Summary
Tumors in the jugular foramen frequently present a great challenge to the neurosurgeon because of its intimate relationship with the facial and lower cranial nerves as well as the internal carotid artery. The high morbidity associated with damage to these structures requires extensive laboratory training and deep knowledge of local anatomy.
26 Tumors of the Jugular Foramen
26.1 Anatomical Background
The jugular foramen is an opening in the skull connecting the posterior cranial fossa and the jugular fossa.1 It is located between the temporal and occipital bones, around the sigmoid and inferior petrosal sinuses, extending in a posterolateral to anteromedial direction. The foramen houses two venous compartments: the sigmoid part, which receives flow from the sigmoid sinus, and the petrosal part, which receives drainage from the inferior petrosal sinus. A fibro-osseous diaphragm separates these two vascular channels, and the lower cranial nerves lie on either side of this partition at the site of the intrajugular processes of the temporal and occipital bones (Fig. 26.1a).2 , 3 , 4
The jugular fossa is a deep depression at the inferior surface of the petrous portion of the temporal bone that communicates with the posterior cranial fossa via the jugular foramen. It hosts the jugular bulb, which continues as the jugular vein inferiorly (Fig. 26.1b). Cranial nerves IX, X, and XI enter the dura on the medial side of the intrajugular process. The entrance orifice of the glossopharyngeal nerve is separated from the entrance of the vagus and accessory nerves by a dural crest in the jugular fossa.5 The glossopharyngeal nerve (Fig. 26.2) passes forward, coursing through the jugular fossa, and exits on the lateral surface of the internal carotid artery deep to the styloid process. The vagus nerve exits the fossa vertically, in intimate relation with the accessory nerve behind the glossopharyngeal nerve on the posteromedial wall of the internal jugular vein.4 The accessory nerve descends laterally between the carotid artery and the internal jugular vein and then backward across the lateral surface of the vein to the sternomastoid and trapezius muscles. The hypoglossal nerve passes through the hypoglossal canal and does not traverse the jugular foramen. It passes adjacent to the vagus nerve and descends between the internal carotid artery and the jugular vein. Then it turns abruptly forward toward the tongue. Lesions located lateral to the fibro-osseous diaphragm frequently displace the nerves medially, favoring their preservation during tumor removal. By contrast, medially positioned tumors displace the cranial nerves onto the lateral tumor surface, where they interpose between the surgeon and the tumor—an unfavorable location.3
The carotid artery passes anteromedial to the internal jugular vein to reach the carotid canal. At the level of the skull base, this artery runs anterior to the vein and is separated from it by the carotid ridge. It ascends a short distance in the canal (the vertical segment), then turns at a right angle anteromedially toward the petrous apex (the horizontal segment). Three branches of the external carotid artery—the ascending pharyngeal, occipital, and posterior auricular arteries—can contribute significant blood supply to lesions of the jugular fossa. The sigmoid sinus (Fig. 26.3) courses down the sigmoid sulcus, turning anteriorly toward the jugular foramen and crossing it into the jugular bulb. It then flows downward behind the carotid canal into the internal jugular vein. The inferior petrosal sinus courses on the surface of the petroclival fissure, forming a plexiform confluence as it enters the petrosal part of the jugular fossa. Because the position of the lower cranial nerves with respect to the inferior petrosal sinus varies, overpacking or cautery over the sinus can injure these nerves.6
26.2 Regional Pathology and Differential Diagnosis
Several lesions can arise within the structures of the jugular foramen and fossa or from contiguous structures. Nevertheless, the surgeon must be able to recognize anatomical variations of the jugular bulb, particularly a high jugular bulb or turbulent flow within the bulb, so as not to misdiagnose them as disease (Fig. 26.4). Though rare, the three most common tumors within the jugular foramen are paragangliomas, schwannomas, and meningiomas.3 , 7 , 8 , 9 Precise preoperative diagnosis of these lesions, though not always possible, is crucial, because each has different surgical considerations, such as the need for preoperative embolization with glomus jugulare tumors or the removal of a certain amount of bone with meningiomas. MRI complemented by thin-cut bony window CT facilitates differentiation between these tumors (Table 26.1).
Differential diagnoses to be considered are acoustic schwannomas and lesions such as chordomas and chondrosarcomas, malignant tumors (carcinomas), metastases, peripheral primitive neuroectodermal tumors, cholesteatomas, chondromas, lymphangiomas, choroid plexus papillomas, salivary gland tumors, lipomas, aneurysmal bone cysts, hemangiopericytomas, plasmacytomas and inflammatory granulomas, pseudomasses such as normal vascular asymmetry, a high jugular bulb or jugular diverticulum, and aneurysms of the petrous carotid artery.7 , 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 A jugular foramen abscess has also been reported.17
26.3 Glomus Jugulare Tumors
26.3.1 Pathology
Benign paragangliomas originating within the jugular foramen are known as glomus jugulare tumors.18 These tumors grow along the path of least resistance and can gain access to the subarachnoid space by penetrating the dura of the posterior fossa, growing along cranial nerves, or, less commonly, penetrating the dura of the middle fossa.19 Glomus jugulare tumors are uncommon tumors of the head and neck, accounting for only 0.03% of all neoplasms and 0.6% of head and neck tumors.20 Nonetheless, they are the most common neoplasms of the middle ear and are the most common tumor involving the temporal bone, after only vestibular schwannomas. Glomus tumors have no clear racial predilection, but they seem to be more common among Caucasians. There is a marked predominance among females; women are affected three to six times more than men, with a peak incidence during the fifth decade of life. Multiple paragangliomas are reported in more than 10% of cases. Familial cases, most of which involve fathers and daughters, have a much higher rate of multicentricity, up to 55%. Evidence supports an autosomal dominant inheritance pattern consistent with genomic imprinting and an association with the haplotype at chromosome band 11q23. Most multicentric tumors are carotid body tumors. Only a few cases of bilateral glomus jugulare tumors associated with carotid body tumors have been reported.21 The two established classifications of these tumors, those of Fisch and Jackson, are based mainly on tumor size, with special emphasis on intracranial extension as a decisive factor for resectability.22 , 23 A subgroup of glomus jugulare tumors is rarely encountered but presents a formidable challenge for treatment. Al-Mefty and colleagues used the following criteria to describe this group24:
Giant size (Fig. 26.5)
Multiple paragangliomas (bilateral or ipsilateral) (Fig. 26.6)
Malignancy (Fig. 26.7)
Catecholamine secretion
Association with other lesions, such as a dural arteriovenous malformation or an adrenal tumor, or previous treatment that produced an adverse outcome that makes surgical intervention a much greater risk, such as sacrifice of the carotid artery, radiation therapy, or postoperative deficits or adverse effects from embolization
Fig. 26.5 Axial T1-weighted postcontrast MRI depicting a giant glomus jugulare tumor: (a) axial and (b) coronal. 
Fig. 26.6 Angiogram of a patient with multiple paragangliomas. (a) Left external carotid artery injection, lateral view, demonstrating a recurrent left glomus jugulare tumor (arrow). (b) Right common carotid artery injection, lateral view, demonstrating a right carotid body tumor. (c) Three-dimensional reconstruction of the right common carotid artery injection demonstrating the carotid body tumor. 
Fig. 26.7 Examples of malignant paraganglioma. (a,b) MRI after previous treatment with surgery and radiotherapy. (c) MRI showing marked growth a year later. (d) MRI after resection. (e) MRI showing rapid growth after 4 months. (f) Immunochemical staining for chromogranin. Note the brown granules in the cytoplasm. (Reproduced with permission from Al-Mefty O, Teixeira A, Complex tumors of the glomus jugulare: criteria, treatment, and outcome, J Neurosurg 2002;97(6):1356–1366.)
26.3.2 Clinical Presentation
Frequently reported symptoms of glomus tumors include pulsatile tinnitus, hearing loss, and cranial nerve palsies.23 Lower cranial nerve deficits are the prominent feature in patients who have symptomatic jugular tumors (Fig. 26.8).24 Conductive hearing loss is the result of mechanical obstruction of the ossicular mechanism by the tumor, whereas sensorineural hearing loss is a result of the involvement of the labyrinth. Patients may also present signs of elevated catecholamine production such as palpitations, excessive sweating, and headache, which must be investigated in all patients who have a glomus jugulare tumor. Eventually, large tumors can cause obstructive hydrocephalus and intracranial hypertension.
26.3.3 Appearance on Diagnostic Imaging
Bony-window CT scans show skull base infiltration with erosion and enlargement of the jugular foramen, characterized by an irregular “moth-eaten” pattern (Fig. 26.9).25 , 26 MRI shows an enhancing tumor with flow voids and a “salt-and-pepper” appearance on T2-weighted sequences (Fig. 26.10) and also discloses the presence of multiple tumors. MRI of the neck is done to exclude associated paragangliomas. The arteriographic findings of glomus jugulare tumors are typically a hypervascular mass with an intense characteristic tumor “blush.” Large feeding vessels and early draining veins are commonly encountered, suggesting early arteriovenous shunting. Like other tumors in this region, glomus jugulare tumors are predominantly supplied by the external carotid artery system, mainly the ascending pharyngeal artery (Fig. 26.11).25 Angiographic studies are critical for assessing the appropriateness of preoperative embolization after the tumor’s blood supply has been delineated. The most critical aspect of angiographic evaluation in patients who have undergone previous embolization or carotid occlusion is the identification of new feeding vessels from the internal carotid artery and the vertebrobasilar circulation (Fig. 26.12).24
26.3.4 Preoperative Preparation
With some modifications, the same preoperative protocol is used for all lesions of the jugular foramen. Audiologic and otolaryngologic evaluations are carried out, and speech evaluations and swallowing studies are conducted before surgery.
Hormonal Studies
Paragangliomas have the potential to secrete a wide variety of neuropeptide hormones, including adrenocortical hormones, serotonin, catecholamines, and dopamine.24 , 27 Patients who have hypersecreting tumors (catecholamine levels at least four times higher than normal) require preparation with combined alpha- and beta-blocker medication before surgery, angiography, or embolization. Beta-blockers should not be given before or without alpha-blockers. Screening for excess catecholamines is necessary in all patients who have a glomus jugulare tumor, and the actual treatment and duration of prophylaxis depend on the level of catecholamine secretion and its source. Patients who have these tumors might also harbor adrenal norepinephrine-secreting tumors. Accordingly, adrenal imaging is part of our work-up and is particularly important for patients who have hypersecreting tumors.
Diagnostic Imaging
MRI scans with and without contrast injection, angiography, and thin-cut bony-window CT scans constitute the radiologic workup needed to explore the anatomy of each patient’s jugular fossa, temporal bone, and condyles, as well as the nature of the tumor (cystic or solid) and its extensions (intracranial, extracranial, or dumbbell) and bone involvement (the presence of sclerosis and enlargement of the canal). The dominant vertebral artery and the characteristics of the vertebrobasilar system are also studied. Special attention is paid to the venous phase with a view to determining the size, dominance, and tributaries (superior petrosal, inferior petrosal, and vein of Labbé) of the transverse and sigmoid sinuses as well as the position and size of the jugular bulb.
Embolization
Embolization is indicated for patients who have paragangliomas and other highly vascular lesions.7 , 13 , 28 Surgery is more challenging when the patient has undergone prior embolization or carotid artery occlusion that was followed by development of new feeding vessels from the internal carotid and vertebrobasilar circulation.24 Current techniques are successful for embolizing the tumor bed and reducing blood loss (Fig. 26.13).
The thoroughness of embolization is critical, but partial embolization of the external carotid feeder augments the internal carotid feeders. Furthermore, embolization has accompanying risks and complications, including reflux cerebral emboli in the internal carotid artery, cranial nerve deficits from a “dangerous anastomosis,” and tumor hemorrhage. Carrier and colleagues reported that preoperative embolization of the inferior petrosal sinus, the anterior condylar vein complex, and the posterior condylar vein reduced preoperative bleeding considerably.29 Because of the absence of shift at the rigid structures of the jugular foramen, intraoperative image-guided frameless navigation is particularly useful during the surgical procedure.
Intraoperative Neurophysiological Monitoring
Cranial nerve X is monitored intraoperatively using an electromyographic endotracheal tube. Electromyographic needles are inserted into the facial musculature, the sternocleidomastoid muscle, and the tongue to monitor cranial nerves VII, XI, and XII, respectively. Auditory evoked potentials are obtained if hearing is present and no plan is made for closing the ear canal or resecting tumor from the middle ear. The external auditory speaker is placed under sterile conditions after the ear is prepared. Multiple paragangliomas present the greatest challenge to treating complex paragangliomas, because the treatment decision is based not on a single tumor but rather on the quality and length of the patient’s life. Whether to treat, when to treat, and which tumors to treat, as well as with which modality (surgery or radiation) and in what sequence, are all questions that must be addressed at the first evaluation and thoroughly considered throughout the patient’s follow-up. The surgeon must try to prevent the consequences of multiple bilateral cranial nerve deficits.24
26.3.5 Surgical Approach
The surgical approach is tailored in each patient to the findings of preoperative imaging, the local anatomy, and the tumor’s characteristics and extension. Jugular foramen tumors that have an intracranial extension should be carefully evaluated with regard to size, position, infiltrative potential, and vascularization. On the basis of these data, the surgeon can then settle on the most appropriate approach.30 Possible approaches include the infratemporal, combined infratemporal–posterior fossa, and combined approaches with a total petrosectomy.24
Patient Position
The patient is placed supine with the head elevated, turned away from the side of the lesion, and fixed in the three-point head frame (Fig. 26.14). The abdomen and thigh are prepared for removal of fat and fascia lata grafts.
Incision and Soft Tissue Dissection
An open C-shaped incision is made behind the ear and extended up to the temporal area and down transversely along the natural skin crease in the neck. In selected patients in whom the middle ear is involved, the external ear canal is transected at the bony cartilaginous junction. The skin of the external ear canal is everted and closed as a blind sac. A small periosteal flap is kept attached to the skin flap and closed over the ear canal. The skin flap, including the auricle, is reflected anteriorly, and the sternomastoid muscle is detached from its insertion in the mastoid process. The neurovascular structures in the neck are dissected and exposed; these include the common carotid artery, internal carotid artery, external carotid artery, jugular vein, and cranial nerves IX–XII.
Bone Removal
The mastoidectomy is done using a high-speed drill, and bleeding is anticipated during drilling of the bone. The eardrum is removed, and the tumor is located in the middle ear. The semicircular canals are exposed, and the facial canal is located caudal to the lateral semicircular canal. The facial nerve is skeletonized from the stylomastoid foramen to the geniculate ganglion.
We have abandoned the practice of routine transposition of the facial nerve; after its skeletonization, we keep it in a tiny protective bony canal.10 If the nerve needs to be transposed, it is moved out of the fallopian canal and secured anteriorly. A radical mastoidectomy exposes the sigmoid sinus down to the jugular bulb and in cases of intradural extension is followed by a lateral and low posterior fossa craniectomy.
Tumor Isolation
To isolate the tumor, the internal carotid artery and the jugular vein are followed upward toward the base of the skull. To expose the tumor, the posterior belly of the digastric muscle and the styloid musculature is transected and the styloid process is removed. The ascending mandibular ramus is dislocated anteriorly if necessary. The sigmoid sinus is then ligated distal to the tumor’s extension and proximal to the mastoid emissary vein. If the tumor extends into the middle ear or along the petrous carotid artery, the remnant of skin in the external ear canal is removed with the tympanic membrane. The internal carotid artery is exposed in the petrous canal by drilling the bone, if not already destroyed by the tumor, over the carotid canal. The Eustachian tube is obliterated using a piece of muscle. The anterior pole of the tumor is then dissected from the internal carotid artery, and the small feeding arteries are coagulated with bipolar electrocautery. At this stage, the extradural tumor is completely exposed.
If the tumor does not extend into the middle ear, the approach should be modified to preserve both the middle and the inner ear, so that the tumor is exposed in the infralabyrinthine space. The superior pole of the tumor is freed from the infratemporal fossa. The inferior pole is removed by dissecting and elevating the jugular vein after it is ligated, to prevent early venous drainage. The lower cranial nerves are preserved as they emerge from the jugular foramen. Intrabulbar dissection, a maneuver described by Al-Mefty and Teixeira, helps preserve the lower cranial nerves.24 This maneuver can be used for any tumor so long as the tumor itself has not penetrated the wall of the jugular bulb or actually infiltrated the cranial nerves. The outer wall of the lower sigmoid sinus is incised along the jugular bulb into the jugular vein. The tumor is then removed from inside the jugular bulb and the sigmoid sinus, and the tail end of the jugular vein is separated from the lower cranial nerves. The innermost venous wall separating the tumor from the nerves is left in situ to minimize dissection, trauma, manipulation, and devascularization of the lower cranial nerves.
Using this technique helps preserve the immediate postoperative function of the lower cranial nerves for patients in whom the tumor does not transgress the venous wall at the jugular foramen. When the tumor does transgress the venous wall, the cranial nerves can be infiltrated on a microanatomical level despite having normal function. In such situations, total resection may not be possible without sacrificing these nerves. Profuse bleeding from the inferior petrosal artery is controlled through gentle and judicious packing with appropriate hemostatic materials.
Intradural Tumor Removal
To remove the intradural portion of the tumor, the dura mater is incised posterior to the sigmoid sinus and carried forward, and the intradural extension of the tumor is exposed. The cranial nerves (VIII–XII) are meticulously dissected from the tumor and kept intact. Tumor encroachment on the medulla is removed through microdissection, and the basilar artery, the anteroinferior cerebellar artery (AICA), and the posteroinferior cerebellar artery (PICA) are dissected from the tumor and preserved. Any tumor extension into the foramen magnum is followed and removed after it is freed from the lateral and anterior surfaces of the medulla and the vertebrobasilar junction. When it is giant, the tumor should be isolated for safe surgical removal. This is best done in one stage through the combined posterior fossa and infratemporal approach described earlier.31 This approach allows the tumor to be devascularized from the intrapetrous carotid artery. It is also used to separate the tumor from the posterior fossa and to dissect the lower portion from the nerves with minimal blood loss while preserving the vessels.
Resecting tumors of the glomus jugulare requires special techniques in the handling of both arterial and venous dissection. Although paragangliomas engulf, adhere to, and receive blood from the internal carotid artery, with the aid of the operating microscope, a plane of dissection can be identified to separate the tumor from the carotid. Thus the carotid artery does not need to be sacrificed or reconstructed. Because exposing tumors of the glomus jugulare requires neck dissection, associated tumors of the carotid body can be removed at the same time without additional morbidity or undue lengthening of the operating time. Glomus jugulare tumors often shunt blood with high venous outflow. Accordingly, they should be handled as arteriovenous malformations. Thus venous drainage from the tumor should be preserved and the proximal end of the jugular vein should not be ligated until the tumor is isolated and its arterial supply is devascularized.
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