Relating Cortical Bone Mechanics to Intracortical Pore Morphology, Distribution and Remodeling History Within the Fibula Diaphysis

Introduction: During aging and osteoporosis, the cortical bone becomes more porous, making it more fragile and susceptible to fractures. The aim of this study was to investigate the intracortical compression-induced strain energy distribution, and determine whether the intracortical pores associated with high strain energy density (SED) in the surrounding bone have a different morphology, distribution and remodeling history than pores with low SED.

Methods: The study was conducted on fibula diaphysis specimens from 20 patients undergoing a jaw reconstruction (age range 41-75 years, 18 men and 8 women). Specimens were plastic embedded, µCT-scanned and sectioned for histology. Threedimensional micro-finite element models of each specimen were tested in compression using a linearly elastic analysis, and the SED of the bone immediately surrounding the pores was calculated within a plane of interest corresponding to the histological sections. The statistical distribution of the SED of all pores, per sample, was used to identify high SED pores (SED > 1.5 times the interquartile range from the 75th percentile) and the remaining low SED pores.

Results: Pores with high SED were larger (p ≤ 0.0001), less circular (p ≤ 0.0001), and were located closer to the endosteal edge of the cortex (p ≤ 0.0001) than low SED pores (Figure 1A-C). A detailed histological analysis of the remodeling events generating the pores revealed that the high SED pores compared to low SED pores had a 13.3-fold higher odds of being a resorptive (70%) or formative (11%) pore rather than a completely remodeled pore (p ≤ 0.0001). The resorption space associated with the 91% of high SED pores overlapped with the pore of a preexisting remodeling event (osteon) (5.9-fold higher odds).

Conclusions: Collectively, these data show that the high SED pores are preferentially enlarged irregular pores positioned closer to the endosteal surface of the cortex, and that these pores tend to be resorptive pores that overlap with the pore of a preexisting parent osteon, suggesting that pores may originate from resorption within preexisting pores rather than from penetrative resorptions generating new pores. Overall, the study demonstrates a strong relationship between cortical bone mechanics and the pores morphology, distribution and remodeling history in the human fibula.

Year	Entry
1988	Schaffler MB, Burr DB. Stiffness of compact bone: effects of porosity and density. J Biomech. 1988;21(1):13-16.
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.
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.
1992	Hogan HA. Micromechanics modeling of Haversian cortical bone properties. J Biomech. May 1992;25(5):549-556.
2001	Bousson V, Meunier A, Bergot C, Vicaut É, Rocha MA, Morais MH, Laval‐Jeantet A, Laredo J. Distribution of intracortical porosity in human midfemoral cortex by age and gender. J Bone Miner Res. July 2001;16(7):1308-1317.
2004	Bousson V, Peyrin F, Bergot C, Hausard M, Sautet A, Laredo J. Cortical bone in the human femoral neck: three‐dimensional appearance and porosity using synchrotron radiation. J Bone Miner Res. May 2004;19(5):794-801.
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.
2006	Nicolella DP, Moravits DE, Gale AM, Bonewald LF, Lankford J. Osteocyte lacunae tissue strain in cortical bone. J Biomech. 2006;39(9):1735-1743.
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.
1988	Ruff CB, Hayes WC. Sex differences in age‐related remodeling of the femur and tibia. J Orthop Res. November 1988;6(6):886-896.
1999	Zysset PK, Guo XE, Hoffler CE, Moore KE, Goldstein SA. Elastic modulus and hardness of cortical and trabecular bone lamellae measured by nanoindentation in the human femur. J Biomech. October 1999;32(10):1005-1012.
2008	Budyn E, Hoc T, Jonvaux J. Fracture strength assessment and aging signs detection in human cortical bone using an X-FEM multiple scale approach. Comput Mech. September 2008;42(4):579-591.
1993	Brockstedt H, Kassem M, Eriksen EF, Mosekilde L, Melsen F. Age- and sex-related changes in iliac cortical bone mass and remodeling. Bone. July–August 1993;14(4):681-691.
2003	Wang X, Ni Q. Determination of cortical bone porosity and pore size distribution using a low field pulsed NMR approach. J Orthop Res. March 2003;21(2):312-319.
2003	Turner CH, Robling AG. Designing exercise regimens to increase bone strength. Exerc Sport Sci Rev. January 2003;31(1):45-50.
1997	Feik SA, Thomas CDL, Clement JG. Age‐related changes in cortical porosity of the midshaft of the human femur. J Anat. October 1997;191(3):407-416.
2012	Verbruggen SW, Vaughan TJ, McNamara LM. Strain amplification in bone mechanobiology: a computational investigation of the in vivo mechanics of osteocytes. J R Soc Interface. October 7, 2012;9(75):2735-2744.
2003	Stone KL, Seeley DG, Lui L-Y, Cauley JA, Ensrud K, Browner WS, Nevitt MC, Cummings SR; The Study of Osteoporotic Fractures research group. BMD at multiple sites and risk of fracture of multiple types: long-term results from the study of osteoporotic fractures. J Bone Miner Res. November 2003;18(11):1947-1954.
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.
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.
1999	Bell KL, Loveridge N, Power J, Garrahan N, Meggitt BF, Reeve J. Regional differences in cortical porosity in the fractured femoral neck. Bone. January 1999;24(1):57-64.
1998	Akiva U, Wagner HD, Weiner S. Modelling the three-dimensional elastic constants of parallel-fibred and lamellar bone. J Mater Sci. March 15, 1998;33(6):1497-1509.
2016	Granke M, Makowski AJ, Uppuganti S, Nyman JS. Prevalent role of porosity and osteonal area over mineralization heterogeneity in the fracture toughness of human cortical bone. J Biomech. September 6, 2016;49(13):2748-2755.
2004	Bayraktar HH, Morgan EF, Niebur GL, Morris GE, Wong EK, Keaveny TM. Comparison of the elastic and yield properties of human femoral trabecular and cortical bone tissue. J Biomech. January 2004;37(1):27-35.
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.
2006	Thomas CDL, Feik SA, Clement JG. Increase in pore area, and not pore density, is the main determinant in the development of porosity in human cortical bone. J Anat. August 2006;209(2):219-230.
2015	Zebaze R, Seeman E. Cortical bone: a challenging geography. J Bone Miner Res. January 2015;30(1):24-29.
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.
1993	Rho JY, Ashman RB, Turner CH. Young's modulus of trabecular and cortical bone material: ultrasonic and microtensile measurements. J Biomech. February 1993;26(2):111-119.
2014	Bala Y, Zebaze R, Ghasem-Zadeh A, Atkinson EJ, Iuliano S, Peterson JM, Amin S, Bjørnerem Å, Melton LJ III, Johansson H, Kanis JA, Khosla S, Seeman E. Cortical porosity identifies women with osteopenia at increased risk for forearm fractures. J Bone Miner Res. June 2014;29(6):1356-1362.
1996	Prendergast PJ, Huiskes R. Microdamage and osteocyte-lacuna strain in bone: a microstructural finite element analysis. J Biomech Eng. May 1996;118(2):240-246.
1987	Frost HM. Bone “mass” and the “mechanostat”: a proposal. Anat Rec. September 1987;219(1):1-9.
2005	Thomas CDL, Feik SA, Clement JG. Regional variation of intracortical porosity in the midshaft of the human femur: age and sex differences. J Anat. February 2005;206(2):115-125.
1999	Turner CH, Rho J, Takano Y, Tsui TY, Pharr GM. The elastic properties of trabecular and cortical bone tissues are similar: results from two microscopic measurement techniques. J Biomech. April 1999;32(4):437-441.
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.
2003	Cooper DML, Turinsky AL, Sensen CW, Hallgrímsson B. Quantitative 3D analysis of the canal network in cortical bone by micro-computed tomography. Anat Rec. September 2003;274B(1):169-179.
2006	Dong XN, Guo XE. Prediction of cortical bone elastic constants by a two-level micromechanical model using a generalized self-consistent method. J Biomech Eng. June 2006;128(3):309-316.
2006	Augat P, Schorlemmer S. The role of cortical bone and its microstructure in bone strength. Age Ageing. September 2006;35(suppl 2):ii27-ii31.
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.
1993	McCalden RW, McGeough JA, Barker MB, Court-Brown CM. Age-related changes in the tensile properties of cortical bone: the relative importance of changes in porosity, mineralization, and microstructure. J Bone Joint Surg. 1993;75A(8):1193-1205.
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.
2000	Smit TH, Burger EH. Is BMU-coupling a strain-regulated phenomenon? a finite element analysis. J Bone Miner Res. February 2000;12(2):301-307.
2003	Seeman E. Reduced bone formation and increased bone resorption: rational targets for the treatment of osteoporosis. Osteoporos Int. March 2003;14(suppl 3):S2-S8.
2012	Feng L, Chittenden M, Schirer J, Dickinson M, Jasiuk I. Mechanical properties of porcine femoral cortical bone measured by nanoindentation. J Biomech. June 26, 2012;45(10):1775-1782.
2002	Burr DB. Targeted and nontargeted remodeling. Bone. January 2002;30(1):2-4.
2014	Cosman F, de Beur SJ, LeBoff MS, Lewiecki EM, Tanner B, Randall S, Lindsay R. Clinician’s guide to prevention and treatment of osteoporosis. Osteoporos Int. October 2014;25(10):2359-2381.
2006	Reginster J-Y, Burlet N. Osteoporosis: a still increasing prevalence. Bone. February 2006;38(2)(suppl 1):4-9.
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.
2012	Abdel-Wahab AA, Maligno AR, Silberschmidt VV. Micro-scale modelling of bovine cortical bone fracture: analysis of crack propagation and microstructure using X-FEM. Comp Mater Sci. February 2012;52(1):128-135.
2006	Hoc T, Henry L, Verdier M, Aubry D, Sedel L, Meunier A. Effect of microstructure on the mechanical properties of Haversian cortical bone. Bone. April 2006;38(4):466-474.
2007	Bolotin HH. DXA in vivo BMD methodology: an erroneous and misleading research and clinical gauge of bone mineral status, bone fragility, and bone remodelling. Bone. July 2007;41(1):138-154.
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.
2013	Andersen TL, Abdelgawad ME, Kristensen HB, Hauge EM, Rolighed L, Bollerslev J, Kjærsgaard-Andersen P, Delaisse J-M. Understanding coupling between bone resorption and formation: are reversal cells the missing link? Am J Pathol. July 2013;183(1):235-246.
1999	Stein MS, Feik SA, Thomas CDL, Clement JG, Wark JD. An automated analysis of intracortical porosity in human femoral bone across age. J Bone Miner Res. April 1999;14(4):624-632.
1997	Rho J-Y, Tsui TY, Pharr GM. Elastic properties of human cortical and trabecular lamellar bone measured by nanoindentation. Biomaterials. 1997;18(20):1325-1330.
2007	Olszta MJ, Cheng X, Jee SS, Kumar R, Kim Y-Y, Kaufman MJ, Douglas EP, Gower LB. Bone structure and formation: a new perspective. Mater Sci Eng R Rep. November 28, 2007;58(3-5):77-116.
1998	Turner CH. Three rules for bone adaptation to mechanical stimuli. Bone. November 1998;23(5):399-407.
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.
2013	Kersh ME, Pandy MG, Bui QM, Jones AC, Arns CH, Knackstedt MA, Seeman E, Zebaze RMD. The heterogeneity in femoral neck structure and strength. J Bone Miner Res. May 2013;28(5):1022-1028.
2012	Tjong W, Kazakia GJ, Burghardt AJ, Majumdar S. The effect of voxel size on high-resolution peripheral computed tomography measurements of trabecular and cortical bone microstructure. Med Phys. April 2012;39(4):1893-1903.
2000	Jordan GR, Loveridge N, Bell KL, Power J, Rushton N, Reeve J. Spatial clustering of remodeling osteons in the femoral neck cortex: a cause of weakness in hip fracture? Bone. March 2000;26(3):305-313.
2000	Hirano T, Turner CH, Forwood MR, Johnston CC, Burr DB. Does suppression of bone turnover impair mechanical properties by allowing microdamage accumulation? Bone. July 2000;27(1):13-20.
1990	Frost HM. Skeletal structural adaptations to mechanical usage (SATMU), III: the hyaline cartilage modeling problem. Anat Rec. April 1990;226(4):423-432.
1966	Jowsey J. Studies of Haversian systems in man and some animals. J Anat. October 1966;100(4):857-864.
1999	Rho J-Y, Roy ME II, Tsui TY, Pharr GM. Elastic properties of microstructural components of human bone tissue as measured by nanoindentation. J Biomed Mater Res. 1999;A45(1):48-54.

Year

Entry

1988

Schaffler MB, Burr DB. Stiffness of compact bone: effects of porosity and density. J Biomech. 1988;21(1):13-16.

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.

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.

1992

Hogan HA. Micromechanics modeling of Haversian cortical bone properties. J Biomech. May 1992;25(5):549-556.

2001

Bousson V, Meunier A, Bergot C, Vicaut É, Rocha MA, Morais MH, Laval‐Jeantet A, Laredo J. Distribution of intracortical porosity in human midfemoral cortex by age and gender. J Bone Miner Res. July 2001;16(7):1308-1317.

2004

Bousson V, Peyrin F, Bergot C, Hausard M, Sautet A, Laredo J. Cortical bone in the human femoral neck: three‐dimensional appearance and porosity using synchrotron radiation. J Bone Miner Res. May 2004;19(5):794-801.

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.

2006

Nicolella DP, Moravits DE, Gale AM, Bonewald LF, Lankford J. Osteocyte lacunae tissue strain in cortical bone. J Biomech. 2006;39(9):1735-1743.

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.

1988

Ruff CB, Hayes WC. Sex differences in age‐related remodeling of the femur and tibia. J Orthop Res. November 1988;6(6):886-896.

1999

Zysset PK, Guo XE, Hoffler CE, Moore KE, Goldstein SA. Elastic modulus and hardness of cortical and trabecular bone lamellae measured by nanoindentation in the human femur. J Biomech. October 1999;32(10):1005-1012.

2008

Budyn E, Hoc T, Jonvaux J. Fracture strength assessment and aging signs detection in human cortical bone using an X-FEM multiple scale approach. Comput Mech. September 2008;42(4):579-591.

1993

Brockstedt H, Kassem M, Eriksen EF, Mosekilde L, Melsen F. Age- and sex-related changes in iliac cortical bone mass and remodeling. Bone. July–August 1993;14(4):681-691.

2003

Wang X, Ni Q. Determination of cortical bone porosity and pore size distribution using a low field pulsed NMR approach. J Orthop Res. March 2003;21(2):312-319.

2003

Turner CH, Robling AG. Designing exercise regimens to increase bone strength. Exerc Sport Sci Rev. January 2003;31(1):45-50.

1997

Feik SA, Thomas CDL, Clement JG. Age‐related changes in cortical porosity of the midshaft of the human femur. J Anat. October 1997;191(3):407-416.

2012

Verbruggen SW, Vaughan TJ, McNamara LM. Strain amplification in bone mechanobiology: a computational investigation of the in vivo mechanics of osteocytes. J R Soc Interface. October 7, 2012;9(75):2735-2744.

2003

Stone KL, Seeley DG, Lui L-Y, Cauley JA, Ensrud K, Browner WS, Nevitt MC, Cummings SR; The Study of Osteoporotic Fractures research group. BMD at multiple sites and risk of fracture of multiple types: long-term results from the study of osteoporotic fractures. J Bone Miner Res. November 2003;18(11):1947-1954.

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.

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.

1999

Bell KL, Loveridge N, Power J, Garrahan N, Meggitt BF, Reeve J. Regional differences in cortical porosity in the fractured femoral neck. Bone. January 1999;24(1):57-64.

1998

Akiva U, Wagner HD, Weiner S. Modelling the three-dimensional elastic constants of parallel-fibred and lamellar bone. J Mater Sci. March 15, 1998;33(6):1497-1509.

2016

Granke M, Makowski AJ, Uppuganti S, Nyman JS. Prevalent role of porosity and osteonal area over mineralization heterogeneity in the fracture toughness of human cortical bone. J Biomech. September 6, 2016;49(13):2748-2755.

2004

Bayraktar HH, Morgan EF, Niebur GL, Morris GE, Wong EK, Keaveny TM. Comparison of the elastic and yield properties of human femoral trabecular and cortical bone tissue. J Biomech. January 2004;37(1):27-35.

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.

2006

Thomas CDL, Feik SA, Clement JG. Increase in pore area, and not pore density, is the main determinant in the development of porosity in human cortical bone. J Anat. August 2006;209(2):219-230.

2015

Zebaze R, Seeman E. Cortical bone: a challenging geography. J Bone Miner Res. January 2015;30(1):24-29.

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.

1993

Rho JY, Ashman RB, Turner CH. Young's modulus of trabecular and cortical bone material: ultrasonic and microtensile measurements. J Biomech. February 1993;26(2):111-119.

2014

Bala Y, Zebaze R, Ghasem-Zadeh A, Atkinson EJ, Iuliano S, Peterson JM, Amin S, Bjørnerem Å, Melton LJ III, Johansson H, Kanis JA, Khosla S, Seeman E. Cortical porosity identifies women with osteopenia at increased risk for forearm fractures. J Bone Miner Res. June 2014;29(6):1356-1362.

1996

Prendergast PJ, Huiskes R. Microdamage and osteocyte-lacuna strain in bone: a microstructural finite element analysis. J Biomech Eng. May 1996;118(2):240-246.

1987

Frost HM. Bone “mass” and the “mechanostat”: a proposal. Anat Rec. September 1987;219(1):1-9.

2005

Thomas CDL, Feik SA, Clement JG. Regional variation of intracortical porosity in the midshaft of the human femur: age and sex differences. J Anat. February 2005;206(2):115-125.

1999

Turner CH, Rho J, Takano Y, Tsui TY, Pharr GM. The elastic properties of trabecular and cortical bone tissues are similar: results from two microscopic measurement techniques. J Biomech. April 1999;32(4):437-441.

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.

2003

Cooper DML, Turinsky AL, Sensen CW, Hallgrímsson B. Quantitative 3D analysis of the canal network in cortical bone by micro-computed tomography. Anat Rec. September 2003;274B(1):169-179.

2006

Dong XN, Guo XE. Prediction of cortical bone elastic constants by a two-level micromechanical model using a generalized self-consistent method. J Biomech Eng. June 2006;128(3):309-316.

2006

Augat P, Schorlemmer S. The role of cortical bone and its microstructure in bone strength. Age Ageing. September 2006;35(suppl 2):ii27-ii31.

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.

1993

McCalden RW, McGeough JA, Barker MB, Court-Brown CM. Age-related changes in the tensile properties of cortical bone: the relative importance of changes in porosity, mineralization, and microstructure. J Bone Joint Surg. 1993;75A(8):1193-1205.

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.

2000

Smit TH, Burger EH. Is BMU-coupling a strain-regulated phenomenon? a finite element analysis. J Bone Miner Res. February 2000;12(2):301-307.

2003

Seeman E. Reduced bone formation and increased bone resorption: rational targets for the treatment of osteoporosis. Osteoporos Int. March 2003;14(suppl 3):S2-S8.

2012

Feng L, Chittenden M, Schirer J, Dickinson M, Jasiuk I. Mechanical properties of porcine femoral cortical bone measured by nanoindentation. J Biomech. June 26, 2012;45(10):1775-1782.

2002

Burr DB. Targeted and nontargeted remodeling. Bone. January 2002;30(1):2-4.

2014

Cosman F, de Beur SJ, LeBoff MS, Lewiecki EM, Tanner B, Randall S, Lindsay R. Clinician’s guide to prevention and treatment of osteoporosis. Osteoporos Int. October 2014;25(10):2359-2381.

2006

Reginster J-Y, Burlet N. Osteoporosis: a still increasing prevalence. Bone. February 2006;38(2)(suppl 1):4-9.

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.

2012

Abdel-Wahab AA, Maligno AR, Silberschmidt VV. Micro-scale modelling of bovine cortical bone fracture: analysis of crack propagation and microstructure using X-FEM. Comp Mater Sci. February 2012;52(1):128-135.

2006

Hoc T, Henry L, Verdier M, Aubry D, Sedel L, Meunier A. Effect of microstructure on the mechanical properties of Haversian cortical bone. Bone. April 2006;38(4):466-474.

2007

Bolotin HH. DXA in vivo BMD methodology: an erroneous and misleading research and clinical gauge of bone mineral status, bone fragility, and bone remodelling. Bone. July 2007;41(1):138-154.

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.

2013

Andersen TL, Abdelgawad ME, Kristensen HB, Hauge EM, Rolighed L, Bollerslev J, Kjærsgaard-Andersen P, Delaisse J-M. Understanding coupling between bone resorption and formation: are reversal cells the missing link? Am J Pathol. July 2013;183(1):235-246.

1999

Stein MS, Feik SA, Thomas CDL, Clement JG, Wark JD. An automated analysis of intracortical porosity in human femoral bone across age. J Bone Miner Res. April 1999;14(4):624-632.

1997

Rho J-Y, Tsui TY, Pharr GM. Elastic properties of human cortical and trabecular lamellar bone measured by nanoindentation. Biomaterials. 1997;18(20):1325-1330.

2007

Olszta MJ, Cheng X, Jee SS, Kumar R, Kim Y-Y, Kaufman MJ, Douglas EP, Gower LB. Bone structure and formation: a new perspective. Mater Sci Eng R Rep. November 28, 2007;58(3-5):77-116.

1998

Turner CH. Three rules for bone adaptation to mechanical stimuli. Bone. November 1998;23(5):399-407.

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.

2013

Kersh ME, Pandy MG, Bui QM, Jones AC, Arns CH, Knackstedt MA, Seeman E, Zebaze RMD. The heterogeneity in femoral neck structure and strength. J Bone Miner Res. May 2013;28(5):1022-1028.

2012

Tjong W, Kazakia GJ, Burghardt AJ, Majumdar S. The effect of voxel size on high-resolution peripheral computed tomography measurements of trabecular and cortical bone microstructure. Med Phys. April 2012;39(4):1893-1903.

2000

Jordan GR, Loveridge N, Bell KL, Power J, Rushton N, Reeve J. Spatial clustering of remodeling osteons in the femoral neck cortex: a cause of weakness in hip fracture? Bone. March 2000;26(3):305-313.

2000

Hirano T, Turner CH, Forwood MR, Johnston CC, Burr DB. Does suppression of bone turnover impair mechanical properties by allowing microdamage accumulation? Bone. July 2000;27(1):13-20.

1990

Frost HM. Skeletal structural adaptations to mechanical usage (SATMU), III: the hyaline cartilage modeling problem. Anat Rec. April 1990;226(4):423-432.

1966

Jowsey J. Studies of Haversian systems in man and some animals. J Anat. October 1966;100(4):857-864.

1999

Rho J-Y, Roy ME II, Tsui TY, Pharr GM. Elastic properties of microstructural components of human bone tissue as measured by nanoindentation. J Biomed Mater Res. 1999;A45(1):48-54.

Year	Entry
2018	Muckatira SK. Error Estimation in Whole Bone Microstrain Measurement When Using Digital Volume Correlation [Master's thesis]. University of Illinois at Urbana-Champaign; 2018.
2019	Livingston E. Morphological and Mechanical Analysis of the Porous Structure of Cortical Bone [Master's thesis]. University of Illinois at Urbana-Champaign; 2019.

Year

Entry

2018

Muckatira SK. Error Estimation in Whole Bone Microstrain Measurement When Using Digital Volume Correlation [Master's thesis]. University of Illinois at Urbana-Champaign; 2018.

2019

Livingston E. Morphological and Mechanical Analysis of the Porous Structure of Cortical Bone [Master's thesis]. University of Illinois at Urbana-Champaign; 2019.