Hybrid treatment of adult pial arteriovenous fistula with multiple venous pouches and flow-related aneurysm: a case report

Abstract

We report a case of adult pial arteriovenous fistula (AVF) with unfavorable angioarchitecture treated by staged hybrid approach. A 62-year-old man had high-flow pial AVF supplied by the superior trunk of the left middle cerebral artery with multiple venous pouches and a flow-related aneurysm. Three-dimensional rotational angiography demonstrated an extremely short arterial segment between the fistulous point and an adjacent normal arterial branch, precluding safe selective occlusion. Coil embolization of the venous pouch reduced flow, enabling next-day microsurgical disconnection. The shunt was completely obliterated without ischemic complications, and follow-up imaging showed aneurysm regression.

Introduction

Pial arteriovenous fistulas (AVFs) are rare intracranial vascular shunt lesions characterized by a direct connection between one or more arterial feeders and a single draining vein without an intervening nidus, distinguishing them from cerebral arteriovenous malformations [4, 14]. Given their high-flow nature, pial AVFs are frequently associated with venous dilation or venous pouch formation, which may contribute to hemorrhage, neurological deterioration, or progressive venous hypertension [3, 10].

Most reported cases of pial AVF have arisen in pediatric populations, and the clinical characteristics, angioarchitecture, and treatment strategies have been extensively described in children [5, 7]. In contrast, adult pial AVF appears uncommon, and the natural history and optimal management thus remain incompletely understood. Adult cases have been reported across a wide age range, including elderly patients, and may be congenital or acquired in nature, further complicating clinical decision-making [6, 8, 10–12].

Various treatment strategies have been reported, including microsurgical, endovascular, and hybrid approaches. The primary goal of treatment is complete interruption of the arteriovenous shunt while preserving normal arterial and venous drainage [1, 3]. Detailed angiographic evaluation is therefore essential for anatomy-based decision-making, particularly in cases with complex angioarchitecture [9, 14].

Here, we report an adult case of high-flow pial AVF with multiple venous pouches and a flow-related aneurysm. Three-dimensional rotation angiography demonstrated an extremely short arterial segment between the fistulous point and adjacent normal arterial branch, making definitive endovascular occlusion at the shunt point potentially unsafe. Therefore, a planned staged hybrid strategy was selected, consisting of initial endovascular flow reduction followed by definitive microsurgical disconnection. The clinical course and rationale for treatment are discussed with reference to the existing literature.

Case description

A 62-year-old man was incidentally found to have an intracranial vascular lesion on magnetic resonance imaging (MRI) performed during evaluations for unrelated symptoms. He had no history of intracranial hemorrhage or focal neurological deficits. Magnetic resonance angiography (MRA) demonstrated abnormal dilated cortical veins in the left sylvian fissure region, raising suspicion of an arteriovenous shunt (Fig. 1).

Fig. 1.

Initial neuroimaging findings. Axial T2-weighted magnetic resonance imaging demonstrates multiple low-intensity lesions along the left sylvian fissure (A). Magnetic resonance angiography demonstrates abnormal vascular structures in the left sylvian region (asterisk) and a flow-related aneurysm arising from the left cerebral artery (B, arrow)

Digital subtraction angiography (DSA) revealed a high-flow pial AVF supplied by the superior trunk of the left middle cerebral artery, with multiple dilated venous pouches and early venous drainage into the vein of Labbe, vein of Trolard, and frontal cortical veins (Fig. 2A, B). Three-dimensional rotational angiography clearly identified a single fistulous point (Fig. 2C). Importantly, a normal arterial branch arose in extremely close proximity to the shunt point, leaving an intervening arterial segment of approximately 7 mm. A flow-related aneurysm was also identified at the origin of anterolateral central artery arising from the left M1 segment, measuring approximately 6 mm (Fig. 2D). Given the high-flow nature of the lesion, the presence of multiple venous pouches, and the uncertain natural history, definitive treatment was planned.

Fig. 2.

Diagnostic cerebral angiography and three-dimensional rotational angiography. Anteroposterior-view (A) and lateral-view (B) left internal carotid artery angiography demonstrate a high-flow pial arteriovenous fistula supplied by the superior trunk of the left middle cerebral artery. Multiple dilated venous pouches and early venous drainage to the vein of Labbé, vein of Trolard, and frontal cortical veins are observed (A, B). Three-dimensional rotational angiography identifies the fistulous point (dashed circle). A normal arterial branch arises in close proximity to the shunt point, with an extremely short intervening segment of approximately 7 mm (arrow) (C). Three-dimensional rotational angiography demonstrates a flow-related aneurysm located at the origin of anterolateral central artery arising from the left M1 segment (D). Schematic illustration (right anterior oblique view) summarizing the angioarchitecture, highlighting the spatial relationship between the shunt point, adjacent normal arterial branch, and venous drainage pathways (E)

Endovascular therapy was performed first as the initial stage of a planned hybrid strategy to achieve flow reduction. Systemic heparinization was administered during the procedure. A 9-Fr balloon guiding catheter was positioned in the left cervical internal carotid artery, then a 3.2-Fr intermediate catheter was advanced into the left M1 segment. Adequate flow reduction was achieved with proximal balloon-guided catheter occlusion alone. A microcatheter was navigated into the venous pouch immediately distal to the fistulous point, and coil embolization was performed using a total of 12 frame- and filling type coils (total length, 570 cm). Embolization was performed carefully within the venous pouch under repeated angiographic monitoring to reduce shunt flow while avoiding excessive outflow compromise. Post-embolization angiography showed marked flow reduction with no definite early venous filling on the final runs (Fig. 3A, B). However, because embolization of the venous pouch alone was not considered sufficiently reliable for definitive cure, microsurgical disconnection was performed as planned.

Fig. 3.

Staged hybrid treatment combining endovascular embolization and microsurgical disconnection. Lateral view during transarterial embolization shows a microcatheter navigated into the venous pouch immediately distal to the fistulous point (A). Lateral-view angiogram after coil embolization of the venous pouch (asterisk) demonstrates marked flow reduction with no definite early venous filling on the final runs (B). Intraoperative photograph during direct surgery demonstrates the fistulous point (dashed circle) and an adjacent normal arterial branch (asterisk). Coils placed within the venous pouch are visible through the vessel wall, and the venous pouch and draining vein show dark reddish discoloration, indicating significant flow reduction (C). Intraoperative photograph demonstrates definitive disconnection of the shunt point using a surgical clip, with preservation of antegrade blood flow in a normal arterial branch located in close proximity to the shunt point (D)

Microsurgical disconnection of the shunt was performed the day following endovascular treatment. This surgery was performed while monitoring somatosensory evoked potential and motor evoked potential. After left frontotemporal craniotomy, the fistulous point was identified by direct inspection shortly after sylvian fissure exposure (Fig. 3C). The venous pouch and draining vein appeared dark reddish, consistent with reduced shunt flow, and the previously deployed coils were visible through the vessel wall. The fistulous connection was definitively disconnected using a surgical clip while preserving antegrade flow in the adjacent normal arterial branch, which was confirmed by intraoperative micro-Doppler ultrasonography and indocyanine green videoangiography (Fig. 3D). Temporary occlusion was not required.

Postoperative diffusion-weighted imaging showed no ischemic lesions (Fig. 4A). Follow-up MRA at 6 months demonstrated no evidence of residual shunt and regression of the flow-related aneurysm (Fig. 4B, C). The patient was discharged without any complications on postoperative day 10. At 6-month follow-up, the patient remained neurologically intact without recurrent symptoms.

Fig. 4.

Postoperative and follow-up imaging. Diffusion-weighted imaging at 5 days postoperatively shows no new ischemic lesions (A). Magnetic resonance angiography (MRA) at the same time point demonstrates complete shunt obliteration with persistence of the flow-related aneurysm (dashed circle) (B). Six-month follow-up MRA demonstrates regression of the flow-related aneurysm following shunt elimination (C)

Discussion

Pial AVF represents a distinct subtype of intracranial arteriovenous shunts, defined by direct arteriovenous connection without a nidus and characterized by high-flow hemodynamics [4, 14]. This unique angioarchitecture predisposes affected veins to marked dilation, venous pouch formation, and, in some cases, the development of flow-related aneurysms due to sustained hemodynamic stress [2, 14].

Natural history and indication for treatment

The natural history of adult pial AVFs remains poorly defined. Several reports have suggested that adult pial AVFs, particularly those with venous pouch formation, may follow a relatively benign course compared with pediatric lesions, and some acquired pial AVFs have been managed conservatively [8, 11, 14]. However, other studies have emphasized that high-flow shunting, extensive venous dilation, and associated aneurysms may increase the risk of hemorrhage or progressive neurological impairment [5, 7, 10]. In addition, a previous review suggested that the presence of a venous varix influences clinical presentation, with adult cases tending to present with hemorrhage [13]. Adult pial AVFs have also been reported in association with other intracranial arteriovenous shunts, underscoring the heterogeneity and potential complexity of these lesions [12].

Although the patient in this case was asymptomatic, the lesion demonstrated a high-flow shunt with multiple large venous pouches and an associated flow-related aneurysm. Given the uncertain natural history and the potential risk of future hemorrhagic or hemodynamic complications, definitive treatment was considered justified.

Treatment strategy and technical considerations

The fundamental principle in treating pial AVFs is complete disconnection of the arteriovenous shunt while preserving normal arterial branches and venous drainage [1, 3]. In some cases, direct occlusion of the fistulous point alone may be feasible. However, in the present case, a normal arterial branch arose approximately 7 mm proximal to the shunt point, rendering selective short-segment occlusion under flow control extremely challenging and potentially hazardous. A schematic overview of this complex angioarchitecture is provided in Fig. 2E to illustrate the spatial relationship between the shunt point, adjacent normal arterial branch, flow-related aneurysm, and venous drainage pathways.

Under these anatomical constraints, embolization of the venous pouch immediately distal to the shunt point was considered a safer means of achieving effective flow reduction. Although venous pouch embolization can reduce shunt flow, definitive cure may not be achieved if endovascular treatment alone is pursued [9, 10]. Liquid embolic material was considered hazardous because of the risk of reflux into the adjacent normal arterial branch in this high-flow lesion. Conversely, primary microsurgical disconnection without prior flow reduction was considered hazardous because of excessive bleeding from the high-flow venous pouch and difficulty identifying the shunt point. Thus, from the outset, the endovascular procedure was intended to achieve flow reduction and improve surgical safety, whereas definitive shunt interruption was planned microsurgically.

Role of hybrid treatment

Hybrid treatment combining endovascular and microsurgical approaches is increasingly recognized as a valuable strategy for complex pial AVFs [2, 13]. Endovascular techniques allow initial flow reduction, while microsurgical disconnection provides definitive shunt interruption. A report by da Silva Martins et al. emphasized that interruption of flow, rather than extensive lesion resection, is sufficient for cure and can be achieved through endovascular, microsurgical, or combined approaches [1].

In the present case, microsurgical disconnection following endovascular flow reduction allowed safe identification of the fistulous point and preservation of the adjacent normal arterial branch, resulting in complete shunt obliteration without ischemic complications.

Hemodynamic changes and flow-related aneurysm regression

Flow-related aneurysms associated with arteriovenous shunts are thought to result from chronic hemodynamic stress, and observation of aneurysm regression after shunt elimination supports a close relationship between aneurysm persistence and abnormal flow dynamics [2, 14]. In the present case, the aneurysm was located at the origin of anterolateral central artery, and regression was assessed on follow-up MRA, which demonstrated interval decrease after shunt elimination. Because postoperative DSA was not obtained, however, a very small residual shunt cannot be completely excluded.

Clinical implications

This case highlights the importance of individualized, anatomy-driven treatment planning for adult pial AVFs. When direct occlusion of the fistulous point is considered unfeasible due to adjacent normal arterial branches, staged hybrid treatment with initial endovascular flow reduction via venous pouch embolization followed by microsurgical disconnection may represent a safe and effective alternative.

Conclusion

This case demonstrates that a hybrid strategy offers a rational solution for adult pial AVF with unfavorable angioarchitecture. In the present patient, conservative management was considered unsafe because of the potential hemorrhagic risk associated with a high-flow shunt and multiple venous pouches, and selective shunt occlusion was technically hazardous due to the extremely short arterial segment between the fistulous point and an adjacent normal branch. Initial venous pouch embolization achieved sufficient flow reduction while preserving normal arterial perfusion, facilitating safe microsurgical disconnection. Regression of the flow-related aneurysm after shunt obliteration further supports a hemodynamics-driven treatment concept.

Author contributions

MK wrote the main manuscript. TM (Takeshi Miyamoto), IY, YY, NY and KS checked the manuscript. TM (Tomohiro Matsuda) prepared the figures. YK revised the manuscript. YT supervised this work. All authors approved the final manuscript.

Funding

No funding was received for conducting this work.

Data availability

Data supporting the findings of this case report are not publicly available due to privacy restrictions but are available from the corresponding author on reasonable request.

Declarations

Ethical approval

The report was prepared in accordance with the Declaration of Helsinki and its later amendments. According to our institutional policy, formal institutional review board approval was not required for a single-patient case report.

Informed consent

Written informed consent for publication of this case report and accompanying images was obtained from the patient.

Competing interests

The authors declare no competing interests.