Download PDF
Semin Musculoskelet Radiol 2003; 7(4): 307-316
DOI: 10.1055/s-2004-815678
Copyright © 2002 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel.: +1(212) 584-4662

BOLD Magnetic Resonance Imaging of Skeletal Muscle

Michael D. Noseworthy1,2,3 , Daniel  P. Bulte2 , Jeff Alfonsi4
  • 1Department of Radiology, , McMaster University
  • 2Department of Medical Physics and Radiation Sciences, McMaster University, Hamilton, Ontario, Canada
  • 3The University of Toronto, Department of Medical Imaging, Toronto, Ontario, Canada
  • 4The Hospital for Sick Children, Department of Diagnostic Imaging, Imaging Physics, Toronto, ON Canada
Further Information

Publication History

Publication Date:
21 January 2004 (online)

Also available at
    Permissions and Reprints

ABSTRACT

Blood-oxygen-level-dependent (BOLD) imaging was a concept introduced in 1990 for evaluating brain activation. The method relies on magnetic resonance imaging (MRI) contrast resulting from changes in the microvascular ratio of oxyhaemoglobin (oxyHb) to deoxyhaemoglobin (deoxyHb). OxyHb is diamagnetic, whereas deoxyHb is paramagnetic, which produces a local bulk magnetic susceptibility effect and subsequent MRI signal change. The changes are typically observed in T 2*-weighted functional MRI scans. However, there has recently been interest in BOLD as a way to evaluate microcirculation of any normal or diseased tissue. This review focuses on the application of BOLD imaging in the understanding of normal and diseased skeletal muscle. In addition we present new findings showing the possible application of BOLD imaging with hyperoxia for evaluating skeletal muscle physiology.

KEYWORDS

Muscle - MRI - BOLD

REFERENCES

  • 1 Ogawa S, Lee T M, Kay A R, Tank D W. Brain magnetic resonance imaging with contrast dependent on blood oxygenation.  Proc Natl Acad Sci USA . 1990;  87 9868-9872
    CrossrefPubMedGoogle Scholar
  • 2 Niemi P, Poncelet B P, Kwong K K. et al . Myocardial intensity changes associated with flow stimulation in blood oxygenation sensitive magnetic resonance imaging.  Magn Reson Med . 1996;  36 78-82
    CrossrefPubMedGoogle Scholar
  • 3 Li D, Dhawale P, Rubin P J, Haacke E M, Gropler R J. Myocardial signal response to dipyridamole and dobutamine: demonstration of the BOLD effect using a double-echo gradient-echo sequence.  Magn Reson Med . 1996;  36 16-20
    CrossrefPubMedGoogle Scholar
  • 4 Herzka D A, Boxerman J L, Post W S. et al . Heterogeneity of BOLD-indexed myocardial perfusion reserve.  Proc Int Soc Mag Reson Med . 1999;  7 1277
    PubMedGoogle Scholar
  • 5 Powell-Braxton L, Veniant M, Latvala R D. et al . A mouse model of human familial hypercholesterolemia: markedly elevated low density lipoprotein cholesterol levels and severe atherosclerosis on a low-fat chow diet.  Nat Med . 1998;  4 934-938
    PubMedGoogle Scholar
  • 6 Greve J, Bernstein L, Williams S P, Powell-Braxton L, Peale F, Bunting S, Van Bruggen N. Age and atherosclerosis adversely affect skeletal muscle functional recovery following femoral artery ligation in the mouse: MRI assessment of functional hyperemia.  Proc Int Soc Mag Reson Med (ISMRM) . 2000;  8 134.
    PubMedGoogle Scholar
  • 7 Groshar D, McEwan A J, Parliament M B. et al . Imaging tumor hypoxia and tumor perfusion.  J Nucl Med . 1993;  34 885-888
    PubMedGoogle Scholar
  • 8 Mark F C, Bock C, Pörtner H O. Oxygen-limited thermal tolerance in Antarctic fish investigated by MRI and 31P-MRS.  Am J Physiol Regul Integr Comp Physiol . 2002;  283 R1254-R1262
    PubMedGoogle Scholar
  • 9 Abramovitch R, Dafni H, Smouha E, Benjamin L E, Neeman M. In vivo prediction of vascular susceptibility to vascular endothelial growth factor withdrawal: magnetic resonance imaging of C6 rat glioma in nude mice.  Cancer Res . 1999;  59 5012-5016
    PubMedGoogle Scholar
  • 10 Ogawa S, Menon R S, Kim S G, Ugurbil K. On the characteristics of functional magnetic resonance imaging of the brain.  Annu Rev Biophys Biomol Struct . 1998;  27 447-474
    CrossrefPubMedGoogle Scholar
  • 11 Ogawa S, Menon R S, Tank D W. et al . Functional brain mapping by blood oxygenation level-dependent contrast magnetic resonance imaging. A comparison of signal characteristics with a biophysical model.  Biophys J . 1993;  64 803-812
    CrossrefPubMedGoogle Scholar
  • 12 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 68-78
    CrossrefPubMedGoogle Scholar
  • 13 Dietz V. Gait disorder in spasticity and Parkinson's disease.  Adv Neurol . 2001;  87 143-154
    PubMedGoogle Scholar
  • 14 Kim S G, Rostrup E, Larsson H B, Ogawa S, Paulson O B. Determination of relative CMRO2 from CBF and BOLD changes: significant increase of oxygen consumption rate during visual stimulation.  Magn Reson Med . 1999;  41 1152-1161
    CrossrefPubMedGoogle Scholar
  • 15 Abramovitch R, Frenkiel D, Neeman M. Analysis of subcutaneous angiogenesis by gradient echo magnetic resonance imaging.  Magn Reson Med . 1998;  39 813-824
    PubMedGoogle Scholar
  • 16 Mazurchuk R, Zhou R, Straubinger R M, Chau R I, Grossman Z. Functional magnetic resonance (fMR) imaging of a rat brain tumor model: implications for evaluation of tumor microvasculature and therapeutic response.  Magn Reson Imaging . 1999;  17 537-548
    PubMedGoogle Scholar
  • 17 Robinson S P, Howe F A, Griffiths J R. Noninvasive monitoring of carbogen-induced changes in tumor blood flow and oxygenation by functional magnetic resonance imaging.  Int J Radiat Oncol Biol Physiol. 1995;  33 855-859
    PubMedGoogle Scholar
  • 18 Al-Hallaq H A, Zamora M, Fish B L, Farrell A, Moulder J E, Karczmar G S. MRI measurements correctly predict the relative effects of tumor oxygenating agents on hypoxic fraction in rodent BA1112 tumors.  {{ERR}}Int J Radiat Oncol Biol Physiol . 2000;  47 481-488
    PubMedGoogle Scholar
  • 19 Robinson S P, Howe F A, Rodrigues L M, Stubbs M, Griffiths J R. Magnetic resonance imaging techniques for monitoring changes in tumor oxygenation and blood flow.  Semin Radiat Oncol . 1998;  8 197-207
    PubMedGoogle Scholar
  • 20 Stainsby J A, Wright G A. Monitoring blood oxygen state in muscle microcirculation with transverse relaxation.  Magn Reson Med . 2001;  45 662-672
    CrossrefPubMedGoogle Scholar
  • 21 Noseworthy M D, Kim J K, Stainsby J A, Stanisz G J, Wright G A. Tracking oxygen effects on MR signal in blood and skeletal muscle during hyperoxia exposure.  J Magn Reson Imaging . 1999;  9 814-820
    CrossrefPubMedGoogle Scholar
  • 22 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;  88 226-233
    PubMedGoogle Scholar
  • 23 Ludeke K M, Roschmann P, Tischler R. Susceptibility artifacts in NMR imaging.  Magn Reson Imaging . 1985;  3 329-343
    CrossrefPubMedGoogle Scholar
  • 24 Villringer A, Rosen B R, Belliveau J W. et al . Dynamic imaging with lanthanide chelates in normal brain: contrast due to magnetic susceptibility effects.  Magn Reson Med . 1988;  6 164-174
    PubMedGoogle Scholar
  • 25 Chu S C, Xu Y, Balschi J A, Springer Jr S C. Bulk magnetic susceptibility shifts in NMR studies of compartmentalized samples: use of paramagnetic reagents.  Magn Reson Med . 1990;  13 239-262
    PubMedGoogle Scholar
  • 26 Springer C S. Physicochemical principles influencing magnetopharmaceuticals. In: Gillies RJ, editor NMR in Physiology and Biomedicine. New York: Academic Press 1994: 75-99.
    Google Scholar
  • 27 Springer C S, Patlak C S, Pályka I, Huang W. Principles of susceptibility contrast based functional MRI: the sign of the functional MRI response. In: Moonen CTW Bandettini PA, editors Functional MRI. New York: Springer; 2000: 91-102.
    Google Scholar
  • 28 Lebon V, Carlier P G, Brillault-Salvat C, Bloch G, Leroy-Willig A. Anisotropy of the BOLD Effect in the Skeletal Muscle.  Proc Int Soc Mag Reson Med . 1998;  6 1421
    PubMedGoogle Scholar
  • 29 Ogawa S, Lee T-M, Nayak A, Glynn P. Oxygenation sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields.  Magn Reson Med . 1990;  14 68-78
    CrossrefPubMedGoogle Scholar
  • 30 Hajnal J, Oatridge A, Wilson J. et al . A study of the MR signal produced by ischemia in human subjects.  Proc Int Soc Mag Reson Med . 1996;  4 1773
    PubMedGoogle Scholar
  • 31 Donahue K, 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 1106-1113
    CrossrefPubMedGoogle Scholar
  • 32 Whittal K P, MacKay A L. Quantitative interpretation of NMR relaxation data.  J Mag Reson . 1989;  84 134-152
    PubMedGoogle Scholar
  • 33 Thulborn K R, Waterton J C, Matthews P M, Radda G K. Oxygenation dependence of the transverse relaxation time of water protons in whole blood at high field.  Biochim Biophys Acta . 1982;  714 265-270
    CrossrefPubMedGoogle Scholar
  • 34 Gomori J M, Grossman R I, Yu-Ip C, Asakura T. NMR relaxation times of blood: dependence on field strength, oxidation state, and cell integrity.  J Comput Assist Tomogr . 1987;  11 684-690
    PubMedGoogle Scholar
  • 35 Bryant R G, Marill K, Blackmore C, Francis C. Magnetic relaxation in blood and blood clots.  Magn Reson Med . 1990;  13 133-144
    PubMedGoogle Scholar
  • 36  L uz, Meiboom S. Chemical exchange and NMR-T2 relaxation, J Chem Physiol .  1963;  39 366-372
    PubMedGoogle Scholar
  • 37 Bowen C, Rutt B K. Measuring blood oxygenation using variable echo spacing CPMG: use of the Luz-Meiboom Equation.  Proc Int Soc Mag Reson Med (ISMRM) . 2001;  9 1223
    PubMedGoogle Scholar
  • 38 Noseworthy M D, Qi X, Stainsby J A, Wright G A. Examination of vx2 tumors using a 2-pool model with proton exchange and dynamic Gd-DTPA enhanced MRI.  Proc Int Soc Mag Reson Med . 2000;  8 1059
    PubMedGoogle Scholar
  • 39 Hazlewood C, Chang D, Nichols B, Woessner D. Nuclear magnetic resonance transverse relaxation times of water protons in skeletal muscle.  Biophys J . 1974;  14 583-606
    PubMedGoogle Scholar
  • 40 English A, Joy M, Henkelman R. Pulsed NMR relaxometry of striated muscle fibers.  Magn Reson Med . 1991;  21 264-281
    PubMedGoogle Scholar
  • 41 Rumeur E L, Certaines J D, Toulouse P, Rochcongar P. Water phases in rat striated muscles as determined by T2 proton NMR relaxation times.  Magn Reson Imaging . 1987;  5 267-272
    PubMedGoogle Scholar
  • 42 Adzamli I, Jolesz F, Bleier A, Mulkern R, Sandor T. The effect of gadolinium DTPA on tissue water compartments in slow- and fasttwitch rabbit muscles.  Magn Reson Med . 1989;  11 172-181
    PubMedGoogle Scholar
  • 43 Belton P S, Jackson R R, Packer K J. Pulsed NMR studies of water in striated muscle: transverse nuclear spin relaxation times and freezing effects.  Biochim Biophys Acta . 1972;  286 16-25
    PubMedGoogle Scholar
  • 44 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;  88 226-233
    PubMedGoogle Scholar
  • 45 Saab G, Marsh G D, Casselman M A, Thompson R T. Changes in human muscle transverse relaxation following short-term creatine supplementation.  Exp Physiol . 2002;  87 383-389
    CrossrefPubMedGoogle Scholar
  • 46 Saab G, Thompson R T. Marsh GD Multicomponent T2 relaxation of in vivo skeletal muscle.  Magn Reson Med . 1999;  42 150-157
    CrossrefPubMedGoogle Scholar
  • 47 Frank L R, Wong E C, Haseler L J, Buxton R B. Dynamic imaging of perfusion in human skeletal muscle during exercise with arterial spin labeling.  Magn Reson Med . 1999;  42 258-267
    CrossrefPubMedGoogle Scholar
  • 48 Hennig J, Scheffler K, Schreiber A. Time resolved observation of BOLD effect in muscle during isometric exercise.  Proc Intl Soc Mag Reson Med . 2000;  8 122
    PubMedGoogle Scholar
  • 49 Meyer R, Mccully K, Reid R W, Prior B. BOLD MRI and NIRS detection of transient hyperemia after single skeletal muscle contractions.  Proc Intl Soc Mag Reson Med . 2001;  9 135
    PubMedGoogle Scholar
  • 50 Brock R W, Tschakovsky M E, Shoemaker J K, Halliwill J R, Joyner M J, Hughson R L. Effects of acetylcholine and nitric oxide on forearm blood flow at rest and after a single muscle contraction.  J Appl Physiol . 1998;  85 2249-2254
    PubMedGoogle Scholar
  • 51 Meyer R A, Prior B M. Functional magnetic resonance imaging of muscle.  Exerc Sport Sci Rev . 2000;  28 89-92
    PubMedGoogle Scholar
  • 52 Büchert M, Bilecen D, Winterer J, Schulte A, Langer M, Hennig J. Time resolved BOLD response in the muscle of patients with peripheral vascular occlusive disease.  Proc Int Soc Mag Reson Med . 2002;  10 0291
    PubMedGoogle Scholar
  • 53 Tadamura E, Hatabu H, Li W, Prasad P V, Edelman R R. Effect of oxygen inhalation on relaxation times in various tissues.  J Magn Reson Imaging . 1997;  7 220-225
    PubMedGoogle Scholar
  • 54 Brooks R A, Brunetti A, Alger J R, DiChiro G. On the origin of paramagnetic inhomogeneity effects in blood.  Magn Reson Med . 1989;  12 241-248
    PubMedGoogle Scholar
  • 55 Thulborn K R, Waterton J C, Mathews P M, Radda G K. Oxygenation dependence of the transverse relaxation time of water protons in whole blood at high field.  Biochim Biophys Acta . 1982;  714 265-270
    CrossrefPubMedGoogle Scholar
  • 56 Wright G A, Hu B S, Macovski A. Estimating oxygen saturation of blood in vivo with MR imaging at 1.5T.  J Magn Reson Imaging . 1991;  1 275-283
    PubMedGoogle Scholar
  • 57 Losert C, Peller M, Schneider P, Reiser M. Oxygen-enhanced MRI of the brain.  Magn Reson Med . 2002;  48 271-277
    CrossrefPubMedGoogle Scholar
  • 58 Bauer W R, Nadler W, Bock M. et al . The relationship between the BOLD-induced T(2) and T(2)(*): a theoretical approach for the vasculature of myocardium.  Magn Reson Med . 1999;  42 1004-1010
    CrossrefPubMedGoogle Scholar
  • 59 Buchert M, Bileen D, Winterer J, Schulte A, Langer M, Hennig J. Time resolved BOLD response in the muscle of patients with peripheral vascular occlusive disease.  Proc Int Soc Mag Reson Med . 2002;  10 0291
    PubMedGoogle Scholar
  • 60 Noll D C, Cohen J D, Meyer C H, Schneider W. Spiral K-space MR imaging of cortical activation.  J Magn Reson Imaging . 1995;  5 49-56
    PubMedGoogle Scholar
  • 61 Cox R W. Software for analysis and visualization of functional magnetic resonance neuroimages.  Comput Biomed Res . 1996;  29 162-173
    CrossrefPubMedGoogle Scholar
  • 62 Barstow T J, Jones A M, Nguyen P H, Casaburi R. Influence of muscle fiber type and pedal frequency on oxygen uptake kinetics of heavy exercise.  J Appl Physiol . 1996;  81 1642-1650
    CrossrefPubMedGoogle Scholar
  • 63 Morikawa S, Inubushi T, Kito K. Heterogeneous metabolic changes in the calf muscle of the rat during ischaemia-reperfusion: in vivo analysis by 31P nuclear magnetic resonance chemical shift imaging and 1H magnetic resonance imaging.  Cardiovasc Surg . 1993;  1 337-342
    PubMedGoogle Scholar
  • 64 Hu L, Fleckenstein J L, Babcock E. Perfusion MRI of post-exercise muscle.  Proc Int Soc Mag Reson Med . 2002;  10 290
    PubMedGoogle Scholar
  • 65 Carusone L M, Srinivasan J, Gitelman D R, Mesulam M M, Parrish T B. Hemodynamic response changes in cerebrovascular disease: implications for functional MR imaging.  Am J Neuroradiol . 2002;  23 1222-1228
    PubMedGoogle Scholar
  • 66 Suwa M, Nakano H, Higaki Y, Nakamura T, Katsuta S, Kumagai S. Increased wheel-running activity in the genetically skeletal muscle fast-twitch fiber-dominant rats.  J Appl Physiol . 2003;  94 185-192
    PubMedGoogle Scholar
      >