Trabecular bone anisotropy and orientation in an Early Pleistocene hominin talus from East Turkana, Kenya

Journal of Human Evolution

Volumn 64, Issue 6, 2013, Pages 667-677

  Su, Anne ^a   Wallace, Ian J ^b   Nakatsukasa, Masato ^c  

^a CLEVELAND STATE UNIVERSITY   (United States)

^b STONY BROOK UNIVERSITY   (United States)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

Ankle; Astragalus; Bone functional adaptation; Cancellous bone; Gait

Indexed keywords

ANISOTROPY; BONE; FUNCTIONAL MORPHOLOGY; HOMINID; LIMB; PLEISTOCENE;

KENYA; RIFT VALLEY; TURKANA;

HOMINIDAE; HOMINOIDEA; PONGO; PONGO PYGMAEUS;

EID: 84877662747     PISSN: 00472484     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhevol.2013.03.003     Document Type: Article

References (74)

1. Abel R., Macho G.A. Ontogenetic changes in the internal and external morphology of the ilium in modern humans. J.Anat. 2011, 218:324-335.
2. Athavale S.A., Joshi S.D., Joshi S.S. Internal architecture of the talus. Foot Ankle Int. 2008, 29:82-86.
3. Barak M.M., Lieberman D.E., Hublin J.J. AWolff in sheep's clothing: trabecular bone adaptation in response to changes in joint loading orientation. Bone 2011, 49:1141-1151.
4. Benn D.I. Fabric shape and the interpretation of sedimentary fabric data. J.Sediment. Res. A 1994, 64:910-915.
5. Bennett M.R., Harris J.W.K., Richmond B.G., Braun D.R., Mbua E., Kiura P., Olago D., Kibunjia M., Omuombo C., Behrensmeyer A.K., Huddart D., Gonzalez S. Early hominin foot morphology based on 1.5-million-year-old footprints from Ileret, Kenya. Science 2009, 323:1197-1201.
6. Carlson K.J., Lublinsky S., Judex S. Do different locomotor modes during growth modulate trabecular architecture in the murine hind limb?. Integr. Comp. Biol. 2008, 48:385-393.
7. Cotter M.M., Simpson S.W., Latimer B.M., Hernandez C.J. Trabecular microarchitecture of hominoid thoracic vertebrae. Anat. Rec. 2009, 292:1098-1106.
8. Cruz-Orive L.M., Karlsson L.M., Larsen S.E., Wainschtein F. Characterizing anisotropy: a new concept. Micron Microsc. Acta 1992, 23:75-76.
9. Cunningham C.A., Black S.M. Development of the fetal ilium - challenging concepts of bipedality. J.Anat. 2009, 214:91-99.
10. Davis R.H. Black Americans in Cleveland from George Peake to Carl B. Stokes, 1796-1969 1972, Associated Publishers, Washington.
11. Day M.H., Wood B.A. Functional affinities of the Olduvai Hominid 8 talus. Man 1968, 3:440.
12. De Wit B., De Clercq D., Aerts P. Biomechanical analysis of the stance phase during barefoot and shod running. J.Biomech. 2000, 33:269-278.
13. DeSilva J.M. Functional morphology of the ankle and the likelihood of climbing in early hominins. Proc. Natl. Acad. Sci. 2009, 106:6567-6572.
14. DeSilva J.M., Devlin M.J. Acomparative study of the trabecular bony architecture of the talus in humans, non-human primates, and Australopithecus. J.Hum. Evol. 2012, 63:536-551.
15. Ding M., Odgaard A., Linde F., Hvid I. Age-related variations in the microstructure of human tibial cancellous bone. J.Orthop. Res. 2002, 20:615-621.
16. Divert C., Mornieux G., Baur H., Mayer F., Belli A. Mechanical comparison of barefoot and shod running. Int. J. Sports Med. 2005, 26:593-598.
17. Doube M., Kłosowski M.M., Arganda-Carreras I., Cordelières F.P., Dougherty R.P., Jackson J.S., Schmid B., Hutchinson J.R., Shefelbine S.J. BoneJ: free and extensible bone image analysis in ImageJ. Bone 2010, 47:1076-1079.
18. Ebraheim N.A., Sabry F.F., Nadim Y. Internal architecture of the talus: implication for talar fracture. Foot Ankle Int. 1999, 20:794-796.
19. Fajardo R., Müller R. Three-dimensional analysis of nonhuman primate trabecular architecture using micro-computed tomography. Am. J. Phys. Anthropol. 2001, 115:327-336.
20. Fisher N.I., Lewis T., Embleton B.J.J. Statistical Analysis of Spherical Data 1987, Cambridge University Press, Cambridge.
21. Fritsch H., Schmitt O., Eggers R. The ossification centre of the talus. Anat. Anzeiger. 1996, 178:455-459.
22. Gebo D.L. Plantigrady and foot adaptation in African apes: implications for hominid origins. Am. J. Phys. Anthropol. 1992, 89:29-58.
23. Gebo D.L., Schwartz G.T. Foot bones from Omo: implications for hominid evolution. Am. J. Phys. Anthropol. 2006, 129:499-511.
24. Gosman J.H., Ketcham R.A. Patterns in ontogeny of human trabecular bone from SunWatch Village in the prehistoric Ohio Valley: general features of microarchitectural change. Am. J. Phys. Anthropol. 2009, 138:318-332.
25. Graham D.J., Midgley N.G. Graphical representation of particle shape using triangular diagrams: an excel spreadsheet method. Earth Surf. Proc. Landf. 2000, 25:1473-1477.
26. Green D.J., Alemseged Z. Australopithecus afarensis scapular ontogeny, function, and the role of climbing in human evolution. Science 2012, 338:514-517.
27. Griffin N.L., D'AoÛt K., Ryan T.M., Richmond B.G., Ketcham R.A., Postnov A. Comparative forefoot trabecular bone architecture in extant hominids. J.Hum. Evol. 2010, 59:202-213.
28. Haile-Selassie Y., Saylor B.Z., Deino A., Levin N.E., Alene M., Latimer B.M. Anew hominin foot from Ethiopia shows multiple Pliocene bipedal adaptations. Nature 2012, 483:565-569.
29. Harrigan T.P., Mann R.W. Characterization of microstructural anisotropy in orthotropic materials using a 2nd rank tensor. J.Mater. Sci. 1984, 19:761-767.
30. Hébert D., Lebrun R., Marivaux L. Comparative three-dimensional structure of the trabecular bone in the talus of primates and its relationship to ankle joint loads generated during locomotion. Anat. Rec. 2012, 295:2069-2088.
31. Homminga J., McCreadie B., Ciarelli T., Weinans H., Goldstein S., Huiskes R. Cancellous bone mechanical properties from normals and patients with hip fractures differ on the structure level, not on the bone hard tissue level. Bone 2002, 30:759-764.
32. Hubbard A.M., Meyer J.S., Davidson R.S., Mahboubi S., Harty M.P. Relationship between the ossification center and cartilaginous anlage in the normal hindfoot in children: study with MR imaging. Am. J. Roentgenol. 1993, 161:849-853.
33. Hunt A., Smith R., Torode M., Keenan A. Inter-segment foot motion and ground reaction forces over the stance phase of walking. Clin. Biomech. 2001, 16:592-600.
34. Hunt K.D. Positional behavior in the Hominoidea. Int. J. Primatol. 1991, 12:95-118.
35. Hunt K.D., Russon A.E., Begun D.R. The special demands of great ape locomotion and posture. The Evolution of Thought 2004, 172-189. Cambridge University Press, Cambridge. A.E. Russon, D.R. Begun (Eds.).
36. Hvid I., Rasmussen O., Jensen N., Nielsen S. Trabecular bone strength profiles at the ankle joint. Clin. Orthop. Relat. R. 1985, 199:306-312.
37. Judex S., Garman R., Squire M., Donahue L.R., Rubin C. Genetically based influences on the site-specific regulation of trabecular and cortical bone morphology. J. Bone Miner. Res. 2004, 19:600-606.
38. Lamy P. The settlement of the longitudinal plantar arch of some African Plio-Pleistocene hominids: a morphological study. J.Hum. Evol. 1986, 15:31-46.
39. Latimer B., Ohman J.C., Lovejoy C.O. Talocrural joint in African hominoids: implications for Australopithecus afarensis. Am. J. Phys. Anthropol. 1987, 74:155-175.
40. Latimer B., Lovejoy C.O. The calcaneus of Australopithecus afarensis and its implications for the evolution of bipedality. Am. J. Phys. Anthropol. 1989, 78:369-386.
41. Lordkipanidze D., Jashashvili T., Vekua A., de Leon M.S.P., Zollikofer C.P.E., Rightmire G.P., Pontzer H., Ferring R., Oms O., Tappen M., Bukhsianidze M., Agustí J., Kahlke R., Kiladze G., Martinez-Navarro B., Mouskhelishvili A., Nioradze M., Rook L. Postcranial evidence from early Homo from Dmanisi, Georgia. Nature 2007, 449:305-310.
42. MacLatchy L., Müller R. Acomparison of the femoral head and neck trabecular architecture of Galago and Perodicticus using micro-computed tomography (μCT). J.Hum. Evol. 2002, 43:89-105.
43. Maga M., Kappelman J., Ryan T.M., Ketcham R.A. Preliminary observations on the calcaneal trabecular microarchitecture of extant large-bodied hominoids. Am. J. Phys. Anthropol. 2006, 129:410-417.
44. Marchi D. Relative strength of the tibia and fibula and locomotor behavior in hominoids. J.Hum. Evol. 2007, 53:647-655.
45. McDougall I., Brown F.H., Vasconcelos P.M., Cohen B.E., Thiede D.S., Buchanan M.J. New single crystal 40Ar/39Ar ages improve time scale for deposition of the Omo Group, Omo-Turkana Basin, East Africa. J.Geol. Soc. Lond. 2012, 169:213-226.
46. Michelson J., Checcone M., Kuhn T., Varner K. Intra-articular load distribution in the human ankle joint during motion. Foot Ankle Int. 2001, 22:226-233.
47. Morio C., Lake M.J., Gueguen N., Rao G., Baly L. The influence of footwear on foot motion during walking and running. J.Biomech. 2009, 42:2081-2088.
48. Müller R., Koller B., Hildebrand T., Laib A., Gianolini S., Ruegsegger P. Resolution dependency of microstructural properties of cancellous bone based on three-dimensional μ-tomography. Technol. Health Care 1996, 4:113.
49. Odgaard A., Kabel J., van Rietbergen B., Dalstra M., Huiskes R. Fabric and elastic principal directions of cancellous bone are closely related. J.Biomech. 1997, 30:487-495.
50. Pal G., Routal R. Architecture of the cancellous bone of the human talus. Anat. Rec. 1998, 252:185-193.
51. Pontzer H., Lieberman D.E., Momin E., Devlin M.J., Polk J.D., Hallgrimsson B., Cooper D.M.L. Trabecular bone in the bird knee responds with high sensitivity to changes in load orientation. J.Exp. Biol. 2006, 209:57-65.
52. Potthast W., Lersch C., Segesser B., Koebke J., Brüggemann G.-P. Intraarticular pressure distribution in the talocrural joint is related to lower leg muscle forces. Clin. Biomech. 2008, 23:632-639.
53. Raikin S.M., Elias I., Zoga A.C., Morrison W.B., Besser M.P., Schweitzer M.E. Osteochondral lesions of the talus: localization and morphologic data from 424 patients using a novel anatomical grid scheme. Foot Ankle Int. 2007, 28:154-161.
54. Ryan T.M., Ketcham R.A. The three-dimensional structure of trabecular bone in the femoral head of strepsirrhine primates. J.Hum. Evol. 2002, 43:1-26.
55. Ryan T.M., Ketcham R.A. Angular orientation of trabecular bone in the femoral head and its relationship to hip joint loads in leaping primates. J.Morphol. 2005, 265:249-263.
56. Ryan T.M., Krovitz G.E. Trabecular bone ontogeny in the human proximal femur. J.Hum. Evol. 2006, 51:591-602.
57. Sacco I.C., Akashi P.M., Hennig E.M. Acomparison of lower limb EMG and ground reaction forces between barefoot and shod gait in participants with diabetic neuropathic and healthy controls. BMC Musculoskel. Dis. 2010, 11:24.
58. Saparin P., Scherf H., Hublin J.J., Fratzl P., Weinkamer R. Structural adaptation of trabecular bone revealed by position resolved analysis of proximal femora of different primates. Anat. Rec. 2011, 294:55-67.
59. Schmitt D., Larson S.G. Heel contact as a function of substrate type and speed in primates. Am. J. Phys. Anthropol. 1995, 96:39-50.
60. Skedros J.G., Hunt K.J., Bloebaum R.D. Relationships of loading history and structural and material characteristics of bone: development of the mule deer calcaneus. J.Morphol. 2004, 259:281-307.
61. Skedros J.G., Sorenson S.M., Hunt K.J., Holyoak J.D. Ontogenetic structural and material variations in ovine calcanei: a model for interpreting bone adaptation. Anat. Rec. 2007, 290:284-300.
62. Sode M., Burghardt A.J., Nissenson R.A., Majumdar S. Resolution dependence of the non-metric trabecular structure indices. Bone 2008, 42:728-736.
63. Stern J.T. Climbing to the top: a personal memoir of Australopithecus afarensis. Evol. Anthropol. 2000, 9:113-133.
64. Tafforeau P., Boistel R., Boller E., Bravin A., Brunet M., Chaimanee Y., Cloetens P., Feist M., Hoszowska J., Jaeger J.-J., Kay R.F., Lazzari V., Marivaux L., Nel A., Nemoz C., Thibault X., Vignaud P., Zabler S. Applications of X-ray synchrotron microtomography for non-destructive 3D studies of paleontological specimens. Appl. Phys. A 2006, 83:195-202.
65. Takechi H., Ito S., Takada T., Nakayama H. Trabecular architecture of the ankle joint. Surg. Radiol. Anat. 1982, 4:227-233.
66. Tanck E., Homminga J., Van Lenthe G., Huiskes R. Increase in bone volume fraction precedes architectural adaptation in growing bone. Bone 2001, 28:650-654.
67. Tochigi Y., Rudert M.J., Saltzman C.L., Amendola A., Brown T.D. Contribution of articular surface geometry to ankle stabilization. J. Bone Jt. Surg. Am. 2006, 88A:2704-2713.
68. Venkataraman V.V., Kraft T.S., Dominy N.J. Tree climbing and human evolution. Proc. Natl. Acad. Sci. 2013, 110:1237-1242.
69. Vereecke E., D'Aout K., de Clercq D., van Elsacker L., Aerts P., van Elsacker L. Dynamic plantar pressure distribution during terrestrial locomotion of bonobos (Pan paniscus). Am. J. Phys. Anthropol. 2003, 120:373-383.
70. Wallace I.J., Tommasini S.M., Judex S., Garland T., Demes B. Geneticvariations and physical activity as determinants of limb bone morphology: an experimental approach using a mouse model. Am. J. Phys. Anthropol. 2012, 148:24-35.
71. Wolf P., List R., Ukelo T., Maiwald C., Stacoff A. Day-to-day consistency oflower extremity kinematics during walking and running. J.Appl. Biomech. 2009, 25:369.
72. Wood B.A. Homo talus from East Rudolf, Kenya. J.Anat. 1974, 117:203-204.
73. Wood B., Constantino P. Paranthropus boisei: fifty years of evidence and analysis. Yearb. Phys. Anthropol. 2007, 50:106-132.
74. Woodcock N.H. Specification of fabric shapes using an eigenvalue method. Geol. Soc. Am. Bull. 1977, 88:1231-1236.