A subgroup of COVID-19 patients with cardiac magnetic resonance imaging evidence of myocardial inflammation may exhibit subendocardial fibrosis, compatible with myocardial infarction, while epicardial coronary arteries are normal. Â© 2021 The Authors. Clinical Case Reports published by John Wiley & Sons Ltd

Asadian, S.

Hosseini, L.

Rezaeian, N.

eprints Iran University of Medical Sciences

Clin Case Rep. 2021;00:1–6.    | 1wileyonlinelibrary.com/journal/ccr31 |  INTRODUCTIONSevere acute respiratory syndrome coronavirus- 2 (SARS- CoV- 2) infection, first reported in Wuhan, China, in December 2019, is spreading rapidly around the world. The site primarily affected by this infection is the respiratory system; however, simultaneous or even isolated cardiac in-volvement has been observed in some cases.1 Coronavirus disease 2019 (COVID- 19) can be diagnosed both via reverse transcription- polymerase chain reaction (RT- PCR) using pharyngeal swab specimens and via high- resolution com-puted tomography (CT) scans of the chest according to the recently published guidelines.2Some investigations have furnished robust evidence of myocardial injury during the active course of COVID- 19,3,4 with 8% of this group of patients suffering an acute myocar-dial insult.5 It is such high risks of virus- induced myocardial damage that render cardiac magnetic resonance (CMR) im-aging helpful for the care of cases with suspected or con-firmed COVID- 19. CMR is an excellent tool for functional and morphological studies in that it confers reliable tissue characterization and differentiation between acute ischemic and nonischemic myocardial injuries.6Late gadolinium enhancement (LGE) sequences are used for the detection of myocardial necrosis and fibro-sis and are deemed to be of prognostic value in determin-ing the increased risk of adverse cardiovascular events.7A greater extent of fibrosis, according to LGE, is associated with a higher risk of potentially life- threatening ventricular arrhythmias.8We herein present the CMR portrait of 2 definite cases of COVID- 19 with evidence of extensive myocardial fibrosis.2 |  CASE 1A 39- year- old woman presented to the emergency depart-ment with dyspnea of 1- month duration. The patient was a known case of asthma. On admission, she had a body tem-perature of 38°C, a blood pressure of 120/80 mm Hg, and a heart rate of 124 bpm. Physical examination revealed de-creased breath sounds at lung bases with rhonchi. Her oxygen saturation level in ambient air was estimated at 89%. Given the coronavirus outbreak, nasopharyngeal and oropharyngeal swabs were immediately obtained, which indicated SARS- CoV- 2 positivity.Received: 3 August 2020 | Revised: 1 February 2021 | Accepted: 9 February 2021DOI: 10.1002/ccr3.3972  C A S E  R E P O R TCardiac magnetic resonance findings in coronavirus disease 2019Nahid Rezaeian1  |   Leila Hosseini1,2  |   Sanaz Asadian1This is an open access article under the terms of the Creative Commons Attribution- NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.© 2021 The Authors. Clinical Case Reports published by John Wiley & Sons Ltd.1Rajaie Cardiovascular Medical and Research Center, Iran University of Medical Sciences, Tehran, Iran2Cardiology Department, North Khorasan University of Medical Sciences, Bojnurd, IranCorrespondenceSanaz Asadian, Rajaie Cardiovascular Medical and Research Center, Rajaie Cardiovascular Medical and Research Center, Niayesh Intersection, Next to Mellat Park, Vali- e- Asr Ave, Tehran, zip code: 1995614331, Iran.Email: Asadian_s@yahoo.comAbstractA subgroup of COVID- 19 patients with cardiac magnetic resonance imaging evi-dence of myocardial inflammation may exhibit subendocardial fibrosis, compatible with myocardial infarction, while epicardial coronary arteries are normal.K E Y W O R D SCardiovascular disorders, COVID- 192 |   REZAEIAN Et Al.Panel electrocardiography (ECG) showed sinus tachy-cardia with nonspecific ST- T wave changes (Figure  1A). Additionally, the level of high- sensitivity troponin I (hs- TnI) was elevated (0.54 µg/L; cut point <0.03 µg/L). Transthoracic echocardiography demonstrated severe left ventricular (LV) systolic dysfunction (ejection fraction  =  30%), associated with akinesia at the mid- to- apical portions of the anteroseptal and inferoseptal regions and hypokinesia in the other LV seg-ments. There was no evidence of ventricular dilation and val-vular abnormality. Also, we observed a mobile clot attached to the inferoapical LV portion, together with mild pericardial effusion (Figure 1B and C). Chest CT depicted severe mul-tifocal consolidation and ground- glass opacity in both lungs (Figure 1D).In the primary center, anticoagulation therapy (enoxapa-rin 60 mg BID, followed by apixaban 5 mg BID at discharge) and heart failure treatment (captopril 25 mg BID and spirono-lactone 25 mg QD, followed by carvedilol 3.25 mg BID after lung congestion reduction at discharge) were administered. Lopinavir/ritonavir was prescribed for COVID- 19 treatment under the supervision of an infectious disease specialist. Electrolytes were monitored during the admission and peri-odically after discharge.Two months after discharge from the primary center, the patient was referred to our tertiary referral center for cardiac evaluation. CMR revealed myocardial edema, pre-dominantly in the septal wall, and hyperemia (evidenced by early gadolinium enhancement sequences). Extensive patchy myocardial fibrosis with subepicardial, midwall, and subendocardial involvement in different LV segments (not in a specific vascular territory) was depicted on LGE sequences (Figure  2A- D). Pulmonary CT after 2  months showed substantial resolution in opacities despite nota-ble cardiac involvement (Figure  1E). Also, computed to-mography angiography (CTA) was performed to rule out coronary artery disease (CAD), which showed normal epi-cardial coronary arteries (Figure 2E- G).Therefore, a diagnosis of active myocarditis due to SARS- CoV- 2 infection with a unique involvement pattern was es-tablished. Given the patient's challenging condition, she was referred to a heart failure specialist for heart failure treatment, to be followed by another CMR 1 month later.F I G U R E  1  Electrocardiography, echocardiography, and chest computed tomography of CASE 1 are illustrated herein. A, Electrocardiography reveals sinus tachycardia with nonspecific ST- T wave changes. B, C, Transthoracic echocardiography shows a large mobile clot attached to the inferoapical left ventricular portion (arrow), together with mild pericardial effusion (arrowhead). D, E, Unenhanced chest computed tomography scan of the patient at initial coronavirus manifestations (D) and after 2 months (E) is depicted. Images are in the parenchymal window and from the maximum involvement level of the lung fields. D, Confluent mixed ground- glass opacity and consolidation areas in both central and peripheral distributions, associated with focal vascular dilatation; additionally, pleural and pericardial effusions are noted. E, There are a few faintly hyperdense residual opacities more in a nodular pattern with the adjacent linear densities, representing a fibrotic reaction   | 3REZAEIAN Et Al.3 |  CASE 2The patient was a 31- year- old man, who had a history of  bicuspid aortic valve with severe aortic valve insufficiency, preserved cardiac function (ejection fraction  =  50%- 55%), and severe LV enlargement in the preceding year. He had refused to undergo valve replacement surgery.On presentation to our center, the patient had dys-pnea, atypical chest pain, a low- grade fever, and coughs. Additionally, he had a body temperature of 38°C, a blood pressure of 135/55  mm  Hg, and a heart rate of 95  bpm. Physical examination was unremarkable, except for basal lung rales and 3/6 diastolic murmurs in the second inter-costal space. ECG illustrated evidence of LV hypertrophy (Figure 3A).Laboratory evaluation revealed an elevated hs- TnI level (0.32 µg/L), combined with a lymphocyte count of 1100/µL. Additionally, RT- PCR through pharyngeal swab specimens was positive.Transthoracic echocardiography showed severe LV sys-tolic dysfunction (ejection fraction = 10%- 15%) and enlarge-ment, severe hypokinesia in all LV segments with preserved tissue, a bicuspid aortic valve (fusion of the left and right coronary cusps) with subsequent severe aortic valve insuffi-ciency, holodiastolic flow reversal in the descending thoracic aorta and the abdominal aorta, and a dilated ascending aorta (Figure 3B- E). In comparison with the previous echocardiog-raphy report, documented a year earlier, a meaningful decline in the ejection fraction without a notable change in LV vol-ume was recorded.Chest CT depicted peripheral pulmonary ground- glass opacity and consolidation (Figure 4A). CMR was carried out for precise evaluation of the cause of the ventricular dysfunc-tion. Similar to CASE 1, there was evidence of myocardial edema, and hyperemia along with extensive myocardial fibro-sis in the subepicardial, midwall, and subendocardial regions (Figure 4B- D). CTA was performed to rule out CAD, which revealed normal epicardial coronary arteries (Figure 5).4 |  DISCUSSIONCOVID- 19– induced myocardial injury, with myocardial edema and fibrosis, is associated with adverse cardiac out-comes.3 Therefore, appropriate treatment crucially requires a prompt diagnosis in the early stages of the infection.In COVID- 19 cases with new- onset heart failure with-out known cardiovascular disease risk factors, myocarditis should be considered. Endomyocardial biopsy is not advis-able in COVID- 19 patients with associated myocarditis.4 The F I G U R E  2  Cardiac magnetic resonance and coronary computed tomography angiography images of CASE 1 are illustrated herein. A, Short tau inversion recovery sequence in the midventricular short- axis view shows evidence of myocardial edema. B- D, Short- axis (B) 3- chamber (C) and 4- chamber (D) views depict evidence of patchy subepicardial, midwall, and subendocardial to transmural late gadolinium enhancement, representative of myocardial fibrosis. E- G, Curved multiplanar reconstruction images of normal left anterior descending (between lines in E), diagonal branch (between lines in F), and right (between lines in G) coronary arteries are depicted herein4 |   REZAEIAN Et Al.CMR diagnosis of myocarditis (Lake Louise criteria) is on the basis of the presence of myocardial edema, hyperemia, and replacement fibrosis, with the latter evidenced by patchy LGE in affected regions. The most common locations of fi-brosis are subepicardial and midmyocardial layers.9In this report, we interpreted the CMR findings of 2 definite cases of COVID- 19 with cardiac involvement. They both exhibited myocardial edema and hyperemia, representing underlying inflammation. In CASE 1, the myocardial edema persisted for 2 months; accordingly, we believe that cardiac involvement in SARS- CoV- 2 infec-tion can progress to a type of chronic active myocarditis or some degree of persistent myocardial edema. In a remark-able study by Puntmann et al,10 a cohort of 100 patients underwent follow- up CMR 79  days after recovery from SARS- CoV- 2 infection, and cardiac involvement and active myocardial edema were scintillatingly detected in 78% and 60%, respectively, independent of preexisting conditions and the disease course. A salient finding in our patients was the concurrent involvement of all 3 myocardial lay-ers, particularly the subendocardial stripe in the different LV segments. Subendocardial fibrosis in a specific vascu-lar territory is a discriminating feature for differentiating acute myocarditis from myocardial infarction in that when present, it makes CAD the most probable of all differen-tial diagnoses. Nonetheless, in both of our cases, CAD was ruled out by CTA. According to the published investiga-tions, COVID- 19– induced myocardial injury is a result of a combination of causes.11The presence of myocardial edema and typical subepi-cardial/midmyocardial fibrosis in our patients may be in line with described inflammatory cascades in the COVID- 19 con-text. The existence of subendocardial fibrosis is attributable to probable microvascular damage caused by COVID- 19. We, thus, postulate that a combination of cytokine storms, inflammatory changes, and microvascular damage was cul-pable for ischemia with consequent acute myocardial injury in our cases.On the other hand, in CASE 1, the presence of an LV clot in the acute phase of the disease indicated the inherent risk of clot formation, which might be due to inflammatory changes. Indeed, we may assume that LV clots can cause coronary artery embolism and the resultant myocardial infarction.12In a case report, Gravinay et al13 described a patient with respiratory symptoms in favor of COVID- 19. Despite the negative RT- PCR and chest CT results, CMR, conducted 8 days after presentation, showed subepicardial inferolateral F I G U R E  3  Electrocardiography, echocardiography, and chest computed tomography of CASE 2 A are illustrated herein. Electrocardiography reveals evidence of left ventricular hypertrophy. B- E, Transthoracic echocardiography in the apical 4- chamber view (B) shows severe left ventricular dilation, continuous- wave Doppler imaging (C) reveals the diastolic jet of aortic regurgitation, and pulsed- wave recording and color M- mode recording (D, E) indicate holodiastolic flow reversal within the abdominal aorta and the descending thoracic aorta, respectively (arrow)   | 5REZAEIAN Et Al.LV wall edema, patchy LGE, and an LV apical clot in the presence of a normal LV function. These findings are com-patible with active myocarditis. Ultimately, serological tests, including immunoglobulin G and immunoglobulin M, for SARS- CoV- 2 immunization, were positive. Gravinay and colleagues, thus, underscored the crucial role of CMR in the diagnostic workup of cases with suspected COVID- 19.With respect to CASE 2, we believe that the severe de-cline in LV systolic function in the absence of a significant rise in LV volume could not have been due to the rapid pro-gression of valve insufficiency. The patient had no disorders such as aortic valve endocarditis that would have caused a sudden deterioration in LV systolic function. Moreover, cor-onary CTA, which is the preferred method to rule out CAD based on the suggested guidelines, showed no abnormality.4 We suspect that the diminished ejection fraction in CASE 2 may have been in consequence of an acute process such as myocarditis induced by SARS- CoV- 2. This notion chimes in with the findings of some studies concluding that heart fail-ure could follow myocarditis in the context of SARS- CoV- 2 infection.11,125 |  CONCLUSIONSSARS- CoV- 2 can influence the heart through different pathophysiologic mechanisms. An unusual pattern of sub-endocardial fibrosis, typical for myocardial infarction, is recognizable in the CMR of these patients in the absence of CAD. Multimodality CMR studies may have a crucial role F I G U R E  4  Cardiac magnetic resonance and chest computed tomography findings of CASE 2 are presented herein. A, Coronal unenhanced pulmonary computed tomography reveals segmental peripheral ground- glass opacities, which are highly suggestive of COVID- 19– related pneumonia. B, Evidence of COVID- 19 myocarditis is depicted in the late gadolinium enhancement sequence in the midventricular short- axis view. C, Short tau inversion recovery sequence in the midventricular short- axis view shows myocardial edema. D, Two- chamber view late gadolinium enhancement sequence demonstrates patchy myocardial fibrosis in the subepicardial and midwall regionsF I G U R E  5  Coronary computed tomography angiography of CASE 2 is demonstrated. A- D, Curved multiplanar reconstruction images of normal left anterior descending (between lines in A), left circumflex (between lines in B), a well- developed obtuse marginal branch (between lines in C), and right (between lines in D) coronary arteries are shown6 |   REZAEIAN Et Al.in the diagnosis of the different pathophysiologic aspects of COVID- 19.ACKNOWLEDGMENTSPublished with written consent of the patient.CONFLICT OF INTERESTThe authors declare no conflicts of interest.AUTHOR CONTRIBUTIONSAll the authors: read and approved the final manuscript. Nahid Rezaeian: planned the case report, evaluated the pa-tients, and played a major part in the writing of the manu-script. Sanaz Asadian: participated in the planning of the case report, evaluated the patients, and reviewed and discussed the manuscript. Leila Hosseini: participated in the writing and reviewing of the manuscript.DATA AVAILABILITY STATEMENTThe datasets generated during the current report are available from the corresponding author on reasonable request.ORCIDNahid Rezaeian   https://orcid.org/0000-0003-3565-5851 Leila Hosseini   https://orcid.org/0000-0002-6617-9053 Sanaz Asadian   https://orcid.org/0000-0003-2371-3575 REFERENCES 1. Yuki K, Fujiogi M, Koutsogiannaki S. COVID- 19 pathophysiol-ogy: A review. Clin Immunol. 2020;215:108427. 2. Song F, Shi N, Shan F, et al. Emerging 2019 novel coronavirus (2019- NCoV) pneumonia. Radiology. 2020;295(1):210- 217. 3. Guo T, Fan Y, Chen M, et al. Cardiovascular implications of fatal outcomes of patients with coronavirus disease 2019 (COVID- 19). JAMA Cardiol. 2020;5(7):848. 4. European Society of Cardiology. ESC guidance for the diagnosis and management of CV disease during the COVID- 19 pandemic. ESC. 2020. 5. Li B, Yang J, Zhao F, et al. Prevalence and impact of cardiovascu-lar metabolic diseases on COVID- 19 in China. Clin Res Cardiol. 2020;109:531- 538. 6. Gottlieb I, Macedo R, Bluemke DA, JA Lima C. Magnetic res-onance imaging in the evaluation of non- ischemic cardiomyopa-thies: Current applications and future perspectives. Hear Fail Rev. 2006;11:313- 323. 7. He D, Ye M, Zhang L, Jiang B. Prognostic significance of late gado-linium enhancement on cardiac magnetic resonance in patients with hypertrophic cardiomyopathy. Hear Lung. 2018;47(2):122- 126. 8. Becker MA, Cornel JH, Van de Ven PM, van Rossum AC, Allaart CPGT. The prognostic value of late gadolinium- enhanced cardiac magnetic resonance imaging in nonischemic dilated cardiomy-opathy: a review and meta- analysis. JACC Cardiovasc Imaging. 2018;11(9):1274- 1284. 9. Luetkens JA, Doerner J, Thomas DK, et al. Acute myo-carditis: Multiparametric cardiac MR imaging. Radiology. 2014;273(2):383- 392. 10. Puntmann VO, Carerj ML, Wieters I, et al. Outcomes of cardio-vascular magnetic resonance imaging in patients recently recov-ered from coronavirus disease 2019 (COVID- 19). JAMA Cardiol. 2020;5(11):1308. 11. Tersalvi G, Vicenzi M, Calabretta D, Biasco L, Pedrazzini GWD. Elevated troponin in patients with Coronavirus Disease 2019 (COVID- 19): possible mechanisms. J Card Fail. 2020;26(6):470- 475. 12. Bikdeli B, Madhavan MV, Jimenez D, et al. COVID- 19 and Thrombotic or Thromboembolic Disease: Implications for Prevention, Antithrombotic Therapy, and Follow- Up. J Am Coll Cardiol. 2020;75(23):2950- 2973. 13. Gravinay P, Issa N, Girard D, Camou FCH. CMR and serology to diagnose COVID- 19 infection with primary cardiac involvement. Eur Hear J Cardiovasc Imaging. 2021;22(1):133.How to cite this article: Rezaeian N, Hosseini L, Asadian S. Cardiac magnetic resonance findings in coronavirus disease 2019. Clin Case Rep. 2021;00:1– 6. https://doi.org/10.1002/ccr3.3972

Cardiac magnetic resonance findings in coronavirus disease 2019

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Cardiac magnetic resonance findings in coronavirus disease 2019

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