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Published in: Acta Neuropathologica 3/2010

Open Access 01-03-2010 | Review

Vascular pathology in the aged human brain

Authors: Lea Tenenholz Grinberg, Dietmar Rudolf Thal

Published in: Acta Neuropathologica | Issue 3/2010

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Abstract

Cerebral atherosclerosis (AS), small vessel disease (SVD), and cerebral amyloid angiopathy (CAA) are the most prevalent arterial disorders in the aged brain. Pathogenetically, AS and SVD share similar mechanisms: plasma protein leakage into the vessel wall, accumulation of lipid-containing macrophages, and fibrosis of the vessel wall. CAA, on the other hand, is characterized by the deposition of the amyloid β-protein in the vessel wall. Despite these differences between CAA, AS and SVD, apolipoprotein E (apoE) is involved in all three disorders. Such a pathogenetic link may explain the correlations between AS, SVD, CAA, and Alzheimer’s disease in the brains of elderly individuals reported in the literature. In addition, AS, SVD, and CAA can lead to tissue lesions such as hemorrhage and infarction. Moreover, intracerebral SVD leads to plasma protein leakage into the damaged vessel wall and into the perivascular space resulting in a blood–brain barrier (BBB) dysfunction. This SVD-related BBB dysfunction is considered to cause white matter lesions (WMLs) and lacunar infarcts. In this review, we demonstrate the relationship between AS, SVD, and CAA as well as their contribution to the development of vascular tissue lesions and we emphasize an important role for apoE in the pathogenesis of vessel disorders and vascular tissue lesions as well as for BBB dysfunction on WML and lacunar infarct development.
Literature
1.
go back to reference Alafuzoff I, Adolfsson R, Grundke-Iqbal I, Winblad B (1985) Perivascular deposits of serum proteins in cerebral cortex in vascular dementia. Acta Neuropathol 66:292–298PubMedCrossRef Alafuzoff I, Adolfsson R, Grundke-Iqbal I, Winblad B (1985) Perivascular deposits of serum proteins in cerebral cortex in vascular dementia. Acta Neuropathol 66:292–298PubMedCrossRef
2.
go back to reference Alafuzoff I, Thal DR, Arzberger T, Bogdanovic N, Al-Sarraj S, Bodi I, Boluda S, Bugiani O, Duyckaerts C, Gelpi E, Gentleman S, Giaccone G, Graeber M, Hortobagyi T, Hoftberger R, Ince P, Ironside JW, Kavantzas N, King A, Korkolopoulou P, Kovacs GG, Meyronet D, Monoranu C, Nilsson T, Parchi P, Patsouris E, Pikkarainen M, Revesz T, Rozemuller A, Seilhean D, Schulz-Schaeffer W, Streichenberger N, Wharton SB, Kretzschmar H (2009) Assessment of beta-amyloid deposits in human brain: a study of the BrainNet Europe Consortium. Acta Neuropathol 117:309–320PubMedCrossRef Alafuzoff I, Thal DR, Arzberger T, Bogdanovic N, Al-Sarraj S, Bodi I, Boluda S, Bugiani O, Duyckaerts C, Gelpi E, Gentleman S, Giaccone G, Graeber M, Hortobagyi T, Hoftberger R, Ince P, Ironside JW, Kavantzas N, King A, Korkolopoulou P, Kovacs GG, Meyronet D, Monoranu C, Nilsson T, Parchi P, Patsouris E, Pikkarainen M, Revesz T, Rozemuller A, Seilhean D, Schulz-Schaeffer W, Streichenberger N, Wharton SB, Kretzschmar H (2009) Assessment of beta-amyloid deposits in human brain: a study of the BrainNet Europe Consortium. Acta Neuropathol 117:309–320PubMedCrossRef
3.
go back to reference Attems J (2005) Sporadic cerebral amyloid angiopathy: pathology, clinical implications, and possible pathomechanisms. Acta Neuropathol 110:345–359PubMedCrossRef Attems J (2005) Sporadic cerebral amyloid angiopathy: pathology, clinical implications, and possible pathomechanisms. Acta Neuropathol 110:345–359PubMedCrossRef
4.
go back to reference Attems J, Jellinger KA (2004) Only cerebral capillary amyloid angiopathy correlates with Alzheimer pathology—a pilot study. Acta Neuropathol (Berl) 107:83–90CrossRef Attems J, Jellinger KA (2004) Only cerebral capillary amyloid angiopathy correlates with Alzheimer pathology—a pilot study. Acta Neuropathol (Berl) 107:83–90CrossRef
5.
go back to reference Beach TG, Wilson JR, Sue LI, Newell A, Poston M, Cisneros R, Pandya Y, Esh C, Connor DJ, Sabbagh M, Walker DG, Roher AE (2007) Circle of Willis atherosclerosis: association with Alzheimer’s disease, neuritic plaques and neurofibrillary tangles. Acta Neuropathol 113:13–21PubMedCrossRef Beach TG, Wilson JR, Sue LI, Newell A, Poston M, Cisneros R, Pandya Y, Esh C, Connor DJ, Sabbagh M, Walker DG, Roher AE (2007) Circle of Willis atherosclerosis: association with Alzheimer’s disease, neuritic plaques and neurofibrillary tangles. Acta Neuropathol 113:13–21PubMedCrossRef
6.
go back to reference Bell RD, Zlokovic BV (2009) Neurovascular mechanisms and blood–brain barrier disorder in Alzheimer’s disease. Acta Neuropathol 118:103–113PubMedCrossRef Bell RD, Zlokovic BV (2009) Neurovascular mechanisms and blood–brain barrier disorder in Alzheimer’s disease. Acta Neuropathol 118:103–113PubMedCrossRef
7.
go back to reference Bergeron C, Ranalli PJ, Miceli PN (1987) Amyloid angiopathy in Alzheimer’s disease. Can J Neurol Sci 14:564–569PubMed Bergeron C, Ranalli PJ, Miceli PN (1987) Amyloid angiopathy in Alzheimer’s disease. Can J Neurol Sci 14:564–569PubMed
8.
go back to reference Boucher P, Gotthardt M, Li WP, Anderson RG, Herz J (2003) LRP: role in vascular wall integrity and protection from atherosclerosis. Science 300:329–332PubMedCrossRef Boucher P, Gotthardt M, Li WP, Anderson RG, Herz J (2003) LRP: role in vascular wall integrity and protection from atherosclerosis. Science 300:329–332PubMedCrossRef
9.
go back to reference Boyd HC, Gown AM, Wolfbauer G, Chait A (1989) Direct evidence for a protein recognized by a monoclonal antibody against oxidatively modified LDL in atherosclerotic lesions from a Watanabe heritable hyperlipidemic rabbit. Am J Pathol 135:815–825PubMed Boyd HC, Gown AM, Wolfbauer G, Chait A (1989) Direct evidence for a protein recognized by a monoclonal antibody against oxidatively modified LDL in atherosclerotic lesions from a Watanabe heritable hyperlipidemic rabbit. Am J Pathol 135:815–825PubMed
10.
go back to reference Boyles JK, Pitas RE, Wilson E, Mahley RW, Taylor JM (1985) Apolipoprotein E associated with astrocytic glia of the central nervous system and with nonmyelinating glia of the peripheral nervous system. J Clin Invest 76:1501–1513PubMedCrossRef Boyles JK, Pitas RE, Wilson E, Mahley RW, Taylor JM (1985) Apolipoprotein E associated with astrocytic glia of the central nervous system and with nonmyelinating glia of the peripheral nervous system. J Clin Invest 76:1501–1513PubMedCrossRef
11.
go back to reference Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82:239–259PubMedCrossRef Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82:239–259PubMedCrossRef
12.
go back to reference Briley DP, Haroon S, Sergent SM, Thomas S (2000) Does leukoaraiosis predict morbidity and mortality? Neurology 54:90–94PubMed Briley DP, Haroon S, Sergent SM, Thomas S (2000) Does leukoaraiosis predict morbidity and mortality? Neurology 54:90–94PubMed
13.
go back to reference Brun A, Englund E (1986) A white matter disorder in dementia of the Alzheimer type: a pathoanatomical study. Ann Neurol 19:253–262PubMedCrossRef Brun A, Englund E (1986) A white matter disorder in dementia of the Alzheimer type: a pathoanatomical study. Ann Neurol 19:253–262PubMedCrossRef
14.
go back to reference Cadavid D, Mena H, Koeller K, Frommelt RA (2000) Cerebral beta amyloid angiopathy is a risk factor for cerebral ischemic infarction. A case control study in human brain biopsies. J Neuropathol Exp Neurol 59:768–773PubMed Cadavid D, Mena H, Koeller K, Frommelt RA (2000) Cerebral beta amyloid angiopathy is a risk factor for cerebral ischemic infarction. A case control study in human brain biopsies. J Neuropathol Exp Neurol 59:768–773PubMed
15.
go back to reference Calhoun ME, Burgermeister P, Phinney AL, Stalder M, Tolnay M, Wiederhold KH, Abramowski D, Sturchler-Pierrat C, Sommer B, Staufenbiel M, Jucker M (1999) Neuronal overexpression of mutant amyloid precursor protein results in prominent deposition of cerebrovascular amyloid. Proc Natl Acad Sci USA 96:14088–14093PubMedCrossRef Calhoun ME, Burgermeister P, Phinney AL, Stalder M, Tolnay M, Wiederhold KH, Abramowski D, Sturchler-Pierrat C, Sommer B, Staufenbiel M, Jucker M (1999) Neuronal overexpression of mutant amyloid precursor protein results in prominent deposition of cerebrovascular amyloid. Proc Natl Acad Sci USA 96:14088–14093PubMedCrossRef
16.
go back to reference Carare RO, Bernardes-Silva M, Newman TA, Page AM, Nicoll JA, Perry VH, Weller RO (2008) Solutes, but not cells, drain from the brain parenchyma along basement membranes of capillaries and arteries: significance for cerebral amyloid angiopathy and neuroimmunology. Neuropathol Appl Neurobiol 34:131–144PubMedCrossRef Carare RO, Bernardes-Silva M, Newman TA, Page AM, Nicoll JA, Perry VH, Weller RO (2008) Solutes, but not cells, drain from the brain parenchyma along basement membranes of capillaries and arteries: significance for cerebral amyloid angiopathy and neuroimmunology. Neuropathol Appl Neurobiol 34:131–144PubMedCrossRef
17.
go back to reference Challa VR, Bell MA, Moody DM (1990) A combined hematoxylin–eosin, alkaline phosphatase and high-resolution microradiographic study of lacunes. Clin Neuropathol 9:196–204PubMed Challa VR, Bell MA, Moody DM (1990) A combined hematoxylin–eosin, alkaline phosphatase and high-resolution microradiographic study of lacunes. Clin Neuropathol 9:196–204PubMed
18.
go back to reference Chuang PT, Cheng HJ, Lin SJ, Jan KM, Lee MM, Chien S (1990) Macromolecular transport across arterial and venous endothelium in rats. Studies with Evans blue-albumin and horseradish peroxidase. Arteriosclerosis 10:188–197PubMed Chuang PT, Cheng HJ, Lin SJ, Jan KM, Lee MM, Chien S (1990) Macromolecular transport across arterial and venous endothelium in rats. Studies with Evans blue-albumin and horseradish peroxidase. Arteriosclerosis 10:188–197PubMed
19.
go back to reference Deane R, Sagare A, Hamm K, Parisi M, Lane S, Finn MB, Holtzman DM, Zlokovic BV (2008) apoE isoform-specific disruption of amyloid beta peptide clearance from mouse brain. J Clin Invest 118:4002–4013PubMedCrossRef Deane R, Sagare A, Hamm K, Parisi M, Lane S, Finn MB, Holtzman DM, Zlokovic BV (2008) apoE isoform-specific disruption of amyloid beta peptide clearance from mouse brain. J Clin Invest 118:4002–4013PubMedCrossRef
20.
go back to reference Deguchi JO, Aikawa E, Libby P, Vachon JR, Inada M, Krane SM, Whittaker P, Aikawa M (2005) Matrix metalloproteinase-13/collagenase-3 deletion promotes collagen accumulation and organization in mouse atherosclerotic plaques. Circulation 112:2708–2715PubMedCrossRef Deguchi JO, Aikawa E, Libby P, Vachon JR, Inada M, Krane SM, Whittaker P, Aikawa M (2005) Matrix metalloproteinase-13/collagenase-3 deletion promotes collagen accumulation and organization in mouse atherosclerotic plaques. Circulation 112:2708–2715PubMedCrossRef
21.
go back to reference Deguchi JO, Aikawa M, Tung CH, Aikawa E, Kim DE, Ntziachristos V, Weissleder R, Libby P (2006) Inflammation in atherosclerosis: visualizing matrix metalloproteinase action in macrophages in vivo. Circulation 114:55–62PubMedCrossRef Deguchi JO, Aikawa M, Tung CH, Aikawa E, Kim DE, Ntziachristos V, Weissleder R, Libby P (2006) Inflammation in atherosclerosis: visualizing matrix metalloproteinase action in macrophages in vivo. Circulation 114:55–62PubMedCrossRef
22.
23.
go back to reference Dollery CM, Owen CA, Sukhova GK, Krettek A, Shapiro SD, Libby P (2003) Neutrophil elastase in human atherosclerotic plaques: production by macrophages. Circulation 107:2829–2836PubMedCrossRef Dollery CM, Owen CA, Sukhova GK, Krettek A, Shapiro SD, Libby P (2003) Neutrophil elastase in human atherosclerotic plaques: production by macrophages. Circulation 107:2829–2836PubMedCrossRef
24.
go back to reference Dufouil C, de Kersaint-Gilly A, Besancon V, Levy C, Auffray E, Brunnereau L, Alperovitch A, Tzourio C (2001) Longitudinal study of blood pressure and white matter hyperintensities: the EVA MRI Cohort. Neurology 56:921–926PubMed Dufouil C, de Kersaint-Gilly A, Besancon V, Levy C, Auffray E, Brunnereau L, Alperovitch A, Tzourio C (2001) Longitudinal study of blood pressure and white matter hyperintensities: the EVA MRI Cohort. Neurology 56:921–926PubMed
25.
go back to reference Englund E (1998) Neuropathology of white matter changes in Alzheimer’s disease and vascular dementia. Dement Geriatr Cogn Disord 9(Suppl 1):6–12PubMedCrossRef Englund E (1998) Neuropathology of white matter changes in Alzheimer’s disease and vascular dementia. Dement Geriatr Cogn Disord 9(Suppl 1):6–12PubMedCrossRef
26.
go back to reference Enzinger C, Fazekas F, Ropele S, Schmidt R (2007) Progression of cerebral white matter lesions—clinical and radiological considerations. J Neurol Sci 257:5–10PubMedCrossRef Enzinger C, Fazekas F, Ropele S, Schmidt R (2007) Progression of cerebral white matter lesions—clinical and radiological considerations. J Neurol Sci 257:5–10PubMedCrossRef
27.
go back to reference Fan J, Donkin J, Wellington C (2009) Greasing the wheels of Abeta clearance in Alzheimer’s disease: the role of lipids and apolipoprotein E. Biofactors 35:239–248PubMedCrossRef Fan J, Donkin J, Wellington C (2009) Greasing the wheels of Abeta clearance in Alzheimer’s disease: the role of lipids and apolipoprotein E. Biofactors 35:239–248PubMedCrossRef
28.
go back to reference Fazekas F, Kleinert R, Offenbacher H, Schmidt R, Kleinert G, Payer F, Radner H, Lechner H (1993) Pathologic correlates of incidental MRI white matter signal hyperintensities. Neurology 43:1683–1689PubMed Fazekas F, Kleinert R, Offenbacher H, Schmidt R, Kleinert G, Payer F, Radner H, Lechner H (1993) Pathologic correlates of incidental MRI white matter signal hyperintensities. Neurology 43:1683–1689PubMed
30.
go back to reference Fisher CM (1965) Lacunes: small, deep cerebral infarcts. Neurology 15:774–784PubMed Fisher CM (1965) Lacunes: small, deep cerebral infarcts. Neurology 15:774–784PubMed
31.
32.
go back to reference Frosst P, Blom HJ, Milos R, Goyette P, Sheppard CA, Matthews RG, Boers GJ, den Heijer M, Kluijtmans LA, van den Heuvel LP et al (1995) A candidate genetic risk factor for vascular disease: a common mutation in methylenetetrahydrofolate reductase. Nat Genet 10:111–113PubMedCrossRef Frosst P, Blom HJ, Milos R, Goyette P, Sheppard CA, Matthews RG, Boers GJ, den Heijer M, Kluijtmans LA, van den Heuvel LP et al (1995) A candidate genetic risk factor for vascular disease: a common mutation in methylenetetrahydrofolate reductase. Nat Genet 10:111–113PubMedCrossRef
33.
go back to reference Gerraty RP, Parsons MW, Barber PA, Darby DG, Desmond PM, Tress BM, Davis SM (2002) Examining the lacunar hypothesis with diffusion and perfusion magnetic resonance imaging. Stroke 33:2019–2024PubMedCrossRef Gerraty RP, Parsons MW, Barber PA, Darby DG, Desmond PM, Tress BM, Davis SM (2002) Examining the lacunar hypothesis with diffusion and perfusion magnetic resonance imaging. Stroke 33:2019–2024PubMedCrossRef
34.
go back to reference Glenner GG, Wong CW (1984) Alzheimer’s disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun 120:885–890PubMedCrossRef Glenner GG, Wong CW (1984) Alzheimer’s disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun 120:885–890PubMedCrossRef
35.
go back to reference Gomis M, Sobrino T, Ois A, Millan M, Rodriguez-Campello A, Perez de la Ossa N, Rodriguez-Gonzalez R, Jimenez-Conde J, Cuadrado-Godia E, Roquer J, Davalos A (2009) Plasma beta-amyloid 1–40 is associated with the diffuse small vessel disease subtype. Stroke 40:3197–3201PubMedCrossRef Gomis M, Sobrino T, Ois A, Millan M, Rodriguez-Campello A, Perez de la Ossa N, Rodriguez-Gonzalez R, Jimenez-Conde J, Cuadrado-Godia E, Roquer J, Davalos A (2009) Plasma beta-amyloid 1–40 is associated with the diffuse small vessel disease subtype. Stroke 40:3197–3201PubMedCrossRef
36.
go back to reference Gouw AA, van der Flier WM, Fazekas F, van Straaten EC, Pantoni L, Poggesi A, Inzitari D, Erkinjuntti T, Wahlund LO, Waldemar G, Schmidt R, Scheltens P, Barkhof F (2008) Progression of white matter hyperintensities and incidence of new lacunes over a 3-year period: the Leukoaraiosis and Disability study. Stroke 39:1414–1420PubMedCrossRef Gouw AA, van der Flier WM, Fazekas F, van Straaten EC, Pantoni L, Poggesi A, Inzitari D, Erkinjuntti T, Wahlund LO, Waldemar G, Schmidt R, Scheltens P, Barkhof F (2008) Progression of white matter hyperintensities and incidence of new lacunes over a 3-year period: the Leukoaraiosis and Disability study. Stroke 39:1414–1420PubMedCrossRef
37.
go back to reference Greenberg SM, Briggs ME, Hyman BT, Kokoris GJ, Takis C, Kanter DS, Kase CS, Pessin MS (1996) Apolipoprotein E epsilon 4 is associated with the presence and earlier onset of hemorrhage in cerebral amyloid angiopathy. Stroke 27:1333–1337PubMed Greenberg SM, Briggs ME, Hyman BT, Kokoris GJ, Takis C, Kanter DS, Kase CS, Pessin MS (1996) Apolipoprotein E epsilon 4 is associated with the presence and earlier onset of hemorrhage in cerebral amyloid angiopathy. Stroke 27:1333–1337PubMed
38.
go back to reference Greenberg SM, Vernooij MW, Cordonnier C, Viswanathan A, Al-Shahi Salman R, Warach S, Launer LJ, Van Buchem MA, Breteler MM (2009) Cerebral microbleeds: a guide to detection and interpretation. Lancet Neurol 8:165–174PubMedCrossRef Greenberg SM, Vernooij MW, Cordonnier C, Viswanathan A, Al-Shahi Salman R, Warach S, Launer LJ, Van Buchem MA, Breteler MM (2009) Cerebral microbleeds: a guide to detection and interpretation. Lancet Neurol 8:165–174PubMedCrossRef
39.
go back to reference Grinberg LT, Amaro Junior E, da Silva AV, da Silva RE, Sato JR, dos Santos DD, de Paula Pacheco S, de Lucena Ferretti RE, Paraizo Leite RE, Pasqualucci CA, Teipel SJ, Flatz WH, Heinsen H (2009) Improved detection of incipient vascular changes by a biotechnological platform combining post mortem MRI in situ with neuropathology. J Neurol Sci 283:2–8PubMedCrossRef Grinberg LT, Amaro Junior E, da Silva AV, da Silva RE, Sato JR, dos Santos DD, de Paula Pacheco S, de Lucena Ferretti RE, Paraizo Leite RE, Pasqualucci CA, Teipel SJ, Flatz WH, Heinsen H (2009) Improved detection of incipient vascular changes by a biotechnological platform combining post mortem MRI in situ with neuropathology. J Neurol Sci 283:2–8PubMedCrossRef
40.
go back to reference Haass C, Koo EH, Mellon A, Hung AY, Selkoe DJ (1992) Targeting of cell-surface beta-amyloid precursor protein to lysosomes: alternative processing into amyloid-bearing fragments. Nature 357:500–503PubMedCrossRef Haass C, Koo EH, Mellon A, Hung AY, Selkoe DJ (1992) Targeting of cell-surface beta-amyloid precursor protein to lysosomes: alternative processing into amyloid-bearing fragments. Nature 357:500–503PubMedCrossRef
41.
go back to reference Hacke W, Schwab S, Horn M, Spranger M, De Georgia M, von Kummer R (1996) ‘Malignant’ middle cerebral artery territory infarction: clinical course and prognostic signs. Arch Neurol 53:309–315PubMed Hacke W, Schwab S, Horn M, Spranger M, De Georgia M, von Kummer R (1996) ‘Malignant’ middle cerebral artery territory infarction: clinical course and prognostic signs. Arch Neurol 53:309–315PubMed
42.
go back to reference Hansson GK, Jonasson L, Seifert PS, Stemme S (1989) Immune mechanisms in atherosclerosis. Arteriosclerosis 9:567–578PubMed Hansson GK, Jonasson L, Seifert PS, Stemme S (1989) Immune mechanisms in atherosclerosis. Arteriosclerosis 9:567–578PubMed
43.
go back to reference Heeren J, Beisiegel U, Grewal T (2006) Apolipoprotein E recycling: implications for dyslipidemia and atherosclerosis. Arterioscler Thromb Vasc Biol 26:442–448PubMedCrossRef Heeren J, Beisiegel U, Grewal T (2006) Apolipoprotein E recycling: implications for dyslipidemia and atherosclerosis. Arterioscler Thromb Vasc Biol 26:442–448PubMedCrossRef
44.
go back to reference Henry-Feugeas MC (2007) MRI of the ‘Alzheimer syndrome’. J Neuroradiol 34:220–227PubMed Henry-Feugeas MC (2007) MRI of the ‘Alzheimer syndrome’. J Neuroradiol 34:220–227PubMed
45.
go back to reference Herzig MC, Winkler DT, Burgermeister P, Pfeifer M, Kohler E, Schmidt SD, Danner S, Abramowski D, Sturchler-Pierrat C, Burki K, van Duinen SG, Maat-Schieman ML, Staufenbiel M, Mathews PM, Jucker M (2004) Abeta is targeted to the vasculature in a mouse model of hereditary cerebral hemorrhage with amyloidosis. Nat Neurosci 7:954–960PubMedCrossRef Herzig MC, Winkler DT, Burgermeister P, Pfeifer M, Kohler E, Schmidt SD, Danner S, Abramowski D, Sturchler-Pierrat C, Burki K, van Duinen SG, Maat-Schieman ML, Staufenbiel M, Mathews PM, Jucker M (2004) Abeta is targeted to the vasculature in a mouse model of hereditary cerebral hemorrhage with amyloidosis. Nat Neurosci 7:954–960PubMedCrossRef
46.
go back to reference Heverin M, Bogdanovic N, Lutjohann D, Bayer T, Pikuleva I, Bretillon L, Diczfalusy U, Winblad B, Bjorkhem I (2004) Changes in the levels of cerebral and extracerebral sterols in the brain of patients with Alzheimer’s disease. J Lipid Res 45:186–193PubMedCrossRef Heverin M, Bogdanovic N, Lutjohann D, Bayer T, Pikuleva I, Bretillon L, Diczfalusy U, Winblad B, Bjorkhem I (2004) Changes in the levels of cerebral and extracerebral sterols in the brain of patients with Alzheimer’s disease. J Lipid Res 45:186–193PubMedCrossRef
47.
go back to reference Hogervorst E, Ribeiro HM, Molyneux A, Budge M, Smith AD (2002) Plasma homocysteine levels, cerebrovascular risk factors, and cerebral white matter changes (leukoaraiosis) in patients with Alzheimer disease. Arch Neurol 59:787–793PubMedCrossRef Hogervorst E, Ribeiro HM, Molyneux A, Budge M, Smith AD (2002) Plasma homocysteine levels, cerebrovascular risk factors, and cerebral white matter changes (leukoaraiosis) in patients with Alzheimer disease. Arch Neurol 59:787–793PubMedCrossRef
48.
go back to reference Ince PG (2005) Acquired forms of vascular dementia. In: Kalimo H (ed) Cerebrovascular diseases. ISN Neuropath Press, Basel, pp 316–323 Ince PG (2005) Acquired forms of vascular dementia. In: Kalimo H (ed) Cerebrovascular diseases. ISN Neuropath Press, Basel, pp 316–323
49.
go back to reference Jackson C, Sudlow C (2005) Are lacunar strokes really different? A systematic review of differences in risk factor profiles between lacunar and nonlacunar infarcts. Stroke 36:891–901PubMedCrossRef Jackson C, Sudlow C (2005) Are lacunar strokes really different? A systematic review of differences in risk factor profiles between lacunar and nonlacunar infarcts. Stroke 36:891–901PubMedCrossRef
50.
51.
go back to reference Jellinger KA (2002) Alzheimer disease and cerebrovascular pathology: an update. J Neural Transm 109:813–836PubMedCrossRef Jellinger KA (2002) Alzheimer disease and cerebrovascular pathology: an update. J Neural Transm 109:813–836PubMedCrossRef
52.
go back to reference Jellinger KA (2007) The enigma of vascular cognitive disorder and vascular dementia. Acta Neuropathol 113:349–388PubMedCrossRef Jellinger KA (2007) The enigma of vascular cognitive disorder and vascular dementia. Acta Neuropathol 113:349–388PubMedCrossRef
53.
go back to reference Jellinger KA (2008) Morphologic diagnosis of “vascular dementia”—a critical update. J Neurol Sci 270:1–12PubMedCrossRef Jellinger KA (2008) Morphologic diagnosis of “vascular dementia”—a critical update. J Neurol Sci 270:1–12PubMedCrossRef
54.
go back to reference Jeong JH, Yoon SJ, Kang SJ, Choi KG, Na DL (2002) Hypertensive pontine microhemorrhage. Stroke 33:925–929PubMedCrossRef Jeong JH, Yoon SJ, Kang SJ, Choi KG, Na DL (2002) Hypertensive pontine microhemorrhage. Stroke 33:925–929PubMedCrossRef
55.
go back to reference Joachim CL, Morris JH, Selkoe DJ (1988) Clinically diagnosed Alzheimer’s disease: autopsy results in 150 cases. Ann Neurol 24:50–56PubMedCrossRef Joachim CL, Morris JH, Selkoe DJ (1988) Clinically diagnosed Alzheimer’s disease: autopsy results in 150 cases. Ann Neurol 24:50–56PubMedCrossRef
56.
go back to reference Johnson MW, Hammond RR, Vinters HV (2005) Fusiform, infectious and other aneurysmal lesions. In: Kalimo H (ed) Cerebrovascular diseases. ISN Neuropath Press, Basel, pp 112–118 Johnson MW, Hammond RR, Vinters HV (2005) Fusiform, infectious and other aneurysmal lesions. In: Kalimo H (ed) Cerebrovascular diseases. ISN Neuropath Press, Basel, pp 112–118
57.
go back to reference Jorgensen L, Torvik A (1969) Ischaemic cerebrovascular diseases in an autopsy series. 2. Prevalence, location, pathogenesis, and clinical course of cerebral infarcts. J Neurol Sci 9:285–320PubMedCrossRef Jorgensen L, Torvik A (1969) Ischaemic cerebrovascular diseases in an autopsy series. 2. Prevalence, location, pathogenesis, and clinical course of cerebral infarcts. J Neurol Sci 9:285–320PubMedCrossRef
58.
go back to reference Kalaria RN, Erkinjuntti T (2006) Small vessel disease and subcortical vascular dementia. J Clin Neurol 2:1–11CrossRef Kalaria RN, Erkinjuntti T (2006) Small vessel disease and subcortical vascular dementia. J Clin Neurol 2:1–11CrossRef
59.
go back to reference Kawamura J, Meyer JS, Terayama Y, Weathers S (1991) Leukoaraiosis correlates with cerebral hypoperfusion in vascular dementia. Stroke 22:609–614PubMed Kawamura J, Meyer JS, Terayama Y, Weathers S (1991) Leukoaraiosis correlates with cerebral hypoperfusion in vascular dementia. Stroke 22:609–614PubMed
60.
go back to reference Kida S, Pantazis A, Weller RO (1993) CSF drains directly from the subarachnoid space into nasal lymphatics in the rat. Anatomy, histology and immunological significance. Neuropathol Appl Neurobiol 19:480–488PubMedCrossRef Kida S, Pantazis A, Weller RO (1993) CSF drains directly from the subarachnoid space into nasal lymphatics in the rat. Anatomy, histology and immunological significance. Neuropathol Appl Neurobiol 19:480–488PubMedCrossRef
61.
go back to reference Kimberly WT, Gilson A, Rost NS, Rosand J, Viswanathan A, Smith EE, Greenberg SM (2009) Silent ischemic infarcts are associated with hemorrhage burden in cerebral amyloid angiopathy. Neurology 72:1230–1235PubMedCrossRef Kimberly WT, Gilson A, Rost NS, Rosand J, Viswanathan A, Smith EE, Greenberg SM (2009) Silent ischemic infarcts are associated with hemorrhage burden in cerebral amyloid angiopathy. Neurology 72:1230–1235PubMedCrossRef
62.
go back to reference Kinnecom C, Lev MH, Wendell L, Smith EE, Rosand J, Frosch MP, Greenberg SM (2007) Course of cerebral amyloid angiopathy-related inflammation. Neurology 68:1411–1416PubMedCrossRef Kinnecom C, Lev MH, Wendell L, Smith EE, Rosand J, Frosch MP, Greenberg SM (2007) Course of cerebral amyloid angiopathy-related inflammation. Neurology 68:1411–1416PubMedCrossRef
63.
go back to reference Koennecke HC (2006) Cerebral microbleeds on MRI: prevalence, associations, and potential clinical implications. Neurology 66:165–171PubMedCrossRef Koennecke HC (2006) Cerebral microbleeds on MRI: prevalence, associations, and potential clinical implications. Neurology 66:165–171PubMedCrossRef
64.
go back to reference Kolovou G, Yiannakouris N, Hatzivassiliou M, Malakos J, Daskalova D, Hatzigeorgiou G, Cariolou MA, Cokkinos DV (2002) Association of apolipoprotein E polymorphism with myocardial infarction in Greek patients with coronary artery disease. Curr Med Res Opin 18:118–124PubMedCrossRef Kolovou G, Yiannakouris N, Hatzivassiliou M, Malakos J, Daskalova D, Hatzigeorgiou G, Cariolou MA, Cokkinos DV (2002) Association of apolipoprotein E polymorphism with myocardial infarction in Greek patients with coronary artery disease. Curr Med Res Opin 18:118–124PubMedCrossRef
65.
go back to reference Kölsch H, Larionov S, Dedeck O, Orantes M, Birkenmeier G, Griffin WS, Thal DR (2007) Association of the glutathione S-transferase omega-1 Ala140Asp polymorphism with cerebrovascular atherosclerosis and plaque-associated interleukin-1 alpha expression. Stroke 38:2847–2850PubMedCrossRef Kölsch H, Larionov S, Dedeck O, Orantes M, Birkenmeier G, Griffin WS, Thal DR (2007) Association of the glutathione S-transferase omega-1 Ala140Asp polymorphism with cerebrovascular atherosclerosis and plaque-associated interleukin-1 alpha expression. Stroke 38:2847–2850PubMedCrossRef
66.
go back to reference Kovanen PT (2005) Pathogenesis of carotid atherosclerosis: molecular and genetic aspects. In: Kalimo H (ed) Pathology and genetics: cerebrovascular diseases. ISN Neuropath Press, Basel, pp 74–84 Kovanen PT (2005) Pathogenesis of carotid atherosclerosis: molecular and genetic aspects. In: Kalimo H (ed) Pathology and genetics: cerebrovascular diseases. ISN Neuropath Press, Basel, pp 74–84
67.
go back to reference Lammie AG (2005) Small vessel disease. In: Kalimo H (ed) Cerebrovascular diseases. ISN Neuropath Press, Basel, pp 85–91 Lammie AG (2005) Small vessel disease. In: Kalimo H (ed) Cerebrovascular diseases. ISN Neuropath Press, Basel, pp 85–91
68.
go back to reference Lammie GA (2002) Hypertensive cerebral small vessel disease and stroke. Brain Pathol 12:358–370PubMed Lammie GA (2002) Hypertensive cerebral small vessel disease and stroke. Brain Pathol 12:358–370PubMed
69.
go back to reference Lammie GA, Brannan F, Slattery J, Warlow C (1997) Nonhypertensive cerebral small-vessel disease. An autopsy study. Stroke 28:2222–2229PubMed Lammie GA, Brannan F, Slattery J, Warlow C (1997) Nonhypertensive cerebral small-vessel disease. An autopsy study. Stroke 28:2222–2229PubMed
70.
go back to reference Larionov S, Dedeck O, Birkenmeier G, Orantes M, Ghebremedhin E, Thal DR (2006) The intronic deletion polymorphism of the a2-macroglobulin gene modulates the severity and extent of atherosclerosis in the circle of Willis. Neuropathol Appl Neurobiol 32:451–454PubMedCrossRef Larionov S, Dedeck O, Birkenmeier G, Orantes M, Ghebremedhin E, Thal DR (2006) The intronic deletion polymorphism of the a2-macroglobulin gene modulates the severity and extent of atherosclerosis in the circle of Willis. Neuropathol Appl Neurobiol 32:451–454PubMedCrossRef
71.
go back to reference Larionov S, Dedeck O, Birkenmeier G, Thal DR (2007) Expression of alpha(2)-macroglobulin, neutrophil elastase, and interleukin-1alpha differs in early-stage and late-stage atherosclerotic lesions in the arteries of the circle of Willis. Acta Neuropathol (Berl) 113:33–43CrossRef Larionov S, Dedeck O, Birkenmeier G, Thal DR (2007) Expression of alpha(2)-macroglobulin, neutrophil elastase, and interleukin-1alpha differs in early-stage and late-stage atherosclerotic lesions in the arteries of the circle of Willis. Acta Neuropathol (Berl) 113:33–43CrossRef
72.
go back to reference Liang J, Liu E, Yu Y, Kitajima S, Koike T, Jin Y, Morimoto M, Hatakeyama K, Asada Y, Watanabe T, Sasaguri Y, Watanabe S, Fan J (2006) Macrophage metalloelastase accelerates the progression of atherosclerosis in transgenic rabbits. Circulation 113:1993–2001PubMedCrossRef Liang J, Liu E, Yu Y, Kitajima S, Koike T, Jin Y, Morimoto M, Hatakeyama K, Asada Y, Watanabe T, Sasaguri Y, Watanabe S, Fan J (2006) Macrophage metalloelastase accelerates the progression of atherosclerosis in transgenic rabbits. Circulation 113:1993–2001PubMedCrossRef
73.
go back to reference Liberato B, Chong JY, Sacco RL (2005) Focal brain ischemia. Clinical features, epidemiology, risk factors and outcome. In: Kalimo H (ed) Cerebrovascular diseases. ISN Neuropath Press, Basel, pp 176–185 Liberato B, Chong JY, Sacco RL (2005) Focal brain ischemia. Clinical features, epidemiology, risk factors and outcome. In: Kalimo H (ed) Cerebrovascular diseases. ISN Neuropath Press, Basel, pp 176–185
74.
go back to reference Lindley RI, Wang JJ, Wong MC, Mitchell P, Liew G, Hand P, Wardlaw J, De Silva DA, Baker M, Rochtchina E, Chen C, Hankey GJ, Chang HM, Fung VS, Gomes L, Wong TY (2009) Retinal microvasculature in acute lacunar stroke: a cross-sectional study. Lancet Neurol 8:628–634PubMedCrossRef Lindley RI, Wang JJ, Wong MC, Mitchell P, Liew G, Hand P, Wardlaw J, De Silva DA, Baker M, Rochtchina E, Chen C, Hankey GJ, Chang HM, Fung VS, Gomes L, Wong TY (2009) Retinal microvasculature in acute lacunar stroke: a cross-sectional study. Lancet Neurol 8:628–634PubMedCrossRef
75.
go back to reference Liu S, Ma J, Ridker PM, Breslow JL, Stampfer MJ (2003) A prospective study of the association between APOE genotype and the risk of myocardial infarction among apparently healthy men. Atherosclerosis 166:323–329PubMedCrossRef Liu S, Ma J, Ridker PM, Breslow JL, Stampfer MJ (2003) A prospective study of the association between APOE genotype and the risk of myocardial infarction among apparently healthy men. Atherosclerosis 166:323–329PubMedCrossRef
76.
go back to reference Lusis AJ, Mar R, Pajukanta P (2004) Genetics of atherosclerosis. Annu Rev Genom Hum Genet 5:189–218CrossRef Lusis AJ, Mar R, Pajukanta P (2004) Genetics of atherosclerosis. Annu Rev Genom Hum Genet 5:189–218CrossRef
77.
go back to reference Mahley RW (1988) Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 240:622–630PubMedCrossRef Mahley RW (1988) Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 240:622–630PubMedCrossRef
78.
go back to reference Mandybur TI (1979) Cerebral amyloid angiopathy: possible relationship to rheumatoid vasculitis. Neurology 29:1336–1340PubMed Mandybur TI (1979) Cerebral amyloid angiopathy: possible relationship to rheumatoid vasculitis. Neurology 29:1336–1340PubMed
79.
go back to reference Mandybur TI (1986) Cerebral amyloid angiopathy: the vascular pathology and complications. J Neuropathol Exp Neurol 45:79–90PubMedCrossRef Mandybur TI (1986) Cerebral amyloid angiopathy: the vascular pathology and complications. J Neuropathol Exp Neurol 45:79–90PubMedCrossRef
80.
go back to reference Markus HS, Hunt B, Palmer K, Enzinger C, Schmidt H, Schmidt R (2005) Markers of endothelial and hemostatic activation and progression of cerebral white matter hyperintensities: longitudinal results of the Austrian Stroke Prevention Study. Stroke 36:1410–1414PubMedCrossRef Markus HS, Hunt B, Palmer K, Enzinger C, Schmidt H, Schmidt R (2005) Markers of endothelial and hemostatic activation and progression of cerebral white matter hyperintensities: longitudinal results of the Austrian Stroke Prevention Study. Stroke 36:1410–1414PubMedCrossRef
81.
82.
go back to reference Masumura M, Hata R, Akatsu H, Kosaka K, Yamamoto T, Nagai Y, Sawada T (2001) Increasing in situ nick end labeling of oligodendrocytes in white matter of patients with Binswanger’s disease. J Stroke Cerebrovasc Dis 10:55–62PubMedCrossRef Masumura M, Hata R, Akatsu H, Kosaka K, Yamamoto T, Nagai Y, Sawada T (2001) Increasing in situ nick end labeling of oligodendrocytes in white matter of patients with Binswanger’s disease. J Stroke Cerebrovasc Dis 10:55–62PubMedCrossRef
83.
go back to reference Masumura M, Hata R, Uetsuki T, Nishimura I, Nagai Y, Sawada T (2001) In vivo gene transfer to cerebral white matter lesions with a recombinant adenovirus vector. Biochem Biophys Res Commun 287:440–444PubMedCrossRef Masumura M, Hata R, Uetsuki T, Nishimura I, Nagai Y, Sawada T (2001) In vivo gene transfer to cerebral white matter lesions with a recombinant adenovirus vector. Biochem Biophys Res Commun 287:440–444PubMedCrossRef
84.
go back to reference Matsusue E, Sugihara S, Fujii S, Ohama E, Kinoshita T, Ogawa T (2006) White matter changes in elderly people: MR-pathologic correlations. Magn Reson Med Sci 5:99–104PubMedCrossRef Matsusue E, Sugihara S, Fujii S, Ohama E, Kinoshita T, Ogawa T (2006) White matter changes in elderly people: MR-pathologic correlations. Magn Reson Med Sci 5:99–104PubMedCrossRef
85.
go back to reference Mazur-Kolecka B, Dickson D, Frackowiak J (2006) Induction of vascular amyloidosis-beta by oxidative stress depends on APOE genotype. Neurobiol Aging 27:804–814PubMedCrossRef Mazur-Kolecka B, Dickson D, Frackowiak J (2006) Induction of vascular amyloidosis-beta by oxidative stress depends on APOE genotype. Neurobiol Aging 27:804–814PubMedCrossRef
86.
go back to reference Mazur-Kolecka B, Frackowiak J, Carroll RT, Wisniewski HM (1997) Accumulation of Alzheimer amyloid-beta peptide in cultured myocytes is enhanced by serum and reduced by cerebrospinal fluid. J Neuropathol Exp Neurol 56:263–272PubMedCrossRef Mazur-Kolecka B, Frackowiak J, Carroll RT, Wisniewski HM (1997) Accumulation of Alzheimer amyloid-beta peptide in cultured myocytes is enhanced by serum and reduced by cerebrospinal fluid. J Neuropathol Exp Neurol 56:263–272PubMedCrossRef
87.
go back to reference McCarron MO, Cohen N, Nicoll JAR (2005) Parenchymal brain hemorrhage. In: Kalimo H (ed) Cerebrovascular diseases. ISN Neuropath Press, Basel, pp 294–300 McCarron MO, Cohen N, Nicoll JAR (2005) Parenchymal brain hemorrhage. In: Kalimo H (ed) Cerebrovascular diseases. ISN Neuropath Press, Basel, pp 294–300
88.
go back to reference McCarron MO, Nicoll JA, Stewart J, Ironside JW, Mann DM, Love S, Graham DI, Dewar D (1999) The apolipoprotein E epsilon2 allele and the pathological features in cerebral amyloid angiopathy-related hemorrhage. J Neuropathol Exp Neurol 58:711–718PubMedCrossRef McCarron MO, Nicoll JA, Stewart J, Ironside JW, Mann DM, Love S, Graham DI, Dewar D (1999) The apolipoprotein E epsilon2 allele and the pathological features in cerebral amyloid angiopathy-related hemorrhage. J Neuropathol Exp Neurol 58:711–718PubMedCrossRef
89.
go back to reference Meyer-Luehmann M, Stalder M, Herzig MC, Kaeser SA, Kohler E, Pfeifer M, Boncristiano S, Mathews PM, Mercken M, Abramowski D, Staufenbiel M, Jucker M (2003) Extracellular amyloid formation and associated pathology in neural grafts. Nat Neurosci 6:370–377PubMedCrossRef Meyer-Luehmann M, Stalder M, Herzig MC, Kaeser SA, Kohler E, Pfeifer M, Boncristiano S, Mathews PM, Mercken M, Abramowski D, Staufenbiel M, Jucker M (2003) Extracellular amyloid formation and associated pathology in neural grafts. Nat Neurosci 6:370–377PubMedCrossRef
90.
go back to reference Mitchell RN, Cotran RS (2003) Hemodynamic disorders, thrombosis, and shock. In: Kumar V, Cotran RS, Robbins SL (eds) Robbins basic pathology. Saunders, Philadelphia Mitchell RN, Cotran RS (2003) Hemodynamic disorders, thrombosis, and shock. In: Kumar V, Cotran RS, Robbins SL (eds) Robbins basic pathology. Saunders, Philadelphia
91.
go back to reference Nag S (1996) Immunohistochemical localization of extracellular matrix proteins in cerebral vessels in chronic hypertension. J Neuropathol Exp Neurol 55:381–388PubMedCrossRef Nag S (1996) Immunohistochemical localization of extracellular matrix proteins in cerebral vessels in chronic hypertension. J Neuropathol Exp Neurol 55:381–388PubMedCrossRef
92.
go back to reference Nag S, Robertson DM, Dinsdale HB (1980) Morphological changes in spontaneously hypertensive rats. Acta Neuropathol 52:27–34PubMedCrossRef Nag S, Robertson DM, Dinsdale HB (1980) Morphological changes in spontaneously hypertensive rats. Acta Neuropathol 52:27–34PubMedCrossRef
93.
go back to reference Namba Y, Tomonaga M, Kawasaki H, Otomo E, Ikeda K (1991) Apolipoprotein E immunoreactivity in cerebral amyloid deposits and neurofibrillary tangles in Alzheimer’s disease and kuru plaque amyloid in Creutzfeldt-Jakob disease. Brain Res 541:163–166PubMedCrossRef Namba Y, Tomonaga M, Kawasaki H, Otomo E, Ikeda K (1991) Apolipoprotein E immunoreactivity in cerebral amyloid deposits and neurofibrillary tangles in Alzheimer’s disease and kuru plaque amyloid in Creutzfeldt-Jakob disease. Brain Res 541:163–166PubMedCrossRef
94.
go back to reference Neve RL, Finch EA, Dawes LR (1988) Expression of the Alzheimer amyloid precursor gene transcripts in the human brain. Neuron 1:669–677PubMedCrossRef Neve RL, Finch EA, Dawes LR (1988) Expression of the Alzheimer amyloid precursor gene transcripts in the human brain. Neuron 1:669–677PubMedCrossRef
95.
go back to reference Nicoll JA, Burnett C, Love S, Graham DI, Ironside JW, Vinters HV (1996) High frequency of apolipoprotein E epsilon 2 in patients with cerebral hemorrhage due to cerebral amyloid angiopathy. Ann Neurol 39:682–683PubMedCrossRef Nicoll JA, Burnett C, Love S, Graham DI, Ironside JW, Vinters HV (1996) High frequency of apolipoprotein E epsilon 2 in patients with cerebral hemorrhage due to cerebral amyloid angiopathy. Ann Neurol 39:682–683PubMedCrossRef
96.
go back to reference O’Brien JT, Erkinjuntti T, Reisberg B, Roman G, Sawada T, Pantoni L, Bowler JV, Ballard C, DeCarli C, Gorelick PB, Rockwood K, Burns A, Gauthier S, DeKosky ST (2003) Vascular cognitive impairment. Lancet Neurol 2:89–98PubMedCrossRef O’Brien JT, Erkinjuntti T, Reisberg B, Roman G, Sawada T, Pantoni L, Bowler JV, Ballard C, DeCarli C, Gorelick PB, Rockwood K, Burns A, Gauthier S, DeKosky ST (2003) Vascular cognitive impairment. Lancet Neurol 2:89–98PubMedCrossRef
97.
go back to reference O’Donnell HC, Rosand J, Knudsen KA, Furie KL, Segal AZ, Chiu RI, Ikeda D, Greenberg SM (2000) Apolipoprotein E genotype and the risk of recurrent lobar intracerebral hemorrhage. N Engl J Med 342:240–245PubMedCrossRef O’Donnell HC, Rosand J, Knudsen KA, Furie KL, Segal AZ, Chiu RI, Ikeda D, Greenberg SM (2000) Apolipoprotein E genotype and the risk of recurrent lobar intracerebral hemorrhage. N Engl J Med 342:240–245PubMedCrossRef
98.
go back to reference O’Sullivan M, Lythgoe DJ, Pereira AC, Summers PE, Jarosz JM, Williams SC, Markus HS (2002) Patterns of cerebral blood flow reduction in patients with ischemic leukoaraiosis. Neurology 59:321–326PubMedCrossRef O’Sullivan M, Lythgoe DJ, Pereira AC, Summers PE, Jarosz JM, Williams SC, Markus HS (2002) Patterns of cerebral blood flow reduction in patients with ischemic leukoaraiosis. Neurology 59:321–326PubMedCrossRef
99.
go back to reference Okamoto Y, Ihara M, Fujita Y, Ito H, Takahashi R, Tomimoto H (2009) Cortical microinfarcts in Alzheimer’s disease and subcortical vascular dementia. Neuroreport 20:990–996PubMedCrossRef Okamoto Y, Ihara M, Fujita Y, Ito H, Takahashi R, Tomimoto H (2009) Cortical microinfarcts in Alzheimer’s disease and subcortical vascular dementia. Neuroreport 20:990–996PubMedCrossRef
100.
go back to reference Olichney JM, Hansen LA, Hofstetter CR, Lee JH, Katzman R, Thal LJ (2000) Association between severe cerebral amyloid angiopathy and cerebrovascular lesions in Alzheimer disease is not a spurious one attributable to apolipoprotein E4. Arch Neurol 57:869–874PubMedCrossRef Olichney JM, Hansen LA, Hofstetter CR, Lee JH, Katzman R, Thal LJ (2000) Association between severe cerebral amyloid angiopathy and cerebrovascular lesions in Alzheimer disease is not a spurious one attributable to apolipoprotein E4. Arch Neurol 57:869–874PubMedCrossRef
101.
go back to reference Pantoni L, Garcia JH (1997) Pathogenesis of leukoaraiosis: a review. Stroke 28:652–659PubMed Pantoni L, Garcia JH (1997) Pathogenesis of leukoaraiosis: a review. Stroke 28:652–659PubMed
102.
go back to reference Petito CK (2005) The neuropathology of focal brain ischemia. In: Kalimo H (ed) Cerebrovascular diseases. ISN Neuropath Press, Basel, pp 215–221 Petito CK (2005) The neuropathology of focal brain ischemia. In: Kalimo H (ed) Cerebrovascular diseases. ISN Neuropath Press, Basel, pp 215–221
103.
go back to reference Premkumar DR, Cohen DL, Hedera P, Friedland RP, Kalaria RN (1996) Apolipoprotein E-epsilon4 alleles in cerebral amyloid angiopathy and cerebrovascular pathology associated with Alzheimer’s disease. Am J Pathol 148:2083–2095PubMed Premkumar DR, Cohen DL, Hedera P, Friedland RP, Kalaria RN (1996) Apolipoprotein E-epsilon4 alleles in cerebral amyloid angiopathy and cerebrovascular pathology associated with Alzheimer’s disease. Am J Pathol 148:2083–2095PubMed
104.
go back to reference Price JL, Davis PB, Morris JC, White DL (1991) The distribution of tangles, plaques and related immunohistochemical markers in healthy aging and Alzheimer’s disease. Neurobiol Aging 12:295–312PubMedCrossRef Price JL, Davis PB, Morris JC, White DL (1991) The distribution of tangles, plaques and related immunohistochemical markers in healthy aging and Alzheimer’s disease. Neurobiol Aging 12:295–312PubMedCrossRef
105.
go back to reference Prins ND, van Dijk EJ, den Heijer T, Vermeer SE, Koudstaal PJ, Oudkerk M, Hofman A, Breteler MM (2004) Cerebral white matter lesions and the risk of dementia. Arch Neurol 61:1531–1534PubMedCrossRef Prins ND, van Dijk EJ, den Heijer T, Vermeer SE, Koudstaal PJ, Oudkerk M, Hofman A, Breteler MM (2004) Cerebral white matter lesions and the risk of dementia. Arch Neurol 61:1531–1534PubMedCrossRef
106.
go back to reference Rebeck GW, Reiter JS, Strickland DK, Hyman BT (1993) Apolipoprotein E in sporadic Alzheimer’s disease: allelic variation and receptor interactions. Neuron 11:575–580PubMedCrossRef Rebeck GW, Reiter JS, Strickland DK, Hyman BT (1993) Apolipoprotein E in sporadic Alzheimer’s disease: allelic variation and receptor interactions. Neuron 11:575–580PubMedCrossRef
107.
go back to reference Reid AH, Maloney AF (1974) Giant cell arteritis and arteriolitis associated with amyloid angiopathy in an elderly mongol. Acta Neuropathol (Berl) 27:131–137CrossRef Reid AH, Maloney AF (1974) Giant cell arteritis and arteriolitis associated with amyloid angiopathy in an elderly mongol. Acta Neuropathol (Berl) 27:131–137CrossRef
108.
go back to reference Revesz T, Holton JL, Lashley T, Plant G, Frangione B, Rostagno A, Ghiso J (2009) Genetics and molecular pathogenesis of sporadic and hereditary cerebral amyloid angiopathies. Acta Neuropathol 118:115–130PubMedCrossRef Revesz T, Holton JL, Lashley T, Plant G, Frangione B, Rostagno A, Ghiso J (2009) Genetics and molecular pathogenesis of sporadic and hereditary cerebral amyloid angiopathies. Acta Neuropathol 118:115–130PubMedCrossRef
109.
go back to reference Roher AE, Esh C, Kokjohn TA, Kalback W, Luehrs DC, Seward JD, Sue LI, Beach TG (2003) Circle of Willis atherosclerosis is a risk factor for sporadic Alzheimer’s disease. Arterioscler Thromb Vasc Biol 23:2055–2062PubMedCrossRef Roher AE, Esh C, Kokjohn TA, Kalback W, Luehrs DC, Seward JD, Sue LI, Beach TG (2003) Circle of Willis atherosclerosis is a risk factor for sporadic Alzheimer’s disease. Arterioscler Thromb Vasc Biol 23:2055–2062PubMedCrossRef
110.
go back to reference Roher AE, Lowenson JD, Clarke S, Woods AS, Cotter RJ, Gowing E, Ball MJ (1993) Beta-amyloid-(1–42) is a major component of cerebrovascular amyloid deposits: implications for the pathology of Alzheimer disease. Proc Natl Acad Sci USA 90:10836–10840PubMedCrossRef Roher AE, Lowenson JD, Clarke S, Woods AS, Cotter RJ, Gowing E, Ball MJ (1993) Beta-amyloid-(1–42) is a major component of cerebrovascular amyloid deposits: implications for the pathology of Alzheimer disease. Proc Natl Acad Sci USA 90:10836–10840PubMedCrossRef
111.
go back to reference Roman GC (2002) On the history of lacunes, etat crible, and the white matter lesions of vascular dementia. Cerebrovasc Dis 13(Suppl 2):1–6PubMed Roman GC (2002) On the history of lacunes, etat crible, and the white matter lesions of vascular dementia. Cerebrovasc Dis 13(Suppl 2):1–6PubMed
112.
go back to reference Roman GC (2004) Brain hypoperfusion: a critical factor in vascular dementia. Neurol Res 26:454–458PubMedCrossRef Roman GC (2004) Brain hypoperfusion: a critical factor in vascular dementia. Neurol Res 26:454–458PubMedCrossRef
113.
go back to reference Rosenberg GA, Kornfeld M, Stovring J, Bicknell JM (1979) Subcortical arteriosclerotic encephalopathy (Binswanger): computerized tomography. Neurology 29:1102–1106PubMed Rosenberg GA, Kornfeld M, Stovring J, Bicknell JM (1979) Subcortical arteriosclerotic encephalopathy (Binswanger): computerized tomography. Neurology 29:1102–1106PubMed
114.
go back to reference Sawada H, Udaka F, Izumi Y, Nishinaka K, Kawakami H, Nakamura S, Kameyama M (2000) Cerebral white matter lesions are not associated with apoE genotype but with age and female sex in Alzheimer’s disease. J Neurol Neurosurg Psychiatry 68:653–656PubMedCrossRef Sawada H, Udaka F, Izumi Y, Nishinaka K, Kawakami H, Nakamura S, Kameyama M (2000) Cerebral white matter lesions are not associated with apoE genotype but with age and female sex in Alzheimer’s disease. J Neurol Neurosurg Psychiatry 68:653–656PubMedCrossRef
115.
go back to reference Schmechel DE, Saunders AM, Strittmatter WJ, Crain BJ, Hulette CM, Joo SH, Pericak-Vance MA, Goldgaber D, Roses AD (1993) Increased amyloid beta-peptide deposition in cerebral cortex as a consequence of apolipoprotein E genotype in late-onset Alzheimer disease. Proc Natl Acad Sci USA 90:9649–9653PubMedCrossRef Schmechel DE, Saunders AM, Strittmatter WJ, Crain BJ, Hulette CM, Joo SH, Pericak-Vance MA, Goldgaber D, Roses AD (1993) Increased amyloid beta-peptide deposition in cerebral cortex as a consequence of apolipoprotein E genotype in late-onset Alzheimer disease. Proc Natl Acad Sci USA 90:9649–9653PubMedCrossRef
116.
go back to reference Singh PP, Singh M, Bhatnagar DP, Kaur TP, Gaur SK (2008) Apolipoprotein E polymorphism and its relation to plasma lipids in coronary heart disease. Indian J Med Sci 62:105–112PubMedCrossRef Singh PP, Singh M, Bhatnagar DP, Kaur TP, Gaur SK (2008) Apolipoprotein E polymorphism and its relation to plasma lipids in coronary heart disease. Indian J Med Sci 62:105–112PubMedCrossRef
117.
go back to reference Smith EB (1977) Molecular interactions in human atherosclerotic plaques. Am J Pathol 86:665–674PubMed Smith EB (1977) Molecular interactions in human atherosclerotic plaques. Am J Pathol 86:665–674PubMed
118.
go back to reference Soontornniyomkij V, Lynch MD, Mermash S, Pomakian J, Badkoobehi H, Clare R, Vinters HV (2009) Cerebral microinfarcts associated with severe cerebral beta-amyloid angiopathy. Brain Pathol 20:459–467CrossRef Soontornniyomkij V, Lynch MD, Mermash S, Pomakian J, Badkoobehi H, Clare R, Vinters HV (2009) Cerebral microinfarcts associated with severe cerebral beta-amyloid angiopathy. Brain Pathol 20:459–467CrossRef
119.
go back to reference Stary HC (2000) Natural history and histological classification of atherosclerotic lesions: an update. Arterioscler Thromb Vasc Biol 20:1177–1178PubMed Stary HC (2000) Natural history and histological classification of atherosclerotic lesions: an update. Arterioscler Thromb Vasc Biol 20:1177–1178PubMed
120.
go back to reference Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W Jr, Rosenfeld ME, Schwartz CJ, Wagner WD, Wissler RW (1995) A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Arterioscler Thromb Vasc Biol 15:1512–1531PubMed Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W Jr, Rosenfeld ME, Schwartz CJ, Wagner WD, Wissler RW (1995) A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Arterioscler Thromb Vasc Biol 15:1512–1531PubMed
121.
go back to reference Stary HC, Chandler AB, Glagov S, Guyton JR, Insull W Jr, Rosenfeld ME, Schaffer SA, Schwartz CJ, Wagner WD, Wissler RW (1994) A definition of initial, fatty streak, and intermediate lesions of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation 89:2462–2478PubMed Stary HC, Chandler AB, Glagov S, Guyton JR, Insull W Jr, Rosenfeld ME, Schaffer SA, Schwartz CJ, Wagner WD, Wissler RW (1994) A definition of initial, fatty streak, and intermediate lesions of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation 89:2462–2478PubMed
122.
go back to reference Steen RG, Miles MA, Helton KJ, Strawn S, Wang W, Xiong X, Mulhern RK (2003) Cognitive impairment in children with hemoglobin SS sickle cell disease: relationship to MR imaging findings and hematocrit. Am J Neuroradiol 24:382–389PubMed Steen RG, Miles MA, Helton KJ, Strawn S, Wang W, Xiong X, Mulhern RK (2003) Cognitive impairment in children with hemoglobin SS sickle cell disease: relationship to MR imaging findings and hematocrit. Am J Neuroradiol 24:382–389PubMed
123.
go back to reference Strittmatter WJ, Weisgraber KH, Huang DY, Dong LM, Salvesen GS, Pericak-Vance M, Schmechel D, Saunders AM, Goldgaber D, Roses AD (1993) Binding of human apolipoprotein E to synthetic amyloid beta peptide: isoform-specific effects and implications for late-onset Alzheimer disease. Proc Natl Acad Sci USA 90:8098–8102PubMedCrossRef Strittmatter WJ, Weisgraber KH, Huang DY, Dong LM, Salvesen GS, Pericak-Vance M, Schmechel D, Saunders AM, Goldgaber D, Roses AD (1993) Binding of human apolipoprotein E to synthetic amyloid beta peptide: isoform-specific effects and implications for late-onset Alzheimer disease. Proc Natl Acad Sci USA 90:8098–8102PubMedCrossRef
124.
go back to reference Sze G, De Armond SJ, Brant-Zawadzki M, Davis RL, Norman D, Newton TH (1986) Foci of MRI signal (pseudo lesions) anterior to the frontal horns: histologic correlations of a normal finding. Am J Roentgenol 147:331–337 Sze G, De Armond SJ, Brant-Zawadzki M, Davis RL, Norman D, Newton TH (1986) Foci of MRI signal (pseudo lesions) anterior to the frontal horns: histologic correlations of a normal finding. Am J Roentgenol 147:331–337
125.
go back to reference Takebayashi S, Kaneko M (1983) Electron microscopic studies of ruptured arteries in hypertensive intracerebral hemorrhage. Stroke 14:28–36PubMed Takebayashi S, Kaneko M (1983) Electron microscopic studies of ruptured arteries in hypertensive intracerebral hemorrhage. Stroke 14:28–36PubMed
126.
go back to reference Tanskanen M, Lindsberg PJ, Tienari PJ, Polvikoski T, Sulkava R, Verkkoniemi A, Rastas S, Paetau A, Kiuru-Enari S (2005) Cerebral amyloid angiopathy in a 95+ cohort: complement activation and apolipoprotein E (ApoE) genotype. Neuropathol Appl Neurobiol 31:589–599PubMedCrossRef Tanskanen M, Lindsberg PJ, Tienari PJ, Polvikoski T, Sulkava R, Verkkoniemi A, Rastas S, Paetau A, Kiuru-Enari S (2005) Cerebral amyloid angiopathy in a 95+ cohort: complement activation and apolipoprotein E (ApoE) genotype. Neuropathol Appl Neurobiol 31:589–599PubMedCrossRef
127.
go back to reference Thal DR (2009) The pre-capillary segment of the blood–brain barrier and its relation to perivascular drainage in Alzheimer’s disease and small vessel disease. Sci World J 9:557–563 Thal DR (2009) The pre-capillary segment of the blood–brain barrier and its relation to perivascular drainage in Alzheimer’s disease and small vessel disease. Sci World J 9:557–563
128.
go back to reference Thal DR, Capetillo-Zarate E, Larionov S, Staufenbiel M, Zurbruegg S, Beckmann N (2009) Capillary cerebral amyloid angiopathy is associated with vessel occlusion and cerebral blood flow disturbances. Neurobiol Aging 30:1936–1948PubMedCrossRef Thal DR, Capetillo-Zarate E, Larionov S, Staufenbiel M, Zurbruegg S, Beckmann N (2009) Capillary cerebral amyloid angiopathy is associated with vessel occlusion and cerebral blood flow disturbances. Neurobiol Aging 30:1936–1948PubMedCrossRef
129.
go back to reference Thal DR, Ghebremedhin E, Orantes M, Wiestler OD (2003) Vascular pathology in Alzheimer’s disease: correlation of cerebral amyloid angiopathy and arteriosclerosis/lipohyalinosis with cognitive decline. J Neuropathol Exp Neurol 62:1287–1301PubMed Thal DR, Ghebremedhin E, Orantes M, Wiestler OD (2003) Vascular pathology in Alzheimer’s disease: correlation of cerebral amyloid angiopathy and arteriosclerosis/lipohyalinosis with cognitive decline. J Neuropathol Exp Neurol 62:1287–1301PubMed
130.
go back to reference Thal DR, Ghebremedhin E, Rüb U, Yamaguchi H, Del Tredici K, Braak H (2002) Two types of sporadic cerebral amyloid angiopathy. J Neuropathol Exp Neurol 61:282–293PubMed Thal DR, Ghebremedhin E, Rüb U, Yamaguchi H, Del Tredici K, Braak H (2002) Two types of sporadic cerebral amyloid angiopathy. J Neuropathol Exp Neurol 61:282–293PubMed
131.
go back to reference Thal DR, Griffin WS, Braak H (2008) Parenchymal and vascular Abeta-deposition and its effects on the degeneration of neurons and cognition in Alzheimer’s disease. J Cell Mol Med 12:1848–1862PubMed Thal DR, Griffin WS, Braak H (2008) Parenchymal and vascular Abeta-deposition and its effects on the degeneration of neurons and cognition in Alzheimer’s disease. J Cell Mol Med 12:1848–1862PubMed
132.
go back to reference Thal DR, Griffin WST, De Vos RAI, Ghebremedhin E (2008) Cerebral amyloid angiopathy and its relationship to Alzheimer’s disease. Acta Neuropathol 115:599–609PubMedCrossRef Thal DR, Griffin WST, De Vos RAI, Ghebremedhin E (2008) Cerebral amyloid angiopathy and its relationship to Alzheimer’s disease. Acta Neuropathol 115:599–609PubMedCrossRef
133.
go back to reference Thal DR, Larionov S, Abramowski D, Wiederhold KH, Van Dooren T, Yamaguchi H, Haass C, Van Leuven F, Staufenbiel M, Capetillo-Zarate E (2007) Occurrence and co-localization of amyloid beta-protein and apolipoprotein E in perivascular drainage channels of wild-type and APP-transgenic mice. Neurobiol Aging 28:1221–1230PubMedCrossRef Thal DR, Larionov S, Abramowski D, Wiederhold KH, Van Dooren T, Yamaguchi H, Haass C, Van Leuven F, Staufenbiel M, Capetillo-Zarate E (2007) Occurrence and co-localization of amyloid beta-protein and apolipoprotein E in perivascular drainage channels of wild-type and APP-transgenic mice. Neurobiol Aging 28:1221–1230PubMedCrossRef
134.
go back to reference Thal DR, Rüb U, Orantes M, Braak H (2002) Phases of Abeta-deposition in the human brain and its relevance for the development of AD. Neurology 58:1791–1800PubMed Thal DR, Rüb U, Orantes M, Braak H (2002) Phases of Abeta-deposition in the human brain and its relevance for the development of AD. Neurology 58:1791–1800PubMed
135.
go back to reference The National Institute on Aging (1997) Consensus recommendations for the postmortem diagnosis of Alzheimer’s disease. The National Institute on Aging, and Reagan Institute Working Group on Diagnostic Criteria for the Neuropathological Assessment of Alzheimer’s Disease. Neurobiol Aging 18:S1–S2CrossRef The National Institute on Aging (1997) Consensus recommendations for the postmortem diagnosis of Alzheimer’s disease. The National Institute on Aging, and Reagan Institute Working Group on Diagnostic Criteria for the Neuropathological Assessment of Alzheimer’s Disease. Neurobiol Aging 18:S1–S2CrossRef
136.
go back to reference Topakian R, Barrick TR, Howe FA, Markus HS (2010) Blood–brain barrier permeability is increased in normal appearing white matter in patients with lacunar stroke and leukoaraiosis. J Neurol Neurosurg Psychiatry 81:192–197 Topakian R, Barrick TR, Howe FA, Markus HS (2010) Blood–brain barrier permeability is increased in normal appearing white matter in patients with lacunar stroke and leukoaraiosis. J Neurol Neurosurg Psychiatry 81:192–197
137.
go back to reference Ueno M, Tomimoto H, Akiguchi I, Wakita H, Sakamoto H (2002) Blood–brain barrier disruption in white matter lesions in a rat model of chronic cerebral hypoperfusion. J Cereb Blood Flow Metab 22:97–104PubMedCrossRef Ueno M, Tomimoto H, Akiguchi I, Wakita H, Sakamoto H (2002) Blood–brain barrier disruption in white matter lesions in a rat model of chronic cerebral hypoperfusion. J Cereb Blood Flow Metab 22:97–104PubMedCrossRef
138.
go back to reference Urbach H, Tschampa H, Flacke S, Thal DR (2007) MRI of vascular dementia and differential diagnoses or is it really dementia? Clin Neuroradiol 17:88–97CrossRef Urbach H, Tschampa H, Flacke S, Thal DR (2007) MRI of vascular dementia and differential diagnoses or is it really dementia? Clin Neuroradiol 17:88–97CrossRef
139.
go back to reference Utter S, Tamboli IY, Walter J, Rijal Upadhaya A, Birkenmeier G, Pietrzik CU, Ghebremedhin E, Thal DR (2008) Cerebral small vessel disease-induced apolipoprotein E leakage is associated with Alzheimer disease and the accumulation of amyloid beta-protein in perivascular astrocytes. J Neuropathol Exp Neurol 67:842–856PubMedCrossRef Utter S, Tamboli IY, Walter J, Rijal Upadhaya A, Birkenmeier G, Pietrzik CU, Ghebremedhin E, Thal DR (2008) Cerebral small vessel disease-induced apolipoprotein E leakage is associated with Alzheimer disease and the accumulation of amyloid beta-protein in perivascular astrocytes. J Neuropathol Exp Neurol 67:842–856PubMedCrossRef
140.
go back to reference van Swieten JC, van den Hout JH, van Ketel BA, Hijdra A, Wokke JH, van Gijn J (1991) Periventricular lesions in the white matter on magnetic resonance imaging in the elderly. A morphometric correlation with arteriolosclerosis and dilated perivascular spaces. Brain 114(Pt 2):761–774PubMedCrossRef van Swieten JC, van den Hout JH, van Ketel BA, Hijdra A, Wokke JH, van Gijn J (1991) Periventricular lesions in the white matter on magnetic resonance imaging in the elderly. A morphometric correlation with arteriolosclerosis and dilated perivascular spaces. Brain 114(Pt 2):761–774PubMedCrossRef
141.
go back to reference Vinters HV (1992) Cerebral amyloid angiopathy. In: Barnett HJM, Mohr JP, Stein BM, Yatsu FM (eds) Stroke. Pathophysiology, diagnosis and management. Churchill Livingstone, New York, pp 821–858 Vinters HV (1992) Cerebral amyloid angiopathy. In: Barnett HJM, Mohr JP, Stein BM, Yatsu FM (eds) Stroke. Pathophysiology, diagnosis and management. Churchill Livingstone, New York, pp 821–858
142.
go back to reference Vinters HV, Ellis WG, Zarow C, Zaias BW, Jagust WJ, Mack WJ, Chui HC (2000) Neuropathologic substrates of ischemic vascular dementia. J Neuropathol Exp Neurol 59:931–945PubMed Vinters HV, Ellis WG, Zarow C, Zaias BW, Jagust WJ, Mack WJ, Chui HC (2000) Neuropathologic substrates of ischemic vascular dementia. J Neuropathol Exp Neurol 59:931–945PubMed
143.
go back to reference Vinters HV, Gilbert JJ (1983) Cerebral amyloid angiopathy: incidence and complications in the aging brain. II. The distribution of amyloid vascular changes. Stroke 14:924–928PubMed Vinters HV, Gilbert JJ (1983) Cerebral amyloid angiopathy: incidence and complications in the aging brain. II. The distribution of amyloid vascular changes. Stroke 14:924–928PubMed
144.
go back to reference Vonsattel JP, Myers RH, Hedley-Whyte ET, Ropper AH, Bird ED, Richardson EP Jr (1991) Cerebral amyloid angiopathy without and with cerebral hemorrhages: a comparative histological study. Ann Neurol 30:637–649PubMedCrossRef Vonsattel JP, Myers RH, Hedley-Whyte ET, Ropper AH, Bird ED, Richardson EP Jr (1991) Cerebral amyloid angiopathy without and with cerebral hemorrhages: a comparative histological study. Ann Neurol 30:637–649PubMedCrossRef
145.
go back to reference Wardlaw JM, Doubal F, Armitage P, Chappell F, Carpenter T, Munoz Maniega S, Farrall A, Sudlow C, Dennis M, Dhillon B (2009) Lacunar stroke is associated with diffuse blood–brain barrier dysfunction. Ann Neurol 65:194–202PubMedCrossRef Wardlaw JM, Doubal F, Armitage P, Chappell F, Carpenter T, Munoz Maniega S, Farrall A, Sudlow C, Dennis M, Dhillon B (2009) Lacunar stroke is associated with diffuse blood–brain barrier dysfunction. Ann Neurol 65:194–202PubMedCrossRef
146.
go back to reference Weller RO, Djuanda E, Yow HY, Carare RO (2009) Lymphatic drainage of the brain and the pathophysiology of neurological disease. Acta Neuropathol 117:1–14PubMedCrossRef Weller RO, Djuanda E, Yow HY, Carare RO (2009) Lymphatic drainage of the brain and the pathophysiology of neurological disease. Acta Neuropathol 117:1–14PubMedCrossRef
147.
go back to reference Weller RO, Massey A, Newman TA, Hutchings M, Kuo YM, Roher AE (1998) Cerebral amyloid angiopathy: amyloid beta accumulates in putative interstitial fluid drainage pathways in Alzheimer’s disease. Am J Pathol 153:725–733PubMed Weller RO, Massey A, Newman TA, Hutchings M, Kuo YM, Roher AE (1998) Cerebral amyloid angiopathy: amyloid beta accumulates in putative interstitial fluid drainage pathways in Alzheimer’s disease. Am J Pathol 153:725–733PubMed
148.
go back to reference Wilcken DE, Wilcken B (1976) The pathogenesis of coronary artery disease. A possible role for methionine metabolism. J Clin Invest 57:1079–1082PubMedCrossRef Wilcken DE, Wilcken B (1976) The pathogenesis of coronary artery disease. A possible role for methionine metabolism. J Clin Invest 57:1079–1082PubMedCrossRef
149.
go back to reference Winkler DT, Bondolfi L, Herzig MC, Jann L, Calhoun ME, Wiederhold KH, Tolnay M, Staufenbiel M, Jucker M (2001) Spontaneous hemorrhagic stroke in a mouse model of cerebral amyloid angiopathy. J Neurosci 21:1619–1627PubMed Winkler DT, Bondolfi L, Herzig MC, Jann L, Calhoun ME, Wiederhold KH, Tolnay M, Staufenbiel M, Jucker M (2001) Spontaneous hemorrhagic stroke in a mouse model of cerebral amyloid angiopathy. J Neurosci 21:1619–1627PubMed
150.
go back to reference Wu CH, Chi JC, Jerng JS, Lin SJ, Jan KM, Wang DL, Chien S (1990) Transendothelial macromolecular transport in the aorta of spontaneously hypertensive rats. Hypertension 16:154–161PubMed Wu CH, Chi JC, Jerng JS, Lin SJ, Jan KM, Wang DL, Chien S (1990) Transendothelial macromolecular transport in the aorta of spontaneously hypertensive rats. Hypertension 16:154–161PubMed
151.
go back to reference Yamauchi H, Fukuda H, Oyanagi C (2002) Significance of white matter high intensity lesions as a predictor of stroke from arteriolosclerosis. J Neurol Neurosurg Psychiatry 72:576–582PubMedCrossRef Yamauchi H, Fukuda H, Oyanagi C (2002) Significance of white matter high intensity lesions as a predictor of stroke from arteriolosclerosis. J Neurol Neurosurg Psychiatry 72:576–582PubMedCrossRef
152.
go back to reference Yamauchi H, Fukuyama H, Nagahama Y, Shiozaki T, Nishizawa S, Konishi J, Shio H, Kimura J (1999) Brain arteriolosclerosis and hemodynamic disturbance may induce leukoaraiosis. Neurology 53:1833–1838PubMed Yamauchi H, Fukuyama H, Nagahama Y, Shiozaki T, Nishizawa S, Konishi J, Shio H, Kimura J (1999) Brain arteriolosclerosis and hemodynamic disturbance may induce leukoaraiosis. Neurology 53:1833–1838PubMed
153.
go back to reference Yamori Y, Horie R, Handa H, Sato M, Fukase M (1976) Pathogenetic similarity of strokes in stroke-prone spontaneously hypertensive rats and humans. Stroke 7:46–53PubMed Yamori Y, Horie R, Handa H, Sato M, Fukase M (1976) Pathogenetic similarity of strokes in stroke-prone spontaneously hypertensive rats and humans. Stroke 7:46–53PubMed
154.
go back to reference Yip AG, McKee AC, Green RC, Wells J, Young H, Cupples LA, Farrer LA (2005) APOE, vascular pathology, and the AD brain. Neurology 65:259–265PubMedCrossRef Yip AG, McKee AC, Green RC, Wells J, Young H, Cupples LA, Farrer LA (2005) APOE, vascular pathology, and the AD brain. Neurology 65:259–265PubMedCrossRef
155.
go back to reference Zhang ET, Richards HK, Kida S, Weller RO (1992) Directional and compartmentalised drainage of interstitial fluid and cerebrospinal fluid from the rat brain. Acta Neuropathol (Berl) 83:233–239CrossRef Zhang ET, Richards HK, Kida S, Weller RO (1992) Directional and compartmentalised drainage of interstitial fluid and cerebrospinal fluid from the rat brain. Acta Neuropathol (Berl) 83:233–239CrossRef
156.
go back to reference Zhang SH, Reddick RL, Piedrahita JA, Maeda N (1992) Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 258:468–471PubMedCrossRef Zhang SH, Reddick RL, Piedrahita JA, Maeda N (1992) Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 258:468–471PubMedCrossRef
157.
go back to reference Zülch KJ (1961) Über die Entstehung und Lokalisation der Hirninfarkte. Acta Neurol Chir 7:1–117 Zülch KJ (1961) Über die Entstehung und Lokalisation der Hirninfarkte. Acta Neurol Chir 7:1–117
Metadata
Title
Vascular pathology in the aged human brain
Authors
Lea Tenenholz Grinberg
Dietmar Rudolf Thal
Publication date
01-03-2010
Publisher
Springer-Verlag
Published in
Acta Neuropathologica / Issue 3/2010
Print ISSN: 0001-6322
Electronic ISSN: 1432-0533
DOI
https://doi.org/10.1007/s00401-010-0652-7

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Acta Neuropathologica 3/2010 Go to the issue

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Thanks to referees

Thanks to referees