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Current Molecular Medicine

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ISSN (Print): 1566-5240
ISSN (Online): 1875-5666

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Review Article

Brain MRI in Monogenic Cerebral Small Vessel Diseases: A Practical Handbook

Author(s): Leonardo Ulivi, Mirco Cosottini, Gianmichele Migaleddu, Giovanni Orlandi, Nicola Giannini, Gabriele Siciliano and Michelangelo Mancuso*

Volume 22, Issue 4, 2022

Published on: 03 August, 2021

Page: [300 - 311] Pages: 12

DOI: 10.2174/1566524021666210510164003

Price: $65

Abstract

Monogenic cerebral small vessel diseases are a topic of growing interest, as several genes responsible have been recently described, and new sequencing techniques such as Next-generation sequencing are available. Brain imaging is significant for the detection of these diseases. Since it is often performed at an initial stage, an MRI is a key to selecting patients for genetic testing and for interpreting nextgeneration sequencing reports. In addition, neuroimaging can be helpful in describing the underlying pathological mechanisms involved in cerebral small vessel disease. In this review, we aim to provide neurologists and stroke physicians with an up-to-date overview of the current neuroimaging knowledge on monogenic small vessel diseases.

Keywords: Small vessels disease, monogenic, MRI, CADASIL, CARASIL, CARASAL, Fabry Disease, COL4, RCVL-S.

« Previous Next »
[1]
Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 2010; 9(7): 689-701.
[http://dx.doi.org/10.1016/S1474-4422(10)70104-6]
[2]
Baykara E, Gesierich B, Adam R, et al. Alzheimer’s Disease Neuroimaging Initiative. A Novel Imaging Marker for Small Vessel Disease Based on Skeletonization of White Matter Tracts and Diffusion Histograms. Ann Neurol 2016; 80(4): 581-92.
[http://dx.doi.org/10.1002/ana.24758] [PMID: 27518166]
[3]
Duyn JH, Schenck J. Contributions to magnetic susceptibility of brain tissue. NMR Biomed 2017; 30(4)
[http://dx.doi.org/10.1002/nbm.3546] [PMID: 27240118]
[4]
Sirol M, Fayad VF, Plaque Imaging ZA. Plaque Imaging and Characterization Using Magnetic Resonance Imaging: Towards Molecular Assessment. Current Molecular Medicine 2006; 6: 541-8. Available from: http://www.eurekaselect.com/node/56490/article
[5]
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(3): 256-9.
[http://dx.doi.org/10.1038/ng0393-256] [PMID: 8485581]
[6]
Yamamoto Y, Craggs L, Baumann M, Kalimo H, Kalaria RN. Review: molecular genetics and pathology of hereditary small vessel diseases of the brain. Neuropathol Appl Neurobiol 2011; 37(1): 94-113.
[http://dx.doi.org/10.1111/j.1365-2990.2010.01147.x] [PMID: 21062344]
[7]
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): 909-27.
[http://dx.doi.org/10.1111/ene.14183] [PMID: 32196841]
[8]
Di Donato I, Bianchi S, De Stefano N, et al. Cerebral Autosomal Dominant Arteriopathy with Subcortical Infarcts and Leukoencephalopathy (CADASIL) as a model of small vessel disease: Update on clinical, diagnostic, and management aspects. BMC Medicine 2017; 2415(1): 41.
[9]
Joutel A, Corpechot C, Ducros A, et al. Notch3 mutations in CADASIL, a hereditary adult-onset condition causing stroke and dementia. Nature 1996; 383(6602): 707-10.
[http://dx.doi.org/10.1038/383707a0] [PMID: 8878478]
[10]
Morroni M, Marzioni D, Ragno M, et al. Role of electron microscopy in the diagnosis of cadasil syndrome: a study of 32 patients. PLoS One 2013; 8(6): e65482.
[http://dx.doi.org/10.1371/journal.pone.0065482] [PMID: 23799017]
[11]
Desmond DW, Moroney JT, Lynch T, Chan S, Chin SS, Mohr JP. The natural history of CADASIL: a pooled analysis of previously published cases. Stroke 1999; 30(6): 1230-3.
[http://dx.doi.org/10.1161/01.STR.30.6.1230] [PMID: 10356105]
[12]
O’Sullivan M, Jarosz JM, Martin RJ, Deasy N, Powell JF, Markus HS. MRI hyperintensities of the temporal lobe and external capsule in patients with CADASIL. Neurology 2001; 56(5): 628-34.
[http://dx.doi.org/10.1212/WNL.56.5.628] [PMID: 11245715]
[13]
Markus HS, Martin RJ, Simpson MA, Dong YB, Ali N, Crosby AH, et al. Diagnostic strategies in CADASIL. Neurology Oct; 2002; 59(8): 1134-8.
[http://dx.doi.org/10.1212/WNL.59.8.1134]
[14]
Yanagawa S, Ito N, Arima K, Ikeda S. Cerebral autosomal recessive arteriopathy with subcortical infarcts and leukoencephalopathy. Neurology 2002; 58(5): 817-20.
[http://dx.doi.org/10.1212/WNL.58.5.817] [PMID: 11889251]
[15]
Verdura E, Hervé D, Bergametti F, et al. Disruption of a miR-29 binding site leading to COL4A1 upregulation causes pontine autosomal dominant microangiopathy with leukoencephalopathy. Ann Neurol 2016; 80(5): 741-53.
[http://dx.doi.org/10.1002/ana.24782] [PMID: 27666438]
[16]
Bersano A, Bedini G, Markus HS, et al. Lombardia GENS-group The role of clinical and neuroimaging features in the diagnosis of CADASIL. J Neurol 2018; 265(12): 2934-43.
[http://dx.doi.org/10.1007/s00415-018-9072-8] [PMID: 30311053]
[17]
Singhal S, Rich P, Markus HS. The spatial distribution of MR imaging abnormalities in cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalo-pathy and their relationship to age and clinical features. AJNR Am J Neuroradiol 2005; 26(10): 2481-7.
[PMID: 16286388]
[18]
Ayrignac X, Carra-Dalliere C, Menjot de Champfleur N, et al. Adult-onset genetic leukoencephalopathies: a MRI pattern-based approach in a comprehensive study of 154 patients. Brain 2015; 138(Pt 2): 284-92.
[http://dx.doi.org/10.1093/brain/awu353] [PMID: 25527826]
[19]
van den Boom R, Lesnik Oberstein SAJ, Ferrari MD, Haan J, van Buchem MA. Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy: MR imaging findings at different ages--3rd-6th decades. Radiology 2003; 229(3): 683-90.
[http://dx.doi.org/10.1148/radiol.2293021354] [PMID: 14593195]
[20]
Pescini F, Nannucci S, Bertaccini B, et al. The Cerebral Autosomal-Dominant Arteriopathy With Subcortical Infarcts and Leukoencephalopathy (CADASIL) Scale: a screening tool to select patients for NOTCH3 gene analysis. Stroke 2012; 43(11): 2871-6.
[http://dx.doi.org/10.1161/STROKEAHA.112.665927] [PMID: 22996955]
[21]
Dichgans M, Holtmannspötter M, Herzog J, Peters N, Bergmann M, Yousry TA. Cerebral microbleeds in CADASIL: a gradient-echo magnetic resonance imaging and autopsy study. Stroke 2002; 33(1): 67-71.
[http://dx.doi.org/10.1161/hs0102.100885] [PMID: 11779891]
[22]
Yamamoto Y, Ihara M, Tham C, et al. Neuropathological correlates of temporal pole white matter hyperintensities in CADASIL. Stroke 2009; 40(6): 2004-11.
[http://dx.doi.org/10.1161/STROKEAHA.108.528299] [PMID: 19359623]
[23]
Duering M, Konieczny MJ, Tiedt S, et al. Serum neurofilament light chain levels are related to small vessel disease burden. J Stroke 2018; 20(2): 228-38.
[http://dx.doi.org/10.5853/jos.2017.02565] [PMID: 29886723]
[24]
Molko N, Pappata S, Mangin JF, et al. Monitoring disease progression in CADASIL with diffusion magnetic resonance imaging: a study with whole brain histogram analysis. Stroke 2002; 33(12): 2902-8.
[http://dx.doi.org/10.1161/01.STR.0000041681.25514.22] [PMID: 12468789]
[25]
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): 1180-5.
[http://dx.doi.org/10.1136/jnnp-2012-302545] [PMID: 22923513]
[26]
Viswanathan A, Gray F, Bousser MG, Baudrimont M, Chabriat H. Cortical neuronal apoptosis in CADASIL. Stroke 2006; 37(11): 2690-5.
[http://dx.doi.org/10.1161/01.STR.0000245091.28429.6a] [PMID: 17008611]
[27]
O’Sullivan M, Singhal S, Charlton R, Markus HS. Diffusion tensor imaging of thalamus correlates with cognition in CADASIL without dementia. Neurology 2004; 62(5): 702-7.
[http://dx.doi.org/10.1212/01.WNL.0000113760.72706.D2] [PMID: 15007117]
[28]
Dichgans M, Filippi M, Brüning R, et al. Quantitative MRI in CADASIL: correlation with disability and cognitive performance. Neurology 1999; 52(7): 1361-7.
[http://dx.doi.org/10.1212/WNL.52.7.1361] [PMID: 10227618]
[29]
Yousry TA, Seelos K, Mayer M, et al. Characteristic MR lesion pattern and correlation of T1 and T2 lesion volume with neurologic and neuropsychological findings in cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL). AJNR Am J Neuroradiol 1999; 20(1): 91-100.
[PMID: 9974062]
[30]
Tuladhar AM, van Norden AGW, de Laat KF, et al. White matter integrity in small vessel disease is related to cognition. Neuroimage Clin 2015; 7: 518-24.
[http://dx.doi.org/10.1016/j.nicl.2015.02.003] [PMID: 25737960]
[31]
Duchesnay E, Hadj Selem F, De Guio F, et al. Different types of white matter hyperintensities in CADASIL. Front Neurol 2018; 9: 526.
[http://dx.doi.org/10.3389/fneur.2018.00526] [PMID: 30042721]
[32]
Lesnik Oberstein SAJ, van den Boom R, van Buchem MA, et al. Dutch CADASIL Research Group Cerebral microbleeds in CADASIL. Neurology 2001; 57(6): 1066-70.
[http://dx.doi.org/10.1212/WNL.57.6.1066] [PMID: 11571335]
[33]
Viswanathan A, Gschwendtner A, Guichard JP, et al. Lacunar lesions are independently associated with disability and cognitive impairment in CADASIL. Neurology 2007; 69(2): 172-9.
[http://dx.doi.org/10.1212/01.wnl.0000265221.05610.70] [PMID: 17620550]
[34]
Jouvent E, Duchesnay E, Hadj-Selem F, et al. Prediction of 3-year clinical course in CADASIL. Neurology 2016; 87(17): 1787-95.
[http://dx.doi.org/10.1212/WNL.0000000000003252] [PMID: 27694265]
[35]
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(9): 1629-36.
[http://dx.doi.org/10.1016/j.neurobiolaging.2008.09.001] [PMID: 18926602]
[36]
O’Sullivan M, Ngo E, Viswanathan A, et al. Hippocampal volume is an independent predictor of cognitive performance in CADASIL. Neurobiol Aging 2009; 30(6): 890-7.
[http://dx.doi.org/10.1016/j.neurobiolaging.2007.09.002] [PMID: 17963999]
[37]
O’Sullivan M, Morris RG, Huckstep B, Jones DK, Williams SCR, Markus HS. Diffusion tensor MRI correlates with exe-cutive dysfunction in patients with ischaemic leukoaraiosis. J Neurol Neurosurg Psychiatry 2004; 75(3): 441-7.
[http://dx.doi.org/10.1136/jnnp.2003.014910] [PMID: 14966162]
[38]
Hara K, Shiga A, Fukutake T, et al. Association of HTRA1 mutations and familial ischemic cerebral small-vessel disease. N Engl J Med 2009; 360(17): 1729-39.
[http://dx.doi.org/10.1056/NEJMoa0801560] [PMID: 19387015]
[39]
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.
[http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2010.11.008] [PMID: 21215656]
[40]
Bianchi S, Di Palma C, Gallus GN, et al. Two novel HTRA1 mutations in a European CARASIL patient. Neurology 2014; 82(10): 898-900.
[http://dx.doi.org/10.1212/WNL.0000000000000202] [PMID: 24500651]
[41]
Ibrahimi M, Nozaki H, Lee A, Onodera O, Reichwein R, Wicklund M, et al. A CARASIL patient from americas with novel mutation and atypical features: Case presentation and literature review. Cerebrovascular Diseases 2017; 44(3-4): 135-40.
[42]
Nozaki H, Sekine Y, Fukutake T, et al. Characteristic features and progression of abnormalities on MRI for CARASIL. Neurology 2015; 85(5): 459-63.
[http://dx.doi.org/10.1212/WNL.0000000000001803] [PMID: 26138950]
[43]
Nozaki H, Nishizawa M, Onodera O. Features of cerebral autosomal recessive arteriopathy with subcortical infarcts and leukoencephalopathy. Stroke 2014; 45: 3447-53.
[http://dx.doi.org/10.1161/STROKEAHA.114.004236]
[44]
Nozaki H, Kato T, Nihonmatsu M, et al. Distinct molecular mechanisms of HTRA1 mutants in manifesting heterozygotes with CARASIL. Neurology 2016; 86(21): 1964-74.
[http://dx.doi.org/10.1212/WNL.0000000000002694] [PMID: 27164673]
[45]
Di Donato I, Bianchi S, Gallus GN, et al. Heterozygous mutations of HTRA1 gene in patients with familial cerebral small vessel disease. CNS Neurosci Ther 2017; 23(9): 759-65.
[http://dx.doi.org/10.1111/cns.12722] [PMID: 28782182]
[46]
Verdura E, Hervé D, Scharrer E, et al. Heterozygous HTRA1 mutations are associated with autosomal dominant cerebral small vessel disease. Brain 2015; 138(Pt 8): 2347-58.
[http://dx.doi.org/10.1093/brain/awv155] [PMID: 26063658]
[47]
Tateoka T, Onda H, Hirota K, et al. Unusual case of cerebral small vessel disease with a heterozygous nonsense mutation in HTRA1 2016.
[http://dx.doi.org/10.1016/j.jns.2016.01.037]
[48]
Uemura M, Nozaki H, Kato T, et al. HTRA1-Related Cerebral Small Vessel Disease: A Review of the Literature. Front Neurol 2020; 11: 545.
[http://dx.doi.org/10.3389/fneur.2020.00545] [PMID: 32719647]
[49]
Bugiani M, Kevelam SH, Bakels HS, et al. Cathepsin A-related arteriopathy with strokes and leukoencephalopathy (CARASAL). Neurology 2016; 87(17): 1777-86.
[http://dx.doi.org/10.1212/WNL.0000000000003251] [PMID: 27664989]
[50]
Hervé D, Chabriat H, Rigal M, et al. A novel hereditary extensive vascular leukoencephalopathy mapping to chromosome 20q13. Neurology 2012; 79(23): 2283-7.
[http://dx.doi.org/10.1212/WNL.0b013e3182768954] [PMID: 23175731]
[51]
Hwang YT, Lakshmanan R, Davagnanam I, et al. Brainstem phenotype of cathepsin A-related arteriopathy with strokes and leukoencephalopathy. Neurology: Genetics 2017; 3(4): e165.
[52]
Bonten EJ, Annunziata I, D’Azzo A. Lysosomal multienzyme complex: Pros and cons of working together. Cellular and Molecular Life Sciences 2014; 71(11): 2017-32.
[53]
Finsterer J, Scorza CA, Scorza FA, Wakil SM. Update on hereditary, autosomal dominant cathepsin-A-related arterio-pathy with strokes and leukoencephalopathy (CARASAL). Acta Neurologica Belgica 2019; 119(3): 299-303.
[54]
Lemmens R, Maugeri A, Niessen HWM, et al. Novel COL4A1 mutations cause cerebral small vessel disease by haploinsufficiency. Hum Mol Genet 2013; 22(2): 391-7.
[http://dx.doi.org/10.1093/hmg/dds436] [PMID: 23065703]
[55]
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(14): 1489-96.
[http://dx.doi.org/10.1056/NEJMoa053727] [PMID: 16598045]
[56]
Lanfranconi S, Markus HS. COL4A1 mutations as a monogenic cause of cerebral small vessel disease: a systematic review. Stroke 2010; 41(8): e513-8.
[http://dx.doi.org/10.1161/STROKEAHA.110.581918] [PMID: 20558831]
[57]
Meuwissen MEC, Halley DJJ, Smit LS, et al. The expanding phenotype of COL4A1 and COL4A2 mutations: clinical data on 13 newly identified families and a review of the literature. Genet Med 2015; 17(11): 843-53.
[http://dx.doi.org/10.1038/gim.2014.210] [PMID: 25719457]
[58]
Zagaglia S, Selch C, Nisevic JR, et al. Neurologic phenotypes associated with COL4A1/2 mutations: Expanding the spectrum of disease. Neurology 2018; 91(22): e2078-88.
[http://dx.doi.org/10.1212/WNL.0000000000006567] [PMID: 30413629]
[59]
de Vries LS, Koopman C, Groenendaal F, et al. COL4A1 mutation in two preterm siblings with antenatal onset of parenchymal hemorrhage. Ann Neurol 2009; 65(1): 12-8.
[http://dx.doi.org/10.1002/ana.21525] [PMID: 19194877]
[60]
van der Knaap MS, Smit LME, Barkhof F, et al. Neonatal porencephaly and adult stroke related to mutations in collagen IV A1. Ann Neurol 2006; 59(3): 504-11.
[http://dx.doi.org/10.1002/ana.20715] [PMID: 16374828]
[61]
Yoneda Y, Haginoya K, Kato M, et al. Phenotypic spectrum of COL4A1 mutations: porencephaly to schizencephaly. Ann Neurol 2013; 73(1): 48-57.
[http://dx.doi.org/10.1002/ana.23736] [PMID: 23225343]
[62]
Tonduti D, Pichiecchio A, La Piana R, et al. COL4A1-related disease: raised creatine kinase and cerebral calcification as useful pointers. Neuropediatrics 2012; 43(5): 283-8.
[http://dx.doi.org/10.1055/s-0032-1325116] [PMID: 22932948]
[63]
Weng YC, Sonni A, Labelle-Dumais C, et al. COL4A1 mutations in patients with sporadic late-onset intracerebral hemorrhage. Ann Neurol 2012; 71(4): 470-7.
[http://dx.doi.org/10.1002/ana.22682] [PMID: 22522439]
[64]
Jeanne M, Labelle-Dumais C, Jorgensen J, et al. COL4A2 mutations impair COL4A1 and COL4A2 secretion and cause hemorrhagic stroke. Am J Hum Genet 2012; 90(1): 91-101.
[http://dx.doi.org/10.1016/j.ajhg.2011.11.022] [PMID: 22209247]
[65]
Plaisier E, Gribouval O, Alamowitch S, et al. COL4A1 mutations and hereditary angiopathy, nephropathy, aneurysms, and muscle cramps. N Engl J Med 2007; 357(26): 2687-95.
[http://dx.doi.org/10.1056/NEJMoa071906] [PMID: 18160688]
[66]
Hagel C, Groden C, Niemeyer R, Stavrou D, Colmant HJ. Subcortical angiopathic encephalopathy in a German kindred suggests an autosomal dominant disorder distinct from CADASIL. Acta Neuropathol 2004; 108(3): 231-40.
[http://dx.doi.org/10.1007/s00401-004-0887-2] [PMID: 15221337]
[67]
Sourander P, Wålinder J. Hereditary multi-infarct dementia. Morphological and clinical studies of a new disease. Acta Neuropathol 1977; 39(3): 247-54.
[http://dx.doi.org/10.1007/BF00691704] [PMID: 906807]
[68]
Siitonen M, Börjesson-Hanson A, Pöyhönen M, et al. Multi-infarct dementia of Swedish type is caused by a 3’UTR mutation of COL4A1. Brain 2017; 140(5): e29.
[69]
Ding XQ, Hagel C, Ringelstein EB, et al. MRI features of pontine autosomal dominant microangiopathy and leukoencephalopathy (PADMAL). J Neuroimaging 2010; 20(2): 134-40.
[http://dx.doi.org/10.1111/j.1552-6569.2008.00336.x] [PMID: 19187480]
[70]
Zhao YY, Duan RN, Ji L, Liu QJ, Yan CZ. Cervical Spinal Involvement in a Chinese Pedigree With Pontine Autosomal Dominant Microangiopathy and Leukoencephalopathy Caused by a 3¢ Untranslated Region Mutation of COL4A1 Gene. Stroke 2019; 50(9): 2307-13.
[http://dx.doi.org/10.1161/STROKEAHA.119.024875] [PMID: 31366314]
[71]
Meikle PJ, Hopwood JJ, Clague AE, Carey WF. Prevalence of lysosomal storage disorders. JAMA 1999; 281(3): 249-54.
[http://dx.doi.org/10.1001/jama.281.3.249] [PMID: 9918480]
[72]
Echevarria L, Benistan K, Toussaint A, et al. X-chromosome inactivation in female patients with Fabry disease. Clin Genet 2016; 89(1): 44-54.
[http://dx.doi.org/10.1111/cge.12613] [PMID: 25974833]
[73]
Satoh K. Globotriaosylceramide induces endothelial dysfunction in fabry disease. Arterioscler Thromb Vasc Biol 2014; 34(1): 2-4.
[http://dx.doi.org/10.1161/ATVBAHA.113.302744] [PMID: 24335674]
[74]
Zarate YA, Hopkin RJ. Fabry’s disease. Lancet 2008; 372(9647): 1427-35.
[http://dx.doi.org/10.1016/S0140-6736(08)61589-5] [PMID: 18940466]
[75]
Mehta A, Ginsberg L. Natural history of the cerebrovascular complications of Fabry disease. Acta Paediatrica. Inter J Paed Suppl 2005; 94: pp. (447): 24-7.
[76]
Grewal RP. Stroke in Fabry’s disease. J Neurol 1994; 241(3): 153-6.
[http://dx.doi.org/10.1007/BF00868342] [PMID: 8164017]
[77]
Burlina AP. Neurological manifestations and psychological aspects of Fabry disease. Clin Ther 2010; 32: S88-9.
[http://dx.doi.org/10.1016/S0149-2918(10)00267-5]
[78]
Rombach SM, Smid BE, Linthorst GE, Dijkgraaf MGW, Hollak CEM. Natural course of Fabry disease and the effectiveness of enzyme replacement therapy: A systematic review and meta-analysis: Effectiveness of ERT in different disease stages. J Inherit Metab Dis 2014; 37(3): 341-52.
[79]
Fellgiebel A, Gartenschläger M, Wildberger K, Scheurich A, Desnick RJ, Sims K. Enzyme replacement therapy stabilized white matter lesion progression in Fabry disease. Cerebrovasc Dis 2014; 38(6): 448-56.
[http://dx.doi.org/10.1159/000369293] [PMID: 25502511]
[80]
Stefaniak JD, Parkes LM, Parry-Jones AR, et al. Enzyme replacement therapy and white matter hyperintensity progression in Fabry disease. Neurology 2018; 91(15): e1413-22.
[http://dx.doi.org/10.1212/WNL.0000000000006316] [PMID: 30209238]
[81]
Körver S, Longo MGF, Lima MR, et al. Determinants of cerebral radiological progression in Fabry disease. J Neurol Neurosurg & Psychiatry 2020; Jul; 191(7): 756-63. Available from: http://jnnp.bmj.com/content/91/7/756
[82]
Okeda R, Nisihara M. An autopsy case of Fabry disease with neuropathological investigation of the pathogenesis of associated dementia. Neuropathology 2008; 28(5): 532-40.
[http://dx.doi.org/10.1111/j.1440-1789.2008.00883.x] [PMID: 18410273]
[83]
Nelson MP, Tse TE, O’Quinn DB, et al. Autophagy-lysosome pathway associated neuropathology and axonal degeneration in the brains of alpha-galactosidase A-deficient mice. Acta Neuropathol Commun 2014; 2: 20.
[http://dx.doi.org/10.1186/2051-5960-2-20] [PMID: 24529306]
[84]
Paavilainen T, Lepomäki V, Saunavaara J, et al. Diffusion tensor imaging and brain volumetry in Fabry disease patients. Neuroradiology 2013; 55(5): 551-8.
[http://dx.doi.org/10.1007/s00234-012-1131-8] [PMID: 23292181]
[85]
Albrecht J, Dellani PR, Müller MJ, et al. Voxel based analyses of diffusion tensor imaging in Fabry disease. J Neurol Neurosurg Psychiatry 2007; 78(9): 964-9.
[http://dx.doi.org/10.1136/jnnp.2006.112987] [PMID: 17449543]
[86]
Lelieveld IM, Böttcher A, Hennermann JB, Beck M, Fellgiebel A. Eight-year follow-up of neuropsychiatric symptoms and brain structural changes in fabry disease. PLoS One 2015; 10(9): e0137603.
[http://dx.doi.org/10.1371/journal.pone.0137603] [PMID: 26340726]
[87]
Schermuly I, Müller MJ, Müller KM, et al. Neuropsychiatric symptoms and brain structural alterations in Fabry disease. Eur J Neurol 2011; 18(2): 347-53.
[http://dx.doi.org/10.1111/j.1468-1331.2010.03155.x] [PMID: 20636371]
[88]
Ulivi L, Kanber B, Prados F, et al. White matter integrity correlates with cognition and disease severity in Fabry disease. Brain 2020; 143(11): 3331-3342 [Internet].
[http://dx.doi.org/10.1093/brain/awaa282] [PMID: 33141169]
[89]
Cocozza S, Russo C, Pontillo G, Pisani A, Brunetti A. Neuroimaging in Fabry disease: current knowledge and future directions. Insights Imaging 2018; 9(6): 1077-88.
[http://dx.doi.org/10.1007/s13244-018-0664-8] [PMID: 30390274]
[90]
Rolfs A, Fazekas F, Grittner U, et al. Stroke in Young Fabry Patients (sifap) Investigators. Acute cerebrovascular disease in the young: the Stroke in Young Fabry Patients study. Stroke 2013; 44(2): 340-9.
[http://dx.doi.org/10.1161/STROKEAHA.112.663708] [PMID: 23306324]
[91]
Reisin RC, Romero C, Marchesoni C, et al. Brain MRI findings in patients with Fabry disease. J Neurol Sci 2011; 305(1-2): 41-44 [Internet].
[http://dx.doi.org/10.1016/j.jns.2011.03.020] [PMID: 21463870]
[92]
Kobayashi M, Kono Y, Wakabayashi T, et al. Characteristics of Cerebral Microbleeds in Patients with Fabry Disease. J Stroke Cerebrovasc Dis NAME/FABRY/Fabry Rev 2016; 25(6): 1320-5. Available from:
[http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2016.02.019]
[93]
Cocozza S, Russo C, Pisani A, et al. Redefining the Pulvinar Sign in Fabry Disease. AJNR Am J Neuroradiol 2017; 38(12): 2264-9.
[http://dx.doi.org/10.3174/ajnr.A5420] [PMID: 29051208]
[94]
Moore DF, Altarescu G, Barker WC, Patronas NJ, Herscovitch P, Schiffmann R. White matter lesions in Fabry disease occur in ‘prior’ selectively hypometabolic and hyperperfused brain regions. Brain Res Bull 2003; 62(3): 231-40.
[http://dx.doi.org/10.1016/j.brainresbull.2003.09.021] [PMID: 14698356]
[95]
Ginat DT, Meyers SP. Intracranial lesions with high signal intensity on T1-weighted MR images: differential diagnosis. Radiographics 2012; 32(2): 499-516.
[http://dx.doi.org/10.1148/rg.322105761] [PMID: 22411945]
[96]
Gavazzi C, Borsini W, Guerrini L, et al. Subcortical damage and cortical functional changes in men and women with Fabry disease: a multifaceted MR study. Radiology 2006; 241(2): 492-500. http://www.ncbi.nlm.nih.gov/pubmed/17057070 [Internet].
[http://dx.doi.org/10.1148/radiol.2412051122] [PMID: 17057070]
[97]
Marino S, Borsini W, Buchner S, et al. Diffuse structural and metabolic brain changes in Fabry disease. J Neurol 2006; 253(4): 434-40.
[http://dx.doi.org/10.1007/s00415-005-0020-z] [PMID: 16541218]
[98]
Fellgiebel A, Wolf DO, Kolodny E, Müller MJ. Hippocampal atrophy as a surrogate of neuronal involvement in Fabry disease. J Inherit Metab Dis 2012; 35(2): 363-7.
[http://dx.doi.org/10.1007/s10545-011-9390-9] [PMID: 21932096]
[99]
Garzuly F, Maródi L, Erdös M, et al. Megadolichobasilar anomaly with thrombosis in a family with Fabry’s disease and a novel mutation in the α-galactosidase A gene. Brain 2005; 128(Pt 9): 2078-83.
[http://dx.doi.org/10.1093/brain/awh546] [PMID: 15947062]
[100]
Fellgiebel A, Müller MJ, Ginsberg L. CNS manifestations of Fabry’s disease. Lancet Neurology 2006; 5(9): 791-5.
[http://dx.doi.org/10.1016/S1474-4422(06)70548-8]
[101]
Fellgiebel A, Keller I, Marin D, et al. Diagnostic utility of different MRI and MR angiography measures in Fabry disease. Neurology 2009; 72(1): 63-8.
[http://dx.doi.org/10.1212/01.wnl.0000338566.54190.8a] [PMID: 19122032]
[102]
Moore DF, Herscovitch P, Schiffmann R. Selective arterial distribution of cerebral hyperperfusion in Fabry disease. J Neuroimaging 2001; 11(3): 303-7.
[http://dx.doi.org/10.1111/j.1552-6569.2001.tb00051.x] [PMID: 11462299]
[103]
Phyu P, Merwick A, Davagnanam I, et al. Increased resting cerebral blood flow in adult Fabry disease: MRI arterial spin labeling study. Neurology 2018; 90(16): e1379-85.
[http://dx.doi.org/10.1212/WNL.0000000000005330] [PMID: 29661900]
[104]
Richards A, van den Maagdenberg AMJM, Jen JC, et al. C-terminal truncations in human 3¢-5¢ DNA exonuclease TREX1 cause autosomal dominant retinal vasculopathy with cerebral leukodystrophy. Nat Genet 2007; 39(9): 1068-70.
[http://dx.doi.org/10.1038/ng2082] [PMID: 17660820]
[105]
Storimans CW, Van Schooneveld MJ, Oosterhuis JA, Bos PJ. A new autosomal dominant vascular retinopathy syndrome. Eur J Ophthalmol 1991; 1(2): 73-8.
[http://dx.doi.org/10.1177/112067219100100204] [PMID: 1821204]
[106]
Jen J, Cohen AH, Yue Q, et al. Hereditary endotheliopathy with retinopathy, nephropathy, and stroke (HERNS). Neurology 1997; 49(5): 1322-30.
[http://dx.doi.org/10.1212/WNL.49.5.1322] [PMID: 9371916]
[107]
de Boer I, Stam AH, Buntinx L, et al. RVCL-S and CADASIL display distinct impaired vascular function. Neurology 2018; 91(10): e956-63.
[http://dx.doi.org/10.1212/WNL.0000000000006119] [PMID: 30076273]
[108]
Pelzer N, Bijkerk R, Reinders MEJ, et al. Circulating endothelial markers in retinal vasculopathy with cerebral leukoencephalopathy and systemic manifestations. Stroke 2017; 48(12): 3301-7.
[http://dx.doi.org/10.1161/STROKEAHA.117.018556] [PMID: 29114091]
[109]
Stam AH, Kothari PH, Shaikh A, et al. Retinal vasculopathy with cerebral leukoencephalopathy and systemic manifestations. Brain 2016; 139(11): 2909-22.
[http://dx.doi.org/10.1093/brain/aww217] [PMID: 27604306]
[110]
Hedderich DM, Lummel N, Deschauer M, et al. Magnetic Resonance Imaging Characteristics of Retinal Vasculopathy with Cerebral Leukoencephalopathy and Systemic Manifestations. Clin Neuroradiol 2020; 30(2): 229-36.
[http://dx.doi.org/10.1007/s00062-018-0755-4] [PMID: 30627749]
[111]
Mateen FJ, Krecke K, Younge BR, et al. Evolution of a tumor-like lesion in cerebroretinal vasculopathy and TREX1 mutation. Neurology 2010; 75(13): 1211-3.
[http://dx.doi.org/10.1212/WNL.0b013e3181f4d7ac] [PMID: 20876473]
[112]
McGlasson S, Rannikmäe K, Bevan S, et al. UK Young Lacunar Stroke Study. Rare variants of the 3¢-5¢ DNA exonuclease TREX1 in early onset small vessel stroke. Wellcome Open Res 2017; 2(0): 106.
[http://dx.doi.org/10.12688/wellcomeopenres.12631.1] [PMID: 29387804]
[113]
Heiss WD. The additional value of PET in the assessment of cerebral small vessel disease. J Nucl Med 2018; 59(11): 1660-4.
[http://dx.doi.org/10.2967/jnumed.118.214270] [PMID: 29959217]
[114]
Charidimou A, Farid K, Baron J-C. Amyloid-PET in sporadic cerebral amyloid angiopathy: A diagnostic accuracy meta-analysis. Neurology 2017; 89(14): 1490-8.
[http://dx.doi.org/10.1212/WNL.0000000000004539] [PMID: 28855406]
[115]
Su J, Huang Q, Ren S, et al. Altered Brain Glucose Metabolism Assessed by 18F-FDG PET Imaging Is Associated with the Cognitive Impairment of CADASIL. Neuroscience 2019; 417: 35-44. http://www.sciencedirect. com/science/article/pii/S0306452219305391 [Internet].
[http://dx.doi.org/10.1016/j.neuroscience.2019.07.048] [PMID: 31394195]
[116]
Korsholm K, Feldt-Rasmussen U, Granqvist H, et al. Positron Emission Tomography and Magnetic Resonance Imaging of the Brain in Fabry Disease: A Nationwide, Long-Time, Prospective Follow-Up. PLoS One 2015; 10(12): e0143940.
[http://dx.doi.org/10.1371/journal.pone.0143940] [PMID: 26629990]
[117]
Moore DF, Altarescu G, Ling GSF, et al. Elevated cerebral blood flow velocities in Fabry disease with reversal after enzyme replacement. Stroke 2002; 33(2): 525-31.
[http://dx.doi.org/10.1161/hs0202.102601] [PMID: 11823664]
[118]
Cuadrado-Godia E, Dwivedi P, Sharma S, et al. Cerebral Small Vessel Disease: A Review Focusing on Pathophysiology, Biomarkers, and Machine Learning Strategies. J Stroke 2018; 20(3): 302-20.
[http://dx.doi.org/10.5853/jos.2017.02922] [PMID: 30309226]

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