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Cardiac Magnetic Resonance in Times of COVID-19: A Disease with Many Cardiac Faces

Although cardiac magnetic resonance (CMR) may proof useful in the diagnosis of myocardial injury triggered by COVID-19, limited experience has yet been published. We report several cases presenting its utility at various COVID-19 disease stages in diagnosing different cardiac manifestations. The current COVID-19 crisis will undoubtedly transform CMR imaging Units.


Introduction
Cardiac Magnetic Resonance (CMR) provides valuable clinical information in the characterization of myocardial injury secondary to COVID-19 infection. CMR not only provides reliable function quantification, but it can also detect acute inflammatory changes and necrotic damage [1]. Moreover, CMR results may have prognostic implications and hence guide clinical management of COVID-19 patients. However, information on the clinical use of CMR to date is limited, possibly due to a misperception of increased risk of infection to health workers, despite not involving direct contact with patients, as do other imaging modalities as, for example, echocardiography. Given that the health crisis will last, CMR Imaging Units will have to adapt the way they operate and redefine indications in times of COVID. Initial reports identified myocarditis as the main cardiac lesion triggered by COVID-19 and, less frequently, cases of a Tako-Tsubo-like syndrome [2,3]. Early diagnosis has proven key in initiating appropriate medical treatment, including aggressive anti-inflammatory therapy with corticosteroids and IL-6 inhibitors [4] or antiplatelet management. Here, we present several COVID-19 clinical cases where CMR plays a role in the differential diagnosis of various forms of cardiac damage at different stages of the disease, both during hospitalization and at follow up after discharge, with prognostic implications. Furthermore, the risk of misdiagnosis of non-COVID cardiomyopathies is yet another challenge we should be attentive to, as represented by two of the following cases. Demographic data, clinical symptoms, PCR test results, blood testing, imaging modalities, and clinical management for each are shown in Table 1.      (Figure 2A-C). In this case, CMR allowed accurate quantification of LV volume and function, overcoming a poor-quality TTE. Although the initial clinical suspicion was myocarditis, CMR did not show any evidence of acute inflammation or fibrosis. Coronary artery disease hence needs to be ruled out as a cause of the episode.

STIR (A) and
LGE (B-C) images with normal myocardial signal. LGE was not performed due to severe renal failure. Prolonged native T1 mapping with normal T2 mapping and T2-STIR images suggest the presence of diffuse myocardial fibrosis, possibly due to uremic cardiomyopathy secondary to the underlying chronic kidney disease ( Figure 3A-C). During hospitalization, both PCR and antiCOVID-19 test results were negative.

Case 6:
A 70-year-old man was referred to a routine CMR for aortic insufficiency evaluation in our Center.  LGE images showing subepicardial/intramyocardial enhancement in the basal inferolateral wall (E-F).

Discussion
COVID-19 era entails an important diagnostic challenge for cardiac imaging. CMR may help in the characterization of myocardial injury at different phases of the disease, as we have shown in cases 1 to 4, including acute/subacute myopericarditis and stress cardiomyopathy, in agreement with previous studies [5,6]. Interestingly, two patients presented with significant left ventricular dysfunction in the acute phase followed by a rapid LVEF recovery without evidence of myocardial scarring on follow-up-CMR, probably in the context of systemic inflammation, hypoxic damage, and a coexisting procoagulant state. Thus, CMR may be particularly useful in providing a differential diagnosis for COVID-19 cardiac damage and hence, guide clinical management [7]. As shown in cases 4 and 5, CMR overcome echocardiographic limitations, such as poor echocardiographic window or limited echo quality by the inconvenience of performing an echo in a COVID setting, because it provides accurate LVEF quantification.
Furthermore, CMR can improve diagnostic accuracy by tissue characterization over troponin levels, which may proof to be less specific in a complex, multisystemic disease such as COVID-19 (as shown by the poor correlation in these cases reflects the importance of CMR in the COVID-19 era. CMR units should keep in mind that any patient might be potentially infected and hence, safety and protection measurements must be implemented. Also, specialists must receive proper equipment and training to ensure safety in managing patients. In this context, the Society of CMR has recently provided guidance for the practice of CMR during the COVID-19 era [3].
Recommendations include the use of a single scanner and implementing shortened protocols. Organizational changes to attend both COVID and non-COVID patients and updated in CMR protocols of each CMR Unit are needed. Carrying out CMR scans for COVID patients at specific time during the day, selecting ambulatory cases, carrying out exhaustive sanitizing of facilities between scans, applying shorter acquisition protocols which should ideally be planned in advance, as well as carrying out remote imaging supervision and offline CMR analysis are among some of the measures that we have implemented in our Center.
In conclusion, the current COVID-19 pandemic has imposed a new reality, which has affected all areas of healthcare, including the CMR field. We have observed different CMR patterns of cardiac involvement at different phases of COVID-19 infection, each representing different diagnostic challenges. CMR can help understanding the cardiac involvement of this novel disease in terms of diagnosis, clinical management and will most probably be key in understanding mid-long term cardiac damage.

Take-Home Messages
-CMR has an important role in characterizing the various presentations of cardiac involvement of COVID-19, which may inform clinical treatment and prognosis.
-A wide differential diagnosis should be considered while characterizing myocardial injury in COVID-19 patients, including transient LV dysfunction secondary to direct and indirect, systemic mechanisms.
-CMR acquisition protocols, patients and staff safety and pre-procedural planning must be revised and updated to meet the challenges imposed by the COVID era.
-Extracardiac findings, such as pulmonary infiltrations on CMR, are key in asymptomatic patients in the diagnosis of current or past covid-19 infection. -CMR studies inform diagnosis, clinical management, and prognosis, and will be key in understanding longer-term cardiac involvement of COVID-19.
-Cardiac imaging Units need to adapt to meet the challenges imposed by COVID-19, including case selection, adapted acquisitions protocols, and safety procedures to guarantee patient and healthcare professional safety.