A Biomechanical Analysis of Ape and Human Thoracic Vertebrae Using Quantitative Computed Tomography Based Finite Element Models

Spontaneous vertebral fractures are common among humans, but not observed in apes. Differences in bone structure associated with increased fracture susceptibility among humans remain unclear. Our aim was to determine how vertebral bone compressive strength varies among apes and humans, and how bone loss affects differences in vertebral strength. QCT-based voxel finite element models derived from quantitative computed tomography (QCT) images of the thoracic vertebrae (T8) were created for apes and humans. Human vertebrae showed significantly reduced bone strength relative to apes with similar body mass (p<0.01) and bone mineral content (p<0.01). Bone loss simulations showed no significant differences in the effect of bone loss on strength among species. Our study suggests human vertebrae are weaker than ape vertebrae after accounting for bone mass, but are not more sensitive to age-related bone loss. Our results support the idea weaker vertebral bone contributes to the unique susceptibility of humans to vertebral fractures.

Year	Entry
1994	Silva MJ, Wang C, Keaveny TM, Hayes WC. Direct and computed tomography thickness measurements of the human, lumbar vertebral shell and endplate. Bone. July 8, 1994;15(4):409-414.
1990	Beaupré GS, Orr TE, Carter DR. An approach for time‐dependent bone modeling and remodeling: theoretical development. J Orthop Res. September 1990;8(5):651-661.
2002	Currey JD. Bones: Structure and Mechanics. Princeton, NJ: Princeton University Press; 2002.
2000	Whealan KM, Kwak SD, Tedrow JR, Inoue K, Snyder BD. Noninvasive imaging predicts failure load of the spine with simulated osteolytic defects. J Bone Joint Surg. September 2000;82A(9):1240-1251.
2001	Hernandez CJ, Beaupré GS, Keller TS, Carter DR. The influence of bone volume fraction and ash fraction on bone strength and modulus. Bone. July 2001;29(1):74-78.
1994	Keyak JH, Lee IY, Skinner HB. Correlations between orthogonal mechanical properties and density of trabecular bone: use of different densitometric measures. J Biomed Mater Res. November 1994;A28(11):1329-1336.
2006	Eswaran SK, Gupta A, Adams MF, Keaveny TM. Cortical and trabecular load sharing in the human vertebral body. J Bone Miner Res. February 2006;21(2):307-314.
2003	Crawford RP, Rosenberg WS, Keaveny TM. Quantitative computed tomography-based finite element models of the human lumbar vertebral body: effect of element size on stiffness, damage, and fracture strength predictions. J Biomech Eng. August 2003;125(4):434-438.
2007	Keaveny TM, Donley DW, Hoffmann PF, Mitlak BH, Glass EV, San Martin JA. Effects of teriparatide and alendronate on vertebral strength as assessed by finite element modeling of qct scans in women with osteoporosis. J Bone Miner Res. January 2007;22(1):149-157.
2003	Liebschner MAK, Kopperdahl DL, Rosenberg WS, Keaveny TM. Finite element modeling of the human thoracolumbar spine. Spine. March 15, 2003;28(6):559-565.
1993	Melton LJ III, Lane AW, Cooper C, Eastell R, O'Fallon WM, Riggs BL. Prevalence and incidence of vertebral deformities. Osteoporos Int. May 1993;3(3):113-119.
2002	Kopperdahl DL, Morgan EF, Keaveny TM. Quantitative computed tomography estimates of the mechanical properties of human vertebral trabecular bone. J Orthop Res. July 2002;20(4):801-805.
2000	Kopperdahl DL, Pearlman JL, Keaveny TM. Biomechanical consequences of an isolated overload on the human vertebral body. J Orthop Res. September 2000;18(5):685-690.
1997	Silva MJ, Keaveny TM, Hayes WC. Load sharing between the shell and centrum in the lumbar vertebral body. Spine. January 1997;22(2):140-150.
1990	Mosekilde L, Mosekilde L. Sex differences in age-related changes in vertebral body size, density and biomechanical competence in normal individuals. Bone. 1990;11(2):67-73.
2001	Keaveny TM. Strength of trabecular bone. In: Cowin SC, ed. Bone Mechanics Handbook. 2nd ed. Boca Raton, FL: CRC Press; 2001:16-1–16-42.
1994	Keller TS. Predicting the compressive mechanical behavior of bone. J Biomech. September 1994;27(9):1159-1168.
2001	Homminga J, Weinans H, Gowin W, Felsenberg D, Huiskes R. Ostehoporosis changes the amount of vertebral trabecular bone at risk of fracture but not the vertebral load distribution. Spine. July 2001;26(14):1555-1560.
1989	Melton LJ III, Kan SH, Frye MA, Wahner HW, O'Fallon WM, Riggs BL. Epidemiology of vertebral fractures in women. Am J Epidemiol. May 1989;129(5):1000-1011.
2002	Cummings SR, Karpf DB, Harris F, Genant HK, Ensrud K, LaCroix AZ, Black DM. Improvement in spine bone density and reduction in risk of vertebral fractures during treatment with antiresorptive drugs. Am J Med. March 2002;112(4):281-289.
1994	Keaveny TM, Wachtel EF, Ford CM, Hayes WC. Differences between the tensile and compressive strengths of bovine tibial trabecular bone depend on modulus. J Biomech. 1994;27(9):1137-1146.
2001	Cao KD, Grimm MJ, Yang K-H. Load sharing within a human lumbar vertebral body using the finite element method. Spine. June 5, 2001;26(12):E253-E260.
1997	Lewis G. Properties of acrylic bone cement: state of the art review. J Biomed Mater Res. Summer 1997;38(2):155-182.
2001	Duan Y, Turner CH, Kim B-T, Seeman E. Sexual dimorphism in vertebral fragility is more the result of gender differences in age-related bone gain than bone loss. J Bone Miner Res. December 2001;16(12):2267-2275.
2006	Hernandez CJ, Gupta A, Keaveny TM. A biomechanical analysis of the effects of resorption cavities on cancellous bone strength. J Bone Miner Res. August 2006;21(8):1248-1255.
2007	Buckley JM, Loo K, Motherway J. Comparison of quantitative computed tomography-based measures in predicting vertebral compressive strength. Bone. March 2007;40(3):767-774.
2007	Melton LJ III, Riggs BL, Keaveny TM, Achenbach SJ, Hoffmann PF, Camp JJ, Rouleau PA, Bouxsein ML, Amin S, Atkinson EJ, Robb RA, Khosla S. Structural determinants of vertebral fracture risk. J Bone Miner Res. December 2007;22(12):1885-1892.
1998	Ladd AJC, Kinney JH, Haupt DL, Goldstein SA. Finite‐element modeling of trabecular bone: comparison with mechanical testing and determination of tissue modulus. J Orthop Res. September 1998;16(5):622-628.
1993	Mosekilde L. Vertebral structure and strength in vivo and in vitro. Calcif Tiss Int. February 1993;53(suppl 1):S121-S126.
1989	Selker F, Carter DR. Scaling of long bone fracture strength with animal mass. J Biomech. 1989;22(11-12):1175-1183.
2003	Crawford RP, Cann CE, Keaveny TM. Finite element models predict in vitro vertebral body compressive strength better than quantitative computed tomography. Bone. 2003;33(4):744-750.
1995	Singer K, Edmondston S, Day R, Breidahl P, Price R. Prediction of thoracic and lumbar vertebral body compressive strength: correlations with bone mineral density and vertebral region. Bone. August 1995;17(2):167-174.
1998	Mosekilde L. The effect of modelling and remodelling on human vertebral body architecture. Technol Health Care. December 1998;6(5-6):287-297.
1999	Ulrich D, van Rietbergen B, Laib A, Rüegsegger P. The ability of three-dimensional structural indices to reflect mechanical aspects of trabecular bone. Bone. 1999;25(1):55-60.
2001	Morgan EF, Keaveny TM. Dependence of yield strain of human trabecular bone on anatomic site. J Biomech. 2001;34(5):569-577.
2000	Heaney RP, Abrams S, Dawson-Hughes B, Looker A, Marcus R, Matkovic V, Weaver C. Peak bone mass. Osteoporos Int. December 2000;11(12):985-1009.
1991	Eastell R, Cedel SL, Wahner HW, Riggs BL, Melton LJ III. Classification of vertebral fractures. J Bone Miner Res. March 1991;6(3):207-215.
1996	Wasnich RD. Vertebral fracture epidemiology. Bone. March 1996;18(3)(suppl 1):S179-S183.
1990	White AA III, Panjabi MM. Clinical Biomechanics of the Spine. 2nd ed. Philadelphia, PA: J.B. Lippincott Company; 1990.
2000	Mosekilde L. Age-related changes in bone mass, structure, and strength: effects of loading. Z Rheumatol. February 2000;59(suppl 1):I1-I9.
1998	Thomsen JS, Ebbesen EN, Mosekilde L. Relationships between static histomorphometry and bone strength measurements in human iliac crest bone biopsies author links open overlay panel. Bone. February 1998;22(2):153-163.
1998	Currey JD. Mechanical properties of vertebrate hard tissues. Proc Inst Mech Eng Part H-J Eng Med. 1998;216(6):399-411.

Year

Entry

1994

Silva MJ, Wang C, Keaveny TM, Hayes WC. Direct and computed tomography thickness measurements of the human, lumbar vertebral shell and endplate. Bone. July 8, 1994;15(4):409-414.

1990

Beaupré GS, Orr TE, Carter DR. An approach for time‐dependent bone modeling and remodeling: theoretical development. J Orthop Res. September 1990;8(5):651-661.

2002

Currey JD. Bones: Structure and Mechanics. Princeton, NJ: Princeton University Press; 2002.

2000

Whealan KM, Kwak SD, Tedrow JR, Inoue K, Snyder BD. Noninvasive imaging predicts failure load of the spine with simulated osteolytic defects. J Bone Joint Surg. September 2000;82A(9):1240-1251.

2001

Hernandez CJ, Beaupré GS, Keller TS, Carter DR. The influence of bone volume fraction and ash fraction on bone strength and modulus. Bone. July 2001;29(1):74-78.

1994

Keyak JH, Lee IY, Skinner HB. Correlations between orthogonal mechanical properties and density of trabecular bone: use of different densitometric measures. J Biomed Mater Res. November 1994;A28(11):1329-1336.

2006

Eswaran SK, Gupta A, Adams MF, Keaveny TM. Cortical and trabecular load sharing in the human vertebral body. J Bone Miner Res. February 2006;21(2):307-314.

2003

Crawford RP, Rosenberg WS, Keaveny TM. Quantitative computed tomography-based finite element models of the human lumbar vertebral body: effect of element size on stiffness, damage, and fracture strength predictions. J Biomech Eng. August 2003;125(4):434-438.

2007

Keaveny TM, Donley DW, Hoffmann PF, Mitlak BH, Glass EV, San Martin JA. Effects of teriparatide and alendronate on vertebral strength as assessed by finite element modeling of qct scans in women with osteoporosis. J Bone Miner Res. January 2007;22(1):149-157.

2003

Liebschner MAK, Kopperdahl DL, Rosenberg WS, Keaveny TM. Finite element modeling of the human thoracolumbar spine. Spine. March 15, 2003;28(6):559-565.

1993

Melton LJ III, Lane AW, Cooper C, Eastell R, O'Fallon WM, Riggs BL. Prevalence and incidence of vertebral deformities. Osteoporos Int. May 1993;3(3):113-119.

2002

Kopperdahl DL, Morgan EF, Keaveny TM. Quantitative computed tomography estimates of the mechanical properties of human vertebral trabecular bone. J Orthop Res. July 2002;20(4):801-805.

2000

Kopperdahl DL, Pearlman JL, Keaveny TM. Biomechanical consequences of an isolated overload on the human vertebral body. J Orthop Res. September 2000;18(5):685-690.

1997

Silva MJ, Keaveny TM, Hayes WC. Load sharing between the shell and centrum in the lumbar vertebral body. Spine. January 1997;22(2):140-150.

1990

Mosekilde L, Mosekilde L. Sex differences in age-related changes in vertebral body size, density and biomechanical competence in normal individuals. Bone. 1990;11(2):67-73.

2001

Keaveny TM. Strength of trabecular bone. In: Cowin SC, ed. Bone Mechanics Handbook. 2nd ed. Boca Raton, FL: CRC Press; 2001:16-1–16-42.

1994

Keller TS. Predicting the compressive mechanical behavior of bone. J Biomech. September 1994;27(9):1159-1168.

2001

Homminga J, Weinans H, Gowin W, Felsenberg D, Huiskes R. Ostehoporosis changes the amount of vertebral trabecular bone at risk of fracture but not the vertebral load distribution. Spine. July 2001;26(14):1555-1560.

1989

Melton LJ III, Kan SH, Frye MA, Wahner HW, O'Fallon WM, Riggs BL. Epidemiology of vertebral fractures in women. Am J Epidemiol. May 1989;129(5):1000-1011.

2002

Cummings SR, Karpf DB, Harris F, Genant HK, Ensrud K, LaCroix AZ, Black DM. Improvement in spine bone density and reduction in risk of vertebral fractures during treatment with antiresorptive drugs. Am J Med. March 2002;112(4):281-289.

1994

Keaveny TM, Wachtel EF, Ford CM, Hayes WC. Differences between the tensile and compressive strengths of bovine tibial trabecular bone depend on modulus. J Biomech. 1994;27(9):1137-1146.

2001

Cao KD, Grimm MJ, Yang K-H. Load sharing within a human lumbar vertebral body using the finite element method. Spine. June 5, 2001;26(12):E253-E260.

1997

Lewis G. Properties of acrylic bone cement: state of the art review. J Biomed Mater Res. Summer 1997;38(2):155-182.

2001

Duan Y, Turner CH, Kim B-T, Seeman E. Sexual dimorphism in vertebral fragility is more the result of gender differences in age-related bone gain than bone loss. J Bone Miner Res. December 2001;16(12):2267-2275.

2006

Hernandez CJ, Gupta A, Keaveny TM. A biomechanical analysis of the effects of resorption cavities on cancellous bone strength. J Bone Miner Res. August 2006;21(8):1248-1255.

2007

Buckley JM, Loo K, Motherway J. Comparison of quantitative computed tomography-based measures in predicting vertebral compressive strength. Bone. March 2007;40(3):767-774.

2007

Melton LJ III, Riggs BL, Keaveny TM, Achenbach SJ, Hoffmann PF, Camp JJ, Rouleau PA, Bouxsein ML, Amin S, Atkinson EJ, Robb RA, Khosla S. Structural determinants of vertebral fracture risk. J Bone Miner Res. December 2007;22(12):1885-1892.

1998

Ladd AJC, Kinney JH, Haupt DL, Goldstein SA. Finite‐element modeling of trabecular bone: comparison with mechanical testing and determination of tissue modulus. J Orthop Res. September 1998;16(5):622-628.

1993

Mosekilde L. Vertebral structure and strength in vivo and in vitro. Calcif Tiss Int. February 1993;53(suppl 1):S121-S126.

1989

Selker F, Carter DR. Scaling of long bone fracture strength with animal mass. J Biomech. 1989;22(11-12):1175-1183.

2003

Crawford RP, Cann CE, Keaveny TM. Finite element models predict in vitro vertebral body compressive strength better than quantitative computed tomography. Bone. 2003;33(4):744-750.

1995

Singer K, Edmondston S, Day R, Breidahl P, Price R. Prediction of thoracic and lumbar vertebral body compressive strength: correlations with bone mineral density and vertebral region. Bone. August 1995;17(2):167-174.

1998

Mosekilde L. The effect of modelling and remodelling on human vertebral body architecture. Technol Health Care. December 1998;6(5-6):287-297.

1999

Ulrich D, van Rietbergen B, Laib A, Rüegsegger P. The ability of three-dimensional structural indices to reflect mechanical aspects of trabecular bone. Bone. 1999;25(1):55-60.

2001

Morgan EF, Keaveny TM. Dependence of yield strain of human trabecular bone on anatomic site. J Biomech. 2001;34(5):569-577.

2000

Heaney RP, Abrams S, Dawson-Hughes B, Looker A, Marcus R, Matkovic V, Weaver C. Peak bone mass. Osteoporos Int. December 2000;11(12):985-1009.

1991

Eastell R, Cedel SL, Wahner HW, Riggs BL, Melton LJ III. Classification of vertebral fractures. J Bone Miner Res. March 1991;6(3):207-215.

1996

Wasnich RD. Vertebral fracture epidemiology. Bone. March 1996;18(3)(suppl 1):S179-S183.

1990

White AA III, Panjabi MM. Clinical Biomechanics of the Spine. 2nd ed. Philadelphia, PA: J.B. Lippincott Company; 1990.

2000

Mosekilde L. Age-related changes in bone mass, structure, and strength: effects of loading. Z Rheumatol. February 2000;59(suppl 1):I1-I9.

1998

Thomsen JS, Ebbesen EN, Mosekilde L. Relationships between static histomorphometry and bone strength measurements in human iliac crest bone biopsies author links open overlay panel. Bone. February 1998;22(2):153-163.

1998

Currey JD. Mechanical properties of vertebrate hard tissues. Proc Inst Mech Eng Part H-J Eng Med. 1998;216(6):399-411.

Year	Entry
2011	Cotter MM. Gross Morphology, Microarchitecture, Strength and Evolution of the Hominoid Vertebral Body [PhD thesis]. Cleveland, OH: Case Western Reserve University; May 2011.

Year

Entry

2011

Cotter MM. Gross Morphology, Microarchitecture, Strength and Evolution of the Hominoid Vertebral Body [PhD thesis]. Cleveland, OH: Case Western Reserve University; May 2011.