Role of Cardiovascular Magnetic Resonance
Imaging in Early Detection of Myocarditis
in Patients Recovered from COVID-19
Hany Hassan Ahmed Ebaid1, khaled Y Elnady2, Ahmed Abdel Moniem1, Mohamed Ibrahim Awadeen1* and Mohamed Mahrous Ali1
1Department of Cardiology, Faculty of Medicine, Benha University, Benha, Egypt
2Department Cardiology, Military Medical Academy, Cairo, Egypt
Submission: September 11, 2023;Published: September 20, 2023
*Corresponding author: Mohamed Ibrahim Awadeen, Faculty of Medicine, Benha University, Benha, Benha, Al-qalyubia governorate, Egypt
How to cite this article:Hany Hassan A E, khaled Y E, Ahmed A M, Mohamed I A, Mohamed M A. Lipoprotein-A vs. Role of Cardiovascular Magnetic Resonance Imaging in Early Detection of Myocarditis in Patients Recovered from COVID-19. J Cardiol & Cardiovasc Ther. 2023; 18(5): 555997. DOI: 10.19080/JOCCT.2023.18.555997
Objective: To assess cardiac involvement in patients recovered from COVID-19 with no clinical evidence of myocarditis, using various non-invasive parameters including Transthoracic Two-dimensional Speckle Tracking Echocardiography (STE) and cardiac magnetic resonance imaging (CMR). Methods: This prospective study was conducted in the Cardiology Departments of Maadi Military Hospital and Benha University Hospitals. A total of 74 patients were initially enrolled during their hospital stay, but only 50 of them met the inclusion and exclusion criteria. The CMR examination was performed in conjunction with echocardiography, ECG, and laboratory investigations on the same day, which occurred 2-12 weeks after recovering from confirmed COVID-19 infection. Patient scheduling for CMR and other examinations depended on the availability of the CMR machine. Results: According to CMR diagnosis, 23 (46%) patients were diagnosed to have myocarditis by CMR, the patients were categorized into two groups based on these results: normal group (27 patients) & myocarditis group (23 patients). According to GLS, 21 (42%) patients were diagnosed to have myocarditis by STE (diagnosis of Myocarditis with Global longitudinal strain was considered with cut-off point of >-21.33 with Sensitivity of 91.30% and Specificity of 92.59% (P <0.0001). 2D STE showed 87.50% sensitivity, 92.31% specificity and 90.00% accuracy to diagnose myocarditis, while CMR showed a 95.83% sensitivity, 96.15% specificity of and 96.00% accuracy. Conclusion: Myocarditis was found in 46% of asymptomatic COVID-19-recovered patients. CMR is a valuable tool for early myocarditis detection when combined with 2D STE, offering high accuracy. Significant differences were observed between suspected myocarditis patients and those with normal results on both 2D STE and CMR.
COVID-19 is a contagious illness caused by the SARS-CoV-2 virus, which was initially identified in Wuhan, China, in December 2019 and subsequently spread worldwide .
The COVID-19 pandemic has had far-reaching effects on global health, society, and economies . The primary target of COVID-19 is the lungs, as the SARS-CoV-2 virus invades pulmonary tissue through the angiotensin-converting enzyme 2 (ACE2) receptor .
ACE2 is not limited to the pulmonary system but is also found in various other organs, including the cardiovascular system . There is evidence linking COVID-19 to various cardiovascular complications, such as arrhythmias, myocarditis, acute coronary syndrome, acute onset heart failure, and cardiac arrest. Additionally, a strong association has been observed between acute cardiac injury and increased mortality rates among COVID-19 patients .
Previous research has indicated that a significant proportion of COVID-19 patients, ranging from 12% to 15%, exhibit elevated levels of high-sensitive cardiac troponin I (hs-cTnI) during their hospitalization, indicating myocardial injury. Furthermore, severe cases of COVID-19 may have cardiac involvement in as many as 31% of patients, but it remains uncertain how long this cardiac involvement persists after recovery [5,6].
SARS-CoV-2 has the potential to induce the release
of chemokines and cytokines, which can lead to vascular
inflammation, destabilization of atherosclerotic plaques, and
myocardial inflammation. Consequently, elevated troponin levels
in these patients could be attributed to stress cardiomyopathy,
microvascular thrombosis, demand ischemia, and the secondary
effects of systemic inflammation. Another possible cause
of myocardial damage associated with COVID-19 is direct
viral infection of the myocardium, potentially indicating viral
myocarditis. While myocarditis-like clinical presentations have
been reported in a small number of COVID- 19 patients, suggesting
that fulminant myocarditis is uncommon .
Cardiovascular magnetic resonance (CMR) has emerged
as the preferred non-invasive imaging technique for assessing
heart volume, function, and myocardial tissue characteristics
in cardiovascular medicine. Abnormalities in cardiac magnetic
resonance (CMR) related to COVID-19 have been identified in
78% of predominantly ambulatory adults .
The main aim of our investigation was to evaluate the degree
of cardiac engagement in individuals who have recuperated from
COVID-19. We achieved this by employing cardiac CMR as a highly
sensitive imaging method and comparing it to Transthoracic
Echocardiography with 2D STE.
This prospective study was done in cardiology department
of Maadi Military hospital & Benha University hospitals over 74
patients who were enrolled for this study during their hospital stay.
Only 50 patients were fulfilling the inclusion and exclusion criteria
and were enrolled in the study after 2-12 weeks after discharge
from hospital with diagnosis of (SARS-CoV-2) by PCR on swab test
of the upper respiratory tract.
The Banha Faculty of Medicine Human Research Ethics
Committee approved the study protocol, and informed consent
were obtained from Benha University prior starting data
collection. This study was conducted over a 1-year duration,
spanning from January 2021 to January 2022.
Patients who previously confirmed with SARS-CoV-2 infection
using (RT-PCR) swab test (who needs hospital admission due to
significant lung affection or decreased oxygen saturation > 90%)
and considered recovered by the discharging criteria ( resolved
respiratory symptoms, normal temperature lasting longer than
3 days, 2 consecutive negative RT-PCR test results separated by
at least 24 h and substantially improved exudative lesions on
chest CT images) and were isolated for two weeks and have no
any cardiac symptoms. All patients agreed to participate and sign
Exclusion criteria were active Covid-19 infection. Previous
myocardial infarction or coronary artery disease (evidence of
coronary artery stenosis > 50%) , history of ischemic heart disease,
previous myocarditis or heart failure, or known cardiomyopathy,
uncontrolled hypertension, extremely irregular heart rates or
previous atrial fibrillation, moderate to severe valvular heart
disease, inability to effectively take part in breath-holding
procedures and is thus unsuitable for undergoing CMR assessment,
intra-cardiac devices non-MRI compatible (ICDs– Pacemakers),
significant renal impairment ((CrCl rate < 30 mL/min/1.73 m2),
contraindications to gadolinium contrast, disagree to participate
or sign informed consent and insufficient CMR image quality for
All cases underwent a full history taking, complete
physical examination, 12 leads Electrocardiogram, laboratory
investigations (Creatinine, Troponin I & CBC), trans-Thoracic
Echocardiography which was done for all patients according to
EACVI Echocardiography guidelines  (Conventional study & 2D
Speckle tracking), and CMR.
Protocol for CMR scanning included the following
conventional sequences: long-axis and short-axis cine,
late gadolinium enhancement (LGE) and T2- weighted imaging
Quantitative mapping sequences: post-contrast T1 mapping
and native T1/T2 mapping.
The diagnosis of myocarditis was confirmed by Updated Lake
Louis criteria (2018) for diagnosis of Myocarditis which consist of
two main criteria (T1-based criterion and T2-based criterion). The
T1-based criteria is regarded as positive when there are increases
in native T1 relaxation durations, increases in extracellular volume
(ECV), or the presence of positive LGE.
The T2-based criterion is positive when there is an increase
in T2 relaxation times, regionally high T2 signal intensities on T2-
weighted images, or an elevation in the global T2-signal intensity
Supportive Criteria: pericardial effusion, pericardial signal
abnormality, systolic LV dysfunction. All CMR images were
evaluated by consultant cardiologist with 6 years of CMR diagnosis
Using PASS software, the minimum sample size required for
specificity and sensitivity tests was calculated (PASS 11 citation:
Hintze J (2011). PASS 11. NCSS, LLC. Kaysville, Utah, USA). The
required sample size for the study is determined to be 50 patients
without accounting for dropout rate.
We conducted the statistical analyses using SPSS software
(Statistical Package for the Social Sciences, version 24, SSPS
Inc, Chicago, IL, USA). Categorical variables were presented
in frequency tables with corresponding percentages, whereas
descriptive statistics like standard deviation and mean were used
to describe numerical data. Data entry, processing, and statistical
analysis were performed using MedCalc ver. 20 (MedCalc, Ostend,
Belgium). We employed various tests of significance, including
logistic multiple regression analysis and ROC Curve analysis. The
choice of analysis method was based on the nature of the data,
whether it was parametric or non-parametric. We considered
p-values less than 0.05 (5%) to be indicative of statistical
Table 1 shows demographic data, risk factors and vital signs in
all studied group. Table 2 shows ECG data, lab investigations, 2D
speckle tracking Echocardiographic parameters and diagnosed
myocarditis by CMR in all studied group.
BMI: body mass index, HTN: hypertension, DM: diabetes mellitus, HR: heart rate, SBP: systolic blood pressure, DBP: diastolic blood pressure,
MAP: Mean Arterial pressure.
EF: Ejection Fraction, LVESD: Left Ventricular End-Systolic Dimension, LVEDD: Left Ventricular End-Diastolic Dimension, LAD: Left Atrial
Dimension, TAPSE: Tricuspid Annular Plane Systolic Excursion.
According to CMR diagnosis, 23 (46%) patient was diagnosed
to have Myocarditis by CMR using Updated Lake Louis criteria
(2018) and patients were categorized into two groups based on
these observations: normal group (27) patients & myocarditis
group (23) patients.
There was no statistically significant difference between both
groups regarding age, sex, BMI, SBP and MAP. While the HR, DBP &
TLC were higher in myocarditis group than in normal group with
statistically significant difference (P=0.008, p=0.006 & p= 0.001
respectively). The lymphocytic count was lower in myocarditis
group with statistically significant difference (p<0.001). Table
3 A statistically significant difference was seen between the two
groups regarding ECG data and Troponin I during hospital stay
with higher incidence of abnormal ECG & elevated Troponin I in
myocarditis group than the other group. (P<0.0001). Time interval
per weeks was about 4.5 weeks between hospital discharge & CMR
& Echocardiographic examination with no significant difference
between both groups. Table 4 Average left ventricular (LV) systolic
function in myocarditis group was significantly lower than the
normal group (P <0.001). Differences between the two groups
were statistically significant concerning the LVESV (P = 0.012) & the
LVEDV (P = 0.002). The average right ventricular ejection fraction
(RVEF) was no significant difference between both groups. Global
native T1, T2 values showed significant elevation in myocarditis
group compared with the normal group (P. <0.001). Global Native
T2 was significant high in the myocarditis group than in the
normal group (P.<0.001). Pericardial enhancement and pericardial
effusion were found in 14 patients (60.8%) of myocarditis group
and was absent in normal group (P. <0.001). According to 2D
STE parameters, there was a statistically significant difference
between both groups regarding EF (P<0.0001), LVESD (P=0.014)
TAPSE (P=0.028) and LAD (P <0.0001).
*: significant P value, BMI: Body Mass Index, DM: Diabetes Mellitus, HTN: Hypertension, HR: Heart Rate, SBP: Systolic Blood Pressure, DBP:
Diastolic Blood Pressure, MAP: Mean Arterial Pressure.
Global longitudinal strain was significantly lower in
myocarditis group (-16.34% vs -23.07%). Also, base longitudinal
strain, mid longitudinal strain and apical longitudinal strain were
lower in myocarditis group (P<0.0001) (Table 5).
2D speckle tracking Echo parameters were used for diagnosis
of myocarditis with global longitudinal strain cut-off point of
>-21.33 with Sensitivity of 91.30% and Specificity of 92.59%
(P <0.0001). 2D STE showed a Sensitivity of 87.50%, Specificity
of 92.31% and Accuracy 90.00% for detection of myocarditis,
while CMR showed a Sensitivity of 95.83%, Specificity of 96.15%
and Accuracy 96.00%. Figure 1 Logistic regression analysis was
conducted for the prediction of myocarditis in the studied patients.
Global longitudinal strain, LVEF, LVESV, LVEDV, NativeT1, NativeT2,
DBP, HR, TLC, Lymphocyte, troponin I, ECG abnormality, EF, LVESD
& TAPSE were associated with the risk of myocarditis in univariate
analysis. Only global longitudinal strain was associated with risk
of myocarditis in both univariate and multivariate analysis Table 6.
*: significant as P-value.
*: significant as P-value, LVEF: Left Ventricular Ejection Fraction, RVEF: Right Ventricular Ejection Fraction, LVESV: Left Ventricular End-Systolic
Volume, LVEDV: Left Ventricular End-Diastolic Volume, LGE: Late Gadolinium Enhancement, SIR: Signal Intensity Ratio.
Myocarditis is a condition that results from inflammation
of the heart muscle, usually caused by a viral infection or an
autoimmune disease. With the outbreak of COVID-19, reports
of myocarditis cases in patients who have recovered from the
virus have emerged. Given the severity of the pandemic, the early
detection and treatment of myocarditis are crucial to prevent longterm
cardiac damage and potential complications.
The mean age in our study group was 35.5 ± 8.24 years, this
was concordant with Huang et al. , who studied 26 patients
who recovered from covid-19 and stated that patients with a
mean age of 38. In contrast Wang et al. , who investigated
cardiac consequences of COVID-19 in 47 recovered patients using
CMR, reported higher mean age as they stated that mean age of
their patients was 47.6 ± 13.3 years, In our study 41(82%) were
males which was consistent with Ulloa et al.  Who studied 57
recovered patients searching for myocardial affection in recovered
patients from covid-19 with male predominance with 80% of
study group were males. In contrast, Huang et al.  showed
female predominance as only 38% of study group were males.
In our study, 28 (56%) of all studied group were smokers, 13
(26%) patients had DM and 19 (38%) had hypertension. This was
comparable with Wang et al.  Who reported that 18% of their
patients had DM and 25% of them had hypertension. In contrast
Huang et al.  in which only 8% of patients were hypertensive
and none had DM..
According to CMR parameters, 23 (46%) patients were
diagnosed to have myocarditis by CMR, and patients were
categorized into two groups based on these results: normal group
(27 patients) & myocarditis group (23 patients).
There was no statistically significant difference between both
groups regarding age, sex, BMI, SBP and MAP. Differences between
the two groups were statistically significant regarding DBP, HR,
TLC and lymphocytic count. In contrast, Huang et al.  reported
that there was no statistically significant difference between
patients with normal and abnormal CMR finding regarding age,
sex, SBP, DBP, HR, TLC and lymphocytic count.
Our study showed statistically significant difference between
both groups regarding level of Tn I as we found 11 (47%) patients
with elevated Tn I in myocarditis group versus only 1 (3.7%)
patient in the normal group. This was in line with Wojtowicz et
al.  who reported statistically significant difference between
the two groups of patients with and without non- ischemic
cardiac injury using CMR regarding Tn I level. In the current
study, there was a statistically significant difference between
both groups regarding ECG abnormality as we found 12 (52%)
patients with ECG abnormality in myocarditis group versus only
1 (3.7%) patient in the normal group. This was supported by a
study by Ulloa et al.  which was conducted in Spain and studied
myocardial affection in post covid-19 patient over 57 patients
and showed statistically significant ECG abnormality which was
found in 24 post covid patients (42%) inform of RBBB (15.8%),
Atrial fibrillation (5.3%), Ventricular extrasystole (1.8%), Negative
precordial T wave (12.3%) and Pathological Q wave (7%).
In our study, Echocardiographic examination showed
statistically significant difference between both groups regarding
EF, LVESD, TAPSE and LAD. In comparison, Özer et al.  who
studied 74 patients with previous Covid-19 infection after 1 month
from recovery reported also statistically significant difference
between patients with elevated troponin group and the other
group without elevated troponin regarding LAD, LVEF but no
statistically significant difference between both groups regarding
LVESD & LVEDD.
Our study found 21 (42%) recovered Covid-19 patients of all
studied group had reduced GLS. This was in line with Mahajan et
al.  who found reduced GLS in 40 (29.9%) recovered Covid-19
patients of his study group.
In our study, Global longitudinal strain was significantly
lower in myocarditis group. Also, Base longitudinal strain, mid
longitudinal strain and apical longitudinal strain. In line with
our study, Mahajan et al.  showed statistically significant
difference between reduced LV GLS group and Normal LV GLS
group regarding LV GLS.
In contrast, Özer et al.  reported no statistically significant
difference between group with myocardial injury and the other
group without myocardial injury regarding LV GLS (-17.7 ± 2.6 Vs
-18.9 ± 1.8, P=0.051). In our study we found 23 out of 50 (46%)
patients had abnormal CMR parameters including myocardial
oedema and LGE and diagnosed as myocarditis by updated Lake
Louise criteria with mean time between hospital discharge and
CMR examination of 34 days. This was in line with Huang et al. 
who found median (IQR) time between COVID-19 diagnosis and
CMR was 47 (36-58) days, and 15 of 26 patients (58%) reported
abnormal CMR results on conventional CMR sequences.
In our study, myocarditis group were significantly different
from healthy one in CMR examination regarding LVEF, LVESV, and
LVEDV. But no statistically significant difference regarding RVEF.
It was in concordance with Wojtowicz et al.  who reported
statistically significant difference between the two groups of
patients with and without Non-Ischemic Cardiac Injury regarding
LVEF (57% vs 61%, P<.001), but no statistically significant
difference regarding LVEDV and RVEF.
Our study showed increased myocardial oedema parameters
with statistically significant difference between myocarditis and
normal groups in form of increased T2 signal intensity ratio
(T2 SIR), increased T2 relaxation time and increased native T1
respectively. In concordance to our study, Huang et al.  revealed
that global native T1, T2, and ECV values were significantly greater
in recovered COVID-19 patients with positive conventional CMR
findings than in patients without positive findings (native T1
1,271 ms versus 1,237 ms, P=0.002), (T2 42.7± 3.1 ms vs 38.1±
2.4 ms, P=0.005), (ECV 28.2% vs 24.8%, P=0.001).
Also, Kunal et al.  reported significantly elevated native T1
(1301ms Vs 1264 ms, P =0.022) and native T2 (55.62 vs 45.25 ms,
P =0.004) in post Covid-19 patients with abnormal CMR group
compared to the other one with normal CMR.
In our study, non-ischemic pattern of LGE was found in 23
patients (46%) mainly sub- epicardial and mid wall enhancement
affecting the apical and mid cardiac muscle segments with P value
<0.001, denoting presence of myocardial fibrosis and/or necrosis.
Wang et al.  reported non-ischemic sub-epicardial and mid
wall LGE in 13 of 44 (30%) of the post-COVID- 19 patients’ group
(a finding similar to our cohort results). Then they performed a
strain study revealing that patients with LGE exhibited poorer LV
and RV Performance.
In our study, Pericardial involvement in form of pericardial
effusion and pericardial LGE which develops as a consequence of
myocardial damage, was also found in 14 patients (28%) of all
studied patients and was found in 60% of myocarditis group. In
concordance, Huang et al.  reported that 7 (28%) of 26 patients
were positive for pericardial LGE and have a minor pericardial
Regarding the validity of 2D speckle tracking Echocardiography
(STE) and CMR in final diagnosis of myocarditis, In previous study
by Luetkens et al.  found that the diagnosis of myocarditis
using Updated Lake Louise Criteria yielded a sensitivity of 87.5%
and a specificity of 96.2%.
In our study, speckle tracking echocardiography showed
a sensitivity of 87.5% and specificity of 92.3 %. A study by
Sharifkazemi et al.  compared the diagnostic performance of
CMR and 2D STE in 57 patients with suspected acute myocarditis.
They found that CMR had a higher sensitivity (96.8%) and
specificity (93.5%) compared to 2D speckle tracking Echo (78.4%
and 77.4%, respectively) in the diagnosis of acute myocarditis.
In our study logistic regression analysis showed that only
global longitudinal strain was associated with risk of myocarditis
in both univariate and multivariate analysis.
Finally, this study had some limitations, as study did not include
long-term follow-up to assess the outcomes of patients with
myocarditis. Also, the study did not provide detailed information
on the severity of COVID-19 in the patients, which may have
influenced the development of myocarditis.
Evidence of myocarditis in asymptomatic patient recovered
from COVID-19 was present in 46% of patients. Non-invasive
predictors of myocarditis are Global longitudinal strain, LVEF,
LVESV, LVEDV, NativeT1, NativeT2, DBP, HR, TLC, Lymphocyte, TnI,
ECG abnormality, EF, LVESD and TAPSE while Global longitudinal
strain was the only independent predictor. According to this
research’s findings, it can be concluded that CMR is a valuable tool
in the early detection of myocarditis in those who have achieved
recovery from COVID-19. The use of CMR in combination with 2D
STE has shown a notable level of accuracy in the detection and
assessment of myocarditis. The findings of this study showed
that there were significant differences between patients with
suspected myocarditis and those with normal results on both
2D STE and CMR. The results also showed that CMR had higher
sensitivity, specificity, and accuracy compared to 2D STE in the
diagnosis of myocarditis. Further studies with larger sample
sizes and multi-center cooperation are needed to validate the
diagnostic accuracy of CMR and 2D STE in the early detection of
myocarditis in patients recovered from COVID- 19.