Hypoplastic Occipital Condyle and Third OccipitalCondyle: Review of their Dysembryology
R. SHANE TUBBS,1 PATRICK RYAN LINGO,1
MARTIN M. MORTAZAVI,1 AND AARON A. COHEN-GADOL2*1Pediatric Neurosurgery, Childrens Hospital, Birmingham, Alabama
2Goodman Campbell Brain and Spine, Department of Neurological Surgery,Indiana University School of Medicine, Indianapolis, Indiana
Disruption or embryologic derailment of the normal bony architecture of thecraniovertebral junction (CVJ) may result in symptoms. As studies of theembryology and pathology of hypoplasia of the occipital condyles and thirdoccipital condyles are lacking in the literature, the present review was per-formed. Standard search engines were accessed and queried for publicationsregarding hypoplastic occipital condyles and third occipital condyles. The liter-ature supports the notion that occipital condyle hypoplasia and a third occipitalcondyle are due to malformation or persistence of the proatlas, respectively.The Pax-1 gene is most likely involved in this process. Clinically, condylar hy-poplasia may narrow the foramen magnum and lead to lateral medullary com-pression. Additionally, this maldevelopment can result in transient vertebralartery compression secondary to posterior subluxation of the occiput. Thirdoccipital condyles have been associated with cervical canal stenosis, hypopla-sia of the dens, transverse ligament laxity, and atlanto-axial instability causingacute and chronic spinal cord compression. Treatment goals are focused oncraniovertebral stability. A better understanding of the embryology and pathol-ogy related to CVJ anomalies is useful to the clinician treating patients pre-senting with these entities. Clin. Anat. 00:000000, 2013. VVC 2013 Wiley Periodicals, Inc.
Key words: anatomy; craniovertebral junction; occiput; pathology; skull base
The craniovertebral junction (CVJ) refers to thebony structures, ligaments, and articulations thatsurround the cervicomedullary junction. This funnel-shaped enclosure, which includes the caudal portionsof the occipital bone, atlas, axis, and associated liga-ments, protects the medulla oblongata and uppercervical spinal cord (Menezes et al., 2001). As partof the occipito-atlantal joint, the occipital condylescontribute largely to flexion and extension of thehead and neck. The median (third) occipital condyle,also known as condylus tertius, is a remnant of theoccipital vertebrae anterior to the foramen magnum(Rao, 2002). This structure can articulate with thedens or the atlas and limit CVJ motion (Menezes,1998; Rao, 2002) and should be distinguished frombasilar processes (Kale et al., 2009). Hypoplasticoccipital condyles and a third occipital condyle are
rare developmental abnormalities of the CVJ that canlead to instability and compression of important sur-rounding neurovascular structures (Fig. 1) (Menezes,1998; Piper and Traynelis, 1998). Understandingtheir embryology, anatomy, biomechanics, and path-ologic influence on the CVJ can help neurosurgeonsdetermine the best treatment of these complexanomalies. Herein we review the literature regardinghypoplasia of the occipital condyle and the presence
*Correspondence to: Aaron A. Cohen-Gadol, MD, MSc, GoodmanCampbell Brain and Spine, Indiana University Department of Neu-rological Surgery, 355 W. 16th Street, Suite 5100, Indianapolis,IN 46202, USA. E-mail: email@example.com
Received 20 July 2012; Revised 17 October 2012; Accepted 21October 2012
Published online in Wiley Online Library (wileyonlinelibrary.com).DOI 10.1002/ca.22205
VVC 2013 Wiley Periodicals, Inc.
Clinical Anatomy 00:000000 (2013)
of a third occipital condyle. The proposed embryol-ogy, clinical presentation, and treatment are pre-sented.
Following a search in human species and in theEnglish language using PubMed, 23 articles werefound detailing the occipital condyle and hypopla-sia or hypoplastic. A search for third occipital con-dyle resulted in six articles, and a search for con-dylus tertius resulted in five publications.
During the fourth week of gestation, paraxial mes-oderm adjacent to the neural tube and notochordsegments form 42 somites. There are 4 occipital, 8cervical, 12 thoracic, 5 lumbar, 5 sacral, and 810coccygeal pairs of somites. Each somite forms anouter dermatome, inner myotome, and medial scle-rotome. The cervical through coccygeal sclerotomeseventually fuse in the midline to form the vertebralbodies of the spinal column. The first and secondoccipital sclerotomes form the clivus, and the thirdsclerotome forms the jugular tubercles. Developmentof the fourth sclerotome, also known as the proatlas(Fig. 2), is key to understanding the anatomy andmalformations of CVJ. Key to the present review, theoccipital condyles are derived from the proatlas(Menezes and VanGilder, 1989; Menezes, 1998,2008; Menezes and Fenoy, 2009). Lastly, it shouldbe mentioned that the resegmentation of thesomites is still a matter of some debate, especiallyresegmentation of their lateral portions (Aoyama andAsamoto, 2000; Huang et al., 2000).
Unlike the first three occipital somites, the fourthoccipital somite undergoes resegmentation, a pro-cess in which the original rostral-caudal boundariesof the somites are reorganized to include cellsderived from adjacent somites (Fig. 2). The caudalhalf of the fourth occipital somite fuses with the ros-tral half of the first cervical somite to form the tran-sitional proatlas sclerotome. At the resegmentationboundary, the severance line forms, and this repre-
sents the final cellular separation of the skull andcervical spine. After primary segmentation, Hoxgenes specify the rostral-caudal identity of cellswithin the somites. Pax-1 expression influences cel-lular partitioning between tissues and thus plays acentral role in resegmentation (Pang and Thompson,2011).
The hypocentrum of the proatlas forms the ante-rior tubercle of the clivus, whereas the centrumforms the apex of the dens and the apical ligament.The neural arch divides into ventral-rostral and dor-sal-caudal segments. The ventral-rostral segmentgives rise to the occipital condyles, the anteriorU-shape of the foramen magnum, and the alar andcruciate ligaments. The dorsal-caudal segment formsthe posterior arch and lateral masses of the atlas(Menezes and VanGilder, 1989; Menezes, 1998,2008; Menezes and Fenoy, 2009). At an early stagein development, a dense band of connective tissueforms ventral to each vertebral segment called thehypochordal bow. The hypochordal bow associatedwith the proatlas normally regresses, but the oneassociated with the first cervical somite contributesto the formation of the anterior arch of the atlas(Menezes and VanGilder, 1989; Menezes, 1998,2008; Rao, 2002).
Failure of any of the above developmental proc-esses can lead to anomalies of the CVJ. Thus,descriptions of CVJ developmental malformations arebased on the underlying embryologic disturbance.Developmental errors can lead to hyperplasia, apla-sia/hypoplasia, midline fusion failure, and resegmen-tation anomalies. Hypoplasia of the lateral elementsof the proatlas, including the neural arch, can lead tooccipital condylar hypoplasia (Fig. 1) (Menezes,1998; Menezes et al., 2001; Pang and Thompson,2011). Persistence or hyperplasia of the hypochordalbow of the proatlas may contribute to the formationof an abnormal articulation between the clivus, theapical dens, and the anterior arch of the atlas knownas the third occipital condyle (Menezes and Van-Gilder, 1989; Menezes, 1998, 2008; Rao, 2002). Ofnote, the notochord has a course through the loca-tion of the third occipital condyle (David et al.,1998).
The occipital condyles are convex projectionslocated at the anterior-lateral margins of the fora-men magnum (Moore and Dalley, 2006). They artic-ulate with the superior facets of the atlas to form theatlanto-occipital joints (Menezes and VanGilder,1989; Moore and Dalley, 2006). They are condyloidsynovial joints with weak capsules that provide littlestabilization. These joints are reinforced by anteriorand posterior atlanto-occipital membranes, whichextend from the anterior and posterior arches of theatlas to the basion and opisthion, respectively(Moore and Dalley, 2006).
Blood supply to the atlanto-occipital joints is pri-marily through a vascular arcade derived from thevertebral arteries. Occipital branches of the externalcarotid artery also contribute to this blood supply.
Fig. 1. Inferior view of the skull base of an adultskull identified with a left hypoplastic occipital condyleand third occipital condyle (TOC). The TOC and hypo-plastic left condyle and normal right-sided condyle havebeen highlighted for clarity.
2 Tubbs et al.
Lymphatic drainage is via the retropharyngeal nodesthat communicate with the deep upper cervicalchain. A watershed area exists for drainage of theparanasal sinuses and nasopharynx and thus thepotential exists for retrograde inflammation of theatlanto-occipital joints from coincident sinusitis withresultant ligamentous laxity (Grisels syndrome)(Menezes and VanGilder, 1989; Menezes et al.,2001).
Within the occipitoatlantoaxial complex, theovoid occipital condyles fit into the obliquely-oriented,elliptically cupped superior facets of the atlas. Thisunique geometry primarily allows flexion-extensionand some lateral bending, but precludes meaningfulrotation. The average range of motion at the atlanto-
occipital joints is 1315 (Menezes and VanGilder,1989; Menezes et al., 2001; Moore and Dalley, 2006).In adults, the angle of the axis of the atlanto-occipitaljoints, the SchmidtFisher angle (Fig. 3), is normally12481278. In children, the occipital condyles aresmaller, and the SchmidtFisher angle is more obtuse,making the atlanto-occiptal joints of youth inherentlyless stable than those of adults (Menezes and Van-Gilder, 1989; Piper and Traynelis, 1998).
Almost no two sets of occipital condyles are alikein their dimensions, and much of the variability isaccounted for by age and sex. Based on a study of202 adult human skulls, the average size of an occi-pital condyle was 23.4 mm 3 10.6 mm 3 9.2 mm(Naderi et al., 2005). However, studies have failed
Fig. 2. Schematic drawing (after Pang and Thomp-son, 2011) of the proposed normal embryology of thecraniocervical junction. Note that the hypochordal bowof the proatlas forms the third occipital condyle (repre-sented here as the basion) and that the more posterior
aspect of the proatlas gives rise to the occipital condyle.Note the severance line through the proatlas and the re-sultant bony derivations (color coded). [Color figure canbe viewed in the online issue, which is available atwileyonlinelibrary.com.]
3Hypoplastic Occipital Condyle and TOC
to show a correlation between condyle length, headcircumference, and foramen magnum anteriorpos-terior diameter (Guidotti, 1984; Naderi et al., 2005).Several morphologic variants of the human occipitalcondyle exist. Up to 50% of condyles are oval-shaped. Other variants include kidney-like, S-like,eight-like, triangular, ring-like, two-portioned, anddeformed (Naderi et al., 2005). The occipital con-dyles may be duplicated (Tubbs et al., 2005) orgrooved (Das et al., 2006). No specific condylarabnormalities appear more commonly in males ver-sus females.
When present, the third occipital condyle is a mid-line projection of the clivus located at the anteriormargin of the foramen magnum (Smoker, 1994;Menezes, 1998; v Ludinghausen et al., 2002; Rao,2002). It has a narrow base and broader inferior sur-face that may possess an articular facet for the apexof the dens (Rao, 2002). More rarely, it may alsoarticulate with the anterior arch of the atlas(Menezes, 1998; Rao, 2002). Third occipital condyleshave been measured up to 6.5 mm in length and 6mm in transverse diameter (Rao, 2002).
Occipital condylar hypoplasia results in flatteningof the condyles and elevation of the atlas and axisrelative to the skull base. This can be confirmedradiographically by measurement of the SchmidtFisher angle, which will be greater than 1258 in thepresence of occipital condylar hypoplasia. Thesedefects can be unilateral or bilateral and are oftenassociated with the paramedian type of basilar inva-gination (Menezes and VanGilder, 1989; Piper andTraynelis, 1998). This is because they share a com-mon embryological defect, hypoplasia of the parts offourth occipital somite forming the lateral aspects ofthe foramen magnum (Menezes, 1998; Piper andTraynelis, 1998; Menezes et al., 2001; Pang andThompson, 2011). When the defect is unilateral orasymmetric, a compensatory scoliotic change of thecervical spine may occur. The foramen magnumitself is often narrowed in the presence of condylarhypoplasia and may cause lateral medullary com-pression. Condylar hypoplasia restricts movement ofthe atlanto-occiptal joint and can lead to transientvertebral artery compression secondary to posteriorsubluxation of the occiput (Menezes and VanGilder,1989). Hypoplastic condyles can occur in isolation or
as part of Morquio disease, Conradi syndrome, andspondyloepiphyseal dysplasia (Piper and Traynelis,1998; Menezes and Vogel, 2008).
Because of its potential articulation with the densor the anterior arch of the atlas, a third occipital con-dyle may limit flexion-extension of the atlanto-occi-pital joints (Rao, 2002). Third occipital condyleshave been associated with cervical canal stenosis,hypoplasia of the dens, transverse ligament laxity,and atlanto-axial instability causing acute andchronic cord compression (Kotil and Kalayci, 2005;Figueiredo et al., 2008). All developmentalabnormalities of the CVJ, including occipital condylarhypoplasia and a third occipital condyle, may beasymptomatic and discovered incidentally at autopsy,during cadaveric dissection, or through radiographicevaluation (Menezes and VanGilder, 1989; Piperand Traynelis, 1998; Menezes et al., 2001; v Luding-hausen et al., 2002; Rao, 2002).
The constellation of symptoms that can presentfrom CVJ instability secondary to occipital condylarhypoplasia or an anomalous third occipital condylemay result from compression of the lower brainstem,cervical spine, cranial nerves, or blood supply. Themost common symptom is suboccipital neck painradiating to the cranial vertex. The most commonneurologic sign is myelopathy associated withmonoparesis, hemiparesis, paraparesis, or tetrapare-sis (Menezes and VanGilder, 1989; Menezes et al.,2001). Sensory abnormalities are usually related tocompression of the dorsal columns (Menezes andVanGilder, 1989). Brain stem and cranial nerve dys-function can present as nystagmus, opthalmoplegia,dysphagia, respiratory difficulty, and sleep apnea.The most common cranial nerve affected with suchmalformations is the vestibulocochlear nerve, result-ing in hearing loss. Transient disruption of the verte-bral and anterior spinal arteries from instability atthe CVJ can lead to focal neurologic deficit or vascu-lar symptoms such as confusion, vertigo, visual fieldloss,...