Jugular Foramen

Albert L. Rhoton, Jr., M.D.

Department of Neurological Surgery, University of Florida, Gainesville, Florida

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The jugular foramen is difficult to understand and to access surgically (3, 11, 15, 19, 24, 28). It is difficult to conceptualize because it varies in size and shape in different crania, from side to side in the same cranium, and from its intracranial to extracranial end in the same foramen, and because of its complex irregular shape, its curved course, its formation by two bones, and the numerous nerves and venous channels that pass through it (Fig. 9.1 A-D, 9.1 E-H). The difficulties in exposing this foramen are created by its deep location and the surrounding structures, such as the carotid artery anteriorly, the facial nerve laterally, the hypoglossal nerve medially, and the vertebral artery inferiorly, all of which block access to the foramen and require careful management. The jugular foramen is divided into three compartments: two venous and a neural or intrajugular compartment. The venous compartments consist of a larger posterolateral venous channel, the sigmoid part, which receives the flow of the sigmoid sinus, and a smaller anteromedial venous channel, the petrosal part, which receives the drainage of the inferior petrosal sinus. The petrosal part forms a characteristic venous confluens by also receiving tributaries from the hypoglossal canal, petroclival fissure, and vertebral venous plexus. The petrosal part empties into the sigmoid part through an opening in the medial wall of the jugular bulb between the glossopharyngeal nerve anteriorly and the vagus and accessory nerves posteriorly. The intrajugular or neural part, through which the glossopharyngeal, vagus, and accessory nerves course, is located between the sigmoid and petrosal parts at the site of the intrajugular processes of the temporal and occipital bones, which are joined by a fibrous or osseous bridge. The glossopharyngeal, vagus, and accessory nerves penetrate the dura on the medial margin of the intrajugular process of the temporal bone to reach the medial wall of the internal jugular vein. The operative approaches that access various aspects of the foramen and adjacent areas are the postauricular transtemporal, retrosigmoid, extreme lateral transcondylar, and preauricular subtemporal-infratemporal approaches.

OSSEOUS RELATIONSHIPS

The jugular foramen is located between the temporal bone and the occipital bone (Figs. 9.1 A-D, 9.1 E-H and 9.2). The right foramen is usually larger than the left. In a previous study, we observed that the right foramen was larger than the left in 68% of the cases, equal to the left in 12%, and smaller than the left in 20% (24). The foramen is configured around the sigmoid and inferior petrosal sinuses. It can be regarded as a hiatus between the temporal and the occipital bones. The structures that traverse the jugular foramen are the sigmoid sinus and jugular bulb, the inferior petrosal sinus, meningeal branches of the ascending pharyngeal and occipital arteries, the glossopharyngeal, vagus, and accessory nerves with their ganglia, the tympanic branch of the glossopharyngeal nerve (Jacobson's nerve), the auricular branch of the vagus nerve (Arnold's nerve), and the cochlear aqueduct. The foramen is situated so that its long axis is directed from posterolateral to anteromedial, giving it an anterolateral margin formed by the temporal bone and a posteromedial margin formed by the occipital bone. From the intracranial end, it is directed forward, medially, and downward. One cannot see through the foramen when viewing the skull from directly above or below because of its roof, formed by the lower surface of the petrous part of the temporal bone. The foramen, when viewed from the intracranial side in a posterior to anterior direction, has a large oval lateral component, referred to as the sigmoid part, because it receives the drainage of the sigmoid sinus, and a small medial part, called the petrosal part, because it receives the drainage of the inferior petrosal sinus. The view through the foramen from directly below reveals the part of the temporal bone forming the dome of the jugular bulb, rather than a clear opening. The junction of the sigmoid and petrosal parts is the site of bony prominences on the opposing surfaces of the temporal and occipital bones, called the intrajugular processes, which are joined by a fibrous, or less commonly, and osseous bridge, the intrajugular septum, separating the sigmoid and petrosal part of the foramen. Although the margins of the jugular foramen are formed by the petrosal part of the temporal bone and the condylar part of the occipital bone, the other parts of these bones also have important relationships to the jugular foramen. The petroclival fissure, the fissure between the lateral edge of the clival part of the occipital bone and the petrous part of the temporal bone, intersects the

anteromedial edge of the foramen, and the occipitomastoid suture, the suture between the mastoid portion of the temporal bone and the condylar part of the occipital bone, intersects its posterolateral edge. The intrajugular processes of the temporal and occipital bones divide the anterior and posterior edges of the foramen between the sigmoid and petrosal parts. The intrajugular process of the temporal bone protrudes farther into the jugular foramen than the opposite process from the occipital bone, and may infrequently reach the smaller intrajugular process of the occipital bone, dividing the jugular foramen into two bony foramina. A ridge, the intrajugular ridge, extends forward from the intrajugular process of the temporal bone along the medial edge of the jugular bulb (Fig. 9.1 A-D, 9.1 E-H). The glossopharyngeal nerve courses along its medial edge. Occasionally, the edge of this ridge extends medially toward the adjacent part of the temporal bone to create a deep groove in which the nerve courses or it may reach the temporal bone to form a canal, which surrounds the glossopharyngeal nerve as it passes through the jugular foramen. The drainage of the sigmoid sinus is directed forward into the sigmoid portion of the foramen, where a high domed recess, the jugular fossa, forms a roof over the top of the jugular bulb (Figs. 9.1 A-D, 9.1 E-H and 9.3). This recess, which has its summit slightly lateral to the entrance of the sigmoid sinus, is usually larger on the right side of the skull, reflecting the larger sigmoid sinus on that side. The dome of the recess is usually smooth as it conforms to the jugular bulb, but the summit may also be ridged and irregular. A small triangular recess, the pyramidal fossa, extends forward on the medial side of the intrajugular process of the temporal bone along the anterior wall of the petrosal part of the foramen. The external aperture of the cochlear canaliculus, which houses the perilymphatic duct and a tubular prolongation of the dura mater, opens into the anterior apex of the pyramidal fossa. The glossopharyngeal nerve enters this fossa below the point at which the cochlear aqueduct joins its apex. The jugular process of the condylar portion of the occipital bone, which extends behind the jugular foramen and connects the clival and squamosal parts of the occipital bone, forms the posteromedial wall of the foramen. This process extends laterally from the area above the posterior half of the occipital condyle and is penetrated by the hypoglossal canal. The upper surface of the jugular process of the occipital bone in the area superomedial to the foramen presents an oval prominence, the jugular tubercle, which is located above the hypoglossal canal. The jugular tubercle often has a shallow furrow marking the site of passage of the glossopharyngeal, vagus, and accessory nerves

across its surface. The terminal end of the sigmoid sinus courses forward on the superior surface of the jugular process in a deep hook-like groove, the sigmoid sulcus, which is directed medially into the sigmoid portion of the jugular foramen. On the lateral wall of the jugular foramen, a few millimeters inside the external edge, just behind the point at which the occipitomastoid suture crosses the lateral edge of the foramen, is a small foramen, the mastoid canaliculus, and a shallow groove leading from medial to lateral across the anterior wall of the sigmoid part to the mastoid canaliculus (Figs. 9.2 and 9.3). The auricular branch of the vagus nerve (Arnold's nerve) courses along the groove and enters the canaliculus. The nerve passes through the mastoid and exits the bone in the inferolateral part of the tympanomastoid suture. At the site where the intrajugular ridge of the temporal bone meets the carotid ridge, a small canal, the tympanic canaliculus, is directed upward, leading the tympanic branch arising from the inferior glossopharyngeal ganglion (Jacobson's nerve) to the tympanic cavity (Figs. 9.2). Looking from below at the extracranial orifice of the jugular foramen, it can be recognized that the glossopharyngeal nerve courses along the medial side of the intrajugular process and ridge to reach the area below the tympanic canaliculus.

ADJACENT BONY STRUCTURES

On the intracranial side, the petrosal part of the foramen is located approximately 5 mm below the porus of the internal canal and 5 mm above the intracranial orifice of the hypoglossal canal (Figs. 9.2 and 9.4 A-D, 9.4 E-H, 9.4 I-N). The lateral edge of the foramen is located below and in approximately the sagittal plane through the lateral end of the internal acoustic meatus. The jugular tubercle, a rounded prominence located at the junc tion of the basal and condylar parts of the occipital bone, is situated approximately 8 mm medial to the medial edge of the jugular foramen. The otic capsule, which is situated in the petrous part of the temporal bone and which contains the semicircular canals and cochlea, is located superior to the dome of the jugular bulb. The occipital condyle is located along the lateral margin of the anterior half of the foramen magnum in the area below and medial to the jugular foramen. The hypoglossal canals, which pass through the condylar part of the occipital bone in the area above the occipital condyles, are located medial to the jugular foramina (Figs. 9.1 A-D, 9.1 E-H and 9.3). The intracranial end of the hypoglossal canal is situated below the jugular tubercle approximately 5

mm inferomedial to the petrosal part of the jugular foramen and several millimeters below the lower part of the petroclival fissure. A more detailed review is included in the chapter on the far-lateral approach. The anterior margin of the jugular foramen, when viewed extracranially, is formed by the narrow ridge of temporal bone, the carotid ridge, which separates the foramen and the carotid canal (Figs. 9.1 A-D, 9.1 E-H and 9.2). The tympanic canaliculus opens on or near the medial part of the carotid ridge. The styloid process and the stylomastoid foramen are located lateral to the outer orifice of the jugular foramen, with the styloid process being located slightly anteromedial to the stylomastoid foramen. The facial nerve exits the stylomastoid foramen approximately 5 mm lateral to the lateral edge of the jugular foramen. The anterior margin of the jugular foramen is located just behind the part of the tympanic bone that forms the posterior wall of the temporomandibular joint and the anterior and inferior wall of the external auditory canal. The vaginal process of the tympanic bone, which separates both the carotid canal and sigmoid part of the foramen from the glenoid fossa, is the site of attachment of the styloid process to the skull base. The styloid process projects downward from the vaginal process of the tympanic bone, lateral to the foramen. The digastric groove is directed posteriorly from the styloid process along the medial margin of the mastoid process. Access to the jugular foramen is blocked laterally by mastoid and styloid processes, the transverse process of the atlas, and the mandibular ramus (Figs. 9.3 and 9.4 A-D, 9.4 E-H, 9.4 I-N). The tympanic cavity, which is located medial to the tympanic membrane, is situated above and lateral to the jugular bulb and the sharp right-angled curve, called the lateral bend, at the junction of the vertical and horizontal segments of the petrous carotid artery (Figs. 9.4 A-D, 9.4 E-H, 9.4 I-N). Several structures that may be exposed during surgery for lesions in the jugular foramen are the vertical and horizontal segments of the petrous portion of the internal carotid artery, the eustachian tube, and the tensor tympani muscle. Both the cochlea and semicircular canals are located in the petrous part of the temporal bone above the dome of the jugular bulb (Figs. 9.4 A-D, 9.4 E-H, 9.4 I-N). The facial nerve in the temporal bone, which often blocks access to lesions in the jugular foramen, descends through the mastoid lateral to the jugular bulb. The endolymphatic sac is situated on the posterior surface of the petrous bone between the two layers of the dura in the corner at which the sigmoid sinus changes its course from a vertical direction to a horizontal one (Figs. 9.3 and 9.5).

Dural architecture

At the intracranial orifice, the jugular foramen is divided into three compartments by the dura mater: the petrosal compartment situated anteromedially, the sigmoid compartment situated posterolaterally, and the intrajugular or neural compartment situated between the petrosal and sigmoid parts at the site of the intrajugular processes of the temporal and occipital bones, the intrajugular septum, and the glossopharyngeal, vagus, and accessory nerves (Figs. 9.3 and 9.5). The dura over the intrajugular part of the foramen, which is located anteromedial to the sigmoid part, has two characteristic perforations, a glossopharyngeal meatus, through which the glossopharyngeal nerve passes, and a vagal meatus, through which the vagus and accessory nerves pass (Figs. 9.5 and 9.6) (24). Both meatus are located on the medial side of the intrajugular processes and septum. The glossopharyngeal and vagal meatus are consistently separated by a dural septum ranging in width from 0.5 to 4.9 mm (13). The only intradural site at which the glossopharyngeal nerve is consistently distinguishable from the vagus nerve is just proximal to this dural septum. The close origins of the glossopharyngeal and vagus nerves at the brainstem, and the arachnoidal adhesions between the two in their course through the subarachnoid space may make separation difficult except in the area just proximal to the dural septum. The superior glossopharyngeal ganglion is easily visible intracranially in about one-third of nerves. The superior ganglion of the vagus can be seen intracranially in only one-sixth of nerves. Although the cranial and spinal portions of the accessory nerve most frequently enter the vagal meatus together, a dural septum may separate them. The upper and lateral margins of the intrajugular part of the foramen are the site of a characteristic thick dural fold that forms a roof or lip that projects inferiorly and medially to partially cover the glossopharyngeal and vagal meatus (Figs. 9.5 and 9.6). This structure, called the jugular dural fold, was ossified on both sides in one specimen (13, 16, 17, 24, 31). The lip projects most prominently over the glossopharyngeal meatus and is comparable to, but smaller than, the posterior lip of the internal acoustic meatus. It is either predominantly bony or fibrous and may project a maximum of 2.5 mm over the margin of the glossopharyngeal meatus. The vagal lip is less prominent, projecting a maximum of 1 mm over the lateral margin of the vagal meatus.

Neural relationships

The glossopharyngeal, vagus, and accessory nerves arise from the medulla as a line of rootlets situated along the posterior edge of the inferior olive in the postolivary sulcus (Figs. 9.3 and 9.5). The hypoglossal nerve arises as a line of rootlets that exit the brainstem along the anterior margin of the lower two-thirds of the olive in the preolivary sulcus, a groove between the olive and medullary pyramid. The glossopharyngeal nerve, at the point at which it penetrates the dural glossopharyngeal meatus, turns abruptly forward and then downward and courses through the jugular foramen in the groove leading from the pyramidal fossa below the opening of the cochlear aqueduct and along the medial side of the intrajugular ridge. After the nerve exits the jugular foramen, it turns forward, crossing the lateral surface of the internal carotid artery deep to the styloid process. As the nerve transverses the jugular foramen, it expands at the site of its superior and inferior ganglia (Fig. 9.5). At the external orifice of the jugular foramen, it gives rise to the tympanic branch (Jacobson's nerve), which traverses the tympanic canaliculus to enter the tympanic cavity where it gives rise to the tympanic plexus, the fibers of which course in shallow grooves on the promontory and regroup to form the lesser petrosal nerve, providing parasympathetic innervation by way of the otic ganglion to the parotid gland. The vagal rootlets enter the dural subcompartment, called the vagal meatus, inferior to the glossopharyngeal meatus from which it is separated by a dural septum (Figs. 9.5 and 9.6). It is joined by the accessory nerve as it enters the dura. After its rootlets gather in the intracranial orifice of the foramen, the vagus nerve expands at the superior ganglion, which is about 2.5 mm in length, and ends below the extracranial orifice of the foramen. It sits on the dura, covering the jugular foramen, and there, along the medial side of the intrajugular process of the temporal bone, it turns downward. At the superior ganglion, the vagus nerve communicates with the accessory nerve, a portion of which blends into the ganglion. The auricular branch (Arnold's nerve) arises at the level of the superior vagal ganglion and is joined by a branch from the inferior glossopharyngeal ganglion (Fig. 9.3). The auricular branch passes laterally in a shallow groove on the anterior wall of the jugular bulb to reach the lateral wall of the jugular fossa, where it enters the mastoid canaliculus and ascends toward the vertical (mastoid) segment of the facial canal, giving off an ascending branch to the facial nerve as it crosses lateral to it before turning downward to exit the temporal bone through the tympanomastoid fissure.

The main trunk of the vagus nerve (or, more accurately, the superior ganglion) courses anterior and inferior as it crosses below the midportion of the intrajugular process of the temporal bone (Figs. 9.3 and 9.5). At the intracranial orifice of the foramen, the intrajugular process of the temporal bone separates the ganglion from the sigmoid sinus. In most cases, in the area immediately below the dura at the level of the intrajugular processes, there are no fibrous bands between the glossopharyngeal nerve and the vagal ganglion. The vagus nerve exits the jugular foramen vertically, retaining an intimate relationship to the accessory nerve (Figs. 9.3, 9.4 A-D, 9.4 E-H, 9.4 I-N, 9.5). At the level the two nerves exit the jugular foramen, they are located behind the glossopharyngeal nerve on the posteromedial wall of the internal jugular vein. As the vagus nerve passes lateral to the outer orifice of the hypoglossal canal, it is joined by the hypoglossal nerve medially. The vagus nerve begins to expand at the site of the inferior vagal ganglion just below the foramen and is approximately 2.5 cm in length.

Accessory nerve

Although the cranial and spinal portions of the accessory nerve most frequently enter the vagal meatus together, they may infrequently be separated by a dural septum. The spinal portion ascends toward the foramen magnum by crawling along the surface of the dura and may even be buried in the dura below the foramen magnum (Figs. 9.3, 9.5, and 9.6). At the dural orifice of the jugular foramen, the nerve is often indistinguishable from the vagus nerve. The accessory nerve usually enters the same dural subcompartment as the vagus nerve and often adheres and blends into the vagus nerve at the level of the superior vagal ganglion. The accessory nerve departs the vagal ganglion after it exits the jugular foramen and descends obliquely laterally between the internal carotid artery and internal jugular vein and then backward across the lateral surface of the vein to reach its muscles. Approximately 30% of nerves descend along the medial, rather than the lateral, surface of the internal jugular vein (8).

Hypoglossal nerve

The hypoglossal nerve does not traverse the jugular foramen (Figs. 9.3, 9.4 A-D, 9.4 E-H, 9.4 I-N, 9.5). However, it joins the nerves exiting the jugular foramen just below the skull and runs with them in the carotid sheath. The nerve exits the inferolateral part of the hypoglossal canal and passes adjacent

to the vagus nerve, descends between the internal carotid artery and the internal jugular vein to the level of the transverse process of the atlas, where it turns abruptly forward along the lateral surface of the internal carotid artery toward the tongue, leaving only the ansa cervicalis to descend with the major vessels.

ARTERIAL RELATIONSHIPS

The arteries that may be involved in pathological abnormalities at the jugular foramen include the upper cervical and petrous portions of the internal carotid artery, the posteriorly directed branches of the external carotid artery, and the upper portion of the vertebral artery (9.4 A-D, 9.4 E-H, 9.4 I-N).

Internal carotid artery

The internal carotid artery passes, almost straightly upward, posterior to the external carotid artery and anteromedial to the internal jugular vein, to reach the carotid canal (9.4 A-D, 9.4 E-H, 9.4 I-N). At the level of the skull base, the internal jugular vein courses just posterior to the internal carotid artery, being separated from it by the carotid ridge. Between them, the glossopharyngeal nerve is located laterally and the vagus, accessory, and hypoglossal nerves medially. After the internal carotid artery enters the carotid canal with the carotid sympathetic nerves and surrounding venous plexus, it ascends a short distance (the vertical segment), reaching the area below and slightly behind the cochlea, where it turns anteromedially at a right angle (the site of the lateral bend) and courses horizontally (the horizontal segment) toward the petrous apex (9.4 A-D, 9.4 E-H, 9.4 I-N). At the medial edge of the foramen lacerum, it turns sharply upward at the site of the medial bend to enter the posterior part of the cavernous sinus.

External carotid artery

The external carotid artery ascends anterior to the internal carotid artery. Proximal to its terminal bifurcation into the maxillary and the superficial temporal arteries, it gives rise to six branches, which can be divided into

anterior and posterior groups according to their directions. The latter group is related to the jugular foramen. The ascending pharyngeal artery, the first branch of the posterior group, often provides the most prominent supply to the meninges around the jugular foramen (9.4 A-D, 9.4 E-H, 9.4 I-N) (18). It arises either at the bifurcation or from the lowest part of the external or internal carotid arteries. Rarely it arises from the origin of the occipital artery. It courses upward between the internal and the external carotid arteries, giving rise to numerous branches to neighboring muscles, nerves, and lymph nodes. Its meningeal branches pass through the foramen lacerum to be distributed to the dura lining the middle fossa and through the jugular foramen or the hypoglossal canal to supply the surrounding dura of the posterior cranial fossa. The ascending pharyngeal artery also gives rise to the inferior tympanic artery, which reaches the tympanic cavity by way of the tympanic canaliculus along with the tympanic branch of the glossopharyngeal nerve. The occipital artery, the second and largest branch of the posterior group, arises from the posterior surface of the external carotid artery and courses obliquely upward between the posterior belly of the digastric muscle and the internal jugular vein (9.4 A-D, 9.4 E-H, 9.4 I-N). Its meningeal branches, which enter the posterior fossa through the jugular foramen or the condylar canal, may make a significant contribution to tumors of the jugular foramen. The posterior auricular artery, the last branch in the posterior group, arises above the posterior belly of the digastric muscle and travels between the parotid gland and the styloid process. At the anterior margin of the mastoid process, it divides into auricular and occipital branches, which are distributed to the postauricular and the occipital regions respectively. The stylomastoid branch, which arises below the stylomastoid foramen, enters the stylomastoid foramen to supply the facial nerve. Its loss can lead to a facial palsy even though it anastomoses with the petrosal branch of the middle meningeal artery. The posterior auricular branch may share a common trunk with the occipital artery, or sometimes it is absent, in which case, the occipital artery gives rise to the stylomastoid artery. Members of the anterior group, whose origins may be visualized in exposing lesions of the jugular foramen, include the superior thyroid, lingual, and facial arteries.

Vertebral artery

The vertebral artery, as it ascends to reach and pass through the transverse foramen of the atlas, is located below and behind the jugular foramen (9.4 A-

D, 9.4 E-H, 9.4 I-N). Branches encountered in approaches to lesions of the jugular foramen include the meningeal, posterior spinal, and posteroinferior cerebellar artery.

VENOUS RELATIONSHIPS

The jugular bulb and adjacent part of the internal jugular vein receives drainage from both intracranial and extracranial sources, which include 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 petroclival fissure (9.4 A-D, 9.4 E-H, 9.4 I-N and 9.5).

Sigmoid sinus and jugular bulb

The sigmoid sinus is the largest channel emptying into the jugular foramen (Figs. 9.1 A-D, 9.1 E-H and 9.3, 9.4 A-D, 9.4 E-H, 9.4 I-N, 9.5). After coursing down the sigmoid sulcus, the sinus turns anteriorly toward the jugular foramen, crossing the occipitomastoid suture immediately proximal to the foramen. From there, the sinus is directed forward below the petrous temporal bone at the site of the jugular bulb. The upward bulging of the superior margin of the jugular bulb creates a rounded fossa in the lower surface of the temporal bone below the internal auditory canal. The dome of the jugular bulb may extend upward in the posterior wall of the internal auditory canal to the level of the upper margin of the canal. The bulb is usually larger on the right side, reflecting the larger diameter of the sigmoid sinus on that side. From the level of the jugular bulb, flow is directed downward behind the tympanic bone and the carotid canal into the internal jugular vein.

Inferior petrosal sinus and venous confluens

The foramen also receives the inflow from the inferior petrosal sinus and the venous confluens in the petrosal part of the foramen. The inferior petrosal sinus, which courses on the intracranial surface of the petroclival fissure, communicates the cavernous sinus and basilar venous plexus at its upper end and with the jugular bulb at its lower end (Figs. 9.3 and 9.5). The inferior petrosal sinus, as it enters the petrosal part of the jugular foramen, forms a plexiform confluens with the venous plexus of the hypoglossal canal, the

inferior petroclival vein, and tributaries from the vertebral venous plexus and posterior condylar emissary vein. This confluens, which fills the petrosal part of the foramen, usually consists of a main channel, 2 to 3 mm in diameter, and several smaller channels, less than 1 mm in diameter. It empties into the medial aspect of the jugular bulb through one or two openings in the venous walls between the glossopharyngeal and vagus nerves or into the internal jugular vein below the extracranial orifice. The inferior petroclival vein courses along the extracranial surface of the petroclival fissure and is a mirror image of the inferior petrosal sinus, which courses along the intracranial surface of the fissure (Fig. 9.5). It empties into the venous confluens at the lower end of the inferior petrosal sinus at or just below the extracranial orifice of the jugular foramen or even above it, through bony clefts between the temporal and occipital bones.

Bridging veins

A bridging vein, which courses posterior to the glossopharyngeal, vagus, and accessory nerves from the dorsolateral medulla to the lower end of the sigmoid sinus, is present in about one-third of cerebellopontine angles (Fig. 9.5, also see Fig. 3.12). Infrequently, a bridging vein extends from the ventral medulla to the lower margin of the inferior petrosal sinus in front of the nerves.

MUSCULAR RELATIONSHIPS

Several muscles that are encountered in the surgical approaches to the jugular foramen and that provide important landmarks in the approach are reviewed in detail in the chapters on the foramen magnum and temporal bone (9.4 A-D, 9.4 E-H, 9.4 I-N). These include the sternocleidomastoid, situated superficially in the lateral neck, and the splenius capitis, longissimus capitis, levator scapulae, and scalenus medius muscles in a deeper muscular layer. More anteriorly is the posterior belly of the digastric muscle, which arises in the digastric groove located medial to the mastoid process and the longissimus capitis. The styloid process and its attached muscles appear in the triangular zone bounded by the posterior belly of the digastric, the external auditory canal, and the mandibular ramus. Reflecting the digastric muscle exposes the transverse process of the atlas, which is covered by the attachments of numerous muscles, including the superior and inferior obliques, which form the upper and lower margin of the suboccipital triangle.

The rectus capitis lateralis muscle is the muscle most intimately related to the jugular foramen. It extends vertically behind the internal jugular vein from the transverse process of the atlas to the jugular process of the occipital bone. On the posterior neck are the trapezius muscle, splenius capitis, and semispinalis capitis. Beneath the semispinalis capitis muscle, three muscles arise between the inferior nuchal line and the margin of the foramen magnum: the rectus capitis posterior major and minor and the superior oblique muscle. The suboccipital triangle, an area defined by the opposing margins of the rectus capitis posterior major and the superior and inferior oblique muscles, is the site at which the vertebral artery courses along the upper posterior surface of the atlas.

SURGICAL APPROACHES

Postauricular transtemporal approach

The postauricular transtemporal approach accesses the region from laterally, through the mastoid, and from below, through the neck (Fig. 9.7 A-D, Fig. 9.7 E-H) (2, 4, 5). A C-shaped postauricular skin incision provides the exposure for a mastoidectomy and the neck dissection. The external auditory canal is either preserved or transected, depending on the anterior extent of the pathological abnormality. The neck dissection is completed initially to gain control of the major vessels and the branches supplying the tumor. The internal carotid artery, branches of the external carotid artery, internal jugular vein, and lower cranial nerves are exposed in the carotid sheath. A mastoidectomy with extensive drilling of the infralabyrinthine region accesses the jugular bulb. A limited mastoidectomy confined to the area behind the stylomastoid foramen and mastoid segment of the facial nerve, combined with removal of the adjacent part of the jugular process of the temporal bone, will provide access to the posterior and posterolateral aspect of the jugular foramen. Three obstacles to exposure of the full lateral half of the jugular foramen, the facial nerve, styloid process, and rectus capitis lateralis muscle are dealt with by transposing the facial nerve, removing the styloid process, and dividing the rectus capitis lateralis muscle. Anterior extensions of the pathological abnormality are reached by sacrificing the external and the middle ear structures. Sensorineural hearing can be preserved by maintaining the foot plate of the stapes in the oval window to avoid opening the labyrinth. Intracranial extensions of the lesion are reached by the retrosigmoid or presigmoid approaches after adding a suboccipital craniectomy. The lesion

can be removed by a transtemporal infralabyrinthine approach directed through the temporal bone below the labyrinth without the neck dissection, if the extracranial extension of the lesion is not prominent. The exposure can be extended by opening the otic capsule (translabyrinthine approach).

Retrosigmoid approach

A pathological abnormality located predominantly intradurally can be resected by the retrosigmoid approach (Fig. 9.6). A lateral suboccipital craniectomy exposes the dura behind the sigmoid sinus. The dura is opened, and the cerebellum is gently elevated away from the posterior surface of the temporal bone to expose the cisterns in the cerebellopontine angle and the intracranial aspect of the cranial nerves entering the jugular foramen, hypoglossal canal, and internal acoustic meatus.

Far-lateral approach

An extended modification of the retrosigmoid approach, the far-lateral approach, the subject of another chapter in this issue, may be selected if the tumor extends down to the foramen magnum in front of or lateral to the lower brainstem (10, 30, 32, 33). In this approach, the jugular foramen is opened from behind. The dura is opened and the cerebellum elevated to expose the intracranial extension of the pathological abnormality at the lower clivus and at the foramen magnum. Several variations, depending on the location and extent of the pathological abnormality, include drilling the jugular tubercle extradurally and removing bone above without disturbing the condyle (21, 33). The extradural reduction of the jugular tubercle aids in minimizing the retraction of the brainstem needed to reach the area anterior to the medulla and pontomedullary junction.

Preauricular subtemporal-infratemporal approach

The preauricular subtemporal-infratemporal approach, reviewed in detail in the chapter on the temporal bone (see Figs. 8.10 A-D, 8.10 E-F, 8.10 G-J and 8.18), exposes the jugular foramen anteriorly. It may be selected for tumors

that extend along the petrous portion of the internal carotid artery, through the eustachian tube, or through the cancellous portion of the petrous apex (29). A preauricular hemicoronal scalp incision is extended down to at least the level of the tragus and possibly into the cervical region, depending on the extent of the pathological finding and whether a neck dissection is needed. The zygomatic arch is removed or reflected downward with the temporalis muscle, taking care to preserve the frontal branch of the facial nerve. A frontotemporal bone flap, which may include the superior or lateral orbital rim, is elevated, and the glenoid fossa and the mandibular condyle with the joint capsule are either dislocated inferiorly or removed. The dura is elevated, and the bone of the middle fossa medial to the glenoid fossa is removed until the carotid canal is opened. The eustachian tube and the tensor tympani muscle, which course anterior to the carotid canal, are sacrificed during this procedure, taking care to protect the lower cranial nerves as they exit the jugular foramen. The styloid process is divided at its base, and the internal carotid artery is reflected anteriorly to gain access to the clivus and anterior aspect of the jugular foramen. Drilling can be extended to the posterior fossa through Kawase's triangle or through the clivus to the contralateral internal carotid artery (14).

DISCUSSION

Pathologies

Tumors are the most common lesions to affect the jugular foramen; the majority are chemodectomas (glomus jugulare tumor), neurinomas, and meningiomas, with a small percentage of other tumors, such as chondrosarcomas and chordomas (12, 25). The glomus jugulare tumor arises either in the adventitia of the jugular dome or from the intumescences along the tympanic branch of the glossopharyngeal nerve or the auricular branch of the vagus nerve in the jugular foramen (9). Tumors of the same nature that arise in the tympanic cavity or in the mastoid on branches of these nerves are referred to as glomus tympanicum tumors. Small glomus jugulare tumors remain confined within the jugular foramen. However, the tumor can extend as follows: 1) along the eustachian tube into the nasopharynx and through the foramina at the base of the skull, 2) along the carotid artery to the middle fossa, 3) through the intracranial orifice of the jugular foramen or along the hypoglossal canal to the posterior fossa, 4) through the tegmen tympani to the floor of the middle fossa, 5) through the round window and the internal

acoustic meatus to the cerebellopontine angle, and 6) through the extracranial orifice of the jugular foramen to the upper cervical region. Neuromas arise either from the glossopharyngeal, vagus, or the accessory nerves, and meningiomas from arachnoid granulations in the jugular bulb or venous sinuses. Although each tumor has characteristic patterns of invasion and destruction, the basic anatomic environment is similar to that of the glomus jugulare tumor.

Selection of surgical approach

The approaches to the jugular foramen can be categorized into three groups: 1) a lateral group directed through the mastoid bone, 2) a posterior group directed through the posterior cranial fossa, and 3) an anterior group directed through the tympanic bone. This categorization is based on the anatomic fact that the block of the temporal bone, excluding the squamous part, is regarded as an irregular pyramid, having its base on the mastoid surface. In addition, the middle fossa approaches could be categorized as in the "superior group" and the neck dissection upward to the jugular foramen as in the "inferior group". However, the latter approaches are usually not suitable when used alone for pathological abnormalities of the jugular foramen.

Lateral approach

The lateral approach directed through a mastoidectomy, used alone or in combination with other approaches, is the route most commonly selected for lesions extending through the jugular foramen (7, 12, 22). Because the jugular foramen is situated under the otic capsule, the approach basic to this group is called the infralabyrinthine approach. The facial nerve is frequently transposed anteriorly to drill the bone inferior to the labyrinth. Avoiding injury to the facial nerve is one of the key points in the lateral approaches (1). Even with special care, some degree of transient facial palsy is common, possibly because of disturbance to the nerve's vasculature. The surgical field can be widened anteriorly by sacrificing the external auditory canal and middle ear structures or medially by drilling away the otic capsule (translabyrinthine approach) or cochlea (transcochlear approach). The postauricular transtemporal approach, when combined with a neck dissection, provides satisfactory exposure of the jugular foramen, mastoid air cells, tympanic cavity, and the extracranial structures in and around the carotid sheath. Removal of the styloid process along with transposition of the facial

nerve facilitates wide opening of the extracranial orifice of the jugular foramen and provides access to the lower part of the petrous portion of the internal carotid artery. A wider exposure for the extracranial tumor can be obtained by removing the transverse process of the atlas or dislocating or resecting the mandibular condyle. The intracranial extension of the tumor is approached either retrosigmoidally or presigmoidally after adding a lateral suboccipital craniectomy or craniotomy (4, 6, 10, 26, 27).

Posterior approach

This group includes the retrosigmoid approach and its more extensive far-lateral and transcondylar variants. These approaches are suited to the intracranial portion of the tu mors. The conventional retrosigmoid approach provides access to the cerebellopontine angle and the intracranial orifice of the jugular foramen. However, extensions of the tumor through the foramen magnum or medially into the clivus are beyond the reach of this approach. The far-lateral and transcondylar modifications access these areas, providing an upward view from below by opening the posterolateral quarter of the foramen magnum and removing the posterior part of the occipital condyle. The posterior and posterolateral margin of the jugular foramen can be accessed by removing the part of the jugular process of the occipital bone located behind the jugular foramen and the portion of the mastoid located behind the mastoid segment of the facial nerve and stylomastoid foramen. A flatter view toward the midline clivus is obtained by additional extradural drilling of the jugular tubercle, although drilling in front of these nerves risks damaging the nerves as they cross the jugular tubercle (21, 23).

Anterior approach

The preauricular subtemporal-infratemporal approach is a major variant of this group of approaches. It uses the pathway anterior to the external auditory canal and through the tympanic bone, which are exposed by removal or displacement of the glenoid fossa and the temporomandibular joint. The approach alone can access the anterior part of the jugular foramen after reflecting the petrous portion of the internal carotid artery anteriorly. Further extensive drilling will expose the middle to upper clivus anteriorly. However, this approach is most often combined with a lateral approach to access an anterior extension of the pathology (22). Fisch et al. call this combined

approach the infratemporal fossa approach, Type B or C according to the anterior extension of the exposure (4). The selection of the optimal approach requires an understanding of the nature and the extension of the lesion. The combination of two or three approaches may be needed either in stages or in combination in one operative procedure (4, 25). Preoperative embolization will often reduce the blood loss with a vascular tumor. Intraoperative electrophysiological monitoring is of great help in avoiding nerve injury, in locating the neural trajectory in and around the tumor, or in predicting postoperative neural function (3, 20). Carefully planned reconstruction is required to reduce postoperative complications, especially leakage of cerebrospinal fluid, and to achieve a satisfactory cosmetic result. Reprint requests: Albert L. Rhoton, Jr., M.D., Department of Neurological Surgery, University of Florida Brain Institute, P.O. Box 100265, 100 S. Newell Drive, Building 59, L2-100, Gainesville, FL 32610-0265.

REFERENCES: 1-33

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