Introduction Endovascular coiling is a valid treatment option for poor-grade ruptured aneurysms. However, little is known about stent-assisted coiling of poor-grade aneurysms.
Objective To compare the safety and efficacy of stent-assisted coiling with coiling alone for poor-grade aneurysms.
Methods Using multicenter data on poor-grade aneurysms, we performed a retrospective analysis of 131 consecutive patients treated with endovascular coiling within 14 days after ictus. Patients were split into two groups: stent-assisted coiling and coiling alone. Baseline characteristics, immediate angiographic results, perioperative complications, and clinical outcomes were compared between the two groups.
Results Twenty-three (17.6%) patients were treated with stent-assisted coiling and 108 (82.4%) with coiling alone. There were no statistically significant differences in patient age, sex, clinical grade, Fisher grade, modified Fisher grade, aneurysm location, and size between the stent-assisted coiling and coiling alone groups. Intraprocedural aneurysm rupture, procedure-related ischemic complication, external ventricular drainage-related hemorrhagic complication, and symptomatic vasospasm did not differ between the two groups. Immediate angiographic results and clinical outcomes at discharge and at 6 and 12 months did not differ between the groups. Aneurysm rebleeding occurred in 4 (17.4%) patients after stent-assisted coiling compared with 2 (1.9%) patients after coiling alone (p<0.007). Multivariate analysis showed that incomplete aneurysm occlusion was independently associated with aneurysm rebleeding (p=0.016), and there was a trend toward aneurysm rebleeding after stent-assisted coiling (p=0.051).
Conclusions Stent-assisted coiling of poor-grade aneurysms is feasible and safe compared with coiling alone. However, the hemorrhagic complication and aneurysm rebleeding may not be negligible.
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Poor-grade ruptured intracranial aneurysms are associated with high rates of morbidity and mortality. In the past, aggressive surgical treatment was proposed to improve outcomes in selected patients.1–3 More recently, endovascular treatment has been recognized as a feasible and reasonable option for poor-grade ruptured aneurysms.4–6 With advances in endovascular technology, stent-assisted coiling has been used in the treatment of ruptured aneurysms. However, few poor-grade aneurysms were included in these studies.7–9
Unlike patients with good-grade ruptured aneurysms, patients with poor-grade aneurysms more often present with acute hydrocephalus, severe intraventricular hemorrhage, microcirculatory disturbances, and multiorgan failure.10 ,11 However, no study has reported the safety and efficacy of stent-assisted coiling of poor-grade ruptured aneurysms.7 ,12 ,13 In this report, we describe a retrospective analysis of consecutive patients with poor-grade aneurysms treated with endovascular coiling using data from a multicenter poor-grade aneurysm study (AMPAS). We compared immediate angiographic results, perioperative complications, and clinical outcomes between groups receiving stent-assisted coiling or coiling alone.
The AMPAS was a prospective, multicenter, and observational registry of consecutive patients who presented with poor-grade ruptured aneurysms. This study protocol was approved by the Chinese Ethics Committee of Registering Clinical Trials. Details of the registry have been published elsewhere.14 ,15 Poor-grade aneurysms were defined as a World Federation of Neurosurgical Societies (WFNS) grade of IV or V after subarachnoid hemorrhage. Between October 2010 and March 2012, 136 consecutive patients who presented with poor-grade aneurysms at the time of treatment and were treated with endovascular coiling were identified from the registry. Of the 136 patients, five underwent endovascular coiling after 14 days and were excluded. Finally, 131 patients with poor-grade aneurysms were included. We collected the following data: patient age, sex, medical history, Glasgow Coma Score and WFNS grade before coiling, Fisher grade and modified Fisher grade before coiling, aneurysm characteristics, timing of coiling, immediate angiographic results, external ventricular drainage (EVD), perioperative complications, and clinical outcomes at discharge and at 6 and 12 months.
The treatment protocol for poor-grade aneurysms, including aggressive resuscitation, early CT angiography or cerebral angiography, multidisciplinary team consultation, early aneurysm treatment, and intensive critical care treatment, has been described previously.14–17 All patients were treated under general anesthesia and systemic heparinization. Stent-assisted coiling was considered in ruptured aneurysms with an unfavorable morphology (aneurysm neck ≥4.0 mm or dome/neck ≤2.0). Procedural techniques and the choice of stent type were based on individual centers. Balloon-assisted coiling was not used in this study.
Anticoagulation and antiplatelet therapy regimens
A bolus of 50 IU/kg of heparin was given after femoral artery sheath placement. Activated clotting time was maintained at two to three times the baseline level. For stent placement, 75 mg of clopidogrel and 100 mg of aspirin were administered daily at least 3 days. For emergency stent placement, a loading dose of 300–450 mg clopidogrel was recommended to be administered by a nasogastric tube or rectally before 2 h of the procedure. After the procedure, 100 mg of aspirin and 75 mg of clopidogrel were given daily for 6–12 weeks, and 100 mg of aspirin was given for at least 12 months. Antiplatelet therapy was routinely prescribed according to individual institutional standards of practice. The individual response to antiplatelet agents was not measured. No patients undergoing EVD placement received platelet infusion during the study.
The outcome measures were immediate angiographic results, perioperative complications, and clinical outcomes. Immediate aneurysm occlusion was assessed using the Raymond grade. Incomplete occlusion was defined as residual neck or dome filling on the final angiography. Perioperative complications included intraprocedural rupture, procedure-related ischemic event, EVD-related hemorrhagic event, aneurysm rebleeding, and symptomatic vasospasm. Clinical outcomes at discharge and at 6 and 12 months were assessed by independent neurosurgeons using the modified Rankin Scale (mRS).
Statistical analysis was conducted with IBM SPSS V.22.0 (IBM SPSS; Armonk, New York, USA). Patient and aneurysm characteristics were compared between stent-assisted coiling and coiling alone groups. An independent samples t test, a χ2 test, and Fisher's exact test were used, as appropriate. No adjustment for multiple comparisons was made to determine the effect of stent-assisted coiling on outcomes because patient and aneurysm characteristics were similar between the two groups, except for aneurysm neck size and timing of treatment. Univariate logistic analysis was used to assess the association between clinical variables and aneurysm rebleeding. Clinical variables with a p value <0.10 in the univariate analysis were entered into the multivariate logistic regression model to assess independent predictors of aneurysm rebleeding using the backward method. The OR and 95% CI were calculated. A p value <0.05 was considered to be statistically significant.
Of the 131 patients, 61 (46.6%) patients were female. The mean age was 54.6±11.9 years (range 23–75). The mean size of the ruptured aneurysm was 5.8±2.9 mm (range 2.0–22.0). Twenty-three (17.6%) patients were treated with stent-assisted coiling and 108 patients (82.4%) were treated with coiling alone. Baseline characteristics between stent-assisted coiling and coiling alone groups are presented in table 1. There were no statistically significant differences in patient age, sex, histories of smoking and hypertension, Glasgow Coma Score and WFNS grade before coiling, Fisher grade and modified Fisher grade before coiling, aneurysm location and aneurysm size, and EVD placement between the two groups. Wider-neck aneurysms were more often treated with stent-assisted coiling (p=0.010). Stent-assisted coiling was more often performed after 72 h compared with coiling alone (p=0.041).
Immediate angiographic results
Immediate angiographic results are presented in table 2.Immediate complete occlusion was achieved in 18 (78.3%) aneurysms in the stent-assisted coiling group and in 96 (88.9%) aneurysms in the coiling group, without statistically significant difference (p=0.168).There were no statistically significant differences in rates of residual neck and dome filling between the two groups.
Perioperative complications are presented in table 2. Aneurysm rebleeding occurred in four (17.4%) of patients in the stent-assisted coiling group and in two (1.9%) patients in the coiling group (p=0.007). There were no statistically significant differences in intraprocedural rupture, procedure-related ischemic complication, and symptomatic vasospasm between the two groups (table 2). Of the six patients with aneurysm rebleeding, three were female with a median age of 61 years (range 44–68). The median size of the aneurysms was 6.0 mm (range 3.5–22.0) and the median neck size of the aneurysms was 4.1 mm (range 3.5–7.0). Four aneurysms were anterior communicating artery aneurysms, and two were posterior communicating artery aneurysms. Incomplete aneurysm occlusion occurred in three patients as shown by angiography. Rebleeding occurred in four patients within 3 days after coiling and occurred in one patient at 6 days after coiling. The time of the rebleeding was missing in one patient. Two patients had experienced rebleeding before coiling. EVD-related hemorrhagic complication occurred in one (4.3%) patient in the stent-assisted coiling group compared with two (1.9%) patients in the coiling alone group; the difference was not significant (p=0.287). All three patients underwent EVD placement after coiling and did not receive platelet infusion. Two patients experienced both aneurysm rebleeding and a hemorrhagic complication.
Clinical outcomes at discharge and at 6 and 12 months are presented in table 3. There were no statistically significant differences in clinical outcomes (mRS 0–2, mRS 3–5, and death) between the stent-assisted coiling group and the coiling alone group.
Multivariate analysis for risk factors of aneurysm rebleeding
Results of univariate and multivariate analyses for aneurysm rebleeding are presented in table 4. A larger aneurysm (p=0.018), a wider-neck aneurysm (p=0.006), stent-assisted coiling (p=0.007), and incomplete aneurysm occlusion (p=0.006) were associated with aneurysm rebleeding. There was a trend toward aneurysm rebleeding in patients with a higher modified Fisher grade (p=0.072). The multivariate analysis showed that incomplete aneurysm occlusion was an independent predictor of aneurysm rebleeding (OR=12.37, 95% CI 1.60 to 95.79, p=0.016).There were trends toward aneurysm rebleeding in patients with a larger aneurysm (p=0.057) and in those treated with stent-assisted coiling (p=0.051).
Although no study has focused on stent-assisted coiling of poor-grade ruptured aneurysms, several case series have mentioned that a very small number of poor-grade aneurysms were treated in this way.8 ,9 ,13 Using a multicenter prospective registry data, our study showed that there were no statistically significant differences in intraprocedural rupture, procedure-related ischemic complication, EVD-related hemorrhagic complication, and symptomatic vasospasm between the stent-assisted coiling group and the coiling alone group. The immediate angiographic results and clinical outcomes at discharge and at 6 and 12 months were similar between the two groups. However, there was a trend toward aneurysm rebleeding in the stent-assisted coiling group. Our results suggest that poor-grade aneurysms can be safely and feasibly treated with stent-assisted coiling compared with coiling alone; however, aneurysm rebleeding may not be negligible with the former method.
Our results showed that stent-assisted coiling was more often performed after 72 h compared with coiling alone. Patients were treated late probably because of delayed referral or antiplatelet preparation. In addition, patient clinical condition, aneurysm complexity, and family decision-making might also affect the timing of treatment. Our results also showed that perioperative complications were similar between stent-assisted coiling and coiling alone groups, except for a trend toward aneurysm rebleeding in the former group. This results are consistent with a recent study showing that procedure-related complications did not differ between stent-assisted coiling of ruptured aneurysms and coiling alone groups.7
We found that EVD-related hemorrhagic complication occurred in one (4.3%) patient after stent-assisted coiling. Previous studies have shown that the hemorrhagic complication more often occurred in patients with acutely ruptured aneurysms after stent-assisted coiling and ventricular drainage probably because of dual antiplatelet therapy.18–20 However, the underlying reason could not be verified in our report because dual antiplatelet therapy was not systematically recorded in all patients. Surgeon's procedure and patient condition might also influence the incidence of the hemorrhagic complication. It is still unknown whether stent-assisted coiling and EVD placement may affect the risk of hemorrhage. Bodily et al21 performed a systematic review of stent-assisted coiling in acutely ruptured aneurysms and found that EVD procedure-related hemorrhagic complication was uncommon. Although our results showed that stent-assisted coiling did not increase the rate of EVD-related hemorrhagic complication compared with coiling alone, the hemorrhagic complication should be considered when patients require EVD or a ventricular peritoneal shunt.
A trend toward aneurysm rebleeding was found in the stent-assisted coiling group, probably because of incomplete aneurysm occlusion. Tähtinen et al9 reported that one of 17 patients with poor-grade aneurysms experienced aneurysm rebleeding after a partial occlusion of stent-assisted coiling. Bechan et al13 reported that early rebleeding occurred in two of 18 patients with poor-grade aneurysms treated with stent-assisted coiling. A larger aneurysm and a wider-neck aneurysm were more often treated with stent-assisted coiling, which resulted in a relatively higher rate of incomplete occlusion than with coiling alone. Our multivariate analysis confirmed that incomplete aneurysm occlusion was independently associated with an increased risk of aneurysm rebleeding. This finding is in agreement with previous studies showing that the incomplete occlusion of aneurysms increases the risk of postoperative rebleeding.22 ,23 These results suggest that development of newer devices and techniques aimed at treating poor-grade ruptured aneurysms is needed to improve immediate angiographic outcomes.
Our results are in line with the study of Yang et al,7 who showed similar clinical outcomes for ruptured aneurysms in the stent-assisted coiling and coiling alone groups. A systematic review suggested that clinical outcomes after stent-assisted coiling of acutely ruptured aneurysms were likely worse than those after coiling alone21; however, there were no data available for the comparison. Chung et al18 reported that the periprocedural complication occurred in 14 (19.4%) of 72 patients with acutely ruptured wide-necked aneurysms during stent-assisted coiling. Although their study suggested that microsurgical clipping or endovascular treatment with a multiple-microcatheter or balloon-assisted technique may be a more appropriate option for patients with ruptured wide-necked aneurysms, especially in patients requiring EVD, they did not report clinical outcomes. In addition, a recent study reported that 211 patients with acutely ruptured aneurysms were treated with stent-assisted coiling, and their results suggested that angiographic and clinical outcomes were similar to those reported using coiling alone or balloon-assisted coiling.24 Therefore, stent-assisted coiling of poor-grade ruptured aneurysms is safe and feasible compared with coiling alone. However, surgical treatment is still a valuable treatment in these patients. A multidisciplinary consultation may help treatment-decision making.15
Although we used a multicenter prospective registry data, this study has several limitations. First, only a small number of patients were treated with stent-assisted coiling. Use of dual antiplatelet therapy was not recorded, and the association between EVD-related hemorrhagic complication and antiplatelet therapy is unknown. Second, this was a retrospective analysis with no randomization. It is difficult to avoid selection bias. However, it is impossible to randomize patients to stent-assisted coiling or to coiling alone because wider-neck aneurysms often require stent assistance. In our report, patient and aneurysm characteristics were comparable between the two groups. Third, we did not have follow-up angiographic results because patients with poor-grade aneurysms have a poor outcome and most of them could not undergo angiographic examinations. Several studies have shown that stent-assisted coiling improves aneurysm occlusion rate and achieves a lower rate of aneurysm recurrence because of more progressive thrombosis after the initial treatment.7 ,12 ,25 Follow-up angiographic results may be better than the initial results after stent-assisted coiling.
Patients treated with stent-assisted coiling and those undergoing coiling alone had similar perioperative complications, immediate angiographic results, and clinical outcomes. These results suggest that stent-assisted coiling may be feasible and safe treatment option for poor-grade ruptured aneurysms. Incomplete aneurysm occlusion was independently associated with aneurysm rebleeding after coiling of poor-grade aneurysms. There was a trend toward aneurysm rebleeding after stent-assisted coiling, which may not be negligible. However, the relationship between EVD-related hemorrhagic complications and endovascular therapy is unknown and requires further study.
Collaborators AMPAS study group: Hongqi Zhang, MD, Xuan Wu Hospital, Capital Medical University; Chuansheng Liang, MD, the first hospital of China Medical University; Huaizhang Shi, MD, the first affiliated hospital of Harbin Medical University; Jing Xu, MD, the second affiliated Hospital, School of Medicine, Zhejiang University; Li Pan, MD, Wuhan General Hospital of Guangzhou Command; Xin Zhang, MD, Nanjing General Hospital of Nanjing Command; Gang Zhu, MD, West South Hospital, the Third Military Medical University; Jianping Deng, MD, Tang Du Hospital, the Fourth Military Medical University; Zhigang Wang, MD, the second affiliated Hospital, School of Medicine, Shandong University.
Contributors BZ and MZ were principal investigators and had the idea for the study and protocol design. BZ, XT, HY, and MZ were involved in data analysis and implementation. BZ, KZ, ZL, and YX were involved in data collection, data verification, and data implementation. BZ drafted the manuscript. XT, HY, and MZ critically reviewed the manuscript. All authors read and approved the final manuscript.
Funding This work was supported by the Chinese Ministry of Health (grant WKJ2010-2-016), the Ministry of Science and Technology of China (grant 2011BAI08B06), and Wenzhou Bureau of Science and Technology (grant Y20090005).
Competing interests None declared.
Patient consent Obtained.
Ethics approval The study was approved by the Chinese Ethics Committee of Registering Clinical Trials.
Provenance and peer review Not commissioned; externally peer reviewed.
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