COMMENTARIES

Role of Epicardial Adipose Tissue in Atherosclerosis and Coronary Artery Disease

Gianluca Iacobellis, M.D., Ph.D.,
Associate Professor of Endocrinology,
Department of Medicine, Cardiovascular Obesity Research and Management,
McMaster University, Hamilton, ON,
Canada

Please address correspondence to:
Dr. Gianluca Iacobellis
Department of Medicine
St. Joseph's Hospital
50 Charlton Avenue East, 5th Fontbonne Bldg
Hamilton, ON
Canada, L8N 4A6
Tel: 905-522-1155-3966
Fax: 905-521-6068
E-mail: gianluca@ccc.mcmaster.ca  or  gianluca.iaco@tin.it

The reason for the growing scientific interest into the fat is the widely-accepted acknowledgement that adipose tissue is not a silent organ, but a very active source of multiple bioactive cytokines, called adipokines. The adipocyte, mini-organ within this neglected organ, sends outputs (adipokines) and accepts inputs (nuclear receptors). The adipose tissue communicates with almost all other organs through endocrine, paracrine, and also autocrine interactions. Hence, both systemic and local regulations of internal organs’ function and morphology have been recently attributed to the adipose tissue. Fat tissue is also a potential great responder, by the presence of multiple receptors that can be modulated, stimulated, or inhibited by drugs with different mechanisms of action and therapeutic purposes. Of additional and supportive note is the fact that the adipose tissue can now be clinically measured and quantified by simple, accurate and reliable diagnostic tools. Both biological and clinical characteristics of the adipose tissue seem to warrant a successful development of new therapeutic strategies.

The concept and importance of proximity of adipose tissue to the organs is also intriguing. Intuitively, the visceral adipose tissue has been evoked as the most desirable therapeutic target. In fact, great interest has been recently focused on the visceral adiposity, namely the fat depots that surround the internal organs. The evidence supporting the visceral adiposity as an independent cardiometabolic risk factor are rapidly emerging.

The scientific and clinical interest in epicardial adipose tissue, the visceral fat located around the heart, is young, but rapidly emerging [1-2]. The presence of adipose tissue on the myocardium and around the great vessels has been recognized by human anatomists at least since the mid-nineteenth century. Nevertheless, its potential role as marker of visceral adiposity and cardiovascular risk factor by itself has only recently been considered. This small visceral fat, previously neglected or rapidly removed by the cardiac surgeons, seems to play as a principal actor, due to its proximity to the heart. We and others showed that epicardial fat is a metabolically active organ and source of several bioactive molecules as well as adiponectin, tumor necrosis factor-alpha (TNF-α), interleukin 1 (IL1), interleukin (IL6), nerve growth factor (NGF), resistin, and free fatty acids, that might substantially affect cardiovascular morphology and function [3-7]. Because the close anatomical relationship to the heart and the absence of fascial boundaries, epicardial adipose tissue may locally interact and modulate the coronary arteries and myocardium through paracrine and direct secretion of anti and pro-inflammatory adipokines [1,8-9]. Paradoxically, a double role, unfavorable and protective, has been also attributed to the cardiac fat. Macrophage infiltration into epicardial fat has been found in subjects with coronary artery disease, suggesting a condition of chronic inflammation in this small cardiac fat depot [4]. Several mechanisms could be evoked to explain the inflammatory cytokine production from epicardial adipose tissue. The regional ischemia could activate visceral adipose tissue oxidant-sensitive inflammatory signals in adjacent adipose stores.

The presence of inflammatory cells in epicardial adipose tissue could also reflect the response to plaque rupture and lead to amplification of vascular inflammation and plaque instability via apoptosis and neovascularization. Of note is our previous observation that human epicardial adipose tissue expresses adiponectin and adiponectin expression is significantly higher in epicardial fat isolated from subjects with normal coronary arteries than in patients with severe coronary artery disease [3]. Thus epicardial fat could also exert favorable effects on the adjacent coronary artery through increased adiponectin production. Recently, epicardial fat thickness was significantly correlated with the severity of coronary artery disease in patients with known coronary artery disease [10]. Different adiponectin secretions from the cardiac fat could be evoked among the potential explanatory mechanisms

          Epicardial fat is clinically related to coronary artery disease, atherosclerosis, and major anthropometric and metabolic predictors of increased cardiovascular risk [11-13]. We recently showed that epicardial adipose tissue, an index of cardiac adiposity is signficantly related to carotid intima-media thickness (IMT), an index of subclinical atherosclerosis, in HIV-infected patients [14-15]. Higher epicardial fat thickness is linearly related to higher left ventricular mass and carotid ITM thickness. The former association could be explained by the closeness of the epicardial fat pad to the myocardium and by paracrine interactions. In fact, both autopsy [9] and echocardiographic findings showed that increases in left ventricle hypertrophy [16] and also in atrial dimensions [17] are associated with a consensual and proportional increase in epicardial adipose mass. However, the relationship of epicardial fat and carotid-IMT could suggest different mechanisms. Because epicardial fat reflects cardiac and visceral adiposity, as we previously demonstrated [11,18] our findings are consistent with the evidence supporting the importance of visceral adiposity in the development of cardiovascular diseases. It is well known that increased visceral fat, as observed in HIV-infected patients is associated with higher cardiometabolic risk and accelerated atherosclerosis.

We proposed and validated echocardiography for the direct assessment of epicardial adipose tissue [18]. Echocardiographic epicardial fat measurement may have some advantages as an index of high cardiometabolic risk. As echocardiography is routinely performed in high-risk cardiac patients, this objective non-invasive measure may be readily available at no extra cost. Our previous studies clearly showed that echocardiographic epicardial fat strongly correlates with abdominal visceral fat measured by magnetic resonance imaging (MRI) [18]. Echocardiographic assessment of epicardial visceral fat would certainly be less expensive than MRI or computed tomography. Given that epicardial fat reflects visceral adiposity, its echocardiographic measurement has been used as therapeutic target in subjects underwent bariatric surgery [19] and in treatment with medications able to modulate and affect adipose tissue, particularly the visceral depots [20]. Intuitively, thiazolidinediones (TZDs), fibrates, angiotensin type 1 receptor blockers (ARBs), and anti-obesity medication, as well as sibutramine, orlistat, and rimonabant, could be targeted to the echocardiographic epicardial fat thickness.

Further studies on the role of epicardial adipose tissue in atherosclerosis and coronary artery disease can open new avenues in cardio-endocrinology research. Echocardiographic epicardial fat measurement may have the potential to be a reliable and easy diagnostic marker of increased visceral adiposity and cardiovascular risk and an effective therapeutic target for treatments modulating the adipose tissue.

References

  1.    Iacobellis G, Corradi D, Sharma AM. Epicardial adipose tissue: anatomic, biomolecular and clinical relationships with the heart. Nat Clin Pract Cardiovasc Med 2005;2:536-43.
  2.    Iacobellis G, Pond CM, Sharma AM. Different "weight" of cardiac and general adiposity in predicting left ventricle morphology. Obesity (Silver Spring). 2006;14:1679-84.
  3.    Iacobellis G, Pistilli D, Gucciardo M, et al. Adiponectin expression in human epicardial adipose tissue in vivo is lower in patients with coronary artery disease. Cytokine 2005;29:251-55.
  4.    Mazurek T, Zhang L, Zalewski A, et al. Human epicardial adipose tissue is a source of inflammatory mediators. Circulation 2003;108:2460-66.
  5.    Baker AR, Silva NF, Quinn DW, et al. Human epicardial adipose tissue expresses a pathogenic profile of adipocytokines in patients with cardiovascular disease. Cardiovasc Diabetol 2006;13:1.
  6.    Chaldakov GN, Fiore M, Stankulov IS, et al. Neurotrophin presence in human coronary atherosclerosis and metabolic syndrome: a role for NGF and BDNF in cardiovascular disease? Prog Brain Res 2004;146:279-89.
  7.    Kremen J, Dolinkova M, Krajickova J, et al. Increased subcutaneous and epicardial adipose tissue production of proinflammatory cytokines in cardiac surgery patients: possible role in postoperative insulin resistance. J Clin Endocrinol Metab 2006;91:4620-27.
  8.    Schejbal, V. Epicardial fatty tissue of the right ventricle: morphology, morphometry and functional significance Pneumologie 1989;43,490-99.
  9.    Corradi D, Maestri R, Callegari S, et al. The ventricular epicardial fat is related to the myocardial mass in normal, ischemic and hypertrophic hearts. Cardiovasc Pathol 2004;13:313-16.
  10.    Jeong JW, Jeong MH, Yun KH, et al Echocardiographic epicardial fat thickness and coronary artery disease. Circ J 2007;71:536-39.
  11.    Iacobellis G, Ribaudo MC, Assael F, et al. Echocardiographic epicardial adipose tissue is related to anthropometric and clinical parameters of metabolic syndrome: a new indicator of cardiovascular risk. J Clin Endocrinol Metab 2003;88:5163-68.
  12.    Iacobellis G, Leonetti F. Epicardial adipose tissue and insulin resistance in obese subjects.J Clin Endocrinol Metab 2005;90:6300-302.
  13.    Kankaanpaa M, Lehto HR, Parkka J, et al. Myocardial triglyceride content and epicardial adipose mass in human obesity: relationship to left ventricular function and serum free fatty acid levels. J Clin Endocrinol Metab 2006;91:4689-95.
  14.    Iacobellis G, Pellicelli AM, Sharma AM, Grisorio B, Barbarini G, Barbaro G. Relation of subepicardial adipose tissue to carotid intima-media thickness in patients with human immunodeficiency virus. Am J Cardiol 2007;99:1470-72.
  15.    Iacobellis G, Sharma AM, Pellicelli AM, Grisorio B, Barbarini G, Barbaro G. Epicardial adipose tissue is related to carotid intima-media thickness and visceral adiposity in HIV-infected patients with highly active antiretroviral therapy-associated metabolic syndrome. Curr HIV Res 2007;5:275-79.
  16.    Iacobellis G, Ribaudo MC, Zappaterreno A, Iannucci CV, Leonetti F. Relation between epicardial adipose tissue and left ventricular mass. Am J Cardiol 2004;94:1084-87.
  17.    Iacobellis G, Leonetti F, Singh N, Sharma AM. Relationship of epicardial adipose tissue with atrial dimensions and diastolic function in morbidly obese subjects. Int J Cardiol 2007;115:272-73.
  18.    Iacobellis G, Assael F, Ribaudo MC, et al. Epicardial fat from echocardiography: a new method for visceral adipose tissue prediction. Obes Res 2003;11:304-10.
  19.    Willens HJ, Byers P, Chirinos JA, Labrador E, Hare JM, de Marchena E. Effects of weight loss after bariatric surgery on epicardial fat measured using echocardiography. Am J Cardiol 2007;99:1242-45.
  20.    Lanes R, Soros A, Flores K, Gunczler P, Carrillo E, Bandel J. Endothelial function, carotid artery intima-media thickness, epicardial adipose tissue, and left ventricular mass and function in growth hormone-deficient adolescents: apparent effects of growth hormone treatment on these parameters. J Clin Endocrinol Metab 2005;90:3978-82.

 

 

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