Nonalcoholic fatty liver disease markers are associated with insulin resistance in type 1 diabetes

Digestive Diseases and Sciences

Volumn 56, Issue 12, 2011, Pages 3655-3663

  Bulum, Tomislav ^a   Kolarić, Branko ^b,c   Duvnjak, Lea ^a,d   Duvnjak, Marko ^d,e  

^a University of Zagreb   (Croatia)

^b UNIVERSITY OF RIJEKA   (Croatia)

^c Zagreb Institute of Public Health   (Croatia)

^d UNIVERSITY OF ZAGREB   (Croatia)

^e SESTRE MILOSRDNICE UNIVERSITY HOSPITAL   (Croatia)

Author keywords

Estimated glucose disposal rate; Insulin resistance; Liver enzymes; Nonalcoholic fatty liver disease; Type 1 diabetes

Indexed keywords

ALANINE AMINOTRANSFERASE; ALKALINE PHOSPHATASE; ASPARTATE AMINOTRANSFERASE; BILIRUBIN; FERRITIN; GAMMA GLUTAMYLTRANSFERASE; HEMOGLOBIN A1C; HIGH DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; TRIACYLGLYCEROL; VERY LOW DENSITY LIPOPROTEIN; BIOLOGICAL MARKER;

ADULT; AGE; AGED; ARTICLE; BODY MASS; CHOLESTEROL BLOOD LEVEL; DIABETIC PATIENT; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE DURATION; DISEASE MARKER; FEMALE; GENDER; HUMAN; HYPERTENSION; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RESISTANCE; INSULIN SENSITIVITY; MAJOR CLINICAL STUDY; MALE; METABOLIC PARAMETERS; NONALCOHOLIC FATTY LIVER; PRIORITY JOURNAL; WAIST HIP RATIO; ADOLESCENT; BLOOD; COMPARATIVE STUDY; FATTY LIVER; FOLLOW UP; GLUCOSE BLOOD LEVEL; METABOLISM; MIDDLE AGED; PROGNOSIS;

ADOLESCENT; ADULT; AGED; ALANINE TRANSAMINASE; ALKALINE PHOSPHATASE; ASPARTATE AMINOTRANSFERASES; BIOLOGICAL MARKERS; BLOOD GLUCOSE; DIABETES MELLITUS, TYPE 1; DISEASE PROGRESSION; FATTY LIVER; FEMALE; FOLLOW-UP STUDIES; GAMMA-GLUTAMYLTRANSFERASE; HUMANS; INSULIN RESISTANCE; MALE; MIDDLE AGED; PROGNOSIS; YOUNG ADULT;

EID: 84856257461     PISSN: 01632116     EISSN: 15732568     Source Type: Journal    
DOI: 10.1007/s10620-011-1807-7     Document Type: Article

References (50)

1. DeFronzo RA, Hendler R, Simonson D. Insulin resistance is a prominent feature of insulin-dependent diabetes. Diabetes. 1982; 31:795-801. (Pubitemid 12062869)
2. Martin FIR, Hopper JL. The relationship of acute insulin sensitivity to the progression of vascular disease in long-term type 1 (insulin-dependent) diabetes mellitus. Diabetologia. 1987;24: 1-9.
3. Yip J, Mattock MB, Morocutti A, Sethi M, Trevisan R, Viberti GC. Insulin resistance in insulin-dependent diabetic patients with microalbuminuria. Lancet. 1993;342:883-887. (Pubitemid 23291590)
4. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28:412-419. (Pubitemid 15018832)
5. Williams KV, Erbey JR, Becker D, Arsianian S, Orchard TJ. Can clinical factors estimate insulin resistance in type 1 diabetes? Diabetes. 2000;49:626-632. (Pubitemid 30183752)
6. Kilpatrick ES, Rigby AS, Atkin SL. Insulin resistance, the metabolic syndrome, and complication risk in type 1 diabetes. Double diabetes in the diabetes control and complications trial. Diabetes Care. 2007;30:707-712. (Pubitemid 46354357)
7. Davis TME, Bruce DG, Davis WA. Prevalence and prognostic implications of the metabolic syndrome in community-based patients with type 1 diabetes: The Fremantle Diabetes Study. Diab Res Clin Prac. 2007;78:412-417. (Pubitemid 350030323)
8. Eckel RH, Grundy SM, Zimmet PZ. The metabolic syndrome. Lancet. 2005;365:1415-1428. (Pubitemid 40523737)
9. Mulhall BP, Ong JP, Younossi ZM. Non-alcoholic fatty liver disease: an overview. J Gastroenterol Hepatol. 2002;17:1136-1143. (Pubitemid 36015607)
10. Angulo P, Lindor KD. Non-alcoholic fatty liver disease. J Gastroenterol Hepatol. 2002;17:S186-S190. (Pubitemid 34539308)
11. Ramesh S, Sanyal AJ. Evaluation and management of nonalcoholic steatohepatitis. J Hepatol. 2005;42:S2-12.
12. Angulo P, Keach JC, Batts KP, Lindor KD. Independent predictors of liver fibrosis in patients with nonalcoholic steatohepatitis. Hepatology. 1999;30:1356-1362.
13. Dichl AM, Goodman Z, Ishak KG. Alcohollike liver disease in nonalcoholics: a clinical and histologic comparison with alcohol-induced liver disease. Gastroenterology. 1988;95:1056-1062.
14. Pinto HC, Baptista A, Camilo ME, Valente A, Saragoca A, de Moura MC. Nonalcoholic steatohepatitis: clinicopathological comparison with alcoholic hepatitis in ambulatory and hospitalized patients. Dig Dis Sci. 1996;41:172-179. (Pubitemid 26064854)
15. Bacon BR, Farahvash MJ, Janney CG, Neuschwander-Tetri BA. Nonalcoholic steatohepatitis: an expanded clinical entity. Gastroenterology. 1994;107:1103-1109. (Pubitemid 24294573)
16. Duckworth WC, Hamel FG, Peavy DE. Hepatic metabolism of insulin. Am J Med. 1988;85:71-76. (Pubitemid 19012375)
17. Michael MD, Kulkarni RN, Postic C, et al. Loss of insulin signalling in hepatocytes leads to severe insulin resistance and progressive hepatic dysfunction. Mol Cell. 2000;6:87-97.
18. Bugianesi E, Gastaldelli A, Vanni E, et al. Insulin resistance in non-diabetic patients with non-alcoholic fatty liver disease: sites and mechanisms. Diabetologia. 2005;48:634-642. (Pubitemid 40591217)
19. Chitturi S, Abeygunasekera S, Farrell GC, et al. Nonalcoholic steatohepatitis and insulin resistance: insulin hypersecretion and specific association with the insulin resistance syndrome. Hepatology. 2002;35:373-379. (Pubitemid 34106377)
20. Cassader M, Gambino R, Musso G, et al. Postprandial triglyceride-rich lipoprotein metabolism and insulin sensitivity in nonalcoholic steatohepatitis patients. Lipids. 2001;36:1117-1124. (Pubitemid 33143966)
21. Tiikkainen M, Tamminen M, Hakkinen AM, et al. Liver-fat accumulation and insulin resistance in obese women with previous gestational diabetes. Obes Res. 2002;10:859-867. (Pubitemid 135688898)
22. Utzschneider KM, Kahn SE. The role of insulin resistance in nonalcoholic fatty liver disease. J Clin Endocrinol Metab. 2006;91:4753-4761. (Pubitemid 44917301)
23. Marchesini G, Bugianesi E, Forlani G, et al. Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology. 2003;37:917-923. (Pubitemid 36397405)
24. Angelico F, Del Ben M, Conti R, et al. Insulin resistance, the metabolic syndrome, and nonalcoholic fatty liver disease. J Clin Endocrinol Metab. 2005; 1578-1582. (Pubitemid 40464021)
25. Isomaa B, Almgren P, Tuomi T, et al. Cardiovascular morbidity and mortality associated with the metabolic syndrome. Diabetes Care. 2001;24:683-689. (Pubitemid 32893993)
26. Vozarova B, Stefan N, Lindsay RS, et al. High alanine aminotransferase is associated with decreased hepatic insulin sensitivity and predicts the development of type 2 diabetes. Diabetes. 2002;51:1889-1895. (Pubitemid 34564303)
27. Rashid M, Roberts EA. Nonalcoholic steatohepatitis in children. J Pediatr Gastroenterol Nutr. 2000;30:48-53. (Pubitemid 30349945)
28. Wanless IR, Lentz JS. Fatty liver hepatitis (steatohepatitis) and obesity: an autopsy study with analysis of risk factors. Hepatology. 1990;12:1106-1110.
29. Amarapurka DN, Amarapurkar AD, Patel ND, et al. Nonalcoholic steatohepatitis (NASH) with diabetes: predictors of liver fibrosis. Ann Hepatol. 2006;5:30-33.
30. Mofrad P, Contos MJ, Haque M, et al. Clinical and histologic spectrum of nonalcoholic fatty liver disease associated with normal ALT values. Hepatology. 2003;37:1286-1292. (Pubitemid 36667307)
31. Lee JY, Kim KM, Lee SG, et al. Prevalence of risk factors of non-alcoholic fatty liver disease in potential living donors in Korea: a review of 589 consecutive liver biopsies in a single center. J Hepatol. 2007;47:239-244. (Pubitemid 47021248)
32. Marchesini G, Brizi M, Morselli-Labate AM, et al. Association of non-alcoholic fatty liver disease to insulin resistance. Am J Med. 1999;107:450-455. (Pubitemid 29528333)
33. Marchesini G, Brizi M, Bianchi G, et al. Nonalcoholic fatty liver disease: a feature of the metabolic syndrome. Diabetes. 2001;50: 1844-1850. (Pubitemid 33641605)
34. Shimada M, Kawahara H, Ozaki K, et al. Usefulness of a combined evaluation of the serum adiponectin level, HOMA-IR, and serum type IV collagen 7S level to predict the early stage of nonalcoholic steatohepatits. Am J Gastroenterol. 2007;102:1931-1938. (Pubitemid 47301507)
35. Nakanishi N, Nishina K, Li W, Sato M, Suzuki K, Tatara K. Serum gamma-glutamyltransferase and development of impaired fasting glucose or type 2 diabetes in middle-aged Japanese men. J Intern Med. 2003; 95-287.
36. Hanley AJ, Williams K, Festa A, et al. Elevations in markers of liver injury and risk of type 2 diabetes: the Insulin Resistance Atherosclerosis Study. Diabetes. 2004;53:2623-2632. (Pubitemid 39299271)
37. Dixon JB, Bhathal PS, O'Brien PE. Nonalcoholic fatty liver disease: predictors of nonalcoholic steatohepatitis and liver fibrosis in the severely obese. Gastroenterology. 2001;121:91-100. (Pubitemid 32591518)
38. Fraser A, Harris R, Sattar N, Ebrahim S, Smith GD, Lawlor DA. Alanine aminotransferase, c-glutamyltransferase, and incident diabetes. Diabetes Care. 2009;32:741-749.
39. Fracanzani AL, Valenti L, Bugianesi E, et al. Risk of severe liver disease in nonalcoholic fatty liver disease with normal aminotransferase levels: a role for insulin resistance and diabetes. Hepatology. 2008;48:792-798.
40. Ekstedt M, Franzen LE, Mathiesen UL, et al. Long term followup of patients with NAFLD and elevated liver enzymes. Hepatology. 2006;44:865-873. (Pubitemid 46489550)
41. Targher G, Bertolini L, Poli F, et al. Nonalcoholic fatty liver disease and risk of future cardiovascular events among type 2 diabetic patients. Diabetes. 2005;54:3541-3546. (Pubitemid 43334347)
42. Browning JD, Szczepaniak LS, Dobbins R, et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology. 2004;40:1387-1395. (Pubitemid 39657013)
43. Reaven GM. Role of insulin resistance in human disease. Diabetes. 1988;37:1595-1607. (Pubitemid 19004941)
44. Kelly DE, McKolanis TM, Hegazi RAF, Kuller LH, Kalhan SC. Fatty liver in type 2 diabetes: relation to regional adiposity, fatty acids, and insulin resistance. Am J Physiol Endocrinol Metab. 2003;285:E906-E916. (Pubitemid 37176440)
45. Seppala-Lindroos A, Vehkavaara S, Hakkinen AM, 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;87:3023-3028. (Pubitemid 34816338)
46. O'Brien RM, Granner DK. Regulation of gene expression by insulin. Biochem J. 1991;278:609-619.
47. Fernandez-Real JM, Ricart-Engel W, Arroyo E, et al. Serum ferritin as a component of the insulin resistance syndrome. Diabetes Care. 1998;21:62-68. (Pubitemid 28030387)
48. Marchesini G, Brizi M, Bianchi G, Tomassetti S, Zoli M, Melchionda N. Metformin in non-alcoholic steatohepatitis. Lancet. 2001;358:893-894. (Pubitemid 32900577)
49. Promrat K, Lutchman G, Uwaifo GI, et al. A pilot study of pioglitazone treatment for non-alcoholic steatohepatitis. Hepatology. 2004;39:188-196. (Pubitemid 38461481)
50. Clark JM, Brancati FL, Diehl AM. The prevalence and etiology of elevated aminotransferase levels in the United States. Am J Gastroenterol. 2003;98:960-967. (Pubitemid 36733754)