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      The structural changes of gray matter in Parkinson disease patients with mild cognitive impairments

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          Abstract

          Objectives

          Parkinson disease (PD) is associated with cognitive impairments. However, the underlying neural mechanism of cognitive impairments in PD is still not clear. This study aimed to investigate the anatomic alternations of gray matter in PD patients with mild cognitive impairment (MCI) and their associations with neurocognitive measurements.

          Methods

          T1-weighted magnetic resonance imaging (MRI) data were acquired from 23 PD patients with MCI, 23 PD patients without MCI, and 23 matched healthy controls. The MRI data were analyzed using voxel-based morphometry (VBM) and surfaced-based morphometry (SBM) methods to assess the structural changes in gray matter volume and cortical thickness respectively. Receiver operating characteristic (ROC) analysis was used to examine the diagnostic accuracies of the indexes of interest. The correlations between the structural metrics and neurocognitive assessments (e.g., Montreal cognitive assessment, MOCA; Mini-mental state examination, MMSE) were further examined.

          Results

          PD patients with MCI showed reduced gray matter volume (GMV) in the frontal cortex (e.g., right inferior frontal gyrus and middle frontal gyrus) and extended to insula as well as cerebellum compared with the healthy controls and PD patients without MIC. Thinner of cortical thickens in the temporal lobe (e.g., left middle temporal gyrus and right superior temporal gyrus) extending to parietal cortex (e.g., precuneus) were found in the PD patients with MCI relative to the healthy controls and PD patients without MCI.ROC analysis indicated that the area under the ROC curve (AUC) values in the frontal, temporal, and subcortical structures (e.g., insula and cerebellum) could differentiate the PD patients with MCI and without MCI and healthy controls. Furthermore, GMV of the right middle frontal gyrus and cortical thickness of the right superior temporal gyrus were correlated with neurocognitive dysfunctions (e.g., MOCA and MMSE) in PD patients with MCI.

          Conclusion

          This study provided further evidence that PD with MCI was associated with structural alternations of brain. Morphometric analysis focusing on the cortical and subcortical regions could be biomarkers of cognitive impairments in PD patients.

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          Most cited references76

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          The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment.

          Ziad S Nasreddine, Natalie Phillips, Valérie Bédirian … (2005)
          To develop a 10-minute cognitive screening tool (Montreal Cognitive Assessment, MoCA) to assist first-line physicians in detection of mild cognitive impairment (MCI), a clinical state that often progresses to dementia. Validation study. A community clinic and an academic center. Ninety-four patients meeting MCI clinical criteria supported by psychometric measures, 93 patients with mild Alzheimer's disease (AD) (Mini-Mental State Examination (MMSE) score > or =17), and 90 healthy elderly controls (NC). The MoCA and MMSE were administered to all participants, and sensitivity and specificity of both measures were assessed for detection of MCI and mild AD. Using a cutoff score 26, the MMSE had a sensitivity of 18% to detect MCI, whereas the MoCA detected 90% of MCI subjects. In the mild AD group, the MMSE had a sensitivity of 78%, whereas the MoCA detected 100%. Specificity was excellent for both MMSE and MoCA (100% and 87%, respectively). MCI as an entity is evolving and somewhat controversial. The MoCA is a brief cognitive screening tool with high sensitivity and specificity for detecting MCI as currently conceptualized in patients performing in the normal range on the MMSE.
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            "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician.

            M F Folstein, S Folstein, P R McHugh (1975)
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              MDS clinical diagnostic criteria for Parkinson's disease.

              Ronald Postuma, Daniela Berg, Matthew Stern … (2015)
              This document presents the Movement Disorder Society Clinical Diagnostic Criteria for Parkinson's disease (PD). The Movement Disorder Society PD Criteria are intended for use in clinical research but also may be used to guide clinical diagnosis. The benchmark for these criteria is expert clinical diagnosis; the criteria aim to systematize the diagnostic process, to make it reproducible across centers and applicable by clinicians with less expertise in PD diagnosis. Although motor abnormalities remain central, increasing recognition has been given to nonmotor manifestations; these are incorporated into both the current criteria and particularly into separate criteria for prodromal PD. Similar to previous criteria, the Movement Disorder Society PD Criteria retain motor parkinsonism as the core feature of the disease, defined as bradykinesia plus rest tremor or rigidity. Explicit instructions for defining these cardinal features are included. After documentation of parkinsonism, determination of PD as the cause of parkinsonism relies on three categories of diagnostic features: absolute exclusion criteria (which rule out PD), red flags (which must be counterbalanced by additional supportive criteria to allow diagnosis of PD), and supportive criteria (positive features that increase confidence of the PD diagnosis). Two levels of certainty are delineated: clinically established PD (maximizing specificity at the expense of reduced sensitivity) and probable PD (which balances sensitivity and specificity). The Movement Disorder Society criteria retain elements proven valuable in previous criteria and omit aspects that are no longer justified, thereby encapsulating diagnosis according to current knowledge. As understanding of PD expands, the Movement Disorder Society criteria will need continuous revision to accommodate these advances.
              Article 0 comments Cited 1627 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Lihua Li: Role: MethodologyRole: Writing – review & editing
                Bingjun Ji:
                ORCID: https://orcid.org/0000-0002-2430-9155
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Ting Zhao: Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Xuan Cui: Role: InvestigationRole: MethodologyRole: VisualizationRole: Writing – review & editing
                Jingtao Chen: Role: MethodologyRole: VisualizationRole: Writing – review & editing
                Zhenyu Wang: Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Emanuele Bartolini: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS One
                Journal ID (publisher-id): plos
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 20 July 2022
                Publication date Collection: 2022
                Volume: 17
                Issue: 7
                Electronic Location Identifier: e0269787
                Affiliations
                [1 ] School of Education, Xinyang College, Xinyang, China
                [2 ] Department of Radiology, Sunshine Union Hospital, Weifang, China
                [3 ] Department of Neurology, Sunshine Union Hospital, Weifang, China
                [4 ] Department of Medical Imaging, Weifang Medical University, Weifang, China
                IRCCS Foundation Stella Maris: IRCCS Fondazione Stella Maris, ITALY
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0002-2430-9155
                Article
                Publisher ID: PONE-D-21-21988
                DOI: 10.1371/journal.pone.0269787
                PMC ID: 9299333
                PubMed ID: 35857782
                SO-VID: c21451ac-54a0-4ac4-a9b5-686151a15346
                Copyright © © 2022 Li et al
                License:

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 6 July 2021
                Date accepted : 30 May 2022
                Page count
                Figures: 4, Tables: 3, Pages: 17
                Funding
                The authors received no specific funding for this work.
                Categories
                Subject: Research Article
                Subject: Medicine and Health Sciences
                Subject: Medical Conditions
                Subject: Neurodegenerative Diseases
                Subject: Movement Disorders
                Subject: Parkinson Disease
                Subject: Medicine and Health Sciences
                Subject: Neurology
                Subject: Neurodegenerative Diseases
                Subject: Movement Disorders
                Subject: Parkinson Disease
                Subject: Biology and Life Sciences
                Subject: Neuroscience
                Subject: Cognitive Science
                Subject: Cognitive Neuroscience
                Subject: Cognitive Neurology
                Subject: Cognitive Impairment
                Subject: Biology and Life Sciences
                Subject: Neuroscience
                Subject: Cognitive Neuroscience
                Subject: Cognitive Neurology
                Subject: Cognitive Impairment
                Subject: Medicine and Health Sciences
                Subject: Neurology
                Subject: Cognitive Neurology
                Subject: Cognitive Impairment
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Nervous System
                Subject: Central Nervous System
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Nervous System
                Subject: Central Nervous System
                Subject: Biology and Life Sciences
                Subject: Neuroscience
                Subject: Brain Mapping
                Subject: Brain Morphometry
                Subject: Voxel-Based Morphometry
                Subject: Medicine and Health Sciences
                Subject: Diagnostic Medicine
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Subject: Brain Morphometry
                Subject: Voxel-Based Morphometry
                Subject: Research and Analysis Methods
                Subject: Imaging Techniques
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Subject: Brain Morphometry
                Subject: Voxel-Based Morphometry
                Subject: Medicine and Health Sciences
                Subject: Radiology and Imaging
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Subject: Brain Morphometry
                Subject: Voxel-Based Morphometry
                Subject: Research and Analysis Methods
                Subject: Imaging Techniques
                Subject: Neuroimaging
                Subject: Brain Morphometry
                Subject: Voxel-Based Morphometry
                Subject: Biology and Life Sciences
                Subject: Neuroscience
                Subject: Neuroimaging
                Subject: Brain Morphometry
                Subject: Voxel-Based Morphometry
                Subject: Research and Analysis Methods
                Subject: Imaging Techniques
                Subject: Morphometry
                Subject: Voxel-Based Morphometry
                Subject: Biology and Life Sciences
                Subject: Neuroscience
                Subject: Brain Mapping
                Subject: Brain Morphometry
                Subject: Surface-Based Morphometry
                Subject: Medicine and Health Sciences
                Subject: Diagnostic Medicine
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Subject: Brain Morphometry
                Subject: Surface-Based Morphometry
                Subject: Research and Analysis Methods
                Subject: Imaging Techniques
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Subject: Brain Morphometry
                Subject: Surface-Based Morphometry
                Subject: Medicine and Health Sciences
                Subject: Radiology and Imaging
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Subject: Brain Morphometry
                Subject: Surface-Based Morphometry
                Subject: Research and Analysis Methods
                Subject: Imaging Techniques
                Subject: Neuroimaging
                Subject: Brain Morphometry
                Subject: Surface-Based Morphometry
                Subject: Biology and Life Sciences
                Subject: Neuroscience
                Subject: Neuroimaging
                Subject: Brain Morphometry
                Subject: Surface-Based Morphometry
                Subject: Research and Analysis Methods
                Subject: Imaging Techniques
                Subject: Morphometry
                Subject: Surface-Based Morphometry
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Brain
                Subject: Cerebral Cortex
                Subject: Cerebellum
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Brain
                Subject: Cerebral Cortex
                Subject: Cerebellum
                Subject: Medicine and Health Sciences
                Subject: Clinical Medicine
                Subject: Signs and Symptoms
                Subject: Atrophy
                Subject: Medicine and Health Sciences
                Subject: Diagnostic Medicine
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Subject: Research and Analysis Methods
                Subject: Imaging Techniques
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Subject: Medicine and Health Sciences
                Subject: Radiology and Imaging
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Custom metadata
                Data Availability All relevant data are within the paper and its Supporting Information files.

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