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Arterial fenestrations and their association with cerebral aneurysms
Journal of Clinical Neuroscience 21 (2014) 2184–2188
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Clinical Study
Arterial fenestrations and their association with cerebral aneurysms Mira A. Patel a, Justin M. Caplan a, Wuyang Yang a, Geoffrey P. Colby a,b,c, Alexander L. Coon a,b,c, Rafael J. Tamargo a,d, Judy Huang a,⇑ a
Department of Neurosurgery, Johns Hopkins University School of Medicine, 1800 Orleans Street, Zayed Tower 6115F, Johns Hopkins Hospital, Baltimore, MD 21287, USA Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD, USA c Department of Radiology and Radiological Science, Johns Hopkins University School of Medicine, Baltimore, MD, USA d Department of Otolaryngology-Head and Neck Surgery, Johns Hopkins University School of Medicine, Baltimore, MD, USA b
a r t i c l e
i n f o
Article history: Received 12 June 2014 Accepted 5 July 2014
Keywords: Aneurysm Cerebral Duplication Fenestration Subarachnoid hemorrhage
a b s t r a c t Fenestrations of intracranial arteries and associated aneurysms are rare. The significance of these fenestrations in relation to aneurysms remains unclear. We present four patients with fenestration-associated aneurysms and a comprehensive review of associations with aneurysms and other vascular lesions. A PubMed search of the literature was conducted from 1970–2012 reporting cases of intracranial aneurysms associated with arterial fenestration or duplications. Data were collected on patient presentation, sex, age, aneurysm and fenestration location, aneurysm treatment, and presence of other vascular lesions. We performed a retrospective review of four patients with intracranial fenestrations associated with aneurysms at our institution from 2012–2013. There were 59 cases of fenestrations and associated aneurysms in the literature. Aneurysms were reported as either arising from (n = 50) or adjacent to but distinct from (n = 13) fenestrations. The most common single fenestration location was at the basilar artery (n = 23, 36.5%); however the majority of fenestrations were in the carotid circulation (n = 34, 54.0%). The majority of patients with aneurysms and fenestrations at all locations except those at the anterior communicating artery (70.5%) presented with subarachnoid hemorrhage. Patients with aneurysms arising from a fenestration or adjacent to a fenestration presented with an additional intracranial vascular lesion in 38% and 31% of cases, respectively. The majority of all aneurysms were treated with microsurgical clipping. Aneurysms associated with cerebral arterial fenestrations are most commonly discovered after subarachnoid hemorrhage and are most often located in the carotid circulation. A high index of suspicion must be maintained for an associated vascular lesion if an intracranial fenestration is discovered. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction Fenestrations of intracranial arteries and their association with cerebral aneurysms are well-described and occur rarely [1–4]. Arterial fenestration is defined as a localized duplication of a vessel, with a divided arterial lumen including division of the endothelium and tunica media, and in some instances the adventitia [5,6]. Case-based reports have shown that the location of fenestrated arteries ranges from the anterior cerebral artery (ACA) to the vertebrobasilar system [7–9]. Hassler first described cerebral arterial fenestrations as ‘‘windows’’ within the internal elastic lamina, and subsequently was the first to report a saccular aneurysm associated with an arterial fenestration [10,11]. Fenestrations alone are benign and often incidentally found arterial variants [1]. While many have discussed the implications of fenestration
⇑ Corresponding author. Tel.: +1 410 502 5767; fax: +1 443 287 0683. E-mail address: [email protected] (J. Huang). http://dx.doi.org/10.1016/j.jocn.2014.07.005 0967-5868/Ó 2014 Elsevier Ltd. All rights reserved.
formation in particular anatomic sites, the significance of fenestrations with respect to risk of aneurysm formation and rupture remains unclear. It has been hypothesized that fenestrations are particularly predisposed to aneurysm formation because of defects in the tunica media as well as hemodynamic stress from increased turbulence at the proximal and distal edges [3,6,12–14]. We present four patients with divergent anatomical characteristics and clinical presentations and sought to conduct a comprehensive review of the literature on cerebral arterial fenestrations and associated aneurysms and other vascular anomalies.
2. Methods A PubMed search of the English literature was conducted for publications from 1970–2012 that described cases of intracranial arterial fenestration or duplication and associated aneurysms. Search terms queried included ‘‘fenestration,’’ ‘‘duplication,’’ ‘‘aneurysm,’’ ‘‘intracranial,’’ and ‘‘cerebral.’’ All case reports that described
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a cerebral arterial fenestration and associated aneurysm were included in the analysis. We only included reports if both a fenestration and aneurysm were described; we excluded reports of fenestrations without an associated aneurysm. Data were collected from published cases on patient presentation, sex, and age, aneurysm and fenestration anatomic location, aneurysm treatment, and other vascular anomalies if present. We also performed a retrospective medical record review of four patients with intracranial fenestrations associated with aneurysms at our institution from 2012–2013. All values were calculated based on available data. 3. Case reports 3.1. Patient 1 A 44-year-old woman with a 25 pack-year history of smoking presented to the emergency room complaining of headache for 4 weeks. Non-contrast head CT scan showed no evidence of subarachnoid hemorrhage (SAH). A CT angiogram was performed which revealed an aneurysm; thus, diagnostic cerebral angiography was performed which revealed a 10.0 7.0 7.0 mm paraophthalmic aneurysm projecting superiorly from the left supraclinoid internal carotid artery (ICA) as well as a 1.9 mm inferomedially projecting anterior communicating artery (ACommA) aneurysm (Fig. 1A, B). Microsurgical clipping for both aneurysms was performed via left pterional craniotomy with neck dissection. After clipping of the paraophthalmic aneurysm, examination of the anterior communicating complex revealed three distinct A2 segments with the thin-walled ACommA aneurysm arising between the left A2 segment and middle A2. The middle and left A2 segments became fused distal to the aneurysm to form a single large vessel. A fenestrated clip was placed across the neck of the small ACommA aneurysm with the ring encircling the middle proximal A2 segment and the blades across the superiorly projecting aneurysm. Intraoperative angiogram confirmed obliteration of both aneurysms. 3.2. Patient 2 A 55-year-old man with diabetes, hypertension, and cigarette smoking presented to the emergency room at an outside hospital with 24 hours of severe headache, vomiting and increasing confusion. He was transferred to our institution with a Glasgow Coma Scale score of 13 and Hunt and Hess grade III SAH with minimal intraventricular hemorrhage and hydrocephalus. Due to increasing somnolence he was intubated and a ventriculostomy was placed. A diagnostic cerebral angiogram revealed a 5 mm ACommA aneurysm arising from a fenestrated anterior communicating artery as well as a 2 mm aneurysm arising from the larger of the two fenestrations (Fig. 1C, D). A right pterional craniotomy for microsurgical clipping of the aneurysms was performed. Two fenestrated clips were placed across the neck of the larger aneurysm with the fenestration encircling the right A1, while one fenestrated clip was placed across the neck of the smaller aneurysm with the fenestration encircling the ipsilateral A2, which was observed to be the source of the SAH. Intraoperative cerebral angiography revealed complete obliteration of both aneurysms. The patient’s postoperative course was complicated by diabetes insipidus and he continues to have cognitive impairment and personality changes 1 year following his SAH.
Fig. 1. Three-dimensional reconstructions demonstrating arterial fenestrations and associated aneurysms. (A, B) Patient 1: Anterior communicating artery aneurysm at fenestrated anterior communicating arteries. (C, D) Patient 2: One anterior communicating artery aneurysm at each of the fenestrated anterior communicating arteries. (E, F) Patient 3: Aneurysm at fenestrated middle cerebral artery (MCA). (G, H) Patient 4: Two mid-basilar aneurysms at fenestrated basilar artery (BA). Thick white arrows depict the site of fenestrated arteries, and thin white arrows depict aneurysms. ICA = internal carotid artery.
The workup included cerebral angiography, which revealed a fenestration of the right middle cerebral artery (MCA) M1 segment and an associated aneurysm measuring 2.3 2.4 2.2 mm that projected superiorly at the proximal origin of the fenestration (Fig. 1E, F). No treatment was recommended for this incidentally found, unruptured aneurysm, and the patient is being monitored annually with magnetic resonance angiography (MRA). 3.4. Patient 4
3.3. Patient 3 An 18-year-old woman with a family history of cerebral aneurysms presented for outpatient evaluation with severe headache.
A 67-year-old man with hypertension, hyperlipidemia, stroke and cigarette smoking presented for outpatient evaluation with a 4 year history of sporadic facial twitching. MRA revealed an
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aneurysm, and subsequent diagnostic cerebral angiography revealed a mid-basilar fenestration and two aneurysms at the level of the fenestration (Fig. 1G, H). One aneurysm projected from the anterior surface and measured 3.7 3.9 4.1 mm, the second aneurysm projected posteriorly and measured 2.8 2.8 2.6 mm. No treatment was recommended for these incidentally discovered aneurysms and the patient was advised to quit smoking and receives annual MRA for monitoring. 4. Results We identified a total of 59 cases in the literature meeting the inclusion criteria in addition to our four patients [5,6,8,15–55]. Overall, aneurysms associated with arterial fenestrations were divided into two categories: (1) aneurysms arising from fenestration and (2) aneurysms located adjacent to fenestrations. There were 50 cases of aneurysms located at cerebral arterial fenestrations and 13 adjacent to fenestrations. The majority of all cases presented with SAH (70.5%).
Fig. 2. Frequency of fenestrations by arterial location. ACA = anterior cerebral artery, ACommA = anterior communicating artery, BA = basilar artery, ICA = internal carotid artery, MCA = middle cerebral artery, PCA = posterior cerebral artery, VA = vertebral artery.
4.1. Fenestrations with aneurysms 4.2. Fenestrations associated with separate aneurysms The average age of presentation was 44.5 years (standard deviation 14.5 years). The majority of patients were male (56.0%) (Table 1). Of the 50 cases of fenestrations from which aneurysms arose, the majority were located in the anterior circulation (52.0%), with 44% at the basilar artery (BA), 22% at the MCA, 14% at the ICA, 10% at the ACA, 6% at the ACommA, 2% at the posterior cerebral artery and 2% at the vertebral artery (VA) (Table 1, Fig. 2). In addition, the prevalence of other concurrent cerebrovascular lesions, in addition to the associated aneurysm, was highest in patients with aneurysms arising from ACA fenestrations (80%) (Table 1). Fenestrations of the BA with associated aneurysms had notably higher rates of rupture (90.0%) (Table 1). For two cases of aneurysms at BA fenestrations, rupture status was unknown. Of those aneurysms arising from fenestrations presenting with SAH, 48.5% were Hunt and Hess Grade IV–V (Table1) [56]. The most common treatment in patients with aneurysms arising from fenestrations was microsurgical clipping (68.0%) (Table 1). Other treatments included no surgical treatment because of death or disappearance of aneurysm, and ligation via Silverstone clamp.
We identified 13 cases of aneurysms adjacent to but distinct from fenestrations. Patients with fenestrations located at the BA and VA presented in the fifth decade of life, whereas patients with fenestrations of the ACA and ICA presented in the sixth and fourth decade, respectively (Table 2). The majority of patients with aneurysms distinct from fenestrations were males (53.8%) (Table 2). Fenestrations associated with distinct aneurysms were limited to the ACA (38.5%), ICA (23.1%), BA (7.7%) and VA (30.8%) (Table 2, Fig. 2). Similar to the presentation of patients with aneurysms arising directly from fenestrated arteries, the majority of patients with distinct aneurysms from a fenestration presented with SAH (76.9%); 30% were Hunt and Hess Grade IV–V (Table 2). Of the five ACA fenestrations, four had aneurysms located at the ACommA. Other cases of fenestrations with distinct aneurysms displayed no particular pattern in aneurysm location. Microsurgical clipping was the most common treatment modality (46.2%) (Table 2). Other management strategies included no surgical treatment because of patient death.
Table 1 Characteristics of patients with aneurysms arising from fenestrations Location of fenestration
ACA
N 5 Age, years, mean ± SD 49.4 ± 13.3 Aneurysm size, mm, mean ± SD Unruptured – Ruptured 5.0 ± 0 Unruptured 1 (20.0) SAH 4 (80.0) a Poor grade 2 (50.0) Female 0 (0) b Other lesions 4 (80.0) Treatment Clipping 5 (100.0) Wrapping 0 (0) Endovascular 0 (0) Other 0 (0) c Combined 0 (0)
2 1 0 2 0 3 0 0 0 0
ACommA
MCA
ICA
PCA
BA
VA
3 50.3 ± 5.7
11 46.5 ± 17.5
7 41.0 ± 7.4
1 11.0 ± 0
22 44.8 ± 14.7
1 35.0 ± 0
1.9 ± 0 5.0 ± 0 (66.7) (33.3) (0) (66.7) (0) (100.0) (0) (0) (0) (0)
5 6 3 5 5 10 0 0 1 0
2.4 ± 0 – (45.4) (54.5) (50.0) (45.4) (45.4) (90.9) (0) (0) (9.1) (0)
5 2 0 5 3
5.0 ± 2.5 3.0 ± 0 (71.4) (28.6) (0) (71.4) (42.9)
0 1 0 0 0
– – (0) (100.0) (0) (0) (0)
3 1 1 0 2
(42.9) (14.3) (14.3) (0) (28.6)
0 0 1 0 0
(0) (0) (100.0) (0) (0)
3.4 ± 0.8 6.6 ± 3.0 2 (10.0) 18 (90.0) 10 (55.6) 10 (45.4) 7 (31.8)
0 1 1 0 0
– – (0) (100.0) (100.0) (0) (0)
13 1 6 2 0
0 0 1 0 0
(0) (0) (100.0) (0) (0)
(59.1) (4.5) (27.2) (9.1) (0)
Values presented as frequencies with percentage in parenthesis unless otherwise indicated. a Hunt and Hess Grade IV–V. b Presence of additional intracranial vascular anomalies. c Combined modalities used. ACA = anterior cerebral artery, ACommA = anterior communicating artery, BA = basilar artery, ICA = internal carotid artery, MCA = middle cerebral artery, PCA = posterior cerebral artery, SAH = subarachnoid hemorrhage, SD = standard deviation, VA = vertebral artery, – = no data.
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M.A. Patel et al. / Journal of Clinical Neuroscience 21 (2014) 2184–2188 Table 2 Characteristics of patients with aneurysms adjacent to but distinct from fenestrations Location of fenestration N Age, years, mean ± SD Aneurysm size, mm, mean ± SD Unruptured Ruptured Unruptured SAH Poor grade a Female Other lesions b Treatment Clipping Wrapping Endovascular Other c Combined
ACA
ICA
BA
VA
5 58.8 ± 5.4
3 37.3 ± 9.0
1 46.0 ± 0
4 49.5 ± 21.4
– 25.0 ± 0
– –
9.2 ± 0 –
40.0 ± 0 –
1 4 2 0 1
(20.0) (80.0) (50.0) (0) (20.0)
0 3 1 3 1
(0) (100.0) (33.3) (100.0) (33.3)
1 0 0 1 1
(100.0) (0) (0) (100.0) (100.0)
1 3 0 2 1
(25.0) (75.0) (0) (50.0) (25.0)
3 0 0 2 0
(60.0) (0) (0) (40.0) (0)
1 1 0 1 0
(33.3) (33.3) (0) (33.3) (0)
0 0 0 1 0
0 0 0 (100.0) (0)
2 0 0 1 1
(50.0) (0) (0) (25.0) (25.0)
Values presented as frequencies with percentage in parenthesis unless otherwise indicated. a Hunt and Hess Grade IV–V. b Presence of additional intracranial vascular anomalies. c Combined modalities used. ACA = anterior cerebral artery, BA = basilar artery, ICA = internal carotid artery, SAH = subarachnoid hemorrhage, SD = standard deviation, VA = vertebral artery, – = no data.
4.3. Associated intracranial vascular lesions Additional cerebrovascular lesions were associated with 38% of fenestrations with aneurysms arising from the fenestration, and 31% of fenestrations associated with aneurysms distinct from the fenestration (Tables 1 and 2). Such malformations included persistent primitive hypoglossal artery, P2 segment of fetal origin, anterior inferior cerebellar artery origin displaced to the posterior inferior cerebellar artery–VA junction, hypoplastic VA, azygous ACA, dolichoectatic BA, VA originating from the aorta, VA duplication, bilateral accessory MCA, hypoplastic A1 segment, premoyamoya like changes, and additional fenestrations [6,12,16,17, 23,34–40,45,48–51].
5. Discussion We present our review of the literature of aneurysms associated with arterial fenestrations in addition to presenting four additional patients. The most common presentation of cerebral aneurysms associated with fenestrated arteries is SAH. Furthermore, the aneurysms associated with fenestrations of the carotid system are most likely to present with SAH. Recognition of these findings may be useful as the majority of patients with fenestration-associated aneurysms present with SAH, and preoperative angiographic identification of fenestrations may be difficult [6,8]. Thus, when a fenestration is incidentally discovered on imaging or intraoperatively, it is important that the surgeon accurately rule out the presence of an associated aneurysm. Moreover, even if a fenestration is not observed on imaging, seemingly anomalous duplicated vasculature found near an aneurysm intraoperatively should raise suspicion for a fenestrated artery and should be explored further to rule out an occult aneurysm. The literature varies regarding the angiographic post mortem incidence of fenestrations. The angiographic incidence of all fenestrations has been reported to be 0.3–0.9%, whereas autopsy studies show the incidence of ACommA fenestrations to be 7.5–40%, BA fenestrations 1–5%, and VA fenestrations to be 1–2% [19,51]. The higher sensitivity of post mortem analysis and the under-reporting of fenestrations on angiography can explain such discrepancies, as fenestrations are often asymptomatic unless accompanied by a symptomatic aneurysm [6]. Several authors have hypothesized that cerebral fenestrations are predisposed to aneurysm formation because of collagen defects
in the tunica media that weaken the arterial wall at the distal and proximal edges of the fenestration [3,12–14]. Moreover, animal models of aneurysm formation show that defects in elastin composition of the tunica media combined with a pro-inflammatory state that further damages an already weakened vascular wall predisposes to aneurysms [59]. In accordance with our findings, others have observed that patients most often present with fenestrations associated with the VA and BA [19]. Through morphologic analysis of the BA, Black and Ansbacher have shown thinning, and even absence, of the tunica media starting 200 lm proximal to the medial and ventral walls of the fenestration and its associated aneurysm, and again at the opposite end of the fenestration where the branches have reunited [12]. Alfano and colleagues have reported that vascular bifurcations with high wall shear stress and accelerated, turbulent flow are especially prone to intracranial aneurysm formation [57]. In fact, studies show that turbulence at the bifurcations of fenestrations produces hemodynamic stress that can predispose the vessel to aneurysms [3,12,14]. In an autopsy study Campos et al. report 35.5% of cases were fenestrated BA, and they explain that the turbulent flow at the vertebrobasilar junction paired with congenital medial defects may explain the high incidence of aneurysms at fenestrated BA [3]. Nevertheless, some have argued that fenestration-associated aneurysms are incidental, and that the incidence of fenestration-related aneurysm is the same as the overall population [2,58]. Our review revealed 13 cases of aneurysms adjacent to fenestrations and 23 cases with concurrent cerebral vascular anomalies in addition to the fenestration and associated aneurysm [8,15,19,20,26,36–42,47,50–53]. Fenestrations themselves arise from the incomplete or absent fusion or division of venous plexuses or primitive neural arteries [6,19]. It is possible that in an environment predisposed to congenital vascular anomaly, other vascular malformations may have the propensity to arise [19]. Whether or not such an association exists remains an avenue for future study.
6. Conclusion We conducted a comprehensive review of the literature on cerebral arterial fenestrations and associated aneurysms and other vascular anomalies. In addition, we present our experience with four additional patients. This review underscores the need for recognizing cerebral arterial fenestration-associated aneurysms and
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their propensity toward rupture. Strong support for the embryologic predisposition of aneurysm formation at fenestrations exists, and further inquiry into the association of arterial fenestration with other cerebrovascular anomalies will be useful. Conflicts of Interest/Disclosures Geoffrey Colby and Alexander Coon receive funding from and/or are associated with Covidien (Dublin, Ireland). The other authors declare that they have no financial or other conflicts of interest in relation to this research and its publication. References [1] Osborn RE, Kirk G. Cerebral arterial fenestration. Comput Radiol 1987;11:141–5. [2] Sanders W, Sorek P, Mehta B. Fenestration of intracranial arteries with special attention to associated aneurysms and other anomalies. AJNR Am J Neuroradiol 1993;14:675–80. [3] Campos J, Fox A, Viñuela F, et al. Saccular aneurysms in basilar artery fenestration. Am J Neuroradiol 1987;8:233–6. [4] de Gast AN, van Rooij WJ, Sluzewski M. Fenestrations of the anterior communicating artery: incidence on 3D angiography and relationship to aneurysms. Am J Neuroradiol 2008;29:296–8. [5] Cademartiri F, Stojanov D, Dippel DWJ, et al. Noninvasive detection of a ruptured aneurysm at a basilar artery fenestration with submillimeter multisection CT angiography. Am J Neuroradiol 2003;24:2009–10. [6] Hacein-Bey L, Muszynski CA, Varelas PN. Saccular aneurysm associated with posterior cerebral artery fenestration manifesting as a subarachnoid hemorrhage in a child. Am J Neuroradiol 2002;23:1291–4. [7] Teal JS, Rumbaugh CL, Bergeron RT, et al. Angiographic demonstration of fenestrations of the intradural intracranial arteries. Radiology 1973;106:123–6. [8] San-Galli F, Leman C, Kien P, et al. Cerebral arterial fenestrations associated with intracranial saccular aneurysms. Neurosurgery 1992;30:279–83. [9] Sun ZK, Li M, Li MH, et al. Fenestrations accompanied by intracranial aneurysms assessed with magnetic resonance angiography. Neurol India 2012;60:45–9. [10] Hassler O. The windows of the internal elastic lamella of the cerebral arteries. Virchows Arch Pathol Anat Physiol Klin Med 1962;335:127–32. [11] Hassler O. Scanning electron microscopy of saccular intracranial aneurysms. Am J Pathol 1972;68:511–20. [12] Black SP, Ansbacher LE. Saccular aneurysm associated with segmental duplication of the basilar artery. J Neurosurg 1984;61:1005–8. [13] De Caro R, Serafini M, Galli S, et al. Anatomy of segmental duplication in the human basilar artery. Possible site of aneurysm formation. Clin Neuropathol 1995;14:303–9. [14] Finlay HM, Canham PB. The layered fabric of cerebral artery fenestrations. Stroke 1994;25:1799–806. [15] Hori E, Kurosaki K, Matsumura N, et al. Multiple aneurysms arising from the origin of a duplication of the middle cerebral artery. J Clin Neurosci 2005;12:812–5. [16] Imaizumi S, Onuma T, Motohashi O, et al. Unruptured carotid-duplicated middle cerebral artery aneurysm: case report. Surg Neurol 2002;58:322–4. [17] In S, In K, Kusano N, et al. A case of duplication of the middle cerebral artery with ruptured aneurysm on its origin during pregnancy (author’s transl). No Shinkei Geka 1981;9:337–41. [18] Takano S, Nose T, Oowada T, et al. Aneurysm arising from duplicated middle cerebral artery: case report. Neurol Med Chir (Tokyo) 1988;28:910–4. [19] Chen Y, Chang F, Hu H, Chao A. Fenestration of the supraclinoid internal carotid artery associated with aneurysm and ischemic stroke. Surg Neurol 2007;68:S60–3 [discussion S63]. [20] Findlay JM, Chui M, Muller PJ. Fenestration of the supraclinoid internal carotid artery. Can J Neurol Sci 1987;14:159–61. [21] Hattori T, Kobayashi H. Fenestration of the supraclinoid internal carotid artery associated with carotid bifurcation aneurysm. Surg Neurol 1992;37:284–8. [22] Ichikawa T, Miyachi S, Izumi T, et al. Fenestration of a supraclinoid internal carotid artery associated with dual aneurysms: case report. Neurosurgery 2011;69:E1005–9 [discussion E1009]. [23] Katsuta T, Matsubara T, Fujii K. Fenestration of the supraclinoid internal carotid artery. Neuroradiology 1993;35:461. [24] Ng PP, Steinfort B, Stoodley MA. Internal carotid artery fenestration with dual aneurysms. J Neurosurg 2006;104:979. [25] Onoda K, Ono S, Tokunaga K, et al. Fenestration of the supraclinoid internal carotid artery with associated aneurysm-case report. Neurol Med 2008;48:118–20. [26] Taylor R, Connolly ES Jr, Duong H. Radiographic evidence and surgical confirmation of a saccular aneurysm on a hypoplastic duplicated A1 segment of the anterior cerebral artery: case report. Neurosurgery 2000;46:482–4. [27] Miyazaki S, Kamata K, Yamaura A. Multiple aneurysms of the vertebrobasilar system associated with fenestration of the vertebral artery. Surg Neurol 1981;15:192–5.
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[56] Hunt WE, Hess RM. Surgical risk as related to the time of intervention in the repair of intracranial aneurysms. J Neurosurg 1968;28:14–20. [57] Alfano JM, Kolega J, Natarajan SK, et al. Intracranial aneurysms occur more frequently at bifurcation sites that typically experience higher hemodynamic stresses. Neurosurgery 2013;73:497–505. [58] Tanaka M, Matsumoto S. Fenestration of the internal carotid artery (author’s transl). Neurol Med Chir (Tokyo) 1982;22:291–4. [59] Ruzevick J, Jackson C, Pradilla G, et al. Aneurysm formation in proinflammatory, transgenic haptoglobin 2–2 mice. Neurosurgery 2013;72:70–6 [discussion 76].
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Clinical Study
Arterial fenestrations and their association with cerebral aneurysms Mira A. Patel a, Justin M. Caplan a, Wuyang Yang a, Geoffrey P. Colby a,b,c, Alexander L. Coon a,b,c, Rafael J. Tamargo a,d, Judy Huang a,⇑ a
Department of Neurosurgery, Johns Hopkins University School of Medicine, 1800 Orleans Street, Zayed Tower 6115F, Johns Hopkins Hospital, Baltimore, MD 21287, USA Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD, USA c Department of Radiology and Radiological Science, Johns Hopkins University School of Medicine, Baltimore, MD, USA d Department of Otolaryngology-Head and Neck Surgery, Johns Hopkins University School of Medicine, Baltimore, MD, USA b
a r t i c l e
i n f o
Article history: Received 12 June 2014 Accepted 5 July 2014
Keywords: Aneurysm Cerebral Duplication Fenestration Subarachnoid hemorrhage
a b s t r a c t Fenestrations of intracranial arteries and associated aneurysms are rare. The significance of these fenestrations in relation to aneurysms remains unclear. We present four patients with fenestration-associated aneurysms and a comprehensive review of associations with aneurysms and other vascular lesions. A PubMed search of the literature was conducted from 1970–2012 reporting cases of intracranial aneurysms associated with arterial fenestration or duplications. Data were collected on patient presentation, sex, age, aneurysm and fenestration location, aneurysm treatment, and presence of other vascular lesions. We performed a retrospective review of four patients with intracranial fenestrations associated with aneurysms at our institution from 2012–2013. There were 59 cases of fenestrations and associated aneurysms in the literature. Aneurysms were reported as either arising from (n = 50) or adjacent to but distinct from (n = 13) fenestrations. The most common single fenestration location was at the basilar artery (n = 23, 36.5%); however the majority of fenestrations were in the carotid circulation (n = 34, 54.0%). The majority of patients with aneurysms and fenestrations at all locations except those at the anterior communicating artery (70.5%) presented with subarachnoid hemorrhage. Patients with aneurysms arising from a fenestration or adjacent to a fenestration presented with an additional intracranial vascular lesion in 38% and 31% of cases, respectively. The majority of all aneurysms were treated with microsurgical clipping. Aneurysms associated with cerebral arterial fenestrations are most commonly discovered after subarachnoid hemorrhage and are most often located in the carotid circulation. A high index of suspicion must be maintained for an associated vascular lesion if an intracranial fenestration is discovered. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction Fenestrations of intracranial arteries and their association with cerebral aneurysms are well-described and occur rarely [1–4]. Arterial fenestration is defined as a localized duplication of a vessel, with a divided arterial lumen including division of the endothelium and tunica media, and in some instances the adventitia [5,6]. Case-based reports have shown that the location of fenestrated arteries ranges from the anterior cerebral artery (ACA) to the vertebrobasilar system [7–9]. Hassler first described cerebral arterial fenestrations as ‘‘windows’’ within the internal elastic lamina, and subsequently was the first to report a saccular aneurysm associated with an arterial fenestration [10,11]. Fenestrations alone are benign and often incidentally found arterial variants [1]. While many have discussed the implications of fenestration
⇑ Corresponding author. Tel.: +1 410 502 5767; fax: +1 443 287 0683. E-mail address: [email protected] (J. Huang). http://dx.doi.org/10.1016/j.jocn.2014.07.005 0967-5868/Ó 2014 Elsevier Ltd. All rights reserved.
formation in particular anatomic sites, the significance of fenestrations with respect to risk of aneurysm formation and rupture remains unclear. It has been hypothesized that fenestrations are particularly predisposed to aneurysm formation because of defects in the tunica media as well as hemodynamic stress from increased turbulence at the proximal and distal edges [3,6,12–14]. We present four patients with divergent anatomical characteristics and clinical presentations and sought to conduct a comprehensive review of the literature on cerebral arterial fenestrations and associated aneurysms and other vascular anomalies.
2. Methods A PubMed search of the English literature was conducted for publications from 1970–2012 that described cases of intracranial arterial fenestration or duplication and associated aneurysms. Search terms queried included ‘‘fenestration,’’ ‘‘duplication,’’ ‘‘aneurysm,’’ ‘‘intracranial,’’ and ‘‘cerebral.’’ All case reports that described
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a cerebral arterial fenestration and associated aneurysm were included in the analysis. We only included reports if both a fenestration and aneurysm were described; we excluded reports of fenestrations without an associated aneurysm. Data were collected from published cases on patient presentation, sex, and age, aneurysm and fenestration anatomic location, aneurysm treatment, and other vascular anomalies if present. We also performed a retrospective medical record review of four patients with intracranial fenestrations associated with aneurysms at our institution from 2012–2013. All values were calculated based on available data. 3. Case reports 3.1. Patient 1 A 44-year-old woman with a 25 pack-year history of smoking presented to the emergency room complaining of headache for 4 weeks. Non-contrast head CT scan showed no evidence of subarachnoid hemorrhage (SAH). A CT angiogram was performed which revealed an aneurysm; thus, diagnostic cerebral angiography was performed which revealed a 10.0 7.0 7.0 mm paraophthalmic aneurysm projecting superiorly from the left supraclinoid internal carotid artery (ICA) as well as a 1.9 mm inferomedially projecting anterior communicating artery (ACommA) aneurysm (Fig. 1A, B). Microsurgical clipping for both aneurysms was performed via left pterional craniotomy with neck dissection. After clipping of the paraophthalmic aneurysm, examination of the anterior communicating complex revealed three distinct A2 segments with the thin-walled ACommA aneurysm arising between the left A2 segment and middle A2. The middle and left A2 segments became fused distal to the aneurysm to form a single large vessel. A fenestrated clip was placed across the neck of the small ACommA aneurysm with the ring encircling the middle proximal A2 segment and the blades across the superiorly projecting aneurysm. Intraoperative angiogram confirmed obliteration of both aneurysms. 3.2. Patient 2 A 55-year-old man with diabetes, hypertension, and cigarette smoking presented to the emergency room at an outside hospital with 24 hours of severe headache, vomiting and increasing confusion. He was transferred to our institution with a Glasgow Coma Scale score of 13 and Hunt and Hess grade III SAH with minimal intraventricular hemorrhage and hydrocephalus. Due to increasing somnolence he was intubated and a ventriculostomy was placed. A diagnostic cerebral angiogram revealed a 5 mm ACommA aneurysm arising from a fenestrated anterior communicating artery as well as a 2 mm aneurysm arising from the larger of the two fenestrations (Fig. 1C, D). A right pterional craniotomy for microsurgical clipping of the aneurysms was performed. Two fenestrated clips were placed across the neck of the larger aneurysm with the fenestration encircling the right A1, while one fenestrated clip was placed across the neck of the smaller aneurysm with the fenestration encircling the ipsilateral A2, which was observed to be the source of the SAH. Intraoperative cerebral angiography revealed complete obliteration of both aneurysms. The patient’s postoperative course was complicated by diabetes insipidus and he continues to have cognitive impairment and personality changes 1 year following his SAH.
Fig. 1. Three-dimensional reconstructions demonstrating arterial fenestrations and associated aneurysms. (A, B) Patient 1: Anterior communicating artery aneurysm at fenestrated anterior communicating arteries. (C, D) Patient 2: One anterior communicating artery aneurysm at each of the fenestrated anterior communicating arteries. (E, F) Patient 3: Aneurysm at fenestrated middle cerebral artery (MCA). (G, H) Patient 4: Two mid-basilar aneurysms at fenestrated basilar artery (BA). Thick white arrows depict the site of fenestrated arteries, and thin white arrows depict aneurysms. ICA = internal carotid artery.
The workup included cerebral angiography, which revealed a fenestration of the right middle cerebral artery (MCA) M1 segment and an associated aneurysm measuring 2.3 2.4 2.2 mm that projected superiorly at the proximal origin of the fenestration (Fig. 1E, F). No treatment was recommended for this incidentally found, unruptured aneurysm, and the patient is being monitored annually with magnetic resonance angiography (MRA). 3.4. Patient 4
3.3. Patient 3 An 18-year-old woman with a family history of cerebral aneurysms presented for outpatient evaluation with severe headache.
A 67-year-old man with hypertension, hyperlipidemia, stroke and cigarette smoking presented for outpatient evaluation with a 4 year history of sporadic facial twitching. MRA revealed an
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aneurysm, and subsequent diagnostic cerebral angiography revealed a mid-basilar fenestration and two aneurysms at the level of the fenestration (Fig. 1G, H). One aneurysm projected from the anterior surface and measured 3.7 3.9 4.1 mm, the second aneurysm projected posteriorly and measured 2.8 2.8 2.6 mm. No treatment was recommended for these incidentally discovered aneurysms and the patient was advised to quit smoking and receives annual MRA for monitoring. 4. Results We identified a total of 59 cases in the literature meeting the inclusion criteria in addition to our four patients [5,6,8,15–55]. Overall, aneurysms associated with arterial fenestrations were divided into two categories: (1) aneurysms arising from fenestration and (2) aneurysms located adjacent to fenestrations. There were 50 cases of aneurysms located at cerebral arterial fenestrations and 13 adjacent to fenestrations. The majority of all cases presented with SAH (70.5%).
Fig. 2. Frequency of fenestrations by arterial location. ACA = anterior cerebral artery, ACommA = anterior communicating artery, BA = basilar artery, ICA = internal carotid artery, MCA = middle cerebral artery, PCA = posterior cerebral artery, VA = vertebral artery.
4.1. Fenestrations with aneurysms 4.2. Fenestrations associated with separate aneurysms The average age of presentation was 44.5 years (standard deviation 14.5 years). The majority of patients were male (56.0%) (Table 1). Of the 50 cases of fenestrations from which aneurysms arose, the majority were located in the anterior circulation (52.0%), with 44% at the basilar artery (BA), 22% at the MCA, 14% at the ICA, 10% at the ACA, 6% at the ACommA, 2% at the posterior cerebral artery and 2% at the vertebral artery (VA) (Table 1, Fig. 2). In addition, the prevalence of other concurrent cerebrovascular lesions, in addition to the associated aneurysm, was highest in patients with aneurysms arising from ACA fenestrations (80%) (Table 1). Fenestrations of the BA with associated aneurysms had notably higher rates of rupture (90.0%) (Table 1). For two cases of aneurysms at BA fenestrations, rupture status was unknown. Of those aneurysms arising from fenestrations presenting with SAH, 48.5% were Hunt and Hess Grade IV–V (Table1) [56]. The most common treatment in patients with aneurysms arising from fenestrations was microsurgical clipping (68.0%) (Table 1). Other treatments included no surgical treatment because of death or disappearance of aneurysm, and ligation via Silverstone clamp.
We identified 13 cases of aneurysms adjacent to but distinct from fenestrations. Patients with fenestrations located at the BA and VA presented in the fifth decade of life, whereas patients with fenestrations of the ACA and ICA presented in the sixth and fourth decade, respectively (Table 2). The majority of patients with aneurysms distinct from fenestrations were males (53.8%) (Table 2). Fenestrations associated with distinct aneurysms were limited to the ACA (38.5%), ICA (23.1%), BA (7.7%) and VA (30.8%) (Table 2, Fig. 2). Similar to the presentation of patients with aneurysms arising directly from fenestrated arteries, the majority of patients with distinct aneurysms from a fenestration presented with SAH (76.9%); 30% were Hunt and Hess Grade IV–V (Table 2). Of the five ACA fenestrations, four had aneurysms located at the ACommA. Other cases of fenestrations with distinct aneurysms displayed no particular pattern in aneurysm location. Microsurgical clipping was the most common treatment modality (46.2%) (Table 2). Other management strategies included no surgical treatment because of patient death.
Table 1 Characteristics of patients with aneurysms arising from fenestrations Location of fenestration
ACA
N 5 Age, years, mean ± SD 49.4 ± 13.3 Aneurysm size, mm, mean ± SD Unruptured – Ruptured 5.0 ± 0 Unruptured 1 (20.0) SAH 4 (80.0) a Poor grade 2 (50.0) Female 0 (0) b Other lesions 4 (80.0) Treatment Clipping 5 (100.0) Wrapping 0 (0) Endovascular 0 (0) Other 0 (0) c Combined 0 (0)
2 1 0 2 0 3 0 0 0 0
ACommA
MCA
ICA
PCA
BA
VA
3 50.3 ± 5.7
11 46.5 ± 17.5
7 41.0 ± 7.4
1 11.0 ± 0
22 44.8 ± 14.7
1 35.0 ± 0
1.9 ± 0 5.0 ± 0 (66.7) (33.3) (0) (66.7) (0) (100.0) (0) (0) (0) (0)
5 6 3 5 5 10 0 0 1 0
2.4 ± 0 – (45.4) (54.5) (50.0) (45.4) (45.4) (90.9) (0) (0) (9.1) (0)
5 2 0 5 3
5.0 ± 2.5 3.0 ± 0 (71.4) (28.6) (0) (71.4) (42.9)
0 1 0 0 0
– – (0) (100.0) (0) (0) (0)
3 1 1 0 2
(42.9) (14.3) (14.3) (0) (28.6)
0 0 1 0 0
(0) (0) (100.0) (0) (0)
3.4 ± 0.8 6.6 ± 3.0 2 (10.0) 18 (90.0) 10 (55.6) 10 (45.4) 7 (31.8)
0 1 1 0 0
– – (0) (100.0) (100.0) (0) (0)
13 1 6 2 0
0 0 1 0 0
(0) (0) (100.0) (0) (0)
(59.1) (4.5) (27.2) (9.1) (0)
Values presented as frequencies with percentage in parenthesis unless otherwise indicated. a Hunt and Hess Grade IV–V. b Presence of additional intracranial vascular anomalies. c Combined modalities used. ACA = anterior cerebral artery, ACommA = anterior communicating artery, BA = basilar artery, ICA = internal carotid artery, MCA = middle cerebral artery, PCA = posterior cerebral artery, SAH = subarachnoid hemorrhage, SD = standard deviation, VA = vertebral artery, – = no data.
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M.A. Patel et al. / Journal of Clinical Neuroscience 21 (2014) 2184–2188 Table 2 Characteristics of patients with aneurysms adjacent to but distinct from fenestrations Location of fenestration N Age, years, mean ± SD Aneurysm size, mm, mean ± SD Unruptured Ruptured Unruptured SAH Poor grade a Female Other lesions b Treatment Clipping Wrapping Endovascular Other c Combined
ACA
ICA
BA
VA
5 58.8 ± 5.4
3 37.3 ± 9.0
1 46.0 ± 0
4 49.5 ± 21.4
– 25.0 ± 0
– –
9.2 ± 0 –
40.0 ± 0 –
1 4 2 0 1
(20.0) (80.0) (50.0) (0) (20.0)
0 3 1 3 1
(0) (100.0) (33.3) (100.0) (33.3)
1 0 0 1 1
(100.0) (0) (0) (100.0) (100.0)
1 3 0 2 1
(25.0) (75.0) (0) (50.0) (25.0)
3 0 0 2 0
(60.0) (0) (0) (40.0) (0)
1 1 0 1 0
(33.3) (33.3) (0) (33.3) (0)
0 0 0 1 0
0 0 0 (100.0) (0)
2 0 0 1 1
(50.0) (0) (0) (25.0) (25.0)
Values presented as frequencies with percentage in parenthesis unless otherwise indicated. a Hunt and Hess Grade IV–V. b Presence of additional intracranial vascular anomalies. c Combined modalities used. ACA = anterior cerebral artery, BA = basilar artery, ICA = internal carotid artery, SAH = subarachnoid hemorrhage, SD = standard deviation, VA = vertebral artery, – = no data.
4.3. Associated intracranial vascular lesions Additional cerebrovascular lesions were associated with 38% of fenestrations with aneurysms arising from the fenestration, and 31% of fenestrations associated with aneurysms distinct from the fenestration (Tables 1 and 2). Such malformations included persistent primitive hypoglossal artery, P2 segment of fetal origin, anterior inferior cerebellar artery origin displaced to the posterior inferior cerebellar artery–VA junction, hypoplastic VA, azygous ACA, dolichoectatic BA, VA originating from the aorta, VA duplication, bilateral accessory MCA, hypoplastic A1 segment, premoyamoya like changes, and additional fenestrations [6,12,16,17, 23,34–40,45,48–51].
5. Discussion We present our review of the literature of aneurysms associated with arterial fenestrations in addition to presenting four additional patients. The most common presentation of cerebral aneurysms associated with fenestrated arteries is SAH. Furthermore, the aneurysms associated with fenestrations of the carotid system are most likely to present with SAH. Recognition of these findings may be useful as the majority of patients with fenestration-associated aneurysms present with SAH, and preoperative angiographic identification of fenestrations may be difficult [6,8]. Thus, when a fenestration is incidentally discovered on imaging or intraoperatively, it is important that the surgeon accurately rule out the presence of an associated aneurysm. Moreover, even if a fenestration is not observed on imaging, seemingly anomalous duplicated vasculature found near an aneurysm intraoperatively should raise suspicion for a fenestrated artery and should be explored further to rule out an occult aneurysm. The literature varies regarding the angiographic post mortem incidence of fenestrations. The angiographic incidence of all fenestrations has been reported to be 0.3–0.9%, whereas autopsy studies show the incidence of ACommA fenestrations to be 7.5–40%, BA fenestrations 1–5%, and VA fenestrations to be 1–2% [19,51]. The higher sensitivity of post mortem analysis and the under-reporting of fenestrations on angiography can explain such discrepancies, as fenestrations are often asymptomatic unless accompanied by a symptomatic aneurysm [6]. Several authors have hypothesized that cerebral fenestrations are predisposed to aneurysm formation because of collagen defects
in the tunica media that weaken the arterial wall at the distal and proximal edges of the fenestration [3,12–14]. Moreover, animal models of aneurysm formation show that defects in elastin composition of the tunica media combined with a pro-inflammatory state that further damages an already weakened vascular wall predisposes to aneurysms [59]. In accordance with our findings, others have observed that patients most often present with fenestrations associated with the VA and BA [19]. Through morphologic analysis of the BA, Black and Ansbacher have shown thinning, and even absence, of the tunica media starting 200 lm proximal to the medial and ventral walls of the fenestration and its associated aneurysm, and again at the opposite end of the fenestration where the branches have reunited [12]. Alfano and colleagues have reported that vascular bifurcations with high wall shear stress and accelerated, turbulent flow are especially prone to intracranial aneurysm formation [57]. In fact, studies show that turbulence at the bifurcations of fenestrations produces hemodynamic stress that can predispose the vessel to aneurysms [3,12,14]. In an autopsy study Campos et al. report 35.5% of cases were fenestrated BA, and they explain that the turbulent flow at the vertebrobasilar junction paired with congenital medial defects may explain the high incidence of aneurysms at fenestrated BA [3]. Nevertheless, some have argued that fenestration-associated aneurysms are incidental, and that the incidence of fenestration-related aneurysm is the same as the overall population [2,58]. Our review revealed 13 cases of aneurysms adjacent to fenestrations and 23 cases with concurrent cerebral vascular anomalies in addition to the fenestration and associated aneurysm [8,15,19,20,26,36–42,47,50–53]. Fenestrations themselves arise from the incomplete or absent fusion or division of venous plexuses or primitive neural arteries [6,19]. It is possible that in an environment predisposed to congenital vascular anomaly, other vascular malformations may have the propensity to arise [19]. Whether or not such an association exists remains an avenue for future study.
6. Conclusion We conducted a comprehensive review of the literature on cerebral arterial fenestrations and associated aneurysms and other vascular anomalies. In addition, we present our experience with four additional patients. This review underscores the need for recognizing cerebral arterial fenestration-associated aneurysms and
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their propensity toward rupture. Strong support for the embryologic predisposition of aneurysm formation at fenestrations exists, and further inquiry into the association of arterial fenestration with other cerebrovascular anomalies will be useful. Conflicts of Interest/Disclosures Geoffrey Colby and Alexander Coon receive funding from and/or are associated with Covidien (Dublin, Ireland). The other authors declare that they have no financial or other conflicts of interest in relation to this research and its publication. References [1] Osborn RE, Kirk G. Cerebral arterial fenestration. Comput Radiol 1987;11:141–5. [2] Sanders W, Sorek P, Mehta B. Fenestration of intracranial arteries with special attention to associated aneurysms and other anomalies. AJNR Am J Neuroradiol 1993;14:675–80. [3] Campos J, Fox A, Viñuela F, et al. Saccular aneurysms in basilar artery fenestration. Am J Neuroradiol 1987;8:233–6. [4] de Gast AN, van Rooij WJ, Sluzewski M. Fenestrations of the anterior communicating artery: incidence on 3D angiography and relationship to aneurysms. Am J Neuroradiol 2008;29:296–8. [5] Cademartiri F, Stojanov D, Dippel DWJ, et al. Noninvasive detection of a ruptured aneurysm at a basilar artery fenestration with submillimeter multisection CT angiography. Am J Neuroradiol 2003;24:2009–10. [6] Hacein-Bey L, Muszynski CA, Varelas PN. Saccular aneurysm associated with posterior cerebral artery fenestration manifesting as a subarachnoid hemorrhage in a child. Am J Neuroradiol 2002;23:1291–4. [7] Teal JS, Rumbaugh CL, Bergeron RT, et al. Angiographic demonstration of fenestrations of the intradural intracranial arteries. Radiology 1973;106:123–6. [8] San-Galli F, Leman C, Kien P, et al. Cerebral arterial fenestrations associated with intracranial saccular aneurysms. Neurosurgery 1992;30:279–83. [9] Sun ZK, Li M, Li MH, et al. Fenestrations accompanied by intracranial aneurysms assessed with magnetic resonance angiography. Neurol India 2012;60:45–9. [10] Hassler O. The windows of the internal elastic lamella of the cerebral arteries. Virchows Arch Pathol Anat Physiol Klin Med 1962;335:127–32. [11] Hassler O. Scanning electron microscopy of saccular intracranial aneurysms. Am J Pathol 1972;68:511–20. [12] Black SP, Ansbacher LE. Saccular aneurysm associated with segmental duplication of the basilar artery. J Neurosurg 1984;61:1005–8. [13] De Caro R, Serafini M, Galli S, et al. Anatomy of segmental duplication in the human basilar artery. Possible site of aneurysm formation. Clin Neuropathol 1995;14:303–9. [14] Finlay HM, Canham PB. The layered fabric of cerebral artery fenestrations. Stroke 1994;25:1799–806. [15] Hori E, Kurosaki K, Matsumura N, et al. Multiple aneurysms arising from the origin of a duplication of the middle cerebral artery. J Clin Neurosci 2005;12:812–5. [16] Imaizumi S, Onuma T, Motohashi O, et al. Unruptured carotid-duplicated middle cerebral artery aneurysm: case report. Surg Neurol 2002;58:322–4. [17] In S, In K, Kusano N, et al. A case of duplication of the middle cerebral artery with ruptured aneurysm on its origin during pregnancy (author’s transl). No Shinkei Geka 1981;9:337–41. [18] Takano S, Nose T, Oowada T, et al. Aneurysm arising from duplicated middle cerebral artery: case report. Neurol Med Chir (Tokyo) 1988;28:910–4. [19] Chen Y, Chang F, Hu H, Chao A. Fenestration of the supraclinoid internal carotid artery associated with aneurysm and ischemic stroke. Surg Neurol 2007;68:S60–3 [discussion S63]. [20] Findlay JM, Chui M, Muller PJ. Fenestration of the supraclinoid internal carotid artery. Can J Neurol Sci 1987;14:159–61. [21] Hattori T, Kobayashi H. Fenestration of the supraclinoid internal carotid artery associated with carotid bifurcation aneurysm. Surg Neurol 1992;37:284–8. [22] Ichikawa T, Miyachi S, Izumi T, et al. Fenestration of a supraclinoid internal carotid artery associated with dual aneurysms: case report. Neurosurgery 2011;69:E1005–9 [discussion E1009]. [23] Katsuta T, Matsubara T, Fujii K. Fenestration of the supraclinoid internal carotid artery. Neuroradiology 1993;35:461. [24] Ng PP, Steinfort B, Stoodley MA. Internal carotid artery fenestration with dual aneurysms. J Neurosurg 2006;104:979. [25] Onoda K, Ono S, Tokunaga K, et al. Fenestration of the supraclinoid internal carotid artery with associated aneurysm-case report. Neurol Med 2008;48:118–20. [26] Taylor R, Connolly ES Jr, Duong H. Radiographic evidence and surgical confirmation of a saccular aneurysm on a hypoplastic duplicated A1 segment of the anterior cerebral artery: case report. Neurosurgery 2000;46:482–4. [27] Miyazaki S, Kamata K, Yamaura A. Multiple aneurysms of the vertebrobasilar system associated with fenestration of the vertebral artery. Surg Neurol 1981;15:192–5.
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