Skip to main content
Top
Published in: Clinical Orthopaedics and Related Research® 8/2011

01-08-2011 | Symposium: Bone Quality: From Bench to Bedside

Functional Interactions Among Morphologic and Tissue Quality Traits Define Bone Quality

Author: Karl J. Jepsen, PhD

Published in: Clinical Orthopaedics and Related Research® | Issue 8/2011

Login to get access

Abstract

Background

Advances in diagnostic and treatment regimens that aim to reduce fracture incidence will benefit from a better understanding of how bone morphology and tissue quality define whole-bone mechanical properties.

Questions/purposes

The goal of this article was to review what is known about the interactions among morphologic and tissue quality traits and how these interactions contribute to bone quality (ie, whole-bone mechanical function). Several questions were addressed. First, how do interactions among morphology and tissue quality traits relate to functional adaptation? Second, what are the emergent patterns of functionally adapted trait sets in long bones? Third, how effective is phenotypic integration at establishing function across a population? Fourth, what are the emergent patterns of functionally adapted trait sets in corticocancellous structures? Fifth, how do functional interactions change with aging?

Methods

A literature review was conducted with papers identified primarily through citations listed in reference sections as well as general searches using Google Scholar and PubMed.

Results

The interactions among adult traits or phenotypic integration are an emergent property of the compensatory mechanisms complex systems used to establish function or homeostasis. Traits are not regulated independently but vary simultaneously (ie, covary) in specific ways to establish function. This covariation results in individuals acquiring unique sets of traits to establish bone quality.

Conclusions and Clinical Relevance

Biologic constraints imposed on the skeletal system result in a population showing a pattern of trait sets that is predictable based on external bone size and that can be used to identify individuals with reduced bone quality relative to their bone size and body size.
Literature
1.
go back to reference Albright F, Smith PH, Richardson AM. Post-menopausal osteoporosis: its clinical features. JAMA. 1941;116:2465–2474. Albright F, Smith PH, Richardson AM. Post-menopausal osteoporosis: its clinical features. JAMA. 1941;116:2465–2474.
2.
go back to reference Beck TJ, Ruff CB, Shaffer RA, Betsinger K, Trone DW, Brodine SK. Stress fracture in military recruits: gender differences in muscle and bone susceptibility factors. Bone. 2000;27:437–444.PubMedCrossRef Beck TJ, Ruff CB, Shaffer RA, Betsinger K, Trone DW, Brodine SK. Stress fracture in military recruits: gender differences in muscle and bone susceptibility factors. Bone. 2000;27:437–444.PubMedCrossRef
3.
go back to reference Bell KL, Loveridge N, Power J, Garrahan N, Stanton M, Lunt M, Meggitt BF, Reeve J. Structure of the femoral neck in hip fracture: cortical bone loss in the inferoanterior to superoposterior axis. J Bone Miner Res. 1999;14:111–119.PubMedCrossRef Bell KL, Loveridge N, Power J, Garrahan N, Stanton M, Lunt M, Meggitt BF, Reeve J. Structure of the femoral neck in hip fracture: cortical bone loss in the inferoanterior to superoposterior axis. J Bone Miner Res. 1999;14:111–119.PubMedCrossRef
4.
go back to reference Black DM, Bouxsein ML, Marshall LM, Cummings SR, Lang TF, Cauley JA, Ensrud KE, Nielson CM, Orwoll ES. Proximal femoral structure and the prediction of hip fracture in men: a large prospective study using QCT. J Bone Miner Res. 2008;23:1326–1333.PubMedCrossRef Black DM, Bouxsein ML, Marshall LM, Cummings SR, Lang TF, Cauley JA, Ensrud KE, Nielson CM, Orwoll ES. Proximal femoral structure and the prediction of hip fracture in men: a large prospective study using QCT. J Bone Miner Res. 2008;23:1326–1333.PubMedCrossRef
5.
go back to reference Bonadio J, Jepsen KJ, Mansoura MK, Jaenisch R, Kuhn JL, Goldstein SA. A murine skeletal adaptation that significantly increases cortical bone mechanical properties: implications for human skeletal fragility. J Clin Invest. 1993;92:1697–1705.PubMedCrossRef Bonadio J, Jepsen KJ, Mansoura MK, Jaenisch R, Kuhn JL, Goldstein SA. A murine skeletal adaptation that significantly increases cortical bone mechanical properties: implications for human skeletal fragility. J Clin Invest. 1993;92:1697–1705.PubMedCrossRef
6.
go back to reference Bousson V, Le Bras A, Roqueplan F, Kang Y, Mitton D, Kolta S, Bergot C, Skalli W, Vicaut E, Kalender W, Engelke K, Laredo JD. Volumetric quantitative computed tomography of the proximal femur: relationships linking geometric and densitometric variables to bone strength: role for compact bone. Osteoporos Int. 2006;17:855–864.PubMedCrossRef Bousson V, Le Bras A, Roqueplan F, Kang Y, Mitton D, Kolta S, Bergot C, Skalli W, Vicaut E, Kalender W, Engelke K, Laredo JD. Volumetric quantitative computed tomography of the proximal femur: relationships linking geometric and densitometric variables to bone strength: role for compact bone. Osteoporos Int. 2006;17:855–864.PubMedCrossRef
7.
go back to reference Brear K, Currey JD, Pond CM. Ontogenetic changes in the mechanical properties of the femur of the polar bear Ursus maritimus. J Zool (Lond). 1990;222:49–58.CrossRef Brear K, Currey JD, Pond CM. Ontogenetic changes in the mechanical properties of the femur of the polar bear Ursus maritimus. J Zool (Lond). 1990;222:49–58.CrossRef
8.
go back to reference Carrier D, Leon LR. Skeletal growth and function in the California gull (Larus californicus). J Zool (Lond). 1990;222:375–389.CrossRef Carrier D, Leon LR. Skeletal growth and function in the California gull (Larus californicus). J Zool (Lond). 1990;222:375–389.CrossRef
9.
go back to reference Carrier DR. Postnatal ontogeny of the musculo-skeletal system in the black-tailed jack rabbit. J Zool (Lond). 1983;201:27–55.CrossRef Carrier DR. Postnatal ontogeny of the musculo-skeletal system in the black-tailed jack rabbit. J Zool (Lond). 1983;201:27–55.CrossRef
10.
go back to reference Chan GM, Hess M, Hollis J, Book LS. Bone mineral status in childhood accidental fractures. Am J Dis Child. 1984;138:569–570.PubMed Chan GM, Hess M, Hollis J, Book LS. Bone mineral status in childhood accidental fractures. Am J Dis Child. 1984;138:569–570.PubMed
11.
go back to reference Cheverud JM. Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution. 1982;36:499–516.CrossRef Cheverud JM. Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution. 1982;36:499–516.CrossRef
12.
go back to reference Cheverud JM. Developmental integration and the evolution of pleiotropy. Am Zool. 1996;36:44–50. Cheverud JM. Developmental integration and the evolution of pleiotropy. Am Zool. 1996;36:44–50.
13.
go back to reference Crawford RP, Cann CE, Keaveny TM. Finite element models predict in vitro vertebral body compressive strength better than quantitative computed tomography. Bone. 2003;33:744–750.PubMedCrossRef Crawford RP, Cann CE, Keaveny TM. Finite element models predict in vitro vertebral body compressive strength better than quantitative computed tomography. Bone. 2003;33:744–750.PubMedCrossRef
14.
go back to reference Crossley K, Bennell KL, Wrigley T, Oakes BW. Ground reaction forces, bone characteristics, and tibial stress fracture in male runners. Med Sci Sports Exerc. 1999;31:1088–1093.PubMedCrossRef Crossley K, Bennell KL, Wrigley T, Oakes BW. Ground reaction forces, bone characteristics, and tibial stress fracture in male runners. Med Sci Sports Exerc. 1999;31:1088–1093.PubMedCrossRef
15.
go back to reference Crow JF. The origins, patterns and implications of human spontaneous mutation. Nat Rev Genet. 2000;1:40–47.PubMedCrossRef Crow JF. The origins, patterns and implications of human spontaneous mutation. Nat Rev Genet. 2000;1:40–47.PubMedCrossRef
16.
go back to reference Currey JD. Mechanical properties of bone tissues with greatly differing functions. J Biomech. 1979;12:313–319.PubMedCrossRef Currey JD. Mechanical properties of bone tissues with greatly differing functions. J Biomech. 1979;12:313–319.PubMedCrossRef
17.
go back to reference Currey JD. Effects of differences in mineralization on the mechanical properties of bone. Philos Trans R Soc Lond B Biol Sci. 1984;304:509–518.PubMedCrossRef Currey JD. Effects of differences in mineralization on the mechanical properties of bone. Philos Trans R Soc Lond B Biol Sci. 1984;304:509–518.PubMedCrossRef
18.
go back to reference Currey JD, Alexander RM. The thickness of the walls of tubular bones. J Zool (Lond). 1985;206:453–468.CrossRef Currey JD, Alexander RM. The thickness of the walls of tubular bones. J Zool (Lond). 1985;206:453–468.CrossRef
19.
go back to reference Duan Y, Beck TJ, Wang XF, Seeman E. Structural and biomechanical basis of sexual dimorphism in femoral neck fragility has its origins in growth and aging. J Bone Miner Res. 2003;18:1766–1774.PubMedCrossRef Duan Y, Beck TJ, Wang XF, Seeman E. Structural and biomechanical basis of sexual dimorphism in femoral neck fragility has its origins in growth and aging. J Bone Miner Res. 2003;18:1766–1774.PubMedCrossRef
20.
go back to reference Duan Y, Parfitt A, Seeman E. Vertebral bone mass, size, and volumetric density in women with spinal fractures. J Bone Miner Res. 1999;14:1796–1802.PubMedCrossRef Duan Y, Parfitt A, Seeman E. Vertebral bone mass, size, and volumetric density in women with spinal fractures. J Bone Miner Res. 1999;14:1796–1802.PubMedCrossRef
21.
go back to reference Duan Y, Seeman E, Turner CH. The biomechanical basis of vertebral body fragility in men and women. J Bone Miner Res. 2001;16:2276–2283.PubMedCrossRef Duan Y, Seeman E, Turner CH. The biomechanical basis of vertebral body fragility in men and women. J Bone Miner Res. 2001;16:2276–2283.PubMedCrossRef
22.
go back to reference Duan Y, Wang XF, Evans A, Seeman E. Structural and biomechanical basis of racial and sex differences in vertebral fragility in Chinese and Caucasians. Bone. 2005;36:987–998.PubMedCrossRef Duan Y, Wang XF, Evans A, Seeman E. Structural and biomechanical basis of racial and sex differences in vertebral fragility in Chinese and Caucasians. Bone. 2005;36:987–998.PubMedCrossRef
23.
go back to reference Eswaran SK, Gupta A, Adams MF, Keaveny TM. Cortical and trabecular load sharing in the human vertebral body. J Bone Miner Res. 2006;21:307–314.PubMedCrossRef Eswaran SK, Gupta A, Adams MF, Keaveny TM. Cortical and trabecular load sharing in the human vertebral body. J Bone Miner Res. 2006;21:307–314.PubMedCrossRef
24.
go back to reference Evans RK, Negus C, Antczak AJ, Yanovich R, Israeli E, Moran DS. Sex differences in parameters of bone strength in new recruits: beyond bone density. Med Sci Sports Exerc. 2008;40:S645–S653.PubMedCrossRef Evans RK, Negus C, Antczak AJ, Yanovich R, Israeli E, Moran DS. Sex differences in parameters of bone strength in new recruits: beyond bone density. Med Sci Sports Exerc. 2008;40:S645–S653.PubMedCrossRef
25.
go back to reference Fazzalari NL, Moore AJ, Byers S, Byard RW. Quantitative analysis of trabecular morphogenesis in the human costochondral junction during the postnatal period in normal subjects. Anat Rec. 1997;248:1–12.PubMedCrossRef Fazzalari NL, Moore AJ, Byers S, Byard RW. Quantitative analysis of trabecular morphogenesis in the human costochondral junction during the postnatal period in normal subjects. Anat Rec. 1997;248:1–12.PubMedCrossRef
26.
27.
go back to reference Giladi M, Milgrom C, Simkin A, Stein M, Kashtan H, Margulies J, Rand N, Chisin R, Steinberg R, Aharonson Z, Kedem R, Frankel VH. Stress fractures and tibial bone width: a risk factor. J Bone Joint Surg Br. 1987;69:326–329.PubMed Giladi M, Milgrom C, Simkin A, Stein M, Kashtan H, Margulies J, Rand N, Chisin R, Steinberg R, Aharonson Z, Kedem R, Frankel VH. Stress fractures and tibial bone width: a risk factor. J Bone Joint Surg Br. 1987;69:326–329.PubMed
28.
go back to reference Gilsanz V, Loro ML, Roe TF, Sayre J, Gilsanz R, Schulz EE. Vertebral size in elderly women with osteoporosis. Mechanical implications and relationship to fractures. J Clin Invest. 1995;95:2332–2337.PubMedCrossRef Gilsanz V, Loro ML, Roe TF, Sayre J, Gilsanz R, Schulz EE. Vertebral size in elderly women with osteoporosis. Mechanical implications and relationship to fractures. J Clin Invest. 1995;95:2332–2337.PubMedCrossRef
29.
go back to reference Glatt V, Canalis E, Stadmeyer L, Bouxsein ML. Age-related changes in trabecular architecture differ in female and male C57BL/6 J mice. J Bone Miner Res. 2007;22:1197–1207.PubMedCrossRef Glatt V, Canalis E, Stadmeyer L, Bouxsein ML. Age-related changes in trabecular architecture differ in female and male C57BL/6 J mice. J Bone Miner Res. 2007;22:1197–1207.PubMedCrossRef
30.
go back to reference Goldman HM, Bromage TG, Thomas CD, Clement JG. Preferred collagen fiber orientation in the human mid-shaft femur. Anat Rec A Discov Mol Cell Evol Biol. 2003;272:434–445.PubMedCrossRef Goldman HM, Bromage TG, Thomas CD, Clement JG. Preferred collagen fiber orientation in the human mid-shaft femur. Anat Rec A Discov Mol Cell Evol Biol. 2003;272:434–445.PubMedCrossRef
31.
go back to reference Heinrich R. Ontogenetic changes in mineralization and bone geometry in the femur of muskoxen (Ovibos moschatus). J Zool (Lond). 1999;247:215–223.CrossRef Heinrich R. Ontogenetic changes in mineralization and bone geometry in the femur of muskoxen (Ovibos moschatus). J Zool (Lond). 1999;247:215–223.CrossRef
32.
go back to reference Jepsen KJ, Courtland HW, Nadeau JH. Genetically-determined phenotype covariation networks control bone strength. J Bone Miner Res. 2010;25:1581–1593.PubMedCrossRef Jepsen KJ, Courtland HW, Nadeau JH. Genetically-determined phenotype covariation networks control bone strength. J Bone Miner Res. 2010;25:1581–1593.PubMedCrossRef
33.
go back to reference Jepsen KJ, Hu B, Tommasini SM, Courtland HW, Price C, Cordova M, Nadeau JH. Phenotypic integration of skeletal traits during growth buffers genetic variants affecting the slenderness of femora in inbred mouse strains. Mamm Genome. 2009;20:21–33.PubMedCrossRef Jepsen KJ, Hu B, Tommasini SM, Courtland HW, Price C, Cordova M, Nadeau JH. Phenotypic integration of skeletal traits during growth buffers genetic variants affecting the slenderness of femora in inbred mouse strains. Mamm Genome. 2009;20:21–33.PubMedCrossRef
34.
go back to reference Jepsen KJ, Hu B, Tommasini SM, Courtland HW, Price C, Terranova CJ, Nadeau JH. Genetic randomization reveals functional relationships among morphologic and tissue-quality traits that contribute to bone strength and fragility. Mamm Genome. 2007;18:492–507.PubMedCrossRef Jepsen KJ, Hu B, Tommasini SM, Courtland HW, Price C, Terranova CJ, Nadeau JH. Genetic randomization reveals functional relationships among morphologic and tissue-quality traits that contribute to bone strength and fragility. Mamm Genome. 2007;18:492–507.PubMedCrossRef
35.
go back to reference Karasik D, Dupuis J, Cupples LA, Beck TJ, Mahaney MC, Havill LM, Kiel DP, Demissie S. Bivariate linkage study of proximal hip geometry and body size indices: the Framingham study. Calcif Tissue Int. 2007;81:162–173.PubMedCrossRef Karasik D, Dupuis J, Cupples LA, Beck TJ, Mahaney MC, Havill LM, Kiel DP, Demissie S. Bivariate linkage study of proximal hip geometry and body size indices: the Framingham study. Calcif Tissue Int. 2007;81:162–173.PubMedCrossRef
36.
go back to reference Khosla S, Riggs BL, Atkinson EJ, Oberg AL, McDaniel LJ, Holets M, Peterson JM, Melton LJ 3rd. Effects of sex and age on bone microstructure at the ultradistal radius: a population-based noninvasive in vivo assessment. J Bone Miner Res. 2006;21:124–131.PubMedCrossRef Khosla S, Riggs BL, Atkinson EJ, Oberg AL, McDaniel LJ, Holets M, Peterson JM, Melton LJ 3rd. Effects of sex and age on bone microstructure at the ultradistal radius: a population-based noninvasive in vivo assessment. J Bone Miner Res. 2006;21:124–131.PubMedCrossRef
37.
go back to reference Kiel DP, Hannan MT, Broe KE, Felson DT, Cupples LA. Can metacarpal cortical area predict the occurrence of hip fracture in women and men over 3 decades of follow-up? Results from the Framingham Osteoporosis Study. J Bone Miner Res. 2001;16:2260–2266.PubMedCrossRef Kiel DP, Hannan MT, Broe KE, Felson DT, Cupples LA. Can metacarpal cortical area predict the occurrence of hip fracture in women and men over 3 decades of follow-up? Results from the Framingham Osteoporosis Study. J Bone Miner Res. 2001;16:2260–2266.PubMedCrossRef
38.
go back to reference Kimura K. Growth of the second metacarpal according to chronological age and skeletal maturation. Anat Rec. 1976;184:147–157.PubMedCrossRef Kimura K. Growth of the second metacarpal according to chronological age and skeletal maturation. Anat Rec. 1976;184:147–157.PubMedCrossRef
39.
go back to reference Kimura T, Amtmann E. Distribution of mechanical robustness in the human femoral shaft. J Biomech. 1984;17:41–46.PubMedCrossRef Kimura T, Amtmann E. Distribution of mechanical robustness in the human femoral shaft. J Biomech. 1984;17:41–46.PubMedCrossRef
40.
go back to reference Koller DL, Liu G, Econs MJ, Hui SL, Morin PA, Joslyn G, Rodriguez LA, Conneally PM, Christian JC, Johnston CC Jr, Foroud T, Peacock M. Genome screen for quantitative trait loci underlying normal variation in femoral structure. J Bone Miner Res. 2001;16:985–991.PubMedCrossRef Koller DL, Liu G, Econs MJ, Hui SL, Morin PA, Joslyn G, Rodriguez LA, Conneally PM, Christian JC, Johnston CC Jr, Foroud T, Peacock M. Genome screen for quantitative trait loci underlying normal variation in femoral structure. J Bone Miner Res. 2001;16:985–991.PubMedCrossRef
41.
go back to reference Kozloff KM, Carden A, Bergwitz C, Forlino A, Uveges TE, Morris MD, Marini JC, Goldstein SA. Brittle IV mouse model for osteogenesis imperfecta IV demonstrates postpubertal adaptations to improve whole bone strength. J Bone Miner Res. 2004;19:614–622.PubMedCrossRef Kozloff KM, Carden A, Bergwitz C, Forlino A, Uveges TE, Morris MD, Marini JC, Goldstein SA. Brittle IV mouse model for osteogenesis imperfecta IV demonstrates postpubertal adaptations to improve whole bone strength. J Bone Miner Res. 2004;19:614–622.PubMedCrossRef
42.
go back to reference Lai YM, Qin L, Hung VW, Chan KM. Regional differences in cortical bone mineral density in the weight-bearing long bone shaft—a pQCT study. Bone. 2005;36:465–471.PubMedCrossRef Lai YM, Qin L, Hung VW, Chan KM. Regional differences in cortical bone mineral density in the weight-bearing long bone shaft—a pQCT study. Bone. 2005;36:465–471.PubMedCrossRef
43.
go back to reference Landin L, Nilsson BE. Bone mineral content in children with fractures. Clin Orthop Relat Res. 1983;178:292–296.PubMed Landin L, Nilsson BE. Bone mineral content in children with fractures. Clin Orthop Relat Res. 1983;178:292–296.PubMed
44.
go back to reference Lanyon L, Skerry T. Postmenopausal osteoporosis as a failure of bone’s adaptation to functional loading: a hypothesis. J Bone Miner Res. 2001;16:1937–1947.PubMedCrossRef Lanyon L, Skerry T. Postmenopausal osteoporosis as a failure of bone’s adaptation to functional loading: a hypothesis. J Bone Miner Res. 2001;16:1937–1947.PubMedCrossRef
45.
go back to reference Li R, Tsaih SW, Shockley K, Stylianou IM, Wergedal J, Paigen B, Churchill GA. Structural model analysis of multiple quantitative traits. PLoS Genetics. 2006;2:e114.PubMedCrossRef Li R, Tsaih SW, Shockley K, Stylianou IM, Wergedal J, Paigen B, Churchill GA. Structural model analysis of multiple quantitative traits. PLoS Genetics. 2006;2:e114.PubMedCrossRef
46.
go back to reference Lotz JC, Cheal EJ, Hayes WC. Stress distributions within the proximal femur during gait and falls: implications for osteoporotic fracture. Osteoporos Int. 1995;5:252–261.PubMedCrossRef Lotz JC, Cheal EJ, Hayes WC. Stress distributions within the proximal femur during gait and falls: implications for osteoporotic fracture. Osteoporos Int. 1995;5:252–261.PubMedCrossRef
47.
go back to reference Manske SL, Liu-Ambrose T, Cooper DM, Kontulainen S, Guy P, Forster BB, McKay HA. Cortical and trabecular bone in the femoral neck both contribute to proximal femur failure load prediction. Osteoporos Int. 2009;20:445–453.PubMedCrossRef Manske SL, Liu-Ambrose T, Cooper DM, Kontulainen S, Guy P, Forster BB, McKay HA. Cortical and trabecular bone in the femoral neck both contribute to proximal femur failure load prediction. Osteoporos Int. 2009;20:445–453.PubMedCrossRef
48.
go back to reference Marder E, Goaillard JM. Variability, compensation and homeostasis in neuron and network function. Nat Rev Neurosci. 2006;7:563–574.PubMedCrossRef Marder E, Goaillard JM. Variability, compensation and homeostasis in neuron and network function. Nat Rev Neurosci. 2006;7:563–574.PubMedCrossRef
50.
go back to reference Melton LJ 3rd, Wahner HW, Richelson LS, O’Fallon WM, Riggs BL. Osteoporosis and the risk of hip fracture. Am J Epidemiol. 1986;124:254–261.PubMed Melton LJ 3rd, Wahner HW, Richelson LS, O’Fallon WM, Riggs BL. Osteoporosis and the risk of hip fracture. Am J Epidemiol. 1986;124:254–261.PubMed
51.
go back to reference Milgrom C, Giladi M, Simkin A, Rand N, Kedem R, Kashtan H, Stein M, Gomori M. The area moment of inertia of the tibia: a risk factor for stress fractures. J Biomech. 1989;22:1243–1248.PubMedCrossRef Milgrom C, Giladi M, Simkin A, Rand N, Kedem R, Kashtan H, Stein M, Gomori M. The area moment of inertia of the tibia: a risk factor for stress fractures. J Biomech. 1989;22:1243–1248.PubMedCrossRef
53.
go back to reference Olson EC, Miller RL Morphological Integration. Chicago, IL: The University of Chicago Press, Ltd; 1958. Olson EC, Miller RL Morphological Integration. Chicago, IL: The University of Chicago Press, Ltd; 1958.
54.
go back to reference Pandey N, Bhola S, Goldstone A, Chen F, Chrzanowski J, Terranova CJ, Ghillani R, Jepsen KJ. Inter-individual variation in functionally adapted trait sets is established during post-natal growth and predictable based on bone robusticity. J Bone Miner Res. 2009;24:1969–1980.PubMedCrossRef Pandey N, Bhola S, Goldstone A, Chen F, Chrzanowski J, Terranova CJ, Ghillani R, Jepsen KJ. Inter-individual variation in functionally adapted trait sets is established during post-natal growth and predictable based on bone robusticity. J Bone Miner Res. 2009;24:1969–1980.PubMedCrossRef
55.
go back to reference Papadimitriou HM, Swartz SM, Kunz TH. Ontogenetic and anatomic variation in mineralization of the wing skeleton of the Mexican free-tailed bat, Tadarida brasiliensis. J Zool (Lond). 1996;240:411–426.CrossRef Papadimitriou HM, Swartz SM, Kunz TH. Ontogenetic and anatomic variation in mineralization of the wing skeleton of the Mexican free-tailed bat, Tadarida brasiliensis. J Zool (Lond). 1996;240:411–426.CrossRef
56.
go back to reference Pearson OM. Activity, climate, and postcranial robusticity: implications for modern human origins and scenarios of adaptive change. Curr Anthropol. 2000;41:569–607.PubMedCrossRef Pearson OM. Activity, climate, and postcranial robusticity: implications for modern human origins and scenarios of adaptive change. Curr Anthropol. 2000;41:569–607.PubMedCrossRef
57.
go back to reference Price CP, Herman BC, Lufkin T, Goldman HM, Jepsen KJ. Genetic variation in bone growth patterns defines adult mouse bone fragility. J Bone Miner Res. 2005;20:1983–1991.PubMedCrossRef Price CP, Herman BC, Lufkin T, Goldman HM, Jepsen KJ. Genetic variation in bone growth patterns defines adult mouse bone fragility. J Bone Miner Res. 2005;20:1983–1991.PubMedCrossRef
58.
go back to reference Riggs BL, Melton LJ 3rd, Robb RA, Camp JJ, Atkinson EJ, Peterson JM, Rouleau PA, McCollough CH, Bouxsein ML, Khosla S. Population-based study of age and sex differences in bone volumetric density, size, geometry, and structure at different skeletal sites. J Bone Miner Res. 2004;19:1945–1954.PubMedCrossRef Riggs BL, Melton LJ 3rd, Robb RA, Camp JJ, Atkinson EJ, Peterson JM, Rouleau PA, McCollough CH, Bouxsein ML, Khosla S. Population-based study of age and sex differences in bone volumetric density, size, geometry, and structure at different skeletal sites. J Bone Miner Res. 2004;19:1945–1954.PubMedCrossRef
59.
go back to reference Rivadeneira F, Houwing-Duistermaat JJ, Vaessen N, Vergeer-Drop JM, Hofman A, Pols HA, Van Duijn CM, Uitterlinden AG. Association between an insulin-like growth factor I gene promoter polymorphism and bone mineral density in the elderly: the Rotterdam Study. J Clin Endocrinol Metab. 2003;88:3878–3884.PubMedCrossRef Rivadeneira F, Houwing-Duistermaat JJ, Vaessen N, Vergeer-Drop JM, Hofman A, Pols HA, Van Duijn CM, Uitterlinden AG. Association between an insulin-like growth factor I gene promoter polymorphism and bone mineral density in the elderly: the Rotterdam Study. J Clin Endocrinol Metab. 2003;88:3878–3884.PubMedCrossRef
60.
go back to reference Rivadeneira F, Zillikens MC, De Laet CE, Hofman A, Uitterlinden AG, Beck TJ, Pols HA. Femoral neck BMD is a strong predictor of hip fracture susceptibility in elderly men and women because it detects cortical bone instability: the Rotterdam Study. J Bone Miner Res. 2007;22:1781–1790.PubMedCrossRef Rivadeneira F, Zillikens MC, De Laet CE, Hofman A, Uitterlinden AG, Beck TJ, Pols HA. Femoral neck BMD is a strong predictor of hip fracture susceptibility in elderly men and women because it detects cortical bone instability: the Rotterdam Study. J Bone Miner Res. 2007;22:1781–1790.PubMedCrossRef
61.
go back to reference Rubin CT, Lanyon LE. Dynamic strain similarity in vertebrates; an alternative to allometric limb bone scaling. J Theor Biol. 1984;107:321–327.PubMedCrossRef Rubin CT, Lanyon LE. Dynamic strain similarity in vertebrates; an alternative to allometric limb bone scaling. J Theor Biol. 1984;107:321–327.PubMedCrossRef
62.
go back to reference 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. 2006;129:484–498.PubMedCrossRef 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. 2006;129:484–498.PubMedCrossRef
63.
go back to reference Ruff CB. Body size, body shape, and long bone strength in modern humans. J Hum Evol. 2000;38:269–290.PubMedCrossRef Ruff CB. Body size, body shape, and long bone strength in modern humans. J Hum Evol. 2000;38:269–290.PubMedCrossRef
64.
go back to reference Rutherford SL. From genotype to phenotype: buffering mechanisms and the storage of genetic information. Bioessays. 2000;22:1095–1105.PubMedCrossRef Rutherford SL. From genotype to phenotype: buffering mechanisms and the storage of genetic information. Bioessays. 2000;22:1095–1105.PubMedCrossRef
65.
go back to reference Rutherford SL, Lindquist S. Hsp90 as a capacitor for morphological evolution. Nature. 1998;396:336–342.PubMedCrossRef Rutherford SL, Lindquist S. Hsp90 as a capacitor for morphological evolution. Nature. 1998;396:336–342.PubMedCrossRef
66.
go back to reference Selker F, Carter DR. Scaling of long bone fracture strength with animal mass. J Biomech. 1989;22:1175–1183.PubMedCrossRef Selker F, Carter DR. Scaling of long bone fracture strength with animal mass. J Biomech. 1989;22:1175–1183.PubMedCrossRef
67.
go back to reference Silva MJ, Gibson LJ. Modeling the mechanical behavior of vertebral trabecular bone: effects of age-related changes in microstructure. Bone. 1997;21:19119–9.CrossRef Silva MJ, Gibson LJ. Modeling the mechanical behavior of vertebral trabecular bone: effects of age-related changes in microstructure. Bone. 1997;21:19119–9.CrossRef
68.
go back to reference Skedros JG, Mendenhall SD, Kiser CJ, Winet H. Interpreting cortical bone adaptation and load history by quantifying osteon morphotypes in circularly polarized light images. Bone. 2009;44:392–403.PubMedCrossRef Skedros JG, Mendenhall SD, Kiser CJ, Winet H. Interpreting cortical bone adaptation and load history by quantifying osteon morphotypes in circularly polarized light images. Bone. 2009;44:392–403.PubMedCrossRef
69.
go back to reference Spadaro JA, Werner FW, Brenner RA, Fortino MD, Fay LA, Edwards WT. Cortical and trabecular bone contribute strength to the osteopenic distal radius. J Orthop Res. 1994;12:211–218.PubMedCrossRef Spadaro JA, Werner FW, Brenner RA, Fortino MD, Fay LA, Edwards WT. Cortical and trabecular bone contribute strength to the osteopenic distal radius. J Orthop Res. 1994;12:211–218.PubMedCrossRef
70.
go back to reference Szulc P, Seeman E, Duboeuf F, Sornay-Rendu E, Delmas PD. Bone fragility: failure of periosteal apposition to compensate for increased endocortical resorption in postmenopausal women. J Bone Miner Res. 2006;21:1856–1863.PubMedCrossRef Szulc P, Seeman E, Duboeuf F, Sornay-Rendu E, Delmas PD. Bone fragility: failure of periosteal apposition to compensate for increased endocortical resorption in postmenopausal women. J Bone Miner Res. 2006;21:1856–1863.PubMedCrossRef
71.
go back to reference Tabensky A, Duan Y, Edmonds J, Seeman E. The contribution of reduced peak accrual of bone and age-related bone loss to osteoporosis at the spine and hip: insights from the daughters of women with vertebral or hip fractures. J Bone Miner Res. 2001;16:1101–1107.PubMedCrossRef Tabensky A, Duan Y, Edmonds J, Seeman E. The contribution of reduced peak accrual of bone and age-related bone loss to osteoporosis at the spine and hip: insights from the daughters of women with vertebral or hip fractures. J Bone Miner Res. 2001;16:1101–1107.PubMedCrossRef
72.
go back to reference Tanck E, Homminga J, van Lenthe GH, Huiskes R. Increase in bone volume fraction precedes architectural adaptation in growing bone. Bone. 2001;28:650–654.PubMedCrossRef Tanck E, Homminga J, van Lenthe GH, Huiskes R. Increase in bone volume fraction precedes architectural adaptation in growing bone. Bone. 2001;28:650–654.PubMedCrossRef
73.
go back to reference Tommasini SM, Hu B, Nadeau JH, Jepsen KJ. Phenotypic integration among trabecular and cortical bone traits establishes mechanical functionality of inbred mouse vertebrae. J Bone Miner Res. 2009;24:606–620.PubMedCrossRef Tommasini SM, Hu B, Nadeau JH, Jepsen KJ. Phenotypic integration among trabecular and cortical bone traits establishes mechanical functionality of inbred mouse vertebrae. J Bone Miner Res. 2009;24:606–620.PubMedCrossRef
74.
go back to reference Tommasini SM, Nasser P, Hu B, Jepsen KJ. Biological co-adaptation of morphological and composition traits contributes to mechanical functionality and skeletal fragility. J Bone Miner Res. 2008;23:236–246.PubMedCrossRef Tommasini SM, Nasser P, Hu B, Jepsen KJ. Biological co-adaptation of morphological and composition traits contributes to mechanical functionality and skeletal fragility. J Bone Miner Res. 2008;23:236–246.PubMedCrossRef
75.
go back to reference Tommasini SM, Nasser P, Schaffler MB, Jepsen KJ. Relationship between bone morphology and bone quality in male tibias: implications for stress fracture risk. J Bone Miner Res. 2005;20:1372–1380.PubMedCrossRef Tommasini SM, Nasser P, Schaffler MB, Jepsen KJ. Relationship between bone morphology and bone quality in male tibias: implications for stress fracture risk. J Bone Miner Res. 2005;20:1372–1380.PubMedCrossRef
76.
go back to reference Ural A, Vashishth D. Interactions between microstructural and geometrical adaptation in human cortical bone. J Orthop Res. 2006;24:1489–1498.PubMedCrossRef Ural A, Vashishth D. Interactions between microstructural and geometrical adaptation in human cortical bone. J Orthop Res. 2006;24:1489–1498.PubMedCrossRef
77.
go back to reference van der Meulen MC, Jepsen KJ, Mikic B. Understanding bone strength: size isn’t everything. Bone. 2001;29:101–104.PubMedCrossRef van der Meulen MC, Jepsen KJ, Mikic B. Understanding bone strength: size isn’t everything. Bone. 2001;29:101–104.PubMedCrossRef
78.
go back to reference Vega E, Ghiringhelli G, Mautalen C, Rey Valzacchi G, Scaglia H, Zylberstein C. Bone mineral density and bone size in men with primary osteoporosis and vertebral fractures. Calcif Tissue Int. 1998;62:465–469.PubMedCrossRef Vega E, Ghiringhelli G, Mautalen C, Rey Valzacchi G, Scaglia H, Zylberstein C. Bone mineral density and bone size in men with primary osteoporosis and vertebral fractures. Calcif Tissue Int. 1998;62:465–469.PubMedCrossRef
79.
go back to reference Waarsing JH, Day JS, Verhaar JA, Ederveen AG, Weinans H. Bone loss dynamics result in trabecular alignment in aging and ovariectomized rats. J Orthop Res. 2006;24:926–935.PubMedCrossRef Waarsing JH, Day JS, Verhaar JA, Ederveen AG, Weinans H. Bone loss dynamics result in trabecular alignment in aging and ovariectomized rats. J Orthop Res. 2006;24:926–935.PubMedCrossRef
80.
go back to reference Wallace JM, Rajachar RM, Allen MR, Bloomfield SA, Robey PG, Young MF, Kohn DH. Exercise-induced changes in the cortical bone of growing mice are bone- and gender-specific. Bone. 2007;40:1120–1127.PubMedCrossRef Wallace JM, Rajachar RM, Allen MR, Bloomfield SA, Robey PG, Young MF, Kohn DH. Exercise-induced changes in the cortical bone of growing mice are bone- and gender-specific. Bone. 2007;40:1120–1127.PubMedCrossRef
81.
go back to reference Wright S. On the nature of size factors. Genetics. 1918;3:367–374.PubMed Wright S. On the nature of size factors. Genetics. 1918;3:367–374.PubMed
82.
go back to reference Zebaze RM, Jones A, Knackstedt M, Maalouf G, Seeman E. Construction of the femoral neck during growth determines its strength in old age. J Bone Miner Res. 2007;22:1055–1061.PubMedCrossRef Zebaze RM, Jones A, Knackstedt M, Maalouf G, Seeman E. Construction of the femoral neck during growth determines its strength in old age. J Bone Miner Res. 2007;22:1055–1061.PubMedCrossRef
Metadata
Title
Functional Interactions Among Morphologic and Tissue Quality Traits Define Bone Quality
Author
Karl J. Jepsen, PhD
Publication date
01-08-2011
Publisher
Springer-Verlag
Published in
Clinical Orthopaedics and Related Research® / Issue 8/2011
Print ISSN: 0009-921X
Electronic ISSN: 1528-1132
DOI
https://doi.org/10.1007/s11999-010-1706-9

Other articles of this Issue 8/2011

Clinical Orthopaedics and Related Research® 8/2011 Go to the issue

Symposium: Bone Quality: From Bench to Bedside

Diseases Affecting Bone Quality: Beyond Osteoporosis

Symposium: UHMWPE for Arthroplasty: From Powder to Debris

Do First-generation Highly Crosslinked Polyethylenes Oxidize In Vivo?