Insulin resistance in nonalcoholic fatty liver disease

Current Pharmaceutical Design

Volumn 16, Issue 17, 2010, Pages 1941-1951

  Bugianesi, E ^a   Moscatiello, S ^b   Ciaravella, M F ^b   Marchesini, G ^b  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Cardiovascular disease; Insulin; Insulin resistance; Metabolic syndrome; Nonalcoholic fatty liver disease

Indexed keywords

BLOOD CLOTTING FACTOR; C REACTIVE PROTEIN; FATTY ACID; GLUCOSE; INSULIN; METFORMIN; ROSIGLITAZONE; THIAZOLIDINE DERIVATIVE; VERY LOW DENSITY LIPOPROTEIN;

ADIPOSE TISSUE; APOPTOSIS; ARTICLE; CARDIOVASCULAR RISK; CLINICAL RESEARCH; DISEASE ASSOCIATION; DISEASE COURSE; FAT INTAKE; FATTY ACID OXIDATION; FATTY LIVER; FIBROGENESIS; GENE INTERACTION; HUMAN; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; INTESTINE FLORA; LIPID PEROXIDATION; LIPID STORAGE; LIPOGENESIS; LIVER CELL; LIVER FATTY DEGENERATION; LIVER FIBROSIS; METABOLIC SYNDROME X; NONALCOHOLIC FATTY LIVER; NONHUMAN; OBESITY; OXIDATIVE STRESS; PRIORITY JOURNAL; ANIMAL; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASES; COMPLICATION; DIABETES MELLITUS, TYPE 2; PATHOPHYSIOLOGY; RISK FACTOR;

ANIMALS; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASES; DIABETES MELLITUS, TYPE 2; FATTY LIVER; HUMANS; INSULIN RESISTANCE; METABOLIC SYNDROME X; RISK FACTORS;

EID: 77953529312     PISSN: 13816128     EISSN: None     Source Type: Journal    
DOI: 10.2174/138161210791208875     Document Type: Article

References (121)

1. Angulo P. Nonalcoholic fatty liver disease. N Engl J Med 2002; 346: 1221-31.
2. Marchesini G, Bugianesi E, Forlani G, Cerrelli F, Lenzi M, Manini R, et al. Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology 2003; 37: 917-23.
3. Expert Panel on Detection Evaluation and Treatment of High Blood Cholesterol in Adults. Executive summary of the third report of the National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III). JAMA 2001; 285: 2486-97.
4. Alberti KG, Zimmet P, Shaw J. The metabolic syndrome-a new worldwide definition. Lancet 2005; 366: 1059-62.
5. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, et al. 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 2009; 120: 1640-5.
6. Kotronen A, Westerbacka J, Bergholm R, Pietilainen KH, YkiJarvinen H. Liver fat in the metabolic syndrome. J Clin Endocrinol Metab 2007; 92: 3490-7.
7. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from plasma fasting glucose and insulin concentrations in man. Diabetologia 1985; 28: 412-9.
8. Katz A, Nambi SS, Mather K, Baron AD, Follmann DA, Sullivan G, et al. Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. J Clin Endocrinol Metab 2000; 85: 2402-10.
9. DeFronzo RA, Tobin JD, Andres R. Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am J Physiol 1979; 237: E214-23.
10. Mari A, Pacini G, Murphy E, Ludvik B, Nolan JJ. A model-based method for assessing insulin sensitivity from the oral glucose tolerance test. Diabetes Care 2001; 24: 539-48.
11. Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care 1999; 22: 1462-70.
12. Angelico F, Del Ben M, Conti R, Francioso S, Feole K, Fiorello S, et al. Insulin resistance, the metabolic syndrome, and nonalcoholic fatty liver disease. J Clin Endocrinol Metab 2005; 90: 1578-82.
13. 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: 722-8.
14. Oh SY, Cho YK, Kang MS, Yoo TW, Park JH, Kim HJ, et al. The association between increased alanine aminotransferase activity and metabolic factors in nonalcoholic fatty liver disease. Metabolism 2006; 55: 1604-9.
15. Liangpunsakul S, Chalasani N. Unexplained elevations in alanine aminotransferase in individuals with the metabolic syndrome: results from the third National Health and Nutrition Survey (NHANES III). Am J Med Sci 2005; 329: 111-6.
16. Gholam PM, Flancbaum L, Machan JT, Charney DA, Kotler DP. Nonalcoholic fatty liver disease in severely obese subjects. Am J Gastroenterol 2007; 102: 399-408.
17. Fracanzani AL, Valenti L, Bugianesi E, Andreoletti M, Colli A, Vanni E, et al. Risk of severe liver disease in NAFLD with normal aminotransferase levels: A role for insulin resistance and diabetes. Hepatology 2008; 48: 792-8.
18. Wellen KE, Hotamisligil GS. Inflammation, stress, and diabetes. J Clin Invest 2005; 115: 1111-9.
19. Palmieri VO, Grattagliano I, Portincasa P, Palasciano G. Systemic oxidative alterations are associated with visceral adiposity and liver steatosis in patients with metabolic syndrome. J Nutr 2006; 136: 3022-6.
20. Ryan MC, Wilson AM, Slavin J, Best JD, Jenkins AJ, Desmond PV. Associations between liver histology and severity of the metabolic syndrome in subjects with nonalcoholic fatty liver disease. Diabetes Care 2005; 28: 1222-4.
21. Rocha R, Cotrim HP, Carvalho FM, Siqueira AC, Braga H, Freitas LA. Body mass index and waist circumference in non-alcoholic fatty liver disease. J Hum Nutr Diet 2005; 18: 365-70.
22. Fraser A, Harris R, Sattar N, Ebrahim S, Davey Smith G, Lawlor DA. Alanine aminotransferase, gamma-glutamyltransferase, and incident diabetes: the British Women's Heart and Health Study and meta-analysis. Diabetes Care 2009; 32: 741-50.
23. Fraser A, Harris R, Sattar N, Ebrahim S, Smith GD, Lawlor DA. Gamma-glutamyltransferase is associated with incident vascular events independently of alcohol intake: analysis of the British Women's Heart and Health Study and Meta-Analysis. Arterioscl Thromb Vasc Biol 2007; 27: 2729-35.
24. Schindhelm RK, Dekker JM, Nijpels G, Bouter LM, Stehouwer CD, Heine RJ, et al. Alanine aminotransferase predicts coronary heart disease events: A 10-year follow-up of the Hoorn Study. Atherosclerosis 2007; 191: 391-6.
25. Lin YC, Lo HM, Chen JD. Sonographic fatty liver, overweight and ischemic heart disease. World J Gastroenterol 2005; 11: 4838-42.
26. 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: 1848-53.
27. 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: 1579-84.
28. Jepsen P, Vilstrup H, Mellemkjaer L, Thulstrup AM, Olsen JH, Baron J, et al. Prognosis of patients with a diagnosis of fatty liver a registry-based cohort study. Hepatogastroenterology 2003; 50: 2101-4.
29. Targher G, Marra F, Marchesini G. Increased risk of cardiovascular disease in non-alcoholic fatty liver disease: causal effect or epiphenomenon? Diabetologia 2008; 51: 1947-53.
30. 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: 72-8.
31. 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: 473-80.
32. Targher G, Bertolini L, Rodella S, Tessari R, Zenari L, Lippi G, et al. Nonalcoholic fatty liver disease is independently associated with an increased incidence of cardiovascular events in type 2 diabetic patients. Diabetes Care 2007; 30: 2119-21.
33. Targher G, Bertolini L, Rodella S, Zoppini G, Lippi G, Day C, et al. Non-alcoholic fatty liver disease is independently associated with an increased prevalence of chronic kidney disease and proliferative/laser-treated retinopathy in type 2 diabetic patients. Diabetologia 2008; 51: 444-50.
34. Arner P. Not all fat is alike. Lancet 1998; 351: 1301-2.
35. Bergman RN, Kim SP, Hsu IR, Catalano KJ, Chiu JD, Kabir M, et al. Abdominal obesity: role in the pathophysiology of metabolic disease and cardiovascular risk. Am J Med 2007; 120: S3-8; discussion S29-32.
36. Kelley DE, McKolanis TM, Hegazi RA, Kuller LH, Kalhan SC. Fatty liver in type 2 diabetes mellitus: relation to regional adiposity, fatty acids, and insulin resistance. Am J Physiol Endocrinol Metab 2003; 285: E906-16.
37. Nguyen-Duy TB, Nichaman MZ, Church TS, Blair SN, Ross R. Visceral fat and liver fat are independent predictors of metabolic risk factors in men. Am J Physiol Endocrinol Metab 2003; 284: E1065-71.
38. Miyazaki Y, Glass L, Triplitt C, Wajcberg E, Mandarino LJ, DeFronzo RA. Abdominal fat distribution and peripheral and hepatic insulin resistance in type 2 diabetes mellitus. Am J Physiol Endocrinol Metab 2002; 283: E1135-43.
39. Seppala-Lindroos A, Vehkavaara S, Hakkinen AM, Goto T, Westerbacka J, Sovijarvi A, et al. Fat accumulation in the liver is associated with defects in insulin suppression of glucose production and serum free fatty acids independent of obesity in normal men. J Clin Endocrinol Metab 2002; 87: 3023-8.
40. Stefan N, Kantartzis K, Machann J, Schick F, Thamer C, Rittig K, et al. Identification and characterization of metabolically benign obesity in humans. Arch Intern Med 2008; 168: 1609-16.
41. Saberi M, Woods NB, de Luca C, Schenk S, Lu JC, Bandyopadhyay G, et al. Hematopoietic cell-specific deletion of toll-like receptor 4 ameliorates hepatic and adipose tissue insulin resistance in high-fat-fed mice. Cell Metab 2009; 10: 419-29.
42. Tabata M, Kadomatsu T, Fukuhara S, Miyata K, Ito Y, Endo M, et al. Angiopoietin-like protein 2 promotes chronic adipose tissue inflammation and obesity-related systemic insulin resistance. Cell Metab 2009; 10: 178-88.
43. Kammoun HL, Chabanon H, Hainault I, Luquet S, Magnan C, Koike T, et al. GRP78 expression inhibits insulin and ER stressinduced SREBP-1c activation and reduces hepatic steatosis in mice. J Clin Invest 2009; 119: 1201-15.
44. Adiels M, Taskinen MR, Packard C, Caslake MJ, Soro-Paavonen A, Westerbacka J, et al. Overproduction of large VLDL particles is driven by increased liver fat content in man. Diabetologia 2006; 49: 755-65.
45. Cali AM, Zern TL, Taksali SE, de Oliveira AM, Dufour S, Otvos JD, et al. Intrahepatic fat accumulation and alterations in lipoprotein composition in obese adolescents: a perfect proatherogenic state. Diabetes Care 2007; 30: 3093-8.
46. Donnelly KL, Smith CI, Schwarzenberg SJ, Jessurun J, Boldt MD, Parks EJ. Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease. J Clin Invest 2005; 115: 1343-51.
47. Musso G, Gambino R, De Michieli F, Cassader M, Rizzetto M, Durazzo M, et al. Dietary habits and their relations to insulin resistance and postprandial lipemia in nonalcoholic steatohepatitis. Hepatology 2003; 37: 909-16.
48. Musso G, Gambino R, De Michieli F, Durazzo M, Pagano G, Cassader M. Adiponectin gene polymorphisms modulate acute adiponectin response to dietary fat: possible pathogenetic role in NAFLD. Hepatology 2008; 46: 1167-77.
49. Toledo FG, Sniderman AD, Kelley DE. Influence of hepatic steatosis (fatty liver) on severity and composition of dyslipidemia in type 2 diabetes. Diabetes Care 2006; 29: 1845-50.
50. Pepys MB, Hirschfield GM. C-reactive protein: a critical update. J Clin Invest 2003; 111: 1805-12.
51. Kerner A, Avizohar O, Sella R, Bartha P, Zinder O, Markiewicz W, et al. Association between elevated liver enzymes and Creactive protein: possible hepatic contribution to systemic inflammation in the metabolic syndrome. Arterioscl Thromb Vasc Biol 2005; 25: 193-7.
52. Park SH, Kim BI, Yun JW, Kim JW, Park DI, Cho YK, et al. Insulin resistance and C-reactive protein as independent risk factors for non-alcoholic fatty liver disease in non-obese Asian men. J Gastroenterol Hepatol 2004; 19: 694-8.
53. Targher G, Arcaro G. Non-alcoholic fatty liver disease and increased risk of cardiovascular disease. Atherosclerosis 2007; 191: 235-40.
54. Yoneda M, Mawatari H, Fujita K, Iida H, Yonemitsu K, Kato S, et al. High-sensitivity C-reactive protein is an independent clinical feature of nonalcoholic steatohepatitis (NASH) and also of the severity of fibrosis in NASH. J Gastroenterol 2007; 42: 573-82.
55. Lautamaki R, Borra R, Iozzo P, Komu M, Lehtimaki T, Salmi M, et al. Liver steatosis coexists with myocardial insulin resistance and coronary dysfunction in patients with type 2 diabetes. Am J Physiol Endocrinol Metab 2006; 291: E282-90.
56. Perseghin G, Lattuada G, De Cobelli F, Esposito A, Belloni E, Ntali G, et al. Increased mediastinal fat and impaired left ventricular energy metabolism in young men with newly found fatty liver. Hepatology 2008; 47: 51-8.
57. Bugianesi E. Nonalcoholic fatty liver disease (NAFLD) and cardiac lipotoxicity: another piece of the puzzle. Hepatology 2008; 47: 2-4.
58. Goland S, Shimoni S, Zornitzki T, Knobler H, Azoulai O, Lutaty G, et al. Cardiac abnormalities as a new manifestation of nonalcoholic fatty liver disease: echocardiographic and tissue Doppler imaging assessment. J Clin Gastroenterol 2006; 40: 94955.
59. Bugianesi E, McCullough AJ, Marchesini G. Insulin resistance: a metabolic pathway to chronic liver disease. Hepatology 2005; 42: 987-1000.
60. Choudhury J, Sanyal AJ. Insulin resistance and the pathogenesis of nonalcoholic fatty liver disease. Clin Liver Dis 2004; 8: 575-94, ix.
61. Bugianesi E, Gastaldelli A, Vanni E, Gambino R, Cassader M, Baldi S, et al. Insulin resistance in non-diabetic patients with nonalcoholic fatty liver disease: sites and mechanisms. Diabetologia 2005; 48: 634-42.
62. Marchesini G, Brizi M, Bianchi G, Tomassetti S, Bugianesi E, Lenzi M, et al. Nonalcoholic fatty liver disease: a feature of the metabolic syndrome. Diabetes 2001; 50: 1844-50.
63. Fryer LG, Parbu-Patel A, Carling D. The anti-diabetic drugs rosiglitazone and metformin stimulate AMP-activated protein kinase through distinct signaling pathways. J Biol Chem 2002; 277: 25226-32.
64. Tiikkainen M, Hakkinen AM, Korsheninnikova E, Nyman T, Makimattila S, Yki-Jarvinen H. Effects of rosiglitazone and metformin on liver fat content, hepatic insulin resistance, insulin clearance, and gene expression in adipose tissue in patients with type 2 diabetes. Diabetes 2004; 53: 2169-76.
65. Kintscher U, Law RE. PPARgamma-mediated insulin sensitization: the importance of fat versus muscle. Am J Physiol Endocrinol Metab 2005; 288: E287-91.
66. Hwang JH, Stein DT, Barzilai N, Cui MH, Tonelli J, Kishore P, et al. Increased intrahepatic triglyceride is associated with peripheral insulin resistance: in vivo MR imaging and spectroscopy studies. Am J Physiol Endocrinol Metab 2007; 293: E1663-9.
67. Bugianesi E, Marchesini G, Gentilcore E, Cua IH, Vanni E, Rizzetto M, et al. Fibrosis in genotype 3 chronic hepatitis C and nonalcoholic fatty liver disease: Role of insulin resistance and hepatic steatosis. Hepatology 2006; 44: 1648-55.
68. Paradis V, Perlemuter G, Bonvoust F, Dargere D, Parfait B, Vidaud M, et al. High glucose and hyperinsulinemia stimulate connective tissue growth factor expression: a potential mechanism involved in progression to fibrosis in nonalcoholic steatohepatitis. Hepatology 2001; 34: 738-44.
69. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science (New York, NY) 2004; 306: 457-61.
70. Svegliati-Baroni G, Ridolfi F, Di Sario A, Casini A, Marucci L, Gaggiotti G, et al. Insulin and insulin-like growth factor-1 stimulate proliferation and type I collagen accumulation by human hepatic stellate cells: differential effects on signal transduction pathways. Hepatology 1999; 29: 1743-51.
71. Day CP, James OFW. Steatohepatitis: a tale of two hits. Gastroenterology 1998; 114: 842-5.
72. Day CP. From fat to inflammation. Gastroenterology 2006; 130: 207-10.
73. Bugianesi E, Manzini P, D'Antico S, Vanni E, Longo F, Leone N, et al. Relative contribution of iron burden, HFE mutations and insulin resistance to fibrosis in nonalcoholic fatty liver. Hepatology 2004; 39: 179-87.
74. Fassio E, Alvarez E, Dominguez N, Landeira G, Longo C. Natural history of nonalcoholic steatohepatitis: a longitudinal study of repeat liver biopsies. Hepatology 2004; 40: 820-6.
75. Biddinger SB, Kahn CR. From mice to men: insights into the insulin resistance syndromes. Annu Rev Physiol 2006; 68: 123-58.
76. Considine RV, Nyce MR, Allen LE, Morales LM, Triester S, Serrano J, et al. Protein kinase C is increased in the liver of humans and rats with non-insulin-dependent diabetes mellitus: an alteration not due to hyperglycemia. J Clin Invest 1995; 95: 2938-44.
77. Taniguchi CM, Ueki K, Kahn R. Complementary roles of IRS-1 and IRS-2 in the hepatic regulation of metabolism. J Clin Invest 2005; 115: 718-27.
78. Brown MS, Goldstein JL. Selective versus total insulin resistance: a pathogenic paradox. Cell Metabol 2008; 7: 95-6.
79. Yamaguchi K, Yang L, McCall S, Huang J, Yu XX, Pandey SK, et al. Inhibiting triglyceride synthesis improves hepatic steatosis but exacerbates liver damage and fibrosis in obese mice with nonalcoholic steatohepatitis. Hepatology 2007; 45: 1366-74.
80. DeFronzo RA. Dysfunctional fat cells, lipotoxicity and type 2 diabetes. Int J Clin Pract Suppl 2004; 143: 9-21.
81. Malhi H, Gores GJ. Molecular mechanisms of lipotoxicity in nonalcoholic fatty liver disease. Semin Liver Dis 2008; 28: 360-9.
82. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 2004; 114: 1752-61.
83. Chalasani N, Deeg MA, Crabb DW. Systemic levels of lipid peroxidation and its metabolic and dietary correlates in patients with nonalcoholic steatohepatitis. Am J Gastroenterol 2004; 99: 1497-502.
84. Seki S, Kitada T, Yamada T, Sakaguchi H, Nakatani K, Wakasa K. In situ detection of lipid peroxidation and oxidative DNA damage in non-alcoholic fatty liver diseases. J Hepatol 2002; 37: 56-62.
85. Sanyal AJ, Campbell-Sargent C, Mirshahi F, Rizzo WB, Contos MJ, Sterling RK, et al. Nonalcoholic steatohepatitis: association of insulin resistance and mitochondrial abnormalities. Gastroenterology 2001; 120: 1183-92.
86. Perez-Carreras M, Del Hoyo P, Martin MA, Rubio JC, Martin A, Castellano G, et al. Defective hepatic mitochondrial respiratory chain in patients with nonalcoholic steatohepatitis. Hepatology 2003; 38: 999-1007.
87. Hannun YA, Obeid LM. The ceramide-centric universe of lipidmediated cell regulation: stress encounters of the lipid kind. J Biol Chem 2002; 277: 25847-50.
88. Mari M, Fernandez-Checa JC. Sphingolipid signalling and liver diseases. Liver Int 2007; 27: 440-50.
89. Li Z, Berk M, McIntyre TM, Gores GJ, Feldstein AE. The lysosomal-mitochondrial axis in free fatty acid-induced hepatic lipotoxicity. Hepatology 2008; 47: 1495-503.
90. Feldstein AE, Werneburg NW, Canbay A, Guicciardi ME, Bronk SF, Rydzewski R, et al. Free fatty acids promote hepatic lipotoxicity by stimulating TNF-alpha expression via a lysosomal pathway. Hepatology 2004; 40: 185-94.
91. Wieckowska A, McCullough AJ, Feldstein AE. Noninvasive diagnosis and monitoring of nonalcoholic steatohepatitis: Present and future. Hepatology 2007; 46: 582-9.
92. Hotamisligil GS, Erbay E. Nutrient sensing and inflammation in metabolic diseases. Nat Rev Immunol 2008; 8: 923-34.
93. Wolowczuk I, Verwaerde C, Viltart O, Delanoye A, Delacre M, Pot B, et al. Feeding our immune system: impact on metabolism. Clin Dev Immunol 2008; 2008: 639803.
94. Arkan MC, Hevener AL, Greten FR, Maeda S, Li ZW, Long JM, et al. IKK-beta links inflammation to obesity-induced insulin resistance. Nat Med 2005; 11: 191-8.
95. DiAngelo JR, Bland ML, Bambina S, Cherry S, Birnbaum MJ. The immune response attenuates growth and nutrient storage in Drosophila by reducing insulin signaling. Proc Natl Acad Sci USA 2009; [Oct 27 Epub ahead of print].
96. Rajala MW, Scherer PE. Minireview: the adipocyte--at the crossroads of energy homeostasis, inflammation, and atherosclerosis. Endocrinology 2003; 144: 3765-73.
97. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 2007; 117: 175-84.
98. Solga SF, Diehl AM. Non-alcoholic fatty liver disease: lumen-liver interactions and possible role for probiotics. J Hepatol 2003; 38: 681-7.
99. Miele L, Valenza V, La Torre G, Montalto M, Cammarota G, Ricci R, et al. Increased intestinal permeability and tight junction alterations in nonalcoholic fatty liver disease. Hepatology 2009; 49: 1877-87.
100. DiBaise JK, Zhang H, Crowell MD, Krajmalnik-Brown R, Decker GA, Rittmann BE. Gut microbiota and its possible relationship with obesity. Mayo Clin Proc 2008; 83: 460-9.
101. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007; 56: 1761-72.
102. Bergheim I, Weber S, Vos M, Kramer S, Volynets V, Kaserouni S, et al. Antibiotics protect against fructose-induced hepatic lipid accumulation in mice: role of endotoxin. J Hepatol 2008; 48: 98392.
103. Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS. TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest 2006; 116: 3015-25.
104. Spruss A, Kanuri G, Wagnerberger S, Haub S, Bischoff SC, Bergheim I. Toll-like receptor 4 is involved in the development of fructose-induced hepatic steatosis in mice. Hepatology 2009; 50: 1094-104.
105. Fiorentino L, Vivanti A, Cavalera M, Marzano V, Ronci M, Fabrizi M, et al. Increased tumor necrosis factor alpha-converting enzyme activity induces insulin resistance and hepatosteatosis in mice. Hepatology 2010; 51: 103-10.
106. Ota T, Takamura T, Kurita S, Matsuzawa N, Kita Y, Uno M, et al. Insulin resistance accelerates a dietary rat model of nonalcoholic steatohepatitis. Gastroenterology 2007; 132: 282-93.
107. Gabbay E, Avraham Y, Ilan Y, Israeli E, Berry EM. Endocannabinoids and liver disease-review. Liver Int 2005; 25: 921-6.
108. Teixeira-Clerc F, Julien B, Grenard P, Tran Van Nhieu J, Deveaux V, Li L, et al. CB1 cannabinoid receptor antagonism: a new strategy for the treatment of liver fibrosis. Nat Med 2006; 12: 671-6.
109. Struben VM, Hespenheide EE, Caldwell SH. Nonalcoholic steatohepatitis and cryptogenic cirrhosis within kindreds. Am J Med 2000; 108: 9-13.
110. Willner IR, Waters B, Patil SR, Reuben A, Morelli J, Riely CA. Ninety patients with nonalcoholic steatohepatitis: insulin resistance, familial tendency, and severity of disease. Am J Gastroenterol 2001; 96: 2957-61.
111. Bathum L, Petersen HC, Rosholm JU, Hyltoft Petersen P, Vaupel J, Christensen K. Evidence for a substantial genetic influence on biochemical liver function tests: results from a population-based Danish twin study. Clin Chem 2001; 47: 81-7.
112. Schwimmer JB, Celedon MA, Lavine JE, Salem R, Campbell N, Schork NJ, et al. Heritability of nonalcoholic fatty liver disease. Gastroenterology 2009; 136: 1585-92.
113. Browning JD, Kumar KS, Saboorian MH, Thiele DL. Ethnic differences in the prevalence of cryptogenic cirrhosis. Am J Gastroenterol 2004; 99: 292-8.
114. Musso G, Gambino R, De Michieli F, Durazzo M, Pagano G, Cassader M. Adiponectin gene polymorphisms modulate acute adiponectin response to dietary fat: Possible pathogenetic role in NASH. Hepatology 2008; 47: 1167-77.
115. Namikawa C, Shu-Ping Z, Vyselaar JR, Nozaki Y, Nemoto Y, Ono M, et al. Polymorphisms of microsomal triglyceride transfer protein gene and manganese superoxide dismutase gene in nonalcoholic steatohepatitis. J Hepatol 2004; 40: 781-6.
116. Miele L, Beale G, Patman G, Nobili V, Leathart J, Grieco A, et al. The Kruppel-like factor 6 genotype is associated with fibrosis in nonalcoholic fatty liver disease. Gastroenterology 2008; 135: 282-91 e1.
117. Kechagias S, Ernersson A, Dahlqvist O, Lundberg P, Lindstrom T, Nystrom FH. Fast-food-based hyper-alimentation can induce rapid and profound elevation of serum alanine aminotransferase in healthy subjects. Gut 2008; 57: 649-54.
118. Petersen KF, Dufour S, Befroy D, Lehrke M, Hendler RE, Shulman GI. Reversal of nonalcoholic hepatic steatosis, hepatic insulin resistance, and hyperglycemia by moderate weight reduction in patients with type 2 diabetes. Diabetes 2005; 54: 603-8.
119. Valtuena S, Pellegrini N, Ardigo D, Del Rio D, Numeroso F, Scazzina F, et al. Dietary glycemic index and liver steatosis. Am J Clin Nutr 2006; 84: 136-42; quiz 268-9.
120. Zelber-Sagi S, Nitzan-Kaluski D, Goldsmith R, Webb M, Blendis L, Halpern Z, et al. Long term nutritional intake and the risk for non-alcoholic fatty liver disease (NAFLD): a population based study. J Hepatol 2007; 47: 711-7.
121. Taylor CG, Zahradka P. Dietary conjugated linoleic acid and insulin sensitivity and resistance in rodent models. Am J Clin Nutr 2004; 79: 1164S-8S.