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Dysphagia in patients with coronavirus disease undergoing orotracheal intubation

Abstract Objective To assess the incidence and the risk factors for the development of dysphagia in patients with coronavirus disease 2019 (COVID‐19) undergoing orotracheal intubation. Study Design Prospective cohort study. Methods In this prospective cohort study, we evaluated consecutive patients diagnosed with COVID‐19 and underwent orotracheal intubation were evaluated. During hospitalization, extubated patients were classified as dysphagic and nondysphagic based on bedside functional assessment of swallowing. Patients discharged from hospital were asked to complete the Eating Assessment Tool‐10 (EAT‐10) questionnaire, followed by an endoscopic examination to identify laryngotracheal lesions, and a fiberoptic endoscopic evaluation of swallowing (FEES). The food consistencies used for FEES were moderately thick, extremely thick, thin, and regular. Results Based on the functional assessment of swallowing, performed a mean of 5.3 days and a median of 4 days after extubation, the incidence of dysphagia in patients with COVID‐19 undergoing orotracheal intubation was 53.6%. In the late evaluation, performed a mean of 102 days after extubation, 12.8% of patients had an EAT‐10 score >2. Orotracheal intubation (OTI) duration and tracheostomy were risk factors for the development of dysphagia. There was an association between EAT‐10 > 2 and the presence of laryngotracheal lesion, with no difference between lesion type and EAT score >2. Conclusions The incidence of dysphagia varied according to the time of assessment, being higher the earlier the assessment after extubation. OTI duration and tracheostomy were risk factors for the development of dysphagia, and the presence of laryngotracheal lesions demonstrated an association with dysphagia. Level of Evidence 3.


| INTRODUCTION
In December 2019, a new disease caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) emerged and spread around the world, and coronavirus disease 2019 (COVID- 19) was declared a pandemic on March 11, 2020 by the World Health Organization. 1,2 SARS-CoV-2 is an RNA virus that can cause symptoms including fever, cough, myalgia, fatigue, odynophagia, and dysphagia. [3][4][5] The severe form of the disease is characterized by acute respiratory distress syndrome (ARDS), which leads to the need for respiratory support using orotracheal intubation (OTI) and mechanical ventilation. 1 Early OTI is the most recommended first-line intervention for patients infected with SARS-CoV-2 who develop ARDS. This procedure has the potential to trigger acute and chronic symptoms resulting from injury from the endotracheal tube (ETT). OTI is a risk factor for the development of dysphagia, characterized by dysfunctional coordination between swallowing and breathing, which makes patients susceptible to aspiration of saliva and other secretions. 2,6,7 The assessment of swallowing efficiency is extremely important in COVID-19 survivors because these patients are prone to develop respiratory complications. 8 The objective of this study, therefore, was to assess the incidence of and risk factors for the development of dysphagia in patients with COVID-19 undergoing OTI.

| METHODS
This study was approved by the Institution's Research Ethics Committee under protocol number 38470620.0.0000.5463. A prospective cohort study of consecutive patients undergoing OTI and diagnosed with COVID-19 using real-time polymerase chain reaction test (RT-PCR) and admitted to a tertiary hospital from March 1 to October 31, 2020, was performed.
OTI was performed by the institution's rapid response team, which was composed of members of the anesthesiology team. All patients undergoing OTI were evaluated for outcomes, including death or extubation, followed by evaluation from the dysphagia team, which was composed of speech-language pathologists specialized in dysphagia from the institution's department of speech-language pathologists. Patients extubated and evaluated by the dysphagia team during hospitalization were classified as dysphagic or nondysphagic based on bedside functional assessment of swallowing, that was restricted from invasive methods to reduce the exposure of the dysphagia team in the pandemic. Functional evaluation of swallowing included the initial administration of homogeneous creamy foods, followed by fractionated liquefied creamy foods, and then solid foods. 9,10 Patients discharged from hospital were called for outpatient follow-up to complete the Eating Assessment Tool-10 (EAT-10) 11,12 questionnaire, followed by endoscopic examination (video flexible rhino-pharyngo laryngoscopy and video-laryngoscopy) for diagnosis of laryngotracheal lesions and fiberoptic endoscopic evaluation of swallowing (FEES). Patients with an EAT-10 score >2 underwent FEES. All patients who participated in this stage of the study completed the informed consent for the videoendoscopy exams. . 13 The administered volumes were 3, 5, 10, and 15 ml. The parameters analyzed included saliva stasis in the valleculae and piriform recesses and, after three successive swallows, the presence of laryngeal penetration, laryngotracheal aspiration, and food residue at the base of the tongue, valleculae, and piriform recesses. Videos for the diagnosis of swallowing disorders were analyzed by a multidisciplinary team comprising two laryngologists and a speech-language pathologist specialized in dysphagia, who were all blinded to patient data.
Patients who presented with dysphagia before COVID-19 diagnosis, those unable to undergo testing, and those absent a COVID-19 RT-PCR laboratory diagnosis were excluded. The pre-existing dysphagia was identified through patient self-report. The following data were collected to evaluate the included patients: age; sex; comorbidities (systemic arterial hypertension, diabetes mellitus, and obesity); ETT size; OTI duration (days); tracheostomy; need for reintubation; time between extubation and assessment by the speech-language pathologists team (days); patient classification into dysphagic and nondysphagic; length of hospital stay; length of intensive care unit (ICU) stay; length of ICU stay after extubation; length of hospital stay after extubation (days); and, finally, presence of laryngotracheal lesion(s).
The data collected formed a database developed in a spreadsheet   Table 1).
The mean OTI duration for dysphagic patients was 12.6 ± 7.9 days (range, 3-36 days), and 10.4 ± 8.4 days (range, 3-39 days) for nondysphagic patients. OTI duration (days) was an important risk factor for the development of dysphagia (Table 1). Tracheostomy was performed in six (5.4%) patients among those who were extubated and evaluated by the speech-language pathologist team (n = 112), all of whom were considered dysphagic (Table 2), which was statistically significant (p = .019). Dysphagic patients experienced a statistically increased length of hospital stay, ICU stay, ICU stay after extubation, and hospital stay after extubation (Table 3).
In outpatient evaluation, 94 (54.7%) patients were re-evaluated and completed the EAT-10 questionnaire, 11   patients who were not evaluated at this stage included inability to contact (n = 1), clinical inability to attend the test (n = 1) and moved to another state (n = 1).

| DISCUSSION
The incidence of dysphagia in patients undergoing OTI varies widely (3%-83%), which may be explained by the use of different study methods, time of patient assessment, diagnostic methods, and population heterogeneity (trauma, stroke, acute myocardial infarction, and postoperative period). 6,14,15 Thus, the literature emphasizes that patients undergoing prolonged OTI and with risk factors for dysphagia and aspiration should undergo early speech-language pathologists assessment. 16 Because it is a noninvasive, rapid, and low-cost assessment method, it widely used as the only means of assessing dysphagia in some hospitals. 17  Male patients experienced a more severe course of COVID-19 at an earlier age than females (p = .015). This disease behavior may be related to hormonal factors and the higher prevalence of comorbidities in males (hypertension, smoking, and coronary artery disease). [18][19][20][21][22] The onset of dysphagia can be triggered by the aging process. [23][24][25][26] In the literature, the correlation of age as a risk factor for the development of dysphagia after OTI is controversial for non-COVID patients. 7,14,[27][28][29][30][31] In this study, elderly COVID-19 patients undergoing OTI did not have a higher risk for developing dysphagia than younger patients.
Increased OTI duration and the length of ICU stay are associated with a higher incidence of swallowing disorders. 32 (Table 2), with a statistically significant difference (p = .019). These different incidences can be explained by the different methods used to assess dysphagia and the time of assessment after extubation. 28 Patients developing swallowing disorders during ICU stay are more likely to experience adverse health events such as poor nutritional intake, dehydration, aspiration pneumonia, and death. In addition, dysphagia leads to a prolonged length of hospital stay and increases morbidity and mortality rates. 4,45,46 The presence of dysphagia predicted an increased length of hospital stay, ICU stay, ICU stay after extubation, and hospital stay after extubation ( During the COVID-19 pandemic, health services should be prepared for the adequate assessment and treatment of patients with oropharyngeal dysphagia. Thus, it is necessary to consider swallowing disorder complications and care of health professionals exposed to the risk for aerosol contamination. 55 FEES is an adequate method and is considered to offer adequate sensitivity and specificity for diagnosing dysphagia. [56][57][58] In this study, there was a need to balance the risks and benefits of aerosol exposure, and FEES was performed as the last assessment method. On average, 129.2 days after extubation, only one patient exhibited persistent laryngeal penetration and laryngotracheal aspiration. The context of the COVID-19 pandemic represents a limitation for video-endoscopy. Thus, it was not possible to evaluate patients at specific times (e.g., 90, 120, and 180 days). However, it was possible to verify that the diagnosis of laryngotracheal lesions in patients with COVID-19 undergoing OTI had an association with swallowing disorders or EAT-10 score >2.

| CONCLUSION
The incidence of dysphagia varied according to the time of assessment, and was more prevalent the earlier the assessment after extubation. OTI duration and tracheostomy were risk factors for the development of dysphagia, and the presence of laryngotracheal lesions demonstrated an association with dysphagia, regardless of lesion type (i.e., inflammatory or scarring).

ACKNOWLEDGMENT
The authors would like to thank Vitor Takabatake Gomes Costa for willingness to review our article from a statistical perspective.