Ontogenetic and Regional Morphologic Variations in the Turkey Ulna Diaphysis: Implications for Functional Adaptation of Cortical Bone

Anatomical Record - Part A Discoveries in Molecular, Cellular, and Evolutionary Biology

Volumn 273, Issue 1, 2003, Pages 609-629

  Skedros, John G ^a   Hunt, Kenneth J ^a   Hughes, Paul E ^a   Winet, Howard ^b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b JOINT REPLACEMENT INSTITUTE   (United States)

Author keywords

Bone adaptation; Collagen fiber orientation; Osteocyte lacunae; Osteons; Turkey ulna

Indexed keywords

COLLAGEN FIBER;

ANIMAL TISSUE; ARTICLE; BONE DENSITY; BONE MINERAL; BONE STRUCTURE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; CORRELATION ANALYSIS; CORTICAL BONE; FLOW KINETICS; FLUID FLOW; MALE; MORPHOLOGICAL TRAIT; NONHUMAN; ONTOGENY; OSTEOCYTE; POROSITY; PRIORITY JOURNAL; SHEAR FLOW; SHEAR RATE; THICKNESS; TURKEY (BIRD); ULNA;

ANIMALIA; AVES; FRAXINUS; LACUNA; MELEAGRIS GALLOPAVO;

EID: 0242643488     PISSN: 0003276X     EISSN: None     Source Type: Journal    
DOI: 10.1002/ar.a.10073     Document Type: Article

References (184)

1. Adams DJ, Spirt AA, Brown TD, Fritton SP, Rubin CT, Brand RA. 1997. Testing the daily stress stimulus theory of bone adaptation with natural and experimentally controlled strain histories. J Biomech 30:671-678.
2. Alexander RM. 1998. Symmorphosis and safety factors. In: Weibel ER, Taylor CR, Bolis L, editors. Principles of animal design: the optimization and symmorphosis debate. Cambridge, UK: Cambridge University Press. p 28-35.
3. Amprino R, Sisto L. 1946. Analogies et différences de structure dans les différentes régions d'un mème os. Acta Anat 2:202-214.
4. Amtmann E, Schmitt HP. 1968. On the distribution of cortex density in the human femoral shaft and its significance for the determination of bone consistency. Z Anat Entwicklungsgesch 127:24-41.
5. Ardizzoni A. 2001. Osteocyte lacunar size-lamellar thickness relationships in human secondary osteons. Bone 28:215-219.
6. Ascenzi A, Boyde A, Portigliatti Barbos M, Carando S. 1987. Micro-biomechanics vs. macro-biomechanics in cortical bone. A mechanical investigation of femurs deformed in bending. J Biomech 20: 1045-1053.
7. Bertram JEA, Swartz SM. 1991. The 'law of bone transformation': a case of crying Wolff? Biol Rev 66:245-273.
8. Bertram JEA, Biewener AA. 1988. Bone curvature: sacrificing strength for load predictability? J Theor Biol 131:75-92.
9. Biewener AA. 1993. Safety factors in bone strength. Calcif Tissue Int 53:S68-S74.
10. Biewener AA, Bertram JEA. 1993a. Skeletal strain patterns in relation to exercise training during growth. J Exp Biol 185:51-69.
11. Biewener AA, Bertram JEA. 1993b. Mechanical loading and bone growth in vivo. In: Hall BK, editor. Bone. Vol. VII. Bone growth, part B. Boca Raton, FL: CRC Press. p 1-36.
12. Biewener AA, Bertram JEA. 1994. Structural response of growing bone to exercise and disuse. J Appl Physiol 76:946-955.
13. Biewener AA, Swartz SM, Bertram JEA. 1986. Bone modeling during growth: dynamic strain equilibrium in the chick tibiotarsus. Calcif Tissue Int 39:390-395.
14. Boskey AL, Wright TM, Blank RD. 1999. Collagen and bone strength. J Bone Miner Res 14:330-335.
15. Bouvier M, Hylander WL. 1996. The mechanical or metabolic function of secondary osteonal bone in the monkey Macaca fascicularis. Archs Oral Biol 41:941-950.
16. Brown TD, Pedersen DR, Gray ML, Brand RA, Rubin CT. 1990. Toward an identification of mechanical parameters initiating periosteal remodeling: a combined experimental and analytic approach. J Biomech 23:893-905.
17. Burger EH, Klein-Nulend J. 1999. Mechanotransduction in bone-role of the lacunocanalicular network. FASEB J 13(Suppl):S101-S112.
18. Burr DB, Ruff CB, Thompson DD. 1990. Patterns of skeletal histologic change through time: comparison of an archaic native American population with modern populations. Anat Rec 226:307-313.
19. Cane V, Marotti G, Volpi G, Zaffe D, Palazzini S, Romaggi F, Muglia MA. 1982. Size and density of osteocyte lacunae in different regions of long bones. Calcif Tissue Int 34:558-563.
20. Carando S, Portigliatti Barbos M, Ascenzi A, Boyde A. 1989. Orientation of collagen in human tibial and fibula shaft and possible correlation with mechanical properties. Bone 10:139-142.
21. Carando S, Portigliatti Barbos M, Ascenzi A, Riggs CM, Boyde A. 1991. Macroscopic shape of and lamellar distribution within, the upper limb shafts, allowing inferences about mechanical properties. Bone 12:265-269.
22. Carrier DR. 1983. Postnatal ontogeny of the musculo-skeletal system in the black-tailed jack rabbit (Lepus californicus). J Zool Lond 201:27-55.
23. Carrier DR, Leon LR. 1990. Skeletal growth and function of the California gull (Larus californicus). J Zool Lond 222:375-389.
24. Carter DR, Smith DJ, Spengler DM, Daly CH, Frankel VH. 1980. Measurements and analysis of in vivo strains on the canine radius and ulna. J Biomech 13:27-38.
25. Carter DR, Caler WE, Spengler DM, Frankel VH. 1981. Uniaxial fatigue of human cortical bone. The influence of tissue physical characteristics. J Biomech 14:461-470.
26. Carter DR, Beaupré GS, Giori NJ, Helms JA. 1998. Mechanobiology of skeletal regulation. Clin Orthop Relat Res 355(Suppl):S41-S55.
27. Cullinane DM. 2001. The role of osteocytes in bone regulation: mineral homeostasis versus mechanoreception. J Musculoskeletal Neuronal Interact 2:90.
28. Currey JD. 1984. The mechanical adaptations of bones. Princeton, NJ: Princeton University Press. 294 p.
29. Currey JD, Alexander R McN. 1985. The thickness of the walls of tubular bones. J Zool Lond (A) 206:453-468.
30. de Margerie E. 2002. Laminar bone as an adaptation to torsional loads in flapping flight. J Anat 2016:521-526.
31. de Ricqlès A, Meunier FJ, Castanet L, Francillon-Vieillot H. 1991. Comparative microstructure of bone. In: Hall BK, editor. Bone. Vol. III. Boca Raton, FL: CRC Press. p 1-78.
32. Doden E. 1987. Zur strukturellen variation der langen skeletelemente der hand als greif- und/oder lokomotionsorgan Referat. Verh Anat Ges 81:253-269.
33. Dunstan CR, Lauren PD, Somers NM, Evans RA. 1993. Measurement of osteoclasts and bone resorption by automated image analysis. J Bone Miner Res 8:139-145.
34. Enlow DH. 1963. Principles of bone remodeling. Springfield, IL: Charles C. Thomas Publishing. p 1-131.
35. Ferretti M, Muglia MA, Remaggi F, Cane V, Palumbo C. 1999. Histomorphometric study on the osteocyte lacuno-canalicular network in animals of different species. II. Parallel-fibered and lamellar bones. Ital J Anat Embryol 104:121-131.
36. Frank JD, Ryan M, Kalscheur VL, Ruaux-Mason CP, Hozak RR, Muir P. 2002. Aging and accumulation of microdamage in canine bone. Bone 30:201-206.
37. Fritton SP, Rubin CT. 2001. In vivo measurement of bone deformations using strain gauges. In: Cowin SC, editor. Bone mechanics handbook. 2nd ed. Boca Raton, FL: CRC Press. p 8.1-8.41.
38. Fritton SP, McLeod KJ, Rubin CT. 2000. Quantifying the strain history of bone: spatial uniformity and self-similarity of low-magnitude strains. J Biomech 33:317-325.
39. Frost HM. 1986. Intermediary organization of the skeleton. Vol. 1. Boca Raton, FL: CRC Press. 365 p.
40. Frost HM. 1988a. Structural adaptations to mechanical usage. A proposed "three-way rule" for bone modeling. Part I. Vet Comp Orthop Traumatol 1:7-17.
41. Frost HM. 1988b. Structural adaptations to mechanical usage. A proposed "three-way rule" for bone modeling. Part II. Vet Comp Orthop Traumatol 2:80-85.
42. Fyhrie DP, Kimura JH. 1999. NACOB presentation keynote lecture. Cancellous bone biomechanics. North American Congress on Biomechanics. J Biomech 32:1139-1148.
43. Fyhrie DP, Vashishth D. 2000. Bone stiffness predicts strength similarly for human vertebral cancellous bone in compression and for cortical bone in tension. Bone 26:73-169.
44. Gies AA, Carter DR. 1982. Experimental determination of whole long bone sectional properties. J Biomech 15:297-303.
45. Gross TS, McLeod KJ, Rubin CT. 1992. Characterizing bone strain distributions in vivo using three triple rosette strain gauges. J Biomech 25:1081-1087.
46. Gross TS, Edwards JL, McLeod KJ, Rubin CT. 1997. Strain gradients correlate with sites of periosteal bone formation. J Bone Miner Res 12:982-988.
47. Grynpas M. 1993. Age and disease-related changes in the mineral of bone. Calcif Tissue Int 53(Suppl):S57-S64.
48. Heinrich RE, Ruff CB, Adamczewski JZ. 1999. Ontogenetic changes in mineralization and bone geometry in the femur of muskoxen (Ovibos moschatus). J Zool Lond 247:215-223.
49. Hinkle DE, Wiersma W, Jurs WG. 1979. Applied statistics for the behavioral sciences. Chicago, IL: Rand McNally College Publishing Co. p 84-85.
50. Hodges ERS. 1989. Guild handbook of scientific illustration. New York: Van Nostrand Reinhold. p 341-343.
51. Hunt KJ, Skedros JG. 2001. The role of osteocyte lacunae populations in interpreting loading history of bone. Am J Phys Anthrop 32(Suppl):83.
52. Indrekvan K, Husby OS, Gjerdet NR, Engesaeter LB, Langeland N. 1991. Age-dependent mechanical properties of rat femur. Measured in vivo and in vitro. Acta Orthop Scand 62:248-252.
53. Jacobs CR, Yellowley CE, Davis BR, Zhou Z, Cimbala JM, Donahue HJ. 1998. Differential effect of steady versus oscillating flow on bone cells. J Biomech 31:969-976.
54. Jee WSS, Li XJ, Ke HZ. 1991. The skeletal adaptation to mechanical usage in the rat. Cells Mater (Suppl) 1:131-142.
55. Jepsen KJ, Davy DT. 1997. Comparison of damage accumulation measures in human cortical bone. J Biomech 30:891-894.
56. Judex S, Gross TS, Zernicke RF. 1997. Strain gradients correlate with sites of exercise-induced bone-forming surfaces in the adult skeleton. J Bone Miner Res 12:1737-1745.
57. Kachigan SK. 1986. Statistical analysis: an interdisciplinary introduction to univariate & multivariate methods. New York: Radius Press. 589 p.
58. Kalmey JK, Lovejoy CO. 2002. Collagen fiber orientation in the femoral necks of apes and humans: do their histological structures reflect differences in locomotor loading? Bone 312:327-332.
59. Keller TS, Spengler DM. 1989. Regulation of bone stress and strain in the immature and mature rat femur. J Biomech 22:1115-1127.
60. Kimura T, Amtmann E. 1984. Distribution of mechanical robustness in the human femoral shaft. J Biomech 17:41-46.
61. Knothe Tate ML, Knothe U, Niederer P. 1998. Experimental elucidation of mechanical load-induced fluid flow and its potential role in bone metabolism and function adaptation. Am J Med Sci 34:189-195.
62. Knothe Tate ML, Niederer P. 1998. A theoretical FE-based model developed to predict the relative contribution of convective and diffusive transport mechanisms for the maintenance of local equilibria within cortical bone. Advances in heat and mass transfer in biotechnology. HTD-362/BED-40:133-142.
63. Knothe Tate ML, Steck R, Forwood MR, Niederer P. 2000. In vivo demonstration of load-induced fluid flow in the rat tibia and its potential implications for processes associated with functional adaptation. J Exp Biol 203:2737-2745.
64. Lanyon LE, Baggott DG. 1976. Mechanical function as an influence on the structure and form of bone. J Bone Joint Surg 58-B:436-443.
65. Lanyon LE, Bourn S. 1979. The influence of mechanical function on the development and remodeling of the tibia: an experimental study in sheep. J Bone Joint Surg 61A:263-273.
66. Lanyon LE. 1987. Functional strain in bone tissue as an objective, and controlling stimulus for adaptive bone remodelling. J Biomech 20: 1083-1093.
67. Lanyon LE, Magee PT, Baggott DG. 1979. The relationship of functional stress and strain to the processes of bone remodelling: an experimental study on the sheep radius. J Biomech 12:593-600.
68. Les CM. 1995. Material heterogeneity in the equine metacarpus: documentation and biomechanical consequences. Ph.D. dissertation, University of California-Davis, Davis, CA.
69. Lieberman DE, Crompton AW. 1998. Responses of bone to stress: constraints on symmorphosis. In: Weibel ER, Taylor CR, Bolis L, editors. Principles of animal design: the optimization and symmorphosis debate. Cambridge: Cambridge University Press. p 78-86.
70. Lucas AM, Stettenheim PR. 1972. Avian anatomy: integument. Part I. Washington, D.C.: U.S. Government Printing Office. 340 p.
71. Marotti G. 1976. Map of bone formation rate values throughout the skeleton of the dog. In: Proceedings of the 1st workshop on bone morphometry. Ottawa: Ottawa University Press. p 202-207.
72. Marotti G, Cane V, Palazzini S, Palumbo C. 1990. Structure-function relationships in the osteocyte. Ital J Miner Electrolyte Metab 4:93-106.
73. Marotti G. 1996. The structure of bone tissues and the cellular control of their deposition. Ital J Anat Embryol 101:25-79.
74. Martin RB, Atkinson PJ. 1977. Age and sex-related changes in the structure and strength of the human femoral shaft. J Biomech 10:223-231.
75. Martin RB, Pickett JC, Zinaich S. 1980. Studies of skeletal remodeling in aging men. Clin Orthop 149:268-282.
76. Martin RB, Burr DB. 1989. Structure, function and adaptation of compact bone. New York: Raven Press. 275 p.
77. Martin RB, Ishida J. 1989. The relative effects of collagen fiber orientation, porosity, density, and mineralization on bone strength. J Biomech 22:419-426.
78. Martin RB. 1993. Aging and strength of bone as a structural material. Calcif Tissue Int 53(Suppl 1):S34-S40.
79. Martin RB, Mathews PV, Lau ST, Gibson VA, Stover SM. 1996a. Use of circularly vs. plane polarized light to quantify collagen fiber orientation in bone. Trans Orthop Res Soc 21:606.
80. Martin RB, Mathews PV, Lau ST, Gibson VA, Stover SM. 1996b. Collagen fiber organization is related to mechanical properties and remodeling in equine bone. A comparison of two methods. J Biomech 29:1515-1521.
81. Martin RB. 2000. Does osteocyte formation cause the nonlinear refilling of osteons? Bone 26:71-78.
82. Martin RB. 2002. Is all cortical bone remodeling initiated by micro-damage? Bone 30:8-13.
83. Mason MW, Skedros JG, Bloebaum RD. 1995. Evidence of strain-mode-related cortical adaptation in the diaphysis of the horse radius. Bone 17:229-237.
84. McDonald F, Pitt Ford TR. 1993. Blood flow changes in the tibia during external loading. J Orthop Res 11:36-48.
85. McLeod KJ, Rubin CT, Otter MW, Qin YX. 1998. Skeletal cell stresses and bone adaptation. Am J Med Sci 316:176-183.
86. McMahon JM, Boyde A, Bromage TG. 1995. Pattern of collagen fiber orientation in the ovine calcaneal shaft and its relation to locomotor-induced strain. Anat Rec 242:147-158.
87. Mullender MG, Huiskes R. 1995. Proposal for the regulatory mechanism of Wolff's law. J Orthop Res 13:503-512.
88. Mullender MG, Huiskes R, Versleyen H, Buma P. 1996a. Osteocyte density and histomorphometric parameters in cancellous bone of the proximal femur in five mammalian species. J Orthop Res 14: 972-979.
89. Mullender MG, van der Meer DD, Huiskes R, Lips P. 1996b. Osteocyte density changes in aging and osteoporosis. Bone 18:109-113.
90. Mullender MG, Huiskes R. 1997. Osteocytes and bone lining cells: which are the best candidates for mechano-sensors in cancellous bone? Bone 20:527-532.
91. Nagurka ML, Hayes SC. 1980. An interactive graphics package for calculating cross-sectional properties of complex shapes. J Biomech 13:59-64.
92. Norman TL, Nivargikar SV, Burr DB. 1996. Resistance to crack growth in human cortical bone is greater in shear than in tension. J Biomech 29:1023-1031.
93. Nunamaker DM, Butterweck DM, Black J. 1987. Fatigue fractures in thoroughbred racehorses: relationship with age and strain. Trans Orthop Res Soc 12:72.
94. Nunamaker DM, Butterweck DM, Provost MT. 1990. Fatigue fractures in thoroughbred racehorses: relationships with age, peak bone strain, and training. J Orthop Res 8:604-611.
95. Ohman JC, Lovejoy CO. 2001. The shape of a long bone's shaft: bending stress or growth plate form? Am J Phys Anthrop 32(Suppl): 115.
96. Owan I, Burr DB, Turner CH, Qiu J, Tu Y, Onyia JE, Duncan RL. 1997. Mechanotransduction in bone: osteoblasts are more responsive to fluid forces than mechanical strain. Am J Physiol Cell Physiol 273:C810-C815.
97. Oyen OJ, Russell MD. 1982. Histogenesis of the craniofacial skeleton and models of facial growth. In: McNamara Jr JA, Carlson DS, Ribbens KA, editors. The effect of surgical intervention on craniofacial growth. Monograph no. 12, craniofacial growth series. Ann Arbor, MI: Center for Human Growth and Development, University of Michigan. p 361-372.
98. Parfitt AM, Mundy GR, Roodman GD, Hughes DE, Boyce BF. 1996. A new model for the regulation of bone resorption, with particular reference to the effects of bisphosphonates. J Bone Miner Res 11: 150-159.
99. Parfitt AM. 2002. Misconceptions 2: turnover is always higher in cancellous than in cortical bone. Bone 30:807-809.
100. Pearson O, Lieberman D. 2002. Effects of age and exercise on long bone modeling and remodeling. Am J Phys Anthropol 34(Suppl): 123.
101. Pidaparti RMV, Turner CH. 1997. Cancellous bone architecture: advantages of nonorthogonal trabecular alignment under multidirectional loading. J Biomech 30:979-983.
102. Pollack SR. 2001. Streaming potentials in bone. In: Cowin SC, editor. Bone mechanics handbook. 2nd ed. Boca Raton, FL: CRC Press. p 24.1-24.22.
103. Portigliatti Barbos M, Bianco P, Ascenzi A. 1983. Distribution of osteonic and interstitial components in the human femoral shaft with reference to structure, calcification and mechanical properties. Acta Anat 115:178-186.
104. Portigliatti Barbos M, Bianco P, Ascenzi A, Boyde A. 1984. Collagen orientation in compact bone: II. Distribution of lamellae in the whole of the human femoral shaft with reference to its mechanical properties. Metab Bone Dis Relat Res 5:309-315.
105. Power J, Noble BS, Loveridge N, Bell KL, Rushton N, Reeve J. 2001. Osteocyte lacunar occupancy in the femoral neck cortex: an association with cortical remodeling in hip fracture cases and controls. Calcif Tissue Int 69:13-19.
106. Proctor NS, Lynch PJ. 1993. Manual of ornithology: avian structure & function. New Haven, CT: Yale University Press. 340 p.
107. Puustjarvi K, Nieminen J, Rasanen T, Hyttinen M, Helminen HJ, Kroger H, Huuskonen J, Alhava E, Kovanen V. 1999. Do more highly organized collagen fibrils increase bone mechanical strength in loss of mineral density after one-year running training? J Bone Miner Res 14:321-329.
108. Qin L, Mak AT, Cheng CW, Hung LK, Chan KM. 1999. Histomorphological study on pattern of fluid movement in cortical bone in goats. Anat Rec 255:380-387.
109. Qin Y-X, Rubin CT, McLeod KJ. 1998. Nonlinear dependence of loading intensity and cycle number in the maintenance of bone mass and morphology. J Orthop Res 16:482-489.
110. Qin Y-X, Cute M, Rubin CT. 2001. The relationship between bone fluid flow and adaptation as stimulated by intramedullary hydraulic loading. Trans Orthop Res Soc 26:319.
111. Qin Y-X, Lin W, Rubin CT. 2002. The pathway of bone fluid flow as defined by in vivo intramedullary pressure and streaming potential measurements. Ann Biomed Eng 30:693-702.
112. Qiu S, Palnitkar S, Rao D. 2001. Observation on interstitial fluid flow in the lacunar-canalicular network. J Bone Miner Res 16(Suppl 1):S240.
113. Reilly GC, Currey JD, Goodship AE. 1997. Exercise of young thoroughbred horses increases impact strength of the third metacarpal bone. J Orthop Res 15:862-868.
114. Reilly GC, Currey JD. 1999. The development of microcracking and failure in bone depends on the loading mode to which it is adapted. J Exp Biol 202:543-552.
115. Reilly GC. 2000. Observations of microdamage around osteocyte lacunae in bone. J Biomech 33:1131-1134.
116. Reilly GC, Currey JD. 2000. The effects of damage and microcracking on the impact strength of bone. J Biomech 33:337-343.
117. Remaggi F, Cane V, Palumbo C, Ferretti M. 1998. Histomorphometric study on the osteocyte lacuno-canalicular network in animals of different species. I. Woven-fibered and parallel-fibered bones. Ital J Anat Embryol 103:145-155.
118. Riches PE, Everitt NM, McNally DS. 2000. Knoop microhardness anisotropy of ovine radius. J Biomech 33:1551-1557.
119. Ricos V, Pedersen DR, Brown TD, Ashman RB, Rubin CT, Brand RA. 1996. Effects of anisotropy and material axis registration on computed stress and strain distributions in the turkey ulna. J Biomech 29:261-267.
120. Riggs CM, Vaughan LC, Evans GP, Lanyon LE, Boyde A. 1993a. Mechanical implications of collagen fibre orientation in cortical bone of the equine radius. Anat Embryol 187:239-248.
121. Riggs CM, Lanyon LE, Boyde A. 1993b. Functional associations between collagen fibre orientation and locomotor strain direction in cortical bone of the equine radius. Anat Embryol 187:231-238.
122. Robling AG, Stout SD. 1999. Morphology of the drifting osteon. Cells Tissues Organs 164:192-204.
123. Rubin CT, Lanyon LE. 1985. Regulation of bone mass by mechanical strain magnitude. Calcif Tiss Int 37:411-417.
124. Rubin CT, Lanyon LE. 1987. Osteoregulatory nature of mechanical stimuli: function as a determinant of adaptive remodeling in bone. J Orthop Res 5:300-310.
125. Rubin CT, McLeod KJ, Lanyon LE. 1989. Prevention of osteoporosis by pulsed electromagnetic fields. J Bone Joint Surg Am 71A:411-417.
126. Rubin CT, Bain SD, McLeod KJ. 1992. Suppression of the osteogenic response in the aging skeleton. Calcif Tissue Int 50:306-313.
127. Rubin CT, Gross TS, McLeod KJ, Bain SD. 1995. Morphologic stages in lamellar bone formation stimulated by a potent mechanical stimulus. J Bone Miner Res 10:488-495.
128. Rubin CT, McLeod KJ. 1996. Inhibition of osteopenia by biophysical intervention. In: Marcus R, Feldman D, Kelsey J, editors. Osteoporosis. New York: Academic Press. p 351-371.
129. Rubin CT, Gross T, Qin YX, Fritton S, Guilak F, McLeod K. 1996. Differentiation of the bone-tissue remodeling response to axial and torsional loading in the turkey ulna. J Bone Joint Surg 78A:1523-1533.
130. Ruff CB. 1981. Structural changes in the lower limb bones with aging at Pecos Pueblo. Ph.D. dissertation, University of Philadelphia, Philadelphia, PA.
131. Ruff CB, Hayes WC. 1983. Cross-sectional geometry of Pecos Pueblo femora and tibiae-a biomechanical investigation: I. Method and general patterns of variation. Am J Phys Anthropol 60:359-381.
132. Ruff CB. 1989. New approaches to structural evolution of limb bones in primates. Folia Primatol 53:142-159.
133. Salzstein RA, Pollack SR, Mak AF, Petrov N. 1987. Electromechanical potentials in cortical bone. I. A continuum approach. J Biomech 20:261-270.
134. Schaffler MG, Burr DB, Jungers WL, Ruff CB. 1985. Structural and mechanical indicators of limb specialization in primates. Folia Primatol 45:61-75.
135. Shelton DR, Gibeling JC, Martin RB, Stover SM. 2000. Fatigue crack growth rates in equine cortical bone. Conference Proceedings of the American Society of Biomechanics 24th Annual Meeting, Chicago, IL. p 247-248.
136. Skedros JG, Bloebaum RD, Bachus KN, Boyce TM, Constantz B. 1993a. Influence of mineral content and composition on graylevels in backscattered electron images of bone. J Biomed Mater Res 27:57-64.
137. Skedros JG, Ota D, Bloebaum RD. 1993b. Mineral content analysis of tension/compression skeletal systems: indications of potential strain-specific differences. J Bone Miner Res 8(Suppl 1):789.
138. Skedros JG. 1994. Collagen fiber orientation in skeletal tension/compression systems: A potential role of variant strain stimuli in the maintenance of cortical bone organization. J Bone Miner Res 9(Suppl 1):S251.
139. Skedros JG, Bloebaum RD, Mason MW, Bramble DM. 1994a. Analysis of a tension/compression skeletal system: possible strain-specific differences in the hierarchical organization of bone. Anat Rec 239: 396-404.
140. Skedros JG, Mason MW, Bloebaum RD. 1994b. Differences in osteonal micromorphologies between tensile and compressive cortices of a bending skeletal system: indications of potential strain-specific differences in bone microstructure. Anat Rec 239:405-413.
141. Skedros JG, Mason MW, Nelson MC, Bloebaum RD. 1996a. Evidence of structural and material adaptation to specific strain features in cortical bone. Anat Rec 246:47-63.
142. Skedros JG, Dietch KC, Zirovich MD, Mason MW. 1996b. Uniform osteocyte lacuna population densities in a limb bone with nonuniform customary strain milieu and heterogeneous material organization. J Bone Miner Res 11(Suppl 1):S268.
143. Skedros JG, Su SC, Bloebaum RD. 1997. Biomechanical implications of mineral content and microstructural variations in cortical bone of horse, elk and sheep calcanei. Anat Rec 249:297-316.
144. Skedros JG, Kuo TY. 1999. Ontogenetic changes in regional collagen fiber orientation suggest a role for variant strain stimuli in cortical bone construction. J Bone Miner Res 14(Suppl 1):S441.
145. Skedros JG, Hughes PE, Nelson K, Winet H. 1999. Collagen fiber orientation in the proximal femur: challenging Wolff's tension/compression interpretation. J Bone Miner Res 14(Suppl 1):S441.
146. Skedros JG. 2000. Do BMUs adapt osteon cross-sectional shape for habitual tension vs. compression loading? J Bone Miner Res 15(Suppl 1):S347.
147. Skedros JG, Dayton MR, Bachus KN. 2000a. Relative effects of collagen fiber orientation, mineralization, porosity, and percent and population density of osteonal bone on equine cortical bone mechanical properties in mode-specific loading. Conference Proceedings of the American Society of Biomechanics 24th Annual Meeting, Chicago, IL. p 173-174.
148. Skedros JG, Hunt KJ, Gingell D. 2000b. Changes in osteocyte densities during skeletal organogenesis. J Bone Miner Res 15(Suppl 1):S459.
149. Skedros JG, Hunt KJ, Attaya EN, Zirovich MD. 2000c. Uniform osteocyte lacuna population densities in a limb bone with highly non-uniform strain milieu. J Bone Miner Res 15(Suppl 1):S347.
150. Skedros JG. 2001. Collagen fiber orientation: a characteristic of strain-mode-related regional adaptation in cortical bone. Bone 28: S110-S111.
151. Skedros JG, Hunt KJ, Dayton MT, Bloebaum RD, Bachus KN. 2001a. Relative contributions of material characteristics to failure properties of cortical bone in strain-mode-specific loading: implications for fragility in osteoporosis and aging. Trans Am Soc Biomech 25:215-216.
152. Skedros JG, Hunt KJ, Bachus KN. 2001b. Strain-mode-specific loading of cortical bone reveals an important role for collagen fiber orientation in energy absorption. Trans Orthop Res Soc 26:519.
153. Skedros JG, Mason MW, Bloebaum RD. 2001c. Modeling and remodeling in a developing artiodactyl calcaneus: a model for evaluating Frost's mechanostat hypothesis and its corollaries. Anat Rec 263: 167-185.
154. Skedros JG. 2002. Use of predominant collagen fiber orientation for interpreting cortical bone loading history: bending vs. torsion. J Bone Miner Res 17(Suppl 1):72.
155. Skedros JG, Hunt KJ, Sybrowsky CL. 2002a. Ontogenetic development of the ovine calcaneus: a model for examining the relative contributions of genetic, epigenetic, and extra-genetic stimuli. J Bone Miner Res 17(Suppl 1):81.
156. Skedros JG, Hunt KJ, Dayton MR, Bloebaum RD, Bachus, KN. 2003a. The influence of collagen fiber orientation on mechanical properties of cortical bone of an artiodactyl calcaneus: implications for broad applications in bone adaptation. Trans Orthop Res Soc 28:411.
157. Skedros JG, Sybrowsky CL, Dayton MR, Bloebaum RD, Bachus KN. 2003b. The role of osteocyte lacuna population density on the mechanical properties of cortical bone. Trans Orthop Res Soc 28:414.
158. Skedros JG, Sybrowsky CL, Parry TR, Bloebaum RD. 2003c. Regional differences in cortical bone organization and microdamage prevalence in Rocky Mountain mule deer. Anat Rec (in press).
159. 2 in osteoblasts by wall-shear stress but not mechanical strain. Am J Physiol Endrocrinol Metab 273:E751-E758.
160. Smit TH, Burger EH. 2000. Is BMU-coupling a strain-regulated phenomenon? A finite element analysis. J Bone Miner Res 15:301-307.
161. Smit TH, Burger EH, Huyghe JM. 2002. A case for strain-induced fluid flow as a regulator of BMU-coupling and osteonal alignment. J Bone Miner Res 17:2021-2029.
162. Smith JW. 1960. The arrangement of collagen fibres in human secondary osteons. J Bone Joint Surg 42A:588-605.
163. Sokal RR, Rohlf FJ. 1995. Biometry. The principles and practice of statistics. 3rd ed. New York: W.H. Freeman and Co. 887 p.
164. Srinivasan S, Gross TS. 2000. Canalicular fluid flow induced by bending of a long bone. Med Eng Phys 22:127-133.
165. Steck R, Niederer P, Knothe Tate ML. 2000. A finite difference model of load-induced fluid displacements within bone under mechanical loading. Med Eng Phys 22:117-125.
166. Stover SM, Pool RR, Martin RB, Morgan JP. 1992. Histological features of the dorsal cortex of the third metacarpal bone mid-diaphysis during postnatal growth in thoroughbred horses. J Anat 1813: 455-469.
167. Su M, Borke JL, Donahue HJ, Warshawsky NM, Russell CM, Lewis JE. 1997. Expression of connexin 43 in rat mandibular bone and peridontal ligament PDL cells during experimental tooth movement. J Dent Res 76:1357-1366.
168. Su S, Skedros JG, Bloebaum RD, Bachus KN. 1999. Loading conditions and cortical construction of an artiodactyl calcaneus. J Exp Biol 202:3239-3254.
169. Swartz SM. 1993. Biomechanics of primate limbs. In: Gebo DL, editor. Postcranial adaptation in nonhuman primates. DeKalb, IL: Northern Illinois University Press. p 5-42.
170. Takano Y, Turner CH, Owan I, Martin RB, Lau ST, Forwood MR, Burr DB. 1999. Elastic anisotropy and collagen orientation of osteonal bone are dependent on the mechanical strain distribution J Orthop Res 17:59-66.
171. Turner CH, Owan I, Alvey T, Hulman J, Hock JM. 1998. Recruitment and proliferative responses of osteoblasts after mechanical loading in vivo determined using sustained-release bromodeoxyuridine. Bone 22:463-469.
172. Turner CH, Wang T, Burr DB. 2001. Shear strength and fatigue properties of human cortical bone determined from pure shear tests. Calcif Tissue Int 69:373-378.
173. van der Meulen MCH, Ashford Jr MW, Kiratli BJ, Bachrach LK, Carter DR. 1996. Determinants of femoral geometry and structure during adolescent growth. J Orthop Res 14:22-29.
174. Vashishth D, Verborgt O, Divine G, Schaffler MB, Fyhrie DP. 2000. Decline in osteocyte lacunar density in human cortical bone is associated with accumulation of microcracks with age. Bone 26: 375-380.
175. Vashishth D, Gibson G, Kimura J, Schaffler MB, Fyhrie DP. 2002. Determination of bone volume by osteocyte population. Anat Rec 267:292-295.
176. Wainwright SA, Biggs WD, Currey JD, Gosline JM. 1982. Mechanical design in organisms. Princeton, NJ: Princeton University Press. 436 p.
177. Wang L, Fritton SP, Cowin SC, Weinbaum S. 1999. Fluid pressure relaxation depends upon osteonal microstructure: modeling an oscillatory bending experiment. J Biomech 32:663-672.
178. Weinbaum S, Cowin SC, Zeng Y. 1994. A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech 27:339-360.
179. Woo SLY, Keui SC, Amiel D, Gomez MA, Hayes WC, White FC, Akeson WH. 1981. The effect of prolonged physical training on the properties of long bone: a study of Wolff's law. J Bone Joint Surg 63A:780-787.
180. Yeni YN, Norman TL. 2000. Calculation of porosity and osteonal cement line effects on the effective fracture toughness of cortical bone in longitudinal crack growth. J Biomed Mater Res 51:504-509.
181. Yeni YN, Vashishth D, Fyhrie D. 2001. Estimation of bone matrix apparent stiffness variation caused by osteocyte lacunar size and density. J Biomech Eng 123:10-17.
182. Yeni YN, Fyhrie DP. 2002. Fatigue damage-fracture mechanics interaction in cortical bone. Bone 30:509-514.
183. You J, Yellowley CE, Donahue HJ, Zhang Y, Chen Q, Jacobs CR. 2000. Substrate deformation levels associated with routine physical activity are less stimulatory to bone cells relative to loading-induced oscillatory fluid flow. J Biomech Eng 122:387-393.
184. You L, Cowin SC, Schaffler MB, Weinbaum S. 2001. A model for strain amplification in the actin cytoskeleton of osteocytes due to fluid drag on pericellular matrix. J Biomech 34:1375-1386.