Endovascular Treatment of Brain Arteriovenous Fistulas

Materials and Methods

From March 2006 to March 2008, a total of 9 consecutive patients with nontraumatic noniatrogenic BAVFs were treated with neuroendovascular techniques at Beijing Tiantan Hospital in Beijing, China. Conventional cerebral angiography was used to define the lesions for each patient. We strictly defined BAVFs for our study because these lesions had 1 or more direct arteriovenous connections with no intervening nidus. Dural AVFs and Galen aneurysmal malformations were excluded from this analysis. All lesions were treated with endovascular techniques. Medical records, cerebral angiograms, and endovascular reports were reviewed retrospectively. Clinical and angiographic follow-up was obtained for each patient. Clinical outcome was assessed according to the modified Rankin Scale.

Results

The lesions in our 9 patients (2 female, 7 male; mean age, 17.8 years; age range, 2–40 years) were diagnosed as BAVFs. The presenting symptoms are documented in the Table. The presentations leading to diagnosis were intracranial hemorrhage,²⁰ headaches,²¹ seizure,⁵ and no symptoms (2 patients). The location of the hemorrhage was intracerebral in 1 patient, intracerebellar in 1, and subarachnoid in 2 patients. No patients experienced neurologic deficits as a result of intracranial hemorrhage.

The topography of the lesions is listed in the Table. False venous aneurysms were found in all AVFs. There was no dural sinus stenosis, pial vein reflux, or flow-related arterial aneurysms. Eight lesions were single AVFs, and 1 lesion had 3 feeders converging toward a single pouch. The lesions were supratentorial and supplied by the branches of the anterior cerebral artery (ACA) in 4 patients, the middle cerebral artery in 1 patient, the posterior cerebral artery in 2 patients, and the basilar artery in 1 patient. Eight lesions were drained supratentorially and 1 drained supertentorially and infratentorially.

Seven patients were treated with detachable coils alone, 1 with Onyx-34 and 1 by a combination of coils and n-BCA. A single embolization session was performed in 7 patients, of which complete obliteration was obtained immediately in 4 patients. One patient was cured with 2 procedures, and another patient was cured with 4 procedures. A single pedicle was embolized in 7 patients, 2 in 1 patient, and 3 in 1 patient.

With a mean clinical follow-up of 5.7 months (range, 3–12 months), all patients were categorized as neurologically excellent without any symptoms (modified Rankin Scale, 0). Follow-up angiography was also performed at 3 to 12 months (mean, 5.7 months). Three lesions which were initially treated thrombosed spontaneously, and the other 6 lesions were completely obliterated at follow-up angiographic study. In all 9 patients, disconnection of the AV shunt resulted in obliteration of the abnormality of draining vein.

Illustrative Cases

Patient 1.

A 7-year-old boy presented with intracranial hemorrhage. Diagnostic cerebral angiography showed pial fistula with an aneurysmal venous dilation, fed by the right ACA at the junction of A1 and A2 and drained into the left sigmoid sinus (Fig 1A). A 0.5-mL Onyx-34 injection was delivered via a Marathon microcatheter (Fig 1B). The anteroposterior view of the right internal carotid artery angiogram demonstrated complete obliteration of the fistula (Fig 1C).

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Fig 1.

Patient 1. A, Angiogram of right internal carotid injection, anteroposterior view, shows a conglomerate of abnormally dilated vessels at the A1/A2 junction of the right ACA with a venous aneurysm (arrow). The lesion drains into the left sigmoid sinus and sphenoparietal sinus contralaterally via the right frontal basal vein and left tentorial sinus. B, Superselective angiography shows an arteriovenous fistula. C, Control angiogram of the right internal carotid injection after Onyx embolization, anteroposterior view, shows that the fistula was obliterated completely.

Patient 2.

A 26-year-old woman presented with headaches. Cerebral angiography showed a giant venous aneurysm, nourished by the left ACA (Fig 2A). Two detachable coils (10 × 30 Orbit, Cordis, Miami Lakes, Fla; 12 × 30, Microvention) were placed proximal to the fistula via an Echelon 14 (ev3) microcatheter (Fig 2B), and complete occlusion of the fistula was achieved spontaneously after 4 months (Fig 2C).

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Fig 2.

Patient 2. A, Angiogram of left internal carotid injection shows a pial AVF supplied by the left distal ACA with a giant venous aneurysm. B, Angiogram of the left internal carotid injection after the procedure shows that the fistula is occluded partially. C, Control angiogram at 4-month follow-up shows the fistula thrombosis spontaneously.

Patient 3.

A 7-year-old boy presented with mild head trauma. MR imaging showed a giant flow-void signal intensity in the front of the midbrain, which suggested a vascular lesion (Fig 3A). Cerebral angiography showed a large aneurysmal venous dilation, nourished by the primitive trigeminal artery from the basilar artery and drained into the basal vein of Rosenthal (Fig 3B). A 20 × 50-mm detachable coil (Microvention) was deployed via a microcatheter (Excelsior, Boston Scientific; Fig 3C). After 7 months, a left vertebral artery angiogram demonstrated complete occlusion of the fistula (Fig 3D), and MR imaging showed that the venous aneurysm had disappeared (Fig 3E).

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Fig 3.

Patient 3. A, T2-weighted MR imaging of the head at the level of the midbrain shows giant flow-void signal intensity in the interpeduncular cistern. B, Anteroposterior view of the left vertebral artery injection demonstrates that the fistula is supplied by the primitive trigeminal artery and drained into the basal vein of Rosenthal, with an associated venous varix. C, After coil embolization, anteroposterior view of the left vertebral artery injection demonstrates incomplete disconnection of the fistula by the coils. D, Follow-up angiogram obtained at 7 months shows spontaneous occlusion of the fistula with preserved patency of the basilar artery. E, Disappearance of the venous varix on follow-up T2-weighted MR imaging.

Discussion

BAVFs of the brain are characterized by an immediate AV transition without a capillary bed or “nidus” as occurs in BAVMs.²² BAVFs can result from trauma or may be congenital.^3,4 Congenital AVFs usually present in childhood (5 of 9 patients in our study were pediatric patients). The pathophysiologic mechanisms giving rise to these lesions is still not clear.^1,20,23 It is likely that a misstep in embryologic development of the cerebrovasculature produces these lesions. The connection between an arterial feeder directly into a solitary draining vein without any intervening tangle of vessels creates conditions for rapid high flow. The pathologic features of congenital BAVFs arise principally from its high-flow nature. Associated venous varices are produced by the high, turbulent flow from AV shunt surgery.^9,10,20,24 BAVFs can be asymptomatic or, more often, can cause increased intracranial pressure, seizures, cerebral hemorrhage, neurologic deficit, cardiac failure in neonates and infants, and intracranial bruit for which treatment is necessary.^5–8,10 They can also be part of a syndrome such as Klippel-Trenaunay-Weber or Rendu-Osler-Weber (hereditary hemorrhagic telangiectasia).^17,25–27 The risk for hemorrhage from BAVFs is not clear.⁸ Single-venous drainage and small size have been thought to contribute to the risk for BAVM hemorrhage,²⁸ both of which are characteristics of pial AVFs. However, it is not clear whether venous varices and venous drainage (superficial or deep) associated with pial AVFs are associated with an increased risk for hemorrhage.

Once the connection to the high-flow system is eliminated, so is the abnormality and any accompanying elements (such as venous varices). The preferred treatment of BAVF is interruption of the fistula or obliteration of all feeding vessels as close to the fistula as possible, while leaving the venous drainage intact.^2,3 Because there is no nidus, surgical clipping for disconnection of the AV shunt should eliminate the abnormality without the necessity for resection of the lesion.¹⁴ Removal of the varix is not attempted unless the malformation bleeds with a resultant hematoma, or the accessible varix produces a mass effect.²⁹ This has proved effective; however, sometimes this procedure is impossible because of the deep location and difficulty in exposure.³ In addition, as a result of the longstanding shunt, arterialization and thickening of the draining veins can occur, making identification of the exact fistula site more difficult. Lesions in deep and eloquent locations can be associated with a high surgical risk for neurologic morbidity. Also, deep hypothermic cardiopulmonary bypass will be needed to perform surgical resection of such technically difficult lesions.^29,30 With a surgical approach, it may also be difficult to localize the lesion intraoperatively because the fistula can be quite small and is not associated with a nidus or tangle of vessels to help in visual identification.

Endovascular applications have been reported as successful ways to disconnect AVFs with several different agents such as balloons, coils, glue, and Onyx.^{3,9,21,23,31–33} When the lesion is surgically risky, at a deep or inaccessible location, we use endovascular techniques because we find them to be safe and effective. Endovascular treatment can be implemented in stages, and it may reduce the risk for postoperative hemorrhage, possibly by preventing normal perfusion pressure breakthrough in high-flow lesions. Even a single venous channel has multiple arterial connections; therefore, it is possible to eliminate the AVF from a transarterial approach. In our series, patient 4 had 3 arterial connections, and he underwent transarterial embolization in 4 stages that resulted in complete obliteration of the fistula. Detachable coils are useful because they can be repositioned until a stable and safe position is obtained; therefore, distal embolization can be eliminated or minimized. In addition, they can act as a template for the deposition of other embolic materials, such as glue. The use of a high concentration of n-BCA or pure n-BCA in high-flow shunts for brain AVMs may occlude the fistula within seconds because the flow of n-BCA is, to some extent, unpredictable. Inadvertent migration of the glue into the draining veins may result in immediate hemorrhage by blocking venous outflow. We inserted detachable coils at the fistula site to decrease the flow and thereby facilitate the injection of n-BCA in patient 7.

Recently, the new liquid embolic agent Onyx has become available for embolization of brain AVMs. Onyx is nonadhesive and polymerizes slowly. Onyx is available in several concentrations, and the high-concentrated Onyx can be used to slowly occlude small AV shunts in a more controlled way than that achieved with n-BCA. However, a simple Onyx injection is not always feasible; in some very high-flow shunts, Onyx may migrate through the fistula into the distal draining veins. Adjuvant use of a microballoon to block the flow to enable gradual occlusion of the large high-flow shunts with Onyx has been reported.^21,32 We believe that this abrupt disconnection may result in hyperemia on evocation of the normal perfusion pressure breakthrough phenomenon.

The endovascular management of AVFs is challenging because of the high flow through the fistula and the large size of the afferent and efferent vessels. Hemodynamic derangements of the cerebral circulation predispose to edema, infarction, and hemorrhage in the brain after resection of the lesions.^34–36 Fortunately, we did not encounter this problem in the treatment of our 9 patients. In high-flow fistulas, we initially coiled them partially and the patient was observed. After 3 months, control angiography would be obtained. Spontaneous thrombosis will develop in some patients; if not, another embolization will be performed. Also, in our series, no morbidity or mortality occurred. If the embolization is too proximal to the AV connection, the fistula is only partially obliterated, or new arterial connections can be recruited with recurrence of the fistula.³ In general, we place the coils proximal to the fistula point. Although some authors suggest that the endovascular occlusion of the BAVF is difficult compared with placement of detachable platinum coils^14,17,21,37 and embolic agent deposits, we obtained good angiographic outcome in all patients. There are several reports of unsuccessful attempts at endovascular embolization of an AVF because of migration of the embolization agent into a varix; into the lung; or, most dangerously, into the draining vein or elsewhere in the cerebral vasculature.^3,21,37 In our series, there was no such event.

Regardless of the agent used, it is important to consider that a complete fistula cure may produce devastating complications from extensive thrombosis of the draining veins initially arterialized and a risk for venous infarction or hemorrhage. Therefore, the patients who presented with headaches after embolization were treated with intravenous heparin, aimed at achieving an activated clotting time of twice the normal value for 24 hours postoperatively, and then low-molecular-weight heparin at a preventive dose for 2 to 15 days until the headaches were alleviated.

Conclusions

From our experience and that of others, with the advent of recent endovascular techniques, a number of groups have been convinced of the application of endovascular therapies to treatment of BAVFs. Different types of high-flow AV shunts can safely be occluded with endovascular techniques tailored to the specific anatomic configuration of the shunt.