Electrocardiographic features of patients with COVID-19: One year of unexpected manifestations

Abstract

Coronavirus Disease 2019 (COVID-19) is the clinical manifestation of infection with Severe Acute Respiratory Syndrome Coronavirus-2 (SARS-CoV-2) [[1]Cheng Z.J. Shan J. 2019 Novel coronavirus: where we are and what we know.Infection. 2020; 48: 155-163https://doi.org/10.1007/s15010-020-01401-yCrossref PubMed Scopus (321) Google Scholar -[3]Angeli F. Zappa M. Reboldi G. Trapasso M. Cavallini C. Spanevello A. Verdecchia P. The pivotal link between ACE2 deficiency and SARS-CoV-2 infection: one year later.Eur J Intern Med. 2021; https://doi.org/10.1016/j.ejim.2021.09.007Abstract Full Text Full Text PDF Scopus (20) Google Scholar]. COVID-19 is frequently characterized by symptoms and signs of respiratory tract infection which may progress to pneumonia, acute respiratory distress syndrome (ARDS) and shock. [[1]Cheng Z.J. 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Nonetheless, COVID-19 can also cause a variety of cardiovascular complications including myocardial injury, myocarditis, acute myocardial infarction, stress cardiomyopathy, heart failure, dysrhythmias, and thromboembolic events [5Long B. Brady W.J. Koyfman A. Gottlieb M. Cardiovascular complications in COVID-19.Am J Emerg Med. 2020; 38: 1504-1507https://doi.org/10.1016/j.ajem.2020.04.048Abstract Full Text Full Text PDF PubMed Scopus (488) Google Scholar, 6Sandoval Y. Januzzi J.L. Jaffe A.S. Cardiac Troponin for Assessment of Myocardial Injury in COVID-19: JACC Review Topic of the Week.J Am Coll Cardiol. 2020; 76 (Jr): 1244-125810.1016/j.jacc.2020.06.068Crossref PubMed Scopus (202) Google Scholar [14]Zhou F. Yu T. Du R. Fan G. Liu Y. Liu Z. Xiang J. Wang Y. Song B. Gu X. 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: 1054-1062https://doi.org/10.1016/S0140-6736(20)30566-3Abstract Full Text Full Text PDF PubMed Scopus (15780) Google Scholar]. In this context, standard electrocardiography (ECG) showed to be a crucial test in the diagnosis of cardiac complications in patients with SARS-CoV-2. A study of 756 patients hospitalized with COVID-19 in New York, documented a range of COVID-19-related ECG findings including atrial fibrillation (5.6%), atrial and ventricular premature beats (7.7% and 3.4%, respectively), right bundle branch block (7.8%), left bundle branch block (1.5%), T-wave inversion (10.5%), and nonspecific repolarization abnormalities (29.0%) [[15]McCullough S.A. Goyal P. Krishnan U. Choi J.J. Safford M.M. Okin P.M. Electrocardiographic Findings in Coronavirus Disease-19: Insights on Mortality and Underlying Myocardial Processes.J Card Fail,. 2020; 26: 626-632https://doi.org/10.1016/j.cardfail.2020.06.005Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar]. These manifestations are believed to be the result of several pathogenetic mechanisms including cytokine and Angiotensin II storms, activation of coagulation cascade, hypoxic injury, endothelial and myocardial injuries, and atherosclerotic plaque destabilization and rupture [[5]Long B. Brady W.J. Koyfman A. Gottlieb M. Cardiovascular complications in COVID-19.Am J Emerg Med. 2020; 38: 1504-1507https://doi.org/10.1016/j.ajem.2020.04.048Abstract Full Text Full Text PDF PubMed Scopus (488) Google Scholar, [7]Angeli F. Marazzato J. Verdecchia P. Balestrino A. Bruschi C. Ceriana P. Chiovato L. Dalla Vecchia L.A. De Ponti R. 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Reboldi G. Fabbri L.M. Verdecchia P. Electrocardiographic features of patients with COVID-19 pneumonia.Eur J Intern Med. 2020; 78: 101-10610.1016/j.ejim.2020.06.015Abstract Full Text Full Text PDF PubMed Scopus (68) Google Scholar] published in the 2020 August issue of the European Journal of Internal Medicine [[18]Angeli F. Spanevello A. De Ponti R. Visca D. Marazzato J. Palmiotto G. Feci D. Reboldi G. Fabbri L.M. Verdecchia P. Electrocardiographic features of patients with COVID-19 pneumonia.Eur J Intern Med. 2020; 78: 101-10610.1016/j.ejim.2020.06.015Abstract Full Text Full Text PDF PubMed Scopus (68) Google Scholar] was one of the first studies to report a wide spectrum of unexpected ECG features of COVID-19 which exhibited a late onset and mostly occurred after recovery from the acute phase. In patients hospitalized for COVID-19 pneumonia, we found a 6% incidence of atrial fibrillation, a 2% incidence of brady-tachy syndrome, a 2% incidence of persistent ST-T changes not associated with increase in troponin I levels nor pericardial effusion, and a 12% incidence of ST-T changes associated with acute pericarditis [[18]Angeli F. Spanevello A. De Ponti R. Visca D. Marazzato J. Palmiotto G. Feci D. Reboldi G. Fabbri L.M. Verdecchia P. Electrocardiographic features of patients with COVID-19 pneumonia.Eur J Intern Med. 2020; 78: 101-10610.1016/j.ejim.2020.06.015Abstract Full Text Full Text PDF PubMed Scopus (68) Google Scholar]. The main aim of this narrative review was to explore incidence and pathogenesis of ECG features of COVID-19, with particularly emphasis to “unexpected” manifestations. Our review was performed according to standard methods. [[19]Haynes R.B. Kastner M. Wilczynski N.L. Hedges T. Developing optimal search strategies for detecting clinically sound and relevant causation studies in EMBASE.BMC Med Inform Decis Mak. 2005; 5: 8https://doi.org/10.1186/1472-6947-5-8Crossref PubMed Scopus (47) Google Scholar] We searched for eligible studies or case reports using research methodology filters [[20]Wong S.S. Wilczynski N.L. Haynes R.B. Hedges T. Developing optimal search strategies for detecting clinically relevant qualitative studies in MEDLINE.Stud Health Technol Inform. 2004; 107: 311-316PubMed Google Scholar]. We used PubMed, Scopus, and Web of Science for literature searches. The following search terms were used: “ECG”, “electrocardiography”, “EKG”, “COVID-19″, “SARS-CoV-2″, and “coronavirus”. At the beginning of the pandemic, much attention has been focused on ECG features of “common” cardiovascular complications of SARS-CoV-2 infections [8Zheng Y.Y. Ma Y.T. Zhang J.Y. Xie X. COVID-19 and the cardiovascular system.Nat Rev Cardiol. 2020; 17: 259-260https://doi.org/10.1038/s41569-020-0360-5Crossref PubMed Scopus (1909) Google Scholar, 9Akhmerov A. Marban E. COVID-19 and the Heart.Circ Res. 2020; https://doi.org/10.1161/CIRCRESAHA.120.317055Crossref PubMed Scopus (423) Google Scholar, 10Clerkin K.J. Fried J.A. Raikhelkar J. Sayer G. Griffin J.M. Masoumi A. Jain S.S. Burkhoff D. Kumaraiah D. Rabbani L. et al.Coronavirus Disease 2019 (COVID-19) and Cardiovascular Disease.Circulation. 2020; https://doi.org/10.1161/CIRCULATIONAHA.120.046941Crossref Scopus (964) Google Scholar [11]Fried J.A. Ramasubbu K. Bhatt R. Topkara V.K. Clerkin K.J. Horn E. Rabbani L. Brodie D. Jain S.S. Kirtane A. et al.The Variety of Cardiovascular Presentations of COVID-19.Circulation. 2020; https://doi.org/10.1161/CIRCULATIONAHA.120.047164Crossref Scopus (329) Google Scholar]. Several reports described “typical” features of COVID-19 complications including arrhythmias, ischemic ST-T abnormalities (spanning from acute coronary syndromes to Takotsubo syndrome), pulmonary embolism, acute heart failure, and myocarditis [[8]Zheng Y.Y. Ma Y.T. Zhang J.Y. Xie X. COVID-19 and the cardiovascular system.Nat Rev Cardiol. 2020; 17: 259-260https://doi.org/10.1038/s41569-020-0360-5Crossref PubMed Scopus (1909) Google Scholar [11]Fried J.A. Ramasubbu K. Bhatt R. Topkara V.K. Clerkin K.J. Horn E. Rabbani L. Brodie D. Jain S.S. Kirtane A. et al.The Variety of Cardiovascular Presentations of COVID-19.Circulation. 2020; https://doi.org/10.1161/CIRCULATIONAHA.120.047164Crossref Scopus (329) Google Scholar]. Remarkably, ECG abnormalities are common, being present up to 93% of critically ill patients [[21]Bertini M. Ferrari R. Guardigli G. Malagu M. Vitali F. Zucchetti O. D'Aniello E. Volta C.A. Cimaglia P. Piovaccari G. et al.Electrocardiographic features of 431 consecutive, critically ill COVID-19 patients: an insight into the mechanisms of cardiac involvement.Europace. 2020; 22: 1848-1854https://doi.org/10.1093/europace/euaa258Crossref PubMed Scopus (52) Google Scholar]. For these conditions, interpretation of the ECG is unchanged from the non-COVID-19 patient [[16]Long B. Brady W.J. Bridwell R.E. Ramzy M. Montrief T. Singh M. Gottlieb M. Electrocardiographic manifestations of COVID-19.Am J Emerg Med. 2021; 41: 96-103https://doi.org/10.1016/j.ajem.2020.12.060Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar]. It is the most common ECG manifestation overall in patients with COVID-19. It may reflect several underlying mechanisms including intrinsic sinus node hyperactivity, autonomic dysfunction and a hyperadrenergic state (fever, hypovolemia, hypoxia, pain, anxiety, and hypoperfusion) [[22]Olshansky B. Sullivan R.M. Inappropriate sinus tachycardia.Europace. 2019; 21: 194-207https://doi.org/10.1093/europace/euy128Crossref PubMed Scopus (30) Google Scholar]. Nonetheless, inflammatory cytokines released by patients with COVID-19 may affect the function of myocardial ion channels and perpetuate the sinus tachycardia [[23]Lazzerini P.E. Laghi-Pasini F. Boutjdir M. Capecchi P.L. Cardioimmunology of arrhythmias: the role of autoimmune and inflammatory cardiac channelopathies.Nat Rev Immunol. 2019; 19: 63-64https://doi.org/10.1038/s41577-018-0098-zCrossref PubMed Scopus (72) Google Scholar]. As in the general population, other etiologies of sinus tachycardia should be considered (i.e. pulmonary embolism) [[24]Desai A.D. Boursiquot B.C. Melki L. Wan E.Y. Management of Arrhythmias Associated with COVID-19.Curr Cardiol Rep. 2020; 23: 2https://doi.org/10.1007/s11886-020-01434-7Crossref PubMed Scopus (32) Google Scholar]. Atrial arrhythmias are the most commonly reported features in patients with COVID-19. Specifically, atrial fibrillation is commonly observed among COVID-19 patients (as detected in 19% to 21% of all cases) [[25]Gopinathannair R. Merchant F.M. Lakkireddy D.R. Etheridge S.P. Feigofsky S. Han J.K. Kabra R. Natale A. Poe S. Saha S.A. et al.COVID-19 and cardiac arrhythmias: a global perspective on arrhythmia characteristics and management strategies.J Interv Card Electrophysiol. 2020; 59: 329-336https://doi.org/10.1007/s10840-020-00789-9Crossref PubMed Scopus (97) Google Scholar, [26]Inciardi R.M. Adamo M. Lupi L. Cani D.S. Di Pasquale M. Tomasoni D. Italia L. Zaccone G. Tedino C. Fabbricatore D. et al.Characteristics and outcomes of patients hospitalized for COVID-19 and cardiac disease in Northern Italy.Eur Heart J. 2020; 41: 1821-1829https://doi.org/10.1093/eurheartj/ehaa388Crossref PubMed Scopus (311) Google Scholar]. The etiology of atrial arrhythmias remains to be fully elucidated. However, a reduction in angiotensin-converting enzyme 2 (ACE2) receptor availability, CD147- and sialic acid-spike protein interaction, enhanced inflammatory signaling, direct viral endothelial damage, metabolic derangements, electrolytes and acid-base balance abnormalities in the acute phase of COVID-19 have been suggested as putative mechanisms [[27]Gawalko M. Kaplon-Cieslicka A. Hohl M. Dobrev D. Linz D. COVID-19 associated atrial fibrillation: Incidence, putative mechanisms and potential clinical implications.Int J Cardiol Heart Vasc. 2020; 30100631https://doi.org/10.1016/j.ijcha.2020.100631Crossref PubMed Scopus (72) Google Scholar]. For atrial fibrillation, it is worth mentioning that epicardial fat has been linked to atrial electrical remodeling and the progression of atrial fibrillation [[28]Friedman D.J. Wang N. Meigs J.B. Hoffmann U. Massaro J.M. Fox C.S. Magnani J.W. Pericardial fat is associated with atrial conduction: the Framingham Heart Study.J Am Heart Assoc. 2014; 3e000477https://doi.org/10.1161/JAHA.113.000477Crossref PubMed Scopus (52) Google Scholar, [29]Thanassoulis G. Massaro J.M. O'Donnell C.J. Hoffmann U. Levy D. Ellinor P.T. Wang T.J. Schnabel R.B. Vasan R.S. Fox C.S. et al.Pericardial fat is associated with prevalent atrial fibrillation: the Framingham Heart Study.Circ Arrhythm Electrophysiol. 2010; 3: 345-350https://doi.org/10.1161/CIRCEP.109.912055Crossref PubMed Scopus (303) Google Scholar]. Although it is likely that atrial fibrillation may be related to COVID-19 infection (systemic hyperinflammation, fever, hypoxia, adrenergic tone), the involvement of epicardial adipocytes (as demonstrated by ECG signs of pericarditis and development of pericardial effusion) during SARS-CoV-2 infection could predispose to the development of atrial fibrillation [[18]Angeli F. Spanevello A. De Ponti R. Visca D. Marazzato J. Palmiotto G. Feci D. Reboldi G. Fabbri L.M. Verdecchia P. Electrocardiographic features of patients with COVID-19 pneumonia.Eur J Intern Med. 2020; 78: 101-10610.1016/j.ejim.2020.06.015Abstract Full Text Full Text PDF PubMed Scopus (68) Google Scholar]. These arrhythmias may occur among COVID-19 patients with myocarditis, metabolic abnormalities, or treated with QT interval prolonging medications [[5]Long B. Brady W.J. Koyfman A. Gottlieb M. Cardiovascular complications in COVID-19.Am J Emerg Med. 2020; 38: 1504-1507https://doi.org/10.1016/j.ajem.2020.04.048Abstract Full Text Full Text PDF PubMed Scopus (488) Google Scholar, [16]Long B. Brady W.J. Bridwell R.E. Ramzy M. Montrief T. Singh M. Gottlieb M. Electrocardiographic manifestations of COVID-19.Am J Emerg Med. 2021; 41: 96-103https://doi.org/10.1016/j.ajem.2020.12.060Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar, [30]Kang Y. Chen T. Mui D. Ferrari V. Jagasia D. Scherrer-Crosbie M. Chen Y. Han Y. 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Although the distinction between a ST-elevation myocardial infarction and myocarditis remains difficult, diagnosis of acute myocardial infarction is suggested with focal ST-segment elevations; conversely, myocardial injury demonstrates diffuse or widespread ST-segment elevation [[39]Bangalore S. Sharma A. Slotwiner A. Yatskar L. Harari R. Shah B. Ibrahim H. Friedman G.H. Thompson C. Alviar C.L. et al.ST-Segment Elevation in Patients with Covid-19 - A Case Series.N Engl J Med. 2020; 382: 2478-2480https://doi.org/10.1056/NEJMc2009020Crossref PubMed Scopus (472) Google Scholar]. It has been proposed that mechanisms of SARS-CoV-2 myocardial injury may be explained by a combination of direct cell injury and T-lymphocyte-mediated cytoxicity [[40]Buckley B.J.R. Harrison S.L. Fazio-Eynullayeva E. Underhill P. Lane D.A. Lip G.Y.H. 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The S1Q3T3 sign (prominent S wave in lead I, Q wave and inverted T wave in lead III) is a classic sign of acute cor pulmonale (acute pressure and volume overload of the right ventricle because of pulmonary hypertension) with increased right ventricular strain [[45]Chan T.C. Vilke G.M. Pollack M. Brady W.J. Electrocardiographic manifestations: pulmonary embolism.J Emerg Med. 2001; 21: 263-270https://doi.org/10.1016/s0736-4679(01)00389-4Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar]. Nonetheless, a single center, retrospective observational cohort study of COVID-19 patients diagnosed with pulmonary embolism showed that the S1Q3T3 sign was present in less than 10% of cases and that non-specific ST-T abnormalities or T wave changes were the most common ECG findings of pulmonary embolism [[44]Kho J. Ioannou A. Van den Abbeele K. Mandal A.K.J. Missouris C.G. Pulmonary embolism in COVID-19: Clinical characteristics and cardiac implications.Am J Emerg Med. 2020; 38: 2142-2146https://doi.org/10.1016/j.ajem.2020.07.054Abstract Full Text Full Text PDF PubMed Scopus (15) Google Scholar]. Evidences on unexpected ECG features of COVID-19 have been recently accrued, showing that uncertainties still overshadow our clinical knowledge in the field [[16]Long B. Brady W.J. Bridwell R.E. Ramzy M. Montrief T. Singh M. Gottlieb M. Electrocardiographic manifestations of COVID-19.Am J Emerg Med. 2021; 41: 96-103https://doi.org/10.1016/j.ajem.2020.12.060Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar, [36]Mehraeen E. Seyed Alinaghi S.A. Nowroozi A. Dadras O. Alilou S. Shobeiri P. Behnezhad F. Karimi A. A systematic review of ECG findings in patients with COVID-19.Indian Heart J. 2020; 72: 500-507https://doi.org/10.1016/j.ihj.2020.11.007Crossref PubMed Scopus (32) Google Scholar]. Interestingly, in our previous report of ECG features of patients with COVID-19 pneumonia, we documented that the development of ECG abnormalities during hospitalization was unrelated to the severity of respiratory function [[18]Angeli F. Spanevello A. De Ponti R. Visca D. Marazzato J. Palmiotto G. Feci D. Reboldi G. Fabbri L.M. Verdecchia P. Electrocardiographic features of patients with COVID-19 pneumonia.Eur J Intern Med. 2020; 78: 101-10610.1016/j.ejim.2020.06.015Abstract Full Text Full Text PDF PubMed Scopus (68) Google Scholar]. Moreover, abnormal serum levels of high sensitivity troponin I were recorded in the 38% of cases and ECG abnormalities showed a late onset from hospitalization and initiation of COVID-19 symptoms. The average time for development of ECG abnormalities was 20 and 30 days from admission and onset of symptoms, respectively [[18]Angeli F. Spanevello A. De Ponti R. Visca D. Marazzato J. Palmiotto G. Feci D. Reboldi G. Fabbri L.M. Verdecchia P. Electrocardiographic features of patients with COVID-19 pneumonia.Eur J Intern Med. 2020; 78: 101-10610.1016/j.ejim.2020.06.015Abstract Full Text Full Text PDF PubMed Scopus (68) Google Scholar]. Notably, a large proportion of patients (54%) experienced ECG abnormalities immediately before the scheduled discharge from hospital and after 2 consecutive negative nasopharyngeal swabs [[18]Angeli F. Spanevello A. De Ponti R. Visca D. Marazzato J. Palmiotto G. Feci D. Reboldi G. Fabbri L.M. Verdecchia P. Electrocardiographic features of patients with COVID-19 pneumonia.Eur J Intern Med. 2020; 78: 101-10610.1016/j.ejim.2020.06.015Abstract Full Text Full Text PDF PubMed Scopus (68) Google Scholar]. COVID-19 patients with acute respiratory failure may present QRS complex axis deviation with right ventricular strain (prominent R waves in leads V1 and V2, ST segment depression or T wave inversion in leads II, III, aVF, V1,V2, V3, and V4) [[33]Elias P. Poterucha T.J. Jain S.S. Sayer G. Raikhelkar J. Fried J. Clerkin K. Griffin J. DeFilippis E.M. Gupta A. et al.The Prognostic Value of Electrocardiogram at Presentation to Emergency Department in Patients With COVID-19.Mayo Clin Proc. 2020; 95: 2099-2109https://doi.org/10.1016/j.mayocp.2020.07.028Abstract Full Text Full Text PDF PubMed Scopus (31) Google Scholar]. Of note, right ventricular strain seems to be associated with an increased risk of death or need of mechanical ventilation during hospitalization [[33]Elias P. Poterucha T.J. Jain S.S. Sayer G. Raikhelkar J. Fried J. Clerkin K. Griffin J. DeFilippis E.M. Gupta A. et al.The Prognostic Value of Electrocardiogram at Presentation to Emergency Department in Patients With COVID-19.Mayo Clin Proc. 2020; 95: 2099-2109https://doi.org/10.1016/j.mayocp.2020.07.028Abstract Full Text Full Text PDF PubMed Scopus (31) Google Scholar, [46]Barman H.A. Atici A. Sahin I. Dogan O. Okur O. Tugrul S. Avci I. Yildirmak M.T. Gungor B. Dogan S.M. Prognostic value of right ventricular strain pattern on ECG in COVID-19 patients.Am J Emerg Med. 2021; 49: 1-5https://doi.org/10.1016/j.ajem.2021.05.039Abstract Full Text Full Text PDF PubMed Scopus (5) Google Scholar]. Incidence of bradicardias, atrioventricular blocks, and brady-tachy syndromes is not well characterized among COVID-19 patients [[16]Long B. Brady W.J. Bridwell R.E. Ramzy M. Montrief T. Singh M. Gottlieb M. Electrocardiographic manifestations of COVID-19.Am J Emerg Med. 2021; 41: 96-103https://doi.org/10.1016/j.ajem.2020.12.060Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar, [18]Angeli F. Spanevello A. De Ponti R. Visca D. Marazzato J. Palmiotto G. Feci D. Reboldi G. Fabbri L.M. Verdecchia P. Electrocardiographic features of patients with COVID-19 pneumonia.Eur J Intern Med. 2020; 78: 101-10610.1016/j.ejim.2020.06.015Abstract Full Text Full Text PDF PubMed Scopus (68) Google Scholar, [47]He J. Wu B. Chen Y. Tang J. Liu Q. Zhou S. Chen C. Qin Q. Huang K. Lv J. et al.Characteristic Electrocardiographic Manifestations in Patients With COVID-19.Can J Cardiol. 2020; 36 (966 e1-966 e4)https://doi.org/10.1016/j.cjca.2020.03.028Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar]. To date, these ECG manifestations are considered as disease-caused deterioration [[47]He J. Wu B. Chen Y. Tang J. Liu Q. Zhou S. Chen C. Qin Q. Huang K. Lv J. et al.Characteristic Electrocardiographic Manifestations in Patients With COVID-19.Can J Cardiol. 2020; 36 (966 e1-966 e4)https://doi.org/10.1016/j.cjca.2020.03.028Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar]. However, a recent case series by Dagher and co-workers [[48]Dagher L. Wanna B. Mikdadi G. Young M. Sohns C. Marrouche N.F. High-degree atrioventricular block in COVID-19 hospitalized patients.Europace. 2021; 23: 451-455https://doi.org/10.1093/europace/euaa333Crossref PubMed Scopus (10) Google Scholar] described four cases of COVID-19 patients who developed a transient high-degree atrioventricular block during the course of their hospitalization, not requiring permanent pacing [[48]Dagher L. Wanna B. Mikdadi G. Young M. Sohns C. Marrouche N.F. High-degree atrioventricular block in COVID-19 hospitalized patients.Europace. 2021; 23: 451-455https://doi.org/10.1093/europace/euaa333Crossref PubMed Scopus (10) Google Scholar]. Similar findings were also reported in our cohort [[18]Angeli F. Spanevello A. De Ponti R. Visca D. Marazzato J. Palmiotto G. Feci D. Reboldi G. Fabbri L.M. Verdecchia P. Electrocardiographic features of patients with COVID-19 pneumonia.Eur J Intern Med. 2020; 78: 101-10610.1016/j.ejim.2020.06.015Abstract Full Text Full Text PDF PubMed Scopus (68) Google Scholar] and by Eneizat Mahdawi and co-workers in a case series of heart blocks [[49]Eneizat Mahdawi T. Wang H. Haddadin F.I. Al-Qaysi D. Wylie J.V. Heart block in patients with coronavirus disease 2019: A case series of 3 patients infected with SARS-CoV-2.HeartRhythm Case Rep. 2020; 6: 652-656https://doi.org/10.1016/j.hrcr.2020.06.014Abstract Full Text Full Text PDF PubMed Scopus (25) Google Scholar]. Postmortem studies have identified pericarditis in about 20% of the COVID-19 cases [[50]Basso C. Leone O. Rizzo S. De Gaspari M. van der Wal A.C. Aubry M.C. Bois M.C. Lin P.T. Maleszewski J.J. Stone J.R. Pathological features of COVID-19-associated myocardial injury: a multicentre cardiovascular pathology study.Eur Heart J. 2020; 41: 3827-3835https://doi.org/10.1093/eurheartj/ehaa664Crossref PubMed Scopus (231) Google Scholar, [51]Hanley B. Naresh K.N. Roufosse C. Nicholson A.G. Weir J. Cooke G.S. Thursz M. Manousou P. Corbett R. Goldin R. et al.Histopathological findings and viral tropism in UK patients with severe fatal COVID-19: a post-mortem study.Lancet Microbe. 2020; 1: e245-e253https://doi.org/10.1016/S2666-5247(20)30115-4Abstract Full Text Full Text PDF PubMed Scopus (314) Google Scholar] and several case reports reported acute pericarditis in patients with SARS-CoV-2 infection with typical ECG signs (diffuse ST elevation and PR depression) [[52]Furqan M.M. Verma B.R. Cremer P.C. Imazio M. Klein A.L. Pericardial Diseases in COVID19: a Contemporary Review.Curr Cardiol Rep. 2021; 23: 90https://doi.org/10.1007/s11886-021-01519-xCrossref PubMed Scopus (22) Google Scholar [56]Kumar R. Kumar J. Daly C. Edroos S.A. Acute pericarditis as a primary presentation of COVID-19.BMJ Case Rep. 2020; 13https://doi.org/10.1136/bcr-2020-237617Crossref Scopus (27) Google Scholar]. Data from 63,822 COVID patients attending 50 Spanish emergency department during the COVID outbreak were used to analyze the frequency of (myo)pericarditis [[57]Miro O. Llorens P. Jimenez S. Pinera P. Burillo-Putze G. Martin A. Martin-Sanchez F.J. Gonzalez Del Castillo J. Spanish n. Investigators in Emergency Situations TeAm, Frequency of five unusual presentations in patients with COVID-19: results of the UMC-19-S1.Epidemiol Infect. 2020; 148: e189https://doi.org/10.1017/S0950268820001910Crossref PubMed Scopus (18) Google Scholar]. Compared with general emergency department population, COVID patients developed more frequently (myo)pericarditis (odds ratio [OR]: 1.45, 95% confidence interval [CI]: 1.07–1.97) [[57]Miro O. Llorens P. Jimenez S. Pinera P. Burillo-Putze G. Martin A. Martin-Sanchez F.J. Gonzalez Del Castillo J. Spanish n. Investigators in Emergency Situations TeAm, Frequency of five unusual presentations in patients with COVID-19: results of the UMC-19-S1.Epidemiol Infect. 2020; 148: e189https://doi.org/10.1017/S0950268820001910Crossref PubMed Scopus (18) Google Scholar]. Similarly, in a retrospective cohort study involving 718,365 patients with COVID-19, 10,706 (1.5%) patients developed new-onset pericarditis with a 6-months all-cause mortality of 15.5% (vs 6.7% in matched controls, OR: 2.55, 95% CI: 2.24 2.91) [[40]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 Invest. 2021; : e13679https://doi.org/10.1111/eci.13679Crossref PubMed Scopus (29) Google Scholar]. In our study cohort [[18]Angeli F. Spanevello A. De Ponti R. Visca D. Marazzato J. Palmiotto G. Feci D. Reboldi G. Fabbri L.M. Verdecchia P. Electrocardiographic features of patients with COVID-19 pneumonia.Eur J Intern Med. 2020; 78: 101-10610.1016/j.ejim.2020.06.015Abstract Full Text Full Text PDF PubMed Scopus (68) Google Scholar], ECG signs of acute pericarditis were the most common ECG manifestations of COVID-19. Notably, we diagnosed acute pericarditis by ECG evidence of new widespread concave ST elevation and PR depression throughout most of the limb (I, II, III, aVL, aVF) and precordial (V2-V6) leads, reciprocal ST depression, and PR elevation in aVR, and a ST segment/T wave ratio> 0.25 [[58]Adler Y. Charron P. Imazio M. Badano L. Baron-Esquivias G. Bogaert J. Brucato A. Gueret P. Klingel K. Lionis C. et al.2015 ESC Guidelines for the diagnosis and management of pericardial diseases: The Task Force for the Diagnosis and Management of Pericardial Diseases of the European Society of Cardiology (ESC)Endorsed by: The European Association for Cardio-Thoracic Surgery (EACTS).Eur Heart J. 2015; 36: 2921-2964https://doi.org/10.1093/eurheartj/ehv318Crossref PubMed Scopus (1028) Google Scholar]. We also noted late persistence of ECG signs of acute pericarditis (Fig. 1). Similar findings were documented by Soewono [[59]Soewono K.Y. Raney 3rd, K.C. Sidhu M.S. Pericarditis with pericardial effusion as a delayed complication of COVID-19.Proc (Bayl Univ Med Cent). 2021; 34: 629-630https://doi.org/10.1080/08998280.2021.1918975Crossref PubMed Scopus (4) Google Scholar] and Eiros and co-workers [[60]Eiros, R., Pericarditis and myocarditis long after SARS-CoV-2 infection: a cross-sectional descriptive study in health-care workers. https://www.medrxiv.org/content/10.1101/2020.07.12.20151316v1, 2020.Google Scholar]. Specifically, Soewono et al. described the case of a 30-year-old man with diagnosis of acute pericarditis 6 weeks after respiratory symptoms and a positive test for SARS-CoV-2 infection [[59]Soewono K.Y. Raney 3rd, K.C. Sidhu M.S. Pericarditis with pericardial effusion as a delayed complication of COVID-19.Proc (Bayl Univ Med Cent). 2021; 34: 629-630https://doi.org/10.1080/08998280.2021.1918975Crossref PubMed Scopus (4) Google Scholar]. Eiros et al. studied 139 health-care workers with confirmed past SARS-CoV-2 infection. Participants underwent clinical assessment, electrocardiography, laboratory tests including immune cell profiling and cardiac magnetic resonance (CMR). Overall, 14% of the total participants fulfilled the pericarditis criteria at week 10 [[60]Eiros, R., Pericarditis and myocarditis long after SARS-CoV-2 infection: a cross-sectional descriptive study in health-care workers. https://www.medrxiv.org/content/10.1101/2020.07.12.20151316v1, 2020.Google Scholar]. To date, the exact pathophysiological mechanism of pericardial involvement is not fully understood. As proposed mechanisms, systemic inflammatory reaction (with cytokine storm), and endothelial damage induced by COVID-19 may lead to pericardial involvement [[52]Furqan M.M. Verma B.R. Cremer P.C. Imazio M. Klein A.L. Pericardial Diseases in COVID19: a Contemporary Review.Curr Cardiol Rep. 2021; 23: 90https://doi.org/10.1007/s11886-021-01519-xCrossref PubMed Scopus (22) Google Scholar]. 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Transient Brugada-Like Electrocardiographic Pattern in a Patient With COVID-19.JACC Case Rep. 2020; 2: 1245-1249https://doi.org/10.1016/j.jaccas.2020.04.007Crossref PubMed Google Scholar], standard ECG revealed a Brugada-like pattern in a 61-year-old man presented with fever, shortness of breath, and chest pain (with coronary angiography demonstrating normal coronary arteries). In the second, a 49-year-old Bangladeshi man without significant medical history and positive for COVID-19 showed a Brugada syndrome, with the combination of the Brugada ECG pattern and clinical symptoms [[72]Chang D. Saleh M. Garcia-Bengo Y. Choi E. Epstein L. Willner J. COVID-19 Infection Unmasking Brugada Syndrome.HeartRhythm Case Rep. 2020; 6: 237-240https://doi.org/10.1016/j.hrcr.2020.03.012Abstract Full Text Full Text PDF PubMed Scopus (53) Google Scholar]. COVID-19 impacts the cardiovascular system, causing a variety of cardiac complications and leading to a range of ECG abnormalities [[73]Dherange P. 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