Transarterial embolization of anterior cranial fossa dural arteriovenous fistulas as a first-line approach: a retrospective single-center study

doi:10.21203/rs.3.rs-4946120/v1

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Transarterial embolization of anterior cranial fossa dural arteriovenous fistulas as a first-line approach: a retrospective single-center study

https://doi.org/10.21203/rs.3.rs-4946120/v1

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Background

Anterior cranial fossa (ACF) dural arteriovenous fistulas (DAVFs) present unique treatment challenges due to their complex angioarchitecture and high risk of hemorrhage. Recent advancements in endovascular techniques have highlighted the potential of transarterial embolization in managing these fistulas.

Objective

The purpose of this study is to evaluate the clinical and angiographic outcomes of transarterial embolization (TAE) as a first-line treatment for ACF DAVFs over a twenty-year period.

Methods

From March 2001 to September 2021, a total of 54 patients harboring ACF DAVFs underwent TAE as a first-line approach at our institution. The clinical presentation, angiographic features, procedure-related complications, clinical outcomes, and angiographic results were analyzed retrospectively.

Results

Among 54 ACF DAVF treated, there were 48 males and 6 females, with a mean age of 52.5 (52.5 ± 13.0) years. Intracranial hemorrhage (51.9%, 28/54) was the most common symptom. A total of 57 embolization attempts were performed. 83.3% achieved complete angiographic occlusion immediately post-TAE. The average hospital stay post-treatment was 10.4 days. Complications occurred in 3.7% of patients. 97.6% (41/42) experienced symptom improvement or stabilization during clinical follow-up. DSA follow-up showed that 85.0% (34/40) maintained complete fistula occlusion. Angiographic recurrence occurred in one (2.9%, 1/34,) patient without any symptoms.

Conclusions

TAE for ACF DAVFs demonstrates a high rate of complete occlusion with an acceptable safety profile. Further comparative studies with other treatment approaches are recommended to validate these findings.

Dural arteriovenous fistula

Anterior cranial base

Transarterial embolization

Outcomes

Complications

Anterior cranial fossa (ACF) dural arteriovenous fistulas (DAVFs) account for approximately 10% of all DAVF cases and are categorized as Borden type III and Cognard type III or IV due to the absence of large venous sinuses in the anterior fossa^1,2. These fistulas predominantly drain through the olfactory vein to the basal vein of Rosenthal or via ascending cortical veins to the superior sagittal sinus, resulting in an aggressive natural history with a high risk of hemorrhage. Intervention is recommended regardless of symptomatic presentation.

The management of ACF DAVFs is challenging due to the absence of standardized treatment protocols. Surgical interventions, such as resection via frontal craniotomy, carry significant risks, including paranasal sinus exposure, cerebrospinal fluid leakage, intradural infection, and potential damage to the frontal lobe and olfactory nerves^3,4. Although endovascular embolization is less invasive, it has been historically constrained by the risk of occluding the central retinal artery and the complexities of tortuous and fragile draining veins^5,6.

Recent advancements in endovascular techniques and instrumentation have improved the effectiveness of endovascular treatment (EVT) for DAVFs. As a result, EVT has become the preferred treatment approach in many specialized centers^7–9, mainly due to the successful application of transarterial and transvenous embolization techniques, which have achieved notable cure rates and positive clinical outcomes.

The purpose of this study is to detail the clinical and angiographic outcomes observed in patients with ACF DAVFs who received TAE as their initial treatment modality.

Study design

We retrospectively reviewed the DAVF database for all patients who underwent TAE as the primary intervention at our institution from March 2001 to September 2021. Patients who underwent stand-alone surgical ligation or TVE as the first-line treatment were excluded. The study included 54 patients and adhered to STROBE guidelines. The institution’s ethics committee provided a waiver for written informed consent from the participants. Figure 1 shows the study enrollment flow diagram.

Endovascular Procedure

Interventions were performed under general anesthesia and systemic heparinization. The most suitable feeding artery was used for TAE. Venous access was an alternative in cases of tortuous and thin feeding arteries, pre-existing blindness in the contralateral eye, incomplete occlusion after transarterial treatment, or failed transarterial catheterization. If EVT failed, clip ligation was used as a backup.

Occlusion of the fistulous point and venous collector was achieved via a transarterial approach utilizing nBCA (N-butyl 2-cyanoacrylate liquid embolic system) (Glubran; GEM SRL, Viareggio, Italy) or nonadhesive liquid embolic agents such as ethylene vinyl alcohol copolymer (Onyx, Medtronic, Irvine, USA). Embolic agent injection was only performed when the microcatheter was positioned distally to the origin of the central retinal artery, as close as possible to the fistulous zone, to avoid inadvertent embolization. In cases where the distal portion of the ethmoidal artery was tortuous or the angulation between the origin of the ophthalmic artery and the internal carotid artery (ICA) was acute, balloon-assisted catheterization was employed to facilitate superselective catheterization.

Occlusion of the fistulous point and venous collector was achieved via a transarterial approach using nBCA (N-butyl 2-cyanoacrylate) or nonadhesive liquid embolic agents like Onyx. If the microcatheter was not positioned distal to the origin of the central retinal artery, embolic agent injection was avoided. Balloon-assisted embolization was performed when the fistula was near the central retinal artery.

Data Collection and Follow-Up

All data were prospectively collected. The preoperative data included age, sex, clinical presentation, visual status, modified Rankin Scale (mRS) score, Cognard type, feeding arteries, and draining veins. Operative data focused on the vessels accessed, the types of embolic agents used, and any technical complications encountered. Postoperative assessments included angiographic results, any ensuing complications, changes in visual status, and mRS scores at the time of discharge and a 6-month follow-up. Angiographic follow-up was comprehensive, involving immediate post-treatment digital subtraction angiography (DSA) and a repeated DSA/MRA 6 months later. All visual examinations were conducted by independent ophthalmologists to ensure unbiased assessment.

Statistical analysis

Continuous variables were reported as mean and standard deviation, while categorical variables were represented as frequency and percentages.

Patient and DAVF baseline characteristics

Between 2001 and 2021, 54 patients with ACF DAVFs received EVT as first-line treatment at our center. The average age was 52.5 ± 13 years, with a predominant male representation of 88.8% (48/54). Notably, 29.6% (16/54) of these cases were either incidentally found in association with other diseases or presents as asymptomatic. The remaining 70.4% (38/54) of the patients exhibited symptoms, with hemorrhage being the most common symptomatic presentation (51.9%, 28/54), followed by non-hemorrhagic neurological deficits (NHNDs) and venous hypertensive symptoms (VHS). Multiple symptoms in a single patient were observed in 3.7% (2/54) of the cases. Before treatment, visual impairment was noted in 1.9% (1/54) of the patients. Before treatment, 26 patients (58.1%, 26/54) presented with an mRS score of 2 or higher.

Fistulas were classified as Cognard type III in 21 (38.9%) patients and type IV in 33 (61.1%) patients. Also, multiple feeders were observed in 41 (76.0%) patients. Thirty-fourth (63.0%) of fistulas received bilateral supply. Only one (1.9%, 1/54) ACF DAVF had no arterial supply from OA branch. The branches of OA involved predominantly included the anterior ethmoidal artery (AEA) in 90.0% (47/54) of cases, posterior ethmoidal artery in 3.7% (2/54), and anterior falx artery in 27.8% (15/54). The arterial supplies from middle meningeal artery (MMA) were 38.9% (21/54). Other arterial supplies included internal maxillary artery (27.8%, 15/54), pial arteries from the anterior cerebral artery (26.0%, 14/54) and the facial artery (5.6%, 3/54). Unsurprisingly, all cases demonstrated drainage via the frontal basal cortical veins. The most common drainage routes were through the frontal veins into the superior sagittal sinus (SSS), observed in 79.6% (43/54) of cases. Drainage via the olfactory vein to the cavernous sinus was noted in 14.8% (8/54), while the superficial and deep cerebral veins accounted for drainage in 24.1% (13/54) of cases. The superficial and deep cerebral veins specifically included the vein of Galen, the basal vein of Rosenthal, the vein of Trolard, and the superficial middle cerebral vein. A total of 55.6% (30/54) of the ACF DAVFs had drainage restrictions. The most frequent type of drainage restriction observed was narrowing at the junction between the cortical veins and the SSS (83.3%, 25/30), followed by occlusion at the junction (10.0%, 3/30) and SSS occlusion with drainage into deep cerebral veins (6.7%, 2/30). The baseline characteristics of these 54 patients are detailed in Table 1.

Table 1

Baseline characteristics of the 54 patients and anterior cranial base dural arteriovenous fistulas treated with EVT.
Variable		n (%)
Demographics
Total no. of patients		54
Age, years (mean ± SD)		52.5 ± 13
Male/female		48/6
Clinical presentation
Hemorrhage		28 (51.9)
NHND^†		2 (3.7)
VHS^‡		6 (11.1)
NHND and VHS		2 (3.7)
Asymptomatic		16 (29.6)
DAVF side
Rt		15 (27.8)
Lt		14 (25.9)
Midline		25 (46.3)
No. of feeders
One		13 (24.1)
Multiples		41 (75.9)
Arterial feeders^£
Ophthalmic artery		53 (98.1)
Anterior ethmoidal artery		47 (87.0)
Posterior ethmoidal artery		2 (3.7)
Anterior falx artery		15 (27.8)
Internal maxillary artery		15 (27.8)
Middle meningeal artery		21 (38.9)
Anterior cerebral artery		14 (25.9)
Facial artery		3 (5.6)
Venous drainage: frontal basal vein to
SSS		43 (79.6)
Cavernous sinus		8 (14.8)
Superficial and deep cerebral veins^¶		13 (24.1)
Cognard type
III		21 (38.9)
IV		33 (61.1)
Drainage restriction		30 (55.6)
SSS occlusion		3 (5.6)
Narrowing of the junction		25 (46.3)
Occlusion of the junction		2 (6.7)
Modified Rankin Scale score before TAE
≥ 2		26 (48.1)
† Non-hemorrhagic neurological deficitis (NHNDs) included deficits caused by venous hypertension such as: dementia, psychiatric symptoms, seizures, ataxia, sensory and motor deficits, aphasia/dysarthria, cranial nerve palsies (excluding cranial nerves III, IV and VI) and hydrocephalus. ‡ Venous hyperdynamic symptoms (VHS) included symptoms that were caused by increased blood flow such as: tinnitus, bruits, chemosis/proptosis, ophthalmoplegia/ diplopia and isolated headache not attributable to hemorrhage. £ One DAVF might have multiple arterial feeders. ¶ There might be several drainage veins in a DAVF. The superficial and deep cerebral veins mainly referred to the vein of Galen, the basal vein of Rosenthal, the vein of Trolard, the superficial middle cerebral vein.

Treatment Characteristics

Fifty-four patients received a total of fifty-seven EVT treatments, with three of them receiving it twice. The OA (86%, 49/57) was the most frequently attempted access, followed by the MMA (15.8%, 9/57) and the internal maxillary artery (10.5%, 6/57) (Figs. 2 and 3). The detailed outcomes of TAE on the 54 patients are summarized in Table 2.

Table 2

Characteristics and outcomes of transarterial embolization for 54 anterior with 57 embolization attempts
Variable		n (%)
Attempted embolization		57
Embolized artery
Ophthalmic artery		49 (86.0)
Middle meningeal artery		9 (15.8)
Internal maxillary artery		6 (10.5)
Embolic agent
Onxy-18		57 (100)
Onxy-34		4 (7.0)
nBCA		5 (8.8)
Coils		2 (3.5)
Mean vol of embolic agent injected per pedicle in ml (range)		5.3 (2.3-8.0)
Balloon-assisted microcatheterization		10 (18.5)
Immediate angiographic result*
Complete occlusion		46 (85.2)
Partial occlusion		8 (14.8)
Immediate clinical result*
no change		41 (75.9)
improvement		11 (20.4)
worsening		2 (3.7)
Complications*
Retinal ischemia		1 (1.8)
Cerebral ischemia		0 (0)
Subarachnoid hemorrhage		1 (1.8)
DSA follow-up period, months (median (IQR))		6.7 (1–36.8)
DSA follow-up^†
Complete occlusion		25 (83.9)
Stabilization		4 (12.9)
Progression		1 (3.2)
Recurrence		1 (3.2)
MRA follow-up period, months (median (IQR))		6.2 (1.2–32.4)
MRA/CTA follow-up^§
Complete occlusion		9 (100)
Recurrence		0 (0)
Clinical follow-up^‡
Asymptomatic		35 (83.3)
Improvement of symptoms		6 (14.3)
Worsening of symptoms		1 (2.4)
Death		0 (0)
Modified Rankin Scale score^‡
≥ 2		16 (38.1)
Values are presented as number (%), unless indicated otherwise. * Based on the total number of patients (n = 54). † Based on 31 (31/54, 57.4%) patients with DSA follow-up § Based on 9 (9/54, 16.7%) patients with MRA/CTA follow-up ‡ Based on 42 (42/54, 77.7%) patients with clinical follow-up

Complete immediate angiographic occlusion was achieved in 85.2% (46/54) of patients. In patients with partial embolization (14.8%, 8/54), one patient was referred for surgery, while the rest were managed conservatively with vigilant observation. One of the fistulas spontaneously occluded in the third month after partial embolization. Onyx-18 was the most frequently used agent (100%, 57/57), followed by nBCA (%,5/57), Onyx-34 (%, 4/57) and colis (%, 2/57). Balloon-assisted microcatheterization was performed on 10 (18.5%) patients (Fig. 3).

A total of 98.1% (52/54) of the patients who received TAE experienced immediate improvement or no change in symptoms. Complications arising after the procedure were observed in two (3.7%) patients. One patient (1.9%, 1/54) experienced retinal ischemia after TAE via the branches of the OA. In the other patient with sudden onset mild headache because of acute intraparenchymal hemorrhage with an associated ACF DAVF, a transarterial attempt via OA was complicated by subarachnoid hemorrhage due to intraoperative perforation. Surgical interruption of the shunt was performed immediately.

Follow-up

A total of 40 (40/54, 74.1%) patients had at least one DSA or MRA follow-up. The DSA follow-up periods (months, median, IQR) were 6.7 (1–36.8) mouths. Thirty-four (85.0%) DAVFs were totally occluded. One patient (2.5%) experienced angiographic recurrence, with stable condition compared to baseline neurological status whose early angiography had been judged to be totally occluded. Among 54 patients, 42 (90.0%) were followed-up either as inpatients, outpatients, or by telephone. Only one patient (2.4%, 1/42) reported worsening symptoms as a result of retinal ischemia following TAE, as previously mentioned. When the patient was discharged, he could not see anything within 1 meter. He was advised to visit the ophthalmology clinic. At the recent follow-up performed by telephone (36 months after the embolization), the vision in his right eye only returned to counting fingers within 50 centimeters. Regarding the patient with intraoperative microperforation, although the headache was relatively severe and persistent on the first postoperative day, it gradually disappeared on the fifth postoperative day, and no analogous symptom onset was observed during follow-up.

In our facility, TAE is the first-line treatment for the ACF DAVF. The OA and MMA are the predominant arterial access routes for embolization. Surgical ligation is as a salvage treatment. Based on our experience, the incidences of neurological and visual complications following TAE are notably low. Follow-up assessments using DSA or MRA reveal that a substantial majority of patients achieve angiographic cure post-TAE.

The location of the fistulous connection is typically at the level of the cribriform plate, either off-midline or centrally situated, within the lateral epidural compartment adjacent to the lamina cribrosa and the orbital roof. Given the absence of a dural sinus in the anterior cranial fossa, venous drainage is facilitated by fragile, dilated pial veins within the frontal sulci, leading to the proximal sinuses. This altered venous drainage pattern, with increased reliance on cortical veins, may contribute to venous engorgement and the associated risk of intracranial hemorrhage¹⁰. In our study, the trend towards a predisposition for intracranial hemorrhage was observed, although previous series revealed that it was heterogeneous^8,11,12.

The understanding of DAVF angioarchitecture is crucial for successful embolization. In our patient cohort, the AEA was the primary arterial feeder in 90.0% (47/54) of cases, consistent with Xu et al.’s findings of 93% AEA involvement in their study². The AEA shows significant variability in origin and trajectory, further complicated by contributions from the frontal branch of the middle meningeal artery (20% of cases) and the septal branch of the sphenopalatine artery, with anastomoses to the anterior and posterior ethmoidal arteries (20–60% of cases)^13–15. This diversity explains the variable angioarchitecture of ACF DAVFs.

The efficacy of EVT for ACF DAVFs is debated, with previous studies reporting low occlusion rates. Gross et al. found an overall endovascular occlusion rate of 22%, with only 1 of 8 transarterial embolizations achieving complete occlusion¹³. This may be due to the challenges of delivering embolic agents effectively. A meta-analysis of five studies with 81 patients showed complete obliteration in 100% of surgical cases, compared to 47% following embolization¹². These findings highlight the complexity and risks of EVT, questioning its suitability as a primary treatment for ACF DAVFs.

Advancements in neurointerventional techniques have made TAE a viable option for ACF DAVFs. Su et al. reported a single-center study where TAE was the first-line treatment in 40 patients, achieving an 82.5% immediate complete angiographic cure rate with one complication and no recurrences⁹. Similarly, Trivelato et al. documented endovascular embolization as the primary treatment in 35 ACF DAVFs, achieving 84.2% complete occlusion in cases treated exclusively with the transarterial approach, despite complications in 8.7% of procedures⁸. Our results are consistent, with a slightly higher immediate complete occlusion rate and a 3.7% complication rate, similar to other studies reporting 0–17%. However, publication bias, underreporting, and small sample sizes may underestimate the complication risks, particularly vision loss from central retinal artery occlusion during trans-ophthalmic artery embolization.

From the transarterial approach, superselective microcatheterization and embolization via the ophthalmic artery present risks such as arterial dissection or inadvertent reflux/embolization into the central retinal artery, potentially leading to monocular blindness. However, it should be noted that the incidence of permanent vision loss is likely to be very low, with no reported cases to date. Nonetheless, the potential for publication bias, underreporting, and limitations inherent in small series might lead to an underestimation of the risk of vision loss associated with trans-ophthalmic artery embolization. Additionally, challenges such as cranial neuropathy in cases where embolization is performed through MMA or internal maxillary artery, and difficulties in delivering embolic agents through tortuous arteries, continue to pose significant challenges in TAE treatments^3,16,17.

The utilization of specialized balloon microcatheters in TAE procedures can play a significant role in facilitating superselective catheterization and mitigating the risk of embolysate reflux into the ophthalmic artery and its branches^7,18. Additionally, these balloons can be strategically deployed to temporarily occlude the internal carotid artery distal to the ophthalmic artery origin⁸. This technique is particularly useful given that the ophthalmic artery often originates from the internal carotid artery at an acute angle, which can complicate catheter navigation. In our series, balloon-assisted microcatheterization was employed in 35.4% of embolization attempts. Notably, we observed no incidences of central retinal artery occlusion or embolization failures due to the inability to access the targeted arterial feeder using this method.

The advancement of newer generation distal access guide catheters, which facilitate navigation through the dural sinuses to the anterior aspect of the superior sagittal sinus (SSS), has broadened the therapeutic options for DAVFs beyond TAE^3,6. Transvenous embolization (TVE) has emerged as a significant alternative for the primary treatment of DAVFs. This approach is particularly appealing for avoiding ophthalmic artery catheterization and its associated risk of retinal ischemia and may also serve as a secondary option in cases where TAE is unsuccessful. Although some studies suggest TVE may be superior to TAE as a first-line strategy for ACF DAVFs, we did not employ TVE in our series. The challenges associated with navigating through the long distances of the SSS and small, tortuous cortical veins, often presenting with venopathy, deterred its use. Such navigation and manipulation with microcatheters and microwires can lead to vessel rupture, posing substantial risk^8,19. Additionally, factors like venous drainage directions other than to the SSS, the presence of venous aneurysms, and drainage restrictions further limit the feasibility of TVE. Therefore, in our study, we did not employ TVE, even when it appeared technically possible.

It is well known that DAVFs cure requires complete penetration of the fistulous point and draining vein (or common venous outlet). However, there was one case of recurrence in our series despite seemingly adequate venous penetration. Although the mechanism of recurrence is not addressed at present, it is generally accepted to be related to suboptimal casting of the draining vein²⁰. Ambekar et al²¹. presented the first large series explicitly aimed at identifying features predictive of recurrence in endovascular-treated lesions only. Of the 58 patients treated at their institution (CCFs excluded), they limited the analysis to the 26 patients who underwent endovascular embolization with Onyx, 21 of whom had angiographic follow-up. Three patients (14.3%) experienced recurrence. In 1 case, the authors found on rereviewing the initial treatment angiogram that there was not, in fact, complete penetration of the common venous outlet. For the other 2 patients, the authors suggested that there may have been a patent channel within the Onyx cast—given that the agent precipitates in a radial fashion from outward to inward—that permitted recurrence in a delayed fashion. In other words, this highlights the notion that an initial angiographic cure may merely be temporary angiographic nonopacification of the DAVF (due to stagnant flow and a partial cast in the fistula/venous outlet). Subsequent meningeal recruitment can then expand a small residual dAVF²². In addition, previous studies have indicated that Borden type III lesions treated endovascularly (as opposed to surgically) were significantly more likely to experience recurrence²⁰. Therefore, long-term control angiography is mandatory.

Limitation

This was a single-center, retrospective study. It has the inherent limitations of self-report bias and no core laboratory adjudication. Some (65%) patients were followed up with imaging, while only 45% were followed up with DSA, which may, to some extent, understate the recurrence rate of DAVFs. The number of surgery patients was also insufficient to compare the various treatment modalities.

Our experience suggests that TAE treatment for ACF DAVFs has an acceptable safety profile with high rates of complete occlusion, providing a reasonable alternative to surgical ligation and TVE. Further study is needed to compare these different treatment modalities.

Author contributions Conception and design Conception and design: QL, JL. Acquisition of data: GZ, DG, MP, RC, CS, XD, YZ. Drafting the article: GZ. Critically revising the article: YX, QL, QH. All the authors have read and approved the final manuscript.

Funding This research was supported by 234 Discipline Peak Climbing Program of Changhai Hospital (2020YXK033); Project from Shanghai Science and Technology Commission (23Y11906700); Shanghai Shenkang Three-year Action Plan Major Clinical Research Project (SHDC2023CRT007).

Data availability The data are available from the corresponding author on reasonable request.

Acknowledgements Not applicable.

Conflict of interest statement The authors declare that they have no competing interests.

Ethics approval The study was conducted in accordance with the STROBE guidelines. The ethics committee waived the need for written informed consent from the participants.

Declarations Conflict of interests None.

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Transarterial embolization of anterior cranial fossa dural arteriovenous fistulas as a first-line approach: a retrospective single-center study

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