454 CARDIOVASCULAR SYSTEM Zdrav Vestn | July – August 2021 | Volume 90 | https://doi.org/10.6016/ZdravVestn.3230 Copyright (c) 2021 Slovenian Medical Journal. This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. Return to play for athletes after COVID-19 Vračanje športnika v proces treniranja po prebolelem covidu-19 Nejc Planinc,1 Petra Zupet,1 Gregor Kavaš,2 Matjaž Turel,3 Rok Zbačnik,4 Borut Jug,5 Zlatko Fras,6 Katja Ažman Juvan7 Abstract Most athletes with COVID-19 are asymptomatic or mildly symptomatic, but there are now consistent reports that COVID-19 positive athletes may present with persistent and residual symptoms many weeks to months after initial infection. Most often the respiratory system is affected, but COVID-19 can also entail pathological consequences on other organ systems. Athletes are especially at risk for cardiovascular complications but attention must also be paid to other organ systems (neurological, gastrointestinal, musculoskeletal…) when treating an athlete. COVID-19 can cause myocardial damage among athletes that can be due to myocarditis, which is an important cause of sudden cardiac death among them. The following article describes an approach to return to play after COVID-19 for three different athlete groups: elite athletes, child athletes under 15 years old and highly active recreational athletes. We designed four groups according to the course of COVID-19: asymptomatic athletes, athletes with mild symptoms, moderate to severe or prolonged symptoms (≥ 14 days), and with severe disease that requires hospitalization. The content of the article is adjusted to current knowledge, COVID-19 restrictions, capacity and organization of the health system in Slovenia, and is subject to additional adjustments as new evidence becomes available. 1 Institute for Medicine and Sport d.o.o., Ljubljana, Slovenia 2 Center for Sports Medicine, Institute of Occupational, Traffic and Sports Medicine, University Medical Centre Ljubljana, Ljubljana, Slovenia 3 Department of Pulmonary Diseases and Allergy, University Medical Centre Ljubljana, Ljubljana, Slovenia 4 Insitute of Radiology, University Medical Centre Ljubljana, Ljubljana, Slovenia 5 Department of Vascular Disease, University Medical Centre Ljubljana, Ljubljana, Slovenia 6 Division of Internal Medicine, University Medical Centre Ljubljana, Ljubljana, Slovenia 7 Department of Cardiovascular Surgery, University Medical Centre Ljubljana, Ljubljana, Slovenia Correspondence / Korespondenca: Katja Ažman Juvan, e: katja.azman@gmail.com Key words: athlete; return to play; COVID-19; pandemic Ključne besede: športnik; vračanje v proces treniranja; covid-19; pandemija Received / Prispelo: 19. 2. 2021 | Accepted / Sprejeto: 1. 5. 2021 Cite as / Citirajte kot: Planinc N, Zupet P, Kavaš G, Turel M, Zbačnik R, Jug B, et al. Return to play for athletes after COVID-19. Zdrav Vestn. 2021;90(7–8):454–63. DOI: https://doi.org/10.6016/ZdravVestn.3230 eng slo element en article-lang 10.6016/ZdravVestn.3230 doi 19.2.2021 date-received 1.5.2021 date-accepted Cardiovascular system Srce in obtočila discipline Professional article Strokovni članek article-type Return to play for athletes after COVID-19 Vračanje športnika v proces treniranja po pre- bolelem covidu-19 article-title Return to play for athletes after COVID-19 Vračanje športnika v proces treniranja po pre- bolelem covidu-19 alt-title athlete, return to play, COVID-19, pandemic športnik, vračanje v proces treniranja, covid-19, pandemija kwd-group The authors declare that there are no conflicts of interest present. Avtorji so izjavili, da ne obstajajo nobeni konkurenčni interesi. conflict year volume first month last month first page last page 2021 90 7 8 545 463 name surname aff email Katja Ažman Juvan 7 katja.azman@gmail.com name surname aff Nejc Planinc 1 Petra Zupet 1 Gregor Kavaš 2 Matjaž Turel 3 Rok Zbačnik 4 Borut Jug 5 Zlatko Fras 6 eng slo aff-id Institute for Medicine and Sport d.o.o., Ljubljana, Slovenia Inštitut za medicino in šport d.o.o., Ljubljana, Slovenija 1 Center for Sports Medicine, Institute of Occupational, Traffic and Sports Medicine, University Medical Centre Ljubljana, Ljubljana, Slovenia Center za medicino športa, Klinični inštitut za medicino dela, prometa in športa, Univerzitetni klinični center Ljubljana, Ljubljana, Slovenija 2 Department of Pulmonary Diseases and Allergy, University Medical Centre Ljubljana, Ljubljana, Slovenia Klinični oddelek za pljučne bolezni in alergijo, Univerzitetni klinični center Ljubljana, Ljubljana, Slovenija 3 Insitute of Radiology, University Medical Centre Ljubljana, Ljubljana, Slovenia Klinični inštitut za radiologijo, Univerzitetni klinični center Ljubljana, Ljubljana, Slovenija 4 Department of Vascular Disease, University Medical Centre Ljubljana, Ljubljana, Slovenia Klinični oddelek za žilne bolezni, Univerzitetni klinični center Ljubljana, Ljubljana, Slovenija 5 Division of Internal Medicine, University Medical Centre Ljubljana, Ljubljana, Slovenia Interna klinika, Univerzitetni klinični center Ljubljana, Ljubljana, Slovenija 6 Department of Cardiovascular Surgery, University Medical Centre Ljubljana, Ljubljana, Slovenia Klinični oddelek za kirurgijo srca in ožilja, Univerzitetni klinični center Ljubljana, Ljubljana, Slovenija 7 Slovenian Medical Journallovenian Medical Journal 455 PROFESSIONAL ARTICLE Return to play for athletes after COVID-19 1 Introduction In the autumn of 2020, the second wave of the COVID-19 pandemic spread throughout most of the world. In Slovenia, we also experienced a significant in- crease in the number of infections, confirming almost 180,000 cases by 12 February 2021 (1). Among them were athletes, mostly asymptomatic or mildly symp- tomatic. However, there are more and more cases of athletes presenting with symptoms (cough, tachycar- dia, fatigue, dyspnoea), persisting for weeks to months (2). The respiratory system is most commonly affected, but other organ systems can also be part of a systemic inflammatory process. For athletes, the cardiovascular system damage is most threatening as myocarditis is an important cause of sudden cardiac death among them and can appear in athletes with confirmed COVID-19. Most of the data on cardiovascular complications of COVID-19 has been obtained from the elderly with co- morbidities, while the data on cardiovascular compli- cations in athletes remain modest (3). In some studies, signs of myocarditis were found in a high proportion of young elite athletes using cardiac magnetic resonance imaging (cardiac MRI) (15%) (4), while in others, such a high prevalence has not been confirmed (0–3%) (5- 8). The results of the latest and at the same time the most comprehensive study, which included 789 pro- fessional athletes after infection with the SARS-CoV-2 virus, are consistent with the results of the latter stud- ies. None had a severe disease course and 41.8% were asymptomatic. Before returning to training, troponin concentrations and a 12-lead electrocardiogram (ECG) and echocardiography were performed. Abnormalities were found in 3.8% of athletes, with MRI signs of in- flammation (myocarditis or pericarditis) in only 0.6% Izvleček Večina športnikov s covidom-19 nima simptomov ali pa ima blage simptome, a vse več je primerov, ko simptomi vztrajajo še nekaj tednov do mesecev po okužbi. Najpogosteje so prizadeta dihala, vendar so lahko v sklopu sistemskega vnetja prizadeti tudi drugi organski sistemi. Športnika najbolj ogroža prizadetost srčno-žilnega sistema. Pri obravnavi je potrebno poleg srčno-žilnega sistema in dihal upoštevati tudi druge organske sisteme, ki jih lahko covid-19 prizadene (centralni in periferni živčni sistem, prebavila, skeletne mišice …). Pri športnikih so v posameznih primerih ugotavljali različno stop- njo prizadetosti miokarda, kar je lahko povezano z razvojem miokarditisa, ki je pomemben vzrok za nenadno srčno smrt športnikov. V prispevku predstavljamo vračanje v proces treniranja po prebolelem covidu-19 za tri skupine športnikov: tekmovalni športniki, športniki otroci (do 15 let) in zelo aktivni rekreativni športniki. Razdelili smo jih v štiri skupine glede na potek covida-19: športniki brez simptomov, športniki z blagimi simptomi, športniki s težjimi ali z vztrajajočimi simp- tomi (≥ 14 dni) in športniki s težjim potekom bolezni, ki zahteva bolnišnično obravnavo. Vsebina prispevka je usklajena s trenutnim znanjem, z omejevalnimi ukrepi, organizacijo zdravstvenega varstva športnikov in zmogljivostmi zdravstvenega sistema v Sloveniji. Treba jo bo prilagajati novimi dognanjem. (8). The symptoms and signs of myocarditis are varied. It is one of the most common causes of sudden cardi- ac death among young athletes (2–22%) (9,10) and the most common cause of sudden cardiac death among USA military recruits (11). Sudden cardiac death can occur without preceding symptoms or signs. The most typical are chest pain, palpitations, tachycardia, dys- pnoea, syncope, lightheadedness (particulatly during exertion) and a significant decline in physical perfor- mance. Myocarditis can be asymptomatic or with un- characteristic symptoms of a viral illness, or it can be fulminant with cardiogenic shock (12). Symptoms and signs of myocarditis can also appear in other cardiovas- cular or respiratory diseases. Therefore, it is important to combine diagnostic methods for both organ systems when determining their cause. With athletes, it is also important to consider other organ systems COVID-19 can affect (the central and peripheral nervous system, gastrointestinal and musculoskeletal systems ...) (13). Due to the risk COVID-19 poses to athletes, numer- ous authors from Europe and the USA have already made various recommendations for return to play af- ter COVID-19 (2,13-17). The return to play should al- ways be gradual. In case of confirmed infection with SARS-CoV-2, the athlete should rest for at least 10 days with at least seven of those days being asymptomatic before return to play. During the gradual return to play process, the athlete’s heart rate, dyspnoea and well-be- ing (fatigue, myalgias, insomnia) should be monitored during and after training. If symptoms appear when training intensity is increased (tachycardia, dyspnoea, disproportionate to exertion, excessive fatigue, poor re- generation after training), the training intensity should 456 CARDIOVASCULAR SYSTEM Zdrav Vestn | July – August 2021 | Volume 90 | https://doi.org/10.6016/ZdravVestn.3230 be reduced and a physician consulted. The return to play process takes 1–2 weeks on average, depending on the sport and possible problems during training inten- sification. In individual cases, return to play can take three weeks or more (18). The process of return to play, prepared by members of the Slovenian Sports Medicine Association and the Section for Sports and Exercise Cardiology at the Slove- nian Society of Cardiology, is adapted to the restrictive measures against the spread of COVID-19, organiza- tion of athlete healthcare and capacity of the healthcare system in Slovenia. It summarizes the knowledge exist- ing to date and is subject to additional adjustments as new evidence becomes available. 2 Athlete classification We divided athletes with proved infection with SARS-CoV-2 into four groups: 1. 1. Asymptomatic athletes with proved infection with SARS-CoV-2. 2. 2. Athletes with mild COVID-19 symptoms (mild fatigue, headache, cough, pharyngitis, coryza, nau- sea, vomiting, diarrhoea, anosmia/ageusia) which have completely subsided (16). 3. Athletes with moderate to severe COVID-19 symp- toms (persistent fever ≥ 38.0°C, chills, severe fatigue, pneumonia, dyspnoea, chest pain, syncope) (16) or persistent symptoms (≥ 14 days) without the need for hospitalization. 4. Athletes with severe COVID-19 who require hospi- talization. Separately we present the management of elite ath- letes, child athletes under 15 years of age and highly active recreational athletes. It is intended to identi- fy possible damage to the cardiovascular system and respiratory system. For athletes who have never had COVID-19, we propose the same as before – regular pre-participation examinations (PPE). 3 Return to play of elite athletes Elite athletes are athletes who train regularly and participate in national and international competitions. In the 1st group are asymptomatic athletes with proved infection with SARS-CoV-2. They should self-isolate for 10 days (19). During this period, rest is required with only walking and ordinary activities be- ing allowed; individual training during the self-isolation period is advised against. As there is currently insuffi- cient scientific basis on the possible effects of SARS- CoV-2 infection on the health of asymptomatic athletes, it is sensible that before return to play, these athletes should undergo a regular PPE, including checking the inflammatory parameters. Return to play should be gradual and at least a week long, depending on the sport and possible problems during training intensification. If any problems apper during the return to play process, a checkup with a specialist in occupational, traffic and sports medicine, subspecialized in sports medicine (in subsequent text: sports medicine specialist) is required. Athletes with previously known respiratory diseases (e.g. asthma) should continue with chronic therapy, modified as needed. In the 2nd group are athletes with mild COVID-19 symptoms which have completely subsided. They should self-isolate for at least 10 days, starting with the first day of illness (19). They can gradually return to play after they have been asymptomatic for at least seven days and at least 10 days have passed since symptoms started. Re- turn to play should be at least a week long, depending on the sport and possible problems during training in- tensification. If symptoms do not subside after 14 days or even worsen, the athlete should be managed as group 3 (severe or persistent symptoms). Before return to play, the athletes should be seen by a sports medicine spe- cialist. In addition to a patient history and physical ex- am directed at the cardiovascular system, an ECG and troponin concentration should be performed. In case of abnormalities or symptoms suggestive of myocarditis (chest pain, palpitations, tachycardia, dyspnoea, synco- pe), the athlete should be seen by a cardiologist and ad- ditional investigations should be performed (echocar- diography and, depending on the results, a cardiac MRI and 24-hour Holter monitoring). Finally, if myocarditis is excluded, cardiopulmonary exercise testing (CPET) should be performed. The respiratory system does not need additional investigations. Athletes with previously known respiratory diseases (e.g. asthma) should contin- ue with chronic therapy, modified as needed. In the 3rd group are athletes with severe or persistent symptoms (≥ 14 days). Before return to play, they should be seen by a sports medicine specialist. In case of persistent respiratory symptoms, a thorough workup is required to exclude thromboembolic events and dam- age to the respiratory and cardiovascular systems. In ad- dition to patient history and physical exam, a 12-lead ECG, spirometry, chest radiography and blood work (C-reactive protein – CRP, troponin, D-dimer) should 457 PROFESSIONAL ARTICLE Return to play for athletes after COVID-19 be performed. In case of abnormalities or symptoms sug- gestive of myocarditis (chest pain, palpitations, tachy- cardia, dyspnoea, syncope), the athlete should be seen by a cardiologist and additional investigations should be performed (echocardiography and/or cardiac MRI, 24-hour Holter monitoring, CPET). Stepwise manage- ment is recommended to avoid maximally straining an already ill athlete. If spirometry reveals obstructive lung disease, further follow-ups by a pulmonologist are required. Investigations to differentiate between de no- vo asthma and bronchial hyperresponsiveness after an infection are required. Basic tests include the broncho- dilator test and exhaled nitric oxide (NO) test to deter- mine inflammation of the airways. Depending on the results of these basic investigations, we decide on fur- ther diagnostic tests, such as the bronchoprovocation test. If possible, it is useful to compare the lung function testing results to previous ones. In case of suspicion of involvement of the pulmonary parenchyma, pulmonary vasculature or of thromboembolic complications, the athlete should be seen by a pulmonologist who then de- cides on further investigations (chest CT to determine both the states of the pulmonary parenchyma and vas- culature, diffusing capacity for carbon monoxide – DL- CO). If the cause of dyspnoea remains unclear, a CPET can be of help. Return to play depends on the results of these investigations. In case of pathologic findings, appropriate treatment is required according to current recommendations. If diagnostic investigations fail to show abnormali- ties, return to play should be more gradual, taking at least 1–2 weeks, depending on the sport and possible problems during training intensification. In the 4th group are athletes who require hospital- ization. Before returning to play, in addition to blood work (CRP, troponin, D-dimer), extensive diagnostic procedures should be undertaken by a cardiologist and pulmonologist. The extent of investigations (12-lead ECG, echocardiography and/or cardiac MRI, 24-hour Holter monitoring, spirometry, DLCO, chest radiog- raphy, chest CT, CPET) is decided on individually, de- pending on the investigations already performed during hospitalization and their results. Return to play depends on the results of testing and clinical course. It should always be gradual and take at least 1–2 weeks, depend- ing on the sport and possible problems during training intensification. Return to play of elite athletes is summarized in Fig- ure 1. 4 Return to play of child athletes under 15 years Most children have an asymptomatic or mildly symp- tomatic COVID-19 course, but in certain cases, multi- system inflammatory syndrome (MIS-C) can develop a few weeks after the infection. The risk of myocarditis in children is low, but myocardial damage can occur as part of MIS-C. Particular care is required in such cases (16). Child athletes aged 15 or more with signs of puberty are managed as adult athletes. Asymptomatic child athletes under 15 years of age with proved infection with SARS-CoV-2 do not need additional investigations apart from regular PPE or we decide on them individually. Unlike elite athletes, child athletes under 15 years do not require additional in- vestigations after mild COVID-19 apart from regular PPE. Return to play should always be gradual, starting at least seven days after symptoms have subsided and at least 10 days since symptoms started. It should take at least a week, depending on the sport and possible prob- lems during training intensification. In case of prob- lems during the return-to-play process, the child athlete should be seen by a paediatrician or sports medicine specialist to determine the cardiovascular risk and need for additional investigations (12-lead ECG, troponin). Depending on the problems and investigations results, they will decide on a possible referral to a cardiologist or pulmonologist. Child athletes under 15 years with severe or persistent symptoms (≥ 14 days) and all who required hospitalization should be seen by a paediatrician or sports medicine specialist after symptoms subside to de- termine the cardiovascular risk and need for additional investigations (12-lead ECG, troponin). Depending on the problems and investigations results, they will decide on a possible referral to a cardiologist or pulmonologist. Return to play should be gradual and should not start before 10–14 days after all symptoms have subsided. It should take at least 1–2 weeks, depending on the sport and possible problems during training intensification. Return to play of child athletes under 15 is summa- rized in Figure 2. 5 Return to play of highly active recreational athletes Highly active recreational athletes are people who are active several times a week or engage in high-inten- sity exercise. 458 CARDIOVASCULAR SYSTEM Zdrav Vestn | July – August 2021 | Volume 90 | https://doi.org/10.6016/ZdravVestn.3230 Figure 1: Algorithm for return to play of elite athletes after COVID-19. * Symptoms suggestive of myocarditis (chest pain, palpitations, tachycardia, dyspnoea, syncope, significant decline in physical performance). ** The extent of investigations should be individualized depending on symptoms and the results of previously performed investigations. *** The extent of investigations should be individualized depending on investigations performed during hospitalization and their results. Abbreviations: PPE – pre-participation examination; CRP – C-reactive protein; ECG – 12-lead echocardiogram; LAB – laboratory blood tests; ECHO – echocardiography; MRI – magnetic resonance imaging; CPET – cardiopulmonary exercise testing; CXR – chest radiography; DLCO – diffusing capacity for carbon monoxide; CT – computed tomography scan. History and physical exam Heart: ECG Lungs: no investigations LAB: troponin Rest and 10 days of self-isolation History and physical exam Heart: ECG Lungs: spirometry, CXR LAB: CRP, troponin, D-dimer History and physical exam LAB: CRP, troponin, D-dimer Cardiologist: ECG, ECHO ± cardiac MRI , 24-hour Holter monitoring, CPET Pulmonologist: spirometry, DLCO, CXR, chest CT, CPET Asymptomatic athletes Mildly symptomatic athletes Athletes with severe or persistent symptoms (≥ 14 days) Athletes who required hospitalization*** and/or Regular PPE + CRP Additional investigations are not required Normal Abnormalities* Abnormalities* Cardiologist**: ECHO ± cardiac MRI , 24–hour Holter monitoring, CPET Pulmonologist**: DLCO, chest CT , CPET Abnormalities Gradual return to play (aer at least 7 days without symptoms and 10 days since symptoms started), taking at least 1-2 weeks, depending on the sport and possible problems during training intensification Restriction of training, further investigations and appropriate treatment of myocarditis or other diseases Normal Normal Abnormalities Normal Abnormalities 459 PROFESSIONAL ARTICLE Return to play for athletes after COVID-19 Asymptomatic highly active recreational athletes with proved infection with SARS-CoV-2 and mildly symptomatic highly active recreational athletes do not need additional investigations before returning to play. It should be gradual and start at least seven days after symptoms have subsided and at least 10 days after the first symptoms appeared. It should take at least a week, depending on the sport and possible problems during training intensification. In case of problems during the return-to-play process, a checkup with a family medi- cine or sports medicine specialist is required, who will decide on additional investigations (12-lead ECG, tro- ponin, chest radiography, spirometry) or a referral to a cardiologist or pulmonologist. In addition to highly active recreational athletes with severe or persistent symptoms (≥ 14 days) who did not require hospitaliza- tion, there are also athletes over 65 years or with known cardiovascular diseases or risk factors in the 3rd group. To decide on return to play, a checkup with a family or sports medicine specialist is sensible once acute symp- toms subside. Depending on symptoms, the specialist will decide on additional investigations (e.g. a 12-lead ECG, troponin, CRP, D-dimer, chest radiography, spi- rometry). If all results are normal, a gradual return to play is required, which should not start before 10–14 days after all symptoms have subsided and should take Figure 2: Algorithm for return to play of child athletes under 15 after COVID-19. Child athletes over 15 years and with signs of puberty are treated as adult athletes. * In case of problems during the return-to-play process, the child athlete should be seen by a paediatrician or sports medicine specialist to determine the cardiovascular risk and the need for additional investigations (ECG, troponin) or to refer the child to a cardiologist or pulmonologist. Abbreviations: PPE – pre-participation examination; ECG – 12-lead echocardiogram; ECHO – echocardiography. Rest for at least 7 days since symptoms subsided and 10 days since symptoms started Rest and 10 days of self-isolation Rest for at least 10-14 days since symptoms subsided Checkup with a paediatrician or sports medicine specialist before return to play Asymptomatic child athletes Mildly symptomatic child athletes Child athletes with severe or persistent symptoms ( ≥ 14 days), who did not require hospitalization Child athletes who required hospitalization Gradual return to play taking at least 1-2 weeks, depending on the sport and possible problems during training intensification* Cardiovascular risk assessment and additional investigations as required (ECG, troponin, ECHO/cardiologist checkup, pulmonologist checkup if required) Regular PPE Additional investigations are not required or are decided on individually 460 CARDIOVASCULAR SYSTEM Zdrav Vestn | July – August 2021 | Volume 90 | https://doi.org/10.6016/ZdravVestn.3230 at least 1–2 weeks, depending on the sport and possi- ble problems during training intensification. In case of abnormalities, a checkup with a cardiologist or pulm- onologist is warranted. In case of pathologic findings, appropriate treatment is required according to current recommendations. Highly active recreational athletes with severe COVID-19 who required hospitalization require, similarly to elite athletes, extensive diagnos- tic investigations of the cardiovascular and respiratory systems, the extent of which is determined individually based on tests performed during hospitalization and their results before return to play. In case of normal results, a gradual return to play is warranted, but not before 10–14 days after all symptoms have subsided. It should take at least 1–2 weeks, depending on the sport and possible problems during training intensification. In case of abnormalities, appropriate treatment of dis- ease is required. Return to play of highly active recreational athletes is summarized in Figure 3. 6 Problems with assessing myocardial damage in athletes after COVID-19 Currently, a clear definition of clinically significant myocardial damage after COVID-19 in elite athletes does not exist. The data have been mostly obtained from the hospitalized, usually elderly patients with comorbidities with COVID-19 and have not been confirmed to the same extent in younger elite ath- letes. Myocardial changes, which can be secondary to long-term strenuous physical activity, also present a problem as they overlap with myocardial changes after COVID-19 (16). Among the limitations of the use of troponin (par- ticularly high-sensitivity troponin) is the lack of ref- erence values for athletes in particular and the well known release of troponin from the myocardium during strenuous physical activity. As exercise-associ- ated troponin release normalizes in 24-48 hours, the athletes should rest for at least 48 hours before tropo- nin concentrations are determined. If elevated tropo- nin concentrations are the only pathologic finding, its concentration should be determined again after anoth- er 48 hours of strict rest. Troponin concentrations can be normal despite established myocarditis, so addi- tional investigations can be performed (12-lead ECG, echocardiography and/or cardiac MRI) before return to play (20). The changes that appear in a 12-lead ECG during myocarditis or pericarditis are most commonly repo- larization abnormalities (changes in the ST segment and/or T waves), ventricular extrasystoles or arrhyth- mias, bundle branch blocks and atrioventricular (AV) conduction abnormalities. The sensitivity of these ab- normalities for the diagnosis of myopericarditis is poor (only 47%) (21). Additionally, repolarization abnor- malities are common in athletes (in more than 70%) and may be misinterpreted as a sign of myocarditis. In such cases, comparing the ECG to previous traces can be helpful to observe potential dynamics. An addition- al problem with determining myocardial damage with a 12-lead ECG is its normalization during myocarditis. With echocardiography, we can determine the global and segmental ventricular contraction, dyastol- ic function of the left ventricle and pericardial damage. In the acute phase, the left ventricle wall can be region- ally thickened due to oedema. In some (particularly endurance athletes), exercise over the years can lead to a significant increase in cardiac chamber volumes and borderline weakened ventricle contraction at rest, mimicking changes seen in mild myocarditis. An ad- ditional problem are cases of myocarditis, diagnosed only based on changes observed with a cardiac MRI, while the athletes were asymptomatic and with nor- mal troponin concentrations, 12-lead ECG at rest and echocardiograpy. Speckle tracking echocardiography plays an im- portant role in determining subtle myocardial chang- es, and cardiac MRI is even more precise as it can de- termine both the presence of oedema and myocardial fibrosis. Cardiac MRI is a useful method to determine the presence of myocarditis in symptomatic athletes (chest pain, impaired physical performance, ventricular ar- rhythmias) and/or abnormalities, found with e.g. 12-lead ECG or echocardiography with a moderate or high pretest probability of myocarditis. Currently, there is insufficient evidence to support the screening of all athletes with suspected or confirmed COVID-19 for myocarditis with a cardiac MRI, as the specificity of the current criteria for cardiac MRI in diagnosing myocarditis in a healthy and asymptomatic popula- tion is not yet known. Cardiac MRI norms for young healthy athletes are also lacking. Therefore, the insuf- ficient measurement standardization in athletes could lead to too many false positive results, leading to un- necessary further diagnostic investigations and train- ing restrictions (16). 461 PROFESSIONAL ARTICLE Return to play for athletes after COVID-19 Figure 3: Algorithm for return to play of highly active recreational athletes after COVID-19. * In case of problems during the return-to-play process, the athlete should be seen by a family or sports medicine specialist to determine the need for additional investigations (ECG, troponin, chest radiography, spirometry) or to refer the athlete to a cardiologist or pulmonologist. Abbreviations: ECG – 12-lead electrocardiogram; CRP – C-reactive protein; CXR – chest radiography; CVD – cardiovascular diseases. Rest for at least 7 days since symptoms subsided and 10 days since symptoms started Rest and 10 days of self-isolation Checkup with family or sports medicine specialist once acute symptoms subside Extensive cardiovascular and/or respiratory system diagnostic investigations at a cardiologist/pulmonologist Asymptomatic recreational athletes Mildly symptomatic recreational athletes Recreational athletes with severe or persistent symptoms ( ≥ 14 days), who did not require hospitalization, or athletes over 65 years with cardiovascular diseases or risk factors Recreational athletes who required hospitalization Additional investigations are not required Normal Cardiologist and/or pulmonologist Abnormalities Gradual return to play taking at least 1-2 weeks, depending on the sport and possible problems during training intensification* Restriction of training, further investigations and appropriate treatment of myocarditis or other diseases Normal Normal Abnormalities Think about additional investigations (ECG, troponin, CRP, D-dimer, CXR, spirometry) The extent of additional investigations is tailored to previously performed investigations during hospitalization and their results Abnormalities 462 CARDIOVASCULAR SYSTEM Zdrav Vestn | July – August 2021 | Volume 90 | https://doi.org/10.6016/ZdravVestn.3230 7 Conclusion Return to play should always be individually tai- lored to the athlete’s health, taking into account any comorbidities and type of sport. A multidisciplinary approach and cooperation of all involved (athlete, sports medicine specialist, paediatrician, family medi- cine specialist, possibly a cardiologist, pulmonologist, coach and other club representatives) is important. In the patient history and physical examination, it is im- portant to consider other organ systems (central and peripheral nervous systems, gastrointestinal and mus- culoskeletal systems) in addition to the cardiovascular and respiratory systems. Return to play should always be gradual and should not start earlier than seven days since the last symptoms and at least 10 days since the first symptoms started. It should take at least a week, depending on the sport and possible problems during training intensification. In case of any problems during the return-to-play process, a checkup with a physician is required. The article is adapted to the restrictive measures against the spread of COVID-19, organiza- tion of athlete healthcare and capacity of the healthcare system in Slovenia. It is based on the knowledge exist- ing to date and is subject to additional adjustments as new evidence becomes available. Conflict of interest None declared. References 1. Dnevno spremljanje okužb s SARS-CoV-2 (COVID-19). Ljubljana: Nacionalni inštitut za javno zdravje; 2021 [cited 2021 Feb 13]. Available from: https://www.nijz.si/sl/dnevno-spremljanje-okuzb-s-sars-cov-2- COVID-19. 2. Wilson MG, Hull JH, Rogers J, Pollock N, Dodd M, Haines J, et al. Cardiorespiratory considerations for return-to-play in elite athletes after COVID-19 infection: a practical guide for sport and exercise medicine physicians. Br J Sports Med. 2020;54(19):1157-61. DOI: 10.1136/ bjsports-2020-102710 PMID: 32878870 3. Jørstad HT, Piek JJ. COVID-19, sports, and myocardial consequences. Neth Heart J. 2020;28(11):563-4. DOI: 10.1007/s12471-020-01499-7 PMID: 33030658 4. Rajpal S, Tong MS, Borchers J, Zareba KM, Obarski TP, Simonetti OP, et al. Cardiovascular Magnetic Resonance Findings in Competitive Athletes Recovering From COVID-19 Infection. JAMA Cardiol. 2021;6(1):116-8. PMID: 32915194 5. Starekova J, Bluemke DA, Bradham WS, Eckhardt LL, Grist TM, Kusmirek JE, et al. Evaluation for Myocarditis in Competitive Student Athletes Recovering From Coronavirus Disease 2019 With Cardiac Magnetic Resonance Imaging. JAMA Cardiol. 2021:e207444. DOI: 10.1001/ jamacardio.2020.7444 PMID: 33443537 6. Clark DE, Parikh A, Dendy JM, Diamond AB, George-Durrett K, Fish FA, et al. COVID-19 Myocardial Pathology Evaluated Through scrEening Cardiac Magnetic Resonance (COMPETE CMR). MedRxiv [Preprint]. 2020. DOI: 10.1101/2020.08.31.20185140 PMID: 32908996 7. Małek ŁA, Marczak M, Miłosz-Wieczorek B, Konopka M, Braksator W, Drygas W, et al. Cardiac involvement in consecutive elite athletes recovered from Covid-19: A magnetic resonance study. J Magn Reson Imaging. 2021;53(6):1723-9. DOI: 10.1002/jmri.27513 PMID: 33474768 8. Martinez MW, Tucker AM, Bloom OJ, Green G, DiFiori JP, Solomon G, et al. Prevalence of Inflammatory Heart Disease Among Professional Athletes With Prior COVID-19 Infection Who Received Systematic Return- to-Play Cardiac Screening. JAMA Cardiol. 2021:e210565. DOI: 10.1001/ jamacardio.2021.0565 PMID: 33662103 9. Cooper LT, Keren A, Sliwa K, Matsumori A, Mensah GA. The global burden of myocarditis: part 1: a systematic literature review for the Global Burden of Diseases, Injuries, and Risk Factors 2010 study. Glob Heart. 2014;9(1):121-9. DOI: 10.1016/j.gheart.2014.01.007 PMID: 25432122 10. Maron BJ. Sudden death in young athletes. N Engl J Med. 2003;349(11):1064-75. DOI: 10.1056/NEJMra022783 PMID: 12968091 11. Rauka NP, Cooper LT. Implications of SARS-CoV-2-Associated Myocarditis in the Medical Evaluation of Athletes. Sports Health. 2021;13(2):145-8. DOI: 10.1177/1941738120974747 PMID: 33201768 12. Halle M, Binzenhöfer L, Mahrholdt H, Schindler MJ, Esefeld K, Tschöpe C. Myocarditis in athletes: A clinical perspective. Eur J Prev Cardiol. 2020:2047487320909670. DOI: 10.1177/2047487320909670 PMID: 32126831 13. Nieß AM, Bloch W, Friedmann-Bette B, Grim C, Halle M, Hirschmüller A, et al. Position stand: return to sport in the current Coronavirus pandemic (SARS-CoV-2/COVID-19). Dtsch Z Sportmed. 2020;71(5):1-4. DOI: 10.5960/ dzsm.2020.437 14. Löllgen H, Bachl N, Papadopoulou T, Shafik A, Holloway G, Vonbank K, et al. Infographic. Clinical recommendations for return to play during the COVID-19 pandemic. Br J Sports Med. 2021;55(6):344-6. DOI: 10.1136/ bjsports-2020-102985 PMID: 32883690 15. Phelan D, Kim JH, Chung EH. A Game Plan for the Resumption of Sport and Exercise After Coronavirus Disease 2019 (COVID-19) Infection. JAMA Cardiol. 2020;5(10):1085-6. DOI: 10.1001/jamacardio.2020.2136 PMID: 32402054 16. Kim JH, Levine BD, Phelan D, Emery MS, Martinez MW, Chung EH, et al. Coronavirus Disease 2019 and the Athletic Heart: Emerging Perspectives on Pathology, Risks, and Return to Play. JAMA Cardiol. 2021;6(2):219-27. DOI: 10.1001/jamacardio.2020.5890 PMID: 33104154 17. Löllgen H, Bachl N, Papadopoulou T, Shafik A, Holloway G, Vonbank K, et al. Recommendations for return to sport during the SARS-CoV-2 pandemic. BMJ Open Sport Exerc Med. 2020;6(1):e000858. DOI: 10.1136/ bmjsem-2020-000858 18. Elliott N, Martin R, Heron N, Elliott J, Grimstead D, Biswas A. Infographic. Graduated return to play guidance following COVID-19 infection. Br J Sports Med. 2020;54(19):1174-5. DOI: 10.1136/bjsports-2020-102637 PMID: 32571796 19. Navodila za bolnike s COVID-19, ki ne potrebojejo bolnišnične oskrbe. Ljubljana: Nacionalni inštitut za javno zdravje; 2021 [cited 2021 Jan 1]. Available from: https://www.nijz.si/sites/www.nijz.si/files/uploaded/ navodila_za_osebe_s_covid-19_doma_23.4.pdf. 463 PROFESSIONAL ARTICLE Return to play for athletes after COVID-19 20. Phelan D, Kim JH, Chung EH. Return-to-Play Guidelines for Athletes After COVID-19 Infection-Reply. JAMA Cardiol. 2020;6(4):479-80. DOI: 10.1001/ jamacardio.2020.5351 PMID: 33146679 21. Morgera T, Di Lenarda A, Dreas L, Pinamonti B, Humar F, Bussani R, et al. Electrocardiography of myocarditis revisited: clinical and prognostic significance of electrocardiographic changes. Am Heart J. 1992;124(2):455-67. DOI: 10.1016/0002-8703(92)90613-Z PMID: 1636589