Intracellular and extracellular skeletal muscle triglyceride metabolism during alternating intensity exercise in humans

1 The main purpose of this study was to evaluate non‐invasively with magnetic resonance spectroscopy (1H‐MRS) changes in the concentrations of intracellular (IT) and extracellular (between muscle fibres) triglycerides (ET) in skeletal muscles of trained males (age range: 24–38 years) during two standard exercise protocols of alternating velocities. 2 Protocol 1 consisted of locomotion in a shuttle manner between two lines 30 m apart at four different velocities (1, 2, 3 and 4 m s−1) which were alternated every minute in a standard routine for 90 min, whereas Protocol 2 included locomotion between two lines 20 m apart at only three velocities (2, 2.7 and 4 m s−1) until volitional exhaustion. The heart rate during both protocols fluctuated between 140 and 200 beats min−1. 3 Using pre‐exercise muscle water to quantify individual total creatine (TCr) that was utilized as an internal standard and assuming that TCr does not change during exercise, subjects’ mean IT and ET concentrations in soleus (Sol) muscle before Protocol 1 (n= 8) were 45.8 ± 4.8 mmol (kg dry weight)−1 (mean ± s.e.m.) and 93.1 ± 14.1 mmol (kg dry weight)−1, respectively. After the exercise, the concentrations of IT and ET were not significantly different from the values at rest. Before Protocol 2 (n= 4), IT concentrations in Sol, gastrocnemius (Gast) and tibialis (Tib) muscles were 46.4 ± 13.6, 35.0 ± 12.1 and 23.1 ± 4.8 mmol (kg dry weight)−1, respectively, and were not affected by the exhaustive exercise. The ET concentrations in Sol, Gast and Tib were 136.4 ± 38.1, 175.3 ± 86.5 and 79.3 ± 20.0 mmol (kg dry weight)−1, respectively, and they did not change significantly after exhaustion. 4 The study showed that levels of IT and ET were not affected by alternating intensity exercise to fatigue. This suggests that IT and ET in human Sol, Gast and Tib muscles do not contribute significantly to the energy turnover during this type of exercise. Energy for this type of muscle contraction may arise primarily from muscle phosphocreatine (PCr) and glycogen breakdown, circulating glucose and fatty acids from triglycerides other than those encountered within and between muscle cells.

[1]  G. Dalsky,et al.  Muscle triglyceride utilization during exercise: effect of training. , 1986, Journal of applied physiology.

[2]  J A Romijn,et al.  Regulation of endogenous fat and carbohydrate metabolism in relation to exercise intensity and duration. , 1993, The American journal of physiology.

[3]  P A Bottomley,et al.  Total creatine in muscle: imaging and quantification with proton MR spectroscopy. , 1997, Radiology.

[4]  D. Constantin-Teodosiu,et al.  Anaerobic energy production in human skeletal muscle in intense contraction: a comparison of 31P magnetic resonance spectroscopy and biochemical techniques , 1997, Experimental physiology.

[5]  L. Hagenfeldt,et al.  Utilization of blood‐borne and intramuscular substrates during continuous and intermittent exercise in man. , 1977, The Journal of physiology.

[6]  P D Gollnick,et al.  Selective glycogen depletion pattern in human muscle fibres after exercise of varying intensity and at varying pedalling rates , 1974, The Journal of physiology.

[7]  E. Hultman.  Studies on muscle metabolism of glycogen and active phosphate in man with special reference to exercise and diet. , 1967, Scandinavian journal of clinical and laboratory investigation. Supplementum.

[8]  B. Kiens,et al.  Lipoprotein metabolism influenced by training-induced changes in human skeletal muscle. , 1989, The Journal of clinical investigation.

[9]  A. Keys,et al.  Density and composition of mammalian muscle , 1960 .

[10]  G. Heigenhauser,et al.  Variability of triacylglycerol content in human skeletal muscle biopsy samples. , 1996, Journal of applied physiology.

[11]  E. Hultman,et al.  Carbohydrate metabolism and electrolyte changes in human muscle tissue during heavy work. , 1971, Journal of applied physiology.

[12]  P. Bottomley.  Spatial Localization in NMR Spectroscopy in Vivo , 1987, Annals of the New York Academy of Sciences.

[13]  A. Taylor,et al.  Effects of beta 1- vs. beta 1 + beta 2-blockade on exercise endurance and muscle metabolism in humans. , 1989, Journal of applied physiology.

[14]  M. Tarnopolsky,et al.  Effects of training duration on substrate turnover and oxidation during exercise. , 1996, Journal of applied physiology.

[15]  E Jansson,et al.  FIBER TYPES AND METABOLIC POTENTIALS OF SKELETAL MUSCLES IN SEDENTARY MAN AND ENDURANCE RUNNERS * , 1977, Annals of the New York Academy of Sciences.

[16]  R. Shulman,et al.  13C-NMR measurements of muscle glycogen during low-intensity exercise. , 1991, Journal of applied physiology.

[17]  L. Kaijser,et al.  Effect of diet on the utilization of blood-borne and intramuscular substrates during exercise in man. , 1982, Acta physiologica Scandinavica.

[18]  B. Saltin,et al.  NMR and analytic biochemical evaluation of CrP and nucleotides in the human calf during muscle contraction. , 1993, Journal of applied physiology.

[19]  D. Costill,et al.  Effects of diet on muscle triglyceride and endurance performance. , 1997, Journal of applied physiology.

[20]  R De Beer,et al.  Quality assessment in in vivo NMR spectroscopy: VI. Multicentre quantification of MRS test signals. , 1995, Magnetic resonance imaging.

[21]  L. Sidossis,et al.  A new correction factor for use in tracer estimations of plasma fatty acid oxidation. , 1995, The American journal of physiology.

[22]  D. Matthews,et al.  Effect of endurance training on plasma free fatty acid turnover and oxidation during exercise. , 1993, The American journal of physiology.

[23]  J. Frahm,et al.  Localized Proton NMR spectroscopy using stimulated echoes: Applications to human skeletal muscle in vivo , 1991, Magnetic resonance in medicine.

[24]  E. Richter,et al.  Increased plasma FFA uptake and oxidation during prolonged exercise in trained vs. untrained humans. , 1992, The American journal of physiology.

[25]  A. Day.  Syntheses of fused imidazole ring compounds as potential antimetabolites. , 1957, Transactions of the New York Academy of Sciences.

[26]  G K Radda,et al.  Examination of a case of suspected McArdle's syndrome by 31P nuclear magnetic resonance. , 1981, The New England journal of medicine.

[27]  C Boesch,et al.  In vivo determination of intra‐myocellular lipids in human muscle by means of localized 1H‐MR‐spectroscopy , 1997, Magnetic resonance in medicine.

[28]  E Jansson,et al.  Substrate utilization and enzymes in skeletal muscle of extremely endurance-trained men. , 1987, Journal of applied physiology.

[29]  E Hultman,et al.  The contents of high‐energy phosphates in different fibre types in skeletal muscles from rat, guinea‐pig and man. , 1982, The Journal of physiology.

[30]  L. Rowell,et al.  Skeletal muscle lipids. II. Nonutilization of intracellular lipid esters as an energy source for contractile activity. , 1966, The Journal of biological chemistry.

[31]  N. Vøllestad,et al.  Glycogen and lactate metabolism during low-intensity exercise in man. , 1990, Acta physiologica Scandinavica.

[32]  E. Richter,et al.  Membrane associated fatty acid binding protein (FABPpm) in human skeletal muscle is increased by endurance training. , 1997, Biochemical and biophysical research communications.

[33]  D. Gadian.  NMR and its Applications to Living Systems , 1996 .

[34]  B. Saltin,et al.  Skeletal muscle substrate utilization during submaximal exercise in man: effect of endurance training. , 1993, The Journal of physiology.

[35]  P. Luyten,et al.  Accurate quantification of in vivo 31P NMR signals using the variable projection method and prior knowledge , 1988, Magnetic resonance in medicine.

[36]  E Jansson,et al.  Metabolic characteristics of fibre types in human skeletal muscle. , 1975, Acta physiologica Scandinavica.

[37]  F Schick,et al.  Comparison of localized proton NMR signals of skeletal muscle and fat tissue in vivo: Two lipid compartments in muscle tissue , 1993, Magnetic resonance in medicine.

[38]  L. Carlson,et al.  Concentration of Triglycerides, Phospholipids and Glycogen in Skeletal Muscle and of Free Fatty Acids and β‐Hydroxybutyric Acid in Blood in Man in Response to Exercise , 1971, European journal of clinical investigation.