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Living with cracks: Damage and repair in human bone

Abstract

Our bones are full of cracks, which form and grow as a result of daily loading activities. Bone is the major structural material in our bodies. Although weaker than many engineering materials, it has one trick that keeps it ahead — it can repair itself. Small cracks, which grow under cyclic stresses by the mechanism of fatigue, can be detected and removed before they become long enough to be dangerous. This article reviews the work that has been done to understand how cracks form and grow in bone, and how they can be detected and repaired in a timely manner. This is truly an interdisciplinary research field, requiring the close cooperation of materials scientists, biologists and engineers.

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Figure 1: Bone's repair mechanism.
Figure 2: The structure of bone.
Figure 3: Damage in bone.
Figure 4: Investigations of crack behaviour.
Figure 5: Data from Akkus and Rimnac37 showing the growth characteristics of various individual cracks (labelled A1, A2, B1, B2, B3, C1, D1, D2).

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References

  1. Martin, R. B. & Burr, D. B. A hypothetical mechanism for ths timulation of osteonal remodelling by fatigue damage. J. Biomech. 15, 137–139 (1982).

    Article  CAS  Google Scholar 

  2. Martin, R. B. Fatigue damage, remodeling, and the minimization of skeletal weight. J. Theor. Biol. 220, 271–276 (2003).

    Article  Google Scholar 

  3. Burr, D. B. Targeted and nontargeted remodeling. Bone 30, 2–4 (2002).

    Article  CAS  Google Scholar 

  4. Tsuji, K. et al. BMP2 activity, although dispensible for bone formation, is required for the initiation of fracture healing. Nature Genet. 38, 1424–1429 (2006).

    Article  CAS  Google Scholar 

  5. Burr, D. B. & Martin, B. R. Calculating the probability that microcracks initiate resorption spaces. J. Biomech. 26, 613–616 (1993).

    Article  CAS  Google Scholar 

  6. Mori, S. & Burr, D. B. Increased intracortical remodeling following fatigue damage. Bone 14, 103–109 (1993).

    Article  CAS  Google Scholar 

  7. Lee, T. C., Staines, A. & Taylor, D. Bone adaptation to load: Microdamage as a stimulus for bone remodelling. J. Anat. 201, 437–446 (2002).

    Article  CAS  Google Scholar 

  8. Taylor, D. Fatigue of bone and bones: An analysis based on stressed volume. J. Orthop. Res. 16, 163–169 (1998).

    Article  CAS  Google Scholar 

  9. Boyde, A. The real response of bone to exercise. J. Anat. 203, 173–189 (2003).

    Article  Google Scholar 

  10. Frost, H. M. Presence of microscopic cracks in vivo in bone. Henry Ford Hosp. Med. Bull. 8, 25–35 (1960).

    Google Scholar 

  11. O'Brien, F., Taylor, D. & Lee, T. C. An improved labelling technique for monitoring microcrack growth in bone. J. Biomech. 35, 523–526 (2002).

    Article  Google Scholar 

  12. O'Brien, F. J., Taylor, D. & Lee, T. C. Microcrack accumulation at different intervals during fatigue testing of compact bone. J. Biomech. 36, 973–980 (2003).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  15. Li, J., Miller, M. A., Hutchins, G. D. & Burr, D. B. Imaging bone microdamage in vivo with positron emission tomography. Bone 37, 819–824 (2005).

    Article  Google Scholar 

  16. Silva, M. J. et al. In vivo skeletal imaging of 18F-fluoride with positron emission tomography reveals damage- and time-dependent responses to fatigue loading in the rat ulna. Bone 39, 229–236 (2006).

    Article  CAS  Google Scholar 

  17. Lee, T. C. et al. Detecting microdamage in bone. J. Anat. 203, 161–172 (2003).

    Article  CAS  Google Scholar 

  18. Kawahara, D. & Murakami, T. Evaluation for mechanism of diffuse damage in cortical bone. Trans. Jpn Soc. Mech. Eng. A 71, 936–943 (2005).

    Article  CAS  Google Scholar 

  19. Qiu, S., Rao, D. S., Fyhrie, D. P., Palnitkar, S. & Parfitt, A. M. The morphological association between microcracks and osteocyte lacunae in human cortical bone. Bone 37, 10–15 (2005).

    Article  Google Scholar 

  20. Sobelman, O. S. et al. Do microcracks decrease or increase fatigue resistance in cortical bone? J. Biomech. 37, 1295–1303 (2004).

    Article  CAS  Google Scholar 

  21. Frank, J. D. et al. Aging and accumulation of microdamage in canine bone. Bone 30, 201–206 (2002).

    Article  CAS  Google Scholar 

  22. Schaffler, M. B., Choi, K. & Milgrom, C. Aging and matrix microdamage accumulation in human compact bone. Bone 17, 521–525 (1995).

    Article  CAS  Google Scholar 

  23. Fazzalari, N. L., Forwood, M. R., Smith, K., Manthey, B. A. & Herreen, P. Assessment of cancellous bone quality in severe osteoarthrosis: Bone mineral density, mechanics, and microdamage. Bone 22, 381–388 (1998).

    Article  CAS  Google Scholar 

  24. Mori, S., Harruff, R., Ambrosius, W. & Burr, D. B. Trabecular bone volume and microdamage accumulation in the femoral heads of women with and without femoral neck fractures. Bone 21, 521–526 (1997).

    Article  CAS  Google Scholar 

  25. Dai, R. C., Liao, E. Y., Yang, C., Wu, X. P. & Jiang, Y. Microcracks: An alternative index for evaluating bone biomechanical quality. J. Bone Miner. Metab. 22, 215–223 (2004).

    Article  CAS  Google Scholar 

  26. Muir, P. et al. Role of endochondral ossification of articular cartilage and functional adaptation of the subchondral plate in the development of fatigue microcracking of joints. Bone 38, 342–349 (2006).

    Article  CAS  Google Scholar 

  27. Huiskes, R., Rulmerman, R., Van Lenthe, G. H. & Janssen, J. D. Effects of mechanical forces on maintenance and adaptation of form in trabecular bone. Nature 405, 704–706 (2000).

    Article  CAS  Google Scholar 

  28. Taylor, D. & Lee, T. C. Microdamage and mechanical behaviour: Predicting failure and remodelling in compact bone. J. Anat. 203, 203–211 (2003).

    Article  CAS  Google Scholar 

  29. Nalla, R. K., Kruzic, J. J., Kinney, J. H. & Ritchie, R. O. Effect of aging on the toughness of human cortical bone: Evaluation by R-curves. Bone 35, 1240–1246 (2004).

    Article  CAS  Google Scholar 

  30. Nalla, R. K., Kruzic, J. J., Kinney, J. H. & Ritchie, R. O. Mechanistic aspects of fracture and R-curve behavior in human cortical bone. Biomaterials 26, 217–231 (2005).

    Article  CAS  Google Scholar 

  31. Malik, C. L., Stover, S. M., Martin, R. B. & Gibeling, J. C. Equine cortical bone exhibits rising R-curve fracture mechanics. J. Biomech. 36, 191–198 (2003).

    Article  CAS  Google Scholar 

  32. Nalla, R. K., lken, J. S., Kinney, J. H. & Ritchie, R. O. Fracture in human cortical bone: Local fracture criteria and toughening mechanisms. J. Biomech. 38, 1517–1525 (2005).

    Article  CAS  Google Scholar 

  33. Vashishth, D., Tanner, K. E. & Bonfield, W. Experimental validation of a microcracking-based toughening mechanism for cortical bone. J. Biomech. 36, 121–124 (2003).

    Article  CAS  Google Scholar 

  34. Yeni, Y. N. & Fyhrie, D. P. A rate-dependent microcrack-bridging model that can explain the strain rate dependency of cortical bone apparent yield strength. J. Biomech. 36, 1343–1353 (2003).

    Article  Google Scholar 

  35. Currey, J. D. Mechanical properties of bone tissues with greatly differing functions. J. Biomech. 12, 313–319 (1979).

    Article  CAS  Google Scholar 

  36. Hazenberg, J. G., Taylor, D. & Lee, T. C. Mechanisms of short crack growth at constant stress in bone. Biomaterials 27, 2114–2122 (2006).

    Article  CAS  Google Scholar 

  37. Akkus, O. & Rimnac, C. M. Cortical bone tissue resists fatigue fracture by deceleration and arrest of microcrack growth. J. Biomech. 34, 757–764 (2001).

    Article  CAS  Google Scholar 

  38. O'Brien, F. J., Taylor, D. & Lee, T. C. The effect of bone microstructure on the initiation and growth of microcracks. J. Orthop. Res. 23, 475–480 (2005).

    Article  Google Scholar 

  39. Nyman, J. S., Reyes, M. & Wang, X. Effect of ultrastructural changes on the toughness of bone. Micron 36, 566–582 (2005).

    Article  CAS  Google Scholar 

  40. Wang, X., Xiaoe, L. I., Shen, X. & Agrawal, C. M. Age-related changes of noncalcified collagen in human cortical bone. Ann. Biomed. Eng. 31, 1365–1371 (2003).

    Article  Google Scholar 

  41. Zioupos, P., Currey, J. D. & Hamer, A. J. The role of collagen in the declining mechanical properties of aging human cortical bone. J. Biomed. Mater. Res. 45, 108–116 (1999).

    Article  CAS  Google Scholar 

  42. Mitchell, E. J., Stawarz, A. M., Kayacan, R. & Rimnac, C. M. The effect of gamma radiation sterilization on the fatigue crack propagation resistance of human cortical bone. J. Bone Joint Surg. A 86, 2648–2657 (2004).

    Article  Google Scholar 

  43. Currey, J. D. Effects of differences in mineralization on the mechanical properties of bone. Phil. Trans. R. Soc. Lond. B 304, 509–518 (1984).

    Article  CAS  Google Scholar 

  44. Wasserman, N., Yerramshetty, J. & Akkus, O. Microcracks colocalize within highly mineralized regions of cortical bone tissue. Eur. J. Morphol. 42, 43–51 (2005).

    Article  Google Scholar 

  45. Nyman, J. S. et al. The influence of water removal on the strength and toughness of cortical bone. J. Biomech. 39, 931–938 (2006).

    Article  Google Scholar 

  46. Akkus, O., Yeni, Y. N. & Wasserman, N. Fracture mechanics of cortical bone tissue: A hierarchical perspective. Crit. Rev. Biomed. Eng. 32, 379–425 (2004).

    Article  Google Scholar 

  47. Vashishth, D. Age-dependent biomechanical modifications in bone. Crit. Rev. Eukar. Gene 15, 343–357 (2005).

    Article  Google Scholar 

  48. Turner, C. H., Robling, A. G., Duncan, R. L. & Burr, D. B. Do bone cells behave like a neuronal network? Calcified Tissue Int. 70, 435–442 (2002).

    Article  CAS  Google Scholar 

  49. Burger, E. H., Klein-Nulend, J. & Smit, T. H. Strain-derived canalicular fluid flow regulates osteoclast activity in a remodelling osteon — a proposal. J. Biomech. 36, 1453–1459 (2003).

    Article  Google Scholar 

  50. Klein-Nulend, J., Bacabac, R. G. & Mullender, M. G. Mechanobiology of bone tissue. Pathol. Biol. 53, 576–580 (2005).

    Article  CAS  Google Scholar 

  51. Bentolila, V. et al. Intracortical remodeling in adult rat long bones after fatigue loading. Bone 23, 275–281 (1998).

    Article  CAS  Google Scholar 

  52. Noble, B., Alini, M. & Richards, R. G. Bone microdamage and cell apoptosis. Eur. Cells Mater. 6, 46–55 (2003).

    Article  CAS  Google Scholar 

  53. Noble, B. S. et al. Mechanical loading: Biphasic osteocyte survival and targeting of osteoclasts for bone destruction in rat cortical bone. Am. J. Physiol. Cell Ph. 284, C934–C943 (2003).

    Article  CAS  Google Scholar 

  54. Colopy, S. A. et al. Response of the osteocyte syncytium adjacent to and distant from linear microcracks during adaptation to cyclic fatigue loading. Bone 35, 881–891 (2004).

    Article  CAS  Google Scholar 

  55. 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 Min. Res. 15, 60–67 (2000).

    Article  CAS  Google Scholar 

  56. 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, 65–75 (2003).

    Article  CAS  Google Scholar 

  57. Hazenberg, J. G., Freeley, M., Foran, E., Lee, T. C. & Taylor, D. Microdamage: a cell transducing mechanism based on ruptured osteocyte processes. J. Biomech. 39, 2096–2103 (2006).

    Article  Google Scholar 

  58. Huiskes, R. in Non-cemented Total Hip Arthroplasty (ed. Fitzgerald, R.) 283–302 (Raven, New York, 1988).

    Google Scholar 

  59. Prendergast, P. J. & Taylor, D. Prediction of bone adaptation using damage accumulation. J. Biomech. 27, 1067–1076 (1994).

    Article  CAS  Google Scholar 

  60. Martin, B. Mathematical model for repair of fatigue damage and stress fracture in osteonal bone. J. Orthop. Res. 13, 309–316 (1995).

    Article  CAS  Google Scholar 

  61. Hazelwood, S. J., Martin, R. B., Rashid, M. M. & Rodrigo, J. J. A mechanistic model for internal bone remodeling exhibits different dynamic responses in disuse and overload. J. Biomech. 34, 299–308 (2001).

    Article  CAS  Google Scholar 

  62. Nyman, J. S., Yeh, O. C., Hazelwood, S. J. & Martin, R. B. A theoretical analysis of long-term bisphosphonate effects on trabecular bone volume and microdamage. Bone 35, 296–305 (2004).

    Article  CAS  Google Scholar 

  63. Heaney, R. P. Is the paradigm shifting? Bone 33, 457–465 (2003).

    Article  Google Scholar 

  64. Taylor, D. & Lee, T. C. A crack growth model for the simulation of fatigue in bone. Int. J. Fatigue 25, 387–395 (2003).

    Article  Google Scholar 

  65. Taylor, D. Scaling effects in the fatigue strength of bones from different animals. J. Theor. Biol. 206, 299–306 (2000).

    Article  CAS  Google Scholar 

  66. Tortora, G. J. Principles of Human Anatomy (Wiley, New York, 2002).

    Google Scholar 

  67. Zarrinkalam, K. H., Kuliwaba, J. S., Martin, R. B., Wallwork, M. A. B. & Fazzalari, N. L. New insights into the propagation of fatigue damage in cortical bone using confocal microscopy and chelating fluorochromes. Eur. J. Morph. 42, 81–90 (2005).

    Article  CAS  Google Scholar 

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Correspondence to David Taylor.

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Taylor, D., Hazenberg, J. & Lee, T. Living with cracks: Damage and repair in human bone. Nature Mater 6, 263–268 (2007). https://doi.org/10.1038/nmat1866

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