Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-848d4c4894-4rdrl Total loading time: 0 Render date: 2024-06-14T21:07:50.705Z Has data issue: false hasContentIssue false

12 - Structural and Mechanical Changes in Trabecular Bone during Early Development in the Human Femur and Humerus

Published online by Cambridge University Press:  25 March 2017

By
Timothy M. Ryan ,
David A. Raichlen  and
James H. Gosman
Edited by
Christopher J. Percival  and
Joan T. Richtsmeier
Christopher J. Percival
Affiliation:
University of Calgary
Joan T. Richtsmeier
Affiliation:
Pennsylvania State University
Get access
Type
Chapter
Information
Building Bones: Bone Formation and Development in Anthropology , pp. 281 - 302
Publisher: Cambridge University Press
Print publication year: 2017

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abel, R. and Macho, G. A. (2011). Ontogenetic changes in the internal and external morphology of the ilium in modern humans. Journal of Anatomy, 218, 324–335.Google Scholar
Abitbol, M. M. (1987). Evolution of the lumbosacral angle. American Journal of Physical Anthropology, 72, 361–372.Google Scholar
Barak, M. M., Lieberman, D. E. and Hublin, J. J. (2011). A Wolff in sheep’s clothing: trabecular bone adaptation in response to changes in joint loading orientation. Bone, 49, 1141–1151.Google Scholar
Barak, M. M., Lieberman, D. E., Raichlen, D., et al. (2013). Trabecular evidence for a human-like gait in Australopithecus africanus. PLoS ONE, 8, e77687.CrossRefGoogle ScholarPubMed
Bridges, P. S., Blitz, J. H. and Solano, M. C. (2000). Changes in long bone diaphyseal strength with horticultural intensification in West-Central Illinois. American Journal of Physical Anthropology, 112, 217–238.3.0.CO;2-E>CrossRefGoogle ScholarPubMed
Byers, S., Moore, A. J., Byard, R. W. and Fazzalari, N. L. (2000). Quantitative histomorphometric analysis of the human growth plate from birth to adolescence. Bone, 27, 495–501.CrossRefGoogle ScholarPubMed
Carlson, K. J. and Judex, S. (2007). Increased non-linear locomotion alters diaphyseal bone shape. Journal of Experimental Biology, 210, 3117–3125.Google Scholar
Carlson, K. J., Lublinsky, S. and Judex, S. (2008). Do different locomotor modes during growth modulate trabecular architecture in the murine hind limb? Integrative and Comparative Biology, 48, 385–393.Google Scholar
Carter, D. R. and Beaupre, G. S. (2001). Skeletal Function and Form. Cambridge: Cambridge University Press.Google Scholar
Carter, D. R. and Wong, M. (1988). The role of mechanical loading histories in the development of diarthrodial joints. Journal of Orthopaedic Research, 6, 804–816.Google Scholar
Carter, D. R., Orr, T. E. and Fyrhie, D. P. (1989). Relationships between loading history and femoral cancellous bone architecture. Journal of Biomechanics, 22, 231–244.CrossRefGoogle ScholarPubMed
Carter, D. R., Wong, M. and Orr, T. E. (1991). Musculoskeletal ontogeny, phylogeny, and functional adaptation. Journal of Biomechanics, 24, 3–16.CrossRefGoogle ScholarPubMed
Chirchir, H. (2015). A comparative study of trabecular bone mass distribution in cursorial and non-cursorial limb joints. Anatomical Record, 298, 797–809.Google Scholar
Chirchir, H., Kivell, T. L., Ruff, C. B., et al. (2015). Recent origin of low trabecular bone density in modern humans. Proceedings of the National Academy of Sciences of the USA, 112, 366–371.CrossRefGoogle ScholarPubMed
Cowgill, L. W., Warrener, A., Pontzer, H. and Ocobock, C. (2010). Waddling and toddling: the biomechanical effects of an immature gait. American Journal of Physical Anthropology, 143, 52–61.Google Scholar
Cunningham, C. A. and Black, S. M. (2009a). Anticipating bipedalism: trabecular organization in the newborn ilium. Journal of Anatomy, 214, 817–829.CrossRefGoogle ScholarPubMed
Cunningham, C. A. and Black, S. M. (2009b). Development of the fetal ilium: challenging concepts of bipedality. Journal of Anatomy, 214, 91–99.CrossRefGoogle ScholarPubMed
Cunningham, C. A. and Black, S. M. (2010). The neonatal ilium-metaphyseal drivers and vascular passengers. Anatomical Record, 293, 1297–1309.Google Scholar
Currey, J. D. (2002). Bones: Structure and Mechanics. Princeton, NJ: Princeton University Press.CrossRefGoogle Scholar
Desilva, J. M. and Devlin, M. J. (2012). A comparative study of the trabecular bony architecture of the talus in humans, non-human primates, and Australopithecus. Journal of Human Evolution, 63, 536–51.Google Scholar
Doube, M., Kłosowski, M. M., Arganda-Carreras, I., et al. (2010). BoneJ: free and extensible bone image analysis in ImageJ. Bone, 47, 1076–1079.CrossRefGoogle ScholarPubMed
Fajardo, R. J., Muller, R., Ketcham, R. A. and Colbert, M. (2007). Nonhuman anthropoid primate femoral neck trabecular architecture and its relationship to locomotor mode. Anatomical Record, 290, 422–436.Google Scholar
Forwood, M. R. and Burr, D. B. (1993). Physical activity and bone mass – exercises in futility. Bone and Mineral, 21, 89–112.Google Scholar
Gosman, J. H. and Ketcham, R. A. (2009). Patterns in ontogeny of human trabecular bone from SunWatch Village in the Prehistoric Ohio Valley: general features of microarchitectural change. American Journal of Physical Anthropology, 138, 318–332.Google Scholar
Gosman, J. H., Hubbell, Z. R., Shaw, C. N. and Ryan, T. M. (2013). Development of cortical bone geometry in the human femoral and tibial diaphysis. Anatomical Record, 296, 774–787.Google Scholar
Hildebrand, T. and Rüegsegger, P. (1997). A new method for the model-independent assessment of thickness in three-dimensional images. Journal of Microscopy, 185, 67–75.Google Scholar
Hodgskinson, R. and Currey, J. D. (1990). Effects of structural variation on Young’s modulus of non-human cancellous bone. Proceedings of the Institution of Mechanical Engineers. Part H, Journal of Engineering in Medicine, 204, 43–52.CrossRefGoogle ScholarPubMed
Larsen, C. S. (1995). Biological changes in human populations with agriculture. Annual Review of Anthropology, 24, 185–213.Google Scholar
Larsen, C. S. (2015). Bioarchaeology: Interpreting Behavior from the Human Skeleton. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Lazenby, R. A., Angus, S., Cooper, D. M. L. and Hallgrimsson, B. (2008a). A three-dimensional microcomputed tomographic study of site-specific variation in trabecular microarchitecture in the human second metacarpal. Journal of Anatomy, 213, 698–705.CrossRefGoogle ScholarPubMed
Lazenby, R. A., Cooper, D. M., Angus, S. and Hallgrimsson, B. (2008b). Articular constraint, handedness, and directional asymmetry in the human second metacarpal. Journal of Human Evolution, 54, 875–885.Google Scholar
Lazenby, R. A., Skinner, M. M., Hublin, J. J. and Boesch, C. (2011). Metacarpal trabecular architecture variation in the chimpanzee (Pan troglodytes): evidence for locomotion and tool-use? American Journal of Physical Anthropology, 144, 215–225.CrossRefGoogle ScholarPubMed
Lieberman, D. E. (1997). Making behavioral and phylogenetic inferences from hominid fossils: considering the developmental influence of mechanical forces. Annual Reviews in Anthropology, 26, 185–210.Google Scholar
MacLatchy, L. and Müller, R. (2002). A comparison of the femoral head and neck trabecular architecture of Galago and Perodicticus using micro-computed tomography (µCT). Journal of Human Evolution, 43, 89–105.Google Scholar
Maclean, S. J., Black, S. M. and Cunningham, C. A. (2014). The developing juvenile ischium: macro-radiographic insights. Clinical Anatomy, 27, 906–914.Google Scholar
Martin, R. B., Burr, D. B. and Sharkey, N. A. (1998). Skeletal Tissue Mechanics. New York, NY: Springer-Verlag.Google Scholar
Matarazzo, S. A. (2015). Trabecular architecture of the manual elements reflects locomotor patterns in primates. PLoS ONE, 10.3, e0120436.Google Scholar
Milner, G. R., Smith, V. G., Santure, S. K., Harn, A. D. and Esarey, D. (1990). Oneota human skeletal remains. In: Archaeological Investigations at the Morton Village and Norris Farms 36 Cemetery. Springfield, IL: Illinois State Museum.Google Scholar
Mittra, E., Rubin, C. and Qin, Y.-X. (2005). Interrelationships of trabecular mechanical and microstructural properties in sheep trabecular bone. Journal of Biomechanics, 38, 1229–1237.CrossRefGoogle ScholarPubMed
Morgan, E. F., Bayraktar, H. H. and Keaveny, T. M. (2003). Trabecular bone modulus–density relationships depend on anatomic site. Journal of Biomechanics, 36, 897–904.CrossRefGoogle ScholarPubMed
Nafei, A., Danielsen, C. C., Linde, F. and Hvid, I. (2000a). Properties of growing trabecular ovine bone – Part I: Mechanical and physical properties. Journal of Bone and Joint Surgery. British Volume, 82B, 910–920.Google Scholar
Nafei, A., Kabel, J., Odgaard, A., Linde, F. and Hvid, I. (2000b). Properties of growing trabecular ovine bone – Part II: Architectural and mechanical properties. Journal of Bone and Joint Surgery. British Volume, 82B, 921–927.Google Scholar
Odgaard, A. and Gundersen, H. J. G. (1993). Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstruction. Bone, 14, 173–182.CrossRefGoogle Scholar
Parfitt, A. M., Travers, R., Rauch, F. and Glorieux, F. H. (2000). Structural and cellular changes during bone growth in healthy children. Bone, 27, 487–494.Google Scholar
Pearson, O. M. and Lieberman, D. E. (2004). The aging of Wolff’s “law”: ontogeny and responses to mechanical loading in cortical bone. Yearbook of Physical Anthropology, 47, 63–99.CrossRefGoogle Scholar
R Development Core Team. (2013). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for statistical Computing.Google Scholar
Raichlen, D., Gordon, A., Foster, A., et al. (2015). An ontogenetic framework linking locomotion and trabecular bone architecture with applications for reconstructing hominin life history. Journal of Human Evolution, 81, 1–12.Google Scholar
Reissis, D. and Abel, R. L. (2012). Development of fetal trabecular micro-architecture in the humerus and femur. Journal of Anatomy, 220, 496–503.Google Scholar
Ridler, T. W. and Calvard, S. (1978). Picture thresholding using an iterative selection method. IEEE Transactions on Systems, Man and Cybernetics, SMC-8, 630–632.Google Scholar
Ruff, C. B. (2003a). Growth in bone strength, body size, and muscle size in a juvenile longitudinal sample. Bone, 33, 317–329.CrossRefGoogle Scholar
Ruff, C. B. (2003b). Ontogenetic adaptation to bipedalism: age changes in femoral to humeral length and strength proportions in humans, with a comparison to baboons. Journal of Human Evolution, 45, 317–349.Google Scholar
Ruff, C. B. (2005a). Growth tracking of femoral and humeral strength from infancy through late adolescence. Acta Paediatrica, 94, 1030–1037.Google Scholar
Ruff, C. B. (2005b). Mechanical determinants of bone form: insights from skeletal remains. Journal of Musculoskeletal & Neuronal Interactions, 5, 202–212.Google Scholar
Ruff, C. B. (2006). Gracilization of the modern human skeleton – the latent strength in our slender bones teaches lessons about human lives, current and past. American Scientist, 94, 508–514.CrossRefGoogle Scholar
Ruff, C. B. (2009). Relative limb strength and locomotion in Homo habilis. American Journal of Physical Anthropology, 138, 90–100.Google Scholar
Ryan, T. M. and Ketcham, R. A. (2002a). Femoral head trabecular bone structure in two omomyid primates. Journal of Human Evolution, 43, 241–263.Google Scholar
Ryan, T. M. and Ketcham, R. A. (2002b). The three-dimensional structure of trabecular bone in the femoral head of strepsirrhine primates. Journal of Human Evolution, 43, 1–26.CrossRefGoogle ScholarPubMed
Ryan, T. M. and Ketcham, R. A. (2005). The angular orientation of trabecular bone in the femoral head and its relationship to hip joint loads in leaping primates. Journal of Morphology, 265, 249–263.Google Scholar
Ryan, T. M. and Krovitz, G. E. (2006). Trabecular bone ontogeny in the human proximal femur. Journal of Human Evolution, 51, 591–602.Google Scholar
Ryan, T. M. and Shaw, C. N. (2012). Unique suites of trabecular bone features characterize locomotor behavior in human and non-human anthropoid primates. PLoS ONE, 7, e41037.Google Scholar
Ryan, T. M. and Shaw, C. N. (2015). Gracility of the modern Homo sapiens skeleton is the result of decreased biomechanical loading. Proceedings of the National Academy of Sciences of the USA, 112, 372–377.Google Scholar
Ryan, T. M. and Walker, A. (2010). Trabecular bone structure in the humeral and femoral heads of anthropoid primates. Anatomical Record, 293, 719–729.Google Scholar
Salle, B. L., Rauch, F., Travers, R., Bouvier, R. and Glorieux, F. H. (2002). Human fetal bone development: histomorphometric evaluation of the proximal femoral metaphysis. Bone, 30, 823–828.Google Scholar
Santure, S. K., Harn, A. D. and Esarey, D. (1990). Archaeological Investigations at the Morton Village and Norris Farms 36 Cemetery. Springfield, IL: Illinois State Museum.Google Scholar
Schneider, C. A., Rasband, W. S. and Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671–675.Google Scholar
Shaw, C. N. and Ryan, T. M. (2012). Does skeletal anatomy reflect adaptation to locomotor patterns? Cortical and trabecular architecture in human and nonhuman anthropoids. American Journal of Physical Anthropology, 147, 187–200.CrossRefGoogle ScholarPubMed
Shaw, C. N. and Stock, J. T. (2009a). Habitual throwing and swimming correspond with upper limb diaphyseal strength and shape in modern human athletes. American Journal of Physical Anthropology, 140, 160–172.Google Scholar
Shaw, C. N. and Stock, J. T. (2009b). Intensity, repetitiveness, and directionality of habitual adolescent mobility patterns influence the tibial diaphysis morphology of athletes. American Journal of Physical Anthropology, 140, 149–159.Google Scholar
Skinner, M. M., Stephens, N. B., Tsegai, Z. J., et al. (2015). Human evolution. Human-like hand use in Australopithecus africanus. Science, 347, 395–399.Google Scholar
Stanitski, D. F., Nietert, P. J., Stanitski, C. L., Nadjarian, R. K. and Barfield, W. (2000). Relationship of factors affecting age of onset of independent ambulation. Journal of Pediatric Orthopedics, 20, 686–688.Google Scholar
Su, A., Wallace, I. J. and Nakatsukasa, M. (2013). Trabecular bone anisotropy and orientation in an Early Pleistocene hominin talus from East Turkana, Kenya. Journal of Human Evolution, 64, 667–677.Google Scholar
Sutherland, D. (1997). The development of mature gait. Gait and Posture, 6, 163–170.Google Scholar
Sutherland, D. H., Olshen, R. A., Biden, E. N. and Wyatt, M. P. (1988). The Development of Mature Walking. London: MacKeith Press.Google Scholar
Tanck, E., Homminga, J., Van Lenthe, G. H. and Huiskes, R. (2001). Increase in bone volume fraction precedes architectural adaptation in growing bone. Bone, 28, 650–654.Google Scholar
Tardieu, C. and Trinkaus, E. (1994). Early ontogeny of the human femoral bicondylar angle. American Journal of Physical Anthropology, 95, 183–195.Google Scholar
Tracer, D. P. (2002). Did the australopithecines crawl? American Journal of Physical Anthropology, 34, 156–157.Google Scholar
Trussell, H. J. (1979). Comments on “Picture thresholding using an iterative selection method”. IEEE Transactions on Systems, Man and Cybernetics, SMC-9, 311.Google Scholar
Turner, C. H. and Robling, A. G. (2003). Designing exercise regimens to increase bone strength. Exercise and Sport Sciences Reviews, 31, 45–50.Google Scholar
Ulrich, D., van Rietbergen, B., Laib, A. and Rüegsegger, P. (1999). The ability of three-dimensional structural indices to reflect mechanical aspects of trabecular bone. Bone, 25, 55–60.Google Scholar
Valdimarsson, O., Sigurdsson, G., Steingrimsdottir, L. and Karlsson, M. K. (2005). Physical activity in the post-pubertal period is associated with maintenance of pre-pubertal high bone density – a 5-year follow-up. Scandinavian Journal of Medicine & Science in Sports, 15, 280–286.CrossRefGoogle ScholarPubMed
van Rietbergen, B. (2001). Micro-FE analyses of bone: state of the art. Advances in Experimental Medicine and Biology, 496, 21–30.Google Scholar
van Rietbergen, B., Weinans, H., Huiskes, R. and Odgaard, A. (1995). A new method to determine trabecular bone elastic properties and loading using micromechanical finite-element models. Journal of Biomechanics, 28, 69–81.Google Scholar
van Rietbergen, B., Weinans, H., Huiskes, R. and Polman, B. J. W. (1996). Computational strategies for iterative solutions of large FEM applications employing voxel data. International Journal for Numerical Methods in Engineering, 39, 2743–2767.Google Scholar
van Rietbergen, B., Odgaard, A., Kabel, J. and Huiskes, R. (1998). Relationships between bone morphology and bone elastic properties can be accurately quantified using high-resolution computer reconstructions. Journal of Orthopaedic Research, 16, 23–28.Google Scholar
Wallace, I. J., Kwaczala, A. T., Judex, S., Demes, B. and Carlson, K. J. (2013). Physical activity engendering loads from diverse directions augments the growing skeleton. Journal of Musculoskeletal and Neuronal Interactions, 13, 283–288.Google Scholar
Wallace, I. J., Demes, B., Mongle, C., Pearson, O. M., Polk, J. D. and Lieberman, D. E. (2014). Exercise-induced bone formation is poorly linked to local strain magnitude in the sheep tibia. PLoS ONE, 9, e99108.Google Scholar
Wallace, I. J., Gupta, S., Sankaran, J., Demes, B. and Judex, S. (2015). Bone shaft bending strength index is unaffected by exercise and unloading in mice. Journal of Anatomy, 226, 224–228.Google Scholar
Willmore, K. E., Young, N. M. and Richtsmeier, J. T. (2007). Phenotypic variability: Its components, measurement and underlying developmental processes. Evolutionary Biology, 34, 99–120.Google Scholar
Wolschrijn, C. F. and Weijs, W. A. (2004). Development of the trabecular structure within the ulnar medial coronoid process of young dogs. Anatomical Record, 278A, 514–519.Google Scholar
Zeininger, A. (2013). Ontogeny of Bipedalism: Pedal Mechanics and Trabecular Bone Morphology. PhD, University of Texas.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×