The Role of Quantitative Assessment of Visceral Adipose Tissue of the Heart as a Predictor for Cardiovascular Events

Objective of this article – to evaluate possibilities to visualize cardiac visceral adipose tissue by echocardiography, computed tomography (CT), and magnetic resonanse imaging (MRI) and to systematize data on its physiological and pathological roles. To achieve this goal, the authors analyzed relevant Russian and foreign sources of literature in the scientific libraries eLIBRARY and PubMed, by using the keywords: “pericardial fat”, “epicardial fat”, “visceral fat of the heart”, “epicardial adipose tissue”, “pericardial adipose tissue”, and “adipocytokine”. Actual data as of November 2018 were collected. The review presents up-to-date data on the physiological and pathophysiological roles of cytokines secreted by pericardial adipose tissue, as well as on correlations and possible theories of the relationship between the volumes of pericardial adipose tissue and the development of coronary heart disease, atrial fibrillation, and metabolic syndrome. According to echocardiography, epicardial adipose tissue thickness is a reliable predictor for the presence of high-risk atherosclerotic plaques in the coronary arteries. Adipose tissue volume can be measured with high accuracy using CT (manual, semi-automatic, and automatic methods).

A number of studies prove that MRI can be used for assigned tasks. The current notion of the role of these adipose depots can potentially be used in assessing the risk of cardiovascular diseases. The literature review presented confirms that visceral adipose tissue of the heart has a direct effect on the myocardium and coronary arteries and can be quantified using echocardiography, CT and MRI.

1. Polikarpov A.V., Aleksandrova G.A., Golubev N.A., Tyurina E.M., Os'kov Yu.I., Shelepova E.A. et al. Incidence of all population of Russia in 2017. Statistical materials. Part IV. Moscow; 2018: 69–70 (in Russ.).

2. Rosen E.D., Spiegelman B.M. Adipocytes as regulators of energy balance and glucose homeostasis. Nature. 2006; 444: 847–53. DOI: 10.1038/nature05483

3. Bjorndal B., Burri L., Staalesen V., Skorve J., Berge R.K. Different adipose depots: their role in the development of metabolic syndrome and mitochondrial response to hypolipidemic agents. J. Obes. 2011; 2011: 1–15. DOI: 10.1155/2011/490650

4. Drapkina O.M., Korneeva O.N., Drapkina Yu.S. Epicardial fat: a striker or a spare? Rational Pharmacotherapy in Cardiology. 2013; 9 (3): 287–91 (in Russ.).

5. Chumakova G.A., Veselovskaya N.G., Gritsenko O.V., Kozarenko O.V., Subbotan E.A. Epicardial obesity as risk factor of development of coronary atherosclerosis. Cardiology. 2013; 1: 51–5 (in Russ.).

6. Talman A.H., Psaltis P.J., Cameron J.D., Meredith I.T., Seneviratne S.K., Wong D.T. Epicardial adipose tissue: far more than a fat depot. Cardiovasc. Diagn. Ther. 2014; 4: 416–29. DOI: 10.3978/j.issn.2223-3652.2014.11.05

7. Patel V.B., Basu R., Oudit G.Y. ACE2/Ang 1-7 axis: a critical regulator of epicardial adipose tissue inflammation and cardiac dysfunction in obesity. Adipocyte.2016; 5 (3): 306–11. DOI: 10.1080/21623945.2015.1131881

8. Iacobellis G., Bianco A.C. Epicardial adipose tissue: emerging physiological, pathophysiological and clinical features. Trends Endocrinol. Metab. 2011; 22: 450–7. DOI: 10.1016/ j.tem.2011.07.003

9. Iacobelis G. Local and systemic effects of the multifaceted epicardial adipose tissue depot. Nat. Rev. Endocrinol. 2015; 11: 363–71. DOI: 10.1038/nrendo.2015.58

10. Karmazyn M., Purdham D.M., Rajapurohitam V., Zeidan A. Signalling mechanisms underlying the metabolic and other effects of adipokines on the heart. Cardiovasc. Res. 2008; 79: 279–86. DOI: 10.1093/cvr/cvn115

11. Patel V.B., Shah S., Verma S., Oudit G.Y. Epicardial adipose tissue as a metabolic transducer: role in heart failure and coronary artery disease. Heart Fail. Rev. 2017; 22 (6): 889–902. DOI: 10.1007/s10741-017-9644-1

12. Ding J., Hsu F.C., Harris T.B., Liu Y., Kritchevsky S.B., Szklo M. et al. The association of pericardial fat with incident coronary heart disease: the Multi-Ethnic Study of Atherosclerosis (MESA). Am. J. Clin. Nutr. 2009; 90 (3): 499–504. DOI: 10.3945/ajcn.2008.27358

13. Britton K.A., Massaro J.M., Murabito J.M., Kreger B.E., Hoffmann U., Fox C.S. Body fat distribution, incident cardiovascular disease, cancer, and all-cause mortality. J. Am. Coll. Cardiol. 2013; 62: 921–5.

14. Mahabadi A.A., Berg M.H., Lehmann N., Kälsch H., Bauer M., Kara K. et al. Association of epicardial fat with cardiovascular risk factors and incident myocardial infarction in the general population: the Heinz Nixdorf Recall Study. J. Am. Coll. Cardiol. 2013; 61: 1388–95.

15. Forouzandeh F., Chang S.M., Muhyieddeen K., Zaid R.R., Trevino A.R., Xu J. et al. Does quantifying epicardial and intrathoracic fat with noncontrast computed tomography improve risk stratification beyond calcium scoring alone? Circ. Cardiovasc. Imag. 2013; 6 (1): 58–66.

16. Cheng V.Y., Dey D., Tamarappoo B., Nakazato R., Gransar H., Miranda-Peats R., Ramesh A. et al. Pericardial fat burden on ECG-gated noncontrast CT in asymptomatic patients who subsequently experience adverse cardiovascular events. J. Am. Coll. Cardiol. Cardiovasc. Imag. 2010; 3: 352–60.

17. Spearman J.V., Renker M., Schoepf U.J., Krazinski A.W., Herbert T.L., De Cecco C.N. et al. Prognostic value of epicardial fat volume measurements by computed tomography: a systematic review of the literature. Eur. Radiol. 2015; 25 (11): 3372–81. DOI: 10.1007/s00330-015-3765-5

18. Kolbin A.S., Mosikyan A.A., Tatarskiy B.A. Socioeconomic burden of atrial fibrillations in Russia: seven-year trends (2010–2017). Journal of Arrhythmology. 2018; 92: 42–8 (in Russ.).

19. Dereli S., Bayramoglu A., Yontar O.C., Cersit S., Gursoy M.O. Epicardial fat thickness: a new predictor of successful electrical cardioversion and atrial fibrillation recurrence. Echocardiography. 2018; 35 (2): 1926–31. DOI: 10.1111/ echo.14178

20. Mahajan R., Lau D.H., Brooks A.G., Shipp N.J., Manavis J., Wood J. Electrophysiological, electroanatomical and structural remodeling of the atria as a consequence of sustained obesity. J. Am. Coll. Cardiol. 2015; 66 (1): 1–11. DOI: 10.1016/j.jacc.2015.04.058

21. Friedman D.J., Wang N., Meigs J.B., Hoffmann U., Massaro J.M., Fox C.S. et al. Pericardial fat is associated with atrial conduction: the Framingham Heart Study. J. Am. Heart Assoc. 2014; 3 (2): 1–10. DOI: 10.1161/jaha.113.000477

22. Venteclef N., Guglielmi V., Balse E., Gaborit B., Cotillard A., Atassi F. et al. Human epicardial adipose tissue induces fibrosis of the atrial myocardium through the secretion of adipofibrokines. Eur. Heart J. 2013; 36: 795–805. DOI: 10.1093/eurheartj/eht099

23. Despres J.P., Lemieux I. Abdominal obesity and metabolic syndrome. Nature. 2006; 444: 881–7. DOI: 10.1038/ nature05488

24. Gupta P.P., Fonarow G.C., Horwich T.B. Obesity and the obesity paradox in heart failure. Can. J. Cardiol. 2015; 31: 195–202. DOI: 10.1016/j.cjca.2014.08.004

25. Vianello E., Dozio E., Arnaboldi F., Marazzi M.G., Martinelli C., Lamont J. et al. Epicardial adipocyte hypertrophy: association with M1-polarization and toll-like receptor pathways in coronary artery disease patients. Nutr. Metab. Cardiovasc. Dis. 2016; 26: 246–53. DOI: 10.1016/j.numecd.2015.12.005

26. Iacobellis G., Willens H.J., Barbaro G., Sharma A.M. Threshold values of high-risk echocardiographic epicardial fat thickness. Obesity.2008; 16 (4): 887–92. DOI: 10.1038/ oby.2008.6

27. Hruskova J., Maugeri A., Podrouzkova H., Stipalova T., Jakubik J., Barchitta M. et al. Association of cardiovascular health with epicardial adipose tissue and intima media thickness: the kardiovize study. J. Clin. Med. 2018; 7 (5). DOI: 10.3390/jcm7050113

28. Tachibana M., Miyoshi T., Osawa K., Toh N., Oe H., Nakamura K. et al. Measurement of epicardial fat thickness by transthoracic echocardiography for predicting high-risk coronary artery plaques. Heart Vessels. 2016; 31: 1758–66. DOI: 10.1007/s00380-016-0802-5

29. Park J.S., Choi S.Y., Zheng M., Yang H.M., Lim H.S., Choi B.J. et al. Epicardial adipose tissue thickness is a predictor for plaque vulnerability in patients with significant coronary artery disease. Atherosclerosis. 2013; 226: 134–9. DOI: 10.1016/j.atherosclerosis.2012.11.001

30. Lim C., Ahn M.I., Jung J.I., Beck K.S. Simple quantification of paracardial and epicardial fat dimensions at low-dose chest CT: correlation with metabolic risk factors and usefulness in predicting metabolic syndrome. Jpn J. Radiol. 2018; 36 (9): 528–36. DOI: 10.1007/s11604-018-0752-1

31. Miyazawa I., Ohkubo T., Kadowaki S., Fujiyoshi A., Hisamatsu T., Kadota A. et al.; SESSA Research Group. Change in pericardial fat volume and cardiovascular risk factors in a general population of japanese men. Circ. J. 2018; 82 (10): 2542–8. DOI: 10.1253/circj.CJ-18-0153

32. Commandeur F., Goeller M., Betancur J., Cadet S., Doris M., Chen X. et al. Deep learning for quantification of epicardial and thoracic adipose tissue from non-contrast CT. IEEE Trans. Med. Imaging. 2018; 37 (8): 1835–46. DOI: 10.1109/ tmi.2018.2804799

33. Homsi R., Meier-Schroers M., Gieseke J., Dabir D., Luetkens J.A., Kuetting D.L. et al. 3D-Dixon MRI based volumetry of peri- and epicardial fat. Int. J. Cardiovasc. Imaging. 2016; 32 (2): 291–9. DOI: 10.1007/s10554-015-0778-8

34. Nelson A.J., Worthley M.I., Psaltis P.J., Carbone A., Dundon B.K., Duncan R.F. et al. Validation of cardiovascular magnetic resonance assessment of pericardial adipose tissue volume. J. Cardiovasc. Magn. Reson. 2009; 11: 1–8. DOI: 10.1186/1532-429X-11-15