Anticipating bipedalism: Trabecular organization in the newborn ilium

Journal of Anatomy

Volumn 214, Issue 6, 2009, Pages 817-829

  Cunningham, Craig A ^a   Black, Sue M ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Ilium; Juvenile; Micro computed tomography; Quantitative analysis; Trabecular architecture

Indexed keywords

ANATOMICAL VARIATION; ARTICLE; BIOMECHANICS; BONE DEVELOPMENT; BONE RADIOGRAPHY; BONE STRUCTURE; CONTROLLED STUDY; DENSITY GRADIENT; HUMAN; HUMAN TISSUE; ILEUM; LOCOMOTION; MICRO-COMPUTED TOMOGRAPHY; NEWBORN; ONTOGENY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; STRUCTURE ANALYSIS; TRABECULAR BONE; WEIGHT BEARING;

HUMANS; ILIUM; INFANT, NEWBORN; LOCOMOTION; RADIOGRAPHIC IMAGE INTERPRETATION, COMPUTER-ASSISTED; WEIGHT-BEARING; X-RAY MICROTOMOGRAPHY;

ILIA;

EID: 66549127980     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/j.1469-7580.2009.01073.x     Document Type: Article

References (97)

1. Adair FL (1918) The ossification centres of the fetal pelvis. Am J Obst Dis Women Chil 78, 175-199.
2. Aiello L, Dean C (1990) An Introduction to Human Evolutionary Anatomy. London: Academic Press.
3. Alini M, Marriott A, Chen T, Abe S, Poole R (1996) A novel angiogenic molecule produced at the time of chondrocyte hypertrophy during endochondral bone formation. Dev Biol 176, 124-132.
4. Bardeen CR (1905) Studies of the development of the human skeleton. Am J Anat 4, 265-302.
5. Bevill G, Eswaran SK, Gupta A, Papadopoulos P, Keaveny TM (2006) Influence of bone volume fraction and architecture on computed large-deformation failure mechanisms in human trabecular bone. Bone 39, 1218-1225.
6. Biewener AA, Fazzalari NL, Konieczynski DD, Baudinette RV (1996) Adaptive changes in trabecular architecture in relation to functional strain patterns and disuse. Bone 19, 1-8.
7. Bowen V, Cassidy JD (1981) Macroscopic and microscopic anatomy of the sacroiliac joint from embryonic life until the eighth decade. Spine 6, 620-628.
8. Boyd SK, Davison P, Muller R, Gasser JA (2006) Monitoring individual morphological changes over time in ovariectomized rats by in vivo micro-computed tomography. Bone 39, 854-862.
9. Brandi ML, Collin-Osdoby P (2006) Vascular biology and the skeleton. J Bone Min Res 21, 183-192.
10. Byers S, Moore AJ, Byard RW, Fazzalari NL (2000) Quantitative histomorphometric analysis of the human growth plate from birth to adolescence. Bone 27, 495-501.
11. Carter DR, Hayes WC (1977) The compressive behaviour of bone as a two phase porous structure. Am J Bone Joint Surg 59, 954-962.
12. Chappard D, Legrand E, Pascaretti C, BasléMF, Audran M (1999) Comparison of eight histomorphometric methods for measuring trabecular bone architecture by image analysis on histological sections. Microsc Res Tech 45, 303-312.
13. Ciarelli MJ, Goldstein SA, Kuhn JL, Cody DD, Brown MB (1991) Evaluation of orthogonal mechanical properties and density of human trabecular bone from the major metaphyseal regions with materials testing and computed tomography. J Orthopaed Res 9, 674-682.
14. Compston J (2006) Bone quality: What is it and how is it measured? Arq Bras Endocrinol Metabol 50, 579-585.
15. Cooper DML, Turinsky AL, Sensen CW, Hallgrimsson B (2003) Quantitative 3D analysis of the canal network in cortical bone by micro-computed tomography. Anat Rec B New Anat 274(B), 169-179.
16. Crock HV (1996) An Atlas of Vascular Anatomy of the Skeleton & Spinal Cord. London: Martin Dunitz.
17. Cunningham CA, Black SM (2009) Development of the fetal ilium - challenging concepts of bipedality. J Anat 214, 91-99.
18. Dalle Carbonare L, Valenti MT, Bertoldo F, et al. (2005) Bone microarchitecture evaluated by histomorphometry. Micron 36, 609-616.
19. Dalstra M, Huiskes R (1995) Load transfer across the pelvic bone. J Biomech 28, 715-724.
20. Dalstra M, Huiskes R, Odgaard A, Van Erning L (1993) Mechanical and textural properties of pelvic trabecular bone. J Biomech 26, 523-535.
21. Delaere O, Kok V, Nyssen-Behets C, Dhem A (1992) Ossification of the human fetal ilium. Acta Anat 143, 330-334.
22. Ding M, Odgaard A, Hvid I (1999) Accuracy of cancellous bone volume fraction measured by micro-CT scanning. J Biomech 32, 323-326.
23. Ding M, Day JS, Burr D, et al. (2003) Canine cancellous bone microarchitecture after one year of high dose bisphosphonates. Calcified Tissue Int 72, 737-744.
24. Eriksen E F, Eghbali-Fatourechi GZ, Khosla S (2007) Remodeling and vascular spaces in bone. J Bone Min Res 22, 1-6.
25. Evans FG (1957) Stress and Strain in Bones. Springfield, IL: Charles C Thomas.
26. Evans FG (1973) Mechanical Properties of Bone. Springfield, IL: Charles C Thomas.
27. Fajardo RJ, Muller R (2001) Three-dimensional analysis of non-human primate trabecular architecture using micro-computed tomography. Am J Phys Anthropol 115, 327-336.
28. Fajardo RJ, Ryan TM, Kappelman J (2002) Assessing the accuracy of high-resolution X-ray computed tomography of primate trabecular bone by comparisons with histological sections. Am J Phys Anthropol 118, 1-10.
29. Fazekas IGy, Kosa F (1978) Forensic Fetal Osteology. Budapest: Akademiai Kiado.
30. Frost HM (1990) Skeletal structural adaptations to mechanical usage (SATMU): Redefining Wolff's law: The bone modelling problem. Anat Rec 226, 403-413.
31. Gardner E, Grey DJ (1950) Prenatal development of the human hip joint. Am J Anat 87, 163-211.
32. Genant HK, Gordon C, Jiang Y, et al. (2000) Advanced imaging of macrostructure and microstructure of bone. Hormone Res 54, 24-30.
33. Gibson LJ (1985) The mechanical behaviour of cancellous bone. J Biomech 18, 317-328.
34. Glorieux FH, Travers R, Taylor A, et al. (2000) Normative data for iliac bone histomorphometry in growing children. Bone 26, 103-109.
35. Goldstein SA (1987) The mechanical properties of trabecular bone: dependence on anatomic location and function. J Biomech 20, 1055-1061.
36. Gosman JH, Ketcham RA (2008) 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, 318-322.
37. Hadjidakis DJ, Androulakis II (2006) Bone remodeling. Ann NY Acad Sci 1092, 385-396.
38. Hildebrand T, Ruegsegger P (1997) A new method for the model independent assessment of thickness in three dimensional images. J Microsc 185, 67-75.
39. Hildebrand T, Laib A, Muller R, Dequeker J, Ruegsegger P (1999) Direct three-dimensional morphometric analysis of human cancellous bone: Microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Min Res 14, 1167-1174.
40. Huiskes R, Ruimerman R, van Lenthe G, Janssen JD (2000) Effects of mechanical forces on maintenance and adaptation of form in trabecular bone. Nature 405, 704-706.
41. Jee WS (2005) The past, present, and future of bone morphometry: Its contribution to an improved understanding of bone biology. J Bone Min Metabol 23(S), 1-10.
42. Jones KB, Mollano AV, Morcuende JA, Cooper RR, Saltzman CL (2004) Bone and brain: A review of neural, hormonal, and musculoskeletal connections. Iowa Orthop J 24, 123-132.
43. Jones JR, Poologasundarampillai G, Atwood RC, Bernard D, Lee PD (2007) Non-destructive quantitative 3D analysis for the optimization of tissue scaffolds. Biomaterials 28: 1404-1413.
44. Keaveny TM, Morgan EF, Niebur GL, Yeh OC (2001) Biomechanics of trabecular bone. Ann Rev Biomed Eng 3, 307-333.
45. Kim DG, Christopherson GT, Dong XN, Fyhrie DP, Yeni YN (2004) The effect of microcomputed tomography scanning and reconstruction voxel size on the accuracy of stereological measurements in human cancellous bone. Bone 35, 1375-1382.
46. Laib A, Kumer JL, Majumdar S, Lane NE (2001) The temporal changes of trabecular architecture in ovariectomized rats assessed by microCT. Osteop Int 12, 936-941.
47. Lanyon LE (1974) Experimental support for the trajectorial theory of bone structure. J Bone Joint Surg 56B, 160-166.
48. Laurenson RD (1964) The primary ossification of the human ilium. Anat Rec 148, 209-217.
49. Liu XS, Sajda P, Saha PK, Wehrli FW, Guo XE (2006) Quantification of the roles of trabecular architecture and trabecular type in determining the elastic modulus of human trabecular bone. J Bone Min Res 21, 1608-1617.
50. Macchiarelli R, Bondioli L, Galichon V, Tobias PV (1999) Hip bone trabecular architecture shows uniquely distinctive locomotor behaviour in South African australopithecines. J Hum Evol 36, 211-232.
51. Macho GA, Abel RL, Schutkowski H (2005) Age changes in bone microstructure: Do they occur uniformly? Int J Osteoarcheol 15: 421-430.
52. Majumdar S, Kothari M, Augat P, et al. (1998) High-resolution magnetic resonance imaging: Three-dimensional trabecular bone architecture and biomechanical properties. Bone 22, 445-454.
53. Majumder S, Roychowdhury A, Pal S (2004) Variations of stress in pelvic bone during normal walking, considering all active muscles. Trends Biomater Artif Organs 17, 48-53.
54. Martinon-Torres M (2003) Quantifying trabecular orientation in the pelvic cancellous bone of modern Humans, Chimpanzees, and the Kebara 2 Neanderthal. Am J Hum Biol 15, 647-661.
55. McColl DJ, Abel R, Spears IR, Macho GA (2006) Automated method to measure trabecular thickness from microcomputed tomographic scans and its application. Anat Rec A Discov Mol Cell Evol Biol 288A, 982-988.
56. Moore RJ, Durbridge TC, Woods AE, Vernon-Roberts B (1989) Variation in histomorphometric estimates across different sites of the iliac crest. J Clin Pathol 42, 814-816.
57. Mulder L, van Ruijven LJ, Koolstra JH, van Eijden TMGJ (2007) Biomechanical consequences of developmental changes in trabecular architecture and mineralization of the pig mandibular condyle. J Biomech 40, 1575-1582.
58. Müller R (2005) Long-term prediction of three-dimensional bone architecture in simulations of pre-, peri- and post-menopausal microstructural bone remodelling. Osteoporosis Int 16, S25-S35.
59. Müller R, Van Lenthe GH (2006) Trabecular bone failure at the microstructural level. Cur Osteoporosis Rep 4, 80-86.
60. Müller R, Van Campenhout H, Van Damme B, et al. (1998) Morphometric analysis of human bone biopsies: A quantitative structural comparison of histological sections and micro-computed tomography. Bone 23, 59-66.
61. Nagaraja S, Lin ASP, Guldberg RE (2007) Age-related changes in trabecular bone microdamage initiation. Bone 40, 973-980.
62. Nakano H, Watahiki J, Kubota M, et al. (2003) Micro X-ray computed tomography analysis for the evaluation of asymmetrical condylar growth in the rat. Orthod Craniofac Res 6(Suppl. 1), 168-172.
63. Noback CR (1944) The developmental anatomy of the human osseous skeleton during ht eembryonic, fetal and circumnatal periods. Anat Rec 88: 91-125.
64. Noback CR, Robertson GG (1951) Sequences of appearance of ossification centres in the human skeleton during the first five prenatal months. Am J Anat 89, 1-28.
65. Nowlan NC, Murphy P, Prendergast PJ (2007) Mechanobiology of embryonic limb development. Ann NY Acad Sci 1101, 389-411.
66. Nuzzo S, Meneghini C, Braillon P, Bouvier R, Mobilio S, Peyrin F (2003) Microarchitectural and physical changes during fetal growth in human vertebral bone. J Bone Min Res 18(4), 760-768.
67. O'Rahilly R, Gardner E (1975) The timing and sequence of events in the development of the limbs in the human embryo. Anat Embryol 148, 1-23.
68. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ (1987) Bone histomorphometery: Standardization of nomenclature, symbols, and units. J Bone Min Res 2, 595-610.
69. Patel PV, Prevrhal S, Bauer JS, et al. (2005) Trabecular bone structure obtained from multislice spiral computed tomography of the calcaneus predicts osteoporotic vertebral deformities. J Comp Assisted Tomogr 29, 246-253.
70. Petersson J, Brismar T, Smedby O (2006) Analysis of skeletal microstructure with clinical multislice CT. Med Image Comp Comp Assisted Interv: MICCAI 9, 880-887.
71. Pierroz DD, Bouxsein ML, Rizzoli R, Ferrari SL (2006) Combined treatment with a beta-blocker and intermittent PTH improves bone mass and microarchitecture in ovariectomized mice. Bone 39, 260-267.
72. Pitsillides AA (2006) Early effects of embryonic movement: 'a shot out of the dark'. J Anat 208, 417-431.
73. Qin L, Genant HK, Griffith J, Leung KS (2007) Advanced Bioimaging Techniques in Assessment of the Quality of Bone and Scaffold Materials, Techniques and Application, pp. 79-84. Berlin: Springer.
74. Raisz LG (1999) Physiology and pathophysiology of bone remodeling. Clinl Chem 45(8B), 1353-1358.
75. Ripamonti U (2006) Soluble osteogenic molecular signals and the induction of bone formation. Biomaterials 27, 807-822.
76. Ritman EL (2004) Micro-computed tomography-current status and developments. Ann Rev Biomed Eng 6, 185-208.
77. Rodriguez JI, Razquin S, Palacios J, Rubio V (1992) Human growth plate development in the fetal and neonatal period. J Orthop Res 10, 62-71.
78. Rook L, Bondioli L, Kohler M, Moya-Sola S, Macchiarelli R (1999) Oreopithecus was a bipedal ape after all: Evidence from the iliac cancellous architecture. Proc Natl Acad Sci U.S A 96, 8795-8799.
79. Ryan TM, Ketcham RA (2002) Femoral head trabecular bone structure in two omomyid primates. J Hum Evol 43, 241-263.
80. Ryan TM, Krovitz GE (2006) Trabecular bone ontogeny in the human proximal femur. J Hum Evol 51, 591-602.
81. Ryan TM, van Rietbergen B (2005) Mechanical significance of femoral head trabecular bone structure in Loris and Galagos evaluated using micromechanical finite element analysis. Am J Hum Evol 126, 82-96.
82. Salsabili N, Hogg DA (1991) Development of the human sacroiliac joint. Clin Anat 4, 99-108.
83. Saparin P, Thomsen JS, Kurths J, Beller G, Gowin W (2006) Segmentation of bone CT images and assessment of bone structure using measures of complexity. Med Phys 33, 3857-3873.
84. Scheuer L, Black S (2000) Developmental Juvenile Osteology. London: Academic Press.
85. Stauber M, Müller R (2006) Age-related changes in trabecular bone microstructures: Global and local morphometry. Osteoporosis Int 17, 616-626.
86. Stauber M, Müller R (2008) Microcomputed tomography: A method for the non-destructive evaluation of the three dimensional structure of biological specimens. Methods Mol Biol 455, 273-292.
87. Thelen E, Fisher DM, Ridley-Johnson R (2002) The relationship between physical growth and newborn reflex. Inf Behav Devel 25, 72-85.
88. Thomsen JS, Ebbesen EN, Mosekilde LI (2002) Static histomorphometry of human iliac crest and vertebral trabecular bone: A comparative study. Bone 30, 267-274.
89. Turner CH (1998) Three rules for bone adaptation to mechanical stimuli. Bone 23, 339-409.
90. Ulrich D, van Rietbergen B, Laib A, Ruegsegger P (1999) The ability of three-dimensional structural indices to reflect mechanical aspects of trabecular bone. Bone 25, 55-60.
91. Vleeming A, Stoeckart R, Volkers ACW (1990) Relation between form and function in the sacroiliac joint (I): The clinical anatomical aspects. (II): The biomechanical aspects. Spine 15, 130-132.
92. Von Mayer HV (1867) Die Architectur der Spongiosa. Reickert und du Bois-Reymond's Arch 627.
93. Walker JM (1991) Musculoskeletal development: A review. Physl Ther 71, 878-889.
94. Ward FO (1838) Outlook of Human Osteology. London: Renshaw.
95. Whitehouse WJ (1974) The quantitative morphology of anisotropic trabecular bone. J Microsc 101, 153-168.
96. Wolff J (1892) Das Gesetz der Transformation der Knochen. Berlin: Verlag von August Hirschwald.
97. Wolff J (1986) The Law of Bone Remodelling. Berlin: Springer-Verlag. [Translated by P. Maquet and R. Furlong from the original (1892)].