Secondary osteon size and collagen/lamellar organization (" osteon morphotypes") are not coupled, but potentially adapt independently for local strain mode or magnitude

Journal of Structural Biology

Volumn 181, Issue 2, 2013, Pages 95-107

  Skedros, John G ^a,b   Keenan, Kendra E ^a,b   Williams, Tyler J ^a,b   Kiser, Casey J ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Bone adaptation; Chimpanzee femur; Collagen orientation; Deer calcaneus; Equine calcaneus; Equine radius; Human femur; Osteon; Sheep radius; Strain magnitude; Strain mode

Indexed keywords

COLLAGEN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MATRIX; BONE METABOLISM; FEMALE; HUMAN; HUMAN TISSUE; LAMELLAR BODY; MALE; METABOLISM; MORPHOTYPE; NONHUMAN; OSTEOBLAST; OSTEON; PRIORITY JOURNAL; SHEAR STRESS; TENSION;

ADAPTATION, PHYSIOLOGICAL; ANALYSIS OF VARIANCE; ANIMALS; BIOMECHANICS; BIREFRINGENCE; BONE AND BONES; COLLAGEN; DEER; HAVERSIAN SYSTEM; HORSES; HUMANS; PAN TROGLODYTES; SHEAR STRENGTH; SHEEP;

AXIS (DEER); CERVIDAE; EQUIDAE; OVIS ARIES; PAN;

EID: 84873195474     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2012.10.013     Document Type: Article

References (65)

1. Bertram J.E., Biewener A.A. Bone curvature: sacrificing strength for load predictability?. J. Theor. Biol. 1988, 131:75-92.
2. Bigley R.F., Griffin L.V., Christensen L., Vandenbosch R. Osteonal interfacial strength and histomorphometry of equine cortical bone. J. Biomech. 2006, 39:1629-1640.
3. Boyce T.M., Fyhrie D.P., Glotkowski M.C., Radin E.L., Schaffler M.B. Damage type and strain mode associations in human compact bone bending fatigue. J. Orthop. Res. 1998, 16:322-329.
4. Boyde A., Riggs C.M. The quantitative study of the orientation of collagen in compact bone slices. Bone 1990, 11:35-39.
5. Britz H.M., Thomas C.D., Clement J.G., Cooper D.M. The relation of femoral osteon geometry to age, sex, height and weight. Bone 2009, 45:77-83.
6. Bromage T.G., Goldman H.M., McFarlin S.C., Warshaw J., Boyde A., et al. Circularly polarized light standards for investigations of collagen fiber orientation in bone. Anat. Rec. 2003, 274B:157-168.
7. Crescimanno A., Stout S.D. Differentiating fragmented human and nonhuman long bone using osteon circularity. J. Forensic Sci. 2012, 57:287-294.
8. Currey J.D. Bones: Structure and Mechanics 2002, Princeton University Press, Princeton, NJ.
9. Diab T., Vashishth D. Morphology, localization and accumulation of in vivo microdamage in human cortical bone. Bone 2007, 40:612-618.
10. Doblaré M., García Aznar J.M., Gómez M.J. Modelling bone tissue fracture and healing: a review. Eng. Fract. Mech. 2004, 71:1809-1840.
11. Donahue S.W., Galley S.A. Microdamage in bone: implications for fracture, repair, remodeling, and adaptation. Crit. Rev. Biomed. Eng. 2006, 34:215-271.
12. Ebacher V., Tang C., McKay H., Oxland T.R., Guy P., et al. Strain redistribution and cracking behavior of human bone during bending. Bone 2007, 40:1265-1275.
13. Hiller L.P., Stover S.M., Gibson V.A., Gibeling J.C., Prater C.S., et al. Osteon pullout in the equine third metacarpal bone: effects of ex vivo fatigue. J. Orthop. Res. 2003, 21:481-488.
14. Hogan H.A. Micromechanics modeling of Haversian cortical bone properties. J. Biomech. 1992, 25:549-556.
15. Keenan K., Knight A., Tingey S., Kiser C., Thomas S., et al. Drifting osteons occur in higher concentrations in habitual tension environments: a microstructural toughening mechanism?. Am. J. Phys. Anthropol. 2010, Suppl. 50:140.
16. Kerschnitzki M., Wagermaier W., Roschger P., Seto J., Shahar R., et al. The organization of the osteocyte network mirrors the extracellular matrix orientation in bone. J. Struct. Biol. 2011, 173:303-311.
17. Launey M.E., Buehler M.J., Ritchie R.O. On the mechanistic origins of toughness in bone. Annu. Rev. Mater. Res. 2010, 40:25-53.
18. Launey M.E., Chen P.Y., McKittrick J., Ritchie R.O. Mechanistic aspects of the fracture toughness of elk antler bone. Acta Biomater. 2010, 6:1505-1514.
19. Leng H., Dong X.N., Wang X. Progressive post-yield behavior of human cortical bone in compression for middle-aged and elderly groups. J. Biomech. 2009, 42:491-497.
20. Lieberman D.E., Pearson O.M., Polk J.D., Demes B., Crompton A.W. Optimization of bone growth and remodeling in response to loading in tapered mammalian limbs. J. Exp. Biol. 2003, 206:3125-3138.
21. Marotti G. The structure of bone tissues and the cellular control of their deposition. Ital. J. Anat. Embryol. 1996, 101:25-79.
22. Martin R.B., Gibson V.A., Stover S.M., Gibeling J.C., Griffin L.V. Osteonal structure in the equine third metacarpus. Bone 1996, 19:165-171.
23. Martin R.B., Burr D.B., Sharkey N.A. Skeletal Tissue Mechanics 1998, Springer-Verlag, New York, NY.
24. Mason M.W., Skedros J.G., Bloebaum R.D. Evidence of strain-mode-related cortical adaptation in the diaphysis of the horse radius. Bone 1995, 17:229-237.
25. Mohsin S., O'Brien F.J., Lee T.C. Osteonal crack barriers in ovine compact bone. J. Anat. 2006, 208:81-89.
26. Moyle D.D., Bowden R.W. Fracture of human femoral bone. J. Biomech. 1984, 17:203-213.
27. Moyle D.D., Welborn J.W., Cooke F.W. Work to fracture of canine femoral bone. J. Biomech. 1978, 11:435-440.
28. Najafi A., Arshi A., Saffar K., Eslami M., Fariborz S., et al. A fiber-ceramic matrix composite material model for osteonal cortical bone fracture micromechanics: solutions of arbitrary microcracks interaction. J. Mech. Behav. Biomed. Mater. 2009, 2:217-223.
29. Nalla R.K., Stolken J.S., Kinney J.H., Ritchie R.O. Fracture in human cortical bone: local fracture criteria and toughening mechanisms. J. Biomech. 2005, 38:1517-1525.
30. Nalla R.K., Kruzic J.J., Kinney J.H., Ritchie R.O. Mechanistic aspects of fracture and R-curve behavior in human cortical bone. Biomaterials 2005, 26:217-231.
31. Norman T.L., Wang Z. Microdamage of human cortical bone: incidence and morphology in long bones. Bone 1997, 20:375-379.
32. O'Brien F., Taylor D., Lee T.C. The effect of bone microstructure on the initiation and growth of microcracks. J. Orthop. Res. 2005, 23:475-480.
33. Parfitt A.M. The physiologic and clinical significance of bone histomorphometric data. Bone Histomorphometry: Techniques and Interpretation 1983, 143-224. CRC Press, Inc., Boca Raton, (Chapter 9). R.R. Recker (Ed.).
34. Pazzaglia U.E., Congiu T., Zarattini G., Marchese M., Quacci D. The fibrillar organisation of the osteon and cellular aspects of its development : a morphological study using the SEM fractured cortex technique. Anat. Sci. Int. 2011, 86:128-134.
35. Pope M.H., Murphy M.C. Fracture energy of bone in a shear mode. Med. Biol. Eng. 1974, 12:763-767.
36. Rasband, W., 1997-2009. ImageJ, 1.43 ed. U.S. National Institutes of Health, Bethesda, Maryland.
37. Reilly G.C., Currey J.D. The development of microcracking and failure in bone depends on the loading mode to which it is adapted. J. Exp. Biol. 1999, 202:543-552.
38. Reilly G.C., Currey J.D., Goodship A. Exercise of young thoroughbred horses increases impact strength of the third metacarpal bone. J. Orthop. Res. 1997, 15:862-868.
39. Riggs C.M., Lanyon L.E., Boyde A. Functional associations between collagen fibre orientation and locomotor strain direction in cortical bone of the equine radius. Anat. Embryol. 1993, 187:231-238.
40. Riggs C.M., Vaughan L.E., Boyde A., Lanyon L.E. Mechanical implications of collagen fibre orientation in cortical bone of the equine radius. Anat. Embryol. 1993, 187:239-248.
41. Robling A.G. The interaction of biological factors with mechanical signals in bone adaptation: recent developments. Curr. Osteoporos Rep. 2012, 10:126-131.
42. Robling A.G., Stout S.D. Morphology of the drifting osteon. Cells Tissues Organs 1999, 164:192-204.
43. Skedros J.G. Interpreting load history in limb-bone diaphyses: important considerations and their biomechanical foundations. Bone Histology: An Anthropological Perspective 2012, 153-220. CRC Press, Boca Raton, Florida. C. Crowder, S. Stout (Eds.).
44. Skedros J.G., Baucom S.L. Mathematical analysis of trabecular 'trajectories' in apparent trajectorial structures: the unfortunate historical emphasis on the human proximal femur. J. Theor. Biol. 2007, 244:15-45.
45. Skedros J.G., Mason M.W., Nelson M.C., Bloebaum R.D. Evidence of structural and material adaptation to specific strain features in cortical bone. Anat. Rec. 1996, 246:47-63.
46. Skedros J.G., Hughes P.E., Nelson K., Winet H. Collagen fiber orientation in the proximal femur: challenging Wolff's tension/compression interpretation. J. Bone Miner. Res. 1999, 14:S441.
47. Skedros J.G., Mason M.W., Bloebaum R.D. Modeling and remodeling in a developing artiodactyl calcaneus: a model for evaluating Frost's mechanostat hypothesis and its corollaries. Anat. Rec. 2001, 263:167-185.
48. Skedros J.G., Holmes J.L., Vajda E.G., Bloebaum R.D. Cement lines of secondary osteons in human bone are not mineral-deficient: new data in a historical perspective. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 2005, 286:781-803.
49. Skedros J.G., Dayton M.R., Sybrowsky C.L., Bloebaum R.D., Bachus K. The influence of collagen fiber orientation and other histocompositional characteristics on the mechanical properties of equine cortical bone. J. Exp. Biol. 2006, 209:3025-3042.
50. Skedros J.G., Sorenson S.M., Jenson N.H. Are distributions of secondary osteon variants useful for interpreting load history in mammalian bones?. Cells Tissues Organs 2007, 185:285-307.
51. Skedros J.G., Sorenson S.M., Hunt K.J., Holyoak J.D. Ontogenetic structural and material variations in ovine calcanei: a model for interpreting bone adaptation. Anat. Rec. 2007, 290:284-300.
52. Skedros J.G., Mendenhall S.D., Kiser C.J., Winet H. Interpreting cortical bone adaptation and load history by quantifying osteon morphotypes in circularly polarized light images. Bone 2009, 44:392-403.
53. Skedros J.G., Kiser C.J., Mendenhall S.D. A weighted osteon morphotype score out-performs regional osteon percent prevalence calculations for interpreting cortical bone adaptation. Am. J. Phys. Anthropol. 2011, 144:41-50.
54. Skedros J.G., Kiser C.J., Keenan K.E., Thomas S.C. Analysis of osteon morphotype scoring schemes for interpreting load history: evaluation in the chimpanzee femur. J. Anat. 2011, 218:480-499.
55. Skedros, J.G., Keenan, K.E., Halley, J.A., Knight, A.N., Bloebaum, R.D., 2012. Osteon morphotypes and predominant collagen fiber orientation are adaptations for habitual medial-lateral bending in the human proximal diaphysis: implications for understanding the etiology of atypical fractures. 58th Annual Meeting of the Orthopaedic Research Society, vol. 37, p. 1512.
56. Takano Y., Turner C.H., Owan I., Martin R.B., Lau S.T., et al. Elastic anisotropy and collagen orientation of osteonal bone are dependent on the mechanical strain distribution. J. Orthop. Res. 1999, 17:59-66.
57. Turner C.H., Burr D.B. Basic biomechanical measurements of bone: a tutorial. Bone 1993, 14:595-608.
58. van Oers R.F., Ruimerman R., van Rietbergen B., Hilbers P.A., Huiskes R. Relating osteon diameter to strain. Bone 2008, 43:476-482.
59. Vashishth D. Rising crack-growth-resistance behavior in cortical bone: implications for toughness measurements. J. Biomech. 2004, 37:943-946.
60. Wasserman N., Brydges B., Searles S., Akkus O. In vivo linear microcracks of human femoral cortical bone remain parallel to osteons during aging. Bone 2008, 43:856-861.
61. Woodward M. Epidemiology: Study Design and Data Analysis, second ed 1999, Chapman and Hall/CRC, New York.
62. Yeni Y.N., Brown C.U., Wang Z., Norman T.L. The influence of bone morphology on fracture toughness of the human femur and tibia. Bone 1997, 21:453-459.
63. Zimmermann E.A., Launey M.E., Barth H.D., Ritchie R.O. Mixed-mode fracture of human cortical bone. Biomaterials 2009, 30:5877-5884.
64. Zimmermann E.A., Schaible E., Bale H., Barth H.D., Tang S.Y., et al. Age-related changes in the plasticity and toughness of human cortical bone at multiple length scales. Proc. Natl. Acad. Sci. USA 2011, 108:14416-14421.
65. Zioupos P., Currey J.D. Changes in the stiffness, strength, and toughness of human cortical bone with age. Bone 1998, 22:57-66.