Results
Tumors of the Jugular Foramen
Tumors of the jugular foramen may be broadly classified into primary lesions, arising
from within the jugular foramen, such as paragangliomas, schwannomas, meningiomas,
and aneurysmal bone cysts, as well as into lesions with secondary extension into the
jugular foramen, such as chondrosarcomas, chordomas, cholesteatomas, and meningiomas
of the cerebellopontine angle that grow into the jugular foramen.[3] Paragangliomas are by far the most frequent, followed by schwannomas, and, then,
meningiomas.[4] In the present article, we will focus on the surgical nuances for primary lesions,
as they represent the basic concepts and details that may be extrapolated to secondary
tumors.
History of the Craniocervical Approach
The history of the surgery of the jugular foramen has been exquisitely detailed in
previous publications.[1] Since most tumors present with ear symptoms, early literature was dominated by otolaryngologists,
with the first reports of neurosurgical exploration for jugular tumors arising in
1951,[5]
[6] and a further report of a glomic tumor arising from the jugular foramen successfully
resected through a suboccipital approach in the same year.[7] The description of the craniocervical approach as such may be attributed to Shapiro
and Neues in 1864[8] and Gejrot in 1965.[9] They described the cervical resection, radical mastoidectomy and transposition of
the facial nerve, but they did not dare entering the posterior fossa, leaving intracranial
tumors for radiation therapy. In the 70s, with the advent of skull base teams composed
of neurosurgeons, otolaryngologists, and head and neck surgeons, tumors of the jugular
foramen were now thought of as neurosurgical, otological, and cervical problems.[10] In 1971, Kempe et al.[11] performed a suboccipital craniotomy and mastoidectomy to resect a glomus jugulare
tumor of the middle ear and intracranial compartment. They also described the ligation
of the sigmoid sinus and jugular vein, with resection of the tumor inside the jugular
bulb. In the same year, Hilding & Greenberg[12] reported a similar approach that included exposure of the internal carotid artery
through the glenoid fossa and packing of the inferior petrosal sinus after resection
of the tumor. In 1974, Glasscock et al.[13] proposed a protocol for the diagnosis and treatment that described the use of the
extended facial recess to remove tumor from the hypotympanum without transposing the
facial nerve, and reconstruction of the tympanic membrane when the external auditory
canal was exposed (both techniques had been previously described, but not for glomus
jugulare tumors). Finally, Gardner et al.[14] published their series of combined cervical, temporal, and intracranial resection
of glomus jugulare tumors in 1981, and then, Al-Mefty et al.[15] reported its use for large tumors in 1987. Afterwards, several authors have added
small changes to the approach, according to particular extensions, which we will further
discuss below.
The Modern Craniocervical Approach
The craniocervical approach has been described at length in previous articles.[1] Briefly, a complete approach consists of a C-shaped incision extending from the
temporal region to the cervical region anterior to the sternocleidomastoid muscle
([Fig. 1a]). Dissection of the neck consists of identification of the cervical tumor, cranial
nerves IX to XII, carotid artery, jugular vein, and vertebral artery ([Fig. 1b]). Then, a mastoidectomy is performed to expose the jugular foramen and sigmoid sinus,
labyrinth, middle ear, and fallopian canal. A small craniectomy fully exposing the
sigmoid sinus with transposition of the vertebral artery is also performed. ([Fig. 1c]) After complete exposition of the region, the jugular vein and sigmoid sinus are
ligated, and the tumor is removed en bloc from the temporal and cervical areas. The duramater medial to the sigmoid sinus is
opened afterwards to resect the intracranial tumor, and, after hemostasis, the skull
base is reconstructed.
Fig. 1 Steps of a classic right craniocervical approach. (a) Head positioning and skin incision, beginning above the pinna and extending into
the cervical region. (b) Neck dissection, identifying the internal jugular vein (IJV), hypoglossal nerve
(XII), accessory nerve (XI), and mastoid tip (MT). (c) Mastoidectomy and craniectomy, with exposure of the posterior fossa duramater (PFD),
sigmoid sinus (SS), jugular bulb (JB), IJV, hypotympanum (HT), external auditory canal
(EAC), Treutmann triangle duramater (TTD), and fallopian canal (FC). (d) Ligature of the sigmoid sinus. The superior petrosal nerve is not exposed during
the approach.
Rationale for Using the Craniocervical Approach
As previously stated, the rarity of tumors of the jugular foramen limits the exposure
skull base surgeons have to different approaches, so we must rely on a few of them
that allow us to solve most problems and develop an adequate learning curve. Here,
the craniocervical approach is unmatched, giving access to all the compartments the
tumor may grow into; therefore, it may be tailored to each particular case. After
incision and exposure of the craniocervical region and neck dissection, mastoidectomy
and craniotomy are performed according to extension of the tumor into each compartment.
([Fig. 2a]).
Fig. 2 Several extensions of jugular foramen tumors. (a) Giant right glomus jugulare tumor, occupying the entire mastoid bone and extending intracranially
and into the cervical and retropharyngeal space. (b) Left jugular foramen schwannoma from the cerebellopontine angle with limited extension
into the jugular foramen by the glossopharyngeal canal. (c) Vagal schwannoma of the cervical region, extending up into the skull base, but without
entering the jugular foramen. (d) glomus tympanicum extending into the hypotympanum, below the internal auditory canal.
The first tailoring may be performed according to the histology of the tumor. A paraganglioma
almost always grows into the venous system, so regardless of the compartment it occupies,
the cranial and caudal poles of the tumor inside the jugular vein and sigmoid sinus
must be exposed. Schwannomas, on the other hand, usually grow medial to the jugular
bulb and vein, needing greater anterior exposure but usually without needing to sacrifice
the venous system. Meningiomas are probably the most difficult to completely resect,
given their extension into the internal auditory canal, fallopian canal, middle fossa,
infratemporal fossa, and paranasal sinuses,[16] with frequent invasion of the sigmoid sinus and jugular bulb, thus needing to be
removed. The craniocervical approach does allow for complete resection; however, reconstruction
of the skull base must be thoroughly planned beforehand.
Perhaps the only exception for the use of the craniocervical approach is when a tumor
is located mostly in the intracranial compartment and less than 1 cm within the jugular
foramen ([Fig. 2b]), in which case a retrosigmoid infralabyrinthine (suprajugular) approach may be
suitable for some lesions,[17]
[18] though the principles stated above must be considered. This makes schwannomas and
meningiomas ideal for a suprajugular approach, whereas paragangliomas and chordomas/chondrosarcomas
usually need more extensive bone resection.
Technical Nuances
Cervical Extension
This is the most variable part of the approach, and the cervical extension of the
incision is tailored to the tumor extension on preoperative imaging. In most cases,
identification of the bifurcation of the carotid artery is usually necessary to have
proximal arterial control in case of bleeding. Using the carotid bifurcation is a
good landmark to properly expose the inferior pole of a paraganglioma inside the jugular
vein, as well as to identify the cranial nerves IX to XII in the upper cervical region
and avoid unintended traction of the IX and X nerves during dissection. In cases in
which the tumor does not invade the venous system nor extends into the cervical region,
we advocate for a limited upper cervical dissection, so as to expose the extracranial
jugular foramen and to provide an adequate angle of attack to the mastoid region.
Management of Vascular and Nervous Structures
Before the advent of endovascular embolization, the external carotid artery was often
ligated in paragangliomas and meningiomas, given that their primary arterial supply
comes from the ascending pharyngeal and occipital arteries. Nowadays, both the internal
and external carotid arteries are usually left in place, and the bifurcation is used
to identify the hypoglossal nerve travelling 2cm cranial to it. In rare cases, the
internal carotid artery may be eroded by the tumor, and, in those cases, the use of
an extracranial-to-intracranial bypass must be considered before resection. Management
of the jugular vein depends mostly on the histology of the tumor. For schwannomas,
the venous system is usually displaced by the tumor, and, therefore, there is no need
to sacrifice it. In some meningiomas and all paragangliomas, the venous system is
compromised, and the jugular vein must be resected en bloc with the tumor. For that matter, the jugular vein must be completely freed from the
adjacent carotid artery and vagus nerve (passing between them), and then ligated below
the inferior pole of the tumor. Of note, the accessory nerve follows a posteroinferior
course after leaving the jugular foramen, crossing the jugular vein in its anterolateral
surface, and must be carefully preserved when performing en bloc resection ([Fig. 1b]). In case of schwannomas, differentiation of the origin from the glossopharyngeal
or vagus nerve is of uttermost importance when the tumor presents cervical extension,
since a glossopharyngeal schwannoma will be located medial and anterior to the carotid
artery, displacing it posteriorly, whereas a vagal paraganglioma will be located between
the carotid and jugular vein, displacing the carotid anterior and medial, and the
jugular vein posterior and lateral. Finally, the craniocervical approach exposes the
greater auricular nerve during superficial (suprafascial) dissection. The nerve must
be preserved and dissected throughout its cervical course to avoid auricular hypesthesia
or paresthesia, and, eventually, it can also be used as a cable graft if needed, though
sural grafts are preferred.
Temporal Extension
Mastoidectomy is the most crucial part of the approach, and several modifications
may be needed according to the extension of the tumor. The basic mastoidectomy includes
drilling of air cells until identification of the bony labyrinth, identification of
the fallopian canal, opening of the mastoid antrum, exposition of the duramater of
the Treutmann triangle, skeletonization of the jugular bulb and sigmoid sinus up to
the sinodural angle, and removal of the mastoid tip ([Fig. 1c]). In selected cases in which a mainly cervical tumor only occupies the inferior
pole of the petrous bone and there is no invasion of the venous system ([Fig. 2c]), a limited mastoidectomy with resection of the mastoid tip may be performed.
Extension into Hypotympanum and Facial Nerve Transposition
Particularly in paragangliomas extending through the tympanic plexus ([Fig. 2d]), the skin of the external auditory canal may be peeled off the tympanic bone, the
tympanum detached from its posterior insertion, and the posterior wall of the external
auditory canal drilled down to get the tumor through the facial recess, without opening
the fallopian canal ([Fig. 1c]). Nowadays, the only indication to expose and reroute the facial nerve is when the
tumor itself invades the canal/nerve, such as in some meningiomas or paragangliomas,
though it is the exception.
Management of Inner and Middle Ear Structures
Due to earlier diagnosis, tumors of the jugular foramen usually present with normal
hearing, making hearing preservation a goal of surgery. A retrolabyrinthine mastoidectomy
is sufficient to approach tumors of the jugular foramen, since their intracranial
extension is removed via trans-sigmoid craniotomy, avoiding the need of a transcrural/translabyrinthine
extension. The middle ear, however, needs to be exposed during the approach, especially
because the short process of the incus is an important landmark to identify the tympanic
segment of the facial nerve. Special care must be taken to avoid disarticulating the
ossicles when hearing preservation surgery is attempted; however, if the tumor invades
the middle ear (even with preserved hearing), the ossicles are frequently compromised
and must be resected ([Fig. 3]). In cases in which the tympanum has to be detached, tympanoplasty with temporal
fascia[19] must be attempted to preserve conduction. In cases in which hearing was already
compromised, the external auditory canal may be closed, or, most frequently, left
open to the mastoid cavity, which allows for postoperative endoscopic evaluation of
the surgical site.
Fig. 3 Auditory ossicles from a patient with a glomus jugulare tumor and preserved hearing.
Resection of the ossicles was necessary due to invasion of the stapes by tumor.
Management of Vascular and Nervous Structures
In the temporal bone, early identification of the facial nerve is paramount. The tympanic
segment of the facial nerve lays 1.5 cm medial to the spine of Henle, between the
short process of the incus and lateral semicircular canal. At the level of the stylomastoid
foramen, the nerve is identified by the tarsal “pointer.” After removing the mastoid
tip, the mastoid segment of the facial nerve may be delineated by joining both reference
points in the anterior mastoid. In the jugular foramen, it is important to remember
that nerves run medial to the jugular bulb, so paragangliomas will most likely displace
bulbar nerves medially, whereas schwannomas will displace the jugular bulb laterally.
Moreover, the glossopharyngeal nerve passes through its own canal, located more anterior
and superior to the vagal and accessory nerves, and it is separated by a dural fold.
All these anatomical details are extremely important to foresee the location of those
structures in order to preserve them. In the same way, the carotid artery is located
inside the carotid canal, anteromedial to the jugular foramen, and though it is not
usually exposed, a dehiscent canal may be encountered, the tumor may erode into the
carotid artery, or in case of paragangliomas and meningiomas, they may be fed by caroticotympanic
branches arising from the petrous carotid artery, so preoperative images must be evaluated
for these possibilities. Finally, in cases in which the venous system must be sacrificed,
the sigmoid sinus must be ligated below the sinodural angle so as to preserve circulation
between the transverse and superior petrous sinuses ([Fig. 1d]). After en bloc resection of the tumor, brisk bleeding is expected from the inferior petrous sinus,
which can be stopped with packing with oxidized cellulose.
Intracranial Extension
A limited, 3-cm craniectomy anterior and posterior to the sigmoid sinus is usually
sufficient to approach an intradural tumor. Since the jugular foramen lays in the
inferior part of the posterior fossa, transposition of the vertebral artery from the
vertebral sulcus of C1 (and partial resection of the transverse process of C1) provides
ample space to work in the lateral cerebellomedullary cistern. We perform this transposition
in most cases when there is intracranial extension of the tumor, and we consider leaving
the vertebral artery in place only when the intracranial extension is small, particularly
in schwannomas.
Management of Vascular and Nervous Structures
In the lateral cerebellomedullary cistern, the same relationship between bulbar nerves
and the jugular bulb is encountered. The microsurgical technique for separating the
tumor from the nerves depends on the histology of the lesion. Meningiomas and paragangliomas
are adherent to the surrounding nerves, whereas schwannomas are more easily dissected
(except for the nerve it originates from). If the bulbar cranial nerves are infiltrated,
and the patient presents previously deficits, radical tumor removal with the infiltrated
nerves is performed. Damage of these nerves should be avoided if their function has
not been already compromised by the tumor. The intradural vertebral artery and branches
are not usually compromised, but, rarely , they may feed the tumor ([Fig. 4]).
Fig. 4 Right vertebral digital subtraction angiography showing filling of a glomus jugulare
tumor by fine branches of the V3 (atlantic) and V4 (intradural) segments of the vertebral
artery.
Closure and Postoperative Care
Closing the surgical defect must be planned preoperatively. We advocate for the use
of a multilayered closure with pedicled flaps in lieu of avascular fat grafts. Our
group has previously published a technique using temporo-cervical fascia anchored
in the sternocleidomastoid muscle, and temporal and digastric muscles to avoid cerebrospinal
fluid leaks and achieve good cosmetic outcomes.[20]
After surgery, the decision to extubate depends on the degree of manipulation of bulbar
nerves during surgery. Most cases are extubated immediately after surgery, when irritation
of the cranial nerves was minimal according to intraoperative monitoring readings.
When in doubt, it is appropriate to wait until the patient is fully awake to ensure
that the airway is sustained before removing the tube. All patients benefit from early
phonoaudiological evaluation to assess pharyngeal function and begin early oral feeding,
if possible.
