Tissue level mechanical properties of cortical bone in skeletally immature and mature dogs

S.S. Huja; C.A. Phillips; S.A. Fernandez; Y. Li

doi:10.3415/VCOT-08-06-0053

Veterinary and Comparative Orthopaedics and Traumatology, Table of Contents

Vet Comp Orthop Traumatol 2009; 22(03): 210-215
DOI: 10.3415/VCOT-08-06-0053

Original Research

Schattauer GmbH

Tissue level mechanical properties of cortical bone in skeletally immature and mature dogs

Authors

S.S. Huja

¹Section of Orthodontics, College of Dentistry, The Ohio State University, Columbus,Ohio, USA

²Oral Biology, College of Dentistry, The Ohio State University, Columbus, Ohio, USA
C.A. Phillips

¹Section of Orthodontics, College of Dentistry, The Ohio State University, Columbus,Ohio, USA
S.A. Fernandez

³Center for Biostatistics, The Ohio State University, Columbus, Ohio, USA
Y. Li

³Center for Biostatistics, The Ohio State University, Columbus, Ohio, USA

Abstract

Summary

Objectives: The purpose of this study was to quantify the tissue level mechanical properties of cortical bone of skeletally immature (~five-month-old) Beagle dogs and compare them to data from mature dogs measured in a previous study.

Methods: Eight femoral cross sectional specimens (two bone sections / dog) were obtained from four skeletally immature dogs. A pair of calcein bone labels were administered intravenously to the dogs to mark sites of active mineralization prior to euthanasia. Prepared bone specimens were placed in a nanoindenter specimen holder and the previously identified calcein labelled osteons were located. Labelled (n = 128) and neighbouring unlabelled (n = 127) osteons in skeletally immature femurs were examined by instrumented indentation testing. Indents were made to a depth of 500 nm at a loading rate of 10 nm/s. Indentation modulus (IM) and hardness (H) were obtained.

Results: The overall IM of the cortical bone in the skeletally mature groups was significantly greater than in the immature group (p = 0.0011), however overall H was not significantly different. The differences between the groups in IM were significant for the unlabelled osteons (p = 0.001), but not for the labelled osteons (p = 0.56).

Conclusion: There are differences in the IM of unlabelled osteons in skeletally immature and mature groups of Beagle dogs. In contrast to whole bone mechanical tests, where there are obvious differences between growing and mature bones, there are only small differences in the micro-mechanical properties.

Keywords

Bone remodelling - Osteon - Nanoindentation - Age - Dog

Full Text

References

References
1 Smith JW, Walmsley R. Factors affecting the elasticity of bone. J.Anat 1959; 93: 503-523.
2 Reilly DT, Burstein AH. The mechanical properties of bone. J Bone Joint Surg Am 1974; 56 A 1001-1022.
3 Carter DR, Spengler DM. Mechanical properties and composition of cortical bone. Clin Orthop 1978; 135: 192-217.
4 Ekeland A, Engesoeter LB, Langeland N. Influence of age on mechanical properties of healing fractures and intact bones in rats. Acta Orthop Scand 1982; 53: 527-534.
5 Jonsson U, Netz P, Stromberg L. Solid mechanics and strength of bone in young dogs. Acta Orthop Scand 1984; 55: 446-451.
6 Borah B, Dufresne TE, Cockman MD. et al. Evaluation of changes in trabecular bone architecture and mechanical properties of minipig vertebrae by three-dimensional magnetic resonance micro-imaging and finite element modeling. J Bone Miner Res 2000; 15: 1786-1797.
7 Nafei A, Danielsen CC, Linde F. et al. Properties of growing trabecular ovine bone part I: mechanical and physical properties. J Bone Joint Surg Am 2000; 82-B: 910-920.
8 Nafei A, Kabel J, Odgaard A. et al. Properties of growing trabecular ovine bone part II: architectural and mechanical properties. J Bone Joint Surg Am 2000; 82-B: 921-927.
9 Bigot G, Bouzidi A, Rumelhart C. et al. Evolution during growth of the mechanical properties of the cortical bone in equine cannon-bones. Med Eng Phys 1996; 18: 79-87.
10 Kasra M, Grynpas MD. The effects of androgens on the mechanical properties of primate bone. Bone 1995; 17: 265-270.
11 Keller TS, Lovin JD, Spengler DM. et al. Fatigue of immature baboon cortical bone. J Biomech 1985; 18: 297-304.
12 Huja SS, Beck FM, Thurman DT. Indentation properties of young and old osteons. Calcif Tissue Int 2006; 78: 392-397.
13 Huja SS, Beck FM. Bone remodeling in maxilla, mandible, and femur of young dogs. Anat Rec (Hoboken) 2008; 291: 1-5.
14 Huja SS, Fernandez SA, Hill KJ. et al. Remodeling dynamics in the alveolar process in skeletally mature dogs. Anat Rec A Discov Mol Cell Evol Biol 2006; 288: 1243-1249.
15 Thompson JB, Kindt JH, Drake B. et al. Bone indentation recovery time correlates with bond reforming time. Nature 2001; 414: 773-776.
16 Busa B, Miller LM, Rubin CT. et al. Rapid establishment of chemical and mechanical properties during lamellar bone formation. Calcif Tissue Int 2005; 77: 386-394.
17 Hay JL, Pharr GM. Instrumented indentation testing. In. Kuhn H, Medlin D. (eds) ASM Handbook Mechanical Testing and Evaluation. ASM International, Materials Park, Ohio 2000; 232-243.
18 Rho J-Y, Tsui TY, Pharr GM. Elastic properties of human cortical and trabecular lamellar bone measured by nanoindentation. Biomaterials 1997; 18: 1325-1330.
19 Zysset PK, Guo XE, Hoffler CE. et al. Elastic modulus and hardness of cortical and trabecular bone lamellae measured by nanoindentation in the human femur. J Biomech 1999; 32: 1005-1012.
20 Hofmann T, Heyroth F, Meinhard H. et al. Assessment of composition and anisotropic elastic properties of secondary osteon lamellae. J Biomech 2006; 39 (12) 2282-2294.
21 Tang B, Ngan AH, Lu WW. An improved method for the measurement of mechanical properties of bone by nanoindentation. J Mater Sci Mater Med 2007; 18: 1875-1881.
22 Mulder L, Koolstra JH, den Toonder JM. et al. Relationship between tissue stiffness and degree of mineralization of developing trabecular bone. J Biomed Mater Res 2008; A 84: 508-515.
23 Cuy JL, Mann AB, Livi KJ. et al. Nanoindentation mapping of the mechanical properties of human molar tooth enamel. Arch Oral Biol 2002; 47: 281-291.
24 Habelitz S, Marshall Jr. GW, Balooch M. et al. Nanoindentation and storage of teeth. J Biomech 2002; 35: 995-998.
25 Turner CH, Burr DB. Basic biomechanical measurement of bone: a tutorial. Bone 1993; 14: 595-608.
26 Hoffler CE, Moore KE, Kozloff K. et al. Age, gender and bone lamellae elastic moduli. J Orthop Res 2000; 18: 432-437.
27 Xu J, Rho J-Y, Mishra SR. et al. Atomic force microscopy and nanoindentation characterization of human lamellar bone prepared by microtome sectioning and mechanical polishing technique. J Biomed Mater Res 2003; 67: 719-726.
28 Hoffler CE, Guo XE, Zysset PK. et al. Evaluation of bone microstructural properties: effect of testing conditions, depth, repetition, time delay and displacement rate. In: Proceeding of the ASME 1997 Bioengineering Conference. ASME, New York City, New York: 1997: 567-568.
29 Rho J-Y, Roy II ME, Tsui TY. et al. Elastic properties of microstructural components of human bone tissue as measured by nanoindentation. J Biomed Mater Res; 1999; 45: 48-54.
30 Bobji MS, Biswas SK. Estimation of hardness by nanoindentation of rough surfaces. J Mater Res 1998; 13: 3227-3233.
31 Donnelly E, Baker SP, Boskey AL. et al. Effects of surface roughness and maximum load on the mechanical properties of cancellous bone measured by nanoindentation. J Biomed Mater Res 2006; A 77: 426-435.
32 Oliver WC, Pharr GM. An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J Mater Res 1992; 7: 1564-1583.
33 Sneddon IN. The relation between load and penetration in the axisymmetric boussinesq problem for a punch of arbitary profile. Int J Eng Sci 1965; 3: 47-57.
34 Huja SS, Fernandez SA, Hill KJ. et al. Indentation modulus of the alveolar process in dogs. J Dent Res 2007; 86: 237-241.
35 Hoffler CE, Moore KE, Kozloff K. et al. Heterogeneity of bone lamellar-level elastic moduli. Bone 2000; 26: 603-609.
36 Currey JD, Butler G. The mechanical properties of bone tissue in children. J Bone Joint Surg Am 1975; 57 A 810-814.
37 Ding M, Dalstra M, Danielsen CC. et al. Age variations in the properties of human tibial trabecular bone. J Bone Joint Surg Br 1997; 79: 995-1002.
38 Huja SS, Rummel AM, Beck FM. Changes in mechanical properties of bone within the mandibular condyle with age. J Morphol 2008; 269: 138-143.
39 Christoffersen J, Landis WJ. A contribution with review to the description of mineralization of bone and other calcified tissue in vivo. Anat Rec 1991; 230: 435-450.
40 Akkus O, Adar F, Schaffler MB. Age-related changes in physicochemical properties of mineral crystals are related to impaired mechanical function of cortical bone. Bone 2004; 34: 443-453.
41 Martin RB. Osteonal remodeling in response to screw implantation in canine femora. J Orthop Res 1987; 5: 445-452.
42 Martin RB. Label escape theory revisited: the effects of resting periods and section thickness. Bone 1989; 10: 255-264.
43 Grynpas M. Age and disease-related changes in the mineral of bone. Calcif Tissue Int 1993; 53: S57-S64.
44 Boivin G, Meunier PJ. Changes in bone remodeling rate influence the degree of mineralization of bone. Connect Tissue Res 2002; 43: 535-537.