Korean Journal of Cerebrovascular Surgery 2005;7(4):309-316.
Published online December 1, 2005.
Results of Surgical and Endovascular Treatment of Middle Cerebral Artery Bifurcation Aneurysms: Clinical Research.
Chang, In Bok , Ahn, Sung Ki
Department of Neurosurgery, College of Medicine, Hallym University, Anyang, Korea. askns@hallym.ac.kr
Abstract
OBJECTIVE
Endovascular treatment as well as surgical treatment has become a treatment method for the management of the intracerebral aneurysms. The authors present the results of surgical and endovascular treatment of middle cerebral artery (MCA) bifurcation aneurysms. METHODS: From 1999 to 2005, 54 MCA bifurcation aneurysms were treated with surgical or endovascular methods at our hospital. Forty two patients had ruptured aneurysms and 12 had unruptured aneurysms. Of 54 aneurysms, 33 were treated with surgical clipping, 20 with Guglielmi detachable coil (GDC) embolization and 1 with cross over treatment. The medical, radiological and operation records were reviewed retrospectively. RESULTS: Of the 54 patients, 37 (68.5%) were female and 17 (31.5%) were male. In the surgically treated group, 22 (66.7%) experienced excellent or good outcomes (GOS 5 or 4), 8 (24.2%) had fair or poor outcomes (GOS 2 to 3), and 3 (9.1%) died (GOS 1). In the endovascularly treated group, 15 (75%) had excellent or good outcomes, 1 (5.0%) had fair outcomes (GOS 3), and 4 (20%) died. Symptomatic vasospasm revealed 9 (25.7%) in the surgically treated group, and 6 (30%) in the endovascularly treated group. Seven (20.5%) complications occurred from the surgical group, 3 (15%) from the endovascular group. On logistic regression analysis, there were no significant differences in GOS and vasospasm between surgically treated group and endovascularly treated group (p=0.788, 0.643, respectively). CONCLUSION: Endovascular treatment of MCA bifurcation aneurysms results in clinical outcome equal to the outcome of surgical treatment of MCA bifurcation aneurysms and it can be a good alternative method for MCA bifurcation aneurysms treatment.
Key Words: Middle cerebral artery aneurysm, Endovascular treatment, GDC embolization

Introduction


  
As middle cerebral artery (MCA) aneurysm has often small and wide neck and the base of it often incorporates with arterial branches, many neurosurgeons have used the surgical clipping for the management of aneurysms.4)23) In addition, the easy accessibility to the MCA bifurcation area makes neurosurgeons to use surgical treatment for MCA aneurysms.4)25) Although the total obliteration rate of the aneurysms by endovascular treatment is lower than that achieved by surgical clipping, endovascular treatment has been used to treat intracerebral aneurysms.21) Endovascular treatment with Guglielmi detachable coil (GDC) has been considered alternative strategy to prevent of aneurysm rupture in unruptured aneurysm as well as to eliminate the risk of aneurysm rebleeding in ruptured aneurysm.16)23)27) However, it has had tendency to use endovascular treatment in patients with intracranial aneurysms unclippable, in patients who have high potential for morbidity and/or mortality or in old aged patients.13)
   The authors wanted to show variables for predicting functional outcomes in patients who had MCA bifurcation aneurysms and to compare the results of surgical and endovascular treatment.

Materials and Methods

   From July 1999 to May 2005, 54 patients who had MCA bifurcation aneurysms were treated with surgical or endovascular methods at our hospital. Forty two patients had ruptured aneurysms and 12 had unruptured aneurysms. Of 54 aneurysms, 33 were treated with surgical clipping, 20 with endovascular treatment (GDC embolization) and 1 with cross over methods.
   Treatment of the aneurysms was either direct surgical clipping of the aneurysm neck or endovascular coil occlusion of aneurysm sac. Neurosurgeons and interventional neuroradiologist involved in planning the treatment strategy for the patients. Decision factors were high surgical risks, the presence of the major or perforating branches off the aneurysm, aneurysm shape, dome-to-neck ratio, and the patient's and family's wishes. In early period of this study, those patients who had high risks for surgery or unruptured aneurysms or old aged patients were treated with GDC embolization. After 2003, however, endovascular treatment was selected as the first choice for the management of aneurysms unless the vascular anatomy has clearly contraindication for endovascular treatment whether the aneurysms were ruptured or not.23)
   The medical, radiological, operation records and endovascular procedure records were reviewed retrospectively. Two patients with the aneurysms located on proximal or distal of MCA bifurcation were excluded. Follow-up angiography was performed in 33 patients 2 weeks and 3 or 6 month after clipping or endovascular treatment. The mean follow-up period of angiography was 4.7 months (from 2 weeks to 24 months).
   Vasospasm was documented by transcranial Doppler, conventional angiography and clinical symptom. If vasospasm had been confirmed, the patients were treated by triple-H therapy and/or intra-arterial papaverine injection. Papaverine injections were only used in 3 patients who had significant vasospasm identified with cerebral angiographies. Clinical outcome was assessed by using the Glasgow outcome scale (GOS)15) at the time of last follow up. The mean follow-up period was 18 months (from 1 month to 48 months). A GOS ≥4 was considered as good functional outcome.

1. Surgical clipping
  
Surgical treatments were performed within 72 hours after cerebral subarachnoid hemorrhage. In unruptured cases, the aneurysms were identified incidentally by the brain magnetic resonance image or the patients were transferred from medical departments. In all 33 patients, pterional approach was performed and decompressive craniectomy with neck clipping was in 8 patients (24.2%). During the operation, the blood clots of in the subarachnoid space or intracerebral hematomas were removed if possible. After surgical clipping of the neck of aneurysms, the blood flow of MCA vessels was checked by intraoperative Doppler ultrasound.

2. GDC embolization
  
Usually, GDC embolizations of the ruptured aneurysms were performed immediately after diagnostic cerebral angiography. In cases of the patients with unruptured aneurysms, however, GDC embolizations were performed after evaluation of other medical problems. The type of anesthesia was selected according to the patients' clinical state and cooperation. After 2004, we prefer general anesthesia to neuroleptic analgesia because general anesthesia has benefits consisting of better control of the patient's clinical condition, decreasing technical complication, increasing the quality of roadmapping.27) During the procedures, systemic anticoagulation with heparin was performed to decrease the rate of embolic complications.24) And after procedures, heparinization was used until 12 or 24 hours only in the patients who were suspected ischemic events. If there was not any contrast filling of the dome and neck of the aneurysms, embolization was considered to be complete. Incomplete embolization was defined as contrast filling was visible in the dome or neck of the aneurysms. Follow-up angiographies were obtained 2 weeks after the GDC embolization or before discharge. After discharge, follow-up angiographies were performed 6 and 12 months after the GDC embolization. Between the follow-up angiographies, plain skull x-ray films were obtained to evaluate coil mass changes. If residual neck was observed in the follow-up angiography, a 3-month follow-up angiography was planned. As incomplete embolization was significant, a second embolization was planned if possible.

3. Statistical analysis
  
The authors used descriptive statistics to show the distribution of demographic and clinical variables. To compare categorical variables, T-test, the Fisher exact test and chisquare test were applied. Logistic regression analysis was performed by using the response variables to compare clinical outcomes and treatment effect of two groups (Table 1). Multivariate logistic regression analysis was performed by using a model that included variables that were presence of vasospasm, H-H grade, Fisher grade, presence of hydrocephalus, application of craniectomy, and application of lumbar drainage. Level of significance was established at p<0.05.

Results

1. Overall results
  
Of 54 patients, 37 were female and 17 were male. The mean age of patients was 56.4 (34 years to 80 years). The mean size of sac of aneurysms was 5.81±2.33 (standard deviation, SD) and the size of neck was 3.50±1.12 (SD). There were 42 ruptured aneurysms and 12 unruptured aneurysms. Multiple aneurysms were identified in 16 patients (29.6%). Small sized (3 mm≤) aneurysms were 5 (9.3%), medium sized (3-10 mm) aneurysms were 46 (85.1%), and large sized (10 mm≥) aneurysms were 3 (5.6%)(Table 2). Aneurysms with small neck (≤4 mm) were 45 (83%), widenecked (>4 mm) aneurysms were 9 (17%). Thirty nine patients (72.2%) experienced excellent or good outcomes (GOS 5 or 4), 8(14.8%) had fair or poor outcomes (GOS 3 or 2), and 7 (13.0%) were dead (GOS 1)(Table 3). In the patients with ruptured aneurysms, 28 of 42 (66.6%) had excellent or good outcomes and 7 (16.7%) had fair or poor outcomes, and 7 (16.7%) were dead (GOS 1). Of 12 patients with unruptured aneurysms, 10 (83.3%) revealed excellent outcomes (GOS 5), 2 (16.7%) had fair outcomes. Residual necks were seen in 3 cases, 2 were due to incomplete clipping of aneurysm, 1 was due to incomplete GDC embolization. In univariate logistic regression analysis, treatment modality and gender of patients were not statistically significant factors of out-comes. There were significant correlations with outcomes in Hunt and Hess grade (p=0.033), Fisher grade (p=0.034), and symptomatic vasospasm (p<0.001). In multivariate logistic regression analysis, only vasospasm was significantly correlated with poor outcome(Table 4). There were no significant differences in GOS and vasospasm between surgically treated group and endovascularly treated group (p=0.788, 0.643, respectively).

2. Surgical group
  
The surgical group consisted of 33 patients, of whom 9 were men and 24 were women. Three patients (9.1%) were in H-H grade I, 15 (45.5%) in grade II, 4 (12.1%) in grade III, 8 (24.2%) in grade IV, and 3 (9.1%) in grade V. Four (12.1%) patients were in Fisher grade I, 7 (21.2%) in grade II, 10 (30.3%) in grade III, and 12 (36.4%) in grade IV. There were 11 (33.3%) in H-H grade IV and V, and 22 (66.7%) in grade I to III. Also, there were 23 (67.6 %) in Fisher grade III to IV, and 11 (32.4%) in grade I to II. The mean age of the patients was 56.4 years with a range of 41 years to 74 years. The mean size of aneurysms sac was 5.68±2.28 (SD). The mean size of neck was 3.55±1.12 (SD). Twenty three (69.7%) patients revealed excellent or good outcomes (GOS 4 to 5), 7 (21.2%) revealed fair or poor outcomes (GOS 2 to 3), and 3 (9.1%) were dead(Table 5). Of 3 patients, one patient was dead because of rebleeding and two patients due to vasospasm after surgical clipping. Eight of 22 patients who revealed Fisher grade III or IV underwent decompressive craniectomy with neck clipping, 3 of them had good recovery and 2 were dead. Nine of 12 patients with Fisher grade IV had intracerebral hematoma (ICH) and 3 had intraventricular hemorrhage(IVH). Five of 9 patients underwent decompressive craniectomy with hematoma removal. One of 3 patients had IVH underwent extraventricular drainage without craniectomy. Decompressive craniectomy was correlated with poor outcome in univariate logistic regression analysis (p=0.008), but there was not statistical significance in multivariate logistic regression analysis(p=0.708). Residual neck was seen in one case, after clipping of the large aneurysm (12 mm).

3. Endovascular group
  
The endovascular group consisted of 20 patients, of whom 8 were men and 12 were women. Seven patients (35%) were in H-H grade I, 1 (5%) in grade II, 5 (25%) in grade III, 2 (10%) in grade IV, and 5 (25%) in grade V. Eight (40%) patients were in Fisher grade I, 4 (20%) in grade II, 5 (25%) in grade III, and 3 (15%) in grade IV. There were 5 (25%) in H-H grade IV and V, and 15 (75%) in grade I to III. There were 8 (40%) in Fisher grade III to IV, and 12 (60%) in grade I to II. The mean age of the patients was 56.2 years with a range of 34 years to 80years. The mean size of aneurysms sac was 6.0±2.5 (SD) and the mean size of neck was 3.45±1.18 (SD). Fifteen patients (75%) revealed excellent or good out-comes (GOS 4 to 5), 1 (5%) revealed poor outcomes (GOS 2 to 3), and 4 (20%) were dead(Table 4). Causes of death were vasospam in 3 patients and acute myocardial infarction in 1 patient. Residual neck was seen in one case, due to incomplete embolization. Second embolization was not performed because there was only mild neck filling. There were 2 patients with Fisher grade IV. One had ICH and the other had IVH. The patient who had ICH was dead in spite of decompressive craniectomy.

4. Cross over treatment
  
There was one patient who underwent surgical clipping with GDC embolization (Fig. 1). As a small vessel on the aneurysm wall was identified in the operative field and it was impossible to dissect the vessel from the aneurysm wall, incomplete surgical clipping was performed. The patients was treated with GDC embolization one month later and discharged with good result.

5. Vasospasm, Hydrocephalus and Complications
  
Vasospasm revealed 9 patients (31%) in surgical treatment group, 5 (41.7%) in endovascular treatment group and 1 (100%) in the crossover treatment in ruptured aneurysms cases. In unruptured aneurysms cases, no vasospasm was seen in surgical group and one patient (12.5%) revealed vasospasm in GDC embolization group (Table 6).
   Hydrocephalus developed in 8 patients (24%) in surgical treatment group and 4 of 8 patients underwent ventriculoperitoneal (V-P) shunt. There were two patients (10%) with hydrocephalus in endovascular group and they were discharged without V-P shunt. Hydrocephalus was not correlated with clinical outcome in univariate and multivariate logistic regression analysis (p=0.189, 0.583, respectively).
   Seven (20.5%) complications consisting of 2 vascular stenoses, 2 subdural hygromas, 2 minimal epidural hematomas, and 1 infection occurred in the surgical group (Table 7). There were 3 (15%) complications which were 2 embolic strokes and 1 intraoperative bleeding in the endovascular group.

Discussion

   Although many treatment methods consisting of detachable balloons,1)9) pushable microcoils2)14) and liquid embolic agents18) to obliterate intracranial aneurysms have developed, the use of these method has limitations. After reporting the use of the GDC to treat intracranial aneurysms by Guglielmi in 1991, endovascular treatment with GDC has been considered alternative strategy to ruptured aneurysms as well as unruptured aneurysms.11)16)23)27)
   Although the total obliteration rate of the aneurysms by endovascular treatment is lower than that achieved by surgical clipping, complete aneurysmal thrombosis with endovascular treatment can be achieved in 85% of aneurysms with smaller neck than 4 mm, but in only 15% of aneurysms with a neck of 4 mm or greater.8) According to Regli's report, of patients with unruptured MCA aneurysms for which endovascular therapy was suitable, only 6% could be occluded using GDC system;in 32% the attempt at GDC treatment failed and in 62% anatomical contraindications for GDC embolization were founded.23) In his study, the major cause of failure was a wide-necked aneurysm that had not been demonstrated on pretreatment angiogram.
   In our study, there were 6 patients who had definitely incorporated artery with aneurysm sac. Three of them were treated with surgical clipping and 3 with GDC embolization (Fig. 2). One of 6 was seen residual neck and all 6 patients revealed good results. There were 30 (56%) patients who had wide necked aneurysms (>4 mm) or dome to neck ratio of 1.5 or less (≤1.5). Of 30 patients, 10 were treated with GDC embolization (Fig. 3). Eight of 10 patients got good clinical outcomes and 2 were dead due to ischemic complication and acute myocardial infarction, respectively. One of 10 patients showed neck filling in follow-up angiographies. Although there were many wide-necked aneurysms, the authors could get good results with GDC embolization, which were ascribed to three-dimensional (3D) angiography and improvement of coil products and development of various coiling techniques.
   There is no consensus about the criteria for choosing between endovascular treatment and surgical clipping as a treatment for intracranial aneurysms. The factors predicting outcome of surgical clipping are dome size, aneurysm location and patients' age.23) There are many factors contributing to poor outcomes of endovascular treatment;1) wide neck (>4 mm), 2) dome/neck ratio≤1.5, 3) inadequate endovascular access, 4) unstable intraluminal thrombosis, and 5) arterial branch origin incorporated with aneurysm neck.23) Of these factors, wide neck and incorporated artery could be seen frequently in MCA aneurysms.4)23) These findings as well as easy accessibility to the MCA bifurcation area make neurosurgeons use the surgical clipping. Actually endovascular treatment for MCA aneurysms are used lesser frequent than for other site aneurysms, it has been preferentially used in posterior circulation and in the anterior communicating artery within anterior circulation.3)16)
   In the early phase of our study, the first choice of the management of intracranial aneurysms was microsurgical clipping. After introducing endovascular treatment in 1999 at our hospital, GDC embolization has been increased each year. Obtaining of more experience, good outcomes, public information, and endovascular treatment has become primary treatment recommendation for the management of intracranial aneurysms in the beginning of 2004. There were no differences of clinical outcomes and vasospasms between endovascular treatment group and surgical treatment group in our study.
  
Cerebral vasospasm which leads to poor clinical outcomes or to death occurs in 22% to 73% of patients in surgically treated group, and 17% to 37.7% in endovascularly treated group.10)21)22)28). Several factors consisting of age, clinical state, and hyperglycemia have been known to have association with cerebral vasospasm.3)21) Also, the amount of the SAH was confirmed as independent prognostic factor of cerebral vasospasm.20) Presence of erythrocytes in cerebrospinal fluid is essential developing cerebral vasospasm in experimental study7) Removal of cisternal blood clots in early operation for ruptured aneurysms has been useful to decrease the occurrence of cerebral vasospasm.6)10) Cisternal clots, however, cannot be removed in GDC embolization. Nevertheless, there are some reports that symptomatic vasospasm is not associated with the modality of treatment (surgery or GDC embolizatiom).3)4) According to the Yalamanchili's report, the occurrence rates of vasospasm were 73% in surgical treatment group and 22% in GDC embolization group.
   In our study, vasospasm revealed 9 (31%) in surgical treatment group, 5 (41.7%) in endovascular treatment group in ruptured aneurysms cases. Although the rate of vasospasm of endovascular group was higher than that of surgical group, there was no significant statistical difference between two groups (p=0.643). We performed the lumbar drainage for 3-5 days to remove blood clots, but there was no significant effect of decreasing vasospasm. The incidence of vasospasm of our study is similar with that reported previous study. Severe complications were rebleeding and MCA artery obstructions in surgical group. In endovascular group, there were embolic stroke and rebleeding after procedures. These cases were ascribed to wide-necked or incorporated artery with aneurysmal sac. However, the advances of techniques (two microcatheters system, balloon assisted embolization), of coil products, and of intracranial stents will decrease these severe complications,5)6)12)17)19) and increase use of endovascular treatment.

Conclusion

   Although 56% patients revealed wide necked aneurysm or incorporated artery with aneurysm sac, the authors could get good results of 80%. Hunt and Hess grade, Fisher grade, and vasospasm were closely predictive of outcome in univariate logistic regression analysis. Vasospasm was significantly correlated with poor outcome in multivariate logistic regression analysis. There were no significant differences in GOS and vasospasm between surgically treated group and endovascularly treated group. Endovascular treatment of MCA bifurcation aneurysms results in clinical outcome equal to the outcome of surgical treatment of MCA bifurcation aneurysms statistically and we think it can be a good



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