Microarchitecture influences microdamage accumulation in human vertebral trabecular bone

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Arlot, Monique E.¹; Burt‐Pichat, Brigitte¹; Roux, Jean‐Paul¹; Vashishth, Deepak^1,2; Bouxsein, Mary L.³; Delmas, Pierre D.¹

Microarchitecture influences microdamage accumulation in human vertebral trabecular bone

J Bone Miner Res. 2008;23(10):1613-1618

Affiliations

¹Inserm Research Unit 831, Université de Lyon, Lyon, France

²Department of Biomedical Engineering, Center of Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, New York, USA

³Beth Israel Deaconess Medical Center, Boston, Massachusetts, USA
Abstract and keywords

It has been suggested that accumulation of microdamage with age contributes to skeletal fragility. However, data on the age-related increase in microdamage and the association between microdamage and trabecular microarchitecture in human vertebral cancellous bone are limited. We quantified microdamage in cancellous bone from human lumbar (L2) vertebral bodies obtained from 23 donors 54–93 yr of age (8 men and 15 women). Damage was measured using histologic techniques of sequential labeling with chelating agents and was related to 3D microarchitecture, as assessed by high-resolution μCT. There were no significant differences between sexes, although women tended to have a higher microcrack density (Cr.Dn) than men. Cr.Dn increased exponentially with age (r = 0.65, p < 0.001) and was correlated with bone volume fraction (BV/TV; r = −0.55; p < 0.01), trabecular number (Tb.N; r = −0.56 p = 0.008), structure model index (SMI; r = 0.59; p = 0.005), and trabecular separation (Tb.Sp; r = 0.59; p < 0.009). All architecture parameters were strongly correlated with each other and with BV/TV. Stepwise regression showed that SMI was the best predictor of microdamage, explaining 35% of the variance in Cr.Dn and 20% of the variance in diffuse damage accumulation. In addition, microcrack length was significantly greater in the highest versus lowest tertiles of SMI. In conclusion, in human vertebral cancellous bone, microdamage increases with age and is associated with low BV/TV and a rod-like trabecular architecture.

Keywords: microdamage; microcrack; human; vertebral; trabecular bone; microarchitecture; osteoporosis
Links

DOI: 10.1359/jbmr.080517

PubMed: 18518771

WoS: 000259686100011

Cited Works (41)

Year	Entry
1998	Yeni YN, Brown CU, Norman TL. Influence of bone composition and apparent density on fracture toughness of the human femur and tibia. Bone. January 1998;22(1):79-84.
1993	Snyder BD, Piazza S, Edwards WT, Hayes WC. Role of trabecular morphology in the etiology of age-related vertebral fractures. Calcif Tiss Int. February 1993;53(suppl 1):S14-S22.
1997	Griffin LV, Gibeling JC, Martin RB, Gibson VA, Stover SM. Model of flexural fatigue damage accumulation for cortical bone. J Orthop Res. July 1997;15(4):607-614.
2006	Bevill G, Eswaran SK, Gupta A, Papadopoulos P, Keaveny TM. Influence of bone volume fraction and architecture on computed large-deformation failure mechanisms in human trabecular bone. Bone. December 2006;39(6):1218-1225.
2005	Nagaraja S, Couse TL, Guldberg RE. Trabecular bone microdamage and microstructural stresses under uniaxial compression. J Biomech. 2005;38(4):707-716.
2003	Ciarelli TE, Fyhrie DP, Parfitt AM. Effects of vertebral bone fragility and bone formation rate on the mineralization levels of cancellous bone from white females. Bone. March 2003;32(3):311-315.
2006	Nazarian A, Stauber M, Zurakowski D, Snyder BD, Müller R. The interaction of microstructure and volume fraction in predicting failure in cancellous bone. Bone. December 2006;39(6):1196-1202.
1997	Burr DB, Forwood MR, Fyhrie DP, Martin RB, Schaffler MB, Turner CH. Bone microdamage and skeletal fragility in osteoporotic and stress fractures. J Bone Miner Res. January 1997;12(1):6-15.
2006	Stauber M, Müller R. Volumetric spatial decomposition of trabecular bone into rods and plates: a new method for local bone morphometry. Bone. 2006;38(4):475-484.
1985	Burr DB, Martin RB, Schaffler MB, Radin EL. Bone remodeling in response to in vivo fatigue microdamage. J Biomech. 1985;18(3):189-200.
2007	Nagaraja S, Lin ASP, Guldberg RE. Age-related changes in trabecular bone microdamage initiation. Bone. April 2007;40(4):973-980.
1997	Hildebrand T, Rüegsegger P. Quantification of bone microarchitecture with the structure model index. Comput Methods Prog Biomed. 1997;1(1):15-23.
2003	Lee TC, Mohsin S, Taylor D, Parkesh R, Gunnlaugsson T, O'Brien FJ, Giehl M, Gowin W. Detecting microdamage in bone. J Anat. August 2003;203(2):161-172.
2007	Vashishth D. Hierarchy of bone microdamage at multiple length scales. Int J Fatigue. June 2007;29(6):1024-1033.
1996	Pattin CA, Caler WE, Carter DR. Cyclic mechanical property degradation during fatigue loading of cortical bone. J Biomech. January 1996;29(1):69-79.
2006	Winwood K, Zioupos P, Currey JD, Cotton JR, Taylor M. Strain patterns during tensile, compressive, and shear fatigue of human cortical bone and implications for bone biomechanics. J Biomed Mater Res. November 2006;A79(2):289-297.
1998	Boyce TM, Fyhrie DP, Glotkowski MC, Radin EL, Schaffler MB. Damage type and strain mode associations in human compact bone bending fatigue. J Orthop Res. May 1998;16(3):322-329.
1995	Schaffler MB, Choi K, Milgrom C. Aging and matrix microdamage accumulation in human compact bone. Bone. December 1995;17(6):521-525.
2006	Gong H, Zhang M, Qin L, Lee KKH, Guo X, Shi S-Q. Regional variations in microstructural properties of vertebral trabeculae with structural groups. Spine. January 2006;31(1):24-32.
2004	Siris ES, Chen Y-T, Abbott TA, Barrett-Connor E, Miller PD, Wehren LE, Berger ML. Bone mineral density thresholds for pharmacological intervention to prevent fractures. Arch Intern Med. May 24, 2004;164(10):1108-1112.
2000	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(1):32-40.
2006	Diab T, Condo KW, Burr DB, Vashishth D. Age-related change in the damage morphology of human cortical bone and its role in bone fragility. Bone. March 2006;38(3):427-431.
2007	Diab T, Vashishth D. Morphology, localization and accumulation of in vivo microdamage in human cortical bone. Bone. March 2007;40(3):612-618.
1996	Wenzel TE, Schaffler MB, Fyhrie DP. In vivo trabecular microcracks in human vertebral bone. Bone. August 1996;19(2):89-95.
2005	Diab T, Vashishth D. Effects of damage morphology on cortical bone fragility. Bone. July 2005;37(1):96-102.
1998	Fazzalari NL, Forwood MR, Manthey BA, Smith K, Kolesik P. Three-dimensional confocal images of microdamage in cancellous bone. Bone. October 1998;23(4):373-378.
2007	Glatt V, Canalis E, Stadmeyer L, Bouxsein ML. Age‐related changes in trabecular architecture differ in female and male C57BL/6J mice. J Bone Miner Res. August 2007;22(8):1197-1207.
1978	Ridler TW, Calvard S. Picture thresholding using an iterative selection method. IEEE Trans Sys Man Cyb. 1978;8(8):630-632.
1998	Fazzalari NL, Forwood MR, Smith K, Manthey BA, Herreen P. Assessment of cancellous bone quality in severe osteoarthrosis: bone mineral density, mechanics, and microdamage. Bone. 1998;22(4):381-388.
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.
2005	Sornay-Rendu E, Munoz F, Garnero P, Duboeuf F, Delmas PD. Identification of osteopenic women at high risk of fracture: the OFELY study. J Bone Miner Res. October 2005;20(10):1813-1819.
1997	Norman TL, Wang Z. Microdamage of human cortical bone: incidence and morphology in long bones. Bone. April 1997;20(4):375-379.
1998	Bentolila V, Boyce TM, Fyhrie DP, Drumb R, Skerry TM, Schaffler MB. Intracortical remodeling in adult rat long bones after fatigue loading. Bone. September 1998;23(3):275-281.
1997	Hildebrand T, Rüegsegger P. A new method for the model-independent assessment of thickness in three-dimensional images. J Microsc (Oxford). 1997;185(1):67-75.
2006	Seeman E, Delmas PD. Bone quality: the material and structural basis of bone strength and fragility. NEJM. May 25, 2006;354(21):2250-2261.
2007	Chapurlat RD, Arlot M, Burt‐Pichat B, Chavassieux P, Roux JP, Portero‐Muzy N, Delmas PD. Microcrack frequency and bone remodeling in postmenopausal osteoporotic women on long‐term bisphosphonates: a bone biopsy study. J Bone Miner Res. October 2007;22(10):1502-1509.
1967	Bell GH, Dunbar O, Beck JS, Gibb A. Variations in strength of vertebrae with age and their relation to osteoporosis. Calcif Tiss Res. 1967;1(1):75-86.
2000	Vashishth D, Koontz J, Qiu SJ, Lundin-Cannon D, Yeni YN, Schaffler MB, Fyhrie DP. In vivo diffuse damage in human vertebral trabecular bone. Bone. February 2000;26(2):147-152.
1995	Burr DB, Hooser M. Alterations to the en bloc basic fuchsin staining protocol for the demonstration of microdamage produced in vivo. Bone. October 1995;17(4):431-433.
2006	Johnell O, Kanis JA. An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int. December 2006;17(12):1726-1733.
1998	Burr DB, Turner CH, Naick P, Forwood MR, Ambrosius W, Hasan MS, Pidaparti R. Does microdamage accumulation affect the mechanical properties of bone? J Biomech. April 1998;31(4):337-345.

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Year	Entry
2009	Garrison JG, Slaboch CL, Niebur GL. Density and architecture have greater effects on the toughness of trabecular bone than damage. Bone. May 2009;44(5):924-929.
2010	Viguet-Carrin S, Follet H, Gineyts E, Roux JP, Munoz F, Chapurlat R, Delmas PD, Bouxsein ML. Association between collagen cross-links and trabecular microarchitecture properties of human vertebral bone. Bone. February 2010;46(2):342-347.
2010	Shi X, Liu XS, Wang X, Guo XE, Niebur GL. Effects of trabecular type and orientation on microdamage susceptibility in trabecular bone. Bone. May 2010;46(5):1260-1266.
2020	McKay M, Jackman TM, Hussein AI, Guermazi A, Liu J, Morgan EF. Association of vertebral endplate microstructure with bone strength in men and women. Bone. February 2020;131:115147.
2012	Sroga GE, Vashishth D. Effects of bone matrix proteins on fracture and fragility in osteoporosis. Curr Osteoporos Rep. June 2012;10(2):141-150.
2015	Salmon PL, Ohlsson C, Shefelbine SJ, Doube M. Structure model index does not measure rods and plates in trabecular bone. Front Endocrinol (Lausanne). 2015;6:162.
2009	Mc Donnell P, Harrison N, Liebschner MAK, Mc Hugh PE. Simulation of vertebral trabecular bone loss using voxel finite element analysis. J Biomech. 2009;42(16):2789-2796.
2010	Shi X, Liu XS, Wang X, Guo XE, Niebur GL. Type and orientation of yielded trabeculae during overloading of trabecular bone along orthogonal directions. J Biomech. September 17, 2010;43(13):2460-2466.
2011	Green JO, Wang J, Diab T, Vidakovic B, Guldberg RE. Age-related differences in the morphology of microdamage propagation in trabecular bone. J Biomech. October 13, 2011;44(15):2659-2666.
2011	Garrison JG, Gargac JA, Niebur GL. Shear strength and toughness of trabecular bone are more sensitive to density than damage. J Biomech. November 10, 2011;44(16):2747-2754.
2012	Sanyal A, Gupta A, Bayraktar HH, Kwon RY, Keaveny TM. Shear strength behavior of human trabecular bone. J Biomech. October 11, 2012;45(15):2513-2519.
2014	Lambers FM, Bouman AR, Tkachenko EV, Keaveny TM, Hernandez CJ. The effects of tensile-compressive loading mode and microarchitecture on microdamage in human vertebral cancellous bone. J Biomech. November 28, 2014;47(15):3605-3612.
2020	Huang T, Tworoger SS, Redline S, Curhan GC, Paik JM. Obstructive sleep apnea and risk for incident vertebral and hip fracture in women. J Bone Miner Res. November 2020;35(11):2143-2150.
2022	Sacher SE, Hunt HB, Lekkala S, Lopez KA, Potts J, Heilbronner AK, Stein EM, Hernandez CJ, Donnelly E. Distributions of microdamage are altered between trabecular rods and plates in cancellous bone from men with type 2 diabetes mellitus. J Bone Miner Res. April 2022;37(4):740-752.
2020	Acciaioli A, Falco L, Balean M. Measurement of apparent mechanical properties of trabecular bone tissue: accuracy and limitation of digital image correlation technique. J Mech Behav Biomed Mater. March 2020;103:103542.
2011	Karim L, Vashishth D. Role of trabecular microarchitecture in the formation, accumulation, and morphology of microdamage in human cancellous bone. J Orthop Res. November 2011;29(11):1739-1744.
2011	Larrue A, Rattner A, Peter Z-A, Olivier C, Laroche N, Vico L, Peyrin F. Synchrotron radiation micro-CT at the micrometer scale for the analysis of the three-dimensional morphology of microcracks in human trabecular bone. PLoS One. 2011;6(7):e21297.
2013	Lambers FM, Bouman AR, Rimnac CM, Hernandez CJ. Microdamage caused by fatigue loading in human cancellous bone: relationship to reductions in bone biomechanical performance. PLoS One. December 2013;8(12):e83662.
2018	Torres AM. Fatigue Behavior of Cancellous Bone, Microdamage Accumulation, and Biologically Inspired Cellular Solids [PhD thesis]. Ithaca, NY: Cornell University; August 2018.
2021	Sacher S. Characterization of Trabecular Morphology, Microdamage Accumulation, and Collagen Crosslinking in Bone Tissue from Individuals With Type II Diabetes Mellitus [Master's thesis]. Ithaca, NY: Cornell University; May 2021.
2014	Seref-Ferlengez Z. Diffused Microdamage in Bone Vivo: Structural and Mechanical Bases of Repair [PhD thesis]. New York, NY: The City University of New York; 2014.
2010	Wang JL. Effects of Aging and Remodeling on Bone Microdamage Formation [Master's thesis]. Atlanta, GA: Georgia Institute of Technology; December 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.
2010	Shi X. Effects of Architecture on Microdamage Susceptibility in Trabecular Bone [PhD thesis]. University of Notre Dame; April 2010.
2011	Garrison JG. The Relative Importance of Stress State, Microarchitecture, and Damage Burden in the Failure Behavior of Trabecular Bone [PhD thesis]. University of Notre Dame; April 2011.
2011	Wu Z. Measures of Bone Quality and Their Relationship to Bone Mechanical Properties [PhD thesis]. University of Notre Dame; December 2011.
2017	Kreipke TC. Structural, Mechanical, and Biological Relationships of Trabecular Bone in Osteoporosis [PhD thesis]. University of Notre Dame; April 2017.
2022	Khakpour S. Multi-Component Finite Element Analysis of Low- Energy Acetabular Fracture: Computational Study of Pelvic Girdle Fracture Mechanism [PhD thesis]. University of Oulu; 2022.
2011	Karim L. The Biomolecular Basis of Bone Fracture [PhD thesis]. Troy, NY: Rensselaer Polytechnic Institute; November 2011.
2013	Sanyal A. Bone Strength Multi-Axial Behavior: Volume Fraction, Anisotropy and Microarchitecture [PhD thesis]. Berkeley, CA: Berkeley, University of California; 2013.
2022	Rezaee T. Effect of Clinically Relevant Alterations of Mineral and Protein on Bone Biomechanics [PhD thesis]. University of Massachusetts at Dartmouth; May 2022.