Advanced MR Imaging Techniques for Skeletal Muscle Evaluation

 

 Buy Article Permissions and Reprints

ABSTRACT

Diagnostic imaging procedures for muscle evaluation have typically provided basic information concerning gross anatomical change resulting from pathology. Up until recently the musculoskeletal radiologist has been fairly limited to using simple proton-density weighted fat-saturated and short tau inversion recovery magnetic resonance imaging scans for assessment of skeletal muscle. Recent advances, however, have resulted in development of newer scans and postprocessing methods that provide much more than gross muscle structure. Scans providing fine structure, muscle function, and metabolism can easily be done using clinical scanners. Here we describe how diffusion tensor imaging (DTI) and blood oxygenation level-dependent (BOLD) imaging together can provide detailed information on muscle structural and functional changes. DTI is useful for visualizing muscle tears, and BOLD can be used for vascular insufficiency (e.g., compartment syndrome). In clinical sites that are gaining experience using these techniques, imaging of muscle pathology is becoming increasingly thorough. In the future, these methods will reduce the need for invasive approaches to study muscle pathology.

REFERENCES

• 1 Arnold D L, Matthews P M, Radda G K. Metabolic recovery after exercise and the assessment of mitochondrial function in vivo in human skeletal muscle by means of 31P NMR.  Magn Reson Med. 1984;  1(3) 307-315
  CrossrefPubMedGoogle Scholar
• 2 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
• 3 Wells G D, Noseworthy M D, Hamilton J, Tarnopolski M, Tein I. Skeletal muscle metabolic dysfunction in obesity and metabolic syndrome.  Can J Neurol Sci. 2008;  35(1) 31-40
  PubMedGoogle Scholar
• 4 Stejskal E O, Tanner J E. Spin diffusion measurements: spin echoes in the presence of a time-dependent field gradient.  J Chem Phys. 1965;  42 288-292
  CrossrefPubMedGoogle Scholar
• 5 Wesbey G E, Moseley M E, Ehman R L. Translational molecular self-diffusion in magnetic resonance imaging. I. Effects on observed spin-spin relaxation.  Invest Radiol. 1984;  19(6) 484-490
  CrossrefPubMedGoogle Scholar
• 6 Wesbey G E, Moseley M E, Ehman R L. Translational molecular self-diffusion in magnetic resonance imaging. II. Measurement of the self-diffusion coefficient.  Invest Radiol. 1984;  19(6) 491-498
  CrossrefPubMedGoogle Scholar
• 7 Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M. MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders.  Radiology. 1986;  161(2) 401-407
  CrossrefPubMedGoogle Scholar
• 8 Bells S, Noseworthy M D. Effects of Gd bolus on DTI measurements in skeletal muscle. Paper presented at: International Society for Magnetic Resonance in Medicine (ISMRM) May 2006 Seattle WA;
  PubMedGoogle Scholar
• 9 Saupe N, White L M, Stainsby J, Tomlinson G, Sussman M S. Diffusion tensor imaging and fiber tractography of skeletal muscle: optimization of B value for imaging at 1.5 T.  AJR Am J Roentgenol. 2009;  192(6) W282–290
  PubMedGoogle Scholar
• 10 Saupe N, White L M, Sussman M S, Kassner A, Tomlinson G, Noseworthy M D. Diffusion tensor magnetic resonance imaging of the human calf: comparison between 1.5 T and 3.0 T—preliminary results.  Invest Radiol. 2008;  43(9) 612-618
  CrossrefPubMedGoogle Scholar
• 11 Galbán C J, Maderwald S, Uffmann K, de Greiff A, Ladd M E. Diffusive sensitivity to muscle architecture: a magnetic resonance diffusion tensor imaging study of the human calf.  Eur J Appl Physiol. 2004;  93(3) 253-262
  CrossrefPubMedGoogle Scholar
• 12 Zaraiskaya T, Kumbhare D, Noseworthy M D. Diffusion tensor imaging in evaluation of human skeletal muscle injury.  J Magn Reson Imaging. 2006;  24(2) 402-408
  CrossrefPubMedGoogle Scholar
• 13 Pajevic S, Pierpaoli C. Color schemes to represent the orientation of anisotropic tissues from diffusion tensor data: application to white matter fiber tract mapping in the human brain.  Magn Reson Med. 1999;  42(3) 526-540
  CrossrefPubMedGoogle Scholar
• 14 Le Bihan D, Mangin J F, Poupon C et al.. Diffusion tensor imaging: concepts and applications.  J Magn Reson Imaging. 2001;  13(4) 534-546
  CrossrefPubMedGoogle Scholar
• 15 Bammer R, Acar B, Moseley M E. In vivo MR tractography using diffusion imaging.  Eur J Radiol. 2003;  45(3) 223-234
  CrossrefPubMedGoogle Scholar
• 16 Lori N F, Akbudak E, Shimony J S et al.. Diffusion tensor fiber tracking of human brain connectivity: acquisition methods, reliability analysis and biological results.  NMR Biomed. 2002;  15(7-8) 494-515
  CrossrefPubMedGoogle Scholar
• 17 Damon B M, Ding Z, Anderson A W, Freyer A S, Gore J C. Validation of diffusion tensor MRI-based muscle fiber tracking.  Magn Reson Med. 2002;  48(1) 97-104
  CrossrefPubMedGoogle Scholar
• 18 Lansdown D A, Ding Z, Wadington M, Hornberger J L, Damon B M. Quantitative diffusion tensor MRI-based fiber tracking of human skeletal muscle.  J Appl Physiol. 2007;  103(2) 673-681
  CrossrefPubMedGoogle Scholar
• 19 Gaige T A, Benner T, Wang R, Wedeen V J, Gilbert R J. Three dimensional myoarchitecture of the human tongue determined in vivo by diffusion tensor imaging with tractography.  J Magn Reson Imaging. 2007;  26(3) 654-661
  CrossrefPubMedGoogle Scholar
• 20 Jiang H, van Zijl P C, Kim J, Pearlson G D, Mori S. DtiStudio: resource program for diffusion tensor computation and fiber bundle tracking.  Comput Methods Programs Biomed. 2006;  81(2) 106-116
  CrossrefPubMedGoogle Scholar
• 21 Cox R W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages.  Comput Biomed Res. 1996;  29(3) 162-173
  CrossrefPubMedGoogle Scholar
• 22 Smith S M, Jenkinson M, Woolrich M W et al.. Advances in functional and structural MR image analysis and implementation as FSL.  Neuroimage. 2004;  23(suppl 1) S208-S219
  CrossrefPubMedGoogle Scholar
• 23 Wang R, Wedeen V J. Diffusion Toolkit and TrackVis. Berlin, Germany, Proc Intl Soc Mag Reson Med 2007 Available at http://www.trackvis.org Martinos Center for Biomedical Imaging, Massachusetts General Hospital;
  PubMedGoogle Scholar
• 24 Sherbondy A, Akers D, Mackenzie R, Dougherty R, Wandell B. Exploring connectivity of the brain's white matter with dynamic queries.  IEEE Trans Vis Comput Graph. 2005;  11(4) 419-430
  CrossrefPubMedGoogle Scholar
• 25 Papademetris X, Jackowski M, Rajeevan N et al.. Bioimage suite: an integrated medical image analysis suite. The Insight Journal. Available at: http://hdl.handle.net/1926/37,2005
  PubMedGoogle Scholar
• 26 Ogawa S, Lee T M, Nayak A S, Glynn P. Oxygenation-sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields.  Magn Reson Med. 1990;  14(1) 68-78
  CrossrefPubMedGoogle Scholar
• 27 Lebon V, Carlier P G, Brillault-Salvat C, Leroy-Willig A. Simultaneous measurement of perfusion and oxygenation changes using a multiple gradient-echo sequence: application to human muscle study.  Magn Reson Imaging. 1998;  16(7) 721-729
  CrossrefPubMedGoogle Scholar
• 28 Lebon V, Brillault-Salvat C, Bloch G, Leroy-Willig A, Carlier P G. Evidence of muscle BOLD effect revealed by simultaneous interleaved gradient-echo NMRI and myoglobin NMRS during leg ischemia.  Magn Reson Med. 1998;  40(4) 551-558
  CrossrefPubMedGoogle Scholar
• 29 Ledermann H P, Heidecker H G, Schulte A C et al.. Calf muscles imaged at BOLD MR: correlation with TcPO₂ and flowmetry measurements during ischemia and reactive hyperemia—initial experience.  Radiology. 2006;  241(2) 477-484
  CrossrefPubMedGoogle Scholar
• 30 Ledermann H P, Schulte A C, Heidecker H G et al.. Blood oxygenation level-dependent magnetic resonance imaging of the skeletal muscle in patients with peripheral arterial occlusive disease.  Circulation. 2006;  113(25) 2929-2935
  CrossrefPubMedGoogle Scholar
• 31 Schulte A C, Aschwanden M, Bilecen D. Calf muscles at blood oxygen level-dependent MR imaging: aging effects at postocclusive reactive hyperemia.  Radiology. 2008;  247(2) 482-489
  CrossrefPubMedGoogle Scholar
• 32 Duteil S, Wary C, Raynaud J S et al.. Influence of vascular filling and perfusion on BOLD contrast during reactive hyperemia in human skeletal muscle.  Magn Reson Med. 2006;  55(2) 450-454
  CrossrefPubMedGoogle Scholar
• 33 Noseworthy M D, Bulte D P, Alfonsi J. BOLD magnetic resonance imaging of skeletal muscle.  Semin Musculoskelet Radiol. 2003;  7(4) 307-315
  Article in Thieme ConnectPubMedGoogle Scholar
• 34 Bulte D P, Alfonsi J, Bells S, Noseworthy M D. Vasomodulation of skeletal muscle BOLD signal.  J Magn Reson Imaging. 2006;  24(4) 886-890
  CrossrefPubMedGoogle Scholar
• 35 Bulte D P, Bells S, Noseworthy M D. (2004) Nicotine induced changes in muscle BOLD signal at 3T. Paper presented at: International Society for Magnetic Resonance in Medicine (ISMRM) May 2004 Kyoto, Japan;
  PubMedGoogle Scholar
• 36 Meyer R A, Towse T F, Reid R W, Jayaraman R C, Wiseman R W, McCully K K. BOLD MRI mapping of transient hyperemia in skeletal muscle after single contractions.  NMR Biomed. 2004;  17(6) 392-398
  CrossrefPubMedGoogle Scholar
• 37 Wigmore D M, Damon B M, Pober D M, Kent-Braun J A. MRI measures of perfusion-related changes in human skeletal muscle during progressive contractions.  J Appl Physiol. 2004;  97(6) 2385-2394
  CrossrefPubMedGoogle Scholar
• 38 Towse T F, Slade J M, Meyer R A. Effect of physical activity on MRI-measured blood oxygen level-dependent transients in skeletal muscle after brief contractions.  J Appl Physiol. 2005;  99(2) 715-722
  CrossrefPubMedGoogle Scholar
• 39 Damon B M, Hornberger J L, Wadington M C, Lansdown D A, Kent-Braun J A. Dual gradient-echo MRI of post-contraction changes in skeletal muscle blood volume and oxygenation.  Magn Reson Med. 2007;  57(4) 670-679
  CrossrefPubMedGoogle Scholar
• 40 Towse T F, Slade J M, Ambrose J A, DeLano M C, Ronald R A. Quantitative analysis of the post-contractile BOLD effect in human skeletal muscle. Paper presented at: International Society for magnetic Resonance in Medicine (ISMRM) April 2009 Honolulu, HI;
  PubMedGoogle Scholar
• 41 Davis A D, Falk B, Noseworthy M D. Comparison of EPI and two-shot spiral in/out for muscle BOLD imaging during exercise.  Magma. 2009;  22(suppl 1) 241-242
  CrossrefPubMedGoogle Scholar
• 42 Raymer G H, Allman B L, Rice C L, Marsh G D, Thompson R T. Characteristics of a MR-compatible ankle exercise ergometer for a 3.0 T head-only MR scanner.  Med Eng Phys. 2006;  28(5) 489-494
  CrossrefPubMedGoogle Scholar
• 43 Isbell D C, Epstein F H, Zhong X et al.. Calf muscle perfusion at peak exercise in peripheral arterial disease: measurement by first-pass contrast-enhanced magnetic resonance imaging.  J Magn Reson Imaging. 2007;  25(5) 1013-1020
  CrossrefPubMedGoogle Scholar
• 44 Toussaint J F, Kwong K K, Mkparu F O et al.. Perfusion changes in human skeletal muscle during reactive hyperemia measured by echo-planar imaging.  Magn Reson Med. 1996;  35(1) 62-69
  CrossrefPubMedGoogle Scholar
• 45 Donahue K M, Van Kylen J, Guven S et al.. Simultaneous gradient-echo/spin-echo EPI of graded ischemia in human skeletal muscle.  J Magn Reson Imaging. 1998;  8(5) 1106-1113
  CrossrefPubMedGoogle Scholar
• 46 Jordan B F, Kimpalou J Z, Beghein N, Dessy C, Feron O, Gallez B. Contribution of oxygenation to BOLD contrast in exercising muscle.  Magn Reson Med. 2004;  52(2) 391-396
  CrossrefPubMedGoogle Scholar
• 47 Tschakovsky M E, Joyner M J. Nitric oxide and muscle blood flow in exercise.  Appl Physiol Nutr Metab. 2008;  33(1) 151-161
  CrossrefPubMedGoogle Scholar
• 48 Rowell L B. Ideas about control of skeletal and cardiac muscle blood flow (1876-2003): cycles of revision and new vision.  J Appl Physiol. 2004;  97(1) 384-392
  CrossrefPubMedGoogle Scholar
• 49 McFadden D, Burr J, Cormier T et al.. Muscle blood-oxygen level dependent (BOLD) imaging: a potential tool to evaluate chronic compartment syndrome. Paper presented at: International Society for Magnetic Resonance Technologists (SMRT) April 2007 Berlin, Germany;
  PubMedGoogle Scholar
• 50 Wardlaw G, Wong R, Noseworthy M D. Identification of intratumour low frequency microvascular components via BOLD signal fractal dimension mapping.  Phys Med. 2008;  24(2) 87-91
  CrossrefPubMedGoogle Scholar
• 51 Biswal B, DeYoe A E, Hyde J S. Reduction of physiological fluctuations in fMRI using digital filters.  Magn Reson Med. 1996;  35(1) 107-113
  CrossrefPubMedGoogle Scholar
• 52 Biswal B, Hudetz A G, Yetkin F Z, Haughton V M, Hyde J S. Hypercapnia reversibly suppresses low-frequency fluctuations in the human motor cortex during rest using echo-planar MRI.  J Cereb Blood Flow Metab. 1997;  17(3) 301-308
  PubMedGoogle Scholar
• 53 Baudelet C, Ansiaux R, Jordan B F, Havaux X, Macq B, Gallez B. Physiological noise in murine solid tumours using T2*-weighted gradient-echo imaging: a marker of tumour acute hypoxia?.  Phys Med Biol. 2004;  49(15) 3389-3411
  CrossrefPubMedGoogle Scholar
• 54 Baudelet C, Cron G O, Ansiaux R et al.. The role of vessel maturation and vessel functionality in spontaneous fluctuations of T2*-weighted GRE signal within tumors.  NMR Biomed. 2006;  19(1) 69-76
  CrossrefPubMedGoogle Scholar
• 55 Braun R D, Lanzen J L, Dewhirst M W. Fourier analysis of fluctuations of oxygen tension and blood flow in R3230Ac tumors and muscle in rats.  Am J Physiol. 1999;  277(2 Pt 2) H551-H568
  PubMedGoogle Scholar
• 56 Wardlaw G, Noseworthy M D. Method and system for imaging muscle tissue.  Patent pending.
  PubMedGoogle Scholar
• 57 Hoult D I, Busby S JW, Gadian D G, Radda G K, Richards R E, Seeley P J. Observation of tissue metabolites using 31P nuclear magnetic resonance.  Nature. 1974;  252(5481) 285-287
  CrossrefPubMedGoogle Scholar
• 58 Taylor D J. Clinical utility of muscle MR spectroscopy.  Semin Musculoskelet Radiol. 2000;  4(4) 481-502
  Article in Thieme ConnectPubMedGoogle Scholar
• 59 Mattei J P, Bendahan D, Cozzone P. P-31 magnetic resonance spectroscopy. A tool for diagnostic purposes and pathophysiological insights in muscle diseases.  Reumatismo. 2004;  56(1) 9-14
  PubMedGoogle Scholar
• 60 Weber M A, Nielles-Vallespin S, Essig M, Jurkat-Rott K, Kauczor H U, Lehmann-Horn F. Muscle Na+ channelopathies: MRI detects intracellular 23Na accumulation during episodic weakness.  Neurology. 2006;  67(7) 1151-1158
  CrossrefPubMedGoogle Scholar
• 61 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
• 62 Hilal S K, Maudsley A A, Ra J B et al.. In vivo NMR imaging of sodium-23 in the human head.  J Comput Assist Tomogr. 1985;  9(1) 1-7
  CrossrefPubMedGoogle Scholar
• 63 Granot J. Sodium imaging of human body organs and extremities in vivo.  Radiology. 1988;  167(2) 547-550
  PubMedGoogle Scholar
• 64 Maudsley A A, Hilal S K. Biological aspects of sodium-23 imaging.  Br Med Bull. 1984;  40(2) 165-166
  PubMedGoogle Scholar
• 65 Constantinides C D, Gillen J, Boada F, Bottomley P A. ²³Na imaging and quantification of skeletal muscle at 1.5T. Paper presented at: International Society for magnetic Resonance in Medicine (ISMRM) May 1999 Denver CO;
  PubMedGoogle Scholar
• 66 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
• 67 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
• 68 Kushnir T, Knubovets T, Itzchak Y et al.. In vivo 23Na NMR studies of myotonic dystrophy.  Magn Reson Med. 1997;  37(2) 192-196
  CrossrefPubMedGoogle Scholar
• 69 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

Michael D NoseworthyPh.D. 

Imaging Research Centre, Brain-Body Institute, St. Joseph's Healthcare

50 Charlton Ave. East, Hamilton, Ontario L8N 4A6 Canada

Email: nosewor@mcmaster.ca