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

European Radiology

Volumn 28, Issue 4, 2018, Pages 1345-1355

  Brouha, Sharon S ^a   Nguyen, Phirum ^a,b   Bettencourt, Ricki ^a,b   Sirlin, Claude B ^a   Loomba, Rohit ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Coronary disease; Liver fibrosis; Magnetic resonance imaging; Multidetector computed tomography; Non alcoholic fatty liver disease

Indexed keywords

ALANINE AMINOTRANSFERASE; ALKALINE PHOSPHATASE; ASPARTATE AMINOTRANSFERASE; FATTY ACID; FERRITIN; GAMMA GLUTAMYLTRANSFERASE; GLUCOSE; HEMOGLOBIN A1C; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INSULIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; TRIACYLGLYCEROL;

ADIPOSE TISSUE; ADULT; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALKALINE PHOSPHATASE BLOOD LEVEL; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BODY MASS; CARDIOVASCULAR RISK; CHOLESTEROL BLOOD LEVEL; COMPUTER ASSISTED TOMOGRAPHY; CORONARY ARTERY CALCIUM SCORE; CORRELATIONAL STUDY; CROSS-SECTIONAL STUDY; DIABETIC PATIENT; DISEASE SEVERITY; ELASTOGRAPHY; EPICARDIAL FAT; FAT CONTENT; FATTY ACID BLOOD LEVEL; FEMALE; FERRITIN BLOOD LEVEL; GAMMA GLUTAMYL TRANSFERASE BLOOD LEVEL; GLUCOSE LEVEL; HEMOGLOBIN BLOOD LEVEL; HOMEOSTASIS MODEL ASSESSMENT; HUMAN; INFORMED CONSENT; INSTITUTIONAL REVIEW; INSULIN LEVEL; INSULIN RESISTANCE; ISCHEMIC HEART DISEASE; LIVER FIBROSIS; MAGNETIC RESONANCE ELASTOGRAPHY; MAJOR CLINICAL STUDY; MALE; MEDICAL HISTORY; MIDDLE AGED; NON INSULIN DEPENDENT DIABETES MELLITUS; NONALCOHOLIC FATTY LIVER; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSICAL EXAMINATION; PLATELET COUNT; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTON DENSITY FAT FRACTION; RADIOCARDIOGRAPHY; RADIOLOGICAL PROCEDURES; TRIACYLGLYCEROL BLOOD LEVEL; COMPLICATION; CORONARY ARTERY DISEASE; DIAGNOSTIC IMAGING; LIVER; LIVER CIRRHOSIS; PATHOLOGY; PERICARDIUM; PROCEDURES; SEVERITY OF ILLNESS INDEX;

ADIPOSE TISSUE; CORONARY DISEASE; CROSS-SECTIONAL STUDIES; DIABETES MELLITUS, TYPE 2; ELASTICITY IMAGING TECHNIQUES; FEMALE; HUMANS; LIVER; LIVER CIRRHOSIS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NON-ALCOHOLIC FATTY LIVER DISEASE; PERICARDIUM; PROSPECTIVE STUDIES; SEVERITY OF ILLNESS INDEX;

EID: 85031933822     PISSN: 09387994     EISSN: 14321084     Source Type: Journal    
DOI: 10.1007/s00330-017-5075-6     Document Type: Article

References (49)

1. Vernon G, Baranova A, Younossi ZM (2011) Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther 34:274–285
2. Targher G, Day CP, Bonora E (2010) Risk of cardiovascular disease in patients with nonalcoholic fatty liver disease. N Engl J Med 363:1341–1350
3. 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 7:279–286
4. Targher G, Bertolini L, Padovani R et al (2007) Prevalence of nonalcoholic fatty liver disease and its association with cardiovascular disease among type 2 diabetic patients. Diabetes Care 30:1212–1218
5. Targher G, Bertolini L, Rodella S et al (2007) Nonalcoholic fatty liver disease is independently associated with an increased incidence of cardiovascular events in type 2 diabetic patients. Diabetes Care 30:2119–2121
6. 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 103:3029–3035
7. Lautamaki R, Borra R, Iozzo P et al (2006) Liver steatosis coexists with myocardial insulin resistance and coronary dysfunction in patients with type 2 diabetes. Am J Physiol Endocrinol Metab 291:E282–E290
8. VanWagner LB, Ning H, Lewis CE et al (2014) Associations between nonalcoholic fatty liver disease and subclinical atherosclerosis in middle-aged adults: the Coronary Artery Risk Development in Young Adults Study. Atherosclerosis 235:599–605
9. Chen CH, Nien CK, Yang CC, Yeh YH (2010) Association between nonalcoholic fatty liver disease and coronary artery calcification. Dig Dis Sci 55:1752–1760
10. Al Rifai M, Silverman MG, Nasir K et al (2015) The association of nonalcoholic fatty liver disease, obesity, and metabolic syndrome, with systemic inflammation and subclinical atherosclerosis: the Multi-Ethnic Study of Atherosclerosis (MESA). Atherosclerosis 239:629–633
11. Chhabra R, O'Keefe JH, Patil H et al (2013) Association of coronary artery calcification with hepatic steatosis in asymptomatic individuals. Mayo Clin Proc 88:1259–1265
12. Lee YH, Wu YJ, Liu CC et al (2011) The severity of Fatty liver disease relating to metabolic abnormalities independently predicts coronary calcification. Radiol Res Pract 2011:586785
13. Greenland P, LaBree L, Azen SP, Doherty TM, Detrano RC (2004) Coronary artery calcium score combined with Framingham score for risk prediction in asymptomatic individuals. JAMA 291:210–215
14. Petta S, Argano C, Colomba D et al (2015) Epicardial fat, cardiac geometry and cardiac function in patients with non-alcoholic fatty liver disease: association with the severity of liver disease. J Hepatol 62:928–933
15. Sung KC, Wild SH, Kwag HJ, Byrne CD (2012) Fatty liver, insulin resistance, and features of metabolic syndrome: relationships with coronary artery calcium in 10,153 people. Diabetes Care 35:2359–2364
16. Kwak MS, Yim JY, Kim D et al (2015) Nonalcoholic fatty liver disease is associated with coronary artery calcium score in diabetes patients with higher HbA1c. Diabetol Metab Syndr 7:28
17. Spearman JV, Renker M, Schoepf UJ et al (2015) Prognostic value of epicardial fat volume measurements by computed tomography: a systematic review of the literature. Eur Radiol. https://doi.org/10.1007/s00330-015-3765-5
18. Mahabadi AA, Berg MH, Lehmann N et al (2013) 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 61:1388–1395
19. Arita Y, Kihara S, Ouchi N et al (2002) Adipocyte-derived plasma protein adiponectin acts as a platelet-derived growth factor-BB-binding protein and regulates growth factor-induced common postreceptor signal in vascular smooth muscle cell. Circulation 105:2893–2898
20. Hirata Y, Kurobe H, Akaike M et al (2011) Enhanced inflammation in epicardial fat in patients with coronary artery disease. Int Heart J 52:139–142
21. Hirata Y, Tabata M, Kurobe H et al (2011) Coronary atherosclerosis is associated with macrophage polarization in epicardial adipose tissue. J Am Coll Cardiol 58:248–255
22. Laine P, Kaartinen M, Penttila A, Panula P, Paavonen T, Kovanen PT (1999) Association between myocardial infarction and the mast cells in the adventitia of the infarct-related coronary artery. Circulation 99:361–369
23. Mazurek T, Zhang L, Zalewski A et al (2003) Human epicardial adipose tissue is a source of inflammatory mediators. Circulation 108:2460–2466
24. Mahabadi AA, Reinsch N, Lehmann N et al (2010) Association of pericoronary fat volume with atherosclerotic plaque burden in the underlying coronary artery: a segment analysis. Atherosclerosis 211:195–199
25. Alexopoulos N, McLean DS, Janik M, Arepalli CD, Stillman AE, Raggi P (2010) Epicardial adipose tissue and coronary artery plaque characteristics. Atherosclerosis 210:150–154
26. Virmani R, Kolodgie FD, Burke AP, Farb A, Schwartz SM (2000) Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions. Arterioscler Thromb Vasc Biol 20:1262–1275
27. Mohar DS, Salcedo J, Hoang KC et al (2014) Epicardial adipose tissue volume as a marker of coronary artery disease severity in patients with diabetes independent of coronary artery calcium: findings from the CTRAD study. Diabetes Res Clin Pract 106:228–235
28. Wang CP, Hsu HL, Hung WC et al (2009) Increased epicardial adipose tissue (EAT) volume in type 2 diabetes mellitus and association with metabolic syndrome and severity of coronary atherosclerosis. Clin Endocrinol 70:876–882
29. Iacobellis G, Barbarini G, Letizia C, Barbaro G (2014) Epicardial fat thickness and nonalcoholic fatty liver disease in obese subjects. Obesity (Silver Spring) 22:332–336
30. Cikim AS, Topal E, Harputluoglu M et al (2007) Epicardial adipose tissue, hepatic steatosis and obesity. J Endocrinol Investig 30:459–464
31. Psychari SN, Rekleiti N, Papaioannou N et al (2015) Epicardial Fat in Nonalcoholic Fatty Liver Disease: Properties and Relationships With Metabolic Factors, Cardiac Structure, and Cardiac Function. Angiology. https://doi.org/10.1177/0003319715576672
32. Tang A, Tan J, Sun M et al (2013) Nonalcoholic fatty liver disease: MR imaging of liver proton density fat fraction to assess hepatic steatosis. Radiology 267:422–431
33. Permutt Z, Le TA, Peterson MR et al (2012) Correlation between liver histology and novel magnetic resonance imaging in adult patients with non-alcoholic fatty liver disease - MRI accurately quantifies hepatic steatosis in NAFLD. Aliment Pharmacol Ther 36:22–29
34. Loomba R, Sirlin CB, Ang B et al (2015) Ezetimibe for the treatment of nonalcoholic steatohepatitis: assessment by novel magnetic resonance imaging and magnetic resonance elastography in a randomized trial (MOZART trial). Hepatology 61:1239–1250
35. Cui J, Heba E, Hernandez C et al (2016) Magnetic resonance elastography is superior to acoustic radiation force impulse for the Diagnosis of fibrosis in patients with biopsy-proven nonalcoholic fatty liver disease: A prospective study. Hepatology 63:453–461
36. Dulai PS, Sirlin CB, Loomba R (2016) MRI and MRE for non-invasive quantitative assessment of hepatic steatosis and fibrosis in NAFLD and NASH: Clinical trials to clinical practice. J Hepatol. in press
37. Doycheva I, Cui J, Nguyen P et al (2016) Non-invasive screening of diabetics in primary care for NAFLD and advanced fibrosis by MRI and MRE. Aliment Pharmacol Ther 43:83–95
38. Loomba R, Wolfson T, Ang B et al (2014) Magnetic resonance elastography predicts advanced fibrosis in patients with nonalcoholic fatty liver disease: a prospective study. Hepatology 60:1920–1928
39. Noureddin M, Lam J, Peterson MR et al (2013) Utility of magnetic resonance imaging versus histology for quantifying changes in liver fat in nonalcoholic fatty liver disease trials. Hepatology 58:1930–1940
40. Loomba R, Cui J, Wolfson T et al (2016) Novel 3D Magnetic Resonance Elastography for the Noninvasive Diagnosis of Advanced Fibrosis in NAFLD: A Prospective Study. Am J Gastroenterol 111:986–994
41. Agatston AS, Janowitz WR, Hildner FJ, Zusmer NR, Viamonte M Jr, Detrano R (1990) Quantification of coronary artery calcium using ultrafast computed tomography. J Am Coll Cardiol 15:827–832
42. Dey D, Nakazato R, Li D, Berman DS (2012) Epicardial and thoracic fat - Noninvasive measurement and clinical implications. Cardiovasc Diagn Ther 2:85–93
43. Grundy SM, Cleeman JI, Daniels SR et al (2005) Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation 112:2735–2752
44. Graner M, Nyman K, Siren R et al (2015) Ectopic fat depots and left ventricular function in nondiabetic men with nonalcoholic fatty liver disease. Circ Cardiovasc Imaging 8
45. Clark JM, Brancati FL, Diehl AM (2002) Nonalcoholic fatty liver disease. Gastroenterology 122:1649–1657
46. Dong MH, Bettencourt R, Brenner DA, Barrett-Connor E, Loomba R (2012) Serum levels of alanine aminotransferase decrease with age in longitudinal analysis. Clin Gastroenterol Hepatol 10(285-290):e281
47. Adams LA, Sanderson S, Lindor KD, Angulo P (2005) The histological course of nonalcoholic fatty liver disease: a longitudinal study of 103 patients with sequential liver biopsies. J Hepatol 42:132–138
48. Fassio E, Alvarez E, Dominguez N, Landeira G, Longo C (2004) Natural history of nonalcoholic steatohepatitis: a longitudinal study of repeat liver biopsies. Hepatology 40:820–826
49. Mahabadi AA, Lehmann N, Kalsch H et al (2014) Association of epicardial adipose tissue with progression of coronary artery calcification is more pronounced in the early phase of atherosclerosis: results from the Heinz Nixdorf recall study. JACC Cardiovasc Imaging 7:909–916