Download PDF
Neuroradiologie Scan 2014; 04(02): 123-147
DOI: 10.1055/s-0034-1364918
Fortbildung
© Georg Thieme Verlag KG Stuttgart · New York

Zerebrale Mikroblutungen: Leitfaden für den Nachweis und die klinische Relevanz bei verschiedenen Krankheitsbildern[1]

Cerebral microbleeds: a guide to detection and clinical relevance in different disease settings
Andreas Charidimou
,
Anant Krishnan
,
David J. Werring
,
H. Rolf Jäger
Further Information

Publication History

Publication Date:
17 April 2014 (online)

Also available at
    Permissions and Reprints

Zusammenfassung

Zerebrale Mikroblutungen sind mittlerweile ein wichtiger neuer Bildgebungsmarker für zerebrale Mikroangiopathien. Die Entwicklung von magnetresonanztomografischen Methoden, die besonders empfindlich für paramagnetische Blutprodukte sind, wie beispielsweise T2*-gewichtete Gradientenecho- und suszeptibilitätsgewichtete Sequenzen, hat den Nachweis von Mikroblutungen bei einer zunehmend größeren Zahl von Patienten in Schlaganfall- und Gedächtnissprechstunden sowie bei gesunden älteren Menschen und bei einer Vielzahl von anderen, selteneren Erkrankungen und Syndromen ermöglicht. Der Nachweis zerebraler Mikroblutungen ist für die Diagnose der zugrunde liegenden Mikroangiopathie, für die Sicherheit der Behandlung mit Antithrombotika und bezüglich der Gefahr einer symptomatischen intrazerebralen Blutung, aber auch bei kognitiver Beeinträchtigung und Demenz von klinischer Bedeutung. Dieser Fortbildungsbeitrag beruht auf einer umfassenden Literaturrecherche und eigenen Befunden aus Forschung und klinischer Praxis und bietet einen Leitfaden für den Nachweis und die klinische Relevanz von zerebralen Mikroblutungen bei verschiedenen Krankheitsbildern.

Abstract

Cerebral microbleeds have emerged as an important new imaging marker of cerebral small vessel disease. With the development of MRI techniques that are exquisitely sensitive to paramagnetic blood products, such as T2*-weighted gradient-recalled echo and susceptibility-weighted sequences, microbleeds have been detected in ever-increasing numbers of patients in stroke and cognitive clinics, as well as in healthy older people and in a variety of other rarer diseases and syndromes. Detection of cerebral microbleeds has clinical implications with respect to the diagnosis of the underlying small vessel disease, the safety of antithrombotic use, and the risk of symptomatic intracerebral haemorrhage, cognitive impairment and dementia. This article provides a guide to the detection and clinical relevance of cerebral microbleeds in different conditions based on a comprehensive review of the literature and own findings in research and clinical practice.

Kernaussagen

  • Zerebrale Mikroblutungen sind auf T2*w GRE- oder SWI-MRT-Sequenzen als kleine, rundliche, homogene, hypointense Herde definiert.

  • Zerebrale Mikroblutungen gehen vorwiegend mit 2 Arten sporadischer Mikroangiopathie einher: hypertoner Arteriopathie oder zerebraler Amyloidangiopathie.

  • Zerebrale Mikroblutungen sind in der allgemeinen älteren Bevölkerung sehr häufig und stehen mit einer Reihe von Erkrankungen in Zusammenhang, darunter ischämischer Schlaganfall, spontane intrazerebrale Blutung, Morbus Alzheimer, vaskuläre kognitive Beeinträchtigung sowie eine Vielzahl anderer, seltenerer Krankheitsbilder.

  • Die immer besser funktionierende Erkennung von zerebralen Mikroblutungen hat klinische Konsequenzen für die Diagnose der zugrunde liegenden Mikroangiopathie, für die Sicherheit der Behandlung mit Antithrombotika und anderer therapeutischer Maßnahmen sowie für das Risiko einer intrazerebralen Blutung und einer kognitiven Beeinträchtigung.

1 © 2013 Springer-Verlag Berlin Heidelberg. All rights reserved. Originally published in English in Neuroradiology 2013; 55: 655 – 674. Online published in 10.1007/s00234-013-1175-4. Translated and reprinted with permission of Springer-Verlag Berlin Heidelberg. Springer-Verlag Berlin Heidelberg is not responsible for any inaccuracy or error arising from the translation from English to German.


 

  • Literatur

  • 1 Scharf J, Brauherr E, Forsting M et al. Significance of haemorrhagic lacunes on MRI in patients with hypertensive cerebrovascular disease and intracerebral haemorrhage. Neuroradiology 1994; 36: 504-508
    CrossrefGoogle Scholar
  • 2 Offenbacher H, Fazekas F, Schmidt R et al. MR of cerebral abnormalities concomitant with primary intracerebral hematomas. AJNR Am J Neuroradiol 1996; 17: 573-578
    Google Scholar
  • 3 Werring D. Cerebral microbleeds: pathophysiology to clinical practice. Cambridge: University Press; 2011
    CrossrefGoogle Scholar
  • 4 Greenberg SM, Vernooij MW, Cordonnier C et al. Microbleed Study G. Cerebral microbleeds: a guide to detection and interpretation. Lancet Neurol 2009; 8: 165-174
    CrossrefGoogle Scholar
  • 5 Cordonnier C, Al-Shahi Salman R, Wardlaw J. Spontaneous brain microbleeds: systematic review, subgroup analyses and standards for study design and reporting. Brain 2007; 130: 1988-2003
    CrossrefGoogle Scholar
  • 6 Fazekas F, Kleinert R, Roob G et al. Histopathologic analysis of foci of signal loss on gradient-echo T2*-weighted MR images in patients with spontaneous intracerebral hemorrhage: evidence of microangiopathy-related microbleeds. AJNR Am J Neuroradiol 1999; 20: 637-642
    Google Scholar
  • 7 Shoamanesh A, Kwok CS, Benavente O. Cerebral microbleeds: histopathological correlation of neuroimaging. Cerebrovasc Dis 2011; 32: 528-534
    CrossrefGoogle Scholar
  • 8 Schrag M, McAuley G, Pomakian J et al. Correlation of hypointensities in susceptibility-weighted images to tissue histology in dementia patients with cerebral amyloid angiopathy: a postmortem MRI study. Acta Neuropathol 2009; 119: 291-302
    Google Scholar
  • 9 Charidimou A, Werring DJ. Cerebral microbleeds: detection, mechanisms and clinical challenges. Futur Neurol 2011; 6: 587-611
    CrossrefGoogle Scholar
  • 10 Poels MM, Venooij MW, Ikram MA et al. Prevalence and risk factors of cerebral microbleeds: an update of the Rotterdam scan study. Stroke 2010; 41 (Suppl. 10) 103-S106
    CrossrefGoogle Scholar
  • 11 Sveinbjornsdottir S, Sigurdsson S, Aspelund T et al. Cerebral microbleeds in the population based AGES-Reykjavik study: prevalence and location. J Neurol Neurosurg Psychiatry 2008; 79: 1002-1006
    CrossrefGoogle Scholar
  • 12 Werring DJ, Coward LJ, Losseff NA et al. Cerebral microbleeds are common in ischemic stroke but rare in TIA. Neurology 2005; 65: 1914-1918
    CrossrefGoogle Scholar
  • 13 Pettersen JA, Sathiyamoorthy G, Gao FQ et al. Microbleed topography, leukoaraiosis, and cognition in probable Alzheimer disease from the Sunnybrook dementia study. Arch Neurol 2008; 65: 790-795
    CrossrefGoogle Scholar
  • 14 Cordonnier C, van der Flier WM. Brain microbleeds and Alzheimer’s disease: innocent observation or key player?. Brain 2011; 134: 335-344
    CrossrefGoogle Scholar
  • 15 Cordonnier C, van der Flier WM, Sluimer JD et al. Prevalence and severity of microbleeds in a memory clinic setting. Neurology 2006; 66: 1356-1360
    CrossrefGoogle Scholar
  • 16 Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 2010; 9: 689-701
    CrossrefGoogle Scholar
  • 17 Werring DJ. Cerebral microbleeds: clinical and pathophysiological significance. J Neuroimaging 2007; 17: 193-203
    CrossrefGoogle Scholar
  • 18 Gregoire SM, Brown MM, Kallis C et al. MRI detection of new microbleeds in patients with ischemic stroke: five-year cohort follow-up study. Stroke 2010; 41: 184-186
    CrossrefGoogle Scholar
  • 19 Poels MM, Ikram MA, van der Lugt A et al. Incidence of cerebral microbleeds in the general population: the Rotterdam Scan Study. Stroke 2011; 42: 656-661
    CrossrefGoogle Scholar
  • 20 Goos JD, Henneman WJ, Sluimer JD et al. Incidence of cerebral microbleeds: a longitudinal study in a memory clinic population. Neurology 2010; 74: 1954-1960
    CrossrefGoogle Scholar
  • 21 Jeon SB, Kwon SU, Cho AH et al. Rapid appearance of new cerebral microbleeds after acute ischemic stroke. Neurology 2009; 73: 1638-1644
    CrossrefGoogle Scholar
  • 22 Kidwell CS, Greenberg SM. Red meets white: Do microbleeds link hemorrhagic and ischemic cerebrovascular disease?. Neurology 2009; 73: 1614-1615
    CrossrefGoogle Scholar
  • 23 Kakar P, Charidimou A, Werring D. Cerebral microbleeds: a new dilemma in stroke medicine. JRSM Cardiovascular Disease 2012; ; DOI: DOI: 10.1177/2048004012474754.
    Google Scholar
  • 24 Haacke EM, Mittal S, Wu Z et al. Susceptibility-weighted imaging: technical aspects and clinical applications. Part I. AJNR Am J Neuroradiol 2009; 30: 19-30
    CrossrefPubMedGoogle Scholar
  • 25 Atlas SW, Mark AS, Grossman RI et al. Intracranial hemorrhage: gradient-echo MR imaging at 1,5 T. Comparison with spin-echo imaging and clinical applications. Radiology 1988; 168: 803-807
    CrossrefGoogle Scholar
  • 26 Greenberg SM, Finklestein SP, Schaefer PW. Petechial hemorrhages accompanying lobar hemorrhage: detection by gradient-echo MRI. Neurology 1996; 46: 1751-1754
    CrossrefGoogle Scholar
  • 27 Gregoire SM, Werring DJ, Chaudhary UJ et al. Choice of echo time on GRE T2*-weighted MRI influences the classification of brain microbleeds. Clin Radiol 2010; 65: 391-394
    CrossrefGoogle Scholar
  • 28 Tatsumi S, Ayaki T, Shinohara M et al. Type of gradient recalled-echo sequence results in size and number change of cerebral microbleeds. AJNR Am J Neuroradiol 2008; 29: e13
    CrossrefGoogle Scholar
  • 29 Vernooij MW, Ikram MA, Wielopolski PA et al. Cerebral microbleeds: accelerated 3D T2*-weighted GRE MR imaging versus conventional 2D T2*-weighted GRE MR imaging for detection. Radiology 2008; 248: 272-277
    CrossrefGoogle Scholar
  • 30 Nandigam RN, Viswanathan A, Delgado P et al. MR imaging detection of cerebral microbleeds: effect of susceptibility-weighted imaging, section thickness, and field strength. AJNR Am J Neuroradiol 2009; 30: 338-343
    Google Scholar
  • 31 Stehling C, Wersching H, Kloska SP et al. Detection of asymptomatic cerebral microbleeds: a comparative study at 1,5 and 3,0 T. Acad Radiol 2008; 15: 895-900
    CrossrefGoogle Scholar
  • 32 Conijn MM, Geerlings MI, Biessels GJ et al. Cerebral microbleeds on MR imaging: comparison between 1,5 and 7 T. AJNR Am J Neuroradiol 2011; 32: 1043-1049
    CrossrefGoogle Scholar
  • 33 Haacke EM, Boikov AS, Barnes E et al. Susceptibility-weighted imaging. In: Werring DJ, ed. Cerebral microbleeds: pathophysiology to clinical practice. Cambridge: Cambridge University Press; 2011: 22-33
    CrossrefGoogle Scholar
  • 34 Haacke EM, Xu Y, Cheng YC et al. Susceptibility weighted imaging (SWI). Magn Reson Med 2004; 52: 612-618
    CrossrefGoogle Scholar
  • 35 Ayaz M, Boikov AS, Haacke EM et al. Imaging cerebral microbleeds using susceptibility weighted imaging: one step toward detecting vascular dementia. J Magn Reson Imaging 2010; 31: 142-148
    CrossrefGoogle Scholar
  • 36 Wu Z, Mittal S, Kish K et al. Identification of calcification with MRI using susceptibility-weighted imaging: a case study. J Magn Reson Imaging 2009; 29: 177-182
    CrossrefGoogle Scholar
  • 37 Mittal S, Wu Z, Neelavalli J et al. Susceptibility-weighted imaging: technical aspects and clinical applications. Part II. AJNR Am J Neuroradiol 2009; 30: 232-252
    CrossrefPubMedGoogle Scholar
  • 38 Goos JD, van der Flier WM, Knol DL et al. Clinical relevance of improved microbleed detection by susceptibility-weighted magnetic resonance imaging. Stroke 2011; 42: 1894-1900
    CrossrefGoogle Scholar
  • 39 Poels MM, Ikram MA, Vernooij MW. Improved MR imaging detection of cerebral microbleeds more accurately identifies persons with vasculopathy. AJNR Am J Neuroradiol 2012; 33: 1553-1556
    CrossrefGoogle Scholar
  • 40 Greenberg SM. Small vessels, big problems. N Engl J Med 2006; 354: 1451-1453
    CrossrefGoogle Scholar
  • 41 Charidimou A, Gang Q, Werring DJ. Sporadic cerebral amyloid angiopathy revisited: recent insights into pathophysiology and clinical spectrum. J Neurol Neurosurg Psychiatry 2012; 83: 124-137
    CrossrefGoogle Scholar
  • 42 Vernooij MW, van der Lugt A, Ikram MA et al. Prevalence and risk factors of cerebral microbleeds: the Rotterdam Scan Study. Neurology 2008; 70: 1208-1214
    CrossrefGoogle Scholar
  • 43 Maxwell SS, Jackson CA, Paternoster L et al. Genetic associations with brain microbleeds: systematic review and meta-analyses. Neurology 2011; 77: 159-167
    Google Scholar
  • 44 Dierksen GA, Skehan ME, Khan MA et al. Spatial relation between microbleeds and amyloid deposits in amyloid angiopathy. Ann Neurol 2010; 68: 545-548
    CrossrefGoogle Scholar
  • 45 Lee SH, Bae HJ, Kwon SJ et al. Cerebral microbleeds are regionally associated with intracerebral hemorrhage. Neurology 2004; 62: 72-76
    CrossrefGoogle Scholar
  • 46 Roob G, Lechner A, Schmidt R et al. Frequency and location of microbleeds in patients with primary intracerebral hemorrhage. Stroke 2000; 31: 2665-2669
    CrossrefGoogle Scholar
  • 47 Smith EE, Nandigam KR, Chen YW et al. MRI markers of small vessel disease in lobar and deep hemispheric intracerebral hemorrhage. Stroke 2010; 41: 1933-1938
    CrossrefGoogle Scholar
  • 48 Lummel N, Lutz J, Bruckmann H et al. The value of magnetic resonance imaging for the detection of the bleeding source in non-traumatic intracerebral haemorrhages: a comparison with conventional digital subtraction angiography. Neuroradiology 2012; 54: 673-680
    CrossrefGoogle Scholar
  • 49 Knudsen KA, Rosand J, Karluk D et al. Clinical diagnosis of cerebral amyloid angiopathy: validation of the Boston criteria. Neurology 2001; 56: 539-539
    Google Scholar
  • 50 Rosand J, Muzikansky A, Kumar A et al. Spatial clustering of hemorrhages in probable cerebral amyloid angiopathy. Ann Neurol 2005; 58: 459-462
    CrossrefGoogle Scholar
  • 51 van Rooden S, van der Grond J, van den Boorn R et al. Descriptive analysis of the Boston criteria applied to a Dutch-type cerebral amyloid angiopathy population. Stroke 2009; 40: 3022-3027
    CrossrefGoogle Scholar
  • 52 Linn J, Herms J, Dichgans M et al. Subarachnoid hemosiderosis and superficial cortical hemosiderosis in cerebral amyloid angiopathy. AJNR Am J Neuroradiol 2008; 29: 184-186
    CrossrefGoogle Scholar
  • 53 Raposo N, Viguier A, Cuvincjuc V et al. Cortical subarachnoid haemorrhage in the elderly: a recurrent event probably related to cerebral amyloid angiopathy. Eur J Neurol 2011; 18: 597-603
    CrossrefGoogle Scholar
  • 54 Linn J, Halpin A, Dernaerel P et al. Prevalence of superficial siderosis in patients with cerebral amyloid angiopathy. Neurology 2010; 74: 1346-1350
    CrossrefGoogle Scholar
  • 55 Sperling RA, Jack Jr CR, Black SE et al. Amyloid-related imaging abnormalities in amyloid-modifying therapeutic trials: recommendations from the Alzheimer’s Association Research Roundtable Workgroup. Alzheimers Dement 2011; 7: 367-385
    CrossrefGoogle Scholar
  • 56 Charidimou A, Law R, Werring DJ. Amyloid „spells“ trouble. Lancet 2012; 380: 1620
    CrossrefGoogle Scholar
  • 57 Greenberg SM, Vonsattel JP, Stakes JW et al. The clinical spectrum of cerebral amyloid angiopathy: presentations without lobar hemorrhage. Neurology 1993; 43: 2073-2079
    CrossrefGoogle Scholar
  • 58 Roch JA, Nighoghossian N, Hermier M et al. Transient neurologic symptoms related to cerebral amyloid angiopathy: usefulness of T2*-weighted imaging. Cerebrovasc Dis 2005; 20: 412-414
    CrossrefGoogle Scholar
  • 59 Smith DB, Hitchcock M, Philpott PJ. Cerebral amyloid angiopathy presenting as transient ischemic attacks. Case report. J Neurosurg 1985; 63: 963-964
    CrossrefGoogle Scholar
  • 60 Charidimou A, Peeters A, Fox Z et al. Spectrum of transient focal neurological episodes in cerebral amyloid angiopathy: multicentre magnetic resonance imaging cohort study and meta-analysis. Stroke 2012; 43: 2324-2330
    CrossrefPubMedGoogle Scholar
  • 61 Menon RS, Kidwell CS. Neuroimaging demonstration of evolving small vessel ischemic injury in cerebral amyloid angiopathy. Stroke 2009; 40: e675-e677
    CrossrefGoogle Scholar
  • 62 Kimberly WT, Gilson A, Rost NS et al. Silent ischemic infarcts are associated with hemorrhage burden in cerebral amyloid angiopathy. Neurology 2009; 72: 1230-1235
    CrossrefGoogle Scholar
  • 63 Smith EE, Schneider JA, Wardlaw JM et al. Cerebral microinfarcts: the invisible lesions. Lancet Neurol 2012; 11: 272-282
    CrossrefGoogle Scholar
  • 64 Ellis RJ, Olichney JM, Thal LJ et al. Cerebral amyloid angiopathy in the brains of patients with Alzheimer’s disease: the CERAD experience. Part XV. Neurology 1996; 46: 1592-1596
    CrossrefGoogle Scholar
  • 65 De Reuck J, Deramecourt V, Cordonnier C et al. The impact of cerebral amyloid angiopathy on the occurrence of cerebrovascular lesions in demented patients with Alzeimer features: a neuropathological study. Eur J Neurol 2011; 18: 913-918
    CrossrefGoogle Scholar
  • 66 Joutel A, Corpechot C, Ducros A et al. Notch3 mutations in CADASIL, a hereditary adult-onset condition causing stroke and dementia. Nature 1996; 383: 707-710
    CrossrefGoogle Scholar
  • 67 Tournier-Lasserve E, Joutel A, Melki J et al. Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy maps to chromosome 19q12. Nat Genet 1993; 3: 256-259
    CrossrefGoogle Scholar
  • 68 Dichgans M, Mayer M, Uttner I et al. The phenotypic spectrum of CADASIL: clinical findings in 102 cases. Ann Neurol 1998; 44: 731-739
    CrossrefGoogle Scholar
  • 69 Viswanathan A, Chabriat H, Dichgans M. Cerebral microbleeds in CADASIL. In: Werring DJ, ed. Cerebral microbleeds: pathophysiology to clinical practice. Cambridge: Cambridge University Press; 2011: 135-141
    CrossrefGoogle Scholar
  • 70 O’Sullivan M, Jarosz JM, Martin RJ et al. MRI hyperintensities of the temporal lobe and external capsule in patients with CADASIL. Neurology 2001; 56: 628-634
    CrossrefGoogle Scholar
  • 71 Labauge P. Magnetic resonance findings in leucodystrophies and MS. Int MS J 2009; 16: 47-56
    PubMedGoogle Scholar
  • 72 Lesnik Oberstein SA, van den Boom R, van Buchem MA et al. Cerebral microbleeds in CADASIL. Neurology 2001; 57: 1066-1070
    CrossrefGoogle Scholar
  • 73 Dichgans M, Holtmannspotter M, Herzog J et al. Cerebral microbleeds in CADASIL: a gradient-echo magnetic resonance imaging and autopsy study. Stroke 2002; 33: 67-71
    CrossrefGoogle Scholar
  • 74 Viswanathan A, Guichard JP, Gschwendtner A et al. Blood pressure and haemoglobin A1c are associated with microhaemorrhage in CADASIL: a two-centre cohort study. Brain 2006; 129: 2375-2383
    CrossrefGoogle Scholar
  • 75 Liem MK, Lesnik Oberstein SA, Haan J et al. MRI correlates of cognitive decline in CADASIL: a 7-year follow-up study. Neurology 2009; 72: 143-148
    CrossrefGoogle Scholar
  • 76 Viswanathan A, Godin O, Jouvent E et al. Impact of MRI markers in subcortical vascular dementia: a multi-modal analysis in CADASIL. Neurobiol Aging 2010; 31: 1629-1636
    CrossrefGoogle Scholar
  • 77 Lanfranconi S, Markus HS. COL4A1 mutations as a monogenic cause of cerebral small vessel disease: a systematic review. Stroke 2010; 41: e513-e518
    CrossrefGoogle Scholar
  • 78 Gould DB, Phalan FC, van Mil SE et al. Role of COL4A1 in small-vessel disease and hemorrhagic stroke. N Engl J Med 2006; 354: 1489-1496
    CrossrefGoogle Scholar
  • 79 Alamowitch S, Plaisier E, Favrole P et al. Cerebrovascular disease related to COL4A1 mutations in HANAC syndrome. Neurology 2009; 73: 1873-1882
    CrossrefGoogle Scholar
  • 80 Klein I, Iung B, Wolff M et al. Silent T2* cerebral microbleeds: a potential new imaging clue in infective endocarditis. Neurology 2007; 68: 2043
    CrossrefGoogle Scholar
  • 81 Nandigam RN. Re: Silent T2* cerebral microbleeds: a potential new imaging clue in infective endocarditis. Neurology 2008; 70: 323 , author reply 323–324
    CrossrefGoogle Scholar
  • 82 Klein I, Iung B, Labreuche J et al. Cerebral microbleeds are frequent in infective endocarditis: a case-control study. Stroke 2009; 40: 3461-3465
    CrossrefGoogle Scholar
  • 83 Okazaki S, Sakaguchi M, Hyun B et al. Cerebrl microbleeds predict impending intracranial hemorrhage in infective endocarditis. Cerebrovasc Dis 2011; 32: 483-488
    CrossrefGoogle Scholar
  • 84 Vanacker P, Nelissen N, Van Laere K et al. Images in neurology. Scattered cerebral microbleeds due to cardiac myxoma. Arch Neurol 2009; 66: 796-797
    Google Scholar
  • 85 Jeon SB, Lee JW, Kim SJ et al. New cerebral lesions on T2*-weighted gradient-echo imaging after cardiac valve surgery. Cerebrovasc Dis 2010; 30: 194-199
    CrossrefGoogle Scholar
  • 86 Kim GM, Kim CH, Kim BS. Multiple cerebral infarction and microbleeds associated with adult-onset paroxysmal cold hemoglobinuria. J Clin Neurosci 2009; 16: 348-349
    CrossrefGoogle Scholar
  • 87 Llufriu S, Cervera A, Capurro S et al. Neurological picture. Familial Sneddons’s syndrome with microbleeds in MRI. J Neurol Neurosurg Psychiatry 2008; 79: 962
    CrossrefGoogle Scholar
  • 88 Yokoyama S, Hirano H, Uomizu K et al. High incidence of microbleeds in hemodialysis patients detected by T2*-weighted gradient-echo magnetic resonance imaging. Neurol Med Chir (Tokyo) 2005; 45: 556-560 , discussion 560
    CrossrefGoogle Scholar
  • 89 Cho AH, Lee SB, Han SJ et al. Impaired kidney function and cerebral microbleeds in patients with acute ischemic stroke. Neurology 2009; 73: 1645-1648
    CrossrefGoogle Scholar
  • 90 Ryu WS, Lee SH, Kim CK et al. The relation between chronic kidney disease and cerebral microbleeds: difference between patients with and without diabetes. Int J Stroke 2012; 7: 551-557
    CrossrefGoogle Scholar
  • 91 Kikuta K, Takagi Y, Nozaki K et al. Asymptomatic microbleeds in moyamoya disease: T2*-weighted gradient-echo magnetic resonance imaging study. J Neurosurg 2005; 102: 470-475
    CrossrefGoogle Scholar
  • 92 Ishikawa T, Kuroda S, Nakayama N et al. Prevalence of asymptomatic microbleeds in patients with moyamoya disease. Neurol Med Chir (Tokyo) 2005; 45: 495-500 , discussion 500
    CrossrefGoogle Scholar
  • 93 Kikuta K, Takagi Y, Nozaki K et al. The presence of multiple microbleeds as a predictor of subsequent cerebral hemorrhage in patients with moyamoya disease. Neurosurgery 2008; 62: 104-111 , discussion 111–112
    CrossrefGoogle Scholar
  • 94 Tanaka M, Sakaguchi M, Miwa K et al. Cerebral microbleeds in patients with moyamoya-like vessels secondary to atherosclerosis. Intern Med 2012; 51: 167-172
    CrossrefGoogle Scholar
  • 95 Bartynski WS. Posterior reversible encephalopathy syndrome. Part I: fundamental imaging and clinical features. AJNR Am J Neuroradiol 2008; 29: 1036-1042
    CrossrefPubMedGoogle Scholar
  • 96 McKinney AM, Short J, Truwit CL et al. Posterior reversible encephalopathy syndrome: incidence of atypical regions of involvement and imaging findings. AJR Am J Roentgenol 2007; 189: 904-912
    CrossrefPubMedGoogle Scholar
  • 97 McKinney AM, Sarikaya B, Gustafson C et al. Detection of microhemorrhage in posterior reversible encephalopathy syndrome using susceptibility-weighted imaging. AJNR Am J Neuroradiol 2012; 33: 896-903
    CrossrefPubMedGoogle Scholar
  • 98 Lupo JM, Chuang CF, Chang SM et al. 7-Tesla susceptibility-weighted imaging to assess the effects of radiotherapy on normal-appearing brain in patients with glioma. Int J Radiat Oncol Biol Phys 2012; 82: e493-500
    CrossrefGoogle Scholar
  • 99 Scheid R. Cerebral microbleeds in relation to brain trauma. In: Werring DJ, ed. Cerebral microbleeds: pathophysiology to clinical practice. Cambridge: University Press; 2011: 125-134
    CrossrefGoogle Scholar
  • 100 Charidimou A, Jager HR, Werring DJ. Cerebral microbleeds detection and mapping: principles, methodological aspects and rationale in vascular dementia. Exp Gerontol 2012; 47: 843-852
    CrossrefGoogle Scholar
  • 101 Raychaudhuri R, Batjer HH, Awad IA. Intracranial cavernous angioma: a practical review of clinical and biological aspects. Surg Neurol 2005; 63: 319-328 , discussion 328
    CrossrefGoogle Scholar
  • 102 Samarasekera N, Potter G, Al-Shahi Salman R. Cerebral microbleed mimics. In: Werring DJ, ed. Cerebral microbleeds: pathophysiology to clinical practice. Cambridge: University Press; 2011: 44-48
    CrossrefGoogle Scholar
  • 103 Teo JTH, Ramadan H, Gregoire SM et al. Can cerebral microbleeds cause an acute stroke syndrome?. Neurol Clin Practice 2011; 1: 75-77
    Google Scholar
  • 104 Watanabe A, Kobashi T. Lateral gaze disturbance due to cerebral microbleed in the medial lemniscus in the mid-pontine region: a case report. Neuroradiology 2005; 47: 908-911
    CrossrefGoogle Scholar
  • 105 Gorelick PB, Scuteri A, Black SE et al. Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2011; 42: 2672-2713
    CrossrefGoogle Scholar
  • 106 Hachinski V, Iadecola C, Petersen RC et al. National Institute of Neurological Disorders and Stroke – Canadian Stroke Network vascular cognitive impairment harmonization standards. Stroke 2006; 37: 2220-2241
    CrossrefGoogle Scholar
  • 107 Charidimou A, Werring DJ. Cerebral microbleeds and cognition in cerebrovascular disease: an update. J Neurol Sci 2012; 15: 50-55
    Google Scholar
  • 108 Werring DJ, Frazer DW, Coward LJ et al. Cognitive dysfunction in patients with cerebral microbleeds on T2*-weighted gradient-echo MRI. Brain 2004; 127: 2265-2275
    CrossrefGoogle Scholar
  • 109 Seo SW, Hwa Lee B, Kim EJ et al. Clinical significance of microbleeds in subcortical vascular dementia. Stroke 2007; 38: 1949-1951
    CrossrefGoogle Scholar
  • 110 Yakushiji Y, Nishiyama M, Yakushiji S et al. Brain microbleeds and global cognitive function in adults without neurological disorder. Stroke 2008; 39: 3323-3328
    CrossrefGoogle Scholar
  • 111 van Es AC, van der Grond J, de Craen AJ et al. Cerebral microbleeds and cognitive functioning in the PROSPER study. Neurology 2011; 77: 1446-1452
    CrossrefGoogle Scholar
  • 112 van Norden AG, van den Berg HA, de Laat KF et al. Frontal and temporal microbleeds are related to cognitive function: the Radboud University Nijmegen Diffusion Tensor and Magnetic Resonance Cohort (RUN DMC) Study. Stroke 2011; 42: 3382-3386
    CrossrefGoogle Scholar
  • 113 Poels MM, Ikram MA, van der Lugt A et al. Cerebral microbleeds are associated with worse cognitive function: the Rotterdam Scan Study. Neurology 2012; 78: 326-333
    CrossrefGoogle Scholar
  • 114 Greenberg SM, Eng JA, Ning M et al. Hemorrhage burden predicts recurrent intracerebral hemorrhage after lobar hemorrhage. Stroke 2004; 35: 1415-1420
    CrossrefGoogle Scholar
  • 115 Biffi A, Halpin A, Towfighi A et al. Aspirin and recurrent intracerebral hemorrhage in cerebral amyloid angiopathy. Neurology 2010; 75: 693-698
    CrossrefGoogle Scholar
  • 116 Thijs V, Lemmens R, Schoofs C et al. Microbleeds and the risk of recurrent stroke. Stroke 2010; 41: 2005-2009
    CrossrefGoogle Scholar
  • 117 Flaherty ML, Kissela B, Woo D et al. The increasing incidence of anticoagulant-associated intracerebral hemorrhage. Neurology 2007; 68: 116-121
    CrossrefGoogle Scholar
  • 118 Flaherty ML. Anticoagulant-associated intracerebral hemorrhage. Semin Neurol 2010; 30: 565-572
    Article in Thieme ConnectGoogle Scholar
  • 119 Lovelock CE, Molyneux AJ, Rothwell PM. Change in incidence and aetiology of intracerebral haemorrhage in Oxfordshire, UK, between 1981 and 2006: a population-based study. Lancet Neurol 2007; 6: 487-493
    CrossrefGoogle Scholar
  • 120 Fan YH, Mok VC, Lam WW et al. Cerebral microbleeds and white matter changes in patients hospitalized with lacunar infarcts. J Neurol 2004; 251: 537-541
    CrossrefGoogle Scholar
  • 121 Imaizumi T, Horita Y, Hashimoto Y et al. Dotlike hemeosiderin spots on T2*-weighted magnetic resonance imaging as a predictor of stroke recurrence: a prospective study. J Neurosurg 2004; 101: 915-920
    CrossrefGoogle Scholar
  • 122 Naka H, Nomura E, Takahashi T et al. Combinations of the presence or absence of cerebral microbleeds and advanced white matter hyperintensity as predictors of subsequent stroke types. AJNR Am J Neuroradiol 2006; 27: 830-835
    Google Scholar
  • 123 Soo YO, Yang SR, Lam WW et al. Risk vs benefit of anti-thrombotic therapy in ischaemic stroke patients with cerebral microbleeds. J Neurol 2008; 255: 1679-1686
    CrossrefGoogle Scholar
  • 124 Lovelock CE, Cordonnier C, Naka H et al. Antithrombotic drug use, cerebral microbleeds, and intracerebral hemorrhage: a systematic review of published and unpublished studies. Stroke 2010; 41: 1222-1228
    CrossrefGoogle Scholar
  • 125 Rosand J, Hylek EM, O’Donnell HC et al. Warfarin-associated hemorrhage and cerebral amyloid angiopathy: a genetic and pathologic study. Neurology 2000; 55: 947-951
    CrossrefGoogle Scholar
  • 126 Nicoll JA, Burnett C, Love S et al. High frequency of apolipoprotein E epsilon 2 allele in hemorrhage due to cerebral amyloid angiopathy. Ann Neurol 1997; 41: 716-721
    CrossrefGoogle Scholar
  • 127 Biff A, Sonni A, Anderson CD et al. Variants at APOE influence risk of deep and lobar intracerebral hemorrhage. Ann Neurol 2010; 68: 934-943
    CrossrefGoogle Scholar
  • 128 Charidimou A, Shakeshaft C, Werring DJ. Cerebral microbleeds on magnetic resonance imaging and anticoagulant-associated intracerebral hemorrhage risk. Front Neurol 2012; 3: 133
    Google Scholar
  • 129 Vinters HV. Cerebral amyloid angiopathy. A critical review. Stroke 1987; 18: 311-324
    CrossrefPubMedGoogle Scholar
  • 130 Passero S, Burgalassi L, D’Andrea P et al. Recurrence of bleeding in patients with primary intracerebral hemorrhage. Stroke 1995; 26: 1189-1192
    CrossrefGoogle Scholar
  • 131 Kidwell CS, Saver JL, Villablanca JP et al. Magnetic resonance imaging detection of microbleeds before thrombolysis: an emerging application. Stroke 2002; 33: 95-98
    CrossrefGoogle Scholar
  • 132 Fiehler J, Albers GW, Boulanger JM et al. Bleeding risk analysis in stroke imaging before thrombolysis (BRASIL): pooled analysis of T2*-weighted magnetic resonance imaging data from 570 patients. Stroke 2007; 38: 2738-2744
    CrossrefGoogle Scholar
  • 133 Shoamanesh A, Kwok CS, Lim PA et al. Postthrombolysis intracranial hemorrhage risk of cerebral microbleeds in acute stroke patients: a systematic review and meta-analysis. Int J Stroke 2012; ; DOI: DOI: 10.1111/j.1747-4949.2012.00869.x.
    Google Scholar
  • 134 Charidimou A, Kakar P, Fox Z et al. Cerebral microbleeds and the risk of intracerebral haemorrhage after thrombolysis for acute ischaemic stroke: systematic review and meta-analysis. J Neurol Neurosurg Psychiatry 2012; 84: 277-280
    Google Scholar
  • 135 McCarron MO, Nicoll JA. Cerebral amyloid angiopathy and thrombolysis-related intracerebral haemorrhage. Lancet Neurol 2004; 3: 484-492
    CrossrefGoogle Scholar
  • 136 Sloan MA, Price TR, Petito CK et al. Clinical features and pathogenesis of intracerebral hemorrhage after rt-PA and heparin therapy for acute myocardial infarction: the Thrombolysis in Myocardial Infarction (TIMI) II Pilot and Randomized Clinical Trial combined experience. Neurology 1995; 45: 649-658
    CrossrefGoogle Scholar
  • 137 Sperling R, Salloway S, Brooks DJ et al. Amyloid-related imaging abnormalities in patients with Alzheimer’s disease treated with bapineuzumab: a retrospective analysis. Lancet Neurol 2012; 11: 241-249
    CrossrefGoogle Scholar
  • 138 Nicoll JA, Wilkinson D, Holmes C et al. Neuropathology of human Alzeimer disease after immunization with amyloid-beta peptide: a case report. Nat Med 2003; 9: 448-452
    CrossrefGoogle Scholar
  • 139 Ferrer I, Boada Rovira M, Sanchez Guerra ML et al. Neuropathology and pathogenesis of encephalitis following amyloid-beta immunization in Alzheimer’s disease. Brain Pathol 2004; 14: 11-20
    CrossrefGoogle Scholar
  • 140 Staekenborg SS, Koedam EL, Hennemann WJ et al. Progression of mild cognitive impairment to dementia: contribution of cerebrovascular disease compared with medial temporal lobe atrophy. Stroke 2009; 40: 1269-1274
    CrossrefGoogle Scholar