A residual stiffness-based model for the fatigue damage of biological soft tissues

Abstract Biologically-derived and chemically-treated collagenous tissues such as glutaraldehyde-treated bovine pericardium (GLBP) are widely used in many medical applications. The long-term cyclic loading-induced tissue fatigue damage has been identified as one of the primary factors limiting the durability of such medical devices and an in-depth understanding of the fatigue behaviors of biological tissues is critical to increase device durability. However, a limited number of fatigue damage experiments were performed on biological tissues due to complexity and time-consuming nature of such fatigue experiments. Consequently, accurate constitutive models for fatigue damage are also lacking. In this study, we performed a rigorous fatigue experiment on GLBP tissues. The stress, strain and permanent set at a maximum of 8 different fatigue cycles, up to 15 million cycles, were obtained, which demonstrated a nonlinear stress softening and a nonlinear permanent set accumulation. Based on the experimental data, we developed a novel residual stiffness-based fatigue model. The fatigue model considers the fatigue-induced reduction of initial stiffness and stiffening effect, in contrast to our previous damage-based model that only considered the fatigue-induced reduction of the initial stiffness. Moreover, a new constitutive relation was proposed to describe how the fatigue life (the cycle number at failure) depends on the equivalent strain, analogous to the stress versus fatigue life (S-N) curve for traditional engineering material. The new fatigue model can characterize the stress softening and nonlinear permanent set effects when referring to the pre-fatigued configuration. It can also describe the nonlinear stress stiffening effect when referring to the post-fatigued configuration. The model predictions are in good agreement with the experiment. The experimental results and the novel model could be applied to fatigue analyses of medical devices to improve the durability.

[1]  Ray W. Ogden,et al.  A constitutive model for the Mullins effect with permanent set in particle-reinforced rubber , 2004 .

[2]  M. Rubin,et al.  A nonlinear Cosserat interphase model for residual stresses in an inclusion and the interphase that bonds it to an infinite matrix , 2015 .

[3]  Zhigang Suo,et al.  Fatigue of double-network hydrogels , 2017 .

[4]  M. Sacks,et al.  Response of heterograft heart valve biomaterials to moderate cyclic loading. , 2004, Journal of biomedical materials research. Part A.

[5]  Gerhard A. Holzapfel,et al.  Nonlinear Solid Mechanics: A Continuum Approach for Engineering Science , 2000 .

[6]  N. Broom,et al.  Fatigue-induced damage in glutaraldehyde-preserved heart valve tissue. , 1978, The Journal of thoracic and cardiovascular surgery.

[7]  Zhigang Suo,et al.  Fatigue Fracture of Self-Recovery Hydrogels. , 2018, ACS macro letters.

[8]  M. Sacks,et al.  Collagen fiber disruption occurs independent of calcification in clinically explanted bioprosthetic heart valves. , 2002, Journal of biomedical materials research.

[9]  Wei Sun,et al.  A new inverse method for estimation of in vivo mechanical properties of the aortic wall. , 2017, Journal of the mechanical behavior of biomedical materials.

[10]  Zhigang Suo,et al.  Fatigue fracture of tough hydrogels , 2017 .

[11]  R. Ogden,et al.  A pseudo–elastic model for the Mullins effect in filled rubber , 1999, Proceedings of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[12]  M Doblaré,et al.  A constitutive formulation of vascular tissue mechanics including viscoelasticity and softening behaviour. , 2010, Journal of biomechanics.

[13]  Mikhail Itskov,et al.  Modeling of anisotropic softening phenomena: Application to soft biological tissues , 2009 .

[14]  Peter Regitnig,et al.  Layer-specific damage experiments and modeling of human thoracic and abdominal aortas with non-atherosclerotic intimal thickening. , 2012, Journal of the mechanical behavior of biomedical materials.

[15]  Wei Sun,et al.  Modeling of long-term fatigue damage of soft tissue with stress softening and permanent set effects , 2013, Biomechanics and modeling in mechanobiology.

[16]  N. Broom,et al.  An 'in vitro' study of mechanical fatigue in glutaraldehyde-treated porcine aortic valve tissue. , 1980, Biomaterials.

[17]  Z. Suo,et al.  Fracture Toughness and Fatigue Threshold of Tough Hydrogels. , 2018, ACS macro letters.

[18]  Jianxiang Wang,et al.  A criterion for failure mode prediction of angle-ply composite laminates under in-plane tension , 2015 .

[19]  J Bonnoit,et al.  A Visco-hyperelastic Model With Damage for the Knee Ligaments Under Dynamic Constraints , 2002, Computer methods in biomechanics and biomedical engineering.

[20]  Sanjay Govindjee,et al.  A micro-mechanically based continuum damage model for carbon black-filled rubbers incorporating Mullins' effect , 1991 .

[21]  G. Holzapfel,et al.  Stress softening and permanent deformation in human aortas: Continuum and computational modeling with application to arterial clamping. , 2016, Journal of the mechanical behavior of biomedical materials.

[22]  S. Pinho,et al.  Failure mechanisms of biological crossed-lamellar microstructures applied to synthetic high-performance fibre-reinforced composites , 2019, Journal of the Mechanics and Physics of Solids.

[23]  K Y Volokh,et al.  Prediction of arterial failure based on a microstructural bi-layer fiber-matrix model with softening. , 2008, Journal of biomechanics.

[24]  T. Nguyen,et al.  Micromechanical models for the stiffness and strength of UHMWPE macrofibrils , 2018, Journal of the Mechanics and Physics of Solids.

[25]  Wei Sun,et al.  Fatigue damage of collagenous tissues: experiment, modeling and simulation studies. , 2015, Journal of long-term effects of medical implants.

[26]  D. Kelly,et al.  Inelasticity of Human Carotid Atherosclerotic Plaque , 2011, Annals of Biomedical Engineering.

[27]  M. Sacks,et al.  Simulated bioprosthetic heart valve deformation under quasi-static loading. , 2005, Journal of biomechanical engineering.

[28]  G. Holzapfel,et al.  Multiscale modeling of fiber recruitment and damage with a discrete fiber dispersion method , 2019, Journal of the Mechanics and Physics of Solids.

[29]  E. Peña Prediction of the softening and damage effects with permanent set in fibrous biological materials , 2011 .

[30]  Wei Sun,et al.  Identification of in vivo nonlinear anisotropic mechanical properties of ascending thoracic aortic aneurysm from patient-specific CT scans , 2019, Scientific Reports.

[31]  M. Sacks,et al.  The biomechanical effects of fatigue on the porcine bioprosthetic heart valve. , 2001, Journal of long-term effects of medical implants.

[32]  G. Holzapfel,et al.  Brain tissue deforms similarly to filled elastomers and follows consolidation theory , 2006 .

[33]  Daniel Balzani,et al.  Constitutive framework for the modeling of damage in collagenous soft tissues with application to arterial walls , 2012 .

[34]  Daniel K. Hildebrand,et al.  Effects of collagen fiber orientation on the response of biologically derived soft tissue biomaterials to cyclic loading. , 2007, Journal of biomedical materials research. Part A.

[35]  G. Holzapfel,et al.  Modeling of damage in soft biological tissues , 2017 .

[36]  S. Yazdani,et al.  A constitutive model of the artery with damage , 1997 .

[37]  Bhushan Lal Karihaloo,et al.  An improved Puck’s failure theory for fibre-reinforced composite laminates including the in situ strength effect , 2014 .

[38]  N. Broom,et al.  The stress/strain and fatigue behaviour of glutaraldehyde preserved heart-valve tissue. , 1977, Journal of biomechanics.

[39]  Larry Lessard,et al.  Progressive Fatigue Damage Modeling of Composite Materials, Part I: Modeling , 2000 .

[40]  Manuel Doblaré,et al.  A stochastic-structurally based three dimensional finite-strain damage model for fibrous soft tissue , 2006 .

[41]  Zhigang Suo,et al.  Fatigue of hydrogels , 2019, European Journal of Mechanics - A/Solids.

[42]  Manuel Doblaré,et al.  On finite‐strain damage of viscoelastic‐fibred materials. Application to soft biological tissues , 2008 .

[43]  Manuel Doblaré,et al.  An uncoupled directional damage model for fibred biological soft tissues. Formulation and computational aspects , 2007 .

[44]  D. B. Smith,et al.  Effects of accelerated testing on porcine bioprosthetic heart valve fiber architecture. , 1998, Biomaterials.

[45]  R. Rolfes,et al.  A review of computational modelling approaches to compressive failure in laminates , 2019, Composites Science and Technology.

[46]  Michael S Sacks,et al.  Modeling the response of exogenously crosslinked tissue to cyclic loading: The effects of permanent set. , 2017, Journal of the mechanical behavior of biomedical materials.

[47]  Konstantin Y. Volokh,et al.  Hyperelasticity with softening for modeling materials failure , 2007 .

[48]  Z. Suo,et al.  Fatigue-Resistant elastomers , 2020 .

[49]  R. Ogden,et al.  A New Constitutive Framework for Arterial Wall Mechanics and a Comparative Study of Material Models , 2000 .

[50]  Bhushan Lal Karihaloo,et al.  A new fatigue failure theory for multidirectional fiber-reinforced composite laminates with arbitrary stacking sequence , 2016 .

[51]  K Y Volokh,et al.  Modeling failure of soft anisotropic materials with application to arteries. , 2011, Journal of the mechanical behavior of biomedical materials.

[52]  D. Kelly,et al.  An anisotropic inelastic constitutive model to describe stress softening and permanent deformation in arterial tissue. , 2012, Journal of the mechanical behavior of biomedical materials.

[53]  P. J. Drury,et al.  The in vivo durability of bioprosthetic heart valves--modes of failure observed in explanted valves. , 1987, Engineering in medicine.

[54]  R. Ogden,et al.  Hyperelastic modelling of arterial layers with distributed collagen fibre orientations , 2006, Journal of The Royal Society Interface.

[55]  F J Schoen,et al.  Founder's Award, 25th Annual Meeting of the Society for Biomaterials, perspectives. Providence, RI, April 28-May 2, 1999. Tissue heart valves: current challenges and future research perspectives. , 1999, Journal of biomedical materials research.

[56]  H. Schürmann,et al.  FAILURE ANALYSIS OF FRP LAMINATES BY MEANS OF PHYSICALLY BASED PHENOMENOLOGICAL MODELS 1 This articl , 1998 .

[57]  Wei Sun,et al.  Comparison of transcatheter aortic valve and surgical bioprosthetic valve durability: A fatigue simulation study. , 2015, Journal of biomechanics.