Myocardial Strain for the Differentiation of Myocardial Involvement in the Post-Acute Sequelae of COVID-19-A Multiparametric Cardiac MRI Study

Abstract

Myocardial involvement was shown to be associated with an unfavorable prognosis in patients with COVID-19, which could lead to fatal outcomes as in myocardial injury-induced arrhythmias and sudden cardiac death. We hypothesized that magnetic resonance imaging (MRI) myocardial strain parameters are sensitive markers for identifying subclinical cardiac dysfunction associated with myocardial involvement in the post-acute sequelae of COVID-19 (PASC). This study evaluated 115 subjects, including 65 consecutive COVID-19 patients, using MRI for the assessment of either post-COVID-19 myocarditis or other cardiomyopathies. Subjects were categorized, based on the results of the MRI exams, as having either 'suspected' or 'excluded' myocarditis. A control group of 50 matched individuals was studied. Along with parameters of global cardiac function, the MRI images were analyzed for measurements of the myocardial T1, T2, extracellular volume (ECV), strain, and strain rate. Based on the MRI late gadolinium enhancement and T1/T2/ECV mappings, myocarditis was suspected in 7 out of 22 patients referred due to concern of myocarditis and in 9 out of 43 patients referred due to concern of cardiomyopathies. The myocardial global longitudinal, circumferential, and radial strains and strain rates in the suspected myocarditis group were significantly smaller than those in the excluded myocarditis group, which in turn were significantly smaller than those in the control group. The results showed significant correlations between the strain, strain rate, and global cardiac function parameters. In conclusion, this study emphasizes the value of multiparametric MRI for differentiating patients with myocardial involvement in the PASC based on changes in the myocardial contractility pattern and tissue structure.

Keywords: COVID-19; MRI; myocarditis; strain; strain rate.

Figure 1

Study groups. A total of 65 consecutive COVID-19 patients who underwent MRI post-COVID-19 were included in the study. The patients were referred due to concerns of myocarditis (Mycts; group 1, n = 22) or other cardiac concerns (group 2, N = 43). MRI evaluation categorized the patients as either suspected or excluded myocarditis, which resulted in two study groups: ‘suspected myocarditis’ in 16 patients and ‘excluded myocarditis’ in 49 patients. We also included a third study group of non-COVID-19 matched controls (N = 50).

Figure 2

Myocardial strain and strain rate in the different study groups. Representative global (A) longitudinal (GLS), circumferential (GCS), and radial (GRS) strain curves. and global (B) longitudinal (GLSR), circumferential (GCSR), and radial (GRSR) strain rate curves for subjects in the control, excluded myocarditis, and suspected myocarditis groups. The vertical white arrows represent the peak systolic strains and peak diastolic strain rates. The peak systolic strains and peak diastolic strain rates (in absolute value) in the suspected myocarditis group are smaller than those in the excluding myocarditis group, which in turn are smaller than those in the control group (note that the vertical scale is different for each panel).

Figure 3

Global strain and strain rate analysis. Distribution of global (A) longitudinal (GLS), (B) circumferential (GCS) and (C) radial (GRS) strain measurements, and global (D) longitudinal (GLSR), (E) circumferential (GCSR) and (F) radial (GRSR) strain rate measurements in the control (blue), excluded myocarditis (green), and suspected myocarditis (red) groups. Note that the GLS, GCS, and GRSR are represented in absolute values (original measurements are negative) for presentation clarity. The vertical black lines mark the mean ± one standard deviation. Statistically significant (p < 0.05) differences between the study groups are represented by asterisks. The number of asterisks in the figure represent the significance level (number of zeros after decimal point in p).

Figure 4

Myocardial parametric mapping. MRI-derived extracellular volume (ECV), T1, and T2 maps in subjects from the control, excluded myocarditis, and suspected myocarditis groups. All the parameters show larger values in the suspected myocarditis group compared to those in the excluded myocarditis group, which in turn are larger than those in the control group, reflecting increased diffuse fibrosis, inflammation, and edema.

Figure 5

Global ECV, T1, and T2 analysis. (A) Extracellular volume (ECV) measurements in the control (blue), excluded myocarditis (green), and suspected myocarditis (red) groups. (B,C) Distribution of the T1 measurements from the (B) 3T scans and (C) 1.5T scans in the control (blue), excluded myocarditis (green), and suspected myocarditis (red) groups. (D,E) Distribution of the T2 measurements from the (D) 3T scans and (E) 1.5T scans in the control (blue), excluded myocarditis (green), and suspected myocarditis (red) groups. The vertical black lines show the mean ± one standard deviation. Statistically significant (p < 0.05) differences between the study groups are represented by asterisks. The number of asterisks in the figure represent the significance level (number of zeros after decimal point in p).

Figure 6

Correlation heatmap for all the studied parameters. The color scale represents the correlation values between −1 (red) and 1 (blue), while white represents zero correlation. Moderate-to-high positive and negative correlations are typed in BOLD font inside boxes. Specifically, there existed significant moderate correlations between the strain vs. strain rate parameters, and between both the strain and strain rate parameters vs. LVEF and RVEF (positive correlations) and vs. LVEDV, LVESV and LV mass (negative correlations).

Figure 7

Linear regressions of the strain (GLS, GCS, GRS) vs. strain rate (GLSR, GCSR, GRSR) parameters. There exist significant moderate positive correlations between the strain and strain rate parameters in all directions, implying simultaneous deterioration in systolic and diastolic functions.

Figure 8

Linear regressions of the GLS, GCS, GRS strains vs. global cardiac function parameters. There exist significant moderate positive correlations between the strains/strain rates and LVEF, and significant moderate negative correlations between the strains/strain rates and LVEDV, LVESV, and LV mass, implying that deterioration in systolic function is accompanied by ventricular remodeling.

Figure 9

Linear regressions of the GLSR, GCSR, GRSR strain rates vs. global cardiac function parameters. There exist significant moderate positive correlations between the strains/strain rates and LVEF, and significant moderate negative correlations between the strains/strain rates and LVEDV, LVESV, and LV mass, implying that deterioration in systolic function is accompanied by ventricular remodeling.