Skip to main content

Reflex Cough and Disease Duration as Predictors of Swallowing Dysfunction in Parkinson’s Disease

Abstract

Patients with Parkinson’s disease (PD) have progressive and pervasive disorders of airway protection. Recent work has highlighted the relationship between reflex and voluntary cough and swallowing safety. The goal of this study was to test the sensitivity and specificity of several airway protective and disease-specific factors for predicting swallowing safety outcomes in PD. Sixty-four participants (44 males) completed measures of voluntary and reflex cough, and swallowing safety. Clinical predictors included disease severity and duration, and cough airflow and sensitivity measures. ROC and Chi-square analyses identified predictors of swallowing safety (penetration–aspiration score) in PD. Disease duration significantly discriminated between patients with normal and abnormal swallowing safety (p = 0.027, sensitivity: 71 %, specificity: 55.4 %). Cough reflex sensitivity significantly discriminated between patients who penetrated above the level of the vocal folds and those with more severe penetration/aspiration (p = 0.021, sensitivity: 71.0 %, specificity 57.6 %). Urge-to-cough sensitivity (log–log linear slope) was the only variable which significantly discriminated between patients with penetration versus aspiration (p = 0.017, sensitivity: 85.7 %, specificity 73.2 %). It is important to identify the factors which influence airway protective outcomes in PD especially given that aspiration pneumonia is a leading cause of death. Results from this study highlight the ecological validity of reflex cough in the study of airway protection and this study further identifies important factors to consider in the screening of airway protective deficits in PD.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. 1.

    Fernandez HH, Lapane KL. Predictors of mortality among nursing home residents with a diagnosis of Parkinson’s disease. Med Sci Monit. 2002;8(4):CR241–6.

    PubMed  Google Scholar 

  2. 2.

    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(11):1312–6.

    Article  PubMed  Google Scholar 

  3. 3.

    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(1):33–7.

    Article  PubMed  Google Scholar 

  4. 4.

    Gorell JM, Johnson CC, Rybicki BA. Parkinson’s disease and its comorbid disorders: an analysis of Michigan mortality data, 1970 to 1990. Neurology. 1994;4(10):1865–8.

    Article  Google Scholar 

  5. 5.

    Miller N, Noble E, Jones D, Burn D. Hard to swallow: dysphagia in Parkinson’s disease. Age Ageing. 2006;35(6):614–8.

    Article  PubMed  Google Scholar 

  6. 6.

    Pitts T, Bosler DC, Rosenbeck JC, Troche MS, Sapienza C. Voluntary cough production and swallow dysfunction in Parkinson’s disease. Dysphagia. 2008;23(3):297–301.

    Article  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Pitts T, Troche MS, Mann G, Rosenbeck JC, Okun MS, Sapienza C. Using voluntary cough to detect penetration and aspiration during oropharyngeal swallowing in patients with Parkinson disease. Chest. 2010;138(6):1426–31.

    Article  PubMed  Google Scholar 

  8. 8.

    Troche MS, Brandimore AE, Okun MS, Davenport PW, Hegland KW. Decreased cough sensitivity and aspiration in Parkinson’s disease. Chest. 2014;146(5):1294–9.

    Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    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(4):502–6.

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Smith Hammond CA, Goldstein LB, Horner RD, Ying J, Gray L, Gonzalez-Rothi DC, Bolser DC. Predicting aspiration in patients with ischemic stroke: comparison of clinical signs and aerodynamic measures of voluntary cough. Chest. 2009;135(3):769–77.

    Article  PubMed  Google Scholar 

  11. 11.

    Hegland KW, Okun MS, Troche MS. Sequential voluntary cough and aspiration or aspiration risk in Parkinson’s disease. Lung. 2014;192(4):601–8.

    Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Wheeler Hegland K, Troche MS, Brandimore AE, Davenport PW, Okun MS. Comparison of voluntary and reflex cough effectiveness in Parkinson’s disease. Parkinsonism Relat Disord. 2014;20(11):1226–30.

    Article  PubMed  Google Scholar 

  13. 13.

    Vovk A, Bolser DC, Hey JA, Danzig M, Vickroy T, Berry R, Martin AD, Davenport PW. Capsaicin exposure elicits complex airway defensive motor patterns in normal humans in a concentration-dependent manner. Pulm Pharmacol Ther. 2007;20(4):423–32.

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Hegland KW, Troche MS, Davenport PW. Cough expired volume and airflow rates during sequential induced cough. Front Physiol. 2013;4:167.

    Article  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Rosenbeck JC, Robbins JA, Roecker EB, Coyle JL, Wood JL. A penetration-aspiration scale. Dysphagia. 1996;11(2):93–8.

    Article  Google Scholar 

  16. 16.

    Troche MS, Brandimore AE, Godoy J, Hegland KW. A framework for understanding shared substrates of airway protection. J Appl Oral Sci. 2014;22(4):251–60.

    Article  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Bolser DC, Poliacek J, Jakus J, Fuller DD, Davenport PW. Neurogenesis of cough, other airway defensive behaviors and breathing: a holarchical system. Respir Physiol Neurobiol. 2006;152(3):255–65.

    Article  PubMed  PubMed Central  Google Scholar 

  18. 18.

    Davenport PW, Bolser DC, Morris KF. Swallow remodeling of respiratory neural networks. Head Neck. 2013;33(Suppl 1):S8–13.

    Google Scholar 

  19. 19.

    Mazzone SB, McGovern AE, Yang SK, Woo A, Phipps S, Ando A, Leech J, Farrel MJ. Sensorimotor circuitry involved in the higher brain control of coughing. Cough. 2013;9(1):7.

    Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Mazzone SB, Cole LJ, Ando A, Egan GF, Farrel MJ. Investigation of the neural control of cough and cough suppression in humans using functional brain imaging. J Neurosci. 2011;31(8):2948–58.

    CAS  Article  PubMed  Google Scholar 

  21. 21.

    Simonyan K, Saad ZS, Loucks TM, Poletto CJ, Ludlow CL. Functional neuroanatomy of human voluntary cough and sniff production. Neuroimage. 2007;37(2):401–9.

    Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Davenport PW. Clinical cough I: the urge-to-cough: a respiratory sensation. Handb Exp Pharmacol. 2009;187:263–76.

    Article  Google Scholar 

  23. 23.

    Theurer JA, Bihari F, Barr AM, Martin RE. Oropharyngeal stimulation with air-pulse trains increases swallowing frequency in healthy adults. Dysphagia. 2005;20(4):254–60.

    Article  PubMed  Google Scholar 

  24. 24.

    Davenport PW, Sapienza CS, Bolser D. Psychophysical assessment of the urge-to-cough. Eur Respir J. 2002;12(85):249–53.

    Google Scholar 

  25. 25.

    Davenport PW, Bolser DC, Vickroy T, Berry RB, Martin AD, Hey JA, Danzig M. The effect of codeine on the urge-to-cough response to inhaled capsaicin. Pulm Pharmacol Ther. 2007;20(4):338–46.

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    Ebihara S, Saito H, Kanda A, Nakajoh M, Takahashi H, Arai H, Sasaki H. Impaired efficacy of cough in patients with Parkinson disease. Chest. 2003;124(3):1009–15.

    Article  PubMed  Google Scholar 

  27. 27.

    Fontana GA, Pantaleo T, Lavorini F, Benvenuti F, Gangemi S. Defective motor control of coughing in Parkinson’s disease. Am J Respir Crit Care Med. 1998;158(2):458–64.

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    Hegland KW, Troche MS, Brandimore AE, Okun MS, Davenport PW. Comparison of two methods for inducing reflex cough in patients with Parkinson’s disease, with and without dysphagia. Dysphagia. 2016;31(1):66–73.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to first acknowledge the participants and caregivers who so generously gave of their time to participate in this study. We also acknowledge the support of the National Parkinson Foundation Center of Excellence at the University of Florida and of the NIH (NCATS) CTSA through the University of Florida (UL1TR000064 and KL2TR000065) awarded to Dr. Michelle S. Troche.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Michelle S. Troche.

Ethics declarations

Conflict of Interest

Dr. Troche’s work was supported in part by an NIH (NCATS) CTSA through the University of Florida (UL1TR000064 and KL2TR000065). She has no other disclosures or conflicts of interest to report. Ms. Schumann has no financial disclosures to report. Dr. Brandimore’s work was supported in part by a predoctoral fellowship through the Department of Veterans Affairs. Dr. Okun serves as a consultant for the National Parkinson Foundation, and has received research grants from NIH, NPF, the Michael J. Fox Foundation, the Parkinson Alliance, Smallwood Foundation, the Bachmann-Strauss Foundation, the Tourette Syndrome Association, and the UF Foundation. Dr. Okun has previously received honoraria, but in the past >36 months has received no support from industry. Dr. Okun has received royalties for publications with Demos, Manson, Amazon, and Cambridge (movement disorders books). Dr. Okun is an associate editor for New England Journal of Medicine Journal Watch Neurology. Dr. Okun has participated in CME activities on movement disorders in the last 36 months sponsored by PeerView, Prime, and by Vanderbilt University. The institution and not Dr. Okun receives grants from Medtronic and ANS/St. Jude, and the PI has no financial interest in these grants. Dr. Okun has participated as a site PI and/or co-I for several NIH, foundation, and industry sponsored trials over the years but has not received honoraria. Dr. Hegland’s work is supported in part by the American Heart Association, National Institutes of Health and BAE defense systems.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Troche, M.S., Schumann, B., Brandimore, A.E. et al. Reflex Cough and Disease Duration as Predictors of Swallowing Dysfunction in Parkinson’s Disease. Dysphagia 31, 757–764 (2016). https://doi.org/10.1007/s00455-016-9734-6

Download citation

Keywords

  • Deglutition
  • Deglutition disorders
  • Parkinson’s disease
  • Reflex cough
  • Dystussia
  • Dysphagia
  • Aspiration