The Cleveland Clinic experience of eosinophilic myocarditis in the setting of hypereosinophilic syndrome: demographics, cardiac imaging, and outcomes

Introduction

Hypereosinophilic syndrome (HES) is a heterogenous group of rare disorders distinguished by sustained peripheral or tissue hypereosinophilia (HE) with concurrent evidence of eosinophil-mediated organ damage (1). HES was first proposed by Chusid et al. in 1975 (2). At the 2021 Working Conference on Eosinophil Disorders and Syndromes, the following criteria for HE and HES were recommended (3). HE could be diagnosed if absolute eosinophil count (AEC) is >1.5×10⁴/µL on two examinations at least 2 weeks apart; and HES could be diagnosed if there is organ damage attributed to HE (3). It was also suggested when HE is not present, tissue HE could be diagnosed if the following conditions are met: (I) the percentage of eosinophils exceeds 20% of all nucleated cells in bone marrow sections; (II) a pathologist is of the opinion that tissue infiltration by eosinophils is extensive compared with “normal physiologic ranges”; or (III) immunostaining reveals marked deposition of eosinophil granule proteins (3). This was found to be limiting as multiple patients demonstrated organ involvement with only a mild blood eosinophil count. HES is a rare disease with limited contemporary data. A study surveyed in the United Kingdom between 2010 and 2018 utilizing HES diagnostic codes estimated an annual incidence of 0.04 to 0.17 cases per 100,000 and a total prevalence of 0.15 to 0.89 per 100,000 persons (4). The causative etiologies of HES include myeloproliferative diseases, Churg-Strauss syndrome (5), and parasitic infections (6). The most common type of HES is idiopathic (7) and parasitic infections are common in developing countries (6). There have also been reports of HES triggered by coronavirus disease 2019 (COVID-19) infection (8).

Activated eosinophils sometimes infiltrate into the myocardium and cause eosinophilic myocarditis (EM). EM has been divided into three stages: an acute necrotic stage, a thrombotic stage and a fibrotic stage (9). Loeffler’s endocarditis is characterized by chronic progressive disease with lesions in the endocardium, and is classified as the thrombotic and fibrotic stage (10). Endomyocardial thickening, mural thrombosis, and features of restrictive cardiomyopathy can be appreciated as the disease progresses due to activation of the coagulation system or fibrosis (11). Szczerba et al. reported that a mass lesion associated with EM invaded the mitral valve and exacerbated valvular disease (12). Estimates regarding the rate of cardiovascular involvement in HES vary widely with some studies estimating involvement in up to 60% of cases (13-15). Currently, there is a lack of universal consensus on the optimal diagnostic workup for cardiac involvement in HES (16). EM is definitively diagnosed by endomyocardial biopsy (EMB), but clinicians often could make a diagnosis based on laboratory parameters and cardiac imaging findings in the context of appropriate clinical presentation (17). Endomyocardial wall thickening and left ventricular (LV) thrombus are the more suggestive findings of the disease (16,18), though these findings are non-specific for EM and should be evaluated in detail, according to the clinical presentation of each patient. Cardiac magnetic resonance (CMR) imaging is the gold standard for noninvasive diagnosis of myocarditis, but descriptions of suggestive findings in HES are even more limited (19). Much of the literature available describing the cardiac involvement of HES is restricted to individual case reports or small systematic reviews of varying populations (17,20-22). Therefore, we aim to report a contemporary single-center experience of the clinical characteristics, cardiac imaging evaluation, management strategies, and patient outcomes of this rare disease process. We present this article in accordance with the STROBE reporting checklist (available at https://cdt.amegroups.com/article/view/10.21037/cdt-24-347/rc).

Methods

Study design and setting

This is a single-center cross-sectional study performed at a quaternary referral center in the United States. The institutional electronic medical record was queried to identify all echocardiograms performed at our center between September 1986 and January 2023 with the associated ICD-10 code (D72.1) for eosinophilia. We included patients with HES diagnosed by reference to the 2021 HES consensus document (3). Exclusion criteria were patients younger than 18 years of age. Data regarding clinical presentation, medical history, medication use, comorbidities, management strategies, imaging, hospital course, cardiac imaging studies, laboratory data, and demographics were collected. Echocardiography and CMR databases were reviewed to obtain the relevant imaging data. Follow-up data, including mortality and date of death were obtained when appropriate. We defined the diagnosis of EM when eosinophils were present on EMB, or when there was evidence of endocardial wall thickening or LV thrombus on imaging in the process of HES. This study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and was approved by the Cleveland Clinic institutional review board (IRB: 20-1300). Due to retrospective nature of the study, patient consent was waived.

Statistical analysis

Comparisons were made between patients who had cardiac involvement in HES and patients without cardiac involvement. Normally distributed continuous parameters were presented as mean ± standard deviation, and skewed continuous parameters were expressed as median (interquartile range defined as between first and third quartiles). The Shapiro-Wilk test was used to evaluate for normally distributed data. Categorical data were presented as percentages. Differences between patients with EM and HES patients without cardiac involvement in clinical variables were assessed by the unpaired t-test for continuous variables and the Chi-squared test for categorical variables. All statistical tests were two-sided and P values of <0.05 were considered statistically significant. Statistical analysis was performed using SPSS version 25 (SPSS Inc., Chicago, IL, USA).

Results

Clinical characteristics

The initial institutional echocardiographic database query resulted in 1,664 patients who underwent echocardiography with an associated ICD-10 code for eosinophilia between September 1986 and January 2023. A total of 36 patients with a definite diagnosis of HES were identified; of these, 11 patients were diagnosed with EM. Of the patients diagnosed with EM, six cases were diagnosed by EMB and five by imaging. One patient was diagnosed with EM by echocardiography alone, which showed endocardial thickening and LV thrombus, typical features of EM.

Baseline characteristics of the entire study population, and the subgroups stratified to the EM group and the HES without cardiac involvement group, are presented in Table 1. The mean age of patients with EM was 57±12 years, with 63.6% being female. Asthma was the most common presenting comorbidity (54.5%). Hypertension (27.3%), diabetes mellitus (18.2%), coronary artery disease (9.1%), atrial fibrillation (18.2%), and preceding heart failure (9.1%) were less common. There were no significant differences in baseline characteristics between the two groups. Idiopathic HES was the most common etiology, followed by leukemia in both groups (Figure 1).

Figure 1 Etiologies of hypereosinophilic syndrome in the study. EGPA, eosinophilic granulomatosis with polyangiitis; HES, hypereosinophilic syndrome.

Examination findings

The initial symptoms of HES were shown in Figure 2. The most common initial presenting symptom was cough (41.7%) in the entire group. Cough, rash, and gastrointestinal symptoms such as abdominal pain, nausea and diarrhea were the most frequent initial symptoms (32.0%) in non-cardiac involvement group. Cough and shortness of breath were the most frequent initial symptoms (63.6%) in EM group. Patients with EM had significantly more shortness of breath (P<0.01), neuropathy (P=0.04), and fatigue (P=0.04) than HES patients without cardiac involvement. Table 1 shows the laboratory findings. The median value of AEC was 7.3×10⁴/µL (interquartile range, 2.7–14.9 ×10⁴/µL), without significant differences between the groups. All patients had blood eosinophil counts higher than 1.5×10⁴/µL. Patients with EM had significantly higher N-terminal pro B-type natriuretic peptide (NT-pro BNP) (2,206 vs. 101 pg/mL, P<0.01) and troponin T (0.77 vs. 0.01 ng/mL, P<0.01). Of the 11 patients with EM, 10 patients had available electrocardiograms for review, and three (30%) had abnormal Q waves. No patients had ST-segment elevation, likely because the patients presented in the chronic stage.

Figure 2 The initial presenting symptoms and signs of hypereosinophilic syndrome. *, P<0.01; **, P<0.05. SOB, shortness of breath; HES, hypereosinophilic syndrome.

Data regarding diagnostic imaging are shown in Table 2. Of 11 patients with EM, echocardiography was performed in ten patients (91%), CMR in eight patients (73%) and EMB in six patients (55%). On echocardiography, in patients with EM, median LV ejection fraction was 59% (interquartile range, 56–64%), 50.0% had endocardial thickening, and 30.0% had LV thrombus. On CMR, median LV ejection fraction was 46% (interquartile range, 30–57%), 50.0% had endocardial thickening and 62.5% had LV thrombus. Most cases of LV thrombus were in the apex, and one case of thrombus was found in the vicinity of the posterior mitral valve leaflet. Right ventricular thrombus occurred in one patient who also had LV thrombus. Delayed enhancement imaging was performed in seven patients with EM. Six patients had subendocardial patterns of late gadolinium enhancement (LGE) (6/7, 85.7%). One patient did not undergo delayed enhancement imaging because of severe kidney dysfunction. Of six patients who underwent EMB, five patients were found to have eosinophils (5/6, 83.3%). Of 25 patients without cardiac involvement, echocardiography was performed in 24 patients (96%), CMR in seven patients (28%) and EMB was not performed in any patient (0%). Delayed enhancement imaging was performed in seven patients without cardiac involvement, however, none of these patients had abnormal patterns of LGE (0/7, 0%).

Treatment and outcomes

Most patients received corticosteroids (91.7%) (Table 3). All patients with EM received aspirin, six patients (54.5%) received warfarin; four patients were prescribed warfarin for intracardiac thrombosis, one for atrial fibrillation, and one for a mechanical mitral valve. Patients with EM, when compared to HES patients without cardiac involvement received significantly more heparin (81.8% vs. 40.0%, P=0.02) and aspirin (100.0% vs. 44.0%, P<0.01), and less imatinib (0.0% vs. 40.0%, P=0.01). During the follow-up period, two patients with EM underwent cardiac surgery for valvular disease (one for mitral stenosis and another for mitral regurgitation), and one patient without EM underwent surgery for mitral regurgitation.

The outcomes for patients are shown in Table 4. During a median follow-up of 87 months (25^th–75^th quartile range, 44–138 months), 8 patients (22.2%) died: 2 patients (18.2%) in the EM group and 6 patients (24.0%) in the non-cardiac involvement group. By log-rank test, there were no significant mortality differences between the groups (P>0.99). EM patients developed significantly more thromboembolic events compared to HES patients without cardiac involvement (63.6% vs. 24.0%, P=0.02), including stroke (36.4% vs. 12.0%, P=0.09) and venous thromboembolism (36.4% vs. 12.0%, P=0.09). We summarized the treatment and outcomes for patients with EM in Table 5.

Discussion

The main findings of the study were (I) laboratory findings of elevated troponin, NT-pro BNP, and C-reactive protein (CRP) were seen in all cases of EM; (II) the most common advanced cardiac imaging finding of EM was a subendocardial pattern of LGE on CMR; (III) patients with EM had significantly more thromboembolic events compared to HES patients without cardiac involvement, although mortality was not significantly different between the two groups.

Symptoms of HES

The most common symptoms of HES include cutaneous manifestations, pulmonary involvement, and peripheral neuropathies, in addition to cardiac involvement (23). In this study, cough was the most frequent symptom, and some patients had shortness of breath even in the absence of cardiac involvement or cough. Pulmonary symptoms are reported to be present in about 40% of patients with HES (24), but the prevalence of pulmonary symptoms in this study were more prevalent than previously reported. Shortness of breath, neuropathy, and fatigue were more related to EM. Shortness of breath may be attributable to systolic and diastolic dysfunction and heart failure caused by EM. Peripheral neuropathy has been reported to be associated with heart failure, but the cause is unclear (25).

Laboratory data, electrocardiogram and EM

Troponin and NT-pro BNP are useful markers for the detection of cardiac involvement in HES, and can be used during serial follow-up (26). In this study, troponin T and NT-pro BNP were elevated in all patients with EM who had these markers measured. Notably, troponin T is also used to identify patients at risk of development of acute heart failure after start of imatinib mesylate for treatment of HES (27). It has also been reported that troponin T can evaluate immunosuppressive therapy response (28). Median white blood cell and eosinophil counts were higher in patients with EM, but the difference was not statistically significant.

Imaging and EM

Definitive diagnosis of cardiac involvement relies on histopathological diagnosis via EMB. However, modern approaches to a presumptive diagnosis are often made based on limited descriptions of cardiac imaging findings (29). Echocardiography and CMR are two major imaging modalities utilized for non-invasive diagnosis of EM. Prior reviews suggest that classical imaging findings of EM include endocardial thickening and LV thrombus (10,30-32). In this cohort, these findings were identified in the about half of cases (Figure 3). Echocardiography and CMR were similar for the detection of endocardial thickening. On the other hand, there were two cases in which LV thrombus was not detected by echocardiography but was detected by CMR a few days later. Echocardiography has been reported to be less sensitive than CMR in detecting LV thrombus (33). In particular, echocardiography may be less sensitive for LV thrombus which is small or layered (34). The use of ultrasound-enhancing-agent during echocardiography can significantly increase the sensitivity of LV thrombus detection (35). In this study, four patients without cardiac involvement underwent contrast echocardiography, and no LV thrombus was detected in these patients. If EM is suspected or CMR is not possible, the use of ultrasound-enhancing-agent should be considered to increase diagnostic sensitivity. Of the patients with EM who underwent gadolinium contrast, the majority of patients had subendocardial patterns of LGE. CMR is an important adjunct imaging modality in the diagnosis of EM and the detection of LV thrombus in patients with HES and is the gold standard for non-invasive evaluation in myocarditis. CMR is also valuable to visualize the extent of endomyocardial involvement in the treatment of EM (5). A multimodality imaging approach using echocardiography and CMR is very important in the diagnostic workup of EM in HES (36). EMB can be associated with a high risk of iatrogenic embolization, especially in EM patients with thrombotic complications, and the diagnosis should be comprehensively made using non-invasive imaging studies, consisting of echocardiography and CMR.

Figure 3 Classic cardiac imaging findings of eosinophilic myocarditis encountered in the study. Upper row: cardiac magnetic resonance obtained in a patient with acute HES cardiomyopathy. (A) SSFP horizontal long-axis image demonstrating an area of low signal intensity in the apex measuring 2.3 cm × 0.7 cm (red asterisk). (B) PSIR sequence with long inversion time for late gadolinium enhancement imaging confirmed the presence of an apical thrombus (red asterisk). Lower row: multimodality evaluation of a patient with chronic HES cardiomyopathy. (C) Transthoracic echocardiogram with apical 4 chamber view, demonstrating abnormal thickening at the apex (red arrow). (D) Cardiac magnetic resonance PSIR sequence reveals the presence of diffuse subendocardial enhancement corresponding to diffuse fibrotic and scarring changes at the cardiac apex (red arrow). HES, hypereosinophilic syndrome; SSFP, steady state free procession; PSIR, phase sensitive inversion recovery.

Thromboembolism and EM

Nine patients (9/36, 25.0%) had thromboembolism at the time of HES diagnosis, five of whom (5/9, 55.6%) were patients with EM. Five patients (5/36, 13.9%) had thromboembolism during follow-up. Of them, three patients had EM (3/5, 60.0%) and the duration from follow-up start to thromboembolism were under a year. In this cohort, patients with EM had significantly more thromboembolic events. EM may be strongly related to thromboembolism, but there are no guidelines on the role of antithrombotic or anticoagulant therapy in HES and EM. Of three patients with EM who had thromboembolism during follow-up, one patient was on apixaban, one was on heparin, and one was not on any antithrombotic medication. Patients with HES have a long-term elevated risk of thromboembolism. The use of anticoagulants should be considered to prevent mural thrombus formation. On the other hand, there is a lack of data in the literature on how long anticoagulants should be continued in EM. The current study highlights the need for more prospective data and dedicated guidelines regarding antithrombotic therapy in this patient population.

Future perspectives

Previous reviews and case reports have described only limited use of CMR in the diagnosis and evaluation of cardiac HES (37). This study presents the largest study containing EM patients who underwent CMR.

In this study, 20% of patients without cardiac involvement were hospitalized for heart failure during the follow-up period. Most of them underwent echocardiography, but only 28% of them underwent CMR. It is possible that certain cases of subclinical EM were not diagnosed. Screening by CMR should be considered in patients with HES.

Future directions for research include evaluating the role of anticoagulant therapy for patients with HES especially in the setting of thrombotic complications, and the comparison of CMR versus echocardiography for diagnosis and prognostication. Due to the limited number of cardiac HES cases, a multicenter trial would provide a high enough volume and thus power in determining the most effective imaging modality for HES diagnosis. Additionally, identifying the specific etiologies of HES associated with cardiac manifestations may provide further insight to management, risk factors, and preventative strategies for patients who have HES.

Limitations

This was a single-center retrospective study at a quaternary center, with potential bias in the selection of cases. Certain cases may not be captured due to coding issues in electronic medical records. The study selected patients with suspected HE from 1986 to 2023, during which time the diagnostic criteria for HE was updated twice. It is possible that some patients were omitted from the selection process due to differences in diagnostic criteria at the time of presentation, although all the patients included were selected according to the current diagnostic criteria. Because the study spanned a long period of time, changes and improvements in imaging technologies may have affected some of the cardiac imaging findings over time.

Conclusions

In a 37-year cohort of HES in EM, echocardiography was the first-line imaging modality, while CMR was an important adjunct imaging modality. Although there were no significant mortality differences during a median follow-up of 87 months, patients with EM had a higher incidence of thromboembolic events compared to HES patients without cardiac involvement.

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://cdt.amegroups.com/article/view/10.21037/cdt-24-347/rc

Data Sharing Statement: Available at https://cdt.amegroups.com/article/view/10.21037/cdt-24-347/dss

Peer Review File: Available at https://cdt.amegroups.com/article/view/10.21037/cdt-24-347/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://cdt.amegroups.com/article/view/10.21037/cdt-24-347/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. This study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and was approved by the Cleveland Clinic institutional review board (IRB: 20-1300). Due to retrospective nature of the study, patient consent was waived.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

References

1. Valent P, Klion AD, Horny HP, et al. Contemporary consensus proposal on criteria and classification of eosinophilic disorders and related syndromes. J Allergy Clin Immunol 2012;130:607-612.e9. [Crossref] [PubMed]
2. Chusid MJ, Dale DC, West BC, et al. The hypereosinophilic syndrome: analysis of fourteen cases with review of the literature. Medicine (Baltimore) 1975;54:1-27. [Crossref] [PubMed]
3. Valent P, Klion AD, Roufosse F, et al. Proposed refined diagnostic criteria and classification of eosinophil disorders and related syndromes. Allergy 2023;78:47-59. [Crossref] [PubMed]
4. Requena G, Logie J, Gibbons DC, et al. The increasing incidence and prevalence of hypereosinophilic syndrome in the United Kingdom. Immun Inflamm Dis 2021;9:1447-51. [Crossref] [PubMed]
5. Petersen SE, Kardos A, Neubauer S. Subendocardial and papillary muscle involvement in a patient with Churg-Strauss syndrome, detected by contrast enhanced cardiovascular magnetic resonance. Heart 2005;91:e9. [Crossref] [PubMed]
6. Tefferi A, Patnaik MM, Pardanani A. Eosinophilia: secondary, clonal and idiopathic. Br J Haematol 2006;133:468-92. [Crossref] [PubMed]
7. Ogbogu PU, Bochner BS, Butterfield JH, et al. Hypereosinophilic syndrome: a multicenter, retrospective analysis of clinical characteristics and response to therapy. J Allergy Clin Immunol 2009;124:1319-25.e3. [Crossref] [PubMed]
8. Mapelli M, Cefalù C, Zaffalon D, et al. Hypereosinophilic syndrome onset with Loeffler's endocarditis after COVID-19 infection. Eur Heart J Cardiovasc Imaging 2022;23:e472. [Crossref] [PubMed]
9. Thambidorai SK, Korlakunta HL, Arouni AJ, et al. Acute eosinophilic myocarditis mimicking myocardial infarction. Tex Heart Inst J 2009;36:355-7. [PubMed]
10. Mankad R, Bonnichsen C, Mankad S. Hypereosinophilic syndrome: cardiac diagnosis and management. Heart 2016;102:100-6. [Crossref] [PubMed]
11. Mubarik A, Iqbal AM. Loeffler Endocarditis. In: StatPearls. Treasure Island (FL) ineligible companies. StatPearls [Internet]; 2024.
12. Szczerba E, Kowalik R, Gorska K, et al. Severe mitral stenosis secondary to eosinophilic granulomatosis resolving after pharmacological treatment. Echocardiography 2018;35:2099-103. [Crossref] [PubMed]
13. Cogan E, Roufosse F. Clinical management of the hypereosinophilic syndromes. Expert Rev Hematol 2012;5:275-89; quiz 290. [Crossref] [PubMed]
14. Ogbogu PU, Rosing DR, Horne MK 3rd. Cardiovascular manifestations of hypereosinophilic syndromes. Immunol Allergy Clin North Am 2007;27:457-75. [Crossref] [PubMed]
15. Parrillo JE. Heart disease and the eosinophil. N Engl J Med 1990;323:1560-1. [Crossref] [PubMed]
16. Polito MV, Hagendorff A, Citro R, et al. Loeffler's Endocarditis: An Integrated Multimodality Approach. J Am Soc Echocardiogr 2020;33:1427-41. [Crossref] [PubMed]
17. Brambatti M, Matassini MV, Adler ED, et al. Eosinophilic Myocarditis: Characteristics, Treatment, and Outcomes. J Am Coll Cardiol 2017;70:2363-75. [Crossref] [PubMed]
18. Ommen SR, Seward JB, Tajik AJ. Clinical and echocardiographic features of hypereosinophilic syndromes. Am J Cardiol 2000;86:110-3. [Crossref] [PubMed]
19. Syed IS, Martinez MW, Feng DL, et al. Cardiac magnetic resonance imaging of eosinophilic endomyocardial disease. Int J Cardiol 2008;126:e50-2. [Crossref] [PubMed]
20. Amini R, Nielsen C. Eosinophilic myocarditis mimicking acute coronary syndrome secondary to idiopathic hypereosinophilic syndrome: a case report. J Med Case Rep 2010;4:40. [Crossref] [PubMed]
21. Boussir H, Ghalem A, Ismaili N, et al. Eosinophilic myocarditis and hypereosinophilic syndrome. J Saudi Heart Assoc 2017;29:211-3. [Crossref] [PubMed]
22. Khalid M, Gayam V, Dahal S, et al. Hypereosinophilic Syndrome Complicated by Eosinophilic Myocarditis With Dramatic Response to Steroid. J Investig Med High Impact Case Rep 2018;6:2324709618764512. [Crossref] [PubMed]
23. Weller PF, Bubley GJ. The idiopathic hypereosinophilic syndrome. Blood 1994;83:2759-79. [Crossref] [PubMed]
24. Wechsler ME. Pulmonary eosinophilic syndromes. Immunol Allergy Clin North Am 2007;27:477-92. [Crossref] [PubMed]
25. Minà C, Bagnato S, Sant'Angelo A, et al. Risk Factors Associated With Peripheral Neuropathy in Heart Failure Patients Candidates for Transplantation. Prog Transplant 2018;28:36-42. [Crossref] [PubMed]
26. Ponikowski P, Voors AA, Anker SD, et al. 2016 ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure: The Task Force for the diagnosis and treatment of acute and chronic heart failure of the European Society of Cardiology (ESC). Developed with the special contribution of the Heart Failure Association (HFA) of the ESC. Eur J Heart Fail 2016;18:891-975. [Crossref] [PubMed]
27. Pitini V, Arrigo C, Azzarello D, et al. Serum concentration of cardiac Troponin T in patients with hypereosinophilic syndrome treated with imatinib is predictive of adverse outcomes. Blood 2003;102:3456-7; author reply 3457. [Crossref] [PubMed]
28. Kadota S, Takeuchi Y, Izuhara M, et al. The importance of serial cardiac troponin measurement for evaluating the response to immunosuppressive therapy for myocarditis. J Cardiol 2008;52:154-8. [Crossref] [PubMed]
29. Baandrup U. Eosinophilic myocarditis. Herz 2012;37:849-52. [Crossref] [PubMed]
30. Davies J, Gibson DG, Foale R, et al. Echocardiographic features of eosinophilic endomyocardial disease. Br Heart J 1982;48:434-40. [Crossref] [PubMed]
31. Gottdiener JS, Maron BJ, Schooley RT, et al. Two-dimensional echocardiographic assessment of the idiopathic hypereosinophilic syndrome. Anatomic basis of mitral regurgitation and peripheral embolization. Circulation 1983;67:572-8. [Crossref] [PubMed]
32. Plastiras SC, Economopoulos N, Kelekis NL, et al. Magnetic resonance imaging of the heart in a patient with hypereosinophilic syndrome. Am J Med 2006;119:130-2. [Crossref] [PubMed]
33. Bulluck H, Chan MHH, Paradies V, et al. Incidence and predictors of left ventricular thrombus by cardiovascular magnetic resonance in acute ST-segment elevation myocardial infarction treated by primary percutaneous coronary intervention: a meta-analysis. J Cardiovasc Magn Reson 2018;20:72. [Crossref] [PubMed]
34. Velangi PS, Choo C, Chen KA, et al. Long-Term Embolic Outcomes After Detection of Left Ventricular Thrombus by Late Gadolinium Enhancement Cardiovascular Magnetic Resonance Imaging: A Matched Cohort Study. Circ Cardiovasc Imaging 2019;12:e009723. [Crossref] [PubMed]
35. Weinsaft JW, Kim RJ, Ross M, et al. Contrast-enhanced anatomic imaging as compared to contrast-enhanced tissue characterization for detection of left ventricular thrombus. JACC Cardiovasc Imaging 2009;2:969-79. [Crossref] [PubMed]
36. Russo M, Ismibayli Z, Antonaci S, et al. Eosinophilic myocarditis: from etiology to diagnostics and therapy. Minerva Cardiol Angiol 2024;72:656-73. [Crossref] [PubMed]
37. Debl K, Djavidani B, Buchner S, et al. Time course of eosinophilic myocarditis visualized by CMR. J Cardiovasc Magn Reson 2008;10:21. [Crossref] [PubMed]