containing the ICA and the sixth nerve in the deep and running the CNs III, IV and V1, V2 through this septum but not in the superficial layer. Harris and Rhoton (1976) found two dural layers of the lateral wall and the nerves III, IV and V1 running between them. Umansky and Nathan (1982) studied the lateral wall of the CS in 70 specimens and found neither a septum dividing the CS, nor a single dural layer. They observed a superficial and a deep layer that were loosely attached to each other. The sheaths of the CNs III, IV and V1, V2 and an often incomplete reticular membrane extending between the sheaths, formed the deep layer.

The CN III penetrates the posterior CS via the oculomotor foramen (Umansky et al. 1994; Inoue et al. 1990) and courses anteriorly along the inferior surface of the anterior clinoid process to reach the SOF through the annulus of Zinn (Keller et al. 1997).

The CN IV enters the CS in a dural opening between the anterior and posterior petroclinoid ligaments (Umansky and Nathan 1982, 1987; Umansky et al. 1994) and crosses the III CN before entering the SOF without coursing through the Annulus of Zinn (Keller et al. 1997).

The CN V1 courses from the Gasserian ganglion to the SOF inferior and lateral to CN IV and VI and lies at the level of the SOF lateral to CN VI (Keller et al. 1997).

The CN VI exits the pontomedullary junction and courses through the subarachnoid space to reach Dorello’s canal, a small triangular space formed beneath the petroclinoid ligament (Gruber’s ligament) from the petrous apex to the posterior clinoid process (PCP) (Keller et al. 1997). This canal contains the CN VI, usually lying laterally to the IPS and the dorsal meningeal artery from the meningohypophyseal trunk (MHT). The abducens nerve is considered the only true intracavernous nerve because of its course along the lateral surface of the ICA after leaving Dorellos canal (Keller et al. 1997).

The arterial blood supply to these CNs is provided by multiple small branches mainly arising from the inferolateral trunk (ILT) and the MHT and in part arising from dural branches of the ECA territory (see below).

The development and increasing use of transarterial embolizations of DCSFs in the late 1980s and early 1990s required us to study in more detail the arterial blood supply of the CNs in the CS region (Knosp et al. 1987b). At the present time this knowledge plays a minor role due to the introduction of transvenous occlusion techniques, being increasingly employed to treat DCSFs since 1990.

3.2.1

Autonomic Nervous System

A detailed knowledge of the sympathetic and parasympathetic nervous systems within the CS is still missing. It is known that the sympathetic fibers course along the extracranial ICA, through the carotid canal, to reach the petrous and cavernous portion where they form a plexus (Keller et al. 1997; Paullus et al. 1997; Mitchel 1953). Recently, parasympathetic fibers and ganglia have been found in the CS as well, probably connected with rami orbitalis arising from the sphenopalatine ganglion and coursing through the SOF (Suzuki and Hardebo 1993). Bleys et al. (2001); while performing immunohistochemical studies in rats, found that the cavernous sinus ganglia, consisting of the pterygopalatine ganglion and small cavernous ganglia, contribute to parasympathetic cerebrovascular innervation and that the cavernous nerve plexus and abducens nerve are involved in the pathway from these ganglia to the cerebral arteries. It can be assumed that not only the sympathetic but also parasympathetic innervations play a role in the tone regulation of cerebral vessels (Suzuki and Hardebo 1993).

3.3

Vascular Anatomy

3.3.1

Arterial Anatomy (Figs. 3.5–3.7)

3.3.1.1

Internal Carotid Artery

The ICA provides the anterior circulation that supplies the largest part of the cerebrum, the eye and other intraorbital structures. The ICA also gives rise to the branches of the forehead and the nose. The artery begins at the bifurcation of the common carotid artery (CCA), usually at the level of the fourth cervical vertebra, where it is enlarged to form the so-called carotid sinus. Fischer (1938) divided the ICA into four segments: the cervical, the petrous, the cavernous and the cerebral segment (Fig. 3.5).

The cervical segment extends almost vertically to the base of the skull to reach the Apertura externa (external aperture) of the Canalis caroticus (carotid canal) to enter the petrous bone. Just before entering

C1

C2

C3

C4

C5

Petrous canal

©

C7

C6

C5

C4

C3

Petrous canal

©

Cisternal (cerebral) segment (C1–C2)

Cavernous segment (C3–C5)

Petrous segment

Cervical segment

C7: Communicating segment

C6: Ophthalmic segment

C5: Clinoid segment

C4: Cavernous segment

C3: Lacerum segment

C2 C2: Petrous segment

C1

C1: Cervical segment

Fig. 3.5. Original classification of ICA segments after Fisher (1938, modified after Krayenbuehl and Yasargil, 1997). Although somewhat limited in accuracy, it is still used by many neuroradiologists and neurosurgeons.

Cavernous segment: Between apex of petrous pyramid and base of anterior clinoid process. Petrous segment: Between entrance into the skull base and apex of petrous pyramid.

C5: “Ganglion segment” after Fisher, because the artery lies in close proximity to the frontal pole of the trigeminal ganglion.

C4: Horizontal and lateral to the pituitary gland. C3: Below the base of the clinoid process

(“carotid knee”).

C2: After penetration of the dura lateral to clinoid process, beneath the optic nerve.

C1: Ascends and divides at the circle of Willis. “Carotid siphon“ after Moniz: Curved portion within and above the cavernous sinus (C2–C5). The MHT most commonly arises from the C5 segment.

Fig. 3.6. New classification of ICA segments after Bouthillier (1996). The new classification divides the internal carotid artery according to its course through the skull base from proximal to distal. This approach, using a more logical numerical scale, may be more practical since it follows the blood flow and helps identify pertinent parts of anatomy, given current techniques of cranial base surgery and identified abnormalities. (Ogilvy, comment in Neurosurgery, Volume 38 (3), March 1996, pp 425-433 1996). Transitions:

C2 to C2: Vaginal process of carotid canal. C2 to C3: End of carotid canal at the postero-

lateral margin of the foramen lacerum. C3 to C4: Level of the petrolingual ligament.

C4 to C5: Proximal dural ring.

C5 to C6: Distal dural ring.

C6 to C7: Origin of posterior communicating artery.

the canal, the ICA forms a medial convex curve. The cervical segment lies medial to the internal jugular vein (IJV), the vagus nerve usually between both vessels.

The ICA enters the cranium by passing through the carotid canal. This canal is lined by periosteum and is located in the petrous portion of the temporal bone. The posterior orifice of the canal opens onto the posterior wall of the foramen lacerum, adjacent to the jugular foramen. The anterior or internal orifice of the canal is located at the petrous apex (Miller N 1998).

The petrous segment can be divided into a vertical and a horizontal portion with a course depending on the configuration and development of the skull base, particularly on the shape of the petrous bone. The total length of this segment is about 25–35 mm. The vertical portion courses 6–15 mm in the vertical direction then turns medially and anteriorly to form a genu and becomes the horizontal portion. The horizontal portion courses anteriorly and medially above the foramen lacerum to eventually leave the bony canal near the petrous apex. The petrous segment can give rise to two small arterial branches

in 38% of the cases. The vidian artery, usually arising from the internal maxillary artery (see below), can also arise from the petrous ICA (30%) (Paullus et al. 1977). The small caroticotympanic artery, previously reported to be the most common branch, is thought to enter the tympanic cavity through a foramen in the wall of the carotid canal, was not found by Paullus et al. (1977), but often seen by Lang (1983). The latter also saw periosteal twigs ramifying in the periosteum of the carotid canal and the neighborhood of the foramen lacerum, which have been described only by Lazorthes (1961). They may be responsible for retrograde filling of the petrous ICA in patients with ICA occlusions.

The cavernous segment begins at the superior margin of the petrolingual ligament at the posterior aspect of the CS and ends at the root of the anterior clinoid process. This segment lies within the CS, surrounded by its venous spaces and by some trabecular connective tissue. From the petrous apex medial and rostral towards the lateral side of the sphenoid bone, the ICA is separated from the Gasserian ganglion by a thin osseous or connective tissue septum. Because the posterior limits of the cavernous segment vary and are difficult to exactly define, this segment was also divided into a presellar and juxtasellar segment by some authors (Dilenge and Heon 1974).

Above the foramen lacerum the ICA courses almost perpendicularly cranial in a groove along the lateral side of the sphenoid bone and lies directly adjacent to the frontal pole of the Gasserian ganglion [C5 after Fischer (1938) or ascending segment]. From here the ICA passes rostrally to reach the root of the anterior clinoid process, to which it lies laterally. Lateral to the pituitary fossa the ICA lies in a shallow groove of the lateral sphenoid bone (C4, or horizontal segment). The medial wall of the ICA lies within the CS, which is separated from the pituitary gland by a thin sheet of the dura mater. Underneath the root of the anterior clinoid process ,the ICA forms the so-called “knee of the carotid”, a sharp, anteriorly convex curve (C3 or clinoid segment).

After piercing the dura and the arachnoid membrane at the medial margin of the anterior clinoid process, the ICA courses within the subarachnoid space (cerebral or cisternal segment, C2) upward and posteriorly underneath the optical nerve that enters the optic canal. Finally, the ICA ascends to reach its bifurcation into the middle and anterior cerebral artery (MCA and ACA) to form the circle of Willis (C1, terminal segment after Fischer). In this manner the segments C3–C5 form the cavernous and C1–C2

form the cerebral segment of the ICA. The double or S-shape curve of the ICA within and above the CS is, according to Moniz (1927), called the “carotid siphon”. After Krayenbühl and Yasargil (1997), the shape of this carotid siphon may differ remarkably: a U-shape, a V-shape, Arcus-shape and Omegashape, a double siphon, a megasiphon or a dolichosiphon can be seen. The first three types are seen more frequently, while in older patients (51–74 years) the omega type occurs more often.

Today, Fischer’s system is considered somewhat limited as it is anatomically inaccurate and numbers the ICA segments opposite the direction of blood flow. It has been modified or replaced by several others, e.g. by Bouthillier et al. (1996), who divided the ICA into seven segments using a numerical scale in the direction of the blood flow: C1 = cervical, C2 = petrous, C3 = lacerum, C4 = cavernous, C5 = clinoid, C6 = ophthalmic and C7 = terminal segment (Fig. 3.6). Lasjaunias et al. (2001) have pointed out that the morphological continuity of the ICA obscures significant differences between various segments which can also be marked by the origins of embryonic vessels (see below). In clinical practice, however, the classification of Fischer is still widely used.

3.3.1.1.1

Branches of the ICA

Branches of the Cavernous Segment (Fig. 3.7 and Figures in Sects. 7.2.1–7.2.12)

Within the CS, the C5 segment usually gives rise to one (MHT), and the C4 segment gives rise to two small but important branches (ILT, capsular arteries).

Meningohypophyseal Trunk (MHT)

Luschka (1860) first described the Arteria hypophysialis inferior. Mc Conell (1953) studied the arterial supply of the pituitary gland by a small arterial trunk, of which the inferior hypophyseal artery is the largest. Later on, Schnüerer and Stattin (1963), Parkinson (1965), and Rhoton and

Inoue (1991) gave a more detailed description of these anatomic vascular relationships. Origin and branching of the small arteries vary significantly. Most frequently, a 0.75-mm meningohypophyseal ramus arises from the dorsal circumference of the C5 segment, just immediately before the vertical part turns into the horizontal part. This vessel is in the English literature commonly named the

meningohypophyseal trunk (MHT) according to Parkinson (1965, 1990), the inferior hypophyseal artery according to Mc Connell (1953), the dorsal main stem artery according to Schuerer and Stattin (1963) or the posterior trunk according to Tran-Dinh (1987). The classification of Parkinson (1984) differentiated initially three main branches of the MHT, the radiological appearance of which was described by Pribam et al. (1966).

The marginal tentorial artery (artery of the free margin of the tentorium cerebelli, tentorial artery, medial tentorial artery), first described by Bernasconi and Cassinari (1956) ascends to the roof of the CS, courses along the free edge of the tentorium and gives two branches for the third and fourth cranial nerve and to the roof of the CS. It supplies the medial third of the tentorium and may anastomose with a meningeal branch of the ophthalmic artery, with a corresponding contralateral branch and a meningeal branch of the ascending pharyngeal artery. This artery was found by Lasjaunias et al. (1977) to arise from the superior branch of the ILT in 8/20 cases (see below).

The lateral clival artery (dorsal meningeal artery or dorsal clival artery) arose from the MHT in 90% of 50 studied cadavers (Harris and Rhoton 1976), supplies the sixth cranial nerve and anastomoses with the contralateral side and branches of the vertebral artery and the jugular ramus of the APA. This artery supplies the dura of the dorsum sellae and clivus and is most often involved in the arterial supply of DCSF (Barrow et al. 1985).

The inferior hypophyseal artery (posteroinferior hypophyseal artery) crosses the CS medially, divides into superior and inferior branches, connects with the corresponding artery of the contralateral side and supplies the posterior lobe of the pituitary gland, the dura of the posterior clinoid process, the floor of the sella and parts of the posterior CS. According to Martins et al. (2005) this dural territory is supplied by a medial clival artery, which can also arise directly from the ICA and anastomoses with the hypoglossal ramus of the APA. The inferior hypophyseal artery is often superimposed on angiograms and difficult to identify (Lasjaunias et al. 2001).

Further described are:

A basal tentorial branch (lateral tentorial artery) by

Schnüerer and Stattin (1963) and Lasjaunias et al. (1978a) which can arise from a common

trunk with medial tentorial artery (Martins et al. 2005).

A medial clival artery has been described by Lasjaunias et al. (2001) and Martins et al. (2005) (see above).

It should be mentioned that Pribram et al. (1966) have already emphasized that the classic MHT arising as a single trunk is not constantly seen. The existence of a singular trunk was observed by Lasjaunias et al. (1978a) in only 10% of the cases. He suggested instead that these branches more often arise independently as single vessels corresponding to the remnants of two transient embryonic vessels, the primitive maxillary and the primitive trigeminal artery. The former gives rise to the inferior hypophyseal artery, the latter to the medial and lateral clival arteries as well as to the basal tentorial artery. Lasjaunias et al. (1978a) furthermore pointed out that the marginal tentorial artery of Bernasconi may originate from eight different pedicles, [including the accessory meningeal (Silvela and Zamarron 1978), middle meningeal, intraorbital ophthalmic and lacrimal arteries], of which the C5 siphon is only one.

The term MHT is nevertheless widely used, although it not only supplies the meninges and the pituitary gland but also the oculomotor, trochlear and abducens nerves. In over 200 cavernous carotid dissections it was identified in 100% of the cases (Parkinson 1965).

Martins et al. (2005) have recently provided a comprehensive review of the anatomy of dural arteries within the CS region and differentiate the MHT into the following components:

1.Tentorial trunk

–Medial tentorial artery (marginal tentorial artery, Bernasconi)

–Lateral tentorial artery (basal tentorial artery)

2.Dorsal meningeal artery (lateral clival artery)

–Medial branch

–Medial clival branch

–Lateral branch

3.Inferior hypophyseal artery

–Hypophyseal circle

–Medial clival artery

The inferolateral trunk (ILT) according to

Lasjaunias et al. (1977), also named artery of the inferior cavernous sinus (Miller 1998; Parkinson 1965), the lateral main stem (Schnürer and Stattin 1963) or the lateral trunk (Tran-Dinh 1987) in the

Fig. 3.7.=Arterial anatomy in the cavernous sinus region

(artist’s drawing of small dural arteries arising from ICA and ECA, considered so-called “dangerous anastomoses”, in the cavernosus sinus region, lateral view.) The dural arteries of the ICA and ECA connecting both territories in the cavernous sinus region are also referred to as “dangerous anastomoses”. Because of their small caliber these branches are often not (or not completely) visualized in diagnostic arteriograms, unless they are enlarged due to increased flow caused by AV-shunting lesions, arterial occlusions or tumors. The numerous possibilities of inadvertent migration of embolic material into the cerebral circulation during transarterial embolization of ECA branches are obvious. However, it is not the vessel per se which is “dangerous”, but lack of knowledge or negligence of the particular anatomy in this region. In cases of arteriovenous shunts developing within or adjacent to the cavernous sinus, these branches become supplying feeders and are recruited from ipsiand contralateral ECA and ICA territory. Even in case of a successful positioning of a microcatheter in the ILT or MHT, reflux of embolic material such as particles or glue may easily occur and poses a risk for neurological complications.

4

a10

b

c d

English literature, corresponds to the remnant of the dorsal ophthalmic artery (Lasjaunias et al. 1977). It arises from the lateral aspect of the horizontal portion of the cavernous portion of the ICA distal to the origin of the MHT (C4 segment). It usually curves over the CN VI (96%) and divides into three main branches:

The superior ramus (ramus tentorii marginalis, marginal tentorial artery) supplies the roof of the CS and the proximal part of CN III and IV. It can

replace or anastomose with the tentorial artery of the MHT.

The anterior ramus divides into a lateral and medial branch. The anteromedial ramus passes to the supraorbital fissure and supplies the distal parts of the CN III and IV. It ends as deep recurrent ophthalmic artery (or dorsal ophthalmic artery) and anastomoses with the intraorbital ophthalmic artery. The anterolateral ramus courses together with the second division of