{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,22]],"date-time":"2026-10-22T02:28:21Z","timestamp":1792636101563,"version":"4.5.0"},"reference-count":30,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2020,2,10]],"date-time":"2020-02-10T00:00:00Z","timestamp":1581292800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2020,2,10]],"date-time":"2020-02-10T00:00:00Z","timestamp":1581292800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100009708","name":"Novo Nordisk Fonden","doi-asserted-by":"publisher","award":["NNF OC0013659"],"award-info":[{"award-number":["NNF OC0013659"]}],"id":[{"id":"10.13039\/501100009708","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Cardiovasc Diabetol"],"published-print":{"date-parts":[[2020,12]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n<jats:title>Background<\/jats:title>\n<jats:p>Cardiac adipose tissue may have local paracrine effects on epicardial arteries and the underlying myocardium, promoting calcification and affecting myocardial microcirculation. We explored whether the total amount of cardiac adipose tissue was associated with coronary artery calcium score (CAC) and myocardial flow reserve in persons with type 1 or type 2 diabetes and healthy controls.<\/jats:p>\n<\/jats:sec><jats:sec>\n<jats:title>Methods<\/jats:title>\n<jats:p>We studied three groups: (1) 30 controls, (2) 60 persons with type 1 diabetes and (3) 60 persons with type 2 diabetes. The three groups were matched for sex and age. The three groups derived from retrospective analysis of two clinical studies. All underwent cardiac <jats:sup>82<\/jats:sup>Rb positron emission tomography\/computed tomography (PET\/CT) scanning. Cardiac adipose tissue volume (the sum of epicardial and pericardial fat), CAC, and myocardial flow reserve (ratio of pharmacological stress flow and rest flow) were evaluated using semiautomatic software. We applied linear regression to assess the association between cardiac adipose tissue, CAC and myocardial flow reserve.<\/jats:p>\n<\/jats:sec><jats:sec>\n<jats:title>Results<\/jats:title>\n<jats:p>Mean (SD) cardiac adipose tissue volume was 99 (61) mL in the control group, 106 (78) mL in the type 1 diabetes group and 228 (97) mL in the type 2 diabetes group. Cardiac adipose tissue was positively associated with body mass index in all three groups (p\u2009\u2264\u20090.02). In the controls, cardiac adipose tissue was positively associated with CAC score (p\u2009=\u20090.008) and negatively associated with myocardial flow reserve (p\u2009=\u20090.005). However, cardiac adipose tissue was not associated with CAC or myocardial flow reserve in the groups including persons with type 1 or type 2 diabetes (p\u2009\u2265\u20090.50).<\/jats:p>\n<\/jats:sec><jats:sec>\n<jats:title>Conclusions<\/jats:title>\n<jats:p>In contrast to what was found in healthy controls, we could not establish a relation between cardiac adipose tissue and coronary calcification or myocardial microvascular function in person with type 1 or type 2 diabetes. The role of cardiac adipose tissue in cardiovascular disease in diabetes remains unclear.<\/jats:p>\n<\/jats:sec>","DOI":"10.1186\/s12933-020-0995-x","type":"journal-article","created":{"date-parts":[[2020,2,10]],"date-time":"2020-02-10T17:02:50Z","timestamp":1581354170000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":24,"title":["Relation of cardiac adipose tissue to coronary calcification and myocardial microvascular function in type 1 and type 2 diabetes"],"prefix":"10.1186","volume":"19","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3318-7070","authenticated-orcid":false,"given":"Emilie H.","family":"Zobel","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Regitse H\u00f8jgaard","family":"Christensen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Signe A.","family":"Winther","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Philip","family":"Hasbak","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christian Stevns","family":"Hansen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bernt J.","family":"von Scholten","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lene","family":"Holmvang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andreas","family":"Kjaer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"Rossing","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tine W.","family":"Hansen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2020,2,10]]},"reference":[{"issue":"10","key":"995_CR1","doi-asserted-by":"publisher","first-page":"1177","DOI":"10.1016\/j.jcmg.2015.12.024","volume":"9","author":"AA Mahabadi","year":"2016","unstructured":"Mahabadi AA, Lehmann N, Mohlenkamp 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\u201385.","journal-title":"JACC Cardiovasc Imaging"},{"issue":"1","key":"995_CR2","doi-asserted-by":"publisher","first-page":"114","DOI":"10.1186\/s12933-019-0917-y","volume":"18","author":"RH Christensen","year":"2019","unstructured":"Christensen RH, von Scholten BJ, Hansen CS, Jensen MT, Vilsboll T, Rossing P, et al. Epicardial adipose tissue predicts incident cardiovascular disease and mortality in patients with type 2 diabetes. Cardiovasc Diabetol. 2019;18(1):114.","journal-title":"Cardiovasc Diabetol"},{"key":"995_CR3","doi-asserted-by":"publisher","first-page":"230","DOI":"10.1016\/j.atherosclerosis.2019.01.033","volume":"284","author":"Z Liu","year":"2019","unstructured":"Liu Z, Wang S, Wang Y, Zhou N, Shu J, Stamm C, et al. Association of epicardial adipose tissue attenuation with coronary atherosclerosis in patients with a high risk of coronary artery disease. Atherosclerosis. 2019;284:230\u20136.","journal-title":"Atherosclerosis"},{"issue":"1","key":"995_CR4","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1186\/s12933-019-0927-9","volume":"18","author":"M Packer","year":"2019","unstructured":"Packer M. Disease-treatment interactions in the management of patients with obesity and diabetes who have atrial fibrillation: the potential mediating influence of epicardial adipose tissue. Cardiovasc Diabetol. 2019;18(1):121.","journal-title":"Cardiovasc Diabetol"},{"issue":"10","key":"995_CR5","doi-asserted-by":"publisher","first-page":"1492","DOI":"10.1016\/j.hrthm.2019.06.009","volume":"16","author":"A Sepehri Shamloo","year":"2019","unstructured":"Sepehri Shamloo A, Schoene K, Stauber A, Darma A, Dagres N, Dinov B, et al. Epicardial adipose tissue thickness as an independent predictor of ventricular tachycardia recurrence following ablation. Heart Rhythm. 2019;16(10):1492\u20138.","journal-title":"Heart Rhythm"},{"issue":"1","key":"995_CR6","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1186\/s12933-019-0861-x","volume":"18","author":"M Svanteson","year":"2019","unstructured":"Svanteson M, Holte KB, Haig Y, Klow NE, Berg TJ. Coronary plaque characteristics and epicardial fat tissue in long term survivors of type 1 diabetes identified by coronary computed tomography angiography. Cardiovasc Diabetol. 2019;18(1):58.","journal-title":"Cardiovasc Diabetol"},{"issue":"20","key":"995_CR7","doi-asserted-by":"publisher","first-page":"2460","DOI":"10.1161\/01.CIR.0000099542.57313.C5","volume":"108","author":"T Mazurek","year":"2003","unstructured":"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\u20136.","journal-title":"Circulation"},{"issue":"5","key":"995_CR8","doi-asserted-by":"publisher","first-page":"1153","DOI":"10.3390\/ijms20051153","volume":"20","author":"N D\u2019Onofrio","year":"2019","unstructured":"D\u2019Onofrio N, Pieretti G, Ciccarelli F, Gambardella A, Passariello N, Rizzo MR, et al. Abdominal fat SIRT6 expression and its relationship with inflammatory and metabolic pathways in pre-diabetic overweight patients. Int J Mol Sci. 2019;20(5):1153.","journal-title":"Int J Mol Sci"},{"key":"995_CR9","doi-asserted-by":"publisher","first-page":"1030","DOI":"10.3389\/fphys.2018.01030","volume":"9","author":"C Sardu","year":"2018","unstructured":"Sardu C, Pieretti G, D\u2019Onofrio N, Ciccarelli F, Paolisso P, Passavanti MB, et al. Inflammatory cytokines and SIRT1 levels in subcutaneous abdominal fat: relationship with cardiac performance in overweight pre-diabetics patients. Front Physiol. 2018;9:1030.","journal-title":"Front Physiol"},{"issue":"20","key":"995_CR10","doi-asserted-by":"publisher","first-page":"2360","DOI":"10.1016\/j.jacc.2018.03.509","volume":"71","author":"M Packer","year":"2018","unstructured":"Packer M. Epicardial adipose tissue may mediate deleterious effects of obesity and inflammation on the myocardium. J Am Coll Cardiol. 2018;71(20):2360\u201372.","journal-title":"J Am Coll Cardiol"},{"issue":"4","key":"995_CR11","doi-asserted-by":"publisher","first-page":"303","DOI":"10.1016\/j.jcct.2015.03.005","volume":"9","author":"Y Otaki","year":"2015","unstructured":"Otaki Y, Hell M, Slomka PJ, Schuhbaeck A, Gransar H, Huber B, et al. Relationship of epicardial fat volume from noncontrast CT with impaired myocardial flow reserve by positron emission tomography. J Cardiovasc Comput Tomogr. 2015;9(4):303\u20139.","journal-title":"J Cardiovasc Comput Tomogr"},{"issue":"1","key":"995_CR12","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1016\/j.amjcard.2013.09.022","volume":"113","author":"WJ Chen","year":"2014","unstructured":"Chen WJ, Danad I, Raijmakers PG, Halbmeijer R, Harms HJ, Lammertsma AA, et al. Effect of type 2 diabetes mellitus on epicardial adipose tissue volume and coronary vasomotor function. Am J Cardiol. 2014;113(1):90\u20137.","journal-title":"Am J Cardiol"},{"issue":"6","key":"995_CR13","doi-asserted-by":"publisher","first-page":"876","DOI":"10.1111\/j.1365-2265.2008.03411.x","volume":"70","author":"CP Wang","year":"2009","unstructured":"Wang CP, Hsu HL, Hung WC, Yu TH, Chen YH, Chiu CA, et al. Increased epicardial adipose tissue (EAT) volume in type 2 diabetes mellitus and association with metabolic syndrome and severity of coronary atherosclerosis. Clin Endocrinol. 2009;70(6):876\u201382.","journal-title":"Clin Endocrinol"},{"issue":"8","key":"995_CR14","doi-asserted-by":"publisher","first-page":"e006379","DOI":"10.1161\/JAHA.117.006379","volume":"6","author":"N Nerlekar","year":"2017","unstructured":"Nerlekar N, Brown AJ, Muthalaly RG, Talman A, Hettige T, Cameron JD, et al. Association of epicardial adipose tissue and high-risk plaque characteristics: a systematic review and meta-analysis. J Am Heart Assoc. 2017;6(8):e006379.","journal-title":"J Am Heart Assoc"},{"issue":"6","key":"995_CR15","doi-asserted-by":"publisher","first-page":"517","DOI":"10.1093\/ehjci\/jes024","volume":"13","author":"MO Versteylen","year":"2012","unstructured":"Versteylen MO, Takx RA, Joosen IA, Nelemans PJ, Das M, Crijns HJ, et al. Epicardial adipose tissue volume as a predictor for coronary artery disease in diabetic, impaired fasting glucose, and non-diabetic patients presenting with chest pain. Eur Heart J Cardiovasc Imaging. 2012;13(6):517\u201323.","journal-title":"Eur Heart J Cardiovasc Imaging"},{"issue":"3","key":"995_CR16","doi-asserted-by":"publisher","first-page":"e002676","DOI":"10.1161\/CIRCIMAGING.114.002676","volume":"8","author":"Y Tanami","year":"2015","unstructured":"Tanami Y, Jinzaki M, Kishi S, Matheson M, Vavere AL, Rochitte CE, 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.","journal-title":"Circ Cardiovasc Imaging"},{"issue":"8","key":"995_CR17","doi-asserted-by":"publisher","first-page":"1244","DOI":"10.1161\/CIRCRESAHA.115.307765","volume":"118","author":"V Parisi","year":"2016","unstructured":"Parisi V, Rengo G, Perrone-Filardi P, Pagano G, Femminella GD, Paolillo S, et al. Increased epicardial adipose tissue volume correlates with cardiac sympathetic denervation in patients with heart failure. Circ Res. 2016;118(8):1244\u201353.","journal-title":"Circ Res"},{"issue":"2","key":"995_CR18","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1007\/s00125-015-3799-x","volume":"59","author":"BJ von Scholten","year":"2016","unstructured":"von Scholten BJ, Hasbak P, Christensen TE, Ghotbi AA, Kjaer A, Rossing P, et al. Cardiac (82)Rb PET\/CT for fast and non-invasive assessment of microvascular function and structure in asymptomatic patients with type 2 diabetes. Diabetologia. 2016;59(2):371\u20138.","journal-title":"Diabetologia"},{"key":"995_CR19","doi-asserted-by":"publisher","first-page":"796","DOI":"10.1093\/ehjci\/jey174","volume":"20","author":"EH Zobel","year":"2018","unstructured":"Zobel EH, Winther SA, Hasbak P, von Scholten BJ, Holmvang L, Kjaer A, et al. Myocardial flow reserve assessed by cardiac 82Rb positron emission tomography\/computed tomography is associated with albumin excretion in patients with Type 1 diabetes. Eur Heart J Cardiovasc Imaging. 2018;20:796\u2013803.","journal-title":"Eur Heart J Cardiovasc Imaging"},{"key":"995_CR20","doi-asserted-by":"publisher","first-page":"1277","DOI":"10.2337\/db18-1313","volume":"68","author":"EH Zobel","year":"2019","unstructured":"Zobel EH, Hasbak P, Winther SA, Stevns C, Fleischer J, von Scholten BJ, et al. Cardiac autonomic function is associated with myocardial flow reserve in type 1 diabetes. Diabetes. 2019;68:1277\u201386.","journal-title":"Diabetes"},{"issue":"10","key":"995_CR21","doi-asserted-by":"publisher","first-page":"3129","DOI":"10.2337\/db16-0437","volume":"65","author":"BJ von Scholten","year":"2016","unstructured":"von Scholten BJ, Hansen CS, Hasbak P, Kjaer A, Rossing P, Hansen TW. Cardiac autonomic function is associated with the coronary microcirculatory function in patients with type 2 diabetes. Diabetes. 2016;65(10):3129\u201338.","journal-title":"Diabetes"},{"issue":"5","key":"995_CR22","doi-asserted-by":"publisher","first-page":"605","DOI":"10.1161\/CIRCULATIONAHA.107.743062","volume":"117","author":"GA Rosito","year":"2008","unstructured":"Rosito GA, Massaro JM, Hoffmann U, Ruberg FL, Mahabadi AA, Vasan RS, et al. Pericardial fat, visceral abdominal fat, cardiovascular disease risk factors, and vascular calcification in a community-based sample: the Framingham Heart Study. Circulation. 2008;117(5):605\u201313.","journal-title":"Circulation"},{"issue":"10151","key":"995_CR23","doi-asserted-by":"publisher","first-page":"929","DOI":"10.1016\/S0140-6736(18)31114-0","volume":"392","author":"EK Oikonomou","year":"2018","unstructured":"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(10151):929\u201339.","journal-title":"Lancet"},{"issue":"1","key":"995_CR24","doi-asserted-by":"publisher","first-page":"126","DOI":"10.1186\/s12933-019-0931-0","volume":"18","author":"C Sardu","year":"2019","unstructured":"Sardu C, D\u2019Onofrio N, Torella M, Portoghese M, Loreni F, Mureddu S, et al. Pericoronary fat inflammation and Major Adverse Cardiac Events (MACE) in prediabetic patients with acute myocardial infarction: effects of metformin. Cardiovasc Diabetol. 2019;18(1):126.","journal-title":"Cardiovasc Diabetol"},{"issue":"10","key":"995_CR25","doi-asserted-by":"publisher","first-page":"1946","DOI":"10.2337\/dc18-2356","volume":"42","author":"C Sardu","year":"2019","unstructured":"Sardu C, Paolisso P, Sacra C, Mauro C, Minicucci F, Portoghese M, et al. Effects of metformin therapy on coronary endothelial dysfunction in patients with prediabetes with stable angina and nonobstructive coronary artery stenosis: the CODYCE multicenter prospective study. Diabetes Care. 2019;42(10):1946\u201355.","journal-title":"Diabetes Care"},{"issue":"5","key":"995_CR26","doi-asserted-by":"publisher","first-page":"287","DOI":"10.4330\/wjc.v7.i5.287","volume":"7","author":"Z Saad","year":"2015","unstructured":"Saad Z, El-Rawy M, Donkol RH, Boghattas S. Quantification of epicardial fat: which method can predict significant coronary artery disease? World J Cardiol. 2015;7(5):287\u201392.","journal-title":"World J Cardiol"},{"issue":"1","key":"995_CR27","doi-asserted-by":"publisher","first-page":"18","DOI":"10.2478\/jce-2019-0001","volume":"5","author":"M Ratiu","year":"2018","unstructured":"Ratiu M, Rat N, Nyulas T, Moldovan G, Rus V, Benedek T, et al. Coronary plaque geometry and thoracic fat distribution in patients with acute chest pain\u2014a CT angiography study. J Cardiovasc Emerg. 2018;5(1):18\u201324.","journal-title":"J Cardiovasc Emerg"},{"key":"995_CR28","doi-asserted-by":"publisher","first-page":"2006","DOI":"10.1111\/dom.13758","volume":"21","author":"RH Christensen","year":"2019","unstructured":"Christensen RH, Hansen CS, von Scholten BJ, Jensen MT, Pedersen BK, Schnohr P, et al. Epicardial and pericardial adipose tissues are associated with reduced diastolic and systolic function in type 2 diabetes. Diabetes Obes Metab. 2019;21:2006\u201311.","journal-title":"Diabetes Obes Metab"},{"issue":"1","key":"995_CR29","doi-asserted-by":"publisher","first-page":"35","DOI":"10.5152\/dir.2018.18037","volume":"25","author":"G Milanese","year":"2019","unstructured":"Milanese G, Silva M, Bruno L, Goldoni M, Benedetti G, Rossi E, et al. Quantification of epicardial fat with cardiac CT angiography and association with cardiovascular risk factors in symptomatic patients: from the ALTER-BIO (Alternative Cardiovascular Bio-Imaging markers) registry. Diagn Interv Radiol. 2019;25(1):35\u201341.","journal-title":"Diagn Interv Radiol"},{"issue":"3","key":"995_CR30","doi-asserted-by":"publisher","first-page":"422","DOI":"10.1038\/ijo.2011.117","volume":"36","author":"B Gaborit","year":"2012","unstructured":"Gaborit B, Kober F, Jacquier A, Moro PJ, Cuisset T, Boullu S, 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. 2012;36(3):422\u201330.","journal-title":"Int J Obes"}],"container-title":["Cardiovascular Diabetology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12933-020-0995-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1186\/s12933-020-0995-x\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12933-020-0995-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,2,9]],"date-time":"2021-02-09T01:35:46Z","timestamp":1612834546000},"score":1,"resource":{"primary":{"URL":"https:\/\/cardiab.biomedcentral.com\/articles\/10.1186\/s12933-020-0995-x"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,2,10]]},"references-count":30,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2020,12]]}},"alternative-id":["995"],"URL":"https:\/\/doi.org\/10.1186\/s12933-020-0995-x","relation":{},"ISSN":["1475-2840"],"issn-type":[{"value":"1475-2840","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,2,10]]},"assertion":[{"value":"20 November 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"27 January 2020","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"10 February 2020","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"Both studies were conducted in accordance with the Helsinki declaration. The protocols were approved by the local Ethics Committee and all participants gave informed written consent.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"16"}}