergola G, McClure LA, Hart RG (2014) Clinical-MRI correlations in a multiethnic cohort with recent lacunar stroke: the SPS3 trial. Int J Stroke 9:1057–1064PubMed Benavente OR, Pearce LA, Bazan C, Roldan AM, Catanese L, Bhat Livezey VM, Vidal-Pergola G, McClure LA, Hart RG (2014) Clinical-MRI correlations in a multiethnic cohort with recent lacunar stroke: the SPS3 trial. Int J Stroke 9:1057–1064PubMed
27.
go back to reference Valdes Hernandez MD, Qiu X, Wang X, Wiseman S, Sakka E, Maconick LC, Doubal F, Sudlow CL, Wardlaw JM (2017) Interhemispheric characterization of small vessel disease imaging markers after subcortical infarct. Brain Behav 7:e00595PubMed Valdes Hernandez MD, Qiu X, Wang X, Wiseman S, Sakka E, Maconick LC, Doubal F, Sudlow CL, Wardlaw JM (2017) Interhemispheric characterization of small vessel disease imaging markers after subcortical infarct. Brain Behav 7:e00595PubMed
28.
go back to reference Valdes Hernandez Mdel C, Maconick LC, Munoz Maniega S, Wang X, Wiseman S, Armitage PA, Doubal FN, Makin S, Sudlow CL, Dennis MS, Deary IJ, Bastin M, Wardlaw JM (2015) A comparison of location of acute symptomatic vs. ‘silent’ small vessel lesions. Int J Stroke 10:1044–1050PubMed Valdes Hernandez Mdel C, Maconick LC, Munoz Maniega S, Wang X, Wiseman S, Armitage PA, Doubal FN, Makin S, Sudlow CL, Dennis MS, Deary IJ, Bastin M, Wardlaw JM (2015) A comparison of location of acute symptomatic vs. ‘silent’ small vessel lesions. Int J Stroke 10:1044–1050PubMed
29.
go back to reference Duan Z, Fu C, Chen B, Xu G, Tao L, Tang T, Hou H, Fu X, Yang M, Liu Z, Zhang X (2015) Lesion patterns of single small subcortical infarct and its association with early neurological deterioration. Neurol Sci 36:1851–1857PubMed Duan Z, Fu C, Chen B, Xu G, Tao L, Tang T, Hou H, Fu X, Yang M, Liu Z, Zhang X (2015) Lesion patterns of single small subcortical infarct and its association with early neurological deterioration. Neurol Sci 36:1851–1857PubMed
30.
go back to reference Duan Z, Sun W, Liu W, Xiao L, Huang Z, Cao L, Li H, Xiong Y, Liu D, Xu G, Liu X (2015) Acute diffusion-weighted imaging lesion patterns predict progressive small subcortical infarct in the perforator territory of the middle cerebral artery. Int J Stroke 10:207–212PubMed Duan Z, Sun W, Liu W, Xiao L, Huang Z, Cao L, Li H, Xiong Y, Liu D, Xu G, Liu X (2015) Acute diffusion-weighted imaging lesion patterns predict progressive small subcortical infarct in the perforator territory of the middle cerebral artery. Int J Stroke 10:207–212PubMed
31.
go back to reference Arboix A, Garcia-Plata C, Garcia-Eroles L, Massons J, Comes E, Oliveres M, Targa C (2005) Clinical study of 99 patients with pure sensory stroke. J Neurol 252:156–162PubMed Arboix A, Garcia-Plata C, Garcia-Eroles L, Massons J, Comes E, Oliveres M, Targa C (2005) Clinical study of 99 patients with pure sensory stroke. J Neurol 252:156–162PubMed
32.
go back to reference Arboix A, Padilla I, Massons J, Garcia-Eroles L, Comes E, Targa C (2001) Clinical study of 222 patients with pure motor stroke. J Neurol Neurosurg Psychiatry 71:239–242PubMedPubMedCentral Arboix A, Padilla I, Massons J, Garcia-Eroles L, Comes E, Targa C (2001) Clinical study of 222 patients with pure motor stroke. J Neurol Neurosurg Psychiatry 71:239–242PubMedPubMedCentral
33.
go back to reference Duering M, Csanadi E, Gesierich B, Jouvent E, Herve D, Seiler S, Belaroussi B, Ropele S, Schmidt R, Chabriat H, Dichgans M (2013) Incident lacunes preferentially localize to the edge of white matter hyperintensities: insights into the pathophysiology of cerebral small vessel disease. Brain 136:2717–2726PubMed Duering M, Csanadi E, Gesierich B, Jouvent E, Herve D, Seiler S, Belaroussi B, Ropele S, Schmidt R, Chabriat H, Dichgans M (2013) Incident lacunes preferentially localize to the edge of white matter hyperintensities: insights into the pathophysiology of cerebral small vessel disease. Brain 136:2717–2726PubMed
34.
go back to reference Gesierich B, Duchesnay E, Jouvent E, Chabriat H, Schmidt R, Mangin JF, Duering M, Dichgans M (2016) Features and determinants of lacune shape: relationship with fiber tracts and perforating arteries. Stroke 47:1258–1264PubMed Gesierich B, Duchesnay E, Jouvent E, Chabriat H, Schmidt R, Mangin JF, Duering M, Dichgans M (2016) Features and determinants of lacune shape: relationship with fiber tracts and perforating arteries. Stroke 47:1258–1264PubMed
35.
go back to reference Tsai HH, Pasi M, Tsai LK, Chen YF, Lee BC, Tang SC, Fotiadis P, Huang CY, Yen RF, Gurol ME, Jeng JS (2018) Distribution of lacunar infarcts in asians with intracerebral hemorrhage: a magnetic resonance imaging and amyloid positron emission tomography study. Stroke 49:1515–1517PubMedPubMedCentral Tsai HH, Pasi M, Tsai LK, Chen YF, Lee BC, Tang SC, Fotiadis P, Huang CY, Yen RF, Gurol ME, Jeng JS (2018) Distribution of lacunar infarcts in asians with intracerebral hemorrhage: a magnetic resonance imaging and amyloid positron emission tomography study. Stroke 49:1515–1517PubMedPubMedCentral
36.
go back to reference Hong YJ, Kim CM, Kim JE, Roh JH, Kim JS, Seo SW, Na DL, Lee JH (2017) Regional amyloid burden and lacune in pure subcortical vascular cognitive impairment. Neurobiol Aging 55:20–26PubMed Hong YJ, Kim CM, Kim JE, Roh JH, Kim JS, Seo SW, Na DL, Lee JH (2017) Regional amyloid burden and lacune in pure subcortical vascular cognitive impairment. Neurobiol Aging 55:20–26PubMed
37.
go back to reference Benjamin P, Trippier S, Lawrence AJ, Lambert C, Zeestraten E, Williams OA, Patel B, Morris RG, Barrick TR, MacKinnon AD, Markus HS (2018) Lacunar infarcts, but not perivascular spaces, are predictors of cognitive decline in cerebral small-vessel disease. Stroke 49:586–593PubMedPubMedCentral Benjamin P, Trippier S, Lawrence AJ, Lambert C, Zeestraten E, Williams OA, Patel B, Morris RG, Barrick TR, MacKinnon AD, Markus HS (2018) Lacunar infarcts, but not perivascular spaces, are predictors of cognitive decline in cerebral small-vessel disease. Stroke 49:586–593PubMedPubMedCentral
38.
go back to reference Chen Y, Wang A, Tang J, Wei D, Li P, Chen K, Wang Y, Zhang Z (2015) Association of white matter integrity and cognitive functions in patients with subcortical silent lacunar infarcts. Stroke 46:1123–1126PubMed Chen Y, Wang A, Tang J, Wei D, Li P, Chen K, Wang Y, Zhang Z (2015) Association of white matter integrity and cognitive functions in patients with subcortical silent lacunar infarcts. Stroke 46:1123–1126PubMed
39.
go back to reference Reijmer YD, Freeze WM, Leemans A, Biessels GJ (2013) The effect of lacunar infarcts on white matter tract integrity. Stroke 44:2019–2021PubMed Reijmer YD, Freeze WM, Leemans A, Biessels GJ (2013) The effect of lacunar infarcts on white matter tract integrity. Stroke 44:2019–2021PubMed
40.
go back to reference Thong JY, Hilal S, Wang Y, Soon HW, Dong Y, Collinson SL, Anh TT, Ikram MK, Wong TY, Venketasubramanian N, Chen C, Qiu A (2013) Association of silent lacunar infarct with brain atrophy and cognitive impairment. J Neurol Neurosurg Psychiatry 84:1219–1225PubMed Thong JY, Hilal S, Wang Y, Soon HW, Dong Y, Collinson SL, Anh TT, Ikram MK, Wong TY, Venketasubramanian N, Chen C, Qiu A (2013) Association of silent lacunar infarct with brain atrophy and cognitive impairment. J Neurol Neurosurg Psychiatry 84:1219–1225PubMed
41.
go back to reference Makin SD, Turpin S, Dennis MS, Wardlaw JM (2013) Cognitive impairment after lacunar stroke: systematic review and meta-analysis of incidence, prevalence and comparison with other stroke subtypes. J Neurol Neurosurg Psychiatry 84:893–900PubMed Makin SD, Turpin S, Dennis MS, Wardlaw JM (2013) Cognitive impairment after lacunar stroke: systematic review and meta-analysis of incidence, prevalence and comparison with other stroke subtypes. J Neurol Neurosurg Psychiatry 84:893–900PubMed
42.
go back to reference van Leijsen EMC, Bergkamp MI, van Uden IWM, Ghafoorian M, van der Holst HM, Norris DG, Platel B, Tuladhar AM, de Leeuw FE (2018) Progression of white matter hyperintensities preceded by heterogeneous decline of microstructural integrity. Stroke 49:1386–1393PubMed van Leijsen EMC, Bergkamp MI, van Uden IWM, Ghafoorian M, van der Holst HM, Norris DG, Platel B, Tuladhar AM, de Leeuw FE (2018) Progression of white matter hyperintensities preceded by heterogeneous decline of microstructural integrity. Stroke 49:1386–1393PubMed
43.
go back to reference Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA (1987) MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. Am J Roentgenol 149:351–356 Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA (1987) MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. Am J Roentgenol 149:351–356
45.
go back to reference Shim YS, Yang DW, Roe CM, Coats MA, Benzinger TL, Xiong C, Galvin JE, Cairns NJ, Morris JC (2015) Pathological correlates of white matter hyperintensities on magnetic resonance imaging. Dement Geriatr Cogn Disord 39:92–104PubMed Shim YS, Yang DW, Roe CM, Coats MA, Benzinger TL, Xiong C, Galvin JE, Cairns NJ, Morris JC (2015) Pathological correlates of white matter hyperintensities on magnetic resonance imaging. Dement Geriatr Cogn Disord 39:92–104PubMed
47.
go back to reference Osborn KE, Liu D, Samuels LR, Moore EE, Cambronero FE, Acosta LMY, Bell SP, Babicz MA, Gordon EA, Pechman KR, Davis LT, Gifford KA, Hohman TJ, Blennow K, Zetterberg H, Jefferson AL (2018) Cerebrospinal fluid beta-amyloid42 and neurofilament light relate to white matter hyperintensities. Neurobiol Aging 68:18–25PubMedPubMedCentral Osborn KE, Liu D, Samuels LR, Moore EE, Cambronero FE, Acosta LMY, Bell SP, Babicz MA, Gordon EA, Pechman KR, Davis LT, Gifford KA, Hohman TJ, Blennow K, Zetterberg H, Jefferson AL (2018) Cerebrospinal fluid beta-amyloid42 and neurofilament light relate to white matter hyperintensities. Neurobiol Aging 68:18–25PubMedPubMedCentral
48.
go back to reference Scott JA, Braskie MN, Tosun D, Maillard P, Thompson PM, Weiner M, DeCarli C, Carmichael OT (2016) Cerebral amyloid is associated with greater white-matter hyperintensity accrual in cognitively normal older adults. Neurobiol Aging 48:48–52PubMedPubMedCentral Scott JA, Braskie MN, Tosun D, Maillard P, Thompson PM, Weiner M, DeCarli C, Carmichael OT (2016) Cerebral amyloid is associated with greater white-matter hyperintensity accrual in cognitively normal older adults. Neurobiol Aging 48:48–52PubMedPubMedCentral
49.
go back to reference Valdes Hernandez M, Allerhand M, Glatz A, Clayson L, Munoz Maniega S, Gow A, Royle N, Bastin M, Starr J, Deary I, Wardlaw J (2016) Do white matter hyperintensities mediate the association between brain iron deposition and cognitive abilities in older people? Eur J Neurol 23:1202–1209PubMedPubMedCentral Valdes Hernandez M, Allerhand M, Glatz A, Clayson L, Munoz Maniega S, Gow A, Royle N, Bastin M, Starr J, Deary I, Wardlaw J (2016) Do white matter hyperintensities mediate the association between brain iron deposition and cognitive abilities in older people? Eur J Neurol 23:1202–1209PubMedPubMedCentral
50.
go back to reference Nam KW, Kwon HM, Jeong HY, Park JH, Kim SH, Jeong SM, Yoo TG, Kim S (2017) Cerebral white matter hyperintensity is associated with intracranial atherosclerosis in a healthy population. Atherosclerosis 265:179–183PubMed Nam KW, Kwon HM, Jeong HY, Park JH, Kim SH, Jeong SM, Yoo TG, Kim S (2017) Cerebral white matter hyperintensity is associated with intracranial atherosclerosis in a healthy population. Atherosclerosis 265:179–183PubMed
51.
go back to reference Squair JW, Field TS, Phillips AA (2018) Journal club: relationship between carotid arterial properties and cerebral white matter hyperintensities. Neurology 90:338–340PubMedPubMedCentral Squair JW, Field TS, Phillips AA (2018) Journal club: relationship between carotid arterial properties and cerebral white matter hyperintensities. Neurology 90:338–340PubMedPubMedCentral
52.
go back to reference Della-Morte D, Dong C, Markert MS, Elkind MSV, Sacco RL, Wright CB, Rundek T (2018) Carotid intima-media thickness is associated with white matter hyperintensities: the Northern Manhattan study. Stroke 49:304–311PubMed Della-Morte D, Dong C, Markert MS, Elkind MSV, Sacco RL, Wright CB, Rundek T (2018) Carotid intima-media thickness is associated with white matter hyperintensities: the Northern Manhattan study. Stroke 49:304–311PubMed
53.
go back to reference Park JH, Kwon HM, Lee J, Kim DS, Ovbiagele B (2015) Association of intracranial atherosclerotic stenosis with severity of white matter hyperintensities. Eur J Neurol 22:44–52, e42–43PubMed Park JH, Kwon HM, Lee J, Kim DS, Ovbiagele B (2015) Association of intracranial atherosclerotic stenosis with severity of white matter hyperintensities. Eur J Neurol 22:44–52, e42–43PubMed
54.
go back to reference Rostanski SK, Zimmerman ME, Schupf N, Manly JJ, Westwood AJ, Brickman AM, Gu Y (2016) Sleep disordered breathing and white matter hyperintensities in community-dwelling elders. Sleep 39:785–791PubMedPubMedCentral Rostanski SK, Zimmerman ME, Schupf N, Manly JJ, Westwood AJ, Brickman AM, Gu Y (2016) Sleep disordered breathing and white matter hyperintensities in community-dwelling elders. Sleep 39:785–791PubMedPubMedCentral
55.
go back to reference Cloonan L, Fitzpatrick KM, Kanakis AS, Furie KL, Rosand J, Rost NS (2015) Metabolic determinants of white matter hyperintensity burden in patients with ischemic stroke. Atherosclerosis 240:149–153PubMedPubMedCentral Cloonan L, Fitzpatrick KM, Kanakis AS, Furie KL, Rosand J, Rost NS (2015) Metabolic determinants of white matter hyperintensity burden in patients with ischemic stroke. Atherosclerosis 240:149–153PubMedPubMedCentral
56.
go back to reference Silbert LC, Lahna D, Promjunyakul NO, Boespflug E, Ohya Y, Higashiuesato Y, Nishihira J, Katsumata Y, Tokashiki T, Dodge HH (2018) Risk factors associated with cortical thickness and white matter hyperintensities in dementia free Okinawan elderly. J Alzheimers Dis 63:365–372PubMedPubMedCentral Silbert LC, Lahna D, Promjunyakul NO, Boespflug E, Ohya Y, Higashiuesato Y, Nishihira J, Katsumata Y, Tokashiki T, Dodge HH (2018) Risk factors associated with cortical thickness and white matter hyperintensities in dementia free Okinawan elderly. J Alzheimers Dis 63:365–372PubMedPubMedCentral
57.
go back to reference Molad J, Kliper E, Korczyn AD, Ben Assayag E, Ben Bashat D, Shenhar-Tsarfaty S, Aizenstein O, Shopin L, Bornstein NM, Auriel E (2017) Only white matter hyperintensities predicts post-stroke cognitive performances among cerebral small vessel disease markers: results from the TABASCO study. J Alzheimers Dis 56:1293–1299PubMed Molad J, Kliper E, Korczyn AD, Ben Assayag E, Ben Bashat D, Shenhar-Tsarfaty S, Aizenstein O, Shopin L, Bornstein NM, Auriel E (2017) Only white matter hyperintensities predicts post-stroke cognitive performances among cerebral small vessel disease markers: results from the TABASCO study. J Alzheimers Dis 56:1293–1299PubMed
59.
go back to reference Moon SY, de Souto Barreto P, Rolland Y, Chupin M, Bouyahia A, Fillon L, Mangin JF, Andrieu S, Cesari M, Vellas B (2018) Prospective associations between white matter hyperintensities and lower extremity function. Neurology 90:e1291–e1297PubMed Moon SY, de Souto Barreto P, Rolland Y, Chupin M, Bouyahia A, Fillon L, Mangin JF, Andrieu S, Cesari M, Vellas B (2018) Prospective associations between white matter hyperintensities and lower extremity function. Neurology 90:e1291–e1297PubMed
60.
go back to reference Habes M, Erus G, Toledo JB, Bryan N, Janowitz D, Doshi J, Volzke H, Schminke U, Hoffmann W, Grabe HJ, Wolk DA, Davatzikos C (2018) Regional tract-specific white matter hyperintensities are associated with patterns to aging-related brain atrophy via vascular risk factors, but also independently. Alzheimer’s Dement (Amsterdam, Neth) 10:278–284 Habes M, Erus G, Toledo JB, Bryan N, Janowitz D, Doshi J, Volzke H, Schminke U, Hoffmann W, Grabe HJ, Wolk DA, Davatzikos C (2018) Regional tract-specific white matter hyperintensities are associated with patterns to aging-related brain atrophy via vascular risk factors, but also independently. Alzheimer’s Dement (Amsterdam, Neth) 10:278–284
61.
go back to reference Tuladhar AM, Reid AT, Shumskaya E, de Laat KF, van Norden AG, van Dijk EJ, Norris DG, de Leeuw FE (2015) Relationship between white matter hyperintensities, cortical thickness, and cognition. Stroke 46:425–432PubMed Tuladhar AM, Reid AT, Shumskaya E, de Laat KF, van Norden AG, van Dijk EJ, Norris DG, de Leeuw FE (2015) Relationship between white matter hyperintensities, cortical thickness, and cognition. Stroke 46:425–432PubMed
62.
go back to reference Kynast J, Lampe L, Luck T, Frisch S, Arelin K, Hoffmann KT, Loeffler M, Riedel-Heller SG, Villringer A, Schroeter ML (2018) White matter hyperintensities associated with small vessel disease impair social cognition beside attention and memory. J Cereb Blood Flow Metab 38:996–1009PubMed Kynast J, Lampe L, Luck T, Frisch S, Arelin K, Hoffmann KT, Loeffler M, Riedel-Heller SG, Villringer A, Schroeter ML (2018) White matter hyperintensities associated with small vessel disease impair social cognition beside attention and memory. J Cereb Blood Flow Metab 38:996–1009PubMed
63.
go back to reference van den Berg E, Geerlings MI, Biessels GJ, Nederkoorn PJ, Kloppenborg RP (2018) White matter hyperintensities and cognition in mild cognitive impairment and Alzheimer’s disease: a domain-specific meta-analysis. J Alzheimers Dis 63:515–527PubMed van den Berg E, Geerlings MI, Biessels GJ, Nederkoorn PJ, Kloppenborg RP (2018) White matter hyperintensities and cognition in mild cognitive impairment and Alzheimer’s disease: a domain-specific meta-analysis. J Alzheimers Dis 63:515–527PubMed
64.
go back to reference Iliff JJ, Lee H, Yu M, Feng T, Logan J, Nedergaard M, Benveniste H (2013) Brain-wide pathway for waste clearance captured by contrast-enhanced MRI. J Clin Investig 123:1299–1309PubMedPubMedCentral Iliff JJ, Lee H, Yu M, Feng T, Logan J, Nedergaard M, Benveniste H (2013) Brain-wide pathway for waste clearance captured by contrast-enhanced MRI. J Clin Investig 123:1299–1309PubMedPubMedCentral
65.
go back to reference Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, Benveniste H, Vates GE, Deane R, Goldman SA, Nagelhus EA, Nedergaard M (2012) A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci Transl Med 4:147ra111PubMedPubMedCentral Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, Benveniste H, Vates GE, Deane R, Goldman SA, Nagelhus EA, Nedergaard M (2012) A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci Transl Med 4:147ra111PubMedPubMedCentral
66.
go back to reference Weed LH (1914) Studies on cerebro-spinal fluid. No. III: The pathways of escape from the subarachnoid spaces with particular reference to the arachnoid villi. J Med Res 31:51–91PubMedPubMedCentral Weed LH (1914) Studies on cerebro-spinal fluid. No. III: The pathways of escape from the subarachnoid spaces with particular reference to the arachnoid villi. J Med Res 31:51–91PubMedPubMedCentral
67.
go back to reference Aspelund A, Antila S, Proulx ST, Karlsen TV, Karaman S, Detmar M, Wiig H, Alitalo K (2015) A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules. J Exp Med 212:991–999PubMedPubMedCentral Aspelund A, Antila S, Proulx ST, Karlsen TV, Karaman S, Detmar M, Wiig H, Alitalo K (2015) A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules. J Exp Med 212:991–999PubMedPubMedCentral
68.
go back to reference Louveau A, Smirnov I, Keyes TJ, Eccles JD, Rouhani SJ, Peske JD, Derecki NC, Castle D, Mandell JW, Lee KS, Harris TH, Kipnis J (2015) Structural and functional features of central nervous system lymphatic vessels. Nature 523:337–341PubMedPubMedCentral Louveau A, Smirnov I, Keyes TJ, Eccles JD, Rouhani SJ, Peske JD, Derecki NC, Castle D, Mandell JW, Lee KS, Harris TH, Kipnis J (2015) Structural and functional features of central nervous system lymphatic vessels. Nature 523:337–341PubMedPubMedCentral
69.
go back to reference Hurford R, Charidimou A, Fox Z, Cipolotti L, Jager R, Werring DJ (2014) MRI-visible perivascular spaces: relationship to cognition and small vessel disease MRI markers in ischaemic stroke and TIA. J Neurol Neurosurg Psychiatry 85:522–525PubMed Hurford R, Charidimou A, Fox Z, Cipolotti L, Jager R, Werring DJ (2014) MRI-visible perivascular spaces: relationship to cognition and small vessel disease MRI markers in ischaemic stroke and TIA. J Neurol Neurosurg Psychiatry 85:522–525PubMed
70.
go back to reference Shams S, Martola J, Charidimou A, Larvie M, Granberg T, Shams M, Kristoffersen-Wiberg M, Wahlund LO (2017) Topography and determinants of magnetic resonance imaging (MRI)-visible perivascular spaces in a large memory clinic cohort. J Am Heart Assoc 6:e006279PubMedPubMedCentral Shams S, Martola J, Charidimou A, Larvie M, Granberg T, Shams M, Kristoffersen-Wiberg M, Wahlund LO (2017) Topography and determinants of magnetic resonance imaging (MRI)-visible perivascular spaces in a large memory clinic cohort. J Am Heart Assoc 6:e006279PubMedPubMedCentral
71.
go back to reference Zhu YC, Tzourio C, Soumare A, Mazoyer B, Dufouil C, Chabriat H (2010) Severity of dilated Virchow–Robin spaces is associated with age, blood pressure, and MRI markers of small vessel disease: a population-based study. Stroke 41:2483–2490PubMed Zhu YC, Tzourio C, Soumare A, Mazoyer B, Dufouil C, Chabriat H (2010) Severity of dilated Virchow–Robin spaces is associated with age, blood pressure, and MRI markers of small vessel disease: a population-based study. Stroke 41:2483–2490PubMed
72.
go back to reference Xiao L, Lan W, Sun W, Dai Q, Xiong Y, Li L, Zhou Y, Zheng P, Fan W, Ma N, Guo Z, Chen X, Xie X, Xu L, Zhu W, Xu G, Liu X (2015) Chronic kidney disease in patients with lacunar stroke: association with enlarged perivascular spaces and total magnetic resonance imaging burden of cerebral small vessel disease. Stroke 46:2081–2086PubMed Xiao L, Lan W, Sun W, Dai Q, Xiong Y, Li L, Zhou Y, Zheng P, Fan W, Ma N, Guo Z, Chen X, Xie X, Xu L, Zhu W, Xu G, Liu X (2015) Chronic kidney disease in patients with lacunar stroke: association with enlarged perivascular spaces and total magnetic resonance imaging burden of cerebral small vessel disease. Stroke 46:2081–2086PubMed
73.
go back to reference Yang S, Zhang X, Yuan J, Yin J, Hu W (2017) Serum uric acid is independently associated with enlarged perivascular spaces. Sci Rep 7:16435PubMedPubMedCentral Yang S, Zhang X, Yuan J, Yin J, Hu W (2017) Serum uric acid is independently associated with enlarged perivascular spaces. Sci Rep 7:16435PubMedPubMedCentral
74.
go back to reference Duperron MG, Tzourio C, Sargurupremraj M, Mazoyer B, Soumare A, Schilling S, Amouyel P, Chauhan G, Zhu YC, Debette S (2018) Burden of dilated perivascular spaces, an emerging marker of cerebral small vessel disease, is highly heritable. Stroke 49:282–287PubMed Duperron MG, Tzourio C, Sargurupremraj M, Mazoyer B, Soumare A, Schilling S, Amouyel P, Chauhan G, Zhu YC, Debette S (2018) Burden of dilated perivascular spaces, an emerging marker of cerebral small vessel disease, is highly heritable. Stroke 49:282–287PubMed
75.
go back to reference Charidimou A, Meegahage R, Fox Z, Peeters A, Vandermeeren Y, Laloux P, Baron JC, Jager HR, Werring DJ (2013) Enlarged perivascular spaces as a marker of underlying arteriopathy in intracerebral haemorrhage: a multicentre MRI cohort study. J Neurol Neurosurg Psychiatry 84:624–629PubMed Charidimou A, Meegahage R, Fox Z, Peeters A, Vandermeeren Y, Laloux P, Baron JC, Jager HR, Werring DJ (2013) Enlarged perivascular spaces as a marker of underlying arteriopathy in intracerebral haemorrhage: a multicentre MRI cohort study. J Neurol Neurosurg Psychiatry 84:624–629PubMed
76.
go back to reference Riba-Llena I, Jimenez-Balado J, Castane X, Girona A, Lopez-Rueda A, Mundet X, Jarca CI, Alvarez-Sabin J, Montaner J, Delgado P (2018) Arterial stiffness is associated with basal ganglia enlarged perivascular spaces and cerebral small vessel disease load. Stroke 49:1279–1281PubMed Riba-Llena I, Jimenez-Balado J, Castane X, Girona A, Lopez-Rueda A, Mundet X, Jarca CI, Alvarez-Sabin J, Montaner J, Delgado P (2018) Arterial stiffness is associated with basal ganglia enlarged perivascular spaces and cerebral small vessel disease load. Stroke 49:1279–1281PubMed
77.
go back to reference Del Brutto OH, Mera RM (2017) Enlarged perivascular spaces in the basal ganglia are independently associated with intracranial atherosclerosis in the elderly. Atherosclerosis 267:34–38PubMed Del Brutto OH, Mera RM (2017) Enlarged perivascular spaces in the basal ganglia are independently associated with intracranial atherosclerosis in the elderly. Atherosclerosis 267:34–38PubMed
78.
go back to reference van Veluw SJ, Biessels GJ, Bouvy WH, Spliet WG, Zwanenburg JJ, Luijten PR, Macklin EA, Rozemuller AJ, Gurol ME, Greenberg SM, Viswanathan A, Martinez-Ramirez S (2016) Cerebral amyloid angiopathy severity is linked to dilation of juxtacortical perivascular spaces. J Cereb Blood Flow Metab 36:576–580PubMed van Veluw SJ, Biessels GJ, Bouvy WH, Spliet WG, Zwanenburg JJ, Luijten PR, Macklin EA, Rozemuller AJ, Gurol ME, Greenberg SM, Viswanathan A, Martinez-Ramirez S (2016) Cerebral amyloid angiopathy severity is linked to dilation of juxtacortical perivascular spaces. J Cereb Blood Flow Metab 36:576–580PubMed
79.
go back to reference Charidimou A, Hong YT, Jager HR, Fox Z, Aigbirhio FI, Fryer TD, Menon DK, Warburton EA, Werring DJ, Baron JC (2015) White matter perivascular spaces on magnetic resonance imaging: marker of cerebrovascular amyloid burden? Stroke 46:1707–1709PubMed Charidimou A, Hong YT, Jager HR, Fox Z, Aigbirhio FI, Fryer TD, Menon DK, Warburton EA, Werring DJ, Baron JC (2015) White matter perivascular spaces on magnetic resonance imaging: marker of cerebrovascular amyloid burden? Stroke 46:1707–1709PubMed
80.
go back to reference Hansen TP, Cain J, Thomas O, Jackson A (2015) Dilated perivascular spaces in the Basal Ganglia are a biomarker of small-vessel disease in a very elderly population with dementia. Am J Neuroradiol 36:893–898PubMedPubMedCentral Hansen TP, Cain J, Thomas O, Jackson A (2015) Dilated perivascular spaces in the Basal Ganglia are a biomarker of small-vessel disease in a very elderly population with dementia. Am J Neuroradiol 36:893–898PubMedPubMedCentral
81.
go back to reference Yao M, Zhu YC, Soumare A, Dufouil C, Mazoyer B, Tzourio C, Chabriat H (2014) Hippocampal perivascular spaces are related to aging and blood pressure but not to cognition. Neurobiol Aging 35:2118–2125PubMed Yao M, Zhu YC, Soumare A, Dufouil C, Mazoyer B, Tzourio C, Chabriat H (2014) Hippocampal perivascular spaces are related to aging and blood pressure but not to cognition. Neurobiol Aging 35:2118–2125PubMed
82.
go back to reference Jimenez-Balado J, Riba-Llena I, Garde E, Valor M, Gutierrez B, Pujadas F, Delgado P (2018) Prevalence of hippocampal enlarged perivascular spaces in a sample of patients with hypertension and their relation with vascular risk factors and cognitive function. J Neurol Neurosurg Psychiatry 89:651–656PubMed Jimenez-Balado J, Riba-Llena I, Garde E, Valor M, Gutierrez B, Pujadas F, Delgado P (2018) Prevalence of hippocampal enlarged perivascular spaces in a sample of patients with hypertension and their relation with vascular risk factors and cognitive function. J Neurol Neurosurg Psychiatry 89:651–656PubMed
83.
go back to reference Zhu YC, Dufouil C, Mazoyer B, Soumare A, Ricolfi F, Tzourio C, Chabriat H (2011) Frequency and location of dilated Virchow–Robin spaces in elderly people: a population-based 3D MR imaging study. Am J Neuroradiol 32:709–713PubMedPubMedCentral Zhu YC, Dufouil C, Mazoyer B, Soumare A, Ricolfi F, Tzourio C, Chabriat H (2011) Frequency and location of dilated Virchow–Robin spaces in elderly people: a population-based 3D MR imaging study. Am J Neuroradiol 32:709–713PubMedPubMedCentral
84.
go back to reference Bouvy WH, Zwanenburg JJ, Reinink R, Wisse LE, Luijten PR, Kappelle LJ, Geerlings MI, Biessels GJ (2016) Perivascular spaces on 7 T brain MRI are related to markers of small vessel disease but not to age or cardiovascular risk factors. J Cereb Blood Flow Metab 36:1708–1717PubMedPubMedCentral Bouvy WH, Zwanenburg JJ, Reinink R, Wisse LE, Luijten PR, Kappelle LJ, Geerlings MI, Biessels GJ (2016) Perivascular spaces on 7 T brain MRI are related to markers of small vessel disease but not to age or cardiovascular risk factors. J Cereb Blood Flow Metab 36:1708–1717PubMedPubMedCentral
85.
go back to reference Liang Y, Chan YL, Deng M, Chen YK, Mok V, Wang F, Ungvari GS, Chu CW, Tang WK (2018) Enlarged perivascular spaces in the centrum semiovale are associated with poststroke depression: a 3-month prospective study. J Affect Disord 228:166–172PubMed Liang Y, Chan YL, Deng M, Chen YK, Mok V, Wang F, Ungvari GS, Chu CW, Tang WK (2018) Enlarged perivascular spaces in the centrum semiovale are associated with poststroke depression: a 3-month prospective study. J Affect Disord 228:166–172PubMed
86.
go back to reference Arba F, Quinn TJ, Hankey GJ, Lees KR, Wardlaw JM, Ali M, Inzitari D (2018) Enlarged perivascular spaces and cognitive impairment after stroke and transient ischemic attack. Int J Stroke 13:47–56PubMed Arba F, Quinn TJ, Hankey GJ, Lees KR, Wardlaw JM, Ali M, Inzitari D (2018) Enlarged perivascular spaces and cognitive impairment after stroke and transient ischemic attack. Int J Stroke 13:47–56PubMed
87.
go back to reference Ding J, Sigurethsson S, Jonsson PV, Eiriksdottir G, Charidimou A, Lopez OL, van Buchem MA, Guethnason V, Launer LJ (2017) Large perivascular spaces visible on magnetic resonance imaging, cerebral small vessel disease progression, and risk of dementia: the age, gene/environment susceptibility-Reykjavik study. JAMA Neurol 74:1105–1112PubMedPubMedCentral Ding J, Sigurethsson S, Jonsson PV, Eiriksdottir G, Charidimou A, Lopez OL, van Buchem MA, Guethnason V, Launer LJ (2017) Large perivascular spaces visible on magnetic resonance imaging, cerebral small vessel disease progression, and risk of dementia: the age, gene/environment susceptibility-Reykjavik study. JAMA Neurol 74:1105–1112PubMedPubMedCentral
88.
go back to reference Ishikawa M, Yamada S, Yamamoto K (2018) Dilated perivascular spaces in the centrum semiovale begin to develop in middle age. J Alzheimers Dis 61:1619–1626PubMed Ishikawa M, Yamada S, Yamamoto K (2018) Dilated perivascular spaces in the centrum semiovale begin to develop in middle age. J Alzheimers Dis 61:1619–1626PubMed
89.
go back to reference Charidimou A, Jaunmuktane Z, Baron JC, Burnell M, Varlet P, Peeters A, Xuereb J, Jager R, Brandner S, Werring DJ (2014) White matter perivascular spaces: an MRI marker in pathology-proven cerebral amyloid angiopathy? Neurology 82:57–62PubMedPubMedCentral Charidimou A, Jaunmuktane Z, Baron JC, Burnell M, Varlet P, Peeters A, Xuereb J, Jager R, Brandner S, Werring DJ (2014) White matter perivascular spaces: an MRI marker in pathology-proven cerebral amyloid angiopathy? Neurology 82:57–62PubMedPubMedCentral
90.
go back to reference Banerjee G, Kim HJ, Fox Z, Jager HR, Wilson D, Charidimou A, Na HK, Na DL, Seo SW, Werring DJ (2017) MRI-visible perivascular space location is associated with Alzheimer’s disease independently of amyloid burden. Brain 140:1107–1116PubMed Banerjee G, Kim HJ, Fox Z, Jager HR, Wilson D, Charidimou A, Na HK, Na DL, Seo SW, Werring DJ (2017) MRI-visible perivascular space location is associated with Alzheimer’s disease independently of amyloid burden. Brain 140:1107–1116PubMed
91.
go back to reference Laveskog A, Wang R, Bronge L, Wahlund LO, Qiu C (2018) Perivascular spaces in old age: assessment, distribution, and correlation with white matter hyperintensities. Am J Neuroradiol 39:70–76PubMedPubMedCentral Laveskog A, Wang R, Bronge L, Wahlund LO, Qiu C (2018) Perivascular spaces in old age: assessment, distribution, and correlation with white matter hyperintensities. Am J Neuroradiol 39:70–76PubMedPubMedCentral
92.
go back to reference Lee WJ, Jung KH, Ryu YJ, Kim JM, Lee ST, Chu K, Kim M, Lee SK, Roh JK (2018) Association of cardiac hemodynamic factors with severity of white matter hyperintensities in chronic valvular heart disease. JAMA Neurol 75:80–87PubMed Lee WJ, Jung KH, Ryu YJ, Kim JM, Lee ST, Chu K, Kim M, Lee SK, Roh JK (2018) Association of cardiac hemodynamic factors with severity of white matter hyperintensities in chronic valvular heart disease. JAMA Neurol 75:80–87PubMed
93.
go back to reference Shams S, Granberg T, Martola J, Charidimou A, Li X, Shams M, Fereshtehnejad SM, Cavallin L, Aspelin P, Wiberg-Kristoffersen M, Wahlund LO (2017) Cerebral microbleeds topography and cerebrospinal fluid biomarkers in cognitive impairment. J Cereb Blood Flow Metab 37:1006–1013PubMed Shams S, Granberg T, Martola J, Charidimou A, Li X, Shams M, Fereshtehnejad SM, Cavallin L, Aspelin P, Wiberg-Kristoffersen M, Wahlund LO (2017) Cerebral microbleeds topography and cerebrospinal fluid biomarkers in cognitive impairment. J Cereb Blood Flow Metab 37:1006–1013PubMed
94.
go back to reference Akoudad S, Portegies ML, Koudstaal PJ, Hofman A, van der Lugt A, Ikram MA, Vernooij MW (2015) Cerebral microbleeds are associated with an increased risk of stroke: the Rotterdam study. Circulation 132:509–516PubMed Akoudad S, Portegies ML, Koudstaal PJ, Hofman A, van der Lugt A, Ikram MA, Vernooij MW (2015) Cerebral microbleeds are associated with an increased risk of stroke: the Rotterdam study. Circulation 132:509–516PubMed
95.
go back to reference Laible M, Horstmann S, Mohlenbruch M, Wegele C, Rizos T, Schuler S, Zorn M, Veltkamp R (2015) Renal dysfunction is associated with deep cerebral microbleeds but not white matter hyperintensities in patients with acute intracerebral hemorrhage. J Neurol 262:2312–2322PubMed Laible M, Horstmann S, Mohlenbruch M, Wegele C, Rizos T, Schuler S, Zorn M, Veltkamp R (2015) Renal dysfunction is associated with deep cerebral microbleeds but not white matter hyperintensities in patients with acute intracerebral hemorrhage. J Neurol 262:2312–2322PubMed
96.
go back to reference Romero JR, Preis SR, Beiser A, DeCarli C, Viswanathan A, Martinez-Ramirez S, Kase CS, Wolf PA, Seshadri S (2014) Risk factors, stroke prevention treatments, and prevalence of cerebral microbleeds in the Framingham Heart Study. Stroke 45:1492–1494PubMedPubMedCentral Romero JR, Preis SR, Beiser A, DeCarli C, Viswanathan A, Martinez-Ramirez S, Kase CS, Wolf PA, Seshadri S (2014) Risk factors, stroke prevention treatments, and prevalence of cerebral microbleeds in the Framingham Heart Study. Stroke 45:1492–1494PubMedPubMedCentral
97.
go back to reference Yang Q, Yang Y, Li C, Li J, Liu X, Wang A, Zhao J, Wang M, Zeng X, Fan D (2015) Quantitative assessment and correlation analysis of cerebral microbleed distribution and leukoaraiosis in stroke outpatients. Neurol Res 37:403–409PubMed Yang Q, Yang Y, Li C, Li J, Liu X, Wang A, Zhao J, Wang M, Zeng X, Fan D (2015) Quantitative assessment and correlation analysis of cerebral microbleed distribution and leukoaraiosis in stroke outpatients. Neurol Res 37:403–409PubMed
98.
go back to reference Chung CP, Chou KH, Chen WT, Liu LK, Lee WJ, Huang AC, Chen LK, Lin CP, Wang PN (2017) Location of cerebral microbleeds and their association with carotid intima-media thickness: a community-based study. Sci Rep 7:12058PubMedPubMedCentral Chung CP, Chou KH, Chen WT, Liu LK, Lee WJ, Huang AC, Chen LK, Lin CP, Wang PN (2017) Location of cerebral microbleeds and their association with carotid intima-media thickness: a community-based study. Sci Rep 7:12058PubMedPubMedCentral
99.
go back to reference Ding L, Hong Y, Peng B (2017) Association between large artery atherosclerosis and cerebral microbleeds: a systematic review and meta-analysis. Stroke Vasc Neurol 2:7–14PubMedPubMedCentral Ding L, Hong Y, Peng B (2017) Association between large artery atherosclerosis and cerebral microbleeds: a systematic review and meta-analysis. Stroke Vasc Neurol 2:7–14PubMedPubMedCentral
100.
go back to reference Romero JR, Preis SR, Beiser A, DeCarli C, D’Agostino RB, Wolf PA, Vasan RS, Polak JF, Seshadri S (2016) Carotid atherosclerosis and cerebral microbleeds: the Framingham Heart Study. J Am Heart Assoc 5:e002377PubMedPubMedCentral Romero JR, Preis SR, Beiser A, DeCarli C, D’Agostino RB, Wolf PA, Vasan RS, Polak JF, Seshadri S (2016) Carotid atherosclerosis and cerebral microbleeds: the Framingham Heart Study. J Am Heart Assoc 5:e002377PubMedPubMedCentral
101.
go back to reference Ding J, Mitchell GF, Bots ML, Sigurdsson S, Harris TB, Garcia M, Eiriksdottir G, van Buchem MA, Gudnason V, Launer LJ (2015) Carotid arterial stiffness and risk of incident cerebral microbleeds in older people: the Age, Gene/Environment Susceptibility (AGES)-Reykjavik study. Arterioscler Thromb Vasc Biol 35:1889–1895PubMedPubMedCentral Ding J, Mitchell GF, Bots ML, Sigurdsson S, Harris TB, Garcia M, Eiriksdottir G, van Buchem MA, Gudnason V, Launer LJ (2015) Carotid arterial stiffness and risk of incident cerebral microbleeds in older people: the Age, Gene/Environment Susceptibility (AGES)-Reykjavik study. Arterioscler Thromb Vasc Biol 35:1889–1895PubMedPubMedCentral
102.
go back to reference Banerjee G, Wahab KW, Gregoire SM, Jichi F, Charidimou A, Jager HR, Rantell K, Werring DJ (2016) Impaired renal function is related to deep and mixed, but not strictly lobar cerebral microbleeds in patients with ischaemic stroke and TIA. J Neurol 263:760–764PubMed Banerjee G, Wahab KW, Gregoire SM, Jichi F, Charidimou A, Jager HR, Rantell K, Werring DJ (2016) Impaired renal function is related to deep and mixed, but not strictly lobar cerebral microbleeds in patients with ischaemic stroke and TIA. J Neurol 263:760–764PubMed
103.
go back to reference Overbeek EC, Staals J, van Oostenbrugge RJ (2016) Decreased kidney function relates to progression of cerebral microbleeds in lacunar stroke patients. Int J Stroke 11:695–700PubMed Overbeek EC, Staals J, van Oostenbrugge RJ (2016) Decreased kidney function relates to progression of cerebral microbleeds in lacunar stroke patients. Int J Stroke 11:695–700PubMed
104.
go back to reference Zhang JB, Liu LF, Li ZG, Sun HR, Ju XH (2015) Associations between biomarkers of renal function with cerebral microbleeds in hypertensive patients. Am J Hypertens 28:739–745PubMed Zhang JB, Liu LF, Li ZG, Sun HR, Ju XH (2015) Associations between biomarkers of renal function with cerebral microbleeds in hypertensive patients. Am J Hypertens 28:739–745PubMed
105.
go back to reference Ding J, Sigurdsson S, Garcia M, Phillips CL, Eiriksdottir G, Gudnason V, van Buchem MA, Launer LJ (2015) Risk factors associated with incident cerebral microbleeds according to location in older people: the age, gene/environment susceptibility (AGES)-Reykjavik study. JAMA Neurol 72:682–688PubMedPubMedCentral Ding J, Sigurdsson S, Garcia M, Phillips CL, Eiriksdottir G, Gudnason V, van Buchem MA, Launer LJ (2015) Risk factors associated with incident cerebral microbleeds according to location in older people: the age, gene/environment susceptibility (AGES)-Reykjavik study. JAMA Neurol 72:682–688PubMedPubMedCentral
106.
go back to reference Chung PW, Park KY, Kim JM, Shin DW, Ha SY (2014) Carotid artery calcification is associated with deep cerebral microbleeds. Eur Neurol 72:60–63PubMed Chung PW, Park KY, Kim JM, Shin DW, Ha SY (2014) Carotid artery calcification is associated with deep cerebral microbleeds. Eur Neurol 72:60–63PubMed
107.
go back to reference Yates PA, Desmond PM, Phal PM, Steward C, Szoeke C, Salvado O, Ellis KA, Martins RN, Masters CL, Ames D, Villemagne VL, Rowe CC (2014) Incidence of cerebral microbleeds in preclinical Alzheimer disease. Neurology 82:1266–1273PubMedPubMedCentral Yates PA, Desmond PM, Phal PM, Steward C, Szoeke C, Salvado O, Ellis KA, Martins RN, Masters CL, Ames D, Villemagne VL, Rowe CC (2014) Incidence of cerebral microbleeds in preclinical Alzheimer disease. Neurology 82:1266–1273PubMedPubMedCentral
108.
go back to reference Gregg NM, Kim AE, Gurol ME, Lopez OL, Aizenstein HJ, Price JC, Mathis CA, James JA, Snitz BE, Cohen AD, Kamboh MI, Minhas D, Weissfeld LA, Tamburo EL, Klunk WE (2015) Incidental cerebral microbleeds and cerebral blood flow in elderly individuals. JAMA Neurol 72:1021–1028PubMedPubMedCentral Gregg NM, Kim AE, Gurol ME, Lopez OL, Aizenstein HJ, Price JC, Mathis CA, James JA, Snitz BE, Cohen AD, Kamboh MI, Minhas D, Weissfeld LA, Tamburo EL, Klunk WE (2015) Incidental cerebral microbleeds and cerebral blood flow in elderly individuals. JAMA Neurol 72:1021–1028PubMedPubMedCentral
109.
go back to reference Graff-Radford J, Simino J, Kantarci K, Mosley TH Jr, Griswold ME, Windham BG, Sharrett AR, Albert MS, Gottesman RF, Jack CR Jr, Vemuri P, Knopman DS (2017) Neuroimaging correlates of cerebral microbleeds: The ARIC study (Atherosclerosis Risk in Communities). Stroke 48:2964–2972PubMedPubMedCentral Graff-Radford J, Simino J, Kantarci K, Mosley TH Jr, Griswold ME, Windham BG, Sharrett AR, Albert MS, Gottesman RF, Jack CR Jr, Vemuri P, Knopman DS (2017) Neuroimaging correlates of cerebral microbleeds: The ARIC study (Atherosclerosis Risk in Communities). Stroke 48:2964–2972PubMedPubMedCentral
110.
go back to reference Akoudad S, Wolters FJ, Viswanathan A, de Bruijn RF, van der Lugt A, Hofman A, Koudstaal PJ, Ikram MA, Vernooij MW (2016) Association of cerebral microbleeds with cognitive decline and dementia. JAMA Neurol 73:934–943PubMedPubMedCentral Akoudad S, Wolters FJ, Viswanathan A, de Bruijn RF, van der Lugt A, Hofman A, Koudstaal PJ, Ikram MA, Vernooij MW (2016) Association of cerebral microbleeds with cognitive decline and dementia. JAMA Neurol 73:934–943PubMedPubMedCentral
111.
go back to reference Chung CP, Chou KH, Chen WT, Liu LK, Lee WJ, Chen LK, Lin CP, Wang PN (2016) Strictly lobar cerebral microbleeds are associated with cognitive impairment. Stroke 47:2497–2502PubMed Chung CP, Chou KH, Chen WT, Liu LK, Lee WJ, Chen LK, Lin CP, Wang PN (2016) Strictly lobar cerebral microbleeds are associated with cognitive impairment. Stroke 47:2497–2502PubMed
112.
go back to reference Marti-Fabregas J, Delgado-Mederos R, Granell E, Morenas Rodriguez E, Marin Lahoz J, Dinia L, Carrera D, Perez de la Ossa N, Sanahuja J, Sobrino T, De Arce AM, Alonso de Lecinana M (2013) Microbleed burden and hematoma expansion in acute intracerebral hemorrhage. Eur Neurol 70:175–178PubMed Marti-Fabregas J, Delgado-Mederos R, Granell E, Morenas Rodriguez E, Marin Lahoz J, Dinia L, Carrera D, Perez de la Ossa N, Sanahuja J, Sobrino T, De Arce AM, Alonso de Lecinana M (2013) Microbleed burden and hematoma expansion in acute intracerebral hemorrhage. Eur Neurol 70:175–178PubMed
113.
go back to reference Tsivgoulis G, Zand R, Katsanos AH, Turc G, Nolte CH, Jung S, Cordonnier C, Fiebach JB, Scheitz JF, Klinger-Gratz PP, Oppenheim C, Goyal N, Safouris A, Mattle HP, Alexandrov AW, Schellinger PD, Alexandrov AV (2016) Risk of symptomatic intracerebral hemorrhage after intravenous thrombolysis in patients with acute ischemic stroke and high cerebral microbleed burden: a meta-analysis. JAMA Neurol 73:675–683PubMed Tsivgoulis G, Zand R, Katsanos AH, Turc G, Nolte CH, Jung S, Cordonnier C, Fiebach JB, Scheitz JF, Klinger-Gratz PP, Oppenheim C, Goyal N, Safouris A, Mattle HP, Alexandrov AW, Schellinger PD, Alexandrov AV (2016) Risk of symptomatic intracerebral hemorrhage after intravenous thrombolysis in patients with acute ischemic stroke and high cerebral microbleed burden: a meta-analysis. JAMA Neurol 73:675–683PubMed
114.
go back to reference Charidimou A, Imaizumi T, Moulin S, Biffi A, Samarasekera N, Yakushiji Y, Peeters A, Vandermeeren Y, Laloux P, Baron JC, Hernandez-Guillamon M, Montaner J, Casolla B, Gregoire SM, Kang DW, Kim JS, Naka H, Smith EE, Viswanathan A, Jager HR, Al-Shahi Salman R, Greenberg SM, Cordonnier C, Werring DJ (2017) Brain hemorrhage recurrence, small vessel disease type, and cerebral microbleeds: a meta-analysis. Neurology 89:820–829PubMedPubMedCentral Charidimou A, Imaizumi T, Moulin S, Biffi A, Samarasekera N, Yakushiji Y, Peeters A, Vandermeeren Y, Laloux P, Baron JC, Hernandez-Guillamon M, Montaner J, Casolla B, Gregoire SM, Kang DW, Kim JS, Naka H, Smith EE, Viswanathan A, Jager HR, Al-Shahi Salman R, Greenberg SM, Cordonnier C, Werring DJ (2017) Brain hemorrhage recurrence, small vessel disease type, and cerebral microbleeds: a meta-analysis. Neurology 89:820–829PubMedPubMedCentral
115.
go back to reference Lau KK, Lovelock CE, Li L, Simoni M, Gutnikov S, Kuker W, Mak HKF, Rothwell PM (2018) Antiplatelet treatment after transient ischemic attack and ischemic stroke in patients with cerebral microbleeds in 2 large cohorts and an updated systematic review. Stroke 6:1434–1442 Lau KK, Lovelock CE, Li L, Simoni M, Gutnikov S, Kuker W, Mak HKF, Rothwell PM (2018) Antiplatelet treatment after transient ischemic attack and ischemic stroke in patients with cerebral microbleeds in 2 large cohorts and an updated systematic review. Stroke 6:1434–1442
116.
go back to reference Wilson D, Charidimou A, Ambler G, Fox ZV, Gregoire S, Rayson P, Imaizumi T, Fluri F, Naka H, Horstmann S, Veltkamp R, Rothwell PM, Kwa VI, Thijs V, Lee YS, Kim YD, Huang Y, Wong KS, Jager HR, Werring DJ (2016) Recurrent stroke risk and cerebral microbleed burden in ischemic stroke and TIA: a meta-analysis. Neurology 87:1501–1510PubMedPubMedCentral Wilson D, Charidimou A, Ambler G, Fox ZV, Gregoire S, Rayson P, Imaizumi T, Fluri F, Naka H, Horstmann S, Veltkamp R, Rothwell PM, Kwa VI, Thijs V, Lee YS, Kim YD, Huang Y, Wong KS, Jager HR, Werring DJ (2016) Recurrent stroke risk and cerebral microbleed burden in ischemic stroke and TIA: a meta-analysis. Neurology 87:1501–1510PubMedPubMedCentral
118.
go back to reference Charidimou A, Boulouis G, Shams S, Calvet D, Shoamanesh A (2017) Intracerebral haemorrhage risk in microbleed-positive ischaemic stroke patients with atrial fibrillation: preliminary meta-analysis of cohorts and anticoagulation decision schema. J Neurol Sci 378:102–109PubMed Charidimou A, Boulouis G, Shams S, Calvet D, Shoamanesh A (2017) Intracerebral haemorrhage risk in microbleed-positive ischaemic stroke patients with atrial fibrillation: preliminary meta-analysis of cohorts and anticoagulation decision schema. J Neurol Sci 378:102–109PubMed
119.
go back to reference Wilson D, Ambler G, Shakeshaft C, Brown MM, Charidimou A, Al-Shahi Salman R, Lip GYH, Cohen H, Banerjee G, Houlden H, White MJ, Yousry TA, Harkness K, Flossmann E, Smyth N, Shaw LJ, Warburton E, Muir KW, Jager HR, Werring DJ (2018) 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 17:539–547PubMedPubMedCentral Wilson D, Ambler G, Shakeshaft C, Brown MM, Charidimou A, Al-Shahi Salman R, Lip GYH, Cohen H, Banerjee G, Houlden H, White MJ, Yousry TA, Harkness K, Flossmann E, Smyth N, Shaw LJ, Warburton E, Muir KW, Jager HR, Werring DJ (2018) 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 17:539–547PubMedPubMedCentral
120.
go back to reference Romero JR, Preis SR, Beiser A, Himali JJ, Shoamanesh A, Wolf PA, Kase CS, Vasan RS, DeCarli C, Seshadri S (2017) Cerebral microbleeds as predictors of mortality: the Framingham Heart Study. Stroke 48:781–783PubMedPubMedCentral Romero JR, Preis SR, Beiser A, Himali JJ, Shoamanesh A, Wolf PA, Kase CS, Vasan RS, DeCarli C, Seshadri S (2017) Cerebral microbleeds as predictors of mortality: the Framingham Heart Study. Stroke 48:781–783PubMedPubMedCentral
121.
go back to reference Romero JR, Beiser A, Himali JJ, Shoamanesh A, DeCarli C, Seshadri S (2017) Cerebral microbleeds and risk of incident dementia: the Framingham Heart Study. Neurobiol Aging 54:94–99PubMedPubMedCentral Romero JR, Beiser A, Himali JJ, Shoamanesh A, DeCarli C, Seshadri S (2017) Cerebral microbleeds and risk of incident dementia: the Framingham Heart Study. Neurobiol Aging 54:94–99PubMedPubMedCentral
122.
go back to reference Xu X, Chan QL, Hilal S, Goh WK, Ikram MK, Wong TY, Cheng CY, Chen CL, Venketasubramanian N (2017) Cerebral microbleeds and neuropsychiatric symptoms in an elderly Asian cohort. J Neurol Neurosurg Psychiatry 88:7–11PubMed Xu X, Chan QL, Hilal S, Goh WK, Ikram MK, Wong TY, Cheng CY, Chen CL, Venketasubramanian N (2017) Cerebral microbleeds and neuropsychiatric symptoms in an elderly Asian cohort. J Neurol Neurosurg Psychiatry 88:7–11PubMed
123.
go back to reference van Norden AG, van Uden IW, de Laat KF, Gons RA, Kessels RP, van Dijk EJ, de Leeuw FE (2013) Cerebral microbleeds are related to subjective cognitive failures: the RUN DMC study. Neurobiol Aging 34:2225–2230PubMed van Norden AG, van Uden IW, de Laat KF, Gons RA, Kessels RP, van Dijk EJ, de Leeuw FE (2013) Cerebral microbleeds are related to subjective cognitive failures: the RUN DMC study. Neurobiol Aging 34:2225–2230PubMed
124.
go back to reference Banerjee G, Jang H, Kim HJ, Kim ST, Kim JS, Lee JH, Im K, Kwon H, Lee JM, Na DL, Seo SW, Werring DJ (2018) Total MRI small vessel disease burden correlates with cognitive performance, cortical atrophy, and network measures in a memory clinic population. J Alzheimers Dis 63:1485–1497PubMed Banerjee G, Jang H, Kim HJ, Kim ST, Kim JS, Lee JH, Im K, Kwon H, Lee JM, Na DL, Seo SW, Werring DJ (2018) Total MRI small vessel disease burden correlates with cognitive performance, cortical atrophy, and network measures in a memory clinic population. J Alzheimers Dis 63:1485–1497PubMed
125.
go back to reference Cummings JL (1993) Frontal-subcortical circuits and human behavior. Arch Neurol 50:873–880PubMed Cummings JL (1993) Frontal-subcortical circuits and human behavior. Arch Neurol 50:873–880PubMed
126.
go back to reference De Groot JC, De Leeuw FE, Oudkerk M, Van Gijn J, Hofman A, Jolles J, Breteler MM (2002) Periventricular cerebral white matter lesions predict rate of cognitive decline. Ann Neurol 52:335–341PubMed De Groot JC, De Leeuw FE, Oudkerk M, Van Gijn J, Hofman A, Jolles J, Breteler MM (2002) Periventricular cerebral white matter lesions predict rate of cognitive decline. Ann Neurol 52:335–341PubMed
127.
go back to reference Filley CM (1998) The behavioral neurology of cerebral white matter. Neurology 50:1535–1540PubMed Filley CM (1998) The behavioral neurology of cerebral white matter. Neurology 50:1535–1540PubMed
128.
129.
go back to reference Tuladhar AM, Lawrence A, Norris DG, Barrick TR, Markus HS, de Leeuw FE (2017) Disruption of rich club organisation in cerebral small vessel disease. Hum Brain Mapp 38:1751–1766PubMed Tuladhar AM, Lawrence A, Norris DG, Barrick TR, Markus HS, de Leeuw FE (2017) Disruption of rich club organisation in cerebral small vessel disease. Hum Brain Mapp 38:1751–1766PubMed
130.
go back to reference Lawrence AJ, Zeestraten EA, Benjamin P, Lambert CP, Morris RG, Barrick TR, Markus HS (2018) Longitudinal decline in structural networks predicts dementia in cerebral small vessel disease. Neurology 90:e1898–e1910PubMedPubMedCentral Lawrence AJ, Zeestraten EA, Benjamin P, Lambert CP, Morris RG, Barrick TR, Markus HS (2018) Longitudinal decline in structural networks predicts dementia in cerebral small vessel disease. Neurology 90:e1898–e1910PubMedPubMedCentral
131.
go back to reference Loos CMJ, Makin SDJ, Staals J, Dennis MS, van Oostenbrugge RJ, Wardlaw JM (2018) Long-term morphological changes of symptomatic lacunar infarcts and surrounding white matter on structural magnetic resonance imaging. Stroke 49:1183–1188PubMedPubMedCentral Loos CMJ, Makin SDJ, Staals J, Dennis MS, van Oostenbrugge RJ, Wardlaw JM (2018) Long-term morphological changes of symptomatic lacunar infarcts and surrounding white matter on structural magnetic resonance imaging. Stroke 49:1183–1188PubMedPubMedCentral
132.
go back to reference Hatate J, Miwa K, Matsumoto M, Sasaki T, Yagita Y, Sakaguchi M, Kitagawa K, Mochizuki H (2016) Association between cerebral small vessel diseases and mild parkinsonian signs in the elderly with vascular risk factors. Parkinson Relat Disord 26:29–34 Hatate J, Miwa K, Matsumoto M, Sasaki T, Yagita Y, Sakaguchi M, Kitagawa K, Mochizuki H (2016) Association between cerebral small vessel diseases and mild parkinsonian signs in the elderly with vascular risk factors. Parkinson Relat Disord 26:29–34
133.
go back to reference van der Holst HM, van Uden IW, Tuladhar AM, de Laat KF, van Norden AG, Norris DG, van Dijk EJ, Esselink RA, Platel B, de Leeuw FE (2015) Cerebral small vessel disease and incident parkinsonism: the RUN DMC study. Neurology 85:1569–1577PubMedPubMedCentral van der Holst HM, van Uden IW, Tuladhar AM, de Laat KF, van Norden AG, Norris DG, van Dijk EJ, Esselink RA, Platel B, de Leeuw FE (2015) Cerebral small vessel disease and incident parkinsonism: the RUN DMC study. Neurology 85:1569–1577PubMedPubMedCentral
134.
go back to reference de Laat KF, Tuladhar AM, van Norden AG, Norris DG, Zwiers MP, de Leeuw FE (2011) Loss of white matter integrity is associated with gait disorders in cerebral small vessel disease. Brain 134:73–83PubMed de Laat KF, Tuladhar AM, van Norden AG, Norris DG, Zwiers MP, de Leeuw FE (2011) Loss of white matter integrity is associated with gait disorders in cerebral small vessel disease. Brain 134:73–83PubMed
135.
go back to reference van der Holst HM, Tuladhar AM, Zerbi V, van Uden IWM, de Laat KF, van Leijsen EMC, Ghafoorian M, Platel B, Bergkamp MI, van Norden AGW, Norris DG, van Dijk EJ, Kiliaan AJ, de Leeuw FE (2018) White matter changes and gait decline in cerebral small vessel disease. Neuroimage Clin 17:731–738PubMed van der Holst HM, Tuladhar AM, Zerbi V, van Uden IWM, de Laat KF, van Leijsen EMC, Ghafoorian M, Platel B, Bergkamp MI, van Norden AGW, Norris DG, van Dijk EJ, Kiliaan AJ, de Leeuw FE (2018) White matter changes and gait decline in cerebral small vessel disease. Neuroimage Clin 17:731–738PubMed
136.
go back to reference Kim YJ, Kwon HK, Lee JM, Cho H, Kim HJ, Park HK, Jung NY, San Lee J, Lee J, Jang YK, Kim ST, Lee KH, Choe YS, Kim YJ, Na DL, Seo SW (2016) Gray and white matter changes linking cerebral small vessel disease to gait disturbances. Neurology 86:1199–1207PubMed Kim YJ, Kwon HK, Lee JM, Cho H, Kim HJ, Park HK, Jung NY, San Lee J, Lee J, Jang YK, Kim ST, Lee KH, Choe YS, Kim YJ, Na DL, Seo SW (2016) Gray and white matter changes linking cerebral small vessel disease to gait disturbances. Neurology 86:1199–1207PubMed
137.
go back to reference Zijlmans JC, Daniel SE, Hughes AJ, Revesz T, Lees AJ (2004) Clinicopathological investigation of vascular parkinsonism, including clinical criteria for diagnosis. Mov Disord 19:630–640PubMed Zijlmans JC, Daniel SE, Hughes AJ, Revesz T, Lees AJ (2004) Clinicopathological investigation of vascular parkinsonism, including clinical criteria for diagnosis. Mov Disord 19:630–640PubMed
138.
go back to reference Rensma SP, van Sloten TT, Launer LJ, Stehouwer CDA (2018) Cerebral small vessel disease and risk of incident stroke, dementia and depression, and all-cause mortality: a systematic review and meta-analysis. Neurosci Biobehav Rev 90:164–173PubMedPubMedCentral Rensma SP, van Sloten TT, Launer LJ, Stehouwer CDA (2018) Cerebral small vessel disease and risk of incident stroke, dementia and depression, and all-cause mortality: a systematic review and meta-analysis. Neurosci Biobehav Rev 90:164–173PubMedPubMedCentral
139.
go back to reference Brookes RL, Herbert V, Lawrence AJ, Morris RG, Markus HS (2014) Depression in small-vessel disease relates to white matter ultrastructural damage, not disability. Neurology 83:1417–1423PubMedPubMedCentral Brookes RL, Herbert V, Lawrence AJ, Morris RG, Markus HS (2014) Depression in small-vessel disease relates to white matter ultrastructural damage, not disability. Neurology 83:1417–1423PubMedPubMedCentral
140.
go back to reference Taylor WD, Aizenstein HJ, Alexopoulos GS (2013) The vascular depression hypothesis: mechanisms linking vascular disease with depression. Mol Psychiatry 18:963–974PubMedPubMedCentral Taylor WD, Aizenstein HJ, Alexopoulos GS (2013) The vascular depression hypothesis: mechanisms linking vascular disease with depression. Mol Psychiatry 18:963–974PubMedPubMedCentral
141.
go back to reference Hollocks MJ, Lawrence AJ, Brookes RL, Barrick TR, Morris RG, Husain M, Markus HS (2015) Differential relationships between apathy and depression with white matter microstructural changes and functional outcomes. Brain 138:3803–3815PubMed Hollocks MJ, Lawrence AJ, Brookes RL, Barrick TR, Morris RG, Husain M, Markus HS (2015) Differential relationships between apathy and depression with white matter microstructural changes and functional outcomes. Brain 138:3803–3815PubMed
Metadata
Title
Cerebral small vessel disease: neuroimaging markers and clinical implication
Authors
Xiaodong Chen
Jihui Wang
Yilong Shan
Wei Cai
Sanxin Liu
Mengyan Hu
Siyuan Liao
Xuehong Huang
Bingjun Zhang
Yuge Wang
Zhengqi Lu
Publication date
01-10-2019
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 10/2019
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-018-9077-3

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