Parametric Mapping Cardiac Magnetic Resonance Imaging for the Diagnosis of Myocarditis in Children in the Era of COVID-19 and MIS-C

Bibhuti B Das, Jyothsna Akam-Venkata, Mubeena Abdulkarim, Tarique Hussain, Bibhuti B Das, Jyothsna Akam-Venkata, Mubeena Abdulkarim, Tarique Hussain

Abstract

Myocarditis comprises many clinical presentations ranging from asymptomatic to sudden cardiac death. The history, physical examination, cardiac biomarkers, inflammatory markers, and electrocardiogram are usually helpful in the initial assessment of suspected acute myocarditis. Echocardiography is the primary tool to detect ventricular wall motion abnormalities, pericardial effusion, valvular regurgitation, and impaired function. The advancement of cardiac magnetic resonance (CMR) imaging has been helpful in clinical practice for diagnosing myocarditis. A recent Scientific Statement by the American Heart Association suggested CMR as a confirmatory test to diagnose acute myocarditis in children. However, standard CMR parametric mapping parameters for diagnosing myocarditis are unavailable in pediatric patients for consistency and reliability in the interpretation. The present review highlights the unmet clinical needs for standard CMR parametric criteria for diagnosing acute and chronic myocarditis in children and differentiating dilated chronic myocarditis phenotype from idiopathic dilated cardiomyopathy. Of particular relevance to today's practice, we also assess the potential and limitations of CMR to diagnose acute myocarditis in children exposed to severe acute respiratory syndrome coronavirus-2 infections. The latter section will discuss the multi-inflammatory syndrome in children (MIS-C) and mRNA coronavirus disease 19 vaccine-associated myocarditis.

Keywords: COVID-19; cardiac MRI; children; mRNA COVID-19 vaccine; multisystem inflammatory syndrome in children; myocarditis.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
T1 mapping demonstrates a global increase in myocardial T1 relaxation times at the base (A), mid-ventricular level (B), and the apex (C). The average left ventricular myocardial T1 relaxation time is prolonged (1067 ms), and myocardial extracellular volume is elevated (32%).
Figure 2
Figure 2
T2 mapping demonstrating the regional increase in myocardial T2 relaxation times at the basal anteroseptal and anterolateral segments (A), with normal T2 times at the mid-ventricular level (B) and the apex (C). Clinical vignette: A 20-month-old female with myocarditis associated with rhino/enterovirus, rapid left ventricular ejection fraction recovery from 24% to 48%, elevated troponin, and diffuse low voltage QRS complexes on electrocardiogram. There was no evidence of myocardial delayed enhancement after gadolinium contrast emphasizing the additional utility of T1 and T2 mapping in the evaluation of myocarditis.
Figure 3
Figure 3
Late gadolinium enhancement (LGE) imaging allows the noninvasive visualization of areas affected by myocardial scar, conferring clinicians the unique ability to differentiate ischemic from nonischemic lesions based on typical LGE patterns.
Figure 4
Figure 4
CMR in an adolescent with acute myocarditis: (A) Shows subepicardial early gadolinium enhancement (EGE) (white arrow); (B) Shows subepicardial LGE (white arrow).
Figure 5
Figure 5
T1 mapping demonstrating the global increase in myocardial T1 relaxation times at the base (A), mid-ventricular level (B), and the apex (C). The average left ventricular myocardial T1 relaxation time is mildly prolonged (1077 ms).
Figure 6
Figure 6
T2 mapping demonstrating normal myocardial T2 relaxation times at the base (A), mid-ventricular level (B), and at the apex (C). Clinical vignette: 12-year-old female with possible chronic myocarditis associated with Parvovirus B19, dilated LV with decreased LVEF 22%.
Figure 7
Figure 7
Several putative mechanisms of myocarditis due to SARS-CoV-2 and other common cardiotropic viruses.
Figure 8
Figure 8
LGE in the mid myocardium of the inferior and lateral wall (white arrows). Clinical vignette: 15-year-old-female soccer player with COVID-19-associated myocarditis. This subject reported shortness of breath and chest pain with activity and was found to have ventricular ectopy and non-sustained runs of ventricular tachycardia on Holter monitoring.
Figure 9
Figure 9
CMR shows no LGE (A) but diffusely elevated T1 time (B).
Figure 10
Figure 10
A 16-year-old-male with mRNA COVID-19 vaccine-associated myocarditis. (A) subepicardial LGE (white arrow); (B) subepicardial LGE (white arrow); (C) early gadolinium enhancement (EGE) (white arrow); and (D) shows enhanced T2 signal (white arrow).

References

    1. Klugman D., Berger J.T., Sable C.A., He J., Khandelwal S.G., Slonim A.D. Pediatric patients hospitalized with myocarditis: A multi-institutional analysis. Pediatric Cardiol. 2010;31:222–228. doi: 10.1007/s00246-009-9589-9.
    1. Ghelani Sunil J., Spaeder Michael C., Pastor W., Spurney Christopher F., Klugman D. Demographics, Trends, and Outcomes in Pediatric Acute Myocarditis in the United States, 2006 to 2011. Circ. Cardiovasc. Qual. Outcomes. 2012;5:622–627. doi: 10.1161/CIRCOUTCOMES.112.965749.
    1. Rodriguez-Gonzalez M., Sanchez-Codez M.I., Lubian-Gutierrez M., Castellano-Martinez A. Clinical presentation and early predictors for poor outcomes in pediatric myocarditis: A retrospective study. World J. Clin. Cases. 2019;7:548–561. doi: 10.12998/wjcc.v7.i5.548.
    1. Canter C.E., Simpson K.E. Diagnosis and treatment of myocarditis in children in the current era. Circulation. 2014;129:115–128. doi: 10.1161/CIRCULATIONAHA.113.001372.
    1. Dasgupta S., Iannucci G., Mao C., Clabby M., Oster M.E. Myocarditis in the pediatric population: A review. Cong Heart Dis. 2019;14:868–877. doi: 10.1111/chd.12835.
    1. Bejiqi R., Retkoceri R., Maloku A., Mustafa A., Bejiqi H., Bejiqi R. The diagnostic and clinical approach to pediatric myocarditis: A review of the current literature. Open Access Maced. J. Med. Sci. 2019;7:162–173. doi: 10.3889/oamjms.2019.010.
    1. Martinez-Villar M., Gran F., Sabaté-Rotés A., Tello-Montoliu A., Castellote A., Figueras-Coll M., Ferrer Q., Roses-Noguer F. Acute myocarditis with infarct-like presentation in a pediatric population: Role of cardiovascular magnetic resonance. Pediatric Cardiol. 2018;39:51–56. doi: 10.1007/s00246-017-1726-2.
    1. Abrar S., Ansari M.J., Mittal M., Kushwaha K.P. Predictors of mortality in pediatric myocarditis. J. Clin. Diagn. Res. 2016;10:Sc12–Sc16.
    1. Kociol R.D., Cooper L.T., Fang J.C. recognition and initial management of fulminant myocarditis: A scientific statement from the American Heart Association. Circulation. 2020;141:e69–e92. doi: 10.1161/CIR.0000000000000745.
    1. Law Y.M., Lal A.K., Chen S., Cihakova D., Cooper L.T., Deshpande S., Godown J., Grosse-Wortmann L., Robinson J.D., Towbin J.A., et al. American Heart Association Pediatric Heart Failure and Transplantation Committee of the Council on Lifelong Congenital Heart Disease and Heart Health in the Young and Stroke Council. Diagnosis and management of myocarditis in children: A scientific statement from the American Heart Association. Circulation. 2021;144:e123–e135.
    1. Ammirati E., Frigerio M., Adler E., Basso C., Birnie D.H., Brambatti M., Hare J.M., Heidecker B., Heymans S., Hubner N., et al. Management of acute myocarditis and chronic inflammatory cardiomyopathy: An expert consensus document. Circ. Heart Fail. 2020;13:e007405. doi: 10.1161/CIRCHEARTFAILURE.120.007405.
    1. McNamara D.M., Starling R.C., Cooper L.T., Boehmer J.P., Mather P.J., Janosko K.M., Gorscan J., 3rd, Kip K.E., Dec G.W. Clinical and demographic predictors of outcomes in recent-onset dilated cardiomyopathy. Results of the IMAC (Intervention in Myocarditis and Acute Cardiomyopathy)-2 study. J. Am. Coll. Cardiol. 2011;58:1112–1118. doi: 10.1016/j.jacc.2011.05.033.
    1. Caforio A.L.P., Pankuweit S., Arbustini E., Basso C., Gimeno-Blanes J., Felix S.B., Fu M., Heliö T., Heymans S., Jahns R., et al. Current state of knowledge on aetiology, diagnosis, management, and therapy of myocarditis: A position statement of the European Society of Cardiology Working Group on Myocardial and Pericardial Diseases. Eur. Heart J. 2013;34:2636–4814. doi: 10.1093/eurheartj/eht210.
    1. Tschope C., Ammirati E., Bozkurt B., Caforio A.L.P., Cooper L.T., Felix S.B., Hare J.M., Heidecker B., Heymans S., Hübner N., et al. Myocarditis and inflammatory cardiomyopathy: Current evidence and future directions. Nat. Rev. Cardiol. 2021;18:169–193. doi: 10.1038/s41569-020-00435-x.
    1. Klein A.L., Abbara S., Agler D.A., Appleton C.P., Asher C.R., Hoit B., Hung J., Garcia M.J., Kronzon I., Oh J.K., et al. American Society of Echocardiography clinical recommendations for multimodality cardiovascular imaging of patients with pericardial disease. J. Am. Soc. Echocardiogr. 2013;26:965–1012. doi: 10.1016/j.echo.2013.06.023.
    1. Friedrich M.G., Sechtem U., Schulz-Menger J., Holmvang G., Alakija P., Cooper L.T., Liu P., White J.A., Abdel-Aty H., Gutberlet M., et al. Cardiovascular magnetic resonance in myocarditis: A JACC white paper. J. Am. Coll. Cardiol. 2009;53:1475–1487. doi: 10.1016/j.jacc.2009.02.007.
    1. Wei S., Fu J., Chen L., Yu S. Performance of cardiac magnetic resonance imaging for diagnosis of myocarditis compared with endomyocardial biopsy. Med. Sci. Monit. 2017;23:3687–3696. doi: 10.12659/MSM.902155.
    1. Pan J.A., Lee Y.J., Salerno M. Diagnostic performance of extracellular volume, native T1, and T2 mapping versus lake Louis criteria by cardiac magnetic resonance for detection of acute myocarditis: A meta-analysis. Circ. Cardiovasc. Imaging. 2018;11:e007598. doi: 10.1161/CIRCIMAGING.118.007598.
    1. Ferreira V.M., Schulz-Menger J., Holmvang G., Kramer C.M., Carbone I., Sechtem U., Kinderman I., Gutberlet M., Cooper L.T., Liu P., et al. Cardiovascular magnetic resonance in nonischemic myocardial inflammation: Expert recommendations. J. Am. Coll. Cardiol. 2018;72:3158–3176. doi: 10.1016/j.jacc.2018.09.072.
    1. Luetkens J.A., Faron A., Isaak A., Kuetting D., Gliem C., Dabir D., Kornblum C., Thomas D. Comparison of original and 2018 Lake Louise criteria for diagnosis of acute myocarditis: Results of a validation cohort. Radiol. Cardiothorac. Imaging. 2019;1:e190010. doi: 10.1148/ryct.2019190010.
    1. Isaak A., Bischoff L., Faron A., Endler C., Mesropyan N., Sprinkart A., Peiper C.C., Kuetting D., Dabir D., Attenberger U., et al. Multiparametric cardiac magnetic resonance imaging in pediatric and adolescent patients with acute myocarditis. Pediatric Radiol. 2021;51:2470–2480. doi: 10.1007/s00247-021-05169-7.
    1. Cornicelli M.D., Rigsby C.K., Rychlik K., Pahl E., Robinson J.D. Diagnostic performance of cardiovascular magnetic resonance native T1 and T2 mapping in pediatric patients with acute myocarditis. J. Cardiovasc. Magn. Reson. 2019;21:40. doi: 10.1186/s12968-019-0550-7.
    1. Hales-Kharazmi A., Hirsch N., Slesnik T., Deshpande S.R. Utility of cardiac MRI in pediatric myocarditis. Cardiol. Young. 2018;3:377–385. doi: 10.1017/S1047951117001093.
    1. Banka P., Robinson J.D., Uppu S.C., Harris M.A., Hasbani K., Lai W.W., Richmond M., Fratzz S., Jain S., Johnson T.R., et al. Cardiovascular magnetic resonance techniques and findings in children with myocarditis: A multicenter retrospective study. J. Cardiovasc. Magn. Reson. 2015;17:96. doi: 10.1186/s12968-015-0201-6.
    1. Chinali M., Franceschini A., Ciancarella P., Lisignoli V., Curione D., Ciliberti P., Esposito C., Pasqua A.D., Rinelli G., Secinaro A. Echocardiographic two-dimensional speckle tracking identifies acute regional myocardial edema and sub-acute fibrosis in pediatric focal myocarditis with normal ejection fraction: Comparison with cardiac magnetic resonance. Sci. Rep. 2020;10:11321. doi: 10.1038/s41598-020-68048-5.
    1. Francone M., Chimenti C., Galea N., Scopelliti F., Verardo R., Galea R., Carbone I., Catalano C., Fedele F., Frustaci A. CMR sensitivity varies with clinical presentation and extent of cell necrosis in biopsy-proven acute myocarditis. JACC Cardiovasc. Imaging. 2014;7:254–263. doi: 10.1016/j.jcmg.2013.10.011.
    1. Yuan W.-F., Zhao X.-X., Sun W.-J., Shao-Ping W., Ya-Bin L., Tang X. LGE-MRI in the assessment of left ventricular remodeling in myocarditis. Curr. Med. Imaging. 2019;15:900–905. doi: 10.2174/1573405614666180912100253.
    1. Martins D.S., Ait-Ali L., Khraiche D., Festa P., Barison A., Martini N., Benadjaoud Y., Anjos R., Boddaert N., Bonnet D., et al. Evolution of acute myocarditis in a pediatric population: An MRI based study. Int. J. Cardiol. 2021;329:226–233. doi: 10.1016/j.ijcard.2020.12.052.
    1. Grigoratus C., Bella G.D., Aquaro G.D. Diagnostic and prognostic role of cardiac magnetic resonance in acute myocarditis. Heart Fail. Rev. 2019;24:81–90. doi: 10.1007/s10741-018-9724-x.
    1. Dusenbery S.M., Newburger J.W., Colan S.D., Gauvreau K., Baker A., Powell A.J. Myocardial fibrosis in patients with a history of Kawasaki disease. IJC Heart Vasc. 2021;32:100713. doi: 10.1016/j.ijcha.2021.100713.
    1. Secinaro A., Ntsinjana H., Tann O., Schuler P.K., Muthurangu V., Hughes M., Tsang V., Taylor A.M. Cardiovascular magnetic resonance findings in repaired anomalous left coronary artery to pulmonary artery connection (ALCAPA) J. Cardiovasc. Magn. Reson. 2011;1391:27. doi: 10.1186/1532-429X-13-27.
    1. Mahrholdt H., Wagner A., Deluigi C.C., Kispert E., Hager S., Meinhardt G., Vogelseberg H., Fritz P., Dippon J., C-Thomas B., et al. Presentation, patterns of myocardial damage, and clinical course of viral myocarditis. Circulation. 2006;114:1581–1590. doi: 10.1161/CIRCULATIONAHA.105.606509.
    1. Saeed M., Hetts S.W., Jablonowski R., Wilson M.W. Magnetic resonance imaging and multi-detector computed tomography assessment of extracellular compartment in ischemic and nonischemic myocardial pathologies. World J. Cardiol. 2014;6:1192–1218. doi: 10.4330/wjc.v6.i11.1192.
    1. Messroghli D.R., Moon J.C., Ferreira V.M., Grosse-Wortmann L., He T., Kellman P. 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.
    1. Gagliardi M.G., Bevilacqua M., Di Renzi P., Picardo S., Passariello R., Marcelletti C. Usefulness of magnetic resonance imaging for diagnosis of acute myocarditis in infants and children, and comparison with endomyocardial biopsy. Am. J. Cardiol. 1991;68:1089–1091. doi: 10.1016/0002-9149(91)90501-B.
    1. Dubey S., Agarwal A., Nguyen S., Adebo D. Persistence of late gadolinium enhancement on follow-up CMR imaging in children with acute myocarditis. Pediatric Cardiol. 2020;41:1777–1782. doi: 10.1007/s00246-020-02445-5.
    1. Lurz P., Luecke C., Eitel I., Fohrenbach F., Frank C., Grothoff M., de Waha S., Rommel K.P., Lurz J.A., Klingel K., et al. Comprehensive cardiac magnetic resonance imaging in patients with suspected myocarditis: The MyoRacer-Trial. J. Am. Coll. Cardiol. 2016;67:1800–1811. doi: 10.1016/j.jacc.2016.02.013.
    1. Cooper L.T., Baughman K.L., Feldman A.M., Frustaci A., Jessup M., American Heart Association. American College of Cardiology. European Society of Cardiology. Heart Failure Society of America. Heart Failure Association of the European Society of Cardiology The role of endomyocardial biopsy in the management of cardiovascular disease: A scientific statement from the American Heart Association, the American College of Cardiology, and the European Society of Cardiology. Endorsed by the Heart Failure Society of America and the Heart Failure Association of the European Society of Cardiology. J. Am. Coll. Cardiol. 2007;50:1914–1931.
    1. Brambatti M., Matassini M.V., Adler E.D., Klingel K., Camici P.G., Ammirati E. Eosinophilic myocarditis characteristics, treatment, and outcomes. J. Am. Coll. Cardiol. 2017;70:2363–2375. doi: 10.1016/j.jacc.2017.09.023.
    1. Frustaci A., Russo M.A., Chimenti C. Randomized study on the efficacy of immunosuppressive therapy in patients with virus-negative inflammatory cardiomyopathy: The TIMIC study. Eur. Heart J. 2009;30:1995–2002. doi: 10.1093/eurheartj/ehp249.
    1. Baccouche H., Mahrholdt H., Meinhardt G., Merher R., Voehringer M., Hill S., Klingel K., Kanndolf R., Sechtem U., Yilmaz A. Diagnostic synergy of noninvasive cardiovascular magnetic resonance and invasive endomyocardial biopsy in troponin-positive patients without coronary artery disease. Eur. Heart J. 2009;30:2869–2879. doi: 10.1093/eurheartj/ehp328.
    1. Windram J., Grosse-Wortmann L., Shariat M., Greer M.-L., Crawford M.W., Yoo S.-J. Cardiovascular MRI without sedation or general anesthesia using a feed-and-sleep technique in neonates and infants. Pediatric Radiol. 2012;42:183–187. doi: 10.1007/s00247-011-2219-8.
    1. Fogel M.A., Weinberg P.M., Parave E., Harris C., Montenegro L., Harris M.A., Concepcion M. Deep sedation for cardiac magnetic resonance imaging: A comparison with cardiac anesthesia. J. Pediatric. 2008;152:534–539. doi: 10.1016/j.jpeds.2007.08.045.
    1. Odegard K.C., DiNardo J.A., Tsai-Goodman B., Powell A.J., Geva T., Laussen P.C. Anesthesia considerations for cardiac MRI in infants and small children. Pediatric Anesth. 2004;14:471–476. doi: 10.1111/j.1460-9592.2004.01221.x.
    1. Stockton E., Hughes M., Broadhead M., Taylor A., McEwan A. A prospective audit of safety issues associated with general anesthesia for pediatric cardiac magnetic resonance imaging. Paediatr. Anaesth. 2012;22:1087–1093. doi: 10.1111/j.1460-9592.2012.03833.x.
    1. Sarikouch S., Schaeffler R., Körperich H., Dongas A., Haas N.A., Beerbaum P. Cardiovascular magnetic resonance imaging for intensive care infants: Safe and effective? Pediatric Cardiol. 2009;30:146–152. doi: 10.1007/s00246-008-9295-z.
    1. Mitchell F.M., Prasad S.K., Greil G.F., Drivas P., Vassiliou V.S., Raphael C.E. Cardiovascular magnetic resonance: Diagnostic utility and specific considerations in the pediatric population in children: Review Paper. World J. Clin. Pediatric. 2016;5:1. doi: 10.5409/wjcp.v5.i1.1.
    1. Hinojar R., Foote L., Ucar E.A., Jackson T., Jabbour A., Yu C.-Y., mcChohon J., Higgins D.M., Carr-White G., Mayr M., et al. Native T1 in discrimination of acute and convalescent stages in patients with clinical diagnosis of myocarditis: A proposed diagnostic algorithm using CMR. JACC Cardiovasc. Imaging. 2015;8:37–46. doi: 10.1016/j.jcmg.2014.07.016.
    1. Bohnen S., Radunski U.K., Lund G.K., Kandolf R., Stehning C., Schnackenburg B., Adam G., Blankenberg S., Muellerleile K. Performance of T1 and T2 mapping cardiovascular magnetic resonance to detect active myocarditis in patients with recent-onset heart failure. Circ. Cardiovasc. Imaging. 2015;8:e003073. doi: 10.1161/CIRCIMAGING.114.003073.
    1. Latus H., Gummel K., Klingel K., Moysich A., Khalil M., Mazhari N., Bauer J., Kandolf R., Schranz D., Apitz C. Focal myocardial fibrosis assessed by late gadolinium enhancement cardiovascular magnetic resonance in children and adolescents with dilated cardiomyopathy. J. Cardiovasc. Magn. Reson. 2015;17:34. doi: 10.1186/s12968-015-0142-0.
    1. Grun S., Schumm J., Greulich S., Wagner A., Schneider S., Burder O., Kispert E.M., Hill S., Ong P., Klingel K., et al. Long-term follow-up of biopsy-proven myocarditis: Predictors of mortality and incomplete recovery. J. Am. Coll. Cardiol. 2012;59:1604–1615. doi: 10.1016/j.jacc.2012.01.007.
    1. Ait-Ali L., Martins D.S., Khraiche D., Festa P., Barison A., Martini N., Benadjaoud Y., Anjos R., Boddaert N., Bonnet D., et al. Cardiac MRI prediction of recovery in children with acute myocarditis. JACC Cardiovasc. Imaging. 2021;14:693–695. doi: 10.1016/j.jcmg.2020.08.033.
    1. Baessler B., Luecke C., Lurz J., Klingel K., Das A., von Roeder M., de Waha-Thiele S., Besler C., Rommel K.-P., Mantiz D., et al. Cardiac MRI and texture analysis of myocardial T1 and T2 maps in myocarditis with acute versus chronic symptoms of heart failure. Radiology. 2019;292:608–617. doi: 10.1148/radiol.2019190101.
    1. Foerster S.R., Canter C.E., Cinar A., Sleeper L.A., Webber S.A., Pahl E., Kantor P.F., Alvarez J.A., Colan S.D., Jefferies J.L., et al. Ventricular remodeling and survival are more favorable for myocarditis than for idiopathic dilated cardiomyopathy in childhood: An outcomes study from the Pediatric Cardiomyopathy Registry. Circ. Heart Fail. 2010;3:689–697. doi: 10.1161/CIRCHEARTFAILURE.109.902833.
    1. Lurz P., Eitel I., Adam J., Steiner J., Grothoff M., Desch S., Fuernau G., de Eaha S., Sareban M., Luecke C., et al. Diagnostic performance of CMR imaging compared with EMB in patients with suspected myocarditis. JACC Cardiovasc. Imaging. 2012;5:513–524. doi: 10.1016/j.jcmg.2011.11.022.
    1. Aquaro G.D., Ghebru Habtemicael Y., Camastra G., Monti L., Dellegrottaglie S., Moro C., Lanzillo C., Scatteia A., Di Roma M., Pontone G., et al. “Cardiac Magnetic Resonance” Working Group of the Italian Society of Cardiology. Prognostic value of repeating cardiac magnetic resonance in patients with acute myocarditis. J. Am. Coll. Cardiol. 2019;74:2439–2448. doi: 10.1016/j.jacc.2019.08.1061.
    1. Buckley B.J.R., Harrison S.L., Fazio-Eynullayeva E., Underhill P., Lane D.A., Lip G.Y.H. Prevalence and clinical outcomes of myocarditis and pericarditis in 718,365 COVID-19 patients. Eur. J. Clin. Investig. 2021;51:e13679. doi: 10.1111/eci.13679.
    1. Shi S., Qin M., Shen B., Cai Y., Liu T., Yang F., Gong W., Liu X., Liang J., Zhao Q., et al. Association of cardiac injury with mortality in hospitalized patients with COVID-19 in Wuhan, China. JAMA Cardiol. 2020;5:802–810. doi: 10.1001/jamacardio.2020.0950.
    1. Tavazzi G., Pellegrini C., Maurelli M., Belliato M., Sciutti F., Bottazzi A., Sepe P.A., Resasco T., Camporotondo R., Bruno R., et al. Myocardial localization of coronavirus in COVID-19 cardiogenic shock. Eur. J. Heart Fail. 2020;22:911–915. doi: 10.1002/ejhf.1828.
    1. Lindner D., Fitzek A., Brauninger H., Aleshcheva G., Edler C., Meissner K., Scherschel K., Kirchohof P., Escher F., Schultheiss H.P., et al. Association of cardiac infection with SARS-CoV-2 in confirmed COVID-19 autopsy cases. JAMA Cardiol. 2020;5:1281–1285. doi: 10.1001/jamacardio.2020.3551.
    1. Halushka M.K., Vander Heide R.S. Myocarditis is rare in COVID-19 autopsies: Cardiovascular findings across 277 postmortem examinations. Cardiovasc. Pathol. 2021;50:107300. doi: 10.1016/j.carpath.2020.107300.
    1. Kawakami R., Sakamoto A., Kawai K., Gianatti A., Pellegrini D., Nasr A., Kutys B., Guo L., Cornelissen A., Mori M., et al. Pathological evidence of SARS-CoV2 as a cause of myocarditis: JACC review topic of the week. J. Am. Coll. Cardiol. 2021;77:314–325. doi: 10.1016/j.jacc.2020.11.031.
    1. Bearse M., Hung Y.P., Krauson A.J., Bonanno L., Boyraz B., Harris C.K., Helland T.L., Hilburn C.F., Hutichison B., Jobbagy S., et al. Factors associated with myocardial SARS-CoV-2 infection, myocarditis, and cardiac inflammation in patients with COVID-19. Mod. Pathol. 2021;34:1345–1357. doi: 10.1038/s41379-021-00790-1.
    1. Li W., Moore M.J., Vasilieva N., Sui J., Wong S.K., Berne M.A., Somasundaran M., Sullivan J.L., Luzuriaga K., Grrenough T.C., et al. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature. 2003;426:450–454. doi: 10.1038/nature02145.
    1. Banu N., Panikar S.S., Leal L.R., Leal A.R. Protective role of ACE2 and its downregulation in SARS-CoV-2 infection leading to macrophage activation syndrome: Therapeutic implications. Life Sci. 2020;256:117905. doi: 10.1016/j.lfs.2020.117905.
    1. Das B.B., Tejtel S.K.S., Deshpande S., Shekerdemian L.S. A review of the cardiovascular effects of COVID-9 in adults and children. Tex. Heart Inst. J. 2021;48:e207395. doi: 10.14503/THIJ-20-7395.
    1. Incardi R.M., Lupi L., Zaccone G., Italia L., Raffo M., Tomasoni D., Cani D.S., Cerini M., Farina M., Gavazzi E., et al. Cardiac involvement in pa patient eith coronavirus disease 2019 (COVID-19) JAMA Cardiol. 2020;5:819–824. doi: 10.1001/jamacardio.2020.1096.
    1. Kelle S., Bucciarelli-Ducci C., Judd R.M., Kwong R.Y., Simonetti O., Plein S., Raimondi F., Weinsaft J.W., Wong T.C., Carr J. 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. doi: 10.1186/s12968-020-00656-6.
    1. Puntmann V.O., Carerj M.L., Wieters I., Fahim M., Arendt C., Hoffmann J., Shchendrygina A., Escher F., Vasa-Nicotera M., Zeiher A.M., et al. Outcomes of cardiovascular magnetic resonance imaging in patients recently recovered from coronavirus disease 2019 (COVID-19) JAMA Cardiol. 2020;5:1265–7365. doi: 10.1001/jamacardio.2020.3557.
    1. Gnecchi M., Moretti F., Bassi E.M., Leonardi S., Totaro R., Perotti L., Zuccaro V., Perilin S., Preda L., Baldanti F., et al. Myocarditis in a 16-year-old boy positive for SARS-CoV-2. Lancet. 2020;395:e116. doi: 10.1016/S0140-6736(20)31307-6.
    1. Das B.B. SARS-CoV-2 Myocarditis in a High School Athlete after COVID-19 and Its Implications for Clearance for Sports. Children. 2021;8:427. doi: 10.3390/children8060427.
    1. Rajpal S., Tong M.S., Borchers J. Cardiovascular magnetic resonance findings in competitive athletes recovering from COVID-19 infection. JAMA Cardiol. 2021;6:116–118. doi: 10.1001/jamacardio.2020.4916.
    1. Clark D.E., Parikh A., Dendy J.M. COVID-19 myocardial pathology evaluation in athletes with cardiac magnetic resonance (COMPETE CMR) Circulation. 2021;143:609–612. doi: 10.1161/CIRCULATIONAHA.120.052573.
    1. Starekova J., Bluemke D.A., Bradham W.S. Evaluation for myocarditis in competitive student-athletes recovering from coronavirus disease 2019 with cardiac magnetic resonance imaging. JAMA Cardiol. 2021;6:945–950. doi: 10.1001/jamacardio.2020.7444.
    1. Kim I.N.-C., Kim J.Y., Kim H.A., Han S. COVID-19-related myocarditis in a 21-year-old female patient. Eur. Heart J. 2020;41:1859. doi: 10.1093/eurheartj/ehaa288.
    1. Luetkens J.A., Isaak A., Öztürk C., Mesropyan N., Monin M., Schlabe S., Reinert M., Faron A., Heine A., Velten M., et al. Cardiac MRI in Suspected Acute COVID-19 Myocarditis. Radiol. Cardiothorac. Imaging. 2021;3:e200628. doi: 10.1148/ryct.2021200628.
    1. Maurus S., Weckbach L.T., Marschner C., Kunz W.G., Ricke J., Kazmierczak P.M., Bieber S., Brado J., Kraechan A., Hellmuth J.C., et al. Differences in cardiac magnetic resonance imaging markers between patients with COVID-19 associated myocardial injury and patients with clinically suspected myocarditis. J. Thorac. Imaging. 2021;36:279–285. doi: 10.1097/RTI.0000000000000599.
    1. Theocharis P., Wong J., Pushparajah K., Mathur S.K., Simpson J.M., Pascall E., Cleary A., Stewart K., Adhvaryu K., Savis A., et al. Multimodality cardiac evaluation in children and young adults with multisystem inflammation associated with COVID-19. Eur. Heart J. Cardiovasc. Imaging. 2021;22:896–903. doi: 10.1093/ehjci/jeaa212.
    1. Libby P., Lüscher T. COVID-19 is, in the end, an endothelial disease. Eur. Heart J. 2020;41:3038–3044. doi: 10.1093/eurheartj/ehaa623.
    1. Bartoszek M., Małek Ł., Barczuk-Falęcka M., Brzewski M. Cardiac magnetic resonance follow-up of children after pediatric inflammatory multisystem syndrome temporally associated with SARS-CoV-2 with initial cardiac involvement. J. Magn. Reson. Imaging. 2021;55:27870. doi: 10.1002/jmri.27870.
    1. Webster G., Patel A.B., Carr M.R., Rigsby C.K., Rychlik K., Rowley A.H., Robinson J.D. Cardiovascular magnetic resonance imaging in children after recovery from symptomatic COVID-19 or MIS-C: A prospective study. J. Cardiovasc. Magn. Reson. 2021;23:86. doi: 10.1186/s12968-021-00786-5.
    1. Aeschliman F.A., Misra N., Hussein T., Panaioli E., Soslow J.H., Crum K., Steele J.M., Huber S., Marcora S., Brambilla P., et al. Myocardial involvement in children with post-COVID multisystem inflammatory syndrome: A cardiovascular magnetic resonance-based multicenter international study—The CARDOVID registry. J. Cardiovasc. Magn. Reson. 2021;23:140. doi: 10.1186/s12968-021-00841-1.
    1. Blondiaux E., Parisot P., Redheuil A., Tzaroukian L., Levy Y., Sileo C., Schnuriger A., Lorrot M., Guedj R., le Pointe H.D. Cardiac MRI in Children with multisystem inflammatory syndrome associated with COVID-19. Radiology. 2020;297:E283–E288. doi: 10.1148/radiol.2020202288.
    1. Chakraborty A., Philip R., Santoso M., Naik R., Merlocco A., Johnson J.N. Cardiovascular magnetic resonance imaging in children with multisystem inflammatory syndrome in children (MIS-C) associated with COVID-19: Institutional protocol-based medium-term follow-up study. Pediatric Cardiol. 2022 doi: 10.1007/s00246-022-02927-8.
    1. Matsubara D., Chang J., Kauffman H.L., Wang Y., Nadaraj S., Patel C., Paridon S.M., Fogel M.A., Quartemain M.D., Banerjee A. Longitudinal Assessment of Cardiac Outcomes of Multisystem Inflammatory Syndrome in Children Associated With COVID-19 Infections. JAHA. 2022;11:e023251. doi: 10.1161/JAHA.121.023251.
    1. Jain S.S., Steele J.M., Fonseca B., Huang S., Shah S., Maskatia S.A., Buddhe S., Misra N., Ramachandran P., Gaur L., et al. COVID-19 vaccination-associated myocarditis in adolescents. Pediatrics. 2021;148:e2021053427. doi: 10.1542/peds.2021-053427.
    1. Das B.B., Kohli U., Ramachandran P., Nguyen H.H., Greil G., Hussain T., Tandon A., Kane C., Avula S., Duru C., et al. Myopericarditis after mRNA COVID-19 vaccination in adolescents 12 to 18 years of age. J. Pediatrics. 2021;30:26–32.e1. doi: 10.1016/j.jpeds.2021.07.044.
    1. Marshall M., Ferguson I.D., Lewis P., Jaggi P., Gagliardo C., Collins J.S., Shaughnessy R., Caron R., Fuss C., Corbin K.J.E., et al. Symptomatic acute myocarditis in seven adolescents following Pfizer-BioNTech COVID-19 vaccination. Pediatrics. 2021;148:e2021052478. doi: 10.1542/peds.2021-052478.
    1. Snapiri O., Rosenberg Danziger C., Shirman N., Weissbach A., Lowenthal A., Ayalon I., Adam D., Yarden-Bilavsky H., Bilavsky E. Transient cardiac injury in adolescents receiving the BNT162b2 mRNA COVID-19 vaccine. Pediatric Infect. Dis. J. 2021;40:e360. doi: 10.1097/INF.0000000000003235.
    1. Tano E., San Martin S., Girgis S., Martinez-Fernandez Y., Sanchez Vegas C. Perimyocarditis in adolescents after Pfizer-BioNTech COVID-19 vaccine. J. Pediatric Infect. Dis. Soc. 2021;10:962–966. doi: 10.1093/jpids/piab060.
    1. Bozkurt B., Kamat I., Hotez P.J. Myocarditis with COVID-19 mRNA vaccines. Circulation. 2021;144:471–484. doi: 10.1161/CIRCULATIONAHA.121.056135.
    1. Shay D.K., Shimabukuro T.T., DeStefano F. Myocarditis occurring after immunization with mRNA-based COVID-19 vaccines. JAMA Cardiol. 2021;6:1196–1201. doi: 10.1001/jamacardio.2021.2821.
    1. Dionne A., Sperotto F., Chamberlain S., Baker A.L., Powell A.J., Prakash A., Castellanos D.A., Saleeb S.F., de Ferranti S.D., Newburger J.W., et al. Association of Myocarditis With BNT162b2 Messenger RNA COVID-19 Vaccine in a Case Series of Children. JAMA Cardiol. 2021;6:1446–1450. doi: 10.1001/jamacardio.2021.3471.
    1. Muthukumar A., Narasimhan M., Li Q.Z., Mahimainathan L., Hitto I., Fuda F., Batra K., Jiang X., Zhu C., Schoggins J., et al. In-Depth evaluation of a case of presumed myocarditis after the second dose of COVID-19 mRNA vaccine. Circulation. 2021;144:487–498. doi: 10.1161/CIRCULATIONAHA.121.056038.
    1. Vojdani A., Kharrazian D. Potential antigenic cross-reactivity between SARS-CoV-2 and human tissue with a possible link to an increase in autoimmune diseases. Clin. Immunol. 2020;217:108480. doi: 10.1016/j.clim.2020.108480.
    1. Tsilingiris D., Vallianou N.G., Karampela I., Liu J., Dalamaga M. Potential implications of lipid nanoparticles in the pathogenesis of myocarditis associated with the use of mRNA vaccines against SARS-CoV-2. Metabol Open. 2022;13:100159. doi: 10.1016/j.metop.2021.100159.
    1. Aljohani O.A., Mackie D., Bratincsak A., Bradley J.S., Perry J.C. Spectrum of Viral Pathogens Identified in Children with Clinical479Myocarditis (Pre-Coronavirus Disease-2019, 2000-2018): Etiologic Agent Versus Innocent Bystander. J. Pediatrics. 2022;242:18–24. doi: 10.1016/j.jpeds.2021.11.011.

Source: PubMed

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