Dural arteriovenous fistula draining into the superior petrosal vein: a comparative analysis of two case reports for enhanced anatomical understanding and optimal treatment strategy

Introduction

Cerebral dural arteriovenous fistulas (dAVFs) are vascular lesions where arterial blood shunts into the wall of a dural venous sinus or a cortical vein. The incidence of these lesions is 0.805 per 100,000 person per year (1).

dAVFs are defined mainly as idiopathic, even though they are sometimes related to previous trauma or craniotomy or dural sinus thrombosis (2). Two main classifications for dAVF subdivision are currently used in the literature: Borden (3) and Cognard (4).

These two classifications are based on hemodynamics of dAVFs, lacking predictability of their architecture and the options of treatment. Nevertheless, they provide important information regarding the natural history of the fistula and the need of treatment. In Borden type I and Cognard types ≤2a, the lack of cortical venous outflow is related to a benign behavior, with a low risk of intracranial hemorrhage (5). In contrast, Borden type ≥2 and Cognard ≥2b are considered high risk lesions with an annual mortality rate of 10.4%, an annual risk of intracranial hemorrhage of 8.1% and an annual risk of neurological deficits’ occurrence of 6.9% (6). The annual rebleeding rate for dAVF with cortical venous drainage is estimated at 7.3%, substantiating the recommendation for treatment within five days of the initial bleeding episode (7).

Cerebral dAVFs are mainly located in the cavernous sinuses or in the region of the transverse and sigmoid sinuses; only rarely, 8% of the cases (8), they are located in the petroclival region (9), where they have an aggressive behavior that justifies a prompt treatment. dAVFs draining in superior petrosal vein (SPV), also known as Dandy’s vein, are an even rarer subtype of cerebral fistula, sometimes reported in literature as tentorial fistula or superior petrosal sinus fistula (10). dAVFs draining in the SPV are usually challenging due to their deep localization and drainage veins in the vicinity of highly eloquent areas. They are considered as rare lesion, for which there are no evidence for a standard treatment, but the strategy should be discussed in a multidisciplinary board and tailored on every single case. Tentorial (11) dAVFs and the presence of ectatic vessels are identified as independent predictors of both initial bleeding and subsequent re-bleeding events (7). While many dAVFs benefit from an endovascular treatment, which aim is to occlude the draining vein, dAVFs draining in the SPV are usually difficult to be treated with endovascular methods, and surgery may be an effective technique. This is because of the long and tortuous route to the draining vein through vessels that are difficult to reach with endovascular procedures. This paper describes two clinical cases in which the advantages of physiopathological assessment and accurate diagnosis were used to find the best personalized solution by both endovascular and microsurgical means.

We present this article in accordance with the CARE reporting checklist (available at https://asj.amegroups.com/article/view/10.21037/asj-23-46/rc).

Case presentation

Case 1

A 63-year-old healthy woman, with unremarkable past medical history, was admitted to the emergency department after being found unconscious. She rapidly returned to consciousness with a right-side body hemiparesis.

The clinical evaluation showed a Glasgow Coma Score (GCS) of 14 (E4, V4, M6), A right-sided sensory and motor hemi-syndrome with plegia of the upper extremity and severe paresis of the lower extremity, right hemianopsia and fluent aphasia, accounting for a National Institutes of Health Stroke Scale (NIHSS) of 17 points.

The computed tomography (CT) scan, performed 1 h after she was found lying on the ground in her house and 4 h after she was seen for the last time normal, showed a left thalamic hemorrhage with intraventricular bleeding in all four cerebral ventricles (Figure 1A) and left peri-mesencephalic tortuous ectatic vascular structures. An external ventricular drainage (EVD) was acutely positioned with a flow of 10 mL/h of hematic liquor during the subsequent days.

Figure 1 Case 1 diagnostic work up. (A) CT at emergency department arrival showing a left thalamic hemorrhage with intraventricular bleeding. (B) 3D-DSA showing the foot vein (white arrow) at the apex of the petrosal bone. (C) Selective angiogram of the left ICA shoving the dAVF supplied by petrosal branches of left MMA and by the artery of the foramen rotundum (red arrow), draining directly into left petrosal vein (blue arrow) continuing in the ipsilateral latero-mesencephalic vein and basal vein of Rosenthal. Note the ectasia and varix of draining vein (green arrow). (D) 3D-DSA showing the ectasia and varix (blue arrow) of the draining vein continuing in the ipsilateral deep middle cerebral vein and then, through the anterior communicating vein (red arrow), in the contralateral deep middle cerebral vein, right basal vein of Rosenthal and finally in the ampulla of Galen. Note the absence of a connection between ectasic and varicose venous structures and the ampulla of Galen on the left side (asterisk). CT, computed tomography; DSA, digital subtraction angiography; ICA, internal carotid artery; dAVF, dural arteriovenous fistula; MMA, middle meningeal artery.

A digital subtraction angiography (DSA) with additional high-resolution cone-beam CT (Vaso-CT, Philips Medical Systems, Best, The Netherlands) showed a dural arterio-venous fistula draining in the left SPV (Figure 1B-1D). Many arterial feeders were identified from the meningohypophyseal trunk of both carotids, from petrosal vessels of the left middle meningeal artery and from vessels from the ipsilateral artery of the foramen rotundum. The draining vein was identified in a tortuous and ectasic left petrosal vein continuing in the ipsilateral latero-mesencephalic vein, basal vein of Rosenthal and deep middle cerebral vein (Figure 1D); then it went contralaterally through the anterior communicating vein, converging in the contralateral deep middle cerebral vein, right basal vein of Rosenthal and finally in the ampulla of Galen. Because of the direct drainage not in a sinus and the venous ectasia, the fistula was classified as a petrosal dAVFs Borden III, Cognard IV. Because the multiple feeding arteries were fine and tortuous and meningeal branches came from highly eloquent arteries, a transarterial approach was considered not feasible. A transvenous approach had also been excluded due to the lack of connection with the homolateral SPV, while the retrograded venous navigation through ectasia and varices of the drainage vein (Figure 1C,1D) was considered not feasible and with a high risk of venous perforation.

To better plan the surgical approach, a pre-op magnetic resonance (MR) was also performed showing the infra-tentorial localization of the draining vein (Figure 2A).

Figure 2 Case 1 surgical images and follow up. (A) MRI T2 weighted coronal section image. The MRI study allowed to understand the infratentorial location of the foot vein (white arrow) in order to plan the best surgical approach. (B) Intraoperative image after foot vein clipping A nearby branch (*) is preserved and the distal part of the foot vein is not vascularized anymore after the clip positioning (#). (C) Intraoperative fluorescence check after clip positioning. The nearby vessel (*) is fluorescent contrary to the distal part of the clipped foot vein (#). (D) MIP image angio-CT scan performed on day 3 after surgery showing complete regression of ectasic and varicose venous structure. MRI, magnetic resonance imaging; MIP, maximum intensity projection; CT, computed tomography.

We performed an asterion-centered left retrosigmoid approach with patient in right park bench position. The whole surgery was performed with intra-operative neuromonitoring. After semicircular dural opening, cerebellar relaxation was obtained by cisterna magna opening. The draining vein was identified, thanks to indocyanine green (ICG) fluoroscopy, on the inferior margin of the tentorium and the dura fistula point was localized. Cranial nerve (CN) V, VII and IV were identified as well. Intraoperatively, double clipping (L-Lasic, Tuttlingen, Germany) of the vein was sufficient to interrupt the fistulous circulation, as evidenced by ICG fluoroscopy, eliminating the need to divide the vein (Figure 2B,2C). The intraoperative neuromonitoring was performed for 20 minutes after clips positioning, excluding complications related to the new venous setting.

During the subsequent days in intensive care unit (ICU), the patient was extubated and the neurological examination was unchanged compared to the preoperative status.

Angio-CT scan performed on day 3 after surgery showed complete regression of ectasic and varicose venous structure (Figure 2D) and DSA at day 7 showed the complete exclusion of the fistula.

The case was presented to the multidisciplinary neurovascular board. The patient, with a stable neurological condition, was subsequently discharged to a neuro-rehabilitation clinic. A 6- and 18-month angio-magnetic resonance imaging (MRI) follow-up showed no residual flow in the fistula nor complications related to the surgery. The clinical status of the patient improved with complete regression of the aphasia and a significant improvement of the right hemiparesis.

Case 2

A 61-year-old healthy woman, with unremarkable past medical history, was admitted to the emergency department after the sudden onset of headache with GCS 10, emesis and a right hemiparesis. An angio-CT, performed 1.5 h after the onset of symptoms scan, showed a left pontine hemorrhage (Figure 3A) with tortuous and ectasic veins in proximity. A DSA was performed showing an arteriovenous shunt with a nidus-like architecture with drainage in the SPV toward the superior petrosal sinus (Figure 3B-3D). The arterial supply was identified coming from a left duplicate superior cerebellar artery (SCA). Minor arterial supplies were also identified coming from the left meningohypophyseal trunk and from petrosal branches of left middle meningeal artery. The Vaso-CT demonstrated the extra-parenchymal location of arterial-vein connection, allowing the diagnosis of dAVF draining directly in the left SPV. After multidisciplinary discussion, an endovascular approach was chosen. Microsurgical intervention was also carefully evaluated but ultimately deemed not viable due to the complex collateral circulatory patterns and the heightened anesthetic risks involved. The neurosurgical team assessed these risks as disproportionately high, guiding the decision against pursuing a surgical approach. A transarterial embolization with glue [25% of Glubran^®2 (GEM SRL, Viareggio, Italy) and 75% of Lipiodol^® (Ultra Fluid, Guerbet, Villepinte, France)] was performed. The embolization procedure was started from the superior division branch of proximal trunk of the duplicated SCA (Figure 3D). The super-selective catheterization of the inferior division branch of proximal trunk of the duplicated SCA was not feasible even after multiple attempts and, because of the persistence of the shunt, the embolization procedure was continued through the distal trunk of the duplicate SCA. In the latter branch, the glue injection was stopped due to its reflux up to the proximal portion of the SCA (Figure 4A-4C). The post-embolization angiogram did not show persistence of the shunt, suggesting an initial successful intervention (Figure 4D). However, the subsequent follow-up indicates the need for a more nuanced understanding of the embolic process and its outcomes.

Figure 3 Case 2 diagnostic work up. (A) CT at arrival at emergency department showing a left pontine hemorrhage. (B) Selective angiogram of the left vertebral artery showing a nidus-like architecture of an arteriovenous shunt supplied by a duplicated SCA, draining directly into left petrosal vein and then into ipsilateral superior petrosal sinus (white arrow). (C) 3D-DSA showing the extraparenchymal location of the shunt, at the apex of the petrosal bone, draining directly into left petrosal vein (red arrow). (D) Superselective angiogram (anteroposterior projections) of the superior division branch of proximal trunk of duplicated SCA. CT, computed tomography; SCA, superior cerebellar artery; DSA, digital subtraction angiography.

Figure 4 Case 2 Intraprocedural DSA images. (A) Angiogram after glue injection from the superior division branch of proximal trunk of duplicated SCA showing the persistence of the shunt mainly supplied by the inferior division branch of proximal trunk of duplicated SCA. (B) Superselective angiogram (anteroposterior projections) of distal trunk of duplicated SCA. (C) Glue cast at the end of the procedure penetrating up to the proximal part of petrosal vein only. (D) Angiogram at the end of the transarterial embolization showing the complete exclusion of the shunt and occlusion of proximal and distal trunks of duplicated left SCA. DSA, digital subtraction angiography; SCA, superior cerebellar artery.

In the ICU, the patient was successfully extubated and she was then transferred to the stroke unit with a GCS 11, severe dysphagia, requiring the positioning of a digiunostomy, right hemiplegia, right cerebellar syndrome and expressive aphasia. An MRI was performed 9 days after the acute onset, showing stable dimension of the hematoma and a recent ischemic lesion in the left SCA area. The patient was then discharged towards a rehabilitation clinic at the beginning, where she only partially recovered from the severe deficit, and finally to a retirement home.

A follow-up-DSA 8 months after the onset of the symptoms showed the persistence of a high flow arterio-venous shunt with feeding branches from the meningohypophyseal trunk of the left internal carotid artery (ICA) and from both the branches of a left duplicated SCA (Figure 5A-5C). At this time, the superior petrosal sinus was not identified and the draining vein was identified in the left petrous vein with subsequent drainage in the cerebello-pontine fissure vein, in the lateral recess of the IV ventricle vein, through the midline in a right inferior cerebellar vein and from there to the right transverse sinus (Figure 5D).

Figure 5 Case 2 imaging follow up. (A-C) Selective injection of the left ICA, 2D anteroposterior (A) and lateral (B) projections, 3D DSA (C) showing persistent of the shunt supplied by the left meningohypophyseal trunk. Note that at this time the superior petrosal sinus was not identified; dAVF drained directly into left petrous vein with subsequent drainage in the cerebello-pontine fissure (blue arrow image C) vein, in the lateral recess of the IV ventricle vein, through the midline in the right inferior cerebellar vein (red arrow image A) and from there to the right transverse sinus (green arrow image A). (D) Selective angiography from the left vertebral artery showing the persistence of the blood supply to the fistula from the shunt from the recanalized inferior division branch of proximal trunk of duplicated SCA. ICA, internal carotid artery; DSA, digital subtraction angiography; dAVF, dural arteriovenous fistula; SCA, superior cerebellar artery.

Clinically, the patient, at 8 months after the onset of symptoms, presented with a modified Rankin Scale (mRS) of 4. The case was then collegially discussed and, because of the general condition of the patient, a wait-and-see approach was expected with 3-month MRI follow-up.

All procedures performed in this study were in accordance with the ethical standards of the institutional and/or national research committee(s) and with the Helsinki Declaration (as revised in 2013). Written informed consent was obtained directly from the patient of case 1 and from patient’s husband of case 2. for the publication of this case report and accompanying images. A copy of the written consent is available for review by the editorial office of this journal.

Discussion

The treatment of cerebral dural fistulas draining into the SPV is still controversial because of their complex angio-architectural features and variable venous involvement: a shared classification and guidelines for the treatment are far to be found. A complete imaging work-up is mandatory in the management of these lesions: conventional CT and standard MRI are of limited value for the classification of dAVFs (12) but they can provide additional information useful for the definition of a treatment strategy. In case 1, the MRI allowed to understand the infratentorial location of the draining vein: no vessels were approachable by catheterization and an indication to microsurgical treatment with a retrosigmoid approach was given (13-15).

Architecture of the SPV

The SPV, also known as the petrosal vein or the Dandy’s vein, which origins from the cerebellopontine fissure vein alone or in union with other tributaries (16), drains the anterior portions of the cerebellum and brainstem into the superior petrosal sinus and its preservation is fundamental during microsurgical approaches to the cerebellopontine angle (17-19). Tanriover (20) classified the superior petrosal venous complex on the basis of its drainage patters in relation with the entry point into the superior petrosal sinus, Meckel’s cave and the internal acoustic meatus. Type I drains into the superior petrosal sinus (SPS) above and lateral to the boundaries of the internal auditory meatus (IAM). Type II, the most common type, drains between the lateral limit of the trigeminal nerve at the Meckel’s cave and the medial limit of the facial nerve at the IAM. Type III drains into the SPS above or medial to the Meckel’s cave.

Clinical manifestations of dAVFs draining in the SPV

The peculiarity of dAVFs draining in the SPV is related to their aggressive behavior resulting in hemorrhages or progressive focal neurological deficits in 97% of the cases (8). dAVFs draining in the SPV, sometimes defined in literature as tentorial dAVFs, are a subtype of petroclival fistula. Direct drainage into the petrosal vein leads to venous ectasia and varices in the supratentorial space resulting in massive hemorrhages, as in case 1. The relationships between the SPV and the lateral mesencephalic vein (21) should be verified preoperatively on DSA angiography to avoid further complications. Neurological deficits caused by the presence of these lesions alone can be as disabling as a stroke: for example, dementia is a typical non-hemorrhagic symptom resulting from venous hypertension in the cerebral cortex or bilateral thalami, identifiable as thalamic edema and caused by dAVFs draining into the SPV (22).

Treatment options: endovascular approach

The aggressive behavior of dAVFs draining in the SPV justifies an aggressive treatment even in the absence of hemorrhages findings (23).

Even though endovascular therapy, with a transarterial, transvenous or combined approaches, has become the first-line treatment for many dAVFs (24), in case of dAVFs draining in the SPV, it seems difficult to achieve complete cure by endovascular approach only (10). The small diameter as well as the tortuosity of the arterial feeders of these dAVF, as for example in case 1, makes a selective arterial catheterization technically very challenging. Additionally, these anatomic features can limit the penetration of the liquid embolic material preventing a definitive shunt obliteration (25). For example, in case 2, not achieving a sufficient glue progression up to the venous side of the fistula (Figure 4C) probably led to the persistence of the shunt at the follow-up. The transvenous embolization (TVE) may be another option for endovascular treatment. TVE is nowadays an established treatment for intracranial dAVFs involving the major dural sinuses (26,27), but regarding dAVFs draining in the SPV, this can be technically difficult and there is still, to our knowledge, limited literature (28). Transvenous catheterization through the superior petrosal sinus may not be possible as the sinus is often occluded, narrowed or without a connection with the petrosal vein as for example in case 1. Furthermore, the TVE through the fragile subarachnoid veins might result in premature rupture and hemorrhage (28,29). Failure to occlude the fistula point exposes the patient to a risk of recurrence and re-bleeding. In this context, it should be highlighted that reaching the fistula point by vein microcatheterization in the DAVFs that drain directly into a subarachnoid vein rather than into the adjacent sinuses is typically more difficult thus resulting in a risk of incomplete treatment associated with the complications described above (26-30).

Treatment options: surgical approach

Direct surgery represents an effective option (10-25). ICG-fluoroscopy is an aid to the surgeon during the procedure in order to discriminate between an arterialized SPV and a normal SPV, with the latter that, in our opinion, should be, as far as possible, preserved (31).

The retrosigmoid approach used for case 1 is based on Lawton (32) classification for tentorial dAVFs, which he divided into six subtypes, each one having unique architecture and ideal surgical approach: galenic, straight sinus, torcular, tentorial sinus, superior petrosal sinus and incisural.

The contribution of Vaso-CT

Currently, 2D DSA is the gold standard to evaluate dAVFs hemodynamic but it can require multiple projections or selective injections resulting in increased dose of radiation and contrast medium (33). Another limitation of this method is that it provides exclusively vascular anatomic details. High-resolution cone-beam CT (Vaso-CT) can overcome certain limitations of the 2D DSA as a consequence of the volumetric nature of its acquisition and it has recently become essential in obtaining more detailed information (33-35). Regarding case 2, the 3D-DSA demonstrated the extra-parenchymal location of the arteriovenous shunt as well as the drainage directly into the petrosal vein, allowing the diagnosis of dural fistula despite the nidus-like architecture of the malformation and the poor dural feeders originating from the external carotid artery.

The 8-month DSA showed the persistence of the fistula justifying the opinion of authors that suggest that when a transvenous embolization, in combination with a transarterial approach, is not feasible, surgery should be performed (13,36,37). Nevertheless, in this case, surgery was not performed due to general conditions of the patient.

Limitations

Literature regarding dAVFs draining in the SPV is still poor: our sample is too small to provide indication regarding the management of these lesions, but it offers an overview of two different approaches for the same pathology.

Conclusions

Wide disposal of a complete radiological exam allows the deep understanding of the anatomy, dynamic of flow and the architecture of dAVFs draining in the SPV. In case 1, MRI allowed to understand the infratentorial location of the draining vein, despite a supratentorial hemorrhage, while in case 2, 3D-DSA allowed to identify an extra-parenchymal location of the lesion helping to understand the type of the malformation.

This report of two apparently similar cases that presented to our ER in a brief period of time shows completely opposite options of treatment and supports current literature where surgery and endovascular procedures should be personalized and selected after a careful analysis of the case, with excellent outcomes in both cases.

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the CARE reporting checklist. Available at https://asj.amegroups.com/article/view/10.21037/asj-23-46/rc

Peer Review File: Available at https://asj.amegroups.com/article/view/10.21037/asj-23-46/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://asj.amegroups.com/article/view/10.21037/asj-23-46/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. All procedures performed in this study were in accordance with the ethical standards of the institutional and/or national research committee(s) and with the Helsinki Declaration (as revised in 2013). Written informed consent was obtained directly from the patient of case 1 and from patient’s husband of case 2. for the publication of this case report and accompanying images. A copy of the written consent is available for review by the editorial office of this journal.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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