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Efficacy of Early Inpatient Rehabilitation of Post-COVID-19 Survivors

Efficacy of Early Inpatient Rehabilitation of Post-COVID-19 Survivors ORIGINAL RESEARCH ARTICLE Efficacy of Early Inpatient Rehabilitation of Post-COVID-19 Survivors Single-Center Retrospective Analysis Ning Cao, MD, Jaclyn Barcikowski, DO, Franklin Womble, MD, Bianca Martinez, MD, Yevgeniya Sergeyenko, MD, Jacob H. Koffer, MD, Michael Kwasniewski, MD, Thomas Watanabe, MD, Rui Xiao, PhD, and Alberto Esquenazi, MD n late 2019, a highly pathogenic novel coronavirus Objective: The aim of this study was to understand the demographic, I (COVID-19) causing severe acute respiratory syndrome clinical characteristics, and effectiveness of early inpatient rehabilita- (SARS)-CoV-2 emerged in Wuhan, China, and soon spread tion of post-COVID survivors. 1,2 throughout the world, causing a global pandemic. Many pa- Design: A single-center retrospective chart review analysis of 100 pa- tients with COVID-19 infection required prolonged hospitalization, tients admitted to a newly created acute COVID rehabilitation unit assisted ventilation, and critical care management. As a result, (CORE+) from April to December 2020 was conducted. many COVID-19 survivors developed deconditioning; physical, Results: The demographic and clinical characteristics and complica- cognitive, and psychologic sequelae; and persistent respiratory tions of 100 post-COVID patients were reviewed. Functional out- 3–5 problems, as well as other complications that are even now not comes of GG Self-care and Mobility Activities Items (Section fully appreciated. Data from countries initially affected by the pan- GG0130 and GG0170) of the Centers for Medicare & Medicaid Ser- demic demonstrated that the rapid spread of the infection quickly vices of the Inpatient Rehabilitation Facility Patient Assessment In- 6,7 overloaded their national health systems. strument (Version 3.0) at admission and discharge, prevalence of oxy- Historical data from Medicare suggest that more than gen requirement, the need for cognitive and neuropsychology support 30% of patients hospitalized with sepsis, a condition with inpa- by discharge, and dispositions after completion of inpatient rehabilita- tient mortality like that associated with COVID-19, require tion facility stay were analyzed. The functional outcomes of 59 pri- facility-based care. Post acute care often serves as a “pop-off mary pulmonary manifestations of COVID patients were further ana- valve” for hospital capacity, in that transferring patients to a such lyzed based on the presence of intensive care unit stay before transfer a setting once they recover from the most acute phase of their ill- to the COVID rehabilitation unit. Most patients demonstrated signifi- ness could free up acute care hospital beds. Because of the cant functional gains after completion of inpatient rehabilitation facil- COVID-19 patient surge, along with reallocation of post– ity stay; however, a considerable number of patients continued to re- acute care facilities as acute care spaces and workforce deple- quire cognitive support by discharge. tion, post acute care became strained, as was first seen in the Conclusion: The data suggested the benefit of early rehabilitation for major cities of Boston and New York City. hospitalized post-COVID patients. Services need to be geared to in- At the authors’ institution, a specialized acute inpatient re- clude patients’ cognitive deficits. habilitation unit to address the functional and medical needs of Key Words: Inpatient Rehabilitation, Functional Outcomes, post-COVID patients early after the critical acute care phase Post-COVID, Post-ICU Syndrome was created, as well as for those patients in need of inpatient re- habilitation for another reason but who became actively in- (Am J Phys Med Rehabil 2023;102:498–503) fected. The development of a dedicated “center of excellence” specializing in and assuming the care of patients recovering from COVID-19 was developed through what was termed the CORE+ unit (COVID rehabilitation unit). Patients would un- dergo a comprehensive rehabilitation program with a multidis- From the MossRehab, Elkins Park, Pennsylvania (NC, JB, FW, BM, YS, JHK, MK, ciplinary team with staff provided appropriate safety equip- TW, AE); Temple University Hospital, Philadelphia, Pennsylvania (FW, BM, ment, training, and adequate personal protective equipment to JHK); and Biostatistics and Epidemiology at the Hospital of the University of provide this care safely. The unit opened in April 2020 and Pennsylvania, Philadelphia, Pennsylvania (RX). All correspondence should be addressed to: Ning Cao, MD, MossRehab, 60 closed on July 1, 2021. The alpha and delta variants of Township Line Road, Elkins Park, PA 19027. COVID-19 were the dominant strains during this time period. Ning Cao current affiliation: Physical Medicine and Rehabilitation Department, Johns Hopkins University School of Medicine, 600 N. Wolfe St., Baltimore, MD 21287. This study reports on the demographics, clinical character- Franklin Womble, Bianca Martinez, and Jacob H. Koffer are in training. istics, and functional outcomes, including cognitive/psychologic Financial disclosure statements have been obtained, and no conflicts of interest have been and ultimate discharge destination, of the patients treated in the reported by the authors or by any individuals in control of the content of this article. Copyright © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. This is CORE+ unit from April 2020 to December 2020 (before vac- an open-access article distributed under the terms of the Creative Commons cines were available). The purpose of this retrospective re- Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC-ND), view has many folds. The comorbidities and clinical charac- where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in any way or used commercially without teristics of the hospitalized COVID patients were analyzed permission from the journal. to assess any underlying factors contributing to the patients ISSN: 0894-9115 DOI: 10.1097/PHM.0000000000002122 who might have a risk of developing primary respiratory 498 www.ajpmr.com American Journal of Physical Medicine & Rehabilitation � Volume 102, Number 6, June 2023 Volume 102, Number 6, June 2023 Efficacy of Early Rehab of Post-COVID Patients symptoms as opposed to those in the cohort with minimal re- Outcomes spiratory symptoms after COVID infection. Furthermore, The electronic medical records of patients admitted to the physical and cognitive aspects of outcomes were analyzed the CORE+ unit during April to December 2020 were re- in the primary COVID-19 patients who received ventilator vs. viewed. Patients’ demographics (age, sex, and body mass in- no ventilator treatment to evaluate how patients with different dex), comorbidities, length of hospital stay (including inten- severities of respiratory disease responded to interdisciplinary sive care unit [ICU]) before transfer to rehabilitation, length treatment in the CORE+ unit. of rehabilitation stay, and data regarding newly developed The results are intended to provide insights on the effective- thromboembolic complications were collected. ness of early interdisciplinary rehabilitation for post-COVID In addition, the functional outcomes assessed at admission survivors, particularly given that the potential risk factors and re- and discharge were composed of GG Self-care and Mobility habilitation needs of patients with severe COVID disease and Activities Items (Section GG0130 and GG0170) of the Centers their trajectory of recovery were not known. for Medicare & Medicaid Services–issued Inpatient Rehabilita- tion Facility Patient Assessment Instrument Version 3.0; speech/ cognitive therapy need as assessed by speech and occupational therapists using various tools including the Orientation log METHODS (O-Log), Montreal Cognitive Assessment, Saint Louis University Mental Status, and Cognitive Linguistic Quick Test based on pa- Statistical Analysis tients’ clinical characteristics; supplemental oxygen requirement; The demographic and clinical characteristics of the pa- the need for neuropsychology support; and disposition to home/ tients were summarized by standard descriptive statistics, acute care/skilled nursing facility setting after completion of IRF. that is, mean and standard deviation (SD) or median and in- terquartile range (IQR) for continuous variables as appropri- Intervention ate and count and percentage for categorical variables. Com- The admission criteria warranted providing early inten- parisons between groups were done by two-sample t test or sive rehabilitation program in post–acute COVID-19 patients. Wilcoxon ranks sum test for continuous variables and by The functional status of individuals at admission was thor- chi-square test or Fisher exact test for categorical variables. oughly assessed by the multidisciplinary team composed of A prespecified significance level of 0.05 (two sided) was physiatrists and medical consultants, physical therapists, oc- used for all analyses. Statistical analyses were performed cupational therapists, speech therapists, neuropsychologists, using STATA 15.0 (College Station, TX). The medical re- respiratory therapists, and rehabilitation nursing to capture cords of 100 patients admitted in the CORE+ unit from the full range of consequences of COVID-19 infection. The April to December 2020 were included for review and no re- patient-tailored treatment protocol was determined by team cords were excluded. evaluation and prioritized taking the patients’ goals into ac- Exemption from institutional review board review and count. The program was delivered in 3 hrs of one-on-one waiver of informed consent were approved as a retrospective treatment per day and 5 to 7 days per week in a contained en- chart review study. vironment with separated gym space and equipment. For pa- tients who required respiratory support, the treatment plan in- Participants corporated pulmonary rehabilitation including but not limited This retrospective review included 100 patients admitted to optimization of overall medical management, progressive to the CORE+ unit consecutively from April 2020 to exercise protocol with closely monitored vital signs and pulse December 2020. Admission criteria were variable during the oximetry, energy conservation techniques, and respiratory period of retrospective study. Initially, any patient from within 12,13 physiotherapy. In addition, the mobility and daily activity or outside the authors’ institution who met the following ad- functional training activities were tailored to address the indi- mission criteria was considered to the CORE+ unit : 7 days vidual’s functional deficits. For patients with cognitive im- from the diagnosis of COVID-19; at least 72 hrs nonfebrile pairment, cognitive therapy involved a combination of reme- without taking fever-reducing medication; may have a trache- diation through direct training, metacognitive strategy in- ostomy but no need for prescribed suction; oxygen need ≤5 struction, and use of compensatory techniques. All L at rest; improving COVID-19-related symptoms and in need patients were able to access daily speech/swallow pathology of rehabilitation, while also considering individual psychoso- and neuropsychology service for cognition assessment and cial needs such as home environment and impact on family 14,15 psychologic support as well, if needed. members; non-COVID (+) rehabilitation unit patients who be- came positive on screening and developed mild symptoms; and RESULTS ability to tolerate and participate 3 hrs per day of therapy (phys- ical therapy, occupational therapy, and/or speech therapy) 5 to Among the 100 patients admitted to the CORE+ unit, 59 7 days per week in commensurate with inpatient rehabilitation (mean age, 65 ± 13.2 yrs) were admitted because of functional facility (IRF) requirements under the regulation of the Centers impairment primarily stemming from COVID-19 (the pri- for Medicare & Medicaid Services. The isolation ended based mary pulmonary cohort). The remaining 41 patients (mean on the polymerase chain reaction testing result initially; later in age, 62 ± 16.7 yrs) were admitted because of other debility di- the pandemic, the isolation precaution was based on agnoses (the COVID-19 coinfection cohort), with coincident symptom-based strategy as per the Centers for Disease Control coinfection with COVID-19 (positive polymerase chain reac- and Prevention guideline that was in effect at the given time. tion test result or mild symptoms, but no need for active © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. www.ajpmr.com 499 Cao et al. Volume 102, Number 6, June 2023 TABLE 1. Clinical characteristics comparison between COVID-19 patients with primary pulmonary manifestation and patients with other rehabilitation diagnosis with COVID-19 coinfection in the CORE+ unit COVID 19 With Primary Pulmonary COVID-19 Coinfection P No. of patients 59 42 Age, mean (SD), years 65 (13.2) 62 (16.7) 0.34 Sex, n (%) 1.0 Male 31 (52.5) 22 (52.4) Female 28 (47.5) 19 (45.2) BMI, mean (SD), kg/m 30 (7.6) 28.6 (6.1) 0.31 Habitual smokers, n (%) 14 (23.7) 14 (33.3) 0.40 Comorbidities, n (%) Hypertension 48 (81.4) 26 (61.9) 0.051 Diabetes type 2 23 (40) 18 (42.9) 0.85 Cardiac dysfunction 23 (40) 21 (50) 0.37 COPD 8 (14) 3 (7.1) 0.35 Kidney disease 13 (22) 10 (23.8) 1.0 Malignance 5 (8.5) 6 (14.3) 0.52 Complications, n (%) DVT 5 (8.5) 1 (2.4) 0.40 Pulmonary embolism 5 (8.5) 3 (7.1) 1.0 BMI indicates body mass index; COPD, chronic obstructive pulmonary disease; DVT, deep vein thrombosis. treatment; Table 1). Among the 41 rehabilitation patients with followed by cardiac disease (including heart failure, coronary COVID-19 coinfection, stroke (15), spinal cord injury (11), artery disease, cardiac surgery, and atrial fibrillation) and dia- and medical complex patients (8) comprised most of the pri- betes, prevalent among 40%–50% of patients. Fewer than mary rehabilitation diagnoses. The demographic and clinical 15% of patients had a history of chronic obstructive pulmo- characteristics of these two cohorts were compared and ana- nary disease; approximately 20%–30% were recorded as ac- lyzed. No statistically significant differences were found be- tive smokers (Table 1). tween the two cohorts in terms of age, sex, body mass index, or In terms of thromboembolic complications developed in other comorbidities. Body mass index in both groups was catego- acute care as well as in the CORE+ unit, a slightly higher rate rized as overweight/obese or not. Hypertension was the most com- of deep vein thrombosis was detected in the primary pulmo- mon comorbidity identified in both cohorts ( P = 0.051), nary cohort, but this difference was not statistically significant TABLE 2. Demographic and clinical characteristics of patients with primarily pulmonary manifestations of COVID-19 stratified by requirement for invasive mechanical ventilation while in the acute care hospital COVID-19 Patients With Primary Pulmonary Presentation Ventilation Before IRF No Ventilation Before IRF P No. of patients 14 45 Age, mean (SD), years 63 (11.6) 67 (12) 0.28 Sex, n (%) 0.37 Male 9 (64) 22 (49) Female 5 (36) 23 (51) BMI, mean (SD), kg/m 30 (6.4) 30 (7.6) 1.0 Habitual smokers, n (%) 2 (14) 12 (27) 0.48 Comorbidities, n (%) Hypertension 13 (93) 35 (78) 0.27 Diabetes type 2 6 (43) 17 (38) 0.76 Cardiac dysfunction 5 (36) 18 (40) 1.0 COPD 2 (14) 6 (13) 1.0 Kidney disease 2 (14) 11 (24) 0.71 Malignance 1 (7) 4 (9) 1.0 Complications, n (%) DVT 2 (14) 2 (4) 0.24 Pulmonary embolism 3 (21) 3 (6.7) 0.14 BMI indicates body mass index; COPD, chronic obstructive pulmonary disease; DVT, deep vein thrombosis. 500 www.ajpmr.com © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. Volume 102, Number 6, June 2023 Efficacy of Early Rehab of Post-COVID Patients TABLE 3. Rehabilitation outcomes in COVID-19 patients with primary pulmonary manifestation Post-ICU Without ICU P No. of patients 14 45 ICU LOS, median (IQR) 9.0 (4.0, 11.8) NA NA Acute care LOS, median (IQR) 18 (16, 26) 10 (7, 13) <0.0001 Rehabilitation LOS, median (IQR) 13 (10, 16) 12.5 (11, 15.3) 0.62 Section GG functional measure PT (mobility), mean (SD) Admission 27 (8.0) 31 (12.4) 0.17 Discharge 71 (22.3) 72 (22.96) 0.89 Functional change 44 (21.3) 41 (18.2) 0.64 OT (self-care), mean (SD) Admission 19 (19.2) 20 (5.4) 0.85 Discharge 35 (8.3) 34 (9.2) 0.70 Functional change 17 (7.5) 14 (6.4) 0.19 SLP cognitive support, n (%) Admission 11 (78.6%) 34 (75.6%) 1.0 Discharge 5 (35.7%) 28 (62.2%) 0.12 P <0.05. LOS indicates length of stay; OT, occupational therapy; PT, physical therapy; SLP, speech therapy. compared with the rate of deep vein thrombosis diagnosed in Table 3). In terms of cognitive impairment assessed by speech the COVID-19 coinfection cohort (Table 1). and occupational therapists, more than 70% of the patients in Among the 59 patients who presented primarily for both groups needed cognitive therapy support on admission. acute respiratory manifestations due to COVID-19 infection, Although most of the patients responded to cognitive reha- 14 required invasive mechanical ventilation. The demo- bilitation treatment, approximately 30% of post-ICU pa- graphic and clinical characteristics of the cohort were further tients required continuous cognitive therapy on discharge. analyzed and compared based on the need for mechanical Cognitive impairment was also persistent in approximately ventilation. The prevalence of chronic obstructive pulmo- 60% of patients who did not require ventilator treatment. It nary disease was similar in patients who did or did not re- was observed that orientation was mostly improved in these quire mechanical ventilation (13% vs. 14%, P = 1.0). Hyper- patients at discharge, but deficits in memory, attention to de- tension, diabetes mellitus, and cardiac pathology were tails, and information processing persisted. among the most prevalent comorbidities in both groups of Other aspects of outcomes were analyzed, as shown in patients (Table 2). Deep vein thromboses and pulmonary Table 4. The percentage of patients who experienced mood emboli were more common in patients who received me- changes (primarily anxiety and depression) that required chanical ventilation than in patients who did not receive me- neuropsychology support was not significantly different be- chanical ventilation, but these differences were not statisti- tween the two groups. The number of patients who had cally significant (14% and 21% vs. 4% and 6.7%, P =0.24 and P = 0.14). Five post-ICU patients developed critical ill- ness neuropathy/myopathy, which were based on physical TABLE 4. Other outcomes in COVID-19 patients with primary pulmonary manifestation examination on admission (later confirmed by electromyo- graphy/nerve conduction study). The diagnosis of post– Post-ICU Without ICU P intensive care syndrome, defined as new or worsened phys- ical, cognitive, and/or mental health impairment that persists Neuropsychology need, n (%) 1 (7.1) 7 (15.5) 0.67 after ICU stay, was attempted by interdisciplinary team as- Dysphagia, n (%) 4,15 sessment on admission ; however, physical/mental de- Admission 5 (35.7) 7 (15.6) 0.13 cline was highly prevalent in both cohorts, which might have Discharge 0 (0) 1 (2) 1.0 Oxygen requirement, n (%) been confounded by the impact of COVID-19 infection. Admission 6 (42.9) 21 (46.7) 1.0 The functional outcomes were further analyzed in the Discharge 0 (0) 2 (4.4) 1.0 group of patients who required ventilation or experienced an Disposition, n (%) 0.038 ICU stay. Compared with the patients who did not experience Home 11 (78.6) 44 (97.8) an ICU stay, they had a similar length of rehabilitation stay (13 post-ICU vs. 12.5 non-ICU, 3 and 12.5 was based on me- SNF 1 (7.1) 0 (0) dian [IQR]), but a significantly longer acute care length of stay Acute 2 (14.3) 1 (2.2) (18 vs. 10 P < 0.05) before transfer to the CORE+ unit. All of P <0.05. the patients had significant functional gains in the occupational SNF indicates skilled nursing facility. therapy and physical therapy GG section scale (shown in © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. www.ajpmr.com 501 Cao et al. Volume 102, Number 6, June 2023 difficulty swallowing after ICU stay was greater than that in University Mental Status Examination and health-related the group of patients who did not experience an ICU stay, but quality of life-14 as part of the assessments, in addition to the most of the patients completely recovered by discharge. A 6-min walk and forced expiratory volume in 1 sec, to track pa- similar phenomenon was observed in the outcomes of pul- tients’ recovery after being discharged from the CORE+ unit. monary rehabilitation. Although more than 40% of patients re- The authors would like to stress that of the severely af- quired new supplemental oxygen (since COVID infection) on fected patients who received ventilation treatment, 85.7% were CORE+ unit admission, almost all patients were able to be able to complete the program and presented a good response to weaned off oxygen by discharge. There were no significant dif- the rehabilitation program in their institution. However, the ferences observed in the patients who required ventilator treat- acute transfer and skilled nursing facility discharge rate were ment. In comparison with the patients who did not experience significantly higher in patients who received mechanical venti- an ICU stay, the post-ICU patients had a statistically significant lation. This may imply that post–intensive care syndrome might higher rate of acute care transfers (14.3%) and discharges to have played a role in hindering them from reaching community skilled nursing facility (Table 4). Length of stay and disposi- independence. This finding is consistent with the outcomes ob- 19,22 tion were primarily driven by their achieved independence served from other rehabilitation centers with similar settings. level and family support needed while also being impacted In contrast, Curci et al. reported that 41 post-ICU COVID pa- by the general guidelines of individual insurance payer. tients in Italy who received less intensive (two 30-min sessions daily) rehabilitation treatment had a much longer length of stay (31.97 ± 9.06 days) to reach their baseline function, although no- DISCUSSION tably the mean age of the cohort was older (72.15 ± 11.07 yrs) Based on the analysis, there was no significant difference in than the other cohorts. This might suggest that higher intensity baseline demographic and clinical characteristics identified to of therapy could be more beneficial and potentially help the pa- contribute to the risk of developing debilitated pulmonary symp- tients achieve independence in a shorter period. toms when compared with the group without significant respira- tory symptoms after COVID-19 infection. The clinical charac- Limitations teristics of the cohort of patients in this study did have a higher The authors need to point out that this study reports only on prevalence of obesity (100%), hypertension (70%–90%), and unvaccinated patients with COVID-19 (alpha and delta variants) diabetes (>40%) than other published cohorts in Austria, admitted for inpatient rehabilitation care based on admission France, and United Kingdom, but comparable with character- criteria that included assessment of potential to recover. There- 18,19 istics found in other cohorts in North America. fore, the results are not necessarily representative of the entire In comparison with the rehabilitation outcomes from other COVID-19 population, especially with changes in COVID-19 19,20 inpatient rehabilitation facilities, it was observed that the variants and acute infection management. These data might post-COVID survivors who met the acute inpatient rehabilita- not be generalized to other rehabilitation centers with different tion admission criteria set up for the CORE+ unit demonstrated admission criteria or IRF regulation internationally. excellent potential to regain their previous physical indepen- dence and return to community after a relatively short rehabili- CONCLUSION tation stay regardless of their previous ICU stay. The average of length of stay (around 15 days) for the primary pulmonary Tremendous efforts made to advance therapeutic interven- COVID patients in the CORE+ unit was comparable with that tions resulted in reducing the mortality of patients with severe (around 14 days) for the medically complex patients admitted COVID-19 illness. However, functional impairment for most to the non-COVID rehabilitation unit during the same period. survivors and their recovery process has not been fully ad- With regard to respiratory functional outcomes, it was observed dressed owing to the overwhelmed acute care system, includ- that most post-COVID-19 patients recovered considerably well ing rehabilitation centers, in highly prevalent regions. Fortu- from a pulmonary standpoint as they generally did not require nately, the authors’ institution was one of the first inpatient fa- any oxygen support on discharge from IRF. cilities that were able to respond in a timely manner during the It is important to highlight in this study that cognitive im- first and second pandemic waves before vaccination and pro- pairment was found to be quite prevalent in the hospitalized vided effective acute inpatient rehabilitation service to meet pa- COVID-19 patients and seemed more challenging to ad- tients’ needs. The early multidisciplinary team treatment dress, even in the patients who did not receive intubation or proved to be an effective approach to maximize their indepen- stay in the ICU. Although there is greater appreciation for this dence, efficiently utilize healthcare resources, and prepare this now, at the time, there was much less information regarding vulnerable population for the future. These data reflect the out- this important complication. The mechanisms of the neurolo- comes of a single rehabilitation center but are a valuable contri- gic sequelae of post-COVID-19 infection are multifactorial bution to the current limited understanding of the recovery pro- 2,4,11 and had been widely reported. Therefore, cognitive as- cess in hospitalized COVID-19 survivors. The experience will sessment on admission for COVID-19 patients is essential for also help to design rehabilitation programs geared to the rehabilitation, and community rehabilitation support must be expanding spectrum of nonpulmonary involvements in geared to the needs of patients with cognitive decline and other COVID-19 patients. To the authors’ best knowledge, the data nonpulmonary manifestations that could play a major role in presented are the one of very few studies to investigate compre- the long COVID-19 recovery and to optimize quality of life. hensively a post–acute care cohort of COVID-19 patients re- Based on the findings, a framework was developed and imple- garding their functional status and rehabilitation intervention mented in the COVID outpatient clinic to include Saint Louis and outcomes. 502 www.ajpmr.com © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. Volume 102, Number 6, June 2023 Efficacy of Early Rehab of Post-COVID Patients 11. Sheehy LM: Considerations for postacute rehabilitation for survivors of covid-19. ACKNOWLEDGMENTS JMIR Public Health Surveill 2020;6:e19462 The authors thank the interdisciplinary team of providers 12. Centers for Disease Control and Prevention: Ending isolation and precautions for people with COVID-19: Interim guidance. 2021. 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Abstract

ORIGINAL RESEARCH ARTICLE Efficacy of Early Inpatient Rehabilitation of Post-COVID-19 Survivors Single-Center Retrospective Analysis Ning Cao, MD, Jaclyn Barcikowski, DO, Franklin Womble, MD, Bianca Martinez, MD, Yevgeniya Sergeyenko, MD, Jacob H. Koffer, MD, Michael Kwasniewski, MD, Thomas Watanabe, MD, Rui Xiao, PhD, and Alberto Esquenazi, MD n late 2019, a highly pathogenic novel coronavirus Objective: The aim of this study was to understand the demographic, I (COVID-19) causing severe acute respiratory syndrome clinical characteristics, and effectiveness of early inpatient rehabilita- (SARS)-CoV-2 emerged in Wuhan, China, and soon spread tion of post-COVID survivors. 1,2 throughout the world, causing a global pandemic. Many pa- Design: A single-center retrospective chart review analysis of 100 pa- tients with COVID-19 infection required prolonged hospitalization, tients admitted to a newly created acute COVID rehabilitation unit assisted ventilation, and critical care management. As a result, (CORE+) from April to December 2020 was conducted. many COVID-19 survivors developed deconditioning; physical, Results: The demographic and clinical characteristics and complica- cognitive, and psychologic sequelae; and persistent respiratory tions of 100 post-COVID patients were reviewed. Functional out- 3–5 problems, as well as other complications that are even now not comes of GG Self-care and Mobility Activities Items (Section fully appreciated. Data from countries initially affected by the pan- GG0130 and GG0170) of the Centers for Medicare & Medicaid Ser- demic demonstrated that the rapid spread of the infection quickly vices of the Inpatient Rehabilitation Facility Patient Assessment In- 6,7 overloaded their national health systems. strument (Version 3.0) at admission and discharge, prevalence of oxy- Historical data from Medicare suggest that more than gen requirement, the need for cognitive and neuropsychology support 30% of patients hospitalized with sepsis, a condition with inpa- by discharge, and dispositions after completion of inpatient rehabilita- tient mortality like that associated with COVID-19, require tion facility stay were analyzed. The functional outcomes of 59 pri- facility-based care. Post acute care often serves as a “pop-off mary pulmonary manifestations of COVID patients were further ana- valve” for hospital capacity, in that transferring patients to a such lyzed based on the presence of intensive care unit stay before transfer a setting once they recover from the most acute phase of their ill- to the COVID rehabilitation unit. Most patients demonstrated signifi- ness could free up acute care hospital beds. Because of the cant functional gains after completion of inpatient rehabilitation facil- COVID-19 patient surge, along with reallocation of post– ity stay; however, a considerable number of patients continued to re- acute care facilities as acute care spaces and workforce deple- quire cognitive support by discharge. tion, post acute care became strained, as was first seen in the Conclusion: The data suggested the benefit of early rehabilitation for major cities of Boston and New York City. hospitalized post-COVID patients. Services need to be geared to in- At the authors’ institution, a specialized acute inpatient re- clude patients’ cognitive deficits. habilitation unit to address the functional and medical needs of Key Words: Inpatient Rehabilitation, Functional Outcomes, post-COVID patients early after the critical acute care phase Post-COVID, Post-ICU Syndrome was created, as well as for those patients in need of inpatient re- habilitation for another reason but who became actively in- (Am J Phys Med Rehabil 2023;102:498–503) fected. The development of a dedicated “center of excellence” specializing in and assuming the care of patients recovering from COVID-19 was developed through what was termed the CORE+ unit (COVID rehabilitation unit). Patients would un- dergo a comprehensive rehabilitation program with a multidis- From the MossRehab, Elkins Park, Pennsylvania (NC, JB, FW, BM, YS, JHK, MK, ciplinary team with staff provided appropriate safety equip- TW, AE); Temple University Hospital, Philadelphia, Pennsylvania (FW, BM, ment, training, and adequate personal protective equipment to JHK); and Biostatistics and Epidemiology at the Hospital of the University of provide this care safely. The unit opened in April 2020 and Pennsylvania, Philadelphia, Pennsylvania (RX). All correspondence should be addressed to: Ning Cao, MD, MossRehab, 60 closed on July 1, 2021. The alpha and delta variants of Township Line Road, Elkins Park, PA 19027. COVID-19 were the dominant strains during this time period. Ning Cao current affiliation: Physical Medicine and Rehabilitation Department, Johns Hopkins University School of Medicine, 600 N. Wolfe St., Baltimore, MD 21287. This study reports on the demographics, clinical character- Franklin Womble, Bianca Martinez, and Jacob H. Koffer are in training. istics, and functional outcomes, including cognitive/psychologic Financial disclosure statements have been obtained, and no conflicts of interest have been and ultimate discharge destination, of the patients treated in the reported by the authors or by any individuals in control of the content of this article. Copyright © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. This is CORE+ unit from April 2020 to December 2020 (before vac- an open-access article distributed under the terms of the Creative Commons cines were available). The purpose of this retrospective re- Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC-ND), view has many folds. The comorbidities and clinical charac- where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in any way or used commercially without teristics of the hospitalized COVID patients were analyzed permission from the journal. to assess any underlying factors contributing to the patients ISSN: 0894-9115 DOI: 10.1097/PHM.0000000000002122 who might have a risk of developing primary respiratory 498 www.ajpmr.com American Journal of Physical Medicine & Rehabilitation � Volume 102, Number 6, June 2023 Volume 102, Number 6, June 2023 Efficacy of Early Rehab of Post-COVID Patients symptoms as opposed to those in the cohort with minimal re- Outcomes spiratory symptoms after COVID infection. Furthermore, The electronic medical records of patients admitted to the physical and cognitive aspects of outcomes were analyzed the CORE+ unit during April to December 2020 were re- in the primary COVID-19 patients who received ventilator vs. viewed. Patients’ demographics (age, sex, and body mass in- no ventilator treatment to evaluate how patients with different dex), comorbidities, length of hospital stay (including inten- severities of respiratory disease responded to interdisciplinary sive care unit [ICU]) before transfer to rehabilitation, length treatment in the CORE+ unit. of rehabilitation stay, and data regarding newly developed The results are intended to provide insights on the effective- thromboembolic complications were collected. ness of early interdisciplinary rehabilitation for post-COVID In addition, the functional outcomes assessed at admission survivors, particularly given that the potential risk factors and re- and discharge were composed of GG Self-care and Mobility habilitation needs of patients with severe COVID disease and Activities Items (Section GG0130 and GG0170) of the Centers their trajectory of recovery were not known. for Medicare & Medicaid Services–issued Inpatient Rehabilita- tion Facility Patient Assessment Instrument Version 3.0; speech/ cognitive therapy need as assessed by speech and occupational therapists using various tools including the Orientation log METHODS (O-Log), Montreal Cognitive Assessment, Saint Louis University Mental Status, and Cognitive Linguistic Quick Test based on pa- Statistical Analysis tients’ clinical characteristics; supplemental oxygen requirement; The demographic and clinical characteristics of the pa- the need for neuropsychology support; and disposition to home/ tients were summarized by standard descriptive statistics, acute care/skilled nursing facility setting after completion of IRF. that is, mean and standard deviation (SD) or median and in- terquartile range (IQR) for continuous variables as appropri- Intervention ate and count and percentage for categorical variables. Com- The admission criteria warranted providing early inten- parisons between groups were done by two-sample t test or sive rehabilitation program in post–acute COVID-19 patients. Wilcoxon ranks sum test for continuous variables and by The functional status of individuals at admission was thor- chi-square test or Fisher exact test for categorical variables. oughly assessed by the multidisciplinary team composed of A prespecified significance level of 0.05 (two sided) was physiatrists and medical consultants, physical therapists, oc- used for all analyses. Statistical analyses were performed cupational therapists, speech therapists, neuropsychologists, using STATA 15.0 (College Station, TX). The medical re- respiratory therapists, and rehabilitation nursing to capture cords of 100 patients admitted in the CORE+ unit from the full range of consequences of COVID-19 infection. The April to December 2020 were included for review and no re- patient-tailored treatment protocol was determined by team cords were excluded. evaluation and prioritized taking the patients’ goals into ac- Exemption from institutional review board review and count. The program was delivered in 3 hrs of one-on-one waiver of informed consent were approved as a retrospective treatment per day and 5 to 7 days per week in a contained en- chart review study. vironment with separated gym space and equipment. For pa- tients who required respiratory support, the treatment plan in- Participants corporated pulmonary rehabilitation including but not limited This retrospective review included 100 patients admitted to optimization of overall medical management, progressive to the CORE+ unit consecutively from April 2020 to exercise protocol with closely monitored vital signs and pulse December 2020. Admission criteria were variable during the oximetry, energy conservation techniques, and respiratory period of retrospective study. Initially, any patient from within 12,13 physiotherapy. In addition, the mobility and daily activity or outside the authors’ institution who met the following ad- functional training activities were tailored to address the indi- mission criteria was considered to the CORE+ unit : 7 days vidual’s functional deficits. For patients with cognitive im- from the diagnosis of COVID-19; at least 72 hrs nonfebrile pairment, cognitive therapy involved a combination of reme- without taking fever-reducing medication; may have a trache- diation through direct training, metacognitive strategy in- ostomy but no need for prescribed suction; oxygen need ≤5 struction, and use of compensatory techniques. All L at rest; improving COVID-19-related symptoms and in need patients were able to access daily speech/swallow pathology of rehabilitation, while also considering individual psychoso- and neuropsychology service for cognition assessment and cial needs such as home environment and impact on family 14,15 psychologic support as well, if needed. members; non-COVID (+) rehabilitation unit patients who be- came positive on screening and developed mild symptoms; and RESULTS ability to tolerate and participate 3 hrs per day of therapy (phys- ical therapy, occupational therapy, and/or speech therapy) 5 to Among the 100 patients admitted to the CORE+ unit, 59 7 days per week in commensurate with inpatient rehabilitation (mean age, 65 ± 13.2 yrs) were admitted because of functional facility (IRF) requirements under the regulation of the Centers impairment primarily stemming from COVID-19 (the pri- for Medicare & Medicaid Services. The isolation ended based mary pulmonary cohort). The remaining 41 patients (mean on the polymerase chain reaction testing result initially; later in age, 62 ± 16.7 yrs) were admitted because of other debility di- the pandemic, the isolation precaution was based on agnoses (the COVID-19 coinfection cohort), with coincident symptom-based strategy as per the Centers for Disease Control coinfection with COVID-19 (positive polymerase chain reac- and Prevention guideline that was in effect at the given time. tion test result or mild symptoms, but no need for active © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. www.ajpmr.com 499 Cao et al. Volume 102, Number 6, June 2023 TABLE 1. Clinical characteristics comparison between COVID-19 patients with primary pulmonary manifestation and patients with other rehabilitation diagnosis with COVID-19 coinfection in the CORE+ unit COVID 19 With Primary Pulmonary COVID-19 Coinfection P No. of patients 59 42 Age, mean (SD), years 65 (13.2) 62 (16.7) 0.34 Sex, n (%) 1.0 Male 31 (52.5) 22 (52.4) Female 28 (47.5) 19 (45.2) BMI, mean (SD), kg/m 30 (7.6) 28.6 (6.1) 0.31 Habitual smokers, n (%) 14 (23.7) 14 (33.3) 0.40 Comorbidities, n (%) Hypertension 48 (81.4) 26 (61.9) 0.051 Diabetes type 2 23 (40) 18 (42.9) 0.85 Cardiac dysfunction 23 (40) 21 (50) 0.37 COPD 8 (14) 3 (7.1) 0.35 Kidney disease 13 (22) 10 (23.8) 1.0 Malignance 5 (8.5) 6 (14.3) 0.52 Complications, n (%) DVT 5 (8.5) 1 (2.4) 0.40 Pulmonary embolism 5 (8.5) 3 (7.1) 1.0 BMI indicates body mass index; COPD, chronic obstructive pulmonary disease; DVT, deep vein thrombosis. treatment; Table 1). Among the 41 rehabilitation patients with followed by cardiac disease (including heart failure, coronary COVID-19 coinfection, stroke (15), spinal cord injury (11), artery disease, cardiac surgery, and atrial fibrillation) and dia- and medical complex patients (8) comprised most of the pri- betes, prevalent among 40%–50% of patients. Fewer than mary rehabilitation diagnoses. The demographic and clinical 15% of patients had a history of chronic obstructive pulmo- characteristics of these two cohorts were compared and ana- nary disease; approximately 20%–30% were recorded as ac- lyzed. No statistically significant differences were found be- tive smokers (Table 1). tween the two cohorts in terms of age, sex, body mass index, or In terms of thromboembolic complications developed in other comorbidities. Body mass index in both groups was catego- acute care as well as in the CORE+ unit, a slightly higher rate rized as overweight/obese or not. Hypertension was the most com- of deep vein thrombosis was detected in the primary pulmo- mon comorbidity identified in both cohorts ( P = 0.051), nary cohort, but this difference was not statistically significant TABLE 2. Demographic and clinical characteristics of patients with primarily pulmonary manifestations of COVID-19 stratified by requirement for invasive mechanical ventilation while in the acute care hospital COVID-19 Patients With Primary Pulmonary Presentation Ventilation Before IRF No Ventilation Before IRF P No. of patients 14 45 Age, mean (SD), years 63 (11.6) 67 (12) 0.28 Sex, n (%) 0.37 Male 9 (64) 22 (49) Female 5 (36) 23 (51) BMI, mean (SD), kg/m 30 (6.4) 30 (7.6) 1.0 Habitual smokers, n (%) 2 (14) 12 (27) 0.48 Comorbidities, n (%) Hypertension 13 (93) 35 (78) 0.27 Diabetes type 2 6 (43) 17 (38) 0.76 Cardiac dysfunction 5 (36) 18 (40) 1.0 COPD 2 (14) 6 (13) 1.0 Kidney disease 2 (14) 11 (24) 0.71 Malignance 1 (7) 4 (9) 1.0 Complications, n (%) DVT 2 (14) 2 (4) 0.24 Pulmonary embolism 3 (21) 3 (6.7) 0.14 BMI indicates body mass index; COPD, chronic obstructive pulmonary disease; DVT, deep vein thrombosis. 500 www.ajpmr.com © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. Volume 102, Number 6, June 2023 Efficacy of Early Rehab of Post-COVID Patients TABLE 3. Rehabilitation outcomes in COVID-19 patients with primary pulmonary manifestation Post-ICU Without ICU P No. of patients 14 45 ICU LOS, median (IQR) 9.0 (4.0, 11.8) NA NA Acute care LOS, median (IQR) 18 (16, 26) 10 (7, 13) <0.0001 Rehabilitation LOS, median (IQR) 13 (10, 16) 12.5 (11, 15.3) 0.62 Section GG functional measure PT (mobility), mean (SD) Admission 27 (8.0) 31 (12.4) 0.17 Discharge 71 (22.3) 72 (22.96) 0.89 Functional change 44 (21.3) 41 (18.2) 0.64 OT (self-care), mean (SD) Admission 19 (19.2) 20 (5.4) 0.85 Discharge 35 (8.3) 34 (9.2) 0.70 Functional change 17 (7.5) 14 (6.4) 0.19 SLP cognitive support, n (%) Admission 11 (78.6%) 34 (75.6%) 1.0 Discharge 5 (35.7%) 28 (62.2%) 0.12 P <0.05. LOS indicates length of stay; OT, occupational therapy; PT, physical therapy; SLP, speech therapy. compared with the rate of deep vein thrombosis diagnosed in Table 3). In terms of cognitive impairment assessed by speech the COVID-19 coinfection cohort (Table 1). and occupational therapists, more than 70% of the patients in Among the 59 patients who presented primarily for both groups needed cognitive therapy support on admission. acute respiratory manifestations due to COVID-19 infection, Although most of the patients responded to cognitive reha- 14 required invasive mechanical ventilation. The demo- bilitation treatment, approximately 30% of post-ICU pa- graphic and clinical characteristics of the cohort were further tients required continuous cognitive therapy on discharge. analyzed and compared based on the need for mechanical Cognitive impairment was also persistent in approximately ventilation. The prevalence of chronic obstructive pulmo- 60% of patients who did not require ventilator treatment. It nary disease was similar in patients who did or did not re- was observed that orientation was mostly improved in these quire mechanical ventilation (13% vs. 14%, P = 1.0). Hyper- patients at discharge, but deficits in memory, attention to de- tension, diabetes mellitus, and cardiac pathology were tails, and information processing persisted. among the most prevalent comorbidities in both groups of Other aspects of outcomes were analyzed, as shown in patients (Table 2). Deep vein thromboses and pulmonary Table 4. The percentage of patients who experienced mood emboli were more common in patients who received me- changes (primarily anxiety and depression) that required chanical ventilation than in patients who did not receive me- neuropsychology support was not significantly different be- chanical ventilation, but these differences were not statisti- tween the two groups. The number of patients who had cally significant (14% and 21% vs. 4% and 6.7%, P =0.24 and P = 0.14). Five post-ICU patients developed critical ill- ness neuropathy/myopathy, which were based on physical TABLE 4. Other outcomes in COVID-19 patients with primary pulmonary manifestation examination on admission (later confirmed by electromyo- graphy/nerve conduction study). The diagnosis of post– Post-ICU Without ICU P intensive care syndrome, defined as new or worsened phys- ical, cognitive, and/or mental health impairment that persists Neuropsychology need, n (%) 1 (7.1) 7 (15.5) 0.67 after ICU stay, was attempted by interdisciplinary team as- Dysphagia, n (%) 4,15 sessment on admission ; however, physical/mental de- Admission 5 (35.7) 7 (15.6) 0.13 cline was highly prevalent in both cohorts, which might have Discharge 0 (0) 1 (2) 1.0 Oxygen requirement, n (%) been confounded by the impact of COVID-19 infection. Admission 6 (42.9) 21 (46.7) 1.0 The functional outcomes were further analyzed in the Discharge 0 (0) 2 (4.4) 1.0 group of patients who required ventilation or experienced an Disposition, n (%) 0.038 ICU stay. Compared with the patients who did not experience Home 11 (78.6) 44 (97.8) an ICU stay, they had a similar length of rehabilitation stay (13 post-ICU vs. 12.5 non-ICU, 3 and 12.5 was based on me- SNF 1 (7.1) 0 (0) dian [IQR]), but a significantly longer acute care length of stay Acute 2 (14.3) 1 (2.2) (18 vs. 10 P < 0.05) before transfer to the CORE+ unit. All of P <0.05. the patients had significant functional gains in the occupational SNF indicates skilled nursing facility. therapy and physical therapy GG section scale (shown in © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. www.ajpmr.com 501 Cao et al. Volume 102, Number 6, June 2023 difficulty swallowing after ICU stay was greater than that in University Mental Status Examination and health-related the group of patients who did not experience an ICU stay, but quality of life-14 as part of the assessments, in addition to the most of the patients completely recovered by discharge. A 6-min walk and forced expiratory volume in 1 sec, to track pa- similar phenomenon was observed in the outcomes of pul- tients’ recovery after being discharged from the CORE+ unit. monary rehabilitation. Although more than 40% of patients re- The authors would like to stress that of the severely af- quired new supplemental oxygen (since COVID infection) on fected patients who received ventilation treatment, 85.7% were CORE+ unit admission, almost all patients were able to be able to complete the program and presented a good response to weaned off oxygen by discharge. There were no significant dif- the rehabilitation program in their institution. However, the ferences observed in the patients who required ventilator treat- acute transfer and skilled nursing facility discharge rate were ment. In comparison with the patients who did not experience significantly higher in patients who received mechanical venti- an ICU stay, the post-ICU patients had a statistically significant lation. This may imply that post–intensive care syndrome might higher rate of acute care transfers (14.3%) and discharges to have played a role in hindering them from reaching community skilled nursing facility (Table 4). Length of stay and disposi- independence. This finding is consistent with the outcomes ob- 19,22 tion were primarily driven by their achieved independence served from other rehabilitation centers with similar settings. level and family support needed while also being impacted In contrast, Curci et al. reported that 41 post-ICU COVID pa- by the general guidelines of individual insurance payer. tients in Italy who received less intensive (two 30-min sessions daily) rehabilitation treatment had a much longer length of stay (31.97 ± 9.06 days) to reach their baseline function, although no- DISCUSSION tably the mean age of the cohort was older (72.15 ± 11.07 yrs) Based on the analysis, there was no significant difference in than the other cohorts. This might suggest that higher intensity baseline demographic and clinical characteristics identified to of therapy could be more beneficial and potentially help the pa- contribute to the risk of developing debilitated pulmonary symp- tients achieve independence in a shorter period. toms when compared with the group without significant respira- tory symptoms after COVID-19 infection. The clinical charac- Limitations teristics of the cohort of patients in this study did have a higher The authors need to point out that this study reports only on prevalence of obesity (100%), hypertension (70%–90%), and unvaccinated patients with COVID-19 (alpha and delta variants) diabetes (>40%) than other published cohorts in Austria, admitted for inpatient rehabilitation care based on admission France, and United Kingdom, but comparable with character- criteria that included assessment of potential to recover. There- 18,19 istics found in other cohorts in North America. fore, the results are not necessarily representative of the entire In comparison with the rehabilitation outcomes from other COVID-19 population, especially with changes in COVID-19 19,20 inpatient rehabilitation facilities, it was observed that the variants and acute infection management. These data might post-COVID survivors who met the acute inpatient rehabilita- not be generalized to other rehabilitation centers with different tion admission criteria set up for the CORE+ unit demonstrated admission criteria or IRF regulation internationally. excellent potential to regain their previous physical indepen- dence and return to community after a relatively short rehabili- CONCLUSION tation stay regardless of their previous ICU stay. The average of length of stay (around 15 days) for the primary pulmonary Tremendous efforts made to advance therapeutic interven- COVID patients in the CORE+ unit was comparable with that tions resulted in reducing the mortality of patients with severe (around 14 days) for the medically complex patients admitted COVID-19 illness. However, functional impairment for most to the non-COVID rehabilitation unit during the same period. survivors and their recovery process has not been fully ad- With regard to respiratory functional outcomes, it was observed dressed owing to the overwhelmed acute care system, includ- that most post-COVID-19 patients recovered considerably well ing rehabilitation centers, in highly prevalent regions. Fortu- from a pulmonary standpoint as they generally did not require nately, the authors’ institution was one of the first inpatient fa- any oxygen support on discharge from IRF. cilities that were able to respond in a timely manner during the It is important to highlight in this study that cognitive im- first and second pandemic waves before vaccination and pro- pairment was found to be quite prevalent in the hospitalized vided effective acute inpatient rehabilitation service to meet pa- COVID-19 patients and seemed more challenging to ad- tients’ needs. The early multidisciplinary team treatment dress, even in the patients who did not receive intubation or proved to be an effective approach to maximize their indepen- stay in the ICU. Although there is greater appreciation for this dence, efficiently utilize healthcare resources, and prepare this now, at the time, there was much less information regarding vulnerable population for the future. These data reflect the out- this important complication. The mechanisms of the neurolo- comes of a single rehabilitation center but are a valuable contri- gic sequelae of post-COVID-19 infection are multifactorial bution to the current limited understanding of the recovery pro- 2,4,11 and had been widely reported. Therefore, cognitive as- cess in hospitalized COVID-19 survivors. The experience will sessment on admission for COVID-19 patients is essential for also help to design rehabilitation programs geared to the rehabilitation, and community rehabilitation support must be expanding spectrum of nonpulmonary involvements in geared to the needs of patients with cognitive decline and other COVID-19 patients. To the authors’ best knowledge, the data nonpulmonary manifestations that could play a major role in presented are the one of very few studies to investigate compre- the long COVID-19 recovery and to optimize quality of life. hensively a post–acute care cohort of COVID-19 patients re- Based on the findings, a framework was developed and imple- garding their functional status and rehabilitation intervention mented in the COVID outpatient clinic to include Saint Louis and outcomes. 502 www.ajpmr.com © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. Volume 102, Number 6, June 2023 Efficacy of Early Rehab of Post-COVID Patients 11. Sheehy LM: Considerations for postacute rehabilitation for survivors of covid-19. ACKNOWLEDGMENTS JMIR Public Health Surveill 2020;6:e19462 The authors thank the interdisciplinary team of providers 12. Centers for Disease Control and Prevention: Ending isolation and precautions for people with COVID-19: Interim guidance. 2021. 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