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High Prevalence of Pericardial Involvement in College Student Athletes Recovering From COVID-19

Original Research

J Am Coll Cardiol Img, 14 (3) 541–555
Sections

Central Illustration

Abstract

Objectives

This study sought to explore the spectrum of cardiac abnormalities in student athletes who returned to university campus in July 2020 with uncomplicated coronavirus disease 2019 (COVID-19).

Background

There is limited information on cardiovascular involvement in young individuals with mild or asymptomatic COVID-19.

Methods

Screening echocardiograms were performed in 54 consecutive student athletes (mean age 19 years; 85% male) who had positive results of reverse transcription polymerase chain reaction nasal swab testing of the upper respiratory tract or immunoglobulin G antibodies against severe acute respiratory syndrome coronavirus type 2. Sequential cardiac magnetic resonance imaging was performed in 48 (89%) subjects.

Results

A total of 16 (30%) athletes were asymptomatic, whereas 36 (66%) and 2 (4%) athletes reported mild and moderate COVID-19 related symptoms, respectively. For the 48 athletes completing both imaging studies, abnormal findings were identified in 27 (56.3%) individuals. This included 19 (39.5%) athletes with pericardial late enhancements with associated pericardial effusion. Of the individuals with pericardial enhancements, 6 (12.5%) had reduced global longitudinal strain and/or an increased native T1. One patient showed myocardial enhancement, and reduced left ventricular ejection fraction or reduced global longitudinal strain with or without increased native T1 values was also identified in an additional 7 (14.6%) individuals. Native T2 findings were normal in all subjects, and no specific imaging features of myocardial inflammation were identified. Hierarchical clustering of left ventricular regional strain identified 3 unique myopericardial phenotypes that showed significant association with the cardiac magnetic resonance findings (p = 0.03).

Conclusions

More than 1 in 3 previously healthy college athletes recovering from COVID-19 infection showed imaging features of a resolving pericardial inflammation. Although subtle changes in myocardial structure and function were identified, no athlete showed specific imaging features to suggest an ongoing myocarditis. Further studies are needed to understand the clinical implications and long-term evolution of these abnormalities in uncomplicated COVID-19.

  • 1. Huang L., Zhao P., Tang D., et al. "Cardiac involvement in patients recovered from COVID-2019 identified using magnetic resonance imaging". J Am Coll Cardiol Img 2020;13:2330-2339.

    View ArticleGoogle Scholar
  • 2. Wang Y., Wang Y., Chen Y., Qin Q. "Unique epidemiological and clinical features of the emerging 2019 novel coronavirus pneumonia (COVID-19) implicate special control measures". J Med Virol 2020;92:568-576.

    CrossrefMedlineGoogle Scholar
  • 3. Zhou F., Yu T., Du R., et al. "Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study". Lancet 2020;395:1054-1062.

    CrossrefMedlineGoogle Scholar
  • 4. Puntmann V.O., Carerj M.L., Wieters I., et al. "Outcomes of cardiovascular magnetic resonance imaging in patients recently recovered from coronavirus disease 2019 (COVID-19)". JAMA Cardiol 2020;5:1265-1273.

    CrossrefMedlineGoogle Scholar
  • 5. Rajpal S., Tong M.S., Borchers J., et al. "Cardiovascular magnetic resonance findings in competitive athletes recovering from COVID-19 infection". JAMA Cardiol 2021;6:116-118.

    MedlineGoogle Scholar
  • 6. Lisboa Bastos M., Tavaziva G., Abidi S.K., et al. "Diagnostic accuracy of serological tests for COVID-19: systematic review and meta-analysis". BMJ 2020;370:m2516.

    CrossrefMedlineGoogle Scholar
  • 7. Centers for Disease Control and Prevention. "Coronavirus disease 2019 (COVID-19): symptoms of coronavirus". 2020. Available at: https://www.cdc.gov/coronavirus/2019-ncov/symptoms-testing/symptoms.html. Accessed November 4, 2020.

    Google Scholar
  • 8. World Medical Association. "World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects". JAMA 2013;310:2191-2194.

    CrossrefMedlineGoogle Scholar
  • 9. Lang R.M., Badano L.P., Mor-Avi V., et al. "Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging". J Am Soc Echocardiogr 2015;28:1-39.e14.

    CrossrefMedlineGoogle Scholar
  • 10. Rudski L.G., Lai W.W., Afilalo J., et al. "Guidelines for the echocardiographic assessment of the right heart in adults: a report from the American Society of Echocardiography endorsed by the European Association of Echocardiography, a registered branch of the European Society of Cardiology, and the Canadian Society of Echocardiography". J Am Soc Echocardiogr 2010;23:685-713.quiz 786–8.

    CrossrefMedlineGoogle Scholar
  • 11. Baggish A.L., Battle R.W., Beaver T.A., et al. "Recommendations on the use of multimodality cardiovascular imaging in young adult competitive athletes: a report from the American Society of Echocardiography in Collaboration with the Society of Cardiovascular Computed Tomography and the Society for Cardiovascular Magnetic Resonance". J Am Soc Echocardiogr 2020;33:523-549.

    CrossrefMedlineGoogle Scholar
  • 12. Phelan D., Kim J., Elliott M., et al. "Screening potential cardiac involvement in young athletes recovering from COVID-19: an international expert consensus statement". J Am Coll Cardiol Img 2020;13:2635-2652.

    View ArticleGoogle Scholar
  • 13. Addis D.R., Townsley M.M. "Imaging considerations for the athletically conditioned heart: an echocardiography-focused overview of the 2020 American Society of Echocardiography recommendations on the use of multimodality cardiovascular imaging in young adult competitive athletes". J Cardiothorac Vasc Anesth 2020;34:2867-2870.

    CrossrefMedlineGoogle Scholar
  • 14. Wiesmueller M., Wuest W., Heiss R., Treutlein C., Uder M., May M.S. "Cardiac T2 mapping: robustness and homogeneity of standardized in-line analysis". J Cardiovasc Magn Reson 2020;22:39.

    CrossrefMedlineGoogle Scholar
  • 15. Piechnik S.K., Ferreira V.M., Dall’Armellina E., et al. "Shortened modified look-locker inversion recovery (ShMOLLI) for clinical myocardial T1-mapping at 1.5 and 3 T within a 9 heartbeat breathhold". J Cardiovasc Magn Reson 2010;12:69.

    CrossrefMedlineGoogle Scholar
  • 16. Messroghli D.R., Moon J.C., Ferreira V.M., et al. "Clinical recommendations for cardiovascular magnetic resonance mapping of T1, T2, T2∗ and extracellular volume: a consensus statement by the Society for Cardiovascular Magnetic Resonance (SCMR) endorsed by the European Association for Cardiovascular Imaging (EACVI)". J Cardiovasc Magn Reson 2017;19:75.

    CrossrefMedlineGoogle Scholar
  • 17. von Knobelsdorff-Brenkenhoff F., Schuler J., Doganguzel S., et al. "Detection and monitoring of acute myocarditis applying quantitative cardiovascular magnetic resonance". Circ Cardiovasc Imaging 2017;10:e005242.

    CrossrefGoogle Scholar
  • 18. Mei Y., Weinberg S.E., Zhao L., et al. "Risk stratification of hospitalized COVID-19 patients through comparative studies of laboratory results with influenza". EClinicalMedicine 2020;26:100475.

    CrossrefMedlineGoogle Scholar
  • 19. Ferreira V.M., Schulz-Menger J., Holmvang G., et al. "Cardiovascular magnetic resonance in nonischemic myocardial inflammation: expert recommendations". J Am Coll Cardiol 2018;72:3158-3176.

    View ArticleGoogle Scholar
  • 20. National Institutes of Health. "COVID-19 treatment guidelines panel. coronavirus disease 2019 (COVID-19) treatment guidelines". Available at: https://www.covid19treatmentguidelines.nih.gov/. Accessed August 25, 2020.

    Google Scholar
  • 21. Feldstein L.R., Rose E.B., Horwitz S.M., et al. "Multisystem inflammatory syndrome in U.S. children and adolescents". N Engl J Med 2020;383:334-346.

    CrossrefMedlineGoogle Scholar
  • 22. Ackermann M., Verleden S.E., Kuehnel M., et al. "Pulmonary vascular endothelialitis, thrombosis, and angiogenesis in Covid-19". N Engl J Med 2020;383:120-128.

    CrossrefMedlineGoogle Scholar
  • 23. Sousa I.R.F., Pereira I.C.C., Morais L.J., Teodoro L., Rodrigues M.L.P., Gomes R. "Pericardial parietal mesothelial cells: source of the angiotensin-converting-enzyme of the bovine pericardial fluid". Arq Bras Cardiol 2017;109:425-431.

    MedlineGoogle Scholar
  • 24. Chao C.J., DeValeria P.A., Sen A., et al. "Reversible cardiac dysfunction in severe COVID-19 infection, mechanisms and case report". Echocardiography 2020;37:1465-1469.

    CrossrefMedlineGoogle Scholar
  • 25. Goerlich E., Gilotra N.A., Minhas A.S., Bavaro N., Hays A.G., Cingolani O.H. "Prominent longitudinal strain reduction of basal left ventricular segments in patients with COVID-19". J Card Fail 2021;27:100-104.

    CrossrefMedlineGoogle Scholar
  • 26. Lairez O., Blanchard V., Houard V., et al. "Cardiac imaging phenotype in patients with coronavirus disease 2019 (COVID-19): results of the cocarde study". Int J Cardiovasc Imaging 2020Sep9. [E-pub ahead of print].

    CrossrefGoogle Scholar
  • 27. Perez-Bermejo J.A., Kang S., Rockwood S.J., et al. "SARS-CoV-2 infection of human iPSC-derived cardiac cells predicts novel cytopathic features in hearts of COVID-19 patients". bioRxiv [Pre-print] 2020Sep12. 2020.08.25.265561.

    Google Scholar
  • 28. Kasner M., Aleksandrov A., Escher F., et al. "Multimodality imaging approach in the diagnosis of chronic myocarditis with preserved left ventricular ejection fraction (MCpEF): the role of 2D speckle-tracking echocardiography". Int J Cardiol 2017;243:374-378.

    CrossrefMedlineGoogle Scholar
  • 29. Leitman M., Vered Z., Tyomkin V., et al. "Speckle tracking imaging in inflammatory heart diseases". Int J Cardiovasc Imaging 2018;34:787-792.

    MedlineGoogle Scholar
  • 30. Uzieblo-Zyczkowska B., Mielniczuk M., Ryczek R., Krzesinski P. "Myocarditis successfully diagnosed and controlled with speckle tracking echocardiography". Cardiovasc Ultrasound 2020;18:19.

    CrossrefMedlineGoogle Scholar
  • 31. Meyer P., Degrauwe S., Van Delden C., Ghadri J.R., Templin C. "Typical takotsubo syndrome triggered by SARS-CoV-2 infection". Eur Heart J 2020;41:1860.

    CrossrefMedlineGoogle Scholar
  • 32. Imazio M., Pivetta E., Palacio Restrepo S., et al. "Usefulness of cardiac magnetic resonance for recurrent pericarditis". Am J Cardiol 2020;125:146-151.

    CrossrefMedlineGoogle Scholar
  • 33. Cremer P.C., Kumar A., Kontzias A., et al. "Complicated pericarditis: understanding risk factors and pathophysiology to inform imaging and treatment". J Am Coll Cardiol 2016;68:2311-2328.

    View ArticleGoogle Scholar
  • 34. Escher F., Westermann D., Gaub R., et al. "Development of diastolic heart failure in a 6-year follow-up study in patients after acute myocarditis". Heart 2011;97:709-714.

    CrossrefMedlineGoogle Scholar
  • 35. Zorzi A., Perazzolo Marra M., Rigato I., et al. "Nonischemic left ventricular scar as a substrate of life-threatening ventricular arrhythmias and sudden cardiac death in competitive athletes". Circ Arrhythm Electrophysiol 2016;9:e004229.

    CrossrefGoogle Scholar
  • 36. La Gerche A., Baggish A.L., Knuuti J., et al. "Cardiac imaging and stress testing asymptomatic athletes to identify those at risk of sudden cardiac death". J Am Coll Cardiol Img 2013;6:993-1007.

    View ArticleGoogle Scholar
  • 37. Mavrogeni S., Bratis C., Kitsiou A., et al. "CMR assessment of myocarditis in patients with cardiac symptoms during H1N1 viral infection". J Am Coll Cardiol Img 2011;4:307-309.

    View ArticleGoogle Scholar
  • 38. McDiarmid A.K., Swoboda P.P., Erhayiem B., et al. "Athletic cardiac adaptation in males is a consequence of elevated myocyte mass". Circ Cardiovasc Imaging 2016;9:e003579.

    CrossrefMedlineGoogle Scholar
  • 39. Domenech-Ximenos B., Sanz-de la Garza M., Prat-Gonzalez S., et al. "Prevalence and pattern of cardiovascular magnetic resonance late gadolinium enhancement in highly trained endurance athletes". J Cardiovasc Magn Reson 2020;22:62.

    CrossrefMedlineGoogle Scholar