Subject Review. Endovascular Treatment of Intracranial Aneurysms

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1 Subject Review Endovascular Treatment of Intracranial Aneurysms DOUGLAS A. NICHOLS, M.D., FREDRIC B. MEYER, M.D., DAVID G. PIEPGRAS, M.D., AND PATSY L. SMITH, R.N. Objective: To examine the techniques, reported experiences, and advantages and disadvantages associated with the endovascular treatment of intracranial aneurysms. Design: We review the endovascular techniques used for the treatment of intracranial aneurysms and the sequelae of subarachnoid hemorrhage, which have evolved during the past 10 years. Material and Methods: Two broad categories of endovascular therapy for intracranial aneurysms are described: occlusion of the parent artery and preservation of the parent artery by selective occlusion of the aneurysm with balloons or metallic coils. The Mayo protocol for testing tolerance of patients before permanent balloon occlusion of the parent artery is described, as are the types of aneurysms most amenable to this treatment. In addition, use of balloon angioplasty for cerebral vasospasm after subarachnoid hemorrhage is reviewed. Results: Recent improvements in microcatheter technology have facilitated the safe navigation of per- cutaneously introduced catheters in the intracranial circulation and selective catheterization of intracranial aneurysms. Surgically difficult aneurysms are now being treated with endovascular techniques more frequently than in the past. Early results from animal experiments and human trials have shown that selective occlusion of aneurysms with metallic coils may have a role in the treatment of intracranial aneurysms. Balloon angioplasty of symptomatic cerebral vasospasm has demonstrated improvement in neurologic function in approximately 70% of patients. Conclusion: As technology continues to improve and as greater experience is obtained, interventional neuroradiologists will continue to have an increasingly important role in the treatment of intracranial aneurysms. (Mayo Clin Proc 1994; 69: ) CT = computed tomography; HMPAO = hexamethylpropyleneamine oxime; SPECT = single photon emission computed tomography Intracranial aneurysms are a major cause of neurovascularrelated morbidity and mortality in.adults. In autopsy series, the frequency of intracranial aneurysms in adults has been reported to be between 2 and 7.6%.13 In the general population, the incidence of subarachnoid hemorrhage because of rupture of an aneurysm is approximately 10 per 100,000 annually4 and progressively increases with advancing age. Rupture of an aneurysm that results in subarachnoid hemorrhage is devastating; 90 days after subarachnoid hemorrhage, the rate of favorable outcome is less than 50%, the mortality rate is 36%, and the rate of serious morbidity is 18%.5 Because of their mass effect on vital structures at the base of the brain, unruptured aneurysms may also cause serious problems, such as hydrocephalus, cranial nerve palsies, paralysis, and coma. From the Department of Diagnostic Radiology (D.A.N., P.L.S.) and Department of Neurologic Surgery (F.B.M., D.G.P.), Mayo Clinic Rochester, Rochester, Minnesota. Address reprint requests to Dr. D. A. Nichols, Department of Diagnostic Radiology, Mayo Clinic Rochester, 200 First Street SW, Rochester, MN The mainstay of treatment of intracranial aneurysms is neurosurgical clipping of the neck of the aneurysm. In a subset of patients with aneurysms, however, surgical clipping may be associated with a high risk because of the site or size of the aneurysm, the presence of a wide or calcified aneurysmal neck, or the poor condition of the patient attributable to severe subarachnoid hemorrhage or other medical problems. For this subset of patients, endovascular treatment is used. During the 1970s, a Russian neurosurgeon, Fjordor A. Serbinenko, pioneered the development of endovascular techniques by using balloons for intracranial aneurysms.6 7 Since that time, numerous other European, Asian, and North American investigators have also reported their experiences.813 Endovascular therapy for intracranial aneurysms can be classified into two broad categories: (1) occlusion of the parent artery and (2) preservation of the parent artery by selective occlusion of the aneurysm with detachable balloons or metallic coils. The method of treatment primarily depends on the site, size, and morphologic features of the aneurysm. The various methods of treatment, indications, Mayo Clin Proc 1994; 69: Mayo Foundation for Medical Education and Research

2 Mayo Clin Proc, March 1994, Vol 69 ENDOVASCULAR TREATMENT OF INTRACRANIAL ANEURYSMS 273 advantages and disadvantages, and reported results are discussed herein. BALLOON OCCLUSION OF THE PARENT ARTERY Often, in patients with aneurysms at increased risk for complications of surgical clipping, the aneurysm can be occluded with endovascular techniques, and the parent vessel can be preserved. Some aneurysms with wide necks and ectatic and fusiform aneurysms are unamenable to selective occlusion and are treated with detachable-balloon occlusion of the parent vessel. 813 Before the parent vessel (either the cervical internal carotid artery or the vertebral artery) that is harboring an aneurysm is permanently occluded, it is temporarily occluded with a double-lumen balloon catheter to test the patient's tolerance to occlusion. Protocols for testing tolerance before permanent balloon occlusion of the internal carotid or vertebral artery vary from institution to institution. The subsequent material describes how the procedure is currently performed at the Mayo Clinic (Fig. 1). All procedures are performed in the interventional neuroradiology angiography suite. With use of neuroleptic analgesia (intravenously administered fentanyl citrate and midazolam), arterial sheaths are placed in both femoral arteries of the patient. A complete cerebral angiogram is obtained, and additional oblique views of the aneurysm to be treated are obtained to define the anatomy adequately. A baseline activated clotting time is determined, and the patient receives 4,000 to 5,000 U of intravenously administered heparin. The rate of metabolism and excretion of heparin is dose-dependent 14 and varies from patient to patient. We obtain serial activated clotting times at half-hour intervals, and additional heparin is given when necessary to maintain adequate anticoagulation throughout the duration of the procedure. After the patient receives systemic anticoagulant therapy, we prefer to keep the activated clotting time at 2 times the baseline level. A 5.0- or 7.0-F double-lumen balloon catheter is placed in the cervical segment of the internal carotid or vertebral artery and slowly inflated until the artery is occluded. Occlusion is maintained for 30 minutes, during which time the patient is closely monitored for any change in neurologic function. The collateral circulation through the circle of Willis to the vascular territory to be occluded is assessed during the period of balloon occlusion by obtaining digital subtraction angiograms of the contralateral carotid artery, the ipsilateral external carotid artery, and the dominant vertebral artery (when the internal carotid artery is occluded) or the contralateral vertebral artery and both internal carotid arteries (when the vertebral artery is occluded). Because angiographically demonstrated collateral circulation to a vascular territory is an inexact measure of cerebral perfusion, xenon cerebral blood flow studies are routinely performed. "Tc-hexamethylpropyleneamine oxime ( 99m Tc- HMPAO) is injected intravenously for delayed cerebral perfusion single photon emission computed tomography (SPECT) during balloon occlusion of an internal carotid artery. A baseline xenon cerebral blood flow study is done before temporary balloon occlusion. The xenon, 400 μθ, is injected through the distal lumen of the double-lumen balloon catheter. Washout of the injected xenon is measured by an external probe placed over the ipsilateral frontoparietal region, and cerebral blood flow (in milliliters per 100 g of brain tissue per minute) is computed. Xenon is again injected, and the balloon is inflated immediately. During occlusion of the internal carotid artery, washout of the injected xenon is again measured, and cerebral blood flow is computed. In general, in an awake, sedated patient, measurements of the cerebral blood flow before occlusion range from 35 to 50 ml/100 g of brain tissue per minute. In cases being considered for permanent occlusion of the internal carotid artery, we prefer that the blood flow during temporary occlusion be at least two-thirds the baseline flow or more than 25 ml/100 g of brain tissue per minute. After the xenon cerebral blood flow study has been completed, 20 mci of "Tc-HMPAO is injected intravenously, and a cerebral perfusion SPECT scan is obtained after the patient leaves the angiography suite. Xenon measurements of cerebral blood flow and SPECT imaging are suboptimal for evaluating perfusion in the posterior fossa, and these tests have not been performed during trial balloon occlusion of a vertebral artery. Preliminary experience at the Mayo Clinic and elsewhere 1517 suggests that SPECT imaging is a sensitive indicator for the presence of cerebral hypoperfusion. SPECT imaging is only semiquantitative and usually reveals flow patterns that correspond to one of three categories: symmetric perfusion, slightly abnormal asymmetric perfusion, or unequivocally abnormal asymmetric perfusion. Patients who tolerate temporary balloon occlusion and have symmetric or slightly abnormal asymmetric perfusion have a low risk for subsequent stroke after occlusion of the parent artery. 17 Insufficient data are available to know the risk of stroke for those patients who tolerate temporary balloon occlusion but have unequivocally abnormal asymmetric perfusion on subsequent SPECT imaging. Investigators have suggested that SPECT imaging may be too sensitive and that patients who could potentially tolerate occlusion of the carotid artery may be denied this therapeutic alternative because of abnormal findings on SPECT imaging; therefore, a more quantitative measure of cerebral blood flow such as stable xenon-computed tomography (CT) has been advocated in conjunction with the temporary balloon occlusion

3 274 ENDOVASCULAR TREATMENT OF INTRACRANIAL ANEURYSMS Mayo Clin Proc, March 1994, Vol 69 Fig. 1. Angiograms of 14-year-old boy with palsy of left cranial nerve VI due to 2.5-cm aneurysm of cavernous segment of left internal carotid artery. Lateral (A) and Towne (ß) views of left common carotid artery, demonstrating aneurysm. C, Digital subtraction angiogram. Towne view of right common carotid artery obtained during temporary balloon occlusion of left internal carotid artery, demonstrating good collateral opacification of left carotid intracranial circulation through patent anterior communicating artery. D, Digital subtraction angiogram. Towne view of left vertebral artery also obtained during temporary balloon occlusion of left internal carotid artery, demonstrating good collateral opacification of left middle cerebral circulation through patent left posterior communicating artery. test.18 This procedure, however, necessitates transportation of the patient from the angiography suite to the CT scanning area with an indwelling double-lumen balloon catheter in the internal carotid artery and inflating and deflating the balloon in a blind fashion. This method has some associated risk, including the possibility of a carotid dissection.19 In addition, many radiology departments do not have the accessory equipment necessary to perform stable xenon-ct cerebral blood flow imaging. No studies have compared the sensitivity and specificity of stable xenon-ct cerebral blood flow imaging and "mtc-hmpao cerebral perfusion SPECT imaging. We do not have extensive experience with use of an acetazolamide challenge test20 or pharmacologically induced hypotension during temporary balloon occlusion of the carotid artery for predicting which patients will or will not tolerate permanent balloon occlusion of the carotid artery. We prefer to review the results of the SPECT scan before proceeding with permanent balloon occlusion of the parent artery. Although this method necessitates a second catheterization procedure, the additional time and expense involved are worth the information received from the SPECT examination. If the patient does not clinically tolerate temporary balloon occlusion of the parent artery or if the xenon cerebral blood flow studies or the cerebral perfusion SPECT scans strongly suggest cerebral hypoperfusion (even though the patient clinically tolerated temporary balloon occlusion), we

4 Mayo Clin Proc, March 1994, Vol 69 ENDOVASCULAR TREATMENT OF INTRACRANIAL ANEURYSMS 275 augment cerebral circulation with an extracranial-to-intracranial bypass procedure before permanent occlusion of the parent artery (either by balloon or by surgical ligation). Despite the sophisticated functional testing just described, the temporary balloon occlusion test is not 100% predictive of tolerance to permanent balloon occlusion of the parent artery. Higashida and associates" reported that among 68 patients, 7 (10.3%) had transient cerebral ischemia that responded to volume expansion or antiplatelet therapy and 3 (4.4%) had stroke after permanent balloon occlusion of the internal carotid artery. Delayed stroke may occur after permanent balloon occlusion of a vertebral or internal carotid artery because of two mechanisms. 21 Hypoperfusion due to inadequate collateral flow or transient hypotension may result in a hemodynamic stroke. Transient hypotension is particularly a problem in elderly patients. Propagated thromboembolism from the parent artery distal to the occluding balloon or from the aneurysm itself may also result in a stroke despite adequate collateral flow. Temporary anticoagulant therapy is of value in decreasing this risk although such treatment may be undesirable, especially in cases in which aneurysmal hemorrhage has occurred. Several delivery catheter and detachable-balloon configurations are available, 2227 the pros and cons of which are beyond the scope this article. In general, balloons can be mounted on delivery catheters that range from 1 to 3 F in diameter and can be detached either by simple traction or by being "pushed" off the delivery catheter with a coaxial catheter. Detachable balloons are available in various sizes and configurations and are made of either latex or silicone. The detachable balloon attached to the catheter is positioned in the parent artery just proximal to or across the neck of the aneurysm. Appropriate positioning of the balloon within the artery is usually not technically difficult because the balloon will be directed by blood flow or curves can be formed on the delivery catheter to assist with navigation of the balloon. The balloon is inflated with either a 50:50 mixture of sterile water and iopamidol 61% (Squibb, New Brunswick, New Jersey) or 200 mg/dl of metrizamide (Winthrop, New York, New York). Because both solutions are radiopaque and isosmotic to blood, the balloon will not enlarge further nor contract after detachment as a result of osmosis across the balloon wall. The balloon is detached, and a second "safety" balloon is immediately detached just proximal to the initial balloon in order to prevent distal migration and embolization of the initially detached balloon should it deflate prematurely (Fig. 2). All balloons filled with nonsolidifying liquids will slowly deflate during a period of weeks to months. In the case of aneurysms treated by occlusion of the parent artery, this deflation is not a problem because arterial and aneurysmal thrombosis will have occurred by the time the balloon has deflated. Among the aneurysms that involve the carotid circulation, which are successfully treated only by permanent balloon occlusion of the internal carotid artery and are considered unamenable to surgical clipping, are fusiform or wide-necked aneurysms that affect the cavernous segment of the internal carotid artery or the paraclinoid internal carotid artery proximal to the origin of the ophthalmic artery. As previously mentioned, Higashida and colleagues" reported the largest North American series of 68 patients with aneurysms of the cavernous carotid artery treated by permanent balloon occlusion of the internal carotid artery across or just proximal to the neck of the aneurysm. They described symptoms attributable to transient cerebral ischemia in seven patients and permanent morbidity in three as a result of stroke after balloon occlusion of the internal carotid artery. All patients treated by balloon occlusion of the internal carotid artery had aneurysmal thrombosis. Fox and coworkers 10 described 37 patients with aneurysms of the cavernous or the paraclinoid internal carotid artery proximal to the origin of the ophthalmic artery that could not be treated by clipping, and thus they underwent balloon occlusion of the internal carotid artery. Three patients had transient ischemie complications, and two had transient worsening of cranial nerve palsies. No permanent complications occurred in their series, and all aneurysms demonstrated complete thrombosis. The results of permanent balloon occlusion of the internal carotid artery for treatment of unclippable aneurysms of the cavernous carotid artery compare favorably with surgical series 28 in which the common carotid or cervical internal carotid artery was ligated with various clamps. Detachableballoon occlusion has several advantages in comparison with surgical ligation of the internal carotid artery. Because it is performed with use of local anesthesia, the patient is awake during the procedure, and neurologic monitoring can be easily performed during test occlusion. In addition, because the balloon is detached at or just proximal to the neck of the aneurysm, the possibility of refilling of the aneurysm by means of collaterals from the external carotid artery to the cavernous internal carotid artery is decreased. The risk of embolie complications is believed to be less if the arterial occlusion is distal, close to the neck of the aneurysm rather than in the cervical internal or common carotid artery. 29 This theory, however, has not been substantiated by controlled clinical trials. Finally, because balloon occlusion is performed transfemorally, systemic anticoagulant therapy can be used during and after the procedure to decrease the chance of embolie complications. Because of the limitations of the anatomy of the vertebralbasilar intracranial circulation, permanent balloon occlusion

5 276 ENDOVASCULAR TREATMENT OF INTRACRANIAL ANEURYSMS Mayo Clin Proc, March 1994, Vol 69 Fig. 2. Radiographie studies of same patient described in Figure 1. Lateral (A) and Towne (B) radiographs, demonstrating contrast-filled detached No. 17 latex Debrun balloons (black arrows) in proximal cavernous and petrous segments of left internal carotid artery. Note stagnant contrast medium in cavernous carotid aneurysm (curved white arrows). At 6 weeks after balloon occlusion, spin-densityweighted axial magnetic resonance imaging scan (C), demonstrating complete thrombosis of aneurysm (arrow). At 18 months after balloon occlusion, spin-density-weighted axial magnetic resonance imaging scan (D), demonstrating substantial decrease in size of thrombosed aneurysm so that it is no longer apparent. Patient's palsy of left cranial nerve VI had completely resolved at 18-month followup clinical examination. of one or both vertebral arteries for the treatment of intracranial vertebral or basilar artery aneurysms unamenable to direct surgical clipping or selective occlusion by endovascular techniques is a riskier procedure and performed less frequently than is balloon occlusion of the internal carotid artery The difficulty and risks associated with occlusion of the parent artery for aneurysms of the posterior circulation primarily depend on the site and morphologic features of the aneurysm. For example, unclippable aneurysms of the intracranial vertebral artery proximal to the origin of the posterior inferior cerebellar artery can be treated relatively easily by detaching a balloon just proximal to the neck of the aneurysm if adequate vertebral-basilar collateral circulation is present. Fusiform aneurysms that involve the basilar artery trunk are often partially thrombosed and are difficult to treat. These aneurysms have been treated by balloon occlusion of one or both vertebral arteries after demonstration of tolerance to temporary balloon occlusion and angiographie evidence of collateral supply to the basilar artery through the posterior communicating arteries. Brain stem infarction, however, can occur as a result of occlusion of perforating vessels off the basilar artery as thrombosis of the aneurysmal segment occurs. The advantages of balloon occlusion of the parent artery over surgical ligation of the internal carotid artery for aneurysms of the carotid circulation also apply to aneurysms of

6 Mayo Clin Proc, March 1994, Vol 69 ENDOVASCULAR TREATMENT OF INTRACRANIAL ANEURYSMS 277 the vertebral-basilar circulation. The results and long-term outcome of aneurysms of the posterior circulation treated by balloon occlusion of the parent artery 13 cannot be validly compared with the results of surgical ligation 31 because of the small numbers in reported series and the wide variation in site and complexity of the aneurysms treated. SELECTIVE OCCLUSION OF ANEURYSMS Detachable Balloons. Endovascular treatment of intracranial aneurysms was initially limited to balloon occlusion of the parent artery. Advancements in balloon and catheter technology, digital subtraction angiography, fluoroscopy with road-mapping capabilities, and liquid solidifying agents for balloons have allowed treatment of aneurysms with welldefined necks by selective positioning of detachable balloons within the aneurysmal sac in an attempt to induce permanent thrombosis of the sac and preserve the parent artery (Fig. 3) ' 34 During the procedure, the patient receives systemic anticoagulant therapy, and digital subtraction angiography and fluoroscopic road-mapping guidance are used to navigate the catheter-balloon system into the aneurysm to be treated. The distal catheter can have special curves formed on it to assist during navigation through the cerebral vasculature. The balloon is slowly inflated within the aneurysm. Extreme care is taken to avoid overinflation of the balloon, which may result in rupture of the aneurysm. For thrombosis and occlusion of large aneurysms, two or more balloons may be needed to fill the lumen of the aneurysm adequately. Shcheglov 34 described 617 patients with intracranial aneurysms whose initial manifestation was acute or subacute subarachnoid hemorrhage that was treated with detachable balloons. In 91% of the patients, the aneurysm was occluded, and the parent artery was left patent; in 9%, the parent artery was occluded. The mortality rate was 1.7% among 338 patients who were in "fair" condition at treatment and 22.0% among 71 patients who were in "poor" condition. This series was from the Kiev Research Institute of Neurosurgery, where treatment of intracranial aneurysms with detachable balloons is preferred over neurosurgical clipping. In a report by Higashida and associates, patients with intracranial aneurysms were treated with detachable balloons, and the parent artery was preserved. This series consisted of a high-risk group of patients who had already undergone unsuccessful neurosurgical clipping or who had aneurysms considered high risk for complications of neurosurgical clipping because of their size or site or the poor medical condition of the patient. At initial examination, 54% of the patients had symptoms attributable to mass effect, 37% had subarachnoid hemorrhage, and the rest had other symptoms, including transient ischemie attacks due to emboli, pseudoaneurysm caused by trauma, or carotid-cavernous fistula resulting from a ruptured intracavernous carotid aneurysm. The aneurysm was occluded in 65 patients (77.4%), and subtotal occlusion of more than 85% of the volume of the aneurysm was obtained in 19 patients (22.6%). Permanent morbidity and mortality were high 9 cases of stroke (10.7%) and 15 deaths (17.9%). These morbidity and mortality rates can be at least partly attributed to the high-risk group of patients in whom safe surgical alternatives were unavailable. Treating intracranial aneurysms with detachable balloons has several disadvantages that have prevented this method from becoming widely accepted and viable. As previously stated, all balloons filled with contrast material will eventually deflate. Often, a balloon detached within an aneurysm deflates slowly enough to maintain thrombosis of the aneurysm. Occasionally, however, the aneurysm will recanalize after the balloon deflates. Therefore, recanalization of an aneurysm as a result of balloon deflation is usually avoided by exchanging the contrast material within the balloon for a liquid solidifying agent before detachment of the balloon. The process of deflating and reinflating a balloon inside an aneurysm has associated risks. Hydroxyethylmethacrylate is the most commonly used solidifying agent Although balloons are available in a limited variety of sizes and shapes (spherical or cylindrical), finding a particular balloon or a combination of balloons that will not only fill 100% of the volume of the aneurysm but also obliterate the neck of the aneurysm is difficult. Several published reports describe delayed rupture of the aneurysm after subtotal occlusion A "water-hammer effect" from pulsating arterial blood on the balloon, which is transmitted to the wall of the aneurysm, is postulated to be the cause of delayed rupture or enlargement of the aneurysm after subtotal balloon occlusion. 39 Balloons may also migrate into the thrombus of a partially thrombosed aneurysm and cause refilling of the aneurysm. Because the balloon exerts pressure on the wall of the aneurysm during the inflation process, most investigators have been reluctant to treat aneurysms during the acute phase (first 72 hours) after subarachnoid hemorrhage. Obliteration of aneurysms during the acute phase after subarachnoid hemorrhage can improve clinical results by decreasing the frequency of rehemorrhage and by facilitating aggressive treatment of delayed ischemie deficit attributed to vasospasm, if it occurs. 40 For all the reasons previously stated, the practice of selective occlusion of aneurysms with detachable balloons has been essentially abandoned. Metallic Coils. Because of the difficulties associated with detachable balloon therapy for intracranial aneurysms, recent work has focused on finding other occlusive agents that can be placed inside an aneurysm endovascularly that will occlude the aneurysm and preserve the parent artery. Early results from animal experiments and human trials have

7 278 ENDOVASCULAR TREATMENT OF INTRACRANIAL ANEURYSMS Mayo Clin Proc, March 1994, Vol 69 Fig. 3. Radiographie studies of 70-year-old woman with history of increasing confusion, ataxia, and left hemiparesis. A, Proton-densityweighted axial magnetic resonance imaging scan, demonstrating 4-cm, partially thrombosed aneurysm with associated mass effect resulting in obstructive hydrocephalus. B, Lateral angiogram of right carotid artery, demonstrating that aneurysm (arrow) arises from origin of posterior communicating artery. Note that most of aneurysm is thrombosed and remaining patent portion is approximately 1 cm in maximal diameter. C, Angiogram of left carotid artery obtained immediately after successful detachment of No. 19 latex Debrun balloon filled with hydroxyethylmethacrylate (arrowheads) within aneurysm. D, Computed tomographic scan of head obtained after treatment, demonstrating detached balloon (arrow) within aneurysm. Note relationship of size of balloon to overall size of thrombosed aneurysm. shown that selective occlusion of aneurysms with metallic coils may have a major role in the treatment of intracranial aneurysms.4'49 Applying coil technology to the treatment of intracranial aneurysms was limited initially because of the inability to deposit coils consistently in the desired sites. A coil was placed in the delivery catheter and then pushed out the distal end by a pusher guidewire. If the coil did not assume an appropriate position within the aneurysm or if it migrated into the parent vessel, it could not be retrieved endovascularly without considerable technical difficulty. A major advancement in the endovascular treatment of intracranial aneurysms occurred with the development of a "detachable" coil system. Guglielmi and associates46 developed the Guglielmi detachable coil, which facilitates the controlled delivery of soft platinum coils within intracranial aneurysms. The system works on the principles of electrolysis and electrothrombosis (Fig. 4 and 5).

8 Mayo Clin Proc, March 1994, Vol69 ENDOVASCULAR TREATMENT OF INTRACRANIAL ANEURYSMS 279 Fig. 4. Diagram of Guglielmi detachable platinum coil. A, Helical diameter of coil. B, Length of coil. C, Microsolder connecting distal stainless steel wire to platinum coil. D, Uninsulated segment of distal stainless steel wire. E, Proximal Teflon-insulated stainless steel wire. Briefly, a platinum coil is attached to a stainless steel guidewire with a microsolder. The platinum coils are available in various helical diameters and lengths. A Tracker-10 or Tracker-18 microcatheter (Target Therapeutics, Inc., Fre- mont, California) is introduced into the intracranial circulation and, under fluoroscopic road-mapping and digital subtraction angiographie guidance, the tip of the microcatheter is navigated into the lumen of the aneurysm. When the platinum coil is in the microcatheter, it becomes straight; when it exits the microcatheter, it becomes circular, folds on itself, and conforms to the shape of the aneurysm. If the coil assumes an unsatisfactory position as it exits the microcatheter, it can be withdrawn into the microcatheter by simple retraction of the proximal end of the guidewire. The coil can be advanced and withdrawn repeatedly until it assumes a satisfactory position within the aneurysm. The platinum coil is then detached from the stainless steel guidewire by the process of electrolysis. A 2.5-V, 1.0-mA direct electric current is applied to the proximal end of the guidewire. A negative ground needle is placed in the subcutaneous soft tissues of the patient. The stainless steel guidewire is insulated with Teflon, except for a short portion just proximal to the platinum coil. The current dissolves the Fig. 5. Occlusion of aneurysm with Guglielmi detachable coil. A, Aneurysm of basilar artery before treatment. B, Microcatheter has been placed inside aneurysm, andfirstcoil has been delivered inside aneurysm but not yet detached. Arrow depicts junction between guidewire and coil. C, Coil has been detached, and guidewire has been withdrawn proximally into microcatheter (arrow). D, Appearance of aneurysm after completion of treatment. Aneurysm isfilledand excluded from intracranial circulation by combination of thrombus and multiple coils. Microcatheter is being withdrawn from basilar artery (arrow).

9 280 ENDOVASCULAR TREATMENT OF INTRACRANTAL ANEURYSMS Mayo Clin Proc, March 1994, Vol 69 microsolder junction between the stainless steel guidewire and the platinum coil during a 5- to 10-minute period and thereby detaches the platinum coil from the guidewire. Platinum is unaffected by electrolysis. During the process of detachment of the coil, the platinum coil assumes a positive charge and attracts negatively charged blood products such as platelets, fibrinogen, leukocytes, and erythrocytes. A thrombus forms around the coil within the aneurysm; this process is called electrothrombosis. The platinum coil acts as a mesh and prevents embolization of the thrombus from the aneurysm. Therefore, the aneurysm is occluded by a combination of the thrombus and the intertwined detached platinum coils. The Guglielmi detachable coil system is an investigational device, and its use is currently limited to 20 investigational sites in North America. Long-term follow-up data are still unavailable, but preliminary experience at the Mayo Clinic and other investigational sites has been encouraging." Aneurysms that manifest with subarachnoid hemorrhage have been treated successfully within the first few hours after rupture. The best results immediately after the procedure and at 6-month follow-up angiography have involved small aneurysms with small necks. 48,50 The platinum coils are extremely soft and pliable; thus, placing them inside the lumen of an aneurysm is almost an atraumatic experience. On follow-up angiograms, we and others have observed that the coils compact or change position slightly within the lumen of the aneurysm. This phenomenon is particularly common in aneurysms with a wide neck in which the water-hammer effect exerted on the coils near the neck of the aneurysm is substantial. Usually, the patient can be re-treatedx>n one or more occasions, and 99 to 100% occlusion of the aneurysm can be achieved (Fig. 6). The timing of surgical treatment of an aneurysm after subarachnoid hemorrhage has been a subject of controversy in the neurosurgical literature. 41 ' 5154 Advocates of early treatment (within the first 72 hours after subarachnoid hemorrhage) cite a lower frequency of complications related to rebleeding. In addition, early treatment of aneurysms facilitates aggressive medical or endovascular management of vasospasm, a possible sequela of subarachnoid hemorrhage. The ischemie complications associated with vasospasm are best treated medically by expanding intravascular volume and maintaining normotension or hypertension. If medical management is unsuccessful, vasospasm can also be treated with balloon angioplasty or infusion of papaverine hydrochloride intra-arterially (or both). Because of the risk of rehemorrhage associated with aggressive medical and endovascular therapy for vasospasm, neither treatment can be safely implemented until the aneurysm is excluded from the intracranial circulation. Advocates of delayed treatment (more than 10 days after subarachnoid hemorrhage) cite a better outcome in patients who survived to undergo late operation because of more stable patient conditions and easier operating conditions when the acute effects of subarachnoid hemorrhage, including ischemia and cerebral edema, have abated. Endovascular treatment of recently ruptured aneurysms during the acute phase is theoretically attractive because it would substantially decrease or eliminate the possibility of rehemorrhage, facilitate the aggressive medical or endovascular management of vasospasm, and avoid the difficulties associated with direct surgical procedures on an already injured brain. Thus, the long-term survival and outcome of patients with subarachnoid hemorrhage may be improved. 55 BALLOON ANGIOPLASTY OF VASOSPASM A discussion of the endovascular treatment of aneurysms would be incomplete without mentioning the role of endovascular techniques for cerebral vasospasm after subarachnoid hemorrhage. Among patients who survive the initial hemorrhage, 30% will have symptomatic cerebral vasospasm that results in a delayed ischemie deficit Initial therapy to prevent or to modify a delayed ischemie deficit attributable to vasospasm includes the administration of nimodipine, a calcium channel antagonist. Hypertension and hypervolemia are initiated at the first sign of a delayed ischemie deficit. If medical treatment fails, endovascular techniques may have a role in the treatment of vasospasm. Fig. 6. Radiographie studies of 39-year-old man with sudden onset of severe headache and decreased level of consciousness. A, Computed tomographic scan of head, demonstrating diffuse subarachnoid hemorrhage, most prominent in region of interpeduncular cistern (arrow). B, Angiogram of left vertebral artery, Towne view, demonstrating aneurysm, 16 mm in maximal diameter, at tip of basilar artery. Aneurysm was treated with Guglielmi detachable coils 48 hours after onset of symptoms. C, Angiogram of left vertebral artery, Towne view, obtained immediately after treatment of aneurysm. Seven coils, a total of 180 cm in length, were detached within aneurysm. Note small portion of base of aneurysm that remains patent after initial treatment (arrow). It was technically impossible to place a coil in remaining patent portion of aneurysm because of its small size. D, Radiograph, unsubtracted Towne view, demonstrating position and configuration of detached coils after initial treatment. E, Angiogram of left vertebral artery, Towne view, obtained 6 weeks after treatment, demonstrating slight interval enlargement of aneurysmal remnant (arrow). (Compare with C.) F, Aneurysmal remnant was successfully treated by detaching a single additional coil, 8 cm in length and 2 mm in diameter. G, Radiograph, unsubtracted Towne view, demonstrating position of additional detached coil (arrow). (Compare with D.)

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11 282 ENDOVASCULAR TREATMENT OF INTRACRANIAL ANEURYSMS Mayo Clin Proc, March 1994, Vol 69 Balloon angioplasty of symptomatic vasospasm has the best chance of being successful and of reversing the neurologic deficit if performed as soon as possible after the onset of symptoms unresponsive to maximal medical therapy. 58 Optimally, patients should be treated within the first 6 to 12 hours after the onset of symptoms. Angioplasty, however, may be performed within 48 hours, and recovery may be good. Other criteria for the selection of patients include exclusion of other potential causes of a new neurologic deficit, such as hydrocephalus or hematoma, and angiographically demonstrated vasospasm in a site accountable for the neurologic findings. Preferably, the aneurysm that was the source of the subarachnoid hemorrhage should be either surgically clipped or treated by endovascular techniques before balloon angioplasty because the increase in cerebral perfusion, which occurs after angioplasty, can lead to rerupture of an untreated aneurysm. In 1984, Zubkov and colleagues 59 were the first to report the successful use of balloon angioplasty, with latex balloons, for the treatment of cerebral vasospasm. A balloon of silicone elastomers that has superior expansion and elongation properties and yet maintains a soft, low-tension shell (Interventional Therapeutics Corporation, South San Francisco, California) has since become available and now is the balloon most commonly used for angioplasty procedures for vasospasm. 60 A transfemoral approach is used, and the patient receives systemic anticoagulant therapy. The microcatheter with the attached angioplasty balloon is navigated into the vascular territory to be treated. Digital subtraction angiography and fluoroscopic road-mapping guidance are necessary to avoid inflating the balloon in small branch vessels that may rupture. A steerable guidewire can be advanced through the catheter to aid in the catheterization of vessels that are difficult to access. 61 When catheterization of the vessel to be treated is successful, the balloon is inflated for 1 to 2 seconds and then deflated. Usually, the vessel is dilated in a proximal to distal fashion (Fig. 7). The results at the Mayo Clinic and those reported by other institutions 5862 for balloon angioplasty of symptomatic cerebral vasospasm have demonstrated improvement in neurologic function in approximately 70% of patients. In general, reversal of a neurologic deficit is good if the angiographically demonstrated and treated vasospasm is in a vascular territory that correlates with the observed neurologic deficit and if the vasospasm is treated within the first 12 hours after the onset of the deficit. Morbidity increases when the aneurysm, which was the source of the hemorrhage, has not been treated. Rupture and occlusion of vessels have also been reported After a vessel has been dilated to its normal luminal diameter, recurrent vasospasm on follow-up angiography is rare. When the silicone balloon is maximally inflated, it is 4 mm in diameter and 12 mm in length. Therefore, the angioplasty procedure is usually limited to the intracranial carotid artery, the M-l segment of the middle cerebral artery, the A-l segment of the anterior cerebral artery, the intracranial vertebral artery, the basilar artery, and the P-l segment of the posterior cerebral artery. More distal catheterization is usually possible, but balloon dilation of the distal cortical branches is associated with a high risk of overdistention and rupture If, after dilation of the accessible vessels, severe vasospasm persists in the distal untreated vessels on follow-up angiography, the remaining vasospasm can be treated by infusing papaverine intra-arterially through a microcatheter placed in the intracranial circulation or through a larger catheter placed in the cervical internal carotid or vertebral artery This technique is relatively new, and results are preliminary. Dosages and rates of administration are empiric, but we have consistently observed angiographie improvement of distally located vasospasm after infusing 150 mg of papaverine diluted in isotonic saline for a half hour through a microcatheter placed just proximal to the angiographically observed vasospasm. Corresponding improvement in neurologic function occurs in about 50% of patients. Unlike the results with balloon angioplasty, recurrent vasospasm of the treated vessels has been observed several days after treatment; thus, re-treatment is sometimes necessary. Fig. 7. Radiographie studies of 35-year-old man with severe subarachnoid hemorrhage resulting from ruptured aneurysm at tip of basilar artery. A, Computed tomogram of head, demonstrating subarachnoid blood, which is particularly prominent in sylvian fissures (straight arrows) and pontine cistern (curved arrow). B, Lateral angiogram of left vertebral artery, demonstrating bilobed aneurysm, 5 mm in maximal diameter, at tip of basilar artery (arrow). Aneurysm was treated by detaching four Guglielmi coils, a total of 38 cm in length, inside aneurysm. C, Lateral angiogram of left vertebral artery, demonstrating successful coil occlusion of aneurysm (arrow). D and E, Angiograms, Towne view, ofrightand left common carotid arteries obtained immediately after coil occlusion of aneurysm, demonstrating severe vasospasm involving supraclinoid internal carotid arteries (open arrows), M-l segments of middle cerebral arteries (solid arrows), A-l segments of anterior cerebral arteries (large arrowheads), and small cortical branches of distal middle and anterior cerebral arteries (small arrowheads). Supraclinoid internal carotid arteries and M-l segments of middle cerebral arteries were treated by balloon angioplasty, and then 100 mg of papaverine was infused directly into both internal carotid arteries for 30 minutes. F and G, Angiograms, Towne view, of right and left internal carotid arteries obtained immediately after balloon angioplasty and infusion of papaverine, demonstrating substantial improvement in diameter of vessels treated with angioplasty and also of more distal branches treated with infusion of papaverine.

12 Mayo Clin Proc, March 1994, Vol 69 ENDOVASCULAR TREATMENT OF INTRACRANIAL ANEURYSMS 283

13 284 ENDOVASCULAR TREATMENT OF INTRACRANIAL ANEURYSMS Mayo Clin Proc, March 1994, Vol 69 CONCLUSION The endovascular techniques used for the treatment of intracranial aneurysms and the sequelae of subarachnoid hemorrhage have evolved rapidly during the past decade, and they continue to evolve. Neurosurgical clipping of the neck of the aneurysm remains the therapy of choice; however, in some patients, endovascular techniques may be the best treatment because of the poor condition of the patient or the characteristics of the aneurysm. As technology continues to improve and as greater experience is obtained, interventional neuroradiologists will continue to have an increasingly important role in the treatment of intracranial aneurysms. REFERENCES 1. Chason JL, Hindman WM. Berry aneurysms of the circle of Willis: results of a planned autopsy study. Neurology 1958; 8: Housepian EM, Pool JL. A systematic analysis of intracranial aneurysms from the autopsy file of the Presbyterian Hospital: 1914 to J Neuropathol Exp Neurol 1958; 17: Stehbens WE. Aneurysms and anatomical variation of cerebral arteries. ArchPathol 1963;75: Phillips LH Π, Whisnant JP, O'Fallon WM, Sundt TM Jr. The unchanging pattern of subarachnoid hemorrhage in a community. Neurology 1980;30: Adams HP Jr, Kassell NF, Tomer JC, Nibbelink DW, Sahs AL. Early management of aneurysmal subarachnoid hemorrhage: a report of the Cooperative Aneurysm Study. JNeurosurg 1981; 54: Serbinenko FA. Catheterization and occlusion of major cerebral vessels and prospects for the development of vascular neurosurgery. Vopr Neirokhir 1971; 35(No. 5): Serbinenko FA. Balloon catheterization and occlusion of major cerebral vessels. JNeurosurg 1974;41: Debrun G, Fox A, Drake C, Peerless S, Girvin J, Ferguson G. Giant unclippable aneurysms: treatment with detachable balloons. AJNR Am J Neuroradiol 1981;-2: Berenstein A, Ransohoff J, Kupersmith M, Hamm E, Graeb D. Transvascular treatment of giant aneurysms of the cavernous carotid and vertebral arteries: functional investigation and embolization. Surg Neurol 1984;21: Fox AJ, Vinuela F, Pelz DM, Peerless SJ, Ferguson GG, Drake CG, et al. Use of detachable balloons for proximal artery occlusion in the treatment of unclippable cerebral aneurysms. J Neurosurg 1987; 66: Higashida RT, Halbach VV, Dowd C, Bamwell SL, Dormandy B, Bell J, et al. Endovascular detachable balloon embolization therapy of cavernous carotid artery aneurysms: results in 87 cases. J Neurosurg 1990; 72: Higashida RT, Halbach VV, Dowd CF, Barnwell SL, Hieshima GB. Intracranial aneurysms: interventional neurovascular treatment with detachable balloons results in 215 cases. Radiology 1991; 178: Aymard A, Gobin YP, Hodes JE, Bien S, Rüfenacht D, Reizine D, et al. Endovascular occlusion of vertebral arteries in the treatment of unclippable vertebrobasilar aneurysms. J Neurosurg 1991; 74: Hillman RS. Vitamin B 12, folic acid, and the treatment of megaloblastic anemias. In: Gilman AG, Goodman LS, Gilman A, editors. The Pharmacological Basis of Therapeutics. 6th ed. New York: Macmillan, 1980: Peterman SB, Taylor A Jr, Hoffman JC Jr. Improved detection of cerebral hypoperfusion with internal carotid balloon test occlusion and "Tc-HMPAO cerebral perfusion SPECT imaging. AJNR Am J Neuroradiol 1991; 12: Monsein LH, Jeffery PJ, van Heerden BB, Szabo Z, Schwartz JR, Camargo EE, et al. Assessing adequacy of collateral circulation during balloon test occlusion of the internal carotid artery with T c- HMPAO SPECT. AJNR Am J Neuroradiol 1991;12: Eckard DA, Purdy PD, Bonté FJ. Temporary balloon occlusion of the carotid artery combined with brain blood flow imaging as a test to predict tolerance prior to permanent carotid sacrifice. AJNR Am J Neuroradiol 1992; 13: Yonas H, Linskey M, Johnson DW, Horton JA, Janecka IP, Witt J-P, et al. Internal carotid balloon test occlusion does require quantitative CBF [letter]. AJNR Am J Neuroradiol 1992;13: Tarr RW, Jungreis CA, Pentheny S, Horton JA. Complications of preoperative balloon test occlusion of the internal carotid arteries: experience in 300 cases. Presented at the 29th Annual Meeting of the American Society of Neuroradiology; 1991 Jun 9-14; Washington (DC) 20. Rogg J, Rutigliano M, Yonas H, Johnson DW, Pentheny S, Latchaw RE. The acetazolamide challenge: imaging techniques designed to evaluate cerebral blood flow reserve. AJNR Am J Neuroradiol 1989; 10: Eskridge JM. The challenge of carotid occlusion. AJNR Am J Neuroradiol 1991; 12: Hieshima GB, Grinnell VS, Mehringer CM. A detachable balloon for therapeutic transcatheter occlusions. Radiology 1981; 138: Higashida RT, Halbach VV, Dormandy B, Bell JD, Hieshima GB. Endovascular treatment of intracranial aneurysms with a new silicone microballoon device: technical considerations and indications for therapy. Radiology 1990;174: Romodanov AP, Shcheglov VI. Intravascular occlusion of saccular aneurysms of the cerebral arteries by means of a detachable balloon catheter. In: Krayenbühl H, editor. Advances and Technical Standards in Neurosurgery. Vol 9. New York: Springer-Verlag, 1982: Debrun G, Lacour P, Caron J-P, Hurth M, Comoy J, Keravel Y. Detachable balloon and calibrated-leak balloon techniques in the treatment of cerebral vascular lesions. J Neurosurg 1978; 49: Nelson M. A versatile, steerable, flow-guided catheter for delivery of detachable balloons. AJNR Am J Neuroradiol 1990; 11: Rüfenacht DA, Nichols DA. A 1.1 F/2.7 F coaxial catheter system for intracranial balloon detachment. Presented at the 29th Annual Meeting of the American Society of Neuroradiology; 1991 Jun 9-14; Washington (DC) 28. Scott M, Skwarok E. The treatment of cerebral aneurysms by ligation of the common carotid artery. Surg Gynecol Obstet 1961; 113: Gonzalez CF, Moret J. Balloon occlusion of the carotid artery prior to surgery for neck tumors. AJNR Am J Neuroradiol 1990; 11: Higashida RT, Halbach VV, Cahan LD, Hieshima GB, Konishi Y. Detachable balloon embolization therapy of posterior circulation intracranial aneurysms. JNeurosurg 1989;71: Steinberg GK, Drake CG, Peerless SJ. Deliberate basilar or vertebral artery occlusion in the treatment of intracranial aneurysms: immediate results and long-term outcome in 201 patients. J Neurosurg 1993;79: Higashida RT, Halbach W, Bamwell SL, Dowd C, Dormandy B, Bell J, et al. Treatment of intracranial aneurysms with preservation of the parent vessel: results of percutaneous balloon embolization in 84 patients. AJNR Am J Neuroradiol 1990;11: Moret J, Boulin A, Mawad M, Castaings L. Endovascular treatment of berry aneurysms by endosaccular balloon occlusion. Neuroradiology 1991; 33(Suppl):S135-S Shcheglov VI. Endovascular occlusion of saccular intracranial aneurysms: results in 617 patients. Presented at the 27th Annual Meeting

14 Mayo Clin Proc, March 1994, Vol 69 ENDOVASCULAR TREATMENT OF INTRACRANIAL ANEURYSMS 285 of the American Society of Neuroradiology; 1989 Mar 18-24; Orlando (FL) 35. Taki W, Handa H, Yamagata S, Ishikawa M, Iwata H, Ikada Y. Radiopaque solidifying liquids for releasable balloon technique: a technical note. Surg Neurol 1980;13: Goto K, Halbach VV, Hardin CW, Higashida RT, Hieshima GB. Permanent inflation of detachable balloons with a low-viscosity hydrophilic polymerizing system. Radiology 1988; 169: Strother CM, Lunde S, Graves V, Toutant S, Hieshima GB. Late paraophthalmic aneurysm rupture following endovascular treatment: case report. J Neurosurg 1989;71: Hodes JE, Fox AJ, Pelz DM, Peerless SJ. Rupture of aneurysms following balloon embolization. J Neurosurg 1990;72: Kwan ESK, Heilman CB, Shucart WA, Klucznik RP. Enlargement of basilar artery aneurysms following balloon occlusion "waterhammer effect": report of two cases. J Neurosurg 1991; 75: Kassell NF, Tomer JC, Jane JA, Haley EC Jr, Adams HP. The International Cooperative Study on the Timing of Aneurysm Surgery. Part 2. Surgical results. J Neurosurg 1990; 73: Graves VB, Strother CM, Rappe AH. Treatment of experimental canine carotid aneurysms with platinum coils. AJNR Am J Neuroradiol 1993; 14: Hilal SK, Khandji AG, Chi TL, Stein BM, Bello JA, Silver AJ. Synthetic fiber-coated platinum coils successfully used for the endovascular treatment of arteriovenous malformations, aneurysms and direct arteriovenous fistulas of the CNS [abstract]. AJNR Am J Neuroradiol 1988; 9: Hilal SK, Chi LT, Khandji A, Friedman D, Cross D, Solomon R. Preshaped thrombogenic coils for the treatment of intracranial aneurysms. Presented at the 28th Annual Meeting of the American Society of Neuroradiology; 1990 Mar 19-23; Los Angeles 44. Graves VB, Partington CR, Rüfenacht DA, Rappe AH, Strother CM. Treatment of carotid artery aneurysms with platinum coils: an experimental study in dogs. AJNR Am J Neuroradiol 1990; 11: Dowd CF, Halbach VV, Higashida RT, Bamwell SL, Hieshima GB. Endovascular coil embolization of unusual posterior inferior cerebellar artery aneurysms. Neurosurgery 1990;27: Guglielmi G, Vifluela F, Sepetka I, Macellari V. Electrothrombosis of saccular aneurysms via endovascular approach. Part 1. Electrochemical basis, technique, and experimental results. J Neurosurg 1991;75: Guglielmi G, Vifiuela F, Dion J, Duckwiler G. Electrothrombosis of saccular aneurysms via endovascular approach. Part 2. Preliminary clinical experience. J Neurosurg 1991;75: Guglielmi G, Vifluela F, Duckwiler G, Dion J, Lylyk P, Berenstein A, et al. Endovascular treatment of posterior circulation aneurysms by electrothrombosis using electrically detachable coils. J Neurosurg 1992;77: Casasco AE, Aymard A, Gobin YP, Houdart E, Rogopoulos A, George B, et al. Selective endovascular treatment of 71 intracranial aneurysms with platinum coils. J Neurosurg 1993;79: Vifiuela F. North American experience in the embolization of intracranial aneurysms with the GDC system. Presented at the 30th Annual Meeting of the American Society of Neuroradiology; 1992 May 31-Jun 5; St. Louis 51. Kassell NF, Boarini DJ, Adams HP Jr, Sahs AL, Graf CJ, Tomer JC, et al. Overall management of ruptured aneurysm: comparison of early and late operation. Neurosurgery 1981;9: Kassell NF, Drake CG. Timing of aneurysm surgery. Neurosurgery 1982; 10: Kassell NF, Tomer JC, Haley EC Jr, Jane JA, Adams HP, Kongable GL. The International Cooperative Study on the Timing of Aneurysm Surgery. Part 1. Overall management results. J Neurosurg 1990;73: Chyatte D, Fode NC, Sundt TM Jr. Early versus late intracranial aneurysm surgery in subarachnoid hemorrhage. J Neurosurg 1988; 69: Nichols DA. Endovascular treatment of the acutely ruptured intracranial aneurysm [editorial]. J Neurosurg 1993;79: Allcock JM, Drake CG. Ruptured intracranial aneurysms the role of arterial spasm. J Neurosurg 1965;22: Mullan S. Conservative management of the recently ruptured aneurysm. Surg Neurol 1975;3: Eskridge JM, Newell DW, Pendleton GA. Transluminal angioplasty for treatment of vasospasm. Neurosurg Clin North Am 1990 Apr; 1: Zubkov YN, Nikiforov BM, Shustin VA. Balloon catheter technique for dilatation of constricted cerebral arteries after aneurysmal SAH. Acta Neurochir 1984;70: Higashida RT, Halbach VV, Dormandy B, Bell J, Brant-Zawadzki M, Hieshima GB. New microballoon device for transluminal angioplasty of intracranial arterial vasospasm. AJNR Am J Neuroradiol 1990;11: Brothers MF, Holgate RC. Intracranial angioplasty for treatment of vasospasm after subarachnoid hemorrhage: technique and modifications to improve branch access. AJNR Am J Neuroradiol 1990; 11: Higashida RT, Halbach VV, Cahan LD, Brant-Zawadzki M, Barnwell S, Dowd C, et al. Transluminal angioplasty for treatment of intracranial arterial vasospasm. J Neurosurg 1989;71: Linskey ME, Horton JA, Rao GR, Yonas H. Fatal rupture of the intracranial carotid artery during transluminal angioplasty for vasospasm induced by subarachnoid hemorrhage: case report. J Neurosurg 1991;74: Brothers MF, Hedlund LW, Friedman AH. Arterial rupture during "distal" vasospasm angioplasty [abstract]. Neuroradiology 1991; 33(Suppl):S Schueler BA, Rüfenacht DA. Risk factors leading to cerebral arterial rupture by intravascular balloon. AJNR Am J Neuroradiol 1993; 14: Kassell NF, Helm G, Simmons N, Phillips CD, Cail WS. Treatment of cerebral vasospasm with intra-arterial papaverine. J Neurosurg 1992; 77: Kaku Y, Yonekawa Y, Tsukahara T, Kazekawa K. Superselective intra-arterial infusion of papaverine for the treatment of cerebral vasospasm after subarachnoid hemorrhage. J Neurosurg 1992; 77:

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