JBiSE  Vol.7 No.8 , June 2014
Assessment of Mechanical Properties of Muscles from Multi-Parametric Magnetic Resonance Imaging
ABSTRACT
We hypothesized that a relationship existed between the mechanical properties and the magnetic resonance imaging (MRI) parameters of muscles, as already demonstrated in cartilaginous tissues. The aim was to develop an indirect evaluation tool of the mechanical properties of degenerated muscles. Leg and arm muscles of adult rabbits were dissected, and tested 12 hours post mortem, in a state of rigor mortis, or 72 hours post mortem, in a state of post-rigor mortis. The tests consisted of a multi-parametric MRI acquisition followed by a uniaxial tensile test until failure. The statistical analysis consisted of multiple linear regressions and principal component analysis. Significant differences existed between the rigor mortis and post-rigor mortis groups for E but not for the MRI parameters. 78%, 60% or 33% of the Young’s modulus could be explained by the MRI parameters in the post-rigor mortis group, rigor mortis group or both groups respectively. These relationships were confirmed by the principal component analysis. The proposed multi-parametric MRI protocol associated to principal component analysis is a promising tool for the indirect evaluation of muscle mechanical properties and should be useful to find biomarkers and predictive factors of the evolution of the pathologies.

Cite this paper
Grenier, R. , Périé, D. , Gilbert, G. , Beaudoin, G. and Curnier, D. (2014) Assessment of Mechanical Properties of Muscles from Multi-Parametric Magnetic Resonance Imaging. Journal of Biomedical Science and Engineering, 7, 593-603. doi: 10.4236/jbise.2014.78060.
References
[1]   Stephenson, D.G. and Williams, D.A. (1981) Calcium-Activated Force Responses in Fast- and Slow-Twitch Skinned Muscle Fibres of the Rat at Different Temperatures. The Journal of Physiology, 317, 281-302.

[2]   Van Ee, C.A., Chasse, A.L. and Myers, B.S. (2000) Quantifying Skeletal Muscle Properties in Cadaveric Test Specimens: Effects of Mechanical Loading, Postmortem Time, and Freezer Storage. Journal of Biomechanical Engineering, 122, 9-14.
http://dx.doi.org/10.1115/1.429621

[3]   Horowits, R., Dalakas, M.C. and Podolsky, R.J. (1990) Single Skinned Muscle Fibers in Duchenne Muscular Dystrophy Generate Normal Force. Annals of Neurology, 27, 636-641.
http://dx.doi.org/10.1002/ana.410270609

[4]   Zoabli, G., Mathieu, P.A. and Aubin, C.E. (2008) Magnetic Resonance Imaging of the Erector Spinae Muscles in Duchenne Muscular Dystrophy: Implication for Scoliotic Deformities. Scoliosis, 3, 21.
http://dx.doi.org/10.1186/1748-7161-3-21

[5]   Tsai, Y.T., Leong, C.P., Huang, Y.C., Kuo, S.H., Wang, H.C., Yeh, H.C. and Lau, Y.C. (2010) The Electromyographic Responses of Paraspinal Muscles during Isokinetic Exercise in Adolescents with Idiopathic Scoliosis with a Cobb’s Angle Less than Fifty Degrees. Chang Gung Medical Journal, 33, 540-550.

[6]   Zoabli, G., Mathieu, P.A. and Aubin, C.E. (2007) Back Muscles Biometry in Adolescent Idiopathic Scoliosis. The Spine Journal, 7, 338-344.
http://dx.doi.org/10.1016/j.spinee.2006.04.001

[7]   Mahaudens, P. and Mousny, M. (2010) Gait in Adolescent Idiopathic Scoliosis. Kinematics, Electromyographic and Energy Cost Analysis. Studies in Health Technology and Informatics, 158, 101-106.

[8]   Gosselin, L.E., Adams, C., Cotter, T.A., McCormick, R.J. and Thomas, D.P. (1998) Effect of Exercise Training on Passive Stiffness in Locomotor Skeletal Muscle: Role of Extracellular Matrix. Journal of Applied Physiology, 85, 1011-1016.

[9]   Kragstrup, T.W., Kjaer, M. and Mackey, A.L. (2011) Structural, Biochemical, Cellular, and Functional Changes in Skeletal Muscle Extracellular Matrix with Aging. Scandinavian Journal of Medicine Science in Sports, 21, 749-757.
http://dx.doi.org/10.1111/j.1600-0838.2011.01377.x

[10]   Jeneson, J.A. and Bruggeman, F.J. (2004) Robust Homeostatic Control of Quadriceps pH during Natural Locomotor Activity in Man. The FASEB Journal, 18, 1010-1012.

[11]   Bensamoun, S.F., Glaser, K.J., Ringleb, S.I., Chen, Q., Ehman, R.L. and An, K.N. (2008) Rapid magnetic Resonance Elastography of Muscle Using One-Dimensional Projection. Journal of Magnetic Resonance Imaging, 27, 1083-1088.
http://dx.doi.org/10.1002/jmri.21307

[12]   Bensamoun, S.F., Ringleb, S.I., Chen, Q., Ehman, R.L., An, K.N. and Brennan, M. (2007) Thigh Muscle Stiffness Assessed with Magnetic Resonance Elastography in Hyperthyroid Patients before and after Medical Treatment. Journal of Magnetic Resonance Imaging, 26, 708-713.
http://dx.doi.org/10.1002/jmri.21073

[13]   Samosky, J.T., Burstein, D., Eric Grimson, W., Howe, R., Martin, S. and Gray, M.L. (2005) Spatially-Localized Correlation of dGEMRIC-Measured GAG Distribution and Mechanical Stiffness in the Human Tibial Plateau. Journal of Orthopaedic Research, 23, 93-101.
http://dx.doi.org/10.1016/j.orthres.2004.05.008

[14]   Chen, C.T., Fishbein, K.W., Torzilli, P.A., Hilger, A., Spencer, R.G., Horton, Jr., W.E. (2003) Matrix Fixed-Charge Density as Determined by Magnetic Resonance Microscopy of Bioreactor-Derived Hyaline Cartilage Correlates with Biochemical and Biomechanical Properties. Arthritis Rheumatology, 48, 1047-1056.
http://dx.doi.org/10.1002/art.10991

[15]   Kurkijarvi, J.E., Nissi, M.J., Kiviranta, I., Jurvelin, J.S. and Nieminen, M.T. (2004) Delayed Gadolinium-Enhanced MRI of Cartilage (dGEMRIC) and T2 Characteristics of Human Knee Articular Cartilage: Topographical Variation and Relationships to Mechanical Properties. Magnetic Resonance in Medicine, 52, 41-46.
http://dx.doi.org/10.1002/mrm.20104

[16]   Lammentausta, E., Kiviranta, P., Nissi, M.J., Laasanen, M.S., Kiviranta, I., Nieminen, M.T. and Jurvelin, J.S. (2006) T2 Relaxation Time and Delayed Gadolinium-Enhanced MRI of Cartilage (dGEMRIC) of Human Patellar Cartilage at 1.5 T and 9.4 T: Relationships with Tissue Mechanical Properties. Journal of Orthopaedic Research, 24, 366-374.
http://dx.doi.org/10.1002/jor.20041

[17]   Nieminen, M.T., Toyras, J., Laasanen, M.S., Silvennoinen, J., Helminen, H.J. and Jurvelin, J.S. (2004) Prediction of Biomechanical Properties of Articular Cartilage with Quantitative Magnetic Resonance Imaging. Journal of Biomechanics, 37, 321-328.
http://dx.doi.org/10.1016/S0021-9290(03)00291-4

[18]   Nissi, M.J., Rieppo, J., Toyras, J., Laasanen, M.S., Kiviranta, I., Nieminen, M.T. and Jurvelin, J.S. (2007) Estimation of Mechanical Properties of Articular Cartilage with MRI-dGEMRIC, T2 and T1 Imaging in Different Species with Variable Stages of Maturation. Osteoarthritis and Cartilage, 15, 1141-1148.
http://dx.doi.org/10.1016/j.joca.2007.03.018

[19]   Wheaton, A.J., Dodge, G.R., Elliott, D.M., Nicoll, S.B. and Reddy, R. (2005) Quantification of Cartilage Biomechanical and Biochemical Properties via T1ρ Magnetic Resonance Imaging. Magnetic Resonance in Medicine, 54, 1087-1093.
http://dx.doi.org/10.1002/mrm.20678

[20]   Nguyen, A.M., Johannessen, W., Yoder, J.H., Wheaton, A.J., Vresilovic, E.J., Borthakur, A. and Elliott, D.M. (2008) Noninvasive Quantification of Human Nucleus Pulposus Pressure with Use of T1ρ-Weighted Magnetic Resonance Imaging. Journal of Bone and Joint Surgery, 90, 796-802.
http://dx.doi.org/10.2106/JBJS.G.00667

[21]   Perie, D., Iatridis, J.C., Demers, C.N., Goswami, T., Beaudoin, G., Mwale, F. and Antoniou, J. (2006) Assessment of Compressive Modulus, Hydraulic Permeability and Matrix Content of Trypsin-Treated Nucleus Pulposus Using Quantitative MRI. Journal of Biomechanics, 39, 1392-1400.
http://dx.doi.org/10.1016/j.jbiomech.2005.04.015

[22]   Mwale, F., Iatridis, J.C. and Antoniou, J. (2008) Quantitative MRI as a Diagnostic Tool of Intervertebral Disc Matrix Composition and Integrity. European Spine Journal, 17, 432-440.
http://dx.doi.org/10.1007/s00586-008-0744-4

[23]   Recuerda, M., Périé, D., Gilbert, G. and Beaudoin, G. (2012) Assessment of Mechanical Properties of Isolated Bovine Intervertebral Discs from Multi-Parametric Magnetic Resonance Imaging. BMC Musculoskeletal Disorders, 13, 195.
http://dx.doi.org/10.1186/1471-2474-13-195

[24]   Heemskerk, A.M., Strijkers, G.J., Vilanova, A., Drost, M.R. and Nicolay, K. (2005) Determination of Mouse Skeletal Muscle Architecture Using Three-Dimensional Diffusion Tensor Imaging. Magnetic Resonance in Medicine, 53, 1333-1340.
http://dx.doi.org/10.1002/mrm.20476

[25]   Hatakenaka, M., Yabuuchi, H., Matsuo, Y., Okafuji, T., Kamitani, T., Setoguchi, T., Nishikawa, K. and Honda, H. (2008) Effect of Passive Muscle Length Change on Apparent Diffusion Coefficient: Detection with Clinical MR Imaging. Magnetic Resonance in Medical Sciences, 7, 59-63.
http://dx.doi.org/10.2463/mrms.7.59

[26]   Kinugasa, R., Kawakami, Y. and Fukunaga, T. (2006) Mapping Activation Levels of Skeletal Muscle in Healthy Volunteers: An MRI Study. Journal of Magnetic Resonance Imaging, 24, 1420-1425.
http://dx.doi.org/10.1002/jmri.20772

[27]   Patten, C., Meyer, R.A. and Fleckenstein, J.L. (2003) T2 Mapping of Muscle. Seminars in Musculoskeletal Radiology, 7, 297-305.
http://dx.doi.org/10.1055/s-2004-815677

[28]   Wright, P., Mougin, O., Totman, J., Peters, A., Brookes, M., Coxon, R., Morris, P., Clemence, M., Francis, S., Bowtell, R. and Gowland, P. (2008) Water Proton T1 Measurements in Brain Tissue at 7, 3, and 1.5T Using IR-EPI, IR-TSE, and MPRAGE: Results and Optimization. Magnetic Resonance Materials in Physics, Biology and Medicine, 21, 121-130.

[29]   Wang, C., Witschey, W., Goldberg, A., Elliott, M., Borthakur, A. and Reddy, R. (2010) Magnetization Transfer Ratio Mapping of Intervertebral Disc Degeneration.

[30]   Henkelman, R.M., Stanisz, G.J. and Graham, S.J. (2001) Magnetization Transfer in MRI: A Review. NMR in Biomedicine, 14, 57-64.
http://dx.doi.org/10.1002/nbm.683

[31]   Kingsley, P.B. (2006) Introduction to Diffusion Tensor Imaging Mathematics: Part I. Tensors, Rotations, and Eigenvectors. Concepts in Magnetic Resonance Part A, 28A, 101-122.
http://dx.doi.org/10.1002/cmr.a.20048

[32]   Kingsley, P.B. (2006) Introduction to Diffusion Tensor Imaging Mathematics: Part II. Anisotropy, Diffusion-Weighting Factors, and Gradient Encoding Schemes. Concepts in Magnetic Resonance Part A, 28A, 123-154.
http://dx.doi.org/10.1002/cmr.a.20049

[33]   Le Bihan, D., Breton, E., Lallemand, D., Grenier, P., Cabanis, E. and Laval-Jeantet, M. (1986) MR Imaging of Intravoxel Incoherent Motions: Application to Diffusion and Perfusion in Neurologic Disorders. Radiology, 161, 401-407.

[34]   Offer, G.K.P. (1988) The Structural Basis of Water-Holding in Meat. Developments in Meat Science.

[35]   Antoniou, J., Mwale, F., Demers, C.N., Beaudoin, G., Goswami, T., Aebi, M. and Alini, M. (2006) Quantitative Magnetic Resonance Imaging of Enzymatically Induced Degradation of the Nucleus Pulposus of Intervertebral Discs. Spine (Phila Pa 1976), 31, 1547-1554.

[36]   Antoniou, J., Pike, G.B., Steffen, T., Baramki, H., Poole, A.R., Aebi, M. and Alini, M. (1998) Quantitative Magnetic Resonance Imaging in the Assessment of Degenerative Disc Disease. Magnetic Resonance in Medicine, 40, 900-907.
http://dx.doi.org/10.1002/mrm.1910400616

[37]   Nieminen, M.T., Töyräs, J., Rieppo, J., Hakumäki, J.M., Silvennoinen, J., Helminen, H.J. and Jurvelin, J.S. (2000) Quantitative MR Microscopy of Enzymatically Degraded Articular Cartilage. Magnetic Resonance in Medicine, 43, 676-681.
http://dx.doi.org/10.1002/(SICI)1522-2594(200005)43:5<676::AID-MRM9>3.0.CO;2-X

[38]   Paajanen, H., Komu, M., Lehto, I., Laato, M. and Haapasalo, H. (1994) Magnetization Transfer Imaging of Lumbar Disc Degeneration. Correlation of Relaxation Parameters with Biochemistry. Spine (Phila Pa 1976), 19, 2833-2837.

[39]   Antoniou, J., Demers, C.N., Beaudoin, G., Goswami, T., Mwale, F., Aebi, M. and Alini, M. (2004) Apparent Diffusion Coefficient of Intervertebral Discs Related to Matrix Composition and Integrity. Magnetic Resonance Imaging, 22, 963-972.
http://dx.doi.org/10.1016/j.mri.2004.02.011

[40]   Virta, A., Komu, M., Lundbom, N. and Kormano, M. (1998) T1ρ MR Imaging Characteristics of Human Anterior Tibial and Gastrocnemius Muscles. Academic Radiology, 5, 104-110.
http://dx.doi.org/10.1016/S1076-6332(98)80130-X

[41]   Franczak, M.B., Ulmer, J.L., Jaradeh, S., McDaniel, J.D., Mark, L.P. and Prost, R.W. (2000) Spin-Lock Magnetic Resonance Imaging of Muscle in Patients with Autosomal Recessive Limb Girdle Muscular Dystrophy. Journal of Neuro-imaging, 10, 73-77.

[42]   van Zijl, P.C. and Yadav, N.N. (2011) Chemical Exchange Saturation Transfer (CEST): What Is in a Name and What Isn’t? Magnetic Resonance in Medicine, 65, 927-948.
http://dx.doi.org/10.1002/mrm.22761

[43]   Heemskerk, A.M., Sinha, T.K., Wilson, K.J., Ding, Z. and Damon, B.M. (2009) Quantitative Assessment of DTI-Based Muscle Fiber Tracking and Optimal Tracking Parameters. Magnetic Resonance in Medicine, 61, 467-472.
http://dx.doi.org/10.1002/mrm.21819

[44]   Heemskerk, A.M., Sinha, T.K., Wilson, K.J., Ding, Z. and Damon, B.M. (2010) Repeatability of DTI-Based Skeletal Muscle Fiber Tracking. NMR in Biomedicine, 23, 294-303.

[45]   Bensamoun, S., Stevens, L., Fleury, M.J., Bellon, G., Goubel, F. and Tho, M.C.H.B. (2006) Macroscopic-Microscopic Characterization of the Passive Mechanical Properties in Rat Soleus Muscle. Journal of Biomechanics, 39, 568-578.
http://dx.doi.org/10.1016/j.jbiomech.2004.04.036

[46]   Gennisson, J.L., Deffieux, T., Macé, E., Montaldo, G., Fink, M. and Tanter, M. (2010) Viscoelastic and Anisotropic Mechanical Properties of in Vivo Muscle Tissue Assessed by Supersonic Shear Imaging. Ultrasound in Medicine and Biology, 36, 789-801.
http://dx.doi.org/10.1016/j.ultrasmedbio.2010.02.013

[47]   Van Loocke, M., Simms, C.K. and Lyons, C.G. (2009) Viscoelastic Properties of Passive Skeletal Muscle in Compression—Cyclic Behaviour. Journal of Biomechanics, 42, 1038-1048.
http://dx.doi.org/10.1016/j.jbiomech.2009.02.022

 
 
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