Cardiac MRI in Suspected Acute COVID-19 Myocarditis.

Keywords: COVID-19; coronavirus; myocarditis; cardiac MRI; T1 mapping; T2 mapping.

Acute changes in myocardial tissue characteristics during hospitalization in patients with COVID-19.

Background: Patients with a history of COVID-19 infection are reported to have cardiac abnormalities on cardiovascular magnetic resonance (CMR) during convalescence. However, it is unclear whether these abnormalities were present during the acute COVID-19 illness and how they may evolve over time. Methods: We prospectively recruited unvaccinated patients hospitalized with acute COVID-19 (n = 23), and compared them with matched outpatient controls without COVID-19 (n = 19) between May 2020 and May 2021. Only those without a past history of cardiac disease were recruited. We performed in-hospital CMR at a median of 3 days (IQR 1-7 days) after admission, and assessed cardiac function, edema and necrosis/fibrosis, using left and right ventricular ejection fraction (LVEF, RVEF), T1-mapping, T2 signal intensity ratio (T2SI), late gadolinium enhancement (LGE) and extracellular volume (ECV). Acute COVID-19 patients were invited for follow-up CMR and blood tests at 6 months. Results: The two cohorts were well matched in baseline clinical characteristics. Both had normal LVEF (62 ± 7 vs. 65 ± 6%), RVEF (60 ± 6 vs. 58 ± 6%), ECV (31 ± 3 vs. 31 ± 4%), and similar frequency of LGE abnormalities (16 vs. 14%; all p > 0.05). However, measures of acute myocardial edema (T1 and T2SI) were significantly higher in patients with acute COVID-19 when compared to controls (T1 = 1,217 ± 41 ms vs. 1,183 ± 22 ms; p = 0.002; T2SI = 1.48 ± 0.36 vs. 1.13 ± 0.09; p < 0.001). All COVID-19 patients who returned for follow up (n = 12) at 6 months had normal biventricular function, T1 and T2SI. Conclusion: Unvaccinated patients hospitalized for acute COVID-19 demonstrated CMR imaging evidence of acute myocardial edema, which normalized at 6 months, while biventricular function and scar burden were similar when compared to controls. Acute COVID-19 appears to induce acute myocardial edema in some patients, which resolves in convalescence, without significant impact on biventricular structure and function in the acute and short-term. Further studies with larger numbers are needed to confirm these findings.

Ventricular function and tissue characterization by cardiac magnetic resonance imaging following hospitalization for multisystem inflammatory syndrome in children: a prospective study.

BACKGROUND: Multisystem inflammatory syndrome in children (MIS-C) is a severe life-threatening manifestation of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection that often presents with acute cardiac dysfunction and cardiogenic shock. While recovery from acute illness is excellent, the long-term myocardial impact is unknown. OBJECTIVE: To compare cardiac MRI findings in children 6-9 months after their hospitalization with MIS-C against MRI findings in healthy controls to assess for residual myocardial disease. MATERIALS AND METHODS: We prospectively performed cardiac MRI on 13 children 6-9 months following their hospitalization with MIS-C: eight of these children had a history of left ventricle ejection fraction (LVEF) < 50%, persistent symptoms, or electrocardiogram (ECG) abnormalities and underwent clinical MRI; five of these children without cardiac abnormalities during their hospitalization underwent research MRIs. We compared their native T1 and T2 mapping values with those of 20 normal controls. RESULTS: Cardiac MRI was performed at 13.6 years of age (interquartile range [IQR] 11.9-16.4 years) and 8.2 months (IQR 6.8-9.6 months) following hospitalization. Twelve children displayed normal ejection fraction: left ventricle (LV) 57.2%, IQR 56.1-58.4; right ventricle (RV) 53.1%, IQR 52.0-55.7. One had low-normal LVEF (52%). They had normal extracellular volume (ECV) and normal T2 and native T1 times compared to controls. There was no qualitative evidence of edema. One child had late gadolinium enhancement (LGE) with normal ejection fraction, no edema, and normal T1 and T2 times. When stratifying children who had MIS-C according to history of LVEF <55% on echocardiography, there was no difference in MRI values. CONCLUSION: Although many children with MIS-C present acutely with cardiac dysfunction, residual myocardial damage 6-9 months afterward appears minimal. Long-term implications warrant further study.

Myocardial Tissue Characterization in Cardiac Magnetic Resonance Studies of Patients Recovering From COVID-19: A Meta-Analysis.

Background Meta-analysis can identify biological factors that moderate cardiac magnetic resonance myocardial tissue markers such as native T1 (longitudinal magnetization relaxation time constant) and T2 (transverse magnetization relaxation time constant) in cohorts recovering from COVID-19 infection. Methods and Results Cardiac magnetic resonance studies of patients with COVID-19 using myocardial T1, T2 mapping, extracellular volume, and late gadolinium enhancement were identified by database searches. Pooled effect sizes and interstudy heterogeneity (I2) were estimated with random effects models. Moderators of interstudy heterogeneity were analyzed by meta-regression of the percent difference of native T1 and T2 between COVID-19 and control groups (%ΔT1 [percent difference of the study-level means of myocardial T1 in patients with COVID-19 and controls] and %ΔT2 [percent difference of the study-level means of myocardial T2 in patients with COVID-19 and controls]), extracellular volume, and the proportion of late gadolinium enhancement. Interstudy heterogeneities of %ΔT1 (I2=76%) and %ΔT2 (I2=88%) were significantly lower than for native T1 and T2, respectively, independent of field strength, with pooled effect sizes of %ΔT1=1.24% (95% CI, 0.54%-1.9%) and %ΔT2=3.77% (95% CI, 1.79%-5.79%). %ΔT1 was lower for studies in children (median age: 12.7 years) and athletes (median age: 21 years), compared with older adults (median age: 48 years). Duration of recovery from COVID-19, cardiac troponins, C-reactive protein, and age were significant moderators for %ΔT1 and/or %ΔT2. Extracellular volume, adjusted by age, was moderated by recovery duration. Age, diabetes, and hypertension were significant moderators of the proportion of late gadolinium enhancement in adults. Conclusions T1 and T2 are dynamic markers of cardiac involvement in COVID-19 that reflect the regression of cardiomyocyte injury and myocardial inflammation during recovery. Late gadolinium enhancement and to a lesser extent extracellular volume, are more static biomarkers moderated by preexisting risk factors linked to adverse myocardial tissue remodeling.

Characterization of COVID-19-Related Lung Involvement in Patients Undergoing Magnetic Resonance T1 and T2 Mapping Imaging: A Pilot Study.

Tissue characterization by mapping techniques is a recent magnetic resonance imaging (MRI) tool that could aid the tissue characterization of lung parenchyma in coronavirus disease-2019 (COVID-19). The aim of the present study was to compare lung MRI findings, including T1 and T2 mapping, in a group of n = 11 patients with COVID-19 pneumonia who underwent a scheduled cardiac MRI, and a cohort of healthy controls. MRI scout images were used to identify affected and remote lung regions within the patients' cohort and appropriate regions of interest (ROIs) were drawn accordingly. Both lung native T1 and T2 values were significantly higher in the affected areas of patients with COVID-19 as compared to the controls (1375 ms vs. 1201 ms, p = 0.016 and 70 ms vs. 30 ms, p < 0.001, respectively), whereas no significant differences were detected between the remote lung parenchyma of the COVID-19 patients and the controls (both p > 0.05). When a larger ROI was identified, comprising the whole lung parenchyma within the image irrespective of the affected and remote areas, the COVID-19 patients still retained higher native T1 (1278 ms vs. 1149 ms, p = 0.003) and T2 values (38 ms vs. 34 ms, p = 0.04). According to the receiver operator characteristics curves, the T2 value of the affected region retained the higher accuracy for the differentiation of the COVID-19 patients against the controls (area under the curve 0.934, 95% confidence interval 0.826−0.999). These findings, possibly driven by the ability of MRI tissue mapping to detect ongoing inflammation in the lungs of patients with COVID-19, suggest that T1 and T2 mapping of the lung is a feasible approach in this clinical scenario.

Case Report: Transient Increase of CMR T1 Mapping Indices in a Patient With COVID-19 mRNA Vaccine Induced Acute Myocarditis.

Background: Acute myocarditis is commonly associated with viral infections, including severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2). Myocarditis following mRNA COVID-19 vaccination has also been reported, however this is rare and usually resolves within days or weeks. We present a case of acute myocarditis reported after vaccination with mRNA-1273 COVID-19 vaccine (Moderna) diagnosed using cardiac magnetic resonance imaging (CMR). This report describes the utility of CMR in the diagnosis and follow-up of such patients using parameters which could suggest the clinical course of myocarditis. Case Summary: A 23-year-old male presented in the emergency department with complaints of chest pain radiating to the left arm following vaccination with the second dose of COVID-19 mRNA-1273 vaccine (Moderna). Patient's history revealed an incidence of myocarditis in the past. CMR showed a mid-range left ventricular ejection fraction (38%) and subepicardial late gadolinium enhancement (LGE) in the inferolateral and apical myocardial segments with diffuse elevation of native T1 mapping relaxation times in all myocardial segments. The patient was admitted briefly in the intensive care unit and after a favorable clinical course was discharged from the hospital in stable condition. A follow-up CMR after 3 months revealed normalization of LVEF (57%) and native T1- times in most segments. Scarred myocardium reflecting chronic myocarditis continued to show elevated T1 times. Conclusions: Our patient presenting with acute myocarditis after recent COVID-19 mRNA vaccination reported a favorable clinical course. CMR revealed increased T1 mapping relaxation times diffusely spread across the myocardium and an impairment of the left ventricular function (LVEF) during the acute phase. However, the LVEF as well as the T1 times normalized at follow-up in all segments except for myocardium affected by chronic myocarditis.

Serial Cardiovascular Magnetic Resonance Studies Prior to and After mRNA-Based COVID-19 Booster Vaccination to Assess Booster-Associated Cardiac Effects.

Background: mRNA-based COVID-19 vaccination is associated with rare but sometimes serious cases of acute peri-/myocarditis. It is still not well known whether a 3rd booster-vaccination is also associated with functional and/or structural changes regarding cardiac status. The aim of this study was to assess the possible occurrence of peri-/myocarditis in healthy volunteers and to analyze subclinical changes in functional and/or structural cardiac parameters following a mRNA-based booster-vaccination. Methods and Results: Healthy volunteers aged 18-50 years (n = 41; m = 23, f = 18) were enrolled for a CMR-based serial screening before and after 3rd booster-vaccination at a single center in Germany. Each study visit comprised a multi-parametric CMR scan, blood analyses with cardiac markers, markers of inflammation and SARS-CoV-2-IgG antibody titers, resting ECGs and a questionnaire regarding clinical symptoms. CMR examinations were performed before (median 3 days) and after (median 6 days) 3rd booster-vaccination. There was no significant change in cardiac parameters, CRP or D-dimer after vaccination, but a significant rise in the SARS-CoV-2-IgG titer (p < 0.001), with a significantly higher increase in females compared to males (p = 0.044). No changes regarding CMR parameters including global native T1- and T2-mapping values of the myocardium were observed. A single case of a vaccination-associated mild pericardial inflammation was detected by T2-weighted CMR images. Conclusion: There were no functional or structural changes in the myocardium after booster-vaccination in our cohort of 41 healthy subjects. However, subclinical pericarditis was observed in one case and could only be depicted by multiparametric CMR.

Heart and Lung Fibrosis in a Patient with COVID-19-Related Myocarditis.

A COVID-19 patient, in whom pneumonia lesions were first detected by chest computed tomography, was further evaluated by cardiac magnetic resonance (CMR) due to a suspected myocarditis. Beyond heart alterations, CMR revealed peculiar features of affected pulmonary areas in T1 mapping sequences and showed a particular distribution of late gadolinium enhancement in the same regions. The noninvasive assessment of the cellular, fluid, or fibrotic content of lung lesions may provide key information about the underlying pathophysiological pathways in the search of a tailored medical therapy and ventilatory support for COVID-19 patients.

Cardiac involvement in patients recovering from Delta Variant of COVID-19: a prospective multi-parametric MRI study.

AIMS: The cardiac injury and sequelae of Delta Variant of coronavirus disease 2019 (COVID-19) remain unknown. This study aimed to evaluate the presence of cardiac involvement in patients recovering from Delta Variant of COVID-19 based on multi-parametric cardiac magnetic resonance imaging (MRI). METHODS AND RESULTS: We prospectively assessed patients recovering from Delta Variant of COVID-19 using multi-parametric cardiac magnetic resonance imaging (MRI) between June 2021 and July 2021. Comparison was made with 25 healthy controls. Forty-four patients (median age 51 years, 28 women) recovering from Delta Variant were recruited and had a median time of 35 days between diagnosis and cardiac MRI. There were no patients with chest pain (0/44, 0%) and high sensitivity cardiac troponin T troponin elevation (median levels 2.20 pg/mL, IQR levels 0.85-4.40 pg/mL). Regarding the cardiac imaging findings, a total of 14 (32%) patients presented cardiac tissue feature abnormalities, and a total of 9 (20%) patients had a myocarditis-like injury based on cardiac MRI 2018 Lake Louise criteria. When we further assessed the T1 and T2 mapping values for of patients' individual, abnormal raised global native T1, T2, and extracellular volume were seen in 6 (14%), 6 (14%), and 4 (9%) patients, respectively. Comparing with controls, the patients had lower LV global longitudinal strain and (-22.2 ± 2.8% vs. -24.6 ± 2.0%, P < 0.001) and global circumferential strain (-20.7 ± 6.8% vs. -24.3 ± 2.9%, P = 0.014), but higher global native T1 (1318.8 ± 55.5 ms vs. 1282.9 ± 38.1 ms, P = 0.006). Four (9%) patients presented myocardial late gadolinium enhancement with subepicardial pattern mostly common seen, and two (5%) patients presented pericardial enhancement. CONCLUSIONS: The cardiac MRI could detect subclinical functional and myocardial tissue characteristic abnormalities in individuals who were recovering from Delta Variant without cardiac-related clinical findings. The native T1 mapping and strain imaging may be a sensitive tool for the noninvasive detection of a subset of patients who are at risk for cardiac sequelae and more prone to myocardial damage in survivors with Delta Variant.

Assessment of dynamic hepatic and renal imaging changes in COVID-19 survivors using T1 mapping and IVIM-DWI.

PURPOSE: To explore the imaging changes of the liver and kidneys in COVID-19 survivors using variable flip angle (VFA) T1 mapping and intravoxel incoherent motion-diffusion weighted imaging (IVIM-DWI). METHODS: This prospective study included 37 discharged COVID-19 participants and 24 age-matched non-COVID-19 volunteers who underwent abdominal MRI with VFA T1 mapping and IVIM-DWI sequencing as a COVID-19 group and control group, respectively. Among those discharged COVID-19 participants, 23 patients underwent two follow-up MRI scans, and were enrolled as the 3-month follow-up group and 1-year follow-up group, respectively. The demographics, clinical characteristics, and laboratory tests were collected. Imaging parameters of the liver and kidneys were measured. All collected values were compared among different groups. RESULTS: The 3-month follow-up group had the lowest hepatic T1 value, which was significantly lower than the value in the control group (P < 0.001). Additionally, the 3-month follow-up group had the highest hepatic ADC and D values, cortical ADC and f values, which were significantly higher than those in the control group (for all, P < 0.05). The hepatic D value in the 1-year follow-up group decreased significantly in comparison with that in the 3-month follow-up group (P = 0.001). Compared to non-severe patients, severe cases had significantly higher hepatic D* and f*D* values (P = 0.031, P = 0.015, respectively). CONCLUSION: The dynamic alterations of hepatic and renal imaging parameters detected with T1 mapping and IVIM-DWI suggested that COVID-19 survivors might develop mild, non-symptomatic liver and kidney impairments, of which liver impairment could probably relieve over time and kidney impairment might be long-existing.

Reference Values of Native T1 at 3T Cardiac Magnetic Resonance-Standardization Considerations between Different Vendors.

This study aimed at establishing native T1 reference values for a Canon Vantage Galan 3T system and comparing them with previously published values from different vendors. A total of 20 healthy volunteers (55% Women; 33.9 ± 11.1 years) underwent left ventricular T1 mapping at 3T MR. A MOLLI 5(3)3 sequence was used, acquiring three short-axis slices. Native T1 values are shown as means (±standard deviation) and Student's independent samples t-test was used to test gender differences in T1 values. Pearson's correlation coefficient analysis was used to compare two processes of T1 analysis. The results show a global native T1 mean value of 1124.9 ± 55.2 ms (exponential analysis), that of women being statistically higher than men (1163 ± 30.5 vs. 1077.9 ± 39.5 ms, respectively; p < 0.001). There were no specific tendencies for T1 times in different ventricular slices. We found a strong correlation (0.977, p < 0.001) with T1 times derived from parametric maps (1136.4 ± 60.2 ms). Native T1 reference values for a Canon 3T scanner were provided, and they are on par with those already reported from other vendors for a similar sequence. We also found a correlation between native T1 and gender, with higher values for women.

[IRM et myocardite infectieuse]. / IRM et myocardite infectieuse.

Over the past ten years, cardiac MRI has become an indispensable tool for acute myocarditis diagnosis. Under appropriate conditions, cardiac MRI may allow postponement of initial coronary angiography in many instances. The 2020 ESC guidelines give a class I recommendation to its use in the setting of MINOCA for differential diagnosis between acute myocardial infarction, myocarditis, Tako-Tsubo and other cardiac pathologies, in order to improve therapeutic management and follow-up. This article describes the technical characteristics of MRI in myocarditis (Lake Louise diagnostic criteria and criteria based on myocardial tissue mapping), the main differential diagnoses, the prognostic value and addresses the issue of myocarditis in the setting of COVID-19.