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Research Papers

Mechanical Characteristics of Bovine Glisson's Capsule as a Model Tissue for Soft Collagenous Membranes

[+] Author and Article Information
Kevin Bircher

Institute for Mechanical Systems,
ETH Zurich,
Zurich 8092, Switzerland
e-mail: bircher@imes.mavt.ethz.ch

Alexander E. Ehret

Institute for Mechanical Systems,
ETH Zurich,
Zurich 8092, Switzerland;
Empa,
Swiss Federal Laboratories
for Materials Science and Technology,
Dübendorf 8600, Switzerland
e-mail: ehret@imes.mavt.ethz.ch

Edoardo Mazza

Institute for Mechanical Systems,
ETH Zurich,
Zurich 8092, Switzerland;
Empa,
Swiss Federal Laboratories
for Materials Science and Technology,
Dübendorf 8600, Switzerland
e-mail: mazza@imes.mavt.ethz.ch

Manuscript received December 18, 2015; final manuscript received June 3, 2016; published online June 30, 2016. Assoc. Editor: Guy M. Genin.

J Biomech Eng 138(8), 081005 (Jun 30, 2016) (11 pages) Paper No: BIO-15-1651; doi: 10.1115/1.4033917 History: Received December 18, 2015; Revised June 03, 2016

An extensive multiaxial experimental campaign on the monotonic, time- and history-dependent mechanical response of bovine Glisson's capsule (GC) is presented. Reproducible characteristics were observed such as J-shaped curves in uniaxial and biaxial configurations, large lateral contraction, cyclic tension softening, large tension relaxation, and moderate creep strain accumulation. The substantial influence of the reference state selection on the kinematic response and the tension versus stretch curves is demonstrated and discussed. The parameters of a large-strain viscoelastic constitutive model were determined based on the data of uniaxial tension relaxation experiments. The model is shown to well predict the uniaxial and biaxial viscoelastic responses in all other configurations. GC, the corresponding model, and the experimental protocols are proposed as a useful basis for future studies on the relation between microstructure and tissue functionality and on the factors influencing the mechanical response of soft collagenous membranes.

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References

Kuntz, E. , and Kuntz, H.-D. , 2006, Hepatology, Principles and Practice: History, Morphology, Biochemistry, Diagnostics, Clinic, Therapy, Springer Science & Business Media, Berlin, Germany.
Schünke, M. , Schulte, E. , and Schumacher, U. , 2007, THIEME Atlas of Anatomy: Neck and Internal Organs, Thieme, Stuttgart, Germany.
Arnold, G. , Gressner, A. , and Clahsen, H. , 1976, “ Experimental Studies of the Historheology of the Liver Capsule (experimentelle untersuchungen zur historheologie der leberkapsel),” Anat. Anz., 142(3), pp. 180–191.
Snedeker, J. , Niederer, P. , Schmidlin, F. , Farshad, M. , Demetropoulos, C. , Lee, J. , and Yang, K. , 2005, “ Strain-Rate Dependent Material Properties of the Porcine and Human Kidney Capsule,” J. Biomech., 38(5), pp. 1011–1021. [CrossRef] [PubMed]
Stingl, J. , Báca, V. , Cech, P. , Kovanda, J. , Kovandová, H. , Mandys, V. , Rejmontová, J. , and Sosna, B. , 2002, “ Morphology and Some Biomechanical Properties of Human Liver and Spleen,” Surg. Radiol. Anat., 24(5), pp. 285–289. [CrossRef] [PubMed]
Tamura, A. , Omori, K. , Miki, K. , Lee, J. , Yang, K. , and King, A. , 2002, “ Mechanical Characterization of Porcine Abdominal Organs,” Stapp Car Crash J., 46, pp. 55–69. [PubMed]
Brunon, A. , Bruyère-Garnier, K. , and Coret, M. , 2010, “ Mechanical Characterization of Liver Capsule Through Uniaxial Quasi-Static Tensile Tests Until Failure,” J. Biomech., 43(11), pp. 2221–2227. [CrossRef] [PubMed]
Tinkoff, G. , Esposito, T. , Reed, J. , Kilgo, P. , Fildes, J. , Pasquale, M. , and Meredith, J. , 2008, “ American Association for the Surgery of Trauma Organ Injury Scale I: Spleen, Liver, and Kidney, Validation Based on the National Trauma Data Bank,” J. Am. Coll. Surg., 207(5), pp. 646–655. [CrossRef] [PubMed]
Hollenstein, M. , 2011, “ Mechanics of the Human Liver: Experiments and Modeling,” Ph.D. thesis, ETH-Zürich, Zürich, Switzerland.
Umale, S. , Chatelin, S. , Bourdet, N. , Deck, C. , Diana, M. , Dhumane, P. , Soler, L. , Marescaux, J. , and Willinger, R. , 2011, “ Experimental In Vitro Mechanical Characterization of Porcine Glisson's Capsule and Hepatic Veins,” J. Biomech., 44(9), pp. 1678–1683. [CrossRef] [PubMed]
Gressner, A. , Clahsen, H. , Arnold, G. , and Fessel, H. , 1977, “ Biomechanical Investigations of the Liver Capsule (biomechanische untersuchungen der leberkapsel),” Res. Exp. Med., 171(2), pp. 191–199. [CrossRef]
Arnold, G. , Gressner, A. , Clahsen, H. , and Krönchen, A. , 1977, “ On the Biomechanical Function of the Liver Capsule,” Experientia, 33(8), pp. 1089–1091. [CrossRef] [PubMed]
Brunon, A. , Bruyère-Garnier, K. , and Coret, M. , 2011, “ Characterization of the Nonlinear Behaviour and the Failure of Human Liver Capsule Through Inflation Tests,” J. Mech. Behav. Biomed. Mater., 4(8), pp. 1572–1581. [CrossRef] [PubMed]
Jayyosi, C. , Coret, M. , and Bruyère-Garnier, K. , 2013, “ Imaging of the Human Glisson's Capsule by Two-Photon Excitation Microscopy and Mechanical Characterisation by Uniaxial Tensile Tests,” Comput. Methods Biomech. Biomed. Eng., 16(Suppl. 1), pp. 282–283. [CrossRef]
Jayyosi, C. , Fargier, G. , Coret, M. , and Bruyere-Garnier, K. , 2014, “ Photobleaching as a Tool to Measure the Local Strain Field in Fibrous Membranes of Connective Tissues,” Acta Biomater., 10(6), pp. 2591–2601. [CrossRef] [PubMed]
Carter, F. , Frank, T. , Davies, P. , McLean, D. , and Cuschieri, A. , 2001, “ Measurements and Modelling of the Compliance of Human and Porcine Organs,” Med. Image Anal., 5(4), pp. 231–236. [CrossRef] [PubMed]
Ottensmeyer, M. , 2002, “ Tempest 1-D: An Instrument for Measuring Solid Organ Soft Tissue Properties,” Exp. Tech., 26(3), pp. 48–50. [CrossRef]
Samur, E. , Sedef, M. , Basdogan, C. , Avtan, L. , and Duzgun, O. , 2007, “ A Robotic Indenter for Minimally Invasive Measurement and Characterization of Soft Tissue Response,” Med. Image Anal., 11(4), pp. 361–373. [CrossRef] [PubMed]
Nava, A. , Mazza, E. , Furrer, M. , Villiger, P. , and Reinhart, W. , 2008, “ In Vivo Mechanical Characterization of Human Liver,” Med. Image Anal., 12(2), pp. 203–216. [CrossRef] [PubMed]
Mazza, E. , Nava, A. , Hahnloser, D. , Jochum, W. , and Bajka, M. , 2007, “ The Mechanical Response of Human Liver and Its Relation to Histology: An In Vivo Study,” Med. Image Anal., 11(6), pp. 663–672. [CrossRef] [PubMed]
Buerzle, W. , 2014, “ Mechanical Characterization and Modeling of Human Fetal Membrane Tissue,” Ph.D. thesis, ETH-Zürich, Zürich, Switzerland.
Mauri, A. , Perrini, M. , Ehret, A. , De Focatiis, D. , and Mazza, E. , 2015, “ Time-Dependent Mechanical Behavior of Human Amnion: Macroscopic and Microscopic Characterization,” Acta Biomater., 11(1), pp. 314–323. [CrossRef] [PubMed]
Perrini, M. , Mauri, A. , Ehret, A. , Ochsenbein-Kölble, N. , Zimmermann, R. , Ehrbar, M. , and Mazza, E. , 2015, “ Mechanical and Microstructural Investigation of the Cyclic Behavior of Human Amnion,” ASME J. Biomech. Eng., 137(6), p. 061010. [CrossRef]
Ohtani, O. , 1988, “ Three-Dimensional Organization of the Collagen Fibrillar Framework of the Human and Rat Livers,” Arch. Histol. Cytol., 51(5), pp. 473–488. [CrossRef] [PubMed]
Martinez-Hernandez, A. , and Amenta, P. , 1993, “ The Hepatic Extracellular Matrix. I. Components and Distribution in Normal Liver,” Virchows Arch. A: Pathol. Anat. Histol., 423(1), pp. 1–11. [CrossRef]
Porto, L. , Chevallier, M. , Peyrol, S. , Guerret, S. , and Grimaud, J.-A. , 1990, “ Elastin in Human, Baboon, and Mouse Liver: An Immunohistochemical and Immunoelectron Microscopic Study,” Anat. Rec., 228(4), pp. 392–404. [CrossRef] [PubMed]
Rauterberg, J. , Voss, B. , Pott, P. D. G. , and Gerlach, U. , 1981, “ Connective Tissue Components of the Normal and Fibrotic Liver,” Klin. Wochenschr., 59(14), pp. 767–779. [CrossRef] [PubMed]
Stenman, S. , and Vaheri, A. , 1978, “ Distribution of a Major Connective Tissue Protein, Fibronectin, in Normal Human Tissues,” J. Exp. Med., 147(4), pp. 1054–1064. [CrossRef] [PubMed]
Lee, J. , Kim, S. , Kwack, S. , Kim, C. , Moon, T. , Lee, S. , Cho, M. , Kang, D. , and Kim, G. , 2008, “ Hepatic Capsular and Subcapsular Pathologic Conditions: Demonstration With CT and MR Imaging,” Radiographics, 28(5), pp. 1307–1323. [CrossRef] [PubMed]
Jayyosi, C. , Coret, M. , and Bruyère-Garnier, K. , 2016, “ Characterizing Liver Capsule Microstructure Via In Situ Bulge Test Coupled With Multiphoton Imaging,” J. Mech. Behav. Biomed. Mater., 54, pp. 229–243. [CrossRef] [PubMed]
Buerzle, W. , Haller, C. , Jabareen, M. , Egger, J. , Mallik, A. , Ochsenbein-Koelble, N. , Ehrbar, M. , and Mazza, E. , 2013, “ Multiaxial Mechanical Behavior of Human Fetal Membranes and Its Relationship to Microstructure,” Biomech. Model. Mechanobiol., 12(4), pp. 747–762. [CrossRef] [PubMed]
Hopf, R. , Bernardi, L. , Menze, J. , Zündel, M. , Mazza, E. , and Ehret, A. , 2016, “ Experimental and Theoretical Analyses of the Age-Dependent Large-Strain Behavior of Sylgard 184 (10:1) Silicone Elastomer,” J. Mech. Behav. Biomed. Mater., 60, pp. 425–437. [CrossRef] [PubMed]
Mauri, A. , Ehret, A. , Perrini, M. , Maake, C. , Ochsenbein-Koelble, N. , Ehrbar, M. , Oyen, M. , and Mazza, E. , 2015, “ Deformation Mechanisms of Human Amnion: Quantitative Studies Based on Second Harmonic Generation Microscopy,” J. Biomech., 48(9), pp. 1606–1613. [CrossRef] [PubMed]
Hollenstein, M. , Nava, A. , Valtorta, D. , Snedeker, J. , and Mazza, E. , 2006, “ Mechanical Characterization of the Liver Capsule and Parenchyma,” Biomedical Simulation (Lecture Notes in Computer Science, Vol. 4072), Springer-Verlag, Berlin, Germany, pp. 150–158.
Mauri, A. , Ehret, A. , De Focatiis, D. S. A. , and Mazza, E. , “ A Model for the Compressible, Viscoelastic Behavior of Human Amnion Addressing Tissue Variability Through a Single Parameter,” Biomech. Model. Mechanobiol, epub.
Rubin, M. , and Bodner, S. , 2002, “ A Three-Dimensional Nonlinear Model for Dissipative Response of Soft Tissue,” Int. J. Solids Struct., 39(19), pp. 5081–5099. [CrossRef]
Rubin, M. , and Papes, O. , 2011, “ Advantages of Formulating Evolution Equations for Elastic-Viscoplastic Materials in Terms of the Velocity Gradient Instead of the Spin Tensor,” J. Mech. Mater. Struct., 6(1–4), pp. 529–543. [CrossRef]
Hollenstein, M. , Jabareen, M. , and Rubin, M. , 2013, “ Modeling a Smooth Elastic-Inelastic Transition With a Strongly Objective Numerical Integrator Needing No Iteration,” Comput. Mech., 52(3), pp. 649–667. [CrossRef]
Buerzle, W. , and Mazza, E. , 2013, “ On the Deformation Behavior of Human Amnion,” J. Biomech., 46(11), pp. 1777–1783. [CrossRef] [PubMed]
Vader, D. , Kabla, A. , Weitz, D. , and Mahadevan, L. , 2009, “ Strain-Induced Alignment in Collagen Gels,” PLoS One, 4(6), p. e5902. [CrossRef] [PubMed]
Lake, S. , and Barocas, V. , 2011, “ Mechanical and Structural Contribution of Non-Fibrillar Matrix in Uniaxial Tension: A Collagen-Agarose Co-Gel Model,” Ann. Biomed. Eng., 39(7), pp. 1891–1903. [CrossRef] [PubMed]
Lynch, H. , Johannessen, W. , Wu, J. , Jawa, A. , and Elliott, D. , 2003, “ Effect of Fiber Orientation and Strain Rate on the Nonlinear Uniaxial Tensile Material Properties of Tendon,” ASME J. Biomech. Eng., 125(5), pp. 726–731. [CrossRef]
Hewitt, J. , Guilak, F. , Glisson, R. , and Parker Vail, T. , 2001, “ Regional Material Properties of the Human Hip Joint Capsule Ligaments,” J. Orthop. Res., 19(3), pp. 359–364. [CrossRef] [PubMed]
Jayyosi, C. , 2015, “ Mechanical and Microstructural Characterization of Glisson's Capsule Behavior up to Failure, for the Prediction of Human Hepatic Tissues Injury Risk,” Ph.D. thesis, IFSTTAR, Grenoble, France.
Umale, S. , Deck, C. , Bourdet, N. , Dhumane, P. , Soler, L. , Marescaux, J. , and Willinger, R. , 2012, “ Experimental Mechanical Characterization of Abdominal Organs: Liver, Kidney & Spleen,” J. Mech. Behav. Biomed. Mater., 17, pp. 22–33. [CrossRef] [PubMed]
Itskov, M. , Ehret, A. , and Mavrilas, D. , 2006, “ A Polyconvex Anisotropic Strain-Energy Function for Soft Collagenous Tissues,” Biomech. Model. Mechanobiol., 5(1), pp. 17–26. [CrossRef] [PubMed]
Sacks, M. , and Chuong, C. , 1998, “ Orthotropic Mechanical Properties of Chemically Treated Bovine Pericardium,” Ann. Biomed. Eng., 26(5), pp. 892–902. [CrossRef] [PubMed]
Sacks, M. , Chuong, C. , and More, R. , 1994, “ Collagen Fiber Architecture of Bovine Pericardium,” ASAIO J., 40(3), pp. M632–M637. [CrossRef] [PubMed]
Mavrilas, D. , Sinouris, E. , Vynios, D. , and Papageorgakopoulou, N. , 2005, “ Dynamic Mechanical Characteristics of Intact and Structurally Modified Bovine Pericardial Tissues,” J. Biomech., 38(4), pp. 761–768. [CrossRef] [PubMed]
Boyce, B. , Jones, R. , Nguyen, T. , and Grazier, J. , 2007, “ Stress-Controlled Viscoelastic Tensile Response of Bovine Cornea,” J. Biomech., 40(11), pp. 2367–2376. [CrossRef] [PubMed]
Woo, S.-Y. , Gomez, M. , and Akeson, W. , 1981, “ The Time and History-Dependent Viscoelastic Properties of the Canine Medial Collateral Ligament,” ASME J. Biomech. Eng., 103(4), pp. 293–298. [CrossRef]
Sverdlik, A. , and Lanir, Y. , 2002, “ Time-Dependent Mechanical Behavior of Sheep Digital Tendons, Including the Effects of Preconditioning,” ASME J. Biomech. Eng., 124(1), pp. 78–84. [CrossRef]
Sung, H.-W. , Chang, Y. , Chiu, C.-T. , Chen, C.-N. , and Liang, H.-C. , 1999, “ Crosslinking Characteristics and Mechanical Properties of a Bovine Pericardium Fixed With a Naturally Occurring Crosslinking Agent,” J. Biomed. Mater. Res., 47(2), pp. 116–126. [CrossRef] [PubMed]
Ehret, A. , Hollenstein, M. , Mazza, E. , and Itskov, M. , 2012, “ Porcine Dermis in Uniaxial Cyclic Loading: Sample Preparation, Experimental Results and Modeling,” J. Mech. Mater. Struct., 6(7–8), pp. 1125–1135.
Thornton, G. , Oliynyk, A. , Frank, C. , and Shrive, N. , 1997, “ Ligament Creep Cannot Be Predicted From Stress Relaxation at Low Stress: A Biomechanical Study of the Rabbit Medial Collateral Ligament,” J. Orthop. Res., 15(5), pp. 652–656. [CrossRef] [PubMed]
Provenzano, P. , Lakes, R. , Keenan, T. , and Vanderby, R., Jr. , 2001, “ Nonlinear Ligament Viscoelasticity,” Ann. Biomed. Eng., 29(10), pp. 908–914. [CrossRef] [PubMed]
Liao, J. , Yang, L. , Grashow, J. , and Sacks, M. , 2007, “ The Relation Between Collagen Fibril Kinematics and Mechanical Properties in the Mitral Valve Anterior Leaflet,” ASME J. Biomech. Eng., 129(1), pp. 78–87. [CrossRef]
Grashow, J. , Sacks, M. , Liao, J. , and Yoganathan, A. , 2006, “ Planar Biaxial Creep and Stress Relaxation of the Mitral Valve Anterior Leaflet,” Ann. Biomed. Eng., 34(10), pp. 1509–1518. [CrossRef] [PubMed]
Purslow, P. , Wess, T. , and Hukins, D. , 1998, “ Collagen Orientation and Molecular Spacing During Creep and Stress-Relaxation in Soft Connective Tissues,” J. Exp. Biol., 201(1), pp. 135–142. [PubMed]
Screen, H. , Seto, J. , Krauss, S. , Boesecke, P. , and Gupta, H. , 2011, “ Extrafibrillar Diffusion and Intrafibrillar Swelling at the Nanoscale Are Associated With Stress Relaxation in the Soft Collagenous Matrix Tissue of Tendons,” Soft Matter, 7(23), pp. 11243–11251. [CrossRef]
Svensson, R. , Hassenkam, T. , Hansen, P. , and Peter Magnusson, S. , 2010, “ Viscoelastic Behavior of Discrete Human Collagen Fibrils,” J. Mech. Behav. Biomed. Mater., 3(1), pp. 112–115. [CrossRef] [PubMed]
Thornton, G. , Frank, C. , and Shrive, N. , 2001, “ Ligament Creep Behavior Can Be Predicted From Stress Relaxation by Incorporating Fiber Recruitment,” J. Rheol., 45(2), pp. 493–507. [CrossRef]
Screen, H. , 2008, “ Investigating Load Relaxation Mechanics in Tendon,” J. Mech. Behav. Biomed. Mater., 1(1), pp. 51–58. [CrossRef] [PubMed]
Sopakayang, R. , De Vita, R. , Kwansa, A. , and Freeman, J. , 2012, “ Elastic and Viscoelastic Properties of a Type I Collagen Fiber,” J. Theor. Biol., 293, pp. 197–205. [CrossRef] [PubMed]
Raischel, F. , Kun, F. , and Herrmann, H. , 2006, “ Failure Process of a Bundle of Plastic Fibers,” Phys. Rev. E, 73(6), p. 066101. [CrossRef]
Guo, Z. , and De Vita, R. , 2009, “ Probabilistic Constitutive Law for Damage in Ligaments,” Med. Eng. Phys., 31(9), pp. 1104–1109. [CrossRef] [PubMed]
Legerlotz, K. , Riley, G. , and Screen, H. , 2013, “ Gag Depletion Increases the Stress-Relaxation Response of Tendon Fascicles, but Does Not Influence Recovery,” Acta Biomater., 9(6), pp. 6860–6866. [CrossRef] [PubMed]

Figures

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Fig. 1

Fibrils and fiber bundles in bovine GC: (a) multiphoton microscopy (second harmonic generation) and (b) scanning electron microscopy from Ref. [9]

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Fig. 2

Top-view illustration of clampings (black) and samples (white) in uniaxial tension, strip-biaxial tension, and membrane inflation. The free lengths L0 and widths W0 in the reference state of uniaxial and strip-biaxial tests as well as the inner diameter di of membrane inflation are defined and the areas to extract the local deformation field are shown (gray). On the left, an example is shown of the markers applied to determine the strain field in the center of the test pieces.

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Fig. 3

The inflated membrane in the reference (dashed line) and deformed (solid line) state as well as radius of curvature R and apex displacement d are shown. Two cameras record top- and side-view images, where the high degree of illumination from the LED panel is visible in the side-view images.

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Fig. 4

Tension–stretch curves and kinematic responses of M-UA tests, interpreted with force thresholds of Fth = 0.1 N (dashed lines) and Fth = 0.01 N (solid lines)

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Fig. 5

Tension–strain curves of the M-I experiments represented for two pressure thresholds pth = 0.3 mbar (solid) and pth = 3 mbar (dashed)

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Fig. 6

Average tension–stretch curves and kinematic responses of the ten loadings in uniaxial cyclic tests

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Fig. 7

Normalized tension versus strain curves of the four different time-dependent tests. The strain normalization procedure proposed by Mauri et al. [22] was applied. R: relaxation, C: creep, UA: uniaxial, SB: strip-biaxial, I: inflation, 1: first holding phase, and 2: second holding phase.

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Fig. 8

Mean normalized tension relaxation (R) and creep (C) strains in the first (solid lines) and second (dashed lines) holding phases of the time-dependent tests in uniaxial (UA), strip-biaxial (SB), and equibiaxial (I) tension states. Error bars represent the standard deviation.

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Fig. 9

Mean curves and standard deviation of the normalized lateral contraction in uniaxial relaxation (R-UA) and creep (C-UA) experiments for the first (solid) and second (dashed) holding phases

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Fig. 10

Flowchart illustrating the model parameter identification procedure, similar to Ref. [35]. The optimization OPT0 is performed with mean data of uniaxial relaxation tests in order to identify the ten fixed model parameters. For the sample-specific constitutive model parameters, only μ¯0 was varied in OPT(i) for all time-dependent experiments.

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Fig. 11

Experimental data (mean ± SD) of the first holding phase (solid lines) of creep (C) and relaxation (R) tests in uniaxial (UA), strip-biaxial (SB), and equibiaxial (I) tension states as well as model prediction (mod) with parameters given in Table 5 (dashed lines)

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Fig. 12

Experimental data of the first loading ramp and holding phase of all relaxation and creep tests together with the corresponding model prediction based on the sample-specific parameter μ¯0. (Row 1: uniaxial relaxation, row 2: strip-biaxial relaxation, row 3: uniaxial creep, and row 4: equibiaxial creep).

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