Applications of magnetic resonance elastography to healthy and pathologic skeletal muscle
Stacie I. Ringleb PhD
Biomechanics Laboratory, Division of Orthopedic Research, Mayo Clinic, College of Medicine, Rochester, Minnesota, USA
Search for more papers by this authorSabine F. Bensamoun PhD
Biomechanics Laboratory, Division of Orthopedic Research, Mayo Clinic, College of Medicine, Rochester, Minnesota, USA
Search for more papers by this authorQingshan Chen MS
Biomechanics Laboratory, Division of Orthopedic Research, Mayo Clinic, College of Medicine, Rochester, Minnesota, USA
Search for more papers by this authorArmando Manduca PhD
Department of Radiology, Mayo Clinic College of Medicine, Rochester, Minnesota, USA
Search for more papers by this authorKai-Nan An PhD
Biomechanics Laboratory, Division of Orthopedic Research, Mayo Clinic, College of Medicine, Rochester, Minnesota, USA
Search for more papers by this authorCorresponding Author
Richard L. Ehman MD
Department of Radiology, Mayo Clinic College of Medicine, Rochester, Minnesota, USA
Department of Radiology, Mayo Clinic College of Medicine, 200 First Street SW, Rochester, MN 55905Search for more papers by this authorStacie I. Ringleb PhD
Biomechanics Laboratory, Division of Orthopedic Research, Mayo Clinic, College of Medicine, Rochester, Minnesota, USA
Search for more papers by this authorSabine F. Bensamoun PhD
Biomechanics Laboratory, Division of Orthopedic Research, Mayo Clinic, College of Medicine, Rochester, Minnesota, USA
Search for more papers by this authorQingshan Chen MS
Biomechanics Laboratory, Division of Orthopedic Research, Mayo Clinic, College of Medicine, Rochester, Minnesota, USA
Search for more papers by this authorArmando Manduca PhD
Department of Radiology, Mayo Clinic College of Medicine, Rochester, Minnesota, USA
Search for more papers by this authorKai-Nan An PhD
Biomechanics Laboratory, Division of Orthopedic Research, Mayo Clinic, College of Medicine, Rochester, Minnesota, USA
Search for more papers by this authorCorresponding Author
Richard L. Ehman MD
Department of Radiology, Mayo Clinic College of Medicine, Rochester, Minnesota, USA
Department of Radiology, Mayo Clinic College of Medicine, 200 First Street SW, Rochester, MN 55905Search for more papers by this authorAbstract
Magnetic resonance elastography (MRE) is capable of noninvasively quantifying the mechanical properties of skeletal muscles in vivo. This information can be clinically useful to understand the effects of pathologies on the mechanical properties of muscle and to quantify the effects of treatment. Advances in inversion algorithms quantify muscle anisotropy in two-dimensional (2D) and three-dimensional (3D) imaging. Databases of the shear stiffness of skeletal muscle have been presented in the relaxed and contracted states in the upper extremity (biceps brachii, flexor digitorum profundus, and upper trapezius), distal leg muscles (tibialis anterior, medial gastrocnemius, lateral gastrocnemius, and trapezius), and proximal leg muscles (vastus lateralis, vastus medialis, and sartorius). MRE measurements have successfully validated a mathematical model of skeletal muscle behavior in the biceps brachii, correlated to electromyographic data in the distal leg muscles and quantified the effects of pathologies on the distal and proximal leg muscles. Future research efforts should be directed toward improving one-dimensional (1D) and 3D MRE data acquisition and image processing, tracking the effects of treatment on pathologic muscle and correlating the shear stiffness with clinical measurements. J. Magn. Reson. Imaging 2007. © 2007 Wiley-Liss, Inc.
REFERENCES
- 1 Bizzini M, Mannion AF. Reliability of a new, hand-held device for assessing skeletal muscle stiffness. Clin Biomech 2003; 18: 459–461.
- 2 Leonard CT, Brown JS, Price TR, Queen SA, Mikhailenok EL. Comparison of surface electromyography and myotonometric measurements during voluntary isometric contractions. J Electromyogr Kinesiol 2004; 14: 709–714.
- 3 Arokoski JP, Surakka J, Ojala T, Kolari P, Jurvelin JS. Feasibility of the use of a novel soft tissue stiffness meter. Physiol Meas 2005; 26: 215–228.
- 4 Leonard CT, Deshner WP, Romo JW, Suoja ES, Fehrer SC, Mikhailenok EL. Myotonometer intra- and interrater reliabilities. Arch Phys Med Rehabil 2003; 84: 928–932.
- 5 Sinha S, Hodgson JA, Finni T, Lai AM, Grinstead J, Edgerton VR. Muscle kinematics during isometric contraction: development of phase contrast and spin tag techniques to study healthy and atrophied muscles. J Magn Reson Imaging 2004; 20: 1008–1019.
- 6 Finni T, Hodgson JA, Lai AM, Edgerton VR, Sinha S. Mapping of movement in the isometrically contracting human soleus muscle reveals details of its structural and functional complexity. J Appl Physiol 2003; 95: 2128–2133.
- 7 Finni T, Hodgson JA, Lai AM, Edgerton VR, Sinha S. Nonuniform strain of human soleus aponeurosis-tendon complex during submaximal voluntary contractions in vivo. J Appl Physiol 2003; 95: 829–837.
- 8 Finni T, Hodgson JA, Lai AM, Edgerton VR, Sinha S. Muscle synergism during isometric plantar flexion in Achilles tendon rupture patients and in normal subjects revealed by velocity-encoded cine phase-contrast MRI. Clin Biomech (Bristol, Avon) 2006; 21: 67–74.
- 9 Zhong X, Blemker SS, Spottiswoode BS, Helm PA, Hess AT, Epstein FH. Application of cine DENSE MRI to studying skeletal muscle mechanics during joint motion. In: Proceedings of the 14th Annual Meeting of ISMRM, Seattle, WA, USA, 2006 (Abstract 256).
- 10 Adams GR, Duvoisin MR, Dudley GA. Magnetic resonance imaging and electromyography as indexes of muscle function. J Appl Physiol 1992; 73: 1578–1583.
- 11 Ploutz LL, Tesch PA, Biro RL, Dudley GA. Effect of resistance training on muscle use during exercise. J Appl Physiol 1994; 76: 1675–1681.
- 12 Yue G, Alexander AL, Laidlaw DH, Gmitro AF, Unger EC, Enoka RM. Sensitivity of muscle proton spin-spin relaxation time as an index of muscle activation. J Appl Physiol 1994; 77: 84–92.
- 13 Gold GE. Dynamic and functional imaging of the musculoskeletal system. Semin Musculoskelet Radiol 2003; 7: 245–248.
- 14 Meyer RA, Towse TF, Reid RW, Jayaraman RC, Wiseman RW, McCully KK. Bold MRI mapping of transient hyperemia in skeletal muscle after single contractions. NMR Biomed 2004; 17: 392–398.
- 15 Levinson SF, Shinagawa M, Sato T. Sonoelastic determination of human skeletal muscle elasticity. J Biomech 1995; 28: 1145–1154.
- 16 Gennisson JL, Catheline S, Chaffai S, Fink M. Transient elastography in anisotropic medium: application to the measurement of slow and fast shear wave speeds in muscles. J Acoust Soc Am 2003; 114: 536–541.
- 17 Levinson SF, Catheline S, Fink M. Anisotropic elasticity and viscosity deduced from supersonic shear imaging in muscle. International Society of Biomechanics, XXth Congress. 29th Annual Meeting of the American Society of Biomechanics, Cleveland, OH. p 101.
- 18 Gennisson JL, Cornu C, Catheline S, Fink M, Portero P. Human muscle hardness assessment during incremental isometric contraction using transient elastography. J Biomech 2005; 38: 1543–1550.
- 19 Heers G, Jenkyn T, Alex Dresner M, et al. Measurement of muscle activity with magnetic resonance elastography. Clin Biomech (Bristol, Avon) 2003; 18: 537–542.
- 20 Muthupillai R, Lomas D, Rossman P, Greenleaf JF, Manduca A, Ehman RL. Magnetic resonance elastography by direct visualization of propagating acoustic strain waves. Science 1995; 269: 1854–1857.
- 21 Manduca A, Oliphant TE, Dresner MA, et al. Magnetic resonance elastography: Non-invasive mapping of tissue elasticity. Med Image Anal 2001; 5: 237–254.
- 22 Basford JR, Jenkyn TR, An K-N, Ehman RL, Heers G, Kaufman KR. Evaluation of healthy and diseased muscle with magnetic resonance elastography. Arch Phys Med Rehabil 2002; 83: 1530–1536.
- 23
Dresner M,
Rose G,
Rossman P,
Muthupillai R,
Manduca A,
Ehman RL.
Magnetic resonance elastography of skeletal muscle.
J Magn Reson Imaging
2001;
13:
269–276.
10.1002/1522-2586(200102)13:2<269::AID-JMRI1039>3.0.CO;2-1 CAS PubMed Web of Science® Google Scholar
- 24 Jenkyn TR, Ehman RL, An KN. Noninvasive muscle tension measurement using the novel technique of magnetic resonance elastography (MRE). J Biomech 2003; 36: 1917–1921.
- 25 Ringleb SI, Littrell L, Chen Q, et al. Magnetic resonance elastography for the assessment of muscles in hyperthyroidism. In: 28th Annual Meeting of the American Society of Biomechanics, 2004; Portland, OR.
- 26 Ringleb SI, Kaufman KR, Basford JR, Ehman RL, An KN. Bilateral symmetry of the gastrocnemius stiffness measured with magnetic resonance elastography in healthy and pathologic muscle. International Society of Biomechanics, XXth Congress, 29th Annual Meeting of the American Society of Biomechanics, 2005; Cleveland, OH. p 373.
- 27 Uffmann K, Maderwald S, Ajaj W, et al. In vivo elasticity measurements of extremity skeletal muscle with MR elastography. NMR Biomed 2004; 17: 181–190.
- 28 Sack I, Bernarding J, Braun J. Analysis of wave patterns in MR elastography of skeletal muscle using coupled harmonic oscillator simulations. Magn Reson Imaging 2002; 20: 95–104.
- 29 Chan QCC, Li G, Ehman RL, Yang ES. Observation of anisotropic properties of skeletal muscle in MR elastography via a needle device. In: Proceedings of the 14th Annual Meeting of ISMRM, Seattle, WA, USA, 2006 (Abstract 1704).
- 30 Bensamoun SF, Ringleb SI, Littrell L, et al. Determination of thigh muscle stiffness using magnetic resonance elastography. J Magn Reson Imaging 2006; 23: 242–247.
- 31 Galban CJ, Maderwald S, Herrmann BL, et al. Measuring skeletal muscle elasticity in patients with hypogonadism by MR elastography. In: Proceedings of the 13th Annual Meeting of ISMRM, Miami Beach, FL, USA, 2005 (Abstract 2016).
- 32 Ringleb SI, Kaufman KR, Basford JR, et al. Magnetic resonance elastography: A non-invasive method to differentiate between healthy and pathologic muscle stiffness. 30th Annual Meeting of the American Society of Biomechanics, 2006, Blacksburg, VA.
- 33 Sinkus R, Lorenzen J, Schrader D, Lorenzen M, Dargatz M, Holz D. High-resolution tensor MR elastography for breast tumour detection. Phys Med Biol 2000; 45: 1649–1664.
- 34 Van Houten E, Miga M, Weaver J, Kennedy F. Three-dimensional subzone-based reconstruction algorithm for MR elastography. Magn Reson Med 2001; 45: 827–837.
- 35 Romano A, Shirron J, Bucaro J. On the noninvasive determination of material parameters from a knowledge of elastic displacements: theory and numerical simulation. IEEE Trans Ultrason Ferroelectr Freq Control 1998; 45: 751–759.
- 36 Romano A, Bucaro J, Ehman R, Shirron J. Evaluation of a material parameter extraction algorithm using MRI based displacement measurements. IEEE Trans Ultrason Ferroelectr Freq Control 2000; 47: 1575–1581.
- 37 Papazoglou S, Braun J, Hamhaber U, Sack I. Two-dimensional waveform analysis in MR elastography of skeletal muscles. Phys Med Biol 2005: 1313–1325.
- 38 Romano AJ, Abraham PB, Ringleb SI, Rossman PJ, Bucaro JA, Ehman RL. Analysis of anisotropic velocity profiles utilizing wave-guide constrained magnetic resonance elastography. In: Proceedings of the 14th Annual Meeting of ISMRM, Seattle, WA, USA, 2006 (Abstract 1725).
- 39 Romano AJ, Abraham PB, Ringleb SI, Rossman PJ, Bucaro JA, Ehman RL. Analysis of anisotropic propagation utilizing wave-guide constrained magnetic resonance elastography. In: Proceedings of the 13th Annual Meeting of ISMRM, 2005; Miami Beach, FL, USA (Abstract 2556).
- 40 Romano AJ, Abraham PB, Rossman PJ, Bucaro JA, Ehman RL. Determination and analysis of guided wave propagation using magnetic resonance elastography. Magn Reson Med 2005; 54: 893–900.
- 41 Roe C, Steingrimsdottir OA, Knardahl S, Bakke ES, Vollestad NK. Long-term repeatability of force, endurance time and muscle activity during isometric contractions. J Electromyogr Kinesiol 2006; 16: 103–113.
- 42 Canepari M, Cappelli V, Pellegrino MA, Zanardi MC, Reggiani C. Thyroid hormone regulation of MHC isoform composition and myofibrillar ATPase activity in rat skeletal muscles. Arch Physiol Biochem 1998; 106: 308–315.
- 43 Glaser KJ, Felmlee JP, Ehman RL. Rapid shear stiffness estimations using 2-D spatial excitations in magnetic resonance elastography. In: Proceedings of the 10th Annual Meeting of ISMRM, Honolulu, HI, USA, 2002 (Abstract 39).
- 44 Bensamoun SF, Glaser K, Chen Q, Ringleb SI, Ehman RL, An KN. Rapid magnetic resonance elastography of skeletal muscle using one dimensional projection. 5th World Congress of Biomechanics, 2006. p 4631.