Clinical neuroimaging in intracerebral haemorrhage related to cerebral small vessel disease: contemporary practice and emerging concepts

References

• van Asch Cj, Luitse MJ, Rinkel GJ, et al. Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: a systematic review and meta-analysis. Lancet Neurol. 2010;9(2):167–176.
   PubMed Web of Science ®Google Scholar
• Casolla B, Moulin S, Kyheng M, et al. Five-year risk of major ischemic and hemorrhagic events after intracerebral hemorrhage. Stroke. 2019;50:11001107.
   Web of Science ®Google Scholar
• Banerjee G, Wilson D, Ambler G, et al. Longer term stroke risk in intracerebral haemorrhage survivors. J Neurol Neurosurg Psychiatry. 2020;91(8):840–845.
   PubMed Web of Science ®Google Scholar
• Wardlaw JM, Smith C, Dichgans M. Small vessel disease: mechanisms and clinical implications. Lancet Neurol. 2019;18(7):684–696.
   PubMed Web of Science ®Google Scholar
• Jackson CA, Sudlow CL. Is hypertension a more frequent risk factor for deep than for lobar supratentorial intracerebral haemorrhage? J Neurol Neurosurg Psychiatry. 2006;77(11):1244–1252.
   PubMed Web of Science ®Google Scholar
• Hostettler IC, Seiffge DJ, Werring DJ. Intracerebral hemorrhage: an update on diagnosis and treatment. Expert Rev Neurother. 2019;19(7):679–694.
   PubMed Web of Science ®Google Scholar
• Goeldlin MB, Mueller A, Siepen BM, et al. Etiology, 3-month functional outcome and recurrent events in non-traumatic intracerebral hemorrhage. J Stroke. 2022;24(2):266–277.
   PubMed Web of Science ®Google Scholar
• Hilkens NA, van Asch CJJ, and Werring DJ, et al. Predicting the presence of macrovascular causes in non-traumatic intracerebral haemorrhage: the DIAGRAM prediction score. J Neurol Neurosurg Psychiatry. 2018;89(7):674–679.
   PubMed Web of Science ®Google Scholar
• Krishnamurthi RV, Ikeda T, Feigin VLG. Regional and country-specific burden of ischaemic stroke, intracerebral haemorrhage and subarachnoid haemorrhage: a systematic analysis of the global burden of disease study 2017. Neuroepidemiology. 2020;54(2):171–179.
   PubMed Web of Science ®Google Scholar
• Sakai K, Ueda M, Fukushima W, et al. Nationwide survey on cerebral amyloid angiopathy in Japan. Eur J Neurol. 2019;26(12):1487–1493.
   PubMed Web of Science ®Google Scholar
• Yakushiji Y, Tanaka J, Wilson D, et al. Proportion of intracerebral haemorrhage due to cerebral amyloid angiopathy in the east and west: comparison between single hospital centres in Japan and the United Kingdom. J Neurol Sci. 2020;416:117037.
   PubMed Web of Science ®Google Scholar
• Blanc C, Viguier A, Calviere L, et al. Underlying small vessel disease associated with mixed cerebral microbleeds. Front Neurol. 2019;10:1126.
   PubMed Web of Science ®Google Scholar
• Rodrigues MA, Samarasekera N, and Lerpiniere C, et al. The Edinburgh CT and genetic diagnostic criteria for lobar intracerebral haemorrhage associated with cerebral amyloid angiopathy: model development and diagnostic test accuracy study. Lancet Neurol. 2018;17(3):232–240.
   PubMed Web of Science ®Google Scholar
• Mancuso M, Arnold M, Bersano A, et al. Monogenic cerebral small-vessel diseases: diagnosis and therapy. Consensus recommendations of the European Academy of Neurology. Eur J Neurol. 2020;27(6):909–927.
   PubMed Web of Science ®Google Scholar
• Poon MT, Fonville AF, Al-Shahi Salman R. Long-term prognosis after intracerebral haemorrhage: systematic review and meta-analysis. J Neurol Neurosurg Psychiatry. 2014;85(6):660–667.
   PubMed Web of Science ®Google Scholar
• Demchuk AM, Dowlatshahi D, Rodriguez-Luna D, et al. Prediction of haematoma growth and outcome in patients with intracerebral haemorrhage using the CT-angiography spot sign (PREDICT): a prospective observational study. Lancet Neurol. 2012;11(4):307–314.
   PubMed Web of Science ®Google Scholar
• Morotti A, Boulouis G, Dowlatshahi D, et al. Standards for detecting, interpreting, and reporting noncontrast computed tomographic markers of intracerebral hemorrhage expansion. Ann Neurol. 2019;86(4):480–492.
   PubMed Web of Science ®Google Scholar
• Wilson D, Ogungbemi A, Ambler G, et al. Developing an algorithm to identify patients with intracerebral haemorrhage secondary to a macrovascular cause. Eur Stroke J. 2017;2(4):369–376.
   PubMed Web of Science ®Google Scholar
• van Asch Cj, Velthuis BK, Rinkel GJ, et al. Diagnostic yield and accuracy of CT angiography, MR angiography, and digital subtraction angiography for detection of macrovascular causes of intracerebral haemorrhage: prospective, multicentre cohort study. BMJ. 2015;351(nov09 2):h5762.
   PubMedGoogle Scholar
• Amukotuwa SA, Heit JJ, Marks MP, et al. Detection of cortical venous drainage and determination of the borden type of dural arteriovenous fistula by means of 3D pseudocontinuous arterial spin-labeling MRI. AJR Am J Roentgenol. 2016;207(1):163–169.
   PubMed Web of Science ®Google Scholar
• Wardlaw JM, Smith EE, and Biessels GJ, et al. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol. 2013;12(8):822–838.
   PubMed Web of Science ®Google Scholar
• Baldwin KJ, Cummings CL. Herpesvirus infections of the nervous system. Continuum (Minneap Minn). 2018;24(5, Neuroinfectious Disease):1349–1369.
   PubMedGoogle Scholar
• Sarti C, Picchioni A, Telese R, et al. “When should primary angiitis of the central nervous system (PACNS) be suspected?”: literature review and proposal of a preliminary screening algorithm. Neurol Sci. 2020;41(11):3135–3148.
   PubMed Web of Science ®Google Scholar
• Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol. 2010;9(7):689–701.
   PubMed Web of Science ®Google Scholar
• Gouw AA, Seewann A, van der Flier WM, et al. Heterogeneity of small vessel disease: a systematic review of MRI and histopathology correlations. J Neurol Neurosurg Psychiatry. 2011;82(2):126–135.
   PubMed Web of Science ®Google Scholar
• Charidimou A, Gang Q, Werring DJ. Sporadic cerebral amyloid angiopathy revisited: recent insights into pathophysiology and clinical spectrum. J Neurol Neurosurg Psychiatry. 2012;83(2):124–137.
   PubMed Web of Science ®Google Scholar
• Banerjee G, Carare R, Cordonnier C, et al. The increasing impact of cerebral amyloid angiopathy: essential new insights for clinical practice. Journal of Neurology, Neurosurgery & Psychiatry. 2017;88(11):982–994.
   PubMed Web of Science ®Google Scholar
• Case NF, Charlton A, Zwiers A, et al. Cerebral amyloid angiopathy is associated with executive dysfunction and mild cognitive impairment. Stroke. 2016;47(8):2010–2016.
   PubMed Web of Science ®Google Scholar
• Smith EE, Charidimou A, Ayata C, et al. Cerebral amyloid angiopathy–related transient focal neurologic episodes. Neurology. 2021;97(5):231–238.
   PubMed Web of Science ®Google Scholar
• Holling M, Jeibmann A, Fischer BR, et al. Histopathological analysis of intracerebral hemorrhage: implications for clinical management. Acta Neurochir (Wien). 2012;154(3):439–443.
   PubMed Web of Science ®Google Scholar
• Doden T, Sato H, Sasahara E, et al. Clinico-radiological characteristics and pathological diagnosis of cerebral amyloid angiopathy-related intracerebral hemorrhage. J Stroke Cerebrovasc Dis. 2016;25(7):1736–1745.
   PubMed Web of Science ®Google Scholar
• Greenberg SM, and Vonsattel JP. Diagnosis of cerebral amyloid angiopathy. Sensitivity and specificity of cortical biopsy. Stroke. 1997;28(7):1418–1422.
   PubMed Web of Science ®Google Scholar
• Guidoux C, Hauw JJ, Klein IF, et al. Amyloid angiopathy in brain hemorrhage: a postmortem neuropathological-magnetic resonance imaging study. Cerebrovascular Dis. 2018;45(3–4):124–131.
   PubMed Web of Science ®Google Scholar
• Auriel E, Charidimou A, Gurol ME, et al. Validation of clinicoradiological criteria for the diagnosis of cerebral amyloid angiopathy-related inflammation. JAMA Neurol. 2016;73(2):197–202.
   PubMed Web of Science ®Google Scholar
• Eng JA, Frosch MP, Choi K, et al. Clinical manifestations of cerebral amyloid angiopathy-related inflammation. Ann Neurol. 2004;55(2):250–256.
   PubMed Web of Science ®Google Scholar
• Scolding NJ, Joseph F, Kirby PA, et al. Abeta-related angiitis: primary angiitis of the central nervous system associated with cerebral amyloid angiopathy. Brain. 2005;128(3):500–515.
   PubMedGoogle Scholar
• Kinnecom C, Lev MH, Wendell L, et al. Course of cerebral amyloid angiopathy-related inflammation. Neurology. 2007;68(17):1411–1416.
   PubMed Web of Science ®Google Scholar
• Kirshner HS, Bradshaw M. The inflammatory form of cerebral amyloid angiopathy or “cerebral amyloid angiopathy-related inflammation” (CAARI). Curr Neurol Neurosci Rep. 2015;15(8):54.
   PubMed Web of Science ®Google Scholar
• 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(3):241–249.
   PubMed Web of Science ®Google Scholar
• Avgerinos KI, Ferrucci L, Kapogiannis D. Effects of monoclonal antibodies against amyloid-beta on clinical and biomarker outcomes and adverse event risks: a systematic review and meta-analysis of phase III RCTs in Alzheimer’s disease. Ageing Res Rev. 2021;68:101339.
   PubMed Web of Science ®Google Scholar
• Maat-Schieman M, Roos R, van Duinen S. Hereditary cerebral hemorrhage with amyloidosis-Dutch type. Neuropathology. 2005;25(4):288–297.
   PubMed Web of Science ®Google Scholar
• Martinez-Ramirez S, van Rooden S, Charidimou A, et al. Perivascular spaces volume in sporadic and hereditary (Dutch-type) cerebral amyloid angiopathy. Stroke. 2018;49(8):1913–1919.
   PubMed Web of Science ®Google Scholar
• van Rooden S, van Opstal AM, Labadie G, et al. Early magnetic resonance imaging and cognitive markers of hereditary cerebral amyloid angiopathy. Stroke. 2016;47(12):3041–3044.
   PubMed Web of Science ®Google Scholar
• Schultz AP, Kloet RW, Sohrabi HR, et al. Amyloid imaging of Dutch-type hereditary cerebral amyloid angiopathy carriers. Ann Neurol. 2019;86(4):616–625.
   PubMed Web of Science ®Google Scholar
• Schouten TM, de Vos F, van Rooden S, et al. Multiple approaches to diffusion magnetic resonance imaging in hereditary cerebral amyloid angiopathy mutation carriers. J Am Heart Assoc. 2019;8(3):e011288.
   PubMed Web of Science ®Google Scholar
• Choi JC. Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy: a genetic cause of cerebral small vessel disease. J Clin Neurol. 2010;6(1):1–9.
   PubMed Web of Science ®Google Scholar
• Ratelade J, Klug NR, Lombardi D, et al. Reducing hypermuscularization of the transitional segment between arterioles and capillaries protects against spontaneous intracerebral hemorrhage. Circulation. 2020;141(25):2078–2094.
   PubMed Web of Science ®Google Scholar
• Choi JC, Kang SY, Kang JH, et al. Intracerebral hemorrhages in CADASIL. Neurology. 2006;67(11):2042–2044.
   PubMed Web of Science ®Google Scholar
• Lee JS, Kang CH, Park SQ, et al. Clinical significance of cerebral microbleeds locations in CADASIL with R544C NOTCH3 mutation. PLoS One. 2015;10(2):e0118163.
   PubMed Web of Science ®Google Scholar
• Bersano A, Bedini G, Markus HS, et al. The role of clinical and neuroimaging features in the diagnosis of CADASIL. J Neurol. 2018;265(12):2934–2943.
   PubMed Web of Science ®Google Scholar
• Choi JC. Genetics of cerebral small vessel disease. J Stroke. 2015;17(1):7–16.
   PubMed Web of Science ®Google Scholar
• Mendioroz M, Fernández-Cadenas I, Del Río-Espinola A, et al. A missense HTRA1 mutation expands CARASIL syndrome to the Caucasian population. Neurology.2010;75.2033.DOI:10.1212/WNL.0b013e3181ff96ac.
   PubMed Web of Science ®Google Scholar
• Fukutake T. Cerebral autosomal recessive arteriopathy with subcortical infarcts and leukoencephalopathy (CARASIL): from discovery to gene identification. J Stroke Cerebrovasc Dis. 2011;20(2):85–93.
   PubMed Web of Science ®Google Scholar
• Lemmens R, Maugeri A, Niessen HW, et al. Novel COL4A1 mutations cause cerebral small vessel disease by haploinsufficiency. Hum Mol Genet. 2013;22(2):391–397.
   PubMed Web of Science ®Google Scholar
• Zagaglia S, Selch C, Nisevic JR, et al. Neurologic phenotypes associated withCOL4A1/ 2mutations. Neurology. 2018;91(22):e2078–e2088.
   PubMedGoogle Scholar
• Rannikmae K, Davies G, Thomson PA, et al. Common variation in COL4A1/COL4A2 is associated with sporadic cerebral small vessel disease. Neurology. 2015;84(9):918–926.
   PubMed Web of Science ®Google Scholar
• Rannikmae K, Sivakumaran V, Millar H, et al. COL4 is associated with lacunar ischemic stroke and deep ICH. Neurology. 2017;89(17):1829–1839.
   PubMed Web of Science ®Google Scholar
• Linn J, Halpin A, and Demaerel P, et al. Prevalence of superficial siderosis in patients with cerebral amyloid angiopathy. Neurology. 2010;74(17):1346–1350.
   PubMed Web of Science ®Google Scholar
• Charidimou A, Frosch MP, Al-Shahi Salman R, et al. Advancing diagnostic criteria for sporadic cerebral amyloid angiopathy: study protocol for a multicenter MRI-pathology validation of Boston criteria v2.0. Int J Stroke. 2019;14(9):956–971.
   PubMed Web of Science ®Google Scholar
• Werring DJ. CT scanning to diagnose CAA: back to the future? Lancet Neurol. 2018;17(3):197–198.
   PubMed Web of Science ®Google Scholar
• van Etten ES, Kaushik K, van Zwet EW, et al. Sensitivity of the Edinburgh criteria for lobar intracerebral hemorrhage in hereditary cerebral amyloid angiopathy. Stroke. 2020;51(12):3608–3612.
   PubMed Web of Science ®Google Scholar
• Ornello R, Colangeli E, Tommasino E, et al. Clinical usefulness of Edinburgh CT criteria in patients with lobar intracerebral hemorrhage. Eur Stroke J. 2021;6(1):36–43.
   PubMed Web of Science ®Google Scholar
• Appleton JP, Woodhouse LJ, Adami A, et al. Imaging markers of small vessel disease and brain frailty, and outcomes in acute stroke. Neurology. 2020;94(5):e439–e452.
   PubMed Web of Science ®Google Scholar
• Wardlaw JM, Valdes Hernandez MC, Munoz-Maniega S. What are white matter hyperintensities made of? Relevance to vascular cognitive impairment. J Am Heart Assoc. 2015;4(6):001140.
   PubMed Web of Science ®Google Scholar
• Haller S, Vernooij MW, Kuijer JPA, et al. Cerebral microbleeds: imaging and clinical significance. Radiology. 2018;287(1):11–28.
   PubMed Web of Science ®Google Scholar
• Gregoire SM, Chaudhary UJ, Brown MM, et al. The microbleed anatomical rating scale (Mars): reliability of a tool to map brain microbleeds. Neurology. 2009;73(21):1759–1766.
   PubMed Web of Science ®Google Scholar
• 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(4):637–642.
   PubMed Web of Science ®Google Scholar
• Conijn MM, Hoogduin JM, van der Graaf Y, et al. Microbleeds, lacunar infarcts, white matter lesions and cerebrovascular reactivity – a 7 T study. Neuroimage. 2012;59(2):950–956.
   PubMed Web of Science ®Google Scholar
• Graff-Radford J, Botha H, Rabinstein AA, et al. Cerebral microbleeds: prevalence and relationship to amyloid burden. Neurology. 2019;92(3):e253–e262.
   PubMed Web of Science ®Google Scholar
• Haller S, Montandon ML, Lazeyras F, et al. Radiologic-histopathologic correlation of cerebral microbleeds using pre-mortem and post-mortem MRI. PLoS One. 2016;11(12):e0167743.
   PubMed Web of Science ®Google Scholar
• Pasi M, Pongpitakmetha T, Charidimou A, et al. Cerebellar microbleed distribution patterns and cerebral amyloid angiopathy. Stroke. 2019;50(7):1727–1733.
   PubMed Web of Science ®Google Scholar
• Renard D, Tatu L, Thouvenot E. Infratentorial cerebral microbleeds in patients with cerebral amyloid angiopathy. J Stroke Cerebrovasc Dis. 2018;27(9):2534–2537.
   PubMed Web of Science ®Google Scholar
• Tsai HH, Pasi M, Tsai LK, et al. Superficial cerebellar microbleeds and cerebral amyloid angiopathy: a magnetic resonance imaging/positron emission tomography study. Stroke. 2020;51(1):202–208.
   PubMed Web of Science ®Google Scholar
• Pasi M, Marini S, Morotti A, et al. Cerebellar hematoma location: implications for the underlying microangiopathy. Stroke. 2018;49(1):207–210.
   PubMed Web of Science ®Google Scholar
• Charidimou A, Linn J, Vernooij MW, et al. Cortical superficial siderosis: detection and clinical significance in cerebral amyloid angiopathy and related conditions. Brain. 2015;138(8):2126–2139.
   PubMedGoogle Scholar
• De Reuck J, Deramecourt V, Cordonnier C, et al. Detection of microbleeds in post-mortem brains of patients with frontotemporal lobar degeneration: a 7.0-Tesla magnetic resonance imaging study with neuropathological correlates. Eur J Neurol. 2012;19(10):1355–1360.
   PubMed Web of Science ®Google Scholar
• Charidimou A, Boulouis G, Roongpiboonsopit D, et al. Cortical superficial siderosis multifocality in cerebral amyloid angiopathy: a prospective study. Neurology. 2017;89(21):2128–2135.
   PubMed Web of Science ®Google Scholar
• Charidimou A, Perosa V, Frosch MP, et al. Neuropathological correlates of cortical superficial siderosis in cerebral amyloid angiopathy. Brain. 2020;143(11):3343–3351.
   PubMedGoogle Scholar
• Charidimou A, Boulouis G, Fotiadis P, et al. Acute convexity subarachnoid haemorrhage and cortical superficial siderosis in probable cerebral amyloid angiopathy without lobar haemorrhage. Journal of Neurology, Neurosurgery & Psychiatry. 2018;89(4):397–403.
   PubMed Web of Science ®Google Scholar
• Takeda S, Yamazaki K, Miyakawa T, et al. Subcortical hematoma caused by cerebral amyloid angiopathy: does the first evidence of hemorrhage occur in the subarachnoid space? Neuropathology. 2003;23(4):254–261.
   PubMed Web of Science ®Google Scholar
• Boulouis G, Charidimou A, Jessel MJ, et al. Small vessel disease burden in cerebral amyloid angiopathy without symptomatic hemorrhage. Neurology. 2017;88(9):878–884.
   PubMed Web of Science ®Google Scholar
• Charidimou A, Jager RH, Fox Z, et al. Prevalence and mechanisms of cortical superficial siderosis in cerebral amyloid angiopathy. Neurology. 2013;81(7):626–632.
   PubMed Web of Science ®Google Scholar
• Boulouis G, van Etten ES, Charidimou A, et al. Association of key magnetic resonance imaging markers of cerebral small vessel disease with hematoma volume and expansion in patients with lobar and deep intracerebral hemorrhage. JAMA Neurol. 2016;73(12):1440–1447.
   PubMed Web of Science ®Google Scholar
• Charidimou A, Imaizumi T, Moulin S, et al. Brain hemorrhage recurrence, small vessel disease type, and cerebral microbleeds: a meta-analysis. Neurology. 2017;89(8):820–829.
   PubMed Web of Science ®Google Scholar
• Charidimou A, Peeters AP, Jager R, et al. Cortical superficial siderosis and intracerebral hemorrhage risk in cerebral amyloid angiopathy. Neurology. 2013;81(19):1666–1673.
   PubMed Web of Science ®Google Scholar
• Rajani RM, Quick S, Ruigrok SR, et al. Reversal of endothelial dysfunction reduces white matter vulnerability in cerebral small vessel disease in rats. Sci Transl Med. 2018;10(448). DOI:10.1126/scitranslmed.aam9507
   PubMed Web of Science ®Google Scholar
• Munoz Maniega S, Chappell FM, Valdes Hernandez MC, et al. Integrity of normal-appearing white matter: influence of age, visible lesion burden and hypertension in patients with small-vessel disease. J Cereb Blood Flow Metab. 2017;37(2):644–656.
   PubMed Web of Science ®Google Scholar
• Duering M, Finsterwalder S, Baykara E, et al. Free water determines diffusion alterations and clinical status in cerebral small vessel disease. Alzheimer’s & Dementia. 2018;14(6):764–774.
   PubMed Web of Science ®Google Scholar
• Fazekas F, Chawluk JB, Alavi A, et al. MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol. 1987;149(2):351–356.
   PubMed Web of Science ®Google Scholar
• van Swieten JC, Hijdra A, Koudstaal PJ, et al. Grading white matter lesions on CT and MRI: a simple scale. J Neurol Neurosurg Psychiatry. 1990;53(12):1080–1083.
   PubMed Web of Science ®Google Scholar
• Charidimou A, Boulouis G, Haley K, et al. White matter hyperintensity patterns in cerebral amyloid angiopathy and hypertensive arteriopathy. Neurology. 2016;86(6):505–511.
   PubMed Web of Science ®Google Scholar
• Renard D, Tatu L, Demattei C, et al. Characterizing deep white matter hyperintensities in patients with symptomatic isolated cortical superficial siderosis. J Stroke Cerebrovasc Dis. 2017;26(3):465–469.
   PubMed Web of Science ®Google Scholar
• Doubal FN, MacLullich AMJ, Ferguson KJ, et al. Enlarged perivascular spaces on MRI are a feature of cerebral small vessel disease. Stroke. 2010;41(3):450–454.
   PubMed Web of Science ®Google Scholar
• Charidimou A, Meegahage R, Fox Z, et al. Enlarged perivascular spaces as a marker of underlying arteriopathy in intracerebral haemorrhage: a multicentre MRI cohort study. J Neurol Neurosurg Psychiatry. 2013;84(6):624–629.
   PubMed Web of Science ®Google Scholar
• Charidimou A, Jaunmuktane Z, Baron JC, et al. White matter perivascular spaces: an MRI marker in pathology-proven cerebral amyloid angiopathy? Neurology. 2014;82(1):57–62.
   PubMed Web of Science ®Google Scholar
• Greenberg SM, Charidimou A. Diagnosis of cerebral amyloid angiopathy: evolution of the Boston criteria. Stroke. 2018;49(2):491–497.
   PubMed Web of Science ®Google Scholar
• Charidimou A, Boulouis G, Frosch M, et al. Abstract 36: the Boston criteria V2.0 for cerebral amyloid angiopathy: updated criteria and multicenter MRI-Neuropathology validation. Stroke. 2021;52(Suppl_1):A36–A36.
   Google Scholar
• Best JG, Barbato C, Ambler G, et al. Association of enlarged perivascular spaces and anticoagulant-related intracranial hemorrhage. Neurology. 2020;95(16):e2192–e2199.
   PubMed Web of Science ®Google Scholar
• Pasi M, Boulouis G, Fotiadis P, et al. Distribution of lacunes in cerebral amyloid angiopathy and hypertensive small vessel disease. Neurology. 2017;88(23):2162–2168.
   PubMed Web of Science ®Google Scholar
• Duering M, Csanadi E, Gesierich B, et al. Incident lacunes preferentially localize to the edge of white matter hyperintensities: insights into the pathophysiology of cerebral small vessel disease. Brain. 2013;136(9):2717–2726.
   PubMedGoogle Scholar
• Molina C, Sabin JA, Montaner J, et al. Impaired cerebrovascular reactivity as a risk marker for first-ever lacunar infarction: a case-control study. Stroke. 1999;30(11):2296–2301.
   PubMed Web of Science ®Google Scholar
• Boulanger M, Schneckenburger R, Join-Lambert C, et al. Diffusion-weighted imaging hyperintensities in subtypes of acute intracerebral hemorrhage. Stroke. 2018;STROKEAHA118021407. DOI:10.1161/STROKEAHA.118.021407.
   PubMedGoogle Scholar
• Wu B, Yao X, Lei C, et al. Enlarged perivascular spaces and small diffusion-weighted lesions in intracerebral hemorrhage. Neurology. 2015;85(23):2045–2052.
   PubMed Web of Science ®Google Scholar
• Prabhakaran S, Naidech AM. Ischemic brain injury after intracerebral hemorrhage: a critical review. Stroke. 2012;43(8):2258–2263.
   PubMed Web of Science ®Google Scholar
• Auriel E, Gurol ME, Ayres A, et al. Characteristic distributions of intracerebral hemorrhage-associated diffusion-weighted lesions. Neurology. 2012;79(24):2335–2341.
   PubMed Web of Science ®Google Scholar
• Beitzke M, Enzinger C, Pichler A, et al. Acute diffusion-weighted imaging lesions in cerebral amyloid angiopathy-related convexal subarachnoid hemorrhage. J Cereb Blood Flow Metab. 2018;38(2):225–229.
   PubMed Web of Science ®Google Scholar
• Gregoire SM, Charidimou A, Gadapa N, et al. Acute ischaemic brain lesions in intracerebral haemorrhage: multicentre cross-sectional magnetic resonance imaging study. Brain. 2011;134(8):2376–2386.
   PubMedGoogle Scholar
• Charidimou A, Schmitt A, Wilson D, et al. The cerebral haemorrhage anatomical rating inStrument (CHARTS): development and assessment of reliability. J Neurol Sci. 2017;372:178–183.
   PubMed Web of Science ®Google Scholar
• Biffi A, Anderson CD, Falcone GJ, et al. Novel insights into the genetics of intracerebral hemorrhage. Stroke. 2013;44(6_suppl_1):S137.
   PubMed Web of Science ®Google Scholar
• Biffi A, Anderson CD, Jagiella JM, et al. APOE genotype and extent of bleeding and outcome in lobar intracerebral haemorrhage: a genetic association study. Lancet Neurol. 2011;10(8):702–709.
   PubMed Web of Science ®Google Scholar
• Biffi A, Sonni A, Anderson CD, et al. Variants at APOE influence risk of deep and lobar intracerebral hemorrhage. Ann Neurol. 2010;68(6):934–943.
   PubMed Web of Science ®Google Scholar
• Biffi A, Urday S, Kubiszewski P, et al. Combining imaging and genetics to predict recurrence of anticoagulation-associated intracerebral hemorrhage. Stroke. 2020;51(7):2153–2160.
   PubMed Web of Science ®Google Scholar
• Charidimou A, Zonneveld HI, Shams S, et al. APOE and cortical superficial siderosis in CAA. Neurology. 2019;93(4):e358–e371.
   PubMed Web of Science ®Google Scholar
• Ye X, Li G, Liu X, et al. Apolipoprotein E genotype predicts subarachnoid extension in spontaneous intracerebral haemorrhage. Eur J Neurol. 2021;28(6):1992–1999.
   PubMed Web of Science ®Google Scholar
• Charidimou A, Friedrich JO, Greenberg SM, et al. Core cerebrospinal fluid biomarker profile in cerebral amyloid angiopathy: a meta-analysis. Neurology. 2018;90(9):e754–e762.
   PubMed Web of Science ®Google Scholar
• Catak C, Zedde M, Malik R, et al. Decreased CSF levels of ss-amyloid in patients with cortical superficial siderosis. Front Neurol. 2019;10:439.
   PubMed Web of Science ®Google Scholar
• Yamada M. Cerebral amyloid angiopathy: emerging concepts. Journal of Stroke. 2015;17(1):17–30.
   PubMed Web of Science ®Google Scholar
• Chang S, Zhang J, Liu T, et al. Quantitative susceptibility mapping of intracerebral hemorrhages at various stages. J Magn Reson Imaging. 2016;44(2): 420–425.
   PubMed Web of Science ®Google Scholar
• Koyama T, Tsuji M, Nishimura H, et al. Diffusion tensor imaging for intracerebral hemorrhage outcome prediction: comparison using data from the Corona radiata/internal capsule and the cerebral peduncle. J Stroke Cerebrovasc Dis. 2013;22(1):72–79.
   PubMed Web of Science ®Google Scholar
• Goh SY, Irimia A, Torgerson CM, et al. Longitudinal quantification and visualization of intracerebral haemorrhage using multimodal magnetic resonance and diffusion tensor imaging. Brain Injury. 2015;29(4):438–445.
   PubMed Web of Science ®Google Scholar
• Cheng CY, Hsu CY, Huang YC, et al. Motor outcome of deep intracerebral haemorrhage in diffusion tensor imaging: comparison of data from different locations along the corticospinal tract. Neurol Res. 2015;37(9):774–781.
   PubMed Web of Science ®Google Scholar
• Kumar P, Yadav AK, Misra S, et al. Prediction of upper extremity motor recovery after subacute intracerebral hemorrhage through diffusion tensor imaging: a systematic review and meta-analysis. Neuroradiology. 2016;58(10):1043–1050.
   PubMed Web of Science ®Google Scholar
• Baykara E, Gesierich B, Adam R, et al. A novel imaging marker for small vessel disease based on skeletonization of white matter tracts and diffusion histograms. Ann Neurol. 2016;80(4):581–592.
   PubMed Web of Science ®Google Scholar
• Conijn MM, Geerlings MI, Biessels GJ, et al. Cerebral microbleeds on MR imaging: comparison between 1.5 and 7T. AJNR Am J Neuroradiol. 2011;32(6):1043–1049.
   PubMed Web of Science ®Google Scholar
• Koemans EA, Voigt S, Rasing I, et al. Striped occipital cortex and intragyral hemorrhage: novel magnetic resonance imaging markers for cerebral amyloid angiopathy. Int J Stroke. 2021;16(9):1031–1038.
   PubMed Web of Science ®Google Scholar
• Bulk M, Moursel LG, van der Graaf LM, et al. Cerebral amyloid angiopathy with vascular iron accumulation and calcification. Stroke. 2018;49(9):2081–2087.
   PubMed Web of Science ®Google Scholar
• Koemans EA, van Etten ES, van Opstal AM, et al. Innovative magnetic resonance imaging markers of hereditary cerebral amyloid angiopathy at 7 Tesla. Stroke. 2018;49(6):1518–1520.
   PubMed Web of Science ®Google Scholar
• Ni J, Auriel E, Martinez-Ramirez S, et al. Cortical localization of microbleeds in cerebral amyloid angiopathy: an ultra high-field 7T MRI study. J Alzheimers Dis. 2015;43(4):1325–1330.
   PubMed Web of Science ®Google Scholar
• van Veluw Sj, Jolink WM, Hendrikse J, et al. Cortical microinfarcts on 7T MRI in patients with spontaneous intracerebral hemorrhage. J Cereb Blood Flow Metab. 2014;34(7):1104–1106.
   PubMed Web of Science ®Google Scholar
• Liem MK, Lesnik Oberstein SA, Versluis MJ, et al. 7 T MRI reveals diffuse iron deposition in putamen and caudate nucleus in CADASIL. J Neurol Neurosurg Psychiatry. 2012;83(12):1180–1185.
   PubMed Web of Science ®Google Scholar
• Bonnier G, Fischi-Gomez E, Roche A, et al. Personalized pathology maps to quantify diffuse and focal brain damage. NeuroImage Clin. 2019;21:101607.
   PubMed Web of Science ®Google Scholar
• Ma D, Gulani V, Seiberlich N, et al. Magnetic resonance fingerprinting. Nature. 2013;495(7440):187–192.
   PubMed Web of Science ®Google Scholar
• Charidimou A, Farid K, Baron JC. Amyloid-PET in sporadic cerebral amyloid angiopathy: a diagnostic accuracy meta-analysis. Neurology. 2017;89(14):14901498.
   Web of Science ®Google Scholar
• Baron JC, Farid K, Dolan E, et al. Diagnostic utility of amyloid PET in cerebral amyloid angiopathy-related symptomatic intracerebral hemorrhage. J Cereb Blood Flow Metab. 2014;34(5):753–758.
   PubMed Web of Science ®Google Scholar
• Gurol ME, Becker JA, Fotiadis P, et al. Florbetapir-PET to diagnose cerebral amyloid angiopathy: a prospective study. Neurology. 2016;87(19):2043–2049.
   PubMed Web of Science ®Google Scholar
• Raposo N, Planton M, Peran P, et al. Florbetapir imaging in cerebral amyloid angiopathy-related hemorrhages. Neurology. 2017;89(7):697–704.
   PubMed Web of Science ®Google Scholar
• Tsai HH, Pasi M, Tsai LK, et al. Microangiopathy underlying mixed-location intracerebral hemorrhages/microbleeds: a PiB-PET study. Neurology. 2019;92(8):e774–e781.
   PubMed Web of Science ®Google Scholar
• Tsai HH, Tsai LK, Chen YF, et al. Correlation of cerebral microbleed distribution to amyloid burden in patients with primary intracerebral hemorrhage. Sci Rep. 2017;7(1):44715.
   PubMedGoogle Scholar
• Meretoja A, Strbian D, and Putaala J, et al. SMASH-U: a proposal for etiologic classification of intracerebral hemorrhage. Stroke. 2012;43(10):2592–2597.
   PubMed Web of Science ®Google Scholar
• Marti-Fabregas J, Prats-Sanchez L, and Martinez-Domeno A, et al. The H-ATOMIC criteria for the etiologic classification of patients with intracerebral hemorrhage. PLoS One. 2016;11(6):e0156992.
   PubMed Web of Science ®Google Scholar
• Zanon Zotin MC, Sveikata L, Viswanathan A, et al. Cerebral small vessel disease and vascular cognitive impairment: from diagnosis to management. Curr Opin Neurol. 2021;34(2):246–257.
   PubMed Web of Science ®Google Scholar
• Chantran Y, Capron J, Alamowitch S, et al. Anti-abeta antibodies and cerebral amyloid angiopathy complications. Front Immunol. 2019;10:1534.
   PubMed Web of Science ®Google Scholar
• Blevins BL, Vinters HV, Love S, et al. Brain arteriolosclerosis. Acta Neuropathol. 2021;141(1):1–24.
   PubMed Web of Science ®Google Scholar
• DiFrancesco JC, Longoni M, Piazza F. Anti-Aβ autoantibodies in amyloid related imaging abnormalities (aria): candidate biomarker for immunotherapy in alzheimer’s disease and cerebral amyloid angiopathy. Front Neurol. 2015;6:207.
   PubMed Web of Science ®Google Scholar
• Carpenter AM, Singh IP, Gandhi CD, et al. Genetic risk factors for spontaneous intracerebral haemorrhage. Nat Rev Neurol. 2016;12(1):40–49.
   PubMed Web of Science ®Google Scholar
• Cao Y, Adamcik J, Diener M, et al. Different folding states from the same protein sequence determine reversible vs irreversible amyloid fate. J Am Chem Soc. 2021;143(30):11473–11481.
   PubMed Web of Science ®Google Scholar