|Year : 2014 | Volume
| Issue : 1 | Page : 184-190
Safety and efficacy of endovascular treatment of ruptured cerebral aneurysms
Ahmed S. Mansour1, Essam E. Gaber1, Tamer Hassan2, Hytham AlBeltagy1, Waseem Hamed2, Mohammed Shadad3, Shawky S. Gad4
1 Department of Neurosurgery, Faculty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of Neurosurgery, Faculty of Medicine, Alexandria University, Alexandria, Egypt
3 Department of Neurosurgery, Faculty of Medicine, Tanta University, Tanta, Egypt
4 Department of General Surgery Department, Faculty of Medicine, Menoufia University, Menoufia, Egypt
|Date of Submission||16-Sep-2013|
|Date of Acceptance||07-Nov-2013|
|Date of Web Publication||20-May-2014|
Ahmed S. Mansour
Department of Neurosurgery, Menoufia Faculty of Medicine, Yaseen Abdelghaffar Street, Shebin El-Koum
Source of Support: None, Conflict of Interest: None
The aim of this study was to study the safety and efficacy of endovascular treatment of ruptured cerebral aneurysms.
Endovascular treatment has become a standard method for the treatment of intracranial aneurysms.
Materials and methods
A total of 12 patients were referred for endovascular treatment of ruptured aneurysms: six women and six men, with a mean age of 48.8 years. Patients were classified according to the Hunt and Hess grading system. There were one grade I patient (8.3%), five grade II (41.6%) patients, and six grade III (50%) patients. No patient belonged to grade IV (0%) or grade V (0%). Clinical follow-up was conducted at 6 months, and the results are classified according to the Glasgow Outcome Scale (GOS). Control angiograms were obtained immediately and at 6 months.
Immediate angiographic results were satisfactory in seven patients (58.3%; complete obliteration), and five patients experienced some residual symptoms of their aneurysms (41.6%). The mortality and morbidity was low. At 6 months, the outcomes were as follows: GOS score of 1, two patients (16.6%); GOS score of 2, seven patients (58.3%); GOS score of 3, three patients (25%); and GOS score of 4 and 5, zero patients (0%). Six-month angiographic follow-up data were available for 10 patients (83.3%). The morphological results were satisfactory in most patients: complete occlusion in seven patients (58.3%) and residual or incomplete occlusion in three patients (25%); two patients (16.6%) underwent recoiling.
Endovascular treatment of ruptured aneurysms was attempted without clinically significant complications in 91.6% of patients. Morphological results were unsatisfactory in 16.6% of patients. Complete obliteration of the sac, with or without residual neck, is essential to prevent subsequent bleeding, which occurred in 66.6% of patients. The overall outcome at 6 months was satisfactory, despite a selected group of patients [three patients (25%)] having residual complications or residual aneurysms.
Keywords: Complete occlusion, endovascular treatment, Glasgow outcome score, ruptured cerebral aneurysms
|How to cite this article:|
Mansour AS, Gaber EE, Hassan T, AlBeltagy H, Hamed W, Shadad M, Gad SS. Safety and efficacy of endovascular treatment of ruptured cerebral aneurysms. Menoufia Med J 2014;27:184-90
|How to cite this URL:|
Mansour AS, Gaber EE, Hassan T, AlBeltagy H, Hamed W, Shadad M, Gad SS. Safety and efficacy of endovascular treatment of ruptured cerebral aneurysms. Menoufia Med J [serial online] 2014 [cited 2017 Dec 14];27:184-90. Available from: http://www.mmj.eg.net/text.asp?2014/27/1/184/132798
| Introduction|| |
The National Institute of Neurological Disorders defines a cerebral aneurysm as dilatation, bulging, or ballooning out of a part of the wall of a vein or artery in the brain. As the aneurysm enlarges, the risk of rupture increases. Once an aneurysm ruptures, blood is pumped out of the vessel at high pressure into the subarachnoid space, ventricles, surrounding brain substance, or subdural space . The incidence of subarachnoid hemorrhage is estimated to be 5-10 per 100000 per year. The true incidence of intracranial aneurysms is unknown but is estimated at 1-6% of the population. Of the patients, 10-30% have multiple intracranial aneurysms. The overall female-to-male ratio is 5:1. Cerebral aneurysms can be classified into saccular, fusiform, or dissecting aneurysms. Approximately 86.5% of all intracranial aneurysms arise on the anterior side (carotid). About 10% of all intracranial aneurysms arise on the posterior side (vertebrobasilar) . Most intracranial aneurysms are asymptomatic but may be discovered incidentally during neuroimaging studies. Unruptured aneurysms are also detected when symptoms appear because of the compression of nerves or adjacent brain tissue: bulging of an aneurysm can cause headache, vomiting, and an altered level of consciousness; however, in some cases an aneurysm is not detected until it has ruptured. A ruptured intracranial aneurysm beneath the subarachnoid membrane causes bleeding into the brain, that is, subarachnoid hemorrhage, causing ischemia and brain damage, decreased cerebral perfusion, brain shift and herniation, hydrocephalus, severe motor and sensory loss, and possibly coma and death. The International Study on Unruptured Intracranial Aneurysms has also suggested that coil embolization is a valid alternative to surgery, especially in patients older than 50 years with aneurysms greater than 10mm in size and those of the posterior circulation. The endovascular technique is divided into a vascular access phase, which involves placing a guide catheter in the internal carotid artery or vertebral artery, and an interventional phase, which involves placement of a microcatheter in the aneurysm and deployment of the coils, as well as the adjunctive technique such as stent-assisted or balloon-assisted coiling .
| Materials and methods|| |
From 2011 until 2013, 12 patients were referred for endovascular treatment of ruptured aneurysms. These included six women and six men with a mean age of 48.8 years. Patients were classified according to the Hunt and Hess grading system [Table 1] . There were one grade I patient (8.3%), five grade II patients (41.6%), and six grade III patients (50%). No patients were of grade IV (0%) or grade V (0%). Clinical follow-up was conducted at 6 months, and results were classified according to the Glasgow Outcome Scale (GOS) [Table 2] . Control angiograms were obtained immediately and at 6 months.
All patients were assessed before the procedure.
Complete personal history including name, age, sex, and information on hypertension, smoking status, alcohol intake, and trauma was obtained. Enquires were also made on family history of stroke, hypertension, and diabetes mellitus. While taking the history of present illness, the onset, course and duration were stressed upon. Patients were asked about their symptoms, including headache, vomiting, failure of visual acuity, double vision, epileptic fits, neck pain or stiffness, facial weakness, motor weakness, sphincter disturbances, and deterioration in the level of consciousness.
Patients were examined by assessing their vital signs and for the presence of stretch signs, using the Hunt and Hess grading system and Glasgow Coma Scale, and by conducting complete neurological examination.
Investigations included routine laboratory investigations and neuroradiological investigations such as computed tomography (CT).
The volume of blood in the initial CT scan was classified according to the Fisher grading scale [Table 3] . Angiography was performed; the angiographic procedures included one or more of the following procedures: three dimensional CT angiography, magnetic resonance angiography, conventional four-vessel cerebral angiography, or digital subtraction.
Emergency care included assessment of the adequacy of the airway, breathing, and circulatory function. Most patients were admitted to the intensive care unit.
True contraindications are rare. They include coagulation disorders and known adverse reactions to heparin, history of anaphylactic or severe adverse reactions to contrast material, and renal failure and other conditions restricting the use of contrast material. Procedural assessment included collection of data on the procedure, including timing of the procedure, anesthesia used, type of the procedure, materials used, and procedural complications. Postprocedural assessment included assessment of the patient's clinical condition using the Hunt and Hess grading scale and evaluation of the clinical outcome at the latest clinical follow-up using GOS and the modified Rankin Scale [Table 4] . Clinical data were obtained through thorough neurological examination before treatment and during follow-up visits. Radiological follow-up included CT of the brain and digital subtraction angiography. Immediately after the procedure, digital subtraction angiography was performed to assess the degree of initial aneurysmal occlusion, which was classified as follows: (i) complete obliteration of the aneurysm, (ii) residual neck, defined as the persistence of any portion of the original defect of the arterial wall, (iii) residual aneurysm, defined as any opacification of the sac. The mean follow-up period after endovascular treatment was 3-6 months.
The endovascular procedure was commenced within 4-10 days from the onset of symptoms, whenever equipment and materials were available and suitable preparations were made.
The materials required were an angiography tray (prepacked), bowls, syringes, 4΄4 sterile sponges, towel clips, sharp holders, other accessories, and sterile covers for X-ray tube.
Fluid systems materials included a vascular sheath, a puncture system, guiding catheters, guidewires, microcatheters, and coils. The coils selected during treatment are operator-dependant. The selection is usually based on the shape and size of the aneurysm, determined before treatment using angiography.
Anesthesia and anticoagulants were appropriately administered.
Endosaccular embolization includes three steps: framing or caging, filling, and finishing.
The angiographic results were evaluated in the immediate postembolization angiographic projections. A qualitative assessment of the aneurysm occlusion was performed using a three-point Raymond scale. The aneurysm occlusion was considered a 'complete occlusion' when the aneurysm had dense packing and no contrast filling of the aneurysm sac or neck on multiple projections, it was considered a 'neck remnant' if there was residual filling of a part of the neck of the aneurysm, and it was considered a 'residual aneurysm' if there was continuing contrast filling of the dome or sac.
| Results|| |
Immediate angiographic results were considered to be satisfactory in seven patients (58.3%; complete obliteration). Five patients experienced some residual symptoms of their aneurysms (41.6%). Procedure-related mortality and morbidity was low. At 6 months, the outcomes were as follows: GOS score of 1, two patients (16.6%); GOS score of 2, seven patients (58.3%); GOS score of 3, three patients (25%); and GOS scores of 4 and 5, 0 patients (0%). Six-month angiographic follow-up data were available for 10 patients (83.3%).
The morphological results were considered to be satisfactory in most of these patients: complete occlusion was seen in seven patients (58.3%) [Figure 1] and residual or incomplete occlusion in three patients (25%); two patients (16.6%) underwent recoiling.
There was one anterior choroidal artery aneurysm, one supraclinoid artery aneurysm, four anterior communicating artery aneurysms, and six posterior communicating artery aneurysms.
These procedures could be performed without any complication in seven patients (58.3%). Coil migration during treatment did not occur in any of our patients. One patient (8.3%) suffered from symptomatic vasospasm, documented by angiography, for which intra-arterial papaverine was administered. Residual vasospasm remained and frontal manifestations were present after a period of disturbance of consciousness and residual hemiparesis.
Subsequent bleeding from the aneurysms after embolization occurred in two patients (16%). In five patients, occlusion of the aneurysmal sacs was incomplete; on initial morphological testing, the aneurysms were designated as 'residual aneurysms'. All three were posterior communicating aneurysms that were difficult to reach, either because of vessel tortuosity or vasospasm.
Immediate angiographic results were considered to be satisfactory in seven patients (58.3%; complete obliteration). Five patients experienced some residual symptoms of their aneurysms (41.6%). Morphological results were considered to be satisfactory in most of these patients. Complete occlusion was seen in seven patients (58.3%); residual or incomplete occlusion was seen in three patients (25%). Two patients (16.6%) underwent recoiling.
Recurrences, defined as any change in angiographic morphology, were observed in two patients 6 months after treatment. Angiography performed 6 months after treatment in all patients showed recurrences in two patients (16.6%). These patients were subsequently treated by coiling.
At 6 months, the outcomes were as follows: GOS score of 1, two patients (16.6%); GOS score of 2, seven patients (58.3%); GOS score of 3, three patients (25%); and GOS scores of 4 and 5, 0 patients (0%). Six-month angiographic follow-up data were available for 10 patients (83.3%).
| Discussion|| |
Our results may provide some indications of the efficacy of endovascular treatment, as well as an estimation of risks inherent to the technique. Endovascular series should theoretically not be compared with surgical series because indications differ for these approaches.
These procedures could be performed without any complication in seven patients (58.3%).
Intraprocedural aneurysm rupture occurred in four of the first 91 patients treated by Guglielmi and Viñuela . Iatrogenic bleeding was reported in 2.7% of patients treated acutely using guglielmi detachable coils (GDC) in a study conducted at eight centers, with the largest center being in the USA . The population of patients differed from that in our series in terms of sizes of aneurysms and timing of treatment.
Ischemic complications occurred in 5.52% of patients in the multicentric GDC study in the USA . In the present series, arterial occlusions were responsible for a long-term deficit in one patient (8.3% of patients). Catheter-related emboli were observed in none of our patients. These complications may be decreased by more aggressive use of anticoagulants during the procedures. A more conservative attitude during these procedures may prevent arterial occlusions by deliberate underpacking at the expense of a higher incidence of residual neck and recurrences. Delayed ischemic complications are probably related to clot formation on protrusion of loops of coils into the parent artery and may be decreased with the use of anticoagulants for 72h after embolization.
Arterial occlusions are readily detected during endovascular procedures, and immediate treatment can be administered. Intra-arterial urokinase led to thrombolysis of the clot in four patients and is a useful tool to minimize the clinical consequences of thromboembolic complications. Thrombolysis can usually be performed safely once the aneurysm is protected by coils because complications most often occur at the end of the procedure.
GDC is clearly a more controllable system with which to perform endovascular treatment, but inadvertent dislodgment of a previously detached coil can occur occasionally. Perforator vessels, particularly at the basilar tip, are more at risk with surgery than when an endovascular approach is used ,. Symptomatic thromboembolic complications during endovascular treatment were less frequent and more rarely related to unfavorable outcomes compared with those reported in some recently published surgical series ,,.
Coil migration during treatment did not occur in any of our patients.
It is believed that the incidence of vasospasm might reduce on evacuation of the clot and bloody cerebrospinal fluid at the time of surgical intervention, but clinical experience has not always supported this notion ,. Because patients treated using the endovascular route do not benefit from evacuation of blood, a higher incidence of significant vasospasm could be expected. The incidence of symptomatic delayed ischemia after subarachnoid hemorrhage has been reported to be ∼20-33% ,,, with resulting infarction, disability, or death in half of these patients. With early surgery and optimal medical management, including the use of calcium channel blockers, the morbidity and mortality rate from vasospasm has decreased to ∼4-12% ,,,,,,,. One patient (8.3%) suffered from symptomatic vasospasm, documented by angiography, for which intra-arterial papaverine was administered. Residual vasospasm remained and frontal manifestations were present after a period of disturbance of consciousness and residual hemiparesis. Although it is still too early to state whether spasm will be more prevalent with endovascular treatment, it did not cause a clear excess of poor results in our series.
Prevention of subsequent bleeding is the main goal of early treatment of aneurysms ,,,. Short-term subsequent bleeding has rarely been reported after treatment using GDC . Experimental studies have shown that partial obliteration of the aneurysm is insufficient to prevent subsequent bleeding . Subsequent bleeding from the aneurysms after embolization occurred in two patients (16%). In five patients, occlusion of the aneurysmal sacs was incomplete. On initial morphological evaluation, the aneurysms were designated as 'residual aneurysms'. All three were posterior communicating aneurysms that were difficult to reach, either because of vessel tortuosity or vasospasm. This problem may be overcome with improvements in catheter and guidewire design and with increased experience.
Endovascular treatment was as effective as surgery in preventing subsequent bleeding, provided the aneurysmal sac could be completely occluded.
Complete obliteration, dog ears, and residual necks were considered to be satisfactory results because they were not associated with subsequent bleeding in 84% of the patients. Patients with residual aneurysms are at risk of subsequent bleeding, as we have observed in two patients, and obliteration of the aneurysm should be attempted by a second endovascular procedure.
The follow-up was defective and further follow-up may be needed to show the effect of recoiling in these two patients.
In some large aneurysms with wide necks, even after the introduction of multiple coils, sluggish and stagnant opacifications may still be observed near the end of the procedure. If this minimal opacification is thought to persist artificially because of full heparinization, the procedure can be interrupted, and control angiography a few hours later may reveal thrombosis of the sac. If this is not the case, more coils should be added. We think that such a strategy can be adopted occasionally in large lesions, but with caution; however, it is dangerous for small aneurysms because the patient may not be protected from subsequent bleeding.
Residual necks after surgical clipping are not infrequent, but we think that they are more stable than they would be after endovascular treatment ,,,,,,,. Because of the nature of endovascular treatment, we suspect a residual neck or dog ear in virtually all cases, although they may not always be easy to demonstrate using angiography. Complete exclusion of the neck is probably possible only when the neck is narrow and short or when coils slightly protrude into the parent artery ,. Neck remnants are residual weaknesses on which new aneurysms may form within a few years ,,. Our follow-up period is too short to document the growth of new aneurysms, but midterm recurrences from coil compaction were observed in two patients. They were more often observed in aneurysms with wide necks but may also occur in lesions with narrow necks . These recurrences were not associated with new neurological events in any patient.
But the concern of future subsequent bleeding persists. Subsequent rupture during follow-up has been reported in 1.5-2% of patients . The age of the patient, the patient's medical condition, the site of the aneurysm, and the presence of sufficient space between the mass of coils and the parent artery are factors that will influence the decision as regards the recoiling technique ,.
Recurrences, defined as any change in angiographic morphology, were observed in two patients 6 months after treatment. Angiography performed 6 months after treatment in all patients showed recurrences in two patients (16.6%), which were subsequently treated by coiling.
Further, medical complications, which have been said to be responsible for 23% of deaths in a multicentric trial , may be decreased with less invasive treatment in certain patients. Finally, if endovascular treatment is proven to improve outcome at 6 months, it will be at the expense of a number of suboptimal angiographic results with persisting concerns of late subsequent bleeding from regrowth of aneurysms. During a mean follow-up of 31 months, subsequent treatment using GDC or surgery was judged necessary in 11 patients (15% of all patients), but subsequent bleeding did not occur in any of these patients. The long-term risks involved with residual necks after endovascular treatment is currently not known ,,. We speculate that the risk of subsequent bleeding in patients with residual necks 6 months after endovascular treatment will be no higher, and probably lesser, than the risks of subsequent bleeding of unclipped aneurysms after 6 months. Subsequent rupture has been noted in 1.5% of patients treated using GDC in one series . Late subsequent bleeding after surgical clipping is also possible, with an estimated incidence between 0.3 and 0.9% per year ,.
Immediate angiographic results were considered to be satisfactory in seven patients (58.3%; complete obliteration). Five patients experienced some residual symptoms of their aneurysms (41.6%). The morphological results were considered to be satisfactory in most of these patients: complete occlusion in seven patients (58.3%) and residual or incomplete occlusion in three patients (25%); two patients (16.6%) underwent recoiling.
The criteria for selection of patients for endovascular treatment may vary from one center to another. Characteristics of patients or lesions may influence outcome in such a way that it may be impossible to draw meaningful conclusions by comparing surgical and endovascular series. Criteria for endovascular treatment could be defined more scientifically after a randomized study than on the basis of empirical opinions based on individual experiences .
| Conclusion|| |
Endovascular treatment of ruptured aneurysms was attempted without clinically significant complication in most of the patients. Complete obliteration of the sac, with or without residual neck, is essential to prevent subsequent bleeding. The overall outcome at 6 months was satisfactory, despite a selected group of patients having residual complications or residual aneurysms.
Considering that this is a new therapeutic approach, we think that the results will improve in future series. The clinical outcome after endovascular treatment is encouraging, but research should focus on improvement of long-term angiographic results. A randomized study comparing endovascular treatment with surgery may be the most scientific way to better define the role of this new therapeutic approach in the management of acutely ruptured aneurysms. In our opinion, the uncertainty related to long-term angiographic results is acceptable when trying to improve the immediate outcomes for many patients [Figure 2],[Figure 3] and [Figure 4].
| Acknowledgements|| |
Conflicts of interest
There are no conflicts of interest.
| References|| |
|1.||Schonfeld AR, Mcmullen MA. Treatment of brain aneurysms. Radiol Technol 2008; 6:515-532. |
|2.|| Brisman JL, Song JK, Newell DW. Cerebral aneurysms. N Engl J Med 2006; 355:928-939. |
|3.|| Harrigan MR, Howington JU, Hanel RA. The neuroform stent, the first microcatheter delivered stent for use in the intracranial circulation. Neurosurgery 2004; 54:2-17. |
|4.|| Hunt WE, Hess RM. Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg 1968; 28:14-20. |
|5.|| Jennett B, Bond M. Assessment of outcome after severe brain damage. Lancet 1975; 1:480-484. |
|6.|| Fisher CM, Kistler JP, Davis JM. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by CT scanning. Neurosurgery 1980; 6:1-9. |
|7.|| Lindley RI, Waddell F, Livingstone M. Can simple questions assess outcomes after stroke? Cerebrovasc Dis 1994; 4:314-324. |
|8.|| Guglielmi G, Viñuela F. Intracranial aneurysms: guglielmi electrothrombotic coils. Neurosurg Clin N Am 1994; 5:427-435. |
|9.|| Duckwiler G, Guglielmi G, Viñuela F. Guglielmi detachable coil (GDC) embolization in acutely ruptured intracranial aneurysms: perioperative anatomic and clinical outcome in four hundred three patients. Presented at the 34th Annual Meeting of the American Society of Neuroradiology. Seattle, Washington: AM. J Neuroradiol 1996. |
|10.||1McDougall CG, Halbach VV, Dowd CF. Endovascular treatment of basilar tip aneurysms using electrolytically detachable coils. J Neurosurg 1996; 84:393-399. |
|11.||1Raymond J, Roy D, Bojanowski M. Endovascular treatment of acutely ruptured and unruptured aneurysms of the basilar bifurcation. J Neurosurg 1997; 86:211-219. |
|12.||1Le Roux PD, Elliott JP, Downey L. Improved outcome after rupture of anterior circulation aneurysms: a retrospective 10-year review of 224 good-grade patients. J Neurosurg 1995; 83:394-402. |
|13.||1Proust F, Hannequin D, Langlois O. Causes of morbidity and mortality after ruptured aneurysm surgery in a series of 230 patients: the importance of control angiography. Stroke 1995; 26:1553-1557. |
|14.||1Säveland H, Brandt L. Which are the major determinants for outcome in aneurysmal subarachnoid hemorrhage? A prospective total management study from a strictly unselected series. Acta Neurol Scand 1994; 90:245-250. |
|15.||1Kassell NF, Torner JC, Jane JA. The international cooperative study on the timing of aneurysm surgery: part 2 - surgical results. J Neurosurg 1990; 73:37-47. |
|16.||1Peerless SJ, Hernesniemi JA, Gutman FB. Early surgery for ruptured vertebrobasilar aneurysms. J Neurosurg 1994; 80:643-649. |
|17.||1Kassell NF, Torner JC, Haley EC. The international cooperative study on the timing of aneurysm surgery: part 1 - overall management results. J Neurosurg 1990; 73:18-36. |
|18.||1Macdonald RL, Wallace MC, Coyne TJ. The effect of surgery on the severity of vasospasm. J Neurosurg 1994; 80:433-439. |
|19.||1Findlay JM, Kassell NF, Weir BKA. A randomized trial of intraoperative, intracisternal tissue plasminogen activator for the prevention of vasospasm. Neurosurgery 1995; 37:168-178. |
|20.||2Fridriksson SM, Hillman J, Saveland H. Intracranial aneurysm surgery in the 8th and 9th decades of life: Impact on population-based management outcome. Neurosurgery 1995; 37:627-632. |
|21.||2Inagawa T. Cerebral vasospasm in elderly patients treated by early operation for ruptured intracranial aneurysms. Acta Neurochir (Wien) 1992; 115:79-85. |
|22.||2Origitano TC, Wascher TM, Reichman OH. Sustained increased cerebral blood flow with prophylactic hypertensive hypervolemic hemodilution ("Triple-H" therapy) after subarachnoid hemorrhage. Neurosurgery 1990; 27:729-740. |
|23.||2Seiler RW, Reulen HJ, Huber P. Outcome of aneurysmal subarachnoid hemorrhage in a hospital population: a prospective study including early operation, intravenous nimodipine and transcranial doppler ultrasound. Neurosurgery 1988; 23:598-604. |
|24.||2Miyaoka M, Sato K, Ishii S. A clinical study of the relationship of timing to outcome of surgery for ruptured cerebral aneurysms: a retrospective analysis of 1622 cases. J Neurosurg 1993; 79:373-378. |
|25.||2Graves VB, Strother CM, Duff TA. Early treatment of ruptured aneurysms with Guglielmi detachable coils: effect on subsequent bleeding. Neurosurgery 1995; 37:640-648. |
|26.||2Byrne JV, Hubbard N, Morris JH. Endovascular coil occlusion of experimental aneurysms: partial treatment does not prevent subsequent rupture. Neurol Res 1994; 16:425-427. |
|27.||2Derdeyn CP, Moran CJ, Cross DT. Intraoperative digital subtraction angiography: a review of 112 consecutive examinations. AJNR Am J Neuroradiol 1995; 16:307-318. |
|28.||2Drake CG, Friedman AH, Peerless SJ. Failed aneurysm surgery: reoperation in 115 cases. J Neurosurg 1984; 61:848-856. |
|29.||2Feuerberg I, Lindquist C, Lindquist M. Natural history of post-operative aneurysm rests. J Neurosurg 1987; 66:30-34. |
|30.||3Fujiwara S, Fujii K, Nishio S. Long term results of wrapping of intracranial ruptured aneurysms. Acta Neurochir (Wien) 1990; 103:27-29. |
|31.||3Lin T, Fox AJ, Drake CG. Regrowth of aneurysm sacs from residual neck following aneurysm clipping. J Neurosurg 1989; 70:556-560. |
|32.||3Macdonald RL, Wallace C, Kestle JRW. Role of angiography following aneurysm surgery. J Neurosurg 1993; 79:826-832. |
|33.||3Fernandez-Zubillaga AF, Guglielmi G, Viñuela F. Endovascular occlusion of intracranial aneurysms with electrically detachable coils: correlation of aneurysm neck size and treatment results. AJNR Am J Neuroradiol 1994; 15:815-820. |
|34.||3Byrne J, Bacon F, Higgins N. Coil embolization of intracranial aneurysms: Follow-up results. Presented at the 34th Annual Meeting of the American Society of Neuroradiology. Seattle, Washington: AM. J Neuroradiol 1996. |
|35.||3Civit T, Auque J, Marchal JC. Aneurysm clipping after endovascular treatment with coils: a report of eight patients. Neurosurgery 1996; 38:955-961. |
|36.||3Gurian JH, Guglielmi G, Viñuela F. Neurosurgical management of cerebral aneurysms following unsuccessful or incomplete endovascular embolization. J Neurosurg 1995; 83:843-853. |
|37.||3Solenski NJ, Haley EC, Kassell NF. Medical complications of aneurysmal subarachnoid hemorrage: a report of the multicenter, cooperative aneurysm study. Crit Care Med 1995; 23:1007-1017. |
|38.||3Todd NV, Tocher JL, Jones PA. Outcome following aneurysm wrapping: a 10-year follow-up review of clipped and wrapped aneurysms. J Neurosurg 1989; 70:841-846. |
|39.||3Winn HR, Almaani WS, Berga SL. Incidence of late hemorrhage and implications for treatment of incidental aneurysms: the long-term outcome in patients with multiple aneurysms. J Neurosurg 1983; 59:642-651. |
|40.||4Sugita K, Kobayashi S, Shintani A. Microneurosurgery for aneurysms of the basilar artery. J Neurosurg 1979; 51:615-620. |
|41.||4Sundt TM Jr, Whisnant JP. Subarachnoid hemorrhage from intracranial aneurysms: surgical management and natural history of disease. N Engl J Med 1987; 299:116-122. |
|42.||4Nichols DA. Endovascular treatment of the acutely ruptured intracranial aneurysms. J Neurosurg 1993; 79:1-2. |
[Figure 1], [Figure 2], [Figure 3], [Figure 4]
[Table 1], [Table 2], [Table 3], [Table 4]