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Bilateral Cavernous Carotid Aneurysms: The Growth Potential of a Contralateral Aneurysm after Therapeutic Unilateral Internal Carotid Artery Occlusion
Bilateral Cavernous Carotid Aneurysms: The Growth Potential of a Contralateral Aneurysm after Therapeutic Unilateral Internal Carotid Artery Occlusion Kazuhiko Nishino, MD, Hitoshi Hasegawa, MD, Yasushi Ito, MD, and Yukihiko Fujii, MD
Background: Although the introduction of flow-diverter stents has been recognized as a major revolution in the treatment of cavernous carotid aneurysms (CCAs), therapeutic internal carotid artery occlusion (TICAO) remains a reliable procedure for alleviating symptoms caused by CCAs. However, TICAO has the potential risk of the enlargement of coexisting aneurysms that are frequently detected in CCA patients. The purpose of this study is to assess the occurrence of the enlargement of aneurysms coexisting with CCAs after TICAO. Methods: We reviewed medical charts of CCA patients who were managed using unilateral TICAO. Coexisting aneurysms were identified using angiograms obtained before TICAO, and imaging data in long follow-up periods were retrospectively examined to determine the extent of the enlargement after TICAO. Results: Of 12 patients with CCAs, 10 had 12 coexisting aneurysms; 5 of the coexisting aneurysms (41.7%) showed enlargement during a mean follow-up period of 8.1 years, and all enlarged aneurysms were smaller of the bilateral CCAs; the larger CCA had been managed by TICAO. Five of 6 (83.3%) patients with bilateral CCAs showed enlargement of the contralateral aneurysm after TICAO. Two contralateral CCAs showed marked enlargement after TICAO and were subsequently treated with stent-assisted coil embolization. Conclusions: Contralateral, smaller aneurysms frequently enlarge after unilateral TICAO in patients with bilateral CCAs. The findings emphasize the importance of long-term observation after TICAO and appropriate interventions against enlarging contralateral aneurysms. Key Words: Therapeutic carotid occlusion—cavernous carotid aneurysm—stent-assisted coil embolization—enlargement. Ó 2015 by National Stroke Association
The emergence of flow-diverter stents has promised to revolutionize the treatment of cavernous carotid aneurysms (CCAs), and recent reports demonstrated the excellent clinical results and high rates of complete occlusion, given the ideal vessel characteristics of the cavernous segment of internal carotid artery (ICA) for flow diversion.1 Meanwhile, therapeutic ICA occlusion (TICAO) is
occasionally the safest and most effective method to alleviate the mass effect caused by CCAs.2,3 However, TICAO may predispose patients to long-term complications, including the formation of de novo aneurysms and enlargement of any coexisting aneurysms. Although several authors have conducted detailed characterizations of the de novo aneurysms following TICAO,4,5 the
From the Department of Neurosurgery, Brain Research Institute, Niigata University, Niigata, Japan. Received March 6, 2015; revision received April 11, 2015; accepted April 17, 2015. The authors declare that they did not receive any grant support. The authors declare that they have no conflicts of interest.
Address correspondence to Kazuhiko Nishino, MD, Department of Neurosurgery, Brain Research Institute, Niigata University, 1-757, Asahimachidori, Chuo-ku, Niigata 951-8585, Japan. E-mail: [email protected]. 1052-3057/$ - see front matter Ó 2015 by National Stroke Association http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2015.04.025
Journal of Stroke and Cerebrovascular Diseases, Vol. 24, No. 8 (August), 2015: pp 1865-1872
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enlargement of coexisting aneurysms after TICAO has rarely been documented.6-8 CCAs frequently coexist with intracranial aneurysms in other locations9,10 and sometimes arise from the bilateral ICA as mirror aneurysms.11,12 Therefore, it is important to clarify the possibility that coexisting aneurysms will enlarge after TICAO in CCA patients. If the contralateral aneurysm enlarged after unilateral TICAO in a bilateral CCA patient, the treatment decisions become particularly complicated. This study evaluated the growth potential of coexisting aneurysms following TICAO for the treatment of the CCAs. In addition, we provide a discussion of the treatment options for enlarging, coexisting aneurysms after TICAO.
Methods Eighteen patients with CCAs underwent TICAO at our institute between 1993 and 2011. Patients were excluded from the study if their coexisting aneurysms were treated after the TICAO, follow-up imaging had not been appropriately obtained, or the follow-up period was less than 2 years. Accordingly, 12 patients, including 10 women and 2 men (mean age, 64.2 years; range, 39-77 years), were included in this study. The clinical presentations included ophthalmoplegia (10 patients), visual disturbance (1), and asymptomatic (1). Five patients had preexisting hypertension. All patients underwent cerebral angiography to determine the exact location and configuration of the CCA and to detect coexisting intracranial aneurysms. In all cases, an intravascular balloon test occlusion (BTO) was performed to evaluate TICAO tolerance. For cases determined to be clinically intolerant of TICAO, high-flow bypass was indicated. Patients who were clinically tolerant, but had insufficient collateral circulation, underwent superficial temporal artery-middle cerebral artery (STA-MCA) bypass before TICAO. Patients were treated using TICAO alone, if their collateral flow was sufficient. After TICAO, patients underwent periodic radiographic evaluations using magnetic resonance angiography (MRA) or computed tomography angiography for more than 2 years. Using the follow-up images, we assessed thrombosis and shrinkage of the treated CCAs, recanalization of the occluded ICA, and the enlargement of coexisting aneurysms. The ethics committee at Niigata University School of Medicine approved this study, and informed consent was obtained from each patient.
Results Because all patients were determined to be clinically tolerant, none underwent high-flow bypass; 8 patients underwent TICAO and STA-MCA bypass, and 4 patients underwent TICAO alone. ICAs were therapeutically
occluded in the cervical portion in 4 patients, the petrous portion in 6, and the intracavernous portion (internal trapping) in 2. Used materials for the occlusion were as follows: detachable coils in 7 patients, detachable balloons in 4, and both in 1. The average follow-up period was 8.1 years (range, 3-16 years) after TICAO (Table 1). All treated CCAs showed thrombosis and shrinkage of the sac, and the 11 symptomatic patients showed clinical improvement (Fig 1). STA-MCA bypass was patent in all cases, and recanalization of the occluded ICA was not detected during the follow-up period. Neither disabling stroke nor aggravation of the mass effect occurred after the TICAO, regardless of whether they underwent bypass surgery. However, one patient (case 2) developed a hemiparesis 2 days after TICAO, and another patient (case 8) presented a motor aphasia 2 days later. Both cases responded to medical treatments, and ischemic symptoms resolved within a week. The hypertension was controlled during the follow-up period except for the periprocedural term in all 5 patients. Of the 12 patients, 10 (83.3%) had 12 coexisting aneurysms before TICAO. The aneurysm locations were variable (Table 1), including 6 contralateral CCAs, 2 MCA aneurysms, 1 anterior communicating artery aneurysm, 1 distal anterior cerebral artery aneurysm, 1 basilar artery aneurysm, and 1 vertebral artery aneurysm. The coexisting aneurysms ranged in diameter from 2 mm to 8 mm. Of the 12 coexisting aneurysms, 5 (41.7%) enlarged during the follow-up period; all 5 were smaller of bilateral CCAs and were contralateral to the TICAO-treated larger aneurysm. Thus, 5 of 6 (83.3%) patients with bilateral CCAs showed enlargement of the contralateral aneurysm after TICAO. Of these 5 cases, 4 patients had undergone TICAO with an STA-MCA bypass and one was managed with TICAO, alone. Although the degree and rate of the enlargement was inconsistent among the aneurysms, 2 cases showed marked enlargement to more than 15 mm in diameter (Table 1). Although these large aneurysms remained asymptomatic, they were treated with the stent-assisted coil embolization, resulting in the suppression of further enlargement.
Representative Cases Case 5 A 77-year-old woman presented with a 2-month history of diplopia. A neurologic examination revealed right oculomotor and abducens nerve palsies. Radiographic examinations demonstrated a large CCA on the right side and a small one (3 mm in diameter) in the posterior bend of the cavernous segment of the right ICA (Fig 2, A,B). The patient showed tolerance during the BTO, and collateral flow was considered to be sufficient. Thus, the ICA was occluded at the petrous portion using detachable coils without an STA-MCA bypass. Follow-up MRA demonstrated gradual enlargement of the left CCA, until it
TICAO Case Age/ No. sex
Coexisting aneurysm
Clinical symptoms
Treated aneurysm
Bypass
Site
Materials
Cervical ICA Cervical ICA
Coils, balloons Balloons
1 2
54/F 62/F
Ophthalmoplegia Visual disturbance
R CCA R CCA
STA-MCA STA-MCA
3 4 5 6 7
67/M 69/F 77/F 39/F 77/F
Ophthalmoplegia Ophthalmoplegia Ophthalmoplegia Ophthalmoplegia Ophthalmoplegia
L CCA R CCA L CCA L CCA L CCA
STA-MCA Petrous ICA STA-MCA Cervical ICA None Petrous ICA STA-MCA Petrous ICA None Cavernous ICA
8
68/F
Ophthalmoplegia
L CCA
STA-MCA
9 10 11 12
68/F 46/F 73/M 70/F
Ophthalmoplegia Ophthalmoplegia Asymptomatic Ophthalmoplegia
L CCA L CCA R CCA R CCA
STA-MCA Cavernous ICA STA-MCA Cervical ICA None Petrous ICA None Petrous ICA
Petrous ICA
Periprocedural Followcomplications up (y)
HT
Location/size
Outcome
Treatment
— Growth (2-5 mm)
— Observation
None Transient hemiparesis None None None None None
16 15
— None Treated L CCA/2 mm
14 9 8 7 7
Coils
Transient aphasia
6
— Treated — — — — —
None — BA/5 mm Stable R CCA/3 mm Growth (3-13 mm) R CCA/5 mm Growth (5-10 mm) Acom/2 mm Stable L MCA/5 mm Stable R CCA/8 mm Growth (8-15 mm)
— Observation Observation Observation Observation Observation SAC
Coils Balloons Coils Coils
None None None None
6 5 3 3
Treated Treated Treated —
R VA/6 mm Stable R ACA/3 mm Stable R CCA/8 mm Growth (8-17 mm) R MCA/4 mm Stable L CCA/2 mm Stable
Observation Observation SAC Observation Observation
Balloons Balloons Coils Coils Coils
BILATERAL CAVERNOUS CAROTID ANEURYSMS
Table 1. Patient characteristics, treatment, and coexisting aneurysms
Abbreviations: Acom, anterior communicating artery; ACA, anterior cerebral artery; BA, basilar artery; CCA, cavernous carotid aneurysm; F, female; HT, hypertension; ICA, internal carotid artery; L, left; R, right; M, male; SAC, stent-assisted coil embolization; STA-MCA, superficial temporal artery-middle cerebral artery; TICAO, therapeutic internal carotid artery occlusion; VA, vertebral artery.
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Figure 1. Case 12. Sequential changes of the aneurysm size after therapeutic internal carotid artery occlusion (TICAO). An angiogram obtained before the treatment shows a large right cavernous carotid aneurysm (CCA) (A). The petrous portion of the internal carotid artery was occluded by detachable coils (B). Serial magnetic resonance images (T1-weighted images) obtained after TICAO; 2 days (C), 3 months (D), and 1 year later (E). The CCA shows acute thrombosis and gradual shrinkage of the sac.
reached 13 mm diameter, 8 years after TICAO (Fig 2, C-E). Given that the aneurysm remains asymptomatic and the patient is an octogenarian, we have elected to keep the aneurysm under careful observation. Case 10 A 46-year-old woman presented with a 6-month history of diplopia, also demonstrating left abducens nerve palsy. Radiographic examinations revealed a large CCA on her left side and a smaller one (8 mm in diameter) in the right cavernous segment of the ICA (Fig 3, A,B). Because the patient showed insufficient collateral flow during the BTO, STA-MCA double bypasses were performed, and
the cervical ICA was occluded using detachable balloons. Follow-up MRA demonstrated gradual enlargement, and angiograms obtained 4 years after TICAO revealed marked enlargement of the aneurysm to a diameter of 17 mm, although the aneurysm remained asymptomatic (Fig 3C). The patient underwent stent-assisted coil embolization to avoid the occlusion of her right ICA, suppressing further enlargement (Fig 3D).
Discussion The emergence of flow-diverter stents may be considered one of the biggest breakthroughs in the management
Figure 2. Case 5. An angiogram (A) and magnetic resonance angiography (MRA) (B) obtained before initial treatment. A large right cavernous carotid aneurysm (CCA) is seen. Note a small aneurysm on the posterior bend of the left cavernous segment of the internal carotid artery (ICA; arrow in B). Serial MRA obtained after therapeutic ICA occlusion; 2 years (C), 4 years (D), and 8 years later (E). The left CCA shows gradual enlargement up to 13 mm in diameter.
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Figure 3. Case 10. Angiograms obtained before initial treatment; left internal carotid angiography (ICAG) (A), right ICAG (B). A large left cavernous carotid aneurysm (CCA) is seen (A). Note an aneurysm in the right cavernous segment of the internal carotid artery (ICA; arrow in B). Right ICAG obtained 4 years after therapeutic ICA occlusion with a bypass surgery demonstrates marked enlargement of the right CCA (C). Right ICAG obtained after stentassisted coil embolization (D).
of CCAs, and its use seems to be rapidly growing and moving toward the mainstream of CCA treatment.1,13 Meanwhile, TICAO with bypass surgery has been traditionally considered the safest and most effective method to alleviate the mass effect caused by CCAs, and many case series have demonstrated excellent treatment results.7,14 However, TICAO has a potential risk of long-term complications including de novo aneurysm formation and enlargement of coexisting aneurysms. According to a review article, more than 500 patients with CCA underwent TICAO plus or minus bypass surgery since 1990.15 However, the evaluation for TICAO-related complications was conducted in periprocedural term in almost all articles, and follow-up period was relatively shorter compared with the present study (8.1 years of mean follow-up period). In addition, there are few descriptions about the presence or absence of coexisting aneurysms, despite CCAs are considered to frequently have accompanying aneurysms in other locations. In the present study, we thoroughly examined the presence of aneurysms coexisting with CCAs, including very small aneurysms (,2 mm in diameter), and carefully evaluated the subsequent imaging data to detect the enlargement of the aneurysms over a long period. Interestingly, 50% (6 of 12) of CCA patients had an additional aneurysm arising from contralateral
cavernous segment of ICA as mirror aneurysms, and all the aneurysms that enlarged after unilateral TICAO were the smaller of the bilateral CCAs. We found 7 articles describing the enlargement of coexisting aneurysms after TICAO or therapeutic common carotid artery occlusion (Table 2).6-8,16-19 Among the 9 cases, 6 had bilateral CCAs and the enlargement occurred after parent artery occlusion for the contralateral aneurysms, as in our cases. Therefore, these observations suggest that contralateral aneurysms of bilateral CCAs are more likely to enlarge after unilateral TICAO than aneurysms in other locations. Regarding the growth mechanism of contralateral CCA after unilateral TICAO, hemodynamic stress on the wall of contralateral ICA is the most likely cause, because contralateral ICA would function as main source of collateral blood flow following TICAO. The expected advantages of the bypass surgery associated with TICAO are not confined to the prevention of brain ischemia, but also the reduction of the hemodynamic stress on collateral pathways. Although most cases listed in Table 2 underwent TICAO alone, we actively performed the bypass surgery before TICAO. However, our results indicated that the bypass surgery was unlikely to prevent the enlargement of aneurysms arising from this specific location.
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Table 2. Series of enlargement of coexisting aneurysms after therapeutic ICA or common carotid artery occlusion Initially treated aneurysm Age/ sex
Location
de Morais et al,16 1978 42/F
L CCA
Faria et al,17 1980
41/F
Fujiwara et al,18 1993
Authors and year
Treatment
Enlarged coexisting aneurysm Location
Treatment
L common carotid artery occlusion
R CCA
R CCA
R common carotid artery occlusion
L CCA
54/F
R CCA
L CCA
?/?
ICA
R ICA partial occlusion with EC-IC bypass Common carotid artery occlusion
R common carotid artery occlusion L common carotid artery occlusion —
Larson et al,7 1995 Niiro et al,19 2000
58/? 52/M
ICA L CCA
Clarenc¸on et al,6 2011 Matouk et al,8 2012
50/F 52/F
L CCA CCA
Petrous ICA occlusion with balloons L cervical ICA occlusion with a vascular clamp L petrous ICA occlusion with coils Intracranial ICA occlusion
Present series case 2 Case 5 Case 6 Case 8 Case 10
39/M 62/F 77/F 39/F 68/F 46/F
CCA R CCA L CCA L CCA L CCA L CCA
Intracranial ICA occlusion R ICA occlusion with STA-MCA bypass L ICA occlusion L ICA occlusion with STA-MCA bypass L ICA occlusion with STA-MCA bypass L ICA occlusion with STA-MCA bypass
Contralateral — intradural ICA Acom Clipping R CCA R ICA occlusion with high-flow bypass R CCA Flow-diverter stents Contralateral — CCA BA — L CCA Observation R CCA Observation R CCA Observation R CCA SAC R CCA SAC
Abbreviations: Acom, anterior communicating artery; BA, basilar artery; CCA, cavernous carotid aneurysm; EC-IC, extracranial-intracranial; F, female; ICA, internal carotid artery; L, left; R, right; M, male; SAC, stent-assisted coil embolization; STA-MCA, superficial temporal arterymiddle cerebral artery.
On the other hand, Burns et al20 reported that CCAs showed a higher frequency of spontaneous enlargement than aneurysms arising from other locations, with a frequency that reached 31.6% (6 of 19) over a median 47-month follow-up period. In addition, several authors speculated that congenital factors might have played a role for the pathogenesis of CCAs, considering the predominant occurrence in female patients, the dysplastic nature of the aneurysm, and an association with genetic disorders, including Marfan syndrome, fibromuscular dysplasia, and polycystic kidney.21-23 These findings indicate that CCA is likely to have a different growth potential from aneurysms in other locations, although the growth after TICAO might be triggered by the hemodynamic alteration following TICAO. With respect to the treatment choice, our results indicate that a deliberate strategy is required for treating patients with bilateral CCAs. First, when treating the larger, symptomatic aneurysms, a decision as to whether the ICA should be occluded is critical. Flow-diverter stents are theoretically ideal devices for preserving blood flow in parent vessels and avoiding coil deployment into the aneurysmal lumen. However, if the configuration of cavernous segment of the ICA is unsuitable for the use of flow-diverter stents, its use has a potential risk of serious complications. In addition, there are no data available regarding a long-term efficacy of the treatment with
flow-diverter stents. Considering that a CCA is not a lifethreatening disease, the safety of the treatment should be as high as possible. We believe that TICAO with bypass surgery is occasionally a safe procedure for the management of the symptomatic CCA, providing patients with long-term stability. The second issue is how to treat if the contralateral aneurysm enlarged to a critical size. In case of a patient who had undergone unilateral TICAO, it must be essential to preserve the remaining ICA. The use of flowdiverter stents seems to be ideal in this situation. We performed stent-assisted coil embolization in 2 patients who showed marked enlargement (to .15 mm) of the contralateral aneurysm, despite remaining asymptomatic. Although this option is less effective for symptoms caused by mass effect,24-26 several studies have demonstrated favorite clinical outcomes following stentassisted coil embolization of asymptomatic CCAs.27,28 With respect to this critical size, Choulakian et al24 mentioned that the mean size of CCAs presenting with cranial nerve palsies was 17 mm, in their series of 113 patients. The data should be considered as reference values for decisions on the timing of treatments for enlarging aneurysms. It is naturally important to perform careful follow-up even after the stent-assisted coil embolization, because this procedure tends to be incomplete packing of coils. In the cases that enlarged aneurysms
BILATERAL CAVERNOUS CAROTID ANEURYSMS
had unfavorable configuration for endovascular procedures, therapeutic occlusion of the remaining ICA, in combination with bypass surgery, might be an alternative treatment option for a growing contralateral aneurysm. However, the strategy entails the potential risk of ischemic complications because it results in bilateral ICA occlusion. In addition, such a hemodynamic situation is likely to increase the hemodynamic stress on the vertebrobasilar system that functions as a collateral pathway, increasing the potential risk of de novo aneurysm formation in the basilar artery, posterior cerebral artery, or posterior communicating artery.29,30 The limitations of the present study include the small sample size, retrospective design, and possible selection bias. In addition, we do not have comparable data for patients with untreated bilateral CCAs. We could not also find articles describing the natural course of bilateral CCAs with long-term follow-up. If valuable studies were conducted to demonstrate the natural course of bilateral CCA, they would contribute to identify how unilateral TICAO has an influence on the enlargement of contralateral CCA.
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7.
8.
9.
10.
11.
12.
13.
Conclusions In 83% of bilateral CCA cases, a smaller, contralateral aneurysm enlarged after a unilateral TICAO for a larger CCA aneurysm, and the bypass surgery did not prevent the enlargement. The findings indicate that surgeons should have a deliberate strategy to manage bilateral CCA cases. Additionally, careful follow-up after TICAO is essential for determining the appropriate treatment option and the timing for treating enlarging contralateral aneurysms.
References 1. Puffer RC, Piano M, Lanzino G, et al. Treatment of cavernous sinus aneurysms with flow diversion: results in 44 patients. AJNR Am J Neuroradiol 2014;35:948-951. 2. Turfe ZA, Brinjikji W, Murad MH, et al. Endovascular coiling versus parent artery occlusion for treatment of cavernous carotid aneurysms: a meta-analysis. J Neurointerv Surg 2015;7:250-255. 3. van der Schaaf IC, Brilstra EH, Buskens E, et al. Endovascular treatment of aneurysms in the cavernous sinus: a systematic review on balloon occlusion of the parent vessel and embolization with coils. Stroke 2002;33: 313-318. 4. Arambepola PK, McEvoy SD, Bulsara KR. De novo aneurysm formation after carotid artery occlusion for cerebral aneurysms. Skull base 2010;20:405-408. 5. Arnaout OM, Rahme RJ, Aoun SG, et al. De novo large fusiform posterior circulation aneurysm presenting with subarachnoid hemorrhage 7 years after therapeutic internal carotid artery occlusion: case report and review of literature. Neurosurgery 2012;71:764-771. 6. Clarenc¸on F, Bonneville F, Boch AL, et al. Parent artery occlusion is not obsolete in giant aneurysms of the ICA.
14.
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Experience with very-long-term follow-up. Neuroradiology 2011;53:973-982. Larson JJ, Tew JM Jr, Tomsick TA, et al. Treatment of aneurysms of the internal carotid artery by intravascular balloon occlusion: long-term follow-up of 58 patients. Neurosurgery 1995;36:26-30. Matouk CC, Kaderali Z, terBrugge KG, et al. Long-term clinical and imaging follow-up of complex intracranial aneurysms treated by endovascular parent vessel occlusion. AJNR Am J Neuroradiol 2012;33:1991-1997. Linskey ME, Sekhar LN, Hirsch W Jr, et al. Aneurysms of the intracavernous carotid artery: clinical presentation, radiographic features, and pathogenesis. Neurosurgery 1990;26:71-79. Rinne J, Hernesniemi J, Puranen M, et al. Multiple intracranial aneurysms in a defined population: prospective angiographic and clinical study. Neurosurgery 1994;35: 803-808. Eguchi T, Nakagomi T, Teraoka A. Treatment of bilateral mycotic intracavernous carotid aneurysms. Case report. J Neurosurg 1982;56:443-447. Yamada K, Nakahara T, Kishida K, et al. Multiple ‘‘mirror’’ aneurysms involving intracavernous carotid arteries and vertebral arteries: case report. Surg Neurol 2000;54:361-365. Mattei TA, Ferrell AS, Britz GW. Is flow diversion the death of cerebral bypass and coiling/stent-assisted coiling for giant cavernous aneurysms? A critical review on comparative outcomes and ongoing clinical trials. Neurosurg Rev 2013;36:505-511. Shimizu H, Matsumoto Y, Tominaga T. Parent artery occlusion with bypass surgery for the treatment of internal carotid artery aneurysms: clinical and hemodynamic results. Clin Neurol Neurosurg 2010;112:32-39. Ambekar S, Madhugiri V, Sharma M, et al. Evolution of management strategies for cavernous carotid aneurysms: a review. World Neurosurg 2014;82:1077-1085. de Morais JV, Lana-Peixoto MA. Bilateral intracavernous carotid aneurysms: treatment by bilateral carotid ligation. Surg Neurol 1978;9:379-381. Faria MA Jr, Fleischer AS, Spector RH. Bilateral giant intracavernous carotid aneurysms treated by bilateral carotid ligation. Surg Neurol 1980;14:207-210. Fujiwara S, Fujii K, Fukui M. De novo aneurysm formation and aneurysm growth following therapeutic carotid occlusion for intracranial internal carotid artery (ICA) occlusion. Acta Neurochir (Wien) 1993; 120:20-25. Niiro M, Shimozuru T, Nakamura K, et al. Long-term follow-up study of patients with cavernous sinus aneurysm treated by proximal occlusion. Neurol Med Chir (Tokyo) 2000;40:88-97. Burns JD, Huston J 3rd, Layton KF, et al. Intracranial aneurysm enlargement on serial magnetic resonance angiography: frequency and risk factors. Stroke 2009; 40:406-411. Higashida RT, Halbach VV, Hieshima GB, et al. Cavernous carotid artery aneurysm associated with Marfan’s syndrome: treatment by balloon embolization therapy. Neurosurgery 1988;22:297-300. Ponte KF, Mont’Alverne FJ, Ribeiro EM, et al. [Giant aneurysm of the intracavernous internal carotid artery associated with autosomal dominant polycystic kidney disease: case report]. Arq Neuropsiquiatr 2006;64: 881-884. Rebollo M, Quintana F, Combarros O, et al. Giant aneurysm of the intracavernous carotid artery and bilateral
1872 carotid fibromuscular dysplasia. J Neurol Neurosurg Psychiatry 1983;46:284-285. 24. Choulakian A, Drazin D, Alexander MJ. Endosaccular treatment of 113 cavernous carotid artery aneurysms. J Neurointerv Surg 2010;2:359-362. 25. Kim LJ, Tariq F, Levitt M, et al. Multimodality treatment of complex unruptured cavernous and paraclinoid aneurysms. Neurosurgery 2014;74:51-61. 26. van Rooij WJ, Sluzewski M. Unruptured large and giant carotid artery aneurysms presenting with cranial nerve palsy: comparison of clinical recovery after selective aneurysm coiling and therapeutic carotid artery occlusion. AJNR Am J Neuroradiol 2008;29: 997-1002.
K. NISHINO ET AL. 27. Fargen KM, Hoh BL, Welch BG, et al. Long-term results of enterprise stent-assisted coiling of cerebral aneurysms. Neurosurgery 2012;71:239-244. 28. Lopes DK, Johnson AK, Kellogg RG, et al. Long-term radiographic results of stent-assisted embolization of cerebral aneurysms. Neurosurgery 2014;74:286-291. 29. Yamanaka C, Kiya K, Yoshimoto H, et al. [Basilar bifurcation aneurysm associated with internal carotid artery occlusion. Report of two cases]. Neurol Med Chir (Tokyo) 1989;29:151-156. 30. Araki T, Fujiwara H, Yasuda T, et al. [A case of aneurysmal subarachnoid hemorrhage associated with bilateral common carotid artery occlusion]. No Shinkei Geka 2002;30:853-858.
Background: Although the introduction of flow-diverter stents has been recognized as a major revolution in the treatment of cavernous carotid aneurysms (CCAs), therapeutic internal carotid artery occlusion (TICAO) remains a reliable procedure for alleviating symptoms caused by CCAs. However, TICAO has the potential risk of the enlargement of coexisting aneurysms that are frequently detected in CCA patients. The purpose of this study is to assess the occurrence of the enlargement of aneurysms coexisting with CCAs after TICAO. Methods: We reviewed medical charts of CCA patients who were managed using unilateral TICAO. Coexisting aneurysms were identified using angiograms obtained before TICAO, and imaging data in long follow-up periods were retrospectively examined to determine the extent of the enlargement after TICAO. Results: Of 12 patients with CCAs, 10 had 12 coexisting aneurysms; 5 of the coexisting aneurysms (41.7%) showed enlargement during a mean follow-up period of 8.1 years, and all enlarged aneurysms were smaller of the bilateral CCAs; the larger CCA had been managed by TICAO. Five of 6 (83.3%) patients with bilateral CCAs showed enlargement of the contralateral aneurysm after TICAO. Two contralateral CCAs showed marked enlargement after TICAO and were subsequently treated with stent-assisted coil embolization. Conclusions: Contralateral, smaller aneurysms frequently enlarge after unilateral TICAO in patients with bilateral CCAs. The findings emphasize the importance of long-term observation after TICAO and appropriate interventions against enlarging contralateral aneurysms. Key Words: Therapeutic carotid occlusion—cavernous carotid aneurysm—stent-assisted coil embolization—enlargement. Ó 2015 by National Stroke Association
The emergence of flow-diverter stents has promised to revolutionize the treatment of cavernous carotid aneurysms (CCAs), and recent reports demonstrated the excellent clinical results and high rates of complete occlusion, given the ideal vessel characteristics of the cavernous segment of internal carotid artery (ICA) for flow diversion.1 Meanwhile, therapeutic ICA occlusion (TICAO) is
occasionally the safest and most effective method to alleviate the mass effect caused by CCAs.2,3 However, TICAO may predispose patients to long-term complications, including the formation of de novo aneurysms and enlargement of any coexisting aneurysms. Although several authors have conducted detailed characterizations of the de novo aneurysms following TICAO,4,5 the
From the Department of Neurosurgery, Brain Research Institute, Niigata University, Niigata, Japan. Received March 6, 2015; revision received April 11, 2015; accepted April 17, 2015. The authors declare that they did not receive any grant support. The authors declare that they have no conflicts of interest.
Address correspondence to Kazuhiko Nishino, MD, Department of Neurosurgery, Brain Research Institute, Niigata University, 1-757, Asahimachidori, Chuo-ku, Niigata 951-8585, Japan. E-mail: [email protected]. 1052-3057/$ - see front matter Ó 2015 by National Stroke Association http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2015.04.025
Journal of Stroke and Cerebrovascular Diseases, Vol. 24, No. 8 (August), 2015: pp 1865-1872
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enlargement of coexisting aneurysms after TICAO has rarely been documented.6-8 CCAs frequently coexist with intracranial aneurysms in other locations9,10 and sometimes arise from the bilateral ICA as mirror aneurysms.11,12 Therefore, it is important to clarify the possibility that coexisting aneurysms will enlarge after TICAO in CCA patients. If the contralateral aneurysm enlarged after unilateral TICAO in a bilateral CCA patient, the treatment decisions become particularly complicated. This study evaluated the growth potential of coexisting aneurysms following TICAO for the treatment of the CCAs. In addition, we provide a discussion of the treatment options for enlarging, coexisting aneurysms after TICAO.
Methods Eighteen patients with CCAs underwent TICAO at our institute between 1993 and 2011. Patients were excluded from the study if their coexisting aneurysms were treated after the TICAO, follow-up imaging had not been appropriately obtained, or the follow-up period was less than 2 years. Accordingly, 12 patients, including 10 women and 2 men (mean age, 64.2 years; range, 39-77 years), were included in this study. The clinical presentations included ophthalmoplegia (10 patients), visual disturbance (1), and asymptomatic (1). Five patients had preexisting hypertension. All patients underwent cerebral angiography to determine the exact location and configuration of the CCA and to detect coexisting intracranial aneurysms. In all cases, an intravascular balloon test occlusion (BTO) was performed to evaluate TICAO tolerance. For cases determined to be clinically intolerant of TICAO, high-flow bypass was indicated. Patients who were clinically tolerant, but had insufficient collateral circulation, underwent superficial temporal artery-middle cerebral artery (STA-MCA) bypass before TICAO. Patients were treated using TICAO alone, if their collateral flow was sufficient. After TICAO, patients underwent periodic radiographic evaluations using magnetic resonance angiography (MRA) or computed tomography angiography for more than 2 years. Using the follow-up images, we assessed thrombosis and shrinkage of the treated CCAs, recanalization of the occluded ICA, and the enlargement of coexisting aneurysms. The ethics committee at Niigata University School of Medicine approved this study, and informed consent was obtained from each patient.
Results Because all patients were determined to be clinically tolerant, none underwent high-flow bypass; 8 patients underwent TICAO and STA-MCA bypass, and 4 patients underwent TICAO alone. ICAs were therapeutically
occluded in the cervical portion in 4 patients, the petrous portion in 6, and the intracavernous portion (internal trapping) in 2. Used materials for the occlusion were as follows: detachable coils in 7 patients, detachable balloons in 4, and both in 1. The average follow-up period was 8.1 years (range, 3-16 years) after TICAO (Table 1). All treated CCAs showed thrombosis and shrinkage of the sac, and the 11 symptomatic patients showed clinical improvement (Fig 1). STA-MCA bypass was patent in all cases, and recanalization of the occluded ICA was not detected during the follow-up period. Neither disabling stroke nor aggravation of the mass effect occurred after the TICAO, regardless of whether they underwent bypass surgery. However, one patient (case 2) developed a hemiparesis 2 days after TICAO, and another patient (case 8) presented a motor aphasia 2 days later. Both cases responded to medical treatments, and ischemic symptoms resolved within a week. The hypertension was controlled during the follow-up period except for the periprocedural term in all 5 patients. Of the 12 patients, 10 (83.3%) had 12 coexisting aneurysms before TICAO. The aneurysm locations were variable (Table 1), including 6 contralateral CCAs, 2 MCA aneurysms, 1 anterior communicating artery aneurysm, 1 distal anterior cerebral artery aneurysm, 1 basilar artery aneurysm, and 1 vertebral artery aneurysm. The coexisting aneurysms ranged in diameter from 2 mm to 8 mm. Of the 12 coexisting aneurysms, 5 (41.7%) enlarged during the follow-up period; all 5 were smaller of bilateral CCAs and were contralateral to the TICAO-treated larger aneurysm. Thus, 5 of 6 (83.3%) patients with bilateral CCAs showed enlargement of the contralateral aneurysm after TICAO. Of these 5 cases, 4 patients had undergone TICAO with an STA-MCA bypass and one was managed with TICAO, alone. Although the degree and rate of the enlargement was inconsistent among the aneurysms, 2 cases showed marked enlargement to more than 15 mm in diameter (Table 1). Although these large aneurysms remained asymptomatic, they were treated with the stent-assisted coil embolization, resulting in the suppression of further enlargement.
Representative Cases Case 5 A 77-year-old woman presented with a 2-month history of diplopia. A neurologic examination revealed right oculomotor and abducens nerve palsies. Radiographic examinations demonstrated a large CCA on the right side and a small one (3 mm in diameter) in the posterior bend of the cavernous segment of the right ICA (Fig 2, A,B). The patient showed tolerance during the BTO, and collateral flow was considered to be sufficient. Thus, the ICA was occluded at the petrous portion using detachable coils without an STA-MCA bypass. Follow-up MRA demonstrated gradual enlargement of the left CCA, until it
TICAO Case Age/ No. sex
Coexisting aneurysm
Clinical symptoms
Treated aneurysm
Bypass
Site
Materials
Cervical ICA Cervical ICA
Coils, balloons Balloons
1 2
54/F 62/F
Ophthalmoplegia Visual disturbance
R CCA R CCA
STA-MCA STA-MCA
3 4 5 6 7
67/M 69/F 77/F 39/F 77/F
Ophthalmoplegia Ophthalmoplegia Ophthalmoplegia Ophthalmoplegia Ophthalmoplegia
L CCA R CCA L CCA L CCA L CCA
STA-MCA Petrous ICA STA-MCA Cervical ICA None Petrous ICA STA-MCA Petrous ICA None Cavernous ICA
8
68/F
Ophthalmoplegia
L CCA
STA-MCA
9 10 11 12
68/F 46/F 73/M 70/F
Ophthalmoplegia Ophthalmoplegia Asymptomatic Ophthalmoplegia
L CCA L CCA R CCA R CCA
STA-MCA Cavernous ICA STA-MCA Cervical ICA None Petrous ICA None Petrous ICA
Petrous ICA
Periprocedural Followcomplications up (y)
HT
Location/size
Outcome
Treatment
— Growth (2-5 mm)
— Observation
None Transient hemiparesis None None None None None
16 15
— None Treated L CCA/2 mm
14 9 8 7 7
Coils
Transient aphasia
6
— Treated — — — — —
None — BA/5 mm Stable R CCA/3 mm Growth (3-13 mm) R CCA/5 mm Growth (5-10 mm) Acom/2 mm Stable L MCA/5 mm Stable R CCA/8 mm Growth (8-15 mm)
— Observation Observation Observation Observation Observation SAC
Coils Balloons Coils Coils
None None None None
6 5 3 3
Treated Treated Treated —
R VA/6 mm Stable R ACA/3 mm Stable R CCA/8 mm Growth (8-17 mm) R MCA/4 mm Stable L CCA/2 mm Stable
Observation Observation SAC Observation Observation
Balloons Balloons Coils Coils Coils
BILATERAL CAVERNOUS CAROTID ANEURYSMS
Table 1. Patient characteristics, treatment, and coexisting aneurysms
Abbreviations: Acom, anterior communicating artery; ACA, anterior cerebral artery; BA, basilar artery; CCA, cavernous carotid aneurysm; F, female; HT, hypertension; ICA, internal carotid artery; L, left; R, right; M, male; SAC, stent-assisted coil embolization; STA-MCA, superficial temporal artery-middle cerebral artery; TICAO, therapeutic internal carotid artery occlusion; VA, vertebral artery.
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Figure 1. Case 12. Sequential changes of the aneurysm size after therapeutic internal carotid artery occlusion (TICAO). An angiogram obtained before the treatment shows a large right cavernous carotid aneurysm (CCA) (A). The petrous portion of the internal carotid artery was occluded by detachable coils (B). Serial magnetic resonance images (T1-weighted images) obtained after TICAO; 2 days (C), 3 months (D), and 1 year later (E). The CCA shows acute thrombosis and gradual shrinkage of the sac.
reached 13 mm diameter, 8 years after TICAO (Fig 2, C-E). Given that the aneurysm remains asymptomatic and the patient is an octogenarian, we have elected to keep the aneurysm under careful observation. Case 10 A 46-year-old woman presented with a 6-month history of diplopia, also demonstrating left abducens nerve palsy. Radiographic examinations revealed a large CCA on her left side and a smaller one (8 mm in diameter) in the right cavernous segment of the ICA (Fig 3, A,B). Because the patient showed insufficient collateral flow during the BTO, STA-MCA double bypasses were performed, and
the cervical ICA was occluded using detachable balloons. Follow-up MRA demonstrated gradual enlargement, and angiograms obtained 4 years after TICAO revealed marked enlargement of the aneurysm to a diameter of 17 mm, although the aneurysm remained asymptomatic (Fig 3C). The patient underwent stent-assisted coil embolization to avoid the occlusion of her right ICA, suppressing further enlargement (Fig 3D).
Discussion The emergence of flow-diverter stents may be considered one of the biggest breakthroughs in the management
Figure 2. Case 5. An angiogram (A) and magnetic resonance angiography (MRA) (B) obtained before initial treatment. A large right cavernous carotid aneurysm (CCA) is seen. Note a small aneurysm on the posterior bend of the left cavernous segment of the internal carotid artery (ICA; arrow in B). Serial MRA obtained after therapeutic ICA occlusion; 2 years (C), 4 years (D), and 8 years later (E). The left CCA shows gradual enlargement up to 13 mm in diameter.
BILATERAL CAVERNOUS CAROTID ANEURYSMS
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Figure 3. Case 10. Angiograms obtained before initial treatment; left internal carotid angiography (ICAG) (A), right ICAG (B). A large left cavernous carotid aneurysm (CCA) is seen (A). Note an aneurysm in the right cavernous segment of the internal carotid artery (ICA; arrow in B). Right ICAG obtained 4 years after therapeutic ICA occlusion with a bypass surgery demonstrates marked enlargement of the right CCA (C). Right ICAG obtained after stentassisted coil embolization (D).
of CCAs, and its use seems to be rapidly growing and moving toward the mainstream of CCA treatment.1,13 Meanwhile, TICAO with bypass surgery has been traditionally considered the safest and most effective method to alleviate the mass effect caused by CCAs, and many case series have demonstrated excellent treatment results.7,14 However, TICAO has a potential risk of long-term complications including de novo aneurysm formation and enlargement of coexisting aneurysms. According to a review article, more than 500 patients with CCA underwent TICAO plus or minus bypass surgery since 1990.15 However, the evaluation for TICAO-related complications was conducted in periprocedural term in almost all articles, and follow-up period was relatively shorter compared with the present study (8.1 years of mean follow-up period). In addition, there are few descriptions about the presence or absence of coexisting aneurysms, despite CCAs are considered to frequently have accompanying aneurysms in other locations. In the present study, we thoroughly examined the presence of aneurysms coexisting with CCAs, including very small aneurysms (,2 mm in diameter), and carefully evaluated the subsequent imaging data to detect the enlargement of the aneurysms over a long period. Interestingly, 50% (6 of 12) of CCA patients had an additional aneurysm arising from contralateral
cavernous segment of ICA as mirror aneurysms, and all the aneurysms that enlarged after unilateral TICAO were the smaller of the bilateral CCAs. We found 7 articles describing the enlargement of coexisting aneurysms after TICAO or therapeutic common carotid artery occlusion (Table 2).6-8,16-19 Among the 9 cases, 6 had bilateral CCAs and the enlargement occurred after parent artery occlusion for the contralateral aneurysms, as in our cases. Therefore, these observations suggest that contralateral aneurysms of bilateral CCAs are more likely to enlarge after unilateral TICAO than aneurysms in other locations. Regarding the growth mechanism of contralateral CCA after unilateral TICAO, hemodynamic stress on the wall of contralateral ICA is the most likely cause, because contralateral ICA would function as main source of collateral blood flow following TICAO. The expected advantages of the bypass surgery associated with TICAO are not confined to the prevention of brain ischemia, but also the reduction of the hemodynamic stress on collateral pathways. Although most cases listed in Table 2 underwent TICAO alone, we actively performed the bypass surgery before TICAO. However, our results indicated that the bypass surgery was unlikely to prevent the enlargement of aneurysms arising from this specific location.
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Table 2. Series of enlargement of coexisting aneurysms after therapeutic ICA or common carotid artery occlusion Initially treated aneurysm Age/ sex
Location
de Morais et al,16 1978 42/F
L CCA
Faria et al,17 1980
41/F
Fujiwara et al,18 1993
Authors and year
Treatment
Enlarged coexisting aneurysm Location
Treatment
L common carotid artery occlusion
R CCA
R CCA
R common carotid artery occlusion
L CCA
54/F
R CCA
L CCA
?/?
ICA
R ICA partial occlusion with EC-IC bypass Common carotid artery occlusion
R common carotid artery occlusion L common carotid artery occlusion —
Larson et al,7 1995 Niiro et al,19 2000
58/? 52/M
ICA L CCA
Clarenc¸on et al,6 2011 Matouk et al,8 2012
50/F 52/F
L CCA CCA
Petrous ICA occlusion with balloons L cervical ICA occlusion with a vascular clamp L petrous ICA occlusion with coils Intracranial ICA occlusion
Present series case 2 Case 5 Case 6 Case 8 Case 10
39/M 62/F 77/F 39/F 68/F 46/F
CCA R CCA L CCA L CCA L CCA L CCA
Intracranial ICA occlusion R ICA occlusion with STA-MCA bypass L ICA occlusion L ICA occlusion with STA-MCA bypass L ICA occlusion with STA-MCA bypass L ICA occlusion with STA-MCA bypass
Contralateral — intradural ICA Acom Clipping R CCA R ICA occlusion with high-flow bypass R CCA Flow-diverter stents Contralateral — CCA BA — L CCA Observation R CCA Observation R CCA Observation R CCA SAC R CCA SAC
Abbreviations: Acom, anterior communicating artery; BA, basilar artery; CCA, cavernous carotid aneurysm; EC-IC, extracranial-intracranial; F, female; ICA, internal carotid artery; L, left; R, right; M, male; SAC, stent-assisted coil embolization; STA-MCA, superficial temporal arterymiddle cerebral artery.
On the other hand, Burns et al20 reported that CCAs showed a higher frequency of spontaneous enlargement than aneurysms arising from other locations, with a frequency that reached 31.6% (6 of 19) over a median 47-month follow-up period. In addition, several authors speculated that congenital factors might have played a role for the pathogenesis of CCAs, considering the predominant occurrence in female patients, the dysplastic nature of the aneurysm, and an association with genetic disorders, including Marfan syndrome, fibromuscular dysplasia, and polycystic kidney.21-23 These findings indicate that CCA is likely to have a different growth potential from aneurysms in other locations, although the growth after TICAO might be triggered by the hemodynamic alteration following TICAO. With respect to the treatment choice, our results indicate that a deliberate strategy is required for treating patients with bilateral CCAs. First, when treating the larger, symptomatic aneurysms, a decision as to whether the ICA should be occluded is critical. Flow-diverter stents are theoretically ideal devices for preserving blood flow in parent vessels and avoiding coil deployment into the aneurysmal lumen. However, if the configuration of cavernous segment of the ICA is unsuitable for the use of flow-diverter stents, its use has a potential risk of serious complications. In addition, there are no data available regarding a long-term efficacy of the treatment with
flow-diverter stents. Considering that a CCA is not a lifethreatening disease, the safety of the treatment should be as high as possible. We believe that TICAO with bypass surgery is occasionally a safe procedure for the management of the symptomatic CCA, providing patients with long-term stability. The second issue is how to treat if the contralateral aneurysm enlarged to a critical size. In case of a patient who had undergone unilateral TICAO, it must be essential to preserve the remaining ICA. The use of flowdiverter stents seems to be ideal in this situation. We performed stent-assisted coil embolization in 2 patients who showed marked enlargement (to .15 mm) of the contralateral aneurysm, despite remaining asymptomatic. Although this option is less effective for symptoms caused by mass effect,24-26 several studies have demonstrated favorite clinical outcomes following stentassisted coil embolization of asymptomatic CCAs.27,28 With respect to this critical size, Choulakian et al24 mentioned that the mean size of CCAs presenting with cranial nerve palsies was 17 mm, in their series of 113 patients. The data should be considered as reference values for decisions on the timing of treatments for enlarging aneurysms. It is naturally important to perform careful follow-up even after the stent-assisted coil embolization, because this procedure tends to be incomplete packing of coils. In the cases that enlarged aneurysms
BILATERAL CAVERNOUS CAROTID ANEURYSMS
had unfavorable configuration for endovascular procedures, therapeutic occlusion of the remaining ICA, in combination with bypass surgery, might be an alternative treatment option for a growing contralateral aneurysm. However, the strategy entails the potential risk of ischemic complications because it results in bilateral ICA occlusion. In addition, such a hemodynamic situation is likely to increase the hemodynamic stress on the vertebrobasilar system that functions as a collateral pathway, increasing the potential risk of de novo aneurysm formation in the basilar artery, posterior cerebral artery, or posterior communicating artery.29,30 The limitations of the present study include the small sample size, retrospective design, and possible selection bias. In addition, we do not have comparable data for patients with untreated bilateral CCAs. We could not also find articles describing the natural course of bilateral CCAs with long-term follow-up. If valuable studies were conducted to demonstrate the natural course of bilateral CCA, they would contribute to identify how unilateral TICAO has an influence on the enlargement of contralateral CCA.
1871
7.
8.
9.
10.
11.
12.
13.
Conclusions In 83% of bilateral CCA cases, a smaller, contralateral aneurysm enlarged after a unilateral TICAO for a larger CCA aneurysm, and the bypass surgery did not prevent the enlargement. The findings indicate that surgeons should have a deliberate strategy to manage bilateral CCA cases. Additionally, careful follow-up after TICAO is essential for determining the appropriate treatment option and the timing for treating enlarging contralateral aneurysms.
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1872 carotid fibromuscular dysplasia. J Neurol Neurosurg Psychiatry 1983;46:284-285. 24. Choulakian A, Drazin D, Alexander MJ. Endosaccular treatment of 113 cavernous carotid artery aneurysms. J Neurointerv Surg 2010;2:359-362. 25. Kim LJ, Tariq F, Levitt M, et al. Multimodality treatment of complex unruptured cavernous and paraclinoid aneurysms. Neurosurgery 2014;74:51-61. 26. van Rooij WJ, Sluzewski M. Unruptured large and giant carotid artery aneurysms presenting with cranial nerve palsy: comparison of clinical recovery after selective aneurysm coiling and therapeutic carotid artery occlusion. AJNR Am J Neuroradiol 2008;29: 997-1002.
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