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Dysphagia Characteristics of Patients Post SARS-CoV-2 During Inpatient Rehabilitation

Published:October 29, 2021DOI:https://doi.org/10.1016/j.apmr.2021.10.007

      Highlights

      • High prevalence of post-COVID dysphagia in inpatient rehabilitation
      • 15% increased odds of silent aspiration with each additional day of intubation
      • Clinical swallow evaluation was a poor predictor of aspiration
      • Heterogeneity of dysphagia after COVID requires instrumental evaluation

      Abstract

      Objective

      To investigate dysphagia in patients recovering from SARS-CoV-2 admitted to acute inpatient rehabilitation by summarizing clinical swallow evaluation and videofluoroscopic swallow study findings.

      Design

      Retrospective cohort study.

      Setting

      Urban inpatient rehabilitation hospital.

      Participants

      The first inpatients admitted with SARS-CoV-2 (N=40) who participated in a videofluoroscopic swallow study.

      Interventions

      Not applicable.

      Main Outcome Measures

      Patient characteristics upon admission (duration of intubation, tracheostomy status, comorbidities, videofluoroscopic swallow study (VFSS) completion at previous level of care); admission International Dysphagia Diet level (IDDSI); Mann Assessment of Swallowing Ability (MASA), Functional Oral Intake Scale (FOIS), dysphagia severity rating; penetration aspiration scale (PAS) rated during VFSS; and IDDSI level recommended after completion of VFSS.

      Results

      Twenty percent of patients had been evaluated by videofluoroscopy in acute care. Nineteen of 37 (51%) individuals were upgraded to IDDSI level 7 regular diet with level 0 thin liquids and achieved a FOIS of 7 after the completion of the VFSS. Five individuals (13%) received a diet downgrade or remained on the same diet recommendations from their admission. Total numerical score (TNS) of less than 170 on the MASA predicted presence of aspiration in 27% of patients (6 of 22). Seventy-two percent of the sample (16 of 22) had a TNS less than 170 but did not demonstrate any instances of aspiration. The odds of patients having a PAS of 3 or greater increased by approximately 15% (odds ratio, 1.15; 95% confidence interval, 1.03-1.27; P=.013). Thus, with each additional day of intubation during acute care stay, there was a 15% greater likelihood of having airway invasion.

      Conclusions

      Instrumental swallow evaluations are imperative to diagnose and treat dysphagia in the post-coronavirus disease population. Because of the heterogeneity of this population, high incidence of prolonged intubation, and limitations of the clinical swallowing evaluation, instrumental assessments need to be performed on a more consistent basis as infection prevention protocols evolve.

      Keywords

      List of abbreviations:

      FEES (fiberoptic endoscopic evaluation of swallowing), FOIS (Functional Oral Intake Scale), IDDSI (International Dysphagia Diet Standardization Initiative), LAR (likelihood of aspiration ratio for stroke patients), MASA (Mann Assessment of Swallowing Ability), PAS (penetration aspiration scale), SLP (speech language pathologist), TNS (total numerical score), VFSS (videofluoroscopic swallow study)
      Patients recovering from severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) reportedly present with dysphagia or difficulty swallowing.
      • Frajkova Z
      • Tedla M
      • Tedlova E
      • Suchankova M
      • Geneid A.
      Postintubation dysphagia during COVID-19 outbreak-contemporary review.
      With the onset of the coronavirus disease 2019 (COVID-19) pandemic, the nature of dysphagia care shifted significantly, with multiple guidelines published to address the safe evaluation and treatment of patients with dysphagia in acute care.
      • Bolton L
      • Mills C
      • Wallace S
      • Brady MC
      Royal College of Speech and Language Therapists (RCSLT) COVID-19 Advisory Group. Aerosol generating procedures, dysphagia assessment and COVID-19: a rapid review.
      • Brodsky MB
      • Gilbert RJ.
      The long-term effects of COVID-19 on dysphagia evaluation and treatment.
      • Mattei A
      • de la Bretèque BA
      • Crevier-Buchman L
      • et al.
      Guidelines of clinical practice for the management of swallowing disorders and recent dysphonia in the context of the COVID-19 pandemic.
      • Miles A
      • Connor NP
      • Desai RV
      • et al.
      Dysphagia care across the continuum: a multidisciplinary Dysphagia Research Society Taskforce report of service-delivery during the COVID-19 global pandemic.
      However, little has been published providing guidance for the evaluation and treatment of this patient population after they leave acute care and enter inpatient rehabilitation.
      The pandemic prompted reflection on infection prevention protocols as well as a designation by some groups that dysphagia assessment and treatment produce aerosolized droplets, resulting in recommendations to use noninvasive and noninstrumental means to evaluate dysphagia.
      • Bolton L
      • Mills C
      • Wallace S
      • Brady MC
      Royal College of Speech and Language Therapists (RCSLT) COVID-19 Advisory Group. Aerosol generating procedures, dysphagia assessment and COVID-19: a rapid review.
      ,
      • Brodsky MB
      • Gilbert RJ.
      The long-term effects of COVID-19 on dysphagia evaluation and treatment.
      ,
      • Miles A
      • Connor NP
      • Desai RV
      • et al.
      Dysphagia care across the continuum: a multidisciplinary Dysphagia Research Society Taskforce report of service-delivery during the COVID-19 global pandemic.
      However, instrumental examination via videofluoroscopy (VFSS) or via fiberoptic endoscopic evaluation of swallowing (FEES) is considered best practice in evaluating swallowing physiology, determining the presence or absence of aspiration, directing behavioral interventions to improve function, and guiding diet consistency recommendations.
      • Martin-Harris B
      • Canon CL
      • Bonilha HS
      • Murray J
      • Davidson K
      • Lefton-Greif MA.
      Best practices in modified barium swallow studies.
      With more restricted use of instrumental assessments, a higher reliance was placed on the clinical swallow examination, with caveats limiting completion of a full oral mechanism examination, assessment of cough strength, and gag reflex.
      • Namasivayam-MacDonald AM
      • Riquelme LF.
      Speech-language pathology management for adults with COVID-19 in the acute hospital setting: initial recommendations to guide clinical practice.
      To date, specific information related to the etiology and nature of dysphagia has not yet been published for the inpatient rehabilitation setting after acute care hospitalization for COVID-19.
      • Brodsky MB
      • Gilbert RJ.
      The long-term effects of COVID-19 on dysphagia evaluation and treatment.
      Proposed mechanisms of dysphagia after COVID-19 include peripheral and central nervous system disruption, intubation, debility, and pulmonary dysfunction.
      • Frajkova Z
      • Tedla M
      • Tedlova E
      • Suchankova M
      • Geneid A.
      Postintubation dysphagia during COVID-19 outbreak-contemporary review.
      Confounding the effect of SARS-CoV-2 on swallowing function was an acute care management trend toward longer periods of endotracheal intubation.
      • Piazza C
      • Filauro M
      • Dikkers FG
      • et al.
      Long-term intubation and high rate of tracheostomy in COVID-19 patients might determine an unprecedented increase of airway stenoses: a call to action from the European Laryngological Society.
      The Centers for Disease Control and Prevention identifies tracheostomy placement as a procedure that produces aerosolized droplets with greater risk for infection spread, and many infection prevention protocols initially discouraged tracheostomy placement with this population.
      • Piazza C
      • Filauro M
      • Dikkers FG
      • et al.
      Long-term intubation and high rate of tracheostomy in COVID-19 patients might determine an unprecedented increase of airway stenoses: a call to action from the European Laryngological Society.
      • Mattioli F
      • Fermi M
      • Ghirelli M
      • et al.
      Tracheostomy in the COVID-19 pandemic.
      • McGrath BA
      • Brenner MJ
      • Warrillow SJ
      • et al.
      Tracheostomy in the COVID-19 era: global and multidisciplinary guidance.
      As a result, increased durations of intubation were observed.
      • Kwak PE
      • Connors JR
      • Benedict PA
      • et al.
      Early outcomes from early tracheostomy for patients with COVID-19.
      For example, during the first month of the pandemic, Hur et al report that 64% of patients in acute care were intubated for more than 14 days.
      • Hur K
      • Price CP
      • Gray EL
      • et al.
      Factors associated with intubation and prolonged intubation in hospitalized patients with COVID-19.
      Before the SARS-CoV-2 outbreak, a relationship between prolonged intubation and dysphagia had been found in critically-ill patients requiring mechanical ventilation
      • Macht M
      • King CJ
      • Wimbish T
      • et al.
      Post-extubation dysphagia is associated with longer hospitalization in survivors of critical illness with neurologic impairment.
      as well as those with acute respiratory distress syndrome.
      • Frajkova Z
      • Tedla M
      • Tedlova E
      • Suchankova M
      • Geneid A.
      Postintubation dysphagia during COVID-19 outbreak-contemporary review.
      Dysphagia was present in greater than 50% of patients who were intubated longer than 48 hours.
      • Skoretz SA
      • Flowers HL
      • Martino R.
      The incidence of dysphagia following endotracheal intubation: a systematic review.
      Moderate to severe dysphagia was seen in patients who were intubated for longer than 7 days.
      • Brodsky MB
      • Huang M
      • Shanholtz C
      • et al.
      Recovery from dysphagia symptoms after oral endotracheal intubation in acute respiratory distress syndrome survivors. A 5-year longitudinal study.
      Prolonged intubation may lead to reduced laryngeal sensation, which can result in silent aspiration.
      • Borders JC
      • Fink D
      • Levitt JE
      • et al.
      Relationship between laryngeal sensation, length of intubation, and aspiration in patients with acute respiratory failure.
      Although previous literature establishes a relationship between intubation and dysphagia, it is not clear how the swallowing mechanisms and physiology are affected by SARS-CoV-2. Given the limited information to date on dysphagia during inpatient rehabilitation in patients after COVID-19, our aims were: (1) to describe clinical and VFSS characteristics at admission to inpatient rehabilitation and (2) to explore the relationships between clinical swallow evaluation results, VFSS results, and prior intubation in patients admitted to an inpatient rehabilitation hospital after acute hospitalization for SARS-CoV-2.

      Methods

      This retrospective study was conducted at a large urban acute rehabilitation hospital. Our institutional review board approved extraction of patient data from the electronic health record and granted a waiver of informed consent for use of deidentified, historical data. Objective measures were used to classify patient performance to avoid recall bias. We reviewed the electronic medical records of the first 40 patients with prior SARS-CoV-2 diagnoses who were referred for a VFSS between the months of April and August 2020. Referrals for VFSS were determined by the evaluating speech-language pathologist (SLP) after completion of a comprehensive speech, language, and swallowing evaluation that included a clinical swallow examination with administration of the Mann Assessment of Swallowing Ability (MASA)
      • Mann G.
      MASA: the Mann assessment of swallowing ability.
      and the Functional Oral Intake Scale (FOIS).
      • Crary MA
      • Mann GD
      • Groher ME.
      Initial psychometric assessment of a functional oral intake scale for dysphagia in stroke patients.
      Demographic characteristics were extracted from the electronic medical record, including current medical comorbidities. Comorbidities were extracted based on admitting physicians International Classification of Diseases, 10th revision, codes.

      World Health Organization. International statistical classification of diseases and related health problems, tenth revision. Geneva: World Health Organization; 2004.

      The first 40 patients who were referred for a VFSS were considered to be a representative sample of the 121 patients admitted to inpatient rehabilitation with COVID-19 acute respiratory disease, pneumonia owing to SARS-associated coronavirus and/or pneumonia owing to SARS-associated coronavirus diagnosis. An independent reviewer completed a reliability check on data extracted from 20% of the patients included in the sample determining reliability to be 97% with the electronic health record.

      Measures

      MASA

      The MASA
      • Mann G.
      MASA: the Mann assessment of swallowing ability.
      was administered at admission and discharge as a part of the standardized clinical swallow examination.
      • Garand KL
      • McCullough G
      • Crary M
      • Arvedson JC
      • Dodrill P.
      Assessment across the life span: the clinical swallow evaluation.
      The MASA standardizes administration and scoring components of the clinical swallowing evaluation to determine the presence of dysphagia and severity of impairments. The MASA was initially validated in patients after acute stroke.
      • Mann G.
      MASA: the Mann assessment of swallowing ability.
      It provides a score that ranges from 0 to 200, with a stroke-based risk cutoff score of 170 or greater indicating no abnormality.
      • Antonios N
      • Carnaby-Mann G
      • Crary M
      • et al.
      Analysis of a physician tool for evaluating dysphagia on an inpatient stroke unit: the modified Mann assessment of swallowing ability.
      Furthermore, likelihood ratios were used to create 4 categories to define the risk for aspiration as follows: unlikely (≥170), possible (149-169), probable (141-148), and definite (≤140).
      • Kwon S
      • Sim J
      • Park J
      • et al.
      Assessment of aspiration risk using the Mann assessment of swallowing ability in brain-injured patients with cognitive impairment.
      Although not validated with the post-COVID population, research has shown application of the MASA with populations other than stroke
      • Ohira M
      • Ishida R
      • Maki Y
      • et al.
      Evaluation of a dysphagia screening system based on the Mann Assessment of Swallowing Ability for use in dependent older adults.
      ,
      • Su CL
      • Chen SL
      • Tsai SW
      • et al.
      Efficacy of predicting videofluoroscopic results in dysphagic patients with severe cerebral palsy using the Mann Assessment of Swallowing Ability.
      and thus it is administered as a part of the hospital's usual care to standardize the clinical swallow evaluation.

      FOIS

      The FOIS
      • Crary MA
      • Mann GD
      • Groher ME.
      Initial psychometric assessment of a functional oral intake scale for dysphagia in stroke patients.
      was rated at admission and discharge by the treating SLP. The FOIS is a 7-point scale that documents the effect of dysphagia on oral intake of food and liquid, and includes both feeding tube dependence and consistency modifications. The FOIS has adequate reliability, validity, and sensitivity to change in functional oral intake over the course of rehabilitation.
      • Crary MA
      • Mann GD
      • Groher ME.
      Initial psychometric assessment of a functional oral intake scale for dysphagia in stroke patients.

      International Dysphagia Diet Standardization Initiative

      The International Dysphagia Diet Standardization Initiative (IDDSI) framework consists of 8 food and liquid consistencies on a scale from 0 to 7.
      • Cichero JA
      • Steele C
      • Duivestein J
      • et al.
      The need for international terminology and definitions for texture-modified foods and thickened liquids used in dysphagia management: foundations of a global initiative.
      Each patient's admission and discharge IDDSI diet as well as recommended IDDSI diet after VFSS were extracted from the electronic health record.

      VFSS and penetration aspiration scale

      A VFSS was completed on each of the patients. If a patient had more than 1 VFSS for reassessment purposes during the study period, only the first was included in this study. A VFSS evaluates the “functional anatomy and physiology of the swallowing mechanism, swallowing efficiency, and airway protection.”
      • Martin-Harris B
      • Brodsky MB
      • Michel Y
      • Ford CL
      • Walters B
      • Heffnre J.
      Breathing and swallowing dynamics across the adult lifespan.
      The SLP who completed the VFSS determined the presence or absence of aspiration using the penetration aspiration scale (PAS),
      • Rosenbek JC
      • Robbins JA
      • Roecker EB
      • Coyle JL
      • Wood JL.
      A penetration-aspiration scale.
      identified the need for compensatory strategies and provided diet recommendations. The PAS is an 8-point scale that rates the degree of airway invasion. Scores of 3 or greater indicate airway invasion, whereas a score of 6 or greater indicates aspiration. For this study, we extracted the highest (worst) PAS score, the IDDSI food or liquids bolus consistency on which it occurred, and the size of the bolus. This extracted score reflects the nature of the presenting dysphagia and is a common method for summarizing PAS scores.
      • Borders JC
      • Brates D.
      Use of the penetration-aspiration scale in dysphagia research: a systematic review.

      Statistical analysis

      Descriptive statistics were used to characterize patient demographic information and comorbidities, MASA and FOIS scores, and results of the VFSS. Correlation coefficients were used to determine the relationship between the MASA total numerical score (TNS) and the PAS determined from the VFSS. We used a logistic regression with a single continuous predictor (number of days of intubation) to estimate the odds of patients having a penetration aspiration score of 3 or greater (indicating airway invasion), compared with having a penetration aspiration score of less than 3. The presence of stroke and the presence of having a tracheostomy were assessed as independent predictors for PAS because strokes and tracheostomies may be associated with PAS impairments to a greater extent than intubation alone. Analyses were performed using SAS version 9.4.
      • Frajkova Z
      • Tedla M
      • Tedlova E
      • Suchankova M
      • Geneid A.
      Postintubation dysphagia during COVID-19 outbreak-contemporary review.
      ,a

      Results

      Patient characteristics

      A total of 40 patients with confirmed diagnosis of SARS-COV-2 at the time of inpatient rehabilitation were included in data collection (age range, 32-86y; mean age, 65.9±13y; 29 identified as men, 11 identified as women). Most (43%) individuals had at least 1 acute comorbidity, the most common of which were hematologic and neurologic (table 1). Five patients experienced an acute stroke. During the acute care stay, 34 of the 40 patients (85%) underwent endotracheal intubation (duration of intubation, 5-68d; median, 15d). Of these 34 patients, 10 (29%) had repeated intubation. Three of the 40 patients had an unknown history of intubation during their acute hospitalization for SARS-CoV-2 and 3 were not intubated. Seven patients from the entire sample (17%) had tracheostomies during the acute care stay.
      Table 1Patient characteristics (N=40)
      Respiratory Informationn (%)
      Days with endotracheal intubation (mean ± SD)17±14
      Tracheostomy placed7 (18)
      Acute medical complexities
      Type of medical complication
      Hematologic14 (35)
      Neurologic12 (30)
      Cardiac9 (23)
      Genitourinary and Hepatology8 (20)
      Infectious Disease7 (18)
      Medical complexities
      09 (23)
      117 (43)
      26 (15)
      37 (18)

      Initial evaluation data

      At the time of initial evaluation during inpatient rehabilitation, 37 patients (93%) had a FOIS score of 6 or less, indicating restriction of oral intake (table 2). Of the 40 patients, 3 (8%) were achieving nutrition by mouth with no modifications; 62% of patients achieved all nutrition by mouth but with modification to consistencies, 10% achieved some oral intake but required supplementation by gastrostomy tube, and 20% could consume nothing by mouth and were dependent on a gastrostomy tube for nutrition and hydration (table 3). Additionally, 18 (45%) achieved a likelihood of aspiration ratio (LAR) of unlikely (170-200) on the MASA. In our sample, only 20% of patients had been evaluated previously by videofluoroscopy in acute care. FEES was not conducted at the previous level of care for any of the patients in our sample.
      Table 2Dysphagia characteristics during inpatient rehabilitation (N=40)
      Measures at Initial Evaluationn (%)
      MASA score on admission ≤170 (indicates potential aspiration risk)22 (55)
      FOIS score ≤6 upon admission (indicating modified diet)37 (93)
      PAS Scores on VFSS
      Degree of aspiration
      PAS score of 3 or 5 (penetration without ejection)8 (20)
      PAS score of ≥6 (aspiration)12 (30)
      PAS score of 8 (silent aspiration)11 (28)
      PAS score achieved with IDDSI consistency or volume
      PAS score of ≥3 on IDDSI liquids levels—thin, mildly thick, moderately thick22 (55)
      PAS score of ≥3 occurring on bolus of SS or STRS12 (30)
      PAS score of ≥3 occurring on bolus smaller than NS13 (32.5)
      Recommendations following VFSS information
      Upgraded to 0 from modified liquids or NPO20 (67)
      Upgraded or remained on 0 with swallow guidelines11 of 28 (39)
      Downgraded diet or remained ordered liquid modification or NPO5 (13)
      Upgraded to 7.0 - including with compensatory strategy use19 of 37 (51.4)
      Discharge diet and measures
      P upgraded to 7.0 at discharge from modified diet25 of 37 (68)
      MASA scores upon discharge ≤170 (indicating potential aspiration risk)2 (6)
      FOIS score ≤6 upon discharge (indicating modified diet)9 of 37 (22)
      NOTES. Number is out of 40 patients unless indicated otherwise. MASA score ≤170 indicates potential aspiration risk, FOIS score ≤6 indicates diet modification, and PAS ≥6 indicates aspiration and PAS ≥3 indicates airway invasion.
      Abbreviations: NPO, nothing by mouth; NS, natural sip; SS, serial swallows; STRS, straw sip.
      Table 3VFSS information
      PreadmissionAdmissionVFSSDiet Recommendation After VFSS
      Patient No.VFSS at OSHNo. of Days IntubatedIDDSIMASAFOISPASIDDSI LevelBolus SizeIDDSI Level Recommendation
      1No27NPO1551303 mLNPO
      2U866.0186550SS, STRSUpgrade to 7, remain *0
      3Yes10NPO1561803 mLUpgrade to 4, 3
      4NoU7, 2170610AllUpgrade to 7.0
      5No76.2163510.4, 7Allupgrade to 7, 0
      6No306.01865803 mLUpgrade to 7, remain 0
      7U116.0167520All 0Upgrade to 7, remain 0
      8No24NPO165180SSUpgrade to level 7, *0
      9NoU5.2182550NS, SSRemain on 5.2
      10No74.3136450.2, 35 mL, SSTrial 5.3
      11No164.4168460NSUpgrade to 6.0
      12No245.0175380SSUpgrade to 7, remain on 0
      13Yes117.0167720All 0Remain on 7.0
      14NoN/A4.3157310.4All trials Trials of 0Trial of 5.0
      15Yes156.3184580NS, SSUpgrade to 7,*0
      16No21NPO162110.4, 7AllUpgrade to level 5.0
      17No244.2157480.2NS 2Downgrade to level 3, Upgrade to level 5
      18No9NPO167120SSUpgrade to 7, remain *0
      19No25NPO1601503 mL, 5 mLUpgrade to level 7, 2
      20Yes224.21834305 mL, 10 mL, NS, SSUpgrade to 7,*0
      21UU4.0180420All 0Upgrade to level 5, remain 0
      22No96.2165580SSUpgrade to level 7,*0
      23No23NPO167130NSUpgrade to 4.2
      24U164.21764805 mL, 10 mL, NSUpgrade to 6, remain on 2
      25No107.0192710AllRemain on 7.0
      26No135.2165510.4, 7AllUpgrade to level 7.0
      27Yes257.2181620SSUpgrade to level 7, 0
      28No145.21813305 mL, 10 mL, NS, SSUpgrade to *6.0
      29Yes214.2164410.4, 7AllUpgrade 6.0
      30UN/A4.2167410NSUpgrade to *7.0
      31U155.2162580NSRemain on 5, 2
      32Yes197.3171620NS, SSUpgrade to 7.0
      33U284.0196480SSUpgrade to 7,*0
      34No56.2181510.4, 7AllUpgrade to 7.0
      35Yes136.3171580SSUpgrade to *7.0
      36No65.0156310.4, 7AllUpgrade to 6, Remain 0
      37No167.2181610.4, 7AllUpgrade to 7.0
      38No107.0154750STRSRemain on 7,*0
      39No05.3124520NS, SSUpgrade to 5.0
      40No14NPO1731503ML, 5MLUpgrade to level 7.2
      NOTES. MASA score ≤170 indicates potential aspiration risk.
      FOIS score ≤6 indicates diet modification. Level 1: nothing by mouth. Level 2: tube dependent with minimal attempts of food or liquid. Level 3: tube dependent with consistent oral intake of food or liquid. Level 4: total oral diet of a single consistency. Level 5: total oral diet with multiple consistencies, but requiring special preparation or compensations. Level 6: total oral diet with multiple consistencies without special preparation, but with specific food limitations. Level 7: total oral diet with no restrictions.
      IDDSI: Level 7: regular diet. Level 6: soft and bite-size. Level 5: moist and minced. Level 4: puree, liquids–extremely thick liquids. Level 3: moderately thick liquids. Level 2: mildly thick liquids. Level 0: thin liquids.
      PAS: 1 indicates no penetration or aspiration; 2 indicates penetration, contrast remains above the vocal folds and subsequently ejected; 3 indicates penetration, contrast remains above the vocal fold and not ejected; 4 indicates penetration, contrast contacts vocal folds and subsequently ejected; 5 indicates penetration, contrast contacts vocal folds and not ejected; 6 indicates aspiration, contrast below vocal folds and subsequently ejected; 7 indicates aspiration not ejected despite effort; and 8 indicates aspiration, no effort made to eject.
      Abbreviations: OSH, outside hospital; N/A, not available; NPO, nothing by mouth; NS, natural sip; SS, serial swallows; STRS, straw sip U, unknown.

      Data from VFSS

      After their VFSS during inpatient rehabilitation, 30% (12 of 40) of patients demonstrated a PAS score of 6 or greater, indicating aspiration on a least 1 trial during VFSS. An additional 25% (10 patients) demonstrated penetration without ejection on VFSS. Nineteen individuals (51%) were upgraded to IDDSI level 7 regular diet with level 0 thin liquids and achieved a FOIS of 7, indicating that no food or liquid modifications were needed for safe intake. Of the 30 patients admitted on modified liquids or who were allowed nothing by mouth, 20 (67%) were upgraded to level 0, thin liquids, with 11 patients being restricted from straws and consecutive swallows to achieve safety with upgrade to level 0 liquids. After the VFSS, 5 individuals (13%) received a downgrade of liquids or remained on the same modified liquid recommendations from their admission to inpatient rehabilitation.

      Relationship between clinical swallow examination and VFSS

      We compared the MASA score from the clinical swallowing evaluation with results obtained during the VFSS. We calculated the TNS and LAR achieved on the MASA. A TNS of less than 170 predicted the presence of aspiration with 27% (6/22) accuracy; 72% of the patients (16/22) had a TNS less than 170 but did not demonstrate any instances of aspiration. Fifty percent of patients who aspirated (6 of 12) achieved an LAR of “unlikely to aspirate” on the MASA; 7% (2 of 27) achieved a “definite” LAR but did not aspirate.

      Relationship between intubation and dysphagia

      Results of the logistic regression indicated that for each additional day of intubation, the odds of patients having a PAS of 3 or greater increased by approximately 15% (odds ratio, 1.15; 95% confidence interval, 1.03-1.27; P=.013). Thus, with each additional day of intubation, there was a 15% greater likelihood of having airway invasion. Stroke and tracheostomy placement were not significant predictors of PAS alone or in combination with days intubated.

      Discussion

      Our study shows that instrumental swallow evaluation provides important information for the diagnosis and treatment of dysphagia in patients who have had SARS-CoV-2 and are admitted to inpatient rehabilitation. The retrospective analysis also demonstrates a high correlation between acute care intubation and ongoing dysphagia during inpatient rehabilitation for patients with SARS-CoV-2 diagnoses. Specifically, the likelihood of airway invasion, as identified on videofluoroscopy, increases with each day of intubation and persists into the subacute rehabilitation period of recovery. This finding is consistent with prior evidence that prolonged intubation decreased laryngeal sensation and puts patients at risk for silent aspiration or airway invasion.
      • Brodsky MB
      • Huang M
      • Shanholtz C
      • et al.
      Recovery from dysphagia symptoms after oral endotracheal intubation in acute respiratory distress syndrome survivors. A 5-year longitudinal study.
      ,
      • Borders JC
      • Fink D
      • Levitt JE
      • et al.
      Relationship between laryngeal sensation, length of intubation, and aspiration in patients with acute respiratory failure.
      In addition to increased duration of intubation, other underlying factors likely affected dysphagia. Many of the patients in this sample experienced multiple acute comorbidities. Critical illness contributes to deconditioning and debility, impaired cognition, neuromyopathy, and decreased coordination of swallow and breathing.
      • Macht M
      • King CJ
      • Wimbish T
      • et al.
      Post-extubation dysphagia is associated with longer hospitalization in survivors of critical illness with neurologic impairment.
      ,
      • Brodsky MB
      • Huang M
      • Shanholtz C
      • et al.
      Recovery from dysphagia symptoms after oral endotracheal intubation in acute respiratory distress syndrome survivors. A 5-year longitudinal study.
      ,
      • Borders JC
      • Fink D
      • Levitt JE
      • et al.
      Relationship between laryngeal sensation, length of intubation, and aspiration in patients with acute respiratory failure.
      The presence of airway invasion and silent aspiration in our sample may indicate a common pathophysiology of dysphagia in patients after SARS-CoV-2 intubation. The incidence of aspiration after an acute stroke varies, but can be as high as 33%.
      • Hammond CAS
      • Goldstein LB.
      Cough and aspiration of food and liquids due to oral-pharyngeal dysphagia: ACCP evidence-based clinical practice guidelines.
      A high number of patients in this study experienced a neurologic comorbidity, yet our analysis found that the presence of stroke was a noncontributing factor for airway invasion in this population. Furthermore, previous literature supports a high incidence rate of aspiration in patients with tracheostomies, citing rates as high as 30% to 50%.
      • Elpern EH
      • Scott MG
      • Petro L
      • Ries MH.
      Pulmonary aspiration in mechanically ventilated patients with tracheostomies.
      ,
      • Leder SB
      • Espinosa JF.
      Aspiration risk after acute stroke: comparison of clinical examination and fiberoptic endoscopic evaluation of swallowing.
      Again, our analysis found that the presence of a tracheostomy alone was a noncontributing factor for airway invasion in this population.
      Silent aspiration occurred in 27% of the patients sampled. An instrumental swallow study would be imperative for identification and intervention. VFSS was important for identifying strategies that were appropriate for helping patients return to intake of unmodified liquids. Although 11 patients were able to upgrade or remain on level 0 thin liquids, they required modifications for safe liquid intake, including taking single cup sips, restriction from using straws, and drinking a small volume, which could only have been determined with the completion of the VFSS.
      Furthermore, our analysis underscores the need for conducting instrumental swallowing evaluations in this patient population. In our sample, MASA TNS and LAR were poor predictors of aspiration; 56% of patients achieved a TNS of less than 170 but did not aspirate, and 50% of patients who aspirated achieved a LAR of “unlikely” on the MASA. Only 20% of patients in our sample had a VFSS conducted during their acute care hospitalization, yet 93% were receiving modified diets as rated on the FOIS, indicating conservative management in acute care. This management trend may reflect early decision-making during the pandemic to hold or defer VFSS and FEES given infection prevention concerns with aerosol generating procedures.
      Collaboration with the hospital infection preventionist allowed early implementation of measures to allow completion of VFSS with the SARS-CoV-2 population at our rehabilitation hospital. Our guidelines limited exposure during patient transport, reduced the number of personnel during the examination, and placed a time restriction on room use after the completion of the aerosol generating procedure. Later in the pandemic, guidelines such as these were suggested for the medical community.
      • Fritz MA
      • Howell RJ
      • Brodsky MB
      • et al.
      Moving forward with dysphagia care: implementing strategies during the COVID-19 pandemic and beyond.
      Our study supports recent efforts of many hospital systems to revisit their protocols for instrumental dysphagia evaluations with COVID-positive patients.
      • Bolton L
      • Mills C
      • Wallace S
      • Brady MC
      Royal College of Speech and Language Therapists (RCSLT) COVID-19 Advisory Group. Aerosol generating procedures, dysphagia assessment and COVID-19: a rapid review.

      Study limitations

      There are several limitations related to the retrospective nature of this study. Compared with prospective dysphagia research, we report fewer objective measures of swallowing physiology, because the VFSS were documented using standard clinical rather than research practices. The timing of the completion of the VFSS was not extracted as part of this data analysis. One limitation of using FOIS is that it can be influenced by nondysphagia-related factors such as poor dentition or consistency preference, which we did not track owing to their low frequency of occurrence in this sample. Our patient sample was taken early in the pandemic and may not represent current patients discharged from acute care given evolving practices in acute care management.

      Conclusion

      Instrumental swallow evaluations are imperative to diagnose and treat dysphagia in the post-COVID population. Because of the heterogeneity of this population, the potential for multiple medical comorbidities, and the lack of sensitive screening tools, instrumental assessments need to be performed on a more consistent basis. Infection prevention protocols need to evolve to prioritize the completion of instrumental swallow studies such as videofluoroscopy for this patient population. This population, which has a high incidence of prolonged intubation, is at greater risk for aspiration, and clinical swallow evaluations are limited in their sensitivity in identifying aspiration. Further research is warranted to specify the pathophysiology of dysphagia in this population through more precise measurement.

      Supplier

      a. SAS, version 9.4; SAS Institute.

      References

        • Frajkova Z
        • Tedla M
        • Tedlova E
        • Suchankova M
        • Geneid A.
        Postintubation dysphagia during COVID-19 outbreak-contemporary review.
        Dysphagia. 2020; 35: 549-557
        • Bolton L
        • Mills C
        • Wallace S
        • Brady MC
        Royal College of Speech and Language Therapists (RCSLT) COVID-19 Advisory Group. Aerosol generating procedures, dysphagia assessment and COVID-19: a rapid review.
        Int J Lang Commun Disord. 2020; 55: 629-636
        • Brodsky MB
        • Gilbert RJ.
        The long-term effects of COVID-19 on dysphagia evaluation and treatment.
        Arch Phys Med Rehabil. 2020; 101: 1662-1664
        • Mattei A
        • de la Bretèque BA
        • Crevier-Buchman L
        • et al.
        Guidelines of clinical practice for the management of swallowing disorders and recent dysphonia in the context of the COVID-19 pandemic.
        Eur Ann Otorhinolaryngol Head Neck Dis. 2020; 137: 173-175
        • Miles A
        • Connor NP
        • Desai RV
        • et al.
        Dysphagia care across the continuum: a multidisciplinary Dysphagia Research Society Taskforce report of service-delivery during the COVID-19 global pandemic.
        Dysphagia. 2021; 36: 170-182
        • Martin-Harris B
        • Canon CL
        • Bonilha HS
        • Murray J
        • Davidson K
        • Lefton-Greif MA.
        Best practices in modified barium swallow studies.
        Am J Speech Lang Pathol. 2020; 29: 1078-1093
        • Namasivayam-MacDonald AM
        • Riquelme LF.
        Speech-language pathology management for adults with COVID-19 in the acute hospital setting: initial recommendations to guide clinical practice.
        Am J Speech Lang Pathol. 2020; 29: 1850-1865
        • Piazza C
        • Filauro M
        • Dikkers FG
        • et al.
        Long-term intubation and high rate of tracheostomy in COVID-19 patients might determine an unprecedented increase of airway stenoses: a call to action from the European Laryngological Society.
        Eur Arch Otorhinolaryngol. 2021; 278: 1-7
        • Mattioli F
        • Fermi M
        • Ghirelli M
        • et al.
        Tracheostomy in the COVID-19 pandemic.
        Eur Arch Otorhinolaryngol. 2020; 277: 2133-2135
        • McGrath BA
        • Brenner MJ
        • Warrillow SJ
        • et al.
        Tracheostomy in the COVID-19 era: global and multidisciplinary guidance.
        Lancet Respir Med. 2020; 8: 717-725
        • Kwak PE
        • Connors JR
        • Benedict PA
        • et al.
        Early outcomes from early tracheostomy for patients with COVID-19.
        JAMA Otolaryngol Head Neck Surg. 2021; 147: 239-244
        • Hur K
        • Price CP
        • Gray EL
        • et al.
        Factors associated with intubation and prolonged intubation in hospitalized patients with COVID-19.
        Otolaryngol Head Neck Surg. 2020; 163: 170-178
        • Macht M
        • King CJ
        • Wimbish T
        • et al.
        Post-extubation dysphagia is associated with longer hospitalization in survivors of critical illness with neurologic impairment.
        Crit Care. 2013; 17: R119
        • Skoretz SA
        • Flowers HL
        • Martino R.
        The incidence of dysphagia following endotracheal intubation: a systematic review.
        Chest. 2010; 137: 665-673
        • Brodsky MB
        • Huang M
        • Shanholtz C
        • et al.
        Recovery from dysphagia symptoms after oral endotracheal intubation in acute respiratory distress syndrome survivors. A 5-year longitudinal study.
        Ann Am Thorac Soc. 2017; 14: 376-383
        • Borders JC
        • Fink D
        • Levitt JE
        • et al.
        Relationship between laryngeal sensation, length of intubation, and aspiration in patients with acute respiratory failure.
        Dysphagia. 2019; 34: 521-528
        • Mann G.
        MASA: the Mann assessment of swallowing ability.
        Singular/Thomson Learning, Clifton Park, NY2002
        • Crary MA
        • Mann GD
        • Groher ME.
        Initial psychometric assessment of a functional oral intake scale for dysphagia in stroke patients.
        Arch Phys Med Rehabil. 2005; 86: 1516-1520
      1. World Health Organization. International statistical classification of diseases and related health problems, tenth revision. Geneva: World Health Organization; 2004.

        • Garand KL
        • McCullough G
        • Crary M
        • Arvedson JC
        • Dodrill P.
        Assessment across the life span: the clinical swallow evaluation.
        Am J Speech Lang Pathol. 2020; 29: 919-933
        • Antonios N
        • Carnaby-Mann G
        • Crary M
        • et al.
        Analysis of a physician tool for evaluating dysphagia on an inpatient stroke unit: the modified Mann assessment of swallowing ability.
        J Stroke Cerebrovasc Dis. 2010; 19: 49-57
        • Kwon S
        • Sim J
        • Park J
        • et al.
        Assessment of aspiration risk using the Mann assessment of swallowing ability in brain-injured patients with cognitive impairment.
        Front Neurol. 2019; 10: 1264
        • Ohira M
        • Ishida R
        • Maki Y
        • et al.
        Evaluation of a dysphagia screening system based on the Mann Assessment of Swallowing Ability for use in dependent older adults.
        Geriatr Gerontol Int. 2017; 17: 561-567
        • Su CL
        • Chen SL
        • Tsai SW
        • et al.
        Efficacy of predicting videofluoroscopic results in dysphagic patients with severe cerebral palsy using the Mann Assessment of Swallowing Ability.
        Am J Phys Med Rehabil. 2016; 95: 270-276
        • Cichero JA
        • Steele C
        • Duivestein J
        • et al.
        The need for international terminology and definitions for texture-modified foods and thickened liquids used in dysphagia management: foundations of a global initiative.
        Curr Phys Med Rehabil Rep. 2013; 1: 280-291
        • Martin-Harris B
        • Brodsky MB
        • Michel Y
        • Ford CL
        • Walters B
        • Heffnre J.
        Breathing and swallowing dynamics across the adult lifespan.
        Arch Otolaryngol Head Neck Surg. 2005; 131: 762-770
        • Rosenbek JC
        • Robbins JA
        • Roecker EB
        • Coyle JL
        • Wood JL.
        A penetration-aspiration scale.
        Dysphagia. 1996; 11: 93-98
        • Borders JC
        • Brates D.
        Use of the penetration-aspiration scale in dysphagia research: a systematic review.
        Dysphagia. 2020; 35: 583-597
        • Hammond CAS
        • Goldstein LB.
        Cough and aspiration of food and liquids due to oral-pharyngeal dysphagia: ACCP evidence-based clinical practice guidelines.
        Chest. 2006; 129: 154S-168S
        • Elpern EH
        • Scott MG
        • Petro L
        • Ries MH.
        Pulmonary aspiration in mechanically ventilated patients with tracheostomies.
        Chest. 1994; 105: 563-566
        • Leder SB
        • Espinosa JF.
        Aspiration risk after acute stroke: comparison of clinical examination and fiberoptic endoscopic evaluation of swallowing.
        Dysphagia. 2002; 17: 214-218
        • Fritz MA
        • Howell RJ
        • Brodsky MB
        • et al.
        Moving forward with dysphagia care: implementing strategies during the COVID-19 pandemic and beyond.
        Dysphagia. 2021; 36: 161-169