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linicopathologic Featuresf Jugular Foramen Tumors

ames T. Kryzanski, M.D., and Carl B. Heilman, M.D.

The jugular foramen (JF) is an anatomically complex region where important bony, neural,and vascular structures converge. Tumors are the primary cause of JF pathology and oftenpresent therapeutic challenges. In this article we discuss the clinical and pathologicaspects of JF tumors. These aspects include the classic JF clinical syndromes, imagingcharacteristics of specific JF tumors, and gross pathologic and histopathologic features.The three most common and important JF tumors, glomus jugulare tumors, meningiomas,and schwannomas, are discussed in depth. A wide variety of tumors can occur in the JF.Nonetheless, our current clinical and radiographic knowledge usually allows a clinician toascertain the pathology of a JF tumor preoperatively with a high degree of certainty. Doingso allows the clinician not only to formulate the most effective treatment plan but also toprovide accurate and thorough preoperative counseling to patients harboring these seriouslesions.Oper Tech Neurosurg 8:6-12 © 2005 Elsevier Inc. All rights reserved.

KEYWORDS jugular foramen, meningioma, schwannoma, glomus jugulare

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he jugular foramen (JF) region is a complex anatomicalarea that is an important though relatively uncommon

ocation for skull base tumors. Pathology in the JF may man-fest with dysfunction of only the traversing cranial nervesCN IX, X, XI). More commonly, however, surroundingtructures such as the middle ear, cerebellopontine angle, origh retropharyngeal space are also involved. In the surgical

iterature the term, JF tumor, usually refers not only to tu-ors that arise in the foramen itself (eg, glomus jugulare

umors) but also to tumors that arise in the jugular fossadjacent to the foramen such as jugular fossa meningiomas.

The differential involvement of the lower cranial nerves byisease processes in and near the JF led to the characteriza-ion of a number of JF syndromes.1 These syndromes must benderstood in context because the most common JF tumor,lomus jugulare, rarely ever leads to one of them. When seen,F syndromes usually result from less common lesions likechwannomas or metastases. Though termed JF syndromes,hese clinical pictures may result from lesions from therainstem nuclei to the extracranial retropharyngeal spaceTable 1).

JF (Vernet’s) syndrome: Unilateral involvement of CNs IX,, XI leads to loss of taste in the posterior third of the tongue;emianesthesia of the palate, pharynx, and larynx; and weak-

ufts-New England Medical Center Department of Neurosurgery, Boston,MA.

ddress reprint requests to James T. Kryzanski, M.D., Tufts-New EnglandMedical Center Department of Neurosurgery, 750 Washington Street,

aBox 178, Boston, MA 02111. E-mail: jkryzanski@tufts-nemc.org

1092-440X/05/$-see front matter © 2005 Elsevier Inc. All rights reserved.doi:10.1053/j.otns.2005.07.004

ess or paralysis of the vocal cords, palate, trapezius, andternocleidomastoid muscle.

Posterior lacerocondylar (Collet-Sicard) syndrome: Involve-ent of the hypoglossal (CN XII) nerve in addition to CNs IX,, and XI leads to tongue atrophy and weakness or paralysis.Posterior retropharyngeal (Villaret’s) syndrome: This syn-

rome has the same clinical picture as the Collet-Sicard syn-rome with the addition of Horner’s syndrome, usually re-

ated involvement of the sympathetic nerves near the highervical or petrous internal carotid artery.

Allied syndromes: Several other syndromes involving lowerranial nerve dysfunction also have been described. They aresually the result of brainstem ischemic injury and rarelyecause of tumor. In Avellis’s syndrome, vocal cord/palate pa-alysis (CN X) is associated with contralateral dissociativenesthesia (spinothalamic tract). Schmidt’s syndrome involvespsilateral anesthesia of the pharynx and larynx (CN X), pa-alysis of the soft palate and larynx (CN X), and weakness oraralysis of the trapezius and sternocleidomastoid musclesspinal CN XI). Tapia’s syndrome involves paralysis of thepsilateral tongue, pharynx, and larynx because of a lesionffecting the motor nuclei of CNs X and XII. Finally, Jackson’syndrome involves ischemic nuclear or radicular injury toNs X, XI, and XII.Many etiologies other than tumor and brainstem ischemiaust be considered in patients presenting with one of the JF

yndromes or a single lower cranial nerve deficit. Histori-ally, foremost among these are leptomeningeal processesuch as tuberculosis and syphilis, which used to account for

lmost half of the cases of JF or related syndromes.1 Other

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Clinicopathologic features of JF tumors 7

eptomeningeal processes include neurosarcoidosis and car-inomatous meningitis. Basilar skull fractures, retropharyn-eal abscesses, jugular vein thrombosis, and aneurysms are aew of the other rare causes of JF syndromes.

maging of JF Lesionsdvances in neuroimaging have greatly simplified the diag-osis of pathology involving the JF. With respect to tumors,ssessment with magnetic resonance imaging (MRI), com-uted tomography (CT), and cerebral angiography can usu-lly suggest the pathologic entity with a high degree of cer-ainty. This has obvious advantages for preoperative decisionaking, including the choice of approach, surgical goals,eed for preoperative embolization, and patient counseling.The most common tumors involving the JF are glomus

umors, meningiomas, and schwannomas.2 Less commonlyound are metastatic lesions, primary bone tumors, chordo-

as, chondrosarcomas, and epidermoid tumors. Among thehree most common tumors of the JF, glomus tumors are byar the most numerous. A comprehensive review of JF lesionsevealed 509 glomus jugulare tumors in comparison to 104chwannomas and 34 meningiomas.3 Because glomus tu-

able 1 JF and Allied Syndromes

Syndrome

JF (Vernet’s) syndromePosterior lacerocondylar (Collet-Sicard) syndromePosterior retropharyngeal (Villaret’s) syndromeAvellis’s syndromeSchmidt’s syndromeTapia’s syndromeJackson’s syndrome

able 2 Imaging Characteristics of Common JF Area Tumors

Tumor MRI

eningioma Isointense to cortex onT1- and T2-weightedimages, homogeneousenhancement withgadolinium, enhancingdural tail, absence ofvascular flow voids

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lomus jugulare Salt and pepperappearance, intenseenhancement withgadolinium

Erosirr

erve sheath tumor:schwannoma orneurofibroma

Irregular enhancementwith gadolinium, highsignal intensity on T2-weighted images

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hondrosarcoma Slight enhancement withgadolinium, high signalintensity on T2-

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weighted images

ors, meningiomas, and nerve sheath tumors compose mostF lesions, the surgeon must have an intimate knowledge ofheir imaging characteristics.4

This will be reviewed in the next article, but the salienteatures for these tumors are listed in Table 2.

linicopathologicspects of Individual Tumors

eningiomas, schwannomas, and glomus jugulare tumorsompose more than 80% of tumors involving the JF in oneeries2 and probably compose a higher proportion of tumorshose primary involvement is the JF. Considering them in-ividually is useful.

F Meningiomasrimary meningiomas of the jugular fossa and foramen areare tumors; fewer than 50 cases have been reported. Theirarity is attested to by their absence from the authoritativeeningioma treatises by both Cushing and Eisenhardt5 andastellano and Ruggiero.6 The largest published series haveontained only eight patients,7,8 and in a series of 161 poste-

Neurologic involvement

CN IX, X, XICN IX, X, XI, XIICN IX, X, XI, XII, sympathetic chainCN X, spinothalamic tractCN X, spinal XICN X, XIICN X, XI, XII

CT Angiography

ramen is notd, occasionaltions, hyperostosis

Faint tumor blush

largement of JF withr bony margins

Extreme vascularity with obvioustumor blush, AV shunting, JFfilling defect, occasionallytumor extends intraluminallyup the sigmoid sinus or downthe jugular vein

callopedment of the JF, lowensity

Minimal if any tumor blush

largement of JF withr bony margins

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ior fossa meningiomas only seven lesions were classified asF meningiomas.9

The most important fact concerning the presentation of JFeningiomas is that they often mimic the presentation of theuch more common glomus jugulare tumors. The most

ommon presenting signs and symptoms are hearing loss,innitus, the presence of a middle ear mass on otoscopy, andower cranial nerve deficits.7,8,10-12 Variation in the presentingigns and symptoms in the published series of JF meningio-as may reflect referral bias. The two largest series in the

tolaryngologic literature reported preoperative hearing lossn 11 of 14 patients, tinnitus in 8 of 14, and a middle ear massn 11 of 14. Notably, lower CN (IX–XII) deficits were onlyresent in 4 of 14 patients and involved a single lower cranialerve; no patients had multiple lower cranial nerve syn-romes. Other presenting signs and symptoms were facialeakness in 2 of 14 and dizziness in 5 of 14 patients.7,10

In the neurosurgical literature the preoperative lower CNysfunction was the most severe. The two largest neurosur-ical series reported lower cranial nerve dysfunction in 10 of5 patients, including two patients with Vernet’s syndromend one with Collet-Sicard syndrome.8,9 All published serieshow that these tumors have a strong female predominance,nd the typical age for occurrence is in the fourth or fifthecade of life.7,8,9,11

Anatomically, meningiomas historically termed JF mayrise in the foramen itself or more commonly in the jugularossa directly adjacent. There is no generally accepted ana-omic classification. One group8 divides meningiomas of theF area into three groups depending on their predominantocation relative to the jugular bulb: anterior, posterior, orcclusive. These categories indicate a suprajugular, retro-ugular, or transjugular surgical approach, respectively. Me-ingiomas arising in the jugular fossa resemble the typicalessile, well-circumscribed, solid lesions seen throughout theosterior fossa. Meningiomas that arise in the JF itself have aore invasive growth pattern with intraosseous growth into

he skull base.7,10 The hypotympanum and middle ear7 areften invaded. The posterior fossa component varies from amall nodule to a large tumor mass causing symptomaticrainstem compression.Extracranially, tumor extension is usually limited to the

arotid space where carotid artery encasement and jugularein occlusion are common.10 CN involvement depends onhe exact origin of the tumor and the growth pattern andends to be significant. In one series, the incidence was 50%f the patients.7 This involvement is likely the cause of highates of new postoperative lower cranial nerve deficits seen inperative series, ranging from 58% to 68% for each lowerranial nerve (CN IX-XI) in one review.3

Though meningiomas have been histologically dividednto numerous subtypes, the World Health OrganizationWHO) has adopted a three-grade system with respect toggressive behavior and likelihood of recurrence.13 Review ofhe published series’ and reports reveals the meningothelialWHO grade I) variant to be the most common. In 30 re-orted cases where histopathologic subtype was included,here were 27 WHO grade I tumors (17 meningothelial me-ingiomas, five transitional meningiomas, five psammoma-ous meningiomas, one WHO grade II (atypical meningi-

ma), and two grade III tumors (one anaplastic meningioma p

nd one malignant meningioma).7,8,11 Although most JF me-ingiomas are low grade, their tendency to invade bone andurrounding neural structures makes their resection a chal-enge. Among the three tumors that commonly arise in the JF,

eningiomas have the worst prognosis for postoperative cra-ial nerve function and recurrence.

lomus Jugulare Tumorsost tumors arising primarily in the JF are glomus jugulare

umors. Glomus tumors in the head and neck (jugulare, tym-anicum, and vagale) share a common cell of origin, patho-

ogic appearance, and the small possibility of symptomaticatecholamine secretion. The clinical presentations of headnd neck glomus tumors vary according to their location.lomus jugulare tumors arise in the paraganglionic tissue

ining the jugular bulb and are usually clinically silent whenmall and readily diagnosed when large. They grow insidi-usly and seldom become symptomatic until they involve theiddle ear.In several large clinical series (�50 patients), middle ear

ndings have been the most common; hearing loss hasanged from 63% to 91% and pulsatile tinnitus from 52% to3%.14-17 In one series all 231 patients had at least one ofhose two findings.15 Hearing loss is usually conductive as aesult of tumor in the middle ear, but it can also be sensori-eural reflecting invasion of the inner ear. Other signs andymptoms of ear involvement are common and include auralain, discharge, bleeding, vertigo and a vascular mass visibleehind the tympanic membrane (Fig. 1).Next to hearing loss, cranial neuropathies are the most

ommon neurologic manifestations of glomus juglare tu-ors. The facial nerve is most commonly affected, ranging

rom 21% to 33% of patients.14,16,17 Lower cranial neuropa-hies, found in 10% to 30% of patients,14,16 usually occur inxtensive tumors and are often well compensated for becausef a slow onset. Extensive tumors occasionally cause Horner’syndrome through carotid involvement or CN V and CN VI

igure 1 Setting sun sign as seen on otoscopy of the external earanal. When a glomus jugulare tumor (asterisk) extends to the mid-le ear, a vascular tumor can sometimes be evident behind theosterior inferior aspect of the tympanic membrane. S, superior; A,nterior; I, Inferior.

alsy from intradural or extradural growth.18 Glomus jugu-

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Clinicopathologic features of JF tumors 9

are tumors may also cause venous hypertension and elevatedntracranial pressure from extensive unilateral or bilateralnvolvement of the jugular bulb.19 Finally, catecholamine se-retion can be demonstrated in about 4% of glomus jugulareumors through 24-hour urinary collection of vanillylman-elic acid, metanephrines, and catecholamines.16,20,21 Al-hough rarely symptomatic preoperatively, this deficit canead to perioperative hemodynamic instability.

Anatomically, glomus tumors in the temporal bone aresually divided into glomus jugulare and glomus tympani-um tumors. This distinction is likely because of clinical dif-erences between the tumors more than to the actual distri-ution of glomus bodies in the temporal bone. Rockley andawke22 studied the anatomic distribution of glomus bodies

n the temporal bone. They suggested that tumors arisingrom glomus bodies adjacent to the jugular bulb or proximalo Jacobsen’s nerve in the inferior tympanic canaliculusould enlarge into the jugular bulb and present as glomus

ugulare tumors. In contrast, tumors arising from Jacobsen’serve or the promontory would present as glomus tympani-um tumors.

Glomus jugulare tumors usually arise in the lateral com-artment of the jugular bulb and displace the cranial nervesedially.3 They tend to spread first to the temporal bone andiddle ear. From there they may spread to involve adjacent

tructures through preformed pathways: Down the eusta-hian tube into the nasopharynx, along the carotid artery orhrough the tegmen tympani to the middle fossa, along theugular vein or hypoglossal canal to the posterior fossa, orhrough the round window and internal auditory canal to theerebellopontine angle.17 Several anatomic classifications oflomus jugulare tumors categorize low-grade tumors as thoseimited to the jugular bulb, middle ear, and mastoid whereasigh-grade tumors display intracranial or intradural inva-ion.16,23

Glomus jugulare tumors display a strong female:male pre-ominance—between 3:1 and 6:1 in large series—and mostften manifest in the fourth or fifth decade.14-16 In general,ead and neck paragangliomas will be multiple in 3% of allatients and in 26% of patients with familial tumors.24 There-ore, a radiological evaluation of the side contralateral to anown glomus jugulare tumor must be performed as a cru-ial part of the diagnostic work-up.

Familial occurrence of paragangliomas was noted as earlys 1933.25 Current evidence supports an autosomal domi-ant pattern of inheritance consistent with genomic imprint-

ng where the gene does not result in the development ofumors when maternally inherited.26 Screening after the agef 16 is therefore recommended among family members ofaraganglioma patients.Glomus jugulare tumors share identical histopathologic

haracteristics to paragangliomas in other head and neck lo-ations. These features include the ‘Zellballen’ appearance ofhief cell clusters surrounded by thin-walled capillaries andn extensive reticulin network. Electron microscopy revealsense secretory granules in the cytoplasm of these cells iden-ical to those in catecholamine-producing tissue. Histochem-cal analyses also have identified norepinephrine in tumorpecimens.27 Tumors may have various numbers of mitosesr degrees of nuclear atypia, but these changes have not been

ssociated with clinically significant behavior. Glomus jugu- s

are tumors usually exhibit slow growth. Rarely, however,hese tumors grow aggressively and may even demonstrateegional and distant metastasis.28,29

F Schwannomasike meningiomas, JF schwannomas are relatively rare tu-ors accounting for only 2.9% of all intracranial schwanno-as.30 More than 100 cases have now been reported in the

urgical and radiosurgical literature.30-41 Before the advent ofRI and high-resolution CT, most patients with JF schwan-omas were thought preoperatively to have vestibularchwannomas or glomus jugulare tumors because theirresentations can be similar.31

The presentation of a JF schwannoma usually dependsost on the anatomic location of the tumor. Predominantly

ntracranial tumors with slight involvement of the JF tend toresent as a cerebellopontine angle mass associated with sen-orineural hearing loss, tinnitus, vertigo, and ataxia and ofteno demonstrable lower cranial nerve deficit.31 Radiographi-ally, these lesions can be mistaken for vestibular schwanno-as although they can usually be distinguished by careful

eview of imaging studies. Like vestibular schwannomas,hey can displace the facial nerve significantly. According toome authors,31 preoperative facial weakness is rare but it haseen present in 20% to 25% of patients in some large se-ies.32,34 Predominantly extracranial tumors or those cen-ered in the JF usually manifest with slowly progressive lowerranial nerve deficits and may cause a classic JF syndrome.hey also may extend into the middle ear leading to a middlear mass and conductive hearing loss. A palpable neck massay be present.Considering all JF schwannomas, the most common pre-

entations are hearing loss and lower cranial nerve deficits.earing loss is present in as many as 60 to 75% of pa-

ients.31,32,34 Hoarseness and swallowing difficulties are theost common symptoms of lower cranial nerve dysfunction.

reoperative lower CN (IX–XII) deficits have been present in0% to 81% of large series31,32,34 although the incidence ofN IX deficits may be underreported. Other initial findings

nclude facial numbness or pain, long tract signs, papille-ema,42 nystagmus, and diplopia.For intracranial schwannomas as a whole, a 2:1 female-to-ale predilection has been described.43 In large series of JF

chwannomas, however, gender distribution has been rela-ively equal34 or even favoring a male predilection.32,35 Age ofresentation is usually the fourth through sixth decades bututlying cases presenting in the second or seventh decadeave been reported.31,34,38

JF schwannomas may be predominantly intracranial, ex-racranial, or foraminal. They also may assume a dumbbellhape and involve all of these areas. This distribution haseen hypothesized to result from variations in the tumor’soint of origin on the lower cranial nerves.44 Thus, tumorsriginating on the proximal nerve expand into the posteriorossa. Tumors in the midportion of the nerve expand into theone of the JF, and tumors of the distal nerves expand ex-racranially.

These patterns of growth have led to several anatomic clas-ifications for JF schwannomas. Kaye and co-workers31 clas-

ified these tumors into three groups: primarily intracranial

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type A), primarily involving bone (type B), and primarilyxtracranial (type C). A type D was added to this classificationy Pellet and co-workers45 to denote dumbbell-shaped tu-ors involving all of these areas. This expanded classificationas also used by Samii and co-workers,32 Franklin and co-orkers also classified JF schwannomas according to a glo-us jugulare system, which includes categories based on

ntracranial tumor size and involvement of the carotid artery.his system was subsequently modified by Mazzoni and co-orkers34 to account for the size of any neck component.The exact cranial nerve of origin was discussed in two large

eries. In a review of 45 JF schwannomas by Hakuba ando-workers38 the cranial nerve of origin was found to be theN IX, X, and XI complex in 19 cases, CN IX alone in 11, CN

X or CN X in 6, CN X in 4, and CN XI in two patients. In aeries of 16 cases, Samii and co-workers32 found the CNX-XI complex to be the origin of the tumor in two patients,N IX alone in 7, CN X in 6, and CN XI in one patient.The histopathology of JF schwannomas is similar to that of

ther intracranial schwannomas and does not vary with tu-or location.31 Histopathologic features of intracranial

chwannomas include areas of compact spindle-shapedeoplastic Schwann cells with occasional nuclear palisadingAntoni A pattern), which alternate with less cellular lip-dized tumor areas (Antoni B pattern). Verocay bodies, par-llel arrays of tumor cell nuclei and cell processes, are oftenound within Antoni A areas. Occasional mitotic figures maye seen but do not indicate malignancy.Grossly, JF schwannomas may be solid or cystic. Kaye and

oworkers31 noted two of their 13 cases were predominantlyystic tumors and both were primarily intracranial lesions.arvalho and coworkers36 described five cystic tumorsmong 21 cases of JF schwannomas. These tumors occurredn younger patients and also were predominantly intracranialumors; all extended to the cerebellopontine angle and com-ressed the brainstem. They further subdivided tumors intowo categories: Type 1 cystic lesions were single large cystsith a thin, enhancing tumor wall. Type 2 cystic lesions hadultiple cysts with a thick, irregularly enhancing cyst wall.lthough cystic schwannomas have a tenacious and adherentapsule, there was no significant difference in outcomes com-ared to patients with solid JF schwannomas.

hordomas and Chondrosarcomaeveral cases of chordomas and chondrosarcomas, rareauses of tumors centered in the JF, have been reported.46-49

hese tumors more commonly involve the JF through sec-ndary extension. Chordomas arise from notochordal rem-ants (ecchordosis physalliphora) found along the clivalone marrow. They usually arise extradurally in the clivusear the midline but may grow to involve the paramediankull base extensively. In addition to the conventional chor-oma subtype, which makes up 70% to 90% of tumors, therere dedifferentiated and chondroid subtypes.50 The dediffer-ntiated subtype has a significantly poorer prognosis whilehe chondroid subtype contains cartilaginous and chon-romatous elements. Whether the latter is a true chordomar a chondrosarcoma variant is debated.Chondrosarcomas are slow-growing malignancies derived

rom cartilage that usually arise from skull base synchondro- c

es, typically from the petrooccipital synchondrosis.50 Unlikehordomas, chondrosarcomas usually arise in a paramedianocation. Like chordomas, they may grow extradurally to in-olve the JF. They also have three pathologic subtypes: con-entional, mesenchymal, and dedifferentiated. The mesen-hymal and dediffererentiated subtypes contain variousmounts of small undifferentiated stromal cells and have aorse prognosis than conventional subtypes.Chordomas and chondrosarcomas usually manifest with

eadaches and diplopia. In 50% of cases, the diplopia isecause of CN VI palsy.51 Trigeminal numbness is the nextost common cranial neuropathy. Dysfunction of CNs VII–II is less common, occurring in approximately 20%.50 Mul-

iple ipsilateral cranial neuropathies are more common tohondrosarcomas than chordomas.51 Radiographically,hordomas and chondrosarcomas display highly variableeterogeneous enhancement, lobulation, calcification, bonyrosion, and high signal intensity on T2-weighted MRI. Com-ined with the previous characteristics, involvement of thelivus or the petrooccipital synchondrosis is highly sugges-ive of these tumors. Chondrosarcomas and chordomashemselves may be difficult to distinguish radiographicallyxcept that chordomas tend to occur in the midline andhondrosarcomas in paramedian locations.

ther JF Lesionsrimary bone tumors may present as JF lesions. They arencommon and include a large number of pathologic entitiesuch as giant cell tumors, aneurysmal bone cysts, osteoblas-omas, plasmacytomas, ossifying fibromas, nonossifying fi-romas, fibrous dysplasia, osteoid osteomas, solitary boneysts, and osteitis fibrosa cystica of hyperparathyroidism.52

ew lesion on this list merit additional discussion. Giant cellumors of the JF may mimic glomus jugulare tumors, pre-enting with pulsatile tinnitus, hearing loss, and a hypervas-ular mass behind the tympanic membrane visible on oto-copy. Importantly, angiography reveals small, intricateeeding vessels to a giant cell tumor in contrast to the largeessels that usually supply glomus jugulare tumors and otheraragangliomas.52 Cranial plasmacytomas also may presents vascular lesions of the JF. Though arteriovenous shuntings not usually seen on angiography, it has been reported53 andlosely resembles the angiographic appearance of a glomusugulare tumor.

Metastatic lesions are an important cause of JF lesions andre a more common cause of a classic Vernet or Collet-Sicardyndrome than primary JF tumors.1 A review of nine patientsith JF metastases by Greenberg and co-workers54 under-

cores the aggressive nature of these lesions. Of nine patients,ight had significant lower CN deficits and five had pain as arominent presenting feature, including glossopharyngealeuralgia in two patients. Head and neck tumors, accountedor four of the nine cases. Head and neck cancers may reacho the JF by direct extension or by hematogenous or perineu-al spread.55 The radiologic appearance of other metastaticesions may closely resemble that of glomus jugulare tumors:

etastatic melanomas,56 renal cell carcinomas,57 and adeno-

arcinomas.58

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Clinicopathologic features of JF tumors 11

onclusionwide variety of tumors can affect the JF, including glomus

ugulare tumors, meningiomas, schwannomas, chordomas,hondrosarcomas, primary bone tumors, and metastases. Ineneral, radiographic and clinical features of each tumor typellow preoperative identification with reasonable accuracy.ccurate preoperative diagnosis is important because of theomplexity of surgical treatment and to the growing availabil-ty of nonsurgical treatment modalities such as stereotacticadiosurgery, which may be undertaken without tissue diag-osis.

eferences1. Svien HJ, Baker HL, Rivers MH: Jugular foramen syndrome and allied

syndromes. Neurology 13:797-809, 19632. Samii M, Bini W: Surgical strategy for jugular foramen tumors, in

Sekhar LN, Janecka IP (eds.): Surgery of Cranial Base Tumors. NewYork, NY: Raven Press Ltd., 1993, pp 379-388

3. Lustig LR, Jackler RK: The variable relationship between the lowercranial nerves and jugular foramen tumors: Implications for neuralpreservation. Am J Otol 117:658-668, 1996

4. Chong VFH, Fan YF: Pictorial review: Radiology of the jugular foramen.Clin Radiol 53:405-416, 1998

5. Cushing H, Eisenhardt L: Meningiomas: Their Classification, RegionalBehavior, Life History, and Surgical End Results. Springfield: Charles CThomas, 1938

6. Castellano F, Ruggiero G: Meningiomas of the posterior fossa. ActaRadiol 104:1-164(suppl), 1953

7. Molony TB, Brackmann DE, Lo WWM: Meningiomas of the jugularforamen. Otolaryngol Head Neck Surg 106:128-136, 1992

8. Arnautovic KI, Al-Mefty O: Primary meningiomas of the jugular fossa.J Neurosurg 97:12-20, 2002

9. Roberti F, Sekhar LN, Kalavakonda C, et al: Posterior fossa meningio-mas: Surgical experience in 161 cases. Surg Neurol 56:8-21, 2001

0. Gilbert ME, Shelton C, McDonald A, et al: Meningioma of the jugularforamen: Glomus jugulare mimic and surgical challenge. Laryngoscope114:25-32, 2004

1. Tekkok IH, Ozcan OE, Turan E, et al: Jugular foramen meningioma.J Neurolog Sci 41:283-292, 1997

2. Inagawa T, Kamiya K, Hosoda I, et al: Jugular foramen meningioma.Surg Neurol 31:295-299, 1989

3. Kleihues P, Cavenee WK: WHO Classification: Tumors of the NervousSystem. Lyon: IARC Press, 2000

4. Alford BR, Guilford FR: A comprehensive study of tumors of the glo-mus jugulare. Laryngoscope 72:765-787, 1962

5. Brown JS: Glomus jugulare tumors revisited: A ten-year statistical fol-low-up of 231 cases. Laryngoscope 95:284-288, 1985

6. Jackson CG, Harris PF, Glasscock ME III, et al: Diagnosis and manage-ment of paragangliomas of the skull base. Am J Surg 159:389-393,1990

7. Spector GJ, Druck NS, Gado M: Neurologic manifestations of glomustumors in the head and neck. Arch Neurol 33:270-274, 1976

8. Brodkey JA, Robertson JH, Robertson JT: Glomus jugulare tumors, inRobertson JT, Coakham HB, Robertson JH (eds.): Cranial Base Surgery.Philadelphia, PA: Churchill Livingston, 2000, pp XXX-XXX

9. Beck DW, Kassell NF, Drake CG: Glomus juglare tumor presentingwith increased intracranial pressure: Case report. J Neurosurg 50:823-825, 1979

0. Matishiak MZ, Symon L, Cheeseman A, et al: Catecholamine-secretingparagangliomas of the base of the skull. J Neurosurg 66:604-608, 1987

1. Schwaber MK, Glasscock ME, Nissen AJ, et al: Diagnosis and manage-ment of catecholamine secreting glomus tumors. Laryngoscope 94:1008-1015, 1984

2. Rockley TJ, Hawke M: Glomus bodies in the temporal bone. J Otolar-yngol 19:50-56, 1990

3. Fisch U: The infratemporal fossa approach for extensive tumors of thetemporal bone and base of the skull, in Silverstein H, Norrell H (eds.),

Neurological Surgery of the Ear. Birmingham, AL: Aesculapius, 1977

4. Cook RL: Bilateral chemodectoma in the neck. J Laryngol Otol 91:611-618, 1977

5. Chase WH: Familial and bilateral tumours of the carotid body. J PatholBacteriol 36:1-12, 1933

6. McCaffrey TV, Meyer FB, Michels VV, et al: Familial paragangliomas ofthe head and neck. Arch Otolaryngol Head Neck Surg 120:1211-1216,1994

7. DeLellis RA, Roth JA: Norepinephrine in a glomus jugulare tumor:Histochemical demonstration. Arch Pathol 73:92, 1971

8. Taylor DM, Alford BR, Greenberg SD: Metastases of glomus jugularetumors. Arch Otolaryngol 82:5, 1965

9. Johnston F, Symon L: Malignant paraganglioma of the glomus jugulare:A case report. Br J Neurosurg 6:255, 1992

0. Tan LC, Bordi L, Symon L, et al: Jugular foramen neuromas: A review of14 cases. Surg Neurol 34:205-211, 1990

1. Kaye AH, Hahn JF, Kinney SE, et al: Jugular foramen schwannomas.J Neurosurg 60:1045-1053, 1984

2. Samii M, Babu RP, Tatagiba M, et al: Surgical treatment of jugularforamen schwannomas. J Neurosurg 82:924-932, 1995

3. Van Calenbergh F, Noens B, Desloovere C, et al: Jugular foramenschwannoma: Surgical experience in six cases. Acta Chir Belg 104:435-439, 2004

4. Mazzoni A, Sanna M, Saleh E, et al: Lower cranial nerve schwannomasinvolving the jugular foramen. Ann Otol Rhinol Laryngol 106:370-379,1997

5. Muthukumar N, Kondziolka D, Lunsford LD, et al: Stereotactic radio-surgery for jugular foramen schwannomas. Surg Neurol 52:172-179,1999

6. Carvalho GA, Tatagiba M, Samii M: Cystic schwannomas of the jugularforamen: Clinical and surgical remarks. Neurosurgery 46:560-566,2000

7. Fink LH, Early CB, Bryan RN: Glossopharyngeal schwannomas. SurgNeurol 9:239-245, 1978

8. Hakuba A, Hashi K, Fujitani K, et al: Jugular foramen neurinomas. SurgNeurol 11:83-94, 1979

9. Crumley RL, Wilson C: Schwannomas of the jugular foramen. Laryn-goscope 94:772-778, 1984

0. Horn KL, House WF, Hitselberger WE: Schwannomas of the jugularforamen. Laryngoscope 95:761-765, 1985

1. Franklin DJ, Moore GF, Fisch U: Jugular foramen peripheral nervesheath tumors. Laryngoscope 99:1081-1087, 1989

2. Pluchino F, Crivelli G, Vaghi MA: Intracranial neurinomas of the nervesof the jugular foramen. Report of 12 personal cases. Acta Neurochir31:201-221, 1975

3. Casadei GP, Komori T, Scheithauer BW, et al: Intracranial parenchymalschwannoma. A clinicopathological and neuroimaging study of ninecases. J Neurosurg 79:217-222, 1993

4. Kinney SE, Dohn DF, Hahn JF, et al: Neuromas of the jugular foramen,in Brackmann DE (ed.): Neurological Surgery of the Ear and Skull Base.New York, Raven Press, 1982, pp 361-367

5. Pellet W, Cannoni M, Pech A: The widened transcochlear approach tojugular foramen tumors. J Neurosurg 69:887-894, 1988

6. Kaufmann BA, Francel PC, Roberts RL, et al: Chondroid chordoma ofthe lateral skull base. Pediatr Neurosurg 23:159-165, 1995

7. Harvey SA, Wiet RJ, Kazan R: Chondrosarcoma of the jugular foramen.Am J Otol 15:257-263, 1994

8. Cummings TJ, Bridge JA, Fukashima T: Extraskeletal myxoid chondro-sarcoma of the jugular foramen. Clin Neuropathol 23:232-237, 2004

9. Iwasaki S, Ito K, Takai Y, et al: Chondroid chordoma at the jugularforamen causing retrolabyrinthine lesions in both the cochlear andvestibular branches of the eighth cranial nerve. Ann Otol Rhinol Lar-yngol 113:82-86, 2004

0. Strugar J, Sekhar LN: Chordomas and Chondrosarcomas, in RobertsonJT, Coakham HB, Robertson JH (eds.): Cranial Base Surgery. Philadel-phia, PA: Churchill Livingston, 2000

1. Volpe NJ, Liebsch NJ, Munzenrider JE, et al: Neuroophthalmalogicfindings in chordoma and chondrosarcoma of the skull base. Am JOphthalmol 115:97, 1993

2. Rosenbloom JS, Storper IS, Aviv JE, et al: Giant cell tumors of thejugular foramen. Am J Otolaryngol 20:176-179, 1999

3. Miyachi S, Negoro M, Saito K, et al: Myeloma manifesting as a large

jugular tumor: Case report. Neurosurgery 27:971-977, 1990

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4. Greenberg HS, Deck MDF, Vikram B, et al: Metastasis to the base of theskull: Clinical findings in 43 patients. Neurology 31:530-537, 1981

5. Ballantyne AJ, McCarten AB, Ibanez ML: Extension of cancer of thehead and neck through peripheral nerves. Am J Surg 106:651-667,1963

6. Schweinfurth JM, Johnson JT, Weissman J: Jugular foramen syndrome

as a complication of metastatic melanoma. Am J Otolaryngol14:168-174, 1993

7. Boileau MA, Grotta JC, Borit A, et al: Metastatic renal cell carcinomasimulating glomus jugulare tumor. J Surg Onc 35:201-203, 1987

8. Chao CK, Sheen TS, Lien HC, et al: Metastatic carcinoma to the jugular

foramen. Otolaryngol-Head Neck Surg 122:922-923, 2000