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      Brain olfactory‐related atrophy in isolated rapid eye movement sleep behavior disorder

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          Abstract

          Objective

          To investigate structural and functional connectivity changes in brain olfactory‐related structures in a longitudinal prospective cohort of isolated REM sleep behavior disorder (iRBD) and their clinical correlations, longitudinal evolution, and predictive values for phenoconversion to overt synucleinopathies, especially Lewy body diseases.

          Methods

          The cohort included polysomnography‐confirmed iRBD patients and controls. Participants underwent baseline assessments including olfactory tests, neuropsychological evaluations, the Movement Disorders Society–Unified Parkinson's Disease Rating Scale, 3T brain MRI, and 18F‐FP‐CIT PET scans. Voxel‐based morphometry (VBM) was performed to identify regions of atrophy in iRBD, and volumes of relevant olfactory‐related regions of interest (ROI) were estimated. Subgroups of patients underwent repeated volumetric MRI and resting‐state functional MRI (fMRI) scans after four years.

          Results

          A total of 51 iRBD patients were included, with 20 of them converting to synucleinopathy (mean time to conversion 3.08 years). Baseline VBM analysis revealed atrophy in the right olfactory cortex and gyrus rectus in iRBD. Subsequent ROI comparisons with controls showed atrophy in the amygdala. These olfactory‐related atrophies tended to be associated with worse depression, anxiety, and urinary problems in iRBD. Amygdala 18F‐FP‐CIT uptake tended to be reduced in iRBD patients with hyposmia (nonsignificant after multiple comparison correction) and correlated with urinary problems. Resting‐state fMRI of 23 patients and 32 controls revealed multiple clusters with aberrant olfactory‐related functional connectivity. Hypoconnectivity between the putamen and olfactory cortex was associated with mild parkinsonian signs in iRBD. Longitudinal analysis of volumetric volumetric MRI in 22 iRBD patients demonstrated four‐year progression of olfactory‐related atrophy. Cox regression analysis revealed that this atrophy significantly predicted phenoconversion.

          Interpretation

          Progressive atrophy of central olfactory structures may be a potential indicator of Lewy body disease progression in iRBD.

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          Most cited references49

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

          Yoav Benjamini, Yosef Hochberg (1995)
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            Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain.

            N. Tzourio-Mazoyer, B Landeau, D Papathanassiou … (2003)
            An anatomical parcellation of the spatially normalized single-subject high-resolution T1 volume provided by the Montreal Neurological Institute (MNI) (D. L. Collins et al., 1998, Trans. Med. Imag. 17, 463-468) was performed. The MNI single-subject main sulci were first delineated and further used as landmarks for the 3D definition of 45 anatomical volumes of interest (AVOI) in each hemisphere. This procedure was performed using a dedicated software which allowed a 3D following of the sulci course on the edited brain. Regions of interest were then drawn manually with the same software every 2 mm on the axial slices of the high-resolution MNI single subject. The 90 AVOI were reconstructed and assigned a label. Using this parcellation method, three procedures to perform the automated anatomical labeling of functional studies are proposed: (1) labeling of an extremum defined by a set of coordinates, (2) percentage of voxels belonging to each of the AVOI intersected by a sphere centered by a set of coordinates, and (3) percentage of voxels belonging to each of the AVOI intersected by an activated cluster. An interface with the Statistical Parametric Mapping package (SPM, J. Ashburner and K. J. Friston, 1999, Hum. Brain Mapp. 7, 254-266) is provided as a freeware to researchers of the neuroimaging community. We believe that this tool is an improvement for the macroscopical labeling of activated area compared to labeling assessed using the Talairach atlas brain in which deformations are well known. However, this tool does not alleviate the need for more sophisticated labeling strategies based on anatomical or cytoarchitectonic probabilistic maps.
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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 2091 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Kyung Ah Woo:
                ORCID: https://orcid.org/0000-0001-5457-7348
                neurowoo@gmail.com
                Hyunwoo Nam:
                ORCID: https://orcid.org/0000-0003-3345-7069
                hwnam85@gmail.com
                Yu Kyeong Kim:
                ORCID: https://orcid.org/0000-0002-3282-822X
                yk3181@snu.ac.kr
                Jee‐Young Lee:
                ORCID: https://orcid.org/0000-0002-9120-2075
                wieber04@snu.ac.kr
                Journal
                Journal ID (nlm-ta): Ann Clin Transl Neurol
                Journal ID (iso-abbrev): Ann Clin Transl Neurol
                Journal ID (doi): 10.1002/(ISSN)2328-9503
                Journal ID (publisher-id): ACN3
                Title: Annals of Clinical and Translational Neurology
                Publisher: John Wiley and Sons Inc. (Hoboken )
                ISSN (Electronic): 2328-9503
                Publication date (Electronic): 25 September 2023
                Publication date Collection: December 2023
                Volume: 10
                Issue: 12 ( doiID: 10.1002/acn3.v10.12 )
                Pages: 2192-2207
                Affiliations
                [ 1 ] Department of Neurology Seoul Metropolitan Government–Seoul National University Boramae Medical Center, Seoul National University College of Medicine Seoul Republic of Korea
                [ 2 ] Department of Nuclear Medicine Seoul Metropolitan Government–Seoul National University Boramae Medical Center, Seoul National University College of Medicine Seoul Republic of Korea
                [ 3 ] Institute of Radiation Medicine, Medical Research Center Seoul National University Seoul Republic of Korea
                [ 4 ] Memory Network Medical Research Center Seoul National University Seoul Republic of Korea
                [ 5 ] Department of Neurology Seoul National University Hospital, Seoul National University College of Medicine Seoul Republic of Korea
                Author notes
                [*] [* ] Correspondence

                Yu Kyeong Kim, Department of Nuclear Medicine, Seoul Metropolitan Government‐Seoul National University Boramae Medical Center, Seoul National University College of Medicine, Seoul, Republic of Korea. Tel: 82‐2‐870‐2581; Fax: 82‐2‐870‐3863; E‐mail: yk3181@ 123456snu.ac.kr

                Jee‐Young Lee, Department of Neurology, Seoul Metropolitan Government‐Seoul National University Boramae Medical Center, Seoul National University College of Medicine, Seoul, Republic of Korea. Tel: 82‐2‐870‐2476; Fax: 82‐2‐831‐2826; E‐mail: wieber04@ 123456snu.ac.kr

                *These authors contributed equally to this work.

                Author information
                https://orcid.org/0000-0001-5457-7348
                https://orcid.org/0000-0003-4182-3612
                https://orcid.org/0000-0003-3345-7069
                https://orcid.org/0000-0003-2491-3544
                https://orcid.org/0000-0002-3282-822X
                https://orcid.org/0000-0002-9120-2075
                Article
                Publisher ID: ACN351905 Other ID: ACN3-2023-04-0264.R2
                DOI: 10.1002/acn3.51905
                PMC ID: 10723229
                PubMed ID: 37743764
                SO-VID: 4f396a3c-350f-40ce-bcb1-fad8b7797d42
                Copyright © © 2023 The Authors. Annals of Clinical and Translational Neurology published by Wiley Periodicals LLC on behalf of American Neurological Association.
                License:

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.

                History
                Date revision received : 10 August 2023
                Date received : 14 April 2023
                Date accepted : 09 September 2023
                Page count
                Figures: 5, Tables: 2, Pages: 2207, Words: 9415
                Funding
                Funded by: Ministry of Education, Science and Technology , doi 10.13039/501100004085;
                Award ID: NRF‐2018R1A5A2025964
                Award ID: NRF‐2018R1C1B3008971
                Award ID: NRF‐2020R1I1A1A01054095
                Funded by: Ministry of Science and ICT, South Korea , doi 10.13039/501100014188;
                Award ID: 2022R1A2C4001834
                This work was funded by Ministry of Education, Science and Technology , doi 10.13039/501100004085; grants NRF‐2018R1A5A2025964, NRF‐2018R1C1B3008971, and NRF‐2020R1I1A1A01054095; Ministry of Science and ICT, South Korea , doi 10.13039/501100014188; grant 2022R1A2C4001834.
                Categories
                Subject: Research Article
                Subject: Research Articles
                Custom metadata
                source-schema-version-number 2.0
                cover-date December 2023
                details-of-publishers-convertor Converter:WILEY_ML3GV2_TO_JATSPMC version:6.3.6 mode:remove_FC converted:15.12.2023

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