Neurology India, Vol. 58, No. 2, March-April, 2010, pp. 292-297
Surgical management of intracranial aneurysms previously treated with endovascular therapy
Rajiv Kumar, CE Deopujari, Rajan Shah, Rakesh Luhana
Department of Neurosurgery, Bombay Hospital Institute of Medical Sciences, Mumbai, India
Correspondence Address:Rajiv Kumar, Department of Neurosurgery, 2nd Floor, L.T.M.G. Hospital, Sion (W), Mumbai - 400 022, India, email@example.com
Date of Acceptance: 02-Oct-2009
Code Number: ni10073
AbstractEndovascular treatment with coils of cerebral aneurysm is being increasingly used for definitive treatment. An increasing number of patients are coming for surgical intervention either for recurrences, incomplete coil embolization or its complications. Our objective was to assess the surgical management in such patients. This was a retrospective analysis of the patients who were initially treated with endovascular embolization and later managed surgically with clipping either for unsuccessful coiling, recurrence of aneurysm or post-procedural complication, between 2003 and 2007. Anatomical results were excellent in all five patients, and all the aneurysms were totally excluded from the circulation. All patients had good recovery. None of the patients suffered any major intraoperative or postoperative complication. Neurosurgical management of intracranial aneurysms previously treated with endovascular therapy is an emerging challenge, but with proper patient selection and careful planning, this subset of aneurysms can be managed with good results.
Keywords: Aneurysm recurrence, coil embolization, clipping, subarachnoid hemorrhage
Endovascular therapy has evolved rapidly in the last two decades and emerged as an effective treatment option for selected intracranial aneurysms. ,,,, As the use of endovascular techniques becomes more widespread, a growing number of patients are coming for surgical intervention either for failed embolization, residual aneurysm, recurrent aneurysm, or for postembolization complications. We report a series of five patients that were initially treated with endovascular embolization and later managed surgically with clipping either for unsuccessful coiling, recurrence of aneurysm or post-procedural complication.
It is a retrospective analysis of the patients who had endovascular embolization previously and were later managed surgically with clipping for various reasons. From 2003 to 2007, a total of 120 patients of aneurysms were surgically treated. Out of these, five patients were previously treated with endovascular therapy. All data regarding patient′s age, sex, clinical findings, aneurysm location, size, and geometry were collected. All angiograms and operative notes were reviewed.
For Select Cases of Intracranial Aneurysms
A 46-year-old female presented with a Hunt and Hess Grade I subarachnoid hemorrhage. Her angiogram revealed right middle cerebral artery aneurysm [Figure - 1]a for which coiling was attempted. The aneurysm ruptured while coiling, so the procedure was abandoned. Post-coiling angiogram showed patent aneurysm and part of the coil lying outside the aneurysm [Figure - 1]b. She was then referred to our institute for surgical management. We did clipping of the aneurysm by pterional craniotomy. On opening the sylvian fissure, coil was seen and was traced up to the aneurysm. We did not try to remove the coil and clipped the aneurysm after obtaining proximal and distal control. Postoperative angiogram showed complete exclusion of the aneurysm [Figure - 1]c. Patient was neurologically intact postoperatively and was discharged without any deficit.
A 52-year-old male presented with a Hunt and Hess Grade I subarachnoid hemorrhage. Angiogram showed wide-necked left internal carotid artery meningohypophyseal aneurysm with persistent trigeminal artery [Figure - 2]a. The aneurysm was coiled and postoperative angiogram done showed complete exclusion of the aneurysm [Figure - 2]b. But patient woke up with right hemiparesis and aphasia, and computed tomogram (CT) scan done showed left middle cerebral artery territory infarct. He had a partial recovery from his deficit and one year later he again presented with subarachnoid hemorrhage. Angiogram showed re-growth of an aneurysm [Figure - 2]c. Endovascular coiling was ruled out, as clot was seen at the neck and a loop of the coil was lying in a parent vessel. We utilized the endovascular technique for proximal control by placing a balloon in front of the origin of persistent trigeminal artery and inflating the balloon while aneurysm neck dissected. Aneurysm was clipped successfully. His postoperative angiogram showed complete aneurysm exclusion from the circulation [Figure - 2]d. His postoperative recovery was uneventful.
A 70-year-old female had an unruptured internal carotid artery posterior communicating aneurysm. She underwent endovascular coil embolization, but complete coil embolization could not be achieved. Follow-up angiogram at three months showed significant residual aneurysm. She underwent pterional craniotomy and aneurysm was clipped successfully. Her postoperative angiogram showed complete exclusion of the aneurysm and she remained neurologically intact.
A 45-year-old male presented with a Hunt and Hess Grade I subarachnoid hemorrhage. His angiogram showed anterior communicating artery aneurysm which was coiled. Follow-up angiogram at three months detected re-growth of an aneurysm. He underwent pterional craniotomy and the aneurysm was clipped successfully. His postoperative angiogram showed complete exclusion of an aneurysm and he had an uneventful recovery.
A 39-year-old, right-handed businessman presented with a Hunt and Hess Grade I subarachnoid hemorrhage. Angiogram of cerebral vessels showed a small, wide-necked, pear-shaped anterior communicating artery aneurysm [Figure - 3]a. He underwent coiling of the aneurysm. On different views, coil mass appeared to be in the aneurysmal sac [Figure - 3]b. Patient was extubated and shifted to intensive care unit with no focal neurological deficit. After 30 min he developed transient right-sided hemiparesis, which recovered within 15 min. Computed tomography of brain did not show any fresh hemorrhage, but the coil appeared a little higher than expected on the lateral scanogram. With a suspicion of distal coil migration, angiography of the cerebral vessels was repeated. Left common carotid artery angiogram showed that the coil mass had moved distally into proximal left A2 [Figure - 3]c. The anterior communicating artery aneurysm was opacified completely. After discussing with the patient′s relative, he was taken up for surgical clipping of the aneurysm. A left pterional craniotomy was performed and the aneurysm was clipped successfully. Post-clipping angiography showed exclusion of the aneurysm from circulation. [Figure - 3]d As coil mass was seen retained in the left A2 with flow across, it was decided to leave coil untouched. After 48 h he was started on antiplatelet therapy to prevent thromboembolic episodes. Postoperatively he made an uneventful recovery. A repeat computed tomography brain however, showed a left frontopolar infarct.
The first attempt by a neurosurgeon to treat an aneurysm using an endovascular technique was made in 1964 by Luessenhop and Velasquez to occlude an aneurysm by advancing a silicon balloon into a supraclinoid carotid lesion.  However, this treatment was unsuccessful. In 1973 Serbinenko selectively obliterated an aneurysm using a latex balloon.  The introduction of retrievable detachable coils in 1991 revolutionized the treatment of patients with intracranial aneurysms.  In the ensuing 30 years steady advances have been made in the techniques and material used in endovascular therapy.  The ISAT (International Subarachnoid Aneurysm Trial) has resulted in increasing numbers of patients with a ruptured aneurysm undergoing endovascular coiling.  Although endovascular therapy has its own complications and treatment failures. Also, the issue of regrowth of aneurysm, rebleeding and long-term efficacy has not yet been resolved. Incomplete initial treatments or aneurysm recurrences are not uncommon, necessitating repeat treatment using either surgical or endovascular technique.
In our series of five patients, three patients had regrowth of aneurysms; while in two patients regrowth was detected on follow-up angiography, the third patient presented with subarachnoid hemorrhage. Two other patients treated surgically had endovascular procedure-related complications, namely aneurysm rupture during coiling and distal coil migration. In a study by Thornton et al., of 143 aneurysms treated by guglielmi detachable coils (GDC) and followed up for at least six months, they observed that, among aneurysms that were considered to be 100% occluded in the initial examination, recurrence was 1.8%.  They also noted that of the 87 aneurysms that were considered incompletely cured initially, 46% exhibited progressive thrombosis, 26% exhibited stable neck remnants, and 28% exhibited enlargement of the residual neck.  Thornton et al. had summarized the angiographic follow-up results for a large number of coiled aneurysms, as reported in the available literature.  They reviewed the results of 12 series including 1042 aneurysms for which angiographic follow-up data was available for six months or more and found that recurrence was observed for 0 to 37% of aneurysms, which were 90 to 100% occluded in the initial angiogram. Lin et al., reported 16 cases of verified regrowth of a residual neck. 
Recurrent subarachnoid hemorrhage from previously coiled aneurysms has been reported in the literature and rate varies from 0 to 5%. ,,,,, In the ISAT, the endovascular group had a rehemorrhage rate of 3.2% after one-year follow-up  . Byrne et al., calculated the yearly risk of rehemorrhage, and found it to be 0.4%, 0.6%, 0.8% and 0% for years 1, 2, 3, and 4.  Lin et al., and Drake , have shown that incomplete treatment of an aneurysm might result in recurrent hemorrhage.
Procedure-related complications of endovascular coil occlusion vary between 9% and 15%.  Following parent vessel occlusion, transient neurological deficit may occur in up to 12% of cases with permanent deficit in 1.5-4.45%.  In a meta-analysis of endovascular treatment of 1811 intracranial aneurysms, procedural complications encountered were aneurysm perforation (3.6%), thromboembolic events (9.1%), coil malposition (2.5%), coil malposition and thrombosis (0.1%). Coil malposition and thrombotic occlusion of the parent artery was seen in two (0.1%) patients. 
Distal coil migration is a rare, but hazardous procedural complication of aneurysm coil embolization.  In a randomized controlled trial of 111 patients by Kuopio, in which 52 patients had Guglielmi detachable coil, one had coil migration.  In the multicentre study of 403 patients by Vinuela et al., two (0.5%) patients had coil migration.  Thornton et al., described two cases in which coils migrated out of the aneurysm and extended along the parent artery. Both patients developed ischemic symptoms within 48 h of coiling. Both cases were in small aneurysms.  In a series of 21 cases by Zhang et al., in which neurosurgical management of cerebral aneurysm was done following unsuccessful or incomplete endovascular embolization, one patient had coil migration.  Picard et al., had six cases of coil migration in a series of 135 patients.  Risk of coil displacement from the aneurysm to the parent vessel is high, if the neck of the aneurysm is wide.
The literature on the surgical management of previously embolized aneurysm is limited [2, 3, 23, 25-27] and only a few articles specifically address the issues of aneurysm retreatment. [3, 25, 27] In 1995, Gurian et al., presented a series of 141 aneurysms that had been embolized using Guglielmi detachable coils, and eight of the lesions
later required surgical management for aneurysm remnants.  Out of eight, five were clipped, two were bypassed and trapped, and one was managed with Hunterian ligation. All patients had well to excellent results. He made a number of suggestions regarding retreatment, as follows. 1) If retreatment is required, repeat embolization should be attempted before considering surgical option. 2) Important factors in the decision of retreatment and choosing the modality include aneurysms, location of aneurysm, degree of neck occlusion, elapsed time since the previous embolization, and patient′s age and neurological status. 3) Aneurysms without coil in the neck are easier to treat with clipping, whereas aneurysms with coil mass in the neck are difficult to clip without coil extraction. 4) Clipping of large partially coiled aneurysms can be difficult because of relatively immobile mass making visualization around the lesion difficult. Intraoperative angiography can be valuable in such cases. Civic et al., and Horowitz et al.,  also made similar observations. While treating a partially coiled aneurysm or recurrent lesion surgically, Horowitz et al.,  observed that the basic goals of maximal exposure and early acquisition of proximal and distal control of afferent and efferent vessels is the key to successful retreatment. Horowitz et al.,  recommend liberal temporary occlusion in the management of both primary and secondary treated lesions. When an aneurysm has sufficient coil mass within the fundus to preclude clipping, Horowitz et al.,  use temporary clipping, fundal incision, coil removal, and neck clipping. Civic et al.,  noted that the volume produced by the coils in the aneurysms allows easy dissection. Veznedaroglu et al.,  and Minh et al.,  emphasized on more difficulties in the dissection, and in avoiding perforator injury. Minh et al.,  reported that with partially coiled aneurysms, clipping can be accomplished without technical difficulties, but, when the packing of the aneurysm with coils is near total, difficulties may arise during surgery.
In our series, all aneurysms were clipped using standard microsurgical techniques. All aneurysms were approached by pterional craniotomy. Proximal and distal controls of afferent and efferent vessels were acquired early. Temporary clipping was used while manipulation of aneurysm and neck dissection was performed. We found that when neck was free from coils, coiling was easier. In our first patient, who had rupture of aneurysm while coiling, coil was seen on opening the sylvian fissure and was traced up to the aneurysm. We did not try to remove the coil, and clipped the aneurysm after obtaining proximal and distal control. In three other patients who had regrown aneurysm, standard microsurgical techniques were used. In our Case 5, the postembolization angiogram had shown complete exclusion of the aneurysm from circulation. However, he developed transient hemiplegia 30 min later, from which he recovered within the next 15 min. The probable explanation would be that when the coil migrated from the aneurysm it caused a transient occlusion, before being pushed back in the A2 or vasospasm of the parent artery, which was relieved later on. If we had missed that transitory hemiplegia, coil migration would not have been picked up immediately. A high index of suspicion led us to diagnose this complication. In our case, the patient was immediately taken for surgical clipping of the aneurysm and the migrated coil was left in situ. This case demonstrates that a neurosurgical team should be available to handle any complication during an endovascular procedure, so that appropriate neurosurgical intervention can be carried out without delay.
Coils that migrate can be recovered with various retriever devices. Various micro snare devices have been developed to address this problem.  However, herniation of a short length of coil into parent artery is no cause for alarm and is best managed by leaving it in situ, and maintaining anticoagulation and antiplatelet therapy for up to two months.  Also, one or two coil loops in a parent vessel may be harmless in terms of thrombus or embolus generation. Opinion regarding coil extraction is varied. Civic et al., advocated no coil removal.  Thornton et al., used coil extraction in operating on almost all coiled aneurysms.  Zhang et al., and Horowitz et al., used coil extraction only when the coil mass impeded an initial clipping trial. , Similarly, we do not advocate routine coil removal as it might be incorporated in the vessel wall and may cause parent vessel damage. When it is decided to remove the coils, liberal use of temporary clipping can be done to achieve complete aneurysm trapping followed by partial coil removal. 
Hopkins et al., had made recommendations regarding prevention of coil migration.  They recommended that the initial coils should be as long as possible to create an anchored matrix in the aneurysm cavity. Successive shorter coils should be introduced above the initial coil, pushing it down toward the aneurysm neck. In this way, the largest single bulk of coil is subjected to the most turbulent region of blood flow, which minimizes coil migration out of the body. Turbulent blood flow can remodel coil morphology during the first 24-48 h after coiling.  Moret et al., had improved the technique of coil occlusion by using a nondetachable balloon.  Placement of balloon or self-expandable stent over the aneurysm neck followed by packing of coils prevents coil migration.
Basic principles of aneurysm surgery are highly relevant in the operative management of partially treated aneurysms. Maximal exposure with judicious use of cranial base techniques and early acquisition of proximal and distal control of afferent and efferent vessels are the keys to success. 
Neurosurgical management of intracranial aneurysms previously treated with endovascular therapy is an emerging challenge, but with proper patient selection and careful planning, this subset of aneurysms can be clipped with good results. One requires working with a high index of suspicion, when post-endovascular-procedure patients present with neurological signs. We would strongly recommend immediate digital substraction asngiography (DSA) and surgical intervention in such cases.
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