Abstract
Summary
Age-related changes of vertebra and iliac crest 3D microstructure were investigated, and we showed that they were in general similar. The 95th percentile of vertebral trabecular thickness distribution increased with age for women. Surprisingly, vertebral and iliac crest bone microstructure was only weakly correlated (r = 0.38 to 0.75), despite the overall similar age-related changes.
Introduction
The purposes of the study were to determine the age-related changes in iliac and vertebral bone microstructure for women and men over a large age range and to investigate the relationship between the bone microstructure at these skeletal sites.
Methods
Matched sets of transiliac crest bone biopsies and lumbar vertebral body (L2) specimens from 41 women (19–96 years) and 39 men (23–95 years) were micro-computed tomography (μCT) scanned, and the 3D microstructure was quantified.
Results
For both women and men, bone volume per total volume (BV/TV), connectivity density (CD), and trabecular number (Tb.N) decreased significantly, while structure model index (SMI) and trabecular separation (Tb.Sp) increased significantly with age at either skeletal site. Vertebral trabecular thickness (Tb.Th) was independent of age for both women and men, while iliac Tb.Th decreased significantly with age for men, but not for women. In general, the vertebral and iliac age-related changes were similar. The 95th percentile of the Tb.Th distribution increased significantly with age for women but was independent of age for men at the vertebral body, while it was independent of age for either sex at the iliac crest. The Tb.Th probability density functions at the two skeletal sites became significantly more similar with age for women, but not for men. The microstructural parameters at the iliac crest and the vertebral bodies were only moderately correlated from r = 0.38 for SMI in women to r = 0.75 for Tb.Sp in men.
Conclusion
Age-related changes in vertebral and iliac bone microstructure were in general similar. The iliac and vertebral Tb.Th distributions became more similar with age for women. Despite the overall similar age-related changes in trabecular bone microstructure, the vertebral and iliac bone microstructural measures were only weakly correlated (r = 0.38 to 0.75).
Similar content being viewed by others
References
Ulrich D, van Rietbergen B, Laib A, Rüegsegger P (1999) The ability of three-dimensional structural indices to reflect mechanical aspects of trabecular bone. Bone 25:55–60
Zhou B, Sherry Liu X, Wang J, Lucas Lu X, Fields AJ, Edward Guo X (2014) Dependence of mechanical properties of trabecular bone on plate-rod microstructure determined by individual trabecula segmentation (ITS). J Biomech 47:702–708
Stauber M, Rapillard L, van Lenthe GH, Zysset P, Müller R (2006) Importance of individual rods and plates in the assessment of bone quality and their contribution to bone stiffness. J Bone Miner Res 21:586–595
Graeff C, Marin F, Petto H, Kayser O, Reisinger A, Peña J, Zysset P, Glüer CC (2013) High resolution quantitative computed tomography-based assessment of trabecular microstructure and strength estimates by finite-element analysis of the spine, but not DXA, reflects vertebral fracture status in men with glucocorticoid-induced osteoporosis. Bone 52:568–577
Ito M, Ikeda K, Nishiguchi M, Shindo H, Uetani M, Hosoi T, Orimo H (2005) Multi-detector row CT imaging of vertebral microstructure for evaluation of fracture risk. J Bone Miner Res 20:1828–1836
Glüer CC, Marin F, Ringe JD, Hawkins F, Möricke R, Papaioannu N, Farahmand P, Minisola S, Martínez G, Nolla JM, Niedhart C, Guañabens N, Nuti R, Martín-Mola E, Thomasius F, Kapetanos G, Peña J, Graeff C, Petto H, Sanz B, Reisinger A, Zysset PK (2013) Comparative effects of teriparatide and risedronate in glucocorticoid-induced osteoporosis in men: 18-month results of the EuroGIOPs trial. J Bone Miner Res 28:1355–1368
Recker RR (2013) Bone biopsy and histomorphometry in clinical practice. In: Rosen CJ (ed) Primer on the metabolic bone diseases and disorders of mineral metabolism. Wiley-Blackwell, pp 307–316
O'Neill TW, Felsenberg D, Varlow J, Cooper C, Kanis JA, Silman AJ (1996) The prevalence of vertebral deformity in european men and women: the European Vertebral Osteoporosis Study. J Bone Miner Res 11:1010–1018
Amling M, Grote HJ, Pösl M, Hahn M, Delling G (1994) Polyostotic heterogeneity of the spine in osteoporosis. Quantitative analysis and three-dimensional morphology. Bone Miner 27:193–208
Dempster DW, Ferguson-Pell MW, Mellish RWE, Cochran GVB, Xie F, Fey C, Horbert W, Parisien M, Lindsay R (1993) Relationships between bone structure in the iliac crest and bone structure and strength in the lumbar spine. Osteoporos Int 3:90–96
Amling M, Herden S, Pösl M, Hahn M, Ritzel H, Delling G (1996) 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
Thomsen JS, Ebbesen EN, Mosekilde L (2002) Static histomorphometry of human iliac crest and vertebral trabecular bone: a comparative study. Bone 30:267–274
Mosekilde L, Mosekilde L (1988) Iliac crest trabecular bone volume as predictor for vertebral compressive strength, ash density and trabecular bone volume in normal individuals. Bone 9:195–199
Day JS, Ding M, Odgaard A, Sumner DR, Hvid I, Weinans H (2000) Parallel plate model for trabecular bone exhibits volume fraction-dependent bias. Bone 27:715–720
Hildebrand T, Laib A, Müller R, Dequeker J, Rügsegger P (1999) Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res 14:1167–1174
Thomsen JS, Laib A, Koller B, Prohaska S, Mosekilde L, Gowin W (2005) Stereological measures of trabecular bone structure: comparison of 3D micro computed tomography with 2D histological sections in human proximal tibial bone biopsies. J Microsc 218:171–179
Feldkamp LA, Goldstein SA, Parfitt AM, Jesion G, Kleerekoper M (1989) The direct examination of three-dimensional bone architecture in vitro by computed tomography. J Bone Miner Res 4:3–11
Hildebrand T, Rügsegger P (1997) A new method for the model-independent assessment of thickness in three-dimensional images. J Microsc 185:67–75
Lochmüller EM, Matsuura M, Bauer J, Hitzl W, Link TM, Müller R, Eckstein F (2008) Site-specific deterioration of trabecular bone architecture in men and women with advancing age. J Bone Miner Res 23:1964–1973
Eckstein F, Matsuura M, Kuhn V, Priemel M, Müller R, Link TM, Lochmüller EM (2007) Sex differences of human trabecular bone microstructure in aging are site-dependent. J Bone Miner Res 22:817–824
Borah B, Dufresne TE, Ritman EL, Jorgensen SM, Liu S, Chmielewski PA, Phipps RJ, Zhou X, Sibonga JD, Turner RT (2006) Long-term risedronate treatment normalizes mineralization and continues to preserve trabecular architecture: sequential triple biopsy studies with micro-computed tomography. Bone 39:345–352
Akhter MP, Lappe JM, Davies KM, Recker RR (2007) Transmenopausal changes in the trabecular bone structure. Bone 41:111–116
Sikjaer T, Rejnmark L, Thomsen JS, Tietze A, Brüel A, Andersen G, Mosekilde L (2012) Changes in 3-dimensional bone structure indices in hypoparathyroid patients treated with PTH(1–84): a randomized controlled study. J Bone Miner Res 27:781–788
Ebbesen EN, Thomsen JS, Beck-Nielsen H, Nepper-Rasmussen HJ, Mosekilde L (1999) Lumbar vertebral body compressive strength evaluated by dual-energy X-ray absorptiometry, quantitative computed tomography, and ashing. Bone 25:713–724
Ebbesen EN, Thomsen JS, Beck-Nielsen H, Nepper-Rasmussen HJ, Mosekilde L (1999) Age- and gender-related differences in vertebral bone mass, density, and strength. J Bone Miner Res 14:1394–1403
Thomsen JS, Ebbesen EN, Mosekilde L (2002) Age-related differences between thinning of horizontal and vertical trabeculae in human lumbar bone as assessed by a new computerized method. Bone 31:136–142
Thomsen JS, Niklassen AS, Ebbesen EN, Brüel A (2013) Age-related changes of vertical and horizontal lumbar vertebral trabecular 3D bone microstructure is different in women and men. Bone 57:47–55
Ebbesen EN, Thomsen JS, Beck-Nielsen H, Nepper-Rasmussen HJ, Mosekilde L (1998) Vertebral bone density evaluated by dual-energy X-ray absorptiometry and quantitative computed tomography in vitro. Bone 23:283–290
Thomsen JS, Ebbesen EN, Mosekilde L (2000) A new method of comprehensive static histomorphometry applied on human lumbar vertebral cancellous bone. Bone 27:129–138
Bordier P, Matrajt H, Miravet L, Hioco D (1964) Mesure histologique de la masse et de la résorption des travées osseuses. Pathol Biol (Paris) 12:1238–1243
Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Müller R (2010) Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res 25:1468–1486
Laib A, Rüegsegger P (1999) Comparison of structure extraction methods for in vivo trabecular bone measurements. Comput Med Imaging Graph 23:69–74
Odgaard A, Gundersen HJG (1993) Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. Bone 14:173–182
Hildebrand T, Rügsegger P (1997) Quantification of bone microarchitecture with the structure model index. Comput Methods Biomech Biomed Eng 1:15–23
Thomsen JS, Ebbesen EN, Mosekilde L (1998) Relationships between static histomorphometry and bone strength measurements in human iliac crest bone biopsies. Bone 22:153–163
Clemons TE, Bradley EL Jr (2000) A nonparametric measure of the overlapping coefficient. Comput Stat Data Anal 34:51–61
Inman HF, Bradley EL Jr (1989) The overlapping coefficient as a measure of agreement between probability distributions and point estimation of the overlap of two normal densities. Commun Stat Theory Methods 18:3851–3874
Ostojić Z, Cvijanović O, Bobinac D, Zoričić S, Šoša I, Marić I, Crnčević-Orlić Ž, Mihelić R, Ostojić L, Petrović P (2006) Age-related and gender-related differences between human vertebral and iliac crest bone—a histomorphometric study on the population of the Mediterranean Coast of Croatia. Coll Anthropol 30:49–54
Rehman MTA, Hoyland JA, Denton J, Freemont AJ (1994) Age related histomorphometric changes in bone in normal British men and women. J Clin Pathol 47:529–534
Ebbesen EN, Thomsen JS, Mosekilde L (1997) Nondestructive determination of iliac crest cancellous bone strength by pQCT. Bone 21:535–540
Ballanti P, Bonucci E, Della RC, Milani S, Lo CV, Lo IB (1990) Bone histomorphometric reference values in 88 normal Italian subjects. Bone Miner 11:187–197
Chen H, Shoumura S, Emura S, Bunai Y (2008) Regional variations of vertebral trabecular bone microstructure with age and gender. Osteoporos Int 19:1473–1483
Chappard C, Marchadier A, Benhamou L (2008) Interindividual and intraspecimen variability of 3-D bone microarchitectural parameters in iliac crest biopsies imaged by conventional micro-computed tomography. J Bone Miner Metab 26:506–513
Stauber M, Müller R (2006) Age-related changes in trabecular bone microstructures: global and local morphometry. Osteoporos Int 17:616–626
Dos Reis LM, Batalha JR, Muñoz DR, Borelli A, Correa PH, Carvalho AB, Jorgetti V (2007) Brazilian normal static bone histomorphometry: effects of age, sex, and race. J Bone Miner Metab 25:400–406
Cohen A, Dempster DW, Müller R, Guo XE, Nickolas TL, Liu XS, Zhang XH, Wirth AJ, van Lenthe GH, Kohler T, McMahon DJ, Zhou H, Rubin MR, Bilezikian JP, Lappe JM, Recker RR, Shane E (2010) Assessment of trabecular and cortical architecture and mechanical competence of bone by high-resolution peripheral computed tomography: comparison with transiliac bone biopsy. Osteoporos Int 21:263–273
Thomsen JS, Ebbesen EN, Mosekilde L (2002) Zone-dependent changes in human vertebral trabecular bone: clinical implications. Bone 30:664–669
Acknowledgments
The μCT scanner was donated by the VELUX Foundation. The Helga and Peter Korning Foundation and the A.P. Møller Foundation for the Advancement of Medical Science are acknowledged for financial support of the study.
Conflicts of interest
None.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Thomsen, J.S., Jensen, M.V., Niklassen, A.S. et al. Age-related changes in vertebral and iliac crest 3D bone microstructure—differences and similarities. Osteoporos Int 26, 219–228 (2015). https://doi.org/10.1007/s00198-014-2851-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00198-014-2851-x