|Year : 2021 | Volume
| Issue : 2 | Page : 150-157
Role of Cardiac Magnetic Resonance Imaging in Assessment of Cardiovascular Abnormalities in Patients with Coronavirus Disease 2019: Our Experience and Review of Literature
Priya D Chudgar, Nitin J Burkule, Srinivas Lakshmivenkateshiah, Nikhil V Kamat
Department of Radiology, Jupiter Hospital, Thane, Mumbai, Maharashtra, India
|Date of Submission||15-Jun-2021|
|Date of Acceptance||08-Jul-2021|
|Date of Web Publication||19-Aug-2021|
Dr. Priya D Chudgar
504, Shankar Bhuvan, Opp. Rajawadi Garden, Ghatkopar East, Mumbai - 400 077, Maharashtra
Source of Support: None, Conflict of Interest: None
Background: Long-term effects of coronavirus disease-2019 (COVID-19) causing pulmonary fibrosis are a well-established fact. Whether similar changes persist in myocardium remains a cause of concern. Cardiac magnetic resonance imaging (MRI), although logistically limited during the acute phase of illness, is an excellent modality for evaluating persisting myocardial involvement in patients recovering from COVID-19. No previous study has described cardiac MRI in Indian patients with COVID-19. Materials and Methods: We summarize cardiac MRI findings in 43 patients (29 males) who underwent cardiac MRI at our center for various clinical indications after recovering from their COVID-19 episodes. All cardiac MRI examinations were performed on Siemens Verio 3 Tesla Scanner System with 70 cm bore. Necessary precautions and safety measures were taken as per the Society for Cardiovascular Magnetic Resonance recommendations and standard imaging protocols were followed. Results: Half of all patients (22, 51.2%) had presented after 6 weeks of their initial COVID-19, whereas most of the remaining patients (19, 44.2%) underwent MRI during 3–6 weeks after recovering from COVID-19. Exercise intolerance was the most common clinical presentation observed in 22 (51.2%) patients, followed by fatigue or generalized weakness (15 patients), fast heart rate (12 patients), and breathlessness (12 patients). The most common cardiac MRI finding was elevated T1 and T2 mapping values (14 patients, 32.6%). The other common findings were late gadolinium enhancement in 12 (27.9%) patients, pericardial effusion ± enhancement in 12 (27.9%) patients, and impaired left ventricular systolic function in 9 (20.9%) patients. Eleven (25.6%) patients had normal cardiac MRI. Conclusions: Our findings summarize common cardiac abnormalities detected by cardiac MRI in patients with recent COVID-19. Although these results cannot be postulated to estimate the overall burden of cardiac involvement in COVID-19, they provide valuable insight into clinical spectrum of these patients in Indian scenario.
Keywords: Late gadolinium enhancement, myocarditis, post-COVID sequelae, severe acute respiratory distress coronavirus-2
|How to cite this article:|
Chudgar PD, Burkule NJ, Lakshmivenkateshiah S, Kamat NV. Role of Cardiac Magnetic Resonance Imaging in Assessment of Cardiovascular Abnormalities in Patients with Coronavirus Disease 2019: Our Experience and Review of Literature. J Indian Acad Echocardiogr Cardiovasc Imaging 2021;5:150-7
|How to cite this URL:|
Chudgar PD, Burkule NJ, Lakshmivenkateshiah S, Kamat NV. Role of Cardiac Magnetic Resonance Imaging in Assessment of Cardiovascular Abnormalities in Patients with Coronavirus Disease 2019: Our Experience and Review of Literature. J Indian Acad Echocardiogr Cardiovasc Imaging [serial online] 2021 [cited 2021 Oct 24];5:150-7. Available from: https://www.jiaecho.org/text.asp?2021/5/2/150/324096
| Introduction|| |
Cardiovascular complications are common in coronavirus disease-2019 (COVID-19).,, Varied clinical presentations ranging from asymptomatic tachycardia, heart failure, myopericarditis, acute coronary syndrome, and thromboembolic complications are observed during different phases of the illness. Different pathogenic mechanisms such as direct viral injury, systemic inflammation, microvascular thrombosis have been postulated to explain these complications. In addition, several unrelated diseases such as tuberculosis which coexist in endemic countries, may also get unmasked due to concurrent COVID-19. These diverse manifestations often pose challenges in appropriate patient management.
Detailed history and clinical examination, combined with various biomarkers such as cardiac troponins, natriuretic peptides, D-dimer, and other inflammatory markers, are the mainstay in the initial suspicion and diagnosis of cardiovascular complications in patients with COVID-19. Echocardiography is the most important imaging modality employed for further evaluation of these patients. It provides valuable information regarding morphology and function of cardiac chambers, valves, and intracardiac hemodynamics, all of which significantly aid in the patient management.
Cardiac magnetic resonance imaging (MRI) is generally not recommended in patients with COVID-19, especially during the acute phase of illness, due to the obvious logistic constraints. However, in patients recovering from COVID-19 in whom there is strong clinical suspicion of cardiac involvement but echocardiography findings are equivocal, cardiac MRI can be of immense help and should be actively sought. The patients with severe acute illness requiring intensive care unit (ICU) admission pose challenge for MRI assessment. However, in such patients, MRI can be safely performed during recovering phase of illness as the signs of myocardial injury on cardiac MRI often persist for a longer duration. Cardiac MRI offers many advantages due to its noninvasive nature and the ability to permit comprehensive assessment of cardiac structure and function along with the assessment of myocardial edema and fibrosis. Multicomponent imaging can be performed in single setting with various imaging tools. Cine images in multiple planes provide accurate and highly reproducible measurements of cardiac function and volume. MRI can differentiate myocarditis from acute coronary syndrome during acute phase of illness. Tissue characterization with late gadolinium enhancement (LGE) helps in assessment and quantification of replacement fibrosis and scar. Pathophysiologic changes due to edema, hyperemia, and fibrosis are evaluated with parametric mapping of T1 and T2 relaxation time. The extent of pericardial involvement can be assessed with multiplanar imaging and free-breathing sequences. Thus, cardiac MRI provides valuable information for diagnosis and risk stratification in a single-planned study.
In this study, we describe our experience with cardiac MRI in patients with a history of COVID-19 infection.
| Materials and Methods|| |
The main objective of this observational study was to evaluate the role of cardiac MRI in the assessment of cardiac abnormalities in patients convalescing from COVID-19. This is a single-center study performed at a tertiary care hospital in Mumbai, during first and second waves of COVID-19 in India.
The patients with recent COVID-19, referred from pulmonologists, internists, and cardiologists, with different clinical presentations were evaluated with comprehensive, dedicated cardiac MRI protocol. Asymptomatic tachycardia, breathlessness on exertion, exercise intolerance, and rise in cardiac enzymes were the main presenting symptoms [Table 1]. Patients referred for other clinical indication (left bundle branch block, syncope, arrhythmia) but with a history of recent COVID-19 (3–6 months) were also included in the study. The study involved retrospective compilation of imaging findings from clinically indicated cardiac MRI scans and formal ethics committee approval was sought for the same.
|Table 1: Our single-centre experience of cardiovascular abnormalities on cardiac magnetic resonance imaging in patients with recent coronavirus disease 2019|
Click here to view
All cardiac MRI examinations were performed on Siemens Verio 3 Tesla Scanner System with 70 cm bore. Necessary precautions and safety measures were taken as per Society for Cardiovascular Magnetic Resonance protocol. All cardiac MRI examinations were conducted with electrocardiographic (ECG) gating and performed with adequate breath-hold using both anterior and posterior array coils. Segmented acquisition of 25 phases of cardiac cycle was obtained for each long-axis and short-axis view. Complete examination with cine images in three long-axis and six short-axis views, flow imaging of aorta and pulmonary artery with phase-contrast sequences, and LGE imaging using inversion recovery sequences was performed as per routine protocol. Parametric mapping was performed with a modified Look-Locker sequence, in mid-cavity short-axis. Native T1 mapping was performed prior to contrast administration and post-contrast acquisition was performed after 10 min of contrast injection. Postprocessing was done on a dedicated analysis software from Suiteheart®.
All the data were managed in a Microsoft Excel worksheet. Standard descriptive analysis was performed to summarize various clinical characteristics and cardiac MRI findings. The variables were described as counts and proportions.
| Results|| |
This is an observational study to share cardiac MRI experience at our center and includes all clinically referred patients with a history of COVID-19. [Table 1] summarizes the average age group, predisposing conditions along with clinical picture and radiologic findings seen in our patients.
Majority (93%) of our patients were in 35–60 years of age group but 3 children were also included. Two-thirds of all patients were males. Half of all patients (22, 51.2%) had presented after 6 weeks of their initial COVID-19, whereas most of the remaining patients (19, 44.2%) underwent MRI during 3–6 weeks after recovering from COVID-19. Exercise intolerance was the commonest clinical presentation observed in 22 (51.2%) patients, followed by fatigue or generalized weakness (15 patients), fast heart rate (12 patients) and dyspnea on exertion (12 patients). Nearly one-third of the patients underwent MRI in view of abnormal ECG or echocardiography findings.
The most common cardiac MRI finding was elevated T1 and T2 mapping values (14 patients, 32.6%). The other common findings were LGE in 12 (27.9%) patients, pericardial effusion +/-enhancement in 12 (27.9%) patients, and impaired left ventricular (LV) systolic function in 9 (20.9%) patients. Eleven (25.6%) patients had normal cardiac MRI.
A few interesting cases are described below in greater detail for illustrative purposes.
A 55-year-old doctor with a history of severe COVID-19 with 3 weeks of ICU stay was referred for cardiac MRI. There was significant pulmonary involvement on computed tomography (CT severity score=18/25) with elevated troponin levels and cytokine storm during acute phase of illness. He presented to MRI department after 3 months of COVID-19 as he noticed continued breathlessness on exertion and resting sinus tachycardia. Echocardiography findings were unremarkable. Cardiac MRI revealed patchy mid-myocardial and epicardial LGE. T1 and T2 mapping values were elevated (T1 value = 1275 ms [normal range <1150 ms], T2 value = 44 ms [normal range <40 ms]) [Figure 1]. Cardiac function and volume were within normal limits. There was no LV regional wall motion abnormality. These features were suggestive of fibrosis as sequelae to myocarditis. The patient was advised beta-blocker, angiotensine receptor blocker, and spironolactone and was advised to avoid strenuous exercise.
|Figure 1: Short-axis phase-sensitive inversion-recovery image (a) reveals patchy midmyocardial hyperenhancement in inferior and inferoseptal segments suggesting interstitial fibrosis. T1 (b) and T2 (c) mapping color-coded image demonstrate myocardial fibrosis. (Please note, every center needs to obtain normal ranges of T1 and T2 values for their magnetic resonance imaging machines. For our 3-Tesla machine the normal values are- T1= 1150 ms, T2= 40 ms)|
Click here to view
A 33-year-old female with a history of COVID-19 1 month ago with 7 days of uneventful hospitalization presented to the emergency department with palpitations and giddiness. Heart rate on admission was 250 bpm and systolic blood pressure was < 80 mm of Hg. ECG revealed ventricular tachycardia. She received direct-current cardioversion and was shifted to ICU for further management. Echocardiography revealed reduced LV systolic function with mild global hypokinesia. Troponin-I level was significantly elevated (2720 ng/mL). Cardiac MRI revealed normal morphology of cardiac chambers with no LV regional wall motion abnormality. However, there was patchy mid-myocardial and epicardial LGE involving septum and anterior wall of the LV [Figure 2]. T1 value (1285 ms), extracellular volume (ECV, 44%), and T2 value (60 ms) were also elevated. Presumptive diagnosis of viral myocarditis was considered and automatic implantable cardioverter-defibrillator insertion was performed. However, such extensive patchy LGE is not classical for COVID myocarditis in non-heart failure patients. Therefore, further workup with positron-emission tomography scan was done to evaluate for granulomatous myocarditis. It revealed multiple thoracic and abdominal lymph nodes and ileo-coecal bowel wall thickening. Supraclavicular lymph node biopsy and culture confirmed tuberculosis. The patient was started on anti-tuberculosis treatment. Follow-up evaluation showed reduced episodes of ventricular tachyarrhythmias during the first 3 months and complete resolution of arrhythmias at the end of 6 months. This case may point to the possibility of reactivation of tuberculosis due to COVID-19 and the immunosuppressive effect of short-term steroid therapy.
|Figure 2: Long-axis four-chamber (a) and short-axis (b) phase-sensitive inversion-recovery images reveal patchy midmyocardial and epicardial hyperenhancement. This type of late gadolinium enhancement is uncommon in coronavirus disease-2019. Further work up with positron emission tomography revealed bowel wall thickening and cervical lymph nodes (c). Histopathology confirmed tuberculous disease process (d)|
Click here to view
A 12-year-old child, with recent history of fever, vomiting, and headache, presented to the pediatric department. There was laboratory evidence of inflammation with increased levels of white blood cells, C-reactive protein (CRP), lactate dehydrogenase, and ferritin levels. On clinical examination, the patient had generalized anasarca with swollen hands and feet. Persistent fever warranted hospitalization. COVID immunoglobulin G (IgG) antibodies were reactive. During illness, renal parameters were abnormal. Echocardiography revealed mild LV hypokinesia with impaired systolic function (LV ejection fraction [LVEF] 45%). In view of clinically severe illness with multi-system organ involvement (renal, hematology, gastrointestinal, cardiac), a diagnosis of multisystem inflammatory syndrome secondary to COVID-19 was considered. Cardiac MRI was performed after good clinical recovery (>2 weeks). It revealed significantly high T1 and T2 values (native T1 = 1312 ms, ECV = 32%, T2 = 52 ms) [Figure 3]. There was no evidence of focal LGE. The patient received steroid therapy and was discharged when clinically stable.
|Figure 3: Significantly high T1 mapping values are seen with subtle patchy midmyocardial enhancement in short-axis projection|
Click here to view
A 9-year-old child presented to the emergency department, with a positive COVID RT-PCR test, high fever and symptoms of heart failure. All laboratory parameters for infection were increased, including white blood cells, CRP, D-dimer, lactate dehydrogenase, and serum ferritin levels. Echocardiography revealed global LV hypokinesia with a significant reduction of LVEF. The patient was shifted to pediatric ICU and started on inotropic support. Cardiac MRI study was performed after 10 days when the patient was stable. It revealed reduction of LVEF (20%), with significantly high T1 and T2 values [Figure 4]. Subtle focal LGE was seen involving mid inferolateral segment. Clinical presentation and MRI features suggested acute fulminant viral myocarditis. The patient was closely monitored and treated for the same.
|Figure 4: Significantly high T1 (1420 ms/normal 1150 ms) (a) and T2 (56 ms/normal 44 ms) values are seen along with subtle epicardial foci of late gadolinium enhancement along inferolateral wall (c). These fulfill the revised Lake Louise criteria for viral myocarditis|
Click here to view
A 58-year-old female was treated at home for COVID-19. She continued to have generalized weakness and malaise, however, these symptoms were ignored. Nearly after 6 months, she presented to the emergency department with severe breathlessness and abdominal distension. Echocardiography revealed pericardial effusion with the suggestion of constrictive physiology.
D-dimer and CRP levels were significantly elevated. She was referred for CT pulmonary angiogram which revealed lung parenchymal changes related to COVID-19 and massive pleural effusion on the left side [Figure 5]. There was significant pericardial thickening. No evidence of pulmonary thromboembolism was seen, however eccentric thrmobus was seen in ascending aorta. Cardiac MRI was performed in the same sitting in view of pericardial thickening and abnormal echocardiography findings. It revealed pericardial thickening with intense postcontrast enhancement suggestive of pericarditis. Both ventricles were elongated and tubular in shape. There was bi-atrial dilatation with the presence of respirophasic septal bounce on cine images. Imaging features were suggestive of constrictive physiology. All markers for active tuberculosis including pleural fluid cytology, adenosine deaminase, GeneXpert, and Mantoux test were negative. COVID IgG antibody was significantly elevated. Unfortunately, due to her late clinical presentation, she deteriorated rapidly and finally succumbed.
|Figure 5: Axial images reveal pericardial thickening and left sided pleural effusion (a). Also note patchy subpleural parenchymal opacification in both lungs (b) with thrombus in aorta (c). There is intense post-contrast enhancement involving pericardium (d) suggestive of pericarditis|
Click here to view
A 50-year-old male doctor-developed COVID-19 pneumonia during the first wave of infection while actively treating COVID-19 patients. His hospital stay was stormy due to cytokine storm which required high-dose steroids and anti-interleukin drugs. No cardiac markers were investigated at that time, as cardiac involvement was not suspected by medical community due to limited experience. Postdischarge, he continued to have resting sinus tachycardia and exercise intolerance. He was reassured that it would settle in couple of months along with lung changes. However, despite complete resolution of pulmonary changes, he continued to be symptomatic for the next 11 months. His ECG was unremarkable, but echocardiography showed mildly reduced LV systolic function (LVEF 48%) with global hypokinesia. Cardiac MRI showed normal morphology with no LV regional wall motion abnormality. However, there was impaired LV systolic function (LVEF = 52%, LV global longitudinal strain = −15%) and presence of interstitial fibrosis (native T1 = 1285 ms, T2 = 40 ms) with patchy mid-myocardial LGE in septum [Figure 6]. This case apparently showed persistent sequelae of COVID-19 myocarditis (long COVID), after 11 months of initial COVID-19 episode.
|Figure 6: Cardiac magnetic resonance feature-tracking method can estimate global longitudinal strain (a) which can add value to T1 mapping (b) and late gadolinium enhancement (c) images to calculate burden of myocardial involvement|
Click here to view
| Discussion|| |
This is the first report from India, describing cardiac MRI findings in patients convalescing from COVID-19. Although these findings cannot be postulated to estimate overall burden of cardiac involvement in COVID-19, they provide valuable insight into clinical spectrum of these patients in the Indian scenario.
[Table 2] summarizes different clinical scenarios and cardiovascular presentations of COVID-19, as also illustrated in our examples above. Acute phase reactants with high troponin levels may suggest fulminant myocarditis. However, long-term myocardial effects (long COVID) of this illness are still not completely understood. The atypical presentations due to secondary infections or re-activation of tuberculosis are also not uncommon in endemic countries.
|Table 2: Spectrum of cardiovascular abnormalities in coronavirus disease 2019|
Click here to view
COVID-19 in the pediatric age group has different manifestations and complications. Limited reports available indicate that COVID-19 associated multisystem inflammatory syndrome in children can cause rapid deterioration; hence, increased index of suspicion and discussion regarding higher level of care are warranted early.
Given these observations, careful clinical screening and appropriately tailored use of diagnostic modality is advocated to address the specific clinical query in an individual patient.
Cardiac involvement with COVID-19 has varied clinical presentations.,, Acute cardiac injury is identified with the elevation of serum troponin levels in critically ill patients admitted in ICUs. However, this group is difficult to be evaluated with MRI and bedside echocardiography remains the investigation of choice.
Various mechanisms are postulated for chronic cardiac injury in COVID-19 patients. The cardiovascular inflammation is usually a bystander casualty as a result of immune overdrive during the period of cytokine storm., This type of myocarditis occurs without any direct viral infiltration and results in myocyte injury and replacement fibrosis. This group of patients, after discharge from the hospital, can be followed up using MRI with parametric mapping and LGE imaging. Secondary mechanisms of myocardial injury in COVID-19 include hemodynamic stress, hypoxia, acidosis (related to viral pneumonia), and coronary thromboembolism leading to myocardial infarction. Patients are also at risk for acute coronary syndrome due to viral illness with heightened inflammation and thrombotic environment. Any of the above mechanisms of cardiac injury can eventually lead to heart failure. These changes are comprehensively evaluated with multimodality imaging techniques.
Several prospective and retrospective imaging studies with cardiac MRI have been performed during acute illness and thereafter at various time intervals. These studies reveal varying degrees of myocardial injury in different cohorts of patients.
A prospective observational study done by Puntman et al. was published after first wave of COVID-19 illness. This was a single center study in a selected cohort of 100 patients who had recently recovered from COVID-19. Nearly 78% of them had cardiovascular involvement, irrespective of the preexisting conditions. The myocardial involvement was not related to severity of pulmonary involvement or the overall course of COVID-19 presentation. LGE and parametric mapping were found to be the most sensitive biomarkers to diagnose early cardiac damage. Persistent peri-and epicardial LGE was attributed to ongoing active pericarditis.
Another study done by Wang et al. included mid-term follow-up of 47 patients who recovered from moderate to severe COVID-19. It confirmed the presence of myocardial injury in nearly one-third of the patients at 3 months' interval. Impaired global longitudinal and circumferential strain involving left and right ventricles were useful marker to detect residual myocardial damage.
Another prospective study was performed by Joy et al. in healthcare workers with history of mild COVID-19. The study participants underwent cardiac MRI after 5 months of initial infection. The study concluded that there were no residual or permanent cardiovascular abnormalities seen in these healthcare workers with a history of mild COVID-19.
The persistence of myocardial injury in competitive athletes with a history of COVID-19 has been a major source of concern. In a cohort study of 1597 US competitive athletes, cardiac MRI screening was performed after COVID-19. Only 37 (2.3%) athletes were diagnosed with clinical and subclinical myocarditis, indicating an overall low prevalence of residual myocardial damage in them. However, long-term follow-up studies including control populations are required to understand the prognostic significance of these changes in competitive athletes. Furthermore, despite the reported low prevalence of myocardial injury, this group requires close monitoring due to the potential risk of catastrophic complications.
In our study also, we found evidence of LV myocardial involvement on cardiac MRI in more than half of the symptomatic subjects who underwent imaging. Majority of these patients had less extensive pulmonary involvement on CT during the acute phase of their illness. Moreover, in many of these patients, cardiac MRI abnormalities were detected despite an unremarkable echocardiography study (e.g. case 1 described above). These findings underscore the need to have a high clinical index of suspicion and performance of cardiac MRI in appropriately selected individuals. This also highlights the fact that in significantly symptomatic patients, it would be inappropriate to disregard the symptoms as non-organic in origin or merely due to physical deconditioning.
Before COVID-19 became a global pandemic, India was dealing with endemic tuberculosis. The link between tuberculosis and COVID-19 is bi-directional. The temporary immunosuppression induced by tuberculosis may increase the susceptibility of patients to COVID-19, and the latter, in turn, may increase susceptibility to tuberculosis due to immunosuppression. Further, although, there is no causal or direct association between COVID-19 and tuberculosis, both share common biosocial determinants such as overcrowding and malnutrition. This coexistence of tuberculosis and COVID-19 poses diagnostic challenges. COVID-19 has unmasked latent tuberculosis in many patients. Whether it is only a coincidental occurrence or coinfection, it finally leads to poor outcome.
Children and adolescents show different patterns of COVID-19 complications. Pediatric age group patients often have atypical clinical presentation with multisystem inflammatory syndrome similar to Kawasaki disease. These patients present with a history of fever, cervical lymphadenopathy, skin rash, and myopericarditis with elevated COVID IgG antibody levels. MRI signs of diffuse myocardial edema and hyperemia without evidence of focal myocardial necrosis have been reported in such patients. The pathophysiology is still unclear but an immune response to a COVID antigen is one of the likely mechanisms.
Our study had several limitations that merit attention. Due to logistic constraints, patients during the acute phase of illness were not included. Hence the true severity of cardiovascular complications in COVID-19 could not be assessed. Second, only the patients presenting with one or more symptoms warranting cardiac MRI were included. Due to this inevitable referral bias, our findings cannot be extrapolated to estimate overall burden of cardiovascular involvement in COVID-19. Third, ours was a single-center study in a small group of subjects and hence, our findings cannot be generalized to a wider population with different clinical presentations, risk profiles, and initial disease severity. Finally, the use of different MRI sequence parameters and post-processing approaches may yield different results in different settings.
| Conclusions|| |
Cardiovascular involvement with COVID-19 has diverse clinical manifestations. However, true prevalence and long term myocardial effects of COVID-19 remain unclear and long term follow up is required. Tissue characterization ability and parametric mapping with cardiac MRI can provide important diagnostic and prognostic information. Given this unique ability, cardiac MRI appears to be an optimal imaging modality to evaluate the multitude of cardiovascular effects of COVID-19 and should be performed in symptomatic patients. However, mildly symptomatic patients with community spread of infection should not undergo cardiac MRI study as it would be a waste of societal resources. Multidisciplinary team approach is crucial for ensuring optimal resource utilization and successful clinical outcomes.
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent forms. In the form, the legal guardian has given his consent for images and other clinical information to be reported in the journal. The guardian understands that names and initials will not be published and due efforts will be made to conceal identity, but anonymity cannot be guaranteed.
All CMR data post processing has been done using suiteHEART®, NeoSoft LLC, Wisconsin, USA.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Chang WT, Toh HS, Liao CT, Yu WL. Cardiac involvement of COVID-19: A comprehensive review. Am J Med Sci 2021;361:14-22.
Sharma YP, Agstam S, Yadav A, Gupta A, Gupta A. Cardiovascular manifestations of COVID-19: An evidence-based narrative review. Indian J Med Res 2021;153:7-16.
] [Full text]
Bansal M. Cardiovascular disease and COVID-19. Diabetes Metab Syndr 2020;14:247-50.
Shrinivasan R, Rane S, Pai M. India's syndemic of tuberculosis and COVID-19. BMJ Glob Health 2020;5:e003979.
Ferreira VM, Piechnik SK. CMR parametric mapping as a tool for myocardial tissue characterization. Korean Circ J 2020;50:658-76.
Kelle S, Bucciarelli-Ducci C, Judd RM, Kwong RY, Simonetti O, Plein S, et al.
Society for Cardiovascular Magnetic Resonance (SCMR) recommended CMR protocols for scanning patients with active or convalescent phase COVID-19 infection. J Cardiovasc Magn Reson 2020;22:61.
Kramer CM, Barkhausen J, Flamm SD, Kim RJ, Nagel E; Society for Cardiovascular Magnetic Resonance Board of Trustees Task Force on Standardized Protocols. Standardized cardiovascular magnetic resonance imaging (CMR) protocols, society for cardiovascular magnetic resonance: Board of trustees task force on standardized protocols. J Cardiovasc Magn Reson 2008;10:35.
Abbasi J. Researchers investigate what COVID-19 does to the heart. JAMA 2021;325:808-11.
Hennon TR, Yu KO, Penque MD, Abdul-Aziz R, Chang AC, McGreevy MB, et al.
COVID-19 associated multisystem inflammatory syndrome in children (MIS-C) guidelines; Revisiting the Western New york approach. Prog Pediatr Cardiol 2020, May 23:101232.
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;5:1265-73.
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;23:14.
Joy G, Artico J, Kurdi H, Seraphim A, Lau C, Thornton GD, et al.
Prospective case-control study of cardiovascular abnormalities 6 months following mild COVID-19 in healthcare workers. JACC Cardiovasc Imaging 2021 Feb-May (In Press).
Daniels CJ, Rajpal S, Greenshields JT, Rosenthal GL, Chung EH, Terrin M, et al.
Prevalence of clinical and subclinical myocarditis in competitive athletes with recent SARS-CoV-2 infection: Results from the big ten COVID-19 cardiac registry. JAMA Cardiol 2021May 27:e212065.
Kim JH, Levine BD, Phelan D, Emery MS, Martinez MW, Chung EH, et al.
Coronavirus disease 2019 and the athletic heart: Emerging perspectives on pathology, risks, and return to play. JAMA Cardiol 2021;6:219-27.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]
[Table 1], [Table 2]