Cardiac Involvement in Patients Recovered From COVID-2019 Identified Using Magnetic Resonance Imaging

Abstract

Objectives: This study evaluated cardiac involvement in patients recovered from coronavirus disease-2019 (COVID-19) using cardiac magnetic resonance (CMR).

Background: Myocardial injury caused by COVID-19 was previously reported in hospitalized patients. It is unknown if there is sustained cardiac involvement after patients' recovery from COVID-19.

Methods: Twenty-six patients recovered from COVID-19 who reported cardiac symptoms and underwent CMR examinations were retrospectively included. CMR protocols consisted of conventional sequences (cine, T2-weighted imaging, and late gadolinium enhancement [LGE]) and quantitative mapping sequences (T1, T2, and extracellular volume [ECV] mapping). Edema ratio and LGE were assessed in post-COVID-19 patients. Cardiac function, native T1/T2, and ECV were quantitatively evaluated and compared with controls.

Results: Fifteen patients (58%) had abnormal CMR findings on conventional CMR sequences: myocardial edema was found in 14 (54%) patients and LGE was found in 8 (31%) patients. Decreased right ventricle functional parameters including ejection fraction, cardiac index, and stroke volume/body surface area were found in patients with positive conventional CMR findings. Using quantitative mapping, global native T1, T2, and ECV were all found to be significantly elevated in patients with positive conventional CMR findings, compared with patients without positive findings and controls (median [interquartile range]: native T1 1,271 ms [1,243 to 1,298 ms] vs. 1,237 ms [1,216 to 1,262 ms] vs. 1,224 ms [1,217 to 1,245 ms]; mean ± SD: T2 42.7 ± 3.1 ms vs. 38.1 ms ± 2.4 vs. 39.1 ms ± 3.1; median [interquartile range]: 28.2% [24.8% to 36.2%] vs. 24.8% [23.1% to 25.4%] vs. 23.7% [22.2% to 25.2%]; p = 0.002; p < 0.001, and p = 0.002, respectively).

Conclusions: Cardiac involvement was found in a proportion of patients recovered from COVID-19. CMR manifestation included myocardial edema, fibrosis, and impaired right ventricle function. Attention should be paid to the possible myocardial involvement in patients recovered from COVID-19 with cardiac symptoms.

Keywords: ACE2, angiotensin-converting enzyme 2; AHA, American Heart Association; BSA, body surface area; CI, cardiac index; CMR, cardiac magnetic resonance; CO, cardiac output; COVID-19, coronavirus disease-2019; ECV, extracellular volume; EDV, end-diastolic volume; EF, ejection fraction; ER, edema ratio; ESV, end-systolic volume; FA, flip angle; FOV, field of view; IQR, interquartile range; LGE, late gadolinium enhancement; LV, left ventricle; LVEF, left ventricular ejection fraction; PSIR, phase-sensitive inversion-recovery; RT-PCR, reverse transcription and polymerase chain reaction; RV, right ventricle; RVEF, right ventricular ejection fraction; SARS-CoV-2, severe acute respiratory syndrome-coronavirus-2; SI, signal intensity; SSFP, steady state free precession; STIR, short tau inversion recovery; SV, stroke volume; T2WI, T2-weighted imaging; TE, echo time; TR, repetition time; cardiac involvement; cardiac magnetic resonance imaging; coronavirus disease-2019; hs-cTnI, high-sensitive cardiac troponin I.

Conflict of interest statement

This work was supported in part by the National Natural Science Foundation of China (81471637 and 81873889), the National Mega Project on Major Infectious Disease Prevention (2017ZX10103005-007), and the National Key Research and Development Program of China (2018YFE0204500). All authors have reported that they have no relationships relevant to the contents of this paper to disclose.

© 2020 by the American College of Cardiology Foundation. Published by Elsevier.

Figures

Graphical abstract

Central Illustration

Dominant Location and Distribution of Myocardial Edema Segments and Myocardial LGE Segments in Patients Recovered From COVID-19 (A) Number of myocardial edemas distributed in the AHA 16 segments’ model in all 15 patients with positive conventional CMR findings. (B) Number of myocardial LGEs distributed in the AHA 16 segments’ model in all 15 patients with positive conventional CMR findings. AHA = American Heart Association; COVID-19 = coronavirus disease-2019; CMR = cardiac magnetic resonance; LGE = late gadolinium enhancement; NA = not applicable.

Figure 1

Focal Myocardial Fibrosis in Patients Recovered From COVID-19 A 29-year-old male patient (first row) underwent cardiac CMR 1 month after the onset of palpitations. A 60-year-old male patient (second row) underwent cardiac CMR 2 months after the onset of palpitations. PSIR sequences in short-axis view (A, C) showed focal LGE (black arrows) in inferior and septal segments of left ventricle, respectively. Results were confirmed on the PSIR sequences in 2-chamber view (C) and 4-chamber view (D). Images A and D demonstrated a small pericardial effusion (white arrow) in both patients. COVID-19 = coronavirus disease-2019; CMR = cardiac magnetic resonance; LGE = late gadolinium enhancement; PSIR = phase-sensitive inversion recovery.

Figure 2

Cardiac Involvement in Patients Recovered From COVID-19 Identified Using Quantitative Cardiac CMR A 60-year-old male patient (first row) underwent cardiac CMR 2 months after the onset of palpitations. Short-axis STIR sequence (A) showed no evidence of myocardial edema. However, PSIR image (B) of the same slice showed focal LGE in the LV septal and inferior segments (black arrows). Increased native T1 (1,434 ± 43 ms), ECV (30 ± 2%), and normal T2 values (38 ± 2 ms) were shown in the corresponding location of focal LGE on the T1 (C), T2 (D), and ECV maps (E) (black arrows). A 29-year-old female patient (second row) underwent cardiac CMR 1 and a half months after the onset of palpitations. Short-axis STIR (F) and PSIR sequence (G) showed global myocardial signal hyperintensity but no apparent LGE, global T1, and ECV values were significantly increased on the T1 (H) and ECV maps (J). T2-mapping sequence (I) showed increased T2 values at inferior septal (41 ± 8 ms), anterior (41 ± 6 ms), and inferior lateral segments (43 ± 5 ms), which matched the location with significantly increased signal intensity on short-axis STIR sequence (F) (white arrows). ECV = extracellular volume; LV = left ventricle; STIR = short tau inversion recovery; other abbreviations as in Figure 1.