Cerebral aneurysm

The relationship between changes of blood flow velocities in cerebral arteries measured by transcranial Doppler ultrasonography and aneurysm localization was investigated in a group of 165 patients after aneurysmal subarachnoid hemorrhage (SAN). Mean blood flow velocities (MFV) in the middle cerebral artery (MCA) and anterior cerebral artery (ACA) were registered. In patients with aneurysm of internal carotid artery and MCA (group A) statistically significant higher values of MFV from the Ist to the 5th day and on the 12th, 13th, 14th, 15th, and 19th day after SAH were found compared to patients with aneurysm of the anterior communicating artery, ACA, and pericallosal artery (group B). Pathological values of MFV exceeding 120 cm sec-I in MCA were registered during 14 days in group A and during eight days in group B. Blood flow velocities in ACA were statistically significantly higher in group B on the 2nd, 7th, 9th and 11 th day compared to group A. Pathological values of MFV exceeding 90 cm sec-' in ACA were registered during nine days in both groups. MFV differences between group A and group B in 38 patients subjected to delayed surgery were not observed. The influence of aneurysm localization was observed between the 7th and 14th day after SAH. Critical MFV values for vasospasm in the MCA should be 120 cm sec-1 and in the ACA 90 cm sec . [Neurol Res 2001; 23: 23-28]

Keywords: Cerebral aneurysm; vasospasm; blood flow velocity; subarachnoid hemorrhage; Transcranial Doppler Ultrasonography

INTRODUCTION

Vasospasm of cerebral arteries is the most frequently occurring complication associated with subarachnoid hemorrhage (SAH). The incidence of vasospasm ranges from 28% to 86%'-7. The maximum severity of vasospasm occurs between the 7th and 14th days after SAH and depends on the amount of blood clots in the subarachnoid space' . In 1982 Aaslid et aL introduced transcranial Doppler ultrasonography (TCD) to measure blood flow velocity in cerebral arteries. Since that time the principles for detection and monitoring of vasospasm with TCD have been established. Recent data suggest that blood flow velocity in middle cerebral artery (MCA) allows us to observe precisely the development of vasospasm related to arterial narrowing' 9. The criteria for vasoconstriction in TCD included mean blood flow velocity (MFV) values exceeding 120 cm sec-1, coexisting with normal values of systemic blood pressure, intracranial pressure (ICP), normal pCOZ level and hematocrit level. MFV changes in the MCA are widely used as a basis for vasospasm monitoring in the post-operative period . Many authors'2-16 suggest that the anterior cerebral artery (ACA) is inadequate for the evaluation of vasoconstriction due to the anatomical variability observed in more than 25% of cases and difficulties in the assessment of Al segment. The results of TCD measurement of MFV in ACA should be interpreted carefully. In some cases increased MFV in ACA is related to hyperkinetic blood flow due to the hypoplastic contralateral artery. Moreover, decrease in blood flow velocity does not exclude vasospasm and can be related to difficulties in the Al segment detection by TCD examination 2,14. Vasospasm is mostly observed close to the ruptured aneurysm. In rare cases vasoconstriction is detected in arteries far from the aneurysm sitel.6,12. These data suggest necessity for objective study to compare changes in blood flow velocity between ACA and MCA in relation to localization of the ruptured aneurysm.

We conducted this study to compare blood flow velocity in ACA and in MCA in patients after aneurysmal SAH in relation to aneurysm localization and to evaluate the use of blood flow velocity in ACA in the detection of vasospasm.

MATERIALS AND METHODS

The study was performed in a group of 165 patients (75 men and 78 women) with a mean age of 46 years (range 20-69 years) with aneurysmal SAH treated surgically at the Department of Neurosurgery, School of Medicine in Wroclaw between January 1995 and July 1997. Patients with intracranial hematomas which caused a mass effects and/or with severe brain edema on computed tomography (CT) and in poor neurological condition (V grade of Hunt-Hess scale) were excluded from the analysis. Patients with monitored ICP, in whom ICP exceeded 20 mmHg were not analyzed. Cases of angiographically documented arterial stenosis not related to vasospasm, vascular occlusion, hypoplasia or aplasia were also not included in the study. The neurological status was assessed according to HuntHess scale". Grade IV, III, II, and I were found in 29 (18%), 63 (38%), 62 (37%) and 11 (7%) patients respectively. The number of blood clots in the initial CT was evaluated according to Fisher scales. Grade IV, III, II and I were detected in 52 (31%), 68 (41%), 29 (18%) and 16 (10%) of patients respectively. All patients were divided into two groups according to the localization of the ruptured aneurysm: Group A, patients with aneurysms of the MCA and the internal carotid artery (ICA); Group B, patients with aneurysms of the ACA, anterior communicating artery (ACoA) or pericallosal artery (PA), Table 1.

The blood flow velocity (BFV) was measured by TCD (2000 S/N, Eden Medizinische Electronik GmbH, Uberlingen, Germany) with a pulsed, range-gated 2 MHz probe. The standard transtemporal technique was used to insonate and identify cerebral arteries. TCD examinations were performed every day up to 21 st day after SAH in MCA and in ACA. Cases with 20% difference in MFV between the right and left ACA and with more than 20% difference of MFV in ACA compared to the mean normal values for this artery were excluded from the study. The first TCD examination was performed within 48 h after SAH in patients subjected to early surgery and within 24 h before operation in patients selected for delayed surgery. The maximum of MFV in ACA and in MCA was registered on the operated side as well as on the non-operated side. According to the literature values of MFV exceeding 120 cm sec-1 in MCA were assumed to be diagnostic for vasospasm' . In our group of 50 healthy volunteers (average age 48 years) we found the mean MFV value of about 684 cm sec-1 in MCA and 543 cm sec-1 in ACA. The difference between MFV values between MCA and ACA was about 30%. We assumed MFV of 90 cm sec-1 in ACA to be a borderline value for vasospasm evaluation.

Patients subjected to early surgery were treated with a calcium channel blocker (nimodipine, Bayer) administered intravenously at a dose of 2 mg h during two weeks and later applied orally at a dose of 6x 80 mg day-'. We analyzed MFV measurements only if PC02 and pOz, arterial blood pressure (140160 mmHg), pulse (65-90 min) and hematocrit level (38%-48%) remained unchanged during TCD examination.

Statistical analysis of the data was performed using a set of computer programs STATISTICA. Comparison of the MFV values was performed using the Student' t-test with p

RESULTS

In the group of 165 patients, 127 (77%) were operated within the first 72 h after SAH (early surgery) and 38 (33%) 10 days after SAH (delayed surgery). Pterional approach was used in 142 patients (86%) and anterior interlobar approach in 23 (14%). One aneurysm was detected in 146 patients, two aneurysms in 17 patients, and three in two patients. Results are presented in Table 1.

In patients subjected to early surgery the most pronounced differences between groups A and B were found in MCA on the operated side (Figure 1). In group A mean values of MFV ranged from 76 12 cm sec-1 to 157+23 cm sec-1 (mean 127+27 cm sec-1) and in group B from 64 - 16 cm sec-1 to 135 - 22 cm sec-1 (mean 108 34 cm sec-1). The values of MFV greater than 120 cm sec-1 were observed in group A during 14 days (between the 7th and 18th day after SAH) and in group B during eight days (between the 7th and 14th day after SAH). The differences of MFV values between both groups on the 5th, 12th, 13th, 14th, and 19th day after SAH were statistically significant (p

In patients subjected to delayed surgery higher values of MFV in MCA on the operated side were found in group A (Figure 5). The highest value of MFV in group A was 122 21 cm sec- and in group B 116+19 cm sec-1. The smallest differences of MFV between both groups were detected between the 8th and 14th day after SAH. MFV value exceeding 90 cm sec-1 were not registered during 21 days of observation. The highest value of MFV in group A was 88 11 cm sec-1 and in group B 84 9 cm sec-1. Differences of MFV in MCA and in ACA between both groups were not statistically significant on the nonoperated side.

DISCUSSION

The results of this study show that MFV differences in MCA between patients with MCA and ICA aneurysms (group A) and patients with ACA, ACoA and AP aneurysms (group B) were statistically significant during the first two weeks after SAH. In this period of time MFV differences in ACA between these two groups were not statistically significant. However, between the 8th and 15th day after SAH higher values of MFV in ACA were registered in patients from group B compared to patients from group A. It may indicate that the increase in blood flow velocity both in MCA and ACA occurs more often in case of MCA and ICA aneurysms. On the other hand higher MFV values in ACA than in MCA in group B may suggest that in case of such localization differences are more pronounced in ACA than in MCA in the second week after SAH, when according to the literature the highest incidence of vasospasm is observed'

According to Sloan et al.z3 vasospasm in ACA occurs more often than in MCA in case of ACoA aneurysms. They based the criteria for vasospasm diagnosis in MCA on the values of 110 cm sec-I and more and obtained sensitivity of 85% and specificity of 98%. In case of MFV of 120 cm sec-1 sensitivity and specificity was 59% and 100% respectively. In a group of 40 patients with anterior communicating artery aneurysm rupture Proust et al." found 12 cases of vasospasm. The distribution of angiographically documented vaospasm was 95.5% for ACA, 77.3% for AP and only 59.1% for MCA. They suggest MFV exceeding 80 cm sec-1 to be a borderline value for vasospasm in ACA (Al segment) in TCD examination. They obtained sensitivity of 83.3% and specificity of 75% to the diagnosis of ACA vasospasm by TCD examination. In a group of 41 patients Lennihan et al.12 observed angiographically diagnosed vasospasm of ACA confirmed by TCD examination in six patients. All of them had aneurysms of the anterior communicating artery. Our results and reports of the other authors 12,13,2 suggest that ACA examination appears to be better than MCA in the vasospasm evaluation in patients with aneurysm of the ACoA region. It is also confirmed by Creissard et aLl.", who in 54 patients after aneurysmal SAH observed TCD sensitivity for vasospasm detection of 93% in case of the middle cerebral artery aneurysm rupture and only of 55% in case of the anterior communicating artery rupture.

MFV changes in MCA and ACA were similar in both groups A and B though there were some differences in the registered values. Assuming 120 cm sec-1 as a borderline velocity for vasospasm pathological MFV values in MCA were observed in group A during 14 days and in group B only during 8 days. If MFV values in MCA and ACA are interpreted similarly then no pathological MFV values in ACA are observed during three weeks after SAH. But the maximum MFV values measured in ACA were more than 75% and more than 80% higher in group A and group B respectively compared to the initial values. MFV values in ACA are much lower than those in MCA under physiological conditions. We assumed 68 4 cm sec-I in MCA and 54 3 cm sec-1 in ACA to be the normal MFV values. If 120 cm sec-1 as an assumed borderline value for vasospasm in MCA, means an increase of the normal value by 70%, then 90 cm sec-1 in ACA is also an increase of the normal value by approximately 70%, and can be considered as a borderline value for vasospasm in ACA. Using the new borderline MFV value for vasospasm in ACA pathological values were observed over the period of nine days in group A (between the 6th and 14th day after SAH) and in group B (between the 7th and 15th day after SAH). Lennihan et al.12 evaluated sensitivity and specificity of TCD examination of MFV in MCA and ACA (patients with angiographically diagnosed vasospasm had MFV of 120 cm sec-' and 140 cm sec-1 respectively). Using 140 cm sec-1 as borderline value for vasospasm in MCA they obtained sensitivity of 86% and specificity of 96%. In case of 120 cm sec-1 sensitivity remained unchanged and specificity dropped to 86%. In case of ACA sensitivity was 13% and specificity was 100% when the borderline MFV value for vasospasm of 140 cm sec-1 was used. Sensitivity remained unchanged but specificity dropped to 96% for 120 cm sec-'.

In our group of patients subjected to early surgery angiography was performed within the first 48 h after SAH. According to the literature vasospasm occurs very rarely in this period'6,20. Angiographically documented vasospasm was found in only 12 patients in a group of 127 patients, confirmed in all cases by TCD examination. In this subgroup 8 patients with MCA and ICA aneurysms had pathological MFV in MCA (mean value of 147 22 cm sec-') and slightly elevated MFV in ACA (mean MFV value 79+16 cm sec-'). From a subgroup of four patients with the ACoA region aneurysms one patient had MFV exceeding 120 cm sec-', the other three patients had MFV values exceeding 90 cm sec-1. Grosset et al.5 compared TCD examination with the results of angiography performed within 24 h after SAH in 102 patients and found statistically significant correlation between the MCA diameter and blood flow velocity in MCA. No such correlation was observed in ACA.

Gromulid et aL's found TCD sensitivity of 70% when the borderline value for vasospasm of 120 cm sec-1 was used. The criteria for vasospasm in ACA are different and sensitivity ranges from 13% to 70%. Wozniak et al.15 defined TCD-determined vasospasm in ACA and PCA by MFV of at least 120 cm sec-1 and 90 cm sec-1 respectively. They found sensitivity for ACA vasospasm detection of 18% and specificity of 65%. For PCA sensitivity was 48% and specificity 69%.

The most serious complication of vasospasm is delayed ischemic deficit (DID) occurring in 18% to 47% of patients according to different authors' DID was observed in 27 patients from our group, only one of whom had delayed surgery. In all of them TCD examination was specific for vasospasm. In six patients ischemia in the ACA area was observed. In all cases MFV values in ACA exceeding 90 cm sec-1 were registered during seven days of observation on average (including five cases with MFV in ACA higher than 120 cm sec-1). All these patients had aneurysms of the anterior communicating artery region. The other 21 patients had ischemic changes only in the MCA area (17 patients) and both in ACA and MCA areas (four patients). In this group MCA and ICA aneurysms were found in 18 cases and ACoA region aneurysms in three cases. It turns out that ACA vasospasm registered in TCD (90 cm sec-1 as a borderline value for vasospasm) may lead to DID. The isolated increase of MFV in ACA along with normal or slightly elevated MFV in MCA is observed in 96% of patients with ischemic changes in ACA area. In such cases TCD monitoring of blood flow velocity in MCA would be insufficient to diagnose vasospasm. It is particularly important in case of ACoA region aneurysms. No statistically significant differences in MFV In ACA between groups A and B were found, but there were statistically significant differences in case of MFV in MCA between both groups. Grosset et a1.24 investigated in a group of 121 patients with aneurysmal SAH the correlation between the increased velocities measured by TCD and regional cerebral perfusion defects using SPECT method. They think that the highest velocity usually corresponds to the site of aneurysm and the site of perfusion defect on SPECT. This correlation is clearly stronger for MCA than for ACA. The authors suggest that poor correlation between TCD velocity in ACA and cerebral perfusion is probably due to the collateral capacity of the ACA via the ACoA.

Comparing MFV on the operated and non-operated side, higher MFV values both in ACA and MCA were observed on the operated side. Mechanical irritation of vessels during microsurgical preparation and usually more clots on the operated side probably influence significantly MFV in the examined vesse IS23-25. In patients subjected to delayed surgery no significant MFV differences in ACA and MCA between groups A and B were observed and pathological MFV values were not registered. It may suggest that aneurysm localization and intra-operative irritation of vessels do not have such an important impact upon the MFV changes like the SAH distribution-za. In a group of 113 patients Brint et al.28 demonstrated that aneurysm localization did not predict time to normalization of MFV values measured by TCD. However, the median time to normalization in the SAH absent group was longer if the aneurysm was located in the ICA or ACoA location compared to the MCA or basilar artery (BA). In the SAH present group, the longer time was associated with the aneurysm of ICA or BA.

Summarizing, we suggest that pathological MFV value for vasospasm in ACA of 120 cm sec-I must be verified. We propose 90 cm sec-1 as a borderline value for vasospasm in ACA. Aneurysm localization does not have a statistically significant influence on the occurrence of pathological MFV in ACA and MCA. However, in cases of ACoA region aneurysm higher MFV values in ACA are observed compared to those in MCA. It is particularly important in ACoA aneurysm when symptomatic vasospasm coexist with normal MFV values in MCA. ACA examination in TCD might enable detection of the anterior arteries vasospasm. Our results confirm that monitoring of MFV in MCA remains the basic prognostic factor for vasospasm diagnosis. However, we think that the opinion of Laumer etal.16, that `the MCA is the only artery about which it is possible to draw conclusions concerning the presence of vasospasm from TCD findings' should be carefully interpreted.

CONCLUSION

* The highest MFV values were observed in MCA compared to ACA.

* Differences of MFV values in ACA between patients with ACA, ACoA, AP aneurysm and patients with MCA and ICA aneurysm were not statistically significant, however, from the 8th day after SAH higher values of MFV in patients with ACA, ACoA, and AP aneurysms were found.

* Higher values of MFV were detected on the operated side.

* In patients subjected to early surgery values of MFV were much higher than in patients after delayed operations.

* The effect of aneurysm localization on blood flow velocity in both groups of patients was less clear between the 7th and 14th day after SAH.

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Katarzyna jarus-Dziedzic*, jacek Bogucki* and Wojciech Zubt *Department of Neurosurgery, Medical Research Centre, Polish Academy of Sciences, Warsaw tDepartment of Neurosurgery, School of Medicine, Wroclaw, Poland

Correspondence and reprint requests to: Katarzyna larus-Dziedzic, MD, Department of Neurosurgery, Medical Research Centre, Polish Academy of Sciences, Barska str. 16/20, 02-315 Warsaw, Poland. Accepted for publication April 2000.

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