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Clinical Aspects and Diagnostic Criteria of Sporadic CAA-Related Hemorrhage

  • Steven M. Greenberg
Chapter

Abstract

Cerebral amyloid angiopathy (CAA) is a major cause of hemorrhagic stroke in the elderly, including hemorrhages that occur with anticoagulant treatment. Though fundamentally a neuropathologic diagnosis, CAA can be identified with good reliability during life by the presence on gradient-echo MRI of multiple, strictly lobar hemorrhages without other definite cause. The relatively good recovery from a first CAA-related hemorrhage is counterbalanced by the tendency for these hemorrhages to recur at approximately 10% per year. Higher rates of recurrence are predicted by a history of previous hemorrhage and the presence of the apolipoprotein E ɛ2 and ɛ4 alleles. Improving tools for the diagnosis and staging of CAA, together with an emerging understanding of β-amyloid deposition and toxicity, form a strong foundation for future trials aimed at prevention of hemorrhage recurrence.

Keywords

Intracerebral Hemorrhage Cerebral Hemorrhage Cerebral Amyloid Angiopathy Central Nervous System Vasculitis Vascular Amyloid 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Kase, C.S., Vonsattel, J.P. and Richardson, E.P. (1988) Case Records of the Massachusetts General Hospital, case 10–1988, N. Engl. J. Med. 318, 623–631.CrossRefGoogle Scholar
  2. 2.
    DeWitt, L.D. and Louis, D.N. (1991) Case records of the Massachusetts General Hospital, case 27–1991, N. Engl. J. Med. 325, 42–54.CrossRefGoogle Scholar
  3. 3.
    Greenberg, S.M. and Edgar, M.A. (1996) Case records of the Massachusetts General Hospital, case 22–1996, N. Engl. J. Med. 335, 189–196.CrossRefGoogle Scholar
  4. 4.
    Brott, T., Thalinger, K. and Hertzberg, V. (1986) Hypertension as a risk factor for spontaneous intracerebral hemorrhage, Stroke 17, 1078–1083.PubMedCrossRefGoogle Scholar
  5. 5.
    Broderick, J.P., Brott, T., Tomsick, T., Huster, G. and Miller, R. (1992) The risk of subarachnoid and intracerebral hemorrhages in blacks as compared with whites, N. Engl. J. Med. 326, 733–736.PubMedCrossRefGoogle Scholar
  6. 6.
    Schutz, H., Bodeker, R.H., Damian, M., Krack, P. and Dorndorf, W. (1990) Age-related spontaneous intracerebral hematoma in a German community, Stroke 21, 1412–1418.PubMedCrossRefGoogle Scholar
  7. 7.
    Kase, C.S. (1994) Lobar hemorrhage, in C.S. Kase and L.R. Caplan (eds.), Intracerebral Hemorrhage, Butterworth-Heinemann, Boston, pp. 363–382.Google Scholar
  8. 8.
    Lee, S.S. and Stemmermann, G.N. (1978) Congophilic angiopathy and cerebral hemorrhage, Arch. Pathol. Lab. Med. 102, 317–321.PubMedGoogle Scholar
  9. 9.
    Itoh, Y., Yamada, M., Hayakawa, M., Otomo, E. and Miyatake, T. (1993) Cerebral amyloid angiopathy: a significant cause of cerebellar as well as lobar cerebral hemorrhage in the elderly, J. Neurol. Sci. 116, 135–141.PubMedCrossRefGoogle Scholar
  10. 10.
    Broderick, J., Brott, T., Tomsick, T. and Leach, A. (1993) Lobar hemorrhage in the elderly. The undiminishing importance of hypertension, Stroke 24, 49–51.PubMedCrossRefGoogle Scholar
  11. 11.
    Tomonaga, M. (1981) Cerebral amyloid angiopathy in the elderly, J. Am. Geriatric Soc. 29, 151–157.Google Scholar
  12. 12.
    Vinters, H.V. and Gilbert, J.J. (1983) Cerebral amyloid angiopathy: incidence and complications in the aging brain. II. The distribution of amyloid vascular changes, Stroke 14, 924–928.PubMedCrossRefGoogle Scholar
  13. 13.
    Masuda, J., Tanaka, K., Ueda, K. and Omae, T. (1988) Autopsy study of incidence and distribution of cerebral amyloid angiopathy in Hisayama, Japan, Stroke 19, 205–210.PubMedCrossRefGoogle Scholar
  14. 14.
    Greenberg, S.M. and Vonsattel, J.-P.G. (1997) Diagnosis of cerebral amyloid angiopathy. Sensitivity and specificity of cortical biopsy., Stroke 28, 1418–1422.PubMedCrossRefGoogle Scholar
  15. 15.
    Jellinger, K. (1977) Cerebrovascular amyloidosis with cerebral hemorrhage, J. Neurol. 214, 195–206.PubMedCrossRefGoogle Scholar
  16. 16.
    Vinters, H.V. (1987) Cerebral amyloid angiopathy. A critical review., Stroke 18, 311–324.PubMedCrossRefGoogle Scholar
  17. 17.
    Sytkowski, P.A., D’Agostino, R.B., Belanger, A.J. and Kannel, W.B. (1996) Secular trends in long-term sustained hypertension, long-term treatment, and cardiovascular mortality. The Framingham Heart Study 1950 to 1990, Circulation 93, 697–703.PubMedCrossRefGoogle Scholar
  18. 18.
    Ferreiro, J.A., Ansbacher, L.E. and Vinters, H.V. (1989) Stroke related to cerebral amyloid angiopathy: the significance of systemic vascular disease, J. Neurol. 236, 267272.Google Scholar
  19. 19.
    Bahemuka, M. (1987) Primary intracerebral hemorrhage and heart weight: a clinicopathologic case-control review of 218 patients, Stroke 18, 531–536.PubMedCrossRefGoogle Scholar
  20. 20.
    Massaro, A.R., Sacco, R.L., Mohr, J.P., Foulkes, M.A., Tatemichi, T.K., Price, T.R., Hier, D.B. and Wolf, P.A. (1991) Clinical discriminators of lobar and deep hemorrhages: the Stroke Data Bank, Neurology 41, 1881–1885.Google Scholar
  21. 21.
    Greenberg, S.M., Briggs, M.E., Hyman, B.T., Kokoris, G.J., Takis, C., Kanter, D.S., Kase, C.S. and Pessin, M.S. (1996) Apolipoprotein E 64 is associated with the presence and earlier onset of hemorrhage in cerebral amyloid angiopathy., Stroke 27, 1333–1337.PubMedCrossRefGoogle Scholar
  22. 22.
    Greenberg, S.M., Rebeck, G.W., Vonsattel, J.P.V., Gomez-Isla, T. and Hyman, B.T. (1995) Apolipoprotein E e4 and cerebral hemorrhage associated with amyloid angiopathy, Ann. Neurol. 38, 254–259.Google Scholar
  23. 23.
    Premkumar, D.R., Cohen, D.L., Hedera, P., Friedland, R.P. and Kalaria, R.N. (1996) Apolipoprotein E-epsilon4 alleles in cerebral amyloid angiopathy and cerebrovascular pathology associated with Alzheimer’s disease, Am. J. Pathol. 148, 2083–2095.PubMedGoogle Scholar
  24. 24.
    Nicoll, J.A., Burnett, C., Love, S., Graham, D.I., Dewar, D., Ironside, J.W., Stewart, J. and Vinters, H.V. (1997) High frequency of apolipoprotein E epsilon 2 allele in hemorrhage due to cerebral amyloid angiopathy, Ann. Neurol. 41, 716–721.Google Scholar
  25. 25.
    Greenberg, S.M., Vonsattel, J.P., Segal, A.Z., Chiu, R.I., Clatworthy, A.E., Liao, A., Hyman, B.T. and Rebeck, G.W. (1998) Association of apolipoprotein E epsilon2 and vasculopathy in cerebral amyloid angiopathy, Neurology 50, 961–965.PubMedCrossRefGoogle Scholar
  26. 26.
    Graffagnino, C., Herbstreith, M.H., Schmechel, D.E., Levy, E., Roses, A.D. and Alberts, M.J. (1995) Cystatin C mutation in an elderly man with sporadic amyloid angiopathy and intracerebral hemorrhage, Stroke 26, 2190–2193.PubMedCrossRefGoogle Scholar
  27. 27.
    Levy, E., Carman, M.D., Fernandez Madrid, I.J., Power, M.D., Lieberburg, I., van Duinen, S.G., Bots, G.T., Luyendijk, W. and Frangione, B. (1990) Mutation of the Alzheimer’s disease amyloid gene in hereditary cerebral hemorrhage, Dutch type, Science 248, 1124–1126.PubMedCrossRefGoogle Scholar
  28. 28.
    Hendriks, L., van Duijn, C.M., Cras, P., Cruts, M., Van Hul, W., van Harskamp, F., Warren, A., McInnis, M.G., Antonarakis, S.E., Martin, J.J., Hofman, A. and Van Broeckhoven, C. (1992) Presenile dementia and cerebral hemorrhage linked to a mutation at codon 692 of the beta-amyloid precursor protein gene, Nat. Genet. 1, 218–221.PubMedCrossRefGoogle Scholar
  29. 29.
    Palsdottir, A., Abrahamson, M., Thorsteinsson, L., Amason, A., Olafsson, I., Grubb, A. and Jensson, O. (1988) Mutation in cystatin C gene causes hereditary brain hemorrhage, Lancet 2, 603–604.PubMedCrossRefGoogle Scholar
  30. 30.
    Graffagnino, C., Herbstreith, M.H., Roses, A.D. and Alberts, M.J. (1994) A molecular genetic study of intracerebral hemorrhage, Arch. Neurol. 51, 981–984.PubMedCrossRefGoogle Scholar
  31. 31.
    Anders, K.H., Wang, Z.Z., Kornfeld, M., Gray, F., Soontornniyomkij, V., Reed, L.A., Hart, M.N., Menchine, M., Secor, D.L. and Vinters, H.V. (1997) Giant cell arteritis in association with cerebral amyloid angiopathy: immunohistochemical and molecular studies, Hum. Pathol. 28, 1237–1246.PubMedCrossRefGoogle Scholar
  32. 32.
    Itoh, Y. and Yamada, M. (1997) Cerebral amyloid angiopathy in the elderly: the clinicopathological features, pathogenesis, and risk factors, Journal of Medical and Dental Sciences 44, 11–19.PubMedGoogle Scholar
  33. 33.
    Nagai, A., Kobayashi, S., Shimode, K., Imaoka, K., Umegae, N., Fujihara, S. and Nakamura, M. (1998) No mutations in cystatin C gene in cerebral amyloid angiopathy with cystatin C deposition, Mol. Chem. Neuropathol. 33, 63–78.PubMedCrossRefGoogle Scholar
  34. 34.
    Rosand, J., Hylek, E.M., O’Donnell, H.C. and Greenberg, S.M. (1999) Cerebral amyloid angiopathy and warfarin-associated hemorrhage. A genetic and neuropathological study., Neurology (abs) 52, A503.Google Scholar
  35. 35.
    Ramsay, D.A., Penswick, J.L. and Robertson, D.M. (1990) Fatal streptokinase-induced intracerebral hemorrhage in cerebral amyloid angiopathy, Can. J. Neurol. Sci. 17, 336341.Google Scholar
  36. 36.
    Pendlebury, W.W., Iole, E.D., Tracy, R.P. and Dill, B.A. (1991) Intracerebral hemorrhage related to cerebral amyloid angiopathy and t-PA treatment, Ann. Neurol. 29, 210–213.PubMedCrossRefGoogle Scholar
  37. 37.
    Leblanc, R., Haddad, G and Robitaille, Y. (1992) Cerebral hemorrhage from amyloid angiopathy and coronary thrombolysis, Neurosurgery 31, 586–590.PubMedCrossRefGoogle Scholar
  38. 38.
    Wijdicks, E.F. and Jack, C.R.J. (1993) Intracerebral hemorrhage after fibrinolytic therapy for acute myocardial infarction, Stroke 24, 554–557.PubMedCrossRefGoogle Scholar
  39. 39.
    Sloan, M.A., Price, T.R., Petito, C.K., Randall, A.M.Y., Solomon, R.E., Terrin, M.L., Gore, J., Collen, D., Kleinman, N., Feit, F., Babb, J., Herman, M., Roberts, W.C., Sopko, G., Bovill, E., Forman, S. and Knatterud, G.L. (1995) 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 45, 649–658.PubMedCrossRefGoogle Scholar
  40. 40.
    Kase, C.S., Robinson, R.K., Stein, R.W., DeWitt, L.D., Hier, D.B., Harp, D.L., Williams, J.P., Caplan, L.R. and Mohr, J.P. (1985) Anticoagulant-related intracerebral hemorrhage, Neurology 35, 943–948.PubMedCrossRefGoogle Scholar
  41. 41.
    Gore, J.M., Sloan, M., Price, T.R., Randall, A.M.Y., Bovill, E., Collen, D., Forman, S., Knatterud, G.L., Sopko, G. and Terrin, M.L. (1991) Intracerebral hemorrhage, cerebral infarction, and subdural hematoma after acute myocardial infarction and thrombolytic therapy in the Thrombolysis in Myocardial Infarction study: Thrombolysis in Myocardial Infarction, Phase II, Pilot and Clinical Trial, Circulation 83, 448–459.PubMedCrossRefGoogle Scholar
  42. 42.
    Kase, C.S., Pessin, M.S., Zivin, J.A., del Zoppo, G.J., Furlan, A.J., Buckley, J.W., Snipes, R.G. and Little John, J.K. (1992) Intracranial hemorrhage after coronary thrombolysis with tissue plasminogen activator, Am. J. Med. 92, 384–390.PubMedCrossRefGoogle Scholar
  43. 43.
    Hylek, E.M. and Singer, D.E. (1994) Risk factors for intracranial hemorrhage in outpatients taking warfarin, Ann. Intern. Med. 120, 897–902.PubMedCrossRefGoogle Scholar
  44. 44.
    McMechan, S.R. and Adgey, A.A. (1998) Age related outcome in acute myocardial infarction. Elderly people benefit from thrombolysis and should be included in trials (editorial), BMJ317, 1334–1335.Google Scholar
  45. 45.
    Mendelson, G. and Aronow, W.S. (1998) Underutilization of warfarin in older persons with chronic nonvalvular atrial fibrillation at high risk for developing stroke, J. Am. Geriatr. Soc. 46, 1423–1424.PubMedGoogle Scholar
  46. 46.
    Ropper, A.H. and Davis, K.R. (1980) Lobar cerebral hemorrhages: acute clinical syndromes in 26 cases, Ann. Neurol. 8, 141–147.PubMedCrossRefGoogle Scholar
  47. 47.
    Weisberg, L.A., Stazio, A., Shamsnia, M. and Elliott, D. (1990) Nontraumatic parenchymal brain hemorrhages, Medicine 69, 277–295.PubMedCrossRefGoogle Scholar
  48. 48.
    Brott, T., Broderick, J., Kothari, R., Barsan, W., Tomsick, T., Sauerbeck, L., Spilker, J., Duldner, J. and Khoury, J. (1997) Early hemorrhage growth in patients with intracerebral hemorrhage, Stroke 28, 1–5.Google Scholar
  49. 49.
    Weisberg, L.A., Shamsnia, M. and Elliott, D. (1991) Seizures caused by nontraumatic parenchymal brain hemorrhages, Neurology 41, 1197–1199.PubMedCrossRefGoogle Scholar
  50. 50.
    Cuny, E., Loiseau, H., Rivel, J., Vital, C. and Castel, J.P. (1996) Amyloid angiopathyrelated cerebellar hemorrhage., Surg. Neurol.46, 235–239.Google Scholar
  51. 51.
    Yamada, M., Itoh, Y., Otomo, E., Hayakawa, M. and Miyatake, T. (1993) Subarachnoid hemorrhage in the elderly: a necropsy study of the association with cerebral amyloid angiopathy, J. Neurol. Neurosurg. Psychiatry 56, 543–547.PubMedCrossRefGoogle Scholar
  52. 52.
    Kase, C.S., Williams, J.P., Wyatt, D.A. and Mohr, J.P. (1982) Lobar intracerebral hematomas: clinical and CT analysis of 22 cases, Neurology 32, 1146–1150.PubMedCrossRefGoogle Scholar
  53. 53.
    Helweg-Larsen, S., Sommer, W., Strange, P., Lester, J. and Boysen, G. (1984) Prognosis for patients treated conservatively for spontaneous intracerebral hematomas, Stroke 15, 1045–1048.PubMedCrossRefGoogle Scholar
  54. 54.
    Passero, S., Burgalassi, L., D’Andrea, P. and Battistini, N. (1995) Recurrence of bleeding in patients with primary intracerebral hemorrhage, Stroke 26, 1189–1192.PubMedCrossRefGoogle Scholar
  55. 55.
    O’Donnell, H.C., Rosand, J., Knudsen, K.A., Furie, K.L., Segal, A.Z., Chiu, R.I., Ikeda, D. and Greenberg, S.M. (2000) Apolipoprotein E genotype and risk of recurrent lobar hemorrhage. A prospective study, N. Engl. J. Med. in press.Google Scholar
  56. 56.
    Arakawa, S., Saku, Y., Ibayashi, S., Nagao, T. and Fujishima, M. (1998) Blood pressure control and recurrence of hypertensive brain hemorrhage, Stroke 29, 1806–1809.PubMedCrossRefGoogle Scholar
  57. 57.
    Counsell, C., Boonyakarnkul, S., Dennis, M., P., S., Bamford, J., Burn, J. and Warlow, C. (1995) Primary intracerebral hemorrhage in the Oxfordshire Community Stroke Project. 2. Prognosis., Cerebrovasc. Dis. 5, 26–34.Google Scholar
  58. 58.
    Neau, J.P., Ingrand, P., Couderq, C., Rosier, M.P., Bailbe, M., Dumas, P., Vandermarcq, P. and Gil, R. (1997) Recurrent intracerebral hemorrhage, Neurology 49, 106–113.Google Scholar
  59. 59.
    Gonzalez-Duarte, A., Cantu, C., Ruiz-Sandoval, J.L. and Barinagarrementeria, F. (1998) Recurrent primary cerebral hemorrhage: frequency, mechanisms, and prognosis, Stroke 29, 1802–1805.PubMedCrossRefGoogle Scholar
  60. 60.
    Kase, C.S. (1994) Cerebral amyloid angiopathy, in C.S. Kase and L.R. Caplan (eds.), Intracerebral Hemorrhage, Butterworth-Heinemann, Boston, pp. 179–200.Google Scholar
  61. 61.
    Smith, D.B. Hitchcock, M. and Philpott, P.J. (1985) Cerebral amyloid angiopathy presenting as transient ischemic attacks. Case report, J. Neurosurg. 63 963–964.Google Scholar
  62. 62.
    Greenberg, S.M., Vonsattel, J.P., Stakes, J.W., Gruber, M. and Finklestein, S.P. (1993) The clinical spectrum of cerebral amyloid angiopathy: presentations without lobar hemorrhage, Neurology 43, 2073–2079.PubMedCrossRefGoogle Scholar
  63. 63.
    Okazaki, H., Reagan, T.J. and Campbell, R.J. (1979) Clinicopathologic studies of primary cerebral amyloid angiopathy, Mayo Clin. Proc. 54, 22–31.Google Scholar
  64. 64.
    Olichney, J.M., Hansen, L.A., Hofstetter, C.R., Grundman, M., Katzman, R. and Thal, L.J. (1995) Cerebral infarction in Alzheimer’s disease is associated with severe amyloid angiopathy and hypertension, Arch. Neurol. 52, 702–708.PubMedCrossRefGoogle Scholar
  65. 65.
    Briceno, C.E., Resch, L. and Bernstein, M. (1987) Cerebral amyloid angiopathy presenting as a mass lesion, Stroke 18, 234–239.PubMedCrossRefGoogle Scholar
  66. 66.
    Le Coz, P., Mikol, J., Ferrand, J., Woimant, F., Masters, C., Beyreuther, K., Haguenau, M., Cophignon, J. and Pepin, B. (1991) Granulomatous angiitis and cerebral amyloid angiopathy presenting as a mass lesion, Neuropathology and Applied Neurobiology 17, 149155.Google Scholar
  67. 67.
    Mandybur, T.I. and Balko, G. (1992) Cerebral amyloid angiopathy with granulomatous angiitis ameliorated by steroid-cytoxan treatment, Clin. Neuropharm. 15, 241–247.CrossRefGoogle Scholar
  68. 68.
    Fountain, N.B. and Eberhard, D.A. (1996) Primary angiitis of the central nervous system associated with cerebral amyloid angiopathy: report of two cases and review of the literature., Neurology 46, 190–197.PubMedCrossRefGoogle Scholar
  69. 69.
    Ginsberg, L., Geddes, J. and Valentine, A. (1988) Amyloid angiopathy and granulomatous angiitis of the central nervous system: a case responding to corticosteroid treatment, J Neurol. 235, 438–440.PubMedCrossRefGoogle Scholar
  70. 70.
    Gray, F., Vinters, H.V., Le Noan, H., Salama, J., Delaporte, P. and Poirier, J. (1990) Cerebral amyloid angiopathy and granulomatous angiitis: immunohistochemical study using antibodies to the Alzheimer A4 peptide, Hum. Pathol. 21, 1290–1293.PubMedCrossRefGoogle Scholar
  71. 71.
    Vonsattel, J.P. Myers, R.H., Hedley-Whyte, E.T., Ropper, A.H., Bird, E.D. and Richardson, E.P. (1991) Cerebral amyloid angiopathy without and with cerebral hemorrhages: a comparative histological study, Ann. Neurol. 30 637–649.Google Scholar
  72. 72.
    Powers, J.M., Stein, B.M. and Torres, R.A. (1990) Sporadic cerebral amyloid angiopathy with giant cell reaction, Acta Neuropathol. 81, 95–98.PubMedCrossRefGoogle Scholar
  73. 73.
    Hendricks, H.T., Franke, C.L. and Theunissen, P.H. (1990) Cerebral amyloid angiopathy: diagnosis by MRI and brain biopsy, Neurology 40, 1308–1310.PubMedCrossRefGoogle Scholar
  74. 74.
    Yoshimura, M., Yamanouchi, H., Kuzuhara, S., Mori, H., Sugiura, S., Mizutani, T., Shimada, H., Tomonaga, M. and Toyokura, Y. (1992) Dementia in cerebral amyloid angiopathy: a clinicopathological study, J. Neurol. 239, 441–450.PubMedCrossRefGoogle Scholar
  75. 75.
    Silbert, P.L., Bartleson, J.D., Miller, G.M., Parisi, J.E., Goldman, M.S. and Meyer, F.B. (1995) Cortical petechial hemorrhage, leukoencephalopathy, and subacute dementia associated with seizures due to cerebral amyloid angiopathy, Mayo Clin. Proc. 70, 477480.Google Scholar
  76. 76.
    Gray, F., Dubas, F., Roullet, E. and Escourolle, R. (1985) Leukoencephalopathy in diffuse hemorrhagic cerebral amyloid angiopathy, Ann. Neurol. 18, 54–59.PubMedCrossRefGoogle Scholar
  77. 77.
    Bogucki, A., Papierz, W., Szymanska, R. and Staniaszczyk, R. (1988) Cerebral amyloid angiopathy with attenuation of the white matter on CT scans: subcortical arteriosclerotic encephalopathy (Binswanger) in a normotensive patient, J. Neurol. 235, 435–437.PubMedCrossRefGoogle Scholar
  78. 78.
    Caplan, L.R. (1995) Binswanger’s disease-revisited., Neurology 45, 626–633.PubMedCrossRefGoogle Scholar
  79. 79.
    Bomebroek, M., Haan, J., van Buchem, M.A., Lanser, J.B., de Vries, V.D., Weerd, M.A., Zoeteweij, M. and Roos, R.A. (1996) White matter lesions and cognitive deterioration in presymptomatic carriers of the amyloid precursor protein gene codon 693 mutation, Arch. Neurol. 53, 43–48.CrossRefGoogle Scholar
  80. 80.
    Schmechel, D.E., Saunders, A.M., Strittmatter, W.J., Crain, B.J., Hulette, C.M., Joo, S.H., Pericak-Vance, M.A., Goldgaber, D. and Roses, A.D. (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, 9649–9653.CrossRefGoogle Scholar
  81. 81.
    Olichney, J.M., Hansen, L.A., Galasko, D., Saitoh, T., Hofstetter, C.R., Katzman, R. and Thal, L.J. (1996) The apolipoprotein E epsilon 4 allele is associated with increased neuritic plaques and cerebral amyloid angiopathy in Alzheimer’s disease and Lewy body variant, Neurology 47, 190–196.PubMedCrossRefGoogle Scholar
  82. 82.
    Ellis, R.J., Olichney, J.M., Thal, L.J., Mirra, S.S., Morris, J.C., Beekly, D. and Heyman, A. (1996) Cerebral amyloid angiopathy in the brains of patients with Alzheimer’s disease: the CERAD experience, Part XV, Neurology 46, 1592–1596.PubMedCrossRefGoogle Scholar
  83. 83.
    Mandybur, T.I. (1986) Cerebral amyloid angiopathy: the vascular pathology and complications, JNeuropathol. Exp. Neurol. 45, 79–90.CrossRefGoogle Scholar
  84. 84.
    Vinters, H.V., Natte, R., Maat-Schieman, M.L., van Duinen, S.G., Hegeman Kleinn, I., Welling Graafland, C., Haan, J. and Roos, R.A. (1998) Secondary microvascular degeneration in amyloid angiopathy of patients with hereditary cerebral hemorrhage with amyloidosis, Dutch type (HCHWA-D), Acta Neuropathol. 95, 235–244.PubMedCrossRefGoogle Scholar
  85. 85.
    McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D. and Stadlan, E.M. (1984) Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s Disease, Neurology 34, 939–944.PubMedCrossRefGoogle Scholar
  86. 86.
    Joachim, C.L., Morris, J.H. and Selkoe, D.J. (1988) Clinically diagnosed Alzheimer’s disease: autopsy results in 150 cases, Ann. Neurol. 24, 50–56.PubMedCrossRefGoogle Scholar
  87. 87.
    Gearing, M., Mirra, S.S., Hedreen, J.C., Sumi, S.M., Hansen, L.A. and Heyman, A. (1995) The Consortium to Establish a Registry for Alzheimer’s Disease (CERAD). Part X. Neuropathology confirmation of the clinical diagnosis of Alzheimer’s disease, Neurology 45, 461–466.PubMedCrossRefGoogle Scholar
  88. 88.
    Greenberg, S.M. (1998) Cerebral amyloid angiopathy. Prospects for clinical diagnosis and treatment., Neurology 51, 690–694.PubMedCrossRefGoogle Scholar
  89. 89.
    Atlas, S.W., Mark, A.S., Grossman, R.I. and Gomori, J.M. (1988) Intracranial hemorrhage: gradient-echo MR imaging at 1.5 T. Comparison with spin-echo imaging and clinical applications, Radiology 168, 803–807.PubMedGoogle Scholar
  90. 90.
    Greenberg, S.M., Finklestein, S.P. and Schaefer, P.W. (1996) Petechial hemorrhages accompanying lobar hemorrhages: Detection by gradient-echo MRI, Neurology 46, 1751 1754.Google Scholar
  91. 91.
    Offenbacher, H., Fazekas, F., Schmidt, R., Koch, M., Fazekas, G. and Kapeller, P. (1996) MR of cerebral abnormalities concomitant with primary intracerebral hematomas, AJNR Am. J. Neuroradiol. 17, 573–578.PubMedGoogle Scholar
  92. 92.
    Van Nostrand, W.E., Wagner, S.L., Shankle, W.R., Farrow, J.S., Dick, M., Rozemuller, J.M., Kuiper, M.A., Wolters, E.C., Zimmerman, J., Cotman, C.W. and et, al. (1992) Decreased levels of soluble amyloid beta-protein precursor in cerebrospinal fluid of live Alzheimer disease patients, Proc. Natl. Acad. Sci. USA 89, 2551–2555.PubMedCrossRefGoogle Scholar
  93. 93.
    Shimode, K., Fujihara, S., Nakamura, M., Kobayashi, S. and Tsunematsu, T. (1991) Diagnosis of cerebral amyloid angiopathy by enzyme-linked immunosorbent assay of cystatin C in cerebrospinal fluid, Stroke 22, 860–866.PubMedCrossRefGoogle Scholar
  94. 94.
    Hart, R.G., Boop, B.S. and Anderson, D.C. (1995) Oral anticoagulants and intracranial hemorrhage, Stroke 26, 1471–1477.PubMedCrossRefGoogle Scholar
  95. 95.
    He, J., Whelton, P.K., Vu, B. and Klag, M.J. (1998) Aspirin and risk of hemorrhagic stroke: a meta-analysis of randomized controlled trials, JAMA 280, 1930–1935.PubMedCrossRefGoogle Scholar
  96. 96.
    Greene, G.M., Godersky, J.C., Biller, J., Hart, M.N. and Adams, H.P.J. (1990) Surgical experience with cerebral amyloid angiopathy, Stroke 21, 1545–1549.PubMedCrossRefGoogle Scholar
  97. 97.
    Matkovic, Z., Davis, S., Gonzales, M., Kamins, R. and Masters, C.L. (1991) Surgical risk of hemorrhage in cerebral amyloid angiopathy, Stroke 22, 456–461.PubMedCrossRefGoogle Scholar
  98. 98.
    Minakawa, T., Takeuchi, S., Sasaki, O., Koizumi, T., Honad, Y., Fujii, Y., Ozawa, T., Ogawa, H., Koike, T. and Tanaka, R. (1995) Surgical experience with massive lobar hemorrhage caused by cerebral amyloid angiopathy, Acta Neurochir. 132, 48–52.PubMedCrossRefGoogle Scholar
  99. 99.
    Izumihara, A., Ishihara, T., Iwamoto, N., Yamashita, K. and Ito, H. (1999) Postoperative outcome of 37 patients with lobar intracerebral hemorrhage related to cerebral amyloid angiopathy, Stroke 30, 29–33.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2000

Authors and Affiliations

  • Steven M. Greenberg
    • 1
  1. 1.Department of NeurologyMassachusetts General Hospital and Harvard Medical SchoolBostonUSA

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