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The craniovertebral junction, between osseous variants and abnormalities: insight from a paleo-osteological study

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Abstract

The bony components of the craniovertebral junction (CVJ) have been investigated in 172 skeletons, dug up from several archaeological sites, to define the frequency of developmental dysmorphisms, and to acquire qualitative and quantitative data about their morphology. A review of the pertinent literature is also presented. Twenty-five individuals (14.5%) exhibited at least one dysmorphism, which ranged from a condition of simple variant to a true malformation. Four individuals presented two or more anomalies at the same time (2.3% of the whole sample, 16% of the affected individuals). The most frequently observed abnormalities were: (i) the presence of a complete bony bridge in the atlas, forming a canal surrounding the vertebral artery (arcuate foramen, supertransverse foramen, and the simultaneous occurrence of arcuate foramen and supertransverse foramen); (ii) the presence of basilar processes. Basilar processes displayed a great variety in shape and dimension. They also differed with respect to their relationship with atlas and axis. The less frequently detected anomalies were: (i) complete absence of the posterior arch of C1, (ii) fusion of C2 and C3, and (iii) irregular segmentation of C2. A broad array of structural defects has been described at the CVJ. They may occur either isolated or as part of complex multisystem syndromes. Although harmless in many cases, they can notwithstanding cause severe, even life-threatening complications. When unrecognized, they may generate trouble during surgery. Hence, accurate knowledge of CVJ arrangement, including its multifarious variations, is a critical issue for radiologists, clinicians, surgeons, and chiropractors.

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References

  • Adams SJ, Rakheja R, Bryce R, Babyn PS (2018) Incidence and economic impact of incidental findings on 18F-FDG PET/CT Imaging. Can Assoc Radiol J 69:63–70

    PubMed  Google Scholar 

  • Ankith NV, Avinash M, Srivijayanand KS, Ajoy PS, Rishi MK, Shanmuganathan R (2019) Congenital osseous anomalies of the cervical spine: occurrence, morphological characteristics, embryological basis and clinical significance: a computed tomography based study. Asian Spine J 13:535–543

    Google Scholar 

  • Badve SA, Bhojraj S, Nene A, Raut A, Ramakanthan R (2010) Occipito-atlanto-axial osteoarthritis. Spine 35:434–438

    PubMed  Google Scholar 

  • Berry AC (1975) Factors affecting the incidence of non-metrical skeletal variants. J Anat 120:519–535

    CAS  PubMed  PubMed Central  Google Scholar 

  • Berry AC, Berry RJ (1967) Epigenetic variation in the human cranium. J Anat 101:361–379

    PubMed  PubMed Central  Google Scholar 

  • Brenner DJ, Hricak H (2010) Radiology exposure from medical imaging: time to regulate? JAMA 304:208–209

    CAS  PubMed  Google Scholar 

  • Brown M, Verheyden C (2009) Posterior fossa infarction following cleft palate repair and the arcuate foramen. Plast Reconstr Surg 124:237e–239e

    PubMed  Google Scholar 

  • Brown MW, Templeton AW, Hodges FJ 3rd (1964) The incidence of acquired and congenital fusions in the cervical spine. AJR 92:1255–1259

    CAS  Google Scholar 

  • Buikstra JE, Ubelaker DH (1994) Standards for data collection from human skeletal remains, Research Series, no. 44. Arkansas Archaeological Survey, Fayetteville

  • Cave AJ (1930) On fusion of the atlas and axis vertebrae. J Anat 64:337–343

    CAS  PubMed  PubMed Central  Google Scholar 

  • Clarke RA, Catalan G, Diwan AD, Kearsley JH (1998) Heterogeneity in Klippel-Feil syndrome: a new classification. Pediatr Radiol 28:967–974

    CAS  PubMed  Google Scholar 

  • Coumans JV, Walcott BP (2011) Incidental vertebral lesions. Neurosurg Focus 31:E17

    PubMed  Google Scholar 

  • Currarino G, Rollins N, Diehl JT (1994) Congenital defects of the posterior arch of the atlas: a report of seven cases including an affected mother and son. AJNR 15:249–254

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cushing KE, Ramesh V, Gardner-Medwin D et al (2001) Tethering of the vertebral artery in the congenital arcuate foramen of the atlas vertebra: a possible cause of vertebral artery dissection in children. Dev Med Child Neurol 43:491–496

    CAS  PubMed  Google Scholar 

  • Elliott RE, Tanweer O (2014) The prevalence of the ponticulus posticus (arcuate foramen) and its importance in the Goel-Harms procedure: meta-analysis and review of the literature. World Neurosurg 82:e335-343

    PubMed  Google Scholar 

  • Fadzil F (2011) Median occipital condyle associated with atlantoaxial instability and myelopathy: a case report. Med J Malaysia 66:365–366

    CAS  PubMed  Google Scholar 

  • Feil A (1919) L’absence et la diminution des vértebras cervicales (etude clinique et pathogenique): le syndrome de la reduction numerique cervicale. Master/Doctorate Degree Thesis, Paris, University of Paris

  • Fielding JW, Hensinger RN, Hawkins RJ (1980) Os odontoideum. J Bone Joint Surg Am 62:376–383

    CAS  PubMed  Google Scholar 

  • Figueiredo N, Moraes LB, Serra A, Castelo S, Gonsales D, Medeiros RR (2008) Median (third) occipital condyle causing atlantoaxial instability and myelopathy. Arq Neuropsiquiatr 66:90–92

    PubMed  Google Scholar 

  • Freyschmidt J, Brossmann J, Wiens J, Sternberg A (2003) Borderlands of normal and early pathological findings in skeletal radiography. Thieme, New York

    Google Scholar 

  • Geipel P (1955) Zur kenntnis der spaltbildungen des atlas und epistropheus. Teil IV Zentralbl Allg Pathol 94:19–84

    CAS  Google Scholar 

  • Gunderson CH, Greenspan RH, Glaser GH, Lubs HA (1967) The Klippel-Feil syndrome: genetic and clinical reevaluation of cervical fusion. Medicine 46:491–512

    CAS  PubMed  Google Scholar 

  • Hasan M, Shukla S, Siddiqui MS, Singh D (2001) Posterolateral tunnels and ponticuli in human atlas vertebrae. J Anat 199:339–343

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hauser G, De Stefano GF (1989) Epigenetic variants of the human skull. Schweizerbart, Stuttgard, p 135

    Google Scholar 

  • Hensinger RN (1989) Congenital anomalies of the odontoid congenital agenesis, hypoplasia, and os odontoideum). In: Committee CSRSE (ed) The cervical spine, 2nd edn. JB Lippincott, Philadelphia, p 248

    Google Scholar 

  • Hong JT, Lee SW, Son BC et al (2008) Analysis of anatomical variations of bone and vascular structures around the posterior atlantal arch using three-dimensional computed tomography angiography. J Neurosurg Spine 8:230–236

    PubMed  Google Scholar 

  • Hori T (1925) Uber die Anomalien des Hinterhauptbeines. Folia Anat Japon 3:291–312

    Google Scholar 

  • Hosalkar HS, Sankar WN, Wills BP, Goebel J, Dormans JP, Drummond DS (2008) Congenital osseous anomalies of the upper cervical spine. J Bone Joint Surg Am 90:337–348

    PubMed  Google Scholar 

  • Huang MJ, Glaser JA (2003) Complete arcuate foramen precluding C1 lateral mass screw fixation in a patient with rheumatoid arthritis: case report. Iowa Orthop J 23:96–99

    PubMed  PubMed Central  Google Scholar 

  • Janssen N, Mebis W, Gielen J (2019) Unilateral paracondylar-epitransverse neo-articulation with secondary atlas-axis rotation anomaly. J Belg Soc Radiol 103:42

    PubMed  PubMed Central  Google Scholar 

  • Jones ET, Mayer P (2000) Distúrbios regionais do sistema muscoloesquelético—região cervical. In: Weinstein SL, Buckwalter JA (eds) Ortopedia de Turek—Princípios e Sua Aplicação, 5th edn. Manole Editor, Paulo, pp 345–363

    Google Scholar 

  • Jumah F, Alkhdour S, Mansour S et al (2017) Os odontoideum: a comprehensive clinical and surgical review. Cureus 9:e1551

    PubMed  PubMed Central  Google Scholar 

  • Kadadi SP, Mallikarjun M, Jayaprakash BR (2016) A study of fusion of cervical vertebrae—C2 with C3. IJBR 7:12–15

    Google Scholar 

  • Karau PB, Ogengo JA, Hassanali J, Odula P (2010) Anatomy and prevalence of atlas vertebrae bridges in a Kenyan population: an osteological study. Clin Anat 23:649–653

    PubMed  Google Scholar 

  • Kessel M, Balling R, Gruss P (1990) Variations of cervical vertebrae after expression of a Hox-1.1 transgene in mice. Cell 61:301–308

    CAS  PubMed  Google Scholar 

  • Kim KH, Park KW, Manh TH, Yeom JS, Chang BS, Lee CK (2007) Prevalence and morphologic features of ponticulus posticus in Koreans: analysis of 312 radiographs and 225 three-dimensional CT scans. Asian Spine J 1:27–31

    PubMed  PubMed Central  Google Scholar 

  • Klimo P, Blumenthal DT, Couldwell WT (2003) Congenital partial aplasia of the posterior arch of the atlas causing myelopathy: case report and review of the literature. Spine 28:224–228

    Google Scholar 

  • Kotil K, Kalayci M, Bilge T (2007) Management of cervicomedullary compression in patients with congenital and acquired osseous-ligamentous pathologies. Clin Neurosci 14:540–549

    Google Scholar 

  • Lamendin H (1992) A simple technique for age estimation in adult corpses: the two criteria dental method. J Forensic Sci 37:1373–1379

    CAS  PubMed  Google Scholar 

  • Lombardi G (1961) The occipital vertebra. Am J Roentgenol 86:260–269

    CAS  Google Scholar 

  • Lucy P (1890) Les anomalies de l’occipital expliquées par l’anatomie comparée et le développement. Imprimerie Nouvelle, Lyon, pp 50–52

    Google Scholar 

  • Mahdi E, Whitehead MT (2017) Coronal clival cleft in CHARGE syndrome. Neuroradiol J 30:574–577

    PubMed  PubMed Central  Google Scholar 

  • Meckel JF (1815) Uber einige Abnormitaten der Knochen. Dtsch Arch Physiol (halle/berlin) 1:641–644

    Google Scholar 

  • Menezes AH (2008) Craniocervical developmental anatomy and its implications. Childs Nerv Syst 4:1109–1122

    Google Scholar 

  • Menezes AH, Fenoy KA (2009) Remnants of occipital vertebrae: proatlas segmentation abnormalities. Neurosurgery 64:945–954

    PubMed  Google Scholar 

  • Menezes AH, VanGilder JC (1989) Anomalies of the craniovertebraljunction. In: Youmans JR (ed) Neurological surgery, 3rd edn. WB Saunders, Philadelphia, pp 1359–1420

    Google Scholar 

  • Mitchell J (1998a) The incidence and dimensions of the retroarticular canal of the atlas vertebra. Acta Anat 163:113–120

    CAS  PubMed  Google Scholar 

  • Mitchell J (1998b) The incidence of the lateral bridge of the atlas vertebra. J Anat 193:283–285

    PubMed  PubMed Central  Google Scholar 

  • Mold JW, Stein HFC (1986) The cascade effect in the clinical care of patients. N Engl J Med 314:512–514

    CAS  PubMed  Google Scholar 

  • Montrisaet R, Petcharunpaisan S (2020) Proatlas anomalies in craniofacial malformations: 5-year experience in King Chulalongkorn Memorial Hospital. Childs Nerv Syst 36:2829–2834

    PubMed  Google Scholar 

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

    Google Scholar 

  • Murjani B, Bhosale R, Ramaswami E, Kadam S, Ramchandani A (2021) Anatomical variations of clivus: a descriptive anatomical study. Surg Radiol Anat 43:945–951

    PubMed  Google Scholar 

  • Nagy L, Ray C (2014) Spontaneously improving occipitocondylar hyperplasia: a case report. J Neurol Surg Rep 75:e141-143

    PubMed  PubMed Central  Google Scholar 

  • Ossenfort WP (1926) The atlas in whites and negroes. Am J Phys Anthropol 9:439–443

    Google Scholar 

  • Pang D, Thompson DNP (2011) Embryology and bony malformations of the craniovertebral junction. Childs Nerv Syst 27:523–564

    PubMed  Google Scholar 

  • Paraskevas G, Papaziogas B, Tsonidis C, Kapetanos G (2005) Gross morphology of the bridges over the vertebral artery groove on the atlas. Surg Radiol Anat 27:129–136

    PubMed  Google Scholar 

  • Pękala PA, Henry BM, Pękala JR et al (2017) Prevalence of foramen arcuale and its clinical significance: a meta-analysis of 55,985 subjects. J Neurosurg Spine 27:276–290

    PubMed  Google Scholar 

  • Pérez-Vallina JR, Riaño-Galán I, Cobo-Ruisánchez A, Orejas-Rodriguez-Arango G, López-Muñiz C, Fernández-Martínez JM (2002) Congenital anomaly of craniovertebral junction: atlas–dens fusion with C1 anterior arch cleft. J Spinal Disord Tech 15:84–87

    PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rao PV, Mbajiorgu EF, Levy LF (2002) Bony anomalies of the craniocervical junction. Cent Afr J Med 48:17–23

    PubMed  Google Scholar 

  • Ravikanth R, Majumdar P (2020) Embryological considerations and evaluation of congenital anomalies of craniovertebral junction: a single-center experience. Tzu Chi Med J 33:175–180

    PubMed  PubMed Central  Google Scholar 

  • Roy PP, Arun DM, Shedge SA (2018) Fusion of axis with third cervical vertebra. J Evol Med Dent Sci 7:3763–3765

    Google Scholar 

  • Scheuer L, Black S, Christie A (2000) Developmental juvenile osteology. Academic Press, San Diego

    Google Scholar 

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

    CAS  Google Scholar 

  • Sedney CL, Rosen CL (2011) Cervical abnormalities causing vertebral artery dissection in children. J Neurosurg Pediatry 7:272–275

    Google Scholar 

  • Senoglu M, Safavi-Abbasi S, Theodore N, Bambakidis NC, Crawford NR, Sonntag VK (2007) The frequency and clinical significance of congenital defects of the posterior and anterior arch of the atlas. J Neurosurg Spine 7:399–402

    PubMed  Google Scholar 

  • Shah M, Halalmeh DR, Sandio A, Tubbs RS, Moisi MD (2020) Anatomical variations that can lead to spine surgery at the wrong level: part I, cervical spine. Cureus 12:e8667

    PubMed  PubMed Central  Google Scholar 

  • Shapiro R, Robinson F (1976) Anomalies of the craniovertebral border. Am J Roentgenol 127:281–287

    CAS  Google Scholar 

  • Shoja MM, Ramdhan R, Jensen CJ et al (2018) Embryology of the craniocervical junction and posterior cranial fossa, part I: development of the upper vertebrae and skull. Clin Anat 31:466–487

    PubMed  Google Scholar 

  • Sjøvold T (1984) A report on the heritability of some cranial measurements and non-metric traits. In: Van Vark GN, Howells WW (eds) Multivariate statistical methods in physical anthropology. Springer, Dordrecht, pp 223–246

    Google Scholar 

  • Smoker WR (1994) Craniovertebral junction: normal anatomy, craniometry, and congenital anomalies. Radiographics 14:255–277

    CAS  PubMed  Google Scholar 

  • Smoker WR, Khanna G (2008) Imaging the craniocervical junction. Childs Nerv Syst 24:1123–1145

    PubMed  Google Scholar 

  • Split W, Sawrasewicz-Rybak M (2002) Character of headache in Kimmerle anomaly. Headache 42:911–916

    PubMed  Google Scholar 

  • Stubbs DM (1992) The arcuate foramen. Variability in distribution related to race and sex. Spine 17:1502–1504

    CAS  PubMed  Google Scholar 

  • Taitz C, Nathan H (1986) Some observations on the posterior and lateral bridge of the atlas. Acta Anat 127:212–217

    CAS  PubMed  Google Scholar 

  • Tayebi Meybodi K, Tajik F, Sadrhosseini SM, Nejat F, Zeinalizadeh M (2015) Bilateral occipito-condylar hyperplasia: a very rare anomaly treated with endoscopic endo-nasal approach. Childs Nerv Syst 31:1201–1205

    PubMed  Google Scholar 

  • Travan L, Sabbadini G, Saccheri P, Crivellato E (2008) Unusual case of occipital vertebra in a medieval skeleton. Anat Sci Int 83:286–290

    PubMed  Google Scholar 

  • Travan L, Saccheri P, Sabbadini G, Crivellato E (2011) Bilateral arcuate foramen associated with partial defect of the posterior arch of the atlas in a medieval skeleton: case report and review of the literature. Looking backward to go forward. Surg Radiol Anat 33:495–500

    PubMed  Google Scholar 

  • Travan L, Saccheri P, Toso F, Crivellato E (2013) Congenital axis dysmorphism in a medieval skeleton. Childs Nerv Syst 29:707–712

    PubMed  Google Scholar 

  • Travan L, Saccheri P, Gregoraci G, Mardegan C, Crivellato E (2015) Normal anatomy and anatomic variants of vascular foramens in the cervical vertebrae: a paleo-osteological study and review of the literature. Anat Sci Int 90:308–323

    PubMed  Google Scholar 

  • Trinkaus E (2018) An abundance of developmental anomalies and abnormalities in Pleistocene people. Proc Natl Acad Sci USA 115:11941–11946

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuang F, Chen J, Wang Y, Lai D-M (2011) Occipitocervical malformation with atlas duplication. J Neurol Neurosurg Psychiatry 82:1101–1102

    PubMed  Google Scholar 

  • Tubbs RS, Wellons JC III, Blount JP, Grabb PA, Oakes WJ (2003) Inclination of the odontoid process in the pediatric Chiari I malformation. J Neurosurg 98:43–49

    PubMed  Google Scholar 

  • Tubbs RS, Hansasuta A, Loukas M, Louis RG Jr, Shoja MM, Salter EG, Oakes WJ (2007) The basilar venous plexus. Clin Anat 20:755–759

    PubMed  Google Scholar 

  • Tubbs RS, Griessenauer CJ, Loukas M, Zurada A, Shoja MM, Cohen-Gadol AA (2010) The enigmatic clival canal: anatomy and clinical significance. Childs Nerv Syst 26:1207–1210

    PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Ulmer JL, Elster AD, Ginsberg LE, Williams DW 3rd (1993) Klippel-Feil syndrome: CT and MR of acquired and congenital abnormalities of cervical spine and cord. J Comput Assist Tomogr 17:215–224

    CAS  PubMed  Google Scholar 

  • von Torklus D, Gehle W (1972) The upper cervical spine. Thieme, Stuttgard

    Google Scholar 

  • Wackenheim A (1974) Roentgen diagnosis of the craniovertebral region. Springer, New York

    Google Scholar 

  • Wight S, Osborn N, Breen AC (1999) Headache. Incidence of ponticulus posterior of the atlas in migraine and cervicogenic. J Manipulative Physiol Ther 22:15–20

    CAS  PubMed  Google Scholar 

  • Wolf-Vollenbröker M, Prescher A (2021) The ligamentum condylicum posterius as a precursor structure of the processus condylicus posterior, another proatlas-manifestation of the human occipital bone. J Anat. https://doi.org/10.1111/joa.13444

    Article  PubMed  Google Scholar 

  • Wysocki J, Bubrowski M, Reymond J, Kwiatkowski J (2003) Anatomical variants of the cervical vertebrae and the first thoracic vertebra in man. Folia Morphol 62:357–363

    Google Scholar 

  • Young JP, Young PH, Ackermann MJ, Anderson PA, Riew KD (2005) The ponticulus posticus: implications for screw insertion into the first cervical lateral mass. J Bone Joint Surg Am 87:2495–2498

    PubMed  Google Scholar 

  • Zeoli T, Iwanaga J, Bui CJ, Dumont AS, Tubbs RS (2020) Duplication of the odontoid process with other congenital defects of the craniocervical junction: case report and review of the literature. Anat Cell Biol 53:522–526

    PubMed  PubMed Central  Google Scholar 

  • Zhou PL, Poorman GW, Wang C et al (2019) Klippel-Feil: a constellation of diagnoses, a contemporary presentation, and recent national trends. J Craniovertebr Junction Spine 10:133–138

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors are grateful to the Soprintendenza Archeologia, belle arti e paesaggio of Friuli Venezia Giulia for providing access to skeletal material and to Giorgia Gregoraci to for her help in conducting the statistical analysis.

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  1. Department of Medicine, Section of Human Anatomy, University of Udine, P.le Kolbe 3, 33100, Udine, Italy

    Paola Saccheri & Luciana Travan

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  1. Paola Saccheri
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Saccheri, P., Travan, L. The craniovertebral junction, between osseous variants and abnormalities: insight from a paleo-osteological study. Anat Sci Int 97, 197–212 (2022). https://doi.org/10.1007/s12565-021-00642-7

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