Multidisciplinary management of laryngeal pathology identified in patients with COVID-19 following trans-laryngeal intubation and tracheostomy

Abstract

Background

COVID-19 disease often requires invasive ventilatory support. Trans-laryngeal intubation of the trachea may cause laryngeal injury, possibly compounded by coronavirus infection. Fibreoptic Endoscopic Evaluation of Swallowing (FEES) provides anatomical and functional assessment of the larynx, guiding multidisciplinary management. Our aims were to observe the nature of laryngeal abnormalities in patients with COVID-19 following prolonged trans-laryngeal intubation and tracheostomy, and to describe their impact on functional laryngeal outcomes, such as tracheostomy weaning.

Methods

A retrospective observational cohort analysis was undertaken between March and December 2020, at a UK tertiary hospital. The Speech and Language Therapy team assessed patients recovering from COVID-19 with voice/swallowing problems identified following trans-laryngeal intubation or tracheostomy using FEES. Laryngeal pathology, treatments, and outcomes relating to tracheostomy and oral feeding were noted.

Results

Twenty-five FEES performed on 16 patients identified a median of 3 (IQR 2–4) laryngeal abnormalities, with 63% considered clinically significant. Most common pathologies were: oedema (n = 12, 75%); abnormal movement (n = 12, 75%); atypical lesions (n = 11, 69%); and erythema (n = 6, 38%). FEES influenced management: identifying silent aspiration (88% of patients who aspirated (n = 8)), airway patency issues impacting tracheostomy weaning (n = 8, 50%), targeted dysphagia therapy (n = 7, 44%); ENT referral (n = 6, 38%) and reflux management (n = 5, 31%).

Conclusions

FEES is beneficial in identifying occult pathologies and guiding management for laryngeal recovery. In our cohort, the incidence of laryngeal pathology was higher than a non-COVID-19 cohort with similar characteristics. We recommend multidisciplinary investigation and management of patients recovering from COVID-19 who required prolonged trans-laryngeal intubation and/or tracheostomy to optimise laryngeal recovery.

Introduction

The global pandemic caused by COVID-19 disease associated with the novel SARS-CoV-2 virus has placed a significant strain on all areas of healthcare, particularly critical care. As the pandemic unfolded, the majority of critical care admissions required invasive ventilation, typically for longer duration when compared with other viral pneumonias, ¹ and with a significant but variable proportion (16-61%) subsequently requiring tracheostomy, dependent on local strategy, services and approach. ² , ³

Laryngeal complications can arise because of (trans-laryngeal) intubation (intubation of the trachea via the mouth) but may also be caused or compounded by subsequent management of the critically ill patient, including prone positioning, cuff over-inflation and multiple reintubations.^4–10 Tracheostomies are an established part of the management of the critically ill, particularly for those patients requiring (or predicted to require) prolonged invasive ventilatory support. Tracheostomies can play an important role in the management of patients with COVID-19 disease, and may reduce airway complications, morbidity associated with prolonged Intensive Care Unit (ICU) stay and potentially influence mortality. ² However, the evidence defining the role of tracheostomy in COVID-19 remains limited mostly to single centre experiences and expert opinion, with a focus on patient selection, timing, technique and the impact on outcomes.^11,12

Coronaviruses can cause laryngitis and airway oedema which may complicate airway management, contributing to the development of laryngeal pathologies alongside likely intubation trauma (for example, ulceration, granulomata and vocal cord palsies) and lead to dysphagia and dysphonia. ¹³ One report describes 16 patients who underwent laryngoscopy following COVID-19-associated critical illness: all had some form of laryngeal pathology (65% had undergone tracheal intubation and 45% had a tracheostomy at some point) frequently with multiple pathologies detected. ¹⁴ In comparison, a study completed in our centre in 2013 identified only 58% (19/33) of ICU patients tracheostomised to facilitate weaning from prolonged ventilation had identifiable pathology on FEES, ¹⁵ with others identifying structural abnormalities in 39% of tracheostomised critically ill patients outside of the current pandemic. ¹⁶

Visualisation of the structure and function of the larynx is essential in understanding the functional impact of impairments, knowledge which can then guide airway management decisions (for example, decannulation), respiratory management and weaning from ventilation (for example, tracheostomy cuff deflation or one-way valve tolerance), commencement of oral intake and ultimately guide safe ICU or hospital discharge. Without this information, significant consequences may occur, including: aspiration pneumonia; prolonged ventilation with associated risks of ventilator-acquired pneumonia; delayed diagnosis and treatment of pathology; delayed laryngeal rehabilitation; and a lack of functional communication. ¹⁷ Fibreoptic Endoscopic Evaluation of the Swallowing (FEES) is an instrumental assessment of laryngeal structure and function (see http://www.tracheostomy.org.uk/healthcare-staff/vocalisation/fees-swallowing-assessments-and-how-they-help). Ideally, FEES is performed by Speech and Language Therapists (SLTs) as part of a multidisciplinary assessment and utilised to investigate and manage dysphonia, dysphagia, trouble-shoot tolerance of cuff deflation and use of a one-way valve, and management of saliva secretions.^18,19

The aims of this study were to retrospectively examine the FEES dataset collected by the tracheostomy multidisciplinary team at a large tertiary centre in the UK, specifically to understand the incidence, characteristics, and patterns of laryngeal pathology in patients following prolonged trans-laryngeal intubation or tracheostomy as a result of COVID-19 disease.

Methods

The Health Research Authority research ethics decision tool (www.hra-decisiontools.org.uk/research) confirmed that our retrospective analysis of routinely collected clinical data in this cohort of patients did not require formal research ethics committee approval. The project was conducted under the supervision of the University of Manchester Academic Critical Care Research group.

During the initial ‘wave’ of the pandemic (March-June 2020) routine FEES ceased following national guidelines restricting nasendoscopy/FEES due to the perceived risks associated with potential aerosol generation. ²⁰ During the second ‘wave’ (June – December 2020), FEES practice resumed under revised guidance. ²⁰ Following clinical bedside assessment of all previously intubated patients, FEES was undertaken if there were concerns over secretion management, dysphonia, or dysphagia. This cohort included patients who had undergone primary extubation with subsequent clinical suspicion of laryngeal pathology (failed extubation, stridor, dysphonia) and all patients requiring tracheostomy. SLT assessment involved case history (including information relating to duration of trans-laryngeal intubation, reintubation, date of tracheostomy insertion and any premorbid swallowing or voice impairments), oromotor examination, perceptual assessment of voice quality and clinical swallowing assessment as indicated. Multidisciplinary data describing comorbidities, respiratory status and support, secretion loads, sedation levels and overall medical stability were also recorded.

FEES was conducted by an experienced SLT team using a XION Medical EndoFLEX System, videonasopharyngoscope (model EV-NC) and associated DiVAS software (DP Medical Systems, Chessington, UK). Images were captured, reported, and archived on the hospital electronic patient record. Images were interpreted and reported at the bedside utilising validated scoring systems evaluating laryngeal anatomy, physiology and function (described in detail by the authors previously)^21,22 (Supplementary Material Table 1) and a narrative report. Findings were discussed and agreed between at least two senior SLTs, but no formal inter-rater agreement or validation was undertaken. Any structural abnormalities considered clinically significant were reviewed by the local Ear Nose and Throat (ENT) team and management discussed with the SLT and intensivists. Clinically significant laryngeal pathology was defined as pathology that was directly impacting airway patency, secretion management, swallowing safety and aspiration risk, and prognosis relating to dysphagia or tracheostomy weaning potential. A management plan was made by the multidisciplinary team and communicated to the patient. These data were supplemented by routinely collected demographic and ICU outcome data.

For this study, the SLT FEES database from Wythenshawe Hospital (a tertiary respiratory and Extra-Corporeal Membrane Oxygenation centre in the North of England) was retrospectively examined. Patients assessed by FEES in the Acute or Cardio-thoracic adult ICUs between 1 March to 31 December 2020 with a diagnosis of COVID-19 requiring trans-laryngeal intubation or a tracheostomy were included in the cohort, with no exclusion criteria.

Statistical analysis was performed using SPSS 27 (IBM Corp). Univariate binary logistic regression was used to assess predictive likelihood of patient characteristics with at least one identified clinically significant laryngeal pathology (see Supplementary Material Table 1). Statistical significance was accepted at p < 0.05. Data is presented as median (interquartile range [IQR], range) or mean (standard deviation [SD], range) depending on distribution.

The primary outcome was to describe the nature and severity of laryngeal pathologies identified by FEES in COVID-19 patients following trans-laryngeal intubation or tracheostomy. Secondary outcomes included describing laryngeal functional outcomes in relation to decannulation from tracheostomy, swallowing and relationships between laryngeal pathology, patient characteristics, and ICU outcomes.

Results

A total of 25 FEES were performed on 16 different patients. Eight patients had a single examination, seven underwent two procedures, and one patient had three FEES. Repeat FEES were required for monitoring the impact of implemented medication changes, swallowing rehabilitation or spontaneous recovery, and were conducted up to a week apart. Patient characteristics were typical of those requiring invasive ventilation due to COVID-19 in the UK (Supplementary Material Table 2). ¹ , ²³ All patients had experienced severe respiratory failure: patients had been managed in the prone position a median of two times (IQR 0–5) during their stay and fourteen patients (88%) required tracheostomy to facilitate weaning from prolonged ventilation. Figure 1 demonstrates the typical timeline of the patient’s hospital journey. The patients had a median of 27 days of trans-laryngeal intubation; 34 days with a tracheostomy; and 51 days total ICU length of stay. By comparison, our hospital’s ICU databases record a total of 162 patients with COVID-19 requiring invasive ventilation during the same period, with a median of eight (3–16) days of trans-laryngeal intubation and a 22% tracheostomy rate.

Figure 1.

Timeline of patient journey. Numbers correspond to median days (IQR).

Laryngeal abnormalities analysis

Every one of the 16 patients had at least one laryngeal pathology seen on initial FEES (median number of abnormalities 3 [2–4 (1–9)]). Ten patients (63%) had at least one clinically significant structural pathology identified. Sixty-six out of the 70 identified pathologies affected the glottis, one was visualised in the immediate subglottic region, and two were more diffuse throughout the larynx. The true vocal folds were the most affected area (47% of pathologies), followed by the false vocal folds and arytenoids equally (both 23% of abnormalities). The other affected areas included the vocal processes (two pathologies), posterior glottis (two), the whole larynx including arytenoid cartilages (two) and subglottic region (one) (Figure 2). The pathologies are characterised in Table 1. The nature and distribution of these pathologies was unexpected considering the typical FEES findings following prolonged trans-laryngeal intubation prior to the coronavirus pandemic, ¹⁰ and this is highlighted in the case illustrations in Figure 3 (with and other clinically interesting cases detailed in Supplementary Material Figure 1).

Figure 2.

Location of laryngeal pathology identified at FEES. Level of shading corresponds to overall proportion of effected area.

Table 1.

Incidence of different laryngeal abnormalities in the 16 patients.

Type	Abnormalities detected, n (%)	Patients with abnormality, n (%)
Oedema	20 (29)	12 (75)
Abnormal movement	20 (29)	12 (75)
Significant vocal fold paralysis	6 (9)	6 (38)
Recovering paralysis/paresis	5 (7)	3 (19)
Compensatory true vocal fold movement/ hyperfunction	3 (4)	3 (19)
False vocal fold hypertrophy	6 (9)	3 (19)
Altered anatomy	13 (18)	11 (69)
Vocal fold atrophy	11 (16)	9 (56)
Arytenoid collapse	1 (1)	1 (6)
Pseudosulcus vocalis	1 (1)	1 (6)
Erythema	7 (10)	6 (38)
Granuloma tissue	5 (7)	3 (19)
Mucosal trauma	2 (3)	2 (13)
Stenosis	1 (1)	1 (6)
Ulceration	1 (1)	1 (6)
Cystic lesions	1 (1)	1 (6)

Note: Total abnormalities detected in all FEES was 70. Subcategory percentages do not necessarily add up to total category percentage as individual patients could have multiple abnormalities.

Figure 3.

Illustrative case vignettes demonstrating laryngeal injury pattern seen on FEES following prolonged trans-laryngeal intubation in 2 patients with COVID-19 disease. Case summaries and images are presented with the permission of the patients.

There were no significant predictive patient characteristics or outcomes for the development of at least one significant laryngeal pathology as detected on FEES (Supplementary Material Table 3).

Functional outcomes

All patients had a degree of dysphagia and dysphonia, and there was a high burden of laryngeal incompetence with eight patients having visible aspiration on initial FEES, of these seven (88%) had clinically significant silent aspiration and remained nil-by-mouth as a result. Reflux, aspiration and secretion scores were higher than expected (Table 2). The twenty-five FEES prompted a change in management in all patients (Table 2). Repeat FEES was recommended in eight (50%) patients, institution of targeted dysphagia therapy in seven (44%) patients and a referral for ENT opinion in six (38%) patients following FEES.

Table 2.

Assessment of laryngeal function at FEES (n = 25) and resulting management.

SLT assessment scores	Median	IQR	Range	Patients with a severe score (%)
Belafsky Reflux Finding Score (n = 16)	11	7–14	0–25	69
New Zealand Secretion Scale (n = 16)	5	2–6	0–7	50
Airway Protection Scale (n = 13)	6	3–7	0–7	N/A
Penetration-Aspiration Scale (n = 16)	4	1–7	1–8	31
Clinical outcomes for those with repeat FEES	First FEES		Second FEES
Feeding (n = 8)
Nil by mouth	7		0
Full oral intake	1		8
Tracheostomy weaning (n = 7)
Progressing well with weaning	3		6
Unable to progress	4		1
Management	Times recommended per FEES, n (%)		Times recommended per patient, n (%)
Repeat FEES	9 (36)		8 (50)
Dysphagia therapy plan	8 (32)		7 (44)
ENT referral	7 (28)		6 (38)
Reflux management (increase or decrease in PPI)	6 (24)		5 (31)
Nebulisers/secretion medication	4 (16)		4 (25)
Steroids	3 (12)		3 (19)
Tracheostomy outcomes	2 (8)		2 (13)
Reinflate tracheostomy cuff	1 (4)		1 (6)
Use one-way valve	1 (4)		1 (6)
Videofluoroscopy when off ICU	1 (4)		1 (6)

Note: Multiple recommendations were often made per FEES. “Severe” scores are defined in Supplemental Material Table 1. PPI: Proton Pump Inhibitor. Scoring systems are described in detail by the authors previously. ²¹ , ²²

The results from the FEES assessments were used to proactively manage the laryngeal problems identified, rather than as a purely observational test. FEES prompted therapies to optimise management of excessive secretions, laryngeal oedema, or laryngo-pharyngeal reflux on thirteen occasions. Four patients with tracheostomies were unable to tolerate one-way valve due to laryngeal oedema impacting on upper airway patency promoting safer tracheostomy care. In those with a repeat FEES (n = 9), FEES aided progression of tracheostomy weaning on three occasions and an increase in nature and quantity of oral intake on eight occasions (Table 2). Repeating the FEES assessment allowed for evaluation of the impact of the therapies, re-assessment of laryngeal function and readiness for decannulation and targeted laryngeal rehabilitation strategies and optimal introduction of oral intake.

FEES findings were discussed with Dietetic colleagues leading to the following recommendations for nasogastric tube (NGT) feeding: keep the NGT on thirteen occasions (57%), reduce the use of the NGT following commencement of oral intake on nine occasions (36%) and remove the NGT in two. One patient was discharged home with their tracheostomy in situ due to severe glottic stenosis and is awaiting laryngeal surgery. One patient was readmitted to hospital with stridor post discharge due to a recurrent granuloma, this was subsequently surgically removed.

Discussion

Our study identified at least one identifiable laryngeal pathology in all patients undergoing FEES following tracheostomy or prolonged trans-laryngeal intubation for COVID-19, over half of which were clinically significant. By comparison, our 2013 (pre-COVID-19) study identified a smaller proportion of critical care patients with laryngeal pathology on FEES. ¹⁵ Of note, half of our patients with tracheostomy experienced a lack of progress in their respiratory and tracheostomy weaning program, which was subsequently explained by the laryngeal pathology seen on FEES. Whilst there is currently little evidence linking prone positioning and development of laryngeal pathology in intubated and tracheostomised patients, it can be hypothesised that increased movement and pressure on the larynx from the tracheal tube could initiate or propagate the pathologies identified in our study. This may have contributed to the unusual pattern of pathology tissue seen in Figure 3, with granulation tissue observed on the prolapsed arytenoid, underside of the epiglottis and bilateral true vocal folds concurrently. These findings could be plausibly linked to injury from the necessary trans-laryngeal intubation and associated airway management frequently required to manage COVID-19 respiratory failure, and /or to a direct effect from SARS-CoV-2 viral infection. Laryngeal complications may prevent successful extubation and tracheostomy decannulation, ²⁴ and both are associated with an increase in mortality. ²⁵

It is well documented that clinical assessment alone can miss laryngeal pathology which is later identified at FEES in as many as 62% of assessments (specialist staff), rising to 97% when clinically assessed by medical staff. ¹⁹ Clinical assessment also often tends to lead to a more cautious approach to management of swallowing difficulties. Without FEES or endoscopic laryngeal visualisation, laryngeal pathologies might remain undetected until problems developed, and management strategies that directly impact patient psychological wellbeing and recovery such as decannulation, commencing or advancing oral intake, preventing aspiration–related respiratory complications or facilitating vocalisation would be delayed. With a median of 3 distinct pathologies identified on initial FEES, this raises the question of whether FEES or endoscopic laryngeal visualisation should be undertaken in more COVID-19 patients following prolonged trans-laryngeal intubation or tracheostomy.

The majority of patients who aspirated (with and without tracheostomy) were identified to be silently aspirating (without triggering a laryngeal reflex response). Pulmonary aspiration via an incompetent larynx occurs in 33–70% of non-COVID-19 tracheostomised patients, of which the majority are silent due to impaired laryngopharyngeal sensorium.^15,26,27 Abnormal laryngeal movement was seen in 75% of our patient and, when compounded by sensory impairments and oedema, this likely translated into the high New Zealand Secretion and Penetration Aspiration Scales observed; in turn associated with morbidity, mortality and prolonged hospital stays.^28–30 The high rates of laryngopharyngeal reflux also seen in our population led to increase/re-commencement of proton pump inhibitor (PPI) therapy in nearly one-quarter. It is unclear whether the reflux we observed is associated with increased rates of underlying obesity in our cohort (predisposing to severe COVID-19), ¹ or as a consequence of ventilation, prone positioning and laryngeal pathology. With routine PPI use considered an accepted standard of ventilator care bundles worldwide, ³¹ it would be interesting to study the impact of high dose PPI from the outset in obese patients with COVID-19 requiring trans-laryngeal intubation. Targeted dysphagia therapy plans were instituted in one-third of our cohort, aiming to rehabilitate laryngopharyngeal function. Fatigue, delirium or cognitive impairments limited early swallowing therapy.

Laryngeal oedema is associated with respiratory distress and/or stridor following extubation. Crude clinical screening for oedema with an endotracheal cuff leak test may be reassuring prior to an attempt at primary extubation, but the sensitivity and specificity of such tests are unclear. ³² Any patient without an audible cuff leak should be considered for airway endoscopy prior to extubation due to the high likelihood of laryngeal pathology in those with prolonged trans-laryngeal intubation. The universal use of systemic corticosteroids to treat severe COVID-19 may mitigate airway oedema, ³³ although persistent oedema was noted in our cohort, the majority of whom had received dexamethasone early in their ICU admission. Nebulised corticosteroids have similar efficacy to systemic steroids for treating laryngeal oedema ³⁴ and anecdotally, we have been pleasantly surprised at the impact of inhaled steroids instigated following FEES in this patient population.

In our centre, FEES proved clinically useful, directly influencing timely multidisciplinary interventions, potentially preventing acute and chronic complications. Around half of COVID-19-related laryngeal pathologies identified at endoscopy require later intervention. ¹⁴ Our own follow up data shows around one-quarter of ICU patients recovering from COVID-19 who were referred to SLT team remained dysphonic at hospital discharge and around 20% report persistent dysphagia symptoms, despite recommencing largely normal diet textures at post-ICU telehealth follow-up clinics.

Our retrospective, observational study of a limited number of patients has several limitations. Given the small cohort seen in this retrospective study, we would recommend further prospective research to enable more specific comparisons in laryngeal pathology between patients with and without COVID-19, taking consideration to the prolonged mechanical ventilation times seen in our cohort. This would enable us to further understand the impact of COVID-19 on the larynx and to possibly predict and manage these issues prospectively. Secondly, a FEES service may not be universally available in many ICUs, limiting the applicability of some of our recommendations. Finally, all patients in our study survived to hospital discharge, raising the possibility of selection bias towards patients well enough to undergo FEES. Laryngeal pathology rates may be even greater if sicker patients also underwent assessment. Answers to the questions raised by our work can only be answered by systematic collection and analysis of relevant data, and initiatives such as the Global Tracheostomy (Quality Improvement) Collaborative should be encouraged.^11,35

Based on our multidisciplinary experience managing patients requiring prolonged respiratory support during the COVID-19 pandemic, we offer the following clinical practice recommendations which may help to identify and proactively manage laryngeal pathology:

• Use of post-ICU screening questionnaires to help identify swallowing voice and airway problems that may be missed by clinical evaluation alone. ³⁶

• FEES should be conducted by specialist staff following current guidance for PPE and aerosol generation. See www.rcslt.org/learning/covid-19/.

• Routine use of endoscopic laryngeal visualisation by SLT and/or ENT teams should be considered in all patients with COVID-19 who require:

• Prolonged trans-laryngeal intubation.

• Tracheostomy.

• Clinical suspicion of laryngeal pathology (no cuff leak, post-extubation dysphonia and dysphagia, for example).

• Identification of occult pathology by FEES should guide multidisciplinary dysphagia management, oral and alternative feeding decisions, secretion management pharmacological treatments, and optimise tracheostomy weaning decisions.

• Prior to extubation:

• Perform a cuff leak test.

• Consider endoscopic laryngeal visualisation if no leak identified.

• Treat confirmed or suspected laryngeal oedema with corticosteroids (either systemic or nebulised).

• Further research to quantify the impact of intubation strategies, tracheal tube size, patient positioning, corticosteroids, antacid therapies, and the timing of tracheostomy on the nature and severity of laryngeal pathology associated with critical illness.

Conclusions

There is a high incidence of structural and functional laryngeal pathologies occurring in our cohort of patients requiring prolonged trans-laryngeal intubation and tracheostomy with COVID-19, the aetiology of which is multifactorial. Laryngeal pathology may cause acute problems associated with morbidity and mortality, with many requiring further investigation and proactive interventions. Chronic consequences are yet to be understood. This study demonstrates the crucial role the SLT can play in identifying laryngeal problems during FEES, and this information supports the multidisciplinary team to provide individualised treatment options to enable expedited troubleshooting for weaning from tracheostomy, early recommencement of oral intake and identifying and treating concomitant dysphonia and dysphagia. What is clear is that identification of predictable laryngeal pathology by early expert FEES is invaluable in guiding the management and rehabilitation of patients recovering from severe COVID-19 disease.

ORCID iDs

Sarah Boggiano https://orcid.org/0000-0002-7233-3416

Thomas Williams https://orcid.org/0000-0003-3887-7740

Sonya E Gill https://orcid.org/0000-0001-8083-6390