Skip to main content
Log in

Impact of sleep-related breathing disorder on motor and non-motor symptoms in multiple system atrophy

  • Sleep Breathing Physiology and Disorders • Original Article
  • Published:
Sleep and Breathing Aims and scope Submit manuscript

Abstract

Introduction

Although several studies suggested that sleep-related breathing disorder (SRBD) is a frequent symptom of multiple system atrophy (MSA), whether SRBD has influence on the motor and non-motor symptoms of MSA is unknown.

Methods

A total of 40 MSA patients and 40 healthy volunteers (HVs) underwent video-polysomnography (PSG) in the current study. All the MSA individuals were assessed using the Epworth Sleepiness Scale (ESS), Unified Multiple-System Atrophy Rating Scale (UMSARS), Hamilton Depression Scale (HAMD), Hamilton Anxiety Scale, Frontal assessment battery (FAB), Parkinson’s Disease Questionnaire-39 (PDQ-39), and the Montreal Cognitive Assessment (MoCA).

Results

We found apnea-hypopnea index (AHI) of the MSA patients recorded by PSG was 16.4 ± 20.2. SRBD was found in 65% of the MSA patients (26/40), which was significantly higher than HVs (8/40, 20%) (p = 0.0001). Compared to the MSA patients without SRBD, MSA individuals with SRBD showed higher total UMSARS, UMSARS-II, FAB, and HAMD scores, more frequent occurrence of excessive daytime sleepiness, hypopneas, longer mean times for hypopneas, and obstructive sleep apnea (OSA), as well as longer time for OSA. This study suggested that SRBD is frequently seen in MSA patients.

Conclusion

MSA individuals with SRBD are prone to be severe motor deficits, depression, frontal lobe dysfunction, and excessive daytime sleepiness.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Stefanova N, Bucke P, Duerr S, Wenning GK (2009) Multiple system atrophy: an update. The Lancet Neurology 8(12):1172–1178. https://doi.org/10.1016/s1474-4422(09)70288-1

    Article  CAS  PubMed  Google Scholar 

  2. Ghorayeb I, Yekhlef F, Chrysostome V, Balestre E, Bioulac B, Tison F (2002) Sleep disorders and their determinants in multiple system atrophy. J Neurol Neurosurg Psychiatry 72(6):798–800. https://doi.org/10.1136/jnnp.72.6.798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Ferini-Strambi L, Marelli S (2012) Sleep dysfunction in multiple system atrophy. Curr Treat Options Neurol 14(5):464–473. https://doi.org/10.1007/s11940-012-0189-2

    Article  PubMed  Google Scholar 

  4. Gaig C, Iranzo A (2012) Sleep-disordered breathing in neurodegenerative diseases. Curr Neurol Neurosci Rep 12(2):205–217. https://doi.org/10.1007/s11910-011-0248-1

    Article  PubMed  Google Scholar 

  5. Giannini G, Calandra-Buonaura G, Mastrolilli F, Righini M, Bacchi-Reggiani ML, Cecere A, Barletta G, Guaraldi P, Provini F, Cortelli P (2016) Early stridor onset and stridor treatment predict survival in 136 patients with MSA. Neurology 87(13):1375–1383. https://doi.org/10.1212/wnl.0000000000003156

    Article  PubMed  Google Scholar 

  6. Vetrugno R, Provini F, Cortelli P, Plazzi G, Lotti EM, Pierangeli G, Canali C, Montagna P (2004) Sleep disorders in multiple system atrophy: a correlative video-polysomnographic study. Sleep Med 5(1):21–30. https://doi.org/10.1016/j.sleep.2003.07.002

    Article  PubMed  Google Scholar 

  7. Guo XY, Cao B, Lei F, Huang L, Chen K, Song W, Zhao B, Tang X, Shang H (2013) Clinical and polysomnographic features of patients with multiple system atrophy in Southwest China. Sleep Breath 17(4):1301–1307. https://doi.org/10.1007/s11325-013-0839-y

    Article  PubMed  Google Scholar 

  8. Moreno-Lopez C, Santamaria J, Salamero M, Del Sorbo F, Albanese A, Pellecchia MT, Barone P, Overeem S, Bloem B, Aarden W, Canesi M, Antonini A, Duerr S, Wenning GK, Poewe W, Rubino A, Meco G, Schneider SA, Bhatia KP, Djaldetti R, Coelho M, Sampaio C, Cochen V, Hellriegel H, Deuschl G, Colosimo C, Marsili L, Gasser T, Tolosa E (2011) Excessive daytime sleepiness in multiple system atrophy (SLEEMSA study). Arch Neurol 68(2):223–230. https://doi.org/10.1001/archneurol.2010.359

    Article  PubMed  Google Scholar 

  9. Gama RL, Tavora DG, Bomfim RC, Silva CE, de Bruin VM, de Bruin PF (2010) Sleep disturbances and brain MRI morphometry in Parkinson’s disease, multiple system atrophy and progressive supranuclear palsy—a comparative study. Parkinsonism Relat Disord 16(4):275–279. https://doi.org/10.1016/j.parkreldis.2010.01.002

    Article  PubMed  Google Scholar 

  10. Gilman S, Wenning GK, Low PA, Brooks DJ, Mathias CJ, Trojanowski JQ, Wood NW, Colosimo C, Duerr A, Fowler CJ, Kaufmann H, Klockgether T, Lees A, Poewe W, Quinn N, Revesz T, Robertson D, Sandroni P, Seppi K, Vidailhet M (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71(9):670–676. https://doi.org/10.1212/01.wnl.0000324625.00404.15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of levodopa dose equivalency reporting in Parkinson's disease. Mov Disord 25(15):2649–2653. https://doi.org/10.1002/mds.23429

    Article  PubMed  Google Scholar 

  12. Wenning GK, Tison F, Seppi K, Sampaio C, Diem A, Yekhlef F, Ghorayeb I, Ory F, Galitzky M, Scaravilli T, Bozi M, Colosimo C, Gilman S, Shults CW, Quinn NP, Rascol O, Poewe W (2004) Development and validation of the unified multiple system atrophy rating scale (UMSARS). Mov Disord 19(12):1391–1402. https://doi.org/10.1002/mds.20255

    Article  PubMed  Google Scholar 

  13. Iber C A-IS, Chesson A, Quan SF, American Academy of Sleep Medicine (2007) The AASM manual for the scoring of sleep and associated events: rules, terminology and technical specifications, 2nd edn. American Academy of Sleep Medicine, Westchester

    Google Scholar 

  14. Berry RB, Budhiraja R, Gottlieb DJ, Gozal D, Iber C, Kapur VK, Marcus CL, Mehra R, Parthasarathy S, Quan SF, Redline S, Strohl KP, Davidson Ward SL, Tangredi MM, American Academy of Sleep M (2012) Rules for scoring respiratory events in sleep: update of the 2007 AASM Manual for the Scoring of Sleep and Associated Events. Deliberations of the Sleep Apnea Definitions Task Force of the American Academy of Sleep Medicine. J Clin Sleep Med 8(5):597–619. https://doi.org/10.5664/jcsm.2172

    Article  PubMed  PubMed Central  Google Scholar 

  15. Valko PO, Hauser S, Sommerauer M, Werth E, Baumann CR (2014) Observations on sleep-disordered breathing in idiopathic Parkinson’s disease. PLoS One 9(6):e100828. https://doi.org/10.1371/journal.pone.0100828

    Article  PubMed  PubMed Central  Google Scholar 

  16. American Academy of Sleep Medicine (2005) The international classification of sleep disorders. Second Edition ICSD-2

  17. Ghorayeb I, Yekhlef F, Bioulac B, Tison F (2005) Continuous positive airway pressure for sleep-related breathing disorders in multiple system atrophy: long-term acceptance. Sleep Med 6(4):359–362. https://doi.org/10.1016/j.sleep.2004.10.002

    Article  PubMed  Google Scholar 

  18. Benarroch EE (2007) Brainstem respiratory control: substrates of respiratory failure of multiple system atrophy. Mov Disord 22(2):155–161. https://doi.org/10.1002/mds.21236

    Article  PubMed  Google Scholar 

  19. Merlo IM, Occhini A, Pacchetti C, Alfonsi E (2002) Not paralysis, but dystonia causes stridor in multiple system atrophy. Neurology 58(4):649–652. https://doi.org/10.1212/WNL.58.4.649

    Article  PubMed  Google Scholar 

  20. Iranzo A, Santamaria J, Tolosa E, Vilaseca I, Valldeoriola F, Marti MJ, Munoz E (2004) Long-term effect of CPAP in the treatment of nocturnal stridor in multiple system atrophy. Neurology 63(5):930–932. https://doi.org/10.1212/01.WNL.0000137043.76383.A4

    Article  CAS  PubMed  Google Scholar 

  21. Shimohata T, Nakayama H, Tomita M, Ozawa T, Nishizawa M (2012) Daytime sleepiness in Japanese patients with multiple system atrophy: prevalence and determinants. BMC Neurol 12(1):130. https://doi.org/10.1186/1471-2377-12-130

    Article  PubMed  PubMed Central  Google Scholar 

  22. Muntean ML, Sixel-Doring F, Trenkwalder C (2013) No difference in sleep and RBD between different types of patients with multiple system atrophy: a pilot video-polysomnographical study. Sleep Disord 2013:258390. https://doi.org/10.1155/2013/258390

    Article  PubMed  PubMed Central  Google Scholar 

  23. Soylu AC, Levent E, Sariman N, Yurtlu S, Alparslan S, Saygi A (2012) Obstructive sleep apnea syndrome and anthropometric obesity indexes. Sleep Breath 16(4):1151–1158. https://doi.org/10.1007/s11325-011-0623-9

    Article  PubMed  Google Scholar 

  24. Chen WC, Lim PS, Wu WC, Chiu HC, Chen CH, Kuo HY, Tsai TW, Chien PI, Su YJ, Su YL, Hung SH, Woods HF (2006) Sleep behavior disorders in a large cohort of chinese (Taiwanese) patients maintained by long-term hemodialysis. Am J Kidney Dis 48(2):277–284. https://doi.org/10.1053/j.ajkd.2006.04.079

    Article  PubMed  Google Scholar 

  25. Benarroch EE, Schmeichel AM, Low PA, Parisi JE (2013) Parabrachial nucleus involvement in multiple system atrophy. Auton Neurosci 177(2):170–174. https://doi.org/10.1016/j.autneu.2013.04.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Vincken WG, Gauthier SG, Dollfuss RE, Hanson RE, Darauay CM, Cosio MG (1984) Involvement of upper-airway muscles in extrapyramidal disorders. A cause of airflow limitation. N Engl J Med 311(7):438–442. https://doi.org/10.1056/nejm198408163110704

    Article  CAS  PubMed  Google Scholar 

  27. Takaya M, Atsumi M, Hirose T, Ishii K, Shirakawa O (2015) Cognitive impairment before changes appear on [18F]-fluoro-D-glucose positron emission tomography images in a patient with possible early-stage cerebellar-predominant multiple system atrophy. Psychogeriatrics 16(3):216–221. https://doi.org/10.1111/psyg.12134

    Article  PubMed  Google Scholar 

  28. Shiota S, Takekawa H, Matsumoto SE, Takeda K, Nurwidya F, Yoshioka Y, Takahashi F, Hattori N, Tabira T, Mochizuki H, Takahashi K (2013) Chronic intermittent hypoxia/reoxygenation facilitate amyloid-beta generation in mice. J Alzheimer's Dis 37(2):325–333. https://doi.org/10.3233/jad-130419

    Article  CAS  Google Scholar 

  29. Ancoli-Israel S, Palmer BW, Cooke JR, Corey-Bloom J, Fiorentino L, Natarajan L, Liu L, Ayalon L, He F, Loredo JS (2008) Cognitive effects of treating obstructive sleep apnea in Alzheimer’s disease: a randomized controlled study. J Am Geriatr Soc 56(11):2076–2081. https://doi.org/10.1111/j.1532-5415.2008.01934.x

    Article  PubMed  PubMed Central  Google Scholar 

  30. Cao B, Zhao B, Wei QQ, Chen K, Yang J, Ou R, Wu Y, Shang HF (2015) The global cognition, frontal lobe dysfunction and behavior changes in Chinese patients with multiple system atrophy. PLoS One 10(10):e0139773. https://doi.org/10.1371/journal.pone.0139773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Chotinaiwattarakul W, Dayalu P, Chervin RD, Albin RL (2011) Risk of sleep-disordered breathing in Parkinson’s disease. Sleep Breath 15(3):471–478. https://doi.org/10.1007/s11325-010-0362-3

    Article  PubMed  Google Scholar 

  32. Kylstra WA, Aaronson JA, Hofman WF, Schmand BA (2013) Neuropsychological functioning after CPAP treatment in obstructive sleep apnea: a meta-analysis. Sleep Med Rev 17(5):341–347. https://doi.org/10.1016/j.smrv.2012.09.002

    Article  PubMed  Google Scholar 

Download references

Funding

Sichuan University provided financial support in the form of Young scholars’ scientific research funding (Grant No.2016SCU11017). The sponsor had no role in the design or conduct of this research.

Author information

Authors and Affiliations

Authors

Contributions

Bei Cao: Clinical data collection, data analysis, and writing this paper;

Qian-Qian Wei: Clinical data collection and following up;

Ruwei Ou: Clinical data collection and following up;

Bi Zhao: Clinical data collection and following up;

Tao Hu: Clinical data collection and following up;

Yongping Chen: Clinical data collection and following up;

Jing Yang: Clinical data collection and following up;

Fei Lei: Data collection of sleep study;

Xiangdong Tang: Explaining the data of sleep study;

Hui-Fang Shang: Designing this study and revising this paper.

Corresponding authors

Correspondence to Xiangdong Tang or Hui-Fang Shang.

Ethics declarations

Conflicts of interest

The authors declare that they have no conflicts of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of Sichuan University research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The Ethics Committee of Sichuan University approved this study. Informed consent was obtained from all individual participants included in the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cao, B., Wei, QQ., Ou, R. et al. Impact of sleep-related breathing disorder on motor and non-motor symptoms in multiple system atrophy. Sleep Breath 22, 981–987 (2018). https://doi.org/10.1007/s11325-018-1632-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11325-018-1632-8

Keywords

Navigation