Distinctive Pattern of Metal Deposition in Neurologic Wilson Disease: Insights From 7T Susceptibility-Weighted Imaging

. 2024 Jun 25 ; 102 (12) : e209478. [epub] 20240603

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38830145

BACKGROUND AND OBJECTIVES: Noninvasive and accurate biomarkers of neurologic Wilson disease (NWD), a rare inherited disorder, could reduce diagnostic error or delay. Excessive subcortical metal deposition seen on susceptibility imaging has suggested a characteristic pattern in NWD. With submillimeter spatial resolution and increased contrast, 7T susceptibility-weighted imaging (SWI) may enable better visualization of metal deposition in NWD. In this study, we sought to identify a distinctive metal deposition pattern in NWD using 7T SWI and investigate its diagnostic value and underlying pathophysiologic mechanism. METHODS: Patients with WD, healthy participants with monoallelic ATP7B variant(s) on a single chromosome, and health controls (HCs) were recruited. NWD and non-NWD (nNWD) were defined according to the presence or absence of neurologic symptoms during investigation. Patients with other diseases with comparable clinical or imaging manifestations, including early-onset Parkinson disease (EOPD), multiple system atrophy (MSA), progressive supranuclear palsy (PSP), and neurodegeneration with brain iron accumulation (NBIA), were additionally recruited and assessed for exploratory comparative analysis. All participants underwent 7T T1, T2, and high-resolution SWI scanning. Quantitative susceptibility mapping and principal component analysis were performed to illustrate metal distribution. RESULTS: We identified a linear signal intensity change consisting of a hyperintense strip at the lateral border of the globus pallidus in patients with NWD. We termed this feature "hyperintense globus pallidus rim sign." This feature was detected in 38 of 41 patients with NWD and was negative in all 31 nNWD patients, 15 patients with EOPD, 30 patients with MSA, 15 patients with PSP, and 12 patients with NBIA; 22 monoallelic ATP7B variant carriers; and 41 HC. Its sensitivity to differentiate between NWD and HC was 92.7%, and specificity was 100%. Severity of the hyperintense globus pallidus rim sign measured by a semiquantitative scale was positively correlated with neurologic severity (ρ = 0.682, 95% CI 0.467-0.821, p < 0.001). Patients with NWD showed increased susceptibility in the lenticular nucleus with high regional weights in the lateral globus pallidus and medial putamen. DISCUSSION: The hyperintense globus pallidus rim sign showed high sensitivity and excellent specificity for diagnosis and differential diagnosis of NWD. It is related to a special metal deposition pattern in the lenticular nucleus in NWD and can be considered as a novel neuroimaging biomarker of NWD. CLASSIFICATION OF EVIDENCE: The study provides Class II evidence that the hyperintense globus pallidus rim sign on 7T SWI MRI can accurately diagnose neurologic WD.

Zobrazit více v PubMed

Czlonkowska A, Litwin T, Dusek P, et al. . Wilson disease. Nat Rev Dis Primers. 2018;4(1):21. doi:10.1038/s41572-018-0018-3 PubMed DOI PMC

Ferenci P, Caca K, Loudianos G, et al. . Diagnosis and phenotypic classification of Wilson disease. Liver Int. 2003;23(3):139-142. doi:10.1034/j.1600-0676.2003.00824.x PubMed DOI

Walter U, Krolikowski K, Tarnacka B, Benecke R, Czlonkowska A, Dressler D. Sonographic detection of basal ganglia lesions in asymptomatic and symptomatic Wilson disease. Neurology. 2005;64(10):1726-1732. doi:10.1212/01.WNL.0000161847.46465.B9 PubMed DOI

Shribman S, Poujois A, Bandmann O, Czlonkowska A, Warner TT. Wilson's disease: update on pathogenesis, biomarkers and treatments. J Neurol Neurosurg Psychiatry. 2021;92(10):1053-1061. doi:10.1136/jnnp-2021-326123 PubMed DOI

Beinhardt S, Leiss W, Stättermayer AF, et al. . Long-term outcomes of patients with Wilson disease in a large Austrian cohort. Clin Gastroenterol Hepatol. 2014;12(4):683-689. doi:10.1016/j.cgh.2013.09.025 PubMed DOI

Merle U, Schaefer M, Ferenci P, Stremmel W. Clinical presentation, diagnosis and long-term outcome of Wilson's disease: a cohort study. Gut. 2007;56(1):115-120. doi:10.1136/gut.2005.087262 PubMed DOI PMC

European Association for Study of Liver. EASL clinical practice guidelines: Wilson's disease. J Hepatol. 2012;56(3):671-685. doi:10.1016/j.jhep.2011.11.007 PubMed DOI

Zhong W, Huang Z, Tang X. A study of brain MRI characteristics and clinical features in 76 cases of Wilson's disease. J Clin Neurosci. 2019;59:167-174. doi:10.1016/j.jocn.2018.10.096 PubMed DOI

Prashanth L, Sinha S, Taly A, Vasudev M. Do MRI features distinguish Wilson's disease from other early onset extrapyramidal disorders? An analysis of 100 cases. Mov Disord. 2010;25(6):672-678. doi:10.1002/mds.22689 PubMed DOI

Rędzia-Ogrodnik B, Członkowska A, Antos A, et al. . Pathognomonic neuroradiological signs in Wilson's disease: truth or myth? Parkinsonism Relat Disord. 2023;107:105247. doi:10.1016/j.parkreldis.2022.105247 PubMed DOI

Lallas M, Desai J. Wernicke encephalopathy in children and adolescents. World J Pediatr. 2014;10(4):293-298. doi:10.1007/s12519-014-0506-9 PubMed DOI

Das SK, Ray K. Wilson's disease: an update. Nat Clin Pract Neurol. 2006;2(9):482-493. doi:10.1038/ncpneuro0291 PubMed DOI

Dusek P, Bahn E, Litwin T, et al. . Brain iron accumulation in Wilson disease: a post mortem 7 Tesla MRI: histopathological study. Neuropathol Appl Neurobiol. 2017;43(6):514-532. doi:10.1111/nan.12341 PubMed DOI

Litwin T, Gromadzka G, Szpak G, Jabłonka-Salach K, Bulska E, Członkowska A. Brain metal accumulation in Wilson's disease. J Neurol Sci. 2013;329(1-2):55-58. doi:10.1016/j.jns.2013.03.021 PubMed DOI

Zhou X, Xiao X, Li XH, et al. . A study of susceptibility-weighted imaging in patients with Wilson disease during the treatment of metal chelator. J Neurol. 2020;267(6):1643-1650. doi:10.1007/s00415-020-09746-y PubMed DOI

Li G, Wu R, Tong R, et al. . Quantitative measurement of metal accumulation in brain of patients with Wilson's disease. Mov Disord. 2020;35(10):1787-1795. doi:10.1002/mds.28141 PubMed DOI

Dusek P, Lescinskij A, Ruzicka F, et al. . Associations of brain atrophy and cerebral iron accumulation at MRI with clinical severity in Wilson disease. Radiology. 2021;299(3):662-672. doi:10.1148/radiol.2021202846 PubMed DOI

Su D, Zhang Z, Zhang Z, et al. . Microstructural and functional impairment of the basal ganglia in Wilson's disease: a multimodal neuroimaging study. Front Neurosci. 2023;17:1146644. doi:10.3389/fnins.2023.1146644 PubMed DOI PMC

Yuan XZ, Li GY, Chen JL, Li JQ, Wang XP. Paramagnetic metal accumulation in the deep gray matter nuclei is associated with neurodegeneration in Wilson's disease. Front Neurosci. 2020;14:573633. doi:10.3389/fnins.2020.573633 PubMed DOI PMC

Dusek P, Hofer T, Alexander J, Roos PM, Aaseth JO. Cerebral iron deposition in neurodegeneration. Biomolecules. 2022;12(5):714. doi:10.3390/biom12050714. PubMed DOI PMC

Cong F, Liu X, Liu C, et al. . Improved depiction of subthalamic nucleus and globus pallidus internus with optimized high-resolution quantitative susceptibility mapping at 7 T. NMR Biomed. 2020;33(11):e4382. doi:10.1002/nbm.4382 PubMed DOI

Yao B, Li T, Gelderen P, Shmueli K, de Zwart J, Duyn J. Susceptibility contrast in high field MRI of human brain as a function of tissue iron content. Neuroimage. 2009;44(4):1259-1266. doi:10.1016/j.neuroimage.2008.10.029 PubMed DOI PMC

Blazejewska AI, Schwarz ST, Pitiot A, et al. . Visualization of nigrosome 1 and its loss in PD: pathoanatomical correlation and in vivo 7 T MRI. Neurology. 2013;81(6):534-540. doi:10.1212/WNL.0b013e31829e6fd2 PubMed DOI PMC

Dal-Bianco A, Grabner G, Kronnerwetter C, et al. . Long-term evolution of multiple sclerosis iron rim lesions in 7 T MRI. Brain. 2021;144(3):833-847. doi:10.1093/brain/awaa436 PubMed DOI

Schrag A, Schott JM. Epidemiological, clinical, and genetic characteristics of early-onset parkinsonism. Lancet Neurol. 2006;5(4):355-363. doi:10.1016/S1474-4422(06)70411-2 PubMed DOI

Ravanfar P, Loi S, Syeda W, et al. . Systematic review: quantitative susceptibility mapping (QSM) of brain iron profile in neurodegenerative diseases. Front Neurosci. 2021;15:618435. doi:10.3389/fnins.2021.618435 PubMed DOI PMC

Levi S, Tiranti V. Neurodegeneration with brain iron accumulation disorders: valuable models aimed at understanding the pathogenesis of iron deposition. Pharmaceuticals (Basel). 2019;12(1):27. doi:10.3390/ph12010027 PubMed DOI PMC

Postuma RB, Berg D, Stern M, et al. . MDS clinical diagnostic criteria for Parkinson's disease. Mov Disord. 2015;30(12):1591-1601. doi:10.1002/mds.26424 PubMed DOI

Gilman S, Wenning GK, Low PA, et al. . Second consensus statement on the diagnosis of multiple system atrophy. Neurology. 2008;71(9):670-676. doi:10.1212/01.wnl.0000324625.00404.15 PubMed DOI PMC

Hoglinger GU, Respondek G, Stamelou M, et al. . Clinical diagnosis of progressive supranuclear palsy: the movement disorder society criteria. Mov Disord. 2017;32(6):853-864. doi:10.1002/mds.26987 PubMed DOI PMC

Shribman S, Bocchetta M, Sudre CH, et al. . Neuroimaging correlates of brain injury in Wilson's disease: a multimodal, whole-brain MRI study. Brain. 2022;145(1):263-275. doi:10.1093/brain/awab274 PubMed DOI PMC

Aggarwal A, Aggarwal N, Nagral A, Jankharia G, Bhatt M. A novel global assessment scale for Wilson's disease (GAS for WD). Mov Disord. 2009;24(4):509-518. doi:10.1002/mds.22231 PubMed DOI

Członkowska A, Tarnacka B, Möller J, et al. . Unified Wilson's Disease Rating Scale: a proposal for the neurological scoring of Wilson's disease patients. Neurol Neurochir Pol. 2007;41:1-12. PubMed

Dusek P, Smolinski L, Redzia-Ogrodnik B, et al. . Semiquantitative scale for assessing brain MRI abnormalities in Wilson disease: a validation study. Mov Disord. 2020;35(6):994-1001. doi:10.1002/mds.28018 PubMed DOI

Acosta-Cabronero J, Milovic C, Mattern H, Tejos C, Speck O, Callaghan MF. A robust multi-scale approach to quantitative susceptibility mapping. Neuroimage. 2018;183:7-24. doi:10.1016/j.neuroimage.2018.07.065 PubMed DOI PMC

Burgetova R, Dusek P, Burgetova A, et al. . Age-related magnetic susceptibility changes in deep grey matter and cerebral cortex of normal young and middle-aged adults depicted by whole brain analysis. Quant Imaging Med Surg. 2021;11(9):3906-3919. doi:10.21037/qims-21-87 PubMed DOI PMC

Coffey AJ, Durkie M, Hague S, et al. . A genetic study of Wilson's disease in the United Kingdom. Brain. 2013;136(pt 5):1476-1487. doi:10.1093/brain/awt035 PubMed DOI PMC

Cheng N, Wang H, Wu W, et al. . Spectrum of ATP7B mutations and genotype-phenotype correlation in large-scale Chinese patients with Wilson Disease. Clin Genet. 2017;92(1):69-79. doi:10.1111/cge.12951 PubMed DOI

Hoch MJ, Bruno MT, Faustin A, et al. . 3T MRI whole-brain microscopy discrimination of subcortical anatomy, part 2: basal forebrain. AJNR Am J Neuroradiol. 2019;40(7):1095-1105. doi:10.3174/ajnr.A6088 PubMed DOI PMC

De Barros A, Arribarat G, Lotterie J, Dominguez G, Chaynes P, Péran P. Iron distribution in the lentiform nucleus: a post-mortem MRI and histology study. Brain Struct Funct. 2021;226(2):351-364. doi:10.1007/s00429-020-02175-7 PubMed DOI

Dezortova M, Lescinskij A, Dusek P, et al. . Multiparametric quantitative brain MRI in neurological and hepatic forms of Wilson's disease. J Magn Reson Imaging. 2020;51(6):1829-1835. doi:10.1002/jmri.26984 PubMed DOI

Jing X-Z, Yuan X-Z, Li G-Y, et al. . Increased magnetic susceptibility in the deep gray matter nuclei of Wilson's disease: have we been ignoring atrophy? Front Neurosci. 2022;16:794375. doi:10.3389/fnins.2022.794375 PubMed DOI PMC

Han Y, Dong J, Xu C, et al. . Application of 9.4T MRI in Wilson disease model TX mice with quantitative susceptibility mapping to assess copper distribution. Front Behav Neurosci. 2020;14:59. doi:10.3389/fnbeh.2020.00059 PubMed DOI PMC

Fritzsch D, Reiss-Zimmermann M, Trampel R, Turner R, Hoffmann K, Schäfer A. Seven-tesla magnetic resonance imaging in Wilson disease using quantitative susceptibility mapping for measurement of copper accumulation. Invest Radiol. 2014;49(5):299-306. doi:10.1097/RLI.0000000000000010 PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...