Dural Artery from Supraclinoid Internal Carotid Artery to Anterior Clinoid Process: Origin, Course, and Clinical Implications

Dural Artery from Supraclinoid Internal Carotid Artery to Anterior Clinoid Process: Origin, Course, and Clinical Implications

Original Article Dural Artery from Supraclinoid Internal Carotid Artery to Anterior Clinoid Process: Origin, Course, and Clinical Implications Pravin...

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Original Article

Dural Artery from Supraclinoid Internal Carotid Artery to Anterior Clinoid Process: Origin, Course, and Clinical Implications Pravin Salunke, Apinderpreet Singh, Rajasekhar Rekhapalli

BACKGROUND: Dura of the anterior clinoid process (ACP) is presumably supplied by the ophthalmic and external carotid artery branches. There is a less recognized artery described by Yasargil that arises directly from the supraclinoid internal carotid artery (ICA) and supplies the ACP dura. We studied the origin and course of this direct branch in patients in whom the carotid cistern was dissected for lesions not involving the carotid cistern and ACP dura. The management implications of this arterial twig have been described.

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METHODS: Thirty patients operated through the transsylvian route for suprasellar lesions were included. The arterial branch from the supraclinoid ICA to the clinoidal dura was dissected and studied under high magnification.

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RESULTS: A thin solitary artery could be delineated in 21 patients. In 14 patients, it originated from the dorsomedial surface of the ICA at its bifurcation close to the A1 origin. In the remaining 7, it was seen arising from the dorsomedial surface of the ICA, 2e4 mm proximal to bifurcation. The artery coursed from medial to lateral and pierced the clinoidal dura, 1e3 mm lateral to the entry of the carotid artery. The artery had no branches.

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CONCLUSIONS: The knowledge of this arterial twig to the clinoidal dura is important as this supply may be responsible for feeding the tumor arising from the dura arising from the anterior clinoid, making preoperative embolization impossible. In addition, the tumor may grow along with this vessel and infiltrate the adventitia of the ICA at the origin of this vessel.

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INTRODUCTION

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he arterial supply of anterior cranial base is shared between the branches of the internal carotid artery (ICA) and external carotid artery (ECA). In general, the midline segment is supplied by ethmoidal arteries (indirect ICA branches) and the lateral segment by branches of the ECA.1 The clinoid process is the portion that connects the lateral and middle segments with the optic canal medially and lacrimal foramen laterally. It is likely that the dura over the anterior clinoid is supplied by the ophthalmic artery, lacrimal artery (indirect branches form the ICA), and its anastomosis with the recurrent meningeal branch from the middle meningeal artery (ECA branch).2 A direct branch from the ICA arising close to its bifurcation has been described by Yasargil but is less recognized.3 This has implications, especially in the management of dural-based lesions of anterior clinoid process. These lesions may have a predominant blood supply from the ICA and are not amenable to preoperative embolization despite advances in the techniques.4 We have attempted to delineate this less recognized direct branch from the ICA to the clinoid and discussed the implications thereof.

MATERIALS AND METHODS Thirty consecutive patients operated for suprasellar masses through the transsylvian route were included prospectively. The mean age was 33.2 years (range: 3e65 years). The ratio of male and female patients was 1:1. Of them, 19 patients had craniopharyngioma, 7 had tuberculum sella meningioma, 2 had an optic pathwayehypothalamic glioma and 2 had functional large residual pituitary macroadenoma (acromegaly). None of them had tumors involving the carotid cistern. Patients with subarachnoid bleed were not included as cisternal blood makes it difficult to delineate apparently inconspicuous twigs.

Key words Anterior clinoid process - Dural blood supply - ICA branches - Meningioma - Supraclinoid ICA

Department of Neurosurgery, PGIMER, Chandigarh, India

Abbreviations and Acronyms ACP: Anterior clinoid process ECA: External carotid artery ICA: Internal carotid artery

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To whom correspondence should be addressed: Apinderpreet Singh, M.Ch. [E-mail: [email protected]] Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2018.12.071 Journal homepage: www.journals.elsevier.com/world-neurosurgery 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.

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ICA BRANCH TO ACP

We do not routinely obtain preoperative angiograms for managing such lesions. However, the preoperative angiogram was obtained in 2 patients in whom an associated aneurysm was suspected. Patients were positioned supine with neck extension, contralateral lateral tilt, and 15- to 20-degree rotation. A curvilinear frontotemporal skin incision was used to raise the frontotemporal myocutaneous flap. Frontotemporal craniotomy and sphenoid ridge excision up to the orbitotemporal periosteal band were performed using a high-speed drill. After reflection of dura, the sylvian fissure was dissected from lateral to medial using the operating microscope. Static retraction of brain was avoided as much as possible. The pace of dissection was deliberately slowed down and switched to high magnification as we approached the carotid cistern. While opening the carotid cistern, the arterial twig supplying the dura of clinoid was carefully dissected and traced up to its origin. The number, site of origin, and its course were noted. RESULTS In 21 patients, a solitary artery could be dissected and delineated from its origin to the dura. In the remaining 9 patients, we were not able to identify this separate vessel. The branch was of the size of an ICA perforator. The twig originated from the superomedial surface of the ICA close to its bifurcation, just proximal to the origin of the anterior cerebral artery in 14 patients (Figure 1A, B). The origin was about 2e4 mm proximal to bifurcation in the remaining 7 patients (Figure 1C). In all 21 patients it consistently branched from the dorsomedial surface of the ICA. After its origin the artery coursed from medial to lateral on the dorsal surface of the ICA and then traversed straight to the clinoid process to pierce the dura. The point where it pierced the dura was consistently lateral to the exiting point of the ICA on the edge of dural fold. The point of dural entry ranged between 1 and 3 mm from the lateral surface of ICA at its exit beneath the

Figure 1. (ALC) Intraoperative images of 3 different patients with variation in the origin and its course of the twig from the internal carotid artery (ICA) to the clinoidal dura. (A) Branch arising from the dorsal aspect of the ICA at the bifurcation and coursing straight to the clinoidal dura (arrows). (B) Origin of clinoidal artery from the dorsomedial aspect of the ICA at the

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ACP. It neither gave any branches as it coursed nor ramified into a network of small vessels close to the dural surface. Intraoperatively, the dural artery was seen in both the patients in whom a preoperative angiogram was obtained. However, on retrospective analysis the preoperative angiogram did not reveal any separate dural branch from the ICA to the ACP. DISCUSSION There is a significant overlap in the vascular supply around the orbit with a rich collateral network between ICA and ECA branches. In cases of ICA occlusion, blood flows through these collaterals from ECA, preventing ischemia of cerebral and visual apparatus, unless the end arteries are blocked. The branches from the ophthalmic and middle meningeal artery form a major part of this preexisting anastomotic channel.2 Knowledge of this anastomosis and its variation is important for surgeons, especially if preoperative embolization is planned. There is a risk of central retinal artery occlusion causing blindness when embolizing within this region, or stroke due to retrograde filling of the ICA.5 Occasionally, the ECA branches may predominantly supply the optic nerve and nerve head due to persistence of embryonic channels.2 The anterior clinoid process extends medially from the body of the sphenoid to the lacrimal foramen laterally. Laterally the ACP is covered by the sphenoorbital fold. The recurrent orbitomeningeal artery, an anastomotic branch between the ophthalmic artery and middle meningeal artery, traverses through this fold and is likely to irrigate the ACP and its dura. The medial portion possibly receives its blood supply from the ethmoidal arteries while the lateral edge receives it from the meningeal branches.1,2 The recurrent orbitomeningeal artery is likely to supply the dural fold. Direct dural branches from the ICA arise from its cavernous segment. It is considered that the supraclinoid ICA or its branches do not give any direct branches to the dura. Rarely, the dura over

bifurcation closer to the A1 origin and curving dorsolaterally over the ICA to supply the clinoidal dura (arrows). (C) Clinoidal artery originating from the dorsomedial aspect (arrow) of the ICA but 3 mm proximal to the ICA bifurcation curving dorsolaterally into clinoidal dura.

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ORIGINAL ARTICLE PRAVIN SALUNKE ET AL.

Figure 2. (A) Preoperative contrast magnetic resonance image showing a left clinoid meningioma encasing the internal carotid artery (ICA), middle cerebral artery (MCA), and anterior cerebral artery (ACA) (triad). (B) Digital subtraction angiography (DSA) showing ipsilateral ECA study with no flow/blush to meningioma. (C and D) DSA, anteroposterior view

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ICA BRANCH TO ACP

showing tumor blush from the ipsilateral ICA appearing in the early phase and persisting until the late phase along the entire supraclinoid ICA. (E and F) Lateral view of the DSA showing persistent ICA blush of tumor. However no flow/blush is noticed from the ophthalmic branch (open black arrows), which is seen separately and away from the tumor.

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the planum may be supplied by direct branches from the anterior cerebral arteries.5 Though other dural arteries from the intradural ICA and its branches are infrequent, the artery to clinoidal dura from the supraclinoid ICA is more or less a regular phenomenon and has been described.3 According to Yasragil, his dural branch arises from the superomedial surface of ICA bifurcation and occasionally from A1.3 In our study, we found the artery to arise from ICA bifurcation or 2e4 mm proximal to it. These dural twigs had a small caliber and are unlikely to be identified on preoperative angiograms. The dural-based tumors like meningiomas possibly derive their blood supply from branches supplying the dura. Preoperative embolization of these arteries reduces the vascularity and facilitates surgical extirpation. In case of anterior skull base meningiomas, the blood supply is usually from the middle meningeal, internal maxillary, or ethmoidal arteries. In the past, embolization of these branches was fraught with the danger of a retrograde stroke or central retinal occlusion and blindness due to a collateral network. With advances in neurointervention, the ethmoidal arteries can be embolized with relative safety.4 Despite these advances, the access to ethmoidal arteries has been difficult due to invasiveness and the size of the tumor. In such case it is possible to surgically ligate these vessels, allowing good resection of tumor.6 Unfortunately, the clinoidal meningiomas form a distinct entity. The digital subtraction angiography of patients with clinoid meningiomas show blush mainly around the supraclinoid ICA (Figure 2) all along its entire length until bifurcation and not the ECA or ophthalmic artery or its branches. This possibly indicates that the tumors derive their blood supply from the supraclinoid ICA and not from ophthalmic or ECA branches. It is likely that the direct branch from the supraclinoid ICA to ACP dura supplies the meningioma. With this branch of ICA

REFERENCES 1. Martins C, Yasuda A, Campero A, Ulm AJ, Tanriover N, Rhoton AJ. Microsurgical anatomy of the dural arteries. Neurosurgery. 2005;56(suppl 2): 211-251. 2. Perrini P, Cardia A, Fraser K, Lanzino G. A microsurgical study of the anatomy and course of the ophthalmic artery and its possibly dangerous anastomoses. J Neurosurg. 2007;106:142-150. 3. Yasargil MG. Operative anatomy. In: Yasargil MG, ed. Microneurosurgery. 1st ed. New York, NY: Georg Thieme Verlag Stuttgart; 1984:70-71. 4. Terada T, Kinoshita Y, Yokote H, et al. Preoperative embolization of meningiomas fed by ophthalmic branch arteries. Surg Neurol. 1996;45:161-166.

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feeding the tumor, it is impossible to embolize or surgically ligate/ coagulate it before tumor excision. Large meningiomas tend to engulf the arteries.7 However, the arachnoid between the vessel and tumor makes resection from these vessels possible. Rarely, the meningioma may infiltrate the adventitia of the artery by breaching the arachnoid.8 The ICA lacks arachnoid in the cavernous sinus, where such involvement is more common.9 In its supraclinoid course, the artery and its branches are suspended in arachnoid layers with trabeculae, making infiltration of the vessel wall difficult. The arterial twig after piercing the dura would lack arachnoid. As it feeds the meningioma, the cells may grow along the artery right to its origin from the ICA and infiltrate the adventitia at that point. The origin of this vessel is close to bifurcation, making tumor dissection risky at this point. In surgeries for other pathologies, this arterial twig can be sacrificed while dissecting in the carotid cistern. However, there is the possibility of this branch being larger and its avulsion from the origin would lead to profuse bleeding from the ICA.

Limitations We tried to delineate this arterial twig in the cadaveric head after injection of dye. Unfortunately, the artery could not be delineated properly. In conclusion, a neurosurgeon/neurointerventionist should of aware of this thin twig from the ICA, which irrigates the ACP dura. This vessel is likely to supply the tumors arising from anterior clinoid dura, making preoperative embolization difficult. Surgically, it can be sacrificed without any risks. However, in cases of meningiomas it may be a potential cause of infiltration of ICA adventitia.

5. Signorelli F, Scholtes F, Kauffmann C, McLaughlin N, Bojanowski MW. Dural artery from the anterior cerebral artery to the planum sphenoidale. Acta Neurochir (Wien). 2010;152:1807-1808. 6. Cecchini G. Anterior and posterior ethmoidal artery ligation in anterior skull base meningiomas: a review on microsurgical approaches. World Neurosurg. 2015;84:1161-1165. 7. McCracken DJ, Higginbotham RA, Boulter JH, et al. Degree of vascular encasement in sphenoid wing meningiomas predicts postoperative ischemic complications. Neurosurgery. 2017;80:957-966. 8. Rim NJ, Kim HS, Kim SY. A "benign" sphenoid ridge meningioma manifesting as a subarachnoid hemorrhage associated with tumor invasion into the middle cerebral artery. Kor J Radiol. 2008;(suppl 0):S10-S13.

9. Kotapka MJ, Kalia KK, Martinez AJ, Sekhar LN. Infiltration of the carotid artery by cavernous sinus meningioma. J Neurosurg. 1994;81:252-255.

Conflict of interest statement: The authors received no financial support or grants and declare no conflicts of interest. Received 3 October 2018; accepted 7 December 2018 Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2018.12.071 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.

WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.12.071