Top

Published in:

Open Access 01-12-2021 | Computed Tomography | Critical Review

Role of advanced imaging in COVID-19 cardiovascular complications

Authors: Federica Catapano, Livia Marchitelli, Giulia Cundari, Francesco Cilia, Giuseppe Mancuso, Giacomo Pambianchi, Nicola Galea, Paolo Ricci, Carlo Catalano, Marco Francone

Published in: Insights into Imaging | Issue 1/2021

Abstract

Clinical manifestations of COVID-19 patients are dominated by respiratory symptoms, but cardiac complications are commonly observed and associated with increased morbidity and mortality. Underlying pathological mechanisms of cardiac injury are still not entirely elucidated, likely depending on a combination of direct viral damage with an uncontrolled immune activation. Cardiac involvement in these patients ranges from a subtle myocardial injury to cardiogenic shock. Advanced cardiac imaging plays a key role in discriminating the broad spectrum of differential diagnoses. Present article aims to review the value of advanced multimodality imaging in patients with suspected SARS-CoV-2-related cardiovascular involvement and its essential role in risk stratification and tailored treatment strategies. Based on our experience, we also sought to suggest possible diagnostic algorithms for the rationale utilization of advanced imaging tools, such as cardiac CT and CMR, avoiding unnecessary examinations and diagnostic delays.

Guzik TJ, Mohiddin SA, Dimarco A et al (2020a) COVID-19 and the cardiovascular system: implications for risk assessment, diagnosis, and treatment options. Cardiovasc Res. https://doi.org/10.1093/cvr/cvaa106CrossRefPubMedPubMedCentral

Zheng YY, Ma YT, Zhang JY, Xie X (2020) COVID-19 and the cardiovascular system. Nat Rev Cardiol 17:259–260CrossRef

Shi S, Qin M, Shen B et al (2020) Association of cardiac injury with mortality in hospitalized patients with COVID-19 in Wuhan, China. JAMA Cardiol. https://doi.org/10.1001/jamacardio.2020.0950CrossRefPubMedPubMedCentral

Guo T, Fan Y, Chen M et al (2020) Cardiovascular implications of fatal outcomes of patients with coronavirus disease 2019 (COVID-19). JAMA Cardiol. https://doi.org/10.1001/jamacardio.2020.1017CrossRefPubMedPubMedCentral

Luetkens JA, Isaak A, Zimmer S et al (2020) Diffuse myocardial inflammation in COVID-19 associated myocarditis detected by multiparametric cardiac magnetic resonance imaging. Circ Cardiovasc Imaging 13:e010897CrossRef

Rajpal S, Tong MS, Borchers J et al (2020) Cardiovascular magnetic resonance findings in competitive athletes recovering from COVID-19 infection. JAMA Cardiol 6:116–118

Bangalore S, Sharma A, Slotwiner A et al (2020) ST-segment elevation in patients with Covid-19—a case series. N Engl J Med. https://doi.org/10.1056/nejmc2009020CrossRefPubMedPubMedCentral

Sauer F, Dagrenat C, Couppie P et al (2020) Pericardial effusion in patients with COVID-19: case series. Eur Hear J Case Rep. https://doi.org/10.1093/ehjcr/ytaa287CrossRef

Wu L, O’Kane AM, Peng H et al (2020) SARS-CoV-2 and cardiovascular complications: from molecular mechanisms to pharmaceutical management. Biochem Pharmacol 2020:114114CrossRef

10.

Nishiga M, Wang DW, Han Y et al (2020) COVID-19 and cardiovascular disease: from basic mechanisms to clinical perspectives. Nat Rev Cardiol 17:543–558CrossRef

11.

Lindner D, Fitzek A, Bräuninger H et al (2020) Association of cardiac infection with SARS-CoV-2 in confirmed COVID-19 autopsy cases. JAMA Cardiol. https://doi.org/10.1001/jamacardio.2020.3551CrossRefPubMed

12.

Oudit GY, Kassiri Z, Jiang C et al (2009) SARS-coronavirus modulation of myocardial ACE2 expression and inflammation in patients with SARS. Eur J Clin Invest. https://doi.org/10.1111/j.1365-2362.2009.02153.xCrossRefPubMedPubMedCentral

13.

Ferrario CM, Chappell MC, Tallant EA et al (1997) Counterregulatory actions of angiotensin-(1-7). Hypertension. https://doi.org/10.1161/01.HYP.30.3.535CrossRefPubMed

14.

Li B, Yang J, Zhao F et al (2020) Prevalence and impact of cardiovascular metabolic diseases on COVID-19 in China. Clin Res Cardiol 109:531–538CrossRef

15.

Corrales-Medina VF, Musher DM, Shachkina S, Chirinos JA (2013) Acute pneumonia and the cardiovascular system. Lancet 381:496–505CrossRef

16.

Nguyen JL, Yang W, Ito K et al (2016) Seasonal influenza infections and cardiovascular disease mortality. JAMA Cardiol. https://doi.org/10.1001/jamacardio.2016.0433CrossRefPubMedPubMedCentral

17.

Kwong JC, Schwartz KL, Campitelli MA et al (2018) Acute myocardial infarction after laboratory-confirmed influenza infection. N Engl J Med. https://doi.org/10.1056/nejmoa1702090CrossRefPubMed

18.

Bonow RO, O’Gara PT, Yancy CW (2020) Cardiology and COVID-19. JAMA J Am Med Assoc 5:751–753

19.

Huang C, Wang Y, Li X et al (2020) Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. https://doi.org/10.1016/S0140-6736(20)30183-5CrossRefPubMedPubMedCentral

20.

Wang D, Hu B, Hu C et al (2020) Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA J Am Med Assoc. https://doi.org/10.1001/jama.2020.1585CrossRef

21.

Zhou F, Yu T, Du R et al (2020) Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet. https://doi.org/10.1016/S0140-6736(20)30566-3CrossRefPubMedPubMedCentral

22.

Guan W, Ni Z, Hu Y et al (2020) Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med. https://doi.org/10.1056/nejmoa2002032CrossRefPubMedPubMedCentral

23.

Agricola E, Beneduce A, Esposito A et al (2020) Heart and lung multimodality imaging in COVID-19. JACC Cardiovasc Imaging 13:1792–1808CrossRef

24.

Guzik TJ, Mohiddin SA, Dimarco A et al (2020b) COVID-19 and the cardiovascular system: implications for risk assessment, diagnosis, and treatment options. Cardiovasc Res 116:1666–1687CrossRef

25.

Fung G, Luo H, Qiu Y et al (2016) Myocarditis. Circ Res 118:496–514CrossRef

26.

Alhogbani T (2016) Acute myocarditis associated with novel Middle East respiratory syndrome coronavirus. Ann Saudi Med. https://doi.org/10.5144/0256-4947.2016.78CrossRefPubMedPubMedCentral

27.

Zeng JH, Liu YX, Yuan J et al (2020) First case of COVID-19 complicated with fulminant myocarditis: a case report and insights. Infection. https://doi.org/10.1007/s15010-020-01424-5CrossRefPubMedPubMedCentral

28.

Kim IC, Kim JY, Kim HA, Han S (2020) COVID-19-related myocarditis in a 21-year-old female patient. Eur Heart J. https://doi.org/10.1093/eurheartj/ehaa288CrossRefPubMedPubMedCentral

29.

Trogen B, Gonzalez FJ, Shust GF (2020) COVID-19-associated myocarditis in an adolescent. Pediatr Infect Dis J. https://doi.org/10.1097/INF.0000000000002788CrossRefPubMed

30.

Esposito A, Palmisano A, Natale L et al (2020) Cardiac magnetic resonance characterization of myocarditis-like acute cardiac syndrome in COVID-19. JACC Cardiovasc Imaging 13:2462–2465CrossRef

31.

Inciardi RM, Lupi L, Zaccone G et al (2020) Cardiac involvement in a patient with coronavirus disease 2019 (COVID-19). JAMA Cardiol. https://doi.org/10.1001/jamacardio.2020.1096CrossRefPubMed

32.

Peretto G, Sala S, Caforio ALP (2020) Acute myocardial injury, MINOCA, or myocarditis? Improving characterization of coronavirus-associated myocardial involvement. Eur Heart J 41:2118–2119CrossRef

33.

Cundari G, Galea N, De Rubeis G et al (2020) Use of the new Lake Louise Criteria improves CMR detection of atypical forms of acute myocarditis. Int J Cardiovasc Imaging. https://doi.org/10.1007/s10554-020-02097-9CrossRefPubMed

34.

Huang L, Zhao P, Tang D et al (2020) Cardiac involvement in patients recovered from COVID-2019 identified using magnetic resonance imaging. JACC Cardiovasc Imaging. https://doi.org/10.1016/j.jcmg.2020.05.004CrossRefPubMedPubMedCentral

35.

Moody WE, Mahmoud-Elsayed HM, Senior J et al (2020) Impact of right ventricular dysfunction on mortality in patients hospitalized with COVID-19, according to race. CJC Open. https://doi.org/10.1016/j.cjco.2020.09.016CrossRefPubMedPubMedCentral

36.

Galea N, Carbone I, Cannata D et al (2013) Right ventricular cardiovascular magnetic resonance imaging: normal anatomy and spectrum of pathological findings. Insights Imaging 4:231CrossRef

37.

Sala S, Peretto G, Gramegna M et al (2020) Acute myocarditis presenting as a reverse Tako-Tsubo syndrome in a patient with SARS-CoV-2 respiratory infection. Eur Heart J. https://doi.org/10.1093/eurheartj/ehaa286CrossRefPubMedPubMedCentral

38.

Tian S, Xiong Y, Liu H et al (2020) Pathological study of the 2019 novel coronavirus disease (COVID-19) through postmortem core biopsies. Mod Pathol. https://doi.org/10.1038/s41379-020-0536-xCrossRefPubMedPubMedCentral

39.

Xu Z, Shi L, Wang Y et al (2020) Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respir Med. https://doi.org/10.1016/S2213-2600(20)30076-XCrossRefPubMedPubMedCentral

40.

Puntmann VO, Carerj ML, Wieters I et al (2020) Outcomes of cardiovascular magnetic resonance imaging in patients recently recovered from coronavirus disease 2019 (COVID-19). JAMA Cardiol. https://doi.org/10.1001/jamacardio.2020.3557CrossRefPubMedPubMedCentral

41.

Imazio M, Spodick DH, Brucato A et al (2010) Diagnostic issues in the clinical management of pericarditis. Int J Clin Pract 64:1384–1392CrossRef

42.

Farina A, Uccello G, Spreafico M et al (2020) SARS-CoV-2 detection in the pericardial fluid of a patient with cardiac tamponade. Eur J Intern Med 76:100CrossRef

43.

Blagojevic NR, Bosnjakovic D, Vukomanovic V et al (2020) Acute pericarditis and SARS-CoV-2: case report. Int J Infect Dis. https://doi.org/10.1016/j.ijid.2020.09.1440CrossRefPubMedPubMedCentral

44.

Dabbagh MF, Aurora L, D’Souza P et al (2020) Cardiac tamponade secondary to COVID-19. JACC Case Rep. https://doi.org/10.1016/j.jaccas.2020.04.009CrossRefPubMedPubMedCentral

45.

Purohit R, Kanwal A, Pandit A et al (2020) Acute myopericarditis with pericardial effusion and cardiac tamponade in a patient with COVID-19. Am J Case Rep. https://doi.org/10.12659/AJCR.925554CrossRefPubMed

46.

Asif T, Kassab K, Iskander F, Alyousef T (2020) Acute pericarditis and cardiac tamponade in a patient with COVID-19: a therapeutic challenge. Eur J Case Reports Intern Med. https://doi.org/10.12890/2020_001701CrossRef

47.

Hua A, O’Gallagher K, Sado D, Byrne J (2020) Life-threatening cardiac tamponade complicating myo-pericarditis in COVID-19. Eur Heart J. https://doi.org/10.1093/eurheartj/ehaa253CrossRefPubMedPubMedCentral

48.

Maisch B, Seferović PM, Ristić AD et al (2004) Guidelines on the diagnosis and management of pericardial diseases: executive summary. The task force on the diagnosis and management of pericardial diseases of the European Society of Cardiology. Eur Heart J 25:587–610CrossRef

49.

Adler Y, Charron P, Imazio M et al (2015) 2015 ESC guidelines for the diagnosis and management of pericardial diseases. Eur. Heart J 36:2921–2964CrossRef

50.

Kirkpatrick JN, Mitchell C, Taub C et al (2020) ASE statement on protection of patients and echocardiography service providers during the 2019 novel coronavirus outbreak: endorsed by the American College of Cardiology. J Am Soc Echocardiogr. https://doi.org/10.1016/j.echo.2020.04.001CrossRefPubMedPubMedCentral

51.

Long B, Brady WJ, Koyfman A, Gottlieb M (2020) Cardiovascular complications in COVID-19. Am J Emerg Med 38:1504–1507CrossRef

52.

Corrales-Medina VF, Alvarez KN, Weissfeld LA et al (2015) Association between hospitalization for pneumonia and subsequent risk of cardiovascular disease. JAMA J Am Med Assoc. https://doi.org/10.1001/jama.2014.18229CrossRef

53.

Akhmerov A, Marbán E (2020) COVID-19 and the heart. Circ Res 126:1443–1455CrossRef

54.

Pontone G, Baggiano A, Conte E et al (2020) “Quadruple rule out” with cardiac computed tomography in COVID-19 patient with equivocal acute coronary syndrome presentation. JACC Cardiovasc Imaging. https://doi.org/10.1016/j.jcmg.2020.04.012CrossRefPubMedPubMedCentral

55.

DeFilippis AP, Nasir K, Blaha MJ (2019) Myocardial infarction as a clinical end point in research. Circ Res. https://doi.org/10.1161/circresaha.119.315101CrossRefPubMed

56.

Meyer P, Degrauwe S, Van Delden C et al (2020) Typical takotsubo syndrome triggered by SARS-CoV-2 infection. Eur Heart J 41:1860CrossRef

57.

Oyarzabal L, Gómez-Hospital JA, Comin-Colet J (2020) Síndrome de tako-tsubo asociado con COVID-19. Rev Española Cardiol. https://doi.org/10.1016/j.recesp.2020.06.022CrossRef

58.

Iacucci I, Carbone I, Cannavale G et al (2013) Myocardial oedema as the sole marker of acute injury in Takotsubo cardiomyopathy: a cardiovascular magnetic resonance (CMR) study. Radiol Med. https://doi.org/10.1007/s11547-013-0931-1CrossRefPubMed

59.

Ng M-Y, Ferreira VM, Leung ST et al (2020) Recovered COVID-19 patients show ongoing subclinical myocarditis as revealed by cardiac magnetic resonance imaging. JACC Cardiovasc Imaging. https://doi.org/10.1016/j.jcmg.2020.08.012CrossRefPubMedPubMedCentral

60.

Wang Y, Wang Z, Tse G et al (2020) Cardiac arrhythmias in patients with COVID-19. J Arrhythmia 8:5250–5283

61.

Liu K, Fang YY, Deng Y et al (2020) Clinical characteristics of novel coronavirus cases in tertiary hospitals in Hubei Province. Chin Med J (Engl). https://doi.org/10.1097/CM9.0000000000000744CrossRefPubMedPubMedCentral

62.

Colon CM, Barrios JG, Chiles JW et al (2020) Atrial arrhythmias in COVID-19 patients. JACC Clin Electrophysiol 6:1193–1204CrossRef

63.

Thapa SB, Kakar TS, Mayer C, Khanal D (2020) Clinical outcomes of in-hospital cardiac arrest in COVID-19. JAMA Intern Med 28:e2024796

64.

Baldi E, Sechi GM, Mare C et al (2020) Out-of-hospital cardiac arrest during the covid-19 outbreak in Italy. N Engl J Med. https://doi.org/10.1056/nejmc2010418CrossRefPubMedPubMedCentral

65.

Chen N, Zhou M, Dong X et al (2020) Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study. Lancet. https://doi.org/10.1016/S0140-6736(20)30211-7CrossRefPubMedPubMedCentral

66.

Bikdeli B, Madhavan MV, Jimenez D et al (2020) COVID-19 and thrombotic or thromboembolic disease: implications for prevention, antithrombotic therapy, and follow-up: JACC state-of-the-art review. J Am Coll Cardiol 75:2950–2973CrossRef

67.

Helms J, Tacquard C, Severac F et al (2020) High risk of thrombosis in patients with severe SARS-CoV-2 infection: a multicenter prospective cohort study. Intensive Care Med. https://doi.org/10.1007/s00134-020-06062-xCrossRefPubMedPubMedCentral

68.

Panigada M, Bottino N, Tagliabue P et al (2020) Hypercoagulability of COVID-19 patients in intensive care unit: a report of thromboelastography findings and other parameters of hemostasis. J Thromb Haemost. https://doi.org/10.1111/jth.14850CrossRefPubMedPubMedCentral

69.

Grillet F, Behr J, Calame P et al (2020) Acute pulmonary embolism associated with COVID-19 pneumonia detected by pulmonary CT angiography. Radiology. https://doi.org/10.1148/radiol.2020201544CrossRefPubMedPubMedCentral

70.

Leonard-Lorant I, Delabranche X, Severac F et al (2020) Acute pulmonary embolism in COVID-19 patients on CT angiography and relationship to D-dimer levels. Radiology. https://doi.org/10.1148/radiol.2020201561CrossRefPubMedPubMedCentral

71.

Poissy J, Goutay J, Caplan M et al (2020) Pulmonary embolism in patients with COVID-19: awareness of an increased prevalence. Circulation 142:184–186CrossRef

72.

Konstantinides SV, Meyer G, Bueno H et al (2020) 2019 ESC Guidelines for the diagnosis and management of acute pulmonary embolism developed in collaboration with the European Respiratory Society (ERS). Eur Heart J 41:543–603CrossRef

73.

Rubin GD, Haramati LB, Kanne JP et al (2020) The role of chest imaging in patient management during the COVID-19 pandemic: a multinational consensus statement from the Fleischner society. Radiology. https://doi.org/10.1148/radiol.2020201365CrossRefPubMedPubMedCentral

74.

Revel MP, Parkar AP, Prosch H et al (2020) COVID-19 patients and the radiology department—advice from the European Society of Radiology (ESR) and the European Society of Thoracic Imaging (ESTI). Eur Radiol. https://doi.org/10.1007/s00330-020-06865-yCrossRefPubMedPubMedCentral

75.

Simpson S, Kay FU, Abbara S et al (2020) Radiological society of north america expert consensus statement on reporting chest CT findings related to COVID-19. Endorsed by the Society of Thoracic Radiology, the American College of Radiology, and RSNA. Radiol Cardiothorac Imaging. https://doi.org/10.1148/ryct.2020200152CrossRefPubMedCentral

76.

Esposito A, Gallone G, Palmisano A et al (2020) The current landscape of imaging recommendations in cardiovascular clinical guidelines: toward an imaging-guided precision medicine. Radiol Med. https://doi.org/10.1007/s11547-020-01286-9CrossRefPubMedPubMedCentral

77.

Han Y, Chen T, Bryant J et al (2020) Society for Cardiovascular Magnetic Resonance (SCMR) guidance for the practice of cardiovascular magnetic resonance during the COVID-19 pandemic. J Cardiovasc Magn Reson. https://doi.org/10.1186/s12968-020-00628-wCrossRefPubMedPubMedCentral

78.

Beitzke D, Salgado R, Francone M et al (2020) Cardiac imaging procedures and the COVID-19 pandemic: recommendations of the European Society of Cardiovascular Radiology (ESCR). Int J Cardiovasc Imaging 36:1801–1810CrossRef

79.

Galea N, Catapano F, Marchitelli L et al (2020) How to perform a Cardio-thoracic MRI in COVID-19: comprehensive assessment of heart, pulmonary arteries and lung parenchyma. Eur Hear J Cardiovasc Imaging. https://doi.org/10.1093/ehjci/jeaa335CrossRef

Title: Role of advanced imaging in COVID-19 cardiovascular complications
Authors: Federica Catapano
Livia Marchitelli
Giulia Cundari
Francesco Cilia
Giuseppe Mancuso
Giacomo Pambianchi
Nicola Galea
Paolo Ricci
Carlo Catalano
Marco Francone
Publication date: 01-12-2021
Publisher: Springer International Publishing
Keywords: Computed Tomography
Myocarditis
Computed Tomography
SARS-CoV-2
COVID-19
Published in: Insights into Imaging / Issue 1/2021
Electronic ISSN: 1869-4101
DOI: https://doi.org/10.1186/s13244-021-00973-z

At a glance: The STEP trials

Springer Medicine

Role of advanced imaging in COVID-19 cardiovascular complications

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2021

Cystic pancreatic lesions: MR imaging findings and management

Evidence levels in radiology: the insights into imaging approach

Understanding patient needs and gaps in radiology reports through online discussion forum analysis

Spectral CT of the abdomen: Where are we now?

CT imaging of peritoneal carcinomatosis with surgical correlation: a pictorial review

Significance of intra-nodular vessel sign in differentiating benign and malignant pulmonary ground-glass nodules