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Coordination of Pharyngeal and Laryngeal Swallowing Events During Single Liquid Swallows After Oral Endotracheal Intubation for Patients with Acute Respiratory Distress Syndrome

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Abstract

To evaluate timing and duration differences in airway protection and esophageal opening after oral intubation and mechanical ventilation for acute respiratory distress syndrome (ARDS) survivors versus age-matched healthy volunteers. Orally intubated adult (≥ 18 years old) patients receiving mechanical ventilation for ARDS were evaluated for swallowing impairments via a videofluoroscopic swallow study (VFSS) during usual care. Exclusion criteria were tracheostomy, neurological impairment, and head and neck cancer. Previously recruited healthy volunteers (n = 56) served as age-matched controls. All subjects were evaluated using 5-ml thin liquid barium boluses. VFSS recordings were reviewed frame-by-frame for the onsets of 9 pharyngeal and laryngeal events during swallowing. Eleven patients met inclusion criteria, with a median (interquartile range [IQR]) intubation duration of 14 (9, 16) days, and VFSSs completed a median of 5 (4, 13) days post-extubation. After arrival of the bolus in the pharynx, ARDS patients achieved maximum laryngeal closure a median (IQR) of 184 (158, 351) ms later than age-matched, healthy volunteers (p < 0.001) and it took longer to achieve laryngeal closure with a median (IQR) difference of 151 (103, 217) ms (p < 0.001), although there was no significant difference in duration of laryngeal closure. Pharyngoesophageal segment opening was a median (IQR) of − 116 (− 183, 1) ms (p = 0.004) shorter than in age-matched, healthy controls. Evaluation of swallowing physiology after oral endotracheal intubation in ARDS patients demonstrates slowed pharyngeal and laryngeal swallowing timing, suggesting swallow-related muscle weakness. These findings may highlight specific areas for further evaluation and potential therapeutic intervention to reduce post-extubation aspiration.

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References

  1. Adhikari NK, Fowler RA, Bhagwanjee S, Rubenfeld GD. Critical care and the global burden of critical illness in adults. Lancet. 2010;376(9749):1339–46.

    Article  Google Scholar 

  2. Wunsch H, Angus DC, Harrison DA, et al. Variation in critical care services across North America and Western Europe. Crit Care Med. 2008;36(10):2787–2793; e2781–2789.

    Article  Google Scholar 

  3. Angus DC, Shorr AF, White A, Dremsizov TT, Schmitz RJ, Kelley MA. Critical care delivery in the United States: distribution of services and compliance with Leapfrog recommendations. Crit Care Med. 2006;34(4):1016–24.

    Article  Google Scholar 

  4. Higgins TL, Kramer AA, Nathanson BH, Copes W, Stark M, Teres D. Prospective validation of the intensive care unit admission mortality probability model (MPM0-III). Crit Care Med. 2009;37(5):1619–23.

    Article  Google Scholar 

  5. Zilberberg MD, de Wit M, Pirone JR, Shorr AF. Growth in adult prolonged acute mechanical ventilation: implications for healthcare delivery. Crit Care Med. 2008;36(5):1451–5.

    Article  Google Scholar 

  6. Zilberberg MD, de Wit M, Shorr AF. Accuracy of previous estimates for adult prolonged acute mechanical ventilation volume in 2020: update using 2000–2008 data. Crit Care Med. 2012;40(1):18–20.

    Article  Google Scholar 

  7. Puthucheary ZA, Rawal J, McPhail M, et al. Acute skeletal muscle wasting in critical illness. JAMA. 2013;310(15):1591–600.

    Article  CAS  Google Scholar 

  8. Demoule A, Jung B, Prodanovic H, et al. Diaphragm dysfunction on admission to the intensive care unit. Prevalence, risk factors, and prognostic impact-a prospective study. Am J Respir Crit Care Med. 2013;188(2):213–9.

    Article  Google Scholar 

  9. Dres M, Dube BP, Mayaux J, et al. Coexistence and impact of limb muscle and diaphragm weakness at time of liberation from mechanical ventilation in medical intensive care unit patients. Am J Respir Crit Care Med. 2017;195(1):57–66.

    Article  Google Scholar 

  10. Bass NH. The Neurology of Swallowing. In: Groher ME, editor. Dysphagia: diagnosis and management. Boston: Butterworth-Heinemann; 1997. p. 7–36.

    Google Scholar 

  11. Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev. 2001;81(2):929–69.

    Article  CAS  Google Scholar 

  12. Miller AJ. Deglutition. Physiol Rev. 1982;62(1):129–84.

    Article  CAS  Google Scholar 

  13. Skoretz SA, Flowers HL, Martino R. The incidence of dysphagia following endotracheal intubation: a systematic review. Chest. 2010;137(3):665–73.

    Article  Google Scholar 

  14. Brodsky MB, Gellar JE, Dinglas VD, et al. Duration of oral endotracheal intubation is associated with dysphagia symptoms in acute lung injury patients. J Crit Care. 2014;29(4):574–9.

    Article  Google Scholar 

  15. Macht M, King CJ, Wimbish T, et al. Post-extubation dysphagia is associated with longer hospitalization in survivors of critical illness with neurologic impairment. Crit Care. 2013;17(3):R119.

    Article  Google Scholar 

  16. Macht M, Wimbish T, Clark BJ, et al. Postextubation dysphagia is persistent and associated with poor outcomes in survivors of critical illness. Crit Care. 2011;15(5):R231.

    Article  Google Scholar 

  17. Langmore SE, Terpenning MS, Schork A, et al. Predictors of aspiration pneumonia: how important is dysphagia? Dysphagia. 1998;13(2):69–81.

    Article  CAS  Google Scholar 

  18. Martin BJ, Corlew MM, Wood H, et al. The association of swallowing dysfunction and aspiration pneumonia. Dysphagia. 1994;9(1):1–6.

    Article  CAS  Google Scholar 

  19. Bartlett JG, Gorbach SL. The triple threat of aspiration pneumonia. Chest. 1975;68(4):560–6.

    Article  CAS  Google Scholar 

  20. Marik PE. Aspiration pneumonitis and aspiration pneumonia. N Engl J Med. 2001;344(9):665–71.

    Article  CAS  Google Scholar 

  21. Kozlow JH, Berenholtz SM, Garrett E, Dorman T, Pronovost PJ. Epidemiology and impact of aspiration pneumonia in patients undergoing surgery in Maryland, 1999–2000. Crit Care Med. 2003;31(7):1930–7.

    Article  Google Scholar 

  22. Marik PE. Pulmonary aspiration syndromes. Curr Opin Pulm Med. 2011;17(3):148–54.

    Article  Google Scholar 

  23. 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.

    Article  CAS  Google Scholar 

  24. 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.

    PubMed  PubMed Central  Google Scholar 

  25. 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.

    Article  CAS  Google Scholar 

  26. El-Solh AA, Pietrantoni C, Bhat A, et al. Microbiology of severe aspiration pneumonia in institutionalized elderly. Am J Respir Crit Care Med. 2003;167(12):1650–4.

    Article  Google Scholar 

  27. Tolep K, Getch CL, Criner GJ. Swallowing dysfunction in patients receiving prolonged mechanical ventilation. Chest. 1996;109(1):167–72.

    Article  CAS  Google Scholar 

  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.

    Article  Google Scholar 

  29. Macht M, Wimbish T, Clark BJ, et al. Diagnosis and treatment of post-extubation dysphagia: results from a national survey. J Crit Care. 2012;27(6):578–86.

    Article  Google Scholar 

  30. Herridge MS, Angus DC. Acute lung injury–affecting many lives. N Engl J Med. 2005;353(16):1736–8.

    Article  CAS  Google Scholar 

  31. Brodsky MB, Huang M, Shanholtz C, 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.

    Article  Google Scholar 

  32. Colodny N. Dysphagic independent feeders’ justifications for noncompliance with recommendations by a speech-language pathologist. Am J Speech Lang Pathol. 2005;14(1):61–70.

    Article  Google Scholar 

  33. Steele CM, Cichero JA. Physiological factors related to aspiration risk: a systematic review. Dysphagia. 2014;29(3):295–304.

    Article  Google Scholar 

  34. Steele CM, Alsanei WA, Ayanikalath S, et al. The influence of food texture and liquid consistency modification on swallowing physiology and function: a systematic review. Dysphagia. 2015;30(1):2–26.

    Article  Google Scholar 

  35. Definition Task Force ARDS, Ranieri VM, Rubenfeld GD, et al. Acute respiratory distress syndrome: the Berlin definition. JAMA. 2012;307(23):2526–33.

    Google Scholar 

  36. 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(9):762–70.

    Article  Google Scholar 

  37. 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;94(5):1735–43.

    Article  Google Scholar 

  38. Dodds WJ, Stewart ET, Logemann JA. Physiology and radiology of the normal oral and pharyngeal phases of swallowing. Am J Roentgenol. 1990;154(5):953–63.

    Article  CAS  Google Scholar 

  39. Logemann JA. Evaluation and treatment of swallowing disorders. 2nd ed. Austin: Pro-Ed; 1998.

    Google Scholar 

  40. Palmer JB, Kuhlemeier KV, Tippett DC, Lynch C. A protocol for the videofluorographic swallowing study. Dysphagia. 1993;8(3):209–14.

    Article  CAS  Google Scholar 

  41. Kahrilas PJ, Dodds WJ, Dent J, Logemann JA, Shaker R. Upper esophageal sphincter function during deglutition. Gastroenterology. 1988;95(1):52–62.

    Article  CAS  Google Scholar 

  42. Cook IJ, Dodds WJ, Dantas RO, et al. Timing of videofluoroscopic, manometric events, and bolus transit during the oral and pharyngeal phases of swallowing. Dysphagia. 1989;4(1):8–15.

    Article  CAS  Google Scholar 

  43. Jacob P, Kahrilas PJ, Logemann JA, Shah V, Ha T. Upper esophageal sphincter opening and modulation during swallowing. Gastroenterology. 1989;97(6):1469–78.

    Article  CAS  Google Scholar 

  44. Dodds WJ, Logemann JA, Stewart ET. Radiologic assessment of abnormal oral and pharyngeal phases of swallowing. Am J Roentgenol. 1990;154(5):965–74.

    Article  CAS  Google Scholar 

  45. Logemann JA, Kahrilas PJ, Cheng J, et al. Closure mechanisms of laryngeal vestibule during swallow. Am J Physiol. 1992;262(2):G338–44.

    CAS  PubMed  Google Scholar 

  46. Molfenter SM, Steele CM. Variation in temporal measures of swallowing: sex and volume effects. Dysphagia. 2013;28(2):226–33.

    Article  Google Scholar 

  47. Clayton NA, Carnaby GD, Peters MJ, Ing AJ. Impaired laryngopharyngeal sensitivity in patients with COPD: the association with swallow function. Int J Speech Lang Pathol. 2014;16(6):615–23.

    Article  Google Scholar 

  48. Martin-Harris B. Optimal patterns of care in patients with chronic obstructive pulmonary disease. Semin Speech Lang. 2000;21(4):311–321; quiz 320–311.

  49. Gross RD, Prigent H. Chronic obstructive pulmonary disease and occult aspiration: a review of the recent literature. Curr Phys Med Rehabil Rep. 2015;3(4):280–6.

    Article  Google Scholar 

  50. Perlman AL, Booth BM, Grayhack JP. Videofluoroscopic predictors of aspiration in patients with oropharyngeal dysphagia. Dysphagia. 1994;9(2):90–5.

    Article  CAS  Google Scholar 

  51. Miller AJ. Significance of sensory inflow to the swallowing reflex. Brain Res. 1972;43(1):147–59.

    Article  CAS  Google Scholar 

  52. 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.

    Article  Google Scholar 

  53. Burgess GE III, Cooper JR Jr, Marino RJ, Peuler MJ, Warriner RA III. Laryngeal competence after tracheal extubation. Anesthesiology. 1979;51(1):73–7.

    Article  Google Scholar 

  54. de Larminat V, Montravers P, Dureuil B, Desmonts JM. Alteration in swallowing reflex after extubation in intensive care unit patients. Crit Care Med. 1995;23(3):486–90.

    Article  Google Scholar 

  55. McKay RE, Malhotra A, Cakmakkaya OS, Hall KT, McKay WR, Apfel CC. Effect of increased body mass index and anaesthetic duration on recovery of protective airway reflexes after sevoflurane vs desflurane. Br J Anaesth. 2010;104(2):175–82.

    Article  CAS  Google Scholar 

  56. Sasaki CT, Yu Z, Xu J, Hundal J, Rosenblatt W. Effects of altered consciousness on the protective glottic closure reflex. Ann Otol Rhinol Laryngol. 2006;115(10):759–63.

    Article  Google Scholar 

  57. Nishino T, Honda Y, Kohchi T, Shirahata M, Yonezawa T. Effects of increasing depth of anaesthesia on phrenic nerve and hypoglossal nerve activity during the swallowing reflex in cats. Br J Anaesth. 1985;57(2):208–13.

    Article  CAS  Google Scholar 

  58. Martin-Harris B, Brodsky MB, Michel Y, Lee FS, Walters B. Delayed initiation of the pharyngeal swallow: normal variability in adult swallows. J Speech Lang Hear Res. 2007;50(3):585–94.

    Article  Google Scholar 

  59. Lear CS, Flanagan JB Jr, Moorrees CF. The frequency of deglutition in man. Arch Oral Biol. 1965;10(1):83–100.

    Article  CAS  Google Scholar 

  60. Seidl RO, Nusser-Müller-Busch R, Ernst A. The influence of tracheotomy tubes on the swallowing frequency in neurogenic dysphagia. Otolaryngol Head Neck Surg. 2005;132(3):484–6.

    Article  Google Scholar 

  61. Lee CM, Fan E. ICU-acquired weakness: what is preventing its rehabilitation in critically ill patients? BMC Med. 2012;10:115.

    Article  Google Scholar 

  62. De Jonghe B, Lacherade J-C, Sharshar T, Outin H. Intensive care unit-acquired weakness: risk factors and prevention. Crit Care Med. 2009;37(10):S309–15.

    Article  Google Scholar 

  63. Fan E, Dowdy DW, Colantuoni E, et al. Physical complications in acute lung injury survivors: a two-year longitudinal prospective study. Crit Care Med. 2014;42(4):849–59.

    Article  Google Scholar 

  64. 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.

    Article  Google Scholar 

  65. Hogue CW Jr, Lappas GD, Creswell LL, et al. Swallowing dysfunction after cardiac operations. Associated adverse outcomes and risk factors including intraoperative transesophageal echocardiography. J Thorac Cardiovasc Surg. 1995;110(2):517–22.

    Article  Google Scholar 

  66. Doty RW, Bosma JF. An electromyographic analysis of reflex deglutition. J Neurophysiol. 1956;19(1):44–60.

    Article  CAS  Google Scholar 

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Acknowledgements

The authors thank Lisa Aronson Friedman, Sc.M. for her statistical assistance and Therese Cole, M.A., CCC-SLP, BCS-S, and Nicole Langton-Frost M.A. CCC-SLP, BCS-S for their contributions in analyzing video event timings. The authors also thank Bonnie Martin-Harris, Ph.D., CCC-SLP, BCS-S for the healthy volunteers dataset.

Funding

Research was supported by the National Institutes of Health (Grants: P050HL73994, R01HL088045, and 5K23DC013569).

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Correspondence to Martin B. Brodsky.

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This study was funded by the National Institutes of Health.

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Brodsky, M.B., De, I., Chilukuri, K. et al. Coordination of Pharyngeal and Laryngeal Swallowing Events During Single Liquid Swallows After Oral Endotracheal Intubation for Patients with Acute Respiratory Distress Syndrome. Dysphagia 33, 768–777 (2018). https://doi.org/10.1007/s00455-018-9901-z

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