Regional, age and gender differences in architectural measures of bone quality and their correlation to bone mechanical competence in the human radius of an elderly population

wbldb

Mueller, Thomas L.¹; van Lenthe, G. Harry^1,2; Stauber, Martin¹; Gratzke, Christian³; Eckstein, Felix⁴; Müller, Ralph¹

Regional, age and gender differences in architectural measures of bone quality and their correlation to bone mechanical competence in the human radius of an elderly population

Bone. November 2009;45(5):882-891

©2009 Elsevier Inc. All rights reserved.

Affiliations

¹Institute for Biomechanics, ETH Zurich, Zurich, Switzerland

²Division of Biomechanics and Engineering Design, K. U. Leuven, Leuven, Belgium

³Institute of Anatomy, Ludwig-Maximilians-University (LMU) Munich, Munich, Germany

⁴Institute of Anatomy and Musculoskeletal Research, Paracelsus Medical University Salzburg, Salzburg, Austria
Abstract

An accurate prediction of bone strength in the human radius is of major interest because distal radius fractures are amongst the most common in humans. The objective of this study was to determine gender and age-related changes in bone morphometry at the radius and how these relate to bone strength. Specifically, our aims were to (i) analyze gender differences to get an insight into different bone quantities and qualities between women and men, (ii) to determine which microarchitectural bone parameters would best correlate with strength, (iii) to find the region of interest for the best assessment of bone strength, and (iv) to determine how loss of bone quality depends on age. Intact right forearms of 164 formalin-fixed cadavers from a high-risk elderly population were imaged with a new generation high-resolution pQCT scanner (HR-pQCT). Morphometric indices were derived for six different regions and were related to failure load as assessed by experimental uniaxial compression testing. Significant gender differences in bone quantity and quality were found that correlated well with measured failure load. The most relevant region to determine failure load based on morphometric indices assessed in this study was located just below the proximal end of the subchondral plate; this region differed from the one measured clinically today. Trends in bone changes with increasing age were found, even though for all morphometric indices the variation between subjects was large in comparison to the observed age-related changes. We conclude that HR-pQCT systems can determine how gender and age-related changes in morphometric parameters relate to bone strength, and that HR-pQCT is a promising tool for the assessment of bone quality in patient populations.
Links

DOI: 10.1016/j.bone.2009.06.031

PubMed: 19615477

WoS: 000271071500008
History

Received: 2008-12-24

Revised: 2009-06-25

Accepted: 2009-06-30

Online: 2009-07-15

Cited Works (36)

Year	Entry
2006	Khosla S, Riggs BL, Atkinson EJ, Oberg AL, McDaniel LJ, Holets M, .Peterson JM, Melton LJ III. Effects of sex and age on bone microstructure at the ultradistal radius: a population-based noninvasive in vivo assessment. J Bone Miner Res. January 2006;21(1):124-131.
1967	Atkinson PJ. Variation in trabecular structure of vertebrae with age. Calcif Tiss Res. December 1967;1(1):24-32.
1966	Chalmers J, Weaver JK. Cancellous bone: its strength and changes with aging and an evaluation of some methods for measuring its mineral content, II: an evaluation of some methods for measuring osteoporosis. J Bone Joint Surg. March 1966;48A(2):299-308.
1995	Riggs BL, Melton LJ III. The worldwide problem of osteoporosis: insights afforded by epidemiology. Bone. November 1995;17(5)(suppl 1):S505-S511.
2008	MacNeil JA, Boyd SK. Bone strength at the distal radius can be estimated from high-resolution peripheral quantitative computed tomography and the finite element method. Bone. June 2008;42(6):1203-1213.
2002	Pistoia W, van Rietbergen B, Lochmüller E-M, Lill CA, Eckstein F, Rüegsegger P. Estimation of distal radius failure load with micro-finite element analysis models based on three-dimensional peripheral quantitative computed tomography images. Bone. June 2002;30(6):842-848.
1967	Dunnill MS, Anderson JA, Whitehead R. Quantitative histological studies on age changes in bone. J Pathol Bacteriol. October 1967;94(2):275-291.
1960	Beck JS, Nordin BEC. Histological assessment of osteoporosis by iliac crest biopsy. J Pathol Bacteriol. 1960;80(2):391-397.
1985	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 Tiss Int. 1985;37(6):594-597.
2005	Boutroy S, Bouxsein ML, Munoz F, Delmas PD. In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab. December 2005;90(12):6508-6515.
1997	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. March 1997;79A(3):421-427.
2002	Ding M, Odgaard A, Linde F, Hvid I. Age-related variations in the microstructure of human tibial cancellous bone. J Orthop Res. May 2002;20(3):615-621.
2008	MacNeil JA, Boyd SK. Improved reproducibility of high-resolution peripheral quantitative computed tomography for measurement of bone quality. Med Eng Phys. July 2008;30(6):792-799.
1987	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(2):79-85.
2007	Eckstein F, Matsuura M, Kuhn V, Priemel M, Müller R, Link TM, Lochmüller E. Sex differences of human trabecular bone microstructure in aging are site‐dependent. J Bone Miner Res. June 2007;22(6):817-824.
1994	Müller R, Hildebrand T, Rüegsegger P. Non-invasive bone biopsy: a new method to analyse and display the three-dimensional structure of trabecular bone. Phys Med Biol. January 1994;39(1):145-164.
1969	Wakamatsu E, Sissons HA. The cancellous bone of the iliac crest. Calcif Tiss Res. December 1969;4(1):147-161.
2007	MacNeil JA, Boyd SK. Accuracy of high-resolution peripheral quantitative computed tomography for measurement of bone quality. Med Eng Phys. December 2007;29(10):1096-1105.
2009	Dalzell N, Kaptoge S, Morris N, Berthier A, Koller B, Braak L, van Rietbergen B, Reeve J. Bone micro-architecture and determinants of strength in the radius and tibia: age-related changes in a population-based study of normal adults measured with high-resolution pQCT. Osteoporos Int. October 2009;20(10):1683-1694.
2009	Mueller TL, Stauber M, Kohler T, Eckstein F, Müller R, van Lenthe GH. Non-invasive bone competence analysis by high-resolution pQCT: an in vitro reproducibility study on structural and mechanical properties at the human radius. Bone. February 2009;44(2):364-371.
2004	Riggs BL, Melton LJ III, Robb RA, Camp JJ, Atkinson EJ, Peterson JM, Rouleau PA, McCollough CH, Bouxsein ML, Khosla S. Population-based study of age and sex differences in bone volumetricdensity, size, geometry, and structure at different skeletal sites. J Bone Miner Res. December 2004;19(12):1945-1954.
1990	Cummings SR, Black DM, Nevitt MC, Browner WS, Cauley JA, Genant HK, Mascioli SR, Scott JC, Seeley DG, Steiger P, Vogt TM; The Study of Osteoporotic Fractures Research Group. Appendicular bone density and age predict hip fracture in women. JAMA. February 2, 1990;263(5):665-668.
1989	Mosekilde L. Sex differences in age-related loss of vertebral trabecular bone mass and structure—biomechanical consequences. Bone. 1989;10(6):425-432.
1999	Laib A, Rüegsegger P. Comparison of structure extraction methods for in vivo trabecular bone measurements. Comput Vis Image Understand. March–April 1999;23(2):69-74.
1983	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. October 1983;72(4):1396-1409.
1988	Bergot C, Laval-Jeantet A-M, Prêteux F, Meunier A. Measurement of anisotropic vertebral trabecular bone loss during aging by quantitative image analysis. Calcif Tiss Int. September 1988;43(3):143-149.
1978	Melsen F, Melsen B, Mosekilde L, Bergmann S. Histomorphometric analysis of normal bone from the iliac crest. Acta Pathol Microbiol Scand. July 1978;86A(1-6):70-81.
2007	MacNeil JA, Boyd SK. Load distribution and the predictive power of morphological indices in the distal radius and tibia by high resolution peripheral quantitative computed tomography. Bone. July 2007;41(1):129-137.
1990	Turner CH, Cowin SC, Rho JY, Ashman RB, Rice JC. The fabric dependence of the orthotropic elastic constants of cancellous bone. J Biomech. 1990;23(6):549-561.
1999	Hildebrand T, Laib A, Müller R, Dequeker J, Rüegsegger P. Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res. July 1999;14(7):1167-1174.
2006	Stauber M, Rapillard L, van Lenthe GH, Zysset P, Müller R. Importance of individual rods and plates in the assessment of bone quality and their contribution to bone stiffness. J Bone Miner Res. April 2006;21(4):586-595.
1987	Weinstein RS, Hutson MS. Decreased trabecular width and increased trabecular spacing contribute to bone loss with aging. Bone. 1987;8(3):137-142.
2008	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. March 2008;23(3):392-399.
2007	Burge R, Dawson‐Hughes B, Solomon DH, Wong JB, King A, Tosteson A. Incidence and economic burden of osteoporosis‐related fractures in the United States, 2005–2025. J Bone Miner Res. March 2007;22(3):465-475.
1960	Trotter M, Broman GE, Peterson RR. Densities of bones of white and Negro skeletons. J Bone Joint Surg. January 1960;42A(1):50-58.
2007	Melton LJ, Riggs BL, van Lenthe GH, Achenbach SJ, Müller R, Bouxsein ML, Amin S, Atkinson EJ, Khosla S. Contribution of in vivo structural measurements and load/strength ratios to the determination of forearm fracture risk in postmenopausal women. J Bone Miner Res. September 2007;22(9):1442-1448.

Cited By (21)

Year	Entry
2021	Hunter RL, Haverfield Z, Agnew AM. Investigation of sex-specific effects on variation in cortical bone morphometrics of the radius. In: Proceedings of the 2021 International IRCOBI Conference on the Biomechanics of Injury. September 8-10, 2021; Online.268-307.
2010	Sode M, Burghardt AJ, Kazakia GJ, Link TM, Majumdar S. Regional variations of gender-specific and age-related differences in trabecular bone structure of the distal radius and tibia. Bone. June 2010;46(6):1652-1660.
2010	Varga P, Pahr DH, Baumbach S, Zysset PK. HR-pQCT based FE analysis of the most distal radius section provides an improved prediction of Colles' fracture load in vitro. Bone. November 2010;47(5):982-988.
2011	Mueller TL, Christen D, Sandercott S, Boyd SK, van Rietbergen B, Eckstein F, Lochmüller E-M, Müller R, van Lenthe GH. Computational finite element bone mechanics accurately predicts mechanical competence in the human radius of an elderly population. Bone. June 1, 2011;48(6):1232-1238.
2014	Ellouz R, Chapurlat R, van Rietbergen B, Christen P, Pialat J-B, Boutroy S. Challenges in longitudinal measurements with HR-pQCT: evaluation of a 3D registration method to improve bone microarchitecture and strength measurement reproducibility. Bone. June 2014;63:147-157.
2015	Nirody JA, Cheng KP, Parrish RM, Burghardt AJ, Majumdar S, Link TM, Kazakia GJ. Spatial distribution of intracortical porosity varies across age and sex. Bone. June 2015;75:88-95.
2022	Revel M, Bermond F, Duboeuf F, Mitton D, Follet H. Influence of loading conditions in finite element analysis assessed by HR–pQCT on ex vivo fracture prediction. Bone. January 2022;154:116206.
2011	Burghardt AJ, Link TM, Majumdar S. High-resolution computed tomography for clinical imaging of bone microarchitecture. Clin Orthop Relat Res. August 2011;469:2179-2193.
2011	Edwards WB, Troy KL. Simulating distal radius fracture strength using biomechanical tests: a modeling study examining the influence of boundary conditions. J Biomech Eng. November 2011;133(11):114501.
2010	Burghardt AJ, Kazakia GJ, Sode M, de Papp AE, Link TM, Majumdar S. A longitudinal HR-pQCT study of alendronate treatment in postmenopausal women with low bone density: relations among density, cortical and trabecular microarchitecture, biomechanics, and bone turnover. J Bone Miner Res. December 2010;25(12):2558-2571.
2010	Stein EM, Liu XS, Nickolas TL, Cohen A, Thomas V, McMahon DJ, Zhang C, Yin PT, Cosman F, Nieves J, Guo XE, Shane E. Abnormal microarchitecture and reduced stiffness at the radius and tibia in postmenopausal women with fractures. J Bone Miner Res. December 2010;25(12):2572-2581.
2011	Szulc P, Boutroy S, Vilayphiou N, Chaitou A, Delmas PD, Chapurlat R. Cross-sectional analysis of the association between fragility fractures and bone microarchitecture in older men: the STRAMBO study. J Bone Miner Res. June 2011;26(6):1358-1367.
2010	Burghardt AJ, Issever AS, Schwartz AV, Davis KA, Masharani U, Majumdar S, Link TM. High-resolution peripheral quantitative computed tomographic imaging of cortical and trabecular bone microarchitecture in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab. 2010;95(11):5045-5055.
2014	Kawalilak CE, Johnston JD, Olszynski WP, Kontulainen SA. Characterizing microarchitectural changes at the distal radius and tibia in postmenopausal women using HR-pQCT. Osteoporos Int. August 2014;25(8):2057-2066.
2017	Bonaretti S, Majumdar S, Lang TF, Khosla S, Burghardt AJ. The comparability of HR-pQCT bone measurements is improved by scanning anatomically standardized regions. Osteoporos Int. July 2017;28(7):2115-2128.
2020	Stuck AK, Schenk D, Zysset P, Bütikofer L, Mathis A, Lippuner K. Reference values and clinical predictors of bone strength for HR-pQCT-based distal radius and tibia strength assessments in women and men. Osteoporos Int. October 2020;31(10):1913-1923.
2010	Müller T. Bioimaging and Biomechanics of Bone Competence and Implant Stability [PhD thesis]. Swiss Federal Institute of Technology Zürich; 2010.
2011	O'Neal JM. The Effects of Aging and Remodeling on Bone Quality and Microdamage [PhD thesis]. Atlanta, GA: Georgia Institute of Technology; August 2011.
2019	Du J. Mechanical Adaptation of Human Trabecular Bone: Experimental and Computational Study [PhD thesis]. Loughborough University; 2019.
2013	Christen P. Deciphering the Secret Message Within Bone Microstructure [PhD thesis]. Eindhoven University of Technology; 2013.
2018	Hosseinitabatabaei S. High-Resolution Peripheral Quantitative Computed Tomography Based Finite Element Modelling of Distal Radius Strength: Assessing Effect of Heterogeneous Material Properties and Scan Site [Master's thesis]. University of Saskatchewan; October 2018.