{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T12:28:41Z","timestamp":1791894521429,"version":"4.3.4"},"reference-count":66,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,4,18]],"date-time":"2024-04-18T00:00:00Z","timestamp":1713398400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Neurosci."],"abstract":"<jats:sec><jats:title>Introduction<\/jats:title><jats:p>Mild cognitive impairment (MCI) is a common symptom observed in individuals with Parkinson\u2019s disease (PD) and a main risk factor for progressing to dementia. Our objective was to identify early anatomical brain changes that precede the transition from healthy cognition to MCI in PD.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>Structural T1-weighted magnetic resonance imaging data of PD patients with healthy cognition at baseline were downloaded from the Parkinson\u2019s Progression Markers Initiative database. Patients were divided into two groups based on the annual cognitive assessments over a 5-year time span: (i) PD patients with unstable healthy cognition who developed MCI over a 5-year follow-up (PD-UHC, <jats:italic>n<\/jats:italic> = 52), and (ii) PD patients who maintained stable healthy cognitive function over the same period (PD-SHC, <jats:italic>n<\/jats:italic> = 52). These 52 PD-SHC were selected among 192 PD-SHC patients using propensity score matching method to have similar demographic and clinical characteristics with PD-UHC at baseline. Seventy-five percent of these were used to train a support vector machine (SVM) algorithm to distinguish between the PD-UHC and PD-SHC groups, and tested on the remaining 25% of individuals. Shapley Additive Explanations (SHAP) feature analysis was utilized to identify the most informative brain regions in SVM classifier.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>The average accuracy of classifying PD-UHC vs. PD-SHC was 80.76%, with 82.05% sensitivity and 79.48% specificity using 10-fold cross-validation. The performance was similar in the hold-out test sets with all accuracy, sensitivity, and specificity at 76.92%. SHAP analysis showed that the most influential brain regions in the prediction model were located in the frontal, occipital, and cerebellar regions as well as midbrain.<\/jats:p><\/jats:sec><jats:sec><jats:title>Discussion<\/jats:title><jats:p>Our machine learning-based analysis yielded promising results in identifying PD individuals who are at risk of cognitive decline from the earliest disease stage and revealed the brain regions which may be linked to the prospective cognitive decline in PD before clinical symptoms emerge.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fnins.2024.1375395","type":"journal-article","created":{"date-parts":[[2024,4,18]],"date-time":"2024-04-18T04:20:16Z","timestamp":1713414016000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":13,"title":["Predicting the occurrence of mild cognitive impairment in Parkinson\u2019s disease using structural MRI data"],"prefix":"10.3389","volume":"18","author":[{"given":"Iman","family":"Beheshti","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ji Hyun","family":"Ko","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2024,4,18]]},"reference":[{"key":"B1","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1016\/j.jns.2009.08.034","article-title":"The epidemiology of dementia associated with Parkinson disease.","volume":"289","author":"Aarsland","year":"2010","journal-title":"J. Neurol. Sci."},{"key":"B2","doi-asserted-by":"publisher","first-page":"387","DOI":"10.1001\/archneur.60.3.387","article-title":"Prevalence and characteristics of dementia in Parkinson disease: An 8-year prospective study.","volume":"60","author":"Aarsland","year":"2003","journal-title":"Arch. Neurol."},{"key":"B3","article-title":"Parkinson disease-associated cognitive impairment.","volume":"7","author":"Aarsland","year":"2021","journal-title":"Nat. Rev. Dis. Prim."},{"key":"B4","doi-asserted-by":"crossref","first-page":"1121","DOI":"10.1212\/01.wnl.0000338632.00552.cb","article-title":"\u201cCognitive impairment in incident, untreated Parkinson disease: The Norwegian ParkWest study.","volume":"72","author":"Aarsland","year":"2009","journal-title":"Neurology"},{"key":"B5","doi-asserted-by":"crossref","first-page":"1062","DOI":"10.1212\/WNL.0b013e3181f39d0e","article-title":"Mild cognitive impairment in Parkinson disease: A multicenter pooled analysis.","volume":"75","author":"Aarsland","year":"2010","journal-title":"Neurology"},{"key":"B6","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1038\/nrneurol.2017.27","article-title":"Cognitive decline in Parkinson disease.","volume":"13","author":"Aarsland","year":"2017","journal-title":"Nat. Rev. Neurol."},{"key":"B7","doi-asserted-by":"crossref","first-page":"1255","DOI":"10.1002\/mds.20527","article-title":"A systematic review of prevalence studies of dementia in Parkinson\u2019s disease.","volume":"20","author":"Aarsland","year":"2005","journal-title":"Mov. Disord."},{"key":"B8","doi-asserted-by":"crossref","first-page":"159","DOI":"10.3233\/JPD-160925","article-title":"Dementia predictors in Parkinson disease: A validation study.","volume":"7","author":"Anang","year":"2017","journal-title":"J. Parkinsons Dis."},{"key":"B9","doi-asserted-by":"crossref","DOI":"10.1016\/j.neulet.2021.136105","article-title":"Role of the cerebellum in the phenotype of neurodegenerative diseases: Mitigate or exacerbate?","volume":"760","author":"Azizi","year":"2021","journal-title":"Neurosci. Lett."},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.1186\/s10020-021-00284-5","article-title":"Modulating brain networks associated with cognitive deficits in Parkinson\u2019s disease.","volume":"27","author":"Beheshti","year":"2021","journal-title":"Mol. Med."},{"key":"B11","doi-asserted-by":"crossref","first-page":"364","DOI":"10.1001\/archneur.1978.00500300038006","article-title":"\u201cVisuospatial judgment: A clinical test\u201d.","volume":"35","author":"Benton","year":"1978","journal-title":"Arch. Neurol."},{"key":"B12","doi-asserted-by":"publisher","first-page":"254","DOI":"10.1136\/jnnp.2006.093849","article-title":"A magnetic resonance imaging study of patients with Parkinson\u2019s disease with mild cognitive impairment and dementia using voxel-based morphometry.","volume":"78","author":"Beyer","year":"2007","journal-title":"J. Neurol. Neurosurg. Psychiatry"},{"key":"B13","doi-asserted-by":"crossref","first-page":"2284","DOI":"10.1016\/S0140-6736(21)00218-X","article-title":"Parkinson\u2019s disease.","volume":"397","author":"Bloem","year":"2021","journal-title":"Lancet"},{"key":"B14","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1080\/13854049108403297","article-title":"The Hopkins verbal learning test: Development of a new memory test with six equivalent forms.","volume":"5","author":"Brandt","year":"1991","journal-title":"Clin. Neuropsychol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"695","DOI":"10.1017\/S1355617713000295","article-title":"Cognitive change in newly-diagnosed patients with Parkinson\u2019s disease: A 5-year follow-up study.","volume":"19","author":"Broeders","year":"2013","journal-title":"J. Int. Neuropsychol. Soc."},{"key":"B16","author":"Caminero","year":"2019","journal-title":"Neuroanatomy, mesencephalon midbrain."},{"key":"B17","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1016\/S1474-4422(06)70373-8","article-title":"Non-motor symptoms of Parkinson\u2019s disease: Diagnosis and management.","volume":"5","author":"Chaudhuri","year":"2006","journal-title":"Lancet Neurol."},{"key":"B18","first-page":"S782","article-title":"Classify Parkinson\u2019s disease with mild cognitive impairment: Machine learning approach.","volume":"34","author":"Cho","year":"2019","journal-title":"Mov. Disord."},{"key":"B19","doi-asserted-by":"publisher","DOI":"10.3389\/fnagi.2021.668559","article-title":"Posterior cortical cognitive deficits are associated with structural brain alterations in mild cognitive impairment in Parkinson\u2019s disease.","volume":"13","author":"Devignes","year":"2021","journal-title":"Front. Aging Neurosci."},{"key":"B20","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1111\/ane.12375","article-title":"Cognitive function in the early phase of Parkinson\u2019s disease, a five-year follow-up.","volume":"132","author":"Domell\u00f6f","year":"2015","journal-title":"Acta Neurol. Scand."},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.3389\/fneur.2017.00428","article-title":"Comparing CAT12 and VBM8 for detecting brain morphological abnormalities in temporal lobe epilepsy.","volume":"8","author":"Farokhian","year":"2017","journal-title":"Front. Neurol."},{"key":"B22","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1016\/j.neulet.2017.08.028","article-title":"Changes of brain structure in Parkinson\u2019s disease patients with mild cognitive impairment analyzed via VBM technology.","volume":"658","author":"Gao","year":"2017","journal-title":"Neurosci. Lett."},{"key":"B23","article-title":"CAT-a computational anatomy toolbox for the analysis of structural MRI data.","author":"Gaser","year":"2022","journal-title":"bioRxiv"},{"key":"B24","doi-asserted-by":"crossref","first-page":"2129","DOI":"10.1002\/mds.22340","article-title":"Movement disorder society-sponsored revision of the unified Parkinson\u2019s disease rating scale (MDS-UPDRS): Scale presentation and clinimetric testing results.","volume":"23","author":"Goetz","year":"2008","journal-title":"Mov. Disord."},{"key":"B25","doi-asserted-by":"publisher","first-page":"876","DOI":"10.1002\/mds.27665","article-title":"Modifiable risk factors for cognitive impairment in Parkinson\u2019s disease: A systematic review and meta-analysis of prospective cohort studies.","volume":"34","author":"Guo","year":"2019","journal-title":"Mov. Disord."},{"key":"B26","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1177\/0891988712447894","article-title":"Validity of a brief computerized cognitive screening test in dementia.","volume":"25","author":"Hammers","year":"2012","journal-title":"J. Geriatr. Psychiatry Neurol."},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.1038\/s41531-022-00409-5","article-title":"Machine learning-based prediction of cognitive outcomes in de novo Parkinson\u2019s disease.","volume":"8","author":"Harvey","year":"2022","journal-title":"NPJ Parkinsons Dis."},{"key":"B28","doi-asserted-by":"publisher","first-page":"837","DOI":"10.1002\/mds.21956","article-title":"The Sydney multicenter study of Parkinson\u2019s disease: The inevitability of dementia at 20 years.","volume":"23","author":"Hely","year":"2008","journal-title":"Mov. Disord."},{"key":"B29","doi-asserted-by":"publisher","DOI":"10.3389\/fpsyg.2019.01020","article-title":"Automatic scoring of semantic fluency.","volume":"10","author":"Kim","year":"2019","journal-title":"Front. Psychol."},{"key":"B30","doi-asserted-by":"crossref","first-page":"648","DOI":"10.1136\/jnnp-2016-315099","article-title":"Stability of mild cognitive impairment in newly diagnosed Parkinson\u2019s disease.","volume":"88","author":"Lawson","year":"2017","journal-title":"J. Neurol. Neurosurg. Psychiatry"},{"key":"B31","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0269787","article-title":"The structural changes of gray matter in Parkinson disease patients with mild cognitive impairments.","volume":"17","author":"Li","year":"2022","journal-title":"PLoS One"},{"key":"B32","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.neuroimage.2013.04.011","article-title":"Subregions of the human superior frontal gyrus and their connections.","volume":"78","author":"Li","year":"2013","journal-title":"Neuroimage"},{"key":"B33","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1080\/13803395.2011.643227","article-title":"Use of the CogState brief battery in the assessment of Alzheimer\u2019s disease related cognitive impairment in the Australian imaging, biomarkers and lifestyle (AIBL) study.","volume":"34","author":"Lim","year":"2012","journal-title":"J. Clin. Exp. Neuropsychol."},{"key":"B34","doi-asserted-by":"publisher","first-page":"576","DOI":"10.1136\/jnnp-2013-305805","article-title":"Cognitive deficits in mild Parkinson\u2019s disease are associated with distinct areas of grey matter atrophy.","volume":"85","author":"Mak","year":"2014","journal-title":"J. Neurol. Neurosurg. Psychiatry"},{"key":"B35","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1007\/978-3-030-57321-8_2","article-title":"The explanation game: Explaining machine learning models using shapley values","author":"Merrick","year":"2020","journal-title":"Proceedings of the machine learning and knowledge extraction: 4th IFIP TC 5, TC 12, WG 8.4, WG 8.9, WG 12.9 international cross-domain conference, CD-MAKE 2020, Dublin, Ireland, August 25\u201328, 2020"},{"key":"B36","doi-asserted-by":"publisher","first-page":"1021","DOI":"10.1007\/s11682-018-9922-0","article-title":"Brain degeneration in Parkinson\u2019s disease patients with cognitive decline: A coordinate-based meta-analysis.","volume":"13","author":"Mihaescu","year":"2019","journal-title":"Brain Imaging Behav."},{"key":"B37","doi-asserted-by":"publisher","first-page":"223","DOI":"10.1016\/j.neurobiolaging.2013.06.025","article-title":"Effect of mild cognitive impairment on the patterns of neural activity in early Parkinson\u2019s disease.","volume":"35","author":"Nagano-Saito","year":"2014","journal-title":"Neurobiol. Aging"},{"key":"B38","doi-asserted-by":"publisher","first-page":"580","DOI":"10.1001\/jamaneurol.2013.2110","article-title":"Prognosis of mild cognitive impairment in early Parkinson disease: The Norwegian ParkWest study.","volume":"70","author":"Pedersen","year":"2013","journal-title":"JAMA Neurol."},{"key":"B39","doi-asserted-by":"publisher","first-page":"767","DOI":"10.1212\/WNL.0000000000003634","article-title":"Natural course of mild cognitive impairment in Parkinson disease: A 5-year population-based study.","volume":"88","author":"Pedersen","year":"2017","journal-title":"Neurology"},{"key":"B40","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3233\/JAD-230633","article-title":"Analysis of costs for imaging-assisted pharmaceutical intervention in Alzheimer\u2019s disease with lecanemab: Snapshot of the first 3 years.","volume":"8","author":"Perron","year":"2023","journal-title":"J. Alzheimers Dis."},{"key":"B41","first-page":"1","article-title":"Parkinson disease.","volume":"3","author":"Poewe","year":"2017","journal-title":"Nat. Rev. Dis. Prim."},{"key":"B42","doi-asserted-by":"crossref","first-page":"708","DOI":"10.1038\/nrneurol.2014.205","article-title":"Neuroimaging in Parkinson disease: From research setting to clinical practice.","volume":"10","author":"Politis","year":"2014","journal-title":"Nat. Rev. Neurol."},{"key":"B43","doi-asserted-by":"publisher","first-page":"88","DOI":"10.1016\/j.jns.2018.08.014","article-title":"Repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex to alleviate depression and cognitive impairment associated with Parkinson\u2019s disease: A review and clinical implications.","volume":"393","author":"Randver","year":"2018","journal-title":"J. Neurol. Sci."},{"key":"B44","doi-asserted-by":"publisher","first-page":"386","DOI":"10.1055\/s-0033-1359312","article-title":"Neuroimaging biomarkers of neurodegenerative diseases and dementia.","volume":"33","author":"Risacher","year":"2013","journal-title":"Semin. Neurol."},{"key":"B45","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroimage.2019.116189","article-title":"Automated anatomical labelling atlas 3.","volume":"206","author":"Rolls","year":"2020","journal-title":"Neuroimage"},{"key":"B46","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1038\/nrn.2017.62","article-title":"Non-motor features of Parkinson disease.","volume":"18","author":"Schapira","year":"2017","journal-title":"Nat. Rev. Neurosci."},{"key":"B47","doi-asserted-by":"publisher","first-page":"104","DOI":"10.1016\/j.parkreldis.2021.12.004","article-title":"Machine learning trained with quantitative susceptibility mapping to detect mild cognitive impairment in Parkinson\u2019s disease.","volume":"94","author":"Shibata","year":"2022","journal-title":"Parkinson. Relat. Disord."},{"key":"B48","doi-asserted-by":"publisher","first-page":"390","DOI":"10.1148\/radiol.2021203383","article-title":"Cortical thickness from MRI to predict conversion from mild cognitive impairment to dementia in Parkinson disease: A machine learning\u2013based model.","volume":"300","author":"Shin","year":"2021","journal-title":"Radiology"},{"key":"B49","author":"Smith","year":"1973","journal-title":"Symbol digit modalities test."},{"key":"B50","article-title":"Predicting future cognitive impairment in de novo parkinson\u2019s disease using clinical data and structural MRI.","author":"Smith","year":"2021","journal-title":"medRxiv"},{"key":"B51","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1002\/mds.23477","article-title":"The pattern of cortical atrophy in patients with Parkinson\u2019s disease according to cognitive status.","volume":"26","author":"Song","year":"2011","journal-title":"Mov. Disord."},{"key":"B52","doi-asserted-by":"publisher","first-page":"3775","DOI":"10.21037\/apm-22-1396","article-title":"Predictive value of machine learning in diagnosing cognitive impairment in patients with Parkinson\u2019s disease: A systematic review and meta-analysis.","volume":"11","author":"Sun","year":"2022","journal-title":"Ann. Palliat. Med."},{"key":"B53","doi-asserted-by":"publisher","first-page":"318","DOI":"10.1111\/jnc.13691","article-title":"The clinical symptoms of Parkinson\u2019s disease.","volume":"139","author":"Sveinbjornsdottir","year":"2016","journal-title":"J. Neurochem."},{"key":"B54","doi-asserted-by":"publisher","first-page":"697","DOI":"10.1016\/S1474-4422(12)70152-7","article-title":"Cognitive impairment in patients with Parkinson\u2019s disease: Diagnosis, biomarkers, and treatment.","volume":"11","author":"Svenningsson","year":"2012","journal-title":"Lancet Neurol."},{"key":"B55","doi-asserted-by":"publisher","DOI":"10.1037\/1040-3590.12.3.253","article-title":"Updating to the WAIS\u2013III and WMS\u2013III: Considerations for research and clinical practice.","volume":"12","author":"Tulsky","year":"2000","journal-title":"Psychol. Assess."},{"key":"B56","doi-asserted-by":"publisher","first-page":"2958","DOI":"10.1093\/brain\/awp245","article-title":"The distinct cognitive syndromes of Parkinson\u2019s disease: 5 year follow-up of the CamPaIGN cohort.","volume":"132","author":"Williams-Gray","year":"2009","journal-title":"Brain"},{"key":"B57","doi-asserted-by":"publisher","first-page":"1258","DOI":"10.1136\/jnnp-2013-305277","article-title":"The CamPaIGN study of Parkinson\u2019s disease: 10-year outlook in an incident population-based cohort.","volume":"84","author":"Williams-Gray","year":"2013","journal-title":"J. Neurol. Neurosurg. Psychiatry"},{"key":"B58","doi-asserted-by":"crossref","first-page":"696","DOI":"10.1093\/brain\/aws360","article-title":"The cerebellum in Parkinson\u2019s disease.","volume":"136","author":"Wu","year":"2013","journal-title":"Brain"},{"key":"B59","doi-asserted-by":"publisher","first-page":"839","DOI":"10.1002\/mds.27335","article-title":"\u201cSelection of normative group affects rates of mild cognitive impairment in Parkinson\u2019s disease\u201d.","volume":"33","author":"Wyman","year":"2018","journal-title":"Mov. Disord."},{"key":"B60","doi-asserted-by":"publisher","first-page":"178","DOI":"10.1177\/0891988717701001","article-title":"Diagnostic accuracy and confidence in the clinical detection of cognitive impairment in early-stage Parkinson disease.","volume":"30","author":"Wyman-Chick","year":"2017","journal-title":"J. Geriatr. Psychiatry Neurol."},{"key":"B61","doi-asserted-by":"publisher","first-page":"973","DOI":"10.1111\/ene.12974","article-title":"Substantia nigra hyperechogenicity is related to decline in verbal memory in healthy elderly adults.","volume":"23","author":"Yilmaz","year":"2016","journal-title":"Eur. J. Neurol."},{"key":"B62","doi-asserted-by":"crossref","first-page":"7386","DOI":"10.1007\/s00330-020-07575-1","article-title":"Identifying Parkinson\u2019s disease with mild cognitive impairment by using combined MR imaging and electroencephalogram.","volume":"31","author":"Zhang","year":"2021","journal-title":"Eur. Radiol."},{"key":"B63","doi-asserted-by":"publisher","DOI":"10.1016\/j.jns.2020.117077","article-title":"An SBM-based machine learning model for identifying mild cognitive impairment in patients with Parkinson\u2019s disease.","volume":"418","author":"Zhang","year":"2020","journal-title":"J. Neurol. Sci."},{"key":"B64","doi-asserted-by":"crossref","DOI":"10.1038\/s41531-022-00347-2","article-title":"A review on pathology, mechanism, and therapy for cerebellum and tremor in Parkinson\u2019s disease.","volume":"8","author":"Zhong","year":"2022","journal-title":"NPJ Parkinsons Dis."},{"key":"B65","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1111\/cns.13188","article-title":"Progressive brain atrophy in Parkinson\u2019s disease patients who convert to mild cognitive impairment.","volume":"26","author":"Zhou","year":"2020","journal-title":"CNS Neurosci. Ther."},{"key":"B66","doi-asserted-by":"publisher","first-page":"2586","DOI":"10.1007\/s11682-022-00714-w","article-title":"Cortical atrophy is associated with cognitive impairment in Parkinson\u2019s disease: A combined analysis of cortical thickness and functional connectivity.","volume":"16","author":"Zhu","year":"2022","journal-title":"Brain Imaging Behav."}],"container-title":["Frontiers in Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnins.2024.1375395\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,4,18]],"date-time":"2024-04-18T04:20:29Z","timestamp":1713414029000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnins.2024.1375395\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,4,18]]},"references-count":66,"alternative-id":["10.3389\/fnins.2024.1375395"],"URL":"https:\/\/doi.org\/10.3389\/fnins.2024.1375395","relation":{},"ISSN":["1662-453X"],"issn-type":[{"value":"1662-453X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,4,18]]},"article-number":"1375395"}}