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The Journal of Clinical Endocrinology & Metabolism Vol. 86, No. 12 5755-5761
Copyright © 2001 by The Endocrine Society

Other Original Articles

Skeletal Muscle Lipid Content and Insulin Resistance: Evidence for a Paradox in Endurance-Trained Athletes

Bret H. Goodpaster, Jing He, Simon Watkins and David E. Kelley

Departments of Medicine (B.H.G., J.H., D.E.K.) and Cell Biology (S.W.), University of Pittsburgh, Pittsburgh, Pennsylvania 15261

Address all correspondence and requests for reprints to: Dr. Bret H. Goodpaster, E1140 Biomedical Science Tower, University of Pittsburgh, Pittsburgh, Pennsylvania 15261. E-mail: bgood+{at}pitt.edu

Abstract

We examined the hypothesis that an excess accumulation of intramuscular lipid (IMCL) is associated with insulin resistance and that this may be mediated by the oxidative capacity of muscle. Nine sedentary lean (L) and 11 obese (O) subjects, 8 obese subjects with type 2 diabetes mellitus (D), and 9 lean, exercise-trained (T) subjects volunteered for this study. Insulin sensitivity (M) determined during a hyperinsulinemic (40 mU·m-2min-1) euglycemic clamp was greater (P < 0.01) in L and T, compared with O and D (9.45 ± 0.59 and 10.26 ± 0.78 vs. 5.51 ± 0.61 and 1.15 ± 0.83 mg·min-1kg fat free mass-1, respectively). IMCL in percutaneous vastus lateralis biopsy specimens by quantitative image analysis of Oil Red O staining was approximately 2-fold higher in D than in L (3.04 ± 0.39 vs. 1.40 ± 0.28% area as lipid; P < 0.01). IMCL was also higher in T (2.36 ± 0.37), compared with L (P < 0.01). The oxidative capacity of muscle determined with succinate dehydrogenase staining of muscle fibers was higher in T, compared with L, O, and D (50.0 ± 4.4, 36.1 ± 4.4, 29.7 ± 3.8, and 33.4 ± 4.7 optical density units, respectively; P < 0.01). IMCL was negatively associated with M (r = -0.57, P < 0.05) when endurance-trained subjects were excluded from the analysis, and this association was independent of body mass index. However, the relationship between IMCL and M was not significant when trained individuals were included. There was a positive association between the oxidative capacity and M among nondiabetics (r = 0.37, P < 0.05). In summary, skeletal muscle of trained endurance athletes is markedly insulin sensitive and has a high oxidative capacity, despite having an elevated lipid content. In conclusion, the capacity for lipid oxidation may be an important mediator of the association between excess muscle lipid accumulation and insulin resistance.




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Am J Physiol Endocrinol Metab, November 1, 2004; 287(5): E857 - E862.
[Abstract] [Full Text] [PDF]

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E. Erol, G. W. Cline, J. K. Kim, H. Taegtmeyer, and B. Binas
Nonacute effects of H-FABP deficiency on skeletal muscle glucose uptake in vitro
Am J Physiol Endocrinol Metab, November 1, 2004; 287(5): E977 - E982.
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J. He and D. E. Kelley
Muscle glycogen content in type 2 diabetes mellitus
Am J Physiol Endocrinol Metab, November 1, 2004; 287(5): E1002 - E1007.
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L. J. C. van Loon
Use of intramuscular triacylglycerol as a substrate source during exercise in humans
J Appl Physiol, October 1, 2004; 97(4): 1170 - 1187.
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R. J. Sigal, G. P. Kenny, D. H. Wasserman, and C. Castaneda-Sceppa
Physical Activity/Exercise and Type 2 Diabetes
Diabetes Care, October 1, 2004; 27(10): 2518 - 2539.
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B. Braun, C. Sharoff, S. R. Chipkin, and F. Beaudoin
Effects of insulin resistance on substrate utilization during exercise in overweight women
J Appl Physiol, September 1, 2004; 97(3): 991 - 997.
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P. Iozzo, T. Takala, V. Oikonen, J. Bergman, T. Gronroos, E. Ferrannini, P. Nuutila, and J. Knuuti
Effect of Training Status on Regional Disposal of Circulating Free Fatty Acids in the Liver and Skeletal Muscle During Physiological Hyperinsulinemia
Diabetes Care, September 1, 2004; 27(9): 2172 - 2177.
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N. da Costa, C. McGillivray, Q. Bai, J. D. Wood, G. Evans, and K.-C. Chang
Restriction of Dietary Energy and Protein Induces Molecular Changes in Young Porcine Skeletal Muscles
J. Nutr., September 1, 2004; 134(9): 2191 - 2199.
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S. R. Kashyap, R. Belfort, R. Berria, S. Suraamornkul, T. Pratipranawatr, J. Finlayson, A. Barrentine, M. Bajaj, L. Mandarino, R. DeFronzo, et al.
Discordant effects of a chronic physiological increase in plasma FFA on insulin signaling in healthy subjects with or without a family history of type 2 diabetes
Am J Physiol Endocrinol Metab, September 1, 2004; 287(3): E537 - E546.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
L. J. C. van Loon, R. Koopman, R. Manders, W. van der Weegen, G. P. van Kranenburg, and H. A. Keizer
Intramyocellular lipid content in type 2 diabetes patients compared with overweight sedentary men and highly trained endurance athletes
Am J Physiol Endocrinol Metab, September 1, 2004; 287(3): E558 - E565.
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G. Perseghin, M. Comola, P. Scifo, S. Benedini, F. De Cobelli, R. Lanzi, F. Costantino, G. Lattuada, A. Battezzati, A. Del Maschio, et al.
Postabsorptive and insulin-stimulated energy and protein metabolism in patients with myotonic dystrophy type 1
Am. J. Clinical Nutrition, August 1, 2004; 80(2): 357 - 364.
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A. K. Fox, A. E. Kaufman, and J. F. Horowitz
Adding fat calories to meals after exercise does not alter glucose tolerance
J Appl Physiol, July 1, 2004; 97(1): 11 - 16.
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 J. Biol. Chem.Home page
G. Perdomo, S. R. Commerford, A.-M. T. Richard, S. H. Adams, B. E. Corkey, R. M. O'Doherty, and N. F. Brown
Increased {beta}-Oxidation in Muscle Cells Enhances Insulin-stimulated Glucose Metabolism and Protects against Fatty Acid-induced Insulin Resistance Despite Intramyocellular Lipid Accumulation
J. Biol. Chem., June 25, 2004; 279(26): 27177 - 27186.
[Abstract] [Full Text] [PDF]

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 NEJMHome page
K. R. Short, K. S. Nair, C. S. Stump, M. Bajaj, L. J. Mandarino, P. J. Raubenheimer, M. Mohlig, F. Isken, M. Ristow, K. F. Petersen, et al.
Impaired Mitochondrial Activity and Insulin-Resistant Offspring of Patients with Type 2 Diabetes
N. Engl. J. Med., June 3, 2004; 350(23): 2419 - 2421.
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B. H Goodpaster, V A. Stenger, F. Boada, T. McKolanis, D. Davis, R. Ross, and D. E Kelley
Skeletal muscle lipid concentration quantified by magnetic resonance imaging
Am. J. Clinical Nutrition, May 1, 2004; 79(5): 748 - 754.
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C. Neumann-Haefelin, A. Beha, J. Kuhlmann, U. Belz, M. Gerl, M. Quint, G. Biemer-Daub, M. Broenstrup, M. Stein, E. Kleinschmidt, et al.
Muscle-Type Specific Intramyocellular and Hepatic Lipid Metabolism During Starvation in Wistar Rats
Diabetes, March 1, 2004; 53(3): 528 - 534.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
D.-H. Han, L. A. Nolte, J.-S. Ju, T. Coleman, J. O. Holloszy, and C. F. Semenkovich
UCP-mediated energy depletion in skeletal muscle increases glucose transport despite lipid accumulation and mitochondrial dysfunction
Am J Physiol Endocrinol Metab, March 1, 2004; 286(3): E347 - E353.
[Abstract] [Full Text]

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S. R. Stannard and N. A. Johnson
Insulin resistance and elevated triglyceride in muscle: more important for survival than 'thrifty' genes?
J. Physiol., February 1, 2004; 554(3): 595 - 607.
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A. P. Russell, P. Schrauwen, E. Somm, G. Gastaldi, M. K. C. Hesselink, G. Schaart, E. Kornips, S. K. Lo, D. Bufano, J.-P. Giacobino, et al.
Decreased Fatty Acid {beta}-Oxidation in Riboflavin-Responsive, Multiple Acylcoenzyme A Dehydrogenase-Deficient Patients Is Associated with an Increase in Uncoupling Protein-3
J. Clin. Endocrinol. Metab., December 1, 2003; 88(12): 5921 - 5926.
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L. J C van Loon, R. Koopman, J. H C H Stegen, A. J M Wagenmakers, H. A Keizer, and W. H M Saris
Intramyocellular lipids form an important substrate source during moderate intensity exercise in endurance-trained males in a fasted state
J. Physiol., December 1, 2003; 553(2): 611 - 625.
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 Am. J. Physiol. Endocrinol. Metab.Home page
G. Perseghin, G. Lattuada, M. Danna, L. P. Sereni, P. Maffi, F. De Cobelli, A. Battezzati, A. Secchi, A. Del Maschio, and L. Luzi
Insulin resistance, intramyocellular lipid content, and plasma adiponectin in patients with type 1 diabetes
Am J Physiol Endocrinol Metab, December 1, 2003; 285(6): E1174 - E1181.
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C. R. Bruce, M. J. Anderson, A. L. Carey, D. G. Newman, A. Bonen, A. D. Kriketos, G. J. Cooney, and J. A. Hawley
Muscle Oxidative Capacity Is a Better Predictor of Insulin Sensitivity than Lipid Status
J. Clin. Endocrinol. Metab., November 1, 2003; 88(11): 5444 - 5451.
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B. H. Goodpaster, A. Katsiaras, and D. E. Kelley
Enhanced Fat Oxidation Through Physical Activity Is Associated With Improvements in Insulin Sensitivity in Obesity
Diabetes, September 1, 2003; 52(9): 2191 - 2197.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
J. W. Helge and F. Dela
Effect of Training on Muscle Triacylglycerol and Structural Lipids: A Relation to Insulin Sensitivity?
Diabetes, August 1, 2003; 52(8): 1881 - 1887.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
H. M. Wilmsen, T. P. Ciaraldi, L. Carter, N. Reehman, S. R. Mudaliar, and R. R. Henry
Thiazolidinediones upregulate impaired fatty acid uptake in skeletal muscle of type 2 diabetic subjects
Am J Physiol Endocrinol Metab, August 1, 2003; 285(2): E354 - E362.
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I. R. Schlaepfer, L. K. Pulawa, L. D. M. C-B. Ferreira, D. E. James, W. H. Capell, and R. H. Eckel
Increased expression of the SNARE accessory protein Munc18c in lipid-mediated insulin resistance
J. Lipid Res., June 1, 2003; 44(6): 1174 - 1181.
[Abstract] [Full Text] [PDF]

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 Diabetes CareHome page
S. K. Gan, A. D. Kriketos, B. A. Ellis, C. H. Thompson, E. W. Kraegen, and D. J. Chisholm
Changes in Aerobic Capacity and Visceral Fat but not Myocyte Lipid Levels Predict Increased Insulin Action After Exercise in Overweight and Obese Men
Diabetes Care, June 1, 2003; 26(6): 1706 - 1713.
[Abstract] [Full Text] [PDF]

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 Diabetes CareHome page
D. Kim, S. Nam, C. Ahn, K. Kim, S. Yoon, J. Kim, B. Cha, S. Lim, K. Kim, H. Lee, et al.
Correlation Between Midthigh Low- Density Muscle and Insulin Resistance in Obese Nondiabetic Patients in Korea
Diabetes Care, June 1, 2003; 26(6): 1825 - 1830.
[Abstract] [Full Text] [PDF]

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M. I. Goran, G. D. C. Ball, and M. L. Cruz
Obesity and Risk of Type 2 Diabetes and Cardiovascular Disease in Children and Adolescents
J. Clin. Endocrinol. Metab., April 1, 2003; 88(4): 1417 - 1427.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
V. B. Schrauwen-Hinderling, P. Schrauwen, M. K. C. Hesselink, J. M. A. van Engelshoven, K. Nicolay, W. H. M. Saris, A. G. H. Kessels, and M. E. Kooi
The Increase in Intramyocellular Lipid Content Is a Very Early Response to Training
J. Clin. Endocrinol. Metab., April 1, 2003; 88(4): 1610 - 1616.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
C. Thamer, J. Machann, O. Bachmann, M. Haap, D. Dahl, B. Wietek, O. Tschritter, A. Niess, K. Brechtel, A. Fritsche, et al.
Intramyocellular Lipids: Anthropometric Determinants and Relationships with Maximal Aerobic Capacity and Insulin Sensitivity
J. Clin. Endocrinol. Metab., April 1, 2003; 88(4): 1785 - 1791.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
G. J. Crowther, J. M. Milstein, S. A. Jubrias, M. J. Kushmerick, R. K. Gronka, and K. E. Conley
Altered energetic properties in skeletal muscle of men with well-controlled insulin-dependent (type 1) diabetes
Am J Physiol Endocrinol Metab, April 1, 2003; 284(4): E655 - E662.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
R. E. Gray, C. J. Tanner, W. J. Pories, K. G. MacDonald, and J. A. Houmard
Effect of weight loss on muscle lipid content in morbidly obese subjects
Am J Physiol Endocrinol Metab, April 1, 2003; 284(4): E726 - E732.
[Abstract] [Full Text] [PDF]

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 Diabetes CareHome page
V. Simha, L. S. Szczepaniak, A. J. Wagner, A. M. DePaoli, and A. Garg
Effect of Leptin Replacement on Intrahepatic and Intramyocellular Lipid Content in Patients With Generalized Lipodystrophy
Diabetes Care, January 1, 2003; 26(1): 30 - 35.
[Abstract] [Full Text] [PDF]

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M. J. Watt, G. J. F. Heigenhauser, and L. L. Spriet
Intramuscular triacylglycerol utilization in human skeletal muscle during exercise: is there a controversy?
J Appl Physiol, October 1, 2002; 93(4): 1185 - 1195.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Endocrinol. Metab.Home page
G. Perseghin, P. Scifo, M. Danna, A. Battezzati, S. Benedini, E. Meneghini, A. Del Maschio, and L. Luzi
Normal insulin sensitivity and IMCL content in overweight humans are associated with higher fasting lipid oxidation
Am J Physiol Endocrinol Metab, September 1, 2002; 283(3): E556 - E564.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
C. Bernal-Mizrachi, S. Weng, B. Li, L. A. Nolte, C. Feng, T. Coleman, J. O. Holloszy, and C. F. Semenkovich
Respiratory Uncoupling Lowers Blood Pressure Through a Leptin-Dependent Mechanism in Genetically Obese Mice
Arterioscler. Thromb. Vasc. Biol., June 1, 2002; 22(6): 961 - 968.
[Abstract] [Full Text] [PDF]


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