Endoscopic Endonasal Transclival Approach to the Ventral Brainstem: Anatomic Study of the Safe Entry Zones Combining Fiber Dissection Technique with 7 Tesla Magnetic Resonance Guided Neuronavigation

1. Endoscopic Endonasal Transclival Approach to the Ventral
Brainstem: Anatomic Study of the Safe Entry Zones Combining
Fiber Dissection Technique with 7 Tesla Magnetic Resonance
Guided Neuronavigation
Operative Neurosurgery 0:1–11, 2018
DOI: 10.1093/ons/opy080
Copyright © 2018 by the Congress of Neurological Surgeons
Alessandro Weiss, MD∗ ‡ § Paolo Perrini, MD, PhD§ # Matteo De Notaris, MD, PhD
∗Department of Neurosurgery, Hospital of Livorno, Livorno, Italy;
‡Laboratory of Surgical NeuroAnatomy (LSNA), University of Barcelona, Barcelona, Spain;
§Microneurosurgical Laboratory, University of Pisa, Pisa, Italy;St. Luke’s Medical Center, Aurora Neuroscience
Innovation Institute, Milwaukee, Wisconsin

2. BACKGROUND
• Treatment of intrinsic lesions of the ventral brainstem is a surgical challenge that
requires complex skull base antero- and posterolateral approaches.
• During the past decade, skull-base surgery has been enriched by the introduction of
endoscopic endonasal approaches to access lesions located in the ventral skull-base.
• Several transcranial approaches have been described to access intrinsic lesions of the
ventral brainstem; nevertheless, these approaches require extensive drilling of bone,
manipulation of neurovascular structures, and do not provide a direct working angle
to the ventral brainstem.
• More recently, anatomic and clinical studies concerning the endoscopic endonasal
transclival approach (EETA) documented the possibility of obtaining a wide exposure
of the brainstem ventral surface.
• In the present study, the authors explored the anterolateral surface of brainstem via
EETA to evaluate the degree of exposure of the safe entry zones.
• In addition, the identified safe entry zones were further investigated combining white
matter dissection with ultra-high-field MRI in formalin-fixed brainstems co-registered
using a neuronavigation system.

3. METHODS
• After approval from the the ethical committee; The specimens were obtained in the
first 12-h postmortem from donors without clinical history of neurological disease.
Endoscopic Endonasal Transclival Approach
• Endoscopic dissections were performed on 8 fresh-frozen latex injected cadaver heads
using a rigid endoscope 4 mm in diameter, 18 cm in length, with 0◦ optics (Karl-Storz,
Tuttlingen, Germany) connected to a light source through and a camera.
• EETA was performed following the steps as described in the literature.
• The nasal steps of dissections included monolateral right middle turbinectomy,
lateralization of the contralateral middle turbinate, posterior septectomy, anterior
sphenoidotomy, and antrostomy of the maxillary sinus.
• After opening of the sella, the tuberculum sellae, the dorsum sellae, and the posterior
clinoids were removed exposing the retrosellar area. The vomer and the sphenoidal
floor were removed.

4. • The pterygoid canals were identified about 4 mm lateral to the vomer–sphenoid junction.
• The bone of the clivus was progressively removed down to the anterior arch of C1.
• The caudal lateral boundaries of the bone removal were represented by the anterior third
of the occipital condyles.
• In all specimens an extradural anterior petrosectomy was performed to evaluate the effect
of lateral extending of bone removal on exposure of peritrigeminal zone.
• At this point, the dura was opened along the midline. The resulting intradural working area
is a rectangular space delimited superiorly by the indentation of tuberculum sellae,
caudally by the anterior arch of C1, and laterally by the parasellar and paraclival segments
of the internal carotid artery (ICA).
• The operative field obtained with EETA can be divided into 3 surgical working areas, namely
upper, middle, and lower levels .

5. • The upper level is limited by the posterior clinoid processes superiorly and by the abducens nerves entering the
dural porus inferiorly (red-dotted line).
• The middle level is limited upwardly by a line joining the abducens nerves and downwardly by a line joining the
intracranial openings of the hypoglossal canal (pale blue-dotted line).
• The lower level is bounded superiorly by the middle level and inferiorly by the superior margin of C1 (green-
dotted line).
 ICAc, clival segment of the internal carotid artery; ICAs, sellar segment of the internal carotid artery;

6. • The grade of exposure of selected safe entry zones for each working area was
evaluated.
• The safe entry zones explored were as follows: the lateral mesencephalic sulcus and the
perioculomotor zone at the upper level, the peritrigeminal zone at the middle level, and
the anterolateral sulcus at the lower level.
• The extent of exposure for each working area was evaluated by using a numerical
grading system as described by Kawashima et al.
 0 - a structure that is not exposed at all,
 1 - structure is exposed in less than 50% of specimens,
 2 - an exposure comprised between 50% and 99% of specimens, and
 3 - full exposure in 100% of specimens.
• Fiber Dissection and Neuronavigation Eight formalin-fixed brainstems were prepared
using the method originally described by Klinger in order to dissect the safe entry zones
identified through EETA.

7. • MRI sections were performed on a 7.0-T
BioSpec70/30 horizontal scanner
(Bruker-BioSpin, Ettlingen, Germany),
equipped with a circular polarized
transmit/receive coil actively shielded
gradient system (400 mT/m).
• The MRI was subsequently loaded in a
Medtronic-AxiEM electromagnetic-
neuronavigation system (Medtronic,
Minneapolis, Minnesota), and the
brainstems were registered.
• The dissections were performed in a
stepwise manner under microscopic
magnification with wooden spatulas
and microsurgical instruments. After
exposure of fiber tracts and their nuclei,
several measurements were taken with
an electronic digital caliper (±0.01 mm).

8. RESULTS
Endoscopic Dissection
• The transection of the inferior hypophyseal artery and the dissection of ligaments
between the pituitary gland and the lateral aspect of the dura allowed the gland to be
mobilized cranially.
Endoscopic view of the upper working area.
A. At this level the pituitary gland limits the exposure of the ventral surface of the
midbrain.
B. After dissection of the soft attachments of the pituitary gland with the lateral sellar
dura, the pituitary gland can be mobilized with exposure of the C, basilar apex, superior
cerebellar artery, P1 and P2 segments of PCA, and the oculomotor nerves.
D. The operative access to the perioculomotor zone passes inferiorly to the superior
cerebellar artery and is limited by a perforating branch.
E. The perioculomotor zone is exposed (red area).

9. • The lateral mesencephalic sulcus,
which extends from the
pontomesencephalic sulcus to the
medial geniculate body, was not
visible.
• The perioculomotor zone, which is
located laterally to the emergence of
the III on the medial one-third of the
cerebral peduncle, was visible in 60%
of the specimens.
• In the remaining cases, the anterior
pontomesencephalic segment of SCA
with its short perforators obstructed
the exposure of the area.

10. Endoscopic view of the middle working area
A. At this level the pons and medulla ventral surfaces, the
emergence of the VI from the bulbopontine sulcus and
presents a caudocranial and mediolateral direction
toward the Dorello’s canal, the basilar artery (BA), and
the anterior segment of anteroinferior cerebellar
artery (AICA) were visualized.
B. Drilling of the petrous bone is required to fully expose
the apparent origin of trigeminal nerve in the pons
and the peritrigeminal zone (orange area).
• The petrous apex limits the
dissection of the peritrigeminal
zone, located between the
emergences of trigeminal (V) and
facial nerves (VII). This area is
located medial to the V and laterally
to the corticospinal tract (CST).
• The exposure of the peritrigeminal
zone was obtained in all specimens
by an extradural anterior
petrosectomy behind the paraclival
carotids and then moving the
endoscope laterally under the
course of the VI.
• After the anterior petrosectomy, the
lateral pontine segment of the AICA
was observed in its course toward
the cerebellopontine angle.

11. • In 8 sides (50%) the AICA passed
through the peritrigeminal zone
halfway between the V superiorly
and the VII and vestibulocochlear
nerves inferiorly.
• In this scenario, the surgical access
requires a careful dissection in
order to avoid vascular injury of
perforating arteries.

12. • The lower level is limited by the
hypoglossal nerve (XII) entering
its canal cranially and the
superior margin of C1 caudally.
• The anterolateral sulcus was
exposed in 60% of specimens
moving the endoscope laterally
and inferiorly to the vertebral
artery (VA) and the rootlets of
the glossopharyngeal nerve.
• The variability of the course of
the VA lying on the
anterolateral sulcus hindered
the surgical exposure of this
entry zone in 40% of
specimens.
Endoscopic view of the lower working area
The exposure of the anterolateral sulcus is limited by VA.

13. Fiber Dissection Guided with 7T-MRI Neuronavigation
Perioculomotor zone
• Removing the basis of the cerebral peduncle laterally to the emergence of the
oculomotor nerve uncovers the substantia nigra. At this point, the red nucleus (RN) was
identified and correlated with the 7T-MRI.
• The distance between the RN and the surface of cerebral peduncle at the level of
frontopontine tract averaged 7.8 mm. The dissection should not fully expose the RN
because of the risk of damaging the fibers of III curving around its medial aspect.
• The medial lemniscus (ML) courses posteriorly and laterally to the RN.
A. This entry zone (orange area) is located between the exit point of the oculomotor nerve medially and the corticospinal tract laterally (medial one-
third of the cerebral peduncle).
Neuronavigation in axial B, sagittal C, and coronal plane D, and fiber dissection of perioculomotor zone E.
E. The pointer is located on the anterior wall of the RN just above the course of the intramesencephalic segment of the oculomotor nerve.
 FPT, frontopontine tract; OPTPT, occipito-parietotemporo-pontine tract

14. Peritrigeminal zone
• Progressive removal of superficial transverse pontine fibers discloses the pontine nuclei and the deep transverse
fibers.
• The CST is broken up into discrete bundles separated by the transverse fibers and is located medially to the
peritrigeminal zone.
• The average distance between the emergence of V and its motor nucleus was 13.7 mm.
• Extending the dissection medially, there is the risk of damaging the CST that is located 6 mm medial to the
intrapontine segment of the V.
• Enlarging the dissection behind the deep transverse fibers there is the risk to injury the ML, the spinothalamic
tract, and the lateral lemniscus, which on MRI form paired “crescents” that arc dorsally.
• A. This entry zone (orange area) is located between the origin of trigeminal and facial nerves and averaged 8.9 mm.
• Fiber-dissection of the peritrigeminal zone and neurovavigation in axial B, sagittal C, and coronal planes D.
• The peritrigeminal zone is bounded medially by the corticospinal tract, laterally by the intrapontine fibers of the trigeminal nerve, dorsally by
the trigeminal motor nucleus and the trigeminal spinal tract, and inferiorly by the intrapontine fibers of the facial nerve.
• E. The pointer is located on the trigeminal motor nucleus.
 CTT, central tegmental tract; MCP, middle cerebellar peduncle; O, olive; SCP, TST, trigeminal spinal tract.

15. Anterolateral sulcus
• A. This entry zone (orange area) is located between the inferior
roots of the hypoglossal nerve (the ventral surface of the
medulla along the anterolateral preolivary sulcus) and the
superior C1 rootlets.
• Fiber-dissection of the anterolateral sulcus and
neuronavigation in axial (B), sagittal (C), and coronal plane (D).
• E. The pointer is located in the anterolateral sulcus just below
the apparent origin of the hypoglossal nerve.
• The CST in the medulla is located anteromedially to the inferior
olivary nucleus and defines the medial border of the entry zone.

16. DISCUSSION
• The entry zones described in the literature for microsurgical resection of ventral
intrinsic lesions of the brainstem include the perioculomotor zone and the lateral
mesencephalic sulcus in the midbrain, the peritrigeminal zone in the pons, and the
anterolateral and postolivary sulci in the medulla.
• The EETA allowed exposure of the perioculomotor zone at the midbrain level, the
peritrigeminal zone at the pons level, and the anterolateral sulcus at the medulla
level.
• The endoscopic transclival exposure of the ventral surface of midbrain at the upper
level requires mobilization of the pituitary gland and offers a wide view of the
interpeduncular cistern.
• Pituitary transposition is the key step when the exposure of interpeduncular cistern
is planned through an EETA.

17. • Kassam et al. described the intradural transposition of the pituitary gland to access
tumors extending to the interpeduncular fossa.
• However, this surgical maneuver is associated with a nonnegligible risk of producing
pituitary dysfunction. Extradural pituitary transposition, which consists of mobilization
of the gland covered by both layers of dura (meningeal and periosteal), and interdural
transposition, which involves mobilization of the gland covered by the medial wall of
the cavernous sinus, minimize the risk of pituitary dysfunction and provide access to
selected extradural lesions and tumors with parasellar–retrosellar–suprasellar
extensions.
• Recently, He et al. treated a symptomatic ventral midbrain cavernoma via EETA using
pituitary transposition.
• This study showed that the endoscopic transclival exposure of the ventral pons allows
unobstructed view of BA, of anterior pontine segment of AICA, and of the cisternal
portion of VI.
• Moreover, the emergences of V and VII were barely visible. The exposure of the
peritrigeminal zone was obtained with an extradural anterior petrosectomy that
required removal of the additional bone surrounding the inferomedial surface of the
horizontal segment of the petrous ICA.

18. Brainstem Fiber Dissection Combined With Ultra-High-Field MRI
• Ultra-high resolution MRI allows improved visualization of tiny anatomic structures
of brainstem and offers unique opportunity for a detailed study of safe entry zones.
 Neurotomy in perioculomotor zone (surgical corridor located lateral to the
emergence of the III and medial to the CST) should be performed in a rostrocaudal
direction parallel to the frontopontine fibers running through the medial one-fifth of
the cerebral peduncle.
 This surgical corridor is minute and care must be taken to avoid injury of the
intra-mesencepahalic segment of III medially, of the CST laterally, and of the RN
that is located approximately 8 mm from the pial surface.

19.  The peritrigeminal zone is actually considered the safest entry zone for the pontine
lesions.
 Some authors favor a transverse neurotomy respecting the course of the
pontocerebellar fibers to minimize the damage.
 When a transverse incision is performed, care should be taken to avoid damage
to the CST located approximately 6 mm medially to the intrapontine segment of
the V.
 The neurotomy should remain medially to the emergences of V and VII to
preserve their intrapontine segments and their nuclei.

20.  The approach through the anterolateral sulcus, proposed for lesions of the
anterolateral medulla, requires a vertical incision between the inferior roots of the
XII and the superior C1 rootlets.
 The resultant surgical corridor is extremely narrow and carries high risk of
damaging the CST.
 Accordingly, lesions at this level should be resected only when come to the
surface and provide a direct corridor of attack.

21. Limitations
• Because this study is based on findings from normal cadaveric specimens, the
conclusions are not strictly applicable to clinical cases in which the anatomic
structures can be displaced by the pathology.
• In addition, although the authors investigated the extent of exposure of different
working areas, they did not analyze the degree to which the different anatomic
areas are suitable for surgical maneuvers.

22. Conclusion
• EETA allows the exposure of selected safe entry zones of the ventral brainstem.
• The perioculomotor zone, exposed at midbrain level, requires mobilization of the
pituitary gland and can be hindered by the SCA.
• The peritrigeminal zone is exposed at pontine level after extradural removal of
anterior petrous bone.
• The anterolateral sulcus is exposed at medullary level although the course of VA
can complicate its access.
• The combination of high-definition anatomic information provided by ultra-
highfield MRI and fiber-dissection of the same specimen resulted useful in
understanding the internal architecture of the brainstem.

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24. ThankYou!