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Embolization of ruptured aneurysms in the acute stage: experience at a single institute
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Surgical Neurology 69 (2008) 478 – 482 www.surgicalneurology-online.com
Aneurysm
Embolization of ruptured aneurysms in the acute stage: experience at a single institute Makoto Sonobe, MD, PhD4, Yasunobu Nakai, MD, Kyoichi Sugita, MD, PhD, Noriyuki Kato, MD, PhD, Soshi Okamoto, MD, PhD Department of Neurosurgery, National Hospital Organization, Mito Medical Center, Ibaraki, Ibaraki 311-3193, Japan Received 17 July 2006; accepted 5 January 2007
Abstract
Background: Recently, several reports have shown embolization to be more beneficial than surgical clipping for the treatment of ANs, because the former is less invasive. In our department, GDCE has been the first choice of treatment for ANs since 1977. In this work, we present our clinical results with GDCE and suggest this approach as an alternative treatment of ruptured ANs in the acute stage. Methods: We treated 247 consecutive patients with acute-stage AN ruptures using GDC. To prevent symptomatic vasospasm, continuous lumbar drainage was performed before GDCE. If blood clots in the basal cisterns were dense on computerized tomography, TPA was administered through a lumbar spinal drainage tube. Results: Of the 247 patients, 196 (79%) had excellent or good outcomes at 3 months after treatment. Symptomatic vasospasm occurred in 27 patients (13.9%), and 25 required chemical or mechanical angioplasty. Permanent morbidity due to vasospasm occurred in 8 patients (4.1%), and 3 patients died (1.5%). Conclusion: Subjects, perioperative treatment methods, and outcomes were assessed consecutively and prospectively in a single institution, making the results of this study particularly valuable. Although very long-term results of treating ANs with GDCE have yet to be obtained, our results suggest that embolization of ruptured ANs in the acute stage with GDC is a safe, feasible method of treatment. D 2008 Elsevier Inc. All rights reserved.
Keywords:
Intracranial aneurysm; Subarachnoid hemorrhage; Acute stage; Guglielmi detachable coil; Vasospasm
1. Introduction Surgical clipping based on the development of microsurgical techniques has long been a gold standard for the treatment of ANs. However, for patients who are not suitable surgical candidates because of the anatomical location of their ANs or who are in critical condition, other methods of Abbreviations: ANs, aneurysms; BF, body filling; CO, complete occlusion; DSA, digital subtraction angiography; GDCE, Guglielmi detachable coil embolization; GDC, Guglielmi detachable coils; ISAT, International Subarchnoid Aneurysm Trial; NR, neck remnant; SAH, subarachnoid hemorrhage; TPA, tissue plasminogen activator. 4 Corresponding author. Tel.: +1 81 29 240 7711; fax: +1 81 29 240 7788. E-mail address: [email protected] (M. Sonobe). 0090-3019/$ – see front matter D 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.surneu.2007.01.036
treatment including the use of detachable balloons, pushable microcoils, interlocking detachable coils, and liquid embolic agents to occlude ANs with preservation of the parent arteries, have been reported. In 1991, Guglielmi et al [2-4] developed the GDCE device, a groundbreaking tool for the treatment of ANs. Large numbers of ANs have since been treated, worldwide, using GDCE. There have been several reports on the efficacy of this new technique [1,5-8, 10,13,14]. For ruptured AN, the primary goal of treatment is to prevent rebleeding. Several reports have recently shown that GDCE is more beneficial than surgical clipping in that it is less invasive. In addition, the ISAT concluded that in patients with ruptured ANs, for which endovascular coiling and neurosurgical clipping are therapeutic options, the outcome in terms of disability-free survival at 1 year
M. Sonobe et al. / Surgical Neurology 69 (2008) 478 – 482
479
Table 1 Distribution of ruptured ANs (N = 247) by location
Table 2 Outcomes at 3 months in patients with ruptured ANs
Location
No. of ruptured ANs
Glasgow Outcome Scale
Anterior communicating artery Internal carotid artery Middle cerebral artery Basilar tip Anterior cerebral artery Vertebral artery Posterior cerebral artery Total
76 71 37 24 17 20 2 247
Hunt and Kosnick grade at embolization
GR
MD
SD
VS
Dead
Total
I II III IV V Total
17 75 59 21 3 175
2 5 5 7 2 21
1 5 4 10 1 21
1 1 5 2 9
1 8 8 4 21
20 87 77 51 12 247
GR indicates good recovery; MD, moderate disability; SD, severe disability; VS, vegetative state.
follow-up is significantly better with treatment using endovascular coiling [9]. Although recent studies have repeatedly confirmed the usefulness of GDCE, based on analysis of relatively large patient populations from different institutions, little effort has been made to assess results by using the same perioperative treatment methods and assessing outcomes consecutively and prospectively in a single institution. In our department, GDCE has been the first choice of treatment for condition since March 1997. Using the same treatment criteria for ruptured ANs in our institution, 247 patients were enrolled in this study. We describe herein the outcomes of treated patients and the effectiveness of GDCE, and suggest that this technique is a treatment option for ruptured ANs in the acute stage. 2. Materials and methods 2.1. Patient population Between March 1997 and October 2005, a total of 507 patients with SAH were admitted to the emergency care center of our hospital. Of these 507 patients, 84 were treated by surgical clipping and 176 were excluded without treatments by reason that 132 patients were serious on admission with Glasgow Coma Scale scores of 7 or lower, 28 had critical complications, and the origin of SAH was not found in 10. The remaining 247 patients were treated by GDCE in the acute stage after episodes of SAH (within 7 days after the onset) at Mito Medical Center. The study population consisted of 153 women and 94 men, with a mean age of 59.9 years (range, 29-88 years). All operations were performed by 2 of the authors (MS and YN), and perioperative management was performed by the same surgical team. Aneurysms were smaller than 15 mm but larger than 2 mm in diameter, and all had a clear neck portion. Aneurysms that did not meet the criteria were selected for clipping. The clippings were selected from patients with intracranial hematomas and those with severe atherosclerotic changes in the arteries adjacent to the ANs. The clippings were also selected from patients in which the ANs were in a hazardous anatomic location. Immediately before the operation, the patients were classified by using the Hunt and Kosnik grading system: grade I, 20; grade II, 87; grade III, 77; grade IV, 51; and grade V, 12. The locations of the ANs were as follows (Table 1): 76 ANs were in the anterior communicating artery,
71 in the internal carotid artery, 24 in the basilar tip, 17 in the anterior cerebral artery, 20 in the vertebral artery, 2 in the posterior cerebral artery, and 37 in the middle cerebral artery. The number of ANs involving the middle cerebral artery was smaller than the standard distribution because 41 ANs with this location were treated by surgical clipping. 2.2. Treatment of patients Operative procedures were performed under general anesthesia in all cases. A 6F guiding catheter, 2F nonbladed microcatheter, 0.012 microwire, and the GDC 10 system (Boston Scientific, Natick, MA) were routinely used. Systemic heparinization was performed in all cases after insertion of the sheath catheter. Before embolization of the ANs, spinal drains had been placed whenever possible to allow continuous drainage for about 14 days. For patients in whom computerized tomography (CT) revealed a dense clot in the basal cistern, the Hounsfield number was greater than 70 and the AN was completely occluded, 1 mg TPA was administered once within 72 hours after the onset of SAH through the spinal drainage catheter. Fasdile chloride (30 mg) was given intravenously every 8 hours for 2 weeks to prevent vasospasm. Balloon and/or chemical angioplasty (papaverine chloride) was performed when hyperdynamic therapy failed to reduce the symptoms and signs of vasospasm. Continuous heparinization after embolization depended on coil density status in the AN. 3. Results 3.1. Clinical features and outcomes Hunt and Kosnik grades and the corresponding outcomes at 3 months after treatment are summarized in Table 2. One hundred and ninety-six patients (79%) lived Table 3 Causes of morbidity and mortality Glasgow Outcome Scale N 3
No. of cases
Primary brain damage by SAH Rerupture Complications Cerebral vasospasm Poor condition
17 6 8 9 11
480
M. Sonobe et al. / Surgical Neurology 69 (2008) 478 – 482
Fig. 1. Symptomatic vasospasm.
independently (good recovery or moderate disability), 21 had severe disability, 9 were in a vegetative state, and 21 had died. Immediately after initial embolization, 145 (59%) ANs showed complete occlusion (CO) and 47 (19%) an NR, whereas 55 (22%) showed BF. Results of early follow-up
angiography prompted additional surgical clipping in 4 cases and additional embolization in 1 case, within 2 weeks after the initial embolization. On the other hand, embolization was performed in 2 cases judged as having unclippable AN. Follow-up angiographic results, more than 3 months after treatment, were available for 164 (72%) of the 226 surviving cases. Ninety-nine ANs (60%) exhibited complete occlusion, 30 (18%) an NR, and 35 (21%) BF. Two additional clipping and 2 reembolization procedures were performed for ANs with NR. Three clipping surgeries and 5 reembolizations were performed for ANs. Four patients with BF refused the additional treatment. During follow-up, rebleeding occurred in 8 patients, 4 of whom died. Causes of morbidity and mortality could be determined for 51 patients, including 17 with primary brain damage after SAH onset, 6 with rebleeding, 8 with treatment-related complications, 9 with vasospasm, and 11 with other critical medical complications (Table 3). On the other hand, in 84 patients treated by surgical clipping, 57patients (68%) lived independently (good
Fig. 2. A: CT scan showing a SAH. Hounsfield number of the basal cistern (star) is 82 F 24. B: DSA demonstrating an aneurysm arising from the ICA. C: DSA showing complete occlusion of the aneurysm by GDC. D: CT scan, obtained 3 days after TPA administration, demonstrates almost complete clearance of SAH from the basal cisterns.
M. Sonobe et al. / Surgical Neurology 69 (2008) 478 – 482
recovery or moderate disability), 15 had severe disability, 1 was in a vegetative state, and 11 had died. The difference between GDCE and the clipping group was not significant ( P = .42). 3.2. Complications Complications related to treatment procedures included 11 embolisms (4.4%) and 4 perforations of the AN (1.6%). Of the former 11 patients, 4 exhibited neurologic deterioration. Among the latter 4 patients, 1 died and 1 exhibited neurologic deterioration. The rate of permanent morbidity related to the treatment procedures was 2%, and the total mortality rate was 0.4%. Seven patients with embolisms and 2 with aneurysmal rupture had asymptomatic clinical manifestations. Eight cases had rebleeding within 3 months after the treatment procedures; 2 affected patients showed severe worsening of their disabilities and 4 died. 3.3. Symptomatic vasospasm Symptomatic vasospasm was mainly evaluated by neurologic examination. Of 247 patients, 193 (78.1%) were evaluable whereas 54 were not, due to persistent disturbance of consciousness and/or neurologic deficits before GDCE. Symptomatic vasospasm occurred in 27 patients (13.9%), and 25 required chemical or mechanical angioplasty. Permanent morbidity due to vasospasm occurred in 8 patients (4.1%), and 3 deaths were related to vasospasm (1.5%) (Fig. 1). 3.4. Illustrative case This 49-year-old man was transferred from another hospital 8 hours after the onset of SAH. The hemorrhage was classified as Hunt and Kosnik clinical grade 3. Computerized tomography scans revealed SAH predominantly in the basal cisterns and left Sylvian fissure. DSA revealed an AN at the left internal carotid artery. Under general anesthesia, a spinal drain was inserted and GDCE was performed to occlude the AN. Twelve hours after GDCE, TPA (1 mg) was administered via the spinal drain. The patient’s postoperative course was uneventful and he was discharged, ambulatory, with no morbidity. Computerized tomography obtained 3 days after administration of TPA revealed almost complete clearance of SAH from the basal cisterns (Fig. 2).
4. Discussion In 199l and l992, Guglielmi and colleagues [3,4] initially reported and then confirmed the use of detachable platinum microcoils to occlude ANs. Several reports have recently shown that embolization is more beneficial than surgical clipping in that it is less invasive. In 2002, a report from the ISAT indicated the usefulness of the embolization method and had a strong impact on the treatment of ANs [9]. In our department, since March 1997, GDCE has been the first
481
choice of treatment for ANs under the following conditions. In our experience, it is important to select ruptured ANs smaller than 15 mm but larger than 2 mm in diameter, which have a clear neck portion. Subarachnoid hemorrhages complicated by intracranial hematoma or associated with severe atherosclerotic changes in the arteries adjacent to ANs are contraindications for GDCE. The anatomical location and angiographic configuration of ANs are also very important factors in assuring the success of embolization. Because the subjects in this study were assessed consecutively and prospectively in a single institute, we believe the results obtained to be particularly valuable. Our institute is a central hospital serving an area with a population of 500 000. All patients with SAH in this area must be transferred to the medical emergency center of this hospital. During the period of this study (March 1997October 2005), a total of 507 patients with SAH were admitted to our hospital. Of these 507 patients, 84 were treated by surgical clipping and 176 were excluded from this study because of other medical conditions. The remaining 247 patients were treated by GDCE in the acute stage in our hospital after SAH episodes. Thus, 75% of treatable SAH patients were appropriate candidates for GDCE. As in previous reports, GDCE was contraindicated in most middle cerebral ANs because of the complex angiographic architecture of the AN. Thus, the total number of middle cerebral artery ANs was smaller than expected. We consider our results to be favorable because our morbidity plus mortality rate was relatively low at 51 (21%) of 247 patients. Furthermore, among the 51 affected patients, 8 (15.6%) were older than 75 years and some of them were surgically difficult cases. As to complications related to treatment procedures, there were 4 AN perforations, all of which occurred in patients treated before the year 2000. We believe that there is a learning curve for this technique. Eight cases experienced rebleeding in the acute period after GDCE resulting in death or severe disability. Four elderly patients (aged 77, 80, 80, and 84 years) with rebleeding due to insufficient embolization were not considered appropriate candidates for clipping because of their poor medical conditions. In these 4 patients, it was not possible to deliver a sufficient number of coils to prevent rebleeding because of severe atherosclerotic changes. Two of our patients experienced rebleeding despite the achievement of complete occlusion, the causes of which are unknown. Another patient with rebleeding had a good outcome after clipping surgery and reembolization. Direct removal of SAH clots is impossible in the treatment of ANs by endovascular procedures. We therefore placed spinal drains, to assure continuous drainage, in nearly all patients and administered TPA through the drainage tube to treat those with dense clots in the basal cisterns when the CT Hounsfield number exceeded 70. These treatment methods facilitated the drainage of cisternal clots and thus prevented vasospasm. Kinugasa et al [6] showed that emergent coil thrombosis of a ruptured AN followed by immediate
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M. Sonobe et al. / Surgical Neurology 69 (2008) 478 – 482
administration of TPA is a safe and effective means of preventing vasospasm and improving patient outcome. Paul et al [12] recently reported that drainage of bloody cerebrospinal fluid through a lumbar drainage tube after an episode of SAH markedly reduces the risk of clinically evident vasospasm and its sequelae, as well as shortening hospitalization and improving outcome. In our study, the rate of symptomatic vasospasm was 13.9%, and the permanent morbidity and mortality rates were 4.1% and 1.5%, respectively. By comparison, Murayama et al [11] reported a higher rate of complications including a symptomatic spasm rate of 23%, and permanent morbidity and mortality rates of 2.9% each. Debrun et al [1] reported symptomatic spasm, permanent morbidity, and mortality rates of 22%, 3.6%, and 5.3%, respectively. To our knowledge, we obtained the lowest reported incidence of symptomatic vasospasm with the same GDCE procedure. We thus suggest that endovascular treatment does not increase the rate of symptomatic vasospasm, and that continuous drainage of bloody cerebrospinal fluid with intrathecal TPA administration promotes clot lysis and may thereby decrease the incidence and severity of vasospasm after GDCE. 5. Conclusions In conclusion, GDCE for treatment of ruptured cerebral ANs in the acute stage is less invasive than surgical clipping and can yield the same results. This treatment, in conjunction with continuous spinal drainage, is associated with a low incidence of symptomatic vasospasm. Guglielmi detachable coil embolization can thus serve as the first-line treatment of ruptured cerebral ANs. Because subjects, perioperative treatment methods, and outcomes were assessed consecutively and prospectively in a single institution, our results are particularly valuable. Very longterm follow-up of patients who have received this treatment is, however, essential. Acknowledgments We thank Dr. Bierta Barfod for language editing and her invaluable advice. References [1] Debrun M, Aletich A, Pierre K, et al. Selection of cerebral aneurysms for treatment using Guglielmi detachable coils: the preliminary University of Illinois at Chicago experience. Neurosurgery 1998;43: 1281 - 95. [2] Guglielmi G, Vinuela F, Ivan S, et al. Electrothrombosis of saccular aneurysms via endovascular approach: Part 1. Electrochemical basis, technique, and experimental results. J Neurosurg 1991;75:1 - 7.
[3] Guglielmi G, Vinuela F, Jacques D, et al. Electrothrombosis of saccular aneurysms via endovascular approach: Part 2. Preliminary clinical experience. J Neurosurg 1991;75:8 - 14. [4] Guglielmi G, Vinuela F, Gary D, et al. Endovascular treatment of posterior circulation aneurysms by electrothrombosis using electrically detachable coils. J Neurosurg 1992;77:515 - 24. [5] Graves B, Strother M, Thomas D, et al. Early treatment of ruptured aneurysms with Guglielmi detachable coils: effect on subsequent bleeding. Neurosurgery 1995;37:640 - 8. [6] Kinugasa K, Kamata I, Hirotune N, et al. Early treatment of subarachnoid hemorrhage after preventing re-rupture of an aneurysm. J Neurosurg 1995;83:34 - 41. [7] Malisch W, Guglielmi G, Vinuela F, et al. Intracranial aneurysms treated with the Guglielmi detachable coil: midterm clinical results in a consecutive series of 100 patients. J Neurosurg 1997;87:176 - 83. [8] Matsumaru Y, Sonobe M, Sugita K, et al. The embolization of ruptured aneurysms in acute stage with Guglielmi detachable coils. Interv Neuroradiol 1999;5(Suppl 1):191 - 3. [9] Molyneux A, Kerr R, Stratton I, et al. International Subarachnoid Aneurysm Trial (ISAT) Collaborative Group: International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet 2002;360(9342):1267 - 74. [10] Moret J, Cognard C, Weill A, et al. The bRemodeling techniqueQ in the treatment of wide neck intracranial aneurysms. Interv Neuroradiol 1997;3:2 - 35. [11] Murayama Y, Malisch T, et al. Incidence of cerebral vasospasm after endovascular treatment of acutely ruptured aneurysms: report on 69 cases. J Neurosurg 1997;87:830 - 5. [12] Paul K, John K, Joel M, et al. Marked reduction of cerebral vasospasm with lumbar drain of cerebral fluid after subarachnoid hemorrhage. J Neurosurg 2004;100:215 - 24. [13] Shibuya M, Suzuki Y, et al. Effect of AT877 on cerebral vasospasm after aneurysmal subarachnoid hemorrhage: result of a prospective placebo-controlled double-blind trial. J Neurosurg 1992;76:571 - 7. [14] Vinuela F, Duckwiler G, Michel M, et al. Guglielmi detachable coil embolization of acute intracranial aneurysms: perioperative anatomical and clinical outcome in 403 patients. J Neurosurg 1997;86:475 - 82.
Commentary The authors present their treatment outcome of ruptured aneurysms with GDC coil embolization in the acute stage. They show an excellent outcome with GDC. However, the results may be influenced with the use of spinal drainage and tissue plasminogen activator. The article is especially meaningful because this is 1 of the earliest trials to treat ruptured aneurysm with coil first strategy in the Japanese populations. In this study, they excluded 176 patients because of the initial severity of SAH or other reasons. Therefore, care must be taken in interpreting their results. Nobuhito Saito, MD, PhD Department of Neurosurgery Gunma University Graduate School of Medicine Gunma 371-8511, Japan
Surgical Neurology 69 (2008) 478 – 482 www.surgicalneurology-online.com
Aneurysm
Embolization of ruptured aneurysms in the acute stage: experience at a single institute Makoto Sonobe, MD, PhD4, Yasunobu Nakai, MD, Kyoichi Sugita, MD, PhD, Noriyuki Kato, MD, PhD, Soshi Okamoto, MD, PhD Department of Neurosurgery, National Hospital Organization, Mito Medical Center, Ibaraki, Ibaraki 311-3193, Japan Received 17 July 2006; accepted 5 January 2007
Abstract
Background: Recently, several reports have shown embolization to be more beneficial than surgical clipping for the treatment of ANs, because the former is less invasive. In our department, GDCE has been the first choice of treatment for ANs since 1977. In this work, we present our clinical results with GDCE and suggest this approach as an alternative treatment of ruptured ANs in the acute stage. Methods: We treated 247 consecutive patients with acute-stage AN ruptures using GDC. To prevent symptomatic vasospasm, continuous lumbar drainage was performed before GDCE. If blood clots in the basal cisterns were dense on computerized tomography, TPA was administered through a lumbar spinal drainage tube. Results: Of the 247 patients, 196 (79%) had excellent or good outcomes at 3 months after treatment. Symptomatic vasospasm occurred in 27 patients (13.9%), and 25 required chemical or mechanical angioplasty. Permanent morbidity due to vasospasm occurred in 8 patients (4.1%), and 3 patients died (1.5%). Conclusion: Subjects, perioperative treatment methods, and outcomes were assessed consecutively and prospectively in a single institution, making the results of this study particularly valuable. Although very long-term results of treating ANs with GDCE have yet to be obtained, our results suggest that embolization of ruptured ANs in the acute stage with GDC is a safe, feasible method of treatment. D 2008 Elsevier Inc. All rights reserved.
Keywords:
Intracranial aneurysm; Subarachnoid hemorrhage; Acute stage; Guglielmi detachable coil; Vasospasm
1. Introduction Surgical clipping based on the development of microsurgical techniques has long been a gold standard for the treatment of ANs. However, for patients who are not suitable surgical candidates because of the anatomical location of their ANs or who are in critical condition, other methods of Abbreviations: ANs, aneurysms; BF, body filling; CO, complete occlusion; DSA, digital subtraction angiography; GDCE, Guglielmi detachable coil embolization; GDC, Guglielmi detachable coils; ISAT, International Subarchnoid Aneurysm Trial; NR, neck remnant; SAH, subarachnoid hemorrhage; TPA, tissue plasminogen activator. 4 Corresponding author. Tel.: +1 81 29 240 7711; fax: +1 81 29 240 7788. E-mail address: [email protected] (M. Sonobe). 0090-3019/$ – see front matter D 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.surneu.2007.01.036
treatment including the use of detachable balloons, pushable microcoils, interlocking detachable coils, and liquid embolic agents to occlude ANs with preservation of the parent arteries, have been reported. In 1991, Guglielmi et al [2-4] developed the GDCE device, a groundbreaking tool for the treatment of ANs. Large numbers of ANs have since been treated, worldwide, using GDCE. There have been several reports on the efficacy of this new technique [1,5-8, 10,13,14]. For ruptured AN, the primary goal of treatment is to prevent rebleeding. Several reports have recently shown that GDCE is more beneficial than surgical clipping in that it is less invasive. In addition, the ISAT concluded that in patients with ruptured ANs, for which endovascular coiling and neurosurgical clipping are therapeutic options, the outcome in terms of disability-free survival at 1 year
M. Sonobe et al. / Surgical Neurology 69 (2008) 478 – 482
479
Table 1 Distribution of ruptured ANs (N = 247) by location
Table 2 Outcomes at 3 months in patients with ruptured ANs
Location
No. of ruptured ANs
Glasgow Outcome Scale
Anterior communicating artery Internal carotid artery Middle cerebral artery Basilar tip Anterior cerebral artery Vertebral artery Posterior cerebral artery Total
76 71 37 24 17 20 2 247
Hunt and Kosnick grade at embolization
GR
MD
SD
VS
Dead
Total
I II III IV V Total
17 75 59 21 3 175
2 5 5 7 2 21
1 5 4 10 1 21
1 1 5 2 9
1 8 8 4 21
20 87 77 51 12 247
GR indicates good recovery; MD, moderate disability; SD, severe disability; VS, vegetative state.
follow-up is significantly better with treatment using endovascular coiling [9]. Although recent studies have repeatedly confirmed the usefulness of GDCE, based on analysis of relatively large patient populations from different institutions, little effort has been made to assess results by using the same perioperative treatment methods and assessing outcomes consecutively and prospectively in a single institution. In our department, GDCE has been the first choice of treatment for condition since March 1997. Using the same treatment criteria for ruptured ANs in our institution, 247 patients were enrolled in this study. We describe herein the outcomes of treated patients and the effectiveness of GDCE, and suggest that this technique is a treatment option for ruptured ANs in the acute stage. 2. Materials and methods 2.1. Patient population Between March 1997 and October 2005, a total of 507 patients with SAH were admitted to the emergency care center of our hospital. Of these 507 patients, 84 were treated by surgical clipping and 176 were excluded without treatments by reason that 132 patients were serious on admission with Glasgow Coma Scale scores of 7 or lower, 28 had critical complications, and the origin of SAH was not found in 10. The remaining 247 patients were treated by GDCE in the acute stage after episodes of SAH (within 7 days after the onset) at Mito Medical Center. The study population consisted of 153 women and 94 men, with a mean age of 59.9 years (range, 29-88 years). All operations were performed by 2 of the authors (MS and YN), and perioperative management was performed by the same surgical team. Aneurysms were smaller than 15 mm but larger than 2 mm in diameter, and all had a clear neck portion. Aneurysms that did not meet the criteria were selected for clipping. The clippings were selected from patients with intracranial hematomas and those with severe atherosclerotic changes in the arteries adjacent to the ANs. The clippings were also selected from patients in which the ANs were in a hazardous anatomic location. Immediately before the operation, the patients were classified by using the Hunt and Kosnik grading system: grade I, 20; grade II, 87; grade III, 77; grade IV, 51; and grade V, 12. The locations of the ANs were as follows (Table 1): 76 ANs were in the anterior communicating artery,
71 in the internal carotid artery, 24 in the basilar tip, 17 in the anterior cerebral artery, 20 in the vertebral artery, 2 in the posterior cerebral artery, and 37 in the middle cerebral artery. The number of ANs involving the middle cerebral artery was smaller than the standard distribution because 41 ANs with this location were treated by surgical clipping. 2.2. Treatment of patients Operative procedures were performed under general anesthesia in all cases. A 6F guiding catheter, 2F nonbladed microcatheter, 0.012 microwire, and the GDC 10 system (Boston Scientific, Natick, MA) were routinely used. Systemic heparinization was performed in all cases after insertion of the sheath catheter. Before embolization of the ANs, spinal drains had been placed whenever possible to allow continuous drainage for about 14 days. For patients in whom computerized tomography (CT) revealed a dense clot in the basal cistern, the Hounsfield number was greater than 70 and the AN was completely occluded, 1 mg TPA was administered once within 72 hours after the onset of SAH through the spinal drainage catheter. Fasdile chloride (30 mg) was given intravenously every 8 hours for 2 weeks to prevent vasospasm. Balloon and/or chemical angioplasty (papaverine chloride) was performed when hyperdynamic therapy failed to reduce the symptoms and signs of vasospasm. Continuous heparinization after embolization depended on coil density status in the AN. 3. Results 3.1. Clinical features and outcomes Hunt and Kosnik grades and the corresponding outcomes at 3 months after treatment are summarized in Table 2. One hundred and ninety-six patients (79%) lived Table 3 Causes of morbidity and mortality Glasgow Outcome Scale N 3
No. of cases
Primary brain damage by SAH Rerupture Complications Cerebral vasospasm Poor condition
17 6 8 9 11
480
M. Sonobe et al. / Surgical Neurology 69 (2008) 478 – 482
Fig. 1. Symptomatic vasospasm.
independently (good recovery or moderate disability), 21 had severe disability, 9 were in a vegetative state, and 21 had died. Immediately after initial embolization, 145 (59%) ANs showed complete occlusion (CO) and 47 (19%) an NR, whereas 55 (22%) showed BF. Results of early follow-up
angiography prompted additional surgical clipping in 4 cases and additional embolization in 1 case, within 2 weeks after the initial embolization. On the other hand, embolization was performed in 2 cases judged as having unclippable AN. Follow-up angiographic results, more than 3 months after treatment, were available for 164 (72%) of the 226 surviving cases. Ninety-nine ANs (60%) exhibited complete occlusion, 30 (18%) an NR, and 35 (21%) BF. Two additional clipping and 2 reembolization procedures were performed for ANs with NR. Three clipping surgeries and 5 reembolizations were performed for ANs. Four patients with BF refused the additional treatment. During follow-up, rebleeding occurred in 8 patients, 4 of whom died. Causes of morbidity and mortality could be determined for 51 patients, including 17 with primary brain damage after SAH onset, 6 with rebleeding, 8 with treatment-related complications, 9 with vasospasm, and 11 with other critical medical complications (Table 3). On the other hand, in 84 patients treated by surgical clipping, 57patients (68%) lived independently (good
Fig. 2. A: CT scan showing a SAH. Hounsfield number of the basal cistern (star) is 82 F 24. B: DSA demonstrating an aneurysm arising from the ICA. C: DSA showing complete occlusion of the aneurysm by GDC. D: CT scan, obtained 3 days after TPA administration, demonstrates almost complete clearance of SAH from the basal cisterns.
M. Sonobe et al. / Surgical Neurology 69 (2008) 478 – 482
recovery or moderate disability), 15 had severe disability, 1 was in a vegetative state, and 11 had died. The difference between GDCE and the clipping group was not significant ( P = .42). 3.2. Complications Complications related to treatment procedures included 11 embolisms (4.4%) and 4 perforations of the AN (1.6%). Of the former 11 patients, 4 exhibited neurologic deterioration. Among the latter 4 patients, 1 died and 1 exhibited neurologic deterioration. The rate of permanent morbidity related to the treatment procedures was 2%, and the total mortality rate was 0.4%. Seven patients with embolisms and 2 with aneurysmal rupture had asymptomatic clinical manifestations. Eight cases had rebleeding within 3 months after the treatment procedures; 2 affected patients showed severe worsening of their disabilities and 4 died. 3.3. Symptomatic vasospasm Symptomatic vasospasm was mainly evaluated by neurologic examination. Of 247 patients, 193 (78.1%) were evaluable whereas 54 were not, due to persistent disturbance of consciousness and/or neurologic deficits before GDCE. Symptomatic vasospasm occurred in 27 patients (13.9%), and 25 required chemical or mechanical angioplasty. Permanent morbidity due to vasospasm occurred in 8 patients (4.1%), and 3 deaths were related to vasospasm (1.5%) (Fig. 1). 3.4. Illustrative case This 49-year-old man was transferred from another hospital 8 hours after the onset of SAH. The hemorrhage was classified as Hunt and Kosnik clinical grade 3. Computerized tomography scans revealed SAH predominantly in the basal cisterns and left Sylvian fissure. DSA revealed an AN at the left internal carotid artery. Under general anesthesia, a spinal drain was inserted and GDCE was performed to occlude the AN. Twelve hours after GDCE, TPA (1 mg) was administered via the spinal drain. The patient’s postoperative course was uneventful and he was discharged, ambulatory, with no morbidity. Computerized tomography obtained 3 days after administration of TPA revealed almost complete clearance of SAH from the basal cisterns (Fig. 2).
4. Discussion In 199l and l992, Guglielmi and colleagues [3,4] initially reported and then confirmed the use of detachable platinum microcoils to occlude ANs. Several reports have recently shown that embolization is more beneficial than surgical clipping in that it is less invasive. In 2002, a report from the ISAT indicated the usefulness of the embolization method and had a strong impact on the treatment of ANs [9]. In our department, since March 1997, GDCE has been the first
481
choice of treatment for ANs under the following conditions. In our experience, it is important to select ruptured ANs smaller than 15 mm but larger than 2 mm in diameter, which have a clear neck portion. Subarachnoid hemorrhages complicated by intracranial hematoma or associated with severe atherosclerotic changes in the arteries adjacent to ANs are contraindications for GDCE. The anatomical location and angiographic configuration of ANs are also very important factors in assuring the success of embolization. Because the subjects in this study were assessed consecutively and prospectively in a single institute, we believe the results obtained to be particularly valuable. Our institute is a central hospital serving an area with a population of 500 000. All patients with SAH in this area must be transferred to the medical emergency center of this hospital. During the period of this study (March 1997October 2005), a total of 507 patients with SAH were admitted to our hospital. Of these 507 patients, 84 were treated by surgical clipping and 176 were excluded from this study because of other medical conditions. The remaining 247 patients were treated by GDCE in the acute stage in our hospital after SAH episodes. Thus, 75% of treatable SAH patients were appropriate candidates for GDCE. As in previous reports, GDCE was contraindicated in most middle cerebral ANs because of the complex angiographic architecture of the AN. Thus, the total number of middle cerebral artery ANs was smaller than expected. We consider our results to be favorable because our morbidity plus mortality rate was relatively low at 51 (21%) of 247 patients. Furthermore, among the 51 affected patients, 8 (15.6%) were older than 75 years and some of them were surgically difficult cases. As to complications related to treatment procedures, there were 4 AN perforations, all of which occurred in patients treated before the year 2000. We believe that there is a learning curve for this technique. Eight cases experienced rebleeding in the acute period after GDCE resulting in death or severe disability. Four elderly patients (aged 77, 80, 80, and 84 years) with rebleeding due to insufficient embolization were not considered appropriate candidates for clipping because of their poor medical conditions. In these 4 patients, it was not possible to deliver a sufficient number of coils to prevent rebleeding because of severe atherosclerotic changes. Two of our patients experienced rebleeding despite the achievement of complete occlusion, the causes of which are unknown. Another patient with rebleeding had a good outcome after clipping surgery and reembolization. Direct removal of SAH clots is impossible in the treatment of ANs by endovascular procedures. We therefore placed spinal drains, to assure continuous drainage, in nearly all patients and administered TPA through the drainage tube to treat those with dense clots in the basal cisterns when the CT Hounsfield number exceeded 70. These treatment methods facilitated the drainage of cisternal clots and thus prevented vasospasm. Kinugasa et al [6] showed that emergent coil thrombosis of a ruptured AN followed by immediate
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administration of TPA is a safe and effective means of preventing vasospasm and improving patient outcome. Paul et al [12] recently reported that drainage of bloody cerebrospinal fluid through a lumbar drainage tube after an episode of SAH markedly reduces the risk of clinically evident vasospasm and its sequelae, as well as shortening hospitalization and improving outcome. In our study, the rate of symptomatic vasospasm was 13.9%, and the permanent morbidity and mortality rates were 4.1% and 1.5%, respectively. By comparison, Murayama et al [11] reported a higher rate of complications including a symptomatic spasm rate of 23%, and permanent morbidity and mortality rates of 2.9% each. Debrun et al [1] reported symptomatic spasm, permanent morbidity, and mortality rates of 22%, 3.6%, and 5.3%, respectively. To our knowledge, we obtained the lowest reported incidence of symptomatic vasospasm with the same GDCE procedure. We thus suggest that endovascular treatment does not increase the rate of symptomatic vasospasm, and that continuous drainage of bloody cerebrospinal fluid with intrathecal TPA administration promotes clot lysis and may thereby decrease the incidence and severity of vasospasm after GDCE. 5. Conclusions In conclusion, GDCE for treatment of ruptured cerebral ANs in the acute stage is less invasive than surgical clipping and can yield the same results. This treatment, in conjunction with continuous spinal drainage, is associated with a low incidence of symptomatic vasospasm. Guglielmi detachable coil embolization can thus serve as the first-line treatment of ruptured cerebral ANs. Because subjects, perioperative treatment methods, and outcomes were assessed consecutively and prospectively in a single institution, our results are particularly valuable. Very longterm follow-up of patients who have received this treatment is, however, essential. Acknowledgments We thank Dr. Bierta Barfod for language editing and her invaluable advice. References [1] Debrun M, Aletich A, Pierre K, et al. Selection of cerebral aneurysms for treatment using Guglielmi detachable coils: the preliminary University of Illinois at Chicago experience. Neurosurgery 1998;43: 1281 - 95. [2] Guglielmi G, Vinuela F, Ivan S, et al. Electrothrombosis of saccular aneurysms via endovascular approach: Part 1. Electrochemical basis, technique, and experimental results. J Neurosurg 1991;75:1 - 7.
[3] Guglielmi G, Vinuela F, Jacques D, et al. Electrothrombosis of saccular aneurysms via endovascular approach: Part 2. Preliminary clinical experience. J Neurosurg 1991;75:8 - 14. [4] Guglielmi G, Vinuela F, Gary D, et al. Endovascular treatment of posterior circulation aneurysms by electrothrombosis using electrically detachable coils. J Neurosurg 1992;77:515 - 24. [5] Graves B, Strother M, Thomas D, et al. Early treatment of ruptured aneurysms with Guglielmi detachable coils: effect on subsequent bleeding. Neurosurgery 1995;37:640 - 8. [6] Kinugasa K, Kamata I, Hirotune N, et al. Early treatment of subarachnoid hemorrhage after preventing re-rupture of an aneurysm. J Neurosurg 1995;83:34 - 41. [7] Malisch W, Guglielmi G, Vinuela F, et al. Intracranial aneurysms treated with the Guglielmi detachable coil: midterm clinical results in a consecutive series of 100 patients. J Neurosurg 1997;87:176 - 83. [8] Matsumaru Y, Sonobe M, Sugita K, et al. The embolization of ruptured aneurysms in acute stage with Guglielmi detachable coils. Interv Neuroradiol 1999;5(Suppl 1):191 - 3. [9] Molyneux A, Kerr R, Stratton I, et al. International Subarachnoid Aneurysm Trial (ISAT) Collaborative Group: International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet 2002;360(9342):1267 - 74. [10] Moret J, Cognard C, Weill A, et al. The bRemodeling techniqueQ in the treatment of wide neck intracranial aneurysms. Interv Neuroradiol 1997;3:2 - 35. [11] Murayama Y, Malisch T, et al. Incidence of cerebral vasospasm after endovascular treatment of acutely ruptured aneurysms: report on 69 cases. J Neurosurg 1997;87:830 - 5. [12] Paul K, John K, Joel M, et al. Marked reduction of cerebral vasospasm with lumbar drain of cerebral fluid after subarachnoid hemorrhage. J Neurosurg 2004;100:215 - 24. [13] Shibuya M, Suzuki Y, et al. Effect of AT877 on cerebral vasospasm after aneurysmal subarachnoid hemorrhage: result of a prospective placebo-controlled double-blind trial. J Neurosurg 1992;76:571 - 7. [14] Vinuela F, Duckwiler G, Michel M, et al. Guglielmi detachable coil embolization of acute intracranial aneurysms: perioperative anatomical and clinical outcome in 403 patients. J Neurosurg 1997;86:475 - 82.
Commentary The authors present their treatment outcome of ruptured aneurysms with GDC coil embolization in the acute stage. They show an excellent outcome with GDC. However, the results may be influenced with the use of spinal drainage and tissue plasminogen activator. The article is especially meaningful because this is 1 of the earliest trials to treat ruptured aneurysm with coil first strategy in the Japanese populations. In this study, they excluded 176 patients because of the initial severity of SAH or other reasons. Therefore, care must be taken in interpreting their results. Nobuhito Saito, MD, PhD Department of Neurosurgery Gunma University Graduate School of Medicine Gunma 371-8511, Japan