ORIGINAL ARTICLE

Surgical approaches to jugular foramen schwannomas: An anatomic study Noritaka Komune, MD, PhD,1,2 Ken Matsushima, MD,1 Toshio Matsushima, MD, PhD,3 Shizuo Komune, MD, PhD,2 Albert L. Rhoton Jr, MD1* 1

Department of Neurosurgery, University of Florida, College of Medicine, Gainesville, Florida, 2Department of Otorhinolaryngology Head and Neck Surgery, Kyushu University, Fukuoka, Japan, 3Department of Neurosurgery, Saga University, Saga, Japan.

Accepted 31 May 2015 Published online 4 September 2015 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/hed.24156

ABSTRACT: Background. The variety of surgical approaches to jugular schwannomas makes selection of an approach difficult. The purpose of this study was to define the anatomic elements of these approaches. Methods. Ten adult cadaveric heads were examined. Results. There are lateral, posterior, and anterior routes that access various parts of the jugular foramen. Removal of the jugular process of the occipital bone provides access to the posterior aspect of the foramen, the infralabyrinthine mastoidectomy provides access to the lateral edge and dome of the jugular bulb, and the preauricular approaches provide access to the anterior margin of the bulb and foramen. Additions to these

INTRODUCTION Twenty-five percent of schwannomas are found in the head and neck.1 Intracranial schwannomas can arise from cranial nerves (CNs), however, except for the vestibular schwannoma, they are uncommon.2–4 Jugular foramen schwannomas arise mainly from the ganglion of CNs IX and X. Song et al5 proposed that the growth pattern of these tumors in the jugular foramen depends on the ganglion of origin. However, the variable location and nerve and vessel involvements make the precise site of origin of some tumors difficult to define.5–9 Advances in imaging have aided in differentiating jugular foramen schwannomas from glomus jugulare, meningioma, and other tumors, and in defining the precise location, extension, and vascular relationships of the tumor.9 Selection of an appropriate approach should be based on the preoperative neurological findings, and on tumor size, location, and extension revealed by MRI, CT, and angiographic studies. Several classifications of jugular foramen schwannomas have been based on tumor location, size, and extension.3,7,10,11 The classification by Kaye et al7 is popular and Pellet et al10 added an hourglass-type tumor. Type A tumors are primarily intracranial with some extension into the foramen; type B tumors are primarily in the foramen with or without intracranial extension; type C tumors are primarily extracranial with a minor extension into the foramen or into the posterior fossa; and type D tumors are dumbbell-shaped with

approaches may include cervical and vertebral artery exposure, facial nerve transposition, foramen magnum exposure, and external canal and condylar resection. Conclusion. An understanding of the anatomy of the jugular foramen is C 2015 crucial in achieving total tumor removal while minimizing risk. V Wiley Periodicals, Inc. Head Neck 38: E1041–E1053, 2016

KEY WORDS: jugular foramen, jugular process, schwannoma, temporal bone, skull base

intracranial and extracranial extension linked via the foramen. Placing the tumor in one of these categories facilitates operative planning and selection of an appropriate surgical approach. The jugular foramen is commonly accessed by posterior and lateral approaches and less commonly by anterior approaches. This abundance of approaches to the foramen has given rise to confusion in selecting the appropriate approach. In this study, the literature on the approaches to the jugular foramen was combined with dissections defining the main anatomic features of each approach (Table 1).3,6,7,12–33

MATERIALS AND METHODS Ten hemicrania from formalin-perfused adult cadaveric heads in which the arteries and veins were injected with red or blue silicone rubber (Dow Corning, Midland, MI), Thinner 200 (Dow Corning), and RTV catalyst (Dow Corning), were dissected using 33 to 340 magnifications of the surgical microscope and a 08, 18-cm Hopkins endoscope (Karl Storz GmbH, KG, Tottlingen, Germany) connected to a xenon light source and a high-definition camera. The lateral suboccipital, far lateral,20,32,34 postauricular transtemporal,14,35 preauricular subtemporal infratemporal fossa,28 and endoscopic transnasal/ transmaxillary transpterygoid approaches16,36,37 were performed to open the jugular foramen from a variety of angles.

RESULTS Microsurgical anatomy of the jugular foramen and its surrounding area

*Corresponding author: A. L. Rhoton, Jr, Department of Neurosurgery, University of Florida, College of Medicine, P.O. Box 100265, Gainesville, FL 32610-0265. E-mail: [email protected]

The petrous part of the temporal bone forms the anterosuperior part of the foramen and dome of the jugular HEAD & NECK—DOI 10.1002/HED

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1903 1986 1990 1991 1997 2013

Krause33 Heros20 Sen29 Sasaki31 Wen32 Nakamizo25

Mann24 Seyfried30 Mazzoni13 Kim21 Liu23 1991 1994 1995 2001 2006

Hakuba19 1979

1977 1979 1984 1985 1987 1994 1995 1995 1997 2004 2004 2013

Gardner17 Fisch12 Kaye7 Lambert22 Sekhar28 Tedeschi14 Samii3 George18 Pensak27 Oghalai26 Kadri6 Cinibulak15

IL Limited IL IL IL

IL

2 2 IL 2 Limited Limited

IL IL IL IL 2 IL IL Limited IL IL IL IL

JP

Dura

Elements of approach Cond.

1 1 1 1 1

1

2 2 1 2 N.D. 1

1 1 1 1 1

1

2 2 1 1 1 1

Si Si Si Si Si

RS or Si

RS RS RS RS RS Si

If necessary Posterolateral If necessary 2 1/3 posterior

2

2 2 Posterior half Posterior 2 1/3 posterior

1 1 2 2 1 2 Possible 2 1 2 2 2 1 2 2 2 1 2 2 2 1 1 Pre or RS or Si 2 1 1 Pre Posterior 1 1 Possible (Si) 1/3 posterior 2 2 2 2 1 N.D. Si 2 1 Posterior Pre 1/2-2/3 posterior 2 2 Pre 2

Year A B C Ant. Mast. Neck

Dallan16 2010

Author

Tumor type

2 2 2 2 2 2 2 1 2 2 2 2

C1

2 2 2 2 2 2 2 Possible 2 2 2 2

2 1 2 2 1

2

2 1 2 2 2

1

2 1 2 2 1

2

2 2 1 1 If necessary

2

2 2 2 2 2 2

1 1 1 1 2 1 2 2 2 2 2 2

FN

2 2 2 2 2

2

2 2 2 2 2 2

If necessary 1 1 1 2 1 2 2 2 2 2 2

EAC

Optional exposure if needed VA

2 2 2 1 2 2 1 2 2 1 2 2 1 Possible Possible 1 1 2

2 2 2 2 2 2 2 2 2 2 1 2

FM

Abbreviations: Ant., anterior; Mast., mastoidectomy; Neck, neck dissection; JP, jugular process; Dura, dura opening; Cond., removal of occipital condyle; FM, opening of foramen magnum; C1, removal of C1 transverse process; VA, vertebral artery translocation; FN, translocation of the facial nerve; EAC, resection of the external ear canal; IL, infralabyrinthine; Pre, presigmoid; RS, retrosigmoid; Si, resection of the sigmoid sinus; N.D., not described; JF, jugular foramen. Yellow includes infralabyrinthine approach; light green includes resection of jugular process; dark orange represents the applicable tumor type; and light orange is used for selected cases.

Anterior Endoscopic transnasal/transmaxillary transpterygoid Lateral Gardner’s approach Type A infratemporal fossa Infralabyrinthine Infralabyrinthine Preauricular subtemporal infratemporal fossa Postauricular transtemporal Cervical transmastoid Juxtacondylar Fallopian bridge technique Transjugular craniotomy with fallopian bridge technique Transcondylar suprajugular Presigmoidal suprabulbar infralabyrinthine Posterior Retrosigmoid lateral suboccipital Far lateral Extreme lateral Suboccipital approach with opening JF Paracondylar Posterior transjugular and transcervical Combined Suboccipital craniectomy with retrolabyrinthine removal/ retromastoideal craniectomy combined with a mastoidectomy Transsigmoid Transcondylar Petrooccipital Transsigmoid Hearing preservation technique The combined transmastoid retrolabyrinthine and Infralabyrinthine transjugular transcondylar transtubercular high cervical

Approach by route

TABLE 1. Review of literature on approaches to the jugular foramen.

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bulb. The jugular process of the occipital bone forms the posterior margin of the foramen. The jugular foramen is positioned between the occipitomastoid suture laterally and petro-occipital fissure medially (see Figure 1). The

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dome of the jugular bulb is located just below the vestibular labyrinth. The jugular foramen is divided into 3 parts: a petrosal part through which the petrosal sinus passes, a sigmoid

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part through which the sigmoid sinus passes, and an intrajugular part through which the nerves pass. The intrajugular part is positioned between the sigmoid and petrosal parts, and is the site of bony prominences called the intrajugular processes on the opposing surfaces of the temporal and occipital bones (Figure 1A). An intrajugular ridge extends forward from the intrajugular process of the temporal bone along the medial edge of the jugular bulb to meet the ridge along the posterior edge of the entrance into the carotid canal called the carotid ridge. The intrajugular ridge of the temporal bone is directed slightly medial and is the site of a shallow glossopharyngeal groove on its medial surface along which the glossopharyngeal nerve courses. The carotid ridge separates the jugular foramen and carotid canal and meets the styloid process near its lateral edge (Figures 1B and 1C). CNs IX, X, and XI pass through the intrajugular part of the jugular foramen. The dura covering the jugular foramen is divided by a dural fold into the glossopharyngeal and vagal meati. CN IX enters the glossopharyngeal meatus above and lateral to where CNs X and XI enter the vagal meatus. CN XII, after passing through the hypoglossal canal, joins CNs X and XI to descend with them in the carotid sheath (Figures 1D–1F). The occipital condyle is situated along the lateral margin of the anterior half of the foramen magnum in the area below and medial to the jugular foramen (Figures 1B and 1C). The occipital condyle is located anterior and inferior to a shallow depression, the condylar fossa, in which the posterior condylar emissary vein enters the posterior condylar canal to reach and empty into the sigmoid sinus. The jugular process of the occipital bone extends laterally from the area just above the posterior half of the occipital condyle and forms the posterior margin of the foramen. Removing the jugular process provides access to the posterior edge of the jugular bulb and internal jugular vein when combined with the lateral suboccipital approach, infralabyrinthine mastoidectomy, or cervical exposure. The occipitomastoid suture passes between the lateral edge of the jugular process and the medial edge of the digastric groove and styloid process to end at the jugular foramen (Figures 1B and 1C). The stylomastoid foramen, through which the facial nerve passes, is located just anterolateral to the jugular process.

The jugular bulb and adjacent part of the internal jugular vein receive drainage from both intracranial and extracranial veins, including the sigmoid and inferior petrosal sinuses, the vertebral venous plexus, the venous plexus of the hypoglossal canal, the posterior condylar emissary vein, and the vein coursing along the inferior aspect of the petro-occipital fissure. The inferior petrosal sinus communicates with the cavernous sinus and basilar venous plexus at its upper end and with the jugular bulb or the internal jugular vein at its lower end (Figure 1F).38

Multi-approach exposure of the jugular foramen No single previously reported operative approach provides access to the full margin of the jugular foramen, however, selection from among the reported approaches provides access to selective segments of all edges of the foramen depending on the approach selected. In evaluating this, the approaches exposing the anterior, lateral, and posterior surface of the foramen were performed on single specimens. It began with the postauricular transtemporal approach with a high cervical exposure to gain control of the internal carotid artery, internal jugular vein, and lower CNs below the jugular foramen. The initial step involved detaching the muscles attached to the mastoid process, including the sternocleidomastoid, semispinalis, longissimus, and digastric, to expose the occipital artery, rectus capitis lateralis, transverse process of C1, and suboccipital triangle. After this first step, the transverse process of C1, mastoid tip, parotid gland covering the facial nerve, and rectus capitis lateralis remain as obstacles to exposing the foramen (Figure 2A). Next, the infralabyrinthine mastoidectomy was performed to expose the superior and lateral aspects of the jugular bulb (Figure 2B). Removing the mastoid tip and extending the drilling downward along the occipitomastoid suture and exposing the sigmoid sinus accessed the attachment of the rectus capitis lateralis to the inferior surface of the jugular process. The sigmoid sinus crosses the occipitomastoid suture just before emptying into the jugular bulb. This surgical field is limited if the facial nerve is not transposed anteriorly and the jugular process is not removed (Figure 2C). Detaching the rectus capitis lateralis and removing the jugular process of the occipital bone opened the posteroinferior aspect of the jugular foramen and provided wide access for tumor

FIGURE 1. (A) Posterior superior view of the right jugular foramen. The foramen is divided into 3 parts: petrosal, sigmoid, and intrajugular. The intrajugular part, through which cranial nerves (CNs) IX, X, and XI pass, is the site of the intrajugular process and ridge, which separates the sigmoid and petrosal parts. The sigmoid sinus drains through the sigmoid part and the inferior petrosal sinus passes through the petrosal part. (B and C) Inferior view of the jugular foramen and jugular process. The occipital condyle is located anterior to the condylar fossa (interrupted line). The jugular process (green) is located posterior to the jugular foramen and extends laterally from the posterior half of the occipital condyle. The jugular fossa and foramen are positioned superior and lateral to the anterior half of the occipital condyle. (D) Posterior view, right cerebellopontine angle. The jugular foramen is located between the internal acoustic meatus and the jugular tubercle. The rectus capitis lateralis attaches to the inferior surface of the jugular process, which is located posterior to the jugular foramen. (E) Endoscopic view of the right jugular foramen. CNs IX, X, and XI pass through the intrajugular part of the foramen. The dural roof of the foramen is the site of the glossopharyngeal and vagal meati. A dural septum separates the 2 meati. (F) Lateral view of the intrajugular part of the left jugular foramen. The jugular bulb has been translocated posteriorly after removing all of the temporal bone except the petrous apex. The inferior petrosal sinus passes between the glossopharyngeal and vagus nerves to empty into the jugular bulb. The accessory nerve passes posterior to the vagus nerve. A., artery; Ac., acoustic; Atlanto-occip., atlantooccipital; Cap., capitis; Car., carotid; Cond., condylar, condyle; Fiss., fissure; Flocc., flocculus; For., foramen; Glossopharyng., glossopharyngeal; Hypogloss., hypoglossal; Inf., inferior; Int., internal; Intrajug., intrajugular; Jug., jugular; Lat., lateralis; Lt., left; M., muscle; Mag., magnum; Mast., mastoid; Meat., meatus; N., nerve; Occip., occipital; Occipitomast., occipitomastoid; Pet., petrosal; Petro-occip., petro-occipital; P.I.C.A., posterior inferior cerebellar artery; Proc., process; Pyramid., pyramidal; Rec., rectus; Rt., right; Sig., sigmoid; Styl., styloid; Stylomast., stylomastoid; Sup., superior; Temp., temporal; Tuberc., tubercle; Vag., vaginal; Vert., vertebral.

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removal without transposition of the facial nerve (Figure 2D). Extending the drilling medially above the jugular bulb exposes the cochlear aqueduct, which opens into the pyramidal fossa located medial to the glossopharyngeal groove of the temporal bone (Figures 1C and 2E). Next,

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several steps were added to widen the surgical field. The fallopian bridge technique in which the facial canal is skeletonized without transposition is completed to expose the junction of the inferior petrosal sinus, the jugular bulb, the area anterolateral to the jugular bulb, and the

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middle ear cavity (Figure 2E).27,39 An intracranial extension of the tumor can be accessed by opening the presigmoid or retrosigmoid dura. In the presigmoid approach, the otic capsule will rarely be an obstacle if the sigmoid sinus and the posterior fossa dura behind the cochlear canaliculus are exposed to provide access to the area between the jugular foramen and the nerves entering the internal acoustic meatus (Figure 2F). For the retrosigmoid approach, the superior oblique muscle is detached from the superior nuchal line and a lateral suboccipital craniectomy is completed to access the lower CNs intradurally (Figure 2G). The far lateral approach, a modification of the lateral suboccipital approach used to access the lower cerebellopontine angle and foramen magnum, was completed by drilling the edge of the foramen magnum up to the posterior edge of the occipital condyle (see Figure 3). The basic far lateral approach without drilling of the occipital condyle provides increased access to the entry of CNs IX, X, and XI into the dural roof and intrajugular part of the jugular foramen (Figures 3C and 3D).32 Detaching the muscles attached to the superior and inferior nuchal lines exposed the condylar fossa, vertebral artery, and surrounding venous plexus, which is continuous with the posterior condylar emissary vein passing through the condylar canal located superior to the occipital condyle (Figures 3A and 3B). From the posterior view, the insertion of the rectus capitis lateralis is identified medial to the occipital artery and digastric muscle. Opening the posterior edge of the jugular foramen extradurally required the removal of the jugular process, which extends laterally behind the jugular foramen (Figures 3C and 3E). The jugular process is removed after detaching the rectus capitis lateralis from its inferior surface to expose the posteroinferior surface of the jugular foramen, as described by Wen et al32 (Figure 3E). Drilling the occipital condyle and area above the condyle to expose the hypoglossal canal and its junction with the medial surface of the internal jugular vein adds minimally to the exposure of the foramen, is infrequently needed, and may result in cervicocranial instability requiring occipitocervical fusion (Figure 3E). The accessory nerve occasionally passes between the C1 transverse process and the internal jugular vein.40

The Fisch and Pillsbury12 and Fisch et al41 type A infratemporal fossa approach or Sekhar et al28 and Sen and Sekhar42 preauricular subtemporal infratemporal fossa approach, both lateral approaches, were utilized to access the anterolateral aspect of the jugular foramen. The preauricular subtemporal infratemporal fossa approach, as described by Sekhar et al,28 provides access to the middle and infratemporal fossae and the anterolateral aspect of the jugular bulb and makes it possible to translocate the petrous carotid anteriorly and access the petrous apex (Figures 4A and 4B). Removing the floor of the middle fossa around the foramen ovale, petrous carotid, inferior petrosal sinus, and the medial half of the inferior part of the vaginal process of the temporal bone exposed the anterior edge of the jugular bulb, carotid ridge, and exit site of the glossopharyngeal nerve (Figure 4B). Removing the styloid process allowed exposure of the anterolateral edge of the opening of the jugular bulb, however, care had to be taken to avoid injury of the facial nerve at this site. Recently, the jugular foramen has been exposed endoscopically.16,36,37,43 In this technique, dissection extended posteriorly along the eustachian tube via the transnasal/ transmaxillary and transpterygoid routes (Figure 4C). The eustachian tube is an important landmark for reaching the jugular foramen. After transecting the lateral pterygoid muscle, the medial pterygoid and tensor veli palatini muscles are reflected laterally to expose the eustachian tube, tubal attachment of the levator veli palatini muscle, and the stylopharyngeal fascia (aponeurosis), which covers the internal carotid artery, internal jugular vein, and lower CNs, and is opened to expose the area just below the jugular foramen. The internal carotid artery ascends just anteromedial to the internal jugular vein. CN IX descends laterally between the internal jugular vein and internal carotid artery after it exits the jugular foramen (Figure 4D). The vaginal process enclosing the base of the styloid process covers the anterolateral to lateral aspects of the junction of the internal jugular vein and jugular bulb (Figure 4D). Finally, after completing the far lateral approach, infralabyrinthine mastoidectomy, resection of the jugular process while preserving its inferior surface, and the

FIGURE 2. (A) High cervical exposure. The insert (upper left) shows the left postauricular C-shaped incision. The high cervical dissection has exposed the mastoid tip, rectus capitis lateralis, and suboccipital triangle (dotted line) between the superior and inferior oblique and rectus capitis posterior major muscles. (B) The infralabyrinthine mastoidectomy. Each semicircular canal has been exposed; superior (S), lateral (L), and posterior (P). The infralabyrinthine and retrofacial air cells have been removed to expose the jugular bulb. A posterior tympanotomy has been performed to facilitate exposure of the facial canal. (C) Removing the mastoid tip exposes the attachment of the rectus capitis lateralis to the inferior surface of the jugular process. To avoid injuring the facial nerve, the cuff of fibrous tissue encasing the nerve and the stylomastoid artery at the stylomastoid foramen have been preserved. (D) Removing the jugular process and rectus capitis lateralis exposes the posterior surface of the jugular bulb. The posterior condylar emissary vein connects the jugular bulb and the vertebral venous plexus. (E) Fallopian bridge technique, which leaves a thin shell of bone around the facial nerve. The drilling has been extended below the facial recess, and the bone between the facial canal (fallopian canal) and the posterior wall of the external auditory canal have been removed to provide a view into the middle ear and the anterolateral aspect of the jugular foramen. (F) Presigmoid exposure. The cochlear aqueduct has been exposed before opening the presigmoid dura. The dura in front of the sigmoid sinus has been opened to expose cranial nerves (CNs) VII to XI. (G) Retrosigmoid exposure. The dura behind the sigmoid sinus has been opened to expose CNs VII to XI. A., artery; A.I.C.A, anterior inferior cerebellar artery; Acc., accessory; Ant., anterior; Aque., aqueduct; Aud., auditory; Auric., auricular; Br., branch; Cap., capitis; Car., carotid; Chor., chorda, choroid; Cochl., cochlear; Cond., condylar; Dig., digastric; Emiss., emissary; Endolymph., endolymphatic; Ext., external; Flocc., flocculus; For., foramen; Gl., gland; Gr., greater; Inf., inferior; Int., internal; Jug., jugular; Lat., lateral, lateralis; Lev., lavator; M., muscle; Mast., mastoid; Meat., meatus; N., nerve; Obl., oblique; Occip., occipital; Occipitomast., occipitomastoid; Pet., petrosal; Plex., plexus; Post., posterior; Rec., rectus; Scap., scapulae; Sig., sigmoid; Stylomast., stylomastoid; Suboccip., suboccipital; Sup., superior; Surf., surface; Temp., temporal; Tymp., tympani, tympanic; V., vein.

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FIGURE 3. (A) Right suboccipital exposure with head in sitting position. Detaching the muscles from the superior and inferior nuchal lines exposes the suboccipital area, vertebral artery, area surrounding the vertebral venous plexus, and rectus capitis lateralis. (B) The craniotomy has been performed while preserving the cranial sutures. The condylar emissary vein, which connects with the vertebral venous plexus and sigmoid sinus, enters the posterior condylar canal in the condylar fossa. The rectus capitis lateralis attaches to the inferior surface of the jugular process. (C) The retrosigmoid exposure provides a view of cranial nerves (CNs) VII to XII. The cancellous bone above the occipital condyle has been drilled to expose the hypoglossal canal, which passes above the occipital condyle. The jugular process has been preserved. (D) Enlarged view of 3C. (E–G) Drilling of the occipital condyle to show that removing the condyle does not expose the posterior surface of the jugular bulb (E and F). Detaching the rectus capitis lateralis from the inferior surface of the jugular process exposes the carotid sheath, which encloses the internal jugular vein, carotid artery, and the accessory nerve. (G) Removing the jugular process exposes the posterior surface of the jugular bulb. The hypoglossal canal passes anterolaterally above the condyle. The venous plexus in the hypoglossal canal empties into the junction of the jugular bulb and the internal jugular vein. A., artery; Atlanto-occip., atlanto-occipital; Cap., capitis; Car., carotid; Cond., condylar, condyle; Dig., digastric; Emiss., emissary; Flocc., flocculus; For., foramen; Hypogloss., hypoglossal; Inf., inferior; Int., internal; Jug., jugular; Lat., lateralis; M., muscle; Mag., magnum; Maj., major; Min., minor; Obl., oblique; Occip., occipital; Occipitomast., occipitomastoid; Plex., plexus; Post., posterior; Proc., process; Rec., rectus; Sig., sigmoid; Styl., styloid; Sup., superior; Surf., surface; Trans., transverse; Tuberc., tubercle; V., vein; Ven., venous; Vert., vertebral.

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FIGURE 4. (A) The insert (upper left) shows the incision for the preauricular subtemporal infratemporal fossa exposure. The parotid gland is mobilized anteriorly while preserving the facial nerve. The middle fossa floor, mandibular condyle, and lateral pterygoid muscle have been removed to expose the infratemporal fossa and retromandibular space. Translocating the internal carotid artery forward and drilling part of the vaginal process of the tympanic part of the temporal bone exposes the anterior aspect of the jugular foramen, glossopharyngeal nerve, and carotid ridge. (B) Enlarged view of the exposure. The medial part of the vaginal process of the temporal bone has been drilled to expose the anterior part of the jugular foramen and the junction of the internal jugular vein and jugular foramen. The glossopharyngeal nerve descends just posterior to the carotid ridge into the neck. (C) Transnasal/transmaxillary transpterygoid approach to the jugular foramen. The insert (upper left) shows the right maxillary sinus and nasal cavity. The posterior wall of the right maxillary sinus has been removed, the sphenoid sinus is opened, and the lateral pterygoid muscle resected to expose the maxillary artery and the infratemporal and pterygopalatine fossae. (D) Retracting the medial pterygoid muscle and separating the tensor veli palatini from the eustachian tube and resecting it opens a corridor to the jugular foramen. Opening the stylopharyngeal aponeurosis exposes the internal carotid artery entering the carotid canal, and the internal jugular vein and glossopharyngeal nerve. A., artery; Apon., aponeurosis; Auric., auricular; Car., carotid; Cav., cavernous; Chor., chorda; CN, cranial nerve; Eust., eustachian; Fibrocart., fibrocartilage; Gang., ganglion; Gen., geniculate; Gl., gland; Gr., greater; Inf., inferior; Int., internal; Jug., jugular; Lev., levator; M., muscle; Max., maxillary; Mandib., mandibular; Med., medial; Men., meningeal; Mid., middle; N., nerve; Orb., orbital; Pal., palatine; Palat., palatini; Pet., petrosal; Proc., process; Pteryg., pterygoid; Sternocleidomast., sternocleidomastoid; Sphenopal., sphenopalatine; Stylopharyng., stylopharyngeal; Sup., superior; Temp., temporal; Tens., tensor; Tymp., tympani; V., vein; Vag., vaginal.

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preauricular subtemporal infratemporal fossa approach, the specimen was examined to determine the extent to which each approach added to the exposure of the jugular foramen (see Figure 5). This dissection shows that the external ear canal, facial canal, mastoid process, and root of the styloid process are obstacles to opening the jugular foramen completely and that resecting the jugular process provides wide access for the removal of tumor within the foramen

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(Figures 5B–5D). In the preauricular subtemporal infratemporal fossa approach, drilling the medial part of the vaginal process exposed the anterolateral part of the jugular bulb (Figures 5E and 5F), and resection of the styloid process widened this exposure. The lateral suboccipital approach combined with resection of the jugular process provided access to the jugular foramen both extracranially and intracranially, and widened the exposure of the posteroinferior

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aspect of the jugular bulb. Resection of the occipital condyle provided access to the hypoglossal canal, but did not increase the exposure of the jugular foramen (Figures 5G and 5H).

DISCUSSION Most jugular foramen schwannomas are approached by a lateral or posterior route. Some of these lateral and posterior approaches are similar but named differently, and some are a combination of previous approaches given new names (Table 1). This adds difficulty in selecting a surgical approach. The purpose of this study was to define the anatomic steps in the approaches to the jugular foramen. Among the operative steps involved in the approaches to the jugular foramen, resection of the jugular process is one of the most important. Wen et al,32 Nakamizo et al,25 Nakamizo et al,31 and Sanna et al44 described the importance of resection of the jugular process for exposing the posteroinferior surface of the jugular bulb (Figure 6A). It is reasonable to consider adding the removal of the jugular process if the tumor within the foramen extends posteriorly or occludes the bulb.3,6,8,14,17,19,21,23–26,29,30,45 Care should be taken to avoid injury to the facial nerve during drilling of the jugular process, because the stylomastoid foramen is located just lateral to the jugular process. Another important step is the infralabyrinthine mastoidectomy, which is commonly included in lateral or combined approaches but can also be included in a posterior approach (Table 1). The type A infratemporal fossa approach12,41 and preauricular subtemporal infratemporal fossa approaches,28,42 both lateral routes, provide access to the anterolateral and anterior edges of the jugular foramen. The jugular foramen is formed by the petrous part of the temporal bone anterosuperiorly and by the jugular process of the occipital bone posteroinferiorly. The vaginal process enclosing the base of the styloid process blocks access to the anterolateral to lateral aspects of the junction of the internal jugular vein and jugular bulb. The exposure of the anterolateral aspect of the jugular foramen is challenging

because the lower opening of the foramen is positioned just posterolateral to the carotid canal. Accessing the anterolateral aspect of the foramen may require translocation of the facial nerve, management of the petrous carotid artery, sacrifice of the external ear canal and middle ear, and drilling of the vaginal process. The approach described by Fisch and Pillsbury12 in 1979 provides superior, lateral, and anterior exposure of the jugular foramen and includes anterior translocation of the facial nerve and sacrifice of the external auditory canal and tympanic cavity as needed. Since then, others have modified and extended Fisch’s approach. Mazzoni and Sanna13 proposed the petro-occipital trans-sigmoid approach for posterolateral exposure of the jugular foramen, and Tedeschi and Rhoton14 introduced a postauricular transtemporal approach. Sanna et al44 reported the infratemporal fossa approach type A with transcondylar and transtubercular extension to obtain posteroinferior and medial access to the jugular bulb. In addition, a variety of other surgical approaches to the jugular foramen have been described.3,6–8,13,15–32,44–47 The endoscopic transnasal/ transmaxillary transpterygoid approach is an infrequently utilized anterior route. In our dissections, the external ear canal, facial canal, and root of the styloid process prevented the complete opening of the lateral aspect of the jugular foramen. The only area that cannot be opened without the transposition of the facial nerve is just medial to the root of the styloid process (Figures 5 and 6A). Complete resection of jugular foramen schwannomas is generally possible without anterior transposition of the facial nerve, which may cause facial nerve deficit.27,48 The transmastoid approach with sacrifice of the labyrinth and cochlea to enlarge the surgical field is rarely selected for jugular foramen schwannoma because preservation and improvement in hearing is common after tumor removal.49–51 Translocation of the vertebral artery, which ascends in the transverse foramen and runs horizontally behind the atlantal or occipital condyles, is not necessary. However, removal of the transverse process of the atlas is helpful

FIGURE 5. Multi-approach exposure of the jugular foramen. (A–H) The far lateral, preauricular transtemporal infratemporal, and transmastoid infralabyrinthine exposures have been completed on the right side to show the extent of exposure of the jugular bulb that can be achieved without resection of the external ear canal and translocation of the facial nerve. The parotid has been removed to make it easier to see the facial nerve and the area around the jugular foramen. The angle of view of each figure is shown in the insert using 3D coordinate axes. (A) Lateral view. The mastoid tip, styloid process, and external ear canal are obstacles to exposing the jugular foramen. (B) Posterolateral exposure viewed parallel to the external ear canal. The superior and lateral surfaces of the jugular bulb can be identified from this angle. In this view, the mastoid tip does not block access to the lateral aspect of the jugular bulb. However, the facial canal blocks access to the jugular bulb. (C) A 45o posterolateral view. The jugular process has been removed while preserving its inferior surface. Removing the jugular process exposes the posterior wall of the jugular bulb. (D) Rotating the view posteriorly provides a view of cranial nerves (CNs) IX, X, and XI entering the dural roof of the jugular foramen. (E) Lateral view of the preauricular subtemporal infratemporal fossa approach. The floor of the middle fossa has been removed and the medial half of the vaginal process of the tympanic part of the temporal bone drilled to expose the sigmoid sinus at the anterior edge of the jugular foramen. The parotid gland has been removed to facilitate the view of the anterior edge of the jugular foramen. (F) Superolateral view. The floor of the middle fossa lateral to the cochlea has been removed. The inferior petrosal sinus empties into the internal jugular vein just below the jugular bulb. The glossopharyngeal nerve descends through the dural glossopharyngeal meatus and turns downward lateral to the inferior petrosal sinus. (G) Lateral suboccipital (retrosigmoid) approach. This approach accesses the dural roof of the jugular foramen. Removing the jugular process of the temporal bone exposes the posterior and inferior surfaces of the jugular bulb. In this view, the vertebral artery partially blocks the view of the course of the accessory nerve. (H) View lateral to that shown in panel G. The intracranial, posterior/inferior surfaces of the jugular foramen, and hypoglossal canal have been exposed. The course of the accessory nerve is visible without translocation of the vertebral artery. A., artery; Atlanto-occip., atlanto-occipital; Aud., auditory; Car., carotid; Dig., digastric; Ext., external; Gr., greater; Hypogloss., hypoglossal; Inf., inferior; Int., internal; Jug., jugular; M., muscle; Mast., mastoid; Max., maxillary; N., nerve; Pet., petrosal; P.I.C.A., posterior inferior cerebellar artery; Post., posterior; Proc., process; Sig., sigmoid; Styl., styloid; Sup., superior; Surf., surface; Temp., temporal; Trans., transverse; V., vein; Vert., vertebral.

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FIGURE 6. (A) Inferior view of jugular foramen. The site of the jugular bulb (dark blue), internal carotid artery (red), and sigmoid sinus (light blue) are shown on an image of the lower surface of the right jugular foramen. The margin of the foramen exposed by removal of the jugular process is shown (green). The area exposed by the preauricular infratemporal approach is along the anterolateral edge of the foramen (solid black line) and removal of the vaginal process of the tympanic part (black interrupted line) allows anterior transposition of the carotid artery and drilling of the anterior margin of the foramen. (B) Anterior view of the posterior face of a coronal section through the skull posterior to the right external acoustic meatus at the level of the white line shown in the insert in the upper corner of panel B. The infralabyrinthine mastoidectomy opens a wide area from the top of the dome to the lateral side of the jugular bulb (solid purple line in panel B). The cervical exposure provides access to the internal jugular vein below the foramen (interrupted purple line in panel B). The lateral suboccipital approach (retrosigmoid exposure) can access the jugular foramen intracranially (orange circle area in panel B). A., artery; Ac., acoustic; CN, cranial nerve; Car., carotid; Cond., condyle; Int., internal; JF, jugular foramen; Jug., jugular; Mand., mandibular; Mast., mastoid; Meat., meatus; N., nerve; Occip., occipital; Pet., petrosal; Proc., process; Sig., sigmoid; Stylomast., stylomastoid; V., vein.

because it widens the surgical field posterior to the sigmoid sinus and internal jugular vein and the lower CNs without translocation of the vertebral artery.25,45 Removing the occipital condyle without resection of the jugular process does not aid in opening the jugular fossa and is unnecessary.32 Resection of the posterolateral edge of the condyle may prove helpful in exposing the posteromedial edge of the internal jugular vein, but removing more than the posterior one third of the condyle may cause craniocervical instability. Sacrifice of the sinus with ligation of both the sigmoid sinus and internal jugular vein and opening the jugular bulb, developed for glomus jugulare tumors in the region, may infrequently be considered for achieving complete removal of the jugular foramen schwannoma occluding the sinus.6

Approaches based on tumor type The key steps to expose the contents of the foramen and jugular bulb are the infralabyrinthine mastoidectomy and/or resection of the jugular process, which may be combined with the lateral suboccipital approach or a postauricular transtemporal approach and/or cervical exposure. The selection of which procedures should be selected is based on the pattern of growth of an intraforaminal tumor. Infralabyrinthine mastoidectomy would be added if the foraminal part of the tumor extends into the infralabyrinthine area and pushes the jugular bulb inferiorly. Resection of the jugular process would be added if the tumor extends posteroinferiorly. The combined infralabyrinthine and jugular process resection can add a much wider field for resection of foraminal tumors.

The lateral suboccipital approach has a variety of modifications. The far lateral extension will aid in removing tumors extending anterior to the lower brainstem.20 For foraminal tumors with intracranial growth, the lateral suboccipital approach may be combined with infralabyrinthine mastoidectomy and/or removal of the jugular process. The petro-occipital trans-sigmoid approach utilizes a combination of a retrolabyrinthine and infralabyrinthine mastoidectomy and the lateral suboccipital approach with sacrifice of the sigmoid sinus.13 This approach can access the intracranial, foraminal, and cervical pathology while preserving facial nerve function, and the external auditory canal, tympanic cavity, and labyrinth.52 If a type A (intracranial) tumor has some extension into only the upper part of the foramen, the suprajugular extension, in which only the medial part of the roof of the jugular foramen is removed, may allow complete tumor removal.26,53 Recently, an endoscopic retrosigmoid approach that includes drilling only the roof of the foramen in the area below the internal acoustic meatus has been developed that may allow complete removal of a tumor with small extension into the foramen.54 The infralabyrinthine mastoidectomy provides access along the dome and lateral side of the jugular bulb.15,55 When a tumor within the jugular fossa extends upward above the bulb or displaces the jugular bulb inferiorly without extension intracranially, the infralabyrinthine mastoidectomy is a good option but provides only limited space for accessing the tumor and should often be combined with another approach to widen the exposure. For a type B (foraminal) tumor with some intracranial extension, an infralabyrinthine mastoidectomy combined with HEAD & NECK—DOI 10.1002/HED

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the presigmoid exposure, which allows minimum retraction of the cerebellum, is a good option for removing tumors extending anteromedially or superiorly in the area between the acoustic meatus and jugular foramen.6,15,47 High cervical exposure will provide access to the area just below the jugular foramen, but is often combined with the infralabyrinthine mastoidectomy and/or resection of the jugular process for a tumor within the foramen that extends downward into the high cervical area, or a primarily extracranial tumor that extends upward into the foramen. This combination, which includes the Kaye et al,7 Lambert et al,22 and Gardner et al17 approaches and was originally called the infralabyrinthine approach, can provide a wide exposure from the top of the jugular bulb to the neck (Figure 6B). Jugular foramen schwannomas often involve several regions; A1B, B1C, and D tumors. The reported approaches for type D tumors are combined approaches, which include the lateral suboccipital approach and cervical exposure combined with infralabyrinthine mastoidectomy and/or jugular process resection.14,18,21,23,45 Almost all reported approaches added resection of the jugular process. However, previous studies have reported that the transcondylar suprajugular approach with preservation of the wall of the jugular bulb usually results in preservation of its patency after tumor removal even if the preoperative studies revealed an absence of its flow into the jugular bulb.6,56,57 Generally, an approach with modifications to widen the surgical field is advantageous. Cervical exposure combined with an infralabyrinthine mastoidectomy and resection of the jugular process can provide a wide surgical field that can be enlarged further through a variety of modifications, including the fallopian bridge technique without translocation of the facial nerve, which provides more surgical space and improves the visualization for the tumor extending to the hypotympanum or anterolateral part of the jugular bulb. If the tumor extends intracranially, the retrosigmoid or presigmoid approach can be added. If the tumor extends in the direction of the petrous apex and encases the petrous carotid, it may be necessary to translocate the facial nerve after resecting the external ear canal as in Fisch’s type A infratemporal fossa approach.11,12,41 If facial nerve translocation is needed, preserving the stylomastoid artery and a fascial cuff around the facial nerve will aid in avoiding facial paralysis. However, the most effective way to preserve the function of the facial nerve is to avoid opening the facial canal. If the schwannoma cannot be separated from the jugular bulb or internal jugular vein, sacrifice of the bulb after ligation of both the sigmoid sinus and internal jugular vein can be added to enlarge the surgical field if preoperative studies show compromised flow through the foramen. If a foraminal schwannoma extends anteriorly, a type A infratemporal fossa approach or preauricular subtemporal infratemporal fossa approach can be used to expose the anterolateral aspects of the foramen. An endoscopic transnasal/transmaxillary transpterygoid approach may be considered for tumors that extend to the infratemporal fossa and along the petrous portion of the internal carotid artery through the eustachian tube, or to the cancellous portion E1052

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of the petrous apex. However, the application of this approach is limited and should be considered only if the tumor occupies the infratemporal fossa and creates a surgical corridor by displacing the carotid artery and internal jugular vein posteriorly, and only minimum dissection of the pterygoid muscles is required.16,36,37 Foraminal and intracranial tumors with anterior extension are difficult to approach. Sanna et al44 proposed that the type A infratemporal fossa approach be combined with the transjugular, transcondylar, and transtubercular extensions to treat Fisch’s type C2 to C4 tympanojugular paraganglioma, with some technical refinements, which includes the anterior rerouting of the facial nerve creating a new bony canal using fibrin glue, and the extraluminal compression of the sigmoid sinus with Surgicel (Johnson & Johnson, Piscataway, NJ) as compared to the type A infratemporal fossa approach. This extension allows posteroinferior and medial access in addition to the superior and anterolateral exposure of the foramen. Schwannomas rarely extend anteriorly with infiltration of the wall of the petrous carotid artery. However, if the schwannoma expands aggressively from the intracranial and foraminal areas to the petrous apex along with the petrous carotid artery, this approach should be considered.

CONCLUSION Selecting the best approach from among the numerous reported approaches should be based on the preoperative examinations showing the size and location of these tumors. Care should be taken to avoid injury to the CNs, because jugular foramen schwannomas are mostly benign and slow-growing and usually cause minimal CN deficits. A precise understanding of each approach and the complex anatomy involved of the jugular foramen is important in achieving complete removal of tumors while minimizing risk.

Acknowledgments The authors appreciate Ms. Robin Barry for assistance with the preparation of the illustrations and Ms. Jessica Striley for editorial assistance.

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