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Abstract
Background Intracranial aneurysms are increasingly treated with endovascular treatment. Based on our observation that cerebral complications are associated with this treatment, we predict that the number of intraprocedural complications will rise as a result of this trend.
Methods Between January 2007 and December 2013, 1739 patients underwent 1764 detachable coil embolizations to treat intracranial aneurysms (637 ruptured and 1127 unruptured). We reviewed their records and images to evaluate the periprocedural complications and related morbidity and mortality.
Results 61 complications occurred during coil embolization and 33 periprocedural complications occurred within 1 week. These complications were observed in 8.6% of ruptured aneurysm embolization procedures (55/637) and in 3.5% of unruptured aneurysm embolization procedures (39/1127). There were 17 (0.96%) cerebral thromboembolisms, 34 (1.93%) intraprocedural aneurysm ruptures, 8 (0.45%) coil migrations, 13 (0.74%) postprocedural aneurysmal ruptures, and 22 (1.24%) neurologic deficits or transient neurologic deficits related to embolization. 63 complications had no neurologic consequences, 3 were associated with transient neurologic morbidity, 15 resulted in persistent neurologic morbidity on discharge, and 12 resulted in death. The procedure-related neurologic morbidity and mortality rates for all 1764 procedures were 0.85% in ruptured aneurysms and 0.68% in unruptured aneurysms.
Conclusions The periprocedural complication rate was higher in ruptured aneurysms than in unruptured aneurysms. The main causes of morbidity and mortality were thromboembolisms, intraprocedural aneurysm perforations, and postprocedural aneurysmal ruptures. While some periprocedural complications are inevitable, we can minimize the occurrence of such complications by advancing our skill and experience, thereby improving patient prognosis.
- Intracranial aneurysms
- endovascular treatment
- periprocedural complication
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Introduction
Since the approval of coils by the Food and Drug Administration in 1995, endovascular embolization of intracranial aneurysms has become an alternative treatment to aneurysm clipping and has shown a better clinical outcome.1–5 As endovascular therapy becomes more commonly used, the prevalence of intraprocedural complications is expected to rise accordingly.6–9 The purpose of this study was to review our experience with periprocedural complications associated with endovascular coil embolization of intracranial aneurysms and to summarize the current literature describing the types and frequency of complications observed.
Methods
Between January 2007 and December 2013, 1739 patients underwent 1764 detachable coil embolizations to treat intracranial aneurysms; 637 of these aneurysms were ruptured and 1127 were unruptured. Five endovascular surgeons performed the procedures. A review of medical records and endovascular procedure reports, location of the aneurysm, etiology of rupture, management, and clinical outcome was conducted.
All patients in this study were taken to the angiography suite for aneurysm embolization. Procedures were performed either with the patient under general endotracheal anesthesia (n=1601, 90.8%) or local anesthesia (n=163, 9.2%). A 5.0 or 6.0 Fr Envoy guiding catheter (Cordis, Miami Lakes, Florida, USA) was placed in the internal carotid artery or distal vertebral artery. Under fluoroscopic guidance, a microcatheter (Echelon-14; Covidien, Irvine, California, USA) was navigated to the orifice of the aneurysm. Coil placement was performed with detachable coils (Stryker Neurovascular, Freemont, California, USA; Gugliemi detachable coils; NXT fiber coils, Covidien; Microplex, Microvention, Tustin, California, USA). Generally, small aneurysms were treated preferentially with bare platinum coils while a mixture of bare platinum and bioactive coils was used in larger aneurysms. Coils were inserted until the aneurysm was excluded from the circulation or until no more coils could be delivered.10
Patients in whom stent-assisted coiling was anticipated were pretreated with daily doses of 100 mg aspirin and 75 mg clopidogrel for 3 days before the procedure. These patients received systemic heparinization after placement of the sheath. Activated clotting time was maintained at 2–3 times baseline throughout the procedure. The use of stent-assisted coiling was generally indicated for wide-necked aneurysms (>4 mm) or those with an unfavorable dome-to-neck ratio (<1.5) and in cases of failed balloon-assisted coiling. All stents were deployed following the standard procedure recommended by the manufacturer. The coil microcatheter was positioned into the aneurysm through the stent or before stent placement. Finally, the aneurysm was sequentially coiled using detachable coils.
Follow-up angiograms were evaluated using MR angiography 3 months after discharge or using digital subtraction angiography at least 6 months after discharge. At least one follow-up angiogram was performed for most patients, usually 6 months after the procedure.
Results
Between January 2007 and December 2013, 1764 detachable coil embolization procedures were performed on 637 ruptured aneurysms and 1127 unruptured aneurysms in 1739 consecutive patients at Huashan Hospital (table 1). Of these, 1393 (79%) intracranial aneurysms were located in the anterior circulation and 371 (21%) in the posterior circulation (table 2). Of the 1764 patients who received regular intravascular interventional treatment therapies, 1147 cases were treated with simple coil embolization, 363 with stent-assisted coiling, 186 with balloon-assisted coiling, 6 with flow diversion, 6 with onyx and coil, 29 with single stent implantation, and 27 with multiple stent implantation (table 3).
Patient and aneurysm characteristics
Locations of aneurysms
Embolization type in 1764 intracranial aneurysms
Ninety-four (5.3%) complications occurred in these procedures. Among these, 61 occurred during coil embolization and 33 within 1 week after embolization. Complication rates for embolizations of ruptured and unruptured aneurysms were 8.6% (55/637) and 3.5% (39/1127), respectively. Complications included 17 cerebral thromboembolisms (0.96%), 34 intraprocedural ruptures (1.93%), 8 coil migrations (0.45%), 13 postprocedural aneurysmal rupture (0.74%), and 22 neurologic deficits or transient neurologic deficits related to embolization (1.24%) (table 4). Fifty complications had no neurologic consequences, 17 were associated with transient neurologic morbidity, 15 resulted in persistent neurologic morbidity on discharge, and 12 resulted in death. Procedure-related permanent neurologic morbidity and mortality rates for all 1764 procedures were 0.85% and 0.68%, respectively.
Procedure-related complications and prognosis
The 637 cases of ruptured intracranial aneurysm can be graded according to the World Federation of Neurological Societies(WFNS) scale into 448 grade I, 102 grade II, 15 grade III, 65 grade IV, and 7 grade V cases. The outcome of the 637 cases with ruptured intracranial aneurysms included 619 cases who improved postoperatively (97.17%), eight deaths (1.26%), four had paraplegia (0.63%), two had hemianopsia (0.31%), three had facial paralysis (0.47%), and one had aphasia (0.16%).
Intraprocedural aneurysm ruptures (IPARs)
Intraprocedural aneurysm ruptures (IPARs) occurred in 34 patients (1.93%) during the procedures. Of these 34 patients, 26 were women, the mean±SD age was 49.8±11.7 years (range 29–76 years), and the follow-up time was 6 months; 29 were located in the anterior circulation and 5 in the posterior circulation. In our study the rate of IPARs in ruptured aneurysms was higher than in unruptured aneurysms (3.45% vs 1.06%, p<0.05; table 5). Three patients with an initial WFNS grade I died due to IPAR. Twenty-nine intraprocedural ruptures had no clinical consequence, one resulted in hemiplegia, one resulted in hemianopia and three resulted in death. The morbidity rate from IPAR of an already ruptured aneurysm was 4.34% and the mortality rate was 13.04%. Overall morbidity and mortality rates at discharge from IPAR were 5.89% and 8.82%, respectively.
IPAR and aneurysm rupture
Periprocedural thromboembolism
Thromboembolic complications occurred in 17 (0.96%) of 1764 procedures. Of these, 10 resulted in no neurological consequence, one resulted in transient neurologic deficits (motor aphasia), three resulted in persistent neurologic abnormalities on discharge, and three resulted in death. The morbidity rate on discharge due to thromboembolic complications was 17.65% and the mortality rate was also 17.65%. Twelve thromboembolic complications occurred during the procedure and five were documented on post-embolization follow-up radiographic studies.
Early hemorrhagic complications
Thirteen patients (0.74%) had fatal early hemorrhagic complications during the 30 days after initial embolization. Patients with ruptured aneurysms (8/637, 1.25%) were more prone to early hemorrhagic complications than those with unruptured aneurysms (5/1127, 0.44%; table 6). Of these 13 aneurysms with early hemorrhagic complications, 11 were located in the anterior circulation and two in the posterior circulation. Five patients died of early hemorrhagic complications and two patients suffered neurologic abnormalities. The morbidity rate on discharge due to early hemorrhagic complications was 15.38% and the mortality rate was 38.46% on discharge.
Procedural complications in 1764 intracranial aneurysms
Coil migration
Coil migration during treatment occurred in eight (0.45%) of 1764 aneurysms. All coil migrations occurred in the anterior circulation. Seven migrated coils were retrieved successfully by stent in our studies with no clinical consequences. One patient experienced permanent hemiplegia after unsuccessful coil retrieval.
Complications related to embolization
In addition to the clinical complications mentioned above, 22 cases of neurologic deficits or transient neurologic deficits were related to embolization (1.24%) without obvious reasons. Three patients were discharged with hemiplegia, two with hemianopsia, and two with facial paralysis. Fifteen patients had transient neurologic morbidity. We suspect this was due to the compressive effect of a coiled aneurysm, postoperative vasospasm, and postoperative hemodynamic changes. One patient died of multiple organ dysfunction although embolization was very successful.
Discussion
Many studies have reported procedural complication rates related to endovascular aneurysm coil placement. Henkes et al1 reported a procedural complication rate of 17.7% in 1579 patients with 1811 aneurysms, an early procedural morbidity rate of 5.3%, a procedural mortality rate of 1.5%, and a management mortality rate of 4.4%. Brilstra et al6 reviewed 48 studies (1383 patients) on coil embolization, noting a 12% procedure-related complication rate. Procedure-related morbidity and mortality rates were 3.7% and 1.1%, respectively. Our overall complication rate for all aneurysms was 5.33% and the overall procedural morbidity and mortality rates were 0.85% and 0.68%, respectively. Complication rates for embolizations of ruptured and unruptured aneurysms were 8.6% (55/637) and 3.5% (39/1127), respectively. In ruptured aneurysms, the procedure-related neurologic morbidity rate was 1.57% and the mortality rate was 1.26%. Two main causes of procedural morbidity and mortality in this group were intraprocedural rupture and early hemorrhage. In unruptured aneurysms, procedure-related neurologic morbidity and mortality rates were 0.44% and 0.18%, respectively. Thromboembolism was the main cause of procedural morbidity and mortality in this group.
Intraprocedural aneurysm rupture (IPAR)
IPAR during endovascular embolization of intracranial aneurysms was an adverse event. The rates of IPAR reported by different single-center series varied considerably, ranging from 1% to 8.7%.2 ,7–9 In our retrospective analysis, 34 of the 1764 patients without preoperative neurologic deficits suffered from rupture of their cerebral aneurysms during intervention procedures. The incidence of IPAR was 1.93%, with a mortality rate of 14.71% in these 34 aneurysms with IPAR compared with other studies. In a meta-analysis of 2008 patients across 14 series, the risk of IPAR was 2.8%.6 Levy and colleagues reported IPAR in 2% of their 274 patients, with a mortality of 33%.7 In 2013, Zhang presented 176 consecutively treated aneurysms from April 2005 to March 2009, 161 of which were treated with coils, and IPAR occurred in 12 patients. One patient died, yielding a mortality rate of 8.3%.8 These findings showed that, although intraoperative rupture is rare, it has been encountered in each center.
IPARs may be related to the microcatheter, coils, or the guidewire itself. Oversizing the coils, overpacking the aneurysm, or using stiff three-dimensional coils has also been associated with IPARs. Even the deployment of a single coil inside an aneurysm may increase the intraluminal pressure and result in an IPAR.8 In our series, approximately half of the IPARs were caused by aneurysm perforation with the microcatheter and microwire, and IPARs were more frequent in acutely ruptured aneurysms. In a meta-analysis, Cloft and coworkers determined that the risk of IPAR during coil embolization in patients with previously unruptured aneurysms was significantly lower than in patients with previously ruptured aneurysms (0.7% vs 4.1%).3 IPAR of a previously unruptured aneurysm necessitates the de novo creation of a rent in the aneurysm wall while IPAR in a previously ruptured aneurysm does not have this same requirement and could occur because of the dislodgement of a clot that occludes the site of original rupture or because of additional tearing of an already torn and fragile aneurysm wall. Aneurysms with a history of rupture may also have a wall that is more fragile than those without a history of rupture. These differences most likely explain the higher rate of perforation in ruptured aneurysms than in unruptured aneurysms,8 which suggests that we should be more careful when performing embolization on ruptured aneurysms.
Previous series have reported a 0–40% risk of death, 0–33.3% risk of disability, and a 14.3–66.6% combined risk of disability and death in patients.4 ,8 ,11–13 In a meta-analysis of 72 patients with IPAR across 17 series, the rates of disability and mortality were 5.5% and 31.5%, respectively.14 In our study, two of the 34 patients with IPR suffered disability (5.89%) and a relatively low rate of mortality (8.8%). When an IPAR occurred, we quickly reversed heparin and lowered the blood pressure. We never pulled back the protruded coil or microcatheter, but rapidly coiled from that point on and the perforated portion was closed in a few minutes. With this method we observed no increase in the incidence of subarachnoid hemorrhage. After embolization we performed antivascular spasm, dehydration treatment and ventricular drainage, if necessary. It is worth noting that three of the deaths in our study were in patients with modified Fisher grades III or IV. We therefore speculate that the prognosis of these patients was closely related to the bleeding volume.
Periprocedural thromboembolism
Endovascular coil embolization of intracranial aneurysms is associated with a risk of thromboembolic events and ischemic complications. Thromboembolic complications within 24 h of coil embolization occurred in 3–28% of the procedures.14–17 Diffusion-weighted imaging indicates that microemboli may also occur and be asymptomatic.18 In our study, thromboembolic complications occurred in 17 (0.96%) of the 1764 procedures and five of the 17 thromboembolic complications occurred within 24 h of embolization. In our study, the two main reasons related to thromboembolic complications were: (1) tearing of the original thrombus that was attached to the vessel wall by the microcatheter or microwire resulting in a distal vascular thrombosis; and (2) formation of local thrombosis after earlier operations and subsequent operations leading to distal vascular thromboses because of emboli shedding. Acute intraprocedural thrombus formation complicating endovascular cerebral aneurysm treatment is often treated with intra-arterial or intravenous administration of thrombolytic agents or glycoprotein IIb/IIIa (GpIIb/IIIa) inhibitors. Cronqvist et al reported the results of superselective intra-arterial fibrinolytic therapy in 19 patients for treating thromboembolic complications during endovascular aneurysm treatment. Complete recanalization was achieved in 10 patients and partial recanalization in nine.19 In recent years abciximab, a chimeric monoclonal antibody fragment against the platelet glycoprotein IIb/IIIa receptor complex, has been used to manage acute thromboembolisms during endovascular coil placement in intracranial aneurysms. Brinjikji et al20 reported that patients receiving only fibrinolytics had significantly higher rates of mortality than patients receiving glycoprotein IIb/IIIa inhibitors alone (26.0% (18/69) vs 14.5% (35/241); p=0.02). In a meta-analysis, Brinjikji et al21 reported that patients receiving glycoprotein IIb/IIIa inhibitors had significantly lower perioperative morbidity than those treated with fibrinolytics and were significantly less likely to have long-term morbidity. There was a trend towards higher recanalization rates among patients treated with glycoprotein IIb/IIIa inhibitors compared with those treated with fibrinolytics. Cho et al22 reported only two cases of non-consequential intracerebral hemorrhage following intra-arterial infusion of abciximab in 39 patients. They considered that intra-arterial tirofiban infusion seemed to be efficacious and safe for thrombolysis during coil embolization in patients with ruptured intracranial aneurysms. In our study, the morbidity rate on discharge due to thromboembolic complications was 0.17% and the mortality rate was 0.17%. Mechanical embolectomy was performed in one patient without neurologic consequences on discharge. The other 16 patients were managed with local or systemic administration of fibrinolytics or antiplatelet agents. Although there was difficulty in mechanical embolectomy, it often resulted in fewer postoperative complications.
Early hemorrhagic complications
The incidence of periprocedural hemorrhagic complications within 30 days was reportedly not high with endovascular treatment but was associated with high mortality and morbidity rates. The greatest risk of hemorrhagic complications associated with endovascular coil treatment of aneurysms occurs during the initial 48 h.23 In our study of 1764 aneurysms under endovascular treatment, 13 patients suffered early hemorrhagic complications (0.74%), which occurred more commonly with ruptured than unruptured aneurysms (1.25% vs 0.44%).
The risk factors for such early hemorrhagic complications are not well known. Cho et al24 reported that the incidence of early rebleeding after coiling of a ruptured saccular aneurysm was 1.1% (13/1167) and the mortality was 31% (4/13). They thought that the use of intra-arterial abciximab infusion or thrombolytic interventions during the procedure, maintenance of anticoagulation after the procedure, incomplete treatment of the aneurysms, and the presence of intracerebral hemorrhage seemed to be related to hyperacute rebleeding after coiling. Increased aneurysmal size and coil compaction could induce subacute and delayed early rebleeding. Dmytriw et al25 reported a series of 137 cases with ruptured aneurysms who underwent endovascular treatment in which two cases had early hemorrhagic complications (1.4%). Of these, one patient received recombinant tissue plasminogen activator and both received acetylsalicylic acid. In general, technical issues such as microwire perforation of intracranial aneurysm or perforator avulsion can be the main reason for this unfortunate outcome in our study. Also, the hemodynamic changes incited by the presence of blood in the arachnoid system and the use of antiplatelet therapy along with intraprocedural heparin administration are additional risk factors.
Coil migration
Migration of detachable coils is a potentially serious intraprocedural complication. Coil masses are highly thrombogenic, so migration out of the aneurysm sac into the parent artery may be devastating. Few studies have reported cases of coil migration. Henkes et al1 reported the results in 1811 aneurysms under endovascular treatment; 46 patients suffered from coil migration (2.5%) with only a small difference between those with ruptured and those with unruptured aneurysms (2.4% vs 2.7%). However, only one patient with coil migration developed arterial thrombosis (0.1%). In another early study, Casasco et al reported parent vessel occlusion from coil migration in four of 71 cases (5.6%), which resulted in death in two patients (2.8%) and moderate neurologic deficits at long-term follow-up in the other two patients (2.8%).26 In our study, coil migration was observed in 8/1764 procedures (0.43%). No deaths occurred, but one disability caused by coil migration was observed.
How can we manage intraprocedural coil migration? When should we perform coil removal? Most instances of minor coil migration, which can be classified as protrusion or prolapse, may be managed conservatively with anticoagulation or antiplatelet therapy.27 Ding and Liu28 reported that a small degree of coil protrusion without angiographic evidence of thromboembolism or large vessel occlusion is typically treated with 24–48 h of anticoagulation with a heparin infusion followed by antiplatelet therapy for 6 months. In their view, significant degrees of coil displacement including stretching, fracture, and migration necessitate prompt intervention to avoid significant neurologic morbidity and mortality. Of 37 cases of coil migration reported by Koseoglu et al,29 a goose neck snare was successfully used for retrieval in eight cases (21.6%). Otherwise, surgery for coil removal should be performed in cases of progressive coil migration and/or cerebral ischemic attacks after the initiation of antiplatelet medication.30 In our hospital, the incidence of coil migration is lower than previously reported and all but one migrated coils were removed successfully using a stent retriever.
According to the statistical findings in our single institution, the annual incidence of complications showed a declining tendency, although with occasional rebounding in some years, as shown in figure 1. The declining rates of complications of endovascular intervention can be explained by improvements in skills and exchange of practical experience. We comprehensively arranged all crucial steps before, during, and after the surgery to decrease complication rates. First, the selection of a rational treatment strategy is of paramount importance. Determination of aneurysm treatment, as judged by both experienced cerebrovascular surgeons and endovascular specialists, should be a multidisciplinary decision based on the characteristics of the patient and the aneurysm. Second, thorough discussion before the operation is routinely practiced to yield a detailed treatment protocol, including coping schemes and measures against various complications. Third, modification of the microcatheter and the selection of coils should be done during treatment according to the shape, size, and location of the intracranial aneurysm under treatment. Finally, regular discussion on intractable cases to exchange experience with colleagues contributes to a decrease in the complication rate.
Annual incidence of complications between 2007 and 2013.
Limitations of the study
Our study is limited by its retrospective design and the absence of long-term follow-up data. The results reflect the experience of a single neurovascular center and may not be readily generalizable to other centers. Regarding follow-up, more results will be reported in the future.
Conclusion
Our review indicates that endovascular coil embolization of an intracranial aneurysm is a safe technique with low morbidity and mortality. Technological advances, skill improvements, and accumulation of experience in endovascular coil embolization have decreased the threshold for the endovascular treatment of aneurysms. Consequently, more patients with difficult aneurysms such as wide-necked aneurysms, small aneurysms or giant aneurysms can undergo endovascular treatment. Although periprocedural complications are occasionally inevitable, we believe the likelihood can be minimized and the patient prognosis improved through skill improvements and exchange of practical experience among neuroradiologists.
References
Footnotes
YZ and YL contributed equally and should be considered joint first authors.
Contributors Conception and design: BL and YZ. Analysis and interpretation of data: BL, YZ, YL, FX and YT. Drafting the article: YZ. All authors critically revised the article, reviewed the final version of the manuscript, and approved it for submission.
Competing interests None.
Provenance and peer review Not commissioned; externally peer reviewed.