key: cord-0779958-s4fcnyr6 authors: Clayton, Nicola A.; Walker, Elizabeth; Freeman-Sanderson, Amy title: Clinical profile and recovery pattern of dysphagia in the COVID-19 patient: a prospective observational cohort within NSW date: 2022-01-14 journal: Aust Crit Care DOI: 10.1016/j.aucc.2022.01.001 sha: 45007ee7876ba2fa145fba92439c753d458c47c1 doc_id: 779958 cord_uid: s4fcnyr6 BACKGROUND: The impact of COVID-19 on swallowing function is not well understood. Despite low hospital admission rates in Australia, the virus and subsequent treatment affects swallow function in those requiring Intensive Care Unit (ICU) treatment. As such, the current pandemic provides the unique opportunity to describe swallowing function, outline dysphagia characteristics and trajectory of recovery for a series of cases across NSW. AIM: To describe 1) physiological characteristics of swallowing dysfunction and 2) pattern of swallowing recovery and outcomes, in ICU patients with COVID-19. METHODS: All patients admitted to 17 participating NSW Health ICU sites over a 12-month period (March 2020–March 2021), diagnosed with COVID-19, treated with the aim for survival and seen by Speech Pathology for clinical swallowing examination during hospital admission, were considered for inclusion. Demographic, critical care airway management, speech pathology treatment and swallowing outcome data were collected. RESULTS: 27 patients (22-male; 5-female) median age 65 years (IQR=15.5) were recruited. All required mechanical ventilation. Almost 90% of the total cohort had pre-existing co-morbidities with the two most frequently observed being diabetes (63%, 95%CI=44%–78%) and cardiac (59%, 95%CI=40%-75%) in origin. Prevalence of dysphagia was 93% with the majority (44%) exhibiting profound dysphagia at initial assessment. Median duration to initiate oral feeding was 38.5 days (IQR=31.25) from ICU admission, and 33% received dysphagia rehabilitation. Dysphagia recovery was observed in 81% with a median duration of 44 days (IQR=29). Positive linear associations were identified between duration of intubation, mechanical ventilation, Hospital and ICU LOS, and the duration to Speech Pathology assessment (p<0.005), dysphagia severity (p<0.002), commencing oral intake (p<0.02), dysphagia recovery (p<0.004) and enteral feeding (p<0.024). CONCLUSION: COVID-19 considerably impacted swallowing function in the current study. Whilst many patients recovered within an acceptable timeframe, some experienced persistent severe dysphagia and a protracted recovery with dependence on enteral nutrition. The speech pathologist, as a core member of the multidisciplinary Intensive Care Unit (ICU) team, is responsible for the timely and comprehensive management of complex swallowing and communication disorders. Such disorders may arise as a result of patient's medical or surgical diagnosis, and/or as a result of necessary ICU therapies including mechanical ventilation. Dysphagia in ICU patients has been associated with variables including duration of intubation 1,2,3,4,5,6,7,8,9 , presence of tracheostomy 10 , advanced age 11 in addition to acute deconditioning 12 . Presence of dysphagia in respiratory disease is also not uncommon, with incidence rates in conditions such as Chronic Obstructive Pulmonary Disease (COPD) documented as high as 85% 13 . The pathophysiology behind dysphagia in both the ICU as well as respiratory patient appears to be multifactorial in nature, with evidence indicating anatomical changes 14 , physiological deficits in laryngopharyngeal sensitivity 15 , laryngeal and pharyngeal motor function 16, 17, 18, 19, 20, 21 , as well as altered breath-swallow synchrony 22 . These physiological and anatomical changes translate into altered patterns of swallowing 20, 21 manifesting as a reduction in bolus flow efficiency, impaired airway closure as well as diminished airway responsiveness. As such, patients in the ICU and with respiratory disease are at greater risk of dysphagia and aspiration, and may take an increased duration to commence oral intake, thus increasing their dependence on enteral nutrition. Given the complex and multifactorial profile of dysphagia in ICU patients, evidence suggests that application of instrumental swallowing assessment should be considered 23, 24 . Flexible Endoscopic Evaluation of Swallowing (FEES) is frequently reported as the instrument of preference 25, 26, 16 given the high incidence of laryngeal impairment, medical fragility and inability to easily transport these patients to the radiology department for other instrumental swallow assessments such as videofluoroscopy 23 . Furthermore, although the role of the Speech Pathologist and application of FEES within the ICU is well recognised in the literature, referral protocols and degree of Speech Pathology input along the care pathway remain largely site specific and at the discretion of the treating intensivist. A patient under the care of a Speech Pathologist within ICU, as well as throughout acute and rehabilitative admission receives assessment and treatment in line with national standards as outlined by the national peak body, Speech Pathology Australia. Dysphagia management includes regular clinical review of swallowing function and application of compensatory as well as therapeutic strategies with the aim to optimise safe diet and fluid consumption, enhance nutritional intake in addition to maximising quality of life 27 . The impact of severe acute respiratory distress syndrome coronavirus 2 (SARS-COV2) on swallowing function is currently not well understood 28, 29 . Whilst the literature regarding dysphagia in patients with COVID-19 is currently limited, early evidence suggests a dysphagia prevalence of approximately J o u r n a l P r e -p r o o f 30% in those requiring hospitalisation 30 . Looking specifically at the COVID-19 patient in ICU, data from international colleagues suggest that this dysphagia prevalence increases, with rates cited from 50% 25 to 90% 31, 32 in those who require ICU treatment. Furthermore, authors have indicated that in this population, both the presence and duration of an endotracheal tube is positively correlated with dysphagia 33,25 however there is conflicting data regarding whether prone positioning for ventilation is associated with or predictive of dysphagia 28, 27 . Encouragingly, overall dysphagia recovery in the ICU COVID-19 patient post extubation is rapid 26 with 70-90% regaining normal swallowing function during inpatient admission 28, 25, 27 . Those who did experience persistent dysphagia frequently had pre-existing swallowing impairment or neurological diagnosis 28 . Currently in Australia, we are fortunate to have much lower rates of COVID-19 than our international colleagues. Subsequently, we have had a relatively low rate of COVID-19 hospital admissions although we still see that the virus and its subsequent treatments, can affect swallow function in those who require ICU treatment. As such, speech pathology assessment and management of COVID-19 related dysphagia has been necessary. With evidence defining the impact of COVID-19 on swallow function still emerging, the current pandemic provided us with the unique opportunity to describe swallowing function, outline clinical dysphagia characteristics and trajectory of recovery for a series of Australian cases treated in ICU with confirmed COVID-19. The aims of the study were to describe the 1) physiological characteristics of swallowing dysfunction, and 2) pattern of recovery and outcomes for swallowing, in Intensive Care Unit (ICU) patients with COVID-19. This study has been conducted and reported in line the STROBE statement 34 . A multi-site prospective observational cohort study. A cohort of adult patients (aged 18-100 years) with confirmed COVID-19, admitted to Intensive Care Units across 17 participating NSW Public Hospitals (metropolitan and rural), and referred to Speech Pathology for face-to-face assessment of swallowing function during their acute hospital admission as per usual site specific referral practices, were considered for inclusion within the study. The study J o u r n a l P r e -p r o o f was conducted over a period of 12 months (1st March 2020 -1st March 2021) with patients recruited only if the intention to treat was for survival. Demographic data points collected on all participants from medical records included age, sex, hospital length of stay (LOS) in days and past medical history including pre-existing dysphagia. Intensive Care Unit (ICU) specific data collected incorporated ICU LOS (days), APACHE-II 35 3=tube dependent with consistent intake of food and fluid; 4=total oral diet of a single consistency; 5=total oral diet with multiple consistencies but requiring special preparation or compensations; 6=total oral with multiple consistencies without special preparation, but with specific food limitations; 7= total oral diet with no restriction. Dysphagia management was deemed complete once the patient had either achieved a premorbid level of swallowing function ability, or their swallow function had plateaued such that further improvement was deemed unlikely by the treating Speech Pathologist. Dysphagia resolution was defined by the ability to consume a full oral diet and fluids without modification or the aid of compensatory strategies. Other specific swallowing endpoints included capturing information relevant to commencing oral intake, dysphagia rehabilitation, dysphagia resolution, instrumental assessment outcomes (if conducted) and non-oral (enteral) feeding. These endpoints are further detailed in Table 1 . All swallowing data relating to duration were calculated in days from the time of ICU admission. In the J o u r n a l P r e -p r o o f instance that Videofluoroscopic Swallowing Study (VFSS) was conducted as part of standard of care, swallowing outcome measures applied to describe swallowing impairment were the Penetration-Aspiration Scale (PAS) (Rosenbek et al 1996) The PAS is an 8-point scale that describes the degree of food/fluid airway invasion and airway response, where 1 = no laryngeal penetration/aspiration and 8 = aspiration below the level of the vocal folds with nil airway response. The BRS is a 6-point scale which describes the degree of postswallow pharyngeal residue, where 1 = no residue and 6 = residue in the valleculae and posterior pharyngeal wall and piriform sinus. Each of these scales are simple tools that can be efficiently applied to objectify VFSS interpretation specific to penetration/aspiration and pharyngeal clearance. Insert Table 1 about here Individual site data were collected and entered by local site investigators and input into a purpose built password protected REDCap database 38 via a secure survey link. A data dictionary defining each data point was provided to all sites to minimise bias. To ensure completeness of data, the REDCap database 32 was designed so that each data field (with the exception of APACHE-II 30 score) was mandatory. Anonymised data (de-identified at the point of data entry) was exported via an encrypted secure link generated by REDCap 32 . This was subsequently downloaded for analysis in Excel and the Statistical Package for Social Sciences (SPSS Version 27.0). Descriptive statistics were utilised to analyse all data. Normally distributed data is presented as means and standard deviation [mean (SD)], with non-normal data reported as medians and IQR [median (IQR)]. Categorical data is presented as a proportion of the sample [n(%)]. Correlation statistics between variables determined a priori, was conducted using non-parametric assessments (Mann-Whitney U) between continuous and dichotomous variables, Spearman's rho between two continuous variables and Fishers Exact Test between dichotomous variables, with statistical significance set at p<0.05. Precisions of estimates were reported as 95% confidence intervals (CI, with normal approximation method). This study received ethical approval (2020/ETH01301) from the CRGH Human Research & Ethics Committee. Written consent for the purposes of gathering outcomes was sought and obtained from all cases prior to data collection. A total of 27 patients (22 male; 5 female) were recruited to participate in the study over the 12 month period (March 2020 -March 2021). Seventeen NSW Public Hospitals contributed to participant recruitment. The median age of the cohort was 65 years (range 38-81, IQR 15.5) with all requiring mechanical ventilation and 59% (n=16) tracheostomy as part of their ICU treatment. Almost 90% (n=24) of the total cohort had pre-existing co-morbidities with the 2 most frequently observed being diabetes (63%, n=17; 95%CI = 44% -78%) and cardiac disease (59%, n=16; 95%CI = 41% -75%). Only one patient, who had multiple co-morbidities including gastro-oesophageal reflux and recurrent oesophageal stenosis, had a known pre-existing dysphagia prior to admission (4%, n=1; 95%CI = 1% -18%). The majority (74%, n=20) of participants exhibited under five co-morbidities indexed prior to hospital admission. During the study period, a range of in-hospital complications were documented for participants. The most frequently occurring complications were ICU Acquired Weakness (74%, n=20; 95%CI = 55% -87%) and delirium (70%, n=19; 95%CI = 51% -84%). Participant discharge destination was most commonly home (70%, n=19; 95%CI = 51% -84%) followed by another inpatient facility (26%, n=7; 95%CI = 13% -45%). The in-hospital survival rate was 96% (n=26; 95%CI = 82% -99%). The detailed summary of demographic and critical care data is contained in Table 2 . Insert Table 2 Prevalence of dysphagia on initial assessment across the total cohort was 93% (n=25) with the majority (n=12, 44%) exhibiting profound dysphagia (FOIS 1) followed by those (n=10, 37%) who were able to commence a modified diet (FOIS 5) at the point of initial assessment. Of the remaining 11% (n=3) who were dysphagic on initial assessment, 4% (n=1) were tube dependent with minimal attempts of food or fluid and 7% (n=2) were able to tolerate a total oral diet but required specific food limitations. Calculated from the time of ICU admission, median duration to initial Speech J o u r n a l P r e -p r o o f Pathology consultation (DSPA) (either face-to-face or via TeleHealth) was 29 days (IQR 23) whereas median duration to face-to-face initial assessment (DFSPA) was 33 days (IQR 18). Duration to initiation of oral feeding (DIOF) was observed at a median of 38.5 days (IQR 31.25) from time of admission to the ICU, and for those who received therapeutic dysphagia rehabilitation (33%), the period to commencing dysphagia rehabilitation (DCDR) occurred at a median of 39 days (IQR 17). Dysphagia rehabilitation was not indicated in 63% (n=17) of participants (due to persistent delirium and/or favouring traditional compensatory strategies), and was not able to be provided due to COVID considerations in 4% (n=1). Resolution of dysphagia by time of discharge from the acute care facility was achieved in 81% (n=22) of all participants, with a median duration (DROD) of 44 days (IQR 29). Enteral feeding was required in all cases, with a median period (DOEF) of 40 days (IQR 37). For the one third of participants who received dysphagia rehabilitation (n=9), the majority (n=8, 89%; 95%CI = 57% -98%) had a FOIS score of 1 or 2 indicating profound dysphagia at the point of initial assessment. These participants also took longer commence oral intake (median 48 days, IQR 11) compared to those who did not require dysphagia rehabilitation (median 34 days, IQR 24). Of note, dysphagia rehabilitation was initiated prior to commencing oral intake in all but one of the nine cases, dysphagia resolution took longer (median 77 days, IQR 27), with four (44.45%) unable to achieve dysphagia resolution. Furthermore, enteral feeding duration was longer in the rehabilitation No association was identified between participant age and any swallowing outcomes reported. Nor was there an association between duration of intubation or mechanical ventilation and duration to J o u r n a l P r e -p r o o f commence dysphagia rehabilitation. There was however, significant positive linear associations identified between duration of intubation, mechanical ventilation, Hospital and ICU LOS, and the duration to Speech Pathology assessment, commencing oral intake, dysphagia recovery and enteral feeding. Conversely, a negative linear association was identified between dysphagia severity and duration of intubation, mechanical ventilation, Hospital and ICU LOS. This is reflective of a lower FOIS score (indicating more severe swallowing impairment) being associated with longer duration of medical interventions and LOS. All swallow association results are summarised in Table 3 . More than half of participants within the cohort required tracheostomy as part of their ICU treatment (n=16). Whilst the presence of tracheostomy was not associated with whether dysphagia recovery was achieved (p=0.06), nor the duration to commence dysphagia rehabilitation (Z=-2.049, p=0.056), it was associated with severity of dysphagia (Z=-2.100, p=0.05), DIOF (Z=-2.934, p=0.002), DROD (Z=-3.056, p=0.001) and DOEF (Z=-3.112, p=0.001). Pathology is high. ICU Acquired Weakness and delirium also commonly occur in these patients and is likely the sequelae of critical illness. Severity of dysphagia is found to often be profound on initial assessment and is associated with increase duration of endotracheal intubation, mechanical ventilation, ICU and hospital LOS. Prognosis for dysphagia recovery during the acute admission is relatively good with most patients discharged home or transferred to inpatient rehabilitation on separation from the acute care facility. Participant demographic and critical care data within the current cohort were overall consistent with those existing published studies who also examined patients referred to Speech Pathology. Similar characteristics included elevated rates of delirium 25, 28 , and mean age 25, 27 although average duration of endotracheal intubation in the current study was longer (19 days compared to 14 days) 28, 27 . Despite the cohort being much smaller to those of our international colleagues, dysphagia prevalence was comparable to those recently published studies 25, 28, 27 . Furthermore, our observed severity of dysphagia was also comparable to the data presented by Dawson et al (2020) 25 Optimistically and similar to existing literature 26, 28, 25, 27 , we observed encouraging rates of dysphagia J o u r n a l P r e -p r o o f resolution at the point of discharge from the acute care facility. Interestingly however, whilst our international colleagues have commented on adverse neurological co-morbidities as the cause for persistent dysphagia 28 , secondary neurological pathology was fortunately not observed in our cohort. Penetration-aspiration results on instrumental assessment have only been documented in one other published study to date. Similar to the current study, Sandblom et al (2021) 35 observed worse PAS scores for fluids compared with solids. Furthermore, impaired pharyngeal clearance 41 (defined by BRS in the current study) also appeared to be a feature consistent between to the two studies. The cause for worse PAS and BRS scores is postulated to be commensurate with the profile of swallowing impairment in critical illness which is further explored below. We identified several associations between critical care data and swallowing outcomes. Specifically, presence and duration of endotracheal intubation, presence of tracheostomy, duration of mechanical ventilation, ICU and hospital LOS were associated with poorer swallowing outcomes and increased periods of enteral feeding. These results are analogous with those already published 25, 28, 27 . Contrary to our findings however, Regan et al (2021) 27 identified that age was also associated with poorer swallowing outcomes where we did not. Moreover, Regan et al (2021) 27 identified two other variables as predictors for dysphagia: proning and history of respiratory disease. Proning was not captured in the present study and history of respiratory disease, whilst present in some participants, was not observed at a high frequency. Finally, the duration to initiate oral intake calculated from the point of intubation was able to be compared with the Dawson et al (2020) 25 study only, with an apparent increased delay in commencing oral intake for participants in the present study (40 days compared to 22 days). Postulating the pathophysiology behind the mechanism of dysphagia specifically in the COVID-19 patient, there are several aspects that are consistent with existing literature on dysphagia in critical illness 24 . Existing evidence indicates that dysphagia in critical illness may manifest as delay in swallow onset, impaired airway closure, high rates of laryngeal penetration and aspiration, diminished efficiency and effectiveness of cough response with worse swallow outcomes observed when various forms of laryngeal injury were co-present 16 . Further to this, presence of the endotracheal tube itself has been associated with a reduction in base of tongue muscle bulk, base of tongue strength, in addition to diminished laryngeal sensation, vocal cord damage and compression of the recurrent laryngeal nerve by the endotracheal tube cuff 14 . In addition to critical illness, other cooccurring medical conditions including neurological 8, 42 and respiratory disease 26 are known to J o u r n a l P r e -p r o o f further complicate the swallowing profile. Specifically, diseases of the respiratory system such as Acute Respiratory Distress Syndrome (ARDS) can disrupt normal coordination of the respiratoryswallow cycle 26 . Whilst there is no evidence regarding breath-swallow synchrony in COVID-19, this is another factor that needs to be considered. To date, only one very recent study has documented the pathophysiology of dysphagia in the COVID-19 patient, suggesting in accordance with Flexible Endoscopic Evaluation of Swallowing (FEES) outcomes that reduced pharyngeal muscle strength, impaired airway closure and laryngeal sensation were at the core of dysphagia in this population 35 . Interestingly however, both Lima et al (2021) 26 and Archer et al (2021) 28 describe that dysphagia resolves more rapidly in COVID-19 patients when compared to non-COVID critically ill patients, highlighting the importance of assessment and compensatory strategies, and suggesting that weakness alone may not be the primary origin for dysphagia. This indicates that more work is required to fully understand the mechanisms underpinning dysphagia in the COVID-19 patient. Further to this, knowledge gained will also guide methods of multidisciplinary team driven rehabilitation, to optimise and expedite dysphagia recovery which is clearly indicated in a proportion of these patients 43 . This paper is the first of its kind across Australia to describe the clinical profile of dysphagia in ICU patients with COVID-19 and the clinical applicability of results is strengthened by its multi-site methodology and use of clearly defined outcome measures. There are however, several limitations to the execution and interpretation of this study. Firstly, routine instrumental assessment and specifically FEES, which is accessible in many tertiary ICUs and well accepted to be the gold standard for the provision of swallow kinematic information in ICU patients was lacking. This was due to the universally and internationally accepted recommendations to avoid Aerosol Generating Procedures in the efforts to promote staff safety by minimising viral transmission 44 . Other studies to date have also cited this aspect as a limitation to investigating the nature of dysphagia in the COVID-19 positive patient 25, 28, 27 . Secondly, the absence of detail regarding dysphagia rehabilitation strategies has not allowed for in depth understanding of the swallowing rehabilitation needs of this population. Thirdly, the small sample size, whilst fortunate from a population health perspective, suggests that these results should be interpreted with caution. Fourthly, the sample was limited by the inclusion criteria that not all those patients admitted to ICU were seen by Speech Pathology, only those who were referred resulting in a possible under reporting of dysphagia prevalence. However, the inclusion of only those who were referred to speech pathology for assessment may also lead to an overestimation of the severity of dysphagia in the cohort, as those with only mild issues may not have been referred. It would be challenging to assert that COVID-19 patients undergo routine J o u r n a l P r e -p r o o f Speech Pathology examination, again due to the highly transmissible nature of this virus. Furthermore, differences in individual site practices and infection control protocols may have resulted in delays in the provision of care. Finally, very recent studies from international colleagues indicate that laryngeal pathology may be an issue in the post-extubation and tracheostomy patient with COVID-19 27, 35, 45, 38 . As such, future studies examining the ICU COVID-19 patient, detailing outcomes specific to voice, laryngeal pathology as well as dysphagia rehabilitation is recommended. Consistent with international evidence, diagnosis of COVID-19 in the current study had considerable impact upon patients' swallowing function across NSW ICU's, with high prevalence and severity dysphagia apparent on initial assessment. Dysphagia was associated with increased duration of intubation, mechanical ventilation, hospital and ICU LOS with one third requiring active dysphagia rehabilitation. Whilst many patients in the present study recovered within an acceptable timeframe, some experienced persistent severe dysphagia and a protracted recovery with dependence on enteral nutrition. Further work is required to investigate the pathophysiology underpinning dysphagia in this population and the appropriate multidisciplinary rehabilitative strategies that should be applied to optimise and expedite swallow recovery. 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