Comparison of Cardiac Magnetic Resonance Imaging Findings in COVID-19 Myocarditis and Nonspecific Viral Myocarditis

Comparison of Cardiac Magnetic Resonance Imaging Findings in COVID-19 Myocarditis and Nonspecific Viral Myocarditis | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Comparison of Cardiac Magnetic Resonance Imaging Findings in COVID-19 Myocarditis and Nonspecific Viral Myocarditis Sedat Altay, Kazım Ayberk Sinci, Ezgi Suat Bayraktar, Emre Ozdemir, and 1 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-1662922/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract PURPOSE: This study aimed to compare laboratory, echocardiography, and cardiac magnetic resonance imaging (CMR) findings in patients with coronavirus disease-2019 (COVID-19) associated myocarditis and nonspecific viral myocarditis (NSVM). METHODS: We retrospectively evaluated 25 patients who were considered to have COVID-19-associated myocarditis according to the Lake-Louise criteria and clinical findings. We retrospectively evaluated 41 patients who were accepted as NSVM according to the Lake Louse criteria between January 2016 and March 2020. Late gadolinium enhancement (LGE), ejection fraction, stroke volume, peak ejection rate, and cardiac index data were analyzed for two groups. Echocardiography findings and clinical data were evaluated. Comparisons were made one-way analysis of variance and Student's t-test. RESULTS: LGE was detected in 25 (30%) patients with COVID-19 through CMR examination. LGE was detected most frequently in the inferior segments (mean 2.8 segments) in the patients. Pericardial thickening was observed in 8 (32%) patients. In the NSVM patients, LGE was observed only in the inferior segments in 25 patients, in the lateral–inferior segments in 10 patients, and the septal–inferior segments in 6 patients (mean of 2.4 segments). Pericardial thickening was present in 14 (34%) patients. T2 hyperintensity was not observed. Echocardiography findings were within normal limits in myocarditis groups. There was no statistically significant difference between myocarditis groups' CMR functional data (p = 0.027). CONCLUSION: Functional heart parameters and laboratory findings were similar and normal limits, and no significant difference was observed in imaging features and functional data ​​between NSVM and COVID-19-associated myocarditis. Cardiac magnetic resonance imaging COVID-19 Heart Myocarditis Figures Figure 1 Figure 2 Figure 3 Figure 4 Introduction Nonspecific viral myocarditis (NSVM) is inflammation of the myocardium secondary to viral infection. The clinical presentation of viral myocarditis is very heterogeneous and can range from subclinical nonspecific symptoms of malaise and fatigue to a more severe presentation such as acute cardiogenic shock and, in severe cases, sudden cardiac death. ( 1 – 3 ). In the early days of viral myocarditis, there is edema, necrosis, and myocyte damage due to direct viral spread. The myocardium is usually cleared of the virus within 5 days. Complete tissue and functional recovery usually occur within 3 to 4 weeks. Necrosis and fibrosis occur in severe myocarditis ( 3 ). Endomyocardial biopsy is an invasive procedure and is considered to be the gold standard test to confirm viral myocarditis. However, the sensitivity is low when myocardial involvement is focal. Cardiac imaging hence plays an essential role in the noninvasive evaluation of viral myocarditis ( 4 ). Coronavirus disease-2019 (COVID-19) has been a global epidemic since March 2020. COVID-19 disease due to severe acute respiratory syndrome-coronavirus-2 (SARS-CoV-2) infection has spread to more than 200 countries. The coronavirus attacks tissue through Angiotensin-converting enzyme 2 (ACE2). The lungs and cardiovascular structures are therefore the main organs affected by COVID-19 ( 4 – 8 ). Myocarditis-related problems are an important clinical problem in patients with COVID-19. In the literature, it has been reported that highly sensitive cardiac troponin I (Hs-cTnI), which indicates myocardial damage, is elevated in 12–15% of patients, and cardiac involvement reaches up to 31% in patients with severe COVID-19 ( 9 – 11 ). Clinical information, endomyocardial biopsy (EMB), and cardiac magnetic resonance imaging (CMR) are used in the diagnosis of COVID-19 myocarditis ( 4 , 7 ). This study aimed to compare the laboratory, echocardiography, and CMR imaging features and clinical findings in patients with COVID-19-associated myocarditis and NSVM, and to determine the similarities and differences between the features. Methods The local ethics committee approved this retrospective study and waived the need for informed consent because of the retrospective evaluation of anonymized medical data. All CMR studies were analyzed by a board-certified radiologist with extensive CMR experience (> 9 years). In the NSVM group, clinical, laboratory, and CMR characteristics of 97 patients who were found to have NSVM in routine CMR examination between January 2016 and January 2020 were analyzed retrospectively. Patients were evaluated using CMR, echocardiography, laboratory, and clinical findings. Eighty-three patients with COVID-19 confirmed by polymerase chain reaction (PCR) test who underwent CMR between June 2020 and March 2022 were retrospectively analyzed. The patients were evaluated based on clinical findings, laboratory values, echocardiography, and CMR imaging features. To calculate the range of contact and CMR, we assumed the date of admission to the hospital as the first day of probable COVID-19 diagnosis. Baseline characteristics and hospital treatment details were obtained from patients' medical records. CMR protocols All examinations are planned with standardized image interpretation and post-processing in CMR 2020 update ( 12 ). CMR studies were performed on a 1.5 Tesla scanner (Aera®, Siemens Healthineers, Erlangen, Germany). Patients were scanned with the electrocardiogram (ECG)- triggered using a 16-channel surface phased array of body coils. After standard localizer scan images, breath-hold cine images were acquired in the 2-chamber and 4-chamber views for ventriculus. We administered 0.2 mmol/kg intravenous injection of contrast agents Dotarem (gadoterate meglumine; Guerbet LLC, Villepinte, France). CMR imaging analysis CMR images were acquired from our picture archive system. CMR examinations were evaluated by a radiologist who has a cardiac imaging certificate with extensive CMR experience (> 9 years). Left ventriculi (LV) ejection fraction (EF), stroke volume (SV), mass, and cardiac output (CO) were calculated automatically over functional sequences in multi-sectional 2 and 4 chamber images. Contrast enhancement in late gadolinium enhancement (LGE) images was marked with the AHA 17 segment model. The presence of myocardial fibrosis was analyzed as present or absent regardless of segment size. Myocardial edema was evaluated on short tau inversion recovery (STIR) and T2 weighted image (WI) images. A comparison was made with the muscle tissue included in the section for the presence of myocardial edema. STIR and T2WI signals increased 2 times more than muscle tissue was considered myocardial edema. Current Lake Louise criteria were used for the diagnosis of myocarditis ( 13 ). Laboratory Analysis We obtained laboratory data from the patient information system of our hospital database. We evaluated High-sensitivity cardiac troponin I (Hs-cTnI), and C-reactive protein (CRP). Hs-cTnI levels greater than 3 pg/ml were considered significant. Statistical analysis All statistical analysis was performed using SPSS version 23.0 (IBM statistics, Armonk, New York). Categorical variables were expressed as counts (percentage), and continuous variables as mean ± SD. Qualitative values were reported as percentages. For normally distributed data, the unpaired T-test was used under the non-equal variances condition, and the Wilcoxon test otherwise. Comparison between the 2 groups was performed using an unpaired Student’s t-test (for normal distribution) or Mann-Whitney U test (for non-normal distribution). For all tests, significance was set to p < 0.05. Results A total of 97 patients with nonspecific viral myocarditis (NSVM) according to the Lake Louise criteria were included in the study. 56 of these patients with having hypertension (31), diabetes mellitus ( 12 ), a history of coronary artery disease ( 10 ), and inadequate CMR images ( 3 ) were excluded from the study. As a result, 41 NSVM patients were included in the study, their mean age was 43 years (24–66 years), and 26 of them were women. The reasons for admission were fatigue (35), palpitation (22), rhythm disturbance ( 12 ), dyspnea ( 7 ), and syncope ( 3 ). The time between contact and CMR could not be evaluated because the acute infections of the patients were usually unclear. In the pericardial examination, pericardial thickness increased by an average of 3.4 mm (3–5 mm) in 14 (36%) patients. In NSVM cases, ECG examinations showed bundle branch block in 2 (4%) patients and T inversion in 8 (%19) patients. echocardiography examination revealed minimal hypokinesia in 3 (7%) patients and a diffuse increase in myocardial echogenicity in 2 (4%) patients. Laboratory values were within normal limits. In the CMR examination of 83 patients diagnosed with COVID-19 by PCR, 25 (30%) patients were accepted as probable myocarditis according to the Lake Louise criteria and included in the study. 58 patients CMR had not LGE and other findings are not according to myocarditis. The mean age of the patient was 40.88 years (22–61 years), and seven patients were female (Table). Fifteen patients were treated as inpatients in the hospital. In 13 (52%) hospitalized patients, Hs-cTnI was higher at 18 pg/ml (8–34) on average and CRP at 25 mg/L (8–65) during the acute infection period. Oxygen therapy with a mask was required for an average of 40 hours (10–45 h) in 4 patients. All patients were considered moderately infected with COVID-19, as respiratory and life support were not needed. Remdesivir was used in 22 patients and remdesivir with hydroxychloroquine in 18 patients. Antiviral treatment was not applied to three patients. The reasons for admission after recovery were chest pain ( 17 ), palpitation ( 12 ), dyspnea ( 9 ), and rhythm disturbance ( 5 ). The mean time between contact and CMR was 192,88 days (45–362 days). Concurrent laboratory data with CMR examination were normal in patients. A mean increase of 4.1 mm (3.2–7 mm) was detected in 8 (32%) patients in the pericardium examination in COVID-19 cases. ECG examinations performed simultaneously with CMR revealed ST depression in seven patients and T inversion in two patients. The mean time between contact and echocardiography examination was 175,4 days (35–310 days). Echocardiography examinations and myocardial echoes were normal. No significant pathology was detected in the functional data. Table The CMR characteristics of patients with COVID-19 myocarditis and the time between PCR and CMR are shown in the table. Gender Age (year) LV EF (%) LV SV (ml) LV CO (L/min) LV mass (gr) Number of LGE segments Time between PCR and CMR (day) Male 56 54 78 7 163 1 250 Woman 45 56 86 5,5 123 2 140 Woman 55 49 52 3,8 90 2 210 Woman 45 59 71 5,8 94 2 362 Male 26 49 85 6,3 122 3 260 Male 66 43 87 6,3 155 3 170 Woman 55 38 56 3,7 69 5 180 Male 26 62 106 6,2 144 1 254 Male 45 57 88 5,3 161 2 145 Male 32 59 102 6,6 120 1 124 Male 25 50 87 6,5 131 3 156 Woman 30 55 65 7 96 3 189 Male 61 55 65 4 124 3 231 Male 25 54 101 6,6 156 3 256 Male 32 40 54 3,6 124 5 195 Woman 22 63 63 5 89 1 257 Male 36 52 84 5,8 116 5 167 Male 35 53 99 8,3 163 4 201 Male 56 36 56 3,2 127 2 94 Woman 24 55 68 5,4 102 2 157 Male 54 41 75 7,5 188 3 144 Male 59 35 42 2,7 63 4 282 Male 49 50 80 5,3 137 2 104 Male 22 46 65 6,1 163 3 301 Male 17 58 94 6,1 140 6 45 MEAN 39,92 50,76 76,36 5,584 126,4 2,84 194,96 Abbreviations: Left ventriculi (LV), ejection fraction (EF), stroke volume (SV), cardiac output (CO), polymerase chain reaction (PCR), cardiac magnetic resonance imaging (CMR). On CMR examination on day 45 after diagnosis of COVID-19, an increase in signal consistent with myocarditis was observed in the STIR sequence (Fig. 1 ). In PSIR sequences taken in the late phase, an average of 2.8 LGE for COVID-19 myocarditis was observed (in 1–6 segments) (Fig. 2 , 3 ) and an average of 2.4 (1–7 segments) LGE for NSVM (Fig. 4 ). Involvement of myocardial inferior and septal segments was common in both groups of myocarditis patients. No contraction pathology was observed in the cine images. Heart functional data were similar in both groups compared to the normal group. No statistically significant difference was observed. Constrictive pericarditis was not observed in patients with pericarditis sequela imaging findings. There was no statistical difference between laboratory and CMR data between NSVM and COVID-19 myocarditis patients (p = 0.002). LGE-detected segments were similar in both groups. When the functional data of both groups were compared no statistically significant difference was observed (p = 0.062). Myocarditis cases were compared in terms of cardiac functions, no change was observed in functional data. Myocarditis did not cause a statistically significant deterioration in cardiac functions. Discussion In this study, cases of COVID-19-associated myocarditis and nonspecific viral myocarditis (NSVM) were evaluated in comparison with clinical, laboratory, and imaging findings. In our study, the frequency of myocarditis (25%) in cardiac symptomatic patients with COVID-19 was found to be like that in the literature. When the patients were evaluated together with their CMR, echocardiography, laboratory, and clinical data, no significant difference was observed between the NSVM and COVID-19 myocarditis groups. The segments involved in myocarditis patients were similar. We did not observe a statistically significant difference between the myocarditis groups due to cardiac functional values ​​and preserved systolic functions. Cardiac functional values were normal limits. Our study showed that COVID-19 myocarditis and NSVM imaging and laboratory data were similar; in addition, they did not cause deterioration in cardiac functional values. Huang et al. also found in their study that ventricular functions were preserved in patients with myocarditis ( 9 , 14 ). Fulminant myocarditis secondary to acute COVID-19 shows severe functional deterioration, and left ventricular functions are within normal limits in many studies after recovery ( 9 ). Our study showed the importance of PCR positivity in the diagnosis of COVID-19 since there was no difference between imaging and laboratory data between COVID-19 myocarditis and NSVM. In the differential diagnosis of COVID-19 myocarditis, a PCR test and infection history are required. Caforio et al. defined our current knowledge on the diagnosis and treatment of myocarditis using endomyocardial biopsy (EMB) ( 15 – 17 ). The success of myocarditis treatment depends on the etiologic diagnosis to distinguish between infectious and immune-mediated disease ( 15 , 16 ). Early intervention with intravenous immunoglobulins has been the most effective treatment for inflammatory viral myocarditis. With the COVID-19 pandemic, the coronavirus is an important factor in the etiology of myocarditis. Our study is useful in detecting the etiology of NSVM in CMR examinations. Dilated cardiomyopathy, another possible outcome of myocarditis, also requires an etiologic diagnosis ( 18 ). This study had some limitations. First, the sample size was small. Second, the included patients had moderate COVID-19; therefore, this study does not include severe and critical COVID-19 patients. Possible myocarditis was included in our study because there was no pathological evaluation. One of our clinical limitations was the lack of CMR examination and long-term clinical follow-ups in the acute infection period. Another limitation is the lack of early pandemic hospital cardiac biomarker data in 12 (55%) patients. In addition, patient selection was not unbiased, as all CMR studies were obtained retrospectively and performed with clinical indication. A major limitation was that the CMR examination was performed by a single radiologist. Therefore, the inter and intra-observer reliability could not be evaluated. As seen in the results of our study, COVID-19 myocarditis and NSVM have similar imaging and laboratory data. Cardiac functions were preserved in myocarditis cases and were similar to the normal group. This study should be extended prospectively with EMB data and a larger patient group. Declarations Conflict of interest disclosure The authors declared no conflicts of interest. Financial Support: The authors have no relevant financial information to disclose. Conflict of Interest: The authors have no potential conflicts to disclose. Main points Myocarditis may develop after viral infection and COVID-19. CMR may be important in differentiating between COVID-19-associated myocarditis and other viral myocarditis. Our study examined the effectiveness of using CMR to predict the myocarditis factor. There were no distinctive imaging findings for COVID-19-associated myocarditis. References Leone O, Pieroni M, Rapezzi C, Olivotto I. The spectrum of myocarditis: from pathology to the clinics. Virchows Arch. 2019;475(3):279-301. doi:10.1007/s00428-019-02615-8 Ammirati E, Veronese G, Bottiroli M, et al. Update on acute myocarditis. Trends Cardiovasc Med. 2021;31(6):370-379. doi:10.1016/j.tcm.2020.05.008 Olejniczak M, Schwartz M, Webber E, Shaffer A, Perry TE. Viral Myocarditis-Incidence, Diagnosis and Management. J Cardiothorac Vasc Anesth. 2020;34(6):1591-1601. doi:10.1053/j.jvca.2019.12.052 Friedrich MG, Marcotte F. Cardiac magnetic resonance assessment of myocarditis. Circ Cardiovasc Imaging. 2013;6(5):833-839. doi:10.1161/CIRCIMAGING.113.000416 Tanacli R, Doeblin P, Götze C, et al. COVID-19 vs. Classical Myocarditis Associated Myocardial Injury Evaluated by Cardiac Magnetic Resonance and Endomyocardial Biopsy. Front Cardiovasc Med. 2021;8:737257. Published 2021 Dec 24. doi:10.3389/fcvm.2021.737257. Giustino G, Croft LB, Stefanini GG, et al. Characterization of myocardial injury in patients with COVID-19. J Am Coll Cardiol. (2020) 76:2043–55. doi: 10.1016/j.jacc.2020.08.069 Adeboye A, Alkhatib D, Butt A, Yedlapati N, Garg N. A Review of the Role of Imaging Modalities in the Evaluation of Viral Myocarditis with a Special Focus on COVID-19-Related Myocarditis. Diagnostics (Basel). 2022;12(2):549. Published 2022 Feb 21. doi:10.3390/diagnostics12020549 Huang L, Zhao P, Tang D, et al. Cardiac Involvement in Patients Recovered From COVID-2019 Identified Using Magnetic Resonance Imaging. JACC Cardiovasc Imaging. 2020; 13(11):2330-2339. doi:10.1016/j.jcmg.2020.05.004 Urmeneta Ulloa J, Martínez de Vega V, Salvador Montañés O, et al. Cardiac magnetic resonance in recovering COVID-19 patients. Feature tracking and mapping analysis to detect persistent myocardial involvement. Int J Cardiol Heart Vasc. 2021; 36:100854. doi:10.1016/j.ijcha.2021.100854 Chapman AR, Bularga A, Mills NL. High-Sensitivity Cardiac Troponin Can Be an Ally in the Fight Against COVID-19. Circulation. 2020;141(22):1733-1735. doi:10.1161/CIRCULATIONAHA.120.047008 Wu Z, McGoogan JM. Characteristics of and Important Lessons From the Coronavirus Disease 2019 (COVID-19) Outbreak in China: Summary of a Report of 72 314 Cases From the Chinese Center for Disease Control and Prevention. JAMA. 2020;323(13):1239-1242. doi:10.1001/jama.2020.2648 Kramer CM, Barkhausen J, Bucciarelli-Ducci C, Flamm SD, Kim RJ, Nagel E. Standardized cardiovascular magnetic resonance imaging (CMR) protocols: 2020 update. J Cardiovasc Magn Reason 2020;22:17. Ferreira VM, Schulz-Menger J, Holmvang G, et al. Cardiovascular Magnetic Resonance in Nonischemic Myocardial Inflammation: Expert Recommendations. J Am Coll Cardiol. 2018;72(24):3158-3176. doi:10.1016/j.jacc.2018.09.072 Huang C, Wang Y, Li X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China Lancet. 2020;15:395(10223):497-506. doi: 10.1016/S0140-6736(20)30183-5. Rose NR. Viral myocarditis. Curr Opin Rheumatol. 2016;28(4):383-389. doi:10.1097/BOR.0000000000000303 Reinthaler M, Empen K, Herda LR, et al. The effect of a repeated immunoadsorption in patients with dilated cardiomyopathy after recurrence of severe heart failure symptoms. J Clin Apher. 2015;30(4):217-223. doi:10.1002/jca.21364. Kindermann I, Barth C, Mahfoud F, et al. Update on myocarditis. J Am Coll Cardiol. 2012;59(9):779-792. doi:10.1016/j.jacc.2011.09.074 Pankuweit S, Lüers C, Richter A, Ruppert V, Gelbrich G, Maisch B. Influence of different aetiologies on clinical course and outcome in patients with dilated cardiomyopathy. Eur J Clin Invest. 2015;45(9):906-917. doi:10.1111/eci.12483 Additional Declarations No competing interests reported. Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-1662922","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":107458630,"identity":"ac24b9f5-59a1-4ad9-9b99-191c7e18ad4b","order_by":0,"name":"Sedat Altay","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAA40lEQVRIiWNgGAWjYHACAyC2AGLmAwyMDcRqOcAgIcHAwJZAshYeA+K0yLc3b/z8oUaijn9GzjeJnzts5BjYDx/dgNeKM8eKJQ4ck5CQuJG7TbL3TJoxA09a2g28WiRyDCQOsAEdBtQiwdt2OLFBgscMrxb5+W+Mfxz4JyEhfyPnmeRfYrQw3OAxkzjYJiFhcCOHTZooWwzOpJVZnO2TkNx45pmxtWxbmjEbIb/Itx/efKPimw2/3PHkhzffttnI8bMfPobfYXAgkMAiAaLZiFMOAvwHmD8Qr3oUjIJRMApGEgAAxO1M1Yvt0qEAAAAASUVORK5CYII=","orcid":"","institution":"Izmir Kâtip Çelebi University","correspondingAuthor":true,"submittingAuthor":false,"prefix":"","firstName":"Sedat","middleName":"","lastName":"Altay","suffix":""},{"id":107458631,"identity":"09747e3c-e452-49e3-9fe8-cb7883393582","order_by":1,"name":"Kazım Ayberk Sinci","email":"","orcid":"","institution":"Izmir Kâtip Çelebi University","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Kazım","middleName":"Ayberk","lastName":"Sinci","suffix":""},{"id":107458632,"identity":"d95fb2c0-417e-4dc7-a8f1-bd9af9434105","order_by":2,"name":"Ezgi Suat Bayraktar","email":"","orcid":"","institution":"Izmir Kâtip Çelebi University","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Ezgi","middleName":"Suat","lastName":"Bayraktar","suffix":""},{"id":107458636,"identity":"64eead86-509f-4d98-9dbf-9af245a926bc","order_by":3,"name":"Emre Ozdemir","email":"","orcid":"","institution":"Izmir Kâtip Çelebi University","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Emre","middleName":"","lastName":"Ozdemir","suffix":""},{"id":107458637,"identity":"4c9da7de-3a05-488e-9427-2f5bb5bd7eef","order_by":4,"name":"Cesur Gümüş","email":"","orcid":"","institution":"Izmir Kâtip Çelebi University","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Cesur","middleName":"","lastName":"Gümüş","suffix":""}],"badges":[],"createdAt":"2022-05-16 20:44:13","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-1662922/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-1662922/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":21878936,"identity":"4dde2c1c-1222-4e73-b1f2-2fae1832aaa9","added_by":"auto","created_at":"2022-05-25 16:05:23","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":754759,"visible":true,"origin":"","legend":"\u003cp\u003e25-year-old male post-COVID-19 patient with myocarditis. on the 45th day after PCR positivity, myocarditis is showing on the left ventricular lateral wall in 2 chamber 2D-phase-sensitive-inversion-recovery (2D-PSIR) (a), and 4 chamber PSIR (b) images in the CMR examination. (arrows). 4 chamber Short-tau-inversion-recovery (STIR) (c) and 4 chambers Steady-state free precession (SSFP) (d) images show regional myocardial edema (arrows).\u003c/p\u003e\u003cp\u003e\u003cbr\u003e\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-1662922/v1/7633139a098190a8c6789eda.png"},{"id":21878937,"identity":"88d78099-5374-4812-8a85-c78cf08a301f","added_by":"auto","created_at":"2022-05-25 16:05:24","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":261907,"visible":true,"origin":"","legend":"\u003cp\u003e2-chamber PSIR images show mid myocardial late gadolinium contrast (LGE) in the interventricular septum (A) in a 52-year-old man (a) and a 60-year-old woman (b) with COVID-19-associated myocarditis (arrows). (arrows).\u003c/p\u003e\u003cp\u003e\u003cbr\u003e\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-1662922/v1/dac9a573f5d9177fcc1dabf1.png"},{"id":21878129,"identity":"7b80a7fd-78c8-42ec-b4ef-a57d8d887c3f","added_by":"auto","created_at":"2022-05-25 16:00:23","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":143147,"visible":true,"origin":"","legend":"\u003cp\u003eFocal late gadolinium potentiation (LGE) was observed in 2-chamber PSIR images in cases of a 43-year-old female (a) and 30-year-old male (b) with COVID-19-associated myocarditis (arrows).\u003c/p\u003e\u003cp\u003e\u003cbr\u003e\u003c/p\u003e","description":"","filename":"3.png","url":"https://assets-eu.researchsquare.com/files/rs-1662922/v1/e5a77fabb00c550aa4bdbcaf.png"},{"id":21878131,"identity":"43392471-a49e-440c-91de-8bf4bbf74611","added_by":"auto","created_at":"2022-05-25 16:00:24","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":254538,"visible":true,"origin":"","legend":"\u003cp\u003e2-chamber PSIR sequences of a 43-year-old female (a) and a 30-year-old man (b) NSVM patients show focal late gadolinium potentiation (LGE) in the septum which non-ischemic myocardial injury (arrows).\u003c/p\u003e\u003cp\u003e\u003cbr\u003e\u003c/p\u003e","description":"","filename":"4.png","url":"https://assets-eu.researchsquare.com/files/rs-1662922/v1/bce407d6c162a071a9a808a8.png"},{"id":21878939,"identity":"1065ec88-f1f2-4a94-87bc-3acfc14e91ce","added_by":"auto","created_at":"2022-05-25 16:05:27","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1274426,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-1662922/v1/6c061077-ab2b-4912-9cf4-763c2b57caf4.pdf"},{"id":21878938,"identity":"5399b350-2c38-4974-9b18-1c8e0c59d089","added_by":"auto","created_at":"2022-05-25 16:05:26","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":591220,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-1662922/v1/4a60f63d-3203-4777-b9e8-d99698ac0bf1.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Comparison of Cardiac Magnetic Resonance Imaging Findings in COVID-19 Myocarditis and Nonspecific Viral Myocarditis","fulltext":[{"header":"Introduction","content":"\u003cp\u003eNonspecific viral myocarditis (NSVM) is inflammation of the myocardium secondary to viral infection. The clinical presentation of viral myocarditis is very heterogeneous and can range from subclinical nonspecific symptoms of malaise and fatigue to a more severe presentation such as acute cardiogenic shock and, in severe cases, sudden cardiac death. (\u003cspan additionalcitationids=\"CR2\" citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e). In the early days of viral myocarditis, there is edema, necrosis, and myocyte damage due to direct viral spread. The myocardium is usually cleared of the virus within 5 days. Complete tissue and functional recovery usually occur within 3 to 4 weeks. Necrosis and fibrosis occur in severe myocarditis (\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e). Endomyocardial biopsy is an invasive procedure and is considered to be the gold standard test to confirm viral myocarditis. However, the sensitivity is low when myocardial involvement is focal. Cardiac imaging hence plays an essential role in the noninvasive evaluation of viral myocarditis (\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eCoronavirus disease-2019 (COVID-19) has been a global epidemic since March 2020. COVID-19 disease due to severe acute respiratory syndrome-coronavirus-2 (SARS-CoV-2) infection has spread to more than 200 countries. The coronavirus attacks tissue through Angiotensin-converting enzyme 2 (ACE2). The lungs and cardiovascular structures are therefore the main organs affected by COVID-19 (\u003cspan additionalcitationids=\"CR5 CR6 CR7\" citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e). Myocarditis-related problems are an important clinical problem in patients with COVID-19. In the literature, it has been reported that highly sensitive cardiac troponin I (Hs-cTnI), which indicates myocardial damage, is elevated in 12\u0026ndash;15% of patients, and cardiac involvement reaches up to 31% in patients with severe COVID-19 (\u003cspan additionalcitationids=\"CR10\" citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e). Clinical information, endomyocardial biopsy (EMB), and cardiac magnetic resonance imaging (CMR) are used in the diagnosis of COVID-19 myocarditis (\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e, \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThis study aimed to compare the laboratory, echocardiography, and CMR imaging features and clinical findings in patients with COVID-19-associated myocarditis and NSVM, and to determine the similarities and differences between the features.\u003c/p\u003e"},{"header":"Methods","content":"\u003cp\u003eThe local ethics committee approved this retrospective study and waived the need for informed consent because of the retrospective evaluation of anonymized medical data. All CMR studies were analyzed by a board-certified radiologist with extensive CMR experience (\u0026gt;\u0026thinsp;9 years).\u003c/p\u003e\n\u003cp\u003eIn the NSVM group, clinical, laboratory, and CMR characteristics of 97 patients who were found to have NSVM in routine CMR examination between January 2016 and January 2020 were analyzed retrospectively. Patients were evaluated using CMR, echocardiography, laboratory, and clinical findings.\u003c/p\u003e\n\u003cp\u003eEighty-three patients with COVID-19 confirmed by polymerase chain reaction (PCR) test who underwent CMR between June 2020 and March 2022 were retrospectively analyzed. The patients were evaluated based on clinical findings, laboratory values, echocardiography, and CMR imaging features. To calculate the range of contact and CMR, we assumed the date of admission to the hospital as the first day of probable COVID-19 diagnosis. Baseline characteristics and hospital treatment details were obtained from patients\u0026apos; medical records.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCMR protocols\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAll examinations are planned with standardized image interpretation and post-processing in CMR 2020 update (\u003cspan class=\"CitationRef\"\u003e12\u003c/span\u003e). CMR studies were performed on a 1.5 Tesla scanner (Aera\u0026reg;, Siemens Healthineers, Erlangen, Germany). Patients were scanned with the electrocardiogram (ECG)- triggered using a 16-channel surface phased array of body coils. After standard localizer scan images, breath-hold cine images were acquired in the 2-chamber and 4-chamber views for ventriculus. We administered 0.2 mmol/kg intravenous injection of contrast agents Dotarem (gadoterate meglumine; Guerbet LLC, Villepinte, France).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCMR imaging analysis\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eCMR images were acquired from our picture archive system. CMR examinations were evaluated by a radiologist who has a cardiac imaging certificate with extensive CMR experience (\u0026gt;\u0026thinsp;9 years). Left ventriculi (LV) ejection fraction (EF), stroke volume (SV), mass, and cardiac output (CO) were calculated automatically over functional sequences in multi-sectional 2 and 4 chamber images. Contrast enhancement in late gadolinium enhancement (LGE) images was marked with the AHA 17 segment model. The presence of myocardial fibrosis was analyzed as present or absent regardless of segment size. Myocardial edema was evaluated on short tau inversion recovery (STIR) and T2 weighted image (WI) images. A comparison was made with the muscle tissue included in the section for the presence of myocardial edema. STIR and T2WI signals increased 2 times more than muscle tissue was considered myocardial edema. Current Lake Louise criteria were used for the diagnosis of myocarditis (\u003cspan class=\"CitationRef\"\u003e13\u003c/span\u003e).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eLaboratory Analysis\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eWe obtained laboratory data from the patient information system of our hospital database. We evaluated High-sensitivity cardiac troponin I (Hs-cTnI), and C-reactive protein (CRP). Hs-cTnI levels greater than 3 pg/ml were considered significant.\u003c/p\u003e\n\u003cdiv class=\"Section2\" id=\"Sec3\"\u003e\n \u003ch2\u003eStatistical analysis\u003c/h2\u003e\n \u003cp\u003eAll statistical analysis was performed using SPSS version 23.0 (IBM statistics, Armonk, New York). Categorical variables were expressed as counts (percentage), and continuous variables as mean\u0026thinsp;\u0026plusmn;\u0026thinsp;SD. Qualitative values were reported as percentages. For normally distributed data, the unpaired T-test was used under the non-equal variances condition, and the Wilcoxon test otherwise. Comparison between the 2 groups was performed using an unpaired Student\u0026rsquo;s t-test (for normal distribution) or Mann-Whitney U test (for non-normal distribution). For all tests, significance was set to p\u0026thinsp;\u0026lt;\u0026thinsp;0.05.\u003c/p\u003e\n\u003c/div\u003e"},{"header":"Results","content":"\u003cp\u003eA total of 97 patients with nonspecific viral myocarditis (NSVM) according to the Lake Louise criteria were included in the study. 56 of these patients with having hypertension (31), diabetes mellitus (\u003cspan class=\"CitationRef\"\u003e12\u003c/span\u003e), a history of coronary artery disease (\u003cspan class=\"CitationRef\"\u003e10\u003c/span\u003e), and inadequate CMR images (\u003cspan class=\"CitationRef\"\u003e3\u003c/span\u003e) were excluded from the study. As a result, 41 NSVM patients were included in the study, their mean age was 43 years (24\u0026ndash;66 years), and 26 of them were women. The reasons for admission were fatigue (35), palpitation (22), rhythm disturbance (\u003cspan class=\"CitationRef\"\u003e12\u003c/span\u003e), dyspnea (\u003cspan class=\"CitationRef\"\u003e7\u003c/span\u003e), and syncope (\u003cspan class=\"CitationRef\"\u003e3\u003c/span\u003e). The time between contact and CMR could not be evaluated because the acute infections of the patients were usually unclear. In the pericardial examination, pericardial thickness increased by an average of 3.4 mm (3\u0026ndash;5 mm) in 14 (36%) patients. In NSVM cases, ECG examinations showed bundle branch block in 2 (4%) patients and T inversion in 8 (%19) patients. echocardiography examination revealed minimal hypokinesia in 3 (7%) patients and a diffuse increase in myocardial echogenicity in 2 (4%) patients. Laboratory values were within normal limits.\u003c/p\u003e\n\u003cp\u003eIn the CMR examination of 83 patients diagnosed with COVID-19 by PCR, 25 (30%) patients were accepted as probable myocarditis according to the Lake Louise criteria and included in the study. 58 patients CMR had not LGE and other findings are not according to myocarditis. The mean age of the patient was 40.88 years (22\u0026ndash;61 years), and seven patients were female (Table). Fifteen patients were treated as inpatients in the hospital. In 13 (52%) hospitalized patients, Hs-cTnI was higher at 18 pg/ml (8\u0026ndash;34) on average and CRP at 25 mg/L (8\u0026ndash;65) during the acute infection period. Oxygen therapy with a mask was required for an average of 40 hours (10\u0026ndash;45 h) in 4 patients. All patients were considered moderately infected with COVID-19, as respiratory and life support were not needed. Remdesivir was used in 22 patients and remdesivir with hydroxychloroquine in 18 patients. Antiviral treatment was not applied to three patients. The reasons for admission after recovery were chest pain (\u003cspan class=\"CitationRef\"\u003e17\u003c/span\u003e), palpitation (\u003cspan class=\"CitationRef\"\u003e12\u003c/span\u003e), dyspnea (\u003cspan class=\"CitationRef\"\u003e9\u003c/span\u003e), and rhythm disturbance (\u003cspan class=\"CitationRef\"\u003e5\u003c/span\u003e). The mean time between contact and CMR was 192,88 days (45\u0026ndash;362 days). Concurrent laboratory data with CMR examination were normal in patients. A mean increase of 4.1 mm (3.2\u0026ndash;7 mm) was detected in 8 (32%) patients in the pericardium examination in COVID-19 cases. ECG examinations performed simultaneously with CMR revealed ST depression in seven patients and T inversion in two patients. The mean time between contact and echocardiography examination was 175,4 days (35\u0026ndash;310 days). Echocardiography examinations and myocardial echoes were normal. No significant pathology was detected in the functional data.\u003c/p\u003e\n\u003cp style=\"text-align: center;\"\u003eTable\u003c/p\u003e\n\u003cp style=\"text-align: center;\"\u003e\u0026nbsp;The CMR characteristics of patients with COVID-19 myocarditis and the time between PCR and CMR are shown in the table.\u003c/p\u003e\n\u003cdiv align=\"center\"\u003e\n \u003ctable border=\"1\" cellpadding=\"0\" cellspacing=\"0\" width=\"0\"\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003eGender\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003eAge (year)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"14.6875%\"\u003e\n \u003cp\u003eLV EF (%)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003eLV SV (ml)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003eLV CO (L/min)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003eLV mass (gr)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003eNumber of LGE segments\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003eTime between PCR and CMR (day)\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003eMale\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e56\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"14.6875%\"\u003e\n \u003cp\u003e54\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e78\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e7\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e163\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e1\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e250\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"12.1875%\"\u003e\n \u003cp\u003eWoman\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e45\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"14.6875%\"\u003e\n \u003cp\u003e56\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e86\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e5,5\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e123\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e2\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e140\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"12.1875%\"\u003e\n \u003cp\u003eWoman\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e55\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"14.6875%\"\u003e\n \u003cp\u003e49\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e52\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e3,8\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e90\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e2\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e210\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd valign=\"top\" width=\"12.1875%\"\u003e\n \u003cp\u003eWoman\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e45\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"14.6875%\"\u003e\n \u003cp\u003e59\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e71\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e5,8\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e94\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e2\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e362\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003eMale\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e26\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"14.6875%\"\u003e\n \u003cp\u003e49\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e85\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e6,3\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e122\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e3\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e260\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003eMale\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e66\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"14.6875%\"\u003e\n \u003cp\u003e43\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e87\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e6,3\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e155\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e3\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e170\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003eWoman\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e55\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"14.6875%\"\u003e\n \u003cp\u003e38\u003c/p\u003e\n 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width=\"12.1875%\"\u003e\n \u003cp\u003e25\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"14.6875%\"\u003e\n \u003cp\u003e54\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e101\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e6,6\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e156\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e3\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e256\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003eMale\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e32\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"14.6875%\"\u003e\n \u003cp\u003e40\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e54\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e3,6\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e124\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e5\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e195\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003eWoman\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e22\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"14.6875%\"\u003e\n \u003cp\u003e63\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e63\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e5\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e89\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e1\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e257\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003eMale\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e36\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"14.6875%\"\u003e\n \u003cp\u003e52\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e84\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e5,8\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e116\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e5\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e167\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003eMale\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e35\u003c/p\u003e\n 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width=\"12.1875%\"\u003e\n \u003cp\u003eMale\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e17\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"14.6875%\"\u003e\n \u003cp\u003e58\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e94\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e6,1\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e140\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e6\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e45\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003eMEAN\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e39,92\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"14.6875%\"\u003e\n \u003cp\u003e50,76\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e76,36\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e5,584\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e126,4\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e2,84\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"12.1875%\"\u003e\n \u003cp\u003e194,96\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n \u003c/table\u003e\n\u003c/div\u003e\n\u003cp\u003e\u0026nbsp;Abbreviations: Left ventriculi (LV), ejection fraction (EF), stroke volume (SV), cardiac output (CO), polymerase chain reaction (PCR), cardiac magnetic resonance imaging (CMR).\u003c/p\u003e\n\u003cp\u003eOn CMR examination on day 45 after diagnosis of COVID-19, an increase in signal consistent with myocarditis was observed in the STIR sequence (Fig. \u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e). In PSIR sequences taken in the late phase, an average of 2.8 LGE for COVID-19 myocarditis was observed (in 1\u0026ndash;6 segments) (Fig. \u003cspan class=\"InternalRef\"\u003e2\u003c/span\u003e,\u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003e) and an average of 2.4 (1\u0026ndash;7 segments) LGE for NSVM (Fig. \u003cspan class=\"InternalRef\"\u003e4\u003c/span\u003e). Involvement of myocardial inferior and septal segments was common in both groups of myocarditis patients. No contraction pathology was observed in the cine images. Heart functional data were similar in both groups compared to the normal group. No statistically significant difference was observed. Constrictive pericarditis was not observed in patients with pericarditis sequela imaging findings.\u003c/p\u003e\n\u003cp\u003eThere was no statistical difference between laboratory and CMR data between NSVM and COVID-19 myocarditis patients (p\u0026thinsp;=\u0026thinsp;0.002). LGE-detected segments were similar in both groups. When the functional data of both groups were compared no statistically significant difference was observed (p\u0026thinsp;=\u0026thinsp;0.062). Myocarditis cases were compared in terms of cardiac functions, no change was observed in functional data. Myocarditis did not cause a statistically significant deterioration in cardiac functions.\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eIn this study, cases of COVID-19-associated myocarditis and nonspecific viral myocarditis (NSVM) were evaluated in comparison with clinical, laboratory, and imaging findings. In our study, the frequency of myocarditis (25%) in cardiac symptomatic patients with COVID-19 was found to be like that in the literature. When the patients were evaluated together with their CMR, echocardiography, laboratory, and clinical data, no significant difference was observed between the NSVM and COVID-19 myocarditis groups. The segments involved in myocarditis patients were similar. We did not observe a statistically significant difference between the myocarditis groups due to cardiac functional values ​​and preserved systolic functions. Cardiac functional values were normal limits. Our study showed that COVID-19 myocarditis and NSVM imaging and laboratory data were similar; in addition, they did not cause deterioration in cardiac functional values.\u003c/p\u003e \u003cp\u003eHuang et al. also found in their study that ventricular functions were preserved in patients with myocarditis (\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e, \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e). Fulminant myocarditis secondary to acute COVID-19 shows severe functional deterioration, and left ventricular functions are within normal limits in many studies after recovery (\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e). Our study showed the importance of PCR positivity in the diagnosis of COVID-19 since there was no difference between imaging and laboratory data between COVID-19 myocarditis and NSVM. In the differential diagnosis of COVID-19 myocarditis, a PCR test and infection history are required.\u003c/p\u003e \u003cp\u003eCaforio et al. defined our current knowledge on the diagnosis and treatment of myocarditis using endomyocardial biopsy (EMB) (\u003cspan additionalcitationids=\"CR16\" citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e). The success of myocarditis treatment depends on the etiologic diagnosis to distinguish between infectious and immune-mediated disease (\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e, \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e). Early intervention with intravenous immunoglobulins has been the most effective treatment for inflammatory viral myocarditis. With the COVID-19 pandemic, the coronavirus is an important factor in the etiology of myocarditis. Our study is useful in detecting the etiology of NSVM in CMR examinations. Dilated cardiomyopathy, another possible outcome of myocarditis, also requires an etiologic diagnosis (\u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThis study had some limitations. First, the sample size was small. Second, the included patients had moderate COVID-19; therefore, this study does not include severe and critical COVID-19 patients. Possible myocarditis was included in our study because there was no pathological evaluation. One of our clinical limitations was the lack of CMR examination and long-term clinical follow-ups in the acute infection period. Another limitation is the lack of early pandemic hospital cardiac biomarker data in 12 (55%) patients. In addition, patient selection was not unbiased, as all CMR studies were obtained retrospectively and performed with clinical indication. A major limitation was that the CMR examination was performed by a single radiologist. Therefore, the inter and intra-observer reliability could not be evaluated.\u003c/p\u003e \u003cp\u003eAs seen in the results of our study, COVID-19 myocarditis and NSVM have similar imaging and laboratory data. Cardiac functions were preserved in myocarditis cases and were similar to the normal group. This study should be extended prospectively with EMB data and a larger patient group.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eConflict of interest disclosure\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors declared no conflicts of interest.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFinancial Support:\u003c/strong\u003e\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eThe authors have no relevant financial information to disclose.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConflict of Interest:\u003c/strong\u003e\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eThe authors have no potential conflicts to disclose.\u003c/p\u003e"},{"header":"Main points","content":"\u003cul\u003e\n \u003cli\u003eMyocarditis may develop after viral infection and COVID-19. CMR may be important in differentiating between COVID-19-associated myocarditis and other viral myocarditis.\u003c/li\u003e\n \u003cli\u003eOur study examined the effectiveness of using CMR to predict the myocarditis factor.\u003c/li\u003e\n \u003cli\u003eThere were no distinctive imaging findings for COVID-19-associated myocarditis.\u003c/li\u003e\n\u003c/ul\u003e"},{"header":"References","content":"\u003col\u003e\n \u003cli\u003eLeone O, Pieroni M, Rapezzi C, Olivotto I. The spectrum of myocarditis: from pathology to the clinics. Virchows Arch. 2019;475(3):279-301. doi:10.1007/s00428-019-02615-8\u003c/li\u003e\n \u003cli\u003eAmmirati E, Veronese G, Bottiroli M, et al. Update on acute myocarditis. Trends Cardiovasc Med. 2021;31(6):370-379. doi:10.1016/j.tcm.2020.05.008\u003c/li\u003e\n \u003cli\u003eOlejniczak M, Schwartz M, Webber E, Shaffer A, Perry TE. Viral Myocarditis-Incidence, Diagnosis and Management. J Cardiothorac Vasc Anesth. 2020;34(6):1591-1601. doi:10.1053/j.jvca.2019.12.052\u0026nbsp;\u003c/li\u003e\n \u003cli\u003eFriedrich MG, Marcotte F. Cardiac magnetic resonance assessment of myocarditis. Circ Cardiovasc Imaging. 2013;6(5):833-839. doi:10.1161/CIRCIMAGING.113.000416\u003c/li\u003e\n \u003cli\u003eTanacli R, Doeblin P, G\u0026ouml;tze C, et al. COVID-19 vs. Classical Myocarditis Associated Myocardial Injury Evaluated by Cardiac Magnetic Resonance and Endomyocardial Biopsy. Front Cardiovasc Med. 2021;8:737257. Published 2021 Dec 24. doi:10.3389/fcvm.2021.737257.\u0026nbsp;\u003c/li\u003e\n \u003cli\u003eGiustino G, Croft LB, Stefanini GG, et al. Characterization of myocardial injury in patients with COVID-19. J Am Coll Cardiol. (2020) 76:2043\u0026ndash;55. doi: 10.1016/j.jacc.2020.08.069\u003c/li\u003e\n \u003cli\u003eAdeboye A, Alkhatib D, Butt A, Yedlapati N, Garg N. A Review of the Role of Imaging Modalities in the Evaluation of Viral Myocarditis with a Special Focus on COVID-19-Related Myocarditis.\u0026nbsp;Diagnostics (Basel). 2022;12(2):549. Published 2022 Feb 21. doi:10.3390/diagnostics12020549\u003c/li\u003e\n \u003cli\u003eHuang L, Zhao P, Tang D, et al. Cardiac Involvement in Patients Recovered From COVID-2019 Identified Using Magnetic Resonance Imaging. JACC Cardiovasc Imaging. 2020; 13(11):2330-2339. doi:10.1016/j.jcmg.2020.05.004\u003c/li\u003e\n \u003cli\u003eUrmeneta Ulloa J, Mart\u0026iacute;nez de Vega V, Salvador Monta\u0026ntilde;\u0026eacute;s O, et al. Cardiac magnetic resonance in recovering COVID-19 patients. Feature tracking and mapping analysis to detect persistent myocardial involvement. Int J Cardiol Heart Vasc. 2021; 36:100854. doi:10.1016/j.ijcha.2021.100854\u003c/li\u003e\n \u003cli\u003eChapman AR, Bularga A, Mills NL. High-Sensitivity Cardiac Troponin Can Be an Ally in the Fight Against COVID-19. Circulation. 2020;141(22):1733-1735. doi:10.1161/CIRCULATIONAHA.120.047008\u003c/li\u003e\n \u003cli\u003eWu Z, McGoogan JM. Characteristics of and Important Lessons From the Coronavirus Disease 2019 (COVID-19) Outbreak in China: Summary of a Report of 72 314 Cases From the Chinese Center for Disease Control and Prevention.\u0026nbsp;JAMA. 2020;323(13):1239-1242. doi:10.1001/jama.2020.2648\u0026nbsp;\u003c/li\u003e\n \u003cli\u003eKramer CM, Barkhausen J, Bucciarelli-Ducci C, Flamm SD, Kim RJ, Nagel E. Standardized cardiovascular magnetic resonance imaging (CMR) protocols: 2020 update. J Cardiovasc Magn Reason 2020;22:17.\u003c/li\u003e\n \u003cli\u003eFerreira VM, Schulz-Menger J, Holmvang G, et al. Cardiovascular Magnetic Resonance in Nonischemic Myocardial Inflammation: Expert Recommendations. J Am Coll Cardiol. 2018;72(24):3158-3176. doi:10.1016/j.jacc.2018.09.072\u0026nbsp;\u003c/li\u003e\n \u003cli\u003eHuang C, Wang Y, Li X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China Lancet. 2020;15:395(10223):497-506. doi: 10.1016/S0140-6736(20)30183-5.\u003c/li\u003e\n \u003cli\u003eRose NR. Viral myocarditis. Curr Opin Rheumatol. 2016;28(4):383-389. doi:10.1097/BOR.0000000000000303\u003c/li\u003e\n \u003cli\u003eReinthaler M, Empen K, Herda LR, et al. The effect of a repeated immunoadsorption in patients with dilated cardiomyopathy after recurrence of severe heart failure symptoms. J Clin Apher. 2015;30(4):217-223. doi:10.1002/jca.21364.\u003c/li\u003e\n \u003cli\u003eKindermann I, Barth C, Mahfoud F, et al. Update on myocarditis. J Am Coll Cardiol. 2012;59(9):779-792. doi:10.1016/j.jacc.2011.09.074\u003c/li\u003e\n \u003cli\u003ePankuweit S, L\u0026uuml;ers C, Richter A, Ruppert V, Gelbrich G, Maisch B. Influence of different aetiologies on clinical course and outcome in patients with dilated cardiomyopathy. Eur J Clin Invest. 2015;45(9):906-917. doi:10.1111/eci.12483\u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"Cardiac magnetic resonance imaging, COVID-19, Heart, Myocarditis","lastPublishedDoi":"10.21203/rs.3.rs-1662922/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-1662922/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003e\u003cstrong\u003ePURPOSE: \u003c/strong\u003eThis study aimed to compare laboratory, echocardiography, and cardiac magnetic resonance imaging (CMR) findings in patients with coronavirus disease-2019 (COVID-19) associated myocarditis and nonspecific viral myocarditis (NSVM).\u003c/p\u003e\u003cp\u003e\u003cstrong\u003eMETHODS:\u003c/strong\u003e We retrospectively evaluated 25 patients who were considered to have COVID-19-associated myocarditis according to the Lake-Louise criteria and clinical findings. We retrospectively evaluated 41 patients who were accepted as NSVM according to the Lake Louse criteria between January 2016 and March 2020. Late gadolinium enhancement (LGE), ejection fraction, stroke volume, peak ejection rate, and cardiac index data were analyzed for two groups. Echocardiography findings and clinical data were evaluated. Comparisons were made one-way analysis of variance and Student's t-test.\u003c/p\u003e\u003cp\u003e\u003cstrong\u003eRESULTS:\u003c/strong\u003e LGE was detected in 25 (30%) patients with COVID-19 through CMR examination. LGE was detected most frequently in the inferior segments (mean 2.8 segments) in the patients. Pericardial thickening was observed in 8 (32%) patients. In the NSVM patients, LGE was observed only in the inferior segments in 25 patients, in the lateral–inferior segments in 10 patients, and the septal–inferior segments in 6 patients (mean of 2.4 segments). Pericardial thickening was present in 14 (34%) patients. T2 hyperintensity was not observed. Echocardiography findings were within normal limits in myocarditis groups. There was no statistically significant difference between myocarditis groups' CMR functional data (p = 0.027).\u003c/p\u003e\u003cp\u003e\u003cstrong\u003eCONCLUSION:\u003c/strong\u003e Functional heart parameters and laboratory findings were similar and normal limits, and no significant difference was observed in imaging features and functional data ​​between NSVM and COVID-19-associated myocarditis.\u0026nbsp;\u003c/p\u003e","manuscriptTitle":"Comparison of Cardiac Magnetic Resonance Imaging Findings in COVID-19 Myocarditis and Nonspecific Viral Myocarditis","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2022-05-25 16:00:21","doi":"10.21203/rs.3.rs-1662922/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"b14badd9-b114-4d04-b584-acf4a796b973","owner":[],"postedDate":"May 25th, 2022","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2022-05-25T16:05:23+00:00","versionOfRecord":[],"versionCreatedAt":"2022-05-25 16:00:21","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-1662922","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-1662922","identity":"rs-1662922","version":["v1"]},"buildId":"7rjqhiLT3MXkJMwkYKINL","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}