To understand Wolff’s law, bone adaptation by remodeling at the cellular and tissue levels has been discussed extensively through experimental and simulation studies. For the clinical application of a bone remodeling simulation, it is significant to establish a macroscopic model that incorporates clarified microscopic mechanisms. In this study, we proposed novel macroscopic models based on the microscopic mechanism of osteocytic mechanosensing, in which the flow of fluid in the lacuno-canalicular porosity generated by fluid pressure gradients plays an important role, and theoretically evaluated the proposed models, taking biological rationales of bone adaptation into account. The proposed models were categorized into two groups according to whether the remodeling equilibrium state was defined globally or locally, i.e., the global or local uniformity models. Each remodeling stimulus in the proposed models was quantitatively evaluated through image-based finite element analyses of a swine cancellous bone, according to two introduced criteria associated with the trabecular volume and orientation at remodeling equilibrium based on biological rationales. The evaluation suggested that nonuniformity of the mean stress gradient in the local uniformity model, one of the proposed stimuli, has high validity. Furthermore, the adaptive potential of each stimulus was discussed based on spatial distribution of a remodeling stimulus on the trabecular surface. The theoretical consideration of a remodeling stimulus based on biological rationales of bone adaptation would contribute to the establishment of a clinically applicable and reliable simulation model of bone remodeling.
Bone adaptation Wolff’s law Biological rationale Model reduction Multiscale biomechanics Mechanobiology
This is a preview of subscription content, log in to check access.
This work was partially supported by the Advanced Research and Development Programs for Medical Innovation from the Japan Agency for Medical Research and Development (AMED-CREST).
Adachi T, Tomita Y, Sakaue H, Tanaka M (1997) Simulation of trabecular surface remodeling based on local stress nonuniformity. JSME Int Ser C 40:782–792CrossRefGoogle Scholar
Adachi T, Tsubota K, Tomita Y, Hollister SJ (2001) Trabecular surface remodeling simulation for cancellous bone using microstructural voxel finite element models. J Biomech Eng 123:403–409. doi:10.1115/1.1392315CrossRefGoogle Scholar
Burger EH, Klein-Nulend J (1999) Mechanotransduction in bone—role of the lacuno-canalicular network. FASEB J 13:S101–S112Google Scholar
Busse B, Djonic D, Milovanovic P et al (2010) Decrease in the osteocyte lacunar density accompanied by hypermineralized lacunar occlusion reveals failure and delay of remodeling in aged human bone. Aging Cell 9:1065–1075. doi:10.1111/j.1474-9726.2010.00633.xCrossRefGoogle Scholar
Fritsch A, Hellmich C (2007) “Universal” microstructural patterns in cortical and trabecular, extracellular and extravascular bone materials: Micromechanics-based prediction of anisotropic elasticity. J Theor Biol 244:597–620. doi:10.1016/j.jtbi.2006.09.013CrossRefGoogle Scholar
Hambli R, Katerchi H, Benhamou C-L (2011) Multiscale methodology for bone remodelling simulation using coupled finite element and neural network computation. Biomech Model Mechanobiol 10:133–145. doi:10.1007/s10237-010-0222-xCrossRefGoogle Scholar
Hasegawa M, Adachi T, Takano-Yamamoto T (2015) Computer simulation of orthodontic tooth movement using CT image-based voxel finite element models with the level set method. Comput Methods Biomech Biomed Eng. doi:10.1080/10255842.2015.1042463Google Scholar
Huiskes R, Ruimerman R, van Lenthe GH, Janssen JD (2000) Effects of mechanical forces on maintenance and adaptation of form in trabecular bone. Nature 405:704–706. doi:10.1038/35015116CrossRefGoogle Scholar
Kameo Y, Ootao Y, Ishihara M (2016) Theoretical investigation of the effect of bending loads on the interstitial fluid flow in a poroelastic lamellar trabecula. J Biomech Sci Eng 11:15–00663. doi:10.1299/jbse.15-00663CrossRefGoogle Scholar
Reina-Romo E, Gómez-Benito MJ, Sampietro-Fuentes A et al (2011) Three-dimensional simulation of mandibular distraction osteogenesis: Mechanobiological analysis. Ann Biomed Eng 39:35–43. doi:10.1007/s10439-010-0166-4CrossRefGoogle Scholar
Tsubota K, Adachi T (2005) Spatial and temporal regulation of cancellous bone structure: characterization of a rate equation of trabecular surface remodeling. Med Eng Phys 27:305–11. doi:10.1016/j.medengphy.2004.09.013
Tsubota K, Adachi T (2006) Simulation study on local and integral mechanical quantities at single trabecular level as candidates of remodeling stimuli. J Biomech Sci Eng 1:124–135. doi:10.1299/jbse.1.124CrossRefGoogle Scholar
Tsubota K, Adachi T, Tomita Y (2002) Functional adaptation of cancellous bone in human proximal femur predicted by trabecular surface remodeling simulation toward uniform stress state. J Biomech 35:1541–1551. doi:10.1016/S0021-9290(02)00173-2CrossRefGoogle Scholar
Tsubota K, Suzuki Y, Yamada T et al (2009) Computer simulation of trabecular remodeling in human proximal femur using large-scale voxel FE models: approach to understanding Wolff’s law. J Biomech 42:1088–1094. doi:10.1016/j.jbiomech.2009.02.030CrossRefGoogle Scholar
van Hove RP, Nolte PA, Vatsa A et al (2009) Osteocyte morphology in human tibiae of different bone pathologies with different bone mineral density - Is there a role for mechanosensing? Bone 45:321–329. doi:10.1016/j.bone.2009.04.238CrossRefGoogle Scholar