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. 2024 Jun 13;47(6):zsae007.
doi: 10.1093/sleep/zsae007.

Comorbid neurotrauma increases neurodegenerative-relevant cognitive, motor, and autonomic dysfunction in patients with rapid eye movement sleep behavior disorder: a substudy of the North American Prodromal Synucleinopathy Consortium

Jonathan E Elliott  1   2 , Brittany R Ligman  1 , Mohini D Bryant-Ekstrand  1 , Allison T Keil  1   3 , Katherine Powers  1 , Cosette Olivo  1 , Lee E Neilson  1   2 , Ronald B Postuma  3   4   5   6 , Amélie Pelletier  5   6 , Jean-François Gagnon  4   5 , Ziv Gan-Or  3   7 , Eric Yu  3   7 , Lang Liu  3   7 , Erik K St Louis  8 , Leah K Forsberg  8 , Julie A Fields  8 , Owen A Ross  8 , Daniel E Huddleston  9 , Donald L Bliwise  9 , Alon Y Avidan  10 , Michael J Howell  11   12 , Carlos H Schenck  11 , Jennifer McLeland  13 , Susan R Criswell  14 , Aleksandar Videnovic  15   16 , Emmanuel H During  17   18   19 , Mitchell G Miglis  17   18 , David R Shprecher  20 , Joyce K Lee-Iannotti  21 , Bradley F Boeve  8   22 , Yo-El S Ju  13   22 , Miranda M Lim  2   23   24 ; North American Prodromal Synucleinopathy (NAPS) Consortium
Collaborators, Affiliations

Comorbid neurotrauma increases neurodegenerative-relevant cognitive, motor, and autonomic dysfunction in patients with rapid eye movement sleep behavior disorder: a substudy of the North American Prodromal Synucleinopathy Consortium

Jonathan E Elliott et al. Sleep. .

Abstract

Study objectives: Rapid eye movement sleep behavior disorder (RBD) is strongly associated with phenoconversion to an overt synucleinopathy, e.g. Parkinson's disease (PD), Lewy body dementia, and related disorders. Comorbid traumatic brain injury (TBI) and posttraumatic stress disorder (PTSD)-henceforth "neurotrauma" (NT)-increase the odds of RBD by ~2.5-fold and are associated with an increased rate of service-connected PD in Veterans. Thus, RBD and NT are both independently associated with PD; however, it is unclear how NT influences neurological function in patients with RBD.

Methods: Participants ≥18 years with overnight polysomnogram-confirmed RBD were enrolled between 8/2018 to 4/2021 through the North American Prodromal Synucleinopathy Consortium. Standardized assessments for RBD, TBI, and PTSD history, as well as cognitive, motor, sensory, and autonomic function, were completed. This cross-sectional analysis compared cases (n = 24; RBD + NT) to controls (n = 96; RBD), matched for age (~60 years), sex (15% female), and years of education (~15 years).

Results: RBD + NT reported earlier RBD symptom onset (37.5 ± 11.9 vs. 52.2 ± 15.1 years of age) and a more severe RBD phenotype. Similarly, RBD + NT reported more severe anxiety and depression, greater frequency of hypertension, and significantly worse cognitive, motor, and autonomic function compared to RBD. No differences in olfaction or color vision were observed.

Conclusions: This cross-sectional, matched case:control study shows individuals with RBD + NT have significantly worse neurological measures related to common features of an overt synucleinopathy. Confirmatory longitudinal studies are ongoing; however, these results suggest RBD + NT may be associated with more advanced neurological symptoms related to an evolving neurodegenerative process.

Keywords: Parkinson’s disease; RBD; REM sleep without atonia; posttraumatic stress disorder; synucleinopathy; trauma-associated sleep disorder; traumatic brain injury.

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Figures

Graphical Abstract
Graphical Abstract
Figure 1.
Figure 1.
Data for the RBD + NT and the RBD groups from (A) The Montreal Cognitive Assessment (MoCA), (B) Craft Story Verbatim, (C) The Movement Disorder Society-Sponsored Revision of the Unified Parkinson’s Disease Rating Scale 3 (MDS-UPDRS III), (D) The Alternative Tap Test (Alt Tap), (E) The Brief Smell Identification Test (BSIT), (F) The Farnsworth-Munsell 100-Hue test (FM-100), (G) change in systolic blood pressure between supine to after 3 minutes of standing (ΔSBP), and (H) The Scale for Outcomes in Parkinson’s disease-Autonomic Test (SCOPA-AUT). Data are mean ± standard deviation with the percent abnormal listed above/below the dashed line appropriate to the directionality for each outcome. Comparisons were unpaired with two-tailed t-tests.
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