Disclaimer: Given that the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2, which causes Covid-19) is a novel coronavirus, etiopathology of Covid-19 remains incompletely understood, as do the long-term consequences and recovery from the disease. It is important to note that the current approaches to care described below are based on treatments extrapolated from diverse underlying health conditions and that the literature on this topic is evolving rapidly.

The focus of the initial response to Covid-19 has been saving lives. Rightly so; be it in the hospital and ICU or preventing transmission and developing treatments or vaccines. For the majority, (81%) (1), infection with the Covid-19 virus will confer a mild to moderate disease; however, for a significant minority, the infection may have very serious consequences. In those patients requiring hospitalisation, a relatively high proportion (20.3%) have required management in an ICU environment, the most common reason being the development of acute respiratory distress syndrome (ARDS) (32.8%) (2). Less commonly, patients may develop acute liver injury, acute cardiac injury, acute kidney injury, and viraemic septic shock (3). The leading cause of death following Covid-19 is acute respiratory failure, and disseminated intravascular coagulopathy has been reported in 71% of non-survivors (3).

Rehabilitation is a core component of patient-centred care in responding to disasters. Rehab professionals and facilities will play an important role in helping speed the recovery of those survivors with residual impairments after ICU treatment, and also a critical role in providing an appropriate outlet for acute services, creating space for newly affected patients to receive the acute care they need (4). Ideally rehabilitation should be routinely incorporated into pandemic response plans early on, rather than in retrospect only after widespread disability becomes apparent (4).

Early intervention for successful rehab is key. Many patients will not have had access to this owing to fears of infection/reinfection and lockdown status in their area. Patients who have been hospitalised may have had respiratory therapy with a physical therapist. But has their care continued since discharge? What about the millions of mild to moderate cases of Covid-19 survivors who weren’t admitted to hospital? They too will have residual lung tissue damage with reduced exercise capacity, which could affect their lifestyle and workability in the future. Our knowledge of the range of impairments and disabilities is still evolving; however, Covid-19 is a multisystemic condition and some of the effects will be long-lasting (5,6). A third of patients being discharged from hospital require assistance in activities of daily living and a similar proportion have significant neurological sequelae (5,6). Physical therapy can mediate the deleterious pulmonary, respiratory and immobility complications that are common. Moreover, sports rehabilitation can offer a cost-effective strategy that can restore physical activity capacity, as well as mental and emotional quality of life (6).

Persistent mental health impairment is commonly described following treatment in the ICU, with pooled estimates reporting high prevalence rates of depression (29%), PTSD (22%) and anxiety (34%) affecting survivors at 1 year (4). Beyond this, pandemics are associated with high levels of emotional distress across society (4). On the individual level, dyspnoea is generally recognised as a distressing experience in its own right (4). For patients and families, admission to hospital with a Covid-19 diagnosis may raise fears for survival. So, for any patient recovering from Covid-19, no matter the severity, we must be cognisant that sports rehabilitation will not only be for the physical health of the individual but psychological and social too.

Owing to the diversity in potential conditions that could result from Covid-19, sports rehabilitation will have to be tailored depending on the needs of each patient. Cardiopulmonary rehabilitation including respiratory exercises and a graded exercise routine will be required for most patients. However, hands-on specialist care for patients recovering from any neurological deficits, severe weakness acquired from prolonged bedrest may be necessary. Awareness of chronic pain syndromes and chronic fatigue syndrome (CFS) should be kept in mind, as these biopsychosocial conditions may evolve as a consequence of survival.

As we have needed an army of medical personnel to get through the acute phase of this virus, so too will we need a team of sports rehabilitation specialists to ensure a successful long-term outcome. That team will potentially comprise physicians, psychiatric and neuropsychiatric support, rehabilitation nursing, physical therapy, occupational therapy, clinical psychology/neuropsychology, speech and language therapy, dietetics and social work.

Modifications to Rehabilitation

Pulmonary rehabilitation (PR) is a first-line management strategy in patients with respiratory diseases as it reduces breathlessness, increases exercise capacity and improves health‐related quality of life (HRQoL). A small but significant increase in physical activity in patients with chronic obstructive pulmonary disease (COPD) has also been shown following PR (7,8). However, 8–50% of those referred to PR never attend, and 10–32% of those who commence do not complete the programme (9). Barriers to attendance and completion include difficulty accessing the programme, poor mobility, lack of transport and cost of travel (8).

Home‐based PR may overcome the barriers to attendance at a centre‐based programme and resolve some of the concerns regarding Covid-19 patients interacting with other people. One-to-one or group sports rehabilitation classes would be hugely beneficial to the patient provided that strict social distancing, the use of masks and sanitising procedures can be followed (10). Some of the interventions, including breathing exercises are aerosol-generating procedures, which pose a significant health risk to the professionals who treat patients, as well as a risk of spreading infection to others (10).

A recent study showed that supervised pulmonary telerehabilitation produced equivalent results to standard hospital-based group PR (7). More participants, however, completed the telerehabilitation, where better compliance may result in better outcomes over the long term. Previous clinical trials comparing standard PR versus online, web-based sessions have shown to be neither inferior nor superior to face-to-face therapy (11,12,13).

Therefore, in the context of the Covid-19 pandemic, virtual-care outpatient consultations may be preferable to face-to-face interactions for multiple reasons. Firstly, in order to take care of patients, healthcare providers must themselves be in good health – fear for your own (and your family’s) safety or exposure to Covid-19 is understandable. Secondly, from a patient, family and wider societal perspective, delivering healthcare in settings where groups of people gather, such as ‘waiting rooms’ or a group sports rehabilitation class, is actively discouraged for fear of further community spread. In this context, it is also possible that a healthcare provider may be carrying Covid-19 asymptomatically; in such a case the healthcare provider may then inadvertently become a ‘super spreader’ (4). Regular and repeated testing for Covid-19 will be necessary to support segregation (of those still positive, from those being negative) and it is essential that staff have access to all the necessary personal protective equipment to be able to treat patients safely (4,10).

Suggestions for your practice or clinic include the following.

1. Patients should be unaccompanied where possible. Family or friends are not to wait in a waiting area but remain in their vehicles or outdoors.
2. Appointments should be staggered, with 15-minute intervals between, to allow time to sanitise equipment and prevent congestion of people.
3. Therapists and patients should wear masks and practise social distancing where possible.
4. Temperature checks on arrival, as well as short questionnaire checking patients’ symptoms, should be done routinely.
5. Therapists and patients should hand sanitise on arrival.
6. Patients can bring their own linen or towels to use during treatment and take home for their own washing.
7. Each therapist should have their own designated working area or cubicle to avoid cross-over within the practice.

Virtual care circumvents these issues and allows personalised consultation and treatment via telephone, live internet connections, or via pre-recorded sessions for more generic materials. In some countries, well-developed, secure virtual-care platforms already exist; in others, media such as Zoom, Skype, Facetime and others may be suitable alternatives. You may be able to have a group sports rehabilitation class through a video conference or Zoom facility. Patients gain support and encouragement from each other (albeit through a screen), plus seeing others during this lonely time may boost morale. Additionally, having a set ‘appointment’ time may keep patients motivated to do their sports rehabilitation exercises. However, virtual care also has many limitations, such as availability of equipment, technical malfunctions, potential for inadvertent personal data disclosure, limited scope for physical examination, and the process largely relies upon the patient being able to attend sessions, handle the technology, communicate and interact accordingly. This may not be possible for all patients. Rehabilitation providers should start to consider the scope and limitations of virtual physical examinations and make patients expressly aware of this accordingly (4,10). Programmes already exist and are available online for cardiac rehabilitation (www.activateyourheart.org.uk) and COPD (www.spaceforcopd.co.uk) that may be beneficial to some patients.

Baseline Testing

There are many tests that can be performed to assess the pulmonary function and exercise tolerance of a patient recovering from Covid-19. As Covid-19 is such a complex disease, components of all aspects of a biopsychosocial model may need to be incorporated. These too may have to be selected depending on your and the patients’ access to clinics/hospitals and equipment for testing. Tests can form part of a baseline score from which PR can progress, as well as monitoring the improvement and motivating patients over the weeks ahead.

Specific strength tests or neurological assessment may be necessary for Covid-19 patients who may have suffered deep vein thrombosis, stroke or prolonged bed-rest in ICU, for example. The majority of patients may follow a form of graded PR programme, which physical therapists are familiar with. However, combining patients into different levels of ability/disability may be required if group sessions, be it face-to-face or online, are to be effective.

Tests may include:

1. Pulmonary Function Test

Spirometry [forced expiratory volume in 1 second (FEV1) and forced vital capacity (FVC)], diffusing capacity of the lung for carbon monoxide (DLCO) and static lung volumes by body plethysmography may be performed according to the guidelines (9,14,15). Lung disease severity of each patient can then be classified according to the Global Initiative for Obstructive Lung Disease spirometric criteria (16).

2. Exercise Test

Exercise capacity can be assessed by the 6-minute walk test (6MWT) (17), the incremental shuttle walk test (ISWT) and the endurance shuttle walk test (ESWT) according to standardised protocols (18,19,20,21). A primary outcome for patients may be endurance exercise capacity, measured by the ESWT. Modifications may be necessary for 6MWT as the distance recommended of a 30–45m long, straight course may not be possible depending on the patient’s location. This may become a 20m (or even less) distance along the lounge floor or corridor that the patient repeats loops of for the 6-minute duration. Provided the distance and space remains the same with each test/re-test, improvement can be monitored based on distance or number of laps in the given 6-minute time. Ideally two tests should be performed for each walk test over two visits/sessions within 7 days of each other, separated by at least 30‐minutes’ rest. The better test result can then be used in the baseline. SpO2 (peripheral capillary oxygen saturation) and heart rate (HR) should be monitored with a pulse oximeter, where possible. Dyspnoea and rate of perceived exertion should be assessed before and after each exercise test using the modified 0–10-point Borg category‐ratio scale (22). Reference values for the 6MWT are based on an Australian study of healthy individuals (23).

3. Quality of Life

The Chronic Respiratory Disease Questionnaire (CRDQ) can be used to measure HRQoL. The minimal important difference for the four domains in this questionnaire are 2.5 for dyspnoea, 2 for fatigue, 3.5 for emotional function, 2 for mastery and 10 for the total score (24).

4. Physical Activity

The use of smart phones, Fitbits, and watches with activity or fitness trackers that monitor step counts, calorie expenditure and activity levels can be helpful in recording and motivating a patient’s physical activity.

5. Physical Performance

Physical performance can be assessed by using the Functional Performance Inventory – Short Form (FPI‐SF) which evaluates the level of difficulty respondents have in six domains including body care (five items), maintaining the household (eight items), physical exercise (five items), recreation (five items), spiritual activities (four items), and social interaction (five items). For ease of use, activities assessed are organised according to these domains. For each item/activity, respondents are asked to rate how difficult the activity is for them to perform on a simple three-point scale: ‘no difficulty’, ‘some difficulty’, or ‘much difficulty’. If respondents do not perform an activity, they can select one of two options: ‘don’t do for health reasons’ or ‘choose not to’ (25,26).

6. Health Status

COPD health status can be assessed using the COPD Assessment Test (CAT) which quantifies the impact of COPD on well‐being (https://www.mdcalc.com/copd-assessment-test-cat) (27,28).

7. Dyspnoea

Dyspnoea can be assessed with the modified Medical Research Council (mMRC) dyspnoea scale (Table 1). The mMRC assesses dyspnoea as part of the BODE (BMI, airway obstruction, dyspnoea, exercise capacity) index which has been determined in this study (29). The MRC dyspnoea scale has been proven to be a reliable index of disease severity and health status in elderly COPD patients which should prove useful for remote monitoring of COPD and for rating health status for epidemiological purposes (30).

Table 1: Medical Research Council (MRC) and modified MRC (mMRC) scale and severity of dyspnoea (Sourced 30,31,32)

8. Psychological Status

Anxiety and depression can be measured using the Hospital Anxiety and Depression Scale (HADS) (33).

9. Self‐efficacy

The Pulmonary Rehabilitation Adapted Index of Self‐Efficacy (PRAISE) tool can be used to measure self‐efficacy (Fig. 1) (34,35).

Figure 1: Pulmonary rehabilitation adapted index of self-efficacy (PRAISE) tool [Vincent E, Sewell L, Wagg K et al. Measuring a change in self‐efficacy following pulmonary rehabilitation: an evaluation of the PRAISE tool. Chest 2011;140(6):1534–1539 (34)]

Exercise Training

Exercise training has been acknowledged as the cornerstone of a comprehensive PR programme 36). Eight to ten weeks of exercise-based PR can lead to clinically relevant improvements in daily symptoms (dyspnoea, fatigue, anxiety and/or depression), physical capacity, physical activity and quality of life in patients with COPD, without a significant change in the degree of airflow limitation. Indeed, if exercise training is lacking, there is no significant improvement in physical activity tolerance (36).

Most training studies focused on the effects of whole-body endurance exercise training (ie. treadmill walking and/or stationary cycling). Nevertheless, not all patients are able to exercise for a continuous period of 20 minutes or more at a training intensity of 60% or more of the predetermined maximal exercise tolerance (36). Therefore, many other exercise training modalities and settings have been studied, ranging from Nordic walking for patients with a relatively well-preserved exercise tolerance to neuromuscular electrical stimulation for the most dyspnoeic, weakened and perhaps even mechanically ventilated patients (36). Even though multiple training modalities and settings are available, a true personalisation of the exercise training based on the pre-rehabilitation assessment is often lacking. A one-size-fits-all approach is common practice, but may not be successful in the Covid-19 arena with such a range of ages, disease severity and comorbidities affecting patients’ rehabilitation.

Reasoning from traits that are modifiable during exercise training, there are multiple options. Resistance training (training small muscle groups at 70–80% of the one repetition maximum (1RM), 4 sets of 8–12 repetitions) should be considered for patients with lower limb muscle weakness/atrophy and a moderate degree of dyspnoea (mMRC 2) (36). For weakened patients with (very) severe dyspnoea, resistance training may still be too burdensome to their weakened ventilatory system, and neuromuscular electrical stimulation should be considered as a substitute for resistance training (36). Whole-body vibration has also been suggested as a useful means of increasing lower limb muscle strength but seems not to be used very often in daily clinical rehabilitation practice (36).

Whole-body exercise training can be considered for patients with a clear exercise intolerance.

1. Patients who are mainly restricted by reaching their maximal HR during the cardiopulmonary exercise test, should be offered whole-body exercise training (at 60% to 80% of the predetermined maximal cycling load/walking speed, for 20–30min), which can range from treadmill walking to stationary cycling, and outdoor walking, including Nordic walking, elliptical trainer (36).
2. Patients who are mainly restricted by the ventilatory system, should undergo a constant work rate cycling endurance test (CWRT) at 75% of the peak cycling load. If the CWRT lasts ≥10min, endurance training (starting at 60%) is still an option. If the CWRT lasts <10min, interval training (at >80% of the predetermined maximal cycling load/walking speed, for 30–60s per exercise bout, for 20 to 40 bouts) using treadmill walking or stationary cycling should be proposed. Interestingly, patients who cycle <10min also have weaker quadriceps muscle (36).
3. In turn, interval training should most probably be combined with resistance training.
4. The rehabilitation goals of the patient should be taken into the equation, as interval training matches to a greater extent the metabolic load of activities of daily living than endurance training (36).

Table 2: Example of conventional group pulmonary rehabilitation programme. Table first published as Supplementary Table 9 in Hansen H, Bieler T, Beyer N et al. Supervised pulmonary tele-rehabilitation versus pulmonary rehabilitation in severe COPD: a randomised multicentre trial. Thorax 2020;75:413-421 (7), republished here with permission.

Table 3: Example of telecommunication or group home based (using online conferencing facility) pulmonary rehabilitation programme. Table first published as Supplementary Tables 11, 12 and 13 in Hansen H, Bieler T, Beyer N et al. Supervised pulmonary tele-rehabilitation versus pulmonary rehabilitation in severe COPD: a randomised multicentre trial. Thorax 2020;75:413-421 (7), republished here with permission.

Suggestions for patient education topics in both group hospital/clinic/practice-based rehabilitation and individual or group home rehabilitation via online portal include (7):

1. welcome, individual introduction or presentation
2. Covid-19, the disease, treatment and management
3. early signs of exacerbation, chronic fatigue and action plan
4. medication, use of any devices, inhalers, oxygen support; breathing techniques
5. physical activity and exercise
6. food, nutrition and the importance for health and immune system
7. smoking cessation
8. anxiety, stress, depression
   • avenues for coping mechanisms, support, therapy and help
   • identify vulnerable individuals to refer for counselling, include education on relaxation techniques.

In all these education topics allocate approximately 20 minutes for information, discussion and reflection. A number of sessions may be required for each topic to allow adequate time for questioning and practising breathing/relaxation techniques for example.

A number of studies have been conducted comparing the traditional face-to-face PR to a home-based programme (8,11,12,13). The home-based programme can be delivered in a number of ways (real-time, online pre-recorded sessions, website based, telephone monitoring or interactive group video conferencing) all of which have been shown to improve exercise tolerance and physical activity capacity; this in turn improves patients’ symptoms of fatigue, dyspnoea and ability to carry out daily chores.

Some programmes run for 6 weeks whereas others for 10 or 12 weeks or even up to 4 months; you may choose to alter these timelines depending on the severity of the patient’s symptoms and their rehab progress. In addition to this there are many ways one can exercise at home or in a clinic depending on equipment available. Provided it has an element of cardiovascular endurance work and some strength training, sessions could include:

• A ‘basic level’ of the programme consisted of 15–25min of exercise with mini-ergometer without load and 30min of callisthenic exercises, performed three times/week and free walking twice a week. The ‘high level’ consisted of 30–45min of mini-ergometer with incremental load (from 0 to 60W), 30–40min of muscle reinforcement exercises using 0.5kg weights and pedometer-based walking, performed from 3 to 7 days/week (13).
• 10 exercises increased by 30 s, starting from 60s in week 1, to 3.5min in week 6. Exercises included biceps curls, squats, push-ups against a wall, leg extensions in a sitting position, upright row with weights, sit-to-stand, arm swings with a stick, leg kicks to the side, arm punches with weights and step-ups. Both the online and face-to-face programmes also included warm-up and cool-down sessions (11).
• Lower limb cycle ergometer, 15–20min at 60–80% of peak work rate estimated from the best 6-minute walk distance at baseline using an algorithm for cycle exercise prescription (37). Progressing in increments of 5W. Followed by 5min rest and a further 15–20min walking at 80% of best 6-minute walk test. Followed by 5min rest and strength training involving squats and sit-to-stand (3 sets of 10 repetitions each) (8).

Exercise monitoring and progression should be based on both the modified Borg dyspnoea (Table 4) and rate of perceived exertion 0–10 category-ratio scales (22, 38) with participants encouraged to exercise with symptoms between moderate to somewhat severe (a score of 3–4).

A simple visual analogue scale (VAS) consisting of a line, usually 100mm in length, placed either horizontally or vertically on a page, with anchors to indicate extremes of a sensation can also be used. The anchors on the scale have not been standardised, but ‘not breathless at all’ to ‘extremely breathless’; and ‘no shortness of breath’ to ‘shortness of breath as bad as can be’ are frequently used. Scoring is accomplished by measuring the distance from the bottom of the scale (or left side if oriented horizontally) to the level indicated by the subject. The reliability and validity of the VAS as a measure of dyspnoea has been reported (39).

If there are clear signs of exercise-induced oxygen-desaturation during the cardiopulmonary exercise test, the rehabilitation team may want to consider the use of oxygen supplementation during the whole-body exercise training, although its use has been questioned recently. Indeed, Alison et al. showed that a 10-week exercise training programme was safe and effective in patients with mild exercise-induced O2-desaturation who were training with oxygen supplementation or room air supplementation (40). SpO2 and HR can be monitored via the finger-tip pulse oximeter intermittently during training. If SpO2 falls below 88% and/or HR increases above 80% of predicted maximum HR (predicted by age) then participants should rest with the pulse oximeter continuing to record. Participants can resume exercising when the SpO2 reaches 88% or above and HR drops to below 80% of maximum predictedPhysiotherapy HR. Participants should be asked to report the pulse oximeter readings either by presenting it in front of the camera or by verbally reporting it to the physiotherapist supervising the session (8).

To prevent exercise-induced oxygen-desaturation, again, interval training should be considered. Moreover, patients with severely exercise-induced lung hyperinflation may be in need of ventilatory support during whole-body interval training. This can be provided using non-invasive ventilation (36). This requires fewer patients per therapist compared to ‘regular’ supervision of exercise training, which may be an organisational challenge. Obviously, the first step here is to teach patients to use pursed-lips breathing, which may partly prevent dynamic lung hyperinflation (36). Besides stationary biking (instead of treadmill walking), water-based walking seems also a valid option for patients with obesity and/or arthrosis of hip/knee/lower back.

To date, exercise training generally results in an improved exercise tolerance in patients with COPD and two-thirds of patients achieve a clinically relevant improvement in physical capacity (36). It is possible to consider that these benefits will be conferred to recovering Covid-19 patients. A further personalisation of the exercise training intervention(s) as part of a comprehensive PR programme may be required depending on the patient’s needs.

Respiratory Training

Following Covid-19 infection there appears to be residual alveolar damage and possible fibrosis of lung tissue, even after resolution of symptoms. This may result in long-term respiratory issues such as breathlessness or dyspnoea at rest or on exertion affecting a patient’s ability to carry out daily chores, work or physical activity. In a vicious cycle, reduced physical activity due to dyspnoea actually leads to increased symptoms of breathlessness owing to reduced exercise tolerance and muscle weakness. The difficulty is to motivate patients on the importance of exercise training when it is perceived to exacerbate their symptoms. Patients may be fearful, anxious, fatigued and have depression. Breathing exercises can address issues of panic, anxiety and depression as well as improve breathlessness by strengthening respiratory muscles.

As the result of peripheral airway obstruction, air may become trapped in the lungs (ie. hyperinflation). The respiratory rate may increase because of inspiration, which is initiated before emptying the lungs of air. Adjustment of rapid shallow breathing may lead to fatigue of the respiratory muscles. Hyperinflation may lower the dome of the diaphragm, shorten respiratory muscle fibres, and impair the possibility of muscle contraction. In addition, gas exchange may be inefficient. Hence, patients develop symptoms of breathlessness or dyspnoea (41).

Various breathing control exercises (BCEs) and respiratory muscle training (RMT) are being used to improve breathlessness. For example, BCEs include diaphragmatic breathing, pursed-lip breathing, relaxation techniques, and body position exercises. BCEs aim to decrease the effort required for breathing and assist relaxation by deeper breathing, which may result in an improved breathing pattern through decreased respiratory rate and reduced breathlessness (41,42). In regard to RMT, the aim is to improve muscle strength and endurance where the respiratory muscles are impaired, hopefully resulting in a greater ability to control the breathing pattern and reduce breathlessness (41,42). RMT requires a training programme using an adjusted breathing resistance device (41).

Active expiration is another exercise requiring contraction of abdominal muscles, increasing abdominal pressure during active expiration, which lengthens the diaphragm and contributes to operating the diaphragm close to its optimal length. In addition, active expiration increases the elastic recoil pressure of the diaphragm and the ribcage, the release of which after relaxation of the expiratory muscles assists the next inspiration (43).

A description of BCEs and RMT is shown in Figure 2 (41)].

Figure 2: Description of breathing control exercises and respiratory muscle retraining. Figure first published in Borge CR, Hagen KB, Mengshoel AM et al. Effects of controlled breathing exercises and respiratory muscle training in people with chronic obstructive pulmonary disease: results from evaluating the quality of evidence in systematic reviews. BMC Pulmonary Medicine 2014;14:184 (41) and reproduced under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0)

The goal of breathing or respiratory exercises should be to (42):

1. reduce dynamic hyperinflation of the ribcage and improve gas exchange;
2. increase strength and endurance of the respiratory muscles;
3. optimise the pattern of thoracoabdominal motion; and
4. induce psychological effects (such as controlling respiration) that might also contribute to the effectiveness of controlled breathing.

Fatigue

Fatigue is a symptom common to many illnesses, such as cancer, depression, autoimmune diseases, hormonal disorders and infections, and it is associated with poorer health outcomes. Most health conditions that cause fatigue, such as fatigue secondary to deconditioning, cancer and neuromuscular disorders, have aetiologies that are attributable to specific pathologies that may respond favourably to various forms of intervention, such as physical therapist management. However, some people may demonstrate fatigue related to causes that remain unclear. It is not clear or understood as yet, why many patients recovering from Covid-19 have reported fatigue. This may improve with time and simply be delayed symptom resolution. However, it is speculated that with the complex nature of Covid-19 (and the manner in which it attacks multiple systems within a patient’s body, combined with the psychological and social impact of the virus) persistent fatigue may become more sinister.

In clinical practice, many individuals presenting with the common symptom of persistent fatigue may benefit from activity-based behavioural interventions, as suggested by Friedberg et al. (44). However, persistent fatigue is not equivalent to the multisymptom debilitating illness of ME/CFS. Despite the lack of approved treatments or a fully articulated standard of medical care, there are still many actions physical therapists can take to help. Clinicians can help patients to better manage a major illness challenge: how to minimise debilitating post-exertional malaise by learning to stay within their ‘energy envelope’ (45).

The energy envelope delineates the amount of energy that a myalgic encephalomyelitis (ME)/CFS patient has available to perform all activities. The size of this energy envelope can vary from day to day and between patients, with some patients lacking energy for basic activities of daily living. When patients exceed their limited energy levels, they experience post-exertional worsening of symptoms and functioning. Medical providers can teach patients how to recognise their own personal energy limits and use ‘pacing’ (dividing symptom-producing activities into smaller parts with interspersed rest intervals) to stay within those limits (45,46). Once pacing is effectively used, some patients may be able to use an individualised exercise plan to increase available energy and functioning while avoiding post-exertional worsening (45,46).

Standard of care for ME/CFS has been cognitive behaviour therapy and graded exercise therapy (47). Both interventions had been recommended by the US Centres for Disease Control and the UK NICE guidelines. Multiple literature reviews have reported that these therapies are not only effective at improving fatigue and, to a lesser extent, physical function in ME/CFS but are also safe. It would seem obvious then that good clinical care of these patients would include these behavioural interventions (47). A paper by Davenport et al. illustrates pacing and load introduction/adaptation over time with CFS patients as well as ideas on graded exercise intervention (48).

A brief self-management intervention for patients with unexplained chronic fatigue or CFS appeared to be clinically effective for reducing the impact of fatigue on functioning (44). In the long term, however, using the guided exercise self-help booklet alone is unlikely to be adequate to support patients sufficiently. Additional guidance from skilled physio /health professionals who demonstrate an understanding of what it is like to cope with ME/CFS is also important (49).

Pharmacological interventions for pain and unrefreshing sleep can be prescribed. If needed, patients can be referred for counselling to improve coping with the severe impacts of ME/CFS on quality of life. Essentially, optimal patient care will require a multidisciplinary team.

Conclusions

Without a clear picture of exactly what each Covid-19 survivor will look like, it is hard to plan ahead to be fully prepared. Based on the pathophysiology of the virus and case reports of patients, it is reasonable to assume a degree of pulmonary, even cardiopulmonary, rehabilitation will be required together with breathing exercises. It will be critically important to be aware of the chronic manifestations of pain and fatigue and dealing with these complex biopsychosocial issues may require the involvement of a multidisciplinary team. In addition to this, patients may require specific musculoskeletal or neurological rehabilitation, so programmes will have to be tailored to the individual. Traditional therapy will need to be adapted to account for social distancing, lockdown regulations and fear of infection. These are unprecedented times; your requirement to deliver treatment to these patients is vital, while still protecting your health as a primary priority. Creativity may be the key word for long-term Covid-19 care.

Key Points

1. Rehabilitation is a core component of patient-centred care in responding to disasters, and early intervention for successful rehabilitation is key.
2. Our knowledge of the range of impairments and disabilities is still evolving; however, Covid-19 is a multisystemic condition and some of the effects will be long-lasting.
3. Physical therapy can mediate the deleterious pulmonary, respiratory and immobility complications that are common, as well as conditions arising from venous thromboembolism and the stress, anxiety and depression of having survived Covid-19.
4. Pulmonary rehabilitation (PR) is a first-line management strategy in patients with respiratory diseases as it reduces breathlessness, increases exercise capacity and improves health‐related quality of life (HRQoL).
5. Assessment may include 6MWT, ISWT, ESWT, FEV1, FVC, Borge scale of dynspnoea and Medical Research Council (MRC) dyspnoea scale, questionnaires for quality of life (CRDQ) and physical performance (FPI-SF), neuromuscular assessment, as well as psychological (HADS) and self-efficacy testing (PRAISE).
6. Exercise training has been acknowledged as the cornerstone of a comprehensive PR programme.
7. Whole-body endurance exercise training and strength training can be progressed over 6 weeks or more.
8. Supervised home-based PR has been proven to be equivalent in efficacy to traditional group clinic/hospital-based PR.
9. Various breathing control exercises (BCEs) and respiratory muscle training (RMT) are proven to improve breathlessness.
10. Modifications in PR delivery will need to be made accounting for social distancing, and lockdown regulations, including telerehabilitation, video conferencing and online portals.
11. With the complex nature of Covid-19, one should be aware of possible developments of biopsychosocial syndromes such as chronic pain and chronic fatigue syndrome.

Discussions

1. What are your thoughts or plans to make rehabilitation of Covid-19 patients safe for everyone involved?
2. How can you make pulmonary rehabilitation effective and fun to ensure participation, compliance and success even when performed in the virtual setting?
3. What other rehabilitation protocols do you feel will be beneficial for a Covid-19 survivor?

Quotations/Important Points

“For any patient recovering from Covid-19, we must be cognisant that rehabilitation will not only be for the physical health of the individual but psychological and social too”

“in the context of the Covid-19 pandemic, virtual-care outpatient consultations may be preferable to face-to-face interactions”

“breathing control exercises and respiratory muscle training can be used to improve breathlessness”

“Covid-19 survivors might experience persistent fatigue; this can often be helped with activity-based behavioural interventions”

“Treatment of the varied and complex conditions that a Covid-19 survivor might face may require the care of a multidisciplinary team”

References

1. Cascella M, Rajnik M, Cuomo A et al. Features, evaluation and treatment coronavirus (COVID-19). StatPearls Publishing 2020
2. Rodriguez-Morales AJ, Cardona-Ospina JA, Gutiérrez-Ocampo E et al. Clinical, laboratory and imaging features of COVID-19: a systematic review and meta-analysis. Travel Medicine and Infectious Disease 2020:101623
3. Beeching NJ, Fletcher TE, Fowler R. Coronoavirus disease 2019 (COVID-19). BMJ Best Practices 2020
4. Simpson R, Robinson L. Rehabilitation following critical illness in people with COVID-19 infection. American Journal of Physical Medicine & Rehabilitation 2020;doi:10.1097/PHM.0000000000001443 [Epub ahead of print]
5. Landry M, Tupetz A, Jalovcic D et al. The novel coronavirus (COVID-19): making a connection between infectious disease outbreaks and rehabilitation. Physiotherapy Canada 2020;doi:10.3138/ptc-2020-0019 [Advance online article]
6. Philips M, Turner-Stokes L Wade D et al. Rehabilitation in the wake of Covid-19 – a phoenix from the ashes. British Society of Rehabilitation Medicine 2020;1 27.4.2020
7. Hansen H, Bieler T, Beyer N et al. Supervised pulmonary tele-rehabilitation versus pulmonary rehabilitation in severe COPD: a randomised multicentre trial. Thorax 2020;75:413–421
8. Tsai LLY, McNamara RJ, Moddel C et al. Home-based telerehabilitation via real-time videoconferencing improves endurance exercise capacity in patients with COPD: the randomized controlled TeleR study. Respirology 2017;22:699–707
9. Standardization of spirometry, 1994 update. American Thoracic Society. American Journal of Respiratory and Critical Care Medicine 1995;152:1107–1136
10. Percy E, Luc JGY, Vervoort D et al. Post-discharge cardiac care in the era of coronavirus 2019: how should we prepare? Canadian Journal of Cardiology 2020
11. Bourne S, DeVos R, North M et al. Online versus face-to-face pulmonary rehabilitation for patients with chronic obstructive pulmonary disease: randomised controlled trial. BMJ Open 2017;7:e014580
12. Chaplin E, Hewitt S, Apps L et al. Interactive web-based pulmonary rehabilitation programme: a randomised controlled feasibility trial. BMJ Open 2017;7:e013682
13. Bernocchi P, Vitacca M, La Rovere MT et al. Home-based telerehabilitation in older patients with chronic obstructive pulmonary disease and heart failure: a randomised controlled trial. Age Ageing 2018;47:82–88
14. American Thoracic Society. Single‐breath carbon‐monoxide diffusing capacity (transfer factor). Recommendations for a standard technique – 1995 update. American Journal of Respiratory and Critical Care Medicine 1995;152:2185–2198
15. Blonshine S, Foss C, Ruppel G. American Association for Respiratory Care clinical practice guidelines: body plethysmography: 2001 revision and update. Respiratory Care 2001;46(5):506–513
16. Pothirat C, Chaiwong W, Limsukon A et al. Detection of acute deterioration in health status visit among COPD patients by monitoring COPD assessment test score. International Journal of Chronic Obstructive Pulmonary Disease 2015;10:277–282
17. Agarwala P, Salzman SH. Six-minute walk test: clinical role, technique, coding, and reimbursement. Chest 157(3):603-611
18. Singh SJ, Morgan MD, Scott S et al. Development of a shuttle walking test of disability in patients with chronic airways obstruction. Thorax 1992;47:1019–1024
19. Holland AE, Spruit MA, Trooster T et al. An official European Respiratory Society/American Thoracic Society technical standard: field walking tests in chronic respiratory disease. European Respiratory Journal 2014;44:1428–1446
20. Revill SM, Morgan MD, Singh SJ et al. The endurance shuttle walk: a new field test for the assessment of endurance capacity in chronic obstructive pulmonary disease. Thorax 1999;54:213–222
21. Agarwal B, Shah M, Andhare N et al. Incremental shuttle walk test: reference values and predictive equation for healthy Indian adults. Lung India 2016;33(1):36–41
22. Borg GAV. Psychophysical bases of perceived exertion. Medicine and Science in Sports and Exercise 1982;14(5):377–381
23. Camarri B, Eastwood PR, Cecins NM et al. Six minute walk distance in healthy subjects aged 55–75 years. Respiratory Medicine 2006;100:658–665
24. Guyatt GH, Berman LB, Townsend M et al. A measure of quality of life for clinical trials in chronic lung disease. Thorax 1987;42(10):773–778
25. Leidy NK, Wilcox TK, Jones PW et al. Standardizing measurement of chronic obstructive pulmonary disease exacerbations. Reliability and validity of a patient‐reported diary. American Journal of Respiratory and Critical Care Medicine 2011;183:323–329
26. Leidy NK, Hamilton A, Becker K. Assessing patient report of function: content validity of the Functional Performance Inventory-Short Form (FPI-SF) in patients with chronic obstructive pulmonary disease (COPD). International Journal of Chronic Obstructive Pulmonary Disease 2012;7:543–554
27. Gupta N, Pinto LM, Morogan A, Bourbeau J. The COPD assessment test: a systematic review. European Respiratory Journal 2014;44:873–884
28. Dodd JW, Hogg L, Nolan J et al. The COPD assessment test (CAT): response to pulmonary rehabilitation. A multicentre, prospective study. Thorax 2011;66:425–429
29. Celli BR, Cote CG, Marin JM et al. The body‐mass index, airflow obstruction, dyspnea, and exercise capacity index in chronic obstructive pulmonary disease. New England Journal of Medicine 2004;350(10):1005–1012
30. Paladini L, Hodder R, Cecchini I et al. The MRC dyspnoea scale by telephone interview to monitor health status in elderly COPD patients. Respiratory Medicine 104(7):1027–1034
31. Stenton C The MRC breathlessness scale. Occupational Medicine 2008;58(3):226–227
32. Hsu KY, Lin JR, Lin MS et al. The modified Medical Research Council dyspnoea scale is a good indicator of health-related quality of life in patients with chronic obstructive pulmonary disease. Singapore Medical Journal 2013;54(6):321–327
33. Dowson C, Laing R, Barraclough R et al. The use of the Hospital Anxiety and Depression Scale (HADS) in patients with chronic obstructive pulmonary disease: a pilot study. New Zealand Medical Journal 2001;114(1141):447–449
34. Vincent E, Sewell L, Wagg K et al. Measuring a change in self‐efficacy following pulmonary rehabilitation: an evaluation of the PRAISE tool. Chest 2011;140(6):1534–1539
35. Liacos A, McDonald CF, Mahal A et al. The Pulmonary Rehabilitation Adapted Index of Self-Efficacy (PRAISE) tool predicts reduction in sedentary time following pulmonary rehabilitation in people with chronic obstructive pulmonary disease (COPD). Physiotherapy 2019;105(1):90–97
36. Wouters EF, Posthuma R, Koopman M et al An update on pulmonary rehabilitation techniques for patients with chronic obstructive pulmonary disease. Expert Review of Respiratory Medicine 2020;14(2):149–161
37. Hill K, Jenkins S, Cecins N et al. Estimating maximum work rate during incremental cycle ergometry testing from six-minute walk distance in patients with chronic obstructive pulmonary disease. Archives of Physical Medicine and Rehabilitation 2008;89(9):1782–1187
38. Wilson R, Jones P. A comparison of the visual analogue scale and modified Borg scale for the measurement of dyspnoea during exercise. Clinical Science 1989;76:277–282
39. Dyspnea: mechanisms, assessment, and management: a consensus statement. American Thoracic Society. American Journal of Respiratory and Critical Care Medicine 1999;159(1):321–340
40. Alison JA, McKeough ZJ, Leung RWM et al. Oxygen compared to air during exercise training in COPD with exercise-induced desaturation. European Respiratory Journal 2019;53(5):pii:1802429
41. Borge CR, Hagen KB, Mengshoel AM et al. Effects of controlled breathing exercises and respiratory muscle training in people with chronic obstructive pulmonary disease: results from evaluating the quality of evidence in systematic reviews. BMC Pulmonary Medicine 2014;14:184
42. Gosselink R. Controlled breathing and dyspnea in patients with chronic obstructive pulmonary disease (COPD). Journal of Rehabilitation Research and Development 2003;40(5 Suppl 2):25–33
43. Valenza M, Valenza-Peña G, Torres-Sánchez et al. Effectiveness of controlled breathing techniques on anxiety and depression in hospitalized patients with COPD: a randomized clinical trial. Respiratory Care 2014;59(2):209–215
44. Friedberg F, Napoli A, Coronel J et al. Chronic fatigue self-management in primary care. A randomized trial. Psychosomatic Medicine 2013;75(7):650–657
45. Goudsmit EM, Nijs J, Jason LA et al. Pacing as a strategy to improve energy management in myalgic encephalomyelitis/chronic fatigue syndrome: a consensus document. Disability and Rehabilitation 2012;34(13)1140–1147
46. Friedberg F, Sunnquist M, Nacul L. Rethinking the standard of care for myalgic encephalomyelitis/chronic fatigue syndrome. Journal of General Internal Medicine 2020;35(3):906–909
47. Kim DY, Lee JS, Park SY et al. Systematic review of randomized controlled trials for chronic fatigue syndrome/myalgic encephalomyelitis (CFS/ME). Journal of Translational Medicine 2020;18(1):7
48. Davenport TE, Stevens SR, VanNess MJ et al. Conceptual model for physical therapist management of chronic fatigue syndrome/myalgic encephalomyelitis. Physical Therapy 2010;90(4):602–14)
49. Cheshire A, Ridge D, Clark L et al. Guided graded exercise self-help for chronic fatigue syndrome: patient experiences and perceptions. Disability and Rehabilitation 2020;42:3,368–377.