Effect of clot removal on cerebral vasospasm TETSUJI INAGAWA, M.D., MITSUO YAMAMOTO, M.D., AND KAZUKO KAMIYA, M.D.

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1 J Neurosurg 72: , 1990 Effect of clot removal on cerebral vasospasm TETSUJI INAGAWA, M.D., MITSUO YAMAMOTO, M.D., AND KAZUKO KAMIYA, M.D. Department of Neurosurgery, Shimane Prefectural Central Hospital, Izumo, Japan t,- The effect of clot removal on cerebral vasospasm was studied in 104 patients with aneurysmal subarachnoid hemorrhage (). The series included patients who fulfilled all of the following criteria: operation was performed by Day 3 after the ictus; the patient's preoperative clinical grade was between Grades I and IV; there was no rebleeding; computerized tomography (CT) showed only ; and carotid angiograms were performed by Day 2 and repeated between Days 7 and 9. Both the degree of on CT and angiographic vasospasm were graded from 0 to III. The relationship of the grade in the basal frontal interhemispheric fissure (IHF) to the presence of vasospasm at the A2 segments of the anterior cerebral artery and the relationship of the grade in the sylvian stems to the presence of vasospasm at the M~ segments of the middle cerebral artery were analyzed. Correlation of preoperative and postoperative grades with the angiographic vasospasm grades, with the incidence of symptomatic vasospasm, and with the low-density area on CT could be found in the A2 and M~ territories. Decrease of cisternal blood measured by CT after the operation did not relate directly to the reduction of vasospasm. When the was Grade II or III in the basal frontal IHF, the angiographic vasospasm grades at the A2 were significantly lower in patients with surgery via the interhemispheric approach than in those with surgery via the pterional approach. vasospasm occurred in two of the eight cases operated on by the interhemispheric approach compared with 11 of the 22 cases approached via the pterional route. In patients with a pterional approach, there was no significant difference in severity of vasospasm in the M~ territory between the side of approach and the opposite side. No consistent relationship could be found between the time interval from to operation and the severity of vasospasm. While clot removal may ameliorate cerebral vasospasm, its effect per se does not seem to be significant. KEY WORDS " cerebral aneurysm subarachnoid hemorrhage 9 clot removal 9 vasospasm I N describing the clinical manifestations surrounding subarachnoid hemorrhage (), Fisher, et al., 3"4 reported that correlations between the site of major subarachnoid blood clots and the location of severe vasospasm as well as between the particular artery affected by vasospasm and the delayed clinical syndrome were almost exactly the same. These articles are very impressive, considering that there is a consistent anatomical relationship between the cisterns and the corresponding major blood vessels. On the other hand, early operation with evacuation of cisternal hematoma surrounding the major cerebral arteries has been attempted by many surgeons in order to reduce the incidence or severity of cerebral vasospasm. 2,5,7,1~ Clinical studies report a possible role for the mechanical removal of subarachnoid blood clots. However, surprisingly, no study has been made to date to determine whether the narrowing of blood vessels is ameliorated by removing the clot from the corresponding cistern. In order to clarify the effect of removing blood clots in such cisterns as the basal frontal interhemispheric fissure (IHF) and sylvian stem, the angiographic vasospasm and symptomatic vasospasm must be studied in territories such as the A1 and A2 segments of the anterior cerebral artery (ACA) and the M~ segments of the middle cerebral artery (MCA) corresponding to each cistern. The present study was conducted to investigate these questions. Clinical Material and Methods During the 8-year period from 1980 to 1987, 412 patients who had suffered aneurysmal were admitted to the Department of Neurosurgery of Shimane Prefectural Central Hospital. On admission, each patient's clinical condition was graded according to the classification of Hunt and Hess, 8 without modification. The operations were conducted via the direct approach 224 J. Neurosurg. / Volume 72/February, 1990

2 Effect of clot removal on cerebral vasospasm using microsurgical techniques and by the same surgeon (T.I.). In accordance with a policy of early operation for ruptured intracranial aneurysms of the anterior circle, surgery was usually performed on the day following admission. 9 Until December, 1985, the pterional approach 3~ was used in cases with anterior communicating artery (ACoA) aneurysms, and the interhemispheric approach ~ was used thereafter. In cases with internal carotid artery (ICA) or MCA aneurysms, the pterional approach was used. Bilateral craniotomy was carried out in cases with severe clot on the side opposite to the to remove the clot. An attempt was made to evacuate as much of the blood clot as possible following aneurysm clipping, and the subarachnoid space was irrigated with lactated Ringer's solution. Induced hypervolemia or hypertension was not used for treatment of symptomatic vasospasm. Aneurysmal was classified by computerized tomography (CT) into four anatomical types: alone; intracerebral hematoma; intraventricular hemorrhage; and subdural hematoma. The amount of blood in the subarachnoid space on the admission CT scan was measured at the basal frontal IHF and both "sylvian stems" according to the terminology of Fisher, et al. 3 In each cistern, the thickness of the blood deposits was classified subjectively in four categories: Grade 0 = no observable blood; Grade I = slight blood deposits; Grade II = moderate blood deposits; and Grade III = severe blood deposits. The Hounsfield number for each cistern was also determined. Repeat CT was performed immediately after the operation, and the amount of blood in the cisterns was classified again. The cisterns in which the amount of blood could not be measured accurately, due to such artifacts as aneurysmal clips, were excluded from this analysis. The day of was defined as Day 0. Carotid angiography was performed at the time of admission, whenever possible on patients hospitalized in the acute stage, and again between Days 7 to 9 after to analyze the degree of vasospasm. The vessels studied for the purpose of assessing angiographic vasospasm were the A~ and A2 segments of the ACA and the M~ segment of the MCA. The degree of vasospasm of each vessel demonstrated on carotid angiograms obtained between Days 7 and 9 after was assessed by comparing the same portion with the initial angiogram obtained by Day 2. The angiographic vasospasm of each vessel was divided into four groups: Grade 0 = no vasospasm detected; Grade I = slight vasospasm; Grade II = moderate vasospasm; and Grade III = severe vasospasm with more than 50% reduction of arterial caliber. In assessing symptomatic vasospasm, if symptoms were newly observed without preceding symptoms from other causes, such as surgical or medical complications, then hemiparesis, monoparesis, and aphasia were considered to be caused by vasospasm of the MCA. Paralysis of the lower extremities, disturbance of consciousness, and mental disturbance were thought to be related to vasospasm of the ACA. If the symptoms subsequently disappeared, they were regarded as transient, but if the symptoms persisted until discharge from the hospital, they were regarded as permanent. Computerized tomography was repeated in order to detect persistence of subarachnoid clot and to identify areas of ischemia. The appearance of a new low-density area, which had not been visualized on a previous CT scan and was not caused by other factors such as the operation, was regarded as due to vasospasm with or without clinical symptoms. Data of all the cases was input into a microcomputer after the patients' discharge. The cases that fulfilled all of the following criteria were selected: 1) admission by Day 2 after initial ; 2) operation performed by Day 3; 3) preoperative clinical grade between Grades I and IV; 4) no rebleeding either prior to or following admission; 5) availability of CT scans performed on admission and again after the operation; 6) was the sole abnormality on CT scans; and 7) availability of carotid angiograms obtained by Day 2 and again between Days 7 and 9. There were 104 cases which fulfilled all of these criteria. Bilateral carotid angiograms were analyzed in 96 cases, and unilateral carotid angiograms were studied in eight cases. Of the 104 cases, 45 were men and 59 were women, with ages ranging from 20 to 84 years (mean age 58.4 years). Three points were studied by examining the relationships of the grade on CT of the basal frontal IHF and both sylvian stems to the later development of cerebral vasospasm in the A~ and A2 segments of the ACA and in both MI segments; these were: 1) the time of the CT scan in relation to vasospasm; 2) the relationship of the operative approach used to vasospasm occurrence; and 3) the relationship of the timing of surgery to vasospasm. Statistical analyses were calculated using the chi-square test. Results Of the 104 ruptured aneurysms in this series, 45 arose from the ACoA, 28 from the ICA, 26 from the MCA, and five from the ACA. The patients' preoperative clinical condition was Grades I or II in 68 cases, Grade III in 29 cases, and Grade IV in seven cases. Significant relationships were observed between the grade and CT Hounsfield number in both the basal frontal IHF and the sylvian stem ( = , x 2 = ; both p < 0.01) (Table 1). Relationship of Time of CT Scan to Vasospasm In both A2 and M1 territories, a correlation between the preoperative grades and the angiographic vasospasm grades, the incidence of symptomatic vasospasm, and the appearance of a low-density area on CT were found: in A2, X 2 = , , and , respectively (all p< 0.01); in M1, = (p < 0.05), x 2 = (p < 0.01), and = (p < 0.01), respectively (Tables 2 and 3). In both territories, J. Neurosurg. / Volume 72 / February,

3 T. Inagawa, M. Yamamoto, and K. Kamiya TABLE 1 Relationship between grade and Hounsfield number* Cistern basal frontal IHF sylvian stem Grade Hounsfield Number in Cistern -< _> I II III I II III * = subarachnoid hemorrhage; IHF = interhemispheric fissure. even after operation, the higher the postoperative grade the higher were the angiographic vasospasm grades and the incidence of symptomatic vasospasm and a low-density area on CT. The angiographic vasospasm grades of A2 were significantly higher in patients with postoperative Grade I or II than in those with preoperative Grade I or II (x 2 = , p < 0.01) (Table 2). However, in the angiographic vasospasm grades of MI, there was no significant difference between postoperative and preoperative I or II (Table 3). In the 42 cases with postoperative s I and II of the basal frontal IHF, symptomatic vasospasm occurred in 21% (nine cases) and a low-density area was observed on CT in 17% (seven cases) (Table 2). These rates were significantly higher than those in the 51 cases with preoperative s I and II, which were 4% (two cases; x 2 = 6.769, p < 0.01) and 2% (one case; x 2 = 6.335, p < 0.05), respectively. In the 80 cases with postoperative I or II at the sylvian stem, symptomatic vasospasm occurred in 13% (10 cases) and a low-density area was observed on CT in 14% (11 cases) (Table 3). These rates were also significantly higher than those for preoperative I or II, TABLE 2 Time of CT scan in relation to vasospasm of A2 in 104 patients* at A2 Vasospasm of ACA Territory Time of CT Scant at Basal Frontal IHF 0 I II III Low-Density Area Vasospasm on CT preoperative postoperative I II III I II III (T, P) (0, o) (0, o) (1, 1) (2, 11) (0, o) (2, 3) (0, 4) (1,2) 3 3 * CT = computerized tomography; = subarachnoid hemorrhage; IHF = interhemispheric fissure; ACA = anterior cerebral artery; -- = absent; + = present; T = transient; P = permanent. t CT scans were performed on admission and immediately after operation. TABLE 3 Time of CT scan in relation to vasospasm of MI in 104 patients* at Mj Vasospasm of MCA Territory Time of Low-Density CT Scant at Sylvian Stem 0 I II III Vasospasm Area on CT preoperative postoperative - + (T, P) (0, 0) 42 0 I (0, 0) 62 0 II (0, 2) 46 3 III (0, 13) (0, 0) 69 0 I (0,7) 51 8 II (0, 3) 18 3 III (0, 0) 1 0 * CT = computerized tomography; = subarachnoid hemorrhage; MCA = middle cerebral artery; - = absent; + = present; T = transient; P = permanent. t CT scans were performed on admission and immediately after operation. 226 J. Neurosurg. / Volume 72/February, 1990

4 Effect of clot removal on cerebral vasospasm which were 2% (two of the 111 cases, x 2 = 9.032) and 3% (three of the 111 cases x 2 = 8.353), respectively (both p < 0.01). Relationship of Operative Approach to Vasospasm The effects of the interhemispheric approach and the pterional approach on vasospasm of the A~ and A2 segments of the ACA are shown in Table 4. With both approaches, the higher the grade of the basal frontal IHF was, the higher were the angiographic vasospasm grade and the incidence of symptomatic vasospasm and low-density area on CT. When was Grades II and III at the basal frontal IHF, the angiographic vasospasm grades of the A2 were significantly lower in cases with the interhemispheric approach than in cases with the pterional approach (x 2 = for Grade II, x 2 = for Grade III; both p < 0.05). However, there were no significant differences between these approaches with respect to the angiographic vasospasm grades for the A~. In III, both symptomatic vasospasm and low-density areas on CT occurred in only 25 % of cases with the interhemispheric approach (two of the eight cases), while they occurred in 50% (11 of the 22 cases) and 45% (10 of the 22 cases) of cases with the pterional approach, respectively. However, the difference in occurrence of symptomatic vasospasm and CT low-density areas between the two approaches was not significant. The relationship between the side of the operative approach and vasospasm of the M~ territory is shown in Table 5. In cases with III, the angiographic vasospasm grades and the incidence of symptomatic vasospasm and CT low-density areas were slightly higher for the approach side than for the opposite side; however, these differences were not significant. Relationship of Time of Operation to Vasospasm Of the 104 cases, 20 underwent surgery on Day 0, 56 on Day 1, 19 on Day 2, and nine on Day 3. Tables 6 and 7 show the relationship of the time of surgery to TABLE 4 Operative approach and grade at basal frontal IHF correlated with vasospasm of A~ and Ae segments in 104 patients* Vasospasm of ACA Territory Operative at Basal At AI At A2 Low-Density Approach Frontal IHF Vasospasm Area on CT interhemispheric pterional 0 I II III 0 I II III - +(T, P) (0, 0) 1 0 I (0, 0) 5 0 II (1, 0) 9 0 III (0, 2) (0, 0) 22 0 I (0, 0) 17 0 II (0, 1) 19 1 III tl (2, 9) * = subarachnoid hemorrhage; IHF = interhemispheric fissure; CT = computerized tomography; ACA = anterior cerebral artery; - = absent; + = present; T = transient; P = permanent. TABLE 5 Operative approach and grade of sylvian stem correlated with vasospasm of M, in 104 patients* at MI Vasospasm of MCA Territory Operative at Sylvian Low-Density Approacht Stem 0 I II III Vasospasm Area on CT approach side opposite side - + (T, P) (0, 0) 11 0 I (0, 0) 26 0 II (0, 1) 22 1 III (0, 11) (0, 0) 31 0 I (0, 0) 36 0 II (0, 1) 24 2 III (0, 2) 15 3 * = subarachnoid hemorrhage; CT = computerized tomography; MCA = middle cerebral artery; - = absent; + = present; T = transient; P = permanent. t Bilateral sylvian stems were categorized as the approach side in patients whose clot was removed by bilateral frontotemporal craniotomy, and in cases with interhemispheric approach they were classified as the opposite side. J. Neurosurg. / Volume 72/February,

5 T. Inagawa, M. Yamamoto, and K. Kamiya the grade of vasospasm of the A2 segment of the ACA and the M I segment of the MCA. When the at the basal frontal IHF was Grade III, the angiographic vasospasm grade of A2 was significantly lower in patients with surgery on Day 0 than in those with operations on Days 1 to 3 ( = , p < 0.01). Conversely, when the was Grade II, the angiographic vasospasm grades were significantly higher in patients undergoing surgery on Day 0 than in those with operations on Days 1 to 3 ( , p < 0.01). When at the basal frontal IHF was Grade III, both symptomatic vasospasm and low-density areas on CT occurred in 17% (one of six cases) of patients undergoing surgery on Day 0; they occurred in 50% (12 cases) and in 46% (11 cases) of the 24 patients with surgery on Days 1 to 3, respectively. However, no significant relationships could be found between timing of the operations and the incidence of symptomatic Grader III Day of Operation TABLE 6 Day of operation correlated with grade of vasospasm of the A2 segment* Vasospasm Low-Density Area on CT 0 I II III - + (T, P) - + Day (0, l) 4 1 Day (1, 0) 14 0 Day (0, 0) 9 0 Day (0, 0) 1 0 Day (0, 1) 5 1 Day (2, 9) 9 10 Day (0, 1) 2 1 Day (0, 0) 2 0 * = subarachnoid hemorrhage; CT = computerized tomography; - = absent; + = present; T = transient; P = permanent. t The grade at the basal frontal interhemispheric fissure on CT performed on admission. Gradet II III Day of Operation TABLE 7 Day of operation correlated with grade of vasospasm of the MI segment* Vasospasm Low-Density Area on CT 0 I II III - + (T, P) - + Day (0, 1) 12 1 Day (0, 1) 19 1 Day (0, 0) 13 1 Day (0, 0) 2 0 Day (0, 2) 10 2 Day (0, 9) Day (0, 2) 5 2 Day (0, 0) 1 0 * = subarachnoid hemorrhage; CT = computerized tomography; - = absent; + = present; T = transient; P = permanent. t The grade at the sylvian stem on CT performed on admission. Grader III Day of Operation TABLE 8 Day of operation by vasospasm of M~ segment on operative approach side* Vasospasm Low Density Area on CT 0 I II III - + (T, P) - + Day (0, 1) 6 1 Day (0, 0) 10 0 Day (0, 0) 5 0 Day (0, 0) 1 0 Day (0, 2) 6 2 Day (0, 7) 18 7 Day (0, 2) 1 2 Day (0, 0) 1 0 * = subarachnoid hemorrhage; CT = computerized tomography; - = absent; + = present; T = transient; P = permanent. t The grade of the sylvian stem on CT performed on admission. 228 J. Neurosurg. / Volume 72/February, 1990

6 Effect of clot removal on cerebral vasospasm vasospasm and low-density areas on CT in the A2 territory. No effect of timing of the operations on the angiographic vasospasm grades and the incidence of symptomatic vasospasm and low-density area on CT could be found in the M~ territory (Table 7). Table 8 presents data on the day of operation and the degree of vasospasm of the M~ on the operative approach side on[y, showing no significant relationship. Discussion In patients with early post- operation, correlations of both the preoperative and postoperative grades to the angiographic vasospasm grades and the incidence of symptomatic vasospasm and low-density areas on CT were found in both the A2 and M~ territoties. There is undoubtedly a strict correlation between the amount of cisternal blood detected by CT soon after and the subsequent development of vasospasm.3,53 5,16,18,~ 9,25,28 The angiographic vasospasm grades and the incidence of symptomatic vasospasm and low-density areas on CT were higher in patients with s I and II on postoperative CT than when the same grades were seen on preoperative CT scans; that is, a decrease in the amount of cisternal blood on CT after operation is not directly related to the reduction of vasospasm. Since patients in the acute stage after usually have been operated on the day following admission, there is a difference of 1 day between the preoperative and postoperative CT scans. Therefore, a possible influence of the difference in time cannot be denied. In addition, grades on CT scans performed immediately after operation may be judged to be lower than the actual value, because the subarachnoid space is irrigated with abundant lactated Ringer's solution during surgery. It should be noted that there is a difference between preoperative and postoperative grades. Fisher, eta[., 3 observed a higher incidence of vasospasm of the ACA compared to the MCA, and Siiveland, et al., 2~ reported that five of their I00 patients with aneurysmal who developed permanent symptomatic vasospasm had aneurysms of the ACA complex. As for the operative approach to the ACA territory, in cases of s II and III at the basal frontal IHF, the angiographic vasospasm grades of the A2 were significantly lower when the interhemispheric approach had been used than with the pterional approach. When the was Grade III, both symptomatic vasospasm and low-density areas on CT occurred in only two of the eight cases operated on via the interhemispheric approach, while they occurred in 11 and 10, respectively, of the 22 cases with the pterional approach. In cases with ACoA aneurysms, the pterional approach was used at our hospital until December, 1985, and the interhemispheric approach was used thereafter. Therefore, differences in technique as well as approach cannot be denied. However, as stated by Mizukami, et al., ~4 it is difficult to remove subarachnoid blood from the IHF via the pterional approach. The interhemispheric approach 11 may be more useful for prevention of vasospasm of the ACA territory. Taneda, et al., 24 and Wakabayashi and Fujita 26 reported that patients with the pterional approach developed severe vasospasm on the side opposite to the operative approach but that they developed either no or mild vasospasm on the side of surgery. In the present study, with regard to the MI territory, there were no significant differences between the approach side and the opposite side in angiographic vasospasm grades and the incidence of symptomatic vasospasm and low-density areas on CT. With of Grade III, the angiographic vasospasm grades and the incidence of symptomatic vasospasm and low-density area on CT were slightly higher on the operative side. In analyzing these findings, several factors should be taken in consideration. First, symptomatic vasospasm and low-density areas on CT of the MCA territory also depend on the vascular narrowing of the M2 segment of the MCA, and it is difficult to remove subarachnoid blood in the insular cistern where the M2 segments are situated. Second, the sylvian stem lies in a plane horizontal to that of the CT section and, thus, accurate estimation of the amount of subarachnoid blood from CT scans is sometimes limited. 3 In fact, in this study, a better correlation between grade and Hounsfield number was observed in the basal frontal IHF than in the sylvian stem. Third, vasospasm is usually more severe on the side of the ruptured aneurysm. 4,28 In animal experiments, Nosko, et al., 17 and Handa, et al., 6 demonstrated that clot removal 24 hours after induction of, but not later than 48 hours after, completely prevented the development of chronic vasospasm and delayed ischemic deficits in primate models. On the other hand, Alexander, et al.,l reported that cisternal lavage 24 hours after hemorrhage has no effect on the angiographic vasospasm and symptomatic vasospasm in spite of evidence of clot removal as seen at sacrifice. In this clinical study, in cases where is Grade III at the basal frontal IHF, the severity of vasospasm of the A2 territory seems to be lower in cases with surgery on Day 0 than on Days 1 to 3. As a whole, however, no consistent relationship could be found between the timing of operations and vasospasm. The etiology and pathogenesis of vasospasm are still not well understood, and there is no animal model that duplicates all of the key aspects of human cerebral vasospasm. 12'2v Further clinical studies may be necessary to determine the critical time when clot removal is most effective. In cases operated on via the interhemispheric approach, vasospasm of the A2 segments seems to have been reduced by clot removal. However, in cases operated on via the pterional approach, the effect of clot removal on vasospasm of the M~ segments could not be confirmed. Further detailed studies should be done J. Neurosurg. / Volume 72/February,

7 T. Inagawa, M. Yamamoto, and K. Kamiya to clarify if clot removal per se is effective in preventing or ameliorating the narrowing of blood vessels. References 1. Alexander E IIl, Black PM, Liszczak TM, et al: Delayed CSF lavage for arteriographic and morphological vasospasm after experimental. J Neurosurg 63: , Auer LM: Acute operation and preventive nimodipine improve outcome in patients with ruptured cerebral aneurysms. Neurosurgery 15:57-66, Fisher CM, Kistler JP, Davis JM: Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 6: 1-9, Fisher CM, Roberson GH, Ojemann RG: Cerebral vasospasm with ruptured saccular aneurysm -- the clinical manifestations. Neurosurgery 1: , Fujita S: Computed tomographic grading with Hounsfield number related to delayed vasospasm in cases of ruptured cerebral aneurysm. Neurosurgery 17: , Handa Y, Weir BKA, Nosko M, et al: The effect of timing of clot removal on chronic vasospasm in a primate model. J Neurosurg 67: , Hashi K, Nin K, Shimotake K: Surgery in the prevasospastic interval. Acta Nenrochir 63: , Hunt WE, Hess RM: Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg 28:14-20, Inagawa T, Yamamoto M, Kamiya K, et al: Management of elderly patients with aneurysmal subarachnoid hemorrhage. J Neurosurg 69: , Ito U, Tomita H, Yamazaki S, et al: Enhanced cisternal drainage and cerebral vasospasm in early aneurysm surgery. Acta Neurochir 80:18-23, Ito Z: The microsurgical anterior interhemispheric approach suitably applied to ruptured aneurysms of the anterior communicating artery in the acute stage. Acta Neurochir 63:85-99, Kassell NF, Sasaki T, Colohan ART, et al: Cerebral vasospasm following aneurysmal subarachnoid hemorrhage. Stroke 16: , Kawakami Y, Shimamura Y: Cisternal drainage after early operation of ruptured intracranial aneurysm. Neurosurgery 20:8-14, Mizukami M, Kawase T, Usami T, et al: Prevention of vasospasm by early operation with removal of subarachnoid blood. Neurosurgery 10: , Mizukami M, Takemae T, Tazawa T, et al: Value of computed tomography in the prediction of cerebral vasospasm after aneurysm rupture. Neurosurgery 7: , Mohsen F, Pomonis S, Illingworth R: Prediction of delayed cerebral ischemia after subarachnoid hemorrhage by computed tomography. 3 Neurol Nenrosnrg Psychiatry 47: , Nosko M, Weir BKA, Lunt A, et al: Effect of clot removal at 24 hours on chronic vasospasm after in the primate model. J Neurosurg 66: , t Pasqualin A, Rosta L, Da Plan R, et al: Role of computed tomography in the management of vasospasm after subarachnoid hemorrhage. Neurosurgery 15: , Saito I, Sano K: Vasospasm following rupture of cerebral aneurysms. Neuroi Med Chit 19: , Saito I, Ueda I, Sano K: Significance of vasospasm in the treatment of ruptured intracranial aneurysms. 3 Neurosurg 47: , Sfiveland H, Ljunggren B, Brandt L, et al: Delayed ischemic deterioration in patients with early aneurysm operation and intravenous nimodipine. Neurosurgery 18: , Suzuki J, Yoshimoto T, Onuma T: Early operations for ruptured intracranial aneurysms -- study of 31 cases operated on within the first four days after ruptured aneurysms. Neurol Med Chir 18:83-89, Taneda M: Effect of early operation for ruptured aneurysms on prevention of delayed ischemic symptoms. J Neurosnrg 57: , Taneda M, Wakayama A, Ozaki K, et al: Biphasic occurrence of delayed ischemia after early aneurysm surgery. Case report. J Nenrosurg 58: , Van der Werf AJM: Clinical aspects of subarachnoid hemorrhage and significance of vasospasm. Psychiatr Neurol Neurochir 75: , Wakabayashi T, Fujita S: Removal of subarachnoid blood clots after subarachnoid hemorrhage. Surg Neurol 21: , Wilkins RH: Attempts at prevention or treatment of intracranial arterial spasm: an update. Neurosurgery 18: , Wilkins RH, Alexander JA, Odom GL: Intracranial arterial spasm: a clinical analysis. 3 Neurosurg 29: , Yamamoto I, Hara M, Ogura K, et al: Early operation for ruptured intracranial aneurysms: comparative study with computed tomography. Neurosurgery 12: , Ya~argil MG, Fox JL: The microsurgical approach to intracranial aneurysms. Surg Neurol 3:7-14, 1975 Manuscript received June 5, Accepted in final form July 24, Address reprint requests to: Tetsuji lnagawa, M.D., Department of Neurosurgery, Shimane Prefectural Central Hospital, 116 Imaichi-cho, Izumo, Shimane 693, Japan. 230 J. Neurosurg. / Volume 72/Febntarv, 1990

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