Skip to main content
SpringerLink
Log in

The Influence of Cortical Porosity on the Strength of Bone During Growth and Advancing Age

  • Epidemiology and Pathophysiology (F Cosman and D Shoback, Section Editors)
  • Published:
Current Osteoporosis Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

Bone densitometry provides a two-dimensional projected areal apparent bone mineral density that fails to capture the heterogeneity of bone’s material composition and macro-, micro-, and nano-structures critical to its material and structural strength. Assessment of the structural basis of bone fragility has focused largely on trabecular bone based on the common occurrence of fragility fractures at sites with substantial amounts of trabecular bone. This review focuses on the contribution of cortical bone to bone fragility throughout life.

Recent Findings

Accurately differentiating cortical and trabecular bone loss has important implications in quantifying bone fragility as these compartments have differing effects on bone strength. Recent advances in imaging methodology have improved distinction of these two compartments by (i) recognition of a cortico-trabecular transitional zone and (ii) quantifying bone microstructure in a region of interest that is a percentage of bone length rather than a fixed point. Additionally, non-invasive three-dimensional imaging methods allow more accurate quantification of changes in the cortical, trabecular, and cortico-trabecular compartments during growth, aging, disease, and treatment.

Summary

Over 75% of the skeleton is assembled as cortical bone. Of all fragility fractures, ~ 80% are appendicular and involve regions rich in cortical bone and ~ 70% of all age-related appendicular bone loss is cortical and is mainly due to unbalanced intracortical remodeling which increases cortical porosity. The failure to achieve the optimal peak bone microstructure during growth due to disease and the deterioration in cortical and trabecular bone produced by bone loss compromise bone strength. The loss of strength produced by microstructural deterioration is disproportionate to the bone loss producing this deterioration. The reason for this is that the loss of strength increases as a 7th power function of the rise in cortical porosity and a 3rd power function of the fall in trabecular density (Schaffler and Burr in J Biomech. 21(1):13–6, 1988), hence the need to quantify bone microstructure.

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. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. Schaffler MB, Burr DB. Stiffness of compact bone: effects of porosity and density. J Biomech. 1988;21(1):13–6.

    Article  CAS  PubMed  Google Scholar 

  2. Currey JD. The mechanical consequences of variation in the mineral content of bone. J Biomech. 1969;2(1):1–11.

    Article  CAS  PubMed  Google Scholar 

  3. Diab T, Condon KW, Burr DB, Vashishth D. Age-related change in the damage morphology of human cortical bone and its role in bone fragility. Bone. 2006;38(3):427–31. https://doi.org/10.1016/j.bone.2005.09.002.

    Article  PubMed  Google Scholar 

  4. 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. https://doi.org/10.1056/NEJMra053077.

    Article  CAS  PubMed  Google Scholar 

  5. Granke M, Does MD, Nyman JS. The role of water compartments in the material properties of cortical bone. Calcif Tissue Int. 2015;97(3):292–307. https://doi.org/10.1007/s00223-015-9977-5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Buenzli PR, Sims NA. Quantifying the osteocyte network in the human skeleton. Bone. 2015;75:144–50. https://doi.org/10.1016/j.bone.2015.02.016.

    Article  CAS  PubMed  Google Scholar 

  7. Currey J. Incompatible mechanical properties in compact bone. J Theor Biol. 2004;231(4):569–80. https://doi.org/10.1016/j.jtbi.2004.07.013.

    Article  PubMed  Google Scholar 

  8. Frost HM. The Utah paradigm of skeletal physiology: an overview of its insights for bone, cartilage and collagenous tissue organs. J Bone Miner Metab. 2000;18(6):305–16.

    Article  CAS  PubMed  Google Scholar 

  9. Ruff CB, Hayes WC. Sex differences in age-related remodeling of the femur and tibia. J Orthop Res. 1988;6(6):886–96. https://doi.org/10.1002/jor.1100060613.

    Article  CAS  PubMed  Google Scholar 

  10. Bjornerem A, Bui QM, Ghasem-Zadeh A, Hopper JL, Zebaze R, Seeman E. Fracture risk and height: an association partly accounted for by cortical porosity of relatively thinner cortices. J Bone Miner Res. 2013;28(9):2017–26. https://doi.org/10.1002/jbmr.1934.

    Article  PubMed  Google Scholar 

  11. Zebaze RM, Jones A, Knackstedt M, Maalouf G, Seeman E. Construction of the femoral neck during growth determines its strength in old age. J Bone Miner Res. 2007;22(7):1055–61. https://doi.org/10.1359/jbmr.070329.

    Article  PubMed  Google Scholar 

  12. Wang Q, Wang XF, Iuliano-Burns S, Ghasem-Zadeh A, Zebaze R, Seeman E. Rapid growth produces transient cortical weakness: a risk factor for metaphyseal fractures during puberty. J Bone Miner Res. 2010;25(7):1521–6. https://doi.org/10.1002/jbmr.46.

    Article  PubMed  Google Scholar 

  13. Cadet ER, Gafni RI, McCarthy EF, McCray DR, Bacher JD, Barnes KM, et al. Mechanisms responsible for longitudinal growth of the cortex: coalescence of trabecular bone into cortical bone. J Bone Joint Surg Am. 2003;85-A(9):1739–48.

    Article  PubMed  Google Scholar 

  14. Enlow DH. A study of the post-natal growth and remodeling of bone. Am J Anat. 1962;110:79–101. https://doi.org/10.1002/aja.1001100202.

    Article  CAS  PubMed  Google Scholar 

  15. Wang Q, Ghasem-Zadeh A, Wang XF, Iuliano-Burns S, Seeman E. Trabecular bone of growth plate origin influences both trabecular and cortical morphology in adulthood. J Bone Miner Res. 2011;26(7):1577–83. https://doi.org/10.1002/jbmr.360.

    Article  PubMed  Google Scholar 

  16. Bala Y, Bui QM, Wang XF, Iuliano S, Wang Q, Ghasem-Zadeh A, et al. Trabecular and cortical microstructure and fragility of the distal radius in women. J Bone Miner Res. 2015;30(4):621–9. https://doi.org/10.1002/jbmr.2388.

    Article  PubMed  Google Scholar 

  17. Zebaze RM, Jones A, Welsh F, Knackstedt M, Seeman E. Femoral neck shape and the spatial distribution of its mineral mass varies with its size: clinical and biomechanical implications. Bone. 2005;37(2):243–52. https://doi.org/10.1016/j.bone.2005.03.019.

    Article  PubMed  Google Scholar 

  18. Wang Q, Cheng S, Alen M, Seeman E, Finnish Calex Study G. Bone’s structural diversity in adult females is established before puberty. J Clin Endocrinol Metab. 2009;94(5):1555–61. https://doi.org/10.1210/jc.2008-2339.

    Article  CAS  PubMed  Google Scholar 

  19. Yeni YN, Brown CU, Wang Z, Norman TL. The influence of bone morphology on fracture toughness of the human femur and tibia. Bone. 1997;21(5):453–9.

    Article  CAS  PubMed  Google Scholar 

  20. Rho JY, Zioupos P, Currey JD, Pharr GM. Microstructural elasticity and regional heterogeneity in human femoral bone of various ages examined by nano-indentation. J Biomech. 2002;35(2):189–98.

    Article  CAS  PubMed  Google Scholar 

  21. Currey JD. Bones: structure and mechanics. 2nd ed. Princeton: Princeton University Press; 2006.

    Google Scholar 

  22. Diab T, Vashishth D. Morphology, localization and accumulation of in vivo microdamage in human cortical bone. Bone. 2007;40(3):612–8. https://doi.org/10.1016/j.bone.2006.09.027.

    Article  PubMed  Google Scholar 

  23. Fantner GE, Hassenkam T, Kindt JH, Weaver JC, Birkedal H, Pechenik L, et al. Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nat Mater. 2005;4(8):612–6. https://doi.org/10.1038/nmat1428.

    Article  CAS  PubMed  Google Scholar 

  24. Gupta HS, Seto J, Wagermaier W, Zaslansky P, Boesecke P, Fratzl P. Cooperative deformation of mineral and collagen in bone at the nanoscale. Proc Natl Acad Sci U S A. 2006;103(47):17741–6. https://doi.org/10.1073/pnas.0604237103.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Hattner R, Epker BN, Frost HM. Suggested sequential mode of control of changes in cell behaviour in adult bone remodelling. Nature. 1965;206(983):489–90.

    Article  CAS  PubMed  Google Scholar 

  26. Vignery A, Baron R. Dynamic histomorphometry of alveolar bone remodeling in the adult rat. Anat Rec. 1980;196(2):191–200. https://doi.org/10.1002/ar.1091960210.

    Article  CAS  PubMed  Google Scholar 

  27. Bala Y, Farlay D, Delmas PD, Meunier PJ, Boivin G. Time sequence of secondary mineralization and microhardness in cortical and cancellous bone from ewes. Bone. 2010;46(4):1204–12. https://doi.org/10.1016/j.bone.2009.11.032.

    Article  PubMed  Google Scholar 

  28. Parfitt AM. Skeletal heterogeneity and the purposes of bone remodelling: implications for the understanding of osteoporosis. In: Marcus RFD, Kelsey J, editors. Osteoporosis. San Diego: Academic; 1996. p. 315–39.

    Google Scholar 

  29. Hernandez CJ, Gupta A, Keaveny TM. A biomechanical analysis of the effects of resorption cavities on cancellous bone strength. J Bone Miner Res. 2006;21(8):1248–55. https://doi.org/10.1359/jbmr.060514.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Khosla S, Riggs BL, Atkinson EJ, Oberg AL, McDaniel LJ, Holets M, et al. Effects of sex and age on bone microstructure at the ultradistal radius: a population-based noninvasive in vivo assessment. J Bone Miner Res. 2006;21(1):124–31. https://doi.org/10.1359/JBMR.050916.

    Article  PubMed  Google Scholar 

  31. Riggs BL, Melton LJ, Robb RA, Camp JJ, Atkinson EJ, McDaniel 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. 2008;23(2):205–14. https://doi.org/10.1359/jbmr.071020.

    Article  PubMed  Google Scholar 

  32. • Bjornerem A, Wang X, Bui M, Ghasem-Zadeh A, Hopper JL, Zebaze R, et al. Menopause-related appendicular bone loss is mainly cortical and results in increased cortical porosity. J Bone Miner Res. 2017; https://doi.org/10.1002/jbmr.3333. This prospective study demonstrates the dominant role of cortical bone loss to overall loss of bone after menopause and challenges the notion that bone loss is mainly trabecular in origin.

    Article  CAS  PubMed  Google Scholar 

  33. Vedi S, Compston JE, Webb A, Tighe JR. Histomorphometric analysis of dynamic parameters of trabecular bone formation in the iliac crest of normal British subjects. Metab Bone Dis Relat Res. 1983;5(2):69–74.

    Article  PubMed  Google Scholar 

  34. Lips P, Courpron P, Meunier PJ. Mean wall thickness of trabecular bone packets in the human iliac crest: changes with age. Calcif Tissue Res. 1978;26(1):13–7.

    Article  CAS  PubMed  Google Scholar 

  35. Manolagas SC. Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev. 2000;21(2):115–37. https://doi.org/10.1210/edrv.21.2.0395.

    Article  CAS  PubMed  Google Scholar 

  36. Compston JE, Mellish RW, Croucher P, Newcombe R, Garrahan NJ. Structural mechanisms of trabecular bone loss in man. Bone Miner. 1989;6(3):339–50.

    Article  CAS  PubMed  Google Scholar 

  37. • Zebaze RM, Ghasem-Zadeh A, Bohte A, Iuliano-Burns S, Mirams M, Price RI, et al. Intracortical remodelling and porosity in the distal radius and post-mortem femurs of women: a cross-sectional study. Lancet. 2010;375(9727):1729–36. https://doi.org/10.1016/S0140-6736(10)60320-0. This study demonstrates the underestimation of the age-related increase in cortical porosity and decrease in trabecular density produced when cortical and trabecular compartments are incorrectly segmented (separated) from each other.

    Article  PubMed  Google Scholar 

  38. • Bjornerem A, Ghasem-Zadeh A, Bui M, Wang X, Rantzau C, Nguyen TV, et al. Remodeling markers are associated with larger intracortical surface area but smaller trabecular surface area: a twin study. Bone. 2011;49(6):1125–30. https://doi.org/10.1016/j.bone.2011.08.009. This study illustrates that bone remodeling is surface dependent; the higher the cortical surface area is, the higher the remodeling.

    Article  PubMed  Google Scholar 

  39. Shigdel R, Osima M, Ahmed LA, Joakimsen RM, Eriksen EF, Zebaze R, et al. Bone turnover markers are associated with higher cortical porosity, thinner cortices, and larger size of the proximal femur and non-vertebral fractures. Bone. 2015;81:1–6. https://doi.org/10.1016/j.bone.2015.06.016.

    Article  PubMed  Google Scholar 

  40. Parfitt AM. Morphological basis of bone mineral measurements: transient and steady state effects of treatment in osteoporosis. Miner Electrolyte Metab. 1980;4:273–87.

    Google Scholar 

  41. Andreasen CM, Delaisse JM, van der Eerden BCJ, van Leeuwen J, Ding M, Andersen TL. Understanding age-induced cortical porosity in women: the accumulation and coalescence of eroded cavities upon existing intracortical canals is the main contributor. J Bone Miner Res. 2017;33:606–20. https://doi.org/10.1002/jbmr.3354.

    Article  Google Scholar 

  42. Foldes J, Parfitt AM, Shih MS, Rao DS, Kleerekoper M. Structural and geometric changes in iliac bone: relationship to normal aging and osteoporosis. J Bone Miner Res. 1991;6(7):759–66. https://doi.org/10.1002/jbmr.5650060714.

    Article  CAS  PubMed  Google Scholar 

  43. Han ZH, Palnitkar S, Rao DS, Nelson D, Parfitt AM. Effects of ethnicity and age or menopause on the remodeling and turnover of iliac bone: implications for mechanisms of bone loss. J Bone Miner Res. 1997;12(4):498–508. https://doi.org/10.1359/jbmr.1997.12.4.498.

    Article  CAS  PubMed  Google Scholar 

  44. Parfitt AM. Misconceptions (2): turnover is always higher in cancellous than in cortical bone. Bone. 2002;30(6):807–9.

    Article  CAS  PubMed  Google Scholar 

  45. Recker R, Lappe J, Davies KM, Heaney R. Bone remodeling increases substantially in the years after menopause and remains increased in older osteoporosis patients. J Bone Miner Res. 2004;19(10):1628–33. https://doi.org/10.1359/JBMR.040710.

    Article  PubMed  Google Scholar 

  46. Zebaze R, Seeman E. Cortical bone: a challenging geography. J Bone Miner Res. 2015;30(1):24–9. https://doi.org/10.1002/jbmr.2419.

    Article  PubMed  Google Scholar 

  47. Seeman E. Bone morphology in response to alendronate as seen by high-resolution computed tomography: through a glass darkly. J Bone Miner Res. 2010;25(12):2553–7. https://doi.org/10.1002/jbmr.261.

    Article  CAS  PubMed  Google Scholar 

  48. Tang T, Cripton PA, Guy P, McKay HA, Wang R. Clinical hip fracture is accompanied by compression induced failure in the superior cortex of the femoral neck. Bone. 2017;108:121–31. https://doi.org/10.1016/j.bone.2017.12.020.

    Article  PubMed  Google Scholar 

  49. Bouxsein ML. Determinants of skeletal fragility. Best Pract Res Clin Rheumatol. 2005;19(6):897–911. https://doi.org/10.1016/j.berh.2005.07.004.

    Article  PubMed  Google Scholar 

  50. Rockoff SD, Sweet E, Bleustein J. The relative contribution of trabecular and cortical bone to the strength of human lumbar vertebrae. Calcif Tissue Res. 1969;3(2):163–75.

    Article  CAS  PubMed  Google Scholar 

  51. Holzer G, von Skrbensky G, Holzer LA, Pichl W. Hip fractures and the contribution of cortical versus trabecular bone to femoral neck strength. J Bone Miner Res. 2009;24(3):468–74. https://doi.org/10.1359/jbmr.081108.

    Article  PubMed  Google Scholar 

  52. Nawathe S, Nguyen BP, Barzanian N, Akhlaghpour H, Bouxsein ML, Keaveny TM. Cortical and trabecular load sharing in the human femoral neck. J Biomech. 2015;48(5):816–22. https://doi.org/10.1016/j.jbiomech.2014.12.022.

    Article  PubMed  Google Scholar 

  53. Lotz JC, Cheal EJ, Hayes WC. Stress distributions within the proximal femur during gait and falls: implications for osteoporotic fracture. Osteoporos Int. 1995;5(4):252–61.

    Article  CAS  PubMed  Google Scholar 

  54. McCalden RW, McGeough JA, Barker MB, Court-Brown CM. Age-related changes in the tensile properties of cortical bone. The relative importance of changes in porosity, mineralization, and microstructure. J Bone Joint Surg Am. 1993;75(8):1193–205.

    Article  CAS  PubMed  Google Scholar 

  55. Granke M, Grimal Q, Saied A, Nauleau P, Peyrin F, Laugier P. Change in porosity is the major determinant of the variation of cortical bone elasticity at the millimeter scale in aged women. Bone. 2011;49(5):1020–6. https://doi.org/10.1016/j.bone.2011.08.002.

    Article  PubMed  Google Scholar 

  56. Dong XN, Guo XE. The dependence of transversely isotropic elasticity of human femoral cortical bone on porosity. J Biomech. 2004;37(8):1281–7. https://doi.org/10.1016/j.jbiomech.2003.12.011.

    Article  PubMed  Google Scholar 

  57. 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(3):392–9. https://doi.org/10.1359/jbmr.071108.

    Article  PubMed  Google Scholar 

  58. Bala Y, Zebaze R, Ghasem-Zadeh A, Atkinson EJ, Iuliano S, Peterson JM, et al. Cortical porosity identifies women with osteopenia at increased risk for forearm fractures. J Bone Miner Res. 2014;29(6):1356–62. https://doi.org/10.1002/jbmr.2167.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Siris ES, Chen YT, Abbott TA, Barrett-Connor E, Miller PD, Wehren LE, et al. Bone mineral density thresholds for pharmacological intervention to prevent fractures. Arch Intern Med. 2004;164(10):1108–12. https://doi.org/10.1001/archinte.164.10.1108.

    Article  PubMed  Google Scholar 

  60. Sanders KM, Nicholson GC, Watts JJ, Pasco JA, Henry MJ, Kotowicz MA, et al. Half the burden of fragility fractures in the community occur in women without osteoporosis. When is fracture prevention cost-effective? Bone. 2006;38(5):694–700. https://doi.org/10.1016/j.bone.2005.06.004.

    Article  PubMed  Google Scholar 

  61. Schuit SC, van der Klift M, Weel AE, de Laet CE, Burger H, Seeman E, et al. Fracture incidence and association with bone mineral density in elderly men and women: the Rotterdam Study. Bone. 2004;34(1):195–202.

    Article  CAS  PubMed  Google Scholar 

  62. Ahmed LA, Shigdel R, Joakimsen RM, Eldevik OP, Eriksen EF, Ghasem-Zadeh A, et al. Measurement of cortical porosity of the proximal femur improves identification of women with nonvertebral fragility fractures. Osteoporos Int. 2015;26(8):2137–46. https://doi.org/10.1007/s00198-015-3118-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Ghasem-Zadeh A, Burghardt A, Wang XF, Iuliano S, Bonaretti S, Bui M, et al. Quantifying sex, race, and age specific differences in bone microstructure requires measurement of anatomically equivalent regions. Bone. 2017;101:206–13. https://doi.org/10.1016/j.bone.2017.05.010.

    Article  PubMed  Google Scholar 

  64. Delmas PD. Treatment of postmenopausal osteoporosis. Lancet. 2002;359(9322):2018–26. https://doi.org/10.1016/S0140-6736(02)08827-X.

    Article  CAS  PubMed  Google Scholar 

  65. Seeman E, Martin TJ. Co-administration of antiresorptive and anabolic agents: a missed opportunity. J Bone Miner Res. 2015;30(5):753–64. https://doi.org/10.1002/jbmr.2496.

    Article  CAS  PubMed  Google Scholar 

  66. Donnelly E, Saleh A, Unnanuntana A, Lane JM. Atypical femoral fractures: epidemiology, etiology, and patient management. Curr Opin Support Palliat Care. 2012;6(3):348–54. https://doi.org/10.1097/SPC.0b013e3283552d7d.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Lo JC, Huang SY, Lee GA, Khandelwal S, Provus J, Ettinger B, et al. Clinical correlates of atypical femoral fracture. Bone. 2012;51(1):181–4. https://doi.org/10.1016/j.bone.2012.02.632.

    Article  PubMed  Google Scholar 

  68. Marcano A, Taormina D, Egol KA, Peck V, Tejwani NC. Are race and sex associated with the occurrence of atypical femoral fractures? Clin Orthop Relat Res. 2014;472(3):1020–7. https://doi.org/10.1007/s11999-013-3352-5.

    Article  PubMed  Google Scholar 

  69. Seeman E. Clinical review 137: sexual dimorphism in skeletal size, density, and strength. J Clin Endocrinol Metab. 2001;86(10):4576–84. https://doi.org/10.1210/jcem.86.10.7960.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Medicine, The University of Melbourne, Austin Health, Melbourne, Australia

    Sabashini K. Ramchand & Ego Seeman

  2. Department of Endocrinology, Level 2 Centaur Wing, Austin Health Repatriation Campus, 300 Waterdale Road, Heidelberg Heights, Melbourne, Victoria, 3081, Australia

    Sabashini K. Ramchand & Ego Seeman

  3. Australian Catholic University, Melbourne, Australia

    Ego Seeman

Authors
  1. Sabashini K. Ramchand
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ego Seeman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sabashini K. Ramchand.

Ethics declarations

Conflict of Interest

Ego Seeman reports research support and lecture fees from Amgen, Allergan, and Eli Lilly, outside the submitted work. Dr. Seeman also has a patent (StrAx1.0) and is the director of the board and shareholder of StraxCorp. Sabashini Ramchand declares no conflict of interest.

Human and Animal Rights and Informed Consent

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

Additional information

This article is part of the Topical Collection on Epidemiology and Pathophysiology

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ramchand, S.K., Seeman, E. The Influence of Cortical Porosity on the Strength of Bone During Growth and Advancing Age. Curr Osteoporos Rep 16, 561–572 (2018). https://doi.org/10.1007/s11914-018-0478-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11914-018-0478-0

Keywords

Search

Navigation