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ANATOMIC REPORTS

COMPARISON OF THE FAR LATERAL AND EXTREME


LATERAL VARIANTS OF THE ATLANTO-OCCIPITAL
TRANSARTICULAR APPROACH TO ANTERIOR EXTRADURAL
LESIONS OF THE CRANIOVERTEBRAL JUNCTION
Masatou Kawashima, M.D. OBJECTIVE: Managing lesions situated in the anterior aspect of the craniovertebral
Department of Neurological junction (CVJ) remains a challenging neurosurgical problem. The purposes of this
Surgery, University of Florida,
Gainesville, Florida
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
Necmettin Tanriover, M.D. lateral atlanto-occipital transarticular approaches. The far lateral approach, as origi-
Department of Neurological nally described, is a lateral suboccipital approach directed behind the sternocleido-
Surgery, University of Florida, mastoid muscle and the vertebral artery and just medial to the occipital and atlantal
Gainesville, Florida
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 sternocleido-
Albert L. Rhoton, Jr., M.D.
mastoid muscle and behind the internal jugular vein along the front of the vertebral
Department of Neurological
Surgery, University of Florida, artery. Both approaches permit drilling of the condyles at the atlanto-occipital joint but
Gainesville, Florida provide a different exposure because of the differences in the direction of the
approach.
Arthur J. Ulm, M.D.
METHODS: Fifteen adult cadaveric specimens were studied using a magnification of
Department of Neurological
Surgery, University of Florida, ⫻3 to ⫻40 after perfusion of the arteries and veins with colored silicone. The
Gainesville, Florida microsurgical anatomy of the extradural aspects of the CVJ and the two atlanto-
occipital transarticular approaches were examined in stepwise dissections.
Toshio Matsushima, M.D. RESULTS: The far lateral atlanto-occipital transarticular approach provides excellent
Department of Neurosurgery,
Neurological Institute, Graduate
exposure of the extradural lesions located in the ipsilateral anterior and anterolateral
School of Medical Sciences, aspects of the extradural region of the CVJ. The extreme lateral atlanto-occipital
Kyushu University, Fukuoka, Japan 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 contralat-
Reprint requests:
Albert L. Rhoton, Jr., M.D.,
eral atlanto-occipital joint and the lower clivus.
Department of Neurological CONCLUSION: The far lateral and extreme lateral variants of the atlanto-occipital
Surgery, University of Florida Brain
Institute, P.O. Box 100265, 100
transarticular approach provide an alternative to the transoral approach to the anterior
South Newell Drive, Building 59, extradural structures at the CVJ. Compared with the transoral approach, both ap-
L2-100, Gainesville, FL proaches provide a shorter operative route, avoid the contaminated nasopharynx,
32610-0265.
Email:
reduce the incidence of cerebrospinal fluid leak, and are not limited laterally by the
rhoton@neurosurgery.ufl.edu atlanto-occipital joint.
KEY WORDS: Atlanto-occipital transarticular approach, Craniovertebral junction, Extradural lesion, Extreme
Received, December 18, 2002.
lateral, Far lateral, Microsurgical anatomy
Accepted, April 24, 2003.
Neurosurgery 53:662-675, 2003 DOI: 10.1227/01.NEU.0000080070.16099.BB www.neurosurgery-online.com

D
irect surgical approaches to extradural lesions of the site of neoplastic, vascular, traumatic, congenital, and degen-
anterior aspect of the craniovertebral junction (CVJ) erative lesions that may be approached anteriorly, posteriorly,
remain a challenge because of their deep location, the or laterally (6, 20) (Fig. 1, A and B). The anterior approaches,
vital neural structures in the area, and their relationship with which are mainly used for extradural lesions located in the
the vertebral artery and nasopharynx. The CVJ is a common anterior aspect of the CVJ, have significant disadvantages,

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ATLANTO-OCCIPITAL TRANSARTICULAR APPROACH VARIANTS

FIGURE 1. Surgical approaches to an


extradural lesion in the anterior aspect
of the CVJ. A and B (enlarged view),
anterior transoral approach (white ar-
row) and posterior, far lateral, and ex-
treme lateral approaches (blue arrow).
The atlanto-occipital transarticular ap-
proaches 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 ap-
proaches. E and F, the far lateral atlanto-
occipital transarticular approach pro-
vides access to the anterior or
anterolateral aspects of the CVJ, includ-
ing the odontoid process and the ipsilat-
eral 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 con-
dyle (H). Ant., anterior; Cond., con-
dyle; Cruc., cruciform; Horiz., horizon-
tal; ICA, internal carotid artery; Lat.,
lateral; Lig., ligament; Occip., occipital;
Post., posterior; Proc., process; PLL,
posterior longitudinal ligament; Trans.,
transverse; VA, vertebral artery.

including a contaminated field and the frequency of cerebro- anatomy of the anterior aspect of the CVJ, focusing especially
spinal fluid fistulae, lateral exposure limited by the atlanto- on the extradural space, and to examine the extent of the
occipital joint, and the depth of the operative field (5, 12, 17). anterior extradural exposure obtained with the atlanto-
The posterior approaches are preferred for most intradural occipital transarticular variants of the far lateral and extreme
lesions, especially those located lateral or posterior to the lateral approaches.
cervicomedullary junction (22). Both the far lateral transcon-
dylar approach and the extreme lateral transcondylar ap- MATERIALS AND METHODS
proach provide excellent surgical access to intradural lesions
of the anterolateral CVJ (3, 4, 9, 13, 19, 23, 24, 27), but they may The exposure obtained with the atlanto-occipital transartic-
also be used to reach anterior extradural lesions (Fig. 1, C–H). ular variants of the far lateral and extreme lateral approaches
The purposes of this study were to examine the microsurgical and related anatomy were examined in stepwise dissections

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KAWASHIMA ET AL.

using 15 adult cadaveric specimens and a magnification of ⫻3 nected in front by a short anterior arch and behind by a longer,
to ⫻40. The arteries and veins were perfused with colored curved posterior arch. The position of the usual vertebral body
silicone. The bone dissections were performed with the Midas is occupied by the odontoid process of the axis. The anterior
Rex drill (Fort Worth, TX). arch is convexed forward and has a median anterior tubercle.
The posterior arch is convexed backward and has a median
RESULTS posterior tubercle and a groove on the lateral part of its
upper-outer surface in which the vertebral artery courses. The
Anatomic Considerations upper surface of each lateral mass has an oval concave facet
that faces upward and medially and articulates with the oc-
Osseous Relationship cipital condyle that faces downward and laterally. The inferior
The osseous structures that must be considered in planning surface of each lateral mass has a circular, flat, or slightly
an approach to the region of the CVJ are the occipital bone, the concave facet that faces downward, medially, and slightly
atlas, and the axis. backward and that articulates with the superior articular facet
Occipital Bone. The occipital bone surrounds the foramen of the axis. The medial aspect of each lateral mass has a small
magnum. The foraminal opening is oval shaped and is wider tubercle for the attachment of the transverse ligament of the
posteriorly than anteriorly. The occipital bone is divided into atlas that passes behind the odontoid process. Each transverse
a basal part situated in front of the foramen magnum, paired foramen is situated between the lateral mass and the trans-
condylar parts located lateral to the foramen magnum, and a verse process and transmits a vertebral artery. Note that the
squamosal part located above and behind the foramen cervical spinal cord is located at the level of the posterior
magnum. margin of the lateral mass.
The basilar part of the occipital bone, which is also referred The axis, the second cervical vertebra, more closely resem-
to as the clivus, is a thick quadrangular plate of bone that bles the typical vertebrae than the atlas, but it is distinguished
extends forward and upward. It joins the sphenoid bone at the by the odontoid process (dens) that projects upward from the
sphenoccipital synchondrosis just below the dorsum sellae. body. On the front of the dens is an articular facet that forms
The superior surface of the clivus is concave from side to side a joint with the facet on the back of the anterior arch of the
and is separated on each side from the petrous part of the atlas. The dens has a pointed apex that is joined by the apical
temporal bone by the petroclival fissure. On the inferior sur- ligament, has a flattened side where the alar ligaments are
face of the basilar part in front of the foramen magnum, a attached, and is grooved at the base of its posterior surface
small elevation, the pharyngeal tubercle, gives an attachment where the transverse ligament of the atlas passes. The dens
to the fibrous raphe of the pharynx. and body are flanked by a pair of large oval facets that extend
The paired condylar parts are situated at the lateral sides of laterally from the body onto the adjoining parts of the pedicles
the foramen magnum. The occipital condyles, which articulate and articulate with the inferior facets of the atlas. The anterior
with the atlas, protrude from the external surface of these aspect of the body is hollowed out on each side of the midline
parts. The condyles are located lateral to the anterior half of in the area where the longus colli muscles attach. The lamina
the foramen magnum. They are oval in shape, convex down- of the axis is thicker than those of any other cervical vertebrae,
ward, face downward and laterally, and have their long axes the pedicles are more stout, and the spinous process is larger
directed forward and medially. A tubercle that gives an at- (Fig. 3).
tachment to the alar ligament of the odontoid process is situ- The Atlantoaxial Joint. Articulation of the atlas and axis
ated on the medial side of each condyle. The hypoglossal comprises four synovial joints: two median ones on the front
canal, which transmits the hypoglossal nerve, is situated and back of the dens and paired lateral ones between the
above the condyle and may be partially or completely divided opposing articular facets on the lateral masses of the atlas and
by a bony septum. The condylar fossa, a depression located on axis. The median joints are situated on the front and back of
the external surface behind the condyle, is often perforated to the dens and have their own fibrous capsule and synovial
form the posterior condylar canal, through which an emissary cavity. The anterior one is situated between the anterior sur-
vein connects the vertebral venous plexus with the sigmoid face of the dens and the posterior aspect of the anterior arch of
sinus. the atlas. The posterior one has an even larger synovial cavity
The squamous part is an internally concave plate located and lies between the cartilage-covered anterior surface of the
above and behind the foramen magnum. It contains several transverse ligament of the atlas and the posterior surface of the
prominences, such as the external occipital protuberance and dens.
ridges, including nuchal lines on which the numerous muscles The atlas and axis are united by the cruciform ligament, the
of the neck attach (Fig. 2). anterior and posterior longitudinal ligaments, and the articu-
Complex of the Atlas and the Axis. The atlas, the first cervical lar capsules surrounding the joints between the opposing
vertebra, differs from the other cervical vertebrae by being articular facets on the lateral masses. The cruciform ligament
ring shaped and by lacking a vertebral body and spinous has transverse and vertical parts that form a cross behind the
process. It consists of two thick lateral masses situated at the dens. The transverse part, called the transverse ligament, is a
anterolateral parts of the ring. The lateral masses are con- thick, strong band that arches across the ring of the atlas

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ATLANTO-OCCIPITAL TRANSARTICULAR APPROACH VARIANTS

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 pro-
vided 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 mag-
num. 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 situ-
ated lateral to the anterior half of the
foramen magnum on the external sur-
face. Arrows show the direction of the
far lateral (red) and extreme lateral
(yellow) atlanto-occipital transarticu-
lar approaches. B, left oblique view
directed through the foramen magnum
from the left side to show the intracra-
nial aspect of the right hypoglossal
canal situated above the condyle. The
condylar fossa is located behind the
condyle and may open into the condy-
lar 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.

behind the dens and divides the vertebral canal into a larger the atlas, and laterally to the capsule of the atlanto-occipital
posterior compartment containing the dura and the spinal joints. The posterior atlanto-occipital membrane is a thin sheet
cord and a smaller anterior compartment containing the odon- connected above to the posterior margin of the foramen mag-
toid process. num and below to the upper border of the posterior arch of the
On the ventral surface, the atlas and axis are connected by atlas. The lateral border of the membrane is free and arches
the anterior longitudinal ligament, which is a wide band fixed behind the vertebral artery and the first cervical nerve root.
above to the lower border of the anterior arch of the atlas and The lateral edge of this membrane may be ossified in the area
below to the front of the body of the axis. The posterior where it arches over the posterior aspect of the vertebral
longitudinal ligament is attached below to the posterior sur- artery, thus creating a partial or complete osseous ring around
face of the body of the axis and above to the transverse part of the artery on the medial side of the atlanto-occipital joint (Fig.
the cruciform ligament and the clivus (Figs. 3 and 4). 4A).
The Atlanto-occipital Joint. The atlas and the occipital bone Axis and Occipital Bone. Four fibrous bands—the tectorial
are united by the articular capsules surrounding the atlanto- membrane, the paired alar ligaments, and the apical liga-
occipital joints and by the anterior and posterior atlanto- ment—connect the axis and the occipital bone. The tectorial
occipital membranes. The anterior atlanto-occipital membrane membrane is a cephalic extension of the posterior longitudinal
is attached superiorly to the anterior edge of the foramen ligament that covers the dens and cruciform ligament. It is
magnum, inferiorly to the superior edge of the anterior arch of attached below to the posterior surface of the body of the axis,

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KAWASHIMA ET AL.

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 indistin-
guishably into the medulla at a
level arbitrarily set to be at the
upper limit of the dorsal and ven-
tral rootlets forming the first cer-
vical nerve. It is easier to differen-
tiate 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 ab-
sent in many cases. The fact that
FIGURE 3. The atlas and the axis. A, superior view; B, the junction of the spinal cord and
anterior view; C, posterior view; D, oblique left posterior medulla is situated at the rostral
view; E, right lateral view. A, the atlas consists of two
margin of the first cervical root
thick lateral masses situated anterolaterally that are con-
nected in front by a short anterior arch and behind by a
means that the medulla, and not
longer curved posterior arch. The medial aspect of each the spinal cord, occupies the fora-
lateral mass has a small tubercle for the attachment of men magnum (Figs. 3A and 4A).
the transverse ligament of the atlas, which passes behind
the odontoid process. The anterior arch is convexed for- Cervical Nerve Roots
ward and has a median anterior tubercle. The position of Each dorsal and ventral root is
the vertebral body is occupied by the odontoid process of composed of a series of six to
the axis. Note that the posterior margin of the lateral eight rootlets that fan out to enter
mass is located lateral to the anterior part of the spinal cord. B, the axis is distinguished from the typical vertebrae by
the posterolateral and anterolat-
the odontoid process (dens), which projects upward from the body. On the front of the dens is an articular facet that
eral surfaces of the spinal cord,
forms a joint with the facet on the posterior surface of the anterior arch of the atlas. The dens and body are flanked by
respectively. The dorsal and ven-
paired large oval facets that extend laterally from the body onto the adjoining parts of the pedicles and articulate with
tral roots cross the subarachnoid
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 space and transverse the dura ma-
median posterior tubercle and a groove on the lateral part of its upper-outer surface in which the vertebral artery ter separately, then unite close to
courses. The upper surface of each lateral mass has an oval concave facet that faces upward and medially and articu- the intervertebral foramen to form
lates with the occipital condyle, which faces downward and laterally. The dens has a pointed apex that is joined by the spinal nerves. The rootlets in
the apical ligament and flattened sides where the alar ligaments are attached. The lamina of the axis is thicker than the region of the foramen mag-
any other cervical vertebrae, and the spinous process is larger. The C2 nerve emerges between the posterior arch of num pass almost directly lateral
the atlas and the lamina of the axis. Distal to the ganglion, the nerve divides into larger dorsal and smaller ventral
to reach their dural foramina. The
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.,
neurons of the dorsal roots collect
ventral. to form ganglia located just prox-
imal to the union of the dorsal
and ventral root; however, the
above to the upper surface of the occipital bone in front of the first cervical dorsal root and associated ganglion may be absent.
foramen magnum, and laterally to the medial sides of the The C1, C2, and C3 nerves, distal to the ganglion, divide into
atlanto-occipital joints. The alar ligaments are two strong dorsal and ventral rami. The dorsal rami divide into medial and
bands that arise on each side of the upper part of the dens and lateral branches that supply the skin and muscles of the posterior
extend obliquely superolateral to attach to the medial surfaces region of the neck. The C1 nerve, termed the suboccipital nerve,
of the occipital condyles. The apical ligament of the odontoid leaves the vertebral canal between the occipital bone and atlas
process extends from the tip of the dens to the anterior margin and has a dorsal ramus that is larger than the ventral ramus. The
of the foramen magnum and is situated between the anterior dorsal ramus courses between the posterior arch of the atlas and

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ATLANTO-OCCIPITAL TRANSARTICULAR APPROACH VARIANTS

FIGURE 4. Extradural region of the an-


terior aspect of the CVJ. A–G, posterior
views; H, lateral view of stepwise dissec-
tion. 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 an-
terior aspect of the CVJ. The dura is situ-
ated in front of the spinal cord. The ver-
tebral 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 lig-
ament. D, the tectorial membrane has
been removed to expose the cruciform and
alar ligaments. The horizontal portion of
the cruciform ligament, called the trans-
verse ligament of the atlas, extends later-
ally 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 liga-
ments pass upward and laterally and at-
tach to the lateral edges of the occipital
condyle. E, the cruciform and alar liga-
ments have been removed to expose the
dens. The apical ligament of the dens ex-
tends 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 atlanto-
occipital transarticular approach. The in-
ferior 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., ca-
pitis; 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.

the vertebral artery. The C1 ventral ramus courses between the medial branch, called the greater occipital nerve, and a small
posterior arch of the atlas and the vertebral artery and passes lateral branch. The C2 ventral ramus courses between the verte-
forward, lateral to the lateral mass of the atlas and medial to the bral arches and transverse processes of the atlas and axis and
vertebral artery, and supplies the rectus capitis lateralis. The C2 behind the vertebral artery to leave this operative field (Figs. 3
nerve emerges between the posterior arch of the atlas and lamina and 4).
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 Arterial Relationships
smaller ventral ramus. After passing below and supplying the Vertebral Artery (Extradural Portion). The paired vertebral
inferior oblique muscle, the dorsal ramus divides into a large arteries arise from the subclavian arteries, ascend through the

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KAWASHIMA ET AL.

FIGURE 5. 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 infe-
riorly 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 mus-
cle. 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 rec-
tus capitis posterior major inferiorly and medially, the superior oblique lat-
erally, 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. (Figure and leg-
end continue on next page.)

transverse processes of the upper six cervical vertebrae, pass between the deep cervical and epidural veins. The C1 nerve
behind the lateral masses of the atlas, enter the dura mater root passes through the dura mater on the lower surface of the
behind the occipital condyles, ascend through the foramen vertebral artery and between the artery and the groove on the
magnum to the front of the medulla, and join to form the posterior arch of the atlas. This bony groove is sometimes
basilar artery at the pontomedullary junction. transformed into a bony canal that completely surrounds a
The extradural part of the vertebral artery is divided into short segment of the artery. The terminal extradural segment
three segments. The origin of the first segment extends from of the vertebral artery gives rise to the posterior meningeal
the subclavian artery to enter the lowest transverse foramen, and posterior spinal arteries, deep cervical musculature
usually at the C6 level. The second segment ascends through branches, and sometimes the posteroinferior cerebellar artery
the transverse foramina of the upper six cervical vertebrae in (Figs. 3 and 4).
front of the cervical nerve roots. This segment deviates later-
ally just above the axis to reach the laterally placed transverse
foramen of the atlas. The third segment, the one most inti- Venous Relationships
mately related to the foramen magnum, extends from the Extradural Groups. Venous flow in this area empties into
foramen in the transverse process of the atlas to the site of two systems, one drained by the internal jugular vein and
passage through the dura mater. The third segment passes another drained by the vertebral venous plexus. The internal
medially behind the lateral mass of the atlas and atlanto- jugular vein originates at the jugular foramen by the conflu-
occipital joint and is pressed into the groove on the upper ence of the sigmoid and inferior petrosal sinuses. The venous
surface of the lateral part of the posterior arch of the atlas, plexus surrounding the vertebral artery in the suboccipital
where it courses along the floor of the suboccipital triangle. It triangle is formed by numerous small channels that empty
enters the vertebral canal by passing anterior to the lateral into the internal vertebral plexuses (between the dura and the
border of the atlanto-occipital membrane. The vertebral artery vertebrae), which issue from the vertebral canal above the
is surrounded by a venous plexus composed of anastomoses posterior arch of the atlas. The posterior condylar emissary

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ATLANTO-OCCIPITAL TRANSARTICULAR APPROACH VARIANTS

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 ca-
nal to connect the basilar venous
plexus with the marginal sinus
that encircles the foramen mag-
num (Fig. 4A).

The Far Lateral and Extreme


Lateral Variants of the
Atlanto-occipital
Transarticular Approach
The description of the far lat-
eral and extreme lateral ap-
proaches (Fig. 1, C–H, and Fig. 2,
A and C–E) to the anterior as-
pect of the CVJ is divided into
two anatomic stages. The first
stage, the muscular dissection,
consists of the skin incision, re-
flection of muscles (including
those forming the suboccipital
triangle), and examination of the
relationship of the muscles to
the vertebral arteries, the verte-
bral venous plexus, the trans-
verse process of the atlas, and
the upper cervical nerves. The
second stage, the extradural dis-
FIGURE 5. Continued
E, exposure and control of the vertebral artery is a most important aspect of the procedure. The artery, section, examines the transposi-
after ascending through the transverse process of the atlas, turns medially behind the lateral mass of the tion of the vertebral artery, the
atlas and the atlanto-occipital joint and is pressed into the groove, marking its course on the upper surface extent of the atlanto-occipital ar-
of the lateral part of the posterior arch of the atlas. F, the C1 nerve courses on the lower surface of the ticular removal, and the expo-
artery between the artery and posterior arch of the atlas. The subperiosteal dissection is continued until the sure and identification of the ex-
vertebral artery is identified within its groove on the superior aspect of the atlas. The inferior aspect of the tradural space of the anterior
periosteal sheath of the vertebral artery is freed from this groove using subperiosteal dissection. The poste- aspect of the CVJ.
rior arch of the atlas is removed from just beyond the midline on the opposite side to the ipsilateral trans-
verse foramen. G, transposing the vertebral artery out of the atlantal transverse foramen allows a more lat- Far Lateral Atlanto-occipital
eral exposure. This requires prolongation of the subperiosteal dissection inside the transverse foramen of Transarticular Approach
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 Muscular Stage. The proce-
occipital condyle and the superior articular facet of the axis is totally removed. Resection of the ipsilateral dure is performed with the pa-
transverse and alar ligaments exposes the odontoid process. I, the inferior surface of the occipital condyle tient in the sitting or modified
can be removed if it is difficult to see the superior aspect of the dens. Care should be taken to avoid damag- park-bench position (3). The ex-
ing the hypoglossal nerve as it passes above the occipital condyle. J, the contralateral occipital condyle is posure is accomplished using a
not exposed, but the contralateral edge of the dens can be seen and removed, with or without mild retrac- horseshoe scalp flap because it
tion of the ventral aspect of the dural sac. The dural sac can be retracted posteriorly to see the dens and provides a better display of the
ipsilateral half of the lower clivus. The area can be drilled using the far lateral approach, as shown in Fig-
muscular layers and their rela-
ure 1, E and F. A-O, atlanto-occipital; Ant., anterior; Art., articular; Cap., capitis; CN, cranial nerve;
tionships to the neural and vas-
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; cular structures than a linear in-
Obl., oblique; Occip., occipital; P.I.C.A., posteroinferior cerebellar artery; Post., posterior; Proc., process; cision (Fig. 5A). The incision
Rec., rectus; Semispin., semispinalis; Splen., splenius; Suboccip., suboccipital; Sup., superior; Trans., begins in the midline, approxi-
transverse; V., vein; VA, vertebral artery; Vent., ventral. mately 5 cm below the external

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KAWASHIMA ET AL.

with the scalp to expose the


muscles forming the suboccipi-
tal triangle; however, stepwise
muscular dissection was per-
formed on the cadavers to see
the relationship of muscles su-
perficial to the triangle.
The skin flap is reflected down-
ward and medially to expose the
upper part of the superficial layer
of muscles formed by the sterno-
cleidomastoid and splenius capi-
tis muscles laterally and the tra-
pezius and the semispinalis
capitis muscles medially (Fig. 5B).
Dividing the sternocleidomastoid
just below, with preservation of
the fascial attachment to the oc-
cipital bone for closure, exposes
the upper extension of the sple-
nius capitis. Detaching the trape-
zius and splenius capitis muscles
exposes the semispinalis capitis
muscle, which is reflected down-
ward to expose the superior and
inferior oblique muscles and the
transverse process of the atlas,
which has a prominent apex pal-
pable through the skin between
the mastoid process and mandib-
ular angle. The suboccipital trian-
gle, which is limited by three
muscles (above and medially by
FIGURE 6. Extreme lateral atlanto-occipital transarticular approach: muscular (A–F) and extradural (G–N) stages. A, the rectus capitis posterior major,
the skin incision starts approximately 6 cm below the tip of the mastoid process and follows the anterior border of the above and laterally by the supe-
sternocleidomastoid muscle up to the level of the external acoustic meatus, where it curves posteriorly above the
rior oblique, and below and later-
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 ally by the inferior oblique), is ex-
runs in a fatty and lymphatic sheath that covers the deep aspect of the muscle. The average distance between the tip of posed by reflecting the more
the mastoid process and the accessory nerve entering the sternocleidomastoid muscle is 3.5 cm. Therefore, the upper few superficial muscles downward
centimeters of the muscle can be dissected quickly, but the lower portion must be dissected carefully. Reflecting the (Fig. 5C). The suboccipital triangle
sternocleidomastoid inferolaterally exposes the plane between the internal jugular vein and the sternocleidomastoid is opened by reflecting the rectus
muscle. D and E, reflecting the splenius capitis, semispinalis capitis, and longissimus capitis muscles inferomedially capitis posterior major inferiorly
exposes the suboccipital triangle and the attachment of the superior and inferior oblique, the rectus capitis lateralis, and and medially, the superior
the levator scapulae muscles to the transverse process of the atlas. The transverse process of the atlas can be palpated in oblique laterally, and the inferior
the exposure. F, reflecting the muscles forming the suboccipital triangle exposes the vertebral artery between the
oblique medially. Opening the tri-
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. (Figure and angle exposes the portion of the
legend continue on next page.) vertebral venous plexus that sur-
rounds the vertebral artery as it
occipital protuberance, and is directed upward to just above passes behind the atlanto-occipital joint and across the upper
the external occipital protuberance, turns laterally just edge of the posterior arch of the atlas. The C2 nerve emerges
above the superior nuchal line, reaches the mastoid, and turns between the posterior arch of the atlas and the lamina of the axis.
downward in front of the posterior border of the sternoclei- Distal to the ganglion, the nerve divides into a larger dorsal and
domastoid muscle onto the lateral aspect of the neck to ap- a smaller ventral rami (Fig. 5D).
proximately 5 cm below the mastoid tip and below where the Extradural Stage. Exposure and control of the vertebral
transverse process of the atlas can be palpated through artery is a very important aspect of the procedure. The verte-
the skin. The muscles are generally reflected in a single layer bral artery, above the transverse foramen of the axis, is di-

670 | VOLUME 53 | NUMBER 3 | SEPTEMBER 2003 www.neurosurgery-online.com


ATLANTO-OCCIPITAL TRANSARTICULAR APPROACH VARIANTS

FIGURE 6. Continued
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 spi-
nal accessory nerve when the sterno-
cleidomastoid muscle is reflected
inferolaterally. The deepest muscle is
formed by the uppermost slip of the
levator scapulae, the superior and infe-
rior 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 nec-
essary. 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 atlanto-
occipital 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., contralat-
eral; 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.

rected somewhat laterally as it ascends to reach the transverse the atlas (Fig. 5E). The C1 nerve courses on the lower surface
foramen of the atlas, which is situated further lateral than the of the artery between the artery and the posterior arch of the
transverse foramen of the axis. The artery, after ascending atlas. The inferior margin of the posterior arch of the atlas is
through the transverse process of the atlas, turns medially first exposed subperiosteally beginning at the midline and
behind the lateral mass of the atlas and the atlanto-occipital proceeding to the transverse process. The exposure then
joint and is pressed into the groove, marking its course on the progresses toward the superior margin of the posterior arch.
upper surface on the lateral part of the posterior arch of The subperiosteal dissection is continued until the vertebral

NEUROSURGERY VOLUME 53 | NUMBER 3 | SEPTEMBER 2003 | 671


KAWASHIMA ET AL.

artery is identified within its groove on the superior aspect of nerve root is exposed between the atlas and the axis. The
the atlas. The inferior aspect of the periosteal sheath of the ventral ramus of the C2 nerve root curves around the vertebral
vertebral artery is freed from this groove using subperiosteal artery. The posterior belly of the digastric muscle is preserved
dissection to minimize bleeding from the vertebral venous to protect the facial nerve that exits the skull at the anterior
plexus. The posterior arch of the atlas is removed from just margin of the muscle (Fig. 6F).
beyond the midline on the opposite side to the ipsilateral Extradural Stage. An important aspect of the approach is the
transverse foramen (Fig. 5F). Transposing the vertebral artery exposure and control of the vertebral artery. The artery is iden-
out of the atlantal transverse foramen allows a more lateral tified in the groove on the upper surface of the C1 arch after
exposure. The subperiosteal dissection is extended along the exposing the transverse process and the lateral part of the pos-
posterior root of the transverse foramen, then the transverse terior arch of the atlas. This groove marks the posterior edge of
foramen is unroofed by removing the posterior root. The the lateral mass of the atlas (Fig. 6, G–J). The periosteal sheath
vertebral artery is dissected free of the axis and displaced lining the groove is elevated using subperiosteal dissection, and
medially and caudally (Fig. 5G). The lateral mass of the atlas the transverse process is unroofed using a drill or small rongeur.
between the occipital condyle and the superior articular facet Exposing the vertebral artery subperiosteally reduces bleeding
of the axis is totally removed. Resection of the ipsilateral from the vertebral venous plexus that lies inside the periosteal
transverse and alar ligaments exposes the odontoid process sheath surrounding the artery. Removal of the posterior root of
(Fig. 5H). The inferior surface of the occipital condyle can be the transverse foramen permits the artery to be displaced down-
removed if it is difficult to see the superior aspect of the dens ward and laterally, away from the atlanto-occipital joint and
(Fig. 5I). Care should be taken to avoid damaging the hypo- lateral mass of the atlas (Fig. 6K). The lateral mass of the atlas is
glossal nerve as it passes above the occipital condyle. The totally removed up to the occipital condyle and down to the
contralateral occipital condyle is not exposed, but the con- superior articular facet of the axis, thus exposing the odontoid
tralateral edge of the dens can be seen and removed, with or process of the axis. The occipital condyle projects downward
without mild retraction of the ventral aspect of the dural sac. along the lateral edges of the anterior half of the foramen mag-
The anterior part of the cervical spinal cord is located medial num. The superior articular facet of the axis is positioned along
to the posterior part of the lateral mass. Gentle retraction of the the lateral side of the base of the odontoid process (Fig. 6L).
dural sac permits visualization of the dens and the ipsilateral Drilling can be extended to the lower surface of the occipital
half of the lower clivus (Fig. 5J). condyle to expose the superior aspect of the dens (Fig. 6M).
Removing the odontoid process exposes the medial aspect of the
Extreme Lateral Atlanto-occipital Transarticular Approach contralateral atlanto-occipital joint and the inferior surface of the
lower clivus (Fig. 6N). Care is taken to avoid damage to the
Muscular Stage. The patient is placed in the straight lateral internal jugular vein, which is located immediately anterior to
position. The skin incision starts approximately 6 cm below the transverse process of the atlas.
the tip of the mastoid process and follows the anterior border
of the sternocleidomastoid muscle up to the level of the exter-
nal acoustic meatus, where it curves posteriorly above the DISCUSSION
attachment of the muscle (Fig. 6A). The insertion of the ster-
nocleidomastoid muscle is divided, leaving a musculofascial Neoplastic, vascular, traumatic, congenital, and degenera-
cuff attached to the mastoid process for closure. Care should tive lesions involving the extradural space of the anterior
be taken to identify the spinal accessory (XI) nerve, which runs aspect of the CVJ are not rare. Some controversy exists regard-
in a fatty and lymphatic sheath that covers the deep aspect of ing the appropriate approach to lesions in this region. The
the muscle. The average distance between the tip of the mas- anterior approaches, including the transoral approach and its
toid process and the accessory nerve entering the sternoclei- variations, are used predominantly for extradural lesions lo-
domastoid muscle is 3.5 cm. Therefore, the upper few centi- cated in the anterior aspect of the CVJ (5, 12, 14, 15, 17).
meters of the muscle can be dissected quickly, but the lower Posterior, posterolateral, and lateral approaches have fre-
portion must be dissected carefully. Reflecting the sternoclei- quently been used to access intradural lesions located along
domastoid muscle inferolaterally exposes the plane between the anterior or anterolateral aspect of the CVJ (4, 11, 13, 22–24).
the internal jugular vein and the sternocleidomastoid muscle However, detailed microsurgical anatomic studies of the ex-
(Fig. 6, B and C). Reflecting the splenius capitis, semispinalis tradural space of the anterior aspect of the CVJ are rare (1, 2,
capitis, and longissimus capitis muscles inferomedially ex- 25).
poses the suboccipital triangle and the attachment of the su- A wide variety of posterolateral surgical approaches for the
perior and inferior oblique, the rectus capitis lateralis, and the anterior or anterolateral CVJ have been described (3, 4, 9, 11,
levator scapulae muscles to the transverse process of the atlas 13, 16, 18, 21–24, 27). These approaches are categorized into
(Fig. 6, D and E). The transverse process of the atlas can be two major groups: far lateral and transcondylar approaches.
palpated in the exposure. Dividing the insertion of and reflect- Without drilling of the occipital condyle, the basic far lateral
ing the muscles forming the suboccipital triangle exposes the approach, which is also described as a posterolateral ap-
vertebral artery between the transverse foramen of the axis proach, may be all that is required to reach some lesions
and the point where it penetrates the dura mater. The C2 located along the anterolateral margin of the foramen mag-

672 | VOLUME 53 | NUMBER 3 | SEPTEMBER 2003 www.neurosurgery-online.com


ATLANTO-OCCIPITAL TRANSARTICULAR APPROACH VARIANTS

num. However, it also provides a route through which the vantage in not allowing visualization of the contralateral anterior
transcondylar, supracondylar, and paracondylar approaches extradural operative field. Some retraction of the dural sac is
and several modifications of the far lateral approach can be necessary in identifying the contralateral structures. Extradural
completed (19, 27). The atlanto-occipital transarticular ap- lesions located in the ipsilateral anterolateral aspect of the CVJ
proaches can be divided into two types: far lateral (postero- can be managed with the far lateral atlanto-occipital transarticu-
lateral) and extreme lateral, depending on the extent of the lar approach.
anterior extradural exposure at the CVJ. These two transartic- The extreme lateral atlanto-occipital transarticular approach,
ular routes are similar but completely distinct from each other directed from laterally through the articular pillars and the mas-
from several points of view, including the direction of the toid tip, was first described by Sen and Sekhar (23, 24). This
approach, the muscular, neural, and vascular dissection, and approach is also called the anterolateral approach (11) or the
the anatomic structures exposed. transcondylar approach (1). The extent of drilling is the same as
The far lateral approach is defined as a lateral occipital ap- with the far lateral atlanto-occipital transarticular approach. Dif-
proach directed from posterolaterally behind the sternocleido- ferences between the extreme lateral transatlantal approach and
mastoid muscle, as first reported by Heros (13). The muscular the far lateral atlanto-occipital transarticular approach are the
dissection is one of the most important aspects of the procedure. skin incision, the muscular reflection, and the direction of the
A detailed description of the muscular dissection in the far lateral approach. In the extreme lateral approach, the sternocleidomas-
approach has been reported previously (19, 27). To gain access to toid muscle is incised along its anterior border and is completely
the anterior aspect of the CVJ laterally, the muscular exposure is divided at the point of attachment to the occipital and temporal
performed using a horseshoe scalp flap because it provides easier bones. Reflecting the muscle and spinal accessory nerve infero-
reflection of the muscle layers inferiorly or inferolaterally, thus laterally provides direct lateral access to the anterior aspect of the
allowing a wider exposure of the lateral side and room for an CVJ between the internal jugular vein and the dural sac. The
upper cervical approach. The muscles are reflected in a single basics of this exposure are similar to those described by Verbiest
layer with the scalp because reflecting the muscles individually (26), who used this technique to remove osteophytes compress-
makes the closure more difficult and is associated with a high ing the vertebral artery and nerve roots in the lower cervical
incidence of wound problems, such as pseudomeningocele. Re- spine; however, this approach did not access the midline. This
flecting the muscles forming the suboccipital triangle exposes the technique is also similar to the oblique corpectomy, as described
vertebral artery, which is surrounded by a rich venous plexus. by George et al. (10). The extreme lateral atlanto-occipital trans-
The far lateral atlanto-occipital transarticular approach requires articular approach has its main application in treating extradural
that the transverse process be opened and the third segment of lesions (1, 2, 8, 25), but it has also been used for intradural lesions
the vertebral artery be transposed inferomedially. George and (23, 24). For extradural nonneoplastic lesions of the CVJ, Al-
Laurian (7) and George et al. (9) were the first to describe the Mefty et al. (1) reported using the transcondylar approach with
medial transposition of the vertebral artery from the axis to drilling of the mastoid tip, the occipital condyle up to the inferior
the dural entry point. This technique reduces the risk of injury surface to the hypoglossal canal, and the condylar surface of the
of the vertebral artery during drilling of the medial portion of the atlas. Care is required to preserve the spinal accessory nerve
atlanto-occipital joint. The subperiosteal exposure of the verte- when the sternocleidomastoid muscle is reflected inferolaterally.
bral artery is a key point to avoid bleeding from the vertebral In the extreme lateral atlanto-occipital transarticular approach,
venous plexus. Drilling away or removing the entire lateral mass the muscles attached to the transverse process of the atlas are
of the atlas increases access to the anterior aspect of the CVJ in detached from their insertion on the transverse process. Care is
front of the spinal cord, because the posterior margin of the taken not to damage the vertebral artery, the internal jugular
lateral mass is usually located at the level of the anterior part of vein, and the ventral rami of the spinal nerves, all of which exist
the spinal cord. Removing the entire lateral mass, including the beneath these muscles. This approach also requires transposition
anterior portion, provides greater access and is safer for retrac- of the vertebral artery, as does the far lateral atlanto-occipital
tion of the dural sac than removal of only the posterior portion of transarticular approach, using subperiosteal dissection along the
the lateral mass. Removing the inferior surface of the occipital upper margin of the axis. After mobilizing of the vertebral artery,
condyle exposes the superior part of the odontoid process. It is the complete lateral mass of the atlas is drilled away, followed by
not necessary to open the hypoglossal canal unless the lesion is the removal of the inferior surface of the occipital condyle if
situated above the lower clivus. This approach has several ad- necessary. The extreme lateral atlanto-occipital transarticular ap-
vantages over the anterior transoral approach, including shorter proach, in addition to having the advantages of the far lateral
distance to the lesion, control of the vertebral artery, easy access approach, provides exposure of the entire odontoid process, the
to laterally located lesions, and the wide and sterile operative inferior aspect of the lower clivus, and the medial surface of the
view; in addition, posterior stabilization is possible if needed. contralateral atlanto-occipital joint. Moreover, this approach
The far lateral atlanto-occipital transarticular approach, com- eliminates the need to retract the dural sac to expose the odon-
pared with the extreme lateral approach, provides an easy ori- toid and clivus anterior to the cervicomedullary junction. Com-
entation familiar to neurosurgeons and eliminates manipulation plete drilling of the lateral atlantal mass by either the far lateral or
near great vessels and the spinal accessory nerve. However, the extreme lateral approaches must be followed by occipital-
far lateral atlanto-occipital transarticular approach has a disad- cervical stabilization and fusion. This stabilization, however, can

NEUROSURGERY VOLUME 53 | NUMBER 3 | SEPTEMBER 2003 | 673


KAWASHIMA ET AL.

be performed in the same operative field in both approaches, 15. James D, Crockard HA: Surgical access to the base of skull and upper
whereas the anterior transoral approach requires another proce- cervical spine by extended maxillotomy. Neurosurgery 29:411–416, 1991.
16. Lot G, George B: The extent of drilling in lateral approaches to the cranio-
dure if posterior occipital-cervical fusion is needed. cervical junction area from a series of 125 cases. Acta Neurochir (Wien)
In summary, the far lateral atlanto-occipital transarticular 141:111–118, 1999.
approach would be chosen for lesions located in the ipsilateral 17. Menezes AH, VanGilder JC: Transoral-transpharyngeal approach to the
anterior or anterolateral aspects of the extradural region of the anterior craniocervical junction: Ten-year experience with 72 patients.
J Neurosurg 69:895–903, 1988.
CVJ. When lesions extend to the contralateral atlanto-occipital
18. Muhlbauer M, Knosp E: The lateral transfacetal retrovascular approach for
joint and the lower clivus, the extreme lateral atlanto-occipital an anteriorly located chordoma originating from the second cervical verte-
transarticular approach would be chosen. These approaches bra. Acta Neurochir (Wien) 143:369–376, 2001.
would be ideal for lesions that involve the adjoining occipital 19. Rhoton AL Jr: The far-lateral approach and its transcondylar, supracondylar,
and atlantal condyles and extend into the structures bordering and paracondylar extensions. Neurosurgery 47[Suppl 1]:S195–S209, 2000.
20. Rhoton AL Jr: The foramen magnum. Neurosurgery 47[Suppl 1]:S155–S193,
the anterior extradural space, but not necessarily for lesions 2000.
strictly localized to the odontoid process and median part of 21. Salas E, Sekhar LN, Ziyal IM, Caputy AJ, Wright DC: Variations of the
the anterior arch of the atlas, which might best be approached extreme-lateral craniocervical approach: Anatomical study and clinical anal-
by the transoral route. ysis of 69 patients. J Neurosurg 90[Suppl 4]:206–219, 1999.
22. Samii M, Klekamp J, Carvalho G: Surgical results for meningiomas of the
The far lateral and extreme lateral atlanto-occipital transar-
craniocervical junction. Neurosurgery 39:1086–1095, 1996.
ticular approaches provide an alternative to the transoral ap- 23. Sen CN, Sekhar LN: An extreme lateral approach to intradural lesions of the
proach for exposure of extradural lesions in the CVJ. Both cervical spine and foramen magnum. Neurosurgery 27:197–204, 1990.
approaches avoid the contaminated nasopharynx and provide 24. Sen CN, Sekhar LN: Surgical management of anteriorly placed lesions at the
a shorter operative route. craniocervical junction: An alternative approach. Acta Neurochir (Wien)
108:70–77, 1991.
25. Ture U, Pamir MN: Extreme lateral-transatlas approach for resection of the
dens of the axis. J Neurosurg 96[Suppl 1]:73–82, 2002.
26. Verbiest H: A lateral approach to the cervical spine: Technique and indica-
REFERENCES tions. J Neurosurg 28:191–203, 1968.
27. Wen HT, Rhoton AL Jr, Katsuta T, de Oliveira EP: Microsurgical anatomy of
1. Al-Mefty O, Borba LA, Aoki N, Angtuaco E, Pait TG: The transcondylar the transcondylar, supracondylar, and paracondylar extensions of the far-
approach to extradural nonneoplastic lesions of the craniovertebral junction. lateral approach. J Neurosurg 87:555–585, 1997.
J Neurosurg 84:1–6, 1996.
2. Babu RP, Sekhar LN, Wright DC: Extreme lateral transcondylar approach:
Technical improvements and lessons learned. J Neurosurg 81:49–59, 1994. Acknowledgments
3. Baldwin HZ, Miller CG, van Loveren HR, Keller JT, Daspit CP, Spetzler RF: We thank Ronald Smith, M.S., Director, and David Peace, M.S., Medical
The far lateral/combined supra- and infratentorial approach: A human Illustrator, of the Microneuroanatomy Laboratory, Department of Neurological
cadaveric prosection model for routes of access to the petroclival region and Surgery, University of Florida, for constant support. We also thank Laura
ventral brain stem. J Neurosurg 81:60–68, 1994. Dickinson for assistance with preparation of the manuscript.
4. Bertalanffy H, Seeger W: The dorsolateral, suboccipital, transcondylar ap-
proach to the lower clivus and anterior portion of the craniocervical junc-
tion. Neurosurgery 29:815–821, 1991.
5. Crockard HA, Pozo JL, Ransford AO, Stevens JM, Kendall BE, Essigman
COMMENTS
WK: Transoral decompression and posterior fusion for rheumatoid atlanto-
axial subluxation. J Bone Joint Surg Br 68B:350–356, 1986.
6. de Oliveira EP, Rhoton AL Jr, Peace D: Microsurgical anatomy of the region
of the foramen magnum. Surg Neurol 24:293–352, 1985.
T his is a wonderful anatomic description of the craniocer-
vical junction (CCJ) focusing on how far all of the previ-
ously described surgical approaches can reach. In fact, there
7. George B, Laurian C: Surgical approach to the whole length of the vertebral are so many names that have been given to these surgical
artery with special reference to the third portion. Acta Neurochir (Wien)
techniques that one gets a little confused. However, consider-
51:259–272, 1980.
8. George B, Lot G: Anterolateral and posterolateral approaches to the foramen ing the anatomy of the CCJ, there are three main access points
magnum: Technical description and experience from 97 cases. Skull Base to it: 1) the posterior access, which is the standard midline
Surg 5:9–19, 1995. posterior approach and is the simplest, does not destroy im-
9. George B, Dematons C, Cophignon J: Lateral approach to the anterior portant structures but is limited to the posterior aspect of the
portion of the foramen magnum: Application to surgical removal of 14
benign tumors—Technical note. Surg Neurol 29:484–490, 1988.
CCJ; 2) the anterior access, which is the transoral approach
10. George B, Gauthier N, Lot G: Multisegmental cervical spondylotic myelop- with all its variants, is rather simple because in the depth of
athy and radiculopathy treated by multilevel oblique corpectomies without the mouth there are only small layers of mucosa and muscle
fusion. Neurosurgery 44:81–90, 1999. before one reaches the bone; however, it, too, is limited to the
11. George B, Lot G, Boissonnet H: Meningioma of the foramen magnum: A
midline; and 3) the lateral access, which is directed to the
series of 40 cases. Surg Neurol 47:371–379, 1997.
12. Hadley MN, Spetzler RF, Sonntag VKH: The transoral approach to the lateral wall of the CCJ and includes (from top of bottom) the
superior cervical spine: A review of 53 cases of extradural cervicomedullary jugular tubercle, occipital condyle, lateral mass of the atlas,
compression. J Neurosurg 71:16–23, 1989. and lateral part of the C2 vertebral body.
13. Heros RC: Lateral suboccipital approach for vertebral and vertebrobasilar The key structure in this approach is the vertebral artery (VA),
artery lesions. J Neurosurg 64:559–562, 1986.
14. Hitotsumatsu T, Rhoton AL Jr: Unilateral upper and lower subtotal maxil-
which courses around the lateral wall. To reach this lateral wall
lectomy approaches to the cranial base: Microsurgical anatomy. Neuro- and to expose the VA, there are two routes following two differ-
surgery 46:1416–1453, 2000. ent axes: one is posterior to the sternomastoid muscle, which

674 | VOLUME 53 | NUMBER 3 | SEPTEMBER 2003 www.neurosurgery-online.com


ATLANTO-OCCIPITAL TRANSARTICULAR APPROACH VARIANTS

gives access to the inside part of the bony canal, and the other is
anterior to the sternomastoid muscle and leads to the outside
part of the bony canal. Therefore, depending on the location of
K awashima et al. have provided us with another beauti-
fully illustrated demonstration of variants of surgical
approaches to the craniovertebral junction. This article pro-
the lesion, one route is preferred to the other. Another point that vides an excellent conceptual illustration of the variations
must be taken into account is the preservation of CCJ stability, of the transcondylar approach. I must admit that I have
whenever it is intact. This anatomic work by Kawashima et al. generally considered the two approaches presented by
demonstrates which structures can be reached by drilling these authors as a continuum rather than two separate
through the lateral wall of the CCJ. Obviously, both lateral ap- techniques with different nomenclature. Their comments
proaches can reach the odontoid process but with more or less regarding the difference in the soft tissue and muscle dis-
extensive drilling of the C0–C1 and/or C1–C2 joints; this should section for the two approaches are appreciated, because
be compared with any other approach that may respect stability. clearly the musculature can be an issue when trying to gain
Very often, when this question is raised, CCJ stability is already a more anterior and lateral exposure corridor. Certainly,
compromised and the surgical approach does not worsen the this article, along with its illustrations, should be required
problem. reading for residents and those unfamiliar with these ap-
When describing a lateral approach, I generally prefer to proaches before practice in the laboratory and attempting
refer to it as anterolateral or posterolateral and then describe such an exposure in the operating room.
the action performed (exposure, mobilization, or transposition
John D. Day
of the VA) and whether it is transatlantal, transcondylar, or
Pittsburgh, Pennsylvania
both. This indicates exactly which axis of work through which
structure has been used. In the present article, I often got lost
and had to return to the definition of each term (transcondy-
lar, far, extreme lateral, etc.).
K awashima et al. have provided a detailed description of
the far and extreme lateral approaches to the cranioverte-
bral junction. In addition to a detailed anatomic description,
Finally, as stated in this article and as already demonstrated the typical surgical pitfalls of each approach are discussed. An
by several clinical reports, the lateral approach may be a good important disadvantage of both approaches compared with
alternative to the transoral approach. However, most surgeons transoral procedures is the possible need for stabilization. An
need some time to become comfortable with these approaches advantage is the wide and sterile exposure near the surgeon’s
because there are several technical points (essentially VA con- view. The advantage of vertebral artery control is obscured by
trol) that require training. The main technical point in VA the need for vessel manipulation with medial exposure. The
exposure and control is subperiosteal dissection to keep the advantage of the extreme lateral approach compared with the
periosteal sheath surrounding the VA and its venous plexus far lateral one is contralateral accessibility, to reduce the need
intact. This article is a nice adjunct that should help anyone for manipulation of major vessels and nerves, such as the
starting with these techniques to better understand the com- internal jugular vein and the accessory nerve.
plex anatomy of this region. It is important to bear in mind that the transoral approach
has the advantage of a midline approach with access to both
Bernard George
sides. The authors should ask themselves how a cerebro-
Paris, France
spinal fluid leak could be a risk in a transoral approach to

T he approach to extradural lesions anterior to the craniover-


tebral junction evokes vigorous debate. There are strong pro-
ponents for the anterior transoral approach and the lateralized
purely extradural lesions of the craniovertebral junction. It
is highly questionable to draw conclusions from cadaver
studies regarding the suitability of such extensive ap-
extrapharyngeal approaches. For surgeons opting for the latter, proaches with the need for vessel exposure and postopera-
Kawashima et al. have produced an article that clearly describes tive stabilization.
and demonstrates, with excellent figures, two lateralized ap- The authors should present clinical examples in which such
proaches to the anterior craniovertebral junction, the far lateral extensive approaches with drilling of the condyles are justi-
and extreme lateral approaches. They further contrast the utility fied. It should be pointed out that each lesion in this area
of each approach and demonstrate the strengths and weaknesses should be addressed using the approach with the most mini-
of each approach. Anatomic information and recognition are mal resulting morbidity, and, if possible, the neurosurgeon
highly critical for these approaches, and this article makes a should apply an approach with a familiar orientation, as the
significant contribution to our knowledge. authors have done.

Jason A. Heth Wolf Lüdemann


Ossama Al-Mefty Madjid Samii
Little Rock, Arkansas Hannover, Germany

NEUROSURGERY VOLUME 53 | NUMBER 3 | SEPTEMBER 2003 | 675

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