Download PDF
Exp Clin Endocrinol Diabetes 2017; 125(09): 598-602
DOI: 10.1055/s-0042-114035
Article
© Georg Thieme Verlag KG Stuttgart · New York

Evaluation of Epicardial Adipose Tissue in Patients of Type 2 Diabetes Mellitus by Echocardiography and its Correlation with Intimal Medial Thickness of Carotid Artery

Zihang Wang
1   Department of Diagnostic Ultrasound, Second Affiliated Hospital of Dalian Medical University, Dalian, P. R. China
,
Yuhong Zhang
1   Department of Diagnostic Ultrasound, Second Affiliated Hospital of Dalian Medical University, Dalian, P. R. China
,
Weiwei Liu
2   Library of Dalian Medical University, Dalian, P. R. China
,
Benli Su
3   Department of Endocrinology, Second Affiliated Hospital of Dalian Medical University, Dalian, P. R. China
› Author Affiliations
Further Information

Publication History

received   13 February 2016
first decision 28 July 2016

accepted    29 July 2016

Publication Date:
11 May 2017 (online)

Also available at
    Permissions and Reprints

Abstract

The present study aimed to evaluate the diagnostic value of echocardiography in measuring the thickness of epicardial adipose tissue (EAT) of the patients of type 2 diabetes mellitus (T2DM) and its correlation with the intimal-medial thickness of the carotid artery (cIMT) to investigate the relationship between EAT and cIMT. 68 patients of T2DM were enrolled and were divided into 2 groups: group of T2DM with duration≤10 years (35 cases) and group of T2DM with duration>10 years (33 cases). And 30 healthy subjects were enrolled as the control group. The thickness of EAT and cIMT were measured by echocardiography and high-frequency ultrasonography. The thickness of EAT and IMT of the carotid artery of 2 type 2 diabetic groups (duration≤10 years and>10 years) were significantly higher than that of the control group (all p<0.05), and the thickness of EAT and cIMT of the group of T2DM with duration>10 years were significantly higher than that of the group of T2DM with duration≤10 years (p<0.05). In univariate analysis, the thickness of EAT was positively and significantly associated with age (r=0.412, p<0.05), BMI (r=0.566, p<0.05), waist circumference (r=0.475, p<0.05), LDL (r=0.425, p<0.05), TG (r=0.496, p<0.05), duration of diabetes (r=0.384, p<0.05) and cIMT (r=0.456, p<0.05). In multiple stepwise regression analyses, age, BMI and IMT of carotid artery were appeared to be significantly associated with EAT (p<0.05 for all). In conclusion, routine screening of EAT and cIMT by ultrasonography in type 2 diabetic patients helps us to predict cardiovascular risks and prevent further development of cardiovascular complications.

Key words

epicardial adipose tissue - type 2 diabetes mellitus - intimal-medial thickness - carotid artery - echocardiography
 

  • References

  • 1 Dale AC, Vatten LJ, Nilsen TI. et al. Secular decline in mortality from coronary heart disease in adults with diabetes mellitus: cohort study. BMJ 2008; 337: a236
    CrossrefPubMedGoogle Scholar
  • 2 Goldfine AB, Fonseca V. Management of diabetes mellitus in patients with cardiovascular disease in the Bypass Angioplasty Revascularization Investigation 2 Diabetes (BARI 2D) trial. Circulation 2010; 121: 2447-2449
    CrossrefPubMedGoogle Scholar
  • 3 Forbes JM, Yee LT, Thallas V. et al. Advanced glycation end product interventions reduce diabetes-accelerated atherosclerosis. Diabetes 2004; 53: 1813-1823
    CrossrefPubMedGoogle Scholar
  • 4 Gaede P, Lund-Andersen H, Parving HH. et al. Effect of a multifactorial intervention on mortality in type 2 diabetes. N Engl J Med 2008; 358: 580-591
    CrossrefPubMedGoogle Scholar
  • 5 Hanley AJ, Williams K, Stern MP. et al. Homeostasis model assessment of insulin resistance in relation to the incidence of cardiovascular disease: the San Antonio Heart Study. Diabetes care 2002; 25: 1177-1184
    CrossrefPubMedGoogle Scholar
  • 6 Lam HC. Role of endothelin in diabetic vascular complications. Endocrine 2001; 14: 277-284
    CrossrefPubMedGoogle Scholar
  • 7 Yusuf S, Ostergren JB, Gerstein HC. et al. Effects of candesartan on the development of a new diagnosis of diabetes mellitus in patients with heart failure. Circulation 2005; 112: 48-53
    CrossrefPubMedGoogle Scholar
  • 8 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: 313-316
    CrossrefPubMedGoogle Scholar
  • 9 Bettencourt N, Toschke AM, Leite D. et al. Epicardial adipose tissue is an independent predictor of coronary atherosclerotic burden. Int J Cardiol 2012; 158: 26-32
    CrossrefPubMedGoogle Scholar
  • 10 Cheng VY, Dey D, Tamarappoo B. et al. Pericardial fat burden on ECG-gated noncontrast CT in asymptomatic patients who subsequently experience adverse cardiovascular events. JACC Cardiovasc Imaging 2010; 3: 352-360
    CrossrefPubMedGoogle Scholar
  • 11 Ding J, Hsu FC, Harris TB. 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: 499-504
    CrossrefPubMedGoogle Scholar
  • 12 Konishi M, Sugiyama S, Sugamura K. et al. Association of pericardial fat accumulation rather than abdominal obesity with coronary atherosclerotic plaque formation in patients with suspected coronary artery disease. Atherosclerosis 2010; 209: 573-578
    CrossrefPubMedGoogle Scholar
  • 13 Rosito GA, Massaro JM, Hoffmann U. et al. Pericardial fat, visceral abdominal fat, cardiovascular disease risk factors, and vascular calcification in a community-based sample: the Framingham Heart Study. Circulation 2008; 117: 605-613
    CrossrefPubMedGoogle Scholar
  • 14 World Health Organization. Definition, diagnosis, and classification of diabetes mellitus and its complications. Geneva: Switzerland: 1999
    Google Scholar
  • 15 Iacobellis G, Assael F, Ribaudo MC. et al. Epicardial fat from echocardiography: a new method for visceral adipose tissue prediction. Obes Res 2003; 11: 304-310
    CrossrefPubMedGoogle Scholar
  • 16 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: 5163-5168
    CrossrefPubMedGoogle Scholar
  • 17 Salonen JT, Salonen R. Ultrasonographically assessed carotid morphology and the risk of coronary heart disease. Arterioscler Thromb 1991; 11: 1245-1249
    CrossrefPubMedGoogle Scholar
  • 18 Sidhu PS, Desai SR. A simple and reproducible method for assessing intimal-medial thickness of the common carotid artery. Br J Radiol 1997; 70: 85-89
    CrossrefPubMedGoogle Scholar
  • 19 Mazurek T, Zhang L, Zalewski A. et al. Human epicardial adipose tissue is a source of inflammatory mediators. Circulation 2003; 108: 2460-2466
    CrossrefPubMedGoogle Scholar
  • 20 Sengul C, Ozveren O. Epicardial adipose tissue: a review of physiology, pathophysiology, and clinical applications. Anadolu Kardiyol Derg 2013; 13: 261-265
    PubMedGoogle Scholar
  • 21 Kwon HM, Sangiorgi G, Ritman EL. et al. Enhanced coronary vasa vasorum neovascularization in experimental hypercholesterolemia. J Clin Invest 1998; 101: 1551-1556
    CrossrefPubMedGoogle Scholar
  • 22 Yudkin JS, Eringa E, Stehouwer CD. “Vasocrine” signalling from perivascular fat: a mechanism linking insulin resistance to vascular disease. Lancet 2005; 365: 1817-1820
    CrossrefPubMedGoogle Scholar
  • 23 Iacobellis G, Bianco AC. Epicardial adipose tissue: emerging physiological, pathophysiological and clinical features. Trends Endocrinol Metab 2011; 22: 450-457
    CrossrefPubMedGoogle Scholar
  • 24 Ouwens DM, Sell H, Greulich S. et al. The role of epicardial and perivascular adipose tissue in the pathophysiology of cardiovascular disease. J Cell Mol Med 2010; 14: 2223-2234
    CrossrefPubMedGoogle Scholar
  • 25 Noyes AM, Dua K, Devadoss R. et al. Cardiac adipose tissue and its relationship to diabetes mellitus and cardiovascular disease. World J Diabetes 2014; 5: 868-876
    CrossrefPubMedGoogle Scholar
  • 26 Akarsu E, Korkmaz H, Oguzkan Balci S. et al. Subcutaneous adipose tissue type II deiodinase gene expression reduced in obese individuals with metabolic syndrome. Exp Clin Endocrinol Diabetes 2016; 124: 11-15
    Article in Thieme ConnectPubMedGoogle Scholar
  • 27 Xie LJ, Cheng MH. Body adipose distribution among patients with type 2 diabetes mellitus. Obes Res Clin Prac 2012; 6: e263-e346
    PubMedGoogle Scholar
  • 28 Li X, Allayee H, Xiang AH. et al. Variation in IGF2BP2 interacts with adiposity to alter insulin sensitivity in Mexican Americans. Obesity (Silver Spring) 2009; 17: 729-736
    CrossrefPubMedGoogle Scholar
  • 29 Ru Y, Ma M, Ma T. et al. Association of SNP276 in adiponectin gene with type 2 diabetes mellitus and insulin sensitivity. Zhonghua yi xue yi chuan xue za zhi 2005; 22: 698-701
    PubMedGoogle Scholar
  • 30 Stephens JW, Hurel SJ, Cooper JA. et al. A common functional variant in the interleukin-6 gene is associated with increased body mass index in subjects with type 2 diabetes mellitus. Mol Genet Metab 2004; 82: 180-186
    CrossrefPubMedGoogle Scholar
  • 31 Price TM, O'Brien SN, Welter BH. et al. Estrogen regulation of adipose tissue lipoprotein lipase – possible mechanism of body fat distribution. Am J Obstet Gynecol 1998; 178: 101-107
    CrossrefPubMedGoogle Scholar
  • 32 Zhao X, Zhong J, Mo Y. et al. Association of biochemical hyperandrogenism with type 2 diabetes and obesity in Chinese women with polycystic ovary syndrome. Int J Gynaecol Obstet 2010; 108: 148-151
    CrossrefPubMedGoogle Scholar
  • 33 Davis JN, Le KA, Walker RW. et al. Increased hepatic fat in overweight Hispanic youth influenced by interaction between genetic variation in PNPLA3 and high dietary carbohydrate and sugar consumption. Am J Clin Nutr 2010; 92: 1522-1527
    CrossrefPubMedGoogle Scholar
  • 34 Tuttle LJ, Sinacore DR, Cade WT. et al. Lower physical activity is associated with higher intermuscular adipose tissue in people with type 2 diabetes and peripheral neuropathy. Phys Ther 2011; 91: 923-930
    CrossrefPubMedGoogle Scholar
  • 35 Bays HE, Gonzalez-Campoy JM, Henry RR. et al. Is adiposopathy (sick fat) an endocrine disease?. Int J Clin Pract 2008; 62: 1474-1483
    CrossrefPubMedGoogle Scholar
  • 36 Goto T, Nakayama R, Yamanaka M. et al Effects of DSP-8658, a novel selective peroxisome proliferator-activated receptors a/γ modulator, on adipogenesis and glucose metabolism in diabetic obese mice. Exp Clin Endocrinol Diabetes 2015; 123: 492-499
    Article in Thieme ConnectPubMedGoogle Scholar
  • 37 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: 4620-4627
    CrossrefPubMedGoogle Scholar
  • 38 Bonetti PO, Lerman LO, Lerman A. Endothelial dysfunction: a marker of atherosclerotic risk. Arterioscler Thromb Vasc Biol 2003; 23: 168-175
    CrossrefPubMedGoogle Scholar
  • 39 Hwang MH, Kim S. Type 2 Diabetes: Endothelial dysfunction and Exercise. J Exerc Nutrition Biochem 2014; 18: 239-247
    PubMedGoogle Scholar
  • 40 Celik A, Topuz M, Gozukara Y. et al. The relationship between epicardial adipose tissue and endothelial dysfunction in patients with type 2 diabetes mellitus. Turk Kardiyol Dern Ars 2014; 42: 450-455
    CrossrefPubMedGoogle Scholar