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Original research
Balloon-assisted coil embolization of intracranial aneurysms is not associated with increased periprocedural complications
  1. Alejandro Santillan1,
  2. Y Pierre Gobin1,
  3. Jan C Mazura1,
  4. Valerie Meausoone1,
  5. Lewis Z Leng1,
  6. Edward Greenberg1,
  7. Howard A Riina2,
  8. Athos Patsalides1
  1. 1Division of Interventional Neuroradiology, Department of Neurological Surgery, New York Presbyterian Hospital, Weill Cornell Medical Center, New York, New York, USA
  2. 2Department of Neurosurgery, New York University Langone Medical Center, New York, New York, USA
  1. Correspondence to Dr Alejandro Santillan, 525 E. 68th St, Division of Interventional Neuroradiology, Department of Neurosurgery, New York Presbyterian Hospital/Weill Cornell Medical Center, New York, NY 10065, USA; als2052{at}med.cornell.edu

Abstract

Background The balloon-assisted coil embolization (BACE) technique represents an effective tool for the treatment of complex wide-necked intracranial aneurysms; however, its safety is a matter of debate. This study presents the authors' institutional experience regarding the safety of the BACE technique.

Methods 428 consecutive patients with 491 intracranial aneurysms (274 acutely ruptured and 217 unruptured) treated with conventional coil embolization (CCE) or with BACE were retrospectively reviewed. All procedure-related adverse events were reported, regardless of clinical outcome. Thromboembolic events, intraprocedural aneurysm ruptures, device-related complications, morbidity and mortality were compared between the CCE and BACE groups.

Results The total rate of procedural and periprocedural adverse events was 9.6% (47/491 embolizations). Thromboembolic events, intraprocedural aneurysmal rupture and device-related complications occurred in 2.4%, 3.9% and 3.3% of procedures, respectively. The risk of thromboembolic events and device-related problems was similar between the CCE and BACE groups. A trend towards a higher risk of intraprocedural aneurysm rupture was observed in the BACE group (not statistically significant). The total cumulative morbidity and mortality for both groups was 2.6% (11/428 patients) and there was no statistically significant difference in the morbidity, mortality and cumulative morbidity and mortality rates between the two groups.

Conclusion In this series of patients with acutely ruptured and unruptured aneurysms, the BACE technique allowed treatment of aneurysms with unfavorable anatomic characteristics without increasing the incidence of procedural complications.

  • Balloon-assisted technique
  • coil embolization
  • intracranial aneurysm
  • morbidity
  • mortality
  • aneurysm
  • angiography
  • angioplasty
  • arteriovenous malformation
  • coil
  • drug
  • subarachnoid
  • stroke
  • blood pressure

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Introduction

Coil endovascular treatment is considered a first-line treatment for the management of most intracranial aneurysms. The balloon-assisted coil embolization technique (BACE), first described by Moret et al,1 has gained favor among many interventional neuroradiologists and endovascular neurosurgeons as a safe and effective tool for the treatment of complex and wide-neck intracranial aneurysms and has been studied in several series with mixed results. Some studies showed no increase in adverse events2–10 while others have demonstrated an increase in adverse outcomes11–15 compared with conventional coil embolization (CCE). For example, a study by Sluzewski et al published in 200612 raised serious concern about the safety of the balloon remodeling technique when they demonstrated significantly higher procedure-related complications compared with the CCE group. More recent large multicenter prospective studies from France16 ,17 contradict the assertion that balloon remodeling carries a greater risk than coil embolization alone. At our institution we frequently use the balloon remodeling technique when performing embolizations for both ruptured and unruptured aneurysms and in this paper we provide our institutional experience regarding the safety of this technique.

Materials and methods

Patient demographics

We retrospectively reviewed the medical records and angiograms of 428 consecutive patients with a total of 491 intracranial aneurysms, both ruptured and unruptured, that were treated with CCE or with the balloon remodeling technique from March 2002 to February 2010. Patients who were treated with stent-assisted coiling were excluded from the analysis, even when BACE was initially used. Patients in whom stent-assisted coiling was the primary intended treatment were excluded from this analysis, even when BACE was used prior to stent placement. Patients who required stent placement because of a technical problem such as coil migration (‘bailout therapy’) were included in the analysis. CCE was performed in 204 patients and balloon remodeling was performed in 224 patients. Patient age and sex, the presence of a ruptured intracranial aneurysm and the number of treated aneurysms per patient were recorded.

Endovascular procedure

BACE was defined as the placement of a compliant balloon across the aneurysm neck during coil deployment, regardless of whether or not it was inflated. All procedures were performed at New York Presbyterian Hospital/Weill Cornell Medical College by the senior authors (YPG, HR, and AP) using standard interventional neuroradiology techniques. All patients were anticoagulated with heparin to achieve activated clotting time 2–3 times the baseline value. Anticoagulation was initiated following femoral arterial puncture for patients with unruptured aneurysms and following initial coil deposition for patients with acutely ruptured aneurysms. A subset of patients was treated with a single periprocedural dose of aspirin at the discretion of the operator. The anticoagulation protocol was similar in the CCE and BACE groups. For patients treated with emergency stenting, the following antiplatelet regimen is used: abciximab 10 mg intravenously as a bolus and aspirin 300 mg per rectum prior to stent placement, followed by clopidogrel 600 mg via nasogastric tube immediately after the procedure. The patients remain on daily aspirin 325 mg and clopidogrel 75 mg. All patients with subarachnoid hemorrhage (SAH) were treated within 24 h from the time of admission to our institution. The majority of patients were treated with bare platinum detachable coils, with the exception of 56 aneurysms that were treated with polymer-coated platinum detachable coils (Matrix; Boston Scientific/Target, Fremont, California, USA). The decision to use CCE or BACE was made by the attending neurointerventionalist on a case-by-case basis. All BACE procedures were performed using HyperForm or HyperGlide balloons (eV3, Irvine, California, USA). Embolization was deemed sufficient when dense coil packing was obtained and no additional coil could be safely inserted.

Data collection

Aneurysm characteristics including location, size, neck size and dome-to-neck ratio were recorded. All treatment-related adverse events were reported, even if they resulted in no clinical sequelae. The adverse events were separated into three categories: thromboembolic events, intraprocedural aneurysm rupture and device-related problems. A thromboembolic event was defined as parent vessel occlusion secondary to thrombus formation, a new filling defect in the parent vessel near the aneurysm neck or a new filling defect in more distal branches within the vascular territory of the treated aneurysm. Post-procedure thromboembolic events were identified using digital subtraction angiography and/or MRI, performed as clinically indicated in cases of neurological deterioration. In asymptomatic patients, post-procedure MRI scans were not routinely performed. Intraprocedural aneurysm rupture was defined as violation of the aneurysmal sac by coil loops or the microcatheter, with or without associated contrast extravasation. Device-related problems included any significant problems related to the use of microcatheters, microguidewires, coils and balloons that could not be managed in the usual way, such as inability to navigate the microcatheter into the aneurysm neck secondary to the presence of the balloon, insufficient protection afforded by the balloon across the neck of the aneurysm to allow for safe coil deployment, and coil migration after detachment. Clinical outcomes of all adverse events were reviewed and classified as none, transient neurologic deficit, permanent neurologic deficit and death. A transient neurological deficit was defined as the presence of a neurological deficit that resolved within 24 h. Procedure-related morbidity was defined as the presence of a new permanent neurological deficit or the need to perform a repeat procedure (endovascular or surgical) attributed to any procedure-related complication.

Data analysis

Two interventional neuroradiologists reviewed all clinical and procedural data. The aneurysm location was classified into the following groups: internal carotid artery, anterior cerebral artery (including the anterior communicating artery), middle cerebral artery and vertebrobasilar system (including the posterior cerebral artery). The dome and neck of the aneurysm were measured by 3D rotational angiography and the size of the aneurysm sac was defined as the greatest diameter. All aneurysms were classified into two groups according to dome size: ≥7 mm and <7 mm. The aneurysms were also further subclassified according to their neck size (≤4 mm and >4 mm) and according to their dome-to-neck ratios (≤1.5 or >1.5).18

The following parameters were compared in both the CCE and the BACE groups: (1) occurrence of procedure-related complications (thromboembolic events, intraprocedural aneurysm rupture and device-related complications); (2) morbidity, mortality and cumulative morbidity and mortality associated with procedure-related complications.

Statistical analysis

Descriptive statistics (including mean, SD, median, range, frequency and per cent) for aneurysm characteristics were calculated for the BACE and CCE aneurysm groups. The two-sample t test or Wilcoxon rank sum test was used, as appropriate, to compare continuous aneurysm characteristics between the BACE and CCE groups. The t test was used to compare mean age between the two groups (table 1) and the χ2 test was used to compare categorical variables between the two procedure groups (tables 1 and 2). Univariate logistic regression was performed to assess the effect of CCE on the risk of thromboembolic events, intraprocedural aneurysm ruptures and device-related problems relative to the BACE aneurysm group. ORs were computed along with 95% CIs for the ORs to assess the precision of the obtained estimates. The Fisher exact test was also used to compare morbidity, mortality and cumulative morbidity and mortality between the BACE and CCE procedure groups. All p values are two-sided with statistical significance evaluated at the 0.05 α levels. All analyses were performed in SPSS V.19.0 (SPSS Inc).

Table 1

Patient and aneurysm characteristics

Table 2

Characteristics of 491 treated aneurysms

Results

Patients

A total of 224 patients (178 women, 46 men, mean±SD 51.1±12.5 years, range 11–92 years) with 236 aneurysms were treated with the balloon remodeling technique and 204 patients (138 women, 66 men, mean±SD 57.3±13.3 years, range 24–87 years) with 255 aneurysms were treated with coils alone (table 1). Stent placement was used as ‘bailout therapy’ in three patients in the BACE group and in two patients in the CCE group who had significant coil loop protrusion or coil migration. There were no additional adverse events related to stent placement. Patients in the CCE group were older than those in the BACE group and aneurysms treated with CCE were more likely to be acutely ruptured than those treated with BACE (67.8% vs 42.8%, p<0.0001, table 1).

Aneurysm characteristics

Of the 236 aneurysms treated with BACE, 156 (66.1%) involved the internal carotid artery, 36 (15.3%) involved the anterior cerebral or anterior communicating artery, 18 (7.6%) involved the middle cerebral artery and 26 (11%) involved the vertebrobasilar system. Of the 255 aneurysms treated with CCE, 104 (40.8%) involved the internal carotid artery, 78 (30.6%) involved the anterior cerebral artery or anterior communicating artery, 19 (7.5%) involved the middle cerebral artery and 53 (20.8%) involved the vertebrobasilar system (table 2). Three hundred and three aneurysms (61.8%) measured <7 mm in maximal sac diameter and 188 (38.2%) measured ≥7 mm in maximal sac diameter. The aneurysm neck was ≤4 mm in 398 aneurysms (81.1%) and >4 mm in 93 aneurysms (18.9%). The dome-to-neck ratio was ≤1.5 in 169 (34.4%) and >1.5 in 322 (65.6%, table 2). BACE was used in 54/93 (58.1%) aneurysms with neck measuring >4 mm and in 182/398 (45.7%) aneurysms with neck measuring ≤4 mm (p=0.03). BACE was used in 93/187 (49.7%) aneurysms ≥7 mm and in 143/303 (47.2%) aneurysms measuring <7 mm (p=0.59). BACE was used in 87/169 (51.5%) aneurysms with a dome-to-neck ratio of ≤1.5 and in 154/322 (47.8%) aneurysms with a dome-to-neck ratio >1.5 (p=0.88, table 2). There were few statistically significant differences in the aneurysm characteristics between the CCE and BACE groups.

Complications

The total rate of procedural and periprocedural adverse events was 9.6% (47/491 embolizations). Thromboembolic events, intraprocedural aneurysm rupture and device-related problems were encountered in 12 (2.4%), 19 (3.9%) and 16 (3.3%) procedures, respectively. The risk of thromboembolic events was the same in the CCE group compared with the BACE group (OR 0.92; 95% CI 0.29 to 2.91; p=0.89). A trend towards a higher risk of intraprocedural aneurysm rupture was observed in the BACE group, but the difference was not statistically significant (OR 0.53; 95% CI 0.20 to 1.36; p=0.19). There was no statistically significant difference in the rate of device-related problems in the CCE group compared with the BACE group (OR 0.92; 95% CI 0.34 to 2.50; p=0.88) (figure 1).

Figure 1

Bar chart showing periprocedural complications related to treatment in conventional coil embolization (CCE) and balloon-assisted coil embolization (BACE) groups. N, number of embolization procedures.

Thromboembolic events were encountered in 6/236 (2.5%) BACE procedures, four occurred during the procedure and two that were delayed occurred within 6 h following aneurysm embolization. All four cases with thromboembolic events identified during aneurysm embolization were treated with intra-arterial infusion of abciximab and resulted in successful thrombolysis. Of the patients treated with abciximab, three remained asymptomatic but the fourth patient, who was admitted with SAH (Hunt and Hess grade IV), had an enlarging hematoma in the Sylvian fissure and transient neurological deficit that resolved after subsequent surgical evacuation. One patient with a delayed thromboembolic event had transient neurological deficits that resolved following repeat endovascular procedure and intra-arterial thrombolysis with abciximab. Mechanical clot retrieval was attempted in the second patient with a delayed thromboembolic event but this was unsuccessful; the patient developed a cerebral infarct and permanent neurological deficit. Thromboembolic events were encountered in 6/255 (2.4%) CCE procedures, two of which occurred within 8 h of the aneurysm embolization. All four cases with thromboembolic events identified during the aneurysm embolization were treated with an intra-arterial infusion of abciximab resulting in thrombolysis and no neurological sequelae. One patient with a delayed thromboembolic event developed transient neurological deficits that resolved after repeat endovascular procedure and intra-arterial thrombolysis with abciximab. The second patient with a delayed thromboembolic event developed infarct and permanent neurological deficit.

Intraprocedural aneurysm ruptures occurred in 12/236 (5.1%) BACE procedures and in 7/255 (2.7%) CCE procedures (p=0.19). Bleeding was controlled by inflating the balloon across the aneurysm neck in all patients in the BACE group. Intraprocedural aneurysm rupture resulted in transient neurologic deficits in two patients and death in one patient in the BACE group. The remaining nine patients in the BACE group did not have new or worse neurological findings. Of the seven patients in the CCE group with intraprocedural aneurysm rupture, four patients had transient neurologic deficits, one died and two patients did not have new or worse neurological findings. Three patients, all in the BACE group, had previously unruptured aneurysms and new SAH as a result of the procedure. They did not have neurological deficits other than mild headaches and were observed for 48–72 h prior to discharge; they were also followed closely as outpatients.

Device-related complications were encountered in 8/236 (3.4%) BACE procedures and in 8/255 (3.1%) CCE procedures (p=0.88). Of the eight patients with device-related complications in the BACE group, seven had coil migration. In four patients the coils were retrieved without sequelae, in one patient the coil migrated in a distal branch without compromising flow and retrieval was not attempted (the patient remained asymptomatic) and in the remaining two patients with coil migration the coils could not be retrieved and resulted in large infarcts with permanent deficits. One of these patients had surgery to retrieve the coil and subsequently died. One patient had a device-related complication secondary to increased mass effect of an anterior communicating artery aneurysm that resulted in compression and occlusion of the A2 segment of the left anterior cerebral artery and caused a left frontal stroke with resultant permanent neurological deficit. No device-related complication in the CCE group was symptomatic. There were five procedures with coil migrations all of which were successfully retrieved. In the three remaining patients, one or few coil loops herniated into the parent artery but resulted in no sequelae.

Among procedures for ruptured aneurysms, thromboembolic events, intraprocedural aneurysm rupture and device-related problems occurred in 8/274 (2.9%), 16/274 (5.8%) and 7/274 (2.5%) embolizations, respectively. In the unruptured aneurysm subgroup, thromboembolic events, intraprocedural aneurysm rupture and device-related problems occurred in 4/217 (1.8%), 3/217 (1.1%) and 9/217 (4.1%) embolizations, respectively. The sample size is unfortunately insufficient for statistical subgroup analysis.

The morbidity and mortality rates resulting from all procedure-related complications in the BACE group were 5/224 and 2/224, respectively, with a cumulative morbidity and mortality rate of 7/224. The morbidity and mortality rates resulting from all procedure-related complications in the CCE group were 3/204 and 1/204, respectively, with a cumulative morbidity and mortality rate of 4/204 (2%). The overall cumulative morbidity and mortality for both groups was 11/428 (2.6%). There was no statistically significant difference in mortality and morbidity between the two groups (table 3).

Table 3

Global morbidity, global mortality and cumulative morbidity and mortality rates

Discussion

This was a retrospective study based on our institutional experience from March 2002 through February 2010 evaluating the safety of BACE in a series of patients with acutely ruptured and unruptured intracranial aneurysms, and is among the very few large studies that provide a comparison regarding the rate of periprocedural complications in both BACE and CCE groups. Since the primary objective of this study was to compare complications between the CCE and BACE techniques, patients treated with stent-assisted coiling were excluded in order to avoid including complications related to stent placement. In addition, patients treated with stents require dual antiplatelet therapy which reduces the periprocedural embolic complications. In our practice, patients treated with CCE or BACE are not routinely treated with antiplatelet therapy. A number of safety parameters were explored for the CCE and BACE groups to provide preliminary estimates on the safety of these two techniques. Hence, we present important data supporting the safety of BACE and corroborating the findings of the ATENA and CLARITY studies.16 ,17 In our analysis we reported all procedure-related complications regardless of clinical outcome and, within the limitations of a retrospective study, we showed that the procedure-related adverse events, morbidity, mortality and cumulative morbidity and mortality were not different between the BACE and CCE groups. The two patient groups had similar age distributions, with a slightly higher percentage of women in the BACE group. The aneurysm dome size and the dome-to-neck ratio were similar in the two groups. The latter reflects the fact that we do not apply strict criteria (ie, dome-to-neck ratio ≤1.5) for using a balloon during aneurysm embolization. For instance, we often place a balloon across the aneurysm neck when treating very small aneurysms (≤3 mm), especially when acutely ruptured, because they pose an increased risk of intraprocedural aneurysm rupture.19–21 In these cases the balloon remains deflated and is inflated only if there is an intraprocedural aneurysm rupture. These patients were included in the analysis because complications may arise from balloon inflation and also from navigation of the balloon, as well as from positioning the balloon and the associated microwire in the intracranial circulation. There were, however, important differences between the two groups. As expected, the patients in the BACE group were more likely to have wide-necked aneurysms (neck measuring >4 mm), which is a classic indication for balloon remodeling.22 There were less acutely ruptured aneurysms in the BACE group, and the BACE technique was used less frequently in the anterior cerebral/anterior communicating artery and the vertebrobasilar artery aneurysms. The navigation of a balloon in the anterior cerebral artery complex has been challenging in the past, but improvements in balloon design and increased variety in both balloon diameter and length make navigation in the anterior cerebral and the anterior communicating arteries more feasible today.21 In our series the rate of BACE was 52.3%, which is higher than the rates reported in the ATENA17 (37.3%) and CLARITY16 series (20.5%).

The most serious complications of the endovascular treatment of intracranial aneurysms are thromboembolic events and intraprocedural aneurysm rupture. Our study showed that the incidence of these complications was similar in the BACE and CCE groups and corroborates the results of recent studies8 ,16 ,17 that showed similar safety profiles in the standard coiling and the balloon remodeling technique. The rate of thromboembolic events was lower in our series, which may reflect differences in systemic anticoagulation among the various authors, the use of periprocedural aspirin and different percentages of patients with SAH, which is known to be a hypercoagulable condition.23 In addition, in a small number of cases the balloon was positioned across the aneurysm neck but was not inflated for safety in case of rupture. This technique was only used for embolization of very small aneurysms (≤3 mm) that have a high risk of intraprocedural aneurysm rupture.

In very small aneurysms with increased risk of rupture we propose the use of BACE. While some would argue that positioning a balloon across the aneurysm neck when CCE is feasible carries an increased thromboembolic risk, we feel that in the event of rupture, the balloon serves as a safety net that can be used to minimize bleeding and promote intra-aneurysmal thrombosis. The rate of intraprocedural aneurysm ruptures in our series was comparable to the rates published by Pierot et al in 2009 and 2011.16 ,17 There was a trend for more intraprocedural aneurysm ruptures in the BACE group in our series, but no statistically significant difference. This could be explained by the fact that BACE was used in more complex aneurysms and with small aneurysms that carry a higher risk of intraprocedural aneurysm rupture.20 ,24–26 In all cases of intraprocedural aneurysm rupture in the BACE group, inflation of the balloon across the aneurysm neck allowed for hemostasis immediately after the rupture was identified. The incidence of device-related problems was reported in the ATENA study17 to be slightly lower than reported in our series (2.7% vs 3.3%). Since the definition of this complication is somewhat arbitrary, a definitive comparison between the studies is problematic. The important finding in both our study and the ATENA study is that the risk of device-related problems was similar between the CCE and BACE groups. The procedure-related mortality and morbidity rates in our series were slightly higher in the BACE group, but the difference was not statistically significant. In 2006, Sluzewski et al12 reported their results of a single-center retrospective analysis of 827 ruptured and unruptured aneurysms and showed that the incidence of thromboembolic events, intraprocedural aneurysm ruptures, procedure-related morbidity and mortality was significantly higher with the remodeling technique than with CCE. Similarly, our study was retrospective, performed at a single institution and contained a mix of patients with both acutely ruptured and unruptured aneurysms. In contradistinction, our study did not demonstrate a statistically significant increase in clinically significant adverse outcomes in patients undergoing BACE compared with those who undergo CCE. It is important to point out that, in the study by Sluzewski et al,12 the balloon remodeling technique was implemented in a small percentage of patients (8.6%)—namely, in those patients in which standard coil embolization had failed, was impossible or in those cases where the anticipated surgical risk was too high. Thus, their data were in no doubt skewed to favor a higher complication rate as the patients treated with BACE were those with the most technically complex aneurysms and/or the most complicated clinical picture. On the other hand, some may argue that our data are somewhat skewed to favor positive outcomes as the preference of our group is, at times, to have a balloon present for aneurysms that would not traditionally require balloon remodeling. As described above, this ‘unconventional’ use of the BACE technique was limited to aneurysms measuring ≤3 mm, which only represented a small percentage of the total aneurysms in our series. Lastly, we would like to address the fact that a total of 56 aneurysms were treated with polymer-coated coils. Our group recently published a paper comparing treatment results between bare platinum and polymer-coated coils and showed no significant difference in complication rates.27 Thus, the use of polymer-coated coils did not affect the complication rates in this series.

Our study has several limitations. First, it was a retrospective study and power analysis was not performed because all patients treated with either CCE or BACE during this time period were included in the analysis. Second, this was not a randomized study. Since certain aneurysm characteristics (ie, neck size) were different between the two groups, they would act as confounders. In addition, the indications for BACE and CCE are not the same and a randomized trial would be difficult to design. Second, the operator determined the indication for BACE on a case-by-case basis without strict criteria. A third limitation of the study is that we included a mixture of acutely ruptured and unruptured aneurysms that represent different clinical situations with different levels of acuity and complexity. Finally, ours is a single-center study with operators experienced in the BACE technique; thus, some may question the generalizability of our results in the entire community.

In conclusion, our study shows that the use of compliant balloons as adjuncts for intracranial aneurysm coil embolization is not associated with increased procedure-related risks. In our series of patients with acutely ruptured and unruptured aneurysms, the BACE technique allowed us to treat aneurysms with unfavorable anatomic characteristics without increasing the incidence of procedure-related complications and allowed for immediate control in cases of intraprocedural aneurysm rupture. We consider that the BACE technique represents a crucial tool for the embolization of intracranial aneurysms.

Acknowledgments

The authors thank Paul Christos for his statistical analysis in preparing the manuscript. His work was partially supported by the following grant: Clinical Translational Science Center (CTSC) (UL1-RR024996).

References

Footnotes

  • Competing interests None.

  • Ethics approval The study was approved by the ethics committee of New York Presbyterian Hospital/Weill Cornell Medical Center.

  • Provenance and peer review Not commissioned; externally peer reviewed.