The concept of sporadic cerebral small vessel disease: A road map on key definitions and current concepts

International Journal of Stroke

Volumn 11, Issue 1, 2016, Pages 6-18

  Charidimou, Andreas ^a,b   Pantoni, Leonardo ^c   Love, Seth ^d  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b NATIONAL HOSPITAL FOR NEUROLOGY AND NEUROSURGERY   (United Kingdom)

^c CAREGGI UNIVERSITY HOSPITAL   (Italy)

^d SOUTHMEAD HOSPITAL   (United Kingdom)

Author keywords

antithrombotics; cerebral amyloid angiopathy; Cerebral microbleeds; cerebral small vessel disease; intracerebral hemorrhage; leukoaraiosis

Indexed keywords

AMYLOID BETA PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN;

ARTICLE; BLOOD VESSEL DIAMETER; BRAIN ATROPHY; BRAIN HEMORRHAGE; BRAIN INFARCTION; CEREBROVASCULAR DISEASE; CLINICAL FEATURE; CORTICAL SUPERFICIAL SIDEROSIS; DISEASE ASSOCIATION; DISEASE MARKER; HISTOPATHOLOGY; HUMAN; HYPERTENSIVE ARTERIOPATHY; IMAGE ANALYSIS; MEDICAL RESEARCH; MOLECULAR IMAGING; NEUROIMAGING; NEUROPATHOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PERIVASCULAR SPACE; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RADIATION AND RADIATION RELATED PHENOMENA; SIDEROSIS; SMALL SUBCORTICAL INFARCT; SPORADIC CEREBRAL SMALL VESSEL DISEASE; STANDARDIZATION; VASCULAR AMYLOIDOSIS; WHITE MATTER HYPERINTENSITY; BRAIN; CEREBRAL SMALL VESSEL DISEASES; PATHOLOGY; PROCEDURES; STANDARDS;

BRAIN; CEREBRAL SMALL VESSEL DISEASES; HUMANS; NEUROIMAGING;

EID: 84953384244     PISSN: 17474930     EISSN: 17474949     Source Type: Journal    
DOI: 10.1177/1747493015607485     Document Type: Article

References (78)

1. Greenberg SM. Small vessels, big problems. N Engl J Med 2006; 354: 1451-1453.
2. Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 2010; 9: 689-701.
3. Wardlaw JM, Smith C, Dichgans M. Mechanisms of sporadic cerebral small vessel disease: insights from neuroimaging. Lancet Neurol 2013; 12: 483-497.
4. Thompson CS, Hakim AM. Living beyond our physiological means: small vessel disease of the brain is an expression of a systemic failure in arteriolar function: a unifying hypothesis. Stroke 2009; 40: e322-e330.
5. Debette S, Markus HS. The clinical importance of white matter hyperintensities on brain magnetic resonance imaging: systematic review and meta-analysis. BMJ 2010; 341: c3666.
6. Altmann-Schneider I, Trompet S, de Craen AJ. Cerebral microbleeds are predictive of mortality in the elderly. Stroke 2011; 42: 638-644.
7. Charidimou A, Gang Q, Werring DJ. Sporadic cerebral amyloid angiopathy revisited: recent insights into pathophysiology and clinical spectrum. J Neurol Neurosurg Psychiatry 2012; 83: 124-137.
8. Reijmer YD, van Veluw SJ, Greenberg SM. Ischemic brain injury in cerebral amyloid angiopathy. J Cerebr Blood Flow Metab 2015. Epub, doi: 10.1038/jcbfm.2015.88.
9. Norrving B. Evolving concept of small vessel disease through advanced brain imaging. J Stroke 2015; 17: 94-100.
10. Wardlaw JM, Smith EE, Biessels GJ. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol 2013; 12: 822-838.
11. Smith EE, Schneider JA, Wardlaw JM, Greenberg SM. Cerebral microinfarcts: the invisible lesions. Lancet Neurol 2012; 11: 272-282.
12. Charidimou A, Linn J, Vernooij MW. Cortical superficial siderosis: detection and clinical significance in cerebral amyloid angiopathy and related conditions. Brain 2015; 138: 2126-2139.
13. Greenberg SM, Vernooij MW, Cordonnier C. Cerebral microbleeds: a guide to detection and interpretation. Lancet Neurol 2009; 8: 165-174.
14. Pantoni L, Sarti C, Alafuzoff I. Postmortem examination of vascular lesions in cognitive impairment: a survey among neuropathological services. Stroke 2006; 37: 1005-1009.
15. Alafuzoff I, Gelpi E, Al-Sarraj S. The need to unify neuropathological assessments of vascular alterations in the ageing brain: multicentre survey by the BrainNet Europe consortium. Exp Gerontol 2012; 47: 825-833.
16. Salamon N. Neuroimaging of cerebral small vessel disease. Brain Pathol 2014; 24: 519-524.
17. Challa VR, Bell MA, Moody DM. A combined hematoxylin-eosin, alkaline phosphatase and high-resolution microradiographic study of lacunes. Clin Neuropathol 1990; 9: 196-204.
18. Blinder P, Tsai PS, Kaufhold JP, Knutsen PM, Suhl H, Kleinfeld D. The cortical angiome: an interconnected vascular network with noncolumnar patterns of blood flow. Nat Neurosci 2013; 16: 889-897.
19. Scuteri A, Nilsson PM, Tzourio C, Redon J, Laurent S. Microvascular brain damage with aging and hypertension: pathophysiological consideration and clinical implications. J Hypertens 2011; 29: 1469-1477.
20. Fisher CM. Lacunar strokes and infarcts: a review. Neurology 1982; 32: 871-876.
21. Gorelick PB, Scuteri A, Black SE. Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the American heart association/American stroke association. Stroke 2011; 42: 2672-2713.
22. The Lancet N. A united approach to vascular disease and neurodegeneration. Lancet Neurol 2012; 11: 293.
23. Launer LJ, Hofman A. Frequency and impact of neurologic diseases in the elderly of Europe: a collaborative study of population-based cohorts. Neurology 2000; 54: S1-S8.
24. Gouw AA, Seewann A, van der Flier WM. Heterogeneity of small vessel disease: a systematic review of MRI and histopathology correlations. J Neurol Neurosurg Psychiatry 2011; 82: 126-135.
25. van Swieten JC, Staal S, Kappelle LJ, Derix MM, van Gijn J. Are white matter lesions directly associated with cognitive impairment in patients with lacunar infarcts? J Neurol 1996; 243: 196-200.
26. Schmidt R, Grazer A, Enzinger C. MRI-detected white matter lesions: do they really matter? J Neural Transm 2011; 118: 673-681.
27. Charidimou A, Werring DJ. Cerebral microbleeds: detection, mechanisms and clinical challenges. Future Neurol 2011; 6: 587-611.
28. Smith EE, Schneider JA, Wardlaw JM, Greenberg SM. Cerebral microinfarcts: the invisible lesions. Lancet Neurol 2012; 11: 272-282.
29. Doubal FN, MacLullich AM, Ferguson KJ, Dennis MS, Wardlaw JM. Enlarged perivascular spaces on MRI are a feature of cerebral small vessel disease. Stroke 2010; 41: 450-454.
30. Duering M, Righart R, Csanadi E. Incident subcortical infarcts induce focal thinning in connected cortical regions. Neurology 2012; 79: 2025-2028.
31. van Veluw SJ, Zwanenburg JJ, Rozemuller AJ, Luijten PR, Spliet WG, Biessels GJ. The spectrum of MR detectable cortical microinfarcts: a classification study with 7-tesla postmortem MRI and histopathology. J Cerebr Blood Flow Metab 2015; 35: 676-683.
32. Muller M, Appelman AP, van der Graaf Y, Vincken KL, Mali WP, Geerlings MI. Brain atrophy and cognition: interaction with cerebrovascular pathology? Neurobiol Aging 2011; 32: 885-893.
33. Appelman AP, Exalto LG, van der Graaf Y, Biessels GJ, Mali WP, Geerlings MI. White matter lesions and brain atrophy: more than shared risk factors? A systematic review. Cerebrovasc Dis 2009; 28: 227-242.
34. Love S, Miners S, Palmer J, Chalmers K, Kehoe P. Insights into the pathogenesis and pathogenicity of cerebral amyloid angiopathy. Front Biosci (Landmark Ed) 2009; 14: 4778-4792.
35. Vinters HV. Cerebral amyloid angiopathy. A critical review. Stroke 1987; 18: 311-324.
36. Vinters HV, Gilbert JJ. Cerebral amyloid angiopathy: incidence and complications in the aging brain. II. The distribution of amyloid vascular changes. Stroke 1983; 14: 924-928.
37. Attems J, Jellinger K, Thal DR, Van Nostrand W. Review: sporadic cerebral amyloid angiopathy. Neuropathol Appl Neurobiol 2011; 37: 75-93.
38. Fisher M. MRI screening for chronic anticoagulation in atrial fibrillation. Front Neurol 2013; 4: 137.
39. Wang Z, Soo YO, Mok VC. Cerebral microbleeds: is antithrombotic therapy safe to administer? Stroke 2014; 45: 2811-2817.
40. Knudsen KA, Rosand J, Karluk D, Greenberg SM. Clinical diagnosis of cerebral amyloid angiopathy: validation of the Boston criteria. Neurology 2001; 56: 537-539.
41. Linn J, Halpin A, Demaerel P. Prevalence of superficial siderosis in patients with cerebral amyloid angiopathy. Neurology 2010; 74: 1346-1350.
42. Pantoni L, Garcia JH. The significance of cerebral white matter abnormalities 100 years after Binswanger's report. A review. Stroke 1995; 26: 1293-1301.
43. Lammie GA. Hypertensive cerebral small vessel disease and stroke. Brain Pathol 2002; 12: 358-370.
44. Lammie GA, Brannan F, Slattery J, Warlow C. Nonhypertensive cerebral small-vessel disease. An autopsy study. Stroke 1997; 28: 2222-2229.
45. Cole FM, Yates P. Intracerebral microaneurysms and small cerebrovascular lesions. Brain 1967; 90: 759-768.
46. Feigin I, Prose P. Hypertensive fibrinoid arteritis of the brain and gross cerebral hemorrhage: a form of "hyalinosis". Arch Neurol 1959; 1: 98-110.
47. Rosenblum WI. Cerebral hemorrhage produced by ruptured dissecting aneurysm in miliary aneurysm. Ann Neurol 2003; 54: 376-378.
48. Fisher CM. Pathological observations in hypertensive cerebral hemorrhage. J Neuropathol Exp Neurol 1971; 30: 536-550.
49. Takebayashi S, Kaneko M. Electron microscopic studies of ruptured arteries in hypertensive intracerebral hemorrhage. Stroke 1983; 14: 28-36.
50. Rosenblum WI. Fibrinoid necrosis of small brain arteries and arterioles and miliary aneurysms as causes of hypertensive hemorrhage: a critical reappraisal. Acta Neuropathol 2008; 116: 361-369.
51. Werring DJ (ed.) Cerebral Microbleeds: Pathophysiology to Clinical Practice. Cambridge, England: Cambridge University Press, 2011, pp.49-64.
52. Charidimou A. Applied Clinical Neuroimaging in Cerebral Amyloid Angiopathy and Spontaneous Intracerebral Haemorrhage. Thesis. London, UK: University College London (UCL), 2015.
53. Hawkes CA, Hartig W, Kacza J. Perivascular drainage of solutes is impaired in the ageing mouse brain and in the presence of cerebral amyloid angiopathy. Acta Neuropathol 2011; 121: 431-443.
54. Fazekas F, Kleinert R, Offenbacher H. Pathologic correlates of incidental MRI white matter signal hyperintensities. Neurology 1993; 43: 1683-1689.
55. Braffman BH, Zimmerman RA, Trojanowski JQ, Gonatas NK, Hickey WF, Schlaepfer WW. Brain MR: pathologic correlation with gross and histopathology. 1. Lacunar infarction and Virchow-Robin spaces. Am J Roentgenol 1988; 151: 551-558.
56. van Swieten JC, van den Hout JH, van Ketel BA, Hijdra A, Wokke JH, van Gijn J. Periventricular lesions in the white matter on magnetic resonance imaging in the elderly. A morphometric correlation with arteriolosclerosis and dilated perivascular spaces. Brain 1991; 114: 761-774.
57. Fisher CM. The arterial lesions underlying lacunes. Acta Neuropathol 1968; 12: 1-15.
58. Fisher CM. Hypertensive cerebral hemorrhage. Demonstration of the source of bleeding. J Neuropathol Exp Neurol 2003; 62: 104-107.
59. Bokura H, Kobayashi S, Yamaguchi S. Distinguishing silent lacunar infarction from enlarged Virchow-Robin spaces: a magnetic resonance imaging and pathological study. J Neurol 1998; 245: 116-122.
60. Cumurciuc R, Guichard JP, Reizine D, Gray F, Bousser MG, Chabriat H. Dilation of Virchow-Robin spaces in CADASIL. Eur J Neurol 2006; 13: 187-190.
61. Shoamanesh A, Kwok CS, Benavente O. Cerebral microbleeds: histopathological correlation of neuroimaging. Cerebrovasc Dis 2011; 32: 528-534.
62. Staals J, Makin SD, Doubal FN, Dennis MS, Wardlaw JM. Stroke subtype, vascular risk factors, and total MRI brain small-vessel disease burden. Neurology 2014; 83: 1228-1234.
63. Klarenbeek P, van Oostenbrugge RJ, Rouhl RP, Knottnerus IL, Staals J. Ambulatory blood pressure in patients with lacunar stroke: association with total MRI burden of cerebral small vessel disease. Stroke 2013; 44: 2995-2999.
64. Huijts M, Duits A, van Oostenbrugge RJ, Kroon AA, de Leeuw PW, Staals J. Accumulation of MRI markers of cerebral small vessel disease is associated with decreased cognitive function. A study in first-ever lacunar stroke and hypertensive patients. Front Aging Neurosci 2013; 5: 72.
65. Jickling GC, Chen C. Rating total cerebral small-vessel disease: does it add up? Neurology 2014; 83: 1224-1225.
66. Deramecourt V, Slade JY, Oakley AE. Staging and natural history of cerebrovascular pathology in dementia. Neurology 2012; 78: 1043-1050.
67. Smallwood A, Oulhaj A, Joachim C. Cerebral subcortical small vessel disease and its relation to cognition in elderly subjects: a pathological study in the Oxford Project to Investigate Memory and Ageing (OPTIMA) cohort. Neuropathol Appl Neurobiol 2012; 38: 337-343.
68. Love S, Chalmers K, Ince P. Development, appraisal, validation and implementation of a consensus protocol for the assessment of cerebral amyloid angiopathy in post-mortem brain tissue. Am J Neurodegener Dis 2014; 3: 19-32.
69. Barker R, Ashby EL, Wellington D. Pathophysiology of white matter perfusion in Alzheimer's disease and vascular dementia. Brain 2014; 137: 1524-1532.
70. Barker R, Wellington D, Esiri MM, Love S. Assessing white matter ischemic damage in dementia patients by measurement of myelin proteins. J Cereb Blood Flow Metab 2013; 33: 1050-1057.
71. Love S, Miners JS. White matter hypoperfusion and damage in dementia: post-mortem assessment. Brain Pathol 2015; 25: 99-107.
72. Miners S, Moulding H, de Silva R, Love S. Reduced vascular endothelial growth factor and capillary density in the occipital cortex in dementia with Lewy bodies. Brain Pathol 2014; 24: 334-343.
73. Thomas T, Miners S, Love S. Post-mortem assessment of hypoperfusion of cerebral cortex in Alzheimer's disease and vascular dementia. Brain 2015; 138: 1059-1069.
74. Ly JV, Donnan GA, Villemagne VL. 11C-PIB binding is increased in patients with cerebral amyloid angiopathy-related hemorrhage. Neurology 2010; 74: 487-493.
75. Dierksen GA, Skehan ME, Khan MA. Spatial relation between microbleeds and amyloid deposits in amyloid angiopathy. Ann Neurol 2010; 68: 545-548.
76. Greenberg SM, Grabowski T, Gurol ME. Detection of isolated cerebrovascular beta-amyloid with Pittsburgh compound B. Ann Neurol 2008; 64: 587-591.
77. Charidimou A, Jager HR. Developing biomarkers for cerebral amyloid angiopathy trials: do potential disease phenotypes hold promise? Lancet Neurol 2014; 13: 538-540.
78. Investigators SPS, Benavente OR, Hart RG. Effects of clopidogrel added to aspirin in patients with recent lacunar stroke. N Engl J Med 2012; 367: 817-825.