Modeling and remodeling responses to normal loading in the human lower limb

American Journal of Physical Anthropology

Volumn 129, Issue 3, 2006, Pages 403-409

  Drapeau, Michelle S M ^a   Streeter, Margaret A ^b  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b BOISE STATE UNIVERSITY   (United States)

Author keywords

Cross sectional geometry; Femur; Histomorphometry; Microdamage; Tibia

Indexed keywords

ARTICLE; BODY MASS; BONE STRENGTH; GEOMETRY; HUMAN; HUMAN TISSUE; LEG; LOCOMOTION; MORPHOMETRICS; STRESS FRACTURE; STUDENT T TEST; WEIGHT BEARING;

BIOMECHANICS; BODY WEIGHTS AND MEASURES; FEMALE; FEMUR; HUMANS; MALE; MODELS, THEORETICAL; TIBIA; WEIGHT-BEARING;

EID: 33144467395     PISSN: 00029483     EISSN: None     Source Type: Journal    
DOI: 10.1002/ajpa.20336     Document Type: Article

References (114)

1. Alexander RM. 1991. Characteristics and advantages of human bipedalism. In: Rayner JMV, Wootton RJ, editors. Biomechanics in evolution. Cambridge: Cambridge University Press, p 255-266.
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: Cambridge University Press, p 28-35.
3. Anderson C, Danylchuk KD. 1978. Bone-remodeling rates of the beagle: a comparison between different sites on the same rib. Am J Vet Res 39:1763-1765.
4. Bentolila V, Boyce TM, Fyhrie DP, Drumb R, Skerry TM, Schaffler MB. 1998. Bone 23:275-281.
5. Bertram JEA, Swartz SM. 1991. The "law of bone transformation:" a case of crying Wolff? Biol Rev Cambridge Philosophic Soc 66:245-273.
6. Biewener AA, Taylor CR. 1986. Bone strain: a determinant of gait and speed? J Exp Biol 123:383-400.
7. Boyce TM, Fyhrie DP, Glotkowski MC, Radin EL, Schaffler MB. 1998. Damage type and strain mode associations in human compact bone bending fatigue. J Orthop Res 16:322-329.
8. Bramble DM, Lieberman DE. 2004. Endurance running and the evolution of Homo. Nature 432:345-352.
9. Burger EH, Klein-Nulend J. 1999. Mechanotransduction in bone-role of the lacuno-canalicular network. FASEB J 13:101-112.
10. Burr DB. 2002. Targeted and nontargeted remodeling. Bone 30:2-4.
11. Burr DB, Martin RB, Schaffler MB, Radin EL. 1985. Bone remodeling in response to in vivo fatigue microdamage. J Biomech 18:189-200.
12. Burr DB, Yoshikawa T, Ruff CB. 1995. Moderate exercise increases intracortical activation frequency in old dogs. Trans Orthop Res Soc 20:204.
13. Caler WE, Carter DR. 1989. Bone creep-fatigue damage accumulation. J Biomech 22:625-635.
14. Carter DR. 1987. Mechanical loading history and skeletal biology. J Biomech 20:1095-1109.
15. Corando S, Portigliatti Barbos M, Ascenzi A, Boyde A. 1989. Orientation of collagen in human tibial and fibular shaft and possible correlation with mechanical properties. Bone 10:139-142.
16. Cowin SC. 1984. Mechanical modeling of the stress adaptation process in bone. Calcif Tissue Int 36:98-103.
17. Cowin SC. 1989. The mechanical properties of cortical bone tissue. In: Cowin SC, editor. Bone mechanics. Boca Raton, FL: CRC Press, Inc. p 97-127.
18. Currey J. 1984. The mechanical adaptations of bones. Princeton, NJ: Princeton University Press.
19. Danova NA, Colopy SA, Radtke CL, Kalscheur VL, Markel MD, Vanderby R, McCabe RP, Escarcega AJ, Muir P. 2003. Degradation of bone structural properties by accumulation and coalescence of microcracks. Bone 33:197-205.
20. Dellanini L, Hawkins D, Martin RB, Stover S. 2003. An investigation of the interactions between lower-limb bone morphology, limb inertial properties and limb dynamics. J Biomech 36:913-919.
21. Donahue SW, Jacobs CR, Dohahue HJ. 2001. Flow-induced calcium oscillations in rat osteoblasts are age, loading frequency, and shear stress dependent. Am J Physiol Cell Physiol 281:1635-1641.
22. Enlow DH. 1977. The remodeling of bone. Yrbk Phys Anthropol 20:19-34.
23. Evans FG. 1976. Mechanical properties and histology of cortical bone from younger and older men. Anat Rec 185:1-12.
24. Evans FG. 1978. Relation between torsion properties and histology of adult human compact bone. J Biomech 11:157-165.
25. Evans FG, Bang S. 1967. Differences and relationships between the physical properties and the microscopic structure of human femoral, tibial and fibular cortical bone. Am J Anat 120:79-88.
26. Evans FG, Riolo ML. 1970. Relations between the fatigue life and histology of adult human cortical bone. J Bone Joint Surg [Am] 52:1579-1586.
27. Fedak MA, Pinshow B, Schmidt-Nielsen K. 1974. Energy cost of bipedal running. Am J Physiol 227:1038-1044.
28. Forwood MR, Parker AW 1989. Microdamage in response to repetitive torsional loading in the rat tibia. Calcif Tissue Int 45:47-53.
29. Frost HM. 1958. Preparation of thin, undecalcified bone sections by a rapid manual method. Stain Technol 33:272-276.
30. Frost HM. 1960. Presence of microscopic cracks in vivo in bone. Henry Ford Hosp Med Bull 8:25-35.
31. Frost HM. 1964. Dynamics of bone remodeling. In: Frost HM, editor. Bonebiodynamics. Boston, MA: Little, Brown and Co. p 315-333.
32. Frost HM. 1973a. Bone remodeling and its relationship to metabolic bone diseases. Springfield, IL: Charles C. Thomas.
33. Frost HM. 1973b. Orthopaedic biomechanics. Springfield, IL: Charles C. Thomas.
34. Frost HM. 1985. The "new bone:" some anthropological potentials. Yrbk Phys Anthropol 28:211-226.
35. Frost HM. 1987a. Secondary osteon population densities: an algorithm for estimating the missing osteons. Yrbk Phys Anthropol 30:239-254.
36. Frost HM. 1987b. Secondary osteon population densities: an algorithm for determining mean bone tissue age. Yrbk Phys Anthropol 30:221-238.
37. Frost HM. 1990. Skeletal structural adaptations to mechanical usage (SATMU): 2. Redefining Wolff's law: the remodeling problem. Anat Rec 226:414-422.
38. Frost HM. 2003. Bone's mechanostat: a 2003 update. Anat Rec [A] Discov Mol Cell Evol Biol 275:1081-1101.
39. Goldman HM, Bromage TG, Thomas CDL, Clement JG. 2003. Preferred collagen fiber orientation in the human mid-shaft femur. Anat Rec [A] Discov Mol Cell Evol Biol 272:434-445.
40. Hert J, Pribylová E, Lisková M. 1972. Reaction of bone to mechanical stimuli. Acta Anat (Basel) 82:218-230.
41. Hildebrand M. 1985. Walking and running. In: Hildebrand M, Bramble DM, Liem KF, Wake DB, editors. Functional vertebrate morphology. Cambridge: Belknap Press, p 38-57.
42. Hildebrand M, Goslow GE Jr. 2001. Analysis of vertebrate structure. New York: John Wiley & Sons, Inc.
43. Hildebrand M, Hurley JP. 1985. Energy of the oscillating legs of a fast-moving cheetah, pronghorn, jackrabbit, and elephant. J Morphol 184:23-31.
44. Holliday TW. 1999. Brachial and crural indices of European late Upper Paleolithic and Mesolithic humans. J Hum Evol 36:549-566.
45. Holliday TW, Ruff CB. 2001. Relative variation in human proximal and distal limb segment lengths. Am J Phys Anthropol 116:26-33.
46. Jaworski ZFG. 1984. Lamellar bone turnover systems and its effector organ. Calcif Tissue Int 35:46-55.
47. Kerley ER. 1965. The microscopic determination of age in human bone. Am J Phys Anthropol 23:149-164.
48. Kerley ER, Ubelaker DH. 1978. Revision in the microscopic method of estimating age at death in human cortical bone. Am J Phys Anthropol 49:545-546.
49. Lanyon LE. 1981. Locomotor loading and functional adaptation in limb bones. In: Day MH, editor. Vertebrate locomotion. London: Academic Press, p 305-329.
50. Lanyon LE. 1984. Functional strain as a determinant for bone remodeling. Calcif Tissue Int 36:56-61.
51. Lanyon LE. 1992. Control of bone architecture by functional load bearing. J Bone Miner Res 7:369-375.
52. Lanyon LE, Baggott DG. 1976. Mechanical function as an influence on the structure and form of bone. J Bone Joint Surg [Br] 58:436-443.
53. 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 ratius. J Biomech 12:595-600.
54. Lanyon LE, Goodship AE, Pye CJ, MacFie JH. 1982. Mechanically adaptive bone remodelling. J Biomech 15:141-154.
55. Leonard WR, Robertson ML. 1995. Energetic efficiency of human bipedality. Am J Phys Anthropol 97:335-338.
56. Leonard WR, Robertson ML. 1997. Rethinking the energetics of bipedality. Curr Anthropol 38:304-309.
57. Les CM, Stover SM, Keyak JH, Taylor KT, Willis NH. 1997. The distribution of material properties in the equine third metacarpal bone serves to enhance sagittal bending. J Biomech 30:355-361.
58. Li J, Mashiba T, Burr DB. 2001. Bisphosphonate treatment suppresses not only stochastic remodeling but also the targeted repair of microdamage. Calcif Tissue Int 69:281-286.
59. Lieberman DE, Crompton AW 1998. Responses of bone to stress: constraints on symmorphosis. In: Webel ER, Taylor CR, Bolis L, editors. Principles of animal design: the optimization and symmorphosis debate. Cambridge: Cambridge University Press, p 78-86.
60. Lieberman DE, Peason OM. 2001. Trade-off between modeling and remodeling responses to loading in the mammalian limb. Bull Mus Comp Zool 156:269-282.
61. Lieberman DE, Pearson OM, Polk JD, Demes B, Crompton AW. 2003. Optimization of bone growth and remodeling in response to loading in tapered mammalian limbs. J Exp Biol 206:3125-3138.
62. Martin RB. 2002. Is all cortical bone remodeling initiated by microdamage? Bone 30:8-13.
63. Martin RB. 2003. Fatigue damage, remodeling, and the minimization of skeletal weight. J Theor Biol 220:271-276.
64. Martin RB. 2004. Functional adaptation and fragility of the skeleton. In: Agarwal SC, Stout SD, editors. Bone loss and osteoporosis: an anthropological perspective. New York: Kluwer Academic/ Plenum Publishers, p 121-138.
65. Martin RB, Burr DB. 1982. A hypothetical mechanism for the stimulation of osteonal remodelling by fatigue damage. J Biomech 15:137-139.
66. Martin RB, Burr DB. 1989. Structure, function, and adaptation of compact bone. New York: Raven Press.
67. Martin RB, Burr DB, Sharkey NA. 1998. Skeletal tissue mechanics. New York: Springer.
68. Mashiba T, Turner CH, Hirano T, Forwood MR, Johnston CC, Burr DB. 2001. Effects of suppressed bone turnover by bisphosphonates on microdamage accumulation and biomechanical properties in clinically relevant skeletal sites in beagles. Bone 28:524-531.
69. Meade JB. 1989. The adaptation of bone to mechanical stress: experimentation and current concepts. In: Cowin SC, editor. Bone mechanics. Boca Raton, FL: CRC Press, Inc. p 211-251.
70. Mishra S, Knothe Tate ML. 2003. Effect of lacunocanalicular architecture on hydraulic conductance in bone tissue: implications for bone health and evolution. Anat Rec [A] Discov Mol Cell Evol Biol 273:752-762.
71. Moore KL, Dalley AR. 1999. Clinically oriented anatomy. Philadelphia: Lippincott Williams & Wilkins.
72. Mori S, Burr DB. 1993. Increased intracortical remodeling following fatigue damage. Bone 14:102-109.
73. Nalla RK, Kruzie JJ, Ritchie RO. 2004. On the origin of the toughness of mineralized tissue: microcracking or crack bridging? Bone 34:790-798.
74. Noble BS, Stevens H, Loveridge N, Reeve J. 1997. Identification of apoptotic changes in osteocytes in normal and pathological human bone. Bone 20:273-282.
75. O'Connor JA, Lanyon LE, MacFie H. 1982. The influence of strain rate on adaptive bone remodeling. J Biomech 15:767-781.
76. Ortner DJ. 1975. Aging effects on osteon remodeling. Calcif Tissue Res 18:27-36.
77. Parfitt AM. 1988. Bone remodeling: relationship to the amount and structure of bone, and the pathogenesis and prevention of fractures. In: Riggs BL, Melton LJ III, editors. Osteoporosis: etiology, diagnosis and management. New York: Raven Press, p 45-94.
78. Parfitt AM. 1994. Osteonal and hemi-osteonal remodeling: the spatial and temporal framework for signal traffic in adult human bone. J Cell Biochem 55:276-286.
79. Parfitt AM. 2002. Targeted and nontargeted bone remodeling: relationship to basic multicellular unit origination and progression. Bone 30:5-7.
80. Pearson OM, Lieberman DE. 2004. The aging of Wolff's "law:" ontogeny and responses to mechanical loading in cortical bone. Yrbk Phys Anthropol 47:63-99.
81. Pfeiffer S, Lazenby R, Chiang J. 1995. Cortical remodeling data are affected by sampling location. Am J Phys Anthropol 96:89-92.
82. Raab DM, Crenshaw TD, Kimmel DB, Smith EL. 1991. A histomorphometric study of cortical bone activity during increased weight-bearing exercise. J Bone Miner Res 6:741-749.
83. Reilley 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.
84. Riggs CM, Lanyon LE, Boyde A. 1993. Functional associations between collagen fibre orientation and locomotor strain direction in cortical bone of the equine radius. Anat Embryol (Berl) 187:231-238.
85. Robling AG. 1998. Histomorphometric assessment of mechanical loading history from human skeletal remains: the relationship between mircromorphology and macromorphology at the femoral midshaft. Ph.D. dissertation, University of Missouri-Columbia.
86. Robling AG, Stout SD. 2000. Histomorphometry of human cortical bone: applications to age estimation. In: Katzenberg MA, Saunders SR, editors. Biological anthropology of the human skeleton. New York: Wiley-Liss, Inc. p 187-213.
87. Rodman RS, McHenry HM. 1980. Bioenergetics and the origin of hominid bipedalism. Am J Phys Anthropol 52:103-106.
88. Rubin CT, Bain SD, McLeod KJ. 1992. Suppression of the osteogenic response in the aging skeleton. Calcif Tissue Int 50:306-313.
89. Ruff CB. 1995. Biomechanics of the hip and birth in early Homo. Am J Phys Anthropol 98:527-574.
90. Ruff CB. 2000a. Biomechanial analysis of archaeological human skeletons. In: Katzenberg MA, Saunders SR, editors. Biological anthropology of the human skeleton. New York: Wiley-Liss, Inc. p 71-102.
91. Ruff CB. 2000b. Body size, body shape, and long bone strength in modern humans. J Hum Evol 38:269-290.
92. 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.
93. Schaffler MB, Burr DB. 1984. Primate cortical bone microstructure: relationship to locomotion. Am J Phys Anthropol 65:191-197.
94. Schaffler MB, Choi K, Milgrom C. 1995. Aging and matrix microdamage accumulation in human comparct bone. Bone 17:521-525.
95. Skedros JG, Dayton MR, Sybrowsky CL, Bloebaum RD, Bachus KN. 2003. Are uniform regional safety factors an objective of adaptive modeling/remodeling in cortical bone? J Exp Biol 206:2431-2439.
96. 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.
97. Sommerfeldt DW, Rubin CT. 2001. Biology of bone and how it orchestrates the form and function of the skeleton. Eur Spine J 10:86-95.
98. Steudel K. 1996. Limb morphology, bipedal gait, and the energetics of hominid locomotion. Am J Phys Anthropol 99:345-355.
99. Steudel K, Beattie J. 1993. Scaling of cursoriality in mammals. J Morphol 217:55-63.
100. Steudel-Numbers KL. 2001. Role of locomotor economy in the origin of bipedal posture and gait. Am J Phys Anthropol 116:171-173.
101. Steudel-Numbers KL. 2003. The energetic cost of locomotion: humans and primates compared to generalized endotherms. J Hum Evol 44:255-262.
102. Stout SD. 1982. The effects of long-term immobilization on the histomorphology of human cortical bone. Calcif Tissue Int 34:337-342.
103. Stout SD. 1998. The application of histological techniques for age at death determination. In: Reichs KJ, editor. Forensic osteology: advances in the identification of human remains. Springfield, IL: Charles C. Thomas, p 237-252.
104. Stout SD, Paine RR. 1992. Histological age estimation using rib and clavicle. Am J Phys Anthropol 87:111-115.
105. Stout SD, Paine RR. 1994. Bone remodeling rates: a test of an algorithm for estimating missing osteons. Am J Phys Anthropol 93:123-129.
106. Tami AE, Nasser P, Schaffler MB, Knoth Tate ML. 2003. Noninvasive fatigue fracture model of the rat ulna. J Orthop Res 21:1018-1024.
107. Taylor CR, Heglund NC, Maloiy GMO. 1982. Energetics and mechanics of terrestrial locomotion. J Exp Biol 97:1-21.
108. 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.
109. Verborgt O, Gibson GJ, Schaffler MB. 2000. Loss of osteocyte integrity in association with microdamage and bone remodeling after fatigue in vivo. J Bone Miner Res 15:60-67.
110. Wolff J. 1986. The law of bone remodeling [translated by P. Marquet and R. Furlong]. Berlin: Springer-Verlag (original work published 1892).
111. Woo SL-Y, Kuei 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 [Am] 63:780-787.
112. Wu K, Schubeck KE, Frost HM, Villanueva A. 1970. Haversian bone formation rates determined by a new method in a mastodon, and in human diabetes mellitus and osteoporosis. Calcif Tissue Res 6:204-219.
113. Yeni YN, Fyhrie DP. 2002. Fatigue damage-fracture mechanics interaction in cortical bone. Bone 30:509-514.
114. You L, Weinbaum S, Cowin SC, Schaffler MB. 2004. Ultrastructure of the osteocyte process and its pericellular matrix. Anat Rec [A] Discov Mol Cell Evol Biol 278:505-513.