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Microsurgical Clipping for Recurrent Aneurysms After Initial Endovascular Coil Embolization
Peer-Review Reports
Microsurgical Clipping for Recurrent Aneurysms After Initial Endovascular Coil Embolization Tsuyoshi Izumo, Takayuki Matsuo, Yoichi Morofuji, Takeshi Hiu, Nobutaka Horie, Kentaro Hayashi, Izumi Nagata
Key words Aneurysm recurrence - Endovascular coiling - Intracranial aneurysms - Microsurgical clipping - Neurosurgery -
Abbreviations and Acronyms Acom: Anterior communicating artery CARAT: Cerebral Aneurysm Rerupture After Treatment DSA: Digital subtraction angiography ICA: Internal carotid artery ICG-VA: Indocyanine green video angiography ISAT: The International Subarachnoid Aneurysm Trial OA-PICA: Occipital artery to posterior inferior cerebellar artery PAO: Parent artery occlusion Pcom: Posterior communicating artery PICA: Posterior inferior cerebellar artery SAH: Subarachnoid hemorrhage From the Department of Neurosurgery, Nagasaki University Graduate School of Biomedical Sciences, Sakamoto, Nagasaki, Japan To whom correspondence should be addressed: Tsuyoshi Izumo, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2014.08.013 Supplementary digital content available online. Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
- OBJECTIVE:
Surgical treatment for recurrent lesions of embolized aneurysms is difficult and challenging for many neurosurgeons because intra-aneurysmal coil masses are sometimes scarred to the wall of the aneurysm or adherent to adjacent vital structures. To assess the efficacy and safety of surgical treatment without coil removal for recurrent aneurysms after previous coil embolization, we retrospectively studied clinical results, angiographic results, and complications in patients treated with additional microsurgical clipping.
- METHODS:
From April 2003 to April 2013, 7 patients with recurrent previous embolized aneurysms underwent microsurgical treatment.
- RESULTS:
This series included 1 man and 6 women receiving endovascular coiling as the first-line treatment. One patient’s aneurysm was unruptured, whereas the other 6 were ruptured. The aneurysm locations were posterior communicating (n [ 3), anterior communicating (n [ 2), ophthalmic (n [ 1), and posterior inferior cerebellar (n [ 1). The initial sizes ranged from 3e11.5 mm in diameter (mean, 6.6 mm), and the aspect ratios were 1.2 to 3.4 (mean, 1.9). In these aneurysms, the initial coiling result was complete occlusion in 5 patients, and neck remnants in 2 patients. The mechanism underlying aneurysm recurrence was coil compaction in 3 aneurysms, aneurysm regrowth in 3 aneurysms, and fundal migration in 1 aneurysm. The median recurrence latency was 28.8 months (range, 0.7e115 months). Microsurgical clippings without coil removal were used in 6 patients; a parent artery occlusion under bypass protection was done in 1 case with a posterior inferior cerebellar aneurysm. Fenestrated clips in combination with another type of clip were successfully used for 4 of 6 patients who were treated with direct neck clipping. No postoperative morbidity was observed, and postoperative imaging studies revealed complete occlusion of the aneurysms in all cases. There were no recurrences of aneurysms during the follow-up period (mean, 44.7 months; range, 0.5e118 months).
- CONCLUSIONS:
INTRODUCTION Endovascular treatment of intracranial aneurysms has been widely accepted as an established treatment for aneurysmal subarachnoid hemorrhage (SAH) (20, 24). Although the International Subarachnoid Aneurysm Trial (ISAT) data proved the initial clinical advantage of endovascular treatment of ruptured aneurysms, coil instability necessitating aneurysm retreatment remains a major shortcoming of endovascular treatment (23, 28). In patients in whom relevant aneurysm recurrences are documented on imaging follow-up, both endovascular and surgical techniques can be used. To assess the efficacy and safety of surgical treatment for recurrent aneurysms
The microsurgical clipping without coil removal for recurrent lesions of embolized aneurysms is effective and safe when it is technically feasible. The tandem clipping in combination with a fenestrated clip is a crucial method for direct neck clipping without coil removal for previously coiled recurrent aneurysms. For unclippable lesions, a parent artery occlusion under bypass protection should be taken into consideration. after previous embolization, we retrospectively studied angiographic results, clinical results, and complications in patients treated with additional surgery. METHODS From April 2003 to April 2013, patients with recurrent aneurysms after initial endovascular coil embolization, who were treated
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at our institution were included in this study. During this period, 274 patients underwent endovascular treatment for intracranial aneurysms as the first-line treatment, including 105 patients with SAH and ruptured aneurysms (38.3%). Our retreatment indication for recurrent aneurysm after endovascular coil embolization is 1) residually more than 30% of the original aneurysm, 2) progressing neck remnants, 3) aneurysm
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growth without coil compaction, and 4) outgrowth of a new daughter aneurysm. It was our policy to individualize treatment of recurrent aneurysms. When technically feasible, such as when recurrent aneurysms could be treated by simply adding coils in the previous cage or new cages could be made for additional coils, we attempted to treat endovascular aneurysm recurrences by additional coiling procedures. Among aneurysms not feasible for standard recoiling (e.g., aneurysms with a wide neck and remarkable space for applying clips) microsurgical clippings were selected. All operations were performed by a senior investigator (I.N.). Clinical evaluations were performed at 1 and 6 months after treatment, and annually thereafter. Follow-up imaging study was, or will be, annually performed in all patients by 3-dimensional computed tomographic angiography. The protocol was approved by the Ethics Committee of our institution, and written informed consent was obtained from all patients. Surgical Technique In patients with aneurysms in the posterior communicating artery (Pcom), anterior communicating artery (Acom), and ophthalmic segment of the internal carotid artery (Oph), microsurgical clipping was performed through the ipsilateral pterional approach. In the case with an ophthalmic aneurysm, ipsilateral proximal internal carotid artery (ICA) was prepared at the neck for proximal control. In the patient with vertebral artery-posterior
inferior cerebellar artery (PICA) aneurysm, ipsilateral lateral suboccipital craniotomy was performed. In all cases, except for a patient with a PICA aneurysm, direct neck clipping without intraaneurysmal coil removal was performed successfully. In the patient with a PICA aneurysm, direct clipping of the aneurysm was decided against due to the close proximity of the perforating artery to the medulla oblongata; therefore, an occipital artery to posterior inferior cerebellar artery (OA-PICA) bypass and a parent artery occlusion (PAO) was performed. Successful exclusion of the aneurysm and preservation of the branches was verified using intraoperative indocyanine green video angiography (ICG-VA) and/or intraoperative microvascular Doppler ultrasonography.
RESULTS During the 10-year study period, 21 patients, or 7.7 % of the group, received endovascular treatment for cerebral aneurysms, and experienced relevant aneurysm recurrences. Eight of the 21 patients refused the treatment and were followed by imaging studies. Therefore, 13 patients required additional treatment. Six patients were treated with endovascular recoiling, and 7 patients were treated surgically. The surgical series included 1 man and 6 women. The mean age was 60.3 years (range, 45e68 years) (Tables 1 and 2). The initial presentations were an SAH with Hunt and Kosnik grades _, III, and IV in each patient, grade III in 3 patients, and incidental finding in 1 patient. The
aneurysm locations were Pcom (3 cases), Acom (2 cases), ophthalmic segment of ICA (1 case), and PICA (1 case). The initial sizes ranged from 3e11.5 mm in diameter (mean, 6.6 mm), maximum neck width ranged from 2.2e6.7 mm (mean, 4.5 mm), and aspect ratio was 1.2 to 3.4 (mean, 1.9). Four of 7 aneurysms had a neck width more than 4 mm. In these 7 aneurysms, the initial coiling was performed without adjunctive techniques (e.g., balloon-assisted coiling or stent-assisted coiling). The results of the initial coiling were complete occlusion in 5 patients and neck remnants in 2 patients. The mechanisms underlying aneurysm recurrence were coil compaction in 3 aneurysms, aneurysm regrowth in 3 aneurysms, and fundal migration in 1 aneurysm. The median recurrence latency was 28.8 months (range, 0.7e115 months). Regarding multiple intracranial aneurysms, case 4 had a left middle cerebral artery aneurysm, and case 6 had an Acom aneurysm. Direct neck clipping of the aneurysm without coil removal was achieved in 6 patients. One patient (case 6) was treated by a PAO under OA-PICA bypass protection. Fenestrated clips in combination with another type of clip were used for 4 of 6 patients who were treated with direct neck clipping. The mean interval between coiling and surgery was 28.8 month (range, 21 dayse115 months). In all cases, except case 4, complete occlusion of the aneurysms was surgically achieved as proven by postoperative 3-dimensional computed tomographic angiography. Only in case 4 was the exclusion of the aneurysm confirmed by digital
Table 1. Patient Characteristics
Sex
Initial Status
H and K Grade
Aneurysm Location
Maximum Width (mm)
Neck Width (mm)
Aspect Ratio
Result of Initial Embolization
Mode of Recurrence
45
M
SAH
2
Acom
7.4
4.3
1.2
Complete obliteration
Regrowth
2
68
F
SAH
3
Acom
11.5
6.7
3.4
Complete obliteration
Compaction
3
63
F
SAH
2
Pcom
3
3
2
Complete obliteration
Fundal migration
4
58
F
SAH
2
PICA
4.3
2.2
2
Slight neck remnant
Regrowth
5
62
F
Unruptured
0
Oph
4.3
4.8
1.6
Complete obliteration
Regrowth
6
65
F
SAH
1
Pcom
7.7
3.9
1.6
Complete obliteration
Compaction
7
61
F
SAH
4
Pcom
8
6.4
1.8
Slight neck remnant
Compaction
Case No.
Age (year)
1
M, male; F, female; SAH, subarachnoid hemorrhage; H and K, Hunt and Kosnik; Acom, anterior communicating artery; Pcom, posterior communicating artery; PICA, posterior inferior cerebellar artery; Oph, ophthalmic artery.
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CLIPPING FOR COILED RECURRENT ANEURYSMS
Table 2. Microsurgical Results
Case No. 1
Mode of Recurrence
Technique of Surgery
Interval Between 1st and Last Treatment
Result After Last Treatment
Surgical Complications
Surgical Outcomes (mRS) (before / after additional treatment)
Regrowth
Clipping
21 days
Complete obliteration
None
1/1
2
Compaction
Clipping
14 months
Complete obliteration
None
0/0
3
Fundal migration
Clipping
41 months
Complete obliteration
Intraoperative rupture
2/2
4
Compaction
PAO w/bypass
21 months
Complete obliteration
None
1/1
5
Regrowth
Clipping
115 months
Complete obliteration
None
0/0
6
Compaction
Clipping
6.5 months
Complete obliteration
None
3/3
7
Compaction
Clipping
3.5 months
Complete obliteration
None
0/0
PAO, parent artery occlusion; w/, with; mRS, modified Rankin scale.
subtraction angiography (DSA). Two patients presented with preoperative neurological deficits such as hemiparesis or dysarthria. All patients kept the same modified Rankin scale postoperatively. Aside from 1 case of intraoperative rupture of the aneurysm (case 3), perioperative morbidity was not observed. There were no recurrences of aneurysms during the followup period (mean, 44.7 months; range, 0.5e118 months).
dome. Major bleeding was seen from the aneurysm (Figure 1F). A temporary clip was applied to the right proximal ICA to stop the bleeding. Then, a fenestrated-type clip was applied to the far-side neck of the aneurysm (Figure 1G). The temporary clip was removed and no bleeding from the aneurysm was confirmed. The postoperative imaging study showed no complication and complete obliteration of the aneurysm (Figure 1H, I). No aneurysm recurrence was observed during the follow-up period of 118 months.
Illustrative Case Examples Case 3. A 63-year-old woman presented Case 4. A 58-year-old woman presented with an SAH. DSA of her right ICA with a with an SAH. DSA of her left vertebral lateral position revealed a right Pcom artery revealed a left PICA aneurysm aneurysm (Figure 1A). She was treated with (Figure 2A). She was treated with coil coil embolization initially, and the aneuembolization initially, and the aneurysm rysm was completely obliterated was obliterated with a slight neck remnant (Figure 1B). Follow-up DSA revealed an (Figure 2B). The follow-up DSA revealed aneurysm recurrence 40 months after the an aneurysm recurrence 20 months after initial coil embolization (Figure 1C). In this the initial coil embolization (Figure 2C). case, direct neck clipping was thought to be Twenty-one months after the initial treatfeasible. Forty-one months after the initial ment, an additional surgery was pertreatment, an additional surgery was performed. The intraoperative findings formed (Video 1 [case 3]). Coil masses inrevealed that perforating arteries, which side the aneurysm were observed through were originating from the left the wall of the dome, partly proximal PICA, were very close extruded through the aneuand adhered to the neck of the rysm wall, and compressing aneurysm (Figure 2D). Conseand adherent to the right ocquently, direct neck clipping of ulomotor nerve (Figure 1D). A Video available at the aneurysm was decided straight-type titanium clip WORLDNEUROSURGERY.org against and a left OA-PICA was applied to the neck of the bypass and ligation of the left aneurysm (Figure 1E). This PICA was performed (Figure 2E, F). The procedure was thought to have completely obliterated the aneurysm. The dome was postoperative imaging study showed no incised with microscissors to release the complications, the patency of the left ococulomotor nerve from compression by the cipital artery, and complete obliteration of
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the aneurysm (Figure 2F,G, H). No aneurysm recurrence was observed during the follow-up period of 109 months. Case 6. A 65-year-old woman presented with an Hunt and Kosnik grade _, and Fisher group 3 SAH. DSA of her right ICA with a lateral position revealed a right Pcom aneurysm (Figure 3A). She was treated with coil embolization initially and the aneurysm was completely obliterated. However, two loops of coil protruded into the parent artery (Figure 3B). Follow-up DSA revealed a coil compaction 6 months after the initial coil embolization (Figure 3C). This recurrence was thought to have an adequate space for aneurysmal neck clipping. The additional surgery was performed 6.5 months after the initial coiling (Video 2 [case 6]). Coil masses inside the aneurysm were seen through, not only the wall of the dome, but also the wall of the neck. A straight-type titanium clip was first applied, and the tip of this clip slipped toward the Pcom due to the coil mass inside the dome of the aneurysm (Figure 3D). This clip was removed from the aneurysm. After, a fenestrated-type clip was applied to the far-side neck in partial occlusion of the aneurysm (Figure 3E). Intraoperative ICG-VA revealed a patency in the right ICA, Pcom, and anterior choroidal artery, and nonfilling of the aneurysm (Figure 3F). We added a straight clip in parallel to the near-side of the aneurysmal neck to completely obliterate the aneurysm (Figure 3G). Postoperative imaging studies showed no complications and complete obliteration of the aneurysm
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Figure 1. A 63-year-old woman presented with a ruptured right posterior communicating artery aneurysm (A). She was initially treated with endovascular coil embolization, and the aneurysm was completely obliterated (B). The follow-up digital subtraction angiography revealed an aneurysm recurrence 40 months after the initial coil embolization (C), and she was treated with additional surgery. An intraoperative finding revealed that the coil mass extruded through the aneurysm wall and was compressing and adherent to right oculomotor nerve (D). A clip was applied
(Figure 3H, I). During the follow-up period of 11 months, no aneurysm recurrence was observed.
to the neck of the aneurysm and this procedure was thought to have completely obliterated the aneurysm (E).The dome was incised to release the oculomotor nerve from compression, and this led to major bleeding from the aneurysm (F). Under proximal control, a fenestrated clip was applied to the far-side of the neck of the aneurysm (G). The temporally clip was removed and no bleeding from the aneurysm was confirmed. Postoperative imaging study revealed no complications and complete obliteration of the aneurysm (H and I).
DISCUSSION
7 cases were successfully treated with microsurgical direct neck clipping. For 1 patient, who had an unclippable recurrent aneurysm, a PAO under extracranialintracranial bypass protection was safely performed.
In the present study, we demonstrated that the microsurgical treatment without coil removal for recurrent aneurysms after initial endovascular coil embolization was an effective and safe modality. Six of
Aneurysm Retreatment After Initial Embolization Retreatment indication for recurrent aneurysms after previous endovascular coil
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embolization has often been discussed (12, 25, 32, 36, 37). Reported rates of aneurysm recurrence after initial endovascular treatment range from 3.6%e40% (3, 8, 16, 27, 30). Also, according to the Cerebral Aneurysm Rerupture After Treatment (CARAT) study, rerupture rates of incompletely obliterated aneurysms were as high as 17.6% during a mean follow-up of 4 years, when less than 70% of the aneurysm was occluded (4, 13, 16).
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Figure 2. A 58-year-old woman presented with a ruptured left posterior inferior cerebellar artery (PICA) aneurysm (A). She was treated with coil embolization initially and the aneurysm was obliterated with a slight neck remnant (B). The follow-up digital subtraction angiography revealed an aneurysm recurrence 20 months after the initial coil embolization (C), and an additional surgery was performed. The intraoperative findings revealed
Byrne et al. (2) also reported that the degree of aneurysm occlusion after treatment was associated with the risk of rerupture. A rebleeding rate of 0.4% for stable nonprogressing aneurysmal remnants after endovascular treatment and a 7.7% rebleeding rate for angiographically unstable aneurysmal residual have been
that perforating arteries, which originated from the left proximal PICA, were very close and adhered to the neck of the aneurysm (D). Consequently, a left occipital artery (OA) to the posterior inferior cerebellar artery bypass and ligation of the PICA was performed (E and F). Postoperative imaging studies showed no complication, patency of left OA, and complete obliteration of the aneurysm (G, H, and I).
reported (4). Loose-packed and growing remnant aneurysms are prone to rupture. Therefore, remarkable residual or recurrent aneurysms need close followup evaluations by imaging studies to determine whether they should be managed with endovascular retreatment or microsurgery.
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Treatment Selection Individualization of treatment for recurrent aneurysms after initial endovascular coil embolization was our policy. Although there are strong current trends that endovascular retreatment is selected for patients with endovascular aneurysmal recurrence (10, 12, 15, 22, 31, 35). In our cases,
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Figure 3. A 65-year-old woman presented with a ruptured right posterior communicating artery (Pcom) aneurysm (A). She was initially treated with endovascular coil embolization, and the aneurysm was completely obliterated (B). The follow-up digital subtraction angiography revealed an aneurysm recurrence (C) and was treated with additional surgery 6.5 months after the initial coil embolization. A tip of the applied clip slipped toward the Pcom due to a coil mass inside the dome of the aneurysm (D).
6 patients with endovascular aneurysm recurrence were successfully treated with endovascular recoiling during the same period of this study. There is a clearcut correlation between the width of the aneurysm neck, aneurysm size, and coil stability (6, 8, 19, 29). Recently, balloon and stent assistance have been commonly used for unfavorable intracranial aneurysms (38). Although these adjunctive techniques
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The clip was removed. A fenestrated-type clip was applied in partial occlusion of the far-side of the neck of the aneurysm (E). The intraoperative indocyanine green video angiography revealed a patency of the right internal carotid artery, Pcom, and anterior choroidal artery, and nonfilling of the aneurysm (F). A straight-type clip was applied in parallel to the near-side of the aneurysmal neck (G). The postoperative imaging study revealed no complications and complete obliteration of the aneurysm (H and I).
provide durable aneurysm closure, they are potentially associated with thromboembolic complications (26, 38). Older patients have higher aneurysm recanalization rates after stent-assisted coiling (5). Dorfer et al. (12) emphasized that coil stability after endovascular retreatment was significantly correlated with the underlying mechanism of aneurysm recurrence. Aneurysm recurrences due to coil
compaction without changes in aneurysmal morphology can be effectively treated by additional coiling. Conversely, recurrences due to aneurysmal regrowth without coil compaction have a tendency to recur (12). Therefore, we have selected microsurgical clipping for remarkable aneurysmal regrowth or recurrent aneurysms with wide necks, and this policy led us to obtain the best results.
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Surgical Techniques for Recurrences There is controversy about the danger and necessity of coil removal during surgery (7, 12, 25, 32-34, 37). Some investigators recommend systematic extraction of coils, even if they have protruded into the neck of the aneurysm or parent arteries (25, 33). Coiled aneurysms are often hard and not collapsible because of the coil mass inside or intra-aneurysmal thrombus formation. In these situations, the coil mass inside the aneurysm has to be removed to appropriately apply clips (25, 33). Other investigators emphasize the danger of removing coils from previously embolized aneurysms (11, 12, 34). Dorfer et al. (12) reported on a patient who was operated on 4 years after the embolization, and the attempted coil removal resulted in aneurysm rupture at the neck and ultimately led to sacrificing the ICA, which resulted in permanent morbidity. In chronic cases, coil extrusion from the wall of the aneurysm is not rare (12, 34). In our case 3, previous coils extruded and heavily scarred against the right oculomotor nerve. Thus, the previous coils are often ingrown into the wall of the aneurysm, parent arteries, or adjacent vital nerves, and attempted coil removal can be harmful to these structures. Among this surgical series, all endovascular recurrences were safely treated without removing coils. Also, in 6 of the 7 cases, clips were successfully applied beneath the coil mass. In 1 case of PICA aneurysm recurrence, PAO under the bypass protection was successfully performed. Tandem Clipping Technique Tandem clipping in combination with a fenestrated clip is a crucial method for direct neck clipping without coil removal for previously coiled recurrent aneurysms. Previously coiled aneurysms are difficult to clip because coil loops and masses inside or the thick and hard wall of the aneurysm can prevent the clip blades from completely closing. Unfortunately, accurate aneurysm wall thickness or consistency is not measurable by imaging studies preoperatively (18), and the dome of a cerebral aneurysm is a highly heterogenous region with areas of varying thicknesses(17). Therefore, the precise assessment of coil mass inside the proximity to closure line of an aneurysmal neck outside can be made, not by preoperative
CLIPPING FOR COILED RECURRENT ANEURYSMS
imaging studies, but by intraoperative findings (33). Thus, clips sometimes have to be applied to the neck of aneurysms with hard aneurysm walls, coil loops inside, or close proximity of the coil mass. In these cases, strong closing forces of clips are needed for complete closure. The closing force of the aneurysm clips gradually increases from the tip to the base of the clip blades (14). There must be a residual flow into the aneurysm after a single clip is applied, as illustrated in case 3, because of inadequate closure of the farside of the neck by the obstacles listed previously (Figure 4A). Hence, a tandem clipping method using a fenestrated clip in combination with another type of clip, reported previously for complex aneurysms (1, 9, 11, 21), is a useful technique for complete closure of previously coiled aneurysms (Figure 4B). The former can be applied for closure of the far-side aneurysmal neck, the latter for closing the near-side of the neck. In 4 of 6 of our patients, who were treated by direct neck clipping, aneurysms were successfully occluded using this tandem clipping method.
Limitations of the Study A limitation of this study is that the number of patients was relatively small. Further investigations are required for an accurate evaluation of the surgical outcome.
CONCLUSION For recurrent aneurysms after initial endovascular coil embolizations that are not feasible for standard recoiling, the microsurgical clipping without coil extraction is recommended when possible, and this policy led to successful clinical results in our practice. The tandem clipping method, in combination with a fenestrated clip, is crucial for direct neck clipping without coil removal for previously coiled recurrent aneurysms. REFERENCES 1. Anson JA, Lawton MT, Spetzler RF: Characteristics and surgical treatment of dolichoectatic and fusiform aneurysms. J Neurosurg 84:185-193, 1996. 2. Byrne JV, Sohn MJ, Molyneux AJ, Chir B: Five-year experience in using coil embolization for ruptured intracranial aneurysms: outcomes and incidence of late rebleeding. J Neurosurg 90:656-663, 1999. 3. Campi A, Ramzi N, Molyneux AJ, Summers PE, Kerr RS, Sneade M, Yarnold JA, Rischmiller J, Byrne JV: Retreatment of ruptured cerebral aneurysms in patients randomized by coiling or clipping in the International Subarachnoid Aneurysm Trial (ISAT). Stroke 38:1538-1544, 2007. 4. CARAT Investigators: Rates of delayed rebleeding from intracranial aneurysms are low after surgical and endovascular treatment. Stroke 37:1437-1442, 2006. 5. Chalouhi N, Jabbour P, Singhal S, Drueding R, Starke RM, Dalyai RT, Tjoumakaris S, Gonzalez LF, Dumont AS, Rosenwasser R, Randazzo CG: Stentassisted coiling of intracranial aneurysms: predictors of complications, recanalization, and outcome in 508 cases. Stroke 44:1348-1353, 2013. 6. Chalouhi N, Tjoumakaris S, Gonzalez LF, Dumont AS, Starke RM, Hasan D, Wu C, Singhal S, Moukarzel LA, Rosenwasser R, Jabbour P: Coiling of large and giant aneurysms: complications and long-term results of 334 cases. AJNR Am J Neuroradiol 35:546-552, 2014. 7. Chung J, Lim YC, Kim BS, Lee D, Lee KS, Shin YS: Early and late microsurgical clipping for initially coiled intracranial aneurysms. Neuroradiology 52:1143-1151, 2010. 8. Civit T, Auque J: Delayed aneurysm regrowth. J Neurosurg 90:807-809, 1999.
Figure 4. Schematic representation of direct neck clipping for previously coiled aneurysm recurrence. A single clip application results in an inadequate closure of the far-side of the aneurysmal neck due to obstacle coil loops inside (black dots) (A). A tandem clipping method using a straight fenestrated clip in combination with another straight clip secures the complete obliteration of the aneurysm, even if coil loops are inside (black dots) (B).
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9. Clatterbuck RE, Galler RM, Tamargo RJ, Chalif DJ: Orthogonal interlocking tandem clipping technique for the reconstruction of complex middle cerebral artery aneurysms. Neurosurgery 59:ONS347-351, 2006. 10. Corns R, Zebian B, Tait MJ, Walsh D, Hampton T, Deasy N, Tolias C: Prevalence of recurrence and retreatment of ruptured intracranial aneurysms treated with endovascular coil occlusion. Br J Neurosurg 27:30-33, 2013.
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11. Davies JM, Lawton MT: Advances in open microsurgery for cerebral aneurysms. Neurosurgery 74 (Suppl 1):S7-16, 2014. 12. Dorfer C, Gruber A, Standhardt H, Bavinzski G, Knosp E: Management of residual and recurrent aneurysms after initial endovascular treatment. Neurosurgery 70:537-553, 2012. 13. Elijovich L, Higashida RT, Lawton MT, Duckwiler G, Giannotta S, Johnston SC, Investigators CARATC: Predictors and outcomes of intraprocedural rupture in patients treated for ruptured intracranial aneurysms: the CARAT study. Stroke 39:1501-1506, 2008. 14. Horiuchi T, Rahmah NN, Yanagawa T, Hongo K: Revisit of aneurysm clip closing forces: comparison of titanium versus cobalt alloy clip. Neurosurg Rev 36:133-137 [discussion 137-138], 2013. 15. Islak C: The retreatment: indications, technique and results. Eur J Radiol 82:1659-1664, 2013. 16. Johnston SC, Dowd CF, Higashida RT, Lawton MT, Duckwiler GR, Gress DR; CARAT Investigators: Predictors of rehemorrhage after treatment of ruptured intracranial aneurysms: the Cerebral Aneurysm Rerupture After Treatment (CARAT) study. Stroke 39:120-125, 2008. 17. Kadasi LM, Dent WC, Malek AM: Cerebral aneurysm wall thickness analysis using intraoperative microscopy: effect of size and gender on thin translucent regions. J Neurointerv Surg 5:201-206, 2013. 18. Kadasi LM, Dent WC, Malek AM: Colocalization of thin-walled dome regions with low hemodynamic wall shear stress in unruptured cerebral aneurysms. J Neurosurg 119:172-179, 2013. 19. Knap D, Gruszczy nska K, Partyka R, Ptak D, Korzekwa M, Zbroszczyk M, Baron J: Results of endovascular treatment of aneurysms depending on their size, volume and coil packing density. Neurol Neurochir Pol 47:467-475, 2013. 20. Lanzino G, Fraser K, Kanaan Y, Wagenbach A: Treatment of ruptured intracranial aneurysms since the International Subarachnoid Aneurysm Trial: practice utilizing clip ligation and coil embolization as individual or complementary therapies. J Neurosurg 104:344-349, 2006. 21. Lawton MT, Spetzler RF: Surgical strategies for giant intracranial aneurysms. Neurosurg Clin N Am 9:725-742, 1998. 22. Li YD, Li MH, Gao BL, Fang C, Cheng YS, Wang W, Li WB, Zhao JG, Zhang PL, Wang J, Li M: Endovascular treatment of recurrent intracranial aneurysms with re-coiling or covered
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CLIPPING FOR COILED RECURRENT ANEURYSMS
stents. J Neurol Neurosurg Psychiatry 81:74-79, 2010. 23. Molyneux AJ, Kerr RS, Birks J, Ramzi N, Yarnold J, Sneade M, Rischmiller J; Collaborators I: 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. Lancet Neurol 8:427-433, 2009. 24. Molyneux AJ, Kerr RS, Yu LM, Clarke M, Sneade M, Yarnold JA, Sandercock P; Group ISATIC: International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet 366:809-817, 2005. 25. Nakamura M, Montibeller GR, Götz F, Krauss JK: Microsurgical clipping of previously coiled intracranial aneurysms. Clin Neurol Neurosurg 115: 1343-1349, 2013. 26. Ogilvy CS, Natarajan SK, Jahshan S, Karmon Y, Yang X, Snyder KV, Hopkins LN, Siddiqui AH, Levy EI: Stent-assisted coiling of paraclinoid aneurysms: risks and effectiveness. J Neurointerv Surg 3:14-20, 2011. 27. Park HK, Horowitz M, Jungreis C, Genevro J, Koebbe C, Levy E, Kassam A: Periprocedural morbidity and mortality associated with endovascular treatment of intracranial aneurysms. AJNR Am J Neuroradiol 26:506-514, 2005. 28. Raper DM, Allan R: International subarachnoid trial in the long run: critical evaluation of the long-term follow-up data from the ISAT trial of clipping vs coiling for ruptured intracranial aneurysms. Neurosurgery 66:1166-1169 [discussion 1169], 2010. 29. Raymond J, Salazkin I, Georganos S, Guilbert F, Desfaits AC, Gevry G, Weill A, Roy D: Endovascular treatment of experimental wide neck aneurysms: comparison of results using coils or cyanoacrylate with the assistance of an aneurysm neck bridge device. AJNR Am J Neuroradiol 23: 1710-1716, 2002.
Lanzino G, Boulos AS: Defining the risk of retreatment for aneurysm recurrence or residual after initial treatment by endovascular coiling: a multicenter study. Neurosurgery 65:311-315 [discussion 315], 2009. 32. Romani R, Lehto H, Laakso A, Horcajadas A, Kivisaari R, Fraunberg M, Niemelä M, Rinne J, Hernesniemi J: Microsurgical technique for previously coiled aneurysms. J Neurosurg Sci 55: 139-150, 2011. 33. Rubino PA, Castro JM, Kitroser M, Bottan JS, Salas E, Lambre J, Chiarullo M, Bustamante J: Microsurgical Clipping of Previously Coiled Aneurysms. World Neurosurg 82:e203-e208, 2013. 34. Sanai N, Caldwell N, Englot DJ, Lawton MT: Advanced technical skills are required for microsurgical clipping of posterior communicating artery aneurysms in the endovascular era. Neurosurgery 71:285-294, 2012. 35. Sedat J, Chau Y, Moubarak K, Vargas J, Lonjon M: Endovascular treatment of recurrent coiled aneurysms: assessment of complications and rebleeding during a decade in a single center. Interv Neuroradiol 18:14-19, 2012. 36. Tirakotai W, Sure U, Yin Y, Benes L, Schulte DM, Bien S, Bertalanffy H: Surgery of intracranial aneurysms previously treated endovascularly. Clin Neurol Neurosurg 109:744-752, 2007. 37. Waldron JS, Halbach VV, Lawton MT: Microsurgical management of incompletely coiled and recurrent aneurysms: trends, techniques, and observations on coil extrusion. Neurosurgery 64: 301-315, 2009. 38. Wang Y, Li Y, Jiang C, Wu Z, Jiang F, Meng H, Siddiqui AH, Yang X: Could the types of paraclinoid aneurysm be used as a criterion in choosing endovascular treatment? Neuro-radiologists’ view. Acta Neurochir (Wien) 155:2019-2027, 2013.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
30. Renowden SA, Koumellis P, Benes V, Mukonoweshuro W, Molyneux AJ, McConachie NS: Retreatment of previously embolized cerebral aneurysms: the risk of further coil embolization does not negate the advantage of the initial embolization. AJNR Am J Neuroradiol 29:1401-1404, 2008.
Received 28 January 2014; accepted 6 August 2014
31. Ringer AJ, Rodriguez-Mercado R, Veznedaroglu E, Levy EI, Hanel RA, Mericle RA, Lopes DK,
1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2014.08.013 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com
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Microsurgical Clipping for Recurrent Aneurysms After Initial Endovascular Coil Embolization Tsuyoshi Izumo, Takayuki Matsuo, Yoichi Morofuji, Takeshi Hiu, Nobutaka Horie, Kentaro Hayashi, Izumi Nagata
Key words Aneurysm recurrence - Endovascular coiling - Intracranial aneurysms - Microsurgical clipping - Neurosurgery -
Abbreviations and Acronyms Acom: Anterior communicating artery CARAT: Cerebral Aneurysm Rerupture After Treatment DSA: Digital subtraction angiography ICA: Internal carotid artery ICG-VA: Indocyanine green video angiography ISAT: The International Subarachnoid Aneurysm Trial OA-PICA: Occipital artery to posterior inferior cerebellar artery PAO: Parent artery occlusion Pcom: Posterior communicating artery PICA: Posterior inferior cerebellar artery SAH: Subarachnoid hemorrhage From the Department of Neurosurgery, Nagasaki University Graduate School of Biomedical Sciences, Sakamoto, Nagasaki, Japan To whom correspondence should be addressed: Tsuyoshi Izumo, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014). http://dx.doi.org/10.1016/j.wneu.2014.08.013 Supplementary digital content available online. Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
- OBJECTIVE:
Surgical treatment for recurrent lesions of embolized aneurysms is difficult and challenging for many neurosurgeons because intra-aneurysmal coil masses are sometimes scarred to the wall of the aneurysm or adherent to adjacent vital structures. To assess the efficacy and safety of surgical treatment without coil removal for recurrent aneurysms after previous coil embolization, we retrospectively studied clinical results, angiographic results, and complications in patients treated with additional microsurgical clipping.
- METHODS:
From April 2003 to April 2013, 7 patients with recurrent previous embolized aneurysms underwent microsurgical treatment.
- RESULTS:
This series included 1 man and 6 women receiving endovascular coiling as the first-line treatment. One patient’s aneurysm was unruptured, whereas the other 6 were ruptured. The aneurysm locations were posterior communicating (n [ 3), anterior communicating (n [ 2), ophthalmic (n [ 1), and posterior inferior cerebellar (n [ 1). The initial sizes ranged from 3e11.5 mm in diameter (mean, 6.6 mm), and the aspect ratios were 1.2 to 3.4 (mean, 1.9). In these aneurysms, the initial coiling result was complete occlusion in 5 patients, and neck remnants in 2 patients. The mechanism underlying aneurysm recurrence was coil compaction in 3 aneurysms, aneurysm regrowth in 3 aneurysms, and fundal migration in 1 aneurysm. The median recurrence latency was 28.8 months (range, 0.7e115 months). Microsurgical clippings without coil removal were used in 6 patients; a parent artery occlusion under bypass protection was done in 1 case with a posterior inferior cerebellar aneurysm. Fenestrated clips in combination with another type of clip were successfully used for 4 of 6 patients who were treated with direct neck clipping. No postoperative morbidity was observed, and postoperative imaging studies revealed complete occlusion of the aneurysms in all cases. There were no recurrences of aneurysms during the follow-up period (mean, 44.7 months; range, 0.5e118 months).
- CONCLUSIONS:
INTRODUCTION Endovascular treatment of intracranial aneurysms has been widely accepted as an established treatment for aneurysmal subarachnoid hemorrhage (SAH) (20, 24). Although the International Subarachnoid Aneurysm Trial (ISAT) data proved the initial clinical advantage of endovascular treatment of ruptured aneurysms, coil instability necessitating aneurysm retreatment remains a major shortcoming of endovascular treatment (23, 28). In patients in whom relevant aneurysm recurrences are documented on imaging follow-up, both endovascular and surgical techniques can be used. To assess the efficacy and safety of surgical treatment for recurrent aneurysms
The microsurgical clipping without coil removal for recurrent lesions of embolized aneurysms is effective and safe when it is technically feasible. The tandem clipping in combination with a fenestrated clip is a crucial method for direct neck clipping without coil removal for previously coiled recurrent aneurysms. For unclippable lesions, a parent artery occlusion under bypass protection should be taken into consideration. after previous embolization, we retrospectively studied angiographic results, clinical results, and complications in patients treated with additional surgery. METHODS From April 2003 to April 2013, patients with recurrent aneurysms after initial endovascular coil embolization, who were treated
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at our institution were included in this study. During this period, 274 patients underwent endovascular treatment for intracranial aneurysms as the first-line treatment, including 105 patients with SAH and ruptured aneurysms (38.3%). Our retreatment indication for recurrent aneurysm after endovascular coil embolization is 1) residually more than 30% of the original aneurysm, 2) progressing neck remnants, 3) aneurysm
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growth without coil compaction, and 4) outgrowth of a new daughter aneurysm. It was our policy to individualize treatment of recurrent aneurysms. When technically feasible, such as when recurrent aneurysms could be treated by simply adding coils in the previous cage or new cages could be made for additional coils, we attempted to treat endovascular aneurysm recurrences by additional coiling procedures. Among aneurysms not feasible for standard recoiling (e.g., aneurysms with a wide neck and remarkable space for applying clips) microsurgical clippings were selected. All operations were performed by a senior investigator (I.N.). Clinical evaluations were performed at 1 and 6 months after treatment, and annually thereafter. Follow-up imaging study was, or will be, annually performed in all patients by 3-dimensional computed tomographic angiography. The protocol was approved by the Ethics Committee of our institution, and written informed consent was obtained from all patients. Surgical Technique In patients with aneurysms in the posterior communicating artery (Pcom), anterior communicating artery (Acom), and ophthalmic segment of the internal carotid artery (Oph), microsurgical clipping was performed through the ipsilateral pterional approach. In the case with an ophthalmic aneurysm, ipsilateral proximal internal carotid artery (ICA) was prepared at the neck for proximal control. In the patient with vertebral artery-posterior
inferior cerebellar artery (PICA) aneurysm, ipsilateral lateral suboccipital craniotomy was performed. In all cases, except for a patient with a PICA aneurysm, direct neck clipping without intraaneurysmal coil removal was performed successfully. In the patient with a PICA aneurysm, direct clipping of the aneurysm was decided against due to the close proximity of the perforating artery to the medulla oblongata; therefore, an occipital artery to posterior inferior cerebellar artery (OA-PICA) bypass and a parent artery occlusion (PAO) was performed. Successful exclusion of the aneurysm and preservation of the branches was verified using intraoperative indocyanine green video angiography (ICG-VA) and/or intraoperative microvascular Doppler ultrasonography.
RESULTS During the 10-year study period, 21 patients, or 7.7 % of the group, received endovascular treatment for cerebral aneurysms, and experienced relevant aneurysm recurrences. Eight of the 21 patients refused the treatment and were followed by imaging studies. Therefore, 13 patients required additional treatment. Six patients were treated with endovascular recoiling, and 7 patients were treated surgically. The surgical series included 1 man and 6 women. The mean age was 60.3 years (range, 45e68 years) (Tables 1 and 2). The initial presentations were an SAH with Hunt and Kosnik grades _, III, and IV in each patient, grade III in 3 patients, and incidental finding in 1 patient. The
aneurysm locations were Pcom (3 cases), Acom (2 cases), ophthalmic segment of ICA (1 case), and PICA (1 case). The initial sizes ranged from 3e11.5 mm in diameter (mean, 6.6 mm), maximum neck width ranged from 2.2e6.7 mm (mean, 4.5 mm), and aspect ratio was 1.2 to 3.4 (mean, 1.9). Four of 7 aneurysms had a neck width more than 4 mm. In these 7 aneurysms, the initial coiling was performed without adjunctive techniques (e.g., balloon-assisted coiling or stent-assisted coiling). The results of the initial coiling were complete occlusion in 5 patients and neck remnants in 2 patients. The mechanisms underlying aneurysm recurrence were coil compaction in 3 aneurysms, aneurysm regrowth in 3 aneurysms, and fundal migration in 1 aneurysm. The median recurrence latency was 28.8 months (range, 0.7e115 months). Regarding multiple intracranial aneurysms, case 4 had a left middle cerebral artery aneurysm, and case 6 had an Acom aneurysm. Direct neck clipping of the aneurysm without coil removal was achieved in 6 patients. One patient (case 6) was treated by a PAO under OA-PICA bypass protection. Fenestrated clips in combination with another type of clip were used for 4 of 6 patients who were treated with direct neck clipping. The mean interval between coiling and surgery was 28.8 month (range, 21 dayse115 months). In all cases, except case 4, complete occlusion of the aneurysms was surgically achieved as proven by postoperative 3-dimensional computed tomographic angiography. Only in case 4 was the exclusion of the aneurysm confirmed by digital
Table 1. Patient Characteristics
Sex
Initial Status
H and K Grade
Aneurysm Location
Maximum Width (mm)
Neck Width (mm)
Aspect Ratio
Result of Initial Embolization
Mode of Recurrence
45
M
SAH
2
Acom
7.4
4.3
1.2
Complete obliteration
Regrowth
2
68
F
SAH
3
Acom
11.5
6.7
3.4
Complete obliteration
Compaction
3
63
F
SAH
2
Pcom
3
3
2
Complete obliteration
Fundal migration
4
58
F
SAH
2
PICA
4.3
2.2
2
Slight neck remnant
Regrowth
5
62
F
Unruptured
0
Oph
4.3
4.8
1.6
Complete obliteration
Regrowth
6
65
F
SAH
1
Pcom
7.7
3.9
1.6
Complete obliteration
Compaction
7
61
F
SAH
4
Pcom
8
6.4
1.8
Slight neck remnant
Compaction
Case No.
Age (year)
1
M, male; F, female; SAH, subarachnoid hemorrhage; H and K, Hunt and Kosnik; Acom, anterior communicating artery; Pcom, posterior communicating artery; PICA, posterior inferior cerebellar artery; Oph, ophthalmic artery.
2
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Table 2. Microsurgical Results
Case No. 1
Mode of Recurrence
Technique of Surgery
Interval Between 1st and Last Treatment
Result After Last Treatment
Surgical Complications
Surgical Outcomes (mRS) (before / after additional treatment)
Regrowth
Clipping
21 days
Complete obliteration
None
1/1
2
Compaction
Clipping
14 months
Complete obliteration
None
0/0
3
Fundal migration
Clipping
41 months
Complete obliteration
Intraoperative rupture
2/2
4
Compaction
PAO w/bypass
21 months
Complete obliteration
None
1/1
5
Regrowth
Clipping
115 months
Complete obliteration
None
0/0
6
Compaction
Clipping
6.5 months
Complete obliteration
None
3/3
7
Compaction
Clipping
3.5 months
Complete obliteration
None
0/0
PAO, parent artery occlusion; w/, with; mRS, modified Rankin scale.
subtraction angiography (DSA). Two patients presented with preoperative neurological deficits such as hemiparesis or dysarthria. All patients kept the same modified Rankin scale postoperatively. Aside from 1 case of intraoperative rupture of the aneurysm (case 3), perioperative morbidity was not observed. There were no recurrences of aneurysms during the followup period (mean, 44.7 months; range, 0.5e118 months).
dome. Major bleeding was seen from the aneurysm (Figure 1F). A temporary clip was applied to the right proximal ICA to stop the bleeding. Then, a fenestrated-type clip was applied to the far-side neck of the aneurysm (Figure 1G). The temporary clip was removed and no bleeding from the aneurysm was confirmed. The postoperative imaging study showed no complication and complete obliteration of the aneurysm (Figure 1H, I). No aneurysm recurrence was observed during the follow-up period of 118 months.
Illustrative Case Examples Case 3. A 63-year-old woman presented Case 4. A 58-year-old woman presented with an SAH. DSA of her right ICA with a with an SAH. DSA of her left vertebral lateral position revealed a right Pcom artery revealed a left PICA aneurysm aneurysm (Figure 1A). She was treated with (Figure 2A). She was treated with coil coil embolization initially, and the aneuembolization initially, and the aneurysm rysm was completely obliterated was obliterated with a slight neck remnant (Figure 1B). Follow-up DSA revealed an (Figure 2B). The follow-up DSA revealed aneurysm recurrence 40 months after the an aneurysm recurrence 20 months after initial coil embolization (Figure 1C). In this the initial coil embolization (Figure 2C). case, direct neck clipping was thought to be Twenty-one months after the initial treatfeasible. Forty-one months after the initial ment, an additional surgery was pertreatment, an additional surgery was performed. The intraoperative findings formed (Video 1 [case 3]). Coil masses inrevealed that perforating arteries, which side the aneurysm were observed through were originating from the left the wall of the dome, partly proximal PICA, were very close extruded through the aneuand adhered to the neck of the rysm wall, and compressing aneurysm (Figure 2D). Conseand adherent to the right ocquently, direct neck clipping of ulomotor nerve (Figure 1D). A Video available at the aneurysm was decided straight-type titanium clip WORLDNEUROSURGERY.org against and a left OA-PICA was applied to the neck of the bypass and ligation of the left aneurysm (Figure 1E). This PICA was performed (Figure 2E, F). The procedure was thought to have completely obliterated the aneurysm. The dome was postoperative imaging study showed no incised with microscissors to release the complications, the patency of the left ococulomotor nerve from compression by the cipital artery, and complete obliteration of
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the aneurysm (Figure 2F,G, H). No aneurysm recurrence was observed during the follow-up period of 109 months. Case 6. A 65-year-old woman presented with an Hunt and Kosnik grade _, and Fisher group 3 SAH. DSA of her right ICA with a lateral position revealed a right Pcom aneurysm (Figure 3A). She was treated with coil embolization initially and the aneurysm was completely obliterated. However, two loops of coil protruded into the parent artery (Figure 3B). Follow-up DSA revealed a coil compaction 6 months after the initial coil embolization (Figure 3C). This recurrence was thought to have an adequate space for aneurysmal neck clipping. The additional surgery was performed 6.5 months after the initial coiling (Video 2 [case 6]). Coil masses inside the aneurysm were seen through, not only the wall of the dome, but also the wall of the neck. A straight-type titanium clip was first applied, and the tip of this clip slipped toward the Pcom due to the coil mass inside the dome of the aneurysm (Figure 3D). This clip was removed from the aneurysm. After, a fenestrated-type clip was applied to the far-side neck in partial occlusion of the aneurysm (Figure 3E). Intraoperative ICG-VA revealed a patency in the right ICA, Pcom, and anterior choroidal artery, and nonfilling of the aneurysm (Figure 3F). We added a straight clip in parallel to the near-side of the aneurysmal neck to completely obliterate the aneurysm (Figure 3G). Postoperative imaging studies showed no complications and complete obliteration of the aneurysm
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Figure 1. A 63-year-old woman presented with a ruptured right posterior communicating artery aneurysm (A). She was initially treated with endovascular coil embolization, and the aneurysm was completely obliterated (B). The follow-up digital subtraction angiography revealed an aneurysm recurrence 40 months after the initial coil embolization (C), and she was treated with additional surgery. An intraoperative finding revealed that the coil mass extruded through the aneurysm wall and was compressing and adherent to right oculomotor nerve (D). A clip was applied
(Figure 3H, I). During the follow-up period of 11 months, no aneurysm recurrence was observed.
to the neck of the aneurysm and this procedure was thought to have completely obliterated the aneurysm (E).The dome was incised to release the oculomotor nerve from compression, and this led to major bleeding from the aneurysm (F). Under proximal control, a fenestrated clip was applied to the far-side of the neck of the aneurysm (G). The temporally clip was removed and no bleeding from the aneurysm was confirmed. Postoperative imaging study revealed no complications and complete obliteration of the aneurysm (H and I).
DISCUSSION
7 cases were successfully treated with microsurgical direct neck clipping. For 1 patient, who had an unclippable recurrent aneurysm, a PAO under extracranialintracranial bypass protection was safely performed.
In the present study, we demonstrated that the microsurgical treatment without coil removal for recurrent aneurysms after initial endovascular coil embolization was an effective and safe modality. Six of
Aneurysm Retreatment After Initial Embolization Retreatment indication for recurrent aneurysms after previous endovascular coil
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embolization has often been discussed (12, 25, 32, 36, 37). Reported rates of aneurysm recurrence after initial endovascular treatment range from 3.6%e40% (3, 8, 16, 27, 30). Also, according to the Cerebral Aneurysm Rerupture After Treatment (CARAT) study, rerupture rates of incompletely obliterated aneurysms were as high as 17.6% during a mean follow-up of 4 years, when less than 70% of the aneurysm was occluded (4, 13, 16).
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Figure 2. A 58-year-old woman presented with a ruptured left posterior inferior cerebellar artery (PICA) aneurysm (A). She was treated with coil embolization initially and the aneurysm was obliterated with a slight neck remnant (B). The follow-up digital subtraction angiography revealed an aneurysm recurrence 20 months after the initial coil embolization (C), and an additional surgery was performed. The intraoperative findings revealed
Byrne et al. (2) also reported that the degree of aneurysm occlusion after treatment was associated with the risk of rerupture. A rebleeding rate of 0.4% for stable nonprogressing aneurysmal remnants after endovascular treatment and a 7.7% rebleeding rate for angiographically unstable aneurysmal residual have been
that perforating arteries, which originated from the left proximal PICA, were very close and adhered to the neck of the aneurysm (D). Consequently, a left occipital artery (OA) to the posterior inferior cerebellar artery bypass and ligation of the PICA was performed (E and F). Postoperative imaging studies showed no complication, patency of left OA, and complete obliteration of the aneurysm (G, H, and I).
reported (4). Loose-packed and growing remnant aneurysms are prone to rupture. Therefore, remarkable residual or recurrent aneurysms need close followup evaluations by imaging studies to determine whether they should be managed with endovascular retreatment or microsurgery.
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Treatment Selection Individualization of treatment for recurrent aneurysms after initial endovascular coil embolization was our policy. Although there are strong current trends that endovascular retreatment is selected for patients with endovascular aneurysmal recurrence (10, 12, 15, 22, 31, 35). In our cases,
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Figure 3. A 65-year-old woman presented with a ruptured right posterior communicating artery (Pcom) aneurysm (A). She was initially treated with endovascular coil embolization, and the aneurysm was completely obliterated (B). The follow-up digital subtraction angiography revealed an aneurysm recurrence (C) and was treated with additional surgery 6.5 months after the initial coil embolization. A tip of the applied clip slipped toward the Pcom due to a coil mass inside the dome of the aneurysm (D).
6 patients with endovascular aneurysm recurrence were successfully treated with endovascular recoiling during the same period of this study. There is a clearcut correlation between the width of the aneurysm neck, aneurysm size, and coil stability (6, 8, 19, 29). Recently, balloon and stent assistance have been commonly used for unfavorable intracranial aneurysms (38). Although these adjunctive techniques
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The clip was removed. A fenestrated-type clip was applied in partial occlusion of the far-side of the neck of the aneurysm (E). The intraoperative indocyanine green video angiography revealed a patency of the right internal carotid artery, Pcom, and anterior choroidal artery, and nonfilling of the aneurysm (F). A straight-type clip was applied in parallel to the near-side of the aneurysmal neck (G). The postoperative imaging study revealed no complications and complete obliteration of the aneurysm (H and I).
provide durable aneurysm closure, they are potentially associated with thromboembolic complications (26, 38). Older patients have higher aneurysm recanalization rates after stent-assisted coiling (5). Dorfer et al. (12) emphasized that coil stability after endovascular retreatment was significantly correlated with the underlying mechanism of aneurysm recurrence. Aneurysm recurrences due to coil
compaction without changes in aneurysmal morphology can be effectively treated by additional coiling. Conversely, recurrences due to aneurysmal regrowth without coil compaction have a tendency to recur (12). Therefore, we have selected microsurgical clipping for remarkable aneurysmal regrowth or recurrent aneurysms with wide necks, and this policy led us to obtain the best results.
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Surgical Techniques for Recurrences There is controversy about the danger and necessity of coil removal during surgery (7, 12, 25, 32-34, 37). Some investigators recommend systematic extraction of coils, even if they have protruded into the neck of the aneurysm or parent arteries (25, 33). Coiled aneurysms are often hard and not collapsible because of the coil mass inside or intra-aneurysmal thrombus formation. In these situations, the coil mass inside the aneurysm has to be removed to appropriately apply clips (25, 33). Other investigators emphasize the danger of removing coils from previously embolized aneurysms (11, 12, 34). Dorfer et al. (12) reported on a patient who was operated on 4 years after the embolization, and the attempted coil removal resulted in aneurysm rupture at the neck and ultimately led to sacrificing the ICA, which resulted in permanent morbidity. In chronic cases, coil extrusion from the wall of the aneurysm is not rare (12, 34). In our case 3, previous coils extruded and heavily scarred against the right oculomotor nerve. Thus, the previous coils are often ingrown into the wall of the aneurysm, parent arteries, or adjacent vital nerves, and attempted coil removal can be harmful to these structures. Among this surgical series, all endovascular recurrences were safely treated without removing coils. Also, in 6 of the 7 cases, clips were successfully applied beneath the coil mass. In 1 case of PICA aneurysm recurrence, PAO under the bypass protection was successfully performed. Tandem Clipping Technique Tandem clipping in combination with a fenestrated clip is a crucial method for direct neck clipping without coil removal for previously coiled recurrent aneurysms. Previously coiled aneurysms are difficult to clip because coil loops and masses inside or the thick and hard wall of the aneurysm can prevent the clip blades from completely closing. Unfortunately, accurate aneurysm wall thickness or consistency is not measurable by imaging studies preoperatively (18), and the dome of a cerebral aneurysm is a highly heterogenous region with areas of varying thicknesses(17). Therefore, the precise assessment of coil mass inside the proximity to closure line of an aneurysmal neck outside can be made, not by preoperative
CLIPPING FOR COILED RECURRENT ANEURYSMS
imaging studies, but by intraoperative findings (33). Thus, clips sometimes have to be applied to the neck of aneurysms with hard aneurysm walls, coil loops inside, or close proximity of the coil mass. In these cases, strong closing forces of clips are needed for complete closure. The closing force of the aneurysm clips gradually increases from the tip to the base of the clip blades (14). There must be a residual flow into the aneurysm after a single clip is applied, as illustrated in case 3, because of inadequate closure of the farside of the neck by the obstacles listed previously (Figure 4A). Hence, a tandem clipping method using a fenestrated clip in combination with another type of clip, reported previously for complex aneurysms (1, 9, 11, 21), is a useful technique for complete closure of previously coiled aneurysms (Figure 4B). The former can be applied for closure of the far-side aneurysmal neck, the latter for closing the near-side of the neck. In 4 of 6 of our patients, who were treated by direct neck clipping, aneurysms were successfully occluded using this tandem clipping method.
Limitations of the Study A limitation of this study is that the number of patients was relatively small. Further investigations are required for an accurate evaluation of the surgical outcome.
CONCLUSION For recurrent aneurysms after initial endovascular coil embolizations that are not feasible for standard recoiling, the microsurgical clipping without coil extraction is recommended when possible, and this policy led to successful clinical results in our practice. The tandem clipping method, in combination with a fenestrated clip, is crucial for direct neck clipping without coil removal for previously coiled recurrent aneurysms. REFERENCES 1. Anson JA, Lawton MT, Spetzler RF: Characteristics and surgical treatment of dolichoectatic and fusiform aneurysms. J Neurosurg 84:185-193, 1996. 2. Byrne JV, Sohn MJ, Molyneux AJ, Chir B: Five-year experience in using coil embolization for ruptured intracranial aneurysms: outcomes and incidence of late rebleeding. J Neurosurg 90:656-663, 1999. 3. Campi A, Ramzi N, Molyneux AJ, Summers PE, Kerr RS, Sneade M, Yarnold JA, Rischmiller J, Byrne JV: Retreatment of ruptured cerebral aneurysms in patients randomized by coiling or clipping in the International Subarachnoid Aneurysm Trial (ISAT). Stroke 38:1538-1544, 2007. 4. CARAT Investigators: Rates of delayed rebleeding from intracranial aneurysms are low after surgical and endovascular treatment. Stroke 37:1437-1442, 2006. 5. Chalouhi N, Jabbour P, Singhal S, Drueding R, Starke RM, Dalyai RT, Tjoumakaris S, Gonzalez LF, Dumont AS, Rosenwasser R, Randazzo CG: Stentassisted coiling of intracranial aneurysms: predictors of complications, recanalization, and outcome in 508 cases. Stroke 44:1348-1353, 2013. 6. Chalouhi N, Tjoumakaris S, Gonzalez LF, Dumont AS, Starke RM, Hasan D, Wu C, Singhal S, Moukarzel LA, Rosenwasser R, Jabbour P: Coiling of large and giant aneurysms: complications and long-term results of 334 cases. AJNR Am J Neuroradiol 35:546-552, 2014. 7. Chung J, Lim YC, Kim BS, Lee D, Lee KS, Shin YS: Early and late microsurgical clipping for initially coiled intracranial aneurysms. Neuroradiology 52:1143-1151, 2010. 8. Civit T, Auque J: Delayed aneurysm regrowth. J Neurosurg 90:807-809, 1999.
Figure 4. Schematic representation of direct neck clipping for previously coiled aneurysm recurrence. A single clip application results in an inadequate closure of the far-side of the aneurysmal neck due to obstacle coil loops inside (black dots) (A). A tandem clipping method using a straight fenestrated clip in combination with another straight clip secures the complete obliteration of the aneurysm, even if coil loops are inside (black dots) (B).
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Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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Received 28 January 2014; accepted 6 August 2014
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