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Cardiac Magnetic Resonance Imaging in Coronavirus
Disease 2019 (COVID-19)
A Systematic Review of Cardiac Magnetic Resonance
Imaging Findings in 199 Patients
Vineeta Ojha, MD,* Mansi Verma, MD,* Niraj N. Pandey, DM,*
Avinash Mani, MD,†Amarinder S. Malhi, DM,* Sanjeev Kumar, MD,*
Priya Jagia, MD,* Ambuj Roy, DM,‡and Sanjiv Sharma, MD*
Objective: Cardiac magnetic resonance imaging (CMR) with its new
quantitative mapping techniques has proved to be an essential
diagnostic tool for detecting myocardial injury associated with
coronavirus disease 2019 (COVID-19) infection. This systematic
review sought to assess the important imaging features on CMR in
patients diagnosed with COVID-19.
Materials and Methods: We performed a systematic literature review
within the PubMed, Embase, Google Scholar, and WHO databases
for articles describing the CMR findings in COVID-19 patients.
Results: A total of 34 studies comprising 199 patients were included
in the final qualitative synthesis. Of the CMRs 21% were normal.
Myocarditis (40.2%) was the most prevalent diagnosis. T1 (109/150;
73%) and T2 (91/144; 63%) mapping abnormalities, edema on T2/
STIR (46/90; 51%), and late gadolinium enhancement (LGE)
(85/199; 43%) were the most common imaging findings. Perfusion
deficits (18/21; 85%) and extracellular volume mapping abnormalities
(21/40; 52%), pericardial effusion (43/175; 24%), and pericardial LGE
(22/100; 22%) were also seen. LGE was most commonly seen in the
subepicardial location (81%) and in the basal-mid part of the left
ventricle in inferior segments. In most of the patients, ventricular
functions were normal. Kawasaki-like involvement with myocardial
edema without necrosis/LGE (4/6; 67%) was seen in children.
Conclusion: CMR is useful in assessing the prevalence, mechanism,
and extent of myocardial injury in COVID-19 patients. Myocarditis
is the most common imaging diagnosis, with the common imaging
findings being mapping abnormalities and myocardial edema on T2,
followed by LGE. As cardiovascular involvement is associated with
poor prognosis, its detection warrants prompt attention and
appropriate treatment.
Key Words: cardiac magnetic resonance imaging, coronavirus disease
2019, systematic review
(J Thorac Imaging 2021;36:73–83)
KEY POINTS
(1) Myocarditis was the most prevalent diagnosis on cardiac
magnetic resonance imaging in patients with Coronavirus
disease 2019 (COVID-19).
(2) Mapping abnormalities were the most common imaging
findings, followed by edema and late gadolinium
enhancement (LGE). Subepicardial LGE in the basal to
mid left ventricle was the most prevalent pattern of LGE.
(3) Ventricular functions were normal in most of the patients.
INTRODUCTION
The rapid emergence of COVID-19 caused by novel
coronavirus (SARS-Cov-2) has led to an unprecedented
global health crisis.1Although the clinical course is pri-
marily characterized by respiratory symptoms, cardiac
involvement in COVID-19 has been documented and is seen
to cause substantial morbidity and mortality. Adverse out-
comes have been reported especially in patients with
preexisting cardiovascular disease. COVID-19 has been
implicated in a wide gamut of cardiac manifestations including
heart failure, cardiogenic shock, arrhythmias, myocardial
inflammation, and coronary involvement, among others.2
The putative mechanisms for myocardial injury in
COVID-19 include exaggerated immune response or direct
viral damage. It has been hypothesized that SARS-CoV-2
binds to angiotensin-converting enzyme-2 (ACE-2) recep-
tors on cardiac myocytes followed by its incorporation and
replication resulting in direct damage to the cardiac tissue.3
Other possible mechanisms include activation of inter-
leukins and interferons especially interleukin-6 and the
subsequent cytokine storm, microcirculatory endothelial
dysfunction due to systemic inflammatory response and
hypoxic injury.4A hypercoagulable state created by this
virus can also cause thrombosis of coronary arteries leading
to ischemia.2
Cardiac complications can be diagnosed by a variety of
modalities available. Cardiac magnetic resonance (CMR)
imaging has the unique ability of providing morphologic
and functional information and tissue characterization and
is recommended by the American Heart Association to
detect myocardial insult.5It is imperative for the health care
workers to be aware of the spectrum of CMR findings in
COVID-19 to provide timely diagnosis and prompt insti-
tution of appropriate treatment. Our knowledge pertaining
to cardiac complications is still evolving and the literature
From the Departments of *Cardiovascular Radiology & Endovascular
Interventions; ‡Cardiology, All India Institute of Medical Sciences,
New Delhi; and †Department of Cardiology, Sri Chitra Tirunal
Institute for Medical Sciences and Technology, Trivandrum, Kerala,
India.
The authors declare no conflicts of interest.
Correspondence to: Sanjiv Sharma, MD, Department of Cardiovascular
Radiology & Endovascular Interventions, All India Institute of Medical
Sciences, New Delhi 110029, India (e-mail: meetisv@yahoo.com).
Supplemental Digital Content is available for this article. Direct URL
citations appear in the printed text and are provided in the HTML
and PDF versions of this article on the journal’s website, www.
thoracicimaging.com.
Copyright © 2020 Wolters Kluwer Health, Inc. All rights reserved.
DOI: 10.1097/RTI.0000000000000574
ORIGINAL ARTICLE
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regarding cardiac manifestations of this disease entity is
sparse and scattered with lack of a cohesive compilation. To
our knowledge, this is the first systematic review to compile
the data in the current published literature regarding cardiac
involvement in COVID-19 as depicted on CMR.
MATERIALS AND METHODS
Search Strategy
We sought to conduct a narrative synthesis of the reported
CMR findings in patients with COVID-19 (synthesis without
meta-analysis [SWiM]). We developed our search strategy
according to the PRISMA (Preferred Reporting Items for
Systematic Reviews and Meta-Analysis) guidelines.6The study
protocol was registered in PROSPERO (CRD42020199104).
Comprehensive electronic search of the PubMed, Embase,
Google Scholar, and World Health Organization Library
databases was performed on August 4, 2020 using the search
terms: (“covid”or “covid-19”or “coronavirus”or “SARS-
CoV-2”or “2019-nCoV”or “n-CoV”)AND(“MRI”OR
“MR”OR “CMR”OR “Magnetic Resonance”). The search
was limited to articles published in the year 2020. Additional
search of the gray literature and the reference lists of the
extracted studies selected was done to extract other relevant
studies. Duplicates were excluded.
Study Selection
The published articles (including case reports or series)
describing CMR findings in patients with confirmed COVID-19
infection were included in the review. Additional inclusion cri-
teria were articles conducted on human beings, published in
English and with extractable full text. No restrictions were
applied based on the country of research. Reviews, preprints,
editorials, guidelines, and recommendations were excluded.
Two independent reviewers screened the titles and abstracts of
the included articles according to the criteria mentioned above.
Any disagreements were solved mutually and by the senior
author, if required.
Quality of Study Assessment
Two independent reviewers rated all the included
studies for their quality based on the National Institutes of
Health (NIH) Quality Assessment Tool for Case Series
Studies.7The included studies had a small sample size due to
rarity of reported cases. The methodological quality of the
studies was generally rated as fair indicative of the limited
and low-quality data available pertaining to CMR findings.
Data Extraction
We retrieved the full texts of the articles included for the
final review and further screened them for their eligibility. After
careful scrutiny, articles included for the systematic review and
final analysis were shortlisted. Two independent reviewers
extracted the relevant data from the full texts of the included
articles into a Microsoft Excel database using the following
fields: author, study design, journal, country, demographics,
sample size, clinical features, CMR imaging features, and
follow-up. To extract the granular data, various subfields were
also used such as biomarker elevation, distribution of lesions,
etc. Discrepancies were resolved by mutual discussion between
the 2 reviewers. Data was analyzed using Microsoft Excel.
CMR Data Analysis
Substantial heterogeneity existed within the data.
Many studies described findings according to the standard
magnetic resonance imaging (MRI) definitions for con-
ditions such as myocarditis (Lake Louise criteria 2009 in 4
studies and modified Lake Louise criteria 2018 in 6). For
those studies that did not give the definition, the analysis
was done in accordance with the Lake Louise criteria
2018.8,9 For most of the studies, edema was defined to be
present when the ratio of myocardium: skeletal muscle sig-
nal intensity was >2.10 Myocarditis-like LGE was defined
as the one not corresponding to any vascular territory and
sparing the subendocardium.11
RESULTS
Characteristics of Included Studies
After removing the duplicate studies, a total of 289
unique records were identified from the 4 databases (Fig. 1).
After initial screening, a total of 63 records met the criteria
for a full text review. Out of these, 34 studies were finally
included for analysis after careful scrutiny. Table 1 describes
the demographic information pertaining to the study pop-
ulation. In 34 included studies, a total of 221 patients
underwent 224 MRI scans (including 3 follow-ups). How-
ever, the second largest study in this systematic review
described in detail the findings on CMR in only 29 patients
(with unknown etiology) out of a total of 51 patients.11 So,
we excluded the remaining 22 patients from the final analysis,
giving a total of 199 patients. Most of the studies were case
reports except for 5 retrospective and 1 prospective obser-
vational studies. CMR findings were reported in all these
studies. The findings were reported from many countries
across the globe; however, Germany, England, and China
constituted maximum proportion of the sample size. Meth-
odologic quality of the studies was evaluated using the NIH
Quality Assessment Tool for Case Series and was fair for all
the included studies (Supplementary Table 1, Supplemental
Digital Content 1, http://links.lww.com/JTI/A182). The
diagnosis of COVID-19 was confirmed by real-time reverse
transcriptase polymerase chain reaction (RT-PCR) in all the
patients included in this systematic review, except 5 (in 2
studies) who were positive on serology.10,19 Most of the
patients had recovered from COVID-19, rather than har-
boring active disease. All the studies reported raised troponin
levels. Thirteen studies comprising 80 patients described
raised NT-proBNP levels (Table 2).
Common Imaging Findings on CMR
Various CMR imaging findings have been described
across the included studies as described in Table 2. Table 3
provides the pooled incidence of various imaging findings. The
mean duration of CMR from symptom onset varied widely,
ranging from day 2 to day 71. Myocarditis (80/199; 40.2%) was
the most prevalent diagnosis, whereas normal CMR was seen in
21.1% (42/199) of the patients. Uncommon CMR diagnoses
included inducible ischemia in 2.5% (5/199), acute dual ischemic
plus nonischemic pattern in 2% (4/199), Takotsubo syndrome,
and myopericarditis in 1.5% (3/199) of the patients, each.
ThemostprevalentMRIfindings (described out of >100
patients) included T1 mapping abnormalities (109/150; 72.7%),
T2 mapping abnormalities (91/144; 63.2%), and LGE (85/199;
42.7%). Other common findings (described out of <100
patients) included perfusion deficits (18/21; 85.71%), edema on
T2-weighted sequences (46/90; 51.11%), and extracellular vol-
ume mapping (ECV) abnormalities (21/40; 52.5%). Findings
on perfusion imaging were mentioned for a total of 21 patients
(Supplementary Table 2, Supplemental Digital Content 2,
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Copyright r2020 Wolters Kluwer Health, Inc. All rights reserved.
http://links.lww.com/PAS/B52). Knight et al11 described
ischemia in 9/19 and inducible ischemia in 8/19 patients. Per-
icardial effusion and pericardial LGE were also noted in 24%
and 22% of the patients, respectively. One patient was having
preexisting ventricular noncompaction (Table 3).28 Mean left
ventricular ejection fraction across the studies was 52% and
right ventricular ejection fraction was 56%. Right ventricle
(RV) dysfunction was described in 4 of 9 studies which men-
tioned RV function. Information regarding regional wall
motion abnormalities was provided in 13 case reports and
diffuse hypokinesia was the most common pattern (9/13;
69.2%) (Supplementary Table 2, Supplemental Digital Content
2, http://links.lww.com/PAS/B52).
Distribution of LGE and Mapping Abnormalities
LGE, when present, was most commonly seen involving
the basal (60%) and mid-ventricular (67%) part of the left
ventricle (LV) and involving the inferior, inferolateral, and
inferoseptal LV (26/41; 63.4%). A subepicardial nonischemic
pattern of LGE typical for myocarditis was the most prevalent
pattern (43/53; 81.1%). Mid-wall LGE was seen in 33.9%
(15/53) and ischemic pattern of LGE (subendocardial LGE
in coronary distribution) was seenin~17%(21/53).Diffuse
biventricular and transmural LGE were seen in one case each
(Supplementary Table 2, Supplemental Digital Content 2,
http://links.lww.com/PAS/B52).
Average T1 and T2 mapping values across all the
studies were 1165.59 and 54.65 ms. Very few studies described the
segments with mapping abnormalities. Whereas T1 mapping
values were variable, T2 mapping value was higher in lateral
segments (67 ms: lateral wall in 1 case and 69 ms: posterolateral
wall in 1 case). Average ECV values were also higher (34.24 ms)
in COVID-19 survivors (Supplementary Table 2, Supplemental
Digital Content 2, http://links.lww.com/PAS/B52).
Uncommon Imaging Findings on CMR
Some uncommon imaging findings were also described.
For example, LV hypertrophy (including pseudohypertrophy
due to inflammation) was described in 6 case reports (Table 3).
Two case reports mentioned the presence of apical left ven-
tricular thrombus including one in the presence of the Takot-
subo syndrome.19,34 Pericardial thickening was also found in
2cases.
41,42 Reduced global longitudinal strain, left atrial
enlargement, and diastolic dysfunction of the LV were described
in one case each.18,31,41 In addition, lymphadenopathy was
conspicuously absent in all the patients.
Imaging Findings in Children
A case series of four children admitted in the intensive
care described Kawasaki-like clinical features in these children.
Acute myocarditis occurred within a week of symptom onset.
CMR (3 in acute stage, 1 in recovery phase) demonstrated
FIGURE 1. PRISMA 2009 flowchart describing selection of studies included in the systematic review. (Adapted from Moher et al.6
Therefore, in order to reprint this adapted figure, authorization must be obtained both from the owner of the copyright in the original
work and from the owner of copyright in the translation or adaptation.)
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diffuse myocardial edema (on T2/STIR sequences and native
T1 mapping) without any LGE, suggesting myocardial
inflammation without necrosis/fibrosis (Fig. 2).10 However, 2
case reports in children also described the presence of sub-
epicardial LGE suggestive of typical myocarditis pattern along
with edema.35,42 In the report by Oberweis et al,42 the repeat
CMR showed complete resolution of inflammation and LGE
on immunomodulatory treatment.
Endomyocardial Biopsy (EMB) Findings
EMB data were available in 2 studies.12,27 Three patients
with severe disease were referred for EMB in the study by
Puntmann et al12 and all of them showed active lymphocytic
inflammation without any viral genome. In the case report of a
patient with Takotsubo-like syndrome, there was presence of
diffuse lymphocytic inflammatory infiltrates, interstitial edema,
and patchy necrosis without any replacement fibrosis. No viral
genome was found on molecular analysis.27
Findings on Follow-up CMR
Follow-up CMR findings were available for 3 patients
(in 3 different case reports). Whereas myocardial edema (T2
hyperintensity) resolved in all the 3 cases, 1 case with sub-
epicardial LGE remained constant, suggesting irreversible
fibrosis. Decrease in LV wall thickness and improvement in
left ventricular ejection fraction were also seen in 1 case
(Table 4).39,40,42
DISCUSSION
CMR may depict various imaging manifestations of
myocardial injury caused by COVID-19. In this systematic
review, we have compiled the data from the existing liter-
ature regarding the various common and uncommon
imaging findings in patients with COVID-19 on cardiac
MRI. Most of the studies in this review were of fair quality
suggesting risk of some bias. However, the scarcity of data
in the literature on this subject in this emergent pandemic
situation makes this bias unavoidable. Most of the data is
descriptive, nonblinded, and describes the preliminary
experience in this less well-known entity. However, we
aimed to evaluate the imaging findings on CMR and these
shortcomings were not strong enough to invalidate our
results.
Myocarditis was the most common imaging diagnosis
(~40%) on CMR in recovered/active patients with COVID-19.
More than three-fourth of the cases from the largest cohort till
date had findings of myocarditis on CMR, demonstrating that
TABLE 1. Overview of the Included Studies and the Demographic Profile of the Population
References Country of Study Study Design
Number of Patients With
CMR Findings Male
Age (y)
(Mean or Median)
Puntmann et al12 Germany Prospective observational 100 53/100 (53%) 49 (45-53)
Knight et al11 England Retrospective
observational, letter 29 24 /29 (83%) 64 ± 9
Blondiaux et al10 France Retrospective case series 4 1/4 (25%) 9 ± 3 (range 6-12)
Esposito et al13 Italy Case series 10 2/10 (20%) 52 ± 6
Huang et al14 China Retrospective observational 26 10/26 (38.5%) Median =38;
[IQR: 32-45]
Caballeros Lam et al15 Spain Scientific letter, case series 2 1/2 (50%) 26, 13
Coyle et al16 US Case report 1 1 57
Beşler et al17 Turkey Case report 1 1 20
Inciardi et al18 Italy Case report 1 0 53
Gravinay et al19 France Case report 1 1 51
Trogen et al20 US Case report 1 1 17
Luetkens et al21 Germany Case report 1 1 79
Manka et al22 Switzerland Case report 1 1 75
Pavon et al23 Switzerland Case report 1 1 64
Sardari et al24 Iran Case report 1 1 31
Gnecchi et al25 Italy Case report 1 1 16
Paul et al26 France Case report 1 1 35
Sala et al27 Italy Case report 1 0 43
Bonnet et al28 France Case report 1 1 27
Kim et al29 Korea Case report 1 0 21
Doyen et al30 France Case report 1 1 69
Warchołet al31 Poland Case report 1 1 74
Sassone et al32 Italy Case report 1 1 38
Salamanca et al33 Spain Case report 1 1 44
Bernardi et al34 Italy Case report 1 1 74
Fischer et al35 France Case report 1 1 15
Bernal-Torres et al36 Spain Case report 1 0 38
Weinsaft et al37 Case report 1 0 36
Madamanchi et al38 US Case report 1 1 41
Yuan et al39 China Case report 1 1 33
Garot et al40 France Case report 1 1 18
Monmeneu et al41 Spain Case report 1 1 43
Oberweis et al42 Luxembourg Case report 1 1 8
Frédéric et al43 France Case report 1 1 39
IQR indicates interquartile range.
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the prevalence of myocardial injury in COVID-19 is higher
than previously thought.12 The common imaging findings on
CMR included increased T1 and T2 mapping values and
edema on T2/STIR sequences. LGE was seen in less than half
of the patients. When present, LGE was most commonly seen
in the subepicardial location in inferior, inferoseptal, and
inferolateral segments, similar to viral myocarditis.9The
absence or small amounts of LGE observed in many cases is in
agreement with the limited number of histologic findings
published in the literature for this disease, reporting limited or
absent myocyte necrosis.12,27 EMB data in 2 of these studies
showed presence of lymphocytic infiltrates without evidence of
viral genome, again suggesting that immune-mediated myo-
cardial inflammation is the principal mechanism of cardiac
involvement in COVID-19.12,27 This inflammation (myocarditis)
is evident on CMR as raised T1 and T2 mapping values and
edema.8In most of the cases, the involvement was diffuse rather
than regional.
Mapping abnormalities were more common than T2
hyperintensity (edema) in our pooled analysis. The pro-
posed reason may be that tissue characterization using
only the signal intensities may not be possible or accurate
in cases of diffuse inflammation. Because of diffuse
increase in signal intensity and lack of reference “normal”
myocardium, discrete lesions may not be identified. Fur-
ther, even if diffusely inflamed myocardium shows raised
signal intensity ratio compared with the skeletal muscle,
the coexisting skeletal muscle edema may give rise to
false-negative results.8Mapping techniques can allow for
direct quantitative pixel by pixel measurement of myo-
cardial relaxation times in acute inflammation, thus
avoiding the limitations of semiquantitative techniques.
Inflamed myocardium shows raised T1, T2, and ECV
values. Previous studies have shown excellent diagnostic
accuracy of mapping techniques for suspected myocardi-
tis. Pooled area under the curve (AUC) for the detection
of acute myocarditis, from the available literature, are 89,
80, and 74 for T1, T2, and ECV mapping, respectively,
compared with 73, 73, and 83 for T2, early gadolinium
enhancement and LGE, respectively.8The MyoRacer
myocarditis trial also demonstrated native T1 mapping to
be most accurate (diagnostic accuracy: 81%) of all CMR
parameters for acute myocarditis.44
In the largest studies included in this review, ven-
tricular functions were predominantly normal. These
studies have demonstrated that tissue abnormalities pre-
cede functional abnormalities and that the patients could
be in relatively earlier phase of cardiac involvement.14
Indeed, our results showed that mapping abnormalities
were more prevalent than ventricular dysfunction. This
further strengthens the case for mapping techniques as a
sensitive tool for detecting early myocardial involvement
in COVID. However, it is important that patients are
further followed up longitudinally for possible adverse
functional remodeling of myocardium. RV dysfunction
was described in four studies (18/153 patients; 12%). The
proposed mechanism may relate to the fact that even
slight increase in pulmonary vascular resistance (due to
pulmonary disease) can cause impairment of RV function
as it acts as a passive conduit chamber.14
Ischemia was seen in 9 of 29 patients with identifiable
CMR findings of COVID-19 in the series by Knight and
colleagues, out of which 4 were concomitant with non-
ischemic pattern. There is an increasing evidence that there
is abnormal activation of the coagulation cascade and
microcirculatory dysfunction, which happens due to
heightened immune response and endothelial dysfunction in
COVID-19 and this can cause ischemia and acute coronary
syndrome.45 When present, it is associated with poor prog-
nosis. This mechanism is also postulated for the occurrence
of ventricular thrombus as a rare complication of COVID-
19 infection.19,34
Approximately one-fifth of the patients in this review
had normal CMR despite cardiac symptoms. This can have
two possible explanations. Considering the fact that normal
CMR was more commonly seen in case series with a higher
gap between symptoms and time of acquisition, the most
likely reason is that patients may have had myocarditis, but
were imaged later in the course of the disease when edema
had already resolved. Another reason could be that
TABLE 2. Pooled Incidence of Various Abnormalities on CMR in
COVID-19 Patients
Number of
Studies
Included
Pooled Incidence
(as Per Total Number
of MRI Performed)
CMR diagnosis
Myocarditis
(4 with Kawasaki like
manifestation, 1 with
reverse Takotsubo)
34 80/199 (40.2%)
Myopericarditis 34 3/199 (1.5%)
Takotsubo 34 3/199 (1.5%)
Ischemia 34 5/199 (2.5%)
Dual ischemic plus
nonischemic 34 4/199 (2.0%)
Normal CMR 34 42/199 (21.1%)
Mean ejection fractions on CMR
Mean LVEF* 24 51.6% (6609.7/128)
Mean RVEF 24 56.2% (6126.3/109)
Major abnormalities on cardiac MRI
Regional wall motion
abnormality (RWMA) 20 13/32 (40.6%)
Edema on T2 or STIR 28 46/90 (51.11%)
Perfusion deficit 3 18/21 (85.71%)
LGE 34 85/199 (42.7%)
T1 mapping abnormality 13 109/150 (72.7%)
T2 mapping abnormality 10 91/144 (63.2%)
ECV mapping
abnormality 6 21/40 (52.5%)
Pericardial effusion 11 43/175 (24.6%)
Pericardial LGE 1 22/100 (22%)
Left ventricle
hypertrophy†
66
Pericardial thickening 2 2
LV apical thrombus 2 2
Early gadolinium
enhancement
2 1/2
Other findings:
Diastolic dysfunction 1 1
Left atrial enlargement 1 1
LV wall thinning 1 1
Reduced global
longitudinal strain 11
*1 study did not mention exact LVEF but it was <40% in 2 patients,
>55% in 5 patients, 40-55% in 3 patients.13
†Cumulative percentages for some of the findings have not been calcu-
lated as they were mentioned in a very few studies/number of patients and are
not truly representative.
LVEF indicates left ventricular ejection fraction; RVEF, right ventricular
ejection fraction; STIR, short tau inversion recovery.
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TABLE 3. Pooled Incidence of Various Imaging Finding Across the Included Studies
References Troponin
N-terminal
Pro-B-type
Natriuretic
Peptide
CK-
MB CRP
Clinical
Presentation
CMR
Diagnosis
Normal
MRI
Gap
Between
Symptom
Onset and
CMR
LVEF
on MRI
RVEF
MRI
Puntmann
et al12 Raised in 76 Raised in 68 NA Raised Recoverd patients with
increased serological
markers chest pain (17)
palpitation (20) shortness of
breath (36)
Myocarditis (78) 22/100 71 d (from
positive
testing)
56% 56%
Knight et al11 Raised NA NA NA Discharged patients with
elevated troponin
NI: 11, I: 5, Dual:4,
No cause: 9 (13/
29 myocarditis,
9/29 ischemic,
7-ischemia; 1
prior MI)
9/29 (31%) 46 ± 15 d 67.7 ± 11.4% 63.7% ± 9.5%
Blondiaux
et al10 Raised in all NA NA NA MIS-C and Kawasaki like: pain
(4), vomiting (2), diarrhea
(2), and fever.
Myocarditis 0 3: acute, 1:
recovery
phase
68, 51, 52,
56
63, 53, 57, 55
Esposito et al13 Raised NA NA NA 8/10 (80%) experienced
oppressive chest pain. 2/10
(20%)had dyspnea
2:Takutsubo 8:
myocarditis like
0 1 wk 2: <40%,
5: >55%,
3: 40-
55%
NA
Huang et al14 At admission, 13/26
patients: median
[IQR] peak value of
2.2 [1.9-2.6] pg/mL;
normal at time of
CMR
NA NA NA Precordial chest pain 3/26
(12%), palpitation 23/26
(88%), and chest distress 6/
26 (23%); history of
hypertension before
COVID-19 2/26 (8%)
15/26 had
myocardial
edema and/or
LGE
11/26 (42%) 47 d (IQR: 36-
58)
60.7 (45% in
one)
36.5
Caballeros Lam
et al15 Raised, raised NA NA NA,
raised
Chest pain, mild cough and
fever (2 patient)
Myocarditis 0 7 d, NA 59%,
normal
function
in second
NA
Coyle et al16 Raised NA NA NA Shortness of breath, fever,
cough, myalgia
Myocarditis 0 25 d 82% NA
Beşler et al17 Raised Raised Raised Raised Fever, chest pain Myocarditis 0 14 d 64% NA
Inciardi et al18 Raised Raised Raised Raised Fatigue (fever and dry cough a
week before)
Acute
myopericarditis
with systolic
dysfunction
0 2 d 35% NA
Gravinay
et al19 Raised NA NA NA Fever, atypical chest pain Myocarditis 0 8 d Normal NA
Trogen et al20 Raised NA NA NA Fever Myocarditis 0 NA 40% 39%
Luetkens et al21 Raised Raised NA Raised Fatigue, SOB Myocarditis 0 10 d 49% Normal
Manka et al22 Raised Raised NA Raised Fever, dyspnea Diffuse myocardial
injury
0 6 d 59% 72%
Pavon et al23 Raised NA NA NA Chest pain, dyspnea Late acute
myocarditis
0 6 wk 42% NA
Sardari et al24 Normal at time of
CMR
NA NA NA Dyspnea, fever Myocarditis 0 3 wk 50% NA
Gnecchi et al25 Raised NA Raised Raised Chest pain, fever Myocarditis 0 11 d NA NA
Paul et al26 Raised NA NA NA Chest pain, fatigue Myocarditis 0 NA NA NA
Sala et al27 Raised Raised NA Raised Chest pain, dyspnea for 3d Acute virus-negative
lymphocytic
myocarditis
associated with
SARS-CoV-2
0 7 d 64% NA
Bonnet et al28 Raised Raised NA NA Respiratory distress Myocarditis with
underlying
isolated
ventricular
noncompaction
0 30 d NA NA
Kim et al29 Raised Raised NA NA Fever, dyspnea Myocarditis 0 NA NA NA
Doyen et al30 Raised NA NA NA Vomiting, diarrhea, fever,
dyspnea (history of
hypertension)
Myocarditis 0 NA NA NA
Warchołet al31 Raised NA Raised NA VT Myocarditis 0 NA 20% NA
Sassone et al32 Raised NA NA Raised Chest pain Acute myocarditsi 0 NA NA NA
Salamanca
et al33 Raised NA NA NA Dyspnea, syncope Myocarditis 0 14 d 75% NA
Bernardi et al34 Raised NA NA NA Chest pain, fever Takutsubo 0 NA 22% NA
Fischer et al35 Raised Raised NA Raised Chest pain, fever Acute myocarditsi 0 4 d 48% Normal
Bernal-Torres
et al36 Raised NA NA NA Papitations, no respiratory
symptoms
Myocarditis 0 18 d 60% NA
Weinsaft et al37 Raised NA NA NA Chest pain Myocarditis 0 NA 38% NA
Madamanchi
et al38 Raised NA NA NA Syncope Myocarditis 0 NA 33% NA
Yuan et al39 NA NA NA NA Chest pain, fever and muscle
ache
Myocarditis 0 5 d Decreased
slightly
NA
Garot et al40 Raised Raised NA Raised Cough, fever, fatigue, and
myalgias
Myocarditis 0 Day 7 and 14 33% NA
Monmeneu
et al41 tNt raised raised NA Raised Fever, dry cough, and
haemoptoic sputum
Subacute
myopericarditis
0 Day 15 53% NA
Oberweis et al42 Raised hs troponin T:
0.044 ng/mL
Raised 5112
pg/mL)
NA Raised Fever, cough, fatigue Myocarditis 0 Day 3 41% 46%
Frédéric et al43 Raised 15.4 μg/L Raised NA Raised Chest pain, dyspnea Myopericarditis 0 5 d NA NA
EGE indicates early gadolinium enhancement; GGO, ground-glass opacities; GLS, global longitudinal strain; LVEF, left ventricular ejection fraction; LVH,
left ventricle hypertrophy; N, normal; NA, data not available; RVEF, right ventricular ejection fraction; RWMA, regional wall motion abnormality; STIR, short
tau inversion recovery; Y, yes.
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TABLE 3. Pooled Incidence of Various Imaging Finding Across the Included Studies
RWMA
(Dyskinesia/
Hypokinesia)
LV Wall
Thickness
Edema on
T2 or
STIR
(Y/N)
Segments
T2
Adenosine
Stress
Perfusion
EGE
(Y/N) LGE
Pattern of
LGE
Segments
LGE
(Y/N)
NA NA NA NA NA NA Y Myocardial (32),
nonischemic
(20), ischemic
(12)
NA
NA NA N (51 ms in
myocarditis as
well as non
myocarditis)
Myocarditis like: 2
(1-2.5)
Done in 19 pts
Ischemia: 9
Inducible
ischemia: 8
NA NI: 11, I: 5, Dual:4,
No cause: 9,
Myocarditis like
LGE: 13 non
sp mid wall: 2
NA
No NA Y (3) N: (1) 3:
ratio >2. 2:
47.62 ms
NA NA N N N
No NA Y (8): ratio 2.3 2:apical 8:diffuse NA NA 7:N, 3: Y Thin
sunepicardial
striae
Lateral wall
NA NA Y (14) 54% 33% (137/416) LV the
majority of T2
signal
hyperintensity was
located in the
interventricular
septum, anterior,
anterior-lateral,
and inferior wall at
base and mid-
chamber
NA NA Y(8) 31% Focal linear
subepicardial
and patchy
mid-wall LGE
Most LGE (9/15)
[60%] lesions
were located
at inferior and
inferior-
lateral
segments at
base and mid-
LV
No NA NA NA NA NA Y, N Mesocardial and
subepicardial
Basal and mid-
inferoseptal
and inferior
myocardial
segments
NA NA Y Diffuse biventricular
and biatrial
NA NA Y Focal mid wall Basal
inferolateral
segments
NA NA Y Subepicardial mid
posterolateral LV
NA NA Y Subepicardial Mid PL
Diffuse biventricular
hypokinesis,
especially in the
apical segments
LVH Y Diffuse biventricular NA NA Y Diffuse
biventricular
NA
No NA Y Subepicardial lateral
and inferior LV
NA NA Y Subepicardial Inferior and
lateral LV
Yes (focal) NA Y Mid wall inferior RV-
LV junction
NA NA Y Mid wall Inferio r RV-LV
junction
Global hypokinesis NA Y T2 ratio 2.2 Di ffuse edema
(image: basal)
NA NA N N N
No NA Y Diffuse edema NA NA N N N
Mild hypokinesia NA NA NA NA NA Y Subepicardial Anterior IVS,
inferior and
inferolateral
wall base.
Mid cavity
apex
NA NA Y Mid inferoseptal and
inferior wall
NA NA Y Subepicardial Mid inferior wall
Hypokinesia of
inferior and
inferoseptal
segment (echo)
NA Y Patchy lateral wall NA NA Y Subepicardial Lateral wall
NA NA NA NA NA NA Y Subepicardial Lateral and
inferior wall
Mild hypokinesia at
basal and mid left
ventricular
segments
NA Y Diffuse basal and mid
level, IVS
NA NA N N N
NA NA NA NA NA NA Y Subepicardial Inferior wall mid
cavity (image)
NA LVH, LV mass
index: 111.3
g/m2
Y ratio 2.2 Diffuse lateral LV
wall
NA NA Y Extensive
transmural
Diffuse lateral LV
No (echo) LVH (echo)
(chronic htn)
NA NA NA NA Y Subepicardial Apex and
inferolateral
wall (mid
cavity in
figure)
Global LV
hypokinesia
NA N N NA NA Y Large, patchy,
and linear
localized
subepicar-
dially and
intramurally
Basal and mid-
cavity
segments of
the inferior
and
inferolateral
wall and in
the apical
segments of
the inferior
wall
NA NA Y Mid-basal LV lateral
wall
NA NA Y Subepicardial
(image)
Mid-basal LV
lateral wall
No NA Y Diffuse with less
involvement of
inferolateral wall
NA NA N N N
Hypokinesia of
medio-apical
segments of the left
ventricle with the
NA Y Mid-apical segments
of the left ventricle
NA NA N N N
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TABLE 3. Pooled Incidence of Various Imaging Finding Across the Included Studies
T1 Mapping
Abnormality
(Y/N)
T1
Mapping Value
(Segment)
T2 Mapping
Abnormality
(Y/N)
T2
Mapping Value
(Segment) ECV
Pericardial
Thickening/
Effusion
Other
Cardiac
Findings
Lung Findings
(Chest X-ray
and/or CT)
Y (73) 1130 ms Y(60) NA NA Effusion (20)
pericardial
LGE (22)
—NA
NA NA NA NA NA Effusion: 2/29 with
unknown
etiology (7%)
—Lung parenchymal
changes 20/29
(69%); pleural
effusion 4/29 (14%)
3:Y 3: >1100 ms 1: 1050ms NA NA NA Effusion: 3 —Peripheral opacities on
CT: 3, normal: 1
Y (8) 1.5T:1,156 ms, 3 T:1378ms Y (8) 62ms 2 patients: 30 and 36% Effusion: 6/8
(75%);
Thickening:
None
—NA
Y (15) 1271ms [IQR: 1243-1298] vs.
1237 ms [IQR: 1216-1262] in
patients with and without
positive MRI, respectively
Y (15) 42.7 [IQR: 3.1] vs. 38.1
[IQR: 2.4] in patients
with and without
positive MRI,
respectively
28.2% [IQR: 24.8-36.2] vs.
24.8% [IQR: 23.1-25.4] in
patients with and without
positive MRI, respectively
Effusion: 7 —NA
Y 1303, 1110 ms Y 53, 54 ms NA Effusion in second
patient
—NA
NA NA NA NA No effusion —Bilateral patchy
interstitial opacities
(CT and CXR)
NA NA NA NA NA NA —Subpleural
consolidation in left
upper lobe (CXR
and CT )
Y NA NA NA NA Effusion (12mm) Mild LV
diastolic
dysfunction
Normal
NA NA NA NA NA NA Apical LV
thrombus
CT normal
NA NA NA NA NA NA —Hazy GGOs at
bilateral lower
lobes (CXR)
Y 1035 Y 62 ms NA Effusion (10 mm) —GGOs in the left upper
lobe and pleural
and pericardial
effusions (CT)
Y 1090 Y 56 ms NA NA —NA
NA NA Y 55-57ms NA NA —GGOs in the right lung
NA NA NA NA NA NA —NA
NA NA NA NA NA NA —NA
NA NA NA NA NA NA —NA
Y 1188 ms Y 61 ms NA NA —Bilateral GGOs; no
pleural effusion
NA NA NA NA NA NA —Consolidation
Y Mid-septum, 1431 ms; lateral
wall, 1453 ms
NA NA NA NA —Bilateral multifocal
consolidation
NA NA NA NA NA NA —Bilateral GGOs and
condensations
NA NA NA NA NA NA Left atrial
enlargement
NA
NA NA NA NA NA NA —Bilateral GGOs,
consolidationS
(CT)
Y 1120 ms NA NA 36% NA —Bilateral pneumonia
(CXR)
NA NA Y NA NA NA Apical
thrombus
NA NA NA NA NA Effusion —Normal (CT)
NA NA NA NA NA NA —Alveolar opacities;
GGOs (CT)
NA NA NA NA NA NA —
NA NA Normal NA NA NA Ct: inferolateral
myocardial
wall
thinning,
consolidation
NA NA NA NA NA NA —Nodular calcification
in left upper lobe
and local
thickening of the
right pleura
Y Anteroseptal 1102 ms;
posterolateral 1209 ms
Y 57 ms in anteroseptal and
69 ms in posterolateral
33% in anteroseptal; 39% in
posterolateral
NA No perfusion
defect
Crazy paving
Y Average, 1110 ms; mid-septum,
1047 ms; lateral wall, 1204 ms
Y Average, 60 ms; mid-
septum, 53 ms; lateral
wall, 67 ms
Average, 33%; mid-septum,
29%; lateral wall, 39%
Pericardial edema
without
associated
effusion
GLS decreased Diffuse bilateral
opacities; right
pleural effusion
NA 1148 ± 67 ms NA NA NA Mild thickening of
pericardium
—Bilateral lower lobe
pneumonias;
bilateral pleural
effusions (CT)
NA NA NA NA NA Effusion —Pleural effusion,
atelectasis
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FIGURE 2. Cardiac MRI of 4 children with Kawasaki-like symptoms due to COVID-19 and with clinical diagnosis of acute myocarditis. The
top panel shows the cine images with minimal pericardial effusion. The second panel demonstrates edema in the form of increased
T2-STIR signal intensity ratio between the myocardium and the skeletal muscle ( >2:1) in patient 2, 3, and 4. The third panel
demonstrates abnormal native-T1 mapping ( >1100 ms) in patients 2, 3, and 4 and normal native T1 in patient 1. The bottom panel
demonstrates absence of late gadolinium enhancement in patients 2 and 3 (myocardial null times were recognized as too short in patient
4 but could not be repeated due to lack of further patient cooperation). (Reproduced with permission from Blondiaux et al.10)
TABLE 4. Follow Up MRI Findings in Cases Where Repeat MRI was Performed
References
Number of
Patients
Duration of Follow
Up MRI Follow Up MRI Findings
Yuan et al39 1 Day 12 T2WI hyperintensity resolved, indicating myocarditis
Garot et al40 1 Day 14 Significant reverse LV remodelling (wall thickness decreased to 11 mm from
14 mm), LV end diastolic index decreased to 88 mL/m
2
from 127 mL/m
2
and LVEF improved to 54% from 33%), decrease of focal myocardial
edema and EGE in the posterolateral wall, and stable LGE lesions in the
subepicardium of the posterolateral wall
Oberweis et al42 1 Day 7 Normal systolic function (initially 53%) and resolution of myocardial edema.
Native T1 mapping showed slightly decreased T1 values at 1048 ± 78 ms
(from initial 1110 ms)
EGE indicates early gadolinium enhancement; LGE, late gadolinium enhancement; LVEF, left ventricular ejection fraction.
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symptoms were because of residual pulmonary involvement
rather than the cardiac.12,14
The mean duration of CMR from symptom onset
ranged from day 2 to day 71. In 3 of the largest studies, the
mean duration was 71, 46, and 47 days, respectively, and
there were significant findings on CMR, denoting that car-
diac involvement in COVID-19 persists beyond the acute
stage and without any trend toward the decrease in these
imaging findings through the recovery period. This high-
lights the importance of clinical surveillance beyond the
initial phase in patients with COVID-19. Some additional
insight into the course of this disease was also provided by
the 3 cases in which follow-up MRI was done (Table 4).
Although, edema seemed to decrease in all the 3 cases, LGE
lesions did not resolve in 1 study (which described the fol-
low-up LGE findings) suggesting fibrosis. The reversibility
of myocardial dysfunction and inflammation puts forth the
Takotsubo syndrome as a reasonable differential diagnosis
in these cases. Indeed, Takotsubo syndrome has also been
described in association with COVID-19.27,34 The putative
mechanism is stress-related exaggerated catecholamine
response. However, further studies with longitudinal follow-
up are warranted to study the evolution of myocardial
lesions in COVID-19.
The CMR findings in children with COVID-19 were
also intriguing. In the case series by Blondiaux and col-
leagues, all 4 children presented with Kawasaki-like multi-
system inflammatory syndrome. CMR showed edema and
inflammation without LGE, suggesting absence of necrosis,
contrary to the findings in many of the adult patients.18,29
This is similar to histopathologic findings in Kawasaki dis-
ease where inflammatory infiltrates are found in the myo-
cardium (likely because of cytokine storm), with little
myocardial necrosis. This is different from viral myocarditis
where the immune response is directed toward the viral
infiltration of the myocardium. In Kawasaki-like disease,
myocardial inflammation peaks at day 10 after the disease
onset and disappears by 20 days and the putative mecha-
nism is the cytokine storm syndrome. Similar findings were
noted in this case series.10 This multisystem inflammatory
syndrome, with mucocutaneous, dermatologic, and gastro-
intestinal manifestations along with cardiac dysfunction is
being frequently described in children hospitalized with
COVID-19 infection.46
As described above, CMR can help in detection,
prognostication, management, and follow-up of myocardial
injury in COVID-19 survivors and to avoid invasive pro-
cedures. Performing EMB or coronary angiograms for the
diagnosis of myocardial involvement in this setting could be
challenging given the risks associated with the procedure,
the critical condition of the patients, and potential viral
exposure to health care workers. Recently published clinical
scenario-based guidelines for COVID-19 suggest that CMR
is indicated in patients with signs of myocardial infarction
with nonobstructive coronary arteries or in patients with
new-onset LV systolic dysfunction without the evidence of
CAD.47 CMR can help detect edema, necrosis, and con-
tractile dysfunction allowing for close monitoring of
affected individuals and promptly deciding appropriate
therapeutic strategies.
This review has the following limitations. Data search
was restricted to articles published in English-language liter-
ature. This may have resulted in missing data published in
other languages. The number of studies included in this review
is less because of paucity of data on this topic. Moreover, the
data across the studies is heterogeneous as regards clinical
presentation, description of imaging findings, sample sizes,
data availability, scanner used, acquisition protocols, and
individual experience of the personnel interpreting the data.
Hence, the findings from this review should be interpreted in a
suitable clinical context and with caution. Some findings such
as follow-up MRI features were based on only 3 case reports.
Although, a meta-analysis could not be performed in this
review due to lack of adequate robust studies, a meta-analysis
will be required in the future to address these challenges. Also,
the future cardiovascular outcomes of these subclinical finding
remain to be studied.
We conclude that the findings on CMR in patients
recovered from COVID-19 may provide insights into the
prevalence, mechanism, extent, and prognosis of myocardial
injury in these patients. The most common imaging diagnosis is
myocarditis and the most common imaging findings include T1
and T2 mapping abnormalities and myocardial edema followed
by LGE. Our systematic review highlights the utility of CMR
with its new quantitative mapping techniques as an essential
diagnostic tool to detect diffuse myocardial inflammation
associated with COVID-19 infection. It is essential that the
physicians and radiologists interpreting CMR are familiar with
a myriad of imaging spectrum of COVID, so that they can
influence the clinical decision-making in these patients.
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