Korean Journal of Cerebrovascular Surgery 2008;10(3):411-418.
Published online September 1, 2008.
Coiling of Middle Cerebral Artery Bifurcation Aneurysms : Clinical and Angiographic Outcomes.
Lee, Jung Hwan , Ko, Jun Kyeung , Lee, Sang Weon , Lee, Tae Hong , Choi, Chang Hwa
1Department of Neurosurgery, School of Medicine, Pusan National University, Busan, Korea. sangweonlee@pusan.ac.kr
2Department of Radiology, School of Medicine, Pusan National University, Busan, Korea.
Abstract
OBJECTIVE
The anatomy of middle cerebral artery (MCA) bifurcation aneurysms has been noted to be unfavorable for endovascular treatment. Our purpose was to analyze the clinical and angiographic results of coiling of the MCA bifurcation aneurysms. METHODS: From January 2004 to April 2007, 26 patients harboring 29 MCA bifurcation aneurysms were treated with coils. Of these patients, 16 had subarachnoid hemorrhages (SAH). The bleeding source was a ruptured MCA bifurcation aneurysm in 11 patients and a ruptured aneurysm in a different location in 5 patients, respectively. Treatment-related complications, clinical outcomes, and postprocedural and follow-up angiography results were retrospectively evaluated. RESULTS: 29 MCA bifurcation aneurysms (11 ruptured, 18 unruptured) were occluded with coils in 26 patients. Occlusion was complete for 24 (82.8%) of the 29 aneurysms, incomplete for 3 (10.3%), and partial for 2 (6.9%) aneurysms. Procedural complications included thromboembolism in 6, a small nonocclusive thrombus formation in 1, and intraprocedural aneurysmal rupture in 1. All of symptomatic complications were thromboembolic events that occurred 3 patients with unruptured aneurysm and they discharged with moderate disability state. Follow-up angiograms were available on 16 patients with 18 aneurysms and 1 patient with an initial complete occlusion had a slight neck recanalization. CONCLUSION: Coiling of MCA bifurcation aneurysm could be achieved without treatment-induced neurologic deficit in 88.5% (23/26) of the patients while at the same time obtaining favorable anatomic results. Improvements in device technology and technique will certainly greatly increase the safety of coiling of MCA bifurcation aneurysm, widening its indications.
Key Words: Cerebral aneurysm, Middle cerebral artery bifurcation, Coiling, Thromboembolism

Introduction 


  
Coiling of cerebral aneurysms has developed into a safe and effective therapeutic alternative to open surgery. With increasing experience and development of appropriate devices, the indications for coiling of cerebral aneurysm have considerably widened. The recently published results of the International Subarachnoid Aneurysm Trial (ISAT) study have done much to make aneurysm coiling acceptable.11) There are still, however, some lesions, such as middle cerebral artery (MCA) bifurcation aneurysms, for which the ideal treatment is not obvious. As opposed to aneurysms of the posterior circulation, which are far less amenable to surgical clipping, MCA bifurcation aneurysms are easily accessible surgically and often have features that may be unfavorable to coiling. One of these features is an unfavorable dome-to-neck ratio, which can now be overcome with a combination of many options that includes the following: 1) new types of coils; 2) balloon remodeling; and 3) intracranial stents.8)9)20) Other obstacles such as incorporate neighboring arterial branches in the aneurysm base are difficult to overcome with current coiling technologies.8)9)20) We reviewed our technical results and clinical outcomes in 26 patients treated with coiling for the MCA bifurcation aneurysm over a 4-year period. 

Materials and Methods 

   During the past 4 years, 29 MCA bifurcation aneurysms in 26 patients were intended to be treated with detachable coils at our institution. Of these patients, 16 had subarachnoid hemorrhages (SAH). The bleeding source was a ruptured MCA bifurcation aneurysm in 11 patients and a ruptured aneurysm in a different location in 5 patients, respectively. 
   In our institution, surgical clipping is still the first option for treating MCA aneurysm without regard to rupture. Therefore, most of lesions treated by coils were selected based upon the vascular neurosurgeon's opinion that the patient was deemed a high risk for open surgical therapy such as old age or poor medical condition. Medical condition of high risk for open surgery included warfarinization or antiplatelet agent medication and underlying pulmonary or cardiac disease that had high risk for general anesthesia. Some of the patients treated by coils had been referred to our institution to be treated endovascularly as a first option and a few patients refused open surgery. Patients with a partially thrombosed fundus, or efferent vessels protruding from the aneurysm were not selected for coiling. Wide-necked aneurysms were treated with balloon assisted and/or two microcatheters technique. 
   We retrospectively reviewed the medical records, angiograms, and endovascular procedure reports of these 26 patients to determine the technical results, periprocedural complication rate, Hunt-Hess grade, and clinical outcome defined by the GOS. In this retrospective study, the analysis of angioarchitecture was performed by one neurosurgeon and one neuroradiologist on the basis of precise three dimensional angiograms. We confined aneurysm locations to first major bifurcation of MCA excluding M1 or M2 segment. Giant or Fusiform aneurysms were excluded from the analysis. 
   Coiling was performed as soon as possible after admission. All patients with a ruptured aneurysm were treated within 3 days after primary SAH. Most of patients with multiple aneurysms were treated with coiling simultaneously. All aneurysm coilings were performed with detachable coils by using a femoral approach. All patients were given an initial bolus of 5000 IU of heparin followed by the continuous infusion of 2500-3000 IU/h to maintain an activated clotting time (ACT) between 200 and 300 seconds. In accordance with our anticoagulation protocol, a 250mg intravenous bolus of acetylsalicylic acid (ASA) was administered to the patients for whom the aneurysm was not ruptured. Heparin was discontinued after embolization in the majority of patients. 
   Angiographic images were reviewed to determine the degree of obliteration of the aneurysm immediately postprocedure and at follow-up. A "complete" occlusion (100%) was considered when the aneurysm sac and neck were packed and there was no filling of the aneurysm sac by contrast material. A "incomplete" occlusion (95
~99%) was defined when the sac was occluded but a neck remnant either was thought to be present or was obviously present, and "partial" occlusion (<95%) considered when there was persistent opacification of a sac remnant. Coiling results were determined as a function of dome-to-neck ratio. Correlation of the occlusion rate with these factors was analyzed statistically by the Mann-Whitney U test. The statistical level of significance was set at P=0.05. 

Results 

Patient demographic data 
   Coiling was achieved for 29 aneurysms in 26 patients. These patients had an average age of 49 years (range, 23
~73 years) at presentation. Of these patients, 16 had SAH. The bleeding source was a ruptured MCA bifurcation aneurysm in 11 patients and a ruptured aneurysm in a different location in 5 patients, respectively. 
   In 4 (36.4%) of the 11 patients with SAH caused by an MCA bifurcation aneurysms, the SAH was given a Hunt and Hess grade of Ⅱ; in 2 (18.2%) patients, it was given a grade of Ⅲ; in 5 (45.5%) patients, it was given a grade of Ⅳ. Sixteen (55.2%) of the 26 patients had a single aneurysm, while 10 (38.5%) patients had multiple aneurysms. Three of the 10 patients with multiple aneurysms had both MCA bifurcation aneurysms 

Angioarchitecture 
   Aneurysms treated with coiling were confined at the first major bifurcation. On the basis of measurements performed on the three-dimensional angiograms, aneurysm maximum diameters ranged from 1.8 to 11.7 mm (mean, 6 mm±3 [standard deviation]), and aneurysm neck sizes ranged from 1.4 to 6.9 mm (mean, 3.2 mm±1.3 [standard deviation]). Dome-to-neck ratio of 12 (41.4%) aneurysms were >1.5. 

Clinical outcomes 
   For 11 patients with ruptured MCA bifurcation aneurysm, clinical outcomes (GOS) at discharge were good recovery (GR) in 6 patients; moderate disability (MD) and persistent vegetative state (PV) in each 1 (Table 1). Three died as a consequence of SAH (two died because of the primary brain damage caused by the hemorrhage, and the other one died as a consequence of vasospasm and subsequent cerebral ischemia). No patients with ruptured aneurysms died or handicapped of treatment-induced complications. 
   We excluded the 5 patients with different bleeding source among the 15 patients with unruptured MCA bifurcation aneurysm for analysis of clinical outcomes. 7 (70.0%) showed no change in baseline neurological function postembolization. The remaining three patients have undergone coiling-induced thromboembolic strokes in the ipsilateral MCA territory leading to a mild hemiparesis and discharged with MD state. 

Angiographic results 
   At the end of the procedure, occlusion was complete for 24 (82.8%) of the 29 aneurysms, incomplete for 3 (10.3%), and partial for 2 (6.9%) aneurysms. The occlusion rate immediately after coiling according to dome-to-neck ratio and mode of presentation had no significant difference (Table 2, 3). 
   Follow-up angiograms were available on 16 patients with 18 aneurysms. At follow-up, the angiographic results were nearly identical to that at discharge except one. At 13-month follow-up, 1 patient with an initial total occlusion had a slight contrast opacification at the aneurysm base without evidence for coil compaction or significant recanalization (Fig. 1). Retreatment was not considered necessary, and the patient were scheduled for further follow-up. 

Treatment-induced complications according to mode of presentation 
   Procedural complications included thromboembolic occlusion of a neighboring MCA branch (segment M2) in 6 patients, including 1 patient with protrusion of a coil loop bulging into the parent artery (segment M2)(Fig. 2). Abciximab (ReoPro; Centocor, Malvern, PA) was administered intraarterially through the coil delivery microcatheter (Excelsior; Boston/Target, Fremont, CA) with its distal tip inserted in the occluded artery adjacent to the thrombus in all 6 patients. Abciximab, diluted in saline to achieve a concentration of 0.2 mg/mL, was administered as a bolus of 4-10 mg over a period of 10-20 minutes, depending on how fast thrombus resolution was achieved while preventing injections exceeding 10 mg. Complete recanalization was achieved in 83.3% (5/6) of cases. 1 patient undergone failed thrombolysis and 2 of 5 recanalized patients had neurologic deficits (moderate disability) at discharge because of MCA infarction persisting in 3 patient (Fig. 3). 
   In 1 patient with an unruptured MCA bifurcation aneurysm, a small nonocclusive thrombus formation was observed at the neighboring M2 segment. Abciximab (0.25 mg/kg) was administered intravenously and then infused (10 μg/min). Serial angiograms showed complete resolution of the thrombus and no distal emboli were observed. The patient had no neurologic deficit.
   Intraprocedural aneurysmal rupture occurred in 1 patient with a ruptured MCA bifurcation aneurysm during third coil insertion. We identified extravasation of contrast agent angiographically. It was controlled easily with further coil embolization and a systemic protamine injection for heparin reversal. The patient was neurologically intact postprocedure and at follow-up (Table 4). 
   All of symptomatic complications were thromboembolic events and occurred in patients with unruptured aneurysm. The rate of symptomatic thromboembolism was 20.0% (three of 15 patients) for an unruptured. Other complications including nonocclusive thrombus formation and intraprocedural rupture were subclinical. Coiling was performed without symptomatic complications for 88.5% (23/26) of the treated patients. 

Discussion 

   MCA aneurysms account for 18% to 22% of all intracranial aneurysms with up to 85% of the lesions located at the main trunk division into M2 branches.5)17) The anatomy of MCA bifurcation aneurysms has often been noted to be unfavorable for endovascular coiling; the neck of MCA bifurcation aneurysms often seem to be wide and to incorporate an MCA branch.5)6)17) For these reasons, coiling of MCA bifurcation aneurysms remain controversial. Thus, there are few published papers considering the outcomes associated specifically with MCA bifurcation aneurysms after endovascular coiling.4)5)6)15)17) Although the results of ISAT revealed an absolute risk reduction of 6.9% for dependence favoring endovascular therapy, the ISAT did not, however, address the specific issue of patients with ruptured MCA aneurysm, who represented only 303 (14.1%) of the 2143 enrolled patients.11) The International Study of Unruptured Intracranial Aneurysms show that the surgical management of unruptured aneurysms yields a surprisingly poor clinical outcome with a combined morbidity and mortality rate of 13.7%.21) However, the number of MCA aneurysms that were endovascularly treated was low (n = 54) compared with the number of MCA aneurysms that were surgically treated (n = 650).21) 
   In 2005, Iijima et al reported the clinical and radiologic outcomes of endovascular treatment with coils of 149 MCA berry aneurysms.6) The authors noted coiling without treatment induced major neurologic deficits were achieved in 97% of patients with unruptured aneurysm and in 93% of patients with ruptured aneurysm. Morphologic findings revealed total obliteration of 77.2% of the aneurysms that were treated with coil placement. 
   However, Regli et al, after prospective study to delineate the most appropriate treatment option for unruptured MCA aneurysms, reported that despite major technical advances in imaging and in endovascular treatment of cerebral aneurysms, surgical clipping still is the most efficient treatment for unruptured MCA aneurysms at the beginning of the new millennium.17) 
   In our series of 29 coiled MCA bifurcation aneurysms, 82.8% of lesions were considered completely coiled at discharge. The difference in the rate of occlusion between ruptured and unruptured aneurysms was found to be not significant. A dome-to-neck ratio of aneurysm did not affect the rate of occlusion in our series. Aneurysms with wide necks remain difficult to treat surgically and, in the same way, both wide-necked and geometrically difficult aneurysms have remained a challenge for endovascular therapy. Currently, thanks to advances in materials and techniques, an endovascular treatment is possible in widenecked and fusiform aneurysms that could previously only be treated by surgical clip placement. The selective endovascular treatment of wide-necked aneurysms now involves a combination of many options that includes the following: 1) new types of coils; 2) balloon remodeling; and 3) intracranial stents.8)9)13)19)20) Above options enabled to coil wide-necked aneurysms without any difficulty in our series. Therefore, the occlusion rates for 29 aneurysms treated by coiling were higher than expected before. 
   In our consecutive series of 29 MCA bifurcation aneurysms, treatment-related adverse events with or without clinical modification were encountered in 8 patients (30.8%). The comparison of treatment-related adverse events from one series to another is difficult, because some totally silent events were not reported, like small clots close to the neck or partial deployment of 1 coil outside the limit of the aneurysms.12)18) In our series, the rate of aneurysm perforation during treatment was 3.4% and thromboembolic events were observed in 20.7% of cases. In the most recent and largest series, the rate of aneurysm perforation during endovascular treatment was 2.4
~4.5%, 3.6% and the rate of thromboembolic complications was 8.5%, 9.5%.2)12)14)16)18)23) The global rate of thromboembolism seems high in our series because of the fact that all of the adverse events, even with no clinical modifications, were reported. In our series, all of clinically relevant complications were thromboembolic events and occurred in 3 patients with unruptured aneurysm. And so, the treatment-induced mortality rate was 0% and the procedure-related morbidity rate was 11.5% (3 aneurysms). Most of the procedural complications are transient or reversible, and only a minority of them cause permanent morbidity and mortality.12)16)18) The reported procedural morbidity and mortality rates range between 3.7% and 9.1%, and between 1.5% and 7.8%, respectively.2)12)14)16)18)23) 
   In a multicenter retrospective study, Wirth et al analyzed the result of surgical treatment of 37 incidental MCA aneurysm and reported no mortalities and 8.1% morbidity.22) And Regli et al reported one minor complication from clipping of 32 unruptured MCA aneurysms, so overall morbidity was 2.5%.17) In our series, coiling of unruptured MCA aneurysms had 16.7% morbidity and no mortality. Compared with reported results of surgical clipping, our morbidity seems to be higher in coiling of unruptured MCA aneurysms, but there was no statistical significance (P=0.381). In ruptured series, Cho et al analyzed the result of surgical treatment of 50 ruptured MCA aneurysms and reported 2% of surgical mortality and 10% of surgical morbidity.1) We had just 9.1% of procedure-related morbidity with no mortality in coiling of ruptured MCA aneurysms without statistical significance between two studies(P=1.0). 
  
Anticoagulation management is of great importance in this setting. Because most procedural-related complications are of a thromboembolic nature, periprocedural anticoagulation therapy is of great importance.12)16)18) In the absence of contraindication, we use intravenous heparin therapy in all patients undergoing endovascular aneurysm treatment. In unruptured aneurysms, we also administer aspirin intravenously. There seems to be fundamental agreement among institutions about the usage of heparin during aneurysm embolization because reported anticoagulation strategies are similar.12)18) The different action of ASA might have an additive effect on coagulation to heparin alone in endovascular therapy.7)18) The presented data suggest that intraoperative ASA application is associated with a significant reduction in the rate of thromboembolic events without increasing in the rate or severity of intraoperative bleedings.7)18) 
   In our series, intraarterial thrombolysis with Abciximab was performed in all 6 patients with intra-procedural thromboembolic complication and resulted in recanalization in 5 of 6 cases. Abciximab has been demonstrated to be a safe and effective first-line treatment for patients with procedural thrombotic complications.3)10)12) In the study of Mounayer et al., the investigators administered an intraarterial bolus of Abciximab (4
~10 mg) to 13 patients suffering a procedural thrombotic complication and reported total recanalization of the thrombus in 92% of the treatments with no hemorrhagic complications.12) In our series



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