Characterisation of Trabecular Bone Structure

Studies in Mechanobiology, Tissue Engineering and Biomaterials

Volumn 5, Issue , 2013, Pages 31-51

  Parkinson, Ian H ^a,b   Fazzalari, Nicola L ^a,b  

^a Bone and Joint Research Laboratory   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Bone Histomorphometry; Distal Radius; Peak Bone Mass; Skeletal Site; Trabecular Bone

Indexed keywords

EID: 85085218872     PISSN: 18682006     EISSN: 18682014     Source Type: Book Series    
DOI: 10.1007/8415_2011_113     Document Type: Chapter

References (113)

1. Aaron, J.E., Makins, N.B., et al.: The microanatomy of trabecular bone loss in normal aging men and women. Clin. Orthop. Relat. Res. 215, 260–271 (1987)
2. Aaron, J.E., Shore, P.A., et al.: Trabecular architecture in women and men of similar bone mass with and without vertebral fracture: II. Three-dimensional histology. Bone 27, 277–282 (2000)
3. Amling, M., Herden, S., et al.: Polyostotic heterogeneity of the spine in osteoporosis. Quantitative analysis and three-dimensional morphology. Bone Miner. 27, 193–208 (1994)
4. Amling, M., Herden, S., et al.: Heterogeneity of the skeleton: comparison of the trabecular microarchitecture of the spine, the iliac crest, the femur and the calcaneus. J. Bone Miner. Res. 11, 36–45 (1996)
5. Anonymous. World Medical Association Declaration of Helsinki. W. M. Association (2008)
6. Badiei, A., Bottema, M.J., et al.: Influence of orthogonal overload on human vertebral trabecular bone mechanical properties. J. Bone Miner. Res. 22, 1690–1699 (2007)
7. Bevill, G., Eswaran, S.K., et al.: Influence of bone volume fraction and architecture on computed large-deformation failure mechanisms in human trabecular bone. Bone 39, 1218–1225 (2006)
8. Biewener, A.A.: Safety factors in bone strength. Calcif. Tissue Int. 53(Suppl 1), 68–74 (1993)
9. Birkenhager-Frenkel, D.H., Courpron, P., et al.: Age-related changes in cancellous bone structure. Bone Miner. 4, 197–216 (1988)
10. Borah, B., Defresne, T.E., et al.: Long-term risedronate treatment normalizes mineralization and continues to preserve trabecular architecture: sequential triple biopsy studies with micro-computed tomography. Bone 39, 345–352 (2006)
11. Borah, B., Ritman E.L., et al.: The effect of risedronate on bone mineralization as measured by micro-computed tomography with synchrotron radiation: correlation to histomorphometric indices of turnover. Bone 37, 1–9 (2005)
12. Bouxsein, M.L., Boyd, S.K., et al.: Guidlines for assessment of bone microsctructure in rodents using micro-computed tomography. J. Bone Miner. Res. 25, 1468–1486 (2010)
13. Burr, D.B.: Targeted and nontargeted remodeling. Bone 30, 2–4 (2002)
14. Byers, S., Moore, A., et al.: Quantitative histomorphometric analysis of the human growth plate from birth to adolescence. Bone 27, 495–501 (2000)
15. Callis, G.M.: Bone. Theory and practice of histological techniques. In: Bancroft, J.D., Gamble, M. (eds.) pp. 333–364. Churchill Livingstone, London (2008)
16. Carneiro, R.M., Prebehalla, L., et al.: Lactation and bone turnover: a conundrum of marked bone loss in the setting of coupled bone turnover. J. Clin. Endocrinol. Metab. 95, 1767–1776 (2010)
17. Chappard, C., Peyrin, F., et al.: Subchondral bone micro-architectural alterations in osteoarthritis: a synchrotron micro-computed tomography study. Osteoarthr. Cartil. 14, 215–223 (2006)
18. Chappard, D., Legrand E., et al.: Measuring trabecular bone architecture by image analysis of histological sections. Microsc. Anal. 13, 23–25 (1997)
19. Chappard, D., Legrand, E., et al.: Altered trabecular architecture induced by corticosteroids: a histomorphometric study. J. Bone Miner. Res. 5, 676–685 (1996)
20. Chavassieux, P., Meunier, P.J.: Histomorphometric approach of bone loss in men. Calcif. Tissue Intern. 69, 209–213 (2001)
21. Compston, J.E.: Bone histomorphometry––the renaissance. BoneKEy-Osteovis. 1, 9–12 (2004)
22. Compston, J.E., Mellish, R.W.E., et al.: Structural mechanisms of trabecular bone loss in man. Bone Miner. 6, 339–350 (1989)
23. Currey, J.: Minimum mass of cancellous bone. Bone: structure and mechanics J. Currey, pp. 224–225. Princeton, Princeton University Press (2002)
24. Dempster, D.W., Ferguson-Pell, M., et al.: Relationships between bone structure in the iliac crest and bone structure in the lumbar spine. Osteoporos. Int. 3, 90–96 (1993)
25. Ebbesen, E.N., Thomsen, J.S., et al.: Age-and gender-related differences in vertebral bone mass, density, and strength. J. Bone Miner. Res. 14, 1394–1403 (1999)
26. Eckstein, F., Matsuura, M., et al.: Sex differences of human trabecular bone microstructure in aging are site specific. J. Bone Miner. Res. 22, 817–824 (2007)
27. Engelke, K., Gluer, C.C., et al.: Structural and fractal analyses of the trabecular network using micro computed tomography images. J. Bone Miner. Res. 8, S354 (1993)
28. Fazzalari, N.L., Crisp, D.J., et al.: Mathematical modelling of trabecular bone structure: the evaluation of analytical and quantified surface to volume relationships in the femoral head and iliac crest. J. Biomech. 22, 901–910 (1989)
29. Fazzalari, N.L., Darracott, J., et al.: A quantitative description of selected stress regions of cancellous bone in the head of the femur using automatic image analysis. Metab. Bone Dis. Relat. Res. 5, 119–125 (1983)
30. Fazzalari, N.L., Forwood, M.R., et al.: Assessment of cancellous bone quality in severe oseoarthritis: bone mineral dnesity, mechanics and microdamage. Bone 22, 381–388 (1998)
31. Fazzalari, N.L., Kuliwaba, J.S., et al.: The ratio of messenger RNA levels of receptor activator of nuclear factor kB ligand to osteoprotegerin correlates with bone remodeling indices in normal human cancellous bone but not in osteoarthritis. J. Bone Miner. Res. 16, 1015–1027 (2001)
32. Fazzalari, N.L., Kuliwaba, J.S., et al.: Cancellous bone microdamage in the proximal femur: influence of age and osteoarthritis on damage morphology and regional distribution. Bone 31, 697–702 (2002)
33. Fazzalari, N.L., Moore, A., et al.: Quantitative analysis of trabecular morphogenesis in the human costochondral junction during postnatal period in normal subjects. The Anat. Rec. 248, 1–12 (1997)
34. Fazzalari, N.L., Moore, R.J., et al.: Comparative study of iliac crest and subchondral femoral bone in osteoarthritic patients. Bone 13, 331–335 (1992)
35. Fazzalari, N.L., Parkinson, I.H.: Femoral trabecular bone of osteoarthritic and normal subjects in an age and sex matched group. Osteoarthr. Cartil. 6, 377–382 (1998)
36. Fazzalari, N.L., Parkinson, I.H., et al.: Antero-postero differences in cortical thickness and cortical porosity of thoraco-lumbar vertebral bodies. Jt. Bone Spine 73, 293–297 (2006)
37. Feldkamp, L.A., Goldstein, S.A., et al.: The direct examination of three-dimensional bone architecture in vitro by computed tomography. J. Bone Miner. Res. 4, 3–11 (1989)
38. Fields, A.J., Eswaran, S.K., et al.: Role of trabecular microarchitecture in whole-vertebral body biomechanical behavior. J. Bone Miner. Res. 24, 1523–1530 (2009)
39. Frost, H.M.: Tetracycline-based histological analysis of bone remodeling. Calcif. Tissue Res. 3, 211–237 (1969)
40. Frost, H.M.: Bone histomorphometry: analysis of trabecular bone dynamics. In: Recker R.R. (ed.) Bone histomorphometry: techniques and interpretation, pp. 109–131. CRC Press, Boca Raton (1983)
41. Frost, H.M.: From Wolff’s law to the Utah paradigm: insights about bone physiology and its clinical applications. The Anatomical Record 262, 398–419 (2001)
42. Glorieux, F.H., Salle, B.L., et al.: Dynamic histomorphometric evaluation of human fetal bone formation. Bone 12, 377–381 (1991)
43. Guggenbuhl, P.: Osteoporosis in males and females: is there really a difference? Jt. Bone Spine 76, 595–601 (2009)
44. Guo, X.E., Kim, C.H.: Mechanical consequence of trabecular bone loss and its treatment: a three-dimension model simulation. Bone 30, 404–411 (2002)
45. Heaney, R.P., Abrams, S., et al.: Peak bone mass. Osteoporos. Int. 11, 985–1009 (2000)
46. Hildebrand, T., Laib, A., et al.: Direct three-dimensional morphometric analysis of human cancellous bone: microstrucural data from spine, femur, iliac crest, and calcaneus. J. Bone Miner. Res. 14, 1167–1174 (1999)
47. Hildebrand, T., Ruegsegger, P.: A new method for the model-independent assessment of thickness in three-dimensional images. J. Microsc. 185, 67–75 (1997)
48. Hildebrand, T., Ruegsegger, P.: Quantification of bone microarchitecture with the structure model index. Comput. Meth. Biomech. Biomed. Eng. 1, 15–23 (1997)
49. Homminga, J., McCreadie, B.R., et al.: Cancellous bone mechanical properties from normals and patients with hip fractures differ on the structural level, not on the bone hard tissue level. Bone 30, 759–764 (2002)
50. Hordon, L.D., Raisa, M., et al.: Trabecular architecture in women and men of similar bone mass with and without vertebral fracture: I. Two dimensional histology. Bone 27, 271–276 (2000)
51. Ito, M., Nakmura, T., et al.: Analysis of trabecular microarchitecture of human iliac bone using microcomputed tomography in patients with hip arthrosis with and without vertebral fracture. Bone 23, 163–169 (1998)
52. Johnell, O., Kanis, J.A.: An estimate of the worldwide prevalence, mortality and disability associated with hip fracture. Osteoporos. Int. 15, 897–902 (2004)
53. Johnell, O., Kanis, J.A.: An estimate of the worldwide prevalence and disability with osteoporotic fractures. Osteoporos. Int. 17, 1726–1733 (2006)
54. Kanis, J.A., Borgstrom, F., et al.: Assessment of fracture risk. Osteoporos. Int. 16, 581–589 (2005)
55. Kaufman, J.M., Goemaere, S.: Osteoporosis in men. Best Pract. Res. Clin. Endocrinol. Metab. 22, 787–812 (2008)
56. Kimmel, D.B., Jee, W.S.S.: Measurements of area, perimeter and distance: details of data collection in bone histomorphometry. Bone histomorphometry: techniques and interpretation. Recker R.R., pp. 89–108. Boca Raton, CRC Press (1983)
57. Krug, R., Banerjee, S., et al.: Feasibility of in vivo structural analysis of high-resolution magnetic resonance images of the proximal femur. Osteoporos. Int. 16, 1307–1314 (2005)
58. Kuliwaba, J.S., Findlay, D.M., et al.: Enhanced expression of oseocalcin mRNS in human osteoarthitic trabecular bone of the proximal femur is associated with decreased expression of interleukin-6 and interleukin-11 mRNA. J. Bone Miner. Res. 15, 332–341 (2000)
59. Ladinsky, G.A., Vasilic, B., et al.: Trabecular structure quantified with the MRI-based virtual bone biopsy in postmenopausal women contributes to vertebral deformity burden independent of areal vertebral BMD. J. Bone Miner. Res. 23, 64–74 (2008)
60. Landin, L.A.: Fracture patterns in children. Acta Orthop. Scand. 202, 100–109 (1983)
61. Link, T.M., Vieth, V., et al.: High-resolution MRI vs multislice CT: which technique depicts the trabecular structure best? Eur. Radiol. 13, 663–671 (2003)
62. Liu, X.S., Bevill, G., et al.: Micromechanical analyses of vertebral trabecular bone based on individual trabeculae segmentation of plates and rods. J. Biomech. 42, 249–256 (2009)
63. Liu, X.S., Sajda, P., et al.: Complete volumetric decomposition of individual trabecular plates and rods and its morphological correlations with anisotropic elastic moduli in human trabecular bone. J. Bone Miner. Res. 23, 223–235 (2008)
64. Liu, X.S., Sajda, P., et al.: Quantification of the roles of trabecular microarchitecture and trabecular type in determining the elastic modulus of human trabecular bone. J. Bone Miner. Res. 21, 1608–1617 (2006)
65. Liu, X.S., Zhang, X.H., et al.: Contributions of trabecular rods of various orientations in determining the elastic properties of human vertebral trabecular bone. ASME Summer Bioengineering Conference, Keystone, Colorado (2007)
66. Lochmuller, E.M., Matsuura, M., et al.: Site-specific deterioration of trabecular bone architecture in men and women with advancing age. J. Bone Miner. Res. 23, 1964–1973 (2008)
67. Majumdar, S.: A review of magnetic resonance (MR) imaging of trabecular bone microarchitecture: contribution to the prediction of biomechanical properties and fracture prevalence. Technol. Health Care 6, 321–327 (1998)
68. Mazess, R.B.: On aging bone loss. Clin. Orthop. Relat. Res. 165, 239–252 (1982)
69. Meunier, P.J.: Histomorphometry of the skeleton. In: Peck, W.A. (ed.) Bone and mineral research annual, pp. 191–222. Excerpta Medica, Amsterdam (1983)
70. Moore, R.J., Durbridge, T.C., et al.: Trabecular spacing in post-menopausal Australian women with and without vertebral fractures. Australian and New Zealand J. Med. 22, 269–273 (1992)
71. Morgan, E.F., Keaveny, T.M.: Dependence of yoield strain of human trabecular bone on anatomic site. J. Biomech. 34, 569–577 (2001)
72. Mori, S., Harruff, R., et al.: Trabecular bonevolume and microdamage accumulation in the femoral heads of women with and without femoral neck fractures. Bone 21, 521–526 (1997)
73. Mosekilde, L.: Sex differences in age-related loss of vertebral trabecular bone mass and structure-biomechanical consequences. Bone 10, 425–432 (1989)
74. Mueller, T.L., Van Lenthe, G.H., et al.: Regional, age and gender differences in architectural measures of bone quality and their contribution to bone mechanical competence in the human radius of an elderly population. Bone 45, 882–891 (2009)
75. Muller, R., Hahn, M., et al.: Morphometric analysis of noninvasively assessed bone biopsies: comparison of high-resolution computed tomography and histological sections. Bone 18, 215–220 (1996)
76. Muller, R., Hildebrand, T., et al.: Non-invasive bone biopsy: a new method to analyse and display the three-dimensional structure of trabecular bone. Phys. Med. Biol. 39, 145–164 (1994)
77. Muller, R., Koller, B., et al.: Resolution dependency of microstructural properties of cancellous bone based on three-dimensional micro-tomography. Technol. Health Care 4, 113–119 (1996)
78. Muller, R., van Campenhout, H., et al.: Morphometric analysis of human bone biopsies: a quantitative structural comparison of histological sections and micro-computed tomography. Bone 23, 59–66 (1998)
79. Odgaard, A.: Three-dimensional methods for quantification of cancellous bone architecture. Bone 20, 315–328 (1997)
80. Odgaard, A., Gundersen, H.J.: Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. Bone 14, 173–182 (1993)
81. Pahr, D.H., Zysset, P.K.: A comparison of enhanced continuum FE with micro FE models of human vertebral bodies. J. Biomech. 42, 455–462 (2009)
82. Parfitt, A.M.: Size of bone in the ages: endocortical resorption. J. Bone Miner. Res. 17, 1306 (2002)
83. Parfitt, A.M.: Targeted and nontargeted bone remodeling: Relationship to basic multicellular unit origination and progression. Bone 30, 5–7 (2002)
84. Parfitt, A.M., Drezner, M.K., et al.: Bone histomorphometry: standardization of nomenclature, symbols, and units. J. Bone Miner. Res. 2, 595–610 (1987)
85. Parfitt, A.M., Mathews, C.H.E., et al.: Relationships between surface, volume and thickness if iliac trabecular bone in aging and in osteoporosis. J. Clin. Investig. 72, 1396–1409 (1983)
86. Parkinson, I.H., Fazzalari, N.L.: Cancellous bone structure analysis using image analysis. Australasian Phys. Eng. Sci. Med. 417, 64–67 (1994)
87. Parkinson, I.H., Fazzalari, N.L.: Interrelationships between structural parameters of cancellous bone reveal accelerated structural change at low bone volume. J. Bone Miner. Res. 18, 2200–2205 (2003)
88. Parkinson, I.H., Forbes, D., et al.: Model-independent 3D descriptorss of vertebral cancellous bone architecture. J. Osteoporos. (2010). doi:10.4061/2010/641578
89. Reginster, J.-Y., Minne, H.W., et al.: Randomized trial of the effects of risedronate on vertebral fractures in women with established postmenopausal osteoporosis. Osteoporos. Int. 11, 83–91 (2000)
90. Riggs, B.L., Melton, L.J.: Involutional osteoporosis. The New England J. Med. 314, 1676–1686 (1986)
91. Riggs, B.L., Melton, L.J.: Bone turnover matters: the raloxifene treatment paradox of dramatic decreases in vertebral fractures without commensurate increases in bone density. J. Bone Miner. Res. 17, 11–14 (2002)
92. Riggs, B.L., Melton 3rd, L.J., et al.: Population-based study of age and sex differences in bone volumetric density, size, geometry, and structure at different skeletal sites. J. Bone Miner. Res. 19, 1945–1954 (2004)
93. Robling, A., Castillo, A., et al.: Biomechanical and molecular regulation of bone remodeling. Annu. Rev. Biomed. Eng. 8, 455–498 (2006)
94. Roux, J.P., Wegrzyn, J., et al.: Contribution of trabecular and cortical components to biomechanical behaviour of human vertebrae: an ex vivo study. J. Bone Miner. Res. 25, 356–3561 (2010)
95. Schaffler, M.B., Choi, K., et al.: Aging and matrix microdamage accumulation in human compact bone. Bone 17, 521–525 (1995)
96. Schuit, S.C.E., van der Klift, M., et al.: Fracture incidence and association with bone mineral density in elderly men and women: the Rotterdam study. Bone 34, 195–202 (2004)
97. Silva, M.J., Gibson, L.J.: Modeling the mechanical behavior of vertebral trabecular bone: effects of age-related changes in microstructure. Bone 21, 191–199 (1997)
98. Simpson, E.K., Parkinson, I.H., et al.: Intervertebral disc disorganisation is related to trabecular bone architecture in the lumbar spine. J. Bone Miner. Res. 16, 681–687 (2001)
99. Sornay-Rendu, E., Boutroy, S., et al.: Cortical and trabevular architecture are altered in postmenopausal women with fractures. Osteoporos. Int. 20, 1291–1297 (2009)
100. Stauber, M., Muller, R.: Age-related changes in trabecular bone microstructures: global and local morphometry. Osteoporos. Int. 17, 616–626 (2006)
101. Stauber, M., Muller, R.: Volumetric spatial decomposition of trabecular bone into rods and plates—a new method for local bone morphometry. Bone 38, 475–484 (2006)
102. Stauber, M., Rapillard, L., et al.: Importance of individual rods and plates in the assessment of bone quality and their contribution to the bone stiffness. J. Bone Miner. Res. 21, 586–595 (2006)
103. Szulc, P., Kaufman, J.M., et al.: Biochemical assessment of bone turnover in men. Osteoporos. Int. 18, 1451–1461 (2007)
104. Thomsen, J.S., Ebbesen, E.N., et al.: Static histomorphometry of human iliac crest and vertebral trabecular bone: a comparative study. Bone 30, 267–274 (2002)
105. Townsend, P.R., Rose, R.M., et al.: Buckling studies of single human trabeculae. J. Biomech. 8, 199–201 (1975)
106. Tsangari, H., Findlay, D.M., et al.: Structural and remodeling indices in the cancellous bone of the proximal femur across adulthood. Bone 40(1), 211–217 (2006)
107. van der Linden, J.C., Homminga, J., et al.: Mechanical consequences of bone loss in cancellous bone. J. Bone Miner. Res. 16, 457–465 (2001)
108. van Staa, T.P., Dennison, E.M., et al.: Epidemiology of fractures in England and Wales. Bone 29, 517–522 (2001)
109. Wang, Q., Seeman, E.: Skeletal growth and peak bone strength. Best Pract. Res. Clin. Endocrinol. Metab. 22, 687–700 (2008)
110. Wegrzyn, J., Roux, J.P., et al.: Role of trabecular microarchitecture and its heterogeneity parameters in the mechanical behavior of ex vivo human L3 vertebrae. J. Bone Miner. Res. 25, 2324–2331 (2010)
111. Weinstein, R.S., Hutson, M.S.: Decreased trabecular width and increased trabecular spacing contribute to bone loss with aging. Bone 8, 137–142 (1987)
112. Whitehouse, W.J.: The quantitative morphology of anisotropic trabecular bone. J. Microsc. 101, 153–168 (1974)
113. Yeni, Y.N., Zinno M.J., et al.: Variability of trabecular microstructure is age-, gender-, race-and anatomic site-dependent and affects stiffness and stress distribution properties of human vertebral cancellous bone. Bone 49, 886–894 (2011)