Stent-assisted coil embolization of ruptured wide-necked aneurysms in the acute period: incidence of and risk factors for periprocedural complications

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Object

The purpose of this study was to report the authors' experiences in stent-assisted coil embolization (SAC) of ruptured wide-necked aneurysms in the acute period and to evaluate the incidence of and risk factors for periprocedural complications.

Methods

A total of 72 patients were recruited for this study between March 2007 and June 2012. All patients met the following criteria: 1) the presence of ruptured intracranial wide-necked saccular aneurysms, and 2) the patient underwent SAC for treatment of those aneurysms within 72 hours of rupture. All of the patients with clinically poor grades or acute hydrocephalus underwent external ventricular drainage (EVD) before SAC. The incidence of and risk factors for periprocedural complications were retrospectively evaluated.

Results

Of the 72 patients included in this study, periprocedural complications occurred in 14 (19.4%), including asymptomatic complications in 4 (5.6%) and symptomatic complications in 10 (13.9%); there were symptomatic thromboembolic complications in 5 patients (6.9%), and symptomatic hemorrhagic complications in 5 (6.9%). The authors observed no subacute or delayed thromboembolic complications during the follow-up period of 18.8 months. Use of EVD (OR 1.413, 95% CI 0.088–2.173; p = 0.046) was the only independent risk factor for periprocedural complications on multivariate logistic regression analysis.

Conclusions

The periprocedural complication rate during SAC was 19.4% among 72 patients. Because of the high complication rate, microsurgical clipping or endovascular treatment with another technique (multiple-microcatheter or balloon-assisted technique) may be a more appropriate option for first-line treatment than SAC, especially in patients requiring EVD.

Abbreviations used in this paper:ACT = activated clotting time; EVD = external ventricular drainage; GOS = Glasgow Outcome Scale; GP = glycoprotein; IPH = intraparenchymal hemorrhage; SAC = stent-assisted coil embolization; SAH = subarachnoid hemorrhage.

Abstract

Object

The purpose of this study was to report the authors' experiences in stent-assisted coil embolization (SAC) of ruptured wide-necked aneurysms in the acute period and to evaluate the incidence of and risk factors for periprocedural complications.

Methods

A total of 72 patients were recruited for this study between March 2007 and June 2012. All patients met the following criteria: 1) the presence of ruptured intracranial wide-necked saccular aneurysms, and 2) the patient underwent SAC for treatment of those aneurysms within 72 hours of rupture. All of the patients with clinically poor grades or acute hydrocephalus underwent external ventricular drainage (EVD) before SAC. The incidence of and risk factors for periprocedural complications were retrospectively evaluated.

Results

Of the 72 patients included in this study, periprocedural complications occurred in 14 (19.4%), including asymptomatic complications in 4 (5.6%) and symptomatic complications in 10 (13.9%); there were symptomatic thromboembolic complications in 5 patients (6.9%), and symptomatic hemorrhagic complications in 5 (6.9%). The authors observed no subacute or delayed thromboembolic complications during the follow-up period of 18.8 months. Use of EVD (OR 1.413, 95% CI 0.088–2.173; p = 0.046) was the only independent risk factor for periprocedural complications on multivariate logistic regression analysis.

Conclusions

The periprocedural complication rate during SAC was 19.4% among 72 patients. Because of the high complication rate, microsurgical clipping or endovascular treatment with another technique (multiple-microcatheter or balloon-assisted technique) may be a more appropriate option for first-line treatment than SAC, especially in patients requiring EVD.

It is well established that wide-necked aneurysms are difficult to treat endovascularly due to the risk of coil protrusion into the parent artery and aneurysm recurrence. For these endovascularly challenging aneurysms, various techniques such as balloon-assisted,7,23 stent-assisted,2,5,24 or multiple-microcatheter techniques20,21 have been developed. Recently, stent-assisted coil embolization (SAC) has become a popular option for treatment of aneurysms that are not amenable to endovascular treatment.1,2,5,12,24 This technique, however, requires that a foreign body (the stent) remain within the artery, thereby requiring anticoagulation or antiplatelet therapy to prevent procedure-related thromboembolic complications. Therefore, neurosurgeons and neurointerventionists have been reluctant to treat ruptured aneurysms with stent assistance because of the potential risk of hemorrhagic complications if patients require additional surgical procedures, as well as thromboembolic complications caused by the stent. Thus, the purpose of this study is to report our experiences with SAC of ruptured wide-necked aneurysms in the acute period and to evaluate the incidence of and risk factors for periprocedural complications.

Methods

Patient Selection

This retrospective study was approved by our institutional review board and informed consent was waived. Beginning in March 2007, patient data were gathered from 4 hospitals where ruptured aneurysms were treated endovascularly, using the same anticoagulation and antiplatelet regimens as well as preoperative external ventricular drainage (EVD). We also had a prospectively collected database containing a series of 908 consecutive ruptured aneurysms treated using endovascular methods between March 2007 and June 2012. Among them, 131 patients were treated using a single or multiple stents. A total of 72 patients (male/female ratio 15:57, mean age [± SD] 58.3 ± 11.8 years, range 32–85 years) were recruited for this study, and all patients met the following criteria: 1) presence of ruptured intracranial wide-necked saccular aneurysms, and 2) treatment with SAC for those aneurysms within 72 hours of rupture. Fifty-nine patients were excluded due to the following reasons: 1) SAC was used as a stent salvage technique after procedure-related complications9 (n = 15); 2) ruptured dissecting aneurysms were present (n = 26); 3) blood blister–like aneurysms were present (n = 12); and 4) patients underwent SAC more than 72 hours after rupture (n = 6).

Clinically poor-grade patients were defined as those with an initial Hunt and Hess grade of IV or V. Acute hydrocephalus was diagnosed on CT scans. Patients with clinically poor grades or acute hydrocephalus underwent EVD before the embolization to reduce the risk of catheter-related hemorrhagic complications due to antiplatelet therapy. Aneurysm size and morphological characteristics were determined using digital subtraction angiography with 3D rotational imaging. A wide-necked saccular aneurysm was defined as having a dome-to-neck ratio of < 2 or a neck diameter of ≥ 4 mm. Thromboembolic complications were defined as angiographic evidence of thrombosis during or at the end of SAC. Hemorrhagic complications were defined as newly developed hemorrhage on CT or MRI studies within 30 days of the procedure. The type of hemorrhage, including intraparenchymal hemorrhage (IPH), subarachnoid hemorrhage (SAH), or catheter-related bleeding was determined by 2 independent investigators. The incidence of and risk factors for periprocedural complications were retrospectively evaluated.

The SAC Procedure

When stent assistance was required for endovascular treatment in patients with ruptured wide-necked aneurysms, surgical clip occlusion was considered as the first treatment option. Treatment decisions with respect to patient comorbidities, clinical status, surgical feasibility, and grade of hemorrhage were made in consensus among the neurosurgeons and neurointerventionists. All operations were performed under general anesthesia. A 6-Fr or 7-Fr guiding catheter was positioned in the internal carotid artery via the common femoral artery for anterior circulation aneurysms or in the vertebral artery for posterior circulation aneurysms. Types of stents used in this procedure included the Neuroform stent (Stryker Neurovascular), the Enterprise stent (Codman Neurovascular), and the Solitaire stent (ev3). Stents were chosen according to the surgeon's preference with respect to anatomical variations. There were no cases of suboptimal stent positioning in this study.

While treating the ruptured intracranial aneurysms endovascularly, heparin was not injected intravenously or subcutaneously, but was instead mixed into the saline flushes during the procedure. Thus, the activated clotting time (ACT) was not checked during the procedure. After the femoral artery puncture, loading doses of clopidogrel (300–600 mg32) and aspirin (200–400 mg) were given via the nasogastric tube. After the procedure, patients were prescribed 75 mg clopidogrel daily for 3 months and 100 mg aspirin daily for a minimum of 12 months. During the procedure, 1 mg of glycoprotein (GP) IIb/IIIa antagonist (tirofiban) was injected intraarterially when the parent artery was occluded by a thromboembolism. Postprocedural surgical management such as EVD or ventriculoperitoneal shunt insertion was conducted without discontinuation of the antiplatelet agents.

Clinical and Radiographic Outcomes

Angiographic results and clinical outcomes were reviewed retrospectively. Follow-up angiography was performed in 56 of the 72 patients between 6 and 36 months (mean 14.8 months) after the procedure, and clinical follow-up was performed for 6 to 54 months (mean 18.8 months) in 61 of the 72 patients (11 patients were lost to follow-up, 5 due to death). The angiographic results were evaluated by 2 independent investigators and categorized as complete occlusion (without a neck remnant), neck remnant (> 90% occlusion with small neck remnant or dog ear), or partial occlusion (filling of the aneurysm lumen). Clinical outcomes were assessed based on the Glasgow Outcome Scale (GOS). In-stent stenosis was defined as > 50% stenosis on follow-up angiography. A favorable outcome was defined as a GOS score of 4 or 5 (moderate disability or better), and a poor outcome was defined as a GOS score of 2 or 3 (severe disability or vegetative state). A GOS score of 1 was indicative of death.

Statistical Analysis

All statistical analyses were performed by a biostatistician using SPSS version 18.0 (SPSS, Inc.). The Mann-Whitney U-test was used for numeric variables. Chi-square or Fisher exact tests were used for nominal variables. Univariate analysis was performed to determine the association of thromboembolic complications with other factors. Binary logistic regression analysis was then performed on variables with an unadjusted effect and a p value of < 0.10 on univariate analysis to determine independent associations of thromboembolic complication with other factors. A p value of less than 0.05 for a 95% confidence interval was considered to be statistically significant.

Results

Of the 72 patients included in this study, the majority had a good Hunt and Hess grade (51 patients, 70.8%) and anterior circulation aneurysms (46 patients, 63.9%). In 36 (50%) of the 72 patients EVD was performed; preembolization EVD in 34 (47.2%) and postembolization EVD in 2 (2.8%). Among the 36 patients in whom EVD was performed, 7 received a ventriculoperitoneal shunt. There were no decompressive craniectomies or microsurgical clippings after SAC in this study. Overall, periprocedural complications occurred in 14 patients (19.4%): asymptomatic thromboembolic complications in 4 (5.6%), symptomatic thromboembolic complications in 5 (6.9%), and symptomatic hemorrhagic complications in 5 (6.9%). All hemorrhagic complications were symptomatic. Therefore, 10 (13.9%) of the 72 patients experienced symptomatic periprocedural complications in this study. Table 1 shows the details for the 14 patients with periprocedural complications.

TABLE 1:

Demographic and clinical data in 14 patients with ruptured wide-necked aneurysms treated with SAC who had periprocedural complications*

Case No.Age (yrs), SexHH GradeLesion LocationLesion Size (mm)StentHCEVDVasospasmComplicationsGOS Score
LengthWidthDepthNeckAt DischargeAt 6 MosAt 12 Mos
thromboembolic complications
160, FIIBA bifurcation4.75.66.28.5Enterprisenononoparent artery thrombosis555
258, MIIIICA (ventral wall)15.98.67.37.2Enterpriseyesyesnoin-stent thrombosis555
347, FIIACoA4.34.33.63.1Neuroformnononoin-stent thrombosis555
461, FIIIPCoA10.27.85.34.4Neuroformyesyesnoin-stent thrombosis555
548, FIIIICA (dorsal wall)2.575.87Enterpriseyesyesyesin-stent thrombosis & distal embolism444
665, FIVICA (VM wall)7.75.44.77.2Enterprisenoyesnoin-stent thrombosis & distal embolism444
772, FIIIPCoA3.83.83.33.1Neuroformyesyesnoin-stent thrombosis & distal embolism333
871, FIIIPCoA6.84.15.43.5Neuroformyesyesnoin-stent thrombosis & distal embolism444
943, MIVACoA7.24.35.64.1Neuroformyesyesnodistal embolism22lost to FU
hemorrhagic complications
1036, MVPICA5.78.56.24.8Neuroformnoyesnorebleeding1NANA
1147, FIIIPCoA4.26.13.93.5NeuroformyesyesnoIPH (EVD site)333
1250, FIIIICA (dorsal wall)2.710.26.17.3EnterprisenononoIPH (remote, unrelated site)344
1382, FIIIPCoA54.97.75.6Enterprisenoyesnorebleeding1NANA
1481, FIVBA bifurcation6.17.86.68.1EnterpriseyesyesyesIPH (shunt site)21NA

ACoA = anterior communicating artery; BA = basilar artery; FU = follow-up; HC = hydrocephalus; HH = Hunt and Hess; ICA = internal carotid artery; NA = not applicable; PCoA = posterior communicating artery; PICA = posterior inferior cerebellar artery; VM = ventromedial.

Nine patients with thromboembolic complications underwent intraarterial thrombolysis in which a GP IIb/IIIa antagonist (tirofiban) was used; 4 of these patients experienced successful recanalization without any symptoms (Cases 1–4) and 5 had morbid complications (Cases 5–9). Only 1 of these patients experienced severe disability (GOS score of 3), however, whereas the remaining 8 patients had favorable outcomes (GOS score of 4 or 5). Among these 9 patients, there were no hemorrhagic complications related to using the GP IIb/IIIa antagonist. We did not observe any subacute or delayed thromboembolic complications during the follow-up period. Hemorrhagic complications, on the other hand, occurred in 5 patients (6.9%) and were all symptomatic. Two patients experienced rebleeding after partial occlusion of the embolization and another 3 patients experienced IPH (ventriculostomy-related bleeding in 2 and remote unrelated site in 1). These patients experienced unfavorable outcomes (3 patients, including 1 death during the follow-up period) or death (2 patients).

The location of the aneurysm, hydrocephalus, EVD, and types of stents, with a p value of < 0.10 on univariate analysis (p = 0.088, 0.097, 0.053, and 0.075, respectively), were included in multivariate logistic regression analysis to determine independent associations of periprocedural complications with other factors. Use of EVD (OR 1.413, 95% CI 0 .088–2.173; p = 0.046) remained the only independent risk factor for periprocedural complications on multivariate logistic regression analysis (Table 2).

TABLE 2:

Risk factors for periprocedural complications during or after SAC of ruptured wide-necked aneurysms in 72 patients in the acute period

VariableNo. of PatientsPeriprocedural Complications (%)*p Value
YesNoUnivariate AnalysisLogistic Regression (OR, 95% CI)
mean age in yrs, ± SD58.6 ± 14.358.3 ± 11.30.898
sex0.603
 male153 (20.0)12 (80.0)
 female5711 (19.3)46 (80.7)
HH grade0.327
 good5110 (19.6)41 (80.4)
 poor214 (19.0)17 (81.0)
hypertension0.340
 yes358 (22.9)27 (77.1)
 no376 (16.2)31 (83.8)
diabetes0.487
 yes133 (23.1)10 (76.9)
 no5911 (18.6)48 (81.4)
smoking0.575
 yes122 (16.7)10 (83.3)
 no6012 (20.0)48 (80.0)
coronary artery disease0.625
 yes62 (33.3)4 (66.7)
 no6612 (18.2)54 (81.8)
aneurysm location0.0880.149 (0.802, 0.241–3.278)
 anterior circulation4611 (23.9)35 (76.1)
 posterior circulation263 (11.5)23 (88.5)
mean neck size in mm, ± SD4.92 ± 2.525.25 ± 1.840.389
aneurysm size0.126
 very small30 (0)3 (100)
 small303 (10.0)27 (90.0)
 medium258 (32.0)17 (68.0)
 large143 (21.4)11 (78.6)
IPH0.512
 yes81 (12.5)7 (87.5)
 no6413 (20.3)51 (79.7)
HC0.0970.167 (1.285, 0.446–5.812)
 yes308 (26.7)22 (73.3)
 no426 (14.3)36 (85.7)
EVD0.0530.046 (1.413, 0.088–2.173)
 yes3611 (30.6)25 (69.4)
 no363 (8.3)33 (91.7)
types of stents0.0750.081 (1.524, 0.416–2.549)
 Neuroform227 (31.8)15 (68.2)
 Enterprise497 (14.3)42 (85.7)
 Solitaire10 (0)1 (100)

Fourteen patients had complications and 58 did not.

According to the Mann-Whitney U-test.

Immediate postembolization angiographic results showed complete occlusion in 41 patients (56.9%), neck remnant in 20 (27.8%), and partial occlusion in 11 (15.3%). Follow-up angiographic results were obtained in 56 (77.8%) of 72 patients and showed complete occlusion in 38 (67.9%) and neck remnant in 18 (32.1%) of the 56 patients. There was no in-stent stenosis (> 50% stenosis) seen on follow-up angiography. With respect to clinical outcomes, 51 (70.8%) of the 72 patients achieved favorable outcomes at the time of discharge and 51 (83.6%) of the 61 patients (11 were lost to follow-up) achieved favorable outcomes during the follow-up period.

Discussion

The decision to use a stent when performing endovascular treatment for ruptured wide-necked aneurysms is affected not only by the risk of potential thromboembolic complications due to foreign body placement, but also hemorrhagic complications due to antiplatelet therapy. In this study, patients with clinically poor grades or acute hydrocephalus underwent EVD before embolization to reduce the risk of catheter-related hemorrhagic complications due to antiplatelet therapy or anticoagulation. We found that the periprocedural complication rate was 19.4% among 72 patients with ruptured wide-necked aneurysms treated by SAC. The overall procedure-related thromboembolic complication rate was 12.5%; 4 (5.6%) were asymptomatic and 5 (6.9%) were symptomatic. This outweighed the 6.9% risk of hemorrhagic complications, all of which were symptomatic.

During the same period, we treated 1412 patients with unruptured intracranial aneurysms by using endovascular methods. Among them, 459 patients were treated with SAC. There were 36 (7.8%) thromboembolic complications in the acute period; 31 (6.7%) were asymptomatic and 5 (1.1%) were symptomatic. Eight patients (1.7%) had hemorrhagic complications, including 2 patients (0.4%) with fatal hemorrhages. Compared with the complication rates of thromboembolism and hemorrhage in unruptured aneurysms, those of ruptured aneurysms seemed to be higher in this study.

In a recent study, Chalouhi et al.8 concluded that higher complication rates and worse outcomes are associated with SAC of ruptured aneurysms. Similar to our results, they reported that stent insertion for acutely ruptured aneurysms is associated with higher thromboembolic and hemorrhagic complications than stent insertion for unruptured aneurysms (25% vs 4.7%). Additionally, Lessne et al.22 reported thromboembolic complications after Neuroform stent–assisted treatment of cerebral aneurysms in 235 patients with 274 stents. There were 6 (3.1%) thromboembolisms in 194 patients with unruptured aneurysms and 6 (20%) among 30 patients with ruptured aneurysms. Their results suggested that the thromboembolic event rate is low in unruptured aneurysms but is much higher in ruptured aneurysms, probably due to restricted use of antiplatelet therapy. However, Bodily et al.6 concluded that thromboembolic complications were reasonably well controlled and ventriculostomy-related hemorrhagic complications were uncommon in SAC of acutely ruptured aneurysms, even though they found clinically significant intracranial hemorrhagic complications in 8% of patients and clinically significant thromboembolic events in 6%. This might be an inappropriate conclusion because 14% of procedure-related complications would not be acceptable; not if these were clinically significant lesions.

There was a high potential for asymptomatic lesions to become symptomatic lesions. In our study, periprocedural complications were found to be 19.4% and thromboembolic complications outweighed hemorrhagic complications. However, hemorrhagic complications seemed to be more fatal compared with thromboembolic complications. Previous studies showed similar results. Tähtinen et al.30 evaluated outcomes of 61 consecutive patients with acutely ruptured wide-necked aneurysms who were treated with SAC. The technique-related complication rate was 21% (13 of 61), with thromboembolic complications in 9 patients and aneurysm perforations in 4 patients. Amenta et al.1 reported a retrospective study of 65 patients with ruptured wide-necked aneurysms treated with SAC in whom there were 10 (15.38%) major complications associated with bleeding secondary to either antiplatelet therapy or intraoperative in-stent thrombosis (5 patients each, 7.7%). Three patients (4.6%) suffered a fatal hemorrhage.

External ventricular drainage was the only independent risk factor for periprocedural complications in our study. Among the 36 patients who underwent EVD, 11 (30.6%) experienced periprocedural complications; that is, 7 (77.8%) of the 9 who experienced thromboembolic complications and 4 (80%) of the 5 who experienced hemorrhagic complications. During endovascular treatment of intracranial aneurysms, there were many reports about EVD-related thromboembolic complications as well as hemorrhagic complications.

External ventricular drainage is a relatively safe but not risk-free procedure. A meta-analysis of 1790 ventriculostomies regarding the hemorrhage risks related to EVD has revealed a hemorrhage rate of 5.7%, with a clinically significant hemorrhage rate of 0.61%.4 However, in the context of anticoagulant or antiplatelet therapy, ventriculostomy should be considered as a significant risk factor for hemorrhagic complications.28,31 Antiplatelet agents inhibit the coagulation of bleeding from vessels injured by EVD, making the hemorrhage size larger. Kim et al.19 showed the hemorrhage risks associated with SAC. Approximately 6% of their patients developed IPH or subdural hemorrhage while receiving antithrombotic therapy for neutralization of platelet aggregation. These authors found that all hemorrhagic complications in patients with acutely ruptured aneurysms occurred in cases with concomitant ventriculostomy.

Tumialán et al.31 have cautioned on the elevated risk of hemorrhage associated with dual-antiplatelet therapy in patients with EVD. Three (42.9%) of 7 patients in their series experienced ventricular catheter–related hemorrhage. They concluded that the necessity of dual-antiplatelet therapy in the SAC procedure significantly increases the risk of intracranial hemorrhagic complications and possible rebleeding from an incompletely treated aneurysm.

Placement of the EVD catheter prior to coil embolization and initiation of dual-antiplatelet therapy has been suggested, but this is not free from delayed hemorrhagic events.31 According to the same concept, we performed EVD before SAC to reduce the risk of catheter-related hemorrhagic complications in patients with clinically poor grades or acute hydrocephalus. However, we did not reduce the rate of hemorrhagic complications. In addition, we have not used heparin bolus because of the risk of hemorrhagic complications, and it may be connected to the increment rate of thromboembolic complications. When hemorrhagic complications occurred, we discontinued clopidogrel while continuing aspirin because abrupt cessation of dual-antiplatelet therapy may increase the risk of stent occlusion. Fortunately, we did not experience stent-related thromboembolic complications after cessation of clopidogrel in our cases with hemorrhagic complications. However, Kim et al.19 reported that 2 of the 4 symptomatic patients who were removed from dual-antiplatelet therapy after hemorrhage actually developed occlusion of the stent site, with newly developed infarction in the corresponding arterial territory. Therefore, cessation of all antiplatelet agents is not advisable unless a hemorrhage would be fatal.

The term “hypercoagulability” has been used to describe an elevated risk of pathological thrombus formation.3 During the postoperative period, patients with ruptured intracranial aneurysms are in a hypercoagulable state not only because of the surgical procedure, but also because SAH in the acute period triggers the coagulation cascade. In patients with intracerebral lesions, a major surgical complication is the high incidence of thromboembolic events,17 including life-threatening pulmonary embolisms.15 Lessne et al.22 showed that acute SAH before stent placement proved to be a risk factor for subsequent thromboembolic events. Cronqvist et al.11 reasoned that patients who have SAH might demonstrate an increased thromboembolic rate after coil embolization compared with patients who have unruptured aneurysms, so it follows that the thromboembolic rate in ruptured aneurysms after SAC would be higher as well. Colwell et al.10 assessed activity of the coagulation cascade in patients undergoing surgical procedures by measuring thrombin generation. They demonstrated that thrombin production was significantly increased, confirming a hypercoagulable postoperative state.

In addition, not only does the intracranial stent activate platelet function and potentially trigger thromboembolism, but the additional step of stent placement adds to the length of the procedure and increases the amount of time in which the patient is exposed to platinum, which could also increase the risk of thromboembolic complications. This might explain why EVD was related to thromboembolic complications in patients with ruptured intracranial aneurysms treated by SAC. Thus, it is possible that SAC with EVD increases the risk of periprocedural thromboembolic complications as well as hemorrhagic complications. In patients requiring EVD, microsurgical clipping may be a more appropriate first-line treatment option. To avoid hemorrhagic complications other endovascular techniques should also be considered, such as the multiple-catheter technique or balloon-assisted coil insertion.

Our overall clinical outcomes at the time of discharge (70.8% with favorable outcomes) and during follow-up (83.6% with favorable outcomes) are similar to those of previous studies.1,25,27 Use of the SAC procedure has achieved excellent occlusion of the aneurysms and decreased the rates of angiographic recurrence.12,27 In this study, follow-up angiographic results (mean 14.8 months) showed that 67.9% of aneurysms were completely occluded, which was improved compared with the immediate postembolization angiographic results (56.9% with complete occlusion). In addition, long-term angiographic follow-up is important with regard to the risk of delayed in-stent stenosis and durability. There were no cases of in-stent stenosis during the mean follow-up period of 15 months.

Intracranial stents for aneurysm treatment have low radial force compared with stents for atherosclerotic disease, so that healthy, nonatherosclerotic vessels that are not traumatized during stent placement would have lower in-stent stenosis rates. However, in-stent stenosis of aneurysm stents has been reported and is still considerable. Fiorella et al.13 reported that 9 (5.8%) of 156 patients who were followed after treatment with SAC were found to have delayed in-stent stenosis, and 2 were symptomatic. Biondi et al.5 published a prospective study of 45 aneurysms treated with 47 Neuroform stents. Angiographic follow-up was available for 33 of 45 treated aneurysms, with a mean interval of 9 months. Only 1 patient developed significant in-stent stenosis (3% of patients with imaging follow-up), which was asymptomatic.

There are several limitations to this study. First, this is a retrospective study without randomization, and there was not a true control group for comparison of the effects of antiplatelet agents on thromboembolic as well as hemorrhagic complications.

Second, the individual response to each antiplatelet agent was not evaluated. A recent study on coronary intervention suggested that 30% of patients demonstrate relative clopidogrel resistance.26 Thus, there was probably a subset of patients who were insufficiently treated with antiplatelet agents. For patients with ruptured aneurysms, we did not have sufficient time to test for responses to aspirin and clopidogrel. However, we should have tried to identify patients with a higher risk of thromboembolic complications. Antiplatelet therapy before SAC, based on results from coronary intervention, is considered to be the standard of care and has been shown to be effective in reducing the number of periprocedural thromboembolic complications.14,16,29,33 Oral pretreatment with antiplatelet agents or loading with aspirin and clopidogrel at the time of intervention appears to be sufficient prophylaxis5,13 and does not increase the hemorrhagic complication rate.33 However, we found high rates of periprocedural thromboembolic and hemorrhagic complications in patients on dual-antiplatelet therapy in this study, so that the results of those previously published studies could not be applied to acutely ruptured aneurysms.

Third, we did not monitor ACT because we mixed heparin with saline flushes during the procedure rather than using heparin boluses. Our data indicated that hemorrhagic complications might have been traded for thromboembolic complications by not using procedural heparin. In addition, varied individual responses to anticoagulation therapy could have affected the risk of thromboembolic and hemorrhagic complications. To date, there are no standardized anticoagulation therapies for patients with ruptured aneurysms. Most of the previous studies did not routinely administer anticoagulants prior to the procedure, although most patients did receive intraprocedural heparin for SAC performed in the setting of acutely ruptured aneurysms.1,8,18,22,30 In most patients with ruptured aneurysms, only after several coils had entered the aneurysm would full heparinization take place, with a goal ACT of approximately 250 seconds.18,30 Chalouhi et al.8 gave patients intraprocedural clopidogrel (600 mg) and a heparin bolus (50 U/kg) after delivery of the first coil. However, they could not avoid periprocedural thromboembolic complications. Proper anticoagulation therapy in acutely ruptured aneurysms is still controversial because hemorrhagic complications are more often fatal compared with thromboembolic complications.

Finally, we did not assess activity of the coagulation cascade. Estimation of an individual's potential to generate thrombin may correlate closely with a hypercoagulable state, which may have supported our results. Therefore, monitoring changes in prothrombin time, partial thromboplastin time, or thrombin generation10 may help to predict periprocedural complications.

Conclusions

The periprocedural complication rate during SAC was 19.4% among 72 patients with ruptured wide-necked aneurysms in the acute period, and EVD was found to be an independent risk factor for periprocedural complications. Because of the high complication rate, microsurgical clipping or endovascular treatment with another technique (multiple-microcatheter or balloon-assisted technique) may be a more appropriate option for first-line treatment than SAC, especially in patients with poor clinical grades or acute hydrocephalus who are likely to require EVD.

Disclosure

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author contributions to the study and manuscript preparation include the following. Conception and design: Shin, Chung, Lim. Acquisition of data: Chung, Lim, Shim, BS Kim. Analysis and interpretation of data: Chung, Lim, Suh, YB Kim, BS Kim. Drafting the article: Chung. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Shin. Statistical analysis: Chung, YB Kim. Study supervision: Shin.

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    Chung JKim YBHong CKJoo JYShin YSLim YC: Stent salvage using the Enterprise stent for procedure-related complication during coil embolization of ruptured intracranial aneurysms. Acta Neurochir (Wien) 155:2232292013

  • 10

    Colwell ASReish RGKuter DJDamjanovic BAusten WG JrFogerty AE: Abdominal contouring procedures increase activity of the coagulation cascade. Ann Plast Surg 69:1291332012

  • 11

    Cronqvist MWirestam RRamgren BBrandt LNilsson OSäveland H: Diffusion and perfusion MRI in patients with ruptured and unruptured intracranial aneurysms treated by endovascular coiling: complications, procedural results, MR findings and clinical outcome. Neuroradiology 47:8558732005

  • 12

    Fargen KMHoh BLWelch BGPride GLLanzino GBoulos AS: Long-term results of enterprise stent-assisted coiling of cerebral aneurysms. Neurosurgery 71:2392442012

  • 13

    Fiorella DAlbuquerque FCWoo HRasmussen PAMasaryk TJMcDougall CG: Neuroform in-stent stenosis: incidence, natural history, and treatment strategies. Neurosurgery 59:34422006

  • 14

    Fiorella DThiabolt LAlbuquerque FCDeshmukh VRMcDougall CGRasmussen PA: Antiplatelet therapy in neuroendovascular therapeutics. Neurosurg Clin N Am 16:517540vi2005

  • 15

    Heesen MWinking MKemkes-Matthes BDeinsberger WDietrich GVMatthes KJ: What the neurosurgeon needs to know about the coagulation system. Surg Neurol 47:32341997

  • 16

    Hwang GJung CPark SQKang HSLee SHOh CW: Thromboembolic complications of elective coil embolization of unruptured aneurysms: the effect of oral antiplatelet preparation on periprocedural thromboembolic complication. Neurosurgery 67:7437482010

  • 17

    Inci SErbengi ABerker M: Pulmonary embolism in neurosurgical patients. Surg Neurol 43:1231291995

  • 18

    Kanaan HJankowitz BAleu AKostov DLin RLee K: In-stent thrombosis and stenosis after neck-remodeling device-assisted coil embolization of intracranial aneurysms. Neurosurgery 67:152315332010

  • 19

    Kim DJSuh SHKim BMKim DIHuh SKLee JW: Hemorrhagic complications related to the stent-remodeled coil embolization of intracranial aneurysms. Neurosurgery 67:73792010

  • 20

    Kwon OKKim SHKwon BJKang HSKim JHOh CW: Endovascular treatment of wide-necked aneurysms by using two microcatheters: techniques and outcomes in 25 patients. AJNR Am J Neuroradiol 26:8949002005

  • 21

    Kwon OKKim SHOh CWHan MHKang HSKwon BJ: Embolization of wide-necked aneurysms with using three or more microcatheters. Acta Neurochir (Wien) 148:113911452006

  • 22

    Lessne MLShah PAlexander MJBarnhart HXPowers CJGolshani K: Thromboembolic complications after Neuroform stent-assisted treatment of cerebral aneurysms: the Duke Cerebrovascular Center experience in 235 patients with 274 stents. Neurosurgery 69:3693752011

  • 23

    Malek AMHalbach VVPhatouros CCLempert TEMeyers PMDowd CF: Balloon-assist technique for endovascular coil embolization of geometrically difficult intracranial aneurysms. Neurosurgery 46:139714072000

  • 24

    Mocco JSnyder KVAlbuquerque FCBendok BRAlan SBCarpenter JS: Treatment of intracranial aneurysms with the Enterprise stent: a multicenter registry. Clinical article. J Neurosurg 110:35392009

  • 25

    Molyneux AJKerr RSBirks JRamzi NYarnold JSneade M: Risk of recurrent subarachnoid haemorrhage, death, or dependence and standardised mortality ratios after clipping or coiling of an intracranial aneurysm in the International Subarachnoid Aneurysm Trial (ISAT): long-term follow-up. Lancet Neurol 8:4274332009

  • 26

    Nguyen TADiodati JGPharand C: Resistance to clopidogrel: a review of the evidence. J Am Coll Cardiol 45:115711642005

  • 27

    Piotin MBlanc RSpelle LMounayer CPiantino RSchmidt PJ: Stent-assisted coiling of intracranial aneurysms: clinical and angiographic results in 216 consecutive aneurysms. Stroke 41:1101152010

  • 28

    Ross IBDhillon GS: Ventriculostomy-related cerebral hemorrhages after endovascular aneurysm treatment. AJNR Am J Neuroradiol 24:152815312003

  • 29

    Steinhubl SRBerger PBMann JT IIIFry ETDeLago AWilmer C: Early and sustained dual oral antiplatelet therapy following percutaneous coronary intervention: a randomized controlled trial. JAMA 288:241124202002

  • 30

    Tähtinen OIVanninen RLManninen HIRautio RHaapanen ANiskakangas T: Wide-necked intracranial aneurysms: treatment with stent-assisted coil embolization during acute (<72 hours) subarachnoid hemorrhage—experience in 61 consecutive patients. Radiology 253:1992082009

  • 31

    Tumialán LMZhang YJCawley CMDion JETong FCBarrow DL: Intracranial hemorrhage associated with stent-assisted coil embolization of cerebral aneurysms: a cautionary report. J Neurosurg 108:112211292008

  • 32

    von Beckerath NTaubert DPogatsa-Murray GSchömig EKastrati ASchömig A: Absorption, metabolization, and antiplatelet effects of 300-, 600-, and 900-mg loading doses of clopidogrel: results of the ISAR-CHOICE (Intracoronary Stenting and Antithrombotic Regimen: Choose Between 3 High Oral Doses for Immediate Clopidogrel Effect) Trial. Circulation 112:294629502005

  • 33

    Yamada NKCross DT IIIPilgram TKMoran CJDerdeyn CPDacey RG Jr: Effect of antiplatelet therapy on thromboembolic complications of elective coil embolization of cerebral aneurysms. AJNR Am J Neuroradiol 28:177817822007

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Article Information

Address correspondence to: Yong Sam Shin, M.D., Ph.D., Department of Neurosurgery, Seoul St. Mary's Hospital, The Catholic University of Korea, 505 Banpo-Dong, Seocho-Gu, Seoul 137-701, Republic of Korea. email: nsshin@catholic.ac.kr.

Please include this information when citing this paper: published online May 16, 2014; DOI: 10.3171/2014.4.JNS131662.

© AANS, except where prohibited by US copyright law.

Headings

References

1

Amenta PSDalyai RTKung DToporowski AChandela SHasan D: Stent-assisted coiling of wide-necked aneurysms in the setting of acute subarachnoid hemorrhage: experience in 65 patients. Neurosurgery 70:141514292012

2

Benitez RPSilva MTKlem JVeznedaroglu ERosenwasser RH: Endovascular occlusion of wide-necked aneurysms with a new intracranial microstent (Neuroform) and detachable coils. Neurosurgery 54:135913682004

3

Bick RLPegram M: Syndromes of hypercoagulability and thrombosis: a review. Semin Thromb Hemost 20:1091321994

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Binz DDToussaint LG IIIFriedman JA: Hemorrhagic complications of ventriculostomy placement: a meta-analysis. Neurocrit Care 10:2532562009

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Biondi AJanardhan VKatz JMSalvaggio KRiina HAGobin YP: Neuroform stent-assisted coil embolization of wide-neck intracranial aneurysms: strategies in stent deployment and midterm follow-up. Neurosurgery 61:4604692007

6

Bodily KDCloft HJLanzino GFiorella DJWhite PMKallmes DF: Stent-assisted coiling in acutely ruptured intracranial aneurysms: a qualitative, systematic review of the literature. AJNR Am J Neuroradiol 32:123212362011

7

Cekirge HSYavuz KGeyik SSaatci I: HyperForm balloon remodeling in the endovascular treatment of anterior cerebral, middle cerebral, and anterior communicating artery aneurysms: clinical and angiographic follow-up results in 800 consecutive patients. Clinical article. J Neurosurg 114:9449532011

8

Chalouhi NJabbour PSinghal SDrueding RStarke RMDalyai RT: Stent-assisted coiling of intracranial aneurysms: predictors of complications, recanalization, and outcome in 508 cases. Stroke 44:134813532013

9

Chung JKim YBHong CKJoo JYShin YSLim YC: Stent salvage using the Enterprise stent for procedure-related complication during coil embolization of ruptured intracranial aneurysms. Acta Neurochir (Wien) 155:2232292013

10

Colwell ASReish RGKuter DJDamjanovic BAusten WG JrFogerty AE: Abdominal contouring procedures increase activity of the coagulation cascade. Ann Plast Surg 69:1291332012

11

Cronqvist MWirestam RRamgren BBrandt LNilsson OSäveland H: Diffusion and perfusion MRI in patients with ruptured and unruptured intracranial aneurysms treated by endovascular coiling: complications, procedural results, MR findings and clinical outcome. Neuroradiology 47:8558732005

12

Fargen KMHoh BLWelch BGPride GLLanzino GBoulos AS: Long-term results of enterprise stent-assisted coiling of cerebral aneurysms. Neurosurgery 71:2392442012

13

Fiorella DAlbuquerque FCWoo HRasmussen PAMasaryk TJMcDougall CG: Neuroform in-stent stenosis: incidence, natural history, and treatment strategies. Neurosurgery 59:34422006

14

Fiorella DThiabolt LAlbuquerque FCDeshmukh VRMcDougall CGRasmussen PA: Antiplatelet therapy in neuroendovascular therapeutics. Neurosurg Clin N Am 16:517540vi2005

15

Heesen MWinking MKemkes-Matthes BDeinsberger WDietrich GVMatthes KJ: What the neurosurgeon needs to know about the coagulation system. Surg Neurol 47:32341997

16

Hwang GJung CPark SQKang HSLee SHOh CW: Thromboembolic complications of elective coil embolization of unruptured aneurysms: the effect of oral antiplatelet preparation on periprocedural thromboembolic complication. Neurosurgery 67:7437482010

17

Inci SErbengi ABerker M: Pulmonary embolism in neurosurgical patients. Surg Neurol 43:1231291995

18

Kanaan HJankowitz BAleu AKostov DLin RLee K: In-stent thrombosis and stenosis after neck-remodeling device-assisted coil embolization of intracranial aneurysms. Neurosurgery 67:152315332010

19

Kim DJSuh SHKim BMKim DIHuh SKLee JW: Hemorrhagic complications related to the stent-remodeled coil embolization of intracranial aneurysms. Neurosurgery 67:73792010

20

Kwon OKKim SHKwon BJKang HSKim JHOh CW: Endovascular treatment of wide-necked aneurysms by using two microcatheters: techniques and outcomes in 25 patients. AJNR Am J Neuroradiol 26:8949002005

21

Kwon OKKim SHOh CWHan MHKang HSKwon BJ: Embolization of wide-necked aneurysms with using three or more microcatheters. Acta Neurochir (Wien) 148:113911452006

22

Lessne MLShah PAlexander MJBarnhart HXPowers CJGolshani K: Thromboembolic complications after Neuroform stent-assisted treatment of cerebral aneurysms: the Duke Cerebrovascular Center experience in 235 patients with 274 stents. Neurosurgery 69:3693752011

23

Malek AMHalbach VVPhatouros CCLempert TEMeyers PMDowd CF: Balloon-assist technique for endovascular coil embolization of geometrically difficult intracranial aneurysms. Neurosurgery 46:139714072000

24

Mocco JSnyder KVAlbuquerque FCBendok BRAlan SBCarpenter JS: Treatment of intracranial aneurysms with the Enterprise stent: a multicenter registry. Clinical article. J Neurosurg 110:35392009

25

Molyneux AJKerr RSBirks JRamzi NYarnold JSneade M: Risk of recurrent subarachnoid haemorrhage, death, or dependence and standardised mortality ratios after clipping or coiling of an intracranial aneurysm in the International Subarachnoid Aneurysm Trial (ISAT): long-term follow-up. Lancet Neurol 8:4274332009

26

Nguyen TADiodati JGPharand C: Resistance to clopidogrel: a review of the evidence. J Am Coll Cardiol 45:115711642005

27

Piotin MBlanc RSpelle LMounayer CPiantino RSchmidt PJ: Stent-assisted coiling of intracranial aneurysms: clinical and angiographic results in 216 consecutive aneurysms. Stroke 41:1101152010

28

Ross IBDhillon GS: Ventriculostomy-related cerebral hemorrhages after endovascular aneurysm treatment. AJNR Am J Neuroradiol 24:152815312003

29

Steinhubl SRBerger PBMann JT IIIFry ETDeLago AWilmer C: Early and sustained dual oral antiplatelet therapy following percutaneous coronary intervention: a randomized controlled trial. JAMA 288:241124202002

30

Tähtinen OIVanninen RLManninen HIRautio RHaapanen ANiskakangas T: Wide-necked intracranial aneurysms: treatment with stent-assisted coil embolization during acute (<72 hours) subarachnoid hemorrhage—experience in 61 consecutive patients. Radiology 253:1992082009

31

Tumialán LMZhang YJCawley CMDion JETong FCBarrow DL: Intracranial hemorrhage associated with stent-assisted coil embolization of cerebral aneurysms: a cautionary report. J Neurosurg 108:112211292008

32

von Beckerath NTaubert DPogatsa-Murray GSchömig EKastrati ASchömig A: Absorption, metabolization, and antiplatelet effects of 300-, 600-, and 900-mg loading doses of clopidogrel: results of the ISAR-CHOICE (Intracoronary Stenting and Antithrombotic Regimen: Choose Between 3 High Oral Doses for Immediate Clopidogrel Effect) Trial. Circulation 112:294629502005

33

Yamada NKCross DT IIIPilgram TKMoran CJDerdeyn CPDacey RG Jr: Effect of antiplatelet therapy on thromboembolic complications of elective coil embolization of cerebral aneurysms. AJNR Am J Neuroradiol 28:177817822007

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