{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,3]],"date-time":"2026-07-03T07:18:52Z","timestamp":1783063132356,"version":"3.54.6"},"reference-count":50,"publisher":"Wiley","license":[{"start":{"date-parts":[[2026,7,2]],"date-time":"2026-07-02T00:00:00Z","timestamp":1782950400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"},{"start":{"date-parts":[[2026,7,2]],"date-time":"2026-07-02T00:00:00Z","timestamp":1782950400000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Ann Clin Transl Neurol"],"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Objective<\/jats:title>\n                    <jats:p>Cutaneous phosphorylated \u03b1\u2010synuclein (p\u2010syn) and \u03b1\u2010synuclein seeding activity are promising biomarkers for Parkinson's disease (PD), but their clinical value remains uncertain due to disease heterogeneity. This study evaluates these two biomarkers in PD patients to inform phenotype\u2010specific diagnosis and disease severity assessment.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>We compared the diagnostic performance of cutaneous p\u2010syn immunostaining and \u03b1\u2010synuclein seed amplification assay (syn\u2010SAA) in 108 PD patients and 60 controls. Additional analyses assessed the influence of clinical subtypes on p\u2010syn distribution (positive rates and diffusion coefficients across regions), and syn\u2010SAA characteristics, along with their correlations with clinical scales.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      Cutaneous p\u2010syn immunostaining showed 100% specificity and 75% sensitivity, whereas syn\u2010SAA showed 93.3% specificity and 86.1% sensitivity. Among the clinical subtypes, a significant regional difference in the diffusion coefficient was observed only in the suspected REM sleep behavior disorder subgroup, with higher values in the distal leg than in the posterior cervical region (\n                      <jats:italic>p<\/jats:italic>\n                      \u2009=\u20090.001). The diffusion coefficient correlated with the severity of both motor and non\u2010motor symptoms (all\n                      <jats:italic>p<\/jats:italic>\n                      \u2009&lt;\u20090.05). No significant differences in syn\u2010SAA positivity rates or parameters were found across clinical subtypes. Syn\u2010SAA parameters were consistent across biopsy sites and associated with disease duration and non\u2010motor symptom severity, but not with motor symptom severity.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Interpretation<\/jats:title>\n                    <jats:p>These findings highlight complementary roles for skin biomarkers in PD. P\u2010syn deposition shows regional \u03b1\u2010synuclein aggregation, reflecting clinical heterogeneity and supporting phenotype\u2010specific diagnosis and severity assessment, whereas \u03b1\u2010synuclein seeding activity enables early diagnosis and may serve as a potential biomarker for monitoring disease progression.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1002\/acn3.70465","type":"journal-article","created":{"date-parts":[[2026,7,3]],"date-time":"2026-07-03T06:49:19Z","timestamp":1783061359000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Characterizing Cutaneous \u03b1\u2010Synuclein Deposition and Seeding Activity in Parkinson's Disease Subtypes"],"prefix":"10.1002","author":[{"given":"Yuting","family":"Jin","sequence":"first","affiliation":[{"name":"Department of Neurology The First Affiliated Hospital of Zhengzhou University  Zhengzhou Henan China"},{"name":"Department of Neurology Kaifeng Central Hospital  Kaifeng Henan China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tianyuan","family":"Yang","sequence":"additional","affiliation":[{"name":"Department of Neurology The First Affiliated Hospital of Zhengzhou University  Zhengzhou Henan China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6722-1305","authenticated-orcid":false,"given":"Minglei","family":"Liu","sequence":"additional","affiliation":[{"name":"Department of Neurology The First Affiliated Hospital of Zhengzhou University  Zhengzhou Henan China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haiyang","family":"Luo","sequence":"additional","affiliation":[{"name":"Department of Neurology The First Affiliated Hospital of Zhengzhou University  Zhengzhou Henan China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jing","family":"Yuan","sequence":"additional","affiliation":[{"name":"Department of Neurology The First Affiliated Hospital of Zhengzhou University  Zhengzhou Henan China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ke","family":"Zhang","sequence":"additional","affiliation":[{"name":"Department of Neurology The First Affiliated Hospital of Zhengzhou University  Zhengzhou Henan China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8630-5926","authenticated-orcid":false,"given":"Xinsheng","family":"Han","sequence":"additional","affiliation":[{"name":"Department of Neurology Kaifeng Central Hospital  Kaifeng Henan China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7356-5083","authenticated-orcid":false,"given":"Jing","family":"Yang","sequence":"additional","affiliation":[{"name":"Department of Neurology The First Affiliated Hospital of Zhengzhou University  Zhengzhou Henan China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2689-9897","authenticated-orcid":false,"given":"Yuming","family":"Xu","sequence":"additional","affiliation":[{"name":"Department of Neurology The First Affiliated Hospital of Zhengzhou University  Zhengzhou Henan China"},{"name":"Tianjian Laboratory of Advanced Biomedical Sciences, School of Life Sciences Zhengzhou University  Zhengzhou Henan China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,7,2]]},"reference":[{"key":"e_1_2_11_2_1","doi-asserted-by":"crossref","first-page":"1298","DOI":"10.1001\/jama.2024.0792","article-title":"Skin Biopsy Detection of Phosphorylated \u03b1\u2010Synuclein in Patients With Synucleinopathies","volume":"331","author":"Gibbons C. H.","year":"2024","journal-title":"JAMA"},{"key":"e_1_2_11_3_1","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/S0140-6736(23)01478-2","article-title":"The Pathogenesis of Parkinson's Disease","volume":"403","author":"Morris H. R.","year":"2024","journal-title":"Lancet"},{"key":"e_1_2_11_4_1","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1007\/s00401-010-0664-3","article-title":"Multi\u2010Organ Distribution of Phosphorylated \u03b1\u2010Synuclein Histopathology in Subjects With Lewy Body Disorders","volume":"119","author":"Beach T. 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M.","year":"2017","journal-title":"Journal of Neuropathology and Experimental Neurology"},{"key":"e_1_2_11_7_1","doi-asserted-by":"crossref","first-page":"1362","DOI":"10.1212\/WNL.0000000000000316","article-title":"Skin Nerve \u03b1\u2010Synuclein Deposits: A Biomarker for Idiopathic Parkinson Disease","volume":"82","author":"Donadio V.","year":"2014","journal-title":"Neurology"},{"key":"e_1_2_11_8_1","doi-asserted-by":"crossref","first-page":"1452","DOI":"10.1002\/mds.27794","article-title":"Value of In\u00a0Vivo \u03b1\u2010Synuclein Deposits in Parkinson's Disease: A Systematic Review and Meta\u2010Analysis","volume":"34","author":"Tsukita K.","year":"2019","journal-title":"Movement Disorders"},{"key":"e_1_2_11_9_1","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1002\/acn3.52282","article-title":"Alpha\u2010Synuclein RT\u2010QuIC Assay in Gastroduodenal and Skin Biopsies of Parkinson Disease Patients","volume":"12","author":"Emmi A.","year":"2025","journal-title":"Annals of Clinical Translational Neurology"},{"key":"e_1_2_11_10_1","doi-asserted-by":"crossref","first-page":"517","DOI":"10.3233\/JPD-181434","article-title":"Feasibility and Safety of Multicenter Tissue and Biofluid Sampling for \u03b1\u2010Synuclein in Parkinson's Disease: The Systemic Synuclein Sampling Study (S4)","volume":"8","author":"Chahine L. M.","year":"2018","journal-title":"Journal of Parkinson's Disease"},{"key":"e_1_2_11_11_1","doi-asserted-by":"crossref","first-page":"895","DOI":"10.1002\/mds.28399","article-title":"Immunohistochemical Detection of Synuclein Pathology in Skin in Idiopathic Rapid Eye Movement Sleep Behavior Disorder and Parkinsonism","volume":"36","author":"Al\u2010Qassabi A.","year":"2021","journal-title":"Movement Disorders"},{"key":"e_1_2_11_12_1","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1001\/jamaneurol.2020.3311","article-title":"Skin \u03b1\u2010Synuclein Aggregation Seeding Activity as a Novel Biomarker for Parkinson Disease","volume":"78","author":"Wang Z.","year":"2020","journal-title":"JAMA Neurology"},{"key":"e_1_2_11_13_1","doi-asserted-by":"crossref","first-page":"e2513","DOI":"10.1212\/WNL.0000000000011935","article-title":"In Vivo Diagnosis of Synucleinopathies: A Comparative Study of Skin Biopsy and RT\u2010QuIC","volume":"96","author":"Donadio V.","year":"2021","journal-title":"Neurology"},{"key":"e_1_2_11_14_1","doi-asserted-by":"crossref","first-page":"2310","DOI":"10.1093\/brain\/awv138","article-title":"Phosphorylated \u03b1\u2010Synuclein in Skin Nerve Fibres Differentiates Parkinson's Disease From Multiple System Atrophy","volume":"138","author":"Zange L.","year":"2015","journal-title":"Brain"},{"key":"e_1_2_11_15_1","doi-asserted-by":"crossref","first-page":"1649","DOI":"10.1002\/mds.28126","article-title":"Skin Biopsy May Help to Distinguish Multiple System Atrophy\u2013Parkinsonism From Parkinson's Disease With Orthostatic Hypotension","volume":"35","author":"Donadio V.","year":"2020","journal-title":"Movement Disorders"},{"key":"e_1_2_11_16_1","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1038\/s41531-024-00730-1","article-title":"Disease Progression in Proposed Brain\u2010First and Body\u2010First Parkinson's Disease Subtypes","volume":"10","author":"Xu Z.","year":"2024","journal-title":"NPJ Parkinsons Disease"},{"key":"e_1_2_11_17_1","doi-asserted-by":"crossref","first-page":"2128","DOI":"10.1212\/WNL.0000000000003989","article-title":"Skin Nerve Phosphorylated \u03b1\u2010Synuclein Deposits in Idiopathic REM Sleep Behavior Disorder","volume":"88","author":"Antelmi E.","year":"2017","journal-title":"Neurology"},{"key":"e_1_2_11_18_1","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1007\/s00401-017-1684-z","article-title":"Dermal Phospho\u2010Alpha\u2010Synuclein Deposits Confirm REM Sleep Behaviour Disorder as Prodromal Parkinson's Disease","volume":"133","author":"Doppler K.","year":"2017","journal-title":"Acta Neuropathologica"},{"key":"e_1_2_11_19_1","doi-asserted-by":"crossref","first-page":"856","DOI":"10.1093\/brain\/awaf313","article-title":"Skin Intraneural Phosphorylated \u03b1\u2010Synuclein Is a Highly Specific Biomarker for Early Parkinson's Disease","volume":"149","author":"Donadio V.","year":"2026","journal-title":"Brain"},{"key":"e_1_2_11_20_1","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/S0197-4580(02)00065-9","article-title":"Staging of Brain Pathology Related to Sporadic Parkinson's Disease","volume":"24","author":"Braak H.","year":"2003","journal-title":"Neurobiology of Aging"},{"key":"e_1_2_11_21_1","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1038\/nrn3887","article-title":"Spreading of Pathology in Neurodegenerative Diseases: A Focus on Human Studies","volume":"16","author":"Brettschneider J.","year":"2015","journal-title":"Nature Reviews. 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R.","year":"2018","journal-title":"Acta Neuropathologica Communications"},{"key":"e_1_2_11_26_1","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1111\/ane.12247","article-title":"Alpha\u2010Synuclein in Peripheral Tissues and Body Fluids as a Biomarker for Parkinson's Disease \u2010 a Systematic Review","volume":"130","author":"Malek N.","year":"2014","journal-title":"Acta Neurologica Scandinavica"},{"key":"e_1_2_11_27_1","doi-asserted-by":"crossref","first-page":"812","DOI":"10.1002\/acn3.338","article-title":"Alpha\u2010Synuclein RT\u2010QuIC in the CSF of Patients With Alpha\u2010Synucleinopathies","volume":"3","author":"Fairfoul G.","year":"2016","journal-title":"Annals of Clinical and Translational Neurology"},{"key":"e_1_2_11_28_1","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1038\/s41582-021-00486-9","article-title":"Prodromal Parkinson Disease Subtypes \u2014 Key to Understanding Heterogeneity","volume":"17","author":"Berg D.","year":"2021","journal-title":"Nature Reviews. Neurology"},{"key":"e_1_2_11_29_1","doi-asserted-by":"crossref","first-page":"1591","DOI":"10.1002\/mds.26424","article-title":"MDS Clinical Diagnostic Criteria for Parkinson's Disease","volume":"30","author":"Postuma R. B.","year":"2015","journal-title":"Movement Disorders"},{"key":"e_1_2_11_30_1","doi-asserted-by":"crossref","first-page":"2314","DOI":"10.1002\/mds.21844","article-title":"Diagnostic Procedures for Parkinson's Disease Dementia: Recommendations From the Movement Disorder Society Task Force","volume":"22","author":"Dubois B.","year":"2007","journal-title":"Movement Disorders"},{"key":"e_1_2_11_31_1","doi-asserted-by":"crossref","first-page":"952","DOI":"10.1016\/j.sleep.2014.03.020","article-title":"Validation Study of REM Sleep Behavior Disorder Questionnaire\u2010Hong Kong (RBDQ\u2010HK) in East China","volume":"15","author":"Shen S. 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G.","year":"2025","journal-title":"eBioMedicine"},{"key":"e_1_2_11_50_1","doi-asserted-by":"crossref","first-page":"104076","DOI":"10.1016\/j.ebiom.2022.104076","article-title":"Skin Alpha\u2010Synuclein Deposit Patterns: A Predictor of Parkinson's Disease Subtypes","volume":"80","author":"Han Y.","year":"2022","journal-title":"eBioMedicine"},{"key":"e_1_2_11_51_1","doi-asserted-by":"crossref","first-page":"580","DOI":"10.1016\/S1474-4422(25)00157-7","article-title":"Diagnostic and Prognostic Value of \u03b1\u2010Synuclein Seed Amplification Assay Kinetic Measures in Parkinson's Disease: A Longitudinal Cohort Study","volume":"24","author":"Orr\u00fa C. 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