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Management of intracranial aneurysms: factors that influence clinical grade and surgical outcome. (Original Article).

Background: We report the experience in managing intracranial aneurysms at our medical center.

Methods: We retrospectively analyzed 297 intracranial aneurysms managed during a 6-year period. Risk factors were analyzed with respect to their influence on Outcome after surgery as measured by Glasgow Outcome Scale score.

Results: Fifty-eight patients had multiple aneurysms. Of all aneurysms, 83% were in the anterior circulation, 37% were unruptured, and 59% were larger than 10 mm in size. Good outcome was achieved in 75% of patients, and another 16% had fair outcomes. The mortality rate was 4%, and significant morbidity occurred in 5% of patients. Significant indicators of poor outcome were worsened clinical grade, posterior aneurysm location, and large aneurysm size.

Conclusion: Hypertensive patients, older patients, and patients with posterior circulation aneurysms had poorer neurologic status, which significantly influenced outcome. Larger aneurysms and vertebrobasilar aneurysms were associated with poor outcomes.

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When adjusted for age and sex, the prevalence of intracranial aneurysms has been reported to be about 83 in 100,000 people in the general population, (1) with a frequency of 0.2 to 9.9% (2) This suggests that 10 to 15 million people in the United States have aneurysms, and it is estimated that aneurysms are the cause of death or severe disability in 28,000 people annually. (3) Early diagnosis and surgery resulting in a good neurologic condition of the patient after subarachnoid hemorrhage (SAH) are generally recommended to obtain a good neurologic outcome. (4,5) Apart from the clinical condition of the patient, other characteristics of aneurysms have a significant influence on outcome, both independently and through their association with poor neurologic grade. These factors include preoperative smoking, alcohol intake, hypertension, patient age, size and location of the aneurysm, and occurrence of intraoperative rupture. A retrospective study was performed to review the association between these variables an d their influence on neurologic outcome.

Patients and Methods

During a 6-year period, 233 operations were performed in 210 patients with a total of 290 aneurysms. A review of hospital charts and other records, such as angiography reports and notes on the operation, was performed to obtain details about these patients and their aneurysms, including patient demographics. The factors included were age, sex, aneurysm characteristics (size, location, and existence of other aneurysms), number of days from onset of symptoms until presentation at the hospital, clinical grade (expressed according to the Hunt and Hess grading system), Glasgow Coma Scale (GCS) score, number of days until surgery after the onset of symptoms, presence of hydrocephalus, spasm occurrence, intraoperative rupture of the aneurysm, application of a temporary clip, and outcome after 6 months as defined by Glasgow Outcome Scale (GOS) score. Each patient's history of hypertension, cigarette smoking, and alcohol intake also was noted.

Statistical Analysis

Statistical analysis was performed with the use of both univariate and multivariate statistical methods (Fisher's exact test, Spearman rank correlation, Student's t test, linear regression analysis, and forward stepwise regression analysis). Significance was set at P < 0.05.

Results

Age and Sex

The average age of the patients was 48.3 [+ or -] 12 years (range,11-75 yr). Fifty-four percent of the patients were younger than 50 years old, and 30% of the patients were 60 to 69 years of age. Age had no significant influence on the clinical grade of the patient; however, outcome was negatively affected as patient age increased (P < 0.02). Eighty-four percent of patients younger than 50 years of age had good outcomes, whereas 66% of those older than 50 years of age had good outcomes. There was also a significant difference in the morbidity and mortality rates between the two age groups (P < 0.004) (Fig. 1). Two-thirds of the patients were female, and they tended to be younger than male patients. Males tended to present in worse clinical grade than females (Fig. 2). Sixty-five percent of females were in Grades I and II, and 49% of males were in comparable grades. Outcome did not differ significantly by sex.

Postictal Day of Admission and Operation

Eighty percent of patients with SAH were admitted within the first 2 postictal days, and another 10% were admitted within the first week after SAH. The day of admission, however, had no relationship to outcome. With regard to the timing of surgery, 74 operations were performed within the first 3 days of SAH, and 48 operations were performed between the 4th and 14th days after SAH. There was no statistically significant difference in outcome when these two groups were compared (P 0.1). Sixty-five percent of patients who underwent surgery early (ie, surgery performed within the first 3 days after SAH) had good outcomes, as opposed to 79% in the group that had surgery between the 4th and the 14th days after SAH. Seven percent of the first group died, and the mortality rate in the second group was 4%.

Location of the Aneurysm

More than 80% of the aneurysms were located on an anterior circulation artery, and of these, 48% were on the internal carotid artery and 33% were on the posterior communicating artery. Twenty-nine percent of the aneurysms were located on the anterior cerebral artery, and 23% were located on the middle cerebral artery. Fifty-six percent of the posterior circulation aneurysms were on the basilar artery. The location of the aneurysm had a significant relationship with both clinical grade and outcome. Patients with SAH due to a vertebrobasilar aneurysm had a poorer Hunt and Hess grade than did those with aneurysms in other locations (P < 0.02). Eighty-four percent of patients with anterior circulation aneurysms, compared with 51% of those with posterior circulation aneurysms, had good outcomes (P < 0.001). The mortality rate associated with posterior circulation aneurysms was 7.6%, compared with 3% for patients with carotid circulation aneurysms. Patients with posterior circulation aneurysms had worse outcomes, which were reflected in both mortality rate and morbidity rate (P < 0.02), compared with patients with anterior circulation aneurysms (Fig. 3). Nearly 80% of patients with vertebrobasilar aneurysms had good recoveries or recovered with moderate disabilities.

Size of Aneurysm

The average aneurysm size was 11.3 [+ or -] 6.4 mm (range, 3-30 mm). Nearly 60% of the aneurysms operated on were larger than 10 mm; 38% measured 10 to 14 mm, 20% were 6 to 9 mm, and 21% measured less than 5 mm. Approximately 13% were large or giant aneurysms. Among the aneurysms that bled, 40% were smaller than 10 mm in size and 51% measured between 10 and 19 mm. Small aneurysms (<5 mm) constituted more than 20% of the ruptured aneurysms. Size had an important association with clinical grade after SAH. Forty-one (72%) of 57 patients with aneurysms smaller than 10 mm in size were in good clinical grades after SAH, compared with 43 (5 1%) of 85 patients with large aneurysms (>10 mm). Twenty-six percent of patients with large aneurysms were in clinical Grades IV and V, compared with fewer than 7% of those with the small aneurysms (P < 0.005). The influence of risk factors (age, hypertension, alcohol intake, sex, and location of the aneurysm) on size was analyzed, and age (P < 0.00 1) and smoking (P < 0.001) we re found to be significant factors. As patient age increased, aneurysm size was found to be larger. Outcome after treatment for patients with large aneurysms was significantly worse than that for patients with small aneurysms (P < 0.03). The mortality rate for patients with small aneurysms (<10 mm) was 1%, compared with a 6% mortality rate in patients with large ones. The mortality and morbidity rates of patients increased linearly with the size of the aneurysm (P < 0.01) (Fig. 4).

Neurologic Grade (Hunt and Hess Scale)

Eighty-eight patients had unruptured aneurysms, 11% of them had aneurysms that had previously bled, and another 7% had associated neurologic deficits. Among the patients who had SAH, 28% were in Grade I, 31% were in Grade II, 22% were in Grade III, 17% were in Grade IV, and 2% were in Grade V. Clinical grade was significantly influenced by aneurysm location (P < 0.01) and aneurysm size (P < 0.03). Older patients tended to be in worse clinical grades (P = 0.07). Aneurysms larger than 10 mm in size were associated with statistically worse Hunt and Hess grade (P < 0.005) (Fig. 5). Aneurysm grade had a significant relationship with outcome, independent of aneurysm size (P < 0.00 1) (Fig. 6). In the group with unruptured aneurysms, 99% of patients had good recoveries, and those with aneurysms that had previously bled achieved good outcomes 90% of the time. With SAH, the rate of good outcomes diminished with increasing grade, from 90% in Grade I to 56% in Grade III and 37.5% in Grade IV. Similarly, the mortality r ate was 0% in Grade I, 2% in Grade II, 6% in Grade III, and 17% in Grade IV.

Intraoperative Factors

Intraoperative rupture of an aneurysm occurred in 29 patients. Temporary control of the parent vessel was applied electively in 69 patients and after the rupture of an aneurysm in 22 patients. These incidents had a close relationship with each other (P < 0.01). The risk of intraoperative rupture was inversely related to age (P < 0.03). Intraoperative rupture was also significantly associated with poor neurologic result (P < 0.02). A temporary clip application had no correlation with outcome, however.

Preoperative Risk Factors

Patient history of smoking, alcohol intake, and hypertension influenced outcome and clinical grade. Smoking and alcohol intake did not exhibit any significant relationship with the Hunt and Hess grade, but hypertension was associated with poorer grade (P < 0.03). Hypertension also had an influence on GOS score (P < 0.04). Alcohol intake (P < 0.02) and smoking (P < 0.05) were associated with poor GOS scores.

Glasgow Coma Scale

Neurologic status was also assessed using the GCS. Similarly to the clinical Hunt and Hess grade, GCS score also had a strong linear association with outcome (P < 0.001). The lower the patient's GCS score, the poorer the outcome.

Glasgow Outcome Scale

Neurologic outcome was assessed according to the GOS after 6 months. Good outcomes were achieved in 75% of the cases. Another 16% of patients had fair outcomes (moderate disability). There was a 3.4% mortality rate and a 5% morbidity rate in the surgically treated group. Of the nine patients who died, one was in Grade V (not operated), four were in Grade IV, two were in Grade III, and one was in Grade II. The ninth patient had a symptomatic fusiform aneurysm that was repaired under circulatory cardioplegia. He had a fusiform aneurysm of vertebrobasilar artery with repeated episodes of embolic stroke as well as fusiform dilations of the bilateral middle cerebral arteries. Neurologic outcome was significantly associated with clinical grade (Fig. 5) and GCS score (P < 0.001). Older age (P < 0.002), large aneurysms (P < 0.01), posterior circulation aneurysms (P < 0.001), and intraoperative ruptures (P < 0.02) resulted in poor outcome. Multivariate analysis identified posterior circulation aneurysms (P < 0.01) and hypertension (P < 0.028) as risk factors for poor clinical grade. Lower GOS score (P < 0.001), higher Hunt and Hess grade (P < 0.001), posterior aneurysm location (P < 0.01), and large aneurysm size (P < 0.02) resulted in worse outcomes. Older age showed a trend toward poor GOS score in this analysis (P < 0.07).

Discussion

This study identified hypertension, smoking, alcohol intake, and age as significant contributory risk factors in the management of intracranial aneurysms. Although males presented with poorer clinical grades than females, this factor had no significant impact on outcome after treatment. This finding is an interesting one that is probably reported for the first time in our series. We found no reports in the medical literature exploring sex as a variable influencing clinical grade in SAH. This statistically significant finding is worth considering in a larger series of patients. Females outnumbered males in this study, as they have in other studies; but they tended to be younger than their male counterparts at the time of presentation.

The linear relationship between patient age and aneurysm size is important, given that the majority of ruptured aneurysms were larger than 10 mm and that patients with large aneurysms were in significantly worse clinical condition with regard to SAH. It is of note that large aneurysms in our study were associated with poor clinical grade. This observation is seldom reported in the literature. In other studies, clinical grade has been a strong prognostic indicator. Our findings encourage early identification of the patient population with good prognostic factors, such as younger age, aneurysms smaller than 10 mm, good neurologic grade, and without premorbid conditions and predisposing factors.

The International Cooperative Study on the Timing of Aneurysm Surgery (5) concluded that increased age, decreased consciousness, hypertension, preexisting medical conditions, and basilar aneurysms were predictors of mortality. Many subsequent reports emphasized the significance of these factors (6) and also added other risk factors, such as aneurysm size (7) and intraoperative rupture. (8) The vast experience of Rice et al (9) with 1,500 aneurysms accumulated during a 31-year period produced excellent results in the management of posterior circulation aneurysms, with 5% mortality and 10% morbidity rates in their patients.

Although a smaller group is presented here, the patient population with posterior circulation aneurysms had a 7.6% mortality rate. Nearly 80% of patients made good functional recoveries, with a morbidity rate of 13%. The mortality rate for intact aneurysms in the present study is encouraging, with 99% of the patients making good functional recoveries. This rate is similar to that of other reports that have reported 0% mortality in patients with unruptured aneurysms. (10,11) Early operation after SAH is expected to yield favorable results, as reported in the literature; (5,12) however, operative intervention during the spasm risk period of 4 to 14 days did not significantly improve results in our patient population. The improvement in perioperative management is probably a positive factor, although a selection bias cannot be ruled out. For patients in good neurologic condition, the timing of the operation probably had no independent influence, because a majority (88%) of our patients were in good clinical grad es (ie, Grades I-III). A significant proportion (73%) of the poorgrade patients in our study also showed neurologic recovery with good functional outcome, however. This finding supports the recent literature on aggressive management of aneurysmal SAH, regardless of clinical grade. (13-15)

The literature cited defines poor prognostic indicators as those that result in worse clinical grade and those that yield suboptimal treatment results. Hypertension is known to be a significant factor influencing outcome and is slightly greater than expected in the general population. (16-18) Increasing age in association with hypertension, alcohol intake, and smoking can significantly influence the growth of aneurysms. (19,20) The interplay of these predisposing factors may occur through increased aneurysm size and its negative influence on clinical grade after rupture. (21) Clinical grade is poor with large aneurysms, and surgery is also more difficult. (4) With predisposing factors, the majority of these aneurysms present with warning leaks that go unnoticed and reach longer dimensions, so that the presentation can be catastrophic. (22,23) The acceptable methodology of managing these lesions probably lies in early diagnosis and careful consideration of all risk factors that result in the growth and rupture of these aneurysms. Acceptable management of such lesions also includes offering the treatment option with the lowest mortality and morbidity rates. The close association of patient age, aneurysm size, clinical grade, and outcome must be kept in mind to identify patient populations at high risk and to obtain optimal results.

Conclusion

Males and patients with large aneurysms in our study population presented in worse clinical grades than other patients. The age of the patient, the size and location of the aneurysm, and the clinical grade of the patient had statistically significant associations with GOS scores. Early identification of, the patient population with favorable prognostic factors is essential to achieving good surgical outcomes.

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Accepted May 22, 2002.

References

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(2.) Jellinger K. Pathology of intracerebral hemorrhage. Zentralbl Neurochir 1997;38:29-42.

(3.) Torner JC, Kassell NF, Wallace RB, Adams HP Jr. Preoperative prognostic factors for rebleeding and survival in aneurysm patients receiving antifibrinolytic therapy: Report of the Cooperative Aneurysm Study. Neurosurgery 1981;9:506-513.

(4.) Le Roux PD, Elliott JP, Eskridge JM, Cohen W, Winn HR. Risks and benefits of diagnostic angiography after aneurysm surgery: A retrospective analysis of 597 studies. Neurosurgery 1998;42:1248-1255.

(5.) Kassell NF, Tomer JC, Haley EC Jr, Jane JA, Adams HP, Kongable GL. The International Cooperative Study on the Timing of Aneurysm Surgery: Part I--Overall management results. J Neurosurg 1990;73:18-36.

(6.) Gotoh O, Tamura A, Yasui N, Suzuki A, Hadeishi H, Sano K. Glasgow Coma Scale in the prediction of outcome after early aneurysm surgery. Neurosurgery 1996;39:19-25.

(7.) International Study of Unruptured Intracranial Aneurysms Investigators. Unruptured intracranial aneurysms: Risk of rupture and risks of surgical intervention. N Engl J Med 1998;399:1725-1733.

(8.) Bellotti C, Oliveri G, Allegra O, Arrigoni M, Regalia F, Voci A, et al. Temporary clipping in the surgery of endocranial aneurysms. J Neuro surg Sci 1998;42(l Suppl 1):77-79.

(9.) Rice BJ, Peerless SJ, Drake CG. Surgical treatment of unruptured aneurysms of the posterior circulation. J Neurosurg 1990;73:165-173.

(10.) Wirth FP, Laws ER Jr, Piepgras D, Scott RM. Surgical treatment of incidental intracranial aneurysms. Neurosurgery 1983;12:507-511.

(11.) Piepgras DG. Management of incidental intracranial aneurysms. Clin Neurosurg 1989;35:511-518.

(12.) Samson DS, Hodosh RM, Reid WR, Beycr CW, Clark WK. Risk of intracranial aneurysm surgery in the good grade patient: Early versus late operation. Neurosurgery 1979;5:422-426.

(13.) Bailes JE, Spetzler RF, Hadley MN, Baldwin HZ. Management morbidity and mortality of poor-grade aneurysm patients. J Neurosurg 1990;72:559-566.

(14.) Nowak G, Schwachenwald R, Arnold H. Early management in poor grade aneurysm patients. Acta Neurochir (Wien) 1994;126:33-37.

(15.) Rordorf G, Ogilvy CS, Gress DR, Crowell RM, Choi IS. Patients in poor neurological condition after subarachnoid hemorrhage: Early management and long-term outcome. Acta Neurochir (Wien) 1997;139:1143-1151.

(16.) Andrews RJ, Spiegel PK. Intracranial aneurysms: Age, sex, blood pressure, and multiplicity in an unselected series of patients. J Neurosurg 1979;51:27-32.

(17.) McCormick WF, Schmalstieg EJ. The relationship of arterial hypertension to intracranial aneurysms. Arch Neurol 1977;34:285-287.

(18.) Stenbens WE. Etiology of intracranial berry aneurysms. J Neurosurg 1989;70:823-831.

(19.) Juvela S, Porras M, Heiskanen O. Natural history of unruptured intracranial aneurysms: A long-term follow-up study. J Neurosurg 1993;79:174-182.

(20.) Ferguson GG. Physical factors in the initiation, growth, and rupture of human intracranial saccular aneurysms. J Neurosurg J 972;37:666-677.

(21.) Jane JA, Kassell NF, Torner JC, Winn HR. The natural history of aneurysms and arteriovenous malformations. J Neurosurg 1985;62:321-323.

(22.) Jakobsson KE, Saveland H, Hillman J, Edner G, Zygmunt S, Brandt L, et al. Warning leak and management outcome in aneurysmal subarachnoid hemorrhage. J Neurosurg 1996;85:995-999.

(23.) Yasui N, Magarisawa S, Suzuki A, Nishimura H, Okudera T, Abe T. Subarachnoid hemorrhage caused by previously diagnosed, previously unruptured intracranial aneurysms: A retrospective analysis of 25 cases. Neurosurgery 1996;39:1096-1101.

RELATED ARTICLE: Key Points

* Poor clinical grade after subarachnoid hemorrhage was seen in male patients, patients with hypertension, and older patients.

* Patients with posterior circulation aneurysms presented with poor neurologic status.

* Male patients and those with hypertension, increasing age, and posterior circulation aneurysms were at high risk for poor neurologic outcome after treatment due to worse clinical grade at presentation.

* Independent variables predicting poor outcome were large aneurysm size, posterior circulation aneurysm, low Glasgow Coma Scale score, and intraoperative rupture of the aneurysm.

* Prompt diagnosis of patients with favorable variables is suggested for good neurologic outcome after operative treatment of intracranial aneurysms.

From the Department of Neurosurgery, Louisiana State University Health Sciences Center, Shreveport, LA.

Reprint requests to Anil Nanda MD, FACS, Department of Neurosurgery, Louisiana State University Health Sciences Center in Shreveport, 1501 Kings Highway, P.O. Box 33932, Shreveport, LA 71130-3932. Email: ananda@lsuhsc.edu

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Author:Vannemreddy, Prasad
Publication:Southern Medical Journal
Date:Mar 1, 2003
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