Skip to main content
Top
Published in: BMC Cardiovascular Disorders 1/2020

Open Access 01-12-2020 | CT Angiography | Research article

Relation between quantity and quality of peri-coronary epicardial adipose tissue and its underlying hemodynamically significant coronary stenosis

Authors: Yu Du, Lin Yang, Yan Liu, Bangguo Yang, Sai Lv, Chenping Hu, Yong Zhu, Hongkai Zhang, Qian Ma, Zhijian Wang, Yuyang Liu, Dongmei Shi, Yingxin Zhao, Lei Xu, Yujie Zhou

Published in: BMC Cardiovascular Disorders | Issue 1/2020

Login to get access

Abstract

Background

We aimed to investigate the association of lesion-specific epicardial adipose tissue (EAT) volume and density with the presence of myocardial ischemia.

Methods

We enrolled 45 patients (55 lesions) with known or suspected coronary artery disease who underwent coronary computed tomography angiography (CTA) followed by invasive fractional flow reserve (FFR) assessment within 30 days. EAT volume (index) and density in patient-, vessel- and lesion-level were measured on CTA images. Lesion-specific ischemia was defined as a lesion with stenosis diameter > 90% or FFR ≤0.80. Multivariate analysis determined the independent association of EAT parameters with lesion-specific ischemia.

Results

Mean age of the patients was 60 years, and 75% were male. Overall, 55.6% of patients had ischemic lesions and a mean FFR baseline value of 0.82 ± 0.10. Total EAT volume index was significantly higher in patients with functionally or anatomically significant stenosis. Specifically, peri-lesion EAT volume index, not the density, was positively correlated with lesion-specific ischemia independent of luminal stenosis and plaque characteristics (hazard ratio 1.56, 95% confidence interval 1.04–2.33, P = 0.032; per 0.1 ml/m2 increase). Moreover, peri-lesion EAT volume was negatively correlated with lesion FFR values, whereas total EAT volume was positively correlated with fat accumulation and glucose metabolism. In addition, there was no association of EAT volume or density with myocardial ischemia in vessel-level analysis.

Conclusions

Lesion-specific EAT volume index, but not density, seems positively and independently associated with myocardial ischemia, while its incremental diagnostic value of lesion-specific ischemia should be further investigated.
Appendix
Available only for authorised users
Literature
1.
go back to reference Iacobellis G, Corradi D, Sharma AM. Epicardial adipose tissue: anatomic, biomolecular and clinical relationships with the heart. Nat Clin Pract Cardiovasc Med. 2005;2(10):536–43.PubMedCrossRef Iacobellis G, Corradi D, Sharma AM. Epicardial adipose tissue: anatomic, biomolecular and clinical relationships with the heart. Nat Clin Pract Cardiovasc Med. 2005;2(10):536–43.PubMedCrossRef
2.
go back to reference Sinha SK, Thakur R, Jha MJ, Goel A, Kumar V, Kumar A, Mishra V, Varma CM, Krishna V, Singh AK, et al. Epicardial adipose tissue thickness and its association with the presence and severity of coronary artery disease in clinical setting: a cross-sectional observational study. J Clin Med Res. 2016;8(5):410–9.PubMedPubMedCentralCrossRef Sinha SK, Thakur R, Jha MJ, Goel A, Kumar V, Kumar A, Mishra V, Varma CM, Krishna V, Singh AK, et al. Epicardial adipose tissue thickness and its association with the presence and severity of coronary artery disease in clinical setting: a cross-sectional observational study. J Clin Med Res. 2016;8(5):410–9.PubMedPubMedCentralCrossRef
3.
go back to reference Nakazato R, Dey D, Cheng VY, Gransar H, Slomka PJ, Hayes SW, Thomson LE, Friedman JD, Min JK, Berman DS. Epicardial fat volume and concurrent presence of both myocardial ischemia and obstructive coronary artery disease. Atherosclerosis. 2012;221(2):422–6.PubMedCrossRef Nakazato R, Dey D, Cheng VY, Gransar H, Slomka PJ, Hayes SW, Thomson LE, Friedman JD, Min JK, Berman DS. Epicardial fat volume and concurrent presence of both myocardial ischemia and obstructive coronary artery disease. Atherosclerosis. 2012;221(2):422–6.PubMedCrossRef
4.
go back to reference Nerlekar N, Brown AJ, Muthalaly RG, Talman A, Hettige T, Cameron JD, DTL W. Association of Epicardial Adipose Tissue and High-Risk Plaque Characteristics: A Systematic Review and Meta-Analysis. J Am Heart Assoc. 2017;6(8). Nerlekar N, Brown AJ, Muthalaly RG, Talman A, Hettige T, Cameron JD, DTL W. Association of Epicardial Adipose Tissue and High-Risk Plaque Characteristics: A Systematic Review and Meta-Analysis. J Am Heart Assoc. 2017;6(8).
5.
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.PubMedCrossRef 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.PubMedCrossRef
6.
go back to reference Akoumianakis I, Antoniades C. The interplay between adipose tissue and the cardiovascular system: is fat always bad? Cardiovasc Res. 2017;113(9):999–1008.PubMedCrossRef Akoumianakis I, Antoniades C. The interplay between adipose tissue and the cardiovascular system: is fat always bad? Cardiovasc Res. 2017;113(9):999–1008.PubMedCrossRef
7.
go back to reference Shimokawa H, Ito A, Fukumoto Y, Kadokami T, Nakaike R, Sakata M, Takayanagi T, Egashira K, Takeshita A. Chronic treatment with interleukin-1 beta induces coronary intimal lesions and vasospastic responses in pigs in vivo. The role of platelet-derived growth factor. J Clin Invest. 1996;97(3):769–76.PubMedPubMedCentralCrossRef Shimokawa H, Ito A, Fukumoto Y, Kadokami T, Nakaike R, Sakata M, Takayanagi T, Egashira K, Takeshita A. Chronic treatment with interleukin-1 beta induces coronary intimal lesions and vasospastic responses in pigs in vivo. The role of platelet-derived growth factor. J Clin Invest. 1996;97(3):769–76.PubMedPubMedCentralCrossRef
8.
go back to reference Miyata K, Shimokawa H, Kandabashi T, Higo T, Morishige K, Eto Y, Egashira K, Kaibuchi K, Takeshita A. Rho-kinase is involved in macrophage-mediated formation of coronary vascular lesions in pigs in vivo. Arterioscler Thromb Vasc Biol. 2000;20(11):2351–8.PubMedCrossRef Miyata K, Shimokawa H, Kandabashi T, Higo T, Morishige K, Eto Y, Egashira K, Kaibuchi K, Takeshita A. Rho-kinase is involved in macrophage-mediated formation of coronary vascular lesions in pigs in vivo. Arterioscler Thromb Vasc Biol. 2000;20(11):2351–8.PubMedCrossRef
9.
go back to reference McKenney ML, Schultz KA, Boyd JH, Byrd JP, Alloosh M, Teague SD, Arce-Esquivel AA, Fain JN, Laughlin MH, Sacks HS, et al. Epicardial adipose excision slows the progression of porcine coronary atherosclerosis. J Cardiothorac Surg. 2014;9:2.PubMedPubMedCentralCrossRef McKenney ML, Schultz KA, Boyd JH, Byrd JP, Alloosh M, Teague SD, Arce-Esquivel AA, Fain JN, Laughlin MH, Sacks HS, et al. Epicardial adipose excision slows the progression of porcine coronary atherosclerosis. J Cardiothorac Surg. 2014;9:2.PubMedPubMedCentralCrossRef
10.
go back to reference Franssens BT, Nathoe HM, Leiner T, van der Graaf Y, Visseren FL. Relation between cardiovascular disease risk factors and epicardial adipose tissue density on cardiac computed tomography in patients at high risk of cardiovascular events. Eur J Prev Cardiol. 2017;24(6):660–70.PubMedCrossRef Franssens BT, Nathoe HM, Leiner T, van der Graaf Y, Visseren FL. Relation between cardiovascular disease risk factors and epicardial adipose tissue density on cardiac computed tomography in patients at high risk of cardiovascular events. Eur J Prev Cardiol. 2017;24(6):660–70.PubMedCrossRef
11.
go back to reference Antonopoulos AS, Sanna F, Sabharwal N, Thomas S, Oikonomou EK, Herdman L, Margaritis M, Shirodaria C, Kampoli AM, Akoumianakis I, et al. Detecting human coronary inflammation by imaging perivascular fat. Sci Transl Med. 2017;9(398). Antonopoulos AS, Sanna F, Sabharwal N, Thomas S, Oikonomou EK, Herdman L, Margaritis M, Shirodaria C, Kampoli AM, Akoumianakis I, et al. Detecting human coronary inflammation by imaging perivascular fat. Sci Transl Med. 2017;9(398).
12.
go back to reference Oikonomou EK, Marwan M, Desai MY, Mancio J, Alashi A, Hutt Centeno E, Thomas S, Herdman L, Kotanidis CP, Thomas KE, 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 (London). 2018;392(10151):929–39.CrossRef Oikonomou EK, Marwan M, Desai MY, Mancio J, Alashi A, Hutt Centeno E, Thomas S, Herdman L, Kotanidis CP, Thomas KE, 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 (London). 2018;392(10151):929–39.CrossRef
13.
go back to reference Halliburton SS, Abbara S, Chen MY, Gentry R, Mahesh M, Raff GL, Shaw LJ, Hausleiter J. SCCT guidelines on radiation dose and dose-optimization strategies in cardiovascular CT. J Cardiovasc Comput Tomogr. 2011;5(4):198–224.PubMedPubMedCentralCrossRef Halliburton SS, Abbara S, Chen MY, Gentry R, Mahesh M, Raff GL, Shaw LJ, Hausleiter J. SCCT guidelines on radiation dose and dose-optimization strategies in cardiovascular CT. J Cardiovasc Comput Tomogr. 2011;5(4):198–224.PubMedPubMedCentralCrossRef
14.
go back to reference Xu L, Xu Y, Coulden R, Sonnex E, Hrybouski S, Paterson I, Butler C. Comparison of epicardial adipose tissue radiodensity threshold between contrast and non-contrast enhanced computed tomography scans: a cohort study of derivation and validation. Atherosclerosis. 2018;275:74–9.PubMedCrossRef Xu L, Xu Y, Coulden R, Sonnex E, Hrybouski S, Paterson I, Butler C. Comparison of epicardial adipose tissue radiodensity threshold between contrast and non-contrast enhanced computed tomography scans: a cohort study of derivation and validation. Atherosclerosis. 2018;275:74–9.PubMedCrossRef
15.
go back to reference Khawaja T, Greer C, Thadani SR, Kato TS, Bhatia K, Shimbo D, Kontak A, Bokhari S, Einstein AJ, Schulze PC. Increased regional epicardial fat volume associated with reversible myocardial ischemia in patients with suspected coronary artery disease. J Nucl Cardiol. 2015;22(2):325–33.PubMedCrossRef Khawaja T, Greer C, Thadani SR, Kato TS, Bhatia K, Shimbo D, Kontak A, Bokhari S, Einstein AJ, Schulze PC. Increased regional epicardial fat volume associated with reversible myocardial ischemia in patients with suspected coronary artery disease. J Nucl Cardiol. 2015;22(2):325–33.PubMedCrossRef
16.
go back to reference Mahabadi AA, Reinsch N, Lehmann N, Altenbernd J, Kalsch H, Seibel RM, Erbel R, Mohlenkamp S. Association of pericoronary fat volume with atherosclerotic plaque burden in the underlying coronary artery: a segment analysis. Atherosclerosis. 2010;211(1):195–9.PubMedCrossRef Mahabadi AA, Reinsch N, Lehmann N, Altenbernd J, Kalsch H, Seibel RM, Erbel R, Mohlenkamp S. Association of pericoronary fat volume with atherosclerotic plaque burden in the underlying coronary artery: a segment analysis. Atherosclerosis. 2010;211(1):195–9.PubMedCrossRef
17.
go back to reference Pijls NH, De Bruyne B, Peels K, Van Der Voort PH, Bonnier HJ, Bartunek JKJJ, Koolen JJ. Measurement of fractional flow reserve to assess the functional severity of coronary-artery stenoses. N Engl J Med. 1996;334(26):1703–8.PubMedCrossRef Pijls NH, De Bruyne B, Peels K, Van Der Voort PH, Bonnier HJ, Bartunek JKJJ, Koolen JJ. Measurement of fractional flow reserve to assess the functional severity of coronary-artery stenoses. N Engl J Med. 1996;334(26):1703–8.PubMedCrossRef
18.
go back to reference Muthalaly RG, Nerlekar N, Wong DT, Cameron JD, Seneviratne SK, Ko BS. Epicardial adipose tissue and myocardial ischemia assessed by computed tomography perfusion imaging and invasive fractional flow reserve. J Cardiovasc Comput Tomogr. 2017;11(1):46–53.PubMedCrossRef Muthalaly RG, Nerlekar N, Wong DT, Cameron JD, Seneviratne SK, Ko BS. Epicardial adipose tissue and myocardial ischemia assessed by computed tomography perfusion imaging and invasive fractional flow reserve. J Cardiovasc Comput Tomogr. 2017;11(1):46–53.PubMedCrossRef
19.
go back to reference Tanami Y, Jinzaki M, Kishi S, Matheson M, Vavere AL, Rochitte CE, Dewey M, Chen MY, Clouse ME, Cox C, et al. Lack of association between epicardial fat volume and extent of coronary artery calcification, severity of coronary artery disease, or presence of myocardial perfusion abnormalities in a diverse, symptomatic patient population: results from the CORE320 multicenter study. Circ Cardiovasc Imaging. 2015;8(3):e002676.PubMedPubMedCentralCrossRef Tanami Y, Jinzaki M, Kishi S, Matheson M, Vavere AL, Rochitte CE, Dewey M, Chen MY, Clouse ME, Cox C, et al. Lack of association between epicardial fat volume and extent of coronary artery calcification, severity of coronary artery disease, or presence of myocardial perfusion abnormalities in a diverse, symptomatic patient population: results from the CORE320 multicenter study. Circ Cardiovasc Imaging. 2015;8(3):e002676.PubMedPubMedCentralCrossRef
20.
go back to reference Romijn MA, Danad I, Bakkum MJ, Stuijfzand WJ, Tulevski II, Somsen GA, Lammertsma AA, van Kuijk C, van de Ven PM, Min JK, et al. Incremental diagnostic value of epicardial adipose tissue for the detection of functionally relevant coronary artery disease. Atherosclerosis. 2015;242(1):161–6.PubMedCrossRef Romijn MA, Danad I, Bakkum MJ, Stuijfzand WJ, Tulevski II, Somsen GA, Lammertsma AA, van Kuijk C, van de Ven PM, Min JK, et al. Incremental diagnostic value of epicardial adipose tissue for the detection of functionally relevant coronary artery disease. Atherosclerosis. 2015;242(1):161–6.PubMedCrossRef
21.
go back to reference Mancio J, Azevedo D, Saraiva F, Azevedo AI, Pires-Morais G, Leite-Moreira A, Falcao-Pires I, Lunet N, Bettencourt N. 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.PubMedCrossRef Mancio J, Azevedo D, Saraiva F, Azevedo AI, Pires-Morais G, Leite-Moreira A, Falcao-Pires I, Lunet N, Bettencourt N. 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.PubMedCrossRef
22.
go back to reference Verhagen SN, Visseren FL. Perivascular adipose tissue as a cause of atherosclerosis. Atherosclerosis. 2011;214(1):3–10.PubMedCrossRef Verhagen SN, Visseren FL. Perivascular adipose tissue as a cause of atherosclerosis. Atherosclerosis. 2011;214(1):3–10.PubMedCrossRef
23.
go back to reference Verhagen SN, Vink A, van der Graaf Y, Visseren FL. Coronary perivascular adipose tissue characteristics are related to atherosclerotic plaque size and composition. A post-mortem study. Atherosclerosis. 2012;225(1):99–104.PubMedCrossRef Verhagen SN, Vink A, van der Graaf Y, Visseren FL. Coronary perivascular adipose tissue characteristics are related to atherosclerotic plaque size and composition. A post-mortem study. Atherosclerosis. 2012;225(1):99–104.PubMedCrossRef
24.
go back to reference Hassan M, Said K, Rizk H, ElMogy F, Donya M, Houseni M, Yacoub M. Segmental peri-coronary epicardial adipose tissue volume and coronary plaque characteristics. Eur Heart J Cardiovasc Imaging. 2016;17(10):1169–77.PubMedCrossRef Hassan M, Said K, Rizk H, ElMogy F, Donya M, Houseni M, Yacoub M. Segmental peri-coronary epicardial adipose tissue volume and coronary plaque characteristics. Eur Heart J Cardiovasc Imaging. 2016;17(10):1169–77.PubMedCrossRef
25.
go back to reference Balcer B, Dykun I, Schlosser T, Forsting M, Rassaf T, Mahabadi AA. Pericoronary fat volume but not attenuation differentiates culprit lesions in patients with myocardial infarction. Atherosclerosis. 2018;276:182–8.PubMedCrossRef Balcer B, Dykun I, Schlosser T, Forsting M, Rassaf T, Mahabadi AA. Pericoronary fat volume but not attenuation differentiates culprit lesions in patients with myocardial infarction. Atherosclerosis. 2018;276:182–8.PubMedCrossRef
26.
go back to reference Verhagen SN, Buijsrogge MP, Vink A, van Herwerden LA, van der Graaf Y, Visseren FL. Secretion of adipocytokines by perivascular adipose tissue near stenotic and non-stenotic coronary artery segments in patients undergoing CABG. Atherosclerosis. 2014;233(1):242–7.PubMedCrossRef Verhagen SN, Buijsrogge MP, Vink A, van Herwerden LA, van der Graaf Y, Visseren FL. Secretion of adipocytokines by perivascular adipose tissue near stenotic and non-stenotic coronary artery segments in patients undergoing CABG. Atherosclerosis. 2014;233(1):242–7.PubMedCrossRef
27.
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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
28.
go back to reference Marwan M, Hell M, Schuhback A, Gauss S, Bittner D, Pflederer T, Achenbach S. CT attenuation of Pericoronary adipose tissue in Normal versus atherosclerotic coronary segments as defined by intravascular ultrasound. J Comput Assist Tomogr. 2017;41(5):762–7.PubMedCrossRef Marwan M, Hell M, Schuhback A, Gauss S, Bittner D, Pflederer T, Achenbach S. CT attenuation of Pericoronary adipose tissue in Normal versus atherosclerotic coronary segments as defined by intravascular ultrasound. J Comput Assist Tomogr. 2017;41(5):762–7.PubMedCrossRef
29.
go back to reference Konishi M, Sugiyama S, Sato Y, Oshima S, Sugamura K, Nozaki T, Ohba K, Matsubara J, Sumida H, Nagayoshi Y, et al. Pericardial fat inflammation correlates with coronary artery disease. Atherosclerosis. 2010;213(2):649–55.PubMedCrossRef Konishi M, Sugiyama S, Sato Y, Oshima S, Sugamura K, Nozaki T, Ohba K, Matsubara J, Sumida H, Nagayoshi Y, et al. Pericardial fat inflammation correlates with coronary artery disease. Atherosclerosis. 2010;213(2):649–55.PubMedCrossRef
30.
go back to reference Kwiecinski J, Dey D, Cadet S, Lee SE, Otaki Y, Huynh PT, Doris MK, Eisenberg E, Yun M, Jansen MA, et al. Peri-coronary adipose tissue density is associated with (18) F-sodium fluoride coronary uptake in stable patients with high-risk plaques. J Am Coll Cardiol Img. 2019;12(10):2000–10.CrossRef Kwiecinski J, Dey D, Cadet S, Lee SE, Otaki Y, Huynh PT, Doris MK, Eisenberg E, Yun M, Jansen MA, et al. Peri-coronary adipose tissue density is associated with (18) F-sodium fluoride coronary uptake in stable patients with high-risk plaques. J Am Coll Cardiol Img. 2019;12(10):2000–10.CrossRef
31.
go back to reference Hell MM, Ding X, Rubeaux M, Slomka P, Gransar H, Terzopoulos D, Hayes S, Marwan M, Achenbach S, Berman DS, et al. Epicardial adipose tissue volume but not density is an independent predictor for myocardial ischemia. J Cardiovasc Comput Tomogr. 2016;10(2):141–9.PubMedCrossRef Hell MM, Ding X, Rubeaux M, Slomka P, Gransar H, Terzopoulos D, Hayes S, Marwan M, Achenbach S, Berman DS, et al. Epicardial adipose tissue volume but not density is an independent predictor for myocardial ischemia. J Cardiovasc Comput Tomogr. 2016;10(2):141–9.PubMedCrossRef
Metadata
Title
Relation between quantity and quality of peri-coronary epicardial adipose tissue and its underlying hemodynamically significant coronary stenosis
Authors
Yu Du
Lin Yang
Yan Liu
Bangguo Yang
Sai Lv
Chenping Hu
Yong Zhu
Hongkai Zhang
Qian Ma
Zhijian Wang
Yuyang Liu
Dongmei Shi
Yingxin Zhao
Lei Xu
Yujie Zhou
Publication date
01-12-2020
Publisher
BioMed Central
Keyword
CT Angiography
Published in
BMC Cardiovascular Disorders / Issue 1/2020
Electronic ISSN: 1471-2261
DOI
https://doi.org/10.1186/s12872-020-01499-w

Other articles of this Issue 1/2020

BMC Cardiovascular Disorders 1/2020 Go to the issue