Abstract
Oropharyngeal dysphagia frequently presents in people with idiopathic Parkinson’s disease (IPD). Clinical sequelae of dysphagia in this group include weight loss and aspiration pneumonia, the latter of which is the leading cause of hospital admissions and death in IPD. Thermal–tactile stimulation (TTS) is a sensory technique whereby stimulation is provided to the anterior faucial pillars to speed up the pharyngeal swallow. The effects of TTS on swallowing have not yet been investigated in IPD. The aim of this study was to investigate the immediate effects of TTS on the timing of swallow in a cohort of people with IPD and known oropharyngeal dysphagia. Thirteen participants with IPD and known dysphagia attended for videofluoroscopy during which standardised volumes of liquid barium and barium paste were administered preceding and immediately subsequent to TTS. The immediate effects of TTS on swallowing were examined using oral, pharyngeal, and total transit times and pharyngeal delay times as outcome measures. TTS significantly reduced median pharyngeal transit time on fluids (0.20 s, 95% CI = 0.12–0.28, p = 0.004) and on paste (0.3 s, 95% CI = 0.08–0.66, p = 0.01). Median total transit time was also reduced on fluids (0.48 s, 95% CI = 0.00–1.17, p = 0.049) and on paste (0.52 s, 95% CI = 0.08–1.46, p = 0.033). Median pharyngeal delay time was reduced on fluids (0.20 s, 95% CI = 0.12–0.34, p = 0.002). TTS did not significantly alter median oral transit time on either fluid or paste consistency. TTS significantly reduced temporal measures of the pharyngeal phase of swallowing in the IPD population. Significant results may be attributed to the role of sensory stimulation in improving motor function in IPD, with emphasis on the impaired glossopharyngeal and vagus nerves in this population. It is still unclear whether these findings will translate into a clinically beneficial effect.
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Bradley W, Daroff R, Fenichel G, Jankovic J. Neurology in clinical practice. 4th ed. Philadelphia: Butterworth Heinemann; 2004.
Fearnley J, Lees AJ. Pathology of Parkinson’s disease. In: Calne DB, editor. Neurodegenerative diseases. Philadelphia: Saunders; 1991. p. 545–54.
Koller WC. When does Parkinson’s disease begin? Neurology. 1992;42:27–31.
Braak H, Del Tredici K, Rub U, De Vos RA, Cansen Steur EN, Braak E. Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging. 2003;24:197–211.
Damier P, Hirsch EC, Agid Y, Graybiel AM. The substantia nigra of the human brain. II. Patterns of loss of dopaminergic neurons in Parkinson’s disease. Brain. 1999;122:1437–48.
Gibb WRG. Neuropathology of the substantia nigra. Eur Neurol. 1991;31:48–59.
Gibb WRG, Lees AJ. Anatomy, pigmentation, ventral and dorsal subpopulations of the substantia nigra, and differential cell death in Parkinson’s disease. J Neurol Neurosurg Psychiatry. 1991;54:388–96.
de Vos RAI, Jansen Steur ENH, Yilmazer D, Braak H, Braak E. Pathological and clinical features of Parkinson’s disease with and without dementia. In: Perry RH, McKeith IG, Perry EK, editors. Dementia with Lewy bodies. New York: Cambridge University Press; 1996. p. 255–67.
Braak H, Braak E. Pathoanatomy of Parkinson’s disease. J Neurol. 2000;247:3–10.
Braak H, Rüb U, Sandmann-Keil D, Gai WP, de Vos R, Jansen Steur E, et al. Parkinson’s disease: affection of brain stem nuclei controlling premotor and motor neurons of the somatomotor system. Acta Neuropathol. 2000;99:489–95.
Jellinger K. Pathology of Parkinson’s disease. Changes other than the nigrostriatal pathway. Mol Chem Neuropathol. 1991;14:153–97.
Pitts T, Bolser D, Rosenbek J, Troche M, Sapienza C. Voluntary cough production and swallow dysfunction in Parkinson’s disease. Dysphagia. 2008;23:221–340.
Nilsson H, Ekberg O, Olsson R, Hindfelt B. Quantitative assessment of oral and pharyngeal function in Parkinson’s disease. Dysphagia. 1996;11:144–50.
Bushmann M, Domeyer SM, Leeker L, Perlmutter JS. Swallowing abnormalities and their response to treatment in Parkinson’s disease. Neurology. 1989;39:1309–14.
Robbins J, Logemann JA, Kirshner HS. Swallowing and speech production in Parkinson’s disease. Ann Neurol. 1986;19:283–7.
Reilly S, Douglas J, Oates J. Evidence based practice in speech pathology. 2nd ed. London: Whurr; 2003.
Edwards LL, Pfeiffer RE, Quigley EM, Horman R, Balluf M. Gastrointestinal symptoms in Parkinson’s disease. Mov Disord. 1991;6:151–6.
Calne DB, Shaw DG, Spiers AS, Stern GM. Swallowing in Parkinsonism. Br J Radiol. 1970;43:456–7.
Volonte MA, Porta M, Comi G. Clinical assessment of dysphagia in early phases of Parkinson’s disease. Neurol Sci. 2002;23:S121–2.
Clarke CE, Gullaksen E, Macdonald S, Lowe F. Referral criteria for speech and language therapy assessment of dysphagia caused by idiopathic Parkinson’s disease. Acta Neurol Scand. 1998;97:27–35.
Ali GN, Wallace KL, Schwartz R, De Carle DJ, Zagami AS, Cook IJ. Mechanisms of oral-pharyngeal dysphagia in patients with Parkinson’s disease. Gastroenterology. 1996;110:383–92.
Logemann JA. Evaluation and treatment of swallowing disorders. 2nd ed. Austin: Pro-Ed; 1998.
Donner MW. Swallowing mechanism and neuromuscular disorders. Semin Roentgenol. 1974;9:273–82.
Blonsky ER, Logemann JA, Boshes B, Fischer HB. Comparison of speech and swallowing function in patients with tremor disorders and in normal geriatric patients: a cinefluorographic study. J Gerontol. 1975;30:299–330.
Leopold NA, Kagel MC. Laryngeal deglutition movement in Parkinson’s disease. Neurology. 1997;48:373–6.
Wintzen AR, Badrising UA, Roos R, Vielvoye J, Liauw L, Pauwels EK. Dysphagia in ambulant patients with Parkinson’s disease: common, not dangerous. Can J Neurol Sci. 1994;21:53–6.
Eadie MJ, Tyrer JH. Alimentary disorders in Parkinsonism. Australas Ann Med. 1965;14:13–22.
Nagaya M, Kachi T, Yamada T, Igata I. Videofluorographic study of swallowing in Parkinson’s disease. Dysphagia. 1998;13:95–100.
Stroudley J, Walshe M. Radiological assessment of dysphagia in Parkinson’s disease. Br J Radiol. 1991;64:890–3.
Woodford HJ, Walker RW. Emergency hospital admissions in idiopathic Parkinson’s disease. Mov Disord. 2005;20:1104–8.
Tan LC, Tan AK, Tjia HT. The profile of hospitalised patients with Parkinson’s disease. Ann Acad Med Singapore. 1998;27:808–12.
Bachmann G, Trenkwalder C. Body weight in patients with Parkinson’s disease. Mov Disord. 2006;21:1824–30.
Miller N, Noble E, Jones D, Burn D. Hard to swallow: dysphagia in Parkinson’s disease. Age Ageing. 2006;35:614–8.
Okun M, Stover N, Subramanian T, Gearing M, Wainer B, Holder C, et al. Complications of gamma knife surgery for Parkinson disease. Arch Neurol. 2001;58:1995–2002.
Esselink R, de Bie R, de Haan R, Steur E, Beute G, Portman A, et al. Unilateral pallidotomy versus bilateral subthalamic nucleus stimulation in Parkinson’s disease: one year follow-up of a randomised observer-blind multi centre trial. Acta Neurochir. 2006;148:1247–55.
Krack P, Batir A, Van Blercom N, Chabardes S, Fraix V, Ardouin C, et al. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med. 2003;349:1925–34.
Bejjani BP, Damier P, Arnulf I, Thivard L, Bonnet AM, Dormont D, et al. Transient acute depression induced by high-frequency deep-brain stimulation. N Engl J Med. 1999;340:1476–80.
Theodoros DG, Ward EC, Murdoch BE, Silburn P, Lethlean J. The impact of pallidotomy on motor speech function in Parkinson’s disease. J Med Speech Lang Pathol. 2000;8:315–22.
Uitti R. Advancing Parkinson’s disease and treatment of motor complications. In: Alder CH, Ahlskog JE, editors. Parkinson’s disease and movement disorders: diagnosis and treatment guidelines for the practicing physician. Totowa: Mayo Foundation for Medical Education and Research; 2000. p. 129–49.
Hunter P, Crameri J, Austin S, Woodward M, Hughes A. Response of parkinsonian swallowing dysfunction to dopaminergic stimulation. J Neurol Neurosurg Psychiatry. 1997;63:579–83.
Fonda D, Schwartz J, Clinnick S. Parkinsonian medication one hour before meals improves symptomatic swallowing: a case study. Dysphagia. 1995;10:165–6.
Welch MW, Logemann JA, Rademaker AW, Kahrilas PJ. Changes in pharyngeal dimensions effected by chin tuck. Arch Phys Med Rehabil. 1993;74:178–81.
Shanahan TK, Logemann JA, Rademaker AW, Pauloski BR, Kahrilas PJ. Chin-down posture effect on aspiration in dysphagic patients. Arch Phys Med Rehabil. 1993;74:736–9.
Garcia JM, Chambers E, Molander M. Thickened liquids: practice patterns of speech-language pathologists. Am J Speech Lang Pathol. 2003;14:4–13.
Macqueen C, Taubert S, Cotter D, Stevens S, Frost G. Which commercial thickening agent do patients prefer? Dysphagia. 2003;18:46–52.
Logemann J, Gensler G, Robbins J, Lindblat A, Brandt D, Hind J, et al. Randomised study of three interventions for aspiration of thin liquids in people with dementia or Parkinson’s disease. J Speech Lang Hear Res. 2008;51:173–83.
Robbins J, Gensler G, Hind G, Logemann J, Lindblad A, Brandt D, et al. Comparison of 2 interventions for liquid aspiration on pneumonia incidence: a randomized trial. Ann Intern Med. 2008;148:509–18.
Lazzara G, Lazarus CL, Logemann JA. Impact of thermal stimulation on the triggering of the swallowing reflex. Dysphagia. 1986;1:73–7.
Rosenbek JC, Robbins J, Fishback B, Levine RL. Effects of thermal application on dysphagia after stroke. J Speech Lang Hear Res. 1991;34:1257–68.
Rosenbek JC, Roecker EB, Wood JB, Robbins J. Thermal application reduced the duration of stage transition in dysphagia after stroke. Dysphagia. 1996;11:225–33.
Rosenbek JC, Robbins J, Willford WO, Kirk G, Schiltz A, Sowell T, et al. Comparing treatment intensities of tactile-thermal application. Dysphagia. 1998;13:1–9.
Hamdy S, Jilani S, Price V, Parker C, Hall N, Power M. Modulation of human swallowing behaviour by thermal and chemical stimulation in health and after brain injury. Neurogastroenterol Motil. 2003;15:69–77.
Power M, Fraser C, Hobson A, Rothwell JC, Mistry S, Nicholson DA, et al. Changes in pharyngeal corticobulbar excitability and swallowing behavior after oral stimulation. Am J Physiol Gastrointest Liver Physiol. 2004;286:G45–50.
Robey R. A five-phase model for clinical-outcome research. J Commun Disord. 2004;37:401–11.
Hoehn MM, Yahr MD. Parkinsonism: onset, progression and mortality. Neurology. 1967;17:427–42.
O’Neil K, Purdy M, Falk J, Gallo L. The dysphagia outcome and severity scale. Dysphagia. 1999;14:139–45.
Selinger M, Prescott TE, Hoffman I. Temperature acceleration in cold oral stimulation. Dysphagia. 1994;9:83–7.
R Development Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2008. ISBN 3-900051-07-0. http://www.R-project.org.
Johnson ER, McKenzie S, Sievers A. Aspiration and pneumonia in stroke. Arch Phys Med Rehabil. 1993;74:973–6.
Jean A. Brainstem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev. 2001;81:929–69.
Shaker R, Hogan WJ. Reflex-mediated enhancement of airway protective mechanisms. Am J Med. 2000;108(Suppl 4a):8S–14S.
Hamdy S, Aziz Q, Rothwell JC, Hobson A, Thompson DG. Sensorimotor modulation of human cortical swallowing pathways. J Physiol. 1998;506:857–66.
Doty R. Influence of stimulus pattern on reflex deglutition. Am J Physiol. 1951;166:142–55.
Miller AJ. Neuroscience of swallowing: strategies in rehabilitation. Perspect Swallow Swallow Disord (Dysphagia). 2008;17:121–7.
Rosenbek JC, Robbins JA, Roecker EB, Coyle JL. Penetration-aspiration scale. Dysphagia. 1996;11:93–8.
Eisenhuber E, Schima W, Schober E, Pokieser P, Stadler A, Scharitzer M, et al. Videofluoroscopic assessment of patients with dysphagia: pharyngeal retention is a predictive factor for aspiration. AJR Am J Roentgenol. 2002;178:393–8.
Acknowledgments
The authors thank the 15 people with IPD who participated in this study, the three speech and language therapists in AMNCH who provided reliability data, and Dr. Justin Kinsella, Neurology Department, AMNCH, who aided in the statistical analysis of data.
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Regan, J., Walshe, M. & Tobin, W.O. Immediate Effects of Thermal–Tactile Stimulation on Timing of Swallow in Idiopathic Parkinson’s Disease. Dysphagia 25, 207–215 (2010). https://doi.org/10.1007/s00455-009-9244-x
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DOI: https://doi.org/10.1007/s00455-009-9244-x