Complex dural arteriovenous fistulas. Results of combined endovascular and neurosurgical treatment in 16 patients

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J Neurosurg 71:352-358,1989 Complex dural arteriovenous fistulas Results of combined endovascular and neurosurgical treatment in 16 patients STANLEY L. BARNWELL, M.D., PH.D., VAN V. HALBACH, M.D., RANDALL T. HIGASHIDA, M.D., GRANT HIESHIMA, M.D., AND CHARLES B. WILSON, M.D. Departments of Neurological Surgery and Radiology, School of Medicine, University of California, San Francisco, California ~" Of the 88 patients evaluated for symptomatic dural arteriovenous (AV) fistula over the past 8 years, 16 had large or complicated lesions that could not be treated with standard transvascular approaches or in which such treatment had been unsuccessful. Eleven fistulas were located in the transverse sinus, two in the cavernous sinus, two in the straight sinus, and one in the falx-tentorial region near the vein of Galen. The patients were treated with a combination of endovascular and neurosurgical techniques. Fourteen patients underwent preoperative transarterial embolization; this procedure closed the fistula in one patient. In the remaining 15 patients, surgery was performed to provide access to the fistula for embolization from either the venous or the arterial side, or for excision of the fistula. Transvenous embolization completely obliterated the fistula in seven of nine patients; the fistulas were embolized incompletely through the feeding arteries in two patients; and complete surgical resection of the lesion was accomplished in four patients. Complications related to venous occlusion occurred in two patients and one patient suffered communicating hydrocephalus that was effectively treated by shunting. There were no deaths. The results suggest that combined endovascular and neurosurgical techniques are a safe and effective means for the treatment of selected complex dural AV fistulas. KEy WORDS 9 dural arteriovenous fistula 9 interventional neuroradiology transverse sinus 9 transvascular embolization 9 transvenous embolization D URAL arteriovenous (AV) fistulas account for 10% to 15% of all intracranial AV shunts and most often involve the dura surrounding the sigmoid and transverse sinuses. 7 Signs and symptoms of dural AV fistulas include pulse-synchronous tinnitus, bruit, headache, loss of vision, altered mental status, and neurological deficits. 45t3 Dural AV fistulas may also cause intracranial hemorrhage. Compression therapy and embolization through feeding arteries (femoral transarterial embolization) can ameliorate symptoms related to dural AV fistulas, particularly those in certain anatomical locations such as the cavernous sinus. 23 Unless the fistula is completely closed by embolization, however, collateral supply may develop and the fistula will recanalize. Occlusion of feeding vessels in an initial procedure may complicate or prevent later treatment because transarterial ap- proaches may no longer be possible. Complete obliteration of dural AV fistulas by transarterial embolization may not be possible in locations such as the superior sagittal sinus, vein of Galen, or straight sinus. There is a 15% rate of major morbidity and mortality for surgical therapy of dural AV fistulas in the transverse and sigmoid sinuses.~l Surgery of these lesions may cause massive blood loss. Over the past 8 years, 88 patients were evaluated for treatment of symptomatic dural AV fistulas by transvascular techniques. Sixteen patients either failed to respond to standard transvascular treatment or had lesions in anatomical locations that made treatment too hazardous to attempt by this approach. These patients were treated with a combined approach using both endovascular and neurosurgical techniques. The methods used and the results of therapy are reported here. 352 J. Neurosurg. / Volume 71/September, 1989

Complex dural arteriovenous fistulas Clinical Material and Methods Sixteen patients, 11 men and five women, were included in this series. These patients presented with large or complicated dural AV fistulas that produced loud bruits, neurological deficits, or intracranial hemorrhage. Five patients had been treated previously with either embolization or ligation of the feeding vessels. In none of the procedures was the fistula treated directly. In three patients the bruit returned within weeks after treatment. One patient developed progressive neurological deficits and one patient had an intracranial hemorrhage. Treatment Planning The patients were evaluated by neurosurgeons and interventional neuroradiologists. Treatment included preoperative vascular embolization and surgery. Surgical procedures were chosen to expose the draining vein intracranially and to perform transvenous embolization, to expose a feeding artery extracranially close to the fistula and to perform transarterial embolization, or to resect or isolate the fistula. Preoperative Vascular Embolization In 14 patients, transarterial embolization of the major vessels supplying the dural AV fistulas was performed to reduce blood flow before craniotomy. The common carotid artery had been ligated previously in one patient (Case 2), and embolization was performed after direct exposure of the external carotid artery in the neck. In the other patients, a No. 5.5 or 7.5 French sheath was placed in one of the femoral arteries, and a No. 5 or 7 French catheter was passed through the sheath and navigated to either the proximal internal or external carotid artery. A No. 3/2 French Tracker catheter was advanced over a 0.014- or 0.016-in. platinumtipped guidewire into the selected vessel. Embolization of the fistula was performed with liquid adhesive (isobutyl-2-cyanoacrylate)* or particulate embolic agents (polyvinyl alcohol particles ranging from 200 to 1000 in diameter).t Because isobutyl-2-cyanoacrylate is no longer commercially available for intravascular use, n- butyl-2-cyanoacrylatez,~ is used in this procedure. Two patients (Cases 4 and 5) did not undergo embolization preoperatively because previous ligations made the feeding arteries inaccessible to transarterial embolization. Surgical Therapy Fifteen patients were treated with one of three forms of surgical therapy. The operations included: exposure of the draining vein intracranially to allow embolization * Isobutyl-2-cyanoacrylate manufactured by Ethicon. Norderstedt, NL, West Germany. t Polyvinyl alcohol particles manufactured by Pacific Medical Industries, La Mesa, California. N-butyl-2-cyanoacrylate manufactured by CRX Medical Raleigh, North Carolina. by venous route; exposure of feeding arteries extracranially but close to the fistula to allow embolization of previously inaccessible feeders; or craniotomy to resect the fistula. Transvenous Embolization. Five patients (Cases 3, 4, 6, 7, and 10) with fistulas in the transverse sinus underwent embolization via a transvenous route. The venous drainage was occluded by ligating the transverse sinus between the fistula and the venous outflow. In all but one case (Case 7), flow through the transverse sinus was retrograde toward the torcular Herophili because of thrombosis of the sinus at the junction of the sigmoid sinus and the transverse sinus. In these four patients, the transverse sinus was ligated between the torcular Herophili and the lateral portion of the involved transverse sinus; veins with retrograde flow out of the transverse sinus were also ligated, after which a blind venous pouch remained that connected directly to the fistula. The pouch was cannulated with a No. 27 needle and was filled with liquid adhesive to occlude the fistula. Obliteration of the fistula was confirmed with an intraoperative angiogram. Three patients (Cases 14, 15, and 16) with fistulas in the straight sinus or falx-tentorial junction underwent embolization through the transvenous approach. The venous drainage was occluded by ligating the draining veins of the involved dura. The vein was cannulated with a needle and filled with liquid adhesive to occlude the fistula. One patient (Case 13) with a fistula in the cavernous sinus underwent embolization through the transvenous approach. The cavernous sinus was cannulated with a needle and filled with liquid adhesive to occlude the fistula. Transarterial Embolization. Two patients (Cases 5 and 9) were treated by transarterial embolization with liquid adhesives. Previous procedures or ectatic vessels precluded transfemoral arterial embolization. In both patients, vessels that penetrated the cranium and supplied the fistula were exposed surgically. These arteries were cannulated, intraoperative angiograms were obtained, and liquid adhesive was deposited directly into the fistula. Surgical Isolation or Resection. Surgical isolation or resection of the fistula was performed in four patients (Cases 1, 2, 11, and 12). The operation to interrupt all arterial inflow or to resect the lesion required an extensive craniotomy. Patient Population Results The mean age for the 11 men was 56 years and for the five women was 44 years. All had large complicated dural AV fistulas. A summary of the patient characteristics, including age, sex, location of the fistula, arterial supply, venous drainage, previous treatment, embolization, surgery, and outcome is summarized in Table 1. J. Neurosurg. / Volume 71/September, 1989 353

S. L. Barnwell, et al. FIG. 1. Angiograms in Case 14. Left: Angiogram of the left occipital artery, anteroposterior projection, showing a straight sinus dural arteriovenous fistula (arrows). Supply to the fistula was from the occipital artery and the posterior meningeal branch of the vertebral artery. The occipital artery supply was occluded with liquid adhesive. Center. Angiogram of the left vertebral artery, anteroposterior projection (venous phase), showing outflow obstruction with drainage through a superficial cerebellar vein (arrows). The draining vein was ligated and liquid adhesive refluxed into the fistula. Right: Postoperative angiogram of the left external carotid artery, lateral projection, showing complete obliteration of the fistula. Location of Dural Arteriovenous Fistulas The most common site of the dural AV fistula was the transverse sinus: 11 lesions were found in this region, seven of which involved the left side. In the remaining patients, the lesion involved the cavernous sinus in two, the straight sinus in two, and the falxtentorial region at the vein of Galen in one. Arterial Supply The arterial supply to the dural AV fistula was related to the site of the lesion. All lesions involving the transverse sinus were supplied by branches of the external carotid artery, including the occipital, posterior auricular, ascending pharyngeal, superficial temporal, and middle meningeal arteries (Cases 1 to 11). In some patients, this supply was bilateral. The posterior meningeal branch of the vertebral artery supplied the transverse sinus fistula in six patients. In eight of the 11 patients whose dural AV fistula involved the transverse sinus, the lesion was supplied from the internal carotid artery through its meningohypophyseal branch. In both patients with fistulas in the cavernous sinus (Cases 12 and 13), the lesion was supplied from external carotid artery branches. In one of these patients, the lesion was supplied by the internal carotid artery through its meningohypophyseal branch. Fistulas in the straight sinus (Cases 14 and 15) were supplied by branches of the external carotid artery and by the posterior meningeal branch of the vertebral artery. The lesion involving the vein of Galen (Case 16) was supplied by branches of both the internal and external carotid arteries and by dural branches of the posterior cerebral arteries. Venous Drainage Venous drainage of the dural AV fistula was ab in 14 patients. Among the 11 patients with a lesion involving the transverse sinus, nine had either total occlusion or severe stenosis of the transverse-sigmoid sinus outflow. Thrombosis of venous outflow pathways distal to the site of dural AV fistula in some cases resulted in venous ectasia in the draining vein. With the obstruction of venous outflow, alternative pathways for venous drainage developed to the cortical veins, epidural venous plexus, or retrograde into the superior sagittal sinus and across the torcular Herophili. In all three patients with a fistula involving the falx-tentorial junction near the vein of Galen or straight sinus, there was also ab venous drainage to the cortical veins caused by occlusion of the transverse sinus or straight sinus. Preoperative Embolization Preoperative embolization with liquid adhesives or particulate embolic agents to reduce blood flow to the fistula was performed in 14 patients (Cases 1 to 3, and 6 to 16). In one patient (Case 8), the procedure obliterated the fistula and no further therapy was necessary. Transvenous Embolization This procedure was used in nine patients. Fistulas were located in the transverse sinus (five patients), 354 J. Neurosurg. / Volume 71/September, 1989

Complex dural arteriovenous fistulas Fie. 2. Angiograms in Case 16. Left: Angiogram of the left internal carotid artery, lateral projection, showing a dural arteriovenous fistula involving the region just superior and anterior to the enlarged vein of Galen. Arterial supply was from the middle meningeal and pericallosal arteries bilaterally, and from tentorial branches of the meningohypophyseal trunks. Venous drainage was to the vein of Galen then to the straight sinus, which diminished in size as it approached the torcular Herophili. Predominant venous drainage was into the right transverse sinus, which ended abruptly owing to thrombosis of the sigmoid sinus. Venous collateral vessels drained to cortical veins anteriorly, then to the cavernous sinus and basilar plexus. Right: Postoperative angiogram of the left internal cerebral artery, lateral projection, showing complete obliteration of the fistula. straight sinus (two patients), vein of Galen (one patient), and cavernous sinus (one patient). Transvenous embolization produced angiographically confirmed cures in three of five patients with fistulas of the transverse sinus and all of the other patients. All patients have been followed clinically for at least 1 year. In both patients with a fistula involving the straight sinus (Cases 14 and 15), cortical venous drainage was exposed through a craniotomy and the veins were closed (Fig. 1). The blind venous pouch was then cannulated with a No. 27 Angiocath and embolized with liquid adhesive. An intraoperative angiogram showed complete obliteration of the fistula. The patient with a fistula involving the dura near the vein of Galen (Case 16) underwent a staged procedure. In the first operation, the fistula was exposed through a right parieto~ craniotomy. All feeding arteries that could be identified were cut. Three weeks later, the fistula was approached through the same incision. It was noted that when the internal cerebral vein was occluded, the turgor in the vein of Galen was markedly reduced; this indicated that the fistula was proximal to the internal cerebral vein, which was ligated and liquid adhesive was injected into the stump. Liquid adhesive was then injected into the fistula (Fig. 2). In one patient (Case 13), who had a fistula involving the cavernous sinus, previous carotid ligation precluded transarterial embolization. The lateral wall of the sinus was exposed surgically, cannulated with a No. 27 Angiocath, and embolized directly with liquid adhesive. Permanent obliteration of the fistula was not accomplished in two patients. One patient (Case 3) had undergone two embolization procedures and two craniotomies that were performed to interrupt the arterial supply to the dural AV fistula. During the course of those procedures, recruitment of new arterial supply to the fistula and collateral venous drainage to the torcular Herophili had occurred. Although the transvenous embolization did not completely close the fistula, flow was markedly decreased. Because exceptionally low flow through the dural AV fistula may lead to complete thrombosis, no additional therapy was offered. At an 8- month follow-up evaluation, the patient was well and had not suffered recurrent hemorrhages. The other case of unsuccessful treatment occurred in a patient who was found to have complete closure of the fistula after transvenous embolization (Case 7). This case was unique because of a mild venous outflow obstruction (Fig. 3). The transverse sinus was isolated as described earlier. Before liquid adhesive was injected into the venous pouch, the outflow through the sigmoid sinus was temporarily occluded with a nondetachable Silastic balloon introduced into the sigmoid sinus through the internal jugular vein. This step enabled the liquid adhesive to lodge in the fistula instead of being washed out through the sigmoid sinus and jugular vein. After obliteration of the fistula had been confirmed angiographically, the balloon was deflated and removed. Five months later the patient's bruit returned and has not resolved. The patient is doing well clinically and no additional therapy has been performed. Transarterial Embolization The arteries leading to the fistula were surgically exposed in two patients (Cases 5 and 9). Previous surgical ligations or ectatic vessels precluded the femoral transarterial route for embolization. The exposure was performed close to the fistula, although a craniotomy J. Neurosurg. / Volume 71/September, 1989 355

S. L. Barnwell, et al. FIG. 3. Angiograms in Case 7. Left: Angiogram of the left ascending pharyngeal artery, lateral projection, showing a dural arteriovenous fistula (straight arrows) involving the left transverse sinus. Venous drainage was into the left sigmoid sinus and jugular vein (curved arrows) and suboccipital veins. Right: Postoperative angiogram of the left external carotid artery, lateral projection, showing complete obliteration of the fistula. was not necessary. One month after ligation was performed on Case 5, the bruit returned, although it was not disabling and no further therapy has been necessary. In Case 9, postoperative angiography showed a small residual fistula remaining after embolization, although the bruit was gone. Three months later, however, the bruit returned; it was less intense than the preoperative bruit and no further therapy has been needed. Excision of The Fistula Three patients with a dural AV fistula of the transverse sinus (Cases 1, 2, and t 1) and one patient with a fistula of the cavernous sinus (Case 12) were treated by (Fig. 4). An extensive craniotomy was performed to expose the fistula and to resect the involved dura or vessels. The lesion was successfully obliterated in all four patients. FIG. 4. Angiogram of the right external carotid artery, anteroposterior projection, in Case 11 showing a fight transverse sinus dural arteriovenous fistula (arrows) supplied by branches of the external carotid artery and by the vertebral artery. This patient had presented with an intracerebral hemorrhage. The venous drainage was ab, with collateral flow through a cortical vein (curved arrows) to the superior sagittal sinus (open arrows). These changes indicated venous occlusion and severe venous hypertension. The fistula was treated by surgically isolating the fistula from the arterial supply. Complications Complications after treatment of the dural AV fistula were related to venous occlusion in two patients (Cases 1 and 10) and to hydrocephalus in another (Case 16). No complication led to a poor outcome. The venous occlusion in one patient (Case 1) was probably the result of interruption of venous drainage caused by the extensive resection necessary to isolate the transverse sinus fistula. This patient had a homonymous hemianopsia from an occipital lobe infarction that occurred postoperatively. A complication unique to transvenous embolization of dural AV fistulas occurred in one patient (Case 10) with an extensive fistula of the transverse sinus. As the blind venous pouch was filling with liquid adhesive, excess material flowed into and occluded a pontomesencephalic vein draining into the pouch. The patient did well until the 2nd postoperative day, when 356 3". Neurosurg. / Volume 71/September, 1989

Complex dural arteriovenous fistulas TABLE 1 Summary of a series of 16 consecutive patients with large or complicated dural arteriovenous fistulas* Venous Prior Embolization Postop Case Age Presen- Site of Fistula Arterial Occlu- of Arterial Surgery No. (yrs), tation Supply Treatment Angiogram Sex sion Supply! 64, M bruit rt transverse sinus EC, IC yes none EC x 2 2 70, M hemorrhage It transverse sinus EC, vert yes EC ligation x 1 not done 3 60, M hemorrhage rt transverse sinus EC yes no EC x 4 4 54, M diplopia It transverse sinus EC, IC, vert yes EC ligation x 1 not done 5 31, F bruit It transverse sinus EC no EC ligation x 1, not done EC embolization x 2 6 70, M bruit It transverse sinus EC, IC yes no EC 1 7 55, F bruit It transverse sinus EC, IC no EC embolization x 2 EC x 2 8 56, F bruit It transverse sinus EC, vert yes no EC x 2 9 60, M bruit It transverse sinus EC, IC, vert yes no EC x 1 10 47, M diplopia rt transverse sinus EC, IC, vert, yes no EC x 4 postcerebral 11 44, F hemorrhage rt transverse sinus EC, IC, vert yes no EC x 1 12 36, F bruit rt cavernous sinus, EC, IC no no EC x 4 middle fossa 13 31, M bruit It cavernous sinus EC, IC no IC trapping x 1, 1C x 1 EC ligation x 1 14 71, M hemorrhage straight sinus EC, vert yes no EC x 1 15 46, M hemorrhage straight sinus EC, vert yes no EC x 1 16 44, M hemorrhage falx-tentorium, EC, IC, post- yes no EC x 1, vein of Galen cerebral IC x 1 artery embolization not done residual EC supply not done none artery embolization residual supply * EC = branches of external carotid artery; IC = branches of internal carotid artery; vert = branches of vertebral artery; postcerebral = posterior cerebral artery. he became comatose. A computerized tomography scan showed liquid adhesive extending beyond the sinus into the vein. Propagated venous thrombosis occurred and the patient was treated with anticoagulant agents. Over a period of weeks, he recovered and has since returned to work. One patient who had undergone two craniotomies to treat a vein of Galen fistula (Case 16) developed communicating hydrocephalus and was effectively treated by ventriculoperitoneal shunting. Discussion In this series of patients, the natural history of dural AV fistulas correlated well with the location and angiographic characteristics of the lesion. Fistulas involving the transverse sinus are associated with a higher risk of neurological deficits and hemorrhage than are lesions at other sites, s'~ Venous occlusive disease with diversion of arterialized drainage into alternative pathways causes venous hypertension that can be seen on angiograms as retrograde flow of blood into the superior sagittal sinus, across the torcular Herophili, or into cortical veins. An angiographic finding of venous occlusive disease is associated with a high risk of hemorrhage or neurological problems. In this series, eight of 12 patients with venous occlusion presented with hemorrhage or neurological deficits. Four of 16 patients with venous drainage did not present with hemorrhage or progressive neurological deficits. Previous therapeutic approaches to dural AV fistulas have included transarterial embolization and surgical excision. It is now recognized that ligation of feeding arteries is ineffective because of recruitment of collateral flow. Successful treatment of dural AV fistulas requires obliteration of the nidus of the fistula. The combination of surgery to expose draining veins or feeding arteries with endovascular embolization has not been reported in a large series of patients. Transvenous embolization of dural AV fistulas involving the cavernous sinus was first described in 1979 by Mullan. ~ In his series, this technique provided a very effective form of therapy because it obviated the need for extensive resection of the fistula and resulted in a high rate of complete closure of the fistula. Grisoli, et al., t described a method similar to ours in which veins draining dural AV fistulas in the tentorium were exposed and clipped very close to the fistula. This method achieved a complete cure in the three patients so treated. To their approach we have added embolization of the fistula with liquid adhesives to ensure closure of the fistula, which was successful in seven of nine patients treated by this approach. The transvenous approach has several advantages over embolization through the arterial route. There is less likelihood that emboli will pass through branching vessels proximal to the dural AV fistula and lodge in capillary beds. Because feeding vessels are not occluded, any fistula remaining after the initial embo- J. Neurosurg. / Volume 71 /September, 1989 357

S. L. Barnwell, et al. lization can be studied angiographically. If necessary, a second embolization may be performed. Transarterial embolization has been performed more recently using a variety of embolic agents. While complete obliteration of the fistula was rarely achieved in initial studies, 912 higher cure rates have been obtained as more experience has been gainedy 1-~ Cure rates as high as 43% have been reported for transverse sinus lesions treated with this technique? In the series reported here, intraoperative arterial embolization was performed in two patients (Cases 5 and 9) in whom standard femoral transarterial approaches were impossible because of ectatic vessels or because feeding arteries had been occluded in previous procedures. Vessels close to the fistula were exposed surgically. Both patients had complex vasculature that made complete obliteration of the fistula difficult from the arterial side, and complete closure of the fistula was not achieved in either patient. The decision to use this relatively conservative approach was based in part on the lack of severe symptoms or because it was not possible to use a transvenous approach. The nidus of the fistula can be resected either by removing the involved dura or by coagulating all vessels supplying the fistula. These approaches are associated with a high rate of morbidity and mortality related to massive blood loss or venous infarctions.11 Preoperative embolization of these lesions can reduce the blood supply sufficiently to allow surgical resection. In the patients reported here, from one to four preoperative embolization procedures were performed. Even though embolization may reduce blood flow, it rarely occludes the lesion completely and intraoperative blood loss may still be massive. Embolization may not be possible for some fistulas because neither arterial nor venous approaches are available alternatives. Four of the patients reported here (Cases 2, 4, 7, and 13) had previously undergone ligation of feeding arteries or had extensive scarring around the fistula. While this circumstance could not have been overcome easily with standard techniques, treatment by transvenous embolization and surgery was used successfully. For complex dural AV fistulas, standard arterial embolization may not close the fistula effectively, and operative removal may produce unacceptable blood loss. As an alternative, surgical exposure of vessels leading to or from the fistula may allow more effective embolization. In selected cases, surgical exposure of the draining veins to allow access for endovascular therapy provides a new safe and effective form of therapy. References 1. 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Newton TH, Cronqvist S: Involvement of dural arteries in intracranial arteriovenous malformations. Radiology 93:1071-1078, 1969 8. Obrador S, Soto M, Silvela J: Clinical syndromes of arteriovenous malformations of the transverse-sigmoid sinus. J Neurol Neurosurg Psychiatry 38:436-451, 1975 9. Quisling RG, Mickle JP, Ballinger W: Small particle polyvinyl alcohol embolization of cranial lesions with minimal arteriolar-capillary barriers. Surg Neurol 25: 243-252, 1986 10. Russel EJ, Berenstein A: Neurologic applications of interventional radiology. Neurol Cliu 2:873-902, 1984 11. Sundt TM Jr, Piepgras DG: The surgical approach to arteriovenous malformations of the lateral and sigmoid dural sinuses. J Neurosurg 59:32-39, 1983 12. Suzuki J, Komatsu S: New embolization method using estrogen for dural arteriovenous malformation and meningioma. Sure Neuroi 16:438-442, 1981 13. Vifiuela F, Fox A J, Pelz DM, et al: Unusual clinical manifestations of dural arteriovenous malformations. J Neurosurg 64:554-558, 1986 14. Wilkins RH: Natural history of intracranial vascular malformations: a review. Neurosurgery 16:421-430, 1985 Manuscript received January 15, 1988. Accepted in final form March 16, 1989. Address reprint requests to: Stanley L. Barnwell, M.D., Ph.D., c/o The Editorial Office, 1360 Ninth Avenue, Suite 210, San Francisco, California 94122. 358 J. Neurosurg. / Volume 71/September, 1989