1 CHARACTERISING SKELETAL MUSCLE UNDER 2 LARGE STRAIN USING ECCENTRIC & FOURIER 3 TRANSFORMATION-RHEOLOGY

21 Characterising the passive anisotropic properties of soft tissues has been largely limited to the 22 linear viscoelastic regime and shear loading is rarely done in the large deformation regime, 23 despite the physiological significance of such properties. This paper demonstrates the use of 24 eccentric rheology, which allows the anisotropy of skeletal muscle to be investigated. The large 25 amplitude oscillatory strain properties of skeletal muscle were also investigated using Fourier 26 Transform rheology. Histology was used to qualitatively assess the microstructure changes 27 induced by large strain. Results showed that skeletal muscle was strongly anisotropic in the 28 linear regime. The storage and loss moduli were found to be significantly different (p < 0.05) 29 between the three fibre alignment groups; for the group tested with fibres perpendicular to plane 30 of shear was 12.3±1.3 kPa and 3.0±0.35 kPa, parallel to shear direction was 10.6±1.2 kPa and 31 2.4±0.23 kPa, and perpendicular to shear direction was 5.5±0.90 kPa and 1.3±0.21 kPa. The 32 appearance and growth of higher order harmonics at large strain was different in the three 33 testing directions indicating that the anisotropy of muscle affects skeletal muscle behaviour in 34 the nonlinear regime. Histological analysis showed an increasing destruction of extracellular 35 matrix and the rearrangement of fibres with increasing strain indicating mechanical damage at 36 strains of larger than 10%. These microstructural changes could contribute to the complex 37 nonlinear behaviour in skeletal muscle. This paper demonstrates a method of characterising the 38 anisotropic properties in skeletal muscle under large strain whilst giving meaningful information 39 on the physical response of tissue at various strains. 40

[1]  L. Bilston,et al.  Measurement of Passive Skeletal Muscle Mechanical Properties In Vivo: Recent Progress, Clinical Applications, and Remaining Challenges , 2015, Annals of Biomedical Engineering.

[2]  Lynne E Bilston,et al.  Characterising soft tissues under large amplitude oscillatory shear and combined loading. , 2013, Journal of biomechanics.

[3]  Cwj Cees Oomens,et al.  A novel method for visualising and quantifying through-plane skin layer deformations. , 2012, Journal of the mechanical behavior of biomedical materials.

[4]  Kevin M. Moerman,et al.  THE ANISOTROPIC MECHANICAL BEHAVIOUR OF PASSIVE SKELETAL MUSCLE TISSUE SUBJECTED TO LARGE TENSILE STRAIN , 2012 .

[5]  S. Koehler,et al.  Eccentric Rheometry for Viscoelastic Characterization of Small, Soft, Anisotropic, and Irregularly Shaped Biopolymer Gels and Tissue Biopsies , 2012, Annals of Biomedical Engineering.

[6]  Gareth H. McKinley,et al.  A review of nonlinear oscillatory shear tests: Analysis and application of large amplitude oscillatory shear (LAOS) , 2011 .

[7]  Silvia S Blemker,et al.  A mathematical model of force transmission from intrafascicularly terminating muscle fibers. , 2011, Journal of biomechanics.

[8]  Appaji Panchangam,et al.  Non-uniform distribution of strain during stretch of relaxed skeletal muscle fibers from rat soleus muscle , 2011, Journal of Muscle Research and Cell Motility.

[9]  Tusit Weerasooriya,et al.  Dynamic Tensile Response of Porcine Muscle , 2011 .

[10]  Richard L Lieber,et al.  Elucidation of extracellular matrix mechanics from muscle fibers and fiber bundles. , 2011, Journal of biomechanics.

[11]  S. Nicolle,et al.  Dehydration effect on the mechanical behaviour of biological soft tissues: observations on kidney tissues. , 2010, Journal of the mechanical behavior of biomedical materials.

[12]  Peter P. Purslow,et al.  Muscle fascia and force transmission. , 2010, Journal of bodywork and movement therapies.

[13]  Lynne E Bilston,et al.  The effects of preconditioning strain on measured tissue properties. , 2009, Journal of biomechanics.

[14]  C. G. Lyons,et al.  Viscoelastic properties of passive skeletal muscle in compression-cyclic behaviour. , 2009, Journal of biomechanics.

[15]  Kyu Hyun,et al.  Establishing a New Mechanical Nonlinear Coefficient Q from FT-Rheology: First Investigation of Entangled Linear and Comb Polymer Model Systems , 2009 .

[16]  A. Hosoi,et al.  New measures for characterizing nonlinear viscoelasticity in large amplitude oscillatory shear , 2008 .

[17]  J. van Dommelen,et al.  The influence of test conditions on characterization of the mechanical properties of brain tissue. , 2008, Journal of biomechanical engineering.

[18]  K. Ahn,et al.  Fourier-transform rheology under medium amplitude oscillatory shear for linear and branched polymer melts , 2007 .

[19]  T. Letellier,et al.  Physical continuity of the perimysium from myofibers to tendons: involvement in lateral force transmission in skeletal muscle. , 2007, Journal of structural biology.

[20]  A. Yoganathan,et al.  Biaixal Stress–Stretch Behavior of the Mitral Valve Anterior Leaflet at Physiologic Strain Rates , 2006, Annals of Biomedical Engineering.

[21]  G. Schlatter,et al.  Non Linear Rheology for Long Chain Branching characterization, comparison of two methodologies : Fourier Transform Rheology and Relaxation. , 2004 .

[22]  P A Huijing,et al.  Muscle as a collagen fiber reinforced composite: a review of force transmission in muscle and whole limb. , 1999, Journal of biomechanics.

[23]  T. Nishimura,et al.  Structural changes in the intramuscular connective tissue during development of bovine semitendinosus muscle. , 1996, Tissue & cell.

[24]  Peter P. Purslow,et al.  The morphology and mechanical properties of endomysium in series-fibred muscles: variations with muscle length , 1994, Journal of Muscle Research & Cell Motility.

[25]  J. Mcelhaney,et al.  Characterization of the passive responses of live skeletal muscle using the quasi-linear theory of viscoelasticity. , 1994, Journal of biomechanics.

[26]  E. Lamersa,et al.  Large amplitude oscillatory shear properties of human skin , 2016 .

[27]  Kunal Choudhuri.  Large Amplitude Oscillatory Shear (LAOS) Rheology of Pickering Emulsions , 2016 .

[28]  Paul Ackermans,et al.  Linear shear response of the upper skin layers. , 2011, Biorheology.

[29]  E. Tanaka,et al.  A novel constitutive model of skeletal muscle taking into account anisotropic damage. , 2010, Journal of the mechanical behavior of biomedical materials.

[30]  Kenton R Kaufman,et al.  Transversely isotropic tensile material properties of skeletal muscle tissue. , 2010, Journal of the mechanical behavior of biomedical materials.

[31]  C. G. Lyons,et al.  A validated model of passive muscle in compression. , 2006, Journal of biomechanics.

[32]  J. van Dommelen,et al.  The mechanical behaviour of brain tissue: large strain response and constitutive modelling. , 2006, Biorheology.

[33]  C. Oomens,et al.  Passive transverse mechanical properties as a function of temperature of rat skeletal muscle in vitro. , 2005, Biorheology.

[34]  van Jaw Hans Dommelen,et al.  Mechanical behaviour of brain tissue , 2004 .

[35]  K. Ahn,et al.  Nonlinear response of complex fluids under LAOS (large amplitude oscillatory shear) flow , 2003 .

[36]  R. Meijer,et al.  Characterisation of Anisotropic and Non-linear Behaviour of Human Skin In Vivo. , 1999, Computer methods in biomechanics and biomedical engineering.

[37]  T. Nishimura,et al.  Structural weakening of intramuscular connective tissue during conditioning of beef. , 1995, Meat science.

[38]  T. Nishimura,et al.  Structural changes in endomysium and perimysium during post-mortem aging of chicken Semitendinosus muscle-Contribution of structural weakening of intramuscular connective tissue to meat tenderization. , 1994, Meat science.

[39]  T. W. Ridler,et al.  Picture thresholding using an iterative selection method. , 1978 .

[40]  F. G. Evans,et al.  Strength of biological materials , 1970 .