Pathologic aspects of the hemorrhagic consequences of small vessel disease on the brain

Cerebral Small Vessel Disease

Volumn , Issue , 2011, Pages 29-41

  Attems, Johannes ^a   Jellinger, Kurt A ^b  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b University Clinic of Neurology   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84923347529     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1017/CBO9781139382694.005     Document Type: Chapter

References (117)

1. Smallwood A, Oulhaj A, Joachim C, et al. 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.
2. Tanskanen M, Makela M, Myllykangas L, et al. Intracerebral hemorrhage in the oldest old: a population-based study (Vantaa 85+). Front Neurol 2012; 3:103.
3. Seo SW, Hwa Lee B, et al. Clinical significance of microbleeds in subcortical vascular dementia. Stroke 2007; 38:1949-1951.
4. Esiri MM, Joachim C, Sloan C, et al. Cerebral subcortical small vessel disease in subjects with pathologically confirmed Alzheimer’s disease: a clinicopathological study in the Oxford Project to Investigate Memory and Ageing (OPTIMA). Alzheimer Dis ASSOC Disord 2013, Jul 8 [Epub ahead of print].
5. Zekry D, Duyckaerts C, Belmin J, et al. Cerebral amyloid angiopathy in the elderly: vessel wall changes and relationship with dementia. Acta Neuropathol 2003; 106: 367-373.
6. Ferrer I, Kaste M, Kalimo H. Vascular diseases. In Love S, Louis DN, Ellison DW, eds. Greenfield’s Neuropathology, 8th edn. London: Hodder Arnold; 2008: pp. 121-240.
7. Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 2010; 9:689-701.
8. Rosand J, Muzikansky A, Kumar A, et al. Spatial clustering of hemorrhages in probable cerebral amyloid angiopathy. Ann Neurol 2005; 58:459-462.
9. Vinters HV. Cerebral amyloid angiopathy. A critical review. Stroke 1987; 18:311-324.
10. Attems J, Jellinger K, Thal DR, Van Nostrand W. Review: sporadic cerebral amyloid angiopathy. Neuropathol Appl Neurobiol 2011; 37:75-93.
11. Vonsattel JP, Myers RH, Hedley-Whyte ET, et al. Cerebral amyloid angiopathy without and with cerebral hemorrhages: a comparative histological study. Ann Neurol 1991; 30:637-649.
12. Neuropathology Group. Medical Research Council Cognitive Function and Aging Study. Pathological correlates of late- onset dementia in a multicentre, community-based population in England and Wales. Lancet 2001; 357:169-175.
13. Attems J, Lauda F, Jellinger KA. Unexpectedly low prevalence of intracerebral hemorrhages in sporadic cerebral amyloid angiopathy: an autopsy study. J Neurol 2008; 255:70-76.
14. Biffi A, Sonni A, Anderson CD, et al. Variants at ApoE influence risk of deep and lobar intracerebral hemorrhage. Ann Neurol 2010; 68:934-943.
15. McCarron MO, Nicoll JA. High frequency of apolipoprotein E £2 allele is specific for patients with cerebral amyloid angiopathy- related haemorrhage. Neurosci Lett 1998; 247:45-48.
16. Olichney JM, Hansen LA, Hofstetter CR, et al. Association between severe cerebral amyloid angiopathy and cerebrovascular lesions in Alzheimer disease is not a spurious one attributable to apolipoprotein E £4. Arch Neurol 2000; 57:869-874.
17. Jellinger KA, Lauda F, Attems J. Sporadic cerebral amyloid angiopathy- no frequent cause of spontaneous brain haemorrhage. Neuropathol App Neurobiol 2008; 34: S1-14.
18. Jellinger KA, Lauda F, Attems J. Sporadic cerebral amyloid angiopathy is not a frequent causeof spontaneous brain hemorrhage. Eur J Neurol 2007; 14:923-928.
19. Chen YW, Gurol ME, Rosand J, et al. Progression of white matter lesions and hemorrhages in cerebral amyloid angiopathy. Neurology 2006; 67:83-87.
20. Smith EE, Schneider JA, Wardlaw J., Greenberg SM. Cerebral microinfarcts: the invisible lesions. Lancet Neurol 2012; 11:272-282.
21. Gregoire SM, Charidimou A, Gadapa N, et al. Acute ischaemic brain lesions in intracerebral haemorrhage: multicentre crosssectional magnetic resonance imaging study. Brain 2011; 134:2376-2386.
22. Arima H, Tzourio C, Anderson C, et al. Effects of perindopril-based lowering of blood pressure on intracerebral hemorrhage related to amyloid angiopathy: the PROGRESS trial. Stroke 2010; 41:394-396.
23. Revesz T, Holton JL, Lashley T, et al. Genetics and molecular pathogenesis of sporadic and hereditary cerebral amyloid angiopathies. Acta Neuropathol 2009; 118:115-130.
24. Verghese PB, Castellano JM, Holtzman DM. Apolipoprotein E in Alzheimer’s disease and other neurological disorders. Lancet Neurol 2011; 10:241-252.
25. Greenberg SM, Rebeck GW, Vonsattel JP, Gomez-Isla T, Hyman BT. Apolipoprotein E £4 and cerebral hemorrhage associated with amyloid angiopathy. Ann Neurol 1995; 38:254-259.
26. Greenberg SM, Vonsattel JP, Segal AZ, et al. Association of apolipoprotein E £2 and vasculopathy in cerebral amyloid angiopathy. Neurology 1998; 50:961-965.
27. McCarron MO, Nicoll JA, Stewart J, et al. The apolipoprotein E £2 allele and the pathological featuresin cerebral amyloid angiopathy- related hemorrhage. J Neuropathol Exp Neurol 1999; 58:711-718.
28. Nicoll JA, Burnett C, Love S, et al. High frequency of apolipoprotein E E2 allele in hemorrhage due to cerebral amyloid angiopathy. Ann Neurol 1997; 41:716-721.
29. O’Donnell HC, Rosand J, Knudsen KA, et al. Apolipoprotein E genotype and the risk of recurrent lobar intracerebral hemorrhage. N Engl J Med 2000; 342:240-245.
30. Greenberg SM, Briggs ME, Hyman BT, et al. Apolipoprotein E E4 is associated with the presence and earlier onset of hemorrhage in cerebral amyloid angiopathy. Stroke 1996; 27:1333-1337.
31. Biffi A, Anderson CD, Jagiella JM, et al. APOE genotype and extent of bleeding and outcome in lobar intracerebral haemorrhage: a genetic association study. Lancet Neurol 2011; 10:702-709.
32. Montaner J. Genetics of intracerebral haemorrhage: a tsunami effect of APOE E2 genotype on brain bleeding size? Lancet Neurol 2011; 10:673-675.
33. 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.
34. Sumii T, Lo EH. Involvement of matrix metalloproteinase in thrombolysis-associated hemorrhagic transformation after embolic focal ischemia in rats. Stroke 2002; 33:831-836.
35. Hernandez-Guillamon M, Mawhirt S, Fossati S, et al. Matrix metalloproteinase 2 (MMP-2) degrades soluble vasculotropic amyloid-? e22q and l34v mutants, delaying their toxicity for human brain microvascular endothelial cells. JBiol Chem 2010; 285:27144-27158.
36. Rosenberg GA. Matrix metalloproteinases and their multiple roles in neurodegenerative diseases. Lancet Neurol 2009; 8:205-216.
37. Lee JM, Yin KJ, Hsin I, et al. Matrix metalloproteinase-9 and spontaneous hemorrhage in an animal model of cerebral amyloid angiopathy. Ann Neurol 2003; 54:379-382.
38. Del Zoppo GJ. Bleeding in the brain: amyloid-p may keep clots away. Nat Med 2009; 15:1132-1133.
39. Xu F, Previti ML, Nieman MT, et al. Ap APP/APLP2 family of Kunitz serine proteinase inhibitors regulate cerebral thrombosis. J Neurosci 2009; 29:5666-5670.
40. Flaherty ML, Kissela B, Woo D, et al. The increasing incidence of anticoagulant-associated intracerebral hemorrhage. Neurology 2007; 68:116-121.
41. 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; 41:1222-1228.
42. Rosand J, Hylek EM, O’Donnell HC, Greenberg SM. Warfarin-associated hemorrhage and cerebral amyloid angiopathy: a genetic and pathologic study. Neurology 2000; 55:947-951.
43. McCarron MO, Nicoll JA. Cerebral amyloid angiopathy and thrombolysis-related intracerebral haemorrhage. Lancet Neurol 2004; 3:484-492.
44. Sloan MA, Price TR, Petito CK, et al. Clinical features and pathogenesis of intracerebral hemorrhage after RT-PA and heparin therapy for acute myocardial infarction: the Thrombolysis In Myocardial Infarction (TIMI) (ii) pilot and randomized clinical trial combined experience. Neurology 1995; 45:649-658.
45. Kalimo H, Miao Q, Tikka S, et al. CADASIL: the most common hereditary subcortical vascular dementia. Future Neurol 2008; 3:683-704.
46. Choi JC, Kang SY, Kang JH, Park JK. Intracerebral hemorrhages in CADASIL. Neurology 2006; 67:2042-2044.
47. Kumar S, Goddeau RP, Jr., Selim MH, et al. Atraumatic convexal subarachnoid hemorrhage: clinical presentation, imaging patterns, and etiologies. Neurology 2010; 74:893-899.
48. Raposo N, Viguier A, Cuvinciuc V, et al. Cortical subarachnoid haemorrhage in the elderly: a recurrent event probably related to cerebral amyloid angiopathy. EurJ Neurol 2011; 18:597-603.
49. Linn J, Herms J, Dichgans M, et al. Subarachnoid hemosiderosis and superficial cortical hemosiderosis in cerebral amyloid angiopathy. AJNR Am J Neuroradiol 2008; 29:184-186.
50. Cuvinciuc V, Viguier A, Calviere L, et al. Isolated acute nontraumatic cortical subarachnoid hemorrhage. AJNR Am J Neuroradiol 2010; 31:1355-1362.
51. Katoh M, Yoshino M, Asaoka K, et al. A restricted subarachnoid hemorrhage in the cortical sulcus in cerebral amyloid angiopathy: could it be a warning sign? Surg Neurol 2007; 68:457-460.
52. Karabatsou K, Lecky BR, Rainov NG, Broome JC, White RP. Cerebral amyloid angiopathy with symptomatic or occult subarachnoid haemorrhage. Eur Neurol 2007; 57:103-105.
53. Kase CS, Nguyen TN. The clinical conundrum of convexal subarachnoid hemorrhage. Neurology 2010; 74:874-875.
54. Linn J, Halpin A, Demaerel P, et al. Prevalence of superficial siderosis in patients with cerebral amyloid angiopathy. Neurology 2010; 74:1346-1350.
55. Beitzke M, Gattringer T, Enzinger C, et al. Clinical presentation, etiology, and long-term prognosis in patients with nontraumatic convexal subarachnoid hemorrhage. Stroke 2011; 42:3055-3060.
56. Fearnley JM, Stevens JM, Rudge P. Superficial siderosis of the central nervous system. Brain 1995; 118 (Pt 4):1051-1066.
57. Kumar N, Cohen-Gadol AA, Wright RA, et al. Superficial siderosis. Neurology 2006; 66:1144-1152.
58. Feldman HH, Maia LF, Mackenzie IR, et al. Superficial siderosis: a potential diagnostic marker of cerebral amyloid angiopathy in Alzheimer disease. Stroke 2008; 39:2894-2897.
59. Vernooij MW, Ikram MA, Hofman A, et al. Superficial siderosis in the general population. Neurology 2009; 73:202-205.
60. Levy M, Turtzo C, Llinas RH. Superficial siderosis: a case report and review of the literature. Nat Clin Pract Neurol 2007; 3:54-58; quiz 59.
61. Greenberg SM, Vernooij MW, Cordonnier C, et al. Cerebral microbleeds: a guide to detection and interpretation. Lancet Neurol 2009; 8:165-174.
62. Haacke EM, DelProposto ZS, Chaturvedi S, et al. Imaging cerebral amyloid angiopathy with susceptibility-weighted imaging. AJNR Am J Neuroradiol 2007; 28:316-317.
63. Kellner CP, Connolly ES, Jr. Neuroprotective strategies for intracerebral hemorrhage: trials and translation. Stroke 2010; 41: S99-S102.
64. Vernooij MW, van der Lugt A, Ikram MA, et al. Prevalence and risk factors of cerebral microbleeds: the Rotterdam Scan Study. Neurology 2008; 70:1208-1214.
65. Nandigam RN, Viswanathan A, Delgado P, et al. MR imaging detection of cerebral microbleeds: effect of susceptibility-weighted imaging, section thickness, and field strength. AJNR Am J Neuroradiol 2009; 30:338-343.
66. Theysohn JM, Kraff O, Maderwald S, et al. Seven Tesla MRI of microbleeds and white matter lesions as seen in vascular dementia. J Magn Reson Imaging 2011; 33:782-791.
67. Conijn MM, Geerlings MI, Luijten PR, et al. Visualization of cerebral microbleeds with dual-echo T2*- weighted magnetic resonance imaging at 7.0 T. J Magn Reson Imaging 2010; 32:52-59.
68. De Reuck J, Auger F, Cordonnier C, et al. Comparison of 7.0-T T(2)*-magnetic resonance imaging of cerebral bleeds in postmortem brain sections of Alzheimer patients with their neuropathological correlates. Cerebrovasc Dis 2011; 31:511-517.
69. Lee SH, Lee ST, Kim BJ, et al. Dynamic temporal change of cerebral microbleeds: long-term follow-up MRI study. PLoS One 2011; 6:e25930.
70. Tsushima Y, Tanizaki Y, Aoki J, Endo K. MR detection of microhemorrhages in neurologically healthy adults. Neuroradiology 2002; 44:31-36.
71. Cordonnier C. Brain microbleeds: more evidence, but still a clinical dilemma. Curr Opin Neurol 2011; 24:69-74.
72. Loitfelder M, Seiler S, Schwingenschuh P, Schmidt R. Cerebral microbleeds: a review. Panminerva Med 2012; 54:149-160.
73. Hofman A, Breteler MM, van Duijn CM, et al. The Rotterdam Study: 2010 objectives and design update. Eur J Epidemiol 2009; 24:553-572.
74. Koennecke HC. Cerebral microbleeds on MRI: prevalence, associations, and potential clinical implications. Neurology 2006; 66:165-171.
75. Cordonnier C, Al-Shahi Salman R, Wardlaw J. Spontaneous brain microbleeds: systematic review, subgroup analyses and standards for study design and reporting. Brain 2007; 130:1988-2003.
76. Chabriat H, Joutel A, Dichgans M, Tournier-Lasserve E, Bousser MG. CADASIL. Lancet Neurol 2009; 8:643-653.
77. Dichgans M, Holtmannspotter M, Herzog J, et al. Cerebral microbleeds in CADASIL: a gradient-echo magnetic resonance imaging and autopsy study. Stroke 2002; 33:67-71.
78. Van den Boom R, Bornebroek M, Behloul F, et al. Microbleeds in hereditary cerebral hemorrhage with amyloidosis-Dutch type. Neurology 2005; 64:1288-1289.
79. Sveinbjornsdottir S, Sigurdsson S, Aspelund T, et al. Cerebral microbleeds in the population based ages- Reykjavik study: prevalence and location. J Neurol Neurosurg Psychiatry 2008; 79:1002-1006.
80. Poels MM, Vernooij MW, Ikram MA, et al. Prevalence and risk factors of cerebral microbleeds: an update of the Rotterdam Scan Study. Stroke 2010; 41: S103-106.
81. Van Es AC, van der Grond J, de Craen AJ, et al. Cerebral microbleeds and cognitive functioning in the PROSPER study. Neurology 2011; 77:1446-1452.
82. Henneman WJ, Sluimer JD, Cordonnier C, et al. MRI biomarkers of vascular damage and atrophy predicting mortality in a memory clinic population. Stroke 2009; 40:492-498.
83. Altmann-Schneider I, Trompet S, de Craen AJ, et al. Cerebral microbleeds are predictive of mortality in the elderly. Stroke 2011; 42:638-644.
84. Fazekas F, Kleinert R, Roob G, et al. Histopathologic analysis of foci of signal loss on gradient- echo T2*-weighted MR images in patients with spontaneous intracerebral hemorrhage: evidence of microangiopathy- related microbleeds. AJNR Am J Neuroradiol 1999; 20:637-642.
85. Tanaka A, Ueno Y, Nakayama Y, Takano K, Takebayashi S. Small chronic hemorrhages and ischemic lesions in association with spontaneous intracerebral hematomas. Stroke 1999; 30:1637-1642.
86. Schrag M, McAuley G, Pomakian J, et al. Correlation of hypointensities in susceptibility- weighted images to tissue histology in dementia patients with cerebral amyloid angiopathy: a postmortem MRI study. Acta Neuropathol 2010; 119:291-302.
87. Grinberg LT, Thal DR. Vascular pathology in the aged human brain. Acta Neuropathol 2010; 119:277-290.
88. Hommet C, Mondon K, Constans T, et al. Review of cerebral microangiopathy and Alzheimer’s disease: relation between white matter hyperintensities and microbleeds. Dement Geriatr Cogn Disord 2011; 32:367-378.
89. Shoamanesh A, Kwok CS, Benavente O. Cerebral microbleeds: histopathological correlation of neuroimaging. Cerebrovasc Dis 2011; 32:528-534.
90. Greenberg SM, Eng JA, Ning M, Smith EE, Rosand J. Hemorrhage burden predicts recurrent intracerebral hemorrhage after lobar hemorrhage. Stroke 2004; 35:1415-1420.
91. Knudsen KA, Rosand J, Karluk D, Greenberg SM. Clinical diagnosis of cerebral amyloid angiopathy: validation of the Boston criteria. Neurology 2001; 56:537-539.
92. Roob G, Lechner A, Schmidt R, et al. Frequency and location of microbleeds in patients with primary intracerebral hemorrhage. Stroke 2000; 31:2665-2669.
93. Thal DR, Ghebremedhin E, Rub U, et al. Two types of sporadic cerebral amyloid angiopathy. J Neuropathol Exp Neurol 2002; 61:282-293.
94. Maxwell SS, Jackson CA, Paternoster L, et al. Genetic associations with brain microbleeds: systematic review and meta-analyses. Neurology 2011; 77:158-167.
95. Poels MM, Ikram MA, van der Lugt A, et al. Incidence of cerebral microbleeds in the general population: the Rotterdam Scan Study. Stroke 2011; 42:656-661.
96. Jeerakathil T, Wolf PA, Beiser A, et al. Cerebral microbleeds: prevalence and associations with cardiovascular risk factors in the Framingham Study. Stroke 2004; 35:1831-1835.
97. Nakata-Kudo Y, Mizuno T, Yamada K, et al. Microbleeds in Alzheimer disease are more related to cerebral amyloid angiopathy than cerebrovascular disease. Dement Geriatr Cogn Disord 2006; 22:8-14.
98. Charidimou A, Werring DJ. Cerebral microbleeds: detection, mechanisms and clinical challenges. Future Neurol 2011; 6:587-611.
99. Cullen KM, Kocsi Z, Stone J. Microvascular pathology in the aging human brain: evidence that senile plaques are sites of microhaemorrhages. Neurobiol Aging 2006; 27:1786-1796.
100. Tang WK, Chen YK, Lu JY, et al. Absence of cerebral microbleeds predicts reversion of vascular “cognitive impairment no dementia” in stroke. Int J Stroke 2011; 6:498-505.
101. Dierksen GA, Skehan ME, Khan MA, et al. Spatial relation between microbleeds and amyloid deposits in amyloid angiopathy. Ann Neurol 2010; 68:545-548.
102. Lee SH, Bae HJ, Kwon SJ, et al. Cerebral microbleeds are regionally associated with intracerebral hemorrhage. Neurology 2004; 62:72-76.
103. Charidimou A, Shakeshaft C, Werring DJ. Cerebral microbleeds on magnetic resonance imaging and anticoagulant-associated intracerebral hemorrhage risk. Front Neurol 2012; 3:133.
104. Charidimou A, Werring DJ. Cerebral microbleeds and cognition in cerebrovascular disease: an update. J Neurol Sci 2012.
105. Gold G, Kovari E, Herrmann FR, et al. Cognitive consequences of thalamic, basal ganglia, and deep white matter lacunes in brain aging and dementia. Stroke 2005; 36:1184-1188.
106. Werring DJ. Cerebral microbleeds: clinical and pathophysiological significance. J Neuroimaging 2007; 17:193-203.
107. Grabowski TJ, Cho HS, Vonsattel JP, Rebeck GW, Greenberg SM. Novel amyloid precursor protein mutation in an Iowa family with dementia and severe cerebral amyloid angiopathy. Ann Neurol 2001; 49:697-705.
108. Mandybur TI. Cerebral amyloid angiopathy: the vascular pathology and complications. J Neuropathol Exp Neurol 1986; 45:79-90.
109. Okoye MI, Watanabe I. Ultrastructural features of cerebral amyloid angiopathy. Hum Pathol 1982; 13:1127-1132.
110. Viswanathan A, Greenberg SM. Cerebral amyloid angiopathy in the elderly. Ann Neurol 2011; 70:871-880.
111. Okazaki S, Sakaguchi M, Hyun B, et al. Cerebral microbleeds predictimpending intracranial hemorrhage in infective endocarditis. Cerebrovasc Dis 2011; 32:483-488.
112. Gregoire SM, Jager HR, Yousry TA, et al. Brain microbleeds as a potential risk factor for antiplatelet-related intracerebral haemorrhage: hospital-based, case-control study. J Neurol Neurosurg Psychiatry 2010; 81:679-684.
113. Vernooij MW, Haag MD, van der Lugt A, et al. Use of antithrombotic drugs and the presence of cerebral microbleeds: the Rotterdam Scan Study. Arch Neurol 2009; 66:714-720.
114. Wong KS, Chan YL, Liu JY, Gao S, Lam WW. Asymptomatic microbleeds as a risk factor for aspirin-associated intracerebral hemorrhages. Neurology 2003; 60:511-513.
115. Charidimou A, Kakar P, Fox Z, Werring DJ. Cerebral microbleeds and the risk of intracerebral haemorrhage after thrombolysis for acute ischaemic stroke: systematic review and metaanalysis. J Neurol Neurosurg Psychiatry 2013; 84:277-280.
116. Shoamanesh A, Kwok CS, Lim PA, Benavente OR. Postthrombolysis intracranial hemorrhage risk of cerebral microbleeds in acute stroke patients: a systematic review and meta-analysis. Int J Stroke 2013; 8:348-356.
117. Cordonnier C, van der Flier WM. Brain microbleeds and Alzheimer’s disease: innocent observation or key player? Brain 2011; 134:335-344.