Korean Journal of Cerebrovascular Surgery 2005;7(2):130-134.
Published online June 1, 2005.
Comparative Study of Cerebral Vasospasm between Endovascular Treatment and Conventional Surgery of Acutely Ruptured Aneurysms: Clinical Study.
Kim, Jin Sung , Yoo, Seung Hoon , Kim, Seong Rim , Kim, Sang Don , Park, Ik Seong , Baik, Min Woo
Department of Neurosurgery, Holy Family Hospital, Catholic University of Korea, Bucheon, Korea. nsispark@chollian.net
OBJECT: Generally, it seems like that the incidence of vasospasm of vasospasm in endovascular coil embolization is higher than clipping in aneurysmal subarachnoid hemorrhage. But endovascular coil embolization in our study group was not associated with higher incidence of symptomatic vasospasm than direct clipping and we made an analysis of that cause. METHODS: The authors reviewed 220 patients with aneurysmal subarachnoid hemorrhage who had been treated with either neck clipping or coil embolization by a single surgeon between January 1997 and December 2002. Poor initial grade (Hunt & Hess grade IV & V) patients were excluded. Finally 171 patients were enrolled in this study. 126 patients(74%) underwent direct surgical clipping and 45 patients (26%) underwent endovascular treatments of their aneurysms. RESULTS: Overall symptomatic vasospasm occurred in 32 (19%) patients, 4 of 45 patients (9%) were coiling group and 28 of 126 (22%) were surgically treated group. There was no difference between two groups in age, initial Hunt & Hess grade, Glasgow coma scale, operation time, treatment initiation time, patient's medical status. CONCLUSIONS: Patients who underwent coil embolization were not more likely to suffer from symptomatic vasospasm than aneurysm neck clipping in better clinical grades (Hunt & Hess grade of I to III) patients in our institute.
Key Words: Subarachnoid hemorrhage, Vasospasm, Endovascular embolization, Aneurysm clipping


Cerebral vasospasm after subarachnoid hemorrhage(SAH) due to aneurysm rupture remains the leading causes of delayed morbidity and mortality despite the improvements in management of aneurysmal SAH.2)15) It has been known that the most powerful prognostic factors for vasospasm are the amount of blood on the computerized tomography scan obtained at hospital admission,1)4)7)8)9)17)25) a poor clinical grade,27) and loss of consciousness at presentation.12) Early surgical intervention protects patients from subsequent aneurysm bleeding and allows aggressive treatment of cerebral vasospasm. Removal of the blood clots and irrigation of the cisterns by conventional aneurysm neck clipping surgery have been reported to produce some success in preventing cerebral vasospasm.13)33)
   Although craniotomy for aneurysmal clipping is the standard and definitive method of treating saccular aneurysms, endovascular aneurysm occlusion by development of coils provides an effective alternative by excluding the aneurysm from the cerebral circulation.22)34) But this procedure could not remove subarachnoid hemorrhage. So it seemed that vasospasm would occur more frequently in endovascularly treated patients. However, in some recent reports, this method has been shown to diminish the frequency and severity of vasospasm in compare with open surgery.31) The incidence of vasospasm between surgical clipping group and endovascular treatment group is seems to have many different conflicting results according to neurosurgical institute.10)19)28)31)
   The objective of the present study was to analyze the influence of the treatment modality applied(early surgery versus early endovascular therapy) on the severity of cerebral vasospasm in a population of patients with SAH by aneurysm rupture managed by a single neurosurgeon in one institute. Both therapeutic groups were subjected to the same pre-, peri-, and postoperative monitoring and treatment protocol by the same staff of neurosurgeons.

Clinical Materials and Methods

   We retrospectively evaluated all patients admitted to the neurosurgical intensive care unit(NSICU) with the diagnosis of SAH from January 1997 to December 2002. All the 202 patients have been treated with either conventional surgery or endovascular coil embolization respectively by one surgeon along the protocol. The following cases were excluded from this study;the patients with in H&H grade IV, initial GCS score below 7, old patients above 79 years old, fusiform, traumatic, and mycotic aneurysm. It is usually known that the incidence of symptomatic vasospasm in poor H&H grade is usually high regardless of treatment modality, so we excluded the patients in H&H grade IV, V.6)8)10)17)26)
   The patient population consisted of 69 men and 102 women whose ages range from 20 to 79(average age is 59). Of the aneurysm treated, 144 were in the anterior and 27 were in the posterior circulation(Table 1). 126 patients(74 percent) underwent surgical clipping and 45 patients(26 percent) underwent endovascular treatments of their aneurysms.
   Factors considered during the decision-making process in the treatment of aneurysm included dome/neck ratio of the aneurysm, location of aneurysm, H&H grade and surgical or endovascular accessibility.
   All patients were treated with modest hypervolemic therapy and intravenous nimodipine for prophylaxis of cerebral vasospasm. More aggressive triple-H therapy(hypervolemia, hypertension, hemodilution) was instituted in patients with symptomatic vasospasm. 
   Diagnosis of symptomatic vasospasm was based on the following criteria:a) clinical deterioration in the patient's neurologic condition between 3 and 14 days after SAH, including insidious onset of confusion, or decline in level of consciousness or focal deficits that may fluctuate in severity, b) exclusion of structural causes of neurologic worsening by appropriate investigations including brain CT scanning (Rebleeding, hydrocephalus, intracranial hemorrhage);and c) absence of other identifiable causes of neurologic worsening such as serum electrolyte or glucose disturbances, hypoxia, hypercapnia, or seizures. Transcranial Doppler (TCD, EME, Nicolep, Germany) ultrasound monitoring was performed to diagnose the presence of vasospasm, it was typically followed by MR angiography or catheter angiography for diagnostic confirmation.30)
   Precision in the diagnosis of vasospasm by TCD may be enhanced by measurements of the so-called Lindegaard ratio.20)

1. Statistical Analysis
We compared continuous variables by using Student's t-tests and compared categorical variables by using Chi-Square tests. Comparisons between endovascular and clipping groups were made according to confidence intervals of 95%. All statistical tests were two-sided and all analyses were performed using statistical software(SPSS for Windows, 11.0 standard version). A probability value less than 0.05 was considered statistically significant.
   We found that the proportional odds model fit these data adequately. The odds ratio(OR) for the treatment effect is interpreted as the relative odds for incidence of vasospasm in patients treated with surgery rather than endovascular embolization. Consequently, an OR significantly lower than 1 would indicate that vasospasm was less likely to occur after surgery, where as an OR significantly greater than 1 would indicate that vasospasm was less likely to occur after endovascular treatment.


   A total of 220 patients with aneurysmal SAH were enrolled. 102 female(59%) and 69 male(41%) patients had a mean age of 51 years(20 to 79 year, average:51). Of the aneurysm treated, 144 were in the anterior and 27 were in the posterior circulation(Table 1).
   126 patients(74%) underwent surgical clipping and 45(26%) underwent endovascular treatments of their aneurysms. The ruptured aneurysm was located in the anterior circulation in 144(84%) and 27 patients(16%) in the posterior circulation. 
   Baseline information for both treatment groups is displayed in Table 2. There were no definite differences in patient age, sex, or history of hypertension. The clinical grade at presentation was not different between two groups(Table 2). Aneurysms which were located in anterior circulation were predominantly treated with conventional surgery(78% of all anterior circulation aneurysms), whereas almost aneurysm of posterior circulation were treated with coil emblization.
   In this study, the incidence of symptomatic cerebral vasospasm did not differ between two groups(Table 3). Logistic regression analyses controlling for patient age, Hunt-Hess grade, Fisher group, day of treatment, presense of early hydrocephalus, and aneurysm location are shown on Table 4. Symptomatic vasospasm occurred in 19% of patients overall. Global neurological deficits due to vasospasm were present in 4% of coiling group and 16% in clipping group.


   Despite the introduction of nimodipine and the use of induced 3-H therapy, symptomatic vasospasm still remains the major cause of morbidity and mortality in patients with SAH.2)3)29) In contrast with open surgery, removal of subarachnoid clot is not possible during endovascular treatment.18) Early cisternal clot removal decreases cerebral vasospasm in some animals studies, presumably by reducing the level of putative spasmogens.35) This has been proven in experiments conducted in primates.11)23) Despite this, the largest clinical series reports that vasospasm remains the most significant cause of death and disability even in patients undergoing early surgery.16)21)24) Besides this, there is no clear evidence that early surgery significantly reduces the severity of vasospasm. Some reports surgery may aggravate vasospasm becauase of extensive retraction of the brain or direct manipulation of intracranial arteries.25)

1. Review of previous series
According to other literatures, the influence of treatment selection on the incidence and clinical sequelae of cerebral vasospasm following rupture of an intracranial aneurysm has been estimated.1)3)15) Murayama, et al., reviewed the cases of 69 patients treated with endovascular occlusion after aneurysmal SAH.22) The 23% incidence of symptomatic vasospasm in this series compares favorably with that found in conventional surgical series of patients with acute aneurysmal SAH. In spite of the fact that this study focused only on patients with Hunt & Hess Grades I to III, the results compare favorably with surgical and natural history outcomes in patients with similar neurological grades. 
Charpentier, et al., made a multivariate analysis of predictors of cerebral vasospasm on their population of 244 patients with aneurysmal SAH.5) Nearly 40% of all patients were treated surgically, others by endovascular occlusion. The two treatment groups were comparable in baseline characteristics, with the exception of aneurysm location (aneurysms of the posterior preferentially treated with endovascular coil occlusion and aneurysms of the middle cerebral artery were predonminantly treated with craniotomy and clipping). The incidence of symptomatic vasospasm was 17% in the endovascular treatment group and 22% in the craniotomy group, but the difference did not reach statistical significance(p=0.37).
   Gruber, et al., reported that the infarction rate was higher with endovascular treatment versus surgery(37.7 versus 21.6%), as a result of a skewed Fisher Grade 4 infarction pattern in the endovascular treatment group versus the surgery treatment group(66.7 versus 24.5%).10) When patients with Fisher Grade 4 and WFNS grade V were excluded from the analysis, however, the difference between the two treatment groups lost statistical significance. 

2. Incidence of symptomatic vasospasm
In the International Cooperative Study on the Timing of Aneurysm Surgery, 27% of the patients treated surgically developed delayed cerebral ischemia.16) And the incidence of symptomatic vasospasm after conventional craniotomy and clipping varies from 20 to 50%.4)6)7) This variation is probably caused by the difference in the management of patients after SAH:timing of surgery, timing and degree of the 3H therapy, use of cisternal drainage, and use of calcium channel blockers. This clinical study expounds our experience in the treatment of more than 200 patients with aneurysmal SAH over a seven-year period. Compared to the result of previously reported series, the morbidity and mortality rates from SAH and cerebral vasospasm were relatively low. 
In this analysis, the incidence of symptomatic cerebral vasospasm did not reach significance between patients treated surgically and those treated endovascularly(Table 3). 

3. Analysis of the results
Our results show that the incidence of symptomatic vasospasm in the patients treated endovascularly is not higher than in patients treated surgically. Also the patients in this group had not a higher rate of global deficit caused by vasospasm. These findings correspond to those of earlier reports, suggesting an insignificant incidence of symptomatic vasospasm after endovascular treatment of ruptured aneurysms when compared with surgical clipping group.5)22) These results may be due to early aggressive treatment against vasospasm after early obliteration of the aneurysm and relatively lower incidence of vasospasm comparing the previous reports.
   Although the patients with posterior circulation aneurysms were preferentially treated with endovascular coil occlusion, our analysis controlled these baseline differences(aneursysm location, acute hydrocephalus, age, etc), negating their role as potential confounders. Moreover, there is no definitive clue that aneurysm location influences the risk of symptomatic vasospasm;aneurysms in the anterior circulation were associated with a higher risk of symptomatic vasospasm in one series,26) but no in others.32)
   But the amount of blood on the admission CT scan(Fisher grade) was not quantified in all patients and was not included in this analysis. 


   In this consecutive series of patients with aneurysmal SAH, the occurrence of symptomatic vasospasm was not higher in the group of endovascular treatment than that of surgical treatment. Therefore, it is supposed that cerebral vasospasm after aneurysmal SAH may be not associated with treatment procedures.


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