Cervical Myelopathy Peter G Passias
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1Introduction2

Anatomy and Embryology of the Skull Base and Cervical SpineChapter 1

CarolinaBenjamin,
DonatoPacione
 
EMBRYOLOGY
The normal development of the spine is an intricate process that involves the influence of multiple genes and proteins. One of the guiding principles in the embryology of the spine is segmentation, also known as metamerism. This is a phenomenon by which part of an organism is created by multiple consecutive anatomically similar sections.1 Two important genes implicated in the embryonic development of the spine are the Hox and Pax genes. In particular, the Hox genes control rostrocaudal specification and the Pax genes control resegmentation. These genes code for proteins that directly guide normal developmental processes (such as shh, FGF8, BMP) or activate transcription factor pathways that alter the genetic code directly.2-6
An understanding of the embryology of the developing spine allows for an appreciation of normal anatomy as well as pathologic conditions that occur when these processes go awry. This section will focus on the development of the skull base, the atlas, and the axis, which together constitute the craniovertebral junction. Given its function as the transitional zone between the cranium and the remainder of the axial skeleton, the craniovertebral junction plays an important role in the stability and functionality of the spine.
 
Mesenchymal Stage
The three separate stages involved in the formation of the cervicocranium include the mesenchymal or membranous stage, the chondrification or cartilaginous stage, and the ossification stage. The mesenchymal stage takes place during the first 6 weeks of embryonic development. Under the influence of factors secreted by Hensen's node, the notochord develops and induces the formation of the neural plate. As the neural plate involutes to form the neural tube, mesodermal cells migrate laterally and develop into 42–44 paired somites in the rostral-caudal direction. Each somite further differentiates to an outer dermatome, an inner myotome, and a medial sclerotome, which are precursors for skin, paraspinal musculature, and vertebrae, respectively. As the somitic cells proliferate, they surround the notochord and neural tube to form a continuous layer of paraxial mesoderm that can be referred to as the membranous vertebral column. The proliferation of the cells that make up each sclerotome occurs unevenly such that there is a larger concentration of cells cranially and a smaller concentration of cells caudally. When developing into the vertebral column, the more dense caudal mass of one sclerotome joins with the less dense rostral mass of the following sclerotome to form a single vertebral body. This process is termed resegmentation. The dense caudal zone and loose rostral zone are separated by a fissure of von Ebner. The loose rostral zone will line up with the fissure of von Ebner to form the intervertebral boundary zone, which contributes to the intervertebral disks (Fig. 1.1).1,3,7 The embryologic process of somite differentiation accounts for the fact that there are eight cervical somites and nerve roots but only seven resegmented sclerotomes and thus only seven cervical vertebrae. This explains why the C1 nerve root exits above the C1 neural arch and the C8 nerve root exits above the C7 neural arch, which is in fact derived from the eighth somite.1,2
The somites that serve as the embryologic precursors of the cranial base, the atlas, and the axis include the occipital somites and the first two cervical somites. The first three occipital somites do not undergo the aforementioned process of resegmentation. Instead, the first two occipital somites fuse to form the basiocciput and the third occipital somite forms the exoccipital bone, which gives rise to the jugular tubercles (Table 1.1).1,6
The fourth occipital sclerotome is unique and is termed the pro atlas. It is further subdivided into a hypocentrum, a centrum, and a neural arch, which has both a 4dorsal and a ventral component. The hypocentrum gives rise to the anterior tubercle of the clivus, and the centrum forms the apical cap of the dens and the apical ligament. The ventral neural arch forms the anterior margin of the foramen magnum, the occipital condyle, and the midline third occipital condyle. It also gives rise to the alar and cruciate ligaments. The caudal neural arch forms the lateral masses of the atlas as well as the posterior arch of the atlas (Table 1.1).1,6
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Fig. 1.1: Bones of craniovertebral junction separated by colors based on which somite and sclerotome it differentiates from (see Table 1.1).
The first cervical sclerotome is also further subdivided into a hypocentrum, a centrum, and a neural arch. In most scenarios, the hypocentrum disappears. In rare cases, it can persist and give rise to an abnormal joint between the clivus and anterior arch of the atlas. The centrum contributes to the axis body, which is joined by the apical tip that originates from the hypocentrum of the fourth occipital sclerotome to form the ondontoid process. The fusion between the tip and the body of the dens does not occur until around 8 years of life. Until that point, they are joined by a cartilaginous band called the neural central synchrondrosis. The neural arch forms the posterior and inferior portion of the arch of the atlas (Table 1.1).1,6
Similarly, the second cervical sclerotome is subdivided into a hypocentrum, centrum, and a neural arch. The hypocentrum involutes. The centrum becomes the body of the axis. The neural arch gives rise to the facets and the posterior arch of the axis (Table 1.1).1,6
This same process of somite differentiation into segmented sclerotomes that then contribute to different components of each vertebra guides the development of the rest of the spine from C3 to C7.
Table 1.1   List of first four occipital and two cervical sclerotomes and their contributions to bones of craniovertebral junction.
Sclerotome
Structure
Occipital 1
Basiocciput
Occipital 2
Basiocciput
Occipital 3
Exoccipital centers (jugular tubercles)
Occipital 4 (Proatlas)
Anterior tubercle clivus
Apical ligament
Apex of dens
Occipital condyles
Alar and cruciate ligaments
Posterior arch of atlas
Lateral masses of atlas
Cervical 1
Anterior arch atlas
Dens
Posterior inferior arch atlas
Cervical 2
Body of axis
Facets, posterior arch axis
There are eight cervical somites but only seven resegmented sclerotomes, which explains the fact that there are only seven cervical vertebrae.1
 
Chondrification and Ossification Stages
The chondrification stage occurs starting the 6th embryonic week. This is followed by the ossification stage, which occurs in chronologic waves.
The atlas usually has three primary ossification centers at birth, although sometimes it can have two (Fig. 1.2A). Ossification of the atlas initiates in utero with the lateral masses and fuses around the 7–10th year of life (Fig. 1.2B).1,6-9
The axis has six primary ossification centers at birth (Fig. 1.3A). The ossification of the axis begins in utero, occurs in three different waves, and is usually complete by the 7th year of life. The first wave of ossification takes place at 4 months of gestation and begins with the ossification of bilateral centers within the neural arches and a center within the body of the axis. The second wave of ossification takes place at 6 months of gestation as two centers on each side of the basal dens. These two centers typically fuse by birth (Fig. 1.3B).1,6-9 Rarely, these two centers fail to fuse, causing a bifid dens or dens bicornis.1,10,11 The third wave of ossification takes place postnatally at 3–5 years of life at the ossification center at the apical tip of the dens. Failure of this apical dental synchondrosis to ossify causes ossiculum terminale pesistens.1,7,10
5
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Figs. 1.2A and B: (A) Schematic representation of the three ossification centers of C1 at birth, one in the anterior arch (A) and two neurocentral ossification centers (N). In between the ossification centers, the synchondroses (S) can be visualized. (B) Axial computed tomography scan of C1 ossification centers, one in the anterior arch (A) and two neurocentral ossification centers (N). The syndrondroses are visualized as gaps. The small arrowhead points to the tip of the dens. The large arrowhead points to the space in between unfused laminae of C1.
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Figs. 1.3A and B: (A) Schematic representation of the six ossification centers of C2, including one in the body of the axis, one in the bilateral neural arches, two in the body of the dens, and one in the tip of the dens. (B) Axial computed tomography scan of C2 ossification centers. Three of the six ossification centers can be visualized here, including the two in the neural arches and the one in the tip of the dens. The two ossification centers in the base of the dens and the ossification center in the body of the axis are not visualized here. The syndrondroses are visualized as gaps (arrowheads).
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Fig. 1.4: The three parts of the occipital bone that make up the foramen magnum: the clival part anteriorly, the squamosal part posteriorly, and the condylar parts laterally.
 
ANATOMY
 
Foramen Magnum and Hypoglossal Canal
The foramen magnum is a structure whose margins are made up from the three different parts of the occipital bone. The basal or clival portion of the occipital bone is anterior to the foramen magnum, the squamosal portion is posterior to the foramen magnum, and the condylar portions are lateral on either side (Fig. 1.4). On average, the foramen magnum is 35 mm in the sagittal diameter and 28 mm in the transverse diameter.8,12 The occipital condyles are oval structures that face anteromedially and articulate with the superior facet of the atlas. The average condylar length is 21 mm, though longer variants can be > 26 mm and shorter variants can be < 20 mm (Fig. 1.5).8,13-16 On the medial aspect of each condyle, there is an alar tubercle that is attached to the alar ligament of the odontoid process. Superior to each condyle at the middle third is the hypoglossal canal, which transmits the hypoglossal nerve. The hypoglossal canal has an intracranial end and an extracranial end. The intracranial end can be found 5 mm above the junction of the posterior and middle third of the occipital condyle, and the extracranial end can be found 5 mm above the junction of the anterior and middle third of the occipital condyle. Given this orientation, the hypoglossal nerve travels anterolaterally from intracranial to extracranial (Fig. 1.5). From a surgical standpoint, the distance between the posterior margin of the occipital condyle and the intracranial end of the hypoglossal canal is important to avoid violation of the canal and injury to the hypoglossal nerve when drilling. This distance is approximately 10 mm and should be measured with computed tomography (CT) scans preoperatively for confirmation.16-18 The oval shape of the occipital condyle that faces inferolaterally allows for articulation with the convex superior articulating process of the atlas.
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Fig. 1.5: The relationship between the occipital condyles and the hypoglossal canal.
 
Atlas
The atlas is the first cervical vertebrae and is unique in its shape and anatomy. Unlike other cervical vertebrae, the atlas lacks a vertebral body and a spinous process. Instead, it is composed of a shorter anterior arch and a longer posterior arch, which come together to form a ring. Two oval-shaped lateral masses are located at the anteromedial border of the ring on either side (Figs. 1.6A and B). In the midway point of the anterior arch, there is an anterior tubercle. Similarly, in the midway point of the posterior arch there is a posterior tubercle. There are also two tubercles medial to the lateral masses where the transverse ligament of the atlas will attach (Fig. 1.7). The transverse process of the atlas extends from the lateral masses. In comparison to adjacent cervical vertebrae, the transverse process of the atlas extends further out. In between the lateral masses and the transverse process is the foramen transversarium through which the vertebral arteries (VAs) course. The VA will be discussed separately below.
Closely related to the VA at the level of the atlas is the C1 nerve root, also known as the suboccipital nerve.
7The C1 nerve root exits between the occipital bone and the atlas and divides into a dorsal and ventral ramus. The dorsal ramus travels between the posterior arch of the atlas and the VA (Fig. 1.8). It goes on to supply the muscles of the suboccipital triangle including major branches to the rectus capitis posterior major and minor, superior and inferior oblique, and the semispinalis capitis. The ventral ramus travels between the posterior arch of the atlas and the VA and then courses anteriorly in between the lateral mass and the foramen transversarium to supply the rectus capitis lateralis. The C1 nerve root penetrates the dura with the VA.
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Figs. 1.6A and B: Superior and inferior views of C1.
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Fig. 1.7: Axial noncontrast computed tomography image of C1 demonstrating prominent transverse ligament tubercle as well as other relevant anatomy.
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Fig. 1.8: Course of C1 nerve root.
 
Axis
The axis is the second cervical vertebrae and is a transition between the unique anatomy of the atlas and the characteristic anatomy of the remainder of the cervical vertebrae. The body of the axis serves as the base for the odontoid process, which is also known as the dens. On average, the dens is 1.0–1.5 cm in length and 1 cm wide.13,16,19 Anteriorly, the dens articulates with the anterior arch of the atlas. Anterolateral to the body and dens are two large, oval-shaped superior facets that articulate with the back of the anterior arch of the atlas. The two8 inferior facets are also lateral to the body and dens but are situated more posterior than the superior facets. These inferior facets will articulate with the third cervical vertebrae. Lateral to the superior facets are small transverse processes. In between the superior facets and the transverse processes is the foramen transversarium through which the VAs course. The posterior elements of the axis include the pedicle, the lamina, and the spinous process. The laminae of the axis are thicker than that of any other cervical vertebrae. They come together and fuse posteriorly, forming the spinous process (Figs. 1.9A and B).
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Figs. 1.9A and B: Anterior and posterior views of C2.
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Fig. 1.10: Course of C2 nerve root.
The C2 nerve arises between the posterior arch of the atlas and the lamina of the axis and then divides into a dorsal and ventral ramus. The ventral ramus travels between the vertebral arches and transverse processes.
The dorsal ramus sends a branch to supply the inferior oblique muscle and then further subdivides into medial and lateral branch. The medial branch of the dorsal ramus gives rise to the greater occipital nerve, which supplies the semispinalis capitis and the scalp. The lateral branch of the dorsal ramus supplies the splenius, longissimus, and the semisplenius capitis (Fig. 1.10).
 
Joints of the Craniovertebral Junction
 
Occipital-Atlantal Joint
The oval shape of the occipital condyle that faces inferolaterally allows for articulation with the convex trapezoid-shaped superior articulating process of the atlas. This atlanto-occipital joint is cushioned by an articular capsule and strengthened by anterior and posterior atlanto-occipital membranes. The attachments of the anterior atlanto-occipital membranes are the anterior edge of the foramen magnum superiorly, the superior edge of the anterior arch of the atlas inferiorly, and the articular capsule laterally (Figs. 1.11A and B). The attachments of the posterior atlanto-occipital membranes are the posterior edge of the foramen magnum superiorly and the posterior arch of the atlas inferiorly. The posterior atlanto-occipital membrane does not have any lateral attachments and courses behind the VA and first cervical root (Figs. 1.11A and B). If this membrane ossifies, it creates a partial or complete ring around the VA as will be discussed below.
9
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Figs. 1.11A and B: Anterior and posterior view of ligaments of the craniovertebral junction.
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Fig. 1.12: Ligaments between C1 and C2.
 
Atlanto-Axial Joint
The atlanto-axial joint involves four surfaces of articulation. The first articulation is the synovial joint between the anterior surface of the dens and the posterior surface of the anterior arch of the atlas. The second articulation is the synovial joint between the posterior surface of the dens and the anterior surface of the transverse ligament of the atlas. The third and the fourth articulations are the paired lateral ones between the superior facet of C2 and the inferior facet of C1.
In addition to these articular surfaces, there are also ligaments surrounding the C1/2 junction that provide stability while also maintaining range of motion. The cruciform ligament is composed of a transverse portion and a vertical portion that forms a cross behind the dens. The transverse portion, known as the transverse atlantal ligament, attaches to the tubercles that are on the medial border of the lateral masses of C1 (see Fig. 1.7). The vertical portions are known as the superior and inferior longitudinal band and attach to the clivus and to the posterior surface of the body of the axis, respectively (Fig. 1.12). On average, the transverse atlantal ligament is 6–7 mm thick. Its tensile strength and relative inelasticity prevents anterior subluxation of C1 and maintains the stability of the craniovertebral junction.20
The other ligaments that act in a synergistic fashion to the cruciate ligament are the paired alar ligaments. These ligaments have attachments on the posterior surface of the upper third of the dens, and then each alar ligament is further subdivided into two lateral bands. The occipitalalar band inserts on the occipital bone while the atlantoalar band inserts to the lateral mass of C1. In addition to the aforementioned ligaments that provide most of the stability to the craniocervical junction, there are other ligaments that also contribute (Table 1.2).
 
Subaxial Cervical Spine
The anatomy of the subaxial cervical spine is relatively consistent from C3 to C7 with slight variations and trends in the morphology. Each vertebra is comprised of a vertebral body, which is separated from the adjacent vertebral body by the intervertebral disk. The posterolateral aspect of each vertebral body consists of the uncinate process, which articulates with the superior vertebral body, 10forming the uncovertebral joint (Fig. 1.13).
Table 1.2   Accessory ligaments of the craniovertebral junction.
Name
Insertions
Function
Comment
Arnold ligament
Connects the lateral mass of the atlas to the body of the axis
Rotational stability
Also known as accessory atlanto-axial ligament; extends cephalad and has connection to occipital bone
Barkow ligament
Connects the mesial aspect of the two occipital condyles
Rotational stability
Traverses anterior to the superior aspect of the dens and anterior to the alar ligament
Lauth ligament
Attaches to the occipital condyles superior to transverse portion of cruciate ligament and posterosuperior to the alar ligament
Unknown
Also known as transverse occipital ligament
Suspensory ligament
Connects the tip of the dens to the anterior border of the foramen magnum
None, embryologic remnant
Located between the anterior atlanto-occipital membrane and the cruciate ligament
Posterior to the uncovertebral joint is the neural foramen and the exiting nerve root. Laterally the vertebral body is connected to the transverse process. The most lateral portions of the transverse process are the anterior and posterior tubercles between which lies the groove for the exiting nerve root (Fig. 1.14). Transitioning from C3 to C7, the posterior tubercle becomes more lateral and posterior such that at C7 is can resemble a true transverse process (Figs. 1.15A and B). Between the tubercles and the vertebral body there is the transverse foramen, which contains the VA. The vertebral body is connected to the posterior elements by the pedicle. Superior to the pedicle is the neural foramen and the exiting nerve root of the corresponding level. The pedicle connects posteriorly with the lateral mass complex, which consists of a superior articular facet and an inferior articular facet. From C3 to C7 there is a trend such that the height (the distance from the superior facet to the inferior facet) increases and the thickness (AP) decreases (Fig. 1.16).21 The two lateral masses are connected posteriorly by the lamina, which meet to form the spinous process. The spinous process is usually bifid at C3, C4, and C5. At C6, the spinous process is bifid in approximately 50% of patients, whereas C7 is monofid in approximately 99% of patients.22
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Fig. 1.13: Coronal computed tomography angiogram image demonstrating the uncinate process as well as the uncovertebral joint. The vertebral artery is visualized entering the transverse foramen at C6.
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Fig. 1.14: Cervical spine from a lateral view. The nerve root (yellow) is visualized traveling out of the neural foramen within the neural groove. It is located posterior to the vertebral artery (red).
 
Vertebral Artery Anatomy
The VA is composed of four segments, of which the first three are extradural. The V1 segment is the portion of the VA from the takeoff of the subclavian artery until the C6 transverse foramen. There is often asymmetry between the VAs, with the left VA being dominant in 40–60% of patients.23-25 Entrance at the C6 transverse foramen occurs 11in the majority of patients (90–94%), with a small minority entering at C5, C7, and C4.26,27 Although C7 has a transverse foramen, the VA is rarely located within it (0.2%) (Fig. 1.15B).27 The V2 segment begins at the C6 transverse foramen and then the VA travels within each foramen up to C2 (Fig. 1.17). It is located anterior to the nerve root at each interspace lateral to the uncovertebral joint. In anatomic studies, it is found at the posterior one-fourth of the intervertebral disk space (see Fig. 1.14).27 At C2 it makes a turn laterally to enter the C2 transverse foramen. The VA at C2 may be high riding as it loops under the pars interarticularis prior to entering the transverse foramen (Figs. 1.18A and B). The prevalence of a high-riding VA is reported as between 18% and 32%.28 The V3 segment begins as the VA exits the C2 transverse foramen and extends to the point where it enters the foramen magnum (Figs. 1.19A and B). After exiting the C2 transverse foramen, it courses superiorly and slightly anterior to enter the transverse foramen of C1. Upon exiting the C1 foramen, it travels posteromedially in the sulcus of the posterior arch of C1. In up to 43–50% of patients, the groove for the VA may form a partial ring of bone as a result of ossification of the oblique atlanto-occipital ligament and periosteal sheath (Fig. 1.20).17,18,28 A complete ossification resulting in an 12arcuate foramen is found in 14–26% of patients (Fig. 1.21).28 The presence of this should be noted on preoperative CT of the upper cervical spine, as this bone will need to be removed in order to access the VA.
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Figs. 1.15A and B: (A) Axial noncontrast computed tomography (CT) image of C3 demonstrating the anterior and posterior tubercles as well as surrounding relevant anatomy. (B) Noncontrast CT image of C7 demonstrating the anterior and posterior tubercles as well as surrounding relevant anatomy. Note that the vertebral artery is located anterior to the transverse foramen.
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Fig. 1.16: Sagittal noncontrast computed tomography demonstrating the lateral masses from C3 to C7. The height of the lateral mass increases and the thickness decreases from C3 to C7.
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Fig. 1.17: Anterior view of model of the cervical spine demonstrating the path of the vertebral artery (red) and its relationship to the nerve root (yellow).
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Figs. 1.18A and B: (A) Axial noncontrast computed tomography (CT) of C2 demonstrating a high-riding vertebral artery foramen on the right side (white arrow). Note that due to the high-riding vertebral artery, there is a narrow pedicle and thin pars articularis. (B) Coronal non-contrast CT of C2 demonstrating bilateral high-riding vertebral artery (black arrow).
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Figs. 1.19A and B: (A) Coronal computed tomography (CT) angiogram demonstrating the vertebral artery as it travels within the transverse foramen. It is visualized entering at C6 and then travels cranially to C2. At C2, it turns posterolaterally and then enters the C1 transverse foramen. (B) Sagittal CT angiogram demonstrating the vertebral artery traveling within the transverse foramen. It enters at C6, then travels cranially to C2. At C2, it turns posterolaterally and then enters the C1 transverse foramen.
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Fig. 1.20: Sagittal noncontrast computed tomography of C1 demonstrating a partial ossification of the oblique atlanto-occipital ligament surrounding the sulcus arteriosis.
The V3 segment ends as the VA pierces the atlantooccipital membrane at the foramen magnum. This point is located approximately 15–19 mm lateral to the midline posterior tubercle of C1.29 In order to avoid vertebral injury, surgical exposure should not extend farther than 10–15 mm from the midline of the posterior tubercle. An important variant of the V3 segment is the presence of an extradural origin of the posterior inferior cerebellar 13artery (PICA). Although rare, occurring in 5% of cases, inadvertent injury can result in significant neurologic deficit.30,31 If surgical access to or around the V3 segment is necessary, a CT angiogram or conventional angiogram should be performed to identify the possible presence of an extradural PICA origin.
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Fig. 1.21: Lateral image of model of C1. There is complete ossification of the oblique atlanto-occipital ligament surrounding the vertebral artery creating an arcuate foramen (red arrow).
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