High incidence of ICA anterior wall aneurysms in patients with an anomalous origin of the ophthalmic artery: possible relevance to the pathogenesis of aneurysm formation

Clinical article

Masahiro Indo M.D. 1 , Soichi Oya M.D., Ph.D. 1 , Michihiro Tanaka M.D., Ph.D. 2 , and Toru Matsui M.D., D.M.Sc. 1
View More View Less
  • 1 Department of Neurosurgery, Saitama Medical Center, Saitama Medical University, Saitama; and
  • 2 Department of Neurosurgery, Kameda Medical Center, Chiba, Japan
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00
Print or Print + Online

Object

Surgery for aneurysms at the anterior wall of the internal carotid artery (ICA), which are also referred to as ICA anterior wall aneurysms, is often challenging. A treatment strategy needs to be determined according to the pathology of the aneurysm—namely, whether the aneurysm is a saccular aneurysm with firm neck walls that would tolerate clipping or coiling, a dissecting aneurysm, or a blood blister–like aneurysm. However, it is not always possible to properly evaluate the condition of the aneurysm before surgery solely based on angiographic findings.

Methods

The authors focused on the location of the ophthalmic artery (OA) in determining the pathology of ICA anterior wall aneurysms. Between January 2006 and December 2012, diagnostic cerebral angiography, for any reason, was performed on 1643 ICAs in 855 patients at Saitama Medical Center. The authors also investigated the relationship between the origin of the OA and the incidence of ICA anterior wall aneurysms. The pathogenesis was also evaluated for each aneurysm based on findings from both angiography and open surgery to identify any correlation between the location where the OA originated and the conditions of the aneurysm walls.

Results

Among 1643 ICAs, 31 arteries (1.89%) were accompanied by an anomalous origin of the OA, including 26 OAs originating from the C3 portion, 3 originating from the C4 portion, and 2 originating from the anterior cerebral artery. The incidence of an anomalous origin of the OA had no relationship to age, sex, or side. Internal carotid artery anterior wall aneurysms were observed in 16 (0.97%) of 1643 ICAs. Female patients had a significantly higher risk of having ICA anterior wall aneurysms (p = 0.026). The risk of ICA anterior wall aneurysm formation was approximately 50 times higher in patients with an anomalous origin of the OA (25.8% [8 of 31]) than in those with a normal OA (0.5% [8 of 1612], p < 0.0001). Based on angiographic classifications, saccular aneurysms were significantly more common in patients with an anomalous origin of the OA than in those with a normal OA (p = 0.041). Ten of 16 patients with ICA anterior wall aneurysms underwent craniotomies. Based on the intraoperative findings, all 6 aneurysms with normal OAs were dissecting or blood blister–like aneurysms, not saccular aneurysms.

Conclusions

There was a close relationship between the location of the OA origin and the predisposition to ICA anterior wall aneurysms. Developmental failure of the OA and subsequent weakness of the vessel wall might account for this phenomenon, as previously reported regarding other aneurysms related to the anomalous development of parent arteries. The data also appear to indicate that ICA anterior wall aneurysms in patients with an anomalous origin of the OA tend to be saccular aneurysms with normal neck walls. These findings provide critical information in determining therapeutic strategies for ICA anterior wall aneurysms.

Abbreviations used in this paper:BBA = blood blister–like aneurysm; ICA = internal carotid artery; OA = ophthalmic artery; PDOA = primitive dorsal OA; POA = primitive OA; PVOA = primitive ventral OA; SAH = subarachnoid hemorrhage; SOF = superior orbital fissure.

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00

Contributor Notes

Address correspondence to: Soichi Oya, M.D., Ph.D., Department of Neurosurgery, Saitama Medical Center, 1981 Kamoda, Kawagoe, Saitama 350-8550, Japan. email: sooya-tky@umin.ac.jp.

Please include this information when citing this paper: published online November 1, 2013; DOI: 10.3171/2013.9.JNS131030.

  • 1

    Abe M, , Tabuchi K, , Yokoyama H, & Uchino A: Blood blisterlike aneurysms of the internal carotid artery. J Neurosurg 89:419424, 1998

  • 2

    Banach MJ, & Flamm ES: Supraclinoid internal carotid artery fenestration with an associated aneurysm. Case report. J Neurosurg 79:438441, 1993

    • Search Google Scholar
    • Export Citation
  • 3

    Başkaya MK, , Ahmed AS, , Ateş O, & Niemann D: Surgical treatment of blood blister-like aneurysms of the supraclinoid internal carotid artery with extracranial-intracranial bypass and trapping. Neurosurg Focus 24:2 E13, 2008

    • Search Google Scholar
    • Export Citation
  • 4

    Black SP, & Ansbacher LE: Saccular aneurysm associated with segmental duplication of the basilar artery. A morphological study. J Neurosurg 61:10051008, 1984

    • Search Google Scholar
    • Export Citation
  • 5

    Charbel FT, , Gonzales-Portillo G, , Hoffman W, & Cochran E: Distal internal carotid artery pseudoaneurysms: technique and pitfalls of surgical management: two technical case reports. Neurosurgery 45:643649, 1999

    • Search Google Scholar
    • Export Citation
  • 6

    Ezaki Y, , Takahata H, , Kamada K, , Baba S, & Kaminogo M: Aneurysmal embolization of a blisterlike aneurysm of the internal carotid artery: a case report and review of the literature. Surg Neurol 65:628630, 2006

    • Search Google Scholar
    • Export Citation
  • 7

    Finlay HM, & Canham PB: The layered fabric of cerebral artery fenestrations. Stroke 25:17991806, 1994

  • 8

    Fukushima Y, , Miyasaka Y, , Takagi H, , Kurata A, , Suzuki S, & Fujii K: Successful coil embolization for a “three-hump” internal carotid artery anterior wall aneurysm: a case report. Interv Neuroradiol 12:345350, 2006

    • Search Google Scholar
    • Export Citation
  • 9

    Gailloud P, , Albayram S, , Fasel JHD, , Beauchamp NJ, & Murphy KJ: Angiographic and embryologic considerations in five cases of middle cerebral artery fenestration. AJNR Am J Neuroradiol 23:585587, 2002

    • Search Google Scholar
    • Export Citation
  • 10

    Gaughen JR Jr, , Raghavan P, , Jensen ME, , Hasan D, , Pfeffer AN, & Evans AJ: Utility of CT angiography in the identification and characterization of supraclinoid internal carotid artery blister aneurysms. AJNR Am J Neuroradiol 31:640644, 2010

    • Search Google Scholar
    • Export Citation
  • 11

    Hassler W, , Zentner J, & Voigt K: Abnormal origin of the ophthalmic artery from the anterior cerebral artery: neuroradiological and intraoperative findings. Neuroradiology 31:8587, 1989

    • Search Google Scholar
    • Export Citation
  • 12

    Hoffman WF, & Wilson CB: Fenestrated basilar artery with an associated saccular aneurysm. Case report. J Neurosurg 50:262264, 1979

  • 13

    Horie N, , Morikawa M, , Fukuda S, , Hayashi K, , Suyama K, & Nagata I: Detection of blood blister-like aneurysm and intramural hematoma with high-resolution magnetic resonance imaging. Case report. J Neurosurg 115:12061209, 2011

    • Search Google Scholar
    • Export Citation
  • 14

    Ishikawa T, , Nakamura N, , Houkin K, & Nomura M: Pathological consideration of a “blister-like” aneurysm at the superior wall of the internal carotid artery: case report. Neurosurgery 40:403406, 1997

    • Search Google Scholar
    • Export Citation
  • 15

    Joo SP, , Kim TS, , Moon KS, , Kwak HJ, , Lee JK, & Kim JH, : Arterial suturing followed by clip reinforcement with circumferential wrapping for blister-like aneurysms of the internal carotid artery. Surg Neurol 66:424429, 2006

    • Search Google Scholar
    • Export Citation
  • 16

    Kamijo K, & Matsui T: Acute extracranial-intracranial bypass using a radial artery graft along with trapping of a ruptured blood blister–like aneurysm of the internal carotid artery. Clinical article. J Neurosurg 113:781785, 2010

    • Search Google Scholar
    • Export Citation
  • 17

    Kim JH, , Kwon TH, , Kim JH, , Park YK, & Chung HS: Internal carotid artery dorsal wall aneurysm with configurational change: are they all false aneurysms?. Surg Neurol 66:441443, 2006

    • Search Google Scholar
    • Export Citation
  • 18

    Kinouchi H, , Mizoi K, , Nagamine Y, , Yanagida N, , Mikawa S, & Suzuki A, : Anterior paraclinoid aneurysms. J Neurosurg 96:10001005, 2002

  • 19

    Kubo Y, , Ogasawara K, , Tomitsuka N, , Otawara Y, , Watanabe M, & Ogawa A: Wrap-clipping with polytetrafluoroethylene for ruptured blisterlike aneurysms of the internal carotid artery. Technical note. J Neurosurg 105:785787, 2006

    • Search Google Scholar
    • Export Citation
  • 20

    Kurokawa Y, , Wanibuchi M, , Ishiguro M, & Inaba K: New method for obliterative treatment of an anterior wall aneurysm in the internal carotid artery: encircling silicone sheet clip procedure—technical case report. Neurosurgery 49:469472, 2001

    • Search Google Scholar
    • Export Citation
  • 21

    Lasjaunias P, , Berenstein A, & ter Brugge KG: Surgical Neuroangiography 1, Clinical Vascular Anatomy and Variations ed 2 Berlin, Springer-Verlag, 2001. 435455

    • Search Google Scholar
    • Export Citation
  • 22

    Lee BH, , Kim BM, , Park MS, , Park SI, , Chung EC, & Suh SH, : Reconstructive endovascular treatment of ruptured blood blister-like aneurysms of the internal carotid artery. Clinical article. J Neurosurg 110:431436, 2009

    • Search Google Scholar
    • Export Citation
  • 23

    Meling TR, , Sorteberg A, , Bakke SJ, , Slettebø H, , Hernesniemi J, & Sorteberg W: Blood blister-like aneurysms of the internal carotid artery trunk causing subarachnoid hemorrhage: treatment and outcome. J Neurosurg 108:662671, 2008

    • Search Google Scholar
    • Export Citation
  • 24

    Morita A, , Kirino T, , Hashi K, , Aoki N, , Fukuhara S, & Hashimoto N, : The natural course of unruptured cerebral aneurysms in a Japanese cohort. N Engl J Med 366:24742482, 2012

    • Search Google Scholar
    • Export Citation
  • 25

    Murai Y, , Mizunari T, , Umeoka K, , Tateyama K, , Kobayashi S, & Teramoto A: Ischemic complications after radial artery grafting and aneurysmal trapping for ruptured internal carotid artery anterior wall aneurysm. World Neurosurg 77:166171, 2012

    • Search Google Scholar
    • Export Citation
  • 26

    Nakagawa F, , Kobayashi S, , Takemae T, & Sugita K: Aneurysms protruding from the dorsal wall of the internal carotid artery. J Neurosurg 65:303308, 1986

    • Search Google Scholar
    • Export Citation
  • 27

    Nakatomi H, , Nagata K, , Kawamoto S, & Shiokawa Y: Ruptured dissecting aneurysm as a cause of subarachnoid hemorrhage of unverified etiology. Stroke 28:12781282, 1997

    • Search Google Scholar
    • Export Citation
  • 28

    Nishizaki T, , Ikeda N, , Kurokawa Y, , Okamura T, & Abiko S: Ruptured internal carotid artery anterior wall aneurysm identified during vasospasm: case report. Neurosurgery 57:E811, 2005

    • Search Google Scholar
    • Export Citation
  • 29

    Nutik S, & Dilenge D: Carotid-anterior cerebral artery anastomosis. Case report. J Neurosurg 44:378382, 1976

  • 30

    Nutik SL: Ventral paraclinoid carotid aneurysms. J Neurosurg 69:340344, 1988

  • 31

    Ogawa A, , Suzuki M, & Ogasawara K: Aneurysms at nonbranching sites in the surpaclinoid portion of the internal carotid artery: internal carotid artery trunk aneurysms. Neurosurgery 47:578586, 2000

    • Search Google Scholar
    • Export Citation
  • 32

    Ohkuma H, , Nakano T, , Manabe H, & Suzuki S: Subarachnoid hemorrhage caused by a dissecting aneurysm of the internal carotid artery. J Neurosurg 97:576583, 2002

    • Search Google Scholar
    • Export Citation
  • 33

    Padget DH: Development of the cranial arteries in the human embryo. Contrib Embryol 32:205262, 1948

  • 34

    Park JH, , Park IS, , Han DH, , Kim SH, , Oh CW, & Kim JE, : Endovascular treatment of blood blister-like aneurysms of the internal carotid artery. J Neurosurg 106:812819, 2007

    • Search Google Scholar
    • Export Citation
  • 35

    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 106:142150, 2007

    • Search Google Scholar
    • Export Citation
  • 36

    Rinkel GJE, , Djibuti M, , Algra A, & van Gijn J: Prevalence and risk of rupture of intracranial aneurysms: a systematic review. Stroke 29:251256, 1998

    • Search Google Scholar
    • Export Citation
  • 37

    Sade B, , Tampieri D, & Mohr G: Ophthalmic artery originating from basilar artery: a rare variant. AJNR Am J Neuroradiol 25:17301731, 2004

    • Search Google Scholar
    • Export Citation
  • 38

    Satoh A: Ruptured internal carotid artery dorsal wall aneurysm; its clinical features and treatment. Eur J Neurol 17:12251226, 2010

  • 39

    Satoh A, , Nakamura H, , Odaki M, , Kobayashi S, , Kageyama Y, & Fukuda K, : [High risk aneurysms of the internal carotid artery: dorsal IC aneurysms.]. Surg Cereb Stroke 21:467472, 1993. (Jpn)

    • Search Google Scholar
    • Export Citation
  • 40

    Satoh A, , Sugiyama T, , Hongo K, , Kakizawa Y, , Ishihara S, & Matsutani M: Nationwide surveillance of IC anterior (or dorsal) wall aneurysm: with special reference to its dissecting nature. Acta Neurochir Suppl 103:5155, 2008

    • Search Google Scholar
    • Export Citation
  • 41

    Shigeta H, , Kyoshima K, , Nakagawa F, & Kobayashi S: Dorsal internal carotid artery aneurysms with special reference to angiographic presentation and surgical management. Acta Neurochir (Wien) 119:4248, 1992

    • Search Google Scholar
    • Export Citation
  • 42

    Sim SY, , Shin YS, , Cho KG, , Kim SY, , Kim SH, & Ahn YH, : Blood blister-like aneurysms at nonbranching sites of the internal carotid artery. J Neurosurg 105:400405, 2006

    • Search Google Scholar
    • Export Citation
  • 43

    Tsuzuki N, , Katoh H, , Toyooka T, , Uozumi Y, & Shima K: Subarachnoid clot distribution in anterior wall saccular aneurysms of the internal carotid artery. J Clin Neurosci 14:242244, 2007

    • Search Google Scholar
    • Export Citation
  • 44

    Uchino A, , Saito N, , Takahashi M, , Kozawa E, , Mizukoshi W, & Nakajima R, : Persistent dorsal ophthalmic artery and ophthalmic artery arising from the middle meningeal artery diagnosed by MR angiography at 3 T. Surg Radiol Anat [epub ahead of print], 2013

    • Search Google Scholar
    • Export Citation
  • 45

    Wiebers DO, , Whisnant JP, , Huston J III, , Meissner I, , Brown RD Jr, & Piepgras DG, : Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet 362:103110, 2003

    • Search Google Scholar
    • Export Citation
  • 46

    Yaşargil MG, , Smith RD, , Young PH, & Teddy PJ: Microneurosurgery: Clinical Considerations, Surgery of the Intracranial Aneurysms and Results II:New York, Thieme-Stratton, 1984

    • Search Google Scholar
    • Export Citation
  • 47

    Yeon JY, , Hong SC, , Kim JS, , Kim KH, & Jeon P: Unruptured nonbranching site aneurysms located on the anterior (dorsal) wall of the supraclinoid internal carotid artery: aneurysmal characteristics and outcomes following endovascular treatment. Acta Neurochir (Wien) 154:21632171, 2012

    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 247 151 16
Full Text Views 536 32 1
PDF Downloads 327 33 2
EPUB Downloads 0 0 0