Skip to main content

Advertisement

Log in

Bone Quality and Quantity are Mediated by Mechanical Stimuli

  • Bone quality
  • Published:
Clinical Reviews in Bone and Mineral Metabolism Aims and scope Submit manuscript

Abstract

Prevention of fracture through improved bone mechanical strength is of great importance given the large number of bone disease-related fractures each year, the decreased quality of life associated with fractures, and the large anticipated increase in fracture incidence over the upcoming years due to the aging population. Exercise and other forms of mechanical stimulation have been shown to increase bone mass, suggesting improved strength. However, while bone mass is a good indicator of strength, other components (such as bone quality) also contribute to bone mechanical integrity. While increased bone mass has been explored considerably using both exercise and targeted loading models, the role of mechanical stimulation in altering bone quality has been explored to a lesser degree. Understanding how to improve both the quantity and quality of bone is critical to increasing fracture resistance. Herein, we discuss quantity and quality-based improvements that have been observed using both exercise and targeted loading models of bone adaptation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Wolff J. Ueber die innere Architectur der Knochen und ihre Bedeutung für die Frage vom Knochenwachsthum. Arch Pathol Anat Physiol Klin Med. 1870;50(3):389–450.

    Article  Google Scholar 

  2. Koch J. The laws of bone architecture. Am J Anat. 1917;21:177.

    Article  Google Scholar 

  3. Meyer G. Die architektur der spongiosa, archief fur den anatomischen und physiologischen. Wiss Med. 1867;27(4):1389–94.

    Google Scholar 

  4. Frost H. The mechanostat: a proposed pathogenetic mechanism of osteoporoses and the bone mass effects of mechanical and nonmechanical agents. Bone Miner. 1987;2:2.

    Google Scholar 

  5. Rubin CT, Lanyon LE. Osteoregulatory nature of mechanical stimuli: function as a determinant for adaptive remodeling in bone. J Orthop Res. 1987;5(2):300–10.

    Article  CAS  PubMed  Google Scholar 

  6. Krahl H, Michaelis U, Pieper H-G, Quack G, Montag M. Stimulation of bone growth through sports a radiologic investigation of the upper extremities in professional tennis players. Am J Sports Med. 1994;22(6):751–7.

    Article  CAS  PubMed  Google Scholar 

  7. Kelley GA, Kelley KS. Exercise and bone mineral density at the femoral neck in postmenopausal women: a meta-analysis of controlled clinical trials with individual patient data. Am J Obstet Gynecol. 2006;194(3):760–7.

    Article  PubMed  Google Scholar 

  8. Huddleston AL, Rockwell D, Kulund DN, Harrison RB. Bone mass in lifetime tennis athletes. JAMA. 1980;244(10):1107–9.

    Article  CAS  PubMed  Google Scholar 

  9. Warden SJ, Mantila Roosa SM, Kersh ME, Hurd AL, Fleisig GS, Pandy MG, et al. Physical activity when young provides lifelong benefits to cortical bone size and strength in men. Proc Natl Acad Sci. 2014;111(14):5337–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Dalen N, Olsson KE. Bone mineral content and physical activity. Acta Orthop Scand. 1974;45(2):170–4.

    Article  CAS  PubMed  Google Scholar 

  11. Wolman RL, Faulmann L, Clark P, Hesp R, Harries MG. Different training patterns and bone mineral density of the femoral shaft in elite, female athletes. Ann Rheum Dis. 1991;50(7):487–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Brewer V, Meyer BM, Keele MS, Upton SJ, Hagan RD. Role of exercise in prevention of involutional bone loss. Med Sci Sports Exerc. 1983;15(6):445–9.

    Article  CAS  PubMed  Google Scholar 

  13. Fuchs RK, Bauer JJ, Snow CM. Jumping improves hip and lumbar spine bone mass in prepubescent children: a randomized controlled trial. J Bone Miner Res. 2001;16(1):148–56.

    Article  CAS  PubMed  Google Scholar 

  14. Kirchner EM, Lewis RD, O’Connor PJ. Effect of past gymnastics participation on adult bone mass. J Appl Physiol. 1996;80(1):226–32.

    Article  CAS  PubMed  Google Scholar 

  15. Snow CM, Williams DP, LaRiviere J, Fuchs RK, Robinson TL. Bone gains and losses follow seasonal training and detraining in gymnasts. Calcif Tissue Int. 2001;69(1):7–12.

    Article  CAS  PubMed  Google Scholar 

  16. Colletti LA, Edwards J, Gordon L, Shary J, Bell NH. The effects of muscle-building exercise on bone mineral density of the radius, spine, and hip in young men. Calcif Tissue Int. 1989;45(1):12–4.

    Article  CAS  PubMed  Google Scholar 

  17. Jacobson PC, Beaver W, Grubb SA, Taft TN, Talmage RV. Bone density in women: college athletes and older athletic women. J Orthop Res. 1984;2(4):328–32.

    Article  CAS  PubMed  Google Scholar 

  18. Orwoll ES, Ferar J, Oviatt SK, McClung MR, Huntington K. The relationship of swimming exercise to bone mass in men and women. Arch Intern Med. 1989;149(10):2197–200.

    Article  CAS  PubMed  Google Scholar 

  19. Courteix D, Lespessailles E, Peres SL, Obert P, Germain P, Benhamou CL. Effect of physical training on bone mineral density in prepubertal girls: a comparative study between impact-loading and non-impact-loading sports. Osteoporos Int. 1998;8(2):152–8.

    Article  CAS  PubMed  Google Scholar 

  20. Duncan CS, Blimkie CJ, Cowell CT, Burke ST, Briody JN, Howman-Giles R. Bone mineral density in adolescent female athletes: relationship to exercise type and muscle strength. Med Sci Sports Exerc. 2002;34(2):286–94.

    Article  PubMed  Google Scholar 

  21. Kannus P, Haapasalo H, Sankelo M, Sievanen H, Pasanen M, Heinonen A, et al. Effect of starting age of physical activity on bone mass in the dominant arm of tennis and squash players. Ann Intern Med. 1995;123(1):27–31.

    Article  CAS  PubMed  Google Scholar 

  22. Currey JD. Bones: structure and mechanics. Princeton: Princeton University Press; 2002.

    Google Scholar 

  23. Grimm D, Grosse J, Wehland M, Mann V, Reseland JE, Sundaresan A, et al. The impact of microgravity on bone in humans. Bone. 2016;87:44–56.

    Article  PubMed  Google Scholar 

  24. Orwoll ES, Adler RA, Amin S, Binkley N, Lewiecki EM, Petak SM, et al. Skeletal health in long-duration astronauts: nature, assessment, and management recommendations from the NASA bone summit. J Bone Miner Res. 2013;28(6):1243–55.

    Article  PubMed  Google Scholar 

  25. Sibonga JD, Cavanagh PR, Lang TF, LeBlanc AD, Schneider VS, Shackelford LC, et al. Adaptation of the skeletal system during long-duration spaceflight. Clin Rev Bone Miner Metab. 2007;5(4):249–61.

    Article  Google Scholar 

  26. Smith SM, Zwart SR, Heer M, Hudson EK, Shackelford L, Morgan JL. Men and women in space: bone loss and kidney stone risk after long-duration spaceflight. J Bone Miner Res. 2014;29(7):1639–45.

    Article  PubMed  Google Scholar 

  27. LeBlanc AD, Spector ER, Evans HJ, Sibonga JD. Skeletal responses to space flight and the bed rest analog: a review. J Musculoskelet Neuronal Interact. 2007;7(1):33–47.

    CAS  PubMed  Google Scholar 

  28. LeBlanc A, Schneider V, Shackelford L, West S, Oganov V, Bakulin A, et al. Bone mineral and lean tissue loss after long duration space flight. J Musculoskelet Neuronal Interact. 2000;1(2):157–60.

    CAS  PubMed  Google Scholar 

  29. Lang T, LeBlanc A, Evans H, Lu Y, Genant H, Yu A. Cortical and trabecular bone mineral loss from the spine and hip in long-duration spaceflight. J Bone Miner Res. 2004;19(6):1006–12.

    Article  PubMed  Google Scholar 

  30. Pavy-Le Traon A, Heer M, Narici MV, Rittweger J, Vernikos J. From space to Earth: advances in human physiology from 20 years of bed rest studies (1986–2006). Eur J Appl Physiol. 2007;101(2):143–94.

    Article  CAS  PubMed  Google Scholar 

  31. Hargens AR, Vico L. Long-duration bed rest as an analog to microgravity. J Appl Physiol. 2016;120(8):891–903.

    Article  PubMed  Google Scholar 

  32. Lanyon L, Skerry T. Perspective: postmenopausal osteoporosis as a failure of bone’s adaptation to functional loading: a hypothesis*. J Bone Miner Res. 2001;16(11):1937–47.

    Article  CAS  PubMed  Google Scholar 

  33. Bone health and osteoporosis: a report of the Surgeon General. Reports of the Surgeon General. Rockville, MD 2004.

  34. Wallace JM, Rajachar RM, Allen MR, Bloomfield SA, Robey PG, Young MF, et al. Exercise-induced changes in the cortical bone of growing mice are bone and gender specific. Bone. 2007;40(4):1120–7.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Iwamoto J, Yeh JK, Aloia JF. Differential effect of treadmill exercise on three cancellous bone sites in the young growing rat. Bone. 1999;24(3):163–9.

    Article  CAS  PubMed  Google Scholar 

  36. 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. 1997;12(9):1480–5.

    Article  CAS  PubMed  Google Scholar 

  37. Huang TH, Lin SC, Chang FL, Hsieh SS, Liu SH, Yang RS. Effects of different exercise modes on mineralization, structure, and biomechanical properties of growing bone. J Appl Physiol. 2003;95(1):300–7.

    Article  CAS  PubMed  Google Scholar 

  38. Hart KJ, Shaw JM, Vajda E, Hegsted M, Miller SC. Swim-trained rats have greater bone mass, density, strength, and dynamics. J Appl Physiol. 2001;91(4):1663–8.

    CAS  PubMed  Google Scholar 

  39. Notomi T, Okimoto N, Okazaki Y, Tanaka Y, Nakamura T, Suzuki M. Effects of tower climbing exercise on bone mass, strength, and turnover in growing rats. J Bone Miner Res. 2001;16(1):166–74.

    Article  CAS  PubMed  Google Scholar 

  40. Mori T, Okimoto N, Sakai A, Okazaki Y, Nakura N, Notomi T, et al. Climbing exercise increases bone mass and trabecular bone turnover through transient regulation of marrow osteogenic and osteoclastogenic potentials in mice. J Bone Miner Res. 2003;18(11):2002–9.

    Article  PubMed  Google Scholar 

  41. Rubin CT, Lanyon L. Regulation of bone formation by applied dynamic loads. J Bone Joint Surg. 1984;66(3):397–402.

    CAS  PubMed  Google Scholar 

  42. Turner CH, Akhter MP, Raab DM, Kimmel DB, Recker RR. A noninvasive, in vivo model for studying strain adaptive bone modeling. Bone. 1991;12(2):73–9.

    Article  CAS  PubMed  Google Scholar 

  43. Gross TS, Srinivasan S, Liu CC, Clemens TL, Bain SD. Noninvasive loading of the murine tibia: an in vivo model for the study of mechanotransduction. J Bone Miner Res. 2002;17(3):493–501.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Torrance AG, Mosley JR, Suswillo RF, Lanyon LE. Noninvasive loading of the rat ulna in vivo induces a strain-related modeling response uncomplicated by trauma or periostal pressure. Calcif Tissue Int. 1994;54(3):241–7.

    Article  CAS  PubMed  Google Scholar 

  45. Lee KC, Maxwell A, Lanyon LE. Validation of a technique for studying functional adaptation of the mouse ulna in response to mechanical loading. Bone. 2002;31(3):407–12.

    Article  CAS  PubMed  Google Scholar 

  46. De Souza RL, Matsuura M, Eckstein F, Rawlinson SCF, Lanyon LE, Pitsillides AA. Non-invasive axial loading of mouse tibiae increases cortical bone formation and modifies trabecular organization: a new model to study cortical and cancellous compartments in a single loaded element. Bone. 2005;37(6):810–8.

    Article  PubMed  Google Scholar 

  47. Sugiyama T, Price JS, Lanyon LE. Functional adaptation to mechanical loading in both cortical and cancellous bone is controlled locally and is confined to the loaded bones. Bone. 2010;46(2):314–21.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Berman AG, Clauser CA, Wunderlin C, Hammond MA, Wallace JM. Structural and mechanical improvements to bone are strain dependent with axial compression of the tibia in female C57BL/6 mice. PLoS ONE. 2015;10(6):e0130504.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Sample SJ, Collins RJ, Wilson AP, Racette MA, Behan M, Markel MD, et al. Systemic effects of ulna loading in male rats during functional adaptation. J Bone Miner Res. 2010;25(9):2016–28.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Burr DB, Allen MR. Basic and applied bone biology. Amsterdam: Elsevier/Academic Press; 2013.

    Google Scholar 

  51. Turner CH, Forwood MR, Rho JY, Yoshikawa T. Mechanical loading thresholds for lamellar and woven bone formation. J Bone Miner Res. 1994;9(1):87–97.

    Article  CAS  PubMed  Google Scholar 

  52. Turner CH, Owan I, Takano Y. Mechanotransduction in bone: role of strain rate. Am J Physiol Endocrinol Metab. 1995;269(3):E438–42.

    CAS  Google Scholar 

  53. Hsieh Y-F, Robling AG, Ambrosius WT, Burr DB, Turner CH. Mechanical loading of diaphyseal bone in vivo: the strain threshold for an osteogenic response varies with location. J Bone Miner Res. 2001;16(12):2291–7.

    Article  CAS  PubMed  Google Scholar 

  54. Rubin CT, Lanyon LE. Regulation of bone mass by mechanical strain magnitude. Calcif Tissue Int. 1985;37(4):411–7.

    Article  CAS  PubMed  Google Scholar 

  55. Sugiyama T, Meakin LB, Browne WJ, Galea GL, Price JS, Lanyon LE. Bones’ adaptive response to mechanical loading is essentially linear between the low strains associated with disuse and the high strains associated with the lamellar/woven bone transition. J Bone Miner Res. 2012;27(8):1784–93.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Hsieh Y-F, Turner CH. Effects of loading frequency on mechanically induced bone formation. J Bone Miner Res. 2001;16(5):918–24.

    Article  CAS  PubMed  Google Scholar 

  57. Mosley JR, Lanyon LE. Strain rate as a controlling influence on adaptive modeling in response to dynamic loading of the ulna in growing male rats. Bone. 1998;23(4):313–8.

    Article  CAS  PubMed  Google Scholar 

  58. Robling AG, Hinant FM, Burr DB, Turner CH. Improved bone structure and strength after long-term mechanical loading is greatest if loading is separated into short bouts. J Bone Miner Res. 2002;17(8):1545–54.

    Article  PubMed  Google Scholar 

  59. Srinivasan S, Weimer DA, Agans SC, Bain SD, Gross TS. Low-magnitude mechanical loading becomes osteogenic when rest is inserted between each load cycle. J Bone Miner Res. 2002;17(9):1613–20.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Robling AG, Burr DB, Turner CH. Recovery periods restore mechanosensitivity to dynamically loaded bone. J Exp Biol. 2001;204(19):3389–99.

    CAS  PubMed  Google Scholar 

  61. Batra NN, Li YJ, Yellowley CE, You L, Malone AM, Kim CH, et al. Effects of short-term recovery periods on fluid-induced signaling in osteoblastic cells. J Biomech. 2005;38(9):1909–17.

    Article  PubMed  Google Scholar 

  62. Robling AG, Burr DB, Turner CH. Recovery periods restore mechanosensitivity to dynamically loaded bone. J Exp Biol. 2001;204(Pt 19):3389–99.

    CAS  PubMed  Google Scholar 

  63. Lynch ME, Main RP, Xu Q, Walsh DJ, Schaffler MB, Wright TM, et al. Cancellous bone adaptation to tibial compression is not sex dependent in growing mice. J Appl Physiol. 2010;109(3):685–91.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Fritton JC, Myers ER, Wright TM, van der Meulen MCH. Loading induces site-specific increases in mineral content assessed by microcomputed tomography of the mouse tibia. Bone. 2005;36(6):1030–8.

    Article  CAS  PubMed  Google Scholar 

  65. Yang H, Butz KD, Duffy D, Niebur GL, Nauman EA, Main RP. Characterization of cancellous and cortical bone strain in the in vivo mouse tibial loading model using microCT-based finite element analysis. Bone. 2014;66:131–9.

    Article  PubMed  Google Scholar 

  66. Patel TK, Brodt MD, Silva MJ. Experimental and finite element analysis of strains induced by axial tibial compression in young-adult and old female C57Bl/6 mice. J Biomech. 2014;47(2):451–7.

    Article  PubMed  Google Scholar 

  67. Torcasio A, Zhang X, Duyck J, van Lenthe GH. 3D characterization of bone strains in the rat tibia loading model. Biomech Model Mechanobiol. 2012;11(3):403–10.

    Article  PubMed  Google Scholar 

  68. Lu Y, Thiagarajan G, Nicolella DP, Johnson ML. Load/strain distribution between ulna and radius in the mouse forearm compression loading model. Med Eng Phys. 2012;34(3):350–6.

    Article  PubMed  Google Scholar 

  69. Akhter MP, Raab DM, Turner CH, Kimmel DB, Recker RR. Characterization of in vivo strain in the rat tibia during external application of a four-point bending load. J Biomech. 1992;25(10):1241–6.

    Article  CAS  PubMed  Google Scholar 

  70. Dodge T, Wanis M, Ayoub R, Zhao L, Watts NB, Bhattacharya A, et al. Mechanical loading, damping, and load-driven bone formation in mouse tibiae. Bone. 2012;51(4):810–8.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Stadelmann VA, Hocké J, Verhelle J, Forster V, Merlini F, Terrier A, et al. 3D strain map of axially loaded mouse tibia: a numerical analysis validated by experimental measurements. Comput Methods Biomech Biomed Eng. 2009;12(1):95–100.

    Article  Google Scholar 

  72. Moustafa A, Sugiyama T, Prasad J, Zaman G, Gross T, Lanyon L, et al. Mechanical loading-related changes in osteocyte sclerostin expression in mice are more closely associated with the subsequent osteogenic response than the peak strains engendered. Osteoporos Int. 2012;23(4):1225–34.

    Article  CAS  PubMed  Google Scholar 

  73. Sztefek P, Vanleene M, Olsson R, Collinson R, Pitsillides AA, Shefelbine S. Using digital image correlation to determine bone surface strains during loading and after adaptation of the mouse tibia. J Biomech. 2010;43(4):599–605.

    Article  PubMed  Google Scholar 

  74. Akhter PM, Cullen MD, Pedersen AE, Kimmel BD, Recker RR. Bone response to in vivo mechanical loading in two breeds of mice. Calcif Tissue Int. 1998;63(5):442–9.

    Article  CAS  PubMed  Google Scholar 

  75. Robling AG, Turner CH. Mechanotransduction in bone: genetic effects on mechanosensitivity in mice. Bone. 2002;31(5):562–9.

    Article  CAS  PubMed  Google Scholar 

  76. Saxon LK, Jackson BF, Sugiyama T, Lanyon LE, Price JS. Analysis of multiple bone responses to graded strains above functional levels, and to disuse, in mice in vivo show that the human Lrp5 G171 V High Bone Mass mutation increases the osteogenic response to loading but that lack of Lrp5 activity reduces it. Bone. 2011;49(2):184–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Morse A, McDonald MM, Kelly NH, Melville KM, Schindeler A, Kramer I, et al. Mechanical load increases in bone formation via a sclerostin-independent pathway. J Bone Miner Res. 2014;29(11):2456–67.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Lanyon L. Using functional loading to influence bone mass and architecture: objectives, mechanisms, and relationship with estrogen of the mechanically adaptive process in bone. Bone. 1996;18(1):S37–43.

    Article  Google Scholar 

  79. Galea GL, Meakin LB, Sugiyama T, Zebda N, Sunters A, Taipaleenmaki H, et al. Estrogen receptor α mediates proliferation of osteoblastic cells stimulated by estrogen and mechanical strain, but their acute down-regulation of the Wnt antagonist Sost is mediated by estrogen receptor β. J Biol Chem. 2013;288(13):9035–48.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Castillo AB, Triplett JW, Pavalko FM, Turner CH. Estrogen receptor-β regulates mechanical signaling in primary osteoblasts. Am J Physiol Endocrinol Metab. 2014;306(8):E937–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Klein-Nulend J, van Oers RF, Bakker AD, Bacabac RG. Bone cell mechanosensitivity, estrogen deficiency, and osteoporosis. J Biomech. 2015;48(5):855–65.

    Article  PubMed  Google Scholar 

  82. Galea GL, Price JS, Lanyon LE. Estrogen receptors’ roles in the control of mechanically adaptive bone (re)modeling. BoneKEy reports. 2013;2(413):1–7.

    Google Scholar 

  83. Willie BM, Birkhold AI, Razi H, Thiele T, Aido M, Kruck B, 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. 2013;55(2):335–46.

    Article  PubMed  Google Scholar 

  84. Main RP, Lynch ME, van der Meulen MCH. Load-induced changes in bone stiffness and cancellous and cortical bone mass following tibial compression diminish with age in female mice. J Exp Biol. 2014;217(10):1775–83.

    Article  PubMed  PubMed Central  Google Scholar 

  85. Lynch ME, Main RP, Xu Q, Schmicker TL, Schaffler MB, Wright TM, et al. Tibial compression is anabolic in the adult mouse skeleton despite reduced responsiveness with aging. Bone. 2011;49(3):439–46.

    Article  PubMed  PubMed Central  Google Scholar 

  86. Fritton JC, Myers ER, Wright TM, van der Meulen MCH. Bone mass is preserved and cancellous architecture altered due to cyclic loading of the mouse tibia after orchidectomy. J Bone Miner Res. 2008;23(5):663–71.

    Article  PubMed  PubMed Central  Google Scholar 

  87. Sugiyama T, Saxon LK, Zaman G, Moustafa A, Sunters A, Price JS, et al. Mechanical loading enhances the anabolic effects of intermittent parathyroid hormone (1–34) on trabecular and cortical bone in mice. Bone. 2008;43(2):238–48.

    Article  CAS  PubMed  Google Scholar 

  88. Sugiyama T, Galea GL, Lanyon LE, Price JS. Mechanical loading-related bone gain is enhanced by tamoxifen but unaffected by fulvestrant in female mice. Endocrinology. 2010;151(12):5582–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Kanis JA. Diagnosis of osteoporosis and assessment of fracture risk. Lancet. 2002;359(9321):1929–36.

    Article  PubMed  Google Scholar 

  90. Kanis JA, Borgstrom F, De Laet C, Johansson H, Johnell O, Jonsson B, et al. Assessment of fracture risk. Osteoporos Int. 2005;16(6):581–9.

    Article  PubMed  Google Scholar 

  91. Van der Meulen M, Jepsen K, Mikić B. Understanding bone strength: size isn’t everything. Bone. 2001;29(2):101–4.

    Article  PubMed  Google Scholar 

  92. Donnelly E. Methods for Assessing bone quality: a review. Clin Orthop Relat Res. 2011;469(8):2128–38.

    Article  PubMed  Google Scholar 

  93. Judex S, Boyd S, Qin Y-X, Miller L, Müller R, Rubin C. Combining high-resolution micro-computed tomography with material composition to define the quality of bone tissue. Curr Osteoporos Rep. 2003;1(1):11–9.

    Article  PubMed  Google Scholar 

  94. Seeman E, Delmas PD. Bone quality—the material and structural basis of bone strength and fragility. N Engl J Med. 2006;354(21):2250–61.

    Article  CAS  PubMed  Google Scholar 

  95. Launey ME, Buehler MJ, Ritchie RO. On the mechanistic origins of toughness in bone. Annu Rev Mater Res. 2010;40(1):25–53.

    Article  CAS  Google Scholar 

  96. Saito M, Marumo K. Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int. 2010;21(2):195–214.

    Article  CAS  PubMed  Google Scholar 

  97. Taaffe DR, Snow-Harter C, Connolly DA, Robinson TL, Brown MD, Marcus R. Differential effects of swimming versus weight-bearing activity on bone mineral status of eumenorrheic athletes. J Bone Miner Res. 1995;10(4):586–93.

    Article  CAS  PubMed  Google Scholar 

  98. Morel J, Combe B, Francisco J, Bernard J. Bone mineral density of 704 amateur sportsmen involved in different physical activities. Osteoporos Int. 2001;12(2):152–7.

    Article  CAS  PubMed  Google Scholar 

  99. Bourrin S, Ghaemmaghami F, Vico L, Chappard D, Gharib C, Alexandre C. Effect of a five-week swimming program on rat bone: a histomorphometric study. Calcif Tissue Int. 1992;51(2):137–42.

    Article  CAS  PubMed  Google Scholar 

  100. Huang T-H, Hsieh SS, Liu S-H, Chang F-L, Lin S-C, Yang R-S. Swimming training increases the post-yield energy of bone in young male rats. Calcif Tissue Int. 2010;86(2):142–53.

    Article  CAS  PubMed  Google Scholar 

  101. Isaksson H, Tolvanen V, Finnilä MA, Iivarinen J, Tuukkanen J, Seppänen K, et al. Physical exercise improves properties of bone and its collagen network in growing and maturing mice. Calcif Tissue Int. 2009;85(3):247–56.

    Article  CAS  PubMed  Google Scholar 

  102. Wallace JM, Ron MS, Kohn DH. Short-term exercise in mice increases tibial post-yield mechanical properties while two weeks of latency following exercise increases tissue-level strength. Calcif Tissue Int. 2009;84(4):297–304.

    Article  CAS  PubMed  Google Scholar 

  103. Warden SJ, Fuchs RK, Castillo AB, Nelson IR, Turner CH. Exercise when young provides lifelong benefits to bone structure and strength. J Bone Miner Res. 2007;22(2):251–9.

    Article  PubMed  Google Scholar 

  104. Kohn DH, Sahar ND, Wallace JM, Golcuk K, Morris MD. Exercise alters mineral and matrix composition in the absence of adding new bone. Cells Tissues Organs. 2009;189(1–4):33–7.

    PubMed  Google Scholar 

  105. Mosekilde L, Danielsen C, Søgaard C, Thorling E. The effect of long-term exercise on vertebral and femoral bone mass, dimensions, and strength—assessed in a rat model. Bone. 1994;15(3):293–301.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was funded by: K25-AR067221-01A1.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joseph M. Wallace.

Ethics declarations

Conflict of interest

Alycia G. Berman and Joseph M. Wallace have no conflicts of interest to disclose.

Human and Animals Rights

This article does not contain any studies with human or animal subjects performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Berman, A.G., Wallace, J.M. Bone Quality and Quantity are Mediated by Mechanical Stimuli. Clinic Rev Bone Miner Metab 14, 218–226 (2016). https://doi.org/10.1007/s12018-016-9221-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12018-016-9221-5

Keywords

Navigation