Endoscopic Disconnection of Jugular Foramen Dural Arteriovenous Fistula Using Superselective Intra-arterial Indocyanine Green Videoangiography

Chihiro IINUMA; Takeshi KINKORI; Yuhei TAKIDO; Yusuke SATO; Mizuki NAKANO; Taketo HANYU; Shun YAMAMOTO; Ryuta SAITO

doi:10.2176/jns-nmc.2025-0383

Abstract

Jugular foramen dural arteriovenous fistulas are exceedingly rare vascular abnormalities, with only 10 cases documented so far. Their complex angioarchitecture and the risk of postoperative complications necessitate carefully planned treatment strategies. We present the case of an 82-year-old man who presented with transient dizziness. Digital subtraction angiography revealed a Cognard type V dural arteriovenous fistula at the right jugular foramen, fed by the neuromeningeal branch of the right ascending pharyngeal artery and draining into the perimedullary veins of the brainstem and spinal cord via a single right inferior petrosal vein. The lesion was successfully treated in a hybrid operating room using a multimodal approach. The procedure involved continuous neurophysiological monitoring and endoscopic disconnection of the draining vein, guided by superselective intra-arterial indocyanine green videoangiography. Complete disconnection was confirmed intraoperatively by digital subtraction angiography. To our knowledge, this is the first report of endoscopic disconnection of a jugular foramen dural arteriovenous fistula, specifically performed using intra-arterial indocyanine green videoangiography in a hybrid operating room. The combination of minimally invasive neuroendoscopy with superselective intra-arterial indocyanine green videoangiography provides both safety and effectiveness in the treatment of dural arteriovenous fistulas. This approach may be particularly advantageous for lesions in rare and anatomically complex regions such as the jugular foramen.

Introduction

Dural arteriovenous fistulas (dAVFs) are acquired vascular lesions characterized by abnormal arteriovenous shunts within the dura mater. They most often develop in the transverse-sigmoid sinus, cavernous sinus, and superior sagittal sinus; however, involvement of the jugular foramen is very rare, with only 10 cases documented to date.¹^-⁷⁾

The main treatment options for dAVFs are endovascular embolization, microsurgical disconnection, and radiosurgery.⁸^,⁹⁾ Regardless of the modality, a clear understanding of the angioarchitecture―especially the feeding arteries, fistulous point, and venous drainage―is crucial. Although transarterial embolization (TAE) is effective for many dAVFs, it carries a risk of ischemic complications affecting the cranial nerves and normal brain tissues.⁸^,⁹⁾

This report describes a rare case of a jugular foramen dAVF successfully treated in a hybrid operating room using endoscopic disconnection guided by superselective intra-arterial indocyanine green (ICG) videoangiography and confirmed with intraoperative digital subtraction angiography (DSA). It emphasizes the benefit of integrating neuroendoscopy with intra-arterial ICG videoangiography for treating dAVFs in rare and anatomically challenging locations.

Case Report

An 82-year-old man experienced transient dizziness. His medical history included hypertension and kidney stones. Neurological examination was unremarkable apart from dizziness. Brain magnetic resonance imaging showed no signs of acute stroke, but magnetic resonance angiography detected a cluster of abnormal vessels near the brainstem (Figure 1A). T2-weighted images showed a suspected flow void on the anterior aspect of the brainstem; however, no edematous signal change was observed in the brain stem or spinal cord. DSA identified a dAVF at the right jugular foramen, supplied by the neuromeningeal branch of the right ascending pharyngeal artery and draining into the perimedullary veins through the inferior petrosal vein, consistent with a Cognard type V lesion (Figure 1B-D). Considering the simple angioarchitecture with a single draining vein and the risk of lower cranial nerve palsy from TAE through the ascending pharyngeal artery, we chose to perform endoscopic disconnection of the draining vein in a hybrid operating room. Superselective intra-arterial ICG videoangiography facilitated endoscopic identification of the draining vein, while intraoperative DSA confirmed complete disconnection.

Figure 1

Preoperative imaging findings.

(A) MRA showing abnormal vessels surrounding the right jugular foramen.

(B) DSA of the right ascending pharyngeal artery showing a dAVF fed by the neuromeningeal branch (white arrow), draining into the anterior spinal vein (black arrow).

(C, D) MIP images from 3D-DSA of the right ascending pharyngeal artery. The white arrow indicates the feeder, while the black arrow indicates the draining vein, identifying the inferior petrosal vein.

3D-DSA: three-dimensional digital subtraction angiography; dAVF: dural arteriovenous fistula; DSA: digital subtraction angiography; MIP: maximum intensity projection; MRA: magnetic resonance angiography

The patient was positioned supine with the head rotated forcefully to the left and secured in a Mayfield carbon head frame (Figure 2A). Intraoperative neurophysiological monitoring, including assessments of lower cranial nerve function and auditory brainstem responses, was performed throughout the procedure. A 5-cm C-shaped skin incision was made to access the lateral suboccipital area (Figure 2B), followed by a craniotomy measuring 3.5 × 2.5 cm. Using a 4-mm rigid endoscope with ICG fluorescence capability (Karl Storz, Tuttlingen, Germany), the dura mater was opened, and cerebrospinal fluid was released to relax the cerebellum (Figure 2C). The jugular foramen and lower cranial nerves (IX, X, XI) were clearly exposed with minimal cerebellar retraction (Figure 2D). The draining vein, identified as the inferior petrosal vein, was visualized passing through the jugular foramen along the cranial nerves (Figure 2E).

Figure 2

Intraoperative photographs showing patient positioning, skin incision, and endoscopic views.

(A) Patient positioning in the hybrid operating room. (B) Skin incision indicated by the curved black line. (C) Endoscopic view showing CSF drainage. (D) Endoscopic view of the lower cranial nerves. (E) Endoscopic view showing the draining vein of the dAVF (white arrow: the inferior petrosal vein).

CSF: cerebrospinal fluid; dAVF: dural arteriovenous fistula

Although the surgical team exposed the jugular foramen, the endovascular team simultaneously established arterial access. A 4-Fr diagnostic catheter was inserted through the right femoral artery into the right common carotid artery, and a microcatheter was advanced into the neuromeningeal branch of the right ascending pharyngeal artery. Superselective DSA via the microcatheter confirmed the presence of a jugular foramen dAVF (Figure 3A). Afterward, 2 mL of diluted ICG (0.5 mg/mL) was injected through the microcatheter, allowing endoscopic visualization of the target draining vein (Figure 3B). Because cerebrospinal fluid drainage and endoscopic visualization provided a wide surgical corridor, we were able to safely utilize the Sugita clip system typically employed in conventional microsurgery. The draining vein was then clipped using a Sugita Titanium II mini clip (No. 81), and complete obliteration of the dAVF was confirmed by both DSA (Figure 3C) and superselective intra-arterial ICG videoangiography (Figure 3D). Postoperative assessment showed no lower cranial nerve deficits, and the patient's dizziness resolved. Postoperative magnetic resonance angiography confirmed the complete disappearance of the lesion. The patient was discharged 2 weeks after surgery and has experienced no recurrence over a 2-year follow-up.

Figure 3

Intraoperative images of DSA and superselective intra-arterial indocyanine green videoangiography obtained before and after fistula disconnection.

(A) Pre-disconnection DSA showing the dAVF. (B) Pre-disconnection superselective intra-arterial ICG videoangiography highlighting the draining vein (white arrow: the inferior petrosal vein). (C) Post-disconnection DSA confirming complete obliteration of flow into the anterior spinal vein.

(D) Post-disconnection superselective intra-arterial ICG videoangiography showing complete disappearance of flow in the intradural draining vein.

dAVF: dural arteriovenous fistula; DSA: digital subtraction angiography; ICG: indocyanine green;

Discussion

Jugular foramen dAVFs are extremely rare. A systematic review of the literature using the keywords "jugular foramen" and "dural arteriovenous fistula" identified only 7 articles, describing a total of 10 cases (Table 1).¹^-⁷⁾ Out of these 10 cases, 9 involved men, with ages at onset ranging from the 20s to the 80s. All patients were symptomatic. In one case of a Cognard type V fistula, the individual presented with lower limb weakness due to spinal cord venous congestion. All 10 cases underwent therapeutic intervention. Nine were treated with endovascular TAE, whereas 1 individual underwent primary open surgery. Among the patients treated with TAE, 2 subsequently required additional open surgery due to recurrence or residual lesions. Postoperative lower cranial nerve palsies occurred in 2 patients following TAE. Specifically, Case No. 1, who underwent TAE via the neuromeningeal branch of the ascending pharyngeal artery, developed severe lower cranial neuropathies postoperatively.¹⁾

Table 1

Summary of previously reported cases of jugular foramen dural arteriovenous fistulas (dAVFs)

Case No.	Age/ Sex	Symptoms	Feeder (Artery)	Drainer (Vein)	Cognard	Treatment	Complications	Outcome (mRS)	Follow-up
AphA = ascending pharyngeal artery, ICH = intracerebral hemorrhage, IJV = internal jugular vein, IPS = inferior petrosal sinus, IVH = intraventricular hemorrhage, MMA = middle meningeal artery, N/A = not available, OA = occipital artery, PAA = posterior auricular artery. PMA = posterior meningeal artery, SAH = subarachnoid hemorrhage, SOV = superior ophthalmic vein, TSS = transverse sinus, SS = sigmoid sinus
1	63/M	SAH, IVH	AphA	Right lateral medullary veins	IIb	TAE	Lower cranial neuropathies	2	3 months, no recurrence
2	52/M	Lower limb weakness	AphA/OA	Anterior/posterior spinal veins	V	TAE	None	0	3 months, no recurrence
3	70/M	Wallenberg syndrome	AphA/OA	Ascending pontomesencephalic veins	N/A	TAE	None	0	Recurrence followed by surgery
4	59/M	Tinnitus	PMA/MMA	N/A	IIa	TAE	None	0	Residual lesion followed by surgery
5	69/M	ICH(subcortical)	AphA/OA/PAA	TSS/ Labbe and Trolard	IIb	TAE	None	0	11 months, no recurrence
6	47/F	Pulsatile tinnitus	MMA/PAA/PMA	N/A	I	TAE	N/A	0	28 months, no recurrence
7	28/M	Tinnitus	MMA/PAA/PMA	N/A	I	TAE	N/A	0	15 months, no recurrence
8	81/M	ICH(subcortical)	OA/PAA/AphA	SS/Labbe	III	Open surgery	None	1	24 months, no recurrence
9	24/M	Syncope	AphA/OA	IJV	I	TAE	None	0	4 months, no recurrence
10	67/M	Cough, visual impairment	AphA	IPS-SOV	IIb	TAE	Aspiration and hoarseness	0	1 year, no recurrence
Present	82/M	Dizziness	AphA	Right inferior petrosal vein	V	Endoscopic Disconnection	None	0	2 years, no recurrence

Our case demonstrated a relatively simple angioarchitecture. The feeder was the neuromeningeal branch of the ascending pharyngeal artery, specifically the jugular branch, which drained into the perimedullary veins through a single draining vein, the inferior petrosal vein. Although TAE was considered, it carried a high risk of lower cranial nerve palsy because the neuromeningeal branch likely supplies these nerves. Therefore, microsurgical identification and disconnection of the draining vein was considered the safest option to prevent cranial nerve damage.

We performed a retrosigmoid approach using an endoscope. Endoscopic techniques have been documented for dAVFs of the anterior cranial base, falx cerebri, and spinal cord.¹⁰^-¹²⁾ Endoscopic methods provide smaller skin incisions and craniotomies, reduced brain retraction, and improved visualization of the lesion.¹⁰^-¹²⁾ Furthermore, the procedure in our case was performed in the supine position to allow for concurrent endovascular procedures (Figure 2A). In this setting, the use of a microscope results in a nearly horizontal visual axis, making it ergonomically challenging for the surgeon to maintain posture.¹³^,¹⁴⁾ In contrast, the use of an endoscope allowed the visual axis to be freely adjusted regardless of the patient's or surgeon's position. Additionally, compared with the park-bench position, the retrosigmoid approach in the supine position has been suggested to reduce the patient burden associated with positioning.¹³^,¹⁴⁾ It may also minimize the need for cerebellar retraction because the cerebellum falls away due to gravity.¹³^,¹⁴⁾ Therefore, endoscopic assistance was deemed appropriate in this case to minimize procedural invasiveness for both the patient and the surgeon.

To further ensure the safety and certainty of the procedure, we utilized the combined application of advanced intraoperative imaging techniques, including intraoperative DSA and superselective intra-arterial ICG videoangiography. This enabled precise identification of the draining vein and confirmed complete fistula disconnection. Intra-arterial ICG videoangiography offers higher resolution and better contrast than conventional intravenous ICG videoangiography, features a shorter clearance time, and can be performed alongside intraoperative DSA in a hybrid operating room.¹⁵^-¹⁷⁾ Its high-resolution, bright imaging and repeatability facilitate quick and accurate identification of feeders and drainers, as well as the direction of shunt flow, without interrupting the surgical procedure.

To our knowledge, this is the first report of endoscopic disconnection of a jugular foramen dAVF performed using superselective intra-arterial ICG videoangiography in a hybrid operating room. These techniques are especially valuable for rare and unusual lesions, allowing precise targeting of vessels and reliable achievement of treatment goals. Although performing intraoperative angiography increases procedural complexity, these methods can be safely carried out in a hybrid operating room. The integration of advanced imaging in a hybrid operating room contributes to real-time decision-making and improves the safety and reliability of treatment for complex cerebrovascular lesions.

Disclaimer

Author Ryuta Saito is one of the Editorial Board members of the journal. This Author was not involved in the peer review or decision-making process for this paper.

Acknowledgments

No financial assistance was obtained for this study.

Conflicts of Interest Disclosure

All authors have no conflict of interest.

Informed Consent

Informed consent was obtained from the present patient and his family.

Ethical Approval

The superselective intra-arterial administration of indocyanine green in this case was approved by the Institutional Review Board of Okazaki City Hospital.

References

責任著者(Corresponding author)

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