1,042
Views
4
CrossRef citations to date
0
Altmetric
Review

A comprehensive review of the diagnosis and treatment of Parkinson’s disease dysphagia and aspiration

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 411-424 | Received 24 Feb 2020, Accepted 12 May 2020, Published online: 11 Jul 2020

References

  • Mehanna R, Jankovic J. Respiratory problems in neurologic movement disorders. Parkinsonism Related Disord. 2010;16(10):628–638.
  • Kalf JG, de Swart BJM, Bloem BR, et al. Prevalence of oropharyngeal dysphagia in Parkinson’s disease: a meta-analysis. Parkinsonism Related Disord. 2012;18(4):311–315.
  • Ding X, Gao J, Xie C, et al. Prevalence and clinical correlation of dysphagia in Parkinson disease: A study on Chinese patients. Eur J Clin Nutr. 2018;72(1):82–86.
  • Fall PA, Saleh A, Fredrickson M, et al. Survival time, mortality, and cause of death in elderly patients with Parkinson’s disease: a 9-year follow-up. Mov Disord. 2003 Nov;18(11):1312–1316.
  • Mogensen PH, Jakobsen J. Causes of death in a community-based study of Parkinson’s disease. Acta Neurol Scand. 2001;103(1):7–11.
  • Marik PE. Aspiration pneumonitis and aspiration pneumonia. N Engl J Med. 2001;344(9):665–671.
  • Langmore SE, Terpenning MS, Schork A, et al. Predictors of aspiration pneumonia: how important is dysphagia? Dysphagia. 1998;13(2):69–81.
  • Yoneyama T, Yoshida M, Ohrui T, et al. Oral care reduces pneumonia in older patients in nursing homes. J Am Geriatr Soc. 2002;50(3):430–433.
  • Ortega O, Parra C, Zarcero S, et al. Oral health in older patients with oropharyngeal dysphagia. Age Ageing. 2014 Jan;43(1):132–137.
  • Manabe T, Teramoto S, Tamiya N, et al. Risk factors for aspiration pneumonia in older adults. PLoS One Internet]. 2015 Oct 7 [cited 2020 Feb 12];10(10):e0140060. Available from. http://www.ncbi.nlm.nih.gov/pubmed/26444916
  • Suttrup I, Warnecke T. Dysphagia in Parkinson’s disease. Dysphagia. 2016;31(1):24–32.
  • Troche MS, Schumann B, Brandimore AE, et al. Reflex Cough and disease duration as predictors of swallowing dysfunction in Parkinson’s disease. Dysphagia. 2016 Dec 1;31(6):757–764.
  • Fernandez HH, Lapane KL. Predictors of mortality among nursing home residents with a diagnosis of Parkinson’s disease. Med Sci Monit. 2002;8(4):CR624-8.
  • Melo A, Monteiro L. Swallowing improvement after levodopa treatment in idiopathic Parkinson’s disease: lack of evidence. Parkinsonism Related Disord. 2013;19(3):279–281.
  • Plowman-Prine EK, Sapienza CM, Okun MS, et al. The relationship between quality of life and swallowing in Parkinson’s disease. Mov Disord. 2009 Jul 15;24(9):1352–1358.
  • Sung HY, Kim JS, Lee KS, et al. The prevalence and patterns of pharyngoesophageal dysmotility in patients with early stage Parkinson’s disease. Mov Disord. 2010 Oct 30;25(14):2361–2368. Available from. Internet]. [cited 2020 Feb 13].
  • Durcan R, Wiblin L, Lawson RA, et al. Prevalence and duration of non-motor symptoms in prodromal Parkinson’s disease. Eur J Neurol. 2019 Jul 1;26(7):979–985. Available from. Internet]. [cited 2020 Feb 13];
  • Cereda E, Cilia R, Klersy C, et al. Swallowing disturbances in Parkinson’s disease: a multivariate analysis of contributing factors. Park Relat Disord. 2014 Dec 1;20(12):1382–1387.
  • Simons JA, Fietzek UM, Waldmann A, et al. Development and validation of a new screening questionnaire for dysphagia in early stages of Parkinson’s disease. Park Relat Disord. 2014;20(9):992–998.
  • Lam K, Lam FKY, Kwok KL, et al. Simple clinical tests may predict severe oropharyngeal dysphagia in Parkinson’s disease. Mov Disord. 2007 Apr 15;22(5):640–644.
  • Umemoto G, Furuya H. Management of dysphagia in patients with Parkinson’s disease and related disorders. Intern Med. Internet]. 2019 [cited 2019 Dec 7]; Available from: https://www.jstage.jst.go.jp/article/internalmedicine/advpub/0/advpub_2373-18/_article
  • Curtis JA, Molfenter S, Troche MS. Predictors of residue and airway invasion in parkinson’s disease. Dysphagia. 2019;1:3. Available from Internet]. [cited 2019 Dec 7];
  • Barbagelata E, Nicolini A, Tognetti P. Swallowing dysfunctions in Parkinson’s disease patients: a novel challenge for the internist. Ital J Med. 2019;13(2):91–94.
  • Simons JA. Swallowing dysfunctions in Parkinson’s disease. International Review of Neurobiology. Internet]. Nonmotor Parkinson’s: The Hidden Face. Academic Press; 2017 [cited 2019 Dec 6]. p. 1207–1238. Available from https://www.sciencedirect.com/science/article/pii/S0074774217300831?via%3Dihub.
  • Kwon M, Lee J-H. Oro-pharyngeal dysphagia in Parkinson’s disease and related movement disorders. Journal of Movement Disorders Internet]. 2019 [cited 2019 Dec 8]. Available from. ;12(3):152–160.
  • Finger ME, Madden LL, Haq IU, et al. Analysis of the prevalence and onset of dysphonia and dysphagia symptoms in movement disorders at an academic medical center. J Clin Neurosci. 2019 Jun;64(64):111–115.
  • Fabbri M, Coelho M, Abreu D, et al. Dysphagia predicts poor outcome in late-stage Parkinson’s disease. Park Relat Disord. 2019 Jul 1;64:73–81.
  • Suttrup I, Suttrup J, Suntrup-Krueger S, et al. Esophageal dysfunction in different stages of Parkinson’s disease. Neurogastroenterol Motil. 2017 Jan 1;29(1):e12915.
  • Lang IM. Brain stem control of the phases of swallowing. Dysphagia. 2009; Springer 24(3):333–348.
  • Pringsheim T, Jette N, Frolkis A, et al. The prevalence of Parkinson’s disease: a systematic review and meta-analysis. Available from Internet]. Mov Disord. 2014; Vol. 29(13): p. 1583–1590 [cited 2020 Jan 23].
  • Dorsey ER, Sherer T, Okun MS, et al. The emerging evidence of the Parkinson pandemic. J Parkinsons Dis. 2018;8(s1):S3–8. IOS Press.
  • Pflug C, Bihler M, Emich K, et al.2018 Feb 1; Critical dysphagia is common in Parkinson disease and occurs even in early stages: a prospective cohort study. Dysphagia. Available from Internet]. [cited 2019 Dec 8];33(1):41–50.
  • Miller N, Allcock L, Hildreth AJ, et al. Swallowing problems in Parkinson disease: frequency and clinical correlates. J Neurol Neurosurg Psychiatry. 2009;80(9):1047–1049.
  • Fujioka S, Fukae J, Ogura H, et al. Hospital-based study on emergency admission of patients with Parkinson’s disease. eNeurologicalSci. 2016 Sep 4;4:19–21.
  • Tomita S, Oeda T, Umemura A, et al. Video-fluoroscopic swallowing study scale for predicting aspiration pneumonia in Parkinson’s disease. PLoS One. 2018;13(6):e0197608.
  • Jones B. Normal and abnormal swallowing : imaging in diagnosis and therapy. New York, NY: Springer; 2003. p. 287.
  • Mu L, Sobotka S, Chen J, et al. Parkinson disease affects peripheral sensory nerves in the pharynx. J Neuropathol Exp Neurol. 2013 Jul;72(7):614–623.
  • Costa MMB. Neural control of swallowing. Arq Gastroenterol. IBEPEGE - Inst. Bras. Estudos Pesquisas Gastroent 2018;55(suppl 1):61–75.
  • Doty R. Neural organization of deglutition. Alimentary Canal. In: Handbook of physiology. American Physiological Society; 1968. p. 1861–1902.
  • Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiological Reviews Internet] 2001; 81(2):929–969. [cited 2020 Feb 7]. Available from. http://physrev.physiology.org
  • Jean A. Brainstem control of swallowing: localization and organization of the central pattern generator for swallowing. In: Neurophysiology of the Jaws and Teeth. London: Macmillan Education UK; 1990. p. 294–321.
  • Jean A, Kessler J-P TF. Nucleus tractus solitarii and deglutition: monoamines, excitatory amino acids and cellular properties. Barraco IRA. editor. Nucleus of the Solitary Tract [Internet]. 1st editor Boca Raton: CRC Press; 1994. p. 361–375. Available from https://www.taylorfrancis.com/books/9781000005950.
  • Jean A. brain stem control of swallowing. Neuronal Network Cell Mech. Vol. 81, Physiological Reviews. 2001. p. 929–69
  • Jean A, Dallaporta M. Electrophysiologic characterization of the swallowing pattern generator in the brainstem. GI Motil. 2006;9:1–37.
  • Jankovic J. Parkinson’s disease: clinical features and diagnosis. J Neurol Neurosurg Psychiatry. 2008;79(4):368–376.
  • van Hooren MRA, Baijens LWJ, Voskuilen S, et al. Treatment effects for dysphagia in Parkinson’s disease: a systematic review. Parkinsonism Related Disord. 2014; Elsevier Ltd 20(8):800–807.
  • Brabenec L, Mekyska J, Galaz Z, et al. Speech disorders in Parkinson’s disease: early diagnostics and effects of medication and brain stimulation. J Neural Transm. 2017 Mar;124(3):303–334.
  • Chaudhuri KR, Healy DG, Schapira AHV. Non-motor symptoms of Parkinson’s disease: diagnosis and management. Lancet Neurol. 2006;5(3):235–245.
  • Mu L, Sobotka S, Chen J, et al. Altered pharyngeal muscles in parkinson disease. J Neuropathol Exp Neurol. Internet]. 2012 Jun [cited 2020 Feb 19];71(6):520–530. Available from http://www.ncbi.nlm.nih.gov/pubmed/22588389.
  • Jones CA, Hoffman MR, Lin L, et al. Identification of swallowing disorders in early and mid-stage Parkinson’s disease using pattern recognition of pharyngeal high-resolution manometry data. Neurogastroenterol Motil. 2018;30(4):e13236.
  • Mu L, Sobotka S, Chen J, et al. Alpha-synuclein pathology and axonal degeneration of the peripheral motor nerves innervating pharyngeal muscles in Parkinson disease. J Neuropathol Exp Neurol. 2013;72(2):119–129.
  • Hunker CJ, Abbs JH, Barlow SM. The relationship between parkinsonian rigidity and hypokinesia in the orofacial system: a quantitative analysis. Neurology. 1982;32(7):749.
  • Baradaran N, Tan SN, Liu A, et al. Parkinson’s disease rigidity: relation to brain connectivity and motor performance. Front Neurol. 2013;4. Doi:10.3389/fneur.2013.00067.
  • Higo R, Tayama N, Watanabe T, et al. Abnormal elevation of resting pressure at the upper esophageal sphincter of Parkinson’s disease patients. Eur Arch Oto-Rhino-Laryngology. 2001;258(10):552–556.
  • Visanji NP, Marras C, Hazrati LN, et al. Alimentary, my dear Watson? The challenges of enteric α-synuclein as a Parkinson’s disease biomarker. Internet]. Vol. 29, Mov Disord. John Wiley and Sons Inc.; 2014 [cited 2020 Feb 19]. p. 444–450. Available from . ; . http://www.ncbi.nlm.nih.gov/pubmed/24375496 4:.
  • Fasano A, Visanji NP, Liu LWC, et al. Gastrointestinal dysfunction in Parkinson’s disease. Lancet Neurol. 2015;14(6):625–639. Lancet Publishing Group.
  • Umay E, Ozturk E, Gurcay E, et al. Swallowing in Parkinson’s disease: how is it affected? Clin Neurol Neurosurg Internet]. 2019 Feb 1 [cited 2019 Dec 7]; 177:37–41. Available from https://www.sciencedirect.com/science/article/pii/S0303846718304785.
  • Barrera MA, O’Connor Wells B. Presbyphagia versus Dysphagia: normal versus abnormal swallowing symptoms in older Adults with Parkinson disease and multiple sclerosis. Top Geriatr Rehabil. 2019;35(3):217–233.
  • Muhle P, Wirth R, Glahn J, et al. Age-related changes in swallowing: physiology and pathophysiology. Nervenarzt. 2015 Apr;86(4):440-451.
  • Daggett A, Logemann J, Rademaker A, et al. Laryngeal penetration during deglutition in normal subjects of various ages. Dysphagia. 2006.
  • Robbins J, Bridges AD, Taylor A. Oral, pharyngeal and esophageal motor function in aging. GI Motil Online. 2006;21(4):270–274.
  • Malandraki GA, Robbins JA. Effects of aging on the oral phase of deglutition. In: Principles of deglutition: a multidisciplinary text for swallowing and its disorders. New York, NY: Springer New York; 2013. p. 137-149.
  • Argolo N, Sampaio M, Pinho P, et al. Swallowing disorders in Parkinson’s disease: impact of lingual pumping. Int J Lang Commun Disord. Available from Internet] 2015 Sep;50(5):659–664. [cited 2020 Jan 23];
  • Umemoto G, Tsuboi Y, Kitashima A, et al. Impaired food transportation in parkinson’s disease related to lingual bradykinesia. Dysphagia Internet]. 2011 Sep [cited 2020 Feb 13];26(3):250–255. Available from http://www.ncbi.nlm.nih.gov/pubmed/20803220.
  • Wakasugi Y, Yamamoto T, Oda C, et al. Effect of an impaired oral stage on swallowing in patients with Parkinson’s disease. J Oral Rehabil. 2017 Oct 1;44(10):756–762.
  • Ali GN, Wallace KL, Schwartz R, et al. Mechanisms of oral-pharyngeal dysphagia in patients with Parkinson’s disease. Gastroenterology. 1996;110(2):383–392.
  • Pitts LL, Morales S, Stierwalt JAG. Lingual pressure as a clinical indicator of swallowing function in Parkinson’s disease. J Speech Lang Hear Res. 2018;61(2):257–265.
  • Minagi Y, Ono T, Hori K, et al. Relationships between dysphagia and tongue pressure during swallowing in Parkinson’s disease patients. J Oral Rehabil. 2018 Jun 1;45(6):459–466. Internet]. [cited 2020 Apr 9]; Available from..
  • Fukuoka T, Ono T, Hori K, et al. Tongue pressure measurement and videofluoroscopic study of swallowing in Patients with Parkinson’s disease. Dysphagia. 2019 Feb 15;34(1):80–88. Internet]. [cited 2020 Apr 9]; Available from.
  • Curtis JA, Molfenter SM, Troche MS. Pharyngeal area changes in Parkinson’s disease and its effect on swallowing safety, efficiency, and kinematics. Dysphagia. 2020;35(2):389–398.
  • Gaeckle M, Domahs F, Kartmann A, et al. Predictors of penetration-aspiration in Parkinson’s disease patients with Dysphagia: a retrospective analysis. Ann Otol Rhinol Laryngol. 2019;128(8):728–735.
  • Hegland KW, Okun MS, Troche MS. Sequential voluntary cough and aspiration or aspiration risk in Parkinson’s disease. Lung. 2014;192(4):601–608.
  • Silverman EP, Carnaby G, Singletary F, et al. Measurement of voluntary cough production and airway protection in parkinson disease. Arch Phys Med Rehabil. 2016;97(3):413–420.
  • Gross RD, Atwood CW, Ross SB, et al. The coordination of breathing and swallowing in Parkinson’s disease. Dysphagia Internet] 2008 Jun [cited 2020 Feb 19];23(2):136–145. Available from http://www.ncbi.nlm.nih.gov/pubmed/18027027.
  • Schröder JB, Marian T, Claus I, et al. Substance P saliva reduction predicts pharyngeal dysphagia in Parkinson’s disease. Front Neurol Internet]. 2019 Apr 16 [cited 2020 Jan 25];10. Available from https://www.frontiersin.org/article/10.3389/fneur.2019.00386/full
  • Renner B, Ahne G, Grosan E, et al. Tonic stimulation of the pharyngeal mucosa causes pain and a reversible increase of inflammatory mediators. Inflamm Res. 2013;62(12):1045–1051.
  • Imoto Y, Koji MAA, Osawa Y, et al. Cough reflex induced by capsaicin inhalation in patients with dysphagia. Acta Otolaryngol. 2010;131(1):96–100.
  • Niel JP. [Role of substance P in the nervous system control of digestive motility]. Arch Int Physiol Biochim Biophys. 1991 Sep;99(5):A65-76. DOI: 10.3109/13813459109145918.
  • Kooi AHJ, Boo JPL, Ng SYE, et al. The modified Barium swallow impairment profile as a predictor of clinical outcomes of admission for pneumonia or choking in dysphagic patients with Parkinson’s disease. Dysphagia. 2019 Dec 1;34(6):896–903.
  • Bassotti G, Germani U, Pagliaricci S, et al. Esophageal manometric abnormalities in Parkinson’s disease. Dysphagia. 1998;13(1):28–31.
  • Langmore SE, Kenneth SMA, Olsen N. Fiberoptic endoscopic examination of swallowing safety: a new procedure. Dysphagia. 1988 Dec;2(4):216–219.
  • 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(3):115–121.
  • McHorney CA, Earl Bricker D, Robbins J, et al. The SWAL-QOL outcomes tool for oropharyngeal dysphagia in adults: II. Item reduction and preliminary scaling. Dysphagia. 2000;15(3):122–133.
  • McHorney CA, Robbins JA, 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 Mar;17(2):97–114.
  • Belafsky PC, Mouadeb DA, Rees CJ, et al. Validity and reliability of the eating assessment tool (EAT-10). Ann Otol Rhinol Laryngol. 2008;117(12):919–924.
  • Nativ-Zeltzer N, Bayoumi A, Mandin VP, et al. Validation of the PILL-5: a 5-item patient reported outcome measure for pill dysphagia. Front Surg. 2019;6. Doi:10.3389/fsurg.2019.00043.
  • Manor Y, Giladi N, Cohen A, et al. Validation of a swallowing disturbance questionnaire for detecting dysphagia in patients with Parkinson’s disease. Mov Disord. 2007 Oct 15;22(13):1917–1921.
  • Buhmann C, Bihler M, Emich K, et al. Pill swallowing in Parkinson’s disease: a prospective study based on flexible endoscopic evaluation of swallowing. Park Relat Disord. 2019 May 1;62:51–56.
  • Ott DJ, Hodge RG, Pikna LA, et al. Modified barium swallowclinical and radiographic correlation and relation to feeding recommendations. Dysphagia. 1996;11(3):187–190.
  • Langmore SE, Logemann JA. After the clinical bedside swallowing examination. Am J Speech-Language Pathol. 1991;1(1):13–20.
  • McCullough GH, Martino R. Clinical evaluation of patients with dysphagia: importance of history taking and physical exam. In: Manual of diagnostic and therapeutic techniques for disorders of Deglutition. New York, NY: Springer New York; 2013. p.11-30.
  • Kalf H, De Swart B, Bonnier-Baars M, et al. Guidelines for speech-language therapy in Parkinson’s disease. 2008. cited 2020 Jan 25. Internet] Available from www.ParkinsonNet.nl
  • Ertekin C, Aydogdu I, Yüceyar N, et al. Electrodiagnostic methods for neurogenic dysphagia. Electroencephalogr Clin Neurophysiol - Electromyogr Mot Control. 1998;109(4):331–340..
  • Potulska A, Friedman A, Królicki L, et al. Swallowing disorders in Parkinson’s disease. Park Relat Disord. 2003;9(6):349–353.
  • Nathadwarawala KM, McGroary A, Wiles CM. Swallowing in neurological outpatients: use of a timed test. Dysphagia. 1994;9(2):120–129.
  • Brodsky MB, Suiter DM, González-Fernández M, et al. Screening accuracy for aspiration using bedside water swallow tests: a systematic review and meta-analysis. Chest. 2016;150(1):148–163.
  • Mulheren RW, Azola A, González-Fernández M. Do ratings of swallowing function differ by videofluoroscopic rate? An exploratory analysis in patients after acute stroke. Arch Phys Med Rehabil Internet]. 2019 Jun 1 [cited 2020 Feb 7];100(6):1085–1090. Available from http://www.ncbi.nlm.nih.gov/pubmed/30452891
  • Bonilha HS, Blair J, Carnes B, et al. Preliminary investigation of the effect of pulse rate on judgments of swallowing impairment and treatment recommendations. Dysphagia. Internet]. 2013 Dec [cited 2020 Feb 7];28(4):528–538. Available from http://www.ncbi.nlm.nih.gov/pubmed/23559454.
  • Martin-Harris B, Jones B. The videofluorographic swallowing study. Phys Med Rehabil Clin N Am. 2008;19(4):769–785.
  • Langmore SE. History of Fiberoptic Endoscopic evaluation of swallowing for evaluation and management of pharyngeal dysphagia: changes over the years. Dysphagia. 2017;32(1):27–38. Springer New York LLC.
  • Rosenbek JC, Robbins JA, Roecker EB, et al. A penetration-aspiration scale. Dysphagia. 1996;11(2):93–98.
  • Pearson WG, Molfenter SM, Smith ZM, et al. Image-based measurement of post-swallow residue: the normalized residue ratio scale. Dysphagia. 2013;28(2):167–177.
  • Dyer JC, Leslie P, Drinnan MJ. Objective computer-based assessment of valleculae residue - Is it useful? Dysphagia. 2008;23(1):7–15.
  • Rommel N, Borgers C, Van Beckevoort D, et al. Bolus Residue Scale: an easy-to-use and reliable videofluoroscopic analysis tool to score bolus residue in patients with dysphagia. Int J Otolaryngol. 2015;2015:1–7.
  • Neubauer PD, Rademaker AW, Leder SB. The Yale Pharyngeal Residue Severity Rating Scale: an anatomically defined and image-based tool. Dysphagia. 2015;30(5):521–528.
  • Martin-Harris B, Brodsky MB, Michel Y, et al. MBS measurement tool for swallow impairment-MBSimp: establishing a standard. Dysphagia. 2008;23(4):392–405.
  • Ertekin C. Electrophysiological evaluation of oropharyngeal dysphagia in Parkinson’s disease. J Mov Disord. 2014 Oct 30;7(2):31–56.
  • Monteiro L, Souza-Machado A, Pinho P, et al. Swallowing impairment and pulmonary dysfunction in Parkinson’s disease: the silent threats. J Neurol Sci. 2014 Apr 15;339(1–2):149–152.
  • Oh DH, Park JS, Kim WJ. Effect of neuromuscular electrical stimulation on lip strength and closure function in patients with dysphagia after stroke. J Phys Ther Sci. 2017;29(11):1974–1975.
  • Hsiao M-Y, Karunia Wahyuni L, Wang T-G. Ultrasonography in assessing oropharyngeal dysphagia. J Med Ultrasound. 2013. 21(4):181–188. Available from [cited 2020 Jan 27].
  • Tjaden K. Speech and swallowing in Parkinson’s disease. Top Geriatric Rehabil. 2008;24(2):115–126.
  • Ra JY, Hyun JK, Ko KR, et al. Chin tuck for prevention of aspiration: effectiveness and appropriate posture. Dysphagia. 2014 Sep 28;29(5):603–609.
  • Rosenbek JC, Jones HN. Dysphagia in movement disorders. Plural Pub; 2009. p. 265.
  • Ryu JS, Park D, Oh Y, et al. The effects of bolus volume and texture on pharyngeal pressure events using high-resolution manometry and its comparison with videofluoroscopic swallowing study. J Neurogastroenterol Motil. 2016;22(2):231–239.
  • Park JW, Sim GJ, Yang DC, et al. Increased bolus volume effect on delayed pharyngeal swallowing response in post-stroke oropharyngeal dysphagia: a pilot study. Ann Rehabil Med. 2016;40(6):1018..
  • Bisch EM, Logemann JA, Rademaker AW, et al. Pharyngeal effects of bolus volume, viscosity, and temperature in patients with dysphagia resulting from neurologic impairment and in normal subjects. J Speech Hear Res. 1994;37(5):1041–1049.
  • Butler SG, Stuart A, Markley L, et al. Aspiration as a function of age, sex, liquid type, bolus volume, and bolus delivery across the healthy adult life span. Ann Otol Rhinol Laryngol. 2018;127(1):21–32.
  • Troche MS, Okun MS, Rosenbek JC, et al. Attentional resource allocation and swallowing safety in Parkinson’s disease: a dual task study. Park Relat Disord. 2014;20(4):439–443.
  • Logemann JA. The evaluation and treatment of swallowing disorders. Curr Opin Otolaryngol Head Neck Surg. 1998; Lippincott Williams and Wilkins 6(6):395–400.
  • Clavé P, De Kraa M, Arreola V, et al. The effect of bolus viscosity on swallowing function in neurogenic dysphagia. Aliment Pharmacol Ther. 2006;24(9):1385–1394.
  • Cola PC, Gatto AR, Da Silva RG, et al. The influence of sour taste and cold temperature in pharyngeal transit duration in patients with stroke. Arq Gastroenterol. 2010;47(1):18–21.
  • Gatto AR, Cola PC, Da Silva RG, et al. Sour taste and cold temperature in the oral phase of swallowing in patients after stroke. CODAS. 2013;25(2):163–167.
  • Logemann JA, Pauloski BR, Colangelo L, et al. Effects of a sour bolus on oropharyngeal swallowing measures in patients with neurogenic dysphagia. J Speech Hear Res. 1995;38(3):556–563.
  • Logemann JA, Gensler G, Robbins JA, et al. A randomized study of three interventions for aspiration of thin liquids in patients with dementia or Parkinson’s disease. J Speech Lang Hear Res. 2008;51(1):173–183.
  • Gillman A, Winkler R, Taylor NF. Implementing the Free Water Protocol does not result in aspiration pneumonia in carefully selected patients with dysphagia: a systematic review. Dysphagia. 2017 Jun 1;32(3):345–361.
  • Panther K. The Frazier Free Water Protocol. Perspect swallowing swallowing disorders. Dysphagia. 2005 Mar 1;14(1):4.
  • Roche V. Percutaneous endoscopic gastrostomy. Clinical care of PEG tubes in older adults. Geriatrics. 2003 Nov [cited 2020 Jan 28];58(11):22–6. Internet] Available from http://www.ncbi.nlm.nih.gov/pubmed/14628393
  • Loeb M, McGeer A, McArthur M, et al. Risk factors for pneumonia and other lower respiratory tract infections in elderly residents of long-term care facilities. Arch Intern Med. 1999 Sep 27;159(17):2058–2064.
  • Opilla M. Aspiration risk and enteral feeding: a clinical approach. Pract Gastroenterol. 2003 Apr;1(27):89–96.
  • Marik PE, Kaplan D. Aspiration pneumonia and dysphagia in the elderly. Chest. 2003; American College of Chest Physicians 124(1):328–336.
  • Ciocon JO, Silverstone FA, Graver LM, et al. Tube feedings in elderly patients: indications, benefits, and complications. Arch Intern Med. 1988;148(2):429–433.
  • Koch KA. Patient Self-Determination Act. J Fla Med Assoc. 1992 Apr [cited 2020 Jan 27];79(4):240–243. Internet] Available from http://www.ncbi.nlm.nih.gov/pubmed/1588296.
  • Pitts T, Bolser D, Rosenbek J, et al. Impact of expiratory muscle strength training on voluntary cough and swallow function in Parkinson disease. Chest. 2009 May 1;135(5):1301–1308.
  • Sapienza C, Wheeler K. Respiratory muscle strength training: functional outcomes versus plasticity. Semin Speech Lang Internet]. 2006 Nov 27(4):236–244. [cited 2020 Jan 2727]; Available from http://www.thieme-connect.de/DOI/DOI?10.1055/s-2006-955114
  • Saleem AF, Sapienza CM, Okun MS. Respiratory muscle strength training: treatment and response duration in a patient with early idiopathic Parkinson’s disease. NeuroRehabilitation. 2005;20(4):323–333.
  • Troche MS, Okun MS, Rosenbek JC, et al. Aspiration and swallowing in Parkinson disease and rehabilitation with EMST: a randomized trial. Neurology. 2010 Nov 23;75(21):1912–1919.
  • Hegland KW, Davenport PW, Brandimore AE, et al. Rehabilitation of swallowing and cough functions following stroke: an expiratory muscle strength training trial. Arch Phys Med Rehabil. 2016;97(8):1345–1351.
  • Miles A, Jardine M, Johnston F, et al. Effect of Lee Silverman voice treatment (LSVT LOUD®) on swallowing and cough in Parkinson’s disease: a pilot study. J Neurol Sci. 2017 Dec 15;383:180–187.
  • Pitts T, Bolser D, Rosenbek J, et al. Impact of expiratory muscle strength training on voluntary cough and swallow function in Parkinson disease. Chest. 2009 May;135(5):1301–1308.
  • Wheeler-Hegland KM, Rosenbek JC, Sapienza CM. Submental sEMG and hyoid movement during Mendelsohn maneuver, effortful swallow, and expiratory muscle strength training. J Speech Lang Hear Res. 2008 Oct 1;51(5):1072–1087.
  • Ramig LO, Fox C, Sapir S. Speech treatment for Parkinson’s disease. Expert Rev Neurother. 2008;8(2):297–309.
  • Ramig LO, Sapir S, Countryman S, et al. Intensive voice treatment (LSVT®) for patients with Parkinson’s disease: A 2 year follow up. J Neurol Neurosurg Psychiatry. 2001 Oct;71(4):493–498..
  • Sapir S, Spielman JL, Ramig LO, et al. Effects of intensive voice treatment (the Lee Silverman Voice Treatment [LSVT]) on vowel articulation in dysarthric individuals with idiopathic Parkinson disease: acoustic and perceptual findings. J Speech Lang Hear Res. 2007 Aug 1;50(4):899–912.
  • El Sharkawi A, Ramig L, Logemann JA, et al. Swallowing and voice effects of Lee Silverman voice treatment (LSVT®): a pilot study. J Neurol Neurosurg Psychiatry. 2002;72(1):31–36.
  • Miles A, Jardine M, Johnston F, et al. Effect of Lee Silverman voice treatment (LSVT LOUD®) on swallowing and cough in Parkinson’s disease: a pilot study. J Neurol Sci. 2017 Dec;383:180–187.
  • Crary MA, Carnaby GD, Groher ME, et al. Functional benefits of dysphagia therapy using adjunctive sEMG biofeedback. Dysphagia. 2004;19(3). 10.1007/s00455-004-0003-8
  • Park JS, Hwang NK, Kim HH, et al. Effect of neuromuscular electrical stimulation combined with effortful swallowing using electromyographic biofeedback on oropharyngeal swallowing function in stroke patients with dysphagia: a pilot study. Medicine (Baltimore). 2019;98(44):e17702.
  • Hind JA, Nicosia MA, Roecker EB, et al. Comparison of effortful and noneffortful swallows in healthy middle-aged and older adults. Arch Phys Med Rehabil. 2001;82(12):1661–1665.
  • Wheeler-Hegland KM, Rosenbek JC, Sapienza CM. Submental sEMG and hyoid movement during Mendelsohn maneuver, effortful swallow, and expiratory muscle strength training. J Speech Lang Hear Res. 2008 Oct;51(5):1072–1087.
  • Logemann JA. The evaluation and treatment of swallowing disorders. Vol. 6, Current Opinion in Otolaryngology and Head and Neck Surgery. Lippincott Williams and Wilkins; 1998. p. 395–400.
  • McCullough GH, Kim Y. Effects of the Mendelsohn maneuver on extent of hyoid movement and UES opening post-stroke. Dysphagia. 2013 Dec;28(4):511–519.
  • McCullough GH, Kamarunas E, Mann GC, et al. Effects of Mendelsohn maneuver on measures of swallowing duration post stroke. Top Stroke Rehabil. 2012 Jan 1;19(3):234–243.
  • Miloro KV, Pearson WG, Langmore SE. Effortful pitch glide: a potential new exercise evaluated by dynamic MRI. J Speech Lang Hear Res. 2014;57(4):1243–1250.
  • Logemann JA, Pauloski BR, Rademaker AW, et al. Speech and swallowing rehabilitation for head and neck cancer patients. Oncology. 1997;11(5):651–659.
  • Baijens LWJ, Speyer R, Passos VL, et al. The effect of surface electrical stimulation on swallowing in dysphagic parkinson patients. Dysphagia. 2012;27(4):528–537.
  • Chen YW, Chang KH, Chen HC, et al. The effects of surface neuromuscular electrical stimulation on post-stroke dysphagia: a systemic review and meta-analysis. Clin Rehabil. 2016;30(1):24–35.
  • Sun Y, Chen X, Qiao J, et al. .Effects of transcutaneous neuromuscular electrical stimulation on swallowing disorders: a systematic review and meta-analysis. Am J Phys Med Rehabil. 2020:1. Publish Ah. Doi:10.1097/PHM.0000000000001397.
  • Park JS, Oh DH, Hwang NK, et al. Effects of neuromuscular electrical stimulation in patients with Parkinson’s disease and dysphagia: a randomized, single-blind, placebo-controlled trial. NeuroRehabilitation. 2018;42(4):457–463.
  • Kieser J, Jones G, Borlase G, et al. Dental treatment of patients with neurodegenerative disease. N Z Dent J. 1999;95(422):130–134.
  • Cersósimo MG, Perandones C, Micheli FE, et al. Alpha-synuclein immunoreactivity in minor salivary gland biopsies of Parkinson’s disease Patients. Mov Disord. 2011 Jan;26(1):188–190. Available from Internet]. [cited 2020 Jan 27];
  • Barbe AG, Bock N, Derman SHM, et al. Self-assessment of oral health, dental health care and oral health-related quality of life among Parkinson’s disease Patients. Gerodontology. 2017 Mar;341:135–143. Available from Internet]. [cited 2020 Jan 27];
  • Proulx M, de Courval FP, Wiseman MA, et al. Salivary production in Parkinson’s disease. Mov Disord. 2005 Feb;20(2):204–207.
  • Srivanitchapoom P, Pandey S, Hallett M. Drooling in Parkinson’s disease: a review. Parkinsonism Related Disord. 2014;20(11):1109–1118.
  • Dogu O, Apaydin D, Sevim S, et al. Ultrasound-guided versus “blind” intraparotid injections of botulinum toxin-A for the treatment of sialorrhoea in patients with Parkinson’s disease. Clin Neurol Neurosurg. 2004 Mar 1;106(2):93–96.
  • Lagalla G, Millevolte M, Capecci M, et al., Botulinum toxin type A for drooling in Parkinson’s disease: a double-blind, randomized, placebo-controlled study. Mov Disord. 2006 May 1; 21(5): 704–707. Available from Internet]. [cited 2020 Feb 13];
  • Seppi K, Weintraub D, Coelho M, et al.2011 Oct 1;The Movement Disorder Society Evidence-based Medicine Review Update: treatments for the non-motor symptoms of Parkinson’s disease. Mov Disord. Available from. Internet]. [cited 2020 Feb 13];26(S3):S42–80.
  • Srivanitchapoom P, Pandey S, Hallett M. Drooling in Parkinson’s disease: a review. Parkinsonism Related Disord. 2014; Elsevier Ltd 20(11):1109–1118.
  • Jost WH, Friedman A, Michel O, et al. SIAXI: placebo-controlled, randomized, double-blind study of incobotulinumtoxin A for sialorrhea. Neurology. 2019 Apr 23;92(17):E1982–91.
  • Accessdata.fda.gov [Internet]. Maryland: FDA.; 2000 [ updated 2019 Aug; cited 2020 Apr 1]. Available from https://www.accessdata.fda.gov/drugsatfda_docs/label/2018/125360s073lbl.pdf.
  • Accessdata.fda.gov [Internet]. Maryland: FDA.; 2010 [ updated 2019 July; cited 2020 Apr 1]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2018/125360s073lbl.pdf.173.
  • Jolly DE, Paulson RB, Paulson GW, et al. Parkinson’s disease: a review and recommendations for dental management. Spec Care Dent. 1989 May;93:74–78. Available from Internet]. [cited 2020 Jan 27];
  • Johnston BT, Li Q, Castell JA, et al. Swallowing and esophageal function in Parkinson’s disease. Am J Gastroenterol Internet] 1995 Oct [cited 2020 Jan 27];90(10):1741–1746. Available from http://www.ncbi.nlm.nih.gov/pubmed/7572887
  • Einarsdóttir ER, Gunnsteinsdóttir H, Hallsdóttir MH, et al. Dental health of patients with Parkinson’s disease in Iceland. Spec Care Dent. Internet] 2009 May [cited 2020 Jan 27];29(3):123–127. Available from
  • Fukayo S, Nonaka K, Shimizu T, et al. Oral health of patients with Parkinson’s disease: factors related to their better dental status. Tohoku J Exp Med. 2003 Nov;201(3):171–179.
  • Friedlander AH, Mahler M, Norman KM, et al. Parkinson disease: Parkinson disease systemic and orofacial manifestations, medical and dental management. J Am Dent Assoc. 2009;140(6):658–669.
  • Baijens LWJ, Speyer R. Effects of therapy for dysphagia in Parkinson’s disease: systematic review. Dysphagia. 2009;24(1):91–102.
  • Tada A, Miura H. Prevention of aspiration pneumonia (AP) with oral care. Arch Gerontol Geriatr. 2012;55(1):16–21.
  • Yoneyama T, Yoshida M, Matsui T, et al. Oral care and pneumonia. Lancet. 1999;354(9177):515. 8.
  • Adachi M, Ishihara K, Abe S, et al. Professional oral health care by dental hygienists reduced respiratory infections in elderly persons requiring nursing care. Int J Dent Hyg. 2007;5(2):69–74.
  • Bassim CW, Gibson G, Ward T, et al. Modification of the risk of mortality from pneumonia with oral hygiene care. J Am Geriatr Soc. 2008;56(9):1601–1607.
  • Sutton JP. Dysphagia in Parkinson’s disease is responsive to levodopa. Park Relat Disord. 2013;19(3):282–284.
  • Lim A, Leow LP, Huckabee ML, et al. A pilot study of respiration and swallowing integration in Parkinson’s disease: “On” and “Off” levodopa. Dysphagia. 2008 Mar;23(1):76–81.
  • Warnecke T, Suttrup I, Schröder JB, et al. Levodopa responsiveness of dysphagia in advanced Parkinson’s disease and reliability testing of the FEES-Levodopa-test. Park Relat Disord. 2016 Jul 1;28:100–106..
  • Johnston BT, Li Q, Castell JA, et al. Swallowing and esophageal function in Parkinson’s disease. Am J Gastroenterol. 1995 Oct;90(10):1741–1746.
  • Tison F, Wiart L, Guatterie M, et al. Effects of central dopaminergic stimulation by apomorphine on swallowing disorders in Parkinson’s disease. Mov Disord. 1996;11(6):729–732..
  • Monte FS, da Silva FP, Braga-Neto P, et al. Swallowing abnormalities and dyskinesia in Parkinson’s disease. Mov Disord. 2005 Apr;20(4):457–462.
  • Troche MS, Brandimore AE, Foote KD, et al. Swallowing and deep brain stimulation in Parkinson’s disease: A systematic review. Parkinsonism Related Disord. 2013;19(9):783–788.
  • Troche MS, Brandimore AE, Foote KD, et al. Swallowing outcomes following unilateral STN vs. GPi surgery: A retrospective analysis. Dysphagia. 2014;29(4):425–431.
  • 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):415–420..
  • Kim MK, Kantarcigil C, Kim B, et al. Flexible submental sensor patch with remote monitoring controls for management of oropharyngeal swallowing disorders. Sci Adv. 2019 Dec 13;5(12):eaay3210.
  • Manabe T, Teramoto S, Tamiya N, et al. Risk factors for aspiration pneumonia in older adults. PLoS One. 2015 Oct;10(10):e0140060.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.