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Key words - BACKGROUND: Anatomic variations of the anterior clinoid process (ACP)
- Anatomic variation of the anterior clinoid process should be recognized before clinoidectomy to ensure a safe approach. This study
- Caroticoclinoid foramen
- Extradural anterior clinoidectomy
describes the incidence of caroticoclinoid foramen (CCF), interclinoid osseous
- Interclinoid osseous bridge bridge, and pneumatization of the ACP during extradural anterior clinoidectomy.
- Paraclinoid aneurysms The problems and technical issues encountered in such cases are described.
- Pneumatization of the anterior clinoid process
- METHODS: Using multidetector-row computed tomography, 144 sides in 72
Abbreviations and Acronyms cases of paraclinoid aneurysm treated by extradural anterior clinoidectomy
ACP: Anterior clinoid process
AR: Anterior root were analyzed preoperatively.
CCF: Caroticoclinoid foramen - RESULTS:
CT: Computed tomography
CCF, interclinoid osseous bridge, and pneumatization of the ACP
EAC: Extradural anterior clinoidectomy were observed in 16.6%, 2.77%, and 27.7% of cases. Pneumatized patterns were
ICA: Internal carotid artery divided into 3 groups according to route: pneumatization via the optic strut (in
IOB: Interclinoid osseous bridge 74.1%), pneumatization via the anterior root (in 14.8%), and pneumatization via
OS: Optic strut
optic strut and anterior root (in 11.1%). CCF and interclinoid osseous bridge
Department of Neurosurgery, Stroke Center, Teishinkai represent obstacles to complete extradural removal of the ACP. The ACP should
Hospital, Hokkaido, Japan not be moved even after drilling the lateral wall of the ACP, orbital roof, and
To whom correspondence should be addressed: optic strut, so an intradural approach is sometimes needed. A CCF warrants
Nakao Ota, M.D.
[E-mail: nakao1980@gmail.com]
careful removal to open the distal dural ring. Awareness of the routes of
Citation: World Neurosurg. (2015).
pneumatization for the ACP should reduce the risk of tears in the paranasal
http://dx.doi.org/10.1016/j.wneu.2014.12.014 mucosa. If tears arise in the mucosa, suturing and closure are needed to prevent
Journal homepage: www.WORLDNEUROSURGERY.org liquorrhea.
Available online: www.sciencedirect.com
- CONCLUSIONS: Preoperative computed tomography is useful to detect vari-
1878-8750/$ - see front matter ª 2015 Elsevier Inc.
All rights reserved.
ations in the anatomy around the ACP. When performing extradural anterior
clinoidectomy in such anomalous cases, appropriate modifications are needed
INTRODUCTION
to ensure a safe approach.
Extradural anterior clinoidectomy (EAC),
first reported by Dolenc (4), facilitates
complete neck clipping of aneurysms in childhood. An IOB is an osseous bridge This study describes the incidence of
the paraclinoid region or radical removal between the tip of the ACP and posterior CCF, IOB, and pneumatization of the ACP
of tumors by providing wide operative clinoid process. This structure also involves during EAC and intraoperative findings,
exposure of the internal carotid artery (ICA) ossification of the interclinoid ligament along with technical perspectives on these
and superior surface of the cavernous sinus during development (15). The existence of anatomic variants. To our knowledge, this
with minimal brain retraction. However, these bony structures is an important is the first report to correlate preoperative
some anatomic variations of the anterior problem for neurosurgeons, complicating anatomic variation of the ACP with intra-
clinoid process (ACP) have been reported, removal of the ACP (8, 14). Even after operative findings.
such as a caroticoclinoid foramen (CCF), release of the distal dural ring, these
interclinoid osseous bridge (IOB) (3, 5-7, structures encumber mobilization of the
10-12), and pneumatization of the ACP ICA (4). MATERIALS AND METHODS
(2, 9, 13). Pneumatization of the ACP involves During the period April 2012eDecember
CCF was first described by Henle (6) as an extending a paranasal sinus such as the 2013, we examined 144 sides in 72 cases of
osseous bridge between the tip of the middle sphenoid or ethmoid sinus into the ACP paraclinoid aneurysm treated by clipping or
clinoid process and ACP. According to through the optic strut (OS) or anterior trapping with bypass using EAC. Surgical
Williams et al. (15) and Lang (12), this root (AR). Tearing these paranasal sinuses indications were determined with reference
bony structure is formed by ossification can cause pneumocephalus or liquorrhea to the 2009 Japanese guidelines for the
of the caroticoclinoid ligament in early (1, 7, 9, 13). management of stroke. All 144 sides were
analyzed preoperatively for the presence or In each of the patients, helical CT of the external carotid artery-to-middle cerebral
absence of CCF, IOB, or pneumatization of head was performed using a 320-row CT artery anastomosis. A CCF was observed in
ACP using 320-row multidetector computed scanner (Aquilion ONE ViSION Edition; 12 of 72 cases (16.6%): unilaterally in 6 cases
tomography (CT). Although Keyes (11) Toshiba Medical Systems, Tochigi, Japan). (8.3%) and bilaterally in 6 cases (8.3%). Of
classified CCFs into 3 groups of complete Scanning was performed with a collima- the 18 sides showing a CCF, complete type
type, incomplete type, and contact type, tion of 0.5 mm and 0.25-mm slice recon- was observed in 9 sides (50.0%), and
preoperative CT and intraoperative struction. Digital CT data were transferred incomplete type was observed in 9 sides
findings made it difficult to distinguish to the Ziostation 2 version 2.1.x (Qi Im- (50.0%). An IOB was seen in 2 cases (2.8%):
between complete and contact types, and aging, Redwood City, California, USA) unilaterally in 1 case (1.4%) and bilaterally in
so we classified CCFs into 2 groups: for review, axial reconstruction, and three- 1 case (1.4%). Pneumatization of the ACP
complete type (including contact type) and dimensional analysis. was observed in 20 cases (27.7%): unilater-
incomplete type (Figure 1A and B). ally in 13 cases (18.0%) and bilaterally in 7
An IOB was defined as a bony structure cases (9.7%). Patterns of pneumatization
bridging between the apex of the ACP and RESULTS were divided into 3 groups according to the
the posterior clinoid process (Figure 1C). The 72 cases comprised 64 women and 8 route: pneumatization via the OS in 74.1%;
Pneumatization of the ACP was defined men with a mean age of 57.3 years (range, via the AR in 14.8%; and via the OS and AR
as a paranasal sinus extending into the 31e78 years). In terms of treatment, 68 an- in 11.1% (Table 1). No discrepancies were
ACP (even if only slightly) through the AR eurysms were treated by direct clipping, and seen between preoperative CT findings
or OS (Figure 1D and E). 4 aneurysms were treated by trapping with and intraoperative anatomic findings.
Figure 1. Thin-slice computed tomography images of 2 types of and middle clinoid processes but do not touch (arrowhead). (C) Interclinoid
caroticoclinoid foramen (CCF) (A, B), interclinoid osseous bridge (C), and osseous bridge. Spicules of bone extend posteriorly from the anterior and
pneumatization of the anterior clinoid process (D, E). (A) Complete-type posterior clinoid processes. (D) Pneumatization of the anterior clinoid
CCF. The foramen and bridge show the normal anatomy (arrowhead). (B) process is observed via the optic strut (arrowhead). (E) Pneumatization is
Incomplete-type CCF. Spicules of bone extend medially from the anterior observed via the anterior root (arrowhead).
Number of cases 72
Sex
Female 64
Male 8
Patient age (years)
Mean 57.3
Range 31e78
Caroticoclinoid foramen 12 (16.6%)
Bilateral cases 6 (8.3%)
Figure 2. Computed tomography (CT) results. (A) CT angiography shows an unruptured aneurysm
Complete type 9 sides (50%) arising from the C2 portion of the internal carotid artery (arrowhead). (BeD) Three-dimensional
Incomplete type 9 sides (50%) reconstruction of CT images reveals complete-type caroticoclinoid foramen on the left side
(arrowhead) and incomplete-type on the right.
Interclinoid osseous bridge 2 (2.8%)
Bilateral cases 1 (1.4%)
Unilateral cases 1 (1.4%) After removal of this bony structure, the side ICAeposterior communicating artery
ICA achieved sufficient mobility. aneurysm. Preoperative CT angiography
Pneumatization of ACP 20 (27.7%)
revealed that EAC was needed to secure the
Bilateral cases 7 (9.7%) Case 2: Pneumatization of ACP via OS. A ICA because the aneurysm and posterior
Via OS 20 sides (74.1%) 60-year-old woman presented with a right- communicating artery existed close to the
side ICA aneurysm proximal to the poste- distal dural ring. Preoperative CT revealed
Via AR 4 sides (14.8%)
rior communicating artery (Figure 4A). To pneumatization of the ACP via the AR
Via OS and AR 3 sides (11.1%) secure the proximal ICA, clinoidectomy (Figure 6). Aneurysm clipping with EAC was
ACP, anterior clinoid process; AR, anterior root; OS, was needed because the aneurysm arose performed. Immediately after drilling of the
optic strut. immediately after perforating the distal compact bone of the lateral margin of the
dural ring (Figure 4B). Preoperative CT ACP (Figure 7A), the paranasal mucous
revealed a pneumatized ACP via the OS membrane was identified via the AR
(Figure 4CeE). Aneurysm clipping with (Figure 7B). The mucosal tissue was
Illustrative Cases EAC was performed. After drilling the pushed superomedially in the direction
Case 1: Complete-Type CCF. A 44-year-old cancellous bone of the ACP (Figure 5A), a of the optic canal (Figure 7C). The thin
woman presented with a left-side anterior thin bulkhead of compact bone appeared compact bone covering the optic canal was
wall aneurysm of the ICA (Figure 2A). (Figure 5B). Paranasal mucosa via the OS identified under the mucous membrane
Preoperative CT and three-dimensional to the sphenoid sinus appeared under (Figure 7D). After skeletonization by
reconstruction imaging showed a left-side this compact bone (Figure 5C). Using a drilling of the lateral wall of the ACP,
complete-type CCF and a right-side incom- microdissector, the mucous membrane orbital roof, and OS, the ACP was removed
plete-type CCF (Figure 2BeD). Clipping with was pushed anteromedially toward the ICA extradurally.
EAC was performed. The ACP could not be (Figure 5D). Careful drilling of compact
moved even after skeletonization by drilling bone covering the C3 portion of the ICA Case 4: Pneumatization of ACP via OS and
the lateral wall of the ACP, orbital roof, was performed (Figure 5E), and the ACP AR. A 78-year-old woman presented with a
and OS (Figure 3A). The intradural was removed. After opening the dura right-side ICAesuperior hypophyseal artery
approach was added by drilling to mater, the distal dural ring (Figure 5F) and aneurysm. Preoperative CT revealed com-
determine the apex of the ACP (Figure 3B) aneurysm were identified. After opening plete alteration of the cancellous bone of
and investigate bony structures continuing the distal dural ring inferiorly to preserve the ACP to the paranasal sinus (Figure 8).
to the medial clinoid process (Figure 3C). the neck of the aneurysm (Figure 5G), neck Aneurysm clipping with EAC was
The CCF was covered by the distal dural clipping was performed (Figure 5H). performed. Immediately after drilling the
ring. After careful drilling of the ACP, a lateral wall of the lesser wing of the
bony structure continuing to the middle Case 3: Pneumatization of ACP via AR. A sphenoid bone, the mucosa of the
clinoid process was observed (Figure 3D). 45-year-old woman presented with a right- paranasal sinus was identified under the
compact bone. The first mucosal tissue canal (Figure 9A). After pushing up the paranasal sinus via the OS (Figure 9A).
obtained was parallel to the AR and mucosa, a thin bulkhead of compact bone After careful drilling of the thin compact
pushed superomedially toward the optic was found and separated from the bone, the mucosa along the OS was
observed (Figure 9B). The mucosa was
tucked into the OS. Below the mucosa,
the C3 portion of the ICA was seen to be
covered by thin compact bone (Figure 9C).
The apex of the ACP was removed
extradurally (Figure 9D).
DISCUSSION
EAC is an established and safe approach
that allows extensive removal of the ACP
and creation of a wide operative field
(4, 16), but anatomic variations of the ACP
and ophthalmic artery must be kept in
mind to ensure a safe, less invasive
approach. The present study emphasizes
the anatomic importance of the CCF, IOB,
and pneumatization of the ACP.
The sphenoid bone receives attachments
from 3 ligaments: the pterygospinous liga-
Figure 5. Intraoperative findings in case 2. After drilling away the cancellous bone of the anterior
clinoid process (arrowhead) (A), thin compact bone is seen (arrowhead) (B). Paranasal mucosa via the ment between the spine and upper part
optic strut to the sphenoid sinus is seen under this compact bone (arrowhead) (C). Using the of the lateral pterygoid plate, the interclinoid
microdissector, the mucous membrane is pushed inferomedially toward the internal carotid artery ligament between the anterior and posterior
(ICA) (D). Careful drilling of the compact bone covering the C3 portion of the ICA is performed (E), and
the ACP is removed. After opening the dura mater, the distal dural ring (arrowhead) (F) and aneurysm
clinoid processes, and the caroticoclinoid
are identified. After opening the distal dural ring inferiorly (arrowhead) to preserve the neck of the ligament between the anterior and middle
aneurysm (G), neck clipping is performed (H). ON, optic nerve; C3, C3 portion of the internal carotid clinoid processes (15). Some of these
artery; C2, C2 portion of the internal carotid artery; An, aneurysm.
ligaments may ossify, resulting in
alteration of the interrelationships in
anatomic configurations. The latter 2
showed complete-type CCFs, IOBs, and Immediately after drilling the cancellous ligaments are the CCF and IOB. Fibrous
pneumatization of the ACP via the OS and bone of the lesser wing, the compact bone ossification of ligaments is considered a
AR on both sides (Figure 12). Aneurysm covered by mucous membrane via the AR normal physiologic process that occurs
clipping with EAC was performed. was revealed and pushed superomedially with aging, but these ligaments represent
Figure 6. Computed tomography (CT) findings for case 3. (A) CT angiography reveals the aneurysm
arising from the bifurcation of the internal carotid artery and posterior communicating artery. (B) The
aneurysm exists very close to the anterior clinoid process (arrowhead). (CeD) Thin-slice CT shows
bilateral anterior clinoid process pneumatization via the anterior root. An, aneurysm.
Figure 9. Intraoperative findings in case 4, from the right-side approach. (A) sinus is seen. (D) The mucosa of the sphenoid sinus is tucked into the optic
Immediately after drilling the lateral wall of the anterior clinoid process, the strut. Below the mucosa, the C3 portion of the internal carotid artery
mucosa of the paranasal sinus is identified under the compact bone covered in thin compact bone is seen. (E) The apex of the anterior clinoid
(arrowhead). (B) The paranasal sinus is tucked into the anterior root. Thin process is removed extradurally. (F) After opening the dura mater and distal
compact bone covers the mucosa of the sphenoid sinus (arrowhead). (C) dural ring, the aneurysm is shown in the carotid cave. ON, optic nerve; m,
After careful drilling of the thin compact bone, the mucosa of the sphenoid mucosa of the paranasal sinus; C3, C3 portion of the internal carotid artery.
The presence of CCF makes it difficult to findings, the CCF is covered by the distal pneumatized patterns were divided into 3
remove the ACP purely extradurally dural ring. The CCF can be understood as groups according to the route: pneumati-
because detachment of the apex of the ACP a kind of bony distal dural ring. zation occurred via the OS in 41 sides
from the bony structures of the CCF re- IOB was reported in 8.68% of cases in (74.5%), via the AR in 8 sides (14.8%), and
quires drilling under the siphon of the ICA. the series described by Keyes (11). In our via OS and AR in 6 sides (10.9%). The
Intradural drilling out can be performed in study, the incidence of this finding was incidence of ACP pneumatization in our
cases in which full elevation of the dura 1.58%. IOB is less frequent than CCF. series was 27.7%, representing the most
propria from the cavernous membrane and This anomaly should also be confirmed frequent variation when performing ante-
apex is confirmed. However, to ensure a preoperatively because the bony bridge rior clinoidectomy. As in case 2, cases of
safe approach, we recommend extradural continues to the posterior clinoid process pneumatization of the ACP via OS and AR
and intradural removal because the bony and can be drilled deeply to the posterior appeared to involve mucous membrane via
structures of the CCF and apex of the ACP clinoid process. En bloc removal of the OS and AR distinguishable by thin
can be confirmed from a broader space ACP is impossible, and careful drilling compact bone. This is an important point
than with an extradural-only approach and detachment of 4 parts (lateral wall of when performing clinoidectomy because
(Figure 11). The neurosurgeon should the ACP, OS, orbital roof, and IOB) is the direction in which the mucous mem-
be aware of the presence of a CCF required. In cases requiring aneurysm brane of the paranasal sinus needs to be
preoperatively to avoid excessive or clipping, careful extradural drilling is pushed can be predicted preoperatively.
unsuitable manipulation of surrounding needed until sufficient exposure of the Involvement of mucous membrane via the
tissues, which may result in injury of distal dural ring and good mobility of the OS is pushed inferomedially toward the
the ICA, optic nerve, or oculomotor ICA can be achieved. If space for drilling ICA, whereas involvement of mucous
nerve. Even after removal of the ACP, as is insufficient, an intradural approach is membrane via the AR is pushed super-
presented in case 1, bony structures to also needed. omedially toward the optic canal. The
the medial clinoid process prevent Mikami et al. (13) reported 600 sides in neurosurgeon should be familiar with the
mobility of the ICA. This structure must 300 consecutive patients using bony anatomy when performing drilling of
be removed to the fullest extent possible. multidetector-row CT. Pneumatization of the ACP so that the cancellous bone of the
As evidenced by the intraoperative the ACP was found in 55 sides (9.2%), and ACP replaces the paranasal sinus, which is
Figure 10. Computed tomography (CT) findings in case 5. (A) CT angiography reveals an unruptured
aneurysm arising from the C2 portion of the internal carotid artery. (BeD) Three-dimensional CT
reconstruction and thin-slice CT shows an interclinoid osseous bridge on the right side (arrowhead)
and incomplete-form interclinoid osseous bridge on the left side.
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