Biochemical and Physiological MR Imaging of Skeletal Muscle at 7 Tesla and Above

 

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ABSTRACT

Ultra-high field (UHF; ≥7 T) magnetic resonance imaging (MRI), with its greater signal-to-noise ratio, offers the potential for increased spatial resolution, faster scanning, and, above all, improved biochemical and physiological imaging of skeletal muscle. The increased spectral resolution and greater sensitivity to low-gamma nuclei available at UHF should allow techniques such as ¹H MR spectroscopy (MRS), ³¹P MRS, and ²³Na MRI to be more easily implemented. Numerous technical challenges exist in the performance of UHF MRI, including changes in relaxation values, increased chemical shift and susceptibility artifact, radiofrequency (RF) coil design/B₁ ⁺ field inhomogeneity, and greater RF energy deposition. Nevertheless, the possibility of improved functional and metabolic imaging at UHF will likely drive research efforts in the near future to overcome these challenges and allow studies of human skeletal muscle physiology and pathophysiology to be possible at ≥7 T.

REFERENCES

• 1 Prompers J J, Jeneson J A, Drost M R, Oomens C C, Strijkers G J, Nicolay K. Dynamic MRS and MRI of skeletal muscle function and biomechanics.  NMR Biomed. 2006;  19(7) 927-953
  CrossrefPubMedGoogle Scholar
• 2 Carlier P G, Bertoldi D, Baligand C, Wary C, Fromes Y. Muscle blood flow and oxygenation measured by NMR imaging and spectroscopy.  NMR Biomed. 2006;  19(7) 954-967
  CrossrefPubMedGoogle Scholar
• 3 Boesch C, Machann J, Vermathen P, Schick F. Role of proton MR for the study of muscle lipid metabolism.  NMR Biomed. 2006;  19(7) 968-988
  CrossrefPubMedGoogle Scholar
• 4 Boesch C. Musculoskeletal spectroscopy.  J Magn Reson Imaging. 2007;  25(2) 321-338
  CrossrefPubMedGoogle Scholar
• 5 Regatte R R, Schweitzer M E. Ultra-high-field MRI of the musculoskeletal system at 7.0T.  J Magn Reson Imaging. 2007;  25(2) 262-269
  CrossrefPubMedGoogle Scholar
• 6 Krug R, Stehling C, Kelley D A, Majumdar S, Link T M. Imaging of the musculoskeletal system in vivo using ultra-high field magnetic resonance at 7 T.  Invest Radiol. 2009;  44(9) 613-618
  CrossrefPubMedGoogle Scholar
• 7 Hoult D I, Lauterbur P C. The sensitivity of the zeugmatographic experiment involving human samples.  J Magn Reson. 1979;  34 425-433
  PubMedGoogle Scholar
• 8 Collins C M. Radiofrequency field calculations for high field MRI. In: Robitaille PM, Berliner LJ Ultra High Field Magnetic Resonance Imaging. New York, NY; Springer 2006: 209-248
  PubMedGoogle Scholar
• 9 Bottomley P A, Foster T H, Argersinger R E, Pfeifer L M. A review of normal tissue hydrogen NMR relaxation times and relaxation mechanisms from 1-100 MHz: dependence on tissue type, NMR frequency, temperature, species, excision, and age.  Med Phys. 1984;  11(4) 425-448
  CrossrefPubMedGoogle Scholar
• 10 Pruessmann K P. Parallel imaging at high field strength: synergies and joint potential.  Top Magn Reson Imaging. 2004;  15(4) 237-244
  CrossrefPubMedGoogle Scholar
• 11 Schmitt F, Potthast A, Stoeckel B et al.. Aspect of clinical imaging at 7T. In: Robitaille PM, Berliner LJ Ultra High Field Magnetic Resonance Imaging. New York, NY; Springer 2006: 59-103
  PubMedGoogle Scholar
• 12 Ibrahim T S, Lee R, Baertlein B A, Kangarlu A, Robitaille P L. Application of finite difference time domain method for the design of birdcage RF head coils using multi-port excitations.  Magn Reson Imaging. 2000;  18(6) 733-742
  CrossrefPubMedGoogle Scholar
• 13 Vaughan J T, Garwood M, Collins C M et al.. 7T vs. 4T: RF power, homogeneity, and signal-to-noise comparison in head images.  Magn Reson Med. 2001;  46(1) 24-30
  CrossrefPubMedGoogle Scholar
• 14 Wei Q, Liu F, Xia L, Crozier S. An object-oriented designed finite-difference time-domain simulator for electromagnetic analysis and design in MRI—applications to high field analyses.  J Magn Reson. 2005;  172 222-230
  CrossrefPubMedGoogle Scholar
• 15 Beck B L, Jenkins K, Caserta J, Padgett K, Fitzsimmons J, Blackband S J. Observation of significant signal voids in images of large biological samples at 11.1 T.  Magn Reson Med. 2004;  51(6) 1103-1107
  CrossrefPubMedGoogle Scholar
• 16 Collins C M, Smith M B. Signal-to-noise ratio and absorbed power as functions of main magnetic field strength, and definition of “90 degrees ” RF pulse for the head in the birdcage coil.  Magn Reson Med. 2001;  45(4) 684-691
  CrossrefPubMedGoogle Scholar
• 17 Ibrahim T S. A numerical analysis of radiofrequency power requirements in magnetic resonance imaging experiments.  IEEE Trans Microw Theory Tech. 2004;  52(8) 1999-2003
  CrossrefPubMedGoogle Scholar
• 18 Hetherington H P, Hamm J R, Pan J W, Rothman D L, Shulman R G. A fully localized 1H homonuclear editing sequence to observe lactate in human skeletal muscle after exercise.  J Magn Reson. 1989;  82 86-96
  PubMedGoogle Scholar
• 19 Pan J W, Hamm J R, Hetherington H P, Rothman D L, Shulman R G. Correlation of lactate and pH in human skeletal muscle after exercise by 1H NMR.  Magn Reson Med. 1991;  20(1) 57-65
  CrossrefPubMedGoogle Scholar
• 20 Jouvensal L, Carlier P G, Bloch G. Practical implementation of single-voxel double-quantum editing on a whole-body NMR spectrometer: localized monitoring of lactate in the human leg during and after exercise.  Magn Reson Med. 1996;  36(3) 487-490
  CrossrefPubMedGoogle Scholar
• 21 Brillault-Salvat C, Giacomini E, Wary C et al.. An interleaved heteronuclear NMRI-NMRS approach to non-invasive investigation of exercising human skeletal muscle.  Cell Mol Biol (Noisy-le-grand). 1997;  43(5) 751-762
  PubMedGoogle Scholar
• 22 Brault J J, Towse T F, Slade J M, Meyer R A. Parallel increases in phosphocreatine and total creatine in human vastus lateralis muscle during creatine supplementation.  Int J Sport Nutr Exerc Metab. 2007;  17(6) 624-634
  PubMedGoogle Scholar
• 23 Wang Z Y, Noyszewski E A, Leigh Jr J S. In vivo MRS measurement of deoxymyoglobin in human forearms.  Magn Reson Med. 1990;  14(3) 562-567
  CrossrefPubMedGoogle Scholar
• 24 Kruiskamp M J, De Vilder S J, De Graaf R A, Nicolay K. 31P/ and 1H/MRS measurements of metabolite diffusion in rat and mouse hindleg skeletal muscle.  Proc ISMRM. 1999;  7 697
  PubMedGoogle Scholar
• 25 Decombaz J, Schmitt B, Ith M et al.. Postexercise fat intake repletes intramyocellular lipids but no faster in trained than in sedentary subjects.  Am J Physiol Regul Integr Comp Physiol. 2001;  281 R760-R769
  PubMedGoogle Scholar
• 26 Thamer C, Machann J, Bachmann O et al.. Intramyocellular lipids: anthropometric determinants and relationships with maximal aerobic capacity and insulin sensitivity.  J Clin Endocrinol Metab. 2003;  88(4) 1785-1791
  CrossrefPubMedGoogle Scholar
• 27 Goodpaster B H, He J, Watkins S, Kelley D E. Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes.  J Clin Endocrinol Metab. 2001;  86(12) 5755-5761
  CrossrefPubMedGoogle Scholar
• 28 Wang L, Salibi N, Wu Y, Schweitzer M E, Regatte R R. Relaxation times of skeletal muscle metabolites at 7T.  J Magn Reson Imaging. 2009;  29(6) 1457-1464
  CrossrefPubMedGoogle Scholar
• 29 Khuu A, Ren J, Dimitrov I et al.. Orientation of lipid strands in the extracellular compartment of muscle: effect on quantitation of intramyocellular lipids.  Magn Reson Med. 2009;  61(1) 16-21
  CrossrefPubMedGoogle Scholar
• 30 Versluis M J, Kan H E, van Buchem M A, Webb A G. Improved signal to noise in proton spectroscopy of the human calf muscle at 7 T using localized B1 calibration.  Magn Reson Med. 2010;  63(1) 207-211
  PubMedGoogle Scholar
• 31 Fissoune R, Janier M, Briguet A, Hiba B. In vivo assessment of mouse hindleg intramyocellular lipids by 1H-MR spectroscopy.  Acad Radiol. 2009;  16(7) 890-896
  CrossrefPubMedGoogle Scholar
• 32 Fleckenstein J L, Canby R C, Parkey R W, Peshock R M. Acute effects of exercise on MR imaging of skeletal muscle in normal volunteers.  AJR Am J Roentgenol. 1988;  151(2) 231-237
  PubMedGoogle Scholar
• 33 Patten C, Meyer R A, Fleckenstein J L. T2 mapping of muscle.  Semin Musculoskelet Radiol. 2003;  7(4) 297-305
  Article in Thieme ConnectPubMedGoogle Scholar
• 34 Damon B M, Gregory C D, Hall K L, Stark H J, Gulani V, Dawson M J. Intracellular acidification and volume increases explain R(2) decreases in exercising muscle.  Magn Reson Med. 2002;  47(1) 14-23
  CrossrefPubMedGoogle Scholar
• 35 Saab G, Thompson R T, Marsh G D. Effects of exercise on muscle transverse relaxation determined by MR imaging and in vivo relaxometry.  J Appl Physiol. 2000;  88(1) 226-233
  PubMedGoogle Scholar
• 36 Ploutz-Snyder L L, Nyren S, Cooper T G, Potchen E J, Meyer R A. Different effects of exercise and edema on T2 relaxation in skeletal muscle.  Magn Reson Med. 1997;  37(5) 676-682
  CrossrefPubMedGoogle Scholar
• 37 Du J, Hamilton G, Takahashi A, Bydder M, Chung C B. Ultrashort echo time spectroscopic imaging (UTESI) of cortical bone.  Magn Reson Med. 2007;  58(5) 1001-1009
  CrossrefPubMedGoogle Scholar
• 38 Techawiboonwong A, Song H K, Leonard M B, Wehrli F W. Cortical bone water: in vivo quantification with ultrashort echo-time MR imaging.  Radiology. 2008;  248(3) 824-833
  CrossrefPubMedGoogle Scholar
• 39 Du J, Chiang A JT, Chung C B et al.. Orientational analysis of Achilles tendon and enthesis using an ultrashort echo time spectroscopic imaging sequence.  Magn Reson Imaging. 2010;  28(2) 178-184
  CrossrefPubMedGoogle Scholar
• 40 Oatridge A, Herlihy A H, Thomas R W et al.. Magnetic resonance: magic angle imaging of the Achilles tendon.  Lancet. 2001;  358(9293) 1610-1611
  CrossrefPubMedGoogle Scholar
• 41 Borthakur A, Mellon E, Niyogi S, Witschey W, Kneeland J B, Reddy R. Sodium and T1rho MRI for molecular and diagnostic imaging of articular cartilage.  NMR Biomed. 2006;  19(7) 781-821
  CrossrefPubMedGoogle Scholar
• 42 Constantinides C D, Gillen J S, Boada F E, Pomper M G, Bottomley P A. Human skeletal muscle: sodium MR imaging and quantification-potential applications in exercise and disease.  Radiology. 2000;  216(2) 559-568
  CrossrefPubMedGoogle Scholar
• 43 Bansal N, Szczepaniak L, Ternullo D, Fleckenstein J L, Malloy C R. Effect of exercise on (23)Na MRI and relaxation characteristics of the human calf muscle.  J Magn Reson Imaging. 2000;  11(5) 532-538
  CrossrefPubMedGoogle Scholar
• 44 Weber M A, Nielles-Vallespin S, Huttner H B et al.. Evaluation of patients with paramyotonia at 23Na MR imaging during cold-induced weakness.  Radiology. 2006;  240(2) 489-500
  CrossrefPubMedGoogle Scholar
• 45 Nielles-Vallespin S, Weber M A, Bock M et al.. 3D radial projection technique with ultrashort echo times for sodium MRI: clinical applications in human brain and skeletal muscle.  Magn Reson Med. 2007;  57(1) 74-81
  CrossrefPubMedGoogle Scholar
• 46 Park J H, Brown R L, Park C R et al.. Functional pools of oxidative and glycolytic fibers in human muscle observed by 31P magnetic resonance spectroscopy during exercise.  Proc Natl Acad Sci U S A. 1987;  84 8976-8980
  CrossrefPubMedGoogle Scholar
• 47 McCully K K, Boden B P, Tuchler M, Fountain M R, Chance B. Wrist flexor muscles of elite rowers measured with magnetic resonance spectroscopy.  J Appl Physiol. 1989;  67(3) 926-932
  PubMedGoogle Scholar
• 48 Minotti J R, Johnson E C, Hudson T L et al.. Training-induced skeletal muscle adaptations are independent of systemic adaptations.  J Appl Physiol. 1990;  68(1) 289-294
  PubMedGoogle Scholar
• 49 Yoshida T, Watari H. Metabolic consequences of repeated exercise in long distance runners.  Eur J Appl Physiol Occup Physiol. 1993;  67 261-265
  CrossrefPubMedGoogle Scholar
• 50 Ross B D, Radda G K, Gadian D G, Rocker G, Esiri M, Falconer-Smith J. Examination of a case of suspected McArdle's syndrome by 31P nuclear magnetic resonance.  N Engl J Med. 1981;  304(22) 1338-1342
  CrossrefPubMedGoogle Scholar
• 51 Gruetter R, Kaelin P, Boesch C, Martin E, Werner B. Non-invasive 31P magnetic resonance spectroscopy revealed McArdle disease in an asymptomatic child.  Eur J Pediatr. 1990;  149(7) 483-486
  CrossrefPubMedGoogle Scholar
• 52 de Kerviler E, Leroy-Willig A, Jehenson P, Duboc D, Eymard B, Syrota A. Exercise-induced muscle modifications: study of healthy subjects and patients with metabolic myopathies with MR imaging and P-31 spectroscopy.  Radiology. 1991;  181(1) 259-264
  PubMedGoogle Scholar
• 53 Zange J, Grehl T, Disselhorst-Klug C et al.. Breakdown of adenine nucleotide pool in fatiguing skeletal muscle in McArdle's disease: a noninvasive 31P-MRS and EMG study.  Muscle Nerve. 2003;  27(6) 728-736
  CrossrefPubMedGoogle Scholar
• 54 Vorgerd M, Zange J. Carbohydrate oxidation disorders of skeletal muscle.  Curr Opin Clin Nutr Metab Care. 2002;  5(6) 611-617
  CrossrefPubMedGoogle Scholar
• 55 Chance B, Eleff S, Bank W, Leigh Jr J S, Warnell R. 31P NMR studies of control of mitochondrial function in phosphofructokinase-deficient human skeletal muscle.  Proc Natl Acad Sci U S A. 1982;  79(24) 7714-7718
  CrossrefPubMedGoogle Scholar
• 56 Edwards R HT, Dawson M J, Wilkie D R, Gordon R E, Shaw D. Clinical use of nuclear magnetic resonance in the investigation of myopathy.  Lancet. 1982;  1(8274) 725-731
  PubMedGoogle Scholar
• 57 Vissing J, Vissing S F, MacLean D A, Saltin B, Quistorff B, Haller R G. Sympathetic activation in exercise is not dependent on muscle acidosis. Direct evidence from studies in metabolic myopathies.  J Clin Invest. 1998;  101(8) 1654-1660
  CrossrefPubMedGoogle Scholar
• 58 Taivassalo T, De Stefano N, Argov Z et al.. Effects of aerobic training in patients with mitochondrial myopathies.  Neurology. 1998;  50(4) 1055-1060
  PubMedGoogle Scholar
• 59 Kuhl C K, Layer G, Träber F, Zierz S, Block W, Reiser M. Mitochondrial encephalomyopathy: correlation of P-31 exercise MR spectroscopy with clinical findings.  Radiology. 1994;  192(1) 223-230
  CrossrefPubMedGoogle Scholar
• 60 Schunk K, Romaneehsen B, Rieker O et al.. Dynamic phosphorus-31 magnetic resonance spectroscopy in arterial occlusive disease: effects of vascular therapy on spectroscopic results.  Invest Radiol. 1998;  33(6) 329-335
  CrossrefPubMedGoogle Scholar
• 61 Kemp G J, Hands L J, Ramaswami G et al.. Calf muscle mitochondrial and glycogenolytic ATP synthesis in patients with claudication due to peripheral vascular disease analysed using 31P magnetic resonance spectroscopy.  Clin Sci (Lond). 1995;  89(6) 581-590
  PubMedGoogle Scholar
• 62 Scheuermann-Freestone M, Madsen P L, Manners D et al.. Abnormal cardiac and skeletal muscle energy metabolism in patients with type 2 diabetes.  Circulation. 2003;  107(24) 3040-3046
  CrossrefPubMedGoogle Scholar
• 63 Petersen K F, Befroy D, Dufour S et al.. Mitochondrial dysfunction in the elderly: possible role in insulin resistance.  Science. 2003;  300(5622) 1140-1142
  CrossrefPubMedGoogle Scholar
• 64 Kent-Braun J A, Ng A V, Doyle J W, Towse T F. Human skeletal muscle responses vary with age and gender during fatigue due to incremental isometric exercise.  J Appl Physiol. 2002;  93(5) 1813-1823
  PubMedGoogle Scholar
• 65 Horská A, Fishbein K W, Fleg J L, Spencer R G. The relationship between creatine kinase kinetics and exercise intensity in human forearm is unchanged by age.  Am J Physiol Endocrinol Metab. 2000;  279(2) E333-E339
  PubMedGoogle Scholar
• 66 Bogner W, Chmelik M, Schmid A I, Moser E, Trattnig S, Gruber S. Assessment of (31)P relaxation times in the human calf muscle: a comparison between 3 T and 7 T in vivo.  Magn Reson Med. 2009;  62(3) 574-582
  CrossrefPubMedGoogle Scholar
• 67 Duong T Q, Yacoub E, Adriany G et al.. High-resolution, spin-echo BOLD, and CBF fMRI at 4 and 7 T.  Magn Reson Med. 2002;  48(4) 589-593
  CrossrefPubMedGoogle Scholar
• 68 Yacoub E, Van De Moortele P F, Shmuel A, Uğurbil K. Signal and noise characteristics of Hahn SE and GE BOLD fMRI at 7 T in humans.  Neuroimage. 2005;  24(3) 738-750
  CrossrefPubMedGoogle Scholar

Gregory ChangM.D. 

Department of Radiology, Center for Biomedical Imaging, New York University School of Medicine

660 First Ave., New York, NY 10016

Email: gregory.chang@nyumc.org