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Observation of intramyocellular lipids by means of 1H magnetic resonance spectroscopy

Published online by Cambridge University Press:  12 June 2007

Chris Boesch*
Affiliation:
Department of Clinical Research, MR Spectroscopy and Methodology, University of Bern, CH-3010 Bern, Switzerland
Jacques Décombaz
Affiliation:
Nestec Ltd, Nestlé; Research Centre, Lausanne, Switzerland
Johannes Slotboom
Affiliation:
Department of Clinical Research, MR Spectroscopy and Methodology, University of Bern, CH-3010 Bern, Switzerland
Roland Kreis
Affiliation:
Department of Clinical Research, MR Spectroscopy and Methodology, University of Bern, CH-3010 Bern, Switzerland
*
*Corresponding Author: Professor Chris Boesch, fax +41 31 382 24 86, email chris.boesch@insel.ch
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Abstract

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Magnetic resonance imaging (MRI) and magnetic resonance spectroscopy (MRS) are being increasingly used for investigations of human muscle physiology. While MRI reveals the morphology of muscles in great detail (e.g. for the determination of muscle volumes), MRS provides information on the chemical composition of the tissue. Depending on the observed nucleus, MRS allows the monitoring of high-energy phosphates (31P MRS), glycogen (13C MRS), or intramyocellular lipids (1H MRS), to give only a few examples. The observation of intramyocellular lipids (IMCL) by means of 1H MRS is non-invasive and, therefore, can be repeated many times and with a high temporal resolution. MRS has the potential to replace the biopsy for the monitoring of IMCL levels; however, the biopsy still has the advantage that other methods such as those used in molecular biology can be applied to the sample. The present study describes variations in the IMCL levels (expressed in mmol/kg wet weight and ml/100 ml) in three different muscles before and after (0, 1, 2, and 5 d) marathon runs for a well-trained individual who followed two different recovery protocols varying mainly in the diet. It was shown that the repletion of IMCL levels is strongly dependent on the diet post exercise. The monitoring of IMCL levels by means of 1H MRS is extremely promising, but several methodological limitations and pitfalls need to be considered, and these are addressed in the present review.

Type
Meeting Report
Copyright
The Nutrition Society

References

Andersson, A, Sjodin, A, Olsson, R & Vessby, B (1998) Effects of physical exercise on phospholipid fatty acid composition in skeletal muscle. American Journal of Physiology 274, E432E438.Google Scholar
Avison, MJ, Rothman, DL, Nadel, E & Shulman, RG (1988) Detection of human muscle glycogen by natural abundance 13C NMR. Proceedings of the National Academy of Sciences USA 85, 16341636.Google Scholar
Barany, M & Venkatasubramanian, PN (1989) Volume-selective water-suppressed proton spectra of human brain and muscle in vivo. NMR in Biomedicine 2, 711.Google Scholar
Barker, PB, Soher, BJ, Blackband, SJ, Chatham, JC, Mathews, VP & Bryan, RN (1993) Quantitation of proton NMR spectra of the human brain using tissue water as an internal concentration reference. NMR in Biomedicine 6, 8994.Google Scholar
Basser, PJ (1995) Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR in Biomedicine 8, 333344.Google Scholar
Bassett, LW & Gold, RH (1989) Magnetic resonance imaging of the musculoskeletal system – an overview. Clinical Orthopedics and Related Research 244, 1728.Google Scholar
Becker, ED, Fisk, C & Khetrapal, CL (1996) The development of NMR. In Encyclopedia of Nuclear Magnetic Resonance, pp. 1160 [Grant, DM and Harris, RK, editors]. Chichester, West Sussex: John Wiley.Google Scholar
Bergman, BC, Butterfield, GE, Wolfel, EE, Casazza, GA, Lopaschuk, GD & Brooks, GA (1999) Evaluation of exercise and training on muscle lipid metabolism. American Journal of Physiology 276, E106E117.Google Scholar
Boesch, C & Kreis, R (1997) MR-spectroscopy (MRS) of different nuclei applied to human muscle: Additional information obtained by 1H-MRS. International Journal of Sports Medicine 18, S310S312.CrossRefGoogle ScholarPubMed
Boesch, C & Kreis, R (1999) Imaging and spectroscopy of muscle. In Encyclopedia of Nuclear Magnetic Resonance – Medical Spin-Off [Young, IR, Grant, DM and Harris, RK, editors.] Chichester, West Sussex: John Wiley & Sons (In the Press).Google Scholar
Boesch, C, Kreis, R, Howald, H, Matter, S, Billeter, R, Essen-Gustavsson, B & Hoppeler, H (1998) Validation of intra-myocellular lipid (IMCL) levels determined by 1H-MRS, using morphometry and chemical analysis in human biopsy samples. Proceedings of the International Society of Magnetic Resonance in Medicine Annual Meeting 3, 1785 Abstr.Google Scholar
Boesch, C, Slotboom, J, Hoppeler, H & Kreis, R (1997) In vivo determination of intra-myocellular lipids in human muscle by means of localized 1H-MR-spectroscopy. Magnetic Resonance in Medicine 37, 484493.Google Scholar
Boesch, C, Slotboom, J, Kamber, M, Koster, M, Hoppeler, H & Kreis, R (1996) Activity-dependent distribution of intra-myocellular lipids determined by 1H-MRS. Magnetic Resonance Materials in Physics, Biology, and Medicine 4, Suppl., 154155 Abstr.Google Scholar
Bottomley, PA (1984) US Patent no. 4,480,228.Google Scholar
Brooks, GA & Mercier, J (1994) Balance of carbohydrate and lipid utilization during exercise: the ‘crossover’ concept. Journal of Applied Physiology 76, 22532261.CrossRefGoogle ScholarPubMed
Brown, SM & Bradley WG, Jr (1994) Kinematic magnetic resonance imaging of the knee. Magnetic Resonance Imaging Clinics of North America 2, 441449.CrossRefGoogle ScholarPubMed
Bruhn, H, Frahm, J, Gyngell, ML, Merboldt, KD, Haenicke W. Sauter, R (1991) Localized proton NMR spectroscopy using stimulated echoes: Applications to human skeletal muscle in vivo. Magnetic Resonance in Medicine 17, 8294.CrossRefGoogle ScholarPubMed
Conley, KE, Cress, ME, Jubrias, SA, Esselman, PC & Odderson, IR (1995) From muscle properties to human performance, using magnetic resonance. Journal of Gerontology 50, Special no., 3540.Google ScholarPubMed
Cooper, DM & Barstow, TJ (1996) Magnetic resonance imaging and spectroscopy in studying exercise in children. Exercise and Sport Sciences Review 24, 475499.CrossRefGoogle ScholarPubMed
Elliott, MA, Walter, GA, Gulish, H, Sadi, AS, Lawson, DD, Jaffe, W, Insko, EK, Leigh, JS & Vandenborne, K (1997) Volumetric measurement of human calf muscle from magnetic resonance imaging. Magnetic Resonance Materials in Physics, Biology, and Medicine 5, 9398.Google Scholar
Ericsson, A, Franck, A, Sjödin, A, Andersson, A & Wesby, B (1998) Intra-myocellular lipids in human skeletal muscle, after an ultra marathon race studied by in vivo 1H-MRS. Magnetic Resonance Materials in Physics, Biology, and Medicine 6, Suppl. 1, 219 Abstr.Google Scholar
Essen, B (1977) Intramuscular substrate utilization during prolonged exercise. Annals of the New York Academy of Sciences 301, 3044.CrossRefGoogle ScholarPubMed
Evanochko, WT & Pohost, GM (1994) Structural studies of NMR detected lipids in myocardial ischemia. NMR in Biomedicine 7, 269277.Google Scholar
Fleckenstein, JL, Bertocci, LA, Nunnally, RL, Parkey, RW & Peshock;, RM (1989) Exercise-enhanced MR imaging of variations in forearm muscle anatomy and use: importance in MR spectroscopy. American Journal of Roentgenology 153, 693698.Google Scholar
Fleckenstein, JL, Canby, RC, Parkey, RW & Peshock, RM (1988) Acute effects of exercise on MR imaging of skeletal muscle in normal volunteers. American Journal of Roentgenology 151, 231237.CrossRefGoogle ScholarPubMed
Fleckenstein, JL, Weatherall, PT, Bertocci, LA, Ezaki, M, Haller, RG, Greenlee, R, Bryan, WW & Peshock, RM (1991) Locomotor system assessment by muscle magnetic resonance imaging. Magnetic Resonance Quarterly 7, 79103.Google Scholar
Froberg, SO & Mossfeldt, F (1971) Effect of prolonged strenuous exercise on the concentration of triglycerides, phospholipids and glycogen in muscle of man. Acta Physiologica Scandinavica 82, 167171.CrossRefGoogle ScholarPubMed
Fukunaga, T, Roy, RR, Shellock, FG, Hodgson, JA, Day, MK, Lee, PL, Kwong-Fu, H & Edgerton, VR (1992) Physiological cross-sectional area of human leg muscles based on magnetic resonance imaging. Journal of Orthopaedic Research 10, 926934.Google Scholar
Fusch, C, Slotboom, J, Fuehrer, U, Schumacher, R, Zimmermann, W, Moessinger, A, Blum, JW & Boesch, C (1998) Measurement of neonatal body composition: Validation of 1H-3D-CSI and MRI by chemical analysis in piglets. Proceedings of the International Society of Magnetic Resonance in Medicine Annual Meeting 3, 1811 Abstr.Google Scholar
Gruetter, R, Prolla, TA & Shulman, RG (1991) 13C NMR visibility of rabbit muscle glycogen in vivo. Magnetic Resonance in Medicine 20, 327332.Google Scholar
Havel, RJ, Carlson, LA, Ekelund, LG & Holmgren, A (1964) Turnover rate and oxidation of different free fatty acids in man during exercise. Journal of Applied Physiology 19, 613618.CrossRefGoogle ScholarPubMed
Hennig, J (1992) The application of phase rotation for localized in vivo proton spectroscopy with short echo times. Journal of Magnetic Resonance 96, 4049.Google Scholar
Herzog, RJ (1994) Efficacy of magnetic resonance imaging of the elbow. Medicine and Science in Sports and Exercise 26, 11931202.CrossRefGoogle ScholarPubMed
Heymsfield, SB, Gallagher, D, Visser, M, Nunez, C & Wang, ZM (1995) Measurement of skeletal muscle: laboratory and epidemiological methods. Journal of Gerontology 50, Special no., 2329.Google Scholar
Hoppeler, H, Lüthi, P, Claassen, H, Weibel, ER & Howald, H (1973) The ultrastructure of the normal human skeletal muscle. A morphometric analysis on untrained men, women, and well-trained orienteers. Pflügers Archiv 344, 217232.CrossRefGoogle ScholarPubMed
Hurley, BF, Nemeth, PM, Martin, WH, Hagberg, JM, Dalsky, GP & Holloszy, JO (1986) Muscle triglyceride utilization during exercise: effect of training. Journal of Applied Physiology 60, 562567.CrossRefGoogle ScholarPubMed
Kamber, M, Koster, M, Kreis, R, Walker, G, Boesch, C & Hoppeler, H (1999) Creatine supplementation and performance. Part I: Physical performance, clinical chemistry, and muscle volume. Medicine and Science in Sports and Exercise (In the Press).Google Scholar
Kiens, B, Essen-Gustavsson, B, Christensen, NJ & Saltin, B (1993) Skeletal muscle substrate utilization during submaximal exercise in man: effect of endurance training. Journal of Physiology 469, 459478.CrossRefGoogle ScholarPubMed
Kiens, B & Richter, EA (1998) Utilization of skeletal muscle triacylglycerol during postexercise recovery in humans. American Journal of Physiology 275, E332E337.Google ScholarPubMed
Kneeland, JP (1997) MR imaging of muscle and tendon injury. European Journal of Radiology 25, 198208.CrossRefGoogle ScholarPubMed
Kreis, R (1997) Quantitative localized 1H MR spectroscopy for clinical use. Progress in Nuclear Magnetic Resonance Spectroscopy 31, 155195.CrossRefGoogle Scholar
Kreis, R & Boesch, C (1994) Liquid-crystal-like structures of human muscle demonstrated by in vivo observation of direct dipolar coupling in localized proton magnetic resonance spectroscopy. Journal of Magnetic Resonance 104, 189192.Google Scholar
Kreis, R & Boesch, C (1996) Spatially localized, one- and two-dimensional NMR spectroscopy and in vivo application to human muscle. Journal of Magnetic Resonance 113, 103118.Google Scholar
Kreis, R, Ernst, T & Ross, BD (1993) Absolute quantitation of water and metabolites in the human brain. II. Metabolite concentrations. Journal of Magnetic Resonance 102B, 919.CrossRefGoogle Scholar
Kreis, R, Jung, B, Rotman, S, Slotboom, J & Boesch, C (1999) Non-invasive observation of acetyl-group buffering by 1H-MR spectroscopy in exercising human muscle. NMR in Biomedicine(In the Press).3.0.CO;2-A>CrossRefGoogle Scholar
Kreis, R, Koster, M, Kamber, M, Hoppeler, H & Boesch, C (1997) Peak assignment in localized 1H MR spectra of human muscle based on oral creatine supplementation. Magnetic Resonance in Medicine 37, 159163.CrossRefGoogle ScholarPubMed
Krssak, M, Petersen, KF, Bergeron, R, Price, T, Roden, M & Shulman, GI (1998) 13C and 1H NMR assessment of glycogen and intramyocellular lipid utilization during prolonged exercise and recovery in man. Proceedings of the International Society of Magnetic Resonance in Medicine Annual Meeting 1, 389 Abstr.Google Scholar
Krssak, M, Petersen, KF, Dresner, A, DiPietro, L, Vogel, SM, Rothman, DL, Shulman, GI & Roden, M (1999) Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study. Diabetologia 42, 113116.Google Scholar
LeBlanc, AD, Schneider, VS, Evans, HJ, Pientok, C, Rowe, R & Spector, E (1992) Regional changes in muscle mass following 17 weeks of bed rest. Journal of Applied Physiology 73, 21722178.Google Scholar
McColl, RW, Fleckenstein, JL, Bowers, J, Theriault, G & Peshock, RM (1992) Three-dimensional reconstruction of skeletal muscle from MRI. Computerized Medical Imaging and Graphics 16, 363371.CrossRefGoogle ScholarPubMed
McCully, KK & Posner, JD (1995) The application of blood flow measurements to the study of aging muscle. Journal of Gerontology 50, Special no., 130136.Google Scholar
Margaria, R, Cerretelli, P, Aghemo, P & Sassi, G (1963) Energy cost of running. Journal of Applied Physiology 18, 367370.CrossRefGoogle ScholarPubMed
Mendez, J & Keys, A (1960) Density and composition of mammalian muscle. Metabolism 9, 184188.Google Scholar
Narayana, PA, Hazle, JD, Jackson, EF, Fotedar, LK & Kulkarni, MV (1988) In vivo 1H spectroscopic studies of human gastrocnemius muscle at 1.5 T. Magnetic Resonance Imaging 6, 481485.CrossRefGoogle ScholarPubMed
Narici, MV, Landoni, L & Minetti, AE (1992) Assessment of human knee extensor muscles stress from in vivo physiological cross-sectional area and strength measurements. European Journal of Applied Physiology and Occupational Physiology 65, 438444.CrossRefGoogle ScholarPubMed
Ntziachristos, V, Kreis, R, Boesch, C & Quistorff, B (1997) Dipolar resonance frequency shifts in 1H-MR spectra of skeletal muscle: Confirmation in rats at 4.7 T in vivo and observation of changes post-mortem. Magnetic Resonance in Medicine 38, 3339.CrossRefGoogle Scholar
Oberholzer, F, Claassen, H, Moesch, H & Howald, H (1976) Ultrastrukturelle, biochemische und energetische Analyse einer extremen Dauerleistung (100 km-Lauf) (Ultrastructural, biochemical and energy analysis of extreme duration performance (100 km run)). Schweizerische Zeitschrift für Sportmedizin 2, 7198.Google Scholar
Pan, JW, Hamm, JR, Hetherington, HP, Rothman, DL & Shulman, RG (1991) Correlation of lactate and pH in human skeletal muscle after exercise by 1H NMR. Magnetic Resonance in Medicine 20, 5765.Google Scholar
Price, TB, Rothman, DL, Taylor, R, Avison, MJ, Shulman, GI & Shulman, RG (1994) Human muscle glycogen resynthesis after exercise: insulin-dependent and independent phases. Journal of Applied Physiology 76, 104111.Google Scholar
Rico-Sanz, J, Hajnal, JV, Thomas, EL, Mierisova, S, Ala-Korpela, M & Bell, JD (1998) Intracellular and extracellular skeletal muscle triglyceride metabolism during alternating intensity exercise in humans. Journal of Physiology 510, 615622.Google Scholar
Roberts, N, Cruz-Orive, LM, Reid, NMK, Brodie, DA, Bourne, M & Edwards, RHT (1993) Unbiased estimation of human body composition by the Cavalieri method using magnetic resonance imaging. Journal of Microscopy 171, 239253.CrossRefGoogle ScholarPubMed
Romijn, JA, Coyle, EF, Sidossis, LS, Gastaldelli, A, Horowitz, JF, Endert, E & Wolfe, RR (1993) Regulation of endogenous fat and carbohydrate metabolism in relation to exercise intensity and duration. American Journal of Physiology 265, E380E391.Google ScholarPubMed
Schick, F, Eismann, B, Jung, WI, Bongers, H, Bunse, M & Lutz, O (1993) Comparison of localized proton NMR signals of skeletal muscle and fat tissue in vivo: Two lipid compartments in muscle tissue. Magnetic Resonance in Medicine 29, 158167.CrossRefGoogle ScholarPubMed
Sjogaard, G & Saltin, B (1982) Extra- and intracellular water spaces in muscles of man at rest and with dynamic exercise. American Journal of Physiology 243, R271R280.Google Scholar
Slotboom, J, Boesch, C & Kreis, R (1998) Versatile frequency domain fitting using time domain models and prior knowledge. Magnetic Resonance in Medicine 39, 899911.CrossRefGoogle ScholarPubMed
Sonin, AH (1994) Magnetic resonance imaging of the extensor mechanism. Magnetic Resonance Imaging Clinics of North America 2, 401411.CrossRefGoogle ScholarPubMed
Starling, RD, Trappe, TA, Parcell, AC, Kerr, CG, Fink, WJ & Costill, DL (1997) Effects of diet on muscle triglyceride and endurance performance. Journal of Applied Physiology 82, 11851189.CrossRefGoogle ScholarPubMed
Staron, RS, Hikida, RR, Murray, TF, Hagerman, FC & Hagerman, MT (1989) Lipid depletion and repletion in skeletal muscle following marathon. Journal of the Neurological Sciences 94, 2940.Google Scholar
Stein, DT, Szczepaniak, I, Garg, A, Malloy, C & McGarry, JD (1997) Intramuscular lipid is increased in subjects with congenital generalized lipodystrophy. Diabetes 46, Suppl.1, 242A Abstr.Google Scholar
Stein, DT, Szczepaniak, LS, Dobbins, RL, Snell, P & McGarry, JD (1998) Skeletal muscle triglyceride stores are increased in insulin resistant states. Proceedings of the International Society of Magnetic Resonance in Medicine Annual Meeting 1, 388 Abstr.Google Scholar
Terk, MR & Kwong, PK (1994) Magnetic resonance imaging of the foot and ankle. Clinics in Sports Medicine 13, 883908.Google Scholar
Thomas, EL, Cunnane, SC & Bell, JD (1998) Critical assessment of in vivo 13C NMR spectroscopy and gas-liquid chromatography in the study of adipose tissue composition. NMR in Biomedicine 11, 290296.Google Scholar
Tung, GA & Brody, JM (1997) Contemporary imaging of athletic injuries. Clinics in Sports Medicine 16, 393417.Google Scholar
Vessby, B, Tengblad, S & Lithell, H (1994) Insulin sensitivity is related to the fatty acid composition of serum lipids and skeletal muscle phospholipids in 70-year-old men. Diabetologia 37, 10441050.Google Scholar
Vock, R, Hoppeler, H, Claassen, H, Wu, DXY, Weber, JM, Taylor, CR & Weibel, ER (1996) Design of the oxygen and substrate pathways. VI. Structural basis of intracellular substrate supply to mitochondria in muscle cell. Journal of Experimental Biology 199, 16891697.Google Scholar
Walker, CW & Moore, TE (1997) Imaging of skeletal and soft tissue injuries in and around the knee. Radiologic Clinics of North America 35, 631653.Google Scholar
Wary, C, Bloch, G, Jehenson, P & Carlier, PG (1996) C13 NMR spectroscopy of lipids: A simple method for absolute quantitation. Anticancer Research 16, 14791484.Google ScholarPubMed
Wendling, PS, Peters, SJ, Heigenhauser, GJ & Spriet, LL (1996) Variability of triacylglycerol content in human skeletal muscle biopsy samples. Journal of Applied Physiology 81, 11501155.CrossRefGoogle ScholarPubMed
Williams, SR, Gadian, DG, Proctor, E, Sprague, DB, Talbot, DF, Young, IR & Brown, FF (1985) Proton NMR studies of muscle metabolites in vivo. Journal of Magnetic Resonance 63, 406412.Google Scholar