Management strategy of surgical and endovascular treatment of unruptured paraclinoid aneurysms based on the location of aneurysms

Clinical Neurology and Neurosurgery 128 (2015) 72–77

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Management strategy of surgical and endovascular treatment of unruptured paraclinoid aneurysms based on the location of aneurysms Se-yang Oh a , Kwan Sung Lee b , Bum-soo Kim c , Yong Sam Shin b,∗ a

Department of Neurosurgery, Inha University School of Medicine and Hospital, Incheon, Republic of Korea Department of Neurosurgery, Seoul St. Mary’s Hospital, Catholic University of Korea, Seoul, Republic of Korea c Department of Radiology, Seoul St. Mary’s Hospital, Catholic University of Korea, Seoul, Republic of Korea b

a r t i c l e

i n f o

Article history: Received 6 September 2014 Received in revised form 21 October 2014 Accepted 9 November 2014 Available online 15 November 2014 Keywords: Paraclinoid aneurysm Endovascular treatment Microsurgical treatment

a b s t r a c t Objective: Advances in endovascular treatment (EVT) have greatly improved the treatment outcomes of paraclinoid aneurysms. However, EVT had the shortcoming of durability and thromboembolic complications. As well, surgical treatment of paraclinoid aneurysms is still challenging due to the complexity of adjacent structures. The objective of this study is to report our experience with a combined surgical and endovascular treatment of unruptured paraclinoid aneurysms based on the location of aneurysms. Methods: A retrospective review was conducted of 185 cases of unruptured paraclinoid aneurysms that underwent surgical or endovascular treatment between September 2008 and August 2012. Thirty-one aneurysms (16.8%) were treated by microsurgery and 154 (83.2%) were treated by EVT. Fifty aneurysms (27.0%) were classified to the dorsal group and 135 (73%) were classified to the non-dorsal group. Results: Twenty of 50 dorsal group aneurysms (40%) were treated by microsurgery while 124 of 135 nondorsal group aneurysms (91.9%) underwent an EVT. The rate of complete occlusion was 96.8% in surgical series and 60.4% in EVT (P < 0.001). Recanalization occurred in 9 aneurysms (5.8%) of EVT and 1 aneurysm (3.2%) of surgical series (P = 0.360). In non-dorsal group, transient complications (10 aneurysms (5.4%), P = 0.018) and morbidity at last visiting (6 aneurysms (3.2%), P = 0.021) were more present in surgically treated cases rather than in EVT cases. Diplopia and visual field defect occurred in the non-dorsal group only; in 2 of 11 surgical cases (18.2%) and in 1 of 124 EVT series (0.8%) (P = 0.017). The overall rate of excellent or good clinical outcomes (Glasgow outcome scale 5 or 4) was 98.9%. Conclusion: EVT is a safe and effective treatment for the non-dorsal group. Based on angiographic and clinical aspects, microsurgical clipping has prior efficacy with better outcomes in the dorsal group under proper individualized selection. © 2014 Published by Elsevier B.V.

1. Introduction Paraclinoid aneurysms have been defined as intracranial aneurysms that arise from the internal carotid artery (ICA) between the site of its exit from the roof of the cavernous sinus and the origin of the posterior communicating artery [1–3]. Because of the

Abbreviations: EVT, endovascular treatment; ICA, internal carotid artery; ACP, anterior clinoid process; 3D, 3-dimensional; CTA, computed tomography angiography; MRA, magnetic resonance angiography; DSA, digital subtraction angiography; GOS, Glasgow outcome scale. ∗ Corresponding author at: Department of Neurosurgery, Seoul St. Mary’s Hospital, 222 Banpo-daero, Seocho-gu, Seoul 137-701, Republic of Korea. Tel.: +82 10 8703 4289; fax: +82 2 594 4248. E-mail address: [email protected] (Y.S. Shin). http://dx.doi.org/10.1016/j.clineuro.2014.11.008 0303-8467/© 2014 Published by Elsevier B.V.

close relationship to the complexity of adjacent structures such as skull base including anterior clinoid process (ACP), cavernous sinus and critical cranial nerves, surgical treatment of paraclinoid aneurysms remains a technical challenge to many neurosurgeons [1,2,4–8]. The Unruptured Cerebral Aneurysm study of Japanese investigators reported that the risk for a rupture of ICA aneurysm excluding posterior communicating artery and cavernous portion was statistically low compared with the aneurysms located in the anterior communicating or posterior communicating arteries [9]. Owing to their rare incidence of rupture, the indication for the treatment of unruptured paraclinoid aneurysms would be focused on safety. Since the advent of endovascular techniques, excellent results with coil embolization of paraclinoid aneurysms have been reported especially for those lesions with high surgical risk [6,10–13]. However, endovascular treatment (EVT) of aneurysms

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has been considered as associations with significant problems were faced such as durability of obliteration, thromboembolic complications and hemorrhagic complications related with antithrombotic medications [14–16]. Some reports presented a multidisciplinary approach of microsurgery and EVT for the treatment of paraclinoid aneurysms [6,7,12,17,18]. Considering the procedure related risks of unruptured paraclinoid aneurysms, it is important to identify the proper indication as well as to select safe and effective methods for treatment. We applied a more simplified classification based on anatomic relations for the treatment of paraclinoid aneurysms. The purpose of the present study was to assess the outcomes under the multidisciplinary treatment based on a simplified classification. 2. Materials and methods 2.1. Patient population Between September 2008 and August 2012, 185 saccular paraclinoid aneurysms in 176 patients were treated at our institute. The medical records and angiographic data of the patients were retrospectively reviewed. This study was approved by the institutional review board at Catholic Medical Center Office of Human Research Protection Program, Seoul, Republic of Korea (Study No. KC14RISI0147). The pre- and postoperative workup included 3-dimensional (3D) computed tomography angiography (CTA) and magnetic resonance angiography (MRA). Digital subtraction angiography (DSA) was performed in all cases for to confirm the diagnosis and classification. Dual reconstruction technique of 3D DSA was also simultaneously performed to evaluate the relation to the adjacent skull base structure including anterior clinoid process, optic strut and dural ring. Blister-like aneurysms were excluded under angiographically suspected or diagnosed under microsurgical field. 2.2. Classification of aneurysms One hundred eighty-five saccular paraclinoid aneurysms were selected and divided into two groups, according to a simplified modification of previously proposed classifications [19–21]. (1) Dorsal group aneurysms are classified as followed: the neck of aneurysms originates from the superior location of the paraclinoid segment of ICA and the dome project to an anterior or superior direction. The aneurysms that arose from the origin of the ophthalmic artery, so called true ophthalmic aneurysms were also included into the dorsal group. (2) Non-dorsal group aneurysms are classified as follows: the neck of aneurysms originates from inferior, medial or lateral wall of paraclinoid ICA and the dome projects to any direction except anterior or superior direction. Aneurysm size was categorized by the International Study of Unruptured Intracranial Aneurysms (ISUIA) criteria (small, <10 mm; large, 10 to <25 mm; giant, ≥25 mm). To reduce the selection bias, formal angiograph reading, including determination of aneurysm size and location, were conducted by the same neurointerventional radiologist. 2.3. Therapeutic strategy and follow-up Our multidisciplinary team applied the indication for paraclinoid aneurysm following considerations. For medial or ventral paraclinoid aneurysms, EVT was firstly indicated because of the surgical difficulties. However, some large or giant aneurysms that presented with mass effect or predicted to incomplete packing due to wide neck or irregular shape were indicated to microsurgery. For dorsally located paraclinoid aneurysms, microsurgery was indicated if an easily surgical access such as less required extensive

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resection of the ACP was predicted due to pre-operative radiologic studies such as CTA with bone reconstruction and dual reconstruction images of 3D DSA containing bony structures. In addition, if an ophthalmic artery originated from the aneurysmal sac, a microsurgery was preferred to save the branch. In some dorsally located aneurysms, EVT was indicated if the patients were old or clinically deteriorated or a complete packing could be easily achieved. A standard pterional craniotomy was performed for microsurgery of dorsal group aneurysms. For common or internal carotid artery exposure, a sterile draping on the ipsilateral neck was performed on all indicated patients. Before craniotomy, ICA exposure was routinely performed for the extracranial proximal control using temporary clipping. The ACP, the optic canal and optic strut were removed extradurally or intradurally if the needs were proved on dual reconstruction 3D DSA images. The patients for EVT received proper antiplatelet medications for 5–7 or more days before the procedures. EVT was performed under general anesthesia. Standard co-axial technique using a 6- or 7-french guiding catheter was performed, and the patients received systemic heparinization during the procedure. When a remodeling technique was needed, a non-detachable balloon or self-expandable stent was applied. Angiographic results were evaluated with the modified Raymond grading system: class 1, complete obliteration; class 2, residual neck; or class 3, residual sac [10,22]. We checked the routine follow-up imaging in all objective patients at 6 months. MRA was performed to evaluate a recanalized aneurysm after EVT and CTA was performed to evaluate the post-clipping status. An early check-up of DSA was indicated if the patients were suspected for recurrence. “Major recanalization” was defined as a contrast filling within the aneurysm dome or significant coil compaction, and “Minor recanalization” was defined as a minimal coil compaction at the aneurysm neck. Clinical outcomes at discharge and last visits on the out-patient status were evaluated with the Glasgow outcome scale (GOS). A “transient complication” was defined if the complication did not affect the clinical status at discharge, or trivial symptoms were only occurred during a brief period. 2.4. Data analysis All statistical analysis was performed using SPSS Statistics 18th version for Windows (SPSS, Inc., an IBM Company, Chicago, IL, USA). Student’s t-test was used for continuous variables and the chi-square test or Fisher’s exact test was as appropriate used for categorical variables. Statistical significance was defined as a P-value <0.05% for a 95% confidence interval. 3. Results 3.1. Patient demographics The baseline characteristics of study subjects are presented in Table 1. The patients included 148 women (84.1%) and 28 men (15.9%) with a mean age of 53.7 ± 11.0 years (range, 28–81). Multiple aneurysms were found in 49 patients (27.8%). Eight of 176 patients (4.6%) had visual symptoms caused by paraclinoid aneurysms. The other 168 patients (95.4%) were diagnosed due to incidental findings; headache, dizziness, minor head trauma, evaluation for other intracranial lesion and routine medical check etc. Thirty-one aneurysms (16.8%) were treated by microsurgery while 154 (83.2%) were treated by EVT. Based on our proposed classification, 50 aneurysms (27.0%) were included in the dorsal group and 135 (73%) were included in the non-dorsal group. Nine aneurysms (4.9%) were raised from the origin of the ophthalmic artery. In the

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Table 1 Characteristics of 176 patients with 185 paraclinoid aneurysms.

Patients Female Male Average age (years) Presenting symptoms Incidental Visual field defect Diplopia Aneurysms Size of aneurysms (mm) <5 5 to <10 10–25 >25

Total

Dorsal group

176 148 28 53.7

49 39 10 53.6

27.8% 79.6% 20.4%

127 109 18 53.7

72.2% 85.8% 14.2%

84.1% 15.9%

Non-dorsal group

168 5 3 185

95.4% 2.9% 1.7%

47 1 1 50

95.9% 2.0% 2.0% 27.0%

121 4 2 135

95.3% 3.1% 1.6% 73.0%

27 142 15 1

14.6% 76.8% 8.1% 0.5%

5 20 5 1

16.1% 64.5% 16.1% 3.2%

22 122 10 0

14.3% 79.2% 6.5% 0.0%

dorsal group, 20 aneurysms (40.0%) were treated by microsurgery while 30 (60.0%) were treated by EVT. In the non-dorsal group, 11 aneurysms (8.1%) were treated by microsurgery while 124 (91.9%) were treated by EVT (P < 0.001). Clinical and radiological follow-up was available for all patients with a mean period of 27.1 months (range: 6–58 months). Statistical differences of follow-up periods were not shown between the microsurgery groups (26.3 months) and the endovascular treatment groups (27.3 months). 3.2. Angiographic outcomes Angiographic outcomes after treatment in each subgroup are summarized in Table 2. The mean follow-up period for aneurysms without recanalization (175 aneurysms, 94.6%) was 26.6 months, compared for 28.1 months for aneurysms with recanalization (10 aneurysms, 5.4%) (P = 0.378). Two, four, two, and two aneurysms recanalized within 12 months, between 13 and 24 months, between 25 and 36 months, and after 36 months, respectively. All 31 aneurysms treated by microsurgery achieved complete obliteration of aneurysms without residual sac confirmed by CTA within 2 weeks after surgery. Nine aneurysms (5.8%) of EVT and 1 (3.2%) of surgical series presented with major and minor recanalization during the follow-up period were presented (P = 0.360). The overall rate of complete occlusion was 96.8% (30 of 31 aneurysms) in surgical series and 60.4% (93 of 185 aneurysms) in EVT series (P < 0.001). Only 1 microsurgically treated aneurysm presented contrast-filling on follow-up angiography. The aneurysm was classified to the non-dorsal group. The aneurysm was additionally treated by coil embolization immediately after follow-up angiography. In 154 aneurysms treated by EVT, complete occlusions were present in 93 aneurysms (60.4%), residual necks were present in 46 (29.9%), and residual sacs were present in 15 aneurysms (9.7%). The rate of occlusion presented no statistical difference between the dorsal group and the non-dorsal group. Major recanalizations were occurred in 2 aneurysms on follow-up MRA and DSA. One case was included in the dorsal group. An intentionally incomplete packing was demanded for the saving of the ophthalmic artery originated from the neck of aneurysm. The other case, a ventrally located large aneurysm, was included into the non-dorsal group. For this aneurysm was initially accomplished a complete occlusion; however, the 1-year-follow-up angiography showed a major recanalization. The two aneurysms were re-treated by additional coiling. The other 7 aneurysms only showed a minor recanalization. The maximal sac diameter (P = 0.297), neck diameter (P = 0.691), dome-to-neck ratio (P = 0.193), and complex shape (P = 0.601) were not found to significantly influence recanalization.

3.3. Clinical outcomes Overall complication rates in the subgroups of aneurysms are summarized in Table 3. Overall rate of excellent or good (GOS 5 or 4) clinical outcomes was 98.9%. The statistical difference of clinical outcomes between two groups and certain treatment series was not shown. Transient complications presented in 10 of all enrolled cases (5.4%). Statistical differences were not shown between surgically treated and EVT (P = 0.187), dorsal group and non-dorsal group (P = 0.453) and surgically treated and EVT in dorsal group (P = 0.207). However, surgically treated aneurysms in the non-dorsal group exhibited statistical significance on transient complications rather than EVT cases (3 aneurysms (27.3%) versus 5 (4.0%), P = 0.018). Major complications affecting GOS at discharge or during the over one-year-follow-up occurred in 6 aneurysms (11.6%). Surgically treated aneurysms in the non-dorsal group were statistically more influenced due to transient complications rather than EVT cases (2 aneurysms (18.2%) versus 2 (1.6%), P = 0.008). The rate of morbidity at last visiting occurred in 3 cases (1.6%). These cases were in the non-dorsal group. Two aneurysms were treated by surgery (18.2%), and the other aneurysm was treated by EVT (0.8%, P = 0.021). Among twelve ischemic events, 10 cases occurred in EVT series and 2 cases occurred in surgical series (6.4% versus 6.6%, P = 0.604). No statistical difference between locations of aneurysms was exhibited (4 of 30 (13.3%) in the dorsal group versus 6 of 124 (4.8%) in the non-dorsal group (4.8%), P = 0.454). In addition, a statistical difference between surgery and EVT under the groups was also not exhibited. Hemorrhagic complications occurred in 2 of 11 surgical cases (18.2%) and in 2 of 124 EVT series (1.6%) in the non-dorsal group (P = 0.033). Hemorrhagic complications did not occur in the dorsal group. Two surgical cases presented with intracranial hemorrhage that occurred during the post-operative period. One EVT case presented with subarachnoid hemorrhage due to an intraprocedural rupture of the aneurysm and the remaining one EVT case presented with an intracranial hemorrhage occurred at 1 month after stent-assisted coiling. Two EVT cases presented trivial symptoms; however, the other two surgical cases required additional surgery or intervention and presented a morbidity affecting the GOS. Diplopia and visual field defect occurred in 2 of 11 surgical cases (18.2%) and in 1 of 124 EVT series (0.8%) in the non-dorsal group (P = 0.017). All three cases belonged to the non-dorsal group and were located at the ventral side of the ophthalmic segment of ICA. Two cases presented with diplopia due to a 6th nerve palsy; one case was treated by stent-assisted coiling of large aneurysm and the other case was treated by clipping. One case presented with

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Table 2 Angiographic outcomes after microsurgery and endovascular treatment. Total

Post-procedural result Rate of complete occlusion Class 1 (complete) Class 2 (residual neck) Class 3 (residual sac) Last-F/U result Rate of complete occlusion Class 1 (complete) Class 2 (residual neck) Class 3 (residual sac) Recanalization Required re-treatment

P value

Micro-surgery

EVT

31 (100%)

101 (65.6%) 101 (65.6%) 39 (21.1%) 14 (7.6%)

30 (96.8%) 30 (96.8%)

93 (60.4%) 93 (60.4%) 46 (29.9%) 15 (9.7%) 9 (5.8%) 2 (1.3%)

1 (3.2%) 1 (3.2%) 1 (3.2%)

Dorsal group

P value

Micro-surgery

EVT

<0.001

20 (100%)

16 (53.3%) 16 (53.3%) 7 (23.3%) 7 (23.3%)

<0.001

20 (100%)

14 (46.7%) 14 (46.7%) 9 (30.0%) 7 (23.3%) 2 (6.7%) 1 (3.3%)

0.360 0.425

0 (0%) 0 (0%)

visual field defect after clipping of aneurysm. The symptoms were improved for all three cases within 6 month during the follow-up period.

4. Discussion In the literatures, paraclinoid aneurysm accounted for approximately 1.5–11% of all intracranial aneurysms [23–25]. The number of hospitalizations associated with unruptured aneurysms increased between 1996 and 2007 [26,27]. The trend was associated with advances in EVT. Another study noted the trend that EVT has been increased from 1997 to 2008 [12]. With the increasing trend of EVT of paraclinoid aneurysms, several case series reported that paraclinoid aneurysms could be safely and efficaciously performed in the elective setting [11,13,18,28]. However, a debate continued over some points such as durability, thromboembolic complications and problems related to the antiplatelet medications at the present stage of EVT. Microsurgical treatment of paraclinoid aneurysms has been associated with high morbidity owing to the difficulty of safe intracranial approach and proximal control such as anterior clinoidectomy [1,2,4,7,29,30]. However, the development of radiographic techniques such as 3D CTA and dual reconstruction technique of 3D DSA provide information to choose the appropriate treatment. Furthermore, the accumulation and improvement of helpful techniques for microsurgery such as transient hypothermia, neurophysiologic monitoring,

Non-dorsal group

P value

Micro-surgery

EVT

<0.001

11 (100%)

85 (68.5%) 85 (68.5%) 32 (25.8%) 7 (5.6%)

<0.001

<0.001

10 (90.9%)

<0.001

0.355 0.600

1 (9.1%) 1 (9.1%) 1 (9.1%)

79 (63.7%) 79 (63.7%) 37 (29.8%) 8 (6.5%) 7 (5.6%) 1 (0.8%)

0.544 0.157

intraoperative angiography and retrograde suction-decompression technique etc. have produced advanced results in microsurgery [5,31,32]. In this respect, combined and complementary treatment of paraclinoid aneurysm through multidisciplinary neurovascular team approach contained microsurgery and EVT are important. Some studies reported good outcomes in the management of paraclinoid aneurysms by a combined neurovascular team approach [6,7,11,12,17,18]. In these reports, although the morbidity and clinical outcomes were variable, the occlusion rates have been improved for both microsurgery and EVT more recently. In our study were found 65.6% of complete occlusion as initial result of EVT and 100% as initial result of microsurgery. The recent follow up result reported 94.2% stable status of embolization of EVT and 96.8% of microsurgery. The occlusion rates and follow up results of the present study showed more advanced angiographic outcomes compared with some previous reports or were comparable with other series. In early surgical-series, paraclinoid aneurysms were classified due to a method reported by al-Rodhan, Day or Barami et al. [4,19,30]. With this methods, paraclinoid aneurysms were divided to five or six subgroups; superior hypophyseal; ventral; origin of the ophthalmic artery; carotid cave; transitional cavernous and intracavernous. This old classification was based on the surgical anatomy between the extensions of aneurismal sac and adjacent anatomic components for anatomic exposure or clip selection. In respect of angiographic correlation, the terminologies had some impreciseness to apply the indications and to select the proper

Table 3 Clinical outcomes according to the Glasgow outcome scale. Total

Initial outcomes (GOS at discharge) 5 (Good) 4 (Disabled but independent) 3 (Conscious but disabled) 2 (Persistent vegetative) 1 (Death) Overall outcomes (GOS at last F/U) 5 (Good) 4 (Disabled but independent) 3 (Conscious but disabled) 2 (Persistent vegetative) 1 (Death) Overall rate of complications Transient complication (not affecting GOS) Morbidity (affecting GOS at discharge) Permanent disability GOS, Glasgow outcome scale.

P value

Micro-surgery

EVT

28 (90.3%) 2 (6.5%) 1 (3.2%) 0 (0%) 0 (0%)

151 (98.1%) 2 (1.3%) 1 (0.6%) 0 (0%) 0 (0%)

29 (93.5%) 1 (3.2%) 1 (3.2%) 0 (0%) 0 (0%) 6 (19.4%) 3 (9.7%)

153 (99.4%) 0 (0%) 1 (0.6%) 0 (0%) 0 (0%) 10 (6.4%) 7 (4.5%)

Dorsal group

P value

Micro-surgery

EVT

19 (95.0%) 1 (0.5%) 0 (0%) 0 (0%) 0 (0%)

29 (96.7%) 1 (3.3%) 0 (0%) 0 (0%) 0 (0%)

0.084 0.187

20 (100%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%)

30 (100%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 4 (13.3%) 3 (10.0%)

0.160

Non-dorsal group

P value

Micro-surgery

EVT

9 (81.8%) 1 (9.1%) 1 (9.1%) 0 (0%) 0 (0%)

122 (98.4%) 1 (0.8%) 1 (0.8%) 0 (0%) 0 (0%)

0.363 0.207

9 (81.8%) 1 (9.1%) 1 (9.1%) 0 (0%) 0 (0%) 5 (45.5%) 3 (27.3%)

123 (99.2%) 0 (0%) 1 (0.8%) 0 (0%) 0 (0%) 7 (5.6%) 5 (4.0%)

0.645

0.089

0.008

0.999

0.021

0.007 0.018

3 (9.7%)

3 (1.9%)

0.160

1 (0.5%)

1 (3.3%)

0.645

2 (18.2%)

2 (1.6%)

0.008

2 (6.5%)

1 (0.6%)

0.089

0 (0%)

0 (0%)

0.999

2 (18.2%)

1 (0.8%)

0.021

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method for EVT. Therefore, in more recent studies, authors adopted a simple classification based on the angiographic location or direction of the aneurysms [17,18,33]. The authors supposed that the classifications based on angiography were helpful for choosing the shape of microcatheter. However, the new classifications still had three or four subgroups and still had shortcomings with individual differences of each patient. We applied a more simplified classification under two categories. In our angiographic and clinical results and other reports using multidisciplinary approach [17,18], this modified classification has an advantage for choosing the treatment methods between microsurgery and EVT. In previous studies concerning the EVT of dorsally located aneurysms (so called superior or anterior wall aneurysms), a lower occlusion rate and more technical failure were reported compared to other paraclinoid aneurysms [7,10,33]. In early stage of EVT, Roy at el. reported that the rate of complete occlusion of dorsally located aneurysms was only 20%, whereas it was 85% in other groups of aneurysms [10]. After using the balloon remodeling technique, Iihara et al. reported that 15 dorsally located paraclinoid aneurysms treated by coiling presented with unfavorable outcomes than other subgroups; 50% occlusion rate of Raymond class 1 or 2, 6.7% technical failure and 13.3% thromboembolic complications. The suggested reasons were that dorsally located aneurysms have unfavorable aneurysmal geometries such as wider neck with unfavorable dome-to-neck ratio and microcatheter instability associated with abrupt curvature of the carotid siphon [7,34]. For similar reasons, the relatively high rate of recurrence after EVT has been reported [11,15]. In the recent study of Yeon et al., although occlusion rate was improved (63.9% of Raymond class 1 or 2), a stent-assisted embolization was more frequently performed than in other groups. Similarly, in the present study, the occlusion rate of Raymond class 1 or 2 was 76.7% and the rate of recanalization was 6.7% for 30 dorsal group aneurysms treated by EVT. Stent-assisted techniques were used in 20 aneurysms (66.6%). In both the dorsal and the non-dorsal group, the ischemic and hemorrhagic complications after EVT were concerned with stent-assisted coiling. The results concerning EVT presented statistical differences between the dorsal group and the non-dorsal group and presented compatible outcomes with other studies of paraclinoid aneurysms also [12,17,33]. A recanalization after EVT due to insufficient packing is still an important problem in the aspect of durability, in the dorsal group of paraclinoid aneurysms as well as in the non-dorsal group. This is important because paraclinoid aneurysms tend to have two anatomical factors, wide necks and large size that adversely affect the anatomical outcome and the long-term durability of the result after EVT [14,35]. Boet et al. suggested that greater shear hemodynamic stresses at the region of the carotid siphon may slow intimal overgrowth, resulting in high rates of recurrence in the EVT, particularly if the initial occlusion was incomplete [11]. Some reports also noted the problems with higher rates of recurrence associated with an incomplete initial occlusion [16,22,36]. Factors such as wide neck, larger size, an ophthalmic artery originating from the aneurysm neck, and difficult geometry preventing a stable approach with a microcatheter are closely related to incomplete packing and recanalization of paraclinoid aneurysms. In order to increase the occlusion rate, multiple stent or balloon-assisted embolization, endovascular or surgical trap with bypass, or a flowdiverting device should be considered [37–39]. Surgical treatment for aneurysms of the non-dorsal group, especially for ventral aneurysms continues to be challenging and technically difficult. In the literature, the anatomic location that was partly originated intradural and partly intracavernous has been described as the main reason [8,40]. The possibility of incomplete clipping would be increased for the clipping of larger sized aneurysms because of contact between the clip blade and the

adjacent bony structures [7]. In the current report, microsurgically treated aneurysms in the non-dorsal group presented more transient complications and morbidity rather than in EVT series. From a practical view of safety and convenience and in accordance with current and previous reports, we suggest that large or giant non-dorsal paraclinoid aneurysms should be preferred for EVT. In addition, the aneurysms that were considered with a low risk of rupture with small size, a smooth shape without lobulation and daughter sac and a low dome-to-neck ratio should be managed in conservative manners such as with close observation and followup. After the advent of flow-diverting devices, the aneurysm treatment changed rapidly. Flow-diverting devices are a significant advance in endovascular remodeling strategies for aneurysm treatment and have been reported excellent results [38,39,41]. The benefits of flow-diverting devices were determined for treating complex aneurysms which were difficult to treat using conventional methods. In many large series, complication rates were acceptable compared with previous modalities; however, the periprocedural and postprocedural complications of the device such as early and delayed aneurysm ruptures and thromboembolic events were still considerable [39,41–43]. Coil embolization and microsurgery are still excellent methods for simple aneurysms in terms of efficiency, convenience, cost, and durability. However microsurgery and EVT of large or giant paraclinoid aneurysms had the potential risk of complications in this series compatible with previously reported series. Therefore, multidisciplinary approach using conventional microsurgery, coiling, and flowdiverting devices for alternative means to apply the proper indications would lead to good outcomes. The current study has some limitations. First, the cases were of retrospective nature. Second, although this study contained large cases, the results presented single center experiences only. According to the advance of radiologic modalities and techniques of EVT, the technical aspects of our team may not be consistent during periods. Thus, selection and inherent bias associated with the decision on the treatment strategy based on the personal experiences of the surgeons or the interventionists may be included. Third, the modalities of follow-up imaging and observational periods were slightly different from methods of treatment and condition of each patient. However, the patients included in the current study were treated during a relatively short 4-year period. During this time, our multidisciplinary team members have remained the same, and they have consistently used specific algorithms to reduce selection bias. An appropriate treatment was selected after careful discussion of the characteristics of each patient and aneurysm. We think these totally enrolled cases were considerable numbers and presented satisfying outcomes in the radiologic and in clinical aspects under our multidisciplinary approaches and were applying to a simplified classification. Investigation with newly enrolled cases and further follow-up of treated cases are currently in progress.

5. Conclusion Based on our experience, we suggest a more simplified classification for the indication between microsurgery and EVT concerning the treatment of unruptured paraclinoid aneurysms. EVT is the acceptable first line therapy for the non-dorsal group. Microsurgical treatment has prior efficacy in the dorsal group under proper individualized selection. To minimize the risk of recurrences and complications, the proper choice of treatment plan between surgical and endovascular treatment is necessary. The consideration of factors such as age, anatomic relations of surrounded structures and feasibility of EVT etc. is also important to decide the treatment methods.

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Conflict of interest None. References [1] Batjer HH, Kopitnik TA, Giller CA, Samson DS. Surgery for paraclinoidal carotid artery aneurysms. J Neurosurg 1994;80:650–8. [2] De Jesus O, Sekhar LN, Riedel CJ. Clinoid and paraclinoid aneurysms: surgical anatomy, operative techniques, and outcome. Surg Neurol 1999;51:477–87, discussion 487-478. [3] Kim JM, Romano A, Sanan A, van Loveren HR, Keller JT. Microsurgical anatomic features and nomenclature of the paraclinoid region. Neurosurgery 2000;46:670–80, discussion 680-672. [4] Barami K, Hernandez VS, Diaz FG, Guthikonda M. Paraclinoid carotid aneurysms: surgical management, complications, and outcome based on a new classification scheme. Skull Base 2003;13:31–41. [5] Giannotta SL. Ophthalmic segment aneurysm surgery. Neurosurgery 2002;50:558–62. [6] Hoh BL, Carter BS, Budzik RF, Putman CM, Ogilvy CS. Results after surgical and endovascular treatment of paraclinoid aneurysms by a combined neurovascular team. Neurosurgery 2001;48:78–89, discussion 89-90. [7] Iihara K, Murao K, Sakai N, Shindo A, Sakai H, Higashi T, et al. Unruptured paraclinoid aneurysms: a management strategy. J Neurosurg 2003;99:241–7. [8] Yasargil MG, Gasser JC, Hodosh RM, Rankin TV. Carotid-ophthalmic aneurysms: direct microsurgical approach. Surg Neurol 1977;8:155–65. [9] Morita A, Kirino T, Hashi K, Aoki N, Fukuhara S, Hashimoto N, et al. The natural course of unruptured cerebral aneurysms in a Japanese cohort. N Engl J Med 2012;366:2474–82. [10] Roy D, Raymond J, Bouthillier A, Bojanowski MW, Moumdjian R, L’Esperance G. Endovascular treatment of ophthalmic segment aneurysms with Guglielmi detachable coils. AJNR Am J Neuroradiol 1997;18:1207–15. [11] Boet R, Wong GK, Poon WS, Lam JM, Yu SC. Aneurysm recurrence after treatment of paraclinoid/ophthalmic segment aneurysms – a treatment-modality assessment. Acta Neurochir (Wien) 2005;147:611–6, discussion 616. [12] Yadla S, Campbell PG, Grobelny B, Jallo J, Gonzalez LF, Rosenwasser RH, et al. Open and endovascular treatment of unruptured carotidophthalmic aneurysms: clinical and radiographic outcomes. Neurosurgery 2011;68:1434–43, discussion 1443. [13] Jin SC, Kwon do H, Ahn JS, Kwun BD, Song Y, Choi CG. Clinical and radiogical outcomes of endovascular detachable coil embolization in paraclinoid aneurysms: a 10-year experience. J Korean Neurosurg Soc 2009;45:5–10. [14] Hayakawa M, Murayama Y, Duckwiler GR, Gobin YP, Guglielmi G, Vinuela F. Natural history of the neck remnant of a cerebral aneurysm treated with the Guglielmi detachable coil system. J Neurosurg 2000;93:561–8. [15] Park HK, Horowitz M, Jungreis C, Kassam A, Koebbe C, Genevro J, et al. Endovascular treatment of paraclinoid aneurysms: experience with 73 patients. Neurosurgery 2003;53:14–23, discussion 24. [16] Thornton J, Aletich VA, Debrun GM, Alazzaz A, Misra M, Charbel F, et al. Endovascular treatment of paraclinoid aneurysms. Surg Neurol 2000;54:288–99. [17] Chen L, Kato Y, Karagiozov KL, Yoneda M, Imizu S, Hayakawa M, et al. Usefulness of a simplified management scheme for paraclinoid aneurysms based on a modified classification. Cerebrovasc Dis 2008;26:388–96. [18] Sherif C, Gruber A, Dorfer C, Bavinzski G, Standhardt H, Knosp E. Ruptured carotid artery aneurysms of the ophthalmic (C6) segment: clinical and angiographic long term follow-up of a multidisciplinary management strategy. J Neurol Neurosurg Psychiatry 2009;80:1261–7. [19] al-Rodhan NR, Piepgras DG, Sundt Jr TM. Transitional cavernous aneurysms of the internal carotid artery. Neurosurgery 1993;33:993–6, discussion 997-998. [20] Ogilvy C. Paraclinoid carotid aneurysms. In: Ojemann RG, Ogilvy CS, Crowell RM, et al., editors. Surgical management of neurovascular disease. Baltimore: Williams and Wilkins; 1995. p. 185–213. [21] Bouthillier A, van Loveren HR, Keller JT. Segments of the internal carotid artery: a new classification. Neurosurgery 1996;38:425–32, discussion 432-423. [22] Raymond J, Guilbert F, Weill A, Georganos SA, Juravsky L, Lambert A, et al. Long-term angiographic recurrences after selective endovascular treatment of aneurysms with detachable coils. Stroke 2003;34:1398–403.

77

[23] Drake CG, Vanderlinden RG, Amacher AL. Carotid-ophthalmic aneurysms. J Neurosurg 1968;29:24–31. [24] Guidetti B, La Torre E. Management of carotid-ophthalmic aneurysms. J Neurosurg 1975;42:438–42. [25] Locksley HB. Natural history of subarachnoid hemorrhage, intracranial aneurysms and arteriovenous malformations. J Neurosurg 1966;25: 321–68. [26] Brilstra EH, Rinkel GJ, van der Graaf Y, van Rooij WJ, Algra A. Treatment of intracranial aneurysms by embolization with coils: a systematic review. Stroke 1999;30:470–6. [27] Huang MC, Baaj AA, Downes K, Youssef AS, Sauvageau E, van Loveren HR, et al. Paradoxical trends in the management of unruptured cerebral aneurysms in the United States: analysis of nationwide database over a 10-year period. Stroke 2011;42:1730–5. [28] Fulkerson DH, Horner TG, Payner TD, Leipzig TJ, Scott JA, DeNardo AJ, et al. Results, outcomes, and follow-up of remnants in the treatment of ophthalmic aneurysms: a 16-year experience of a combined neurosurgical and endovascular team. Neurosurgery 2009;64:218–29, discussion 229-230. [29] Beretta F, Andaluz N, Zuccarello M. Aneurysms of the ophthalmic (C6) segment of the internal carotid artery: treatment options and strategies based on a clinical series. J Neurosurg Sci 2004;48:149–56. [30] Day AL. Aneurysms of the ophthalmic segment. A clinical and anatomical analysis. J Neurosurg 1990;72:677–91. [31] Parkinson RJ, Bendok BR, Getch CC, Yashar P, Shaibani A, Ankenbrandt W, et al. Retrograde suction decompression of giant paraclinoid aneurysms using a No. 7 French balloon-containing guide catheter. Technical note. J Neurosurg 2006;105:479–81. [32] Ng PY, Huddle D, Gunel M, Awad IA. Intraoperative endovascular treatment as an adjunct to microsurgical clipping of paraclinoid aneurysms. J Neurosurg 2000;93:554–60. [33] Yeon JY, Hong SC, Kim JS, Kim KH, Jeon P. Unruptured non-branching site aneurysms located on the anterior (dorsal) wall of the supraclinoid internal carotid artery: aneurysmal characteristics and outcomes following endovascular treatment. Acta Neurochir (Wien) 2012;154:2163–71. [34] Kwon BJ, Im SH, Park JC, Cho YD, Kang HS, Kim JE, et al. Shaping and navigating methods of microcatheters for endovascular treatment of paraclinoid aneurysms. Neurosurgery 2010;67:34–40, discussion 40. [35] Murayama Y, Vinuela F, Duckwiler GR, Gobin YP, Guglielmi G. Embolization of incidental cerebral aneurysms by using the Guglielmi detachable coil system. J Neurosurg 1999;90:207–14. [36] Campi A, Ramzi N, Molyneux AJ, Summers PE, Kerr RS, Sneade M, et al. Retreatment of ruptured cerebral aneurysms in patients randomized by coiling or clipping in the International Subarachnoid Aneurysm Trial (ISAT). Stroke 2007;38:1538–44. [37] Kim LJ, Tariq F, Levitt M, Barber J, Ghodke B, Hallam DK, et al. Multimodality treatment of complex unruptured cavernous and paraclinoid aneurysms. Neurosurgery 2014;74:51–61, discussion 61; quiz 61. [38] Lylyk P, Miranda C, Ceratto R, Ferrario A, Scrivano E, Luna HR, et al. Curative endovascular reconstruction of cerebral aneurysms with the pipeline embolization device: the Buenos Aires experience. Neurosurgery 2009;64:632–42, discussion 642-633; quiz N636. [39] Nelson PK, Lylyk P, Szikora I, Wetzel SG, Wanke I, Fiorella D. The pipeline embolization device for the intracranial treatment of aneurysms trial. AJNR Am J Neuroradiol 2011;32:34–40. [40] Nutik S. Carotid paraclinoid aneurysms with intradural origin and intracavernous location. J Neurosurg 1978;48:526–33. [41] Saatci I, Yavuz K, Ozer C, Geyik S, Cekirge HS. Treatment of intracranial aneurysms using the pipeline flow-diverter embolization device: a singlecenter experience with long-term follow-up results. AJNR Am J Neuroradiol 2012;33:1436–46. [42] Fischer S, Vajda Z, Aguilar Perez M, Schmid E, Hopf N, Bazner H, et al. Pipeline embolization device (PED) for neurovascular reconstruction: initial experience in the treatment of 101 intracranial aneurysms and dissections. Neuroradiology 2012;54:369–82. [43] Kan P, Siddiqui AH, Veznedaroglu E, Liebman KM, Binning MJ, Dumont TM, et al. Early postmarket results after treatment of intracranial aneurysms with the pipeline embolization device: a U.S. multicenter experience. Neurosurgery 2012;71:1080–7, discussion 1087-1088.