Despite having the tools and techniques for tracheal intubation for >4,000 years,1 and performing oral intubation with positive pressure mechanical ventilation for >50 years,2 only recently has attention focused on patient issues following extubation, particularly swallowing-related complications. The endotracheal tube traverses the oropharynx, larynx, and trachea, with potential for laryngeal and tracheal injury, voice dysfunction, and dysphagia (i.e., swallowing dysfunction). Aspiration (i.e., one consequence of dysphagia) is present in ≥40% of medical-surgical and cardiac patients post-extubation.3–5 When an instrumental evaluation of swallowing demonstrates dysphagia with aspiration, there are important clinical concerns regarding pneumonia,6 with implications for the intensive care unit (ICU) team and other clinicians, including speech-language pathologists/therapists (SLPs/SLTs), otolaryngologists, gastroenterologists, pulmonologists, and radiologists. Unfortunately, there is great variability in screening and diagnosing dysphagia across ICUs and hospitals7,8 – creating a new frontier for research and quality improvement activities.9 Herein, we discuss selected concerns regarding dysphagia in ICU patients post-extubation and outline opportunities for multidisciplinary management.
Mechanisms of Dysphagia Post-extubation
Six mechanisms for post-extubation dysphagia in critically ill patients have been identified: trauma, neuromuscular weakness, altered sensation, impaired cognition, gastroesophageal reflux, and dyssynchronous breathing and swallowing.10 Duration of intubation is associated with some of these mechanisms.11,12 Each mechanism alone could be responsible for dysphagia; however, dysphagia severity may involve multiple mechanisms (Table 1). Nurse screening (see below) in the ICU and post-ICU wards play a vital role in recognizing signs and symptoms of dysphagia caused by these mechanisms, including coughing, choking, wet vocal quality, pocketing food, drooling, and difficulty with swallowing different consistencies of foods and liquids, often indicating the need for formal evaluation. Additionally, nursing staff often provide monitoring and assistance with implementing compensatory strategies during meals and encouraging completion of recommended exercises by SLPs/SLTs.
Table 1.
Considerations for interdisciplinary management of dysphagia in ICU patients after extubation.
Issue | Management consideration | Responsible discipline(s) | Example References* |
---|---|---|---|
Trauma to the oropharynx and larynx | |||
Laryngeal injury, abnormal laryngeal motor reflexes | Laryngoscopy/voice evaluation | SLP, ENT | 1–13 |
Voice treatment | SLP, CC, ENT | 14–19 | |
Neuromuscular weakness | |||
Reduced airway closure and/or reduced upper esophageal sphincter opening | Flexible Endoscopic Evaluation of Swallowing (FEES) | SLP, ENT | 20–22 |
Videofluoroscopic swallow study (VFSS) | SLP, Rad | 22 | |
Treatment/management | SLP | 23–26 | |
Tongue weakness | Cranial nerve exam/tongue strengthening exercise | SLP, CC, PMR, RN, NP, Neuro | 27,28 |
Feeding (hand-to-mouth control) difficulties | Evaluation for ICU-acquired weakness, and impaired coordination and fine motor control | OT, PT, CC, PMR, RN, NP | 29 |
Generalized weakness | Evaluation of strength (e.g., manual muscle testing, dynamometry) | OT, PT, CC, PMR, RN, NP | 30 |
Altered sensation | |||
Medications | Raising awareness; monitoring side effects, and reassessing medications | RN, CC, PMR, NP, SLP, ENT, GI | 31,32 |
Tongue sensory changes | Oral motor/cranial nerve exam | RN, CC, PMR, NP, SLP, ENT, Neuro | 28 |
Glottis sensory changes | Laryngoscopy/voice evaluation | SLP, ENT | 4,10–12,33 |
Impaired cognition | |||
Impaired arousal, attention, memory, communication, thought organization, problem solving, and reasoning | Screening/evaluation and management of delirium and cognition | RN, CC, PMR, NP, SLP, Psych, OT | 34,35 |
Gastroesophageal reflux | |||
Aspiration, pneumonia, pneumonitis | Medical management | CC, GI | 36–40 |
Dyssynchronous breathing and swallowing | |||
Changes to breathing that impact swallowing | Non-invasive monitoring | CC, GI | 31,32 |
Abbreviations: ENT, otolaryngologist; GI, gastroenterologist; CC, critical care physician; Neuro, neurologist; NP, nurse practitioner (may also include physician assistant); OT, occupational therapist; PMR, physiatrist; Psych, psychologist/psychiatrist; PT, physical therapist; Rad, radiologist; RN, critical care nurse; SLP/SLT, speech-language pathologist./speech-language therapist
References are listed in the electronic supplementary material.
Breathing-Swallowing Linkages
Breathing and swallowing share the pharynx,13 necessitating careful monitoring of the aerodigestive system. Healthy adults demonstrate little variation in the tight linkage of breathing-swallowing coordination14 and airway closure during swallowing, but swallowing effectively becomes halted in the presence of an endotracheal tube. This tight linkage – specifically anatomical movements to protect the airway during swallowing – may be disrupted by intubation and muscle weakness during critical illness.15 Deleterious effects on breathing-swallowing coordination have been reported in healthy adults given morphine and midazolam,16 raising potentially important implications for critically ill patients. Expanded investigation into post-extubation breathing-swallowing coordination is important to further understand parameters that are conducive to safe swallowing.17 Along with the ICU team, SLPs/SLTs, otolaryngologists, and pulmonologists are specialists that assess and treat swallowing and airway function, and identify and treat related disease processes.
Screening Swallowing Function Post-extubation
In the United States, the timing and process of screening/evaluation by SLPs/SLTs is variable,8 often beginning ≥24 hours post-extubation.7 Although the reason for delayed assessment is unclear, it may be the consequence of a study of 79 patients that demonstrated a significantly reduced delay in patients’ “swallowing reflex” immediately after extubation compared with assessment at >24 hours.18 However, this study has many limitations, including not directly assessing or visualizing swallowing and administering liquid boluses of ≤1 ml that are not clinically relevant. Two more recent studies evaluated screening for post-extubation dysphagia-related aspiration, both using the 3-oz. water swallow test and both without a 24-hour delay in assessment if patients were otherwise clinically appropriate: the Yale Swallow Protocol19,20 and Post-extubation Dysphagia Screening.21 The Yale Swallow Protocol, using the flexible endoscopic evaluation of swallowing (FEES) as its reference standard, demonstrated 97% sensitivity and 49% specificity in hospitalized patients, including >200 ICU patients post-extubation.20,22 Using the Yale Swallow Protocol’s 3-oz. water swallow test as a reference standard,22 the Post-extubation Dysphagia Screening protocol demonstrated 81% sensitivity and 69% specificity in ICU patients.21 Both approaches concluded that patients’ clinical readiness should be a marker for screening/evaluation, not a fixed duration of time post-extubation, and both are recommended for use post-extubation. Frequently, nurses conduct such screenings, but any trained clinician may be appropriate. Regardless of dysphagia screening method, a cautious approach that includes clinician monitoring of signs and symptoms should be used when starting post-extubation patients on an oral diet.
Instrumental Evaluation of Swallowing Function
After a failed screening test or concern based on clinician evaluation of swallowing, an instrumental evaluation may be necessary. Although SLPs/SLTs most often perform clinical evaluations, their scope of practice for instrumental evaluations varies across settings. An instrumental evaluation has 5 objectives: 1) identify the physiological component(s) of disordered swallowing (i.e., oral, pharyngeal, esophageal impairments), 2) judge severity for each impairment, 3) determine safe and appropriate consistencies and route/manner of nutritional intake, 4) identify the need for further evaluation, and 5) identify and evaluate the effectiveness of compensatory interventions (e.g., chin tuck) and treatment strategies (e.g., exercises). FEES and the videofluoroscopic swallow study (VFSS) are the two instrumental evaluations of swallowing that are reference standards for dysphagia evaluation.23 FEES and VFSS tests are not pass/fail evaluations; rather, each assesses key components of swallowing physiology. Unlike VFSS, FEES does not use ionizing radiation, allowing longer evaluation periods to sample behaviors/swallowing physiology with a direct view to evaluate the nasopharynx, pharynx, and larynx. Alternatively, VFSS provides views of the oral, pharyngeal, and esophageal swallow, assessing swallowing function across the aerodigestive system. Specifically in the ICU, FEES has important advantages of being a portable bedside assessment, providing visual assessment of potential laryngeal injury 12 and secretion management. FEES is also feasible and well-tolerated, given that modern nasoendoscopes are very small (<3.0 mm), and may be performed by a trained SLP/SLT or otolaryngologist without sedation or topical medications.24,25 Because SLPs/SLTs treat swallowing disorders, their role in directly evaluating patients can be invaluable. Concerns for laryngeal or esophageal impairments should result in an otolaryngology or gastroenterology referral, respectively. Minimum requirements to complete a FEES are an awake and cooperative patient permitted to ingest liquids and foods, and has cardiopulmonary stability and no major bleeding risk.
Multiple Disciplines for One Cause—The Patient
Dysphagia is associated with increased inpatient costs, length of stay, and mortality.26 Early screening and evaluation of swallowing function may reduce these risks in ICU patients post-extubation.4 To perform early screening and evaluation effectively, trained clinicians involving multiple disciplines must systematically address integrity of the anatomy, neuromuscular strength and sensation, cognition, gastrointestinal function, and breathing-swallowing coordination. Interdisciplinary care is important to address potential complications from dysphagia in patients post-extubation.27
Supplementary Material
Acknowledgments
This manuscript was supported in part by the National Institutes of Health/National Institute of Nursing Research (R01NR017433, Brodsky, Pandian, Needham).
Footnotes
Conflict of Interest
The authors have no conflicts of interest to declare.
Publisher's Disclaimer: This Author Accepted Manuscript is a PDF file of an unedited peer-reviewed manuscript that has been accepted for publication but has not been copyedited or corrected. The official version of record that is published in the journal is kept up to date and so may therefore differ from this version.
References
- 1.Szmuk P, Ezri T, Evron S, Roth Y, Katz J. A brief history of tracheostomy and tracheal intubation, from the Bronze Age to the Space Age. Intensive Care Med. 2008;34(2):222–228. [DOI] [PubMed] [Google Scholar]
- 2.Slutsky AS. History of mechanical ventilation. From Vesalius to ventilator-induced lung injury. Am J Respir Crit Care Med. 2015;191(10):1106–1115. [DOI] [PubMed] [Google Scholar]
- 3.Skoretz SA, Flowers HL, Martino R. The incidence of dysphagia following endotracheal intubation: A systematic review. Chest. 2010;137(3):665–673. [DOI] [PubMed] [Google Scholar]
- 4.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. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Marvin S, Thibeault S, Ehlenbach WJ. Post-extubation dysphagia: Does timing of evaluation matter? Dysphagia. 2019;34(2):210–219. [DOI] [PubMed] [Google Scholar]
- 6.Shifrin RY, Choplin RH. Aspiration in patients in critical care units. Radiol Clin North Am. 1996;34(1):83–96. [PubMed] [Google Scholar]
- 7.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):578–586. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Brodsky MB, Gonzalez-Fernandez 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):1545–1552. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Latronico N, Herridge M, Hopkins RO, et al. The ICM research agenda on intensive care unit-acquired weakness. Intensive Care Med. 2017;43(9):1270–1281. [DOI] [PubMed] [Google Scholar]
- 10.Macht M, Wimbish T, Bodine C, Moss M. ICU-acquired swallowing disorders. Crit Care Med. 2013;41(10):2396–2405. [DOI] [PubMed] [Google Scholar]
- 11.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):574–579. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Brodsky MB, Levy MJ, Jedlanek E, et al. Laryngeal injury and upper airway symptoms after oral endotracheal intubation with mechanical ventilation during critical care: A systematic review. Crit Care Med. 2018;46(12):2010–2017. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Miller AJ. Deglutition. Physiol Rev. 1982;62(1):129–184. [DOI] [PubMed] [Google Scholar]
- 14.Martin-Harris B, Brodsky MB, Michel Y, Ford CL, Walters B, Heffner J. Breathing and swallowing dynamics across the adult lifespan. Archives of Otolaryngology -Head and Neck Surgery. 2005;131(9):762–770. [DOI] [PubMed] [Google Scholar]
- 15.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):768–777. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Hårdemark Cedborg AI, Sundman E, Boden K, et al. Effects of morphine and midazolam on pharyngeal function, airway protection, and coordination of breathing and swallowing in healthy adults. Anesthesiology. 2015;122(6):1253–1267. [DOI] [PubMed] [Google Scholar]
- 17.Camargo FP, Ono J, Park M, Caruso P, Carvalho CR. An evaluation of respiration and swallowing interaction after orotracheal intubation. Clinics (Sao Paulo). 2010;65(9):919–922. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.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):486–490. [DOI] [PubMed] [Google Scholar]
- 19.Leder SB, Suiter DM. The Yale Swallow Protocol: An evidence-based approach to decision making. Switzerland: Springer; 2014. [Google Scholar]
- 20.Leder SB, Warner HL, Suiter DM, et al. Evaluation of swallow function post-extubation: Is it necessary to wait 24 hours? Ann Otol Rhinol Laryngol. 2019;0(0):3489419836115. [DOI] [PubMed] [Google Scholar]
- 21.Johnson KL. Validation of a postextubation dysphagia screening tool for patients after prolonged endotracheal intubation. Am J Crit Care. 2018;27(2):89–96. [DOI] [PubMed] [Google Scholar]
- 22.Suiter DM, Leder SB. Clinical utility of the 3-ounce water swallow test. Dysphagia. 2008;23(3):244–250. [DOI] [PubMed] [Google Scholar]
- 23.Giraldo-Cadavid LF, Leal-Leano LR, Leon-Basantes GA, et al. Accuracy of endoscopic and videofluoroscopic evaluations of swallowing for oropharyngeal dysphagia. Laryngoscope. 2017;127(9):2002–2010. [DOI] [PubMed] [Google Scholar]
- 24.Aviv JE, Kaplan ST, Thomson JE, Spitzer J, Diamond B, Close LG. The safety of flexible endoscopic evaluation of swallowing with sensory testing (FEESST): An analysis of 500 consecutive evaluations. Dysphagia. 2000;15(1):39–44. [DOI] [PubMed] [Google Scholar]
- 25.Hafner G, Neuhuber A, Hirtenfelder S, Schmedler B, Eckel HE. Fiberoptic endoscopic evaluation of swallowing in intensive care unit patients. Eur Arch Otorhinolaryngol. 2008;265(4):441–446. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Patel DA, Krishnaswami S, Steger E, et al. Economic and survival burden of dysphagia among inpatients in the United States. Dis Esophagus. 2017. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Donovan AL, Aldrich JM, Gross AK, et al. Interprofessional care and teamwork in the ICU. Crit Care Med. 2018;46(6):980–990. [DOI] [PubMed] [Google Scholar]
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