A bone remodelling model including the directional activity of BMUs

Bone is able to adapt itself to the mechanical and biological environment by changing its porosity and/or orientation of its internal microstructure in a process known as bone remodelling. As a consequence, a change of bone mechanical properties is produced leading to an optimum structure, able to bear the external loads with the minimum weight. This adaptation is carried out by a temporal association of cells known as BMUs (basic multicellular units) that resorb old bone and sometimes produce new organic extracellular matrix (osteoid) that is later mineralized. This involves changes in porosity, damage level (density of microcracks accumulated by cyclic loads) and mineral content. All of these features were taken into account in a previous model, but the whole process and therefore the resulting bone constitutive behaviour was considered isotropic. The model proposed herein, recognizing that bone is actually anisotropic, tries to explain how BMUs modify the anisotropy by changing their progressing direction. We check the potential of the model to predict the alignment of the bone microstructure with the external loads in different situations. Then, the model is also applied to obtain the anisotropy and mechanical properties of the human proximal femur under physiological loads with initial conditions corresponding to a heterogeneous, but otherwise isotropic bone.

[1]  Franz G. Rammerstorfer,et al.  Computational simulation of internal bone remodeling , 1997 .

[2]  J. M. Garcı́a,et al.  Anisotropic bone remodelling model based on a continuum damage-repair theory. , 2002, Journal of biomechanics.

[3]  F. Sidoroff,et al.  Damage Induced Elastic Anisotropy , 1982 .

[4]  R. Mann,et al.  Characterization of microstructural anisotropy in orthotropic materials using a second rank tensor , 1984 .

[5]  R. Zadro,et al.  Mechanical Loading Stimulates Differentiation of Periodontal Osteoblasts in a Mouse Osteoinduction Model: Effect on Type I Collagen and Alkaline Phosphatase Genes , 2000, Calcified Tissue International.

[6]  A. Burstein,et al.  The Mechanical Properties of Cortical Bone , 1974 .

[7]  Rik Huiskes,et al.  Effects of mechanical forces on maintenance and adaptation of form in trabecular bone , 2000, Nature.

[8]  R. Martin Porosity and specific surface of bone. , 1984, Critical reviews in biomedical engineering.

[9]  Taiji Adachi,et al.  Functional adaptation of cancellous bone in human proximal femur predicted by trabecular surface remodeling simulation toward uniform stress state. , 2002, Journal of biomechanics.

[10]  W. E. Roberts,et al.  Sensitivity of bone cell populations to weightlessness and simulated weightlessness , 1984 .

[11]  D. Carter,et al.  Cyclic mechanical property degradation during fatigue loading of cortical bone. , 1996, Journal of biomechanics.

[12]  J. Wolff The Law of Bone Remodelling , 1986, Springer Berlin Heidelberg.

[13]  D P Fyhrie,et al.  Trabecular bone density and loading history: regulation of connective tissue biology by mechanical energy. , 1987, Journal of biomechanics.

[14]  Z. Jaworski,et al.  The rate of osteoclastic bone erosion in Haversian remodeling sites of adult dog's rib , 2005, Calcified Tissue Research.

[15]  J. C. Simo,et al.  Adaptive bone remodeling incorporating simultaneous density and anisotropy considerations. , 1997, Journal of biomechanics.

[16]  J. M. García-Aznar,et al.  A bone remodelling model coupling microdamage growth and repair by 3D BMU-activity , 2005, Biomechanics and modeling in mechanobiology.

[17]  G S Beaupré,et al.  An approach for time‐dependent bone modeling and remodeling—theoretical development , 1990, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[18]  S C Cowin,et al.  Mechanosensation and fluid transport in living bone. , 2002, Journal of musculoskeletal & neuronal interactions.

[19]  A. Ascenzi,et al.  An investigation on the mechanical anisotropy of the alternatelystructured osteons , 1976, Calcified Tissue Research.

[20]  Martin Rb Porosity and specific surface of bone. , 1984 .

[21]  A. Parfitt Osteonal and hemi‐osteonal remodeling: The spatial and temporal framework for signal traffic in adult human bone , 1994, Journal of cellular biochemistry.

[22]  Dennis R. Carter,et al.  Mechanical loading histories and cortical bone remodeling , 2006, Calcified Tissue International.

[23]  S. Goldstein,et al.  Elastic modulus and hardness of cortical and trabecular bone lamellae measured by nanoindentation in the human femur. , 1999, Journal of biomechanics.

[24]  A. Ascenzi,et al.  The tensile properties of single osteons , 1967, The Anatomical record.

[25]  Salah Naili,et al.  Sur le remodelage des tissus osseux anisotropes , 2006 .

[26]  M. Rashid,et al.  A mechanistic model for internal bone remodeling exhibits different dynamic responses in disuse and overload. , 2001, Journal of biomechanics.

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

[28]  S. Cowin,et al.  Wolff's law of trabecular architecture at remodeling equilibrium. , 1986, Journal of biomechanical engineering.

[29]  G. Niebur,et al.  Comparison of the elastic and yield properties of human femoral trabecular and cortical bone tissue. , 2004, Journal of biomechanics.

[30]  W C Van Buskirk,et al.  A continuous wave technique for the measurement of the elastic properties of cortical bone. , 1984, Journal of biomechanics.

[31]  D P Fyhrie,et al.  The adaptation of bone apparent density to applied load. , 1995, Journal of biomechanics.

[32]  G. Beaupré,et al.  The influence of bone volume fraction and ash fraction on bone strength and modulus. , 2001, Bone.

[33]  C. H. Turner,et al.  Toward a Mathematical Description of Bone Biology: The Principle of Cellular Accommodation , 1999, Calcified Tissue International.

[34]  D. Carter,et al.  Relationships between loading history and femoral cancellous bone architecture. , 1989, Journal of biomechanics.

[35]  David Taylor,et al.  Predicting stress fractures using a probabilistic model of damage, repair and adaptation , 2004, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[36]  Frost Hm,et al.  The mechanostat: a proposed pathogenic mechanism of osteoporoses and the bone mass effects of mechanical and nonmechanical agents. , 1987 .

[37]  W. J. Whitehouse,et al.  Scanning electron microscope studies of trabecular bone in the proximal end of the human femur. , 1974, Journal of anatomy.

[38]  A. Parfitt,et al.  Theoretical perspective: A new model for the regulation of bone resorption, with particular reference to the effects of bisphosphonates , 1996 .

[39]  R. Recker,et al.  Bone histomorphometry : techniques and interpretation , 1983 .

[40]  M. Warner,et al.  Determination of orthotropic bone elastic constants using FEA and modal analysis. , 2002, Journal of biomechanics.

[41]  M Bagge,et al.  A model of bone adaptation as an optimization process. , 2000, Journal of biomechanics.

[42]  R T Whalen,et al.  Influence of physical activity on the regulation of bone density. , 1988, Journal of biomechanics.

[43]  S J Hollister,et al.  A global relationship between trabecular bone morphology and homogenized elastic properties. , 1998, Journal of biomechanical engineering.

[44]  J. Klein-Nulend,et al.  MECHANOTRANSDUCTION IN BONE : ROLE OF THE LACUNOCANALICULAR NETWORK , 1999 .

[45]  Sabine Bensamoun,et al.  Spatial distribution of acoustic and elastic properties of human femoral cortical bone. , 2004, Journal of biomechanics.

[46]  John D. Currey,et al.  The Mechanical Adaptations of Bones , 1984 .

[47]  R. Martin,et al.  Toward a unifying theory of bone remodeling. , 2000, Bone.

[48]  G. Rodan Introduction to bone biology. , 1992, Bone.

[49]  J. Katz,et al.  Ultrasonic wave propagation in human cortical bone--II. Measurements of elastic properties and microhardness. , 1976, Journal of biomechanics.

[50]  H. Frost,et al.  The mechanostat: a proposed pathogenic mechanism of osteoporoses and the bone mass effects of mechanical and nonmechanical agents. , 1987, Bone and mineral.

[51]  G. Beaupré,et al.  An approach for time‐dependent bone modeling and remodeling—application: A preliminary remodeling simulation , 1990, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[52]  H. Rodrigues,et al.  OPTIMIZATION MODELS IN THE SIMULATION OF THE BONE ADAPTATION PROCESS , 2004 .

[53]  C. Christiansen,et al.  Serum vitamin D metabolites in younger and elderly postmenopausal women , 2006, Calcified Tissue International.

[54]  M Doblaré,et al.  Application of an anisotropic bone-remodelling model based on a damage-repair theory to the analysis of the proximal femur before and after total hip replacement. , 2001, Journal of biomechanics.

[55]  W. J. Whitehouse The quantitative morphology of anisotropic trabecular bone , 1974, Journal of microscopy.

[56]  H. Grootenboer,et al.  Adaptive bone-remodeling theory applied to prosthetic-design analysis. , 1987, Journal of biomechanics.

[57]  X Edward Guo,et al.  The dependence of transversely isotropic elasticity of human femoral cortical bone on porosity. , 2004, Journal of biomechanics.

[58]  Philippe K. Zysset,et al.  An alternative model for anisotropic elasticity based on fabric tensors , 1995 .