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Carter, Dennis R.
1
;
Hayes, Wilson C.
2
Compact bone fatigue damage: a microscopic examination
Clin Orthop Relat Res
. September 1977;127:265-274
Affiliations
1
Department of Orthopaedics and Center for Bioengineering, University of Washington School of Medicine, Seattle, Washington 98195.
2
Department of Orthopaedic Surgery, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19174
Links
DOI:
10.1097/00003086-197709000-00039
PubMed:
912990
WoS:
A1977DV75200039
Ovid:
00003086-197709000-00039
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1975
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Acta Orthop Scand
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1972
Chamay A, Tschantz P. Mechanical influences in bone remodeling: experimental research on Wolff's law.
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1976
Wright TM, Hayes WC. Tensile testing of bone over a wide range of strain rates: effects of strain rate, microstructure and density.
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1977
Carter DR, Hayes WC. Compact bone fatigue damage, I: residual strength and stiffness.
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1966
Sedlin ED, Hirsch C. Factors affecting the determination of the physical properties of femoral cortical bone.
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1974
Freeman MAR, Todd RC, Pirie CJ. The role of fatigue in the pathogenesis of senile femoral neck fractures.
J Bone Joint Surg
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1976
Carter DR, Hayes WC. Bone compressive strength: the influence of density and strain rate.
Science
. September 10, 1976;194(4270):1174-1176.
1976
Wright TM, Hayes WC. The fracture mechanics of fatigue crack propagation in compact bone.
J Biomed Mater Res
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1974
Reilly DT.
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1973
Evans FG.
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1962
Currey JD. Stress concentrations in bone.
Q J Microsc Sci
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1975
Reilly DT, Burstein AH. The elastic and ultimate properties of compact bone tissue.
J Biomech
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1976
Carter DR.
The Fatigue Behavior of Compact Bone
[PhD thesis]. Stanford University; 1976.
1976
Carter DR, Hayes WC, Schurman DJ. Fatigue life of compact bone, II: effects of microstructure and density.
J Biomech
. 1976;9(4):211-218.
1976
Carter DR, Hayes WC. Fatigue life of compact bone, I: effects of stress amplitude, temperature and density.
J Biomech
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1962
Bassett CAL, Becker RO. Generation of electric potentials by bone in response to mechanical stress.
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1971
Griffiths WEG, Swanson SAV, Freeman MAR. Experimental fatigue fracture of the human cadaveric femoral neck.
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1971
Swanson SAV, Freeman MAR, Day WH. The fatigue properties of human cortical bone.
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1974
Gray RJ, Korbacher GK. Compressive fatigue behaviour of bovine compact bone.
J Biomech
. May 1974;7(3):287-292.
1972
Burstein AH, Currey JD, Frankel VH, Reilly DT. The ultimate properties of bone tissue: the effects of yielding.
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Cited By (150)
Year
Entry
1996
Egerer AK, Saha S, McMillan PJ, Rivera J. Morphology of the cement line in human bone and its relationship to bone strength. In:
Proceedings of the 15th Southern Biomedical Engineering Conference
. March 29-31, 1996; Dayton, OH.7-10.
2011
Wang R, Gupta HS. Deformation and fracture mechanisms of bone and nacre.
Ann Rev Mater Res
. August 2011;41:41-73.
1981
Carter DR, Harris WH, Vasu R, Caler WE. The mechanical and biological response of cortical bone to in vivo strain histories. In: Cowin SC, ed.
Mechanical Properties of Bone
. The Joint ASME-ASCE Applied Mechnics, Fluids Engineering and Bioengineering Conference; June 22-24, 1981; Boulder, CO. New York, NY: American Society of Mechical Engineers; 1981:81-92.
1986
Frost HM.
Intermediary Organization of the Skeleton
. Vols. 1-2. Boca Raton, FL: CRC Press; 1986.
2001
Turner CH, Burr DB. Experimental techniques for bone mechanics. In: Cowin SC, ed.
Bone Mechanics Handbook
. 2nd ed. Boca Raton, FL: CRC Press; 2001:7-1–7-35.
2002
Currey JD.
Bones: Structure and Mechanics
. Princeton, NJ: Princeton University Press; 2002.
1998
Martin RB, Burr DB, Sharkey NA.
Skeletal Tissue Mechanics
. New York, NY: Springer-Verlag; 1998.
1981
Carter DR, Caler WE, Spengler DM, Frankel VH. Fatigue behavior of adult cortical bone: the influence of mean strain and strain range.
Acta Orthop Scand
. 1981;52(5):481-490.
1987
Schaffler MB, Burr DB, Frederickson RG. Morphology of the osteonal cement line in human bone.
Anat Rec
. March 1987;217(3):223-228.
2005
Skedros JG, Holmes JL, Vajda EG, Bloebaum AD. Cement lines of secondary osteons in human bone are not mineral‐deficient: new data in a historical perspective.
Anat Rec
. September 2005;286A(1):781-803.
2006
Robling AG, Castillo AB, Turner CH. Biomechanical and molecular regulation of bone remodeling.
Annu Rev Biomed Eng
. 2006;8:455-498.
1993
Mori S, Burr DB. Increased intracortical remodeling following fatigue damage.
Bone
. March–April 1993;14(2):103-109.
1993
Turner CH, Burr DB. Basic biomechanical measurements of bone: a tutorial.
Bone
. 1993;14(4):595-608.
1994
Schaffler MB, Pitchford WC, Choi K, Riddle JM. Examination of compact bone microdamage using back-scattered electron microscopy.
Bone
. September–October 1994;15(5):483-488.
1995
Schaffler MB, Choi K, Milgrom C. Aging and matrix microdamage accumulation in human compact bone.
Bone
. December 1995;17(6):521-525.
1996
Martin RB, Gibson VA, Stover SM, Gibeling JC, Griffins LV. Osteonal structure in the equine third metacarpus.
Bone
. February 1996;18(2):165-171.
1997
Norman TL, Wang Z. Microdamage of human cortical bone: incidence and morphology in long bones.
Bone
. April 1997;20(4):375-379.
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.
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.
1998
Norman TL, Yeni YN, Brown CU, Wang Z. Influence of microdamage on fracture toughness of the human femur and tibia.
Bone
. September 1998;23(3):303-306.
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.
2004
Nalla RK, Kruzic JJ, Ritchie RO. On the origin of the toughness of mineralized tissue: microcracking or crack bridging?
Bone
. May 2004;34(5):790-798.
2007
Ebacher V, Tang C, McKay H, Oxland TR, Guy P, Wang R. Strain redistribution and cracking behavior of human bone during bending.
Bone
. May 2007;40(5):1265-1275.
2012
Kennedy OD, Herman BC, Laudier DM, Majeska RJ, Sun HB, Schaffler MB. Activation of resorption in fatigue-loaded bone involves both apoptosis and active pro-osteoclastogenic signaling by distinct osteocyte populations.
Bone
. May 2012;50(5):1115-1122.
2014
Kennedy OD, Laudier DM, Majeska RJ, Sun HB, Schaffler MB. Osteocyte apoptosis is required for production of osteoclastogenic signals following bone fatigue in vivo.
Bone
. July 2014;64:132-137.
2015
Tang T, Ebacher V, Cripton P, Guy P, McKay H, Wang R. Shear deformation and fracture of human cortical bone.
Bone
. February 2015;71:25-35.
2015
Goff MG, Lambers FM, Nguyen TM, Sung J, Rimnac CM, Hernandez CJ. Fatigue-induced microdamage in cancellous bone occurs distant from resorption cavities and trabecular surfaces.
Bone
. October 2015;79:8-14.
2019
Burr DB. Stress concentrations and bone microdamage: John Currey's contributions to understanding the initiation and arrest of cracks in bone.
Bone
. October 2019;127:517-525.
2021
Loundagin LL, Pohl AJ, Edwards WB. Stressed volume estimated by finite element analysis predicts the fatigue life of human cortical bone: the role of vascular canals as stress concentrators.
Bone
. February 2021;143:115647.
2020
Loundagin LL, Haider IT, Cooper DML, Edwards WB. Association between intracortical microarchitecture and the compressive fatigue life of human bone: a pilot study.
Bone Rep
. June 2020;12:100254.
1993
Martin B. Aging and strength of bone as a structural material.
Calcif Tiss Int
. February 1993;53(suppl 1):S34-S40.
1993
Burr DB. Remodeling and the repair of fatigue damage.
Calcif Tiss Int
. February 1993;53(suppl 1):S75-S81.
1996
Zioupos P, Wang XT, Currey JD. The accumulation of fatigue microdamage in human cortical bone of two different ages in vitro.
Clin Biomech
(Bristol, Avon). October 1996;11(7):365-375.
1978
Carter DR, Spengler DM. Mechanical properties and composition of cortical bone.
Clin Orthop Relat Res
. September 1978;135:192-217.
1990
Burr DB, Stafford T. Validity of the bulk-staining technique to separate artifactual from in vivo bone microdamage.
Clin Orthop Relat Res
. November 1990;260:305-308.
2004
Doblaré M, García JM, Gomez MJ. Modelling bone tissue fracture and healing: a review.
Eng Fract Mech
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2013
Ural A, Mischinski S. Multiscale modeling of bone fracture using cohesive finite elements.
Eng Fract Mech
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1989
Jones BH, Harris JM, Vinh TN, Rubin C. Exercise-induced stress fractures and stress reactions of bone: epidemiology, etiology, and classification.
Exerc Sport Sci Rev
. January 1989;17(1):379-422.
1997
Burr DB. Bone, exercise, and stress fractures.
Exerc Sport Sci Rev
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2016
Osterhoff G, Morgan EF, Shefelbine SJ, Karim L, McNamara LM, Augat P. Bone mechanical properties and changes with osteoporosis.
Injury
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2000
Lee TC, O'Brien FJ, Taylor D. The nature of fatigue damage in bone.
Int J Fract
. November 2000;22(10):847-853.
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.
2006
Mohsin S, O'Brien FJ, Lee TC. Osteonal crack barriers in ovine compact bone.
J Anat
. January 2006;208(1):81-89.
2011
Mischinski S, Ural A. Finite element modeling of microcrack growth in cortical bone.
J Appl Mech
. July 2011;78(4):041016.
1981
Wright TM, Vosburgh F, Burstein AH. Permanent deformation of compact bone monitored by acoustic emission.
J Biomech
. 1981;14(6):405-409.
1982
Martin RB, Burr DB. A hypothetical mechanism for the stimulation of osteonal remodelling by fatigue damage.
J Biomech
. 1982;15(3):137-139.
1984
Lipson SF, Katz JL. The relationship between elastic properties and microstructure of bovine cortical bone.
J Biomech
. 1984;17(4):231-240.
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.
1986
Martens M, van Audekercke R, de Meester P, Mulier JC. Mechanical behaviour of femoral bones in bending loading.
J Biomech
. 1986;19(6):443-454.
1987
Carter DR, Fyhrie DP, Whalen RT. Trabecular bone density and loading history: regulation of connective tissue biology by mechanical energy.
J Biomech
. 1987;20(8):785-794.
1987
Carter DR. Mechanical loading history and skeletal biology.
J Biomech
. 1987;20(11-12):1095-1109.
1988
Burr DB, Schaffler MB, Frederickson RG. Composition of the cement line and its possible mechanical role as a local interface in human compact bone.
J Biomech
. 1988;21(11):939-945.
1989
Caler WE, Carter DR. Bone creep-fatigue damage accumulation.
J Biomech
. 1989;22(6-7):625-635.
1993
Michel MC, Guo X-DE, Gibson LJ, McMahon TA, Hayes WC. Compressive fatigue behavior of bovine trabecular bone.
J Biomech
. April–May 1993;26(4-5):453-463.
1994
Prendergast P, Taylor D. Prediction of bone adaptation using damage accumulation.
J Biomech
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1996
Pattin CA, Caler WE, Carter DR. Cyclic mechanical property degradation during fatigue loading of cortical bone.
J Biomech
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1996
Zioupos P, Wang XT, Currey JD. Experimental and theoretical quantification of the development of damage in fatigue tests of bone and antler.
J Biomech
. August 1996;29(8):989-1002.
1996
Courtney AC, Hayes WC, Gibson LJ. Age-related differences in post-yield damage in human cortical bone: experiment and model.
J Biomech
. November 1996;29(11):1463-1471.
1997
Martin RB, Gibson VA, Stover SM, Gibeling JC, Griffin LV. Residual strength of equine bone is not reduced by intense fatigue loading: implications for stress fracture.
J Biomech
. February 1997;30(2):109-114.
1997
Hoshaw SJ, Cody DD, Saad AM, Fyhrie DP. Decrease in canine proximal femoral ultimate strength and stiffness due to fatigue damage.
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1997
Vashishth D, Behiri JC, Bonfield W. Crack growth resistance in cortical bone: concept of microcrack toughening.
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1998
Burr DB, Turner CH, Naick P, Forwood MR, Ambrosius W, Hasan MS, Pidaparti R. Does microdamage accumulation affect the mechanical properties of bone?
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1998
Taylor D. Microcrack growth parameters for compact bone deduced from stiffness variations.
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1998
Zioupos P, Casinos A. Cumulative damage and the response of human bone in two-step loading fatigue.
J Biomech
. September 1998;31(9):825-833.
2003
Götzen N, Cross AR, Ifju PG, Rapoff AJ. Understanding stress concentration about a nutrient foramen.
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. October 2003;36(10):1511-1521.
2003
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J Biomech
. November 2003;36(11):1683-1689.
2007
Ural A, Vashishth D. Anisotropy of age-related toughness loss in human cortical bone: a finite element study.
J Biomech
. 2007;40(7):1606-1614.
2008
Kosmopoulos V, Schizas C, Keller TS. Modeling the onset and propagation of trabecular bone microdamage during low-cycle fatigue.
J Biomech
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2021
Haider IT, Lee M, Page R, Smith D, Edwards WB. Mechanical fatigue of whole rabbit-tibiae under combined compression-torsional loading is better explained by strained volume than peak strain magnitude.
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1983
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1996
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1998
Guo XE, Liang LC, Goldstein SA. Micromechanics of osteonal cortical bone fracture.
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2003
Moore TLA, Gibson LJ. Fatigue of bovine trabecular bone.
J Biomech Eng
. December 2003;125(6):761-768.
2004
Dong XN, Guo XE. Geometric determinants to cement line debonding and osteonal lamellae failure in osteon pushout tests.
J Biomech Eng
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2000
Phelps JB, Hubbard GB, Wang X, Agrawal CM. Microstructural heterogeneity and the fracture toughness of bone.
J Biomed Mater Res
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1999
Donahue SW, Sharkey NA. Strains in the metatarsals during the stance phase of gait: implications for stress fractures.
J Bone Joint Surg
. September 1999;81A(9):1236-1244.
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.
2009
Cardoso L, Herman BC, Verborgt O, Laudier D, Majeska RJ, Schaffler MB. Osteocyte apoptosis controls activation of intracortical resorption in response to bone fatigue.
J Bone Miner Res
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1999
Reilly GC, Currey JD. The development of microcracking and failure in bone depends on the loading mode to which it is adapted.
J Exp Biol
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2003
Lieberman DE, Pearson OM, Polk JD, Demes B, Crompton AW. Optimization of bone growth and remodeling in response to loading in tapered mammalian limbs.
J Exp Biol
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1985
Carter DR, Caler WE. A cumulative damage model for bone-fracture.
J Orthop Res
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1988
Currey JD. Strain rate and mineral content in fracture models of bone.
J Orthop Res
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1990
Nunamaker DM, Butterweck DM, Provost MT. Fatigue fractures in thoroughbred racehorses: relationships with age, peak bone strain, and training.
J Orthop Res
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1992
Martin B. A theory of fatigue damage accumulation and repair in cortical bone.
J Orthop Res
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1995
Martin B. Mathematical model for repair of fatigue damage and stress fracture in osteonal bone.
J Orthop Res
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1995
Gibson VA, Stover SM, Martin RB, Gibeling JC, Willits NH, Gustafson MB, Griffin LV. Fatigue behavior of the equine third metacarpus: mechanical property analysis.
J Orthop Res
. November 1995;13(6):861-868.
1996
Jepsen KJ, Goldstein SA, Kuhn JL, Schaffler MB, Bonadio J. Type‐I collagen mutation compromises the post‐yield behavior of Mov13 long bone.
J Orthop Res
. May 1996;14(3):493-499.
1996
Martin RB, Stover SM, Gibson VA, Gibeling JC, Griffin LV. In vitro fatigue behavior of the equine third metacarpus: remodeling and microcrack damage analysis.
J Orthop Res
. September 1996;14(5):794-801.
1997
Griffin LV, Gibeling JC, Martin RB, Gibson VA, Stover SM. Model of flexural fatigue damage accumulation for cortical bone.
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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
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2005
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J Orthop Res
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1999
Nanci A. Content and distribution of noncollagenous matrix proteins in bone and cementum: relationship to speed of formation and collagen packing density.
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2005
Dong XN, Zhang X, Guo XE. Interfacial strength of cement lines in human cortical bone.
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2004
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2014
Schwiedrzik J, Raghavan R, Bürki A, LeNader V, Wolfram U, Michler J, Zysset P. In situ micropillar compression reveals superior strength and ductility but an absence of damage in lamellar bone.
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2020
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2004
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2000
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2006
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2012
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The Frequency, Aqueous Solution, Stress Amplitude, Temperature (FAST) Machine: A Device Proposed for Accelerated Fatigue Testing of Cortical Bone
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2002
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Micromechanics of Osteonal Cortical Bone
[PhD thesis]. Columbia University; 2002.
2015
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2003
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An Experimental Investigation Into the Effects of Cyclic Fatigue on Ageing Human Cortical Bone
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2002
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Investigating the Role of Interstitial Fluid Flow in Bone Adaptation and Metabolism
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2004
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2011
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[PhD thesis]. Atlanta, GA: Georgia Institute of Technology; August 2011.
1993
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Fatigue of Trabecular Bone
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1994
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Mechanical Properties of the Proximal Femur: Changes With Age
[PhD thesis]. Cambridge, MA: Harvard University; May 1994.
2009
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2002
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The Relationship Between the Osteonal Cement Line and Bone Strength
[PhD thesis]. Loma Linda University; June 2002.
2023
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Mineralization of Biological Fiber Systems
[PhD thesis]. McGill University; July 2023.
2001
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Microdamage Accumulation in Bovine Trabecular Bone
[PhD thesis]. Cambridge, MA: Massachusetts Institute of Technology; June 2001.
2008
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Osteocytes and Activation of Bone Remodeling
[PhD thesis]. Mount Sinai School of Medicine; 2008.
2020
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Time-Sequence of Biomechanical Adaption in Trabecular Tissue During Estrogen Deficiency
[PhD thesis]. National University of Ireland Galway; March 2020.
2011
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Histomorphometry of the Elderly Rib: A Methodological Approach With Implications for Biomechanics, Function, and Fracture Risk
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2018
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Defining Bone Quality: Cortical Microdamage and Its Contribution to Fracture Risk in the Human Rib
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2012
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Mechanically Induced Calcium Efflux from Bone Matrix Stimulates Osteoblasts
[PhD thesis]. Purdue University; May 2012.
2023
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Constitutive Models of Bone: The Human Femur
[PhD thesis]. Queensland University of Technology; 2023.
2005
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Multiaxial Fracture Characteristics of Aging Human Bone
[PhD thesis]. Troy, NY: Rensselaer Polytechnic Institute; April 2005.
1994
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Simulation of Functional Adaptation in Trabecular and Cortical Bone
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2000
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2008
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1982
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2003
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2011
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2018
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[PhD thesis]. Calgary, AB: University of Calgary; July 2020.
2002
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The Dependence on Anatomic Site of Trabecular Bone Structure-Function Relationships
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1987
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Dorsal Metacarpal Disease in Thoroughbred Horses: Relationship to the Development of the Third Metacarpal Bone
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1999
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Bone Strain and Microdamage At Stress Fracture Sites in Human Metatarsals
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2000
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Fatigue Behavior of Equine Third Metacarpal Bone Tissue
[PhD thesis]. Davis, University of California; 2000.
2001
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Fatigue Crack Growth Behavior in Equine Cortical Bone
[PhD thesis]. Davis, University of California; 2001.
2013
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Multi-Level Micromechanical Modeling of Bone Tissues
[PhD thesis]. Los Angeles, CA: Los Angeles, University of California; 2013.
1996
Adams DJ.
Mechanical Factors Initiating Appositional Bone Formation
[PhD thesis]. University of Iowa; May 1996.
1994
Jepsen KJ.
Characterization of the Hierarchical Composite Properties of Cortical Bone: A Transgenic Approach
[PhD thesis]. University of Michigan; 1994.
2003
Rajachar RM.
Effects of Age -Related Ultra-Structural Level Changes in Bone on Microdamage Mechanisms
[PhD thesis]. University of Michigan; 2003.
2004
Hoffler CE II.
In Pursuit of Accurate Structural and Mechanical Osteocyte Mechanotransduction Models
[PhD thesis]. University of Michigan; 2004.
2009
Sahar ND.
Investigating the Effects of Age and Exercise on Bone Composition and the Impact of Composition on Mechanical Integrity.
[PhD thesis]. University of Michigan; 2009.
2014
Schwiedrzik JJ.
Experimental, Theoretical and Numerical Investigation of the Nonlinear Micromechanical Properties of Bone
[PhD thesis]. Universität Bern; 2014.
2019
Martig S.
Compressive Fatigue Life and Micromorphology of Equine Metacarpal Subchondral Bone
[PhD thesis]. University of Melbourne; June 2019.
1996
Beck BR.
The Relationship of Streaming Potential Magnitude to Strain and Periosteal Modeling
[PhD thesis]. Eugene, OR: University of Oregon; December 1996.
2013
Gaspar AE.
Beyond Bone Mineral Density: Detecting Changes in Fracture Risk in the Absence of Mineral Loss With the Mechanical Response Tissue Analyzer
[Master's thesis]. University of Toronto; 2013.
2011
Islam A.
Mechanistic Model of Nanoscratch Test to Determine the in Situ Toughness of Bone
[Master's thesis]. San Antionio, TX: University of Texas at San Antonio; May 2011.
2000
Funk JR.
The Effect of Active Muscle Tension on the Axial Impact Tolerance of the Human Foot/ankle Complex
[PhD thesis]. Charlottesville, VA: University of Virginia; August 2000.
1985
Schaffler MB.
Stiffness and Fatigue of Compact Bone At Physiological Strains and Strain Rates
[PhD thesis]. West Virginia University; 1985.
1998
Yeni YN.
Fracture Mechanics of Human Cortical Bone: The Relationship of Geometry, Microstructure and Composition With the Fracture of the Tibia, Femoral Shaft and the Femoral Neck
[PhD thesis]. West Virginia University; 1998.
2001
Brown CU.
Time-Dependent Circumferential Deformation of Cortical Bone Subjected to Internal Radial Loading
[PhD thesis]. West Virginia University; 2001.
2001
Parsamian GP.
Damage Mechanics of Human Cortical Bone
[PhD thesis]. West Virginia University; 2001.