The Role of the Sutures in Biomechanical Dynamic Simulation of a Macaque Cranial Finite Element Model: Implications for the Evolution of Craniofacial Form

Anatomical Record

Volumn 295, Issue 2, 2012, Pages 278-288

  Wang, Qian ^a   Wood, Sarah A ^b   Grosse, Ian R ^b   Ross, Callum F ^c   Zapata, Uriel ^a   Byron, Craig D ^d   Wright, Barth W ^e   Strait, David S ^f  

^a MERCER UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b University of Massachusetts   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d MERCER UNIVERSITY   (United States)

^e KANSAS CITY UNIVERSITY OF MEDICINE AND BIOSCIENCES   (United States)

^f STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

Elastic properties; Loading speed; Vertebrate skulls

Indexed keywords

ARTICLE; CRANIOFACIAL MORPHOLOGY; ENERGY; FEMALE; FORCE; MACACA; MALE; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; SKULL; STRESS STRAIN RELATIONSHIP; SUTURE; VELOCITY; VERTEBRATE;

ANIMALS; BIOLOGICAL EVOLUTION; BIOMECHANICS; COMPUTER SIMULATION; CRANIAL SUTURES; FINITE ELEMENT ANALYSIS; MACACA; MODELS, ANATOMIC; SKULL; STRESS, MECHANICAL;

MACACA MULATTA; VERTEBRATA;

EID: 84855814329     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.21532     Document Type: Article

References (90)

1. Antón SC. 1990. Neandertals and the anterior dental hypothesis: a biomechanical evaluation of bite force production. Kroeber Anthropological Society Papers 71-72: 67-76.
2. Antón SC. 1993. Internal masticatory muscle architecture in the Japanese macaque and its influence on bony morphology (Abstract). Am J Phys Anthropol S16: 50.
3. Bastir M, O'Higgins P, Rosas A. 2007. Facial ontogeny in Neanderthals and modern humans. Proc Biol Sci 274: 1125-1132.
4. Behrents RG, Carlson DS, Abdelnour T. 1978. In vivo analysis of bone strain about the sagittal suture in Macaca mulatta during masticatory movements. J Dent Res 57: 904-908.
5. Bright JA, Gröning F. 2011. Strain accommodation in the zygomatic arch of the pig: a validation study using digital speckle pattern interferometry and finite element analysis. J Morphol 272: 1388-1398.
6. Byron CD. 2006. Role of the osteoclast in cranial suture waveform patterning. Anat Rec 288A: 552-563.
7. Byron CD. 2009. Cranial suture morphology and its relationship to diet in Cebus. J Hum Evol 57: 649-655.
8. Byron CD, Borke J, Yu J, Pashley D, Wingard CJ, Hamrick M. 2004. Effects of increased muscle mass on mouse sagittal suture morphology and mechanics. Anat Rec 279A: 676-684.
9. Cho HJ. 2009. A three-dimensional cephalometric analysis. J Clin Orthod 43: 235-252.
10. Daegling DJ. 1996. Growth in the mandibles of African apes. J Hum Evol 30: 315-341.
11. Dechow PC, Carlson DS. 1990. Occlusal force and craniofacial biomechanics during growth in rhesus monkeys. Am J Phys Anthropol 83: 219-237.
12. Dumont ER, Herrel A. 2003. The effects of gape angle and bite point on bite force in bats. J Exp Biol 206: 2117-2123.
13. Dumont ER, Piccirillo J, Grosse IR. 2005. Finite-element analysis of biting behavior and bone stress in the facial skeletons of bats. Anat Rec 283A: 319-330.
14. Farke AA. 2008. Frontal sinuses and head-butting in goats: a finite element analysis. J Exp Biol 211: 3085-3094.
15. Gilbert CC, Frost SR, Strait DS. 2009. Allometry, sexual dimorphism, and phylogeny: a cladistic analysis of extant African papionins using craniodental data. J Hum Evol 57: 298-320.
16. Grosse IR, Dumont ER, Coletta C, Tolleson A. 2007. Techniques for modeling muscle-induced forces in finite element models of skeletal structures. Anat Rec 290: 1069-1088.
17. Hartwig WC. 1991. Fractal analysis of sagittal suture morphology. J Morphol 210: 289-298.
18. Herring SW. 1993. Epigenetic and functional influences on skull growth. Skull 1: 153-206.
19. Herring SW, Mucci RJ. 1991. In vivo strain in cranial sutures: the zygomatic arch. J Morphol 207: 225-239.
20. Herring SW, Rafferty KL. 2000. Cranial and facial sutures: functional loading in relation to growth and morphology. In: Davidovitch Z, Mah J, editors. Biological mechanisms of tooth eruption, resorption and replacement by implants. Boston: Harvard Soc Adv Orthodontics. p 269-276.
21. Herring SW, Teng S. 2000. Strain in the braincase and its sutures during function. Am J Phys Anthropol 112: 575-593.
22. Holliday CM, Gardner NM, Paesani SM, Douthitt M, Ratliff JL. 2010. Microanatomy of the mandibular symphysis in lizards: patterns in fiber orientation and Meckel's cartilage and their significance in cranial evolution. Anat Rec 293: 1350-1359.
23. Hylander WL. 1977a. The adaptive significance of Eskimo craniofacial morphology. In: Dahlberg AA, Graber TM, editors. Orofacial growth and development. The Hague: Mouton. p 129-169.
24. Hylander WL. 1977b. In vivo bone strain in the mandible of Galago crassicaudatus. Am J Phys Anthropol 46: 309-326.
25. Hylander WL, Picq PG, Johnson KR. 1991. Masticatory-stress hypothesis and the supraorbital region of primates. Am J Phys Anthropol 86: 1-36.
26. Jasinoski SC, Rayfield EJ, Chinsamy A. 2010a. Functional implications of dicynodont cranial suture morphology. J Morphol 271: 705-728.
27. Jasinoski SC, Reddy BD, Louw KK, Chinsamy A. 2010b. Mechanics of cranial sutures using the finite element method. J Biomech 43: 3104-3111.
28. Jaslow CR. 1990. Mechanical properties of cranial sutures. J Biomech 23: 313-321.
29. Jaslow CR, Biewener AA. 1995. Strain patterns in the horncores, cranial bones and sutures of goats (Capra hircus) during impact loading. J Zool 235: 193-210.
30. Kupczik K, Dobson CA, Crompton RH, Phillips R, Oxnard CE, Fagan MJ, O'Higgins P. 2009. Masticatory loading and bone adaptation in the supraorbital torus of developing macaques. Am J Phys Anthropol 139: 193-203.
31. 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.
32. Lieberman DE, Krovitz GE, Yates FW, Devlin M, St. Claire M. 2004. Effects of food processing on masticatory strain and craniofacial growth in a retrognathic face. J Hum Evol 46: 655-677.
33. Long CA. 1985. Intricate sutures as fractal curves. J Morphol 185: 285-295.
34. Long CA, Long JE. 1992. Fractal dimensions of cranial sutures and waveforms. Acta Anat (Basel) 145: 201-206.
35. Lynnerup N, Jacobsen JC. 2003. Brief communication: age and fractal dimensions of human sagittal and coronal sutures. Am J Phys Anthropol 121: 332-336.
36. Mendez J, Keys A. 1960. Density and composition of mammalian muscle. Metabolism 9: 184-188.
37. Moazen M, Curtis N, Evans SE, O'Higgins P, Fagan MJ. 2008. Combined finite element and multibody dynamics analysis of biting in a Uromastyx hardwickii lizard skull. J Anat 213: 499-508.
38. Moazen M, Curtis N, O'Higgins P, Evans SE, Fagan MJ. 2009a. Biomechanical assessment of evolutionary changes in the lepidosaurian skull. Proc Natl Acad Sci USA 106: 8273-8277.
39. Moazen M, Curtis N, O'Higgins P, Jones MEH, Evans SE, Fagan MJ. 2009b. Assessment of the role of sutures in a lizard skull: a computer modelling study. Proc R Soc Lond B Biol Sci 276: 39-46.
40. Monteiro LR, Lessa LG. 2000. Comparative analysis of cranial suture complexity in the genus Caiman (Crocodylia, Alligatoridae). Braz J Biol 60: 689-694.
41. Moss ML. 1954. Growth of the calvaria in the rat. The determination of osseous morphology. Am J Anat 94: 333-362.
42. Moss ML. 1957. Experimental alteration of sutural area morphology. Anat Rec 127: 569-589.
43. Moss ML. 1961. Extrinsic determination of sutural area morphology in the rat calvaria. Acta Anat (Basel) 44: 263-272.
44. Moss ML. 1962. The functional matrix. In: Kraus B, Reidel R, editors. Vistas in orthodontics. Philadelphia: Lea & Febiger. p 85-98.
45. Moss ML, Young RW. 1960. A functional approach to craniology. Am J Phys Anthropol 18: 281-292.
46. Odame P, Yu JC, Zhang G. 2005. 3D Finite Element study of stress distribution at the cranial bone/suture interface. Transactions of the Society for Biomaterials 26: 556.
47. Opperman LA. 2000. Cranial sutures as intramembranous bone growth sites. Dev Dyn 219: 472-485.
48. Opperman LA, Chhabra A, Nolen AA, Bao Y, Ogle RC. 1998. Dura mater maintains rat cranial sutures in vitro by regulating suture cell proliferation and collagen production. J Craniofac Genet Dev Biol 18: 150-158.
49. Opperman LA, Passarelli RW, Morgan EP, Reintjes M, Ogle RC. 1995. Cranial sutures require tissue interactions with dura mater to resist osseous obliteration in vitro. J Bone Miner Res 10: 1978-1987.
50. Opperman LA, Sweeney TM, Redmon J, Persing JA, Ogle RC. 1993. Tissue interactions with underlying dura mater inhibit osseous obliteration of developing cranial sutures. Dev Dyn 198: 312-322.
51. Oudhof HAJ, Van Doorenmaalen WJ. 1983. Skull morphogenesis and growth: hemodynamic influence. Acta Anat 117: 181-186.
52. Okazaki M, Fukumoto M, Takahashi J. 1996. Damped oscillation analysis of natural and artificial periodontal membranes. Ann Biomed Eng 24: 234-240.
53. Payne SL, Holliday CM, Vickaryous MK. 2011. An osteological and histological investigation of cranial joints in geckos. Anat Rec 294: 399-405.
54. Popowics TE, Herring SW. 2007. Load transmission in the nasofrontal suture of the pig, Sus scrofa. J Biomech 40: 837-844.
55. Porro LB, Holliday CM, Anapol F, Ontiveros LC, Ontiveros LT, Ross CF. 2011. Free body analysis, beam mechanics, and finite element analysis of the mandible of Alligator mississippiensis. J Morphol 272: 910-937.
56. Rafferty KL, Herring SW. 1999. Craniofacial sutures: Morphology, growth, and in vivo masticatory strains. J Morphol 242: 167-179.
57. Rafferty KL, Herring SW, Marshall CD. 2003. Biomechanics of the rostrum and the role of facial sutures. J Morphol 257: 33-44.
58. Rak Y. 1983. The Australopithecine face. New York: Academic Press.
59. Ravosa MJ. 1991a. Interspecific perspective on mechanical and nonmechanical models of primate circumorbital morphology. Am J Phys Anthropol 86: 369-396.
60. Ravosa MJ. 1991b. Ontogenetic perspective on mechanical and nonmechanical models of primate circumorbital morphology. Am J Phys Anthropol 85: 95-112.
61. Rayfield EJ. 2004. Cranial mechanics and feeding in Tyrannosaurus rex. Proc R Soc Lond B Biol Sci 271: 1451-1459.
62. Rayfield EJ. 2005. Using finite-element analysis to investigate suture morphology: a case study using large carnivorous dinosaurs. Anat Rec 283A: 349-365.
63. Reed DA, Porro LB, Iriarte-Diaz J, Lemberg JB, Holliday CM, Anapol F, Ross CF. 2011. The impact of bone and suture material properties on mandibular function in Alligator mississippiensis: testing theoretical phenotypes with finite element analysis. J Anat 218: 59-74.
64. Reinholt LE, Burrows AM, Eiting TP, Dumont ER, Smith TD. 2009. Histology and micro CT as methods for assessment of facial suture patency. Am J Phys Anthropol 138: 499-506.
65. Ross CF. 2001. In vivo function of the craniofacial haft: the interorbital "pillar." Am J Phys Anthropol 116: 108-139.
66. Ross CF, Metzger KA. 2004. Bone strain gradients and optimization in vertebrate skulls. Ann Anat 186: 387-396.
67. Saito K, Shimizu Y, Ooya K. 2002. Age-related morphological changes in squamous and parietomastoid sutures of human cranium. Cells Tissues Organs 170: 266-273.
68. Sidor CA. 2001. Simplification as a trend in synapsid cranial evolution. Evolution 58: 1419-1442.
69. Skrzat J, Walocha J. 2003a. Application of fractal dimension in evaluation of cranial suture complexity. Harmonic Fractal Image Anal 1: 39-41.
70. Skrzat J, Walocha J. 2003b. Fractal dimensions of the sagittal (interparietal) sutures in humans. Folia Morphol (Warsz) 62: 119-122.
71. Smith KK, Hylander WL. 1985. Strain gauge measurement of mesokinetic movement in the lizard Varanus exanthematicus. J Exp Biol 114: 53-70.
72. Smith TD, Burrows AM, Dumont ER. 2010. Microanatomical assessment of nasomaxillary suture patency. Anat Rec 293: 651-657.
73. Spencer MA, Demes B. 1993. Biomechanical analysis of masticatory system configuration in Neandertals and Inuits. Am J Phys Anthropol 91: 1-20.
74. Stadler JA, Cortes W, Zhang L-L, Hanger CC, Gosain AK. 2006. A reinvestigation of murine cranial suture biology: microcomputed tomography versus histologic technique. Plast Reconstr Surg 118: 626-634.
75. 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 283A: 275-287.
76. Strait DS, Weber GW, Neubauer S, Chalk J, Richmond BG, Lucas PW, Spencer MA, Schrein C, Dechow PC, Ross CF, Grosse IR, Wright BW, Constantino P, Wood BA, Lawn B, Hylander WL, Wang Q, Byron C, Slice DE, Smith AL. 2009. The feeding biomechanics and dietary ecology of Australopithecus africanus. Proc Natl Acad Sci U S A 106: 2124-2129.
77. Strait DS, Wright BW, Richmond BG, Ross CF, Dechow PC, Spencer MA, Wang Q. 2008. Craniofacial strain patterns during premolar loading: implications for human evolution. In: Vinyard C, Ravosa MJ, Wall C, editors. Primate craniofacial function and biology. New York: Springer. p 173-198.
78. Sun Z, Lee E, Herring SW. 2004. Cranial sutures and bones: growth and fusion in relation to masticatory strain. Anat Rec 276A: 150-161.
79. Trinkaus E. 2003. Neandertal faces were not long; modern human faces are short. Proc Natl Acad Sci USA 100: 8142-8145.
80. Vinyard CJ, Wall CE, Williams SH, Hylander WL. 2003. Comparative functional analysis of skull morphology of tree-gouging primates. Am J Phys Anthropol 120: 153-170.
81. Wang Q. 2012. Dental maturity and the ontogeny of sex-based differences in the dentofacial complex of rhesus macaques from Cayo Santiago. In: Wang Q, editor. Bones, Genetics, and Behavior of Rhesus Macaques: Macaca mulatta of Cayo Santiago and Beyond. Springer: New York. p 177-194.
82. Wang Q, Dechow PC. 2006. Elastic properties of external cortical bone in the craniofacial skeleton of the rhesus monkey. Am J Phys Anthropol 131: 402-415.
83. Wang Q, Dechow PC, Wright BW, Ross CF, Strait DS, Richmond BG, Spencer MA, Byron CD. 2008. Surface strain on bone and sutures in a monkey facial skeleton: an in vitro method and its relevance to Finite Element Analysis. In: Vinyard CJ, Ravosa MJ and Wall CE, editors. Primate craniofacial function and biology. New York: Springer. p 149-172.
84. Wang Q, Opperman LA, Havill LM, Carlson DS, Dechow PC. 2006a. Inheritance of sutural patterns at pterion in rhesus monkeys skulls. Anat Rec 288A: 1042-1049.
85. Wang Q, Strait DS, Dechow PC. 2006b. Fusion patterns of craniofacial sutures in rhesus monkey skulls of known age and sex from Cayo Santiago. Am J Phys Anthropol 131: 469-485.
86. Wang Q, Smith AL, Strait DS, Wright BW, Richmond BG, Grosse IR, Byron CD, Zapata U. 2010a. The global impact of sutures assessed in a Finite Element Model of a macaque cranium. Anat Rec 293: 1477-1491.
87. Wang Q, Wright BW, Smith A, Chalk J, Byron CD. 2010b. Mechanical impact of incisor loading on the primate midfacial skeleton and its relevance to human evolution. Anat Rec 293: 607-617.
88. Williams SH, Vinyard CJ, Wall CE, Hylander WL. 2009. Mandibular corpus bone strain in goats and alpacas: implications for understanding the biomechanics of mandibular form in selenodont artiodactyls. J Anat 214: 65-78.
89. Wright BW. 2005. Craniodental biomechanics and dietary toughness in the genus Cebus. J Hum Evol 48: 473-492.
90. Yu JC, Wright RL, Williamson MA, Braselton JP, Abell ML. 2003. A fractal analysis of human cranial sutures. Cleft Palate Craniofac J 40: 409-415.