Role of proton MR for the study of muscle lipid metabolism

NMR in Biomedicine

Volumn 19, Issue 7, 2006, Pages 968-988

  Boesch, Chris ^a   Machann, Juergen ^b   Vermathen, Peter ^a   Schick, Fritz ^b  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Intramyocellular; Lipids; Magnetic resonance imaging; Magnetic resonance spectroscopy; Methodology; Review; Skeletal muscle

Indexed keywords

CELLS; INSULIN; MAGNETIC RESONANCE IMAGING; METABOLISM; METABOLITES; MUSCLE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

HIGH-RESOLUTION SPECTROSCOPIC IMAGING; MULTINUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; MUSCLE LIPID METABOLISM; SKELETAL MUSCLE;

MEDICAL IMAGING;

LIPID;

BONE MARROW; CALIBRATION; CELL LEVEL; CONCENTRATION (PARAMETERS); CONCENTRATION RESPONSE; DIETARY INTAKE; EXERCISE; HUMAN; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID METABOLISM; MAGNETIC FIELD; MATHEMATICAL COMPUTING; METHODOLOGY; MUSCLE CELL; MUSCLE METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; HUMANS; LIPID METABOLISM; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MUSCLE CONTRACTION; MUSCLE, SKELETAL; PROTONS;

EID: 33751375983     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.1096     Document Type: Review

References (136)

1. Schick F, Eismann B, Jung WI, Bongers H, Bunse M, Lutz O. Comparison of localized proton NMR signals of skeletal muscle and fat tissue in vivo: two lipid compartments in muscle tissue. Magn. Reson. Med. 1993; 29: 158-167.
2. Boesch C, Slotboom H, Hoppeler H, Kreis R. In vivo determination of intra-myocellular lipids in human muscle by means of localized 1H-MR-spectroscopy. Magn. Reson. Med. 1997; 37: 484-493.
3. Kreis R, Boesch C. Spatially localized, one- and two-dimensional NMR spectroscopy and in vivo application to human muscle. J. Magn. Reson. Ser. B 1996; 113: 103-118.
4. Kreis R, Boesch C. Liquid-crystal-like structures of human muscle demonstrated by in vivo observation of direct dipolar coupling in localized proton magnetic resonance spectroscopy. J. Magn. Reson. Ser. B 1994; 104: 189-192.
5. Evanochko WT, Pohost GM. Structural studies of NMR detected lipids in myocardial ischemia. NMR Biomed. 1994; 7: 269-277.
6. Boesch C. Molecular aspects of magnetic resonance imaging and spectroscopy. Mol. Asp. Med. 1999; 20: 185-318.
7. Thomas EL, Cunnane SC, Bell JD. Critical assessment of in vivo 13C NMR spectroscopy and gas- liquid chromatography in the study of adipose tissue composition. NMR Biomed. 1998; 11: 290-296.
8. Moonen CT, Dimand RJ, Cox KL. The noninvasive determination of linoleic acid content of human adipose tissue by natural abundance carbon-13 nuclear magnetic resonance. Magn. Reson. Med. 1988; 6: 140-157.
9. 13C MRS at 1.5 T: clinical applications to dietary therapy. NMR Biomed. 2003; 16: 160-167.
10. Stein DT, Szczepaniak LS, Dobbins R, Malloy CR, McGarry JD. Skeletal muscle triglyceride stores are increased in insulin resistance. Diabetes 1997; 46 (Suppl. 1):23A.
11. Machann J, Schick F, Jacob S, Lutz O, Häring HU, Claussen CD. MR-spectroscopic determination of extra- and intramyocellular lipids in human calf muscle and correlation with insulin sensitivity. MAGMA 1998; 6 (Suppl. 1):220.
12. Jacob S, Machann J, Rett K, Brechtel K, Volk A, Renn W, Maerker E, Matthaei S, Schick F, Claussen CD, Haring HU. Association of increased intramyocellular lipid content with insulin resistance in lean nondiabetic offspring of type 2 diabetic subjects. Diabetes 1999; 48: 1113-1119.
13. Krssak M, Petersen KF, Dresner A, DiPietro L, Vogel SM, Rothman DL, Shulman GI, Roden M. Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study. Diabetologia 1999; 42: 113-116.
14. 13C nuclear magnetic resonance spectroscopy assessment in offspring of type 2 diabetic parents. Diabetes 1999; 48: 1600-1606.
15. Kelley DE, Goodpaster BH, Storlien L. Muscle triglyceride and insulin resistance. A. Rev. Nutr. 2002; 22: 325-346.
16. Boden G. Pathogenesis of type 2 diabetes. Insulin resistance. Endocrinol. Metab Clin. N. Am 2001; 30: 801-815.
17. 1H-magnetic resonance spectroscopy. Proc. Nutr Soc. 1999; 58: 841-850.
18. Machann J, Steidle G, Thamer C, Mader I, Schick F. In vivo proton NMR studies in skeletal muscle. A. Rep. NMR Spectrosc. 2003; 50: 1-74.
19. Machann J, Haring H, Schick F, Stumvoll M. Intramyocellular lipids; and insulin resistance. Diabetes Obes. Metab. 2004; 6: 239-248.
20. Decombaz J, Schmitt B, Ith M, Decarli B, Diem P, Kreis R, Hoppeler H, Boesch C. Post-exercise fat intake repletes intramyocellular lipids, but no faster in trained than in sedentary subjects. Am. J. Physiol. 2001; 281: R760-R769.
21. Goodpaster BH, He J, Watkins S, Kelley DE. Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes. J. Clin. Endocrinol. Metab. 2001; 86: 5755-5761.
22. Thamer C, Machann J, Bachmann O, Haap M, Dahl D, Wietek B, Tschritter O, Niess A, Brechtel K, Fritsche A, Claussen C, Jacob S, Schick F, Haring HU, Sturrivoll M. Intramyocellular lipids: anthropometric determinants and relationships with maximal aerobic capacity and insulin sensitivity. J. Clin. Endocrinol. Metab. 2003; 88: 1785-1791.
23. 2 relaxation times measurement of intramyocellular and extra-myocellular lipids in Zucker rats at 7 teslas. C. R. Chim. 2006; 9: 530-533.
24. Kuhlmann J, Neumann-Haefelin C, Belz U, Kramer W, Juretschke HP, Herling AW. Correlation between insulin resistance and intramyocellular lipid levels in rats. Magn. Reson. Med. 2005; 53: 1275-1282.
25. Jucker BM, Schaeffer TR, Haimbach RE, Mayer ME, Ohlstein DH, Smith SA, Cobitz AR, Sarkar SK. Reduction of intramyocellular lipid following short-term rosiglitazone treatment in Zucker fatty rats: an in vivo nuclear magnetic resonance study. Metabolism 2003; 52: 218-225.
26. Hockings PD, Changani KK, Saeed N, Reid DG, Birmingham J, O'Brien P, Osborne J, Toseland CN, Buckingham RE. Rapid reversal of hepatic steatosis, and reduction of muscle triglyceride, by rosiglitazone: MRI/S studies in Zucker fatty rats. Diabetes Obes. Metab. 2003; 5: 234-243.
27. Beha A, Juretschke HP, Kuhlmann J, Neumann-Haefelin C, Belz U, Gerl M, Kramer W, Roden M, Herling AW. Muscle type-specific fatty acid metabolism in insulin resistance: an integrated in vivo study in Zucker diabetic fatty rats. Am. J. Physiol. Endocrinol. Metab 2006; 290: E989-E997.
28. De Feyter HM, Schaart G, Hesselink MK, Schrauwen P, Nicolay K, Prompers JJ. Regional variations in intramyocellular lipid concentration correlate with muscle fiber type distribution in rat tibialis anterior muscle. Magn. Reson. Med. 2006; 56: 19-25.
29. Scheele K, Herzog W, Ritthaler G, Wirth A, Weicker H. Metabolic adaptation to prolonged exercise. Eur. J. Appl. Physiol. Occup. Physiol. 1979; 41: 101-108.
30. Callow M, Morton A, Guppy M. Marathon fatigue: the role of plasma fatty acids, muscle glycogen and blood glucose. Eur. J. Appl. Physiol. Occup. Physiol. 1986; 55: 654-661.
31. Hurley BF, Nemeth PM, Martin WH, Hagberg JM, Dalsky GP, Holloszy JO. Muscle triglyceride utilization during exercise: effect of training. J. Appl. Physiol. 1986; 60: 562-567.
32. Achten J, Gleeson M, Jeukendrup AE. Determination of the exercise intensity that elicits maximal fat oxidation. Med. Sci. Sports Exerc. 2002; 34: 92-97.
33. Howald H, Boesch C, Kreis R, Matter S, Billeter R, Essen-Gustavsson B, Hoppeler H. Content of intramyocellular lipids derived by electron microscopy, biochemical assays, and (1)H-MR spectroscopy. J. Appl. Physiol. 2002; 92: 2264-2272.
34. Brouns F, van der Vusse GJ. Utilization of lipids during exercise in human subjects: metabolic and dietary constraints. Br. J. Nutr. 1998; 79: 117-128.
35. Jeukendrup AE, Saris WHM, Wagenmakers AJ. Fat metabolism during exercise: A review. Part I: Fatty acid mobilization and muscle metabolism. Int. J. Sports Med. 1998; 19: 231-244.
36. Decombaz J, Fleith M, Hoppeler H, Kreis R, Boesch C. Effect of diet on the replenishment of intramyocellular lipids after exercise. Eur. J. Nutr. 2000; 39: 244-247.
37. 1H nuclear magnetic resonance spectroscopy study. J. Clin. Endocrinol. Metab. 2000; 85: 748-754.
38. Rico-Sanz J, Moosavi M, Thomas EL, McCarthy J, Courts GA, Saeed N, Bell JD. In vivo evaluation of the effects of continuous exercise on skeletal muscle triglycerides in trained humans. Lipids 2000; 35: 1313-1318.
39. 1H-MRS). Horm. Metab. Res. 2001; 33: 63-66.
40. Watt MJ, Heigenhauser GJ, Spriet LL. Intramuscular triacylglycerol utilization in human skeletal muscle during exercise: is there a controversy? J. Appl. Physiol. 2002; 93: 1185-1195.
41. Johnson NA, Stannard SR, Mehalski K, Trenell MI, Sachinwalla T, Thompson CH, Thompson MW. Intramyocellular triacylglycerol in prolonged cycling with high- and low-carbohydrate availability. J. Appl. Physiol. 2003; 94: 1365-1372.
42. Schmitt B, Fluck M, Decombaz J, Kreis R, Boesch C, Wittwer M, Graber F, Vogt M, Howald H, Hoppeler H. Transcriptional adaptations of lipid metabolism in tibialis anterior muscle of endurance-trained athletes. Physiol. Genomics 2003; 15: 148-157.
43. Smekal G, von Duvillard SP, Pokan R, Tschan H, Baron R, Hofmann P, Wonisch M, Bachl N. Effect of endurance training on muscle fat metabolism during prolonged exercise: agreements and disagreements. Nutrition 2003; 19: 891-900.
44. van Loon LJ, Schrauwen-Hinderling VB, Koopman R, Wagenmakers AJ, Hesselink MK, Schaart G, Kooi ME, Saris WH. Influence of prolonged endurance cycling and recovery diet on intramuscular triglyceride content in trained males. Am. J. Physiol. Endocrinol. Metab. 2003; 285: E804-E811.
45. White LJ, Robergs RA, Sibbitt WL Jr. Ferguson MA, McCoy S, Brooks WM. Effects of intermittent cycle exercise on intramyocellular lipid use and recovery. Lipids 2003; 38: 9-13.
46. White LJ, Ferguson MA, McCoy SC, Kim H. Intramyocellular lipid changes in men and women during aerobic exercise: a (1)H-magnetic resonance spectroscopy study. J. Clin. Endocrinol. Metab. 2003; 88: 5638-5643.
47. Lange KH. Fat metabolism in exercise - with special reference to training and growth hormone administration. Scand. J. Med Sci. Sports 2004; 14: 74-99.
48. van Loon LJ. Intramyocellular triacylglycerol as a substrate source during exercise. Proc. Nutr Soc. 2004; 63: 301-307.
49. Schrauwen-Hinderling VB, van Loon LJ, Koopman R, Nicolay K, Saris WH, Kooi ME. Intramyocellular lipid content is increased after exercise in nonexercising human skeletal muscle. J. Appl. Physiol. 2003; 95: 2328-2332.
50. Rico-Sanz J, Hajnal JV, Thomas EL, Mierisova S, Ala-Korpela M, Bell JD. Intracellular and extracellular skeletal muscle triglyceride metabolism during alternating intensity exercise in humans. J. Physiol. (Lond.) 1998; 510: 615-622.
51. 1H-magnetic resonance spectroscopy. Ann. NY Acad. Sci. 2000; 904: 25-31.
52. 1H NMR study. Am. J. Physiol. Endocrinol. Metab. 2002; 282: E95-E106.
53. Stettler R, Ith M, Acheson KJ, Decombaz J, Boesch C, Tappy L, Binnert C. Interaction between dietary lipids and physical inactivity on insulin sensitivity and on intramyocellular lipids in healthy men. Diabetes Care 2005; 28: 1404-1409.
54. Bachmann OP, Dahl DB, Brechtel K, Machann J, Haap M, Maier T, Loviscach M, Stumvoll M, Claussen CD, Schick F, Haring HU, Jacob S. Effects of intravenous and dietary lipid challenge on intramyocellular lipid content and the relation with insulin sensitivity in humans. Diabetes 2001; 50: 2579-2584.
55. Thamer C, Machann J, Tschritter O, Haap M, Wietek B, Dahl D, Bachmann O, Fritsche A, Jacob S, Stumvoll M, Schick F, Haring HU. Relationship between serum adiponectin concentration and intramyocellular lipid stores in humans. Horm. Metab Res. 2002; 34: 646-649.
56. Brechtel K, Dahl DB, Machann J, Bachmann OP, Wenzel I, Maier T, Claussen CD, Haring HU, Jacob S, Schick F. Fast elevation of the intramyocellular lipid content in the presence of circulating free fatty acids and hyperinsulinemia: a dynamic (1)H-MRS study. Magn. Reson. Med. 2001; 45: 179-183.
57. Boden G, Lebed B, Schatz M, Homko C, Lemieux S. Effects of acute changes of plasma free fatty acids on intramyocellular fat content and insulin resistance in healthy subjects. Diabetes 2001; 50: 1612-1617.
58. Krssak M, Krebs M, Stingl H, Mlynarik V, Gruber S, Moser E, Roden M. Intramyocellular Lipid (IMCL) stores before and after lipid infusion. Proc. Int. Soc. Magn. Reson. Med. 2000; 8: 1883.
59. Stannard SR, Thompson MW, Fairbairn K, Huard B, Sachinwalla T, Thompson CH. Fasting for 72 h increases intramyocellular lipid content in nondiabetic, physically fit men. Am. J. Physiol. Endocrinol. Metab. 2002; 283: E1185-E1191.
60. Wietek BM, Machann J, Mader I, Thamer C, Haring HU, Claussen CD, Stumvoll M, Schick F. Muscle type dependent increase in intramyocellular lipids during prolonged fasting of human subjects: a proton MRS study. Horm. Metab Res. 2004; 36: 639-644.
61. Schrauwen-Hinderling VB, Schrauwen P, Hesselink MK, van Engelshoven JM, Nicolay K, Saris WH, Kessels AG, Kooi ME. The increase in intramyocellular lipid content is a very early response to training. J. Clin. Endocrinol. Metab. 2003; 88: 1610-1616.
62. Fossum E, Hoieggen A, Moan A, Rostrup, M, Nordby G, Kjeldsen SE. Relationship between insulin sensitivity and maximal forearm blood flow in young men. Hypertension 1998; 32: 838-843.
63. Ward J, Ashley M, Kemp A, Buckley A, Baur LA, Thompson C. Preliminary report: skeletal muscle cell lipid and oxygen supply. Metabolism 2001; 50: 380-381.
64. Petersen KF, Befroy D, Dufour S, Dziura J, Ariyan C, Rothman DL, DiPietro L, Cline GW, Shulman GI. Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 2003; 300: 1140-1142.
65. Zehnder M, Ith M, Kreis R, Saris W, Boutellier U, Boesch C. Gender-specific usage of intramyocellular lipids and glycogen during exercise. Med. Sci. Sports Exerc. 2005; 37: 1517-1524.
66. Perseghin G, Scifo, P, Pagliato E, Battezzati A, Benedini S, Soldini L, Testolin G, Del Maschio A, Luzi L. Gender factors affect fatty acids-induced insulin resistance in nonobese humans: effects of oral steroidal contraception. J. Clin. Endocrinol. Metab. 2001; 86: 3188-3196.
67. Machann J, Thamer C, Schnoedt B, Stefan N, Stumvoll M, Haring HU, Claussen CD, Schick F, Fritsche A. Age and gender related effects on adipose tissue compartments of subjects with increased risk for type 2 diabetes: a whole body MRI/MRS study. MAGMA 2005; 18: 128-137.
68. Gan SK, Kriketos AD, Poynten AM, Furler SM, Thompson CH, Kraegen EW, Campbell LV, Chisholm DJ. Insulin action, regional fat, and myocyte lipid: altered relationships with increased adiposity. Obes. Res. 2003; 11: 1295-1305.
69. Vermathen P, Kreis R, Boesch C. Distribution of intra-myocellular lipids in human calf muscles determined by MR spectroscopic imaging. Magn. Reson. Med. 2004; 51: 253-262.
70. Vermathen P, Boesch C, Kreis R. Mapping fiber orientation in human muscle by proton MR spectroscopic imaging. Magn. Reson. Med. 2003; 49: 424-432.
71. 1H-MR spectra of skeletal muscle: Confirmation in rats at 4.7 T in vivo and observation of changes post-mortem. Magn. Reson. Med. 1997; 38: 33-39.
72. 1H-MR spectra of human muscle based on oral creatine supplementation. Magn. Reson. Med. 1997; 37: 159-163.
73. Boesch C, Kreis R. Dipolar coupling and ordering effects observed in magnetic resonance spectra of skeletal muscle. NMR Biomed. 2001; 14: 140-148.
74. in't Zandt HJ, Klomp DW, Oerlemans F, Wieringa B, Hilbers CW, Heerschap A. Proton MR spectroscopy of wild-type and creatine kinase deficient mouse skeletal muscle: dipole-dipole coupling effects and post-mortem changes. Magn. Reson. Med. 2000; 43: 517-524.
75. 1H NMR spectroscopy. J. Magn. Reson. 1999; 139: 213-224.
76. Asllani I, Shankland E, Pratum T, Kushmerick M. Effects of pH and molecular charge on dipolar coupling interactions of solutes in skeletal muscle observed by DQF, 1H NMR spectroscopy. J. Magn. Reson. 2003; 163: 124-132.
77. Hanstock CC, Thompson RB, Trump ME, Gheorghiu D, Hochachka PW, Allen PS. Residual dipolar coupling of the Cr/PCr methyl resonance in resting human medial gastrocnemius muscle. Magn. Reson. Med. 1999; 42: 421-424.
78. Hu J, Xia Y, Feng W, Xuan Y, Shen Y, Haacke EM, Jiang Q. Orientational dependence of trimethyl ammonium signal in human muscles by (1)H magnetic resonance spectroscopic imaging. Magn. Reson. Imag. 2005; 23: 97-104.
79. Szczepaniak LS, Dobbins RL, Stein DT, McGarry JD. Bulk magnetic susceptibility effects on the assessment of intra- and extramycellular lipids in vivo. Magn. Reson. Med. 2001; 47: 607-610.
80. Chu SCK, Balschi JA, Springer CS. Bulk magnetic susceptibility shifts in NMR studies of compartmentalized samples: use of paramagnetic reagents. Magn. Reson. Med. 1990; 13: 239-262.
81. Boesch C. How MRI and MRS can probe tissue microstructure far below the spatial dimensions of a voxel. (Editorial.) NMR Biomed. 2001; 14: 55-56.
82. Kreis R. Quantitative localized 1H MR spectroscopy for clinical use. Prog. NMR Spectrosc. 1997; 31: 155-195.
83. Barker PB, Sober BJ, Blackband SJ, Chatham JC, Mathews VP, Bryan RN. Quantitation of proton NMR spectra of the human brain using tissue water as an internal concentration reference. NMR Biomed. 1993; 6: 89-94.
84. Sjogaard G, Saltin B. Extra- and intracellular water spaces in muscles of man at rest and with dynamic exercise. Am. J. Physiol. 1982; 243: R271-280.
85. Mendez J, Keys A. Density and composition of mammalian muscle. Metabolism 1960; 9: 184-188.
86. Havel RJ, Carlson LA, Ekelund LG, Holmgren A. Turnover rate and oxidation of different free fatty acids in man during exercise. J. Appl. Physiol. 1964; 19: 613-618.
87. Andersson A, Sjodin A, Olsson R, Vessby B. Effects of physical exercise on phospholipid fatty acid composition in skeletal muscle. Am. J. Physiol. 1998; 274: E432-438.
88. Vessby B, Tengblad S, Lithell H. Insulin sensitivity is related to the fatty acid composition of serum lipids and skeletal muscle phospholipids in 70-year-old men. Diabetologia 1994; 37: 1044-1050.
89. CRC Handbook of Chemistry and Physics. CRC Press: Boca Raton, FL, 1993.
90. 2 relaxation of in vivo skeletal muscle. Magn. Reson. Med. 1999; 42: 150-157.
91. 2 relaxation decay of in vivo muscle. Magn. Reson. Med. 2001; 46: 592-599.
92. Duewell SH, Ceckler TL, Ong K, Wen H, Jaffer FA, Chesnick SA, Balaban RS. Musculoskeletal MR imaging at 4 T and at 1.5 T: comparison of relaxation times and image contrast. Radiology 1995; 196: 551-555.
93. Conley MS, Foley JM, Ploutz-Snyder LL, Meyer RA, Dudley GA. Effect of acute head-down tilt on skeletal muscle cross-sectional area and proton transverse relaxation time. J. Appl. Physiol. 1996; 81: 1572-1577.
94. 2 relaxation in skeletal muscle. Magn. Reson. Med. 1997; 37: 676-682.
95. Machann J, Schick F, Jacob S, Lutz O, Claussen CD. An interleaved sampling strategy for MR spectroscopy in vivo: applications on human calf musculature. Magn. Reson. Imag. 2000; 18: 189-197.
96. Kreis R, Ernst T, Ross BD. Absolute quantitation of water and metabolites in the human brain. II. Metabolite concentrations. J. Magn. Reson. Ser. B 1993; 102: 9-19.
97. 1H-MRSI measurements in human thigh muscles - measurements of metabolite distribution and fiber orientation and determination of reproducibility. Proc. Int. Soc. Magn. Reson. Med. 2005; 13: 62.
98. Hwang JH, Pan JW, Heydari S, Hetherington HP, Stein DT. Regional differences in intramyocellular lipids in humans observed by in vivo (1)H-MR spectroscopic imaging. J. Appl. Physiol. 2001; 90: 1267-1274.
99. Bottomley PA, Lee Y, Weiss RG. Total creatine in muscle: imaging and quantification with proton MR spectroscopy. Radiology 1997; 204: 403-410.
100. Kreis R, Kamber M, Koster M, Felblinger J, Slotboom J, Hoppeler H, Boesch C. Creatine supplementation - part II: in vivo magnetic resonance spectroscopy. Med. Sci. Sports Exerc. 1999; 31: 1770-1777.
101. Kamber M, Koster M, Kreis R, Walker G, Boesch C, Hoppeler H. Creatine supplementation-part I: performance, clinical chemistry, and muscle volume. Med. Sci. Sports Exerc. 1999; 31: 1763-1769.
102. 1H MR spectra of human skeletal muscle. J. Magn. Reson. 1999; 137: 350-357.
103. in't Zandt HJ, de Groof AJ, Renema WK, Oerlemans FT, Klomp DW, Wieringa B, Heerschap A. Presence of (phospho)creatine in developing and adult skeletal muscle of mice without mitochondrial and cytosolic muscle creatine kinase isoforms. J. Physiol. 2003; 548: 847-858.
104. 1H NMR relaxation times of skeletal muscle metabolites at 3 T. MAGMA 2004; 16: 155-159.
105. 1H MR spectroscopic imaging and validation by single voxel spectroscopy. Proc. Int. Soc. Magn. Reson. Med. 2003; 11: 1152.
106. Wendling PS, Peters SJ, Heigenhauser GJ, Spriet LL. Variability of triacylglycerol content in human skeletal muscle biopsy samples. J. Appl. Physiol. 1996; 81: 1150-1155.
107. Szczepaniak LS, Babcock EE, Schick F, Dobbins RL, Garg A, Burns DK, McGarry JD, Stein DT. Measurement of intracellular triglyceride stores by H spectroscopy: validation in vivo. Am. J. Physiol. 1999; 276: E977-E989.
108. 1H-magnetic resonance spectroscopy and a gallery of artifacts. NMR Biomed. 2004; 17: 361-381.
109. Haupt CI, Schuff N, Weiner MW, Maudsley AA. Removal of lipid artifacts in 1H spectroscopic imaging by data extrapolation. Magn. Reson. Med. 1996; 35: 678-687.
110. Slotboom J, Boesch C, Kreis R. Versatile frequency domain fitting using time domain models and prior knowledge. Magn. Reson. Med. 1998; 39: 899-911.
111. Vanhamme L, vandenBoogaart A, Van Huffel S. Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J. Magn. Reson. 1997; 129: 35-43.
112. Naressi A, Couturier C, Devos JM, Janssen M, Mangeat C, de Beer R, Graveron-Demilly D. Java-based graphical user interface for the MRUI quantitation package. MAGMA 2001; 12: 141-152.
113. 1H MR spectroscopy. Radiology 2005; 236: 609-614.
114. Skoch A, Jiru F, Dezortova M, Krusinova E, Kratochvilova S, Pelikanova T, Grodd W, Hajek M. Intramyocellular lipid quantification from 1H long echo time spectra at 1.5 and 3 T by means of the LCModel technique. J. Magn Reson. Imag. 2006; 23: 728-735.
115. Dong Z, Hwang JH. Lipid signal extraction by SLIM: application to 1H MR spectroscopic imaging of human calf muscles. Magn Reson. Med. 2006; 55: 1447-1453.
116. Steidle G, Machann J, Claussen CD, Schick F. Separation of intra- and extramyocellular lipid signals in proton MR spectra by determination of their magnetic field distribution. J. Magn. Reson. 2002; 154: 228-235.
117. Boesch C. Magnetic resonance spectroscopy: basic principles. In Clinical Magnetic Resonance Imaging, Edelman RR, Hesselink JR, Zlatkin MB, Crues JV (eds). Saunders: Philadelphia, PA, 2005.
118. Vermathen P, Schmid JP, Kreis R, Boesch C. Measurement of intra-myocellular lipids (IMCL) in obese subjects using magnetic resonance spectroscopic imaging (MRSI) - a feasibility study. MAGMA 2004; 16: 38.
119. Weis J, Courivaud F, Hansen MS, Johansson L, Ribe LR, Ahistrom H. Lipid content in the musculature of the lower leg: evaluation with high-resolution spectroscopic imaging. Magn. Reson. Med. 2005; 54: 152-158.
120. 1 field inhomogeneities. Magn. Reson. Med 1997; 38: 269-274.
121. Brechtel K, Jacob S, Machann J, Hauer B, Nielsen M, Meissner HP, Matthaei S, Haering HU, Claussen CD, Schick F. Acquired generalized lipoatrophy (AGL): highly selective MR lipid imaging and localized (1)H-MRS. J. Magn. Reson. Imag. 2000; 12: 306-310.
122. Schick F, Machann J, Brechtel K, Strempfer A, Klumpp B, Stein DT, Jacob S. MRI of muscular fat. Magn. Reson. Med. 2002; 47: 720-727.
123. Machann J, Bachmann OP, Brechtel K, Dahl DB, Wictek B, Klumpp B, Haring HU, Claussen CD, Jacob S, Schick F. Lipid content in the musculature of the lower leg assessed by fat selective MRI: intra- and interindividual differences and correlation with anthropometric and metabolic data. J. Magn. Reson. Imag. 2003; 17: 350-357.
124. Braun M, Jung WI, Lutz O, Oeschey R. Magnetic field mapping and NMR imaging by multi-frequency SENEX. Z. Naturf. 1988; 43a: 291-296.
125. Goodpaster BH. Measuring body fat distribution and content in humans. Curr. Opin. Clin. Nutr. Metab Care 2002; 5: 481-487.
126. Ross R. Advances in the application of imaging methods in applied and clinical physiology. Acta Diabetol. 2003; 40(Suppl. 1): S45-S50.
127. Kelley DE, Goodpaster BH. Skeletal muscle triglyceride. An aspect of regional adiposity and insulin resistance. Diabetes Care 2001; 24: 933-941.
128. Shen W, Wang Z, Punyanita M, Lei J, Sinav A, Kral JG, Imielinska C, Ross R, Heymsfield SB. Adipose tissue quantification by imaging methods: a proposed classification. Obes. Res. 2003; 11: 5-16.
129. Pietrobelli A, Tato L. Body composition measurements: from the past to the future. Acta Paediatr. Suppl. 2005; 94: 8-13.
130. Boesch C, Kreis R. Imaging and spectroscopy of muscle. In: Methods in Biomedical Magnetic Resonance Imaging and Spectroscopy (Encyclopedia of Nuclear Magnetic Resonance), Young IR, Grant DM, Harris RK (eds). Wiley: Chichester, 2000.
131. Roden M, Price TB, Perseghin G, Petersen KF, Rothman DL, Cline GW, Shulman GI. Mechanism of free fatty acid-induced insulin resistance in humans. J. Clin. Invest. 1996; 97: 2859-2865.
132. Cline GW, Petersen KF, Krssak M, Shen J, Hundal RS, Trajanoski Z, Inzucchi S, Dresner A, Rothman DL, Shulman GI. Impaired glucose transport as a cause of decreased insulin-stimulated muscle glycogen synthesis in type 2 diabetes. New Engl. J. Med. 1999; 341: 240-246.
133. Cline GW, Magnusson I, Rothman DL, Petersen KF, Laurent D, Shulman GI. Mechanism of impaired insulin-stimulated muscle glucose metabolism in subjects with insulin-dependent diabetes mellitus. J. Clin. Invest. 1997; 99: 2219-2224.
134. 31P NMR studies of glucose transport in human skeletal muscle. Proc. Natl Acad. Sci. USA 1998; 95: 1313-1318.
135. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI. Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. New Engl. J. Med 2004; 350: 664-671.
136. Brehm A, Krssak M, Schmid AI, Nowomy P, Waldhausl W, Roden M. Increased lipid availability impairs insulin-stimulated ATP synthesis in human skeletal muscle. Diabetes 2006; 55: 136-140.