Globally, millions of people are infected with the severe acute respiratory syndrome coronavirus 2, causing the coronavirus disease 19 (COVID-19) (1). A proportion of the of the confirmed COVID-19 patients are admitted to the hospital for acute care, due to severe respiratory symptoms and in some cases even acute respiratory distress requiring prolonged mechanical ventilation (2) .
It is very likely that a proportion of the COVID-19 patients will have a need for rehabilitative interventions during and directly after the hospitalization (3) (4) (5) (6) . This approach is also recommended by the World Health Organization (7). However, data on safety and efficacy of rehabilitation during and/or after hospitalization in these patients are lacking. Equally, healthcare professionals cannot wait for well-designed randomized controlled trials to be published before they can start these rehabilitative interventions in daily clinical practice, as the number of COVID-19 patients increases rapidly every day.
Evidence (CORE) process to make recommendations for the management of COVID-19 (8). The CORE process is a consensus-based approach to making clinical recommendations that has been shown to yield recommendations that are concordant with recommendations developed using Institute of Medicine-adherent methodology (9) . The same methodology was used to develop interim guidance on rehabilitative interventions in the hospital and post-hospital phase in COVID-19 patients pending empirical evidence.
An ad-hoc international Task Force was assembled, including the European Respiratory Society (ERS) and American Thoracic Society (ATS) key opinion leaders as well as key opinion leaders and clinical experts from other relevant societies in the field of pulmonary rehabilitation. Invitations were sent to 93 experts within the field of pulmonary rehabilitation, respiratory and critical care medicine of physical medicine and rehabilitation. Seventy-six agreed to participate (82%). As described before (8), SurveyMonkey platform (SurveryMonkey, San Mateo, CA) was used to create 13-question multiple choice survey. Each question consisted of three parts: 1) presentation of the question in a modified PICO (Patient, Intervention, Comparator, Outcomes) format; 2) a multiple-choice question asking for strong or conditional recommendation for or against a course of action or no recommendation; and 3) a free text box for comments.
After publishing an initial web-based blog on April 3rd 2020 and seeking global input (10), the core team of experts (MAS, AEH, SJS, TT) put together a list of possible relevant questions, and during three teleconferences, consensus was reached amongst about which question to maintain.
Wording of the questions was adapted with input of ERS and ATS methodology teams to ensure unequivocal interpretation and consistency. The survey was not piloted in order to have more timely recommendations.
The survey was administered once from April 27 to May 11, 2020, including several reminders.
Agreement of directionality was tabulated for each multiple-choice question. At least 70% agreement on directionality was necessary to make consensus suggestions. The proportion of respondents per choice per question was calculated and expressed as a percentage of the total number of respondents. As more than 70% agreement on directionality was reached in all questions from the first round, no second round was necessary.
receive rehabilitation at/around the bedside (critical care and/or ward based) until safe for discharge to the home environment.
Rationale. Whilst most people infected with the COVID-19 virus have mild disease (11) , some have more severe symptoms requiring hospital admission, and 20% of those admitted may require intensive care (12) . Hospitalised COVID-19 patients often have comorbidities, such as cardiovascular disease and diabetes (13) and may have prolonged hospital stays (14) . Some COVID-19 survivors have physical impairments that may be exacerbated by prolonged immobility, including muscle weakness, neurological impairment and/or nutritional disturbance (15). Inhospital rehabilitation could effectively address these problems (16). However there may be added challenges for rehabilitation delivery in the setting of COVID-19, related to infection prevention and changes to availability of existing rehabilitation services.
Results. Majority of the experts recommended strongly (55%) or conditionally (37%) for hospitalised patients with COVID-19 receiving rehabilitation at/around the bedside (critical care and/ or ward based) until safe discharge to the home environment ( Figure 1A ; Table 1 ).
Experts commented that patient-tailored early rehabilitative interventions similar to other critically ill patients should start after an assessment, including early mobilization and airway clearance. This may prevent and/or slow down the expected rapid deterioration in physical and emotional functioning. Some experts did express concerns about patients' safety, due to the limited understanding of underlying pathophysiology and the possible impact of rehabilitative interventions. For example, it is unclear if there is any "threshold of illness severity" or any particular features of illness, which pose greater risk of patients undertaking rehabilitative interventions during hospitalization, including pulmonary, cardiovascular and/or neurologic manifestations of COVID-19 infection, in particular, the risk of clotting (micro thrombosis and venous thromboembolism). Moreover, the importance of appropriate personal protective equipment for the healthcare professional was mentioned by multiple experts as clear safety issue.
with COVID-19 should have an assessment of oxygen requirements at rest and during exertion.
Rationale. Hypoxemia is common in hospitalised patients with COVID-19, with hypoxic respiratory failure a prominent feature of severe cases (17). Whilst supplemental oxygen requirements reduce over time, alongside improvements in the underlying lung pathology (18), it is likely that some patients will have ongoing oxygen needs at hospital discharge. Moreover, some patients in the recovery phase may have oxygen desaturation on exertion, which is not associated with resting oxygen saturation, the degree of dyspnoea or feeling unwell.
Results. Majority of the experts recommended strongly (66%) or conditionally (26%) for hospitalised patients with COVID-19 having an assessment of oxygen requirements at rest and during exertion prior to hospital discharge ( Figure 1B ).
Experts commented that assessment of oxygen requirements during exertion may vary between hospitals. However, low oxygen saturation may be a reason for additional assessment for pulmonary and cardiovascular comorbidities. Moreover, some patients do show a severe oxygen desaturation during physical exercise of only moderate intensity. Assessment of oxygen requirement prior to hospital discharge is necessary to prepare the individual COVID-19 patient with the needed equipment upon discharge home. A follow-up assessment on the re-evaluation of oxygen requirement should also be scheduled following hospital discharge, as supplemental oxygen may no longer be needed as the underlying lung pathology resolves. Task Force suggests that patients with COVID-19 should be encouraged to do regular daily activities in the first 6-8 weeks after hospital discharge.
Rationale. Some patients with COVID-19 will resume daily activities without difficulty in the period following hospitalisation, but this may be more challenging in those who have had severe disease, prolonged hospital stays and/or persistent symptoms (19). About two-thirds of the survivors of other critical illnesses experience moderate-to-good recovery of physical function over the first two months (20). However recovery trajectories vary, with ongoing impairments most likely in older patients with longer ICU stays and greater sedation time (20).
Results. Majority of the experts recommended strongly (58%) or conditionally (34%) for encouraging patients with COVID-19 to do regular daily activities in the first 6-8 weeks after hospital discharge ( Figure 1C ). Experts commented that recommencing daily physical activity as early as possible may positively affect functional recovery. However, patients may vary in physical, emotional and/or cognitive functioning. So, further assessment needs to be performed. Moreover, the encouragement to do regular daily activities should be in line with the local regulations for physical distancing and should go along with an advice to take time for recovery and rest periods, also taking an acceptable level of perceived exertion and dyspnoea and oxygen desaturation into consideration. Rationale. COVID-19 infection is associated with a high inflammatory burden (21), which could persist beyond hospital discharge. Exertional desaturation may also persist, even in those without the requirement for supplemental oxygen at rest. Whilst moderate intensity exercise training is safe and feasible in survivors of critical illness (22), the safety of high intensity exercise in patients recovering from COVID-19 is unknown. During the early post hospital period it may not always be possible to conduct a robust exercise assessment or deliver supervised rehabilitation services, with uncertainties regarding the duration that patients remain infectious (23) and/or the need to maintain physical distancing.
Results. Majority of the experts recommended strongly (29%) or conditionally (55%) for encouraging patients with COVID-19 to do low/moderate intensity physical exercise at home (rather than high intensity physical exercise) in the first 6-8 weeks after hospital discharge, if a formal exercise assessment with measures of exertional desaturation has not been conducted.
( Figure 1D ). Some experts stated that the potential benefits of low/moderate physical activity in preventing physical deterioration outweighed any perceived risks of undertaking such exercise without formal assessment. The low/moderate intensity physical exercises should be based on symptom limitation and tailored to the individual needs and limitations of the patients, which may vary largely. In addition to oxygen desaturation on exertion, experts encouraged health professionals to be aware of other possible causes of caution, like cardiomyopathy and (post-)pulmonary embolism. Results. Majority of the experts recommended strongly (75%) or conditionally (22%) for patients with COVID-19 having a formal assessment of physical and emotional functioning at 6-8 weeks following discharge ( Figure 1E ).
Experts stated that post-hospitalization recovery may vary considerably between patients, which justifies a formal assessment (including physical, emotional and cognitive functioning, and return to work) to customize rehabilitation care. Some experts also proposed an evaluation at hospital discharge to ensure patients were discharged to the appropriate setting (e.g., home, rehabilitation centre, nursing home), and to do only a formal assessment in symptomatic patients with limitations in daily functioning. Task Force suggests that follow up of a hospitalised patient with COVID-19 should include the core outcomes set for survivors of acute respiratory failure at 6-8 weeks following hospital discharge.
Rationale. Post-hospital outcomes of COVID-19 survivors are not yet understood. Assessment of physical and psychosocial outcomes following hospitalisation for COVID-19 will allow unmet rehabilitation needs to be addressed. A core outcome set allows essential outcomes to be consistently assessed using the same measurement instruments, so that data can be pooled and confident conclusions drawn. A core outcome set for survivors of acute respiratory failure has already been defined using a consensus process, and includes the EQ-5D, Hospital Anxiety and Depression Scale and Impact of Events Scale-Revised (27). The core outcome set does not include measures of cognition, muscle function, physical function or pulmonary function.
A majority of the experts recommended strongly (63%) or conditionally (30%) for the follow up of a hospitalised patient with COVID-19 including the core outcomes set for survivors of acute respiratory failure at 6-8 weeks following hospital discharge ( Figure 1F ) Experts recognized the importance of administering outcome measures that will help to identify the patients' need in order to direct, plan and devise appropriate interventions and resources to the patients and their caregivers. This may require multiple re-assessments at different time points (e.g., 3,6 and 12 months after hospital discharge). Individual experts suggested the addition of a tool to measure exertional breathlessness (e.g., the MRC dyspnoea grading scale) and cognitive screening (Montreal Cognitive Assessment) and alternative tools to assess the same domains as identified by Needham and colleagues (27) (e.g., Short-Form 36 to assess generic health status; the Primary Care Post-Traumatic Stress Syndrome (PTSD) questionnaire to assess symptoms of PTSD; Patient Health Questionnaire 9, General Anxiety Disorder 7, or the Depression Anxiety Stress Scale 21 to assess symptoms of anxiety and/or depression). Some experts believed that assessment at 6-8 weeks following hospital discharge is too soon, as some sequelae may manifest at later time points. Moreover, some experts indicted that community managed patients may also need a supported recovery programme.
should include measures of respiratory function at 6-8 weeks following hospital discharge.
Rationale. High resolution CT scans of the chest in patients with COVID-19 infection have shown significant respiratory abnormalities including ground glass opacities, inter-and intralobular septal thickening and consolidation. These changes start to resolve after 14 days, but may persist past hospital discharge (18). Long term follow-up of survivors of other severe viral pneumonias (SARS-COV-1 and MERS-COV) suggests that many had normal respiratory function at 1-year, although impaired diffusing capacity was evident in a minority (28, 29). Respiratory function testing is necessary to document ongoing impairments and guide future management, but it is considered an aerosol-generating procedure, which may limit its availability in the COVID-19 era.
A majority of the experts recommended strongly (45%) or conditionally (42%) for the follow up of a hospitalised patient with COVID-19 including measures of respiratory function at 6-8 weeks following hospital discharge ( Figure 1G ).
Experts recognized the importance of measuring respiratory function, as missing respiratory abnormalities are likely to lead to further decline and perhaps downstream new respiratory chronic disease. Experts emphasized to perform assessment only in patients with lingering respiratory symptoms and who were tested COVID negative in the post-hospitalization phase.
Indeed, standard operating procedures need to be in place to prevent possible infection of other patients and/or the lung function technician. Some experts questioned whether local infection control protocols would allow measurements of respiratory function to be obtained.
should include measures of exercise capacity at 6-8 weeks following hospital discharge.
Rationale. Whilst the long-term consequences of Covid-19 are not fully understood, we know that the impact of an ICU stay for acute respiratory distress syndrome (ARDS) has a significant impact on physical function (30). Equally a protracted period of bed rest can have similar detrimental but partially reversible effects in chronic respiratory disease (31). There is some evidence that recovery in physical function is variable in ARDS survivors however the greatest recovery appeared to occur within the first two months (20). An objective measure of exercise capacity (31) is important to document the degree of disability, identify the limitations to exercise and form the foundation of a subsequent rehabilitation programme.
Results. Majority of the experts recommended strongly (61%) or conditionally (29%) for the follow up of a hospitalised patient with COVID-19 including measures of exercise capacity at 6-8 weeks following hospital discharge ( Figure 1H ).
Many experts considered the measurement of exercise capacity to be very important in COVID-19
survivors, but some experts believe that this measurement should be limited to patients who remain physically limited 6-8 weeks following hospital discharge and who are tested negative at the time testing the exercise capacity. Experts emphasized that assessors should be aware of the possible presence of cardiopulmonary sequelae. Some experts questioned whether local infection control protocols would allow measurements of exercise capacity to be obtained.
interventions at 6-8 weeks following hospital discharge (e.g., multiple treatable traits) should receive a comprehensive rehabilitation program, compared to no rehabilitation program.
Rationale. Existing data from survivors of viral pneumonias indicates the wide range of challenges that patients face (20, 24, 25). It is unlikely that a unidimensional programme of physical training will meet the needs of the Covid-19 survivor as they will exhibit multiple treatable traits that a comprehensive rehabilitation programme has the potential to modify favourably. There is a limited evidence base for pulmonary rehabilitation post H1N1-ARDS (32). The programme will potentially be wider in scope than current pulmonary rehabilitation programmes (33) to meet the needs of these individuals and consider the additional burden placed upon survivors as a consequence of this unique virus e.g. social isolation strategies and the associated emotional burden. Survivors may be of a different age group to the 'usual' pulmonary rehabilitation population and supporting a successful return to work will be important.
Results. Majority of the experts recommended strongly (70%) or conditionally (26%) for COVID-19 survivors with a need for rehabilitative interventions at 6-8 weeks following hospital discharge receiving a comprehensive rehabilitation programme ( Figure 1I ).
Many experts commented on the diverse needs of COVID-19 survivors, such that not all survivors will need a comprehensive programme. Some experts commented that a comprehensive rehabilitation programme may not be available in all locations during the COVID-19 pandemic. Rationale. For patients with COPD there is evidence to indicate that recovery after an admission is supported by a structured rehabilitation programme. We know this is both safe and clinically effective and is recommended in national and international guidelines (33, 34). The current guidance for routine post-exacerbation pulmonary rehabilitation is 4 weeks post discharge, however the recommendation to delay this until 6-8 weeks post discharge was based upon the following considerations; there is a lack of data about the decay of the levels of infection in the Covid-19 survivor, the data suggesting that at 2 months a proportion of physical recovery will have occurred (20) and we also know that is a challenge for services to recruit patients to a post exacerbation rehabilitation programme 4 weeks post discharge (35).
Results. Majority of the experts recommended strongly (70%) or conditionally (24%) for COVID-19 survivors with pre-existing/ongoing lung function impairment at 6-8 weeks following hospital discharge receiving a comprehensive pulmonary rehabilitation program consistent with established international standards ( Figure 1J ).
Experts recommended taking patient's individual needs and preferences into consideration when decision regarding comprehensive pulmonary rehabilitation programs are made.
11. The international Task Force suggests that COVID-19 survivors with loss of lower limb muscle mass and/or function at 6-8 weeks following hospital discharge should receive a muscle strengthening program, rather than no strengthening program.
Rationale. For patients with ARDS, prolonged stay in the ICU mostly including prolonged mechanical ventilation) is known to have significant impact on peripheral muscle function, reflected in a loss of muscle mass and power neuropathy and/or myopathy, that is better known as ICU-acquired muscle weakness (30), and occurs early on in the ICU stay (36). Equally, a prolonged period of bed rest can also have a significant effect in chronic respiratory disease (31).
The lack of peripheral muscle strength can severely compromise functional ability and should be evaluated and treated as indicated (33).
Results. Majority of the experts recommended strongly (80%) or conditionally (18%) for COVID-19 survivors with loss of lower limb muscle mass and/or function at 6-8 weeks following hospital discharge receiving a muscle strengthening program ( Figure 1K ).
Experts agreed that a muscle strengthening program was important to optimise recovery.
Moreover, muscle strength needs to be assessed prior to commencement, to enable accurate prescription and tailoring of the strengthening program.
mass at 6-8 weeks following hospital discharge should receive nutritional support rather than no nutritional support.
Rationale. It is well established that optimising caloric and protein intake is important to support recovery of functional muscle mass. The post-ICU COVID-19 survivor will face commonly reported problems with nutrition (e.g., loss of appetite, swallowing disorders) and the additional symptom of loss of taste (ageusia) and smell (anosmia) are now recognised symptom of COVID-19 (37). In general, for those with chronic respiratory disease weight loss and wasting of muscle and bone tissue may be induced or accelerated during severe acute exacerbations of respiratory disease requiring hospitalisation, due to the combination of malnutrition, physical inactivity, hypoxia, systemic inflammation and/or systemic glucocorticoids (38), this is likely to be mirrored in the COVID patient.
Results. Majority of the experts recommended strongly (43%) or conditionally (36%) for COVID-19
survivors with loss of lower-limb muscle mass at 6-8 weeks following hospital discharge receiving nutritional support ( Figure 1L ).
Experts stated that rebuilding muscle mass requires that nutritional support is combined with a training stimulus. Moreover, experts believed that nutritional support may be less well established in some centres and guidance may be needed from expert sources.
psychological distress (using questionnaires) at 6-8 weeks after discharge from the hospital should receive a formal psychological assessment.
Rationale. Common symptoms reported one year later by ICU survivors, including patient with ARDS, include anxiety (34%), depression (33%) and post-traumatic stress disorder (19%) (39).This is compounded for the post COVID-19 survivor by the emotional stress associated with social isolation from family and friends for a protected period of time as a consequence of government lockdown policies. There are questionnaires recommended in the core outcome data set that cover these aspects of anxiety and depression, alongside PTSD (27). It is also acknowledged that the emotional burden of COVID-19 is likely to extend beyond the individual to family and friends (40).
Results. Majority of the experts recommended strongly (71%) or conditionally (24%) for COVID-19 survivors with symptoms of psychological distress at 6-8 weeks after discharge from the hospital receiving a formal psychological assessment ( Figure 1M ).
Experts believed that symptoms of anxiety, depression and PTSD occur commonly in persons after a major life event. Therefore, screening and monitoring of the course of symptoms of psychological distress is important. Experts also emphasized that those patients who show high level of anxiety or depressive symptoms needs to be referred to psychologist or psychiatrist for further assessment, and treatment may be indicated when symptoms continue to exist after 10-12
weeks. Psychological assessment and support for the family of the infected patient was also emphasised by the experts.
The present study provides consensus-based suggestions for the screening and the rehabilitation process during and after a hospital admission for severe COVID-19 infection. Experts reached consensus based upon indirect evidence and non-systematic clinical observations (i.e., clinical experience) on the need for early rehabilitation during the hospital admission, the screening for treatable traits with rehabilitation in all patients at discharge and 6-8 weeks after discharge, and around the content of rehabilitation for these patients. In absence of a formal evidence-based approach, these findings provide interim guidance for referral and multidisciplinary rehabilitation in a subgroup of patients after hospital admission. Altogether the data cast a strong claim on the need for screening and rehabilitation options for patients who were hospitalized. Besides lung function testing (e.g., spirometry, whole-body plethysmography and carbon monoxide transfer factor) (41, 42), this screening should also contain at least an exercise test (cardiopulmonary exercise test, 6-minute walk test or shuttle walk test), muscle strength testing and patientreported outcome measures (19, 43-46). This cannot be ignored by health care systems organizing the care around this pandemic respiratory infection. It should be noted that several experts identified that during the pandemic there has been an absence of rehabilitation options for patients that suffered from COVID-19 .
Early mobilisation and re-engagement in physical activity is important in the prevention of systemic consequences of a critical care and hospital admission. Whenever possible, patients should re-engage in physical exercise tailored to their possibilities. In patients suffering from COVID-19 such early interventions have to be balanced with the critical illness of the patient and the availability of personal protective equipment (PPE) for care givers engaged in the early mobilization protocols (5, 6, 47) . Where rehabilitation staff are not available or cannot access PPE, some rehabilitation tasks at the bedside may be provided by other members of the multidisciplinary team, with appropriate instruction. At discharge from the hospital experts advise a first screening, particularly to investigate the need for oxygen supplementation, in order to guide the first weeks post discharge. Patients may still be infectious (48, 49), which may complicate testing outside the patient room. A one-minute sit-to-stand test has been proposed as a way to evaluate hypoxia on exertion in the patient's room as an alternative to a six minute walking test (50), but needs further validation.
After discharge, patients with COVID-19 should be encouraged to do low/moderate intensity physical exercise at home in the first 6 to 8 weeks. Usually, these tasks range between 1.5 and 6 metabolic equivalents. Please see Ainsworth and colleagues for numerous examples (51, 52).
Moreover, the guidance provided by the ATS/ERS statement on pulmonary rehabilitation (33) may serve as a good framework. In this statement, pulmonary rehabilitation is defined as : "… a comprehensive intervention based on a thorough patient assessment followed by patient-tailored therapies, which include, but are not limited to, exercise training, education, and behaviour change, designed to improve the physical and psychological condition of people with chronic respiratory disease and to promote the long-term adherence of health-enhancing behaviours." Experts seem to agree that this definition also applies to the patient that suffered from severe COVID-19. Clearly there is a need for physiologic (statements 2, 5, 7, 8, and 11), psychologic (statements 5, 6, and 13) and nutritional (statement 13) assessment. For some patients there is a need for an individually tailored rehabilitation intervention (statement 9) and in the case of a pre-existing of remaining respiratory deficit, a pulmonary rehabilitation program (statement 10). Pulmonary rehabilitation programs are indeed well equipped to service this group of patients. Adaptations may need to be made to the rehabilitation program if the program typically deals with patients with obstructive lung disease to cater more to patients with gas exchange abnormalities. The self-management or education modules may also need to be adapted. It is expected that many patients that suffered from severe COVID-19 and particularly those with an ICU admission will have significant skeletal muscle weakness. Following muscle strength testing (46), s specific skeletal muscle training programs, typically offered with resistance training, are advised by experts. This is also the case in conventional pulmonary rehabilitation (53).
To date no prospective studies exist in COVID-19 patients on the proportion of patients in need of some form of (multidisciplinary) rehabilitation. However, symptoms like fatigue and dyspnoea still occur frequently about 30 days after discharge from the hospital, and are accompanied by reduced quality of life in about 40% of the COVID-19 patients (19). In some cases, the program offered could be outside the pulmonary rehabilitation setting. Indeed, early studies from China and confirmed later (54) indicated that >30% of patients suffered from some neurologic and neuromuscular sequelae (55). It is yet unknown how much of this recovers spontaneously. The progression of functional, skeletal muscle and mental health status after an admission for COVID-19 is not yet well described yet. Nevertheless, observational studies after SARS (56) or MERS (57) report an impaired 6-minute walk distance in 18% of the patients, and 43.6% had psychologic comorbidity. Hence health systems need to prepare to accommodate an increased number of referrals.
The exact proportion of COVID-19 patients requiring rehabilitation are difficult to predict, but assuming that patients who received mechanical ventilation would be a minimum set of patients that require rehabilitation post discharge may provide a conservative estimate of the number of new rehabilitation cases. Taking the ISARIC, UK based database as an example, 10% of hospitalised patients required mechanical ventilation (58). In a US (New York) based cohort 23% of patients requiring mechanical ventilation (59). Unfortunately large proportions died in the ICU (e.g. up to 60% in a study from New York, similar numbers in the ISARIC cohort), still rendering 40% of patients admitted to ICU as minimal numbers of new candidates for multidisciplinary rehabilitation, representing 5 to 10% of patients referred to hospital. Likely, a fraction of patients not mechanically ventilated (also including patients on high-flow oxygen therapy) will need to be added, as some of these still have significant functional consequences of the hospital admission An issue not resolved, but of importance to the organisation of rehabilitation for these patients is the duration patients should be considered as infectious. There is currently no consensus on how long patients should be self-isolating. Local infection prevention recommendations should be followed and this may require significant adaptation of the rehabilitation program with for example the adoption of 'tele-rehabilitation' (61). The task force has adopted a 6-8 week time window for reassessment. At this time point (and likely even sooner) many patients will be considered non-infectious (48, 49, 62).
A last point of attention is that despite the robust opinion in favour of rehabilitation after severe COVID-19 disease, these patients may be difficult to reach. Unfortunately several factors may preclude referral or uptake of rehabilitation. An important element that may impair uptake of rehabilitation is that at a population level rehabilitation might be hampered by pre-infection risk factors to be admitted to hospital with COVID-19, which include: having obesity, smoking and living an inactive life style (63). Moreover, it is known that COVID-19 disproportionately affects disadvantaged communities (64), many of whom have poor access to rehabilitation (65). These factors are known to impair uptake of rehabilitation. The offer for rehabilitation therefore need to be made to patients in a personalised and targeted manner, to maximise the likelihood of acceptance.
While the present expert opinion paper followed rigorous methodology to reach consensus, and consensus was reached on all questions, some remarks need to be taken into account. It would be good to offer respondents the option of no response, as respondents may feel that they do not have adequate expertise to respond to a question or they may not understand the question wording. Indeed, some experts stated that there were composite questions, combining a question about the content of care with a question about timing. Moreover, sometimes questions may not have been very specific (e.g. 'measures of respiratory function', 'measures of exercise capacity', 'comprehensive pulmonary rehabilitation program' or 'nutritional support'). Please see online Table 2 for all details. This may complicate interpretation of survey responses. We have taken, where possible written comments of the respondents into account. The current methodology also has strengths. It is fast and provides an interim guidance when randomized controlled studies are not yet available. Moreover, the current sample experts came from all over the world and had a diverse professional background, including medical but not limited to medical specialists, physiotherapists, nurses and psychologists.
To conclude, this multinational task force recommends early, bedside rehabilitation for patients affected by severe COVID-19. It advocates for assessment of oxygen needs at discharge and more comprehensive assessment of rehabilitation needs including physical as well as mental aspects 6-8 weeks after discharge. Based on the deficits identified multidisciplinary rehabilitation should be offered with attention for skeletal muscle and functional as well as mental restoration. The model of pulmonary rehabilitation may suit as a framework, particularly in a subset of patients with preexisting or COVID-19-induced long-term respiratory consequences. 
Patients with COVID-19 should be encouraged to do regular daily activities in the first 6-8 weeks after hospital discharge 4. Patients with COVID-19 should be encouraged to do low/moderate intensity physical exercise at home (rather than high intensity physical exercise) in the first 6-8 weeks after hospital discharge, if a formal exercise assessment with measures of exertional desaturation has not been conducted. 5. Patients with COVID-19 should have a formal assessment of physical and emotional functioning at 6-8 weeks following discharge, to identify unmet rehabilitation needs. 6. Follow up of a hospitalised patient with COVID-19 should include the core outcomes set for survivors of acute respiratory failure at 6-8 weeks following hospital discharge. 7. Follow up of a hospitalised patient with COVID-19 should include measures of respiratory function at 6-8 weeks following hospital discharge 8. Follow up of a hospitalised patient with COVID-19 should include measures of exercise capacity at 6-8 weeks following hospital discharge 9. COVID-19 survivors with a need for rehabilitative interventions at 6-8 weeks following hospital discharge (e.g., multiple treatable traits) should receive a comprehensive rehabilitation program, compared to no rehabilitation program. 10. COVID-19 survivors with pre-existing/ongoing lung function impairment at 6-8 weeks following hospital discharge should receive a comprehensive pulmonary rehabilitation program consistent with established international standards, compared to no pulmonary rehabilitation program 11. COVID-19 survivors with loss of lower limb muscle mass and/or function at 6-8 weeks following hospital discharge should receive a muscle strengthening program, rather than no strengthening program 12. COVID-19 survivors with loss of lower-limb muscle mass at 6-8 weeks following hospital discharge should receive nutritional support rather than no nutritional support. 13. COVID-19 survivors with symptoms of psychological distress (using questionnaires) at 6-8 weeks after discharge from the hospital should receive a formal psychological assessment. 
Comments Rehab (or part) should be installed as soon as possible to prevent avoidable impact of physical inactivity. Recommendation similar to other critically ill patients as long as possible to do in a safe manner for the rehab professional As the acute pathology of these patients continues to be elucidated, I would be cautious regarding the amount and intensity of any exercise intervention in the acute setting. I am primarily thinking of the findings of significant vascular compromise both in the lungs and in other end-organs including the brain-these patients may behave much more like our pulm HTN patients and therefore recognition and ability to treat and react to decompensation will be crucial authors need to define rehabilitation and state of patient Case-by-case decision balancing severity of symptom presentation with safety in the form of appropriate PPE available for the caregiver. Currently available research supports early intervention for mobilization of critically ill patients to avoid progressive muscle weakness, loss of bone density, and facilitate airway clearance and breathing mechanics. Depending on the rehabilitation. Passive mobilization for sedated patients seems not recommended but all the other rehabilitation are strongly recommended Depends on the definition of 'rehabilitation'. All patients should have assessments of their function and have appropriate physiotherapy with the aim of discharge (including early mobilisation in critical care).
If this is referring to exercise training then there isn't a positive evidence base to support this in other conditions. It would be reasonable to discuss a discharge recovery programme. There are decades of critical care research in ARF and ARDS that should inform care of COVID19 cohorts (given they can present to ICU with ARF and ARDS).
High risk for disease transmission, especially in settings of limited PPE. I agree only if the therapist is sufficiently safe from infection. If you do not activate those patients at/around the bedside, it would be critical to discharge them safe and quick to home environment. If those patients get home, they have to do more than they were used in the hospital. Individually adjusted It is important to evaluate each patient and devise a treatment plan that is according to their need. As the evidence for specific intervention for the COVID-19 patients is not entirely clear at this stage. Lack of any rehabilitation poses dire risk of severe decline in functional status for hospitalized patients; those who require ICU care; especially those who require prolonged sedation, mechanical ventilation and/or neuromuscular blockade and/or who receive systemic corticosteroids are at major risk of critical illness neuromyopathy. As such, provision of rehabilitation as able during the hospital stay is of major importance.
The basis of my conditional recommendation for hospital based rehab pertains to safety issues for patients and staff:
Issues are:
1. adequate PPE is needed for provision of rehabilitation to patients infected with COVID 19 and there is as yet no clear data to guide the level of risk to healthcare workers of acquiring COVID-19 from delivering PT to these persons 2. adequate testing should be available for healthcare professionals who do provide rehab to patients infected with COVID 3. safety of providing rehab to people with severe respiratory involvement (pneumonia and/or ARDS) from COVID with severe hypoxemia and/or other cardiovascular or neurologic manifestations of COVID is not clear--in particular, the risk of clotting (micro thrombosis and venous thromboembolism) is a concern (in terms of PE, MI, stroke and limb ischemia risk). Important that we DO NO HARM, and the risks of rehab in this population as compared with risks for non-COVID hospitalized patients is unclear at present. 4 . Also unclear if there is any "threshold of illness severity" or any particular features of illness related to COVID which poses greater risk of patients undertaking rehab during hospitalization
Rehabilitation is recommended only when the patient tolerates the activities and exercises that are administered, mainly in symptoms and physiological variables.
Severaly or critically ill patients should not receive ICU pulmonary rehabilitation, https://pubmed.ncbi.nlm.nih.gov/32251002/. in addition, an increase in biomarkers of cardiac injury has been documented https://pubmed.ncbi.nlm.nih.gov/32252591/ .
Activities such as positioning and early mobilization would be recommended depending on the stability of the patient Some patients would benefit from specialised equipment that would require them to leave their bedside.
The rehab has to be applied safety.
There are some definition issues here as to whatconstitutes PR in this location. I think a modified program is of value. The issue of course is PPE for staff and to what extent patients are treated individually versus in a class. Use of personal protective equipment is an absolute necessity for direct patient care. Acute care may be limited to prone positioning, and passive and active early mobilization if the patient is hemodynamically stable, and the level of sedation permit to apply. Acute care include direct patient contact.
For relatively less ill patients who are relatively active, are able to perform self care activities, being active and mobilization may be adequate. Those patients may do light activities in and around the bed under supervision, if possible using in hospital tele-health options, and leaflets may be given. We have sepsis data WBV seems to be safe
Prior to hospital discharge, should hospitalised patients with COVID-19 have an assessment of oxygen requirements at rest and during exertion?
Comments early insights indicate that an oxygen transport deficiency is present in many patients in the recovery phase and is not always accompanied by dyspnea. Some patients show severe desaturation during exercise of only moderate intensensity
In my opinion NOT ALL patients should be assessed of Oxygen requirements at rest and during exertion. Only on indication Will split response 1) all patients should have a daily assessment of resting oxygen saturation prior to discharge
Pre-discharge ambulatory oxygen assessments are a difficult issue where practice varies internationally even in COPD.
Many hospitalised patients with COVID19 will have exertional hypoxaemia pre discharge even if resting oxygen saturation is reasonable (and many clinicians have lowered reasonable to be 92-94% on air) but this will likely recover. More important that this is reassessed after discharge.
My personal opinion is that post-hospital ambulatory oxygen should only be prescribed where symptoms (exertional breathlessness) are preventing discharge (not degree of exertional hypoxaemia -where events related to hypoxaemia are extremely low) and supplemental oxygen appears to help. Another caveat would be if there is an underlying condition which is complicated by the hypoxaemia such as angina or cardiac arrhythmia.
Again some qualification is needed about 'assessment' -I am assuming this is referring to a standardised walking test on and off oxygen.
evidence that patient do not report feeling unwell despite having low sats and there is an increase in the incidence of VTE in covid Assuming the patient presented with pulmonary symptoms.
There needs to be a distinction between those patients with underlying chronic respiratory diseases and those patients without the disease who contracted COVID-19. If those patients with chronic respiratory disease before admission had long term oxygen therapy then it is important to reassess their need for oxygen therapy. The re-assessment before discharge will help to increase or decrease their oxygen need. Those without respiratory disease, if they recover from the COVID-19, condition is stable they might not need an indepth investigation.
People from ICU suffer from sarcopenia, critical illness poöyneuropathia and respiratory insufficience-Although a reassessment will likely be necessary after 1 month.
I believe that step test is a good way to determine the assessment of O2. NOTT and BMR trials support supplemental oxygen for hypoxemic patients at rest. Supplemental oxygen is also recommended (and reimbursed by Medicare in the USA) for those patients who desaturate with activity below 85-88% SpO2.
This must be assessed prior to hospital discharge to prepare the COVID patient with needed equipment upon discharge home.
If possible should oxygen requirements both at rest and during exertion be assessed. There is at the moment no standardised follow up plan i Norway and it may take quite a long time before especially exercise desaturation could be found. As far as I know has oxygen requirement at exertion not been performed. Maybe should the choice be "strong"..
This is more likely to occur throughout the hospital stay through regular nursing and physiotherapy assessments, rather than a specific assessment prior to hospital discharge. There will be patients however who need to have an assessment of oxygen requirements as a result of their COVID-19 diagnosis. assessment at rest: yes assessment during exertion: not standard Absolutely necessary since it depends on achieving mediumterm goals and being able to perform pulmonary rehabilitation with orientations to the needs of each patient. On the other hand, the information provided could be a predictor of morbidity and mortality, as in some cases of pulmonary fibrosis or pulmonary insterstitial disease.
Suggest to assess if they respond to oxygen during exertion. Those who respond positive may be discharged with oxygen to use during exertion. However, close monitoring is needed to assess whether the patient may have requirements of supplemental oxygen.
A follow-up assessment on the re-evaluation of oxygen requirement should also be scheduled with Hospital discharge because it might be assumed that many COVID patients might need supplemental oxygen only on the short-term but not on the Long-term.
Should patients with COVID-19 be encouraged to do regular daily activities in the first 6-8 weeks after hospital discharge?
Restart physical activity as early as possible may positively affect functional recovery. A problem in this respect is however the frequently observed desaturain on exertion of even moderate intensity. Therefore, patients should be given good personalized advise on discharge from the hospital on the intensity of the activities.
Advice to slowly regain regular daily activities are recommended but this should go along with the advice to take time for recovery and rest periods hall mark for pulm rehab once safe to be sent home assists in clearing of the lungs, quality of life and endurance and function With physical distancing.
I agree there is evidence from the published literature regular daily activities e.g. regular walking has potential benefits for patients with chronic respiratory diseases. Rule out that cardiac problems occured Question way too vague to complete this item.
Disease severity
Definition of regular daily activities --depends on patient's usual, occupation demands etc.
Borg level three of exertion , therefore unlikely to return to complete normal activity but need a routine program Yes modified to enhance mobilization- It maybe that high intensity exercise is not achievable due to post-COVID muscle fatigue etc, but I wouldn't make the caution about high intensity to be around hypoxaemia.
For clarity, agree with recommendation about low/moderate exercise during recovery until safety assessment (it is the issue about exertional desaturation driving my recommendation 'against') only if too frail or old to sweat effiently
The risk of deterioration is greater without low to moderate exercise than it is to do the exercise without formal assessment. Symptom-limited recommended. Should Be Seen at least by GP in advance Again -vague question. Need to define intensity. We are finding very high perceived exertion levels (one measure of intensity) at low MET levels with some patients (another measure of intensity).
We might be placing an unecessarily high value on formal assessments especially at this point. If the initial goals are improvements in peripheral muscle function as well as general mobilization I would be comfortable proceeding with exercising to symptom limitation-provided the therapist had experience in PR. However, there is no reason not to provide the patient with a simple finger pulse oximeter to know baseline and exercise saturation profiles. This might be more important post COVID because of the oxygenation profile.
Considering the virus dissemination and the social restriction, I believe that they have to wait more than a moth after hospital discharge to start exercise at home.
All patients need guidance about the intensity, frequency, and type of exercise to do at home following discharge from the hospital after a major pulmonary insult. Without professional guidance and parameters, patients are often afraid to proceed with activity; consequently, weakness, sedentarism, and a risk of hospital readmission may occur.
This depends on the status of the patient. Even after hospital discharge the severity and impairment vary largely among COVID-19 patients. Some have been in the intensive-care unit for weeks and are highly impaired while some are in relative good status. For the latter, low/moderate-intensity physical exercise could be done without measures of exceptional desaturation. However, in more severe patients information on desaturation during exercise is more important. Depends upon the severity of the illness and the premorbid condition of the patient e.g. if elderly and already have significant mobility limitations there will be little likely gain from formal evaluation of physical function This would seem a sensible time frame to balance natural recovery but not leaving things too long before intervention to intervene where needed. However, by formal assessment I would advice standardised phonecall first to understand ongoing symptoms, mental health issues, lifestyle issues etc as a triage and then 'formal' assessment for those where a deficity in physical or emotional functioning is detected.
This is a composite question. The first part is about need for formal assessment and the second is about timing. This may complicate interpretation of responses to this survey. Some may agree with formal assessment, but not agree with the proposed timing.
The impact of COVID-19 on patients with chronic respiratory diseases could be detrimental especially coping aftermath (admitted to the hospital). We know from the published literature COPD patients experience high level of anxiety and depressive symptoms during hospital admission. Thus, it is important to assess their psychological, emotional, cognitive, and psychosocial needs in their daily activities. This is particularly important for COVID-19 patients.
Assess other aspects that may have been missed early (emotional , cognitive , fatigue , myalgia etc)
Definitely. Based on earlier post ICU studies (Recover Program NEJM) we can expect both to be affected. We tend towards the easier for us -namely physical dysfunction but should be equally available for the emotional needs.
After a this time, I believe that we need to assess functional capacity and determine the exercise intensity for supervisioned or non supervision rehab.
At this point, patients who have had guidance to initiate low to moderate level activity during the first 6 weeks following hospitalization, are usually ready to increase the intensity of a supervised exercise program. This program should include education, assessment of psychosocial status, and monitored strengthening, flexibility, and aerobic exercise.
I think it should be better also a quick evaluation at hospital discharge ( before the 6-8 weeks) in order to address patients to right setting ( home or rehabilitative enviroment)
It is highly important to have a thorough assessment in order to individualize rehabilitation needs This does not routinely occur for post-ICU cohorts but may be an important part of post-ICU care -but again I'm not sure COVID19 patients ought to be treated differently from other ICU survivors because there is a risk of losing all the valuable research that has occurred in this setting. Based on this prior literature (e.g. Post-Intensive Care Syndrome), there may also be other important domains for assessment at 6-8wks e.g. cognitive function, return to work etc.
We need to identify at discharge the patients Who need this assesment at 6-8 weeks Recommend 6-8 week (telephone/video) review to screen / triage, then more structured physical, functional and psychological review at 12 weeks.
Only an assessment if they say that they still have physical of emotional problems. Or if the physiotherapist of doctor thinks it is necessary.
The evidence for other like-conditions indicates long term physical and emotional issues as a result of the illness -this could be improved for COVID-19 if these assessments took place.
We need to have measure to evaluate the effectiveness of the COVID-19 rehabilitation and it is important for the longitudinal follow-up, also.
The recommendation will depend on the conditions of the pandemic in each country, and the mobility and safety restrictions for patients; During the first few weeks there could be a risk of complications if the patient had a prolonged ICU stay (as shown with COVID patients). If the conditions are met patients with clinical or imaging evidence of sequelae should be prioritized https://pubmed.ncbi.nlm.nih.gov/32227758/.
Telephone strategies should be taken into account for those that still showing deficits, functional limitation and or tolerance Given the existing literature and evidence base regarding prolonged manifestations of critical illness, I think survivors of COVID 19, particularly those who have had illness severe enough to receive care in the ICU (with or without mechanical. ventilation), are likely to have some quite prolonged changes in physical, emotional and/or cognitive function; it will be important to routinely assess this to guide optimal strategies for rehabilitation.
There may be some restrictions related to activity level at this stage. If there is a possibility for close contact use of personal protective equipment may be required. Assessments requiring light efforts may be performed. Absolutely necessary.
Should follow up of a hospitalised patient with COVID-19 include the core outcomes set (e.g., EQ-5D, Hospital Anxiety and Depression Scale, Impact of Events Scale-Revised, PMID: 28699762) for survivors of acute respiratory failure at 6-8 weeks following hospital discharge?
Comments I'm not an expert, but my feeling is that a more generic instrument on physical functioning for example SF-36 together with the EQ-5D could give a more comprehensive picture of the consequences.
Instead of the IES-R, the PC-PTSD-5 , a brief screening questionnaire should be used to evaluate symptoms of PTSS 6-8 weeks may be too soon for IESr as PTSD often does not show early so it can be done at this time point but should also be done at 12 months. HADS is important and I would echo thoughts for EQ-5D as above -repeat at 6 and 12 months Public healthy questionnaire 9 is recommended by mental health professionals to replace HADS EQ-5D -yes
Need an assessment of exertional breathlessness -MRC dyspnoea scale as a minimum I don't have experience with the impact of events scale (aware of COMET) mood disorder and ptsd is common (occurs up to 1/3) in patient in critical cre This comment is from Dale Needham who is first author of the paper mentioned below.
I think we need to separate out the recommendation for type of outcome assessment and the timing. For instance, some people may agree with the measurement instrument, but not with the proposed timing. This question is worded as a composite recommendation which generally should be avoided in these types of consensus/survey questions.
Moreover, i think you are trying to cite the Core Outcome Measurement Set paper in AJRCCM, but i tihnk that the PMID, above, is not correct. Don't you mean: I agree with the suggestion to use outcome measures proposed to use in the follow-up patients at 6-8 weeks. I also wonder to include a scale that include 'fear' and 'stress' for patients with respiratory diseases. These are big problems often overlooked by healthcare professionals. I know the Depression Anxiety Stress Scale (DASS-21) measure has been used in patients with respiratory disease e.g. COPD. This might be a potential scale to include in the recommendation. Administering these outcome measures will help to identify the patients' need in order to direct, plan and devise appropriate interventions and resources to the patients and their caregivers especially for older people
Outcomes are important. The exact choice of which represent "core" will vary and should be allowed to do so, with local modification of test selection based on experience and data collection.. For sure! This was rigorously conducted research so yes, important to use this research and avoid research waste! Again is the assesment at discharge that drives the following steps Yes recommend bit at 12 weeks.
Yes EQ-5D and measures for anxiety, depression and post traumatic stress, in UK often use GAD-7 and PHQ-9. The follow up can be done by the hospital or by the other medical care providers. Not every patient with COVID-19 was hospitalised.
It is very useful. it would be necessary to consider the execution of selfdirected questionnaires also need objective physical measures as well to fully understand recovery This is a likely useful starting point to assess patients who have survived acute respiratory failure. Additional, novel outcomes may also be important to add given the spectrum of manifestations of COVID-19 and the potential for unique challenges related to rehabilitation for and recovery from it.
Absolutely necessary I believe this should also be done further out to 3/6/12 mo If those measurements are of relevance for this Group of patients.
Should follow up of a hospitalised patient with COVID-19 include measures of respiratory function at 6-8 weeks following hospital discharge?