Transcranial Endovascular Embolization of Dural Arteriovenous Fistula: A Case Report and Literature Review

The optimal endovascular management of high-grade dural arterial-venous fistulae (dAVF) can be technically challenging in cases where the involved venous sinus segment is inaccessible through the traditional percutaneous approach. In this report, we describe our experience with the transcranial endovascular approach for the treatment of a high-grade dAVF. We also provide a literature review of other reports of transcranial endovascular dAVF embolization. We propose that transcranial endovascular embolization of high-grade dAVF appears to be safe and effective in cases where the fistula is inaccessible to percutaneous routes alone.


Introduction
Intracranial dAVF are abnormal connections between arteries and dural sinuses or veins within the dural leaflets [1].They are commonly graded based on the Borden and Cognard classification schemes [2,3].Lowgrade fistulae can be incidental but should be monitored clinically as they occasionally undergo grade-up conversion [4].Fistulae are characterized as high-grade when they develop cortical venous drainage (CVD) due to venous hypertension and sinus outflow obstruction [1][2][3].High-grade fistulae can cause intracranial hemorrhage or significant non-hemorrhagic neurologic deficits (NHND) due to venous hypertension with resultant cerebral edema [1].High-grade fistulae have an annual rupture rate of 15-35%; thus, they require treatment [4].
The first line of treatment for symptomatic high-grade dAVF is endovascular embolization [4][5][6].This can be done through trans-arterial embolization (TAE), trans-venous embolization (TVE), or a combination of both.The goal of therapy is to completely obliterate the fistula to correct venous shunting [5,6].In TAE, a microcatheter is navigated into the feeding arteries, and embolic material is injected with the goal of occluding the distal feeding arteries with penetration of the fistulous point in the draining vein or sinus [5,6].This is challenging to accomplish in cases that have multiple fistulous points, feeding arteries that have extensive complex collateralization, arteries that supply eloquent territories, or inaccessible arteries due to tortuous or small-caliber vessels [5,6].If not completely obliterated, dAVF can recur by drawing alternative feeder arteries via angiogenesis and dAVF-inducing factors [5,6].The goal of TVE is complete occlusion of the draining sinus segment that is involved in the dAVF [4][5][6].This will result in the complete obliteration of all fistulous points.Unfortunately, TVE is not always feasible, as the involved sinus segment can be challenging to access due to stenosis or venous sinus occlusion that occurs due to rapid arterial flow into the sinus from the fistula [6].In these cases, alternative access to the fistula can be considered, such as a craniotomy for direct transcranial endovascular access.

Case Presentation
A patient in their 60s presented to our facility with diplopia left homonymous hemianopia and severe headaches.The computed tomography head (CTH) showed a right occipito-temporal hemorrhage with surrounding vasogenic edema (Figure 1).Computed tomography angiography (CTA) identified dilated right hemispheric cortical veins with occlusion of the medial right transverse sinus and the right jugular bulb.A diagnostic cerebral angiogram identified bilateral indirect carotid-cavernous (CC) fistulae with retrograde drainage via the left superior ophthalmic vein (SOV) and a Cognard type IIa+b right sigmoid dAVF with multiple arterial feeders coming from branches of the right external carotid artery.Due to the occlusion of the medial right transverse sinus and right jugular bulb, there was extensive CVD.The superior sagittal sinus (SSS) drains via the left transverse and sigmoid sinuses.Percutaneous transvenous endovascular access was unsuccessful via the right internal jugular vein (IJV) due to occlusion at the jugular bulb and via the contralateral left IJV and left transverse sinus due to occlusion at the right medial transverse sinus.The patient underwent TAE of the major feeding arteries with penetration of the right sigmoid sinus.Due to the tortuous and small-caliber feeding arteries, it was difficult to penetrate all fistulous connections.TAE resulted in diminished shunting without fistulous occlusion and a reduction in ecstatically draining veins.The patient's headaches improved, but visual symptoms continued.
Five months later, he developed right-sided pulsatile tinnitus, left ocular proptosis with chemosis, and left cranial nerve (CN) 6 palsy.Repeat angiograms demonstrated recruitment of the right sigmoid dAVF from the right occipital artery and increased shunting at the left CC fistula through the right SOV.Since he failed TAE and the right sigmoid sinus was isolated and inaccessible through the percutaneous route for TVE, we decided to proceed with craniectomy for transcranial endovascular embolization.
The patient was taken to the OR and placed in a prone position with palms facing up (Figure 2).The Stealth neuronavigation system was used to locate the right transverse sinus relative to the sigmoid sinus and torcula.A transverse incision was made over the right transverse sinus.A 3-4 cm craniectomy was performed to expose the right transverse sinus.Two mobile C-arm fluoroscopy units were brought in for angiography.The right wrist was prepped, and the right radial artery was accessed with an introducer sheath.A glide catheter was navigated over a glide wire into the right common carotid artery for angiography.The transverse sinus was surgically opened, and we dissected laterally until some of the obstruction was freed.
We then penetrated through it with a Rhoton 6 dissector and subsequently advanced a short 4-French sheath.The sheath was tunneled into the sigmoid sinus under fluoroscopic roadmap guidance, and a muscle flap was sutured to control bleeding around the sheath.The sheath was then sutured to the skin edge and connected to a rotating hemostat valve.Under roadmap guidance, a microcatheter was navigated caudally into the sigmoid sinus.The sinus was embolized with platinum coils and Onyx 34 until there was a complete occlusion of the fistula (Figure 3).The dura along the superior aspect of the transverse sinus overlying the tentorium was then skeletonized.The open transverse sinus was packed with Surgicel, and a small piece of muscle harvest was sutured over to minimize the risk of venous bleeding.Cranioplasty was performed, and the wound was closed.The patient was then taken to the angiography suite for treatment of the CC fistula.Drainage of the left CC fistula had remodeled due to a new occlusion of the left SOV and was rerouted via superficial cortical and deep veins.We performed percutaneous TVE of the bilateral CC fistulae, resulting in complete occlusion.After achieving complete occlusion of the multiple fistulas, a new left sigmoid sinus Cognard type I dAVF was visualized.
The patient's postoperative course was uncomplicated.He was discharged home in stable condition three days post-operatively.He had a complete resolution of symptoms at follow-up two weeks after discharge.At 12 months postoperatively, he was doing well clinically without any recurrence or new symptoms.He was offered a repeat follow-up angiogram but declined.

Discussion
Transcranial endovascular embolization for dAVF is an uncommon procedure that has been described infrequently in the literature.Due to high venous output-induced veno-occlusive venopathy, percutaneous TVE can be difficult.TAE is an option in such cases; however, it can be difficult to achieve complete obliteration in cases with multiple complex arterial feeders.Failure to achieve complete obliteration can result in re-vascularization of the fistula, with continued risk for serious neurological consequences [4][5][6].The use of flow-diverting stents has been debunked in the treatment of DAVF and results in recanalization and recruitment.
Our institution does not have a hybrid operating room (OR) angiosuite, so we performed the transcranial TVE with two mobile C-arms in the OR.This was beneficial because our neurosurgeon had access to his tools if he needed to surgically intervene.The downsides to using a mobile C-arm in the OR are poor image quality and slow frame rates.We found this set-up acceptable since the mobile C-arm could perform digital subtraction angiography and create a road map.
We decided to treat the right sigmoid sinus dAVF before the bilateral CC fistula because some of the drainage of the right sigmoid sinus dAVF was via medullary veins, which ultimately drained into the right cavernous sinus.Occluding the CC fistula first would have carried an elevated risk of increasing right hemispheric venous pressure and re-rupturing the right sigmoid dAVF.
It is crucial to re-evaluate the vascular drainage of the brain in the setting of multiple cranial fistulae after treating a single fistula.In our patient, the left SOV and left inferior petrosal sinus (IPS) had occluded, which resulted in retrograde cortical venous drainage and thus grade-up conversion of the bilateral CC fistula.It is unclear what resulted in the occlusion of the left SOV; however, consideration was given to the prone positioning during transcranial embolization.Regardless, we recommend that repeat angiography be performed after treating multiple complex dAVFs to confirm cure and reevaluate flow dynamics.
In our review of the literature, we found 23 publications detailing 61 cases of combined transcranial endovascular embolization of dAVF (Table 1) .Forty-five of the 61 cases had an angiographic cure; however, not all cases had long-term follow-up.Twelve of the 61 cases reported complications, which ranged from recurrence of symptoms to death.The technical approaches varied significantly between the authors.Combined neurosurgery and endovascular approaches to intracranial vascular malformations became known after Mickle et al. published "transtorcular embolization of the Vein of Galen Aneurysm" in 1986 [30].Since then, their technique has been modified and used for the combined transcranial endovascular treatment of complex intracranial dAVF.

Year
Barnwell et al. published their experience with the management of complex intracranial dAVF [7].They described 15 patients with dAVF who failed to respond or had lesions that were inaccessible to conventional approaches.The combination therapy they performed included craniotomies with transcranial TVE (nine patients), craniotomies with transcranial TAE (two patients), and open surgical resection (four patients).In the transcranial TVE subgroup, 7 of 9 patients achieved post-op angiographic cure.Clinically, four patients in this subgroup suffered complications.One patient developed transient coma related to embolic material flowing into the ponto-mesencephalic vein and post-operative venous sinus thrombosis.This patient recovered from anticoagulation use.Another patient in this group developed communicating hydrocephalus that required shunting.One of the patients required a repeat procedure for a cure.Their study included two patients in the series who underwent craniotomies for transcranial TAE.One of the patients in the TAE subgroup had a fistulous recurrence.The authors concluded that surgical exposure to allow for intracranial endovascular access in select cases is safe and effective.
Kasai et al. published a report of an 80-year-old male who presented with seizures and was found to have a dAVF [8].There was a thrombus on the distal and proximal ends of the draining fistula, which prevented TVE.TAE was attempted but did not result in a cure.They performed transcranial endovascular embolization.Good clinical and angiographic outcomes were reported after two years of post-treatment follow-up.Cases with similar circumstances were reported by Zink et al. and Bruneau et al. [9,10].In the report by Zink et al., the patient developed hydrocephalus, requiring an extra-ventricular drain immediately after removing the vascular sheath used for embolization.However, the patient reportedly had a good clinical outcome at six months post-treatment.
Pierot et al. reported a case of dAVF of the superior sagittal sinus (SSS) with venous sinus thrombosis of the posterior aspect of the SSS who presented with a coma following a lumbar puncture [11].They attempted TAE with transient symptom improvement, but the fistula remained and developed extensive arterial collateralization.Surgical sinus skeletonization was attempted without success.They proceeded with a combined surgical and endovascular treatment.The patient was taken to the operating room (OR) for exposure to the SSS with a burr hole and cannulization.The patient was then transferred, while under general anesthesia, to the angiography suite for embolization.A post-operative angiogram demonstrated complete occlusion one month later.The patient had an incomplete recovery of his symptoms and suddenly died months after the operation from a suspected pulmonary embolism.
Kuwayama et al. reported a case of CC fistula that couldn't be treated via standard measures [12].The patient underwent craniotomy with cannulation of an arterialized sylvian vein for endovascular embolization.The patient had symptom improvement and an angiographic cure by postoperative day two.[17].They reported an angiographic cure of the fistula at five weeks post-embolization angiogram.
Goto et al. published their reports of combined endovascular and surgical treatment of dAVF in 17 patients [18].They provided a detailed treatment protocol that they followed.They would first perform TAE, followed by TVE, within a few days.If transfemoral TVE was not possible, then they performed transcranial TVE.If the fistula persisted after TAE and TVE with venous reflux, then they proceeded with surgical isolation or resection.Twelve of the 17 patients included in the series underwent intraoperative embolization.Five of the 12 patients had angiographic cures.However, seven of the 12 patients went on to need surgical treatment.Of the five patients who had an angiographic cure with intraoperative embolization, two had persistence of their presenting neurologic deficit at follow-up six and eight years post-treatment.
Houdart et al. published their case series of 10 patients who underwent transcranial endovascular embolization, including their technical recommendations [19].In their first case, they attempted to catheterize the sinus in the OR immediately after craniectomy; however, this was complicated by a subdural hematoma (SDH).Thus, the other nine patients performed venous sinus catheterization one week postcraniectomy in the angiography suite.They had to take seven of their patients back to the OR for enlargement of the craniectomy site.The authors suggested that the craniectomy should expose 5-8 cm of the underlying sinus to make the catheterization straightforward.At three-month follow-ups, five patients had normal neurological examinations, and five patients had symptom improvement.
Shen et al. published their case of a patient with a cerebellar dAVF that was drained by the periclival plexus [20].They performed the procedure in a hybrid OR that was equipped with a robotic angiographic fluoroscopy system.They performed a pterional craniotomy with dissection of the sylvian fissure and direct catheterization of a small vein draining into the periclival venous plexus, which was used for TVE.They reported an angiographic cure for the fistula, and the patient had a good clinical recovery.
Cowie et al. published their experience with two cases [21].In one case, they performed a two-stage procedure with a burr hole made with a beveled anterior edge, followed by a micropuncture technique to insert a four-French endovascular sheath.A fenestrated titanium plate was screwed into place with the endovascular sheath exiting through the fenestration, and the scalp was sutured closed.Afterward, the patient was transferred to the angiogram suite for transcranial embolization, and the endovascular sheath was removed after completion of the procedure in the angio suite.In their other case, they performed a single-stage procedure completely in the angiography suite.Fluoroscopy was used to identify the draining right transverse sinus, and a burr hole was made so that a Camino small-bore cranial access device could be placed.A peripheral venous catheter was inserted through the lumen of the Camino device, and a microcatheter was advanced for transcranial embolization.Both patients reportedly did well without complications.
White et al. reported a successful case of transcranial endovascular embolization of a dAVF along the sphenoid ridge using a novel approach.Instead of a full-thickness craniotomy, they decorticated the outer cortex overlying a calvarial diploic vein, which was then cannulated for TVE.This technique resulted in an angiographic cure, with the patient remaining clinically well at 20 months post-embolization [22].

Conclusions
Our literature review shows that the transcranial embolization procedure has been infrequently performed over the past 30 years.Based on our experience and review, transcranial endovascular embolization appears to be feasible and likely safe.The true risks of the procedure are unknown since all published reports in the literature were just single cases or small case series.More research is needed to determine the optimal and safest way to perform combined transcranial endovascular embolization.More efforts in equipment design should be made to develop technologies specifically for transcranial endovascular embolization.Advances in research and technology in combined open surgical and endovascular techniques could extend the reach of endovascular neurosurgery and give options to patients with "untreatable" lesions.Transcranial TVE of dural arteriovenous fistulas is occasionally necessary for the treatment of complex dAVF.This appears to be a reasonable and feasible approach to the management of high-grade dAVF that cannot be adequately treated through the traditional percutaneous route.
have declared that they have no financial relationships at present or within the previous three years with any organizations that might have an interest in the submitted work.Other relationships: This research was supported (in whole or in part) by HCA Healthcare and/or an HCA Healthcare affiliated entity.The views expressed in this publication represent those of the authors and do not necessarily represent the official views of HCA healthcare or any of its affiliated entities.

FIGURE 1 :
FIGURE 1: Selected initial neuroimaging A) Computed tomography head demonstrating right occipital hemorrhage with vasogenic edema.B) Computed tomography and angiography demonstrate a filling defect in the medial right transverse sinus and prominent cortical veins, which could be suggestive of underlying DAVF.C) Digital subtraction angiography demonstrating right transverse dAVF with cortical venous drainage.

FIGURE 2 :
FIGURE 2: Craniotomy planning and incision A) Incision planning of the right transverse.B) Positioning with the right wrist exposed for angiography.C) Intraoperative set-up with endovascular sheath in the right transverse sinus.

1 .TABLE 1 :
TAE + surgery in 15 patients.Surgery included: 1. exposure of intracranial draining veins for TVE (9), 2. Exposure of intracranial feeding arteries to allow TAE (2) or 3. surgical resection (4) For combined TVE: post op angiographic cure in 7/9 patients.TAE 1 with return of fistula.TVE group 1 patient with hydrocephalus, 1 patient with repeat procedure, 1 patient developed venous sinus thrombosis and coma, 1 patient return of bruit but reported all doing well clinically.Combined TAE group with both with return of bruit.Surgical resection group with 1 Suboccipital craniotomy with intra-op cannulation of posterior fossa vein with TVE 2. Craniotomy exposed 2 branches of middle meningeal artery which were cannulated and performed TAE region in front the SSS which was cannulated in OR and patient transferred to angio suite under anesthesia for patient's clinical status was seen in weeks after embolization.Patient died suddenly a few months which was assumed to be due to pulmonary embolism craniectomy with clipping and puncture of superficial sylvian vein.Catheter Immediate angiogram with no more filling of dAVF.Follow-up angiogram 5 years later with Symptom improvement and recovery 2024 Abu-Alya et al.Cureus 16(7): e65032.DOI 10.7759/cureus.lefttransverse sinus.Craniectomy exposed sinus and the distal portion of the DAVF.Then the patient was moved to the angiography suite under the same anesthesia and placed in supine position.Using fluoroscopic guidance and road mapping the transverse sinus was punctured for TVE.neuronavigation and indocyanine green angiography, direct access of left transverse Immediate angio with cortical reflux reduced to 1 small Improvement visual symptoms POD#1.No neurologic deficits 3 2024 Abu-Alya et al.Cureus 16(7): e65032.DOI 10.7759/cureus.2stage procedure: Burr hole placed overlying sinus with cannulation.Endovascular sheath was held in place with a fenestrated titanium burr hole cover and suture, was taken to angio suite and had TVE then sheath removed.Patient 2 had burr hole in angio suite and Camino device inserted which the TVE was performed through cure reported good outcome for both patients at 3 month followthe TS-SS junction.TCD was used to identify the location of the sinus that was catheterized.Under fluoroscopy in the OR TVE was right external carotid angiography and doppler-flometry, arterialized SMCV isolated and catheterized.C-arm fluoroscopy and right ECAG was to guide the micro catheter that was advanced into the cavernous sinus for Angio suite.Angio left external carotid used to visualize and used to guide access.Drilled used to decorticate the outer cortex to expose diploic vein that was to exposure of arterial sylvian vein was punctured and the CV was catheterized for TVE under fluoroscopic guidance in the OR.After coiling surgical cauterization of the superficial sylvian vein, temporo-polar vein and medial sphenoparietal sinus was performed over MMA and 4F sheath placed.Selective angiography of MMA and micro catheter navigated to fistula Immediate complete immediate post-operative at 2024 Abu-Alya et al.Cureus 16(7): e65032.DOI 10.7759/cureus.Details from prior published case reports M: male, F: female, ICH: intracranial hemorrhage, dAVF: dural arteriovenous fistula, CS: cavernous sinus, SS: straight sinus, TS: transverse sinus, TV-SS: transverse-sigmoid sinus, SSS: superior sagittal sinus, MMA: middle meningeal artery, DSA: digital subtraction angiography, TAE: transartial embolization, TVE: transvenous embolization, MRI: magnetic resonance imaging.
Benndorf et al., Hurley et al., Chaudhary et al., and Fioravanti et al. reported similar cases with good longterm outcomes [13-16].Akamatsu et al. presented a similar case in 2017 that was performed at the junction of an emergency hematoma evacuation in the OR using a mobile C-arm fluoroscopy