Background Current endovascular techniques have been widely used to treat paraclinoid aneurysms.
Methods From January 2009 to December 2011, 126 consecutive patients with 142 saccular paraclinoid aneurysms were treated with endovascular embolization at our institute. A retrospective review of the clinical and imaging data was performed.
Results Of the 142 aneurysms, 121 (86.2%) had small while 21 (14.8%) had large fundus size. 83 aneurysms (58.5%) were narrow necked and 59 (41.5%) were wide necked. The dome–neck ratio was favorable in 26 aneurysms (18.3%) and unfavorable in 116 (81.7%). 24 aneurysms (16.9%) were managed with coil embolization and 118 (83.1%) with a stent assisted coiling technique. Immediate angiography demonstrated complete occlusion in 62 (43.7%), neck remnant occlusion in 47 (33.1%), and residual aneurysm occlusion in 33 (23.2%) aneurysms. The overall recurrence rate in the 112 aneurysms with angiographic follow-up (8.88±3.40 months, mean±SD) was 12.5%. Of the 14 recurrent aneurysms, 10 were managed with endovascular treatment (six by stent assisted coiling, four by coiling) while four are under observation. There were six (4.3%) procedural complications during 137 procedures. Clinical follow-up was available for 119 patients (94%) with a follow-up time of 16.6±13.6 months, and the majority (98%) had a modified Rankin scale score of 0–1.
Conclusions The stent assisted coiling technique is effective for the treatment of paraclinoid aneurysms. Small paraclinoid aneurysms (≤10 mm) are suitable for endovascular treatment, with a low rate of recurrence. In contrast, large paraclinoid aneurysms (>10 mm) treated with current endovascular techniques exhibited a high rate of recurrence.
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Paraclinoid aneurysms can be defined as intracranial aneurysms that arise from a segment of the internal carotid artery (ICA) between the roof of the cavernous sinus and the origin of the posterior communicating artery.1 ,2 Due to the proximity to the skull base, surgical clipping of paraclinoid aneurysms remains a challenge.1 ,3–6 Currently, increasing numbers of paraclinoid aneurysms are referred for interventional treatment.2 ,4 ,7 ,8 Compared with the surgical technique, endovascular treatment of paraclinoid aneurysms is associated with a lower rate of complete occlusion and more frequent recurrence, and this may be related to many factors, such as aneurysm dimension and the endovascular technique used. By reviewing the literatures, we found that the most widely used endovascular technique for paraclinoid aneurysms was detachable coiling with or without balloon remodeling, before 2010. Recently, stent assisted coiling has become more popular.1 ,2 ,4 ,6 ,8 ,9
In this study, we evaluated the efficiency of current endovascular techniques in treating paraclinoid aneurysms by retrospective analysis of the clinical and imaging data of patients treated at our institute. To our knowledge, this is the largest series of paraclinoid aneurysms treated by endovascular techniques to date.
From January 2009 to December 2011, 918 aneurysms were treated by the endovascular team at our institute. All patient data were entered prospectively into a database established at our institute. Among these aneurysms, 136 consecutive patients had 152 saccular paraclinoid aneurysms. At our institute, all ruptured or symptomatic unruptured paraclinoid aneurysms need to be treated. We recommend treating asymptomatic unruptured aneurysms more than 7 mm; however, we do not refuse to treat smaller aneurysms (3–7 mm) if patients express a strong desire to have them treated. The reason for selecting endovascular treatment as a therapeutic alternative is anticipated surgical difficulties or direct referral for embolization. Giant aneurysms in 10 patients who were treated by occlusion of the ICA with or without bypass protection were excluded.
A total of 126 patients with 142 paraclinoid aneurysms were included in the study. A retrospective review of the medical records, radiographic data, endovascular procedure reports, and follow-up records were performed via the database. The protocol was approved by the ethics committee of our institute, and written informed consent was obtained from all patients.
Description of aneurysms
Each patient underwent cerebral angiography with routine use of three-dimensional rotational digital angiography to determine the side, orientation, size, neck width, and exact morphology of the aneurysm.
Aneurysms were classified into two types according to the criteria established by Day.3 Type I aneurysms (ophthalmic artery aneurysms) arose from the ICA just distal to the ophthalmic artery and from the dorsal segment of the ICA. The aneurysms were best visualized on lateral projection angiograms and typically projected superiorly or superomedially. Type II aneurysms (superior hypophyseal artery aneurysm) arose from the ventral, medial, or lateral segment of the ICA, and had no direct association with the ophthalmic artery. They projected either horizontally or inferiorly, although some large ones might project superiorly.
Aneurysm fundus and neck size was taken at the point of maximum length or width. The dome–neck ratio was the ratio of maximum height to neck width. Fundus size was classified as small (≤10 mm) or large (10–25 mm). Neck width was defined as narrow (≤4 mm) or wide (>4 mm). A dome–neck ratio was defined as favorable (≥2) or unfavorable (<2).
All procedures were performed with the patient under general anesthesia. After femoral sheath placement, systemic heparinization was started with a loading dose of 3000 IU and was maintained with a dose of 1000 IU on an hourly basis. For patients with ruptured aneurysms, the same regimen of systemic heparinization was followed after partial embolization. Inside the guiding catheters, microcatheters with proper shapes were introduced over micro guidewires and navigated into the aneurysms. Aneurysms were packed as densely as possible with coils. Coils used included Guglielmi detachable coils (Boston Scientific, Fremont, California, USA), NXT coils (ev3, Irvine, California, USA), microsphere three-dimensional coils (Micrus Co, Mountainview, California, USA), hydrogel coils (HydroCoil; MicroVention, Inc, Aliso Viejo, California, USA), and bioactive platinum coils with polyglycolic–polylactic acid copolymer covering (Matrix and Matrix2, Boston Scientific).
If the neck was narrow and the dome–neck ratio was favorable, endovascular treatment was performed by coil embolization with or without balloon remodeling techniques. If the neck was wide or the dome–neck ratio was unfavorable, a stent assisted coiling technique was used. Stents were usually deployed after the microcatheter was in position (jailing technique) or occasionally deployed prior to that with the microcatheter being delivered through stent struts afterwards. The first technique was our preferred method. We used standard double antiplatelet loading doses and intraprocedural heparinization, as previously reported.10 The stents used included Neuroform2 stent (Boston Scientific-Target Therapeutics, Fremont, California, USA), Enterprise stent (Cordis Codman and Shurtleff Inc, Raynham, Massachusetts, USA), Solitar AB stent (ev3), and Leo stent (Balt, Montmorency, France).
Evaluation of the embolization
The angiographic results were graded using previously published classifications.11 Complete occlusion was defined as cases without any opacification of the neck or sac of the aneurysm (class 1). A residual neck (class 2) was defined as the existence of any portion of the original defect of the arterial wall, as seen on any single projection but without opacification of the aneurysm sac. Any opacification of the sac was classified as residual aneurysm (class 3). Classes 1 and 2 were considered satisfactory results whereas class 3 was considered unsatisfactory. A recurrence was defined as any increase in the size of the remnant.
Angiographic follow-up studies were routinely performed in patients at 6 months after treatment and, if the results were stable, for more incremental periods (1 year, 2 years, etc). Additional follow-up angiographs were performed in patients with a potential risk of recanalization.
Clinical follow-up results were assessed during hospitalization for follow-up angiography or by telephone interview using the modified Rankin scale (mRS) score. The total number of months of clinical follow-up for each patient was recorded.
When two or more aneurysms were present in the same patient, they were considered as independent samples in the statistical analysis. Statistical analysis was performed with SPSS, V.17.0 (SPSS, Chicago, Illinois, USA). Categorical variables were examined with the χ2 test. The Student's t test and t’ test or Fisher's exact test were used to compare continuous variables. A p value < 0.05 was considered significant.
Patients and clinical presentation
The mean age of the 126 patients was 52.1±9.8 years (mean±SD). The majority (94; 74.6%) of patients were women. Multiple aneurysms were found in 24 (19%) patients, including 10 patients with bilateral paraclinoid aneurysms, three patients with three paraclinoid aneurysms, and 11 patients with aneurysms in other locations. Cerebral angiography demonstrated 79 aneurysms on the left side and 63 on the right side.
Eighty-three patients (65.9%) had incidental paraclinoid aneurysms, including one patient admitted with a recurrent paraclinoid aneurysm after coiling in another hospital. Thirteen patients (10.3%) presented with visual symptoms and 24 patients (19%) presented with subarachnoid hemorrhage (SAH). Among patients with SAH, 14 were classified as Hunt–Hess grade I, six as grade II, three as grade III, and one as grade IV. Two patients (1.6%) presented with intracranial hematoma caused by arteriovenous malformation. Four patients (3.2%) presented with cerebral infarction.
Mean fundus size, neck width, and dome–neck ratio of 142 aneurysms were 6.14±4.24 mm, 3.98±1.5 mm, and 1.50±0.67, respectively. The characteristics of these aneurysms are summarized in table 1.
Fifty-six (39%) aneurysms were ophthalmic aneurysms (type I) and 86 (61%) were superior hypophyseal artery aneurysms (type II). The anatomic characteristics of the two types are summarized in table 2. Type I aneurysms tended to be large and have a wide neck compared with type II aneurysms. Type II aneurysms were mainly (94.2%) small aneurysms (≤10 mm) and most (91.9%) had an unfavorable dome–neck ratio.
Among the 142 paraclinoid aneurysms, 10 required more than one session of endovascular treatment to complete treatment; nine of these aneurysms required two sessions and one required three sessions, resulting in a total of 137 endovascular procedures. Twenty-four aneurysms (16.9%) were managed with coil embolization (including balloon remodeling technique) and 118 (83.1%) with a stent assisted coiling technique. The stents were: Enterprise (n=101), Neuroform2 (n=4), LEO (n=3), and Solitar AB stents (n=11).
Immediate angiographic results
Of the 142 aneurysms, 62 aneurysms (43.7%) had complete occlusion (class 1) at the time of the initial coil embolization, 47 (33.1%) had neck remnant occlusion (class 2), and 33 (23.2%) had residual aneurysm occlusion (class 3). The ophthalmic artery remained patent as in pre-procedure in all cases. Fundus size, neck width, dome–neck ratio, and techniques used had no significant impact on the initial treatment outcome (table 3). No statistically significant difference in the adopted techniques and immediate angiographic results were found between the two groups.
Early (<12 months) angiographic follow-up was available for 112 aneurysms (78.9%) with a mean follow-up time of 6.77 ±2.15 months. Middle term (≥1 year) angiographic follow-up was available for 71 aneurysms (50%) (13.41±2.64 months). Angiographic recurrence occurred in 14 aneurysms—10 managed with further endovascular treatment (six by stent assisted coiling, four by coiling) while four are under observation. Among the recurrent aneurysms, three initially demonstrated class 1 occlusion, six class 2 occlusion, and five class 3 occlusion. Fundus size of the recurrent aneurysms was small in six and large in eight cases. The overall recurrence rate in the 112 aneurysms for which angiographic follow-up was available was 12.5% (mean follow-up time 8.88±3.40 months). The mean interval between recurrence and initial treatment was 9.89±5.21 months. Large aneurysms (>10 mm) had a significantly higher recurrence rate (62.5%) than small aneurysms (≤10 mm) (4.2%). The final angiographic results determined on the last available follow-up angiograms of 112 aneurysms showed class 1 occlusion in 71 aneurysms (63.4%), class 2 occlusion in 29 aneurysms (25.9%), and class 3 occlusion in 12 aneurysms (10.7%).
There were six (4.3%) procedural complications during 137 procedures (table 4). All occurred during initial treatment with stent assisted embolization. Partial coil loop protrusion occurred in three patients after stent deployment and these were dealt with by deployment of another stent to compress the coils between the two stents. One of the patients suffered a thromboembolic event later. Thromboembolic complications occurred in three patients, who were managed with local intra-arterial infusion of urokinase or systemic administration of antiplatelet agents. Although thrombolysis failed in one patient, none of these patients experienced neurological deficit due to sufficient compensation. Overall, no permanent morbidity or mortality was found.
Clinical follow-up was available for 119 patients (94%) with a mean±SD follow-up time of 16.6±13.6 months: 106 patients had an mRS score of 0, 11 patients mRS score 1, one patient mRS score 2, and one patient mRS score 3. Six patients lost to follow-up who presented with incidental aneurysms all had an mRS score of 0–1 at discharge. One patient died 4 months after embolization because of pneumonia.
One patient had SAH after near complete occlusion of an unruptured paraclinoid aneurysm by coils 2 months previously. Emergency angiography revealed coil compaction and aneurysm recanalization. After embolization with a stent assisted coiling technique in the acute phase, this patient had an mRS score of 2 after 1 year of follow-up.
Follow-up ophthalmologic data were available for all patients who presented with ophthalmological deficits. Of these patients, nine had no change while four had improvements at follow-up.
We have described a large series of endovascular treatment of paraclinoid aneurysms at one center, using coiling and stent assisted coiling techniques. Most of the paraclinoid aneurysms were unruptured or asymptomatic in our series, which is similar to other reports.2 ,4–6 12–14 There is no consensus on the treatment of unruptured asymptomatic aneurysms. We searched the PubMed database for English language articles after 2000 using the keywords ‘paraclinoid aneurysm’, ‘ophthalmic aneurysm’, or ‘ophthalmic segment aneurysm’ and ‘endovascular’. The results of the literature search (with more than 50 paraclinoid aneurysms) on endovascular treatment of paraclinoid aneurysm before and after 2010 are summarized in supplementary tables 5 and 6 (available online only).
The main endovascular technique for the treatment of paraclinoid aneurysms was coil embolization with or without a balloon remodeling technique before 20101 ,9 ,12–16 ; a stent assisted coiling technique has been more widely used since 2010.2 ,4 ,7 ,8 ,17 That wide necked (>4 mm) aneurysms account for nearly 40–50% of aneurysms and an unfavorable dome–neck ratio (<2) is common may be one of the reasons.9 ,14 ,15 ,17 It is thought that the hemodynamic characteristics at the region may account for the high recurrence rate, and the stent may play a role not only in structural support but also in reconstructing the flow.2 ,18 ,19 Since 2008, at our institute the stent assisted coiling technique has been used in treating wide necked (>4 mm) aneurysms with an unfavorable dome–neck ratio (<2). In the present study, the stent assisted coiling technique predominated in managing wide necked or unfavorable dome–neck ratio paraclinoid aneurysms (83.1% of all cases). To our knowledge, this is the largest series so far of paraclinoid aneurysm treatment using stent assisted coiling.
Initial angiographic results
The proportion of complete occlusion in the initial angiographic results in previous reports ranged from 43.4% to 72.6% before 2010 and from 38% to 68.3% after 2010.1 ,2 ,7–9 12–17 In our study, 76.8% of aneurysm had satisfactory occlusion at the initial angiographic examination, with 43.7% having complete occlusion at the time. Fundus size, neck width, dome–neck ratio, and treatment modalities did not have a significant impact on the occlusion rate (p>0.05). It may be explained by similar occlusion rates in different aneurysms with stent assisted coiling.
Before 2010, the transient morbidity ranged from 0% to 14.3% and permanent morbidity ranged from 0% to 8.3%. The procedure related mortality ranged from 0% to 2.2%.1 ,9 ,12–16 After 2010, transient morbidity and permanent morbidity ranged from 0% to 4.8% and 0% to 3.5%, respectively.2 ,7 ,8 ,17 The rate of procedural complications in our cohort was 4.3%, and permanent morbidity and mortality was 0%, which is similar to previous reports. Interestingly, the incidence of complications was not associated with the use of the stent assisted technique. This suggests that the stent assisted technique is safe in the endovascular treatment of paraclinoid aneurysms. Because the thromboembolic event may occur in aneurysms using a stent assisted technique, we usually deploy stents in the ICA but not in the middle cerebral artery. In the case of ICA thrombosis, the collateral circulation may provide sufficient blood through the anterior communicating artery or posterior communicating artery to avoid catastrophic sequelae. When coiling very tiny aneurysms (≤3 mm), coil loops may protrude from the stent mesh. Because of the impediment effect of stent struts, coils seldom herniated into the parent artery as a whole. By bailout stent deployment, this could avoid permanent neurological deficits.
The ophthalmic artery can be nearly all preserved during interventional treatment of paraclinoid aneurysms with coil embolization alone and stent assisted embolization.7 Even in the treatment of ophthalmic aneurysms with diversion devices, the patency of the ophthalmic artery was observed in 85% of cases immediately after placement of the device.20 Those cases of ophthalmic artery occlusion were well tolerated clinically because the ophthalmic artery has a rich distal collateral supply from the external carotid branches. We believe that the major threat to vision during interventional treatment is related to the progressive mass effect from large/giant aneurysm thrombosis or small emboli to the central retinal artery, which may be prevented by regular anticoagulation during the procedure.
In previous reports (before 2010) on endovascular treatment of paraclinoid aneurysms, the rate of recurrence ranged from 3.9% to 26%.1 ,9 ,12–16 The recurrence rate ranged from 5% to 17.8% after 2010.2 ,7 ,8 ,17 Most of the studies have suggested that 6 month follow-up angiography was insufficient for detecting most recurrences and annual follow-up is recommended.2 ,8 ,9 ,14 ,15 Many authors mentioned size related aneurysm recurrence—that is, aneurysms with a diameter >10 mm have a higher rate of recurrence.2 ,21 In the present study, large aneurysms (>10 mm) had a significantly higher rate of recurrence (62.5%) than small aneurysms (≤10 mm) (4.2%). A paraclinoid aneurysm with a fundus size ≤10 mm is suitable for endovascular treatment with a relatively low rate of recurrence. For large paraclinoid aneurysms, the present endovascular technique cannot produce satisfactory results. Recently, a flow diverter device has been used in the management of paraclinoid aneurysms; however, the efficiency and durability of this technique need more observation.20 ,22 ,23
In our study, the angiographic results at the last follow-up demonstrated higher complete occlusion rates than the initial angiographic results. Twelve class 2 and 5 aneurysms demonstrating class 3 occlusion at the initial angiographic results had progressive thrombosis. This phenomenon was mostly observed in small aneurysms with a small neck.24 However, in our study, this happened mostly in small aneurysms with an unfavorable dome–neck ratio. It may be related to the effect of stents on biological remodeling and hemodynamic remodeling of the defective segment of the parent artery.19
The population studied was a selected group of patients and some of the patients that preferred surgical clipping were not enrolled. Other parameters that could have potentially affected the effectiveness of treatment, such as coil type, were not analyzed.
To our knowledge, this is the largest series to date of paraclinoid aneurysms treated by stent assistance. The angiographic recurrence rate of endovascular treatment of paraclinoid aneurysms was 12.5% in our study. The stent assisted coiling technique was effective for the treatment of paraclinoid aneurysms. Small paraclinoid aneurysms (≤10 mm) were suitable for endovascular treatment which was associated with a low recurrence rate. In contrast, large paraclinoid aneurysms (>10 mm) treated with the present endovascular techniques exhibited a high rate of recurrence.
The authors thank Yong Liu (Department of Health Statistics, Medical College of Nanchang University) for his great help in the statistical analysis.
This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.
Files in this Data Supplement:
- Data supplement 1 - Online table
Contributors YW, FJ and HM: drafting and revising the article. YL and CJ: substantial contributions to the conception and design. AHS: drafting the article, and analysis and interpretation of the data. XY: conception and design, and final approval of the version to be published.
Funding This study was supported by the National Science Foundation of China (grant Nos 81220108007 and 81171079), the Individual Item Assisted by Beijing Excellent Talents Program (grant No 20061D0300400072), High-Level Health Technique Talent Training Plan of Beijing Health System (grant No 2009–3-22), Special Program of Health Commonweal Scientific Research (grant No 200902004), and National 973 Basic Research Program of China (grant No 2010CB732605).
Competing interests None.
Ethics approval The study was approved by the ethics committee of Beijing Neurosurgical Institute.
Provenance and peer review Not commissioned; externally peer reviewed.