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Skull base embryology: a multidisciplinary review

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Abstract

Introduction

The skull base represents a central and complex bone structure of the skull and forms the floor of the cranial cavity on which the brain lies. Anatomical knowledge of this particular region is important for understanding several pathologic conditions as well as for planning surgical procedures. Embryology of the cranial base is of great interest due to its pronounced impact on the development of adjacent regions including the brain, neck, and craniofacial skeleton.

Materials and methods

Information from human and comparative anatomy, anthropology, embryology, surgery, and computed modelling was integrated to provide a perspective to interpret skull base formation and variability within the cranial functional and structural system.

Results and conclusions

The skull base undergoes an elaborate sequence of development stages and represents a key player in skull, face and brain development. Furthering our holistic understanding of the embryology of the skull base promises to expand our knowledge and enhance our ability to treat associated anomalies.

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References

  1. Ross C, Henneberg M (1995) Basicranial flexion, relative brain size, and facial kyphosis in Homo sapiens and some fossil hominids. Am J Phys Anthropol 98:575–593

    Article  CAS  PubMed  Google Scholar 

  2. Tubbs RS, Salter EG, Oakes WJ (2005) Duplication of the occipital condyles. Clin Anat 18:92–95

    Article  PubMed  Google Scholar 

  3. Ross CF, Ravosa MJ (1993) Basicranial flexion, relative brain size, and facial kyphosis in nonhuman primates. Am J Phys Anthropol 91:305–324

    Article  CAS  PubMed  Google Scholar 

  4. Lomholt JF, Fischer-Hansen B, Keeling JW, Reintoft I, Kjaer I (2004) Subclassification of anencephalic human fetuses according to morphology of the posterior cranial fossa. Pediatr Dev Pathol 7:601–606

    Article  PubMed  Google Scholar 

  5. Jeffery N (2005) Cranial base angulation and growth of the human fetal pharynx. Anat Rec A: Discov Mol Cell Evol Biol 284:491–499

    Article  Google Scholar 

  6. Jeffery N, Spoor F (2002) Brain size and the human cranial base: a prenatal perspective. Am J Phys Anthropol 118:324–340

    Article  PubMed  Google Scholar 

  7. Lieberman DE, Ross CF, Ravosa MJ (2000) The primate cranial base: ontogeny, function, and integration. Am J Phys Anthropol Suppl 31:117–169

    Article  Google Scholar 

  8. McBratney-Owen B, Iseki S, Bamforth SD, Olsen BR, Morriss-Kay GM (2008) Development and tissue origins of the mammalian cranial base. Dev Biol 322:121–132

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Nie X (2005) Cranial base in craniofacial development: developmental features, influence on facial growth, anomaly, and molecular basis. Acta Odontol Scand 63:127–135

    Article  PubMed  Google Scholar 

  10. Di Ieva A, Bruner E, Davidson J, Pisano P, Haider T, Stone SS, Cusimano MD, Tschabitscher M, Grizzi F (2013) Cranial sutures: a multidisciplinary review. Childs Nerv Syst 29:893–905

    Google Scholar 

  11. Iaconetta G, Fusco M, Cavallo LM, Cappabianca P, Samii M, Tschabitscher M (2007) The abducens nerve: microanatomic and endoscopic study. Neurosurgery 61:7–14, discussion 14

    Article  PubMed  Google Scholar 

  12. Harris FS, Rhoton AL (1976) Anatomy of the cavernous sinus. A microsurgical study. J Neurosurg 45:169–180

    Article  CAS  PubMed  Google Scholar 

  13. Skrzat J, Walocha J, Srodek R, Nizankowska A (2006) An atypical position of the foramen ovale. Folia Morphol 65:396–399

    CAS  Google Scholar 

  14. Umansky F, Elidan J, Valarezo A (1991) Dorello’s canal: a microanatomical study. J Neurosurg 75:294–298

    Article  CAS  PubMed  Google Scholar 

  15. Standring S (2008) GRAY’S anatomy — the anatomical basis of clinical practice. Churchill Livingstone Elsevier, Edinburgh

    Google Scholar 

  16. Lam A, Holbrook E (2013) Skull base anatomy and CSF rhinorrhea. Adv Oto-Rhino-Laryngol 74:1–11

    Article  Google Scholar 

  17. Koblmüller L (1934) A case of condylus tertius. Anat Anz 71:305–352

    Google Scholar 

  18. Allen W (1880) On tertiary occipital condyle. J Anat Physiol 15:60–68

    CAS  PubMed Central  PubMed  Google Scholar 

  19. Bolk L (1921) Different forms and origniation of Condylus tertius. Anat Anz 54

  20. Jiang X, Iseki S, Maxson RE, Sucov HM, Morriss-Kay GM (2002) Tissue origins and interactions in the mammalian skull vault. Dev Biol 241:106–116

    Article  CAS  PubMed  Google Scholar 

  21. Santaolalla-Montoya F, Martinez-Ibarguen A, Sanchez-Fernandez JM, Sanchez-del-Rey A (2012) Principles of cranial base ossification in humans and rats. Acta Oto-Laryngol 132:349–354

    Article  Google Scholar 

  22. Nie X, Luukko K, Fjeld K, Kvinnsland IH, Kettunen P (2005) Developmental expression of Dkk1-3 and Mmp9 and apoptosis in cranial base of mice. J Mol Histol 36:419–426

    Article  CAS  PubMed  Google Scholar 

  23. Young B, Minugh-Purvis N, Shimo T, St-Jacques B, Iwamoto M, Enomoto-Iwamoto M, Koyama E, Pacifici M (2006) Indian and sonic hedgehogs regulate synchondrosis growth plate and cranial base development and function. Dev Biol 299:272–282

    Article  CAS  PubMed  Google Scholar 

  24. Riccomagno MM, Martinu L, Mulheisen M, Wu DK, Epstein DJ (2002) Specification of the mammalian cochlea is dependent on Sonic hedgehog. Genes Dev 16:2365–2378

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Balczerski B, Zakaria S, Tucker AS, Borycki AG, Koyama E, Pacifici M, Francis-West P (2012) Distinct spatiotemporal roles of hedgehog signalling during chick and mouse cranial base and axial skeleton development. Dev Biol 371:203–214

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Nie X, Luukko K, Kvinnsland IH, Kettunen P (2005) Developmentally regulated expression of Shh and Ihh in the developing mouse cranial base: comparison with Sox9 expression. Anat Rec A: Discov Mol Cell Evol Biol 286:891–898

    Article  Google Scholar 

  27. Couly GF, Coltey PM, Le Douarin NM (1993) The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. Development 117:409–429

    CAS  PubMed  Google Scholar 

  28. Evans DJ, Noden DM (2006) Spatial relations between avian craniofacial neural crest and paraxial mesoderm cells. Dev Dyn 235:1310–1325

    Article  PubMed  Google Scholar 

  29. Cankal F, Ugur HC, Tekdemir I, Elhan A, Karahan T, Sevim A (2004) Fossa navicularis: anatomic variation at the skull base. Clin Anat 17:118–122

    Article  CAS  PubMed  Google Scholar 

  30. Miller RH, Sneed WF (1985) Tornwaldt’s bursa. Clin Otolaryngol Allied Sci 10:21–25

    Article  CAS  PubMed  Google Scholar 

  31. Miyahara H, Matsunaga T (1994) Tornwaldt’s disease. Acta Otolaryngol Suppl 517:36–39

    Article  CAS  PubMed  Google Scholar 

  32. Couly GF, Coltey PM, Le Douarin NM (1992) The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development 114:1–15

    CAS  PubMed  Google Scholar 

  33. Muller F, O'Rahilly R (1994) Occipitocervical segmentation in staged human embryos. J Anat 185(Pt 2):251–258

    PubMed Central  PubMed  Google Scholar 

  34. Kuratani S (2005) Craniofacial development and the evolution of the vertebrates: the old problems on a new background. Zool Sci 22:1–19

    Article  PubMed  Google Scholar 

  35. Hayek H (1927) Analyses of the proatlas, epistropheus, atlas and occipital bone. Morph Jahrb 58

  36. Tubbs RS, Lingo PR, Mortazavi MM, Cohen-Gadol AA (2013) Hypoplastic occipital condyle and third occipital condyle: review of their dysembryology. Clin Anat 26:928–932

    Article  PubMed  Google Scholar 

  37. Nath HD, Mahapatra AK, Gunawat P (2012) A torcular encephalocele with proatlas defect and os-terminale. Asian J Neurosurg 7:84–86

    Article  PubMed Central  PubMed  Google Scholar 

  38. Jacquement (1850) Abnormal articulation of occiput and axis. Bull Soc Anat Paris 25:49

    Google Scholar 

  39. Al-Motabagani MA, Surendra M (2006) Total occipitalization of the atlas. Anat Sci Int 81:173–180

    Article  PubMed  Google Scholar 

  40. Sauser G (1934) Intracranial Manifestation of the last occipital vertebra. Sonderdruck Zeitschr Anat Entwicklungsgeschichte 104

  41. Arey LB (1950) The craniopharyngeal canal reviewed and reinterpreted. Anat Rec 106:1–16

    Article  CAS  PubMed  Google Scholar 

  42. Currarino G, Maravilla KR, Salyer KE (1985) Transsphenoidal canal (large craniopharyngeal canal) and its pathologic implications. AJNR Am J Neuroradiol 6:39–43

    CAS  PubMed  Google Scholar 

  43. Hedlund G (2006) Congenital frontonasal masses: developmental anatomy, malformations, and MR imaging. Pediatr Radiol 36:647–662, quiz 726–647

    Article  PubMed  Google Scholar 

  44. Vermeij-Keers C (1990) Craniofacial embryology and morphogenesis: normal and abnormal. Churchill Livingstone, Edinburgh

    Google Scholar 

  45. Stricker M, Van der Meulen J, Raphael B, Mazzola R (1990) Craniofacial growth and development. Churchill Livingstone, Edinburgh

    Google Scholar 

  46. Davies ML, Macpherson P (1991) Fibrous dysplasia of the skull: disease activity in relation to age. Br J Radiol 64:576–579

    Article  CAS  PubMed  Google Scholar 

  47. Bowers CA, Taussky P, Couldwell WT (2014) Surgical treatment of craniofacial fibrous dysplasia in adults. Neurosurg Rev 37:47–53

    Article  PubMed  Google Scholar 

  48. Smartt JM Jr, Karmacharya J, Gannon FH, Teixeira C, Mansfield K, Hunenko O, Shapiro IM, Kirschner RE (2005) Intrauterine fetal constraint induces chondrocyte apoptosis and premature ossification of the cranial base. Plast Reconstr Surg 116:1363–1369

    Article  CAS  PubMed  Google Scholar 

  49. Scheuer L (2002) Application of osteology to forensic medicine. Clin Anat 15:297–312

    Article  PubMed  Google Scholar 

  50. De Beer G (1937) The development of the vertebrates skull. Clarendon Press, Oxford

    Google Scholar 

  51. Gans C, Northcutt RG (1983) Neural crest and the origin of vertebrates: a new head. Science 220:268–273

    Article  CAS  PubMed  Google Scholar 

  52. Noden DM (1978) The control of avian cephalic neural crest cytodifferentiation: I. Skeletal and connective tissues. Dev Biol 67:296–312

    Article  CAS  PubMed  Google Scholar 

  53. Hanken J, Gross JB (2005) Evolution of cranial development and the role of neural crest: insights from amphibians. J Anat 207:437–446

    Article  PubMed Central  PubMed  Google Scholar 

  54. Kuratani S (1989) Development of the orbital region in the chondrocranium of Caretta caretta. Reconsideration of the vertebrate neurocranium configuration. Anat Anz 169:335–349

    CAS  PubMed  Google Scholar 

  55. Marugan-Lobon J, Buscalioni AD (2009) New insight on the anatomy and architecture of the avian neurocranium. Anat Rec 292:364–370

    Article  Google Scholar 

  56. Milner AC, Walsh SA (2009) Avian brain evolution: new data from Palaeogene birds (Lower Eocene) from England. Zool J Linnean Soc 155:198–219

    Article  Google Scholar 

  57. Huxley TH (1863) Evidence as to man’s place in nature. Appleton, New York

    Google Scholar 

  58. Bruner E, Averini M, Manzi G (2003) Endocranial traits. Prevalence and distribution in a recent human population. Eur J Anat 7:23–33

    Google Scholar 

  59. Lieberman DE, Pearson OM, Mowbray KM (2000) Basicranial influence on overall cranial shape. J Hum Evol 38:291–315

    Article  CAS  PubMed  Google Scholar 

  60. Strait DS (1999) The scaling of basicranial flexion and length. J Hum Evol 37:701–719

    Article  CAS  PubMed  Google Scholar 

  61. Bastir M, Rosas A, Stringer C, Cuetara JM, Kruszynski R, Weber GW, Ross CF, Ravosa MJ (2010) Effects of brain and facial size on basicranial form in human and primate evolution. J Hum Evol 58:424–431

    Article  PubMed  Google Scholar 

  62. McCarthy RC (2001) Anthropoid cranial base architecture and scaling relationships. J Hum Evol 40:41–66

    Article  CAS  PubMed  Google Scholar 

  63. Ross CF, Henneberg M, Ravosa MJ, Richard S (2004) Curvilinear, geometric and phylogenetic modeling of basicranial flexion: is it adaptive, is it constrained? J Hum Evol 46:185–213

    Article  PubMed  Google Scholar 

  64. Lieberman DE, McCarthy RC (1999) The ontogeny of cranial base angulation in humans and chimpanzees and its implications for reconstructing pharyngeal dimensions. J Hum Evol 46:185–213 36:487–517

    Google Scholar 

  65. Jeffery N, Spoor F (2004) Ossification and midline shape changes of the human fetal cranial base. Am J Phys Anthropol 123:78–90

    Article  PubMed  Google Scholar 

  66. Enlow DH (1990) Facial growth. WB Saunders, Philadelphia

    Google Scholar 

  67. Bastir M, Rosas A, O'Higgins P (2006) Craniofacial levels and the morphological maturation of the human skull. J Anat 209:637–654

    Article  PubMed Central  PubMed  Google Scholar 

  68. Moss ML, Young RW (1960) A functional approach to craniology. Am J Phys Anthropol 18:281–292

    Article  CAS  PubMed  Google Scholar 

  69. Moss ML (1959) The pathogenesis of premature cranial synostosis in man. Acta Anat 37:351–370

    Article  CAS  PubMed  Google Scholar 

  70. Strait DS (2001) Integration, phylogeny, and the hominid cranial base. Am J Phys Anthropol 114:273–297

    Article  CAS  PubMed  Google Scholar 

  71. Bruner E, Ripani M (2008) A quantitative and descriptive approach to morphological variation of the endocranial base in modern humans. Am J Phys Anthropol 137:30–40

    Article  PubMed  Google Scholar 

  72. Bastir M, Rosas A (2005) Hierarchical nature of morphological integration and modularity in the human posterior face. Am J Phys Anthropol 128:26–34

    Article  PubMed  Google Scholar 

  73. Bruner E (2007) Cranial shape and size variation in human evolution: structural and functional perspectives. Childs Nerv Syst 23:1357–1365

    Article  PubMed  Google Scholar 

  74. Masters MP (2012) Relative size of the eye and orbit: an evolutionary and craniofacial constraint model for examining the etiology and disparate incidence of juvenile-onset myopia in humans. Med Hypotheses 78:649–656

    Article  PubMed  Google Scholar 

  75. Gunz P, Harvati K (2007) The Neanderthal “chignon”: variation, integration, and homology. J Hum Evol 52:262–274

    Article  PubMed  Google Scholar 

  76. Jeffery N (2002) Differential regional brain growth and rotation of the prenatal human tentorium cerebelli. J Anat 200:135–144

    Article  PubMed Central  PubMed  Google Scholar 

  77. Bastir M, Rosas A (2009) Mosaic evolution of the basicranium in Homo and its relation to modular development. Evol Biol 36:637–654

    Article  Google Scholar 

  78. Zollikofer CPE, Ponce de León MS (2005) Virtual reconstruction: a primer in computer-assisted paleontology and biomedicine. Wiley-Liss, New York

    Google Scholar 

  79. Bookstein FL, Gunz P, Mitteroecker P, Prossinger H, Schaefer K, Seidler H (2003) Cranial integration in Homo: singular warps analysis of the midsagittal plane in ontogeny and evolution. J Hum Evol 44:167–187

    Article  PubMed  Google Scholar 

  80. Bookstein F (1991) Morphometric tools for landmark data. Cambridge Univ. Press, Cambridge

    Google Scholar 

  81. Zelditch ML, Swidersky DL, Sheets HD, Fink WL (2004) Geometric morphometrics for biologists. Elsevier, San Diego

    Google Scholar 

  82. Slice DE (2007) Geometric morphometrics. Annu Rev Anthropol 36:261–281

    Article  Google Scholar 

  83. Whitaker SR, Sprinkle PM, Chou SM (1981) Nasal glioma. Arch Otolaryngol 107:550–554

    Article  CAS  PubMed  Google Scholar 

  84. Ingraham FD, Matson DD (1943) An unusual nasopharyngeal encephalocele. N Engl J Med 228:815–820

    Article  Google Scholar 

  85. Lewinska-Smialek B, Szaro P, Ciszek B (2013) Anatomy of the adult foramen cecum. Eur J Anat 3:142–145

    Google Scholar 

  86. Suwanwela C, Suwanwela N (1972) A morphological classification of sincipital encephalomeningoceles. J Neurosurg 36:201–211

    Article  CAS  PubMed  Google Scholar 

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Di Ieva, A., Bruner, E., Haider, T. et al. Skull base embryology: a multidisciplinary review. Childs Nerv Syst 30, 991–1000 (2014). https://doi.org/10.1007/s00381-014-2411-x

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