Skip to main content

Advertisement

SpringerLink
Log in

Whole Bone Mechanics and Bone Quality

  • Symposium: Bone Quality: From Bench to Bedside
  • Published:
Clinical Orthopaedics and Related Research®

Abstract

Background

The skeleton plays a critical structural role in bearing functional loads, and failure to do so results in fracture. As we evaluate new therapeutics and consider treatments to prevent skeletal fractures, understanding the basic mechanics underlying whole bone testing and the key principles and characteristics contributing to the structural strength of a bone is critical.

Questions/purposes

We therefore asked: (1) How are whole bone mechanical tests performed and what are the key outcomes measured? (2) How do the intrinsic characteristics of bone tissue contribute to the mechanical properties of a whole bone? (3) What are the effects of extrinsic characteristics on whole bone mechanical behavior? (4) Do environmental factors affect whole bone mechanical properties?

Methods

We conducted a PubMed search using specific search terms and limiting our included articles to those related to in vitro testing of whole bones. Basic solid mechanics concepts are summarized in the context of whole bone testing and the determinants of whole bone behavior.

Results

Whole bone mechanical tests measure structural stiffness and strength from load-deformation data. Whole bone stiffness and strength are a function of total bone mass and the tissue geometric distribution and material properties. Age, sex, genetics, diet, and activity contribute to bone structural performance and affect the incidence of skeletal fractures.

Conclusions

Understanding and preventing skeletal fractures is clinically important. Laboratory tests of whole bone strength are currently the only measures for in vivo fracture prediction. In the future, combined imaging and engineering models may be able to predict whole bone strength noninvasively.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1A–B
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Aaron JE, Makins NB, Sagreiya K. The microanatomy of trabecular bone loss in normal aging men and women. Clin Orthop Relat Res. 1987;215:260-271.

    PubMed  Google Scholar 

  2. Aerssens J, van Audekercke R, Talalaj M, van Vlasselaer P, Bramm E, Geusens P, Dequeker J. Effect of 1 alpha-vitamin D3 on bone strength and composition in growing rats with and without corticosteroid treatment. Calcif Tissue Int. 1994;55:443–450.

    PubMed  CAS  Google Scholar 

  3. Akkus O, Adar F, Schaffler MB. Age-related changes in physicochemical properties of mineral crystals are related to impaired mechanical function of cortical bone. Bone. 2004;34:443–453.

    PubMed  CAS  Google Scholar 

  4. Battaglia TC, Tsou AC, Taylor EA, Mikić B. Ash content modulation of torsionally derived effective material properties in cortical mouse bone. J Biomech Eng. 2003;125:615–619.

    PubMed  Google Scholar 

  5. Beamer WG, Donahue LR, Rosen CJ, Baylink DJ. Genetic variability in adult bone density among inbred strains of mice. Bone. 1996;18:397–403.

    PubMed  CAS  Google Scholar 

  6. Benes H, Weinstein RS, Zheng W, Thaden JJ, Jilka RL, Manolagas SC, Shmookler Reis RJ. Chromosomal mapping of osteopenia-associated quantitative trait loci using closely related mouse strains. J Bone Miner Res. 2000;15:626–633.

    PubMed  CAS  Google Scholar 

  7. Bergmann G, Graichen F, Rohlmann A. Hip joint loading during walking and running, measured in two patients. J Biomech. 1993;26:969–990.

    PubMed  CAS  Google Scholar 

  8. Biewener AA. Musculoskeletal design in relation to body size. J Biomech. 1991;24(Suppl 1):19–29.

    PubMed  Google Scholar 

  9. Bischoff-Ferrari HA, Dawson-Hughes B, Willett WC, Staehelin HB, Bazemore MG, Zee RY, Wong JB. Effect of vitamin D on falls: a meta-analysis. JAMA. 2004;291:1999–2006.

    PubMed  CAS  Google Scholar 

  10. Bischoff-Ferrari HA, Dietrich T, Orav EJ, Dawson-Hughes B. Positive association between 25-hydroxy vitamin D levels and bone mineral density: a population-based study of younger and older adults. Am J Med. 2004;116:634–639.

    PubMed  CAS  Google Scholar 

  11. Bischoff-Ferrari HA, Willett WC, Wong JB, Giovannucci E, Dietrich T, Dawson-Hughes B. Fracture prevention with vitamin D supplementation: a meta-analysis of randomized controlled trials. JAMA. 2005;293:2257–22564.

    PubMed  CAS  Google Scholar 

  12. Blank RD. Breaking down bone strength: a perspective on the future of skeletal genetics. J Bone Miner Res. 2001;16:1207–1211.

    PubMed  CAS  Google Scholar 

  13. Bonadio J, Jepsen KJ, Mansoura MK, Jaenisch R, Kuhn JL, Goldstein SA. A murine skeletal adaptation that significantly increases cortical bone mechanical properties: implications for human skeletal fragility. J Clin Invest. 1993;92:1697–1705.

    PubMed  CAS  Google Scholar 

  14. Boskey AL, Wright TM, Blank RD. Collagen and bone strength. J Bone Miner Res. 1999;14:330–335.

    PubMed  CAS  Google Scholar 

  15. Boutroy S, van Rietbergen B, Sornay-Rendu E, Munoz F, Bouxsein ML, Delmas PD. Finite element analysis based on in vivo HR-pQCT images of the distal radius is associated with wrist fracture in postmenopausal women. J Bone Miner Res. 2008;23:392–399.

    PubMed  Google Scholar 

  16. Bouxsein ML, Melton LJ 3rd, Riggs BL, Muller J, Atkinson EJ, Oberg AL, Robb RA, Camp JJ, Rouleau PA, McCollough CH, Khosla S. Age- and sex-specific differences in the factor of risk for vertebral fracture: a population-based study using QCT. J Bone Miner Res. 2006;21:1475–1482.

    PubMed  Google Scholar 

  17. Bouxsein ML, Rosen CJ, Turner CH, Ackert CL, Shultz KL, Donahue LR, Churchill G, Adamo ML, Powell DR, Turner RT, Müller R, Beamer WG. Generation of a new congenic mouse strain to test the relationships among serum insulin-like growth factor I, bone mineral density, and skeletal morphology in vivo. J Bone Miner Res. 2002;17:570–579.

    PubMed  CAS  Google Scholar 

  18. Burghardt AJ, Link TM, Majumdar S. High-resolution Computed Tomography for Clinical Imaging of Bone Microarchitecture. Clin Orthop Relat Res. 2010. DOI 10.1007/s11999-010-1766-x.

  19. Burr DB. The contribution of the organic matrix to bone’s material properties. Bone. 2002;31:8–11.

    PubMed  CAS  Google Scholar 

  20. Burr DB, Martin RB, Schaffler MB, Radin EL. Bone remodeling in response to in vivo fatigue microdamage. J Biomech. 1985;18:189–200.

    PubMed  CAS  Google Scholar 

  21. Burstein AH, Frankel VH. A standard test for laboratory animal bone. J Biomech. 1971;4:155–158.

    PubMed  CAS  Google Scholar 

  22. Burstein AH, Zika JM, Heiple K, Klein L. Contribution of collagen and mineral to the elastic-plastic properties of bone. J Bone Joint Surg Am. 1975;57:956–961.

    PubMed  CAS  Google Scholar 

  23. Callaghan JP, Patla AE, McGill SM. Low back three-dimensional joint forces, kinematics, and kinetics during walking. Clin Biomech (Bristol, Avon). 1999; 14:203–216.

    PubMed  CAS  Google Scholar 

  24. Carter DR, Hayes WC. The compressive behavior of bone as a two-phase porous structure. J Bone Joint Surg Am. 1977;59:954–962.

    PubMed  CAS  Google Scholar 

  25. Chapuy MC, Arlot ME, Duboeuf F, Brun J, Crouzet B, Arnaud S, Delmas PD, Meunier PJ. Vitamin D3 and calcium to prevent hip fractures in the elderly women. N Engl J Med. 1992;327:1637–1642.

    PubMed  CAS  Google Scholar 

  26. Christen D, Webster DJ, Müller R. Multiscale modelling and nonlinear finite element analysis as clinical tools for the assessment of fracture risk. Philos Transact A Math Phys Eng Sci. 2010;368:2653–2668.

    PubMed  Google Scholar 

  27. Ciarelli TE, Fyhrie DP, Schaffler MB, Goldstein SA. Variations in three-dimensional cancellous bone architecture of the proximal femur in female hip fractures and in controls. J Bone Miner Res. 2000;15:32–40.

    PubMed  CAS  Google Scholar 

  28. Courtney AC, Wachtel EF, Myers ER, Hayes WC. Effects of loading rate on strength of the proximal femur. Calcif Tissue Int. 1994;55:53–58.

    PubMed  CAS  Google Scholar 

  29. Crawford RP, Cann CE, Keaveny TM. Finite element models predict in vitro vertebral body compressive strength better than quantitative computed tomography. Bone. 2003;33:744–750.

    PubMed  Google Scholar 

  30. Cummings SR, Black DM, Nevitt MC, Browner W, Cauley J, Ensrud K, Genant HK, Palermo L, Scott J, Vogt TM. Bone density at various sites for prediction of hip fractures. The Study of Osteoporotic Fractures Research Group. Lancet. 1993;341:72–75.

    PubMed  CAS  Google Scholar 

  31. Currey JD. The effect of porosity and mineral content on the Young’s modulus of elasticity of compact bone. J Biomech. 1988;21:131–139.

    PubMed  CAS  Google Scholar 

  32. Dawson-Hughes B, Harris SS, Krall EA, Dallal GE. Effect of calcium and vitamin D supplementation on bone density in men and women 65 years of age or older. N Engl J Med. 1997;337:670–676.

    PubMed  CAS  Google Scholar 

  33. Dequeker J, Nijs J, Verstraeten A, Geusens P, Gevers G. Genetic determinants of bone mineral content at the spine and radius: a twin study. Bone. 1987;8:207–209.

    PubMed  CAS  Google Scholar 

  34. Donaldson CL, Hulley SB, Vogel JM, Hattner RS, Bayers JH, McMillan DE. Effect of prolonged bed rest on bone mineral. Metabolism. 1970;19:1071–1084.

    PubMed  CAS  Google Scholar 

  35. Donnelly E. Methods for assessing bone quality: A review. Clin Orthop Relat Res. 2010 November 30 [Epub ahead of print].

  36. Donnelly E, Boskey AL, Baker SP, van der Meulen MC. Effects of tissue age on bone tissue material composition and nanomechanical properties in the rat cortex. J Biomed Mater Res A. 2010;92:1048–1056.

    PubMed  Google Scholar 

  37. Donnelly E, Chen DX, Boskey AL, Baker SP, van der Meulen MC. Contribution of mineral to bone structural behavior and tissue mechanical properties. Calcif Tissue Int. 2010;87:450–460.

    PubMed  CAS  Google Scholar 

  38. Drake TA, Hannani K, Kabo JM, Villa V, Krass K, Lusis AJ. Genetic loci influencing natural variations in femoral bone morphometry in mice. J Orthop Res. 2001;19:511–517.

    PubMed  CAS  Google Scholar 

  39. Duan Y, Beck TJ, Wang XF, Seeman E. Structural and biomechanical basis of sexual dimorphism in femoral neck fragility has its origins in growth and aging. J Bone Miner Res. 2003;18:1766–1774.

    PubMed  Google Scholar 

  40. Eckstein F, Wunderer C, Boehm H, Kuhn V, Priemel M, Link TM, Lochmüller EM. Reproducibility and side differences of mechanical tests for determining the structural strength of the proximal femur. J Bone Miner Res. 2004;19:379–385.

    PubMed  Google Scholar 

  41. Eswaran SK, Gupta A, Keaveny TM. Locations of bone tissue at high risk of initial failure during compressive loading of the human vertebral body. Bone. 2007;41:733–739.

    PubMed  Google Scholar 

  42. Fields AJ, Eswaran SK, Jekir MG, Keaveny TM. Role of trabecular microarchitecture in whole-vertebral body biomechanical behavior. J Bone Miner Res. 2009;24:1523–1530.

    PubMed  Google Scholar 

  43. Fields AJ, Lee GL, Liu XS, Jekir MG, Guo XE, Keaveny TM. Influence of vertical trabeculae on the compressive strength of the human vertebra. J Bone Miner Res. 2010 August 16 [Epub ahead of print].

  44. Flicker L, Faulkner KG, Hopper JL, Green RM, Kaymacki B, Nowson CA, Young D, Wark JD. Determinants of hip axis length in women aged 10–89 years: a twin study. Bone. 1996;18:41–45.

    PubMed  CAS  Google Scholar 

  45. Galante J, Rostoker W, Ray RD. Physical properties of trabecular bone. Calcif Tissue Res. 1970;5:236–246.

    PubMed  CAS  Google Scholar 

  46. Galfsky I, Wolinsky I, Simkin A, Guggenheim K. Effect of repletion with dietary calcium on composition and mechanical properties of bone of calcium-deprived rats. Nutr Metab. 1975;18:99–104.

    PubMed  CAS  Google Scholar 

  47. Gibson LJ. The mechanical behavior of cancellous bone. J Biomech. 1985;18:317–328.

    PubMed  CAS  Google Scholar 

  48. Giddings VL, Beaupré GS, Whalen RT, Carter DR. Calcaneal loading during walking and running. Med Sci Sports Exerc. 2000;32:627–634.

    PubMed  CAS  Google Scholar 

  49. Goldstein SA, Wilson DL, Sonstegard DA, Matthews LS. The mechanical properties of human tibial trabecular bone as a function of metaphyseal location. J Biomech. 1983;16:965–969.

    PubMed  CAS  Google Scholar 

  50. Gourion-Arsiquaud S, Burket JC, Havill LM, DiCarlo E, Doty SB, Mendelsohn R, van der Meulen MC, Boskey AL. Spatial variation in osteonal bone properties relative to tissue and animal age. J Bone Miner Res. 2009;24:1271–1281.

    PubMed  Google Scholar 

  51. Gross TS, McLeod KJ, Rubin CT. Characterizing bone strain distributions in vivo using three triple rosette strain gages. J Biomech. 1992;25:1081–1087.

    PubMed  CAS  Google Scholar 

  52. Grzesik WJ, Frazier CR, Shapiro JR, Sponseller PD, Robey PG, Fedarko NS. Age-related changes in human bone proteoglycan structure: impact of osteogenesis imperfecta. J Biol Chem. 2002;277:43638–43647.

    PubMed  CAS  Google Scholar 

  53. Gueguen R, Jouanny P, Guillemin F, Kuntz C, Pourel J, Siest G. Segregation analysis and variance components analysis of bone mineral density in healthy families. J Bone Miner Res. 1995;10:2017–2022.

    PubMed  CAS  Google Scholar 

  54. Heaney RP. Calcium in the prevention and treatment of osteoporosis. J Intern Med. 1992;231:169–180.

    PubMed  CAS  Google Scholar 

  55. Heaney RP. Calcium, dairy products and osteoporosis. J Am Coll Nutr. 2000;19:83S–99S.

    PubMed  CAS  Google Scholar 

  56. Heaney RP. Dairy and bone health. J Am Coll Nutr. 2009;28(Suppl 1):82S–90S.

    PubMed  CAS  Google Scholar 

  57. Homminga J, van Rietbergen B, Lochmüller EM, Weinans H, Eckstein F, Huiskes R. The osteoporotic vertebral structure is well adapted to the loads of daily life, but not to infrequent ‘error’ loads. Bone. 2004;34:510–516.

    PubMed  CAS  Google Scholar 

  58. Hui SL, Slemenda CW, Johnston CC Jr. Age and bone mass as predictors of fracture in a prospective study. J Clin Invest. 1988;81:1804–1809.

    PubMed  CAS  Google Scholar 

  59. Hui SL, Slemenda CW, Johnston CC Jr. Baseline measurement of bone mass predicts fracture in white women. Ann Intern Med. 1989;111:355–361.

    PubMed  CAS  Google Scholar 

  60. Jepsen KJ, Akkus OJ, Majeska RJ, Nadeau JH. Hierarchical relationship between bone traits and mechanical properties in inbred mice. Mamm Genome. 2003;14:97–104.

    PubMed  Google Scholar 

  61. Jepsen KJ, Goldstein SA, Kuhn JL, Schaffler MB, Bonadio J. Type-I collagen mutation compromises the post-yield behavior of Mov13 long bone. J Orthop Res. 1996;14:493–499.

    PubMed  CAS  Google Scholar 

  62. Johnell O, Kanis JA, Oden A, Johansson H, De Laet C, Delmas P, Eisman JA, Fujiwara S, Kroger H, Mellstrom D, Meunier PJ, Melton LJ 3rd, O’Neill T, Pols H, Reeve J, Silman A, Tenenhouse A. Predictive value of BMD for hip and other fractures. J Bone Miner Res. 2005;20:1185–1194.

    PubMed  Google Scholar 

  63. Jones HH, Priest JD, Hayes WC, Tichenor CC, Nagel DA. Humeral hypertrophy in response to exercise. J Bone Joint Surg Am. 1977;59:204–208.

    PubMed  CAS  Google Scholar 

  64. Jouanny P, Guillemin F, Kuntz C, Jeandel C, Pourel J. Environmental and genetic factors affecting bone mass: similarity of bone density among members of healthy families. Arthritis Rheum. 1995;38:61–67.

    PubMed  CAS  Google Scholar 

  65. Kazakia GJ, Majumdar S. New imaging technologies in the diagnosis of osteoporosis. Rev Endocr Metab Disord. 2006;7:67–74.

    PubMed  Google Scholar 

  66. Keaveny TM, Pinilla TP, Crawford RP, Kopperdahl DL, Lou A. Systematic and random errors in compression testing of trabecular bone. J Orthop Res. 1997;15:101–110.

    PubMed  CAS  Google Scholar 

  67. Keyak JH, Rossi SA, Jones KA, Skinner HB. Prediction of femoral fracture load using automated finite element modeling. J Biomech. 1998;31:125–133.

    PubMed  CAS  Google Scholar 

  68. Kleerekoper M, Villanueva AR, Stanciu J, Rao DS, Parfitt AM. The role of three-dimensional trabecular microstructure in the pathogenesis of vertebral compression fractures. Calcif Tissue Int. 1985;37:594–597.

    PubMed  CAS  Google Scholar 

  69. Klein RF, Carlos AS, Vartanian KA, Chambers VK, Turner EJ, Phillips TJ, Belknap JK, Orwoll ES. Confirmation and fine mapping of chromosomal regions influencing peak bone mass in mice. J Bone Miner Res. 2001;16:1953–1961.

    PubMed  CAS  Google Scholar 

  70. Klein RF, Turner RJ, Skinner LD, Vartanian KA, Serang M, Carlos AS, Shea M, Belknap JK, Orwoll ES. Mapping quantitative trait loci that influence femoral cross-sectional area in mice. J Bone Miner Res. 2002;17:1752–1760.

    PubMed  CAS  Google Scholar 

  71. Koller DL, Liu G, Econs MJ, Hui SL, Morin PA, Joslyn G, Rodriguez LA, Conneally PM, Christian JC, Johnston CC Jr, Foroud T, Peacock M. Genome screen for quantitative trait loci underlying normal variation in femoral structure. J Bone Miner Res. 2001;16:985–991.

    PubMed  CAS  Google Scholar 

  72. Koller DL, Schriefer J, Sun Q, Shultz KL, Donahue LR, Rosen CJ, Foroud T, Beamer WG, Turner CH. Genetic effects for femoral biomechanics, structure, and density in C57BL/6J and C3 h/HeJ inbred mouse strains. J Bone Miner Res. 2003;18:1758–1765.

    PubMed  CAS  Google Scholar 

  73. Kopperdahl DL, Keaveny TM. Yield strain behavior of trabecular bone. J Biomech. 1998;31:601–608.

    PubMed  CAS  Google Scholar 

  74. Kotzar GM, Davy DT, Goldberg VM, Heiple KG, Berilla J, Heiple KG Jr, Brown RH, Burstein AH. Telemeterized in vivo hip joint force data: a report on two patients after total hip surgery. J Orthop Res. 1991;9:621–633.

    PubMed  CAS  Google Scholar 

  75. Lang DH, Sharkey NA, Mack HA, Vogler GP, Vandenbergh DJ, Blizard DA, Stout JT, McClearn GE. Quantitative trait loci analysis of structural and material skeletal phenotypes in C57BL/6J and DBA/2 second-generation and recombinant inbred mice. J Bone Miner Res. 2005;20:88–99.

    PubMed  CAS  Google Scholar 

  76. Lanyon LE, Hampson WG, Goodship AE, Shah JS. Bone deformation recorded in vivo from strain gauges attached to the human tibial shaft. Acta Orthop Scand. 1975;46:256–268.

    PubMed  CAS  Google Scholar 

  77. LeBlanc A, Schneider V, Krebs J, Evans H, Jhingran S, Johnson P. Spinal bone mineral after 5 weeks of bed rest. Calcif Tissue Int. 1987;41:259–261.

    PubMed  CAS  Google Scholar 

  78. Li X, Masinde G, Gu W, Wergedal J, Mohan S, Baylink DJ. Genetic dissection of femur breaking strength in a large population (MRL/MpJ x SJL/J) of F2 mice: single QTL effects, epistasis, and pleiotropy. Genomics. 2002;79:734–740.

    PubMed  CAS  Google Scholar 

  79. Linde F, Gøthgen CB, Hvid I, Pongsoipetch B. Mechanical properties of trabecular bone by a non-destructive compression testing approach. Eng Med. 1988;17:23–29.

    PubMed  CAS  Google Scholar 

  80. Linde F, Hvid I, Pongsoipetch B. Energy absorptive properties of human trabecular bone specimens during axial compression. J Orthop Res. 1989;7:432–439.

    PubMed  CAS  Google Scholar 

  81. Liu XS, Cohen A, Shane E, Stein E, Rogers H, Kokolus SL, Yin PT, McMahon DJ, Lappe JM, Recker RR, Guo XE. Individual trabeculae segmentation (ITS)-based morphological analysis of high-resolution peripheral quantitative computed tomography images detects abnormal trabecular plate and rod microarchitecture in premenopausal women with idiopathic osteoporosis. J Bone Miner Res. 2010;25:1496–1505.

    PubMed  Google Scholar 

  82. Looker AC, Beck TJ, Orwoll ES. Does body size account for gender differences in femur bone density and geometry? J Bone Miner Res. 2001;16:1291–1299.

    PubMed  CAS  Google Scholar 

  83. Marshall D, Johnell O, Wedel H. Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. BMJ (Int Ed). 1996;312:1254–1259.

    CAS  Google Scholar 

  84. McCalden RW, McGeough JA, Court-Brown CM. Age-related changes in the compressive strength of cancellous bone: the relative importance of changes in density and trabecular architecture. J Bone Joint Surg Am. 1997;79:421–427.

    PubMed  CAS  Google Scholar 

  85. McElhaney JH. Dynamic response of bone and muscle tissue. J Appl Physiol. 1966;21:1231–1236.

    PubMed  CAS  Google Scholar 

  86. Melton LJ 3rd, Atkinson EJ, O’Fallon WM, Wahner HW, Riggs BL. Long-term fracture prediction by bone mineral assessed at different skeletal sites. J Bone Miner Res. 1993;8:1227–1233.

    PubMed  Google Scholar 

  87. Mittra E, Rubin C, Qin YX. Interrelationship of trabecular mechanical and microstructural properties in sheep trabecular bone. J Biomech. 2005;38:1229–1237.

    PubMed  Google Scholar 

  88. Morgan EF, Bayraktar HH, Keaveny TM. Trabecular bone modulus-density relationships depend on anatomic site. J Biomech. 2003;36:897–904.

    PubMed  Google Scholar 

  89. Mosekilde L, Mosekilde L. Normal vertebral body size and compressive strength: relations to age and to vertebral and iliac trabecular bone compressive strength. Bone. 1986;7:207–212.

    PubMed  CAS  Google Scholar 

  90. Mosekilde L, Mosekilde L, Danielsen CC. Biomechanical competence of vertebral trabecular bone in relation to ash density and age in normal individuals. Bone. 1987;8:79–85.

    PubMed  CAS  Google Scholar 

  91. Mosekilde L, Viidik A. Correlation between the compressive strength of iliac and vertebral trabecular bone in normal individuals. Bone. 1985;6:291–295.

    PubMed  CAS  Google Scholar 

  92. Naghii MR, Torkaman G, Mofid M. Effects of boron and calcium supplementation on mechanical properties of bone in rats. Biofactors. 2006;28:195–201.

    PubMed  CAS  Google Scholar 

  93. Nieves JW, Barrett-Connor E, Siris ES, Zion M, Barlas S, Chen YT. Calcium and vitamin D intake influence bone mass, but not short-term fracture risk, in Caucasian postmenopausal women from the National Osteoporosis Risk Assessment (NORA) study. Osteoporos Int. 2008;19:673–679.

    PubMed  CAS  Google Scholar 

  94. Nyman JS, Roy A, Shen XM, Acuna RL, Tyler JH, Wang XD. The influence of water removal on the strength and toughness of cortical bone. J Biomech. 2006;39:931–938.

    PubMed  Google Scholar 

  95. Parfitt AM, Mathews CH, Villanueva AR, Kleerekoper M, Frame B, Rao DS. Relationships between surface, volume, and thickness of iliac trabecular bone in aging and in osteoporosis: implications for the microanatomic and cellular mechanisms of bone loss. J Clin Invest. 1983;72:1396–1409.

    PubMed  CAS  Google Scholar 

  96. Paschalis EP, Betts F, DiCarlo E, Mendelsohn R, Boskey AL. FTIR microspectroscopic analysis of human iliac crest biopsies from untreated osteoporotic bone. Calcif Tissue Int. 1997;61:487–492.

    PubMed  CAS  Google Scholar 

  97. Paschalis EP, Shane E, Lyritis G, Skarantavos G, Mendelsohn R, Boskey AL. Bone fragility and collagen cross-links. J Bone Miner Res. 2004;19:2000–2004.

    PubMed  Google Scholar 

  98. Pistoia W, van Rietbergen B, Rüegsegger P. Mechanical consequences of different scenarios for simulated bone atrophy and recovery in the distal radius. Bone. 2003;33:937–945.

    PubMed  CAS  Google Scholar 

  99. Recker RR, Deng HW. Role of genetics in osteoporosis. Endocrine. 2002;17:55–66.

    PubMed  CAS  Google Scholar 

  100. Rice JC, Cowin SC, Bowman JA. On the dependence of the elasticity and strength of cancellous bone on apparent density. J Biomech. 1988;21:155–168.

    PubMed  CAS  Google Scholar 

  101. Rohlmann A, Graichen F, Kayser R, Bender A, Bergmann G. Loads on a telemeterized vertebral body replacement measured in two patients. Spine (Phila Pa 1976). 2008;33:1170–1179.

    Google Scholar 

  102. Roschger P, Paschalis EP, Fratzl P, Klaushofer K. Bone mineralization density distribution in health and disease. Bone. 2008;42:456–466.

    PubMed  CAS  Google Scholar 

  103. Rosen CJ, Beamer WG, Donahue LR. Defining the genetics of osteoporosis: using the mouse to understand man. Osteoporos Int. 2001;12:803–810.

    PubMed  CAS  Google Scholar 

  104. Ross PD, Davis JW, Epstein RS, Wasnich RD. Pre-existing fractures and bone mass predict vertebral fracture incidence in women. Ann Intern Med. 1991;114:919–923.

    PubMed  CAS  Google Scholar 

  105. Ross PD, Davis JW, Vogel JM, Wasnich RD. A critical review of bone mass and the risk of fractures in osteoporosis. Calcif Tissue Int. 1990;46:149–161.

    PubMed  CAS  Google Scholar 

  106. Ruff CB, Hayes WC. Sex differences in age-related remodeling of the femur and tibia. J Orthop Res. 1988;6:886–896.

    PubMed  CAS  Google Scholar 

  107. Ruppel ME, Burr DB, Miller LM. Chemical makeup of microdamaged bone differs from undamaged bone. Bone. 2006;39:318–324.

    PubMed  CAS  Google Scholar 

  108. Russo CR, Lauretani F, Bandinelli S, Bartali B, Di Iorio A, Volpato S, Guralnik JM, Harris T, Ferrucci L. Aging bone in men and women: beyond changes in bone mineral density. Osteoporos Int. 2003;14:531–538.

    PubMed  CAS  Google Scholar 

  109. Schuit SC, van der Klift M, Weel AE, de Laet CE, Burger H, Seeman E, Hofman A, Uitterlinden AG, van Leeuwen JP, Pols HA. Fracture incidence and association with bone mineral density in elderly men and women: the Rotterdam study. Bone. 2004;34:195–202.

    PubMed  CAS  Google Scholar 

  110. Shea B, Wells G, Cranney A, Zytaruk N, Robinson V, Griffith L, Ortiz Z, Peterson J, Adachi J, Tugwell P, Guyatt G. Meta-analyses of therapies for postmenopausal osteoporosis. VII. Meta-analysis of calcium supplementation for the prevention of postmenopausal osteoporosis. Endocr Rev. 2002;23:552–559.

    PubMed  CAS  Google Scholar 

  111. Silva MJ, Gibson LJ. Modeling the mechanical behavior of vertebral trabecular bone: effects of age-related changes in microstructure. Bone. 1997;21:191–199.

    PubMed  CAS  Google Scholar 

  112. Slemenda CW, Christian JC, Williams CJ, Norton JA, Johnston CC Jr. Genetic determinants of bone mass in adult women: a reevaluation of the twin model and the potential importance of gene interaction on heritability estimates. J Bone Miner Res. 1991;6:561–567.

    PubMed  CAS  Google Scholar 

  113. Smith EL, Gilligan C, McAdam M, Ensign CP, Smith PE. Deterring bone loss by exercise intervention in premenopausal and postmenopausal women. Calcif Tissue Int. 1989;44:312–321.

    PubMed  CAS  Google Scholar 

  114. Snow-Harter C, Bouxsein ML, Lewis BT, Carter DR, Marcus R. Effects of resistance and endurance exercise on bone mineral status of young women: a randomized exercise intervention trial. J Bone Miner Res. 1992;7:761–769.

    PubMed  CAS  Google Scholar 

  115. Snyder BD, Hauser-Kara DA, Hipp JA, Zurakowski D, Hecht AC, Gebhardt MC. Predicting fracture through benign skeletal lesions with quantitative computed tomography. J Bone Joint Surg Am. 2006;88:55–70.

    PubMed  Google Scholar 

  116. Stone KL, Seeley DG, Lui LY, Cauley JA, Ensrud K, Browner WS, Nevitt MC, Cummings SR. BMD at multiple sites and risk of fracture of multiple types: long-term results from the study of osteoporotic fractures. J Bone Miner Res. 2003;18:1947–1954.

    PubMed  Google Scholar 

  117. Timlin JA, Carden A, Morris MD, Rajachar RM, Kohn DH. Raman spectroscopic imaging markers for fatigue-related microdamage in bovine bone. Anal Chem. 2000;72:2229–2236.

    PubMed  CAS  Google Scholar 

  118. Turner CH, Hsieh YF, Müller R, Bouxsein ML, Baylink DJ, Rosen CJ, Grynpas MD, Donahue LR, Beamer WG. Genetic regulation of cortical and trabecular bone strength and microstructure in inbred strains of mice. J Bone Miner Res. 2000;15:1126–1131.

    PubMed  CAS  Google Scholar 

  119. Turner CH, Sun Q, Schriefer J, Pitner N, Price R, Bouxsein ML, Rosen CJ, Donahue LR, Shultz KL, Beamer WG. Congenic mice reveal sex-specific genetic regulation of femoral structure and strength. Calcif Tissue Int. 2003;73:297–303.

    PubMed  CAS  Google Scholar 

  120. Turner RT, Bell NH, Duvall P, Bobyn JD, Spector M, Holton EM, Baylink DJ. Spaceflight results in formation of defective bone. Proc Soc Exp Biol Med. 1985;180:544–549.

    PubMed  CAS  Google Scholar 

  121. Tylavsky FA, Bortz AD, Hancock RL, Anderson JJ. Familial resemblance of radial bone mass between premenopausal mothers and their college-age daughters. Calcif Tissue Int. 1989;45:265–272.

    PubMed  CAS  Google Scholar 

  122. Ulrich D, Hildebrand T, van Rietbergen B, Müller R, Rüegsegger P. The quality of trabecular bone evaluated with micro-computed tomography, FEA and mechanical testing. Stud Health Technol Inform. 1997;40:97–112.

    PubMed  CAS  Google Scholar 

  123. van der Meulen MC, Ashford MW Jr, Kiratli BJ, Bachrach LK, Carter DR. Determinants of femoral geometry and structure during adolescent growth. J Orthop Res. 1996;14:22–29.

    PubMed  Google Scholar 

  124. van der Meulen MC, Jepsen KJ, Mikić B. Understanding bone strength: size isn’t everything. Bone. 2001;29:101–104.

    PubMed  Google Scholar 

  125. van der Meulen MC, Morey-Holton ER, Carter DR. Hindlimb suspension diminishes femoral cross-sectional growth in the rat. J Orthop Res. 1995;13:700–707.

    PubMed  Google Scholar 

  126. van Rietbergen B, Huiskes R, Eckstein F, Rüegsegger P. Trabecular bone tissue strains in the healthy and osteoporotic human femur. J Bone Miner Res. 2003;18:1781–1788.

    PubMed  Google Scholar 

  127. Vico L, Collet P, Guignandon A, Lafage-Proust MH, Thomas T, Rehaillia M, Alexandre C. Effects of long-term microgravity exposure on cancellous and cortical weight-bearing bones of cosmonauts. Lancet. 2000;355:1607–1611.

    PubMed  CAS  Google Scholar 

  128. Volkman SK, Galecki AT, Burke DT, Miller RA, Goldstein SA. Quantitative trait loci that modulate femoral mechanical properties in a genetically heterogeneous mouse population. J Bone Miner Res. 2004;19:1497–1505.

    PubMed  CAS  Google Scholar 

  129. Volkman SK, Galecki AT, Burke DT, Paczas MR, Moalli MR, Miller RA, Goldstein SA. Quantitative trait loci for femoral size and shape in a genetically heterogeneous mouse population. J Bone Miner Res. 2003;18:1497–1505.

    PubMed  CAS  Google Scholar 

  130. Welch JM, Turner CH, Devareddy L, Arjmandi BH, Weaver CM. High impact exercise is more beneficial than dietary calcium for building bone strength in the growing rat skeleton. Bone. 2008;42:660–668.

    PubMed  CAS  Google Scholar 

  131. Woo SL, Kuei SC, Amiel D, Gomez MA, Hayes WC, White FC, Akeson WH. The effect of prolonged physical training on the properties of long bone: a study of Wolff’s law. J Bone Joint Surg Am. 1981;63:780–787.

    PubMed  CAS  Google Scholar 

  132. Yershov Y, Baldini TH, Villagomez S, Young T, Martin ML, Bockman RS, Peterson MG, Blank RD. Bone strength and related traits in HcB/Dem recombinant congenic mice. J Bone Miner Res. 2001;16:992–1003.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Chemistry, University of Michigan, Ann Arbor, MI, USA

    Jacqueline H. Cole PhD

  2. Department of Mechanical and Aerospace Engineering, Cornell University, 219 Upson Hall, Ithaca, NY, 14853, USA

    Marjolein C. H. van der Meulen PhD

  3. Hospital for Special Surgery, New York, NY, USA

    Marjolein C. H. van der Meulen PhD

Authors
  1. Jacqueline H. Cole PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marjolein C. H. van der Meulen PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marjolein C. H. van der Meulen PhD.

Additional information

One or more of the authors received funding from the National Institutes of Health (F32-AR056186 (JHC) and R01-AR053571 (MCHM)).

About this article

Cite this article

Cole, J.H., van der Meulen, M.C.H. Whole Bone Mechanics and Bone Quality. Clin Orthop Relat Res 469, 2139–2149 (2011). https://doi.org/10.1007/s11999-011-1784-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11999-011-1784-3

Keywords

Search

Navigation