HIROYUKI HASHIMOTO, M.D., JUN-ICHI IIDA, M.D., YASUO HIRONAKA, M.D., MASATO OKADA, M.D., AND TOSHISUKE SAKAKI, M.D.

Transcription

1 J Neurosurg 92: , 2000 Use of spiral computerized tomography angiography in patients with subarachnoid hemorrhage in whom subtraction angiography did not reveal cerebral aneurysms HIROYUKI HASHIMOTO, M.D., JUN-ICHI IIDA, M.D., YASUO HIRONAKA, M.D., MASATO OKADA, M.D., AND TOSHISUKE SAKAKI, M.D. Department of Neurosurgery, Okanami General Hospital, Ueno, Japan; and Department of Neurosurgery, Nara Medical University, Kashihara, Japan Object. Patients with subarachnoid hemorrhage (SAH) in whom angiography does not demonstrate diagnostic findings sometimes suffer recurrent disease and actually harbor undetected cerebral aneurysms. The management strategy for such cases remains controversial, but technological advances in spiral computerized tomography (CT) angiography are changing the picture. The purpose of this prospective study was to examine how spiral CT angiography can contribute to the detection of cerebral aneurysms that cannot be visualized on angiography. Methods. In 134 consecutive patients with SAH, a prospective search for the source of bleeding was performed using digital subtraction (DS) and spiral CT angiography. In 21 patients in whom initial DS angiography yielded no diagnostic findings, spiral CT angiography was performed within 3 days. Patients in whom CT angiography provided no diagnostic results underwent second and third DS angiography sessions after approximately 2 weeks and 6 months, respectively. Six patients with perimesencephalic SAH were included in the 21 cases. Six of the other 15 patients had small cerebral aneurysms detectable by spiral CT angiography, five involving the anterior communicating artery and one the middle cerebral artery. Two patients in whom initial angiograms did not demonstrate diagnostic findings proved to have a ruptured dissecting aneurysm of the vertebral artery; in one case this was revealed at autopsy and in the other during the second DS angiography session. A third DS angiography session revealed no diagnostic results in 13 patients. Conclusions. Spiral CT angiography was useful in the detection of cerebral aneurysms in patients with SAH in whom angiography revealed no diagnostic findings. Anterior communicating artery aneurysms are generally well hidden in these types of SAH cases. A repeated angiography session was warranted in patients with nonperimesencephalic SAH and in whom initial angiography revealed no diagnostic findings, although a third session was thought to be superfluous. KEY WORDS computerized tomography angiography subarachnoid hemorrhage cerebral aneurysm S Abbreviations used in this paper: ACoA = anterior communicating artery; CT = computerized tomography; DS = digital subtraction; MCA = middle cerebral artery; SAH = subarachnoid hemorrhage; VA = vertebral artery. 278 UBARACHNOID hemorrhage of unknown cause accounts for 13 to 22% of all cases of SAH and is usually associated with a benign outcome. 2,11,22,26 This favorable prognosis is strongly linked to perimesencephalic SAH because patients with this type have a significantly better prognosis. 15,31,35,42 Although various forms of SAH that are not identifiable on angiograms can be distinguished on CT scans and the patient s prognosis differs, the source of the hemorrhage remains unknown in most cases. Some affected patients suffer recurrent hemorrhage and sustain significant morbidity or mortality. 11,13,22,26,37 In some cases in which angiography does not reveal the source of SAH, exploratory surgery has disclosed small aneurysms or microaneurysms that present as risks for additional episodes of bleeding. 8,10,23,30,32,39,41,44 The development of spiral CT angiography, which allows high-speed scanning, has allowed rapid production of three-dimensional reconstructed images of cerebral aneurysms. 1,7,9,16,25,34 This modality sometimes can disclose small cerebral aneurysms that conventional angiography fails to reveal. 9,20,45 However, it remains unclear to what extent spiral CT angiography can be used to distinguish patients with cerebral aneurysms in whom angiography has not revealed diagnostic findings from individuals who experience SAH of unknown cause. We therefore made a prospective study of patients with SAH in whom the initial angiogram revealed no diagnostic findings and in whom spiral CT and DS angiography were performed according to our protocol. The management of patients with SAH of unknown cause, in particular those with nonperimesencephalic SAH, should be based on the findings of spiral CT angiography. Clinical Material and Methods Patient Population Between July 1995 and June 1999, 134 patients pre-

2 Spiral CT angiography for cerebral aneurysms senting with SAH were admitted to our hospital. The diagnosis of SAH was determined by CT scan or lumbar puncture on admission. Of the 134 patients, 126 initially underwent DS angiography to identify the source of the bleeding; this was performed as four-vessel cerebral angiography with multiple views. The other eight patients could not undergo DS angiography because their clinical states were too severe and they died within 1 week after examination. The initial DS angiograms revealed no diagnostic findings in 21 of the 126 patients: 12 men and nine women ranging in age from 39 to 82 years (mean 60.6 years). The patients conditions were assessed according to the Hunt and Hess scale: 21 the grades were I in five patients, II in eight, III in six, and IV in two patients. Spiral CT angiography has been available at our institution since July Since that time, patients with SAH in whom initial angiography revealed no diagnostic findings have undergone additional examinations within 3 days according to the protocol detailed in this paper. Patients in whom spiral CT angiography revealed no diagnostic findings have undergone second and third DS angiography sessions approximately 2 weeks and 6 months later to search for vascular abnormalities. Spiral CT Angiography Spiral CT angiography was performed using a highspeed helical scanner (model X Press GX; Toshiba Medical Systems Co., Ltd., Tokyo, Japan). A 100-ml dose of iopamidol 300 (Nippon Schering, Osaka, Japan) nonionic contrast medium was delivered into the antecubital vein by means of a power injector at the rate of 3 ml/second. Spiral scanning was initiated after 30 seconds. Thirty scans of the prescribed areas on lateral scout views were obtained in 1-mm slices by using a 1-mm/second table speed. Three-dimensional reconstruction of the images was conducted to overlap 0.5-mm sections for increased resolution by using a workstation with three-dimensional imaging software (CTD-03B; Toshiba Medical Systems). The lower threshold was set at 100 to 120 Hounsfield units to obtain maximum-intensity views of contrast-enhanced arteries. Most intracranial arteries around the circle of Willis are visualized using spiral CT angiography. When a cerebral aneurysm was suspected, the three-dimensional image targeting the lesion was processed for more detailed assessment. When no aneurysm was identified in the first processing session and the distribution of SAH on CT scanning was diffuse and impartial, complexes of the ACoA or posterior circulation were the focus for the second processing session. TABLE 1 Summary of characteristics of six patients with SAH and nondiagnostic findings for cerebral aneurysms on angiography* Age Aneurysm Hunt Case (yrs), Fisher & Hess Shunt No. Sex Location Size (mm) Grade Grade Surgery 1 72, F ACoA III yes 2 62, F ACoA 2 2 II yes 3 44, M ACoA 3 2 II no 4 46, F ACoA 3 4 II no 5 66, F ACoA 3 2 II no 6 48, M MCA 3 3 III yes * Outcome in all six patients was excellent. Results In this series six patients with perimesencephalic SAH were found among the 21 patients in whom initial angiography and CT angiography revealed no diagnostic findings. In six of the other 15 patients with nonperimesencephalic SAH, spiral CT angiography revealed small cerebral aneurysms; five were located on the ACoA and one on the MCA (Table 1). According to the Fisher classification of CT findings for SAH, 12 three of the patients were categorized as Grade 2, one as Grade 3, and two as Grade 4. Four patients were assigned Grade II and two Grade III according to Hunt and Hess scoring. 21 In all six patients, the aneurysms, ranging from 2 to 3 mm, were identified during surgery and were completely clipped. Secondary normalpressure hydrocephalus occurred in three patients and was controlled by shunt placement. All patients had an excellent outcome after surgery. Two patients in whom initial angiography was not diagnostic were later found to have ruptured dissecting aneurysms of the VA. The initial angiograms in both cases revealed a slight stenosis of the affected VAs, which could not be distinguished from atherosclerotic changes. Spiral CT angiography provided no more useful findings than had the initial DS angiography. One of these patients died of repeated rupture 5 days after the initial onset of symptoms, and the correct diagnosis was made at autopsy. The other patient underwent shunt placement for secondary hydrocephalus and a second angiography session revealed a definite stenosis and irregularity of the affected VA. However, that patient has been conservatively managed with no further hemorrhages. The remaining 13 patients, including the six with perimesencephalic SAH, underwent second and third DS angiography studies with no aneurysms found. All patients received careful follow up for a mean of 2.3 years without remarkable findings. Illustrative Case Case 2 This 62-year-old woman presented with sudden onset of severe headache. A CT scan obtained on admission revealed a severe diffuse SAH without localized clots (Fig. 1). Computerized tomography scanning did not reveal a hemorrhagic source and four-vessel angiography with multiple views did not demonstrate a cerebral aneurysm (Fig. 2). On the next day, spiral CT angiography demonstrated a small ACoA aneurysm (Fig. 3), and the patient underwent surgery via a right pterional approach. The aneurysm, which measured 2 mm, was identified as the source of bleeding during surgery and was completely clipped (Fig. 4). Subsequent hydrocephalus was controlled by shunt placement. Postoperatively, the patient regained full capabilities and returned to work. Discussion Angiography Sessions Although there have been extensive debates regarding 279

3 H. Hashimoto, et al. FIG. 1. Case 2. Axial CT scan revealing diffuse SAH without localized clots. This scan does not indicate a source of the SAH. the necessity for repeated angiography in patients with SAH in whom initial angiograms were not diagnostic, the subject remains controversial. 6,13,14,22,24 The rate at which a cerebral aneurysm is detected using repeated angiography varies from 2 to 22%. 13,26,38 Various authors have reported rebleeding rates of 4.7 to 8.6% in patients with SAH in whom angiograms were not diagnostic 6,11,14 and, in fact, many patients with SAH of unknown cause eventually die of a subsequent hemorrhage. 2,4,6,8,11,13,14,18,26,36,37 In the 21 patients with SAH in our study in whom initial angiograms did not yield abnormal findings, eight actually harbored cerebral aneurysms. In six patients, small aneurysms were revealed by spiral CT angiography and in two patients dissecting aneurysms of the VA were found at autopsy or on repeated angiography. Thus, repeated angiography is warranted in cases of nonperimesencephalic SAH in which the initial angiogram was not diagnostic. In cases of nonperimesencephalic SAH in which neither the initial angiography nor spiral CT angiography demonstrates any aneurysm, a second angiographic study should be performed a couple of weeks after onset of symptoms. However, our results demonstrate that performing a third angiographic study in such patients is superfluous. In line with earlier reports of a favorable outcome in patients with perimesencephalic SAH, 15,31,35,42 no aneurysms were identified using either spiral CT angiography or DS angiography in our series of patients with this type of SAH. Therefore, repeated angiography is not indicated in cases of perimesencephalic SAH in which the initial angiograms were not diagnostic. Location of Aneurysms not Revealed on Angiograms Jafar and Weiner 23 reported that focal blood accumulated in the interhemispheric fissure in four of six cases in which exploratory surgery was performed. The distribution of blood in the cisterns may indicate the site of an aneurysm, as other authors have documented. 8,10,22 A high probability of the presence of a cerebral aneurysm seems to be related to certain CT findings. However, in four of our six cases in which cerebral aneurysms were detected using spiral CT angiography, CT scans did not reveal focal blood in the interhemispheric fissure. In the other two cases, ACoA and MCA aneurysms were present. In other words, a certain proportion of cerebral aneurysms not found on angiograms occur in cases with homogeneously diffuse SAHs, in which exploratory surgery might not be appropriate. A review of the literature shows that at least 30 patients have undergone exploratory surgery after the cause of SAH was not revealed on angiographic studies. 8,10,23,30,32,33,39,41,44 The presence of ACoA aneurysms was established in 11 of the 30 cases; in most of these, clots in the interhemispheric fissure had been identified. These lesions included five MCA, four ACoA, and two internal carotid artery aneurysms or microaneurysms with accumulation of blood in the unilateral sylvian fissure. Fifteen ACoA aneurysms FIG. 2. Case 2. Left carotid artery angiograms obtained with the right carotid artery compressed (oblique views) revealing no definite evidence of a cerebral aneurysm. 280

4 Spiral CT angiography for cerebral aneurysms FIG. 3. Case 2. Spiral CT angiograms revealing a small ACoA aneurysm (small arrows). Larger arrows indicate the left A 1 segment. Left: Oblique view obtained from the left side. Right: Oblique view obtained from the right side. were included in 22 lesions confirmed by surgical exploration. In our study ACoA aneurysms accounted for five of the six aneurysms detected on spiral CT angiography. Therefore, spiral CT angiography or repeated angiography in cases of SAH in which initial angiograms were not diagnostic should focus particularly on the ACoA complex. Spiral CT Angiography Although spiral CT angiography is used as a less invasive alternative to DS angiography, whether it can replace DS angiography as the gold standard for detection of cerebral aneurysms remains unclear. 1,9,17,34,35 Using CT angiography to visualize small vessels in the 1-mm range is not as feasible as using high-quality DS angiography. 5,34 In the detection of cerebral aneurysms, the sensitivity and specificity of CT angiography has been found to vary, with ranges of 77 to 97% and 50 to 100%, respectively, 1,3,19,28,43 presumably depending on the level of threshold chosen and the processing program. In a study of 40 patients reported by Anderson, et al., 3 only four (57%) of seven cerebral aneurysms 3 mm or less in diameter that were revealed on DS angiography were detected on CT angiography. In another report, three of six aneurysms 3 mm or smaller were demonstrated on CT angiography. 40 However, the quality of spiral CT angiography depends considerably on the imaging study setup, and these results may have been due to technical problems related to this modality, which can be overcome by appropriate collaboration of skilled technicians and experienced clinicians. In the diagnosis of small cerebral aneurysms, spiral CT angiography often provides crucial information on the relations of aneurysms to associated arteries, which DS angiography cannot. Furthermore, a number of small cerebral aneurysms that were not revealed on other types of angiography have been detected by means of spiral CT angiography. 9,20,45 Although it is thus uncertain which modality is superior, the combination of spiral CT and DS angiography is sure to detect a small aneurysm more accurately than either technique used alone. To date there has been no prospective study in which patients with SAH in whom angiography findings were not diagnostic were examined using spiral CT angiography. In our study, no less than six cerebral aneurysms were disclosed on spiral CT angiograms in 21 cases in which angiograms were not diagnostic. Excluding the cases of perimesencephalic SAH, the rate of detection was a surprising 40% (six of 15 aneurysms). The success rate for repeated angiography in searches for aneurysms varies from 2 to 22% among published series. 13,26,38 Thus, spiral CT angiography may be superior to repeated angiography for this purpose. Management Strategies Several authors have proposed management protocols for patients presenting with clinically verified SAH, in whom angiographic studies are not diagnostic. 23,27,29,41 Although technological advances in CT angiography have been remarkable, the current study appears to be the first to demonstrate that spiral CT angiography deserves reconsideration in this context. Tatter and colleagues 41 reported that surgical exploration confirmed three aneurysms and four microaneurysms to be responsible for SAH in nine patients; in six of whom there were subtle angiographic abnormalities. However, we have some reservations about the claim that microaneurysms, which are tiny vascular lesions, were the actual sources of the hemorrhage. If available, angiographic findings of small abnormalities should be further examined by spiral CT angiography before surgery. Jafar and Weiner 23 described a protocol for patients with SAH in whom angiography proved to be nondiagnostic based on findings of positive surgical exploration in five of six patients. They concluded that exploratory surgery was justified in patients in whom the SAH was predominantly located in the basal interhemispheric fissure after two angiography sessions proved to be nondiagnostic. Aneurysms of the ACoA complex were thought to be the only lesions falling into this category. However, we do not agree with the necessity of exploratory surgery according to their protocol. Five patients in our study were found to have an ACoA aneurysm by using spiral CT angiography. The CT scans obtained in four of the five revealed neither predominant nor focal distribution of SAH in the basal interhemispheric fissure. Thus, a considerable number of ACoA aneurysms, for which CT findings never indicate a location of the bleeding source, 281

5 H. Hashimoto, et al. FIG. 4. Case 2. Operative photograph showing an ACoA aneurysm (small arrow) measuring 2 mm. Larger arrow indicates the left A 1 segment. are certainly included in angiographically nondiagnostic cases of SAH. In cases in which results of spiral CT and DS angiography are not diagnostic, but CT findings are highly suggestive of a ruptured aneurysm, exploratory surgery may be justified. Two patients in our series were found to have a dissecting aneurysm of the VA after CT angiography did not provide a definite diagnosis. Our evaluation of the initial angiograms and CT angiograms might be an error of observation, although it was difficult to distinguish the tiny radiological findings from atherosclerotic changes. The use of magnetic resonance imaging might have led to the correct diagnosis. Our management protocol in cases of SAH in which there were nondiagnostic angiographic findings should be improved in some respects. The results of all studies in patients with perimesencephalic SAH were nondiagnostic, which probably indicates that there is no need for repeated angiography. Follow-up examination using magnetic resonance or CT angiography may be appropriate. A third session of angiography was thought to be superfluous even in patients with nonperimesencephalic SAH. Conclusions In this prospective study, we show that spiral CT angiography deserves reconsideration in patients with angiographically nondiagnostic SAH. Spiral CT angiography was found to be a valuable modality in the detection of cerebral aneurysms, with ACoA aneurysms predominating. Repeated angiography was warranted in patients with nonperimesencephalic SAH in whom angiograms proved to be nondiagnostic, although a third angiography session is probably unnecessary. Acknowledgments We thank Toshihiro Tabata and Kunihiro Nakatsuji for technical assistance with the imaging setup of spiral CT scanning. References 1. Alberico RA, Patel M, Casey S, et al: Evaluation of the circle of Willis with three-dimensional CT angiography in patients with suspected intracranial aneurysms. AJNR 16: , Alexander MSM, Dias PS, Uttley D: Spontaneous subarachnoid hemorrhage and negative cerebral panangiography. Review of 140 cases. J Neurosurg 64: , Anderson GB, Findlay JM, Steinke DE, et al: Experience with computed tomographic angiography for the detection of intracranial aneurysms in the setting of acute subarachnoid hemorrhage. Neurosurgery 41: , Andrioli GC, Salar G, Rigobello L, et al: Subarachnoid haemorrhage of unknown aetiology. Acta Neurochir 48: , Aoki S, Sasaki Y, Machida T, et al: Cerebral aneurysms: detection and delineation using 3-D-CT angiography. AJNR 13: , Brismar J, Sundbärg G: Subarachnoid hemorrhage of unknown origin: prognosis and prognostic factors. J Neurosurg 63: , Dillon EH, van Leeuwen MS, Fernandez MA, et al: Spiral CT angiography. AJR 160: , Di Lorenzo N, Guidetti G: Anterior communicating aneurysm missed at angiography: report of two cases treated surgically. Neurosurgery 23: , Dorsch NWC, Young N, Kingston RJ, et al: Early experience with spiral CT in the diagnosis of intracranial aneurysms. Neurosurgery 36: , Endo S, Suzuki J: Anterior communicating artery aneurysm not visualized by angiography: report of two successfully operated cases, in Suzuki J (ed): Cerebral Aneurysms. Tokyo: Neuron Publishing, 1979, pp Eskesen V, Sørensen EB, Rosenørn J, et al: The prognosis in subarachnoid hemorrhage of unknown etiology. J Neurosurg 61: , Fisher CM, Kistler JP, Davis JM: Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 6:1 9, Forster DMC, Steiner L, Hakanson S, et al: The value of repeat pan-angiography in cases of unexplained subarachnoid hemorrhage. J Neurosurg 48: , Giombini S, Bruzzone MG, Pluchino F: Subarachnoid hemorrhage of unexplained cause. Neurosurgery 22: , Goergen SK, Barrie D, Sacharias N, et al: Perimesencephalic subarachnoid hemorrhage: negative angiography and favourable prognosis. Australas Radiol 37: , Görzer H, Heimberger K, Schindler E: Spiral CT angiography with digital subtraction of extra- and intracranial vessels. J Comput Assist Tomogr 18: , Harrison MJ, Johnson BA, Gardner GM, et al: Preliminary results on the management of unruptured intracranial aneurysms with magnetic resonance angiography and computed tomographic angiography. Neurosurgery 40: , Hayward RD: Subarachnoid haemorrhage of unknown aetiology. A clinical and radiological study of 51 cases. J Neurol Neurosurg Psychiatry 40: , Hope JKA, Wilson JL, Thomson FJ: Three-dimensional CT angiography in the detection and characterization of intracranial berry aneurysms. AJNR 17: , Hsiang JNK, Liang EY, Lam JMK, et al: The role of computed tomographic angiography in the diagnosis of intracranial aneurysms and emergent aneurysm clipping. Neurosurgery 38: , Hunt WE, Hess RM: Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg 28:14 20, Iwanaga H, Wakai S, Ochiai C, et al: Ruptured cerebral aneurysms missed by initial angiographic study. Neurosurgery 27: 45 51, Jafar JJ, Weiner HL: Surgery for angiographically occult cerebral aneurysms. J Neurosurg 79: , Juul R, Fredriksen TA, Ringkjøb R: Prognosis in subarachnoid hemorrhage of unknown etiology. J Neurosurg 64: ,

6 Spiral CT angiography for cerebral aneurysms 25. Katz DA, Marks MP, Napel SA, et al: Circle of Willis: evaluation with spiral CT angiography, MR angiography, and conventional angiography. Radiology 195: , Nishioka H, Torner JC, Graf CJ, et al: Cooperative study of intracranial aneurysms and subarachnoid hemorrhage: a longterm prognostic study. III. Subarachnoid hemorrhage of undetermined etiology. Arch Neurol 41: , O Boynick P, Brackett CE: Special problems associated with subarachnoid hemorrhage, in Fein JM, Flamm ES (eds): Cerebrovascular Surgery. New York: Springer-Verlag, 1985, Vol 3, pp Ogawa T, Okudera T, Noguchi K, et al: Cerebral aneurysms: evaluation with three-dimensional CT angiography. AJNR 17: , Ojemann, RG, Heros RC, Crowell RM: Surgical Management of Cerebrovascular Disease, ed 2. Baltimore: Williams & Wilkins, 1987, pp Pertuiset B, Haisa T, Bordi L, et al: Detection of a ruptured aneurysmal sac by MRI in a case of negative angiogram. Successful clipping of an anterior communicating artery aneurysm. Case report. Acta Neurochir 100:84 86, Rinkel GJE, Wijdicks EFM, Hasan D, et al: Outcome in patients with subarachnoid haemorrhage and negative angiography according to pattern of haemorrhage on computed tomography. Lancet 338: , Sakai N, Yamada H, Ando T, et al: Prevention of rebleeding after operation for subarachnoid hemorrhage of unknown cause. Neurosurgery 17: , Schievink WI, Wijdicks EFM, Piepgras DG, et al: Perimesencephalic subarachnoid hemorrhage. Additional perspectives from four cases. Stroke 25: , Schwartz RB, Tice HM, Hooten SM, et al: Evaluation of cerebral aneurysms with helical CT: correlation with conventional angiography and MR angiography. Radiology 192: , Schwartz TH, Solomon RA: Perimesencephalic nonaneurysmal subarachnoid hemorrhage: review of the literature. Neurosurgery 39: , Shephard RH: Prognosis of spontaneous (non-traumatic) subarachnoid haemorrhage of unknown cause. A personal series Lancet 1: , Spallone A, Ferrante L, Palatinsky E, et al: Subarachnoid haemorrhage of unknown origin. Acta Neurochir 80:12 17, Suzuki S, Kayama T, Sakurai Y, et al: Subarachnoid hemorrhage of unknown cause. Neurosurgery 21: , Takai N, Ezuka I, Sorimachi T, et al: Surgical intervention for angiographically unexplained subarachnoid hemorrhage report of three cases. Neurol Med Chir 33: , Tampieri D, Leblanc R, Oleszek J, et al: Three-dimensional computed tomographic angiography of cerebral aneurysms. Neurosurgery 36: , Tatter SB, Crowell RM, Ogilvy CS: Aneurysmal and microaneurysmal angio-negative subarachnoid hemorrhage. Neurosurgery 37:48 55, van Gijn J, van Dongen KJ, Vermeulen M, et al: Perimesencephalic hemorrhage: a nonaneurysmal and benign form of subarachnoid hemorrhage. Neurology 35: , Vieco PT, Shuman WP, Alsofrom GF, et al: Detection of circle of Willis aneurysms in patients with acute subarachnoid hemorrhage: a comparison of CT angiography and digital subtraction angiography. AJR 165: , Yoshida M, Anegawa S, Moritaka K: Significance of infundibular dilatation in unexplained subarachnoid hemorrhage. Neurosurgery 9: , Zouaoui A, Sahel M, Marro B, et al: Three-dimensional computed tomographic angiography in detection of cerebral aneurysms in acute subarachnoid hemorrhage. Neurosurgery 41: , 1997 Manuscript received July 19, Accepted in final form October 12, Address reprint requests to: Hiroyuki Hashimoto, M.D., Department of Neurosurgery, Okanami General Hospital, 1734 Kuwamachi, Ueno, Mie, , Japan. 283