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SURGICAL ANATOMY Surgical Anatomy and Technique

Victor A. Morera, MD
Department of Neurological Surgery,
University of Pittsburgh School of
Medicine,
Pittsburgh, Pennsylvania
Far-Medial Expanded Endonasal Approach to
Juan C. Fernandez-Miranda, MD
Department of Neurological Surgery,
University of Pittsburgh School of
the Inferior Third of the Clivus: The Transcondylar
Medicine,
Pittsburgh, Pennsylvania
and Transjugular Tubercle Approaches
Daniel M. Prevedello, MD
Department of Neurological Surgery, OBJECTIVE: The endoscopic endonasal transclival approach is a valid alternative for treat-
University of Pittsburgh School of ment of lesions in the clivus. The major limitation of this approach is a significant lateral
Medicine,
Pittsburgh, Pennsylvania extension of the tumor. We aim to identify a safe corridor through the occipital condyle
to provide more lateral exposure of the foramen magnum.
Ricky Madhok, MD
Department of Neurological Surgery, METHODS: Sixteen parameters were measured in 25 adult skulls to analyze the exact
University of Pittsburgh School of extension of a safe corridor through the condyle. Endonasal endoscopic anatomic dissec-
Medicine,
Pittsburgh, Pennsylvania
tions were carried out in nine colored latexinjected heads.
Juan Barges-Coll, MD
RESULTS: Drilling at the lateral inferior clival area exposed two compartments divided by
Department of Neurological Surgery, the hypoglossal canal: the jugular tubercle (superior) and the condylar (inferior). Completion
University of Pittsburgh School of of a unilateral ventromedial condyle resection opens a 3.5 mm (transverse length) 10
Medicine,
Pittsburgh, Pennsylvania
mm (vertical length) lateral surgical corridor, facilitating direct access to the vertebral artery
at its dural entry point into the posterior fossa. The supracondylar groove is a reliable land-
Paul Gardner M.D mark for locating the hypoglossal canal in relation to the condyle. The hypoglossal canal
Department of Neurological Surgery,
University of Pittsburgh School of is used as the posterior limit of the condyle removal to preserve more than half of the
Medicine, condylar mass. The transjugular tubercle approach is accomplished by drilling above the
Pittsburgh, Pennsylvania
hypoglossal canal, and increases the vertical length of the lateral surgical corridor by 8
Ricardo Carrau, MD mm, allowing for visualization of the distal cisternal segment of the lower cranial nerves.
Neuroscience Institute,
John Wayne Cancer Institute at
CONCLUSION: The transcondylar and transjugular tubercle far medial expansions of the
Saint John's Health Center, endoscopic endonasal approach to the inferior third of the clivus provide a unique surgi-
Santa Monica, California cal corridor to the ventrolateral surface of the ponto- and cervicomedullary junctions.
Carl H. Snyderman MD KEY WORDS: Clivectomy, Condylectomy, Endoscopic, Endonasal, Skull base tumor
Department of Neurological Surgery
and Department of Otolaryngology,
Neurosurgery 66[ONS Suppl 2]:ons211-ons220, 2010 DOI: 10.1227/01.NEU.0000369926.01891.5D
University of Pittsburgh School of
Medicine,
Pittsburgh, Pennsylvania

B
Albert L. Rhoton Jr, MD y using the endonasal endoscopic transcli- morphometric analysis of the hypoglossal canal,
Department of Neurological Surgery,
University of Florida,
val approach we gained progressive access occipital condyle, and foramen magnum to ana-
Gainesville, Florida to the anterior portion of the foramen mag- lyze the exact extension of a safe corridor through
num and the inferior third of the clivus from a the condyle in an endonasal endoscopic approach.
Amin B. Kassam, MD
Department of Neurological Surgery
medial-to-lateral trajectory.1 The major limita-
and Department of Otolaryngology, tion of this approach is a significant lateral exten- MATERIALS AND METHODS
University of Pittsburgh School of sion of the tumor toward the occipital condyle.
Medicine, Standard calipers were used to measure 16 parame-
Pittsburgh, Pennsylvania
Just s a dorsomedial condyle resection added to
the lateral suboccipital approach allows for a more ters from 25 adult skulls of unknown gender to analyze
Reprint requests:
medial surgical trajectory, 2-4 a ventromedial the exact extension of a safe surgical corridor through
Daniel M. Prevedello, MD, the occipital condyle (Figure 1); (Table). Nine cadav-
Department of Neurological Surgery, condyle resection added to the inferior transcli-
eric specimens were prepared for dissection at the neu-
200 Lothrop Street, PUH B400, val approach allows for a more lateral surgical roanatomy laboratory of the Neurosurgical Department
Pittsburgh, PA 15213.
E-mail: dprevedello@gmail.com
corridor.5 We complete an anatomic study and at the University of Pittsburgh School of Medicine. The
common carotid arteries, vertebral arteries, and inter-
Received, August 4, 2009. ABBREVIATIONS: AID, anterior intercondylar dis- nal jugular veins were isolated, cannulated with flexi-
Accepted, January 11, 2010. tance; EETA, endoscopic endonasal transclival
ble tubing, and dyed with red or blue water-soluble
approach; FM, foramen magnum; HC, hypoglossal
Copyright 2010 by the pigments using previously described methods.6 Endonasal
canal; JT, jugular tubercle; OC, occipital condyle
Congress of Neurological Surgeons anatomic dissections were carried out using rod lens

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MORERA ET AL

A B FIGURE 1. Cadaveric skull photographs


showing measurements of the clivus,
foramen magnum (FM), and occipital
condyles (OCs). A, inferoposterior view.
The transverse diameter of the FM is, on
average, 32 mm. The endoscopic endonasal
transclival approach (EETA) is bordered
inferior and laterally by the anterior por-
tion of the OC (AID), limiting the infe-
rior opening to 19 mm. The bilateral
transcondylar supra-articular approach
maximizes exposure to the FM to 26 mm
(the distance between the two inner bor-
ders of the HC). B, anterior view of the
clivus. A, distance from the sellar floor to
the basion; B, distance from the hypoglos-
C D sal canal (HC) to the jugular tubercle
(JT); C, distance between HCs (extracra-
nial); D, AID; E, transverse diameter of
the FM. C, right lateral view of clivus
and occipital condyle. F, distance from
the inferior margin of the HC to the infe-
rior margin of the OC; G, anteroposterior
length of the OC; H, transverse width of
the OC. D, inferolateral view of the fora-
men magnum and the occipital condyles.
I, distance between HC and basion; J,
distance from the anterior margin of the
HC to the anterior margin of the OC;
K, intracranial diameter of the HC.

endoscopes (Karl Storz, 4 mm, 18 cm, Hopkins II) attached to a high- 19 mm (Figures 1A and B, 3B). This demonstrates the natural
definition camera for visualization. convergence of exposure as one approaches the foramen magnum
when performing an inferior clival resection. If more lateral expo-
RESULTS sure is needed inferiorly, particularly for vertebral artery control,
then a condyle resection is necessary.
The surgical approach and our anatomic study are divided into Once the ventral inferior clivus is drilled, the underlying dura
two anatomosurgical stages: the endonasal endoscopic inferior mater and its basilar venous plexus are exposed (Figure 3A).
transclival approach and the far-medial expanded endonasal After opening the dura, the premedullary and inferior portions
inferior transclival approach. of the prepontine and lateral cerebellomedullary cisterns come
into direct view. The lateral dural opening at the level of the
Expanded Endonasal Inferior Transclival Approach lacerum segment of the ICA should be performed under direct
After general exposure is obtained, the mucosal and muscular subdural visualization, because the abducens nerve pierces the dura
layers at the posterior wall of the nasopharynx are removed to expose at this level and travels in the interdural space to enter Dorellos
the basopharyngeal fascia (Figure 2A-C). Once the basopharyngeal canal just superior, and dorsal to the anterior genu of the carotid
fascia is elevated from the inferior ventral clivus, and the longus artery.
capitis, rectus capitis anterior, and anterior atlanto-occipital mem- The sequence for intradural dissection in this segment begins
brane are exposed and resected (or reflected laterally), the ante- with the identification of the vertebral arteries along their cister-
rior ring of C1, capsule of the atlanto-occipital joint, and apical nal course up to the vertebrobasilar junction (VBJ) at the pon-
ligament are exposed (Figure 2D). tomedullary junction (Figures 6B and 7). The abducens nerve can
The clivus is drilled from the floor of the sphenoid sinus to the be identified immediately rostral to the VBJ bilaterally.
basion, for an average distance of 28 mm (Table). The superolat-
eral limit of the inferior clival resection is located between the two Far-Medial Expanded Endonasal Inferior
lacerum segments of the internal carotid artery (ICA), which are, Transclival Approach
on average, 21 mm apart (Figure 3A and B). The inferolateral Once the standard inferior clivectomy is completed, its lateral
limit is located between the occipital condyles (anterior inter- extension is attempted. To gain exposure of the occipital condyle
condylar distance), which are separated by an average distance of it is necessary to remove part of the capsule of the atlanto-occipital

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ENDONASAL ENDOSCOPIC FAR-MEDIAL APPROACH

labyrinthine arteries also are visualized along their course toward


TABLE. Morphometric Study: Results of Measurementsa the internal acoustic meatus (Figure 7E).
Right, Left, Mean, The rootlets that form the hypoglossal nerve arise from the
Measurement medulla in the pre-olivary sulcus and direct forward and laterally
mm mm mm
through the subarachnoid space, passing behind the vertebral
Extracranial diameter of HC 6 6 6
artery to reach the hypoglossal canal. The inner and outer orifices
Intracranial diameter of HC 5 6 5,5
of the hypoglossal canal are oval in shape, and the distance between
Distance from the HC to JT 8.1 7.4 8 the two inner borders of the hypoglossal canal averages 26 mm,
Distance between HC and opisthion 28 29.6 28 which is the narrowest space of the lateral extension of the endo-
Distance between HC and basion 15.1 14.6 14.8 scopic transclival approach.
Distance from posterior margin of 10.1 10 10 The condylar compartment is located caudal to the hypoglos-
HC to posterior margin of OC sal canal. The inferior limit of the condyle resection is formed by
Distance from anterior margin of 11 11.6 11.3 the articular surface (Figure 3C and D). The mean height of this
HC to anterior margin of OC compartment is 10 mm. Intradurally, the occipital condyle is in
Distance from inferior margin of 10.7 9 10 close relationship with the vertebral artery, and medial condyle
HC to inferior margin of OC resection provides access to the vertebral artery at its dural entry
Distance beteween HCs (intracranial) 26
point into the posterior fossa (Figure 6C and D).
Distance between HCs (extracranial) 33.9
Anteroposterior length of OC 24.5 24 24 DISCUSSION
Transverse width of OC 12.5 15 14 With the expanded endonasal approach, the cranial base sur-
Anterior intercondylar distance 19 geon can access the entire cranial base from all 360 degrees of
Posterior intercondylar distance 35.1 approach using a combination of conventional open and endonasal
Distance from sellar floor to basion 27.8 approaches. Selecting the specific approach (or approaches) may
Transverse diameter of FM 32 then be based on the individual patients anatomic and clinical con-
siderations.1,7-9
a
HC, hypoglossal canal; JT, jugular tubercle; OC, occipital condyle; FM, foramen mag- When a lesion is located anterior to the brainstem (eg, midline
num.
lesions located in the ventral foramen magnum, lower clivus, and
ventral aspect of the craniocervical junction), distortion and pos-
joint. This exposes an important osseous groove on the upper sur- terior displacement of the brainstem and lower cranial nerves may
face of the condyle formed by the insertion of the rectus capitis pose a challenge with lateral or posterolateral cranial base approaches
anterior muscle, anterior atlanto-occipital membrane, and capsule (ie, lateral suboccipital, far lateral, retrolabyrinthine presigmoid
joint. This supracondylar groove provides a reliable landmark for approaches, or a combination). The lateral-to-medial trajectory
estimating the position of the hypoglossal canal and its external ori- provided by these approaches requires manipulation of neurovas-
fice, which are situated just posterior and lateral to the groove, cular structures to reach the ventral midline region.
respectively (Figures 3C and D, 4 C and D, and 5D) The expanded endonasal transclival approach (EETA) permits
Drilling at the lateral inferior clival area at the level of the access to clival and foramen magnum lesions via a medial-to-
supracondylar groove leads to the anterior cortical wall of the lateral trajectory, providing a direct route into the lesion. EETA
hypoglossal canal. The hypoglossal canal divides the lateral infe- provides several advantages over the conventional lateral open cra-
rior clival area into two compartments: tubercular (superior) nial base approaches that may minimize the approach-related
and condylar (inferior) (Figures 3D, 6B, and 7A). The tubercu- morbidity of conventional techniques: (1) no need to manipu-
lar compartment, located superior to the hypoglossal canal, is late structures located circumferentially along the perimeter; (2)
the ventral representation of the jugular tubercle (Figure 7Band a wider viewing angle; and (3) no manipulation of the vertebral
C); the lateral limit of this compartment is the medial edge of the artery. Finally, in contrast to most lateral approaches via the mid-
jugular foramen, and its most rostral point is located at the level dle or posterior fossa, it is not necessary to open the dura of the
of the pontomedullary junction. The height of this compart- cranial base to reach extradural tumors, which may reduce the
ment is, on average, 8 mm. Intradurally, the tubercular com- risk of damage to brain tissue via retraction, as well as damage to
partment has a close anatomic relationship in its posterior surface vital vascular structures such as the vein of Labbe.1,5,7,8,10-12
with cranial nerves IX, X, and XI on their way toward the jugu- EETA has some advantages over the conventional anterior
lar foramen. In its medial aspect, the tubercular compartment is approaches as well: (1) it is a fully endoscopic procedure so the
related to the vertebral artery (Figure 7C and E). After extradural self-retaining retractor is not necessary; (2) it allows extra- and
reduction of the jugular tubercle is performed, it is possible to intradural space access to the ventral skull base from the crista
explore the inferolateral portion of the cerebellopontine cistern galli to the craniocervical junction; and (3) it also provides great
with a 45-degree endoscope from a premeatal route. The illuminating power and the ability to look around corners.9 Because

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A B

FIGURE 2. Stepwise illustration of the


general exposure for the EETA. A, the
inferior and middle turbinates project
medially from the lateral nasal wall.
The lower 1 to 2 cm of the posterior
nasal septum was resected, and a sphe-
noidotomy was performed. B, the
eustachian tube, basopharyngeal fas-
cia, and soft palate are identified. C,
the mucosal layer and superior constric-
tor muscle at the posterior wall of the
nasopharynx have been removed to
expose the prevertebral muscles. This
maneuver exposes the longus capitis and
rectus capitis anterior muscles. D, The
C D prevertebral muscles have been removed
to expose the inferior clivus and the
anterior arch of C1. The petroclival
synchondrosis was uncovered. Ant.,
anterior; Basipharyn., basopharyngeal;
Cap., capitis; Eusta., eustachian; Fasc.,
fascia; For., foramen; Inf., inferior;
Long., longus; M., muscle; Midd., mid-
dle; Rect., rectus; Spheno., Sphenoid;
Sphenopetr., sphenopetrous; Turbin.,
turbinate.

it is an endonasal corridor, it does not transgress the oropharynx hypoglossal canal; the amount of condyle resection; and alar lig-
and soft palate, so the surgical field will be exposed to less bacte- ament involvement.
rial contamination, potentially decreasing the risk of infection
risk. Additionally, patients have less postoperative swallowing dys- Relation Between Occipital Condyle and
function, have a decreased risk of hypernasal speech and nasal Parapharyngeal Internal Carotid Artery
regurgitation, are able to be fed orally immediately after the pro- The usual anatomic course of the parapharyngeal ICA is pos-
cedure without the risks of palatal and pharyngeal dehiscence or terolateral to the pharyngeal wall and lateral to the occipital
dysphagia, and avoid facial osteotomies and cosmetically unsatis- condyle. However, parapharyngeal ICA variations have been found
factory incisions.1,5,7, 8,10,13, in 10 to 40% of the population, typically bilaterally.15 Parapharyngeal
Finally, with the development of a nasoseptal flap, the rate of ICA anomalies may place the vessel into close opposition with
cerebrospinal fluid leakage has been reduced to 5.4% after endo- the superior pharyngeal constrictor muscle and Rosenmllers
scopic endonasal intradural cranial base surgery.14 fossa. Therefore, the course of the parapharyngeal ICA course
The endonasal corridor is contraindicated, however, when the should be carefully investigated with CT angiography when plan-
critical neurovascular structures are located medial or ventral to the ning any access to the lower third of the clivus. This is particu-
tumor, requiring their manipulation before entering the lesion. A larly important in older patients who have higher incidence of
relative contraindication to this procedure is a significant lateral ICA anomalies probably based on degenerative changes in the
extension of the tumor at the level of the foramen magnum behind vessel wall secondary to age-related loss of elasticity, artheroscle-
the occipital condyle, because there is risk of injury to the lower cra- rosis, or hypertension.16
nial nerves and of craniocervical junction instability.1,7
For accessing the lateral aspect of the inferior clivus, we pro- Safe Entry Zone Through the Occipital Condyle:
pose the use of a transcondylar or transjugular tubercle approach. Infra-Hypoglossal Canal
Several factors should be considered to safely perform these sur- The external surface of the condylar pars of the occipital bone
gical extensions: the anatomic relationship between the occipi- has a distinctive groove, the supracondylar groove, which is an excel-
tal condyle and the parapharyngeal ICA; the location of the lent landmark for identifying the superior limit of the hypoglossal

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ENDONASAL ENDOSCOPIC FAR-MEDIAL APPROACH

A B FIGURE 3. Stepwise exposure of the


EETA and EETA transcondylar transtu-
bercular approaches. A, the clivus has
been drilled. The superolateral limit of
the inferior EETA is located between the
two lacerum segments of the carotid
artery. The inferolateral limit is located
between the two occipital condyles. Once
the ventral inferior clivus is drilled out,
the underlying dura mater and its basi-
lar venous plexus are exposed. The ante-
rior arch of C1 is positioned at level of the
soft palate. B, the capsule of the left
atlanto-occipital joint has been removed.
The OC is situated behind Rosenmllers
fossa. C, a left anterior transcondylar
C D approach has been performed. The supra-
condylar groove and the lateral pharyn-
geal tubercle have been exposed. D,
medial view of the occipital condyle.
Drilling at the lateral inferior clival area
and using the supracondylar groove as a
reference, the anterior cortical wall of
the hypoglossal canal is exposed. The
hypoglossal canal divides the lateral cli-
val area into two compartments: tuber-
cular or superior and condylar or inferior.
The tubercular compartment (TC) is
located superior to the hypoglossal canal
and is the ventral representation of the
jugular tubercle. The lateral limit of this
compartment is at the medial edge of the
jugular foramen, and its most rostral
E F point is located at the level of the pon-
tomedullary junction. Once the cortical
layer of bone of the OC is removed, the
soft cancellous bone is encountered; fur-
ther drilling exposes another cortical layer
of bone superiorly, the HC. The inferior
limit of the condylectomy is formed by
the articular surface; therefore, the alar
ligament attachment is not disrupted.
Bilateral transcondylar (E) and transtu-
bercular (F) approaches have been made.
A., artery; Ant., anterior; Ap., approach;
Comp., compartment; Condy., condyle;
Eusta., eustachian; F., fossa; For., fora-
men; Hypogl., hypoglossal; Lat., lateral;
Lig., ligament; Occip., occipital; Pharyn.,
pharyngeal; Rosenm., Rosenmllers fossa; Supracondy, supracondylar; Transcondy., transcondylar; Transtuberc., transtubercular; Tuberc., tubercle.

canal. (Figures 3D and 4 A, B, C) The supracondylar groove has drilling inferior to this groove without damaging CN XII. This
not been described before, although it has been successfully used surgical maneuver provides an additional 10 mm of height in the
intraoperatively at our institution. The hypoglossal canal is situ- operative corridor (Figures 3C and D).
ated posterior to the level of the supracondylar groove, with its
outer orifice located lateral to the level of the supracondylar groove Amount of Condyle Resection
(Figure 3). The distance between the supracondylar groove and Although no biomechanical studies have been performed address-
the articular surface of the occipital condyle averages 10 mm. ing the stability of the atlanto-occipital joint after ventromedial
Therefore, the ventromedial condyle resection can be completed by condyle resection, statistically significant hypermobility is pro-

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MORERA ET AL

A B FIGURE 4. Anterior view of the clivus


and occipital condyle. A, the external sur-
face of the condylar pars of the occipital
bone has a groove, the supracondylar
groove, on which the anterior rectus capi-
tis muscle and atlanto-occipital capsule
attach. The hypoglossal canal is situated
behind the supracondylar groove, and its
outer orifice is located lateral to the SG.
This groove is an excellent landmark for
identifying the hypoglossal canal. B, the
mucosal layer and superior constrictor
muscle at the posterior wall of the naso-
pharynx have been removed. The right
C D longus capitis muscle has been removed
to expose the lateral pharyngeal tubercle.
C, the prevertebral muscles have been
removed to expose the right occipital
condyle, the ipsilateral supracondylar
groove, the lateral pharyngeal tubercle,
and the pharyngeal tubercle. D, intra-
operative view with a 0-degree endoscope
showing the supracondylar groove, the
foramen magnum, and the right occipi-
tal condyle. Ant., anterior; Cap., capitis;
Condy., condyle; Eusta., eustachian; F.,
foramen; Hypogl., hypoglossal; Lat., lat-
eral; Long., longus; Occip., occipital;
Pharyn., pharyngeal; Rect., rectus; Supra-
condy, supracondylar; Tuberc., tubercle.

duced at the atlanto-occipital joint after more than 50% of the inferior limit of the ventromedial condyle resection. If only one
dorsomedial condyle is resected.17 In our study, the mean antero- alar ligament must be resected, stability may be preserved. If infe-
posterior length of the occipital condyle was 24 mm, and the rior extension is necessary, including removal of the anterior arch
mean distance of the intracranial part of the hypoglossal canal to of C1, the odontoid process, and the bilateral alar ligaments, spe-
the anterior margin of the occipital condyle was 11 mm, show- cial attention should be paid to craniocervical instability, and
ing that the hypoglossal canal is strategically located at the midlevel fusion should be considered.
of the condyle in the anteroposterior axis (Figure 5A). Therefore,
the anterior cortical layer of bone of the hypoglossal canal should Transcondylar and Transjugular Tubercle Approaches
mark the maximum anteroposterior extent of condyle removal if The far-medial extension of an expanded endoscopic endonasal
more than 50% of the condyle is to be preserved (Figures 3E, 5B approach to the inferior third of the clivus has two variants: (1) the
and 5C). The hypoglossal canal is a reliable landmark to use to transcondylar supra-articular approach (unilateral or bilateral)
determine the posterior limit of the ventromedial condyle resec- and (2) the transjugular tubercle approach (unilateral or bilateral;
tion (Figure 5A and B). Figure 3C, E, and F). The standard endoscopic endonasal approach
to the inferior third of the clivus has a trapezoid shape, deter-
Alar Ligament Insertion mined by the narrower space between the condyles inferiorly. The
Panjabi et al found that alar ligament transection causes an inferolateral border of this corridor is formed by the anterior por-
increase in neutral zone and range of motion in both atlanto- tions of the occipital condyles, which limit the transverse length
occipital and atlantoaxial angular motion.18,19 Therefore, much of of the inferior opening to 19 mm (59% of the transverse length
the passive stabilization of atlanto-occipital and atlantoaxial joint of the foramen magnum). A unilateral ventromedial condyle
comes from the alar ligaments.18,19 It is possible to drill the can- removal can increase the inferior opening of the endoscopic
cellous bone of the condyle to expose the anterolateral portion of endonasal inferior transclival approach to 22.5 mm (70% of the
the foramen magnum while preserving some of the cortical bone transverse length of the foramen magnum; Figure 3C), and a bilat-
of the condyle articular surface (ie, supra-articular condyle resec- eral condyle resection maximizes exposure of the foramen magnum
tion). As a result, the alar ligament attachment is not disrupted to 26 mm (81% of the transverse length of the foramen magnum)
(Figure 3D). The attachment of the alar ligament determines the without transgressing the hypoglossal canals (Figure 3E). Addi-

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ENDONASAL ENDOSCOPIC FAR-MEDIAL APPROACH

A B FIGURE 5. Posterior limit of the medial


condylectomy. A and B, inferolateral
views of the foramen magnum and the
occipital condyles. The mean anteropos-
terior length of the occipital condyle (OC)
is 24 mm. The mean length of the
intracranial part of the hypoglossal canal
to the anterior margins of the OC is 11
mm (it represents 46% of the anteropos-
terior length of the OC); therefore, the
hypoglossal canal is a landmark to deter-
mine the posterior limit of the anterior
condylectomy. Endoscopic endonasal view
C D using a 45-degree endoscope (C) and a 0-
degree endoscope (D) illustrating a left
transcondylar transclival approach. Note
that the long axis of the occipital condyles
is directed from anteromedial to postero-
lateral, and, therefore, the occipital condyles
can be removed safely by drilling in this
direction (white and black arrows), until
the cortical layer of bone of the HC is
encountered. A., artery; Ant., anterior;
Ap., approach; Condy., condyle; F., fossa;
Hypogl., hypoglossal; Lat., lateral; Occip.,
occipital; Pharyn., pharyngeal; Rosenm.,
Rosenmllers fossa; supracondylar;
Transcondy., transcondylar; Tuberc.,
tubercle.

tionally, a ventromedial condyle resection provides an operative cor- tral or ventrolateral foramen magnum meningiomas, chordo-
ridor 10 mm greater in height in the inferolateral aspect of the mas, and chondrosarcomas.
clivus when compared with the standard transclival approach.
Completion of removal of the condyle provides a better visualiza- CONCLUSION
tion of the vertebral artery at its dural entry point into the poste-
rior fossa, allowing for proximal vascular control in case of bleeding. The far-medial expanded endonasal inferior transclival approach
In contrast to the dorsomedial condyle resection, when exposing allows maximization of exposure of the foramen magnum from
lesions located along the anterior portion of the upper cervical 59% (conventional endoscopic endonasal approach for the infe-
cord and cervicomedullary junction, the ventromedial condyle rior third of the clivus) to 70%. It also provides access to the ver-
resection and superior facetectomy of C1 can be accomplished tebral artery, allowing for proximal vascular control. Additional
without the need to retract or mobilize the vertebral artery, because superior extension of this lateral corridor can be obtained with
it is located behind the condyle. the transjugular tubercle approach, which provides visualization
Additional lateral exposure can be obtained by drilling the of the distal cisternal segment of the lower cranial nerves. These
tubercular compartment above the hypoglossal canal. In this modifications offer a lateral operative corridor that the conven-
ventromedial transjugular tubercle approach, the medial por- tional transclival approach does not. If the amount of condylar
tion of the jugular tubercle, which is located just above the resection is less than 50%, the articular surface is preserved, and
hypoglossal canal, is removed extradurally without manipula- the alar ligament attachment is not disrupted, fusion of the cran-
tion of the lower cranial nerves or mobilization of the sigmoid iocervical junction may not be necessary.
sinus. This approach increases the lateral surgical corridor by 8
mm in the vertical axis, and when this is combined with the Disclosures
transcondylar approach, a valuable 18-mm vertical surgical win- Dr. Kassam, Dr. Prevedello is a paid consultant for Stryker Corporation. A.K.,
dow is opened (Figure 3E and F). Once the jugular tubercle is Dr. Snyderman, and Dr. Carrau are paid consultants for Stryker and Karl Storz
Corporations. Dr. Kassam has equities in the NICO Corporation. The study was
removed, direct visualization of the lower cranial nerves just performed with a grant support of the Walter L. Copeland Fund of the Pittsburgh
before their entrance into the jugular foramen is obtained. This Foundation. The other authors have no personal financial or institutional inter-
exposure is a critical issue when dealing with lesions such as ven- est in any of the drugs, materials, or devices described in this article.

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A B FIGURE 6. Endoscopic view using a


0-degree endoscope. A and B, after
opening the dura, the premedullary,
inferior portion of the prepontine and
lateral cerebellomedullary cisterns comes
into direct view. The sequence for
intradural dissection in this segment
begins with the identification of the
vertebral arteries along their cisternal
course up to the vertebrobasilar junc-
tion (VBJ) at the pontomedullary junc-
tion. The abducens nerve can be
identified right above the VBJ bilat-
erally. The origin of the posteroinferior
cerebellar arteries and anterior spinal
artery was visible in the lateral cere-
bellomedullary cistern and premedullary
C D cistern, respectively. C, the hypoglossal
canal (HC) was completely surrounded
and protected by cortical bone. The
rootlets forming the hypoglossal nerve
arise from the medulla in the pre-oli-
vary sulcus and direct forward and lat-
erally through the subarachnoid space,
and pass behind the vertebral artery to
reach the HC. As it passes into the HC,
the hypoglossal nerve is surrounded by
the hypoglossal venous plexus. D, intra-
operative view with a 0-degree endo-
scope of the close relation between the
occipital condyle and the vertebral
artery. The dura of the clivus was
opened. Completion of the anterior
condylectomy provided better visuali-
zation of the intradural segment of the vertebral artery at its dural entry point into the posterior fossa. A very important anatomic relationship to determine C1
and XII rootlets in surgery is the intradural segment of the VA, which is behind the C1 and in front of the hypoglossal nerve. A., artery; AICA, anterior inferior
cerebellar artery; Ant., anterior; CN, cranial nerve; Condy., condyle; Hypogl., hypoglossal; Jug., jugular; Medu., medulla; Oblon., oblongata; Occip., occipital;
Pl., plexus; Spin., spinal; Tuberc., tubercle; Ven., venous; Vert., vertebral.

REFERENCES 8. Kassam AB, Snyderman CH, Mintz A, Gardner P, Carrau RL. Expanded endonasal
approach: the rostrocaudal axis. Part II. Posterior clinoids to the foramen mag-
1. Kassam AB, Snyderman C, Gardner P, Carrau R, Spiro R. The expanded endonasal num. Neurosurg Focus. 2005;19(1):E4.
approach: a fully endoscopic transnasal approach and resection of the odontoid 9. Kassam AB, Snyderman CH, Mintz A, Gardner P, Carrau RL. Expanded endonasal
process: technical case report. Neurosurgery. 2005;57[ONS Suppl 1]:ONS213- approach: the rostrocaudal axis. Part I. Crista galli to the sella turcica. Neurosurg Focus.
ONS214. 2005;19:E3.
2. Arnautovic KI, Al-Mefty O, Husain M. Ventral foramen magnum meningiomas. 10. De Divitiis E, Cavallo LM, Esposito F, Stella L, Messina A. Extended endoscopic
J Neurosurg. 2000;92(1 Suppl):71-80. transsphenoidal approach for tubercle sellae meningiomas. Neurosurgery. 2007;61[ONS
3. Rhoton A. The far-lateral approach and its transcondylar, supracondylar, and para- Suppl 2]:ONS229-ONS238.
condylar extensions. Neurosurgery. 2000;47(3):S195-S209. 11. Kyoshima K, Matsuo K, Kushima H, Oikawa S, Idomari K, Kobayashi S. Degloving
4. Muthukumar N, Swaminathan R, Venkatesh G, Bhanumathy SP. A morphomet- transfacial approach with Le Fort I and nasomaxillary osteotomies: Alternative
transfacial approach. Neurosurgery. 2002;50:813-821.
ric analysis of the foramen magnum region as it relates to the transcondylar approach.
12. Wu J, Huang W, Cheng H, et al. Endoscopic transnasal transclival odontoidec-
Acta Neurochir (Wien). 2005;147:889-895.
tomy: A new approach to decompression: technical case report. Neurosurgery.
5. Kassam AB, Mintz HA, Gardner PA, Horowitz MB, Carrau RL, Snyderman CH.
2008;63[ONS Suppl 1]:ONSE94-ONSE96.
The expanded endonasal approach for an endoscopic transnasal clipping and 13. Nayak JV, Gardner PA, Vescan AD, Carrau RL, Kassam AB, Snyderman CH.
aneurysmorrhaphy of a large vertebral artery aneurysm: technical case report. Experience with the expanded endonasal approach for resection of the odontoid process
Neurosurgery. 2006;57[ONS Suppl 1]:ONS162-ONS165. in rheumatoid disease. Am J Rhinol. 2007;21(5):601-606.
6. Fortes FSG, Sennes LU, Carrau RL, et al. Endoscopic anatomy of the pterygopala- 14. Kassam AB, Thomas A, Carrau RL, et al. Endoscopic reconstruction of the cra-
tine fossa and the transpterygoid approach: development of a surgical instruction nial base using a pedicle nasoseptal flap. Neurosurgery. 2008;63[ONS Suppl
model. Laryngoscope. 2008;118:44-49. 1]:ONS44-ONS53.
7. Dehdashti AR, Karabatsou K, Ganna A, Witterick I, Gentili F. Expanded endo- 15. Paulsen F, Tillmann B, Christofides C, Ritcher W, Koebk J. Curving and looping
scopic endonasal approach for treatment of clival chordomas: early results in 12 of the internal carotid artery in relation to the pharynx: frequency, embryology
patients. Neurosurgery. 2008;63:299-309. and clinical implications. J Anat. 2000;197:373-381.

ons218 | VOLUME 66 | OPERATIVE NEUROSURGERY 2 | JUNE 2010 www.neurosurgery-online.com


ENDONASAL ENDOSCOPIC FAR-MEDIAL APPROACH

A B FIGURE 7. Endoscopic endonasal view


using a 45-degree endoscope in the
right transclival transcondylar transtu-
bercular approach. A, once the stan-
dard inferior clivectomy is completed,
its lateral extension is performed. The
hypoglossal canal divides the lateral
clival area into two compartments:
tubercular or superior and condylar
or inferior. Endoscopic view using
0-degree (C) and 45-degree (D) endo-
scopes of the right tubercular compart-
ment. The tubercular compartment is
located superior to the hypoglossal canal
and is the ventral representation of the
jugular tubercle; its most rostral point
C D is located at the level of the ponto -
medullary junction. The tubercular
compartment has close anatomic rela-
tionships in its posterior surface with
CN IX, X, and XI on their way toward
the jugular foramen. In its medial
aspect, the TC is related to the verte-
bral artery. D and E, the tubercular
compartment has been removed
(transtubercular approach). Using a
45-degree endoscope, it was possible to
explore the cerebellopontine cistern from
a premeatal route. Along the course of
the anteroinferior cerebellar artery, CN
VII and VIII were identified and fol-
lowed along their free cisternal course
to the internal acoustic meatus. It also
E was possible to visualize the labyrinthine
arteries in their course toward the inter-
nal acoustic meatus. Using the same
endoscope, the upper part of the cerebel-
lopontine angle was explored, and the
trigeminal nerve was seen along its
course from the pons toward Meckels
cave. A., artery; AICA, anterior infe-
rior cerebellar artery; Ap., approach;
CN, cranial nerve; Comp., compart-
ment; Hypogl., hypoglossal; PICA, pos-
terior inferior cerebellar artery; Flocc.,
flocculus; Ple., plexus; Transtuberc.,
transtubercular; Tuberc., tubercle; Ven.,
venous; Vert., vertebral.

16. Pfeiffer J, Ridder GJ A clinical classification system for aberrant internal carotid Acknowledgment
arteries. Laryngoscope. 2008;118:1931-1936.
We thank Wendy Fellows, PhD, for her continuous dedication during our lab-
17. Vishteh AG, Crawford NR, Meltona MS, Spetzler RF, Sonntag VKH, Dickman CA.
Stability of the craniovertebral junction after unilateral occipital condyle resection: oratory work.
a biomechanical study. J Neurosurg (Spine 1). 1999;90:91-98.
18. Panjabi MM, Dvork J, Crisco JJ III, Oda T, Wang P, Grob D. Effects of alar liga-
ment transection on upper cervical spine rotation. J Orthop Res. 1991;9(4):584-593. COMMENTS

T
19. Panjabi MM, Dvork J, Crisco JJ III, Oda T, Hilibrand A, Grob D. Flexion, exten-
sion, and lateral bending of the upper cervical spine in response to alar ligament tran- his paper provides a description of the anatomy and the extent of
sections. J Spinal Disord. 1991;4(2):157-167. anterior exposure that can be performed via the endonasal approach

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MORERA ET AL

to the foramen magnum and to the clivus. The utility of this approach results in minimal risk. The main point is that facility with all of these
remains in question especially for intradural pathology. Cerebrospinal approaches is necessary and the surgeon should be able to weigh the pros
fluid (CSF) leak will remain a significant issue with the anterior approaches. and cons of each without bias. Endonasal endoscopic techniques repre-
sent a trend in skull base approaches that are attractive, but may not
Johnny B. Delashaw
always represent the best or safest strategy.
Portland, Oregon
A final caution is with respect to the amount of condyle that can be safely

T
resected without causing instability at the craniocervical junction. No
he authors have completed a cadaveric study of importance in terms studies have been performed to quantify the biomechanics of ventrome-
of solving one of a number of limitations in the endonasal endoscopic dial condylar reduction. We do not know if the dynamics are strictly sim-
transclival approach (EETA). Lateral access at the level of the foramen ilar to dorsolateral reduction of the condyle. The authors base an opinion
magnum is limited and so far seems to be only overcome by utilizing an on their clinical experience, but offer no data as a basis for these state-
angled scope for viewing. The present study demonstrated a couple of ments. I agree that when utilizing such an approach we should be vigi-
points of personal interest to me as my practice has expanded to include lant to confirm stability after surgery.
these techniques. First, it is interesting that the tubercular compartment In conclusion, I appreciate the authors work in advancing our knowl-
was 8mm on average in height and added that to the exposure. From a edge regarding the EETA technique. This study will prove to be useful in
far lateral transtubercular approach extradurally, you are limited in view the hands of those utilizing these approaches.
to the area between the hypoglossal canal and the inferior aspect of the
jugular bulb. Reducing the tubercle via this route is mostly blind, in con- J.D. Day
trast to this ventromedial approach. Secondly, the condylar compart- San Antonio, Texas
ment is also reachable from the far lateral approach but only with removal
of a critical mass of the condyle, which would necessitate a fusion for
acquired instability. These 2 points may be a consideration when plan-
ning an approach for a particular lesion.
T his is a nice study of the anatomy as visualized endoscopically of the
inferolateral clivus. The anatomic relations of the supracondylar groove
to the course of the hypoglossal nerve is a critical piece of information if
Though I have been utilizing this strategy more and more in my prac- injury to the nerve is to be avoided. The most common clinical situa-
tice, and have been learning from the Pittsburgh groups publications, I still tion, in my experience, in which this anatomical knowledge can be applied
do not share the same level of enthusiasm for this technique for certain is during the resection of clival chordomas. The identification of the
lesions. I would argue with the authors that posterior displacement of the hypoglossal nerve in essence quantifies the degree of condylar resection
brain stem by foramen magnum lesions actually presents less of a chal- that has been performed and thus helps decide on the need for craniocer-
lenge, not more, when approaching this area from lateral. Manipulation vical stabilization. Although I have followed primarily extradural pathol-
of the neurovascular structures is usually facilitated by the posterior dis- ogy intradurally to achieve complete resection I have never planned an
placement of the brain stem and the spreading apart of the nerves over anterior clivectomy for totally intradural pathology. CSF leaks originat-
the lateral aspect of the tumor, providing corridors to work. Direct vision ing from defects in the clival dura can be particularly difficulty to treat
of the interface between nerve, vessel, and tumor is clear, which facilitates although I agree that when clinically available (not tumorally involved)
dissection. Dissection is furthermore at a greatly reduced distance in com- the nasal septal flap is particularly useful in this regard. We have used it
parison to the EETA. A common principle of surgery is to reduce the both alone and in conjunction with turbinate flaps.
operative distance in order to facilitate technically demanding maneuvers. Franco DeMonte
No matter the approach, nervous structures and vessels still have to Houston, Texas
be dissected away from the tumor. My experience with the EETA is that

M
this dissection is not always under direct vision. Viewing video demon- orera et al present a detailed and well documented anatomical study
strations of these procedures by the Pittsburgh group and others, also concerning the lateral extensions of foramen magnum endoscopic
confirms my experience with the technique. The far lateral approach to endonasal approach. Their dissections prove the feasibility of this approach
the foramen magnum affords mostly direct vision of such dissection. The and offer important landmarks for safely dealing with this area: the supra-
authors extol the virtues of the EETA as superior for extradural lesions since condylar groove and the external orifice of the hypoglossal canal later-
the dura does not have to be opened. This is not strictly true, as there are ally, the anterior cortical layer of the hypoglossal canal posteriorly. When
examples of lateral approaches that are completely extradural and do not combined, the transjugular and transcondylar extensions should offer a
require dural opening for extradural lesions. A case in point is an extended good exposure of the early V4 segment of the vertebral artery and of the
middle fossa approach for a petrous cholesterol cyst. Another example is lower cranial nerves. As any skull base surgeon knows, any millimeter of
a far lateral approach for a chondrosarcoma that has not penetrated the bony resection counts, so the authors should be commended for this pre-
dura. The authors also infer that it is a disadvantage to expose, control, cious contribution to the surgical anatomy of the foramen magnum.
and mobilize the vertebral artery for a lesion that is medial to the condyle
and lateral mass of C1. I would argue that it is probably safer to have Stephan Gaillard
early control of the artery and that proper mobilization of the vessel Suresnes, France

ons220 | VOLUME 66 | OPERATIVE NEUROSURGERY 2 | JUNE 2010 www.neurosurgery-online.com

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