×

A theory for bone resorption based on the local rupture of osteocytes cells connections: a finite element study. (English) Zbl 1315.92019

Summary: In this work, a bone damage resorption finite element model based on the disruption of the inhibitory signal transmitted between osteocytes cells in bone due to damage accumulation is developed and discussed. A strain-based stimulus function coupled to a damage-dependent spatial function is proposed to represent the connection between two osteocytes embedded in the bone tissue. The signal is transmitted to the bone surface to activate bone resorption. The proposed model is based on the idea that the osteocyte signal reduction is not related to the reduction of the stimulus sensed locally by osteocytes due to damage, but to the difficulties for the signal in travelling along a disrupted area due to microcracks that can destroy connections of the intercellular network between osteocytes and bone-lining cells. To check the potential of the proposed model to predict the damage resorption process, two bone resorption mechano-regulation rules corresponding to two mechanotransduction approaches have been implemented and tested: (1) Bone resorption based on a coupled strain-damage stimulus function without ruptured osteocyte connections (NROC); and (2) Bone resorption based on a strain stimulus function with ruptured osteocyte connections (ROC). The comparison between the results obtained by both models, shows that the proposed model based on ruptured osteocytes connections predicts realistic results in conformity with previously published findings concerning the fatigue damage repair in bone.

MSC:

92C30 Physiology (general)
92C50 Medical applications (general)

References:

[1] Marotti, G.; Cane, V.; Palazzini, S.; Palumbo, C., Structure-function relationships in the osteocytes, Ital. J. Miner. Electrolyte Metab., 93-106 (1990)
[2] Hazenberg, J. G.; Freeley, M.; Foran, A.; Lee, T. C.; Taylor, D., Microdamage: a cell transducing mechanism based on ruptured osteocyte processes, J. Biomech., 39, 2096-2103 (2006)
[3] McNamara, L. M.; Prendergast, J. P., Bone remodeling algorithms incorporating both stain and microdamage stimuli, J. Biomech., 40, 6, 1381-1391 (2007)
[4] Cowin, S. C.; Moss, M. L., Mechanosensory mechanisms in bone, Bone Mechanics Handbook, 29-1-29-17 (2001), CRC Press: CRC Press Boca Raton, Chapter 29
[5] Sikavitsas, V. I.; Temeno, J. S.; Mikos, A. G., Biomaterials and bone mechanotransduction, Biomaterials, 22, 2581-2593 (2001)
[6] Martin, R. B., Toward a unifying theory of bone remodeling, Bone, 26, 1, 1-6 (2000)
[7] Kelly, D. J.; Prendergast, P. J., Mechano-regulation of stem cell differentiation and tissue regeneration in osteochondral defects, J. Biomech., 38, 7, 1413-1422 (2005)
[8] Frost, H. M., Bone microdamage: factors that impair its repair, (Uhthoff, H. K., Current Concepts in Bone Fragility (1985), Springer: Springer Berlin), 123-148
[9] Martin, R. B.; Burr, D. R.; Sharkey, N. A., Skeletal Tissue Mechanics (1998), Springer: Springer New York
[10] Noble, B., Bone microdamage and cell apoptosis, Eur. Cell Mater., 21, 6, 46-55 (2003)
[11] Martin, R. B., Fatigue microdamage as an essential element of bone mechanics and biology, Calcif. Tissue Int., 73, 2, 101-107 (2003)
[12] Taylor, D.; Hazenberg, J. G.; Lee, T. C., The cellular transducer in damage-stimulated bone remodelling: a theoretical investigation using fracture mechanics, J. Theor. Biol., 225, 1, 65-75 (2003) · Zbl 1464.92033
[13] Hambli, R., Connecting mechanics and bone cell activities in the bone remodeling process: an integrated finite element modeling, Front. Bioeng. Biotechnol., 8, 2, 6 (2014)
[14] Hambli, R.; Lespessailles, E.; Benhamou, C. L., Integrated remodeling to-fracture finite element model of human proximal femur behaviour, J. Mech. Behav. Biomed. Mater., 17, 89-106 (2013)
[15] Garcia-Aznar, J. M.; Rueberg, T.; Doblare, M., A bone remodelling model coupling microdamage growth and repair by 3D BMU-activity, Biomech. Model Mechanobiol., 4, 147-167 (2005)
[16] Parfitt, A. M., The cellular basis of bone remodelling: the quantum concept re-examined in light of recent advances in the cell biology of bone, Calcif. Tissue Int., 36, S37-S45 (1984)
[17] Ausk, B. J.; Gross, T. S.; Srinivasan, S., An agent based model for real-time signaling induced ino steocytic networks by mechanical stimuli, J. Biomech., 39, 2638-2646 (2006)
[18] Jahani, M.; Genever, P. G.; Patton, R. J.; Ahwal, F.; Fagan, M. J., The effect of osteocyte apoptosis on signalling in the osteocyte and bone lining cell network: a computer simulation, J. Biomech., 45, 16, 2876-2883 (2012)
[19] Hambli, R.; Soulat, D.; Gasser, A.; Benhamou, C. L., Strain-damage coupled algorithm for cancellous bone mechano-regulation with spatial function influence, Comput. Methods Appl. Mech. Eng., 198, 33-36, 2673-2682 (2009) · Zbl 1228.74048
[20] Chaboche, J. L., Continuum damage mechanics—a tool to describe phenomena before crack initiation, Nucl. Eng. Des., 64, 233-247 (1981)
[22] Mullender, M. G.; Huiskes, R., Proposal for the regulatory mechanism of Wolff’s law, J. Orthop. Res., 13, 4, 503-512 (1995)
[23] Mikic, B.; Carter, D. R., Bone strain gage data and theoretical models of functional adaptation, J. Biomech., 28, 4, 465-469 (1995)
[24] Dooley Dooley, C.; Tisbo, P.; Lee, T. C.; Taylor, D., Rupture of osteocyte processes across microcracks: the effect of crack length and stress, Biomech. Model Mechanobiol., 11, 6, 759-766 (2012)
[26] Cowin, S. C.; Weinbaum, S.; Zeng, Y., A case for bone canaliculi as the anatomical site of strain generated potentials, J. Biomech., 28, 1281-1297 (1995)
[27] You, J.; Yellowley, C. E.; Donahue, H. J.; Zhang, Y.; Chen, Q.; Jacobs, C. R., Substrate deformation levels associated with routine physical activity are less stimulatory to bone cells relative to loading-induced oscillatory fluid flow, J. Biomech. Eng., 122, 387-393 (2000)
[28] Vashishth, D.; Verborgt, O.; Divine, G.; Schaffler, M. B.; Fyhrie, D. P., Decline in osteocyte lacunar density in human cortical bone is associated with accumulation of microcracks with age, Bone, 26, 375-380 (2000)
[29] Mullender, M. G.; van der Meer, D. D.; Huiskes, R.; Lips, P., Osteocyte density changes in aging and osteoporosis, Bone, 18, 2, 109-113 (1996)
[30] Schulte, F. A.; Ruffoni, D.; Lambers, F. M.; Christen, D.; Webster, D. J.; Kuhn, G.; Muller, R., Local mechanical stimuli regulate bone formation and resorption in mice at the tissue level, PLoS ONE, 8, 4, e62172 (2013)
[31] Burr, D. B., Remodeling and the repair of fatigue damage, Calcif. Tissue Int., 53, Suppl. 1, S75-S81 (1993)
[32] Burr, D. B.; Hooser, M., Alteration to the en bloc basic fuschin staining protocol for the demonstration of microdamage produced in vivo, Bone, 17, 431-433 (1995)
[33] Hambli, R.; Barkaoui, A., Physically based 3D finite element model of a single mineralized collagen microfibril, J. Theor. Biol., 301, 28-41 (2012) · Zbl 1397.92052
[34] Knothe Tate, M. L.; Adamson, J. R.; Tami, A. E.; Bauer, T. W., The osteocyte, Int. J. Biochem. Cell Biol., 36, 1-8 (2004)
[35] Marotti, G., The osteocyte as a wiring transmission system, J. Musculoskel. Neuron Interact., 1, 2, 133-136 (2000)
[36] Mi, L. Y.; Basu, M.; Fritton, S. P.; Cowin, S. C., Analysis of avian bone response to mechanical loading, Part Two: Development of a computational connected cellular network to study bone intercellular communication, Biomech. Model Mechanobiol., 4, 132-146 (2005)
[37] Verborgt, O.; Gibson, G. J.; Schaffler, M. B., Loss of osteocyte integrity in association with microdamage and bone remodeling after fatigue in vivo, J. Bone Miner. Res., 15, 60-67 (2000)
[38] Hambli, R., Multiscale prediction of crack density and crack length accumulation in trabecular bone based on neural networks and finite element simulation, Int. J. Numer. Methods Biomed. Eng., 27, 4, 461-475 (2011) · Zbl 1215.92004
[39] Hambli, R.; Allaoui, S., A robust 3D finite element simulation of human proximal femur progressive fracture under stance load with experimental validation, Ann. Biomed. Eng., 41, 12, 2515-2527 (2013)
[40] Burr, D. B.; Martin, R. B.; Schaffler, M. B.; Radin, E. L., Bone remodeling in response to in vivo fatigue microdamage, J. Biomech., 18, 189-200 (1985)
[41] Burr, D. B.; Milgrom, C.; Boyd, R. D.; Higgins, W. L.; Robin, G.; Radin, E. L., Experimental stress fractures of the tibia. Biological and mechanical aetiology in rabbits, J. Bone Joint Surg. Br., 72B, 370-375 (1990)
[42] Schaffler, M. B.; Choi, K.; Milgrom, C., Aging and matrix microdamage accumulation in human compact bone, Bone, 17, 521-525 (1995)
[43] Mori, S.; Burr, D. B., Increased intracortical remodeling following fatigue damage, Bone, 14, 103-109 (1993)
[44] Martin, R. B., Targeted bone remodeling involves BMU steering as well as activation, Bone, 40, 1574-1580 (2007)
[45] Burr, D. B.; Forwood, M. K.; Fyhrie, D. P.; Martin, R. B.; Schaffler, MS; Turner, CH, Bone microdamage and skeletal fragility in osteoporotic and stress fractures, J. Bone Miner. Res., 12, 6-15 (1997)
[46] Noble, B. S.; Peet, N.; Stevens, H. Y.; Brabbs, A.; Mosley, J. R.; Reilly, G. C.; Reeve, J.; Skerry, T. M.; Lanyon, L. E., Mechanical loading: biphasic osteocyte survival and targeting of osteoclasts for bone destruction in rat cortical bone, Am. J. Physiol. - Cell Physiol., 284, C934-C943 (2003)
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.