Bone mechanical properties and changes with osteoporosis

Osterhoff, Georg; Morgan, Elise F.; Shefelbine, Sandra J.; Karim, Lamya; McNamara, Laoise M.; Augat, Peter

Affiliations

¹Division of Orthopaedic Trauma, Department of Orthopaedic Surgery, University of British Columbia, Vancouver, British Columbia, Canada

²Department of Mechanical Engineering, Boston University, Boston, MA 02215, USA

³Department of Mechanical and Industrial Engineering, Northeastern University, Boston, MA 02115, USA

⁴Center for Advanced Orthopedic Studies, Beth Israel Deaconess Medical Center and Department of Orthopedic Surgery, Harvard Medical School, Boston, MA 02215, USA

⁵Centre for Biomechanics Research (BMEC), Department of Biomedical Engineering, NUI Galway, Galway, Republic of Ireland

⁶National Centre for Biomedical Engineering Science (NCBES), NUI Galway, Galway, Republic of Ireland

⁷Institute of Biomechanics, Trauma Center Murnau, Murnau, Germany and Paracelsus Medical University Salzburg, Salzburg, Austria

Abstract and keywords

This review will define the role of collagen and within-bone heterogeneity and elaborate the importance of trabecular and cortical architecture with regard to their effect on the mechanical strength of bone. For each of these factors, the changes seen with osteoporosis and ageing will be described and how they can compromise strength and eventually lead to bone fragility.

Keywords: Bone resorption; Bone loss; Bone fragility; Collagen; Biomechanics

Links

DOI: 10.1016/S0020-1383(16)47003-8

PubMed: 27338221

WoS: 000378348500003

History

Revised: 2016-06-1

Online: 2016-06-20

Cited Works (60)

Year	Entry
1977	Martin RB, Atkinson PJ. Age and sex-related changes in the structure and strength of the human femoral shaft. J Biomech. 1977;10(4):223-231.
1995	Schaffler MB, Choi K, Milgrom C. Aging and matrix microdamage accumulation in human compact bone. Bone. December 1995;17(6):521-525.
2003	Currey JD. Role of collagen and other organics in the mechanical properties of bone. Osteoporos Int. September 2003;14(suppl 5):S29-S36.
1997	Nicholson PHF, Cheng XG, Lowet G, Boonen S, Davie MWJ, Dequeker J, Van der Perre G. Structural and material mechanical properties of human vertebral cancellous bone. Med Eng Phys. October 1997;19(8):729-737.
2000	Whealan KM, Kwak SD, Tedrow JR, Inoue K, Snyder BD. Noninvasive imaging predicts failure load of the spine with simulated osteolytic defects. J Bone Joint Surg. September 2000;82A(9):1240-1251.
1997	Saito M, Marumo K, Fujii K, Ishioka N. Single-column high-performance liquid chromatographic-fluorescence detection of immature, mature, and senescent cross-links of collagen. Anal Ciochem. November 1, 1997;253(1):26-32.
1997	Yeni YN, Brown CU, Wang Z, Norman TL. The influence of bone morphology on fracture toughness of the human femur and tibia. Bone. November 1997;21(4):453-459.
1996	Duey P, Desbois C, Boyce B, Pinerot G, Story B, Dunstan C, Smith E, Bonadioll J, Goldstein S, Gundberg C, Bradley A, Karsenty G. Increased bone formation in osteocalcin-deficient mice. Nature. August 1, 1996;382(6590):448-452.
1977	Carter DR, Hayes WC. Compact bone fatigue damage: a microscopic examination. Clin Orthop Relat Res. September 1977;127:265-274.
1996	Augat P, Reeb H, Claes LE. Prediction of fracture load at different skeletal sites by geometric properties of the cortical shell. J Bone Miner Res. September 1996;11(9):1356-1363.
2001	Crabtree N, Loveridge N, Parker M, Rushton N, Power J, Bell KL, Beck TJ, Reeve J. Intracapsular hip fracture and the region-specific loss of cortical bone: analysis by peripheral quantitative computed tomography. J Bone Miner Res. July 2001;16(7):1318-1328.
1992	Cooper C, Atkinson EJ, O'Fallon WM, Melton JL III. Incidence of clinically diagnosed vertebral fractures: a population‐based study in Rochester, Minnesota, 1985‐1989. J Bone Miner Res. February 1992;7(2):221-227.
1952	Dempster WT, Liddicoat RT. Compact bone as a non-isotropic material. Am J Anat. 1952;91(3):331-362.
1995	McCubbrey DA, Cody DD, Peterson EL, Kuhn JL, Flynn MJ, Goldstein SA. Static and fatigue failure properties of thoracic and lumbar vertebral bodies and their relation to regional density. J Biomech. August 1995;28(8):891-899.
2004	Hong J, Cabe GD, Tedrow JR, Hipp JA, Snyder BD. Failure of trabecular bone with simulated lytic defects can be predicted non-invasively by structural analysis. J Orthop Res. May 2004;22(3):479-486.
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.
2008	Roschger P, Paschalis EP, Fratzl P, Klaushofer K. Bone mineralization density distribution in health and disease. Bone. March 2008;42(3):456-466.
2003	Liebschner MAK, Kopperdahl DL, Rosenberg WS, Keaveny TM. Finite element modeling of the human thoracolumbar spine. Spine. March 15, 2003;28(6):559-565.
2006	Viguet-Carrin S, Garnero P, Delmas PD. The role of collagen in bone strength. Osteoporos Int. March 2006;17(3):319-336.
2003	Ammann P, Rizzoli R. Bone strength and its determinants. Osteoporos Int. March 2003;14(suppl 3):S13-S18.
2001	Wang X, Bank RA, Tekoppele JM, Agrawal CM. The role of collagen in determining bone mechanical properties. J Orthop Res. 2001;19(6):1021-1026.
2000	Gadeleta SJ, Boskey AL, Paschalis E, Carlson C, Menschik F, Baldini T, Peterson M, Rimnac CM. A physical, chemical, and mechanical study of lumbar vertebrae from normal, ovariectomized, and nandrolone decanoate-treated cynomolgus monkeys (macaca fascicularis). Bone. October 2000;27(4):541-550.
2000	Guo XE, Goldstein SA. Vertebral trabecular bone microscopic tissue elastic modulus and hardness do not change in ovariectomized rats. J Orthop Res. March 2000;18(2):333-336.
2009	Holzer G, von Skrbensky G, Holzer LA, Pichl W. Hip fractures and the contribution of cortical versustrabecular bone to femoral neck strength. J Bone Miner Res. March 2009;24(3):468-474.
2007	Hulme PA, Boyd SK, Ferguson SJ. Regional variation in vertebral bone morphology and its contribution to vertebral fracture strength. Bone. December 2007;41(6):946-957.
1999	Oden ZM, Selvitelli DM, Bouxsein ML. Effect of local density changes on the failure load of the proximal femur. J Orthop Res. September 1999;17(5):661-667.
2001	Simpson EK, Parkinson IH, Manthey B, Fazzalari NL. Intervertebral disc disorganization is related to trabecular bone architecture in the lumbar spine. J Bone Miner Res. April 2001;16(4):681-687.
1998	Bailey AJ, Paul RG, Knott L. Mechanisms of maturation and ageing of collagen. Mech Ageing Dev. December 1, 1998;106(1-2):1-56.
2009	Brennan O, Kennedy OD, Lee TC, Rackard SM, O'Brien FJ. Biomechanical properties across trabeculae from the proximal femur of normal and ovariectomised sheep. J Biomech. March 11, 2009;42(4):498-503.
2005	Gong H, Zhang M, Yeung HY, Qin L. Regional variations in microstructural properties of vertebral trabeculae with aging. J Bone Min Metab. March 2005;23(2):174-180.
2001	Banse X, Devogelaer JP, Munting E, Delloye C, Cornu O, Grynpas M. Inhomogeneity of human vertebral cancellous bone: systematic density and structure patterns inside the vertebral body. Bone. 2001;28(5):563-571.
1993	Mizrahi J, Silva MJ, Keaveny TM, Edwards WT, Hayes WC. Finite-element stress analysis of the normal and osteoporotic lumbar vertebral body. Spine. October 15, 1993;18(14):2088-2096.
1994	Bouxsein ML, Myburgh KH, van der Meulen MCH, Lindenberger E, Marcus R. Age-related differences in cross-sectional geometry of the forearm bones in healthy women. Calcif Tiss Int. February 1994;54(2):113-118.
2009	Busse B, Hahn M, Soltau M, Zustin J, Püschel K, Duda GN, Amling M. Increased calcium content and inhomogeneity of mineralization render bone toughness in osteoporosis: mineralization, morphology and biomechanics of human single trabeculae. Bone. December 2009;45(6):1034-1043.
2002	Jaasma MJ, Bayraktar HH, Niebur GL, Keaveny TM. Biomechanical effects of intraspecimen variations in tissue modulus for trabecular bone. J Biomech. 2002;35(2):237-246.
2010	Zebaze RMD, Ghasem-Zadeh A, Bohte A, Iuliano-Burns S, Mirams M, Price RI, Mackie EJ, Seeman E. Intracortical remodelling and porosity in the distal radius and post-mortem femurs of women: a cross-sectional study. Lancet. May 15, 2010;375(9727):1729-1736.
2004	Loveridge N, Power J, Reeve J, Boyde A. Bone mineralization density and femoral neck fragility. Bone. October 2004;35(4):929-941.
2013	Karim L, Tang SY, Sroga GE, Vashishth D. Differences in non-enzymatic glycation and collagen cross-links between human cortical and cancellous bone. Osteoporos Int. September 2013;24(9):2441-2447.
1970	Galante J, Rostoker W, Ray RD. Physical properties of trabecular bone. Calcif Tiss Res. 1970;5(1):236-246.
2002	Wachter NJ, Krischak GD, Mentzel M, Sarkar MR, Ebinger T, Kinz L, Claes L, Augat P. Correlation of bone mineral density with strength and microstructural parameters of cortical bone in vitro. Bone. July 2002;31(1):90-95.
1980	Carter DR, Schwab GH, Spengler DM. Tensile fracture of cancellous bone. Acta Orthop Scand. 1980;51(5):733-741.
2006	Turner CH. Bone strength: current concepts. Annals NY Acad Sci. 2006;1068(1):429-446.
2008	Mittra E, Rubin C, Gruber B, Qin Y-X. Evaluation of trabecular mechanical and microstructural properties in human calcaneal bone of advanced age using mechanical testing, μCT, and DXA. J Biomech. 2008;41(2):368-375.
2006	Saito M, Fujii K, Mori Y, Marumo K. Role of collagen enzymatic and glycation induced cross-links as a determinant of bone quality in spontaneously diabetic WBN/Kob rats. Osteoporos Int. October 2006;17(10):1514-1523.
2003	Crawford RP, Cann CE, Keaveny TM. Finite element models predict in vitro vertebral body compressive strength better than quantitative computed tomography. Bone. 2003;33(4):744-750.
1997	Lang TF, Keyak JH, Heitz MW, Augat P, Liu Y, Mathur A, Genant HK. Volumetric quantitative computed tomography of the proximal femur: precision and relation to bone strength. Bone. July 1997;21(1):101-108.
2007	Kim D-G, Hunt CA, Zauel R, Fyhrie DP, Yeni YN. The effect of regional variations of the trabecular bone properties on the compressive strength of human vertebral bodies. Ann Biomed Eng. November 2007;35(11):1907-1913.
2002	Thomsen JS, Ebbesen EN, Mosekilde L. Zone-dependent changes in human vertebral trabecular bone: clinical implications. Bone. May 2002;30(5):664-669.
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.
2011	Brennan O, Kennedy OD, Lee TC, Rackard SM, O’Brien FJ, McNamara LM. The effects of estrogen deficiency and bisphosphonate treatment on tissue mineralisation and stiffness in an ovine model of osteoporosis. J Biomech. February 3, 2011;44(3):386-390.
2006	McNamara LM, Ederveen AGH, Lyons CG, Price C, Schaffler MB, Weinans H, Prendergast PJ. Strength of cancellous bone trabecular tissue from normal, ovariectomized and drug-treated rats over the course of ageing. Bone. August 2006;39(2):392-400.
1991	Cody DD, Goldstein SA, Flynn MJ, Brown EB. Correlations between vertebral regional bone mineral density (rBMD) and whole bone fracture load. Spine. 1991;16(2):146-154.
2006	Saito M, Fujii K, Soshi S, Tanaka T. Reductions in degree of mineralization and enzymatic collagen cross-links and increases in glycation-induced pentosidine in the femoral neck cortex in cases of femoral neck fracture. Osteoporos Int. July 2006;17(7):986-995.
1976	Burstein AH, Reilly DT, Martens M. Aging of bone tissue: mechanical properties. J Bone Joint Surg. 1976;58A(1):82-86.
2009	Vashishth D. Advanced glycation end-products and bone fractures. IBMS Bonekey. August 2009;6(8):268-278.
1999	Yeh OC, Keaveny TM. Biomechanical effects of intraspecimen variations in trabecular architecture: a three-dimensional finite element study. Bone. August 1999;25(2):223-228.
1995	Knott L, Whitehead CC, Fleming RH, Bailey AJ. Biochemical changes in the collagenous matrix of osteoporotic avian bone. Biochem J. September 15, 1995;310(3):1045-1051.
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.
2006	Saito M, Fujii K, Marumo K. Degree of mineralization-related collagen crosslinking in the femoral neck cancellous bone in cases of hip fracture and controls. Calcif Tiss Int. September 2006;79(3):160-168.
1993	Keaveny TM, Hayes WC. A 20-year perspective on the mechanical properties of trabecular bone. J Biomech Eng. November 1993;115(4B):534-542.

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2021	Li Y, Tseng W-J, de Bakker CMJ, Zhao H, Chung R, Liu XS. Peak trabecular bone microstructure predicts rate of estrogen-deficiency-induced bone loss in rats. Bone. April 2021;145:115862.
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2021	Sahandifar P, Kleiven S. Separate and combined effects of geometrical and mechanical properties changes due to aging on the femoral strength in men and women. Front Mech Eng. May 24, 2021;7:691171.
2022	Buettmann EG, Goldscheitter GM, Hoppock GA, Friedman MA, Suva LJ, Donahue HJ. Similarities between disuse and age-induced bone loss. J Bone Miner Res. August 2022;37(8):1417-1434.
2019	Molino G, Dalpozzi A, Ciapetti G, Lorusso M, Novara C, Cavallo M, Baldini N, Giorgis F, Fiorilli S, Vitale-Brovarone C. Osteoporosis-related variations of trabecular bone properties of proximal human humeral heads at different scale lengths. J Mech Behav Biomed Mater. December 2019;100:103373.
2020	Bokam P, Germaneau A, Rigoard P, Vendeuvre T, Valle V. Evaluation of fracture properties of cancellous bone tissues using digital image correlation/wedge splitting test method. J Mech Behav Biomed Mater. February 2020;102:103469.
2020	Arnold EL, Clement J, Rogers KD, Garcia-Castro F, Greenwood C. The use of μCT and fractal dimension for fracture prediction in osteoporotic individuals. J Mech Behav Biomed Mater. March 2020;103:103585.
2022	Baines AJ, Babazadeh-Naseri A, Dunbar NJ, Lewis VO, Fregly BJ. Bilateral asymmetry of bone density adjacent to pelvic sarcomas: a retrospective study using computed tomography. J Orthop Res. March 2022;40(3):644-653.
2023	Mirzaei M, Jafari R, Allaveisi F, Jafari H, Alavi F. Fracture analysis of healthy and osteoporotic femora using clinical CT images, phantomless densitometry, and linear FE method. J Orthop Res. March 2023;41(3):629-640.
2023	Gupta S, Xiao R, Fainor M, Mauck RL, Smith HE, Gullbrand SE. Level dependent alterations in human facet cartilage mechanics and bone morphometry with spine degeneration. J Orthop Res. March 2023;41(3):674-683.
2023	Mackert GA, Harder M, Harhaus H, Schulte M, Trinler U, Jaeger S, Kneser U, Harhaus L, Wölf C. Validation of a novel testing machine for the investigation of the biomechanical properties of lumbar vertebrae in an osteoporotic rat model. J Orthop Surg Res. March 31, 2023;18:263.
2021	Koudelka P, Kytyr D, Fila T, Sleichrt J, Rada V, Zlamal P, Benes P, Bendova V, Kumpova I, Vopalensky M. A method for evaluation the fatigue microcrack propagation in human cortical bone using differential X-ray computed tomography. Materials. March 11, 2021;14(6):1370.
2020	Jazinizadeh F, Adachi JD, Quenneville CE. Advanced 2D image processing technique to predict hip fracture risk in an older population based on single DXA scans. Osteoporos Int. October 2020;31(10):1925-1933.
2020	Shahriarpour Z, Nasrabadi B, Shariati-Bafghi S-E, Karamati M, Rashidkhani B. Adherence to the dietary approaches to stop hypertension (DASH) dietary pattern and osteoporosis risk in postmenopausal Iranian women. Osteoporos Int. November 2020;31(11):2179-2188.
2020	Jadzic J, Cvetkovic D, Milovanovic P, Tomanovic N, Zivkovic V, Nikolic S, Djuric M, Djonic D. The micro-structural analysis of lumbar vertebrae in alcoholic liver cirrhosis. Osteoporos Int. November 2020;31(11):2209-2217.
2020	Ogurkowska MB, Błaszczyk A. Distribution of Young's modulus at various sampling points in a human lumbar spine vertebral body. Spine J. November 2020;20(11):1861-1875.
2020	Aggleton J. First-Hand Experience: A Methodology for Exploring Bone Architecture [PhD thesis]. Bristol, UK: University of Bristol; January 2020.
2021	Coulombe JC. Diminished Bone Structural Quality in Aging and Microgravity Follow Impairments of the Osteocyte Lacunar-Canalicular System [PhD thesis]. University of Colorado; 2021.
2022	Senwar B. Bone Material Quality, Structure, and Functional Relationships Contribute to Bone Strength and Toughness [Master's thesis]. University of Colorado; 2022.
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2023	Inacio JHV. Application of Virtual Mechanical Testing on Clinical Bone Fractures [PhD thesis]. Lehigh University; January 2023.
2017	Mathavan N. The Anabolic - Anti-Catabolic Paradigm of Augmenting Skeletal Regeneration: A Bone Quality Perspective [PhD thesis]. Lund, Sweden: Lund University; 2017.
2020	Jazinizadeh F. Assessment of Hip Fracture Risk in Older Adults by Considering the Effect of Geometry and Bone Mineral Density Distribution in the Femur Using Single Dual-Energy X-Ray Absorptiometry Scans [PhD thesis]. Hamilton, ON: McMaster University; August 2020.
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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.
2019	Heney AP. Effect of Fatigue-Induced Microdamage on the Compressive Properties of Bovine Trabecular Bone [Master's thesis]. Queen's University; September 2019.
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