pp 1–8 | Cite as

Relationship Between Laryngeal Sensation, Length of Intubation, and Aspiration in Patients with Acute Respiratory Failure

  • James C. BordersEmail author
  • Daniel Fink
  • Joseph E. Levitt
  • Jeffrey McKeehan
  • Edel McNally
  • Alix Rubio
  • Rebecca Scheel
  • Jonathan M. Siner
  • Stephanie Gomez Taborda
  • Rosemary Vojnik
  • Heather Warner
  • S. David White
  • Susan E. Langmore
  • Marc Moss
  • Gintas P. Krisciunas
Original Article


Dysphagia is common in hospitalized patients post-extubation and associated with poor outcomes. Laryngeal sensation is critical for airway protection and safe swallowing. However, current understanding of the relationship between laryngeal sensation and aspiration in post-extubation populations is limited. Acute respiratory failure patients requiring intensive care unit admission and mechanical ventilation received a Flexible Endoscopic Evaluation of Swallowing (FEES) within 72 h of extubation. Univariate and multivariable analyses were performed to examine the relationship between laryngeal sensation, length of intubation, and aspiration. Secondary outcomes included pharyngolaryngeal secretions, pneumonia, and diet recommendations. One-hundred and three patients met inclusion criteria. Fifty-one patients demonstrated an absent laryngeal adductor reflex (LAR). Altered laryngeal sensation correlated with the presence of secretions (p = 0.004). There was a significant interaction between the LAR, aspiration, and duration of mechanical ventilation. Altered laryngeal sensation was significantly associated with aspiration on FEES only in patients with a shorter length of intubation (p = 0.008). Patients with altered laryngeal sensation were prescribed significantly more restricted liquid (p = 0.03) and solid (p = 0.001) diets. No relationship was found between laryngeal sensation and pneumonia. There is a high prevalence of laryngeal sensory deficits in mechanically ventilated patients post-extubation. Altered laryngeal sensation was associated with secretions, aspiration, and modified diet recommendations especially in those patients with a shorter length of mechanical ventilation. These results demonstrate that laryngeal sensory abnormalities impact the development of post-extubation dysphagia.


Deglutition Deglutition disorders Laryngeal sensation FEES Acute respiratory failure Critical illness 



National Institutes of Health (Grant Number: R21NR015886) provided funding for this study.

Compliance with Ethical Standards

Conflicts of interest

All authors declare that they have no conflict of interest.

Ethical Approval

All procedures performed were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Approval was obtained from each site’s Institutional Review Board.

Informed Consent

Informed consent was obtained from all participants prior to enrollment in this research study.


  1. 1.
    Wunsch H, Linde-Zwirble WT, Angus DC, Hartman ME, Milbrandt EB, Kahn JM. The epidemiology of mechanical ventilation use in the United States. Crit Care Med. 2010;38(10):1947–53.CrossRefGoogle Scholar
  2. 2.
    Skoretz SA, Flowers HL, Martino R. The incidence of dysphagia following endotracheal intubation: a systematic review. Chest. 2010;137(3):665–73.CrossRefGoogle Scholar
  3. 3.
    Macht M, Wimbish T, Clark BJ, Benson AB, Burnham EL, Williams A, et al. Postextubation dysphagia is persistent and associated with poor outcomes in survivors of critical illness. Crit Care. 2011;15(5):R231.CrossRefGoogle Scholar
  4. 4.
    Brodsky MB, Huang M, Shanholtz C, Mendez-Tellez PA, Palmer JB, Colantuoni E, et al. Recovery from Dysphagia Symptoms after Oral Endotracheal Intubation in Acute Respiratory Distress Syndrome Survivors. A 5-Year Longitudinal Study. Ann Am Thorac Soc. 2017;14(3):376–83.CrossRefGoogle Scholar
  5. 5.
    Macht M, Wimbish T, Bodine C, Moss M. ICU-acquired swallowing disorders. Crit Care Med. 2013;41(10):2396–405.CrossRefGoogle Scholar
  6. 6.
    Leder SB, Suiter DM, Lisitano Warner H. Answering orientation questions and following single-step verbal commands: effect on aspiration status. Dysphagia. 2009;24(3):290–5.CrossRefGoogle Scholar
  7. 7.
    Metheny NA, Clouse RE, Chang YH, Stewart BJ, Oliver DA, Kollef MH. Tracheobronchial aspiration of gastric contents in critically ill tube-fed patients: frequency, outcomes, and risk factors. Crit Care Med. 2006;34(4):1007–15.CrossRefGoogle Scholar
  8. 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.CrossRefGoogle Scholar
  9. 9.
    Shaker R, Li Q, Ren J, Townsend WF, Dodds WJ, Martin BJ, et al. Coordination of deglutition and phases of respiration: effect of aging, tachypnea, bolus volume, and chronic obstructive pulmonary disease. Am J Physiol. 1992;263:G750–5.CrossRefGoogle Scholar
  10. 10.
    Colton House J, Noordzij JP, Murgia B, Langmore S. Laryngeal injury from prolonged intubation: a prospective analysis of contributing factors. Laryngoscope. 2011;121(3):596–600.CrossRefGoogle Scholar
  11. 11.
    Scheel R, Pisegna JM, McNally E, Noordzij JP, Langmore SE. Endoscopic assessment of swallowing after prolonged intubation in the ICU setting. Ann Otol Rhinol Laryngol. 2016;125(1):43–52.CrossRefGoogle Scholar
  12. 12.
    Su H, Hsiao TY, Ku SC, Wang TG, Lee JJ, Tzeng WC, et al. Tongue weakness and somatosensory disturbance following oral endotracheal extubation. Dysphagia. 2015;30(2):188–95.CrossRefGoogle Scholar
  13. 13.
    Aviv JE, Spitzer J, Cohen M, Ma G, Belafsky P, Close LG. Laryngeal adductor reflex and pharyngeal squeeze as predictors of laryngeal penetration and aspiration. Laryngoscope. 2002;112(2):338–41.CrossRefGoogle Scholar
  14. 14.
    Langmore SE, Schatz K, Olsen N. Fiberoptic endoscopic examination of swallowing safety: a new procedure. Dysphagia. 1988;2(4):216–9.CrossRefGoogle Scholar
  15. 15.
    Domer AS, Kuhn MA, Belafsky PC. Neurophysiology and clinical implications of the laryngeal adductor reflex. Curr Otorhinolaryngol Rep. 2013;1(3):178–82.CrossRefGoogle Scholar
  16. 16.
    Jafari S, Prince RA, Kim DY, Paydarfar D. Sensory regulation of swallowing and airway protection: a role for the internal superior laryngeal nerve in humans. J Physiol. 2003;550(Pt 1):287–304.CrossRefGoogle Scholar
  17. 17.
    Barkmeier JM, Bielamowicz S, Takeda N, Ludlow CL. Modulation of laryngeal responses to superior laryngeal nerve stimulation by volitional swallowing in awake humans. J Neurophysiol. 2000;83(3):1264–72.CrossRefGoogle Scholar
  18. 18.
    Onofri SM, Cola PC, Berti LC, da Silva RG, Dantas RO. Correlation between laryngeal sensitivity and penetration/aspiration after stroke. Dysphagia. 2014;29(2):256–61.CrossRefGoogle Scholar
  19. 19.
    Murray J, Langmore SE, Ginsberg S, Dostie A. The significance of accumulated oropharyngeal secretions and swallowing frequency in predicting aspiration. Dysphagia. 1996;11(2):99–103.CrossRefGoogle Scholar
  20. 20.
    Kaneoka A, Pisegna JM, Inokuchi H, Ueha R, Goto T, Nito T, et al. Relationship between laryngeal sensory deficits, aspiration, and pneumonia in patients with dysphagia. Dysphagia. 2017;33:192–9.CrossRefGoogle Scholar
  21. 21.
    Rosenbek JC, Robbins JA, Roecker EB, Coyle JL, Wood JL. A penetration-aspiration scale. Dysphagia. 1996;11(2):93–8.CrossRefGoogle Scholar
  22. 22.
    Donzelli J, Brady S, Wesling M, Craney M. Predictive value of accumulated oropharyngeal secretions for aspiration during video nasal endoscopic evaluation of the swallow. Ann Otol Rhinol Laryngol. 2003;112(5):469–75.CrossRefGoogle Scholar
  23. 23.
    Brodsky MB, De I, Chilukuri K, Huang M, Palmer JB, Needham DM. Coordination of pharyngeal and laryngeal swallowing events during single liquid swallows after oral endotracheal intubation for patients with acute respiratory distress syndrome. Dysphagia. 2018;33(6):768–77.CrossRefGoogle Scholar
  24. 24.
    Rousou JA, Tighe DA, Garb JL, Krasner H, Engelman RM, Flack JE, et al. Risk of dysphagia after transesophageal echocardiography during cardiac operations. Ann Thorac Surg. 2000;69(2):486–9.CrossRefGoogle Scholar
  25. 25.
    Barker J, Martino R, Reichardt B, Hickey EJ, Ralph-Edwards A. Incidence and impact of dysphagia in patients receiving prolonged endotracheal intubation after cardiac surgery. Can J Surg. 2009;52(2):119–24.Google Scholar
  26. 26.
    Brown CV, Hejl K, Mandaville AD, Chaney PE, Stevenson G, Smith C. Swallowing dysfunction after mechanical ventilation in trauma patients. J Crit Care. 2011;26(1):108.e9–13.CrossRefGoogle Scholar
  27. 27.
    Kwok AM, Davis JW, Cagle KM, Sue LP, Kaups KL. Post-extubation dysphagia in trauma patients: it’s hard to swallow. Am J Surg. 2013;206(6):924–7.CrossRefGoogle Scholar
  28. 28.
    Brodsky MB, González-Fernández M, Mendez-Tellez PA, Shanholtz C, Palmer JB, Needham DM. Factors associated with swallowing assessment after oral endotracheal intubation and mechanical ventilation for acute lung injury. Ann Am Thorac Soc. 2014;11(10):1545–52.CrossRefGoogle Scholar
  29. 29.
    Bordon A, Bokhari R, Sperry J, Testa D, Feinstein A, Ghaemmaghami V. Swallowing dysfunction after prolonged intubation: analysis of risk factors in trauma patients. Am J Surg. 2011;202(6):679–82.CrossRefGoogle Scholar
  30. 30.
    Skoretz SA, Yau TM, Ivanov J, Granton JT, Martino R. Dysphagia and associated risk factors following extubation in cardiovascular surgical patients. Dysphagia. 2014;29(6):647–54.CrossRefGoogle Scholar
  31. 31.
    Ajemian MS, Nirmul GB, Anderson MT, Zirlen DM, Kwasnik EM. Routine fiberoptic endoscopic evaluation of swallowing following prolonged intubation: implications for management. Arch Surg. 2001;136(4):434–7.CrossRefGoogle Scholar
  32. 32.
    El Solh A, Okada M, Bhat A, Pietrantoni C. Swallowing disorders post orotracheal intubation in the elderly. Intensive Care Med. 2003;29(9):1451–5.CrossRefGoogle Scholar
  33. 33.
    Barquist E, Brown M, Cohn S, Lundy D, Jackowski J. Postextubation fiberoptic endoscopic evaluation of swallowing after prolonged endotracheal intubation: a randomized, prospective trial. Crit Care Med. 2001;29(9):1710–3.CrossRefGoogle Scholar
  34. 34.
    Marvin S, Thibeault S, Ehlenbach WJ. Post-extubation Dysphagia: Does timing of evaluation matter? Dysphagia. 2018. Scholar
  35. 35.
    Kaneoka A, Pisegna JM, Krisciunas GP, Nito T, LaValley MP, Stepp CE, et al. Variability of the pressure measurements exerted by the tip of laryngoscope during laryngeal sensory testing: a clinical demonstration. Am J Speech Lang Pathol. 2017;26(3):729–36.CrossRefGoogle Scholar
  36. 36.
    Hammer MJ. Design of a new somatosensory stimulus delivery device for measuring laryngeal mechanosensory detection thresholds in humans. IEEE Trans Biomed Eng. 2009;56(4):1154–9.CrossRefGoogle Scholar
  37. 37.
    Kaneoka A, Krisciunas GP, Walsh K, Raade AS, Langmore SE. A comparison of 2 methods of endoscopic laryngeal sensory testing: a preliminary study. Ann Otol Rhinol Laryngol. 2015;124(3):187–93.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • James C. Borders
    • 1
    Email author
  • Daniel Fink
    • 2
  • Joseph E. Levitt
    • 3
  • Jeffrey McKeehan
    • 4
  • Edel McNally
    • 1
  • Alix Rubio
    • 5
  • Rebecca Scheel
    • 1
  • Jonathan M. Siner
    • 6
  • Stephanie Gomez Taborda
    • 5
  • Rosemary Vojnik
    • 3
  • Heather Warner
    • 7
    • 8
  • S. David White
    • 9
  • Susan E. Langmore
    • 5
    • 10
  • Marc Moss
    • 11
  • Gintas P. Krisciunas
    • 5
  1. 1.Department of OtolaryngologyBoston University Medical CenterBostonUSA
  2. 2.Department of OtolaryngologyUniversity of Colorado DenverAuroraUSA
  3. 3.Division of Pulmonary and Critical CareStanford UniversityStanfordUSA
  4. 4.University of Colorado HospitalAuroraUSA
  5. 5.Department of OtolaryngologyBoston University School of MedicineBostonUSA
  6. 6.Section of Pulmonary, Critical Care, and Sleep MedicineYale University School of MedicineNew HavenUSA
  7. 7.Department of Surgery, Section of OtolaryngologyYale School of MedicineNew HavenUSA
  8. 8.Department of Communication DisordersSouthern Connecticut State UniversityNew HavenUSA
  9. 9.Rehabilitation Therapy ServicesUniversity of Colorado HospitalAuroraUSA
  10. 10.Sargent College of Health and Rehabilitation SciencesBoston UniversityBostonUSA
  11. 11.Division of Pulmonary Sciences and Critical Care MedicineUniversity of Colorado DenverAuroraUSA

Personalised recommendations