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Far-Lateral and Extreme Lateral Approaches

Last Updated: August 20, 2020

ABSTRACT

OBJECTIVE: Managing lesions situated in the anterior aspect of the craniovertebral junction (CVJ) remains a challenging neurosurgical problem. The purposes of this study were to examine the microsurgical anatomy of the anterior extradural aspect of the CVJ and the differences in the exposure obtained by the far lateral and extreme lateral atlanto-occipital transarticular approaches. The far lateral approach, as originally described, is a lateral suboccipital approach directed behind the sternocleidomastoid muscle and the vertebral artery and just medial to the occipital and atlantal condyles and the atlanto-occipital joint. The extreme lateral approach, as originally described, is a direct lateral approach deep to the anterior part of the sternocleidomastoid muscle and behind the internal jugular vein along the front of the vertebral artery. Both approaches permit drilling of the condyles at the atlanto-occipital joint but provide a different exposure because of the differences in the direction of the approach.

METHODS: Fifteen adult cadaveric specimens were studied using a magnification of ×3 to ×40 after perfusion of the arteries and veins with colored silicone. The microsurgical anatomy of the extradural aspects of the CVJ and the two atlantooccipital transarticular approaches were examined in stepwise dissections.

RESULTS: The far lateral atlanto-occipital transarticular approach provides excellent exposure of the extradural lesions located in the ipsilateral anterior and anterolateral aspects of the extradural region of the CVJ. The extreme lateral atlanto-occipital transarticular approach provides excellent exposure, not only on the side of the exposure, but also extending across the midline to the medial aspect of the contralateral atlanto-occipital joint and the lower clivus.

CONCLUSION: The far lateral and extreme lateral variants of the atlanto-occipital transarticular approach provide an alternative to the transoral approach to the anterior extradural structures at the CVJ. Compared with the transoral approach, both approaches provide a shorter operative route, avoid the contaminated nasopharynx, reduce the incidence of cerebrospinal fluid leak, and are not limited laterally by the atlanto-occipital joint.

INTRODUCTION

Direct surgical approaches to extradural lesions of the anterior aspect of the craniovertebral junction (CVJ) remain a challenge because of their deep location, the vital neural structures in the area, and their relationship with the vertebral artery and nasopharynx. The CVJ is a common site of neoplastic, vascular, traumatic, congenital, and degenerative lesions that may be approached anteriorly, posteriorly, or laterally (6, 20) (Fig. 1, A and B). The anterior approaches, which are mainly used for extradural lesions located in the anterior aspect of the CVJ, have significant disadvantages, including a contaminated field and the frequency of cerebrospinal fluid fistulae, lateral exposure limited by the atlantooccipital joint, and the depth of the operative field (5, 12, 17). The posterior approaches are preferred for most intradural lesions, especially those located lateral or posterior to the cervicomedullary junction (22). Both the far lateral transcondylar approach and the extreme lateral transcondylar approach provide excellent surgical access to intradural lesions of the anterolateral CVJ (3, 4, 9, 13, 19, 23, 24, 27), but they may also be used to reach anterior extradural lesions (Fig. 1, C–H). The purposes of this study were to examine the microsurgical anatomy of the anterior aspect of the CVJ, focusing especially on the extradural space, and to examine the extent of the anterior extradural exposure obtained with the atlantooccipital transarticular variants of the far lateral and extreme lateral approaches.

FIGURE 1. Surgical approaches to an extradural lesion in the anterior aspect of the CVJ. A and B (enlarged view), anterior transoral approach (white arrow) and posterior, far lateral, and extreme lateral approaches (blue arrow). The atlanto-occipital transarticular approaches to anterior extradural lesions of the CVJ are shown in the remaining panels. C, E, and G, superior views of the upper surface of the atlas. D, F, and H, inferior views of the occipital bone and foramen magnum. A and B, The extradural region of the anterior aspect of the CVJ consists of the occipital bone, atlas, axis, and its related articulations and ligaments. C and D, direction of the right far lateral (red arrows) and left extreme lateral (yellow arrows) atlanto-occipital transarticular approaches. E and F, the far lateral atlantooccipital transarticular approach provides access to the anterior or anterolateral aspects of the CVJ, including the odontoid process and the ipsilateral lower clivus. The red circled area indicates the extent of the drilling of the atlantal condyle and odontoid process (E) and occipital condyle (F). G and H, the extreme lateral atlanto-occipital transarticular approach proceeds to the anterior aspect of the CVJ, including the dens, lower clivus, and medial surface of the contralateral atlanto-occipital joint from the lateral perspective. The yellow circled area indicates the extent of the drilling of the atlantal condyle and odontoid process (G) and occipital condyle (H). Ant., anterior; Cond., condyle; Cruc., cruciform; Horiz., horizontal; ICA, internal carotid artery; Lat., lateral; Lig., ligament; Occip., occipital; Post., posterior; Proc., process; PLL, posterior longitudinal ligament; Trans., transverse; VA, vertebral artery. (Images courtesy of AL Rhoton, Jr.)

MATERIALS AND METHODS

The exposure obtained with the atlanto-occipital transarticular variants of the far lateral and extreme lateral approaches and related anatomy were examined in stepwise dissections using 15 adult cadaveric specimens and a magnification of ×3 to ×40. The arteries and veins were perfused with colored silicone. The bone dissections were performed with the Midas Rex drill (Fort Worth, TX).

RESULTS

Anatomic Considerations

Osseous Relationship

The osseous structures that must be considered in planning an approach to the region of the CVJ are the occipital bone, the atlas, and the axis.

Occipital Bone. The occipital bone surrounds the foramen magnum. The foraminal opening is oval shaped and is wider posteriorly than anteriorly. The occipital bone is divided into a basal part situated in front of the foramen magnum, paired condylar parts located lateral to the foramen magnum, and a squamosal part located above and behind the foramen magnum.

The basilar part of the occipital bone, which is also referred to as the clivus, is a thick quadrangular plate of bone that extends forward and upward. It joins the sphenoid bone at the sphenoccipital synchondrosis just below the dorsum sellae. The superior surface of the clivus is concave from side to side and is separated on each side from the petrous part of the temporal bone by the petroclival fissure. On the inferior surface of the basilar part in front of the foramen magnum, a small elevation, the pharyngeal tubercle, gives an attachment to the fibrous raphe of the pharynx.

The paired condylar parts are situated at the lateral sides of the foramen magnum. The occipital condyles, which articulate with the atlas, protrude from the external surface of these parts. The condyles are located lateral to the anterior half of the foramen magnum. They are oval in shape, convex downward, face downward and laterally, and have their long axes directed forward and medially. A tubercle that gives an attachment to the alar ligament of the odontoid process is situated on the medial side of each condyle. The hypoglossal canal, which transmits the hypoglossal nerve, is situated above the condyle and may be partially or completely divided by a bony septum. The condylar fossa, a depression located on the external surface behind the condyle, is often perforated to form the posterior condylar canal, through which an emissary vein connects the vertebral venous plexus with the sigmoid sinus.

The squamous part is an internally concave plate located above and behind the foramen magnum. It contains several prominences, such as the external occipital protuberance and ridges, including nuchal lines on which the numerous muscles of the neck attach (Fig. 2).

FIGURE 2. Occipital bone (A and B) and atlantoaxial complex (C–E). A, inferior view; B, left posterior oblique view; C, posterior view; D, view provided by far lateral approach; E, view provided by extreme lateral approach. A, the occipital bone surrounds the oval-shaped foramen magnum. The occipital bone is divided into a basal (clival) part situated in front of the foramen magnum, paired condylar parts located lateral to the foramen magnum, and a squamosal part located above and behind the foramen magnum. The basilar part of the occipital bone, which is also referred to as the clivus, is a thick quadrangular plate of bone that extends forward and upward to join the sphenoid bone just below the dorsum sellae. The condylar parts of the occipital bone, on which the occipital condyles are located, are situated lateral to the anterior half of the foramen magnum on the external surface. Arrows show the direction of the far lateral (red) and extreme lateral (yellow) atlanto-occipital transarticular approaches. B, left oblique view directed through the foramen magnum from the left side to show the intracranial aspect of the right hypoglossal canal situated above the condyle. The condylar fossa is located behind the condyle and may open into the condylar canal, through which an emissary vein passes. The condyles block access to the anterior aspect of the foramen magnum. C, a laminectomy of the atlas exposes the relationships among the lateral mass, transverse process of the atlas, and odontoid process. D, far lateral approach to the dens. The posterior parts of the lateral mass of the atlas and the transverse process have been drilled away. This approach provides the shortest route to the dens but does not gain the clearest contralateral view. E, extreme lateral approach to the dens. This approach accesses the entire odontoid process and the medial surface of the contralateral atlanto-occipital joint from a lateral perspective. Ant., anterior; Art., articular; Cond., condyle; Cont., contralateral; For., foramen; Hypogl., hypoglossal; Inf., inferior; Jug., jugular; Lat., lateral; Occip., occipital; Post., posterior; Proc., process; Sup., superior; Stylomast., stylomastoid; Trans., transverse. (Images courtesy of AL Rhoton, Jr.)

Complex of the Atlas and the Axis. The atlas, the first cervical vertebra, differs from the other cervical vertebrae by being ring shaped and by lacking a vertebral body and spinous process. It consists of two thick lateral masses situated at the anterolateral parts of the ring. The lateral masses are connected in front by a short anterior arch and behind by a longer, curved posterior arch. The position of the usual vertebral body is occupied by the odontoid process of the axis. The anterior arch is convexed forward and has a median anterior tubercle. The posterior arch is convexed backward and has a median posterior tubercle and a groove on the lateral part of its upper-outer surface in which the vertebral artery courses. The upper surface of each lateral mass has an oval concave facet that faces upward and medially and articulates with the occipital condyle that faces downward and laterally. The inferior surface of each lateral mass has a circular, flat, or slightly concave facet that faces downward, medially, and slightly backward and that articulates with the superior articular facet of the axis. The medial aspect of each lateral mass has a small tubercle for the attachment of the transverse ligament of the atlas that passes behind the odontoid process. Each transverse foramen is situated between the lateral mass and the transverse process and transmits a vertebral artery. Note that the cervical spinal cord is located at the level of the posterior margin of the lateral mass.

The axis, the second cervical vertebra, more closely resembles the typical vertebrae than the atlas, but it is distinguished by the odontoid process (dens) that projects upward from the body. On the front of the dens is an articular facet that forms a joint with the facet on the back of the anterior arch of the atlas. The dens has a pointed apex that is joined by the apical ligament, has a flattened side where the alar ligaments are attached, and is grooved at the base of its posterior surface where the transverse ligament of the atlas passes. The dens and body are flanked by a pair of large oval facets that extend laterally from the body onto the adjoining parts of the pedicles and articulate with the inferior facets of the atlas. The anterior aspect of the body is hollowed out on each side of the midline in the area where the longus colli muscles attach. The lamina of the axis is thicker than those of any other cervical vertebrae, the pedicles are more stout, and the spinous process is larger (Fig. 3).

FIGURE 3. The atlas and the axis. A, superior view; B, anterior view; C, posterior view; D, oblique left posterior view; E, right lateral view. A, the atlas consists of two thick lateral masses situated anterolaterally that are connected in front by a short anterior arch and behind by a longer curved posterior arch. The medial aspect of each lateral mass has a small tubercle for the attachment of the transverse ligament of the atlas, which passes behind the odontoid process. The anterior arch is convexed forward and has a median anterior tubercle. The position of the vertebral body is occupied by the odontoid process of the axis. Note that the posterior margin of the lateral mass is located lateral to the anterior part of the spinal cord. B, the axis is distinguished from the typical vertebrae by the odontoid process (dens), which projects upward from the body. On the front of the dens is an articular facet that forms a joint with the facet on the posterior surface of the anterior arch of the atlas. The dens and body are flanked by paired large oval facets that extend laterally from the body onto the adjoining parts of the pedicles and articulate with the inferior facets of the atlas. The anterior aspect of the body is hollowed out on each side of the midline in the area where the longus colli muscles attach. C, D, and E, the posterior arch of the atlas is convexed backward and has a median posterior tubercle and a groove on the lateral part of its upper-outer surface in which the vertebral artery courses. The upper surface of each lateral mass has an oval concave facet that faces upward and medially and articulates with the occipital condyle, which faces downward and laterally. The dens has a pointed apex that is joined by the apical ligament and flattened sides where the alar ligaments are attached. The lamina of the axis is thicker than any other cervical vertebrae, and the spinous process is larger. The C2 nerve emerges between the posterior arch of the atlas and the lamina of the axis. Distal to the ganglion, the nerve divides into larger dorsal and smaller ventral rami. Ant., anterior; Art., articular; Cruc., cruciform; Dors., dorsal; Horiz., horizontal; Inf., inferior; Lat., lateral; Lig., ligament; Post., posterior; Proc., process; Sup., superior; Trans., transverse; VA, vertebral artery; Vent., ventral. (Images courtesy of AL Rhoton, Jr.)

The Atlantoaxial Joint. Articulation of the atlas and axis comprises four synovial joints: two median ones on the front and back of the dens and paired lateral ones between the opposing articular facets on the lateral masses of the atlas and axis. The median joints are situated on the front and back of the dens and have their own fibrous capsule and synovial cavity. The anterior one is situated between the anterior surface of the dens and the posterior aspect of the anterior arch of the atlas. The posterior one has an even larger synovial cavity and lies between the cartilage-covered anterior surface of the transverse ligament of the atlas and the posterior surface of the dens.

The atlas and axis are united by the cruciform ligament, the anterior and posterior longitudinal ligaments, and the articular capsules surrounding the joints between the opposing articular facets on the lateral masses. The cruciform ligament has transverse and vertical parts that form a cross behind the dens. The transverse part, called the transverse ligament, is a thick, strong band that arches across the ring of the atlas behind the dens and divides the vertebral canal into a larger posterior compartment containing the dura and the spinal cord and a smaller anterior compartment containing the odontoid process.

On the ventral surface, the atlas and axis are connected by the anterior longitudinal ligament, which is a wide band fixed above to the lower border of the anterior arch of the atlas and below to the front of the body of the axis. The posterior longitudinal ligament is attached below to the posterior surface of the body of the axis and above to the transverse part of the cruciform ligament and the clivus (Figs. 3 and 4).

FIGURE 4. Extradural region of the anterior aspect of the CVJ. A–G, posterior views; H, lateral view of stepwise dissection. A, the cerebellar tonsil is situated above the foramen magnum. The vertebral artery penetrates the dura at the level of atlanto-occipital joint and ascends through the foramen magnum in front of the dentate ligament and accessory nerves. B, the lower part of the medulla and the upper part of the cervical spinal cord have been removed to expose the anterior aspect of the CVJ. The dura is situated in front of the spinal cord. The vertebral venous plexus, which courses just beneath the dura, can be seen through the dura. C, the dura has been removed to expose the tectorial membrane, a rostral extension of the posterior longitudinal ligament. D, the tectorial membrane has been removed to expose the cruciform and alar ligaments. The horizontal portion of the cruciform ligament, called the transverse ligament of the atlas, extends laterally to attach to the medial edges of the lateral masses of the atlas, and the vertical portion ascends to attach to the anterior margin of the foramen magnum deep to the tectorial membrane. The alar ligaments pass upward and laterally and attach to the lateral edges of the occipital condyle. E, the cruciform and alar ligaments have been removed to expose the dens. The apical ligament of the dens extends upward to attach to the margin of the foramen magnum. F, the transatlantal approach. The left lateral mass of the atlas has been removed. G and H, the atlantooccipital transarticular approach. The inferior surface of the occipital condyle has been removed to show the increased access to the odontoid process provided by the far lateral approach (G) and extreme lateral approach (H). A-O, atlanto-occipital; Ant., anterior; Art., articular; Cap., capitis; CN, cranial nerve; Cond., condyle; Cruc., cruciform; Dent., dentate; Dors., dorsal; Horiz., horizontal; Int., internal; Jug., jugular; Lig., ligament; Long., longus; M., muscle; Memb., membrane; Occip., occipital; P.I.C.A., posteroinferior cerebellar artery; Post., posterior; Proc., process; Sup., superior; Trans., transverse; V., vein; VA, vertebral artery; Vent., ventral. Vert., vertical. (Images courtesy of AL Rhoton, Jr.)

The Atlanto-occipital Joint. The atlas and the occipital bone are united by the articular capsules surrounding the atlantooccipital joints and by the anterior and posterior atlantooccipital membranes. The anterior atlanto-occipital membrane is attached superiorly to the anterior edge of the foramen magnum, inferiorly to the superior edge of the anterior arch of the atlas, and laterally to the capsule of the atlanto-occipital joints. The posterior atlanto-occipital membrane is a thin sheet connected above to the posterior margin of the foramen magnum and below to the upper border of the posterior arch of the atlas. The lateral border of the membrane is free and arches behind the vertebral artery and the first cervical nerve root. The lateral edge of this membrane may be ossified in the area where it arches over the posterior aspect of the vertebral artery, thus creating a partial or complete osseous ring around the artery on the medial side of the atlanto-occipital joint (Fig. 4A).

Axis and Occipital Bone. Four fibrous bands—the tectorial membrane, the paired alar ligaments, and the apical ligament—connect the axis and the occipital bone. The tectorial membrane is a cephalic extension of the posterior longitudinal ligament that covers the dens and cruciform ligament. It is attached below to the posterior surface of the body of the axis, above to the upper surface of the occipital bone in front of the foramen magnum, and laterally to the medial sides of the atlanto-occipital joints. The alar ligaments are two strong bands that arise on each side of the upper part of the dens and extend obliquely superolateral to attach to the medial surfaces of the occipital condyles. The apical ligament of the odontoid process extends from the tip of the dens to the anterior margin of the foramen magnum and is situated between the anterior atlanto-occipital membrane and the superior prolongation of the cruciform ligament (Fig. 4, C–E).

Neural Relationships

Spinal Cord. The spinal cord is surrounded by the dural lining and is situated in a large posterior component of the vertebral canal behind the transverse ligament. The spinal cord blends indistinguishably into the medulla at a level arbitrarily set to be at the upper limit of the dorsal and ventral rootlets forming the first cervical nerve. It is easier to differentiate this level on the ventral than on the dorsal surface because the ventral rootlets of the first cervical nerve are always present, whereas the dorsal rootlets are absent in many cases. The fact that the junction of the spinal cord and medulla is situated at the rostral margin of the first cervical root means that the medulla, and not the spinal cord, occupies the foramen magnum (Figs. 3A and 4A).

Cervical Nerve Roots

Each dorsal and ventral root is composed of a series of six to eight rootlets that fan out to enter the posterolateral and anterolateral surfaces of the spinal cord, respectively. The dorsal and ventral roots cross the subarachnoid space and transverse the dura mater separately, then unite close to the intervertebral foramen to form the spinal nerves. The rootlets in the region of the foramen magnum pass almost directly lateral to reach their dural foramina. The neurons of the dorsal roots collect to form ganglia located just proximal to the union of the dorsal and ventral root; however, the first cervical dorsal root and associated ganglion may be absent. The C1, C2, and C3 nerves, distal to the ganglion, divide into dorsal and ventral rami. The dorsal rami divide into medial and lateral branches that supply the skin and muscles of the posterior region of the neck. The C1 nerve, termed the suboccipital nerve, leaves the vertebral canal between the occipital bone and atlas and has a dorsal ramus that is larger than the ventral ramus. The dorsal ramus courses between the posterior arch of the atlas and the vertebral artery. The C1 ventral ramus courses between the posterior arch of the atlas and the vertebral artery and passes forward, lateral to the lateral mass of the atlas and medial to the vertebral artery, and supplies the rectus capitis lateralis. The C2 nerve emerges between the posterior arch of the atlas and lamina of the axis where the spinal ganglion is located extradurally and medial to the inferior facet of C1 and the vertebral artery. Distal to the ganglion, the nerve divides into a larger dorsal and a smaller ventral ramus. After passing below and supplying the inferior oblique muscle, the dorsal ramus divides into a large medial branch, called the greater occipital nerve, and a small lateral branch. The C2 ventral ramus courses between the vertebral arches and transverse processes of the atlas and axis and behind the vertebral artery to leave this operative field (Figs. 3 and 4).

Arterial Relationships

Vertebral Artery (Extradural Portion). The paired vertebral arteries arise from the subclavian arteries, ascend through the transverse processes of the upper six cervical vertebrae, pass behind the lateral masses of the atlas, enter the dura mater behind the occipital condyles, ascend through the foramen magnum to the front of the medulla, and join to form the basilar artery at the pontomedullary junction.

The extradural part of the vertebral artery is divided into three segments. The origin of the first segment extends from the subclavian artery to enter the lowest transverse foramen, usually at the C6 level. The second segment ascends through the transverse foramina of the upper six cervical vertebrae in front of the cervical nerve roots. This segment deviates laterally just above the axis to reach the laterally placed transverse foramen of the atlas. The third segment, the one most intimately related to the foramen magnum, extends from the foramen in the transverse process of the atlas to the site of passage through the dura mater. The third segment passes medially behind the lateral mass of the atlas and atlantooccipital joint and is pressed into the groove on the upper surface of the lateral part of the posterior arch of the atlas, where it courses along the floor of the suboccipital triangle. It enters the vertebral canal by passing anterior to the lateral border of the atlanto-occipital membrane. The vertebral artery is surrounded by a venous plexus composed of anastomoses between the deep cervical and epidural veins. The C1 nerve root passes through the dura mater on the lower surface of the vertebral artery and between the artery and the groove on the posterior arch of the atlas. This bony groove is sometimes transformed into a bony canal that completely surrounds a short segment of the artery. The terminal extradural segment of the vertebral artery gives rise to the posterior meningeal and posterior spinal arteries, deep cervical musculature branches, and sometimes the posteroinferior cerebellar artery (Figs. 3 and 4).

Venous Relationships

Extradural Groups. Venous flow in this area empties into two systems, one drained by the internal jugular vein and another drained by the vertebral venous plexus. The internal jugular vein originates at the jugular foramen by the confluence of the sigmoid and inferior petrosal sinuses. The venous plexus surrounding the vertebral artery in the suboccipital triangle is formed by numerous small channels that empty into the internal vertebral plexuses (between the dura and the vertebrae), which issue from the vertebral canal above the posterior arch of the atlas. The posterior condylar emissary vein, which passes through the posterior condylar canal, forms a communication between the vertebral venous plexus and the sigmoid sinus. The venous plexus of the hypoglossal canal passes along the hypoglossal canal to connect the basilar venous plexus with the marginal sinus that encircles the foramen magnum (Fig. 4A).

The Far Lateral and Extreme Lateral Variants of the Atlanto-occipital Transarticular Approach

The description of the far lateral and extreme lateral approaches (Fig. 1, C–H, and Fig. 2, A and C–E) to the anterior aspect of the CVJ is divided into two anatomic stages. The first stage, the muscular dissection, consists of the skin incision, reflection of muscles (including those forming the suboccipital triangle), and examination of the relationship of the muscles to the vertebral arteries, the vertebral venous plexus, the transverse process of the atlas, and the upper cervical nerves. The second stage, the extradural dissection, examines the transposition of the vertebral artery, the extent of the atlanto-occipital articular removal, and the exposure and identification of the extradural space of the anterior aspect of the CVJ.

Far Lateral Atlanto-occipital Transarticular Approach

Muscular Stage. The procedure is performed with the patient in the sitting or modified park-bench position (3). The exposure is accomplished using a horseshoe scalp flap because it provides a better display of the muscular layers and their relationships to the neural and vascular structures than a linear incision (Fig. 5A). The incision begins in the midline, approximately 5 cm below the external occipital protuberance, and is directed upward to just above the external occipital protuberance, turns laterally just above the superior nuchal line, reaches the mastoid, and turns downward in front of the posterior border of the sternocleidomastoid muscle onto the lateral aspect of the neck to approximately 5 cm below the mastoid tip and below where the transverse process of the atlas can be palpated through the skin. The muscles are generally reflected in a single layer with the scalp to expose the muscles forming the suboccipital triangle; however, stepwise muscular dissection was performed on the cadavers to see the relationship of muscles superficial to the triangle.

FIGURE 5 (A–D). Far lateral atlanto-occipital transarticular approach: muscular (A–D) and extradural (E–J) stages. A, to gain access to the anterior aspect of the CVJ laterally, the muscular exposure is performed using a horseshoe scalp flap because it provides for easier reflection of the muscle layers inferiorly or inferolaterally, thus allowing a wider exposure of the lateral side and room for an upper cervical laminectomy. The muscles are reflected in a single layer with the scalp, because reflecting the muscles individually makes the closure more difficult and is associated with a high incidence of wound problems, such as pseudomeningocele. The incision begins in the midline approximately 5 cm below the external occipital protuberance and is directed upward to just above the external occipital protuberance, turns laterally just above the superior nuchal line, reaches the mastoid, and turns downward in front of the posterior border of the sternocleidomastoid muscle. B, the skin flap is reflected downward and medially to expose the most superficial layer of muscles formed by the sternocleidomastoid and splenius capitis muscles laterally and the trapezius and the semispinalis capitis muscles medially. C, reflecting the semispinalis capitis downward exposes the superior and inferior oblique muscles and the transverse process of the atlas, which has a prominent apex palpable through the skin between the mastoid process and mandibular angle. The suboccipital triangle is limited by three muscles (above and medially by the rectus capitis posterior major, above and laterally by the superior oblique, and below and laterally by the inferior oblique). D, the suboccipital triangle is opened by reflecting the rectus capitis posterior major inferiorly and medially, the superior oblique laterally, and the inferior oblique medially. Opening the triangle exposes the portion of the vertebral venous plexus that surrounds the vertebral artery, which passes behind the atlanto-occipital joint and crosses the upper edge of the posterior arch of the atlas. The C2 nerve emerges between the posterior arch of the atlas and the lamina of the axis. Distal to the ganglion, the nerve divides into larger dorsal and smaller ventral rami. A-O, atlanto-occipital; Ant., anterior; Art., articular; Cap., capitis; CN, cranial nerve; Cond., condyle; Dent., dentate; Dors., dorsal; For., foramen; Inf., inferior; Int., internal; Jug., jugular; Lig., ligament; Long., longitudinal, longus; M., muscle; Maj., major; Min., minor; OA, occipital artery; Obl., oblique; Occip., occipital; P.I.C.A., posteroinferior cerebellar artery; Post., posterior; Proc., process; Rec., rectus; Semispin., semispinalis; Splen., splenius; Suboccip., suboccipital; Sup., superior; Trans., transverse; V., vein; VA, vertebral artery; Vent., ventral.  (Images courtesy of AL Rhoton, Jr.)

FIGURE 5 (E–J). E, exposure and control of the vertebral artery is a most important aspect of the procedure. The artery, after ascending through the transverse process of the atlas, turns medially behind the lateral mass of the atlas and the atlanto-occipital joint and is pressed into the groove, marking its course on the upper surface of the lateral part of the posterior arch of the atlas. F, the C1 nerve courses on the lower surface of the artery between the artery and posterior arch of the atlas. The subperiosteal dissection is continued until the vertebral artery is identified within its groove on the superior aspect of the atlas. The inferior aspect of the periosteal sheath of the vertebral artery is freed from this groove using subperiosteal dissection. The posterior arch of the atlas is removed from just beyond the midline on the opposite side to the ipsilateral transverse foramen. G, transposing the vertebral artery out of the atlantal transverse foramen allows a more lateral exposure. This requires prolongation of the subperiosteal dissection inside the transverse foramen of the atlas. The transverse foramen is then unroofed by removing the posterior root. The vertebral artery is dissected free of the axis and displaced medially and caudally. H, the lateral mass of the atlas between the occipital condyle and the superior articular facet of the axis is totally removed. Resection of the ipsilateral transverse and alar ligaments exposes the odontoid process. I, the inferior surface of the occipital condyle can be removed if it is difficult to see the superior aspect of the dens. Care should be taken to avoid damaging the hypoglossal nerve as it passes above the occipital condyle. J, the contralateral occipital condyle is not exposed, but the contralateral edge of the dens can be seen and removed, with or without mild retraction of the ventral aspect of the dural sac. The dural sac can be retracted posteriorly to see the dens and ipsilateral half of the lower clivus. The area can be drilled using the far lateral approach, as shown in Figure 1, E and F. A-O, atlanto-occipital; Ant., anterior; Art., articular; Cap., capitis; CN, cranial nerve; Cond., condyle; Dent., dentate; Dors., dorsal; For., foramen; Inf., inferior; Int., internal; Jug., jugular; Lig., ligament; Long., longitudinal, longus; M., muscle; Maj., major; Min., minor; OA, occipital artery; Obl., oblique; Occip., occipital; P.I.C.A., posteroinferior cerebellar artery; Post., posterior; Proc., process; Rec., rectus; Semispin., semispinalis; Splen., splenius; Suboccip., suboccipital; Sup., superior; Trans., transverse; V., vein; VA, vertebral artery; Vent., ventral.  (Images courtesy of AL Rhoton, Jr.)

The skin flap is reflected downward and medially to expose the upper part of the superficial layer of muscles formed by the sternocleidomastoid and splenius capitis muscles laterally and the trapezius and the semispinalis capitis muscles medially (Fig. 5B). Dividing the sternocleidomastoid just below, with preservation of the fascial attachment to the occipital bone for closure, exposes the upper extension of the splenius capitis. Detaching the trapezius and splenius capitis muscles exposes the semispinalis capitis muscle, which is reflected downward to expose the superior and inferior oblique muscles and the transverse process of the atlas, which has a prominent apex palpable through the skin between the mastoid process and mandibular angle. The suboccipital triangle, which is limited by three muscles (above and medially by the rectus capitis posterior major, above and laterally by the superior oblique, and below and laterally by the inferior oblique), is exposed by reflecting the more superficial muscles downward (Fig. 5C). The suboccipital triangle is opened by reflecting the rectus capitis posterior major inferiorly and medially, the superior oblique laterally, and the inferior oblique medially. Opening the triangle exposes the portion of the vertebral venous plexus that surrounds the vertebral artery as it passes behind the atlanto-occipital joint and across the upper edge of the posterior arch of the atlas. The C2 nerve emerges between the posterior arch of the atlas and the lamina of the axis. Distal to the ganglion, the nerve divides into a larger dorsal and a smaller ventral rami (Fig. 5D).

Extradural Stage. Exposure and control of the vertebral artery is a very important aspect of the procedure. The vertebral artery, above the transverse foramen of the axis, is directed somewhat laterally as it ascends to reach the transverse foramen of the atlas, which is situated further lateral than the transverse foramen of the axis. The artery, after ascending through the transverse process of the atlas, turns medially behind the lateral mass of the atlas and the atlanto-occipital joint and is pressed into the groove, marking its course on the upper surface on the lateral part of the posterior arch of the atlas (Fig. 5E). The C1 nerve courses on the lower surface of the artery between the artery and the posterior arch of the atlas. The inferior margin of the posterior arch of the atlas is first exposed subperiosteally beginning at the midline and proceeding to the transverse process. The exposure then progresses toward the superior margin of the posterior arch. The subperiosteal dissection is continued until the vertebral artery is identified within its groove on the superior aspect of the atlas. The inferior aspect of the periosteal sheath of the vertebral artery is freed from this groove using subperiosteal dissection to minimize bleeding from the vertebral venous plexus. The posterior arch of the atlas is removed from just beyond the midline on the opposite side to the ipsilateral transverse foramen (Fig. 5F). Transposing the vertebral artery out of the atlantal transverse foramen allows a more lateral exposure. The subperiosteal dissection is extended along the posterior root of the transverse foramen, then the transverse foramen is unroofed by removing the posterior root. The vertebral artery is dissected free of the axis and displaced medially and caudally (Fig. 5G). The lateral mass of the atlas between the occipital condyle and the superior articular facet of the axis is totally removed. Resection of the ipsilateral transverse and alar ligaments exposes the odontoid process (Fig. 5H). The inferior surface of the occipital condyle can be removed if it is difficult to see the superior aspect of the dens (Fig. 5I). Care should be taken to avoid damaging the hypoglossal nerve as it passes above the occipital condyle. The contralateral occipital condyle is not exposed, but the contralateral edge of the dens can be seen and removed, with or without mild retraction of the ventral aspect of the dural sac. The anterior part of the cervical spinal cord is located medial to the posterior part of the lateral mass. Gentle retraction of the dural sac permits visualization of the dens and the ipsilateral half of the lower clivus (Fig. 5J).

Extreme Lateral Atlanto-occipital Transarticular Approach

Muscular Stage. The patient is placed in the straight lateral position. The skin incision starts approximately 6 cm below the tip of the mastoid process and follows the anterior border of the sternocleidomastoid muscle up to the level of the external acoustic meatus, where it curves posteriorly above the attachment of the muscle (Fig. 6A). The insertion of the sternocleidomastoid muscle is divided, leaving a musculofascial cuff attached to the mastoid process for closure. Care should be taken to identify the spinal accessory (XI) nerve, which runs in a fatty and lymphatic sheath that covers the deep aspect of the muscle. The average distance between the tip of the mastoid process and the accessory nerve entering the sternocleidomastoid muscle is 3.5 cm. Therefore, the upper few centimeters of the muscle can be dissected quickly, but the lower portion must be dissected carefully. Reflecting the sternocleidomastoid muscle inferolaterally exposes the plane between the internal jugular vein and the sternocleidomastoid muscle (Fig. 6, B and C). Reflecting the splenius capitis, semispinalis capitis, and longissimus capitis muscles inferomedially exposes the suboccipital triangle and the attachment of the superior and inferior oblique, the rectus capitis lateralis, and the levator scapulae muscles to the transverse process of the atlas (Fig. 6, D and E). The transverse process of the atlas can be palpated in the exposure. Dividing the insertion of and reflecting the muscles forming the suboccipital triangle exposes the vertebral artery between the transverse foramen of the axis and the point where it penetrates the dura mater. The C2 nerve root is exposed between the atlas and the axis. The ventral ramus of the C2 nerve root curves around the vertebral artery. The posterior belly of the digastric muscle is preserved to protect the facial nerve that exits the skull at the anterior margin of the muscle (Fig. 6F).

FIGURE 6 (A–F). Extreme lateral atlanto-occipital transarticular approach: muscular (A–F) and extradural (G–N) stages. A, the skin incision starts approximately 6 cm below the tip of the mastoid process and follows the anterior border of the sternocleidomastoid muscle up to the level of the external acoustic meatus, where it curves posteriorly above the attachment of the muscle. B and C, the insertion of the sternocleidomastoid muscle is divided, leaving a musculofascial cuff attached to the mastoid process for closure. Care should be taken to identify the spinal accessory (XI) nerve, which runs in a fatty and lymphatic sheath that covers the deep aspect of the muscle. The average distance between the tip of the mastoid process and the accessory nerve entering the sternocleidomastoid muscle is 3.5 cm. Therefore, the upper few centimeters of the muscle can be dissected quickly, but the lower portion must be dissected carefully. Reflecting the sternocleidomastoid inferolaterally exposes the plane between the internal jugular vein and the sternocleidomastoid muscle. D and E, reflecting the splenius capitis, semispinalis capitis, and longissimus capitis muscles inferomedially exposes the suboccipital triangle and the attachment of the superior and inferior oblique, the rectus capitis lateralis, and the levator scapulae muscles to the transverse process of the atlas. The transverse process of the atlas can be palpated in the exposure. F, reflecting the muscles forming the suboccipital triangle exposes the vertebral artery between the transverse foramen of the axis and the point where it penetrates the dura mater. The C2 nerve root is exposed between the atlas and the axis. The posterior belly of the digastric muscle is preserved to protect the facial nerve. A-O, atlanto-occipital; Ant., anterior; Art., articular; Aur., auricular; Br., branch; Cap., capitis; CN, cranial nerve; Cond., condyle; Cont., contralateral; Digast., digastric; Dors., dorsal; For., foramen; Gr., great; Inf., inferior; Int., internal; Jug., jugular; Lat., lateralis; Lev., levator; Long., longissimus or longus; M., muscle; Maj., major; N., nerve; OA, occipital artery; Obl., oblique; Occip., occipital; Post., posterior; Proc., process; Rec., rectus; Scap., scapula; Semispin., semispinalis; Splen., splenius; Sternocleidomas., sternocleidomastoid; Suboccip., suboccipital; Sup., superior; Trans., transverse; V., vein; VA, vertebral artery; Vent., ventral. (Images courtesy of AL Rhoton, Jr.)

FIGURE 6 (G–N). G, the extreme lateral atlanto-occipital transarticular approach proceeds below the tip of the mastoid process and between the internal jugular vein and the dural sac. H, attention should be directed to the preservation of the spinal accessory nerve when the sternocleidomastoid muscle is reflected inferolaterally. The deepest muscle is formed by the uppermost slip of the levator scapulae, the superior and inferior oblique muscles, and the rectus capitis lateralis, all of which attach to the transverse process of the atlas. I and J, an important aspect of this approach is the exposure and control of the vertebral artery. The artery is identified in the groove on the upper surface of the C1 arch after exposing the transverse process and lateral part of the posterior arch of the atlas. This groove marks the posterior edge of the lateral mass of the atlas. Exposing the vertebral artery subperiosteally reduces bleeding from the vertebral venous plexus, which lies inside the periosteal sheath surrounding the artery. K, removal of the posterior root of the transverse foramen permits the artery to be displaced downward and laterally away from the atlanto-occipital joint and posterior aspect of the lateral mass of the atlas. L and M, after mobilizing the vertebral artery, the lateral mass of the atlas is drilled away completely, followed by the removal of the inferior surface of the occipital condyle if necessary. N, the odontoid process has been drilled away. The extreme lateral approach has a greater advantage than the far lateral approach in visualizing the entire odontoid process, inferior surface of the lower clivus, and medial surface of the contralateral atlantooccipital joint. The area that can be drilled using the extreme lateral approach is shown in Figure 1, G and H. A-O, atlanto-occipital; Ant., anterior; Art., articular; Aur., auricular; Br., branch; Cap., capitis; CN, cranial nerve; Cond., condyle; Cont., contralateral; Digast., digastric; Dors., dorsal; For., foramen; Gr., great; Inf., inferior; Int., internal; Jug., jugular; Lat., lateralis; Lev., levator; Long., longissimus or longus; M., muscle; Maj., major; N., nerve; OA, occipital artery; Obl., oblique; Occip., occipital; Post., posterior; Proc., process; Rec., rectus; Scap., scapula; Semispin., semispinalis; Splen., splenius; Sternocleidomas., sternocleidomastoid; Suboccip., suboccipital; Sup., superior; Trans., transverse; V., vein; VA, vertebral artery; Vent., ventral. (Images courtesy of AL Rhoton, Jr.)

Extradural Stage. An important aspect of the approach is the exposure and control of the vertebral artery. The artery is identified in the groove on the upper surface of the C1 arch after exposing the transverse process and the lateral part of the posterior arch of the atlas. This groove marks the posterior edge of the lateral mass of the atlas (Fig. 6, G–J). The periosteal sheath lining the groove is elevated using subperiosteal dissection, and the transverse process is unroofed using a drill or small rongeur. Exposing the vertebral artery subperiosteally reduces bleeding from the vertebral venous plexus that lies inside the periosteal sheath surrounding the artery. Removal of the posterior root of the transverse foramen permits the artery to be displaced downward and laterally, away from the atlanto-occipital joint and lateral mass of the atlas (Fig. 6K). The lateral mass of the atlas is totally removed up to the occipital condyle and down to the superior articular facet of the axis, thus exposing the odontoid process of the axis. The occipital condyle projects downward along the lateral edges of the anterior half of the foramen magnum. The superior articular facet of the axis is positioned along the lateral side of the base of the odontoid process (Fig. 6L). Drilling can be extended to the lower surface of the occipital condyle to expose the superior aspect of the dens (Fig. 6M). Removing the odontoid process exposes the medial aspect of the contralateral atlanto-occipital joint and the inferior surface of the lower clivus (Fig. 6N). Care is taken to avoid damage to the internal jugular vein, which is located immediately anterior to the transverse process of the atlas.

DISCUSSION

Neoplastic, vascular, traumatic, congenital, and degenerative lesions involving the extradural space of the anterior aspect of the CVJ are not rare. Some controversy exists regarding the appropriate approach to lesions in this region. The anterior approaches, including the transoral approach and its variations, are used predominantly for extradural lesions located in the anterior aspect of the CVJ (5, 12, 14, 15, 17). Posterior, posterolateral, and lateral approaches have frequently been used to access intradural lesions located along the anterior or anterolateral aspect of the CVJ (4, 11, 13, 22–24). However, detailed microsurgical anatomic studies of the extradural space of the anterior aspect of the CVJ are rare (1, 2, 25).

A wide variety of posterolateral surgical approaches for the anterior or anterolateral CVJ have been described (3, 4, 9, 11, 13, 16, 18, 21–24, 27). These approaches are categorized into two major groups: far lateral and transcondylar approaches. Without drilling of the occipital condyle, the basic far lateral approach, which is also described as a posterolateral approach, may be all that is required to reach some lesions located along the anterolateral margin of the foramen magnum. However, it also provides a route through which the transcondylar, supracondylar, and paracondylar approaches and several modifications of the far lateral approach can be completed (19, 27). The atlanto-occipital transarticular approaches can be divided into two types: far lateral (posterolateral) and extreme lateral, depending on the extent of the anterior extradural exposure at the CVJ. These two transarticular routes are similar but completely distinct from each other from several points of view, including the direction of the approach, the muscular, neural, and vascular dissection, and the anatomic structures exposed.

The far lateral approach is defined as a lateral occipital approach directed from posterolaterally behind the sternocleidomastoid muscle, as first reported by Heros (13). The muscular dissection is one of the most important aspects of the procedure. A detailed description of the muscular dissection in the far lateral approach has been reported previously (19, 27). To gain access to the anterior aspect of the CVJ laterally, the muscular exposure is performed using a horseshoe scalp flap because it provides easier reflection of the muscle layers inferiorly or inferolaterally, thus allowing a wider exposure of the lateral side and room for an upper cervical approach. The muscles are reflected in a single layer with the scalp because reflecting the muscles individually makes the closure more difficult and is associated with a high incidence of wound problems, such as pseudomeningocele. Reflecting the muscles forming the suboccipital triangle exposes the vertebral artery, which is surrounded by a rich venous plexus. The far lateral atlanto-occipital transarticular approach requires that the transverse process be opened and the third segment of the vertebral artery be transposed inferomedially. George and Laurian (7) and George et al. (9) were the first to describe the medial transposition of the vertebral artery from the axis to the dural entry point. This technique reduces the risk of injury of the vertebral artery during drilling of the medial portion of the atlanto-occipital joint. The subperiosteal exposure of the vertebral artery is a key point to avoid bleeding from the vertebral venous plexus. Drilling away or removing the entire lateral mass of the atlas increases access to the anterior aspect of the CVJ in front of the spinal cord, because the posterior margin of the lateral mass is usually located at the level of the anterior part of the spinal cord. Removing the entire lateral mass, including the anterior portion, provides greater access and is safer for retraction of the dural sac than removal of only the posterior portion of the lateral mass. Removing the inferior surface of the occipital condyle exposes the superior part of the odontoid process. It is not necessary to open the hypoglossal canal unless the lesion is situated above the lower clivus. This approach has several advantages over the anterior transoral approach, including shorter distance to the lesion, control of the vertebral artery, easy access to laterally located lesions, and the wide and sterile operative view; in addition, posterior stabilization is possible if needed. The far lateral atlanto-occipital transarticular approach, compared with the extreme lateral approach, provides an easy orientation familiar to neurosurgeons and eliminates manipulation near great vessels and the spinal accessory nerve. However, the far lateral atlanto-occipital transarticular approach has a disadvantage in not allowing visualization of the contralateral anterior extradural operative field. Some retraction of the dural sac is necessary in identifying the contralateral structures. Extradural lesions located in the ipsilateral anterolateral aspect of the CVJ can be managed with the far lateral atlanto-occipital transarticular approach.

The extreme lateral atlanto-occipital transarticular approach, directed from laterally through the articular pillars and the mastoid tip, was first described by Sen and Sekhar (23, 24). This approach is also called the anterolateral approach (11) or the transcondylar approach (1). The extent of drilling is the same as with the far lateral atlanto-occipital transarticular approach. Differences between the extreme lateral transatlantal approach and the far lateral atlanto-occipital transarticular approach are the skin incision, the muscular reflection, and the direction of the approach. In the extreme lateral approach, the sternocleidomastoid muscle is incised along its anterior border and is completely divided at the point of attachment to the occipital and temporal bones. Reflecting the muscle and spinal accessory nerve inferolaterally provides direct lateral access to the anterior aspect of the CVJ between the internal jugular vein and the dural sac. The basics of this exposure are similar to those described by Verbiest (26), who used this technique to remove osteophytes compressing the vertebral artery and nerve roots in the lower cervical spine; however, this approach did not access the midline. This technique is also similar to the oblique corpectomy, as described by George et al. (10). The extreme lateral atlanto-occipital transarticular approach has its main application in treating extradural lesions (1, 2, 8, 25), but it has also been used for intradural lesions (23, 24). For extradural nonneoplastic lesions of the CVJ, AlMefty et al. (1) reported using the transcondylar approach with drilling of the mastoid tip, the occipital condyle up to the inferior surface to the hypoglossal canal, and the condylar surface of the atlas. Care is required to preserve the spinal accessory nerve when the sternocleidomastoid muscle is reflected inferolaterally. In the extreme lateral atlanto-occipital transarticular approach, the muscles attached to the transverse process of the atlas are detached from their insertion on the transverse process. Care is taken not to damage the vertebral artery, the internal jugular vein, and the ventral rami of the spinal nerves, all of which exist beneath these muscles. This approach also requires transposition of the vertebral artery, as does the far lateral atlanto-occipital transarticular approach, using subperiosteal dissection along the upper margin of the axis. After mobilizing of the vertebral artery, the complete lateral mass of the atlas is drilled away, followed by the removal of the inferior surface of the occipital condyle if necessary. The extreme lateral atlanto-occipital transarticular approach, in addition to having the advantages of the far lateral approach, provides exposure of the entire odontoid process, the inferior aspect of the lower clivus, and the medial surface of the contralateral atlanto-occipital joint. Moreover, this approach eliminates the need to retract the dural sac to expose the odontoid and clivus anterior to the cervicomedullary junction. Complete drilling of the lateral atlantal mass by either the far lateral or extreme lateral approaches must be followed by occipitalcervical stabilization and fusion. This stabilization, however, can be performed in the same operative field in both approaches, whereas the anterior transoral approach requires another procedure if posterior occipital-cervical fusion is needed.

In summary, the far lateral atlanto-occipital transarticular approach would be chosen for lesions located in the ipsilateral anterior or anterolateral aspects of the extradural region of the CVJ. When lesions extend to the contralateral atlanto-occipital joint and the lower clivus, the extreme lateral atlanto-occipital transarticular approach would be chosen. These approaches would be ideal for lesions that involve the adjoining occipital and atlantal condyles and extend into the structures bordering the anterior extradural space, but not necessarily for lesions strictly localized to the odontoid process and median part of the anterior arch of the atlas, which might best be approached by the transoral route.

The far lateral and extreme lateral atlanto-occipital transarticular approaches provide an alternative to the transoral approach for exposure of extradural lesions in the CVJ. Both approaches avoid the contaminated nasopharynx and provide a shorter operative route.

Contributors: Masatou Kawashima, MD, Necmettin Tanriover, MD, Albert L. Rhoton, Jr., MD, Arthur J. Ulm, MD, and Toshio Matsushima, MD

Content from: Kawashima M, Tanriover N, Rhoton AL Jr, Ulm AJ, Matsushima M. Comparison of the far lateral and extreme lateral variants of the atlanto-occipital transarticular approach to anterior extradural lesions of the craniovertebral junction. Neurosurgery 2003;53:662–675, 10.1227/01.NEU.0000080070.16099.BB. With permission of Oxford University Press on behalf of the Congress of Neurological Surgeons.

The Neurosurgical Atlas is honored to maintain the legacy of Albert L. Rhoton, Jr., MD.

REFERENCES

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