Dysphagia in Parkinson’s Disease

Abstract

More than 80 % of patients with Parkinson’s disease (PD) develop dysphagia during the course of their disease. Swallowing impairment reduces quality of life, complicates medication intake and leads to malnutrition and aspiration pneumonia, which is a major cause of death in PD. Although the underlying pathophysiology is poorly understood, it has been shown that dopaminergic and non-dopaminergic mechanisms are involved in the development of dysphagia in PD. Clinical assessment of dysphagia in PD patients is challenging and often delivers unreliable results. A modified water test assessing maximum swallowing volume is recommended to uncover oropharyngeal dysphagia in PD. PD-specific questionnaires may also be useful to identify patients at risk for swallowing impairment. Fiberoptic endoscopic evaluation of swallowing and videofluoroscopic swallowing study are both considered to be the gold standard for evaluation of PD-related dysphagia. In addition, high-resolution manometry may be a helpful tool. These instrumental methods allow a reliable detection of aspiration events. Furthermore, typical patterns of impairment during the oral, pharyngeal and/or esophageal swallowing phase of PD patients can be identified. Therapy of dysphagia in PD consists of pharmacological interventions and swallowing treatment by speech and language therapists (SLTs). Fluctuating dysphagia with deterioration during the off-state should be treated by optimizing dopaminergic medication. The methods used during swallowing treatment by SLTs shall be selected according to the individual dysphagia pattern of each PD patient. A promising novel method is an intensive training of expiratory muscle strength. Deep brain stimulation does not seem to have a clinical relevant effect on swallowing function in PD. The goal of this review is giving an overview on current stages of epidemiology, pathophysiology, diagnosis, and treatment of PD-associated dysphagia, which might be helpful for neurologists, speech-language therapists, and other clinicians in their daily work with PD patients and associated swallowing difficulties. Furthermore areas with an urgent need for future clinical research are identified.

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References

  1. 1.

    Pringsheim T, Jette N, Frolkis A, Steeves T. The prevalence of Parkinson’s disease: a systematic review and meta-analysis. Mov Disord. 2014;29(13):1583–90.

    Article  PubMed  Google Scholar 

  2. 2.

    Dorsey ER, Constantinescu R, Thompson JP, et al. Projected number of people with Parkinson disease in the most populous nation, 2005 through 2030. Neurology. 2007;68(5):384–6.

    Article  PubMed  CAS  Google Scholar 

  3. 3.

    Parkinson J. An essay on the shaking palsy. London: Sherwood, Neely and Jones; 1817.

    Google Scholar 

  4. 4.

    Kalf J, de Swart B, Bloem B, Munneke M. Prevalence of oropoharyngeal dysphagia in Parkinson’s disease: a meta-analysis. Parkinsonism Relat Disord. 2012;18(4):311–5.

    Article  PubMed  CAS  Google Scholar 

  5. 5.

    Miller N, Allcock L, Hildreth AJ, Jones D, Noble E, Burn DJ. Swallowing problems in Parkinson disease: frequency and clinical correlates. J Neurol Neurosurg Psychiatr. 2009;80(9):1047–9.

    Article  PubMed  CAS  Google Scholar 

  6. 6.

    Sapir S, Ramig L, Fox C. Speech and swallowing disorders in Parkinson disease. Curr Opin Otolaryngol Head Neck Surg. 2008;16(3):205–10.

    Article  PubMed  Google Scholar 

  7. 7.

    Edwards L, Quiglex EM, Hofmann R, Pfeiffer RF. Gastrointestinal symptoms in Parkinson’s disesase: 18-month-follow-up study. Mov Disord. 1993;8(1):83–6.

    Article  PubMed  CAS  Google Scholar 

  8. 8.

    Barone P, Antonini A, Colosimo C, et al. The PRIAMO study: a multicenter assessment of nonmotor symptomes and their impact on quality of life in Parkinson’s disease. Mov Disord. 2009;24(11):1641–9.

    Article  PubMed  Google Scholar 

  9. 9.

    Cereda E, Cilia R, Klersy C, et al. Swallowing disturbances in Parkinson’s disease: a multivariate analysis of contributing factors. Parkinsonism Relat Disord. 2014;20(12):1382–7.

    Article  PubMed  Google Scholar 

  10. 10.

    Müller J, Wenning GK, Verny J, et al. Progression of dysarthria and dysphagia in postmortem-confirmed parkinsonian disorders. Arch Neurol. 2001;58(2):259–64.

    Article  PubMed  Google Scholar 

  11. 11.

    Coelho M, Marti MJ, Tolosa E, et al. Late-stage Parkinson’s disease: the barcelona and lisbon cohort. J Neurol. 2010;257(9):1524–32.

    Article  PubMed  Google Scholar 

  12. 12.

    Fuh J, Lee RC, Wang J, et al. Swallowing difficulty in Parkinson’s disease. Clin Neurol Neurosurg. 1997;99(2):106–12.

    Article  PubMed  CAS  Google Scholar 

  13. 13.

    Noyce A, Silveira-Moriyama L, Gilpin P, Ling H, Howard R, Lees A. Severe dysphagia as a presentation of Parkinson’s disease. Mov Disord. 2012;27(3):457.

    Article  PubMed  Google Scholar 

  14. 14.

    Thomas M, Haigh R. Dysphagia, a reversible cause not to be forgotten. Postgrad Med J. 1995;71(832):94–5.

    PubMed Central  Article  PubMed  CAS  Google Scholar 

  15. 15.

    Miller N, Noble E, Jones D, Burn D. Hard to swallow: dysphagia in Parkinson’s disease. Age Ageing. 2006;35(6):614–8.

    Article  PubMed  Google Scholar 

  16. 16.

    Plowman-Prine EK, Sapienza CM, Okun MS, Pollock SL, Jacobson C, Wu SS, et al. The relationship between quality of life and swallowing in Parkinson’s disease. Mov Disord. 2009;24(9):1352–8.

    PubMed Central  Article  PubMed  Google Scholar 

  17. 17.

    Morgante L, Salemi G, Meneghini F, et al. Parkinson disease survival: a population-based study. Arch Neurol. 2000;57(4):507–12.

    Article  PubMed  CAS  Google Scholar 

  18. 18.

    Lin CW, Chang YC, Chen WS, et al. Prolonged swallowing time in dysphagic Parkinsonism patients with aspiration pneumonia. Arch Phys Med Rehabil. 2012;93:2080–4.

    Article  PubMed  Google Scholar 

  19. 19.

    Fasano A, Visanji NP, Liu LW, Lang AE, Pfeiffer RF. Gastrointestinal dysfunction in Parkinson’s disease. Lancet Neurol. 2015;14:625–39.

    Article  PubMed  CAS  Google Scholar 

  20. 20.

    Manor Y, Balas M, Giladi N, Mootanah R, Cohen J. Anxiety, depression and swallowing disorders in patients with Parkinson’s disease. Parkinsonism Relat Disord. 2009;15(6):453–6.

    Article  PubMed  Google Scholar 

  21. 21.

    Michou E, Hamdy S. Dysphagia in Parkinson’s disease: a therapeutic challenge? Expert Rev Neurother. 2010;10(6):875–8.

    Article  PubMed  Google Scholar 

  22. 22.

    Leopold NA, Daniels SK. Supranuclear control of swallowing. Dysphagia. 2010;25(3):250–7.

    Article  PubMed  Google Scholar 

  23. 23.

    Suzuki M, Asada Y, Ito J, Hayashi K, Inoue H, Kitano H. Activation of cerebellum and basal ganglia on volitional swallowing detected by functional magnetic resonance imaging. Dysphagia. 2003;18(2):71–7.

    Article  PubMed  Google Scholar 

  24. 24.

    Warnecke T, Hamacher C, Oelenberg S, Dziewas R. Off and on-state assessment of swallowing function in Parkinson’s disease. Parkinsonism Relat Disord. 2014;20(9):1033–4.

    Article  PubMed  Google Scholar 

  25. 25.

    Troche MS, Brandimore AE, Foote KD, Okun MS. Swallowing and deep brain stimulation in Parkinson’s disease: a systematic review. Parkinsonism Relat Disord. 2013;19(9):783–8.

    PubMed Central  Article  PubMed  Google Scholar 

  26. 26.

    Braak H, Del Tredici K, Rub U, de Vos R, Jansen Steur E, Braak E. Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging. 2003;24(2):197–211.

    Article  PubMed  Google Scholar 

  27. 27.

    Hunter P, Crameri J, Austin S, Woodward M, Hughes A. Response of parkinsonian swallowing dysfunction to dopaminergic stimulation. J Neurol Neurosurg Psychiatry. 1997;63(5):579–83.

    PubMed Central  Article  PubMed  CAS  Google Scholar 

  28. 28.

    Braak H, Del Tredici K, Bratzke H, et al. Staging of the intracerebral inclusion body pathology associated with idiopathic Parkinson’s disease (preclinical and clinical stages). J Neurol. 2002;249(Suppl 3):III1–5.

    Article  Google Scholar 

  29. 29.

    Suntrup S, Teismann I, Bejer J, Suttrup S, Winkels M, Mehler D, Pantev C, Dziewas R, Warnecke T. Evidence for adaptive cortical changes in swallowing in Parkinson’s disease. Brain. 2013;136(3):726–38.

    Article  PubMed  Google Scholar 

  30. 30.

    Berg D, Lang AE, Posturma RB, et al. Changing the research criteria for the diagnosis of Parkinson’s disease: obstacles and opportunities. Lancet Neurol. 2013;12(5):514–24.

    Article  PubMed  Google Scholar 

  31. 31.

    Shannon KM, Keshavarzian A, Dodiya HB, Jakate S, Kordower JH. Is alpha-synuclein in the colon a biomarker for premotor Parkinson’s disease? Evidence from 3 cases. Mov Disord. 2012;27(6):716–9.

    Article  PubMed  Google Scholar 

  32. 32.

    Pan-Montojo F, Reichmann H. Considerations on the role of environmental toxins in idiopathic Parkinson’s disease pathophysiology. Transl Neurodegener. 2014;3:10.

    PubMed Central  Article  PubMed  CAS  Google Scholar 

  33. 33.

    Pan-Montojo F, Anichtchik O, Dening Y. Progression of Parkinson’s disease pathology is reproduced by intragastric administration of rotenone in mice. PLoS ONE. 2010;5(1):e8762.

    PubMed Central  Article  PubMed  CAS  Google Scholar 

  34. 34.

    Pan-Montojo F, Schwarz M, Winkler C, et al. Environmental toxins trigger PD-like progression via increased alpha-synuclein release from enteric neurons in mice. Sci Rep. 2012;2:898.

    PubMed Central  Article  PubMed  CAS  Google Scholar 

  35. 35.

    Sung HY, Kim JS, Lee KS, et al. The prevalence and patterns of pharyngoesophageal dysmotility in patients with early stage Parkinson’s disesase. Mov Disord. 2010;25(14):2361–8.

    Article  PubMed  Google Scholar 

  36. 36.

    Mu L, Sobotka S, Chen J, et al. Alpha-Synuclein pathology and axonal degeneration of the peripheral motor nerves innervating pharyngeal muscles in Parkinson’s disease. J Neuropathol Exp Neurol. 2013;72(2):119–29.

    PubMed Central  Article  PubMed  CAS  Google Scholar 

  37. 37.

    Mu L, Sobotka S, Chen J, et al. Parkinson’s disease affects peripheral sensory nerves in the pharynx. J Neuropathol Exp Neurol. 2013;72(7):614–23.

    PubMed Central  Article  PubMed  Google Scholar 

  38. 38.

    Mu L, Sobotka S, Chen J, et al. Altered pharyngeal muscles in Parkinson disease. Neuropathol Exp Neurol. 2012;71(6):520–30.

    Article  Google Scholar 

  39. 39.

    Ciucci MR, Russell AJ, Schaser AJ, et al. Tongue force and timing deficits in a rat model of Parkinson disease. Behav Brain Res. 2011;222(2):315–20.

    PubMed Central  Article  PubMed  Google Scholar 

  40. 40.

    Ciucci MR, Schaser AJ, Russell JA. Exercise-induced rescue of tongue function without striatal dopamine sparing in a rat neurotoxin model of Parkinson disease. Behav Brain Res. 2013;252:239–45.

    PubMed Central  Article  PubMed  CAS  Google Scholar 

  41. 41.

    Russell AJ, Ciucci MR, Hammer MJ, Connor NP. Videofluorographic assessment of deglutitive behaviors in a rat model of aging and Parkinson disease. Dysphagia. 2013;28(1):95–104.

    PubMed Central  Article  PubMed  Google Scholar 

  42. 42.

    Kane JR, Ciucci MR, Jacobs AN, et al. Asssessing the role of dopamine in limb and cranial-oromotor control in a rat model of Parkinson’s disease. J Commun Disord. 2011;44(5):529–37.

    PubMed Central  Article  PubMed  Google Scholar 

  43. 43.

    Fulceri F, Biagioni F, Lenzi P, et al. Nigrostriatal damage with 6-OHDA: validation of routinely applied procedures. Ann N Y Acad Sci. 2006;1074:344–8.

    Article  PubMed  CAS  Google Scholar 

  44. 44.

    Tillerson JL, Cohen AD, Philhower J, et al. Forced limb-use effects on the behavioral and neurochemical effects of 6-hydroxydopamine. J Neurosci. 2001;21:4427–35.

    PubMed  CAS  Google Scholar 

  45. 45.

    Troche MS, Brandimore AE, Okun MS, Davenprot PW, Hegland KW. Decreased cough sensitivity and aspiration in Parkinson disease. Chest. 2014;146:1294–9.

    PubMed Central  Article  PubMed  Google Scholar 

  46. 46.

    Ebihara S, Saito H, Kanda A, Nakajoh M, Takahashi H, Arai H, Sasaki H. Impaired efficacy of cough in patients with Parkinson disease. Chest. 2003;124(3):1009–15.

    Article  PubMed  Google Scholar 

  47. 47.

    Bird M, Woodward M, Gibson E, Phyland D, Fonda D. Asymptomatic swallowing disorders in elderly patients with Parkinson’s disease: a description of findings on clinical examination and videofluoroscopy in sixteen patients. Age Ageing. 1994;23(3):251–4.

    Article  PubMed  CAS  Google Scholar 

  48. 48.

    Bushmann M, Dobmeyer S, Leeker L, Perlmutter J. Swallowing abnormalities and their responses to treatment in Parkinson’s disease. Neurology. 1989;39:1309–14.

    Article  PubMed  CAS  Google Scholar 

  49. 49.

    Prosiegel M. Neurogene dysphagien. In: Diener H, Weimar C, editors. Leitlinien für Diagnostik und Therapie in der Neurologie. Stuttgart: Georg Thieme Verlag; 2008.

    Google Scholar 

  50. 50.

    Simons JA, Fietzek UM, Waldmann A, Warnecke T, Schuster T, Ceballos-Baumann AO. Development and validation of a new screening questionnaire for dysphagia in early stages of Parkinson’s disease. Parkinsonism Relat Disord. 2014;20(9):992–8.

    Article  PubMed  Google Scholar 

  51. 51.

    Manor Y, Giladi N, Cohen A, Fliss D, Cohen T. Validation of a swallowing disturbance questionnaire for detecting dysphagia in patients with Parkinson’s disease. Mov Disord. 2007;22(13):1917–21.

    Article  PubMed  Google Scholar 

  52. 52.

    Evatt ML, Chaudhuri KR, Chou KL, et al. Dysautonomia rating scales in Parkinson’s disease: sialorrhea, dysphagia and constipation—critique and recommendations by Movement Disorders Task Force on rating scales for Parkinson’s disease. Mov Disord. 2009;24(5):635–46.

    PubMed Central  Article  PubMed  Google Scholar 

  53. 53.

    McHorney CA, Bricker DE, Kramer AE, et al. The SWAL-QOL outcomes tool for oropharyngeal dysphagia in adults: I. Conceptual foundation and item development. Dysphagia. 2000;15:115–21.

    Article  PubMed  CAS  Google Scholar 

  54. 54.

    McHorney CA, Robbins J, Lomax K, et al. The SWAL-QOL and SWAL-CARE outcomes tool for oropharyngeal dysphagia in adults: III. Documentation of reliability and validity. Dysphagia. 2002;17:97–114.

    Article  PubMed  Google Scholar 

  55. 55.

    Chardhuri KR, Prieto-Jurcynska C, Naidu Y, et al. The nondeclaration of nonmotor symptomes of Parkinson’s disease to health care professionals: an international study using the nonmotor symptoms questionnaire. Mov Disord. 2010;25(6):704–9.

    Article  Google Scholar 

  56. 56.

    Boot JA, Chaudhuri KR. Oropharyngeal dysphagia in Parkinson’s disease: comments on paper by Kalf et al. Parkinsonism Relat Disord. 2013;19(2):275.

    Article  PubMed  CAS  Google Scholar 

  57. 57.

    Kalf JG, de Swart BJ, Munneke M, Bloem BR. Author reply to “Oropharyngeal dysphagia in Parkinson’s disease: comments on paper by Kalf et al.” by Boot and Chaudhuri. Parkinsonism Relat Disord. 2013;19(2):276.

    Article  PubMed  CAS  Google Scholar 

  58. 58.

    Fahn S, Elton R. Unified Parkinson’s disease rating scale. In: Fahn S, Marsden C, Calne D, Goldstein M, editors. Recent developments in Parkinson’s disease. Florham Park: Macmillan Healthcare Information; 1987. p. 153–63.

    Google Scholar 

  59. 59.

    Lam K, Lam FK, Lau KK, et al. Simple clinical tests may predict severe oropharyngeal dysphagia in Parkinson’s disease. Mov Disord. 2007;22(5):640–4.

    Article  PubMed  Google Scholar 

  60. 60.

    Norbrega AC, Rodriguez B, Melo A. Silent aspiration in Parkinson’s disease patients with diurnal sialorrhea. Clin Neurol Neurosurg. 2008;110(2):117–9.

    Article  Google Scholar 

  61. 61.

    Kalf H, de Swart B, Bonnier-Baars M, Hofman M, Kanters J, Kocken J, Miltenburg M, Bloem BR, Munneke M. Guidelines for speech-language therapy in Parkinson’s disease. Nijmegen, the Netherlands/Miami (FL), U.S.A.: ParkinsonNet/NPF. Originally published in Dutch as Logopedie bij de ziekte van Parkinson. Een richtlijn van de Nederlandse Vereniging voor Logopedie en Foniatrie; 2008.

  62. 62.

    Ertekin C, Aydogdu I, Yuceyar N, et al. Electrodiagnostic methods for neurogenic dysphagia. Electroencephalogr Clin Neurophysiol. 1998;109(4):331–40.

    Article  PubMed  CAS  Google Scholar 

  63. 63.

    Potulska A, Friedmann A, Krolicki L, et al. Swallowing disorders in Parkinson’s disease. Parkinsonism Relat Disord. 2003;9(6):349–53.

    Article  PubMed  Google Scholar 

  64. 64.

    Nathadwarawala KM, McGroary A, Wiles CM. Swallowing in neurological outpatients: use of a timed test. Dysphagia Spring. 1994;9(2):120–9.

    Article  CAS  Google Scholar 

  65. 65.

    Clarke CE, Gullaksen E, Macdonald S, Lowe F. Referral criteria for speech and language therapy assessement of dysphagia caused by idiopathic Parkinson’s disease. Acta Neurol Scand. 1998;97(1):27–35.

    Article  PubMed  CAS  Google Scholar 

  66. 66.

    Kanna SV, Bhanu K. A simple bedside test to assess the swallowing dysfunction in Parkinson’s disease. Ann Indian Neurol. 2014;17(1):62–5.

    Article  Google Scholar 

  67. 67.

    Carnaby-Mann G, Lenius K. The bedside examination in dysphagia. Phys Med Rehabil Clin N Am. 2008;19(4):747–68.

    Article  PubMed  Google Scholar 

  68. 68.

    Monte F, da Silva-Junior F, Braga-Neto P, Nobre e Sousa M, de Bruin V. Swallowing abnormalities and dyskinesia in Parkinson’s disease. Mov Disord. 2005;20(4):457–62.

    Article  PubMed  Google Scholar 

  69. 69.

    Langmore SE. Evaluation of oropharyngeal dysphagia: which diagnostic tool is superior? Curr Opin Otolaryngnol Head Neck Surg. 2003;11:485–9.

    Article  Google Scholar 

  70. 70.

    Warnecke T, Ringelstein EB, Dziewas R. Neurologische endoskopische Dysphagiediagnostik—Untersuchungstechnik, Einsatzmöglichkeiten und typische Befunde. Klin Neurophysiol. 2009;40:194–203.

    Article  Google Scholar 

  71. 71.

    Logemann JA. Evaluation and treatment of swallowing disorders. 2nd ed. Austin: Pro-Ed; 1998.

    Google Scholar 

  72. 72.

    Suttrup I, Suntrup S, Siemer ML, Bauer J, Hamacher C, Oelenberg S, Domagk D, Dziewas R, Warnecke T. Esophageal swallowing disorders in patients with different parkinsonian syndromes as detected by high resolution manometry. Dysphagia. 2014;29(1):121–81.

    Article  Google Scholar 

  73. 73.

    Warnecke T, Oelenberg S, Teismann I, Hamacher C, Lohmann H, Ringelstein RB, Dziewas R. Endoscopic characteristics and levodopa responsiveness of swallowing function in progressive supranuclear palsy. Mov Disord. 2010;25(9):1239–45.

    Article  PubMed  Google Scholar 

  74. 74.

    Pfeiffer RF. Gastrointestinal dysfunction in Parkinson’s disease. Parkinsonism Relat Disord. 2011;17(1):10–5.

    Article  PubMed  Google Scholar 

  75. 75.

    Castell JA, Johnston BT, Colcher A, Li Q, Gideon RM, Castell DO. Manometric abnormalities of the oesophagus in patients with Parkinson’s disease. Neurogastroenterol Motil. 2001;13(4):361–4.

    Article  PubMed  CAS  Google Scholar 

  76. 76.

    Hammer MJ, Murphy CA, Abrams TM. Airway somatosensory deficits and dysphagia in Parkinson’s disease. J Parkinsons Dis. 2013;3(1):39–44.

    PubMed Central  PubMed  Google Scholar 

  77. 77.

    Troche MS, Okun MS, Rosenbek JC, et al. Attentional resource allocation and swallowing safety in Parkinson’s disease: a duel task study. Parkinsonism Relat Disord. 2014;20(4):439–43.

    PubMed Central  Article  PubMed  Google Scholar 

  78. 78.

    Baijens L, Speyer R. Effects of therapy for dysphagia in Parkinson’s disease: a systematic review. Dysphagia. 2009;24(1):91–102.

    Article  PubMed  Google Scholar 

  79. 79.

    Van Hooren MR, Baijens LW, Vaskuilen S, Oosterloo M, Kremer B. Treatment effects for dysphagia in Parkinson’s disease: a systematic review. Parkinsonism Relat Disord. 2014;20(8):800–7.

    Article  PubMed  Google Scholar 

  80. 80.

    Troche MS, Okun MS, Rosenbek JC, et al. Aspiration and swallowing in Parkinson’s disease and rehabilitation with EMST: a randomized trial. Neurology. 2010;75(21):1912–9.

    PubMed Central  Article  PubMed  CAS  Google Scholar 

  81. 81.

    Troche MS, Rosenbek JC, Okun MS, Sapienza CM. Detraining outcomes with expiratory muscle strength training in Parkinson’s disease. J Rehabil Res Dev. 2014;51(2):305–10.

    PubMed Central  Article  PubMed  Google Scholar 

  82. 82.

    Manor Y, Mootanah R, Freud D, Giladi N, Cohen JT. Video-assisted swallowing therapy for patients with Parkinson’s disease. Parkinsonism Relat Disord. 2013;19(2):207–11.

    Article  PubMed  Google Scholar 

  83. 83.

    El Sharkawi A, Ramig L, Logemann AJ, et al. Swallowing and voice effects of lee silverman voice treatmend (LSVT): a pilot study. J Neurol Neurosurg Psychiatry. 2002;72(1):31–6.

    PubMed Central  Article  PubMed  Google Scholar 

  84. 84.

    Sutton JP. Dysphagia in Parkinson’s disease is responsive to levodopa. Parkinsonism Relat Disord. 2013;19(3):282–4.

    Article  PubMed  Google Scholar 

  85. 85.

    Chaudhuri KR, Healy DG, Schapira AH. Non-motor symptoms of Parkinson’s disease: diagnosis and management. Lancet Neurol. 2006;5(3):235–45.

    Article  PubMed  Google Scholar 

  86. 86.

    Jankovic J. Parkinson’s disease: clinical features and diagnosis. J Neurol Neurosurg Psychiatr. 2008;79(4):368–76.

    Article  PubMed  CAS  Google Scholar 

  87. 87.

    Suttrup I, Oelenberg S, Hamacher C, Dziewas R, Warnecke T. Endoscopic L-dopa-test for parkinsonian dysphagia (a pilot study). Dysphagia. 2011;26:482.

    Google Scholar 

  88. 88.

    Lim A, Leow L, Huckabee M, et al. A pilot study of respiration and swallowing integration in Parkinson’s disease: ‘on’ and ‘off’ levodopa. Dysphagia. 2008;23:76–81.

    Article  PubMed  Google Scholar 

  89. 89.

    Hirano M, Isono C, Sakamoto H, Ueno S, Kusunoki S, Nakamura Y. Rotigotine transdermal patch improves swallowing in dysphagic patients with Parkinson’s disesase. Dysphagia. 2015;30(4):452–6.

    Article  PubMed  Google Scholar 

  90. 90.

    Muller B, Assmus J, Larsen J, Haugarvoll K, Skeie G, Tysnes O. Autonomic symptoms and dopaminergic treatment in de novo Parkinson’s disease. Acta Neurol Scand. 2013;127(4):294.

    Article  CAS  Google Scholar 

  91. 91.

    Lengerer S, Kipping J, Rommel N, et al. Deep brain stimulation does not impair deglutition in Parkinson’s disease. Parkinsonism Relat Disord. 2012;18:847–53.

    Article  PubMed  Google Scholar 

  92. 92.

    Sunstedt S, Olofsson K, van Doorn J, et al. Swallowing function in Parkinson’s patients following zona incerta deep brain stimulation. Acta Neurol Scand. 2012;126:350–6.

    Article  Google Scholar 

  93. 93.

    Kulneff L, Sundstedt S, Olofsson K, et al. Deep brain stimulation-effects on swallowing function in Parkinson’s disease. Acta Neurol Scand. 2012;1:1–8.

    Google Scholar 

  94. 94.

    Silbergleit AK, Lewitt P, Junn F, et al. Comparison of dysphagia before and after deep brain stimulation in Parkinson’s disease. Mov Disord. 2012;27:1763–8.

    Article  PubMed  Google Scholar 

  95. 95.

    Troche MS, Brandimore A, Foote K, et al. Swallowing outcomes following unilateral STN vs. GPi surgery: a retrospective analysis. Dysphagia. 2014;29(4):425–31.

    PubMed Central  Article  PubMed  Google Scholar 

  96. 96.

    Ciucci MR, Brakmeier-Kraemer JM, Shermann SJ. Subthalamic nucleus deep brain stimulation improves deglutition in Parkinson’s disease. Mov Disord. 2008;23(5):676–83.

    Article  PubMed  Google Scholar 

  97. 97.

    Xie T, Vigil J, MacCracken E, et al. Low-frequency stimulation of STN-DBS reduces aspiration and freezing of gait in patients with PD. Neurology. 2015;84(4):415–20.

    PubMed Central  Article  PubMed  Google Scholar 

  98. 98.

    Derrey S, Chastan N, Maltete D, et al. Impact of deep brain stimulation on pharyngo-esophageal motility: a randomized cross-over study. Neurogastroenterol Motil. 2015;27:1214–22.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Tobias Warnecke.

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Suttrup, I., Warnecke, T. Dysphagia in Parkinson’s Disease. Dysphagia 31, 24–32 (2016). https://doi.org/10.1007/s00455-015-9671-9

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Keywords

  • Dysphagia
  • Parkinson’s disease
  • Swallowing
  • Treatment
  • Pathophysiology
  • Diagnosis