Abstract
Multiple investigations have determined that healthy adults swallow most often during exhalation and that exhalation regularly follows the swallow, even when a swallow occurs during inhalation. We hypothesized that persons with idiopathic Parkinson’s disease would demonstrate impaired breathing and swallowing coordination during spontaneous eating. Twenty-five healthy volunteers and 25 Parkinson’s disease patients spontaneously swallowed calibrated pudding and cookie portions while simultaneous nasal airflow and respiratory inductance plethysmography were used to track spontaneous breathing. Surface EMG was used to record the timing of each swallow within the respiratory cycle. When compared to the healthy control group, those with Parkinson’s disease swallowed significantly more often during inhalation and at low tidal volumes. The Parkinson’s participants also exhibited significantly more postswallow inhalation for both consistencies. Only the healthy subjects exhibited significantly longer deglutitive apnea when swallows that occurred during inhalation were compared with those that occurred during exhalation. The high incidence of oropharyngeal dysphagia and risk of aspiration pneumonia found in Parkinson’s disease patients may be partially attributable to impaired coordination of breathing and swallowing.
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Tanner CM, Ben-Shlomo Y. Epidemiology of Parkinson’s disease. Adv Neurol 1999;80:153–159.
Wermuth L, Stenager EN, Stenager E, Boldsen J. Mortality in patients with Parkinson’s disease. Acta Neurol Scand 1995;92:55–58.
D’Amelio M, Ragonese P, Morgante L, Reggio A, Callari G, Salemi G, Savettieri G. Long-term survival of Parkinson’s disease: a population-based study. J Neurol 2006;253:33–37.
Schupbach MW, Welter ML, Bonnet AM, Elbaz A, Grossardt BR, Mesnage V, Houeto JL, Maltete D, Mallet L, Rocca WA, Mallet A, Agid Y. Mortality in patients with Parkinson’s disease treated by stimulation of the subthalamic nucleus. Mov Disord 2007;22:257–261.
Fall PA, Saleh A, Fredrickson M, Olsson JE, Granerus AK. Survival time, mortality, and cause of death in elderly patients with Parkinson’s disease: a 9-year follow-up. Mov Disord 2003;18:1312–1316.
Morgante L, Salemi G, Meneghini F, Di Rosa AE, Epifanio A, Grigoletto F, Ragonese P, Patti F, Reggio A, Di Perri R, Savettieri G. Parkinson disease survival: a population-based study. Arch Neurol 2000;57:507–512.
Bird MR, Woodward MC, Gibson EM, Phyland DJ, 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;23:251–254.
Stroudley J, Walsh M. Radiological assessment of dysphagia in Parkinson’s disease. Br J Radiol 1991;64:890–893.
Potulska A, Friedman A, Krolicki L, Jedrzejowski M, Spychala A. [Swallowing disorders in Parkinson’s disease]. Neurol Neurochir Pol 2002;36:449–456.
Miller N, Noble E, Jones D, Burn D. Hard to swallow: dysphagia in Parkinson’s disease. Age Ageing 2006;35:614–618.
Ali GN, Wallace KL, Schwartz R, DeCarle DJ, Zagami AS, Cook IJ. Mechanisms of oral-pharyngeal dysphagia in patients with Parkinson’s disease. Gastroenterology 1996;110:383–392.
Monte FS, da Silva-Junior FP, Braga-Neto P, Nobre e Souza MA, Sales de Bruin VM. Swallowing abnormalities and dyskinesia in Parkinson’s disease. Mov Disord 2005;20:457–462.
Nilsson H, Ekberg O, Bulow M, Hindfelt B. Assessment of respiration during video fluoroscopy of dysphagic patients. Acad Radiol 1997;4:503–507.
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.
Hunter PC, Crameri J, Austin S, Woodward MC, Hughes AJ. Response of parkinsonian swallowing dysfunction to dopaminergic stimulation. J Neurol Neurosurg Psychiatry 1997;63:579–583.
Ertekin C, Tarlaci S, Aydogdu I, Kiylioglu N, Yuceyar N, Turman AB, Secil Y, Esmeli F. Electrophysiological evaluation of pharyngeal phase of swallowing in patients with Parkinson’s disease. Mov Disord 2002;17:942–949.
Bushmann M, Dobmeyer SM, Leeker L, Perlmutter JS. Swallowing abnormalities and their response to treatment in Parkinson’s disease. Neurology 1989;39:1309–1314.
Duff J, Sime E. Surgical interventions in the treatment of Parkinson’s disease (PD) and essential tremor (ET): medial pallidotomy in PD and chronic deep brain stimulation (DBS) in PD and ET. Axone 1997;18:85–89.
Chou KL, Forman MS, Trojanowski JQ, Hurtig HI, Baltuch GH. Subthalamic nucleus deep brain stimulation in a patient with levodopa-responsive multiple system atrophy. Case report. J Neurosurg 2004;100:553–556.
Okun MS, Stover NP, Subramanian T, Gearing M, Wainer BH, Holder CA, Watts RL, Juncos JL, Freeman A, Evatt ML, Schuele SU, Vitek JL, DeLong MR. Complications of gamma knife surgery for Parkinson disease. Arch Neurol 2001;58:1995–2002.
Esselink RA, de Bie RM, de Haan RJ, Steur EN, Beute GN, Portman AT, Schuurman PR, Bosch DA, Speelman JD. 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 (Wien) 2006;148:1247–1255.
Feroah TR, Forster HV, Fuentes CG, Lang IM, Beste D, Martino P, Pan L, Rice T. Effects of spontaneous swallows on breathing in awake goats. J Appl Physiol 2002;92:1923–1935.
Vercueil L, Linard JP, Wuyam B, Pollak P, Benchetrit G. Breathing pattern in patients with Parkinson’s disease. Respir Physiol 1999;118:163–172.
Pal PK, Sathyaprabha TN, Tuhina P, Thennarasu K. Pattern of subclinical pulmonary dysfunctions in Parkinson’s disease and the effect of levodopa. Mov Disord 2007;22:420–424.
de Bruin PF, de Bruin VM, Lees AJ, Pride NB. Effects of treatment on airway dynamics and respiratory muscle strength in Parkinson’s disease. Am Rev Respir Dis 1993;148:1576–1580.
Hovestadt A, Bogaard JM, Meerwaldt JD, van der Meche FG, Stigt J. Pulmonary function in Parkinson’s disease. J Neurol Neurosurg Psychiatry 1989;52:329–333.
Polatli M, Akyol A, Cildag O, Bayulkem K. Pulmonary function tests in Parkinson’s disease. Eur J Neurol 2001;8:341–345.
Selley WG, Flack FC, Ellis RE, Brooks WA. Respiratory patterns associated with swallowing: Part 1. The normal adult pattern and changes with age. Age Ageing 1989;18:168–172.
Martin-Harris B, Brodsky MB, Price CC, Michel Y, Walters B. Temporal coordination of pharyngeal and laryngeal dynamics with breathing during swallowing: single liquid swallows. J Appl Physiol 2003;94:1735–1743.
Klahn MS, Perlman AL. Temporal and durational patterns associating respiration and swallowing. Dysphagia 1999;14:131–138.
Martin-Harris B, Brodsky MB, Michel Y, Ford CL, Walters B, Heffner J. Breathing and swallowing dynamics across the adult lifespan. Arch Otolaryngol Head Neck Surg 2005;131:762–770.
Martin BJ, Logemann JA, Shaker R, Dodds WJ. Coordination between respiration and swallowing: respiratory phase relationships and temporal integration. J Appl Physiol 1994;76:714–723.
Palmer JB, Hiiemae KM. Eating and breathing: interactions between respiration and feeding on solid food. Dysphagia 2003;18:169–178.
Morton R, Minford J, Ellis R, Pinnington L. Aspiration with dysphagia: the interaction between oropharyngeal and respiratory impairments. Dysphagia 2002;17:192–196.
Pinnington LL, Muhiddin KA, Ellis RE, Playford ED. Non-invasive assessment of swallowing and respiration in Parkinson’s disease. J Neurol 2000;247:773–777.
Nagaya M, Kachi T, Yamada T, Igata A. Videofluorographic study of swallowing in Parkinson’s disease. Dysphagia 1998;13:95–100.
Bayles K, Tomoeda CK. Arizona Battery for Communication Disorders of Dementia. City AZ: Caynonlands Publishing 1993.
Bayles KA, Boone DR, Tomoeda CK, Slauson TJ, Kaszniak AW. Differentiating Alzheimer’s patients from the normal elderly and stroke patients with aphasia. J Speech Hear Disord 1989;54:74–87.
Tarrant SC, Ellis RE, Flack FC, Selley WG. Comparative review of techniques for recording respiratory events at rest and during deglutition. Dysphagia 1997;12:24–38.
Ertekin C, Pehlivan M, Aydogdu I, Ertas M, Uludag B, Celebi G, Colakoglu Z, Sagduyu A, Yuceyar N. An electrophysiological investigation of deglutition in man. Muscle Nerve 1995;18:1177–1186.
Hiss SG, Strauss M, Treole K, Stuart A, Boutilier S. Swallowing apnea as a function of airway closure. Dysphagia 2003;18:293–300.
Leslie P, Drinnan MJ, Ford GA, Wilson JA. Swallow respiratory patterns and aging: presbyphagia or dysphagia? J Gerontol A Biol Sci Med Sci 2005;60:391–395.
Adzaku FK. The morphological and functional characteristics of the innervation of the subglottic mucosa of the larynx. Ann R Coll Surg Engl 1980;62:426–431.
Wyke B: Ventilatory and phonatory control systems: an international symposium. London: Oxford University Press, 1974.
Gross RD, Atwood CW Jr, Grayhack JP, Shaiman S. Lung volume effects on pharyngeal swallowing physiology. J Appl Physiol 2003;95:2211–2217.
Gross RD, Mahlmann J, Grayhack JP. Physiologic effects of open and closed tracheostomy tubes on the pharyngeal swallow. Ann Otol Rhinol Laryngol 2003;112:143–152.
Stachler RJ, Hamlet SL, Choi J, Fleming S. Scintigraphic quantification of aspiration reduction with the Passy-Muir valve. Laryngoscope 1996;106:231–234.
Suiter DM, McCullough GH, Powell PW. Effects of cuff deflation and one-way tracheostomy speaking valve placement on swallow physiology. Dysphagia 2003;18:284–292.
Gross RD, Steinhauer KM, Zajac DJ, Weissler MC. Direct measurement of subglottic air pressure while swallowing. Laryngoscope 2006;116:753–761.
Dettelbach MA, Gross RD, Mahlmann J, Eibling DE. Effect of the Passy-Muir valve on aspiration in patients with tracheostomy. Head Neck 1995;17:297–302.
Muz J, Hamlet S, Mathog R, Farris R. Scintigraphic assessment of aspiration in head and neck cancer patients with tracheostomy. Head Neck 1994;16:17–20.
Elpern EH, Borkgren Okonek M, Bacon M, Gerstung C, Skrzynski M. Effect of the Passy-Muir tracheostomy speaking valve on pulmonary aspiration in adults. Heart Lung 2000;29:287–293.
Leder SB, Tarro JM, Burrell MI. Effect of occlusion of a tracheotomy tube on aspiration. Dysphagia 1996;11:254–258.
Logemann JA, Pauloski BR, Colangelo L. Light digital occlusion of the tracheostomy tube: a pilot study of effects on aspiration and biomechanics of the swallow. Head Neck 1998;20:52–57.
Vincken WG, Gauthier SG, Dollfuss RE, Hanson RE, Darauay CM, Cosio MG. Involvement of upper-airway muscles in extrapyramidal disorders. A cause of airflow limitation. N Engl J Med 1984;311:438–442.
Sabate M, Gonzalez I, Ruperez F, Rodriguez M. Obstructive and restrictive pulmonary dysfunctions in Parkinson’s disease. J Neurol Sci 1996;138:114–119.
Sabate M, Rodriguez M, Mendez E, Enriquez E, Gonzalez I. Obstructive and restrictive pulmonary dysfunction increases disability in Parkinson disease. Arch Phys Med Rehabil 1996;77:29–34.
Izquierdo-Alonso JL, Jimenez-Jimenez FJ, Cabrera-Valdivia F, Mansilla-Lesmes M. Airway dysfunction in patients with Parkinson’s disease. Lung 1994;172:47–55.
Berke GS, Gerratt B, Kreiman J, Jackson K. Treatment of Parkinson hypophonia with percutaneous collagen augmentation. Laryngoscope 1999;109:1295–1299.
Leopold NA, Kagel MC. Laryngeal deglutition movement in Parkinson’s disease. Neurology 1997;48:373–376.
Zesiewicz TA, Baker MJ, Wahba M, Hauser RA. Autonomic nervous system Dysfunction in Parkinson’s disease. Curr Treat Options Neurol 2003;5:149–160.
Baumgartner CA, Sapir S, Ramig TO. Voice quality changes following phonatory-respiratory effort treatment (LSVT) versus respiratory effort treatment for individuals with Parkinson disease. J Voice 2001;15:105–114.
Ramig LO, Countryman S, Thompson LL, Horii Y. Comparison of two forms of intensive speech treatment for Parkinson disease. J Speech Hear Res 1995;38:1232–1251.
Deane KH, Ellis-Hill C, Jones D, Whurr R, Ben-Shlomo Y, Playford ED, Clarke CE. Systematic review of paramedical therapies for Parkinson’s disease. Mov Disord 2002;17:984–991.
Deane KH, Whurr R, Clarke CE, Playford ED, Ben-Shlomo Y. Non-pharmacological therapies for dysphagia in Parkinson’s disease. Cochrane Database Syst Rev 2001;CD002816.
Sharkawi AE, Ramig L, Logemann JA, Pauloski BR, Rademaker AW, Smith CH, Pawlas A, Baum S, Werner C. Swallowing and voice effects of Lee Silverman Voice Treatment (LSVT): a pilot study. J Neurol Neurosurg Psychiatry 2002;72:31–36.
Ramig LO, Countryman S, O’Brien C, Hoehn M, Thompson L. Intensive speech treatment for patients with Parkinson’s disease: short-and long-term comparison of two techniques. Neurology 1996;47:1496–1504.
Kijima M, Isono S, Nishino T. Coordination of swallowing and phases of respiration during added respiratory loads in awake subjects. Am J Respir Crit Care Med 1999;159:1898–1902.
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This work was performed at the VA Pittsburgh Healthcare System, University Drive location, and was funded by the Department of Veteran’s Affairs Research and Rehabilitation Merit Review Program.
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Gross, R.D., Atwood, C.W., Ross, S.B. et al. The Coordination of Breathing and Swallowing in Parkinson’s Disease. Dysphagia 23, 136–145 (2008). https://doi.org/10.1007/s00455-007-9113-4
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DOI: https://doi.org/10.1007/s00455-007-9113-4