Skip to main content
Log in

Respiratory-Swallowing Coordination and Swallowing Safety in Patients with Parkinson’s Disease

  • Original Article
  • Published:
Dysphagia Aims and scope Submit manuscript

Abstract

The purpose of this study was to determine if individuals with Parkinson’s disease (PD) demonstrate abnormal respiratory events when swallowing thin liquids. In addition, this study sought to define associations between respiratory events, swallowing apnea duration, and penetration–aspiration (P–A) scale scores. Thirty-nine individuals with PD were administered ten trials of a 5-ml thin liquid bolus. P–A scale score quantified the presence of penetration and aspiration during the swallowing of a 3-oz sequential bolus. Participants were divided into two groups based on swallowing safety judged during the 3-oz sequential swallowing: Group 1 = P–A ≤ 2; Group 2 = P–A ≥ 3. Swallows were examined using videofluoroscopy coupled with a nasal cannula to record respiratory signals during the event(s). Findings indicated that expiration was the predominant respiratory event before and after swallowing apnea. The data revealed no differences in our cohort versus the percentages of post-swallowing events reported in the literature for healthy adults. In addition, individuals with decreased swallowing safety, as measured by the P–A scale, were more likely to inspire after swallows and to have shorter swallowing apnea duration. Individuals who inspired before swallow also had longer swallowing apnea duration. The occurrence of inspiratory events after a swallow and the occurrence of shorter swallowing apnea durations may serve as important indicators during clinical swallowing assessments in patients at risk for penetration or aspiration with PD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Nishino T, Hiraga K. Coordination of swallowing and respiration in unconscious subjects. J Appl Physiol. 1991;70:988–93.

    Article  PubMed  CAS  Google Scholar 

  2. Zald DH, Pardo JV. The functional neuroanatomy of voluntary swallowing. Ann Neurol. 1999;46:281–6.

    Article  PubMed  CAS  Google Scholar 

  3. Broussard DL, Altschuler SM. Central integration of swallow and airway-protective reflexes. Am J Med. 2000;108(Suppl 4a):62S–7S.

    Article  PubMed  Google Scholar 

  4. Saito Y, Ezure K, Tanaka I. Swallowing-related activities of respiratory and non-respiratory neurons in the nucleus of solitary tract in the rat. J Physiol. 2002;540:1047–60.

    Article  PubMed  CAS  Google Scholar 

  5. Hiss SG, Strauss M, Treole K, Stuart A, Boutilier S. Swallowing apnea as a function of airway closure. Dysphagia. 2003;18:293–300.

    Article  PubMed  Google Scholar 

  6. 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;94:1735–43.

    PubMed  Google Scholar 

  7. 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;131:762–70.

    Article  PubMed  Google Scholar 

  8. Hirst LJ, Ford GA, Gibson GJ, Wilson JA. Swallow-induced alterations in breathing in normal older people. Dysphagia. 2002;17:152–61.

    Article  PubMed  Google Scholar 

  9. Klahn MS, Perlman AL. Temporal and durational patterns associating respiration and swallowing. Dysphagia. 1999;14:131–8.

    Article  PubMed  CAS  Google Scholar 

  10. Preiksaitis HG, Mayrand S, Robins K, Diamant NE. Coordination of respiration and swallowing: effect of bolus volume in normal adults. Am J Physiol. 1992;263:R624–30.

    PubMed  CAS  Google Scholar 

  11. Preiksaitis HG, Mills CA. Coordination of breathing and swallowing: effects of bolus consistency and presentation in normal adults. J Appl Physiol. 1996;81:1707–14.

    PubMed  CAS  Google Scholar 

  12. Martin BJ, Logemann JA, Shaker R, Dodds WJ. Coordination between respiration and swallowing: respiratory phase relationships and temporal integration. J Appl Physiol. 1994;76:714–23.

    PubMed  CAS  Google Scholar 

  13. Smith J, Wolkove N, Colacone A, Kreisman H. Coordination of eating, drinking and breathing in adults. Chest. 1989;96:578–82.

    Article  PubMed  CAS  Google Scholar 

  14. Dozier TS, Brodsky MB, Michel Y, Walters BC Jr, Martin-Harris B. Coordination of swallowing and respiration in normal sequential cup swallows. Laryngoscope. 2006;116:1489–93.

    Article  PubMed  Google Scholar 

  15. Weiner P, Inzelberg R, Davidovich A, Nisipeanu P, Magadle R, Berar-Yanay N, Carasso RL. Respiratory muscle performance and the perception of dyspnea in Parkinson’s disease. Can J Neurol Sci. 2002;29:68–72.

    PubMed  Google Scholar 

  16. 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.

    Article  PubMed  CAS  Google Scholar 

  17. 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.

    Article  PubMed  CAS  Google Scholar 

  18. Vercueil L, Linard JP, Wuyam B, Pollak P, Benchetrit G. Breathing pattern in patients with Parkinson’s disease. Respir Physiol. 1999;118:163–72.

    Article  PubMed  CAS  Google Scholar 

  19. Polatli M, Akyol A, Cildag O, Bayulkem K. Pulmonary function tests in Parkinson’s disease. Eur J Neurol. 2001;8:341–5.

    Article  PubMed  CAS  Google Scholar 

  20. 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;22:420–4.

    Article  PubMed  Google Scholar 

  21. Troche MS, Sapienza CM, Rosenbek JC. Effects of bolus consistency on timing and safety of swallow in patients with Parkinson’s disease. Dysphagia. 2008;23:26–32.

    Article  PubMed  Google Scholar 

  22. Pinnington LL, Muhiddin KA, Ellis RE, Playford ED. Non-invasive assessment of swallowing and respiration in Parkinson’s disease. J Neurol. 2000;247:773–7.

    Article  PubMed  CAS  Google Scholar 

  23. Gross RD, Atwood CW Jr, Ross SB, Eichhorn KA, Olszewski JW, Doyle PJ. The coordination of breathing and swallowing in Parkinson’s disease. Dysphagia. 2008;23:136–45.

    Article  PubMed  Google Scholar 

  24. Pinnington LL, Muhiddin KA, Lobeck M, Pearce VR. Interrater and intrarrater reliability of the Exeter dysphagia assessment technique applied to healthy elderly adults. Dysphagia. 2000;15:6–9.

    Article  PubMed  CAS  Google Scholar 

  25. Selley WG, Ellis RE, Flack FC, Bayliss CR, Pearce VR. The synchronization of respiration and swallow sounds with videofluoroscopy during swallowing. Dysphagia. 1994;9:162–7.

    Article  PubMed  CAS  Google Scholar 

  26. Selley WG, Flack FC, Ellis RE, Brooks WA. The Exeter Dysphagia Assessment Technique. Dysphagia. 1990;4:227–35.

    Article  PubMed  CAS  Google Scholar 

  27. Kelly BN, Huckabee ML, Jones RD, Carroll GJ. The influence of volition on breathing-swallowing coordination in healthy adults. Behav Neurosci. 2007;121:1174–9.

    Article  PubMed  Google Scholar 

  28. Martin-Harris B, Logemann JA, McMahon S, Schleicher M, Sandidge J. Clinical utility of the modified barium swallow. Dysphagia. 2000;15:136–41.

    PubMed  CAS  Google Scholar 

  29. Mendell DA, Logemann JA. Temporal sequence of swallow events during the oropharyngeal swallow. J Speech Lang Hear Res. 2007;50:1256–71.

    Article  PubMed  Google Scholar 

  30. Logemann JA, Rademaker AW, Pauloski BR, Ohmae Y, Kahrilas PJ. Normal swallowing physiology as viewed by videofluoroscopy and videoendoscopy. Folia Phoniatr Logop. 1998;50:311–9.

    Article  PubMed  CAS  Google Scholar 

  31. Dodds WJ, Stewart ET, Logemann JA. Physiology and radiology of the normal oral and pharyngeal phases of swallowing. AJR Am J Roentgenol. 1990;154:953–63.

    PubMed  CAS  Google Scholar 

  32. Dantas RO, Kern MK, Massey BT, Dodds WJ, Kahrilas PJ, Brasseur JG, Cook IJ, Lang IM. Effect of swallowed bolus variables on oral and pharyngeal phases of swallowing. Am J Physiol. 1990;258:G675–81.

    PubMed  CAS  Google Scholar 

  33. Martin-Harris B, Michel Y, Castell DO. Physiologic model of oropharyngeal swallowing revisited. Otolaryngol Head Neck Surg. 2005;133:234–40.

    Article  PubMed  Google Scholar 

  34. Gross RD, Atwood CW Jr, Grayhack JP, Shaiman S. Lung volume effects on pharyngeal swallowing physiology. J Appl Physiol. 2003;95:2211–7.

    PubMed  Google Scholar 

  35. McCool FD. Global physiology and pathophysiology of cough: ACCP evidence-based clinical practice guidelines. Chest. 2006;129:48S–53S.

    Article  PubMed  Google Scholar 

  36. Smith Hammond C. Cough and aspiration of food and liquids due to oral pharyngeal dysphagia. Lung. 2008;186(Suppl 1):S35–40.

    Article  PubMed  Google Scholar 

  37. Smith Hammond CA, Goldstein LB, Zajac DJ, Gray L, Davenport PW, Bolser DC. Assessment of aspiration risk in stroke patients with quantification of voluntary cough. Neurology. 2001;56:502–6.

    PubMed  CAS  Google Scholar 

  38. Martin-Harris B, Brodsky MB, Michel Y, Lee FS, Walters B. Delayed initiation of the pharyngeal swallow: normal variability in adult swallows. J Speech Lang Hear Res. 2007;50:585–94.

    Article  PubMed  Google Scholar 

  39. Potulska A, Friedman A, Krolicki L, Spychala A. Swallowing disorders in Parkinson’s disease. Parkinsonism Relat Disord. 2003;9:349–53.

    Article  PubMed  Google Scholar 

  40. 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;110:383–92.

    Article  PubMed  CAS  Google Scholar 

  41. Fuh JL, Lee RC, Wang SJ, Lin CH, Wang PN, Chiang JH, Liu HC. Swallowing difficulty in Parkinson’s disease. Clin Neurol Neurosurg. 1997;99:106–12.

    Article  PubMed  CAS  Google Scholar 

  42. Nagaya M, Kachi T, Yamada T, Igata A. Videofluorographic study of swallowing in Parkinson’s disease. Dysphagia. 1998;13:95–100.

    Article  PubMed  CAS  Google Scholar 

  43. 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;20:457–62.

    Article  PubMed  Google Scholar 

  44. Hunter PC, Crameri J, Austin S, Woodward MC, Hughes AJ. Response of parkinsonian swallowing dysfunction to dopaminergic stimulation. J Neurol Neurosurg Psychiatry. 1997;63:579–83.

    Article  PubMed  CAS  Google Scholar 

  45. Robbins JA, Logemann JA, Kirshner HS. Swallowing and speech production in Parkinson’s disease. Ann Neurol. 1986;19:283–7.

    Article  PubMed  CAS  Google Scholar 

  46. Fernandez HH, Lapane KL. Predictors of mortality among nursing home residents with a diagnosis of Parkinson’s disease. Med Sci Monit. 2002;8:CR241–6.

    PubMed  Google Scholar 

  47. 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;23:251–4.

    Article  PubMed  CAS  Google Scholar 

  48. Hughes AJ, Daniel SE, Kilford L, Lees AJ. Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry. 1992;55:181–4.

    Article  PubMed  CAS  Google Scholar 

  49. Hoehn MM, Yahr MD. Parkinsonism: onset, progression, and mortality. Neurology. 1967;17:427–42.

    PubMed  CAS  Google Scholar 

  50. Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12:189–98.

    Article  PubMed  CAS  Google Scholar 

  51. Robbins JM, Coyle J, Rosenbek J, Roecker E, Wood J. Differentiation of normal and abnormal airway protection during swallowing using the penetration-aspiration scale. Dysphagia. 1999;14(4):228–32.

    Article  PubMed  CAS  Google Scholar 

  52. Rosenbek JC, Robbins JA, Roecker EB, Coyle JL, Wood JL. A penetration-aspiration scale. Dysphagia. 1996;11:93–8.

    Article  PubMed  CAS  Google Scholar 

  53. Morton R, Minford J, Ellis R, Pinnington L. Aspiration with dysphagia: the interaction between oropharyngeal and respiratory impairments. Dysphagia. 2002;17:192–6.

    Article  PubMed  Google Scholar 

  54. Butler SG, Stuart A, Pressman H, Poage G, Roche WJ. Preliminary investigation of swallowing apnea duration and swallow/respiratory phase relationships in individuals with cerebral vascular accident. Dysphagia. 2007;22(3):215–24.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by VA Merit Grant RR & D B3721R to Christine Sapienza, PhD.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michelle S. Troche.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Troche, M.S., Huebner, I., Rosenbek, J.C. et al. Respiratory-Swallowing Coordination and Swallowing Safety in Patients with Parkinson’s Disease. Dysphagia 26, 218–224 (2011). https://doi.org/10.1007/s00455-010-9289-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00455-010-9289-x

Keywords

Navigation