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Dual Tasking Influences Cough Reflex Outcomes in Adults with Parkinson’s Disease: A Controlled Study

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Abstract

Coughing is an essential airway protective reflex. In healthy young adults, cough somatosensation changes when attention is divided (dual tasking). Whether the same is true in populations at risk of aspiration remains unknown. We present findings from a controlled study testing the effects of divided attention (via a dual-task paradigm) on measures of reflex cough in Parkinson’s disease. Volunteers with Parkinson’s disease (n = 14, age = 43–79 years) and 14 age-matched controls underwent five blocks of capsaicin-induced cough challenges. Within each block, capsaicin ranging from 0 to 200 μM was presented in a randomized order. Two blocks consisted of cough testing only (single task), and two blocks consisted of cough testing with simultaneous tone counting (dual task). Finally, participants completed a suppressed cough task. Measures of cough motor response, self-reported urge to cough, cough frequency, and cough airflow were collected. Historical data from healthy young adults was included for comparison. Between-group analyses revealed no differences between single- and dual-cough-task responses. However, post hoc analysis revealed a significant relationship between dual-task errors and cough frequency that was strongest in people with Parkinson’s disease [p = 0.004, r2 = 0.52]. Specifically, greater errors were associated with fewer reflexive coughs. Unlike healthy participants, participants with Parkinson’s disease did not change the number of coughs between the single-, dual-, and suppressed-task conditions [p > 0.05]. When distracted, people with Parkinson’s disease may prioritize coughing differently than healthy controls. Abnormal cortical resource allocation may be a mechanism involved in aspiration in this population.

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References

  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–R246.

  2. Singer RB. Mortality in patients with Parkinson’s disease treated with dopa. J Insur Med. 1992;24(2):126–7.

    CAS  PubMed  Google Scholar 

  3. 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.

    Article  PubMed  Google Scholar 

  4. D’Amelio M, et al. Long-term survival of Parkinson’s disease: a population-based study. J Neurol. 2006;253(1):33–7.

    Article  PubMed  Google Scholar 

  5. Robbins J, et al. Comparison of 2 interventions for liquid aspiration on pneumonia incidence: a randomized trial. Ann Intern Med. 2008;148(7):509–18.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Logemann JA, et al. A randomized study of three interventions for aspiration of thin liquids in patients with dementia or Parkinson’s disease. J Speech Lang Hear Res. 2008;51(1):173–83.

    Article  PubMed  Google Scholar 

  7. Brodsky MB, Abbott KV, McNeil MR, Palmer CV, Grayhack JP, Martin-Harris B. Effects of divided attention on swallowing in persons with idiopathic Parkinson’s disease. Dysphagia. 2012;27(3):390–400.

    Article  PubMed  Google Scholar 

  8. Troche MS, Okun MS, Rosenbek JC, Altmann LJ, Sapienza CM. Attentional resource allocation and swallowing safety in Parkinson’s disease: a dual task study. Park Relat Disord. 2014;20(4):439–43.

    Article  Google Scholar 

  9. Penko AL, et al. Dual-task interference disrupts parkinson’s gait across multiple cognitive domains. Neuroscience. 2018;379:375–82.

    Article  CAS  PubMed  Google Scholar 

  10. O’Shea S, Morris ME, Iansek R. Dual task interference during gait in people With Parkinson disease: effects of motor versus cognitive secondary tasks. Phys Ther. 2002;82(9):888–97.

    Article  PubMed  Google Scholar 

  11. Camicioli R, Oken B, Sexton G, Kaye J, Nutt J. Verbal fluency task affects gait in Parkinson’s disease with motor freezing. J Geriatr Psychiatry Neurol. 1998;11(4):181–5.

    Article  CAS  PubMed  Google Scholar 

  12. Morris ME, Iansek R, Matyas T, Summers J. Stride length regulation in Parkinson’s disease: normalization strategies and underlying mechanisms. Brain. 1996;119:551–68.

    Article  PubMed  Google Scholar 

  13. Behrman A, Teitelbaum P, Cauraugh J. Verbal instructional sets to normalise the temporal and spatial gait variables in Parkinson’s disease. J Neurol Neurosurg Psychiatry. 1998;65:580–2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Gao L, Zhang J, Hou Y, Hallett M, Chan P, Wu T. The cerebellum in dual-task performance in Parkinson’s disease. Sci Rep. 2017;7:1–11.

    Google Scholar 

  15. Kim Y, Oh B-M, Jung I-Y, Lee JC, Lee GJ, Han TR. Spatiotemporal characteristics of swallowing in Parkinson’s disease. Laryngoscope. 2015;125(2):389–95.

    Article  PubMed  Google Scholar 

  16. Han M, et al. Relationship between dysphagia and depressive states in patients with Parkinson’s disease. Park Relat Disord. 2011;17(6):437–9.

    Article  Google Scholar 

  17. Mamolar Andrés S, Santamarina Rabanal M, Granda Membriela C, Fernández Gutiérrez M, Sirgo Rodríguez P, Álvarez Marcos C. Swallowing disorders in Parkinson’s disease. Acta Otorinolaryngol Española. 2017;68:15–22.

    Article  Google Scholar 

  18. Chou KL, Evatt M, Hinson V, Kompoliti K. Sialorrhea in Parkinson’s disease: a review. Mov Disord. 2007;22(16):2306–13.

    Article  PubMed  Google Scholar 

  19. Rodrigues B, Nóbrega AC, Sampaio M, Argolo N, Melo A. Silent saliva aspiration in Parkinson’s disease. Mov Disord. 2010;26(1):138–41.

    Article  PubMed  Google Scholar 

  20. 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 

  21. Janssens T, Silva M, Davenport PW, Van Diest I, Dupont LJ, Van Den Bergh O. Attentional modulation of reflex cough. Chest. 2014;146(1):135–41.

    Article  PubMed  Google Scholar 

  22. Perry SE, Troche MS. Dual tasking influences cough sensorimotor outcomes in healthy young adults. J Speech Lang Hear Res. 2019;62(9):3596–606.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  24. Davenport PW. Urge-to-cough: what can it teach us about cough? Lung. 2008;186(SUPPL. 1):107–11.

    Article  Google Scholar 

  25. Beck A, Ward C, Mendelsohn M, Mock J, Erbaugh J. An inventory for measuring depression. Arch Gen Psychiatry. 1961;4:561–71.

    Article  CAS  PubMed  Google Scholar 

  26. Nasreddine Z, et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc. 2005;53(4):695–9.

    Article  PubMed  Google Scholar 

  27. Julayanont P, Brousseau M, Chertkow H, Phillips N, Nasreddine ZS. Montreal Cognitive Assessment Memory Index Score (MoCA-MIS) as a predictor of conversion from mild cognitive impairment to Alzheimer’s disease. J Am Geriatr Soc. 2014;62(4):679–84.

    Article  PubMed  Google Scholar 

  28. Jensen AR. Scoring the Stroop test. Acta Psychol (Amst). 1965;24:398–408.

    Article  Google Scholar 

  29. Werheid K, Hoppe C, Thone A, Muller U, Mungersdorf M, von Cramon D. The Adaptive Digit Ordering Test: clinical application, reliability, and validity of a verbal working memory test. Arch Clin Neuropsychol. 2002;17(6):547–65.

    Article  PubMed  Google Scholar 

  30. Lezak M, Howieson D, Loring D. Neuropsychological assessment. 4th ed. New York: Oxford University Press; 2004.

    Google Scholar 

  31. Vovk A, et al. Capsaicin exposure elicits complex airway defensive motor patterns in normal humans in a concentration-dependent manner. Pulm Pharmacol Ther. 2007;20(4):423–32.

    Article  CAS  PubMed  Google Scholar 

  32. Pecova R, Javorkova N, Kudlicka J, Tatar M. Tussigenic agents in the measurement of cough reflex sensitivity. J Physiol Pharmacol. 2007;58(Suppl 5):531–8.

    PubMed  Google Scholar 

  33. Davenport PW, Vovk A. Cortical and subcortical central neural pathways in respiratory sensations. Respir Physiol Neurobiol. 2009;167(1):72–86.

    Article  PubMed  Google Scholar 

  34. Morice A, Higgins K, Yeo W. Adaptation of cough reflex with different types of stimulation. Eur Respir J. 1992;5(10):1296–7.

    Article  Google Scholar 

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

    Article  Google Scholar 

  36. Portney L, Watkins M. Foundations of clinical research: applications to practice. New Jersey: Prentice Hall; 2000.

    Google Scholar 

  37. Brandimore AE, Troche MS, Hegland KW. The influence of age on perception of the urge-to-cough in healthy older adults. Biol Psychol. 2017;129(2017):380.

    Article  Google Scholar 

  38. Schaefer S, Schumacher V. The interplay between cognitive and motor functioning in healthy older adults: findings from dual-task studies and suggestions for intervention. Gerontology. 2011;57(3):239–46.

    Article  PubMed  Google Scholar 

  39. Plummer-D’Amato P, Altmann L, Saracino D, Fox E, Behrman A, Marsiskef M. Interactions between cognitive tasks and gait after stroke: a dual task study. Gait Posture. 2008;27(4):683–8.

    Article  PubMed  Google Scholar 

  40. Patel P, Bhatt T. Attentional demands of perturbation evoked compensatory stepping responses: examining cognitive-motor interference to large magnitude forward pertubations. J Mot Behav. 2015;47(3):201–10.

    Article  PubMed  Google Scholar 

  41. Janssens T, Brepoels S, Dupont L, Van den Bergh O. The impact of harmfulness information on citric acid induced cough and urge-to-cough. Pulm Pharmacol Ther. 2015;31:9–14.

    Article  CAS  PubMed  Google Scholar 

  42. Mosier KM, Liu WC, Maldjian JA, Shah R, Modi B. Lateralization of cortical function in swallowing: a functional MR imaging study. Am J Neuroradiol. 1999;20(8):1520–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Hamdy S, et al. Cortical activation during human volitional swallowing: an event-related fMRI study. Am J Physiol. 1999;277:G219–25.

    CAS  PubMed  Google Scholar 

  44. Farrell MJ, Cole LJ, Chiapoco D, Egan GF, Mazzone SB. Neural correlates coding stimulus level and perception of capsaicin-evoked urge-to-cough in humans. Neuroimage. 2012;61(4):1324–35.

    Article  PubMed  Google Scholar 

  45. Malandraki G, Johnson S, Robbins J. Functional MRI of swallowing: from neurophysiology to neuroplasticity. Head Neck. 2011;33:S14-20.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Malandraki GA, Sutton BP, Perlman AL, Karampinos DC, Conway C. Neural activation of swallowing and swallowing-related tasks in healthy young adults: an attempt to separate the components of deglutition. Hum Brain Mapp. 2009;30(10):3209–26.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Martin RE, Macintosh BJ, Smith RC, Barr AM, Stevens TK, Gati JS. Cerebral areas processing swallowing and tongue movement are overlapping but distinct: a functional magnetic resonance imaging study. J Neurophysiol. 2004;92(4):2428–43.

    Article  PubMed  Google Scholar 

  48. Martin RE, Goodyear BG, Gati JS, Menon RS. Cerebral cortical representation of automatic and volitional swallowing in humans. J Neurophysiol. 2001;85(2):938–50.

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  50. Nieuwhof F, et al. Impaired dual tasking in Parkinson’s disease is associated with reduced focusing of cortico-striatal activity. Brain. 2017;140(5):1384–98.

    Article  PubMed  Google Scholar 

  51. Tombu M, Jolicoæur P. A central capacity sharing model of dual-task performance. J Exp Psychol Hum Percept Perform. 2003;29(1):3–18.

    Article  PubMed  Google Scholar 

  52. Paas F. Training strategies for attaining transfer of problem-solving skill in statistics: a cognitive load approach. J Educ Psychol. 1992;84(4):429–34.

    Article  Google Scholar 

  53. Langmore S, et al. Predictors of aspiration pneumonia: how important is dysphagia? Dysphagia. 1998;13(2):69–81.

    Article  CAS  PubMed  Google Scholar 

  54. Ebihara S, et al. Impaired efficacy of cough in patients with Parkinson disease. Chest. 2003;124(3):1009–15.

    Article  PubMed  Google Scholar 

  55. Reilly CA, Johansen ME, Lanza DL, Lee J, Lim J-O, Yost G. Calcium-dependent and independent mechanisms of capsaicin receptor (TRPV1)-mediated cytokine production and cell death in human bronchial epithelial cells. J Biochem Mol Toxicol. 2005;19(4):266–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Reilly CA, Taylor JL, Lanza DL, Carr BA, Crouch DJ, Yost G. Capsaicinoids cause inflammation and epithelial cell death through activation of vanilloid receptors. Toxicol Sci. 2003;73(1):170–81.

    Article  CAS  PubMed  Google Scholar 

  57. Morice A, et al. ERS guidelines on the assessment of cough. Eur Respir J. 2007;29(6):1256–76.

    Article  CAS  PubMed  Google Scholar 

  58. Carleton R, Abrams M, Asmundson G. The Attentional Resource Allocation Scale (ARAS): psychometric properties of a composite measure for dissociation and absorption. Depress Anxiety. 2010;27(8):775–86.

    Article  CAS  PubMed  Google Scholar 

  59. Robertson I, Ward T, Ridgeway V, Nimmo-Smith I. The structure of normal human attention: the test of everyday attention. J Int Neuropsychol Soc. 1996;2(6):525–34.

    Article  CAS  PubMed  Google Scholar 

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Funding

This study was funded by an ASHFoundation New Investigator’s Research Grant.

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Authors and Affiliations

  1. Laboratory for the Study of Upper Airway Dysfunction, Teachers College, Columbia University, New York, NY, USA

    Sarah E. Perry & Michelle S. Troche

  2. New Zealand Brain Research Institute, Christchurch, New Zealand

    Sarah E. Perry

  3. University of Canterbury Rose Centre for Stroke Recovery & Research at St George’s Medical Centre, Christchurch, New Zealand

    Sarah E. Perry

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  1. Sarah E. Perry
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Correspondence to Sarah E. Perry.

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S. Perry and M. Troche confirm that they have no relevant conflicts of interest to disclose.

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Perry, S.E., Troche, M.S. Dual Tasking Influences Cough Reflex Outcomes in Adults with Parkinson’s Disease: A Controlled Study. Dysphagia 36, 959–973 (2021). https://doi.org/10.1007/s00455-020-10223-x

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