What are the recommendations for returning athletes who have experienced long term COVID-19 symptoms?

Figures & data

Figure 1. PRISMA flow diagram. From ref. Page et al. [30]. For more information, visit: http://www.prisma-statement.org/

Table 1. Recommendations for athletes with ongoing COVID -19 symptoms.

Author and year	Title	Athlete definition	Recommendations
Kim et al. 2021 [13]	Coronavirus Disease 2019 and the Athletic Heart	Athletes involved in competitive sport	Cardiovascular testing should be considered on an individualised basis for athletes with protracted symptoms (≥10 days). Testing should include a clinical evaluation, ECG, hs-cTn (or available cTn) level test, and echocardiography.
	Emerging Perspectives on Pathology, Risks, and Return to Play.		Further testing may include CMR, exercise testing, and extended-duration ambulatory rhythm monitoring, if symptoms persist or recur.
Halle et al. 2021 [14]	Exercise and sports after COVID-19-Guidance from a clinical perspective	Individuals who engage in leisure time or competition level sport/exercise.	A thorough clinical examination should be taken to identify prolonged organ impairment.
			Recommended tests for athletes include: resting ECG for all people recovering from Covid-19 and returning to physical activity, including an echocardiography for people with ongoing mild symptoms. Cardiac MRI may be needed if tests are suggestive of myocarditis.
			An exercise ECG including measures of oxygen saturation is advisable, including lactate testing including oxygen saturation measurements during exercise or blood gas analysis before and after maximal exercise is advisable among people with persistent respiratory limitations. People with post‐pneumonia or myocarditis should undergo spiroergometry with blood gas analysis.
			Maximal CPET or exercise protocol including lactate testing can guide prescribed training intensity when an athlete returns-to-play.
			Measurements of residual volume and total lung capacity by body plethysmography recommended for athletes with signs of persistent respiratory limitations, alongside static and dynamic lung function testing.
			Measurement of inspiratory muscle strength capacity may be considered among athletes with ongoing dyspnoea or unexplained exercise limitation.
			A clinical neurological examination including motor, sensory, and coordination testing, cranial and peripheral nerves should be taken.
			Re-examination including resting ECG and blood tests should be performed at 3–6 months to assess any long-term effects which may occur.
Schellhorn et al. 2020 [15]	Return to sports after COVID-19 infection	Not specified.	The development of cardiovascular complications and long-term consequences of COVID-19 need to be ruled out by follow up (physical exam, resting and exercise ECG, and echocardiography).
Wilson et al. 2020 [16]	Cardiorespiratory considerations for return-to-play in elite athletes after COVID-19 infection: a practical guide for sport and exercise medicine physicians	Elite athletes.	Athletes with persistent symptoms (longer than 14 days) should undergo a thorough history and physical examinations including:
			Cardiac examination: 12-lead ECG and Cardiac MRI
			Respiratory examination: Chest X-ray and lung function
			Biochemistry evaluation: High-sensitivity cardiac troponin T, C-reactive protein and D-Dimer.
			The psychological impact of prolonged recovery among athletes should also be considered.
Elliott et al. 2020 [17]	Infographic. Graduated return to play guidance following COVID-19 infection	Performance athletes who have mild-moderate illness.	Athletes with complicated or prolonged COVID-19 may need further examination including: Blood tests (high sensitivity-Troponin, Brain Natriuretic Peptide and C reactive protein), cardiac monitoring (12-lead ECG, echocardiogram, exercise tolerance test and cardiac MRI), respiratory (spiromtry), renal and haematological monitoring.
Verwoert et al. 2020 [18]	Return to sports after COVID-19: a position paper from the Dutch Sports Cardiology Section of the Netherlands Society of Cardiology	All athletes aged 16 and over.	A record of COVID-19 cases among athletes and highly active individuals, including follow-up, is needed to inform future return to sport guidelines.
McKinney et al. 2020 [19]	COVID-19–Myocarditis and Return to Play: Reflections and Recommendations From a Canadian Working Group	Highly active persons who exercise or compete regularly at either a recreational or a competitive level.	If new/ongoing cardiac symptoms are present (palpitations, syncope, chest pain, dyspnoea, unexplained increase in heart rate), athletes should not engage in moderate-high intensity exercise, and undergo cardiac history assessment and physical examination.
Biswas et al. 2021 [20]	The BASES (British Association of Sport and Exercise Sciences) Expert Statement on Graduated Return to Play Following Covid-19 infection.	Elite and sub-elite athletes	Due to the risk of longer-term complications, return to play should be overseen or at least signed off by a medical doctor.

Figure 2. Flow diagram of athlete protocol for managing ongoing COVID-19 signs and symptoms.

Table 2. Tests to assess physical (and mental) health of athletes.

Measures taken	Reason for taking the measure
Cardiovascular tests
1) 12-lead ECG, echocardiography, cardiac MRI^a	Screen for cardiovascular complications, identify Myocarditis/myocardial oedema
Cardiopulmonary tests
1) CPET with ECG including measurement of respiratory efficiency, O2-saturation during exercise or blood gas analysis after exercise (Recommended by Halle et al. for people with more severe symptoms and/or post‐pneumonia or myocarditis).	Identify subclinical impairment in cardiopulmonary system, e.g. arrhythmias, premature dyspnoea, impaired diffusion capacity and guide future training intensities if returning to play.
Respiratory tests
1) Chest X-ray	Identify Pneumonia
Spirometry: Bronchodilator challenge and bronchoprovocation testing	Identify airway disease (may have been undiagnosed or exacerbated due to COVID-19)
Spirometry: Vital capacity and forced expiratory volume	Identify impaired lung function
FeNO testing	Identify post inflammatory bronchoconstriction
2) CT Thorax (if significant suspicion of thromboembolic or intrapulmonary abnormalities)	Covid-19 related lung damage and pulmonary vasculature pathology
3) Ventilation–perfusion scan (if O2 desaturation during CPET testing is identified and CT thorax scan is normal)	Identify microemboli.
4) Body plethysmography (Recommended by Halle et al. for people with identified pulmonary problems or ongoing symptoms of pulmonary disfunction e.g. breathlessness).	Measure residual volume and total lung capacity
5) Inspiratory muscle strength assessed	To identify potential causes behind unexplained exercise limitation/dyspnoea
Blood tests
1) D-dimer	Identify pulmonary embolism
Troponin (hs-cTn or cTn levels test)^b	Detect damage to the heart
Brain Natriuretic Peptide	Detect heart failure
C reactive protein	Assess inflammation
Blood cell count	Assess inflammation
Creatinine	Assess kidney function
Neurological test
1) Clinical neurological exam	Test for signs of damage to the neurological system, and to test for risks to safety during exercise e.g. symptoms of Vertigo.
Musculoskeletal test
1) Musculoskeletal assessment, e.g. Strength, flexibility, muscular endurance.	Musculoskeletal assessment may be advisable to identify areas of weakness following a period of deconditioning.
Mental health
1) Injury-Psychological Readiness to Return to Sport	To help identify if referral to mental health specialist/sports psychologist may be beneficial.
Mental health screening i.e. screen for symptoms of depression, anxiety.	To help identify if referral to mental health specialist/sports psychologist may be beneficial.

CPET: Cardiopulmonary exercise testing; ECG: Electrocardiogram.

^aAthletes may have anomalies in cardiac screening as a result of sport/exercise training, e.g. wall motion anomalies and pericardial effusion [13].

^bRaised troponin levels may also be an outcome of high intensity sport/exercise¹³.

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Data availability statement

On reasonable request to the corresponding author.