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May 12, 2022Research Article

Evolution of Prodromal REM Sleep Behavior Disorder to Neurodegeneration: A Retrospective, Longitudinal Case-control Study

View ORCID ProfileYaping Liu, Jihui Zhang, Steven WH Chau, Mandy Wai Man Yu, Ngan Yin Chan, Joey WY Chan, Shirley Xin Li, Bei Huang, View ORCID ProfileJing Wang, Hongliang FENG, Li Zhou, Vincent Mok, View ORCID ProfileYun kwok Wing
First published May 12, 2022, DOI: https://doi.org/10.1212/WNL.0000000000200707
Yaping Liu
1Li Chiu Kong Family Sleep Assessment Unit, Department of Psychiatry, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, N.T., Hong Kong SAR, China
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  • ORCID record for Yaping Liu
Jihui Zhang
1Li Chiu Kong Family Sleep Assessment Unit, Department of Psychiatry, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, N.T., Hong Kong SAR, China
2Guangdong Mental Health Center, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, Guangzhou, Guangdong, China
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Steven WH Chau
1Li Chiu Kong Family Sleep Assessment Unit, Department of Psychiatry, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, N.T., Hong Kong SAR, China
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Mandy Wai Man Yu
1Li Chiu Kong Family Sleep Assessment Unit, Department of Psychiatry, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, N.T., Hong Kong SAR, China
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Ngan Yin Chan
1Li Chiu Kong Family Sleep Assessment Unit, Department of Psychiatry, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, N.T., Hong Kong SAR, China
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Joey WY Chan
1Li Chiu Kong Family Sleep Assessment Unit, Department of Psychiatry, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, N.T., Hong Kong SAR, China
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Shirley Xin Li
3Department of Psychology, The University of Hong Kong, Pokfulam, Hong Kong SAR, China; The State Key Laboratory of Brain and Cognitive Sciences, The University of Hong Kong, Pokfulam, Hong Kong SAR, China
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Bei Huang
1Li Chiu Kong Family Sleep Assessment Unit, Department of Psychiatry, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, N.T., Hong Kong SAR, China
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Jing Wang
1Li Chiu Kong Family Sleep Assessment Unit, Department of Psychiatry, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, N.T., Hong Kong SAR, China
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  • ORCID record for Jing Wang
Hongliang FENG
1Li Chiu Kong Family Sleep Assessment Unit, Department of Psychiatry, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, N.T., Hong Kong SAR, China
2Guangdong Mental Health Center, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, Guangzhou, Guangdong, China
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Li Zhou
1Li Chiu Kong Family Sleep Assessment Unit, Department of Psychiatry, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, N.T., Hong Kong SAR, China
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Vincent Mok
4Margaret K.L. Cheung Research Centre for Management of Parkinsonism, Gerald Choa Neuroscience Centre, Lui Che Wo Institute of Innovative Medicine, Department of Medicine and Therapeutics, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, Hong Kong SAR, China
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Yun kwok Wing
1Li Chiu Kong Family Sleep Assessment Unit, Department of Psychiatry, Faculty of Medicine, The Chinese University of Hong Kong, Shatin, N.T., Hong Kong SAR, China
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  • ORCID record for Yun kwok Wing
  • For correspondence: ykwing@cuhk.edu.hk
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Citation
Evolution of Prodromal REM Sleep Behavior Disorder to Neurodegeneration: A Retrospective, Longitudinal Case-control Study
Yaping Liu, Jihui Zhang, Steven WH Chau, Mandy Wai Man Yu, Ngan Yin Chan, Joey WY Chan, Shirley Xin Li, Bei Huang, Jing Wang, Hongliang FENG, Li Zhou, Vincent Mok, Yun kwok Wing
Neurology May 2022, 10.1212/WNL.0000000000200707; DOI: 10.1212/WNL.0000000000200707

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Abstract

Background and Objectives: Individuals with a history of recurrent dream-enactment behaviors, but with subthreshold REM sleep without atonia levels for REM sleep behavior disorder (RBD) diagnosis, are currently classified to have prodromal RBD (pRBD). However, the REM sleep elevated EMG diagnostic cut-off, progression trajectory, and long-term neurodegenerative outcome of pRBD are not well understood. This study aimed to delineate the evolution of REM sleep EMG levels, determine the EMG cut-off score for diagnosing pRBD, and examine the risk for neurodegenerative diseases of pRBD.

Methods: This retrospective longitudinal case-control study recruited pRBD patients and age, sex, and follow-up duration matched controls who were free of neurodegenerative disease at baseline in the Sleep Assessment Unit, the Chinese University of Hong Kong from 1997 to 2018. Patients and controls underwent clinical and video-polysomnography assessments at baseline and follow-up(s). REM sleep EMG activity level on mentalis and anterior tibialis (AT) muscles on video-polysomnography at each visit was scored. The diagnosis of neurodegenerative diseases was confirmed by a neurologist.

Results: 44 patients (67.4 ± 8.2 years old, 6 females) and 44 controls were recruited. The combined REM sleep EMG level on mentalis and AT muscles of pRBD patients significantly increased during 8.2 ± 3.3 years of follow-up (from 19.3 ± 9.7% to 47.3 ± 27.4% with estimated annual increase of 3.9%), yielding 29 pRBD patients (66%) meeting the full-blown RBD diagnostic criteria. Baseline REM sleep mentalis and AT muscles EMG activity of patients who developed full-blown RBD could favourably differentiate pRBD from controls (6.3% for mentalis ‘any’ and 9.1% for combination of mentalis ‘any’ and bilateral AT muscles phasic EMG with AUC of 0.88 [0.78-0.98] and 0.97 [0.92-1.00] respectively). pRBD patients had a higher risk for neurodegenerative diseases (9 developed Parkinson’s disease and 3 developed dementia with Lewy bodies) when compared to controls (5 developed Alzheimer’s disease, adjusted hazard ratio = 2.95, 95% CI = 1.02-8.54).

Conclusions: pRBD has a predictive progression in both pathophysiology and neurodegenerative outcome. This finding has significant implications to the nosological status of pRBD, the current REM sleep-related EMG diagnostic criteria, spectrum concept of RBD and future neuroprotective intervention.

Classification of Evidence: This study provides Class III evidence that EMG activity during REM sleep predicts the development of prodromal REM sleep behavior disorder.

  • Received August 5, 2021.
  • Accepted in final form March 24, 2022.
  • © 2022 American Academy of Neurology

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