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Effects of mechanical forces on maintenance and adaptation of form in trabecular bone

Abstract

The architecture of trabecular bone, the porous bone found in the spine and at articulating joints, provides the requirements for optimal load transfer, by pairing suitable strength and stiffness to minimal weight according to rules of mathematical design1,2,3,4,5,6. But, as it is unlikely that the architecture is fully pre-programmed in the genes7, how are the bone cells informed about these rules, which so obviously dictate architecture? A relationship exists between bone architecture and mechanical usage8—while strenuous exercise increases bone mass9, disuse, as in microgravity and inactivity, reduces it10. Bone resorption cells (osteoclasts) and bone formation cells (osteoblasts) normally balance bone mass in a coupled homeostatic process of remodelling, which renews some 25% of trabecular bone volume per year. Here we present a computational model of the metabolic process in bone that confirms that cell coupling is governed by feedback from mechanical load transfer11,12,13.This model can explain the emergence and maintenance of trabecular architecture as an optimal mechanical structure, as well as its adaptation to alternative external loads.

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Figure 1: Osteocytes are probably mechanosensors which send strain-related signals to lining cells located at the bone surface through the canalicular syncytium.
Figure 2: The trabecular surface is covered by lining cells (LC) and the osteocytes (Ocy) are inside the mineralized tissue.
Figure 3: The proposed regulatory process (see text).
Figure 4: Results of the computer simulation.

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References

  1. Wolff, J. Das Gesetz der Transformation der Knochen (Hirchwild, Berlin, 1892); translated as The Law of Bone Remodeling (trans. Maquet, P. & Furlong, R.) (Springer, Berlin, 1986).

    Google Scholar 

  2. Thompson, D. W. On Growth and Form (Cambridge Univ. Press Cambridge, 1919).

    Google Scholar 

  3. Roesler, H. The history of some fundamental concepts in bone biomechanics. J. Biomechanics 20, 1025–1034 (1987).

    Article  CAS  Google Scholar 

  4. Cowin, S. C. Wollff's law of trabecular bone architecture at remodeling equilibrium. J. Biomech. Engr. 108, 83–88 (1986).

    Article  CAS  Google Scholar 

  5. Carter, D. R., Fyhrie D. P. & Whalen R. T. Trabecular bone density and loading history: Regulation of connective tissue biology by mechanical energy. J. Biomechanics 20, 785–794 (1987).

    Article  CAS  Google Scholar 

  6. Mullender, M. G. & Huiskes, R. A proposal for the regulatory mechanism of Wolff's law. J. Orthop. Res. 13, 503–512 (1995).

    Article  CAS  Google Scholar 

  7. Stewart, I. Life's Other Secret (Allen Lane/Penguin, London, 1998).

    Google Scholar 

  8. Lanyon, L. E. Using functional loading to influence bone mass and architecture: objectives, mechanisms and relationship with estrogen of the mechanically adaptive process in bone. Bone 18, 37S–43S (1996).

    Article  CAS  Google Scholar 

  9. Courteix, D. et al. Effects of physical training on bone mineral density in prepubertal girls: a comparative study between impact-loading and non-impact-loading sports. Osteopor. Int. 8, 152–158 (1998).

    Article  CAS  Google Scholar 

  10. Zerwekh, J. E., Ruml, L. A., Gottschalk, F. & Pak, C. Y. C. The effects of twelve weeks of bed rest on bone histology, biochemical markers of bone turnover, and calcium homeostasis in eleven normal subjects. J. Bone Min. Res. 13, 1594–1601 (1998).

    Article  CAS  Google Scholar 

  11. Frost, H. M. Vital biomechanics. Proposed general concepts for skeletal adaptation to mechanical usage. Calcif. Tissue Int. 45, 145–156 (1987).

    Google Scholar 

  12. Rodan, G. A. Mechanical loading, estrogen deficiency, and the coupling of bone formation to bone resorption. J. Bone Miner. Res. 6, 527–530 (1991).

    Article  CAS  Google Scholar 

  13. Chambers, T. J. The direct and indirect effects of estrogen on bone formation. Adv. Organ Biol. 5B, 627–638 (1998).

    Article  CAS  Google Scholar 

  14. Burger, E. H. & Klein-Nulend, J. Mechanotransduction in bone—role of the lacuno-canalicular network. FASEB J. 13, S101–S112 (1999).

    Article  CAS  Google Scholar 

  15. Skerry, T. M., Bitensky, L., Chayen, J. & Lanyon, L. E. Early strain-related changes in enzyme activity in osteocytes following bone loading in vivo. J. Bone Miner. Res. 4, 783–788 (1989).

    Article  CAS  Google Scholar 

  16. Noble, B. S., Stevens, H., Reeve, J. & Loveridge, N. Identification of apoptotic changes in osteocytes in normal and pathological human bone. Bone 20, 273–282 (1997).

    Article  CAS  Google Scholar 

  17. Smit, T. S. & Burger, E. H. Is BMU-coupling a strain-regulated phenomenon? J. Bone Miner. Res. 15, 301–307 (2000).

    Article  CAS  Google Scholar 

  18. Van Rietbergen, B., Weinans, H., Huiskes, R. & Odgaard, A. A new method to determine trabecular bone elastic properties and loading using micro-mechanical finite-elements methods. J. Biomechanics 28, 69–81 (1995).

    Article  CAS  Google Scholar 

  19. Mosley, J. R. & Lanyon, L. E. Strain rate as a controlling influence on adaptive modeling in response to dynamic loading of the ulna in growing male rats. Bone 23, 313–318 (1998).

    Article  CAS  Google Scholar 

  20. Turner, C. H., Owan, I. & Takano, Y. Mechanotransduction in bone: role of strain rate. Am. J. Physiol. 269, E438–E442 (1995).

    CAS  PubMed  Google Scholar 

  21. Rubin, C. T. & Lanyon, L. E. Osteoregulatory nature of mechanical stimuli: function as a determinant for adaptive bone remodeling. J. Orthop. Res. 5, 300–310 (1987).

    Article  CAS  Google Scholar 

  22. Klein-Nulend, J. et al. Sensivity of osteocytes to biomechanical stress in vitro. FASEB J. 9, 441–445 (1995).

    Article  CAS  Google Scholar 

  23. Cowin, S. C., Moss-Salentijn, L. & Moss, M. L. Candidates for the mechanosensory system in bone. J. Biomech. Eng. 113, 191–197 (1991).

    Article  CAS  Google Scholar 

  24. Burr, D. B., Forwood, M., Fyhrie, D. P., Martin, R. B. & Turner, C. H. Bone microdamage and skeletal fragility in osteoporosis and stress fractures. J. Bone Miner. Res. 12, 6–15 (1997).

    Article  CAS  Google Scholar 

  25. Van Rietbergen, B., Müller, R., Ulrich, D., Rüegsegger, P. & Huiskes, R. Tissue stress and strain in trabeculae of a canine proximal femur can be quantified from computer reconstructions. J. Biomechanics 32, 443–451 (1999).

    Article  CAS  Google Scholar 

  26. Choi, K. & Goldstein, S. A. A comparison of the fatigue behavior of human trabecular and cortical bone tissue. J. Biomechanics 25, 1371–1381 (1992).

    Article  CAS  Google Scholar 

  27. Vashishth, D. et al. In vivo diffuse damage in human vertebral trabecular bone. Bone 26, 147–152 (2000).

    Article  CAS  Google Scholar 

  28. Pazzaglia, U. E., Andrini, L. & Di Nucci, A. The effects of mechanical forces on bones and joints. J. Bone Joint Surg. 79B, 1025–1030 (1997).

    Google Scholar 

  29. Chambers, T. J. & Fuller, K. Bone cells predispose bone surfaces to resorption by exposure of mineral to osteoclastic contact. J. Cell Sci. 6, 155–165 (1985).

    Google Scholar 

  30. Kelly, J. The third culture. Science 279, 992–993 (1998).

    Article  ADS  CAS  Google Scholar 

Download references

Acknowledgements

This work was sponsored in part by the Medical Sciences section of the Netherlands Organization for Research (NWO).

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Correspondence to Rik Huiskes.

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Huiskes, R., Ruimerman, R., van Lenthe, G. et al. Effects of mechanical forces on maintenance and adaptation of form in trabecular bone. Nature 405, 704–706 (2000). https://doi.org/10.1038/35015116

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