Outcomes of Cardiovascular Magnetic Resonance Imaging in Patients Recently Recovered From COVID-19 | Cardiology | JN Learning | AMA Ed Hub [Skip to Content]
Access to paid content on this site is currently suspended due to excessive activity being detected from your IP address 18.206.177.17. Please contact the publisher to request reinstatement.
Outline
Quiz
PDF
Cardiac Imaging

Outcomes of Cardiovascular Magnetic Resonance Imaging in Patients Recently Recovered From Coronavirus Disease 2019 (COVID-19)

Educational Objective
To review the pathophysiology of cardiac involvement in patients recently recovered from coronavirus disease 2019 (COVID-19) and most frequent abnormalities on cardiac magnetic resonance (CMR) imaging.
1 Credit CME
JAMA Cardiology
November 1, 2020
Original Investigation
Valentina O. Puntmann, MD, PhD1;
M. Ludovica Carerj, MD1,2;
Imke Wieters, MD3;
Masia Fahim3;
Christophe Arendt, MD1,4;
Jedrzej Hoffmann, MD1,5;
Anastasia Shchendrygina, MD, PhD1,6;
Felicitas Escher, MD7;
Mariuca Vasa-Nicotera, MD5;
Andreas M. Zeiher, MD5;
Maria Vehreschild, MD3;
Eike Nagel, MD1
Author Affiliations
  • 1Institute for Experimental and Translational Cardiovascular Imaging, DZHK Centre for Cardiovascular Imaging, University Hospital Frankfurt, Frankfurt am Main, Germany
  • 2Department of Biomedical Sciences and Morphological and Functional Imaging, University of Messina, Messina, Italy
  • 3Department of Infectious Diseases, University Hospital Frankfurt, Frankfurt am Main, Germany
  • 4Department of Diagnostic and Interventional Radiology, University Hospital Frankfurt, Frankfurt am Main, Germany
  • 5Department of Cardiology, Goethe University Hospital Frankfurt, Frankfurt am Main, Germany
  • 6Department of Hospital Therapy No. 1, I.M. Sechenov First Moscow State Medical University, Moscow, Russia
  • 7Institute for Cardiac Diagnostic and Therapy, Berlin, Germany
Read article on JAMA Network

MOC/CME Information

editorial comment icon
Editorial
Comment
 related articles icon
Related
Articles
 author interview icon
Interviews
 multimedia icon
Multimedia
Read Article Take Quiz
Key Points

Question  What are the cardiovascular effects in unselected patients with recent coronavirus disease 2019 (COVID-19)?

Findings  In this cohort study including 100 patients recently recovered from COVID-19 identified from a COVID-19 test center, cardiac magnetic resonance imaging revealed cardiac involvement in 78 patients (78%) and ongoing myocardial inflammation in 60 patients (60%), which was independent of preexisting conditions, severity and overall course of the acute illness, and the time from the original diagnosis.

Meaning  These findings indicate the need for ongoing investigation of the long-term cardiovascular consequences of COVID-19.

Abstract

Importance  Coronavirus disease 2019 (COVID-19) continues to cause considerable morbidity and mortality worldwide. Case reports of hospitalized patients suggest that COVID-19 prominently affects the cardiovascular system, but the overall impact remains unknown.

Objective  To evaluate the presence of myocardial injury in unselected patients recently recovered from COVID-19 illness.

Design, Setting, and Participants  In this prospective observational cohort study, 100 patients recently recovered from COVID-19 illness were identified from the University Hospital Frankfurt COVID-19 Registry between April and June 2020.

Exposure  Recent recovery from severe acute respiratory syndrome coronavirus 2 infection, as determined by reverse transcription–polymerase chain reaction on swab test of the upper respiratory tract.

Main Outcomes and Measures  Demographic characteristics, cardiac blood markers, and cardiovascular magnetic resonance (CMR) imaging were obtained. Comparisons were made with age-matched and sex-matched control groups of healthy volunteers (n = 50) and risk factor–matched patients (n = 57).

Results  Of the 100 included patients, 53 (53%) were male, and the mean (SD) age was 49 (14) years. The median (IQR) time interval between COVID-19 diagnosis and CMR was 71 (64-92) days. Of the 100 patients recently recovered from COVID-19, 67 (67%) recovered at home, while 33 (33%) required hospitalization. At the time of CMR, high-sensitivity troponin T (hsTnT) was detectable (greater than 3 pg/mL) in 71 patients recently recovered from COVID-19 (71%) and significantly elevated (greater than 13.9 pg/mL) in 5 patients (5%). Compared with healthy controls and risk factor–matched controls, patients recently recovered from COVID-19 had lower left ventricular ejection fraction, higher left ventricle volumes, and raised native T1 and T2. A total of 78 patients recently recovered from COVID-19 (78%) had abnormal CMR findings, including raised myocardial native T1 (n = 73), raised myocardial native T2 (n = 60), myocardial late gadolinium enhancement (n = 32), or pericardial enhancement (n = 22). There was a small but significant difference between patients who recovered at home vs in the hospital for native T1 mapping (median [IQR], 1119 [1092-1150] ms vs 1141 [1121-1175] ms; P = .008) and hsTnT (4.2 [3.0-5.9] pg/dL vs 6.3 [3.4-7.9] pg/dL; P = .002) but not for native T2 mapping. None of these measures were correlated with time from COVID-19 diagnosis (native T1: r = 0.07; P = .47; native T2: r = 0.14; P = .15; hsTnT: r = −0.07; P = .50). High-sensitivity troponin T was significantly correlated with native T1 mapping (r = 0.33; P < .001) and native T2 mapping (r = 0.18; P = .01). Endomyocardial biopsy in patients with severe findings revealed active lymphocytic inflammation. Native T1 and T2 were the measures with the best discriminatory ability to detect COVID-19–related myocardial pathology.

Conclusions and Relevance  In this study of a cohort of German patients recently recovered from COVID-19 infection, CMR revealed cardiac involvement in 78 patients (78%) and ongoing myocardial inflammation in 60 patients (60%), independent of preexisting conditions, severity and overall course of the acute illness, and time from the original diagnosis. These findings indicate the need for ongoing investigation of the long-term cardiovascular consequences of COVID-19.

Sign in to take quiz and track your certificates

Buy This Activity

JN Learning™ is the home for CME and MOC from the JAMA Network. Search by specialty or US state and earn AMA PRA Category 1 CME Credit™ from articles, audio, Clinical Challenges and more. Learn more about CME/MOC

Related Articles

  1. Coronavirus Disease 2019 (COVID-19) and the Heart
    1.00 CME

  2. Errors in Statistical Numbers and Data

  3. Errors in Statistical Numbers and Data in Study of Cardiovascular Magnetic Resonance Imaging in Patients Recently Recovered From COVID-19

  4. Cardiac Involvement After Recovering From COVID-19

  5. Cardiac Involvement After Recovering From COVID-19

  6. Younger Adults Cautioned to Take COVID-19 Seriously as Demographics Shift
    1.00 CME

  7. JAMA Network Articles of the Year 2020

  8. Researchers Investigate What COVID-19 Does to the Heart

See More

View All Featured

See More About

Cardiology Infectious Diseases Cardiac Imaging Radiology Coronavirus (COVID-19)
Article Information

Accepted for Publication: July 6, 2020.

Published Online: July 27, 2020. doi:10.1001/jamacardio.2020.3557

Correction: This article was corrected on August 25, 2020, to fix pervasive errors in statistical numbers and data in the Abstract, Methods and Results sections, Tables, and Figures 1 and 2.

Open Access: This is an open access article distributed under the terms of the CC-BY License. © 2020 Puntmann VO et al. JAMA Cardiology.

Corresponding Author: Eike Nagel, MD, Institute for Experimental and Translational Cardiovascular Imaging, DZHK Centre for Cardiovascular Imaging, University Hospital Frankfurt, Theodor-Stern-Kai 7, Frankfurt am Main 60590, Germany (eike.nagel@cardiac-imaging.org).

Author Contributions: Drs Puntmann and Nagel had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Study concept and design: Puntmann, Shchendrygina, Vasa-Nicotera, Zeiher, Nagel.

Acquisition, analysis, or interpretation of data: Puntmann, Carerj, Wieters, Fahim, Arendt, Hoffmann, Escher, Vehreschild, Nagel.

Drafting of the manuscript: Puntmann, Shchendrygina, Nagel.

Critical revision of the manuscript for important intellectual content: Puntmann, Carerj, Wieters, Fahim, Arendt, Hoffmann, Escher, Vasa-Nicotera, Zeiher, Vehreschild, Nagel.

Statistical analysis: Puntmann, Nagel.

Obtained funding: Puntmann, Zeiher, Nagel.

Administrative, technical, or material support: Puntmann, Carerj, Wieters, Fahim, Arendt, Escher, Vehreschild, Nagel.

Study supervision: Puntmann, Wieters, Arendt, Vasa-Nicotera, Vehreschild, Nagel.

Conflict of Interest Disclosures: Dr Escher has received personal fees from Institut Kardiale Diagnostik und Therapie outside the submitted work. Dr Zeiher has received grants from the German Centre for Cardiovascular Research during the conduct of the study and personal fees from Sanofi, Amgen, Boehringer Ingelheim, and Novo Nordisk outside the submitted work. Dr Vehreschild has received grants from BioNTech and Takeda outside the submitted work. Dr Nagel has received grants from Bayer, the German Ministry for Education and Research, Deutsche Herzstiftung e.V., Neosoft Technologies, and Cardio-Pulmonary Institute and personal fees from Bayer. No other disclosures were reported.

Funding/Support: Drs Puntmann, Arendt, Escher, Vasa-Nicotera, Zeiher, and Nagel were supported by grants from the German Ministry of Education and Research via the German Centre for Cardiovascular Research (DZHK) partner site RheinMain, Deutsche Herzstiftung e.V., Bayer, and Cardio-Pulmonary Institute

Role of the Funder/Sponsor: The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Additional Contributions: We acknowledge the dedicated support of clinical research support staff of the Institute of Experimental and Translational Cardiovascular Imaging, including Tammy Wolf, Thourier Azdad, Franziska Weis, Deniz Desik, BA, and Layla Laghchioua, MSc, as well as of the Department of Infectious Diseases, University Hospital Frankfurt. We are very grateful to our colleagues of the Department of Anaesthesiology, Intensive Care Medicine and Pain Therapy, University Hospital Frankfurt, Frankfurt am Main, Germany, for treating all critically ill patients with COVID-19. Contributors were not compensated for their work.

References
1.
Shi  S , Qin  M , Shen  B ,  et al.  Association of cardiac injury with mortality in hospitalized patients with COVID-19 in Wuhan, China.   JAMA Cardiol. Published online March 25, 2020. doi:10.1001/jamacardio.2020.0950PubMedGoogle Scholar
2.
Guo  T , Fan  Y , Chen  M ,  et al.  Cardiovascular implications of fatal outcomes of patients with coronavirus disease 2019 (COVID-19).   JAMA Cardiol. Published online March 27, 2020. doi:10.1001/jamacardio.2020.1017PubMedGoogle Scholar
3.
Inciardi  RM , Lupi  L , Zaccone  G ,  et al.  Cardiac involvement in a patient with coronavirus disease 2019 (COVID-19).   JAMA Cardiol. Published online March 27, 2020. doi:10.1001/jamacardio.2020.1096PubMedGoogle Scholar
4.
Li  H , Liu  L , Zhang  D ,  et al.  SARS-CoV-2 and viral sepsis: observations and hypotheses.   Lancet. 2020;395(10235):1517-1520. doi:10.1016/S0140-6736(20)30920-XPubMedGoogle ScholarCrossref
5.
Ruan  Q , Yang  K , Wang  W , Jiang  L , Song  J .  Clinical predictors of mortality due to COVID-19 based on an analysis of data of 150 patients from Wuhan, China.   Intensive Care Med. 2020;46(5):846-848. doi:10.1007/s00134-020-05991-xPubMedGoogle ScholarCrossref
6.
Chen  L , Li  X , Chen  M , Feng  Y , Xiong  C .  The ACE2 expression in human heart indicates new potential mechanism of heart injury among patients infected with SARS-CoV-2.   Cardiovasc Res. 2020;116(6):1097-1100. doi:10.1093/cvr/cvaa078PubMedGoogle ScholarCrossref
7.
Varga  Z , Flammer  AJ , Steiger  P ,  et al.  Endothelial cell infection and endotheliitis in COVID-19.   Lancet. 2020;395(10234):1417-1418. doi:10.1016/S0140-6736(20)30937-5PubMedGoogle ScholarCrossref
8.
Xu  Z , Shi  L , Wang  Y ,  et al.  Pathological findings of COVID-19 associated with acute respiratory distress syndrome.   Lancet Respir Med. 2020;8(4):420-422. doi:10.1016/S2213-2600(20)30076-XPubMedGoogle ScholarCrossref
9.
Wei  X , Fang  Y , Hu  H .  Glucocorticoid and immunoglobulin to treat viral fulminant myocarditis.   Eur Heart J. 2020;41(22):2122-2122. doi:10.1093/eurheartj/ehaa357PubMedGoogle ScholarCrossref
10.
Huang  L , Zhao  P , Tang  D ,  et al.  Cardiac involvement in recovered COVID-19 patients identified by magnetic resonance imaging.   JACC Cardiovasc Imaging. Published online May 12, 2020. doi:10.1016/j.jcmg.2020.05.004Google Scholar
11.
Improving Cardiovascular Risk Stratification Using T1 Mapping in General Population (IMPReSSION). ClinicalTrials.gov identifier: NCT04444128. Updated June 23, 2020. Accessed July 6, 2020. https://clinicaltrials.gov/ct2/show/NCT04444128
12.
International T1 Multicenter Outcome Study (T1Outcome-DE). ClinicalTrials.gov identifier: NCT03749343. Updated November 21, 2018. Accessed July 6, 2020. https://clinicaltrials.gov/ct2/show/NCT03749343
13.
Harris  PA , Taylor  R , Thielke  R , Payne  J , Gonzalez  N , Conde  JG .  Research electronic data capture (REDCap)—a metadata-driven methodology and workflow process for providing translational research informatics support.   J Biomed Inform. 2009;42(2):377-381. doi:10.1016/j.jbi.2008.08.010PubMedGoogle ScholarCrossref
14.
Giannitsis  E , Kurz  K , Hallermayer  K , Jarausch  J , Jaffe  AS , Katus  HA .  Analytical validation of a high-sensitivity cardiac troponin T assay.   Clin Chem. 2010;56(2):254-261. doi:10.1373/clinchem.2009.132654PubMedGoogle ScholarCrossref
15.
Fernández-Jiménez  R , Sánchez-González  J , Agüero  J ,  et al.  Fast T2 gradient-spin-echo (T2-GraSE) mapping for myocardial edema quantification: first in vivo validation in a porcine model of ischemia/reperfusion.   J Cardiovasc Magn Reson. 2015;17(1):92. doi:10.1186/s12968-015-0199-9PubMedGoogle ScholarCrossref
16.
Giri  S , Chung  Y-C , Merchant  A ,  et al.  T2 quantification for improved detection of myocardial edema.   J Cardiovasc Magn Reson. 2009;11(1):56. doi:10.1186/1532-429X-11-56PubMedGoogle ScholarCrossref
17.
Verhaert  D , Thavendiranathan  P , Giri  S ,  et al.  Direct T2 quantification of myocardial edema in acute ischemic injury.   JACC Cardiovasc Imaging. 2011;4(3):269-278. doi:10.1016/j.jcmg.2010.09.023PubMedGoogle ScholarCrossref
18.
Puntmann  VO , Valbuena  S , Hinojar  R ,  et al; SCMR Clinical Trial Writing Group.  Society for Cardiovascular Magnetic Resonance (SCMR) expert consensus for CMR imaging endpoints in clinical research: part I—analytical validation and clinical qualification.   J Cardiovasc Magn Reson. 2018;20(1):67. doi:10.1186/s12968-018-0484-5PubMedGoogle ScholarCrossref
19.
Rogers  T , Dabir  D , Mahmoud  I ,  et al.  Standardization of T1 measurements with MOLLI in differentiation between health and disease—the ConSept study.   J Cardiovasc Magn Reson. 2013;15(1):78. doi:10.1186/1532-429X-15-78PubMedGoogle ScholarCrossref
20.
Schulz-Menger  J , Bluemke  DA , Bremerich  J ,  et al.  Standardized image interpretation and post processing in cardiovascular magnetic resonance: Society for Cardiovascular Magnetic Resonance (SCMR) board of trustees task force on standardized post processing.   J Cardiovasc Magn Reson. 2013;15(1):35. doi:10.1186/1532-429X-15-35PubMedGoogle ScholarCrossref
21.
Dabir  D , Child  N , Kalra  A ,  et al.  Reference values for healthy human myocardium using a T1 mapping methodology: results from the International T1 Multicenter cardiovascular magnetic resonance study.   J Cardiovasc Magn Reson. 2014;16(1):69. doi:10.1186/s12968-014-0069-xPubMedGoogle ScholarCrossref
22.
Puntmann  V , Foote  L , Hinojar Baydes  R , Higgins  D , Nagel  E .  130 Reproducibility of T1 and T2 mapping in health and disease, and assessment of T2 variability across the normal myocardium.   Heart. 2014;100:A76. doi:10.1136/heartjnl-2014-306118.130Google ScholarCrossref
23.
Puntmann  VO , Carr-White  G , Jabbour  A ,  et al; International T1 Multicentre CMR Outcome Study.  Native T1 and ECV of noninfarcted myocardium and outcome in patients with coronary artery disease.   J Am Coll Cardiol. 2018;71(7):766-778. doi:10.1016/j.jacc.2017.12.020PubMedGoogle ScholarCrossref
24.
Puntmann  VO , Carr-White  G , Jabbour  A ,  et al; International T1 Multicentre CMR Outcome Study.  T1-mapping and outcome in nonischemic cardiomyopathy: all-cause mortality and heart failure.   JACC Cardiovasc Imaging. 2016;9(1):40-50. doi:10.1016/j.jcmg.2015.12.001PubMedGoogle ScholarCrossref
25.
Gravinay  P , Issa  N , Girard  D , Camou  F , Cochet  H .  CMR and serology to diagnose COVID-19 infection with primary cardiac involvement.   Eur Heart J Cardiovasc Imaging. Published online June 17, 2020. doi:10.1093/ehjci/jeaa169PubMedGoogle Scholar
26.
Luetkens  JA , Isaak  A , Zimmer  S ,  et al.  Diffuse myocardial inflammation in COVID-19 associated myocarditis detected by multiparametric cardiac magnetic resonance imaging.   Circ Cardiovasc Imaging. 2020;13(5):e010897. doi:10.1161/CIRCIMAGING.120.010897PubMedGoogle Scholar
27.
Caforio  ALP , Pankuweit  S , Arbustini  E ,  et al; European Society of Cardiology Working Group on Myocardial and Pericardial Diseases.  Current state of knowledge on aetiology, diagnosis, management, and therapy of myocarditis: a position statement of the European Society of Cardiology Working Group on Myocardial and Pericardial Diseases.   Eur Heart J. 2013;34(33):2636-2648. doi:10.1093/eurheartj/eht210PubMedGoogle ScholarCrossref
28.
Schumm  J , Greulich  S , Wagner  A ,  et al.  Cardiovascular magnetic resonance risk stratification in patients with clinically suspected myocarditis.   J Cardiovasc Magn Reson. 2014;16(1):14. doi:10.1186/1532-429X-16-14PubMedGoogle ScholarCrossref
29.
Kindermann  I , Kindermann  M , Kandolf  R ,  et al.  Predictors of outcome in patients with suspected myocarditis.   Circulation. 2008;118(6):639-648. doi:10.1161/CIRCULATIONAHA.108.769489PubMedGoogle ScholarCrossref
30.
Gulati  A , Jabbour  A , Ismail  TF ,  et al.  Association of fibrosis with mortality and sudden cardiac death in patients with nonischemic dilated cardiomyopathy.   JAMA. 2013;309(9):896-908. doi:10.1001/jama.2013.1363PubMedGoogle ScholarCrossref
31.
Grün  S , Schumm  J , Greulich  S ,  et al.  Long-term follow-up of biopsy-proven viral myocarditis: predictors of mortality and incomplete recovery.   J Am Coll Cardiol. 2012;59(18):1604-1615. doi:10.1016/j.jacc.2012.01.007PubMedGoogle ScholarCrossref
32.
Winau  L , Hinojar Baydes  R , Braner  A ,  et al.  High-sensitive troponin is associated with subclinical imaging biosignature of inflammatory cardiovascular involvement in systemic lupus erythematosus.   Ann Rheum Dis. 2018;77(11):1590-1598. doi:10.1136/annrheumdis-2018-213661PubMedGoogle ScholarCrossref
If you are not a JN Learning subscriber, you can either:
Subscribe to JN Learning for one year
Buy this activity
jn-learning_Modal_Multimedia_LoginSubscribe_Purchase
Close
If you are not a JN Learning subscriber, you can either:
Subscribe to JN Learning for one year
Buy this activity
jn-learning_Modal_Multimedia_LoginSubscribe_Purchase
Close
With a personal account, you can:
  • Access free activities and track your credits
  • Personalize content alerts
  • Customize your interests
  • Fully personalize your learning experience
Education Center Collection Sign In Modal Right
Close

Name Your Search

Save Search
Privacy Policy|Terms of Use
Close
With a personal account, you can:
  • Track your credits
  • Personalize content alerts
  • Customize your interests
  • Fully personalize your learning experience
jn-learning_Modal_SaveSearch_NoAccess_Purchase
Close

Lookup An Activity

or

Close

My Saved Searches

You currently have no searches saved.

Close
With a personal account, you can:
  • Access free activities and track your credits
  • Personalize content alerts
  • Customize your interests
  • Fully personalize your learning experience
Education Center Collection Sign In Modal Right
Close
Our website uses cookies to enhance your experience. By continuing to use our site, or clicking "Continue," you are agreeing to our Cookie Policy | Continue