Abstract
Respiratory-swallow coordination (RSC) is important for swallowing safety. Atypical RSC is common in Parkinson’s disease (PD) and is associated with the presence of dysphagia and aspiration. Verbal cueing is known to affect RSC in healthy adults, yet an understanding of its effect on RSC in PD is unknown. Therefore, the aims of this study were to: (1) assess the effects of verbal cueing on respiratory-swallow patterning, lung volume initiation, and swallow apnea duration in PD; and (2) determine when during tidal breathing verbal cues should be given in order to increase the likelihood of eliciting optimal RSC. People with PD were prospectively recruited for respiratory-swallowing assessments during cued and non-cued swallowing conditions. Non-cued trials consisted of swallowing in an unprompted fashion, while cued trials consisted of swallowing only once participants were verbally instructed. Verbal cues were given at four specific points during tidal breathing. Nonparametric tests were used to compare differences in patterning, lung volume, and swallow apnea duration between the cued and non-cued swallows. Twenty-five people with PD were enrolled, yielding an analysis of 375 swallows. Verbal cueing significantly affected respiratory-swallow patterning (p < 0.0005), lung volume initiation (p < 0.0005), and swallow apnea duration (p < 0.0005). The effects of verbal cueing on RSC differed significantly depending on when during tidal breathing verbal cues were given. Cues given at high tidal inhalation were most likely to elicit optimal RSC, while cues given at low tidal exhalation were the least likely to elicit optimal RSC. The results of this study demonstrate that verbal cueing significantly affects RSC in PD. Depending on when verbal cues are given during tidal breathing, RSC can become more safe and coordinated or more atypical and risky. Clinicians should be cognizant of these effects by avoiding verbal cues if attempting to evaluate normal RSC during swallowing evaluations and cueing for swallows at the time of high tidal inhalation when targeting more optimal RSC in PD.
Similar content being viewed by others
References
O’Callaghan A, Walker R. A review of pulmonary function in Parkinson’s disease. J Park Restless Legs Syndr. 2018;8:13–23. https://doi.org/10.2147/JPRLS.S114309.
Shill H, Stacy M. Respiratory complications of Parkinson’s disease. Semin Respir Crit Care Med. 2002;23(3):262–5. https://doi.org/10.1016/j.prrv.2006.04.193.
Bushmann M, Dobmeyer SM, Leeker L, Perlmutter JS. Swallowing abnormalities and their response to treatment in Parkinson’s disease. Neurology. 1989;39(10):1309.
Pflug C, Moritz Bihler B, Katharina Emich B, et al. Critical dysphagia is common in Parkinson disease and occurs even in early stages: a prospective cohort study. Dysphagia. 2017. https://doi.org/10.1007/s00455-017-9831-1.
Kalf JG, De Swart BJM, Bloem BR, Munneke M. Prevalence of oropharyngeal dysphagia in Parkinson’s disease: a meta-analysis. Park Relat Disord. 2012;18:311–5. https://doi.org/10.1016/j.parkreldis.2011.11.006.
Takizawa C, Gemmell E, Kenworthy J, Speyer R. A Systematic review of the prevalence of oropharyngeal dysphagia in stroke, Parkinson’s disease, Alzheimer’s disease, head injury, and pneumonia. Dysphagia. 2016;1:8. https://doi.org/10.1007/s00455-016-9695-9.
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.
Gross RD, Atwood CW, Ross SB, Eichhorn KA, Olszewski JW, Doyle PJ. The coordination of breathing and swallowing in Parkinson’s disease. Dysphagia. 2008;23(2):136–45. https://doi.org/10.1007/s00455-007-9113-4.
Wang CM, Shieh WY, Weng YH, Hsu YH, Wu YR. Non-invasive assessment determine the swallowing and respiration dysfunction in early Parkinson’s disease. Park Relat Disord. 2017;42:22–7. https://doi.org/10.1016/j.parkreldis.2017.05.024.
Troche MS, Huebner I, Rosenbek JC, Okun MS, Sapienza CM. Respiratory-swallowing coordination and swallowing safety in patients with parkinson’s disease. Dysphagia. 2011;26:218–24. https://doi.org/10.1007/s00455-010-9289-x.
Leibovitz A, Baumoehl Y, Lubart E, Yaina A, Platinovitz N, Segal R. Dehydration among long-term care elderly patients with oropharyngeal dysphagia. Gerontology. 2007;53:179–83. https://doi.org/10.1159/000099144.
Streicher M, Wirth R, Schindler K, Sieber CC, Hiesmayr M, Volkert D. Dysphagia in Nursing homes—results from the nutrition day project. J Am Med Dir Assoc. 2018;19:141–7. https://doi.org/10.1016/j.jamda.2017.08.015.
Serra-Prat M, Palomera M, Gomez C, et al. Oropharyngeal dysphagia as a risk factor for malnutrition and lower respiratory tract infection in independently living older persons: a population-based prospective study. Age Ageing. 2012;41:376–81. https://doi.org/10.1093/ageing/afs006.
Namasivayam-MacDonald AM, Morrison JM, Steele CM, Keller H. How swallow pressures and dysphagia affect malnutrition and mealtime outcomes in long-term care. Dysphagia. 2017;32:785–96. https://doi.org/10.1007/s00455-017-9825-z.
Langmore SE, Terpenning MS, Schork A, et al. Predictors of aspiration pneumonia: how important is dysphagia? Dysphagia. 1998;13:69–81. https://doi.org/10.1007/PL00009559.
Daniels SK, Ballo LA, Mahoney MC, Foundas AL. Clinical predictors of dysphagia and aspiration risk: outcome measures in acute stroke patients. Arch Phys Med Rehabil. 2000;81:1031–3. https://doi.org/10.1053/apmr.2000.6301.
Beyer MK, Herlofson K, Arsland D, Larsen JP. Causes of death in a community-based study of Parkinson’s disease. Acta Neurol Scand. 2001;103(1):7–11. https://doi.org/10.1034/j.1600-0404.2001.00191.x.
Fall P, Saleh A, Fredrickson M, Olsson J, Granerus A. Survival time, mortality, and cause of death in elderly patients with Parkinson’s disease. Mov Disord. 2003;18(11):1312–6.
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.
Gross RD, Atwood CW, Grayhack JP, Shaiman S. Lung volume effects on pharyngeal swallowing physiology. J Appl Physiol. 2003;95:2211–7. https://doi.org/10.1152/japplphysiol.00316.2003.
Horton KK, Segers LS, Nuding SC, et al. Central respiration and mechanical ventilation in the gating of swallow with breathing. Front Physiol. 2018;9:1–17. https://doi.org/10.3389/fphys.2018.00785.
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. https://doi.org/10.1152/japplphysiol.00806.2002.
Martin BJ, Logemann JA, Shaker R, Dodds WJ. Coordination between respiration and swallowing: respiratory phase relationships and temporal integration. J Appl Physiol. 1994;76(2):714–23.
Perlman AL, He X, Barkmeier J, Van Leer E. Bolus Location associated with videofluoroscopic and respirodeglutometric events. J Speech Lang Hear Res. 2005;48(1):21–33. https://doi.org/10.1530/ERC-16-0328.
McFarland DH, Martin-Harris B, Fortin AJ, Humphries K, Hill E, Armeson K. Respiratory-swallowing coordination in normal subjects: lung volume at swallowing initiation. Respir Physiol Neurobiol. 2016;234:89–96. https://doi.org/10.1016/j.resp.2016.09.004.
Wheeler Hegland KM, Huber JE, Pitts T, Sapienza CM. Lung volume during swallowing: single bolus swallows in healthy young adults. J Speech Lang Hear Res. 2009;52:178–87. https://doi.org/10.1044/1092-4388(2008/07-0165).
Preiksaitis HG, Mills CA. Coordination of breathing and swallowing: effects of bolus consistency and presentation in normal adults. J Appl Physiol. 1996;81(4):1707–14.
Preiksaitis HG, Mayrand S, Robins K, Diamant NE. Coordination of respiration and swallowing: effect of bolus volume in normal adults. Am J Physiol Integr Comp Physiol. 1992;263(3):R624–30.
Lederle A, Hoit JD, Barkmeier-Kraemer J. Effects of sequential swallowing on drive to breathe in Young, healthy adults. Dysphagia. 2012;27(2):221–7. https://doi.org/10.1007/s00455-011-9357-x.
McFarland DH, Harris B-M, Fortin AJ. Enhancing swallowing-respiration coordination. Curr Phys Med Rehabil Rep. 2018;6(4):239–44. https://doi.org/10.1007/s40141-018-0202-0.
Morton R, Minford J, Ellis R, Pinnington LL. Aspiration with dysphagia: the interaction between oropharyngeal and respiratory impairments. Dysphagia. 2002;17:192–6. https://doi.org/10.1007/s00455-002-0051-x.
Nilsson H, Ekberg O, Bülow M, Hindfelt B. Assessment of respiration during video fluoroscopy of dysphagic patients. Acad Radiol. 1997;4(7):503–7. https://doi.org/10.1016/S1076-6332(97)80237-1.
Martin-Harris B, McFarland D, Hill EG, et al. Respiratory-swallow training in patients with head and neck cancer. Arch Phys Med Rehabil. 2015;96:885–93. https://doi.org/10.1016/j.apmr.2014.11.022.
Hiss SG, Treole K, Stuart A. Effects of age, gender, bolus volume, and trial on swallowing apnea duration and swallow/respiratory phase relationships of normal adults. Dysphagia. 2001;16:128–35. https://doi.org/10.1007/s004550011001.
Dozier TS, Brodsky MB, Michel Y, Walters BC, Martin-Harris B. Coordination of swallowing and respiration in normal sequential cup swallows. Laryngoscope. 2006;116:1489–93. https://doi.org/10.1097/01.mlg.0000227724.61801.b4.
Shaker R, Li Q, Ren J, et al. Coordination of deglutition and phases of respiration: effect of aging, tachypnea, bolus volume, and chronic obstructive pulmonary disease. Am J Physiol Liver Physiol. 1992;263(5):G750–5.
Klahn MS, Perlman AL. Temporal and durational patterns associating respiration and swallowing. Dysphagia. 1999;14(3):131–8.
Gross RD, Atwood CW, Ross SB, Olszewski JW, Eichhorn KA. The coordination of breathing and swallowing in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2009;179(7):559–65. https://doi.org/10.1164/rccm.200807-1139OC.
Hegland KW, Huber JE, Pitts T, Davenport PW, Sapienza CM. Lung volume measured during sequential swallowing in healthy young adults. J Speech Lang Hear Res. 2011;54:777–86. https://doi.org/10.1044/1092-4388(2010/09-0237).
Perlman AL, Ettema SL, Barkmeier J. Respiratory and acoustic signals associated with bolus passage during swallowing. Dysphagia. 2000;15(2):89–94. https://doi.org/10.1007/s004550010006.
Hirst LJ, Ford GA, Gibson GJ, Wilson JA. Swallow-induced alterations in breathing in normal older people. Dysphagia. 2002;17:152–61. https://doi.org/10.1007/s00455-001-0115-3.
Kumar R, Bhat JS. Respiratory swallow coordination in healthy individuals. Cloud Publ Int J Adv Speech Hear Res. 2012;1(1):1–9.
Daniels SK, Schroeder MF, Degeorge PC, Corey DM, Rosenbek JC. Effects of verbal cue on bolus flow during swallowing. Am J Speech-Language Pathol. 2007;16:140–7. https://doi.org/10.1044/1058-0360(2007/018).
Nagy A, Leigh C, Hori SF, Molfenter SM, Shariff T, Steele CM. Timing differences between cued and noncued swallows in healthy young adults. Dysphagia. 2013;28:428–34. https://doi.org/10.1007/s00455-013-9456-y.
Molfenter SM, Leigh C, Steele CM. Event sequence variability in healthy swallowing: building on previous findings. Dysphagia. 2014;29:234–42. https://doi.org/10.1007/s00455-013-9501-x.
Curtis JA, Molfenter S, Troche MS. Predictors of residue and airway invasion in Parkinson’s disease. Dysphagia. 2019. https://doi.org/10.1007/s00455-019-10014-z.
Nasreddine ZS, Phillips NA, Bédirian V, et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc. 2005;53(4):695–9.
Cichero JAY, Lam P, Steele CM, et al. Development of international terminology and definitions for texture-modified foods and thickened fluids used in dysphagia management: the IDDSI framework. Dysphagia. 2017;32(2):293–314. https://doi.org/10.1007/s00455-016-9758-y.
Rosenbek JC, Robbins J, Roecker EB, Coyle JL, Wood JL. A penetration-aspiration scale. Dysphagia. 1996;11:93–8.
Neubauer PD, Hersey DP, Leder SB. Pharyngeal Residue severity rating scales based on fiberoptic endoscopic evaluation of swallowing: a systematic review. Dysphagia. 2016. https://doi.org/10.1007/s00455-015-9682-6.
Mead J, Konno JM. Measurement of the separate volume changes of rib cage and abdomen during breathing. J Appl Physiol. 1967;22(3):407–22.
Altman DG. Practical statistics for medical research. London: Chapman & Hall; 1991.
Koo TK, Li MY. A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med. 2016;15:155–63. https://doi.org/10.1016/j.jcm.2016.02.012.
Kelly BN, Huckabee ML, Jones RD, Carroll GJ. The influence of volition on breathing-swallowing coordination in healthy adults. Behav Neurosci. 2007;121(6):1174–9. https://doi.org/10.1037/0735-7044.121.6.1174.
Diez Gross R, Atwood CW Jr, Ross SB, Eichhorn KA, Olszewski JW, Doyle PJ. The coordination of breathing and swallowing in parkinson’s disease. Dysphagia. 2007;23(2):136–45. https://doi.org/10.1007/s00455-007-9113-4.
Acknowledgements
This work was supported in part by grant funds to Dr. Michelle Troche from the Michael J. Fox Foundation.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Authors James A. Curtis and Michelle S. Troche declare they each have no conflicts of interest.
Ethical Approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Curtis, J.A., Troche, M.S. Effects of Verbal Cueing on Respiratory-Swallow Patterning, Lung Volume Initiation, and Swallow Apnea Duration in Parkinson’s Disease. Dysphagia 35, 460–470 (2020). https://doi.org/10.1007/s00455-019-10050-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00455-019-10050-9