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Published online before print December 4, 2007, 10.1148/radiol.2461061915
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(Radiology 2008;246:543-552.)
© RSNA, 2008

Neuroradiology

MR Imaging of the Brain 1 Year after Aneurysmal Subarachnoid Hemorrhage: Randomized Study Comparing Surgical with Endovascular Treatment1

Paula Bendel, MD, Timo Koivisto, MD, PhD, Mervi Könönen, MSc, Tuomo Hänninen, MSc, PhD, Heleena Hurskainen, MSc, Tapani Saari, MD, Matti Vapalahti, MD, PhD, Juha Hernesniemi, MD, PhD, and Ritva Vanninen, MD, PhD

1 From the Departments of Clinical Radiology (P.B., M.K., T.S., R.V.), Neurosurgery (T.K., H.H., M.V., J.H.), and Neurology (T.H.), Kuopio University Hospital and Kuopio University, Puijonlaaksontie 2, 70210 Kuopio, Finland; and Department of Neurosurgery, University of Helsinki, Helsinki, Finland (J.H.). Received November 9, 2006; revision requested January 15, 2007; revision received March 19; accepted April 24; final version accepted June 11. Address correspondence to P.B. (e-mail: paula.bendel{at}kuh.fi).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
APPENDIX: STUDY DESIGN
ADVANCE IN KNOWLEDGE
IMPLICATIONS FOR PATIENT CARE...
 References
 
Purpose: To prospectively evaluate, with magnetic resonance (MR) imaging, long-term outcome of the brain after endovascular versus neurosurgical treatment for aneurysmal subarachnoid hemorrhage (aSAH).

Materials and Methods: Institutional review board approval and informed consent were obtained. One hundred sixty-eight (77 men, 91 women; mean age ± standard deviation, 51 years ± 13) patients were randomly assigned to surgical versus endovascular treatment of the ruptured aneurysm with 138 (67 endovascular, 71 surgical) MR examinations 1 year after aSAH. The presence, localization, volumes, and cause of lesions were analyzed with {chi}2, Mann-Whitney U, and Student t tests. Furthermore, correlation between MR-detectable brain parenchymal high-signal intensity (SI) lesions on T2- and intermediate-weighted MR images and neuropsychologic outcome was evaluated by using Spearman correlation coefficient.

Results: Only 44 (31.9%) of 138 patients had no lesions associated with aSAH. According to intention to treat, lesions were more frequent after surgical rather than endovascular treatment, predominating in the frontal (surgical: n = 50, [70.4%] vs endovascular: n = 34 [50.7%], P = .018) and temporal (n = 34 [47.9%] vs n = 15 [22.4%], P = .002) lobes. Only endovascular patients had subtentorial lesions (n = 4 [6.0%], P = .037). Ischemic lesions in the parental artery territory were more frequent in surgical (n = 33 [46.5%]) than in endovascular (n = 15 [22.4%], P = .003) patients, with corresponding mean lesion volumes of 20.9 cm3 ± 46.5 versus 17.6 cm3 ± 35.8 (P = .209). Ischemic lesions in remote vascular territories were equal in frequency and size. Retraction injuries were common in the surgical (n = 40, [56.3%]) treatment group. Ischemic lesion volumes correlated with neuropsychologic test scores.

Conclusion: Parenchymal high-SI lesions on T2- and intermediate-weighted MR images are more frequent after early surgical rather than endovascular treatment of the ruptured aneurysm, and lesion volumes correlate with the neuropsychologic test performance.

© RSNA, 2007


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
APPENDIX: STUDY DESIGN
ADVANCE IN KNOWLEDGE
IMPLICATIONS FOR PATIENT CARE...
 References
 
Aneurysmal subarachnoid hemorrhage (aSAH) is a life-threatening disease with an overall case fatality of approximately 50% (1). Many of the surviving patients are left with neurologic deficits or neuropsychologic and cognitive impairments (2). Late structural brain damage seen at magnetic resonance (MR) imaging can be associated with the primary hemorrhage itself, damage caused by treatment, or vasospasm (3,4).

Both surgical and endovascular treatment of the ruptured aneurysm can lead to brain infarction owing to large-vessel or perforator vasospasm, unintentional occlusion, or thromboembolic mechanism. Vasospasm may be local, aggravated by mechanical manipulation of the parental artery during either surgical or endovascular procedures, or global, occurring in remote vascular territories (5). Leukoaraiosis and lacunar infarctions associated with hypertension may also contribute to neurologic morbidity after aSAH and are best detected by using MR (6).

Authors of a study suggested that treatment with a coil might cause less structural damage to brain parenchyma (4). The International Subarachnoid Aneurysm Trial demonstrated that treatment with an endovascular coil is more likely to result in independent survival than treatment with a neurosurgical clip in patients assigned a "good" grade, with anterior circulation aneurysms suitable for both treatment methods (7,8). However, most of the long-term radiologic outcome studies after aSAH have been performed after surgical clip treatment (3,9) or by using computed tomography (CT) (10). No randomized studies have focused on late structural brain damage detected at MR after endovascular or surgical treatment of aSAH.

The aim of this study was to prospectively evaluate long-term outcome with MR imaging of the brain after endovascular versus neurosurgical treatment for aSAH.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
APPENDIX: STUDY DESIGN
ADVANCE IN KNOWLEDGE
IMPLICATIONS FOR PATIENT CARE...
 References
 
Study Design, Patient Demographics, and Aneurysms
The ethics committee (Kuopio University, Kuopio, Finland) approved the study and informed consent was obtained. Between February 1995 and December 1999, 467 patients with angiographically proved aSAH were treated in our hospital, the only neurosurgical center in a catchment area of 900 000 people. According to the inclusion criteria (11,12) (Appendix), 168 eligible patients with acute aSAH (91 women, 77 men; mean age, 51 years; range, 14–75 years) were randomly assigned to either endovascular (n = 82) or surgical (n = 86) treatment. The endovascular procedures were performed by two neuroradiologists (R.V., T.S., with 1 and 3 years experience in neurointerventions, respectively) and surgical operations by seven senior neurosurgeons (J.H., M.V., five nonauthors, with 10–30 years experience in neurosurgery each). The ruptured aneurysms (diameter, 2–15 mm; neck width, 1–8 mm) were located in the anterior circulation in 153 (91%) patients and in the posterior circulation in 15 (9%) patients. Brain MR and clinical and neuropsychologic assessment were scheduled 1 year after aSAH.

Fifteen (10.9%) of 138 patients who underwent follow-up MR also underwent combination treatment (endovascular and surgical) of the ruptured aneurysm. The indications for combination treatment were failure in the primary treatment procedure or revascularization in the aneurysm during follow-up angiography. Combination treatment was required more frequently in the endovascular group (n = 13 [19.4%]) than in the surgical group (n = 2 [2.8%], P = .002). Thirty-five (25.4%) of 138 patients had 54 nonruptured aneurysms, which were treated by using the same criteria currently recommended (embolization in six, surgery in 23, combination treatment in three, and angiographic follow-up in 22 cases) (13).

Fisher Grades, Hunt and Hess Grades, and Clinical Vasospasm
Every patient underwent preoperative CT scans, which were evaluated by consensus by a neurosurgeon (T.K.) and a neuroradiologist (R.V.) for assessment of the Fisher grade (14) and possible hydrocephalus. The Fisher grades were split between grades 0–II (minor to moderate bleeding) and grades III–IV (severe bleeding). The Hunt and Hess grades were assessed by six resident neurosurgeons (all nonauthors, with 1–6 years experience each) and confirmed by two senior neurosurgeons (M.V., J.H.). Clinical criteria for symptomatic vasospasm (assessed by M.V., H.H., and five nonauthor senior neurosurgeons) were a decrease of Glasgow Coma Scale rating by two or more scores or appearance of new localizing symptoms (dysphasia or hemiparesis); other reasons for deterioration (eg, hydrocephalus, metabolic disorders, postoperative bleeding, and infections) were ruled out. The clinical outcome 1 year after aSAH was assessed by a single neurosurgeon (T.K.).

MR Imaging
Patients underwent 1.5-T MR imaging (Magnetom Vision; Siemens Medical Systems, Erlangen, Germany) with a circular polarized head coil. MR protocol consisted of transverse T2- and intermediate-weighted MR imaging (repetition time msec/echo time msec/inversion time msec, 2625/98/16; matrix, 260 x 512; and section thickness, 5 mm), MR angiography, and three-dimensional T1-weighted imaging (9.7/4/20; flip angle, 12°; field of view, 250 mm; and matrix, 256 x 256). All coils and surgical clips were nonferromagnetic and safe for MR imaging (15,16).

All MR examinations were analyzed by consensus among three authors (R.V., a neuroradiologist, T.K., a neurosurgeon, and P.B., a resident, with 15, 13, and 5 years experience in MR image interpretation, respectively). Blinded reading was not possible because of characteristic clip and coil artifacts. The presence of any high-signal-intensity (SI) lesions on T2- and intermediate-weighted MR images (low SI on three-dimensional T1-weighted MR images) were visually evaluated and lesion volumes were measured later by the resident. The most probable etiology of the high-SI lesion was determined and classified by consensus with knowledge of all clinical, radiologic, and surgical details of the patient. CT scans and angiographic images were available during the MR evaluation.

The following factors were analyzed and quantified according to anatomic locations (17,18): ischemic lesions in parental artery territory (vascular territory of the ruptured aneurysm) and other vascular territories, on the basis of knowledge of normal vascular anatomy and angiographic findings of each patient; superficial siderosis and residual signs of hematoma; signs of retraction injury due to surgical manipulation and instrumentation; ventricular size and possible hydrocephalus; parenchymal lesions associated with intraventricular cathether and permanent shunt placement; and previous infarctions, degree of possible previous atrophy, and presence of lacunar infarctions and leukoaraiosis.

The parental artery of the ruptured aneurysm was classified as the anterior cerebral artery, middle cerebral artery, internal carotid artery, or vertebrobasilar artery. If the ruptured aneurysm was located in the anterior cerebral artery or the basilar tip, the bilateral vascular territories of frontopolar, callosamarginal, and pericallosal arteries or posterior cerebral arteries were considered as parental arteries. Ischemic lesions in vascular territories other than the parental arteries were considered to represent general vasospastic cause. Signs of parenchymal or sylvian hematoma were evaluated by using primary CT scans. The convexity of the brain, basal cisterns, and the sylvian region were evaluated for possible signs of superficial siderosis at MR.

Approximate adjustment for ventricular size was made visually at consensus reading. As a rough measure of ventricular size, the ventricular width–intracranial width ratio was calculated with the maximum diameter of the lateral ventricles and the intraparenchymal diameter at the same level. The degree of leukoaraiosis was scored as absent, punctuate and/or early confluent, or confluent (19).

Volumes of ischemic and retraction lesions were measured by a single interpreter (P.B.) (on the basis of initial consensus reading) on a picture and archiving communication system workstation (Sectra EE, version 10.2 P4; Limkopinig, Sweden) by drawing a region of interest according to the lesion margin on each T2-weighted MR image and by multiplying the lesion areas by the sum of the section (5 mm) and gap (1.5 mm) thicknesses.

Neuropsychologic Analysis
Detailed neuropsychologic examination was performed by a single neuropsychologist (H.H., with 15 years experience) 1 year after aSAH. The comprehensive evaluation included tests of general intelligence, memory, selected language abilities, assessment of attention, and flexibility of mental processing (11).

Statistical Analysis
Statistical analysis (SPSS, version 11.5, 2002; SPSS, Chicago, Ill) and group comparisons between treatment methods were performed according to intention to treat. Categoric data (ordered by Hunt and Hess grade) and dichotomous variables (ordered by sex, Fisher grade, presence of symptomatic vasospasm, location of aneurysm, presence of high-SI parenchymal lesion on T2- and intermediate-weighted MR images, and presence of different types of MR-detectable lesions) were examined with the {chi}2 test. The Mann-Whitney U test was used to compare nonparametric, continuous-scale data for nonnormally distributed variables (eg, size of the aneurysm, lesion volumes). The Student t test was used to compare normally distributed data (eg, age, ventricular width–intracranial width ratio). Spearman correlation coefficient was used to assess correlations between nonparametric continuous-scale variables (eg, lesion volumes, neuropsychologic outcome, age). A P value of .05 or less was considered to indicate a significant difference.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
APPENDIX: STUDY DESIGN
ADVANCE IN KNOWLEDGE
IMPLICATIONS FOR PATIENT CARE...
 References
 
Comparability of the Study Groups
Sixty-seven (81.7%) of 82 endovascular and 71 (82.6%) of 86 surgical patients (Fig 1) underwent follow-up MR (P = .886). The mean interval ± standard deviation between aSAH and MR was 15.8 months ± 8.5 (range, 9–64 months). The diagnostic quality of the MR examinations was excellent in 134 (97.1%) and suboptimal, but diagnostic, in four (2.9%) examinations. There were no differences between the treatment groups in terms of age, sex, Hunt and Hess grade, Fisher grade, or location and size of the ruptured aneurysm (Table 1). The clinical outcomes of the 148 living patients were comparable: 114 (63 endovascular, 51 surgical) had good recovery, 19 (five endovascular, 14 surgical) had moderate disability, 12 (three endovascular, nine surgical) had severe disability, and three (one endovascular, two surgical) were in a vegetative state (P = .067).


Figure 1
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  		Figure 1: Flowchart shows study population.

 

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  		Table 1. Patients Who Underwent 12-Month MR according to Intention to Treat

 
Parenchymal Lesions
One year after aSAH, only 44 (31.9%) patients (29 endovascular, 15 surgical) showed normal results of brain MR or the finding was analogous to the CT scan at admission. Parenchymal high-SI lesions on T2- and intermediate-weighted MR images of different cause were seen in 38 (56.7%) endovascular and 56 (78.9%) surgical patients (P = .005). In Hunt and Hess grades I–III, parenchymal lesions were seen in 65.1% of patients, while in Hunt and Hess grades IV–V, all patients had parenchymal lesions (P = .013). Patients assigned Fisher grades III–IV had more parenchymal lesions (77.3%) than did patients with Fisher grades 0–II (52.0%, P = .002). Parenchymal lesions of different causes detected at MR are shown in Tables 2 and 3 and Figures 2–6.


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  		Table 2. Parenchymal MR Lesions 1 Year after aSAH

 

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  		Table 3. Brain MR Findings according to Lesion Etiology 1 Year after aSAH

 

Figure 2A
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  		Figure 2a: Digital subraction angiographic images show (a) ruptured basilar tip aneurysm and normal filling of thalamic perforating arteries (arrowheads); (b) after surgery, residual aneurysm and bilateral thalamoperforator occlusions were detected (not shown). Residual aneurysm was treated with additional embolization. (c) Transverse T2-weighted MR image (2625/98) shows bilateral thalamic infarctions (arrowheads) 1 year after aSAH.

 

Figure 2B
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  		Figure 2b: Digital subraction angiographic images show (a) ruptured basilar tip aneurysm and normal filling of thalamic perforating arteries (arrowheads); (b) after surgery, residual aneurysm and bilateral thalamoperforator occlusions were detected (not shown). Residual aneurysm was treated with additional embolization. (c) Transverse T2-weighted MR image (2625/98) shows bilateral thalamic infarctions (arrowheads) 1 year after aSAH.

 

Figure 2C
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  		Figure 2c: Digital subraction angiographic images show (a) ruptured basilar tip aneurysm and normal filling of thalamic perforating arteries (arrowheads); (b) after surgery, residual aneurysm and bilateral thalamoperforator occlusions were detected (not shown). Residual aneurysm was treated with additional embolization. (c) Transverse T2-weighted MR image (2625/98) shows bilateral thalamic infarctions (arrowheads) 1 year after aSAH.

 

Figure 3A
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  		Figure 3a: (a) CT scan shows rupture of right anterior communicating artery aneurysm with left frontobasal hematoma. (b, c) Transverse T2-weighted (2625/98) MR images show high-SI lesion owing to previous frontobasal hematoma (long arrow) with low-SI hemosiderin rim (arrowhead). Small artifact from coil (short arrow) detected after endovascular treatment.

 

Figure 3B
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  		Figure 3b: (a) CT scan shows rupture of right anterior communicating artery aneurysm with left frontobasal hematoma. (b, c) Transverse T2-weighted (2625/98) MR images show high-SI lesion owing to previous frontobasal hematoma (long arrow) with low-SI hemosiderin rim (arrowhead). Small artifact from coil (short arrow) detected after endovascular treatment.

 

Figure 3C
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  		Figure 3c: (a) CT scan shows rupture of right anterior communicating artery aneurysm with left frontobasal hematoma. (b, c) Transverse T2-weighted (2625/98) MR images show high-SI lesion owing to previous frontobasal hematoma (long arrow) with low-SI hemosiderin rim (arrowhead). Small artifact from coil (short arrow) detected after endovascular treatment.

 

Figure 4A
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  		Figure 4a: (a, b) Transverse T2-weighted (2625/98) and (c) sagittal T1-weighted (9.7/4/20) MR images show retraction deficit in apex of right temporal lobe (short arrow) and cortical infarction (long arrow) in the parental artery of the ruptured aneurysm after surgery on ruptured right middle cerebral artery aneurysm.

 

Figure 4B
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  		Figure 4b: (a, b) Transverse T2-weighted (2625/98) and (c) sagittal T1-weighted (9.7/4/20) MR images show retraction deficit in apex of right temporal lobe (short arrow) and cortical infarction (long arrow) in the parental artery of the ruptured aneurysm after surgery on ruptured right middle cerebral artery aneurysm.

 

Figure 4C
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  		Figure 4c: (a, b) Transverse T2-weighted (2625/98) and (c) sagittal T1-weighted (9.7/4/20) MR images show retraction deficit in apex of right temporal lobe (short arrow) and cortical infarction (long arrow) in the parental artery of the ruptured aneurysm after surgery on ruptured right middle cerebral artery aneurysm.

 

Figure 5A
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  		Figure 5a: (a) Transverse T2-weighted (2625/98) MR image shows infarctions in parental (short arrow) and other (long arrow) vascular artery territories after primary embolization and combination surgery of ruptured right middle cranial artery aneurysm and evolved hematoma cavity (arrowhead). (b) Coronal T1-weighted (9.7/4/20) MR image shows large infarction, Wallerian degeneration (short arrow), and atrophy of ipsilateral hippocampus (long arrow).

 

Figure 5B
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  		Figure 5b: (a) Transverse T2-weighted (2625/98) MR image shows infarctions in parental (short arrow) and other (long arrow) vascular artery territories after primary embolization and combination surgery of ruptured right middle cranial artery aneurysm and evolved hematoma cavity (arrowhead). (b) Coronal T1-weighted (9.7/4/20) MR image shows large infarction, Wallerian degeneration (short arrow), and atrophy of ipsilateral hippocampus (long arrow).

 

Figure 6A
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  		Figure 6a: CT angiographic scans show (a) successful embolization treatment of right anterior communicating artery aneurysm; (b, c) severe global vasospasm (arrow) developed 2 weeks later. (d–f) Transverse T2-weighted (2625/98) MR images show severe outcome of vasospasm after coil treatment with widespread lesions 1 year later.

 

Figure 6B
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  		Figure 6b: CT angiographic scans show (a) successful embolization treatment of right anterior communicating artery aneurysm; (b, c) severe global vasospasm (arrow) developed 2 weeks later. (d–f) Transverse T2-weighted (2625/98) MR images show severe outcome of vasospasm after coil treatment with widespread lesions 1 year later.

 

Figure 6C
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  		Figure 6c: CT angiographic scans show (a) successful embolization treatment of right anterior communicating artery aneurysm; (b, c) severe global vasospasm (arrow) developed 2 weeks later. (d–f) Transverse T2-weighted (2625/98) MR images show severe outcome of vasospasm after coil treatment with widespread lesions 1 year later.

 

Figure 6D
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  		Figure 6d: CT angiographic scans show (a) successful embolization treatment of right anterior communicating artery aneurysm; (b, c) severe global vasospasm (arrow) developed 2 weeks later. (d–f) Transverse T2-weighted (2625/98) MR images show severe outcome of vasospasm after coil treatment with widespread lesions 1 year later.

 

Figure 6E
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  		Figure 6e: CT angiographic scans show (a) successful embolization treatment of right anterior communicating artery aneurysm; (b, c) severe global vasospasm (arrow) developed 2 weeks later. (d–f) Transverse T2-weighted (2625/98) MR images show severe outcome of vasospasm after coil treatment with widespread lesions 1 year later.

 

Figure 6F
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  		Figure 6f: CT angiographic scans show (a) successful embolization treatment of right anterior communicating artery aneurysm; (b, c) severe global vasospasm (arrow) developed 2 weeks later. (d–f) Transverse T2-weighted (2625/98) MR images show severe outcome of vasospasm after coil treatment with widespread lesions 1 year later.

 
Ischemic Lesions in the Parental Artery Territory
High-SI lesions on T2- and intermediate-weighted MR images indicating infarction in the vascular territory of the ruptured aneurysm were seen in 15 (22.4%) of 67 endovascular and 33 (46.5%) of 71 surgical patients (P = .003). Four endovascular and seven surgical patients had two separate infarctions each, and two surgical patients had three separate infarctions each in the parental artery territory. In patients who had infarctions, the mean volume of the infarcted tissue was 17.6 cm3 (range, 0.14–121.5 cm3) in the endovascular group and 20.9 cm3 (range, 0.09–261.5 cm3) in the surgical group (P = .209). In all patients included, the mean volume of the infarcted tissue in the parental artery territory was 3.9 cm3 (range, 0.0–121.5 cm3) after endovascular treatment and 9.7 cm3 (range, 0.0–261.5 cm3) after surgical treatment (P = .002).

Ischemic Lesions in Other Vascular Territories
Eighteen (26.9%) of 67 patients with endovascular treatment and 30 (42.3%) of 71 patients with surgical treatment reported symptoms of clinical vasospasm (P = .058). Brain infarctions in vascular territories other than that of the ruptured aneurysm were seen in seven (10.4%) of 67 patients with endovascular treatment and in 11 (15.5%) of 71 patients with surgical treatment (P = .379). In patients who had remote infarctions, the mean volume of the infarcted tissue was 27.6 cm3 (range, 0.17–58.5 cm3) in endovascular and 43.3 cm3 (range, 1.29–247.5 cm3) in surgical patients (P = .821). In the endovascular group, one patient had two infarctions and two patients had three infarctions in remote territories. In the surgical group, one patient had two, two patients had three, and one patient had four separate infarctions in remote territories. In all patients, the mean volume of the ischemic lesions in remote vascular territories was 2.9 cm3 (range, 0.0–58.5 cm3) after endovascular treatment and 6.7 cm3 (range, 0.0–247.5 cm3) after surgical treatment (P = .373).

Residual Signs of Hematoma and Superficial Siderosis
High-SI lesions seen on T2- and intermediate-weighted MR images due to previous intracerebral or sylvian hematoma were detected in 15 (22.4%) endovascular and 18 (25.4%) surgical patients (P = .683). Signs of superficial siderosis were present in 28 (41.8%) patients with endovascular treatment and 28 (39.4%) patients with surgical treatment (P = .778).

Retraction Injury Due to Surgical Manipulation and Instrumentation
Lesions in the brain parenchyma due to mechanical surgical trauma were obviously more common after surgical (n = 40 [56.3%]) than endovascular (n = 10 [14.9%]) treatment (P < .001). Retraction injuries were detected after endovascular treatment because 13 patients with endovascular treatment needed additional surgery and five endovascular patients had nonruptured aneurysms surgically ligated before MR. The mean volumes of the retraction deficits were 4.3 cm3 (range, 1.2–10.2 cm3) after endovascular treatment and 8.4 cm3 (range, 1.4–32.0 cm3) after surgical treatment (P = .055).

Late Hydrocephalus and Permanent Shunt Device
Seven (10.4%) patients with endovascular treatment and nine (12.7%) with surgical treatment had enlarged ventricles (P = .683). Mean ventricular width–intraparenchymal width ratio was 0.23 ± 0.1 after endovascular and 0.24 ± 0.1 after surgical treatment. Compared with patients with endovascular treatment (n = 4 [6.0%]), patients with surgical treatment (n = 12 [16.9%]) more often had a permanent shunt device (P = .045). Parenchymal lesions induced by a ventricular cathether (temporary drainage or permanent shunt device) were seen in 19 (28.4%) patients with endovascular treatment and 24 (33.8%) patients with surgical treatment (P = .490).

Previous Infarctions, Brain Atrophy, Lacunar Infarctions, and Leukoaraiosis
One endovascular patient had an old cortical infarction seen at CT at admission. Previous atrophy was present in one endovascular and two surgical cases (P = .594). At MR, at least one lacunar infarction was detected in 12 (17.9%) endovascular and 21 (29.6%) surgical patients (P = .108). Leukoaraiosis was absent in 42 (62.7%) endovascular and 40 (56.3%) surgical patients, punctuate or early confluent in 24 (35.8%) endovascular and 25 (35.2%) surgical patients, and confluent in one (1.5%) endovascular and six (8.5%) surgical patients (P = .171).

Neuropsychologic Analysis
The neuropsychologic examination 1 year after aSAH was available for 114 (82.6%) of 138 patients who had undergone MR. Nineteen (15.0%) of 127 patients with good or moderate clinical outcome refused the neuropsychologic examination; in five (45.5%) of 11 patients who had severe neurologic deficits or who were in a vegetative state, it was not possible to perform the neuropsychologic examination. Correlations between the observed focal parenchymal lesion volumes and neuropsychologic test performance are shown in Table 4.


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  		Table 4. Correlations between High-SI Lesion Volumes and Neuropsychological Outcome 1 Year after aSAH (n = 114)

 
Combination Treatment and Additional Treatment for Nonruptured Aneurysms
All previous analyses that were performed according to intention to treat were repeated after excluding patients with combination treatment or additional treatment for nonruptured aneurysms. These censored analyses did not produce notable changes in the significant differences between the treatment groups.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
APPENDIX: STUDY DESIGN
ADVANCE IN KNOWLEDGE
IMPLICATIONS FOR PATIENT CARE...
 References
 
The patient groups in our prospective study were statistically balanced in terms of the main predictors of outcome: age, preoperative Hunt and Hess grade, Fisher grade, and location of the aneurysm, (14,20,21). Our aim was to schedule all randomized patients still alive for follow-up MR, even if the clinical indications were not definitive with patients in poor condition. Consequently, we examined brain MR images for 93.2% of all living patients.

Our study suggests a higher incidence of parenchymal high-SI lesions on T2- and intermediate-weighted MR images in surgically rather than in endovascularly treated patients with aSAH, especially in the frontotemporal areas. These parenchymal lesions are of clinical importance, because their volumes are clearly correlated with neuropsychologic test performance. Many lesions were surgery-related brain retraction injuries, but there was also a significantly higher incidence of ischemic lesions in the parental artery territory in the surgical patients. The main parental and small perforating arteries are probably more prone to spasm, occlusion, or thromboembolism during the surgical procedure.

In remote vascular territories, no difference was found between treatment methods, probably representing a more generalized form of global vasospasm. It has been suggested that endovascular patients could have a higher risk for vasospasm because the blood degradation products in the sulci might cause chemical irritation to the leptomeningeal arteries, compared with surgical patients in whom some of the subarachnoid blood may be removed. We observed no beneficial effect; instead, surgical patients tended to have a higher incidence of clinical vasospasm. However, equal frequency and size of ischemic lesions were detected in remote vascular territories, both in cortical branch and perforator artery territories.

Subtentorial parenchymal lesions were detected in four endovascular patients and in none of the surgical patients. Interestingly, only one of these four presented with a posterior circulation aneurysm, indicating that the ischemic lesions were probably caused by thromboembolism during intraarterial catheterization.

Knowledge of the surgical techniques used in each case was important when high-SI lesions on T2- and intermediate-weighted MR images were interpreted to be caused by surgery. A majority of the retraction injury lesions were located in the basal aspect of the frontotemporal lobes. The orbital surface of the frontal lobe can show individual anatomic variations (22,23). Nonetheless, the gyrus rectus was easily identified and sometimes showed focal atrophy due to surgical resection. In addition, there were retraction-related high-SI lesions in the gyrus rectus and the orbital gyrus.

In the temporal lobe, retraction lesions were located in the anteroinferior surface containing the parahippocampal, fusiform, and inferior temporal gyri inferiorly, and the superior and middle temporal gyri anteriorly (22,23). A typical retraction injury does not follow the vascular anatomy of the brain. In the acute phase of aSAH, the brain is generally swollen with vasogenic edema, in addition to the mass effect of the possible hematoma and hydrocephalus, making the surface of the brain especially vulnerable.

The clinical significance of the persisting blood degradation deposits on the brain's surface remains unclear, but clinical manifests such as cerebellar ataxia, sensorineural hearing loss, and myelopathy have been suggested (24). Surprisingly, signs of hematomas and superficial siderosis were more frequent than reported (3) and were almost equal in both treatment groups, suggesting no obvious beneficial effect of surgical cisternal rinsing.

Our study is a relatively small single-center study with a limited power. The neuropsychologic examination was available in 114 (82.6%) of 138 of patients who underwent MR. Thereby, our finding that focal parenchymal lesion volumes correlate with neuropsychologic test performance cannot be generalized in a straightforward manner to all aSAH patients, although we would expect even stronger correlations if those patients with poor clinical outcome had undergone neuropsychologic testing. Many patients with a favorable clinical outcome had already participated in neuropsychologic tests during the primary hospital stay and at 3 months, possibly explaining the relatively high rate of refusals.

In our study, the results are reported according to intention to treat analysis, although 15 (10.9%) of 138 patients (mostly from the endovascular group) needed additional combination treatment to isolate the ruptured aneurysm from the circulation. Furthermore, unruptured aneurysms were treated according to current recommendations (13). However, repeating all the analyses after censoring the patients with combination treatment or additional treatment for nonruptured aneurysms did not produce notable changes in the significant differences between the treatment groups. Thus, our results in light of the long-term MR findings may further support other recent studies (4,7,8). In a certain group of patients, endovascular treatment practice could be advocated after aSAH, although complete occlusion of the aneurysm may require additional surgical treatment.

In conclusion, aSAH is frequently followed by permanent lesions in brain parenchyma, a majority of which are related to the primary bleeding, but some are adverse effects of the treatment procedures. Parental artery territory ischemic lesions seem to be more frequent after surgical rather than endovascular treatment of the ruptured aneurysm, especially in frontotemporal areas. Lesions associated with surgical retraction occur in more than half of the patients treated surgically. To achieve better patient outcome, modern microsurgical and endovascular techniques can help avoid unnecessary damage to the vessel wall, prevent thrombosis or thromboembolism, and leave the small perforating arteries intact. In addition, careful postoperative monitoring could help in preventing late vasospasm.


   APPENDIX: STUDY DESIGN
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
APPENDIX: STUDY DESIGN
ADVANCE IN KNOWLEDGE
IMPLICATIONS FOR PATIENT CARE...
 References
 
The study design was approved by the ethics committee at our hospital. During the study period (February 1, 1995, to December 31, 1999), all patients who were admitted to our university hospital because of primary aSAH were evaluated as potential candidates for the study. After informed consent was obtained from the patient or the patient's closest relative, all consecutive patients with a ruptured aneurysm that was considered to be suitable for both surgical clip and endovascular treatments were included on the basis of the following exclusion criteria: (a) age older than 75 years, (b) bleeding for more than 3 days before the procedure, (c) presence of a large hematoma necessitating surgery, (d) aneurysm associated with mass effect causing a neurologic deficit, or (e) previous surgery for the ruptured aneurysm.

The aneurysm was not considered suitable for endovascular treatment and the patient was not considered for random assignment to a management group if the following findings were present at angiography: (a) the neck of the aneurysm was wider than the fundus, (b) the presence of fusiform aneurysm, (c) the neck and its relationship to the parent vessel and adjacent branches were indistinguishable, or (d) the diameter of the aneurysm was less than 2 mm (smaller than the smallest coil available). The patient's eligibility for random assignment and endovascular treatment was always considered according to the morphology of the aneurysm that had most probably ruptured (aneurysm irregularity, size, and findings seen at CT).

To avoid selection bias, random assignment was performed separately for patient groups with Hunt and Hess grades I–II, grade III, and grades IV–V. After the procedure, patients who underwent surgery and those who underwent endovascular treatment received similar care in the intensive care unit.

Follow-up angiography was scheduled after surgical clip treatment during the primary hospital stay and, in cases of a minor neck remnant, 12 months after clip treatment. Follow-up angiographs were obtained 3 and 12 months after endovascular treatment. If total occlusion was not achieved in the first session, repeat embolization of the residual lumen was attempted in a second session or, in cases of a small neck remnant, at the time of the 3-month angiographic control procedure. Postembolization surgical clip treatment was considered in patients with unsuccessful or incomplete embolization, and repeat coil embolization was considered in patients with an incomplete surgical clip. Unruptured aneurysms were treated by using surgical or endovascular methods according to current recommendations (13).

Neuropsychologic tests were scheduled after surgical or endovascular treatment for ruptured aneurysm during the primary hospital stay and 3 and 12 months after aSAH.


   ADVANCE IN KNOWLEDGE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
APPENDIX: STUDY DESIGN
ADVANCE IN KNOWLEDGE
IMPLICATIONS FOR PATIENT CARE...
 References
 


   IMPLICATIONS FOR PATIENT CARE
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
APPENDIX: STUDY DESIGN
ADVANCE IN KNOWLEDGE
IMPLICATIONS FOR PATIENT CARE...
References
 


   FOOTNOTES
 

Abbreviations: aSAH = aneurysmal subarachnoid hemorrhage • SI = signal intensity

Author contributions: Guarantors of integrity of entire study, P.B., R.V.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, P.B., T.K., T.H., M.V., J.H., R.V.; clinical studies, P.B., T.K., H.H., T.S., M.V., J.H., R.V.; statistical analysis, P.B., T.K., M.K., T.H., R.V.; and manuscript editing, all authors

Authors stated no financial relationship to disclose.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
APPENDIX: STUDY DESIGN
ADVANCE IN KNOWLEDGE
IMPLICATIONS FOR PATIENT CARE...
 References
 

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