Cardiac MRI and Myocardial Injury in COVID-19: Diagnosis, Risk Stratification and Prognosis
Abstract
:1. Introduction
2. Myocardial Injury in COVID-19
2.1. Incidence and Significance
2.2. Mechanisms of Myocardial Injury
2.3. Inflammation-Mediated Myocardial Injury
3. Cardiac MRI for Myocardial Injury in COVID-19
3.1. Acute Myocarditis Workup and CMR
3.2. Pathophysiology of Myocarditis as Seen on CMR
3.2.1. Myocardial Edema
3.2.2. Hyperemia and Extracellular Expansion
3.2.3. Fibrosis and Scar Formation
3.3. Chronic Myocarditis and CMR
3.4. CMR during the COVID-19 Pandemic
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
Abbreviations
Coronavirus disease 2019 | COVID-19 |
Cardiac magnetic resonance imaging | CMR |
Early gadolinium enhancement | EGE |
Late gadolinium enhancement | LGE |
Electrocardiogram | ECG |
Left ventricular ejection fraction | LVEF |
Disseminated intravascular coagulation | DIC |
Acute coronary syndrome | ACS |
Transthoracic echocardiogram | TTE |
Transesophageal echocardiogram | TEE |
Endomyocardial biopsy | EMB |
Lake Louise criteria | LLC |
Ischemic cardiomyopathy | ICM |
Non-ischemic cardiomyopathy | NICM |
References
- Johns Hopkins Coronavirus Resource Center. COVID-19 Map; Johns Hopkins Center for Systems Science and Engineering: Baltimore, MD, USA, 2020. [Google Scholar]
- Hundley, W.G.; Bluemke, D.A.; Finn, J.P.; Flamm, S.D.; Fogel, M.A.; Friedrich, M.G.; Ho, V.B.; Jerosch-Herold, M.; Kramer, C.M.; Manning, W.J.; et al. ACCF/ACR/AHA/NASCI/SCMR 2010 expert consensus document on cardiovascular magnetic resonance: A report of the American College of Cardiology Foundation Task Force on Expert Consensus Documents. Circulaton 2010, 55, 2614–2662. [Google Scholar]
- Friedrich, M.G.; Larose, E.; Patton, D.; Dick, A.; Merchant, N.; Paterson, I. Canadian Society for Cardiovascular Magnetic Resonance (CanSCMR) recommendations for cardiovascular magnetic resonance image analysis and reporting. Can. J. Cardiol. 2013, 29, 260–265. [Google Scholar] [CrossRef] [PubMed]
- Ferreira, V.M.; Schulz-Menger, J.; Holmvang, G.; Kramer, C.M.; Carbone, I.; Sechtem, U.; Kindermann, I.; Gutberlet, M.; Cooper, L.T.; Liu, P.; et al. Cardiovascular magnetic resonance in nonischemic myocardial inflammation: Expert recommendations. J. Am. Coll. Cardiol. 2018, 72, 3158–3176. [Google Scholar] [CrossRef] [PubMed]
- Eike, N.; Kwong, R.Y.; Chandrashekhar, Y.S. CMR in Nonischemic Myocardial Inflammation: Solving the Problem of Diagnosing Myocarditis or Still Diagnostic Ambiguity? JACC Cardiovasc. Imaging 2020, 13, 163. [Google Scholar]
- ** for myocardial edema quantification: First in vivo validation in a porcine model of ischemia/reperfusion. J. Cardiovasc. Magn. Reson. 2015, 17, 1–9. [Google Scholar] [CrossRef] [Green Version]
- Ferreira, V.M.; Piechnik, S.K.; Dall’Armellina, E.; Karamitsos, T.D.; Francis, J.M.; Choudhury, R.P.; Friedrich, M.G.; Robson, M.D.; Piechnik, S.K. Non-contrast T1-map** detects acute myocardial edema with high diagnostic accuracy: A comparison to T2-weighted cardiovascular magnetic resonance. J. Cardiovasc. Magn. Reson. 2012, 14, 42. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Iles, L.M.; Ellims, A.H.; Llewellyn, H.; Hare, J.L.; Kaye, D.M.; McLean, C.A.; Taylor, A.J. Histological validation of cardiac magnetic resonance analysis of regional and diffuse interstitial myocardial fibrosis. Eur. Heart J. 2015, 16, 14–22. [Google Scholar] [CrossRef] [PubMed]
- Friedrich, M.G.; Marcotte, F. Cardiac Magnetic Resonance Assessment of Myocarditis. Circ. Cardiovasc. Imaging 2013, 6, 833–839. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Laissy, J.-P.; Messin, B.; Varenne, O.; Iung, B.; Karila-Cohen, D.; Schouman-Claeys, E.; Steg, P.G. MRI of acute myocarditis: A comprehensive approach based on various imaging sequences. Chest 2002, 122, 1638–1648. [Google Scholar] [CrossRef] [Green Version]
- Sramko, M.; Kubanek, M.; Tintera, J.; Kautznerova, D.; Weichet, J.; Maluskova, J.; Franekova, J.; Kautzner, J. Utility of Combination of Cardiac Magnetic Resonance Imaging and High-Sensitivity Cardiac Troponin T Assay in Diagnosis of Inflammatory Cardiomyopathy. Am. J. Cardiol. 2013, 111, 258–264. [Google Scholar] [CrossRef]
- Radunski, U.K.; Lund, G.K.; Stehning, C.; Schnackenburg, B.; Bohnen, S.; Adam, G.; Blankenberg, S.; Muellerleile, K. CMR in patients with severe myocarditis: Diagnostic value of quantitative tissue markers including extracellular volume imaging. JACC Cardiovasc. Imaging 2014, 7, 667–675. [Google Scholar] [CrossRef] [Green Version]
- Luetkens, J.A.; Doerner, J.; Thomas, D.K.; Dabir, D.; Gieseke, J.; Sprinkart, A.M.; Fimmers, R.; Stehning, C.; Homsi, R.; Schwab, J.O.; et al. Acute Myocarditis: Multiparametric Cardiac MR Imaging. Radiology 2014, 273, 383–392. [Google Scholar] [CrossRef] [Green Version]
- Schumm, J.; Greulich, S.; Wagner, A.; Grün, S.; Ong, P.; Bentz, K.; Klingel, K.; Kandolf, R.; Bruder, O.; Schneider, S.; et al. Cardiovascular magnetic resonance risk stratification in patients with clinically suspected myocarditis. J. Cardiovasc. Magn. Reson. 2014, 16, 14. [Google Scholar] [CrossRef] [Green Version]
- Mahrholdt, H.; Wagner, A.; Deluigi, C.C.; Kispert, E.; Hager, S.; Meinhardt, G.; Vogelsberg, H. Clinical Perspective. Circulation 2006, 114, 1581–1590. [Google Scholar] [CrossRef] [Green Version]
- Vermes, E.; Childs, H.; Faris, P.; Friedrich, M.G. Predictive value of CMR criteria for LV functional improvement in patients with acute myocarditis. Eur. Heart J. 2014, 15, 1140–1144. [Google Scholar] [CrossRef] [Green Version]
- Grün, S.; Schumm, J.; Greulich, S.; Wagner, A.; Schneider, S.; Bruder, O.; Kispert, E.-M. Long-term follow-up of biopsy-proven viral myocarditis: Predictors of mortality and incomplete recovery. J. Am. Coll. Cardiol. 2012, 59, 1604–1615. [Google Scholar] [CrossRef] [PubMed]
- Barone-Rochette, G.; Augier, C.; Rodière, M.; Quesada, J.; Foote, A.; Bouvaist, H.; Marlière, S.; Fagret, D.; Baguet, J.P.; Vanzetto, G. Potentially simple score of late gadolinium enhancement cardiac MR in acute myocarditis outcome. J. Magn. Reson. Imaging 2014, 40, 1347–1354. [Google Scholar] [CrossRef] [PubMed]
- Puntmann, V.O.; Carerj, M.L.; Wieters, I.; Fahim, M.; Arendt, C.; Hoffmann, J.; Shchendrygina, A.; Escher, F.; Vasa-Nicotera, M.; Zeiher, A.M.; et al. Outcomes of Cardiovascular Magnetic Resonance Imaging in Patients Recently Recovered from Coronavirus Disease 2019 (COVID-19). JAMA Cardiol. 2020, 5, 1265. [Google Scholar] [CrossRef]
- Ammann, P.; Naegeli, B.; Schuiki, E.; Straumann, E.; Frielingsdorf, J.; Rickli, H.; Bertel, O. Long-term outcome of acute myocarditis is independent of cardiac enzyme release. Int. J. Cardiol. 2003, 89, 217–222. [Google Scholar] [CrossRef]
- Kobayashi, D.; Aggarwal, S.; Kheiwa, A.; Shah, N. Myopericarditis in Children: Elevated Troponin I Level Does Not Predict Outcome. Pediatr. Cardiol. 2012, 33, 1040–1045. [Google Scholar] [CrossRef]
- Imazio, M.; Brucato, A.; Barbieri, A.; Ferroni, F.; Maestroni, S.; Ligabue, G.; Chinaglia, A.; Cumetti, D.; Della Casa, G.; Bonomi, F.; et al. Response to letter regarding article, good prognosis for pericarditis with and without myocardial involvement: Results from a multicenter, prospective cohort study. Circulation 2014, 129, e443–e444. [Google Scholar] [CrossRef] [Green Version]
- Berg, J.; Kottwitz, J.; Baltensperger, N.; Kissel, C.K.; Lovrinovic, M.; Mehra, T.; Scherff, F.; Schmied, C.M.; Templin, C.; Lüscher, T.F.; et al. Cardiac Magnetic Resonance Imaging in Myocarditis Reveals Persistent Disease Activity Despite Normalization of Cardiac Enzymes and Inflammatory Parameters at 3-Month Follow-Up. Circ. Heart Fail. 2017, 10, e004262. [Google Scholar] [CrossRef]
- Rischpler, C.; Nekolla, S.G.; Heusch, G.; Umutlu, L.; Rassaf, T.; Heusch, P.; Herrmann, K.; Nensa, F. Cardiac PET/MRI—An update. Eur. J. Hybrid Imaging 2019, 3, 1–17. [Google Scholar] [CrossRef] [Green Version]
- Nensa, F.; Kloth, J.; Tezgah, E.; Poeppel, T.D.; Heusch, P.; Goebel, J.; Nassenstein, K.; Schlosser, T. Feasibility of FDG-PET in myocarditis: Comparison to CMR using integrated PET/MRI. J. Nucl. Cardiol. 2018, 25, 785–794. [Google Scholar] [CrossRef]
- Hendel, R.C.; Friedrich, M.G.; Schulz-Menger, J.; Zemmrich, C.; Bengel, F.; Berman, D.S.; Camici, P.G.; Flamm, S.D.; Le Guludec, D.; Kim, R.; et al. CMR First-Pass Perfusion for Suspected Inducible Myocardial Ischemia. JACC Cardiovasc. Imaging 2016, 9, 1338–1348. [Google Scholar] [CrossRef]
- D’Angelo, T.; Grigoratos, C.; Mazziotti, S.; Bratis, K.; Pathan, F.; Blandino, A.; Elen, E.; Puntmann, V.O.; Nagel, E. High-throughput gadobutrol-enhanced CMR: A time and dose optimization study. J. Cardiovasc. Magn. Reson. 2017, 19, 83. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Foley, J.R.; Richmond, C.; Fent, G.J.; Bissell, M.; Levelt, E.; Dall’Armellina, E.; Swoboda, P.P.; Plein, S.; Greenwood, J.P. Rapid Cardiovascular Magnetic Resonance for Ischemic Heart Disease Investigation (RAPID-IHD). JACC Cardiovasc. Imaging 2020. [Google Scholar] [CrossRef] [PubMed]
- Wolk, M.J.; Bailey, S.R.; Doherty, J.U.; Douglas, P.S.; Hendel, R.C.; Kramer, C.M.; Min, J.K. ACCF/AHA/ASE/ASNC/HFSA/HRS/SCAI/SCCT/SCMR/STS 2013 Multimodality Appropriate Use Criteria for the Detection and Risk Assessment of Stable Ischemic Heart Disease: A Report of the American College of Cardiology Foundation Appropriate Use Criteria Task Force, American Heart Association, American Society of Echocardiography, American Society of Nuclear Cardiology, Heart Failure Society of America, Heart Rhythm Society, Society for Cardiovascular Angiography and Interventions, Society of Cardiovascular Computed Tomography, Society for Cardiovascular Magnetic Resonance, and Society of Thoracic Surgeons. J. Am. Coll. Cardiol. 2014, 63, 380–406. [Google Scholar] [PubMed] [Green Version]
- O’Gara, P.T.; Grayburn, P.A.; Badhwar, V.; Afonso, L.C.; Carroll, J.D.; Elmariah, S.; Kithcart, A.P. 2017 ACC expert consensus decision pathway on the management of mitral regurgitation: A report of the American College of Cardiology Task Force on Expert Consensus Decision Pathways. J. Am. Coll. Cardiol. 2017, 70, 2421–2449. [Google Scholar] [PubMed]
- Doherty, J.U.; Kort, S.; Mehran, R.; Schoenhagen, P.; Soman, P.; Dehmer, G.J.; Bashore, T.M. ACC/AATS/AHA/ASE/ASNC/HRS/SCAI/SCCT/SCMR/STS 2019 Appropriate Use Criteria for Multimodality Imaging in the Assessment of Cardiac Structure and Function in Nonvalvular Heart Disease: A Report of the American College of Cardiology Appropriate Use Criteria Task Force, American Association for Thoracic Surgery, American Heart Association, American Society of Echocardiography, American Society of Nuclear Cardiology, Heart Rhythm Society, Society for Cardiovascular Angiography and Interventions, Society of Cardiovascular Computed Tomography, Society for Cardiovascular Magnetic Resonance, and the Society of Thoracic Surgeons. J. Am. Coll. Cardiol. 2019, 73, 488–516. [Google Scholar] [PubMed]
- Carr, J.J.; Hendel, R.C.; White, R.D.; Patel, M.R.; Wolk, M.J.; Bettmann, M.A.; Douglas, P. 2013 appropriate utilization of cardiovascular imaging: A methodology for the development of joint criteria for the appropriate utilization of cardiovascular imaging by the American College of Cardiology Foundation and American College of Radiology. J. Am. Coll. Cardiol. 2013, 10, 456–463. [Google Scholar]
- Goyal, P.; Choi, J.J.; Pinheiro, L.C.; Schenck, E.J.; Chen, R.; Jabri, A.; Satlin, M.J.; Campion, T.R.; Nahid, M.; Ringel, J.B.; et al. Clinical Characteristics of Covid-19 in New York City. N. Engl. J. Med. 2020, 382, 2372–2374. [Google Scholar] [CrossRef]
- Kitkungvan, D.; Nabi, F.; Ghosn, M.G.; Dave, A.S.; Quinones, M.; Zoghbi, W.A.; Val-Derrabano, M.; Shah, D.J. Detection of LA and LAA thrombus by CMR in patients referred for pulmonary vein isolation. JACC Cardiovasc. Imaging 2016, 9, 809–818. [Google Scholar] [CrossRef] [Green Version]
- ClinicalTrials. Cardiopulmonary Inflammation and Multi-System Imaging During the Clinical Course of COVID-19 Infection in Asymptomatic and Symptomatic Persons—Full Text View. Available online: clinicaltri-als.gov/ct2/show/NCT04401449?term=cardiac+MRI (accessed on 1 January 2020).
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Sanghvi, S.K.; Schwarzman, L.S.; Nazir, N.T. Cardiac MRI and Myocardial Injury in COVID-19: Diagnosis, Risk Stratification and Prognosis. Diagnostics 2021, 11, 130. https://doi.org/10.3390/diagnostics11010130
Sanghvi SK, Schwarzman LS, Nazir NT. Cardiac MRI and Myocardial Injury in COVID-19: Diagnosis, Risk Stratification and Prognosis. Diagnostics. 2021; 11(1):130. https://doi.org/10.3390/diagnostics11010130
Chicago/Turabian StyleSanghvi, Saagar K., Logan S. Schwarzman, and Noreen T. Nazir. 2021. "Cardiac MRI and Myocardial Injury in COVID-19: Diagnosis, Risk Stratification and Prognosis" Diagnostics 11, no. 1: 130. https://doi.org/10.3390/diagnostics11010130