Ontogenetic patterning of cortical bone microstructure and geometry at the human mid-shaft femur

Anatomical Record

Volumn 292, Issue 1, 2009, Pages 48-64

  Goldman, Haviva M ^a   McFarlin, S C ^b   Cooper, D M L ^c   Thomas, C D L ^d   Clement, J G ^d  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b THE GEORGE WASHINGTON UNIVERSITY   (United States)

^c UNIVERSITY OF SASKATCHEWAN   (Canada)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Cortical bone; Femur; Growth; Microstructure

Indexed keywords

ADOLESCENT; BONE DENSITY; BONE DEVELOPMENT; BONE REMODELING; CHILD; CHILD, PRESCHOOL; FEMALE; FEMUR; HUMANS; MALE; OSTEOGENESIS; YOUNG ADULT;

EID: 60149103802     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.20778     Document Type: Article

References (114)

1. Amprino R. 1947. La structure du tissu osseoux envisagee comme espression des differences dans la vitesse de l'accroissement. Archives de Biologie 58:315-330.
2. Amprino R, Bairati A. 1936. Processi di ricostruzione e di riassorbimento nella sostanza compatta delle ossa deeluomo. Z. Zellforsch. mikrosk 24:439-511.
3. Baltadjiev G. 1995. Micromorphometric characteristics of osteons in compact bone of growing tibiae of human fetuses. Acta Anat (Basel) 154:181-185.
4. Bass S, Delmas PD, Pearce G, Hendrich E, Tabensky A, Seeman E. 1999. The differing tempo of growth in bone size, mass, and density in girls is region-specific. J Clin Invest 104:795-804.
5. Bell KL, Loveridge N, Reeve J, Thomas CD, Feik SA, Clement JG. 2001. Super-osteons (remodeling clusters) in the cortex of the femoral shaft: influence of age and gender. Anat Rec 264:378-386.
6. Bertelsen PK, Clement JG, Thomas CD. 1995. A morphometric study of the cortex of the human femur from early childhood to advanced old age. Forensic Sci Int 74:63-77.
7. Biewener AA, Bertram JE. 1993a. Skeletal strain patterns in relation to exercise training during growth. J Exp Biol 185:51-69.
8. Biewener AA, Bertram JEA. 1993b. Mechanical loading and bone growth in vivo. In: Hall BK, editor. Bone. Vol. 7: Bone Growth B. Boca Raton: CRC Press. p 1-36.
9. Bousson V, Meunier A, Bergot C, Vicaut E, Rocha MA, Morais MH, Laval-Jeantet AM, Laredo JD. 2001. Distribution of intracortical porosity in human midfemoral cortex by age and gender. J Bone Miner Res 16:1308-1317.
10. Bouvier M, Hylander WL. 1981. Effect of bone strain on cortical bone structure in macaques (Macaca mulatta). J Morphol 167:1-12.
11. Boyde A, Travers R, Glorieux FH, Jones SJ. 1999. The mineralization density of iliac crest bone from children with osteogenesis imperfecta. Calcif Tissue Int 64:185-190.
12. Burton P, Nyssen-Behets C, Dhem A. 1989. Haversian bone remodelling in human fetus. Acta Anat (Basel) 135:171-175.
13. Castanet J. 1993. Bone and individual aging. In: Hall BK, editor. Bone. Boca Raton: CRC Press. p 245-284.
14. Chan AH, Crowder CM, Rogers TL. 2007. Variation in cortical bone histology within the human femur and its impact on estimating age at death. Am J Phys Anthropol 132:80-88.
15. Chinsamy-Turan A. 2005. The microstructure of dinosaur bone: deciphering biology with fine-scale techniques. Baltimore: The Johns Hopkins University Press.
16. Cooper C, Javaid MK, Taylor P, Walker-Bone K, Dennison E, Arden N. 2002. The fetal origins of osteoporotic fracture. Calcif Tissue Int 70:391-394.
17. Cubo J, Ponton F, Laurin M, de Margerie E, Castanet J. 2005. Phylogenetic signal in bone microstructure of sauropsids. Syst Biol 54:562-574.
18. de Margerie E, Cubo J, Castanet J. 2002. Bone typology and growth rate: testing and quantifying 'Amprino's rule' in the mallard (Anas platyrhynchos). C R Biol 325:221-230.
19. de Margerie E, Robin JP, Verrier D, Cubo J, Groscolas R, Castanet J. 2004. Assessing a relationship between bone microstructure and growth rate: a fluorescent labelling study in the king penguin chick ( Aptenodytes patagonicus). J Exp Biol 207:869-879.
20. de Ricqlés A. 1993. Some remarks on palaeohistology from a comparative evolutionary point of view. In: Grupe G, Garland AN, editors. Histology of ancient human bone: methods and diagnosis. Berlin: Springer-Verlag. p 37-77.
21. de Ricqlés A, Meunier FJ, Castanet J, Francillon-Viellot H. 1991. Comparative microstructure of bone. In: Hall BK, editor. Bone. Boca Raton: CRC Press. p 1-78.
22. Demeter G, Matyas J. 1928. Mikroskopisch vergleichend-anatomische studien an rohrenknochen mit besonder rucksicht auf unterscheindung menschlicher und tierischer knochen. Anat Embryol 87:45-99.
23. Drusini AG. 1996. Sampling location in cortical bone histology. Am J Phys Anthropol 100:609-610.
24. Duan Y, Beck TJ, Wang XF, Seeman E. 2003. Structural and biomechanical basis of sexual dimorphism in femoral neck fragility has its origins in growth and aging. J Bone Miner Res 18:1766-1774.
25. Enlow DH. 1962a. A study of the post-natal growth and remodeling of bone. Am J Anat 110:79-101.
26. Enlow DH. 1962b. Functions of the Haversian system. Am J Anat 110:269-305.
27. Enlow DH. 1963. Principles of bone remodeling; an account of postnatal growth and remodeling processes in long bones and the mandible. Springfield, Ill.: Thomas.
28. Enlow DH. 1966. An evaluation of the use of bone histology in forensic medicine and anthropoogy. In: Evans FG, editor. Studies on the anatomy and function of bone and joints. Berlin, New York: Springer-Verlag. p 93-112.
29. Enlow DH. 1976. The remodeling of bone. Yearbook Phys Anthropol 20:19-34.
30. Enlow DH, Hans MG. 1996. Essentials of facial growth. Philadelphia: Saunders.
31. Enlow DH, Moyers RE, Merow WW. 1982. Handbook of facial growth. 2nd ed. Philadelphia: Saunders.
32. Epker BN, Frost HM. 1965. The direction of transverse drift of actively forming Osteons in human rib cortex. J Bone Joint Surg Am 47:1211-1215.
33. Epker BN, Frost HM. 1966. Periosteal appositional bone growth from age two to age seventy in man. A tetracycline evaluation. Anat Rec 154:573-577.
34. Erickson GM. 2005. Assessing dinosaur growth patterns: a microscopic revolution. Trends Ecol Evol 20:677-684.
35. Feik SA, Thomas CD, Bruns R, Clement JG. 2000. Regional variations in cortical modeling in the femoral mid-shaft: sex and age differences. Am J Phys Anthropol 112:191-205.
36. Feik SA, Thomas CD, Clement JG. 1997. Age-related changes in cortical porosity of the midshaft of the human femur. J Anat 191 (Part 3):407-416.
37. Foote JS. 1916. Contribution to the comparative histology of the femur. Washington D.C.: Smithsonian Institution.
38. Francillon-Viellot H, de Buffrenil V, Castanet J, Geraudie J, Meunier FJ, Sire JY, Zylberberg L, de Ricqlés A. 1990. Microstructure and mineralization of vertebrate skeletal tissues. In: Carter JG, editor. Skeletal biomineralization: patterns, processes and evolutionary trends. New York: Van Nostrand Reinhold. p 471-530.
39. Frisancho AR, Garn SM, Ascoli W. 1970. Subperiosteal and endosteal bone apposition during adolescence. Hum Biol 42:639-664.
40. Frost HM. 1973. Bone modeling and skeletal modeling errors. Springfield, Ill.: Thomas.
41. Frost HM. 1986. Intermediary organization of the skeleton. Boca Raton: CRC Press.
42. Garn SM. 1970. The earlier gain and the later loss of cortical bone in nutritional perspective. Springfield, IL: Charles C. Thomas.
43. Gasser T, Kneip A, Binding A, Prader A, Molinari L. 1991. The dynamics of linear growth in distance, velocity and acceleration. Ann Hum Biol 18:187-205.
44. Glorieux FH, Travers R, Taylor A, Bowen JR, Rauch F, Norman M, Parfitt AM. 2000. Normative data for iliac bone histomorphometry in growing children. Bone 26:103-109.
45. Goldman HM. 2001. Histocomposition and geometry at the human mid-shaft femur. Anthropology. New York: City University of New York.
46. Goldman HM, Bromage TG, Boyde A, Thomas CD, Clement JG. 2003a. Intrapopulation variability in mineralization density at the human femoral mid-shaft. J Anat 203:243-255.
47. Goldman HM, Bromage TG, Thomas CD, Clement JG. 2003b. Preferred collagen fiber orientation in the human mid-shaft femur. Anat Rec A Discov Mol Cell Evol Biol 272:434-445.
48. Goldman HM, Kindsvater J, Bromage TG. 1999. Correlative light and backscattered electron microscopy of bone, Part 1. Specimen preparation methods. Scanning 21:40-43.
49. Goldman HM, Thomas CD, Clement JG, Bromage TG. 2005. Relationships among microstructural properties of bone at the human midshaft femur. J Anat 206:127-139.
50. Herrmann B, Danielmeyer A. 1994. Bone structures reflecting rhythm, seasonality, and life-style of past human populations. Naturwissenschaften 81:399-401.
51. Hoyte DA, Enlow DH. 1966. Wolff's law and the problem of muscle attachment on resorptive surfaces of bone. Am J Phys Anthropol 24:205-213.
52. Johnston FE, Watts ES. 1969. Endosteal deposition of bone at the midshaft of the second metacarpals of adolescent females. Anat Rec 163:67-70.
53. Jordan GR, Loveridge N, Bell KL, Power J, Rushton N, Reeve J. 2000. Spatial clustering of remodeling osteons in the femoral neck cortex: a cause of weakness in hip fracture? Bone 26:305-313.
54. Keen M. 1993. Early development and attainment of normal gait. J Prosthet Orthot 5:35-38.
55. Klevezal GA. 1996. Recording structures of mammals: determination of age and reconstruction of life history, Rev. and updated ed. Rotterdam, Brookfield, Vt.: A.A. Balkema.
56. Kontulainen SA, Macdonald HM, Khan KM, McKay HA. 2005. Examining bone surfaces across puberty: a 20-month pQCT trial. J Bone Miner Res 20:1202-1207.
57. Lanyon LE. 1993. Biomechanical properties of bone and response of bone to mechanical stimuli: functional strain as a controlling influence on bone modeling and remodeling behavior. In: Hall BK, editor. Bone. Boca Raton: CRC Press.
58. Lazenby R. 1986. Porosity-geometry interaction in the conservation of bone strength. J Biomech 19:257-258.
59. Lee KC, Lanyon LE. 2004. Mechanical loading influences bone mass through estrogen receptor alpha. Exerc Sport Sci Rev 32:64-68.
60. Macdonald H, Kontulainen S, Petit M, Janssen P, McKay H. 2006. Bone strength and its determinants in pre- and early pubertal boys and girls. Bone 39:598-608.
61. MacMahon EB, Carmines DV, Irani RN. 1995. Physiologic bowing in children: an analysis of the pendulum mechanism. J Pediatr Orthop B 4:100-105.
62. Marshall WA. 1977. Human growth and its disorders. London: Academic Press.
63. Martin RB. 2000. Toward a unifying theory of bone remodeling. Bone 26:1-6.
64. 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.
65. Martin RB, Burr DB. 1989. Structure, function and adaptation of compact bone. New York: Raven Press.
66. McFarlin SC. 2006. Ontogenetic variation in long bone microstructure in catarrhines and its significance for life history research. Anthropology. City University of New York.
67. McFarlin SC, Terranova CJ, Zihlman AL, Enlow DH, Bromage TG. 2008. Regional variability in secondary remodeling within long bone cortices of catarrhine primates: the influence of bone growth dynamics. J Anat 213:308-324.
68. McGuigan FE, Murray L, Gallagher A, Davey-Smith G, Neville CE, Van't Hof R, Boreham C, Ralston SH. 2002. Genetic and environmental determinants of peak bone mass in young men and women. J Bone Miner Res 17:1273-1279.
69. Mittlmeier T, Mattheck C, Dietrich F. 1994. Effects of mechanical loading on the profile of human femoral diaphyseal geometry. Med Eng Phys 16:75-81.
70. Mosley JR, Lanyon LE. 2002. Growth rate rather than gender determines the size of the adaptive response of the growing skeleton to mechanical strain. Bone 30:314-319.
71. Neu CM, Rauch F, Manz F, Schoenau E. 2001. Modeling of cross-sectional bone size, mass and geometry at the proximal radius: a study of normal bone development using peripheral quantitative computed tomography. Osteoporos Int 12:538-547.
72. Newell-Morris L, Sirianni JE. 1982. Parameters of bone growth in the fetal and infant macaque (Macaca nemestrina) humerus as documented by trichromatic bone labels. Prog Clin Biol Res 101:243-258.
73. Oliver H, Jameson KA, Sayer AA, Cooper C, Dennison EM. 2007. Growth in early life predicts bone strength in late adulthood: the Hertfordshire Cohort Study. Bone 41:400-405.
74. Parfitt AM. 1994. The two faces of growth: benefits and risks to bone integrity. Osteoporos Int 4:382-398.
75. Parfitt AM, Travers R, Rauch F, Glorieux FH. 2000. Structural and cellular changes during bone growth in healthy children. Bone 27:487-494.
76. Pauwels F. 1980. Biomechanics of the locomotor apparatus: contributions on the functional anatomy of the locomotor apparatus. Berlin: Springer Verlag.
77. Pearson OM, Lieberman DE. 2004. The aging of Wolff's "law": ontogeny and responses to mechanical loading in cortical bone. Am J Phys Anthropol Suppl 39:63-99.
78. Petit MA, Beck TJ, Shults J, Zemel BS, Foster BJ, Leonard MB. 2005. Proximal femur bone geometry is appropriately adapted to lean mass in overweight children and adolescents. Bone 36:568-576.
79. Pfeiffer S. 1998. Variability in osteon size in recent human populations. Am J Phys Anthropol 106:219-227.
80. Pfeiffer S. 2006. Cortical bone histology in juveniles. Microscopic examinations of bioarchaeological remains. Keeping a close eye on ancient tissues.
81. Pfeiffer S, Crowder C, Harrington L, Brown M. 2006. Secondary osteon and Haversian canal dimensions as behavioral indicators. Am J Phys Anthropol 131:460-468.
82. Pfeiffer S, Lazenby R, Chiang J. 1995. Brief communication: cortical remodeling data are affected by sampling location. Am J Phys Anthropol 96:89-92.
83. Rauch F, Travers R, Glorieux FH. 2006. Cellular activity on the seven surfaces of iliac bone: a histomorphometric study in children and adolescents. J Bone Miner Res 21:513-519.
84. Rauch F, Travers R, Glorieux FH. 2007. Intracortical remodeling during human bone development - a histomorphometric study. Bone 40:274-280.
85. Reid SA, Boyde A. 1987. Changes in the mineral density distribution in human bone with age: image analysis using backscattered electrons in the SEM. J Bone Miner Res 2:13-22.
86. Robling AG, Stout SD. 1999. Morphology of the drifting osteon. Cells Tissues Organs 164:192-204.
87. Roschger P, Paschalis EP, Fratzl P, Klaushofer K. 2008. Bone mineralization density distribution in health and disease. Bone 42:456-466.
88. Ruff C. 2003a. Growth in bone strength, body size, and muscle size in a juvenile longitudinal sample. Bone 33:317-329.
89. Ruff C. 2003b. Ontogenetic adaptation to bipedalism: age changes in femoral to humeral length and strength proportions in humans, with a comparison to baboons. J Hum Evol 45:317-349.
90. Ruff CB. 1987. Sexual dimorphism in human lower limb bone structure: relationship to subsistence strategy and sexual division of labor. J Hum Evol 16:391-416.
91. 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.
92. Ruff CB, Hayes WC. 1988. Sex differences in age-related remodeling of the femur and tibia. J Orthop Res 6:886-896.
93. Ruff CB, Larsen CS, Hayes WC. 1984. Structural changes in the femur with the transition to agriculture on the Georgia coast. Am J Phys Anthropol 64:125-136.
94. Ruff CB, Walker A, Trinkaus E. 1994. Postcranial robusticity in Homo. III. Ontogeny. Am J Phys Anthropol 93:35-54.
95. Sawada J, Kondo O, Nara T, Dodo Y, Akazawa T. 2004. Bone histomorphology of the Dederiyeh Neanderthal child. Anthropol Sci 112:247-256.
96. Schonau E. 1998. The development of the skeletal system in children and the influence of muscular strength. Horm Res 49:27-31.
97. Seeman E. 2003. Periosteal bone formation - a neglected determinant of bone strength. N Engl J Med 349:320-323.
98. Shefelbine SJ, Tardieu C, Carter DR. 2002. Development of the femoral bicondylar angle in hominid bipedalism. Bone 30:765-770.
99. Sinclair D, Dangerfield P. 1998. Human growth after birth. New York: Oxford University Press.
100. Smith SL, Buschang PH. 2004. Variation in longitudinal diaphyseal long bone growth in children three to ten years of age. Am J Hum Biol 16:648-657.
101. Smithgall EB, Johnston FE, Malina RM, Galbraith MA. 1966. Developmental changes in compact bone relationships in the second metacarpal. Hum Biol 38:141-151.
102. Streeter M. 2005. Histomorphometric characteristics of the subadult rib cortex: normal patterns of dynamic bone modeling and remodeling during growth and development. Anthropology. University of Missouri-Columbia.
103. Sumner DR. 1984. Size, shape and bone mineral content of the human femur in growth and aging. Anthropology. University of Arizona.
104. Sumner DR, Andriacchi TP. 1996. Adaptation to differential loading: comparison of growth-related changes in cross-sectional properties of the human femur and humerus. Bone 19:121-126.
105. Sutherland D. 1997. The development of mature gait. Gait Posture 6:163-170.
106. Tardieu C, Damsin JP. 1997. Evolution of the angle of obliquity of the femoral diaphysis during growth-correlations. Surg Radiol Anat 19:91-97.
107. Thomas CD, Feik SA, Clement JG. 2005. Regional variation of intracortical porosity in the midshaft of the human femur: age and sex differences. J Anat 206:115-125.
108. Tommasini SM, Nasser P, Hu B, Jepsen KJ. 2008. Biological co-adaptation of morphological and composition traits contributes to mechanical functionality and skeletal fragility. J Bone Miner Res 23:236-246.
109. Tommasini SM, Nasser P, Jepsen KJ. 2007. Sexual dimorphism affects tibia size and shape but not tissue-level mechanical properties. Bone 40:498-505.
110. Tommasini SM, Nasser P, Schaffler MB, Jepsen KJ. 2005. Relationship between bone morphology and bone quality in male tibias: implications for stress fracture risk. J Bone Miner Res 20:1372-1380.
111. Ural A, Vashishth D. 2006. Interactions between microstructural and geometrical adaptation in human cortical bone. J Orthop Res 24:1489-1498.
112. Wang Q, Alen M, Nicholson P, Lyytikainen A, Suuriniemi M, Helkala E, Suominen H, Cheng S. 2005. Growth patterns at distal radius and tibial shaft in pubertal girls: a 2-year longitudinal study. J Bone Miner Res 20:954-961.
113. Wren TA, Gilsanz V. 2006. Assessing bone mass in children and adolescents. Curr Osteoporos Rep 4:153-158.
114. Zamberlan N, Radetti G, Paganini C, Gatti D, Rossini M, Braga V, Adami S. 1996. Evaluation of cortical thickness and bone density by roentgen microdensitometry in growing males and females. Eur J Pediatr 155:377-382.