{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T22:25:51Z","timestamp":1792794351366,"version":"4.5.0"},"reference-count":43,"publisher":"Oxford University Press (OUP)","issue":"1","license":[{"start":{"date-parts":[[2023,8,1]],"date-time":"2023-08-01T00:00:00Z","timestamp":1690848000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100002996","name":"Dutch Heart Foundation","doi-asserted-by":"crossref","award":["2016 T044"],"award-info":[{"award-number":["2016 T044"]}],"id":[{"id":"10.13039\/501100002996","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100002996","name":"Dutch Heart Foundation","doi-asserted-by":"crossref","award":["2014 T060"],"award-info":[{"award-number":["2014 T060"]}],"id":[{"id":"10.13039\/501100002996","id-type":"DOI","asserted-by":"crossref"}]},{"name":"Netherlands CardioVascular Research Initiative: the Dutch Heart Foundation","award":["CVON 2018-28"],"award-info":[{"award-number":["CVON 2018-28"]}],"id":[{"id":"https:\/\/ror.org\/05nxhgm70","id-type":"ROR","asserted-by":"crossref"}]},{"name":"Netherlands CardioVascular Research Initiative: the Dutch Heart Foundation","award":["2012-06"],"award-info":[{"award-number":["2012-06"]}],"id":[{"id":"https:\/\/ror.org\/05nxhgm70","id-type":"ROR","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001826","name":"Netherlands Organization for Health Research and Development","doi-asserted-by":"crossref","award":["016.126.351"],"award-info":[{"award-number":["016.126.351"]}],"id":[{"id":"10.13039\/501100001826","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,1,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>To investigate whether structural network disconnectivity is associated with parkinsonian signs and their progression, as well as with an increased risk of incident parkinsonism.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>In a prospective cohort (Radboud University Nijmegen Diffusion Tensor and Magnetic Resonance Cohort study) consisting of 293 participants with small vessel disease (SVD), we assessed parkinsonian signs and incident parkinsonism over an 8-year follow-up. In addition, we reconstructed the white matter network followed by graph-theoretical analyses to compute the network metrics. Conventional magnetic resonance imaging markers for SVD were assessed.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>We included 293 patients free of parkinsonism at baseline (2011), with a mean age 68.8 (standard deviation [SD] 8.4) years, and 130 (44.4%) were men. Nineteen participants (6.5%) developed parkinsonism during a median (SD) follow-up time of 8.3 years. Compared with participants without parkinsonism, those with all-cause parkinsonism had higher Unified Parkinson\u2019s Disease Rating scale (UPDRS) scores and lower global efficiency at baseline. Baseline global efficiency was associated with UPDRS motor scores in 2011 (\u03b2 = \u22120.047, p\u2005&amp;lt;\u2005.001) and 2015 (\u03b2 = \u22120.84, p\u2005&amp;lt;\u2005.001), as well as with the changes in UPDRS scores during the 4-year follow-up (\u03b2 = \u22120.63, p\u2005=\u2005.004). In addition, at the regional level, we identified an inter-hemispheric disconnected network associated with an increased UPDRS motor score. Besides, lower global efficiency was associated with an increased risk of all-cause and vascular parkinsonism independent of SVD markers.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>Our findings suggest that global network efficiency is associated with a gradual decline in motor performance, ultimately leading to incident parkinsonism in the elderly with SVD. Global network efficiency may have the added value to serve as a useful marker to capture changes in motor signs.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1093\/gerona\/glad182","type":"journal-article","created":{"date-parts":[[2023,7,28]],"date-time":"2023-07-28T09:01:06Z","timestamp":1690534866000},"source":"Crossref","is-referenced-by-count":5,"title":["Structural Network Efficiency Predicts Conversion to Incident Parkinsonism in Patients With Cerebral Small Vessel Disease"],"prefix":"10.1093","volume":"79","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0927-2558","authenticated-orcid":false,"given":"Mengfei","family":"Cai","sequence":"first","affiliation":[{"name":"Department of Neurology, Guangdong Cardiovascular Institute, Guangdong Neuroscience Institute, Guangdong Provincial People\u2019s Hospital, Guangdong Academy of Medical Sciences, Southern Medical University , Guangzhou , People\u2019s Republic of China"},{"name":"Department of Neurology, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behaviour , Nijmegen , The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mina A","family":"Jacob","sequence":"additional","affiliation":[{"name":"Department of Neurology, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behaviour , Nijmegen , The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jos\u00e9","family":"Marques","sequence":"additional","affiliation":[{"name":"Donders Institute for Brain, Cognition and Behaviour, Radboud University , Nijmegen , The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David G","family":"Norris","sequence":"additional","affiliation":[{"name":"Donders Institute for Brain, Cognition and Behaviour, Radboud University , Nijmegen , The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2302-3136","authenticated-orcid":false,"given":"Marco","family":"Duering","sequence":"additional","affiliation":[{"name":"Medical Image Analysis Center (MIAC AG) and qbig, Department of Biomedical Engineering, University of Basel , Basel , Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rianne A J","family":"Esselink","sequence":"additional","affiliation":[{"name":"Department of Neurology, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behaviour , Nijmegen , The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuhu","family":"Zhang","sequence":"additional","affiliation":[{"name":"Department of Neurology, Guangdong Neuroscience Institute, Guangdong Provincial People\u2019s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University , Guangzhou , People\u2019s Republic of China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Frank-Erik","family":"de Leeuw","sequence":"additional","affiliation":[{"name":"Department of Neurology, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behaviour , Nijmegen , The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anil M","family":"Tuladhar","sequence":"additional","affiliation":[{"name":"Department of Neurology, Radboud University Medical Center, Donders Institute for Brain, Cognition and Behaviour , Nijmegen , The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2023,8,1]]},"reference":[{"issue":"7","key":"2023122103445388200_CIT0001","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1038\/s41582-018-0014-y","article-title":"Cerebral small vessel disease: from a focal to a global perspective","volume":"14","author":"Ter Telgte","year":"2018","journal-title":"Nat Rev Neurol."},{"issue":"10","key":"2023122103445388200_CIT0002","doi-asserted-by":"crossref","first-page":"2574","DOI":"10.1161\/STROKEAHA.112.657130","article-title":"Cerebral white matter lesions and lacunar infarcts contribute to the presence of mild Parkinsonian signs","volume":"43","author":"de Laat","year":"2012","journal-title":"Stroke."},{"issue":"18","key":"2023122103445388200_CIT0003","doi-asserted-by":"crossref","first-page":"1569","DOI":"10.1212\/WNL.0000000000002082","article-title":"Cerebral small vessel disease and incident parkinsonism: the RUN DMC study","volume":"85","author":"van der Holst","year":"2015","journal-title":"Neurology."},{"key":"2023122103445388200_CIT0004","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1016\/j.nicl.2017.12.007","article-title":"White matter changes and gait decline in cerebral small vessel disease","volume":"17","author":"van der Holst","year":"2018","journal-title":"Neuroimage Clin"},{"key":"2023122103445388200_CIT0005","doi-asserted-by":"crossref","first-page":"102667","DOI":"10.1016\/j.nicl.2021.102667","article-title":"Cognition mediates the relation between structural network efficiency and gait in small vessel disease","volume":"30","author":"Cai","year":"2021","journal-title":"NeuroImage: Clin"},{"issue":"3","key":"2023122103445388200_CIT0006","doi-asserted-by":"crossref","first-page":"554","DOI":"10.1093\/gerona\/glab247","article-title":"Longitudinal relation between structural network efficiency, cognition, and gait in cerebral small vessel disease","volume":"77","author":"Cai","year":"2022","journal-title":"J Gerontol A Biol Sci Med Sci."},{"key":"2023122103445388200_CIT0007","doi-asserted-by":"crossref","first-page":"102325","DOI":"10.1016\/j.nicl.2020.102325","article-title":"Structural network efficiency predicts cognitive decline in cerebral small vessel disease","volume":"27","author":"Boot","year":"2020","journal-title":"NeuroImage: Clin"},{"key":"2023122103445388200_CIT0008","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1016\/j.neurobiolaging.2020.08.005","article-title":"White matter hyperintensities and the progression from mild parkinsonian signs to parkinsonism and Parkinson\u2019s disease","volume":"96","author":"Huo","year":"2020","journal-title":"Neurobiol Aging."},{"key":"2023122103445388200_CIT0009","doi-asserted-by":"crossref","first-page":"531993","DOI":"10.3389\/fneur.2020.531993","article-title":"Diffusion tensor imaging in Parkinson\u2019s disease and parkinsonian syndrome: a systematic review","volume":"11","author":"Zhang","year":"2020","journal-title":"Front Neurol."},{"key":"2023122103445388200_CIT0010","doi-asserted-by":"crossref","first-page":"841","DOI":"10.3389\/fneur.2020.00841","article-title":"Structural network analysis using diffusion MRI tractography in Parkinson\u2019s disease and correlations with motor impairment","volume":"11","author":"Kok","year":"2020","journal-title":"Front Neurol."},{"issue":"2","key":"2023122103445388200_CIT0011","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1148\/radiol.2016160274","article-title":"Structural brain connectome and cognitive impairment in Parkinson disease","volume":"283","author":"Galantucci","year":"2017","journal-title":"Radiology."},{"issue":"6","key":"2023122103445388200_CIT0012","doi-asserted-by":"crossref","first-page":"1130","DOI":"10.1002\/ana.26615","article-title":"Cerebral small vessel disease progression increases risk of incident parkinsonism","volume":"93","author":"Jacob","year":"2023","journal-title":"Ann Neurol."},{"issue":"1","key":"2023122103445388200_CIT0013","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1186\/1471-2377-11-29","article-title":"Causes and consequences of cerebral small vessel disease. The RUN DMC study: a prospective cohort study. Study rationale and protocol","volume":"11","author":"van Norden","year":"2011","journal-title":"BMC Neurol."},{"issue":"3","key":"2023122103445388200_CIT0014","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1002\/mds.870100305","article-title":"Teaching tape for the motor section of the unified Parkinson\u2019s disease rating scale","volume":"10","author":"Goetz","year":"1995","journal-title":"Mov Disord."},{"issue":"5","key":"2023122103445388200_CIT0015","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1002\/mds.10459","article-title":"SIC Task Force appraisal of clinical diagnostic criteria for parkinsonian disorders","volume":"18","author":"Litvan","year":"2003","journal-title":"Mov Disord."},{"issue":"5","key":"2023122103445388200_CIT0016","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1001\/archneur.63.5.717","article-title":"History of vascular disease and mild parkinsonian signs in community-dwelling elderly individuals","volume":"63","author":"Louis","year":"2006","journal-title":"Arch Neurol."},{"issue":"3","key":"2023122103445388200_CIT0017","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1136\/jnnp.55.3.181","article-title":"Accuracy of clinical diagnosis of idiopathic Parkinson\u2019s disease: a clinico-pathological study of 100 cases","volume":"55","author":"Hughes","year":"1992","journal-title":"J Neurol Neurosurg Psychiatry"},{"issue":"6","key":"2023122103445388200_CIT0018","doi-asserted-by":"crossref","first-page":"630","DOI":"10.1002\/mds.20083","article-title":"Clinicopathological investigation of vascular parkinsonism, including clinical criteria for diagnosis","volume":"19","author":"Zijlmans","year":"2004","journal-title":"Mov Disord."},{"issue":"2","key":"2023122103445388200_CIT0019","doi-asserted-by":"crossref","first-page":"351","DOI":"10.2214\/ajr.149.2.351","article-title":"MR signal abnormalities at 1.5 T in Alzheimer\u2019s dementia and normal aging","volume":"149","author":"Fazekas","year":"1987","journal-title":"Am J Roentgenol"},{"issue":"9","key":"2023122103445388200_CIT0020","doi-asserted-by":"crossref","first-page":"2789","DOI":"10.1161\/STROKEAHA.121.038099","article-title":"Determinants and temporal dynamics of cerebral small vessel disease: 14-year follow-up","volume":"53","author":"Cai","year":"2022","journal-title":"Stroke."},{"issue":"8","key":"2023122103445388200_CIT0021","doi-asserted-by":"crossref","first-page":"822","DOI":"10.1016\/S1474-4422(13)70124-8","article-title":"Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration","volume":"12","author":"Wardlaw","year":"2013","journal-title":"Lancet Neurol"},{"issue":"12","key":"2023122103445388200_CIT0022","doi-asserted-by":"crossref","first-page":"6246","DOI":"10.1118\/1.4966029","article-title":"Automated detection of white matter hyperintensities of all sizes in cerebral small vessel disease: automated detection of white matter hyperintensities of all sizes","volume":"43","author":"Ghafoorian","year":"2016","journal-title":"Med Phys."},{"issue":"15","key":"2023122103445388200_CIT0023","doi-asserted-by":"crossref","first-page":"1569","DOI":"10.1212\/WNL.0000000000004490","article-title":"Nonlinear temporal dynamics of cerebral small vessel disease: the RUN DMC study","volume":"89","author":"van Leijsen","year":"2017","journal-title":"Neurology."},{"issue":"9","key":"2023122103445388200_CIT0024","doi-asserted-by":"crossref","first-page":"e73021","DOI":"10.1371\/journal.pone.0073021","article-title":"Diffusion weighted image denoising using overcomplete local PCA","volume":"8","author":"Manj\u00f3n","year":"2013","journal-title":"PLoS One."},{"issue":"2","key":"2023122103445388200_CIT0025","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1016\/j.neuroimage.2010.06.014","article-title":"Patching cardiac and head motion artefacts in diffusion-weighted images","volume":"53","author":"Zwiers","year":"2010","journal-title":"Neuroimage."},{"key":"2023122103445388200_CIT0026","doi-asserted-by":"crossref","first-page":"S208","DOI":"10.1016\/j.neuroimage.2004.07.051","article-title":"Advances in functional and structural MR image analysis and implementation as FSL","volume":"23","author":"Smith","year":"2004","journal-title":"Neuroimage."},{"issue":"4","key":"2023122103445388200_CIT0027","doi-asserted-by":"crossref","first-page":"304","DOI":"10.1212\/WNL.0000000000000612","article-title":"Structural network efficiency is associated with cognitive impairment in small-vessel disease","volume":"83","author":"Lawrence","year":"2014","journal-title":"Neurology."},{"issue":"1","key":"2023122103445388200_CIT0028","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1006\/nimg.2001.0978","article-title":"Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain","volume":"15","author":"Tzourio-Mazoyer","year":"2002","journal-title":"Neuroimage."},{"issue":"2","key":"2023122103445388200_CIT0029","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1006\/nimg.2002.1132","article-title":"Improved optimization for the robust and accurate linear registration and motion correction of brain images","volume":"17","author":"Jenkinson","year":"2002","journal-title":"Neuroimage."},{"issue":"3","key":"2023122103445388200_CIT0030","doi-asserted-by":"crossref","first-page":"2033","DOI":"10.1016\/j.neuroimage.2010.09.025","article-title":"A reproducible evaluation of ANTs similarity metric performance in brain image registration","volume":"54","author":"Avants","year":"2011","journal-title":"Neuroimage."},{"issue":"7","key":"2023122103445388200_CIT0031","doi-asserted-by":"crossref","first-page":"e597","DOI":"10.1371\/journal.pone.0000597","article-title":"Mapping human whole-brain structural networks with diffusion MRI","volume":"2","author":"Hagmann","year":"2007","journal-title":"PLoS One."},{"issue":"21","key":"2023122103445388200_CIT0032","doi-asserted-by":"crossref","first-page":"e1898","DOI":"10.1212\/WNL.0000000000005551","article-title":"Longitudinal decline in structural networks predicts dementia in cerebral small vessel disease","volume":"90","author":"Lawrence","year":"2018","journal-title":"Neurology."},{"issue":"3","key":"2023122103445388200_CIT0033","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1089\/brain.2019.0686","article-title":"Effect of fixed-density thresholding on structural brain networks: a demonstration in cerebral small vessel disease","volume":"10","author":"de Brito Robalo","year":"2020","journal-title":"Brain Connect."},{"issue":"2","key":"2023122103445388200_CIT0034","doi-asserted-by":"crossref","first-page":"e17","DOI":"10.1371\/journal.pcbi.0030017","article-title":"Efficiency and cost of economical brain functional networks","volume":"3","author":"Achard","year":"2007","journal-title":"PLoS Comput Biol."},{"issue":"2","key":"2023122103445388200_CIT0035","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1161\/STROKEAHA.114.007146","article-title":"Relationship between white matter hyperintensities, cortical thickness, and cognition","volume":"46","author":"Tuladhar","year":"2015","journal-title":"Stroke."},{"issue":"4","key":"2023122103445388200_CIT0036","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1002\/ana.24758","article-title":"A novel imaging marker for small vessel disease based on skeletonization of white matter tracts and diffusion histograms: novel SVD imaging marker","volume":"80","author":"Baykara","year":"2016","journal-title":"Ann Neurol."},{"issue":"27","key":"2023122103445388200_CIT0037","doi-asserted-by":"crossref","first-page":"4391","DOI":"10.1002\/sim.7501","article-title":"Practical recommendations for reporting Fine-Gray model analyses for competing risk data","volume":"36","author":"Austin","year":"2017","journal-title":"Stat Med."},{"key":"2023122103445388200_CIT0038","doi-asserted-by":"crossref","first-page":"1020","DOI":"10.1177\/0271678X211069228","article-title":"Systematic validation of structural brain networks in cerebral small vessel disease","volume":"42","author":"Dewenter","year":"2021","journal-title":"J Cereb Blood Flow Metab."},{"issue":"8","key":"2023122103445388200_CIT0039","doi-asserted-by":"crossref","first-page":"1652","DOI":"10.1161\/STROKEAHA.110.583229","article-title":"Gait in elderly with cerebral small vessel disease","volume":"41","author":"de Laat","year":"2010","journal-title":"Stroke."},{"issue":"4","key":"2023122103445388200_CIT0040","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1038\/nrneurol.2011.21","article-title":"White matter lesions in Parkinson disease","volume":"7","author":"Bohnen","year":"2011","journal-title":"Nat Rev Neurol."},{"issue":"7","key":"2023122103445388200_CIT0041","doi-asserted-by":"crossref","first-page":"300","DOI":"10.1016\/S0166-2236(96)60018-6","article-title":"Cortex cerebri. performance, structural and functional organization of the cortex","volume":"19","author":"Garey","year":"1996","journal-title":"Trends Neurosci."},{"issue":"12","key":"2023122103445388200_CIT0042","doi-asserted-by":"crossref","first-page":"1494","DOI":"10.1001\/jamaneurol.2021.3996","article-title":"Association of white matter hyperintensities with pathology and progression of parkinsonism in aging","volume":"78","author":"Oveisgharan","year":"2021","journal-title":"JAMA Neurol"},{"issue":"7\u20138","key":"2023122103445388200_CIT0043","doi-asserted-by":"crossref","first-page":"468","DOI":"10.1002\/nbm.781","article-title":"Fiber tracking: principles and strategies\u2014a technical review","volume":"15","author":"Mori","year":"2002","journal-title":"NMR Biomed."}],"container-title":["The Journals of Gerontology: Series A"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/biomedgerontology\/advance-article-pdf\/doi\/10.1093\/gerona\/glad182\/51258800\/glad182.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/biomedgerontology\/article-pdf\/79\/1\/glad182\/54705352\/glad182.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/biomedgerontology\/article-pdf\/79\/1\/glad182\/54705352\/glad182.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,12,20]],"date-time":"2023-12-20T22:46:39Z","timestamp":1703112399000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/biomedgerontology\/article\/doi\/10.1093\/gerona\/glad182\/7235047"}},"subtitle":[],"editor":[{"given":"Lewis A","family":"Lipsitz","sequence":"additional","affiliation":[{"name":"(Medical Sciences Section)"}],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2023,8,1]]},"references-count":43,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2024,1,1]]}},"URL":"https:\/\/doi.org\/10.1093\/gerona\/glad182","relation":{},"ISSN":["1079-5006","1758-535X"],"issn-type":[{"value":"1079-5006","type":"print"},{"value":"1758-535X","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2024,1,1]]},"published":{"date-parts":[[2023,8,1]]},"article-number":"glad182"}}