Nonalcoholic fatty liver disease as a potential risk factor of cardiovascular disease

European Journal of Gastroenterology and Hepatology

Volumn 27, Issue 3, 2015, Pages 193-199

  Luo, Jun ^a   Xu, Li ^b   Li, Jiang ^a   Zhao, Shuiping ^a  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b The First People s Hospital of Changde City)   (China)

Author keywords

cardiovascular disease; nonalcoholic fatty liver disease; obesity

Indexed keywords

ADIPOCYTOKINE; ALPHA TOCOPHEROL; ANGIOTENSIN RECEPTOR ANTAGONIST; GLUCAGON LIKE PEPTIDE 1 DERIVATIVE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; LIVER ENZYME; OMEGA 3 FATTY ACID; PIOGLITAZONE; TETRAHYDROLIPSTATIN;

AMINOTRANSFERASE BLOOD LEVEL; ARTERIAL WALL THICKNESS; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CAUSE OF DEATH; CHILDHOOD OBESITY; CORONARY ARTERY DISEASE; ECHOGRAPHY; ENDOTHELIAL DYSFUNCTION; HIGH RISK PATIENT; HUMAN; INSULIN RESISTANCE; LIFESTYLE MODIFICATION; LIVER BIOPSY; NONALCOHOLIC FATTY LIVER; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; CARDIOVASCULAR DISEASES; COMPLICATION; EVIDENCE BASED MEDICINE; NON-ALCOHOLIC FATTY LIVER DISEASE; OBESITY; PREVALENCE; PROCEDURES; RISK FACTOR;

CARDIOVASCULAR DISEASES; EVIDENCE-BASED MEDICINE; HUMANS; NON-ALCOHOLIC FATTY LIVER DISEASE; OBESITY; PREVALENCE; RISK FACTORS;

EID: 84922399024     PISSN: 0954691X     EISSN: 14735687     Source Type: Journal    
DOI: 10.1097/MEG.0000000000000254     Document Type: Review

References (87)

1. Procopiou M, Philippe J. The metabolic syndrome and type 2 diabetes: epidemiological figures and country specificities. Cerebrovasc Dis 2005; Suppl 1:2-8.
2. Younossi ZM, Gramlich T, Liu YC, Matteoni C, Petrelli M, Goldblum J, et al. Nonalcoholic fatty liver disease: assessment of variability in pathologic interpretations. Mod Pathol 1998; 11:560-565.
3. Browning JD, Szczepaniak LS, Dobbins R, Nuremberg P, Horton JD, Cohen JC, et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 2004; 40:1387-1395.
4. Cohen JC, Horton JD, Hobbs HH. Human fatty liver disease: old questions and new insights. Science 2011; 332:1519-1523.
5. Adams LA, Angulo P. Recent concepts in non-Alcoholic fatty liver disease. Diabet Med 2005; 22:1129-1133.
6. McCullough AJ. Pathophysiology of nonalcoholic steatohepatitis. J Clin Gastroenterol 2006; Suppl 1:S17-S29.
7. Marchesini G, Marzocchi R, Agostini F, Bugianesi E. Nonalcoholic fatty liver disease and the metabolic syndrome. Curr Opin Lipidol 2005; 16:421-427.
8. Neuschwander-Tetri BA. Nonalcoholic steatohepatitis and the metabolic syndrome. Am J Med Sci 2005; 330:326-335.
9. Lavine JE, Schwimmer JB. Nonalcoholic fatty liver disease in the pediatric population. Clin Liver Dis 2004; 8:549-558, viii-ix.
10. Gastaldelli A, Kozakova M, Hjlund K, Flyvbjerg A, Favuzzi A, Mitrakou A, Balkau B. RISC Investigators. Fatty liver is associated with insulin resistance, risk of coronary heart disease, and early atherosclerosis in a large European population. Hepatology 2009; 49:1537-1544.
11. Choi SY, Kim D, Kim HJ, Kang JH, Chung SJ, Park MJ, et al. The relation between non-Alcoholic fatty liver disease and the risk of coronary heart disease in Koreans. Am J Gastroenterol 2009; 104:1953-1960.
12. Yilmaz Y, Senates E, Ayyildiz T, Colak Y, Tuncer I, Ovunc AO, et al. Characterization of nonalcoholic fatty liver disease unrelated to the metabolic syndrome. Eur J Clin Invest 2012; 42:411-418.
13. Ghouri N, Preiss D, Sattar N. Liver enzymes, nonalcoholic fatty liver disease, and incident cardiovascular disease: a narrative review and clinical perspective of prospective data. Hepatology 2010; 52:1156-1161.
14. Targher G, Day CP. Liver enzymes, nonalcoholic fatty liver disease, and incident cardiovascular disease. Hepatology 2011; 53:375.
15. Villanova N, Moscatiello S, Ramilli S, Bugianesi E, Magalotti D, Vanni E, et al. Endothelial dysfunction and cardiovascular risk profile in nonalcoholic fatty liver disease. Hepatology 2005; 42:473-480.
16. Crouse JR , Craven TE, Hagaman AP, Bond MG. Association of coronary disease with segment-specific intimal-medial thickening of the extracranial carotid artery. Circulation 1995; 92:1141-1147.
17. Nagai Y, Metter EJ, Earley CJ, Kemper MK, Becker LC, Lakatta EG, Fleg JL. Increased carotid artery intimal-medial thickness in asymptomatic older subjects with exercise-induced myocardial ischemia. Circulation 1998; 98:1504-1509.
18. Targher G, Bertolini L, Padovani R, Zenari L, Zoppini G, Falezza G. Relation of nonalcoholic hepatic steatosis to early carotid atherosclerosis in healthy men: role of visceral fat accumulation. Diabetes Care 2004; 27:2498-2500.
19. Brea A, Mosquera D, Martín E, Arizti A, Cordero JL, Ros E. Nonalcoholic fatty liver disease is associated with carotid atherosclerosis: a case-control study. Arterioscler Thromb Vasc Biol 2005; 25:1045-1050.
20. Volzke H, Robinson DM, Kleine V, Deutscher R, Hoffmann W, Ludemann J, et al. Hepatic steatosis is associated with an increased risk of carotid atherosclerosis. World J Gastroenterol 2005; 11:1848-1853.
21. Targher G, Bertolini L, Padovani R, Rodella S, Zoppini G, Zenari L, et al. Relations between carotid artery wall thickness and liver histology in subjects with nonalcoholic fatty liver disease. Diabetes Care 2006; 29:1325-1330.
22. Fracanzani AL, Burdick L, Raselli S, Pedotti P, Grigore L, Santorelli G, et al. Carotid artery intima-media thickness in nonalcoholic fatty liver disease. Am J Med 2008; 121:72-78.
23. Kim HC, Kim DJ, Huh KB. Association between nonalcoholic fatty liver disease and carotid intima-media thickness according to the presence of metabolic syndrome. Atherosclerosis 2009; 204:521-525.
24. Sookoian S, Pirola CJ. Non-Alcoholic fatty liver disease is strongly associated with carotid atherosclerosis: a systematic review. J Hepatol 2008; 49:600-607.
25. Maurantonio M, Ballestri S, Odoardi MR, Lonardo A, Loria P. Treatment of atherogenic liver based on the pathogenesis of nonalcoholic fatty liver disease: a novel approach to reduce cardiovascular risk? Arch Med Res 2011; 42:337-353.
26. Bhatia LS, Curzen NP, Calder PC, Byrne CD. Non-Alcoholic fatty liver disease: a new and important cardiovascular risk factor? Eur Heart J 2012; 33:1190-1200.
27. Targher G, Day CP, Bonora E. Risk of cardiovascular disease in patients with nonalcoholic fatty liver disease. N Engl J Med 2010; 363:1341-1350.
28. Basar O, Akbal E, Köklü S, Tuna Y, Koak E, Basar N, et al. Increased H-FABP concentrations in nonalcoholic fatty liver disease. Possible marker for subclinical myocardial damage and subclinical atherosclerosis. Herz 2013; 38:417-422.
29. Targher G, Bertolini L, Padovani R, Rodella S, Tessari R, Zenari L, et al. Prevalence of nonalcoholic fatty liver disease and its association with cardiovascular disease among type 2 diabetic patients. Diabetes Care 2007; 30:1212-1218.
30. Targher G, Bertolini L, Padovani R, Rodella S, Zoppini G, Pichiri I, et al. Prevalence of non-Alcoholic fatty liver disease and its association with cardiovascular disease in patients with type 1 diabetes. J Hepatol 2010; 53:713-718.
31. Lin YC, Lo HM, Chen JD. Sonographic fatty liver, overweight and ischemic heart disease. World J Gastroenterol 2005; 11:4838-4842.
32. Boddi M, Tarquini R, Chiostri M, Marra F, Valente S, Giglioli C, et al. Nonalcoholic fatty liver in nondiabetic patients with acute coronary syndromes. Eur J Clin Invest 2013; 43:429-438.
33. Cicero AF, D'Addato S, Reggi A, Marchesini G, Borghi C. Brisighella Heart Study. Gender difference in hepatic steatosis index and lipid accumulation product ability to predict incident metabolic syndrome in the historical cohort of the Brisighella Heart Study. Metab Syndr Relat Disord 2013; 11:412-416.
34. Schwimmer JB, Deutsch R, Behling C, Lavine JE. Fatty liver as a determinant of atherosclerosis. Hepatology 2005; 42 (Suppl):610A abstract.
35. Matteoni CA, Younossi ZM, Gramlich T, Boparai N, Liu YC, McCullough AJ. Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity. Gastroenterology 1999; 116:1413-1419.
36. Dam-Larsen S, Franzmann M, Andersen IB, Christoffersen P, Jensen LB, Srensen TI, et al. Long term prognosis of fatty liver: risk of chronic liver disease and death. Gut 2004; 53:750-755.
37. Adams LA, Lymp JF, St Sauver J, Sanderson SO, Lindor KD, Feldstein A, Angulo P. The natural history of nonalcoholic fatty liver disease: a populationbased cohort study. Gastroenterology 2005; 129:113-121.
38. Ekstedt M, Franzén LE, Mathiesen UL, Thorelius L, Holmqvist M, Bodemar G, Kechagias S. Long-term follow-up of patients with NAFLD and elevated liver enzymes. Hepatology 2006; 44:865-873.
39. Rafiq N, Bai C, Fang Y, Srishord M, McCullough A, Gramlich T, Younossi ZM. Long-term follow-up of patients with nonalcoholic fatty liver. Clin Gastroenterol Hepatol 2009; 7:234-238.
40. Söderberg C, Stl P, Askling J, Glaumann H, Lindberg G, Marmur J, Hultcrantz R. Decreased survival of subjects with elevated liver function tests during a 28-year follow-up. Hepatology 2010; 51:595-602.
41. Ruttmann E, Brant LJ, Concin H, Diem G, Rapp K, Ulmer H. Vorarlberg Health Monitoring and Promotion Program Study Group. Gamma-glutamyl transferase as a risk factor for cardiovascular disease mortality: an epidemiological investigation in a cohort of 163, 944 Austrian adults. Circulation 2005; 112:2130-2137.
42. Lee DS, Evans JC, Robins SJ, Wilson PW, Albano I, Fox CS, et al. Gamma glutamyl transferase and metabolic syndrome, cardiovascular disease, and mortality risk: the Framingham Heart Study. Arterioscler Thromb Vasc Biol 2007; 27:127-133.
43. Lee DH, Silventoinen K, Hu G, Jacobs DR Jr, Jousilahti P, Sundvall J, Tuomilehto J. Serum gamma-glutamyltransferase predicts non-fatal myocardial infarction and fatal coronary heart disease among 28, 838 middleaged men and women. Eur Heart J 2006; 27:2170-2176.
44. Fraser A, Harris R, Sattar N, Ebrahim S, Smith GD, Lawlor DA. Gammaglutamyltransferase is associated with incident vascular events independently of alcohol intake: analysis of the British Womens Heart and Health Study and Meta-Analysis. Arterioscler Thromb Vasc Biol 2007; 27:2729-2735.
45. Schindhelm RK, Dekker JM, Nijpels G, Bouter LM, Stehouwer CD, Heine RJ, Diamant M. Alanine aminotransferase predicts coronary heart disease events: a 10-year follow-up of the Hoorn Study. Atherosclerosis 2007; 191:391-396.
46. Yun KE, Shin CY, Yoon YS, Park HS. Elevated alanine aminotransferase levels predict mortality from cardiovascular disease and diabetes in Koreans. Atherosclerosis 2009; 205:533-537.
47. Ioannou GN, Weiss NS, Boyko EJ, Mozaffarian D, Lee SP. Elevated serum alanine aminotransferase activity and calculated risk of coronary heart disease in the United States. Hepatology 2006; 43:1145-1151.
48. Hamaguchi M, Kojima T, Takeda N, Nagata C, Takeda J, Sarui H, et al. Nonalcoholic fatty liver disease is a novel predictor of cardiovascular disease. World J Gastroenterol 2007; 13:1579-1584.
49. Targher G, Bertolini L, Poli F, Rodella S, Scala L, Tessari R, et al. Nonalcoholic fatty liver disease and risk of future cardiovascular events among type 2 diabetic patients. Diabetes 2005; 54:3541-3546.
50. Targher G, Bertolini L, Rodella S, Tessari R, Zenari L, Lippi G, Arcaro G. Nonalcoholic fatty liver disease is independently associated with an increased incidence of cardiovascular events in type 2 diabetic patients. Diabetes Care 2007; 30:2119-2121.
51. Haring R, Wallaschofski H, Nauck M, Dörr M, Baumeister SE, Völzke H. Ultrasonographic hepatic steatosis increases prediction of mortality risk from elevated serum gamma-glutamyl transpeptidase levels. Hepatology 2009; 50:1403-1411.
52. Treeprasertsuk S, Leverage S, Adams LA, Lindor KD, St Sauver J, Angulo P. The Framingham risk score and heart disease in nonalcoholic fatty liver disease. Liver Int 2012; 32:945-950.
53. Chan WK, Tan AT, Vethakkan SR, Tah PC, Vijayananthan A, Goh KL. Ultrasonography-diagnosed non-Alcoholic fatty liver disease is not associated with prevalent ischemic heart disease among diabetics in a multiracial Asian hospital clinic population. Clin Res Hepatol Gastroenterol 2014; 38:284-291.
54. Lazo M, Hernaez R, Bonekamp S, Kamel IR, Brancati FL, Guallar E, Clark JM. Non-Alcoholic fatty liver disease and mortality among US adults: prospective cohort study. BMJ 2011; 343:d6891.
55. Stepanova M, Younossi ZM. Independent association between nonalcoholic fatty liver disease and cardiovascular disease in the US population. Clin Gastroenterol Hepatol 2012; 10:646-650.
56. Kim D, Kim WR, Kim HJ, Therneau TM. Association between noninvasive fibrosis markers and mortality among adults with nonalcoholic fatty liver disease in the United States. Hepatology 2013; 57:1357-1365.
57. Schwimmer JB, Deutsch R, Kahen T, Lavine JE, Stanley C, Behling C. Prevalence of fatty liver in children and adolescents. Pediatrics 2006; 118:1388-1393.
58. Zhou YJ, Li YY, Nie YQ, Ma JX, Lu LG, Shi SL, et al. Prevalence of fatty liver disease and its risk factors in the population of South China. World J Gastroenterol 2007; 13:6419-6424.
59. Chan DF, Li AM, Chu WC, Chan MH, Wong EM, Liu EK, et al. Hepatic steatosis in obese Chinese children. Int J Obes Relat Metab Disord 2004; 28:1257-1263.
60. Guzzaloni G, Grugni G, Minocci A, Moro D, Morabito F. Liver steatosis in juvenile obesity: correlations with lipid profile, hepatic biochemical parameters and glycemic and insulinemic responses to an oral glucose tolerance test. Int J Obes Relat Metab Disord 2000; 24:772-776.
61. Shiotani A, Motoyama M, Matsuda T, Miyanishi T. Brachial-Ankle pulse wave velocity in Japanese university students. Intern Med 2005; 44:696-701.
62. Pacifico L, Cantisani V, Ricci P, Osborn JF, Schiavo E, Anania C, et al. Nonalcoholic fatty liver disease and carotid atherosclerosis in children. Pediatr Res 2008; 63:423-427.
63. Alp H, Karaarslan S, Selver Eklioʇlu B, Atabek ME, Altin H, Baysal T. Association between nonalcoholic fatty liver disease and cardiovascular risk in obese children and adolescents. Can J Cardiol 2013; 29:1118-1125.
64. Göke S, Atbinici Z, Aycan Z, Cinar HG, Zorlu P. The relationship between pediatric nonalcoholic fatty liver disease and cardiovascular risk factors and increased risk of atherosclerosis in obese children. Pediatr Cardiol 2013; 34:308-315.
65. Schwimmer JB, Pardee PE, Lavine JE, Blumkin AK, Cook S. Cardiovascular risk factors and the metabolic syndrome in pediatric nonalcoholic fatty liver disease. Circulation 2008; 118:277-283.
66. Wong VW, Hui AY, Tsang SW, Chan JL, Tse AM, Chan KF, et al. Metabolic and adipokine profile of Chinese patients with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 2006; 4:1154-1161.
67. Hamaguchi M, Kojima T, Takeda N, Nakagawa T, Taniguchi H, Fujii K, et al. The metabolic syndrome as a predictor of nonalcoholic fatty liver disease. Ann Intern Med 2005; 143:722-728.
68. Kotronen A, Juurinen L, Tiikkainen M, Vehkavaara S, Yki-Järvinen H. Increased liver fat, impaired insulin clearance, and hepatic and adipose tissue insulin resistance in type 2 diabetes. Gastroenterology 2008; 135:122-130.
69. Fabbrini E, Magkos F, Mohammed BS, Pietka T, Abumrad NA, Patterson BW, et al. Intrahepatic fat, not visceral fat, is linked with metabolic complications of obesity. Proc Natl Acad Sci U S A 2009; 106:15430-15435.
70. Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest 2006; 116:1793-1801.
71. Eriksson P, Nilsson L, Karpe F, Hamsten A. Very-low-density lipoprotein response element in the promoter region of the human plasminogen activator inhibitor-1 gene implicated in the impaired fibrinolysis of hypertriglyceridemia. Arterioscler Thromb Vasc Biol 1998; 18:20-26.
72. Hamsten A, Wiman B, de Faire U, Blombäck M. Increased plasma levels of a rapid inhibitor of tissue plasminogen activator in young survivors of myocardial infarction. N Engl J Med 1985; 313:1557-1563.
73. Lavie CJ, Milani RV, Verma A, O'Keefe JH. C-reactive protein and cardiovascular diseases-is it ready for primetime? Am J Med Sci 2009; 338:486-492.
74. Dowman JK, Tomlinson JW, Newsome PN. Pathogenesis of non-Alcoholic fatty liver disease. QJM 2010; 103:71-83.
75. Tilg H, Moschen AR. Insulin resistance, inflammation, and non-Alcoholic fatty liver disease. Trends Endocrinol Metab 2008; 19:371-379.
76. Kiechl S, Lorenz E, Reindl M, Wiedermann CJ, Oberhollenzer F, Bonora E, et al. Toll-like receptor 4 polymorphisms and atherogenesis. N Engl J Med 2002; 347:185-192.
77. Stefan N, Kantartzis K, Häring HU. Causes and metabolic consequences of fatty liver. Endocr Rev 2008; 29:939-960.
78. McCullough AJ. The clinical features, diagnosis and natural history of nonalcoholic fatty liver disease. Clin Liver Dis 2004; 8:521-533.
79. Moller DE, Kaufman KD. Metabolic syndrome: a clinical and molecular perspective. Annu Rev Med 2005; 56:45-62.
80. Gaziano JM, Hennekens CH, ODonnell CJ, Breslow JL, Buring JE. Fasting triglycerides, high-density lipoprotein, and risk of myocardial infarction. Circulation 1997; 96:2520-2525.
81. Ratziu V, Bellentani S, Cortez-Pinto H, Day C, Marchesini G. A position statement on NAFLD/NASH based on the EASL 2009 special conference. J Hepatol 2010; 53:372-384.
82. Loria P, Adinolfi LE, Bellentani S, Bugianesi E, Grieco A, Fargion S, et al. NAFLD Expert Committee of the Associazione Italiana per lo studio del Fegato. Practice guidelines for the diagnosis and management of nonalcoholic fatty liver disease. A decalogue from the Italian Association for the Study of the Liver (AISF) Expert Committee. Dig Liver Dis 2010; 42:272-282.
83. Nascimbeni F, Pais R, Bellentani S, Day CP, Ratziu V, Loria P, Lonardo A. From NAFLD in clinical practice to answers from guidelines. J Hepatol 2013; 59:859-871.
84. Bhupathiraju SN, Tucker KL. Coronary heart disease prevention: nutrients, foods, and dietary patterns. Clin Chim Acta 2011; 412:1493-1514.
85. Kardassis D, Bech-Hanssen O, Schönander M, Sjöström L, Karason K. The influence of body composition, fat distribution, and sustained weight loss on left ventricular mass and geometry in obesity. Obesity (Silver Spring) 2012; 20:605-611.
86. Frohlich J, Al-Sarraf A. Cardiovascular risk and atherosclerosis prevention. Cardiovasc Pathol 2013; 22:16-18.
87. Mathur N, Pedersen BK. Exercise as a mean to control low-grade systemic inflammation. Mediators Inflamm 2008; 2008:109502.