Correspondence *Department of Medicine, Cardiovascular Obesity Research and Management, McMaster University, Hamilton General Hospital, 237 Barton Street, East Hamilton, Ontario L8L 2X2, Canada

Email gianluca.iaco@tin.it

Introduction

A growing body of evidence suggests that regional fat distribution plays an important part in the development of an unfavorable metabolic and cardiovascular risk profile. Thus, the increased accumulation of visceral fat is now widely seen as a defining characteristic of the so-called metabolic syndrome.^{1, 2} The recognition that adipose tissue is a highly complex endocrine organ that generates various molecules with profound local and systemic effects has spawned a remarkable interest in adipose-tissue research.^{3, 4} Despite their similar qualitative properties, different types of adipose tissue, particularly subcutaneous and visceral adipose depots, are now recognized as having distinct quantitative characteristics.^{5, 6} While much of the interest has focused on the importance of intra-abdominal visceral fat, some extra-abdominal visceral fat depots, including mediastinal and epicardial fat, have also been studied.⁷ In this paper, we briefly review the rapidly emerging evidence pointing to a specific role for EPICARDIAL ADIPOSE TISSUE, both as a cardiac risk marker and as a potentially active player in the development of cardiac pathology.

Anatomic characteristics of epicardial adipose tissue

Students of human anatomy are familiar with the fact that variable amounts of fat cover the epicardial surface of the heart (Box 1).⁸ This is not true, however, for all species. Abundant fat can be found in guinea pigs, rabbits, larger mammals and humans. Little or no epicardial fat is, however, seen in laboratory rats and mice,⁹ which might partly explain why epicardial adipose tissue has been so poorly studied. The lack of epicardial fat in some species contradicts the notion that this tissue is of critical importance for the mechanical function of the heart. Similarly, there is no evidence to suggest that epicardial fat has any function in the mechanical protection of the heart from blunt trauma.

Where present, epicardial and intra-abdominal fat evolve from brown adipose tissue during embryogenesis.⁹ In the adult heart, fully differentiated white adipose tissue can be commonly found in the atrioventricular and interventricular grooves extending to the apex (Figures 1 and 2). Minor foci of fat are also located subepicardially in the free walls of the atria and around the two appendages. As the amount of epicardial fat increases, it progressively fills the space between the ventricles, sometimes covering the entire epicardial surface. A small amount of adipose tissue also extends from the epicardial surface into the myocardium, often following the adventitia of the coronary artery branches. Overall, there appears to be a close functional and anatomic relationship between the adipose and muscular components of the heart. These components share the same coronary blood supply, and no structures resembling a fascia (as found on skeletal muscle) separate the adipose and myocardial layers. This structure makes the accurate dissection of epicardial fat from the myocardium time consuming, if not impossible, especially in smaller animals. Contrary to what might be expected, there is little evidence to suggest that the extent of epicardial fat is strongly related to overall adiposity. Marchington et al.⁹ found no relationship between epicardial fat mass and the abundance of adipose tissue in other fat depots in a variety of wild and domesticated animals. This finding is in line with observations in humans from autopsy,^{10, 11} echocardiography^{12, 13} and MRI,^{14, 15} and suggests that epicardial fat is more closely related to visceral than total fat. Although autopsy examinations have revealed a relationship between epicardial fat and age,¹⁶ echocardiographic studies have not.^{12, 13}

Figure 1 Macroscopic appearance of epicardial fat.

(A) Anterior view of a normal (210 g) heart. (B) Posterior view of a normal (210 g) heart. (C) Anterior view of a hypertrophic (900 g) heart. (D) Posterior view of a hypertrophic (900 g) heart. In the normal heart, the fat distribution is limited to the atrioventricular and interventricular grooves, and along the major coronary branches (A, B). In the hypertrophic heart—the hypertrophy is mainly on the right-hand side—the adipose tissue also fills the epicardial spaces between these sites. Scale bar = 4 cm.

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Figure 2 Microscopic appearance of epicardial fat.

(A) Microscopic appearance of the epicardial layer in the left ventricle. (B) Microscopic appearance of the epicardial layer in the right ventricle. The arrow shows the islands of mature adipocytes. No fascial structure divides the epicardial adipose tissue from the underlying myocardium. Mature adipocytes are more frequent in the right-hand side than the left and might be seen within the subepicardic myocardium. Scale bar = 1 mm.

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Despite the prominence of epicardial fat, descriptive studies in humans and knowledge of its relationship to normal cardiac anatomy and pathology remain limited. In the 1950s and 1960s, Reiner et al.^{17, 18, 19, 20} and other researchers^{21, 22} studied epicardial adipose tissue in normal, hypertensive and ischemic hearts. Their findings showed that epicardial fat constitutes a significant cardiac component. In a later study of 117 human hearts at autopsy, Corradi et al.¹⁰ investigated the relationship between ventricular myocardial and epicardial fat in normal hearts and those that were ischemic, hypertrophic, or both. Left, right and total ventricular fat weights were significantly greater in hypertrophic hearts, but there was no relationship to ischemia. Epicardial fat located over both ventricles accounted for around 20% of the total ventricular mass in all groups. Although left ventricular mass far exceeds that of the right ventricle, the absolute amount of fat tissue was similar in the right and left ventricles. As a result, the ratio of fat to myocardium weight for the right side of the heart was more than three times that of the left side: the mean weight of fat per 1 g muscle mass in the right ventricle was 0.61 g in women and 0.48 g in men, whereas the values in the left ventricle were 0.17 and 0.15 g. Although in nonhypertrophied hearts there was a significant correlation between BMI and the total epicardial fat weight (P <0.05), this was not the case in hypertrophied hearts. Corradi et al. thus concluded that a constant ratio of fat to muscle exists in each ventricle, which is not influenced by ischemia or hypertrophy. The positive relationship between the amount of epicardial fat and ventricular myocardial mass was also noted in an echocardiographic study by Iacobellis et al.²³ in 60 healthy individuals with a wide range of adiposity. Autopsy and echocardiographic findings strongly suggest, therefore, that an increase in myocardial mass during cardiac hypertrophy is associated with a consensual and proportional increase in epicardial adipose mass.

Biochemical properties and adipokine production of epicardial adipose tissue

The presence of excessive epicardial fat adds to the weight of the ventricles and increases the effort involved in pumping blood around the body. Why should such an energy store be located in this vital organ? Lean wild animals have at least as much epicardial fat as domesticated animals and this tissue is not depleted during starvation.²⁴ Epicardial fat might, therefore, have important functions that go beyond the storage of excess calories.

The biochemical properties of epicardial adipose tissue have been studied in animal models and humans (Box 1). In young adult guinea pigs, the rate of free-fatty-acid synthesis, release and breakdown in response to catecholamines by the rather small amount of epicardial adipose tissue was markedly higher than in other adipose depots.⁹ The high lipolysis observed in epicardial adipose tissue might be due to several factors.²⁵ The reduced antilipolytic effect of insulin in visceral adipose tissue and the increased activity of -adrenergic receptors, especially 3 receptors, could be evoked as possible mechanisms. In guinea pigs, the protein content of epicardial fat is higher than that of perirenal and popliteal depots. Nevertheless, no differences in the mitochondrial content among fat depots have been observed, which suggests a weak oxidative capacity of epicardial fat.⁹ Data from monkeys also show that the maximum capacity of glucose use is similar or less than that of abundant fat depots.

The close anatomic relationship of epicardial adipose tissue to the adjacent myocardium suggests possible local interactions between these tissues. Under physiologic conditions, epicardial adipose tissue is thought to act as a buffering system against toxic levels of fatty acids between the myocardium and the local vascular bed.⁹ Thus, increased epicardial fat could scavenge excess fatty acids, which interfere with the generation and propagation of the contractile cycle of the heart, causing ventricular arrythmias and alterations in repolarization.^{26, 27, 28, 29} By contrast, the high lipolytic activity of epicardial fat suggests that this tissue might also serve as a ready source of free fatty acids to meet increased myocardial energy demands, especially under ischemic conditions.

Adipose tissue is now well recognized as an important source of a number of bioactive molecules that can profoundly affect energy metabolism as well as vascular, immunologic and inflammatory responses. Many of these factors have cytokine-like properties and, therefore, the term adipokines is now often used to describe them. Mazurek et al.³⁰ compared epicardial and subcutaneous adipose tissues harvested at the outset of elective coronary artery bypass grafting. They found that epicardial adipose tissue expresses a wide range of inflammatory mediators.³⁰ Thus, epicardial adipose tissue had a significantly higher expression of chemokines (MONOCYTE CHEMOTACTIC PROTEIN-1) and several inflammatory cytokines (including interleukin-1, interleukin-6 and interleukin-6 soluble receptor, and tumor necrosis factor-) than subcutaneous fat. These findings were paralleled by the presence of inflammatory cell infiltrates in epicardial adipose stores. On the basis of these observations, Mazurek et al.³⁰ proposed that adipocyte-derived tumor necrosis factor- acts in an autocrine way, impairing signaling via the insulin receptor and increasing lipolysis. The subsequent release of nonesterified fatty acids might contribute to insulin resistance in peripheral tissues, such as adipose and muscle tissue, the liver and the heart. Interestingly, no relationship was seen between epicardial adipose-tissue inflammation and diabetes, obesity and plasma LDL levels, or the intake of statins, angiotensin-converting enzyme inhibitors or angiotensin-receptor blockers in this population. Iacobellis et al.³¹ showed that expression of ADIPONECTIN, an adipocyte-derived protein that has profound anti-inflammatory and antiatherogenic properties, was around 40% lower in the epicardial adipose tissue of patients with coronary artery disease than in that of normal controls. This finding was independent of BMI and age. Increased expression of RESISTIN, another adipocyte-secreted factor that is strongly linked with insulin resistance, has also been observed in human epicardial fat.³²

Several mechanisms can be suggested to explain the production of inflammatory cytokines by epicardial adipose tissue. Increased generation of radical oxygen species in response to regional ischemia and depressed myocardial function could activate oxidant-sensitive inflammatory signals in visceral adipose tissue in adjacent adipose stores.^{33, 34} The increased presence of inflammatory cells in epicardial adipose tissue could also reflect a response analogous to the inflammatory infiltrates found in the adventitia and perivascular regions adjacent to advanced atherosclerotic lesions.^{35, 36, 37} Mazurek et al.³⁰ suggested that the presence of inflammatory mediators, such as tumor necrosis factor-, in the tissues surrounding human epicardial coronary arteries could lead to amplification of vascular inflammation, plaque instability via apoptosis, and neovascularization. Periadventitial application of endotoxin, monocyte chemotactic protein-1, interleukin-1 or oxidized LDL induces inflammatory cell influx into the arterial wall, coronary vasospasm or intimal lesions. This action suggests that bioactive molecules from the pericoronary tissues alter arterial homeostasis.^{38, 39} Perivascular adipose tissue has also been shown to release factors that might profoundly modulate vascular function⁴⁰ and, possibly, myocardial function. Other potential consequences of the inflammatory reaction derived from epicardial adipose tissue could be beneficial, such as the stimulation of an angiogenic response and the development of collateral circulation in patients with obstructive coronary artery disease.³⁰ Nevertheless, as an increase in inflammatory factors in epicardial fat was observed only in patients undergoing coronary artery bypass grafting, these findings remain to be confirmed in healthy individuals.

Clinical assessment of epicardial adipose tissue

Although epicardial fat is readily visualized on high-speed CT and MRI, widespread use of these methods for its assessment is not practical. Iacobellis et al.^{12, 13} proposed the use of echocardiography for the direct assessment of epicardial adipose tissue. The thickness of epicardial fat was measured on the free wall of the right ventricle from both parasternal long-axis and short-axis views (Figure 3). Imaging constraints were used to ensure that the epicardial fat thickness was not measured obliquely. Measurements were also made of M-MODE STRIPS obtained from both two-dimensional views, with longitudinal cursor-beam orientation in each. The maximum values at any site were measured and the average value considered.

Figure 3 Echocardiographic imaging of epicardial adipose tissue.

Epicardial adipose tissue appears more frequently as an echo-free space than as a hyperechoic space. (A) Modified parasternal view showing epicardial adipose tissue (massive; arrows) on the free wall of the right ventricle in a patient with severe visceral obesity and obstructive lung disease. (B) Parasternal view showing epicardial fat in an overweight person with predominant subcutaneous adiposity. AO, aorta; LA, left atrium; LV, left ventricle; RV, right ventricle.

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The reliability of the measurements of epicardial fat thickness taken from different views was excellent. Epicardial adipose tissue appears as an echo-free or hyperechoic space if it is massive. The measurement of epicardial fat on the right ventricle was chosen for two reasons: first, this point is recognized as having the highest absolute thickness of epicardial fat;¹⁶ and second, parasternal long-axis and short-axis views allow the most accurate measurement of epicardial adipose tissue on the right ventricle, with optimum cursor-beam orientation in each view. Hypertrophy of the right-ventricle trabecula and moderator band, if present, did not confound epicardial adipose tissue calculation. Echocardiographic calculation of adipose tissue on the free wall of the right ventricle also showed good reliability with the MRI epicardial adipose-tissue measurements (Figure 4). Overall, these studies suggest that echocardiographic assessment of epicardial fat might be a simple and practical measure of this tissue in clinical practice and research.

Figure 4 MRI of epicardial adipose tissue.

Epicardial adipose tissue in a patient with severe visceral obesity. The magnetic resonance scans were obtained by TSET1-weighted sequences with oblique axial orientation for a correct study of the four cardiac chambers. A 10 mm thick section with a 1 mm intersection gap, 370° field of view and 256 256 matrix is shown.

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Reliability of echocardiographic assessment to measure visceral adiposity

Increased waist circumference is now widely accepted as a surrogate measure of visceral abdominal obesity and a marker of an adverse metabolic profile associated with high cardiovascular risk.⁴¹ Waist circumference could be confounded, however, by large amounts of subcutaneous fat, particularly in severely obese people, although few studies have measured its relationship with intra-abdominal fat in obesity.^{42, 43, 44} Some of these studies found weak or nonsignificant correlations between waist circumference and intra-abdominal fat, particularly in obese men.^{42, 43, 44} Moreover, high variability within and between examiners might limit the usefulness of this feature for the monitoring of slight variations in abdominal adiposity. In addition, waist circumference seems to quantify subcutaneous fat better than visceral fat,⁴⁵ and might be a less-reliable measure in older than in younger individuals.⁴⁶ Considerable interest has been shown, therefore, in developing more- reliable measures of visceral obesity.^{47, 48}

Iacobellis et al.¹³ have shown that increased epicardial fat is associated with several features of metabolic syndrome, including significant correlations with LDL cholesterol, fasting insulin, adiponectin and arterial blood pressure. Individuals with impaired insulin sensitivity and low adiponectin levels had the highest epicardial fat thickness, irrespective of BMI. Given the poor sensitivity and specificity of waist circumference as a measure of visceral adiposity, echocardiographic measurement of visceral adipose tissue might provide a more-sensitive and more-specific measure of the true visceral fat content. This method might also avoid the possible confounding effect of increased subcutaneous abdominal fat thickness.¹²

The fact that echocardiography is routinely performed in high-risk cardiac patients means that this objective measure could be readily available at no extra cost. Echocardiographic assessment of epicardial visceral fat would be less expensive than MRI or CT and would provide data on cardiac parameters that can be useful in the clinical management of patients with metabolic syndrome. Nevertheless, further studies demonstrating that the echocardiographic measurement of changes in epicardial fat accurately reflect changes in intra-abdominal fat will be required to judge the full potential impact of using this measure to monitor visceral adiposity. Future studies are needed to clarify the relationship between epicardial fat and increased cardiovascular morbidity and mortality.

Conclusions and perspectives

Although there have been relatively few studies of epicardial fat, the evidence reported so far suggests that epicardial adipose tissue is anatomically and clinically related to cardiac morphology and function. Indeed, epicardial fat is a metabolically active organ that generates a variety of bioactive molecules, which could significantly affect cardiac function. The close anatomic relationship of epicardial adipose tissue to the adjacent myocardium could suggest paracrine regulation by this small fat depot, although the relationship could not exclude systemic control. Furthermore, as the epicardial adipose mass reflects intra-abdominal visceral fat, we propose that echocardiographic assessment of this tissue might serve as a reliable marker of visceral adiposity. Further studies of this neglected tissue and its relationship with cardiac function, as well as of its use as a marker of metabolic and cardiovascular risk, should be encouraged.

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Subject areas under which this article appears: Disease markers