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The Periosteal Bone Surface is Less Mechano-Responsive than the Endocortical

Birkhold, Annette I., Razi, Hajar, Duda, Georg N., Weinkamer, Richard, Checa, Sara, Willie, Bettina M.·2016·Scientific Reports
DOI 10.1038/srep23480
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Abstract

Dynamic processes modify bone micro-structure to adapt to external loading and avoid mechanical failure. Age-related cortical bone loss is thought to occur because of increased endocortical resorption and reduced periosteal formation. Differences in the (re)modeling response to loading on both surfaces, however, are poorly understood. Combining in-vivo tibial loading, in-vivo micro-tomography and finite element analysis, remodeling in C57Bl/6J mice of three ages (10, 26, 78 week old) was analyzed to identify differences in mechano-responsiveness and its age-related change on the two cortical surfaces. Mechanical stimulation enhanced endocortical and periosteal formation and reduced endocortical resorption; a reduction in periosteal resorption was hardly possible since it was low, even without additional loading. Endocortically a greater mechano-responsiveness was identified, evident by a larger bone-forming surface and enhanced thickness of formed bone packets, which was not detected periosteally. Endocortical mechano-responsiveness was better conserved with age, since here adaptive response declined continuously with aging, whereas periosteally the main decay in formation response occurred already before adulthood. Higher endocortical mechano-responsiveness is not due to higher endocortical strains. Although it is clear structural adaptation varies between different bones in the skeleton, this study demonstrates that adaptation varies even at different sites within the same bone.

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Research works printed but not linked: 48

  1. Currey, J. D. Bones. Structure and mechanics (Princeton University Press, Princeton, NJ, 2002).
  2. Neu, C. M., Rauch, F., Manz, F. & Schoenau, E. Modeling of cross-sectional bone size, mass and geometry at the proximal radius: a study of normal bone development using peripheral quantitative computed tomography. Osteoporosis int 12, 538–547 (2001). · DOI
  3. Riggs, B. L. et al. A population-based assessment of rates of bone loss at multiple skeletal sites: evidence for substantial trabecular bone loss in young adult women and men. J Bone Miner Res 23, 205–214 (2008). · DOI · Paper page
  4. Szulc, P. & Delmas, P. D. Bone loss in elderly men: increased endosteal bone loss and stable periosteal apposition. The prospective MINOS study. Osteoporosis int 18, 495–503 (2007). · DOI
  5. Szulc, P., Seeman, E., Duboeuf, F., Sornay-Rendu, E. & Delmas, P. D. Bone fragility: failure of periosteal apposition to compensate for increased endocortical resorption in postmenopausal women. J Bone Miner Res 21, 1856–1863 (2006). · DOI
  6. Ruff, C. B. & Hayes, W. C. Sex differences in age-related remodeling of the femur and tibia. J. Orthop. Res. 6, 886–896 (1988). · DOI · Paper page
  7. Frost, H. M. On the estrogen-bone relationship and postmenopausal bone loss: A new model. J Bone Miner Res 14, 1473–1477 (1999). · DOI · Paper page
  8. Eriksen, E. F., Langdahl, B., Vesterby, A., Rungby, J. & Kassem, M. Hormone replacement therapy prevents osteoclastic hyperactivity: A histomorphometric study in early postmenopausal women. J Bone Miner Res 14, 1217–1221 (1999). · DOI
  9. Recker, R., Lappe, J., Davies, K. M. & Heaney, R. Bone remodeling increases substantially in the years after menopause and remains increased in older osteoporosis patients. J Bone Miner Res 19, 1628–1633 (2004). · DOI · Paper page
  10. Uusi-Rasi, K. et al. Effect of alendronate and exercise on bone and physical performance of postmenopausal women: a randomized controlled trial. Bone 33, 132–143 (2003). · DOI
  11. Kukuljan, S. et al. Independent and Combined Effects of Calcium-Vitamin D-3 and Exercise on Bone Structure and Strength in Older Men: An 18-Month Factorial Design Randomized Controlled Trial. J. Clin. Endocrinol. Metab. 96, 955–963 (2011). · DOI · Paper page
  12. Srinivasan, S. et al. Rescuing Loading Induced Bone Formation at Senescence. PLoS Comput. Biol. 6 (2010). · DOI
  13. Turner, C. H., Takano, Y. & Owan, I. Aging changes mechanical loading thresholds for bone formation in rats. J Bone Miner Res 10, 1544–1549 (1995). · DOI · Paper page
  14. Rubin, C. T., Bain, S. D. & McLeod, K. J. Suppression of the osteogenic response in the aging skeleton. Calc tissue int 50, 306–313 (1992). · DOI · Paper page
  15. Willie, B. M. et al. Diminished response to in vivo mechanical loading in trabecular and not cortical bone in adulthood of female C57Bl/6 mice coincides with a reduction in deformation to load. Bone 55, 335–346 (2013). · DOI
  16. Brodt, M. D. & Silva, M. J. Aged mice have enhanced endocortical response and normal periosteal response compared with young-adult mice following 1 week of axial tibial compression. J Bone Miner Res 25, 2006–2015 (2010). · DOI
  17. Buhl, K. M. et al. Aged bone displays an increased responsiveness to low-intensity resistance exercise. J. Appl. Physiol. 90, 1359–1364 (2001). · DOI
  18. Raab, D. M., Smith, E. L., Crenshaw, T. D. & Thomas, D. P. Bone mechanical properties after exercise training in young and old rats. J. Appl. Physiol. 68, 130–134 (1990). · DOI
  19. Umemura, Y., Ishiko, T., Yamauchi, T., Kurono, M. & Mashiko, S. Five jumps per day increase bone mass and breaking force in rats. J Bone Miner Res 12, 1480–1485 (1997). · DOI · Paper page
  20. Holguin, N., Brodt, M. D., Sanchez, M. E. & Silva, M. J. Aging diminishes lamellar and woven bone formation induced by tibial compression in adult C57BL/6. Bone 65, 83–91 (2014). · DOI
  21. Birkhold, A. I. et al. Mineralizing surface is the main target of mechanical stimulation independent of age: 3D dynamic in vivo morphometry. Bone 66, 15–25 (2014). · DOI
  22. Birkhold, A. I. et al. The influence of age on adaptive bone formation and bone resorption. Biomaterials 35, 9290–9301 (2014). · DOI
  23. Birkhold, A. I. et al. Monitoring in vivo (re)modeling: A computational approach using 4D microCT data to quantify bone surface movements. Bone 75, 210–221 (2015). · DOI
  24. Schulte, F. A., Lambers, F. M., Kuhn, G. & Muller, R. In vivo micro-computed tomography allows direct three-dimensional quantification of both bone formation and bone resorption parameters using time-lapsed imaging. Bone 48, 433–442 (2011). · DOI
  25. Waarsing, J. H. et al. Detecting and tracking local changes in the tibiae of individual rats. A novel method to analyse longitudinal in vivo micro-CT data. Bone 34, 163–169 (2004). · DOI · Paper page
  26. Razi, H. et al. Skeletal maturity leads to a reduction in the strain magnitudes induced within the bone: A murine tibia study. Acta biomat 13, 301–310 (2015). · DOI
  27. Nishiyama, K. K., Campbell, G. M., Klinck, R. J. & Boyd, S. K. Reproducibility of bone micro-architecture measurements in rodents by in vivo micro-computed tomography is maximized with three-dimensional image registration. Bone 46, 155–161 (2010). · DOI
  28. Halloran, B. P. et al. Changes in bone structure and mass with advancing age in the male C57BL/6J mouse. J Bone Miner Res 17, 1044–1050 (2002). · DOI · Paper page
  29. Ahlborg, H. G., Johnell, O., Turner, C. H., Rannevik, G. & Karlsson, M. K. Bone loss and bone size after menopause. N. Engl. J. Med. 349, 327–334 (2003). · DOI · Paper page
  30. Kodama, Y. et al. Exercise and mechanical loading increase periosteal bone formation and whole bone strength in C57BL/6J mice but not in C3H/Hej mice. Calc tissue int 66, 298–306 (2000). · DOI
  31. LaMothe, J. M., Hamilton, N. H. & Zernicke, R. F. Strain rate influences periosteal adaptation in mature bone. Med Eng Phys 27, 277–284 (2005). · DOI
  32. Grimston, S. K., Brodt, M. D., Silva, M. J. & Civitelli, R. Attenuated response to in vivo mechanical loading in mice with conditional osteoblast ablation of the connexin43 gene (Gja1). J Bone Miner Res 23, 879–886 (2008). · DOI
  33. Grimston, S. K., Watkins, M. P., Brodt, M. D., Silva, M. J. & Civitelli, R. Enhanced periosteal and endocortical responses to axial tibial compression loading in conditional connexin43 deficient mice. PloS one 7, e44222 (2012). · DOI
  34. Jilka, R. L. The relevance of mouse models for investigating age-related bone loss in humans. J. Gerontol. Ser. A-Biol. Sci. Med. Sci. 68, 1209–1217 (2013).
  35. Schneider, P. et al. Ultrastructural properties in cortical bone vary greatly in two inbred strains of mice as assessed by synchrotron light based micro- and nano-CT. J Bone Miner Res 22, 1557–1570 (2007). · DOI
  36. Kerschnitzki, M. et al. Architecture of the osteocyte network correlates with bone material quality. J Bone Miner Res 28, 1837–1845 (2013). · DOI · Paper page
  37. Razi, H. et al. Aging Leads to a Dysregulation in Mechanically Driven Bone Formation and Resorption. J Bone Miner Res 30, 1864–1873 (2015). · DOI
  38. Edwards, M. H. et al. Muscle size, strength and physical performance and their associations with bone structure in the Hertfordshire Cohort Study. J Bone Miner Res 28, 2295–2304 (2013). · DOI
  39. Sirola, J. et al. Maintenance of muscle strength may counteract weight-loss-related postmenopausal bone loss–a population-based approach. Osteoporosis int 17, 775–782 (2006). · DOI
  40. Burr, D. B. et al. Bone microdamage and skeletal fragility in osteoporotic and stress fractures. J Bone Miner Res 12, 6–15 (1997). · DOI · Paper page
  41. Schaffler, M. B., Choi, K. & Milgrom, C. Aging and matrix microdamage accumulation in human compact bone. Bone 17, 521–525 (1995). · DOI · Paper page
  42. Augat, P. & Schorlemmer, S. The role of cortical bone and its microstructure in bone strength. Age and ageing 35, Suppl 2, ii27–ii31 (2006). · DOI · Paper page
  43. Bass, S. L. et al. The effect of mechanical loading on the size and shape of bone in pre-, peri- and postpubertal girls: a study in tennis players. J Bone Miner Res 17, 2274–2280 (2002). · DOI · Paper page
  44. Chang, G., Regatte, R. R. & Schweitzer, M. E. Olympic fencers: adaptations in cortical and trabecular bone determined by quantitative computed tomography. Osteoporosis int 20, 779–785 (2009). · DOI
  45. Darling, A. L. et al. Adaptations in tibial cortical thickness and total volumetric bone density in postmenopausal South Asian women with small bone size. Bone 55, 36–43 (2013). · DOI
  46. Robling, A. G., Castillo, A. B. & Turner, C. H. Biomechanical and molecular regulation of bone remodeling. Annu Rev Biomed Eng 8, 455–498 (2006). · DOI · Paper page
  47. Huiskes, R. If bone is the answer, then what is the question? J Anat 197, 145–156 (2000). · DOI · Paper page
  48. Lukas, C. et al. Mineralization kinetics in murine trabecular bone quantified by time-lapsed in vivo micro-computed tomography. Bone 56, 55–60 (2013). · DOI

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Metadata

Authors
Birkhold, A. I., Razi, H., Duda, G. N., Weinkamer, R., Checa, S., & Willie, B. M.
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2016-03-23
Volume
6
Issue
1
ISSN
2045-2322
DOI
10.1038/srep23480
Cited by
91
References
2
Language
en
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Birkhold, A. I., Razi, H., Duda, G. N., Weinkamer, R., Checa, S., & Willie, B. M. (2016). The Periosteal Bone Surface is Less Mechano-Responsive than the Endocortical. Scientific Reports. https://doi.org/10.1038/srep23480

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