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Therapeutic strategies for residual or recurrent intracranial aneurysms after microsurgical clipping
Clinical Neurology and Neurosurgery 173 (2018) 110–114
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Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Therapeutic strategies for residual or recurrent intracranial aneurysms after microsurgical clipping
T
Jung Hoon Kima, Joonho Chunga,c, Seung Kon Huha, Keun Young Parka, Dong Joon Kimb, ⁎ Byung Moon Kimb, Jae Whan Leea, a
Department of Neurosurgery, Severance Stroke Center, Severance Hospital, Yonsei University of College of Medicine, Seoul, Republic of Korea Department of Radiology, Severance Stroke Center, Severance Hospital, Yonsei University of College of Medicine, Seoul, Republic of Korea c Severance Institute for Vascular and Metabolic Research, Yonsei University of College of Medicine, Seoul, Republic of Korea b
A R T I C LE I N FO
A B S T R A C T
Keywords: Endovascular treatment Intracranial aneurysm Microsurgery Residual aneurysm Recurrent aneurysm
Objectives: Therapeutic strategies for residual or recurrent aneurysm (RRA) after microsurgical clipping have not been well established. The purpose of this study was to report our retreatment experiences with previously clipped aneurysms and to demonstrate retreatment strategies for these RRAs. Patients and Methods: From 1996–2016, we treated 68 RRAs after previous clipping. Among them, 34 patients underwent microsurgical retreatment, and the other 34 underwent endovascular retreatment. Radiographic images and clinical data were reviewed retrospectively to determine the treatment efficacy, clinical outcomes, and important factors for selecting the proper treatment modality. Results: The most common aneurysm location was the middle cerebral artery (50%) in the microsurgery group and the internal carotid artery (47.1%) in the endovascular surgery group (p = 0.001). In the microsurgery group, 16 (47.1%) patients had additional clipping without removal of previous clips, 17 (50.0%) had clipping with removal of previous clips, and 1 (2.9%) had bypass surgery with trapping. In the endovascular surgery group, 28 (82.4%) patients had simple coiling, 5 (14.7%) had stent-assisted coiling, and 1 (2.9%) had a flow diverter. Procedure-related complications during retreatment occurred in 4 (5.9%) patients. Complete obliteration was achieved in 51 (75.0%) patients (microsurgery group, 82.4% and endovascular surgery group, 67.6%; p = 0.002). Conclusions: In properly selected cases, treatment of RRAs could be safely performed either by microsurgery or endovascular surgery and result in a good clinical outcome with acceptable morbidity. The decision to choose the treatment modality for RRAs after clipping is not easy but should be considered to lower the risk of retreatment.
1. Introduction Durability of treatment is a major concern in choosing the proper treatment modality for intracranial aneurysms. Generally, microsurgical clipping is believed to provide definitive and long-term treatment of intracranial aneurysms [1]. However, residual and recurrent intracranial aneurysms (RRAs) can occur after treatment, and RRAs after microsurgical clipping are challenging for neurosurgeons to retreat. Several studies have reported that the RRA incidence after clipping was 5%–8% and that RRAs had a risk of bleeding and growing [2–4]. RRAs after clipping can be treated by microsurgery or endovascular treatment [5–9]. One study reported that surgical treatment
was safe and efficient for securing RRAs [6]. Another reported that endovascular treatment was safe as the first line treatment for RRAs [5]. However, retreating RRAs after clipping presents some technical difficulties. The previous clips can obscure an RRA in the operating field and make applying new clips difficult. Arachnoid adhesions caused by the previous operation delay the approach to the RRA and prevent the exposure of normal anatomy, inducing premature RRA rupture, parent artery injury, and brain injury. Though several studies have reported on RRA treatment after clipping, therapeutic strategies for those aneurysms have not been well established. Thus, the purpose of this study was to report our retreatment experience with previously clipped aneurysms and to demonstrate retreatment strategies for these RRAs.
⁎ Corresponding author at: Department of Neurosurgery, Severance Stroke Center, Severance Hospital, Yonsei University College of Medicine, 50-1, Yonsei-ro, Seodaemun-gu, Seoul, 03722, Republic of Korea. E-mail address: [email protected] (J.W. Lee).
https://doi.org/10.1016/j.clineuro.2018.08.011 Received 27 June 2018; Received in revised form 3 August 2018; Accepted 5 August 2018 Available online 06 August 2018 0303-8467/ © 2018 Elsevier B.V. All rights reserved.
Clinical Neurology and Neurosurgery 173 (2018) 110–114
J.H. Kim et al.
2. Materials and methods
15 (21.4%), and giant in 3 (4.3%). The RRAs were in the internal carotid artery (ICA) in 20 (29.4%) patients, anterior cerebral artery (ACA) in 21 (30.9%), middle cerebral artery (MCA) in 21 (30.9%), and vertebrobasilar artery-posterior cerebral artery (VB-PCA) in 6 (8.8%). The most common aneurysm location was the MCA (50%) in the microsurgery group and the ICA (47.1%) in the endovascular surgery group, which showed statistical significance (p = 0.001). Procedure-related complications during retreatment occurred in 4 (5.9%) patients: two (2.9%) experienced parent artery injury during microsurgery, one (1.5%) experienced thromboembolic infarction during endovascular surgery, and one (1.5%) experienced postoperative frontal contusion during microsurgery (Table 2). The rate of procedure-related complications did not differ between microsurgery (8.8%) and endovascular surgery (2.9%; p = 0.609). RRAs were completely obliterated in 51 (75.0%) patients, 13 (19.1%) had a neck remnant, and 4 (5.9%) were incomplete. The microsurgery group (82.4%) had more patients with complete obliteration than did to the endovascular surgery group (67.6%, p = 0.002). Fiftyone (75.0%) patients had favorable clinical outcomes at discharge, 14 (20.6%) had unfavorable outcomes, and 3 (4.4%) died. All 3 deaths were caused by brain injury due to rebleeding on admission for retreatment. Clinical outcomes at discharge did not differ between groups (p = 0.584). Our treatment strategies for RRAs are listed in Table 3. In the microsurgery group, 16 (47.1%) patients had additional clipping without removal of previous clips, 17 (50.0%) had clipping with removal of previous clips, and 1 (2.9%) had bypass surgery with trapping. In the endovascular surgery group, 28 (82.4%) patients had simple coiling, 5 (14.7%) had stent-assisted coiling, and 1 (2.9%) had a flow diverter in.
This retrospective study was approved by our institutional review board, and informed consent was waived. All patients who had cerebral aneurysms and underwent microsurgical clipping at our institution were retrospectively reviewed. Between 1996 and 2016, 6036 aneurysms were treated with either microsurgery or endovascular treatment. We treated ruptured aneurysms. And, treatment criteria of unruptured intracranial aneurysms were (1) patients with symptoms, (2) patients below 60 years of age, (3) with aneurysms larger than 5 mm, (4) with a daughter sac, (5) with prior subarachnoid hemorrhage (SAH) or family history, or (6) change of shape during the follow-up period. For the first treatment, treatment modality was selected based on characteristics of individual patients and intracranial aneurysms through interdisciplinary decision making, offering microsurgery as a primary treatment. The patients’ preferences for treatment were also considered. Two microvascular neurosurgeons and two endovascular neurosurgeons decided the treatment strategy, initial treatment plan, and retreatment plan in all cases. An RRA was defined as an aneurysm previously treated by microsurgical clipping with a remnant, regrowth, or rebleeding during the follow-up period. In the present study, 68 patients with previously clipped RRAs undergone retreatment were included. Our indications for the retreatment of RRAs are as follows: (1) rebleeding, 2) symptomatic RRAs, 3) regrowth of the aneurysms during the follow-up period, or 4) residual sacs due to incomplete or partial clipping. Retreatment was performed when the length of the residual sacs of the aneurysm neck represented enough space (more than 1.5 mm) for the placement of clips or coils. Forty-nine patients had previous clipping at our institution and 19 at other hospitals. Forty-seven (69.1%) patients were female and 21 (30.9%) male with a mean age of 49.3 ± 11.2 years at the time of retreatment. Thirty-four patients underwent microsurgery, and the other 34 patients underwent endovascular surgery for RRA. Radiographic images and clinical data were retrospectively reviewed to determine the treatment efficacy, clinical outcome, and important factors for selecting the treatment modality. Aneurysm size was classified as small (< 10 mm), large (10–24 mm), or giant (≥25 mm). Completeness of retreatment was confirmed by digital subtraction angiography (DSA) or CT angiography (CTA). Clinical outcomes (Glasgow Outcome Scale, GOS) were determined independently by a neurovascular nurse practitioner and two neurosurgeons. A favorable outcome was defined as a GOS of 4 or 5 (moderate disability or better), and an unfavorable outcome was defined as a GOS of 2 or 3 (severe disability or vegetative state). A GOS of 1 indicates death. Thirty-nine patients had a postoperative DSA, and all had a CTA.
3.1. Representative cases 3.1.1. Clipping with removal of previous clips A 34-year-old woman came to our hospital owing to a left upper extremity paresis and dysarthria. On her MRI, acute infarction was on the right basal ganglia and a giant thrombosed aneurysm was on the right middle cerebral artery bifurcation. The aneurysm was treated by microsurgical clipping and complete obliteration was achieved and confirmed by postoperative 3D digital subtraction angiography (DSA). After 7 years from the clipping, regrowth of the aneurysm was found on her follow-up 3D DSA (Fig. 1a). The recurred aneurysm had a triangular shape and was recurred from the neck portion. It could not be clipped completely without removing three old clips (Fig. 1b). We removed old clips carefully and performed re-clipping (Fig. 1c). Complete obliteration was achieved and confirmed by postoperative 3D DSA (Fig. 1d). 3.1.2. Simple coiling A 41-year-old man came to our hospital with an asymptomatic giant aneurysm on the left P1-2 junction. The aneurysm was treated by microsurgical clipping using the orbito-pterional approach. While we were removing intra-aneurysmal thrombus to expose the aneurysm neck, massive bleeding from the aneurysm was encountered. We decided to stop the bleeding with partial clipping of the aneurysm and perform endovascular treatment for the residual aneurysm. The residual aneurysm, sized about 2.25 × 1.10 mm, was confirmed on the immediate postoperative 3D DSA (Fig. 2a). Coil embolization without using stents was performed and achieved near complete obliteration of the aneurysm (Fig. 2b).
2.1. Statistical analysis Statistical analysis was performed with SPSS 20.0 (IBM software). Baseline characteristics and clinical outcomes were compared between the microsurgery and endovascular surgery groups with the MannWhitney U test or Student’s t-test for continuous variables and the Chisquare test or Fisher exact test for categorical variables. A p-value of less than 0.05 was considered statistically significant. 3. Results Clinical data and patient outcomes are summarized in Table 1. On admission for initial treatment, 58 (85.3%) patients presented with aneurysmal subarachnoid hemorrhage (aSAH). Retreatment was required for rebleeding in 31 (45.6%) patients, regrowth in 20 (29.4%), and remnant in 17 (25.0%). The median interval from the initial clipping until retreatment was 4.9 years (range, 0–20). Patient factors did not differ significantly between the microsurgery and endovascular surgery groups. Aneurysms were small in 52 (74.3%) patients, large in
4. Discussion Because the incidence of RRAs after microsurgical clipping has been estimated at 5%–8% [2–4], retreatment of these lesions must be discussed individually. RRAs carry a risk of bleeding and growing. The annual hemorrhage risk of RRAs was about 1.9% in dog-ear remnants [3]. The growth rates of dog-ear remnants and broad neck remnants 111
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Table 1 Clinical data and outcomes.
Age at initial treatment (years, mean ± SD) Female, n (%) aSAH as initial presentation, n (%) Cause of retreatment, n (%) Rebleeding Regrowth Remnant
Total (n = 68)
Microsurgery (n = 34)
Endovascular Surgery (n = 34)
p-value
49.3 ± 11.2 47 (69.1) 58 (85.3)
47.9 ± 11.7 21 (61.8) 30 (88.2)
50.7 ± 10.6 26 (76.5) 28 (82.4)
0.306 0.300 0.493 0.471
31 (45.6) 20 (29.4) 17 (25.0)
14 (41.2) 13 (38.2) 7 (20.6)
17 (50.0) 7 (20.6) 10 (29.4)
Median interval (years) Aneurysm size, n (%) Small Large Giant
4.9 (range, 0-20)
6.3 (range, 0-17)
2.3 (range, 0-20)
50 (73.5) 15 (22.1) 3 (4.4)
28 (82.3) 4 (11.8) 2 (5.9)
22 (64.7) 11 (32.4) 1 (2.9)
Aneurysm Location, n (%) ICA ACA MCA VB-PCA
20 (29.4) 21 (30.9) 21 (30.9) 6 (8.8)
4 (11.8) 11 (32.4) 17 (50.0) 2 (5.9)
16 (47.1) 10 (29.4) 4 (11.8) 4 (11.8)
Procedure-related complication, n (%) Parent artery injury Thromboembolic infarction Post-operative hemorrhage
4 2 1 1
3 2 0 1
1 0 1 0
Radiographic outcomes, n (%) Complete Near complete or neck remnant Incomplete
51 (75.0) 13 (19.1) 4 (5.9)
28 (82.4) 6 (17.6) 0 (0)
23 (67.6) 7 (20.6) 4 (11.8)
Clinical outcomes at discharge, n (%) Favorable (GOS 4 or 5) Unfavorable (GOS 2 or 3) Death (GOS 1)
51 (75.0) 14 (20.6) 3 (4.4)
27 (79.4) 6 (17.6) 1 (2.9)
24 (70.6) 8 (23.5) 2 (5.9)
0.244 0.188
0.001
(5.9) (2.9) (1.5) (1.5)
(8.8) (5.9) (0) (2.9)
(2.9) (0) (2.9) (0)
0.609
0.002
0.584
ACA = anterior cerebral artery; aSAH = aneurysmal subarachnoid hemorrhage; GOS = Glasgow Outcome Scale; ICA = internal carotid artery; MCA = middle cerebral artery; SD = standard deviation; VB-PCA = vertebrobasilar artery-posterior cerebral artery. Table 2 List of patients who experienced procedure-related complications. Case
Age (years)
Retreatment modality
Initial presentation
Interval (years)
Aneurysm location
Aneurysm size (mm)
Complications
Outcome (GOS)
22
38
SAH
11
ACOM
8
Frontal lobe contusion
3
28
69
SAH
10
MCBIF
3
Parent artery stenosis
2
32
46
SAH
15
ACOM
16
50
SAH
2
BABIF
6
Cerebral infarction due to parent artery injury Embolic infarction of brainstem
3
55
Clipping without removal of previous clips Clipping with removal of previous clips Clipping with removal of previous clips Simple coiling
3
ACOM = anterior communicating artery; BABIF = basilar artery bifurcation; GOS = Glasgow Coma Scale; MCBIF = middle cerebral artery bifurcation; SAH = subarachnoid hemorrhage.
RRAs should be considered for treatment. According to our experience, 68 (1.4%) of the 4818 patients who had microsurgical clipping underwent retreatment of an RRA by microsurgery and endovascular surgery. Microsurgery consisted of additional clipping with or without removal of previous clips or bypass surgery with trapping. Endovascular surgery consisted of simple coiling, stent-assisted coiling, or a flow diverter. As each patient has different demographic and aneurysm characteristics, developing a standard indication for treating RRAs is difficult. Therefore, a team approach is important in deciding which option is best to completely obliterate an RRA. In the event microsurgical and endovascular techniques were likely to have similar possibility of completely obliterating RRAs, we assessed the durability of treatment and risks associated with each procedure. Microsurgical clipping has been generally accepted as more durable than coil embolization. In ISAT, the risk of aneurysm recanalization after endovascular occlusion was associated with recurrent hemorrhage, although that risk was
Table 3 Treatment strategies for residual or recurrent aneurysms. Microsurgery, n (%)
N = 34
Clipping without removal of previous clips Clipping with removal of previous clips Bypass surgery with trapping Endovascular surgery, n (%) Simple coiling Stent-assisted coiling Flow diverter
16 (47.1) 17 (50.0) 1 (2.9) N = 34 28 (82.4) 5 (14.7) 1 (2.9)
were reported as 25% and 75%, respectively [3]. In ruptured aneurysms that had been clipped, the cumulative risk of aSAH recurrence was 0.5%, 2.2%, 5.5%, and 9.0% at 5, 10, 15, and 20 years, respectively [10]. In unruptured aneurysms, the cumulative risk of developing aSAH was 1.4% at 10 years and 12.4% at 20 years [11]. To avoid these risks,
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Fig. 1. A 34-year-old woman underwent microsurgical clipping due to a giant thrombosed aneurysm on the right middle cerebral artery bifurcation. After 7 years from the first operation, (a) regrowth of the aneurysm was found on her follow-up 3D digital subtraction angiography (DSA). (b) The recurred aneurysm had a triangular shape and was recurred from the neck portion. It could not be clipped completely without removing three old clips. (c) Old clips were removed and the aneurysm was re-clipped. (d) Complete oblitreation was achieved and confirmed by postoperative 3D DSA.
technical difficulties for microsurgery, including bypass surgery. Parent artery injury can cause severe morbidity or mortality. In such cases, with the development of assisted devices, endovascular surgery has been considered technically easier and safer. Therefore, we preferred endovascular surgery for RRAs in the ICA or VB-PCA.
small, with 10 episodes in 1073 patients after 1 year [12,13]. In addition, because of its long-term durability, clipping has an advantage over coiling especially in patients < 40 years old [14]. And in BRAT, which is ongoing, they show high recurrent rate (16.4%) and low complete obliteration rate (48%) in coiling patients so far [15]. Therefore, we prefer surgical treatment, especially in patients with a long-life expectancy. We also considered the risk of each procedure. In the present study, we performed bypass surgery for the retreatment in one patient. We have tried to perform endovascular treatment if bypass surgery was expected for the retreatment. If stents were expected for the retreatment, we have tried to perform microsurgery. If both bypass surgery and stent insertion were expected for the retreatment, risky, we prefer endovascular treatment. Aneurysm locations could affect the decision on treatment modality for RRAs. MCA aneurysms are easy to approach surgically and most had a wide neck [16]. Thus, microsurgical techniques were selected for many RRAs in the MCA. RRAs in the ICA or VB-PCA pose possible
4.1. Retreatment with microsurgery Microsurgical treatment of RRAs previously treated by surgical clipping can be dangerous. Because of the previous clips and tissue adhesions, dissection of the subarachnoid space and around the previous clip is not easy. This situation can result in injury of parent artery and micro surgically resect brain parenchyma. Due to adhesions, proximal control can be difficult. Thus, once we decided on microsurgical treatment for an RRA, we considered and prepared for bypass surgery depending on the lesion and for carotid artery preparation for proximal control with/without suction decompression in RRAs in the Fig. 2. A 41-year-old man with a giant aneurysm on the left P1-2 junction underwent microsurgical clipping While we were removing intra-aneurysmal thrombus to expose the aneurysm neck, massive bleeding from the aneurysm was encountered. We decided to stop the bleeding with partial clipping of the aneurysm and performed endovascular treatment for the residual aneurysm. (a) The residual aneurysm, sized about 2.25 × 1.10 mm, was confirmed on the immediate postoperative 3D digital subtraction angiography. (b) Coil embolization without using stents was performed and achieved near complete obliteration of the aneurysm.
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ICA. Previous clips do not always need to be removed according to our experience. Removing old clips has been reported to be necessary for a wide operation field and complete RRA obliteration [17,18]. However, removing old clips is dangerous [19]. In the present study, we felt that the need to remove old clips could not be predicted before exposing the operation field. We confirmed the anatomical relationship of the old clip in the operation field and then decided whether remove it. If the old clip was disturbing complete obliteration of the RRA and no other options such as a fenestration clip were available, we removed the old clip along the line of the clip blade. Because our retreatment goal was complete obliteration, removing previous clips was not mandatory. If complete obliteration is needed, previous clips should be removed with caution. If additional surgical space is needed, we suck out the brain parenchyma in a non-eloquent area.
Acknowledgment None. References [1] Rates of delayed rebleeding from intracranial aneurysms are low after surgical and endovascular treatment, Stroke 37(6) (2006) 1437-42. [2] C.A. David, A.G. Vishteh, R.F. Spetzler, M. Lemole, M.T. Lawton, S. Partovi, Late angiographic follow-up review of surgically treated aneurysms, J. Neurosurg. 91 (3) (1999) 396–401. [3] J. Kivelev, R. Tanikawa, K. Noda, J. Hernesniemi, M. Niemela, K. Takizawa, T. Tsuboi, N. Ohta, S. Miyata, J. Oda, S. Tokuda, H. Kamiyama, Open surgery for recurrent intracranial aneurysms: techniques and long-term outcomes, World Neurosurg. 96 (2016) 1–9. [4] M. Sindou, J.C. Acevedo, F. Turjman, Aneurysmal remnants after microsurgical clipping: classification and results from a prospective angiographic study (in a consecutive series of 305 operated intracranial aneurysms), Acta Neurochir. (Wien) 140 (11) (1998) 1153–1159. [5] N. Chalouhi, R. Chitale, R.M. Starke, P. Jabbour, S. Tjoumakaris, A.S. Dumont, R.H. Rosenwasser, L.F. Gonzalez, Treatment of recurrent intracranial aneurysms with the Pipeline Embolization Device, J. Neurointerv. Surg. 6 (1) (2014) 19–23. [6] M. el-Beltagy, C. Muroi, P. Roth, J. Fandino, H.G. Imhof, Y. Yonekawa, Recurrent intracranial aneurysms after successful neck clipping, World Neurosurg. 74 (4-5) (2010) 472–477. [7] B.L. Hoh, B.S. Carter, C.M. Putman, C.S. Ogilvy, Important factors for a combined neurovascular team to consider in selecting a treatment modality for patients with previously clipped residual and recurrent intracranial aneurysms, Neurosurgery 52 (4) (2003) 732–738 discussion 738-9. [8] S. Mangiafico, M. Cellerini, G. Villa, F. Ammannati, L. Paoli, P. Mennonna, Endovascular coiling of aneurysm remnants after clipping in patients with followup. A single center experience, Interv. Neuroradiol. 11 (1) (2005) 41–48. [9] A.J. Molyneux, R.S. Kerr, J. Birks, N. Ramzi, J. Yarnold, M. Sneade, J. Rischmiller, Risk of recurrent subarachnoid haemorrhage, death, or dependence and standardised mortality ratios after clipping or coiling of an intracranial aneurysm in the International Subarachnoid Aneurysm Trial (ISAT): long-term follow-up, the Lancet, Neurology 8 (5) (2009) 427–433. [10] K. Tsutsumi, K. Ueki, M. Usui, S. Kwak, T. Kirino, Risk of recurrent subarachnoid hemorrhage after complete obliteration of cerebral aneurysms, Stroke 29 (12) (1998) 2511–2513. [11] K. Tsutsumi, K. Ueki, M. Usui, S. Kwak, T. Kirino, Risk of subarachnoid hemorrhage after surgical treatment of unruptured cerebral aneurysms, Stroke 30 (6) (1999) 1181–1184. [12] P. Mitchell, R. Kerr, A.D. Mendelow, A. Molyneux, Could late rebleeding overturn the superiority of cranial aneurysm coil embolization over clip ligation seen in the International Subarachnoid Aneurysm Trial? J. Neurosurg. 108 (3) (2008) 437–442. [13] A. Molyneux, R. Kerr, I. Stratton, P. Sandercock, M. Clarke, J. Shrimpton, R. Holman, International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial, Lancet 360 (9342) (2002) 1267–1274. [14] E. Guresir, P. Schuss, J. Berkefeld, H. Vatter, V. Seifert, Treatment results for complex middle cerebral artery aneurysms. A prospective single-center series, Acta Neurochir. (Wien) 153 (6) (2011) 1247–1252. [15] R.F. Spetzler, C.G. McDougall, J.M. Zabramski, F.C. Albuquerque, N.K. Hills, J.J. Russin, S. Partovi, P. Nakaji, R.C. Wallace, The barrow ruptured aneurysm trial: 6-year results, J. Neurosurg. 123 (3) (2015) 609–617. [16] M. Hokari, K. Kazumara, N. Nakayama, S. Ushikoshi, T. Sugiyama, K. Asaoka, K. Uchida, D. Shimbo, K. Itamoto, Y. Yokoyama, M. Isobe, T. Imai, T. Osanai, K. Houkin, Treatment of recurrent intracranial aneurysms after clipping: a report of 23 cases and a review of the literature, World Neurosurg. 92 (2016) 434–444. [17] H. Kashimura, K. Ogasawara, Y. Kubo, Y. Otawara, A. Ogawa, Microsurgical removal of previously placed aneurysm clips and application of new clips for recurrent cerebral aneurysms. Technical note, J. Neurosurg. 107 (4) (2007) 881–883. [18] T. Sakaki, T. Takeshima, M. Tominaga, H. Hashimoto, S. Kawaguchi, Recurrence of ICA-PCoA aneurysms after neck clipping, J. Neurosurg. 80 (1) (1994) 58–63. [19] R. Boet, W.S. Poon, S.C. Yu, The management of residual and recurrent intracranial aneurysms after previous endovascular or surgical treatment–a report of eighteen cases, Acta Neurochir. (Wien) 143 (11) (2001) 1093–1101. [20] J. Thornton, Q. Bashir, V.A. Aletich, G.M. Debrun, J.I. Ausman, F.T. Charbel, What percentage of surgically clipped intracranial aneurysms have residual necks? Neurosurgery 46 (6) (2000) 1294–1298 discussion 1298-300.
4.2. Retreatment with endovascular surgery Remarkable endovascular devices have been developed making endovascular surgery a safe and efficient tool to treat RRAs. Previous reports have also indicated successful RRA treatment with endovascular surgery [5,7,8]. But there are some difficulties when we perform endovascular treatment of RRAs. An old clip can hinder the vascular anatomy, induce artifacts, and the aneurysm morphology could be unfavorable for coil embolization. Because of these difficulties, as our result showed, endovascular retreatment had a higher rate of incomplete obliteration than did microsurgery. We overcame this problem with 3D rotational angiography to obtain precise anatomical images. We could understand the anatomical relation of the previous clips and parent vessels. Double-microcatheter, balloon-assisted, and stent-assisted techniques made the treatment safe and efficient, even when the RRA shape was not good for endovascular surgery. Recently, the flow diversion technique has been applied to treat intracranial aneurysms and RRAs [20]. However, studies on this treatment are limited. We only had one patient treated with a flow diverter, and that patient requires longer follow-up. 4.3. Retreatment outcomes We used the above strategies to treat RRAs. Of 34 surgically treated aneurysms, 33 were treated with clipping with or without removal of previous clips, and only one needed bypass surgery with trapping. Four RRAs (5.9%) had incomplete obliteration, all in the endovascular surgery group. Of these, 3 were treated a third time with endovascular surgery and achieved complete obliteration. The other patient is being observed. 5. Conclusion In properly selected cases, treatment of RRAs could be safely performed either by microsurgery or endovascular surgery and result in a good clinical outcome with acceptable morbidity. The decision to choose the treatment modality for RRAs after clipping is not easy but should be considered to lower the risk of retreatment. Thus, neurosurgeons should be aware of the risk of both retreatment modalities. Competing interests The authors declare that they have no competing interests. Funding This research did not receive any specific grant from funding
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Therapeutic strategies for residual or recurrent intracranial aneurysms after microsurgical clipping
T
Jung Hoon Kima, Joonho Chunga,c, Seung Kon Huha, Keun Young Parka, Dong Joon Kimb, ⁎ Byung Moon Kimb, Jae Whan Leea, a
Department of Neurosurgery, Severance Stroke Center, Severance Hospital, Yonsei University of College of Medicine, Seoul, Republic of Korea Department of Radiology, Severance Stroke Center, Severance Hospital, Yonsei University of College of Medicine, Seoul, Republic of Korea c Severance Institute for Vascular and Metabolic Research, Yonsei University of College of Medicine, Seoul, Republic of Korea b
A R T I C LE I N FO
A B S T R A C T
Keywords: Endovascular treatment Intracranial aneurysm Microsurgery Residual aneurysm Recurrent aneurysm
Objectives: Therapeutic strategies for residual or recurrent aneurysm (RRA) after microsurgical clipping have not been well established. The purpose of this study was to report our retreatment experiences with previously clipped aneurysms and to demonstrate retreatment strategies for these RRAs. Patients and Methods: From 1996–2016, we treated 68 RRAs after previous clipping. Among them, 34 patients underwent microsurgical retreatment, and the other 34 underwent endovascular retreatment. Radiographic images and clinical data were reviewed retrospectively to determine the treatment efficacy, clinical outcomes, and important factors for selecting the proper treatment modality. Results: The most common aneurysm location was the middle cerebral artery (50%) in the microsurgery group and the internal carotid artery (47.1%) in the endovascular surgery group (p = 0.001). In the microsurgery group, 16 (47.1%) patients had additional clipping without removal of previous clips, 17 (50.0%) had clipping with removal of previous clips, and 1 (2.9%) had bypass surgery with trapping. In the endovascular surgery group, 28 (82.4%) patients had simple coiling, 5 (14.7%) had stent-assisted coiling, and 1 (2.9%) had a flow diverter. Procedure-related complications during retreatment occurred in 4 (5.9%) patients. Complete obliteration was achieved in 51 (75.0%) patients (microsurgery group, 82.4% and endovascular surgery group, 67.6%; p = 0.002). Conclusions: In properly selected cases, treatment of RRAs could be safely performed either by microsurgery or endovascular surgery and result in a good clinical outcome with acceptable morbidity. The decision to choose the treatment modality for RRAs after clipping is not easy but should be considered to lower the risk of retreatment.
1. Introduction Durability of treatment is a major concern in choosing the proper treatment modality for intracranial aneurysms. Generally, microsurgical clipping is believed to provide definitive and long-term treatment of intracranial aneurysms [1]. However, residual and recurrent intracranial aneurysms (RRAs) can occur after treatment, and RRAs after microsurgical clipping are challenging for neurosurgeons to retreat. Several studies have reported that the RRA incidence after clipping was 5%–8% and that RRAs had a risk of bleeding and growing [2–4]. RRAs after clipping can be treated by microsurgery or endovascular treatment [5–9]. One study reported that surgical treatment
was safe and efficient for securing RRAs [6]. Another reported that endovascular treatment was safe as the first line treatment for RRAs [5]. However, retreating RRAs after clipping presents some technical difficulties. The previous clips can obscure an RRA in the operating field and make applying new clips difficult. Arachnoid adhesions caused by the previous operation delay the approach to the RRA and prevent the exposure of normal anatomy, inducing premature RRA rupture, parent artery injury, and brain injury. Though several studies have reported on RRA treatment after clipping, therapeutic strategies for those aneurysms have not been well established. Thus, the purpose of this study was to report our retreatment experience with previously clipped aneurysms and to demonstrate retreatment strategies for these RRAs.
⁎ Corresponding author at: Department of Neurosurgery, Severance Stroke Center, Severance Hospital, Yonsei University College of Medicine, 50-1, Yonsei-ro, Seodaemun-gu, Seoul, 03722, Republic of Korea. E-mail address: [email protected] (J.W. Lee).
https://doi.org/10.1016/j.clineuro.2018.08.011 Received 27 June 2018; Received in revised form 3 August 2018; Accepted 5 August 2018 Available online 06 August 2018 0303-8467/ © 2018 Elsevier B.V. All rights reserved.
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2. Materials and methods
15 (21.4%), and giant in 3 (4.3%). The RRAs were in the internal carotid artery (ICA) in 20 (29.4%) patients, anterior cerebral artery (ACA) in 21 (30.9%), middle cerebral artery (MCA) in 21 (30.9%), and vertebrobasilar artery-posterior cerebral artery (VB-PCA) in 6 (8.8%). The most common aneurysm location was the MCA (50%) in the microsurgery group and the ICA (47.1%) in the endovascular surgery group, which showed statistical significance (p = 0.001). Procedure-related complications during retreatment occurred in 4 (5.9%) patients: two (2.9%) experienced parent artery injury during microsurgery, one (1.5%) experienced thromboembolic infarction during endovascular surgery, and one (1.5%) experienced postoperative frontal contusion during microsurgery (Table 2). The rate of procedure-related complications did not differ between microsurgery (8.8%) and endovascular surgery (2.9%; p = 0.609). RRAs were completely obliterated in 51 (75.0%) patients, 13 (19.1%) had a neck remnant, and 4 (5.9%) were incomplete. The microsurgery group (82.4%) had more patients with complete obliteration than did to the endovascular surgery group (67.6%, p = 0.002). Fiftyone (75.0%) patients had favorable clinical outcomes at discharge, 14 (20.6%) had unfavorable outcomes, and 3 (4.4%) died. All 3 deaths were caused by brain injury due to rebleeding on admission for retreatment. Clinical outcomes at discharge did not differ between groups (p = 0.584). Our treatment strategies for RRAs are listed in Table 3. In the microsurgery group, 16 (47.1%) patients had additional clipping without removal of previous clips, 17 (50.0%) had clipping with removal of previous clips, and 1 (2.9%) had bypass surgery with trapping. In the endovascular surgery group, 28 (82.4%) patients had simple coiling, 5 (14.7%) had stent-assisted coiling, and 1 (2.9%) had a flow diverter in.
This retrospective study was approved by our institutional review board, and informed consent was waived. All patients who had cerebral aneurysms and underwent microsurgical clipping at our institution were retrospectively reviewed. Between 1996 and 2016, 6036 aneurysms were treated with either microsurgery or endovascular treatment. We treated ruptured aneurysms. And, treatment criteria of unruptured intracranial aneurysms were (1) patients with symptoms, (2) patients below 60 years of age, (3) with aneurysms larger than 5 mm, (4) with a daughter sac, (5) with prior subarachnoid hemorrhage (SAH) or family history, or (6) change of shape during the follow-up period. For the first treatment, treatment modality was selected based on characteristics of individual patients and intracranial aneurysms through interdisciplinary decision making, offering microsurgery as a primary treatment. The patients’ preferences for treatment were also considered. Two microvascular neurosurgeons and two endovascular neurosurgeons decided the treatment strategy, initial treatment plan, and retreatment plan in all cases. An RRA was defined as an aneurysm previously treated by microsurgical clipping with a remnant, regrowth, or rebleeding during the follow-up period. In the present study, 68 patients with previously clipped RRAs undergone retreatment were included. Our indications for the retreatment of RRAs are as follows: (1) rebleeding, 2) symptomatic RRAs, 3) regrowth of the aneurysms during the follow-up period, or 4) residual sacs due to incomplete or partial clipping. Retreatment was performed when the length of the residual sacs of the aneurysm neck represented enough space (more than 1.5 mm) for the placement of clips or coils. Forty-nine patients had previous clipping at our institution and 19 at other hospitals. Forty-seven (69.1%) patients were female and 21 (30.9%) male with a mean age of 49.3 ± 11.2 years at the time of retreatment. Thirty-four patients underwent microsurgery, and the other 34 patients underwent endovascular surgery for RRA. Radiographic images and clinical data were retrospectively reviewed to determine the treatment efficacy, clinical outcome, and important factors for selecting the treatment modality. Aneurysm size was classified as small (< 10 mm), large (10–24 mm), or giant (≥25 mm). Completeness of retreatment was confirmed by digital subtraction angiography (DSA) or CT angiography (CTA). Clinical outcomes (Glasgow Outcome Scale, GOS) were determined independently by a neurovascular nurse practitioner and two neurosurgeons. A favorable outcome was defined as a GOS of 4 or 5 (moderate disability or better), and an unfavorable outcome was defined as a GOS of 2 or 3 (severe disability or vegetative state). A GOS of 1 indicates death. Thirty-nine patients had a postoperative DSA, and all had a CTA.
3.1. Representative cases 3.1.1. Clipping with removal of previous clips A 34-year-old woman came to our hospital owing to a left upper extremity paresis and dysarthria. On her MRI, acute infarction was on the right basal ganglia and a giant thrombosed aneurysm was on the right middle cerebral artery bifurcation. The aneurysm was treated by microsurgical clipping and complete obliteration was achieved and confirmed by postoperative 3D digital subtraction angiography (DSA). After 7 years from the clipping, regrowth of the aneurysm was found on her follow-up 3D DSA (Fig. 1a). The recurred aneurysm had a triangular shape and was recurred from the neck portion. It could not be clipped completely without removing three old clips (Fig. 1b). We removed old clips carefully and performed re-clipping (Fig. 1c). Complete obliteration was achieved and confirmed by postoperative 3D DSA (Fig. 1d). 3.1.2. Simple coiling A 41-year-old man came to our hospital with an asymptomatic giant aneurysm on the left P1-2 junction. The aneurysm was treated by microsurgical clipping using the orbito-pterional approach. While we were removing intra-aneurysmal thrombus to expose the aneurysm neck, massive bleeding from the aneurysm was encountered. We decided to stop the bleeding with partial clipping of the aneurysm and perform endovascular treatment for the residual aneurysm. The residual aneurysm, sized about 2.25 × 1.10 mm, was confirmed on the immediate postoperative 3D DSA (Fig. 2a). Coil embolization without using stents was performed and achieved near complete obliteration of the aneurysm (Fig. 2b).
2.1. Statistical analysis Statistical analysis was performed with SPSS 20.0 (IBM software). Baseline characteristics and clinical outcomes were compared between the microsurgery and endovascular surgery groups with the MannWhitney U test or Student’s t-test for continuous variables and the Chisquare test or Fisher exact test for categorical variables. A p-value of less than 0.05 was considered statistically significant. 3. Results Clinical data and patient outcomes are summarized in Table 1. On admission for initial treatment, 58 (85.3%) patients presented with aneurysmal subarachnoid hemorrhage (aSAH). Retreatment was required for rebleeding in 31 (45.6%) patients, regrowth in 20 (29.4%), and remnant in 17 (25.0%). The median interval from the initial clipping until retreatment was 4.9 years (range, 0–20). Patient factors did not differ significantly between the microsurgery and endovascular surgery groups. Aneurysms were small in 52 (74.3%) patients, large in
4. Discussion Because the incidence of RRAs after microsurgical clipping has been estimated at 5%–8% [2–4], retreatment of these lesions must be discussed individually. RRAs carry a risk of bleeding and growing. The annual hemorrhage risk of RRAs was about 1.9% in dog-ear remnants [3]. The growth rates of dog-ear remnants and broad neck remnants 111
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Table 1 Clinical data and outcomes.
Age at initial treatment (years, mean ± SD) Female, n (%) aSAH as initial presentation, n (%) Cause of retreatment, n (%) Rebleeding Regrowth Remnant
Total (n = 68)
Microsurgery (n = 34)
Endovascular Surgery (n = 34)
p-value
49.3 ± 11.2 47 (69.1) 58 (85.3)
47.9 ± 11.7 21 (61.8) 30 (88.2)
50.7 ± 10.6 26 (76.5) 28 (82.4)
0.306 0.300 0.493 0.471
31 (45.6) 20 (29.4) 17 (25.0)
14 (41.2) 13 (38.2) 7 (20.6)
17 (50.0) 7 (20.6) 10 (29.4)
Median interval (years) Aneurysm size, n (%) Small Large Giant
4.9 (range, 0-20)
6.3 (range, 0-17)
2.3 (range, 0-20)
50 (73.5) 15 (22.1) 3 (4.4)
28 (82.3) 4 (11.8) 2 (5.9)
22 (64.7) 11 (32.4) 1 (2.9)
Aneurysm Location, n (%) ICA ACA MCA VB-PCA
20 (29.4) 21 (30.9) 21 (30.9) 6 (8.8)
4 (11.8) 11 (32.4) 17 (50.0) 2 (5.9)
16 (47.1) 10 (29.4) 4 (11.8) 4 (11.8)
Procedure-related complication, n (%) Parent artery injury Thromboembolic infarction Post-operative hemorrhage
4 2 1 1
3 2 0 1
1 0 1 0
Radiographic outcomes, n (%) Complete Near complete or neck remnant Incomplete
51 (75.0) 13 (19.1) 4 (5.9)
28 (82.4) 6 (17.6) 0 (0)
23 (67.6) 7 (20.6) 4 (11.8)
Clinical outcomes at discharge, n (%) Favorable (GOS 4 or 5) Unfavorable (GOS 2 or 3) Death (GOS 1)
51 (75.0) 14 (20.6) 3 (4.4)
27 (79.4) 6 (17.6) 1 (2.9)
24 (70.6) 8 (23.5) 2 (5.9)
0.244 0.188
0.001
(5.9) (2.9) (1.5) (1.5)
(8.8) (5.9) (0) (2.9)
(2.9) (0) (2.9) (0)
0.609
0.002
0.584
ACA = anterior cerebral artery; aSAH = aneurysmal subarachnoid hemorrhage; GOS = Glasgow Outcome Scale; ICA = internal carotid artery; MCA = middle cerebral artery; SD = standard deviation; VB-PCA = vertebrobasilar artery-posterior cerebral artery. Table 2 List of patients who experienced procedure-related complications. Case
Age (years)
Retreatment modality
Initial presentation
Interval (years)
Aneurysm location
Aneurysm size (mm)
Complications
Outcome (GOS)
22
38
SAH
11
ACOM
8
Frontal lobe contusion
3
28
69
SAH
10
MCBIF
3
Parent artery stenosis
2
32
46
SAH
15
ACOM
16
50
SAH
2
BABIF
6
Cerebral infarction due to parent artery injury Embolic infarction of brainstem
3
55
Clipping without removal of previous clips Clipping with removal of previous clips Clipping with removal of previous clips Simple coiling
3
ACOM = anterior communicating artery; BABIF = basilar artery bifurcation; GOS = Glasgow Coma Scale; MCBIF = middle cerebral artery bifurcation; SAH = subarachnoid hemorrhage.
RRAs should be considered for treatment. According to our experience, 68 (1.4%) of the 4818 patients who had microsurgical clipping underwent retreatment of an RRA by microsurgery and endovascular surgery. Microsurgery consisted of additional clipping with or without removal of previous clips or bypass surgery with trapping. Endovascular surgery consisted of simple coiling, stent-assisted coiling, or a flow diverter. As each patient has different demographic and aneurysm characteristics, developing a standard indication for treating RRAs is difficult. Therefore, a team approach is important in deciding which option is best to completely obliterate an RRA. In the event microsurgical and endovascular techniques were likely to have similar possibility of completely obliterating RRAs, we assessed the durability of treatment and risks associated with each procedure. Microsurgical clipping has been generally accepted as more durable than coil embolization. In ISAT, the risk of aneurysm recanalization after endovascular occlusion was associated with recurrent hemorrhage, although that risk was
Table 3 Treatment strategies for residual or recurrent aneurysms. Microsurgery, n (%)
N = 34
Clipping without removal of previous clips Clipping with removal of previous clips Bypass surgery with trapping Endovascular surgery, n (%) Simple coiling Stent-assisted coiling Flow diverter
16 (47.1) 17 (50.0) 1 (2.9) N = 34 28 (82.4) 5 (14.7) 1 (2.9)
were reported as 25% and 75%, respectively [3]. In ruptured aneurysms that had been clipped, the cumulative risk of aSAH recurrence was 0.5%, 2.2%, 5.5%, and 9.0% at 5, 10, 15, and 20 years, respectively [10]. In unruptured aneurysms, the cumulative risk of developing aSAH was 1.4% at 10 years and 12.4% at 20 years [11]. To avoid these risks,
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Fig. 1. A 34-year-old woman underwent microsurgical clipping due to a giant thrombosed aneurysm on the right middle cerebral artery bifurcation. After 7 years from the first operation, (a) regrowth of the aneurysm was found on her follow-up 3D digital subtraction angiography (DSA). (b) The recurred aneurysm had a triangular shape and was recurred from the neck portion. It could not be clipped completely without removing three old clips. (c) Old clips were removed and the aneurysm was re-clipped. (d) Complete oblitreation was achieved and confirmed by postoperative 3D DSA.
technical difficulties for microsurgery, including bypass surgery. Parent artery injury can cause severe morbidity or mortality. In such cases, with the development of assisted devices, endovascular surgery has been considered technically easier and safer. Therefore, we preferred endovascular surgery for RRAs in the ICA or VB-PCA.
small, with 10 episodes in 1073 patients after 1 year [12,13]. In addition, because of its long-term durability, clipping has an advantage over coiling especially in patients < 40 years old [14]. And in BRAT, which is ongoing, they show high recurrent rate (16.4%) and low complete obliteration rate (48%) in coiling patients so far [15]. Therefore, we prefer surgical treatment, especially in patients with a long-life expectancy. We also considered the risk of each procedure. In the present study, we performed bypass surgery for the retreatment in one patient. We have tried to perform endovascular treatment if bypass surgery was expected for the retreatment. If stents were expected for the retreatment, we have tried to perform microsurgery. If both bypass surgery and stent insertion were expected for the retreatment, risky, we prefer endovascular treatment. Aneurysm locations could affect the decision on treatment modality for RRAs. MCA aneurysms are easy to approach surgically and most had a wide neck [16]. Thus, microsurgical techniques were selected for many RRAs in the MCA. RRAs in the ICA or VB-PCA pose possible
4.1. Retreatment with microsurgery Microsurgical treatment of RRAs previously treated by surgical clipping can be dangerous. Because of the previous clips and tissue adhesions, dissection of the subarachnoid space and around the previous clip is not easy. This situation can result in injury of parent artery and micro surgically resect brain parenchyma. Due to adhesions, proximal control can be difficult. Thus, once we decided on microsurgical treatment for an RRA, we considered and prepared for bypass surgery depending on the lesion and for carotid artery preparation for proximal control with/without suction decompression in RRAs in the Fig. 2. A 41-year-old man with a giant aneurysm on the left P1-2 junction underwent microsurgical clipping While we were removing intra-aneurysmal thrombus to expose the aneurysm neck, massive bleeding from the aneurysm was encountered. We decided to stop the bleeding with partial clipping of the aneurysm and performed endovascular treatment for the residual aneurysm. (a) The residual aneurysm, sized about 2.25 × 1.10 mm, was confirmed on the immediate postoperative 3D digital subtraction angiography. (b) Coil embolization without using stents was performed and achieved near complete obliteration of the aneurysm.
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agencies in the public, commercial, or not-for-profit sectors.
ICA. Previous clips do not always need to be removed according to our experience. Removing old clips has been reported to be necessary for a wide operation field and complete RRA obliteration [17,18]. However, removing old clips is dangerous [19]. In the present study, we felt that the need to remove old clips could not be predicted before exposing the operation field. We confirmed the anatomical relationship of the old clip in the operation field and then decided whether remove it. If the old clip was disturbing complete obliteration of the RRA and no other options such as a fenestration clip were available, we removed the old clip along the line of the clip blade. Because our retreatment goal was complete obliteration, removing previous clips was not mandatory. If complete obliteration is needed, previous clips should be removed with caution. If additional surgical space is needed, we suck out the brain parenchyma in a non-eloquent area.
Acknowledgment None. References [1] Rates of delayed rebleeding from intracranial aneurysms are low after surgical and endovascular treatment, Stroke 37(6) (2006) 1437-42. [2] C.A. David, A.G. Vishteh, R.F. Spetzler, M. Lemole, M.T. Lawton, S. Partovi, Late angiographic follow-up review of surgically treated aneurysms, J. Neurosurg. 91 (3) (1999) 396–401. [3] J. Kivelev, R. Tanikawa, K. Noda, J. Hernesniemi, M. Niemela, K. Takizawa, T. Tsuboi, N. Ohta, S. Miyata, J. Oda, S. Tokuda, H. Kamiyama, Open surgery for recurrent intracranial aneurysms: techniques and long-term outcomes, World Neurosurg. 96 (2016) 1–9. [4] M. Sindou, J.C. Acevedo, F. Turjman, Aneurysmal remnants after microsurgical clipping: classification and results from a prospective angiographic study (in a consecutive series of 305 operated intracranial aneurysms), Acta Neurochir. (Wien) 140 (11) (1998) 1153–1159. [5] N. Chalouhi, R. Chitale, R.M. Starke, P. Jabbour, S. Tjoumakaris, A.S. Dumont, R.H. Rosenwasser, L.F. Gonzalez, Treatment of recurrent intracranial aneurysms with the Pipeline Embolization Device, J. Neurointerv. Surg. 6 (1) (2014) 19–23. [6] M. el-Beltagy, C. Muroi, P. Roth, J. Fandino, H.G. Imhof, Y. Yonekawa, Recurrent intracranial aneurysms after successful neck clipping, World Neurosurg. 74 (4-5) (2010) 472–477. [7] B.L. Hoh, B.S. Carter, C.M. Putman, C.S. Ogilvy, Important factors for a combined neurovascular team to consider in selecting a treatment modality for patients with previously clipped residual and recurrent intracranial aneurysms, Neurosurgery 52 (4) (2003) 732–738 discussion 738-9. [8] S. Mangiafico, M. Cellerini, G. Villa, F. Ammannati, L. Paoli, P. Mennonna, Endovascular coiling of aneurysm remnants after clipping in patients with followup. A single center experience, Interv. Neuroradiol. 11 (1) (2005) 41–48. [9] A.J. Molyneux, R.S. Kerr, J. Birks, N. Ramzi, J. Yarnold, M. Sneade, J. Rischmiller, Risk of recurrent subarachnoid haemorrhage, death, or dependence and standardised mortality ratios after clipping or coiling of an intracranial aneurysm in the International Subarachnoid Aneurysm Trial (ISAT): long-term follow-up, the Lancet, Neurology 8 (5) (2009) 427–433. [10] K. Tsutsumi, K. Ueki, M. Usui, S. Kwak, T. Kirino, Risk of recurrent subarachnoid hemorrhage after complete obliteration of cerebral aneurysms, Stroke 29 (12) (1998) 2511–2513. [11] K. Tsutsumi, K. Ueki, M. Usui, S. Kwak, T. Kirino, Risk of subarachnoid hemorrhage after surgical treatment of unruptured cerebral aneurysms, Stroke 30 (6) (1999) 1181–1184. [12] P. Mitchell, R. Kerr, A.D. Mendelow, A. Molyneux, Could late rebleeding overturn the superiority of cranial aneurysm coil embolization over clip ligation seen in the International Subarachnoid Aneurysm Trial? J. Neurosurg. 108 (3) (2008) 437–442. [13] A. Molyneux, R. Kerr, I. Stratton, P. Sandercock, M. Clarke, J. Shrimpton, R. Holman, International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial, Lancet 360 (9342) (2002) 1267–1274. [14] E. Guresir, P. Schuss, J. Berkefeld, H. Vatter, V. Seifert, Treatment results for complex middle cerebral artery aneurysms. A prospective single-center series, Acta Neurochir. (Wien) 153 (6) (2011) 1247–1252. [15] R.F. Spetzler, C.G. McDougall, J.M. Zabramski, F.C. Albuquerque, N.K. Hills, J.J. Russin, S. Partovi, P. Nakaji, R.C. Wallace, The barrow ruptured aneurysm trial: 6-year results, J. Neurosurg. 123 (3) (2015) 609–617. [16] M. Hokari, K. Kazumara, N. Nakayama, S. Ushikoshi, T. Sugiyama, K. Asaoka, K. Uchida, D. Shimbo, K. Itamoto, Y. Yokoyama, M. Isobe, T. Imai, T. Osanai, K. Houkin, Treatment of recurrent intracranial aneurysms after clipping: a report of 23 cases and a review of the literature, World Neurosurg. 92 (2016) 434–444. [17] H. Kashimura, K. Ogasawara, Y. Kubo, Y. Otawara, A. Ogawa, Microsurgical removal of previously placed aneurysm clips and application of new clips for recurrent cerebral aneurysms. Technical note, J. Neurosurg. 107 (4) (2007) 881–883. [18] T. Sakaki, T. Takeshima, M. Tominaga, H. Hashimoto, S. Kawaguchi, Recurrence of ICA-PCoA aneurysms after neck clipping, J. Neurosurg. 80 (1) (1994) 58–63. [19] R. Boet, W.S. Poon, S.C. Yu, The management of residual and recurrent intracranial aneurysms after previous endovascular or surgical treatment–a report of eighteen cases, Acta Neurochir. (Wien) 143 (11) (2001) 1093–1101. [20] J. Thornton, Q. Bashir, V.A. Aletich, G.M. Debrun, J.I. Ausman, F.T. Charbel, What percentage of surgically clipped intracranial aneurysms have residual necks? Neurosurgery 46 (6) (2000) 1294–1298 discussion 1298-300.
4.2. Retreatment with endovascular surgery Remarkable endovascular devices have been developed making endovascular surgery a safe and efficient tool to treat RRAs. Previous reports have also indicated successful RRA treatment with endovascular surgery [5,7,8]. But there are some difficulties when we perform endovascular treatment of RRAs. An old clip can hinder the vascular anatomy, induce artifacts, and the aneurysm morphology could be unfavorable for coil embolization. Because of these difficulties, as our result showed, endovascular retreatment had a higher rate of incomplete obliteration than did microsurgery. We overcame this problem with 3D rotational angiography to obtain precise anatomical images. We could understand the anatomical relation of the previous clips and parent vessels. Double-microcatheter, balloon-assisted, and stent-assisted techniques made the treatment safe and efficient, even when the RRA shape was not good for endovascular surgery. Recently, the flow diversion technique has been applied to treat intracranial aneurysms and RRAs [20]. However, studies on this treatment are limited. We only had one patient treated with a flow diverter, and that patient requires longer follow-up. 4.3. Retreatment outcomes We used the above strategies to treat RRAs. Of 34 surgically treated aneurysms, 33 were treated with clipping with or without removal of previous clips, and only one needed bypass surgery with trapping. Four RRAs (5.9%) had incomplete obliteration, all in the endovascular surgery group. Of these, 3 were treated a third time with endovascular surgery and achieved complete obliteration. The other patient is being observed. 5. Conclusion In properly selected cases, treatment of RRAs could be safely performed either by microsurgery or endovascular surgery and result in a good clinical outcome with acceptable morbidity. The decision to choose the treatment modality for RRAs after clipping is not easy but should be considered to lower the risk of retreatment. Thus, neurosurgeons should be aware of the risk of both retreatment modalities. Competing interests The authors declare that they have no competing interests. Funding This research did not receive any specific grant from funding
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