Highlights
- •A small difference in epicardial adipose tissue density has been reported between patients with and without coronary events.
- •However, epicardial adipose tissue is composed of beige fat and its activation may change in response to several stimuli.
- •We show that season, clinical and demographic factors induce a change in epicardial adipose tissue attenuation.
- •We conclude that the numerous confounders influencing adipose tissue attenuation may limit its utility as a marker of risk.
Abstract
Background and aims
A small difference in epicardial adipose tissue (EAT) attenuation measured on computed
tomography (CT) imaging has been reported between patients who suffered coronary events
and event-free patients. EAT consists of beige adipose tissue functionally similar
to brown adipose tissue and its attenuation may be affected by seasonal temperature
variations and clinical factors.
Methods
We retrospectively measured EAT attenuation on cardiac CT in 597 patients submitted
to cardiac CT imaging for coronary artery calcium scoring. All scans were performed
on the same CT scanner during the summer (June, July, August) or winter (December,
January, February) months. EAT attenuation in Hounsfield units (HU) was assessed near
the proximal right coronary artery in an area free of artifacts. For comparison, subcutaneous
adipose tissue (SCAT) attenuation was measure along the midaxillary line.
Results
The clinical and demographic characteristics of patients scanned during the summer
(N = 253) and the winter (N = 344) months were similar. One third of patients were
women, one quarter used statins and anti-hypertensive drugs and 30% were obese. The
EAT attenuation was significantly lower during the summer than the winter months (−98.17 ± 6.94
HUs vs −95.64 ± 7.99 HUs; p<0.001). Sex, white race, body mass index, diabetes status, treatment with statins
and anti-hypertensive agents significantly modulated the seasonal variation in EAT
attenuation. SCAT attenuation was not affected by season or other factors.
Conclusions
The measurement of EAT attenuation is complex and is affected by season, demographic
and clinical factors. These factors may hinder the utilization of EAT attenuation
as a biomarker of cardiovascular risk.
Graphical abstract

Graphical Abstract
Keywords
To read this article in full you will need to make a payment
Purchase one-time access:
Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online accessOne-time access price info
- For academic or personal research use, select 'Academic and Personal'
- For corporate R&D use, select 'Corporate R&D Professionals'
Subscribe:
Subscribe to AtherosclerosisAlready a print subscriber? Claim online access
Already an online subscriber? Sign in
Register: Create an account
Institutional Access: Sign in to ScienceDirect
References
- Uncoupling protein-1 and related messenger ribonucleic acids in human epicardial and other adipose tissues: epicardial fat functioning as brown fat.J. Clin. Endocrinol. Metab. 2009; 94: 3611-3615
- Cardiac computed tomography-derived epicardial fat volume and attenuation independently distinguish patients with and without myocardial infarction.PloS One. 2017; 12e0183514
- 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
- Deep learning-based quantification of epicardial adipose tissue volume and attenuation predicts major adverse cardiovascular events in asymptomatic subjects.Circ Cardiovasc Imaging. 2020; 13e009829
- The endocrine function of adipose tissues in health and cardiometabolic disease.Nat. Rev. Endocrinol. 2019; 15: 507-524
- Human Brown fat radiodensity indicates underlying tissue composition and systemic metabolic health.J. Clin. Endocrinol. Metab. 2017; 102: 2258-2267
- Brown adipose tissue and seasonal variation in humans.Diabetes. 2009; 58: 2583-2587
- Seasonal differences in brown adipose tissue density and pulse rate variability in a thermoneutral environment.J. Physiol. Anthropol. 2018; 37: 6
- Statins reduce epicardial adipose tissue attenuation independent of lipid lowering: a potential pleiotropic effect.J Am Heart Assoc. 2019; 8e013104
- Effect size estimates: current use, calculations, and interpretation.J. Exp. Psychol. Gen. 2012; 141: 2-18
- Adult epicardial fat exhibits beige features.J. Clin. Endocrinol. Metab. 2013; 98: E1448-E1455
- Heterogeneity of white adipose tissue: molecular basis and clinical implications.Exp. Mol. Med. 2016; 48: e215
- High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity.Diabetes. 2009; 58: 1526-1531
- Brown adipose tissue in adult humans: a metabolic renaissance.Endocr. Rev. 2013; 34: 413-438
- Inhibition of mevalonate pathway prevents adipocyte browning in mice and men by affecting protein prenylation.Cell Metabol. 2019; 29: 901-916 e8
- Brown adipose tissue is associated with cardiometabolic health.Nat. Med. 2021; 27: 58-65
- The effects of temperature and seasons on subcutaneous white adipose tissue in humans: evidence for thermogenic gene induction.J. Clin. Endocrinol. Metab. 2014; 99: E2772-E2779
- Opposite actions of testosterone and progesterone on UCP1 mRNA expression in cultured brown adipocytes.Cell. Mol. Life Sci. 2002; 59: 1714-1723
- Differences in sensitivity to cold in Japanese men and postmenopausal women aged > or =50 years.Gend. Med. 2007; 4: 359-366
- Browning of subcutaneous white adipose tissue in humans after severe adrenergic stress.Cell Metabol. 2015; 22: 219-227
- Chronic mirabegron treatment increases human brown fat, HDL cholesterol, and insulin sensitivity.J. Clin. Invest. 2020; 130: 2209-2219
- Reduction of FDG uptake in brown adipose tissue in clinical patients by a single dose of propranolol.Eur. J. Nucl. Med. Mol. Imag. 2007; 34: 1018-1022
- Detecting human coronary inflammation by imaging perivascular fat.Sci. Transl. Med. 2017; 9
- State-of-the-art review article. Atherosclerosis affecting fat: what can we learn by imaging perivascular adipose tissue?.J Cardiovasc Comput Tomogr. 2019; 13: 288-296
- 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: 929-939
- Perivascular fat attenuation index stratifies cardiac risk associated with high-risk plaques in the CRISP-CT study.J. Am. Coll. Cardiol. 2020; 76: 755-757
- Determinants of pericoronary adipose tissue attenuation on computed tomography angiography in coronary artery disease.J Am Heart Assoc. 2020; 9e016202
- Perivascular fat attenuation index and high-risk plaque features evaluated by coronary CT angiography: relationship with serum inflammatory marker level.Int. J. Cardiovasc. Imag. 2020; 36: 723-730
Article Info
Publication History
Published online: February 03, 2021
Accepted:
January 29,
2021
Received in revised form:
January 26,
2021
Received:
January 13,
2021
Identification
Copyright
© 2021 Elsevier B.V. All rights reserved.