The role of the interstitial fluid content in bone remodeling

The role of the interstitial fluid content in bone remodeling

Esposito Luca, Zona Renato, Palladino Simone, Minutolo Vincenzo, Fraldi Massimiliano

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Abstract. Bone is an extraordinary biological material able to modify dynamically its outer shape and inner microstructure in response to chemo-mechanical stimuli coming from the environment adapting its hierarchical microstructure to respond to static and dynamic loads for offering optimal mechanical features, in terms of stiffness and toughness. To date, many theories and mathematical models have been proposed by several authors to describe the remodeling phenomenon, all approaches starting from the adaptive elasticity and the bone maintenance theories. Within this framework, one of the most classical strategies employed in the studies is the so-called Stanford’s law, which allows uploading the effect of the time-dependent load-induced stress stimulus into a biomechanical model to guess the bone structure evolution. In the present work, we generalize this approach by introducing the bone poroelasticity, thus incorporating in the model the role of the fluid content that, by driving nutrients and contributing to the removal of wastes of bone tissue cells, synergistically interacts with the classical stress fields, in this way affecting growth and remodeling of the bone tissue. Two paradigmatic example applications, i.e. a cylindrical slice with internal prescribed displacements idealizing a tract of femoral diaphysis pushed out by the pressure exerted by a femur prosthesis and a bone element in a form of a bent beam, and a real study case of a patient subject to total hip replacement, and CT scanned at 24 hours after surgery and at 1 year post-surgery have been considered. It has to note that the proposed model is capable to catch more realistically both the transition between spongy and cortical regions and the expected non-symmetrical evolution of bone tissue density in the medium-long term, unpredictable with the standard approach. Although limitations still characterize some hypotheses at the basis of the present approach, the proposed model overcomes the intrinsic – and unrealistic – independence of the bone remodeling from the stress sign and from the indirect effect of stress gradients driving nutrients through the flow of the fluid content in the tissue, allowing to predict important spatial asymmetries in bone mass density, so paving the way to more reliable mechanobiological strategies and engineering tools for the faithful prediction of bone remodeling, with implications in diagnosis of risk fracture, optimal design of scaffolds and bone prostheses.

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Published online 3/17/2022, 6 pages
Copyright © 2023 by the author(s)
Published under license by Materials Research Forum LLC., Millersville PA, USA

Citation: Esposito Luca, Zona Renato, Palladino Simone, Minutolo Vincenzo, Fraldi Massimiliano, The role of the interstitial fluid content in bone remodeling, Materials Research Proceedings, Vol. 26, pp 293-298, 2023

DOI: https://doi.org/10.21741/9781644902431-48

The article was published as article 48 of the book Theoretical and Applied Mechanics

Content from this work may be used under the terms of the Creative Commons Attribution 3.0 license. Any further distribution of this work must maintain attribution to the author(s) and the title of the work, journal citation and DOI.

References
[1] Minutolo V, Esposito L, Sacco E, Fraldi M. 2020. Designing stress for optimizing and toughening truss-like structures. Meccanica. 55:1603-1622. https://doi.org/10.1007/s11012-020-01189-z
[2] Della Corte A, Giorgio I, Scerrato D. 2020. A review of recent developments in mathematical modeling of bone remodeling. Proc Inst Mech Eng H: J Eng Med. 234(3):273-281. https://doi.org/10.1177/0954411919857599
[3] Cowin SC, Hegedus DH. 1976. Bone remodeling I: Theory of adaptive elasticity. J Elasticity. 6:313-326. https://doi.org/10.1007/BF00041724
[4] Cowin SC, Sadegh AM, Luo GM. 1992. An evolutionary Wolff’s law for trabecular architecture. J Biomech Eng. 114:129-136. https://doi.org/10.1115/1.2895436
[5] Fyhrie DP, Carter DR. 1986. A unifying principle relating stress to trabecular bone morphology. J Orthop Res. 4:304-317. https://doi.org/10.1002/jor.1100040307
[6] Carter DR. 1987. Mechanical loading history and skeletal biology. J Biomech. 20:1095-1109. https://doi.org/10.1016/0021-9290(87)90027-3
[7] Beaupré GS, Orr TE, Carter DR. 1990a. An approach for time-dependent bone modelling and remodeling-theoretical development. J Orthop Res. 8:651-661. https://doi.org/10.1002/jor.1100080506
[8] Fornells P, Garcia-Aznar JM, Doblaré, M. 2007. A finite element dual porosity approach to model deformation-induced fluid flow in cortical bone. Ann Biomed Eng. 35:1687-1698. https://doi.org/10.1007/s10439-007-9351-5
[9] Fritton SP, Weinbaum S. 2009. Fluid and solute transport in bone: flow-induced mechanotransduction. Annu Rev Fluid Mech. 41:347-374. https://doi.org/10.1146/annurev.fluid.010908.165136
[10] Beaupré GS, Orr TE, Carter DR. 1990b. An approach for time-dependent bone modeling and remodeling–Application: a preliminary remodeling simulation, J Orthop Res. 8:662-670. https://doi.org/10.1002/jor.1100080507
[11] Esposito L, Minutolo V, Fraldi M, Sacco E. 2022. Stress peaks, stiffening and back-flow in bilayer poro-elastic metamaterials. Int J Solids Struct. Volumes 236-237:111334. https://doi.org/10.1016/j.ijsolstr.2021.111334
[12] Esposito, L.; Bifulco, P.; Gargiulo, P.; Gislason, M.K.; Cesarelli, C.; Iuppariello, L.; Jonsson, H.J.; Cutolo, A.; Fraldi, M. 2018. Towards a patient‐specific estimation of intraoperative femoral fracture risk. Comput. Methods Biomech. Biomed. Eng. 21:663-672. https://doi.org/10.1080/10255842.2018.1508570
[13] Esposito L, Minutolo V, Gargiulo P, Jonsson, H, Gislason MK, Fraldi M. 2020. Towards an App to Estimate Patient‐Specific Perioperative Femur Fracture Risk. Appl. Sci. 10:6409. https://doi.org/10.3390/app10186409
[14] Cowin SC. 1999. Bone poroelasticity. J Biomech. 32:217-238. https://doi.org/10.1016/S0021-9290(98)00161-4
[15] Esposito L, Bifulco P, Gargiulo P, Fraldi M. 2016. Singularity-free finite element model of bone through automated voxel-based reconstruction Comput Methods Biomech Biomed Engin. 19(3):257-262. https://doi.org/10.1080/10255842.2015.1014347
[16] Bergmann G, Deuretzbacherb G, Hellerc M, Graichena F, Rohlmanna A, Strauss J, Duda GN. 2001. Hip contact forces and gait patterns from routine activities. J Biomech. 34:859-871. https://doi.org/10.1016/S0021-9290(01)00040-9