Advertisement

Dysphagia

, Volume 29, Issue 6, pp 637–646 | Cite as

Associations Between Laryngeal and Cough Dysfunction in Motor Neuron Disease with Bulbar Involvement

  • Deanna BrittonEmail author
  • Joshua O. Benditt
  • Albert L. Merati
  • Robert M. Miller
  • Cara E. Stepp
  • Louis Boitano
  • Amanda Hu
  • Marcia A. Ciol
  • Kathryn M. Yorkston
Original Article

Abstract

True vocal fold (TVF) dysfunction may lead to cough ineffectiveness. In individuals with motor neuron disease (MND), cough impairment in the context of dysphagia increases risk for aspiration and respiratory failure. This study characterizes differences and associations between TVF kinematics and airflow during cough in individuals with bulbar MND. Sequential glottal angles associated with TVF movements during volitional cough were analyzed from laryngeal video endoscopy examinations of adults with bulbar MND (n = 12) and healthy controls (n = 12) and compared with simultaneously collected cough-related airflow measures. Significant group differences were observed with airflow and TVF measures: volume acceleration (p ≤ 0.001) and post-compression abduction TVF angle average velocity (p = 0.002) were lower and expiratory phase rise time (p = 0.001) was higher in the MND group. Reductions in maximum TVF angle during post-compression abduction in the MND group approached significance (p = 0.09). All subjects demonstrated complete TVF and supraglottic closure during the compression phase of cough, except for incomplete supraglottic closure in 2/12 MND participants. A strong positive relationship between post-compression maximum TVF abduction angle and peak expiratory cough flow was observed in the MND group, though it was not statistically significant (r = 0.55; p = 0.098). Reductions in the speed and extent of TVF abduction are seen during the expulsion phase of cough in individuals with MND. This may contribute to cough impairment and morbidity.

Keywords

Motor neuron disease (MND) Cough Laryngeal function True vocal folds (TVFs) Amyotrophic lateral sclerosis (ALS) Primary lateral sclerosis (PLS) Deglutition Deglutition disorders 

Notes

Acknowledgments

We thank the individuals with MND and healthy control participants who took part in this study. Many thanks also to James Kobler, PhD, Harvard Medical School, for the use of his custom angle-marking Matlab code. In addition, many thanks to Carolyn Baylor, PhD, for her help and expertise with reliability measures. This study was supported by NIH/NIDCD F31 DC011689 (2011–2012) and in part by the Walter C. and Anita C. Stolov Research Fund (2010–2011).

Conflict of interest

The authors have no conflicts of interest to declare.

References

  1. 1.
    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.PubMedCrossRefGoogle Scholar
  2. 2.
    Smith Hammond CA, Goldstein LB, Horner RD, Ying J, Gray L, Gonzalez-Rothi L, et al. Predicting aspiration in patients with ischemic stroke: comparison of clinical signs and aerodynamic measures of voluntary cough. Chest. 2009;135(3):769–77.PubMedCrossRefGoogle Scholar
  3. 3.
    Addington WR, Stephens RE, Gilliland K, Rodriguez M. Assessing the laryngeal cough reflex and the risk of developing pneumonia after stroke. Arch Phys Med Rehabil. 1999;80(2):150–4.PubMedCrossRefGoogle Scholar
  4. 4.
    Addington WR, Stephens RE, Gilliland KA. Assessing the laryngeal cough reflex and the risk of developing pneumonia after stroke: an interhospital comparison. Stroke. 1999;30(6):1203–7.PubMedCrossRefGoogle Scholar
  5. 5.
    Addington WR, Stephens RE, Widdicombe JG, Rekab K. Effect of stroke location on the laryngeal cough reflex and pneumonia risk. Cough. 2005;1:4.PubMedCentralPubMedCrossRefGoogle Scholar
  6. 6.
    Pitts T, Bolser D, Rosenbek J, Troche M, Sapienza C. Voluntary cough production and swallow dysfunction in Parkinson’s disease. Dysphagia. 2008;23(3):297–301.PubMedCentralPubMedCrossRefGoogle Scholar
  7. 7.
    Benditt JO. Respiratory complications of amyotrophic lateral sclerosis. Semin Respir Crit Care Med. 2002;23(3):239–47.PubMedCrossRefGoogle Scholar
  8. 8.
    Benditt JO, Boitano L. Respiratory treatment of amyotrophic lateral sclerosis. Phys Med Rehabil Clin N Am. 2008;19(3):559–72 x.PubMedCrossRefGoogle Scholar
  9. 9.
    Boitano LJ. Management of airway clearance in neuromuscular disease. Respir Care. 2006;51(8):913–24.PubMedGoogle Scholar
  10. 10.
    Polkey MI, Lyall RA, Green M. Nigel Leigh P, Moxham J. Expiratory muscle function in amyotrophic lateral sclerosis. Am J Respir Crit Care Med. 1998;158(3):734–41.PubMedCrossRefGoogle Scholar
  11. 11.
    Park JH, Kang SW, Lee SC, Choi WA, Kim DH. How respiratory muscle strength correlates with cough capacity in patients with respiratory muscle weakness. Yonsei Med J. 2010;51(3):392–7.PubMedCentralPubMedCrossRefGoogle Scholar
  12. 12.
    Hadjikoutis S, Wiles CM. Respiratory complications related to bulbar dysfunction in motor neuron disease. Acta Neurol Scand. 2001;103:207–13.PubMedCrossRefGoogle Scholar
  13. 13.
    Chaudri MB, Liu C, Hubbard R, Jefferson D, Kinnear WJ. Relationship between supramaximal flow during cough and mortality in motor neurone disease. Eur Respir J. 2002;19(3):434–8.PubMedCrossRefGoogle Scholar
  14. 14.
    Suarez AA, Pessolano FA, Monteiro SG, Ferreyra G, Capria ME, Mesa L, et al. Peak flow and peak cough flow in the evaluation of expiratory muscle weakness and bulbar impairment in patients with neuromuscular disease. Am J Phys Med Rehabil. 2002;81(7):506–11.PubMedCrossRefGoogle Scholar
  15. 15.
    Hadjikoutis S, Wiles CM. Respiratory complications related to bulbar dysfunction in motor neuron disease. Acta Neurol Scand. 2001;103(4):207–13.PubMedCrossRefGoogle Scholar
  16. 16.
    Sancho J, Servera E, Diaz J, Marin J. Predictors of ineffective cough during a chest infection in patients with stable amyotrophic lateral sclerosis. Am J Respir Crit Care Med. 2007;175(12):1266–71.PubMedCrossRefGoogle Scholar
  17. 17.
    Hillel AD, Miller R. Bulbar amyotrophic lateral sclerosis: patterns of progression and clinical management. Head Neck. 1989;11(1):51–9.PubMedCrossRefGoogle Scholar
  18. 18.
    Chen A, Garrett CG. Otolaryngologic presentations of amyotrophic lateral sclerosis. Otolaryngol Head Neck Surg. 2005;132(3):500–4.PubMedCrossRefGoogle Scholar
  19. 19.
    Forshew DA, Bromberg MB. A survey of clinicians’ practice in the symptomatic treatment of ALS. Amyotroph Lateral Scler Other Motor Neuron Disord. 2003;4(4):258–63.PubMedCrossRefGoogle Scholar
  20. 20.
    van der Graaff MM, Grolman W, Westermann EJ, Boogaardt HC, Koelman H, van der Kooi AJ, et al. Vocal cord dysfunction in amyotrophic lateral sclerosis: four cases and a review of the literature. Arch Neurol. 2009;66(11):1329–33.PubMedGoogle Scholar
  21. 21.
    Murakami Y, Yagi M, Mizuon M, Nomura Y. A histochemical study of the intrinsic laryngeal muscles in amyotrophic lateral sclerosis (ALS). Abstr VIth World Congr Bronchoesophagol. 1990;5(3):171.Google Scholar
  22. 22.
    Vincken W, Elleker G, Cosio MG. Detection of upper airway muscle involvement in neuromuscular disorders using the flow-volume loop. Chest. 1986;90(1):52–7.PubMedCrossRefGoogle Scholar
  23. 23.
    Hadjikoutis S, Wiles CM. Respiratory complications related to bulbar dysfunction in motor neuron disease. Acta Neurol Scand. 2001;103(4):207–13.PubMedCrossRefGoogle Scholar
  24. 24.
    Farrero E, Prats E, Povedano M, Martinez-Matos JA, Manresa F, Escarrabill J. Survival in amyotrophic lateral sclerosis with home mechanical ventilation: the impact of systematic respiratory assessment and bulbar involvement. Chest. 2005;127(6):2132–8.PubMedCrossRefGoogle Scholar
  25. 25.
    Bourke SC, Bullock RE, Williams TL, Shaw PJ, Gibson GJ. Noninvasive ventilation in ALS: indications and effect on quality of life. Neurology. 2003;61(2):171–7.PubMedCrossRefGoogle Scholar
  26. 26.
    Brooks BR, Miller RG, Swash M, Munsat TL. World Federation of Neurology Research Group on Motor Neuron Diseases. El escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord. 2000;1(5):293–9.PubMedCrossRefGoogle Scholar
  27. 27.
    Pringle CE, Hudson AJ, Munoz DG, Kiernan JA, Brown WF, Ebers GC. Primary lateral sclerosis. Clinical features, neuropathology and diagnostic criteria. Brain. 1992;115(Pt 2):495–520.PubMedCrossRefGoogle Scholar
  28. 28.
    Cedarbaum JM, Stambler N, Malta E, Fuller C, Hilt D, Thurmond B, et al. The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J Neurol Sci. 1999;169(1–2):13–21.PubMedCrossRefGoogle Scholar
  29. 29.
    Britton D, Yorkston KM, Eadie T, Stepp CE, Ciol MA, Baylor C, et al. Endoscopic assessment of vocal fold movements during cough. Ann Otol Rhinol Laryngol. 2012;121(1):21–7.PubMedCrossRefGoogle Scholar
  30. 30.
    Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psychol Bull. 1979;86(2):420–8.PubMedCrossRefGoogle Scholar
  31. 31.
    Hankinson JL, Odencrantz JR, Fedan KB. Spirometric reference values from a sample of the general U.S. population. Am J Respir Crit Care Med. 1999;159(1):179–87.PubMedCrossRefGoogle Scholar
  32. 32.
    Kang SW, Bach JR. Maximum insufflation capacity: vital capacity and cough flows in neuromuscular disease. Am J Phys Med Rehabil. 2000;79(3):222–7.PubMedCrossRefGoogle Scholar
  33. 33.
    Bach JR. Amyotrophic lateral sclerosis: predictors for prolongation of life by noninvasive respiratory aids. Arch Phys Med Rehabil. 1995;76:828–32.PubMedCrossRefGoogle Scholar
  34. 34.
    Smith-Hammond C. Cough and aspiration of food and liquids due to oral pharyngeal dysphagia. Lung. 2008;186(Suppl 1):S35–40.PubMedCrossRefGoogle Scholar
  35. 35.
    Hillel AD. The study of laryngeal muscle activity in normal human subjects and in patients with laryngeal dystonia using multiple fine-wire electromyography. Laryngoscope. 2001;111((4 Pt 2 Suppl 97)):1–47.PubMedCrossRefGoogle Scholar
  36. 36.
    Young S, Abdul-Sattar N, Caric D. Glottic closure and high flows are not essential for productive cough. Bull Eur Physiopathol Respir. 1987;23(Suppl 10):11s–7s.PubMedGoogle Scholar
  37. 37.
    Murty GE, Kelly PJ, Bradley PJ. Tussometry: an objective assessment of vocal cord function. Ann Otol Rhinol Laryngol. 1993;102(10):743–7.PubMedCrossRefGoogle Scholar
  38. 38.
    Mahajan RP, Singh P, Murty GE, Aitkenhead AR. Relationship between expired lung volume, peak flow rate and peak velocity time during a voluntary cough manoeuvre. Br J Anaesth. 1994;72(3):298–301.PubMedCrossRefGoogle Scholar
  39. 39.
    Suleman M, Abaza KT, Gornall C, Kinnear WJ, Wills JS, Mahajan RP. The effect of a mechanical glottis on peak expiratory flow rate and time to peak flow during a peak expiratory flow manoeuvre: a study in normal subjects and patients with motor neurone disease. Anaesthesia. 2004;59(9):872–5.PubMedCrossRefGoogle Scholar
  40. 40.
    Slaton RM, Thomas RH, Mbathi JW. Evidence for therapeutic uses of nebulized lidocaine in the treatment of intractable cough and asthma. Ann Pharmacother. 2013;47(4):578–85.PubMedCrossRefGoogle Scholar
  41. 41.
    Lim KG, Rank MA, Hahn PY, Keogh KA, Morgenthaler TI, Olson EJ. Long-term safety of nebulized lidocaine for adults with difficult-to-control chronic cough: a case series. Chest. 2013;143(4):1060–5.PubMedCrossRefGoogle Scholar
  42. 42.
    Mahajan RP, Murty GE, Singh P, Aitkenhead AR. Effect of topical anaesthesia on the motor performance of vocal cords as assessed by tussometry. Anaesthesia. 1994;49(12):1028–30.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Deanna Britton
    • 1
    Email author
  • Joshua O. Benditt
    • 2
  • Albert L. Merati
    • 3
  • Robert M. Miller
    • 4
  • Cara E. Stepp
    • 5
  • Louis Boitano
    • 6
  • Amanda Hu
    • 7
  • Marcia A. Ciol
    • 1
  • Kathryn M. Yorkston
    • 1
  1. 1.Department of Rehabilitation MedicineUniversity of WashingtonSeattleUSA
  2. 2.Division of Pulmonary and Critical Care MedicineUniversity of Washington Medical Center (UWMC)SeattleUSA
  3. 3.Laryngology, Otolaryngology – Head and Neck SurgeryUniversity of Washington Medical Center (UWMC)SeattleUSA
  4. 4.Department of Speech and Hearing SciencesUniversity of WashingtonSeattleUSA
  5. 5.Speech, Language & Hearing Sciences, and Biomedical EngineeringBoston UniversityBostonUSA
  6. 6.Pulmonary/Medicine Specialties ClinicUniversity of Washington Medical Center (UWMC)SeattleUSA
  7. 7.Department of Otolaryngology – Head and Neck SurgeryDrexel University College of MedicinePhiladelphiaUSA

Personalised recommendations