Cardiac Magnetic Resonance Characterization of Myocarditis-Like Acute Cardiac Syndrome in COVID-19.

Novel coronavirus infection causes a systemic disease (coronavirus disease-2019 [COVID-19]) with, most frequently, respiratory involvement. In addition to systemic and respiratory complications, COVID-19 can reveal itself as a myocarditis-like syndrome (AMCovS), whose underlying mechanism is largely unknown. A limited number of case reports have described cardiac magnetic resonance (CMR) findings in AMCovS; only 2 of which included mapping (1,2).

This paper reports the first series of patients with AMCovS (n = 10; 8 females and 2 males; 52 ± 6 years of age) consecutively referred for CMR for suspected myocarditis between March 15 and April 20, 2020, in 4 Italian university hospitals. Local ethical committees approved or waived specific study approval, and the study was conducted according to tenets of the Declaration of Helsinki. Eight of 10 patients (80%) experienced oppressive chest pain. The remaining 2 patients had dyspnea. All patients had unremarkable cardiological history and a low rate of cardiovascular risk factors (median 0 [interquartile range (IQR): 0 to 1]). High-sensitivity troponin (hsTn) concentrations were elevated (median hsTn T in 4 patients was 120 ng/l [IQR: 103 to 157 ng/l]; normal value <14 ng/l; median hsTn I value in 6 patients was 1,626 ng/l [IQR: 1,340 to 2,538 ng/l]; normal value <40 ng/l). Electrocardiography alterations were observed in 8 of 10 patients, with ST-segment elevation in 6 of 10, ST depression in 1 of 10, and T-wave inversions in 1 of 10.

Obstructive coronary artery disease was excluded with invasive coronary angiography in the 8 patients with electrocardiography abnormalities. Furthermore, obstructive coronary artery disease was excluded with coronary computed tomography angiography in 1 patient with reduced ejection at echocardiography in the absence of electrocardiography alterations. Coronary artery disease was not investigated in 1 patient because there were no electrocardiographic and echocardiographic alterations.

All patients underwent CMR (1.5-T in 9 patients and 3-T in 1 patient) within 1 week from troponin rise and onset of cardiac symptoms (median of 3 days [IQR: 2 to 4 days]). CMR protocol included multiplanar cine imaging, short-tau inversion recovery (STIR), and late gadolinium enhanced (LGE) imaging. Native T1 and T2 mapping were available in 8 of 10 patients.

Cine images revealed normal left ventricle end-diastolic volume in all patients (median 67 ml/m2 [IQR: 60 to 76 ml/m2]; normal value <90 ml/m2). Two patients, both females, 58 and 61 years of age, had severe depression of systolic function (ejection fraction <40%) with apical ballooning, apical edema, and absent LGE, suggesting Takotsubo cardiomyopathy. Both of these patients experienced a complete left ventricular function recovery in a few days.

The remaining 8 patients (6 females and 2 males; 50 ± 14 years of age) had no segmental wall motion abnormalities. Five patients had preserved ejection fraction (>55%), and 3 patients had mildly reduced ejection fraction (40% to 55%). In all cases, CMR showed diffuse intense myocardial edema, with increased myocardial-to-skeletal muscle intensity ratio on STIR images (median T2-ratio: 2.3 [IQR: 2.2 to 2.4]; normal value <1.9), increased native-T1 mapping (at 1.5-T: median 1,156 ms [IQR: 1,123 to 1,198 ms]; normal value <1,045 ms; at 3-T: 1,378 ms; normal value <1,240 ms) and increased T2 mapping (median 62 ms [IQR: 59 to 67 ms]; normal value <50 ms). (Figure 1 ). Extracellular volume fraction was only available for 2 of 10 cases. In both cases, the extracellular volume fraction was elevated (30% and 36%, respectively) as was native T1 and T2. Two patients had borderline wall thickening (wall thickness of 13 mm in both cases) in regions of intense edema and mild dysfunction.

Figure 1

CMR Findings In SARS-Cov-2+ Patients With a Myocarditis-Like Syndrome, With Acute Myocardial Injury in the Absence of Obstructive Coronary Artery Disease

CMR = cardiac magnetic resonance; COVID-19 = coronavirus disease-2019; IQR = interquartile range; LGE = late gadolinium enhancement; SARS-Cov-2 = severe acute respiratory syndrome-coronavirus-2; SSFP = steady state free precession; STIR = short tau inversion recovery; T2-ratio = myocardial/skeletal muscle intensity ratio; Tn = troponin.

Mild pericardial effusion was present in 6 of 8 patients (75%) (median: 5 mm [IQR: 3 to 11 mm]) without evidence of pericardial thickening (≤3 mm).

Surprisingly, LGE images were unremarkable (median 0% [IQR: 0% to 2%]). LGE images were completely negative in 5 of 8 patients. In the remaining 3 patients, a few thin and shadowed subepicardial striae of LGE were detectable in the lateral wall, accounting for 1%, 3%, and 3% of LV mass respectively (Figure 1).

Based on updated 2018 Lake Louise criteria, CMR findings, including T1 and T2 myocardial markers, resulted in diagnoses of acute myocarditis in all 8 patients.

All patients were discharged at the time of writing, with regression of cardiac injury markers and left ventricular functional recovery. Nevertheless, no prognoses could be inferred because of the limited population size.

The absence or very minimal amount of LGE observed in these patients with AMCovS agrees with the few histological results published to date, reporting limited or absent myocyte necrosis (1,3), and may suggest an indirect mechanism causing myocardial inflammation. Endomyocardial biopsy was not performed in the present patients, in consideration of clinical stability and rapid functional recovery.

This series suggests inflammation as a possible substrate underlying myocardial injury in COVID-19 patients. Diffuse edema can be the only CMR hallmark of myocardial inflammation in COVID-19, because LGE may be completely absent or minimal, revealing unremarkable myocyte necrosis.