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Skedros, John G.
1
Biomechanical foundations of histological analysis in limb bones: the crucial role of load-complexity categorization and collagen fiber orientation analysis when interpreting bone adaptation
Bone Histology: A Biological Anthropological Perspective
Affiliations
1
Adjunct Associate Professor of Orthopaedic Surgery,
University of Utah
, Salt Lake City, Utah, USA
3
Links
DOI:
10.4324/9781003385608-5
Cited Works (116)
Year
Entry
1979
Lanyon LE, Bourn S. The influence of mechanical function on the development and remodeling of the tibia: an experimental study in sheep.
J Bone Joint Surg
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2007
Schneider P, Stauber M, Voide R, Stampanoni M, Donahue LR, Müller R. Ultrastructural properties in cortical bone vary greatly in two inbred strains of mice as assessed by synchrotron light based micro‐ and nano‐CT.
J Bone Miner Res
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2022
Buss DJ, Kröger R, McKee MD, Reznikov N. Hierarchical organization of bone in three dimensions: a twist of twists.
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2002
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1917
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1974
Lanyon LE. Experimental support for the trajectorial theory of bone structure.
J Bone Joint Surg
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1975
Lanyon LE, Hampson WGJ, Goodship AE, Shah JS. Bone deformation recorded in vivo from strain gauges attached to the human tibial shaft.
Acta Orthop Scand
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2015
Katsamenis OL, Jenkins T, Thurner PJ. Toughness and damage susceptibility in human cortical bone is proportional to mechanical inhomogeneity at the osteonal-level.
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1967
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1968
Ascenzi A, Bonucci E. The compressive properties of single osteons.
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1958
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Acta Anat
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2000
Fritton SP, McLeod KJ, Rubin CT. Quantifying the strain history of bone: spatial uniformity and self-similarity of low-magnitude strains.
J Biomech
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1974
Simkin A, Robin G. Fracture formation in differing collagen fiber pattern of compact bone.
J Biomech
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1993
Riggs CM, Lanyon LE, Boyde A. Functional associations between collagen fibre orientation and locomotor strain direction in cortical bone of the equine radius.
Anat Embryol
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1965
Kerley ER. The microscopic determination of age in human bone.
Am J Phys Anthropol
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2007
Skedros JG, Baucomb SL. Mathematical analysis of trabecular “trajectories” in apparent trajectorial structures: the unfortunate historical emphasis on the human proximal femur.
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2004
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1976
Carter DR, Hayes WC, Schurman DJ. Fatigue life of compact bone, II: effects of microstructure and density.
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2000
Haapasalo H, Kontulainen S, Sievänen H, Kannus P, Järvinen M, Vuori I. Exercise-induced bone gain is due to enlargement in bone size without a change in volumetric bone density: a peripheral quantitative computed tomography study of the upper arms of male tennis players.
Bone
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1998
Zioupos P, Currey JD. Changes in the stiffness, strength, and toughness of human cortical bone with age.
Bone
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2003
Burger EH, Klein-Nulend J, Smit TH. Strain-derived canalicular fluid flow regulates osteoclast activity in a remodelling osteon: a proposal.
J Biomech
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1976
Lanyon LE, Baggott DG. Mechanical function as an influence on the structure and form of bone.
J Bone Joint Surg
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1988
Ruff CB, Hayes WC. Sex differences in age‐related remodeling of the femur and tibia.
J Orthop Res
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1979
Goodship AE, Lanyon LE, McFie H. Functional adaptation of bone to increased stress: an experimental study.
J Bone Joint Surg
. June 1979;61A(4):539-546.
1999
Reilly GC, Currey JD. The development of microcracking and failure in bone depends on the loading mode to which it is adapted.
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1989
Martin RB, Burr DB.
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2005
Mayhew PM, Thomas CD, Clement JG, Loveridge N, Beck TJ, Bonfield W, Burgoyne CJ, Reeve J. Relation between age, femoral neck cortical stability, and hip fracture risk.
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1986
Biewener AA, Swartz SM, Bertram JEA. Bone modeling during growth: dynamic strain equilibrium in the chick tibiotarsus.
Calcif Tiss Int
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1996
Parfitt AM, Mundy GR, Roodman GD, Hughes DE, Boyce BF. A new model for the regulation of bone resorption, with particular reference to the effects of bisphosphonates.
J Bone Miner Res
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2009
Espinoza Orías AA, Deuerling JM, Landrigan MD, Renaud JE, Roeder RK. Anatomic variation in the elastic anisotropy of cortical bone tissue in the human femur.
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1997
Yeni YN, Brown CU, Wang Z, Norman TL. The influence of bone morphology on fracture toughness of the human femur and tibia.
Bone
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2003
Martin RB. Fatigue microdamage as an essential element of bone mechanics and biology.
Calcif Tiss Int
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2001
Cowin SC. Mechanics of materials. In: Cowin SC, ed.
Bone Mechanics Handbook
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2007
Nyman JS, Roy A, Tyler JH, Acuna RL, Gayle HJ, Wang X. Age‐related factors affecting the postyield energy dissipation of human cortical bone.
J Orthop Res
. May 2007;25(7):646-655.
1998
Martin RB, Burr DB, Sharkey NA.
Skeletal Tissue Mechanics
. New York, NY: Springer-Verlag; 1998.
1984
Portigliatti Barbos M, Bianco P, Ascenzi A, Boyde A. Collagen orientation in compact bone, II: distribution of lamellae in the whole of the human femoral shaft with reference to its mechanical properties.
Metab Bone Dis Rel Res
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1997
Judex S, Gross TS, Zernicke RF. Strain gradients correlate with sites of exercise‐induced bone‐forming surfaces in the adult skeleton.
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2010
Barth HD, Launey ME, MacDowell AA, Ager JW III, Ritchie RO. On the effect of X-ray irradiation on the deformation and fracture behavior of human cortical bone.
Bone
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2001
Rho JY, Currey JD, Zioupos P, Pharr GM. The anisotropic Young's modulus of equine secondary osteones and interstitial bone determined by nanoindentation.
J Exp Biol
. May 2001;204(10):1775-1781.
1971
Lambert KL. The weight-bearing function of the fibula: a strain gauge study.
J Bone Joint Surg
. April 1971;53A(3):507-513.
1988
Ascenzi A. The micromechanics versus the macromechanics of cortical bone: a comprehensive presentation.
J Biomech Eng
. November 1988;110(4):357-363.
2011
Feng X, McDonald JM. Disorders of bone remodeling.
Annu Rev Pathol
. 2011;6:121-145.
2023
Vitienes I, Mikolajewicz N, Hosseinitabatabaei S, Bouchard A, Julien C, Graceffa G, Rentsch A, Widowski T, Main RP, Willie BM. Breed and loading history influence in vivo skeletal strain patterns in pre-pubertal female chickens.
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. August 2023;173:116785.
1982
Lanyon LE, Goodship AE, Pye CJ, MacFie JH. Mechanically adaptive bone remodelling.
J Biomech
. 1982;15(3):141-154.
1987
Lanyon LE. Functional strain in bone tissue as an objective, and controlling stimulus for adaptive bone remodelling.
J Biomech
. 1987;20(11-12):1083-1093.
2002
Banse X, Sims TJ, Bailey AJ. Mechanical properties of adult vertebral cancellous bone: correlation with collagen intermolecular cross-links.
J Bone Miner Res
. July 2002;17(9):1621-1628.
1997
Adams DJ, Spirt AA, Brown TD, Fritton SP, Rubin CT, Brand RA. Testing the daily stress stimulus theory of bone adaptation with natural and experimentally controlled strain histories.
J Biomech
. July 1997;30(7):671-678.
2007
Diab T, Vashishth D. Morphology, localization and accumulation of in vivo microdamage in human cortical bone.
Bone
. March 2007;40(3):612-618.
1982
Rubin CT, Lanyon LE. Limb mechanics as a function of speed and gait: a study of functional strains in the radius and tibia of horse and dog.
J Exp Biol
. December 1982;101:187-211.
1985
Rubin CT, Lanyon LE. Regulation of bone mass by mechanical strain magnitude.
Calcif Tiss Int
. 1985;37(4):411-417.
1984
Rubin CT, Lanyon LE. Regulation of bone formation by applied dynamic loads.
J Bone Joint Surg
. March 1984;66A(3):397-402.
1980
Carter DR, Smith DJ, Spengler DM, Daly CH, Frankel VH. Measurement and analysis of in vivo bone strains on the canine radius and ulna.
J Biomech
. 1980;13(1):27-38.
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.
2000
Liu D, Wagner HD, Weiner S. Bending and fracture of compact circumferential and osteonal lamellar bone of the baboon tibia.
J Mater Sci Mater Med
. January 2000;11(1):49-60.
1989
Martin RB, Ishida J. The relative effects of collagen fiber orientation, porosity, density, and mineralization on bone strength.
J Biomech
. 1989;22(5):419-426.
2002
Ehrlich PJ, Lanyon LE. Mechanical strain and bone cell function: a review.
Osteoporos Int
. September 2002;13(9):688-700.
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.
1971
Vincentelli R, Evans FG. Relations among mechanical properties, collagen fibers, and calcification in adult human cortical bone.
J Biomech
. May 1971;4(3):193-201.
2005
Tommasini SM, Nasser P, Schaffler MB, Jepsen KJ. Relationship between bone morphology and bone quality in male tibias: implications for stress fracture risk.
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1970
Yamada H.
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2009
Ciarelli TE, Tjhia C, Rao S, Qiu S, Parfitt M, Fyhrie DP. Trabecular packet-level lamellar density patterns differ by fracture status and bone formation rate in white females.
Bone
. November 2009;45(5):903-908.
2006
Gibson VA, Stover SM, Gibeling JC, Hazelwood SJ, Martin RB. Osteonal effects on elastic modulus and fatigue life in equine bone.
J Biomech
. 2006;39(2):217-225.
1995
Rubin CT, Gross TS, McLeod KJ, Bain SD. Morphologie stages in lamellar bone formation stimulated by a potent mechanical stimulus.
J Bone Miner Res
. March 1995;10(3):488-495.
2019
Zimmermann EA, Riedel C, Schmidt FN, Stockhausen KE, Chushkin Y, Schaible E, Gludovatz B, Vettorazzi E, Zontone F, Püschel K, Amling M, Ritchie RO, Busse B. Mechanical competence and bone quality develop during skeletal growth.
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2006
Bigley RF, Griffin LV, Christensen L, Vandenbosch R. Osteon interfacial strength and histomorphometry of equine cortical bone.
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1991
Bertram JEA, Swartz SM. The “law of bone transformation”: a case of crying Wolff?
Biol Rev
. August 1991;66(3):245-273.
2008
Edwards WB, Gillette JC, Thomas JM, Derrick TR. Internal femoral forces and moments during running: implications for stress fracture development.
Clin Biomech
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1992
Gross TS, McLeod KJ, Rubin CT. Characterizing bone strain distributions in vivo using three triple rosette strain gages.
J Biomech
. September 1992;25(9):1081-1087.
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
. September 15, 2003;206(18):3125-3138.
1996
Biewener AA, Fazzalari NL, Konieczynski DD, Baudinette RV. Adaptive changes in trabecular architecture in relation to functional strain patterns and disuse.
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1985
Vincentelli R, Grigoroi M. The effect of Haversian remodeling on the tensile properties of human cortical bone.
J Biomech
. 1985;18(3):201-207.
1997
Aamodt A, Lund-Larsen J, Eine J, Andersen E, Benum P, Schnell Husby O. In vivo measurements show tensile axial strain in the proximal lateral aspect of the human femur.
J Orthop Res
. November 1997;15(6):927-931.
2005
O'Brien FJ, Taylor D, Lee TC. The effect of bone microstructure on the initiation and growth of microcracks.
J Orthop Res
. March 2005;23(2):475-480.
1997
Han Z-H, Palnitkar S, Rao DS, Nelson D, Parfitt AM. Effects of ethnicity and age or menopause on the remodeling and turnover of iliac bone: implications for mechanisms of bone loss.
J Bone Miner Res
. April 1997;12(4):498-508.
1993
Turner CH, Burr DB. Basic biomechanical measurements of bone: a tutorial.
Bone
. 1993;14(4):595-608.
1999
Muir P, Johnson KA, Ruaux-Mason CP. In vivo matrix microdamage in a naturally occurring canine fatigue fracture.
Bone
. November 1999;25(5):571-576.
1995
Thomas KA, Harris MB, Willis MC, Lu Y, MacEwen GD. The effects of the interosseous membrane and partial fibulectomy on loading of the tibia: a biomechanical study.
Orthopedics
. April 1995;18(3):373-83.
2003
Hiller LP, Stover SM, Gibson VA, Gibeling JC, Prater CS, Hazelwood SJ, Yeh OC, Martin RB. Osteon pullout in the equine third metacarpal bone: effects of ex vivo fatigue.
J Orthop Res
. May 2003;21(3):481-488.
1998
Duda GN, Heller M, Albinger J, Schulz O, Schneider E, Claes L. Influence of muscle forces on femoral strain distribution.
J Biomech
. September 1998;31(9):841-846.
1986
Corondan G, Haworth WL. A fractographic study of human long bone.
J Biomech
. 1986;19(3):207-218.
2000
Reilly GC, Currey JD. The effects of damage and microcracking on the impact strength of bone.
J Biomech
. March 2000;33(3):337-343.
1999
Takano Y, Turner CH, Owan I, Martin RB, Lau ST, Forwood MR, Burr DB. Elastic anisotropy and collagen orientation of osteonal bone are dependent on the mechanical strain distribution.
J Orthop Res
. January 1999;17(1):59-66.
2000
Reilly GC. Observations of microdamage around osteocyte lacunae in bone.
J Biomech
. September 2000;33(9):1131-1134.
2023
Rooney AM, McNeill TJ, Ross FP, Bostrom MPG, van der Meulen MCH. PTH treatment increases cortical bone mass more in response to compression than tension in mice.
J Bone Miner Res
. January 2023;38(1):59-69.
1983
Biewener AA, Thomason J, Goodship A, Lanyon LE. Bone stress in the horse forelimb during locomotion at different gaits: a comparison of two experimental methods.
J Biomech
. 1983;16(8):565-576.
1988
Bertram JEA, Biewener AA. Bone curvature: sacrificing strength for load predictability?
J Theo Biol
. March 7, 1988;131(1):75-92.
1996
Burr DB, Milgrom C, Fyhrie D, Forwood M, Nyska M, Finestone A, Hoshaw S, Saiag E, Simkin A. In vivo measurement of human tibial strains during vigorous activity.
Bone
. May 1996;18(5):405-410.
2020
Robling AG, Bonewald LF. The osteocyte: new insights.
Annu Rev Physiol
. 2020;82:485-506.
2002
Burr DB. The contribution of the organic matrix to bone's material properties.
Bone
. July 2002;31(1):8-11.
2004
Vashishth D. Rising crack-growth-resistance behavior in cortical bone: implications for toughness measurements.
J Biomech
. June 2004;37(6):943-946.
2001
van der Meulen MCH, Jepsen KJ, Mikić B. Understanding bone strength: size isn’t everything.
Bone
. July 2001;29(1):101-104.
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.
2006
Ruff C, Holt B, Trinkaus E. Who's afraid of the big bad Wolff? “Wolff's law” and bone functional adaptation.
Am J Phys Anthropol
. April 2006;129(4):484-498.
2000
Yeni YN, Norman TL. Calculation of porosity and osteonal cement line effects on the effective fracture toughness of cortical bone in longitudinal crack growth.
J Biomed Mater Res
. September 5, 2000;51(3):504-509.
2001
Keaveny TM, Morgan EF, Niebur GL, Yeh OC. Biomechanics of trabecular bone.
Annu Rev Biomed Eng
. 2001;3:307-333.
2006
Ascenzi M-G, Lomovtsev A. Collagen orientation patterns in human secondary osteons, quantified in the radial direction by confocal microscopy.
J Struct Biol
. January 2006;153(1):14-30.
2021
O'Leary TJ, Wardle SL, Gifford RM, Double RL, Reynolds RM, Woods DR, Greeves JP. Tibial macrostructure and microarchitecture adaptations in women during 44 weeks of arduous military training.
J Bone Miner Res
. July 2021;36(7):1300-1315.
2003
Ascenzi M-G, Ascenzi A, Benvenuti A, Burghammer M, Panzavolta S, Bigid A. Structural differences between “dark” and “bright” isolated human osteonic lamellae.
J Struct Biol
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1998
Wang XD, Masilamani NS, Mabrey JD, Alder ME, Agrawal CM. Changes in the fracture toughness of bone may not be reflected in its mineral density, porosity, and tensile properties.
Bone
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1974
Evans FG, Vincentelli R. Relations of the compressive properties of human cortical bone to histological structure and calcification.
J Biomech
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1999
Turner CH. Toward a mathematical description of bone biology: the principle of cellular accommodation.
Calcif Tiss Int
. December 1999;65(6):466-471.
1976
Evans FG. Mechanical properties and histology of cortical bone from younger and older men.
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1974
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J Bone Joint Surg
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1989
Currey JD, Pond CM. Mechanical properties of very young bone in the axis deer (
Axis axis
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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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1975
Reilly DT, Burstein AH. The elastic and ultimate properties of compact bone tissue.
J Biomech
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1978
Moyle DD, Welborn JW III, Cooke FW. Work to fracture of canine femoral bone.
J Biomech
. 1978;11(10-12):435-440.
2001
Hsieh Y, Robling AG, Ambrosius WT, Burr DB, Turner CH. Mechanical loading of diaphyseal bone in vivo: the strain threshold for an osteogenic response varies with location.
J Bone Miner Res
. December 2001;16(10):2291-2297.
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.
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1983
Biewener AA, Thomason J, Lanyon LE. Mechanics of locomotion and jumping in the forelimb of the horse (
Equus
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1975
Turner AS, Mills EJ, Gabel AA. In vivo measurement of bone strain in the horse.
Am J Vet Res
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2000
Beck TJ, Looker AC, Ruff CB, Sievanen H, Wahner HW. Structural trends in the aging femoral neck and proximal shaft: analysis of the third national health and nutrition examination survey dual‐energy x‐ray absorptiometry data.
J Bone Miner Res
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2013
Li S.
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1967
Evans FG, Bang S. Differences and relationships between the physical properties and the microscopic structure of human femoral, tibial and fibular cortical bone.
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. January 1967;120(1):79-88.
1993
Martin RB, Boardman DL. The effects of collagen fiber orientation, porosity, density, and mineralization on bovine cortical bone bending properties.
J Biomech
. September 1993;26(9):1047-1054.
2010
Herman BC, Cardoso L, Majeska RJ, Jepsen KJ, Schaffler MB. Activation of bone remodeling after fatigue: differential response to linear microcracks and diffuse damage.
Bone
. October 2010;47(4):766-772.