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The Journal of Clinical Endocrinology & Metabolism Vol. 87, No. 7 3023-3028
Copyright © 2002 by The Endocrine Society

Special Features

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

Anneli Seppälä-Lindroos, Satu Vehkavaara, Anna-Maija Häkkinen, Takashi Goto, Jukka Westerbacka, Anssi Sovijärvi, Juha Halavaara and Hannele Yki-Järvinen

Department of Medicine, Divisions of Diabetes (A.S.-L., S.V., T.G., J.W., H.Y.-J.) and Clinical Physiology (A.S.), and Departments of Oncology (A.-M.H.) and Radiology (J.H.), University of Helsinki, FIN-00029 HUCH, Helsinki, Finland

Address all correspondence and requests for reprints to: Hannele Yki-Järvinen, M.D., Department of Medicine, Division of Diabetes, University of Helsinki, P.O. Box 340, FIN-00029 HUCH, Helsinki, Finland. E-mail: . ykijarvi{at}helsinki.fi

Abstract

We determined whether interindividual variation in hepatic insulin sensitivity could be attributed to variation in liver fat content (LFAT) independent of obesity. We recruited 30 healthy nondiabetic men whose LFAT (determined by proton spectroscopy); intraabdominal, sc, and total (determined by magnetic resonance imaging) fat; and insulin sensitivity of endogenous glucose rate of production (Ra) and suppression of serum FFA [euglycemic insulin clamp combined with [3-3H]glucose (0–300 min); insulin infusion rate, 0.3 mU/kg·min, 120–300 min] were measured. The men were divided into groups of low (mean ± SD, 1.7 ± 0.2%) and high (10.5 ± 2.0%) LFAT based on their median fat content. The low and high LFAT groups were comparable with respect to age (44 ± 2 vs. 42 ± 2 yr), body mass index (25 ± 1 vs. 26 ± 1 kg/m2 ), waist to hip ratio (0.953 ± 0.013 vs. 0.953 ± 0.013), maximal oxygen uptake (35.6 ± 1.5 vs. 33.5 ± 1.5 ml/kg·min), and intraabdominal, sc, and total fat. The high compared with the low LFAT group had several features of insulin resistance, including fasting hyperinsulinemia (7.3 ± 0.6 vs. 5.3 ± 0.6 mU/liter; P < 0.02, high vs. low LFAT) hypertriglyceridemia (1.4 ± 0.2 vs. 0.9 ± 0.1 mmol/liter; P < 0.02), a low high density lipoprotein (HDL) cholesterol concentration (1.4 ± 0.1 vs. 1.6 ± 0.1 mmol/liter; P < 0.05), and a higher ambulatory 24-h systolic blood pressure (130 ± 3 vs. 122 ± 3 mm Hg; P < 0.05). Basal glucose Ra and serum FFA were comparable between the groups, whereas insulin suppression of glucose Ra [51 ± 8 vs. 20 ± 12 mg/m2 ·min during 240–300 min (P < 0.05) or -55 ± 7 vs. -85 ± 12% below basal (P < 0.05, high vs. low LFAT)] and of serum FFA (299 ± 33 vs. 212 ± 13 µmol/liter; 240–300 min; P < 0.02) were impaired in the high compared with the low LFAT group. Insulin stimulation of glucose Rd were comparable in the men with high LFAT (141 ± 12 mg/m2 ·min) and those with low LFAT (156 ± 14 mg/m2 ·min; P = NS).

Fat accumulation in the liver is, independent of body mass index and intraabdominal and overall obesity, characterized by several features of insulin resistance in normal weight and moderately overweight subjects.




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PNAS, November 28, 2006; 103(48): 18273 - 18277.
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T. S. Burgert, S. E. Taksali, J. Dziura, T. R. Goodman, C. W. Yeckel, X. Papademetris, R. T. Constable, R. Weiss, W. V. Tamborlane, M. Savoye, et al.
Alanine Aminotransferase Levels and Fatty Liver in Childhood Obesity: Associations with Insulin Resistance, Adiponectin, and Visceral Fat
J. Clin. Endocrinol. Metab., November 1, 2006; 91(11): 4287 - 4294.
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G. Perseghin, R. Bonfanti, S. Magni, G. Lattuada, F. De Cobelli, T. Canu, A. Esposito, P. Scifo, G. Ntali, F. Costantino, et al.
Insulin resistance and whole body energy homeostasis in obese adolescents with fatty liver disease
Am J Physiol Endocrinol Metab, October 1, 2006; 291(4): E697 - E703.
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C. Koutsari and M. D. Jensen
Thematic review series: Patient-Oriented Research. Free fatty acid metabolism in human obesity
J. Lipid Res., August 1, 2006; 47(8): 1643 - 1650.
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F. G.S. Toledo, A. D. Sniderman, and D. E. Kelley
Influence of Hepatic Steatosis (Fatty Liver) on Severity and Composition of Dyslipidemia in Type 2 Diabetes
Diabetes Care, August 1, 2006; 29(8): 1845 - 1850.
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P. J. Raubenheimer, M. J. Nyirenda, and B. R. Walker
A Choline-Deficient Diet Exacerbates Fatty Liver but Attenuates Insulin Resistance and Glucose Intolerance in Mice Fed a High-Fat Diet.
Diabetes, July 1, 2006; 55(7): 2015 - 2020.
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J. S. Chang, B. Taouli, N. Salibi, E. M. Hecht, D. G. Chin, and V. S. Lee
Opposed-phase MRI for fat quantification in fat-water phantoms with 1H MR spectroscopy to resolve ambiguity of fat or water dominance.
Am. J. Roentgenol., July 1, 2006; 187(1): W103 - W106.
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H. A Walz, L. Harndahl, N. Wierup, E. Zmuda-Trzebiatowska, F. Svennelid, V. C Manganiello, T. Ploug, F. Sundler, E. Degerman, B. Ahren, et al.
Early and rapid development of insulin resistance, islet dysfunction and glucose intolerance after high-fat feeding in mice overexpressing phosphodiesterase 3B.
J. Endocrinol., June 1, 2006; 189(3): 629 - 641.
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D. E. Larson-Meyer, L. K. Heilbronn, L. M. Redman, B. R. Newcomer, M. I. Frisard, S. Anton, S. R. Smith, A. Alfonso, E. Ravussin, and the Pennington CALERIE Team
Effect of Calorie Restriction With or Without Exercise on Insulin Sensitivity, {beta}-Cell Function, Fat Cell Size, and Ectopic Lipid in Overweight Subjects.
Diabetes Care, June 1, 2006; 29(6): 1337 - 1344.
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X. Lin, Z. Chen, P. Yue, M. R. Averna, R. E. Ostlund Jr., M. A. Watson, and G. Schonfeld
A targeted apoB38.9 mutation in mice is associated with reduced hepatic cholesterol synthesis and enhanced lipid peroxidation
Am J Physiol Gastrointest Liver Physiol, June 1, 2006; 290(6): G1170 - G1176.
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B. Buemann, A. Astrup, O. Pedersen, E. Black, C. Holst, S. Toubro, S. Echwald, J. J. Holst, C. Rasmussen, and T. I. A. Sorensen
Possible Role of Adiponectin and Insulin Sensitivity in Mediating the Favorable Effects of Lower Body Fat Mass on Blood Lipids
J. Clin. Endocrinol. Metab., May 1, 2006; 91(5): 1698 - 1704.
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D. Linden, L. William-Olsson, A. Ahnmark, K. Ekroos, C. Hallberg, H. P. Sjogren, B. Becker, L. Svensson, J. C. Clapham, J. Oscarsson, et al.
Liver-directed overexpression of mitochondrial glycerol-3-phosphate acyltransferase results in hepatic steatosis, increased triacylglycerol secretion and reduced fatty acid oxidation
FASEB J, March 1, 2006; 20(3): 434 - 443.
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S. Franckhauser, S. Munoz, I. Elias, T. Ferre, and F. Bosch
Adipose Overexpression of Phosphoenolpyruvate Carboxykinase Leads to High Susceptibility to Diet-Induced Insulin Resistance and Obesity
Diabetes, February 1, 2006; 55(2): 273 - 280.
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 Int J EpidemiolHome page
M. Snijder, R. van Dam, M Visser, and J. Seidell
What aspects of body fat are particularly hazardous and how do we measure them?
Int. J. Epidemiol., February 1, 2006; 35(1): 83 - 92.
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A. J.G. Hanley, K. Williams, A. Festa, L. E. Wagenknecht, R. B. D'Agostino Jr, and S. M. Haffner
Liver Markers and Development of the Metabolic Syndrome: The Insulin Resistance Atherosclerosis Study
Diabetes, November 1, 2005; 54(11): 3140 - 3147.
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A. Grefhorst, J. Hoekstra, T. G. J. Derks, D. M. Ouwens, J. F. W. Baller, R. Havinga, L. M. Havekes, J. A. Romijn, and F. Kuipers
Acute hepatic steatosis in mice by blocking {beta}-oxidation does not reduce insulin sensitivity of very-low-density lipoprotein production
Am J Physiol Gastrointest Liver Physiol, September 1, 2005; 289(3): G592 - G598.
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X. Lin, P. Yue, Y. Xie, N. O. Davidson, N. Sakata, R. E. Ostlund Jr., Z. Chen, and G. Schonfeld
Reduced intestinal fat absorptive capacity but enhanced susceptibility to diet-induced fatty liver in mice heterozygous for ApoB38.9 truncation
Am J Physiol Gastrointest Liver Physiol, July 1, 2005; 289(1): G146 - G152.
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Y. Tamura, Y. Tanaka, F. Sato, J. B. Choi, H. Watada, M. Niwa, J. Kinoshita, A. Ooka, N. Kumashiro, Y. Igarashi, et al.
Effects of Diet and Exercise on Muscle and Liver Intracellular Lipid Contents and Insulin Sensitivity in Type 2 Diabetic Patients
J. Clin. Endocrinol. Metab., June 1, 2005; 90(6): 3191 - 3196.
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 DiabetesHome page
L. M. Watts, V. P. Manchem, T. A. Leedom, A. L. Rivard, R. A. McKay, D. Bao, T. Neroladakis, B. P. Monia, D. M. Bodenmiller, J. X.-C. Cao, et al.
Reduction of Hepatic and Adipose Tissue Glucocorticoid Receptor Expression With Antisense Oligonucleotides Improves Hyperglycemia and Hyperlipidemia in Diabetic Rodents Without Causing Systemic Glucocorticoid Antagonism
Diabetes, June 1, 2005; 54(6): 1846 - 1853.
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 Am J EpidemiolHome page
D. A. Lawlor, N. Sattar, G. D. Smith, and S. Ebrahim
The Associations of Physical Activity and Adiposity with Alanine Aminotransferase and Gamma-Glutamyltransferase
Am. J. Epidemiol., June 1, 2005; 161(11): 1081 - 1088.
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J. Westerbacka, K. Lammi, A.-M. Hakkinen, A. Rissanen, I. Salminen, A. Aro, and H. Yki-Jarvinen
Dietary Fat Content Modifies Liver Fat in Overweight Nondiabetic Subjects
J. Clin. Endocrinol. Metab., May 1, 2005; 90(5): 2804 - 2809.
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K. H. Pietilainen, A. Rissanen, J. Kaprio, S. Makimattila, A.-M. Hakkinen, J. Westerbacka, J. Sutinen, S. Vehkavaara, and H. Yki-Jarvinen
Acquired obesity is associated with increased liver fat, intra-abdominal fat, and insulin resistance in young adult monozygotic twins
Am J Physiol Endocrinol Metab, April 1, 2005; 288(4): E768 - E774.
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B. Ravikumar, P. E. Carey, J. E. M. Snaar, D. K. Deelchand, D. B. Cook, R. D. G. Neely, P. T. English, M. J. Firbank, P. G. Morris, and R. Taylor
Real-time assessment of postprandial fat storage in liver and skeletal muscle in health and type 2 diabetes
Am J Physiol Endocrinol Metab, April 1, 2005; 288(4): E789 - E797.
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 DiabetesHome page
K. F. Petersen, S. Dufour, D. Befroy, M. Lehrke, R. E. Hendler, and G. I. Shulman
Reversal of Nonalcoholic Hepatic Steatosis, Hepatic Insulin Resistance, and Hyperglycemia by Moderate Weight Reduction in Patients With Type 2 Diabetes
Diabetes, March 1, 2005; 54(3): 603 - 608.
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 Am. J. Physiol. Endocrinol. Metab.Home page
L. S. Szczepaniak, P. Nurenberg, D. Leonard, J. D. Browning, J. S. Reingold, S. Grundy, H. H. Hobbs, and R. L. Dobbins
Magnetic resonance spectroscopy to measure hepatic triglyceride content: prevalence of hepatic steatosis in the general population
Am J Physiol Endocrinol Metab, February 1, 2005; 288(2): E462 - E468.
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 Eur J EndocrinolHome page
S. B Haugaard, O. Andersen, F. Dela, J. J. Holst, H. Storgaard, M. Fenger, J. Iversen, and S. Madsbad
Defective glucose and lipid metabolism in human immunodeficiency virus-infected patients with lipodystrophy involve liver, muscle tissue and pancreatic {beta}-cells
Eur. J. Endocrinol., January 1, 2005; 152(1): 103 - 112.
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 GutHome page
E L Thomas, G Hamilton, N Patel, R O'Dwyer, C J Dore, R D Goldin, J D Bell, and S D Taylor-Robinson
Hepatic triglyceride content and its relation to body adiposity: a magnetic resonance imaging and proton magnetic resonance spectroscopy study
Gut, January 1, 2005; 54(1): 122 - 127.
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 DiabetesHome page
M. Krssak, A. Brehm, E. Bernroider, C. Anderwald, P. Nowotny, C. D. Man, C. Cobelli, G. W. Cline, G. I. Shulman, W. Waldhausl, et al.
Alterations in Postprandial Hepatic Glycogen Metabolism in Type 2 Diabetes
Diabetes, December 1, 2004; 53(12): 3048 - 3056.
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 CirculationHome page
S. Klein, L. E. Burke, G. A. Bray, S. Blair, D. B. Allison, X. Pi-Sunyer, Y. Hong, and R. H. Eckel
Clinical Implications of Obesity With Specific Focus on Cardiovascular Disease: A Statement for Professionals From the American Heart Association Council on Nutrition, Physical Activity, and Metabolism: Endorsed by the American College of Cardiology Foundation
Circulation, November 2, 2004; 110(18): 2952 - 2967.
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 Diabetes CareHome page
C. Thamer, J. Machann, M. Haap, N. Stefan, E. Heller, B. Schnodt, M. Stumvoll, C. Claussen, A. Fritsche, F. Schick, et al.
Intrahepatic Lipids Are Predicted by Visceral Adipose Tissue Mass in Healthy Subjects
Diabetes Care, November 1, 2004; 27(11): 2726 - 2729.
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N. Sattar, O. Scherbakova, I. Ford, D. St. J. O'Reilly, A. Stanley, E. Forrest, P. W. MacFarlane, C. J. Packard, S. M. Cobbe, and J. Shepherd
Elevated Alanine Aminotransferase Predicts New-Onset Type 2 Diabetes Independently of Classical Risk Factors, Metabolic Syndrome, and C-Reactive Protein in the West of Scotland Coronary Prevention Study
Diabetes, November 1, 2004; 53(11): 2855 - 2860.
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 DiabetesHome page
A. J.G. Hanley, K. Williams, A. Festa, L. E. Wagenknecht, R. B. D'Agostino Jr., J. Kempf, B. Zinman, and S. M. Haffner
Elevations in Markers of Liver Injury and Risk of Type 2 Diabetes: The Insulin Resistance Atherosclerosis Study
Diabetes, October 1, 2004; 53(10): 2623 - 2632.
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 NEJMHome page
H. Yki-Jarvinen
Thiazolidinediones
N. Engl. J. Med., September 9, 2004; 351(11): 1106 - 1118.
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M. Chen, M. Haluzik, N. J. Wolf, J. Lorenzo, K. R. Dietz, M. L. Reitman, and L. S. Weinstein
Increased Insulin Sensitivity in Paternal Gnas Knockout Mice Is Associated with Increased Lipid Clearance
Endocrinology, September 1, 2004; 145(9): 4094 - 4102.
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 DiabetesHome page
M. Tiikkainen, A.-M. Hakkinen, E. Korsheninnikova, T. Nyman, S. Makimattila, and H. Yki-Jarvinen
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, August 1, 2004; 53(8): 2169 - 2176.
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 J. Clin. Endocrinol. Metab.Home page
P. Iozzo, A. K. Turpeinen, T. Takala, V. Oikonen, J. Bergman, T. Gronroos, E. Ferrannini, P. Nuutila, and J. Knuuti
Defective Liver Disposal of Free Fatty Acids in Patients with Impaired Glucose Tolerance
J. Clin. Endocrinol. Metab., July 1, 2004; 89(7): 3496 - 3502.
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J. R. Garbow, X. Lin, N. Sakata, Z. Chen, D. Koh, and G. Schonfeld
In vivo MRS measurement of liver lipid levels in mice
J. Lipid Res., July 1, 2004; 45(7): 1364 - 1371.
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 NEJMHome page
S. Klein, L. Fontana, V. L. Young, A. R. Coggan, C. Kilo, B. W. Patterson, and B. S. Mohammed
Absence of an Effect of Liposuction on Insulin Action and Risk Factors for Coronary Heart Disease
N. Engl. J. Med., June 17, 2004; 350(25): 2549 - 2557.
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A. D. Karelis, D. H. St-Pierre, F. Conus, R. Rabasa-Lhoret, and E. T. Poehlman
Metabolic and Body Composition Factors in Subgroups of Obesity: What Do We Know?
J. Clin. Endocrinol. Metab., June 1, 2004; 89(6): 2569 - 2575.
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J. Sutinen, K. Kannisto, E. Korsheninnikova, R. M. Fisher, E. Ehrenborg, T. Nyman, A. Virkamaki, T. Funahashi, Y. Matsuzawa, H. Vidal, et al.
Effects of rosiglitazone on gene expression in subcutaneous adipose tissue in highly active antiretroviral therapy-associated lipodystrophy
Am J Physiol Endocrinol Metab, June 1, 2004; 286(6): E941 - E949.
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T. Tanoli, P. Yue, D. Yablonskiy, and G. Schonfeld
Fatty liver in familial hypobetalipoproteinemia: roles of the APOB defects, intra-abdominal adipose tissue, and insulin sensitivity
J. Lipid Res., May 1, 2004; 45(5): 941 - 947.
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 Am. J. Physiol. Endocrinol. Metab.Home page
R. Buettner, I. Ottinger, J. Scholmerich, and L. C. Bollheimer
Preserved direct hepatic insulin action in rats with diet-induced hepatic steatosis
Am J Physiol Endocrinol Metab, May 1, 2004; 286(5): E828 - E833.
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 EndocrinologyHome page
M. Haluzik, O. Gavrilova, and D. LeRoith
Peroxisome Proliferator-Activated Receptor-{alpha} Deficiency Does Not Alter Insulin Sensitivity in Mice Maintained on Regular or High-Fat Diet: Hyperinsulinemic-Euglycemic Clamp Studies
Endocrinology, April 1, 2004; 145(4): 1662 - 1667.
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