Neurosurgical Review

, Volume 27, Issue 1, pp 22–26

Anatomy of the clinoidal region with special emphasis on the caroticoclinoid foramen and interclinoid osseous bridge in a recent Turkish population

Authors

  • Mete Erturk
    • Department of Anatomy, Faculty of MedicineEge University
    • Department of Anatomy, Faculty of MedicineEge University
  • Figen Govsa
    • Department of Anatomy, Faculty of MedicineEge University
Original Article

DOI: 10.1007/s10143-003-0265-x

Cite this article as:
Erturk, M., Kayalioglu, G. & Govsa, F. Neurosurg Rev (2004) 27: 22. doi:10.1007/s10143-003-0265-x
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Abstract

In this study we present the incidence of caroticoclinoid foramen and interclinoid osseous bridge and some topographic aspects regarding the clinoidal internal carotid artery (ICA) in a recent Turkish population to provide a guide for neurosurgeons in any surgical approach, especially to the cavernous sinus. One hundred nineteen adult dry skulls and 52 adult cadaveric heads were used for this purpose. Caroticoclinoid foramen and the interclinoid osseous bridge were divided into three types based on the classification of Keyers [13]. Caroticoclinoid foramen was observed in 35.67% of the specimens, unilaterally in 23.98%, and bilaterally in 11.69%. The complete-type caroticoclinoid foramen was observed in 4.09% of the specimens, the contact type in 4.68%, and the incomplete type in 14.91%. Transverse diameter of the foramen was 5.32±0.52 mm for the incomplete type. The incidence of interclinoid osseous bridge was 8.18%. The middle clinoid process was prominent in 15.12% of cases and rudimental in 13.23%. The mean distance between the proximal and distal dural rings of the clinoidal ICA was 4.51±0.44 mm, and mean diameter of the distal ring was 5.25±0.59 mm. Right-left differences were assessed for each parameter, and populational differences are discussed.

Keywords

AnatomyAnterior clinoid processCaroticoclinoid foramenClinoidal internal carotid arteryInterclinoid osseous bridge

Introduction

The caroticoclinoid foramen, first described by Henle (1855), is an osseous bridge between the tip of the middle clinoid process and the anterior clinoid process (ACP) [11]. It converts the terminal part of the carotid groove into a bony ring or foramen. The internal carotid artery (ICA) runs forward and medially out of the cavernous sinus through this closed and usually circular ring of bone [18]. The interclinoid osseous bridge extends from the ACP to the posterior clinoid process. Caroticoclinoid foramen and interclinoid osseous bridge result from ossification of the caroticoclinoid and interclinoid ligaments during development [28]. It has been reported that these sellar bridges are laid down in cartilage at an early stage of development and ossify in early childhood [18]. They have been reported to have a high incidence (15–38%) in subjects with hormonal derangement, idiots, criminals, and epileptics [18].

The cavernous sinus, which acquires clinical significance in many different pathologies of the region, is bound anteriorly by the tuberculum sellae and the anterior clinoid processes and posteriorly by the posterior clinoid processes and a triangular region of varying size lateral to and behind the posterior clinoid processes [18, 28]. The ICA exits the anterior superior part of the cavernous sinus on the medial side of the anterior clinoid process and perforates the roof of the cavernous sinus [10, 12]. If a caroticoclinoid foramen is present, the ICA runs forward and medially out of the cavernous sinus through this ring of bone [18]. This close relationship of the cavernous sinuses with the clinoid processes is important in any surgical approach to the region.

The ICA enters the subarachnoid space through a thick ring of dura called the distal dural ring. The ICA is surrounded also with another ring of dura, the proximal dural ring, which is exposed after the ACP is removed. The area between these two dural rings is called the clinoidal space. The clinoidal ICA is located in this space and exposed by removing the ACP. During surgical approaches to the sellar region for tumors or aneurysms, the anterior clinoid process and the optic strut are often removed from the lesser wing. There is a risk of damaging the clinoidal ICA during these approaches.

This study presents bony variations and morphometry of the ACP region and topographic aspects regarding the clinoidal ICA in a recent Turkish population to provide a guide for neurosurgeons in any surgical approach, especially to the cavernous sinus.

Materials and methods

This study was performed on 119 adult dry skulls and 52 adult cadaveric heads obtained from the Department of Anatomy, Ege University Faculty of Medicine. Right and left sides of the parasellar regions were included in the study, yielding 238 bony specimens and 104 cadaveric specimens. The dural layers covering the anterior clinoid processes were removed. In all cases, the anterior, middle, and posterior clinoid processes were examined to reveal their relationship and the incidence of caroticoclinoid foramen and interclinoid osseous bridge, which were in turn divided into three types according to the classification of Keyers [13] (Fig. 1):
Fig. 1.

Schematic illustration of the three types of caroticoclinoid foramen. A incomplete type, B contact type, C complete type, MCP middle clinoid process, ACP anterior clinoid process

  1. a.

    Complete type, if the foramen or bridge occurred properly.

     
  2. b.
    Contact type, if there was a suture between the tips of the anterior and middle clinoid processes (Fig. 2).
    Fig. 2.

    Contact-type caroticoclinoid foramen on the left side and complete type on the right side. CTCF contact type caroticoclinoid foramen, CCF complete type caroticoclinoid foramen

     
  3. c.
    Incomplete type, if spicules of bone extended medially from the anterior and middle clinoid processes but did not touch (Fig. 3).
    Fig. 3.

    Bilateral incomplete caroticoclinoid foramen. ACP anterior clinoid process, ICF incomplete caroticoclinoid foramen

     

For bony specimens, the transverse diameters for the complete and contact types of caroticoclinoid foramen were measured. For the incomplete type, the distance between the two tips of the anterior and middle clinoid processes was measured using a flexible ruler. The incidence of the caroticoclinoid foramen and the interclinoid osseous bridge, distance between the anterior and middle clinoid processes, distance between the proximal and distal dural rings (length of the clinoidal ICA), and the diameter of the distal dural ring were measured in cadaver specimens.

Mean and standard deviation values were calculated for each parameter, and Student's t-test was used for statistical analysis in the assessment of right-left differences.

Results

We observed unilateral caroticoclinoid foramen in 29 (24.37%) and bilateral caroticoclinoid foramen in 15 (12.6%) of the 119 adult dry skulls examined, for a total incidence of 36.97% (Fig. 1). In cadaver specimens, 12 (23.08%) skulls had unilateral foramina and five (9.61%) had bilateral caroticoclinoid foramina, making the total incidence 32.69%. Evaluating bony and cadaver specimens together, the total incidence of caroticoclinoid foramen was 35.67%, 23.98% for unilateral and 11.69% for bilateral foramina. Complete-type caroticoclinoid foramen was observed in 14 specimens (4.09%), the contact type in 16 (4.68%), and the incomplete type in 51 (14.91%). The incidence of unilateral caroticoclinoid foramen was higher on the right side (12.28%) than the left (11.7%), and this difference was statistically insignificant. For the unilateral contact type, incidence was higher on the left side (2.63%) than the right (0.88%). Incidence for the complete type was 1.17% for both right and left sides. The incomplete type was observed at 5.84% on the right side and 5.55% on the left (Table 1).
Table 1.

Incidence of the complete, contact, and incomplete types of caroticoclinoid foramen for bony and cadaveric specimens

Side

Complete

Contact

Incomplete

Unilateral

Right

4 (1.17%)

3 (0.88%)

20 (5.85%)

Left

4 (1.17%)

9 (2.63%)

19 (5.55%)

Bilateral (171 specimens)

3 (1.75%)

2 (1.17%)

6 (3.51%)

Total

14 (4.09%)

16 (4.68%)

51 (14.91%)

The transverse diameter of the foramen was 5.32±0.52 mm, 5.33±0.3 mm on the right side and 5.32±0.73 mm on the left (P>0.5). For the incomplete type, the distance between the two tips of the anterior and middle clinoid processes was measured at 3.03±1.1 mm, 3.12±0.92 mm on the right side and 2.94±1.34 mm on the left (P>0.5) (Fig. 3).

An interclinoid osseous bridge was observed in ten (8.4%) bony specimens, unilaterally in four (3.36%) and bilaterally in six (5.04%) (Fig. 4). These cases included five complete-type, three contact-type, and eight incomplete-type caroticoclinoid foramina. Seven bony specimens (5.88%) with caroticoclinoid foramen had the interclinoid osseous bridge on the opposite side. For cadaver specimens, the interclinoid osseous bridge was observed as unilateral in three cases (5.77%) and bilateral in one (1.92%), making the total incidence 7.69%; of these, four cases (7.69%) with caroticoclinoid foramen had the interclinoid osseous bridge on the opposite side. For bony and cadaveric specimens, interclinoid osseous bridge was observed unilaterally and bilaterally in seven cases each (4.09% for both), and the total incidence was 8.18%. The incidence of interclinoid osseous bridge was higher on the right side (2.34%) than the left (1.75%). The incidences of complete, contact, and incomplete types of caroticoclinoid foramen and interclinoid osseous bridge are shown in Table 1 and Table 2.
Fig. 4.

Bilateral interclinoid osseous bridge. ICB interclinoid osseous bridge

Table 2.

Incidence of the complete, contact and incomplete types of the interclinoid osseous bridge

Side

Complete

Contact

Incomplete

Unilateral

Right

2 (0.58%)

2 (0.58%)

Left

2 (0.58%)

4 (1.17%)

Bilateral (171 specimens)

3 (1.75%)

2 (1.17%)

3 (1.75%)

Total

8 (2.33%)

6 (1.75%)

12 (3.5%)

The middle clinoid process was prominent in 18 cases (15.12%), eight (3.36%) of which had caroticoclinoid foramen, and two (0.84%) had interclinoid osseous bridge on the opposite side. The middle clinoid process was rudimental in 27 cases (13.23%).

In all cadaver specimens, we observed a thin layer of dura lining the surface of the osseous structures around the clinoid segment, forming a fibrous collar (carotid collar). The ICA and thin venous channels, referred to as the clinoid venous plexus, could be observed through the collar (Fig. 5). The mean distance between the proximal and distal rings was 4.51±0.44 mm (range 3.8–5.4), with 4.42±0.39 mm on the right side and 4.6±0.48 mm on the left (P<0.5). The mean diameter of the distal ring was 5.25±0.59 mm (range 3.6–6.7), 5.24±0.66 mm on the right side and 5.25±0.53 mm on the left (P>0.5). The distance between the anterior clinoid processes was measured as 22.6±2.29 mm (range 18.74–27.06) and between the middle clinoid processes as 11.51±1.75 mm (range 8.65–15.3).
Fig. 5.

Microphotograph showing the clinoidal region. DR distal dural ring, ICA internal carotid artery

Discussion

Removal of the anterior clinoid process is an important step in exposing structures of the superior part of the cavernous sinus during the management of proximal ICA aneurysms [12, 21, 25]. Anterior and superior surgical approaches to the ICA or the cavernous sinus require removal of the ACP together with the optic strut (posterior root of the lesser wing), unroofing the optic canal [19, 21, 25, 27]. The ACP may be pneumatized or the bone marrow may be of varying density, and thus the region should be drilled carefully to avoid injury to the ICA and the optic nerve. Also, a caroticoclinoid foramen or interclinoid osseous bridge makes complete removal of the ACP difficult. In removing the ACP to expose the clinoidal ICA, it is important to remember that an interclinoid osseous bridge may form a complete bony ring around the clinoid segment or a caroticoclinoid foramen may affect the course of the ICA in the cavernous sinus [26].

The removal of the ACP reveals the "clinoid space," a small triangular area in the superior surface of the cavernous sinus with thin underlying dura mater. This space varies in dimensions according to the size of the ACP and is lateral to the emergence of the ICA from the cavernous sinus [25]. The clinoidal ICA can be seen through the dura in the medial wall of this space. The clinoidal segment is accepted as intracavernous by some investigators [6, 24, 26, 29]. Kim et al. [14] observed a collar of dura in which venous tributaries of the cavernous sinus lay. On the contrary, other studies consider the clinoidal space to be outside the cavernous sinus [5, 15, 21, 22]. Our observations are in accordance with this, as we did not observe the cavernous sinus extending to the clinoidal space and the carotid artery was directly in contact with the bone surfaces of the anterior clinoid process and the optic strut, yet this issue needs further investigation.

The incidence of caroticoclinoid foramen has been investigated by various authors on different populations, as presented in Table 3. The combined frequencies of the complete and incomplete types were observed as 3.9% in female and 6% in male Japanese [8], 15.7% in Koreans [19], 17% in Alaskan Eskimos [8], 23.4% in Sardinians [20], 34.84% in Caucasian Americans [13], 6.27% in Portuguese [1], and 14% in Germans [23]. Our results represent a higher incidence of the caroticoclinoid foramen (35.67%), close to that of Inoue et al. [12].
Table 3.

Comparative studies on the incidence of the caroticoclinoid foramen and the interclinoid osseous bridge

Author

Number

Caroticoclinoid foramen

Interclinoid osseous bridge

Unilateral

Bilateral

Total

Keyers (1935)

2187

27.46%

8.68%

Azeredo et al. (1988)

270

6 (2.22%)

11 (4.05%)

17 (6.27%)

9 (3.04%)

Inoue et al. (1990)

50

11 (22%)

7 (14%)

18 (36%)

2 (4%)

Lee et al. (1997)

73

15.7%

1.4%

17.1%

Cireli et al. (1990)

50

3 (6%)

3 (6%)

1 (2%)

Deda et al. (1992)

88

6 (6.82%)

7 (7.95%)

13 (14.77%)

4 (4.54%)

Gurun et al. (1994)

198

16 (8.08%)

11 (5.55%)

27 (13.63%)

2 (1.01%)

Erturk et al. (2002)

171

41(23.98%)

20 (11.69%)

61 (35.67%)

14 (8.18%)

Turkish populationa

507

66 (13.02%)

38 (7.5%)

104 (20.51%)

21 (4.14%)

aResults presented for the Turkish population are averages of the results of Turkish authors (Cireli et al. 1990, Deda et al. 1992, Gurun et al. 1994, and Erturk et al. 1999)

When right-left differences were investigated, Lee et al. [19] found the complete and incomplete types in Koreans were more frequent on the right side (9.2%) than on the left (5.5%). In Americans, bilateral caroticoclinoid canals were frequent, and unilateral ones preferentially occurred on the left [13, 17]. In our study, incidence was higher on the left side for contact types, whereas there was no statistically significant difference in the incidence of complete and incomplete types.

The incidence of interclinoid osseous bridge was found to be 8.68% by Keyers [13], 2.22% by Azeredo et al. [1], 4% by Inoue et al. [12], 2% by Cireli et al. [3], 4.54% by Deda et al. [4], and 1.01% by Gurun et al. [9]. In our study, this incidence was as high as 8.18% (Table 3).

Gurun et al. [9] observed the middle clinoid process prominent bilaterally in 34.5% of cases, prominent in one side and rudimental on the other in 23.98% of their specimens. The middle clinoid process was rudimental in 41.52% and usually prominent in unilateral caroticoclinoid foramen. In our study, the middle clinoid process was prominent in 15.12% of the specimens.

The clinoidal ICA is defined above by the distal (upper) ring formed by the dura extending medially from the upper and lower surfaces of the ACP to surround the artery. The proximal (lower) dural ring is formed by the dura extending medially from the lower surface of the ACP and forms the border between the clinoidal and intracavernous ICA [2, 12, 26]. The proximal dural ring fuses medially with the endosteal dura of the carotid canal and provides attachment to the interclinoid ligament that attaches laterally to the posterior clinoid process [27].

The length of the clinoidal ICA (distance between the proximal and distal dural rings) was measured at 4.3 mm (range 2.9–6.3) by De Jesus [5] and at 4–6 mm by Dolenc [7]. Umansky et al. [27] found this distance to be 5.4 mm, and Inoue et al. [12] measured approximately 5 mm. We measured the clinoidal ICA at 4.51±0.44 mm (range 3.8–5.4), 4.42±0.39 mm on the right and 4.6±0.48 mm on the left (P<0.5).

The mean diameter of the distal ring was 5.25±0.58 mm (range 3.6–6.7), 5.24±0.66 mm on the right side and 5.25±0.53 mm on the left (P>0.5). The distance between the anterior clinoid processes was measured as 22.6±2.29 mm (range 18.74–27.06), and the middle clinoid processes were 11.51±1.75 mm (range 8.65–15.3).

The variations in clinoid processes of the sphenoid bone should be carefully studied by all neurosurgeons, especially for approaches to the cavernous sinus. The presence of an osseous bridge between the tip of the ACP and the middle or posterior clinoid process makes removal of the ACP difficult and increases the risk of rupturing or tearing the ICA, leading to fatal cerebral infarction, especially when aneurysm is present. It also makes it impossible to retract or mobilize the cavernous segment of the ICA even after releasing the proximal and distal dural rings. Therefore, preoperative recognition of the caroticoclinoid foramen by imaging studies has great clinical significance when approaching surgical lesions in the region [16].

This study presents morphometry and topographic features of the clinoidal region on bony and cadaveric specimens of a recent Turkish population as a guide for neurosurgeons to provide information on the limited intraoperative view and reduce mortality and morbidity in surgical approaches.

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© Springer-Verlag 2003