Introduction
Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) results in a high incidence of respiratory distress. Between 1/9/20–10/5/21, 7644 individuals in the UK received invasive ventilation within 24 h of admission to hospital [
1]. These patients often receive prolonged mechanical ventilation, prone positioning, deep therapeutic sedation, and the use of muscle relaxants and tracheostomies [
2]. While tracheostomy tubes are often necessary for survival, the iatrogenic effects of these and other artificial airways on the larynx are still emerging.
Tracheostomy decannulation timing and approaches are numerous [
3]. A key question for teams managing patients with tracheostomy tubes relates to timing of safe decannulation. This important rehabilitation consideration facilitates independence, improves communication, reduces dependence on therapeutic interventions (e.g., tube feeding), and improves health outcomes [
4]. In most acute care facilities, decision-making for tracheostomy decannulation is made using multi-disciplinary clinical care pathways. Institution specific protocols tend to govern this decision-making rather than national guidelines [
3]. During the COVID-19 pandemic, decannulation decisions have been challenging due to healthcare system burden as well as the complex clinical presentation; specifically, delirium management [
5], gross inflammatory process and cytokine storms [
6], hypoxemia [
7], coagulation disorders [
8], swallowing impairment or dysphagia [
9], mobility and fatigue [
10], and upper airway compromise [
11]. In order to explore ways to facilitate tracheostomy weaning and expedite rehabilitation of upper airway function, we present our quality assurance audit following laryngeal assessment of patients with severe COVID-19 who underwent tracheostomy tube insertion.
Methods
Prospective data collection was used to gather information on acute laryngeal anatomy and physiology following invasive ventilation and tracheostomy tube placement for treatment of COVID-19. Nasendoscopic examination before decannulation is standard practice in our institution. There is no control group in this study, as the evaluation was undertaken during the second peak of Covid-19 in the UK, where there was no available comparable group due to the intense resource utilisation for COVID-19 patients. We seek to describe this specific pathophysiology, to inform other ENT, intensive care and Speech and Language Therapy teams and to improve outcomes for this complex group of patients. Future prospective work is underway to facilitate comparison between case–control with appropriate methodology and study design. This work uses data provided by patients and collected by the NHS as part of their care and support at the Queen Elizabeth Hospital Birmingham NHS Foundation Trust. It has been approved by University Hospitals Birmingham NHS Foundation Trust, Clinical Audit Registration & Management System and the COVID-19 research facilitation group under application reference CARMS-17155.
Setting
From January 1 to April 28, 2021, we included all consecutive ICU patients considered for tracheostomy weaning at the Queen Elizabeth Hospital Birmingham. Included were those with severe respiratory failure secondary to SARS-CoV-2 with positivity confirmed by real-time polymerase chain reaction testing (nasopharyngeal swabs) or non-directed bronchial lavage/aspirate. Once the patient was able to tolerate oxygen delivery via tracheostomy mask (without invasive ventilation), they were eligible for a fiberoptic nasendoscopy.
Tracheostomy Multi-Disciplinary Team (MDT)
We have described percutaneous tracheostomy tube insertion methods and operational aspects of our MDT previously [
2]. In brief, the majority of tracheostomies were percutaneous, undertaken by a surgical team with therapeutic management led by the Speech and Language Therapists (SLT). Other MDT personnel included: ENT, physiotherapists, altered airway nurses, education leads, respiratory physicians, intensivists, and ward nursing staff.
Laryngeal Assessment
An ENT surgeon and SLT completed the laryngeal assessment via nasendoscopy when the patient tolerated oxygen supplementation via a tracheostomy mask without invasive ventilation. Where patients were sufficiently alert, a swallow assessment was completed with and diet fluid recommendations. The examination was recorded on the AMBU disposable scope system (Ambu® aScope™ 4 RhinoLaryngo Slim). We used a predefined proforma, including laryngeal and pharyngeal motor and sensory assessment and standardised oedema and airway protection scoring during swallowing. The decision to decannulate was made by the treating team (intensive care or respiratory) using their usual clinical parameters. Data collection for audit purposes ceased after decannulation.
Scales, Scoring, and Statistical Analyses
The revised Patterson oedema scale [
12] and Penetration Aspiration scale (PAS)[
13] were used. The revised Patterson Oedema scale is a standardized scoring method to rate upper airway oedema and the PAS is a validated tool which describes airway protection impairment. Raters for all airway scales were SLT and ENT surgeons with expertise in aerodigestive tract anatomy and physiology. Following institutional reliability training, two raters scored each laryngeal assessment with disagreements resolved by consensus. Scores of each component were recorded according to two regions based on anatomical location: region 1 (glottis) included the true vocal fold, false vocal fold, arytenoid and aryepiglottic components; and region 2 (supraglottis) included epiglottis, pharyngo-epiglottic folds, vallecula, and pyriform sinus components.
Presence of Intensive Care acquired weakness (ICUAW) was assessed by a physiotherapist at ICU discharge using Medical Research Council (MRC) sum score [
14]. A validated tool within ICU, the MRC describes muscle power of each limb on an oxford scale from 0 (total paralysis) to 5 (normal power). ICUAW was defined as either ‘significant’ (MRC ≤ 48/60) or severe (MRC ≤ 36/60), with normal being an MRC > 48 [
14]. Functional status was also assessed at ICU discharge using the Manchester Mobility Scale (MMS), a seven-point mobility scale validated for assessing mobility levels within ICU [
15].
For analyses, we dichotomized PAS describing airway protection as ‘normal’ (PAS scores of either 1 or 2) or ‘impaired’ (PAS scores of 3 and above). All continuous variables were summarized according to mean with standard deviation (SD) and median with interquartile range (IQR) depending on whether data were normally distributed, and ordinal/categorical data summarized according to frequency counts. Following stratification of the sample according to normal or impaired PAS, bivariate comparisons were conducted using Mann–Whitney or unpaired 2-sided
t-tests for continuous variables and Pearson’s χ
2 test, likelihood ratio or Fisher’s exact test for proportions as appropriate. Post-hoc, we conducted two exploratory main effect regression analyses for two study outcomes: a logistic backward stepwise regression [
16] to explore predictors for abnormal airway protection and a multiple linear regression to explore predictors for prolonged tracheostomy tube dependency. For these purposes, the following variables were defined as: ICU acquired weakness (yes [severe and significant]/no [normal]), abnormal false vocal fold oedema (moderate and severe), artificial airway duration (intubation + tracheostomy tube duration), and impaired airway protection (PAS ≥ 3). Given the exploratory nature of these regressions and the novel patient population, the five predictor variables which were chosen for our models were informed by our bivariate comparisons and clinical relevance [
17]. Significance for all statistical tests was
p < 0.05.
Discussion
Since the emergence of COVID-19, publications exploring tracheostomy pathways [
18,
19] have enhanced understanding of how tracheostomy may improve outcomes. Few, however, have detailed decannulation rates or provided operational guidance on how to optimise outcomes, like swallowing, while informing acute decision-making. Within our data, at initial assessment over two-thirds presented with an oedema score of 3 or above with impaired airway protection evident in nearly half, lower oedema scores favored normal airway protection. Furthermore, we explored predictors for impaired airway protection and tracheostomy tube duration. Our collective findings not only align with presenting otolaryngological manifestations of COVID-19 (e.g. pharyngeal erythema) [
20] and laryngeal pathologies following intubation in general [
21], they also suggest that inclusion of a functional, multi-disciplinary laryngeal assessment is beneficial. Although decannulation timing may be influenced by many variables, our assessment approach enables clinical teams to make practical risk stratification for decannulation with findings pertinent to ENT surgeons, SLT’s and Intensivist decision-making.
Patients with impaired airway protection had significantly more complex respiratory recovery specifically longer durations of artificial airways (both endotracheal and tracheostomy tubes) and more frequent intubations. In addition, the majority required downsizing or fenestrated tubes. Although our analyses were exploratory, we suggest impaired airway protection may be an independent predictor of tracheostomy duration. While this aligns with other studies on critically ill patients without COVID-19 [
22], this is the first exploration for this novel population. As a result, using objective laryngeal measurements such as the revised Patterson Oedema scale [
12] will afford objective characterization while facilitating a systematic method to monitor change. This enables efficient treatment, standardised recovery monitoring, and streamlining of decannulation processes and resource allocation. Doing so within the ICU is particularly prudent where bed availability is at a premium, particularly during this pandemic.
A common finding in survivors of critical illness is ICUAW [
23]. The majority of our patients (~ 80%) had a CFS < 3, indicating that they were very fit, fit or functioning well prior to admission. Despite this, all had significant or severe ICUAW at rehabilitation commencement. Furthermore, patients with ongoing airway protection issues at ICU discharge were significantly more likely to have persistent ICUAW weakness. In general, physical rehabilitation focuses on extremities and outcomes related to activities of daily living (e.g., ambulation) [
24]. In contrast, the impact of weakness on swallowing particularly following artificial airway use is extremely limited [
25]. While investigating the relationship between ICUAW and dysphagia was not the objective of our study, given the limited evidence in this area, routine screening for the presence of ICUAW using the MRC score, particularly on waking from sedation, may be useful. Not only may it prompt nasendoscopic airway assessment, it may also highlight those who would most benefit from SLT assessment and rehabilitation. Furthermore, future mechanistic studies of swallowing in this population would inform bespoke rehabilitation approaches.
This was a quality assurance audit, undertaken during the third COVID-19 surge in the UK and as a result, our study had limitations and should be considered through the lens of the following design caveats. Our small sample size without a control group limits generalizability and does not elucidate the potential differences between this populations as compared to those with critical illness without COVID-19. However, it is pertinent to couch this methodological limitation in line with other pandemic publications without control groups, which have contributed fundamental learning to this novel and emergent pathophysiology and clinical presentation [
26]. In addition, our small sample size lent itself to analyses primarily focused on associations. In the future, conducting multi-variate regressions with statistically informed models and multiple outcome variables would be useful to develop predictive risk profiles and support practice. As with most clinical research on novel diagnostic groups, the impairment scales used herein have not been validated on this population specifically, however, given the ability of the tools to describe the laryngeal pathology, we suggest this may be clinically valuable to teams moving forwards whilst reliability and validity tests are undertaken. As this was a clinically based team, there was no blinded scoring of the laryngeal assessment increasing risk of confirmation bias. Regardless, our findings offer the first systematic approach to functional airway assessment following tracheostomy and severe COVID-19, offering unique information to clinical teams managing this challenging clinical presentation of laryngeal compromise.
Conclusion
Our findings highlight the functional relationships between the anatomy and physiology of the larynx and cumulative outcomes following artificial airway insertion. In our institution, patients who required tracheostomy following COVID-19 presented with impaired airway protection and marked airway oedema in at least one laryngeal area. Impaired airway protection was associated with longer total duration of artificial airway, longer tracheostomy tube duration, and multiple intubations. We suggest proactive assessment, standardised scoring, and patient risk stratification to enable the clinical team to create collaborative and effective decannulation plans.
Acknowledgements
CD takes responsibility for the content and integrity of the manuscript including the data and analysis. Author contributions: CD, PP, NS, PN contributed substantially to the study design and data collection. SS, NS undertook data analysis and interpretation. CD, NS, SS, PN, DP, JP contributed to writing and review of the manuscript. MW and RC supported data collection and manuscript review. The team thank Sarah Adamson, Niki Oveisi, Robyn Jones and Tahira Tejpar for their significant support managing the data.
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