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Published in: Diabetology & Metabolic Syndrome 1/2014

Open Access 01-12-2014 | Research

Epicardial adipose tissue thickness and plasma homocysteine in patients with metabolic syndrome and normal coronary arteries

Authors: Akif Serhat Balcioğlu, Murtaza Emre Durakoğlugil, Davran Çiçek, Uğur Abbas Bal, Bülent Boyaci, Haldun Müderrisoğlu

Published in: Diabetology & Metabolic Syndrome | Issue 1/2014

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Abstract

Background

Increased epicardial adipose tissue thickness and plasma homocysteine levels are associated with Metabolic Syndrome (MS) and coronary artery disease. The majority of patients with MS have subclinical or manifest coronary artery disease. The aim of this study was to evaluate the relationship between MS and plasma homocysteine levels and epicardial adipose tissue thickness in subjects without epicardial coronary artery disease.

Methods

Patients who underwent coronary angiography due to angina or equivocal symptoms and/or abnormal stress test results and were found to have normal coronary arteries were evaluated for the presence of MS. The study group comprised 75 patients with normal coronary arteries and MS, and the control group included 75 age-gender matched subjects without coronary artery disease or MS.

Results

Epicardial adipose tissue thickness (5.8 ± 1.9 mm vs. 4.3 ± 1.6 mm, p <0.001) and plasma homocysteine levels (21.6 ± 6.1 μmol/L vs. 15.1 ± 5.8 μmol/L, p <0.001) were significantly higher in the MS group. Body mass index, triglyceride level, weight, age and waist circumference were positively and HDL cholesterol level were negatively correlated with both epicardial adipose tissue thickness and plasma homocysteine level. Epicardial adipose tissue thickness had the strongest correlation with plasma homocysteine level (r = 0.584, p < 0.001). For each 1 mm increase in epicardial adipose tissue thickness, an increase of 3.51 μmol/L (95% CI: 2.24-4.79) in plasma homocysteine level was expected.

Conclusions

We observed a close relationship between MS and epicardial adipose tissue thickness and plasma homocysteine levels, even in the absence of overt coronary artery disease.
Literature
1.
go back to reference Grundy SM, Becker D, Clark LT, Cooper RS, Denke MA, Howard WJ, Hunninghake DB, Illingworth DR, Luepker RV, McBride P, McKenney JM, Pasternak RC, Stone NJ, Van Horn L: Third report of the National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III) final report. Circulation. 2002, 106: 3143-3421.CrossRef Grundy SM, Becker D, Clark LT, Cooper RS, Denke MA, Howard WJ, Hunninghake DB, Illingworth DR, Luepker RV, McBride P, McKenney JM, Pasternak RC, Stone NJ, Van Horn L: Third report of the National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III) final report. Circulation. 2002, 106: 3143-3421.CrossRef
2.
go back to reference Stern MP, Williams K, Gonzalez-Villalpando C, Hunt KJ, Haffner SM: Does the metabolic syndrome improve identification of individuals at risk of type 2 diabetes and/or cardiovascular disease?. Diabetes Care. 2004, 27: 2676-2681. 10.2337/diacare.27.11.2676.CrossRefPubMed Stern MP, Williams K, Gonzalez-Villalpando C, Hunt KJ, Haffner SM: Does the metabolic syndrome improve identification of individuals at risk of type 2 diabetes and/or cardiovascular disease?. Diabetes Care. 2004, 27: 2676-2681. 10.2337/diacare.27.11.2676.CrossRefPubMed
3.
go back to reference Grundy SM, Brewer HB, Cleeman JI, Smith SC, Lenfant C, American Heart A: Definition of metabolic syndrome: report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation. 2004, 109: 433-438. 10.1161/01.CIR.0000111245.75752.C6.CrossRefPubMed Grundy SM, Brewer HB, Cleeman JI, Smith SC, Lenfant C, American Heart A: Definition of metabolic syndrome: report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation. 2004, 109: 433-438. 10.1161/01.CIR.0000111245.75752.C6.CrossRefPubMed
4.
go back to reference Clarke R, Collins R, Lewington S, Donald A, Alfthan G, Tuomilehto J, Arnesen E, Bonaa K, Blacher J, Boers GHJ, Bostom A, Bots ML, Grobbee DE, Brattström L, Breteler MMB, Hofman A, Chambers JC, Kooner JS, Coull BM, Evans RW, Kuller LH, Evers S, Folsom AR, Freyburger G, Parrot F, Genest J, Dalery K, Graham IM, Daly L, Hoogeveen EK: Homocysteine and risk of ischemic heart disease and stroke: a meta-analysis. JAMA. 2002, 288: 2015-2022. 10.1001/jama.288.16.2015.CrossRef Clarke R, Collins R, Lewington S, Donald A, Alfthan G, Tuomilehto J, Arnesen E, Bonaa K, Blacher J, Boers GHJ, Bostom A, Bots ML, Grobbee DE, Brattström L, Breteler MMB, Hofman A, Chambers JC, Kooner JS, Coull BM, Evans RW, Kuller LH, Evers S, Folsom AR, Freyburger G, Parrot F, Genest J, Dalery K, Graham IM, Daly L, Hoogeveen EK: Homocysteine and risk of ischemic heart disease and stroke: a meta-analysis. JAMA. 2002, 288: 2015-2022. 10.1001/jama.288.16.2015.CrossRef
5.
go back to reference Stamler JS, Osborne JA, Jaraki O, Rabbani LE, Mullins M, Singel D, Loscalzo J: Adverse vascular effects of homocysteine are modulated by endothelium-derived relaxing factor and related oxides of nitrogen. J Clin Investig. 1993, 91: 308-318. 10.1172/JCI116187.PubMedCentralCrossRefPubMed Stamler JS, Osborne JA, Jaraki O, Rabbani LE, Mullins M, Singel D, Loscalzo J: Adverse vascular effects of homocysteine are modulated by endothelium-derived relaxing factor and related oxides of nitrogen. J Clin Investig. 1993, 91: 308-318. 10.1172/JCI116187.PubMedCentralCrossRefPubMed
6.
go back to reference Tawakol A, Omland T, Gerhard M, Wu JT, Creager MA: Hyperhomocyst(e)inemia is associated with impaired endothelium-dependent vasodilation in humans. Circulation. 1997, 95: 1119-1121. 10.1161/01.CIR.95.5.1119.CrossRefPubMed Tawakol A, Omland T, Gerhard M, Wu JT, Creager MA: Hyperhomocyst(e)inemia is associated with impaired endothelium-dependent vasodilation in humans. Circulation. 1997, 95: 1119-1121. 10.1161/01.CIR.95.5.1119.CrossRefPubMed
7.
go back to reference Wall RT, Harlan JM, Harker LA, Striker GE: Homocysteine-induced endothelial cell injury in vitro: a model for the study of vascular injury. Thromb Res. 1980, 18: 113-121. 10.1016/0049-3848(80)90175-9.CrossRefPubMed Wall RT, Harlan JM, Harker LA, Striker GE: Homocysteine-induced endothelial cell injury in vitro: a model for the study of vascular injury. Thromb Res. 1980, 18: 113-121. 10.1016/0049-3848(80)90175-9.CrossRefPubMed
8.
go back to reference Meigs JB, Jacques PF, Selhub J, Singer DE, Nathan DM, Rifai N, D’Agostino RB, Wilson PW, Framingham Offspring S: Fasting plasma homocysteine levels in the insulin resistance syndrome: the Framingham offspring study. Diabetes Care. 2001, 24: 1403-1410. 10.2337/diacare.24.8.1403.CrossRefPubMed Meigs JB, Jacques PF, Selhub J, Singer DE, Nathan DM, Rifai N, D’Agostino RB, Wilson PW, Framingham Offspring S: Fasting plasma homocysteine levels in the insulin resistance syndrome: the Framingham offspring study. Diabetes Care. 2001, 24: 1403-1410. 10.2337/diacare.24.8.1403.CrossRefPubMed
9.
go back to reference Oron-Herman M, Rosenthal T, Sela BA: Hyperhomocysteinemia as a component of syndrome X. Metabolism. 2003, 52: 1491-1495. 10.1016/S0026-0495(03)00262-2.CrossRefPubMed Oron-Herman M, Rosenthal T, Sela BA: Hyperhomocysteinemia as a component of syndrome X. Metabolism. 2003, 52: 1491-1495. 10.1016/S0026-0495(03)00262-2.CrossRefPubMed
10.
go back to reference Hajer GR, van der Graaf Y, Olijhoek JK, Verhaar MC, Visseren FL, Group SS: Levels of homocysteine are increased in metabolic syndrome patients but are not associated with an increased cardiovascular risk, in contrast to patients without the metabolic syndrome. Heart. 2007, 93: 216-220.PubMedCentralCrossRefPubMed Hajer GR, van der Graaf Y, Olijhoek JK, Verhaar MC, Visseren FL, Group SS: Levels of homocysteine are increased in metabolic syndrome patients but are not associated with an increased cardiovascular risk, in contrast to patients without the metabolic syndrome. Heart. 2007, 93: 216-220.PubMedCentralCrossRefPubMed
11.
go back to reference Sacks HS, Fain JN: Human epicardial adipose tissue: a review. Am Heart J. 2007, 153: 907-917. 10.1016/j.ahj.2007.03.019.CrossRefPubMed Sacks HS, Fain JN: Human epicardial adipose tissue: a review. Am Heart J. 2007, 153: 907-917. 10.1016/j.ahj.2007.03.019.CrossRefPubMed
12.
go back to reference Pierdomenico SD, Pierdomenico AM, Cuccurullo F, Iacobellis G: Meta-analysis of the relation of echocardiographic epicardial adipose tissue thickness and the metabolic syndrome. Am J Cardiol. 2013, 111: 73-78. 10.1016/j.amjcard.2012.08.044.CrossRefPubMed Pierdomenico SD, Pierdomenico AM, Cuccurullo F, Iacobellis G: Meta-analysis of the relation of echocardiographic epicardial adipose tissue thickness and the metabolic syndrome. Am J Cardiol. 2013, 111: 73-78. 10.1016/j.amjcard.2012.08.044.CrossRefPubMed
13.
go back to reference Alam MS, Green R, de Kemp R, Beanlands RS, Chow BJ: Epicardial adipose tissue thickness as a predictor of impaired microvascular function in patients with non-obstructive coronary artery disease. J Nucl Cardiol. 2013, 20: 804-812. 10.1007/s12350-013-9739-6.CrossRefPubMed Alam MS, Green R, de Kemp R, Beanlands RS, Chow BJ: Epicardial adipose tissue thickness as a predictor of impaired microvascular function in patients with non-obstructive coronary artery disease. J Nucl Cardiol. 2013, 20: 804-812. 10.1007/s12350-013-9739-6.CrossRefPubMed
14.
go back to reference Bachar GN, Dicker D, Kornowski R, Atar E: Epicardial adipose tissue as a predictor of coronary artery disease in asymptomatic subjects. Am J Cardiol. 2012, 110: 534-538. 10.1016/j.amjcard.2012.04.024.CrossRefPubMed Bachar GN, Dicker D, Kornowski R, Atar E: Epicardial adipose tissue as a predictor of coronary artery disease in asymptomatic subjects. Am J Cardiol. 2012, 110: 534-538. 10.1016/j.amjcard.2012.04.024.CrossRefPubMed
15.
go back to reference Cheng VY, Dey D, Tamarappoo B, Nakazato R, Gransar H, Miranda-Peats R, Ramesh A, Wong ND, Shaw LJ, Slomka PJ, Berman DS: Pericardial fat burden on ECG-gated noncontrast CT in asymptomatic patients who subsequently experience adverse cardiovascular events. J Am Coll Cardiol Img. 2010, 3: 352-360.CrossRef Cheng VY, Dey D, Tamarappoo B, Nakazato R, Gransar H, Miranda-Peats R, Ramesh A, Wong ND, Shaw LJ, Slomka PJ, Berman DS: Pericardial fat burden on ECG-gated noncontrast CT in asymptomatic patients who subsequently experience adverse cardiovascular events. J Am Coll Cardiol Img. 2010, 3: 352-360.CrossRef
16.
go back to reference Tamarappoo B, Dey D, Shmilovich H, Nakazato R, Gransar H, Cheng VY, Friedman JD, Hayes SW, Thomson LE, Slomka PJ, Rozanski A, Berman DS: Increased pericardial fat volume measured from noncontrast CT predicts myocardial ischemia by SPECT. J Am Coll Cardiol Img. 2010, 3: 1104-1112. 10.1016/j.jcmg.2010.07.014.CrossRef Tamarappoo B, Dey D, Shmilovich H, Nakazato R, Gransar H, Cheng VY, Friedman JD, Hayes SW, Thomson LE, Slomka PJ, Rozanski A, Berman DS: Increased pericardial fat volume measured from noncontrast CT predicts myocardial ischemia by SPECT. J Am Coll Cardiol Img. 2010, 3: 1104-1112. 10.1016/j.jcmg.2010.07.014.CrossRef
17.
go back to reference Alberti KG, Zimmet P, Shaw J: Group IDFETFC: the metabolic syndrome–a new worldwide definition. Lancet. 2005, 366: 1059-1062. 10.1016/S0140-6736(05)67402-8.CrossRefPubMed Alberti KG, Zimmet P, Shaw J: Group IDFETFC: the metabolic syndrome–a new worldwide definition. Lancet. 2005, 366: 1059-1062. 10.1016/S0140-6736(05)67402-8.CrossRefPubMed
18.
go back to reference Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pellikka PA, Picard MH, Roman MJ, Seward J, Shanewise JS, Solomon SD, Spencer KT, Sutton MS, Stewart WJ: Recommendations for chamber quantification: a report from the American Society of Echocardiography’s Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr. 2005, 18: 1440-1463. 10.1016/j.echo.2005.10.005.CrossRefPubMed Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pellikka PA, Picard MH, Roman MJ, Seward J, Shanewise JS, Solomon SD, Spencer KT, Sutton MS, Stewart WJ: Recommendations for chamber quantification: a report from the American Society of Echocardiography’s Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr. 2005, 18: 1440-1463. 10.1016/j.echo.2005.10.005.CrossRefPubMed
19.
go back to reference 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. 10.1210/jc.2003-030698.CrossRefPubMed 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. 10.1210/jc.2003-030698.CrossRefPubMed
20.
go back to reference Clarke R, Daly L, Robinson K, Naughten E, Cahalane S, Fowler B, Graham I: Hyperhomocysteinemia: an independent risk factor for vascular disease. N Engl J Med. 1991, 324: 1149-1155. 10.1056/NEJM199104253241701.CrossRefPubMed Clarke R, Daly L, Robinson K, Naughten E, Cahalane S, Fowler B, Graham I: Hyperhomocysteinemia: an independent risk factor for vascular disease. N Engl J Med. 1991, 324: 1149-1155. 10.1056/NEJM199104253241701.CrossRefPubMed
21.
go back to reference Okyay K, Balcioglu AS, Tavil Y, Tacoy G, Turkoglu S, Abaci A: A relationship between echocardiographic subepicardial adipose tissue and metabolic syndrome. Int J Cardiovasc Imaging. 2008, 24: 577-583. 10.1007/s10554-008-9295-3.CrossRefPubMed Okyay K, Balcioglu AS, Tavil Y, Tacoy G, Turkoglu S, Abaci A: A relationship between echocardiographic subepicardial adipose tissue and metabolic syndrome. Int J Cardiovasc Imaging. 2008, 24: 577-583. 10.1007/s10554-008-9295-3.CrossRefPubMed
22.
go back to reference Ding J, Hsu FC, Harris TB, Liu Y, Kritchevsky SB, Szklo M, Ouyang P, Espeland MA, Lohman KK, Criqui MH, Allison M, Bluemke DA, Carr JJ: 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. 10.3945/ajcn.2008.27358.PubMedCentralCrossRefPubMed Ding J, Hsu FC, Harris TB, Liu Y, Kritchevsky SB, Szklo M, Ouyang P, Espeland MA, Lohman KK, Criqui MH, Allison M, Bluemke DA, Carr JJ: 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. 10.3945/ajcn.2008.27358.PubMedCentralCrossRefPubMed
23.
go back to reference Wald DS, Law M, Morris JK: Homocysteine and cardiovascular disease: evidence on causality from a meta-analysis. BMJ. 2002, 325: 1202-10.1136/bmj.325.7374.1202.PubMedCentralCrossRefPubMed Wald DS, Law M, Morris JK: Homocysteine and cardiovascular disease: evidence on causality from a meta-analysis. BMJ. 2002, 325: 1202-10.1136/bmj.325.7374.1202.PubMedCentralCrossRefPubMed
24.
go back to reference Feng SQ, Ye P, Luo LM, Xiao WK, Xu RY, Wu HM: Relationship between serum homocysteine and metabolic syndrome: a cross-sectional study. Zhonghua Liu Xing Bing Xue Za Zhi. 2012, 33: 256-259.PubMed Feng SQ, Ye P, Luo LM, Xiao WK, Xu RY, Wu HM: Relationship between serum homocysteine and metabolic syndrome: a cross-sectional study. Zhonghua Liu Xing Bing Xue Za Zhi. 2012, 33: 256-259.PubMed
25.
go back to reference Vaya A, Carmona P, Badia N, Perez R, Hernandez Mijares A, Corella D: Homocysteine levels and the metabolic syndrome in a Mediterranean population: a case–control study. Clin Hemorheol Microcirc. 2011, 47: 59-66.PubMed Vaya A, Carmona P, Badia N, Perez R, Hernandez Mijares A, Corella D: Homocysteine levels and the metabolic syndrome in a Mediterranean population: a case–control study. Clin Hemorheol Microcirc. 2011, 47: 59-66.PubMed
26.
go back to reference Agoston-Coldea L, Mocan T, Dobie L, Marginean A, Lupu S: The association between homocysteine level and metabolic syndrome in patients of prior myocardial infarction. Rom J Intern Med. 2010, 48: 151-158.PubMed Agoston-Coldea L, Mocan T, Dobie L, Marginean A, Lupu S: The association between homocysteine level and metabolic syndrome in patients of prior myocardial infarction. Rom J Intern Med. 2010, 48: 151-158.PubMed
27.
go back to reference Mazurek T, Zhang L, Zalewski A, Mannion JD, Diehl JT, Arafat H, Sarov-Blat L, O'Brien S, Keiper EA, Johnson AG, Martin J, Goldstein BJ, Shi Y: Human epicardial adipose tissue is a source of inflammatory mediators. Circulation. 2003, 108: 2460-2466. 10.1161/01.CIR.0000099542.57313.C5.CrossRefPubMed Mazurek T, Zhang L, Zalewski A, Mannion JD, Diehl JT, Arafat H, Sarov-Blat L, O'Brien S, Keiper EA, Johnson AG, Martin J, Goldstein BJ, Shi Y: Human epicardial adipose tissue is a source of inflammatory mediators. Circulation. 2003, 108: 2460-2466. 10.1161/01.CIR.0000099542.57313.C5.CrossRefPubMed
28.
go back to reference Iacobellis G, Di Gioia C, Petramala L, Chiappetta C, Serra V, Zinnamosca L, Marinelli C, Ciardi A, De Toma G, Letizia C: Brown fat expresses adiponectin in humans. Int J Endocrinol. 2013, 2013: 126751-PubMedCentralCrossRefPubMed Iacobellis G, Di Gioia C, Petramala L, Chiappetta C, Serra V, Zinnamosca L, Marinelli C, Ciardi A, De Toma G, Letizia C: Brown fat expresses adiponectin in humans. Int J Endocrinol. 2013, 2013: 126751-PubMedCentralCrossRefPubMed
29.
go back to reference Lidell ME, Betz MJ, Enerback S: Brown adipose tissue and its therapeutic potential. J Intern Med. 2014, in press. doi:10.1111/joim.12255 Lidell ME, Betz MJ, Enerback S: Brown adipose tissue and its therapeutic potential. J Intern Med. 2014, in press. doi:10.1111/joim.12255
30.
go back to reference Wang ZV, Scherer PE: Adiponectin, cardiovascular function, and hypertension. Hypertension. 2008, 51: 8-14. 10.1161/HYPERTENSIONAHA.107.099424.CrossRefPubMed Wang ZV, Scherer PE: Adiponectin, cardiovascular function, and hypertension. Hypertension. 2008, 51: 8-14. 10.1161/HYPERTENSIONAHA.107.099424.CrossRefPubMed
31.
go back to reference Sade LE, Eroglu S, Bozbas H, Ozbicer S, Hayran M, Haberal A, Muderrisoglu H: Relation between epicardial fat thickness and coronary flow reserve in women with chest pain and angiographically normal coronary arteries. Atherosclerosis. 2009, 204: 580-585. 10.1016/j.atherosclerosis.2008.09.038.CrossRefPubMed Sade LE, Eroglu S, Bozbas H, Ozbicer S, Hayran M, Haberal A, Muderrisoglu H: Relation between epicardial fat thickness and coronary flow reserve in women with chest pain and angiographically normal coronary arteries. Atherosclerosis. 2009, 204: 580-585. 10.1016/j.atherosclerosis.2008.09.038.CrossRefPubMed
32.
go back to reference Munzel T, Sinning C, Post F, Warnholtz A, Schulz E: Pathophysiology, diagnosis and prognostic implications of endothelial dysfunction. Ann Med. 2008, 40: 180-196. 10.1080/07853890701854702.CrossRefPubMed Munzel T, Sinning C, Post F, Warnholtz A, Schulz E: Pathophysiology, diagnosis and prognostic implications of endothelial dysfunction. Ann Med. 2008, 40: 180-196. 10.1080/07853890701854702.CrossRefPubMed
33.
go back to reference Iacobellis G, Barbarini G, Letizia C, Barbaro G: Epicardial fat thickness and nonalcoholic fatty liver disease in obese subjects. Obesity. 2014, 22: 332-336. 10.1002/oby.20624.CrossRefPubMed Iacobellis G, Barbarini G, Letizia C, Barbaro G: Epicardial fat thickness and nonalcoholic fatty liver disease in obese subjects. Obesity. 2014, 22: 332-336. 10.1002/oby.20624.CrossRefPubMed
34.
go back to reference Arslan U, Turkoglu S, Balcioglu S, Tavil Y, Karakan T, Cengel A: Association between nonalcoholic fatty liver disease and coronary artery disease. Coron Artery Dis. 2007, 18: 433-436. 10.1097/MCA.0b013e3282583c0d.CrossRefPubMed Arslan U, Turkoglu S, Balcioglu S, Tavil Y, Karakan T, Cengel A: Association between nonalcoholic fatty liver disease and coronary artery disease. Coron Artery Dis. 2007, 18: 433-436. 10.1097/MCA.0b013e3282583c0d.CrossRefPubMed
35.
go back to reference Ormseth MJ, Lipson A, Alexopoulos N, Hartlage GR, Oeser AM, Bian A, Gebretsadik T, Shintani A, Raggi P, Stein CM: Association of epicardial adipose tissue with cardiometabolic risk and metabolic syndrome in patients with rheumatoid arthritis. Arthritis Care Res (Hoboken). 2013, 65: 1410-1415. 10.1002/acr.22027.CrossRef Ormseth MJ, Lipson A, Alexopoulos N, Hartlage GR, Oeser AM, Bian A, Gebretsadik T, Shintani A, Raggi P, Stein CM: Association of epicardial adipose tissue with cardiometabolic risk and metabolic syndrome in patients with rheumatoid arthritis. Arthritis Care Res (Hoboken). 2013, 65: 1410-1415. 10.1002/acr.22027.CrossRef
36.
go back to reference Erdogan T, Cetin M, Kocaman SA, Durakoglugil ME, Ergul E, Ugurlu Y, Canga A: Epicardial adipose tissue is independently associated with increased left ventricular mass in untreated hypertensive patients: an observational study. Anadolu Kardiyol Derg. 2013, 13: 320-327.PubMed Erdogan T, Cetin M, Kocaman SA, Durakoglugil ME, Ergul E, Ugurlu Y, Canga A: Epicardial adipose tissue is independently associated with increased left ventricular mass in untreated hypertensive patients: an observational study. Anadolu Kardiyol Derg. 2013, 13: 320-327.PubMed
37.
go back to reference Iacobellis G, Petramala L, Barbaro G, Kargi AY, Serra V, Zinnamosca L, Colangelo L, Marinelli C, Ciardi A, De Toma G, Letizia C: Epicardial fat thickness and left ventricular mass in subjects with adrenal incidentaloma. Endocrine. 2013, 44: 532-536. 10.1007/s12020-013-9902-5.CrossRefPubMed Iacobellis G, Petramala L, Barbaro G, Kargi AY, Serra V, Zinnamosca L, Colangelo L, Marinelli C, Ciardi A, De Toma G, Letizia C: Epicardial fat thickness and left ventricular mass in subjects with adrenal incidentaloma. Endocrine. 2013, 44: 532-536. 10.1007/s12020-013-9902-5.CrossRefPubMed
Metadata
Title
Epicardial adipose tissue thickness and plasma homocysteine in patients with metabolic syndrome and normal coronary arteries
Authors
Akif Serhat Balcioğlu
Murtaza Emre Durakoğlugil
Davran Çiçek
Uğur Abbas Bal
Bülent Boyaci
Haldun Müderrisoğlu
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Diabetology & Metabolic Syndrome / Issue 1/2014
Electronic ISSN: 1758-5996
DOI
https://doi.org/10.1186/1758-5996-6-62

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