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Application of 3-Dimensional Computerized Tomography Angiography for Defining Cavernous Sinus Aneurysms and Intradural Aneurysms Involving the Internal Carotid Artery Around the Anterior Clinoid Process
Accepted Manuscript Application of 3D-computerized tomography angiography for Defining Cavernous Sinus Aneurysms and Intradural Aneurysms Involving the Internal Carotid Artery around the Anterior Clinoid Process Quan Cheng, Chun-Bo Huang, Jun-yu Wang, Bing Jiang, Long-Bo Zhang, Ming Zeng, Yuan-Bing Chen, Hong-Fu zhang, Feng-Hua Chen PII:
S1878-8750(17)31080-X
DOI:
10.1016/j.wneu.2017.06.172
Reference:
WNEU 6043
To appear in:
World Neurosurgery
Received Date: 23 January 2017 Revised Date:
26 June 2017
Accepted Date: 29 June 2017
Please cite this article as: Cheng Q, Huang C-B, Wang J-y, Jiang B, Zhang L-B, Zeng M, Chen Y-B, zhang H-F, Chen F-H, Application of 3D-computerized tomography angiography for Defining Cavernous Sinus Aneurysms and Intradural Aneurysms Involving the Internal Carotid Artery around the Anterior Clinoid Process, World Neurosurgery (2017), doi: 10.1016/j.wneu.2017.06.172. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
Application of 3D-computerized tomography angiography for Defining Cavernous Sinus Aneurysms and Intradural Aneurysms Involving the Internal Carotid Artery
Department of
1
Neurosurgery and
2
RI PT
around the Anterior Clinoid Process
Radiology, Xiangya Hospital, Center South
*
SC
University, Changsha , P. R. China;
Corresponding author: Fenghua Chen. Department of Neurosurgery, Xiangya Hospital,
M AN U
Center South University, Address: Changsha 410008, Hunan, P. R. China. Telephone:+86-731-89753738;Fax:+86-731-84327401 E-mail:[email protected]
Keywords: three-dimensional computerized tomography angiography; cavernous sinus
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aneurysm; intradural aneurysm; dural ring
Abbreviations: 3D-CTA, three-dimensional computed tomography angiography; CT, curved multiplannar reformation; MIP, maximum
EP
computed tomography; CMPR,
intensity projection reconstruction; MPR, multi-level reconstruction; VR, volume
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rendering
1
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Abstract Objective: The current study aimed to investigate the application of three-dimensional computed tomography angiography (3D-CTA) for defining cavernous sinus aneurysms
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and intradural aneurysms involving the internal carotid artery around the anterior clinoid process.
Methods: Results from 42 patients with an aneurysm of the internal carotid artery around
SC
the anterior clinoid process who underwent 3D-CTA were reviewed and compared with those of observed clinical operations.
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Results: Among the 42 patients, there was a total of 67 intracranial aneurysms of which 45 were aneurysms of the internal carotid artery around the anterior clinoid process. After surgery, 33 of the 45 aneurysms were confirmed as intradural aneurysms and the other 12 were confirmed as aneurysms in the cavernous sinus. 3D-CTA imaging of the medial
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sagittal plane showed that 31 (100%) out of 31 intradural aneurysms of the internal carotid artery were above the virtual line between the inferior border of the anterior clinoid process and the tuberculum sellae, and 12 (86%) out of 14 cavernous sinus
EP
aneurysms were below the virtual line (p<0.0001). Conclusions: The virtual line between the inferior border of the anterior clinoid process
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and the tuberculum sellae on 3D-CTA indicates the proximal dural ring of the internal carotid artery. This line helps differentiate cavernous sinus aneurysms from intradural aneurysms involving the internal carotid artery around the anterior clinoid process.
2
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Introduction Development of cavernous sinus aneurysms and intradural aneurysms involving the internal carotid artery around the anterior clinoid process is different according to the
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anatomical position. Cavernous sinus aneurysm are characterized by an extremely low risk or no risk in inducing subarachnoid hemorrhage, while intradural aneurysms have a high risk and require surgical or endovascular intervention. Therefore, the precise
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important issues in the clinical study of neurosurgery7.
SC
location of aneurysms by imaging approaches in such areas has become one of the most
The dural ring, which is the defining marker of cavernous sinus aneurysms and intradural aneurysms involving the internal carotid artery around the anterior clinoid process, consists of a proximal and distal ring. The clinoid process of the internal carotid artery is
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located between the two rings. The distal dural ring, which is the conventional anatomical dividing line of the inside and outside of the dura mater, has a thick anterolateral wall and is closely connected with the internal carotid artery, but the inner posterior wall of the
EP
dural ring is loose and sometimes incomplete. Therefore, subarachnoid space structures can extend into the posterior and inner side of the internal carotid artery and form a
AC C
“carotid cave”1. Generally, this cave is connected with the subarachnoid space, and as a result, the aneurysm of the clinoid process in the internal carotid artery can cause subarachnoid hemorrhage5,9.
Therefore, based on clinical practice, we consider that the proximal dural ring should be considered as the defining marker of cavernous sinus aneurysms and intradural
3
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aneurysms. However, currently, there is no imaging approach for visualizing the proximal dural ring. According to findings from micro-dissection, the proximal dural ring is located in the inferior border of the interior anterior clinoid process and extends toward
RI PT
the internal back side to form the base of the carotid cave and sellar diaphragm . However, because of the loose structure of the internal back side of the carotid cave, the internal rear side of the proximal dural ring actually connects with the sellar diaphragm, which
SC
extends forward and adheres to the tuberculum sellae at the same level9. Therefore, for bony landmarks, the virtual line between the inferior border of the anterior clinoid
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process and the tuberculum sellae could represent the level of the proximal dural ring (Figure 1). Because three-dimensional computed tomography angiography (3D-CTA) can indicate the relationship between the internal carotid artery and the bony anatomical structure around it, 3D-CTA might be able to locate cavernous sinus aneurysms and
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intradural aneurysms.
This study reviewed 3D-CTA images of patients with aneurysms of the internal carotid
EP
artery around the anterior clinoid process complicated by subarachnoid hemorrhage before and after surgery. We also defined the relationship between the proximal dural
AC C
ring and the aneurysm by the virtual line between the inferior border of the anterior clinoid process and the tuberculum sellae. These results were compared with those observed during surgery to evaluate 3D-CTA for its diagnostic value and its ability to locate cavernous sinus aneurysms and intradural aneurysms involving the internal carotid artery around the anterior clinoid process.
4
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Materials and Methods Study subjects This study reviewed 42 patients with internal carotid aneurysms around the anterior
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clinoid process who were diagnosed between January 2012 to August 2016. There were 17 men and 25 women aged 13-72 years (mean age: 50.6 years). All patients received a 3D-CTA examination before and after surgery, and were with the indications for surgery.
SC
Surgical operations were performed after the patients or the family signed written
Image acquisition and processing
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consent.
A dual-source spiral computed tomography (CT) machine (Somatom Definition, Siemens Medical Systems, Germany) was used for the study. Parameters of scanning were as
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follows: voltage was 100 KV; current was 250 mA; and acquisition was 64×0.6, with a pitch of 0.9, reconstruction slice thickness of 0.75 mm, an interval of 0.5 mm, and a matrix of 512×512. Contrast medium was 370 g/100 ml, with a volume of 70 ml.. We
EP
injected 20 g of nonionic contrast medium through the antecubital vein by tube at a speed of 4.0 ml/s. . A Siemens dedicated workstation for image reconstruction was used. Each
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patient completed the following treatments: (1) multi-level reconstruction (MPR) or curved multiplannar reformation (CMPR) involving axial + sagittal + coronal planes, if necessary, add a variety of the oblique planes; (2) volume rendering (VR); and (3) maximum intensity projection reconstruction (MIP).
Image evaluation and analysis
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Two neurosurgeon independently evaluated the images,disagreements were settled by the snior author. The
imaging evaluation neurosurgeon was independent of the study patients
and was not the operating surgeon.Main outcome measures included the shape, size, and
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neck width of the aneurysm, and the relationship between the tumor and the virtual line between the inferior border of the anterior clinoid process and the tuberculum sellae.
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Fisher's exact tests were used to compare proportions in this study.
Results
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There was a total of 67 intracranial aneurysms in 42 patients. Among these aneurysms, 45 were aneurysms of the internal carotid artery around the anterior clinoid process, with a minimum size of
1.6 mm, a maximum size of 31 mm, and a mean size of 7.9 mm. Of
the 45 aneurysms, 28 were located in the left internal carotid artery and 17 were located
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in the right internal carotid artery. Of the 45 aneurysms, 33 were diagnosed as dural aneurysms and 12 cavernous sinus aneurysms . Of the 33 dural aneurysms, 8 were ophthalmic aneurysms located in the anterior wall of the internal carotid artery. Of the 33
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dural aneurysms, 25 were aneurysms of the clinoid segment located in the medial wall or inner rear wall of the internal carotid artery. Typical 3D-CTA images were shown in
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Figures 2-4. As shown in Table 1, 3D-CTA imaging of the medial sagittal plane showed that 31 (100%) out of 31 intradural aneurysms of the internal carotid artery were above the virtual line between the inferior border of the anterior clinoid process and the tuberculum sellae, and 12 (86%) out of 14 cavernous sinus aneurysms were below the virtual line (p<0.0001), indicating that the virtual line between the inferior border of the anterior clinoid process and the tuberculum sellae on 3D-CTA helps differentiate
6
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cavernous sinus aneurysms from intradural aneurysms involving the internal carotid artery around the anterior clinoid process.
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Discussion
The distal dural ring is the conventional dividing line of the inner side and outer side of the dura mater. The posterior lateral wall of the distal dural ring is thick and closely
SC
connected with the internal carotid artery, while the inner rear wall is loose and sometimes incomplete. Therefore, subarachnoid space structures can protrude into the
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posterior and inner side of the internal carotid artery and form the carotid cave1. Kobayshi et al.6 first named this situation as the carotid cave, which generally connects with the subarachnoid space. Therefore, aneurysms in the clinoid segment could cause subarachnoid hemorrhage5, 9. We consider that the proximal dural ring is the defining
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marker of cavernous sinus aneurysms and intradural aneurysms.
In our study, we found that aneurysms in the clinoid segment of the internal carotid artery
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originated from the lateral wall of the internal carotid artery. Aneurysms were observed over the clinoid segment and ophthalmic segment, and were mostly in the clinoid
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segment, with only part of them in the ophthalmic segment. A possible reason for this finding might be that the lateral and anterior walls of the dural ring of the internal carotid artery are closely connected with the artery, with no bifurcation of the artery. Therefore, it is difficult for an aneurysm to form. We do not consider that the distal dural ring is a marker for defining whether an aneurysm is located within the dura mater. The proximal dural ring is more likely to be the defining marker between the cavernous sinus and the
7
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inside of the dura mater in the internal carotid artery. According to anatomical knowledge, the virtual line between the inferior border of the anterior clinoid process and the tuberculum sellae could represent the level of the proximal dural ring and clearly define
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cavernous sinus aneurysms and intradural aneurysms. The best direction for observation using 3D-CTA is from the inner side of the midline sagittal view, and we contralateral
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observed the ipsilateral tuberculum, anterior clinoid process, and internal carotid artery.
Previously, the origin of the ophthalmic artery was the conventional anatomical
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landmark , which was used to evaluate whether an aneurysm was extradural or intradural.10 However, because of individual variation in the areas from the origin of the ophthalmic artery, it has been reported that 85.7% of the ophthalmic artery originates from the inner side of cerebral dura mater and is located close to the distal end of the
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distal dural ring, 7.6% of the ophthalmic artery originates from the outer side of cerebral dura mater, and 6.7% of the ophthalmic artery originates between the inner and outer side of cerebral dura mater.4 Taptas11 reported that the anterior clinoid process could also be
EP
considered as a better anatomical landmark but because of the difference in volume and shape and the less clearly visualized with conventional angiography, it is not a
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convincing anatomical landmark3,8. With technical developments in recent years, MRI for defining aneurysms in the cavernous sinus of the internal carotid artery and cerebral dura mater has become a hot research topic. Tsuboi et al.14 applied contrast-enhanced 3-dimensional time-of-flight magnetic resonance angiographythat could distinguish the internal carotid artery, the cavernous sinus wall, aneurysms, and the outer structure of blood vessels. Thines et al.12,13 discovered that T2-weighted (fast spin echo) sequences
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showed a high signal in the cerebrospinal fluid. They found that the signal was significantly enhanced in a 3.0 T MRI spatial resolution study, while in continuous thin scanned image, the distal dural ring and relative anatomical relationship were confirmed wall folds of the dural cavernous sinus, and an aneurysm in
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by observation of the upper
the two sides of the cavernous sinus cavity was recognized. Watanabe et al.15 applied with use of fusion images with 3D-MR cisternography and MR angiography , and also
SC
clearly defined the border of cerebrospinal fluid and the cavernous sinus wall, which was used to define the distal dural ring, providing precise information of the relationship
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between the aneurysm and the roof of the cavernous sinus. However, in MRI, there are certain disadvantages to using the distal dural ring as a marker, including an unclear bony image, a long examination time, complex procedures, and unfavorable noise for patients with a ruptured aneurysm. Gonzalez et al.3 believed that the optic strut in CTA could
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precisely define the location of the proximal dural ring; if the aneurysm that originates proximal to the optic strut is observed to lie within the cavernous sinus. Conversely, the aneurysm that originates distal to the optic strut is identified intradurally. Liu et al16
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reported that the optic strut serves as an effective landmark in CTA source images for distinguishing between intradural and extradural paraclinoid aneurysms. However, an
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image of bone and the aneurysm can be developed at the same time, the aneurysm could be coverd
by the optic strut. Additionally, the posterior and anterior walls of the
internal carotid artery cannot be easily observed in coronal sections. In our study, 3D-CTA showed that intradural aneurysms were above the virtual line and aneurysms in the cavernous sinus were under the virtual line, which connects the inferior border of the anterior clinoid process and the tuberculum sellae based on sagittal plane observations.
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Although both our study and Gonzalez's study applied the bony landmark as the defining marker, 3D-CTA showed clearer and more direct image in our study; it can define the proximal dural ring more precisely and is more convenient for clinical applications.
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However, further prospective studies are required to validate our conclusion.
Conclusions
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In this study, we demonstrate that 3D-CTA using the virtual line between the inferior border of the anterior clinoid process and the tuberculum sellae as the surface of the
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proximal dural ring is a very effective method in differentiating cavernous sinus aneurysms from intradural aneurysms involving the internal carotid artery around the
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EP
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anterior clinoid process.
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References 1. Avci E, Bademci G, Ozturk A. Microsurgical landmarks for safe removal of anterior clinoid process. Minim Invasive Neurosurg. 2005;48:268-272.
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2. Bouthillier A, van Loveren HR, Keller JT. Segments of the internal carotid artery: a new classification. Neurosurgery. 1996;38:425-433.
3. Gonzalez LF, Walker MT, Zabramski JM, Partovi S, Wallace RC, Spetzler RF.
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Distinction between paraclinoid and cavernous sinus aneurysms with computed tomographic angiography. Neurosurgery. 2003;52:1131-1139.
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4. Horiuchi T, Tanaka Y, Kusano Y, Yako T, Sasaki T, Hongo K. Relationship between the ophthalmic artery and the dural ring of the internal carotid artery. Clinical article. J Neurosurg 2009;111:119-123.
5. Joo W, Funaki T, Yoshioka F, Rhoton AJ. Microsurgical anatomy of the carotid cave.
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Neurosurgery 2012;70:300-312.
6. Kobayashi S, Kyoshima K, Gibo H, Hegde SA, Takemae T, Sugita K. Carotid cave aneurysms of the internal carotid artery. J Neurosurg. 1989;70:216-221.
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7. Lee N, Jung JY, Huh SK, Kim DJ, Kim DI, Kim J. Distinction between Intradural and Extradural Aneurysms Involving the Paraclinoid Internal Carotid Artery with
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T2-Weighted Three-Dimensional Fast Spin-Echo Magnetic Resonance Imaging. J Korean Neurosurg Soc. 2010;47:437-441. 8. Murayama Y, Sakurama K, Satoh K, Nagahiro S. Identification of the carotid artery dural ring by using three-dimensional computerized tomography angiography. Technical note. J Neurosurg. 2001;95:533-536.
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9. Oikawa S, Kyoshima K, Kobayashi S. Surgical anatomy of the juxta-dural ring area. J Neurosurg. 1998;89:250-254. 10. Punt J. Some observations on aneurysms of the proximal internal carotid artery. J
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Neurosurg. 1979;1:151-154.
11. Taptas JN. Intradural and extradural ICA. J Neurosurg. 1979;51:877-878.
12. Thines L, Delmaire C, Le Gars D, Pruvo JP, Lejeune JP, Lehmann P, et al. MRI
SC
location of the distal dural ring plane: anatomoradiological study and application to paraclinoid carotid artery aneurysms. Eur Radiol. 2006;16:479-488.
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13. Thines L, Lee SK, Dehdashti AR, Agid R, Willinsky RA, Wallace CM, et al. Direct imaging of the distal dural ring and paraclinoid internal carotid artery aneurysms with high-resolution T2 turbo-spin echo technique at 3-T magnetic resonance imaging. Neurosurgery. 2009;64:1059-1064.
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14. Tsuboi T, Tokunaga K, Shingo T, Itoh T, Mandai S, Kinugasa K, et al. Differentiation between intradural and extradural locations of juxta-dural ring aneurysms by
using
contrast-enhanced
3-dimensional
time-of-flight
magnetic
resonance
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angiography. Surg Neurol. 2007;67:381-387. 15. Watanabe Y, Nakazawa T, Yamada N, Higashi M, Hishikawa T, Miyamoto S, et al.
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Identification of the distal dural ring with use of fusion images with 3D-MR cisternography and MR angiography: application to paraclinoid aneurysms. AJNR Am J Neuroradiol. 2009;30:845-850. 16 Comparison of the effectiveness of using the optic strut and tuberculum sellae as radiological landmarks in diagnosing paraclinoid aneurysms with CT angiography. PMID:26745492
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Figure legends Fig. 1. The virtual line(green line) between the inferior border of the anterior clinoid process(black ) and the tuberculum sellae (black triangle) could represent the level of the
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proximal dural ring.
Fig. 2. A male patient (65 years old) with an aneurysm in the anterior clinoid
SC
process of the left internal carotid artery
(A) Pre-surgery image: the virtual line connects the inferior border of the anterior clinoid
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process and the tuberculum sellae. The aneurysm is located above the virtual line. (B) Pre-surgery image: the asterisk indicates the an aneurysm in the aroud anterior clinoid process of the left internal carotid artery. (C) Post-surgery image: we confirmed in
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surgery that the aneurysm was the intradural aneurysms of the left internal carotid artery
Fig. 3. A Female patient (49 years old) with an aneurysm in the anterior clinoid process of the left internal carotid artery
EP
(A) Pre-surgery image: the virtual line connects the inferior border of the anterior clinoid process and the tuberculum sellae. The aneurysm is located above the virtual line. (B)
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Pre-surgery image: the asterisk indicates the an aneurysm in the aroud anterior clinoid process of the left internal carotid artery. (C) Post-surgery image: we confirmed in surgery that the aneurysm was the intradural aneurysms of the left internal carotid artery.
Fig. 4. A female patient (60 years old) with multiple aneurysms had a cavernous sinus aneurysm in the right internal carotid artery
13
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(A) Pre-surgery image: the virtual line connects the inferior border of the anterior clinoid process and the tuberculum sellae. The aneurysm is located above the virtual line. (B) Pre-surgery image: the asterisk indicates the an aneurysm in the aroud anterior clinoid
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process of the left internal carotid artery. This aneurysm was not able to be observed
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EP
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SC
during surgery
14
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Table 1. Differentiating cavernous sinus aneurysms from intradural aneurysms using 3D-
CTA imaging of the virtual line between the inferior border of the anterior clinoid process
Definitive Diagnosis CTA Diagnosis
Intradural Aneurysms
Cavernous Sinus Aneurysms
Intradural Aneurysms
31
0
Cavernous Sinus Aneurysms
2
12
Total
33
12
Total
p
SC
31
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TE D EP AC C
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and the tuberculum sellae
14
45
<0.0001
AC C
EP
TE D
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SC
RI PT
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AC C
EP
TE D
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SC
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EP
TE D
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SC
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EP
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Highlights
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SC M AN U TE D EP
•
The virtual line between the inferior border of the anterior clinoid process and the tuberculum sellae on 3D-CTA indicates the proximal dural ring of the internal carotid artery. This line helps differentiate cavernous sinus aneurysms from intradural aneurysms involving the internal carotid artery around the anterior clinoid process.
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•
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Disclosure-Conflict of Interest: None declared.
S1878-8750(17)31080-X
DOI:
10.1016/j.wneu.2017.06.172
Reference:
WNEU 6043
To appear in:
World Neurosurgery
Received Date: 23 January 2017 Revised Date:
26 June 2017
Accepted Date: 29 June 2017
Please cite this article as: Cheng Q, Huang C-B, Wang J-y, Jiang B, Zhang L-B, Zeng M, Chen Y-B, zhang H-F, Chen F-H, Application of 3D-computerized tomography angiography for Defining Cavernous Sinus Aneurysms and Intradural Aneurysms Involving the Internal Carotid Artery around the Anterior Clinoid Process, World Neurosurgery (2017), doi: 10.1016/j.wneu.2017.06.172. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
Application of 3D-computerized tomography angiography for Defining Cavernous Sinus Aneurysms and Intradural Aneurysms Involving the Internal Carotid Artery
Department of
1
Neurosurgery and
2
RI PT
around the Anterior Clinoid Process
Radiology, Xiangya Hospital, Center South
*
SC
University, Changsha , P. R. China;
Corresponding author: Fenghua Chen. Department of Neurosurgery, Xiangya Hospital,
M AN U
Center South University, Address: Changsha 410008, Hunan, P. R. China. Telephone:+86-731-89753738;Fax:+86-731-84327401 E-mail:[email protected]
Keywords: three-dimensional computerized tomography angiography; cavernous sinus
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aneurysm; intradural aneurysm; dural ring
Abbreviations: 3D-CTA, three-dimensional computed tomography angiography; CT, curved multiplannar reformation; MIP, maximum
EP
computed tomography; CMPR,
intensity projection reconstruction; MPR, multi-level reconstruction; VR, volume
AC C
rendering
1
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Abstract Objective: The current study aimed to investigate the application of three-dimensional computed tomography angiography (3D-CTA) for defining cavernous sinus aneurysms
RI PT
and intradural aneurysms involving the internal carotid artery around the anterior clinoid process.
Methods: Results from 42 patients with an aneurysm of the internal carotid artery around
SC
the anterior clinoid process who underwent 3D-CTA were reviewed and compared with those of observed clinical operations.
M AN U
Results: Among the 42 patients, there was a total of 67 intracranial aneurysms of which 45 were aneurysms of the internal carotid artery around the anterior clinoid process. After surgery, 33 of the 45 aneurysms were confirmed as intradural aneurysms and the other 12 were confirmed as aneurysms in the cavernous sinus. 3D-CTA imaging of the medial
TE D
sagittal plane showed that 31 (100%) out of 31 intradural aneurysms of the internal carotid artery were above the virtual line between the inferior border of the anterior clinoid process and the tuberculum sellae, and 12 (86%) out of 14 cavernous sinus
EP
aneurysms were below the virtual line (p<0.0001). Conclusions: The virtual line between the inferior border of the anterior clinoid process
AC C
and the tuberculum sellae on 3D-CTA indicates the proximal dural ring of the internal carotid artery. This line helps differentiate cavernous sinus aneurysms from intradural aneurysms involving the internal carotid artery around the anterior clinoid process.
2
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Introduction Development of cavernous sinus aneurysms and intradural aneurysms involving the internal carotid artery around the anterior clinoid process is different according to the
RI PT
anatomical position. Cavernous sinus aneurysm are characterized by an extremely low risk or no risk in inducing subarachnoid hemorrhage, while intradural aneurysms have a high risk and require surgical or endovascular intervention. Therefore, the precise
M AN U
important issues in the clinical study of neurosurgery7.
SC
location of aneurysms by imaging approaches in such areas has become one of the most
The dural ring, which is the defining marker of cavernous sinus aneurysms and intradural aneurysms involving the internal carotid artery around the anterior clinoid process, consists of a proximal and distal ring. The clinoid process of the internal carotid artery is
TE D
located between the two rings. The distal dural ring, which is the conventional anatomical dividing line of the inside and outside of the dura mater, has a thick anterolateral wall and is closely connected with the internal carotid artery, but the inner posterior wall of the
EP
dural ring is loose and sometimes incomplete. Therefore, subarachnoid space structures can extend into the posterior and inner side of the internal carotid artery and form a
AC C
“carotid cave”1. Generally, this cave is connected with the subarachnoid space, and as a result, the aneurysm of the clinoid process in the internal carotid artery can cause subarachnoid hemorrhage5,9.
Therefore, based on clinical practice, we consider that the proximal dural ring should be considered as the defining marker of cavernous sinus aneurysms and intradural
3
ACCEPTED MANUSCRIPT
aneurysms. However, currently, there is no imaging approach for visualizing the proximal dural ring. According to findings from micro-dissection, the proximal dural ring is located in the inferior border of the interior anterior clinoid process and extends toward
RI PT
the internal back side to form the base of the carotid cave and sellar diaphragm . However, because of the loose structure of the internal back side of the carotid cave, the internal rear side of the proximal dural ring actually connects with the sellar diaphragm, which
SC
extends forward and adheres to the tuberculum sellae at the same level9. Therefore, for bony landmarks, the virtual line between the inferior border of the anterior clinoid
M AN U
process and the tuberculum sellae could represent the level of the proximal dural ring (Figure 1). Because three-dimensional computed tomography angiography (3D-CTA) can indicate the relationship between the internal carotid artery and the bony anatomical structure around it, 3D-CTA might be able to locate cavernous sinus aneurysms and
TE D
intradural aneurysms.
This study reviewed 3D-CTA images of patients with aneurysms of the internal carotid
EP
artery around the anterior clinoid process complicated by subarachnoid hemorrhage before and after surgery. We also defined the relationship between the proximal dural
AC C
ring and the aneurysm by the virtual line between the inferior border of the anterior clinoid process and the tuberculum sellae. These results were compared with those observed during surgery to evaluate 3D-CTA for its diagnostic value and its ability to locate cavernous sinus aneurysms and intradural aneurysms involving the internal carotid artery around the anterior clinoid process.
4
ACCEPTED MANUSCRIPT
Materials and Methods Study subjects This study reviewed 42 patients with internal carotid aneurysms around the anterior
RI PT
clinoid process who were diagnosed between January 2012 to August 2016. There were 17 men and 25 women aged 13-72 years (mean age: 50.6 years). All patients received a 3D-CTA examination before and after surgery, and were with the indications for surgery.
SC
Surgical operations were performed after the patients or the family signed written
Image acquisition and processing
M AN U
consent.
A dual-source spiral computed tomography (CT) machine (Somatom Definition, Siemens Medical Systems, Germany) was used for the study. Parameters of scanning were as
TE D
follows: voltage was 100 KV; current was 250 mA; and acquisition was 64×0.6, with a pitch of 0.9, reconstruction slice thickness of 0.75 mm, an interval of 0.5 mm, and a matrix of 512×512. Contrast medium was 370 g/100 ml, with a volume of 70 ml.. We
EP
injected 20 g of nonionic contrast medium through the antecubital vein by tube at a speed of 4.0 ml/s. . A Siemens dedicated workstation for image reconstruction was used. Each
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patient completed the following treatments: (1) multi-level reconstruction (MPR) or curved multiplannar reformation (CMPR) involving axial + sagittal + coronal planes, if necessary, add a variety of the oblique planes; (2) volume rendering (VR); and (3) maximum intensity projection reconstruction (MIP).
Image evaluation and analysis
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Two neurosurgeon independently evaluated the images,disagreements were settled by the snior author. The
imaging evaluation neurosurgeon was independent of the study patients
and was not the operating surgeon.Main outcome measures included the shape, size, and
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neck width of the aneurysm, and the relationship between the tumor and the virtual line between the inferior border of the anterior clinoid process and the tuberculum sellae.
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Fisher's exact tests were used to compare proportions in this study.
Results
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There was a total of 67 intracranial aneurysms in 42 patients. Among these aneurysms, 45 were aneurysms of the internal carotid artery around the anterior clinoid process, with a minimum size of
1.6 mm, a maximum size of 31 mm, and a mean size of 7.9 mm. Of
the 45 aneurysms, 28 were located in the left internal carotid artery and 17 were located
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in the right internal carotid artery. Of the 45 aneurysms, 33 were diagnosed as dural aneurysms and 12 cavernous sinus aneurysms . Of the 33 dural aneurysms, 8 were ophthalmic aneurysms located in the anterior wall of the internal carotid artery. Of the 33
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dural aneurysms, 25 were aneurysms of the clinoid segment located in the medial wall or inner rear wall of the internal carotid artery. Typical 3D-CTA images were shown in
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Figures 2-4. As shown in Table 1, 3D-CTA imaging of the medial sagittal plane showed that 31 (100%) out of 31 intradural aneurysms of the internal carotid artery were above the virtual line between the inferior border of the anterior clinoid process and the tuberculum sellae, and 12 (86%) out of 14 cavernous sinus aneurysms were below the virtual line (p<0.0001), indicating that the virtual line between the inferior border of the anterior clinoid process and the tuberculum sellae on 3D-CTA helps differentiate
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cavernous sinus aneurysms from intradural aneurysms involving the internal carotid artery around the anterior clinoid process.
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Discussion
The distal dural ring is the conventional dividing line of the inner side and outer side of the dura mater. The posterior lateral wall of the distal dural ring is thick and closely
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connected with the internal carotid artery, while the inner rear wall is loose and sometimes incomplete. Therefore, subarachnoid space structures can protrude into the
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posterior and inner side of the internal carotid artery and form the carotid cave1. Kobayshi et al.6 first named this situation as the carotid cave, which generally connects with the subarachnoid space. Therefore, aneurysms in the clinoid segment could cause subarachnoid hemorrhage5, 9. We consider that the proximal dural ring is the defining
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marker of cavernous sinus aneurysms and intradural aneurysms.
In our study, we found that aneurysms in the clinoid segment of the internal carotid artery
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originated from the lateral wall of the internal carotid artery. Aneurysms were observed over the clinoid segment and ophthalmic segment, and were mostly in the clinoid
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segment, with only part of them in the ophthalmic segment. A possible reason for this finding might be that the lateral and anterior walls of the dural ring of the internal carotid artery are closely connected with the artery, with no bifurcation of the artery. Therefore, it is difficult for an aneurysm to form. We do not consider that the distal dural ring is a marker for defining whether an aneurysm is located within the dura mater. The proximal dural ring is more likely to be the defining marker between the cavernous sinus and the
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inside of the dura mater in the internal carotid artery. According to anatomical knowledge, the virtual line between the inferior border of the anterior clinoid process and the tuberculum sellae could represent the level of the proximal dural ring and clearly define
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cavernous sinus aneurysms and intradural aneurysms. The best direction for observation using 3D-CTA is from the inner side of the midline sagittal view, and we contralateral
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observed the ipsilateral tuberculum, anterior clinoid process, and internal carotid artery.
Previously, the origin of the ophthalmic artery was the conventional anatomical
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landmark , which was used to evaluate whether an aneurysm was extradural or intradural.10 However, because of individual variation in the areas from the origin of the ophthalmic artery, it has been reported that 85.7% of the ophthalmic artery originates from the inner side of cerebral dura mater and is located close to the distal end of the
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distal dural ring, 7.6% of the ophthalmic artery originates from the outer side of cerebral dura mater, and 6.7% of the ophthalmic artery originates between the inner and outer side of cerebral dura mater.4 Taptas11 reported that the anterior clinoid process could also be
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considered as a better anatomical landmark but because of the difference in volume and shape and the less clearly visualized with conventional angiography, it is not a
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convincing anatomical landmark3,8. With technical developments in recent years, MRI for defining aneurysms in the cavernous sinus of the internal carotid artery and cerebral dura mater has become a hot research topic. Tsuboi et al.14 applied contrast-enhanced 3-dimensional time-of-flight magnetic resonance angiographythat could distinguish the internal carotid artery, the cavernous sinus wall, aneurysms, and the outer structure of blood vessels. Thines et al.12,13 discovered that T2-weighted (fast spin echo) sequences
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showed a high signal in the cerebrospinal fluid. They found that the signal was significantly enhanced in a 3.0 T MRI spatial resolution study, while in continuous thin scanned image, the distal dural ring and relative anatomical relationship were confirmed wall folds of the dural cavernous sinus, and an aneurysm in
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by observation of the upper
the two sides of the cavernous sinus cavity was recognized. Watanabe et al.15 applied with use of fusion images with 3D-MR cisternography and MR angiography , and also
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clearly defined the border of cerebrospinal fluid and the cavernous sinus wall, which was used to define the distal dural ring, providing precise information of the relationship
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between the aneurysm and the roof of the cavernous sinus. However, in MRI, there are certain disadvantages to using the distal dural ring as a marker, including an unclear bony image, a long examination time, complex procedures, and unfavorable noise for patients with a ruptured aneurysm. Gonzalez et al.3 believed that the optic strut in CTA could
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precisely define the location of the proximal dural ring; if the aneurysm that originates proximal to the optic strut is observed to lie within the cavernous sinus. Conversely, the aneurysm that originates distal to the optic strut is identified intradurally. Liu et al16
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reported that the optic strut serves as an effective landmark in CTA source images for distinguishing between intradural and extradural paraclinoid aneurysms. However, an
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image of bone and the aneurysm can be developed at the same time, the aneurysm could be coverd
by the optic strut. Additionally, the posterior and anterior walls of the
internal carotid artery cannot be easily observed in coronal sections. In our study, 3D-CTA showed that intradural aneurysms were above the virtual line and aneurysms in the cavernous sinus were under the virtual line, which connects the inferior border of the anterior clinoid process and the tuberculum sellae based on sagittal plane observations.
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Although both our study and Gonzalez's study applied the bony landmark as the defining marker, 3D-CTA showed clearer and more direct image in our study; it can define the proximal dural ring more precisely and is more convenient for clinical applications.
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However, further prospective studies are required to validate our conclusion.
Conclusions
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In this study, we demonstrate that 3D-CTA using the virtual line between the inferior border of the anterior clinoid process and the tuberculum sellae as the surface of the
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proximal dural ring is a very effective method in differentiating cavernous sinus aneurysms from intradural aneurysms involving the internal carotid artery around the
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anterior clinoid process.
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References 1. Avci E, Bademci G, Ozturk A. Microsurgical landmarks for safe removal of anterior clinoid process. Minim Invasive Neurosurg. 2005;48:268-272.
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2. Bouthillier A, van Loveren HR, Keller JT. Segments of the internal carotid artery: a new classification. Neurosurgery. 1996;38:425-433.
3. Gonzalez LF, Walker MT, Zabramski JM, Partovi S, Wallace RC, Spetzler RF.
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Distinction between paraclinoid and cavernous sinus aneurysms with computed tomographic angiography. Neurosurgery. 2003;52:1131-1139.
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4. Horiuchi T, Tanaka Y, Kusano Y, Yako T, Sasaki T, Hongo K. Relationship between the ophthalmic artery and the dural ring of the internal carotid artery. Clinical article. J Neurosurg 2009;111:119-123.
5. Joo W, Funaki T, Yoshioka F, Rhoton AJ. Microsurgical anatomy of the carotid cave.
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Neurosurgery 2012;70:300-312.
6. Kobayashi S, Kyoshima K, Gibo H, Hegde SA, Takemae T, Sugita K. Carotid cave aneurysms of the internal carotid artery. J Neurosurg. 1989;70:216-221.
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7. Lee N, Jung JY, Huh SK, Kim DJ, Kim DI, Kim J. Distinction between Intradural and Extradural Aneurysms Involving the Paraclinoid Internal Carotid Artery with
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T2-Weighted Three-Dimensional Fast Spin-Echo Magnetic Resonance Imaging. J Korean Neurosurg Soc. 2010;47:437-441. 8. Murayama Y, Sakurama K, Satoh K, Nagahiro S. Identification of the carotid artery dural ring by using three-dimensional computerized tomography angiography. Technical note. J Neurosurg. 2001;95:533-536.
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9. Oikawa S, Kyoshima K, Kobayashi S. Surgical anatomy of the juxta-dural ring area. J Neurosurg. 1998;89:250-254. 10. Punt J. Some observations on aneurysms of the proximal internal carotid artery. J
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Neurosurg. 1979;1:151-154.
11. Taptas JN. Intradural and extradural ICA. J Neurosurg. 1979;51:877-878.
12. Thines L, Delmaire C, Le Gars D, Pruvo JP, Lejeune JP, Lehmann P, et al. MRI
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location of the distal dural ring plane: anatomoradiological study and application to paraclinoid carotid artery aneurysms. Eur Radiol. 2006;16:479-488.
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13. Thines L, Lee SK, Dehdashti AR, Agid R, Willinsky RA, Wallace CM, et al. Direct imaging of the distal dural ring and paraclinoid internal carotid artery aneurysms with high-resolution T2 turbo-spin echo technique at 3-T magnetic resonance imaging. Neurosurgery. 2009;64:1059-1064.
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14. Tsuboi T, Tokunaga K, Shingo T, Itoh T, Mandai S, Kinugasa K, et al. Differentiation between intradural and extradural locations of juxta-dural ring aneurysms by
using
contrast-enhanced
3-dimensional
time-of-flight
magnetic
resonance
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angiography. Surg Neurol. 2007;67:381-387. 15. Watanabe Y, Nakazawa T, Yamada N, Higashi M, Hishikawa T, Miyamoto S, et al.
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Identification of the distal dural ring with use of fusion images with 3D-MR cisternography and MR angiography: application to paraclinoid aneurysms. AJNR Am J Neuroradiol. 2009;30:845-850. 16 Comparison of the effectiveness of using the optic strut and tuberculum sellae as radiological landmarks in diagnosing paraclinoid aneurysms with CT angiography. PMID:26745492
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Figure legends Fig. 1. The virtual line(green line) between the inferior border of the anterior clinoid process(black ) and the tuberculum sellae (black triangle) could represent the level of the
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proximal dural ring.
Fig. 2. A male patient (65 years old) with an aneurysm in the anterior clinoid
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process of the left internal carotid artery
(A) Pre-surgery image: the virtual line connects the inferior border of the anterior clinoid
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process and the tuberculum sellae. The aneurysm is located above the virtual line. (B) Pre-surgery image: the asterisk indicates the an aneurysm in the aroud anterior clinoid process of the left internal carotid artery. (C) Post-surgery image: we confirmed in
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surgery that the aneurysm was the intradural aneurysms of the left internal carotid artery
Fig. 3. A Female patient (49 years old) with an aneurysm in the anterior clinoid process of the left internal carotid artery
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(A) Pre-surgery image: the virtual line connects the inferior border of the anterior clinoid process and the tuberculum sellae. The aneurysm is located above the virtual line. (B)
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Pre-surgery image: the asterisk indicates the an aneurysm in the aroud anterior clinoid process of the left internal carotid artery. (C) Post-surgery image: we confirmed in surgery that the aneurysm was the intradural aneurysms of the left internal carotid artery.
Fig. 4. A female patient (60 years old) with multiple aneurysms had a cavernous sinus aneurysm in the right internal carotid artery
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(A) Pre-surgery image: the virtual line connects the inferior border of the anterior clinoid process and the tuberculum sellae. The aneurysm is located above the virtual line. (B) Pre-surgery image: the asterisk indicates the an aneurysm in the aroud anterior clinoid
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process of the left internal carotid artery. This aneurysm was not able to be observed
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during surgery
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Table 1. Differentiating cavernous sinus aneurysms from intradural aneurysms using 3D-
CTA imaging of the virtual line between the inferior border of the anterior clinoid process
Definitive Diagnosis CTA Diagnosis
Intradural Aneurysms
Cavernous Sinus Aneurysms
Intradural Aneurysms
31
0
Cavernous Sinus Aneurysms
2
12
Total
33
12
Total
p
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31
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and the tuberculum sellae
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45
<0.0001
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Highlights
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The virtual line between the inferior border of the anterior clinoid process and the tuberculum sellae on 3D-CTA indicates the proximal dural ring of the internal carotid artery. This line helps differentiate cavernous sinus aneurysms from intradural aneurysms involving the internal carotid artery around the anterior clinoid process.
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Disclosure-Conflict of Interest: None declared.