Pericardial fat and its influence on cardiac diastolic function

Vera H W de Wit-Verheggen, Sibel Altintas, Romy J M Spee, Casper Mihl, Sander M J van Kuijk, Joachim E Wildberger, Vera B Schrauwen-Hinderling, Bas L J H Kietselaer, Tineke van de Weijer, Vera H W de Wit-Verheggen, Sibel Altintas, Romy J M Spee, Casper Mihl, Sander M J van Kuijk, Joachim E Wildberger, Vera B Schrauwen-Hinderling, Bas L J H Kietselaer, Tineke van de Weijer

Abstract

Background: Pericardial fat (PF) has been suggested to directly act on cardiomyocytes, leading to diastolic dysfunction. The aim of this study was to investigate whether a higher PF volume is associated with a lower diastolic function in healthy subjects.

Methods: 254 adults (40-70 years, BMI 18-35 kg/m2, normal left ventricular ejection fraction), with (a)typical chest pain (otherwise healthy) from the cardiology outpatient clinic were retrospectively included in this study. All patients underwent a coronary computed tomographic angiography for the measurement of pericardial fat volume, as well as a transthoracic echocardiography for the assessment of diastolic function parameters. To assess the independent association of PF and diastolic function parameters, multivariable linear regression analysis was performed. To maximize differences in PF volume, the group was divided in low (lowest quartile of both sexes) and high (highest quartile of both sexes) PF volume. Multivariable binary logistic analysis was used to study the associations within the groups between PF and diastolic function, adjusted for age, BMI, and sex.

Results: Significant associations for all four diastolic parameters with the PF volume were found after adjusting for BMI, age, and sex. In addition, subjects with high pericardial fat had a reduced left atrial volume index (p = 0.02), lower E/e (p < 0.01) and E/A (p = 0.01), reduced e' lateral (p < 0.01), reduced e' septal p = 0.03), compared to subjects with low pericardial fat.

Conclusion: These findings confirm that pericardial fat volume, even in healthy subjects with normal cardiac function, is associated with diastolic function. Our results suggest that the mechanical effects of PF may limit the distensibility of the heart and thereby directly contribute to diastolic dysfunction. Trial registration NCT01671930.

Keywords: Cardiac diastolic function; Epicardial fat; Pericardial fat.

Conflict of interest statement

The authors declare that they have no conflict of interests.

Figures

Fig. 1
Fig. 1
Flowchart of inclusion (n = 254). 254 patients from the Maastricht biomarker CT study were eligible for the analysis of the association of PF and diastolic function in healthy subjects
Fig. 2
Fig. 2
Definition of pericardial fat (PF) and the related adipose tissues. The adipose tissue surrounding the heart is defined as the pericardial fat (PF) and is a combination of epicardial and cardiac fat components. Within the PF, the pericardium demarcates the epicardial adipose tissue (EAT) from the cardiac adipose tissue (CAT). EAT (depicted in blue) is located between the myocardium and visceral pericardium, CAT (depicted in green) is located adherent and external to the parietal pericardium
Fig. 3
Fig. 3
The variation of PF volume to sex, age and BMI in a healthy population. PF volume is higher in males as in females (a), PF volume is not related to age (b) and PF volume is associated with BMI (c)
Fig. 4
Fig. 4
PF is not associated with diastolic function parameters in a healthy population. Data of the entire cohort (n = 254) are displayed. No correlations are found
Fig. 5
Fig. 5
No relation of PF to its CAT and EAT component. The amount of CAT (a) and EAT (b) are not related to PF. Although EAT and CAT volume show a wide variation, they are linearly associated to each other (c), indicating that both increase with an increase of PF

References

    1. Aziz F, Tk LA, Enweluzo C, Dutta S, Zaeem M. Diastolic heart failure: a concise review. J Clin Med Res. 2013;5(5):327–334.
    1. Nagueh SF, Smiseth OA, Appleton CP, Byrd BF, 3rd, Dokainish H, Edvardsen T, et al. Recommendations for the evaluation of left ventricular diastolic function by echocardiography: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr. 2016;29(4):277–314.
    1. Shah RV, Anderson A, Ding J, Budoff M, Rider O, Petersen SE, et al. Pericardial, but not hepatic, fat by CT is associated with CV outcomes and structure: the multi-ethnic study of atherosclerosis. JACC Cardiovasc Imaging. 2017;10(9):1016–1027.
    1. Mahabadi AA, Berg MH, Lehmann N, Kalsch 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(13):1388–1395.
    1. Iacobellis G. Local and systemic effects of the multifaceted epicardial adipose tissue depot. Nat Rev Endocrinol. 2015;11(6):363–371.
    1. Cherian S, Lopaschuk GD, Carvalho E. Cellular cross-talk between epicardial adipose tissue and myocardium in relation to the pathogenesis of cardiovascular disease. Am J Physiol Endocrinol Metab. 2012;303(8):E937–E949.
    1. Iacobellis G, Bianco AC. Epicardial adipose tissue: emerging physiological, pathophysiological and clinical features. Trends Endocrinol Metab. 2011;22(11):450–457.
    1. Gaborit B, Abdesselam I, Dutour A. Epicardial fat: more than just an “epi” phenomenon? Hormone Metab Res. 2013;45(13):991–1001.
    1. Bakkum MJ, Danad I, Romijn MA, Stuijfzand WJ, Leonora RM, Tulevski II, et al. The impact of obesity on the relationship between epicardial adipose tissue, left ventricular mass and coronary microvascular function. Eur J Nucl Med Mol Imaging. 2015;42(10):1562–1573.
    1. Iozzo P. Myocardial, perivascular, and epicardial fat. Diabetes Care. 2011;34(Suppl 2):S371–S379.
    1. Cho DH, Joo HJ, Kim MN, Lim DS, Shim WJ, Park SM. Association between epicardial adipose tissue, high-sensitivity C-reactive protein and myocardial dysfunction in middle-aged men with suspected metabolic syndrome. Cardiovasc Diabetol. 2018;17(1):95.
    1. Mazurek T, Zhang L, Zalewski A, Mannion JD, Diehl JT, Arafat H, et al. Human epicardial adipose tissue is a source of inflammatory mediators. Circulation. 2003;108(20):2460–2466.
    1. Shibasaki I, Nishikimi T, Mochizuki Y, Yamada Y, Yoshitatsu M, Inoue Y, et al. Greater expression of inflammatory cytokines, adrenomedullin, and natriuretic peptide receptor-C in epicardial adipose tissue in coronary artery disease. Regul Pept. 2010;165(2–3):210–217.
    1. Mack M. Inflammation and fibrosis. Matrix Biol. 2018;68–69:106–121.
    1. Dabbah S, Komarov H, Marmor A, Assy N. Epicardial fat, rather than pericardial fat, is independently associated with diastolic filling in subjects without apparent heart disease. Nutr Metab Cardiovasc Dis. 2014;24(8):877–882.
    1. Hua N, Chen Z, Phinikaridou A, Pham T, Qiao Y, LaValley MP, et al. The influence of pericardial fat upon left ventricular function in obese females: evidence of a site-specific effect. J Cardiovasc Magn Reson. 2014;16(1):37.
    1. Konishi M, Sugiyama S, Sugamura K, Nozaki T, Matsubara J, Akiyama E, et al. Accumulation of pericardial fat correlates with left ventricular diastolic dysfunction in patients with normal ejection fraction. J Cardiol. 2012;59(3):344–351.
    1. Wu CK, Tsai HY, Su MM, Wu YF, Hwang JJ, Lin JL, et al. Evolutional change in epicardial fat and its correlation with myocardial diffuse fibrosis in heart failure patients. J Clin Lipidol. 2017;11(6):1421–1431.
    1. Ng ACT, Strudwick M, van der Geest RJ, Ng ACC, Gillinder L, Goo SY, et al. Impact of epicardial adipose tissue, left ventricular myocardial fat content, and interstitial fibrosis on myocardial contractile function. Circ Cardiovasc Imaging. 2018;11(8):e007372.
    1. Rado SD, Lorbeer R, Gatidis S, Machann J, Storz C, Nikolaou K, et al. MRI-based assessment and characterization of epicardial and paracardial fat depots in the context of impaired glucose metabolism and subclinical left-ventricular alterations. Br J Radiol. 2019;92(1096):20180562.
    1. Nerlekar N, Muthalaly RG, Wong N, Thakur U, Wong DTL, Brown AJ, et al. Association of volumetric epicardial adipose tissue quantification and cardiac structure and function. J Am Heart Assoc. 2018;7(23):e009975.
    1. Ladeiras-Lopes R, Moreira HT, Bettencourt N, Fontes-Carvalho R, Sampaio F, Ambale-Venkatesh B, et al. Metabolic syndrome is associated with impaired diastolic function independently of MRI-derived myocardial extracellular volume: the MESA study. Diabetes. 2018;67(5):1007–1012.
    1. Yang FS, Yun CH, Wu TH, Hsieh YC, Bezerra HG, Liu CC, et al. High pericardial and peri-aortic adipose tissue burden in pre-diabetic and diabetic subjects. BMC Cardiovasc Disord. 2013;13:98.
    1. Christensen RH, von Scholten BJ, Hansen CS, Jensen MT, Vilsbøll T, Rossing P, et al. Epicardial adipose tissue predicts incident cardiovascular disease and mortality in patients with type 2 diabetes. Cardiovasc Diabetol. 2019;18(1):114.
    1. Al-Talabany S, Mordi I, Graeme Houston J, Colhoun HM, Weir-McCall JR, Matthew SZ, et al. Epicardial adipose tissue is related to arterial stiffness and inflammation in patients with cardiovascular disease and type 2 diabetes. BMC Cardiovasc Disord. 2018;18(1):31.
    1. Montalescot G, Sechtem U, Achenbach S, Andreotti F, Arden C, Budaj A, et al. 2013 ESC guidelines on the management of stable coronary artery disease: the Task Force on the management of stable coronary artery disease of the European Society of Cardiology. Eur Heart J. 2013;34(38):2949–3003.
    1. Hermann LK, Weingart SD, Yoon YM, Genes NG, Nelson BP, Shearer PL, et al. Comparison of frequency of inducible myocardial ischemia in patients presenting to emergency department with typical versus atypical or nonanginal chest pain. Am J Cardiol. 2010;105(11):1561–1564.
    1. Laufer EM, Mingels AM, Winkens MH, Joosen IA, Schellings MW, Leiner T, et al. The extent of coronary atherosclerosis is associated with increasing circulating levels of high sensitive cardiac troponin T. Arterioscler Thromb Vasc Biol. 2010;30(6):1269–1275.
    1. Cardinaels EP, Altintas S, Versteylen MO, Joosen IA, Jellema LJ, Wildberger JE, et al. High-sensitivity cardiac troponin concentrations in patients with chest discomfort: is it the heart or the kidneys as well? PLoS ONE. 2016;11(4):e0153300.
    1. Voskoboev NV, Larson TS, Rule AD, Lieske JC. Importance of cystatin C assay standardization. Clin Chem. 2011;57(8):1209–1211.
    1. Inker LA, Schmid CH, Tighiouart H, Eckfeldt JH, Feldman HI, Greene T, et al. Estimating glomerular filtration rate from serum creatinine and cystatin C. N Engl J Med. 2012;367(1):20–29.
    1. Agatston AS, Janowitz WR, Hildner FJ, Zusmer NR, Viamonte M, Jr, Detrano R. Quantification of coronary artery calcium using ultrafast computed tomography. J Am Coll Cardiol. 1990;15(4):827–832.
    1. Miller KD, Jones E, Yanovski JA, Shankar R, Feuerstein I, Falloon J. Visceral abdominal-fat accumulation associated with use of indinavir. Lancet (London, England). 1998;351(9106):871–875.
    1. Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pellikka PA, et al. Recommendations for chamber quantification. Eur J Echocardiogr. 2006;7(2):79–108.
    1. Gill CM, Azevedo DC, Oliveira AL, Martinez-Salazar EL, Torriani M, Bredella MA. Sex differences in pericardial adipose tissue assessed by PET/CT and association with cardiometabolic risk. Acta Radiol. 2018;59(10):1203–1209.
    1. Coisne A, Ninni S, Ortmans S, Davin L, Kasprzak K, Longere B, et al. Epicardial fat amount is associated with the magnitude of left ventricular remodeling in aortic stenosis. Int J Cardiovasc Imaging. 2019;35(2):267–273.
    1. Wu FZ, Huang YL, Wu CC, Wang YC, Pan HJ, Huang CK, et al. Differential effects of bariatric surgery versus exercise on excessive visceral fat deposits. Medicine. 2016;95(5):e2616.
    1. Gruzdeva O, Borodkina D, Uchasova E, Dyleva Y, Barbarash O. Localization of fat depots and cardiovascular risk. Lipids Health Dis. 2018;17(1):218.

Source: PubMed

3
Abonnieren