Cardiac MRI in Suspected Acute COVID-19 Myocarditis
2021; Radiological Society of North America; Volume: 3; Issue: 2 Linguagem: Inglês
10.1148/ryct.2021200628
ISSN2638-6135
AutoresJulian A. Luetkens, Alexander Isaak, Can Öztürk, Narine Mesropyan, Malte B. Monin, Sefan Schlabe, Matthäus Reinert, Anton Faron, Annkristin Heine, Markus Velten, Darius Dabir, Christoph Boesecke, Christian P. Strassburg, Ulrike Attenberger, Sebastian Zimmer, Georg Daniel Duerr, Jacob Nattermann,
Tópico(s)Pericarditis and Cardiac Tamponade
ResumoHomeRadiology: Cardiothoracic ImagingVol. 3, No. 2 PreviousNext Research LetterFree AccessPulmonary Imaging/Cardiac MRICardiac MRI in Suspected Acute COVID-19 MyocarditisJulian A. Luetkens* , Alexander Isaak*, Can Öztürk, Narine Mesropyan, Malte Monin, Stefan Schlabe, Matthäus Reinert, Anton Faron, Annkristin Heine, Markus Velten, Darius Dabir, Christoph Boesecke, Christian P. Strassburg, Ulrike Attenberger, Sebastian Zimmer, Georg D. Duerr, Jacob NattermannJulian A. Luetkens* , Alexander Isaak*, Can Öztürk, Narine Mesropyan, Malte Monin, Stefan Schlabe, Matthäus Reinert, Anton Faron, Annkristin Heine, Markus Velten, Darius Dabir, Christoph Boesecke, Christian P. Strassburg, Ulrike Attenberger, Sebastian Zimmer, Georg D. Duerr, Jacob NattermannAuthor AffiliationsFrom the Department of Diagnostic and Interventional Radiology (J.A.L., A.I., N.M., M.R., A.F., D.D., U.A.), Department of Internal Medicine II-Cardiology (C.Ö., S.Z.), Department of Internal Medicine I (M.M., S.S., C.B., C.P.S., J.N.), Department of Internal Medicine III-Oncology (A.H.), Department of Anesthesiology (M.V.), and Department of Cardiac Surgery (G.D.D.), University Hospital Bonn, Venusberg-Campus 1, 53127 Bonn, Germany; and Quantitative Imaging Laboratory Bonn (QILaB), Bonn, Germany (J.A.L., A.I., N.M., M.R., A.F., D.D.).Address correspondence to J.A.L. (e-mail: [email protected]).Julian A. Luetkens* Alexander Isaak*Can ÖztürkNarine MesropyanMalte MoninStefan SchlabeMatthäus ReinertAnton FaronAnnkristin HeineMarkus VeltenDarius DabirChristoph BoeseckeChristian P. StrassburgUlrike AttenbergerSebastian ZimmerGeorg D. DuerrJacob NattermannPublished Online:Mar 4 2021https://doi.org/10.1148/ryct.2021200628MoreSectionsPDF ToolsAdd to favoritesCiteTrack Citations ShareShare onFacebookXLinked In * J.A.L. and A.I. contributed equally to this work.AbstractKeywords: COVID-19; coronavirus; myocarditis; cardiac MRI; T1 mapping; T2 mappingDownload as PowerPointSummaryParticipants with active and symptomatic COVID-19 infection and suspected acute myocarditis had distinct pathologic findings at cardiac MRI with diffuse myocardial edema, which could be best depicted using myocardial mapping techniques.IntroductionSARS-CoV-2 infection, and the resulting COVID-19, has become a worldwide pandemic. Although primarily affecting the respiratory system, COVID-19–associated myocardial injury is common and can occur directly due to myocardial viral infection or indirectly due to systemic inflammation, endothelial activation, and/or microvascular thrombosis (1,2). Besides myocardial infarction, myocardial injury can also be a result of myocardial inflammation (2). However, current information about associated myocardial inflammation is mainly limited to case reports or series (3). As cardiac MRI is important for the diagnostic workup of patients with myocarditis, more data about MRI characteristics of COVID-19–associated acute inflammatory injury are needed. The aim of this study was to describe cardiac MRI findings in participants with active COVID-19 infection and suspected acute myocarditis.Materials and MethodsThe institutional ethics commission approved this prospective study. All participants gave written informed consent. Participants with COVID-19 without structural heart disease and mechanical ventilatory support were included consecutively during the recruitment period from April 2020 to December 2020. Participants had a clinical suspicion for COVID-19–associated myocarditis with signs of acute myocardial injury (elevated troponin levels with or without electrocardiographic changes). Acute coronary syndromes were excluded with cardiac catheterization. The control groups consisted of healthy volunteers and participants with suspected acute non–COVID-19 myocarditis (4).Cardiac MRI was performed at 1.5 T in all participants using previously described acquisition parameters (4). Left ventricular function, average systolic longitudinal strain, T2 signal intensity ratio, T1 relaxation times, T2 relaxation times, extracellular volume, and quantitative late gadolinium enhancement (LGE) were determined. Focal myocardial edema and LGE were visually assessed. Measurements of the blinded readers (J.A.L. and A.I., with 8 and 4 years of experience, respectively, in cardiac MRI) were conducted as described previously (5).Continuous variables between two groups were compared with the Student t test. A χ2 test was used to compare dichotomous variables. One-way analysis of variance followed by Tukey multiple comparison tests was performed to compare variables in the three participant groups. Statistical significance level was set to P < .05.ResultsParticipants with COVID-19 had dyspnea, fever, and positive pneumonic infiltrates on chest CT scans or radiographs. Cardiac MRI was performed 7.6 days ± 4.6 (standard deviation) after positive reverse-transcription polymerase chain reaction test result. C-reactive protein (44.6 mg/L ± 37.1) and troponin T (114 ng/mL ± 249) levels were elevated in participants with COVID-19. Participants with COVID-19 had diffuse global higher T1 and T2 relaxation times compared with healthy participants (T1, 1046 msec ± 45 vs 953 msec ± 32 [P < .001]; T2, 61.7 msec ± 6.6 vs 52.9 msec ± 3.0 [P < .001]). Myocardial T1 and T2 were also prolonged in non–COVID-19 myocarditis, but these participants had a more focal disease with more visible myocardial edema (88% [seven of eight] vs 13% [one of eight]; P = .003) and LGE lesions (88% [seven of eight] vs 38% [three of eight]; P = .04). The T2 ratio was not significantly elevated in participants with COVID-19 myocarditis; however, this was likely secondary to skeletal muscle edema as skeletal muscle T1 was also elevated in participants with COVID myocarditis (Table). A total of 38% (three of eight) of participants with COVID-19 had severe wall-motion abnormalities consistent with patterns of stress-induced cardiomyopathy (Figure). Additionally, 38% (three of eight) of participants with COVID-19 had small pericardial effusions and/or pericardial enhancement.Clinical and Cardiac MRI Characteristics of Healthy Controls, Participants with Suspected Non–COVID-19 Myocarditis, and Participants with Suspected COVID-19 MyocarditisSummary of study results. A, Composition of imaging findings found in our study cohort. Besides signs of active pulmonary COVID-19 infection with pneumonic infiltrates and pleural effusions, participants with suspected acute COVID-19–associated myocarditis had an impaired left ventricular function, also with patterns of stress-induced cardiomyopathy in single cases (a midventricular type of stress-induced cardiomyopathy with corresponding diastolic and systolic images is shown). As a key finding, a distinct diffuse myocardial edema (detected with myocardial T1 and T2 mapping) was present in most participants. Late gadolinium enhanced lesions (white arrows) were less pronounced, especially when compared with participants with non–COVID-19 myocarditis. Late gadolinium enhancement lesions were present in the subepicardium of the lateral wall or in the basal septal midmyocardium. Some participants displayed pericardial enhancement or small pericardial effusions (see white arrows on corresponding images). All image examples are from the described study cohort of participants. B, Column graphs with individual plotted values show distribution of quantitative myocardial MRI parameters in healthy participants and in participants with suspected acute non–COVID-19 and COVID-19 myocarditis. Distributions are given for native myocardial T1 relaxation time, myocardial T2 relaxation time, and extracellular volume fraction. Data are presented as mean with standard deviation error bars. * indicates significant pairwise comparison (P < .05). ANOVA = analysis of variance, ECV = extracellular volume fraction, LVEF = left ventricular ejection fraction. The figure contains a free medical image from Servier Medical Art, licensed under a Creative Commons Attribution 3.0 Unported license (CC BY 3.0) (https://smart.servier.com/).Download as PowerPointDiscussionWe found a pattern of diffuse myocardial edema in participants with symptomatic COVID-19 infection and suspected myocarditis. Myocardial edema affects myocardial function and might be an expression of diffuse inflammation due to a systemic immune response, direct myocardial damage of SARS-CoV-2, or a vascular leakage due to endothelial damage (6). Interestingly, the amount of LGE lesions, as a sign of myocyte necrosis, was lower in participants with COVID-19 myocarditis when compared with participants with acute non–COVID-19 myocarditis, which is primarily induced by cardiotropic viruses (4). This result indicates that the pathomechanism of myocardial inflammation injury might be different in SARS-CoV-2 and is possibly based on an interplay of different broad affections of the cardiovascular system (2). Also, we observed patterns of stress-induced cardiomyopathy as another potential mechanism of myocardial injury in participants with COVID-19. As the occurrence of myocardial injury and features of stress-induced cardiomyopathy are associated with fatal outcome of COVID-19 infection (2), the observed pronounced diffuse cardiac alterations are of particular interest.Disclosures of Conflicts of Interest: J.A.L. Activities related to the present article: disclosed no relevant relationships. Activities not related to the present article: author received payment for lectures from Philips Healthcare. Other relationships: disclosed no relevant relationships. A.I. disclosed no relevant relationships. C.O. disclosed no relevant relationships. N.M. disclosed no relevant relationships. M.M. disclosed no relevant relationships. S.S. Activities related to the present article: disclosed no relevant relationships. Activities not related to the present article: author received travel and meeting expenses covered by Abbvie and ViiV. Other relationships: disclosed no relevant relationships. M.R. disclosed no relevant relationships. A.F. disclosed no relevant relationships. A.H. disclosed no relevant relationships. M.V. disclosed no relevant relationships. D.D. disclosed no relevant relationships. C.B. Activities related to the present article: disclosed no relevant relationships. Activities not related to the present article: author was paid as a consultant by Gilead, Janssen, MSD, and ViiV; institution has grants from DZIF, NEAT ID, and Hector Foundation. Other relationships: disclosed no relevant relationships. C.P.S. disclosed no relevant relationships. U.A. Activities related to the present article: disclosed no relevant relationships. Activities not related to the present article: author received payment for lectures from Siemens Healthineers. Other relationships: disclosed no relevant relationships. S.Z. disclosed no relevant relationships. G.D.D. disclosed no relevant relationships. J.N. disclosed no relevant relationships.Author ContributionsAuthor contributions: Guarantors of integrity of entire study, J.A.L., M.M.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; agrees to ensure any questions related to the work are appropriately resolved, all authors; literature research, J.A.L., A.I., C.Ö., N.M., M.M., M.R., A.F., A.H., M.V., C.P.S., U.A., G.D.D.; clinical studies, J.A.L., A.I., C.Ö., N.M., M.M., S.S., A.F., A.H., M.V., D.D., C.B., S.Z., G.D.D., J.N.; experimental studies, C.Ö., N.M., M.M., A.F., G.D.D.; statistical analysis, J.A.L., C.Ö., N.M., M.M., C.P.S., S.Z., G.D.D.; and manuscript editing, J.A.L., A.I., C.Ö., N.M., M.M., S.S., M.R., A.F., M.V., C.B., C.P.S., U.A., S.Z., G.D.D., J.N.* J.A.L. and A.I. contributed equally to this work.Supported by the German Heart Foundation/German Foundation of Heart Research (F/28/20)References1. Shi S, Qin M, Shen B, et al. Association of Cardiac Injury with Mortality in Hospitalized Patients With COVID-19 in Wuhan, China. JAMA Cardiol 2020;5(7):802–810. MedlineGoogle Scholar2. Giustino G, Pinney SP, Lala A, et al. Coronavirus and Cardiovascular Disease, Myocardial Injury, and Arrhythmia:. JACC Focus Seminar. J Am Coll Cardiol 2020;76(17):2011–2023. MedlineGoogle Scholar3. Esposito A, Palmisano A, Natale L, et al. Cardiac Magnetic Resonance Characterization of Myocarditis-Like Acute Cardiac Syndrome in COVID-19. JACC Cardiovasc Imaging 2020;13(11):2462–2465. MedlineGoogle Scholar4. Luetkens JA, Faron A, Isaak A, et al. Comparison of Original and 2018 Lake Louise Criteria for Diagnosis of Acute Myocarditis: Results of a Validation Cohort. Radiol Cardiothorac Imaging 2019;1(3):e190010. Google Scholar5. Isaak A, Praktiknjo M, Jansen C, et al. Myocardial Fibrosis and Inflammation in Liver Cirrhosis: MRI Study of the Liver-Heart Axis. Radiology 2020;297(1):51–61. Google Scholar6. Rafiee MJ, Babaki Fard F, Friedrich MG. COVID-19, myocardial edema and dexamethasone. Med Hypotheses 2020;145110307. MedlineGoogle ScholarArticle HistoryReceived: Dec 30 2020Revision requested: Jan 25 2021Revision received: Feb 19 2021Accepted: Feb 25 2021Published online: Mar 04 2021 FiguresReferencesRelatedDetailsCited ByImaging Acute and Chronic Cardiac Complications of COVID-19 and after COVID-19 VaccinationFelipe Sánchez Tijmes, Constantin A. Marschner, Joao Francisco Ribeiro Gavina de Matos, Camila M. Urzua Fresno, Jose Miguel Gutiérrez Chacoff, Paaladinesh Thavendiranathan, Cristina Fuss, Kate Hanneman, 24 August 2023 | RadioGraphics, Vol. 43, No. 9The Many Faces of Myocarditis: Role of Cardiac MRIAlbert de Roos, 12 October 2021 | Radiology, Vol. 302, No. 1Cardiac MRI in Patients with Prolonged Cardiorespiratory Symptoms after Mild to Moderate COVID-19Dmitrij Kravchenko, Alexander Isaak, Sebastian Zimmer, Narine Mesropyan, Matthäus Reinert, Anton Faron, Claus C. 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