Korean Journal of Cerebrovascular Surgery 2009;11(4):167-173.
Published online December 1, 2009.
The Predisposing Causes Associated with a Poor Outcome for the Surgical Treatment of Ruptured Cerebral Aneurysms.
Yun, Jung Ho , Cho, Maeng Ki , Cho, Chun Sung
Department of Neurosurgery, Dankook University, College of Medicine, Cheonan, Korea. chomki@dankook.ac.kr
We analyzed the main causes leading to a poor outcome (severe disability, a vegetative state and death) following surgical treatment for ruptured intracerbral aneurysms. METHODS: Between January 1994 and December 2007, we maintained a retrospective database of 339 patients who underwent surgical clipping. The various causes we investigated were the technical problems during operation, the initial SAH or ICH, vasospasm, hydrocephalus and the post-operative medical complications. The clinical outcome was assessed according to the Glasgow Coma Scale (GOS). RESULTS: There were 263 cases of good outcomes (77.6%) and 76 cases of poor outcomes (22.4%). The three main causes of a poor outcome were 1) preoperative causes such as the direct insult of the initial SAH and ICH in 21 cases (27.6%), 2) intra-operative causes such as the technical problems during dissection and clipping of the aneurysm neck in 29 cases (38.2%) and 3) postoperative causes such as clinical vasospasm in 16 cases (21.1%). The mean follow-up period was 17.6 months (range : 2 months to 9 years). CONCLUSION: A meticulous neck dissection and complete obliteration of the aneurysm preserving parent arteries and perforators are the most effective and prime methods that surgeons can employ to reduce the rate of poor outcomes when performing ruptured aneurysm surgery.
Key Words: Microsurgery, Intracerebral aneurysm, Poor outcome


With significant advances in surgical microscopes, surgical instruments, operative techniques and neuro-anesthesia, surgical outcome of ruptured cerebral aneurysm have markedly improved. However, craniotomy and clipping techniques require further improvement. Prognostic factors for surgical treatment of ruptured cerebral aneurysm include operative techniques, surgical experience, intra-operative rupture of cerebral aneurysm, the patientsÕ age, clinical stage, and the size and site of the lesion.5)8)12)20)25) Additionally, there are numerous factors related to a poor outcome such as subarachnoid hemorrhage, neurological deficits due to direct brain injury from intracerebral hemorrhage, re-bleeding and vasospasm.14)24) Most previous studies have reported the ratio of patients with a poor outcome relative to the total number of patients without detailed analysis of clinical parameters. Therefore, this paper was attempted to analyze the etiologic factors which were related to a poor outcome and to provide the clinical data for improving surgical treatment outcome in patients with ruptured cerebral aneurysm.


Materials and Methods

We have enrolled 339 patients who had undergone surgical treatments by a senior author in our hospital during 13 years between January 1994 and December 2007. The mean ages were 54.7 years (range; 33~78 years). The male/female distribution was 78/195(ratio 1:2.5). We summarized patientÕs characteristics in our study (Table 1).

Initial main causes which influence the overall operative results and outcomes were assessed. Intra-operative problems were premature rupture before and during neck dissection, perforator injury, parent artery occlusion, incomplete clipping and retraction injury. Postoperative complications were vasospasm, hydrocephalus and medical problems. Postoperative neurological assessments on the basis of the follow-up study were carried out between 2 months in minimum and 9 years in maximum by telephone or interviews, and review of medical records. According to Glasgow Outcome Scale (GOS), the results are dichotomized as, 1) good outcome (good recovery and moderate disability) and 2) poor outcome (severe disability, persistent vegetative state and death)

We classified into 5 different categories about the causes of the poor outcome; 1) the problems of surgical manipulation, 2) the neurological deficits caused by the direct brain injury of initial SAH and intracerebral hemorrhage (ICH), 3) the prolonged cerebral ischemia by vasospasm, 4) hydrocephalus and 5) other medical complications. If two or more events are involved in the prognosis, the initial provoking one leading to the poor outcome was selected. Multivariate regression analysis was performed to analyze the effect of the following clinical factors on outcome: age, sex, H&H grade, Fisher grade, size of aneurysm (Table 2). Outcomes affected by various factors also were analyzed statistically by SPSS 12.0, and p value less than 0.05 was considered statistically significant.



Overall outcomes

Of a total of 339 patients, 263 (77.6%) were in the good outcome group, and 76(22.4%) were in the poor outcome group. In the good outcome group, 207 patients (61.1%) showed GOS 5, and 56 patients (16.5%) showed GOS 4. In the poor outcome group, 34 patients (10.0%) showed GOS 3, 6 patients (1.8%) showed GOS 2 and 36 patients (10.6%) showed GOS 1.

The poor outcome was shown in 76 patients (22.4%) out of 339 patients. There are various factors influencing outcome. The univariate analysis by chi-square test between poor outcomes and several factors was done. However, the correlation between age, gender, aneurysm size, aneurysm location, surgical timing and outcomes was not statistically significant. But the correlation between H&H grade and poor outcome was statistically significant (p=0.002). Of the 276 patients who were classified as having Hunt and Hess grade I, II or III at presentation, 230 (83.5%) were in the good outcome group. Of the 64 patients who were classified as having Hunt and Hess group IV or V at presentation, 33 (51.6%) were in the good outcome group.

Etiological factors in the poor outcome group

A total of 76 patients (22.4%) showed a poor outcome, and their etiological factors were categorized as problems in operation techniques, direct brain injury due to primary hemorrhage, vasospasm, chronic hydrocephalus and medical complications(Table 3).

1) Technical problem during operation

Of the 76 patients, 29 (38.2%) showed a poor outcome due to the problems in operative techniques. Of the 29 patients, occlusion of the parent artery and perforating branches along with the rupture of cerebral aneurysm was observed in 16 patients (21.1%), delayed hemorrhage due to incomplete clipping in 3 patients, temporary clipping of the parent artery for ¡Ã15 minutes in 4 patients, excessive brain retraction in 2 patients.

2) Direct effect of initial hemorrhage

Of the 76 patients, 21 (27.6%) showed a poor outcome due to initial poor grade of subarachnoid hemorrhage or intracerebral hemorrhage which was the second most common cause.

3) Post-operative causes

Sixteen patients (21.1%) showed a poor outcome due to vasospasm despite intensive triple-H therapy. Four patients (5.3%) showed a poor outcome due to chronic hydrocephalus, which required CSF shunt under the clinical diagnosis of shunt-dependent hydrocephalus without any definitive neurological improvement. Six patients (7.9%) showed a poor outcome due to medical complications including pneumonia, septicemia, adult respiratory distress syndrome, asphyxia and gastrointestinal hemorrhage.



The ultimate treatment goal of spontaneous subarachnoid hemorrhage is to minimize morbidity and mortality. Aneurysmal clipping which is currently the standard treatment for subarachnoid hemorrhage from cerebral aneurysm has been developed within the past 40 years. With significant advances in neurosurgical microsurgery, surgical instruments, neuro-anesthesia and intensive care unit monitoring, treatment outcome after surgery have remarkably improved. However, many cases of ruptured cerebral aneurysm still show a poor outcome, and the operation-related mortality rate has been reported to be between 3.7% and 7%.21)

Prognostic factors include the patientÕs age, Hunt and Hess grades, Fisher grades, size and site of the lesion, the timing of operation, experience of the surgeon, amount of bleeding, absence or presence of re-bleeding, vasospasm, chronic hydrocephalus and medical complications.6)7)8)12)14)17)20)23)24)26) In our study, treatment outcome after surgery were analyzed in terms of some of these factors. Certain factors were excluded in several studies about unruptured cerebral aneurysm. Moreover, since in severe cases of ruptured cerebral aneurysm, many factors are simultaneously associated with the lesion, analysis of the aforementioned factors alone may be inadequate to determine the exact factors related to a poor outcome. Therefore, we analyzed pre-existing causes related to a poor outcome along with the aforementioned factors.

It is known that the incidence of subarachnoid hemorrhage due to ruptured cerebral aneurysm becomes higher with increasing age.16)20) The Framingham study16) reported that aneurysmal subarachnoid hemorrhage occurred annually in 15 per 100,000 persons between their thirties and fifties, 37 per 100,000 persons in their sixties and 78 per 100,000 persons in their seventies, suggesting that itÕs annual incidence abruptly increases with increasing age. This study also indicated that the ratios of females to males were similar up to their thirties but increased thereafter with increasing age.5) In this study, the ratio of females to males was higher, but it was not significantly related to a poor outcome. Additionally, the mean age of the patients with a poor outcome was greater, but the difference was not statistically significant.

It has been indicated that the neurological status assessed by the Hunt and Hess grading system at presentation definitively affects prognosis.25) Seifert et al18) demonstrated that Hunt and Hess grade V patients showed a mortality rate of up to 90% irrespective of surgery and that there was direct brain damage from cerebral ischemia or subarachnoid hemorrhage. They also reported that there is a significant correlation between the amount of bleeding in subarachnoid hemorrhage and the frequency or severity of cerebral vasospasm. It has been indicated that if the amount of subarachnoid hemorrhage is ¡Ã3 mL, prognosis becomes poor due to a higher incidence of hydrocephalus or cerebral vasospasm.11)

The most important factor for a poor outcome was problems in surgical procedures such as the surgeonÕs surgical skill. Neurosurgeons require a great deal of skill in temporary clipping, dissection of the perforator and delicate pedicle clipping in both technical and psychological aspects.8) Lindert et al.23) have reported that intra-operative aneurysmal rupture mainly occurs during surgical procedures such as brain retraction, dissection and clipping and that newly developed neurological symptoms in 21% of the patients are due to incomplete clipping and obstruction of the perforators. They also reported that neurological deficits developed after surgery in 1.8% of all patients with ruptured cerebral aneurysm and that the incidence of intra-operative aneurysmal rupture was 3 times higher in the neurosurgeons who had performed ¡Â10 operations every year than in those who had done more. Intra-operative aneurysmal rupture has a direct influence on the patientÕs outcome. Thus, neurosurgeons should avoid intra-operative aneurysmal ruptures. In particular, since ¡Ã90% of the intra-operative ruptures occur during dissection of the perforators or pedicle clipping, the neurosurgeonÕs prudence and surgical skill greatly influence treatment outcome. Elliott et al.9) have indicated that intra-operative rupture of aneurysm is affected by various factors such as preoperative systolic blood pressure, Fisher grades, cerebral edema and intracerebral hemorrhage. Intra-operative rupture of aneurysm can be safely managed using temporary clipping or tentative clipping by skillful neurosurgeons.19) Fridriksson et al.3) have indicated that surgical complications by an inexperienced surgeon, especially intra-operative rupture of aneurysm lead to a poor outcome. In this study, the most frequent errors in surgical procedures were intra-operative rupture of aneurysm and occlusion of blood vessels surrounding the aneurysm. In cases where blood vessels with abundant blood flow such as the carotid artery are occluded, death frequently occurs due to postoperative ischemia or edema of the cerebral hemisphere. In particular, when blood vessels to the vital structures such as the thalamus are occluded, medical complications such as pneumonia frequently develop due to prolonged unconsciousness. It is conceivable that surgical inexperience and intra-operative technical errors such as rupture of aneurysm, inadvertent clipping, re-bleeding, occlusion of the parent artery and perforators, prolonged temporary clipping of the parent artery, direct injury to the neural tissue, duration and degree of brain retraction and postoperative intracranial hemorrhage can induce neurological deficits and thus influence outcome. In our study, of the 55 patients with a poor outcome, 14 (25.5%) showed subarachnoid hemorrhage or intracerebral hemorrhage from the initial rupture of aneurysm and re-bleeding.

Plum and Posner13) have shown that the causes of death from ruptured cerebral aneurysm are compression and displacement of the brain due to an abrupt increase in intracranial pressure and hematoma formation after the occurrence of subarachnoid hemorrhage. Intracerebral hemorrhage has been reported to be between 19.9% and 34.0%. It has been suggested that there is a significant correlation between the amount of bleeding and the size or site of hematoma.13)22) Tokuda et al.22) reported that the mortality rate of intracerebral hemorrhage associated with ruptured cerebral aneurysm was 47%. Locksley10) reported that intracerebral hemorrhage is the main cause of death within 72 hours of ruptured cerebral aneurysm. Kassel et al.7) reported that the probability of re-bleeding from ruptured cerebral aneurysm was between 20% and 30%. Based on the aforementioned results, it is thought that in patients with ruptured cerebral aneurysm, subarachnoid hemorrhage or intracerebral hemorrhage from the initial rupture of aneurysm and re-bleeding can affect the prognosis of aneurysm.

In this study, clinical vasospasm was defined as progression of unconsciousness and weakeness of extremity movement without abnormalities in brain CT, serum electrolytes or medical complications. It has been reported to be between 20 and 45%.14) Fisher et al2) have indicated that there is a significant correlation between the amount of bleeding and the incidence or severity of vasospasm. They have also found that early removal of hematoma can reduce the incidence of vasospasm with subsequent improvement of treatment outcome.11) In this study, there was a significant correlation between the final treatment outcome and Fisher grades representing the severity of vasospasm.

Hydrocephalus is usually induced 2 to 6 weeks after subarachnoid hemorrhage. Hydrocephalus after subarachnoid hemorrhage has been reported to be between 15% and 40%. Graff-Radford et al.4) have proposed that factors influencing the occurrence of communicating hydrocephalus after subarachnoid hemorrhage include old age, the status of consciousness at presentation, the size of hematoma at presentation, a previous history of hypertension and the site of aneurysm. In this study, of the 76 patients with a poor outcome, 4 patients (7.3%) were associated with chronic hydrocephalus.

It has been indicated that 75% of the total patients on the rehabilitation program after cerebrovascular accidents have experienced one or more medical complications, while 19% required extensive care due to the urgent status, most notably serious neurological deficits.15) Likewise, 7.9% of patients showed poor outcome in this report in which the problems on respiratory system such as postoperative pneumonia, adult respiratory distress syndrome, and sepsis were observed. Therefore, medical complications of the respiratory system should be aggressively managed because they can lead to a poor outcome



Taken together, factors influencing a poor outcome include (1) insufficient surgical procedure which consists of unsafe and incomplete dissection and incomplete clipping, (2) subarachnoid and intracerebral hemorrhage or re-bleeding and (3) clinical vasospasm. The last 2 factors may occur during the progression of ruptured cerebral aneurysm, which have not yet been successfully prevented. Therefore, neurosurgeons should perform safe microdissection and complete clipping of the aneurysm in order to achieve a good outcome.



1)              Chun YI, Ahn JS, Kim JH. Management outcomes of elderly patients with intracranial aneurysms. Kor J Cerebrovascular Disease 2:61-4, 2000

2)              Fisher CM, Kistler JP, Davis JM. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by CT scanning. Neurosurgery 6:1-9, 1980

3)              Fridriksson S, Saveland H, Jakobsson KE, Edner G, Zygmunt S, Brandt L, et al. Intraoperative complications in aneurysm surgery : a prospective national study. J Neurosurg 96:515-22, 2002

4)              Graff-radford NR, Torner J, Adams HP Jr, Kassell NF. Factors associated with hydrocephalus after subarachnoid hemorrhage. Arch Neuro 46:744-52, 1989

5)              Hunt WE, Hess RM. Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg 28:14-20, 1968

6)              Jeong JW, Kang SD, Kim JM. Clinical analysis operated aneurysms in elderly patients. J korean Neurosurg Soc 23:160-6, 1994

7)              Kassell NF, Torner JC, Haley EC Jr, Jane JA, Adams HP, Kongable GL. The international cooperative study on the timing of aneurysm surgery. Part 1 : Overall management results. J Neurosurg 73:18-36, 1990

8)              Kim JH, Hwang HS, Moon SM. Surgical results of anterior circulation aneurysm by inexperienced neurosurgeon. J korean Neurosurg Soc 33:40-3, 2003

9)              Le Roux PD, Elliott JP, Downey L, Newell DW, Grady MS, Mayberg MR, et al. Improved outcome after rupture of anterior circulation aneurysms : a retrospective 10-year review of 224 good-grade patients. J Neurosurg 83:394-402, 1995

10)            Locksley HB. Report on the cooperative study of intracranial aneurysms and subarachnoid hemorrhage. Section V. Part I. natural history of subarachnoid hemorrhage, intracranial aneurysms and A-V malformations. Based on 6368 cases in the cooperative study. J Neurosurg 25:219-39, 1966

11)            Mizukami M, Kawase T, Usami T, Tazawa T. Prevention of vasospasm by early operation with removal of subarachnoid blood. J Neurosurg 10:301-7, 1982

12)            Ogilvy CS, Growell RM. Carotid bifurcation aneurysms, in Apuzzo MLJ(ed) : Brain Surgery. New York : Churchill Livingstone, Vol 1, 1993, pp970-83

13)            Plum F, Posner JB. The diagnosis of stupor and coma, ed 3. Philadelphia : FA Daris, 1980, pp100-101, pp273-4

14)            Rabb CH, Tang G, Chin LS, Giannotta SL. A statistical analysis of factors related to symptomatic cerebral vasospasm. Acta Neurochir(Wien)127:27-31, 1994

15)            Roth EJ, Lovell L, Harvey RL, Heinemann AW, Semik P, Diaz S. Incidence and risk factors for medical complications during stroke rehabilitation. Stroke 32:523-9, 2001

16)            Sacco RL, Wolf PA, Bharucha NE, Meeks SL, Kannel WB, Charette LJ, et al. Subarachnoid hemorrhage : Natural history prognosis, and precursive factors in the Framingham Study. Neurology 34:847-54, 1984

17)            Saveland H, Hillman J, Brandt L, Edner G, Jakobsson KE, Algers G. Overall outcome in aneurysmal subarachnoid hemorrhage. A prospective study from neurosurgical units in Sweden du

Editorial Office
The Journal of Cerebrovascular and Endovascular Neurosurgery (JCEN), Department of Neurosurgery, Wonkwang University
School of Medicine and Hospital, 895, Muwang-ro, Iksan-si, Jeollabuk-do 54538, Korea
Tel: +82-2-2279-9560    Fax: +82-2-2279-9561    E-mail: editor.jcen@the-jcen.org                

Copyright © 2021 by Korean Society of Cerebrovascular Surgeons and Korean NeuroEndovascular Society. All rights reserved.

Developed in M2PI

Close layer
prev next