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Cardiac magnetic resonance imaging in early diagnostics of myocardial inflammation after COVID-19: case series and literature review

Marija Zdravković1,2, Slobodan Klašnja1, Maja Popović1, Predrag Đuran1, Andrea Manojlović1, Milica Brajković1, Olivera Marković1,2, Igor Jovanović1, Marija Branković1,2, Višeslav Popadić1
  • University Hospital Medical Center "Bežanijska kosa", Belgrade, Serbia
  • Faculty of Medicine, University of Belgrade, Belgrade, Serbia

ABSTRACT

Although, in the beginning, it was considered a respiratory infection with bilateral pneumonia as its main manifestation, COVID-19 is more of a multisystemic disease with various extrapulmonary manifestations. Cardiovascular manifestations are caused by direct viral involvement or by the effects of different cytokines on the myocardium and can occur during the acute phase of the disease or in the post-acute stadium. The most common cardiovascular symptoms in the post-acute COVID-19 stadium are fatigue, shortness of breath, chest pain, and palpitations. Routine cardiovascular diagnostics in these patients is usually without significant findings, although underlying myocardial inflammation may be present. Myocardial damage can also be the substrate for the worsening of heart failure and different potentially life-threatening arrhythmias, which is extremely important for further treatment and prognosis. Cardiac magnetic resonance imaging is a sophisticated, non-radiating imaging modality that can provide important information regarding left and right ventricle volumes and function, tissue characterization, and scar quantification. It is the golden standard in non-invasive diagnostics of myocarditis. In patients with prior COVID-19 infection and cardiovascular symptoms, typical signs of myocarditis, including myocardial edema, necrosis, and myocardial scarring, may be seen in cardiac magnetic resonance. Also, there are sophisticated cardiac magnetic resonance imaging modalities that can register subtle changes in the myocardium, in terms of myocardial inflammation, without visible signs in standard sequences.

We present a case series of patients with different myocardial inflammation patterns, followed by a comprehensive review of potential pathophysiological mechanisms, complications, treatment and prognosis of patients with myocarditis or pericarditis after COVID-19


INTRODUCTION

COVID-19 is primarily a respiratory infection caused by the SARS-CoV-2 virus, but with multiple extrapulmonary manifestations that can significantly affect further patient treatment and prognosis, which makes it a multisystemic disease with an unpredictable course and potentially numerous post-COVID complications [1]. A severe clinical condition in patients with COVID-19 is the result of an increased demand on the heart in terms of oxygen, endothelial injury, micro and macrovascular thrombosis, and cytokine storm. Patients with a severe form of the disease are more susceptible to myocardial injury, which is caused by direct viral involvement or by the effects of different cytokines on the myocardium [2]. Sometimes, as the result of different pathophysiological mechanisms, including acute myocardial infarction, pulmonary embolism, septic shock, myocarditis, pericarditis and other conditions, myocardial injury can be the substrate for the worsening of heart function, the development of heart failure or malignant arrhythmias, which may lead to further clinical deterioration and potentially, death [3]. Myocardial injury has been detected in 7.0% to 17.0% of patients hospitalized with COVID-19, while the number of patients admitted to intensive care units with myocardial injury is higher, ranging from 22.0% to 31.0% [4]. Apart from myocardial injury in the milieu of acute COVID-19 infection, different substrates can cause myocardial damage in the post-COVID period, provoking different cardiovascular symptoms and affecting the patient’s quality of life and prognosis [5]. The most common cause is myocardial inflammation, usually undetectable by routine echocardiography.

Cardiac magnetic resonance imaging (CMR) is a sophisticated non-radiating imaging modality that represents the golden standard in estimating myocardial inflammation or myocarditis. It has a high reproducibility and less inter-observer variability than other imaging modalities and can also provide important information regarding left and right ventricle volumes and function, tissue characterization, and scar quantification [6].

At the University Hospital Medical Center Bežanijska kosa, the training for cardiac magnetic resonance imaging started in 2014, under the auspices of the European Society of Cardiology, while the procedure was introduced as a standard diagnostic technique in 2016, by Assistant Professor Marija Zdravković. In the meantime, the CMR team was formed, comprised of both radiologists and cardiologists, whereby a multidisciplinary approach was achieved in resolving diagnostic dilemmas. In 2019, the University Hospital Medical Center Bežanijska kosa received advanced technical hardware and software improvements to the Avanto 1.5 T CMR machine (Siemens), accomplishing sophisticated methods of tissue characterization with T1 i T2 mapping (pre- and post-contrast sequences), thereby significantly improving the sensitivity and specificity of this imaging modality. As of May 2021, at the Laboratory for Cardiac Magnetic Resonance Imaging of the University Hospital Medical Center Bežanijska kosa, the adenosine stress CMR test has been in use, as a part of standard clinical procedure, and this methodological achievement has provided the highest scientific standard for the CMR Lab. Since the beginning of the COVID-19 pandemic until now, more than 316 cardiac magnetic resonance examinations have been performed in patients with suspected myocardial-pericardial post-COVID-19 syndrome.

At the COVID-19 triage facility of the University Hospital Medical Center Bežanijska kosa, in the period starting from June 22, 2020, to the date when this manuscript was finished (November 7, 2021), a total of 41,126 patients were examined, diagnosed and placed into the system for COVID-19 treatment. Cardiac magnetic resonance imaging was performed in 316 patients suspected of the syndrome of post-COVID myopericarditis. In 292 patients (92.4 %), pathological findings indicating the syndrome of post-COVID myopericarditis were detected. In this paper, we present a case series of patients with different myocardial inflammation patterns, detected by cardiac magnetic resonance imaging, and we also present a comprehensive comparative review of currently most relevant research data related to the pathophysiological mechanism, complications, treatment and prognosis of patients with myocardial or pericardial inflammation after COVID-19.

CASE SERIES

Case report 1.

A 24-year-old female patient, two months after asymptomatic COVID-19 infection, was feeling fatigue, palpitations and dizziness. The symptoms were pronounced during physical activity. Echocardiography revealed a preserved ejection fraction, without wall motion abnormalities, without signs of pericardial effusion. ECG revealed a normal sinus rhythm, of a 95/min frequency, with a single ventricular extrasystole, without ST and T abnormalities. 24-hour Holter monitoring showed 4,339 episodes of ventricular extrasystolic beats, polymorphic, from five focuses, with 514 episodes of bigeminy, 20 episodes of trigeminy, 30 couplets, and 2 episodes of non-sustained ventricular tachycardia. High-sensitive troponin T and C-reactive protein were 36 pg/ml (ref. range: 0 – 14 pg/ ml) and 30.9 mg/L (ref range: <5mg/L), respectively.

Bearing in mind the finding of 24-hour Holter monitoring and the laboratory parameters, the patient was referred for cardiac magnetic resonance imaging. Cardiac magnetic resonance imaging was performed using the standardized cardiac imaging protocol. Myocardial edema was registered on STIR sequences, while prolonged mean T2 time and native T1 time was registered in the apical septal segment, in the medial apical anterolateral segments, as well as in the mid-base inferior and inferolateral segments (Figure 1).

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Figure 1. A) T2 myocardial mapping, four-chamber view: Prolonged values of mean T2 time in the apical septal segment and the medioapical lateral segment; B) Native T1 myocardial mapping, short axis view: Prolonged mean native T1 time in the medial inferolateral segment

The mean T2 time on the myocardial mapping sequences was 68 ms, while the mean native T1 time was 1,061 ms. The extracellular volume fraction (ECV) was 28.1 (reference range: 25.3 ± 3.5% at 1.5 T). After the application of the gadolinium contrast medium, the LGE phenomenon was observed in the anterior lateral segments mesomyocardially and subepicardially, in the medial inferior segment. Late pericardial enhancement in front of the lateral wall with effusion up to 7 mm was also noted, indicating pericardial inflammation with consequent pericardial effusion (Figure 2).

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Figure 2. A) Post-contrast sequence (LGE MAG study, short axis view): Mesomycardial LGE phenomenon in the basal anterolateral segment with late pericardial enhancement phenomenon in front of the lateral wall of the left ventricle; B) Post-contrast sequence
(LGE PSIR study, two- chamber view): Mesomycardial LGE phenomenon in the medial anterior segment and subepicardial LGE phenomenon in the medial inferior segment

The global ejection fraction was preserved at the moment of the first examination. Follow-up echocardiography, after one month, revealed a decreased ejection fraction of 40.0% and pericardial accretion in front of the lateral wall. Optimal medical therapy was introduced according to the guidelines of the European Society of Cardiology, which led to the withdrawal of symptoms and an improvement in the patient’s overall condition. It was indicated that the patient needed further cardiological follow-up.

Case report 2.

A 28-year-old woman was hospitalized due to COVID-19, with predominantly gastrointestinal symptoms (diarrhea), but also with myalgia and a cough. She had been febrile or with subfebrile body temperature throughout the first 10 days of the illness. According to protocol, during hospitalization (on the 8th day), computed tomography imaging (CT) of the thorax was performed, without signs of pneumonia. Follow-up radiographies showed no signs of further progression. Six months after the infection the patient began feeling palpitations, instability, chest discomfort, excessive fatigue and her heart rate was usually above 120/min, even during light physical activity. Echocardiography revealed a preserved ejection fraction, without wall motion abnormalities and without signs of pericardial effusion. ECG revealed normal sinus rhythm, of a 77/min frequency, without ST and T abnormalities. 24-hour Holter monitoring revealed a single supraventricular extrasystolic beat.

Bearing in mind the fact that the cardiovascular symptoms had become more pronounced, both at rest and during physical activity, the patient was referred for cardiac magnetic resonance imaging, for further diagnostics. Cardiac magnetic resonance imaging was performed using the standardized cardiac imaging protocol on the Siemens Avanto, 1.5 T machine. On STIR sequences, a small zone of transmural myocardial edema in the apical inferior segment was registered, as well as zones of prolonged T2 time and native T1 time on myocardial mapping sequences, in the apical inferior segment, the medial septal segment and the medial lateral segment (Figure 3).

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Figure 3. A) Pre-contrast STIR T2W sequence, two-chamber view: Transmural edema of the myocardium in the apical inferior segment; B) Native T1 myocardial mapping, two-chamber view: Prolonged mean native T1 time in the apical inferior segment (myocardial edema); C) T2 myocardial mapping, short axis view: Prolonged mean T2 time in the medial inferoseptal segment (myocardial edema)

The mean T2 time on myocardial mapping sequences was 72 ms, while the mean native T1 time was 1.348 ms. Extracellular volume fraction (ECV) was within the reference range. After the application of the gadolinium contrast medium, the transmural LGE phenomenon was observed in the medial inferosepetal and inferolateral segments, as well as the subepicardial LGE phenomenon in the medial inferior segment (Figure 4). The pericardium was with effusion, and its maximum thickness was 7 mm (Figure 5).

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Figure 4. Post-contrast sequence (LGE PSIR study), short axis view: Transmural LGE phenomenon in the medial inferoseptal segment and the medial inferolateral segment, subepicardial LGE phenomenon in the medial inferior segment

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Figure 5. A) Post-contrast sequence (LGE PSIR study), four-chamber view: Pericardial effusion in front of the right ventricular free wall; B) Native T1 myocardial mapping, four-chamber view: Pericardial effusion in front of the right ventricular free wall

Case report 3.

One month after COVID-19, a 62-year-old man was feeling palpitations and chest discomfort, without dyspnea, chest pain, loss of consciousness or swelling of the legs. Echocardiography revealed an enlarged left ventricle, globally hypocontractile, with an initially decreased ejection fraction (EF 45-50%), an interventricular septum with fibrous fine-grained changes, and an enlarged left atrium. ECG revealed normal sinus rhythm (frequency of 67/min), as well as AV block grade I, without ST and T abnormalities. 24-hour Holter monitoring showed 294 episodes of ventricular extrasystolic beats, single, from two focuses, with 3 couplets of monomorphic ventricular extrasystolic beats, two episodes of ventricular tachycardia (monomorphic ventricular extrasystolic beats with a salvo of 15, in the first one) during night sleep, and two episodes of non-sustained ventricular tachycardia (a salvo of 11 ventricular extrasystolic beats, in the second one).

Bearing in mind the echocardiography finding and the 24-hour Holter monitoring results, as well as laboratory parameters, the patient was referred for cardiac magnetic resonance imaging. Cardiac magnetic resonance (CMR) imaging was performed using the standardized cardiac imaging protocol, on the Siemens Avanto, 1.5 T machine. CMR showed a dilated left ventricle, globally hypocontractile, more pronounced in the basal and medial lateral segments, where the walls were thinned. It also revealed reduced ejection fraction (EF 44.97%), as well as increased left ventricular end-diastolic (EDVI 145.9 ml/m2 ) and end-systolic (80.3 ml/m2 ) volumes. Myocardial edema was not registered on STIR sequences. Myocardial mapping showed diffusely inhomogeneous signal intensity in the myocardium, more pronounced in the basal and medial anterior and inferior segments (Figure 6).

01f06

Figure 6. T2 and native T1 myocardial mapping sequences: Inhomogenous mean T2 and native T1 myocardial mapping values in the basal and medial anterior and inferoseptal segments (zones marked with arrows)

The mean T2 time on myocardial mapping sequences was 57 ms, while the mean native T1 time was 1,290 ms. The extracellular volume fraction (ECV) was 26.8%. Rest perfusion study showed a perfusion defect in the subendocardial zone of the lateral wall (Figure 7).

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Figure 7. Post-contrast sequence (rest perfusion), short axis stack (basal, medial and apical view): Subendocardial defect in the perfusion of all lateral wall segments

After application of the gadolinium contrast medium, the mesomyocardial LGE phenomenon was observed in the basal anterior, anteroseptal, and inferoseptal segments, covering 2.0% of the left ventricular myocardial mass. This type of distribution of the LGE phenomenon indicates myocarditis. The subendocardial LGE phenomenon was also registered in all lateral and inferolateral segments, covering 8,0% of the eft ventricular myocardial mass, which, according to its distribution, corresponds with vascular etiology (Figure 8).

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Figure 8. A) Post-contrast sequence (LGE MAG study), short axis view: Subendocardial LGE phenomenon in the medial anterolateral and inferolateral segments (vascular distribution); B) Post-contrast sequence (LGE MAG study), short axis view: Subendocardial LGE phenomenon in the apical lateral segment (vascular distribution); C) Post-contrast sequence (LGE MAG study), short axis view: Mesomyocardial LGE phenomenon in the basal inferoseptal segment (non-vascular distribution – myocarditis); D) Post-contrast sequence (LGE MAG study), short axis view: Mesomyocardial LGE phenomenon in the basal anterior, anteroseptal and inferoseptal segments (non-vascular distribution – myocarditis)

In the segments with registered subendocardial LGE phenomenon, post-contrast T1 myocardial mapping revealed zones of low mean post-contrast T1 time, indicating irreversible chronic ischemia and myocardial fibrosis (Figure 9). The pericardium has adhesions along the lateral wall of the left ventricle.

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Figure 9. A) Post-contrast T1 myocardial mapping, short axis view: Subendocardial zone with decreased mean post-contrast T1 time in the basal anterolateral and inferolateral segments; B) Post-contrast T1 myocardial mapping, short axis view: Subendocardial zone with decreased values of mean post-contrast T1 time in the medial anterolateral and inferolateral segments; C) Post-contrast T1 myocardial mapping, short axis view: Subendocardial zone with decreased values of mean post-contrast T1 time in the apical lateral segment

In view of the CMR finding which, in addition to myocarditis, also indicated coronary artery disease, the patient was referred for coronary angiography. Coronary angiography showed three-vessel disease with an occluded circumflex artery, an occluded first obtuse marginal branch, and intermediate stenosis of the left anterior descending artery (LAD), as well as significant stenosis of the right coronary artery. The patient was presented to the Heart Team which decided to estimate the hemodynamic significance of LAD stenosis and then make a decision on further treatment. It was estimated that the stenosis of the left anterior descending artery was not hemodynamically significant, so percutaneous coronary intervention (PCI) of the right coronary artery was performed, and the patient was left on optimal medical therapy and advised to reduce cardiovascular risk factors as much as possible. This case shows that, in the same patient, two etiologically different pathologies of the cardiac muscle can exist – both coronary disease and a focal inflammation lesion, i.e., myocarditis. 

MYOCARDIAL DAMAGE AND MYOCARDIAL INFLAMMATION IN PATIENTS WITH/AFTER COVID-19 INFECTION

Pathophysiological substrate

In the setting of acute COVID-19 infection, different mechanisms may be responsible for myocardial damage. Hypoxia and microthrombosis, pronounced in patients with the severe form of the disease, may affect the myocardium and cause myocardial injury [7]. Direct viral involvement with its cytopathic effect leads to the necrosis of cardiomyocytes and potentially to myocardial inflammation. A small study carried out by Italian researchers confirmed the presence of the viral genome and proteins in cardiac samples of COVID-19 patients [8]. Various predictive scores have been developed to stratify patients with increased risk of developing the severe form of the disease [9]. Different laboratory parameters, including cytokines, are marked as important predictors of infection severity and mortality, and are responsible for hyperinflammatory syndrome and subsequently multi-organ failure [10]. Cytokines may also induce indirect myocardial damage. It has been shown that a certain group of patients may have elevated cytokine levels weeks after the acute infection, providing a possible explanation of prolonged or late myocardial damage [11]. It has been demonstrated that elevated levels of cytokines and cardiac markers in patients with COVID-19 may be linked to reduced ejection fraction, which can be highly significant for the further prognosis of these patients [12]. Autonomic dysfunction after acute infection can result in postural orthostatic tachycardia and subsequently sinus tachycardia, which is a common finding of 24- hour ECG monitoring in patients, after COVID-19 infection [13]. However, focal myocarditis may be the focus of very serious, life-threatening arrythmias in patients with post-COVID myopericarditis syndrome. Cardiac magnetic resonance imaging is the golden standard for diagnosing these pathologies.

Symptoms and signs

Post-acute COVID-19 is defined as persistent symptoms and delayed or long-term complications of SARS-CoV-2 infection beyond 4weeks from the onset of symptoms [14]. Older people and people with comorbidities are the most likely to experience prolonged COVID-19 symptoms. Among many symptoms, it has been shown that fatigue, shortness of breath, chest pain, and palpitations are the most common. These symptoms may also indicate the exacerbation of the patient’s primary disease, most likely cardiovascular or respiratory. Although these symptoms are usually mild, they significantly affect the patient’s quality of life, increasing the need for proper diagnosis and treatment [15]. A large observational study in the United States of America reported that 32.6% patients had persistent symptoms two months after the infection, with dyspnea, cough and loss of smell or taste as the most common ones [16]. Carvalho-Schneider et al. reported that almost one-third of patients were feeling worse in the post-COVID period than at the onset of acute COVID-19 infection [17]. 

Diagnosis

Clinical and imaging evaluation of patients after COVID-19 should be considered primarily for patients with persistent cardiovascular symptoms. ECG and echocardiogram, as routine modalities, should be performed in every patient reporting cardiovascular symptoms, followed by more advanced cardiovascular imaging modalities, including cardiac magnetic resonance, on a case-to-case basis. Myocardial inflammation after COVID-19 is usually focal and often undetectable by routine echocardiography, with preserved or mildly reduced ejection fraction, while the finding of 24-hour ECG monitoring generally reveals sinus tachycardia, without significant cardiac rhythm abnormalities [18]. Malignant ventricular arrhythmias may be seen in severe forms of myocardial inflammation and are linked with the decrease in ejection fraction, which usually requires hospitalization for further diagnostics and treatment [19].

Treatment and prognosis

The regular cardiovascular treatment regimen should not be suspended during the acute phase of COVID-19 or after the infection has passed, as discontinuation of the guideline therapy may exacerbate existing cardiovascular conditions [20]. Low-dose beta blockers may be important in heart rate management and in reducing adrenergic activity in patients with tachycardia [21]. Therapy with vitamin and oligomineral supplements can boost immune mechanisms and provide a proper defense against direct or indirect viral involvement. The overall long-term impact of cardiac involvement in COVID-19 is yet to be established.

Recovery

Recovery after COVID-19 is extremely important, especially in physically active individuals or professional athletes. In individuals with signs of direct or indirect viral cardiac involvement, following the return-to-play protocols is recommended [22]. In young professional athletes with prior COVID-19 infection, it is important to have at least two weeks rest after symptom onset, including a minimum of seven days after the resolution of all symptoms, or after the cessation of therapy prescribed within the COVID-19 treatment protocol. In athletes with the severe form of COVID-19 and confirmed myocardial involvement, or myocardial inflammation, it is recommended to cease sports activities for at least 3 – 6 months until the complete resolution of symptoms and signs of acute myocardial inflammation, with recommended further clinical follow-up [23]. Gradual return to play, with close monitoring of symptoms (chest pain, fatigue, palpitations, dizziness or fainting), physical examination, and further diagnostics, if necessary, will prevent possible life-threatening complications.

CARDIAC MAGNETIC RESONANCE IMAGING AS THE GOLDEN STANDARD FOR NON-INVASIVE DIAGNOSTICS OF PATIENTS WITH MYOCARDIAL INFLAMMATION AFTER COVID-19

The role of cardiac magnetic resonance imaging in patients with cardiovascular symptoms after COVID-19 is of great importance. Most of these patients have a preserved global systolic function, with mild or moderate symptoms, as well as a predominantly normal finding of laboratory results, which is why there is no justifiable reason for performing myocardial biopsy with the aim of potentially confirming the diagnosis of myocarditis. The optimal time to perform CMR would be as early as possible after the onset of symptoms, as echocardiography is usually inconclusive, while the patient may indeed have acute myocardial of pericardial involvement [24].

The diagnosis of typical myocarditis relies on the Lake-Louise criteria and the detection of myocardial edema, necrosis, and myocardial scarring [25]. In addition to the left gadolinium enhancement phenomenon, which can indicate myocardial necrosis or fibrosis, novel cardiac magnetic resonance methods, primarily myocardial mapping, can provide a wider image of myocardial damage, its extent, and its possible effect on left ventricular function. The updated Lake-Louise criteria now includes implemented myocardial mapping values (T2, native T1 mapping and ECV) as standard criteria for confirming the presence of myocardial edema and fibrosis [26]. The presence of myocardial edema in patients after COVID-19 is detectable via myocardial mapping in a large portion of patients with cardiovascular symptoms, even without detected late gadolinium enhancement. Although these findings are more common in younger, previously healthy individuals, the presence of myocardial damage of this type can affect people with associated previous cardiovascular diseases and exacerbate these diseases.

In their study, Puntmann et al. revealed cardiac involvement on CMR images in 78.0% and ongoing myocardial inflammation in 60.0% of patients with mild to moderate symptoms who had had elevated values of high-sensitivity troponin during the acute infection or after COVID-19 [27]. The most commonly affected segments were the interventricular septum, the basal and medial segments of the anterior and anterolateral wall, as well as the inferior and inferolateral wall at the base and mid-chamber, with mesomyocardial and subepicardial edema or the LGE phenomenon. It is also important to note that, in other types of viral myocarditis, the inferior and inferolateral segments of the left ventricle are usually affected. Myocardial edema was also detected by myocardial mapping sequences. The values of global native T1 above 1,136 ms and T2 values above 40 ms were considered significant [27]. Patients with detected late gadolinium enhancement (LGE) phenomenon had significantly decreased LV peak global circumferential strain (GCS), RV peak GCS, and RV peak global longitudinal strain (GLS) [28].

It is significant to note that patients with postCOVID symptoms indicated for cardiac magnetic resonance imaging can have previously undiscovered cardiac conditions, including structural cardiac diseases, cardiomyopathy or ischemia. This is why it is extremely important not only to search for myocardial damage, in terms of myocarditis, but also to get a wider image of the patient’s current clinical condition and look for other cardiological diseases, which may be the cause of symptoms in these patients.

Pericardial involvement is a significant aspect in patients with cardiovascular symptoms after COVID-19. Brito et al. found, among 160 athletes who had had mild to moderate COVID-19 symptoms, that 39.5% of the participants had only pericardial involvement, with the lateral pericardium affected in a majority of the cases, while 22.0% of patients had both myocardial and pericardial involvement [29]. The global ejection fraction was preserved in all participants, without a statistically significant difference, as compared to healthy controls. Pericardial involvement in these patients was detected mainly as residual pockets of pericardial effusion or late pericardial enhancement, revealing an increased vascularity with pericardial inflammation. According to the CMR findings, a majority of these patients was classified under the subacute or convalescing phase, as most of them had no signs of typical acute pericardial inflammation. This is important to emphasise, as the acute phase probably occurs earlier in the clinical course of COVID-19, especially in patients with cardiovascular symptoms and positive cardiac and inflammatory markers.

Risk assessment is important, as most of the patients usually present in the convalescent phase, after fibrosis and the LGE phenomenon had already developed and are visible on CMR. The quantification of the LGE phenomenon is significant for estimating the risk of potential life-threatening arrhythmias and sudden cardiac death, as the LGE phenomenon has been associated with the risk of SCD more than reduced ejection fraction [30].

CONCLUSION

Myocardial inflammation after COVID-19 is a real clinical scenario that can significantly affect the quality of life, further treatment, and prognosis. Cardiac magnetic resonance imaging, as a sophisticated, non-radiating imaging modality, can provide crucial information on the presence of myocardial inflammation, its extent, and its possible effect on left ventricular function in patients with cardiovascular symptoms after COVID-19 infection, which is why it is the golden standard for diagnosing post-COVID myopericarditis syndrome. Further larger studies will definitely shed more light on the long-term effects of this important condition.

LIST OF ABBREVIATIONS AND ACRONYMS

CMR - cardiac magnetic resonance imaging
COVID-19 - coronavirus disease of 2019
ECG - electrocardiogram
ECV - extracellular volume
EDVI - end-diastolic volume index
EF - ejection fraction
LGE - late gadolinium enhancement
SARS-CoV-2 - severe acute respiratory syndrome coronavirus 2
SCD - sudden cardiac death
STIR - short tau inversion recovery

  • Conflict of interest:
    None declared.

Informations

Volume 2 No 4

December 2021

Pages 323-336
  • Keywords:
    COVID-19, magnetic resonance imaging, heart, myocarditis
  • Received:
    13 November 2021
  • Revised:
    06 December 2021
  • Accepted:
    16 December 2021
  • Online first:
    20 December 2021
  • DOI:
  • Cite this article:
    Zdravković M, Klašnja S, Popović M, Đuran P, Manojlović A, Brajković M, et al. Cardiac magnetic resonance imaging in early diagnostics of myocardial inflammation after COVID-19: Case series and literature review. Serbian Journal of the Medical Chamber. 2021;2(4):323-36. doi: 10.5937/smclk2-34913
Corresponding author

Marija Zdravković
University Hospital Medical Center "Bežanijska kosa"
Dr Žorža Matea Street, 11070 Belgrade, Serbia
E-mail: This email address is being protected from spambots. You need JavaScript enabled to view it.



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20. Zhang P, Zhu L, Cai J, Lei F, Qin JJ, Xie J, et al. Association of Inpatient Use of Angiotensin-Converting Enzyme Inhibitors and Angiotensin II Receptor Blockers With Mortality Among Patients With Hypertension Hospitalized With COVID-19. Circ Res. 2020 Jun 5;126(12):1671-81. doi: 10.1161/CIRCRESAHA.120.317134.[CROSSREF]

21. Vasanthakumar N. Beta-Adrenergic Blockers as a Potential Treatment for COVID-19 Patients. Bioessays. 2020 Nov;42(11):e2000094. doi: 10.1002/bies.202000094.[CROSSREF]

22. Wilson MG, Hull JH, Rogers J, Pollock N, Dodd M, Haines J, et al. Cardiorespiratory considerations for return-to-play in elite athletes after COVID-19 infection: a practical guide for sport and exercise medicine physicians. Br J Sports Med. 2020 Oct;54(19):1157-61. doi: 10.1136/bjsports-2020-102710.[CROSSREF]

23. McKinney J, Connelly KA, Dorian P, Fournier A, Goodman JM, Grubic N, et al. COVID-19-Myocarditis and Return to Play: Reflections and Recommendations From a Canadian Working Group. Can J Cardiol. 2021 Aug;37(8):1165-74. doi: 10.1016/j.cjca.2020.11.007.[CROSSREF]

24. Ojha V, Verma M, Pandey NN, Mani A, Malhi AS, Kumar S, et al. Cardiac Magnetic Resonance Imaging in Coronavirus Disease 2019 (COVID-19): A Systematic Review of Cardiac Magnetic Resonance Imaging Findings in 199 Patients. J Thorac Imaging. 2021 Mar 1;36(2):73-83. doi: 10.1097/RTI.0000000000000574.[CROSSREF]

25. Friedrich MG, Sechtem U, Schulz-Menger J, Holmvang G, Alakija P, Cooper LT, et al.; International Consensus Group on Cardiovascular Magnetic Resonance in Myocarditis. Cardiovascular magnetic resonance in myocarditis: A JACC White Paper. J Am Coll Cardiol. 2009 Apr 28;53(17):1475-87. doi: 10.1016/j. jacc.2009.02.007.[CROSSREF]

26. Ferreira VM, Schulz-Menger J, Holmvang G, Kramer CM, Carbone I, Sechtem U, et al. Cardiovascular Magnetic Resonance in Nonischemic Myocardial Inflammation: Expert Recommendations. J Am Coll Cardiol. 2018 Dec 18;72(24):3158-76. doi: 10.1016/j.jacc.2018.09.072.[CROSSREF]

27. Puntmann VO, Carerj ML, Wieters I, Fahim M, Arendt C, Hoffmann J, et al. Outcomes of Cardiovascular Magnetic Resonance Imaging in Patients Recently Recovered From Coronavirus Disease 2019 (COVID-19). JAMA Cardiol. 2020 Nov 1;5(11):1265-73. doi: 10.1001/jamacardio.2020.3557.[CROSSREF]

28. Wang H, Li R, Zhou Z, Jiang H, Yan Z, Tao X, et al. Cardiac involvement in COVID-19 patients: mid-term follow up by cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2021 Feb 25;23(1):14. doi: 10.1186/s12968-021-00710-x.[CROSSREF]

29. Brito D, Meester S, Yanamala N, Patel HB, Balcik BJ, Casaclang-Verzosa G, et al. High Prevalence of Pericardial Involvement in College Student Athletes Recovering From COVID-19. JACC Cardiovasc Imaging. 2021 Mar;14(3):541-55. doi: 10.1016/j.jcmg.2020.10.023.[CROSSREF]

30. Gräni C, Eichhorn C, Bière L, Murthy VL, Agarwal V, Kaneko K, et al. Prognostic Value of Cardiac Magnetic Resonance Tissue Characterization in Risk Stratifying Patients With Suspected Myocarditis. J Am Coll Cardiol. 2017 Oct 17;70(16):1964-76. doi: 10.1016/j.jacc.2017.08.050.[CROSSREF]

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9. Zdravkovic M, Popadic V, Klasnja S, Pavlovic V, Aleksic A, Milenkovic M, et al. Development and Validation of a Multivariable Predictive Model for Mortality of COVID-19 Patients Demanding High Oxygen Flow at Admission to ICU: AIDA Score. Oxid Med Cell Longev. 2021 Jun 30;2021:6654388. doi: 10.1155/2021/6654388.[CROSSREF]

10. Popadic V, Klasnja S, Milic N, Rajovic N, Aleksic A, Milenkovic M, et al. Predictors of Mortality in Critically Ill COVID-19 Patients Demanding High Oxygen Flow: A Thin Line between Inflammation, Cytokine Storm, and Coagulopathy. Oxid Med Cell Longev. 2021 Apr 20;2021:6648199. doi: 10.1155/2021/6648199.[CROSSREF]

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17. Carvalho-Schneider C, Laurent E, Lemaignen A, Beaufils E, Bourbao-Tournois C, Laribi S, et al. Follow-up of adults with noncritical COVID-19 two months after symptom onset. Clin Microbiol Infect. 2021 Feb;27(2):258-63. doi: 10.1016/j.cmi.2020.09.052.[CROSSREF]

18. Weckbach LT, Curta A, Bieber S, Kraechan A, Brado J, Hellmuth JC, et al. Myocardial Inflammation and Dysfunction in COVID-19-Associated Myocardial Injury. Trends Cardiovasc Med. 2020 Nov;30(8):451-60. doi: 10.1016/j.tcm.2020.08.002.[CROSSREF]

19. Manolis AS, Manolis AA, Manolis TA, Apostolopoulos EJ, Papatheou D, Melita H. COVID-19 infection and cardiac arrhythmias. Trends Cardiovasc Med. 2020 Nov;30(8):451-60. doi: 10.1016/j.tcm.2020.08.002.[CROSSREF]

20. Zhang P, Zhu L, Cai J, Lei F, Qin JJ, Xie J, et al. Association of Inpatient Use of Angiotensin-Converting Enzyme Inhibitors and Angiotensin II Receptor Blockers With Mortality Among Patients With Hypertension Hospitalized With COVID-19. Circ Res. 2020 Jun 5;126(12):1671-81. doi: 10.1161/CIRCRESAHA.120.317134.[CROSSREF]

21. Vasanthakumar N. Beta-Adrenergic Blockers as a Potential Treatment for COVID-19 Patients. Bioessays. 2020 Nov;42(11):e2000094. doi: 10.1002/bies.202000094.[CROSSREF]

22. Wilson MG, Hull JH, Rogers J, Pollock N, Dodd M, Haines J, et al. Cardiorespiratory considerations for return-to-play in elite athletes after COVID-19 infection: a practical guide for sport and exercise medicine physicians. Br J Sports Med. 2020 Oct;54(19):1157-61. doi: 10.1136/bjsports-2020-102710.[CROSSREF]

23. McKinney J, Connelly KA, Dorian P, Fournier A, Goodman JM, Grubic N, et al. COVID-19-Myocarditis and Return to Play: Reflections and Recommendations From a Canadian Working Group. Can J Cardiol. 2021 Aug;37(8):1165-74. doi: 10.1016/j.cjca.2020.11.007.[CROSSREF]

24. Ojha V, Verma M, Pandey NN, Mani A, Malhi AS, Kumar S, et al. Cardiac Magnetic Resonance Imaging in Coronavirus Disease 2019 (COVID-19): A Systematic Review of Cardiac Magnetic Resonance Imaging Findings in 199 Patients. J Thorac Imaging. 2021 Mar 1;36(2):73-83. doi: 10.1097/RTI.0000000000000574.[CROSSREF]

25. Friedrich MG, Sechtem U, Schulz-Menger J, Holmvang G, Alakija P, Cooper LT, et al.; International Consensus Group on Cardiovascular Magnetic Resonance in Myocarditis. Cardiovascular magnetic resonance in myocarditis: A JACC White Paper. J Am Coll Cardiol. 2009 Apr 28;53(17):1475-87. doi: 10.1016/j. jacc.2009.02.007.[CROSSREF]

26. Ferreira VM, Schulz-Menger J, Holmvang G, Kramer CM, Carbone I, Sechtem U, et al. Cardiovascular Magnetic Resonance in Nonischemic Myocardial Inflammation: Expert Recommendations. J Am Coll Cardiol. 2018 Dec 18;72(24):3158-76. doi: 10.1016/j.jacc.2018.09.072.[CROSSREF]

27. Puntmann VO, Carerj ML, Wieters I, Fahim M, Arendt C, Hoffmann J, et al. Outcomes of Cardiovascular Magnetic Resonance Imaging in Patients Recently Recovered From Coronavirus Disease 2019 (COVID-19). JAMA Cardiol. 2020 Nov 1;5(11):1265-73. doi: 10.1001/jamacardio.2020.3557.[CROSSREF]

28. Wang H, Li R, Zhou Z, Jiang H, Yan Z, Tao X, et al. Cardiac involvement in COVID-19 patients: mid-term follow up by cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2021 Feb 25;23(1):14. doi: 10.1186/s12968-021-00710-x.[CROSSREF]

29. Brito D, Meester S, Yanamala N, Patel HB, Balcik BJ, Casaclang-Verzosa G, et al. High Prevalence of Pericardial Involvement in College Student Athletes Recovering From COVID-19. JACC Cardiovasc Imaging. 2021 Mar;14(3):541-55. doi: 10.1016/j.jcmg.2020.10.023.[CROSSREF]

30. Gräni C, Eichhorn C, Bière L, Murthy VL, Agarwal V, Kaneko K, et al. Prognostic Value of Cardiac Magnetic Resonance Tissue Characterization in Risk Stratifying Patients With Suspected Myocarditis. J Am Coll Cardiol. 2017 Oct 17;70(16):1964-76. doi: 10.1016/j.jacc.2017.08.050.[CROSSREF]


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