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ANATOMIC REPORT
ENDOSCOPIC TRANSORAL-TRANSCLIVAL APPROACH TO
THE BRAINSTEM AND SURROUNDING CISTERNAL SPACE:
ANATOMIC STUDY
Oreste de Divitiis, M.D.
Neurosurgical Clinic, University of
Messina School of Medicine,
Messina, Italy
Alfredo Conti, M.D.
Neurosurgical Clinic, University of
Messina School of Medicine,
Messina, Italy
Filippo Flavio Angileri,
M.D.
Neurosurgical Clinic, University of
Messina School of Medicine,
Messina, Italy
Salvatore Cardali, M.D.
Neurosurgical Clinic, University of
Messina School of Medicine,
Messina, Italy
OBJECTIVE: The purpose of this study was to review the endoscopic anatomic features
of the anterior brainstem and surrounding cisternal spaces via a transoral-transclival
approach.
METHODS: Fifteen adult human cadaveric heads, obtained from 10 fresh cadavers
and 5 formalin-fixed cadavers, were used to demonstrate both the feasibility of an
endoscopic transoral-transclival intradural approach and its exposure potential. To
analyze the exact extension of a safe entry zone through the clivus, 20 skull bases were
used to obtain anatomic measurements.
RESULTS: The transoral approach was performed without maxillotomy or mandibulotomy and with a clival opening of 20 by 15 mm. Such a limited clival and dural
opening allowed the insertion of the endoscope and instruments, full visualization of
the anterolateral brainstem and cisternal spaces around it, and reconstruction of all
anatomic layers by means of a paraendoscopic technique.
CONCLUSION: The endoscopic transoral-transclival approach enables full access to
the anterolateral brainstem and to the cisternal space around it. The use of the
endoscope has the potential to reduce the need for a wider cranial base opening and
the danger of postoperative complications.
Domenico La Torre, M.D.
KEY WORDS: Anatomy, Brainstem, Neuroendoscopy, Transoral-transclival approach
Neurosurgical Clinic, University of
Messina School of Medicine,
Messina, Italy
Neurosurgery 54:125-130, 2004
Manfred Tschabitscher,
M.D.
Microsurgical and Endoscopic
Anatomy, University of Vienna,
Vienna, Austria
Reprint requests:
Oreste de Divitiis, M.D.,
Neurosurgical Clinic, University of
Messina, Policlinico Universitario,
Via Consolare Valeria 1, 98125,
Messina, Italy.
Email: [email protected]
Received, January 27, 2003.
Accepted, August 27, 2003.
NEUROSURGERY
T
DOI: 10.1227/01.NEU.0000097271.55741.60
he anterior brainstem and the vertebrobasilar junction are involved in a number of neurosurgical disorders, such as
extra-axial and intrinsic tumors, aneurysms,
and vascular malformations. Nevertheless,
they have long been considered a “no-man’s
land” (15). The development of the modern
concept of cranial base surgery has provided
the neurosurgeon with the technical and anatomic awareness to deal with these challenging anatomic structures. A number of different approaches to these regions have been
developed through anterior, anterolateral, and
posterolateral routes (11, 16, 17, 30, 31, 33–39).
Nevertheless, these cranial base surgical approaches are, in some instances, highly destructive; others require a high degree of cerebral and vascular manipulation, in contrast
with the modern concept of keyhole surgery.
Anatomically, the most physiological and
shortest route to the anterior surface of the
brainstem is represented by an approach per-
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formed through the pharynx and the underlying clival bone. This approach offers a direct
view of the anterior brainstem and vertebrobasilar junction without requiring dislocation
or manipulation of any cerebral or vascular
structure. The transoral approach is considered effective for giving access to ventrally
located abnormalities of the clivus and craniovertebral junction, and it has been used extensively for treatment of extradural lesions (2, 7,
12, 19, 21, 25).
A transoral-transclival approach to the intradural compartment was described for the
first time by Mullan et al. (26) in 1966 for the
treatment of an extra-axial tumor. Since then,
the approach has been used to treat mainly
midbasilar or vertebrobasilar junction aneurysms (13, 27, 32, 41). In 1991, Crockard and
Sen (6) reported seven intradural lesions operated on via this approach; the lesions comprised meningiomas and neurofibromas.
More recently, Perneczky’s group reported
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two cavernous angiomas of the brainstem treated by this
approach (28). Aside from these studies, few series and a
limited number of cases (29) have been reported, probably
because of the technical difficulties (such as the need for
working in a narrow and deep cavity and the lack of proper
instrumentation) or because of the likelihood of postoperative
complications, such as cerebrospinal fluid leakage or velopharyngeal incompetence (6, 13, 18, 20, 27, 32, 38, 40).
Endoscopy has technical characteristics that offer the potential to overcome such difficulties (3, 4, 8, 15). The aims of this
study were to demonstrate the feasibility of this approach and
its exposure potential through a limited clival and dural opening and to describe the anatomic features of an intradural
transoral-transclival approach from the endoscopic
perspective.
RESULTS
Bone Measurements
Figure 1, A and B, shows the distances that were measured
between the anatomic structures that may be jeopardized
during the transclival approach. Table 1 summarizes these
measurements and those obtained by measuring the depth of
the surgical field and the extension of the exposed clival
surface.
Endoscopic Procedure
After opening the dura mater, the premedullary, the prepontine, and the lateral cerebellomedullary cisterns came into
direct view (Fig. 2, A and B). The vertebral arteries could be
MATERIALS AND METHODS
This anatomic study was performed at the Institute of Anatomy of the University of Vienna, Austria. Fifteen cadaver
heads were used for the study, 10 from fresh cadavers and 5
from formalin-fixed cadavers. The arteries of 10 fresh specimens and both the arteries and veins of 5 formalin-fixed
cadavers were injected under pressure with colored silicone
rubber (Dow Corning, Midland, MI) via internal carotid arteries and internal jugular veins. The endoscopes used were rigid
0-, 30-, 45-, and 70-degree rod lens endoscopes 2.7 or 4 mm in
diameter and 11 or 18 cm in length (Karl Storz, GmbH & Co.,
Tuttlingen, Germany).
The specimens were placed in a slightly extended position
in a four-point pin headrest. A self-retaining retractor system
was positioned to keep the mouth open. The soft palate was
split in the midline and fixed with sutures. The hard palate
was left in place. The pharyngeal mucosa was incised from the
anterior arch of the atlas upward through the vault of the
nasopharynx to the posterior border of the vomer. The mucoperiosteal layer was retracted laterally, exposing the clivus
and the craniovertebral junction. On the clival surface, the
pharyngeal tubercle was identified, and a clival craniectomy
with an average diameter of 20 mm in length and 15 mm in
width was initiated just above it with a high-speed drill. The
dura mater was visualized and opened with a vertical incision.
A video recorder (S-VHS SVO 9500 MDP; Sony, Tokyo, Japan)
and a video-capture system (Digital Still Recorder; Sony) were
used for digital acquisition of the endoscopic pictures.
To analyze the exact extension of a safe entry zone through
the clivus, we obtained anatomic measurements in 20 skull
bases. We measured the length of the retropharyngeal surface
of the clivus, and we measured its width at three points: at the
base between the occipital condyles, at the level of the pharyngeal tubercle, and at the upper portion of the border with
the vomer. The distances between hypoglossal channels, jugular foramina, and inferior petrous sinuses were also measured. Finally, the distance of the clivus from the superior
alveolar arch was measured to evaluate the depth of the
surgical field.
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FIGURE 1. Intraoperative views of the extracranial (A) and intracranial
(B) surfaces of the clivus. The overall length of the retropharyngeal surface
of the clivus from the vomer to the foramen magnum (h) and its width at
three points—at the border with the vomer (D1), at the level of the pharyngeal tubercle (D2), and at the base between the occipital condyles
(D3)—were measured. The distances between the inferior petrous sinuses
(D4), the jugular foramina (D5), and the hypoglossal channels (D6) were
also measured on the intracranial surface to analyze a zone of safe entry
through the clivus.
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ENDOSCOPIC ANATOMY
OF
TRANSCLIVAL APPROACH
TABLE 1. Data obtained measuring the mutual distances of
structures surrounding the clival opening, the depth of the
surgical field, and the length of the exposed clival surface
Measurement
Distance (mm)
Length of the exposed clival surface
29 (24 –38)
Depth of the surgical field
20 (16 –27)
Distance between occipital condyles
20 (16 –27)
Distance between petroclival sutures (at
the level of the pharyngeal tubercle)
27 (18 –35)
Distance between petroclival sutures (at
the level of the vomer)
21 (17–26)
Distance between hypoglossal channels
41 (36 – 44)
Distance between jugular foramina
60 (49 – 65)
Distance between inferior petrosal sinuses
21 (18 –25)
followed along their cisternal course up to the vertebrobasilar
junction at the pontomedullary junction. The origin of the two
posteroinferior cerebellar arteries and the anterior spinal artery, as they originated from the vertebral arteries, were visible in the anteriormost lateral cerebellomedullary cistern and
in the premedullary cistern, respectively. The fibers originating in Cranial Nerve XII in the preolivary sulcus were also
observed at this level. In the prepontine cistern, the basilar
artery could be visualized in the lower two-thirds of the field,
permitting observation of the typical variability of dimension
and course (31). The abducens nerve was identified and followed along its course in this cistern toward Dorello’s canal.
By means of a 30- to 45-degree optic lens and a lateral
inclination of the endoscope, it was possible to reach the
cerebellopontine cistern from a premeatal route. Along the
course of the anteroinferior cerebellar artery, the acousticfacial bundle was identified and followed along its free cisternal course to the internal acoustic channel (Fig. 3, A and B).
Anatomic features of the internal acoustic channel could be
observed as a result of the optic properties of the endoscope
(Fig. 3B). At this level, it was also possible to visualize the
labyrinthine arteries in their course toward the internal acoustic channel (Fig. 3, B and C).
Turning the endoscope rostrally and using the same angled
optic lens at 30 degrees and 45 degrees, the upper part of the
cerebellopontine angle was explored. The main structure under this view was represented by the trigeminal nerve along
its course from the pons toward Meckel’s cave (Fig. 3D). By
using the same angled optic lens and turning the endoscope
laterally and downward, it was possible to reach the posterior
part of the lateral cerebellomedullary cistern (Fig. 3, A and C).
The interpeduncular fossa was also reached with this approach. Angled optic lenses at 45 or 70 degrees were needed to
achieve good visualization. The endoscope was directed up-
NEUROSURGERY
FIGURE 2. By use of 0-degree optics, the premedullary (A) and prepontine cisterns (B) were visualized. The lower basilar artery (BA) and the
vertebrobasilar junction were in direct view after the dura mater was
opened. The anterior spinal artery (ASA) descending from the two vertebral arteries (VA) was visible at the pyramid decussation and could be followed down to the spinomedullary junction. The origin of the posteroinferior cerebellar artery (PICA) could also be identified at this level. The
origin of the anteroinferior cerebellar artery (AICA) and the perforating
branches could be visualized along the course of the basilar sulcus to the
upper part of the basilar artery, at the border of the interpeduncular cistern. In the prepontine cistern, the entire free course of both abducens
nerves (VI) could be followed from their origin in the pontomedullary sulcus to Dorello’s canal.
ward with an inclination of approximately 45 degrees, following the basilar artery to its superior third, which was hidden
by the border of the clival craniectomy. It was thus possible to
reach and thoroughly explore the interpeduncular cistern (Fig.
4A).
The perforating branches of the basilar tip and of P1 were
visible in detail and could be followed to their entrance in the
posterior perforated substance (Fig. 4B). The posterior communicating arteries appeared in the anterolateral part of the
surgical field, where they crossed Liliequist’s membrane to
reach the posterior cerebral arteries with a lateral deflection
(Fig. 4C). The mammillary bodies and the tuber cinereum were
also visualized (Fig. 4D). The identification of the oculomotor
nerves completed the exploration of the cistern (Fig. 4, A–C).
DISCUSSION
Minimizing surgical trauma means fewer complications,
shorter hospital stays, and reduced overall psychological consequences. Endoscopy is a leading technique of minimally
invasive neurosurgical procedures. Recently, an important im-
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FIGURE 3. By use of a 30- to 45-degree optic lens and a lateral inclination of the endoscope, it was possible to enter the cerebellopontine cistern
via a premeatal route. Along the anteroinferior cerebellar artery (AICA)
course, the acoustic-facial bundle (VII–VIII) was identified and followed
along its free cisternal course to the internal acoustic channel (IAC).
Because of the optic properties of the endoscope, it was possible to follow
the nerves to their entrance into the IAC and to observe their anatomic
features. The VII–VIII bundle was encircled by the loop formed by the
AICA. At this level, it was possible to visualize the labyrinthine arteries
(LbA) in their course toward the IAC (B and C). By using the same
angled optic lens, and by turning the endoscope laterally and downward,
it was possible to reach the posterior part of the lateral cerebellomedullary
cistern. It was possible to identify the IX and X nerves (IX–X) running
laterally and posteriorly from the retro-olivar sulcus to the jugular foramen, covered in their anterior portion by a tuft of the choroidal plexus
(CP) exiting from the foramen of Luschka and by the variable looping of
the posteroinferior cerebellar artery (A and C). By turning the endoscope
rostrally and using the same angled optic at 30 and 45 degrees, it was
possible to explore the upper part of the cerebellopontine angle. The main
structure under this view was represented by the trigeminal nerve (V). It
was observed along its course from the pons directed anteriorly and superiorly toward Meckel’s cave (D).
pulse in the development of endoscopic surgery was provided
by the introduction of the transnasal-transsphenoidal approach for surgery of the sellar and parasellar regions (3, 9, 10,
23). This experience has spurred the search for new surgical
approaches that would enable access to the entire cranial base
by the use of minimally invasive techniques (1, 22–24).
The use of the endoscope offers several theoretical advantages when dealing with the transoral-transclival approach. In
our anatomic study, we demonstrated that this approach enables full access to the anterolateral brainstem and to the
cisternal space around it, from the spinomedullary junction to
the interpeduncular cistern, including a thorough vision of the
vertebrobasilar arterial system and of Cranial Nerves III to XII.
This endoscopic approach thus provides excellent visualization of some of the most challenging and inaccessible territo-
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FIGURE 4. The interpeduncular cistern was reached by using a 70-degree
optic and an upward inclination of the instrument, following the basilar
artery (BA) to its superior third. In this cisternal space, the visual field
was limited by the tuber cinereum superiorly, Liliequist’s membrane
anterolaterally, and the optic tracts posterolaterally. The basilar tip, the
basilar bifurcation, the superior cerebellar arteries (SCA), and the P1
tracts of the posterior cerebral arteries were completely visible. The perforating branches of the basilar tip and of P1 were visible in detail and were
followed to their entrance into the posterior perforated substance. The posterior communicating arteries (PcoA) appeared in the anterolateral part of
the surgical field, where they crossed Liliequist’s membrane with a lateral
deflection to reach the PCA. Above the posterior perforated substance and
posteriorly to the tuber cinereum, mammillary bodies (MB) were also visualized. The identification of the oculomotor nerves (III) completed the
exploration of the cistern. They coursed from the interpeduncular fossa,
passing between the SCA and PCA in an anterior and superior direction
toward the tentorial edge.
ries of the brain, without requiring extended cranial base
destruction.
Furthermore, most of the limitations of the transoraltransclival procedure may potentially be reduced by the use of
an endoscopic approach. Crockard and Sen (6) suggested a
clival opening of 2 by 3 cm for dealing with intradural lesions;
in this study, the opening was limited to 20 mm in length and
15 mm in width. Such an opening was demonstrated to be
sufficient for the endoscopic view, and it was located in a “safe
entry zone” through the clivus, which we tried to delineate by
obtaining the bone measurements. These data, although already in the literature, were revised in this light to define the
limits of the clivectomy.
It is also worth noting that both labiomandibuloglossotomy
and maxillotomy, which are often required with microscopic
procedures to increase the view caudally and rostrally, were
not needed, and the reduced opening through the clivus did
not limit the complete exploration of the cisternal spaces. A
limited clival opening can reduce the risk of injuring the
condyles with subsequent postoperative instability. Another
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ENDOSCOPIC ANATOMY
potential advantage is represented by the preservation of better velopharyngeal function. A wide clival defect is responsible for the incompetence between the posterior pharyngeal
wall and the soft palate, resulting in difficulties in swallowing
and in phonation.
The dural opening was minimized; it was sized to allow the
introduction of the endoscope and the instruments. With this
approach, it was possible to suture the dura, even though it was
much deeper than the atlantic arch. This suturing was accomplished by using a paraendoscopic technique, which allowed
firm packing and safe sealing (Fig. 5). Both the limited clival and
dural opening, with the possibility of reconstructing each anatomic layer, may represent the basis for a reduced occurrence of
postoperative cerebrospinal leakage and infection, which represent the main complications of the standard approach.
A minimally invasive approach should be well grounded on
anatomic investigations. This study provides a description of
anatomic structures that, although widely known by neurosurgeons, are presented from a new perspective, as a result of
either the different pathway used or the different optical instruments. The view of the anterior aspect of the brainstem
offered in this study may appear, as often happens in anatomic dissection studies, to be simply an idealistic construction. However, it is worth noting that the surgical procedure
was similar to that used in the standard microscopic approach
and that the exposure widening was attributable to the possibility of reaching blind angles.
The application of this approach is, at present, still far from
clinical practice. However, clinical findings on the use of an
endoscopic transoral-transpharyngeal approach to treat
FIGURE 5. Artist’s drawings depicting the operative approach (A) and
the dural closure technique (B–D).
NEUROSURGERY
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TRANSCLIVAL APPROACH
craniocervical junction abnormalities have been reported, and
the endoscope was also used to assist in the removal of two
brainstem cavernous angiomas and a clival ecchordosis physaliphora (5, 14, 28). New technologies and instrumentation,
such as instruments able to work through deep keyholes and
with angled tips to reach blind angles, new clip applicators, or
catheter ultrasound, will make surgical practice easier. The
strategy for the endoscopic transoral-transclival approach will
presumably be selective and aimed mainly at lesions of the
lower ventral brainstem, such as aneurysms, cavernous angiomas, and small intra- and extra-axial tumors.
CONCLUSION
This study shows that the transoral-transclival route enables exploration of the cisterns surrounding the anterolateral
brainstem from the medulla to the lower diencephalon by
means of the endoscope. We obtained a new and original
visual perspective of these anatomic structures. The use of
minimally invasive endoscopic techniques has the potential to
reduce the need for a wider cranial base opening and to
decrease the danger of postoperative complications.
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COMMENTS
d
e Divitiis et al. have provided an anatomic rationale for an
endoscopic transoral-transclival approach to the brainstem. They have arguably demonstrated that the technique is
feasible and that it provides adequate access to the ventral
brainstem. Their anatomic and descriptive portrayal is compelling. Clinical follow-up will determine whether this anatomic study will lead to improved patient outcomes and
safety. The authors’ efforts are significant and meticulous.
Edward C. Benzel
Cleveland, Ohio
T
he authors have completed a basic theoretical study of the
adjunctive use of the endoscope in a transoral-transclival approach to the intradural structures. The study demonstrates that
access can be expanded through this approach with the use of the
endoscope. Although various clinical factors may result in this approach not gaining wide acceptance or common clinical use, this is
a useful article in guiding such attempts. I would also comment that
using such anatomic studies as one’s own platform for clinical
application of the endoscope is insufficient. Rehearsal in the laboratory on one’s own, developing the necessary facility with the endoscope, and working with the altered view provided are also components of a necessary first step. The authors make a case for the
increasing usefulness of the endoscope as an adjunctive imaging
tool in neurosurgery.
John Diaz Day
Pittsburgh, Pennsylvania
I
n this article, de Divitiis et al. have performed a study of an
endoscopic transclival approach to the clivus and the brainstem. It
is clear that the endoscope allows more structures to be visualized
than the microscope (1, 2). However, an important question is
whether the surgeon can “not only look, but actually do” (i.e.,
operate) with the endoscope; for instance, if there were to be bleeding from a branch of the basilar artery, can the surgeon stop the
bleeding and repair the artery? If a cranial nerve is damaged, can it
be repaired? An additional problem with an intradural transoraltransclival approach is repair of the dura at the end of the procedure
to prevent meningitis. This is a significant problem with both the
endoscope and the microscope. We need to make more progress
with regard to techniques than an anatomic study like this allows
before we can start using this technique with confidence.
Laligam N. Sekhar
Great Neck, New York
Dinko Stimac
Annandale, Virginia
1. Kalavakonda C, Sekhar LN, Ramachandran P, Hechl P: Endoscope-assisted
microsurgery for intracranial aneurysms. Neurosurgery 51:1119–1127, 2002.
2. Puxeddu R, Lui MW, Chandrasekar K, Nicolai P, Sekhar LN: Endoscopicassisted transcolumellar approach to the clivus: An anatomical study. Laryngoscope 112:1072–1078, 2002.
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