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Published in: Cardiovascular Diabetology 1/2018

Open Access 01-12-2018 | Original investigation

Association between epicardial adipose tissue, high-sensitivity C-reactive protein and myocardial dysfunction in middle-aged men with suspected metabolic syndrome

Authors: Dong-Hyuk Cho, Hyung Joon Joo, Mi-Na Kim, Do-Sun Lim, Wan Joo Shim, Seong-Mi Park

Published in: Cardiovascular Diabetology | Issue 1/2018

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Abstract

Background

As body fat composition and metabolism differ between men and women, we evaluated sex-related differences in the association among epicardial adipose tissue (EAT), secretome profile, and myocardial function of subjects with suspected metabolic syndrome.

Methods

We evaluated 277 participants (men, n = 140; 56.1 ± 4.7 years) who underwent conventional echocardiography and two-dimensional speckle tracking from the Seoul Metabolic Syndrome cohort. EAT was measured from the right ventricular free wall perpendicular to the aortic annulus at end systole. Global longitudinal strain (GLS) was obtained from 18 apical segments. Apolipoprotein A1, apolipoprotein B, adiponectin, and high-sensitivity C-reactive protein (hs-CRP) levels were measured using immunoturbidimetry assay.

Results

Mean age, body mass index, and hs-CRP level did not differ by sex. Waist circumference, fasting blood glucose level, and triglyceride/high-density lipoprotein cholesterol ratio were higher, and apolipoprotein AI and adiponectin levels were lower in men. No significant difference in mean EAT thickness was found (7.02 ± 1.81 vs. 7.13 ± 1.70 mm, p = 0.613). Men had a higher left ventricular (LV) mass index and lower GLS. EAT thickness was associated with hs-CRP level in men alone (ß = 0.206, p = 0.015). LV mass index (ß = 2.311, p = 0.037) and function represented by e′ (ß = − 0.279, p = 0.001) and GLS (ß = − 0.332, p < 0.001) were independently associated with EAT thickness in men alone.

Conclusions

In middle-aged subjects with suspected metabolic syndrome, EAT was associated with inflammation represented by hs-CRP level, LV mass, and subclinical myocardial dysfunction only in men, suggesting that the inflammatory activity of EAT induced myocardial remodeling and dysfunction in middle-aged subjects but was attenuated in women.
Trial registration NCT02077530 (date of registration: November 1, 2013)
Literature
1.
go back to reference Benjamin EJ, Blaha MJ, Chiuve SE, Cushman M, Das SR, Deo R, de Ferranti SD, Floyd J, Fornage M, Gillespie C, et al. Heart disease and stroke statistics—2017 update: a report from the american heart association. Circulation. 2017;135(10):e146–603.CrossRefPubMedPubMedCentral Benjamin EJ, Blaha MJ, Chiuve SE, Cushman M, Das SR, Deo R, de Ferranti SD, Floyd J, Fornage M, Gillespie C, et al. Heart disease and stroke statistics—2017 update: a report from the american heart association. Circulation. 2017;135(10):e146–603.CrossRefPubMedPubMedCentral
2.
go back to reference Roger VL, Go AS, Lloyd-Jones DM, Adams RJ, Berry JD, Brown TM, Carnethon MR, Dai S, de Simone G, Ford ES, et al. Heart disease and stroke statistics–2011 update: a report from the American Heart Association. Circulation. 2011;123(4):e18–209.CrossRefPubMed Roger VL, Go AS, Lloyd-Jones DM, Adams RJ, Berry JD, Brown TM, Carnethon MR, Dai S, de Simone G, Ford ES, et al. Heart disease and stroke statistics–2011 update: a report from the American Heart Association. Circulation. 2011;123(4):e18–209.CrossRefPubMed
3.
go back to reference Bairey Merz CN, Shaw LJ, Reis SE, Bittner V, Kelsey SF, Olson M, Johnson BD, Pepine CJ, Mankad S, Sharaf BL, et al. Insights from the NHLBI-Sponsored Women’s Ischemia Syndrome Evaluation (WISE) Study: part II: gender differences in presentation, diagnosis, and outcome with regard to gender-based pathophysiology of atherosclerosis and macrovascular and microvascular coronary disease. J Am Coll Cardiol. 2006;47(3 Suppl):S21–9.CrossRefPubMed Bairey Merz CN, Shaw LJ, Reis SE, Bittner V, Kelsey SF, Olson M, Johnson BD, Pepine CJ, Mankad S, Sharaf BL, et al. Insights from the NHLBI-Sponsored Women’s Ischemia Syndrome Evaluation (WISE) Study: part II: gender differences in presentation, diagnosis, and outcome with regard to gender-based pathophysiology of atherosclerosis and macrovascular and microvascular coronary disease. J Am Coll Cardiol. 2006;47(3 Suppl):S21–9.CrossRefPubMed
4.
go back to reference Waters DD, Gordon D, Rossouw JE, Cannon RO 3rd, Collins P, Herrington DM, Hsia J, Langer R, Mosca L, Ouyang P et al: Women’s ischemic syndrome evaluation: current status and future research directions: report of the National Heart, Lung and Blood Institute workshop: October 2–4, 2002 : Section 4: lessons from hormone replacement trials. Circulation 2004, 109(6):e53–5. Waters DD, Gordon D, Rossouw JE, Cannon RO 3rd, Collins P, Herrington DM, Hsia J, Langer R, Mosca L, Ouyang P et al: Women’s ischemic syndrome evaluation: current status and future research directions: report of the National Heart, Lung and Blood Institute workshop: October 2–4, 2002 : Section 4: lessons from hormone replacement trials. Circulation 2004, 109(6):e53–5.
5.
go back to reference Blaak E. Gender differences in fat metabolism. Curr Opin Clin Nutr Metab Care. 2001;4(6):499–502.CrossRefPubMed Blaak E. Gender differences in fat metabolism. Curr Opin Clin Nutr Metab Care. 2001;4(6):499–502.CrossRefPubMed
6.
go back to reference Makovey J, Naganathan V, Sambrook P. Gender differences in relationships between body composition components, their distribution and bone mineral density: a cross-sectional opposite sex twin study. Osteoporos Int. 2005;16(12):1495–505.CrossRefPubMed Makovey J, Naganathan V, Sambrook P. Gender differences in relationships between body composition components, their distribution and bone mineral density: a cross-sectional opposite sex twin study. Osteoporos Int. 2005;16(12):1495–505.CrossRefPubMed
7.
go back to reference Power ML, Schulkin J. Sex differences in fat storage, fat metabolism, and the health risks from obesity: possible evolutionary origins. Br J Nutr. 2008;99(5):931–40.CrossRefPubMed Power ML, Schulkin J. Sex differences in fat storage, fat metabolism, and the health risks from obesity: possible evolutionary origins. Br J Nutr. 2008;99(5):931–40.CrossRefPubMed
8.
go back to reference Ibrahim MM. Subcutaneous and visceral adipose tissue: structural and functional differences. Obes Rev. 2010;11(1):11–8.CrossRefPubMed Ibrahim MM. Subcutaneous and visceral adipose tissue: structural and functional differences. Obes Rev. 2010;11(1):11–8.CrossRefPubMed
9.
go back to reference Camhi SM, Bray GA, Bouchard C, Greenway FL, Johnson WD, Newton RL, Ravussin E, Ryan DH, Smith SR, Katzmarzyk PT. The relationship of waist circumference and BMI to visceral, subcutaneous, and total body fat: sex and race differences. Obesity (Silver Spring). 2011;19(2):402–8.CrossRef Camhi SM, Bray GA, Bouchard C, Greenway FL, Johnson WD, Newton RL, Ravussin E, Ryan DH, Smith SR, Katzmarzyk PT. The relationship of waist circumference and BMI to visceral, subcutaneous, and total body fat: sex and race differences. Obesity (Silver Spring). 2011;19(2):402–8.CrossRef
10.
go back to reference Iacobellis G, Willens HJ. Echocardiographic epicardial fat: a review of research and clinical applications. J Am Soc Echocardiogr. 2009;22(12):1311–9 (quiz 1417-1318).CrossRefPubMed Iacobellis G, Willens HJ. Echocardiographic epicardial fat: a review of research and clinical applications. J Am Soc Echocardiogr. 2009;22(12):1311–9 (quiz 1417-1318).CrossRefPubMed
11.
go back to reference Gruzdeva O, Uchasova E, Dyleva Y, Borodkina D, Akbasheva O, Belik E, Karetnikova V, Brel N, Kokov A, Kashtalap V. Relationships between epicardial adipose tissue thickness and adipo-fibrokine indicator profiles post-myocardial infarction. Cardiovasc Diabetol. 2018;17(1):40.CrossRefPubMedPubMedCentral Gruzdeva O, Uchasova E, Dyleva Y, Borodkina D, Akbasheva O, Belik E, Karetnikova V, Brel N, Kokov A, Kashtalap V. Relationships between epicardial adipose tissue thickness and adipo-fibrokine indicator profiles post-myocardial infarction. Cardiovasc Diabetol. 2018;17(1):40.CrossRefPubMedPubMedCentral
12.
go back to reference Iacobellis G, Pistilli D, Gucciardo M, Leonetti F, Miraldi F, Brancaccio G, Gallo P, di Gioia CR. Adiponectin expression in human epicardial adipose tissue in vivo is lower in patients with coronary artery disease. Cytokine. 2005;29(6):251–5.PubMed Iacobellis G, Pistilli D, Gucciardo M, Leonetti F, Miraldi F, Brancaccio G, Gallo P, di Gioia CR. Adiponectin expression in human epicardial adipose tissue in vivo is lower in patients with coronary artery disease. Cytokine. 2005;29(6):251–5.PubMed
13.
go back to reference Lai YH, Yun CH, Yang FS, Liu CC, Wu YJ, Kuo JY, Yeh HI, Lin TY, Bezerra HG, Shih SC, et al. Epicardial adipose tissue relating to anthropometrics, metabolic derangements and fatty liver disease independently contributes to serum high-sensitivity C-reactive protein beyond body fat composition: a study validated with computed tomography. J Am Soc Echocardiogr. 2012;25(2):234–41.CrossRefPubMed Lai YH, Yun CH, Yang FS, Liu CC, Wu YJ, Kuo JY, Yeh HI, Lin TY, Bezerra HG, Shih SC, et al. Epicardial adipose tissue relating to anthropometrics, metabolic derangements and fatty liver disease independently contributes to serum high-sensitivity C-reactive protein beyond body fat composition: a study validated with computed tomography. J Am Soc Echocardiogr. 2012;25(2):234–41.CrossRefPubMed
14.
go back to reference Hirata Y, Kurobe H, Akaike M, Chikugo F, Hori T, Bando Y, Nishio C, Higashida M, Nakaya Y, Kitagawa T. Enhanced inflammation in epicardial fat in patients with coronary artery disease. Int Heart J. 2011;52(3):139–42.CrossRefPubMed Hirata Y, Kurobe H, Akaike M, Chikugo F, Hori T, Bando Y, Nishio C, Higashida M, Nakaya Y, Kitagawa T. Enhanced inflammation in epicardial fat in patients with coronary artery disease. Int Heart J. 2011;52(3):139–42.CrossRefPubMed
15.
go back to reference Malavazos AE, Ermetici F, Cereda E, Coman C, Locati M, Morricone L, Corsi MM, Ambrosi B. Epicardial fat thickness: relationship with plasma visfatin and plasminogen activator inhibitor-1 levels in visceral obesity. Nutr Metab Cardiovasc Dis. 2008;18(8):523–30.CrossRefPubMed Malavazos AE, Ermetici F, Cereda E, Coman C, Locati M, Morricone L, Corsi MM, Ambrosi B. Epicardial fat thickness: relationship with plasma visfatin and plasminogen activator inhibitor-1 levels in visceral obesity. Nutr Metab Cardiovasc Dis. 2008;18(8):523–30.CrossRefPubMed
16.
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(1):73–8.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(1):73–8.CrossRefPubMed
17.
go back to reference Ueno K, Anzai T, Jinzaki M, Yamada M, Jo Y, Maekawa Y, Kawamura A, Yoshikawa T, Tanami Y, Sato K. Increased epicardial fat volume quantified by 64-multidetector computed tomography is associated with coronary atherosclerosis and totally occlusive lesions. Circ J. 2009;73(10):1927–33.CrossRefPubMed Ueno K, Anzai T, Jinzaki M, Yamada M, Jo Y, Maekawa Y, Kawamura A, Yoshikawa T, Tanami Y, Sato K. Increased epicardial fat volume quantified by 64-multidetector computed tomography is associated with coronary atherosclerosis and totally occlusive lesions. Circ J. 2009;73(10):1927–33.CrossRefPubMed
18.
go back to reference Mahabadi AA, Berg MH, Lehmann N, Kalsch H, Bauer M, Kara K, Dragano N, Moebus S, Jockel KH, Erbel R, et al. Association of epicardial fat with cardiovascular risk factors and incident myocardial infarction in the general population: the Heinz Nixdorf Recall Study. J Am Coll Cardiol. 2013;61(13):1388–95.CrossRefPubMed Mahabadi AA, Berg MH, Lehmann N, Kalsch H, Bauer M, Kara K, Dragano N, Moebus S, Jockel KH, Erbel R, et al. Association of epicardial fat with cardiovascular risk factors and incident myocardial infarction in the general population: the Heinz Nixdorf Recall Study. J Am Coll Cardiol. 2013;61(13):1388–95.CrossRefPubMed
19.
go back to reference Iacobellis G. Local and systemic effects of the multifaceted epicardial adipose tissue depot. Nat Rev Endocrinol. 2015;11(6):363–71.CrossRefPubMed Iacobellis G. Local and systemic effects of the multifaceted epicardial adipose tissue depot. Nat Rev Endocrinol. 2015;11(6):363–71.CrossRefPubMed
20.
go back to reference Cavalcante JL, Tamarappoo BK, Hachamovitch R, Kwon DH, Alraies MC, Halliburton S, Schoenhagen P, Dey D, Berman DS, Marwick TH. Association of epicardial fat, hypertension, subclinical coronary artery disease, and metabolic syndrome with left ventricular diastolic dysfunction. Am J Cardiol. 2012;110(12):1793–8.CrossRefPubMedPubMedCentral Cavalcante JL, Tamarappoo BK, Hachamovitch R, Kwon DH, Alraies MC, Halliburton S, Schoenhagen P, Dey D, Berman DS, Marwick TH. Association of epicardial fat, hypertension, subclinical coronary artery disease, and metabolic syndrome with left ventricular diastolic dysfunction. Am J Cardiol. 2012;110(12):1793–8.CrossRefPubMedPubMedCentral
21.
go back to reference Kim SA, Kim MN, Shim WJ, Park SM. Epicardial adipose tissue is related to cardiac function in elderly women, but not in men. Nutr Metab Cardiovasc Dis. 2017;27(1):41–7.CrossRefPubMed Kim SA, Kim MN, Shim WJ, Park SM. Epicardial adipose tissue is related to cardiac function in elderly women, but not in men. Nutr Metab Cardiovasc Dis. 2017;27(1):41–7.CrossRefPubMed
22.
go back to reference Watanabe K, Kishino T, Sano J, Ariga T, Okuyama S, Mori H, Matsushima S, Ohtsuka K, Ohnishi H, Watanabe T. Relationship between epicardial adipose tissue thickness and early impairment of left ventricular systolic function in patients with preserved ejection fraction. Heart Vessels. 2016;31(6):1010–5.CrossRefPubMed Watanabe K, Kishino T, Sano J, Ariga T, Okuyama S, Mori H, Matsushima S, Ohtsuka K, Ohnishi H, Watanabe T. Relationship between epicardial adipose tissue thickness and early impairment of left ventricular systolic function in patients with preserved ejection fraction. Heart Vessels. 2016;31(6):1010–5.CrossRefPubMed
23.
go back to reference El Khoudary SR, Shields KJ, Janssen I, Hanley C, Budoff MJ, Barinas-Mitchell E, Everson-Rose SA, Powell LH, Matthews KA. Cardiovascular Fat, menopause, and sex hormones in women: the SWAN cardiovascular fat ancillary study. J Clin Endocrinol Metab. 2015;100(9):3304–12.CrossRefPubMedPubMedCentral El Khoudary SR, Shields KJ, Janssen I, Hanley C, Budoff MJ, Barinas-Mitchell E, Everson-Rose SA, Powell LH, Matthews KA. Cardiovascular Fat, menopause, and sex hormones in women: the SWAN cardiovascular fat ancillary study. J Clin Endocrinol Metab. 2015;100(9):3304–12.CrossRefPubMedPubMedCentral
24.
go back to reference Cho SA, Joo HJ, Cho JY, Lee SH, Park JH, Hong SJ, Yu CW, Lim DS. Visceral fat area and serum adiponectin level predict the development of metabolic syndrome in a community-based asymptomatic population. PLoS ONE. 2017;12(1):e0169289.CrossRefPubMedPubMedCentral Cho SA, Joo HJ, Cho JY, Lee SH, Park JH, Hong SJ, Yu CW, Lim DS. Visceral fat area and serum adiponectin level predict the development of metabolic syndrome in a community-based asymptomatic population. PLoS ONE. 2017;12(1):e0169289.CrossRefPubMedPubMedCentral
25.
go back to reference Joo HJ, Cho SA, Cho JY, Lee S, Park JH, Yu CW, Hong SJ, Lim DS. Different relationship between physical activity, arterial stiffness and metabolic status in obese subjects. J Phys Act Health. 2017;14(9):716–25.CrossRefPubMed Joo HJ, Cho SA, Cho JY, Lee S, Park JH, Yu CW, Hong SJ, Lim DS. Different relationship between physical activity, arterial stiffness and metabolic status in obese subjects. J Phys Act Health. 2017;14(9):716–25.CrossRefPubMed
26.
go back to reference Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L, Flachskampf FA, Foster E, Goldstein SA, Kuznetsova T, et al. Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr. 2015;28(1):1 e14–39 e14.CrossRef Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L, Flachskampf FA, Foster E, Goldstein SA, Kuznetsova T, et al. Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr. 2015;28(1):1 e14–39 e14.CrossRef
27.
go back to reference Lin HH, Lee JK, Yang CY, Lien YC, Huang JW, Wu CK. Accumulation of epicardial fat rather than visceral fat is an independent risk factor for left ventricular diastolic dysfunction in patients undergoing peritoneal dialysis. Cardiovasc Diabetol. 2013;12(1):127.CrossRefPubMedPubMedCentral Lin HH, Lee JK, Yang CY, Lien YC, Huang JW, Wu CK. Accumulation of epicardial fat rather than visceral fat is an independent risk factor for left ventricular diastolic dysfunction in patients undergoing peritoneal dialysis. Cardiovasc Diabetol. 2013;12(1):127.CrossRefPubMedPubMedCentral
28.
go back to reference Fernandes-Cardoso A, Santos-Furtado M, Grindler J, Ferreira LA, Andrade JL, Santo MA. Epicardial fat thickness correlates with P-wave duration, left atrial size and decreased left ventricular systolic function in morbid obesity. Nutr Metab Cardiovasc Dis. 2017;27(8):731–8.CrossRefPubMed Fernandes-Cardoso A, Santos-Furtado M, Grindler J, Ferreira LA, Andrade JL, Santo MA. Epicardial fat thickness correlates with P-wave duration, left atrial size and decreased left ventricular systolic function in morbid obesity. Nutr Metab Cardiovasc Dis. 2017;27(8):731–8.CrossRefPubMed
29.
go back to reference Maimaituxun G, Shimabukuro M, Fukuda D, Yagi S, Hirata Y, Iwase T, Takao S, Matsuura T, Ise T, Kusunose K, et al. Local thickness of epicardial adipose tissue surrounding the left anterior descending artery is a simple predictor of coronary artery disease- new prediction model in combination with framingham risk score. Circ J. 2018;82(5):1369–78.CrossRefPubMed Maimaituxun G, Shimabukuro M, Fukuda D, Yagi S, Hirata Y, Iwase T, Takao S, Matsuura T, Ise T, Kusunose K, et al. Local thickness of epicardial adipose tissue surrounding the left anterior descending artery is a simple predictor of coronary artery disease- new prediction model in combination with framingham risk score. Circ J. 2018;82(5):1369–78.CrossRefPubMed
30.
go back to reference Hedgire S, Baliyan V, Zucker EJ, Bittner DO, Staziaki PV, Takx RA, Scholtz JE, Meyersohn N, Hoffmann U, Ghoshhajra B. Perivascular epicardial fat stranding at coronary CT angiography: a marker of acute plaque rupture and spontaneous coronary artery dissection. Radiology. 2018;287(3):808–15.CrossRefPubMed Hedgire S, Baliyan V, Zucker EJ, Bittner DO, Staziaki PV, Takx RA, Scholtz JE, Meyersohn N, Hoffmann U, Ghoshhajra B. Perivascular epicardial fat stranding at coronary CT angiography: a marker of acute plaque rupture and spontaneous coronary artery dissection. Radiology. 2018;287(3):808–15.CrossRefPubMed
31.
go back to reference Iacobellis G, Corradi D, Sharma AM. Epicardial adipose tissue: anatomic, biomolecular and clinical relationships with the heart. Nat Rev Cardiol. 2005;2(10):536.CrossRef Iacobellis G, Corradi D, Sharma AM. Epicardial adipose tissue: anatomic, biomolecular and clinical relationships with the heart. Nat Rev Cardiol. 2005;2(10):536.CrossRef
32.
go back to reference Evin M, Broadhouse KM, Callaghan FM, McGrath RT, Glastras S, Kozor R, Hocking SL, Lamy J, Redheuil A, Kachenoura N, et al. Impact of obesity and epicardial fat on early left atrial dysfunction assessed by cardiac MRI strain analysis. Cardiovasc Diabetol. 2016;15(1):164.CrossRefPubMedPubMedCentral Evin M, Broadhouse KM, Callaghan FM, McGrath RT, Glastras S, Kozor R, Hocking SL, Lamy J, Redheuil A, Kachenoura N, et al. Impact of obesity and epicardial fat on early left atrial dysfunction assessed by cardiac MRI strain analysis. Cardiovasc Diabetol. 2016;15(1):164.CrossRefPubMedPubMedCentral
33.
go back to reference Ji Q, Zhang J, Du Y, Zhu E, Wang Z, Que B, Miao H, Shi S, Qin X, Zhao Y, et al. Human epicardial adipose tissue-derived and circulating secreted frizzled-related protein 4 (SFRP4) levels are increased in patients with coronary artery disease. Cardiovasc Diabetol. 2017;16(1):133.CrossRefPubMedPubMedCentral Ji Q, Zhang J, Du Y, Zhu E, Wang Z, Que B, Miao H, Shi S, Qin X, Zhao Y, et al. Human epicardial adipose tissue-derived and circulating secreted frizzled-related protein 4 (SFRP4) levels are increased in patients with coronary artery disease. Cardiovasc Diabetol. 2017;16(1):133.CrossRefPubMedPubMedCentral
34.
go back to reference Du Y, Ji Q, Cai L, Huang F, Lai Y, Liu Y, Yu J, Han B, Zhu E, Zhang J, et al. Association between omentin-1 expression in human epicardial adipose tissue and coronary atherosclerosis. Cardiovasc Diabetol. 2016;15:90.CrossRefPubMedPubMedCentral Du Y, Ji Q, Cai L, Huang F, Lai Y, Liu Y, Yu J, Han B, Zhu E, Zhang J, et al. Association between omentin-1 expression in human epicardial adipose tissue and coronary atherosclerosis. Cardiovasc Diabetol. 2016;15:90.CrossRefPubMedPubMedCentral
35.
go back to reference Ouchi N, Kihara S, Funahashi T, Nakamura T, Nishida M, Kumada M, Okamoto Y, Ohashi K, Nagaretani H, Kishida K. Reciprocal association of C-reactive protein with adiponectin in blood stream and adipose tissue. Circulation. 2003;107(5):671–4.CrossRefPubMed Ouchi N, Kihara S, Funahashi T, Nakamura T, Nishida M, Kumada M, Okamoto Y, Ohashi K, Nagaretani H, Kishida K. Reciprocal association of C-reactive protein with adiponectin in blood stream and adipose tissue. Circulation. 2003;107(5):671–4.CrossRefPubMed
36.
go back to reference Graner M, Seppala-Lindroos A, Rissanen A, Hakkarainen A, Lundbom N, Kaprio J, Nieminen MS, Pietilainen KH. Epicardial fat, cardiac dimensions, and low-grade inflammation in young adult monozygotic twins discordant for obesity. Am J Cardiol. 2012;109(9):1295–302.CrossRefPubMed Graner M, Seppala-Lindroos A, Rissanen A, Hakkarainen A, Lundbom N, Kaprio J, Nieminen MS, Pietilainen KH. Epicardial fat, cardiac dimensions, and low-grade inflammation in young adult monozygotic twins discordant for obesity. Am J Cardiol. 2012;109(9):1295–302.CrossRefPubMed
37.
go back to reference Turak O, Ozcan F, Canpolat U, Isleyen A, Cebeci M, Oksuz F, Mendi MA, Cagli K, Golbasi Z, Aydogdu S. Increased echocardiographic epicardial fat thickness and high-sensitivity CRP level indicate diastolic dysfunction in patients with newly diagnosed essential hypertension. Blood Press Monit. 2013;18(5):259–64.CrossRefPubMed Turak O, Ozcan F, Canpolat U, Isleyen A, Cebeci M, Oksuz F, Mendi MA, Cagli K, Golbasi Z, Aydogdu S. Increased echocardiographic epicardial fat thickness and high-sensitivity CRP level indicate diastolic dysfunction in patients with newly diagnosed essential hypertension. Blood Press Monit. 2013;18(5):259–64.CrossRefPubMed
38.
go back to reference Kankaanpaa M, Lehto HR, Parkka JP, Komu M, Viljanen A, Ferrannini E, Knuuti J, Nuutila P, Parkkola R, Iozzo P. Myocardial triglyceride content and epicardial fat mass in human obesity: relationship to left ventricular function and serum free fatty acid levels. J Clin Endocrinol Metab. 2006;91(11):4689–95.CrossRefPubMed Kankaanpaa M, Lehto HR, Parkka JP, Komu M, Viljanen A, Ferrannini E, Knuuti J, Nuutila P, Parkkola R, Iozzo P. Myocardial triglyceride content and epicardial fat mass in human obesity: relationship to left ventricular function and serum free fatty acid levels. J Clin Endocrinol Metab. 2006;91(11):4689–95.CrossRefPubMed
39.
go back to reference Gaborit B, Kober F, Jacquier A, Moro PJ, Cuisset T, Boullu S, Dadoun F, Alessi MC, Morange P, Clement K, et al. Assessment of epicardial fat volume and myocardial triglyceride content in severely obese subjects: relationship to metabolic profile, cardiac function and visceral fat. Int J Obes (Lond). 2012;36(3):422–30.CrossRef Gaborit B, Kober F, Jacquier A, Moro PJ, Cuisset T, Boullu S, Dadoun F, Alessi MC, Morange P, Clement K, et al. Assessment of epicardial fat volume and myocardial triglyceride content in severely obese subjects: relationship to metabolic profile, cardiac function and visceral fat. Int J Obes (Lond). 2012;36(3):422–30.CrossRef
41.
go back to reference Kocher C, Christiansen M, Martin S, Adams C, Wehner P, Gress T, Santanam N. Sexual dimorphism in obesity-related genes in the epicardial fat during aging. J Physiol Biochem. 2017;73(2):215–24.CrossRefPubMed Kocher C, Christiansen M, Martin S, Adams C, Wehner P, Gress T, Santanam N. Sexual dimorphism in obesity-related genes in the epicardial fat during aging. J Physiol Biochem. 2017;73(2):215–24.CrossRefPubMed
42.
go back to reference Bolego C, Cignarella A, Staels B, Chinetti-Gbaguidi G. Macrophage function and polarization in cardiovascular disease: a role of estrogen signaling? Arterioscler Thromb Vasc Biol. 2013;33(6):1127–34.CrossRefPubMed Bolego C, Cignarella A, Staels B, Chinetti-Gbaguidi G. Macrophage function and polarization in cardiovascular disease: a role of estrogen signaling? Arterioscler Thromb Vasc Biol. 2013;33(6):1127–34.CrossRefPubMed
43.
go back to reference Khan D, Ansar Ahmed S. The immune system is a natural target for estrogen action: opposing effects of estrogen in two prototypical autoimmune diseases. Front Immunol. 2016;6:635.CrossRefPubMedPubMedCentral Khan D, Ansar Ahmed S. The immune system is a natural target for estrogen action: opposing effects of estrogen in two prototypical autoimmune diseases. Front Immunol. 2016;6:635.CrossRefPubMedPubMedCentral
44.
go back to reference Stubbins RE, Holcomb VB, Hong J, Nunez NP. Estrogen modulates abdominal adiposity and protects female mice from obesity and impaired glucose tolerance. Eur J Nutr. 2012;51(7):861–70.CrossRefPubMed Stubbins RE, Holcomb VB, Hong J, Nunez NP. Estrogen modulates abdominal adiposity and protects female mice from obesity and impaired glucose tolerance. Eur J Nutr. 2012;51(7):861–70.CrossRefPubMed
45.
go back to reference Wang D, Wang C, Wu X, Zheng W, Sandberg K, Ji H, Welch WJ, Wilcox CS. Endothelial dysfunction and enhanced contractility in microvessels from ovariectomized rats: roles of oxidative stress and perivascular adipose tissue. Hypertension. 2014;63(5):1063–9.CrossRefPubMedPubMedCentral Wang D, Wang C, Wu X, Zheng W, Sandberg K, Ji H, Welch WJ, Wilcox CS. Endothelial dysfunction and enhanced contractility in microvessels from ovariectomized rats: roles of oxidative stress and perivascular adipose tissue. Hypertension. 2014;63(5):1063–9.CrossRefPubMedPubMedCentral
46.
go back to reference Arnold AP, Cassis LA, Eghbali M, Reue K, Sandberg K. Sex hormones and sex chromosomes cause sex differences in the development of cardiovascular diseases. Arterioscler Thromb Vasc Biol. 2017;37(5):746–56.CrossRefPubMedPubMedCentral Arnold AP, Cassis LA, Eghbali M, Reue K, Sandberg K. Sex hormones and sex chromosomes cause sex differences in the development of cardiovascular diseases. Arterioscler Thromb Vasc Biol. 2017;37(5):746–56.CrossRefPubMedPubMedCentral
47.
go back to reference Sacks HS, Fain JN, Bahouth SW, Ojha S, Frontini A, Budge H, Cinti S, Symonds ME. Adult epicardial fat exhibits beige features. J Clin Endocrinol Metab. 2013;98(9):E1448–55.CrossRefPubMed Sacks HS, Fain JN, Bahouth SW, Ojha S, Frontini A, Budge H, Cinti S, Symonds ME. Adult epicardial fat exhibits beige features. J Clin Endocrinol Metab. 2013;98(9):E1448–55.CrossRefPubMed
48.
go back to reference Pedersen SB, Bruun JM, Kristensen K, Richelsen B. Regulation of UCP1, UCP2, and UCP3 mRNA expression in brown adipose tissue, white adipose tissue, and skeletal muscle in rats by estrogen. Biochem Biophys Res Commun. 2001;288(1):191–7.CrossRefPubMed Pedersen SB, Bruun JM, Kristensen K, Richelsen B. Regulation of UCP1, UCP2, and UCP3 mRNA expression in brown adipose tissue, white adipose tissue, and skeletal muscle in rats by estrogen. Biochem Biophys Res Commun. 2001;288(1):191–7.CrossRefPubMed
49.
go back to reference Velickovic K, Cvoro A, Srdic B, Stokic E, Markelic M, Golic I, Otasevic V, Stancic A, Jankovic A, Vucetic M, et al. Expression and subcellular localization of estrogen receptors alpha and beta in human fetal brown adipose tissue. J Clin Endocrinol Metab. 2014;99(1):151–9.CrossRefPubMed Velickovic K, Cvoro A, Srdic B, Stokic E, Markelic M, Golic I, Otasevic V, Stancic A, Jankovic A, Vucetic M, et al. Expression and subcellular localization of estrogen receptors alpha and beta in human fetal brown adipose tissue. J Clin Endocrinol Metab. 2014;99(1):151–9.CrossRefPubMed
50.
go back to reference Franssens BT, Hoogduin H, Leiner T, van der Graaf Y, Visseren FLJ. Relation between brown adipose tissue and measures of obesity and metabolic dysfunction in patients with cardiovascular disease. J Magn Reson Imaging. 2017;46(2):497–504.CrossRefPubMed Franssens BT, Hoogduin H, Leiner T, van der Graaf Y, Visseren FLJ. Relation between brown adipose tissue and measures of obesity and metabolic dysfunction in patients with cardiovascular disease. J Magn Reson Imaging. 2017;46(2):497–504.CrossRefPubMed
51.
go back to reference Nam H-Y, Jun S. Association between active brown adipose tissue and coronary artery calcification in healthy men. Nuklearmedizin. 2017;56(05):184–90.CrossRefPubMed Nam H-Y, Jun S. Association between active brown adipose tissue and coronary artery calcification in healthy men. Nuklearmedizin. 2017;56(05):184–90.CrossRefPubMed
52.
go back to reference Basurto Acevedo L, Barrera Hernández S, Fernández Muñoz MdJ, Saucedo García RP, Rodríguez Luna AK, Martínez Murillo C. An increase in epicardial fat in women is associated with thrombotic risk. Clínica e Investigación en Arteriosclerosis (English Edition); 2018. Basurto Acevedo L, Barrera Hernández S, Fernández Muñoz MdJ, Saucedo García RP, Rodríguez Luna AK, Martínez Murillo C. An increase in epicardial fat in women is associated with thrombotic risk. Clínica e Investigación en Arteriosclerosis (English Edition); 2018.
Metadata
Title
Association between epicardial adipose tissue, high-sensitivity C-reactive protein and myocardial dysfunction in middle-aged men with suspected metabolic syndrome
Authors
Dong-Hyuk Cho
Hyung Joon Joo
Mi-Na Kim
Do-Sun Lim
Wan Joo Shim
Seong-Mi Park
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2018
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/s12933-018-0735-7

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