Evidence-based position paper on physical and rehabilitation medicine professional practice for persons with COVID-19, including post COVID-19 condition: the European PRM position (UEMS PRM Section)

Abstract

Although multiple factors still pose challenges to inpatient/outpatient rehabilitation for survivors of COVID-19, rehabilitation plays a key role for this patient population. This study aimed to improve Physical and Rehabilitation Medicine (PRM) physician’s professional practice for persons with COVID-19-related functioning limitations, to promote functional recovery and reduce activity limitations and/or participation restrictions. A systematic review of the scientific literature was performed from December 2019 to August 2022, followed by production of recommendations through 5 Delphi rounds, by consensus among the delegates of all European countries represented in the Union of European Medical Specialists PRM Section. The systematic literature review is reported together with thirty-two recommendations resulting from the Delphi procedure. The PRM physician’s role for persons with COVID-19-related limitations of functioning is to develop, foster, and monitor the implementation of an individual rehabilitation project tailored to the patient’s age, previous medical and functional status, current comorbidities and complications, activity limitations and participation restrictions and personal and environmental factors. This is done by applying the concept of a multi-specialty integrated service model with multi-professional/interdisciplinary teams, providing care at all stages of COVID-19 illness. This evidence-based position paper represents the official position of the European Union through the UEMS PRM Section.

SARS-CoV-2 continues to infect several thousands of people daily, leading to preventable morbidity and mortality worldwide. Globally, as of August 16, 2023, there have been 769,774,646 confirmed cases of COVID-19 (275,854,299 confirmed cases in Europe), including 6,955,141 deaths, reported by the World Health Organization (WHO).¹ At the outset of the pandemic, the rehabilitation needs for patients recovering from COVID-19 were based on evidence from the critical care population and in the sequelae of COVID-19 in the short- and medium-term.^{2, 3} In particular, patients suffering from severe COVID-19 and admitted to the intensive care unit (ICU) were at higher risk of developing post-intensive care syndrome (i.e., older persons with underlying diseases such as diabetes, hypertension, increased frailty, and other chronic disorders), which is a range of impairments including physical deconditioning, respiratory, swallow, cognitive, and mental health symptoms.^{4, 5}

So, early rehabilitation became an indispensable part of the multidisciplinary management of critically ill patients.⁶

However, all hospitalized patients, ICU and non-ICU, reported new illness-related fatigue, breathlessness, post traumatic stress disorder symptoms, pain, voice change, cough, dysphagia, anxiety, depression, and problems with concentration, memory, and continence.⁷

Moreover, hospitalized patients, particularly those with prolonged stay, are susceptible to pressure injuries given inactivity, use of artificial airways, and prone positioning.⁸ So, they are at risk of multisystem impairments predisposing them to require acute inpatient rehabilitation, which has been demonstrated to improve functional recovery and safe discharge at home.^{2, 9, 10}

With the progression of the pandemic, the development of vaccines (as of August 15 2023, 13,498,570.620 vaccine doses have been administered),¹ new treatments for COVID-19 that have substantially reduced hospitalization, the severity of disease and mortality, and patients’ long-term follow-up, further evidence is emerging about COVID-19 related persistent symptoms. Known by various names, including long COVID or long-haul COVID, and listed in the ICD-10 classification as post COVID-19 condition (PCC) since September 2020,¹¹ its occurrence is variable in terms of expression and impact on daily life.

The WHO defines PCC as the condition occurring in individuals with a history of probable or confirmed SARS-CoV-2 infection, usually three months from the onset, with symptoms that last for at least two months and cannot be explained by an alternative diagnosis. PCC is more common in adults than children, in adult females than adult males, and in those hospitalized than those who were not.¹² The empirical findings suggest a PCC global estimated pooled prevalence of approximately 43%.¹² Based on a WHO estimate of 770 million worldwide COVID-19 infections, this global pooled PCC estimate indicates that approximately 330 million individuals currently experience or have previously experienced long-term, health-related consequences of COVID-19. Common symptoms include, but are not limited to, fatigue, shortness of breath, and cognitive dysfunction, which generally impact everyday functioning. Symptoms might be new onset following initial recovery from an acute COVID-19 episode or persist from the initial illness. Symptoms might also fluctuate or relapse over time.¹³ A recent Dutch study acknowledged four subtypes: muscle pain, fatigue, cardiorespiratory, and ageusia/anosmia.¹⁴

The pathophysiological mechanisms of post-COVID symptoms are multiple and potentially overlapping, including persisting viral reservoirs, immune dysfunction, microclotting, and end-organ damage.¹⁵ Due to the complex nature of this condition, the multi-system impact on functioning, a well-coordinated and organized interdisciplinary/multi-professional team that establishes a rehabilitative multidimensional program is required.^{16, 17}

Physical and Rehabilitation Medicine (PRM) is defined as the medicine of functioning. As such, it represents the primary medical specialty that addresses patients’ health needs by referring to the integrative model of functioning, disability, and health proposed by the WHO and applying rehabilitation as a core health strategy. PRM physicians are adequately trained and qualified to organize and manage the Individual rehabilitation project (IRP) for COVID-19 survivors within a holistic teamwork approach in acute, post-acute, and community settings. The aim of this evidence-based position paper (EBPP) is to improve PRM physician’s professional practice for persons with COVID-19-related limitations of functioning, to promote their functional recovery and reduce activity limitations and/or participation restrictions.

Materials and methods

This paper was developed according to the methodology defined by the Professional Practice Committee of the Union of European Medical Specialists (UEMS) PRM Section and described by Negrini et al.¹⁸ It consists of 1) a systematic review of the scientific literature to select papers relevant to the study aim; 2) the development of recommendations grouped in five domains (Table I); c) the progressive selection and refining of recommendations through five Delphi rounds, by consensus among the delegates of all European countries represented in the UEMS PRM Section (Table II).

Table I. —Domains of recommendations listed in the EBPP.

Domain	Heading and subheadings
A	Overall general recommendations
B	Recommendations on PRM physician’s role in Medical Diagnosis according to ICD
C	Recommendations on PRM physician’s role in PRM diagnosis and assessment according to ICF
D	Recommendations on PRM management and process a. Inclusion criteria (e.g., when and why to prescribe PRM interventions) b. Project definition (definition of overall aims and strategies of PRM interventions) c. Teamwork (professionals involved and specific modalities of teamwork) d. PRM interventions e. Outcome criteria f. Length/Duration/Intensity of treatment (overall practical PRM approach) g. Discharge criteria (e.g., when and why to end PRM interventions) h. Follow-up criteria and agenda
E	Recommendations on future research of PRM professional practice

Table II. —Delphi rounds.

Delphi round	Participants	Timing	Agreement on	Levels
1	Authors	14 days	Recommendations	Accept / accept with changes / reject
2	All delegates	14 days	Recommendations	Accept / accept with changes / reject
3	All delegates	14 days	Recommendations	Accept / reject
4	Authors	14 days	Strength of Recommendations	A. It must be normally applied B. It is important but can be applied not in all situations C. Less important, it can be applied on a voluntary basis D. Very low importance
5	All delegates	14 days	Final paper with recommendations	Yes / no

We conducted a comprehensive literature search on September 1st, 2022, covering publication dates between December 1^st, 2019, and August 31^st, 2022. We searched PubMed, Embase, CINAHL, Scopus, Web of Science, and PEDro for “rehabilitation” and “COVID-19”, adapting search strategies to each database-specific thesaurus and applying the string used by Ceravolo et al.²

Due to the expected poor availability of high-quality research, a comprehensive approach was applied, considering all types of studies in the English language. We selected papers addressing the rehabilitation needs of people 1) with a confirmed diagnosis of COVID-19, in any phase, without age, gender, ethnicity, or care setting restrictions; 2) presenting any limitations of functioning of rehabilitation interest (LFRI); 3) receiving any rehabilitation interventions compared with any other interventions; 4) undergoing any assessment to determine the presence of LFRI and 5) evaluated with any outcome measures.

Eventually, the criterion for including the studies was the professional relevance for PRM physicians as judged by two authors (AF and EA), with the main author (MGC) resolving conflicts.

The grading of the strength of evidence (SoE) and Strength of Recommendations (SoR) was done as described in the original “Methodology paper.”¹⁸

Results

Systematic review

The electronic literature search identified 70340 titles. After duplicate removal, 36,327 papers were screened based on titles and abstracts, and those not meeting eligibility criteria were excluded. Of the 615 remaining papers, 514 more were excluded as not relevant to PRM practice based on the full-text content. The remaining 101 articles were considered for the preparation of the recommendations. The selection process is reported in Figure 1. From a former list of 65 recommendations, the consensus procedure ended up with 32 final recommendations, as displayed in Table III. The overall view of the Recommendations, their distribution through the different domains concerning the PRM physician’s role and the grading of evidence, as resulting from the 4th Delphi round, is presented in Table IV.

Figure 1.

—Flow chart of paper selection.

Table III. —Results of the consensus procedure – recommendation selection.

		Accept		Accept with suggestions		Reject
Round	Number of recommendations	Number	%	Number	%	Number	%
1	65	34	52.3	29	44.6	2	3.1
2	63	8	12.7	24	38.1	31	49.2
3	32	32	100.0	NA	NA	0	0

Table IV. —Distribution of recommendations and grading of evidence.

Domain	N. of recommendations	Strength of recommendations				Strength of evidence
	N.	A	B	C	D	I	II	III	IV	NA
Overall general recommendation	1	100%	0	0	0	0	0	0	100%	0
PRM physicians’ role in medical diagnosis according to ICD	5	60%	40%	0	0	0	0	0	80%	20%
PRM physicians’ role in PRM diagnosis and assessment according to ICF	3	100%	0	0	0	0	0	0	66%	33%
Recommendations on PRM management and process	22	77.2%	22.7%	0	0	4.5%	13.6%	0	50%	31.8%
Recommendations on future research on PRM professional practice	1	100%	0	0	0	0	0	0	0	100%
Total	32	68.7%	31.3%	0	0	3.1%	9.4%	0	53.1%	34.4%

The recommendations stated in this EBPP highlight the role of the PRM physician as the leader of the interdisciplinary multi-professional team caring for patients with functional limitations of rehabilitation interest after COVID-19.

Before reporting the recommendations, we describe a few issues emanating from the literature review:

• importance of an early provision of tailored rehabilitation care: It is demonstrated that an IRP, starting as early as possible, considering patients’ exercise tolerance, is effective at preventing the vicious cycle of asthenia, respiratory muscle weakness, and progressive respiratory failure of COVID-19 patients admitted to the ICU.^{19, 20}

• Relevance of the involvement of the PRM physician in the care pathway dedicated to COVID-19 survivors in any phase of the disease to ensure a thorough assessment of the multiple function impairments following the infection, the prescription of rehabilitation interventions of proper amount and intensity,⁹ and the evaluation of their effects through the application of disease-related or generic outcome measures.^20-24

• Need for PRM physicians to schedule regular follow-ups of the patient’s functional status after hospital discharge. The risk for people with COVID-19 to develop a PCC is well-documented, as is the functional relevance of this condition. The PRM physician has specialized competence and skills to provide a comprehensive clinical and functional monitoring of adults with moderate-severe COVID-19 for a minimum of 12 months to tailor rehabilitation interventions for patients with low functional status or post-intensive care syndrome.^25-35

Recommendations

Overall general recommendation

1. In managing patients with COVID-19, a PRM physician’s professional responsibilities include developing, facilitating, and supervising an IRP³⁶ customized to the patient’s age, previous medical and functional status, and type and severity of the symptoms. Any IRP should consider the comorbidities that could hinder a patient’s progress or participation, apply the concept of a multi-speciality integrated service model with multiprofessional/interdisciplinary teams and provide individualized care, taking activity limitations and participation restrictions into account at all stages of COVID-19 illness.^{37, 38} [SoR: A, SoE: IV]

A. Recommendations on PRM physicians’ role in Medical Diagnosis according to ICD

2. It is recommended that the PRM physician acquires knowledge of medical diagnosis and management of individuals with COVID-19 in acute settings. [SoR: B, SoE:NA]

3. It is recommended that the PRM physician working in rehabilitation settings has the skills and knowledge to promptly diagnose COVID-19 in their patients receiving rehabilitation for other conditions through constant surveillance.³⁹ [SoR: A, SoE: IV]

4. It is recommended that the PRM physician has the knowledge and skills to identify and make the preliminary diagnosis of all the medical complications of COVID-19 in an acute hospital and community setting, and provide the proper diagnosis of PCC.^{40, 41} [SoR: A, SoE: IV]

5. It is recommended that the PRM physician has specific expertise in undertaking prompt baseline investigations and ruling out life-threatening conditions in patients with PCC.^{37, 39} [SoR: B, SoE: IV]

6. It is recommended that the PRM physician joins the community care programmes for PCC patients and is involved in a closer follow-up for these patients to suspect, diagnose and manage any body function (e.g. either mental, sensory, autonomic or neuromuscular and movement-related) impairment or delayed return to vocational activity arising from PCC.⁴² [SoR: A, SoE: IV]

B. Recommendations on PRM physicians’ role in PRM diagnosis and assessment according to ICF

7. It is recommended that the PRM physician ensures adequate activities and interventions in the acute setting to prevent complications during the acute phase of COVID-19 by supporting/leading the existing acute interdisciplinary/multi-professional team caring for the patients.^{43, 44} [SoR: A, SoE: IV]

8. It is recommended that the PRM physician participates in a full functional assessment, which includes activities and participation while paying close attention to whether or not PCC patients have particular impairments. [SoR: A, SoE: NA]

9. It is recommended that the PRM physician uses the International Classification of Functioning, Disability, and Health (ICF) framework developed by the WHO to measure the effects of PCC on patients’ physical, cognitive, emotional, and general well-being.^{45, 46} [SoR: A, SoE: IV]

C. Recommendations on PRM management and process

a. Inclusion criteria (e.g., when and why to prescribe PRM interventions)

10. It is recommended that the PRM physician develops and implements the IRP and interventions for patients with COVID-19 who are admitted to the acute wards and for patients with debilitating sequelae of COVID-19 who are admitted to the acute rehabilitation settings.⁴³ [SoR: A, SoE: NA]

11. It is recommended that the PRM physician, following a comprehensive assessment, prescribes and implements a tailored inpatient, outpatient or community-based IRP by leading and coordinating the multi-professional team for patients with PCC presenting with activity limitations and/or participation restrictions. [SoR: A, SoE: NA]

12. It is recommended that the PRM physician re-evaluates the symptoms in patients with PCC and modifies the rehabilitation treatment in patients with a progression of symptoms causing functional impairments, activity limitations or participation restrictions. [SoR: A, SoE:NA]

b. Project definition (definition of the overall aims and strategy of PRM interventions)

13. It is recommended that the PRM physician in the acute setting creates capacity to meet the increasing COVID-19 demand, develops pathways and supports early discharge from the acute care units into a rehabilitation setting as well as safe discharge from the inpatient rehabilitation environment to the outpatient and community environment.⁴³ [SoR: B, SoE: NA]

14. It is recommended that the PRM physician establishes a multi-specialty integrated service model for the care of PCC patients (including specialties such as internal medicine, pulmonology, cardiology, neurology, and neuropsychiatry) in inpatient and outpatient settings.^{37, 47-52} [SoR: A, SoE:IV]

15. It is recommended that the PRM physician, within the multi-specialty integrated service model, specifies the aims and procedures for rehabilitation intervention to provide holistic, long-term care with monitoring of rehabilitation interventions and evaluating outcome measures of PCC patients.^{37, 52} [SoR: A, SoE: IV]

16. It is recommended that the PRM physician consider using self-management tools such as leaflets, information videos, workshops, lectures and webinars to promote positive physical and mental well-being in patients with PCC.^52-57 [SoR: B, SoE: IV]

17. It is recommended that the PRM physician is aware of and adheres to existing recommendations and guidelines while making evidence-based decisions on healthcare interventions for individuals with PCC. [SoR: A, SoE: NA]

c. Teamwork (professionals involved and specific modalities of teamwork)

18. It is recommended that the rehabilitation needs of PCC patients be met by a well-coordinated and organised interdisciplinary/multi-professional team composed of a PRM physician and other pertinent medical professionals (pulmonologists, cardiologists, neurologists, internal medicine physicians, neuropsychiatrists, and primary care physicians). The multi-professional team should include rehabilitation and other relevant health professionals such as physiotherapists, occupational therapists, nurses, clinical (neuro)psychologists, dieticians, speech and language therapists, and social workers to manage patients with PCC. This can be offered at any level of care or setting (including acute care, specialised post-acute care, and community-based services).^{17, 47-49} [SoR: A, SoE: IV]

d. PRM interventions

19. It is recommended that the PRM physician, together with the multi-professional team, have adequate theoretical knowledge, clinical skills, and therapeutic equipment for clinical and functional assessment to provide a base for planning and early performing a patient-tailored rehabilitation intervention through all stages of COVID-19.^58-62 [SoR: A, SoE: IV]

20. It is recommended that the PRM physician provides Individual rehabilitation projects for COVID-19 patients, starting as early as possible, considering exercise tolerance, with the aim of preventing the vicious cycle of asthenia, respiratory muscle weakness and progressive respiratory failure.¹⁹ [SoR: A; SoE: II]

21. It is recommended that the PRM physician knows the indications and develops appropriate knowledge and skills to prescribe, when appropriate, rehabilitation interventions relevant to the different phases of COVID-19 and assesses their effects through the application of disease-related (when available) or generic outcome measures. More in detail, the PRM physician should take care that patients admitted to hospital in the acute COVID-19 phase receive, when appropriate:

a. inspiratory muscle training^20-23 also in combination with group psychological interventions.²⁴ [SoR: A; SoE: II]

b. Nutritional assessment and malnutrition screening.^63-66 [SoR: A; SoE: IV]

c. Swallowing assessment for detecting dysphagia following invasive ventilation and proper swallowing training to promote the recovery of safe oral feeding.^67-70 [SoR: A; SoE: IV]

d. Nonpharmacological therapy (such as meditation) and breathing exercises to manage depression, anxiety, and quality of sleep.⁷¹ [SoR: B; SoE: II]

e. Self-care breathing exercises to improve respiratory symptoms.^{72, 73} [SoR:A; SoE:I]

f. Tailored telerehabilitation programs focused on aerobic, resistance, and respiratory muscle training.^{51, 63, 74-77} [SoR: A; SoE: I]

22. It is recommended that the PRM physician prescribes telerehabilitation programs for persons with COVID-19, not only in the outpatient but also in the inpatient setting, to maximize rehabilitation professionals’ safety while ensuring healthcare delivery.⁷⁷ [SoR: B; SoE: IV]

23. It is recommended that the PRM physician takes care that patients with PCC receive, when appropriate:

a. respiratory rehabilitation comprehensive of respiratory muscle training, cough exercises, diaphragmatic training, stretching and home exercises to improve respiratory function, quality of life, and anxiety.⁷⁸ [SoR: A; SoE: II]

b. A combination of pain education, skills training on energy conservation techniques for the management of fatigue, tailored physical exercise training, psychological support for the management of anxiety and depression, olfactory training for the management of olfactory impairment, goal-oriented skills training for the management of swallowing and voice impairment.^79-87 [SoR: A; SoE: III]

e. Outcome criteria

24. It is recommended that the PRM physician performs a thorough assessment of pulmonary function, endurance,^{17, 74, 76, 78, 88-91} functioning and disability,^{41, 92-94} quality of life, mood, and sleep using standardized assessment tools with adequate psychometric and diagnostic properties for persons with COVID-19.^{74, 88-91, 95, 96} [SoR: A; SoE: I]

f. Length/duration/intensity of treatment (overall practical PRM approach)

25. It is recommended that the PRM physician adapts treatment/decisions/strategies/schedules to the individual needs of the person with COVID-19 and shares any decision on the length, duration, and intensity of specific treatment with the rehabilitation team members, patient, and family. [SoR: A; SoE: NA]

26. It is recommended that the PRM physician carefully plans the amount and intensity of rehabilitation in the COVID-19 acute phase, keeping in mind that the greater the frequency and duration of intervention, the higher the mobility improvement at hospital discharge and the probability of discharge home.⁹ [SoR: B; SoE: IV]

More in detail, the PRM physician should take care that patients admitted to hospital in the acute COVID-19 phase receive, when appropriate:

a. Up to 3 speech and language therapy sessions to recover safe swallowing patterns in case of dysphagia following orotracheal intubation.^{68, 70} [SoR: B; SoE: IV]

b. Moderate-intensity aerobic exercise to decrease the severity and progression of COVID-19-associated disorders and improve quality of life in young and middle-aged persons with mild or moderate ongoing COVID-19.⁹⁷ [SoR: B; SoE: II]

c. Multimodal inpatient cardiopulmonary rehabilitation intervention (i.e., 25-30 min/session, 5-6 sessions/week for 2-4 weeks) for patients with ongoing severe COVID-19.⁹⁸ [SoR: B; SoE: IV]

d. Supervised high-intensity interval training (HIIT), with any of the most widely used HIIT protocols (4×4, 6×1, or 10-20-30), for patients recently hospitalized with severe COVID-19 infection and recovering from acute phase.⁹⁹[ SoR: B; SoE: II]

e. Low-intensity aerobic training exercises (i.e. 30 minutes/sessions, one session/day, four days/week for eight weeks, 40%-60% of maximum heart rate) for older persons with PCC sarcopenia.¹⁰⁰ [SoR: B; SoE: II]

f. Rehabilitation treatment, including pulmonary, aerobic and resistance training (3 sessions/week for 6-8 weeks) for persons with PCC.^{101, 102} [SoR: B; SoE: IV]

27. It is recommended that the PRM physician prescribes exercise protocols comprehensive of a home program to maintain the physical functional performance of patients with COVID-19 throughout the hospital stay and after discharge.¹⁰³ [SoR: B; SoE: IV]

g. Discharge criteria (e.g., when and why to end PRM interventions)

28. It is recommended that a person with COVID-19 concludes the rehabilitation program after reaching the long-term goals set at the beginning, or during the (program can be modified) rehabilitation program or when there has not been any further progress in his/her functional capacity for the defined time period, or when he or she is not able to participate in the rehabilitation program due to deterioration in his/her health or the onset of a significant co-morbidity. [SoR: A; SoE: NA]

h. Follow-up criteria and agenda

29. It is recommended that the PRM physician tailors the follow-up of persons with COVID-19 based on their individual clinical and functional needs.^{25, 104} [SoR: A; SoE: IV]

30. It is recommended that the PRM physician provides a comprehensive clinical and functional monitoring of adults with moderate-severe COVID-19 for a minimum of 12 months to develop specific rehabilitation strategies for patients who exhibit a low functional status and pre-admission frailty, comorbidity, female gender, advanced age, active smoking, severe infection at onset, PaO2/FiO2 ratio <324, BMI ≥33 Kg/m2 at admission to the emergency department, or post-intensive care syndrome.^25-35 [SoR: A; SoE: IV]

31. It is recommended that the PRM physician provides a comprehensive clinical and functional monitoring of children with moderate-severe COVID-19 for a minimum of three months, in particular for those of older age with a history of muscle pain at onset and admission to the ICU.^{35, 105, 106} [SoR: A; SoE: IV]

D. Recommendations on future research about best PRM professional practice

32. It is recommended that the PRM physician participates in research on PRM professional practice, which is focused on the effective and comprehensive rehabilitation of limitations of functioning caused by COVID-19, contributing to understanding the functional impact of the new variants of COVID-19 in the long-term, weigh risk factors for persisting LFRI after COVID-19 and ascertain the impact of the PCC on work abilities. [SoR: A; SoE: NA]

Conclusions

The professional role of the PRM physician requires specific expertise in the assessment of the limitations of functioning of patients with COVID-19, at any stage after the infection, to plan, lead and monitor the rehabilitation process in a multi-professional setting through an interdisciplinary approach. PRM physicians should be involved in the care process dedicated to people with COVID-19 as early as possible, addressing the patients’ rehabilitation needs from the acute to the post-acute phase, in any setting, including the screening and assessment of post-COVID conditions, to plan the IRP and supervise its delivery in the continuum of care. Moreover, the PRM physician should work on the implementation and, where existing, improvement of specialized rehabilitation services dedicated to people with limitations of functioning due to COVID-19 or post-COVID conditions.

This EBPP, approved unanimously by the delegates of the UEMS PRM Section at the end of the Consensus procedure (Delphi Round 5), represents the official position of the Section and describes the professional role of PRM physicians in people with COVID-19.