Skip to main content
Erschienen in: European Radiology 4/2018

20.10.2017 | Cardiac

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

verfasst von: Sharon S. Brouha, Phirum Nguyen, Ricki Bettencourt, Claude B. Sirlin, Rohit Loomba

Erschienen in: European Radiology | Ausgabe 4/2018

Einloggen, um Zugang zu erhalten

Abstract

Objectives

To determine whether severity of non-alcoholic fatty liver disease (NAFLD) and liver fibrosis quantitatively assessed in individuals with diabetes mellitus (DM)-2 correlate with increased coronary heart disease (CHD) risk using non-invasive markers.

Methods

We conducted a single-centre, prospective, cross-sectional study in 100 consecutive diabetic individuals without known CHD recruited between March 2013 and September 2014. History, physical examination, serum markers, cardiac computed tomography (CT), magnetic resonance (MR) imaging-estimated proton density fat fraction (PDFF) and MR elastography (MRE) were obtained for 95 participants. Written informed consent was provided. Institutional review board approved this study. Spearman rank correlation was performed to assess for correlations. Multiple linear regression model determined independent predictors of epicardial adipose tissue (EAT) volume.

Results

A p value < 0.05 determined statistical significance. The EAT volume was higher in the NAFLD group, defined as MR-imaging PDFF ≥ 5 %, compared to the non-NAFLD group (126.5 ml (IQR 80.9) versus 85.4 ml (IQR 44.7), p=0.002). MR imaging-PDFF correlated with EAT (r=0.42, p < 0.0001). MR imaging-PDFF and liver fibrosis were independently associated with EAT.

Conclusions

Higher liver fat content and liver fibrosis may portend worse cardiovascular risk in diabetics.

Key Points

EAT volume is higher in diabetic individuals with NAFLD.
Liver fat content is positively correlated with EAT.
Liver fat content and liver fibrosis were independently associated with EAT.
Higher liver fat content and fibrosis may adversely affect cardiovascular risk.
Literatur
1.
Zurück zum Zitat 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 34:274–285CrossRefPubMed 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 34:274–285CrossRefPubMed
2.
Zurück zum Zitat Targher G, Day CP, Bonora E (2010) Risk of cardiovascular disease in patients with nonalcoholic fatty liver disease. N Engl J Med 363:1341–1350CrossRefPubMed Targher G, Day CP, Bonora E (2010) Risk of cardiovascular disease in patients with nonalcoholic fatty liver disease. N Engl J Med 363:1341–1350CrossRefPubMed
3.
Zurück zum Zitat 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 7:279–286CrossRefPubMed 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 7:279–286CrossRefPubMed
4.
Zurück zum Zitat 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 30:1212–1218CrossRefPubMed 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 30:1212–1218CrossRefPubMed
5.
Zurück zum Zitat 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 30:2119–2121CrossRefPubMed 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 30:2119–2121CrossRefPubMed
6.
Zurück zum Zitat 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 103:3029–3035CrossRefPubMedPubMedCentral 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 103:3029–3035CrossRefPubMedPubMedCentral
7.
Zurück zum Zitat 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–E290CrossRefPubMed 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–E290CrossRefPubMed
8.
Zurück zum Zitat 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 235:599–605CrossRefPubMedPubMedCentral 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 235:599–605CrossRefPubMedPubMedCentral
9.
Zurück zum Zitat Chen CH, Nien CK, Yang CC, Yeh YH (2010) Association between nonalcoholic fatty liver disease and coronary artery calcification. Dig Dis Sci 55:1752–1760CrossRefPubMed Chen CH, Nien CK, Yang CC, Yeh YH (2010) Association between nonalcoholic fatty liver disease and coronary artery calcification. Dig Dis Sci 55:1752–1760CrossRefPubMed
10.
Zurück zum Zitat 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 239:629–633CrossRefPubMedPubMedCentral 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 239:629–633CrossRefPubMedPubMedCentral
11.
Zurück zum Zitat Chhabra R, O'Keefe JH, Patil H et al (2013) Association of coronary artery calcification with hepatic steatosis in asymptomatic individuals. Mayo Clin Proc 88:1259–1265CrossRefPubMed Chhabra R, O'Keefe JH, Patil H et al (2013) Association of coronary artery calcification with hepatic steatosis in asymptomatic individuals. Mayo Clin Proc 88:1259–1265CrossRefPubMed
12.
Zurück zum Zitat 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 2011:586785PubMedPubMedCentral 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 2011:586785PubMedPubMedCentral
13.
Zurück zum Zitat 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 291:210–215CrossRefPubMed 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 291:210–215CrossRefPubMed
14.
Zurück zum Zitat 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 62:928–933CrossRefPubMed 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 62:928–933CrossRefPubMed
15.
Zurück zum Zitat 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 35:2359–2364CrossRefPubMedPubMedCentral 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 35:2359–2364CrossRefPubMedPubMedCentral
16.
Zurück zum Zitat 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 7:28CrossRefPubMedPubMedCentral 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 7:28CrossRefPubMedPubMedCentral
18.
Zurück zum Zitat 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 61:1388–1395CrossRefPubMed 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 61:1388–1395CrossRefPubMed
19.
Zurück zum Zitat 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 105:2893–2898CrossRefPubMed 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 105:2893–2898CrossRefPubMed
20.
Zurück zum Zitat Hirata Y, Kurobe H, Akaike M et al (2011) Enhanced inflammation in epicardial fat in patients with coronary artery disease. Int Heart J 52:139–142CrossRefPubMed Hirata Y, Kurobe H, Akaike M et al (2011) Enhanced inflammation in epicardial fat in patients with coronary artery disease. Int Heart J 52:139–142CrossRefPubMed
21.
Zurück zum Zitat Hirata Y, Tabata M, Kurobe H et al (2011) Coronary atherosclerosis is associated with macrophage polarization in epicardial adipose tissue. J Am Coll Cardiol 58:248–255CrossRefPubMed Hirata Y, Tabata M, Kurobe H et al (2011) Coronary atherosclerosis is associated with macrophage polarization in epicardial adipose tissue. J Am Coll Cardiol 58:248–255CrossRefPubMed
22.
Zurück zum Zitat 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 99:361–369CrossRefPubMed 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 99:361–369CrossRefPubMed
23.
Zurück zum Zitat Mazurek T, Zhang L, Zalewski A et al (2003) Human epicardial adipose tissue is a source of inflammatory mediators. Circulation 108:2460–2466CrossRefPubMed Mazurek T, Zhang L, Zalewski A et al (2003) Human epicardial adipose tissue is a source of inflammatory mediators. Circulation 108:2460–2466CrossRefPubMed
24.
Zurück zum Zitat 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 211:195–199CrossRefPubMed 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 211:195–199CrossRefPubMed
25.
Zurück zum Zitat Alexopoulos N, McLean DS, Janik M, Arepalli CD, Stillman AE, Raggi P (2010) Epicardial adipose tissue and coronary artery plaque characteristics. Atherosclerosis 210:150–154CrossRefPubMed Alexopoulos N, McLean DS, Janik M, Arepalli CD, Stillman AE, Raggi P (2010) Epicardial adipose tissue and coronary artery plaque characteristics. Atherosclerosis 210:150–154CrossRefPubMed
26.
Zurück zum Zitat 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 20:1262–1275CrossRefPubMed 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 20:1262–1275CrossRefPubMed
27.
Zurück zum Zitat 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 106:228–235CrossRefPubMedPubMedCentral 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 106:228–235CrossRefPubMedPubMedCentral
28.
Zurück zum Zitat 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 70:876–882CrossRef 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 70:876–882CrossRef
29.
Zurück zum Zitat Iacobellis G, Barbarini G, Letizia C, Barbaro G (2014) Epicardial fat thickness and nonalcoholic fatty liver disease in obese subjects. Obesity (Silver Spring) 22:332–336CrossRef Iacobellis G, Barbarini G, Letizia C, Barbaro G (2014) Epicardial fat thickness and nonalcoholic fatty liver disease in obese subjects. Obesity (Silver Spring) 22:332–336CrossRef
30.
Zurück zum Zitat Cikim AS, Topal E, Harputluoglu M et al (2007) Epicardial adipose tissue, hepatic steatosis and obesity. J Endocrinol Investig 30:459–464CrossRef Cikim AS, Topal E, Harputluoglu M et al (2007) Epicardial adipose tissue, hepatic steatosis and obesity. J Endocrinol Investig 30:459–464CrossRef
32.
Zurück zum Zitat 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 267:422–431CrossRefPubMedPubMedCentral 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 267:422–431CrossRefPubMedPubMedCentral
33.
Zurück zum Zitat 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 36:22–29CrossRefPubMedPubMedCentral 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 36:22–29CrossRefPubMedPubMedCentral
34.
Zurück zum Zitat 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 61:1239–1250CrossRefPubMedPubMedCentral 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 61:1239–1250CrossRefPubMedPubMedCentral
35.
Zurück zum Zitat 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 63:453–461CrossRefPubMed 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 63:453–461CrossRefPubMed
36.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 43:83–95CrossRefPubMed 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 43:83–95CrossRefPubMed
38.
Zurück zum Zitat 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 60:1920–1928CrossRefPubMedPubMedCentral 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 60:1920–1928CrossRefPubMedPubMedCentral
39.
Zurück zum Zitat 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 58:1930–1940CrossRefPubMedPubMedCentral 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 58:1930–1940CrossRefPubMedPubMedCentral
40.
Zurück zum Zitat 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 111:986–994CrossRefPubMedPubMedCentral 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 111:986–994CrossRefPubMedPubMedCentral
41.
Zurück zum Zitat 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 15:827–832CrossRefPubMed 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 15:827–832CrossRefPubMed
42.
Zurück zum Zitat Dey D, Nakazato R, Li D, Berman DS (2012) Epicardial and thoracic fat - Noninvasive measurement and clinical implications. Cardiovasc Diagn Ther 2:85–93PubMedPubMedCentral Dey D, Nakazato R, Li D, Berman DS (2012) Epicardial and thoracic fat - Noninvasive measurement and clinical implications. Cardiovasc Diagn Ther 2:85–93PubMedPubMedCentral
43.
Zurück zum Zitat 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 112:2735–2752CrossRefPubMed 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 112:2735–2752CrossRefPubMed
44.
Zurück zum Zitat 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 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.
Zurück zum Zitat Clark JM, Brancati FL, Diehl AM (2002) Nonalcoholic fatty liver disease. Gastroenterology 122:1649–1657CrossRefPubMed Clark JM, Brancati FL, Diehl AM (2002) Nonalcoholic fatty liver disease. Gastroenterology 122:1649–1657CrossRefPubMed
46.
Zurück zum Zitat 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 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.
Zurück zum Zitat 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 42:132–138CrossRefPubMed 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 42:132–138CrossRefPubMed
48.
Zurück zum Zitat Fassio E, Alvarez E, Dominguez N, Landeira G, Longo C (2004) Natural history of nonalcoholic steatohepatitis: a longitudinal study of repeat liver biopsies. Hepatology 40:820–826PubMed Fassio E, Alvarez E, Dominguez N, Landeira G, Longo C (2004) Natural history of nonalcoholic steatohepatitis: a longitudinal study of repeat liver biopsies. Hepatology 40:820–826PubMed
49.
Zurück zum Zitat 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 7:909–916CrossRefPubMed 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 7:909–916CrossRefPubMed
Metadaten
Titel
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
verfasst von
Sharon S. Brouha
Phirum Nguyen
Ricki Bettencourt
Claude B. Sirlin
Rohit Loomba
Publikationsdatum
20.10.2017
Verlag
Springer Berlin Heidelberg
Erschienen in
European Radiology / Ausgabe 4/2018
Print ISSN: 0938-7994
Elektronische ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-017-5075-6

Weitere Artikel der Ausgabe 4/2018

European Radiology 4/2018 Zur Ausgabe

Vascular-Interventional

In memoriam Prof. Erik Boijsen

Update Radiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.