Exploration of Unique Porous Bone Materials for Candidacy in Bioinspired Material Design

Bioinspired material design draws inspiration for improved technologies from unique functional adaptations found in nature. Grizzly bear (Ursus arctos horribilis), cave bear (Ursus spelaeus), edmontosaur (Edmontosaurus annectens) (Edmontosaurusregalis), and bighorn sheep (Ovis canadensis) exhibit unique functional examples of porous bone structures. Grizzly bear trabecular bone does not lose bone density during long periods of disuse. Cave bears, being larger than grizzly bears, give a unique perspective of trabecular bone property scaling relationships in animals from the near past. Edmontosaurs were expected to have grown to gigantic sizes weighing 7936±1991 kg creating a unique high force loading environment in dinosaur trabecular bone. Bighorn sheep butt heads during the mating season routinely generating near 100g accelerations and approximately 3400N forces in their horn core bone during impact. Morphological trabecular bone properties of bone volume fraction (BV/TV), trabecular thickness (Tb.Th), trabecular separation (Tb.Sp), and trabecular number (Tb.N) were examined using micro-computed tomography (µCT) imaging for the underlying trabecular bone in the proximal tibias of grizzly bear, cave bear, and edmontosaurus animals. Morphological bone properties were compared against body mass scaling relationships from extant mammals. Cave bear trabecular bone was found to have larger BV/TV and Tb.Th than modern grizzly bears. The larger BV/TV may indicate environmental drivers on cave bear trabecular bone properties. To our knowledge, the measurement of dinosaur trabecular bone properties is a novel concept. Adult edmontosaur BV/TV was measured at an average greater than 60% which was significantly different from extant species BV/TV values. Additionally, adult edmontosaurus Tb.Th, and Tb.Sp were measured at comparable values to small mammals. The difference in edmontosaur BV/TV from extant mammals may be a potential clue in why extant terrestrial animals do not reach the same levels of gigantism as dinosaurs. Additionally, mimicking the continuum properties of edmontosaur trabecular bone in an engineered foam may have potential usage in optimized high strength foams. Bighorn sheep horn core bone exhibits observational and morphological properties different from typical trabecular bone in thickness, separation and number. Due to these differences, the bighorn sheep horn core bone is being considered as a new type of porous bone architecture referred to as 'velar' bone. The velar bone morphology indicates that it is highly adapted to resist high impact bending through widely separated and thick bone formations. Future bioinspired engineering foam designs mimicking the structures of porous bone outlined in this research could be useful for energy absorption in repeated high impact loading. The work presented here does not include efforts to create a bioinspired structural foam. However, this research focuses on the quantification of porous bone structural properties optimized for unique mechanical environments for the purposes of guiding future research towards structural foam design.

Year	Entry
1989	Schaffler MB, Radin EL, Burr DB. Mechanical and morphological effects of strain rate on fatigue of compact bone. Bone. 1989;10(3):207-214.
2001	Bergmann G, Deuretzbacher G, Heller M, Graichen F, Rohlmann A, Strauss J, Duda GN. Hip contact forces and gait patterns from routine activities. J Biomech. July 2001;34(7):859-871.
2006	Bembey AK, Bushby AJ, Boyde A, Ferguson VL, Oyen ML. Hydration effects on the micro-mechanical properties of bone. J Mater Res. August 2006;21(8):1962-1968.
1999	Brodt MD, Ellis CB, Silva MJ. Growing C57Bl/6 mice increase whole bone mechanical properties by increasing geometric and material properties. J Bone Miner Res. December 1999;14(12):2159-2166.
1994	Zysset PK, Sonny M, Hayes WC. Morphology-mechanical property relations in trabecular bone of the osteoarthritic proximal tibia. J Arthoplast. 1994;9(2):203-216.
1969	Currey JD. The relationship between the stiffness and the mineral content of bone. J Biomech. October 1969;2(4):477-480.
1998	Zysset PK, Goulet RW, Hollister SJ. A global relationship between trabecular bone morphology and homogenized elastic properties. J Biomech Eng. October 1998;120(5):640-646.
1979	Currey JD. Mechanical properties of bone tissues with greatly differing functions. J Biomech. 1979;12(4):313-319.
2011	Doube M, Kłosowski MM, Wiktorowicz-Conroy AM, Hutchinson JR, Shefelbine SJ. Trabecular bone scales allometrically in mammals and birds. Proc R Soc B. October 22, 2011;278(1721):3067-3073.
1966	Sedlin‌ ED, Hirsch C. Factors affecting the determination of the physical properties of femoral cortical bone. Acta Orthop Scand. 1966;37(1):29-48.
1986	Fyhrie DP, Carter DR. A unifying principle relating stress to trabecular bone morphology. J Orthop Res. 1986;4(3):304-317.
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.
1976	Carter DR, Hayes WC. Bone compressive strength: the influence of density and strain rate. Science. September 10, 1976;194(4270):1174-1176.
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.
1987	Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR. Bone histomorphometry: standardization of nomenclature, symbols, and units: report of the ASBMR histomorphometry nomenclature committee. J Bone Miner Res. December 1987;2(6):595-610.
1987	Goldstein SA. The mechanical properties of trabecular bone: dependence on anatomic location and function. J Biomech. 1987;20(11-12):1055-1061.
1992	Turner CH. On Wolff's law of trabecular architecture. J Biomech. January 1992;25(1):1-9.
2005	Gibson LJ. Biomechanics of cellular solids. J Biomech. 2005;38(3):377-399.
1996	Sasaki N, Odajima S. Stress-strain curve and Young’s modulus of a collagen molecule as determined by the x-ray diffraction technique. J Biomech. May 1996;29(5):655-658.
2008	Meyers MA, Chen P-Y, Lin AY-M, Seki Y. Biological materials: structure and mechanical properties. Prog Mater Sci. January 2008;53(1):1-206.
2000	Legrand E, Chappard D, Pascaretti C, Duquenne M, Krebs S, Rohmer V, Basle M, Audran M. Trabecular bone microarchitecture, bone mineral density, and vertebral fractures in male osteoporosis. J Bone Miner Res. January 2000;15(1):13-19.
2000	Verborgt O, Gibson GJ, Schaffler MB. Loss of osteocyte integrity in association with microdamage and bone remodeling after fatigue in vivo. J Bone Miner Res. January 2000;15(1):60-67.
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.
1984	Currey JD. Effects of differences in mineralization on the mechanical properties of bone. Philos Trans R Soc Lond B Biol Sci. February 13, 1984;304(1121):509-518.
1999	Hildebrand T, Laib A, Müller R, Dequeker J, Rüegsegger P. Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res. July 1999;14(7):1167-1174.
1997	Hildebrand T, Rüegsegger P. A new method for the model-independent assessment of thickness in three-dimensional images. J Microsc (Oxford). 1997;185(1):67-75.
1982	Gilmore RS, Katz JL. Elastic properties of apatites. J Mater Sci. 1982;17:1131-1141.
2013	Chen H, Zhou X, Fujita H, Onozuka M, Kubo K-Y. Age-related changes in trabecular and cortical bone microstructure. Int J Endocrinol. March 18, 2013;2013:213234.
2006	Hadjidakis DJ, Androulakis II. Bone remodeling. Annals NY Acad Sci. December 2006;1092(1):385-396.
2006	Liu XS, Sajda P, Saha PK, Wehrli FW, Guo XE. Quantification of the roles of trabecular microarchitecture and trabecular type in determining the elastic modulus of human trabecular bone. J Bone Miner Res. October 2006;21(10):1608-1617.
2002	Burr DB. The contribution of the organic matrix to bone's material properties. Bone. July 2002;31(1):8-11.
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.
1991	Linde F, Nørgaard P, Hvid I, Odgaard A, Søballe K. Mechanical properties of trabecular bone: dependency on strain rate. J Biomech. 1991;24(9):803-809.
2015	Florencio-Silva R, Sasso GRdS, Sasso-Cerri E, Simões MJ, Cerri PS. Biology of bone tissue: structure, function, and factors that influence bone cells. BioMed Res Int. 2015;2015:421746.
1984	Rubin CT, Lanyon LE. Dynamic strain similarity in vertebrates: an alternative to allometric limb bone scaling. J Theo Biol. March 21, 1984;107(2):321-327.
2010	Kadir MRA, Syahrom A, Öchsner A. Finite element analysis of idealised unit cell cancellous structure based on morphological indices of cancellous bone. Med Biol Eng Comput. May 2010;48(5):497-505.
2006	Robling AG, Castillo AB, Turner CH. Biomechanical and molecular regulation of bone remodeling. Annu Rev Biomed Eng. 2006;8:455-498.
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.

Year

Entry

1989

Schaffler MB, Radin EL, Burr DB. Mechanical and morphological effects of strain rate on fatigue of compact bone. Bone. 1989;10(3):207-214.

2001

Bergmann G, Deuretzbacher G, Heller M, Graichen F, Rohlmann A, Strauss J, Duda GN. Hip contact forces and gait patterns from routine activities. J Biomech. July 2001;34(7):859-871.

2006

Bembey AK, Bushby AJ, Boyde A, Ferguson VL, Oyen ML. Hydration effects on the micro-mechanical properties of bone. J Mater Res. August 2006;21(8):1962-1968.

1999

Brodt MD, Ellis CB, Silva MJ. Growing C57Bl/6 mice increase whole bone mechanical properties by increasing geometric and material properties. J Bone Miner Res. December 1999;14(12):2159-2166.

1994

Zysset PK, Sonny M, Hayes WC. Morphology-mechanical property relations in trabecular bone of the osteoarthritic proximal tibia. J Arthoplast. 1994;9(2):203-216.

1969

Currey JD. The relationship between the stiffness and the mineral content of bone. J Biomech. October 1969;2(4):477-480.

1998

Zysset PK, Goulet RW, Hollister SJ. A global relationship between trabecular bone morphology and homogenized elastic properties. J Biomech Eng. October 1998;120(5):640-646.

1979

Currey JD. Mechanical properties of bone tissues with greatly differing functions. J Biomech. 1979;12(4):313-319.

2011

Doube M, Kłosowski MM, Wiktorowicz-Conroy AM, Hutchinson JR, Shefelbine SJ. Trabecular bone scales allometrically in mammals and birds. Proc R Soc B. October 22, 2011;278(1721):3067-3073.

1966

Sedlin‌ ED, Hirsch C. Factors affecting the determination of the physical properties of femoral cortical bone. Acta Orthop Scand. 1966;37(1):29-48.

1986

Fyhrie DP, Carter DR. A unifying principle relating stress to trabecular bone morphology. J Orthop Res. 1986;4(3):304-317.

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.

1976

Carter DR, Hayes WC. Bone compressive strength: the influence of density and strain rate. Science. September 10, 1976;194(4270):1174-1176.

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.

1987

Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR. Bone histomorphometry: standardization of nomenclature, symbols, and units: report of the ASBMR histomorphometry nomenclature committee. J Bone Miner Res. December 1987;2(6):595-610.

1987

Goldstein SA. The mechanical properties of trabecular bone: dependence on anatomic location and function. J Biomech. 1987;20(11-12):1055-1061.

1992

Turner CH. On Wolff's law of trabecular architecture. J Biomech. January 1992;25(1):1-9.

2005

Gibson LJ. Biomechanics of cellular solids. J Biomech. 2005;38(3):377-399.

1996

Sasaki N, Odajima S. Stress-strain curve and Young’s modulus of a collagen molecule as determined by the x-ray diffraction technique. J Biomech. May 1996;29(5):655-658.

2008

Meyers MA, Chen P-Y, Lin AY-M, Seki Y. Biological materials: structure and mechanical properties. Prog Mater Sci. January 2008;53(1):1-206.

2000

Legrand E, Chappard D, Pascaretti C, Duquenne M, Krebs S, Rohmer V, Basle M, Audran M. Trabecular bone microarchitecture, bone mineral density, and vertebral fractures in male osteoporosis. J Bone Miner Res. January 2000;15(1):13-19.

2000

Verborgt O, Gibson GJ, Schaffler MB. Loss of osteocyte integrity in association with microdamage and bone remodeling after fatigue in vivo. J Bone Miner Res. January 2000;15(1):60-67.

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.

1984

Currey JD. Effects of differences in mineralization on the mechanical properties of bone. Philos Trans R Soc Lond B Biol Sci. February 13, 1984;304(1121):509-518.

1999

Hildebrand T, Laib A, Müller R, Dequeker J, Rüegsegger P. Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res. July 1999;14(7):1167-1174.

1997

Hildebrand T, Rüegsegger P. A new method for the model-independent assessment of thickness in three-dimensional images. J Microsc (Oxford). 1997;185(1):67-75.

1982

Gilmore RS, Katz JL. Elastic properties of apatites. J Mater Sci. 1982;17:1131-1141.

2013

Chen H, Zhou X, Fujita H, Onozuka M, Kubo K-Y. Age-related changes in trabecular and cortical bone microstructure. Int J Endocrinol. March 18, 2013;2013:213234.

2006

Hadjidakis DJ, Androulakis II. Bone remodeling. Annals NY Acad Sci. December 2006;1092(1):385-396.

2006

Liu XS, Sajda P, Saha PK, Wehrli FW, Guo XE. Quantification of the roles of trabecular microarchitecture and trabecular type in determining the elastic modulus of human trabecular bone. J Bone Miner Res. October 2006;21(10):1608-1617.

2002

Burr DB. The contribution of the organic matrix to bone's material properties. Bone. July 2002;31(1):8-11.

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.

1991

Linde F, Nørgaard P, Hvid I, Odgaard A, Søballe K. Mechanical properties of trabecular bone: dependency on strain rate. J Biomech. 1991;24(9):803-809.

2015

Florencio-Silva R, Sasso GRdS, Sasso-Cerri E, Simões MJ, Cerri PS. Biology of bone tissue: structure, function, and factors that influence bone cells. BioMed Res Int. 2015;2015:421746.

1984

Rubin CT, Lanyon LE. Dynamic strain similarity in vertebrates: an alternative to allometric limb bone scaling. J Theo Biol. March 21, 1984;107(2):321-327.

2010

Kadir MRA, Syahrom A, Öchsner A. Finite element analysis of idealised unit cell cancellous structure based on morphological indices of cancellous bone. Med Biol Eng Comput. May 2010;48(5):497-505.

2006

Robling AG, Castillo AB, Turner CH. Biomechanical and molecular regulation of bone remodeling. Annu Rev Biomed Eng. 2006;8:455-498.

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.

Year	Entry
2020	Aguirre TG, Ingrole A, Fuller L, Seek TW, Fiorillo AR, Sertich JJW, Donahue SW. Differing trabecular bone architecture in dinosaurs and mammals contribute to stiffness and limits on bone strain. PLoS One. August 19, 2020;15(8):e0237042.
2020	Aguirre TG, Fuller L, Ingrole A, Seek TW, Wheatley BB, Steineman BD, Haut Donahue TL, Donahue SW. Bioinspired material architectures from bighorn sheep horncore velar bone for impact loading applications. Sci Rep. 2020;10:18916.
2020	Aguirre TG. Bio-Inspired Design for Engineering Applications: Empirical and Finite Element Studies of Biomechanically Adapted Porous Bone Architectures [PhD thesis]. Colorado State University; Summer 2020.
2023	Fuller LH. Structure-Function Relationships of Bighorn Sheep Horncore Bone and Horn-Horncore Interface Materials for Energy Absorption Applications [PhD thesis]. University of Massachusetts at Amherst; February 2023.

Year

Entry

2020

Aguirre TG, Ingrole A, Fuller L, Seek TW, Fiorillo AR, Sertich JJW, Donahue SW. Differing trabecular bone architecture in dinosaurs and mammals contribute to stiffness and limits on bone strain. PLoS One. August 19, 2020;15(8):e0237042.

2020

Aguirre TG, Fuller L, Ingrole A, Seek TW, Wheatley BB, Steineman BD, Haut Donahue TL, Donahue SW. Bioinspired material architectures from bighorn sheep horncore velar bone for impact loading applications. Sci Rep. 2020;10:18916.

2020

Aguirre TG. Bio-Inspired Design for Engineering Applications: Empirical and Finite Element Studies of Biomechanically Adapted Porous Bone Architectures [PhD thesis]. Colorado State University; Summer 2020.

2023

Fuller LH. Structure-Function Relationships of Bighorn Sheep Horncore Bone and Horn-Horncore Interface Materials for Energy Absorption Applications [PhD thesis]. University of Massachusetts at Amherst; February 2023.