Modeling biological growth and remodeling: Contrasting methods, contrasting needs

Abstract Biological growth and remodeling processes are necessarily time-dependent due to the finite periods needed for the material to be synthesized, deposited, degraded, and/or reorganized and, hence, so have been predominantly modeled for the past 20+ years. However, a full-spectrum examination of the timescales present in these processes reveals the need to explore a new class of models for which time-dependent effects are negligible. These mechanobiologically (quasi-) equilibrated formulations not only appear to apply well in many cases but also provide the modeler with those additional pieces of information, and intuition, always needed when modeling complex time-dependent responses. Material model determination, optimization involving long-term adaptations, and mechanobiological stability analyses could be leveraged by the simplicity and computational efficiency of time-independent models. Although this concept is general, we address it by means of two particular theories for which we also highlight crucial differences entailed by their diametrically different material memory and heterogeneity descriptions.

[1]  Stephen C Cowin,et al.  Tissue growth and remodeling. , 2004, Annual review of biomedical engineering.

[2]  C J Cyron,et al.  Vascular homeostasis and the concept of mechanobiological stability. , 2014, International journal of engineering science.

[3]  Vlado A. Lubarda,et al.  On the mechanics of solids with a growing mass , 2002 .

[4]  S. Cowin,et al.  Bone remodeling I: theory of adaptive elasticity , 1976 .

[5]  J. D. Humphrey,et al.  A homogenized constrained mixture (and mechanical analog) model for growth and remodeling of soft tissue , 2016, Biomechanics and modeling in mechanobiology.

[6]  Jay D Humphrey,et al.  Critical roles of time-scales in soft tissue growth and remodeling , 2018, APL bioengineering.

[7]  J. Humphrey,et al.  Computational Modeling Predicts Immuno-Mechanical Mechanisms of Maladaptive Aortic Remodeling in Hypertension. , 2019, International journal of engineering science.

[8]  K. Grosh,et al.  A continuum treatment of growth in biological tissue: the coupling of mass transport and mechanics , 2003, q-bio/0312001.

[9]  Jay D. Humphrey,et al.  Theory of small on large: Potential utility in computations of fluid–solid interactions in arteries , 2007 .

[10]  M. Rubin An Eulerian formulation of inelasticity: from metal plasticity to growth of biological tissues , 2019, Philosophical Transactions of the Royal Society A.

[11]  W. Cannon ORGANIZATION FOR PHYSIOLOGICAL HOMEOSTASIS , 1929 .

[12]  Meisam Soleimani Finite strain visco-elastic growth driven by nutrient diffusion: theory, FEM implementation and an application to the biofilm growth , 2019, Computational Mechanics.

[13]  A. Marsden,et al.  Optimization of Tissue Engineered Vascular Graft Design Using Computational Modeling. , 2019, Tissue engineering. Part C, Methods.

[14]  K. Rajagopal,et al.  Some remarks and clarifications concerning the restrictions placed on thermodynamic processes , 2019, International Journal of Engineering Science.

[15]  Jay D. Humphrey,et al.  A CONSTRAINED MIXTURE MODEL FOR GROWTH AND REMODELING OF SOFT TISSUES , 2002 .

[16]  A. McCulloch,et al.  Stress-dependent finite growth in soft elastic tissues. , 1994, Journal of biomechanics.

[17]  Antonio DeSimone,et al.  Growth and remodelling of living tissues: perspectives, challenges and opportunities , 2019, Journal of the Royal Society Interface.

[18]  J. Humphrey,et al.  Modeling mechano-driven and immuno-mediated aortic maladaptation in hypertension , 2018, Biomechanics and Modeling in Mechanobiology.

[19]  J. Humphrey,et al.  Mechanobiological Stability of Biological Soft Tissues. , 2019, Journal of the mechanics and physics of solids.

[20]  S. Shadden,et al.  Stability analysis of a continuum-based constrained mixture model for vascular growth and remodeling , 2016, Biomechanics and modeling in mechanobiology.

[21]  Serdar Göktepe,et al.  A generic approach towards finite growth with examples of athlete's heart, cardiac dilation, and cardiac wall thickening , 2010 .

[22]  Jeffrey W Holmes,et al.  Special Issue: Spotlight of the Future of Cardiovascular Engineering Frontiers and Challenges in Cardiovascular Biomechanics. , 2016, Journal of biomechanical engineering.

[23]  P. Papadopoulos,et al.  Material growth in thermoelastic continua: Theory, algorithmics, and simulation , 2010 .

[24]  M. Destrade,et al.  Modified multiplicative decomposition model for tissue growth: Beyond the initial stress-free state , 2018, Journal of the Mechanics and Physics of Solids.

[25]  K. Hayashi,et al.  Remodeling of the arterial wall: Response to restoration of normal blood flow after flow reduction. , 2018, Biorheology.

[26]  Davide Carlo Ambrosi,et al.  Stress-Modulated Growth , 2007 .

[27]  J. Humphrey,et al.  Biomechanics and Mechanobiology of Extracellular Matrix Remodeling , 2019, Multi-scale Extracellular Matrix Mechanics and Mechanobiology.

[28]  C J Cyron,et al.  Growth and remodeling of load-bearing biological soft tissues , 2016, Meccanica.

[29]  J D Humphrey,et al.  Stress, strain, and mechanotransduction in cells. , 2001, Journal of biomechanical engineering.

[30]  W. Lin,et al.  Non-axisymmetric dilatation of a thick-walled aortic aneurysmal tissue , 2019, International Journal of Non-Linear Mechanics.

[31]  L. Taber A model for aortic growth based on fluid shear and fiber stresses. , 1998, Journal of biomechanical engineering.

[32]  J. Humphrey,et al.  Biomechanical diversity despite mechanobiological stability in tissue engineered vascular grafts two years post-implantation. , 2015, Tissue engineering. Part A.

[33]  Gerard A Ateshian,et al.  On the theory of reactive mixtures for modeling biological growth , 2007, Biomechanics and modeling in mechanobiology.

[34]  J. Humphrey,et al.  A mechanobiologically equilibrated constrained mixture model for growth and remodeling of soft tissues , 2018, Zeitschrift fur angewandte Mathematik und Mechanik.

[35]  Jay D Humphrey,et al.  Mechanisms of arterial remodeling in hypertension: coupled roles of wall shear and intramural stress. , 2008, Hypertension.

[36]  Are Homeostatic States Stable? Dynamical Stability in Morphoelasticity , 2018, Bulletin of mathematical biology.

[37]  A. Goriely The Mathematics and Mechanics of Biological Growth , 2017 .

[38]  Ellen Kuhl,et al.  Growing matter: a review of growth in living systems. , 2014, Journal of the mechanical behavior of biomedical materials.

[39]  J. Humphrey,et al.  Excessive Adventitial Remodeling Leads to Early Aortic Maladaptation in Angiotensin-Induced Hypertension , 2016, Hypertension.

[40]  Ruslan Medzhitov,et al.  Homeostasis, Inflammation, and Disease Susceptibility , 2015, Cell.

[41]  C J Cyron,et al.  Homogenized constrained mixture models for anisotropic volumetric growth and remodeling , 2016, Biomechanics and Modeling in Mechanobiology.

[42]  A Rachev,et al.  Theoretical study of the effect of stress-dependent remodeling on arterial geometry under hypertensive conditions. , 1997, Journal of biomechanics.

[43]  Paul Steinmann,et al.  Mass– and volume–specific views on thermodynamics for open systems , 2003, Proceedings of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[44]  A. Grillo,et al.  Growth and remodelling from the perspective of Noether’s theorem , 2019, Mechanics Research Communications.

[45]  S. Farzaneh,et al.  Patient-specific predictions of aneurysm growth and remodeling in the ascending thoracic aorta using the homogenized constrained mixture model , 2019, Biomechanics and Modeling in Mechanobiology.

[46]  Marcelo Epstein,et al.  Thermomechanics of volumetric growth in uniform bodies , 2000 .

[47]  A. Grillo,et al.  A study of growth and remodeling in isotropic tissues, based on the Anand‐Aslan‐Chester theory of strain‐gradient plasticity , 2019, GAMM-Mitteilungen.

[48]  J. Humphrey,et al.  Differential cell-matrix mechanoadaptations and inflammation drive regional propensities to aortic fibrosis, aneurysm or dissection in hypertension , 2017, Journal of The Royal Society Interface.

[49]  G. Holzapfel,et al.  A finite element implementation of a growth and remodeling model for soft biological tissues: Verification and application to abdominal aortic aneurysms , 2019, Computer Methods in Applied Mechanics and Engineering.

[50]  A goal function approach to remodeling of arteries uncovers mechanisms for growth instability , 2014, Biomechanics and modeling in mechanobiology.