REVIEW
Particularities of curation of athletes with protracted course of COVID-19
1 National Research Mordovia State University, Saransk, Russia
2 Federal Research and Clinical Center for Sports Medicine and Rehabilitation of the Federal Medical Biological Agency, Moscow, Russia
3 Pirogov Russian National Research Medical University, Moscow, Russia
Correspondence should be addressed: Maria S. Tarasova
B.Dorogomilovskaya, 5, Moscow, 121059, Russia; ur.abmftrops@smavosarat
Funding: the article was prepared as part of the applied research work "Investigation of the impact of COVID-19 on health and functional state of elite athletes and development of methodological recommendations for examination of athletes, including minors, before allowing them to train and compete after COVID-19, with the aim to ensure restoration of their health and functional state" (code "COVID-22"); the work is done by the Federal Research and Clinical Center of Sports Medicine and Rehabilitation of Federal Medical Biological Agency of Russia under state contract № 107.003.22.14 of July 25, 2022.
Author contributions: LA Balykova — development of the concept, text authoring, editing; AV Zholinsky — development of the concept, editing; MS Tarasova, MV Shirmankina, ZhV Grishina — search for and analysis of sources, text authoring; SA Ivyanskiy, RA Bespalov — search for and analysis of sources, development of the mathematical modeling tool, text authoring; SA Bazanovich — definition of approaches to mathematical modeling and their optimization; PV Efimov — search for and analysis of sources, definition of approaches to mathematical modeling and their optimization, text authoring; SA Parastaev — search for and analysis of sources, editing.
- Zholinsky AV, Kruglova IV, Feshchenko VS, Risukhina YV, Fomin AV, Galaktionova NM, et al. Federal medical biological agency of Russia's efforts to support Russian athletes during COVID-19 outbreak. Sport Sci Health. 2022; 18 (3): 831–7. DOI: 10.1007/ s11332-021-00861-5. Epub 2021 Nov 6. PMID: 34777596; PMCID: PMC8571973.
- World Health Organization. Available from: https://www.who.int/ europe/emergencies/situations/covid-19
- Amirov NB, Davletshina EhI, Vasileva AG, Fatyxov RG. Postkovidnyj sindrom: mul'tisistemnye «deficity». Vestnik sovremennoj klinicheskoj mediciny. 2021; 14 (6). Russian.
- Soriano JB, Murthy S, Marshall JC, Relan P, Diaz JV; WHO clinical case definition working group on post-COVID-19 condition. A clinical case definition of post-COVID-19 condition by a Delphi consensus. Lancet Infect Dis. 2022; 22 (4): e102–e107. DOI: 10.1016/S1473-3099(21)00703-9. Epub 2021 Dec 21. PMID: 34951953; PMCID: PMC8691845.
- Alkodaymi MS, Omrani OA, Fawzy NA, Shaar BA, Almamlouk R, Riaz M, et al. Prevalence of post-acute COVID-19 syndrome symptoms at different follow-up periods: a systematic review and meta-analysis. Clin Microbiol Infect. 2022; 28 (5): 657–66. DOI: 10.1016/j.cmi.2022.01.014. Epub 2022 Feb 3. PMID: 35124265; PMCID: PMC8812092.
- Perrone MA, Volterrani M, Manzi V, Barchiesi F, Iellamo F. Heart rate variability modifications in response to different types of exercise training in athletes. J Sports Med Phys Fitness. 2021; 61 (10): 1411–5. DOI: 10.23736/S0022-4707.21.12480-6. Epub 2021 Jun 17 PMID: 34137572.
- Powell AW, Urbina EM, Orr WB, Hansen JE, Baskar S. EKG abnormalities in a youth athlete following COVID-19: it's not always myocarditis! Pediatr Cardiol. 2022; 43 (8): 1922–5. DOI: 10.1007/s00246-022-02935-8. Epub 2022 May 27. PMID: 35622085; PMCID: PMC9136195.
- Tanacli R, Doeblin P, Götze C, Zieschang V, Faragli A, Stehning C, et al. COVID-19 vs. Classical myocarditis associated myocardial injury evaluated by cardiac magnetic resonance and endomyocardial biopsy. Front Cardiovasc Med. 2021; 8: 737257. DOI: 10.3389/ fcvm.2021.737257. PMID: 35004872; PMCID: PMC8739473
- Wulf HS, Abbafati C, Aerts JG, et al. A global systematic analysis of the occurrence, severity, and recovery pattern of long COVID in 2020 and 2021. medRxiv. 2022.
- Oikonomou E, Lampsas S, Theofilis P, Souvaliotis N, Papamikroulis GA, Katsarou O, et al. Impaired left ventricular deformation and ventricular-arterial coupling in post-COVID-19: association with autonomic dysregulation. Heart Vessels. 2023; 38 (3): 381–93. DOI: 10.1007/s00380-022-02180-2. Epub 2022 Sep 28.
- Antonelli M, et al. Risk factors and disease profile of postvaccination SARS-CoV-2 infection in UK users of the COVID Symptom Study app: a prospective, community-based, nested, case-control study. The Lancet Infectious Diseases. 2022; 22: 43–55
- Taquet M, Dercon Q, Harrison PJ. Six-month sequelae of post-vaccination SARS-CoV-2 infection: a retrospective cohort study of 10,024 breakthrough infections. 2021. DOI: 10.1101/2021.10.26.21265508. Available from: http://medrxiv.org/lookup/doi/10.1101/2021.10.26.21265508.
- Tran V-T, Perrodeau E, Saldanha J, Pane I, Ravaud P. Efficacy of COVID-19 vaccination on the symptoms of patients with long COVID: a target trial emulation using data from the ComPaRe e-cohort in France. 2022. DOI: 10.21203/rs.3.rs-1350429/ v1. Available from: https://www.researchsquare.com/article/rs1350429/v1\.
- Ashton RE, Philips BE, Faghy M. The acute and chronic implications of the COVID-19 virus on the cardiovascular system in adults: A systematic review. Prog Cardiovasc Dis. 2023; 76: 31–37. DOI: 10.1016/j.pcad.2023.01.003.
- Sandoval Y, Januzzi JL, Jr, Jaffe AS. Cardiac troponin for assessment of myocardial injury in COVID-19: JACC review topic of the week. J Am CollCardiol. 2020; 76: 1244–58.
- Carfi A, Bernabei R, Landi F, et al. Persistent symptoms in patients after acute COVID-19. JAMA. 2020; 324: 603–5.
- Logue JK, Franko NM, McCulloch DJ, et al. Sequelae in adults at 6 months after COVID-19 infection. JAMA Netw Open. 2021; 4.
- Giustino G, Croft LB, Stefanini GG, et al. Characterization of myocardial injury in patients with COVID-19. J Am CollCardiol. 2020; 76: 2043–55.
- Puntmann VO, Carerj ML, Wieters I, et al. Outcomes of cardiovascular magnetic resonance imaging in patients recently recovered from coronavirus disease 2019 (COVID-19) JAMA Cardiol. 2020; 5: 1265–73.
- O'Connor FG. COVID-19: Return to sport or strenuous activity following infection. UpToDate. Literature review current through: May 2022. This topic last updated: Mar 28, 2022.
- Ali-Ahmed F, Dalgaard F, Al-Khatib SM. Sudden cardiac death in patients with myocarditis: evaluation, risk stratification, and management. Am Heart J. 2020; 220: 29–40.
- Phelan D, Kim JH, Elliott MD, et al. Screening of potential cardiac involvement in competitive athletes recovering from COVID-19: an expert consensus statement. JACC Cardiovasc Imaging. 2020; 13 (12): 2635–52. DOI: 10.1016/j.jcmg.2020.10.005.
- Pelliccia A, Solberg EE, Papadakis M, et al. Recommendations for participation in competitive and leisure time sport in athletes with cardiomyopathies, myocarditis, and pericarditis: position statement of the Sport Cardiology Section of the European Association of Preventive Cardiology (EAPC). Eur Heart J. 2019; 40 (1): 19–33.
- Wilson MG, Hull JH, Rogers 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.
- Dove J, Gage A, Kriz P, Tabaddor RR, Owens BD. COVID-19 and review of current recommendations for return to athletic play. R I Med J. 2020; 103 (7): 15–20. Published 2020 Sep 1.
- Moulson N, Petek BJ, Drezner JA, et al. SARS-CoV-2 Cardiac Involvement in Young Competitive Athletes. Circulation. 2021; 144 (4): 256–66. DOI: 10.1161/CIRCULATIONAHA.121.054824.
- Kim JY, Han K, Suh YJ. Prevalence of abnormal cardiovascular magnetic resonance findings in recovered patients from COVID-19: a systematic review and meta-analysis. J Cardiovasc Magn Reson. 2021; 23 (1): 100. DOI: 10.1186/s12968-02100792-7.
- Van Hattum JC, Spies JL, Verwijs SM, et al. Cardiac abnormalities in athletes after SARS-CoV-2 infection: a systematic review. BMJ Open Sport Exerc Med. 2021; 7 (4): e001164. Published 2021 Oct 12. DOI: 10.1136/bmjsem-2021-001164.
- Kelle S, Bucciarelli-Ducci C, Judd RM, et al. Society for Cardiovascular Magnetic Resonance (SCMR) recommended CMR protocols for scanning patients with active or convalescent phase COVID-19 infection. J Cardiovasc Magn Reson. 2020; 22: 61.
- Małek LA, Bucciarelli-Ducci C. Myocardial fibrosis in athletesCurrent perspective. Clin Cardiol. 2020; 43 (8): 882–8.
- Ahmad SA, Khalid N, Shlofmitz E, Chhabra L. Myocardial fibrosis and arrhythmogenesis in elite athletes. Clin Cardiol. 2019; 42 (9): 788.
- Zhang CD, Xu SL, Wang XY, Tao LY, Zhao W, Gao W. Prevalence of myocardial fibrosis in intensive endurance training athletes: a systematic review and meta-analysis. Front Cardiovasc Med. 2020; 7: 585692.
- Rajpal S, Tong MS, Borchers J, et al. Cardiovascular magnetic resonance findings in competitive athletes recovering from COVID-19 infection. JAMA Cardiol. 2021; 6 (1): 116–8. DOI: 10.1001/jamacardio.2020.4916.
- Gluckman TJ, Bhave NM, Allen LA, et al. 2022 ACC Expert consensus decision pathway on cardiovascular sequelae of COVID-19 in adults: myocarditis and other myocardial involvement, post-acute sequelae of SARS-CoV-2 infection, and return to play: a report of the American College of Cardiology Solution Set Oversight Committee. J Am Coll Cardiol. 2022; 79 (17): 1717–56.
- Daniels CJ, Rajpal S, Greenshields JT, et al. Prevalence of clinical and subclinical myocarditis in competitive athletes with recent SARS-CoV-2 infection: results from the Big Ten COVID-19 Cardiac Registry. JAMA Cardiol. 2021; 6: 1078–87.
- Brito D, Meester S, Yanamala N, et al. High prevalenceof pericardial involvement in college studentathletes recovering from COVID-19. J Am Coll Cardiol Img. 2021; 14: 541–55.
- Clark DE, Parikh A, Dendy JM, et al. COVID-19 Myocardial Pathology Evaluation in Athletes With Cardiac Magnetic Resonance (COMPETE CMR). Circulation. 2021; 143: 609–12.
- Hwang CE, Kussman A, Christle JW, et al. Findingsfrom cardiovascular evaluation of National Collegiate Athletic Association Division I collegiate studentathletesafter asymptomatic or mildly symptomatic SARS-CoV-2 infection. Clin J Sport Med. Published online June 24, 2021.
- Starekova J, Bluemke DA, Bradham WS, et al. Evaluation for myocarditis in competitive student athletes recovering from coronavirus disease 2019 with cardiac magnetic resonance imaging. JAMA Cardiol. 2021; 6: 945–50.
- Martinez MW, Tucker AM, Bloom OJ, 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; 6: 745–52.
- Valverde I, Singh Y, Sanchez-de-Toledo J, et al. Acute cardiovascular manifestations in 286 children with multisystem inflammatory syndrome associated with COVID-19 infection in Europe. Circulation. 2021; 143: 21–32.
- Sirico D, Basso A, Reffo E, et al. Early echocardiographic and cardiac MRI findings in multisystem inflammatory syndrome in children. J Clin Med. 2021; 10 (15): 3360.
- Palabiyik F, Akcay N, Sevketoglu E, et al. Imaging of multisystem inflammatory disein children (MIS-C) associated With COVID-19. Acad Radiol. 2021; 28: 1200–8.
- Cavigli L, et al. A prospective study on the consequences of SARSCoV-2 infection on the heart of young adult competitive athletes: implications for a safe return-to-play. International journal of cardiology. 2021; 336: 130–6. DOI: 10.1016/j.ijcard.2021.05.042.
- Modica G, Bianco M, Sollazzo F, et al. Myocarditis in athletes recovering from COVID-19: a systematic review and metaanalysis. Int J Environ Res Public Health. 2022; 19 (7): 4279.
- Ibarrola M, Dávolos I. Myocarditis in athletes after COVID-19 infection: the heart is not the only place to screen. Sports Med Health Sci. 2020; 2: 172–3.
- Chevalier L, Cochet H, Mahida S, et al. ASCCOVID investigators. Resuming training in high-level athletes after mild COVID-19 infection: a multicenter prospective study (ASCCOVID-19). Sports Med Open. 2022; 8 (1): 83. DOI: 10.1186/s40798-022-00469-0.
- Gamal DM, Ibrahim RA, Samaan SF. Post COVID-19 syndrome in a prospective cohort study of Egyptian patients. Egypt Rheumatol Rehabil. 2022; 49 (1): 12. Available from: https://doi.org/10.1186/ s43166-021-00104-y.
- Nabavi N. Long COVID: how to define it and how to manage it. BMJ. 2020; 370: m3489. Published 2020 Sep 7. DOI: 10.1136/ bmj.m3489.
- Giusto E, Asplund CA. Persistent COVID and a return to sport. Curr Sports Med Rep. 2022; 21 (3): 100–4.
- Blitshteyn S, Whitelaw S. Postural orthostatic tachycardia syndrome (POTS) and other autonomic disorders after COVID-19 infection: a case series of 20 patients. Immunol Res. 2021; 69 (2): 205–11. DOI: 10.1007/s12026-021-09185-5.
- 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: 1085–6.
- Baggish A, Drezner JA, Kim J, Martinez M, Prutkin JM. The resurgence of sport in the wake of COVID-19: cardiac considerations in competitive athletes. Br J SportsMed. 2020; 54: 1130–1.
- Kim JH, Levine BD, Phelan D, et al. Coronavirus disease 2019 and the athletic heart: emerging perspectives on pathology, risks, and return to play. JAMA Cardiol. 2021; 6: 219–27.
- Feldstein LR, Rose EB, Horwitz SM, et al. Multisystem inflammatory syndrome in U.S. children and adolescents. N Engl J Med. 2020; 383: 334–46.
- Maron BJ, Udelson JE, Bonow RO. Eligibility and disqualification recommendations for competitive athletes with cardiovascular abnormalities: Task Force 3: hypertrophic cardiomyopathy, arrhythmogenic right ventricular cardiomyopathy and other cardiomyopathies, and myocarditis: a scientific statement from the American Heart Association and American College of Cardiology. J Am Coll Cardiol. 2015; 66: 2362–71.