Intracranial carotid rings: A microanatomical study

ABSTRACT

The intracranial carotid  rings were studied in 30 specimens obtained from 15 cadaver heads fixed in formalin.

For didactic purposes, this dural folds were divided into three rings: Proximal, Medial and Distal.

The  first ring is found over the Internal  Carotid Artery (ICA) at its entrance in the cavernous sinus at the level of the foramen lacerum and underneath V1 and the Trigeminal ganglion.

This ring is formed by the petrolingual ligament reinforced by fibers of the endosteal dura of the carotid canal.

The removal of the anterior clinoid process allows the identification of the “Clinoid Space”, in this area, the clinoid segment of the internal carotid artery is surrounded by two fibrous rings which are medial and distal.

The  medial ring is a formation from the dural fiber of the deep layer of the superior wall of the cavernous sinus, and the distal ring is formed by dural fibers from the superficial  layer of the superior wall of the cavernous sinus.

An accurate understanding of the complex fibrous ring anatomy of the parasellar region is of paramount importance when dealing with lesions in this area and also in the strategical approaches.

 

MATERIALS AND METHODS

This Carotid Rings was studied in 30 specimens obtained from fifteen cadaver heads fixed in formalin.

After the brains were carefully removed in order to fully expose the skull base, the heads were placed en the Sugita head holder. They were turned 45 grade from the side of dissection and extended slightly to simulate the surgical position.

After identifying the anterior and posterior petroclinoid ligaments with the aid of the surgical microscope the middle fossa floor dura was dissected from anterior to posterior and lateral to medial.

The bone forming the floor of the middle fossa was removed up to the foramen rotundum, the foramen ovale and the foramen spinosum.

The trigeminal nerve was dissected extradurally in order to identify the proximal carotid ring at the entry  point of the internal carotid artery in the cavernous sinus.

The optic canal was unroofed and the anterior clinoid process removed.

By doing so, we exposed  the  “ Clinoid Space” and within it the clinoid segment of the internal carotid artery, a part of the ethmoidal sinus  as well as a part of the superior wall of the cavernous sinus. We also identified the medial and distal dural rings of the ICA in the superior and inferior limits of this space.

 

ANATOMICAL OBSERVATIONS

The particular disposition of the dural folds permits to surround partially the internal carotid artery in the parasellar region through of the fusion  of various dural fibers groups.

INTERNAL CAROTID RINGS

Proximal Carotid Ring: It’s  located at the exit of the level of the endocranial opening of the foramen lacerum.

This ring is formed by two fiber groups, one from the endosteal fibers of the trigeminal impression “obturatrix membrane” and inner most area of the superior aspect of the petrous vertex forming a tense and hard dural fold which courses over the internal carotid artery lateral aspect. It’s arch shaped fuses with the endosteal dura of the lingula sphenoidalis. This dural formation is also known as the  petrolingual ligament ( Fig.  ). The other fibers group arises from the endosteal dura of the superior aspect of the petrosphenoidal suture ( Fig.  )and ends by fusing with the endosteal dura of the medial wall of the carotid canal (Fig.   ).

These two fiber groups merge at the highest part of the petrosphenoidal suture. As a whole they are “V” shaped  and surround the internal carotid artery except in its anterior aspect where the ring is completed by the endosteal dura of the carotid sulcus ( Fig.  ).

It is possible to visualize the petrolingual ligament by dissecting between V1 and V2. The V1 branch of the trigeminal nerve runs parallel and above the petrolingual ligament.

This ligament is the anatomical landmark which separates the  internal carotid artery cavernous segment from the petrosal one ( Fig.  ).The diameter of the proximal ring was 7.57 +-0.6 mm. The length of the petrolingual ligament was 10.92 +- 0.9 mm, and the height was 1.22+- 0.4 mm. The location of the sympathetic pericarotid trunk in relation to this ligament was in the anterior third 70%, Middle third 25%, and in the posterior third 0.5%. The abducens nerve courses parallel with the petrolingual ligament with an average of distance 2.88 +- 0.6 mm. The distance between the middle third of the petrolingual ligament and the medial carotid ring was 18.12+-0.9 mm. 

 

Medial Carotid Ring:

Once  removed the anterior clinoid process one can identify the clinoid space, and partially the deep layer of the superior wall of the cavernous sinus ( Fig.  ).

This latter layer has a free border that surrounds intimately the posterolateral aspect of the internal carotid artery immediately at the exit of the cavernous sinus. However, in 15% this ring is less closely related with the artery, in such a way that there is a direct communication with the venous compartment of the cavernous sinus.

In the posterior course of this ring, the interclinoid ligament joins it. We have to emphasize that this ligament is not a direct attachment to the anterior clinoid process.

Anteriorly and medially this ring fuses with the endosteal dura of the carotid canal ( Fig.  ).The diameter of this ring was 6.1 +- 0.9 mm.

The distance from the medial carotid ring to the distal carotid ring was 5.4+- 1.2 mm and the ophthalmic artery (origin) was 6.42 +- 1.4mm.

 

Distal Carotid Ring:

This ring is formed by the convergence of dural fibers from various sites. The dural fibers of the lateral aspect of the tubercullum sellae together with the dural fibers of the optic canal, form a fold that courses over the superior aspect of the internal carotid artery just anterior to the ophthalmic artery  origin ( Fig.   ). It fuses afterwards with the medial fibers of the anterior petroclinoid ligament. In the posterior segment, the ring is continuos with the superficial layer of the superior wall of the cavernous sinus; above the distal ring , the internal carotid artery continuous with its supraclinoid segment. The diameter of the distal carotid ring was 6.86+-0.9 mm.

In most instances  there exist a little space between the medial aspect of the carotid artery an the ring which corresponds to the entrance of the so called  “carotid cave”. The depth and width of this semilunar space was 3.2 +- 0.5 mm and  1.9 +- 07 mm  respectively.

The distance from the proximal carotid ring was 21.0+-0.9 mm and the ophthalmic artery (origin) was 1.86+-1.1 mm.

The pericarotid connective tissue layer was found to be loosely attached to the rings in the lateral aspect of the internal carotid artery clinoid segment (Fig.  ).

 

DISCUSSION

The so called “Carotid rings” were described separately and at different times, what we’re calling in the current paper proximal ring corresponds to the “Inferior sphenopetrosal ligament” described by Lang and Strobel (7-8), who stated that it is formed by two parts: the pars saggitalis and the pars transversalis. The pars saggitalis corresponds to the petrolingual ligament and the pars transversalis  corresponds  to the endosteal dura of the superior aspect  of the petrosphenoidal suture. Sekhar (13)  says it’s formed by dural fibers from the carotid canal, and Dolenc (2) calls it “the lateral ring”.

This ligament is white and shiny, being an anatomical landmark to localize the beginning of the intracavernous carotid artery. The pars transversalis of this ligament may be missing. While performing an inferior approach to the cavernous sinus along the  middle fossa floor, the pars  saggitalis may be identified once the Meckel’s cave has been dissected and separated warning the surgeon of the internal carotid artery proximity.

What we name in the current paper medial carotid ring has been called in a number of ways, as early as 1935, Keyes (4) referred to it as what constituted the  “Clinocarotid canal”, he wrote “this clinocarotid canal is formed by a union of the anterior clinoid process on its medial side with the tip of the middle clinoid process as it arises from the tuberculum sellae or the lateral wall of the body of the sphenoid bone”. He classified the clinocarotid canal in three types: complete, incomplete and contact, according to the ossification degree (his study was performed of the basis of dry skulls).

This ring is formed by a condensation of fibers from the deep layer of the superior wall of the cavernous sinus and when ossified clearly  corresponds to what Keyes stated. We can also say this ring is partially constituted by the carotico-oculomotor membrane according to the description made by Inoue et al (12).

The medial ring corresponds to the Dolenc’s proximal ring (2). Knosp et al (5) described a ligament that connects the anterior with the middle clinoid process, which becomes the caroticoclinoid foramen when ossified, suggesting for it the of “carotid or clinoid ligament”.

Finally Umansky et al (14) published in  1994  a microanatomical study of the superior wall, emphasizing that the internal carotid artery extracavernous, is surrounded by two fibrous rings: Distal and proximal rings.

From the surgical point of view, Inoue et al (12) and Matsuoka et al (9)  approach the cavernous sinus through the superior wall after removing the anterior clinoid process, they cut the medial ring and proceed posteriorly following the traject of the interclinoid ligament towards the posterior clinoid process.

In the Dolenc approach (3), the cut  of this ring permits  the  posterior  displacement of the anterior bend of the intracavernous carotid artery, facilitating the access to the anterior part of the venuos compartment of the cavernous sinus and the sellar region.

The distal ring  was first described by Pernecsky in 1985 (10), this ring is more firmly attached to the lateral aspect of the carotid artery than over its medial side, where it can be found a semilunar  small space between the edge of the ring and the artery, corresponding to the entrance of the carotid cave described by Kobayashi (6) as a dural pouch. We didn’t find any redundant dura at the level of the carotid cave, but just a virtual space between the carotid artery and the endosteal dura of the carotid sulcus.

The clinical importance of the carotid cave is that this virtual space may be occupied by an aneurysm.

In dealing with aneurysms of the paraclinoid region it’s necessary  to cut the distal ring to gain more surgical field , Dolenc (1), Perneczky   (10).

The connective tissue layer covering the lateral aspect of the internal carotid artery in  the clinoid space, that unites the medial and distal ring, is considered for us as transitional dura between the dura over and under lying the anterior clinoid process (deep layer of the superior wall of the  cavernous sinus). Knosp (5) and Perneczky (11) refer to the connective tissue surrounding the carotid artery as corresponding to a remnant of the abundant connective tissue in fetal cavernous sinuses. 

The continuous  development of  microsurgical techniques to treat  tumors  in the cavernous sinus and  vascular lesions of the internal carotid artery cavernous and clinoid segments, emphasizes the need for an accurate understanding of the microanatomy of the dural folds that surround the internal carotid artery in the parasellar region.

The fundamental knowledgment of the dural complexity from the parasellar area, allows us surgery strategies procedures with the use of the  above anatomical landmarks described.

 

REFERENCES

1.      DOLENC  V.: A combined epi and subdural  direct approach to carotidophthalmic artery aneurysms: J. Neurosurgery 62: 667- 672. 1985.

2.      DOLENC  V.: Anatomy and surgery of the cavernous sinus: Springer Wien New- York p.4, 1989.

3.      DOLENC  V.: Transcranial Epidural approach to pituitary tumors extending beyond the sella: Neurosurgery 41:542-552, 1997

4.      KEYES  J.: Observation on four thousand optic foramina in human skulls of known origin. Arch Ophthalmic 13:538-568, 1935.

5.      KNOSP  E., Muller  G., Perneczky  A.: the Paraclinoid carotid artery: Anatomical aspects of a microneurosurgical approach: Neurosurgery, 22(5): 896-901, 1988.

6.      KOBAYASHI  S., Kyoshima  K.: Carotid cave aneurysms of the internal carotid artery: J. Neurosurgery 70:216-221, 1989.

7.      LANG  J., Strobel  F.: Uber den einbav des ganglion trigeminale: Vern anat ghs 72:137, 1978.

8.      LANG  J.: Subtemporal approach to aneurysms:Album of neuroanatomy 1991 by F.K. Schattauer Verlagsgesellschaft mbH, lenzhalde 3, 7.000 Stuttgar 1 Germany, Vol 5 II, p. 37, 1991.

9.      MATSUOKA  Y., Hakuba  A., Kishi H., Nishimura S.: Direct surgical treatment of intracavernous internal carotid artery aneurysms: Report of four cases: Surg. Neurol. 26:360-364, 1986.

10.  PERNECZKY A., Knosp E., Vorkapic P., Czech TH.: Direct surgical approach to infraclinoidal aneurysms: Acta Neurochirurgica 76: 36-44, 1985.

11.  PERNECZKY A., Knosp E.: The intracavernous connective tissue cover of the internal carotid artery- anatomy and surgery. IN: Tumors of the skull base. Extra and intracranial surgery of skull base tumors; Schevnemann  H., Schurmann  K., Helms  J. (eds); 171-175, 1986.

12.  INOVE T., Rhoton A.: Surgical approaches to the cavernous sinus: A microsurgical study. Neurosurgery 26 (6):903-932, 1990.

13.  SEKHAR  L., Sen  C.: Comments to Inove T., Rhoton A.: Surgical approaches to the cavernous sinus: A microsurgical study. Neurosurgery 26(6): 903-932, 1990.

14.  UMANSKY  F., Valarezo  A., Elidan  J.: The superior wall of the cavernous sinus: a microanatomical study. J. Neurosurg. 81: 914-920, 1994.

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