Surgical management of superior petrosal sinus dural arteriovenous fistulae with dominant internal carotid artery supply

Abstract

Background

While technological advances have improved the efficacy of endovascular techniques for tentorial dural arteriovenous fistulae (DAVF), superior petrosal sinus (SPS) DAVF with dominant internal carotid artery (ICA) supply frequently require surgical intervention to achieve a definitive cure.

Methods

To compare the angiographic and clinical outcomes of endovascular and surgical interventions in patients with SPS DAVF, the records of all patients with tentorial DAVF from August 2010 to November 2015 were reviewed.

Results

Within this cohort, eight patients with nine SPS DAVF were eligible for evaluation. Five DAVF were initially treated with endovascular embolization, while four underwent surgical occlusion without embolization. Of the SPS DAVF treated with embolization, two (40%) remained occluded on follow-up, while the remaining three (60%) persisted/recurred and required surgical intervention for definitive closure. Of the four SPS DAVF treated with primary surgical occlusion, all four (100%) remained closed on follow-up. In addition, of the three SPS DAVF that persisted/recurred following embolization and required subsequent surgical closure, all three (100%) remained occluded on follow-up. Two (100%) SPS DAVF that were successfully treated with embolization had major or minor external carotid artery supply, while the three (100%) persistent lesions had major ICA supply via the meningohypophyseal trunk (MHT). Three (75%) of the four SPS DAVF treated with primary surgical occlusion had dominant MHT supply.

Conclusion

Complete endovascular closure of SPS DAVF with dominant ICA supply via the MHT may be difficult to achieve, while upfront surgical intervention is associated with a high rate of complete occlusion.

Introduction

Intracranial dural arteriovenous fistulae (DAVF) consist of abnormal connections between dural-based feeding arteries and venous sinuses with the focus of arteriovenous shunting contained within dural leaflets associated with the affected venous sinus. Whereas intracranial arteriovenous malformations (AVMs) can be surgically cured with resection of the vascular nidus, DAVF can often be treated with simple disconnection or occlusion of the draining vein(s) from the point of arteriovenous shunting without need for nidus/fistula pouch resection.^1–3 With advances in endovascular technology, transarterial and transvenous embolization with microcoils and/or liquid embolic agents have emerged as a treatment option for many DAVF.

Tentorial DAVF are rare lesions that have a more dangerous natural history, as they often possess high-risk angiographic characteristics including retrograde subarachnoid venous drainage and venous ectasia.² Lifetime hemorrhage rates ranging from 58% to 74% have been reported.^2,4 Unlike other intracranial DAVF, tentorial DAVF typically have both internal carotid artery (ICA) and external carotid artery (ECA) supply and often drain exclusively into subarachnoid veins, features that often render endovascular therapy challenging. Superior petrosal sinus (SPS) DAVF represent a subset of tentorial DAVF that are located at the petrotentorial junction and often have predominant ICA supply from the meningohypophyseal trunk (MHT) with venous drainage into the petrosal vein, lateral mesencephalic vein, basal vein of Rosenthal, or cerebellar hemispheric veins.³ Given the angio-architectural features of SPS DAVF, the ideal management strategy for these lesions is a topic of debate. In this report, we describe our experience with the endovascular and surgical management of SPS DAVF, with a particular emphasis on the influence of ICA supply on outcomes.

Methods

We performed an observational, retrospective, single-center study to assess the angiographic and clinical outcomes of endovascular and surgical interventions in patients with SPS DAVF. Following institutional review board approval at Massachusetts General Hospital (MGH), the records of 18 patients with 20 tentorial DAVF evaluated between August 2010 and December 2015 were retrospectively reviewed. Of the 20 DAVF reviewed, eight patients had nine SPS DAVF, as delineated by the Lawton-Halbach classification (Table 1).³ One patient with a small Cognard IIa SPS DAVF was managed without intervention. This particular lesion occluded spontaneously on follow-up cerebral angiography and the patient was not included in the study. The study sample was collected by reviewing the MGH cerebrovascular surgery and neuroendovascular databases within the study period. All historical, clinical, radiographic, and follow-up information was obtained from the electronic medical record in accordance with the Health Insurance Portability and Accountability Act.

Table 1.

Lawton-Halbach classification of tentorial dural arteriovenous fistulae.

Type	Dural arteriovenous fistulae	Location	Dural base	Venous sinus	Venous drainage
1	Galenic	Midline	Anterior falcotentorial junction	Vein of Galen	Supra- and infratentorial
2	Straight sinus	Midline	Middle falcotenotrial junction	Straight sinus	Infratentorial
3	Torcular	Midline	Posterior falcotentorial junction	Torcula	Supratentorial
4	Tentorial sinus	Paramedian	Tentorium	Tentorial sinus	Supratentorial
5	Superior petrosal sinus	Lateral	Petrotentorial junction	Superior petrosal sinus	Infratentorial
6	Incisural	Paramedian	Tentorial incisura	None	Supratenorial

Results

Table 2 summarizes the baseline clinical, radiographic, and procedural characteristics of the study population. A total of 18 patients with 20 tentorial DAVF were analyzed, with eight patients having nine SPS DAVF. Of the patients with SPS DAVF, there were seven Cognard IV, one Cognard III, and one Cognard IIb lesions. Two patients each presented incidentally, with headache, or with subarachnoid hemorrhage (SAH). One patient presented with tinnitus and another patient with bilateral SPS DAVF had clinical symptoms of cerebral venous congestion. Five SPS DAVF were initially treated with endovascular transarterial embolization, while the other four underwent surgical occlusion without preoperative embolization. Transvenous embolization was not performed. Of the SPS DAVF treated with embolization, two (40%) remained occluded on follow-up cerebral angiography, while the remaining three (60%) persisted or recurred and required surgical intervention for definitive closure. Of the four SPS DAVF treated with primary surgical occlusion, all four (100%) remained closed on follow-up cerebral angiography. In addition, of the three SPS DAVF that persisted or recurred following embolization and required subsequent surgical closure, all three (100%) remained occluded on follow-up cerebral angiography. For the entire cohort, the mean length of radiographic and clinical follow-up was 3.1 and 6.2 months, respectively. With respect to procedural and operative complications, one patient treated with endovascular embolization had transient cranial nerve V1 distribution numbness following occlusion of the middle meningeal artery (MMA) and one patient cured with surgical occlusion had a mild cranial nerve IV palsy postoperatively.

Table 2.

Characteristics of 18 patients with 20 tentorial dural arteriovenous fistulae.

Patient no.	Tentorial DAVF no.	Age/ Sex	Presentation	Lawton-Halbach type	Cognard grade	No. embolizations	Embolization agent(s)	Angiographic outcome after embolization	Surgical approach	Angiographic outcome at follow-up	mRS
											Pre-	Post-
1	1	51/M	Venous HTN	Galenic	IV	2	Onyx, nBCA	Complete	–	Complete	3	1
2	2	66/F	SAH/IVH	Straight sinus	IV	1	Onyx, coils	Residual	SOC	Complete	0	0
3	3	84/M	IPH	Straight sinus	IV	2	Onyx	Complete	–	Complete	1	1
4	4	60/M	HA	Torcular	I	2	Onyx	Residual	–	Residual	0	0
5	5	52/F	Incidental	Torcular	III	1	Onyx	Complete	SOC	Complete	1	1
6	6	83/M	Venous HTN	Torcular	IV	0	–	–	SOC	Complete	1	1
7	7	57/M	HA	Torcular	IV	1	Onyx	Complete	–	Complete	0	0
8	8	26/M	Incidental	Torcular	I	0	–	–	–	Complete	0	0
9	9	52/M	Seizure	Tentorial	IV	1	Onyx	Complete	–	Complete	1	0
10	10	44/M	Incidental	Tentorial	IV	2	Onyx	Residual	St-IO	Complete	0	0
11	11	58/F	Incidental	Tentorial	III	1	PVA	Residual	RS	Residual	0	0
12	12	64/M	Venous HTN	Superior petrosal sinus	III	0	–	–	RS	Complete	2	2
12	13	64/M	Venous HTN	Superior petrosal sinus	IV	1	Onyx	Complete	–	Complete	2	2
13	14	67/M	Tinnitus	Superior petrosal sinus	IV	1	Onyx	Complete	–	Complete	1	1
14	15	69/M	HA	Superior petrosal sinus	IV	0	–	–	RS	Complete	0	0
7	16	57/M	HA	Superior petrosal sinus	IIb	0	–	–	RS	Complete	0	0
15	17	59/F	SAH	Superior petrosal sinus	IV	3	Onyx	Residual	RS	Complete	1	1
16	18	52/F	Incidental	Superior petrosal sinus	IV	0	–	–	ST/RS	Complete	1	1
17	19	57/M	SAH	Superior petrosal sinus	IV	1	Embospheres	Residual	RS	Complete	0	2
18	20	62/F	Incidental	Superior petrosal sinus	IV	1	Onyx	Residual	RS	Complete	0	0

DAVF: dural arteriovenous fistula; F: female; HA: headache; HTN: hypertension; IPH: intraparenchymal hemorrhage; IVH: intraventricular hemorrhage; M: male; mRS: modified Rankin Scale; nBCA: n-butyl cyanoacrylate; PVA: polyvinyl alcohol; RS: retrosigmoid; SAH: subarachnoid hemorrhage; SOC: suboccipital craniectomy; ST: subtemporal; St-IO: supratentorial-infraoccipital.

Seven (77.8%) SPS DAVF had major arterial supply via the MHT/inferolateral trunk (ILT), two (22.2%) via the MMA, and one (11.1%) via scalp arteries. Five (55.6%) SPS DAVF had minor arterial supply via the MMA, two (22.2%) via scalp arteries, and one (11.1%) each via the MHT/ILT, superior cerebellar artery/posterior cerebral artery (SCA/PCA), and anterior inferior cerebellar artery/posterior inferior cerebellar artery (AICA/PICA). Venous drainage largely occurred via the petrosal vein (66.7%) and the basal vein of Rosenthal (77.8%). Table 3 shows the angiographic outcome of each SPS DAVF following intervention and its associated arterial supply. Two (100%) SPS DAVF that were successfully treated with endovascular embolization had major or minor ECA supply, while the three (100%) persistent lesions had principal ICA supply via the MHT. Three (75%) of the four SPS DAVF treated with primary surgical occlusion had dominant MHT supply.

Table 3.

Summary of nine superior petrosal sinus dural arteriovenous fistulae.

Patient no.	Tentorial DAVF no.	Lawton-Halbach type	No. embolizations	Angiographic outcome after embolization	Surgical approach	Angiographic outcome at follow-up	ICA supply	ECA supply
12	12	Superior petrosal sinus	0	–	RS	Complete	Major	None
12	13	Superior petrosal sinus	1	Complete	–	Complete	Major	Minor
13	14	Superior petrosal sinus	1	Complete	–	Complete	Minor	Major
14	15	Superior petrosal sinus	0	–	RS	Complete	None	Major
7	16	Superior petrosal sinus	0	–	RS	Complete	Major	None
15	17	Superior petrosal sinus	3	Residual	RS	Complete	Major	Minor
16	18	Superior petrosal sinus	0	–	ST/RS	Complete	Major	Minor
17	19	Superior petrosal sinus	1	Residual	RS	Complete	Major	Minor
18	20	Superior petrosal sinus	1	Residual	RS	Complete	Major	Minor

DAVF: dural arteriovenous fistula; ECA: external carotid artery; HA: headache; HTN: hypertension; ICA: internal carotid artery; IPH: intraparenchymal hemorrhage; IVH: intraventricular hemorrhage; mRS: modified Rankin Scale; nBCA: n-butyl cyanoacrylate; PVA: polyvinyl alcohol; RS: retrosigmoid; SAH: subarachnoid hemorrhage; SOC: suboccipital craniectomy; ST: subtemporal; St-IO: supratentorial-infraoccipital.

Case illustrations

Case 1 (Patient #15)

A middle-aged patient with no significant past medical history presented to the emergency department (ED) with acute-onset headache and emesis but an otherwise intact neurological examination. Non-contrast computed tomography (CT) of the head demonstrated small-volume, diffuse cortical SAH, and CT angiography showed a complex left cerebellopontine angle (CPA) vascular lesion consistent with DAVF. Cerebral angiography (Figures 1(a) and (b)) confirmed the presence of a Cognard IV DAVF at the SPS with arterial supply via an enlarged lateral tentorial branch of the MHT, MMA, and SCA with venous egress through ectactic inferior and superior cerebellar veins, basal vein of Rosenthal, and pontomesencephalic veins to the vein of Galen and straight sinus. Embolization with ethylene vinyl alcohol copolymer (Onyx 18) (Medtronic; Minneapolis, MN) via the MMA was performed with complete closure of the DAVF. Six months later, cerebral angiography (Figure 1(c)) demonstrated fistula recurrence, with interval enlargement of the MHT and new arterial supply from the ILT. Scepter C (MicroVention Inc; Tustin, CA) balloon-assisted embolization with Onyx 18 was performed through the MHT, but complete occlusion of the fistula was not achieved. Three months later, cerebral angiography (images not shown) showed persistence of the DAVF with recruitment of additional ECA supply, including an accessory meningeal branch arising from the internal maxillary artery. Embolization with Onyx 18 was attempted through this branch, but the fistula remained. Four months later, given the persistence of the DAVF despite three embolization attempts, the patient underwent left retrosigmoid craniotomy for surgical interruption of the draining vein (Figures 1(d) and (e)) at the petrotentorial junction; immediate postoperative cerebral angiography showed complete SPS DAVF occlusion. Sixteen months later, delayed cerebral angiography confirmed durable closure (Figure 1(f)). The patient remained neurologically intact throughout treatment.

Figure 1.

Case #1, Patient #15. (a) Left internal carotid artery (ICA) angiogram (lateral view) demonstrating a superior petrosal sinus dural arteriovenous fistula (SPS DAVF) with prominent supply from the tentorial branch of the meninghypophyseal trunk (MHT) with drainage through cerebellar hemispheric veins. (b) Left external carotid artery (ECA) angiogram (lateral view) showing middle meningeal artery (MMA) supply to the SPS DAVF. (c) Left ICA angiogram (lateral view) six months following Onyx embolization via the MMA showing increased MHT supply and enlargement of the inferolateral trunk. (d) and (e) Intraoperative photographs demonstrating an Onyx-filled venous varix within the cerebellopontine angle (CPA) at the point where the SPS DAVF draining veins emanated from the petrotentorial junction and (f) subsequent occlusion of the remaining venous outflow of the SPS DAVF with a microsurgical clip. Left ICA angiogram (unsubstracted, lateral view) showing durable closure of the SPS DAVF following clip occlusion.

Case 2 (Patient #17)

A middle-aged patient with a history of hypertension presented to the ED with acute-onset headache. Non-contrast CT of the head showed extensive SAH throughout the skull base cisterns with mild intraventricular hemorrhage, and CT angiography demonstrated a left CPA ectatic vascular lesion with numerous varices suspicious for DAVF. Given somnolence on examination, an external ventricular drain was placed for cerebrospinal fluid (CSF) diversion and intracranial pressure control. Cerebral angiography (Figures 2(a) and (b)) identified a Cognard IV SPS DAVF with arterial supply arising from an enlarged lateral tentorial branch of the MHT and the petrous branch of the MMA with venous egress through the petrosal vein, lateral mesencephalic vein, and basal vein of Rosenthal to the vein of Galen and straight sinus. Embolization with Embospheres (Merit Medical Systems Inc; South Jordan, UT) via the MMA was performed, resulting in a partial reduction in arteriovenous shunting (images not shown). The following day, the patient underwent left retrosigmoid craniotomy for clipping of the SPS DAVF (Figures 2(c) and (d)); immediate postoperative cerebral angiography (Figure 2(e)) confirmed complete closure of the fistula. Twelve months later, delayed cerebral angiography (Figure 2(f)) showed durable cure of the SPS DAVF. The patient remained neurologically stable and did not require permanent CSF diversion.

Figure 2.

Case #2, Patient #17. (a) Left internal carotid artery (ICA) angiogram (lateral view) demonstrating a superior petrosal sinus dural arteriovenous fistula (SPS DAVF) with prominent supply from the tentorial branch of the meningohypophyseal trunk with drainage through the petrosal vein, lateral mesencephalic vein, basal vein of Rosenthal, and vein of Galen. (b) Left external carotid artery angiogram (lateral view) showing middle meningeal artery supply to the SPS DAVF. (c) Intraoperative photograph illustrating a variceal petrosal vein draining the SPS DAVF. (d) Indocyanine green intraoperative angiography showing early filling of the draining veins, confirming rapid arteriovenous shunting. (e) Immediate postoperative left common carotid artery (CCA) angiography (lateral view) and (f) delayed left CCA angiography (unsubtracted, lateral view) demonstrating durable closure of the SPS DAVF following clip occlusion.

Case 3 (Patient #13)

An elderly patient with a history of hypertension and Burkitt lymphoma presented to the outpatient clinic with two to three years of intermittent left tinnitus. Magnetic resonance imaging of the brain showed an enlarged left occipital artery with hypervascularity in the region of the left SPS with congested cerebellar veins. Cerebral angiography (Figures 3(a) and (b)) confirmed a Cognard IV SPS DAVF with arterial supply via the occipital artery, MMA, MHT, and a recurrent meningeal branch off the ophthalmic artery with venous egress into cerebellar hemispheric veins and the inferior and superior vermian veins. Scepter C balloon-assisted embolization with Onyx 18 via the occipital artery was performed with complete occlusion of the fistula (Figure 3(c) and (d)). Six months later, delayed cerebral angiography (images not shown) showed a durable cure of the SPS DAVF. The patient’s tinnitus abated following treatment of the fistula.

Figure 3.

Case #3, Patient #13. (a) Left internal carotid artery (ICA) angiogram (lateral view) demonstrating a superior petrosal sinus dural arteriovenous fistula (SPS DAVF) with supply from the tentorial branch of the meningohypophyseal trunk as well as a recurrent meningeal branch arising from the ophthalmic artery. (b) Left external carotid artery angiogram (lateral view) showing prominent occipital artery and middle meningeal artery supply to the SPS DAVF. (c) and (d) Left ICA angiograms (lateral views, (d) unsubtracted) demonstrating complete closure of the SPS DAVF following Onyx embolization via the enlarged occipital artery.

Discussion

SPS DAVF are complex vascular lesions that often have arterial supply from ECA and ICA branches and venous egress through dural sinuses and subarachnoid veins. Successful treatment of these fistulae relies on disconnection or occlusion of veins emanating from the point of arteriovenous shunting within the dura without the need for nidus resection.^{1,5 6} The angiographic and clinical results from this series of patients with SPS DAVF demonstrate the outcomes of current surgical and endovascular treatment strategies. In this series of SPS DAVF, surgery was associated with a higher rate of cure compared to endovascular treatment, as has been previously described.^3,7 For the few lesions cured with endovascular treatment alone, robust ECA supply provided a better conduit for embolization (as opposed to smaller MHT vessels), theoretically allowing for more effective penetration of the fistulous connection with embolic material, thereby resulting in durable cures. In fact, for lesions with predominant ICA supply, embolization through ECA feeding arteries such as the MMA, even if not robust, may result in complete cures.⁸ This retrospective study does not define the best treatment for SPS DAVF in any given patient, but does support consideration for primary surgical treatment, especially when supply is mainly via the MHT.

When endovascular treatment is considered, it must result in closure of the site of arteriovenous shunting for the treatment to be durable. This is typically achieved by navigating a microcatheter into the distal aspect of an appropriate feeding artery and instilling embolic material (e.g. Onyx or n-butyl cyanoacrylate (nBCA)) into the nidus and proximal venous outflow. Because of the rich network of vascular supply from ICA and ECA territories in DAVF, proximal occlusion of feeding arteries alone is rarely effective. Embolization via ECA, as opposed to ICA, branches has a more favorable risk profile, but ECA-ICA collateral connections and cranial nerve supply by small ECA branches must be considered prior to any embolization procedure.^9,10 Transarterial embolization of ICA branches, including the lateral tentorial branch of the MHT, carries the risk of embolic complications in distal middle cerebral artery and anterior cerebral artery territories in addition to infarction of the cranial nerves traveling through the cavernous sinus. When performed in our practice, transarterial embolization of SPS DAVF via the lateral tentorial branch of the MHT is accomplished by placing a microcatheter as distally as possible in the tentorial branch and a balloon microcatheter in the ICA across the base of the MHT. The balloon is inflated during instillation of the liquid embolic agent to minimize the risk of embolic complications from reflux of embolic agents into the ICA. To this end, van Rooij et al. reported on a series of six SPS DAVF, all with supply from the tentorial branch of the MHT. Five (83.3%) of the six fistulae in this series were completely cured with balloon-assisted embolization with nBCA via the tentorial branch, while one fistula was occluded with placement of a coil in the origin of the MHT. No complications directly related to the procedures were encountered.¹¹ In our series, of eight patients with major or minor MHT supply, balloon-assisted embolization via the tentorial branch was attempted in only one patient (Patient #15) following an appraisal of each patient’s angiographic anatomy and incumbent risks. Despite the results reported by van Rooij et al., though, curative embolization of SPS DAVF via the tentorial branch of the MHT or other enlarged ICA branches is uncommon.^3,12

With results similar to those presented in our series, Ng et al. evaluated 18 SPS DAVF treated at the University of California, San Francisco (UCSF) between 1986 and 2002, 13 (72.2%) of which had arterial supply from the MHT or ILT. Fifteen and four SPS DAVF underwent transarterial and transvenous embolization procedures, respectively, only three (16.7%) of which resulted in durable occlusion. As such, 15 fistulae required surgery for definitive treatment.¹² From a later time period, Lawton et al. reported on a series of nine patients at UCSF with SPS DAVF from 1997 to 2006. In this series, each patient underwent transarterial embolization, but all nine (100%) required surgical disconnection of the draining vein(s) for definitive treatment.³ Our study was performed during the current “endovascular era,” in which next-generation microcatheters, microwires, microcoils, liquid embolic agents, and particles were available for use. Nevertheless, despite these advanced technologies and techniques, we have maintained an aggressive surgical posture toward the treatment of SPS DAVF. In our current practice environment, for SPS DAVF, we generally attempt transarterial embolization through enlarged ECA branches (if present) as first-line treatment. We have observed that SPS DAVF with dominant ICA supply (or without significant ECA supply) are difficult to treat definitively by endovascular means while carrying an excessive risk of embolic complications. In addition, microcatheter access to the tentorial branch of the MHT is often not trivial given its acute origin from the ICA and tortuous anatomy in DAVF cases. While embolization via ECA branches has a lower risk profile, these branches are often small and/or tortuous, features that both render obtaining distal microcatheter access challenging and reduce the likelihood of Onyx or nBCA reaching the nidus for complete closure. In cases of incomplete occlusion, recurrent shunting, or lack of suitable ECA branches, we prefer to proceed to retrosigmoid craniotomy for surgical disconnection of the draining vein(s) from the focus of arteriovenous shunting at the SPS. The petrotentorial junction is surgically accessible by a standard retrosigmoid craniotomy, though use of the extended retrosigmoid craniotomy may expand the operative corridor in cases of significant venous ectasia or variceal disease or cerebellar edema.¹³ Once the arterialized vein is identified as it emanates from the dura, it can be clipped and/or coagulated and divided for definitive closure of the fistula. Inspection for and disconnection of additional draining veins is critical in order to avoid residual arteriovenous shunting. This direct, open approach carries a high rate of complete occlusion and avoids the embolic risks associated with transarterial embolization of high-flow ICA branches.

Our study suffers from limitations inherent to any single-center, retrospective work as well as a small sample size, which precludes robust statistical analyses. Consequently, we simply provide a descriptive report of our modern-era approach to SPS DAVF, in which we employ both endovascular and surgical strategies to achieve fistula occlusion based on the angiographic anatomy of the lesion requiring treatment. Regardless of the results presented here, treatment decisions are ultimately case specific and should be informed by particular angiographic nuances.

Conclusion

Complete endovascular closure of SPS DAVF with dominant ICA supply via the MHT may be difficult to achieve. Upfront surgical intervention is associated with a high rate of complete occlusion.

Declaration of conflicting interests

The authors declared the following potential conflicts of interest with respect to the research, authorship, and/or publication of this article: ABP is a consultant for Penumbra Inc and Medtronic. The other authors have nothing to declare.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.