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Observational Study
. 2020 Nov 1;5(11):1265-1273.
doi: 10.1001/jamacardio.2020.3557.

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

Valentina O Puntmann  1 , M Ludovica Carerj  1   2 , Imke Wieters  3 , Masia Fahim  3 , Christophe Arendt  1   4 , Jedrzej Hoffmann  1   5 , Anastasia Shchendrygina  1   6 , Felicitas Escher  7 , Mariuca Vasa-Nicotera  5 , Andreas M Zeiher  5 , Maria Vehreschild  3 , Eike Nagel  1
Affiliations
Observational Study

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

Valentina O Puntmann et al. JAMA Cardiol. .

Erratum in

  • Errors in Statistical Numbers and Data.
    [No authors listed] [No authors listed] JAMA Cardiol. 2020 Nov 1;5(11):1308. doi: 10.1001/jamacardio.2020.4648. JAMA Cardiol. 2020. PMID: 32840563 Free PMC article. No abstract available.

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.

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Conflict of interest statement

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.

Figures

Figure 1.
Figure 1.. Representative Histologic and Cardiac Magnetic Resonance Imaging Abnormalities in 2 Patients After Coronavirus Disease 2019 (COVID-19) Diagnosis
A and B, Histologic findings in an adult man with severe cardiac magnetic resonance imaging abnormalities 67 days after COVID-19 diagnosis. High-sensitivity troponin T level on the day of cardiac magnetic resonance imaging was 16.7 pg/mL. The patient recovered at home from COVID-19 illness with minimal symptoms, which included loss of smell and taste and only mildly increased temperature lasting 2 days. There were no known previous conditions or regular medication use. Histology revealed intracellular edema as enlarged cardiomyocytes with no evidence of interstitial or replacement fibrosis. Panels A and B show immunohistochemical staining, which revealed acute lymphocytic infiltration (lymphocyte function–associated antigen 1 and activated lymphocyte T antigen CD45R0) as well as activated intercellular adhesion molecule 1. C to F, Representative cardiac magnetic resonance images of an adult woman with COVID-19–related perimyocarditis. Panels C and D show significantly raised native T1 and native T2 in myocardial mapping acquisitions. Panels E and F show pericardial effusion and enhancement (yellow arrowheads) and epicardial and intramyocardial enhancement (white arrowheads) in late gadolinium enhancement (LGE) acquisition.
Figure 2.
Figure 2.. Scatterplots of Native T1, Native T2, and High-Sensitivity Troponin T Measures by Group
There was a small but significant difference between patients who recovered at home vs in the hospital for native T1 (median [interquartile range], 1119 [1092-1150] ms vs 1141 [1121-1175] ms; P = .008) and high-sensitivity troponin T (4.2 [3.0-5.9] pg/dL vs 6.3 [3.4-7.9] pg/dL; P = .002) but not for native T2 or N-terminal pro–b-type natriuretic peptide. For the coronavirus disease 2019 (COVID-19) home recovery group, dark circles indicate symptomatic illness and light circles indicate asymptomatic illness. Boxes indicate overlays of box-whisker plots, midlines indicate medians, and whiskers indicate the farthest data point not regarded as an outlier (ie, within 1.5-fold the interquartile range).
Figure 3.
Figure 3.. Correlation of Myocardial Measures With Time From Coronavirus Disease 2019 (COVID-19) Testing
There was no significant correlation with duration between the positive test for COVID-19 and the measures (native T1: r = 0.07; P = .47; native T2: r = 0.14; P = .15; high-sensitivity troponin T: r = −0.07; P = .50). The trend line indicates the linear regression trend, and the shaded area indicates 95% CIs of the mean.
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