Outcome and Morphofunctional Changes on Cardiac Magnetic Resonance in Patients With Acute Myocarditis Following mRNA COVID-19 Vaccination
2023; Lippincott Williams & Wilkins; Volume: 16; Issue: 6 Linguagem: Inglês
10.1161/circheartfailure.122.010315
ISSN1941-3297
AutoresEnrico Ammirati, L Lupi, Matteo Palazzini, Michele Ciabatti, Valentina A. Rossi, Piero Gentile, Aitor Uribarri, Chiara Vecchio, Daniele Nassiacos, Alberto Cereda, Cristina Conca, Gabriele Tumminello, Nicolas Piriou, Coline Lelarge, Patrizia Pedrotti, Miriam Stucchi, Giovanni Peretto, Michele Galasso, Florent Huang, Umberto Ianni, Antonio Procopio, Gianluigi Saponara, Paolo Cimaglia, Daniela Tomasoni, Francesco Moroni, Annalisa Turco, Simone Sala, Giuseppe Di Tano, Entela Bollano, Claudio Moro, Antonio Abbate, Roberta Della Bona, Italo Porto, Stefano Carugo, Jeness Campodonico, Gianluca Pontone, Aurelia Grosu, Leonardo Bolognese, Jorge Salamanca, Pablo Díez‐Villanueva, Krzysztof Ozierański, Agata Tymińska, Loren Sardo Infirri, Daniel I. Bromage, Antonio Cannatà, Kimberly N. Hong, Marianna Adamo, G Quattrocchi, Alberto Foà, Luciano Potena, Andrea Garascia, Cristina Giannattasio, Eric Adler, Gianfranco Sinagra, Frank Ruschitzka, Paolo G. Camici, Marco Metra, Maurizio Pieroni,
Tópico(s)Viral gastroenteritis research and epidemiology
ResumoHomeCirculation: Heart FailureVol. 16, No. 6Outcome and Morphofunctional Changes on Cardiac Magnetic Resonance in Patients With Acute Myocarditis Following mRNA COVID-19 Vaccination Free AccessLetterPDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissions ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toFree AccessLetterPDF/EPUBOutcome and Morphofunctional Changes on Cardiac Magnetic Resonance in Patients With Acute Myocarditis Following mRNA COVID-19 Vaccination Enrico Ammirati, Laura Lupi, Matteo Palazzini, Michele Ciabatti, Valentina A. Rossi, Piero Gentile, Aitor Uribarri, Chiara R. Vecchio, Daniele Nassiacos, Alberto Cereda, Cristina Conca, Gabriele Tumminello, Nicolas Piriou, Coline Lelarge, Patrizia Pedrotti, Miriam Stucchi, Giovanni Peretto, Michele Galasso, Florent Huang, Umberto Ianni, Antonio Procopio, Gianluigi Saponara, Paolo Cimaglia, Daniela Tomasoni, Francesco Moroni, Annalisa Turco, Simone Sala, Giuseppe Di Tano, Entela Bollano, Claudio Moro, Antonio Abbate, Roberta Della Bona, Italo Porto, Stefano Carugo, Jeness Campodonico, Gianluca Pontone, Aurelia Grosu, Leonardo Bolognese, Jorge Salamanca, Pablo Diez-Villanueva, Krzysztof Ozieranski, Agata Tyminska, Loren Sardo Infirri, Daniel Bromage, Antonio Cannatà, Kimberly N. Hong, Marianna Adamo, Giuseppina Quattrocchi, Alberto Foà, Luciano Potena, Andrea Garascia, Cristina Giannattasio, Eric D. Adler, Gianfranco Sinagra, Frank Ruschitzka, Paolo G. Camici, Marco Metra and Maurizio Pieroni Enrico AmmiratiEnrico Ammirati Correspondence to: Enrico Ammirati, MD, PhD, Niguarda Hospital, Piazza Ospedale Maggiore 3, 20162 Milano, Italy, Email E-mail Address: [email protected] https://orcid.org/0000-0002-1676-5257 Department of De Gasperis Cardio Center, Niguarda Hospital, Milano, Italy (E.A., M. Palazzini, P.G., P.P., G.Q., A. Garascia, C.G.). Search for more papers by this author , Laura LupiLaura Lupi Laura Lupi, MD, Institute of Cardiology, Azienda Socio-Sanitaria Territoriale Spedali Civili di Brescia and Department of Medical and Surgical Specialties, Radiological Sciences, and Public Health, University of Brescia, Piazzale Spedali Civili 1, 25123, Brescia, Italy, Email E-mail Address: [email protected] https://orcid.org/0000-0003-2633-1695 Institute of Cardiology, Azienda Socio-Sanitaria Territoriale Spedali Civili di Brescia and Department of Medical and Surgical Specialties, Radiological Sciences, and Public Health, University of Brescia, Italy (L.L., D.T., M.A., M.M.). Search for more papers by this author , Matteo PalazziniMatteo Palazzini https://orcid.org/0000-0003-1700-7340 Department of De Gasperis Cardio Center, Niguarda Hospital, Milano, Italy (E.A., M. Palazzini, P.G., P.P., G.Q., A. Garascia, C.G.). Department of Medicine and Surgery, Bicocca University, Milano, Italy (M. Palazzini, M.G., C.G.). Search for more papers by this author , Michele CiabattiMichele Ciabatti https://orcid.org/0000-0003-4303-4537 Cardiovascular Department, San Donato Hospital, Arezzo, Italy (M.C., L.B., M. Pieroni). Search for more papers by this author , Valentina A. RossiValentina A. Rossi https://orcid.org/0000-0001-9235-6597 Department of Cardiology, University Heart Center, University Hospital Zurich and University of Zurich, Switzerland (V.A.R., F.R.). Search for more papers by this author , Piero GentilePiero Gentile Department of De Gasperis Cardio Center, Niguarda Hospital, Milano, Italy (E.A., M. Palazzini, P.G., P.P., G.Q., A. Garascia, C.G.). Search for more papers by this author , Aitor UribarriAitor Uribarri https://orcid.org/0000-0002-6911-7480 Cardiology Department, Hospital Universitari Vall d’Hebron, Barcelona, Spain (A.U.). Vall d’Hebron Institute de Recerca, Barcelona, Spain (A.U.). Centro de Investigación Biomédica en Red de Enfermedades Cardiovasculares, Instituto de Salud Carlos III, Madrid, Spain (A.U.). Search for more papers by this author , Chiara R. VecchioChiara R. Vecchio Department of Cardiology, Presidio Ospedaliero di Saronno, Azienda Socio-Sanitaria Territoriale Valle Olona, Saronno, Varese, Italy (C.R.V., D.N.). Search for more papers by this author , Daniele NassiacosDaniele Nassiacos https://orcid.org/0000-0001-5348-7084 Department of Cardiology, Presidio Ospedaliero di Saronno, Azienda Socio-Sanitaria Territoriale Valle Olona, Saronno, Varese, Italy (C.R.V., D.N.). Search for more papers by this author , Alberto CeredaAlberto Cereda Cardiovascular Department, Association Socio Sanitary Territorial Santi Paolo e Carlo, Milano, Italy (A. Cereda, C.C.). Search for more papers by this author , Cristina ConcaCristina Conca Cardiovascular Department, Association Socio Sanitary Territorial Santi Paolo e Carlo, Milano, Italy (A. Cereda, C.C.). Search for more papers by this author , Gabriele TumminelloGabriele Tumminello https://orcid.org/0000-0003-3121-8400 Division of Cardiology, Foundation Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Cà Granda Ospedale Maggiore Policlinico, University of Milan, Italy (G.T., S.C.). Search for more papers by this author , Nicolas PiriouNicolas Piriou https://orcid.org/0000-0002-6677-6552 Nantes Université, CHU Nantes, Centre National de la Recherche Scientifique, Institut National de la Santé et de la Recherche Médicale, l’Institut du Thorax, France (N.P., C.L.). Search for more papers by this author , Coline LelargeColine Lelarge Nantes Université, CHU Nantes, Centre National de la Recherche Scientifique, Institut National de la Santé et de la Recherche Médicale, l’Institut du Thorax, France (N.P., C.L.). Search for more papers by this author , Patrizia PedrottiPatrizia Pedrotti https://orcid.org/0000-0001-8920-1156 Department of De Gasperis Cardio Center, Niguarda Hospital, Milano, Italy (E.A., M. Palazzini, P.G., P.P., G.Q., A. Garascia, C.G.). Search for more papers by this author , Miriam StucchiMiriam Stucchi Cardiology Unit, Azienda Socio-Sanitaria Territoriale della Brianza (MB), Vimercate Hospital, Italy (M.S.). Search for more papers by this author , Giovanni PerettoGiovanni Peretto https://orcid.org/0000-0003-1815-4000 San Raffaele Hospital and Vita Salute University, Milano, Italy (G. Peretto, S.S., P.G.C.). Search for more papers by this author , Michele GalassoMichele Galasso Department of Medicine and Surgery, Bicocca University, Milano, Italy (M. Palazzini, M.G., C.G.). Search for more papers by this author , Florent HuangFlorent Huang https://orcid.org/0000-0002-3063-1546 Service de Cardiologie, Hôpital Foch, Suresnes, France (F.H.). Search for more papers by this author , Umberto IanniUmberto Ianni https://orcid.org/0000-0003-1129-4203 Cardiology Unit, Madonna del Soccorso Hospital, Azienda Sanitaria Unica Regionale Marche 5, San Benedetto del Tronto, Italy (U.I.). Search for more papers by this author , Antonio ProcopioAntonio Procopio https://orcid.org/0000-0002-0422-7769 Intensive Cardiac Care Unit, “F. Renzetti” Hospital, Lanciano, Chieti, Italy (A.P.). Search for more papers by this author , Gianluigi SaponaraGianluigi Saponara Department of Cardiovascular and Thoracic Sciences, Fondazione Policlinico Universitario A. Gemelli IRCCS, Roma, Italy (G.S.). Search for more papers by this author , Paolo CimagliaPaolo Cimaglia https://orcid.org/0000-0002-3326-7663 Maria Cecilia Hospital, GVM Care and Research, Cotignola, Ravenna, Italy (P.C). Search for more papers by this author , Daniela TomasoniDaniela Tomasoni Institute of Cardiology, Azienda Socio-Sanitaria Territoriale Spedali Civili di Brescia and Department of Medical and Surgical Specialties, Radiological Sciences, and Public Health, University of Brescia, Italy (L.L., D.T., M.A., M.M.). Search for more papers by this author , Francesco MoroniFrancesco Moroni https://orcid.org/0000-0002-6101-1403 Pauley Heart Center, Virginia Commonwealth University, Richmond (F.M., A.A.). Search for more papers by this author , Annalisa TurcoAnnalisa Turco Cardiologia, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy (A. Turco). Search for more papers by this author , Simone SalaSimone Sala https://orcid.org/0000-0003-3303-8892 San Raffaele Hospital and Vita Salute University, Milano, Italy (G. Peretto, S.S., P.G.C.). Search for more papers by this author , Giuseppe Di TanoGiuseppe Di Tano Unità Operativa Cardiologia, Azienda Socio-Sanitaria Territoriale di Cremona, Ospedale OglioPo, Casalmaggiore, Cremona, Italy (G.D.T.). Search for more papers by this author , Entela BollanoEntela Bollano https://orcid.org/0000-0003-3341-2434 Department of Cardiology, Sahlgrenska University Hospital, Gothenburg, Sweden (E.B.). Search for more papers by this author , Claudio MoroClaudio Moro Department of Cardiology, Azienda Socio-Sanitaria Territoriale Monza, Desio, Italy (C.M.). Search for more papers by this author , Antonio AbbateAntonio Abbate https://orcid.org/0000-0002-1930-785X Pauley Heart Center, Virginia Commonwealth University, Richmond (F.M., A.A.). Search for more papers by this author , Roberta Della BonaRoberta Della Bona Cardiology Unit, Cardiothoracic and Vascular Department, IRCCS San Martino Hospital, Genoa, Italy (R.D.B., I.P.). Search for more papers by this author , Italo PortoItalo Porto https://orcid.org/0000-0002-9854-5046 Cardiology Unit, Cardiothoracic and Vascular Department, IRCCS San Martino Hospital, Genoa, Italy (R.D.B., I.P.). Department of Internal Medicine and Medical Specialties, University of Genoa, Italy (I.P.). Search for more papers by this author , Stefano CarugoStefano Carugo https://orcid.org/0000-0002-5166-0899 Division of Cardiology, Foundation Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Cà Granda Ospedale Maggiore Policlinico, University of Milan, Italy (G.T., S.C.). Department of Clinical Sciences and Community Health, Università Degli Studi di Milano, Italy (S.C., J.C.). Search for more papers by this author , Jeness CampodonicoJeness Campodonico Department of Clinical Sciences and Community Health, Università Degli Studi di Milano, Italy (S.C., J.C.). Centro Cardiologico Monzino IRCCS, University of Milan, Italy (J.C., G. Pontone). Search for more papers by this author , Gianluca PontoneGianluca Pontone https://orcid.org/0000-0002-1339-6679 Centro Cardiologico Monzino IRCCS, University of Milan, Italy (J.C., G. Pontone). Search for more papers by this author , Aurelia GrosuAurelia Grosu Cardiovascular Department, Azienda Socio-Sanitaria Territoriale Papa Giovanni XXIII, Bergamo, Italy (A. Grosu). Search for more papers by this author , Leonardo BologneseLeonardo Bolognese https://orcid.org/0000-0002-5199-7870 Cardiovascular Department, San Donato Hospital, Arezzo, Italy (M.C., L.B., M. Pieroni). Search for more papers by this author , Jorge SalamancaJorge Salamanca https://orcid.org/0000-0002-5067-5052 Cardiology Department, Hospital Universitario De La Princesa, Madrid, Spain (J.S., P.D.-V.). Search for more papers by this author , Pablo Diez-VillanuevaPablo Diez-Villanueva Cardiology Department, Hospital Universitario De La Princesa, Madrid, Spain (J.S., P.D.-V.). Search for more papers by this author , Krzysztof OzieranskiKrzysztof Ozieranski https://orcid.org/0000-0002-3848-0922 First Department of Cardiology, Medical University of Warsaw, Poland (K.O., A. Tyminska). Search for more papers by this author , Agata TyminskaAgata Tyminska First Department of Cardiology, Medical University of Warsaw, Poland (K.O., A. Tyminska). Search for more papers by this author , Loren Sardo InfirriLoren Sardo Infirri Ospedale di Circolo e fondazione Macchi, Azienda Socio-Sanitaria Territoriale Sette Laghi, Varese, Italy (L.S.I.). Search for more papers by this author , Daniel BromageDaniel Bromage https://orcid.org/0000-0002-4243-5964 School of Cardiovascular Medicine and Metabolic Medicine and Sciences, King’s College London British Heart Foundation Centre of Excellence, King’s College London, United Kingdom (D.B., A. Cannatà). Department of Cardiology, King’s College Hospital London, United Kingdom (D.B., A. Cannatà). Search for more papers by this author , Antonio CannatàAntonio Cannatà https://orcid.org/0000-0001-7609-6297 School of Cardiovascular Medicine and Metabolic Medicine and Sciences, King’s College London British Heart Foundation Centre of Excellence, King’s College London, United Kingdom (D.B., A. Cannatà). Department of Cardiology, King’s College Hospital London, United Kingdom (D.B., A. Cannatà). Search for more papers by this author , Kimberly N. HongKimberly N. Hong Division of Cardiology, Department of Medicine, University of California San Diego (K.N.H., E.D.A.). Search for more papers by this author , Marianna AdamoMarianna Adamo https://orcid.org/0000-0002-3855-1815 Institute of Cardiology, Azienda Socio-Sanitaria Territoriale Spedali Civili di Brescia and Department of Medical and Surgical Specialties, Radiological Sciences, and Public Health, University of Brescia, Italy (L.L., D.T., M.A., M.M.). Search for more papers by this author , Giuseppina QuattrocchiGiuseppina Quattrocchi Department of De Gasperis Cardio Center, Niguarda Hospital, Milano, Italy (E.A., M. Palazzini, P.G., P.P., G.Q., A. Garascia, C.G.). Search for more papers by this author , Alberto FoàAlberto Foà Academic Hospital S. Orsola-Malpighi, Bologna, Italy (A.F., L.P.). Search for more papers by this author , Luciano PotenaLuciano Potena https://orcid.org/0000-0001-7388-5012 Academic Hospital S. Orsola-Malpighi, Bologna, Italy (A.F., L.P.). Search for more papers by this author , Andrea GarasciaAndrea Garascia Department of De Gasperis Cardio Center, Niguarda Hospital, Milano, Italy (E.A., M. Palazzini, P.G., P.P., G.Q., A. Garascia, C.G.). Search for more papers by this author , Cristina GiannattasioCristina Giannattasio Department of De Gasperis Cardio Center, Niguarda Hospital, Milano, Italy (E.A., M. Palazzini, P.G., P.P., G.Q., A. Garascia, C.G.). Department of Medicine and Surgery, Bicocca University, Milano, Italy (M. Palazzini, M.G., C.G.). Search for more papers by this author , Eric D. AdlerEric D. Adler https://orcid.org/0000-0002-4765-0188 Division of Cardiology, Department of Medicine, University of California San Diego (K.N.H., E.D.A.). Search for more papers by this author , Gianfranco SinagraGianfranco Sinagra https://orcid.org/0000-0003-2700-8478 Cardiovascular Department, Center for Diagnosis and Treatment of Cardiomyopathies, Azienda Sanitaria Universitaria Giuliano-Isontina, University of Trieste, Italy (G.S.). Search for more papers by this author , Frank RuschitzkaFrank Ruschitzka Department of Cardiology, University Heart Center, University Hospital Zurich and University of Zurich, Switzerland (V.A.R., F.R.). Center for Translational and Experimental Cardiology, Department of Cardiology, University Hospital Zurich, University of Zurich, Schlieren, Switzerland (F.R.). Search for more papers by this author , Paolo G. CamiciPaolo G. Camici https://orcid.org/0000-0001-5584-0750 San Raffaele Hospital and Vita Salute University, Milano, Italy (G. Peretto, S.S., P.G.C.). Search for more papers by this author , Marco MetraMarco Metra https://orcid.org/0000-0003-4846-8529 Institute of Cardiology, Azienda Socio-Sanitaria Territoriale Spedali Civili di Brescia and Department of Medical and Surgical Specialties, Radiological Sciences, and Public Health, University of Brescia, Italy (L.L., D.T., M.A., M.M.). Search for more papers by this author and Maurizio PieroniMaurizio Pieroni https://orcid.org/0000-0002-6830-4292 Cardiovascular Department, San Donato Hospital, Arezzo, Italy (M.C., L.B., M. Pieroni). Search for more papers by this author Originally published15 May 2023https://doi.org/10.1161/CIRCHEARTFAILURE.122.010315Circulation: Heart Failure. 2023;16Other version(s) of this articleYou are viewing the most recent version of this article. Previous versions: May 15, 2023: Ahead of Print Messenger RNA (mRNA) COVID-19 vaccination has been associated with a higher-than-expected occurrence of acute myocarditis, although the benefits of the vaccine greatly outweigh the risk of myocarditis. Even if the short-term prognosis of mRNA vaccine–related myocarditis has been reported to be favorable, scarce information is available on midterm prognosis. The current series included 7 to 9 patients with baseline and follow-up cardiac magnetic resonance imaging (CMRI).1,2 Questions on acute myocarditis following mRNA COVID-19 vaccination addressed by this study are the risk of adverse events after discharge and the extent of residual myocardial dysfunction and scar formation.We conducted a retrospective, multicenter study involving 31 hospitals in Europe and the United States. The Niguarda Hospital in Milano, Italy, acted as the coordinating center. The Institutional Review Board in Milano, Italy (Ethics Committee Milano Area 3), approved this study during the session of May 2022 (identifier 395-18052022). Written consent was not necessary due to the nature of the study. The data will not be shared because the current ethics approval does not allow us to share these data. We identified 77 patients with a confirmed diagnosis based on consistent cardiac symptoms, which occurred within 30 days since an mRNA COVID-19 vaccination, significant elevation of troponin levels, and CMRI findings consistent with acute myocarditis according to the 2018 updated Lake Louise criteria. Among patients with available follow-up (n=75; 97.4%), none died or required further hospitalization after a median time of 147 (first to third quartile [Q1–Q3], 74–215) days, and none of these patients experienced myocarditis recurrence. None of these patients received a further vaccination after the episode of myocarditis. Five patients (6.7%) had a subsequent SARS-CoV-2 infection without recurrent myocarditis.In 49 (63.6%) patients, a follow-up CMRI was available (median age, 25 [Q1–Q3, 30–34] years; female sex, 18.4%). There were no significant differences between patients with or without CMRI at follow-up (Table). The follow-up CMRI was performed at a median time of 137 days (Q1–Q3, 93–180) after hospitalization. Compared with the baseline CMRI, there were no changes in the left ventricular (LV) ejection fraction and right ventricular ejection fraction, with a median value of 60% and 57%, respectively. A dilated LV in the follow-up was observed in 5 cases (10.6%), with a median indexed LV end-diastolic volume of 97 (Q1–Q3, 95–112) mL/m2. The proportion of patients with persistent edema at follow-up based on conventional T2-weighted imaging was 20.4% (n=10), a figure significantly lower compared with the presence of edema at baseline (95.9%; n=47; in 2 patients, the presence of edema was based on T2 mapping imaging). LV segments with edema mainly involved the inferior or the inferolateral walls. Thirty-nine patients (79.6%) had a residual scar based on late gadolinium enhancement (LGE) on the follow-up CMRI, while on baseline CMRI, LGE was present in 100% of cases. Similarly, we observed a significant reduction of LGE-positive segments from a median of 4 (Q1–Q3, 3–7) to 2 (Q1–Q3, 1–4; P<0.001) at follow-up. LGE generally spared the anterior wall and the septum (only 3 patients; 6.1% had a residual septal LGE). Finally, pericardial effusion decreased from 16 (32.6%) to 3 (6.1%) patients (Table). No difference was found in the main morphofunctional CMRI parameters at follow-up depending on the type of vaccine administered, that is, BNT162b2 (Pfizer/BioNTech, n=36, 73.5%) or mRNA-1273 (Moderna, n=13, 26.5%). Furthermore, 48 (63.3%) patients had at least 1 echocardiogram after discharge, including 15 (31.2%) without follow-up CMRI, and all had preserved biventricular function without ventricular dilation (Table). When these data were compared with 105 (23.7%) of 443 acute myocarditis patients identified from the Lombardy registry with 2 CMRI scans within 1 year (median age, 32 [Q1–Q3, 23–40] years; women, 19.0%; median interval between the scans of 149 [Q1–Q3, 97–213] days),3 we observed a similar proportion of patients with LV ejection fraction 120 ms741 (1.3)*01 (2.1)*1.000ECG monitoring Nonsustained ventricular tachycardia758 (10.7)*5 (19.2)*3 (6.1)0.117 VT/VF751 (1.3)*1 (3.8)*00.347 Sustained atrial arrhythmias75000Cardiac biomarkers Troponin increase on admission (×fold URL)7780 (27–238)58 (24–171)83 (33–330)0.253 Troponin increase at peak (×fold URL)74108 (50–357)73 (39–243)122 (67–522)0.085 Day of troponin peak after admission181 (0–2)1 (0–2)2 (1–2)0.216 First CK-MB, µg/L3027 (10–45)10 (8–29)31 (14–62)0.078 Peak CK-MB, µg/L3231 (11–54)10 (8–38)34 (13–78)0.122 First NT-proBNP, ng/L46323 (136–610)219 (139–688)356 (125–571)0.961 First BNP945 (17–87)33 (12–81)45 (42–46)0.606Inflammatory biomarkers C-reactive protein increase on admission (×fold URL)738 (2–16)5 (2–11)8 (3–19)0.216 Eosinophilia754 (5.3)*2 (7.7)*2 (4.1)0.606Echocardiography‡Baseline echo (n=48 patients)Follow-up echo (n=48 patients)P value Days after hospitalization144 (59–197) LV EF on first echo, %7456 (50–60)56 (52–62)56 (50–60)0.45355 (84–60)60 (60–64)<0.001† Presence of segmental hypokinesia7436 (48.6)*12 (48.0)*24 (49.0)1.00026 (54.2)3 (6.2)<0.001† Inferior or lateral wall7433 (44.6)*9 (36.0)*24 (49.0)0.331 Anterior wall739 (12.3)*4 (16.0)*5 (10.4)*0.482 Septal wall738 (10.9)*3 (12.0)*5 (10.4)*1.000 LVEDD, mm4448 (45–52)48 (45–50)48 (45–52)0.59948 (46–52)48 (45–50)0.183 Dilated LV736 (8.2)*2 (8.3)*4 (8.2)1.0005 (10.4)00.056 Dilated RV7300000 RV-TAPSE <17 mm732 (2.7)*1 (4.2)*1 (2.0)1.0002 (4.2)00.242 Pericardial effusion7412 (16.2)*3 (12.0)*9 (18.4)0.74011 (22.9)0<0.001† Lowest LV EF value, %7356 (50–60)55 (51–61)56 (50–60)0.780Coronary angiography/CT scan excluding coronary artery disease7735 (45.4)10 (35.7)25 (51.0)0.238Available cardiac MRI‡Baselinecardiac MRI (n=49 patients)Follow-up cardiac MRI (n=49 patients)P value Days after hospitalization774 (2–7)3 (2–9)4 (2–7)0.6974 (2–7)137 (93–180) LV EF, %7659 (55–64)60 (55–64)59 (55–65)0.55659 (55–65)60 (57–64)0.507 LV EF <50%765 (6.6)*2 (3.6)*3 (6.2)*1.0003 (6.2)*00.117 LV EF <55%7614 (18.4)*5 (17.8)*9 (18.7)*1.0009 (18.7)*3 (6.1)0.071 Indexed LVEDV, mL/m26282 (72–88)82 (70–89)82 (73–88)0.96982 (73–88)75 (65–84)0.029† Dilated LV758 (10.6)*3 (10.7)7 (14.6)*1.0007 (14.6)*5 (10.6)*0.759 RV EF, %7357 (52–62)58 (52–62)56 (52–62)0.74056 (52–62)57 (52–61)0.563 Dilated RV752 (2.7)*1 (3.6)*1 (2.1)*1.0001 (2.1)*1 (2.1)*1.000 Edema on T2-w imaging7775 (97.4)28 (100)47 (95.9)0.53147 (95.9)10 (20.4)<0.001† Inferior7737 (48.0)11 (39.2)26 (53.0)0.34326 (53.1)3 (6.1)<0.001† Inferolateral7763 (81.8)21 (75.0)43 (87.7)0.20743 (87.7)4 (8.2)<0.001† Anterolateral7740 (51.9)14 (50.0)26 (53.1)0.81726 (53.1)0<0.001† Anterior7720 (26.0)4 (14.2)16 (32.6)0.10516 (32.6)1 (20.4)<0.001† Septal779 (11.7)3 (10.7)6 (12.2)1.0006 (12.2)2 (4.1)0.159 Presence of LGE7777 (100)28 (100)49 (100)49 (100)39 (79.6)0.001† Inferior7737 (48.0)11 (39.2)26 (53.0)0.34326 (53.1)8 (16.3)<0.001† Inferolateral7745 (58.4)13 (46.4)32 (65.3)0.14932 (65.3)12 (24.5)<0.001† Anterolateral7740 (51.9)14 (50.0)26 (53.1)0.81726 (53.1)8 (16.3)<0.001† Anterior7711 (14.3)2 (7.1)9 (18.4)0.3109 (18.4)00.003† Septal777 (9.1)2 (7.1)5 (10.2)1.0005 (10.2)3 (6.1)0.715 Increased T1 mapping signal3122 (71.0)*9 (75.0)*13 (68.4)*1.00013 (68.4)*4 (13.3)*<0.001† Increased T2 mapping signal4135 (85.3)*14 (87.5)*21 (84.0)*1.00021 (84.0)*3 (10.3)*<0.001† Pericardial effusion7710 (13.0)4 (14.3)16 (32.6)0.10616 (32.6)3 (6.1)0.004†Available histology, n (%)779 (11.7)3 (10.7)6 (12.2)1.000 Active myocarditis96 (66.7)*2 (66.7)*4 (66.7)*0.774Treatments Corticosteroids779 (11.7)3 (10.7)6 (12.2)1.000 Other immunosuppressive agents7711 (14.3)4 (14.3)7 (14.3)1.000 NSAIDs7740 (51.9)11 (39.2)29 (59.2)0.104In-hospital outcome Live7575 (100)*26 (100)*49 (100)* Dead75000 Transplanted/LVAD75000Data are reported as n (%) for categorical variables and as median (interquartile range, 1–3) for continuous variables. The Mann-Whitney U test was used to compare continuous variables of patients with or without follow-up CMR. The Wilcoxon matched-pair signed-rank test was used to analyze paired data of baseline vs follow-up CMR. Categorical variables were compared with the Fisher exact test. BNP indicates brain natriuretic peptide; bpm, beats per minute; CK-MB, creatine kinease-myocardial band isoenzyme; CMR, cardiac magnetic resonance; CMRI, cardiac magnetic resonance imaging; CT, computed tomography; EF, ejection fraction; LGE, late gadolinium enhancement; LV, left ventricle; LVAD, left ventricular assist device; LVEDD, left ventricular end-diastolic diameter; LVEDV, left ventricular end-diastolic volume; MRI, magnetic resonance imaging; NSAID, nonsteroidal anti-inflammatory drug; NT-proBNP, N-terminal pro-B-type natriuretic peptide; RT-PCR, real-time polymerase chain reaction; RV, right ventricle; T2-w, T2 weighted; TAPSE, tricuspid annular plane systolic excursion; URL, upper reference limit; VF, ventricular fibrillation; and VT, ventricular tachycardia.* The proportion of patients was calculated on the number of patients with available data.† P<0.05.‡ Presented CMRI and echocardiographic data are not obtained from a centralized revision of the original exams but are based on the available reports from each institute.In conclusion, we observed that in the midterm follow-up, patients who had acute myocarditis after the mRNA COVID-19 vaccine had preserved biventricular function, while 79.6% of patients had a residual scar and 20.4% had persistent edema. These figures are in line with CMRI finding in patients with other forms of myocarditis: after 6 months, edema based on T2-weighted imaging was present in 16% and LGE in 86% of the patients,4 also in agreement with our data derived from a subanalysis of the Lombardy registry of acute myocarditis. No clinical events were reported in the follow-up, and the few patients with COVID-19 after vaccination did not develop recurrent myocarditis. Longer follow-up is needed, even if published long-term data suggest that patients with preserved biventricular ejection fraction without septal LGE involvement have low rates of adverse clinical events.5 As a study limitation, we underline that the causal link between COVID-19 vaccination and myocarditis remains uncertain, albeit the short median time (3 days) from vaccination to symptom onset suggests causality.The observed CMRI findings at baseline and morphofunctional changes over time align with those of classic viral acute myocarditis with a good prognosis.5 This new information should further reassure patients who experience acute myocarditis after the mRNA COVID-19 vaccination.Article InformationSources of FundingThis work was supported by the Italian Ministry of Health (GR-2019-12368506).Disclosures Dr Ammirati received a grant from the Italian Ministry of Health (GR-2019-12368506; principal investigator of the investigator-driven MYTHS trial [Myocarditis Therapy With Steroids]) and a grant from the Italian Ministry of Health and NextGenerationEU (PNRR-MAD-2022-12376225) and is a consultant for Kiniksa and Cytokinetics. Dr Metra reports personal fees from Actelion, Amgen, AstraZeneca, Abbott, Bayer, Servier, Edwards Therapeutics, Livanova, Vifor pharma, and WindTree Therapeutics, as a member of Trials’ Committees or for speeches at sponsored meetings in the last 3 years. Dr Ruschitzka has not received personal payments by pharmaceutical companies or device manufacturers in the past 3 years (remuneration for the time spent in activities, such as participation as a steering committee member of clinical trials and a member of the Pfizer Research Award selection committee in Switzerland, were made directly to the University of Zurich). The Department of Cardiology (University Hospital of Zurich/University of Zurich) reports research, educational, and/or travel grants from Abbott, Abiomed, Alexion, Amgen, AstraZeneca, At the Limits Ltd, Bayer, Berlin Heart, B. Braun, Biosense Webster, Biosensors Europe AG, Biotronik, Boehringer Ingelheim, Boston Scientific, Bracco, Bristol Myers Squibb, Cardinal Health Switzerland, Concept Medical, Corteria, CSL, Daiichi Sankyo, Diatools AG, Edwards Lifesciences, Guidant Europe NV (BS), Hamilton Health Sciences, IHF, Innosuisse, Johnson/Johnson, Kaneka Corporation, Kantar, Kiniksa, Labormedizinisches Zentrum, MedAlliance, Medical Education Global Solutions, Medtronic, MicroPort, MSD, Mundipharma Medical Company, Novartis, Novo Nordisk, Orion, Pfizer, Quintiles Switzerland Sarl, RecorMedical, Roche Diagnostics, Roche Pharma, Sahajanand IN, Sanofi, Sarstedt AG, Servier, SIS Medical, Sorin CRM SAS, SSS International Clinical Research, Stromal, Terumo Deutschland, Trama Solutions, V-Wave, Vascular Medical, Vifor, Wissens Plus, and ZOLL. These grants do not impact on Dr Ruschitzka’s personal remuneration. The other authors report no conflicts.FootnotesFor Sources of Funding and Disclosures, see page 548.This manuscript was sent to Dr Michael Stanley Kiernan, MD, MS, MBA, Guest Editor, for review by expert referees, editorial decision, and final disposition.Correspondence to: Enrico Ammirati, MD, PhD, Niguarda Hospital, Piazza Ospedale Maggiore 3, 20162 Milano, Italy, Email enrico.ammirati@ospedaleniguarda.itLaura Lupi, MD, Institute of Cardiology, Azienda Socio-Sanitaria Territoriale Spedali Civili di Brescia and Department of Medical and Surgical Specialties, Radiological Sciences, and Public Health, University of Brescia, Piazzale Spedali Civili 1, 25123, Brescia, Italy, Email lalli.lupi@gmail.comReferences1. Patel YR, Shah NR, Lombardi K, Agarwal S, Salber G, Patel R, Poppas A, Atalay MK. Follow-up cardiovascular magnetic resonance findings in patients with COVID-19 vaccination-associated acute myocarditis.JACC Cardiovasc Imaging. 2022; 15:2007–2010. doi: 10.1016/j.jcmg.2022.06.009CrossrefMedlineGoogle Scholar2. Pareek M, Steele J, Asnes J, Baldassarre LA, Casale LR, Desai NR, Elder RW, Faherty E, Ferguson I, Fishman RF, et al. Short-term outcomes after myopericarditis related to COVID-19 vaccination.JACC Cardiovasc Imaging. 2022; 15:2002–2005. doi: 10.1016/j.jcmg.2022.03.026CrossrefMedlineGoogle Scholar3. Ammirati E, Cipriani M, Moro C, Raineri C, Pini D, Sormani P, Mantovani R, Varrenti M, Pedrotti P, Conca C, et al; Registro Lombardo delle Miocarditi. Clinical presentation and outcome in a contemporary cohort of patients with acute myocarditis: multicenter lombardy registry.Circulation. 2018; 138:1088–1099. doi: 10.1161/CIRCULATIONAHA.118.035319LinkGoogle Scholar4. Aquaro GD, 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.2019.08.1061CrossrefMedlineGoogle Scholar5. Aquaro GD, Perfetti M, Camastra G, Monti L, Dellegrottaglie S, Moro C, Pepe A, Todiere G, Lanzillo C, Scatteia A, et al; Cardiac Magnetic Resonance Working Group of the Italian Society of Cardiology. Cardiac MR with late gadolinium enhancement in acute myocarditis with preserved systolic function: ITAMY study.J Am Coll Cardiol. 2017; 70:1977–1987. doi: 10.1016/j.jacc.2017.08.044CrossrefMedlineGoogle Scholar Previous Back to top Next FiguresReferencesRelatedDetailsCited By Brociek E, Tymińska A, Giordani A, Caforio A, Wojnicz R, Grabowski M and Ozierański K (2023) Myocarditis: Etiology, Pathogenesis, and Their Implications in Clinical Practice, Biology, 10.3390/biology12060874, 12:6, (874) June 2023Vol 16, Issue 6 Advertisement Article Information Metrics © 2023 American Heart Association, Inc.https://doi.org/10.1161/CIRCHEARTFAILURE.122.010315PMID: 37183708 Originally publishedMay 15, 2023 KeywordsCOVID-19COVID-19 vaccinesmagnetic resonance spectroscopymyocarditisvaccinationPDF download Advertisement Subjects Cardiomyopathy Magnetic Resonance Imaging (MRI)
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