Research Papers

Anisotropic Compressive Properties of Passive Porcine Muscle Tissue

[+] Author and Article Information
Renee Pietsch, Ryan Gilbrech, Rajkumar Prabhu, Jun Liao, Lakiesha N. Williams

Injury Biomechanics Laboratory,
Department of Agricultural and
Biological Engineering,
Mississippi State University,
Mississippi State, MS 39762

Benjamin B. Wheatley, Tammy L. Haut Donahue

Soft Tissue Mechanics Laboratory,
Department of Mechanical Engineering,
Colorado State University,
Fort Collins, CO 80523

Manuscript received February 15, 2014; final manuscript received July 1, 2014; accepted manuscript posted July 28, 2014; published online September 4, 2014. Assoc. Editor: David Corr.

J Biomech Eng 136(11), 111003 (Sep 04, 2014) (7 pages) Paper No: BIO-14-1075; doi: 10.1115/1.4028088 History: Received February 15, 2014; Revised July 01, 2014; Accepted July 28, 2014

The body has approximately 434 muscles, which makes up 40–50% of the body by weight. Muscle is hierarchical in nature and organized in progressively larger units encased in connective tissue. Like many soft tissues, muscle has nonlinear visco-elastic behavior, but muscle also has unique characteristics of excitability and contractibility. Mechanical testing of muscle has been done for crash models, pressure sore models, back pain, and other disease models. The majority of previous biomechanical studies on muscle have been associated with tensile properties in the longitudinal direction as this is muscle's primary mode of operation under normal physiological conditions. Injury conditions, particularly high rate injuries, can expose muscle to multiple stress states. Compressive stresses can lead to tissue damage, which may not be reversible. In this study, we evaluate the structure–property relationships of porcine muscle tissue under compression, in both the transverse and longitudinal orientations at 0.1 s−1, 0.01 s−1, or 0.001 s−1. Our results show an initial toe region followed by an increase in stress for muscle in both the longitudinal and transverse directions tested to 50% strain. Strain rate dependency was also observed with the higher strain rates showing significantly more stress at 50% strain. Muscle in the transverse orientation was significantly stiffer than in the longitudinal orientation indicating anisotropy. The mean area of fibers in the longitudinal orientation shows an increasing mean fiber area and a decreasing mean fiber area in the transverse orientation. Data obtained in this study can help provide insight on how muscle injuries are caused, ranging from low energy strains to high rate blast events, and can also be used in developing computational injury models.

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Schuster, P. J., Chou, C. C., Prasad, P., and Jayaraman, G., 2000, “Development and Validation of a Pedestrian Lower Limb Non-Linear 3-D Finite Element Model,” Stapp Car Crash J., 44(1), pp. 315–334. [PubMed]
Van der Horst, M. J., Van der Simms, C. K., Van Maasdam, R., and Leerdam, P. J. C., 2005, “Occupant Lower Leg Injury Assessment in Landmine Detonations Under a Vehicle,” IUTAM Proc. Impact Biomech., 124, pp. 41–49. [CrossRef]
Lemos, R. R., Epstein, M., Herzog, W., and Wyvill, B., 2004, “A Framework for Structured Modeling of Skeletal Muscle,” Comput. Methods Biomech. Biomed. Eng., 7(6), pp. 305–317. [CrossRef]
Van Loocke, M., Lyons, C. G., and Simms, C. K., 2006, “A Validated Model of Passive Muscle in Compression,” J. Biomech., 39(16), pp. 2999–3009. [CrossRef] [PubMed]
Linder-Ganz, E., and Gefen, A., 2004, “Mechanical Compression-Induced Pressure Sores in Rat Hindlimb: Muscle Stiffness, Histology, and Computational Models,” J. Appl. Physiol., 96(6), pp. 2034–2049. [CrossRef] [PubMed]
Palevski, A., Glaich, I., Portnoy, S., Linder-Ganz, E., and Gefen, A., 2006, “Stress Relaxation of Porcine Gluteus Muscle Subjected to Sudden Transverse Deformation as Related to Pressure Sore Modeling,” ASME J. Biomech. Eng., 128(5), pp. 782–787. [CrossRef]
Basford, J. R., Jenkyn, T. R., An, K.-N., Ehman, R. L., Heers, G., and Kaufman, K. R., 2002, “Evaluation of Healthy and Diseased Muscle With Magnetic Resonance Elastography,” Arch. Phys. Med. Rehabil., 83(11), pp. 1530–1536. [CrossRef] [PubMed]
Lin, R., Chang, G., and Chang, L., 1999, “Biomechanical Properties of Muscle–Tendon Unit Under High-Speed Passive Stretch,” Clin. Biomech. (Bristol, Avon), 14(6), pp. 412–417. [CrossRef]
Crawford, S. K., Haas, C., Butterfield, T. A., Wang, Q., Zhang, X., Zhao, Y., and Best, T. M., 2014, “Effects of Immediate vs. Delayed Massage-Like Loading on Skeletal Muscle Viscoelastic Properties Following Eccentric Exercise,” Clin. Biomech., 29(6), pp. 671–678. [CrossRef]
Best, T. M., McElhaney, J., Garrett, W. E., and Myers, B. S., 1994, “Characterization of the Passive Responses of Live Skeletal Muscle Using the Quasi-Linear Theory of Viscoelasticity,” J. Biomech., 27(4), pp. 413–419. [CrossRef] [PubMed]
Davis, J., Kaufman, K. R., and Lieber, R. L., 2003, “Correlation Between Active and Passive Isometric Force and Intramuscular Pressure in the Isolated Rabbit Tibialis Anterior Muscle,” J. Biomech., 36(4), pp. 505–512. [CrossRef] [PubMed]
Grover, J. P., Corr, D. T., Toumi, H., Manthei, D. M., Oza, A. L., Vanderby, R., and Best, T. M., 2007, “The Effect of Stretch Rate and Activation State on Skeletal Muscle Force in the Anatomical Range,” Clin. Biomech. (Bristol, Avon), 22(3), pp. 360–368. [CrossRef]
Sun, J. S., Tsuang, Y. H., Liu, T. K., Hang, Y. S., Cheng, C. K., and Lee, W. W. L., 1995, “Viscoplasticity of Rabbit Skeletal Muscle Under Dynamic Cyclic Loading,” Clin. Biomech. (Bristol, Avon), 10(5), pp. 258–262. [CrossRef]
Taniguchi, T., Yamamoto, S., Hayakawa, A., Tanaka, E., Kimpara, H., and Miki, K., 2003, “Extension Rate and Muscle-Tonus Dependence of the Failure Properties of Rabbit Tibialis Anterior Muscle,” Abstracts for the Summer Bioengineering Conference, Sonesta Beach Resort, Key Biscayne, FL, June 25–29, pp. 1219–1220.
Aimedieu, P., Mitton, D., Faure, J. P., Denninger, L., and Lavaste, F., 2003, “Dynamic Stiffness and Damping of Porcine Muscle Specimens,” Med. Eng. Phys., 25(9), pp. 795–799. [CrossRef] [PubMed]
Anderson, J., Li, Z., and Goubel, F., 2001, “Passive Stiffness Is Increased in Soleus Muscle of Desmin Knockout Mouse,” Muscle Nerve, 24(8), pp. 1090–1092. [CrossRef] [PubMed]
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,” J. Appl. Physiol., 85(3), pp. 1011–1016. [PubMed]
Morrow, D. A., Haut Donahue, T. L., Odegard, G. M., and Kaufman, K. R., 2010, “Transversely Isotropic Tensile Material Properties of Skeletal Muscle Tissue,” J. Mech. Behav. Biomed. Mater., 3(1), pp. 124–129. [CrossRef] [PubMed]
Anderson, J., Joumaa, V., Stevens, L., Neagoe, C., Li, Z., Mounier, Y., Linke, W. A., and Goubel, F., 2002, “Passive Stiffness Changes in Soleus Muscles From Desmin Knockout Mice Are Not Due to Titin Modifications,” Pflügers Arch.: Eur. J. Physiol., 444(6), pp. 771–776. [CrossRef]
Christensen, M., Young, R. D., Lawson, M. A., Larsen, L. M., and Purslow, P. P., 2004, “Effect of Added μ-Calpain and Post-Mortem Storage on the Mechanical Properties of Bovine Single Muscle Fibres Extended to Fracture,” Meat Sci., 66(1), pp. 105–112. [CrossRef] [PubMed]
Lieber, R. L., 2010, Skeletal Muscle Structure, Function, and Plasticity, Lippincott Williams and Wilkins, Philadelphia, PA.
Mathur, A. B., Collinsworth, A. M., Reichert, W. M., Kraus, W. E., and Truskey, G. A., 2001, “Endothelial, Cardiac Muscle and Skeletal Muscle Exhibit Different Viscous and Elastic Properties as Determined by Atomic Force Microscopy,” J. Biomech., 34(12), pp. 1545–1553. [CrossRef] [PubMed]
Gefen, A., Gefen, N., Linder-Ganz, E., and Margulies, S. S., 2005, “In Vivo Muscle Stiffening Under Bone Compression Promotes Deep Pressure Sores,” ASME J. Biomech. Eng., 127(3), pp. 512–524. [CrossRef]
Gennisson, J.-L., Catheline, S., Chaffaï, S., and Fink, M., 2003, “Transient Elastography in Anisotropic Medium: Application to the Measurement of Slow and Fast Shear Wave Speeds in Muscles,” J. Acoust. Soc. Am., 114(1), pp. 536–541. [CrossRef] [PubMed]
Hawkins, D., and Bey, M., 1997, “Muscle and Tendon Force-Length Properties and Their Interactions In Vivo,” J. Biomech., 30(1), pp. 63–70. [CrossRef] [PubMed]
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,” ASME J. Biomech. Eng., 122(1), pp. 9–14. [CrossRef]
Dresner, M. A., Rose, G. H., Rossman, P. J., Muthupillai, R., Manduca, A., and Ehman, R. L., 2001, “Magnetic Resonance Elastography of Skeletal Muscle,” J. Magn. Reson. Imaging, 13(2), pp. 269–276. [CrossRef] [PubMed]
Uffmann, K., Maderwald, S., Ajaj, W., Galban, C. G., Mateiescu, S., Quick, H. H., and Ladd, M. E., 2004, “in vivo Elasticity Measurements of Extremity Skeletal Muscle With MR Elastography,” NMR Biomed., 17(4), pp. 181–190. [CrossRef] [PubMed]
Gareis, H., Solomonow, M., Baratta, R., Best, R., and D'Ambrosia, R., 1992, “The Isometric Length-Force Models of Nine Different Skeletal Muscles,” J. Biomech., 25(8), pp. 903–916. [CrossRef] [PubMed]
Muhl, Z. F., 1982, “Active Length-Tension Relation and the Effect of Muscle Pinnation on Fiber Lengthening,” J. Morphol., 173(3), pp. 285–292. [CrossRef] [PubMed]
Myers, B. S., Woolley, C. T., Slotter, T. L., Garrett, W. E., and Best, T. M., 1998, “The Influence of Strain Rate on the Passive and Stimulated Engineering Stress—Large Strain Behavior of the Rabbit Tibialis Anterior Muscle,” ASME J. Biomech. Eng., 120(1), pp. 126–132. [CrossRef]
Bosboom, E. M., Hesselink, M. K., Oomens, C. W., Bouten, C. V., Drost, M. R., and Baaijens, F. P., 2001, “Passive Transverse Mechanical Properties of Skeletal Muscle Under In Vivo Compression,” J. Biomech., 34(10), pp. 1365–1368. [CrossRef] [PubMed]
Van Loocke, M., Lyons, C. G., and Simms, C. K., 2008, “Viscoelastic Properties of Passive Skeletal Muscle in Compression: Stress-Relaxation Behaviour and Constitutive Modelling,” J. Biomech., 41(7), pp. 1555–1566. [CrossRef] [PubMed]
Van Loocke, M., Simms, C. K., and Lyons, C. G., 2009, “Viscoelastic Properties of Passive Skeletal Muscle in Compression-Cyclic Behaviour,” J. Biomech., 42(8), pp. 1038–1048. [CrossRef] [PubMed]
Nie, X., Cheng, J.-I., Chen, W. W., and Weerasooriya, T., 2011, “Dynamic Tensile Response of Porcine Muscle,” ASME J. Appl. Mech., 78(2), p. 021009. [CrossRef]
Simon, B. R., 1992, “Multiphase Poroelastic Finite Element Models for Soft Tissue Structures,” ASME Appl. Mech. Rev., 45(6), pp. 191–218. [CrossRef]
Spilker, R. L., Suh, J. K., and Mow, V. C., 1992, “A Finite Element Analysis of the Indentation Stress-Relaxation Response of Linear Biphasic Articular Cartilage,” ASME J. Biomech. Eng., 114(2), pp. 191–201. [CrossRef]
Yang, M., and Taber, L. A., 1991, “The Possible Role of Poroelasticity in the Apparent Viscoelastic Behavior of Passive Cardiac Muscle,” J. Biomech., 24(7), pp. 587–597. [CrossRef] [PubMed]
Yang, M., and Taber, L. A., 1991, “The Possible Role of Poroelasticity in the Apparent Viscoelastic Behavior of Passive Cardiac Muscle,” J. Biomech., 24(7), pp. 587–597. [CrossRef] [PubMed]


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Fig. 3

Stress–strain response for fresh muscle in compression in the longitudinal direction at three strain rates

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Fig. 4

Stress–strain response for fresh muscle in compression in the transverse direction at three strain rates

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Fig. 2

Experimental setup (Biomomentum MACH-1TM) for compression testing

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Fig. 1

Schematic showing fiber direction in the longitudinal (a) and transverse (b) directions

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Fig. 5

Stress–strain response for fresh porcine muscle in compression, showing loading and unloading in the longitudinal direction

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Fig. 6

Stress–strain responses for fresh muscle in compression, comparing the longitudinal and transverse directions at strain rates of 0.1 s−1 (a), 0.01 s−1 (b), and 0.001 s−1 (c). # denotes statistical difference between peak response of longitudinal and transverse data.

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Fig. 7

Micrograph of H&E stained 0% strain (control) muscle with scale bar in micrometers

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Fig. 8

Micrograph of muscle compressed to 30% strain at 0.1 s−1 in the longitudinal (a) and transverse (b) directions with scale bar in micrometers and arrows showing the loading direction

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Fig. 9

Area fraction and mean area (mean with standard deviation error bars) values for all loading conditions. * denotes statistical difference from control and # denotes statistical difference from transverse loaded specimens at 50% strain.




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