Surgical Anatomy and Biomechanics of the Craniovertebral Junction

Overview

The anatomic relationship at the craniovertebral junction (CVJ) is quite complex. The foramen magnum, the atlas, and the axis together comprise the CVJ and provide the anatomic anchor that connects the cranium to the cervical spine below. The special bony configuration and articulation in this transitional zone are unique and have more built-in flexibility than any other region in the spine. The stability and complex movement of the CVJ region is dependent on highly intricate arrangements of ligamentous, membranous, and muscular structures. This chapter covers the developmental embryology of the CVJ, its anatomy, and the biomechanics unique to this region.

Embryology of the Craniovertebral Junction

Normal Developmental Embryology of the Craniovertebral Junction

The CVJ is a unique entity distinct in its form, function, and development from the remainder of the vertebral skeletal system. It comprises the occipital somites and the first three cervical somites ( Fig. 1-1 ): the occipital somites are the first four somites; the first three cervical somites are numbered five through seven. Controversy is ongoing regarding the proper number of occipital somites in vertebrates, ranging from four to five according to various authors; for the purposes of our discussion, we will concede that the first four somites are included in this group. The first three occipital somites give rise to an axial perichordal sclerotome and a lateral sclerotome. The axial perichordal sclerotomes at these levels, however, do not undergo resegmentation and therefore never subdivide into loose cranial and dense caudal zones. Because of the absence of a dense zone, the intervertebral boundary zone (IBZ) fails to form, and they all eventually fuse into a single unit, which chondrifies to become the rostral basiocciput. The lateral sclerotomes of these occipital somites, like their vertebral counterparts, do in fact form dense and loose zones; the loose zones of the second and third sclerotomes ultimately develop into the upper and lower hypoglossal nerve roots and the corresponding arteries, and the dense zones form the bony hypoglossal canal.

The fourth occipital somite differs from the first three in that it does show resegmentation. The caudal dense zone is incorporated into the cranial loose half of the first cervical somite to form the transitional sclerotome called the proatlas. The cranial half of the axial sclerotome of the proatlas combines with the other three axial occipital sclerotomes to form the basion of the skull base, and the most caudal portion of the first cervical axial sclerotome, likely derived from the first cervical somite, forms the foundation for the apical segment of the odontoid. Late in resegmentation, a boundary zone between this apical predecessor of the odontoid and the basiocciput allows this tissue to be incorporated into the odontoid. This unique formation of a physical separation between the basiocciput and the odontoid distinguishes the transitional zone from other vertebral levels. Typically, the IBZ that forms at the caudal end of the dense zone forms intervertebral disks. But at this level, this unique physical separation allows the skull to become completely independent from the vertebral column, thus differentiating it from the development at all other somitic or sclerotomal levels. Finally, the dense zones of the lateral sclerotomes of the proatlas ultimately form the two occipital condyles (OCs) and complete the rim of the foramen magnum (FM).

The first three cervical somites also deserve their distinction from the remainder of the vertebral column. Resegmentation occurs in the typical fashion as the caudal half of somite five and the cranial half of somite six form the first cervical sclerotome; likewise, the caudal half of somite six and the cranial half of somite seven thus form the second cervical sclerotome. The formation of dense and loose zones in the axial perichordal sclerotome also progresses in the usual fashion to form the basal segment of the odontoid, from the axial sclerotome of the first cervical sclerotome and the body of the axis from the axial sclerotome of the second cervical sclerotome. At this point in development, however, the first two cervical sclerotomes do not form true intervertebral disks; the IBZ soon develops into the upper and lower dental synchondroses, which ultimately allows for the fusion of the apical to basal odontoid and the basal odontoid to the body of the axis, respectively.

The development of the vertebral column occurs in three stages: membranous, cartilaginous, and osseous. The somite formation and the sclerotome segmentation occur in the membranous stage in the third week of gestation. At the fourth week, chondrification centers appear on each side of the vertebral body, notochord, and on each half of the neural arch. As these centers form and join, they squeeze the notochord cells into the disk space, where they eventually become the nucleus pulposus. However, at the occipital bone level, the notochord cells regress and do not give rise to any structure.

At the seventh to eighth week of gestation, the ossification stage begins in the midthoracic region and progresses rostrally and caudally. This ossification process continues until early childhood.

Developmental Anomalies of the Craniovertebral Junction

The atlas has three centers of ossification ( Fig. 1-2 ). At birth, the anterior arch consists mainly of cartilage. A separate center appears at the end of the first year and progressively joins the two lateral masses between the sixth and eighth years. Occasionally, only two centers of ossification are present, one on each half and the anterior arch, formed by forward extension of the two lateral masses.

The axis has six centers of ossification ( Fig. 1-3 ). The upper and lower synchondroses separate the apical dental segment, the basal dental segment, and the body of the axis. These three components undergo chondrogenesis around 6 weeks of gestation but remain separated by the two synchondroses. The ossification of the synchondrosis occurs in three waves ( Fig. 1-4 ). The first wave appears as a single ossification center within the axial body around 4 months of gestation. The second wave gives rise to two ossification centers on each side of the basal odontoid at 6 months of gestation; at birth these two centers begin to fuse, and thus begins the bony fusion of the dental process to the body of the axis, although this may not be completed even into the fifth or sixth year of life. Finally, the third wave of ossification occurs at 3 to 5 years of age, at which the tip of the odontoid undergoes bony fusion via the ossification of the upper synchondrosis; this may not be completed until adolescence. As one could presume, abnormalities in the various developmental phases of the CVJ can result in a variety of pathologic conditions, and in fact, embryology can be helpful in identifying some pathologic findings in the CVJ.

Ossiculum terminale persistens is the term for an unfused apical dental segment, likely because of failure of the upper synchondrosis. There is little debate about this finding, and it is usually nonsyndromic. Less clear is the etiology of the more often seen os odontoideum. One theory speculates that os odontoideum is simply a nonunion of an odontoid fracture, whereas another proposes that it is in fact a developmental anomaly in which the basal odontoid fails to fuse with the body of the axis. Another abnormality of resegmentation is the extremely rare os avis, in which the apical dental segment is attached to the basiocciput and not to the main dental process. The odontoid is thus shortened but clearly fused to the axis. Os avis is often associated with neurologic deterioration caused by a posterior dislocation of C1 on C2.

Surgical Anatomy of the Craniovertebral Junction

Bony Structures of the Craniovertebral Junction

Foramen Magnum and Occipital Condyle

The FM is the outlet for the transition of the cranium to the spinal column below. The FM is located in the occipital bone and is flanked anterolaterally by the OCs ( Fig. 1-5 ). The most anterior midline point of the FM is the basion, and the most posterior point is the opisthion. Numerous morphometric anatomic studies have provided considerable understanding of the FM and surrounding areas to assist neurosurgeons with safe navigation through these complex and narrow surgical corridors.

The FM is slightly oval shaped with a sagittal diameter of 34.7 ± 2.5 mm (range, 29.5 to 43.5 mm). The average transverse diameter of the FM is 27.9 mm (range, 23 to 32 mm). The FM is found to be ovoid in 46% to 58% of specimens and is asymmetric 10% of the time. Located anterolaterally from the FM are two OCs that articulate with the first cervical vertebra and provide the transition from the cranium above to the cervical spine below.

Occipital Condyle.

The OC that articulates with the atlas is an oval bone mass located on the anterior half of the FM; it converges mesially toward the basion at 30 ± 7.5 degrees and delineates the lateral limits of the CVJ ( Fig. 1-6 ; see also Fig. 1-5 ). The OC protrudes into the FM in 57% of the skulls examined. In articulating with the trapezoidal lateral mass of the atlas below, the condylar external surface is convex downward, facing outward and sloping cephalocaudal in both sagittal and coronal views. The mean length of the OC is 23.6 ± 2.5 mm, mean width is 10.6 ± 1.4 mm, and mean height is 9.2 ± 1.4 mm. The intercondylar distance is 29.4 mm (range, 26.2 to 37.0 mm).

Although the OC is most commonly oval in shape, known as type 1, other possible shapes include kidney, S, figure-eight, triangle, ring, two-portioned, and deformed profiles. These morphometric parameters have significant clinical implications because the shape of the condyle may influence the extent of the condylectomy during surgical approaches to this region. Among the various profiles, the triangle, kidney-shaped, and deformed condylar types may require more extensive condylar resection to adequately expose the ventral lesions. In addition, the OC varies in length, and it can be classified as short (condylar length <20 mm, 8.6%), moderate (23 ± 3 mm, 77.2%), or long (>26 mm, 14.1%). In all these morphometric analyses, it is well established that no correlation exists between condylar length and head circumference or FM diameter (basion-opisthion distance).

Posterior to the condyle is the condylar fossa, a bony depression located behind the condyle that is often perforated to form the condylar canal (see Fig. 1-6 ), through which the condylar emissary vein connects the vertebral venous plexus with the sigmoid sinus. A more important canal for the surgeon to be aware of when performing the transcondylar approach is the hypoglossal canal (HC), which transmits the hypoglossal nerve anterolaterally, from intracranial to extracranial, at 45 degrees to the sagittal plane ( Fig. 1-7, A ). The average length of the HC is 12.6 mm (range, 11 to 15 mm). The intracranial orifice of the HC is situated about 10 mm (range, 4.2 to 15.8 mm) superior and posterior to the anterior tip of the OC. Most of the time, the intracranial origin of the HC is found in the middle third of the OC. The distance between the posterior margin of the OC and the intracranial HC orifice is critical because it indicates the maximum amount of condyle resectable without violating the HC. The average distance between the posterior OC and HC was found to be 12.2 mm ⁴in one study, although other studies have shown that this distance can be as short as 7.9 mm (average, 9.8 mm; range, 7.5 to 12.2 mm). This distance can be reliably measured with three-dimensional (3D) computed tomography (CT).

The jugular foramen is located lateral and slightly superior to the anterior half of the condyles. It is bordered posteriorly by the jugular process and anteriorly by the jugular fossa. The jugular tubercle (JT) is situated anterosuperior to the OC and HC at the junction of the basilar and condylar portions of the occipital bone. The mean anatomic length, width, and height of the JT were found to be 15.4, 9.6, and 7.7 mm, respectively. In a previous anatomic study, a “tall” JT (height >8.5 mm) was present in 23% of dry specimens, and a “flat” JT (height <3.5 mm) was found in 10%. The average distance from HC to JT was found to be 11.7 mm (range, 8 to 12 mm).

According to Dowd and colleagues, the surgical angle to the petroclival area via the suboccipital craniotomy is narrow and steep (88 degrees), which enables a very limited exposure of deep structures in this region. After resecting the OC up to the HC, exposure can be improved, and the surgical angle can be reduced to 47 degrees. Each millimeter of OC removal decreases the angle by 2.4 degrees. To visualize the contralateral JT, at least 17 mm of OC must be removed. Spektor and colleagues have demonstrated that resecting the OC up to the HC increases the visualization only marginally, from 21% to 28%. The main obstruction that hinders visualization of the clivus is the JT, and resection of JT dramatically increases the exposure, up to 71% in the ipsilateral, contralateral, and rostral directions. Complete OC drilling did not increase exposure significantly but provided a greater degree of surgical freedom at the expense of stability. In general, 25% condylar resection increased the lateral exposure by 3 mm and the angle of exposure by 10.7 degrees, whereas 50% condylar resection increased the exposure by 7 mm and the angle by 15.9 degrees.

The Atlas (C1)

According to Greek mythology, Zeus condemned the Titan warrior Atlas to carry the globe for losing a battle to the Olympians. Hence the first cervical vertebra, which holds the skull, bears his name and the significance associated with it.

The first vertebra, the atlas, is quite different from any other vertebra; it has a ring shape, without the corpus or spinous process. The atlas comprises two dense, cortical lateral masses connected circumferentially to a short anterior arch and a longer posterior arch ( Fig. 1-8 ). The lateral mass provides a thick cortical-cancellous bone as an anchor for C1–C2 lateral mass screw procedures. The lateral mass is trapezoid in shape, wider laterally, and narrower toward the center ( Fig. 1-9 ). The medial height of the lateral mass is 8.81 ± 1.46 mm, and the lateral height is 18.01 ± 2.33 mm. The sagittal depth (anteroposterior [AP] diameter) of the lateral mass is 19.73 ± 1.71 mm. Both arches are convex outward, with each midline defined by a thickened tubercle. The shorter anterior arch is slightly taller and thinner than the posterior arch, which is not as tall but is thicker. The anterior arch height is 15.4 ± 3.2 mm, and its thickness is 6.4 ± 1.0 mm. The longer posterior arch height is 10.0 ± 1.8 mm, and its thickness is 8.0 ± 2.1 mm. The atlas ring is slightly oval with an inner AP (sagittal) diameter of 31.7 ± 2.2 mm and a transverse diameter of 32.2 ± 2.3 mm. The vertebral artery (VA) is nested in an oblong bony sulcus (the arcuate sulcus), etching from the edge of the lateral mass and extending over the top of the posterior arch (see Figs. 1-7 and 1-8 ). The length of the groove is 14.5 mm ± 2.1, which ends about 8 to 13 mm from the median tubercle of the posterior arch. The length of the transverse course of the VA over the groove is 16.6 mm (13 to 19 mm). The diameter of the VA in this area is 3.9 mm (range, 2.3 to 5.9 mm) with left VA greater than the right in 42.9% and equal in diameter in 21.4%. It is recommended that the posterior arch of the atlas not be exposed more than 1 to 1.5 cm from the midline of the posterior arch.

The superior surface of each lateral mass is concave to allow the convex OC to fit snugly into this bowled facet surface. The inferior facet of the lateral mass is a fairly flat, round surface that angulates downward and faces mesially. On sagittal view, both the OC–C1 and C1–C2 facets slope slightly downward from front to back (see Fig. 1-7 ). On coronal view, from mesial to lateral, the trapezoid configuration of the lateral mass creates an upward sloping of the OC–C1 facets, with the occipital condylar surface facing outward and the C1 superior articular surface facing inward. To counterbalance, the C1–C2 facets slope downward, with the inferior articular surface of the C1 lateral mass facing inward (see Fig. 1-9 ).

Juxtaposed immediately behind the anterior arch is the odontoid process, protruding upward from the axis below. Passing behind the odontoid process is the thick transverse ligament, which is anchored to the small, bony tubercle on the mesial edge of each lateral mass (see Fig. 1-8 ). The transverse ligament is part of the cruciate ligament complex that stabilizes the C1–C2 complex to the occiput. Lateral to the lateral mass is the transverse process, which is prominent enough to be palpated digitally between the mandibular angle and the mastoid process (see Fig. 1-8 ). The transverse diameter of the entire atlas, from the tip of the transverse process to the tip of the other, is 78.6 ± 8.1 mm. Within the transverse process is the transverse foramen, which transmits the V2 segment of the vertebral artery.

With its dense cortical bone, the C1 lateral mass provides a secure anchor for placement of lateral mass screws. Insertion of lateral mass screws places the vertebral and carotid arteries, C2 nerve roots, and hypoglossal nerve at risk. Several studies have described the anatomy of C1 for safe placement of lateral mass screws. The mean depth of bicortical screw insertion is 19.3 ± 0.21 mm in the axial plane and 20.9 ± 0.19 mm in the sagittal plane. The mean sagittal entry angle for a lateral mass screw is upward 33.1 degrees ± 8.0 degrees on the right and 37.3 degrees ± 9.1 degrees on the left. The axial angle for the bicortical lateral mass screw is slightly less, with 20.5 degrees angulation mesially from the posterior entry point. Based on these anatomic studies, it is recommended that the ideal entry point for a lateral mass screw is at the junction of the mesial edge of the posterior arch attaching to the lateral mass. The average distance between the vertebral foramen and the screw pathway is 8.8 mm using this landmark. The safe screw angulation is 15 degrees upward and inward.

Axis (C2)

The second cervical vertebra, the axis, also called epistroeus, was named for its configuration because it works as a pivot for the atlas that allows the head to rotate. The odontoid process projects upward from the body of C2 ( Figs. 1-10 and 1-11 ). It is 1.0 to 1.5 cm long and 1 cm wide (9.8 ± 0.8 mm), and it can incline posteriorly from 0 to 30 degrees relative to the body of C2. On the ventral surface of the odontoid is an oval facet that articulates with the back side of the anterior arch of C1. The dorsal surface of the odontoid is a transverse groove, where the transverse ligament traverses from one side of the C1 ring to the other to stabilize the odontoid in its unique position. The odontoid is further stabilized by the apical ligament from its apex to the basion and the paired alar ligaments from the dorsal surface of the odontoid to the FM. The body of the axis is asymmetric and widest at the base, and it tapers to the tip of the odontoid ( Fig. 1-12 ; see also Figs. 1-10 and 1-11 ). The C2 vertebral body height is 22.13 mm (range, 17.0 to 26.0 mm) from the inferior end plate to the base of the odontoid. The vertebral body width is 19.2 ± 2.2 mm at its base and 15.9 ± 1.7 mm mid body.

The odontoid and body are flanked by a pair of oval facets that extend from the body laterally onto the large pedicles and articulate with the inferior facets of the atlas (see Figs. 1-7 and 1-10 ); this articulation slopes downward on both coronal and sagittal views. Extending posteriorly from the superior facet is the pillar pedicle and the lamina of C2. The lamina of the axis is quite thick and can be used as a viable salvage in failed C2 pedicle fixation and in cases of high-riding anomalous vertebral arteries. The C2 laminar thickness is 5.75 ± 1.21 mm with a length of 24.8 ± 1.9 mm. The spinous process–laminar angle is 48.47 ± 5.37 degrees.

The C2 pedicle is fairly solid and is large enough for screw placement (see Fig. 1-11 ). The C2 pedicle height is 8.7 mm (5.90 to 10.90 mm) not including the C2 body. The mean width of the C2 pedicle is 5.8 ± 1.2 mm with an overall pedicle transverse angle of 43.2 ± 3.9 degrees (32.8 to 53.2 degrees) for screw placement. However, the anatomic median angle of the pedicle is only 10.37 degrees (6.00 to 20.00 degrees), and the angle of declination is 28.41 degrees (20.00 to 38.00 degrees). The safe site of screw entry in the axis is the superior and mesial third of the posterior surface of the C2 pedicle. The vertebral artery foramen forms a deep groove in the undersurface of the C2 superior facets and occupies the entire undersurface of the superior facet 15% of the time. As such, the safe trajectory for a C2 pedicle screw is 40 degrees mesial and 20 degrees superior.

The inferior articular facets are situated at the junction of the pedicle and lamina and face downward and forward as they articulate with the superior facets of C3 below. The transverse processes of the axis are small lateral projections that demarcate the lateral margin of the foramen transversarium, in which the vertebral artery courses upward before deviating mesially over the C1 superior sulcus.

Ligamentous and Membranous Structures of the Craniovertebral Junction

The CVJ is a unique entity, not only in its embryologic origins as discussed above, but also in its anatomic elements and their interactions with each other. But despite all of its unique features, the CVJ remains at its core a combination of bone articulated with synovial joints, muscles, ligaments, and membranes. The bony structures that make up the CVJ include the occipital bone, atlas, and axis vertebrae with their associated tubercles and characteristic shapes that allow them to move and function as a single unit.

Destructive osteoarthropathies such as rheumatoid arthritis further illustrate the unique kinematics of the CVJ. As erosion of the bony elements of the spine progresses, attendant destruction of the insertion of the transverse ligament on the atlas follows suit, resulting in ligamentous laxity at the atlantoaxial joint. This can result in atlantoaxial dislocation or an upward translation of the odontoid, a process known as basilar impression.

The ligamentous components of the CVJ can be classified into two types, extrinsic or intrinsic . The extrinsic ligaments include the fibroelastic membranes, which replace the anterior longitudinal ligament; the ligamentum flavum, which lies between the axis and atlas; and the ligamentum nuchae, which extends from the external occipital protuberance to the posterior aspects of the atlas and upper cervical spinous processes. The intrinsic ligaments are composed of the tectorial membrane (TM); the accessory atlantoaxial, cruciate, and odontoid ligaments; and the anterior atlantooccipital membranes. All of the ligaments that make up the intrinsic layer are located anterior to the dura and provide additional support to the bony structures that make up the CVJ (see Fig. 1-12 ).

The special arrangements of the occipitoatlantoaxial ligaments are remarkable, and they allow for complex motion yet provide stability to the area. The articular capsules of the lateral atlantoaxial facets surround the articular surfaces and are strengthened by atlantoaxial ligaments. The capsules are reinforced by lateral fibers that pass in a rostral direction from the TM.

The odontoid-specific ligaments, especially the alar ligaments and transverse atlantal ligament, are most important for CVJ stability. Other odontoid-specific ligaments—such as the apical, atlantodental, and atlantoalar ligaments—perform accessory roles.

The cruciform ligament, as its name suggests, is composed of both vertical and transverse bands that form a cross behind the odontoid ( Fig. 1-13 ; see also Fig. 1-12 ). The transverse band, also called the transverse atlantal ligament, is attached to a tubercle (see Fig. 1-8 ) on the medial side of the lateral masses of the atlas on either side, and it stretches across the ring of the atlas behind the odontoid. Longitudinal bands that extend in the rostrocaudal direction meet the transverse atlantal ligament in the midline to form the cross of the cruciform ligament. This vertical portion inserts on the upper surface of the clivus superiorly and to the posterior surface of the body of the axis inferiorly. The transverse atlantal ligament is the strongest, thickest ligament of the CVJ (mean height/thickness 6 to 7 mm) and as such is the predominant stabilizer of the atlas. Biomechanical studies have demonstrated that the transverse ligament is the primary defense against anterior subluxation of the atlas on the axis and that it is relatively inelastic, only allowing C1 to subluxate approximately 3 to 5 mm before rupturing. The authors of such studies also concluded that the accessory ligaments of the atlantoaxial joints serve as secondary restrictions of the atlas to anterior shift. By functioning as an anteroposterior stabilizer and holding the odontoid in its vertical position, the transverse ligament permits rotation to occur, while the alar ligaments prevent excessive rotation. Disruption of these ligamentous structures destabilizes the CVJ.