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Table of Contents
Vol. 35, No. 3, 2013
Issue release date: April 2013
Section title: Original Paper
Cerebrovasc Dis 2013;35:235-240
(DOI:10.1159/000347078)

Endovascular Treatment of Very Small and Very Large Ruptured Aneurysms of the Anterior Cerebral Circulation: A Single-Center Experience

Mohammadian R.a · Asgari M.b · Sattarnezhad N.a · Mansourizadeh R.c · Mohammadian F.a · Shimia M.b · Talebi M.a · Meshkini A.b · Amirkolahy M.b
aNeuroscience Research Center, and bNeurosurgery Department, Tabriz University of Medical Sciences, and cNeurology Department, Alinasab Hospital, Tabriz, Iran
email Corresponding Author

Reza Mohammadian

Neuroscience Research Center

Tabriz University of Medical Sciences

PO Box 51665-348, Tabriz (Iran)

E-Mail diako30@yahoo.com


Abstract

Introduction: Endovascular treatment of aneurysms has been introduced as a less invasive method for decreasing the rate of aneurysm rerupture and subsequent subarachnoid hemorrhage. The outcome and complication rate for endovascular treatment of very small (≤3 mm) and very large (15-25 mm) intracranial aneurysms has been controversial. Here we report our experience with endovascular coiling of very small and very large ruptured aneurysms of the anterior cerebral circulation. Methods: Patients were included in the study if the maximum dimension of the intracranial ruptured aneurysm was reported to be ≤3 mm or 15-25 mm and if the aneurysm was within the anterior cerebral circulation. The largest dimension was calculated using CT angiography and was confirmed by digital subtraction angiography. Endovascular coiling was performed using Guglielmi detachable coils. All patients underwent follow-up contrast MR angiography every 6 months. Results: A total of 40 cases (18 females and 22 males) were included in this single-center study. Twenty-one very small and 19 very large ruptured aneurysms were analyzed. Preprocedural Hunt and Hess grades were determined. Endovascular coiling was performed successfully in most cases (97.5%), with unsuccessful coiling in 1 patient with a very small ruptured aneurysm. In the very small aneurysm group, the most common location was the anterior communicating artery and, in the large aneurysm group, the most common location was the middle cerebral artery (MCA) bifurcation. The mean follow-up time was 15.08 months (range: 6-30 months). The 6th month modified Rankin scale (mRS) values for very small aneurysm cases were 0 (no symptoms at all) in 16 cases (76.2%) and 1 (no significant disability despite symptoms) in 5 cases (23.80%). For the very large aneurysm cases, the mRS values were 1 in 2 cases (10.5%), 2 in 7 cases (36.8%), 3 in 6 cases (31.6%), 4 in 3 cases (15.8%) and 6 in 1 case (died due to vasospasm 72 h later; 5.2%). The immediate complications that were observed were MCA branch occlusion in 1 very small aneurysm patient and early vasospasms in 3 very large aneurysm patients. The late complication that was observed was recanalization in 1 very small aneurysm case (1/21, 4.76%) and in 5 very large aneurysm cases (5/18, 27.77%). Conclusion: Endovascular treatment of very small aneurysms is an effective method of treatment with acceptable immediate and long-term outcomes. Immediate and long-term complications were more prevalent in very large ruptured aneurysms.

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Introduction

With ruptured aneurysms, intervention is aimed at reduction of the rebleeding rate [1,2,3]. Surgical clipping of ruptured aneurysms was the method of choice for intervention until endovascular treatment was introduced as a less invasive method with a lower complication rate [4,5]. However, this method has some limiting factors, as with any technique [6].

The outcome and complication rate for endovascular treatment of very small (≤3 mm) and very large (15-25 mm) intracranial aneurysms has been controversial. Here we report our experience with endovascular coiling of very small and very large ruptured aneurysms of the anterior cerebral circulation, which is the first such report from northwest Iran.

Materials and Methods

This prospective cohort study was designed to compare intraprocedural, long-term outcomes and complications of endovascular coiling of very small (≤3 mm) and very large (15-25 mm) ruptured aneurysms of the anterior cerebral circulation. Forty patients, who were admitted to our institution from October 2008 to July 2011 and were candidates for endovascular coiling, were included in the study if the maximum dimension of the ruptured aneurysm was reported to be ≤3 mm (very small) or 15-25 mm (very large) and the patient was harboring an aneurysm located within the anterior cerebral circulation. The convenience sampling method was used to select the patients.

The largest dimension of an aneurysm was calculated with the use of CT angiography and was confirmed by digital subtraction angiography (DSA). The patient was excluded if he/she had comorbid conditions such as a parenchymal hematoma with a mass effect. Informed consent was obtained for the use of patient data (i.e., demographic information, complications and follow-up results) for this report. Preprocedural Hunt and Hess (H&H) grades were recorded for each patient. All the cases underwent endovascular coiling after induction of general anesthesia. During the coiling procedure, a heparinized saline flush was used in the coaxial catheters for the prevention of intraprocedural thrombosis. Systemic heparinization was avoided during all procedures. Soft and stretch resistant Guglielmi detachable coils were utilized for coiling. Coiling was done under road mapping guidance. After the first coil has created a mesh, the aneurysm was densely packed with soft coils of decreasing diameter, until no more coils can be deployed into it. Repositioning of the microcatheter tip was done when necessary. We try to avoid using neck-remodeling techniques. These techniques make procedures more challenging and significantly increase the cost of treatment.

Intraprocedural rupture (IPR) was defined as contrast extravasations during intervention. Intraprocedural and postprocedural controls were employed for the detection of any possible signs of stroke or vasospasm. Complete or adequate occlusion was defined as no filling defect or contrast filling in the sac of the coiled aneurysm immediately after the procedure. In the very small aneurysm group, a neck remnant at the end of the procedure was not considered as an incomplete coiling.

Vasospasm was treated with a combination of intravenous and local intra-arterial injection of nimodipine. Intravenous nimodipine started with 1 mg/h in the first 2 h; then it continued with 0.5 mg/h for at least 7 days up to a maximum of 14 days. The dose of nimodipine infused intra-arterially was 1-3 mg per treated vessel and the total dose was 5 mg. The drug was infused at a rate of 0.1 mg/min continuously. Nimodipine was temporarily suspended if refractory hypotension developed.

All patients underwent a control 3-dimensional time-of-flight MR angiography (MRA) 6 months after the procedure; however, for high-risk patients with suspected incomplete occlusion, an additional MRA was done after 1 month. A control MRA was repeated each 6 months and, in the case of evidence of recanalization, DSA was done for further evaluation. The clinical outcome was assessed using a modified Rankin scale (mRS) at the 6th month.

For the purpose of univariate analysis, the Fisher exact test and the Mann-Whitney test were used, if appropriate. All the statistical analyses were performed with SPSS version 17.0.0 software. The probability value was considered to be significant if p ≤ 0.05.

Results

A total of 40 cases were included in this single-center study (18 females and 22 males). Twenty-one very small and 19 very large ruptured aneurysms were analyzed. The mean ± SD age of the patients was 44.37 ± 15.37 years (minimum: 19, maximum: 72). The mean age of the very small group was 34.35 ± 9.33 and the mean age of the very large group was 54.35 ± 14.22 years.

All cases presented with an episode of subarachnoid hemorrhage (SAH), diagnosed as a very small (≤3 mm) or very large (15-25 mm) ruptured aneurysm within the anterior cerebral circulation (aneurysm locations are shown in tables 1 and 2). One patient in the very small aneurysm group had a history of two previous episodes of SAH. He presented with another episode of bleeding because of a very small aneurysm in the anterior communicating artery (ACOM).

Table 1

Location of very small ruptured aneurysms

http://www.karger.com/WebMaterial/ShowPic/174474

Table 2

Location of very large ruptured aneurysms

http://www.karger.com/WebMaterial/ShowPic/174473

The most common location in the very small group was the ACOM (47.60%) and the most common location in the very large aneurysm group was the middle cerebral artery (MCA) bifurcation (63.15%).

The preprocedural H&H grades for very small ruptured aneurysms were 2 in 14 cases (66.7%) and 3 in 7 cases (33.3%). The corresponding grades for very large ruptured aneurysms were 2 in 6 cases (31.6%), 3 in 11 cases (57.9%) and 4 in 2 cases (10.5%).

Complete coiling was accomplished in most very small aneurysms (97.50%), with 1 case with a ruptured aneurysm of the ACOM as unsuccessful. Coiling was unsuccessful due to the failure of coil delivery (2.50%). In the very large aneurysm group, complete coiling was achieved in 16 cases (84.20%) and partial coiling in 3 cases (15.80%).

An immediate complication for cases with very small aneurysms was MCA superior division branch occlusion in 1 case. In this particular case, the aneurysm was located in the left-sided MCA bifurcation. Final control angiography showed the occlusion of the MCA superior branch, which reopened with local infusion of 12 mg rt-PA (fig. 1). The patient did not show any neurological deficits.

Fig. 1

A 36-year-old patient with ruptured very small aneurysm in the left MCA bifurcation. It was coiled successfully. Final control DSA showed occlusion of the superior branch of the MCA (middle image); 12 mg of rt-PA was injected locally and the artery recanalized. The patient did not show any neurological deficit (right image).

http://www.karger.com/WebMaterial/ShowPic/174472

In the very large aneurysm series, immediate complications were 3 cases of vasospasm; 1 of them died 72 h later. All of these cases presented with a very large aneurysm in the MCA bifurcation. We were able to manage vasospasm in all 3 cases. In 2 of these cases, vasospasm occurred in the superior division of the MCA and in another, in the distal M1. All patients had a good angiographic response to local nimodipine injection but, despite an excellent angiographic response, the patient with a left M1 vasospasm developed extensive ischemia in the territory of the left MCA and died 3 days later (fig. 2).

Fig. 2

A 40-year-old lady presented with ruptured very large aneurysm in the left MCA bifurcation. It underwent successful coiling. She developed severe vasospasm in the distal M1 immediately after the coiling (middle image). Vasospasm was treated with local nimodipine injection and there was excellent angiographic response (right image). A few days later, she developed severe ischemia in the territory of same artery and died.

http://www.karger.com/WebMaterial/ShowPic/174471

The mean follow-up time was 15.08 months (range: 6-30 months). The mean follow-up period was 12.5 ± 5.03 months (range: 6-23 months) for very small ruptured aneurysms and 17.82 ± 7.77 months (range: 7-30 months) for very large aneurysm cases.

In long-term follow-up, recanalization was detected in 1 case with a very small aneurysm after 6 months. The patient was a 50-year-old woman with a ruptured aneurysm in the right MCA bifurcation. Investigation, including DSA, showed minor recanalization, which remained asymptomatic.

In the patients with very large aneurysms, 5 cases developed recanalization (2 after 6 months, another after 12 months and, in total, 5 cases after 18 months). A patient with a large aneurysm in the left MCA bifurcation presented with an episode of right-sided paresthesia and speech difficulty 12 months after the procedure. MRA and DSA showed evidence of recanalization (fig. 3). He underwent uneventful coiling, but a month after the procedure he died because of myocardial infarction.

Fig. 3

A 58-year-old male with ruptured aneurysm in the left-sided MCA (left image). It underwent near-complete coiling (middle image). One year later, he presented with right-sided paresthesia and speech difficulty. DSA showed evidence of recanalization (right image). He underwent a second session of coiling, but a month later, he died because of myocardial infarction.

http://www.karger.com/WebMaterial/ShowPic/174470

The 6th month mRS values for very small aneurysm cases were 0 (no symptoms at all) in 16 cases (76.2%) and 1 (no significant disability despite symptoms) in 5 cases (23.80%). For the very large aneurysm cases, the mRS values were 1 in 2 cases (10.5%), 2 in 7 cases (36.8%), 3 in 6 cases (31.6%), 4 in 3 cases (15.8%) and 6 in 1 case (died due to vasospasm 72 h later; 5.2%).

Discussion

In this paper, we report our single-center experience with endovascular coiling of very small (≤3 mm) and very large (15-25 mm) ruptured aneurysms of the anterior cerebral circulation, including intraprocedural and long-term complications in 2 isolated groups.

Outcomes in Patients with Very Small Aneurysms

Successful coiling was achieved in all aneurysms except for the failure of coil delivery in an ACOM aneurysm. In our very small aneurysm case series, an intraprocedural complication was observed as an MCA branch occlusion and a case of recanalization was detected in long-term follow-up. Both patients have remained asymptomatic. Some reports have stated that the recurrence rate for small-size aneurysms is low; however, this rate is higher in patients that suffered from a ruptured aneurysm [7,8,9] and our finding was in accordance with these reports.

In this study, we had a very low rate of complications, one of which was a thrombotic accident that was handled without any neurological consequences. We avoided additional endovascular manipulations during the procedures and this could be one of the main reasons for the low incidence of complications in this study. Although most of the patients had low H&H grades at presentation, follow-up mRS values showed very good functional recovery.

Outcomes in Patients with Very Large Aneurysms

Although the patients in this group had higher H&H grades at presentation and a higher mean age, the results were disappointing in comparison to the very small aneurysm group.

In this series, the results included 3 MCA vasospasms as immediate complications (one of which resulted in death of the patient 72 h later) and 5 cases of recanalization in long-term follow-up. According to our experience, although coiling of very small ruptured aneurysms is technically challenging, it has better long-term outcomes compared with coiling of very large ruptured aneurysms.

Although complete coiling was accomplished without immediate angiographic remnants of the aneurysm in the majority of cases, the recanalization rate was higher in very large aneurysms that were treated in comparison to very small aneurysms. It should also be mentioned that, in the very large aneurysm group, there was a longer follow-up period. It could be partly because we did not use neck-remodeling techniques.

The limitations of our study were that we studied only a small number of cases and were reporting on a single center. Additional prospective studies are warranted. The limited number of the reported cases was due to the novelty of endovascular intervention for regional clinicians and patients. Furthermore, the procedure costs were expensive and unaffordable for most patients. Another limitation is the lack of a surgically clipped aneurysm group.

According to different reports, endovascular treatment of very small (≤3 mm) ruptured aneurysms is associated with a higher risk of complications, especially IPR and consequent rebleeding [10,11,12]. This can be due to the lack of microcatheter insertion space and structural limitations of current microcatheters and coils for coiling of very small aneurysms [6]. Ioannidis et al. [13] reported a high frequency of IPR in coiling of very small aneurysms. However, thromboembolism and recanalization had a lower incidence rate in comparison with large coiled aneurysms. Very small aneurysms have a 5 times higher risk for procedure-related ruptures [14]. Nevertheless, in the case of successful coiling and complete occlusion, the recanalization occurrence is lower for very small aneurysms compared with very large aneurysms, which is in accordance with the results of our study [7,15]. Ruptured aneurysms also had an elevated possibility for intraprocedural complications, of which the most devastating is intraprocedural rerupture [16,17]. The small size of the aneurysm, atherosclerosis, a higher Fisher grade of SAH and cerebral vasospasm have been reported as predisposing factors for IPR [18]. In contrast, Chae et al. [19] suggested endovascular coiling of very small aneurysms as an acceptable method with good initial angiographic outcomes, without any procedural morbidity and mortality. Lum et al. [20] confirmed this statement in their findings, reporting no significant increment in the IPR rate in very small aneurysms. Our results on the very small aneurysm group were in accordance with these findings.

Hwang et al. [21] reported endovascular treatment of 43 very small aneurysms (23 ruptured, 20 unruptured) in 38 patients. There were 5 incidents of thrombosis (12%) and 1 procedural rupture (2%), but there was no definite adverse effect on clinical outcomes. Of 24 patients with SAH, 10 patients (42%) were in poor condition (H&H 3 or H&H 4) on admission. Seventy-one percent of the patients had a good or excellent outcome at discharge. A 6-month or more follow-up angiography and/or MRA revealed minor recanalization in 2 (6%) and major recanalization in 1 (3%).

Suzuki et al. [4] reported 115 MCA, 48 of which were ruptured aneurysms. They reported that endovascular treatment of MCA aneurysms that had less favorable outcomes compared to aneurysms located in other parts of the anterior circulation may be due to technical challenges, such as poor visualization of the location of the aneurysms in MCA bifurcation and fusion of an MCA branch to the neck or body of the aneurysm. Pierot et al. [22] reported a higher frequency of IPR in MCA aneurysms, patients younger than 65 years and hypertensive cases. Most of the very large aneurysms in our study were located in the MCA bifurcation and this could partly explain the more frequent complications in this group. Another interesting finding was complications in the very small aneurysm group (thromboembolism and recanalization), which occurred in the patients with aneurysms in the MCA bifurcation (fig. 1).

Suzuki et al. [4] published their findings on endovascular coiling of MCA aneurysms describing different morphological data but they did not report immediate and long-term complications in very small, very large and also ruptured and unruptured aneurysms separately.

There is a paucity of reports on coiling outcomes for very large aneurysms. In addition, we could not find other studies in the literature that compared the immediate and long-term complications of endovascular treatment of very small and very large ruptured aneurysms as two isolated groups. Our study is unique in this regard.

In conclusion, endovascular treatment of very small aneurysms is a practical method for treatment, with acceptable immediate and long-term outcomes in comparison to very large aneurysms. Long-term complications were more prevalent with very large aneurysms. For more awareness and risk calculation, and attentive selection of the patients, further studies are needed.

Disclosure Statement

We declare that we have no conflicts of interest.


References

  1. Sandvei MS, Romundstad PR, Müller TB, Vatten L, Vik A: Risk factors for aneurysmal subarachnoid hemorrhage in a prospective population study: the HUNT study in Norway. Stroke 2009;40:1958-1962.
  2. Schuette AJ, Hui FK, Spiotta AM, Obuchow-ski NA, Gupta R, Moskowitz SI, Tong FC, Dion JE, Cawley CM: Endovascular therapy of very small aneurysms of the anterior communicating artery: five-fold increased incidence of rupture. Neurosurgery 2011;68:731-717.
  3. Bederson JB, Connolly ES Jr, Batjer HH, Da-cey RG, Dion JE, Diringer MN, Duldner JE Jr, Harbaugh RE, Patel AB, Rosenwasser RH, American Heart Association: Guidelines for the management of aneurysmal subarachnoid hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke 2009;40:994-1025.
  4. Suzuki S, Tateshima S, Jahan R, Duckwiler GR, Murayama Y, Gonzalez NR, Viñuela F: Endovascular treatment of middle cerebral artery aneurysms with detachable coils: an-giographic and clinical outcomes in 115 consecutive patients. Neurosurgery 2009;64:876-888.
  5. Renowden SA, Benes V, Bradley M, Molyneux AJ: Detachable coil embolisation of ruptured intracranial aneurysms: a single center study, a decade experience. Clin Neurol Neurosurg 2009;111:179-188.
  6. Lim YC, Kim BM, Shin YS, Kim SY, Chung J: Structural limitations of currently available microcatheters and coils for endovascular coiling of very small aneurysms. Neuroradiology 2008;50:423-427.
  7. Nguyen TN, Hoh BL, Amin-Hanjani S, Pryor JC, Ogilvy CS: Comparison of ruptured vs unruptured aneurysms in recanalization after coil embolization. Surg Neurol 2007;68:19-23.
  8. Brinjikji W, Lanzino G, Cloft HJ, Rabinstein A, Kallmes DF: Endovascular treatment of very small (3 mm or smaller) intracranial aneurysms: report of a consecutive series and a meta-analysis. Stroke 2010;41:116-121.
  9. Suzuki S, Kurata A, Ohmomo T, Sagiuchi T, Niki J, Yamada M, et al: Endovascular surgery for very small ruptured intracranial aneurysms. Technical note. J Neurosurg 2006;105:777-780.
  10. Akiyama Y, Houkin K, Nozaki K, Hashimoto N: Practical decision-making in the treatment of unruptured cerebral aneurysm in Japan: the U-CARE study. Cerebrovasc Dis 2010;30:491-499.
  11. Sharma DP, Singh D, Jagetia A, Singh H, Tandon M, Ganjoo P: Intra procedure rupture of intracranial aneurysm during endovascular coiling: neurosurgeons' experience and review of the literature. Neurol India 2011;59:690-695.
  12. Iskandar A, Nepper-Rasmussen J: Endovascular treatment of very small intracranial aneurysms. Interv Neuroradiol 2011;17:299-305.
  13. Ioannidis I, Lalloo S, Corkill R, Kuker W, Byrne JV: Endovascular treatment of very small intracranial aneurysms. J Neurosurg 2010;112:551-556.
  14. Nguyen TN, Raymond J, Guilbert F, Roy D, Bérubé MD, Mahmoud M, Weill A: Association of endovascular therapy of very small ruptured aneurysms with higher rates of procedure-related rupture. J Neurosurg 2008;108:1088-1092.
  15. Vanninen R, Koivisto T, Saari T, Hernesniemi J, Vapalahti M: Ruptured intracranial aneurysms: acute endovascular treatment with electrolytically detachable coils - a prospective randomized study. Radiology 1999;211:325-336.
  16. van der Kolk NM, Algra A, Rinkel GJ: Risk of aneurysm rupture at intracranial arterial bifurcations. Cerebrovasc Dis 2010;30:29-35.
  17. van Rooij WJ, Keeren GJ, Peluso JP, Sluzewski M: Clinical and angiographic results of coiling of 196 very small (< or = 3 mm) intracranial aneurysms. Am J Neuroradiol 2009;30:835-839.
  18. Zhang X, Long XA, Luo B, Karuna T, Duan CZ: Factors responsible for poor outcome after intraprocedural rerupture of ruptured intracranial aneurysms: identification of risk factors, prevention and management on 18 cases. Eur J Radiol 2012;81:e77-e85.
  19. Chae KS, Jeon P, Kim KH, Kim ST, Kim HJ, Byun HS: Endovascular coil embolization of very small intracranial aneurysms. Korean J Radiol 2010;11:536-541.
  20. Lum C, Narayanam SB, Silva L, Shankar J, Bussiere M, Dos Santos MP, Lesiuk H: Outcome in small aneurysms (<4 mm) treated by endovascular coiling. J Neurointerv Surg 2012;4:196-198.
  21. Hwang JH, Roh HG, Chun YI, Kang HS, Choi JW, Moon WJ, Cho J, Moon CT, Koh YC: Endovascular coil embolization of very small intracranial aneurysms. Neuroradiology 2011;53:349-357.
  22. Pierot L, Cognard C, Anxionnat R, Ricolfi F, CLARITY Investigators: Ruptured intracranial aneurysms: factors affecting the rate and outcome of endovascular treatment complications in a series of 782 patients (CLARITY study). Radiology 2010;256:916-923.

Author Contacts

Reza Mohammadian

Neuroscience Research Center

Tabriz University of Medical Sciences

PO Box 51665-348, Tabriz (Iran)

E-Mail diako30@yahoo.com


Article / Publication Details

First-Page Preview
Abstract of Original Paper

Received: 10/25/2012 2:06:51 PM
Accepted: 1/9/2013
Published online: 3/19/2013
Issue release date: April 2013

Number of Print Pages: 6
Number of Figures: 3
Number of Tables: 2

ISSN: 1015-9770 (Print)
eISSN: 1421-9786 (Online)

For additional information: http://www.karger.com/CED


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References

  1. Sandvei MS, Romundstad PR, Müller TB, Vatten L, Vik A: Risk factors for aneurysmal subarachnoid hemorrhage in a prospective population study: the HUNT study in Norway. Stroke 2009;40:1958-1962.
  2. Schuette AJ, Hui FK, Spiotta AM, Obuchow-ski NA, Gupta R, Moskowitz SI, Tong FC, Dion JE, Cawley CM: Endovascular therapy of very small aneurysms of the anterior communicating artery: five-fold increased incidence of rupture. Neurosurgery 2011;68:731-717.
  3. Bederson JB, Connolly ES Jr, Batjer HH, Da-cey RG, Dion JE, Diringer MN, Duldner JE Jr, Harbaugh RE, Patel AB, Rosenwasser RH, American Heart Association: Guidelines for the management of aneurysmal subarachnoid hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke 2009;40:994-1025.
  4. Suzuki S, Tateshima S, Jahan R, Duckwiler GR, Murayama Y, Gonzalez NR, Viñuela F: Endovascular treatment of middle cerebral artery aneurysms with detachable coils: an-giographic and clinical outcomes in 115 consecutive patients. Neurosurgery 2009;64:876-888.
  5. Renowden SA, Benes V, Bradley M, Molyneux AJ: Detachable coil embolisation of ruptured intracranial aneurysms: a single center study, a decade experience. Clin Neurol Neurosurg 2009;111:179-188.
  6. Lim YC, Kim BM, Shin YS, Kim SY, Chung J: Structural limitations of currently available microcatheters and coils for endovascular coiling of very small aneurysms. Neuroradiology 2008;50:423-427.
  7. Nguyen TN, Hoh BL, Amin-Hanjani S, Pryor JC, Ogilvy CS: Comparison of ruptured vs unruptured aneurysms in recanalization after coil embolization. Surg Neurol 2007;68:19-23.
  8. Brinjikji W, Lanzino G, Cloft HJ, Rabinstein A, Kallmes DF: Endovascular treatment of very small (3 mm or smaller) intracranial aneurysms: report of a consecutive series and a meta-analysis. Stroke 2010;41:116-121.
  9. Suzuki S, Kurata A, Ohmomo T, Sagiuchi T, Niki J, Yamada M, et al: Endovascular surgery for very small ruptured intracranial aneurysms. Technical note. J Neurosurg 2006;105:777-780.
  10. Akiyama Y, Houkin K, Nozaki K, Hashimoto N: Practical decision-making in the treatment of unruptured cerebral aneurysm in Japan: the U-CARE study. Cerebrovasc Dis 2010;30:491-499.
  11. Sharma DP, Singh D, Jagetia A, Singh H, Tandon M, Ganjoo P: Intra procedure rupture of intracranial aneurysm during endovascular coiling: neurosurgeons' experience and review of the literature. Neurol India 2011;59:690-695.
  12. Iskandar A, Nepper-Rasmussen J: Endovascular treatment of very small intracranial aneurysms. Interv Neuroradiol 2011;17:299-305.
  13. Ioannidis I, Lalloo S, Corkill R, Kuker W, Byrne JV: Endovascular treatment of very small intracranial aneurysms. J Neurosurg 2010;112:551-556.
  14. Nguyen TN, Raymond J, Guilbert F, Roy D, Bérubé MD, Mahmoud M, Weill A: Association of endovascular therapy of very small ruptured aneurysms with higher rates of procedure-related rupture. J Neurosurg 2008;108:1088-1092.
  15. Vanninen R, Koivisto T, Saari T, Hernesniemi J, Vapalahti M: Ruptured intracranial aneurysms: acute endovascular treatment with electrolytically detachable coils - a prospective randomized study. Radiology 1999;211:325-336.
  16. van der Kolk NM, Algra A, Rinkel GJ: Risk of aneurysm rupture at intracranial arterial bifurcations. Cerebrovasc Dis 2010;30:29-35.
  17. van Rooij WJ, Keeren GJ, Peluso JP, Sluzewski M: Clinical and angiographic results of coiling of 196 very small (< or = 3 mm) intracranial aneurysms. Am J Neuroradiol 2009;30:835-839.
  18. Zhang X, Long XA, Luo B, Karuna T, Duan CZ: Factors responsible for poor outcome after intraprocedural rerupture of ruptured intracranial aneurysms: identification of risk factors, prevention and management on 18 cases. Eur J Radiol 2012;81:e77-e85.
  19. Chae KS, Jeon P, Kim KH, Kim ST, Kim HJ, Byun HS: Endovascular coil embolization of very small intracranial aneurysms. Korean J Radiol 2010;11:536-541.
  20. Lum C, Narayanam SB, Silva L, Shankar J, Bussiere M, Dos Santos MP, Lesiuk H: Outcome in small aneurysms (<4 mm) treated by endovascular coiling. J Neurointerv Surg 2012;4:196-198.
  21. Hwang JH, Roh HG, Chun YI, Kang HS, Choi JW, Moon WJ, Cho J, Moon CT, Koh YC: Endovascular coil embolization of very small intracranial aneurysms. Neuroradiology 2011;53:349-357.
  22. Pierot L, Cognard C, Anxionnat R, Ricolfi F, CLARITY Investigators: Ruptured intracranial aneurysms: factors affecting the rate and outcome of endovascular treatment complications in a series of 782 patients (CLARITY study). Radiology 2010;256:916-923.