Relationship of hepatic steatosis severity and coronary artery disease characteristics assessed by coronary CT angiography

  • Nobuo Tomizawa
  • Shinichi Inoh
  • Takeshi Nojo
  • Sunao Nakamura
Original Paper


The objective of this study was to investigate the relationship between the severity of hepatic steatosis and coronary artery disease characteristics assessed by coronary computed tomography (CT) angiography. This retrospective analysis consisted of 2028 patients. Hepatic steatosis was evaluated by liver attenuation on unenhanced CT and the patients were divided into four groups (≥60 HU, 54–59 HU, 43–53 HU, ≤42 HU). Coronary calcification was calculated using the Agatston method. Obstructive disease was defined as ≥50 % stenosis assessed by CT. A high-risk plaque was defined by a remodeling index >1.1 and low attenuation (<30 HU). Patients with a segment involvement score >4 were determined to have extensive disease. Logistic regression analysis was performed to study multivariate associations. Severity of hepatic steatosis was associated with coronary calcification (p = 0.02), obstructive disease (p < 0.0001), presence of a high-risk plaque (p = 0.0001) and extensive disease (p = 0.001) in the univariate analysis. However, the relationships were attenuated in the multivariate analysis with the exception of obstructive disease (p = 0.04). Liver attenuation of <54 HU was significantly associated with obstructive coronary artery disease independent of conventional risk factors such as age, sex, diabetes mellitus, hypertension, dyslipidemia and smoking (hepatic attenuation 43–53 HU, odds ratio 1.52, 95 % confidence interval 1.11–2.10, p = 0.01; ≤42 HU, odds ratio 1.65, 95 % confidence interval 1.10–2.45, p = 0.02). Although conventional risk factors were stronger predictors of coronary calcification and plaque formation, the severity of hepatic steatosis remained an independent risk factor for obstructive coronary artery disease. Coronary CT angiography may play a potential role in risk stratification for patients with hepatic steatosis.


Coronary artery disease Computed tomography angiography Hepatic steatosis 



This study was supported in part by a JSPS KAKENHI Grant No. (15H00648).

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.


  1. 1.
    Angulo P (2002) Nonalcoholic fatty liver disease. N Engl J Med 346:1221–1231CrossRefPubMedGoogle Scholar
  2. 2.
    Oni ET, Agatston AS, Blaha MJ et al (2013) A systematic review: burden and severity of subclinical cardiovascular disease among those with nonalcoholic fatty liver; Should we care? Atherosclerosis 230:257–258CrossRefGoogle Scholar
  3. 3.
    Puchner SB, Lu MT, Mayrhofer T et al (2015) High-risk coronary plaque at coronary CT angiography is associated with nonalcoholic fatty liver disease, independent of coronary plaque and stenosis burden: results from the ROMICAT II Trial. Radiology 274:693–701CrossRefPubMedGoogle Scholar
  4. 4.
    Chhabra R, O’Keefe JH, Patil H et al (2013) Association of coronary artery calcification with hepatic steatosis in asymptomatic individuals. Mayo Clin Proc 88:1259–1265CrossRefPubMedGoogle Scholar
  5. 5.
    Sung KC, Lim YH, Park S et al (2013) Arterial stiffness, fatty liver and the presence of coronary artery calcium in a large population cohort. Cardiovasc Diabetol 12:162CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Kim D, Choi SY, Park EH et al (2012) Nonalcoholic fatty liver disease is associated with coronary artery calcification. Hepatology 56:605–613CrossRefPubMedGoogle Scholar
  7. 7.
    Assy N, Djibre A, Farah R, Grosovski M, Marmor A (2010) Presence of coronary plaques in patients with nonalcoholic fatty liver disease. Radiology 254:393–400CrossRefPubMedGoogle Scholar
  8. 8.
    Mellinger JL, Pencina KM, Massaro JM et al (2015) Hepatic steatosis and cardiovascular disease outcomes: an analysis of the Framingham Heart Study. J Hepatol 63:470–476CrossRefPubMedGoogle Scholar
  9. 9.
    Wong VW, Wong GL, Yip GW et al (2011) Coronary artery disease and cardiovascular outcomes in patients with non-alcoholic fatty liver disease. Gut 60:1721–1727CrossRefPubMedGoogle Scholar
  10. 10.
    Idilman IS, Akata D, Hazirolan T, Doganay EB, 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. J Diabetes 7:279–286CrossRefPubMedGoogle Scholar
  11. 11.
    Akabame S, Hamaguchi M, Tomiyasu K et al (2008) Evaluation of vulnerable coronary plaques and non-alcoholic fatty liver disease (NAFLD) by 64-detector multislice computed tomography (MSCT). Circ J 72:618–625CrossRefPubMedGoogle Scholar
  12. 12.
    Park YS, Park SH, Lee SS et al (2011) Biopsy-proven nonsteatotic liver in adults: estimation of reference range for difference in attenuation between the liver and the spleen at nonenhanced CT. Radiology 258:760–766CrossRefPubMedGoogle Scholar
  13. 13.
    Dey D, Achenbach S, Schuhbaeck A et al (2014) Comparison of atherosclerotic plaque burden from coronary CT angiography in patients with first acute coronary syndrome and stable coronary artery disease. J Cardiovasc Comput Tomogr 8:368–374CrossRefPubMedGoogle Scholar
  14. 14.
    Motoyama S, Sarai M, Harigaya H et al (2009) Computed tomographic angiography characteristics of atherosclerotic plaques subsequently resulting in acute coronary syndrome. J Am Coll Cardiol 54:49–57CrossRefPubMedGoogle Scholar
  15. 15.
    Bittencourt MS, Hulten E, Ghoshhajra B et al (2014) Prognostic value of nonobstructive and obstructive coronary artery disease detected by coronary computed tomography angiography to identify cardiovascular events. Circ Cardiovasc Imaging 7:282–291CrossRefPubMedGoogle Scholar
  16. 16.
    American Diabetes Association (2014) Executive summary: standards of medical care in diabetes—2014 Diabetes Care 37(Suppl 1):S5–S13Google Scholar
  17. 17.
    Japan Atherosclerosis Society (2007) Japan Atherosclerosis Society (JAS) guidelines for prevention of atherosclerotic cardiovascular diseases. J Atheroscler Thromb Apr:5–57 (in Japanese)Google Scholar
  18. 18.
    Morise AP, Haddad WJ, Beckner D (1997) Development and validation of a clinical score to estimate the probability of coronary artery disease in men and women presenting with suspected coronary disease. Am J Med 102:350–356CrossRefPubMedGoogle Scholar
  19. 19.
    Agatston AS, Janowitz WR, Hildner FJ et al (1990) Quantification of coronary artery calcium using ultrafast computed tomography. J Am Coll Cardiol 15:827–832CrossRefPubMedGoogle Scholar
  20. 20.
    Raff GL, Abidov A, Achenbach S et al (2009) SCCT guidelines for the interpretation and reporting of coronary computed tomographic angiography. J Cardiovasc Comput Tomogr 3:122–136CrossRefPubMedGoogle Scholar
  21. 21.
    Nakazato R, Arsanjani R, Achenbach S et al (2014) Age-related risk of major adverse cardiac event risk and coronary artery disease extent and severity by coronary CT angiography: results from 15187 patients from the International Multisite CONFIRM Study. Eur Heart J Cardiovasc Imaging 15:586–594CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Park SH, Kim PN, Kim KW et al (2006) Macrovesicular hepatic steatosis in living liver donors: use of CT for quantitative and qualitative assessment. Radiology 239:105–112CrossRefPubMedGoogle Scholar
  23. 23.
    Alkhouri N, Tamimi TAR, Yerian L et al (2010) The inflamed liver and atherosclerosis: a link between histologic severity of nonalcoholic fatty liver disease and increased cardiovascular risk. Dig Dis Sci 55:2644–2650CrossRefPubMedGoogle Scholar
  24. 24.
    Bhatia LS, Curzen NP, Byrne CD (2012) Nonalcoholic fatty liver disease and vascular risk. Curr Opin Cardiol 27:420–428CrossRefPubMedGoogle Scholar
  25. 25.
    Biddinger SB, Hemandez-Ono A, Rask-Madsen C et al (2008) Hepatic insulin resistance is sufficient to produce dyslipidemia and susceptibility to atherosclerosis. Cell Metab 7:125–134CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Sung KC, Cha SC, Sung JW, So MS, Byrne CD (2014) Metabolically healthy obese subjects are at risk of fatty liver but not of pre-clinical atherosclerosis. Nutr Metab Cardiovasc Dis 24:256–262CrossRefPubMedGoogle Scholar
  27. 27.
    Tomizawa N, Nojo T, Inoh S, Nakamura S (2015) Difference of coronary artery disease severity, extent and plaque characteristics between patients with hypertension, diabetes mellitus or dyslipidemia. Int J Cardiovasc Imaging 31:205–212CrossRefPubMedGoogle Scholar
  28. 28.
    McKimmie RL, Daniel KR, Carr JJ et al (2008) Hepatic steatosis and subclinical cardiovascular disease in a cohort enriched for type 2 diabetes: the Diabetes Heart Study. Am J Gastroenterol 103:3029–3035CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    An J, Shim JH, Kim SO et al (2014) Prevalence and prediction of coronary artery disease in patients with liver cirrhosis: a registry-based matched case-control study. Circulation 130:1353–1362CrossRefPubMedGoogle Scholar
  30. 30.
    Kodama Y, Ng CS, Wu TT et al (2007) Comparison of CT methods for determining the fat content of the liver. Am J Roentgenol 188:1307–1312CrossRefGoogle Scholar
  31. 31.
    Liu J, Fox CS, Hickson D, Bidulescu A, Carr JJ, Taylor HA (2011) Fatty liver, abdominal visceral fat, and cardiometabolic risk factors: the Jackson Heart Study. Arterioscler Thromb Vasc Biol 31:2715–2722CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    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 1:101–104CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Nobuo Tomizawa
    • 1
  • Shinichi Inoh
    • 1
  • Takeshi Nojo
    • 1
  • Sunao Nakamura
    • 2
  1. 1.Department of RadiologyNew Tokyo HospitalMatsudoJapan
  2. 2.Department of CardiologyNew Tokyo HospitalMatsudoJapan

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