Dual microcatheter coil embolization of acutely ruptured wide-necked intracranial aneurysms

Abstract

The dual microcatheter technique is an alternative treatment for stent-assisted coiling in acutely ruptured wide-necked aneurysms because of no antiplatelet therapy. We assessed the safety and efficacy of this technique in ruptured wide-necked aneurysms. Between March 2008 and March 2016, 56 acutely ruptured aneurysms were treated with the dual microcatheter technique. The angiographic results, treatment-related complications, and clinical outcome were documented. Angiographic follow-up was available in 37 patients at a mean of 20.6 months (6 to 81 months). On the postembolization angiograms, 27 (48.2%) aneurysms showed complete occlusion (Raymond 1), 15 (26.8%) showed neck remnant (Raymond 2), and 14 (25.0%) showed body remnant (Raymond 3). Treatment-related complications occurred in seven patients (12.5%) and six patients remained asymptomatic. The permanent complication rate was 1.8% (1/56). A good outcome (modified Rankin Scale (mRS) score, 0–2) was observed in 64.3% of patients at the time of discharge. Five patients had died, all of the sequelae of subarachnoid hemorrhage. The overall mortality rate was 8.9% (5/56); however, the treatment-related mortality rate was 0%. Of the 37 aneurysms for which angiographic follow-up was available, 21 (56.8%) aneurysms demonstrated recanalization. Five aneurysms with recanalization were retreated endovascularly. There was one aneurysm re-rupture on follow-up and it rebled 21 months after the initial procedure. The dual microcatheter technique is a safe and effective treatment for acutely ruptured wide-necked aneurysms due to low treatment-related complication and mortality rate. However, the high rate of postembolization incomplete occlusion and recanalization remains as the main challenge.

Introduction

The neck remodeling technique with stents has been widely used to treat wide-necked intracranial aneurysms.^1–7 With the use of stents in acutely ruptured aneurysms, however, complication rates tend to be higher than with selective coiling or balloon-assisted coiling because of the thrombogenicity of the stents and the need for dual antiplatelet medication with inherent risk in the postoperative period.^1–4,8,9 Moreover, many practitioners regard using dual antiplatelet agents in the stent-assisted technique for ruptured aneurysms as exposing patients to high risk of bleeding-related complications if interventions such as external ventricular drainage placement or ventriculoperitoneal shunt surgery are subsequently required.^3,4,8–10 In contrast, balloon-assisted coiling does not require dual antiplatelet therapy. However, balloon navigation can be difficult in tortuous cervical or intracranial vessels or acute angle of the parent vessel. In case of aneurysms with completely unfavorable dome-to-neck ratio with a very wide neck, the stabilization of coils into the aneurysm sac can be impossible despite inflation of the balloon in front of the neck. In addition, there are significant data to suggest that coil prolapse and following thromboembolic complications may continue to limit the utility of this procedure.¹¹

The dual microcatheter technique is another option for endovascular treatment of wide-necked intracranial aneurysms. The use of two microcatheters for aneurysm embolization is not a new concept. In 1998, Baxter et al.¹² reported two such cases and in 2005, Kwon et al.¹³ and Durst et al.¹⁴ in 2014 reported techniques and outcomes. This technique does not require dual antiplatelet therapy. In this study, we assessed the safety and efficacy of this technique in the setting of acute subarachnoid hemorrhage (SAH).

Materials and methods

This study was approved by the institutional review board. We retrospectively analyzed data in all patients with ruptured wide-necked intracranial aneurysms who were treated with the dual microcatheter technique at National Health Insurance Service Ilsan Hospital in South Korea during the study period (March 2008 to July 2016). During this period, 61 patients presenting with an SAH secondary to a ruptured wide-necked aneurysm were treated with the dual microcatheter technique on the day of admission or on the following day. Five patients were attempted to be treated with the dual microcatheter technique in the beginning; however, the coil mass protruded into the parent artery. Finally, they were treated with balloon-assisted coiling in one patient and a stent-assisted technique in four patients. These patients were excluded, leaving 56 patients. All aneurysms were assessed before endovascular treatment with conventional angiography. Angiography was performed with Biplane Integris Allura angiography units (Philips Healthcare, Best, the Netherlands). The size of each aneurysm and neck was measured in three-dimensional (3D) angiographic images by using the angiography unit software. Wide-necked aneurysms were defined as aneurysms with a dome-to-neck ratio of <2 or a neck diameter of ≥4 mm. In our study there were two aneurysms that showed a dome-to-neck ratio >2; however, they had a neck diameter ≥4 mm. The patients and aneurysm characteristics are detailed in Table 1.

Table 1.

Patient and aneurysm characteristics.

	Number
Age (years)	40–81 (mean, 60.1)
Sex: male/female	21/35
Aneurysm location
MCA	7 (12.5%)
AcomA/ACA	27 (48.2%)
Basilar bifurcation	4 (7.1%)
PcomA/Anterior choroidal artery	16 (28.6%)
ICA bifurcation	1 (1.8%)
VA/PICA	1 (1.8%)
Aneurysm size	3.5–15.6 (mean, 7.3 mm)
Neck size	2.1–8.8 (mean, 4.1 mm)
Dome-to-neck ratio	0.92–2.15 (mean, 1.46)

MCA: middle cerebral artery; AcomA: anterior communicating artery; ACA: anterior cerebral artery; PcomA: posterior communicating artery; ICA: internal carotid artery; VA: vertebral artery; PICA: posterior inferior cerebellar artery.

In all patients, coil embolization was performed as the primary treatment. The dual microcatheter technique was chosen after the failure of conventional single-catheter technique in eight (14.3%) aneurysms. In the remaining 48 (85.7%) aneurysms, the dual microcatheter technique was adopted from the beginning. The patients receiving endovascular coiling were systemically anticoagulated with intravenous heparin after deployment of the first coil with initial boluses of 50 U/kg followed by continuous infusions of 10 U/kg per hour. Technical details of the dual microcatheter technique have been described previously.^13,14

Complications were classified as any hemorrhage, infarction, or dissection that was related to the procedure and resulted in permanent morbidity or mortality. Clinical outcome was evaluated by using the modified Rankin Scale (mRS), with a score of 0–2 defined as a good outcome.¹⁵ Because clinical outcomes are highly dependent on preprocedural clinical conditions, these data were evaluated in the context of the degree of neurologic compromise at the time of presentation, which was usually reported by using the Hunt and Hess grading system.

Angiographic follow-up using digital subtraction angiography or magnetic resonance angiography was available for 37 patients and duration of angiographic follow-up ranged from 6 to 81 months with a mean of 20.6 months. Follow-up angiogram was not available for 19 patients. The causes include death (five), severe disability (six), patients lost to follow-up (four), and patient refusal (four). Follow-up digital subtraction angiography included a repeat of the projections obtained during postembolization check for comparative analysis. The operator obtained additional projections if it was believed to be appropriate (especially if aneurysm recurrence was noted).

The postembolization angiogram and the follow-up angiogram for each aneurysm were assessed in conjunction with two observers (P.H.Y. and J.W.L.). Angiograms were graded on the basis of a modified three-point Raymond scale (Raymond 1 = complete obliteration of aneurysm including the neck; Raymond 2 = contrast filling the neck of the aneurysm without opacification of aneurysm sac; and Raymond 3 = contrast filling the sac of the aneurysm).¹⁶ Aneurysms were then classified as stable (no change in coil configuration, obliteration grade, or contrast filling), improved (progressive occlusion or involution of the neck remnant or contrast filling in aneurysm), and recanalized (aneurysm recurrence evident due to neck growth, coil compaction, coil extrusion by aneurysm degradation, or new sac formation).¹⁷

Results

On the immediate postembolization angiograms, 27 (48.2%) aneurysms showed complete occlusion (Raymond 1), 15 (26.8%) showed contrast filling the neck of the aneurysm (Raymond 2), and 14 (25.0%) showed contrast filling the sac of the aneurysm (Raymond 3).

Treatment-related complications developed in seven (12.5%) of 56 patients: six (10.7%) thromboembolic events and one (1.8%) intraoperative rupture. A permanent neurologic deficit developed in one (1.8%) of 56 patients. Four of six thromboembolic complications were anterior communicating artery aneurysms, one in the middle cerebral artery, and one in the basilar artery. The immediate postembolization angiograms showed thrombus formation around the deployed coil. Thrombi were resolved with an intra-arterial bolus infusion and continuous intravenous infusion of tirofiban. No thrombus formation was demonstrated on delayed angiograms (Figure 1). Five thromboembolic complications resulted in no permanent neurologic deficit. However, one patient had a weakness of the right extremities after the procedure. Diffusion-weighted magnetic resonance images showed multiple infarctions in the cerebral and cerebellar hemispheres including the left pons, resulting in permanent motor deficit. There was one intraoperative rupture of anterior communicating artery aneurysm and extravasation of contrast medium was noted during the coil embolization. Systemic anticoagulation was immediately reversed with protamine and the aneurysm was completely occluded with additional coils. The procedure was terminated after verifying no leakage of contrast medium. The patient had no permanent neurologic deficit afterward. Ultimately, the permanent complication occurred in one (1.8%) of 56 cases.

Figure 1.

Ruptured basilar artery aneurysm in a 52-year-old man treated with the dual microcatheter technique. (a) Conventional and three-dimensional (3D) angiography showed a wide-necked basilar aneurysm. (b) Two microcatheters were introduced into the aneurysmal sac and two coils formed a stable frame. (c) During the procedure, a filling defect at the proximal P1 segment of the right posterior cerebral artery was shown, which improved after administration of intra-arterial tirofiban infusion. The aneurysm was partially occluded with a remnant sac (Raymond 3). (d) and (e) Follow-up conventional and 3D angiography after eight months showed coil compaction with more recanalization of the aneurysm. (f) The patient was retreated and the aneurysm showed nearly complete obliteration after coiling with the dual microcatheter technique.

Thirty-six (64.3%) patients demonstrated good outcome (mRS score, 0–2) at the time of discharge. The individual mRS scores were as follows: 14 (25.0%) mRS of 0, 14 (25.0%) mRS of 1, eight (14.3%) mRS of 2, three (5.4%) mRS of 3, seven (12.5%) mRS of 4, five (8.9%) mRS of 5, and five (8.9%) mRS of 6. Of 43 patients who had favorable initial presentation (Hunt and Hess grade I–III), 35 (81.4%) had good outcomes, and six (14.0%) had poor outcomes, and two (4.7%) died. Of 13 patients who had poor initial presentation (Hunt and Hess grade IV–V), one (7.7%) had a good outcome, and nine (69.2%) had poor outcomes, and three (23.1%) died. Overall, 36 (64.3%) had good outcomes, and 15 (26.8%) had poor outcomes, and five (8.9%) died (Table 2). However, none of the deaths was directly related to the treatment. One patient who developed myocardial infarction died of cardiac arrest. One patient died of sequelae from ventriculitis after external ventricular drainage. The remaining three patients died from devastating neurologic injury directly attributable to the presenting hemorrhage. The overall mortality rate for this series was 8.9%; however, the treatment-related mortality rate was 0%.

Table 2.

Clinical presentations and outcomes.

Clinical outcomes	Clinical presentation		Total
	Favorable (HH I–III)	Poor (HH IV–V)
Favorable outcome (mRS 0–2)	35 (81.4%)	1 (7.7%)	36 (64.3%)
Poor outcome (mRS 3–5)	6 (14.0%)	9 (69.2%)	15 (26.8%)
Death (mRS 6)	2 (4.6%)	3 (23.1%)	5 (8.9%)
Total	43 (76.8%)	13 (26.5%)	56 (100%)

mRS: modified Rankin Scale; HH: Hunt and Hess scale.

Among 56 aneurysms treated with the dual microcatheter technique, follow-up angiograms were available for 37 cases. Of these, 16 (43.2%) showed stable appearance and 21 (56.8%) showed recanalization. No aneurysm showed improved occlusion on follow-up angiogram (Table 3). Among 21 aneurysms that showed recanalization on follow-up angiograms, further follow-up angiograms were performed in nine patients. They all showed no change in aneurysm configuration on the subsequent follow-up angiograms (Figure 2).

Table 3.

Follow-up angiographic results.

Follow-up angiography	Postembolization angiography			Total
	Raymond I	Raymond II	Raymond III
Raymond I	11	0	0	11
Raymond II	5a	5 (2a)	0	10
Raymond III	3a	6a	7 (5a)	16
Total	19	11	7	37
Recanalization	8/19 (42.1%)	8/11 (72.7%)	5/7 (71.4%)	21/37 (56.8%)

Numbers in parentheses are aneurysms demonstrating change in the aneurysm configuration with no change in Raymond scale.

^aAneurysms demonstrating recanalization of the aneurysm.

Figure 2.

Ruptured anterior communicating artery aneurysm in a 42-year-old man treated with the dual microcatheter technique. (a) and (b) Conventional and three-dimensional angiography showed a wide-necked anterior communicating artery aneurysm. (c) Two microcatheters were introduced into the aneurysmal sac. (d) Postembolization angiography showed near complete obliteration of the aneurysm. (e) Follow-up angiography after nine months showed recanalization of the aneurysm in the neck. (f) No change appeared in the aneurysm on 21-month follow-up angiography.

Endovascular retreatment was performed in five of 37 aneurysms (13.5%) for which follow-up angiograms were available. There was one aneurysm re-rupture on follow-up. It occurred at the aneurysm that was incompletely packed during the initial procedure (Raymond 3). It rebled 21 months after the initial procedure and was retreated with a conventional single-catheter technique. Two aneurysms were treated with stent-assisted coiling, one aneurysm with a microcatheter-protective technique, and one aneurysm with the dual microcatheter technique (Figure 1).¹⁸

Discussion

The dual microcatheter technique, which does not require the routine use of dual antiplatelet therapy, represents an alternative endovascular approach to wide-necked intracranial aneurysms. It is also useful when a wide neck width is combined with a distal aneurysm location (e.g. in the distal anterior cerebral artery) because it may be too distal for balloons or stents but not too distal for microcatheters. In our study two patients had distally located aneurysms. One aneurysm was located in the pericalloso-callosomarginal artery junction and the other in the M2–M3 junction of the middle cerebral artery. These locations are quite distal for balloons or stents but not too distal for microcatheters. Thus, dual microcatheter coil embolization has an advantage over balloon remodeling or stent-assisted embolization for distally located aneurysms. In this study, we assessed the safety and efficacy of the dual microcatheter technique for the treatment of acutely ruptured wide-necked aneurysms, primarily compared to those of stent-assisted coiling series.

Postembolization angiographic results

In a review of the literature about stent-assisted coiling in acutely ruptured intracranial aneurysms, 63% of aneurysms showed complete occlusion, 19% showed a neck remnant, and 18% of aneurysms showed residual patency or no occlusion in the aneurysm.³ In a recently published series with a large population size, 87.5% of patients showed immediate occlusion (≥95%).⁴ In our study, 48.2% of aneurysms showed complete occlusion, 26.8% showed contrast filling the neck of the aneurysm, and 25.0% showed contrast filling the sac of the aneurysm. Indeed, our study shows a relatively high rate of incomplete occlusion of aneurysms (51.8%) compared with the stent-assisted technique (37%). This may be due to the fact that complete occlusion of the wide-necked aneurysm with detachable coils in the dual microcatheter technique is difficult. Compared with stent-assisted coiling, the coil instability within the aneurysm or protrusion of coil loops on the parent artery is far more intense. This is one of the inherent shortcomings of the dual microcatheter technique that cannot be easily resolved.

Complications

The two most frequent complications of the endovascular treatment of intracranial aneurysms are thromboembolic events and intraoperative rupture. In a systematic review of the literature about stent-assisted coiling in acutely ruptured intracranial aneurysms, 13% of patients had clinically evident intracranial complications thought to be related to stent-assisted coiling.³ Chalouhi et al.⁴ reported that overall complications were noted in 25% of patients with acutely ruptured aneurysms causing death and permanent morbidity in 12.7%. Bechan et al.¹⁹ also reported a 13% morbidity-mortality rate in patients with a ruptured aneurysm. In another recently reported systematic review of complications in stent-assisted endovascular therapy of ruptured intracranial aneurysms, the event rates of thromboembolism and intra- and postprocedural hemorrhage were 11.2%, 5.4%, and 3.6%, respectively.⁸ Moreover, in patients requiring external ventricular drainage due to acute hydrocephalus, periprocedural complication rates were higher.⁹ In our study, the overall treatment-related complication rate is only 1.8%. This result is much lower than that of stent-assisted coiling series, probably due to absence of thrombogenic stent, absence of dual antiplatelet therapy, and a short operation time in the dual microcatheter technique.

Clinical outcome

In a review of the literature about stent-assisted coiling in acutely ruptured intracranial aneurysms, 67% of patients had favorable clinical outcomes (Glasgow Outcome Scale 4 or 5), 14% had poor clinical outcomes, and 19% died.³ Taylor et al.²⁰ also reported a 73.8% favorable clinical outcome in SAH patients. Our study reported that 64.3% of patients had favorable clinical outcomes and 35.7% of patients had poor clinical outcomes or death. This result is less favorable compared with the result of stent-assisted coiling. Because clinical outcomes are highly dependent on preprocedural clinical conditions, these data were evaluated in the context of the degree of neurologic compromise at the time of presentation, which was usually reported by using the Hunt and Hess grading system. Of 43 patients who had favorable initial presentation (Hunt and Hess grade I–III), 35 (81.4%) had good outcomes and eight (18.6%) had poor outcomes in our series. This result is comparable to the result of stent-assisted coiling, which demonstrated 81% good clinical outcome for good-grade aneurysms.³

Recanalization, re-rupture, and retreatment

In our study, 56.8% of aneurysms for which angiographic follow-up was available showed recanalization and no angiographic improvement of aneurysm occlusion was observed. On the other hand, in a recently reported stent-assisted coiling series with a large population, the rate of recanalization was 12%.⁴ In our study, of the 19 patients who did not have follow-up angiography, eight patients showed complete occlusion of the aneurysm on the immediate postembolization angiography. If these patients had been included, the recanalization rate in our study might have been significantly reduced. Nevertheless, our data clearly show higher recanalization rate and lower angiographic improvement compared with the stent-assisted coiling series. This result may be because of a high rate of incomplete occlusion of the aneurysm on the immediate postembolization angiogram in our study (51.8%). Coiling wide-necked aneurysms without a stent or a balloon may increase the risk of coil herniation and parent artery occlusion, which may lead to a high rate of incomplete occlusion and increased recanalization rate.

Recanalization is a major issue with endovascular treatment; however, its impact on rebleeding rates is not completely clarified. Despite recanalization rates as high as 38%, reports on the incidence of rebleeding after coiling vary.^21–24 In our study, the recanalization rate was as high as 56.8%; however, aneurysm rupture after endovascular treatment was noted in only one of the patients for whom angiographic follow-up was available (2.7%, 1/37). Paradoxically, there have been many reports that the degree of initial aneurysm occlusion is associated with rebleeding.^21,25,26 According to investigators in the Cerebral Aneurysm Rerupture After Treatment study on predictors of rehemorrhage after treatment of ruptured intracranial aneurysms, the degree of aneurysm occlusion was highly predictive of the risk for re-rupture, which increased progressively as the packing attenuation decreased.²¹ Loose packing with coils in ruptured aneurysms seems to lead to an increased risk of recurrent SAH compared with total or nearly total occlusion.²⁶ Even in stent-assisted coiling, compact coil packing should be performed to achieve the best long-term outcomes.²⁷ In our study, there was one aneurysm of re-rupture in follow-up, which was incompletely packed initially. Therefore, when embolizing aneurysms with coils, achieving total or nearly total occlusion is the key to preventing recurrent hemorrhage and regrowth of the aneurysm, even in cases using the dual microcatheter technique.

In Taylor’s report on stent-assisted coiling in acutely ruptured aneurysms, six patients (17.6%) were retreated.²⁰ Chalouhi et al.⁴ reported that 27 patients (6.4%) were retreated after stent-assisted coiling. In Starke’s report, recurrence or retreatment rates were no higher in patients treated with the dual microcatheter technique than in those treated with stent-assisted coil embolization (15.1% versus 17.1%).²⁸ In our study, five aneurysms (13.5%) with recanalization including one re-ruptured case were retreated endovascularly. The retreatment rate in our study is similar to the other results of stent-assisted coiling and dual microcatheter technique series. Although more recurrences can be expected with this technique, the aneurysms with major recanalization on follow-up angiogram can be managed without difficulty with standard coiling, balloon-assisted coiling, stent-assisted coiling, or surgical clipping.

Study limitations

Our study has several limitations. First, the small population size and short follow-up interval of our series may be insufficient to capture the safety, efficacy, and clinical outcome of the dual microcatheter technique that we used in our cohort. Second, the retrospective nature of our study may limit its external validity. Third, we did not evaluate the relationship between the packing density and aneurysm recurrence rate. The mean packing density in our study is 28.7%, and aneurysm packing density of >18%–24% has been reported to lead to a reduced recurrence rate.²⁹ One large series, however, reported no relationship between packing density and recurrence.³⁰ Finally, in some patients magnetic resonance angiography was performed instead of digital subtraction angiography. This might induce the inaccurate comparison between the immediate postoperative and follow-up results. However, we also evaluated the magnetic resonance angiographic source images and it contributed to a more precise comparison. Thus, further study with a large population, prospective design, longer follow-up interval, evaluation of the relationship between packing density and recurrence rate, and digital subtraction angiographic follow-up would be necessary to address these deficiencies.

Conclusion

In this study, our data show that the dual microcatheter technique is safe and effective for coil embolization of acutely ruptured wide-necked intracranial aneurysms with a low treatment-related complication, morbidity, and mortality rate, even though it shows the high rate of the immediate postembolization incomplete occlusion and recanalization of the aneurysm. Larger population size and longer-term angiographic follow-up information are needed to secure the safety and durability of this treatment.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Ilsan Hospital, National Health Insurance Service in 2012 (grant number: 2012-64).