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Subarachnoid hemorrhage on computed tomography scanning and the development of cerebral vasospasm: the Fisher grade revisited
Surgical Neurology 63 (2005) 229 – 235 www.surgicalneurology-online.com
Subarachnoid hemorrhage on computed tomography scanning and the development of cerebral vasospasm: the Fisher grade revisited Michael L. Smith, MDa,*, John M. Abrahams, MDb, Sid Chandela, MDb Michelle J. Smith, MDa, Robert W. Hurst, MDa, Peter D. Le Roux, MDa a
Department of Neurosurgery, Hospital of the University of Pennsylvania, Philadelphia, PA 19146, USA b Department of Neurosurgery, Albert Einstein College of Medicine, New York, NY 10461, USA Received 2 February 2004; accepted 2 June 2004
Abstract
Background: The Fisher grade (FG) is widely used to predict cerebral vasospasm after aneurysmal subarachnoid hemorrhage (SAH). We revisited the grading scale to determine its validity in the era of modern management. Methods: We retrospectively reviewed the records of 134 patients with SAH. The amount and distribution of subarachnoid blood on admission computed tomography (CT) scan was quantified according to the FG and compared with development of symptomatic vasospasm. Results: We reviewed 134 patients (median age, 54) who presented with aneurysmal SAH. Six (5%) were FG 1, 34 (25%) were FG 2, 25 (19%) were FG 3, and 69 (51%) were FG 4. Symptomatic vasospasm developed in no (0%) FG 1, 8 (24%) FG 2, 7 (28 %) FG 3, and 13 (19%) FG 4 patients (28 of 134 total patients; 21%). Development of symptomatic vasospasm was not associated with admission FG, Hunt and Hess grade, age, sex, or location of blood on presenting CT scan. Elevated transcranial Doppler blood flow velocity was associated with blood in the basal cisterns ( P = .0047), lateral ventricles ( P = .026), or blood in any ventricle ( P = .04). Postoperative angiograms were obtained in 57 patients; moderate to severe vasospasm was observed in 5 (15%) FG 2, 6 (24%) FG 3, and 14 (20%) FG 4 patients. Twenty patients (71%) with symptomatic vasospasm had moderate or severe angiographic vasospasm. Angiographic vasospasm was associated with intraventricular blood ( P = .054) but not with FG. Conclusions: Symptomatic vasospasm occurred in 21% of cases. The FG correlated with symptomatic vasospasm in only half the patients. A new predictive CT grading scale for vasospasm may be necessary. D 2005 Elsevier Inc. All rights reserved.
Keywords:
Aneurysm; Cerebral vasospasm; Fisher grade; Subarachnoid hemorrhage
1. Introduction Delayed cerebral ischemia from cerebral artery vasospasm after aneurysmal subarachnoid hemorrhage (SAH) is a known cause of morbidity and mortality. It is important to predict which patients are at risk for vasospasm, because its management relies significantly on prevention. The Fisher computed tomographic grading scale described by Fisher et al [4] in 1980 is widely used to predict which patients are at * Corresponding author. Tel.: +1 215 662 3487; fax: +1 215 349 5534. E-mail address: [email protected] (M.L. Smith). 0090-3019/$ – see front matter D 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.surneu.2004.06.017
risk to develop delayed cerebral ischemia (Table 1). The grading scale described the amount and distribution of subarachnoid blood seen on initial head computed tomography (CT) as it correlated to the development of cerebral vasospasm. Fisher et al found that symptomatic vasospasm only tended to occur in the major subarachnoid blood vessels that were initially surrounded by a thick subarachnoid clot. Though the original manuscript described the findings as preliminary, the scale derived from the 4 groupings of Fisher et al has become a standard tool for initial patient evaluation and prediction of likelihood of delayed cerebral ischemia after SAH.
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Table 1 The 4 Fisher groups Fisher group
Appearance of SAH on head CT
1 2 3 4
No subarachnoid blood visualized Diffuse or thin sheets (vertical layers b1 mm thick) Localized clot and/or vertical layers (z1 mm thick) Diffuse or no SAH, but with intraventricular or intraparenchymal clot
Evaluation and treatment of patients with ruptured aneurysms have evolved the description of the Fisher grade (FG) in 1980. Modern CT scanners have significantly improved resolution for small volumes of intracranial blood compared to those available in 1980. In addition, less than half the patients included in the Fisher et al [4] study had their CT scan on the day of aneurysm rupture. Today, most patients are evaluated and imaged on the day of hemorrhage. Significant changes in treatment include early aneurysm occlusion, the use of calcium channel blockers, which may improve clinical outcome in aneurysmal SAH, and using hypervolemic, hypertensive, hemodilution (triple bHQ) therapy at the onset of documented vasospasm in an attempt to maximize perfusion to areas of brain fed by spastic vessels. These management strategies were not used in 1980. Also, supplemental studies such as transcranial Doppler sonography (TCD) developed during the past decade now play an important role in assessing patients for vasospasm. In view of this it is important to determine whether the FG is a useful tool to predict vasospasm in the modern era. In this study, we retrospectively reviewed the medical records, CT scans, angiograms, and TCD findings of 134 consecutive patients with aneurysmal SAH to determine whether the FG reliably predicts vasospasm. Our results suggest that the FG may need to be revised. 2. Patients and methods 2.1. Patient population We retrospectively reviewed the medical records including hospital charts, CT scans, angiograms, and TCD findings of 134 consecutive patients with a diagnosis of SAH treated at the Hospital of the University of Pennsylvania. Patients with SAH due to trauma, arteriovenous malformations, or of unknown etiology were excluded from the study. Subarachnoid hemorrhage was diagnosed by either CT scanning or lumbar puncture. Patient demographics, date of SAH, day of CT scan, FG, and Hunt and Hess grade were recorded. The date of the hemorrhage was considered day 1 and day of CT scan was recorded relative to this. 2.2. Treatment All patients were treated according to standard protocol, including preoperative resuscitation, early aneurysm occlusion using coil embolization or surgical clipping, and aggressive prevention and treatment of vasospasm. All patients were cared for in the neurosurgical intensive care
unit with invasive hemodynamic monitoring. All patients received nimodipine and phenytoin. Transcranial Doppler sonography was obtained every other day for 14 days and every day for patients suspected of having symptomatic vasospasm. We define symptomatic vasospasm as a clinical entity that includes a new, delayed focal neurologic deficit or mental status decline in the postoperative period without evidence of hydrocephalus, metabolic abnormality, fever, or other systemic factors. It was not quantified by an absolute middle cerebral artery (MCA) blood flow velocity (BFV) with TCD analysis and was made strictly by clinical criteria. If patients became symptomatic from clinically suspected cerebral vasospasm, mean arterial blood pressure was elevated and intravenous fluid resuscitation was maintained in keeping with the triple H therapy. If symptoms did not resolve, patients were taken for angiography. Transcranial Doppler sonography BFV in the MCA was evaluated using a scale of 0 for normal (BFV b 90 cm/s), 1 for mild spasm (BFV = 90 -120 cm/s), 2 for moderate spasm (BFV = 120- 200 cm/s), and 3 for severe spasm (BFV N 200 cm/s). We tabulated the results from the MCA BVF findings for the purpose of this study. Transcranial Doppler sonography analysis was done on each patient assessing BFV in all vessels but we used MCA BFV for the statistical analysis. Each patient was administered 0.9% normal saline and 5% albumin to maintain central venous pressure greater than 8 mm Hg. CT scanning was used to examine patients who demonstrated clinical deterioration. When vasospasm was thought to be the cause of clinical deterioration, hypertensive and hypervolemic therapy was started to maintain systolic blood pressure greater than 180 mm Hg. The diagnosis of symptomatic cerebral vasospasm was confirmed using angiography. When clinical deterioration persisted despite medical management, patients underwent papaverine infusion, balloon angioplasty, or both. 2.3. CT scanning Computed tomography scans were obtained on a General Electric Light Speed Scanner according to standard protocols. Each CT scan was examined by 2 independent observers and in different orders. Cases leading to disagreement between observers were reviewed by both observers together to reach a consensus. The CT scans were examined using the FG—grade 1: none or minimal blood detected; grade 2: diffuse thin layers of subarachnoid blood with layers less than 1 mm thick; grade 3: localized clot and/or thick layers of subarachnoid blood greater than 1 mm thick; grade 4: intracerebral or intraventricular with no or diffuse subarachnoid blood. Blood was also evaluated based on location: Sylvian fissure, interhemispheric fissure, basal cisterns, third ventricle, fourth ventricle, lateral ventricle(s), and the presence of intraparenchymal clot. 2.4. Angiography All patients underwent pretreatment digital subtraction angiography. Aneurysm size and location were recorded.
M.L. Smith et al. / Surgical Neurology 63 (2005) 229 – 235 Table 2 Patient demographics for all patients and those stratified as symptomatic vasospasm All patients
Symptomatic vasospasm
Asymptomatic
134 40/94 16-82 54.4
28 (21%)a 7/21 35-78 51.8
106 (79%)b 33/73 16-82 55.0
Hunt and Hess grade 1 57 2 16 3 29 4 25 5 7
10 5 5 8 0
(18%) (31%) (17%) (32%) ( 0 %)
47 (82%) 11 (69%) 24 (83%) 17 (68%) 7 (100%)
Fisher grade 1 2 3 4
0 8 7 13
( 0%) (24%) (28%) (19%)
6 26 18 56
No. of patients Male/female Age (y) Mean (y)
a b
6 34 25 69
(100%) (76%) (22%) (81%)
Percentage of ball patientsQ who develop symptomatic vasospasm. Percentage of ball patientsQ without signs or symptoms of vasospasm.
Posttreatment angiograms were obtained when vasospasm was suspected as the cause for delayed neurologic deterioration. Angiograms were evaluated by 2 independent observers unaware of the CT FG and classified according to the following scale by comparing pre- and posttreatment studies: 0 for no spasm; 1 for mild spasm (b 25% arterial narrowing); 2 for moderate spasm (25 - 50% arterial narrowing); and 3 for severe spasm (N 50% arterial narrowing). Vasospasm was qualified as the most severe narrowing in any one vessel, independent of the number of other vessels affected. 2.5. Statistical analysis Data are represented as means F SDs or, where samples depart from normal distributions, as a median. The Student t test was used to test differences between groups when the data were normally distributed. The Mann-Whitney procedure was used to examine data that departed from a normal distribution. Both univariate and bivariate analyses were done using analysis of variance, Student t test, and a Pearson v 2 test. The Fischer exact test was substituted when one or more cells had frequencies less than 5. Statistical significance was set at a probability value less than .05. All statistical analyses were performed using commercially available software (SAS Proprietary Software, Version 8, 1999, SAS Institute, Cary, NC). 3. Results 3.1. Patients There were 134 patients, including 40 males and 94 females (median age, 54 years; range, 16-82 years) (Table 2). The FGs and Hunt and Hess grades are listed in Table 2. All patients underwent preoperative digital subtraction angiog-
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raphy except one patient who presented with a large temporal hematoma that required emergent evacuation. In this patient, the presence of an aneurysm was confirmed intraoperatively. There were 116 anterior circulation and 18 posterior circulation ruptured aneurysms. Twenty patients underwent coil embolization (15%) and 114 (85%) underwent surgical clipping. 3.2. Fisher grade and CT scan Twenty-eight patients (21%) developed symptomatic vasospasm. Of these, 8 were FG 2, 7 were FG 3, and 13 were FG 4. The severity of SAH identified on initial CT scan was not associated with symptomatic vasospasm ( P = .50). In both univariate and bivariate analyses, development of symptomatic vasospasm was not associated with admission FG, Hunt and Hess grade, age, sex, or location of blood on presenting CT scan. One hundred eleven (83%) patients had their initial CT scan on the day of SAH (day 1), 6 on day 2, 6 on day 3, 2 on day 4, 3 on day 5, and 6 between days 6 and 9 after SAH. Twenty-one of 28 (75%) patients with symptomatic vasospasm and 90 of 106 (85%) patients without symptomatic vasospasm had their initial CT scan on the day of SAH with no significant difference between groups ( P = .67). The location of subarachnoid blood was similar in patients who developed symptomatic vasospasm and those who were asymptomatic (Table 3) ( P values ranged from .41 to .82 for the different locations analyzed and listed in Table 3). Symptomatic vasospasm developed in 8 of 28 patients (29%) with a focal homogenous collection of subarachnoid blood greater than 10 mm in diameter. Symptomatic vasospasm developed in 15% of patients who did not have focal clots. 3.3. Fisher grade and TCD All patients underwent serial TCD examinations. In those patients with at least 1 episode of TCD BFV greater than 200 cm/s (n = 14), 6 patients (38%) developed symptomatic vasospasm (Table 4). In both univariate and bivariate analyses, elevated TCD MCA BFV was not associated with Table 3 Subarachnoid blood distribution on initial CT scan All patients Unilateral Sylvian fissure blood Bilateral Sylvian fissure blood Interhemispheric blood Basal cisterns Third ventricle Fourth ventricle Lateral ventricle Intraparenchymal clot a
34
Symptomatic vasospasm 6 (18%)a
Asymptomatic 28
55
13 (24%)
42
35
8 (23%)
27
76 16 24 49 28
18 (24%) 2 (13%) 4 (17%) 11 (22%) 8 (29%)
58 14 20 38 20
Percentage of ball patientsQ who develop symptomatic vasospasm.
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Table 4 Assessment of vasospasm using TCD and angiography All patients Elevated TCD None Mild Moderate Severe
85 24 11 14
Preoperative angiogram None 120 Mild 11 Moderate 1 Severe 1
Symptomatic vasospasm 12 8 2 6
(14%)a (33%) (18%) (43%)
73 16 9 8
23 4 1 0
(19%) (36%) (100%) (0%)
97 7 0 1
Postoperative angiogram (n = 57) None 20 2 (10%) Mild 12 3 (25%) Moderate 11 8 (73%) Severe 14 12 (86%) a
Asymptomatic
18 9 3 2
Percentage of ball patientsQ who develop symptomatic vasospasm.
admission FG, Hunt and Hess grade, age, or sex. A significant association was observed between elevated TCD MCA BFV and symptomatic ( P = .005) or angiographic vasospasm ( P = .001). A significant relationship also was observed between increased TCD MCA BFV and the location of blood on initial CT; blood in the basal cisterns ( P = .0047), lateral ventricles ( P = .026), or in any ventricle ( P = .04) was associated with elevated TCD velocities. 3.4. Fisher grade and angiography On preoperative angiograms (n = 133), 11 (8%) patients had mild vasospasm, 1 patient had moderate vasospasm, and 1 patient had severe vasospasm. Fifty-seven (43%) patients underwent postoperative angiography between 3 and 18 days (mean = 6 days) after SAH. Angiographic vasospasm was identified in 37 (65%) patients, including 12 (21%) with mild, 11 (19%) with moderate, and 14 (25%) with severe angiographic vasospasm. In patients with severe angiographic MCA vasospasm, all had TCD MCA BFV greater than 200 cm/s. In contrast, BFV was less than 200 cm/s in all patients with mild or moderate vasospasm. Among the patients who developed symptomatic vasospasm, moderate to severe angiographic vasospasm was observed in 5 patients with FG 2, 6 patients with FG 3, and 9 patients with FG 4 SAH. Our results suggest that there is a statistically significant association between symptomatic vasospasm and angiographic vasospasm. However, only 43% of our patients had postoperative angiograms depending on surgeon preference. The results must be interpreted keeping this in mind. In univariate and bivariate analysis the severity of angiographic vasospasm was not predicted by the severity of SAH classified by the FG on initial head CT scan. In addition, no significant association was observed between angiographic vasospasm and admission FG, Hunt and Hess grade, age, or sex. A significant association was observed between angiographic vasospasm and symptomatic vaso-
spasm ( P b .0001) and elevated TCD MCA BFV ( P = .001). There also was a strong association between angiographic vasospasm and intraventricular blood ( P = .054).
4. Discussion In this retrospective study, we evaluated the CT, angiographic, and TCD findings of 134 patients with aneurysmal SAH to determine whether the initial CT severity of SAH determined by the FG predicts symptomatic cerebral vasospasm. The study was undertaken because there have been significant advances in neurologic imaging and in SAH management since the FG was devised more than 20 years ago that may now bias or invalidate the accuracy of the original grading system. Our results suggest that the FG may not be valid in the modern era. 4.1. Contemporary management of cerebral vasospasm There are several important differences between this study and that which led to the development of the FG. First, neurologic imaging is now more sophisticated. Second, among the 47 patients examined by Fisher et al [4], more than half (26/47) underwent CT scanning in the days after SAH with delayed diagnosis and treatment. In contrast, 83% of the patients (111/134) in our study underwent CT scan on the day of SAH and with the minority of patients having their initial CT scan days after hemorrhage. However, this did not influence our results because 75% of the patients in our study who developed symptomatic vasospasm had their initial CT scan on the day of SAH whereas 85% who did not develop vasospasm did the same. Third, vasospasm prevention and management has changed significantly in the last 20 years. Nearly half of the patients (23/47) included in the Fisher et al [4] study developed symptomatic vasospasm whereas 21% of our patients developed symptomatic vasospasm. Finally, most patients in our series underwent treatment within 3 days of SAH whereas patients examined by Fisher et al [4] had delayed surgery. 4.2. Transcranial Doppler sonography The value of TCD is debated by some. However, rapid and sequential increase in BFV or MCA BFV greater than 200 cm/s is highly correlated with angiographic vasospasm [7,11]. In our study, elevated TCD BFV in the MCA was predictive of angiographic and symptomatic vasospasm. In addition, elevated TCD BFV was significantly correlated with the presence of blood in the basal cisterns, blood in the lateral ventricle, and blood in any ventricle. Other investigators who have recently evaluated predictive factors for vasospasm have also observed a strong association between an early increase in TCD BFV greater than 140 cm/s and vasospasm [3,8]. Seventy-five percent of our patients with TCD evidence of vasospasm who underwent postoperative angiography had angiographic vasospasm.
M.L. Smith et al. / Surgical Neurology 63 (2005) 229 – 235
Although the association between large amounts of subarachnoid blood and vasospasm is well known, our results, as well as those from other studies, have found similar limitations to the FG [3,9]. For example, Schaller et al [9] observed that there was limited association between severe vasospasm identified by TCD and the FG. In that study, severe vasospasm documented by TCD (MCA BFV N160 cm/s on 2 or more consecutive days) was observed in 39% of FG 1 patients, 26% of FG 2 patients, and 34% of FG 3 patients. The authors concluded that the amount of subarachnoid blood identified on the initial CT scan should no longer be used as an indicator to predict symptomatic vasospasm. 4.3. Volume of subarachnoid blood We did not observe a clear association between the FG, the presence of blood clot, and the subsequent cerebral vasospasm. In those patients with intraparenchymal or Sylvian fissure clot, only 8 of 28 patients (29%) developed symptomatic vasospasm. We did not observe a characteristic subarachnoid blood pattern that predicted those patients at high risk for symptomatic vasospasm. We did observe a relationship between intraventricular blood and vasospasm. The amount of blood alone is not the only factor that influences whether someone becomes symptomatic. For example, advanced age is associated with a reduced incidence of vasospasm [12], whereas cigarette smoking may increase the risk of vasospasm [6]. However, this does not exclude the possibility that the overall blood volume rather than distribution may be the more important factor. Friedman et al [5] recently used standard image analysis software to quantify the volume of blood in FG 3 patients with SAH; a significantly greater volume of cisternal blood was observed among patients with symptomatic vasospasm. Intraparenchymal and intraventricular blood was not associated with vasospasm. Our results were consistent with their findings in that elevated TCD BFV in the MCA was associated with blood in the basal cisterns and lateral ventricles. In contrast, others have shown that blood in both ventricles is associated with later vasospasm [3,10]. Why intraventricular hemorrhage is associated with vasospasm however is not certain. This is consistent with a particular volume of subarachnoid blood rather than distribution alone being important in the development of vasospasm and recent studies that demonstrate that thick clot filling any cistern or fissure is significantly associated with vasospasm [1-3,8,10]. Blood filling a cistern was not considered as an independent factor in the FG. 4.4. Study limitations The purpose of this study was to use a retrospective cohort to support evidence that the FG may need to be revisited and developed further to accommodate for contemporary management. However, this study presents a number of limitations. First, although our study is a retrospective review and this may lessen its credibility when compared to a prospective cohort, we do not propose a new
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grading scale based on these early findings. Second, there was no correlation in the development of symptomatic vasospasm to the Hunt and Hess grading scale, another standard in the evaluation of these patients. One reason for this discrepancy could be inherent in the difficulty assessing Hunt and Hess grade 4 and 5 patients for the development of symptomatic vasospasm. For these patients, assessment relies heavily on TCD evaluation and we did not select out this cohort for a separate analysis. Third, based on these initial findings a prospective study should be developed with the intent of developing a new grading system. Finally, until software becomes available such that quantification of blood volume with admission CT is easy to perform and with high accuracy, a prospective study may be difficult to perform. 5. Conclusions The FG did not reliably predict symptomatic vasospasm in this series of patients. The only admission CT finding that seemed to predict symptomatic vasospasm was intraventricular blood. There was no correlation between volume of a subarachnoid blood clot and development of symptomatic vasospasm. Our results do support the correlation of TCD findings to the development of both symptomatic and angiographic vasospasm. For those patients who did develop symptomatic vasospasm, there were more patients in the combined group with FGs 2 (n = 8) and 3 (n = 7) when compared to patients with FG 4 (n = 13). Taken together our data and that of other recent investigations suggest that although the FG is useful it may need revision to reflect modern neurologic imaging and to provide help in vasospasm management. References [1] Adams HP, Kassell NF, Torner JC, et al. Predicting cerebral ischemia after aneurysmal subarachnoid hemorrhage: influences of clinical condition, CT results, and antifibrinolytic therapy. A report of the Cooperative Aneurysm Study. Neurology 1987;37:1586 - 91. [2] Bonhila L, Marques EL, Carelli EF, et al. Risk factors and outcome in 100 patients with aneurysmal subarachnoid hemorrhage. Arq Neuropsiquiatr 2001;59:767 - 80. [3] Claassen J, Bernardini GL, Kreiter K, et al. Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the Fisher scale revisited. Stroke 2001;32:2012 - 20. [4] Fisher CM, Kistler JP, Davis JM. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 1981;6:1 - 9. [5] Friedman JA, Goerss SJ, Meyer FB, et al. Volumetric quantification of Fisher Grade 3 aneurysmal subarachnoid hemorrhage: a novel method to predict symptomatic vasospasm on admission computerized tomography scans. J Neurosurg 2002;97:401 - 7. [6] Lasner TM, Weil RJ, Riina HA, et al. Cigarette smoking-induced increase in the risk of symptomatic vasospasm after aneurysmal subarachnoid hemorrhage. J Neurosurg 1997;87:381 - 4. [7] Newell DW, Grady MS, Eskridge JM, et al. Distribution of angiographic vasospasm after subarachnoid hemorrhage: implications for diagnosis by transcranial Doppler ultrasonography. Neurosurgery 1990;27:574 - 7. [8] Qureshi AI, Sung GY, Razumovsky AY, et al. Early identification of patients at risk for symptomatic vasospasm after aneurysmal subarachnoid hemorrhage. Crit Care Med 2000;28:984 - 90.
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Smith et al reviewed 134 patients with SAH and found no correlation of the admission FG with the development of symptomatic vasospasm. Table 2 displays these results nicely. The authors question the validity of the FG in predicting the risk of vasospasm, given modern CT imaging. There are significant differences between this study and that of Fisher et al [1] 24 years ago. Most notably, all the patients in the first study underwent postoperative angiography whereas only 47% of patients in this present study underwent this test. It can only be assumed that postoperative angiography was selectively used in a manner that biased the performance of this test toward patients with clinical (or bsymptomaticQ) vasospasm. Therefore, the finding of ba significant association . . . between angiographic vasospasm and symptomatic vasospasm . . .Q is irrelevant. Similarly, the association between angiographic spasm and elevated TCD MCA BFV is suspect. The authors propose a prospective study b. . . with the intent of developing a new grading system.Q It is unclear what the authors intend to grade because the only predictor of vasospasm in their study was intraventricular blood. Has the pathophysiology of SAH changed? Maybe the mastery of clinical neurology of CM Fisher explains the higher incidence of symptomatic cerebral ischemia in his series. Stated another way, it may be that as we rely more on radiographic imaging, we simultaneously require more obvious signs of neurologic dysfunction to prod us to order tests that confirm our crude bedside findings. Whether true or not, we choose to agree with the authors that it is improvements in medical management that have reduced the incidence of vasospasm after SAH.
Fisher and colleagues were among the first to publish clinical data relating the volume and location of subarachnoid blood to the risk of cerebral vasospasm [3,8]. The technology used by Fisher et al obviously is outdated, but one cannot argue with several decades of clinical and experimental data that strongly support, if not prove, that angiographic arterial narrowing after SAH is related in part to the volume of clot next to the artery that develops vasospasm [7]. A review of the 1980 paper shows that the computed tomograms were obtained within 5 days of SAH on a scanner with a 160 160 matrix and 16-mm-thick slices. Current imaging has more than 10 times this resolution. The thickness of the clots refers to measurements made on the printed images that had been printed at variable sizes. No magnification standard was included. Therefore, the 1-mm distinction between groups 2 and 3 is not equivalent to an actual 1 mm measured on a CT scan today. With current scanners, a negative head CT scan result within a day of SAH is uncommon (FG 1) and clots with real thickness less than 1 mm also are uncommon (FG 2). I suspect most neurosurgeons distinguish grades 2 and 3 by relatively thin vs relatively thick clots, which was the qualitative system used in more recent clinical trials [5]. The paper by Smith and colleagues found it difficult to correlate FG and vasospasm. This may be because the method for differentiating the FGs in this study is not entirely clear, and the distribution of patients is different from some other series since there is a high percentage of FG 4 patients in this study. In addition, the study is an attempt to correlate 2 imprecisely measured phenomena. The SAH on CT measured by the Fisher scale is only a rough estimate and would be better measured quantitatively using a method such as that used by Friedman et al [4]. The assessment of vasospasm was also imprecise and did not use the gold standard catheter angiography in all cases. In addition, other factors influence the risk of vasospasm, such as the density and duration of persistence of the subarachnoid clot, the presence of intraventricular hemorrhage, the clinical grade, and possibly smoking [1,2,6,9]. This paper is important because it highlights the limitations of the Fisher scale and hopefully will stimulate, as mentioned by the authors, the development of software to easily quantify clot volume and density when the initial CT is acquired, or some method to better predict vasospasm.
References
References
[1] Fisher CM, Kistler JP, Davis JM. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 1980;6:1 - 9.
[1] Charpentier C, Audibert G, Guillemin F, Civit T, Ducrocq X, Bracard S, Hepner H, Picard L, Laxenaire MC. Multivariate analysis of predictors of cerebral vasospasm occurrence after aneurysmal subarachnoid hemorrhage. Stroke 1999;30:1402 - 8. [2] Claassen J, Bernardini GL, Kreiter K, Bates J, Du YE, Copeland D, Connolly ES, Mayer SA. Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the Fisher scale revisited. Stroke 2001;32:2012 - 20. [3] Fisher CM, Kistler JP, Davis JM. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 1980;6:1 - 9.
[9] Schaller C, Rohde V, Meyer B, et al. Amount of subarachnoid blood and vasospasm: current aspects. A transcranial Doppler study. Acta Neurochir (Wien) 1995;136:67 - 71. [10] Shimoda M, Oda S, Shibata M, et al. Results of early surgical evacuation of packed intraventricular hemorrhage from aneurysm rupture in patients with poor-grade subarachnoid hemorrhage. J Neurosurg 1999;91:408 - 14. [11] Skirboll S, Newell DW. Noninvasive physiologic evaluation of the aneurysm patient. Neurosurg Clin N Am 1998;9:463 - 83. [12] Suzuki A, Yasui N, Hadeishi H, et al. Cerebral vasospasm in aged patients with ruptured intracranial aneurysms. Neurol Med Chir (Tokyo) 1988;28:786 - 90.
Commentary
Duke Samson, MD Christopher L. Taylor, MD Department of Neurosurgery UT Southwestern Medical Center Dallas, TX 75235, USA
Subarachnoid hemorrhage on computed tomography scanning and the development of cerebral vasospasm: the Fisher grade revisited Michael L. Smith, MDa,*, John M. Abrahams, MDb, Sid Chandela, MDb Michelle J. Smith, MDa, Robert W. Hurst, MDa, Peter D. Le Roux, MDa a
Department of Neurosurgery, Hospital of the University of Pennsylvania, Philadelphia, PA 19146, USA b Department of Neurosurgery, Albert Einstein College of Medicine, New York, NY 10461, USA Received 2 February 2004; accepted 2 June 2004
Abstract
Background: The Fisher grade (FG) is widely used to predict cerebral vasospasm after aneurysmal subarachnoid hemorrhage (SAH). We revisited the grading scale to determine its validity in the era of modern management. Methods: We retrospectively reviewed the records of 134 patients with SAH. The amount and distribution of subarachnoid blood on admission computed tomography (CT) scan was quantified according to the FG and compared with development of symptomatic vasospasm. Results: We reviewed 134 patients (median age, 54) who presented with aneurysmal SAH. Six (5%) were FG 1, 34 (25%) were FG 2, 25 (19%) were FG 3, and 69 (51%) were FG 4. Symptomatic vasospasm developed in no (0%) FG 1, 8 (24%) FG 2, 7 (28 %) FG 3, and 13 (19%) FG 4 patients (28 of 134 total patients; 21%). Development of symptomatic vasospasm was not associated with admission FG, Hunt and Hess grade, age, sex, or location of blood on presenting CT scan. Elevated transcranial Doppler blood flow velocity was associated with blood in the basal cisterns ( P = .0047), lateral ventricles ( P = .026), or blood in any ventricle ( P = .04). Postoperative angiograms were obtained in 57 patients; moderate to severe vasospasm was observed in 5 (15%) FG 2, 6 (24%) FG 3, and 14 (20%) FG 4 patients. Twenty patients (71%) with symptomatic vasospasm had moderate or severe angiographic vasospasm. Angiographic vasospasm was associated with intraventricular blood ( P = .054) but not with FG. Conclusions: Symptomatic vasospasm occurred in 21% of cases. The FG correlated with symptomatic vasospasm in only half the patients. A new predictive CT grading scale for vasospasm may be necessary. D 2005 Elsevier Inc. All rights reserved.
Keywords:
Aneurysm; Cerebral vasospasm; Fisher grade; Subarachnoid hemorrhage
1. Introduction Delayed cerebral ischemia from cerebral artery vasospasm after aneurysmal subarachnoid hemorrhage (SAH) is a known cause of morbidity and mortality. It is important to predict which patients are at risk for vasospasm, because its management relies significantly on prevention. The Fisher computed tomographic grading scale described by Fisher et al [4] in 1980 is widely used to predict which patients are at * Corresponding author. Tel.: +1 215 662 3487; fax: +1 215 349 5534. E-mail address: [email protected] (M.L. Smith). 0090-3019/$ – see front matter D 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.surneu.2004.06.017
risk to develop delayed cerebral ischemia (Table 1). The grading scale described the amount and distribution of subarachnoid blood seen on initial head computed tomography (CT) as it correlated to the development of cerebral vasospasm. Fisher et al found that symptomatic vasospasm only tended to occur in the major subarachnoid blood vessels that were initially surrounded by a thick subarachnoid clot. Though the original manuscript described the findings as preliminary, the scale derived from the 4 groupings of Fisher et al has become a standard tool for initial patient evaluation and prediction of likelihood of delayed cerebral ischemia after SAH.
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Table 1 The 4 Fisher groups Fisher group
Appearance of SAH on head CT
1 2 3 4
No subarachnoid blood visualized Diffuse or thin sheets (vertical layers b1 mm thick) Localized clot and/or vertical layers (z1 mm thick) Diffuse or no SAH, but with intraventricular or intraparenchymal clot
Evaluation and treatment of patients with ruptured aneurysms have evolved the description of the Fisher grade (FG) in 1980. Modern CT scanners have significantly improved resolution for small volumes of intracranial blood compared to those available in 1980. In addition, less than half the patients included in the Fisher et al [4] study had their CT scan on the day of aneurysm rupture. Today, most patients are evaluated and imaged on the day of hemorrhage. Significant changes in treatment include early aneurysm occlusion, the use of calcium channel blockers, which may improve clinical outcome in aneurysmal SAH, and using hypervolemic, hypertensive, hemodilution (triple bHQ) therapy at the onset of documented vasospasm in an attempt to maximize perfusion to areas of brain fed by spastic vessels. These management strategies were not used in 1980. Also, supplemental studies such as transcranial Doppler sonography (TCD) developed during the past decade now play an important role in assessing patients for vasospasm. In view of this it is important to determine whether the FG is a useful tool to predict vasospasm in the modern era. In this study, we retrospectively reviewed the medical records, CT scans, angiograms, and TCD findings of 134 consecutive patients with aneurysmal SAH to determine whether the FG reliably predicts vasospasm. Our results suggest that the FG may need to be revised. 2. Patients and methods 2.1. Patient population We retrospectively reviewed the medical records including hospital charts, CT scans, angiograms, and TCD findings of 134 consecutive patients with a diagnosis of SAH treated at the Hospital of the University of Pennsylvania. Patients with SAH due to trauma, arteriovenous malformations, or of unknown etiology were excluded from the study. Subarachnoid hemorrhage was diagnosed by either CT scanning or lumbar puncture. Patient demographics, date of SAH, day of CT scan, FG, and Hunt and Hess grade were recorded. The date of the hemorrhage was considered day 1 and day of CT scan was recorded relative to this. 2.2. Treatment All patients were treated according to standard protocol, including preoperative resuscitation, early aneurysm occlusion using coil embolization or surgical clipping, and aggressive prevention and treatment of vasospasm. All patients were cared for in the neurosurgical intensive care
unit with invasive hemodynamic monitoring. All patients received nimodipine and phenytoin. Transcranial Doppler sonography was obtained every other day for 14 days and every day for patients suspected of having symptomatic vasospasm. We define symptomatic vasospasm as a clinical entity that includes a new, delayed focal neurologic deficit or mental status decline in the postoperative period without evidence of hydrocephalus, metabolic abnormality, fever, or other systemic factors. It was not quantified by an absolute middle cerebral artery (MCA) blood flow velocity (BFV) with TCD analysis and was made strictly by clinical criteria. If patients became symptomatic from clinically suspected cerebral vasospasm, mean arterial blood pressure was elevated and intravenous fluid resuscitation was maintained in keeping with the triple H therapy. If symptoms did not resolve, patients were taken for angiography. Transcranial Doppler sonography BFV in the MCA was evaluated using a scale of 0 for normal (BFV b 90 cm/s), 1 for mild spasm (BFV = 90 -120 cm/s), 2 for moderate spasm (BFV = 120- 200 cm/s), and 3 for severe spasm (BFV N 200 cm/s). We tabulated the results from the MCA BVF findings for the purpose of this study. Transcranial Doppler sonography analysis was done on each patient assessing BFV in all vessels but we used MCA BFV for the statistical analysis. Each patient was administered 0.9% normal saline and 5% albumin to maintain central venous pressure greater than 8 mm Hg. CT scanning was used to examine patients who demonstrated clinical deterioration. When vasospasm was thought to be the cause of clinical deterioration, hypertensive and hypervolemic therapy was started to maintain systolic blood pressure greater than 180 mm Hg. The diagnosis of symptomatic cerebral vasospasm was confirmed using angiography. When clinical deterioration persisted despite medical management, patients underwent papaverine infusion, balloon angioplasty, or both. 2.3. CT scanning Computed tomography scans were obtained on a General Electric Light Speed Scanner according to standard protocols. Each CT scan was examined by 2 independent observers and in different orders. Cases leading to disagreement between observers were reviewed by both observers together to reach a consensus. The CT scans were examined using the FG—grade 1: none or minimal blood detected; grade 2: diffuse thin layers of subarachnoid blood with layers less than 1 mm thick; grade 3: localized clot and/or thick layers of subarachnoid blood greater than 1 mm thick; grade 4: intracerebral or intraventricular with no or diffuse subarachnoid blood. Blood was also evaluated based on location: Sylvian fissure, interhemispheric fissure, basal cisterns, third ventricle, fourth ventricle, lateral ventricle(s), and the presence of intraparenchymal clot. 2.4. Angiography All patients underwent pretreatment digital subtraction angiography. Aneurysm size and location were recorded.
M.L. Smith et al. / Surgical Neurology 63 (2005) 229 – 235 Table 2 Patient demographics for all patients and those stratified as symptomatic vasospasm All patients
Symptomatic vasospasm
Asymptomatic
134 40/94 16-82 54.4
28 (21%)a 7/21 35-78 51.8
106 (79%)b 33/73 16-82 55.0
Hunt and Hess grade 1 57 2 16 3 29 4 25 5 7
10 5 5 8 0
(18%) (31%) (17%) (32%) ( 0 %)
47 (82%) 11 (69%) 24 (83%) 17 (68%) 7 (100%)
Fisher grade 1 2 3 4
0 8 7 13
( 0%) (24%) (28%) (19%)
6 26 18 56
No. of patients Male/female Age (y) Mean (y)
a b
6 34 25 69
(100%) (76%) (22%) (81%)
Percentage of ball patientsQ who develop symptomatic vasospasm. Percentage of ball patientsQ without signs or symptoms of vasospasm.
Posttreatment angiograms were obtained when vasospasm was suspected as the cause for delayed neurologic deterioration. Angiograms were evaluated by 2 independent observers unaware of the CT FG and classified according to the following scale by comparing pre- and posttreatment studies: 0 for no spasm; 1 for mild spasm (b 25% arterial narrowing); 2 for moderate spasm (25 - 50% arterial narrowing); and 3 for severe spasm (N 50% arterial narrowing). Vasospasm was qualified as the most severe narrowing in any one vessel, independent of the number of other vessels affected. 2.5. Statistical analysis Data are represented as means F SDs or, where samples depart from normal distributions, as a median. The Student t test was used to test differences between groups when the data were normally distributed. The Mann-Whitney procedure was used to examine data that departed from a normal distribution. Both univariate and bivariate analyses were done using analysis of variance, Student t test, and a Pearson v 2 test. The Fischer exact test was substituted when one or more cells had frequencies less than 5. Statistical significance was set at a probability value less than .05. All statistical analyses were performed using commercially available software (SAS Proprietary Software, Version 8, 1999, SAS Institute, Cary, NC). 3. Results 3.1. Patients There were 134 patients, including 40 males and 94 females (median age, 54 years; range, 16-82 years) (Table 2). The FGs and Hunt and Hess grades are listed in Table 2. All patients underwent preoperative digital subtraction angiog-
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raphy except one patient who presented with a large temporal hematoma that required emergent evacuation. In this patient, the presence of an aneurysm was confirmed intraoperatively. There were 116 anterior circulation and 18 posterior circulation ruptured aneurysms. Twenty patients underwent coil embolization (15%) and 114 (85%) underwent surgical clipping. 3.2. Fisher grade and CT scan Twenty-eight patients (21%) developed symptomatic vasospasm. Of these, 8 were FG 2, 7 were FG 3, and 13 were FG 4. The severity of SAH identified on initial CT scan was not associated with symptomatic vasospasm ( P = .50). In both univariate and bivariate analyses, development of symptomatic vasospasm was not associated with admission FG, Hunt and Hess grade, age, sex, or location of blood on presenting CT scan. One hundred eleven (83%) patients had their initial CT scan on the day of SAH (day 1), 6 on day 2, 6 on day 3, 2 on day 4, 3 on day 5, and 6 between days 6 and 9 after SAH. Twenty-one of 28 (75%) patients with symptomatic vasospasm and 90 of 106 (85%) patients without symptomatic vasospasm had their initial CT scan on the day of SAH with no significant difference between groups ( P = .67). The location of subarachnoid blood was similar in patients who developed symptomatic vasospasm and those who were asymptomatic (Table 3) ( P values ranged from .41 to .82 for the different locations analyzed and listed in Table 3). Symptomatic vasospasm developed in 8 of 28 patients (29%) with a focal homogenous collection of subarachnoid blood greater than 10 mm in diameter. Symptomatic vasospasm developed in 15% of patients who did not have focal clots. 3.3. Fisher grade and TCD All patients underwent serial TCD examinations. In those patients with at least 1 episode of TCD BFV greater than 200 cm/s (n = 14), 6 patients (38%) developed symptomatic vasospasm (Table 4). In both univariate and bivariate analyses, elevated TCD MCA BFV was not associated with Table 3 Subarachnoid blood distribution on initial CT scan All patients Unilateral Sylvian fissure blood Bilateral Sylvian fissure blood Interhemispheric blood Basal cisterns Third ventricle Fourth ventricle Lateral ventricle Intraparenchymal clot a
34
Symptomatic vasospasm 6 (18%)a
Asymptomatic 28
55
13 (24%)
42
35
8 (23%)
27
76 16 24 49 28
18 (24%) 2 (13%) 4 (17%) 11 (22%) 8 (29%)
58 14 20 38 20
Percentage of ball patientsQ who develop symptomatic vasospasm.
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Table 4 Assessment of vasospasm using TCD and angiography All patients Elevated TCD None Mild Moderate Severe
85 24 11 14
Preoperative angiogram None 120 Mild 11 Moderate 1 Severe 1
Symptomatic vasospasm 12 8 2 6
(14%)a (33%) (18%) (43%)
73 16 9 8
23 4 1 0
(19%) (36%) (100%) (0%)
97 7 0 1
Postoperative angiogram (n = 57) None 20 2 (10%) Mild 12 3 (25%) Moderate 11 8 (73%) Severe 14 12 (86%) a
Asymptomatic
18 9 3 2
Percentage of ball patientsQ who develop symptomatic vasospasm.
admission FG, Hunt and Hess grade, age, or sex. A significant association was observed between elevated TCD MCA BFV and symptomatic ( P = .005) or angiographic vasospasm ( P = .001). A significant relationship also was observed between increased TCD MCA BFV and the location of blood on initial CT; blood in the basal cisterns ( P = .0047), lateral ventricles ( P = .026), or in any ventricle ( P = .04) was associated with elevated TCD velocities. 3.4. Fisher grade and angiography On preoperative angiograms (n = 133), 11 (8%) patients had mild vasospasm, 1 patient had moderate vasospasm, and 1 patient had severe vasospasm. Fifty-seven (43%) patients underwent postoperative angiography between 3 and 18 days (mean = 6 days) after SAH. Angiographic vasospasm was identified in 37 (65%) patients, including 12 (21%) with mild, 11 (19%) with moderate, and 14 (25%) with severe angiographic vasospasm. In patients with severe angiographic MCA vasospasm, all had TCD MCA BFV greater than 200 cm/s. In contrast, BFV was less than 200 cm/s in all patients with mild or moderate vasospasm. Among the patients who developed symptomatic vasospasm, moderate to severe angiographic vasospasm was observed in 5 patients with FG 2, 6 patients with FG 3, and 9 patients with FG 4 SAH. Our results suggest that there is a statistically significant association between symptomatic vasospasm and angiographic vasospasm. However, only 43% of our patients had postoperative angiograms depending on surgeon preference. The results must be interpreted keeping this in mind. In univariate and bivariate analysis the severity of angiographic vasospasm was not predicted by the severity of SAH classified by the FG on initial head CT scan. In addition, no significant association was observed between angiographic vasospasm and admission FG, Hunt and Hess grade, age, or sex. A significant association was observed between angiographic vasospasm and symptomatic vaso-
spasm ( P b .0001) and elevated TCD MCA BFV ( P = .001). There also was a strong association between angiographic vasospasm and intraventricular blood ( P = .054).
4. Discussion In this retrospective study, we evaluated the CT, angiographic, and TCD findings of 134 patients with aneurysmal SAH to determine whether the initial CT severity of SAH determined by the FG predicts symptomatic cerebral vasospasm. The study was undertaken because there have been significant advances in neurologic imaging and in SAH management since the FG was devised more than 20 years ago that may now bias or invalidate the accuracy of the original grading system. Our results suggest that the FG may not be valid in the modern era. 4.1. Contemporary management of cerebral vasospasm There are several important differences between this study and that which led to the development of the FG. First, neurologic imaging is now more sophisticated. Second, among the 47 patients examined by Fisher et al [4], more than half (26/47) underwent CT scanning in the days after SAH with delayed diagnosis and treatment. In contrast, 83% of the patients (111/134) in our study underwent CT scan on the day of SAH and with the minority of patients having their initial CT scan days after hemorrhage. However, this did not influence our results because 75% of the patients in our study who developed symptomatic vasospasm had their initial CT scan on the day of SAH whereas 85% who did not develop vasospasm did the same. Third, vasospasm prevention and management has changed significantly in the last 20 years. Nearly half of the patients (23/47) included in the Fisher et al [4] study developed symptomatic vasospasm whereas 21% of our patients developed symptomatic vasospasm. Finally, most patients in our series underwent treatment within 3 days of SAH whereas patients examined by Fisher et al [4] had delayed surgery. 4.2. Transcranial Doppler sonography The value of TCD is debated by some. However, rapid and sequential increase in BFV or MCA BFV greater than 200 cm/s is highly correlated with angiographic vasospasm [7,11]. In our study, elevated TCD BFV in the MCA was predictive of angiographic and symptomatic vasospasm. In addition, elevated TCD BFV was significantly correlated with the presence of blood in the basal cisterns, blood in the lateral ventricle, and blood in any ventricle. Other investigators who have recently evaluated predictive factors for vasospasm have also observed a strong association between an early increase in TCD BFV greater than 140 cm/s and vasospasm [3,8]. Seventy-five percent of our patients with TCD evidence of vasospasm who underwent postoperative angiography had angiographic vasospasm.
M.L. Smith et al. / Surgical Neurology 63 (2005) 229 – 235
Although the association between large amounts of subarachnoid blood and vasospasm is well known, our results, as well as those from other studies, have found similar limitations to the FG [3,9]. For example, Schaller et al [9] observed that there was limited association between severe vasospasm identified by TCD and the FG. In that study, severe vasospasm documented by TCD (MCA BFV N160 cm/s on 2 or more consecutive days) was observed in 39% of FG 1 patients, 26% of FG 2 patients, and 34% of FG 3 patients. The authors concluded that the amount of subarachnoid blood identified on the initial CT scan should no longer be used as an indicator to predict symptomatic vasospasm. 4.3. Volume of subarachnoid blood We did not observe a clear association between the FG, the presence of blood clot, and the subsequent cerebral vasospasm. In those patients with intraparenchymal or Sylvian fissure clot, only 8 of 28 patients (29%) developed symptomatic vasospasm. We did not observe a characteristic subarachnoid blood pattern that predicted those patients at high risk for symptomatic vasospasm. We did observe a relationship between intraventricular blood and vasospasm. The amount of blood alone is not the only factor that influences whether someone becomes symptomatic. For example, advanced age is associated with a reduced incidence of vasospasm [12], whereas cigarette smoking may increase the risk of vasospasm [6]. However, this does not exclude the possibility that the overall blood volume rather than distribution may be the more important factor. Friedman et al [5] recently used standard image analysis software to quantify the volume of blood in FG 3 patients with SAH; a significantly greater volume of cisternal blood was observed among patients with symptomatic vasospasm. Intraparenchymal and intraventricular blood was not associated with vasospasm. Our results were consistent with their findings in that elevated TCD BFV in the MCA was associated with blood in the basal cisterns and lateral ventricles. In contrast, others have shown that blood in both ventricles is associated with later vasospasm [3,10]. Why intraventricular hemorrhage is associated with vasospasm however is not certain. This is consistent with a particular volume of subarachnoid blood rather than distribution alone being important in the development of vasospasm and recent studies that demonstrate that thick clot filling any cistern or fissure is significantly associated with vasospasm [1-3,8,10]. Blood filling a cistern was not considered as an independent factor in the FG. 4.4. Study limitations The purpose of this study was to use a retrospective cohort to support evidence that the FG may need to be revisited and developed further to accommodate for contemporary management. However, this study presents a number of limitations. First, although our study is a retrospective review and this may lessen its credibility when compared to a prospective cohort, we do not propose a new
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grading scale based on these early findings. Second, there was no correlation in the development of symptomatic vasospasm to the Hunt and Hess grading scale, another standard in the evaluation of these patients. One reason for this discrepancy could be inherent in the difficulty assessing Hunt and Hess grade 4 and 5 patients for the development of symptomatic vasospasm. For these patients, assessment relies heavily on TCD evaluation and we did not select out this cohort for a separate analysis. Third, based on these initial findings a prospective study should be developed with the intent of developing a new grading system. Finally, until software becomes available such that quantification of blood volume with admission CT is easy to perform and with high accuracy, a prospective study may be difficult to perform. 5. Conclusions The FG did not reliably predict symptomatic vasospasm in this series of patients. The only admission CT finding that seemed to predict symptomatic vasospasm was intraventricular blood. There was no correlation between volume of a subarachnoid blood clot and development of symptomatic vasospasm. Our results do support the correlation of TCD findings to the development of both symptomatic and angiographic vasospasm. For those patients who did develop symptomatic vasospasm, there were more patients in the combined group with FGs 2 (n = 8) and 3 (n = 7) when compared to patients with FG 4 (n = 13). Taken together our data and that of other recent investigations suggest that although the FG is useful it may need revision to reflect modern neurologic imaging and to provide help in vasospasm management. References [1] Adams HP, Kassell NF, Torner JC, et al. Predicting cerebral ischemia after aneurysmal subarachnoid hemorrhage: influences of clinical condition, CT results, and antifibrinolytic therapy. A report of the Cooperative Aneurysm Study. Neurology 1987;37:1586 - 91. [2] Bonhila L, Marques EL, Carelli EF, et al. Risk factors and outcome in 100 patients with aneurysmal subarachnoid hemorrhage. Arq Neuropsiquiatr 2001;59:767 - 80. [3] Claassen J, Bernardini GL, Kreiter K, et al. Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the Fisher scale revisited. Stroke 2001;32:2012 - 20. [4] Fisher CM, Kistler JP, Davis JM. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 1981;6:1 - 9. [5] Friedman JA, Goerss SJ, Meyer FB, et al. Volumetric quantification of Fisher Grade 3 aneurysmal subarachnoid hemorrhage: a novel method to predict symptomatic vasospasm on admission computerized tomography scans. J Neurosurg 2002;97:401 - 7. [6] Lasner TM, Weil RJ, Riina HA, et al. Cigarette smoking-induced increase in the risk of symptomatic vasospasm after aneurysmal subarachnoid hemorrhage. J Neurosurg 1997;87:381 - 4. [7] Newell DW, Grady MS, Eskridge JM, et al. Distribution of angiographic vasospasm after subarachnoid hemorrhage: implications for diagnosis by transcranial Doppler ultrasonography. Neurosurgery 1990;27:574 - 7. [8] Qureshi AI, Sung GY, Razumovsky AY, et al. Early identification of patients at risk for symptomatic vasospasm after aneurysmal subarachnoid hemorrhage. Crit Care Med 2000;28:984 - 90.
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Smith et al reviewed 134 patients with SAH and found no correlation of the admission FG with the development of symptomatic vasospasm. Table 2 displays these results nicely. The authors question the validity of the FG in predicting the risk of vasospasm, given modern CT imaging. There are significant differences between this study and that of Fisher et al [1] 24 years ago. Most notably, all the patients in the first study underwent postoperative angiography whereas only 47% of patients in this present study underwent this test. It can only be assumed that postoperative angiography was selectively used in a manner that biased the performance of this test toward patients with clinical (or bsymptomaticQ) vasospasm. Therefore, the finding of ba significant association . . . between angiographic vasospasm and symptomatic vasospasm . . .Q is irrelevant. Similarly, the association between angiographic spasm and elevated TCD MCA BFV is suspect. The authors propose a prospective study b. . . with the intent of developing a new grading system.Q It is unclear what the authors intend to grade because the only predictor of vasospasm in their study was intraventricular blood. Has the pathophysiology of SAH changed? Maybe the mastery of clinical neurology of CM Fisher explains the higher incidence of symptomatic cerebral ischemia in his series. Stated another way, it may be that as we rely more on radiographic imaging, we simultaneously require more obvious signs of neurologic dysfunction to prod us to order tests that confirm our crude bedside findings. Whether true or not, we choose to agree with the authors that it is improvements in medical management that have reduced the incidence of vasospasm after SAH.
Fisher and colleagues were among the first to publish clinical data relating the volume and location of subarachnoid blood to the risk of cerebral vasospasm [3,8]. The technology used by Fisher et al obviously is outdated, but one cannot argue with several decades of clinical and experimental data that strongly support, if not prove, that angiographic arterial narrowing after SAH is related in part to the volume of clot next to the artery that develops vasospasm [7]. A review of the 1980 paper shows that the computed tomograms were obtained within 5 days of SAH on a scanner with a 160 160 matrix and 16-mm-thick slices. Current imaging has more than 10 times this resolution. The thickness of the clots refers to measurements made on the printed images that had been printed at variable sizes. No magnification standard was included. Therefore, the 1-mm distinction between groups 2 and 3 is not equivalent to an actual 1 mm measured on a CT scan today. With current scanners, a negative head CT scan result within a day of SAH is uncommon (FG 1) and clots with real thickness less than 1 mm also are uncommon (FG 2). I suspect most neurosurgeons distinguish grades 2 and 3 by relatively thin vs relatively thick clots, which was the qualitative system used in more recent clinical trials [5]. The paper by Smith and colleagues found it difficult to correlate FG and vasospasm. This may be because the method for differentiating the FGs in this study is not entirely clear, and the distribution of patients is different from some other series since there is a high percentage of FG 4 patients in this study. In addition, the study is an attempt to correlate 2 imprecisely measured phenomena. The SAH on CT measured by the Fisher scale is only a rough estimate and would be better measured quantitatively using a method such as that used by Friedman et al [4]. The assessment of vasospasm was also imprecise and did not use the gold standard catheter angiography in all cases. In addition, other factors influence the risk of vasospasm, such as the density and duration of persistence of the subarachnoid clot, the presence of intraventricular hemorrhage, the clinical grade, and possibly smoking [1,2,6,9]. This paper is important because it highlights the limitations of the Fisher scale and hopefully will stimulate, as mentioned by the authors, the development of software to easily quantify clot volume and density when the initial CT is acquired, or some method to better predict vasospasm.
References
References
[1] Fisher CM, Kistler JP, Davis JM. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 1980;6:1 - 9.
[1] Charpentier C, Audibert G, Guillemin F, Civit T, Ducrocq X, Bracard S, Hepner H, Picard L, Laxenaire MC. Multivariate analysis of predictors of cerebral vasospasm occurrence after aneurysmal subarachnoid hemorrhage. Stroke 1999;30:1402 - 8. [2] Claassen J, Bernardini GL, Kreiter K, Bates J, Du YE, Copeland D, Connolly ES, Mayer SA. Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the Fisher scale revisited. Stroke 2001;32:2012 - 20. [3] Fisher CM, Kistler JP, Davis JM. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 1980;6:1 - 9.
[9] Schaller C, Rohde V, Meyer B, et al. Amount of subarachnoid blood and vasospasm: current aspects. A transcranial Doppler study. Acta Neurochir (Wien) 1995;136:67 - 71. [10] Shimoda M, Oda S, Shibata M, et al. Results of early surgical evacuation of packed intraventricular hemorrhage from aneurysm rupture in patients with poor-grade subarachnoid hemorrhage. J Neurosurg 1999;91:408 - 14. [11] Skirboll S, Newell DW. Noninvasive physiologic evaluation of the aneurysm patient. Neurosurg Clin N Am 1998;9:463 - 83. [12] Suzuki A, Yasui N, Hadeishi H, et al. Cerebral vasospasm in aged patients with ruptured intracranial aneurysms. Neurol Med Chir (Tokyo) 1988;28:786 - 90.
Commentary
Duke Samson, MD Christopher L. Taylor, MD Department of Neurosurgery UT Southwestern Medical Center Dallas, TX 75235, USA