Skip to main content

Laryngopharyngeal motor dysfunction and obstructive sleep apnea in Parkinson’s disease

Sleep and Breathing volume 23, pages 543–550 (2019)Cite this article

Abstract

Purpose

Obstructive sleep apnea (OSA) is a common sleep disorder in Parkinson’s disease (PD), but the relationship between these two conditions remains uncertain. Upper airway (UA) dysfunction in PD is well documented in some patients and is believed to be a reflex of the motor involvement of laryngopharyngeal muscles. The aim of this study is to determine whether UA dysfunction and laryngopharyngeal motor dysfunction (LMD) are involved in the obstructive phenomenon of OSA in PD.

Methods

Forty-eight PD patients underwent polysomnography for OSA diagnosis, functional evaluation of the UA by spirometry and a clinical protocol for analysis of laryngopharyngeal muscles and physical examination.

Results

Thirty-one participants (64.6%) fulfilled the criteria for OSA according to the International Classification of Sleep Disorders- third edition (at least respiratory disturbance index of five or higher per hour of sleep plus specific symptoms). UA obstruction was observed in 25% of participants and LMD in 60.4%. Among the clinical indicators of LMD, hypophonia was the most common (58.3%). Participants with LMD had a threefold greater chance of presenting with OSA than those without LMD did (OR = 3.49; 95% CI, 1.01–12.1; p = 0.044). Individuals with LMD had more UA dysfunction (37.9 vs 10.5%, p = 0.037), higher scores on UPDRS III (20 vs 15, p = 0.0005) and the Hoehn-Yahr scale (2.5 vs 2.0, p = 0.008), and higher frequencies of postural changes (51.7 vs 21.1%, p = 0.033) and motor phenomena (65.5 vs 31.6%, p = 0.021). Obesity, snoring, neck circumference, and the Mallampati score did not correlate with OSA in PD.

Conclusion

LMD should be considered a factor that is involved in the obstructive phenomenon of UA in patients with OSA and PD.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1

References

  1. Halliday G, Lees A, Stern M (2011) Milestones in Parkinson’s disease-clinical and pathologic features. Mov Disord 26:1015–1021. https://doi.org/10.1002/mds.23669

    Article  PubMed  Google Scholar 

  2. Cochen De Cock V, Vidailhet M, Arnulf I (2008) Sleep disturbances in patients with parkinsonism. Nat Clin Pract Neurol 4:254–266. https://doi.org/10.1038/ncpneuro0775

    Article  Google Scholar 

  3. Iranzo A, Tolosa E, Gelpi E, Molinuevo JL, Valldeoriola F, Serradell M, Sanchez-Valle R, Vilaseca I, Lomeña F, Vilas D, Lladó A, Gaig C, Santamaria J (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. https://doi.org/10.1016/S1474-4422(13)70056-5

    Article  PubMed  Google Scholar 

  4. De Lau LML, Breteler MMB (2006) Epidemiology of Parkinson’s disease. Lancet Neurol 5:525–535. https://doi.org/10.1016/S1474-4422(06)70471-9

    Article  Google Scholar 

  5. Tufik S, Santos-Silva R, Taddei JA, Bittencourt LR (2010) Obstructive sleep apnea syndrome in the Sao Paulo Epidemiologic Sleep Study. Sleep Med 11:441–446. https://doi.org/10.1016/j.sleep.2009.10.005

    Article  PubMed  Google Scholar 

  6. da Silva-Júnior FP, do Prado GF, Barbosa ER, Tufik S, Togeiro SM (2014) Sleep disordered breathing in Parkinson’s disease: a critical appraisal. Sleep Med Rev 18:173–178. https://doi.org/10.1016/j.smrv.2013.04.005

    Article  PubMed  Google Scholar 

  7. Schwartz AR, Patil SP, Laffan AM, Polotsky V, Schneider H, Smith PL (2008) Obesity and obstructive sleep apnea: pathogenic mechanisms and therapeutic approaches. Proc Am Thorac Soc 5:185–192. https://doi.org/10.1513/pats.200708-137MG

    Article  PubMed  PubMed Central  Google Scholar 

  8. 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 311:438–442. https://doi.org/10.1056/NEJM198408163110704

    Article  CAS  PubMed  Google Scholar 

  9. Sabaté M, González I, Ruperez F, Rodríguez M (1996) Obstructive and restrictive pulmonary dysfunctions in Parkinson’s disease. J Neurol Sci 138:114–119. https://doi.org/10.1016/0022-510X(96)00003-2

    Article  PubMed  Google Scholar 

  10. Shill H, Stacy M (2002) Respiratory complications of Parkinson’s disease. Semin Respir Crit Care Med 23:261–265. https://doi.org/10.1055/s-2002-33034

    Article  PubMed  Google Scholar 

  11. Herer B, Arnulf I, Housset B (2001) Effects of levodopa on pulmonary function in Parkinson’s disease. Chest 119:387–393. https://doi.org/10.1378/chest.119.2.387

    Article  CAS  PubMed  Google Scholar 

  12. Sawczuk A, Mosier KM (2001) Neural control of tongue movement with respect to respiration and swallowing. Crit Rev Oral Biol Med 12:18–37. https://doi.org/10.1177/10454411010120010101

    Article  CAS  PubMed  Google Scholar 

  13. Mu L, Sobotka S, Chen J, Su H, Sanders I, Adler CH, Shill HA, Caviness JN, Samanta JE, Beach TG, Arizona Parkinson’s Disease Consortium (2013) Alpha-synuclein pathology and axonal degeneration of the peripheral motor nerves innervating pharyngeal muscles in Parkinson disease. J Neuropathol Exp Neurol 72:119–129. https://doi.org/10.1097/NEN.0b013e3182801cde

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Baker KK, Ramig LO, Luschei ES, Smith ME (1998) Thyroarytenoid muscle activity associated with hypophonia in Parkinson disease and aging. Neurology 51:1592–1598. https://doi.org/10.1212/WNL.51.6.1592

    Article  CAS  PubMed  Google Scholar 

  15. Cochen De Cock V, Abouda M, Leu S, Oudiette D, Roze E, Vidailhet M, Similowski T, Arnulf I (2010) Is obstructive sleep apnea a problem in Parkinson’s disease? Sleep Med 11:247–252. https://doi.org/10.1016/j.sleep.2009.05.008

    Article  PubMed  Google Scholar 

  16. Maria B, Sophia S, Michalis M, Charalampos L, Andreas P, John ME, Nikolaos SM (2003) Sleep breathing disorders in patients with idiopathic Parkinson’s disease. Respir Med 97:1151–1157. https://doi.org/10.1016/S0954-6111(03)00188-4

    Article  PubMed  Google Scholar 

  17. Neikrug AB, Maglione JE, Liu L, Natarajan L, Avanzino JA, Corey-Bloom J, Palmer BW, Loredo JS, Ancoli-Israel S (2013) Effects of sleep disorders on the non-motor symptoms of Parkinson disease. J Clin Sleep Med 9:1119–1129. https://doi.org/10.5664/jcsm.3148

    Article  PubMed  PubMed Central  Google Scholar 

  18. Trotti LM, Bliwise DL (2010) No increased risk of obstructive sleep apnea in Parkinson’s disease. Mov Disord 25:2246–2249. https://doi.org/10.1002/mds.23231

    Article  PubMed  PubMed Central  Google Scholar 

  19. Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181–184. https://doi.org/10.1136/jnnp.55.3.181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Brazilian Institute of Geography and Statistics (2011). Ethno-racial characteristics of the population – a study of the 2008 classification categories of color or race. Resource https://biblioteca.ibge.gov.br/visualizacao/livros/liv49891.pdf. Accessed 20 May 2018

  21. 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 25:2649–2653. https://doi.org/10.1002/mds.23429

    Article  PubMed  Google Scholar 

  22. Bertolazi AN, Fagondes SC, Hoff LS, Pedro VD, Menna Barreto SSM, Johns MW (2009) Portuguese-language version of the Epworth sleepiness scale: validation for use in Brazil. J Bras Pneumol 35:877–883. https://doi.org/10.1590/S1806-37132009000900009

    Article  PubMed  Google Scholar 

  23. Berry RB, Brooks R, Gramaldo CE, et al For the American Academy of Sleep Medicine (2017) The AASM manual for the scoring of sleep and associated events: rules, terminology and technical specifications. Version 2.4 American Academy of Sleep Medicine, Darien, Illinois

  24. American Academy of Sleep Medicine (2014) International classification of sleep disorders, 3rd edn. American Academy of Sleep Medicine, Darien, Illinois

  25. Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, Crapo R, Enright P, van der Grinten CP, Gustafsson P, Jensen R, Johnson DC, MacIntyre N, McKay R, Navajas D, Pedersen OF, Pellegrino R, Viegi G, Wanger J, ATS/ERS Task Force (2005) Standardisation of spirometry. Eur Respir J 26:319–338. https://doi.org/10.1183/09031936.05.00034805

    Article  CAS  PubMed  Google Scholar 

  26. Pereira CAC, Sato T, Rodrigues SC (2007) New reference values for forced spirometry in white adults in Brazil. J Bras Pneumol 33:397–406. https://doi.org/10.1590/S1806-37132007000400008

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  28. Wang Y, Shao WB, Gao L, Lu J, Gu H, Sun LH (2014) Abnormal pulmonary function and respiratory muscle strength findings in Chinese patients with Parkinson’s disease and multiple system atrophy: comparison with normal elderly. PLoS One 9:e116123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Modrykamien AM, Gudavalli R, McCarthy K, Liu X, Stoller JK (2009) Detection of upper airway obstruction with spirometry results and the flow-volume loop: a comparison of quantitative and visual inspection criteria. Respir Care 54:474–479

    PubMed  Google Scholar 

  30. Hoffstein V, Oliver Z (2003) Pulmonary function and sleep apnea. Sleep Breath 7:159–165. https://doi.org/10.1007/s11325-003-0159-8

    Article  PubMed  Google Scholar 

  31. Yoshida T, Kono I, Yoshikawa K, Hashimoto H, Harada H, Nakagawa M (2003) Improvement of sleep hypopnea by antiparkinsonian drugs in a patient with Parkinson’s disease: a polysomnographic study. Intern Med 42:1135–1138. https://doi.org/10.2169/internalmedicine.42.1135

    Article  PubMed  Google Scholar 

  32. Saletu M, Anderer P, Saletu B, Hauer C, Mandl M, Oberndorfer S, Zoghlami A, Saletu-Zyhlarz G (2000) Sleep laboratory studies in restless legs syndrome patients as compared with normals and acute effects of ropinirole. 2. Findings on periodic leg movements, arousals and respiratory variables. Neuropsychobiology 41:190–199. https://doi.org/10.1159/000026659

    Article  CAS  PubMed  Google Scholar 

  33. Zamarron C, García Paz VC, Riveiro A (2008) Obstructive sleep apnea syndrome is a systemic disease. Current evidence. Eur J Intern Med 19:390–398. https://doi.org/10.1016/j.ejim.2007.12.006

    Article  PubMed  Google Scholar 

  34. Chen JC, Tsai TY, Li CY, Hwang JH (2015) Obstructive sleep apnea and risk of Parkinson’s disease: a population-based cohort study. J Sleep Res 24:432–437. https://doi.org/10.1111/jsr.12289

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Movement Disorder Sector, Neurology Unit, Pedro Ernesto University Hospital, State University of Rio de Janeiro, Av. 28 de setembro, 77, Vila Isabel, Rio de Janeiro, 20550-031, Brazil

    Christianne Martins Corrêa Silva Bahia & João Santos Pereira

  2. Rehabilitation Sciences Post-Graduation Program, Augusto Motta University Center, Rio de Janeiro, Brazil

    Agnaldo José Lopes

Authors
  1. Christianne Martins Corrêa Silva Bahia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. João Santos Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Agnaldo José Lopes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christianne Martins Corrêa Silva Bahia.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Research involving human participants and/or animals

All procedures performed in the studies involving human participants were in accordance with the ethical standards of the Rio de Janeiro State University Research Committee and with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Ethical approval

The study was approved by the institutional research ethics committee under number 500184.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bahia, C.M.C.S., Pereira, J.S. & Lopes, A.J. Laryngopharyngeal motor dysfunction and obstructive sleep apnea in Parkinson’s disease. Sleep Breath 23, 543–550 (2019). https://doi.org/10.1007/s11325-018-1729-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11325-018-1729-0

Keywords

  • Parkinson’s disease
  • Laryngopharyngeal motor dysfunction
  • Upper airway
  • Obstructive sleep apnea
  • Spirometry
  • Mallampati score