REM sleep without atonia in middle-aged and older psychiatric patients and Lewy body disease: a case series
Corresponding Author
Hiroshige Fujishiro
Department of Sleep Medicine, Nagoya University Graduate School of Medicine, Nagoya, Japan
Department of Psychiatry, Nagoya University Graduate School of Medicine, Nagoya, Japan
Correspondence to: H. Fujishiro, MD, PhD, E-mail: [email protected]Search for more papers by this authorMasato Okuda
Department of Sleep Medicine, Nagoya University Graduate School of Medicine, Nagoya, Japan
Search for more papers by this authorKunihiro Iwamoto
Department of Psychiatry, Nagoya University Graduate School of Medicine, Nagoya, Japan
Search for more papers by this authorSeiko Miyata
Department of Sleep Medicine, Nagoya University Graduate School of Medicine, Nagoya, Japan
Search for more papers by this authorHironao Otake
Department of Sleep Medicine, Nagoya University Graduate School of Medicine, Nagoya, Japan
Search for more papers by this authorAkiko Noda
Department of Biomedical Science, Chubu University Graduate School of Life and Health Sciences, Kasugai, Japan
Search for more papers by this authorShuji Iritani
Department of Psychiatry, Nagoya University Graduate School of Medicine, Nagoya, Japan
Search for more papers by this authorNorio Ozaki
Department of Psychiatry, Nagoya University Graduate School of Medicine, Nagoya, Japan
Search for more papers by this authorCorresponding Author
Hiroshige Fujishiro
Department of Sleep Medicine, Nagoya University Graduate School of Medicine, Nagoya, Japan
Department of Psychiatry, Nagoya University Graduate School of Medicine, Nagoya, Japan
Correspondence to: H. Fujishiro, MD, PhD, E-mail: [email protected]Search for more papers by this authorMasato Okuda
Department of Sleep Medicine, Nagoya University Graduate School of Medicine, Nagoya, Japan
Search for more papers by this authorKunihiro Iwamoto
Department of Psychiatry, Nagoya University Graduate School of Medicine, Nagoya, Japan
Search for more papers by this authorSeiko Miyata
Department of Sleep Medicine, Nagoya University Graduate School of Medicine, Nagoya, Japan
Search for more papers by this authorHironao Otake
Department of Sleep Medicine, Nagoya University Graduate School of Medicine, Nagoya, Japan
Search for more papers by this authorAkiko Noda
Department of Biomedical Science, Chubu University Graduate School of Life and Health Sciences, Kasugai, Japan
Search for more papers by this authorShuji Iritani
Department of Psychiatry, Nagoya University Graduate School of Medicine, Nagoya, Japan
Search for more papers by this authorNorio Ozaki
Department of Psychiatry, Nagoya University Graduate School of Medicine, Nagoya, Japan
Search for more papers by this authorAbstract
Objective
Rapid eye movement (REM) sleep behavior disorder (RBD) is commonly associated with Lewy body disease, narcolepsy, or depression. In contrast, the relationship between REM sleep without atonia (RWA), which is a hallmark of RBD on polysomnography, and clinical characteristics remains unclear. The purpose of this study is to investigate the clinical features of psychiatric patients exhibiting RWA and its relevance to Lewy body disease.
Methods
Of 55 consecutive patients who underwent polysomnography at the psychiatric ward, 25 patients with sleep apnea syndrome were excluded, and 12 patients exhibiting RWA were identified. The clinical profiles were compared between the groups with and without RWA.
Results
The mean age and the frequency of neurocognitive disorders were significantly higher in 12 patients with RWA than in 18 without. Only five of the 12 patients exhibiting RWA had episodes of dream-enactment behavior, and fulfilled the clinical criteria for RBD. Two young patients were diagnosed with narcolepsy, while the other middle-aged and older patients fulfilled the clinical criteria for Parkinson's disease (n = 1), dementia with Lewy bodies (n = 4), idiopathic RBD (n = 2), and major depressive disorder (MDD) (n = 3). The patients with MDD exhibited constipation and/or olfactory dysfunction. Moreover, neuroimaging examinations in the patients with MDD revealed isolated occipital hypoperfusion in three patients and mild dopamine transporter deficit in one patient.
Conclusions
Rapid eye movement sleep without atonia itself may be associated with specific clinical profiles, even when dream-enactment behavior is absent. Continued follow-up of the patients with MDD exhibiting RWA is warranted to determine if they represent the prodromal Parkinson's disease/dementia with Lewy bodies. Copyright © 2016 John Wiley & Sons, Ltd.
References
- Alonso A, Rodriguez LA, Logroscino G, Hernan MA. 2009. Use of antidepressants and the risk of Parkinson's disease: a prospective study. J Neurol Neurosurg Psychiatry 80: 671–674. DOI:10.1136/jnnp.2008.152983.
-
American Psychiatric Association. 2013. Diagnostic and Statistical Manual Disorders. 5th edn.American Psychiatric Publishing: Arlington.
10.1176/appi.books.9780890425596 Google Scholar
- American Academy of Sleep Medicine. 2005. International Classification of Sleep Disorders: Diagnostic and Coding Manual. 2nd edn. American Academy of Sleep Medicine: Westchester, IL; 148–152.
- American Academy of Sleep Medicine. 2007. Manual for the Scoring of Sleep and Associated Events: Rules, Technology, and Technical Specifications. 1st edn. American Academy of Sleep Medicine: Westchester, IL; 42–43.
- Boeve BF. 2010. REM sleep behavior disorder: updated review of the core features, the RBD-neurodegenerative disease association, evolving concepts, controversies, and future directions. Ann N Y Acad Sci 1184: 15–54. DOI:10.1111/j.1749-6632.2009.05115.x.
- Boeve BF, Silber MH, Ferman TJ, et al. 2013. Clinicopathologic correlations in 172 cases of rapid eye movement sleep behavior disorder with or without a coexisting neurologic disorder. Sleep Med 14: 754–762. DOI:10.1016/j.sleep.2012.10.015.
- Boot BP, Boeve BF, Roberts RO, et al. 2012. Probable rapid eye movement sleep behavior disorder increases risk for mild cognitive impairment and Parkinson disease: a population-based study. Ann Neurol 71: 49–56. DOI:10.1002/ana.22655.
- Chiba Y, Fujishiro H, Iseki E, et al. 2012. Retrospective survey of prodromal symptoms in dementia with Lewy bodies: comparison with Alzheimer's disease. Dement Geriatr Cogn Disord 33: 273–281. DOI:10.1159/000339363.
- Eisensehr I, Linke R, Tatsch K, et al. 2003. Increased muscle activity during rapid eye movement sleep correlates with decrease of striatal presynaptic dopamine transporters. IPT and IBZM SPECT imaging in subclinical and clinically manifest idiopathic REM sleep behavior disorder, Parkinson's disease, and controls. Sleep 26: 507–512.
- Fahn S, Elton RL. 1987. UPDRS development committee. The unified Parkinson's disease rating scale. In Recent Developments in Parkinson's Disease, S Fahn, CD Marsden, DB Calne, M Goldstein (eds.). Macmillan Healthcare Information: Florham Park, NJ; 153–63.
- Fujishiro H, Iseki E, Kasanuki K, et al. 2012. Glucose hypometabolism in primary visual cortex is commonly associated with clinical features of dementia with Lewy bodies regardless of cognitive conditions. Int J Geriatr Psychiatry 27: 1138–1146. DOI:10.1002/gps.2836.
- Fujishiro H, Iseki E, Nakamura S, et al. 2013a. Dementia with Lewy bodies: early diagnostic challenges. Psychogeriatrics 13: 128–138. doi: 10.1111/psyg.12005.
- Fujishiro H, Iseki E, Kasanuki K, et al. 2013b. A follow up study of non-demented patients with primary visual cortical hypometabolism: prodromal dementia with Lewy bodies. J Neurol Sci 334: 48–54. DOI:10.1016/j.jns.2013.07.013.
- Fujishiro H, Nakamura S, Sato K, Iseki E. 2015. Prodromal dementia with Lewy bodies. Geriatr Gerontol Int 15: 817–826. DOI:10.1111/ggi.12466.
- Frauscher B, Iranzo A, Gaig C, et al. 2012. Normative EMG values during REM sleep for the diagnosis of REM sleep behavior disorder. Sleep 35: 835–847. DOI:10.5665/sleep.1886.
- Frauscher B, Ehrmann L, Högl B. 2013. Defining muscle activities for assessment of rapid eye movement sleep behavior disorder: form a qualitative to a quantitative diagnostic level. Sleep Med 14: 729–733. DOI:10.1016/j.sleep.2012.09.028.
- Frauscher B, Jennum P, Ju YE, et al. 2014. Comorbidity and medication in REM sleep behavior disorder: a multicenter case–control study. Neurology 82: 1076–1079. DOI:10.1212/WNL.0000000000000247.
- Gagnon JF, Postuma RB, Mazza S, Doyon J, Montplaisir J. 2006. Rapid-eye-movement sleep behavior and neurodegenerative diseases. Lancet Neurol 5: 424–432.
- Halliday GM, Holton JL, Revesz T, Dickson DW. 2010. Neuropathology underlying clinical variability in patients with synucleinopathies. Acta Neuropathol 122: 187–204. DOI:10.1007/s00401-011-0852-9.
- Hyman BT, Phelps CH, Beach TG, et al. 2012. National Institute on Aging-Alzheimer's Association guidelines for the neuropathologic assessment of Alzheimer's disease 8: 1–13. DOI:10.1016/j.jalz.2011.10.007.
- Hughes AJ, Daniel SE, Kilford L, Lees AJ. 1992. Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinicopathological study of 100 cases. J Neurol Neurosurg Psychiatry 55: 181–184.
- Iranzo A, Tolosa E, Gelpi E, et al. 2013. Neurodegenerative disease status and post-mortem pathology in idiopathic rapid-eye-movement sleep behaviour disorder: an observational cohort study. Lancet Neurol 12: 443–453. DOI:10.1016/S1474-4422(13)70056-5.
- Ju YE, Larson-Prior L, Duntley S. 2011. Changing demographics in REM sleep behavior disorder: possible effect of autoimmunity and antidepressants. Sleep Med 12: 278–283. DOI:10.1016/j.sleep.2010.07.022.
- Lam SP, Zhang J, Tsoh J, et al. 2010. REM sleep behavior disorder in psychiatric populations. J Clin Psychiatry 71: 1101–1103. DOI:10.4088/JCP.l05877gry.
- Leentjens AF, Van der Akker M, Metsemakers JF, Lousberg R, Verhey FR. 2003. Higher incidence of depression preceding the onset of Parkinson's disease: a register study. Mov Disord 18: 414–418.
- Matsuda H, Mizumura S, Soma T, Takemura N. 2004. Conversion of brain SPECT images between different collimators and reconstruction processes for analysis using statistical parametric mapping. Nucl Med Commun 25: 67–74.
- Matsuda H, Mizumura S, Nagao T, et al. 2007a. An easy Z-score imaging system for discrimination between very early Alzheimer disease and controls using brain perfusion SPECT in a multicentre study. Nucl Med Commun 28: 199–205.
- Matsuda H, Mizumura S, Nagao T, et al. 2007b. Automated discrimination between very early Alzheimer disease and controls using an easy Z-score imaging system for multicenter brain perfusion single-photon emission tomography. AJNR Am Neuroradiol 28: 731–736.
- McCarter SJ, St Louis EK, Sandness DJ, et al. 2015. Antidepressants increase REM sleep muscle tone in patients with and without REM sleep behavior disorder. Sleep 38: 907–917. DOI:10.5665/sleep.4738.
- McKeith IG, Dickson DW, Lowe J, et al. 2005. Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 65: 1863–1872.
- Miyamoto T, Miyamoto M, Suzuki K, et al. 2008. 123I-MIBG Cardiac Scintigraphy provides clues to the underlying neurodegenerative disorder in idiopathic REM sleep behavior disorder. Sleep 31: 717–723.
- Montplaisir J, Gagnon JF, Fantini ML, et al. 2010. Polysomnographic diagnosis of idiopathic REM sleep behavior disorder. Mov Disord 25: 2044–2051. DOI:10.1002/mds.23257.
- Nakajima K, Okuda K, Matsuo S, et al. 2012. Standardization of metaiodobenzylguanidine heart to mediastinum ratio using a calibration phantom: effects of correction on normal databases and a multicenter study. Eur J Nucl Med Mol Imaging 39: 113–119. DOI:10.1007/s00259-011-1963-1.
- Olson EJ, Boeve BF, Silber MH. 2000. Rapid eye movement sleep behavior disorder: demographic, clinical and laboratory findings in 93 cases. Brain 123: 331–339.
- Onofrj M, Bonanni L, Manzoli L, Thomas A. 2010. Cohort study on somatoform disorders in Parkinson disease and dementia with Lewy bodies. Neurology 74: 1598–1606. DOI:10.1212/WNL.0b013e3181df09dd.
- Postuma RB, Gagnon JF, Vendette M, Montplaisir JY. 2009. Markers of neurodegeneration in idiopathic rapid eye movement sleep behaviour disorder and Parkinson's disease. Brain 132: 3298–3307. DOI:10.1093/brain/awp244.
- Postuma RB, Gagnon JF, Tuineaig M, et al. 2013. Antidepressants and REM sleep behavior disorder: isolated side effect or neurodegenerative signal? Sleep 36: 1579–1585. DOI:10.5665/sleep.3102.
- Sasai-Sakuma T, Frauscher B, et al. 2014. Quantitative assessment of isolated rapid eye movement (REM) sleep without atonia without clinical REM sleep behavior disorder: clinical and research implications. Sleep Med 15: 1009–1015.
- Schenck CH, Mahowald MW. 2008. Subclinical REM sleep behavior disorder and its clinical and research implications. Sleep 31: 1627. DOI:10.1016/j.sleep.2014.02.010.
- Spiegel J, Möllers MO, Jost WH, et al. 2005. FP-CIT and MIBG scintigraphy in early Parkinson's disease. Mov Disord 20: 552–561.
- Stefani A, Gabelia D, Högl B, et al. 2015. Long-term follow-up investigation of isolated rapid eye movement sleep without atonia without rapid eye movement sleep behavior disorder: a pilot study. J Clin Sleep Med 11: 1273–1279. DOI:10.5664/jcsm.5184.
- Teman PT, Tippmann-Peikert M, Silber MH, Slocumb NL, Auger RR. 2009. Idiopathic rapid-eye-movement sleep disorder: associations with antidepressants, psychiatric diagnoses, and other factors, in relation to age of onset. Sleep Med 10: 60–65. DOI:10.1016/j.sleep.2007.11.019.
- Tossici-Bolt L, Hoffmann SM, Kemp PM, Mehta RL, Fleming JS. 2006. Quantification of [123I]FP-CIT SPECT brain images: an accurate technique for measurement of the specific binding ratio. Eur J Nucl Med Mol Imaging 33: 1491–9.
- Tsopelas C, Stewart R, Savva GM, et al. 2011. Neuropathological correlates of late-life depression in older people. Br J Psychiatry 198: 109–114. DOI:10.1192/bjp.bp.110.078816.
- Waragai M, Mizumura S, Yamada T, Matsuda H. 2008. Differentiation of early-stage Alzheimer's disease from other types of dementia using brain perfusion single photon emission computed tomography with easy Z-score imaging system analysis. Dement Geriatr Cogn Disord 26: 547–555. DOI:10.1159/000180280.
- Weisskopf MG, Chen H, Schwarzschild MA, Kawachi I, Ascherio A. 2003. Prospective study of phobic anxiety and risk of Parkinson's disease. Mov Disord 18: 646–651.
- Winkelman JW, James L. 2004. Serotonergic antidepressants are associated with REM sleep without atonia. Sleep 27: 317–321.
- Wing YK, Lam SP, Li SX, et al. 2008. REM sleep behavior disorder in Hong Kong Chinese: clinical outcome and gender comparison. J Neurol Neurosurg Psychiatry 79: 1415–1416. DOI:10.1136/jnnp.2008.155374.
- Wing YK, Lam SP, Zhang J, et al. 2015. Reduced striatal dopamine transmission in REM sleep behavior disorder comorbid with depression. Neurology 84: 516–522. DOI:10.1212/WNL.0000000000001215.