Ontogenetic changes in the internal and external morphology of the ilium in modern humans

Journal of Anatomy

Volumn 218, Issue 3, 2011, Pages 324-335

  Abel, Richard ^a   Macho, Gabriele A ^b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b INSTITUT CATALÀ DE PALEONTOLOGIA MIQUEL CRUSAFONT   (Spain)

Author keywords

Human iliac growth; Ontogeny; Trabecular architecture

Indexed keywords

ACETABULUM; ANATOMICAL VARIATION; ANISOTROPY; ARTICLE; BONE DEVELOPMENT; BONE RADIOGRAPHY; CROSS-SECTIONAL STUDY; FEMALE; FUNCTIONAL MORPHOLOGY; GROWTH CURVE; HUMAN; HUMAN TISSUE; ILIAC BONE; LOCOMOTION; MAJOR CLINICAL STUDY; MALE; MORPHOMETRICS; ONTOGENY; PRIORITY JOURNAL; TRABECULAR BONE;

ILIA;

EID: 79551511240     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/j.1469-7580.2011.01342.x     Document Type: Article

References (93)

1. Agarwal SC, Dimitriu M, Tomlinson GA, etal. (2004) Medieval trabecular bone architecture: the influence of age, sex, and lifestyle. Am J Phys Anthropol 124, 33-44.
2. Berge C (1984) Multivariate analysis of the pelvis for hominids and other extant primates: implications for the locomotion and systematics of the different species of australopithecines. J Hum Evol 13, 555-562.
3. Berge C (1994) How did the australopithecines walk? A biomechanical study of the hip and thigh of Australopithecus afarensis J Hum Evol 26, 259-273.
4. Berge C (1998) Heterochronic processes in human evolution: an ontogenetic analysis of the hominid pelvis. Am J Phys Anthropol 105, 441-459.
5. Berge C, Penin X (2004) Ontogenetic allometry, heterochrony, and interspecific differences in the skull of African apes, using 3-dimensional Procrustes analysis. Am J Phys Anthropol 124, 124-138.
6. Biewener AA, Fazzalari NL, Konieczynski DD, etal. (1996) Adaptive changes in trabecular architecture in relation to functional strain patterns and disuse. Bone 19, 1-8.
7. Bogin B (1999) Evolutionary perspective on human growth. Ann Rev Anthropol 28, 109-153.
8. Bogin B (2002) The evolution of human growth. In: Human Growth and Development (ed. Cameron N), pp. 295-320, Amsterdam: Academic Press.
9. Bookstein FL (1991) Morphometric Tools for Landmark Data: Geometry and Biology. Cambridge: Cambridge University Press.
10. Caligiuri P, Giger ML, Favus MJ, etal. (1993) Computerized radiographic analysis of osteoporosis: preliminary evaluation. Radiology 186, 471-474.
11. Carlson KJ, Lublinsky S, Judex S (2008) Do different locomotor modes during growth modulate trabecular architecture in the murine hind limb? Int Comp Biol 48, 385-393.
12. Carter DR, Beaupré GS (2001) Skeletal Function and Form: Mechanobiology of Skeletal Development, Aging, and Regeneration. Cambridge: Cambridge University Press.
13. Chester VL, Tingley M, Biden EN (2006) A comparison of kinetic gait parameters for 3-13 year olds. Clin Biomech 21, 726-732.
14. Corner BD, Lele S, Richtsmeier JT (1992) Measuring precision of three-dimensional landmark data. J Quant Anthropol 3, 347-359.
15. Correnti V (1955) Le basi morfomeccaniche della struttura dell'osso iliaco. Riv Antrop 42, 289-336.
16. Cramon-Taubadel N, Frazier BC, Lahr M (2007) The problem of assessing landmark error in geometric morphometrics: theory, methods, and modifications. Am J Phys Anthropol 134, 24-35.
17. Cunningham CA, Black SM (2009a) Development of the fetal ilium - challenging concepts of bipedality. J Anat 214, 91-99.
18. Cunningham CA, Black SM (2009b) Anticipating bipedalism: trabecular organization in the newborn ilium. J Anat 214, 817-829.
19. Cunningham CA, Black SM (2010) The neonatal ilium - metaphyseal drivers and vascular passengers. Anat Rec 293, 1297-1309.
20. Dalstra M, Huiskes R (1995) Load transfer across the pelvic bone. J Biomech 28, 715-724.
21. Delaere O, Dhem A (1999) Prenatal development of the human pelvis and acetabulum. Acta Orthop Belg 65, 255-260.
22. Delaere O, Kok V, Nyssen-Behets C, etal. (1992) Ossification of the human fetal ilium. Acta Anat 143, 330-334.
23. Fajardo RJ, Müller R, Ketcham RA, etal. (2007) Nonhuman anthropoid primate femoral neck trabecular architecture and its relationship to locomotor mode. Anat Rec 290, 422-436.
24. Frost HM (1990) Skeletal structural adaptations to mechanical usage (SATMU): 2. Redefining Wolff's Law: the remodeling problem. Anat Rec 226, 414-422.
25. Gefen A, Seliktar R (2004) Comparison of the trabecular architecture and isostatic stress flow in the human calcaneus. Med Eng Phys 26, 119-129.
26. Goldman HM, McFarlin SC, Cooper DML, etal. (2009) Ontogenetic patterning of cortical bone microstructure and geometry at the human mid-shaft femur. Anat Rec 292, 48-64.
27. Gosman JH, Ketcham RA (2009) Patterns in ontogeny of human trabecular bone from SunWatch village in the Prehistoric Ohio Valley: general features of microarchitectural change. Am J Phys Anthropol 138, 318-332.
28. Hallemans A, de Clercq D, Otten B, etal. (2005) 3D joint dynamics of walking in toddlers. A cross-sectional study spanning the first rapid development phase of walking. Gait & Posture 22, 107-118.
29. Hammer Ø, Harper DAT, Ryan PD (2001) Past: paleontological statistics software package for education and data analysis. Palaeontol Electronica 4, 9.
30. Harrigan TP, Mann RW (1984) Characterization of microstructural anisotropy in orthotropic materials using a second rank tensor. J Mater Sci 19, 761-767.
31. Hou JC, Salem GJ, Zernicke RF, etal. (1990) Structural and mechanical adaptations of immature trabecular bone to strenuous exercise. J Appl Physiol 69, 1309-1314.
32. Huiskes HWJ (2000) If bone is the answer, then what is the question? J Anat 197, 145-156.
33. Ivanenko YP, Dominici N, Cappellini G, etal. (2005) Kinematics in newly walking toddlers does not depend upon postural stability. J Neurophysiol 94, 754-763.
34. Iwamoto J, Yeh JK, Aloia JF (1999) Differential effect of treadmill exercise on three cancellous bone sites in the young growing rat. Bone 24, 163-169.
35. Klingenberg CP (2008) MorphoJ ().
36. Klingenberg CP, Monteiro LR (2005) Distances and directions in multidimensional shape spaces: implications for morphometric applications. Syst Biol 54, 678-688.
37. Kobayashi S, Takahashi HE, Ito A, etal. (2003) Trabecular minimodeling in human iliac bone. Bone 32, 163-169.
38. Lanyon LE (1974) Experimental support for the trajectorial theory of bone structure. J Bone Joint Surg 56-B, 160-166.
39. Lieberman DE (1996) How and why humans grow thin skulls: experimental evidence for systemic cortical robusticity. Am J Phys Anthropol 101, 217-236.
40. Lieberman DE, Crompton AW (1998) Responses of bone to stress. In: Principles of Biological Design: the Optimization and Symmorphosis Debate (eds Weibel E, Taylor C, Bolis L), pp. 78-86. Cambridge: Cambridge University Press.
41. Lieberman DE, Pearson OM, Polk JD, etal. (2003) Optimization of bone growth and remodeling in response to loading in tapered mammalian limbs. J Exp Biol 206, 3125-3138.
42. Lovejoy CO, Heiple KG, Burstein AH (1973) The gait of Australopithecus. Am J Phys Anthropol 38, 757-779.
43. Lovejoy CO, Cohn MJ, White TD (1999) Morphological analysis of the mammalian postcranium: a developmental perspective. Proc Natl Acad Sci USA 96, 13247-13252.
44. Lovejoy OC, Suwa G, Spurlock S, etal. (2009) The pelvis and femur of Ardipithecus ramidus: the emergence of upright walking. Science 326, 71.
45. Macchiarelli R, Bondioli L, Galichon V, etal. (1999) Hip bone trabecular architecture shows uniquely distinctive locomotor behaviour in South African australopithecines. J Hum Evol 36, 211-232.
46. Macho GA, Abel RL, Schutkowski H (2005) Age changes in bone microstructure: do they occur uniformly? Int J Osteoarchaeol 15, 421-430.
47. Marchi D, Sparacello VS, Holt BM, etal. (2006) Biomechanical approach to the reconstruction of activity patterns in Neolithic Western Liguria, Italy. Am J Phys Anthropol 131, 447-455.
48. Martinon-Torres M (2003) Quantifying trabecular orientation in the pelvic cancellous bone of modern humans, chimpanzees, and the Kebara2 Neanderthal. Am J Hum Biol 15, 647-661.
49. McColl DJ, Abel RL, Spears IR, etal. (2006) An automated method to measure trabecular thickness from micro-computed tomographic scans and its applications. Anat Rec 288A, 982-988.
50. McFarlin SC, Terranova CJ, Zihlman AL, etal. (2008) Regional variability in secondary remodeling within long bone cortices of catarrhine primates: the influence of bone growth history. J Anat 213, 308-324.
51. McHenry HM, Corruccini RS (1975) Multivariate analysis of early hominid pelvic bones. Am J Phys Anthropol 43, 263-270.
52. van der Meulen MCH, Morgan TG, Yang X, etal. (2006) Cancellous bone adaptation to in vivo loading in a rabbit model. Bone 28, 871-877.
53. Mori T, Okimoto N, Sakai A, etal. (2003) Climbing exercise increases bone mass and trabecular bone turnover through transient regulation of marrow osteogenic and osteoclastogenic potentials in mice. J Bone Miner Res 18, 2002-2009.
54. National Center for Health Statistics (2000) Stature-for-Age and Weight-for-Age Percentiles 2 to 20 Years: Boys. [Online] (Updated 21 November 2009). Available at: [Accessed 22 March 2010].
55. Odgaard A (1997) Three-dimensional methods for quantification of cancellous bone architecture. Bone 20, 315-328.
56. Odgaard A, Kabel J, van Rietbergen B, etal. (1997) Fabric and elastic principal directions of cancellous bone are closely related. J Biomech 30, 487-495.
57. Pawlowski B, Grabarczyk M (2003) Center of body mass and the evolution of female body shape. Am J Hum Biol 15, 144-150.
58. Pearson OM, Lieberman DE (2004) The aging of Wolff's "law": ontogeny and responses to mechanical loading in cortical bone. Yrbk Phys Anthrop 125, 63-99.
59. Penin X, Berge C, Baylac M (2002) Ontogenetic study of the skull in modern humans and the common chimpanzees: neotenic hypothesis reconsidered with a 3-dimensional Procrustes analysis. Am J Phys Anthropol 118, 50-62.
60. Pontzer H, Lieberman DE, Momin E, etal. (2006) Trabecular bone in the bird knee responds with high sensitivity to changes in load orientation. J Exp Biol 209, 57-65.
61. Poussa MS, Heliovaara MM, Seitsamo JT, etal. (2005) Development of spinal posture in a cohort of children from the age of 11 to 22 years. Eur Spine J 14, 738-742.
62. Robson-Brown KA, Davies EN, McNally DS (2002) The angular distribution of vertebral trabeculae in modern humans, chimpanzees and the Kebara 2 Neanderthal. J Hum Evol 43, 189-205.
63. Rohlf FJ (2004) tpsDig ().
64. Rook L, Bondioli L, Köhler M, etal. (1999) Oreopithecus was a bipedal ape after all: evidence from the iliac cancellous architecture. Proc Natl Acad Sci USA 96, 8795-8799.
65. Rosas A, Bastir M, Alorcón JA, etal. (2008) Thin-plate spline analysis of the cranial base in African, Asian and European populations and its relationship with different malocclusions. Arch Oral Biol 53, 826-834.
66. Ruff CB (2005) Mechanical determinants of bone form: insights from skeletal remains. J Musculoskelet Neuronal Interact 5, 202-212.
67. Ruff C, Holt B, Trinkaus E (2006) Who's afraid of the big bad wolff?: "wolff's law" and bone functional adaptation. Am J Phys Anthropol 129, 484-498.
68. Russ JC (1994) Fractal Surfaces. New York: Plenum Press.
69. Ryan TM, Ketcham RA (2002) The three-dimensional structure of trabecular bone in the femoral head of strepsirrhine primates. J Hum Evol 43, 1-26.
70. Ryan TM, Krovitz GE (2006) Trabecular bone ontogeny in the human proximal femur. J Hum Evol 51, 591-602.
71. Ryan TM, van Rietbergen B (2005) Mechanical significance of femoral head trabecular bone structure in Loris and Galago evaluated using micromechanical finite element models. Am J Phys Anthropol 126, 82-96.
72. Scheuer L, Black S (2000) Developmental Juvenile Osteology. London: Academic Press.
73. Singleton M (2002) Patterns of cranial shape variation in the Papionini (Primates: Cercopithecinae). J Hum Evol 42, 547-578.
74. Skedros JG, Hunt KJ, Bloebaum RD (2004) Relationships of loading history and structural and material characteristics of bone: development of the mule deer calcaneus. J Morphol 259, 281-307.
75. Skedros JG, Sorenson SM, Hunt KJ, etal. (2007) Ontogenetic structural and material variations in ovine calcanei: a model for interpreting bone adaptation. Anat Rec 290, 284-300.
76. Sládek V, Berner M, Sailer R (2006) Mobility in Central European late Neolithic and Early Bronze Age: Femoral Cross-Sectional Geometry. Am J Phys Anthropol 130, 320-332.
77. Smit TH, Schneider E, Odgaard A (1998) Star length distribution: a volume-based concept for the characterization of structural anisotropy. J Microsc 191, 249-257.
78. Steudel K (1982) Patterns of intraspecific and interspecificallometry in Old World primates. Am J Phys Anthropol 59, 419-430.
79. Stock J, Pfeiffer S (2001) Linking structural variability in long bone diaphyses to habitual behaviours: foragers from the southern African Later Stone Age and the Andaman Islands. Am J Phys Anthropol 115, 337-348.
80. Styne DM (2003) The regulation of pubertal growth. Horm Res 60, 22-26.
81. Sutherland DH, Olshen R, Cooper L, etal. (1980) The development of mature gait. J Bone Joint Surg 62-A, 336-353.
82. Tanck E, Homminga J, van Lenthe GH, etal. (2001) Increase in bone volume fraction precedes architectural adaptation in growing bone. Bone 28, 650-654.
83. Tanner JM (1981) Growth and maturation during adolescence. Nutr Rev 39, 43-55.
84. Tanner JM, Whitehouse RH (1976) Clinical longitudinal standards for height, weight, height velocity, weight velocity, and stages of puberty. Arch Dis Child 51, 170-179.
85. Ulijaszek SJ, Lourie JA (1994) Intra- and inter-observer error in anthropometric measurement. In: Anthropometry: the Individual and the Population (eds Ulijaszek SJ, Mascie-Taylor CGN), pp. 30-55. Cambridge: Cambridge University Press.
86. Vogl C, Atchley WR, Cowley DE, etal. (1993) The epigenetic influence of growth hormone on skeletal development. Growth Dev Aging 57, 163-182.
87. Volpato V (2008) Morphogenèse de l'endostructure osseuse de l'ilion humain. C R Palevol 7, 463-471.
88. Wallace JM, Rajachar RM, Allen MR, etal. (2007) Exercise-induced changes in the cortical bone of growing mice are bone- and gender-specific. Bone 40, 1120-1127.
89. Whitcome KK, Shapiro LJ, Lieberman DF (2007) Fetal load and the evolution of lumbar lordosis in bipedal hominins. Nature 250, 1075-1078.
90. Whitehouse WJ (1974) The quantitative morphology of anisotropic trabecular bone. J Microsc 101, 153-168.
91. Williams FL, Orban R (2007) Ontogeny and phylogeny of the pelvis in Gorilla, Pongo, Pan, Australopithecus and Homo. Folia Primatol 78, 99-117.
92. Wolff J (1892) Das Gesetz der Transformation der Knochen. Berlin: Verlag von August Hirschwald.
93. Zelditch ML, Swiderski DL, Sheets HD, etal. (2004) Geometric Morphometrics for Biologists: a Primer. San Diego: Elsevier Academic Press.