One contribution of 19 to a theme issue ‘ Integrated multiscale biomaterials experiment and modelling : towards function and pathology

Advances in multiscale models and computational power have enabled a broad toolset to predict how molecules, cells, tissues and organs behave and develop. A key theme in biological systems is the emergence of macroscale behaviour from collective behaviours across a range of length and timescales, and a key element of these models is therefore hierarchical simulation. However, this predictive capacity has far outstripped our ability to validate predictions experimentally, particularly when multiple hierarchical levels are involved. The state of the art represents careful integration of multiscale experiment and modelling, and yields not only validation, but also insights into deformation and relaxation mechanisms across scales. We present here a sampling of key results that highlight both challenges and opportunities for integrated multiscale experiment and modelling in biological systems.

[1]  J. Petruska,et al.  A SUBUNIT MODEL FOR THE TROPOCOLLAGEN MACROMOLECULE. , 1964, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Y Lanir,et al.  A structural theory for the homogeneous biaxial stress-strain relationships in flat collagenous tissues. , 1979, Journal of biomechanics.

[3]  M. Nimni,et al.  Mechanism of crosslinking of proteins by glutaraldehyde II. Reaction with monomeric and polymeric collagen. , 1982, Connective tissue research.

[4]  M. Nimni,et al.  Mechanism of crosslinking of proteins by glutaraldehyde I: reaction with model compounds. , 1982, Connective tissue research.

[5]  Y. Lanir.  Constitutive equations for fibrous connective tissues. , 1983, Journal of biomechanics.

[6]  P. Benya,et al.  The presence of intermolecular disulfide cross-links in type III collagen. , 1983, The Journal of biological chemistry.

[7]  M E Nimni,et al.  Toxic reactions evoked by glutaraldehyde-fixed pericardium and cardiac valve tissue bioprosthesis. , 1984, Journal of biomedical materials research.

[8]  N. Perelman,et al.  Mechanism of crosslinking of proteins by glutaraldehyde III. Reaction with collagen in tissues. , 1985, Connective tissue research.

[9]  B. Strates,et al.  Chemically modified collagen: a natural biomaterial for tissue replacement. , 1987, Journal of biomedical materials research.

[10]  Marcel E. Nimni,et al.  Biochemistry and biomechanics , 1988 .

[11]  D A Parry,et al.  The molecular and fibrillar structure of collagen and its relationship to the mechanical properties of connective tissue. , 1988, Biophysical chemistry.

[12]  D R Boughner,et al.  The bovine pericardial xenograft: I. Effect of fixation in aldehydes without constraint on the tensile viscoelastic properties of bovine pericardium. , 1989, Journal of biomedical materials research.

[13]  J M Lee,et al.  The bovine pericardial xenograft: III. Effect of uniaxial and sequential biaxial stress during fixation on the tensile viscoelastic properties of bovine pericardium. , 1989, Journal of biomedical materials research.

[14]  J M Lee,et al.  The bovine pericardial xenograft: II. Effect of tethering or pressurization during fixation on the tensile viscoelastic properties of bovine pericardium. , 1989, Journal of biomedical materials research.

[15]  N. Perelman,et al.  Mechanism of crosslinking of proteins by glutaraldehyde. IV: In vitro and in vivo stability of a crosslinked collagen matrix. , 1990, Connective tissue research.

[16]  D T Cheung,et al.  Correlation of structure and viscoelastic properties in the pericardia of four mammalian species. , 1992, The American journal of physiology.

[17]  D. Courtman,et al.  High Strain Rate Testing and Structural Analysis of Pericardial Bioprosthetic Materials , 1994 .

[18]  Y. Lanir,et al.  Plausibility of Structural Constitutive Equations for Isotropic Soft Tissues in Finite Static Deformations , 1994 .

[19]  N. Sasaki,et al.  Stress-strain curve and Young's modulus of a collagen molecule as determined by the X-ray diffraction technique. , 1996, Journal of biomechanics.

[20]  D. Stamenović,et al.  Dynamic behavior of lung parenchyma in shear. , 1996, Journal of applied physiology.

[21]  M. Kojic,et al.  A numerical algorithm for stress integration of a fiber-fiber kinetics model with Coulomb friction for connective tissue , 1998 .

[22]  N. Ratliff,et al.  Mechanics of explanted bioprosthetic heart valves. , 1999, Biomedical sciences instrumentation.

[23]  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.

[24]  K. Mann,et al.  Noncollagenous bone matrix proteins, calcification, and thrombosis in carotid artery atherosclerosis. , 1999, Arteriosclerosis, thrombosis, and vascular biology.

[25]  S. Wells,et al.  Thermomechanical Characterization of Collagen Crosslinking in Developing Cardiovascular Tissues , 1999, Advances in Bioengineering.

[26]  Michael S. Sacks,et al.  A structural constitutive model for chemically treated planar tissues under biaxial loading , 2000 .

[27]  I Vesely,et al.  Tissue damage and calcification may be independent mechanisms of bioprosthetic heart valve failure. , 2001, The Journal of heart valve disease.

[28]  I Vesely,et al.  The effect of elastin damage on the mechanics of the aortic valve. , 2001, Journal of biomechanics.

[29]  M. Sacks,et al.  Effects of fixation pressure on the biaxial mechanical behavior of porcine bioprosthetic heart valves with long-term cyclic loading. , 2002, Biomaterials.

[30]  I. Alferiev,et al.  Prevention of polyurethane valve cusp calcification with covalently attached bisphosphonate diethylamino moieties. , 2003, Journal of biomedical materials research. Part A.

[31]  T. Aigner,et al.  Collagens--structure, function, and biosynthesis. , 2003, Advanced drug delivery reviews.

[32]  Michael S Sacks,et al.  Incorporation of experimentally-derived fiber orientation into a structural constitutive model for planar collagenous tissues. , 2003, Journal of biomechanical engineering.

[33]  M. Sacks,et al.  Biaxial mechanical response of bioprosthetic heart valve biomaterials to high in-plane shear. , 2003, Journal of biomechanical engineering.

[34]  Wei Sun,et al.  Multiaxial mechanical behavior of biological materials. , 2003, Annual review of biomedical engineering.

[35]  Eric A Nauman,et al.  Mechanical characterization of collagen fibers and scaffolds for tissue engineering. , 2003, Biomaterials.

[36]  Michael S. Sacks,et al.  Orthotropic Mechanical Properties of Chemically Treated Bovine Pericardium , 1998, Annals of Biomedical Engineering.

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

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

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

[40]  Frederick J Schoen,et al.  Calcification of tissue heart valve substitutes: progress toward understanding and prevention. , 2005, The Annals of thoracic surgery.

[41]  Arnab Majumdar,et al.  Mechanical interactions between collagen and proteoglycans: implications for the stability of lung tissue. , 2005, Journal of applied physiology.

[42]  Lin Yang,et al.  Molecular orientation of collagen in intact planar connective tissues under biaxial stretch. , 2005, Acta biomaterialia.

[43]  Michael S Sacks,et al.  The effects of collagen fiber orientation on the flexural properties of pericardial heterograft biomaterials. , 2005, Biomaterials.

[44]  Wei Sun,et al.  Finite element implementation of a generalized Fung-elastic constitutive model for planar soft tissues , 2005, Biomechanics and modeling in mechanobiology.

[45]  Michael S Sacks,et al.  Cyclic loading response of bioprosthetic heart valves: effects of fixation stress state on the collagen fiber architecture. , 2005, Biomaterials.

[46]  Frederick J Schoen,et al.  Cardiac valves and valvular pathology: update on function, disease, repair, and replacement. , 2005, Cardiovascular pathology : the official journal of the Society for Cardiovascular Pathology.

[47]  Jun Liao,et al.  Relationship Between Collagen Fibrils, Glycosaminoglycans, and Stress Relaxation in Mitral Valve Chordae Tendineae , 2004, Annals of Biomedical Engineering.

[48]  H. Kahn,et al.  Nano measurements with micro-devices: mechanical properties of hydrated collagen fibrils , 2006, Journal of The Royal Society Interface.

[49]  Markus J. Buehler,et al.  Atomistic and continuum modeling of mechanical properties of collagen: Elasticity, fracture, and self-assembly , 2006 .

[50]  Ray W. Ogden,et al.  The influence of the invariant I8I8 on the stress deformation and ellipticity characteristics of doubly fiber-reinforced non-linearly elastic solids , 2006 .

[51]  Paul Schmidt,et al.  Bioprosthetic heart valve heterograft biomaterials: structure, mechanical behavior and computational simulation , 2006, Expert review of medical devices.

[52]  A. Yoganathan,et al.  Planar Biaxial Creep and Stress Relaxation of the Mitral Valve Anterior Leaflet , 2006, Annals of Biomedical Engineering.

[53]  Lin Yang,et al.  The relation between collagen fibril kinematics and mechanical properties in the mitral valve anterior leaflet. , 2007, Journal of biomechanical engineering.

[54]  M. Sacks,et al.  Time-dependent biaxial mechanical behavior of the aortic heart valve leaflet. , 2007, Journal of biomechanics.

[55]  Vinod Subramaniam,et al.  Micromechanical bending of single collagen fibrils using atomic force microscopy. , 2007, Journal of biomedical materials research. Part A.

[56]  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.

[57]  M. R. Dodge,et al.  Stress-strain experiments on individual collagen fibrils. , 2008, Biophysical journal.

[58]  Markus J. Buehler,et al.  Atomistic Modeling of Materials Failure , 2008 .

[59]  J. Feijen,et al.  Mechanical properties of single electrospun collagen type I fibers. , 2008, Biomaterials.

[60]  K. Garikipati,et al.  Elastica-based strain energy functions for soft biological tissue , 2007, q-bio/0701006.

[61]  David E. Schmidt,et al.  On the biomechanics of heart valve function. , 2009, Journal of biomechanics.

[62]  Markus J Buehler,et al.  Deformation and failure of protein materials in physiologically extreme conditions and disease. , 2009, Nature materials.

[63]  Iwona M Jasiuk,et al.  Multiscale modeling of elastic properties of cortical bone , 2010 .

[64]  Elliot L Elson,et al.  Phase separation in biological membranes: integration of theory and experiment. , 2010, Annual review of biophysics.

[65]  R. Ritchie,et al.  On the Mechanistic Origins of Toughness in Bone , 2010 .

[66]  M. Buehler,et al.  Multiscale aspects of mechanical properties of biological materials. , 2011, Journal of the mechanical behavior of biomedical materials.

[67]  David I. Spivak,et al.  Reoccurring Patterns in Hierarchical Protein Materials and Music: The Power of Analogies , 2011, 1111.5297.

[68]  David I. Spivak,et al.  Materials by Design: Merging Proteins and Music. , 2012, Nano today.

[69]  Michael S Sacks,et al.  On the biomechanical role of glycosaminoglycans in the aortic heart valve leaflet. , 2013, Acta biomaterialia.

[70]  M. Sacks,et al.  Simulation of planar soft tissues using a structural constitutive model: Finite element implementation and validation. , 2014, Journal of biomechanics.

[71]  G. Genin,et al.  Modelling the mechanics of partially mineralized collagen fibrils, fibres and tissue , 2014, Journal of The Royal Society Interface.

[72]  Corey P. Neu,et al.  Handbook of Imaging in Biological Mechanics , 2014 .

[73]  Michael S Sacks,et al.  Insights into regional adaptations in the growing pulmonary artery using a meso-scale structural model: effects of ascending aorta impingement. , 2014, Journal of biomechanical engineering.

[74]  Michael S Sacks,et al.  On the presence of affine fibril and fiber kinematics in the mitral valve anterior leaflet. , 2015, Biophysical journal.

[75]  G. Genin,et al.  Stochastic interdigitation as a toughening mechanism at the interface between tendon and bone. , 2015, Biophysical journal.

[76]  Chung-Hao Lee,et al.  A generalized method for the analysis of planar biaxial mechanical data using tethered testing configurations. , 2015, Journal of biomechanical engineering.

[77]  Ying Li,et al.  Cell and nanoparticle transport in tumour microvasculature: the role of size, shape and surface functionality of nanoparticles , 2016, Interface Focus.

[78]  L. Hogstrom,et al.  Advancing multiscale structural mapping of the brain through fluorescence imaging and analysis across length scales , 2016, Interface Focus.

[79]  T. Nguyen,et al.  Collagen network strengthening following cyclic tensile loading , 2016, Interface Focus.

[80]  N. Pugno,et al.  Slip knots and unfastening topologies enhance toughness without reducing strength of silk fibroin fibres , 2016, Interface Focus.

[81]  Vivek B. Shenoy,et al.  A chemo-mechanical free-energy-based approach to model durotaxis and extracellular stiffness-dependent contraction and polarization of cells , 2016, Interface Focus.

[82]  L. Soslowsky,et al.  Collagen V-heterozygous and -null supraspinatus tendons exhibit altered dynamic mechanical behaviour at multiple hierarchical scales , 2016, Interface Focus.

[83]  George Em Karniadakis,et al.  Patient-specific blood rheology in sickle-cell anaemia , 2016, Interface Focus.

[84]  Songbai Ji,et al.  Real-time, whole-brain, temporally resolved pressure responses in translational head impact , 2016, Interface Focus.

[85]  A. Weiss,et al.  Force fields for simulating the interaction of surfaces with biological molecules , 2016, Interface Focus.

[86]  Fei Fang,et al.  Modelling approaches for evaluating multiscale tendon mechanics , 2016, Interface Focus.

[87]  K. Dorfman,et al.  Cell–matrix interaction during strain-dependent remodelling of simulated collagen networks , 2016, Interface Focus.

[88]  Lester J. Smith,et al.  Tunability of collagen matrix mechanical properties via multiple modes of mineralization , 2016, Interface Focus.

[89]  R. Ballarini,et al.  Tension tests on mammalian collagen fibrils , 2016, Interface Focus.

[90]  Fereshteh A Sabet,et al.  Modelling of bone fracture and strength at different length scales: a review , 2016, Interface Focus.

[91]  Krista M. Durney,et al.  Continuum theory of fibrous tissue damage mechanics using bond kinetics: application to cartilage tissue engineering , 2016, Interface Focus.

[92]  M. Sacks,et al.  A novel fibre-ensemble level constitutive model for exogenous cross-linked collagenous tissues , 2016, Interface Focus.

[93]  X. Edward Guo,et al.  Experimental studies of bone mechanoadaptation: bridging in vitro and in vivo studies with multiscale systems , 2016, Interface Focus.

[94]  Elliot L Elson,et al.  Tissue constructs: platforms for basic research and drug discovery , 2016, Interface Focus.