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Association of hepatic steatosis with epicardial fat volume and coronary artery disease in symptomatic patients

  • Cardiac radiology
  • Published:
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Abstract

Aims

This study aims to investigate whether HS—when associated with an excessive amount of epicardial adipose tissue—correlates with CAD in subjects with symptoms suggestive of CVD.

Methods and results

CCTA images, demographic and clinical variables of 1.182 individuals were retrieved: semi-automated measurements for EFV, CAC, and MLD were obtained. Individuals were grouped into three categories according to the presence of CAD, resulting in absent (CAD0), non-obstructive (CAD1) or obstructive (CAD2) disease-groups, and into two categories based on the presence of HS (with no HS, named HS−, and with HS, named HS+). EFV was significantly higher in HS+ than in HS− group (p < 0.001), whereas MLD was lower in CAD+ than in CAD− subjects (p < 0.001). Two predictive models for CAD were tested: the former included clinical risk factors for CAD along with age, gender, EFV and MLD, whereas the latter did not include clinical variables. The logistic regression analysis of the second proposed model reliably discriminated CAD0 from CAD1 and CAD2 (AUC of 0.712, range 0.682–0.742).

Conclusion

Lower MLD was associated with increased EFV, and MLD—as a marker of HS—discriminate symptomatic patients with CAD from whom without.

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Abbreviations

AMI:

Acute myocardial infarction

AUC:

Area under the curve

CAC:

Coronary artery calcium

CAD:

Coronary artery disease

CCTA:

Cardiac computed tomographic angiography

CT:

Computed tomography

CVD:

Cardiovascular disease

DM:

Diabetes mellitus

EAT:

Epicardial adipose tissue

EFV:

Epicardial fat volume

HS:

Hepatic steatosis

IQR:

Inter-quartile range

MLD:

Mean liver density

MR:

Magnetic resonance

NAFLD:

Non-alcoholic fatty liver disease

ROC:

Receiver operating curves

ROI:

Regions of interest

SD:

Standard deviation

References

  1. India State-Level Disease Burden Initiative CVDC (2018) The changing patterns of cardiovascular diseases and their risk factors in the states of India: the Global Burden of Disease Study 1990–2016. Lancet Glob Health 6(12):e1339–e1e51

    Article  Google Scholar 

  2. Antoniades C, Kotanidis CP, Berman DS (2019) State-of-the-art review article. Atherosclerosis affecting fat: what can we learn by imaging perivascular adipose tissue? J Cardiovasc Comput Tomogr 13(5):288–296

    Article  Google Scholar 

  3. Christen T, Trompet S, Rensen PCN, van Dijk KW, Lamb HJ, Jukema JW et al (2019) The role of inflammation in the association between overall and visceral adiposity and subclinical atherosclerosis. Nutr Metab Cardiovasc Dis 29(7):728–735

    Article  CAS  Google Scholar 

  4. Mazurek T, Zhang L, Zalewski A, Mannion JD, Diehl JT, Arafat H et al (2003) Human epicardial adipose tissue is a source of inflammatory mediators. Circulation 108(20):2460–2466

    Article  Google Scholar 

  5. Johnson AR, Milner JJ, Makowski L (2012) The inflammation highway: metabolism accelerates inflammatory traffic in obesity. Immunol Rev 249(1):218–238

    Article  CAS  Google Scholar 

  6. Ansaldo AM, Montecucco F, Sahebkar A, Dallegri F, Carbone F (2019) Epicardial adipose tissue and cardiovascular diseases. Int J Cardiol 278:254–260

    Article  Google Scholar 

  7. Younossi Z, Anstee QM, Marietti M, Hardy T, Henry L, Eslam M et al (2018) Global burden of NAFLD and NASH: trends, predictions, risk factors and prevention. Nat Rev Gastroenterol Hepatol 15(1):11–20

    Article  Google Scholar 

  8. Lucas C, Lucas G, Lucas N, Krzowska-Firych J, Tomasiewicz K (2018) A systematic review of the present and future of non-alcoholic fatty liver disease. Clin Exp Hepatol 4(3):165–174

    Article  Google Scholar 

  9. Brouha SS, Nguyen P, Bettencourt R, Sirlin CB, Loomba R (2018) Increased severity of liver fat content and liver fibrosis in non-alcoholic fatty liver disease correlate with epicardial fat volume in type 2 diabetes: A prospective study. Eur Radiol 28(4):1345–1355

    Article  Google Scholar 

  10. Tang K, Lin J, Ji X, Lin T, Sun D, Zheng X et al (2019) Non-alcoholic fatty liver disease with reduced myocardial FDG uptake is associated with coronary atherosclerosis. J Nucl Cardiol. https://doi.org/10.1007/s12350-019-01736-6

  11. Ferrara D, Montecucco F, Dallegri F, Carbone F (2019) Impact of different ectopic fat depots on cardiovascular and metabolic diseases. J Cell Physiol 234(12):21630–21641

    Article  CAS  Google Scholar 

  12. Cerit M, Sendur HN, Cindil E, Erbas G, Yalcin MM, Cerit ET et al (2020) Quantification of liver fat content with ultrasonographic attenuation measurement function: correlation with unenhanced multidimensional computerized tomography. Clin Imaging 65:85–93

    Article  Google Scholar 

  13. Boudinaud C, Abergel A, Joubert-Zakeyh J, Fontarensky M, Pereira B, Chauveau B et al (2019) Quantification of steatosis in alcoholic and nonalcoholic fatty liver disease: evaluation of four MR techniques versus biopsy. Eur J Radiol 118:169–174

    Article  Google Scholar 

  14. Wong VW, Wong GL, Yip GW, Lo AO, Limquiaco J, Chu WC et al (2011) Coronary artery disease and cardiovascular outcomes in patients with non-alcoholic fatty liver disease. Gut 60(12):1721–1727

    Article  CAS  Google Scholar 

  15. Sun L, Lu SZ (2011) Association between non-alcoholic fatty liver disease and coronary artery disease severity. Chin Med J 124(6):867–872

    CAS  PubMed  Google Scholar 

  16. Idilman IS, Akata D, Hazirolan T, Doganay Erdogan B, Aytemir K, Karcaaltincaba M (2015) Nonalcoholic fatty liver disease is associated with significant coronary artery disease in type 2 diabetic patients: a computed tomography angiography study 2. J Diabetes 7(2):279–286

    Article  CAS  Google Scholar 

  17. Gregoratos G (2001) Clinical manifestations of acute myocardial infarction in older patients. Am J Geriatr Cardiol 10(6):345–347

    Article  CAS  Google Scholar 

  18. Thomas CC, Philipson LH (2015) Update on diabetes classification. Med Clin North Am 99(1):1–16

    Article  Google Scholar 

  19. Milanese G, Silva M, Bruno L, Goldoni M, Benedetti G, Rossi E et al (2019) 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 25(1):35–41

    Article  Google Scholar 

  20. Sarin S, Wenger C, Marwaha A, Qureshi A, Go BD, Woomert CA et al (2008) Clinical significance of epicardial fat measured using cardiac multislice computed tomography. Am J Cardiol 102(6):767–771

    Article  Google Scholar 

  21. Milanese G, Silva M, Ledda RE, Goldoni M, Nayak S, Bruno L et al (2020) Validity of epicardial fat volume as biomarker of coronary artery disease in symptomatic individuals: Results from the ALTER-BIO registry. Int J Cardiol 314:20–4

    Article  Google Scholar 

  22. Austen WG, Edwards JE, Frye RL, Gensini GG, Gott VL, Griffith LS et al (1975) A reporting system on patients evaluated for coronary artery disease. Report of the Ad Hoc Committee for Grading of Coronary Artery Disease, Council on Cardiovascular Surgery, American Heart Association. Circulation 51(4 Suppl):5–40

    Article  CAS  Google Scholar 

  23. Hadamitzky M, Freissmuth B, Meyer T, Hein F, Kastrati A, Martinoff S et al (2009) Prognostic value of coronary computed tomographic angiography for prediction of cardiac events in patients with suspected coronary artery disease. JACC Cardiovasc Imaging 2(4):404–411

    Article  Google Scholar 

  24. Kodama Y, Ng CS, Wu TT, Ayers GD, Curley SA, Abdalla EK et al (2007) Comparison of CT methods for determining the fat content of the liver. AJR Am J Roentgenol 188(5):1307–1312

    Article  Google Scholar 

  25. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA et al (2009) Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 120(16):1640–1645

    Article  CAS  Google Scholar 

  26. Wolff L, Bos D, Murad SD, Franco OH, Krestin GP, Hofman A et al (2016) Liver fat is related to cardiovascular risk factors and subclinical vascular disease: the Rotterdam Study. Eur Heart J Cardiovasc Imaging 17(12):1361–1367

    Article  Google Scholar 

  27. Fracanzani AL, Pisano G, Consonni D, Tiraboschi S, Baragetti A, Bertelli C et al (2016) Epicardial adipose tissue (EAT) thickness is associated with cardiovascular and liver damage in nonalcoholic fatty liver disease. PLoS One 11(9):e0162473

    Article  Google Scholar 

  28. Meng X, Wang W, Zhang K, Qi Y, An S, Wang S et al (2018) Epicardial adipose tissue volume is associated with non-alcoholic fatty liver disease and cardiovascular risk factors in the general population. Ther Clin Risk Manag 14:1499–1506

    Article  CAS  Google Scholar 

  29. Iacobellis G, Barbarini G, Letizia C, Barbaro G (2014) Epicardial fat thickness and nonalcoholic fatty liver disease in obese subjects. Obesity (Silver Spring) 22(2):332–336

    Article  Google Scholar 

  30. Colak Y, Karabay CY, Tuncer I, Kocabay G, Kalayci A, Senates E et al (2012) Relation of epicardial adipose tissue and carotid intima-media thickness in patients with nonalcoholic fatty liver disease. Eur J Gastroenterol Hepatol 24(6):613–618

    Article  Google Scholar 

  31. Clifford SM, Murphy DJ (2019) Non-alcoholic fatty liver disease and coronary atherosclerosis-does myocardial glucose metabolism provide the missing link?. J Nucl Cardiol. https://doi.org/10.1007/s12350-019-01783-z

  32. Wu MY, Li CJ, Hou MF, Chu PY (2017) New insights into the role of inflammation in the pathogenesis of atherosclerosis. Int J Mol Sci 18(10):2034

    Article  Google Scholar 

  33. Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K et al (2012) The diagnosis and management of non-alcoholic fatty liver disease: practice Guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology 55(6):2005–2023

    Article  Google Scholar 

  34. Anstee QM, Targher G, Day CP (2013) Progression of NAFLD to diabetes mellitus, cardiovascular disease or cirrhosis. Nat Rev Gastroenterol Hepatol 10(6):330–344

    Article  CAS  Google Scholar 

  35. Tomizawa N, Inoh S, Nojo T, Nakamura S (2016) Relationship of hepatic steatosis severity and coronary artery disease characteristics assessed by coronary CT angiography. Int J Card Imaging 32(Suppl 1):73–82

    Article  Google Scholar 

  36. Liu HH, Cao YX, Sun D, Jin JL, Guo YL, Wu NQ et al (2019) Impact of non-alcoholic fatty liver disease on cardiovascular outcomes in patients with stable coronary artery disease: a matched case-control study. Clin Transl Gastroenterol 10(2):e00011

    Article  Google Scholar 

  37. Agac MT, Korkmaz L, Cavusoglu G, Karadeniz AG, Agac S, Bektas H et al (2013) Association between nonalcoholic fatty liver disease and coronary artery disease complexity in patients with acute coronary syndrome: a pilot study. Angiology 64(8):604–608

    Article  Google Scholar 

  38. Oni ET, Agatston AS, Blaha MJ, Fialkow J, Cury R, Sposito A et al (2013) A systematic review: burden and severity of subclinical cardiovascular disease among those with nonalcoholic fatty liver; should we care? Atherosclerosis 230(2):258–267

    Article  CAS  Google Scholar 

  39. Perseghin G, Lattuada G, De Cobelli F, Esposito A, Belloni E, Ntali G et al (2008) Increased mediastinal fat and impaired left ventricular energy metabolism in young men with newly found fatty liver. Hepatology 47(1):51–58

    Article  CAS  Google Scholar 

  40. Mills SR, Doppman JL, Nienhuis AW (1977) Computed tomography in the diagnosis of disorders of excessive iron storage of the liver. J Comput Assist Tomogr 1(1):101–104

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Division of Scienze Radiologiche, Department of Medicine and Surgery (DiMeC), University of Parma, Parma, Italy

    Roberta Eufrasia Ledda, Gianluca Milanese, Giorgio Benedetti, Mario Silva & Nicola Sverzellati

  2. Department of Radiology, Area Vasta 1/ASUR Marche, Urbino, Italy

    Filippo Cademartiri & Erica Maffei

  3. Department of Medicine and Surgery, University of Parma, Parma, Italy

    Matteo Goldoni

Authors
  1. Roberta Eufrasia Ledda
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  2. Gianluca Milanese
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  3. Filippo Cademartiri
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  4. Erica Maffei
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  5. Giorgio Benedetti
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  6. Matteo Goldoni
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  7. Mario Silva
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Contributions

Conception and design: R.E.L. and G.M.; Analysis and interpretation of data: M.G. and G.M.; Drafting of the manuscript: R.E.L., G.M., and G.B.; Revising of the manuscript: M.S., F.C., and E.M.; Final approval of the manuscript: N.S. and M.S.

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Correspondence to Nicola Sverzellati.

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Ledda, R.E., Milanese, G., Cademartiri, F. et al. Association of hepatic steatosis with epicardial fat volume and coronary artery disease in symptomatic patients. Radiol med 126, 652–660 (2021). https://doi.org/10.1007/s11547-020-01321-9

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  • DOI: https://doi.org/10.1007/s11547-020-01321-9

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