Echocardiographic evaluation of left ventricular mechanics in sarcoidosis patients without overt heart disease: a systematic review and meta-analysis

Main Article Content

Andrea Sonaglioni
Valeria Fagiani
Marta Rigoni
Gian Luigi Nicolosi
Alessandro Lucidi
Antonella Caminati
Michele Lombardo
Sergio Harari

Keywords

extracardiac sarcoidosis, left ventricular mechanics, global longitudinal strain, left ventricular ejection fraction, meta-analysis.

Abstract

Background and aim: During the last decade, a small number of studies have used speckle tracking echocardiography (STE) to investigate sarcoidosis effect on left ventricular (LV) mechanics in patients without overt heart disease. The present systematic review and meta-analysis has been primarily designed to summarize the main findings of these studies and to examine the overall influence of sarcoidosis on LV-global longitudinal strain (GLS) and left ventricular ejection fraction (LVEF). Methods: All echocardiographic studies assessing conventional echoDoppler parameters and myocardial strain indices in patients with extracardiac sarcoidosis (ECS) vs. healthy controls, selected from PubMed and EMBASE databases, were included. The risk of bias was assessed by using the National Institutes of Health (NIH) Quality Assessment of Case-Control Studies. Continuous data (LV-GLS and LVEF) were pooled as a standardized mean difference (SMD) comparing sarcoidosis group with healthy controls. The overall SMDs of LV-GLS and LVEF were calculated using the random-effect model. Results: The full-text of 13 studies with 785 ECS patients and 567 healthy controls were analyzed. Both average LVEF (60.5±6.6 vs 63.0±4.8%, P<0.001) and LV-GLS (-17.4±3.3 vs -21.0±2.7%, P<0.001) were significantly lower in ECS patients than controls. However, sarcoidosis showed a significantly larger effect on LV-GLS (SMD: -1.26, 95%CI -1.61,-0.91, P<0.001) rather than on LVEF (SMD: -0.51, 95%CI -0.83,-0.20, P=0.001). Substantial heterogeneity was found for the studies that assessed LV-GLS (I2=86.4%) and LVEF (I2=85.3%). Egger's test gave a P-value of 0.24 for LV-GLS and 0.32 for LVEF assessment, indicating no publication bias. On meta-regression analysis, none of the moderators was significantly associated with effect modification for both LV-GLS and LVEF (all P <0.05). Conclusions: In patients without overt heart disease, the effect of sarcoidosis on LV-GLS is significantly greater than on LVEF. STE analysis should be implemented in clinical practice for the early detection of myocardial involvement in ECS patients.

Abstract 193 | PDF Downloads 150

References

1. Jain R, Yadav D, Puranik N, Guleria R, Jin JO. Sarcoidosis: Causes, Diagnosis, Clinical Features, and Treatments. J Clin Med. 2020;9(4):1081.
2. Iannuzzi MC, Fontana JR. Sarcoidosis: clinical presentation, immunopathogenesis, and therapeutics. JAMA. 2011;305(4):391-9.
3. Silverman KJ, Hutchins GM, Bulkley BH. Cardiac sarcoid: a clinicopathologic study of 84 unselected patients with systemic sarcoidosis. Circulation. 1978;58(6):1204-11.
4. Hulten E, Aslam S, Osborne M, Abbasi S, Bittencourt MS, Blankstein R. Cardiac sarcoidosis-state of the art review. Cardiovasc Diagn Ther. 2016;6(1):50-63.
5. Mankad P, Mitchell B, Birnie D, Kron J. Cardiac Sarcoidosis. Curr Cardiol Rep. 2019;21(12):152.
6. Jaiswal R, Vaisyambath L, Khayyat A, et al. Cardiac Sarcoidosis Diagnostic Challenges and Management: A Case Report and Literature Review. Cureus. 2022;14(5):e24850.
7. Perry A, Vuitch F. Causes of death in patients with sarcoidosis. A morphologic study of 38 autopsies with clinicopathologic correlations. Arch Pathol Lab Med. 1995;119(2):167-72.
8. Trivieri MG, Spagnolo P, Birnie D, et al. Challenges in Cardiac and Pulmonary Sarcoidosis: JACC State-of-the-Art Review. J Am Coll Cardiol. 2020;76(16):1878-1901.
9. Mohsen A, Jimenez A, Hood RE, et al. Cardiac sarcoidosis: electrophysiological outcomes on long-term follow-up and the role of the implantable cardioverter-defibrillator. J Cardiovasc Electrophysiol. 2014;25(2):171-6.
10. Patel MR, Cawley PJ, Heitner JF, et al. Detection of myocardial damage in patients with sarcoidosis. Circulation. 2009;120(20):1969-77.
11. Ohira H, Birnie DH, Pena E, et al. Comparison of (18)F-fluorodeoxyglucose positron emission tomography (FDG PET) and cardiac magnetic resonance (CMR) in corticosteroid-naive patients with conduction system disease due to cardiac sarcoidosis. Eur J Nucl Med Mol Imaging. 2016;43(2):259-269.
12. Birnie DH, Sauer WH, Bogun F, et al. HRS expert consensus statement on the diagnosis and management of arrhythmias associated with cardiac sarcoidosis. Heart Rhythm. 2014;11(7):1305-23.
13. Vignaux O, Dhote R, Duboc D, et al. Detection of myocardial involvement in patients with sarcoidosis applying T2-weighted, contrast-enhanced, and cine magnetic resonance imaging: initial results of a prospective study. J Comput Assist Tomogr. 2002;26(5):762-7.
14. Potter E, Marwick TH. Assessment of Left Ventricular Function by Echocardiography: The Case for Routinely Adding Global Longitudinal Strain to Ejection Fraction. JACC Cardiovasc Imaging. 2018;11(2 Pt 1):260-274.
15. Shah BN, De Villa M, Khattar RS, Senior R. Imaging cardiac sarcoidosis: the incremental benefit of speckle tracking echocardiography. Echocardiography. 2013;30(7):E213-4.
16. Galderisi M, Cosyns B, Edvardsen T, et al. Standardization of adult transthoracic echocardiography reporting in agreement with recent chamber quantification, diastolic function, and heart valve disease recommendations: an expert consensus document of the European Association of Cardiovascular Imaging. Eur Heart J Cardiovasc Imaging. 2017;18(12):1301-1310.
17. Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097.
18. Ma LL, Wang YY, Yang ZH, Huang D, Weng H, Zeng XT. Methodological quality (risk of bias) assessment tools for primary and secondary medical studies: what are they and which is better? Mil Med Res. 2020;7(1):7.
19. Kul S, Ozcelik HK, Uyarel H, et al. Diagnostic value of strain echocardiography, galectin-3, and tenascin-C levels for the identification of patients with pulmonary and cardiac sarcoidosis. Lung. 2014;192(4):533-42.
20. Orii M, Hirata K, Tanimoto T, et al. Myocardial Damage Detected by Two-Dimensional Speckle-Tracking Echocardiography in Patients with Extracardiac Sarcoidosis: Comparison with Magnetic Resonance Imaging. J Am Soc Echocardiogr. 2015;28(6):683-91.
21. Tigen K, Sunbul M, Karaahmet T, et al. Early Detection of Bi-ventricular and Atrial Mechanical Dysfunction Using Two-Dimensional Speckle Tracking Echocardiography in Patients with Sarcoidosis. Lung. 2015;193(5):669-75.
22. Joyce E, Kamperidis V, Ninaber MK, et al. Prevalence and Correlates of Early Right Ventricular Dysfunction in Sarcoidosis and Its Association with Outcome. J Am Soc Echocardiogr. 2016;29(9):871-8.
23. Murtagh G, Laffin LJ, Patel KV, et al. Improved detection of myocardial damage in sarcoidosis using longitudinal strain in patients with preserved left ventricular ejection fraction. Echocardiography. 2016;33(9):1344-52.
24. Değirmenci H, Demirelli S, Arısoy A, et al. Myocardial deformation and total atrial conduction time in the prediction of cardiac involvement in patients with pulmonary sarcoidosis. Clin Respir J. 2017;11(1):68-77.
25. Schouver ED, Moceri P, Doyen D, et al. Early detection of cardiac involvement in sarcoidosis with 2-dimensional speckle-tracking echocardiography. Int J Cardiol. 2017;227:711-716.
26. Chen J, Lei J, Scalzetti E, et al. Myocardial contractile patterns predict future cardiac events in sarcoidosis. Int J Cardiovasc Imaging. 2018;34(2):251-262.
27. Felekos I, Aggeli C, Gialafos E, et al. Global longitudinal strain and long-term outcomes in asymptomatic extracardiac sarcoid patients with no apparent cardiovascular disease. Echocardiography. 2018;35(6):804-808.
28. Di Stefano C, Bruno G, Arciniegas Calle MC, et al. Diagnostic and predictive value of speckle tracking echocardiography in cardiac sarcoidosis. BMC Cardiovasc Disord. 2020;20(1):21.
29. Bayat F, Fahimi A, Tavana S, Tabary M, Khaheshi I. Subclinical involvement of the heart and its associated factors in patients with sarcoidosis with normal systolic function using 2D speckle tracking. Echocardiography. 2020;37(1):41-46.
30. Kaptan Ozen D, Mutlu B, Kocakaya D, et al. The effect of global longitudinal strain on ımpaired six-minute walk test performance in patients with sarcoidosis. Sarcoidosis Vasc Diffuse Lung Dis. 2020;37(1):66-73.
31. Kusunose K, Fujiwara M, Yamada H, et al. Deterioration of biventricular strain is an early marker of cardiac involvement in confirmed sarcoidosis. Eur Heart J Cardiovasc Imaging. 2020;21(7):796-804.
32. Lehtonen J, Uusitalo V, Pöyhönen P, Mäyränpää MI, Kupari M. Cardiac sarcoidosis: phenotypes, diagnosis, treatment, and prognosis. Eur Heart J. 2023;44(17):1495-1510.
33. Kitai T, Nabeta T, Naruse Y, et al. Comparisons between biopsy-proven versus clinically diagnosed cardiac sarcoidosis. Heart. 2022;108(23):1887-1894.
34. Lynch JP 3rd, Hwang J, Bradfield J, Fishbein M, Shivkumar K, Tung R. Cardiac involvement in sarcoidosis: evolving concepts in diagnosis and treatment. Semin Respir Crit Care Med. 2014;35(3):372-90.
35. Aggeli C, Felekos I, Tousoulis D, Gialafos E, Rapti A, Stefanadis C. Myocardial mechanics for the early detection of cardiac sarcoidosis. Int J Cardiol. 2013;168(5):4820-1.
36. Fahy GJ, Marwick T, McCreery CJ, Quigley PJ, Maurer BJ. Doppler echocardiographic detection of left ventricular diastolic dysfunction in patients with pulmonary sarcoidosis. Chest. 1996;109(1):62-6.
37. Aydin Kaderli A, Gullulu S, Coskun F, Yilmaz D, Uzaslan E. Impaired left ventricular systolic and diastolic functions in patients with early grade pulmonary sarcoidosis. Eur J Echocardiogr. 2010;11(10):809-13.
38. Sonaglioni A, Nicolosi GL, Lombardo M, Gensini GF, Ambrosio G. Influence of chest conformation on myocardial strain parameters in healthy subjects with mitral valve prolapse. Int J Cardiovasc Imaging. 2021;37(3):1009-1022.
39. Sonaglioni A, Nicolosi GL, Lombardo M. The relationship between mitral valve prolapse and thoracic skeletal abnormalities in clinical practice: a systematic review. J Cardiovasc Med (Hagerstown). 2024;25(5):353-363.
40. Kato Y, Morimoto S, Uemura A, Hiramitsu S, Ito T, Hishida H. Efficacy of corticosteroids in sarcoidosis presenting with atrioventricular block. Sarcoidosis Vasc Diffuse Lung Dis. 2003;20(2):133-7.
41. Yodogawa K, Seino Y, Ohara T, Takayama H, Katoh T, Mizuno K. Effect of corticosteroid therapy on ventricular arrhythmias in patients with cardiac sarcoidosis. Ann Noninvasive Electrocardiol. 2011;16(2):140-7.
42. Nakano S, Kimura F, Osman N, et al. Improved myocardial strain measured by strain-encoded magnetic resonance imaging in a patient with cardiac sarcoidosis. Can J Cardiol. 2013;29(11):1531.e9-11.
43. Mirea O, Pagourelias ED, Duchenne J, et al. Intervendor Differences in the Accuracy of Detecting Regional Functional Abnormalities: A Report From the EACVI-ASE Strain Standardization Task Force. JACC Cardiovasc Imaging. 2018;11(1):25-34.
44. Negishi T, Negishi K, Thavendiranathan P, et al. Effect of Experience and Training on the Concordance and Precision of Strain Measurements. JACC Cardiovasc Imaging. 2017;10(5):518-522.
45. Rösner A, Barbosa D, Aarsæther E, Kjønås D, Schirmer H, D'hooge J. The influence of frame rate on two-dimensional speckle-tracking strain measurements: a study on silico-simulated models and images recorded in patients. Eur Heart J Cardiovasc Imaging. 2015;16(10):1137-47.
46. Sonaglioni A, Nicolosi GL, Trevisan R, et al. The influence of pectus excavatum on cardiac kinetics and function in otherwise healthy individuals: A systematic review. Int J Cardiol. 2023;381:135-144.