INTRODUCTION

Obesity is an increasing public health problem that is associated with cardiovascular death [12]. The metabolically deleterious form of obesity is associated with ectopic lipid deposition in multiple tissues, including the heart [345]. Epicardial adipose tissue (EAT) is defined as the adipose tissue between the myocardium and the visceral layer of the pericardium [67]. Epicardial fat covers 80% of the heart's surface and constitutes 20% of the total heart weight. EAT is present along the coronary arteries and over the right ventricle, especially along the acute margin and atrioventricular and interventricular grooves (IVGs) [38]. Because of its anatomical contiguity to the heart, epicardial fat can locally modulate the myocardium and coronary arteries [91011].

Epicardial fat is involved in lipid and energy homeostasis with a substantial capacity for free fatty acid release and uptake and a low rate of glucose utilization [11]. Central obesity and insulin resistance are the key components of metabolic syndrome (MS) [121314]. EAT is a type of visceral adipose tissue that plays an important role in the progression of MS [1516]. The amount of EAT within an individual has been correlated with MS components [71718].

Epicardial fat can be measured with imaging techniques such as echocardiography, cardiac magnetic resonance imaging (MRI), or multidetector computed tomography (MDCT) [11]. MDCT can provide a more accurate measurement of fat around the heart than can other techniques because of its high temporal resolution [19]. Because epicardial fat volume (EFV) measurements require short-axis reformatting and manual tracing of the pericardium, which is time-consuming [5], the epicardial fat area (EFA) was suggested as a simple and quick method for representing EFV [19]. Additionally, measuring the EAT thickness is more convenient and easier than measuring the amount of EAT.

Previous studies have examined the relationship between EAT thickness measured by MDCT and MS [717]. However, no study has investigated the relationship between region-specific EAT thickness measured by MDCT and MS in Korean adults. We aimed to devise a simple method for representing EAT and to examine differences in EAT thickness according to the presence of type 2 diabetes mellitus or obesity in Korean adults.

METHODS

Subjects

We enrolled a total of 94 patients (42.6% with type 2 diabetes mellitus, 53.2% obese, mean age 61±13 years) who were suspected of having coronary artery disease and who underwent MDCT in clinics at Ewha Womans University Mokdong Hospital between March 2012 and June 2013. Subjects were divided into four groups according to presence of type 2 diabetes mellitus or obesity. Diagnoses of type 2 diabetes mellitus were based on American Diabetes Association criteria [20]. Body mass index (BMI) was categorized as <25 and ≥25 kg/m², which is the cut-off point for obesity in Asian populations [21]. None of our subjects had pericardial effusion. Smoking status was classified as no history of smoking or as a current smoker. Those who had stopped smoking for more than 1 year before the examination were considered to be nonsmokers. The institutional review board of Ewha Womans University Mokdong Hospital approved this study.

Methods

Height and weight were measured for all subjects, and BMI was calculated as weight (kg)/height (m)². The blood pressure was calculated as the mean of two manual sphygmomanometer readings with the patient in the seated position.

After an overnight fast of at least 8 hours, a venous blood sample was obtained from each subject. The total serum cholesterol, triglycerides, low density lipoprotein cholesterol (LDL-C), and high density lipoprotein cholesterol (HDL-C) levels were measured using an enzymatic assay on an automated analyzer (Hitachi 7150 Automatic Chemistry Analyzer; Hitachi, Tokyo, Japan). The fasting glucose levels were measured via the glucose oxidase method (Beckman Model Glucose Analyzer 2; Beckman Instruments, Fullerton, CA, USA). Glycosylated hemoglobin (HbA1c) was measured using high-performance liquid chromatography assays standardized to Diabetes Control and Complications Trial values (Tosoh Corp., Kyoto, Japan).

All CT images were obtained using a dual-source multidetector row scanner (SOMATOM Definition Flash; Siemens Medical Solutions, Forchheim, Germany). The heart computed tomography (CT) scan was obtained using prospective electrocardiogram gating (step-and-shoot technique). Diastolic images were used for analysis. We analyzed CT images with 0.75-mm thick slices. We were able to clearly identify the pericardium using a dual-source multidetector row scanner. All of the EAT measurements were completed by one radiologist. In a previous study, EFAs at several anatomical landmarks were correlated with the EFV, and the EFA at the left main coronary artery (LMCA) level showed an excellent correlation with EFV [19]. We used the origin of the LMCA as an anatomical landmark to measure EFA (Fig. 1C).

EAT thickness was measured on the parasternal short (Fig. 1A) and horizontal long axis views (Fig. 1B). EAT thickness over the right ventricular (RV) free wall was measured at three equally spaced points along the RV free wall on the basal short-axis plane. The mean of the three measurements was used for analyses. The maximal EAT thickness over the RV free wall was determined from the myocardial surface to the pericardium. The EAT thicknesses over the RV superior wall and left ventricular (LV) lateral wall were measured on the parasternal short axis view. EAT thicknesses in the grooved segments were measured at three sites on the horizontal long-axis plane (right atrioventricular groove [RAVG], left atrioventricular groove [LAVG], and IVG) and at two sites on the basal short-axis plane (superior and inferior IVG). The mean and maximal EAT thicknesses over the RV anterior wall and EAT thicknesses on the RV apex and LV apex were measured on the horizontal long axis view.

Statistical analysis

Statistical analyses were performed using the SPSS version 18.0 (SPSS Inc., Chicago, IL, USA). Data are presented as percentages for categorical variables and as the means±standard deviations for continuous variables. For comparisons of the mean in two groups, we used an unpaired t-test. The chi-square test was used to examine differences among categorical variables. Multigroup comparisons of variables were performed using one-way analysis of variance followed by a Bonferroni correction for post hoc analysis. To adjust the EAT values for BMI between subjects with type 2 diabetes mellitus and subjects without type 2 diabetes mellitus and to adjust the EAT values for type 2 diabetes mellitus status between obese subjects and nonobese subjects, we used analysis of covariance. Correlations between EFA and EAT thickness and between the EAT values and metabolic components were examined by Pearson correlation analysis. To determine the factors associated with EAT thickness in LAVG, a multiple linear regression analysis was performed. Statistical significance was assessed at P<0.05, and then adjusted for multiple comparisons by the Bonferroni method.

RESULTS

The subjects (n=94) had a mean age of 61±13 years. Among them, 42.6% (n=40) had type 2 diabetes mellitus and 53.2% (n=50) were obese. The clinical and biochemical characteristics of the study subjects are shown in Table 1. The mean age; systolic and diastolic blood pressure; total cholesterol, triglycerides, HDL-C, and LDL-C values; presence of plaque or stenosis of coronary arteries by MDCT; and the proportion of current smokers did not differ among the four groups (P>0.05). The proportion of males was highest in the group with type 2 diabetes mellitus and without obesity (75% vs. 33.3%, 38.5%, and 35.7%; P<0.05). The HbA1c values did not significantly differ between the obese subjects and nonobese subjects with type 2 diabetes mellitus (7.3±2.0 vs. 8.4±2.29, P>0.05).

All of the EAT thicknesses were correlated with EFA at the LMCA level (r=0.235 to 0.613, P<0.05), and the EAT thicknesses in the LAVG had the highest correlation coefficient (r=0.613) (Table 2). BMI was positively correlated with EFA at the LMCA level (r=0.411, P<0.001) and the EAT thickness in the LAVG (r=0.450, P<0.001). Systolic and diastolic blood pressure, triglycerides, total cholesterol, LDL-C, gender, and smoking status were not correlated with EFA at the LMCA level or EAT thickness in the LAVG.

The groups with obesity (with or without type 2 diabetes mellitus) had significantly higher EFA values at the level of LMCA than did the group without type 2 diabetes mellitus and obesity (17.0 mm, 13.7 mm vs. 8.4 mm, P<0.05). The group with type 2 diabetes mellitus and obesity had higher EAT thickness values in the RAVG (19.1 mm vs. 16.1 mm) and the LV apex (4.8 mm vs. 3.3 mm) than did the group without type 2 diabetes mellitus and obesity (P<0.05). The group with type 2 diabetes mellitus and obesity had higher EAT thickness values in the LV apex than did the group without type 2 diabetes mellitus and with obesity (4.8 mm vs. 3.5 mm, P<0.05). In addition, the mean EAT thickness in the LAVG was lowest in the group without type 2 diabetes mellitus and obesity (8.8 mm vs. 13.0 mm, 11.8 mm, and 11.8 mm, P<0.05). Except for EAT thicknesses over the RAVG, the LAVG, and the LV apex, the EAT thicknesses did not differ among the four groups (Table 3).

The EAT thicknesses over the LV lateral wall (3.3±1.7 vs. 2.6±1.6), the RAVG (18.0±3.8 vs. 16.2±4.0), and the LAVG (12.0±3.2 vs. 9.9±2.6) in subjects with coronary artery stenosis were greater than in those subjects without coronary artery stenosis by MDCT (P<0.05). Except for the EAT thicknesses over the LV lateral wall, the RAVG, and the LAVG, the EAT thicknesses did not differ between subjects with and without coronary artery stenosis on MDCT. Because our study was a retrospective study, we could not determine the incidence of cardiovascular diseases in our subjects. When we performed the study, 10 subjects (10.6%) were clinically diagnosed with acute coronary syndrome, such as unstable angina, non-ST-elevation myocardial infarction, or ST-elevation myocardial infarction. The EAT thicknesses over the RAVG, the LAVG, and the LV apex in subjects with acute coronary syndrome were greater than in those subjects without acute coronary syndrome (data not shown).

In the group with type 2 diabetes mellitus, there were no correlations between the EAT values and type 2 diabetes mellitus duration or HbA1c levels. When adjusted for BMI, the EFA values at the LMCA level and the EAT thickness in the RAVG and LAVG and the maximal EAT thickness over the RV anterior wall were higher in the group with type 2 diabetes mellitus than in the group without type 2 diabetes mellitus (P<0.05) (Table 4). When adjusted for type 2 diabetes mellitus, the EFA at the LMCA level and the EAT thicknesses in the RV superior wall, RAVG, and LAVG were higher in the obese group than in the nonobese group (P<0.05) (Table 5).

In multiple linear regression analysis, age, type 2 diabetes mellitus, and BMI were significantly associated with the EAT thickness in LAVG when adjusted for gender, smoking status, systolic blood pressure, triglycerides, and plaque or stenosis of coronary arteries by MDCT (P<0.05) (Table 6).

DISCUSSION

We demonstrated that all of the EAT thicknesses were correlated with the EFA at the LMCA level and that the EAT thicknesses in the LAVG had the highest correlation coefficient. The EAT thickness in the LAVG was significantly associated with type 2 diabetes mellitus and obesity independently.

Precise measurement of EAT is a challenge. Standardized measurement of EFV is difficult due to anatomical variations. The echocardiographic epicardial fat measurement is noninvasive and readily available. However, echocardiography cannot provide an adequate window of all cardiac segments and is inadequate, especially in obese patients. Additionally, this method has poor reproducibility [22]. Because volumetric measurements using MDCT and cardiac MRI are accomplished by manually tracing fat in slices and then summing the individual volume measurements, measurement of the EFV in this manner is time-consuming and cumbersome [23]. In a previous study, EFAs at several anatomical landmarks were correlated with the EFV. Among the EFAs, the EFA at the LMCA level showed an excellent correlation with EFV [19]. In our study, all of the EAT thicknesses measured by MDCT were well correlated with the EFA in LMCA. Measuring the EAT thickness would be a convenient and easy method to measure the amount of EAT.

EAT is a metabolically active organ producing bioactive molecules, free fatty acids, and adiponectin. EAT is suggested to play an important role in the progression of MS. EAT thickness was related to the main anthropometric and clinical parameters of MS [71724252627]. The association between EFV and components of MS was evaluated in patients with type 2 diabetes mellitus [18]. Additionally, the echocardiographic EAT thickness was significantly associated with all of the indices of insulin resistance and glucose intolerance measured in obese subjects [28]. In a study with nondiabetic subjects, the EAT thickness was correlated with fasting plasma glucose [29]. Cardiac steatosis measured with the myocardial triglycerides contents was associated with insulin resistance [3031]. Increased EAT thickness, as assessed by MRI, was an independent risk factor for significant coronary artery stenosis in asymptomatic type 2 diabetes mellitus patients [32]. Consistent with previous studies, we demonstrated that the amount of EAT measured by MDCT was associated with the presence of type 2 diabetes mellitus and obesity. It is possible that the EAT thickness varies according to the severity of diabetes mellitus. However, we did not compare the EAT thickness according to glycemic control status. To the best of our knowledge, no study has examined differences in EAT thicknesses according to glycemic control status. Further studies are required to determine differences in EAT thicknesses according to the severity of diabetes mellitus.

Several studies have examined the EAT thickness in subjects with MS. The relationship between region-specific EAT thickness and MS is controversial. The distribution of EAT is primarily concentrated in the grooves [16]. Previous studies demonstrated that the relationship between EAT measured by MDCT and MS were region-specific and mostly correlated at the LAVG level [3334]. In a separate study, the EAT thicknesses in all of the regions evaluated were correlated with MS parameters [17]. The results of our study demonstrated that the EAT thickness, especially in the LAVG, was associated with type 2 diabetes mellitus and obesity. In particular, the EAT thickness in the LAVG was highly correlated with EFA. The relationships between the EAT thickness and type 2 diabetes mellitus as well as obesity can be attributed to the amount of fat accumulated in the LAVG. Because there is a substantial amount of fat around the great cardiac vein traversing the LAVG, the EAT thickness in the LAVG could be associated with type 2 diabetes mellitus as well as obesity. The distribution of EAT is asymmetric, and the importance of the EAT thicknesses may vary according to the regions. Unlike the results of our study, the EAT thickness at the RAVG, as measured by MRI, was a useful marker for differentiating inflammatory status among obese men with MS [35]. However, the method to measure EAT thicknesses and the subjects were different from those in our study.

A previous study investigated the relationship between the region-specific EAT thickness measured by MDCT with MS components in China [34]. This is the first study to evaluate changes in the region-specific EAT thickness measured by MDCT according to the presence of type 2 diabetes mellitus, and obesity in Korean adults.

Adipose tissue macrophages play an important role in the chronic inflammatory state, such as obesity-associated insulin resistance [33]. EAT has been reported to be the source of inflammatory mediators. Infiltration of inflammatory cells, such as macrophages and CD8-positive T cells and expression of adipocytokines in EAT in subjects with coronary artery disease were greater than in subjects without coronary artery disease [3637]. Because of the presence of these inflammatory mediators in EAT, the EAT thickness in the LAVG could be associated with type 2 diabetes mellitus. Additionally, in our study, the EAT thicknesses over the LAVG and RAVG in subjects with coronary artery stenosis were greater than those in subjects without coronary artery stenosis by MDCT. Further studies including markers of inflammation and adipokines are required to determine the pathophysiologic role of EAT.

However, there are some limitations in this study. First, this is a cross-sectional study, and we could therefore only make assumptions about the possible etiological relationships. Second, waist circumference was not measured, and thus, we could not evaluate the relationship between the EAT thickness and abdominal obesity, which is a key component of MS. Third, we did not measure the markers of inflammation and adipokines, which might give important clues about the pathophysiologic role of EAT. Finally, the sample size of our study population was relatively small and the number of normal subjects in the control group was small.

In conclusion, EAT thickness can be easily measured and is suggested to represent EAT. EAT thickness, especially in the LAVG, may be a useful indicator for type 2 diabetes mellitus and obesity. Further larger and longitudinal studies are needed to elucidate the clinical implications relevant to associations between the EAT thickness and MS components.

NOTES

CONFLICTS OF INTEREST: No potential conflict of interest relevant to this article was reported.

REFERENCES

• 1. Van Gaal LF, Mertens IL, De Block CE. Mechanisms linking obesity with cardiovascular disease. Nature 2006;444:875-880. ArticlePubMedPDF
• 2. Sarin S, Wenger C, Marwaha A, Qureshi A, Go BD, Woomert CA, Clark K, Nassef LA, Shirani J. Clinical significance of epicardial fat measured using cardiac multislice computed tomography. Am J Cardiol 2008;102:767-771. ArticlePubMed
• 3. Rabkin SW. Epicardial fat: properties, function and relationship to obesity. Obes Rev 2007;8:253-261. ArticlePubMed
• 4. Wende AR, Abel ED. Lipotoxicity in the heart. Biochim Biophys Acta 2010;1801:311-319. ArticlePubMed
• 5. Graner M, Siren R, Nyman K, Lundbom J, Hakkarainen A, Pentikainen MO, Lauerma K, Lundbom N, Adiels M, Nieminen MS, Taskinen MR. Cardiac steatosis associates with visceral obesity in nondiabetic obese men. J Clin Endocrinol Metab 2013;98:1189-1197. ArticlePubMed
• 6. Iozzo P. Myocardial, perivascular, and epicardial fat. Diabetes Care 2011;34(Suppl 2):S371-S379. ArticlePubMedPMCPDF
• 7. Gorter PM, van Lindert AS, de Vos AM, Meijs MF, van der Graaf Y, Doevendans PA, Prokop M, Visseren FL. Quantification of epicardial and peri-coronary fat using cardiac computed tomography; reproducibility and relation with obesity and metabolic syndrome in patients suspected of coronary artery disease. Atherosclerosis 2008;197:896-903. ArticlePubMed
• 8. Iacobellis G, Corradi D, Sharma AM. Epicardial adipose tissue: anatomic, biomolecular and clinical relationships with the heart. Nat Clin Pract Cardiovasc Med 2005;2:536-543. ArticlePubMedPDF
• 9. Mahabadi AA, Massaro JM, Rosito GA, Levy D, Murabito JM, Wolf PA, O'Donnell CJ, Fox CS, Hoffmann U. Association of pericardial fat, intrathoracic fat, and visceral abdominal fat with cardiovascular disease burden: the Framingham Heart Study. Eur Heart J 2009;30:850-856. ArticlePubMedPMC
• 10. Katsiki N, Mikhailidis DP, Wierzbicki AS. Epicardial fat and vascular risk: a narrative review. Curr Opin Cardiol 2013;28:458-463. PubMed
• 11. Iacobellis G, Malavazos AE, Corsi MM. Epicardial fat: from the biomolecular aspects to the clinical practice. Int J Biochem Cell Biol 2011;43:1651-1654. ArticlePubMed
• 12. Eckel RH, Grundy SM, Zimmet PZ. The metabolic syndrome. Lancet 2005;365:1415-1428. ArticlePubMed
• 13. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, Fruchart JC, James WP, Loria CM, Smith SC Jr. International Diabetes Federation Task Force on Epidemiology and Prevention. Hational Heart, Lung, and Blood Institute. American Heart Association. World Heart Federation. International Atherosclerosis Society. International Association for the Study of Obesity. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 2009;120:1640-1645. ArticlePubMed
• 14. Galassi A, Reynolds K, He J. Metabolic syndrome and risk of cardiovascular disease: a meta-analysis. Am J Med 2006;119:812-819. ArticlePubMed
• 15. Iacobellis G, Bianco AC. Epicardial adipose tissue: emerging physiological, pathophysiological and clinical features. Trends Endocrinol Metab 2011;22:450-457. ArticlePubMedPMC
• 16. Sacks HS, Fain JN. Human epicardial adipose tissue: a review. Am Heart J 2007;153:907-917. ArticlePubMed
• 17. Yorgun H, Canpolat U, Hazirolan T, Ates AH, Sunman H, Dural M, Sahiner L, Kaya EB, Aytemir K, Tokgozoglu L, Kabakci G, Oto A. Increased epicardial fat tissue is a marker of metabolic syndrome in adult patients. Int J Cardiol 2013;165:308-313. ArticlePubMed
• 18. Wang CP, Hsu HL, Hung WC, Yu TH, Chen YH, Chiu CA, Lu LF, Chung FM, Shin SJ, Lee YJ. Increased epicardial adipose tissue (EAT) volume in type 2 diabetes mellitus and association with metabolic syndrome and severity of coronary atherosclerosis. Clin Endocrinol (Oxf) 2009;70:876-882. ArticlePubMed
• 19. Oyama N, Goto D, Ito YM, Ishimori N, Mimura R, Furumoto T, Kato F, Tsutsui H, Tamaki N, Terae S, Shirato H. Single-slice epicardial fat area measurement: do we need to measure the total epicardial fat volume? Jpn J Radiol 2011;29:104-109. ArticlePubMedPDF
• 20. American Diabetes Association. Standards of medical care in diabetes: 2013. Diabetes Care 2013;36(Suppl 1):S11-S66. ArticlePubMedPDF
• 21. Bassett J. International Diabetes Institute. World Health Organization. Regional Office for the Western Pacific. International Association for the Study of Obesity. International Obesity Task Force. The Asian-Pacific perspective: redefining obesity and its treatment. Geneva: WHO Western Pacific Region; 2000.
• 22. Iacobellis G, Willens HJ. Echocardiographic epicardial fat: a review of research and clinical applications. J Am Soc Echocardiogr 2009;22:1311-1319. ArticlePubMed
• 23. Saremi F, Mekhail S, Sefidbakht S, Thonar B, Malik S, Sarlaty T. Quantification of epicardial adipose tissue: correlation of surface area and volume measurements. Acad Radiol 2011;18:977-983. PubMed
• 24. Bambace C, Sepe A, Zoico E, Telesca M, Olioso D, Venturi S, Rossi A, Corzato F, Faccioli S, Cominacini L, Santini F, Zamboni M. Inflammatory profile in subcutaneous and epicardial adipose tissue in men with and without diabetes. Heart Vessels 2014;29:42-48. ArticlePubMedPDF
• 25. Shimabukuro M. Cardiac adiposity and global cardiometabolic risk: new concept and clinical implication. Circ J 2009;73:27-34. ArticlePubMed
• 26. Karadag B, Ozulu B, Ozturk FY, Oztekin E, Sener N, Altuntas Y. Comparison of epicardial adipose tissue (EAT) thickness and anthropometric measurements in metabolic syndrome (MS) cases above and under the age of 65. Arch Gerontol Geriatr 2011;52:e79-e84. ArticlePubMed
• 27. Iacobellis G, Ribaudo MC, Assael F, Vecci E, Tiberti C, Zappaterreno A, Di Mario U, Leonetti F. 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;88:5163-5168. ArticlePubMed
• 28. Iacobellis G, Leonetti F. Epicardial adipose tissue and insulin resistance in obese subjects. J Clin Endocrinol Metab 2005;90:6300-6302. ArticlePubMed
• 29. Iacobellis G, Barbaro G, Gerstein HC. Relationship of epicardial fat thickness and fasting glucose. Int J Cardiol 2008;128:424-426. ArticlePubMed
• 30. Utz W, Engeli S, Haufe S, Kast P, Hermsdorf M, Wiesner S, Pofahl M, Traber J, Luft FC, Boschmann M, Schulz-Menger J, Jordan J. Myocardial steatosis, cardiac remodelling and fitness in insulin-sensitive and insulin-resistant obese women. Heart 2011;97:1585-1589. ArticlePubMed
• 31. McGavock JM, Lingvay I, Zib I, Tillery T, Salas N, Unger R, Levine BD, Raskin P, Victor RG, Szczepaniak LS. Cardiac steatosis in diabetes mellitus: a 1H-magnetic resonance spectroscopy study. Circulation 2007;116:1170-1175. ArticlePubMed
• 32. Kim HM, Kim KJ, Lee HJ, Yu HT, Moon JH, Kang ES, Cha BS, Lee HC, Lee BW, Kim YJ. Epicardial adipose tissue thickness is an indicator for coronary artery stenosis in asymptomatic type 2 diabetic patients: its assessment by cardiac magnetic resonance. Cardiovasc Diabetol 2012;11:83ArticlePubMedPMC
• 33. Olefsky JM, Glass CK. Macrophages, inflammation, and insulin resistance. Annu Rev Physiol 2010;72:219-246. ArticlePubMed
• 34. Wang TD, Lee WJ, Shih FY, Huang CH, Chang YC, Chen WJ, Lee YT, Chen MF. Relations of epicardial adipose tissue measured by multidetector computed tomography to components of the metabolic syndrome are region-specific and independent of anthropometric indexes and intraabdominal visceral fat. J Clin Endocrinol Metab 2009;94:662-669. ArticlePubMed
• 35. Liang KW, Tsai IC, Lee WJ, Lee IT, Lee WL, Lin SY, Wan CJ, Fu CP, Ting CT, Sheu WH. MRI measured epicardial adipose tissue thickness at the right AV groove differentiates inflammatory status in obese men with metabolic syndrome. Obesity (Silver Spring) 2012;20:525-532. ArticlePubMedPDF
• 36. Hirata Y, Tabata M, Kurobe H, Motoki T, Akaike M, Nishio C, Higashida M, Mikasa H, Nakaya Y, Takanashi S, Igarashi T, Kitagawa T, Sata M. Coronary atherosclerosis is associated with macrophage polarization in epicardial adipose tissue. J Am Coll Cardiol 2011;58:248-255. ArticlePubMed
• 37. Hirata Y, Kurobe H, Akaike M, Chikugo F, Hori T, Bando Y, Nishio C, Higashida M, Nakaya Y, Kitagawa T, Sata M. Enhanced inflammation in epicardial fat in patients with coronary artery disease. Int Heart J 2011;52:139-142. ArticlePubMed

Fig. 1

Epicardial adipose tissue was measured using multidetector computed tomography. (A) Epicardial adipose tissue thickness was measured on the parasternal short axis view. (B) Epicardial adipose tissue thickness was measured on the horizontal long axis view. (C) Epicardial fat area was measured at the left main coronary artery level. SIVG, superior interventricular groove; IIVG, inferior interventricular groove; LAVG, left atrioventricular groove; RAVG, right atrioventricular groove; AIVG, anterior interventricular groove.

Table 1

Clinical and biochemical characteristics of the subjects

Characteristic	Type 2 diabetes mellitus		Non-diabetes mellitus		P value
	Obese (n=24)	Nonobese (n=16)	Obese (n=26)	Nonobese (n=28)
Age, yr	63±13	63±12	61±12	58±16	0.424
Male gender	8 (33.3)	12 (75)a	10 (38.5)b	10 (35.7)b	0.018
Current smoker	3 (12.5)	5 (31.3)	4 (15.3)	2 (7.1)	0.188
Body mass index, kg/m2	28.0±2.3	22.8±1.6a	27.7±3.0b	22.1±2.6a,c	<0.001
SBP, mm Hg	125±13	127±14	127±14	123±15	0.761
DBP, mm Hg	75±7	76±10	79±10	77±10	0.454
Fasting glucose, mmol/L	7.5±2.2	8.1±2.7	5.4±0.7a,b	5.0±0.5a,b	<0.001
TC, mmol/L	4.8±0.8	4.5±1.0	4.6±0.9	4.8±0.9	0.638
Triglycerides, mmol/L	2.3±1.2	1.7±1.9	1.6±0.8	1.5±1.2	0.230
HDL-C, mmol/L	1.2±0.3	1.3±0.5	1.4±0.6	1.4±0.4	0.315
LDL-C, mmol/L	2.8±0.9	2.6±0.7	2.8±1.0	2.8±0.6	0.927
Plaque or stenosis of coronary arteries	18 (75)	12 (75)	13 (50)	14 (50)	0.111
Glycosylated hemoglobin, %	7.3±2.0	8.4±2.3	-	-	0.121
Type of hypoglycemic medication (OHA/insulin/none), %	79/0/21	56/19/25	-	-	-

Values are presented as mean±standard deviation or number (%).

SBP, systolic blood pressure; DBP, diastolic blood pressure; TC, total cholesterol; HDL-C, high density lipoprotein cholesterol; LDL-C, low density lipoprotein cholesterol; OHA, oral hypoglycemic agents.

^aP<0.05 vs. type 2 diabetes mellitus, obese, ^bP<0.05 vs. type 2 diabetes mellitus, nonobese, ^cP<0.05 vs. non-type 2 diabetes mellitus, obese.

Table 2

Correlations between the epicardial fat area at the left main coronary artery level and other epicardial adipose tissue thicknesses

	Pearson correlation coefficients	P value
Superior IV groove	0.601	<0.001
Inferior IV groove	0.235	0.023
RVF mean	0.491	<0.001
RVF max	0.475	<0.001
RV superior wall	0.484	<0.001
LV lateral wall	0.527	<0.001
Right AV groove	0.444	<0.001
Left AV groove	0.613	<0.001
Anterior IV groove	0.509	<0.001
RV apex	0.544	<0.001
LV apex	0.508	<0.001
RVA mean	0.523	<0.001
RVA max	0.522	<0.001

IV, interventricular; RVF, right ventricular free wall; RV, right ventricular; LV, left ventricular; AV, atrioventricular; RVA, right ventricular anterior wall.

Table 3

Epicardial adipose tissue values in the subjects

	Type 2 diabetes mellitus		Non-diabetes mellitus
	Obese (n=24)	Nonobese (n=16)	Obese (n=26)	Nonobese (n=28)
LMCA level area, cm2	17.0±6.9a	12.0±8.5	13.7±6.5a	8.4±6.1
Superior IV groove, mm	11.3±2.3	10.4±2.9	12.0±3.6	10.5±3.1
Inferior IV groove, mm	5.9±1.7	5.7±2.0	5.7±2.3	5.6±2.3
RVF mean, mm	5.8±2.6	5.0±2.6	6.0±2.5	5.2±2.6
RVF max, mm	6.8±2.9	6.0±3.1	7.4±3.2	6.5±3.3
RV sup wall, mm	5.4±2.5	5.1±3.3	5.6±3.1	3.9±1.6
LV lateral wall, mm	3.2±1.6	3.0±1.4	3.1±1.4	2.9±2.2
Right AV groove, mm	19.1±4.3a	16.3±4.0	17.5±3.3	16.1±3.9
Left AV groove, mm	13.0±2.7a	11.8±2.8a	11.8±3.3a	8.8±1.9
Anterior IV groove, mm	7.7±3.9	7.4±2.3	7.7±3.9	6.6±2.7
RV apex, mm	7.2±3.6	6.8±2.7	7.1±2.9	5.5±2.0
LV apex, mm	4.8±2.0a,b	4.5±1.8	3.5±1.3	3.3±1.6
RVA mean, mm	5.4±2.3	4.6±2.1	5.9±2.5	5.1±1.7
RVA max, mm	6.6±2.7	6.1±3.3	6.9±3.0	6.3±2.3

Values are presented as mean±standard deviation.

LMCA, left main coronary artery; IV, interventricular; RVF, right ventricular free wall; RV, right ventricular; LV, left ventricular; AV, atrioventricular; RVA, right ventricular anterior wall.

^aP<0.05 vs. non-type 2 diabetes mellitus, nonobese, ^bP<0.05 vs. non-type 2 diabetes mellitus, obese.

Table 4

Epicardial adipose tissue values according to the presence of type 2 diabetes mellitus adjusted for body mass index

	Type 2 diabetes mellitus (n=40)	Non-diabetes mellitus (n=54)	P value
LMCA level area, cm2	15.0±7.9	11.0±6.8	<0.001
Superior IV groove, mm	10.9±2.5	11.2±3.4	0.026
Inferior IV groove, mm	5.8±1.8	5.7±2.3	0.926
RVF mean, mm	5.5±2.6	5.6±2.5	0.569
RVF max, mm	6.5±3.0	7.0±3.3	0.460
RV sup wall, mm	5.3±2.8	4.7±2.6	0.052
LV lateral wall, mm	3.1±1.5	3.0±1.8	0.785
Right AV groove, mm	18.0±4.4	16.8±3.7	0.006
Left AV groove, mm	12.5±2.8	10.2±3.1	<0.001
Anterior IV groove, mm	7.6±3.3	7.1±3.3	0.581
RV apex, mm	5.1±2.2	5.5±2.1	0.112
LV apex, mm	6.4±2.9	6.6±2.6	0.316
RVA mean, mm	7.0±3.2	6.3±2.6	0.144
RVA max, mm	4.7±1.9	3.4±1.4	0.001

Values are presented as mean±standard deviation.

LMCA, left main coronary artery; IV, interventricular; RVF, right ventricular free wall; RV, right ventricular; LV, left ventricular; AV, atrioventricular; RVA, right ventricular anterior wall.

Table 5

Epicardial adipose tissue values according to the presence of obesity adjusted for type 2 diabetes mellitus

	Obese subjects (n=50)	Nonobese subjects (n=44)	P value
LMCA level area, cm2	15.3±6.8	9.7±7.2	<0.001
Superior IV groove, mm	11.6±3.0	10.5±3.0	0.058
Inferior IV groove, mm	5.8±2.0	5.7±2.2	0.721
RVF mean, mm	5.9±2.5	5.1±2.5	0.123
RVF max, mm	7.1±3.1	6.3±3.2	0.178
RV sup wall, mm	5.5±2.8	4.3±2.4	0.039
LV lateral wall, mm	3.1±1.5	2.9±1.9	0.591
Right AV groove, mm	18.3±3.9	16.2±3.9	0.018
Left AV groove, mm	12.4±3.0	9.8±2.7	<0.001
Anterior IV groove, mm	7.7±3.8	6.9±2.6	0.262
RV apex, mm	7.1±3.2	6.0±2.3	0.090
LV apex, mm	4.1±1.8	3.7±1.8	0.465
RVA mean, mm	5.6±2.4	4.9±1.8	0.076
RVA max, mm	6.8±2.9	6.2±2.6	0.274

Values are presented as mean±standard deviation.

LMCA, left main coronary artery; IV, interventricular; RVF, right ventricular free wall; RV, right ventricular; LV, left ventricular; AV, atrioventricular; RVA, right ventricular anterior wall.

Table 6

Factors associated with epicardial adipose tissue thickness in the left atrioventricular groove by multiple linear regression analysis (R²=0.419)

	β	Standard error	Standardized β	P value
Age	0.089	0.034	0.334	0.013
Type 2 diabetes mellitus	1.524	0.712	0.259	0.038
Body mass index	0.309	0.096	0.397	0.002

Adjusted for gender, smoking status, systolic blood pressure, triglycerides, and plaque or stenosis of coronary arteries in multidetector computed tomography.

Figure & Data

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Citations to this article as recorded by  

• Association of epicardial adipose tissue with early structural and functional cardiac changes in Type 2 diabetes
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  European Journal of Radiology.2024; 174: 111400.     CrossRef
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  Behnoush Gustafsson, Suvi P. Rovio, Saku Ruohonen, Nina Hutri-Kähönen, Mika Kähönen, Jorma S. A. Viikari, Katja Pahkala, Olli T. Raitakari
  Scientific Reports.2024;[Epub]     CrossRef
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  Reviews in Cardiovascular Medicine.2024;[Epub]     CrossRef
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  Santosh K Sanganalmath, Shubham Dubey, Sudhakar Veeranki, Keerthy Narisetty, Prasanna Krishnamurthy
  Cardiovascular Diabetology.2023;[Epub]     CrossRef
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  Mohammed Ali Gameil, Hanan Abdelhay Elsherbiny, Ibrahim Elsayed Youssry, Sara Abdel Gawad, Ahmed Abd EL-Hakim Arafat
  Journal of Diabetes & Metabolic Disorders.2023; 22(1): 735.     CrossRef
• Echocardiographic evaluation of the effect of dapagliflozin on epicardial adipose tissue and left ventricular systolic function in type 2 diabetes mellitus
  Xiang-ting Song, Yu-long Wei, Yi-fei Rui, Li Fan
  Journal of Diabetes and its Complications.2023; 37(7): 108509.     CrossRef
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  Khaoula Bouazizi, Mohamed Zarai, Abdallah Noufaily, Mikaël Prigent, Thomas Dietenbeck, Emilie Bollache, Toan Nguyen, Valéria Della Valle, Eléonore Blondiaux, Karine Clément, Judith Aron-Wisnewsky, Fabrizio Andreelli, Alban Redheuil, Nadjia Kachenoura
  Frontiers in Clinical Diabetes and Healthcare.2023;[Epub]     CrossRef
• Epicardial adipose tissue, metabolic disorders, and cardiovascular diseases: recent advances classified by research methodologies
  Yujie Song, Yanzhen Tan, Meng Deng, Wenju Shan, Wenying Zheng, Bing Zhang, Jun Cui, Lele Feng, Lei Shi, Miao Zhang, Yingying Liu, Yang Sun, Wei Yi
  MedComm.2023;[Epub]     CrossRef
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  Eugene Han, Kyung-do Han, Byung-Wan Lee, Eun Seok Kang, Bong-Soo Cha, Seung-Hyun Ko, Yong-ho Lee
  The Journal of Clinical Endocrinology & Metabolism.2022; 107(5): e1976.     CrossRef
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  Ki-Woon Kang, Ju-Young Ko, Hyunghee Lee, Seung Yong Shin, Wang Soo Lee, Joonhwa Hong, Sang-Wook Kim, Seong-Kyu Lee, Min-Ho Oak
  Journal of Korean Medical Science.2022;[Epub]     CrossRef
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  Maddalena Conte, Laura Petraglia, Paolo Poggio, Vincenza Valerio, Serena Cabaro, Pasquale Campana, Giuseppe Comentale, Emilio Attena, Vincenzo Russo, Emanuele Pilato, Pietro Formisano, Dario Leosco, Valentina Parisi
  Frontiers in Medicine.2022;[Epub]     CrossRef
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  Maria Grazia Tarsitano, Carla Pandozzi, Giuseppe Muscogiuri, Sandro Sironi, Arturo Pujia, Andrea Lenzi, Elisa Giannetta
  Nutrients.2022; 14(14): 2926.     CrossRef
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  Zirong Wang, Tingting Song, Da Yu, Xiaofei Chen, Cailing Pu, Jianping Ding, Xiaoli Ling, Chim C. Lang
  PLOS ONE.2022; 17(9): e0274533.     CrossRef
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  Sumanth KHAKDE, Hafsa JAWAID, Farah YASMIN, Mashal BINTE ALI, Abdur REHMAN
  Minerva Endocrinology.2022;[Epub]     CrossRef
• Effect of caloric restriction with or without physical activity on body composition and epicardial fat in type 2 diabetic patients: A pilot randomized controlled trial
  Josée Leroux-Stewart, Belinda Elisha, Sémah Tagougui, Corinne Suppère, Sophie Bernard, Hortensia Mircescu, Katherine Desjardin, Virginie Messier, Gianluca Iacobellis, Rémi Rabasa-Lhoret
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  JCI Insight.2021;[Epub]     CrossRef
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  Heart Failure Reviews.2021; 28(3): 645.     CrossRef
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  Yousuke Sugita, Katsuhiko Ito, Shigeki Sakurai, Satoshi Sakai, Shinya Kuno
  Journal of Diabetes and its Complications.2020; 34(5): 107552.     CrossRef
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  Rim Rafeh, Anissa Viveiros, Gavin Y. Oudit, Ahmed F. El-Yazbi
  Clinical Science.2020; 134(7): 827.     CrossRef
• High released lactate by epicardial fat from coronary artery disease patients is reduced by dapagliflozin treatment
  Marinela Couselo-Seijas, Rosa María Agra-Bermejo, Angel Luis Fernández, José Manuel Martínez-Cereijo, Juan Sierra, Maeve Soto-Pérez, Adriana Rozados-Luis, José Ramón González-Juanatey, Sonia Eiras
  Atherosclerosis.2020; 292: 60.     CrossRef
• Echocardiography in the Era of Obesity
  Milad C. El Hajj, Sheldon E. Litwin
  Journal of the American Society of Echocardiography.2020; 33(7): 779.     CrossRef
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  Eugene Han, Ji-Yeon Lee, Kyung-do Han, Hanna Cho, Kwang Joon Kim, Byung-Wan Lee, Eun Seok Kang, Bong-Soo Cha, Zobair M Younossi, Yong-ho Lee
  Scientific Reports.2020;[Epub]     CrossRef
• Do most patients with obesity or type 2 diabetes, and atrial fibrillation, also have undiagnosed heart failure? A critical conceptual framework for understanding mechanisms and improving diagnosis and treatment
  Milton Packer
  European Journal of Heart Failure.2020; 22(2): 214.     CrossRef
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  Ying Li, Xuewei Liu, Guangsen Li, Ping Zhang
  International Journal of Diabetes in Developing Countries.2020; 40(4): 500.     CrossRef
• Epicardial fat tissue in patients with diabetes mellitus: a systematic review and meta-analysis
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  Cardiovascular Diabetology.2019;[Epub]     CrossRef
• CoreSlicer: a web toolkit for analytic morphomics
  Louis Mullie, Jonathan Afilalo
  BMC Medical Imaging.2019;[Epub]     CrossRef
• Critical role of the epicardium in mediating cardiac inflammation and fibrosis in patients with type 2 diabetes
  Milton Packer
  Diabetes, Obesity and Metabolism.2019; 21(8): 1765.     CrossRef
• MRI-based assessment and characterization of epicardial and paracardial fat depots in the context of impaired glucose metabolism and subclinical left-ventricular alterations
  Sophia D Rado, Roberto Lorbeer, Sergios Gatidis, Jürgen Machann, Corinna Storz, Konstantin Nikolaou, Wolfgang Rathmann, Udo Hoffmann, Annette Peters, Fabian Bamberg, Christopher L Schlett
  The British Journal of Radiology.2019;[Epub]     CrossRef
• Epicardial adipose tissue and cardiovascular diseases
  Anna Maria Ansaldo, Fabrizio Montecucco, Amirhossein Sahebkar, Franco Dallegri, Federico Carbone
  International Journal of Cardiology.2019; 278: 254.     CrossRef
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  Hiro Kawata, Ashwini Erande, Ola Lafi, Ching Wei Chen, Taishi Hirai, Peter Santucci, Shaista Malik
  International Journal of Cardiology.2019; 293: 109.     CrossRef
• Integration of Gene Expression Profile Data of Human Epicardial Adipose Tissue from Coronary Artery Disease to Verification of Hub Genes and Pathways
  Weitie Wang, Qing Liu, Yong Wang, Hulin Piao, Bo Li, Zhicheng Zhu, Dan Li, Tiance Wang, Rihao Xu, Kexiang Liu
  BioMed Research International.2019; 2019: 1.     CrossRef
• The effect of dapagliflozin treatment on epicardial adipose tissue volume
  Takao Sato, Yoshifusa Aizawa, Sho Yuasa, Shohei Kishi, Koichi Fuse, Satoshi Fujita, Yoshio Ikeda, Hitoshi Kitazawa, Minoru Takahashi, Masahito Sato, Masaaki Okabe
  Cardiovascular Diabetology.2018;[Epub]     CrossRef
• Epicardial Adipose Tissue May Mediate Deleterious Effects of Obesity and Inflammation on the Myocardium
  Milton Packer
  Journal of the American College of Cardiology.2018; 71(20): 2360.     CrossRef
• Relationships between epicardial adipose tissue thickness and adipo-fibrokine indicator profiles post-myocardial infarction
  Olga Gruzdeva, Evgenya Uchasova, Yulia Dyleva, Daria Borodkina, Olga Akbasheva, Ekaterina Belik, Viktoria Karetnikova, Natalia Brel, Alexander Kokov, Vasiliy Kashtalap, Olga Barbarash
  Cardiovascular Diabetology.2018;[Epub]     CrossRef
• Are the effects of drugs to prevent and to treat heart failure always concordant? The statin paradox and its implications for understanding the actions of antidiabetic medications
  Milton Packer
  European Journal of Heart Failure.2018; 20(7): 1100.     CrossRef
• Linking Arrhythmias and Adipocytes: Insights, Mechanisms, and Future Directions
  Maria A. Pabon, Kevin Manocha, Jim W. Cheung, James C. Lo
  Frontiers in Physiology.2018;[Epub]     CrossRef
• Leptin-Aldosterone-Neprilysin Axis
  Milton Packer
  Circulation.2018; 137(15): 1614.     CrossRef
• Do DPP-4 Inhibitors Cause Heart Failure Events by Promoting Adrenergically Mediated Cardiotoxicity?
  Milton Packer
  Circulation Research.2018; 122(7): 928.     CrossRef
• The epicardial adipose inflammatory triad: coronary atherosclerosis, atrial fibrillation, and heart failure with a preserved ejection fraction
  Milton Packer
  European Journal of Heart Failure.2018; 20(11): 1567.     CrossRef
• Assessment of relationships between novel inflammatory markers and presence and severity of preeclampsia: Epicardial fat thickness, pentraxin-3, and neutrophil-to-lymphocyte ratio
  Huseyin Altug Cakmak, Burcu Dincgez Cakmak, Cigdem Abide Yayla, Ebru Inci Coskun, Mehmet Erturk, Ibrahim Keles
  Hypertension in Pregnancy.2017; 36(3): 233.     CrossRef
• Sexual dimorphism in obesity-related genes in the epicardial fat during aging
  Caitlin Kocher, Matthew Christiansen, Sarah Martin, Christopher Adams, Paulette Wehner, Todd Gress, Nalini Santanam
  Journal of Physiology and Biochemistry.2017; 73(2): 215.     CrossRef
• Anatomic fat depots and cardiovascular risk: a focus on the leg fat using nationwide surveys (KNHANES 2008–2011)
  Eugene Han, Yong-ho Lee, Byung-Wan Lee, Eun Seok Kang, In-Kyu Lee, Bong-Soo Cha
  Cardiovascular Diabetology.2017;[Epub]     CrossRef
• Luseogliflozin reduces epicardial fat accumulation in patients with type 2 diabetes: a pilot study
  Ryotaro Bouchi, Masahiro Terashima, Yuriko Sasahara, Masahiro Asakawa, Tatsuya Fukuda, Takato Takeuchi, Yujiro Nakano, Masanori Murakami, Isao Minami, Hajime Izumiyama, Koshi Hashimoto, Takanobu Yoshimoto, Yoshihiro Ogawa
  Cardiovascular Diabetology.2017;[Epub]     CrossRef
• Thickness of carotid intima and epicardial fat in rosacea: a cross-sectional study
  Asli Akin Belli, Ilknur Altun, Ibrahim Altun
  Anais Brasileiros de Dermatologia.2017; 92(6): 820.     CrossRef
• Investigating interactions between epicardial adipose tissue and cardiac myocytes: what can we learn from different approaches?
  Katja Rietdorf, Hilary MacQueen
  British Journal of Pharmacology.2017; 174(20): 3542.     CrossRef
• Impact of Mediterranean diet on metabolic syndrome, cancer and longevity
  Nicola Di Daniele, Annalisa Noce, Maria Francesca Vidiri, Eleonora Moriconi, Giulia Marrone, Margherita Annicchiarico-Petruzzelli, Gabriele D’Urso, Manfredi Tesauro, Valentina Rovella, Antonino De Lorenzo
  Oncotarget.2017; 8(5): 8947.     CrossRef
• Role of miRNAs in Epicardial Adipose Tissue in CAD Patients with T2DM
  Yang Liu, Wenbo Fu, Mu Lu, Shitao Huai, Yaqin Song, Yutao Wei
  BioMed Research International.2016; 2016: 1.     CrossRef
• Circulating SIRT1 inversely correlates with epicardial fat thickness in patients with obesity
  S. Mariani, D. Costantini, C. Lubrano, S. Basciani, C. Caldaroni, G. Barbaro, E. Poggiogalle, L.M. Donini, A. Lenzi, L. Gnessi
  Nutrition, Metabolism and Cardiovascular Diseases.2016; 26(11): 1033.     CrossRef

About this article

Song DK, Hong YS, Lee H, Oh JY, Sung YA, Kim Y. Increased Epicardial Adipose Tissue Thickness in Type 2 Diabetes Mellitus and Obesity. Diabetes Metab J. 2015;39(5):405-413.

Received: Sep 24, 2014; Accepted: Jan 09, 2015

DOI: https://doi.org/10.4093/dmj.2015.39.5.405.

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