{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,11]],"date-time":"2026-04-11T12:12:59Z","timestamp":1775909579939,"version":"3.50.1"},"reference-count":43,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,8,23]],"date-time":"2023-08-23T00:00:00Z","timestamp":1692748800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["JP18H02742"],"award-info":[{"award-number":["JP18H02742"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["JP20K16604"],"award-info":[{"award-number":["JP20K16604"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["JP21H02842"],"award-info":[{"award-number":["JP21H02842"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["JP21K15702"],"award-info":[{"award-number":["JP21K15702"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["JP22K07495"],"award-info":[{"award-number":["JP22K07495"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["JP22K15713"],"award-info":[{"award-number":["JP22K15713"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["JP23K06931"],"award-info":[{"award-number":["JP23K06931"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003478","name":"Ministry of Health, Labour and Welfare","doi-asserted-by":"publisher","award":["201610002B"],"award-info":[{"award-number":["201610002B"]}],"id":[{"id":"10.13039\/501100003478","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003478","name":"Ministry of Health, Labour and Welfare","doi-asserted-by":"publisher","award":["20317603"],"award-info":[{"award-number":["20317603"]}],"id":[{"id":"10.13039\/501100003478","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009619","name":"Japan Agency for Medical Research and Development","doi-asserted-by":"publisher","award":["201442014A"],"award-info":[{"award-number":["201442014A"]}],"id":[{"id":"10.13039\/100009619","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009619","name":"Japan Agency for Medical Research and Development","doi-asserted-by":"publisher","award":["201442071A"],"award-info":[{"award-number":["201442071A"]}],"id":[{"id":"10.13039\/100009619","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Neurol."],"abstract":"<jats:sec><jats:title>Background and objective<\/jats:title><jats:p>Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL) is an inherited cerebral microvascular disease characterized by the development of vascular dementia and lacunar infarctions. This study aimed to identify the genetic and clinical features of CADASIL in Japan.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>We conducted genetic analysis on a case series of patients clinically diagnosed with CADASIL. Clinical and imaging analyses were performed on 32 patients with pathogenic mutations in the <jats:italic>NOTCH3<\/jats:italic> gene. To assess the presence of cerebral microbleeds (CMBs), we utilized several established rating scales including the Fazekas scale, Scheltens rating scale, and Microbleed Anatomical Rating Scale, based on brain MRI images.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>Among the 32 CADASIL patients, 24 cases were found carrying the R75P mutation in <jats:italic>NOTCH3<\/jats:italic>, whereas the remaining eight cases had other <jats:italic>NOTCH3<\/jats:italic> mutations (R75Q, R110C, C134F, C144F, R169C, and R607C). The haplotype analysis of the R75P mutation uncovered the presence of a founder effect. A brain MRI analysis revealed that cases with the R75P mutation had a significantly higher total number of CMBs, particularly in the thalamus when compared to patients with other <jats:italic>NOTCH3<\/jats:italic> mutations. Among 15 out of 24 cases with the R75P mutation, we observed a notable clustering of CMBs in the thalamus, termed microbleed clustering in thalamus sign (MCT sign).<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>We propose that the MCT sign observed in <jats:italic>NOTCH3<\/jats:italic> R75P-related CADASIL patients may serve as a potentially characteristic imaging feature. This finding offers further insights into the interactions between genotypes and phenotypes between <jats:italic>NOTCH3<\/jats:italic> and CADASIL.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fneur.2023.1241678","type":"journal-article","created":{"date-parts":[[2023,8,23]],"date-time":"2023-08-23T09:55:23Z","timestamp":1692784523000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":6,"title":["Microbleed clustering in thalamus sign in CADASIL patients with NOTCH3 R75P mutation"],"prefix":"10.3389","volume":"14","author":[{"given":"Jun","family":"Takei","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yujiro","family":"Higuchi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Masahiro","family":"Ando","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Akiko","family":"Yoshimura","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jun-Hui","family":"Yuan","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Natsumi","family":"Fujisaki","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Takashi","family":"Tokashiki","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Naomi","family":"Kanzato","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Manabu","family":"Jonosono","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Takeshi","family":"Sueyoshi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Naoaki","family":"Kanda","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hideki","family":"Matsuoka","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ryuichi","family":"Okubo","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Masahito","family":"Suehara","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Eiji","family":"Matsuura","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hiroshi","family":"Takashima","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2023,8,23]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"256","DOI":"10.1038\/ng0393-256","article-title":"Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy maps to chromosome 19q12","volume":"3","author":"Tournier-Lasserve","year":"1993","journal-title":"Nat Genet."},{"key":"B2","doi-asserted-by":"publisher","first-page":"707","DOI":"10.1038\/383707a0","article-title":"Notch3 Mutations in CADASIL, a hereditary adult-onset condition causing stroke and dementia","volume":"383","author":"Joutel","year":"1996","journal-title":"Nature."},{"key":"B3","doi-asserted-by":"publisher","first-page":"593","DOI":"10.1586\/14737159.2014.922880","article-title":"Interpretation of NOTCH3 mutations in the diagnosis of CADASIL","volume":"14","author":"Rutten","year":"2014","journal-title":"Expert Rev Mol Diagn"},{"key":"B4","doi-asserted-by":"publisher","first-page":"1001","DOI":"10.1016\/j.ajhg.2013.04.024","article-title":"Mutations in PDGFRB cause autosomal-dominant infantile myofibromatosis","volume":"92","author":"Martignetti","year":"2013","journal-title":"Am J Hum Genet"},{"key":"B5","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1002\/ajmg.a.36863","article-title":"Truncating Mutations in the Last Exon of NOTCH3 cause lateral meningocele syndrome","volume":"167","author":"Gripp","year":"2015","journal-title":"Am J Med Genet A"},{"key":"B6","doi-asserted-by":"publisher","first-page":"1511","DOI":"10.1212\/01.wnl.0000216259.99811.50","article-title":"Characteristics of CADASIL in Korea A novel cysteine-sparing Notch3 mutation","volume":"66","author":"Kim","year":"2006","journal-title":"Neurology."},{"key":"B7","doi-asserted-by":"publisher","first-page":"2067","DOI":"10.2169\/internalmedicine.47.1391","article-title":"Two Japanese CADASIL Families Exhibiting Notch3 Mutation R75P not involving cysteine residue","volume":"47","author":"Mizuno","year":"2008","journal-title":"Internal Med."},{"key":"B8","doi-asserted-by":"publisher","first-page":"1828","DOI":"10.1007\/s00415-015-7782-8","article-title":"Genotypic and phenotypic spectrum of CADASIL in Japan: the experience at a referral Center in Kumamoto University from 1997 to 2014","volume":"262","author":"Ueda","year":"2015","journal-title":"J Neurol."},{"key":"B9","doi-asserted-by":"publisher","first-page":"130","DOI":"10.3389\/fnagi.2020.00130","article-title":"Prevalence and atypical clinical characteristics of NOTCH3 mutations among patients admitted for acute lacunar infarctions","volume":"12","author":"Okada","year":"2020","journal-title":"Front Aging Neurosci."},{"key":"B10","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1161\/hs0102.100885","article-title":"Cerebral Microbleeds in CADASIL a gradient-echo magnetic resonance imaging and autopsy study","volume":"33","author":"Dichgans","year":"2002","journal-title":"Stroke."},{"key":"B11","doi-asserted-by":"publisher","first-page":"256","DOI":"10.1016\/S1474-4422(08)70041-3","article-title":"Imaging of intracranial haemorrhage","volume":"7","author":"Kidwell","year":"2008","journal-title":"Lancet Neurol."},{"key":"B12","doi-asserted-by":"publisher","first-page":"659","DOI":"10.1002\/ana.24612","article-title":"Mutations in MME cause an autosomal-recessive Charcot-Marie-tooth disease type 2","volume":"79","author":"Higuchi","year":"2016","journal-title":"Ann Neurol."},{"key":"B13","doi-asserted-by":"publisher","first-page":"351","DOI":"10.2214\/ajr.149.2.351","article-title":"MR Signal Abnormalities at 15 T in Alzheimer's dementia and normal aging","volume":"149","author":"Fazekas","year":"1987","journal-title":"AJR Am J Roentgenol."},{"key":"B14","doi-asserted-by":"publisher","first-page":"735","DOI":"10.1093\/brain\/115.3.735","article-title":"White matter lesions on magnetic resonance imaging in clinically diagnosed Alzheimer's disease: evidence for heterogeneity","volume":"115","author":"Scheltens","year":"1992","journal-title":"Brain."},{"key":"B15","doi-asserted-by":"publisher","first-page":"1759","DOI":"10.1212\/WNL.0b013e3181c34a7d","article-title":"The Microbleed Anatomical Rating Scale (MARS) reliability of a tool to map brain microbleeds","volume":"73","author":"Gregoire","year":"2009","journal-title":"Neurology."},{"key":"B16","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1148\/radiol.2018170803","article-title":"Cerebral microbleeds: imaging and clinical significance","volume":"287","author":"Haller","year":"2018","journal-title":"Radiology."},{"key":"B17","doi-asserted-by":"publisher","first-page":"683","DOI":"10.1148\/radiol.2293021354","article-title":"Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy: MR imaging findings at different ages\u22123rd\u22126th decades","volume":"229","author":"Van Den Boom","year":"2003","journal-title":"Radiology."},{"key":"B18","doi-asserted-by":"publisher","first-page":"1066","DOI":"10.1212\/WNL.57.6.1066","article-title":"Cerebral microbleeds in CADASIL","volume":"57","author":"Lesnik Oberstein","year":"2001","journal-title":"Neurology."},{"key":"B19","doi-asserted-by":"publisher","first-page":"2375","DOI":"10.1093\/brain\/awl177","article-title":"Blood Pressure and Haemoglobin A1c are associated with microhaemorrhage in CADASIL: a two-centre cohort study","volume":"129","author":"Viswanathan","year":"2006","journal-title":"Brain."},{"key":"B20","doi-asserted-by":"publisher","first-page":"e016233","DOI":"10.1161\/JAHA.120.016233","article-title":"Cerebral microbleed burdens in specific brain regions are associated with disease severity of cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy","volume":"9","author":"Chung","year":"2020","journal-title":"J Am Heart Assoc."},{"key":"B21","doi-asserted-by":"publisher","first-page":"3243","DOI":"10.1111\/ene.15485","article-title":"Comparison of clinical and neuroimaging features between NOTCH3 mutations and nongenetic spontaneous intracerebral haemorrhage","volume":"29","author":"Chen","year":"2022","journal-title":"Eur J Neurol."},{"key":"B22","doi-asserted-by":"publisher","first-page":"1646","DOI":"10.1161\/01.STR.31.7.1646","article-title":"Assessment of lacunar hemorrhage associated with hypertensive stroke by echo-planar gradient-echo T2*-Weighted MRI","volume":"31","author":"Kinoshita","year":"2000","journal-title":"Stroke."},{"key":"B23","doi-asserted-by":"publisher","first-page":"537","DOI":"10.1007\/s00415-004-0359-6","article-title":"Cerebral microbleeds and white matter changes in patients hospitalized with lacunar infarcts","volume":"251","author":"Fan","year":"2004","journal-title":"J Neurol."},{"key":"B24","doi-asserted-by":"publisher","first-page":"214","DOI":"10.1016\/j.jstrokecerebrovasdis.2009.12.001","article-title":"Clinical characteristics by topographical distribution of brain microbleeds, with a particular emphasis on diffuse microbleeds","volume":"20","author":"Yakushiji","year":"2011","journal-title":"J Stroke Cerebrov Dis."},{"key":"B25","doi-asserted-by":"publisher","first-page":"537","DOI":"10.1212\/WNL.56.4.537","article-title":"Clinical diagnosis of cerebral amyloid angiopathy: validation of the boston criteria","volume":"56","author":"Knudsen","year":"2001","journal-title":"Neurology."},{"key":"B26","doi-asserted-by":"publisher","first-page":"e0190878","DOI":"10.1371\/journal.pone.0190878","article-title":"Location, number and factors associated with cerebral microbleeds in an italian-british cohort of CADASIL patients","volume":"13","author":"Nannucci","year":"2018","journal-title":"PLoS ONE."},{"key":"B27","doi-asserted-by":"publisher","first-page":"e0234797","DOI":"10.1371\/journal.pone.0234797","article-title":"Clinical and imaging features of patients with cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy and cysteine-sparing NOTCH3 mutations","volume":"15","author":"Kim","year":"2020","journal-title":"PLoS ONE."},{"key":"B28","doi-asserted-by":"publisher","first-page":"705284","DOI":"10.3389\/fgene.2021.705284","article-title":"NOTCH3 variants and genotype-phenotype features in Chinese CADASIL patients","volume":"12","author":"Hu","year":"2021","journal-title":"Front Genet."},{"key":"B29","doi-asserted-by":"publisher","first-page":"1431","DOI":"10.1016\/j.jstrokecerebrovasdis.2019.03.026","article-title":"The CADASIL Scale-J, a modified scale to prioritize access to genetic testing for Japanese CADASIL-suspected patients","volume":"28","author":"Koizumi","year":"2019","journal-title":"J Stroke Cerebrov Dis."},{"key":"B30","doi-asserted-by":"publisher","first-page":"216","DOI":"10.3389\/fnagi.2020.00216","article-title":"nationwide survey and multicenter registry-based database of cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy in Japan","volume":"12","author":"Shindo","year":"2020","journal-title":"Front Aging Neurosci."},{"key":"B31","doi-asserted-by":"publisher","first-page":"694","DOI":"10.1136\/jnnp-2020-325838","article-title":"NOTCH3 variants are more common than expected in the general population and associated with stroke and vascular dementia: an analysis of 200 000 participants","volume":"92","author":"Cho","year":"2021","journal-title":"J Neurol Neurosur Psychiatry."},{"key":"B32","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1016\/S0022-510X(03)00109-6","article-title":"Genetic, clinical and pathological studies of CADASIL in Japan: a partial contribution of notch3 mutations and implications of smooth muscle cell degeneration for the pathogenesis","volume":"212","author":"Santa","year":"2003","journal-title":"J Neurol Sci."},{"key":"B33","doi-asserted-by":"publisher","first-page":"521","DOI":"10.3390\/medicina55090521","article-title":"Novel characteristics of race-specific genetic functions in Korean CADASIL","volume":"55","author":"Kim","year":"2019","journal-title":"Medicina."},{"key":"B34","doi-asserted-by":"publisher","first-page":"841","DOI":"10.1136\/jnnp-2018-319268","article-title":"Detrimental effects of intracerebral haemorrhage on patients with CADASIL harbouring NOTCH3 R544C mutation","volume":"90","author":"Chen","year":"2019","journal-title":"J Neurol Neurosurg Psychiatry."},{"key":"B35","doi-asserted-by":"publisher","first-page":"499","DOI":"10.3988\/jcn.2022.18.5.499","article-title":"Occurrence of intracranial hemorrhage and associated risk factors in cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy: a systematic review and meta-analysis","volume":"18","author":"Lai","year":"2022","journal-title":"J Clin Neurol."},{"key":"B36","doi-asserted-by":"publisher","first-page":"731","DOI":"10.1002\/ana.410440506","article-title":"The phenotypic spectrum of CADASIL: clinical findings in 102 cases","volume":"44","author":"Dichgans","year":"1998","journal-title":"Ann Neurol."},{"key":"B37","doi-asserted-by":"publisher","first-page":"e0136501","DOI":"10.1371\/journal.pone.0136501","article-title":"Characterization of CADASIL among the Han Chinese in Taiwan: distinct genotypic and phenotypic profiles","volume":"10","author":"Liao","year":"2015","journal-title":"PLoS ONE."},{"key":"B38","doi-asserted-by":"publisher","first-page":"813","DOI":"10.1038\/sj.ejhg.5201221","article-title":"Detection of the founder effect in finnish CADASIL families","volume":"12","author":"Mykk\u00e4nen","year":"2004","journal-title":"Eur J Human Genet."},{"key":"B39","doi-asserted-by":"publisher","first-page":"736","DOI":"10.1136\/jnnp.2004.048207","article-title":"The spectrum of Notch3 mutations in 28 Italian CADASIL families","volume":"76","author":"Dotti","year":"2005","journal-title":"J Neurol Neurosurg Psychiatry."},{"key":"B40","doi-asserted-by":"publisher","first-page":"338","DOI":"10.3174\/ajnr.A1355","article-title":"MR imaging detection of cerebral microbleeds: effect of susceptibility-weighted imaging, section thickness, and field strength","volume":"30","author":"Nandigam","year":"2009","journal-title":"Am J Neuroradiol."},{"key":"B41","doi-asserted-by":"publisher","first-page":"895","DOI":"10.1016\/j.acra.2008.01.013","article-title":"Detection of asymptomatic cerebral microbleeds: a comparative study at 15 and 30 T","volume":"15","author":"Stehling","year":"2008","journal-title":"Academic Radiol."},{"key":"B42","doi-asserted-by":"publisher","first-page":"517","DOI":"10.1007\/s12975-019-00742-7","article-title":"Progression and classification of granular osmiophilic material (GOM) deposits in functionally characterized human NOTCH3 transgenic mice","volume":"11","author":"Gravesteijn","year":"2020","journal-title":"Transl Stroke Res."},{"key":"B43","doi-asserted-by":"publisher","first-page":"e12751","DOI":"10.1111\/nan.12751","article-title":"NOTCH3 variant position is associated with NOTCH3 aggregation load in CADASIL vasculature","volume":"48","author":"Gravesteijn","year":"2022","journal-title":"Neuropathol Appl Neurobiol."}],"container-title":["Frontiers in Neurology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fneur.2023.1241678\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,8,23]],"date-time":"2023-08-23T09:55:28Z","timestamp":1692784528000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fneur.2023.1241678\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,8,23]]},"references-count":43,"alternative-id":["10.3389\/fneur.2023.1241678"],"URL":"https:\/\/doi.org\/10.3389\/fneur.2023.1241678","relation":{},"ISSN":["1664-2295"],"issn-type":[{"value":"1664-2295","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,8,23]]},"article-number":"1241678"}}