Masticatory loading and bone adaptation in the supraorbital torus of developing macaques

American Journal of Physical Anthropology

Volumn 139, Issue 2, 2009, Pages 193-203

  Kupczik, Kornelius ^a,b   Dobson, C A ^c   Crompton, R H ^d   Phillips, R ^c   Oxnard, C E ^b,e   Fagan, M J ^c   O'Higgins, P ^b  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b UNIVERSITY OF YORK   (United Kingdom)

^c UNIVERSITY OF HULL   (United Kingdom)

^d UNIVERSITY OF LIVERPOOL   (United Kingdom)

^e UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Biomechanics; Finite element analysis; Muscle physiological cross sectional area; Primates

Indexed keywords

ANIMAL TISSUE; ARTICLE; BIOMECHANICS; BONE DEVELOPMENT; BONE GROWTH; CADAVER; CONTROLLED STUDY; DECIDUOUS TOOTH; DENTITION; EXPERIMENTAL MODEL; FACE DEVELOPMENT; MACACA; MASTICATION; MORPHOLOGICAL ADAPTATION; MUSCLE FORCE; NONHUMAN; STRESS STRAIN RELATIONSHIP; WEIGHT BEARING; ZYGOMA;

ADAPTATION, PHYSIOLOGICAL; AGE FACTORS; ANIMALS; BIOMECHANICS; BITE FORCE; FACIAL BONES; FINITE ELEMENT ANALYSIS; MACACA FASCICULARIS; MODELS, ANATOMIC; SEX FACTORS; TOMOGRAPHY, X-RAY COMPUTED;

EID: 60549117552     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.20972     Document Type: Article

References (76)

1. Anapol F, Barry K. 1996. Fiber architecture of the extensors of the hindlimb in semiterrestrial and arboreal guenons. Am J Phys Anthropol 99:429-447. (Pubitemid 26073011)
2. Antón SC. 1999. Macaque masseter muscle: internal architecture, fiber length and cross-sectional area. Int J Primatol 20:441-462. (Pubitemid 29345327)
3. Antón SC. 2000. Macaque pterygoid muscles: internal architecture, fiber length, and cross-sectional area. Int J Primatol 21:131-156. (Pubitemid 30124754)
4. Athanasiou KA, Zhu C-F, Lanctot DR, Agrawal CM, Wang X. 2000. Fundamentals of biomechanics in tissue engineering of bone. Tissue Eng 6:361-381. (Pubitemid 30655946)
5. Beaupré GS, Orr TE, Carter DR. 1990. An approach for time-dependent bone modeling and remodeling - theoretical development. J Orthop Res 8:651-661. (Pubitemid 20303669)
6. Bookstein F, Schäfer K, Prossinger H, Seidler H, Fieder M, Stringer C, Weber GW, Arsuaga JL, Slice DE, Rohlf FJ, Recheis W, Mariam AJ, Marcus LF. 1999. Comparing frontal cranial profiles in archaic and modern Homo by morphometric analysis. Anat Rec 257:217-224. (Pubitemid 30032807)
7. Bouvier M, Hylander WL. 1996. The mechanical or metabolic function of secondary osteonal bone in the monkey Macaca fascicularis. Arch Oral Biol 41:941-950. (Pubitemid 27066625)
8. Camacho DLA, Hopper RH, Lin GM, Myers BS. 1997. An improved method for finite element mesh generation of geometrically complex structures with application to the skull base. J Biomech 30:1067-1070. (Pubitemid 27490237)
9. Carter DR, Beaupré GS. 2001. Skeletal function and form: mechanobiology of skeletal development, aging, and regeneration. Cambridge: Cambridge University Press.
10. Carter DR, Van der Meulen MCH, Beaupré GS. 1996. Skeletal development: mechanical consequences of growth, aging and disease. In: Feldman MR, Kelsey J, editors. Osteoporosis. San Diego: Academic Press. p 333-350.
11. Charras GT, Guldberg RE. 2000. Improving the local solution accuracy of large-scale digital image-based finite element analyses. J Biomech 33:255-259. (Pubitemid 30009846)
12. Chen XB, Chen H. 1998. The influence of alveolar structures on the torsional strain field in a gorilla corporeal cross-section. J Hum Evol 35:611-633. (Pubitemid 29089634)
13. Cowin SC. 2001. Bone modeling and remodeling: theories and computation. In: Cowin SC, editor. Bone mechanics handbook, 2nd ed. Boca Raton, FL: CRC Press. p 1-42.
14. Currey JD. 2002. Bones: structure and mechanics. Princeton: Princeton University Press.
15. Currey JD, Butler G. 1975. The mechanical properties of bone tissue in children. J Bone Joint Surg Am 57:810-814.
16. Curtis N, Kupczik K, O'Higgins P, Moazen M, Fagan MJ. 2008. Predicting skull loading: applying multibody dynamics analysis to a macaque skull. Anat Rec (Hoboken) 291:491-501. (Pubitemid 351644523)
17. Dechow PC, Carlson DS. 1990. Occlusal force and craniofacial biomechanics during growth in rhesus monkeys. Am J Phys Anthropol 83:219-237. (Pubitemid 20359124)
18. Duterloo HS, Enlow DE. 1970. A comparative study of cranial growth in Homo and Macaca. Am J Anat 127:357-368.
19. Endo B. 1966. Experimental studies on the mechanical significance of the form of the human facial skeleton. J Fac Sci Univ Tokyo 8:1-106.
20. Frost HM. 1987. Bone mass and the mechanostat - a proposal. Anat Rec 219:1-9. (Pubitemid 18011912)
21. Frost HM. 1990a. Skeletal structural adaptations to mechanical usage (SATMU): 1. Redefining Wolff 's law: the bone modeling problem. Anat Rec 226:403-413.
22. Frost HM. 1990b. Skeletal structural adaptations to mechanical usage (SATMU): 2. Redefining Wolff 's law: the remodeling problem. Anat Rec 226:414-422.
23. Greaves WS. 1985. The mammalian postorbital bar as a torsion-resisting helical strut. J Zool (Lond) 207:125-136.
24. Gross TS, Edwards JL, McLeod KJ, Rubin CT. 1997. Strain gradients correlate with sites of periosteal bone formation. J Bone Miner Res 12:982-988. (Pubitemid 27225010)
25. Guldberg RE, Hollister SJ, Travers GT. 1998. The accuracy of digital image-based finite element models. J Biomech Eng 120: 289-295. (Pubitemid 28194408)
26. Hilloowala RA, Trent RB. 1988a. Supraorbital ridge and masticatory apparatus 1: primates. Hum Evol 3:343-350. (Pubitemid 19097890)
27. Hilloowala RA, Trent RB. 1988b. Supraorbital ridge and masticatory apparatus 2: humans (Eskimos). Hum Evol 3:351-356. (Pubitemid 19097891)
28. Hsieh YF, Robling AG, Ambrosius WT, Burr DB, Turner CH. 2001. Mechanical loading of diaphyseal bone in vivo: the strain threshold for an osteogenic response varies with location. J Bone Miner Res 16:2291-2297. (Pubitemid 33104721)
29. Huiskes R, Ruimerman R, Van Lenthe GH, Janssen JD. 2000. Effects of mechanical forces on maintenance and adaptation of form in trabecular bone. Nature 405:704-706. (Pubitemid 30428659)
30. Huiskes R, Weinans H, Grootenboer HJ, Dalstra M, Fudala B, Slooff TJ. 1987. Adaptive bone-remodeling theory applied to prosthetic-design analysis. J Biomech 20:1135-1150. (Pubitemid 18010111)
31. Hylander WL, Johnson KR. 1992. Strain gradients in the craniofacial region of primates. In: Davidovitch Z, editor. The biological mechanisms of tooth movement and craniofacial adaptation. Columbus: Ohio State University College of Dentistry. p 559-569.
32. Hylander WL, Johnson KR. 1997. In vivo bone strain patterns in the zygomatic arch of macaques and the significance of these patterns for functional interpretations of craniofacial form. Am J Phys Anthropol 102:203-232.
33. Hylander WL, Picq PG, Johnson KR. 1991. Masticatory-stress hypotheses and the supraorbital region of primates. Am J Phys Anthropol 86:1-36.
34. Kupczik K, Dobson CA, Fagan MJ, Crompton RH, Oxnard CE, O'Higgins P. 2007. Assessing mechanical function of the zygomatic region in macaques: validation and sensitivity testing of finite element models. J Anat 210:41-53. (Pubitemid 46040500)
35. Lieberman DE. 1997. Making behavioral and phylogenetic inferences from hominid fossils: considering the developmental influence of mechanical forces. Annu Rev Anthropol 26:185-210.
36. Lieberman DE. 2000. Ontogeny, homology, and phylogeny in the hominid craniofacial skeleton: the problem of the browridge. In: O'Higgins P, Cohn M, editors. Development, growth and evolution: implications for the study of hominid skeletal evolution. London: Academic Press. p 85-122.
37. Lieberman DE, Pearson OM, Polk JD, Demes B, Crompton AW. 2003. Optimization of bone growth and remodeling in response to loading in tapered mammalian limbs. J Exp Biol 206:3125-3138. (Pubitemid 37181412)
38. Macho GA, Shimizu D, Jiang Y, Spears LR. 2005. Australopithecus anamensis: a finite element approach to studying the functional adaptations of extinct hominins. Anat Rec A Discov Mol Cell Evol Biol 283:310-318. (Pubitemid 40478317)
39. Marinescu R, Daegling DJ, Rapoff AJ. 2005. Finite-element modeling of the anthropoid mandible: the effects of altered boundary conditions. Anat Rec A Discov Mol Cell Evol Biol 283:300-309. (Pubitemid 40478316)
40. Martin RB, Burr DB, Sharkey NA. 1998. Skeletal tissue mechanics. Berlin: Springer.
41. McConnell CJ, Crompton RH. 2001. Finite element stress analysis of food-tooth interactions in primates. In: Middleton J, Jones ML, Shrive NG, Pande GN, editors. Computer methods in biomechanics and biomedical engineering. Amsterdam: Gordon and Breach. p 673-678.
42. Moss ML. 1973. A functional analysis of primate craniofacial growth. In: Zingeser MR, editor. Symposium of the IVth International Congress on Primatology. Vol 3. Basel: Karger. p 191-208.
43. Moss ML, Young RW. 1960. A functional approach to craniology. Am J Phys Anthropol 18:281-292.
44. O'Higgins P, Bastir M, Kupczik K. 2006. Shaping the human face. Int Congr Ser 1296:55-73. (Pubitemid 43903711)
45. Oyen OJ, Rice RW. 1980. Supraorbital development in chimpanzees, macaques and baboons. J Med Primatol 9:161-168. (Pubitemid 10078097)
46. Oyen OJ, Walker AC, Rice RW. 1979. Craniofacial growth in olive baboons (Papio cynocephalus): browridge formation. Growth 43:174-187. (Pubitemid 10196073)
47. Pearson OM, Lieberman DE. 2004. The aging of Wolff 's "law": ontogeny and responses to mechanical loading in cortical bone. Yearb Phys Anthropol 47:63-99.
48. Peterson J, Dechow PC. 2003. Material properties of the human cranial vault and zygoma. Anat Rec A Discov Mol Cell Evol Biol 274:785-797. (Pubitemid 37238377)
49. Preuschoft H, Witzel U. 2004. Functional structure of the skull in hominoidea. Folia Primatol 75:219-252. (Pubitemid 39175323)
50. Radhakrishnan P, Mao JJ. 2004. Nanomechanical properties of facial sutures and sutural mineralization front. J Dent Res 83:470-475. (Pubitemid 41756842)
51. Ravosa MJ. 1991a. Ontogenetic perspective on mechanical and nonmechanical models of primate circumorbital morphology. Am J Phys Anthropol 85:85-112.
52. Ravosa MJ. 1991b. Interspecific perspective on mechanical and non-mechanical models of primate circumorbital morphology. Am J Phys Anthropol 86:369-396.
53. Ravosa MJ, Noble VE, Hylander WL, Johnson KR, Kowalski EM. 2000. Masticatory stress, orbital orientation and the evolution of the primate postorbital bar. J Hum Evol 38:667-693. (Pubitemid 30325192)
54. Richmond BG, Wright BW, Grosse L, Dechow PC, Ross CF, Spencer MA, Strait DS. 2005. Finite element analysis in functional morphology. Anat Rec A Discov Mol Cell Evol Biol 283:259-274. (Pubitemid 40478313)
55. Ross C. 2001. In vivo function of the craniofacial haft: the interorbital "pillar". Am J Phys Anthropol 116:108-139.
56. Ross CF. 1995. Muscular and osseous anatomy of the primate anterior temporal fossa and the functions of the postorbital septum. Am J Phys Anthropol 98:275-306.
57. Ross C, Metzger KA. 2004. Bone strain gradients and optimization in vertebrate skulls. Ann Anat 186:387-396. (Pubitemid 40057695)
58. Ross CF, Hylander WL. 1996. In vivo and in vitro bone strain in the owl monkey circumorbital region and the function of the postorbital septum. Am J Phys Anthropol 101:183-215.
59. Ross CF, Patel BA, Slice DE, Strait DS, Dechow PC, Richmond BG, Spencer MA. 2005. Modeling masticatory muscle force in finite element analysis: sensitivity analysis using principal coordinates analysis. Anat Rec A Discov Mol Cell Evol Biol 283:288-299. (Pubitemid 40478315)
60. Rubin J, Rubin C, Jacobs CR. 2006. Molecular pathways mediating mechanical signaling in bone. Gene 367:1-16. (Pubitemid 43286736)
61. 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.
62. Ruimerman R, van Rietbergen B, Hilbers P, Huiskes R. 2005. The effects of trabecular-bone loading variables on the surface signaling potential for bone remodeling and adaptation. Ann Biomed Eng 33:71-78. (Pubitemid 40496061)
63. Russell MD. 1985. The supraorbital torus - a most remarkable peculiarity. Curr Anthropol 26:337-360.
64. Sellers WI, Crompton RH. 2004. Using sensitivity analysis to validate the predictions of a biomechanical model of bite forces. Ann Anat 186:89-95. (Pubitemid 38239924)
65. Smith K, Beighton D. 1986. The effects of the availability of diet on the levels of exoglycosidases in the supragingival plaque of macaque monkeys. J Dent Res 65:1349-1352.
66. Smith K, Beighton D. 1987. Proteolytic activities in the supragingival plaque of monkeys (Macaca fascicularis). Arch Oral Biol 32:473-476.
67. Strait DS, Richmond BG, Spencer MA, Ross CF, Dechow PC, Wood BA. 2007. Masticatory biomechanics and its relevance to early hominid phylogeny: an examination of palatal thickness using finite-element analysis. J Hum Evol 52:585-599. (Pubitemid 46672876)
68. Strait DS, Wang Q, Dechow PC, Ross CF, Richmond BG, Spencer MA, Patel BA. 2005. Modeling elastic properties in finite element analysis: how much precision is needed to produce an accurate model? Anat Rec A Discov Mol Cell Evol Biol 283:275-287.
69. Turner CH. 1999. Toward a mathematical description of bone biology: the principle of cellular accommodation. Calcif Tissue Int 65:466-471.
70. Ulrich D, van Rietbergen B, Weinans H, Rüegsegger P. 1998. Finite element analysis of trabecular bone structure: a comparison of image-based meshing techniques. J Biomech 31:1187-1192. (Pubitemid 29005189)
71. Verhulp E, van Rietbergen B, Huiskes R. 2006. Comparison of micro-level and continuum-level voxel models of the proximal femur. J Biomech 39:2951-2957. (Pubitemid 44803032)
72. Wang Q, Strait DS, Dechow PC. 2006. Fusion patterns of craniofacial sutures in rhesus monkey skulls of known age and sex from Cayo Santiago. Am J Phys Anthropol 131:469-485. (Pubitemid 44760476)
73. Witzel U, Preuschoft H. 2002. Function-dependent shape characteristics of the human skull. Anthropol Anz 60:113-135.
74. Witzel U, Preuschoft H, Sick H. 2004. The role of the zygomatic arch in the statics of the skull and its adaptive shape. Folia Primatol 75:202-218. (Pubitemid 39175322)
75. Wroe S, Moreno K, Clausen P, McHenry C, Curnoe D. 2007. High-resolution three-dimensional computer simulation of hominid cranial mechanics. Anat Rec (Hoboken) 290:1248-1255. (Pubitemid 47573195)
76. Yeni YN, Christophersin GT, Dong XN, Kim D-G, Fyhrie DP. 2005. Effect of microcomputed tomography voxel size on the finite element model accuracy for human cancellous bone. J Biomech Eng 127:1-8. (Pubitemid 40463475)