Skip to main content
Top
Published in: Cardiovascular Diabetology 1/2019

Open Access 01-12-2019 | Type 2 Diabetes | Original investigation

Epicardial adipose tissue predicts incident cardiovascular disease and mortality in patients with type 2 diabetes

Authors: Regitse H. Christensen, Bernt Johan von Scholten, Christian S. Hansen, Magnus T. Jensen, Tina Vilsbøll, Peter Rossing, Peter G. Jørgensen

Published in: Cardiovascular Diabetology | Issue 1/2019

Login to get access

Abstract

Background

Cardiac fat is a cardiovascular biomarker but its importance in patients with type 2 diabetes is not clear. The aim was to evaluate the predictive potential of epicardial (EAT), pericardial (PAT) and total cardiac (CAT) fat in type 2 diabetes and elucidate sex differences.

Methods

EAT and PAT were measured by echocardiography in 1030 patients with type 2 diabetes. Follow-up was performed through national registries. The end-point was the composite of incident cardiovascular disease (CVD) and all-cause mortality. Analyses were unadjusted (model 1), adjusted for age and sex (model 2), plus systolic blood pressure, body mass index (BMI), low-density lipoprotein (LDL), smoking, diabetes duration and glycated hemoglobin (HbA1c) (model 3).

Results

Median follow-up was 4.7 years and 248 patients (191 men vs. 57 women) experienced the composite end-point. Patients with high EAT (> median level) had increased risk of the composite end-point in model 1 [Hazard ratio (HR): 1.46 (1.13; 1.88), p = 0.004], model 2 [HR: 1.31 (1.01; 1.69), p = 0.038], and borderline in model 3 [HR: 1.32 (0.99; 1.77), p = 0.058]. For men, but not women, high EAT was associated with a 41% increased risk of CVD and mortality in model 3 (p = 0.041). Net reclassification index improved when high EAT was added to model 3 (19.6%, p = 0.035). PAT or CAT were not associated with the end-point.

Conclusion

High levels of EAT were associated with the composite of incident CVD and mortality in patients with type 2 diabetes, particularly in men, after adjusting for CVD risk factors. EAT modestly improved risk prediction over CVD risk factors.
Appendix
Available only for authorised users
Literature
1.
go back to reference Cavender MA, Steg PG, Smith SC, Eagle K, Ohman EM, Goto S, et al. Impact of diabetes mellitus on hospitalization for heart failure, cardiovascular events, and death: outcomes at 4 years from the Reduction of Atherothrombosis for Continued Health (REACH) registry. Circulation. 2015;132(10):923–31.CrossRef Cavender MA, Steg PG, Smith SC, Eagle K, Ohman EM, Goto S, et al. Impact of diabetes mellitus on hospitalization for heart failure, cardiovascular events, and death: outcomes at 4 years from the Reduction of Atherothrombosis for Continued Health (REACH) registry. Circulation. 2015;132(10):923–31.CrossRef
3.
go back to reference Li Y, Liu B, Li Y, Jing X, Deng S, Yan Y, et al. Epicardial fat tissue in patients with diabetes mellitus: a systematic review and meta-analysis. Cardiovasc Diabetol. 2019;18:1–10.CrossRef Li Y, Liu B, Li Y, Jing X, Deng S, Yan Y, et al. Epicardial fat tissue in patients with diabetes mellitus: a systematic review and meta-analysis. Cardiovasc Diabetol. 2019;18:1–10.CrossRef
4.
go back to reference Ding J, Hsu F-C, Harris TB, Liu Y, Kritchevsky SB, Szklo M, 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(3):499–504.CrossRef Ding J, Hsu F-C, Harris TB, Liu Y, Kritchevsky SB, Szklo M, 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(3):499–504.CrossRef
5.
go back to reference Cheng VY, Dey D, Tamarappoo B, Nakazato R, Gransar H, Miranda-Peats R, et al. Pericardial fat burden on ECG-Gated noncontrast CT in asymptomatic patients who subsequently experience adverse cardiovascular events. JACC Cardiovasc Imaging. 2010;3(4):352–60.CrossRef Cheng VY, Dey D, Tamarappoo B, Nakazato R, Gransar H, Miranda-Peats R, et al. Pericardial fat burden on ECG-Gated noncontrast CT in asymptomatic patients who subsequently experience adverse cardiovascular events. JACC Cardiovasc Imaging. 2010;3(4):352–60.CrossRef
6.
go back to reference Greif M, Leber AW, Saam T, Uebleis C, Von Ziegler F, Rümmler J, et al. Determination of pericardial adipose tissue increases the prognostic accuracy of coronary artery calcification for future cardiovascular events. Cardiology. 2012;121(4):220–7.CrossRef Greif M, Leber AW, Saam T, Uebleis C, Von Ziegler F, Rümmler J, et al. Determination of pericardial adipose tissue increases the prognostic accuracy of coronary artery calcification for future cardiovascular events. Cardiology. 2012;121(4):220–7.CrossRef
7.
go back to reference Possner M, Liga R, Gaisl T, Vontobel J, Clerc O, Mikulicic F, et al. Quantification of epicardial and intrathoracic fat volume does not provide an added prognostic value as an adjunct to coronary artery calcium score and myocardial perfusion single-photon emission computed tomography. Eur Hear J Cardiovasc Imaging. 2016;17(8):885–91.CrossRef Possner M, Liga R, Gaisl T, Vontobel J, Clerc O, Mikulicic F, et al. Quantification of epicardial and intrathoracic fat volume does not provide an added prognostic value as an adjunct to coronary artery calcium score and myocardial perfusion single-photon emission computed tomography. Eur Hear J Cardiovasc Imaging. 2016;17(8):885–91.CrossRef
8.
10.
go back to reference Gitsioudis G, Schmahl C, Missiou A, Voss A, Schüssler A, Abdel-Aty H, et al. Epicardial adipose tissue is associated with plaque burden and composition and provides incremental value for the prediction of cardiac outcome. A clinical cardiac computed tomography angiography study. PLoS ONE. 2016;11(5):1–15.CrossRef Gitsioudis G, Schmahl C, Missiou A, Voss A, Schüssler A, Abdel-Aty H, et al. Epicardial adipose tissue is associated with plaque burden and composition and provides incremental value for the prediction of cardiac outcome. A clinical cardiac computed tomography angiography study. PLoS ONE. 2016;11(5):1–15.CrossRef
11.
go back to reference Mahabadi AA, Berg MH, Lehmann N, Kälsch H, Bauer M, Kara K, 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.CrossRef Mahabadi AA, Berg MH, Lehmann N, Kälsch H, Bauer M, Kara K, 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.CrossRef
14.
go back to reference Mahabadi AA, Lehmann N, Möhlenkamp S, Pundt N, Dykun I, Roggenbuck U, et al. Noncoronary measures enhance the predictive value of cardiac ct above traditional risk factors and CAC score in the general population. JACC Cardiovasc Imaging. 2016;9(10):1177–85.CrossRef Mahabadi AA, Lehmann N, Möhlenkamp S, Pundt N, Dykun I, Roggenbuck U, et al. Noncoronary measures enhance the predictive value of cardiac ct above traditional risk factors and CAC score in the general population. JACC Cardiovasc Imaging. 2016;9(10):1177–85.CrossRef
15.
go back to reference Mosca L, Barrett-Connor E, Kass Wenger N. Sex/gender differences in cardiovascular disease prevention: what a difference a decade makes. Circulation. 2011;124(19):2145–54.CrossRef Mosca L, Barrett-Connor E, Kass Wenger N. Sex/gender differences in cardiovascular disease prevention: what a difference a decade makes. Circulation. 2011;124(19):2145–54.CrossRef
16.
go back to reference Demerath EW, Sun SS, Rogers N, Lee M, Reed D, Choh AC, et al. Anatomical patterning of visceral adipose tissue: race, sex, and age variation. Obesity (Silver Spring). 2007;15(12):2984–93.CrossRef Demerath EW, Sun SS, Rogers N, Lee M, Reed D, Choh AC, et al. Anatomical patterning of visceral adipose tissue: race, sex, and age variation. Obesity (Silver Spring). 2007;15(12):2984–93.CrossRef
18.
go back to reference Tamara T, Thomas T, Yi Z, Karagiannides I, Pothoulakis C, Jensen M, et al. Mechanisms and metabolic implications of regional differences among fat depots. Cell Metab. 2013;17(5):644–56.CrossRef Tamara T, Thomas T, Yi Z, Karagiannides I, Pothoulakis C, Jensen M, et al. Mechanisms and metabolic implications of regional differences among fat depots. Cell Metab. 2013;17(5):644–56.CrossRef
19.
go back to reference Yudkin JS, Eringa E, Stehouwer CDA. “Vasocrine” signalling from perivascular fat: a mechanism linking insulin resistance to vascular disease. Lancet. 2005;365:1817–20.CrossRef Yudkin JS, Eringa E, Stehouwer CDA. “Vasocrine” signalling from perivascular fat: a mechanism linking insulin resistance to vascular disease. Lancet. 2005;365:1817–20.CrossRef
21.
go back to reference Mazurek T, Zhang L, Zalewski A, Mannion JD, Diehl JT, Arafat H, et al. Human epicardial adipose tissue is a source of inflammatory mediators. Circulation. 2003;108(20):2460–6.CrossRef Mazurek T, Zhang L, Zalewski A, Mannion JD, Diehl JT, Arafat H, et al. Human epicardial adipose tissue is a source of inflammatory mediators. Circulation. 2003;108(20):2460–6.CrossRef
22.
go back to reference Marchington JM, Mattacks CA, Pond CM. Adipose tissue in the mammalian heart and pericardium; structure, fetal development and biochemical properties. Comp Biochem Physiol. 1989;94(2):225–32.CrossRef Marchington JM, Mattacks CA, Pond CM. Adipose tissue in the mammalian heart and pericardium; structure, fetal development and biochemical properties. Comp Biochem Physiol. 1989;94(2):225–32.CrossRef
24.
go back to reference Jørgensen PG, Jensen MT, Mogelvang R, Von Scholten BJ, Bech J, Fritz-Hansen T, et al. Abnormal echocardiography in patients with type 2 diabetes and relation to symptoms and clinical characteristics. Diabetes Vasc Dis Res. 2016;13(5):321–30.CrossRef Jørgensen PG, Jensen MT, Mogelvang R, Von Scholten BJ, Bech J, Fritz-Hansen T, et al. Abnormal echocardiography in patients with type 2 diabetes and relation to symptoms and clinical characteristics. Diabetes Vasc Dis Res. 2016;13(5):321–30.CrossRef
25.
go back to reference Jørgensen PG, Jensen MT, Mogelvang R, Fritz-Hansen T, Galatius S, Biering-Sørensen T, et al. Impact of type 2 diabetes and duration of type 2 diabetes on cardiac structure and function. Int J Cardiol. 2016;2016(221):114–21.CrossRef Jørgensen PG, Jensen MT, Mogelvang R, Fritz-Hansen T, Galatius S, Biering-Sørensen T, et al. Impact of type 2 diabetes and duration of type 2 diabetes on cardiac structure and function. Int J Cardiol. 2016;2016(221):114–21.CrossRef
27.
go back to reference Jørgensen PG, Jensen MT, Biering-Sørensen T, Mogelvang R, Galatius S, Fritz-Hansen T, et al. Cholesterol remnants and triglycerides are associated with decreased myocardial function in patients with type 2 diabetes. Cardiovasc Diabetol. 2016;15(1):1–11.CrossRef Jørgensen PG, Jensen MT, Biering-Sørensen T, Mogelvang R, Galatius S, Fritz-Hansen T, et al. Cholesterol remnants and triglycerides are associated with decreased myocardial function in patients with type 2 diabetes. Cardiovasc Diabetol. 2016;15(1):1–11.CrossRef
32.
go back to reference Mancio J, Azevedo D, Saraiva F, Azevedo AI, Pires-Morais G, Leite-Moreira A, et al. Epicardial adipose tissue volume assessed by computed tomography and coronary artery disease: a systematic review and meta-analysis. Eur Heart J Cardiovasc Imaging. 2018;19(5):490–7.CrossRef Mancio J, Azevedo D, Saraiva F, Azevedo AI, Pires-Morais G, Leite-Moreira A, et al. Epicardial adipose tissue volume assessed by computed tomography and coronary artery disease: a systematic review and meta-analysis. Eur Heart J Cardiovasc Imaging. 2018;19(5):490–7.CrossRef
33.
go back to reference Goeller M, Achenbach S, Marwan M, Doris MK, Cadet S, Commandeur F, et al. Epicardial adipose tissue density and volume are related to subclinical atherosclerosis, inflammation and major adverse cardiac events in asymptomatic subjects. J Cardiovasc Comput Tomogr. 2018;12:67–73.CrossRef Goeller M, Achenbach S, Marwan M, Doris MK, Cadet S, Commandeur F, et al. Epicardial adipose tissue density and volume are related to subclinical atherosclerosis, inflammation and major adverse cardiac events in asymptomatic subjects. J Cardiovasc Comput Tomogr. 2018;12:67–73.CrossRef
34.
go back to reference Britton KA, Massaro JM, Murabito JM, Kreger BE, Hoffmann U, Fox CS. Body fat distribution, incident cardiovascular disease, cancer, and all-cause mortality. J Am Coll Cardiol. 2013;62(10):921–5.CrossRef Britton KA, Massaro JM, Murabito JM, Kreger BE, Hoffmann U, Fox CS. Body fat distribution, incident cardiovascular disease, cancer, and all-cause mortality. J Am Coll Cardiol. 2013;62(10):921–5.CrossRef
35.
go back to reference Oikonomou EK, Marwan M, Desai MY, Mancio J, Alashi A, Hutt Centeno E, et al. Non-invasive detection of coronary inflammation using computed tomography and prediction of residual cardiovascular risk (the CRISP CT study): a post hoc analysis of prospective outcome data. Lancet. 2018;392:929–39.CrossRef Oikonomou EK, Marwan M, Desai MY, Mancio J, Alashi A, Hutt Centeno E, et al. Non-invasive detection of coronary inflammation using computed tomography and prediction of residual cardiovascular risk (the CRISP CT study): a post hoc analysis of prospective outcome data. Lancet. 2018;392:929–39.CrossRef
36.
go back to reference Gruzdeva O, Uchasova E, Dyleva Y, Borodkina D, Akbasheva O, Belik E, et al. Relationships between epicardial adipose tissue thickness and adipo-fibrokine indicator profiles post-myocardial infarction. Cardiovasc Diabetol. 2018;17:40.CrossRef Gruzdeva O, Uchasova E, Dyleva Y, Borodkina D, Akbasheva O, Belik E, et al. Relationships between epicardial adipose tissue thickness and adipo-fibrokine indicator profiles post-myocardial infarction. Cardiovasc Diabetol. 2018;17:40.CrossRef
37.
go back to reference Cho DH, Joo HJ, Kim MN, Lim DS, Shim WJ, Park SM. Association between epicardial adipose tissue, high-sensitivity C-reactive protein and myocardial dysfunction in middle-aged men with suspected metabolic syndrome. Cardiovasc Diabetol. 2018;17:95.CrossRef Cho DH, Joo HJ, Kim MN, Lim DS, Shim WJ, Park SM. Association between epicardial adipose tissue, high-sensitivity C-reactive protein and myocardial dysfunction in middle-aged men with suspected metabolic syndrome. Cardiovasc Diabetol. 2018;17:95.CrossRef
38.
go back to reference Fei J, Cook C, Blough E, Santanam N. Age and sex mediated changes in epicardial fat adipokines. Atherosclerosis. 2010;212(2):488–94.CrossRef Fei J, Cook C, Blough E, Santanam N. Age and sex mediated changes in epicardial fat adipokines. Atherosclerosis. 2010;212(2):488–94.CrossRef
42.
go back to reference Nasri A, Najafian J, Derakhshandeh SM, Madjlesi F. Epicardial fat thickness and severity of coronary heart disease in patients with diabetes mellitus type II. ARYA Atheroscler. 2018;14:32–7.PubMedPubMedCentral Nasri A, Najafian J, Derakhshandeh SM, Madjlesi F. Epicardial fat thickness and severity of coronary heart disease in patients with diabetes mellitus type II. ARYA Atheroscler. 2018;14:32–7.PubMedPubMedCentral
43.
go back to reference Kang J, Kim YC, Park JJ, Kim S, Kang SH, Cho YJ, et al. Increased epicardial adipose tissue thickness is a predictor of new-onset diabetes mellitus in patients with coronary artery disease treated with high-intensity statins. Cardiovasc Diabetol. 2018;17:10.CrossRef Kang J, Kim YC, Park JJ, Kim S, Kang SH, Cho YJ, et al. Increased epicardial adipose tissue thickness is a predictor of new-onset diabetes mellitus in patients with coronary artery disease treated with high-intensity statins. Cardiovasc Diabetol. 2018;17:10.CrossRef
46.
go back to reference Davidovich D, Gastaldelli A, Sicari R. Imaging cardiac fat. Eur Heart J Cardiovasc Imaging. 2013;14(7):625–30.CrossRef Davidovich D, Gastaldelli A, Sicari R. Imaging cardiac fat. Eur Heart J Cardiovasc Imaging. 2013;14(7):625–30.CrossRef
47.
go back to reference Jensen MT, Sogaard P, Andersen HU, Bech J, Hansen TF, Galatius S, et al. Prevalence of systolic and diastolic dysfunction in patients with type 1 diabetes without known heart disease: the Thousand & 1 Study. Diabetologia. 2014;57(4):672–80.CrossRef Jensen MT, Sogaard P, Andersen HU, Bech J, Hansen TF, Galatius S, et al. Prevalence of systolic and diastolic dysfunction in patients with type 1 diabetes without known heart disease: the Thousand & 1 Study. Diabetologia. 2014;57(4):672–80.CrossRef
Metadata
Title
Epicardial adipose tissue predicts incident cardiovascular disease and mortality in patients with type 2 diabetes
Authors
Regitse H. Christensen
Bernt Johan von Scholten
Christian S. Hansen
Magnus T. Jensen
Tina Vilsbøll
Peter Rossing
Peter G. Jørgensen
Publication date
01-12-2019
Publisher
BioMed Central
Keyword
Type 2 Diabetes
Published in
Cardiovascular Diabetology / Issue 1/2019
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/s12933-019-0917-y

Other articles of this Issue 1/2019

Cardiovascular Diabetology 1/2019 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.