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Embryology, Classification, and Surgical Management of Bony Malformations of the Craniovertebral Junction

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Pediatric Craniovertebral Junction Diseases

Part of the book series: Advances and Technical Standards in Neurosurgery ((NEUROSURGERY,volume 40))

Abstract

The embryology of the bony craniovertebral junction (CVJ) is reviewed with the purpose of explaining the genesis and unusual configurations of the numerous congenital malformations in this region. Functionally, the bony CVJ can be divided into a central pillar consisting of the basiocciput and dental pivot; and a two-tiered ring revolving round the central pivot, comprising the foramen magnum rim and occipital condyles above, and the atlantal ring below. Embryologically, the central pillar and the surrounding rings descend from different primordia, and accordingly, developmental anomalies at the CVJ can also be segregated into those affecting the central pillar and the surrounding rings, respectively. A logical classification of this seemingly unwieldy group of malformations is thus possible based on their ontogenetic lineage, morbid anatomy, and clinical relevance. Representative examples of the main constituents of this classification scheme are given, and their surgical treatments are selectively discussed.

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References

  1. Aoyoma H, Asamoto K (1988) Determination of somite cells: independence of cell differentiation and morphogenesis. Development 104:15–28

    Google Scholar 

  2. Bagnall KM (1992) The migration and distribution of somite cells after labelling with the carbocyanine dye, DiI: the relationship of this distribution to segmentation in the vertebrate body. Anat Embryol (Berl) 185:317–324

    Article  CAS  Google Scholar 

  3. Bagnall KM, Sander EJ (1989) The binding pattern of peanut lectin associated with sclerotome migration and the formation of the vertebral axis in the chick embryo. Anat Embryol (Berl) 180:505–513

    Article  CAS  Google Scholar 

  4. Bellairs R (1980) The segmentation of somites in the chick embryo. Bolletino di Zoologia 47:245–252

    Article  Google Scholar 

  5. Burwood RJ (1970) The cranio-cervical junction: anatomy. Thesis, University of Bristol

    Google Scholar 

  6. Cattell JS, Filtzer DL (1965) Pseudosubluxation and other normal variations in the cervical spine in children. J Bone Joint Surg Am 47A:1295–1309

    Google Scholar 

  7. Cave AJE (1938) The morphological constitution of the odontoid process. J Anat 72:621

    Google Scholar 

  8. Chevrel JP (1965) Occipitalization of the atlas. Arch Orthop Trauma Surg 13:104–108

    CAS  Google Scholar 

  9. Chigira M, Kaneko K, Mashio D, Watanabe H (1994) Congenital hypoplasia of the arch of the atlas with abnormal segmentation of the cervical spine. Arch Orthop Trauma Surg 113:110–112

    Article  CAS  PubMed  Google Scholar 

  10. Christ B, Jacob HJ, Jacob M (1978) On the formation of the myotomes in avian embryos. An experimental and scanning electron microscope study. Experentia 34:514–516

    Article  Google Scholar 

  11. Christ B, Jacob HJ, Siefert R (1988) Über die Entwicklung der Zervikookzipitalen Übergangsregion. In: Hohmann D, Kügelgen B, Liebig K (eds) Neuroorthopädie, vol 4. Springer, Berlin/Heidelberg, pp 13–22

    Google Scholar 

  12. Christ B, Wilting J (1992) From somites to vertebral column. Ann Anat 174:23–32

    Article  CAS  PubMed  Google Scholar 

  13. Condie B, Capecchi MR (1993) Mice homozygous for a targeted disruption of Hox d-3 (Hox-4.1) exhibit anterior transformations of the first and second cervical vertebrae, the atlas and axis. Development 119:579–595

    CAS  PubMed  Google Scholar 

  14. 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 

  15. Crockard H, Stevens M (1995) Craniovertebral junction anomalies in inherited disorder: part of the syndrome or caused by the disorder? Eur J Pediatr 154:504–512

    Article  CAS  PubMed  Google Scholar 

  16. Dalgleish AE (1985) A study of the development of thoracic vertebrae in the mouse assisted by autoradiography. Acta Anat (Basel) 122:91–98

    Article  CAS  Google Scholar 

  17. David KM, Crockard A (2005) Congenital malformations of the base of the skull, atlas and dens. In: Benzel EC (ed) The cervical spine, 4th edn. Lippincott Williams and Wilkins, Philadelphia, pp 415–426

    Google Scholar 

  18. David KM, Thorogood P, Stevens JM, Crockard HA (1997) The one bone spine: a failure of notochord/sclerotome signaling? Clin Dysmorphol 6:303–314

    Article  CAS  PubMed  Google Scholar 

  19. David KM, Thorogood PV, Stevens JM, Crockard A (1999) The dysmorphic cervical spine in Klippel-Feil syndrome: interpretations from developmental biology. Neurosurg Focus 6(6):e1

    Article  CAS  PubMed  Google Scholar 

  20. Davis GK, Jaramillo CA, Patel NH (2001) Pax group III genes and the evolution of insect pair-rule patterning. Development 128:3445–3458

    CAS  PubMed  Google Scholar 

  21. Davis GK, Patel NH (1999) The origin and evolution of segmentation. Trends Cell Biol 9:M68–M72

    Article  CAS  PubMed  Google Scholar 

  22. Devi BI, Shenoy SN, Panigrahi MK, Chandramouli BA, Das BS, Jayakumar PN (1997) Anomaly of arch of atlas – a rare cause of symptomatic canal stenosis in children. Pediatr Neurosurg 26:214–218

    Article  CAS  PubMed  Google Scholar 

  23. Dietrich S, Gruss P (1995) Undulated phenotypes suggest a role of Pax-1 for the development of vertebral and extravertebral structures. Dev Biol 167:529–548

    Article  CAS  PubMed  Google Scholar 

  24. Dietrich S, Kessel M (1997) The vertebral column. In: Thorogood P (ed) Embryos, genes and birth defects. Wiley, Chichester, pp 281–302

    Google Scholar 

  25. Dietrich S, Schubert FR, Gruss P (1993) Altered Pax gene expression in notochord mutants of the mouse: the notochord is required for the dorsoventral patterning of the somite. Mech Dev 44:189–207

    Article  CAS  PubMed  Google Scholar 

  26. Dubrulle J, McGrew MJ, Pourquié O (2001) FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell 106:219–232

    Article  CAS  PubMed  Google Scholar 

  27. von Ebner E (1888) Urwirbel und Neugliederung der Wirbelsäule. Sitzungsber Akad Wiss Wein III 97:194–206

    Google Scholar 

  28. Forsberg H, Crozet F, Brown NA (1998) Waves of mouse Lunatic fringe expression, in four-hour cycles at two = hour intervals, precede somite boundary formation. Curr Biol 8:1027–1030

    Article  CAS  PubMed  Google Scholar 

  29. Geipel P (1955) Zur Kenntnis der Spaltbildungen des Atlas und Epistropheus Teil IV. Zbl Path 94:19

    CAS  Google Scholar 

  30. George AW (1919) A method for more accurate study of injuries to the atlas and axis. N Engl J Med Surg 181:395–398

    Google Scholar 

  31. Gholve PA, Hosalker HS, Ricchetti ET, Pollock AN, Dormans JP, Drummond DS (2007) Occipitalization of the atlas in children, morphologic classification, associations, and clinical relevance. J Bone Joint Surg (Am) 89:571–578

    Article  Google Scholar 

  32. Giacomini C (1886) Sull’ esistenza dell’ “osodontoideum: nell” uomo. Gior dr Accaddi med di Torino 49:24–28

    Google Scholar 

  33. Grabb PA, Mapstone TB, Oakes WJ (1999) Ventral brainstem compression in pediatric and young adult patients with Chiari I malformations. Neurosurgery 44:520–528

    Article  CAS  PubMed  Google Scholar 

  34. Haack H, Kessel M (1994) Homeobox genes and skeletal patterning. In: Hall BK (ed) Bone, vol 9. CRC Press, Boca Raton, pp 119–144

    Google Scholar 

  35. Hawkins RJ, Fielding JW, Thompson WJ (1976) Os odontoideum: congenital or acquired? J Bone Joint Surg (Am) 38:413–414

    Google Scholar 

  36. Hensinger RN (1986) Osseous anomalies of the craniovertebral junction. Spine 11:323–333

    Article  CAS  PubMed  Google Scholar 

  37. Hensinger RN, Fielding JW, Hawkins RJ (1978) Congenital anomalies of the odontoid process. Orthop Clin North Am 9:901–912

    CAS  PubMed  Google Scholar 

  38. Huang R, Zhi Q, Ordahl CP, Christ B (1997) The fate of the first avian somite. Anat Embryol (Berl) 195:435–449

    Article  CAS  Google Scholar 

  39. Jacob M, Christ B, Jacob HJ (1975) Über die regionale Determination des paraxialen Mesoderms junger Hühnerembryonen. Verh Anat Ges 69:263–269

    CAS  PubMed  Google Scholar 

  40. Jenkins JFA (1969) The evolution and development of the dens of the mammalian axis. Anat Rec 164:173–184

    Article  PubMed  Google Scholar 

  41. Jones FS, Georges C, Guss P, Edelman GM (1991) Activation of the cytotactin promoter by the homeobox-containing gene Evx-1. Proc Nat Acad Sci USA 89:2091

    Article  Google Scholar 

  42. Jones FS, Prediger EA, Dennis BA, DeRobertis EM, Edelman GM (1991) Cell adhesion molecules as targets for Hox genes: neural cell adhesion molecule promoter activity is modulated by cotransfection with Hox 2.5 and 2.4. Proc Nat Acad Sci USA 89:2091

    Article  Google Scholar 

  43. Kessel M (1992) Respecification of vertebral identities by retinoic acid. Development 115:487–501

    CAS  PubMed  Google Scholar 

  44. Kessel M, Gruss P (1991) Homeotic transformation of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell 67:1–20

    Article  Google Scholar 

  45. Keynes RJ, Stern CD (1988) Mechanisms of vertebrate segmentation. Development 103:413–429

    CAS  PubMed  Google Scholar 

  46. Kieny M, Mauger A, Sengel P (1972) Early regionalization of the somitic mesoderm as studied by the development of the axial skeleton of the chick embryo. Dev Biol 28:42–161

    Article  Google Scholar 

  47. Kirlew KA, Hathout GM, Reiter SD, Gold RH (1993) Os odontoideum in identical twins: perspective on etiology. Skeletal Radiol 22:525–527

    Article  CAS  PubMed  Google Scholar 

  48. Koseki H, Wallin J, Wilting J et al (1993) A role for Pax-1 as mediator of notochordal signals during the dorsoventral specification of vertebrae. Development 119:649–660

    CAS  PubMed  Google Scholar 

  49. Kotil D, Kalayci M (2005) Ventral cervicomedullary junction compression secondary to condylus occipitalis (median occipital condyle), a rare entity. J Spinal Disord Tech 18(4):382–385

    Article  PubMed  Google Scholar 

  50. Le Double AF (1903) Traité des variations des os du crane de l’homme et de leur signification au point de vue de l’Anthropologie zoologique. Vigot Frères, Paris. 1912

    Google Scholar 

  51. Logan WW, Stuard ID (1973) Absence of posterior arch of the atlas. Am J Roentgenol 118:431–434

    Article  CAS  Google Scholar 

  52. von Ludinghausen M, Schindler G, Kageyama I, Pomaroli A (2002) The third occipital condyle, a constituent part of a median occipito-atlanto-odontoid joint: a case report. Surg Radiol Anat 24:71–76

    Article  Google Scholar 

  53. Lufkin T, Mark M, Hart CP, Dollé P, LeMeur M, Chambon P (1992) Homeotic transformation of the occipital bones of the skull by ectopic expression of a homeobox gene. Nature 359:835–841

    Article  CAS  PubMed  Google Scholar 

  54. Macalister A (1893) Notes on the development and variations of the atlas. J Anat Physiol 27:519–542

    CAS  PubMed Central  PubMed  Google Scholar 

  55. Markuske H (1978) Untersuchungen zur Static und Dynamik der kindlichen Halswirbelsäule: Der Aussagewert seitlicher Röntgenaufnahmen. In: Die Wirbelsäule in Forschung und Praxis, vol 50. Hippokrates, Stuttgart

    Google Scholar 

  56. McGrew MJ, Dale JK, Fraboulet S, Pourquié O (1998) The lunatic fringe gene is a target of the molecular clock linked to somite segmentation in avian embryos. Curr Biol 8:979–982

    Article  CAS  PubMed  Google Scholar 

  57. McRae DL (1953) Bony abnormalities in the region of the foramen magnum; correlation of the anatomic and neurologic findings. Acta Radiol 40:335–354

    Article  CAS  PubMed  Google Scholar 

  58. McRae DL (1960) The significance of abnormalities of the cervical spine. Am J Roentgenol 84:3–25

    Google Scholar 

  59. McRae DL, Barnum AS (1953) Occipitalization of the atlas. Am J Roentgenol Radium Ther Nucl Med 70:23–46

    CAS  PubMed  Google Scholar 

  60. Menezes AH (1996) Congenital and acquired abnormalities of the craniovertebral junction. In: Youmans JR (ed) Neurological surgery, 4th edn. WB Saunders, Philadelphia, pp 1035–1089

    Google Scholar 

  61. Menezes AH (1998) Embryology, development, and classification of disorders of the craniovertebral junction. In: Dickman CA, Sonntag VKH, Spetzler RF (eds) Surgery of the craniovertebral junction. Thieme, New York, pp 3–12

    Google Scholar 

  62. Menezes AH, Fenoy KA (2009) Remnants of occipital vertebrae: proatlas segmentation abnormalities. Neurosurgery 64:945–953

    Article  PubMed  Google Scholar 

  63. Menezes AH, Ryken TC (1992) Craniovertebral abnormalities in Down’s syndrome. Neurosurgery 18:24–33

    CAS  Google Scholar 

  64. Morgan MK, Onofrio BM, Bender CE (1989) Familial os odontoideum. Case report. J Neurosurg 70:636–639

    Article  CAS  PubMed  Google Scholar 

  65. Müller F, O’Rahilly R (1980) The human chondrocranium at the end of the embryonic period, proper, with particular reference to the nervous system. Am J Anat 159:33–58

    Article  PubMed  Google Scholar 

  66. Müller F, O’Rahilly R (1994) Occipitocervical segmentation in staged human embryos. J Anat 185:251–258

    PubMed Central  PubMed  Google Scholar 

  67. Müller F, O’Rahilly R (2003) Segmentation in staged human embryos: the occipitocervical region revisited. J Anat 203:251–258

    Article  Google Scholar 

  68. Musil L, Goodenough D (1990) Gap junctional intercellular communication and the regulation of connexin expression and function. Curr Opin Cell Biol 2:875

    Article  CAS  PubMed  Google Scholar 

  69. Nishikawa M, Sakamoto H, Hakuba A, Nakanishi N, Inoue Y (1997) Pathogenesis of Chiari malformation: a morphometric study of the posterior cranial fossa. J Neurosurg 86:40–47

    Article  CAS  PubMed  Google Scholar 

  70. Palmeirim I, Henrique D, Ish-Horowicz D, Pourquié O (1997) Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis. Cell 91:639–648

    Article  CAS  PubMed  Google Scholar 

  71. Pendergrass EP, Schaeffer JP, Hodes PJ (1956) The head and neck in Roentgen diagnosis, 2nd edn. Charles C. Thomas, Springfield, pp 1529–1530

    Google Scholar 

  72. Pollack I, Pang D, Albright LA, Krieger D (1992) Outcome following hind brain decompression of symptomatic Chiari malformations in children previously shunted with myelomeningoceles. J Neurosurg 77:881–888

    Article  CAS  PubMed  Google Scholar 

  73. Pollack I, Pang D, Kocoshis S, Putnam P (1992) Neurogenic dysphagia resulting from Chiari malformations. Neurosurgery 30:709–719

    Article  CAS  PubMed  Google Scholar 

  74. Pourquié O (2003) The segmentation clock: converting embryonic time into spatial pattern. Science 301:328–330

    Article  PubMed  Google Scholar 

  75. Pourquié O (2003) Vertebrate somitogenesis: a novel paradigm for animal segmentation? Int J Dev Biol 47:597–603

    PubMed  Google Scholar 

  76. Prescher A (1997) The craniocervical junction in man, the osseous variations, their significance and differential diagnosis. Ann Anat 179:1–19

    Article  CAS  PubMed  Google Scholar 

  77. Prescher A (1990) The differential diagnosis of isolated ossicles in the region of the dens axis. Gegenbaurs Morphol Jahrb 136:139–154

    CAS  PubMed  Google Scholar 

  78. Prescher A, Brors D, Adam G (1996) Anatomic and radiologic appearance of several variants of the craniocervical junction. Skull Base Surg 6:83–94

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  79. Rao P (2002) Median (third) occipital condyle. Clin Anat 15:148–151

    Article  PubMed  Google Scholar 

  80. Reiter A (1944) Die Frühentwicklung der menschlichen Wirbelsäule. II. Mitteilung: Die Entwicklung der Occipitalsegmente und der Halswirbelsäule. Z Anat Entwicklungsgesch 113:66–104

    Article  Google Scholar 

  81. Remak R (1855) Untersuchungen über die Entwicklung der Wirbeltiere. Reimer, Berlin

    Google Scholar 

  82. Sawada A, Shinya M, Jiang YJ, Kawakami A, Kuroiwa A, Takeda H (2001) Fgf/MAPK signaling is a crucial positional cue in somite boundary formation. Development 128:4873–4880

    CAS  PubMed  Google Scholar 

  83. Schulze P, Buurman R (1980) Absence of the posterior arch of the atlas. Am J Roentgenol 134:178–180

    Article  CAS  Google Scholar 

  84. Sensenig EC (1957) The development of the occipital and cervical segments and their associated structures in human embryos. Contrib Embryol 36:152–161

    Google Scholar 

  85. Smith CA, Tuan RS (1994) Human PAX gene expression and development of the vertebral column. Clin Orthop 302:241–250

    PubMed  Google Scholar 

  86. Stapleton P, Weith A, Urbanek P, Kozmik Z, Busslinger M (1993) Chromosomal localization of seven PAX genes and cloning of a novel family member, PAX-9. Nat Genet 3:292

    Article  CAS  PubMed  Google Scholar 

  87. Starck D (1979) Das Skelettsystem. In: Starck D (ed) Vergleichende Anatomie der Wirbeltiere, vol 2. Springer, Berlin/Heidelberg/New York, pp 44–95

    Chapter  Google Scholar 

  88. Stern CD, Keynes RJ (1987) Interactions between somite cells; the formation and maintenance of segment boundaries in the chick embryo. Development 99:261–272

    CAS  PubMed  Google Scholar 

  89. Stover LJ, Bergan U, Nilsen G, Sjaastad O (1993) Posterior cranial fossa dimensions in the Chiari I malformation: relation to pathogenesis and clinical presentation. Neuroradiology 35:113–118

    Article  Google Scholar 

  90. von Torklus D, Gehle W (1975) Die Obere Halswirbelsäule, 2nd edn. Thieme, Stuttgart

    Google Scholar 

  91. von Torklus D, Gehle W (1972) Anomalies and malformations. In: von Torklus D, Gehle W (eds) The upper cervical spine. Thieme, Stuttgart, pp 14–53

    Google Scholar 

  92. von Torklus D, Gehle W (1969) Neue Perspektiven der Entwicklungsstörungen der oberen Halswirlbelsäule. Z Orthop 105:178

    Google Scholar 

  93. Tramontano-Guerritore G (1927) Die atlanto-occipital union. Anat Anz 64:173–184

    Google Scholar 

  94. Tubbs RS, Iskandar BJ, Bartolucci AA, Oakes WJ (2004) A critical analysis of the Chiari 1.5 malformation. J Neurosurg 101(2 Suppl):179–183

    PubMed  Google Scholar 

  95. Vega A, Quintana F, Berciano J (1990) Basichondrocranium anomalies in adult Chiari type I malformation: a morphometric study. J Neurol Sci 99:137–145

    Article  CAS  PubMed  Google Scholar 

  96. Wadia NH (1967) Myelopathy complicating congenital atlantoaxial dislocation (a study of 28 cases). Brain 90:449–472

    Article  CAS  PubMed  Google Scholar 

  97. Wallin J, Mizutani Y, Imai K et al (1993) A new Pax gene, Pax-9, maps to mouse chromosome 12. Mamm Genome 4:354–358

    Article  CAS  PubMed  Google Scholar 

  98. Wallin J, Wilting J, Koseki H, Fritsch R, Christ B, Balling R (1994) The role of Pax-1 in axial skeleton development. Development 120:1109–1121

    CAS  PubMed  Google Scholar 

  99. Wilting J, Ebensperger C, Müller TS, Koseki H, Wallin J, Christ B (1995) Pax-1 in the development of the cervico-occipital transitional zone. Anat Embryol (Berl) 192:221–227

    Article  CAS  Google Scholar 

  100. Wollin DG (1963) The os odontoideum: separate odontoid process. J Bone Joint Surg Am 45:1459–1484

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Paediatric Neurosurgery, University of California, Davis, CA, USA

    Dachling Pang MD, FRCS(C), FRCS(Eng), FACS

  2. Department of Paediatric Neurosurgery, Regional Centre of Pediatric Neurosurgery, Kaiser Foundation Hospitals of Northern California, Oakland, CA, USA

    Dachling Pang MD, FRCS(C), FRCS(Eng), FACS

  3. Department of Paediatric Neurosurgery, Kaiser Permanente Medical Center, 280 W. MacArthur Blvd., Oakland, CA, 94611, USA

    Dachling Pang MD, FRCS(C), FRCS(Eng), FACS

  4. Department of Paediatric Neurosurgery, Great Ormond Street Hospital for Children NHS Trust, Great Ormond Street, London, UK

    Dominic N. P. Thompson MBBS, BSc, FRCS(SN)

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  1. Dachling Pang MD, FRCS(C), FRCS(Eng), FACS
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  2. Dominic N. P. Thompson MBBS, BSc, FRCS(SN)
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Correspondence to Dachling Pang MD, FRCS(C), FRCS(Eng), FACS .

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  1. INI-International Neuroscience Institute, Hannover, Germany

    Concezio Di Rocco

  2. Department of Neurosurgery, Hacettepe University, Sihhiye, Ankara, Turkey

    Nejat Akalan

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Pang, D., Thompson, D.N.P. (2014). Embryology, Classification, and Surgical Management of Bony Malformations of the Craniovertebral Junction. In: Di Rocco, C., Akalan, N. (eds) Pediatric Craniovertebral Junction Diseases. Advances and Technical Standards in Neurosurgery, vol 40. Springer, Cham. https://doi.org/10.1007/978-3-319-01065-6_2

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