Childs Nerv Syst (2007) 23:491–498
DOI 10.1007/s00381-006-0288-z
INVITED PAPER
Expanded endonasal approach: a fully endoscopic
completely transnasal resection of a skull base
arteriovenous malformation
Amin B. Kassam & Ajith J. Thomas & Lee A. Zimmer &
Carl H. Snyderman & Ricardo L. Carrau &
Arlan Mintz & Michael Horowitz
Received: 21 October 2006 / Published online: 17 January 2007
# Springer-Verlag 2007
Abstract
Objective and importance Vascular lesions with an intraosseus nidus involving the skull base are uncommon and
challenging [Gianoli GJ, Amedee RG Vascular malformation of the sphenoid sinus. Ear Nose Throat J. 70:373–375;
(1991), Malik GM, Mahmood A, Mehta BA Dural
arteriovenous malformation of the skull base with intraosseous vascular nidus. Report of two cases. J. Neurosurg
81:620–623;(1994)]. We present a pediatric patient, with a
life-threatening arteriovenous malformation (AVM) of the
sphenoid sinus, clivus, and ventral skull base, who failed
routine multimodality management of AVMs. An entirely
transsphenoidal fully endoscopic resection was used to
resect this ventral cranial base AVM with an intraosseus
nidus located in the clivus.
A. B. Kassam : L. A. Zimmer : C. H. Snyderman : R. L. Carrau
Department of Otolaryngology, University of Pittsburgh
School of Medicine, UPMC Presbyterian University Hospital,
200 Lothrop Street, B-400,
Pittsburgh, PA 15213, USA
A. B. Kassam (*) : A. J. Thomas : C. H. Snyderman : A. Mintz :
M. Horowitz
Department of Neurosurgery, University of Pittsburgh
School of Medicine, UPMC Presbyterian University Hospital,
200 Lothrop Street, B-400,
Pittsburgh, PA 15213, USA
e-mail: [email protected]
M. Horowitz
Department of Radiology, University of Pittsburgh
School of Medicine, UPMC Presbyterian University Hospital,
200 Lothrop Street, B-400,
Pittsburgh, PA 15213, USA
Clinical presentation A 4-year-old female presented with
recurrent, life-threatening hemorrhages from a clival and
ventral skull base AVM of the entire clivus and ventral skull
base. The patient had been temporized from the age of 2–
4 years with multiple internal and external carotid arterial
particulate and alcohol embolizations, including both external
and internal carotid artery embolizations, intracranial ligation
of the right internal carotid artery, and gamma knife
irradiation. Despite these multiple interventions, the patient
had persistent, life-threatening hemorrhages from arterial
recanalization and recruitment requiring intubation, tracheostomy, and nasopharyngeal packing.
Intervention The patient underwent a three-stage surgical
intervention to resect the AVM. An open subfrontal
approach, as the first procedure, provided minimal access
to the feeding vessels and was therefore aborted. A twostage image-guided fully endoscopic approach via a
sublabial midface approach without external incisions was
performed. Postoperative angiography revealed minimal
residual shunting in the pharynx and cavernous sinus. The
patient has been free of significant hemorrhages over the
past three years.
Conclusion Technological advances in endoscopic surgery
and image guidance are now allowing for purely endoscopic
surgical treatment of previously unresectable lesions with
acceptable morbidity. We report the successful and safe
resection of a ventral cranial base AVM via a fully endoscopic approach. This paper reports the first AVM with a purely
intraosseus nidus of the ventral skull base and demonstrates
the ability to deal with complex ventral skull base lesions
using a fully endoscopic transsphenoidal technique.
Keywords Arteriovenous malformation . Endoscopic
surgery . Skull base
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Introduction
Pediatric arteriovenous malformations (AVMs) of the head
and neck are high flow malformations which are present at
birth and may grow commensurately with the child. The
majority of these lesions in the head and neck (70%) are
found in the midface, while the rest are in the upper third
and lower third of the face [3]. Completely osseous-based
lesions are exceedingly rare. Two adult patients with an
intraosseus nidus have been reported [2]. These were
located in the foramen magnum and lower one-third of
the clivus with drainage through the intracranial veins.
Extrasinusal dural AVMs located at the skull base commonly occur around the edges of the foramen magnum [4].
The treatment of head and neck AVMs in the head and
neck is particularly challenging in the pediatric patient.
Untreated AVMs can be anticipated to cause progressive
deformity and function loss [5]. AVMs that involve the
upper aerodigestive and sinonasal tracts are also at risk for
profound hemorrhage. Treatment options include primary
surgery, external beam irradiation, focused radiosurgery,
and endovascular embolization with or without surgical
resection depending on the anatomic location and associated morbidity [3, 5–8].
We now present a pediatric patient with a life-threatening
AVM of the ventral cranial base that was osseously based
and incorporated into the clivus. The patient presented with
profound life-threatening nasal epistaxis at the age of
18 months. Given the young age, it was felt that surgical
options were limited in this location for fear of blood loss
and disruption of the facial elements; therefore, the patient
was initially managed with endovascular and radiosurgical
therapy but remained refractory presenting with repeated
severe epistaxis. Subsequent transsphenoidal endoscopic
resection was successful. To our knowledge, this is the first
report of an osseous- and soft tissue-based AVM in the
ventral cranial base treated using a purely transsphenoidal
endoscopic AVM resection.
Childs Nerv Syst (2007) 23:491–498
therefore, initial therapy consisted of nasal packing followed by polyvinyl alcohol (PVA) embolization of the right
internal maxillary artery. The epistaxis resolved, and the
patient remained asymptomatic.
Progression of disease and nonsurgical management
Two years later, the patient presented with near-fatal
epistaxis. Nasal packs were placed under general anesthesia, and repeat angiography revealed a complex and
persistent AVM with contributions from both internal
maxillary, facial, ascending pharyngeal, internal carotid,
and ophthalmic arteries (Fig. 2). A consideration was given
towards open surgical resection, but it was felt that the
mortality and morbidity associated with an open craniofacial resection and potential blood loss was too great.
Therefore, the patient underwent staged endovascular
management consisting of four sequential selective embolizations of the feeding vessels under general anesthesia
using PVA particles, tris-acryl gelatin particles, platinum
coils, and 100% alcohol5.
Over the next 17 months the patient continued to have
repeated episodes of significant epistaxis. These were
managed with nasal packing for stabilization followed by
an additional seven endovascular treatments with repeat
selective embolizations and eventual sacrifice of the
external and internal carotid arteries. During one such
embolization, the patient suffered compromise of the right
ophthalmic artery and consequent right eye blindness.
Gamma knife radiosurgery was administered with a
maximal dose of 34 Gy to the AVM.
Despite these interventions, the patient returned 3 months
later with severe and life-threatening epistaxis. She required
a tracheotomy for airway protection and was stabilized with
nasal packings under general anesthesia. Repeat arteriography revealed persistent supply to the AVM from both
vertebral arteries, the right supraclinoid carotid artery via a
large posterior communicating artery (Pcom) which fed the
left ophthalmic artery (the only eye with preserved vision)
and branches of the external carotid artery.
Case report
Initial surgery
Diagnosis
A 4-year-old girl initially presented to the Children’s
Hospital of Pittsburgh with an episode of severe epistaxis
at 18 months of age. Magnetic resonance imaging (MRI),
computed tomography (CT) (Fig. 1) and angiography
demonstrated an AVM of the ventral cranial base extending
along the entire clivus from the sella to the foramen
magnum. The predominant initial supply was from the right
internal maxillary artery. Given the patient’s young age, a
transfacial surgical approach was felt to be prohibitive, and
In an attempt to remove the feeders from the right vertebral
artery via the right Pcom, a pterional craniotomy was
undertaken, and the paraclinoid carotid artery just proximal
to the Pcom and distal to the ophthalmic was clipped. This
was done to remove any retrograde fill from the vertebral
artery through the Pcom into the residual paraclinoid
carotid and into any components of this that were
potentially feeding the paraclival space. Despite this
intervention, the AVM continued to maintain high flow,
and the patient continued to experience severe epistaxis
Childs Nerv Syst (2007) 23:491–498
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Fig. 1 a, b T1 weighted axial
MRI with gadolinium at the
level of the sphenoid and clivus.
Note the enhancement involving
the sphenoid bone and clivus
(arrows), indicating infiltration
of the bone by the AVM. c, d
Axial CT at the level of the
sphenoid and clivus. Arrows
represent the extensive involvement and destruction of the
entire ventral skull base by the
AVM
episodes. Due to the life-threatening nature of the disease
and its relentless progression, the decision was made to
surgically address the lesion despite the possible associated
morbidity.
Fig. 2 Representative arteriogram (a) and MRA (b) showing a complex AVM (arrows) in
the ventral skull base and clivus.
This arteriogram is status post
multiple embolizations including sacrifice of the internal
carotid arteries bilaterally and
staged gamma knife radiation
therapy. The AVM maintained
high flow with feeders from the
vertebral arteries bilaterally and
left ophthalmic artery (patient’s
only seeing eye)
Because we felt that an open anterior craniofacial or
transfacial approach would result in unacceptable morbidity, and the potential blood loss from the exposure could
prove to be significant, an initial subfrontal approach to
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reach the anterior cranial base and upper third of the clivus
was selected. A bifrontal craniotomy with orbital osteotomies and an anterior transbasal approach assisted by nasal
endoscopy and intraoperative navigation (Stryker Corporation, Kalamazoo, MI) was undertaken with somatosensory
and visual evoked potential monitoring. The ethmoid
sinuses and middle turbinates were removed endoscopically
transnasally, and wide sphenoidotomies were performed for
exposure of the lesion from below. This allowed for
simultaneous above and below visualization of the lesion.
The sella was identified, and the overlying bone was
removed from the inferior to the superior intercavernous
sinus.
Using the transcranial window, the optic canal was
drilled away along with the anterior clinoid. A thin shell of
bone was preserved over the optic nerves bilaterally. The
left ophthalmic artery at its origin from subclinoid carotid
was isolated and found to have a significant number of
feeders to the AVM. Proximal ligation of the ophthalmic at
the level of the carotid was deemed too risky given the fact
that the patient had no vision in the contralateral eye.
Therefore, these AVM feeders were isolated distal to their
origin from the ophthalmic artery, coagulated, and divided.
In the end, this approach proved to be of limited value as
the majority of the AVM occupied the subsellar space from
the middle and lower third of the clivus down to the
foreman magnum. From the subfrontal approach this region
could not be effectively accessed. We were not able to
isolate the majority of the feeding vessels which were
inferior and came from branches of the vertebral arteries
and the external carotid artery. An inferiorly based
pericranial flap was rotated to cover the sphenoid defect,
and the single-piece cranioorbital bone grafts were
replaced. The patient remained neurologically unchanged
postoperatively. A postoperative arteriogram did, in fact,
prove to be disappointing revealing persistent supply from
the vertebral arteries and the left ophthalmic artery.
Endoscopic approach A decision was now made to
undertake a staged, fully endoscopic, minimally invasive
resection without external craniofacial incisions. After a 10day period of rest and blood volume recovery, the patient
was brought back to the operating room using image
guidance and neurophysiological monitoring. A purely
transnasal endoscopic approach was limited by the small
size of the patient’s nostrils relative to the instruments.
Therefore, sublabial and anterior nasal septal incisions were
made to provide direct sublabial access directly into the
sphenoid sinus through small apertures via the pyriform
apparatus. The soft tissues of the lip and nose were
retracted superiorly with a Penrose drain, and the bone of
the right medial maxilla was removed to provide additional
access. The nasal septum was disarticulated from the
Childs Nerv Syst (2007) 23:491–498
maxilla and displaced to the contralateral side. The residual
posterior attachment of the nasal septum to the rostrum of
the sphenoid bone was removed allowing visualization of
the previous surgical site (stage I). A midface degloving
exposure had been created without external incisions. This
provided for excellent access facilitating delivery of a rodlensed endoscope, while still allowing for two additional
instrumentations to maintain bimanual dissection. Nasopharyngeal mucosa engorged with draining veins was
encountered inferiorly and was cauterized using bipolar
electrocautery. Mucosal elevation from the underlying bone
exposed the ventral foramen magnum. The longus collis
and capitus muscles were dissected free allowing for
isolation of the anterior C1 ring as confirmed by intraoperative neuronavigation. Complete endoscopic exposure
from the region of the previous orbitocranial bone flap
defect to C1 was now achieved.
With the overlying soft-tissue and engorged venous
system stripped away, it was apparent that the AVM had
incorporated the region’s osseous framework, creating
hundreds of channels within the bone through which
coursed the malformation’s vessels. (Fig. 3). The bony
resection technique consisted of using a high speed
Endonasal drill (TPS system Stryker, Kalamazoo Michigan), allowing for the isolation of individual vessels
coursing through the bony channels. Once exposed, these
vessels were coagulated using an endoscopic bipolar
cautery. Nonspecific generalized bone bleeding was controlled with bone wax and Avitene® packing. This
sequence was systematically repeated until the majority of
the bone in the ventral skull base from the planum to C1
had been removed exposing most of the dura overlying the
brainstem. Stage I of the overall treatment was terminated
to minimize intraoperative blood loss at this stage.
Tisseel Fibrin glue (Baxter Corporation, Deerfield, IL)
was then used to cover the exposed cranial base, and the
septum was returned to midline and anchored to the anterior
nasal septum with a nonabsorbable suture to the anterior
nasal spine. The bone of the medial maxilla was not
replaced. The sublabial and septal incisions were sutured,
and Merocel tampons were placed intranasally. No cerebrospinal fluid nor new neurological deficits were noted
postoperatively.
A postoperative arteriogram revealed residual supply to
the AVM via extracranial branches from the vertebral
arteries and the left ophthalmic artery. The patient
underwent a second stage endoscopic approach 2 weeks
later. After exposure of the nasopharynx and sphenoid
sinus via the previously described route, a 0° endoscope
was used to visualize the surgical site. Residual bone
removal proceeded inferiorly to the lower portion of the
clivus and C1 and laterally to the base of the pterygoid
plates. Bone was removed posteriorly to completely
Childs Nerv Syst (2007) 23:491–498
495
Fig. 3 Endoscopic endonasal intraoperative images demonstrating the
sequence used for resection. Panel a demonstrates exposure of the
clivus (C) following stripping of the soft tissue (ST) using a blunt
disector (D). Note the multiple intraosseus channels (IOC) within the
clivus. Panel b demonstrates isolation of an individual feeding vessel
(FV) run through an IOC. Panel c demonstrates bipolar cauterization
(BP) of a FV. Panel d demonstrates the use of a high-speed diamond
burr to drill through the clivus and expose additional IOCs. Panel e
demonstrates the use of bone wax (BW) to achieve hemostasis
following drilling of the “moth-eaten” bone and exposure of the
individual IOCs
expose the dura over the brainstem. An intraoperative
angiogram revealed residual feeding vessels at the right
inferior sella. Additional bone was removed isolating the
carotid genus. This proved to be somewhat challenging
given the previous embolizations. However, the two feeds
that were still present underneath the pterygoid wedge and
vidian nerve and canals were used to identify the carotid
genu, mobilize them into a lateral position, and directly
access the paramedian clivus in the region of the
petraclival synchondrosis for resection of feeders in this
area. All AVM feeders from the genus were obliterated,
and the wound was closed as before.
sinus (Fig. 4a). It was believed that some of this hypervascularity represented muscular engorgement, as there was
no early draining veins in association with this as had been
in the case with a true arterial venous malformation. The
clival removal extended from the sella to the foramen
magnum (Fig. 4b–d). The patient’s hospital course was
prolonged by pancreatitis and partial necrosis of the left
tongue secondary to multiple oral packings. The patient
was discharged to a rehabilitation center. The gastrostomy
tube and tracheostomy tube have since been removed.
Normal speech and mastication has subsequently followed.
The patient has returned to an unrestricted normal lifestyle
with no further episodes of epistaxis. Interval arteriograms
(at 1 and 2 years) have shown no disease progression.
Three years postoperatively, the patient has returned to
school with normal activities and no restrictions, and most
importantly, with no subsequent epistaxis periods.
Postoperative course
Postoperative arteriography revealed minimal residual
hypervascularity of the skull base lateral to the sphenoid
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Childs Nerv Syst (2007) 23:491–498
Fig. 4 Arteriogram (a) showing
a residual blush in the cavernous
sinus (large arrowhead) and the
pharynx (small arrow). Axial
CT (b–d) scans progressing
from a rostral to caudal direction
through the anterior cranial base
to the foramen magnum demonstrate the extent of the bony
resection of the ventral skull
base
Discussion
The optimal treatment (if tolerable) for symptomatic skull
base AVMs includes embolization followed by resection or
radiosurgery. This report describes the surgical resection of
an embolized ventral cranial base AVM using a fully
endoscopic completely transnasal approach. The current
case was particularly challenging due to the lesion’s
location and the patient’s age. The conventional approach
to the sphenoid sinus and upper third of the clivus includes
an extended subfrontal exposure [9]. This approach is
limited by the optic chiasm posteriorly and the cavernous
sinus and internal carotid arteries laterally. As such, it is not
suitable for panclival lesions. Nevertheless, this approach
was attempted in this case’s first surgical stage and proved
to be of limited value in approaching the lower clivus and
foramen magnum. Isolation and ligation of feeding arteries
which is of paramount importance in the dissection of
AVMs could not be achieved, as they were inferior to the
lesion from a subfrontal approach. This situation was
further aggravated by the fact that much of the feeders
came directly from the left ophthalmic artery, the child’s
only seeing eye. In addition to exposure limitations, this
approach requires some degree of bifrontal brain retraction
and is associated with a high incidence of olfaction loss
despite recent advances in preserving olfaction [10].
Alternatives involve a variety of craniofacial or transfacial approaches [9, 11]. While they would be useful in
adults, they tend to be rather destructive approaches from a
pediatric perspective. Transfacial approaches have high
rates of complications which include meningitis, CSF leak,
wound infection, ocular complications, and palatal dehiscence, and can result in disruption of the major facial
growth plates with malposition of the maxilla resulting in
malocclusion [11]. Transoral transclival approaches could
be used [12]. However velopharyngeal incompetence and
possible CSF leak from transgression of dura into the oral
cavity represents a major problem. The working space
proves to be narrow and deep, and in addition, can be
extremely limited for more rostral superiorly oriented
portions of the lesion that extended to the sella.
The transsphenoidal approach has been modified to
approach the parasellar and clival regions and has been
used at a number of centers [13]. Advantages include
Childs Nerv Syst (2007) 23:491–498
shorter exposure times, avoidance of brain retraction, and
direct access. However, it would be difficult to access the
lower clivus with this approach. Endoscopic endonasal
transsphenoidal approach to the pituitary has been already
established as a safe minimally invasive approach [14–17].
There have been reports of this being extended beyond the
confines of the sella to approach other parts of the ventral
skull base [15, 18–23]. There are certainly elegant anatomic
studies which have laid the groundwork for such an
approach [24–28].
At the University of Pittsburgh over the last decade, we
have used the foundations above to expand the endonasal
approach to regions beyond the sella and accessing the
entire ventral skull base [20–23, 29]. This case is an
illustrative example in this regard. A number of studies
have demonstrated the accuracy and clinical value of image
guidance systems for sinus and cranial base surgery, and as
such, image guidance systems have been an important asset
in the procedure’s evolution [30, 31].
In the present case, a transsphenoidal endoscopic
approach to the sphenoid sinus and clivus was utilized.
The transsphenoidal exposure was expanded with a
sublabial exposure given the patient’s small nares. This
approach with image guidance allowed for excellent
exposure of the surgical field from the planum sphenoidale
superiorly, to the carotid arteries, optic nerves, cavernous
sinus, and pterygoid plates laterally, and C1 inferiorly with
minimal morbidity and no cosmetic defect [20–23].
We believe that this represented a sentinel case in our
evolution of the expanded endonasal approach. Several key
elements were gleamed and lessons learned from this
particular procedure. This was the first pediatric patient
that we operated on where the nares were too small for
direct access; therefore, indirect access to the sphenoid
sinus had to be obtained through a sublabial midface
approach. This case further demonstrated the ability to
manage significant arterial and venous bleeding even in the
case of a child and helped us establish critical techniques
that formed the substrate for many subsequent endonasal
vascular procedures. Finally, this case was imperative to
understand the regional anatomies and limitations of both
the transnasal approach and the augmented corridors that
can be provided via an endonasal approach. It created the
concept of corridor surgery that we have adhered to since
that time with the upper portion of the corridor being the
transnasal approach and the remainder being the endonasal
approach. Most importantly, this was the first case in which
we were able to establish a panclival exposure that
extended from the sella through the arch of C1. It was, in
fact, this very procedure that provided the subsequent
genesis of the transodontoid and foramen magnum modules
that we have utilized and reported since [22, 23]. In fact,
this child gave us many gifts for which we are grateful. The
497
collaboration of a multidisciplinary team of neurosurgeons
and otolaryngologists with endoscopic and endovascular
training is an absolute requirement for this procedure
allowing for preoperative assessment and AVM embolization, intraoperative surgical access and control of bleeding,
and postoperative staging of residual disease. Surgical
staging was critical in removing such a large vascular
lesion as it made blood loss tolerable. Staging also allowed
for postoperative arteriography to document the location of
residual lesion and guide targeted additional surgery.
Conclusion
We report the first successful resection of ventral cranial
base AVM with image guidance assistance, transnasal fully
endoscopic approach. Continued experience with transnasal
endoscopic cranial base surgery will allow for the safe
removal of previously difficult to resect lesions with
minimal morbidity. This case report provides additional
value by demonstrating the feasibility of a completely
endoscopic resection for vascular lesions of this region.
While it has been often opined that vascular lesions serve as
a relative contraindication to an endoscopic approach due to
inadequate visualization and access for hemostasis, this
case establishes the ability to secure effective hemostasis
and excise vascular lesions even in pediatric patients where
issues of access and blood loss are most challenging.
Disclosure Drs. Kassam, Horowitz, and Snyderman serve as Paid
Consultants for Baxter Corp, Stryker-Leibinger Corp., KLS Martin
Corp.
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